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I UNIVERSIDAD REY JUAN CARLOS FACULTAD DE CIENCIAS DE LA SALUD TESIS DOCTORAL Aspectos neurofisiológicos y biomecánicos de la región cervical sobre el dolor cérvico-craneofacial: Implicaciones del tratamiento y el diagnóstico Departamento Bioquímica, Fisiología y Genética Molecular, Farmacología y Nutrición, Anatomía y Embriología Humana e Histología Humana y Anatomía Patológica Roy La Touche Arbizu MADRID, 2014

Transcript of Tesis Roy La Touche.pdf - BURJC-Digital

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UNIVERSIDAD REY JUAN CARLOS

FACULTAD DE CIENCIAS DE LA SALUD

TESIS DOCTORAL

Aspectos neurofisiológicos y biomecánicos de la región

cervical sobre el dolor cérvico-craneofacial:

Implicaciones del tratamiento y el diagnóstico

Departamento Bioquímica, Fisiología y Genética Molecular, Farmacología y

Nutrición, Anatomía y Embriología Humana e Histología Humana y Anatomía

Patológica

Roy La Touche Arbizu

MADRID, 2014

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Facultad de Ciencias de la Salud Departamento de Bioquímica, Fisiología y Genética Molecular,

Farmacología y Nutrición, Anatomía y Embriología Humana e Histología Humana y Anatomía Patológica

III Avda. de Atenas s/n E 28922 Alcorcón Madrid España Tel. 34 91 4888855 Fax 34 91 4888831

Don Carlos Goicoechea García, Profesor Titular de Farmacología del Dpto. de

Bioquímica, Fisiología y Genética Molecular, Farmacología y Nutrición, Anatomía y

Embriología Humana e Histología Humana y Anatomía Patológica y D. Josué

Fernández Carnero, Profesor Colaborador del Dpto. de Fisioterapia, Terapia

Ocupacional, Rehabilitación y Medicina Física de la Universidad Rey Juan Carlos,

CERTIFICAN:

Que el Trabajo de investigación titulado “Aspectos neurofisiológicos y biomecánicos

de la región cervical sobre el dolor cérvico-craneofacial: Implicaciones del tratamiento

y el diagnóstico” ha sido realizado por Don. Roy La Touche Arbizu (D.N.I.: 50349803

C) bajo nuestra supervisión y dirección y cumple con los requisitos necesarios para

optar al grado de Doctor.

Y para que así conste a los efectos oportunos, firmamos el presente certificado en

Madrid, a 3 de Noviembre de 2014

Fdo. D. C. Goicoechea García Fdo. D. J. Fernández-Carnero

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A mis papás, Hilda y Melvin por su amor incondicional, esfuerzo constante y sacrificios

realizados durante toda la vida para que yo pudiera llegar hasta aquí, sin ellos este

proyecto no se hubiera podido realizar, gracias por ser mi ejemplo de vida y por las

enseñanzas en torno al esfuerzo, la perseverancia y la paciencia

A mis 5 hermanos y a todos mis sobrinos por estar ahí y comprender mi ausencia en

momentos importantes, a pesar de la distancia siempre están en mi mente y en mi

corazón

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AGRADECIMIENTOS

Este proyecto al que he dedicado tiempo y esfuerzo, no se hubiera podido

concluir sin la inestimable ayuda y colaboración de muchas personas que han aportado

sus esfuerzos desinteresadamente en las investigaciones que conforman esta tesis, a

todos ellos quisiera expresarles mi más sincera gratitud.

En mi primer lugar quisiera agradecer a mis dos directores de tesis, el Dr. Carlos

Goicoechea García y el Dr. Josué Fernández Carnero por su ayuda y orientación durante

la elaboración de este trabajo.

Al Dr. Carlos Goicochea García quisiera agradecerle especialmente la

motivación que me ofreció para realizar la tesis una vez que terminé el Máster en

Estudio y Tratamiento del Dolor que él dirigía. Tanto el Dr. Carlos Goicochea como

Dra. Mª Isabel Martín Fontelles y todo su equipo han sido referentes para mí por su

dedicación, rigurosidad, humildad y vocación en la investigación del tratamiento del

dolor. Conocerles y que hayan sido mis profesores ha sido un privilegio que me ha

ayudado a orientar mi actividad investigadora y profesional. Siempre estaré agradecido

con ellos…

Al Dr. Josué Fernández Carnero tengo muchas cosas que agradecerle y algunas

van más allá de este mismo proyecto. Durante todos los años que he tardado en finalizar

este proyecto Josué siempre ha estado detrás de cada paso que di, aportando nuevas

ideas, motivándome y dedicando toda su capacidad y conocimiento en cada una de las

investigaciones. Para mí es un premio haberle conocido y poder establecer una

verdadera relación de amistad, tengo el orgullo de decir que además de conseguir

terminar la tesis he conseguido un gran amigo. Gracias al profesor, gracias al tutor y

sobre todo gracias al amigo que has sido durante estos años.

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Haciendo una retrospectiva de lo que han sido estos años y el proceso para llegar

a conseguir este proyecto, tengo que reconocer que hay personas que han facilitado mi

adaptación a un país diferente al mío, pero el que considero un gran país del cual ya

formo parte, y en este sentido quiero agradecer especialmente al Dr. José Antonio

Martín Urrialde de la Universidad San Pablo CEU, quien me tendió una mano

desinteresadamente y me ayudó en todo momento para venir y estar en España y

conseguir finalmente este sueño. Muchas gracias por todo y más…

Hay varios profesores e investigadores de reconocido prestigio internacional que

han participado en algunas de las investigaciones de esta tesis, quiero agradecer su

colaboración al Dr. Mariano Rocabado Seaton de la Universidad Andrés Bello de Chile,

al Dr. Jeffrey Mannheimer de Columbia University de Estados Unidos de América, al

Dr. Harry Von Piekartz de la University of Applied Science Osnabruck de Alemania y

al Dr. Mark Bishop de la University of Florida de Estados Unidos de América.

Agradezco a mis compañeros y amigos del grupo de investigación Motion in

Brains de CSEU La Salle, los profesores Joaquín Pardo, Alfonso Gil, Ibai López de

Uralde y Héctor Beltrán por su colaboración en las últimas investigaciones de esta tesis.

Quiero agradecer a mi amigo el profesor Santiago Angulo Díaz-Parreño de la

Universidad San Pablo CEU por su ayuda y enseñanzas entorno al tratamiento y análisis

estadístico, su aporte a las investigaciones de esta tesis es incalculable. Muchas gracias

amigo por tu conocimiento, dedicación y amistad…

Si el título de doctor se pudiera compartir yo lo haría con mi pareja Alba París,

ella ha sido mi punto de apoyo en todo momento, ha entendido mi dedicación a la

investigación y ha estado implicada en todas los estudios que conforman esta tesis, su

aporte e implicación científica ha sido excepcional y sus palabras de motivación, su

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amor y cariño han sido suficientes para seguir adelante cuando se presentaron las

dificultades. Gracias mi vida por todo y porque cada día es único a tu lado…

A mis cinco hermanos, John, Vivian, Marco, Mayela y Dennis, y todos mis

sobrinos a los que amo mucho y añoro a diario, quiero dedicar esta tesis. Ellos han

sabido comprender mis muchas ausencias en momentos especiales en los que aunque

hubiera querido estar no me ha sido posible, sé que ellos se alegran de los éxitos que he

podido conseguir y yo me alegro de que sean mi familia del cual estoy muy orgulloso

de cada uno de ellos.

Finalmente quiero dedicar este proyecto a mis papás Hilda y Melvin que son

personas excepcionales, bondadosas, esforzadas a las cuales yo tengo una gran

admiración. Ambos con sus actos me han enseñado lecciones de vida impagables, son

pocas las palabras de gratitud que podría escribir en estas frases para expresar mi

profundo agradecimiento, todo y cada una de las cosas he podido conseguir se lo debo a

ellos.

Mi mamá lamentablemente no ha podido ver concluida esta fase profesional que

finalizo con esta tesis, a pesar de esto, en su memoria he querido darle este pequeño

homenaje que en su día le hice la promesa que lo finalizaría con el máximo esfuerzo.

Ella me apoyó en todo momento, sobre todo en los momentos difíciles y me arropó con

sus palabras de amor constantes. Gracias Mami te recuerdo todos los días y te voy a

querer siempre, esto es para ti…

A mi papá Melvin le debo muchas cosas, su vida es ejemplar y ha estado dedicada al

esfuerzo y trabajo por sus seis hijos, su vida es ejemplo de lucha diaria y en todo

momento, sea cual sea la adversidad. La honradez, la dignidad, la constancia y el

esfuerzo son principios que he podido aprender de mi papá, estos me han servido para

entender que el camino hacia un objetivo no siempre es fácil y que las metas no son lo

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más importante sino el esfuerzo que dediques a ello. Gracias Papi por todo, te quiero

mucho y esto para ti…

En toda investigación clínica los pacientes son determinantes y sin duda alguna

lo más importante, quiero agradecer a todos los pacientes que amablemente accedieron

a participar en los estudios que conforman esta tesis, espero que el conocimiento que

hemos generado sirva de alguna manera para mejorar la atención que reciban o en

motivar a otros investigadores que continúen con estas líneas. Gracias a todos los

pacientes con dolor craneofacial, muchas gracias…

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ÍNDICE GENERAL

RESUMEN…………………………………………………………………………...XV

Lista de publicaciones originales………………………………………………...…XIX

Abreviaturas………………………………………………………………..…...…..XXI

1. INTRODUCCIÓN…………………………………………………………………..1

1.1 Aspectos Básicos del Dolor…………………………………………………....2

1.1.1 Proceso de sensibilización periférica………………………………….....4

1.1.2 Proceso de sensibilización central…………………………………….....6

1.2 Dolor Musculoesquelético Crónico…………………………………………...7

1.2.1 Epidemiología…………………………………………………………....7

1.3 Dolor Cervical Crónico………………………………………………………..8

1.3.1 Epidemiología…………………………………………………………..10

1.4 Dolor Craneofacial de Origen Musculoesquelético……………….………..12

1.4.1 Trastornos craneomandibulares………………………………………...12

1.4.2 Epidemiología…………………………………………………………..14

1.4.3 Epidemiología y comorbilidad entre trastornos craneomandibulares,

cefalea y dolor de cuello………………………………………………..16

1.5 Dolor Referido de la Región Cervical hacia la Región

Craneofacial…………………………………………………………………..18

1.6 Aspectos Anatomofuncionales de la Región Craneomandibular y la Región

Craneocervical………………………………………………………………..20

1.6.1 Modelos biomecánicos de la región craneomandibular/craneocervical..21

1.6.2 Estudios in-vivo de la relación craneomandibular/craneocervical……..23

1.6.3 Influencia de la región craneocervical sobre la dinámica mandibular…23

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1.6.4 Sinergias neuromusculares cervicales y masticatorias…………….……24

1.6.5 Cinemática y concomitancia craneocervical/craneomandibular………..27

1.7 Neurofisiología del Dolor Cérvico-craneofacial…………………………….28

1.7.1 Sistema sensorial trigeminal…………………………………………....29

1.7.2 Neuroanatomía de los segmentos cervicales superiores………………..35

1.7.3 Complejo trigeminocervical…………………………………………....37

1.7.4 Sensibilización del complejo trigeminocervical………………………..39

1.8 Modulación del Dolor en el Complejo Trigeminocervical…………………41

1.8.1 Influencia de las aplicaciones terapéuticas sobre el dolor craneofacial..43

2. JUSTIFICACIÓN DEL TRABAJO REALIZADO……………………………..47

3. OBJETIVOS……………………………………………………………….……….51

4. MATERIAL Y MÉTODOS……………………………………………………….57

4.1 Participantes……………………………………………………………….….60

4.2 Variables y Pruebas de Medición…………………………………………....62

4.2.1 Medidas de auto-registro…………………………………………….64

4.2.2 Instrumentos de medición…………………………………………...66

4.3 Resumen de los Procedimientos……………………………………………..70

4.4 Análisis Estadístico…………………………………………………………...72

5. RESULTADOS…………………………………………………………………….77

5.1 Estudio I…………………………………………………………………….....78

5.2 Estudio II……………………………………………………………………...87

5.3 Estudio III………………………………………………...………….……...114

5.4 Estudio IV…………………………………………………………………....123

5.5 Estudio V………………………………………………………………….…138

5.6 Estudio VI………………………………………………………………..…..182

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5.7 Estudio VII……………………………………………………………..……192

6. DISCUSIÓN………………………………………………………………………205

6.1 Diferencias de Género en las Variables Somatosensoriales………….…...207

6.2 Postura Craneocervical, Dinámica Mandibular y

Dolor Craneocervical……………………………………………….………208

6.3 Influencia del Dolor y la Discapacidad Cervical sobre la Actividad

Sensoriomotora Trigeminal………………………………………………...209

6.4 Asociación entre la Discapacidad Cervical y la Discapacidad

Craneofacial/craneomandibular…………………………………………...213

6.5 Factores Bioconductuales Implicados en las Alteraciones Sensoomotoras

Trigeminales y la Discapacidad Craneofacial……………………………..213

6.6 Efecto del Tratamiento en la Región Cervical

sobre el Dolor Craneofacial…………………………………….…………..218

6.7 Implicaciones Científicas y Clínicas………………………………………..219

6.8 Limitaciones y Futuras Investigaciones…………………………………....222

7. CONCLUSIONES……………………………………………………………..…225

8. BIBLIOGRAFÍA………………………………………………………………....229

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RESUMEN

Introducción: El dolor craneofacial (DCF) de origen musculoesquelético, representa la

causa más común de DCF de origen no dental y puede afectar a la musculatura

masticatoria, la articulación temporomandibular y otras estructuras orofaciales. Entre

los diferentes tipos de DCF de origen musculoesquelético el más prevalente son los

denominados trastornos craneomandibulares (TCM) atribuidos o relacionados con el

dolor miofascial. Diversos estudios han descrito la presencia de comorbilidades entre la

cefalea, el dolor de cuello y los TCM, además se ha comprobado que el dolor de cuello

se asocia significativamente con los TCM y que la gravedad de estos se incrementa con

la gravedad del dolor de cuello. Evidencia científica reciente sugiere la existencia de

mecanismos neurofisiológicos trigeminocervicales implicados en las alteraciones

motoras craneomandibulares y en el DCF, a pesar de esto se necesitan más estudios

clínicos que aporten información más precisa en cuanto a la posible repercusión clínica

de características sensoriales y motoras cervicales que afectan a pacientes con DCF.

Objetivo general: Determinar la influencia biomecánica y neurofisiológica de la región

cervical sobre la discapacidad y el DCF, además se pretende identificar como

determinados factores bioconductuales influyen sobre la función craneomandibular, la

discapacidad y el DCF.

Métodos: Se realizaron 4 estudios transversales, un estudio de casos y controles, una

serie de casos y un ensayo clínico aleatorio controlado que incluyeron a pacientes con

dolor de cuello crónico mecánico, pacientes con TCM atribuido a dolor miofascial,

pacientes con dolor cérvico-craneofacial (DCCF) y pacientes con cefalea atribuida a

TCM. En tres de los estudios se realizaron comparaciones con sujetos asintomáticos.

En los estudios se evaluaron características sensoriales, motoras y factores psicológicos

implicados en el DCF mediante:

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- Medidas de auto-registro psicológicas, de dolor y discapacidad (inventario de

dolor y discapacidad craneofacial, IDD-CF; índice de dolor de cuello, IDC;

inventario de depresión BECK, BDI; escala de catastrofismo ante el dolor, ECD;

escala tampa de kinesiofobia, TSK-11; Escala visual analógica del dolor, EVA;

escala visual analógica de la fatiga, EVAF).

- Mediciones de los umbrales de dolor a la presión (UDPs) en áreas trigeminales,

cervicales y extra-trigeminales mediante algometría digital.

- Medición de la máxima apertura interincisal (MAI) libre de dolor.

- Mediciones de la postura craneocervical.

En todos los estudios se realizó un análisis descriptivo e inferencial, y en algunos casos

se utilizaron análisis complementarios a los contrastes de significación como el tamaño

del efecto o el mínimo cambio detectable para determinar la relevancia clínica de los

resultados.

Resultados:

En la comparación de los resultados de los sujetos asintomáticos con respecto a los

pacientes se presentaron los siguientes hallazgos: 1) hay diferencias estadísticamente

significativas en la postura craneocervical en los pacientes con DCCF frente a los

sujetos asintomáticos, sin embargo estas diferencias son pequeñas; 2) Se identificó que

los pacientes con dolor de cuello crónico mecánico presentan hiperalgesia mecánica en

áreas trigeminales y cervicales pero no en otras áreas anatómicas a distancia; 3) Los

pacientes con cefalea atribuida a TCM con moderada discapacidad cervical presentaron

mayores niveles de dolor y fatiga masticatoria, y menores UDPS en áreas trigeminales y

cervicales y menor MAI libre de dolor. En las comparaciones intra-grupos se encontró

una fuerte correlación entre la discapacidad cervical y la discapacidad

craneofacial/craneomandibular en pacientes con TCM atribuido a dolor miofascial. Se

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comprobó que distintas posturas craneocervicales inducidas experimentalmente

modifican la dinámica mandibular y alteran los UDPs de áreas trigeminales y

cervicales. Por otra parte, se identificó que el catastrofismo ante el dolor y la

kinesiofobia fueron predictores del estado funcional mandibular y de la discapacidad y

DCF. Finalmente, en los estudios en donde se realizó una intervención en pacientes con

TMC atribuido a dolor miofascial y en pacientes con DCCF se comprobó que el

ejercicio terapéutico en combinación de terapia manual o únicamente la aplicación de

terapia manual sobre la región cervical producen un efecto inmediato y a corto plazo en

la mejora MAI libre de dolor, una disminución de la intensidad de dolor y un aumento

de los UDPS en áreas trigeminales y cervicales.

Conclusiones:

Los resultados obtenidos en esta tesis sugieren la influencia de mecanismos

neurofisiológicos y biomecánicos de la región cervical sobre la función mandibular, las

alteraciones somatosensoriales en áreas trigeminales y sobre la discapacidad

craneofacial. Se ha demostrado que factores bioconductuales como el catastrofismo ante

el dolor y la kinesiofobia deben ser tomados en cuenta ya que son predictores de las

alteraciones funcionales craneomandibulares y el DCF. A nivel terapéutico se presentan

los primeros hallazgos sobre el efecto del tratamiento de fisioterapia específico sobre la

región cervical en la mejora de la dinámica mandibular y en la modulación del DCF.

Esta tesis aporta nuevos datos que pueden contribuir clínicamente al diagnóstico, la

valoración y el tratamiento de los TCM y el DCF.

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LISTA DE PUBLICACIONES ORIGINALES

Esta tesis está basada en las siguientes publicaciones originales que forman parte de una

línea de investigación que estudia los mecanismos neurofisiológicos, biomecánicos y

bioconductuales de la región cervical en pacientes con dolor craneofacial, las cuales se

presentan de forma completa en el apartado de resultados. En diferentes apartados del

texto se hace referencia a las publicaciones originales mediante números romanos:

I. La Touche R, París-Alemany A, von Piekartz H, Mannheimer JS,

Fernández-Carnero J, Rocabado M. The influence of cranio-cervical posture

on maximal mouth opening and pressure pain threshold in patients with

myofascial temporomandibular pain disorders. Clin J Pain. 2011

Jan;27(1):48-55

II. López-de-Uralde-Villanueva I, Beltran-Alacreu H, Paris-Alemany A,

Angulo-Díaz-Parreño S, La Touche R. Reliability, Standard Error, and

Minimal Detectable Change of Two Tests for Craniocervical Posture

Assessment in Asymptomatic Subjects and Chronic Neck/craniofacial Pain

Patients. (En revisión).

III. La Touche R, Fernández-de-Las-Peñas C, Fernández-Carnero J, Díaz-

Parreño S, Paris-Alemany A, Arendt-Nielsen L. Bilateral mechanical-pain

sensitivity over the trigeminal region in patients with chronic mechanical

neck pain. J Pain. 2010 Mar;11(3):256-63

IV. La Touche R, Pardo-Montero J, Gil-Martínez A, Paris-Alemany A, Angulo-

Díaz-Parreño S, Suárez-Falcón JC, Lara-Lara M, Fernández-Carnero J.

Craniofacial pain and disability inventory (CF-PDI): development and

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psychometric validation of a new questionnaire. Pain Physician. 2014 Jan-

Feb;17(1):95-108.

V. La Touche R, Paris-Alemany A, Gil-Martínez A, Pardo-Montero J, Angulo-

Díaz-Parreño S, Fernández-Carnero J. The Influence of Neck Disability and

Pain Catastrophizing about Trigeminal Sensory-Motor System in Patients

with Headache Attributed to Temporomandibular Disorders. (En revision)

VI. La Touche R, Fernández-de-las-Peñas C, Fernández-Carnero J, Escalante K,

Angulo-Díaz-Parreño S, Paris-Alemany A, Cleland JA. The effects of

manual therapy and exercise directed at the cervical spine on pain and

pressure pain sensitivity in patients with myofascial temporomandibular

disorders. J Oral Rehabil. 2009 Sep;36(9):644-52.

VII. La Touche R, París-Alemany A, Mannheimer JS, Angulo-Díaz-Parreño S,

Bishop MD, Lopéz-Valverde-Centeno A, von Piekartz H, Fernández-

Carnero J. Does mobilization of the upper cervical spine affect pain

sensitivity and autonomic nervous system function in patients with cervico-

craniofacial pain?: A randomized-controlled trial. Clin J Pain. 2013

Mar;29(3):205-15.

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ABREVIATURAS

ATM Articulación temporomandibular

BDI Inventario de depresión Beck

CP Conductancia de la piel

CTC Complejo trigeminocervical

DCCF Dolor cérvico-craneofacial

DCF Dolor craneofacial

DMC Dolor musculoesquelético crónico

ECD Escala de catastrofismo ante el dolor

EMG Electromiografía

END Escala numérica del dolor

ETCM Ejercicio terapéutico de control motor

EVA Escala visual analógica del dolor

EVAF Escala visual analógica de fatiga

FC Frecuencia cardíaca

FR Frecuencia respiratoria

GC Grupo control

GE Grupo experimental

HIT-6 Cuestionario de impacto de la cefalea

IDC Índice de dolor cervical

IDD-CF Inventario de dolor y discapacidad craneofacial

MAI Máxima apertura interincisal

MC Migraña crónica

ME Migraña episódica

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MIAD Modelo integrado de adaptación al dolor

NE Neuronas nociceptivas específicas

NMDA N-metil-D-aspartato

PMG Puntos gatillos miofasciales

RDA Neuronas de rango dinámico amplio

SDM Síndrome de dolor miofascial

STAI Cuestionario de ansiedad estado-rasgo

SVc Sub-núcleo trigeminal caudal

SVi Sub-núcleo trigeminal interpolar

SVo Sub-núcleo trigeminal oral

TC Temperatura cutánea.

TCM Trastornos craneomandibulares

TMO Terapia manual ortopédica

TSK-11 Escala de Tampa de Kinesiofobia

UDP Umbral de dolor a la presión

VPM Núcleo ventral posteromedial del tálamo

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INTRODUCCIÓN

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1. INTRODUCCIÓN

1.1 Aspectos Básicos del Dolor

En el modelo biomédico general, el dolor ha sido considerado como un síntoma

producido por un daño tisular, de manera que la experiencia de dolor se ha

simplificado a que, si no había daño no había dolor, si había daño tendría que

haber dolor y a mayor daño mayor dolor. El conocimiento sobre el dolor

evolucionó a partir de la compresión del procesamiento neurofisiológico del dolor

a nivel medular. Melzack y Wall (Melzack and Wall, 1965) tuvieron una

destacada labor en esta cuestión al proponer la teoría de la regulación del umbral

también conocida como la teoría de la puerta de entrada, básicamente esta teoría

explicaba el mecanismo en que el dolor estaba representado neuralmente en el asta

dorsal de la médula espinal, donde se podía facilitar o inhibir la puerta de entrada

de estímulos dolorosos hacia centros superiores. Esta teoría cobró mucha

importancia hace unas décadas a pesar de no poder explicar fisiológicamente la

situación del dolor crónico (Melzack, 1993), sin embargo lo que si permitió fue la

consideración de los factores psicológicos como parte integral del procesamiento

del dolor.

La teoría de regulación del umbral evolucionó hacia la teoría de la neuromatriz, en

esta se amplía el concepto del dolor integrando las influencias que puedan tener las

funciones cognitivas del cerebro, los sistemas de regulación del estrés y los

estímulos sensoriales (Melzack, 1999), además se expone que el dolor es una

experiencia multidimensional compuesta por la interacción de tres dimensiones:

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- Dimensión sensorial-discriminativa: identifica, evalúa, valora y modifica

todos aquellos factores relacionados con la percepción sensorial del dolor

(intensidad, localización, cualidad, factores temporales y espaciales)

- Dimensión motivacional-afectiva: comporta el aspecto emocional del

dolor. En esta dimensión estarían implicadas estructuras troncoenfálicas y

límbicas.

- Dimensión cognitivo-evaluativa: analiza e interpreta el dolor en función de

la sensación y lo que puede ocurrir.

En la actualidad el dolor se mira desde la óptica del paradigma biopsicosocial, con

lo cual los factores fisiológicos, psicológicos y sociales son tomados en cuenta, así

lo muestra la descripción de dolor definida por la Asociación Internacional para el

Estudio del Dolor:

“Es una experiencia sensorial y emocional desagradable asociada a un daño

tisular real o potencial, o descrita en términos del daño” (Merskey and Bogduk,

1994).

Existen diversas clasificaciones del dolor basadas en el origen, la evolución, los

mecanismos fisiológicos y en la estructura anatómica implicada. Con frecuencia y

desde un punto de vista clínico el dolor musculoesquéletico se clasifica en agudo y

crónico, esta clasificación toma en cuenta la evolución del dolor desde el punto de

vista del tiempo y los aspectos neurofisiológicos relacionados con la génesis y el

mantenimiento.

El dolor agudo tiene un curso temporal relacionado con los procesos de reparación

(Chapman et al., 2011) y representa una señal de alarma disparada por los

sistemas protectores del organismo (Loeser and Treede, 2008). La ineficacia en el

4

tratamiento o en la recuperación del dolor agudo puede generar que este se

mantenga en el tiempo convirtiéndose en un dolor crónico y adquiriendo las

complicaciones que este presenta.

Se define el dolor crónico como “el que persiste más allá del tiempo normal de

reparación de los tejidos, que se supone en el dolor no maligno es de 3 meses…,

pero para fines de investigación se prefiere elegir un tiempo de 6 meses” (Merskey

y Bogduk, 1994). El tiempo (días, meses…) en el que se tiene dolor es el

parámetro más utilizado para definir la diferencia entre el dolor agudo y el dolor

crónico, esta clasificación tiene sus limitaciones teniendo en cuenta que el dolor

crónico presenta una naturaleza multifactorial (Turk and Rudy, 1988). En este

sentido Von Korff y Dunn (Von Korff and Dunn, 2008), han comprobado que un

modelo de clasificación de los pacientes basado en los niveles de discapacidad,

calidad vida, intensidad de dolor, síntomas depresivos y toma de medicamentos

tiene mayor valor predictivo que solo la clasificación basada en el tiempo de dolor

(Von Korff and Dunn, 2008).

1.1.1 Proceso de sensibilización periférica

Desde el punto de vista de la neurofisiología, el dolor agudo es considerado como

una respuesta sensorial de la activación del sistema nociceptivo a consecuencia de

un daño tisular que produce una respuesta inflamatoria que sensibiliza los

nociceptores periféricos (Loeser and Treede, 2008; Woolf, 2004); la

sensibilización se produce a consecuencia de la acción de mediadores químicos de

origen inflamatorio que se liberan en el área del daño tisular, tales como la

sustancia P y el péptido relacionado con el gen de la calcitonina que se liberan en

la periferia y se unen a otros mediadores como neutrófilos, mastocitos y basófilos;

esta unión produce a su vez la liberación de sustancias pro-inflamatorias

5

(citoquinas, bradiquinina, histamina) que favorecen la síntesis de la enzima

ciclooxigenasa-2 (COX-2) que conduce a la producción y secreción

de prostaglandinas (Woolf, 2004). Este mediador actúa como un sensibilizador

que altera la sensibilidad al dolor por el incremento de la capacidad de respuesta

de los nociceptores periféricos (Woolf, 2004).

La sensibilización periférica se define como un proceso en donde hay una

reducción del umbral y una amplificación de la capacidad de respuesta de los

nociceptores, que se produce cuando las terminales periféricas de las neuronas

sensoriales primarias de alto umbral están expuestos a mediadores de inflamación

en el tejido dañado (Chen et al., 1999; Guenther et al., 1999; Hucho and Levine,

2007).

Es un hecho más que contrastado que la sensibilización periférica contribuye a la

sensibilización del sistema nociceptivo y provoca dolor e hipersensibilidad en las

áreas en donde se produce inflamación (hiperalgesia primaria) (Latremoliere and

Woolf, 2009), este fenómeno representa una acción protectora del organismo con

el fin de evitar el uso de estructuras dañadas (Nijs et al., 2010). A la sensación

dolorosa que se extiende más allá del área de la lesión y abarca zonas no afectadas

por la lesión original, se la conoce como hiperalgesia secundaria, pero este no es

un proceso únicamente de carácter periférico, lleva implícitos mecanismos

centrales (Latremoliere and Woolf, 2009; Woolf, 2011).

El proceso de sensibilización periférica se asocia a una alteración en la

sensibilidad térmica, pero no se observa una alteración de la sensibilización

mecánica que parece ser una característica importante de la sensibilización central

(Latremoliere and Woolf, 2009; Woolf, 2004).

6

1.1.2 Proceso de sensibilización central

El dolor crónico está asociado a cambios neuroplásticos sobre mecanismos

periféricos y centrales, estos cambios pueden mantener la percepción de dolor a

pesar de la ausencia de un daño potencial (Woolf and Costigan, 1999); por otra

parte, la característica defensiva propia del dolor agudo no está presente en esta

condición.

Un estímulo doloroso mantenido crónicamente produce una excitación excesiva de

las neuronas medulares y supramedulares, la producción de este proceso hace que

aparezca el mecanismo de la sensibilización central (Latremoliere and Woolf,

2009). La sensibilización central se manifiesta como una reducción prolongada del

umbral y un aumento en la sensibilidad y extensión de las áreas receptoras del asta

dorsal de la medula espinal (Ji et al., 2003), además se ha observado una

ineficiencia en los mecanismos inhibitorios encargados de la modulación del dolor

(Meeus et al., 2008).

Desde el punto de vista clínico la sensibilización central puede provocar que la

percepción de un estímulo no doloroso se convierta en un estímulo doloroso

(alodinia), por otra parte los estímulos dolorosos serían percibidos como una

sensación de dolor desproporcionado (hiperalgesia). Se ha sugerido que la

sensibilización central puede ser el mecanismo por el cual los factores

psicológicos y somáticos se correlacionan desde el punto de vista neurobiológico.

Además, se plantea que el distrés psicológico resultante del proceso de dolor

crónico contribuye al mecanismo de sensibilización central, lo que produce una

amplificación del dolor (Curatolo et al., 2006).

7

1.2 Dolor Musculoesquelético Crónico

Se considera dolor musculoesquelético crónico (DMC) cuando el dolor se

mantiene entre 3 y 6 meses (Walsh et al., 2008). El DMC se producen alteraciones

neurales, somáticas, cognitivas y conductuales (Walsh et al., 2008), que generan

una disminución de la calidad de vida del paciente y de su desempeño laboral.

El dolor musculoesquelético es descrito usualmente por los pacientes como una

sensación firme y de presión, de características difusas y que a menudo se

acompaña de hiperalgesia muscular profunda o alodinia (Graven-Nielsen, 2006),

este tipo de dolor puede manifestarse de forma localizada, regional y generalizado

(Graven-Nielsen and Arendt-Nielsen, 2010). El síndrome de dolor miofascial

(SDM), es un ejemplo de una condición de dolor regional muscular que se

caracteriza por la presencia de bandas tensas y dolor referido característico

causado por puntos gatillo miofasciales (PGM) (Simons, 1996).

La transición de dolor agudo musculoesquelético localizado a dolor crónico

generalizado está probablemente relacionada con la progresión de la

sensibilización periférica y central (Graven-Nielsen and Arendt-Nielsen, 2010). La

neurofisiología del DMC podría explicarse a través del proceso de sensibilización

central (Graven-Nielsen and Arendt-Nielsen, 2010).

1.2.1 Epidemiología

El dolor crónico es muy prevalente en la población general (Elliott et al., 1999) y

genera impacto negativo sobre la calidad de vida, el desempeño laboral y la

interacción psicosocial del paciente (Becker et al., 1997; Breivik et al., 2006).

8

El DMC se ha convertido en el principal motivo de consulta de dolor crónico en

atención primaria en la geografía española (Batlle-Gualda et al., 1998; Català et

al., 2002).

En una reciente revisión se ha descrito que la prevalencia del DMC se encuentra

entre el 13.5% y 47% de la población general y la del DMC generalizado varía

entre 11.4% y 24% (Cimmino et al., 2011).

En relación al SDM se ha sugerido que es el tipo de dolor más prevalente de entre

los de origen musculoesquelético (Simons, 1996), pero no hay datos precisos en

cuanto a la prevalencia de este en relación a la población general; a pesar de esto

en la actualidad clínica se tiene muy en cuenta al SDM, aún más conociendo que

en muchas investigaciones se ha demostrado que los PG son muy prevalentes en

diversos trastornos musculoesqueléticos como la cefalea tensional crónica

(Couppé et al., 2007), el dolor orofacial (Fernández-de-Las-Peñas et al., 2010), los

dolores relacionados con el raquis (Chen and Nizar, 2011), el dolor de hombro

(Bron et al., 2011) o la epicondilalgia lateral (Fernández-Carnero et al., 2007).

1.3 Dolor Cervical Crónico

La Neck Pain Task Force define el dolor cervical como un evento episódico a lo largo

de la vida que presenta una recuperación variable entre los diferentes episodios

(Guzman et al., 2009).

El dolor cervical frecuentemente denominado como no específico, de tejidos blandos o

dolor cervical mecánico se puede definir como aquel localizado en el territorio situado

entre la línea nucal superior y la línea de la espina de la escápula, en la parte posterior

del cuerpo, y en la parte anterior por encima del borde superior de la clavícula y el

esternón dejando fuera el contorno facial; con o sin irradiación a la cabeza, tronco y

9

miembros superiores (Guzman et al., 2009). Los signos de irradiación del dolor son

contemplados por esta definición, en relación con esto Bogduk (Bogduk, 2003) sugiere

que los signos de irradiación hacia la extremidad superior no deben asumirse como

parte del dolor cervical ya que estos son más propios del dolor cervical radicular y

fisiopatológicamente estas dos condiciones son muy distintas, además añade que la

confusión de estas dos entidades clínicas puede llevar a errores en el diagnóstico y

planteamientos de investigación y tratamiento poco adecuados (Bogduk, 2003).

Más acorde con la sugerencia de Bogduk (Bogduk, 2003) es la definición propuesta por

Merskey y Bogduk (Merskey and Bogduk, 1994), en esta, el dolor cervical se define

como el dolor que surge en una región limitada superiormente por la línea nucal

superior, lateralmente por los márgenes laterales del cuello, e inferiormente por una

línea imaginaria transversal a través de la apófisis espinosa T1.

El dolor cervical puede considerarse como un síntoma muy frecuente en la mayoría de

trastornos que afectan al cuadrante superior, aunque rara vez es síntoma de la presencia

de tumor, infección u otra afección grave (Bogduk, 2003). El dolor cervical puede

coexistir junto a otros trastornos musculoesqueléticos (Harris et al., 2006). Y puede

estar provocado o asociado a una patología local o una enfermedad sistémica tales como

lesiones de la piel, alteraciones de la laringe, tumores, infección, fracturas y

dislocaciones, traumatismos, mielopatías, artritis reumatoide u otras enfermedades

reumáticas (Haldeman et al., 2008).

El dolor cervical tiene una etiología multifactorial, con factores de riesgo no

modificables como la edad y el sexo (Hogg-Johnson et al., 2009). En estudios

realizados en población general relacionados con la edad, se ha observado que los

sujetos más jóvenes tienen mejor pronóstico de recuperación de la discapacidad cervical

(Hogg-Johnson et al., 2009). También se ha demostrado que otros trastornos

10

musculoesqueléticos y problemas psicológicos pueden considerarse factores de riesgo

del dolor cervical, y frecuentemente se asocian a él (Carroll et al., 2008; Hogg-Johnson

et al., 2009).

Entre los factores psicológicos asociados a un mal pronóstico de dolor cervical que se

han descrito son los estados de angustia, sufrimiento, enfado o frustración en respuesta

al dolor (Hill et al., 2004), en contraposición a esto se ha observado que el positivismo

y la alta autoestima estuvieron asociados con un mejor pronóstico (Haldeman et al.,

2008).

Existe mucha literatura que avala que los cambios degenerativos cervicales van

unidos a la presencia de dolor cervical persistente e incapacitante, pero no hay evidencia

de que los cambios degenerativos obtenidos con RMN cervical se correlacionen con

síntomas de dolor cervical. Tampoco hay evidencia suficiente para demostrar que la

degeneración de disco sea un factor de riesgo para tener dolor de cuello (Nordin et al.,

2008).

Un factor positivo es el hecho de practicar ejercicio, se ha visto que si se practicaba

ejercicio físico, ante la presencia de un dolor de cuello, éste tendrá mejor pronóstico que

si el paciente es sedentario (Hogg-Johnson et al., 2009), e incluso otro estudio sugiere

que el ejercicio puede tener un efecto protector contra el dolor cervical (van den Heuvel

et al., 2005).

Entre los factores predictivos relacionados con el dolor crónico se han encontrado, el

acoso laboral, trastornos de sueño, el índice de masa corporal en la mujeres, el trabajo

relacionado con el agotamiento emocional en los hombres, presentar dolor cervical

agudo con anterioridad y dolor crónico lumbar (Kääriä et al., 2012).

1.3.1 Epidemiología

El dolor de cuello es una de las condiciones de dolor más frecuente, la prevalencia de

11

dolor de cuello en la población general se ha estimado entre 10% y 15%, siendo más

común en mujeres que en hombres (Borghouts et al., 1999). En un reciente estudio de la

prevalencia de dolor en el cuello en la población española se ha estimado que indica un

19.5% anual entre los adultos españoles (Fernández-de-las-Peñas et al., 2011).

Un 70% aproximadamente de las personas, puede que experimenten un dolor cervical

en algún momento de sus vidas (Côté et al., 1998). En la población que sufre dolor

cervical se ha encontrado que a la hora de cualificarlo se representa en forma de

pirámide, en la que la base es conformada por un gran número de casos de dolor leve,

por encima pocos casos que consultan por su dolor y en la punta solo unos pocos casos

de dolor invalidante (Côté et al., 1998; Hogg-Johnson et al., 2009). Cote y cols.

encontraron que el 39.4 % de los individuos han tenido dolor cervical en los últimos 6

meses (Côté et al., 1998).

La literatura sugiere que entre el 50-80% de la población general que ha experimentado

dolor cervical, lo volverán a sufrir entre 1 -5 años más tarde y la mayor parte no se

recuperan totalmente del problema (Carroll et al., 2008). En general en la literatura se

dividen los grupos de edad en dos grandes grupos: jóvenes y mayores, siendo los de

peor pronóstico estos últimos. Hill y cols. (Hill et al., 2004) realizaron un estudio en el

que los sujetos se dividen en tres grupos de edades; se observó que en el grupo de edad

de entre 45-59 años, existe una tendencia 4 veces mayor a que el dolor cervical se

cronifique, recurra o sea continuo comparado con edades menores y mayores.

Más de 1/3 de los pacientes desarrollan síntomas crónicos que durarán más de 6 meses

(Côté et al., 2008). Entre un 15-32% de los individuos continúan experimentando

síntomas 5 años después del primer episodio de dolor de cuello (Enthoven et al., 2004;

Pernold et al., 2005). Después de 10 años, aproximadamente un 32% de los que

experimentan un primer episodio continuarán presentando síntomas moderados o

12

graves y un 79% mejoran del dolor pero no desaparece completamente (Gore et al.,

1987).

1.4 Dolor Craneofacial de Origen Musculoesquelético

El dolor craneofacial (DCF) es una denominación general que es utilizada para describir

la presencia de dolor en la cara, cabeza y estructuras asociadas, puede estar originado

por una variedad de condiciones, estructuras o etiologías (Armijo Olivo et al., 2006;

Kapur et al., 2003). El DCF se puede clasificar en neuropático, neurovascular y

musculoesquéletico (Benoliel et al., 2011). El DCF de origen musculoesquelético,

representa la causa más común de DCF de origen no dental y puede afectar la

musculatura masticatoria, la articulación temporomandibular (ATM) y estructuras

orofaciales (Okeson and de Leeuw, 2011). Los signos y síntomas más prevalentes que

se han observado en los pacientes con DCF son: dolor al abrir la boca, dolor a la

palpación muscular y dolor articular (Macfarlane et al., 2001), y por orden de

porcentaje, las áreas de expansión del dolor que se han descrito como más prevalentes

son: alrededor de los ojos, alrededor de la región temporal, en la zona anterior a la oreja

y en la ATM y alrededores de esta (Macfarlane, Blinkhorn, Davies, Kincey, et al.,

2002). Los factores psicológicos están muy presentes en el DCF y se han observado

múltiples comorbilidades con otras dolencias y patologías (Macfarlane et al., 2001).

El DCF de origen musculoesquelético según la Asociación Internacional para el Estudio

del Dolor se clasifica en cefalea tensional crónica, trastornos craneomandibulares

(TCM) dolorosos, TCM causados por artritis o artrosis, distonías y discinesias faciales y

traumatismos craneofaciales (Merskey and Bogduk, 1994).

1.4.1 Trastornos craneomandibulares

El término TCM se refiere a una serie de signos y síntomas que afectan a la musculatura

masticatoria, la ATM y estructuras asociadas o ambas (Okeson and de Leeuw, 2011;

13

Okeson, 1997), se considera un proceso patológico multifactorial causado posiblemente

por hiperactividad muscular o por parafunciones, lesiones traumáticas, influencias

hormonales y cambios a nivel articular (Liu and Steinkeler, 2013). Estos trastornos se

caracterizan por: (a) dolor orofacial y/o en la ATM o en los músculos masticatorios; (b)

alteraciones en el movimiento mandibular y/o limitación del rango de movimiento

mandibular; y (c) presencia de ruidos articulares durante la función mandibular (Liu

and Steinkeler, 2013; Okeson and de Leeuw, 2011).

Los factores psicosociales tienen un papel relevante en los TCM, en un reciente estudio

cohorte se identificó que el estrés, la afectividad negativa y las estrategias de

afrontamiento ante el dolor presentan una repercusión importante sobre los TMD

(Fillingim et al., 2011), por otra parte, Kindler y cols. (Kindler et al., 2012)

encontraron que los síntomas depresivos están más presentes en pacientes con TCM

articulares mientras la ansiedad estuvo más asociado con TCM de origen muscular.

Características psicológicas incluyendo la somatización, depresión y la ansiedad

relacionados con el género parecen tener un impacto significativo en la prevalencia de

TCM (Licini et al., n.d.). Evidencia reciente describe que las pacientes femeninas con

TCM presentan mayor percepción de intensidad del dolor y sensibilidad muscular a la

palpación que pacientes masculinos (Schmid-Schwap et al., 2013).

Existen diversos criterios diagnósticos para clasificar los TCM (Benoliel et al., 2011;

Schiffman et al., 2010), sin embargo la clasificación más utilizada en la actualidad son

los Criterios diagnósticos de investigación para TCM (en inglés, Research Diagnostic

Criteria for Temporomandibular Disorders; RDC/TMD) (Dworkin and LeResche, 1992;

Schiffman et al., 2010), estos criterios presentan una fiabilidad y validez contrastada

englobado en un protocolo sistematizado de valoración, diagnóstico y clasificación de

los subtipos más comunes de TCM (Look et al., 2010). Los Criterios diagnósticos de

14

investigación para TCM establecen la clasificación en dos grandes secciones definidos

en dos ejes: Eje I: Diagnóstico del dolor; y el Eje II Estatus psicosocial (Schiffman et

al., 2014). Es importante destacar que estos criterios han sido recientemente revisados y

el Eje I de diagnóstico ha sido dividido en dos grandes grupos de trastornos, TCM

relacionados con dolor y trastornos del disco y patología degenerativa de la ATM

(Tabla 1) (Schiffman et al., 2014).

Tabla 1. Clasificación diagnóstica de los trastornos craneomandibulares (Schiffman et

al., 2014).

Trastornos craneomandibulares

relacionados con dolor

Trastornos del disco y patología

degenerativa de la articulación

temporomandibular.

Mialgia Luxación del disco con reducción

Mialgia local Luxación del disco con reducción y con

bloqueos intermitentes

Dolor miofascial Luxación del disco sin reducción y con

limitación de la apertura

Dolor miofascial referido Luxación del disco sin reducción y sin

limitación de la apertura

Artralgia Trastornos degenerativos

Cefalea atribuida a trastornos

craneomandibulares

Subluxación

1.4.2 Epidemiología

El DCF es una dolencia muy prevalente en la población general en torno a un 17-26%

de los cuales el 11,7% llega a convertirse en condición crónica (Macfarlane, Blinkhorn,

15

Davies, Ryan, et al., 2002). En relación al sexo es más prevalente en mujeres y el rango

de edad donde se presenta con mayor frecuencia es entre los 18-25 años y los 56-65

años (Macfarlane, Blinkhorn, Davies, Kincey, et al., 2002). La presencia de dolor en la

región temporomandibular se produce en aproximadamente un 10% de la población

adulta (LeResche, 1997). Las mujeres presentan en general más signos y síntomas de

TCM y además estos son frecuentes y más severos que en los hombres (Adèrn et al.,

2014; Carlsson, 1999; LeResche, 1997), por otra parte las mujeres tienen menos

probabilidades de recuperarse de sus síntomas (Wänman, 1996) y son más propensas a

buscar tratamiento (Carlsson, 1999). En un reciente estudio se encontró que el 26.8% de

mujeres con TCM evaluadas se clasificaron como trastornos moderados frente a un

9.3% de TCM graves (Campos et al., 2014). En pacientes ancianos se encontró mayor

prevalencia de TCM en mujeres y los trastornos se clasificaron en un 43% leves, 13%

moderados y 4.5% en graves (Camacho et al., 2014).

De Kanter y cols. en un meta-análisis de 51 estudios epidemiológicos encontraron una

prevalencia del 30% de síntomas de TCM (De Kanter et al., 1993), en otro estudio se

observó el 10% de la población estudiada presentaba TCM y de estos el 50% presentó

más de un signo de TCM (Gesch et al., 2004). Se ha observado una mayor prevalencia

de signos y síntomas en edades intermedias (Carlsson, 1999; Yekkalam and Wänman,

2014), Yekkalan y Wanman en un estudio reciente encontraron mayor prevalencia de

signos entre los sujetos de 35 y 50 años (Yekkalam and Wänman, 2014) y la evidencia

muestra una prevalencia menor en edades adultas (Carlsson, 1999; Matsuka et al., 1996;

Yekkalam and Wänman, 2014). Manfredini y cols. en un estudio epidemiológico con

pacientes con TCM encontraron que el 56.4% de los pacientes presentaron un

diagnóstico de dolor muscular, el 42% de luxación del disco y 57.5% otros trastornos

articulares (Manfredini et al., 2012).

16

En cuanto a la incidencia, Kamisaka y cols. realizaron un estudio longitudinal en un

espacio temporal de 4 años y encontraron una incidencia del 6% para el dolor en la

ATM y un 12.9% para ruidos articulares en la ATM, en esta misma investigación se

encontró en los sujetos menores de 40 años un mayor riesgo de presentar ruidos en

ATM y las mujeres presentaban un aumento en el riesgo de perpetuación de dolor en la

ATM (Kamisaka et al., 2000).

1.4.3 Epidemiología y comorbilidad entre trastornos craneomandibulares, cefalea

y dolor de cuello

Los TCM, las cefaleas y el dolor de cuello son trastornos muy relacionados (Sipilä et

al., 2002; Storm and Wänman, 2006; Wiesinger et al., 2007). Varios estudios han

informado que los signos y síntomas se superponen entre los pacientes con TCM,

cefaleas y dolor en el cuello respectivamente (Anderson et al., 2011; Rantala et al.,

2003), se ha demostrado que el dolor de cuello se asocia significativamente con los

TCM y que la gravedad de éstos se incrementa con la gravedad del dolor de cuello

(Ciancaglini et al., 1999; Nilsson et al., 2013; Wiesinger et al., 2009), adicionalmente,

se ha comprobado que los factores psicosociales a su vez están relacionados con la

presencia de cefalea, dolor de cuello y dolor orofacial (Rantala et al., 2003). Stuginski-

Barbosa investigaron recientemente los signos de TCM en pacientes con migraña

crónica (MC) y episódica (ME), en esta investigación se identificó que el 73% de los

pacientes con MC presentaron dolor a la palpación en la musculatura masticatoria, 63%

presentaron dolor a la palpación articular y 64% presentaron dolor a la palpación del

cuello (Stuginski-Barbosa et al., 2010), otras estudios similares, pero realizados en

pacientes adolecentes con cefalea han observado una alta comorbilidad con los TCM

dolorosos, además se encontró una asociación significativa con el dolor de cuello

(Nilsson et al., 2013), además en pacientes adolescentes con TCM, encontraron que los

17

pacientes que presentaban alteraciones musculares y alteraciones musculares y

articulares tuvieron mayores niveles de dolor mandibular y orofacial, cefalea, dolor de

cuello y dificultad para comer alimentos blandos (Karibe et al., 2010).

Se ha sugerido que los TCM, las cefaleas y el dolor de cuello pueden tener una base

fisiopatológica similar (Ashina et al., 2006; Marklund et al., 2010; Svensson, 2007), por

otra parte se ha identificado que la cefalea podría ser un factor de riesgo de sufrir dolor

de cuello (Leclerc et al., 1999).

Rantala y cols. describió que de entre 1339 sujetos evaluados la prevalencia de signos

relacionados con la ATM fue del 10%, el dolor orofacial fue del 7%, la cefalea del 15%

y el dolor de cuello el 39% (Rantala et al., 2003), por otra parte, Plesh y cols. mostró

que el 53% de los pacientes con TCM que presentaron dolor de cabeza severo, el 54%

tenía dolor de cuello (Plesh et al., 2011). Un estudio realizado con 487 mujeres Sami

encontró que un 17% de estas presentó dolor en la regiones mandibular y orofacial que

además lo asociaban a una limitación de su calidad de vida, y en este mismo estudio se

describe que la duración del dolor en la región mandibular, las molestias al realizar la

apertura, el dolor de cuello y un nivel educativo bajo estaban relacionados cuando los

síntomas de TCM influían en la vida cotidiana (Mienna and Wanman, 2012), en

relación con esto dato, Weber y cols. encontraron que el 88,24% de los pacientes con

TCM presentaron a su vez dolor cervical, en esta investigación se sugiere que esta

situación está generada principalmente por factores neurofisiológicos y no por factores

biomecánicos como la postura (Weber et al., 2012).

La prevalencia del latigazo cervical en pacientes con TCM ha sido estudiada en una

revisión sistemática reciente (Häggman-Henrikson et al., 2014), en esta se describe que

la prevalencia del latigazo cervical en pacientes con TCM varía entre 8,4% a un 70%,

este resultado se comparó con la población general sin TCM en donde la prevalencia de

18

latigazo cervical se encuentra entre 1,7% y 13%, además en esta revisión se señala que

los pacientes con TCM con antecedentes de haber sufrido un latigazo cervical presentan

más signos de alteración de la ATM como limitación de la apertura bucal, más dolor

articular, cefalea y síntomas de estrés. Los autores de esta revisión sugieren que el

latigazo cervical puede ser un iniciador y/o un factor agravante, así como una condición

comórbida con los TCM (Häggman-Henrikson et al., 2014)

1.5 Dolor Referido de la Región Cervical hacia la Región Craneofacial

Diversas estructuras de la región cervical pueden provocar dolor referido hacia la región

craneofacial, la literatura científica describe que las articulaciones cervicales, los

ligamentos y los músculos son estructuras relevantes a tener en cuenta en la

identificación de los patrones del dolor que pueden afectar al cráneo, la región

craneomandibular y la región orofacial. Son muchos los estudios que demuestran que

los PGM del trapecio, el esplenio, el esternocleidomastoideo y los músculos sub-

occipitales producen dolor referido hacia la región craneofacial en pacientes con TCM y

cefaleas (Alonso-Blanco et al., 2012; Fernández-de-Las-Peñas et al., 2006, 2010;

Fricton et al., 1985; Wright, 2000). Muchos de estos patrones de dolor referido

evocados por PGM fueron descritos por Simons y cols. (Simons et al., 1999) (Figura

1).

19

Figura 1. Representación modificada de los patrones de dolor referido hacia la región craneofacial provocado por

PGM de músculos de la región cervical.

A nivel de las estructuras articulares de la región cervical, la investigación relacionada

con la infiltración de sustancias algógenas y estudios relacionados con el diagnóstico

estructural han identificado patrones o mapas de dolor referido hacia la región

craneofacial, específicamente Dreyfuss y cols. comprobaron en sujetos sanos que la

infiltración de sustancias algógenas sobre la articulación atlanto-occipital y la

articulación atlanto-axial lateral provocaban patrones de dolor referido sobre la región

cervical superior y la cabeza (Dreyfuss et al., 1994), también Dwyer y cols. con un

procedimiento similar en sujetos sanos identificaron que las articulaciones

zigoapofisarias C2-C3 provocan patrones de dolor referido hacia la región cervical y la

cabeza (Dwyer et al., 1990), estos patrones fueron confirmados con gran similitud en

pacientes (Aprill et al., 1990; Cooper et al., 2007). Se ha sugerido que el patrón de dolor

de las articulaciones zigoapofisarias C3-C4 ocasionalmente puede estar relacionado con

20

la cefalea cevicogénica (Cooper et al., 2007), sin embargo en el caso del disco

intervertebral C2-C3 sí se ha identificado como una fuente importante de dolor referido

hacia la cabeza en pacientes con cefalea cervicogénica (Schofferman et al., 2002)

(Figura 2).

Figura 2. Representación, según la evidencia científica de los patrones de dolor referido de estructuras articulares

cervicales hacia áreas craneocervicales (Aprill et al., 1990; Cooper et al., 2007; Dreyfuss et al., 1994; Dwyer et al.,

1990).

Destacar como hallazgo científico reciente, que Watson y Drummond encontraron

patrones de dolor referido hacia la cabeza muy similares al valorar la articulación

atlanto-occipital y las articulaciones zigoapofisarias C2-C3 en pacientes con migraña y

cefalea tensional (Watson and Drummond, 2012).

1.6 Aspectos Anatomofuncionales de la Región Craneomandibular y la Región

Craneocervical

La asociación entre la región craneomandibular y la región craneocervical ha sido

estudiada en las últimas décadas desde diversos paradigmas, incluyendo enfoques

anatómicos, biomecánicos, neurofisiológicos, y patofisiológicos (Armijo Olivo et al.,

2006), en este apartado se pretende hacer una descripción detallada de la evidencia

21

disponible relacionada con las posibles relaciones entre estas regiones tomando en

cuenta los enfoques anatómicos y biomecánicos desde la función normal.

1.6.1 Modelos biomecánicos de la relación cranemandibular/craneocervical

Uno de los primeros planteamientos teóricos de la dinámica craneomandibular

/craneocervical fue el desarrollado por Brodie (Brodie, 1950), este autor desarrolló un

esquema gráfico (Figura 3), que explicaba cómo la postura erguida de la cabeza se

mantenía mediante el equilibrio neuromuscular de los músculos anteriores y posteriores

de la región craneocervical y cervical. Otro postulado importante que proponía este

modelo es que una actividad mandibular como el apretar isométricamente tendría que

estar equilibrada por la activación de los músculos cervicales cuando la cabeza está

erguida (Brodie, 1950; Thompson and Brodie, 1942), Rocabado desarrolló un modelo

similar al anterior, en este se señala que la estabilidad craneomandibular se mantiene

entre el equilibrio de las fuerzas anteriores (músculos masticatorios, músculos supra e

infrahiodeos, y los músculos cervicales anteriores) y posteriores (músculos cervicales

posteriores), ambos grupos musculares junto a otras estructuras de la región

craneomandibular trabajan de forma sinérgica en una cadena funcional; por otra parte

este autor sugiere que la posición de la mandíbula y del hueso hiodes depende de la

curvatura cervical (Rocabado, 1983).

22

Figura 3. Esta figura representa el esquema diseñado por Brodie, para explicar el equilibrio mecánica neuromuscular

entre las regiones craneocervical y craneomandibular (Brodie, 1950; Thompson and Brodie, 1942).

Resultados de estudios basados en modelos matemáticos apoyan en gran medida las

tesis teóricas anteriormente descritas (Gillies et al., 1998; Suzuki et al., 2003), un

ejemplo de esto es el estudio de Suzuki y cols. en este se generó un sistema mecánico de

análisis dinámico del sistema estomatognático en condiciones de normalidad, se

observó como resultado principal que la actividad muscular de la región cervical influye

sobre la actividad mecánica de la mandíbula, además sugieren que los músculos

cervicales coordinan y resisten los cambios en la postura de la cabeza durante los

movimientos mandibulares (Suzuki et al., 2003). Otro de los modelos biomecánicos

relacionados con la dinámica mandibular, señala que el movimiento de extensión

craneocervical facilita la apertura mandibular y sugieren que esta situación se da para

lograr una mejor activación de los músculos que realizan la apertura y para generar una

posición más favorable para el movimiento (Koolstra and van Eijden, 2004).

23

1.6.2 Estudios in-vivo de la relación craneomandibular/craneocervical

La mayoría de estudios in-vivo en torno a las hipótesis de la relación

craneomandibular/craneocervical se han realizado con electromiografía (EMG), análisis

cinemático y estudios radiológicos; estas investigaciones se han diseñado con el

objetivo de comprobar la influencia mutua de ambas regiones en la dinámica articular

mandibular, en la estabilidad postural y en los aspectos funcionales más generales en los

que participa la ATM y las estructuras asociadas, como por ejemplo la deglución y la

masticación.

1.6.3 Influencia de la región craneocervical sobre la dinámica mandibular

En cuanto a la dinámica mandibular, Visscher y cols. demostraron pequeñas

variaciones en la posición del cóndilo mandibular según la postura craneocervical, sus

hallazgos mostraron que la distancia intra-articular en la ATM en el movimiento de

cierre es menor con retracción craneocervical y mayor con protrusión craneocervical

(Visscher et al., 2000), en relación con esto, Omure y cols. observaron que al inducir

experimentalmente la posición de protrusión craneocervical, el cóndilo mandibular se

posteriorizaba en comparación a la posición neutra (Ohmure et al., 2008), estos

hallazgos confirmarían las observaciones de Solow y Tallegren que en 1976 ya

describieron que el movimiento de extensión craneocervical se asocia a una retrusión

mandibular (Solow and Tallgren, 1976). Otro de los aspectos importantes que se han

investigado sobre la dinámica de la ATM es que la apertura mandibular se ve

directamente influenciada por la posición craneocervical, observándose un aumento de

la apertura mandibular en la posición de protracción craneocervical y una disminución

en la posición de retracción craneocervical cuando se comparan con la posición neutra

(Higbie et al., 1999). Un esquema de la relación de la postura craneocervical y la

dinámica intra-articular de la ATM es representada en la figura 4.

24

Figura 4. Este esquema representa el efecto de la postura de protracción craneocervical sobre la dinámica mandibular

y la musculatura masticatoria según la evidencia científica de estudios experimentales. La imagen A señala un

aumento de la actividad electromiográfica cuando se induce la postura de protracción craneocervical. La imagen B

representa una posteriorización del cóndilo mandibular asociado a la postura de protracción craneocervical.

1.6.4 Sinergias neuromusculares cervicales y masticatorias

La electromiografía ha sido uno de los instrumentos más utilizados para investigar las

acciones coordinadas, sinérgicas o asociadas entre la musculatura de la región

craneomandibular (musculatura masticatoria) y la musculatura del cuello. Diversos

estudios han comprobado la activación del músculo esternocleidomastoideo durante el

apretamiento (Clark et al., 1993; Davies, 1979; Hochberg et al., 1995; Rodríguez et al.,

2011; So et al., 2004; Venegas et al., 2009; Yoshida, 1988) (Figura 5) y el

rechinamiento dentario (Rodríguez et al., 2011; Venegas et al., 2009), en relación con

esto Clark y cols. describieron que para lograr un 5% de la contracción del

esternocleidomastoideo durante el apretamiento dentario se necesita una activación del

A

B

25

50% del músculo masetero (Clark et al., 1993), evidencia reciente demuestra que

durante la masticación se produce una acción concomitante entre los músculos masetero

y esternocleidomastoideo y el nivel activación de estos músculos se modula de acuerdo

a la demanda del elemento que se esté masticando (Häggman-Henrikson et al., 2013);

otras investigaciones realizadas con electromiografía profunda y superficial han

comprobado que durante diversas tareas de apretamiento dentario varios músculos de la

región cervical (esternocleidomastoideo, semiespinales del cuello y la cabeza,

multífidos cervical, elevador de la escápula, esplenio de la cabeza) son activados y este

reclutamiento se produce en torno al 2% y al 14% de la contracción voluntaria máxima

(Giannakopoulos, Hellmann, et al., 2013; Giannakopoulos, Schindler, et al., 2013;

Hellmann et al., 2012). Al contrario de la mayoría de los estudios que se han realizado

con la función de apretamiento dentario, Armijo-Olivo y Magee estudiaron la apertura

mandibular realizada contra resistencia, los resultados mostraron un aumento similar de

la actividad electromiográfica de los músculos masetero, temporal, esplenio de la

cabeza y de las fibras superiores del músculo trapecio. (Armijo-Olivo and Magee,

2007).

A B

26

Figura 5. Esta figura representa un esquema diseñado según la evidencia científica que muestra que el apretamiento

dentario modifica la actividad electromiográfico de músculos cervicales (A). En la figura B se muestra una

concomitancia entre los movimientos craneocervicales y craneomandibulares (el movimiento de apertura bucal se

asocia un movimiento de extensión craneocervical y el movimiento de cierre al movimiento de flexión

craneocervical).

Un hallazgo importante a destacar es que se ha observado que en posiciones de reposo

mandibular se produce un descenso en la actividad electromiográfica de los músculos

trapecio y esternocleidomastoideo (Ceneviz et al., 2006), sin embargo parece ser que los

diferentes tipos de oclusión no influyen sobre la actividad eletromiográfica de la

musculatura del cuello (Ferrario et al., 2006). La figura 5 representa un esquema de la

elevación de la actividad electromiográfica de los músculos cervicales durante el

apretamiento dentario.

En cuanto a la influencia del movimiento craneocervical sobre la actividad

electromiográfica de la musculatura masticatoria, Funakoshi y cols. observaron que se

producía una gran activación del músculo temporal y una moderada activación del

músculo masetero al realizar una extensión craneocervical (Funakoshi et al., 1976), a

diferencia de este estudio, Ballenberger y cols. investigaron la influencia de los

movimientos de la región cervical superior (rotación, extensión, flexión e inclinación

lateral) y encontraron diferencias estadísticamente significativas sobre la actividad

electromiográfica del músculo masetero pero no sobre el músculo temporal, además en

este estudio se señala que la actividad electromiográfica se incrementa más en extensión

que la flexión craneocervical (Ballenberger et al., 2012), en relación con esto, Forsberg

y cols. determinaron que el incremento de actividad de masetero durante la extensión

craneocervical se produce entre 10º y los 20º (Forsberg et al., 1985). Estudios en donde

se ha inducido experimentalmente la posición de protracción craneocervical han

descrito un aumento de la actividad de los músculos masetero (McLean, 2005; Ohmure

27

et al., 2008), digástrico (Ohmure et al., 2008) y geniogloso (Milidonis et al., 1993).

1.6.5 Cinemática y concomitancia craneocervical/craneomandibular

Los estudios que valoran específicamente la cinemática craneomandibular/

craneocervical han encontrado patrones de movimiento con un alto nivel de

coordinación espacio-temporal (Eriksson et al., 1998, 2000; Kohno, Matsuyama, et al.,

2001; Zafar, 2000; Zafar et al., 2000, 2002), estos hallazgos sugieren que las funciones

mandibulares comprenden acciones sincronizadas de la ATM y la región

craneocervical (articulación atlanto-occipital y las articulaciones vertebrales cervicales),

y esta coordinación es mayor en los movimientos más rápidos (Zafar et al., 2000) y en

general el movimiento craneocervical es sincrónico o se anticipa al movimiento

mandibular (Eriksson et al., 2000). Entre los movimientos que presentan una

concomitancia se encuentra, el de apertura mandibular que se acompaña de una

extensión craneocervical y el movimiento de cierre que se acompaña de una flexión

craneocervical (Eriksson et al., 1998) (Figura 5). Resultados similares se han obtenido

en otros estudios (Kohno, Kohno, et al., 2001; Torisu et al., 2002; Yamabe et al., 1999);

es importante destacar que Eriksson y cols. comprobaron que el movimiento

craneocervical es mayor en la apertura (entorno al 50%) y significativamente menor en

el cierre mandibular (entorno al 30-40%) (Eriksson et al., 1998). Un estudio reciente ha

demostrado que el movimiento concomitante de extensión craneocervical al realizar la

apertura mandibular fue significativamente mayor en los niños que en los adultos, los

autores de esta investigación sugieren que esa situación se genera en los niños como

mecanismos para aumentar la magnitud de la apertura mandibular (Kuroda et al., 2011).

Dos de las funciones orales en donde participa la ATM son la fonación y la masticación,

el movimiento de la región craneocervical también está implicado en estas funciones

28

(Häggman-Henrikson and Eriksson, 2004; Miyaoka et al., 2004), específicamente se ha

demostrado que el movimiento de flexo-extensión craneocervical acompaña los ciclos

masticatorios, pero además de acuerdo a como sea el tamaño del bolo alimenticio que se

mastique, el movimiento de extensión craneocervical se ve modificado (Häggman-

Henrikson and Eriksson, 2004); en cuanto a la fonación se ha observado que diversas

tareas en donde se articulan palabras y se realiza apertura-cierre están asociada a

movimientos de la región craneocervical (Miyaoka et al., 2004).

En la actualidad contamos con evidencia científica muy abundante que demuestra las

relaciones anatomofuncionales entre la regiones craneomandibular y la craneocervical,

sin embargo esta información no es suficiente para demostrar los aspectos

neurofisiológicas implicados en ambas funciones; resultados de investigación básica en

conejos han descrito mecanismos neurales supramedulares implicadas en las acciones

rítmicas cervicales y craneomandibulares (Igarashi et al., 2000), otros autores han

teorizado que las acciones concomitantes son comandos pre-programados a nivel central

(Torisu et al., 2001; Zafar, 2000) y que las funciones vienen moduladas por

mecanismos sensoriomotores trigeminocervicales (Eriksson et al., 1998; Zafar, 2000).

El conocimiento entorno a la neurofisiología trigeminocervical puede ayudar a

comprender las situaciones comorbilidad del dolor de cuello y el DCF o las alteraciones

disfuncionales motoras craneocervicales/craneomandibulares; estos aspectos

neurofisiológicos se desarrollan en el siguiente apartado.

1.7 Neurofisiología del Dolor Cérvico-craneofacial

La base neurofisiológica del dolor referido de la región cervical hacia el área

craneofacial se puede explicar mediante un fenómeno anatómico y fisiológico de

convergencia de aferencias nociceptivas trigeminales y cervicales que confluyen en el

núcleo trigeminal espinal y en los segmentos cervicales superiores (Bartsch and

29

Goadsby, 2003a, 2003b; Bartsch, 2005; Piovesan et al., 2003), este centro de

procesamiento del dolor se ha denominado complejo trigeminocervical (CTC). Este

complejo es el responsable de transmitir información sensorial visceral e información

nociceptiva de la cabeza y la región orofacial hacia otros centros superiores como el

tálamo, el hipotálamo y la corteza somatosensorial primaria (Benjamin et al., 2004;

Malick and Burstein, 1998; Malick et al., 2000, 2001) (Figura 6) e inclusive tiene

conexiones neurales con áreas del diencéfalo y el tronco encefálico relacionadas con la

modulación del dolor (Akerman et al., 2011).

1.7.1 Sistema sensorial trigeminal

El sistema sensorial trigeminal lo conforman: a) el nervio trigémino (y sus tres

divisiones: oftálmica, V1; maxilar, V2; y mandibular, V3); b) el ganglio del trigémino

(Gasser); c) la raíces nerviosas trigeminales; y d) los componentes centrales

trigeminales del tronco encefálico (los núcleos trigeminales, los tractos trigeminales y

las vías tálamo-trigeminales) (Sessle, 2005b; Waite and Ashwell, 2004) (Figura 6). El

nervio trigémino es el más grande de los nervios craneales y es considerado un nervio

mixto ya que tiene una división sensorial y una motora (Majoie et al., 1995; Sanders,

2010), además es importante destacar que proporciona la inervación sensorial principal

de la cara, la cavidad oral y parte de cráneo (Majoie et al., 1995; Sessle, 2005a).

30

Figura 6. La imagen representa la organización neuroanatómica del sistema trigeminal desde la periferia hasta las

conexiones neurofisiológicas a nivel central. S1, corteza somatensorial primaria; VMP, núcleo ventral posteromedial

del tálamo; NTE, núcleo trigeminal espinal; GT ganglio trigeminal.

El ganglio de Gasser es una estructura fina, considerado como un análogo craneal de los

ganglios de la raíz dorsal en el sistema nervioso periférico, pero es significativamente

más grande anatómicamente (Dixon, 1963; Kerr, 1963; Moses, 1967). La mayoría de

los cuerpos celulares de aferencias primarias trigeminales procedentes de la tres

divisiones del nervio trigémino (V1, V2 y V3) residen en el ganglio de Gasser, en donde

se encuentran organizadas de manera somatotópica (Borsook et al., 2003; Byers and

Närhi, 1999; Jacquin et al., 1986; Leiser and Moxon, 2006), pero hay que tomar en

cuenta que los cuerpos celulares de algunas aferencias periodontales y de los husos

musculares residen en el núcleo mesencefálico (Capra and Dessem, 1992).

Las fibras aferentes primarias trigeminales terminan en los tejidos craneofaciales como

31

terminaciones nerviosas libres y funcionan como nociceptores, estos pueden activarse

con estímulos nocivos mecánicos, térmicos y químicos. Su activación puede resultar en

la excitación de fibras de pequeño diámetro y de conducción lenta (A-delta o C) (Sessle,

1999, 2005b, 2011; Takemura et al., 2006). Una serie de componentes neuroquímicos

(por ejemplo, la sustancia P, 5-HT, prostaglandinas, bradiquininas) están involucrados

en la activación de estas terminaciones periféricas por estimulación nociva o en su

sensibilización periférica; la sensibilidad de las terminaciones puede aumentar después

de una lesión leve, y esta sensibilización de las terminaciones nociceptivas es un

mecanismo periférico que ayuda a proteger los tejidos lesionados de repetidos agravios

(Sessle, 2000, 2005b, 2011).

La división V1 inerva la región nasal y peri-orbital (incluyendo la córnea y la

conjuntiva), la duramadre supratentorial, así como la frente y la parte superior de la

cabeza que se superpone con el dermatoma C2. La división V2 suministra inervación al

área cigomática, el labio superior, una parte de la cavidad nasal y oral (incluyendo los

dientes del maxilar y su periodonto asociado), y la división V3 inerva a las estructuras

extra e intra-orales restantes en el tercio inferior de la cara (incluyendo los dientes de la

mandíbula y su periodonto), el labio inferior, la piel de la mejilla, y dos tercios

anteriores de la lengua, el mentón, la ATM, además de la piel cubre la mandíbula y el

lado de la cabeza (parte de la región temporal) a excepción de el ángulo de la mandíbula

que es la parte del dermatoma C2 (Majoie et al., 1995; Sanders, 2010). Las fibras

eferentes motoras del V3 inervan los cuatro músculos de la masticación (masetero,

temporal y pterigoideo medial y lateral), el músculo milohiodeo, el fascículo anterior

del músculo digástrico, el músculo tensor del tímpano y el músculo tensor del velo

palatino (Kamel and Toland, 2001; Majoie et al., 1995). En la figura 7 se representan

gráficamente los dermatomas trigeminales (Figura 7).

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Figura 7. Representación gráfica de los dermatomas trigeminales y cervicales.

El nervio trigémino tiene cuatro núcleos centrales en el tronco encefálico (un núcleo

motor y 3 sensoriales): a) el núcleo mesencefálico trigeminal, que media la

propiocepción; b) el núcleo sensitivo principal, que media la sensación táctil

(principalmente tacto epicrítico y en menor medida tacto protopático); c) el núcleo

motor que proporciona inervación motora: y d) el núcleo espinal trigeminal, que media

el dolor, la sensibilidad térmica y táctil (Majoie et al., 1995; Sessle, 2000) (Figura 8).

El núcleo espinal trigeminal consiste en la división de tres sub-núcleos: a) oral (SVo);

b) interpolar (SVi); y c) caudal (SVc) (Sessle, 1999, 2000, 2005b, 2011). Los sub-

núcleos SVo y SVi se asocian con la transmisión de la percepción táctil; por otra parte,

están implicados principalmente en mecanismos nociceptivos orofaciales relacionados

especialmente con el dolor intra-oral y peri-oral (Dallel et al., 1988, 1990; Raboisson et

al., 1995). Los núcleos trigeminales se representan en la figura 8.

33

Figura 8. Representación gráfica de los núcleos trigeminales, también se muestra la subdivisión del núcleo trigeminal

espinal en sus 3 sub-núcleos: SVo, sub-núcleo trigeminal oral; SVi, sub-núcleo trigeminal interpolar; SVc, sub-

núcleo trigeminal caudal.

El sub-núcleo SVc se extiende desde el nivel de la OBEX (bulbo raquídeo) hasta el

nivel de C3 de la médula espinal cervical. Este sub-núcleo es el homólogo de la

sustancia gelatinosa del asta de posterior de la medula espinal ya que sus neuronas

tienen morfología celular similar, así como las conexiones sinápticas, y sus funciones.

Dado que el sub-núcleo SVc se encuentra inmediatamente superior a la sustancia

gelatinosa de los niveles de la médula espinal cervical, también se le denomina como el

"asta dorsal medular" (Sessle and Hu, 1991; Sessle, 1987; Sessle et al., 1986). El sub-

núcleo SVc es considerado como la principal área relacionada con la información

nociceptiva de los tejidos craneofaciales superficiales y profundos (Dubner and Bennett,

1983; Ebersberger et al., 2001; Schepelmann et al., 1999; Sessle and Hu, 1991; Sessle,

34

1987, 2005b).

En las láminas superficiales y profundas del SVc predominan dos tipos de neuronas

nociceptivas (neuronas nociceptivas específicas [NE] y neuronas de rango dinámico

amplio [RDA]), estas neuronas trasmiten información aferente nociceptiva hacia centros

superiores (núcleo ventral posteromedial del tálamo [VPM]) (Sessle, 1987, 2000,

2005a, 2011). Las neuronas NE sólo responden a estímulos nocivos (por ejemplo,

pellizcar, estímulos térmicos nocivos) aplicados a un campo receptivo craneofacial

localizado y reciben impulsos aferentes de fibras de diámetro pequeño (fibras A delta

y/o C); las neuronas RDA son excitadas por estímulos no nocivos (por ejemplo

estímulos táctiles), así como por estímulos nocivos, y pueden recibir impulsos aferentes

de fibras de gran diámetro (fibras A) y de pequeño diámetro (fibras C) (Sessle, 1999).

La mayoría de neuronas NE y RDA, también pueden ser excitadas por otros tipos de

entradas aferentes periféricas de diversas regiones como las meninges, tejido vascular,

los dientes, la ATM o en los músculos masticatorios (Burstein et al., 1998; Dostrovsky

et al., 1991; Sessle, 1996, 1999, 2000). Los extensos patrones convergentes de entradas

aferentes que son característicos de la ATM o de la duramadre son activados por

neuronas NE y RDA en el SVc, este fenómeno podría explicar la mala localización del

dolor profundo, así como la difusión del dolor referido que es condición típica de

dolencias que implican la ATM y la musculatura asociada (Sessle, 1999, 2011).

Las neuronas trigeminales somatosensoriales del tronco encefálico proyectan a otras

estructuras de esta misma región anatómica como la formación reticular y los núcleos

motores de otros nervios craneales; estas conexiones proporcionan respuestas

autonómicas y motoras ante estímulos craneofaciales (Sessle, 1987, 1996, 1999).

Específicamente las neuronas del SVc proyectan hacia el núcleo VPM del tálamo a

través de una vía multisináptica denominada tracto lemnisco trigeminal dorsal (tracto

35

trigeminotalámico dorsal) (Dougherty and Willis, 1992; Dougherty et al., 1992; Sessle,

1999; Sherman et al., 1997) (Figura 9). Las neuronas nociceptivas del núcleo VPM

tienen conexiones con la corteza somatosensorial (Sherman et al., 1997), representando

la dimensión sensorial-discriminativa del dolor. También se ha observado otras

conexiones como por ejemplo con la corteza cingulada anterior, situando a estos

circuitos neurales como parte de la dimensión afectivo-emocional del dolor (Sessle and

Hu, 1991; Sessle, 1999).

Figura 9. Representación gráfica del tracto trigeminotalámico dorsal. GT, ganglio trigeminal; NTE, núcleo

trigeminal espinal; SVc; sub-núcleo trigeminal caudal; VPM, Núcleo ventral posteromedial del tálamo; S1, corteza

somatosensorial primaria.

1.7.2 Neuroanatomía de los segmentos cervicales superiores

La médula espinal cervical superior incluye los segmentos espinales C1 y C2 en donde

emergen periféricamente los tres primeros nervios cervicales que se distribuyen en un

ramo dorsal, un ramo ventral y los nervios sinovertebrales (Alix and Bates, 1999;

36

Bogduk, 1981), estos nervios inervan a nivel motor y sensitivo diversas estructuras de la

parte posterior de la cabeza y el cuello (Bogduk, 2001) que pueden generar dolor

referido hacia la cabeza y la región orofacial (Johnston et al., 2013). El nervio C1

presenta un ganglio de la raíz dorsal ectópico, se ha observado que en algunos casos

(20%) este nervio carece de raíz dorsal y en estos casos las células ganglionares se

pueden encontrar entre las raíces del nervio espinal accesorio (Ouaknine and Nathan,

1973). Este nervio carece de distribución sensitiva cutánea, sin embargo a través de su

rama dorsal inerva sensitivamente a nivel profundo los músculos cortos del triángulo

suboccipital (Bogduk, 1982), su ramo ventral pasa por detrás y debajo de articulación

atlanto-occipital a la que suministra inervación (Bogduk, 2001)

El nervio C2 da inervación sensitiva a las articulaciones atlantoaxoideas laterales y

mediales; la duramadre de la fosa craneal posterior y de la médula espinal superior; y la

arteria carótida y vertebral. La rama ventral de este nervio inerva los músculos

paravertebrales, el músculo esternocleidomastoideo y el trapecio y la rama dorsal los

músculos semiespinales de la cabeza y el músculo esplenio de la cabeza. El nervio

sinovertebral de C2 se une a los de C1 y C3 para suministrar inervación a los

ligamentos transversal, alar y a la membrana tectoria (Bogduk, 2001). La rama ventral

de C3 se une al plexo cervical e inerva los músculos paravertebrales. La rama medial

del ramo dorsal de C3 inerva el músculo semiespinoso cervical y el músculo multifidus

y además inerva las articulaciones cigapofisiarias de C2-C3. El nervio sinovertebral de

C3 inerva el disco intervertebral C2-3 en su cara posterior (Bogduk, 2001; Bogduk et

al., 1988).

A nivel cutáneo la inervación sensitiva de la región craneocervical la suministran los

nervios occipital menor, occipital mayor y el nervio auricular mayor (Poletti, 1991; Shin

et al., 2007), estos tres nervios sensitivos más la zona cutánea que inervan conformarían

37

los dermatomas de la región craneocervical, estos dermatomas (C2, C3) tienen una

representación que incluye la parte posterior del cráneo (cuero cabelludo), el ángulo de

mandíbula, la región sub-occipital, la parte posterior de la oreja y la garganta (Poletti,

1991). Es importante destacar que la mayor distribución cutánea del nervio C2 está

representada por el nervio occipital mayor (Poletti, 1991).

1.7.3 Complejo trigeminocervical

El CTC es una unidad anatómica-funcional que forman las astas dorsales de los dos

segmentos superiores de la médula cervical y el SVc del núcleo espinal trigeminal

(Becker, 2010; Hoskin et al., 1999; Hu et al., 2005; Piovesan et al., 2003). Estudios

anatómicos en animales han encontrado que el CTC se extiende hasta el segmento

cervical C2-C3 (Goadsby and Hoskin, 1997; Kaube et al., 1993; Strassman et al., 1994).

En el CTC se produce una convergencia de neuronas nociceptivas de segundo orden que

reciben aferencias nociceptivas primarias trigeminales y de los tres primeros nervios

cervicales (Bartsch and Goadsby, 2003b; Bartsch, 2005; Bogduk, 2001; Goadsby et al.,

2008; Hu et al., 1995, 2005; Piovesan et al., 2003) (Figura 10). Evidencia científica de

estudios básicos en animales ha demostrado este fenómeno de convergencia (Bartsch

and Goadsby, 2002, 2003a; Hu et al., 1993; Sessle et al., 1986; Yu et al., 1995), y

también se tiene evidencia de este mecanismo en seres humanos (Busch et al., 2006;

Piovesan et al., 2001).

38

Figura 10. Representación gráfica del complejo trigeminocervical (CTC).

El CTC puede ser sensibilizado por aferencias nociceptivas primarias provenientes del

músculo masetero y de la ATM (Cairns et al., 2001, 2002; Nishimori et al., 1986;

Shigenaga et al., 1988), además se ha descrito que las aferencias primarias nociceptivas

provenientes de la piel y de los músculos cervicales son capaces de excitar neuronas del

CTC (Bartsch and Goadsby, 2003a; Le Doaré et al., 2006; Sessle et al., 1986), sin

embargo parece ser que la principal contribución aferente cervical hacia este complejo

neural está mediada por la raíz de C2, representada periféricamente por el nervio

occipital mayor (Bartsch, 2005), en relación con esto, Goadsby y cols. demostraron que

la activación de las fibras aferentes del nervio occipital mayor aumentan la actividad

metabólica de neuronas del CTC (Goadsby et al., 1997), por otra parte, Le Doare y cols.

observaron que los receptores N-metil-D-aspartato (NMDA) glutamatérgicos están

39

implicados en estas sinapsis (Le Doaré et al., 2006), varios estudios han demostrado que

los receptores NMDA son importantes en el desarrollo de la sensibilización central del

SVc (Chiang et al., 1998; Yu et al., 1996), así como los receptores de la neuroquinina y

purinérgicos (Dubner and Ren, 2004). Recientemente se ha comprobado en modelo

animal, que la lesión sobre un nervio espinal superior provoca alodinia mecánica y la

hiperalgesia térmica en la piel de la cara, los resultados de esta investigación también

sugieren que la fosforilación de la kinasa de regulación extracelular en el SVc y en las

neuronas de C1-C2 y la activación de las células astrogliales están involucradas en el

dolor orofacial extraterritorial producido después de una lesión (Kobayashi et al., 2011).

Xie describe que en la sensibilización central trigeminal las células gliales tienen una

importante implicación incluyendo la interacción con los receptores NMDA

glutamatérgicos y purinérgicos (Xie, 2008).

1.7.4 Sensibilización central del complejo trigeminocervical

Neurofisiológicamente la recepción de entradas de aferencias nociceptivas en el sistema

nervioso central forma parte de la sensibilización central que es un proceso fundamental

en el desarrollo y mantenimiento del dolor referido y el dolor crónico (Arendt-Nielsen

et al., 2000; Salter, 2004). En la sensibilización central trigeminal se produce una

expansión de los campos receptivos profundos y cutáneos neuronales, y además se han

observado otros cambios en las propiedades de las neuronas del trigeminales y en las

vías nociceptivas medulares (Bereiter et al., 2005; Chiang et al., 1998, 2005; Lam et al.,

2009; Salter, 2004; Vernon et al., 2009), específicamente se ha demostrado que la

aplicación experimental de una “sopa inflamatoria” en la duramadre puede inducir una

sensibilización central de las neuronas trigeminales nociceptivas de segundo orden en el

SVc, generando una mayor capacidad de respuesta a la estimulación cutánea de la

región facial y en la duramadre (Burstein et al., 1998), en relación con este hallazgo,

40

Bartsch y Goadsby encontraron que la estimulación del nervio occipital mayor podía

causar una sensibilización central con un aumento de la excitabilidad de la entrada de la

duramadre (Bartsch and Goadsby, 2002), además, se ha observado que la activación de

los nociceptores meníngeos por mediadores pro-inflamatorios sensibilizan a las

neuronas de primer orden en el ganglio trigeminal (Strassman et al., 1996) y las

neuronas de segundo orden trigeminovasculares en el CTC (Burstein et al., 1998).

En el proceso de sensibilización central se producen salidas eferentes que involucran

conexiones entre motoneuronas y aferencias nociceptivas neuronales que su vez generan

respuestas motoras (Bartsch, 2005; Sessle, 2002). Evidencia científica basada en

estudios realizados con modelos animales han demostrado que la estimulación química

nociceptiva de estructuras profundas paravertebrales musculares de la región cervical

evocan efectos reflejos, incluyendo un aumento de la actividad electromiográfica en los

músculos masticatorios y cervicales ipsilaterales (Hu et al., 1993, 1996; Shin et al.,

2005) y alteraciones en los reflejos de apertura mandibular (Makowska et al., 2005).

Similares resultados se han observado en la estimulación nociceptiva de las meninges

posteriores de la rata (Hu et al., 1995). Por otra parte, se ha demostrado que la inyección

de bradiquinina en el músculo masetero en conejos provoca un aumento de la actividad

fusimotora de los husos musculares paravertebrales de la región cervical, estos

hallazgos sugieren que existe una potente conexión refleja entre el sistema trigeminal y

el sistema neuromuscular cervical (Hellström et al., 2000, 2002), resultados similares se

han descrito en estudios realizados en sujetos sanos, en donde se observó que un dolor

provocado experimentalmente en el músculo masetero provoca un aumento de la

actividad electromiográfica en los músculos esternocleidomastoideo y el esplenio del

cuello (Svensson et al., 2004), además de un aumento del reflejo de estiramiento de

estos músculos (Wang et al., 2004); otra de las manifestaciones motoras a nivel

41

mandibular que se han observado es la limitación momentánea de la apertura

mandibular después de provocar un dolor experimental en el músculo trapecio mediante

la infiltración de suero salino hipertónico (Komiyama et al., 2005). Un hallazgo

importante observado recientemente es que al provocar un dolor experimental sobre el

músculo masetero se produce una alteración del control motor de las acciones

integradas de la región craneocervical y craneomandibular al realizar los movimientos

de apertura y cierre (Wiesinger et al., 2013).

La sensibilización central del CTC se manifiesta clínicamente con un aumento de las

áreas de expansión del dolor en territorios trigeminales y cervicales, una mala

localización del dolor, hiperalgesia, alodinia mecánica (Katsarava et al., 2002; Kaube et

al., 2002; Sessle, 1999, 2002, 2011) y una disfunción de la activación del sistema

inhibitorio descendente (King et al., 2009; Maixner et al., 1998; Sarlani et al., 2004)

1.8 Modulación del Dolor en el Complejo Trigeminocervical

La recepción de los estímulos nociceptivos por las neuronas de segundo orden del CTC

está modulada por proyecciones inhibitorias descendentes de estructuras del tronco

encefálico, el diencéfalo y la corteza somatosensorial (Akerman et al., 2011; Bartsch

and Goadsby, 2003b; Sessle, 1999, 2000), se ha demostrado que la manipulación de las

neuronas ventrolaterales de la sustancia gris periacueductal (Bartsch, Knight, et al.,

2004; Knight and Goadsby, 2001; Knight et al., 2002), el núcleo magno del rafe

(Edelmayer et al., 2009) y el bulbo rostroventral (Lambert et al., 2008) pueden modular

la actividad nociceptiva evocada en el CTC, evidencia previa ha demostrado que la

estimulación de estas áreas produce un importante efecto inhibitorio anti-nociceptivo

(Fields et al., 1991) (Figura 11), sin embargo es importante destacar que la activación

del bulbo rostroventral también puede facilitar la hiperalgesia, el dolor neuropático y el

dolor crónico (Porreca et al., 2002; Ren and Dubner, 2002; Sugiyo et al., 2005; Venegas

42

et al., 2009). Otros estudios en donde se ha estimulado químicamente la región posterior

del hipotálamo han demostrado que esta región también influye en la modulación

nociceptiva del CTC (Bartsch et al., 2005; Bartsch, Levy, et al., 2004).

Figura 11. Representación gráfica del sistema inhibitorio descendente y las estructuras implicadas en la modulación

de la actividad nociceptiva. SVc, sub-núcleo trigeminal cervical; NTE, núcleo trigeminal espinal; BRV, bulbo

rostroventral; vlPAG; área ventrolateral de la sustancia gris periacueductal; HT, hipotálamo; S1, corteza

somatosensorial primaria.

En el proceso de activación del sistema inhibitorio descendente se producen diversos

mecanismos que incluyen la participación de los receptores opioides y de

neurotransmisores como el GABA y la serotonina (5-HT) (Sessle, 1999, 2002). El SVc

recibe proyecciones serotoninérgicas y encefalinérgicas del núcleo magno del rafe

(Beitz, 1982; Beitz et al., 1987) que tienen una actuación en la modulación del dolor

(Mason and Fields, 1989). Por otra parte, se ha demostrado que en la médula espinal y

en el SVc el principal neurotransmisor que actúa en la actividad eferente inhibitoria en

43

el bulbo rostroventral es la 5-HT (Beitz, 1982; Clatworthy et al., 1988; Fields et al.,

1991), en relación con esto, Okamato y cols. comprobaron en un modelo animal de

dolor inflamatorio persistente de la ATM que los receptores 5-HT3 en el CTC están

involucrados en los circuitos inhibitorios serotoninérgicos centrales que modulan la

actividad nociceptiva profunda y superficial (Okamoto et al., 2005).

Acciones terapéuticas relacionadas con los cambios del comportamiento, intervenciones

farmacológicas y otros tratamientos que actúan a nivel estructural, influyen sobre

mecanismos tronco encefálicos relacionados con la modulación descendente del dolor

craniofacial (Sessle, 2002).

1.8.1 Influencia de las aplicaciones terapéuticas sobre el dolor craneofacial

A partir de los resultados de estudios experimentales sobre mecanismos

neurofisiológicos implicados en la modulación de dolor en el CTC, muchos

investigadores han planteado estrategias terapéuticas para influir sobre estructuras de la

región cervical y a su vez modular el dolor de cabeza y orofacial. Las intervenciones

sobre el nervio occipital han sido de las más utilizadas en las últimas décadas, son

varios los estudios que se sugieren que la neuro-estimulación periférica del nervio

occipital es efectiva en la disminución del dolor orofacial y la cefalea en un porcentaje

importante de los pacientes en los que se aplica este tratamiento (Jasper and Hayek,

2008; Lee and Huh, 2013; Saper et al., 2011; Serra and Marchioretto, 2012; Silberstein

et al., 2012; Slavin et al., 2006). Siguiendo con las intervenciones sobre el nervio

occipital, hay que destacar que Leroux y Ducros en una recientemente revisión de

ensayos clínicos y series de casos, describen que la infiltración mediante cortico-

esteroides con o sin adición de anestésicos locales sobre el nervio occipital en pacientes

con cefalea en racimos produce efectos inmediatos en la disminución de la frecuencia

de los ataques, sin embargo varios estudios describen que el dolor local tras la

44

intervención es un efecto secundario muy común pero no considerado grave (Leroux

and Ducros, 2013), en otra revisión narrativa se sugiere que la infiltración del nervio

occipital mayor presenta efectos positivos sobre los pacientes con migraña pero se

señala que estos datos se interpreten con precaución ya que se han extraído de estudios

con pobres diseños metodológicos (Ashkenazi and Levin, 2007). Posterior a esta

revisión, se publicaron dos ensayos clínicos aleatorizados en donde se pretendía

comprobar el efecto de una infiltración del nervio occipital mayor y de puntos gatillo de

músculos paravertebrales y del trapecio utilizando anestésicos locales con y sin cortico-

esteroides en pacientes con migraña, los resultados de ambas investigaciones

demostraron la efectividad de ambas intervenciones en la reducción del dolor de cuello

y el dolor de cabeza pero no hubo diferencia en la comparación de los dos tratamientos

(Ashkenazi et al., 2008; Saracco et al., 2010). Evidencia científica proveniente de

estudios de series de casos retrospectivos describen que la infiltración intramuscular de

bupivacaina en la musculatura paravertebral reduce el dolor en pacientes adultos

(Mellick and Mellick, 2003, 2008; Mellick et al., 2006) y en niños (Mellick and

Pleasant, 2010) que presentan dolor orofacial y/o cefalea.

La evidencia sobre la administración de bupivacaina intratecal en la región cervical para

dolores refractarios cervicales, de cabeza y orofaciales es limitada, sin embargo las

series de casos publicadas describen una eficacia en la analgesia producida y una

disminución de la utilización de fármacos opiáceos (Appelgren et al., 1996; Lundborg

et al., 2009) por otra parte, los efectos adversos descritos fueron pocos y la mayoría de

los casos transitorios (Lundborg et al., 2009).

Intervenciones específicas de fisioterapia aplicadas al tratamiento de la región cervical

para modular el dolor en pacientes con cefalea han sido muy investigadas en las últimas

dos décadas, específicamente se debe destacar que un gran número de ensayos clínicos

45

muestran que la terapia manual, el ejercicio terapéutico o la combinación de ambas

enfocadas a tratar estructuras musculoesqueléticas de la región cervical han demostrado

efectividad en las disminución de la intensidad y la frecuencia del dolor en pacientes

con cefalea tensional y cefalea cervicogénica (Castien et al., 2011, 2012, 2013; Espí-

López and Gómez-Conesa, 2014; Espí-López et al., 2014; van Ettekoven and Lucas,

2006; Hall et al., 2007; Mongini et al., 2012; Ylinen et al., 2010).

46

47

JUSTIFICACIÓN

48

2. JUSTIFICACIÓN DEL TRABAJO REALIZADO

La región orofacial y el cráneo, que a su vez incluyen estructuras orales y dentales

representan una de las zonas anatómicas más complejas del organismo, esta situación

conlleva a una difícil compresión de los mecanismos fisiopatológicos de los trastornos

que afectan a la región craneofacial como por ejemplo los TCM, las cefaleas y el dolor

orofacial (Fricton, 2014). La comprensión de la clínica, la patogénesis y el tratamiento

es esencial para ayudar a los pacientes que presentan estos problemas (Graff-Radford,

2007).

Es manifiesto que en la últimas décadas se ha incrementado de manera exponencial la

investigación en torno al DCF, estos estudios en su mayoría se han enfocado en estudiar

los mecanismos biológicos periféricos y centrales relacionados con la transmisión y

modulación nociceptiva, así como los sistemas de clasificación del paciente y los

factores psicosociales implicados (Hargreaves, 2011), los resultados de algunas

investigaciones en esta línea sugieren, que áreas extra-trigeminales como la región

cervical parecen tener un papel relevante en la fisiopatología de las cefaleas y el dolor

orofacial (Graff-Radford, 2012), a pesar de esto, consideramos que aún es necesario

contar con más estudios que apoyen los hallazgos demostrados y que además terminen

de identificar con mayor exactitud las implicaciones biomecánicas y neurofisiológicas

de la región cervical sobre el DCF, por otra parte, creemos que es importante aclarar

cómo estos datos se pueden utilizar para el diagnóstico clínico y el planteamiento

terapéutico de fisioterapia. En los últimos años el tratamiento de fisioterapia ha

adquirido un estatus importante en el tratamiento de los TCM y el DCF (Aggarwal and

Keluskar, 2012), sin embargo no contamos con evidencia científica suficiente que

demuestre la relevancia o el papel del tratamiento de fisioterapia sobre la región cervical

en los pacientes con TCM, este es uno de los motivos centrales que justifica esta tesis

49

doctoral y que nos lleva a plantear diversos objetivos entorno a esta cuestión.

La evidencia científica contemporánea nos ha llevado a la reflexión sobre las

limitaciones que presentan los estudios y los abordajes clínicos basados en modelos

mecanicistas o que toman en cuenta únicamente la dimensión sensorial-discriminativa

del DCF (Reid and Greene, 2013), en una parte de esta tesis hemos intentado contestar

interrogantes desde un punto de vista más integral utilizando un enfoque bioconductual

en el que planteamos las posibles interacciones entre el dolor y la discapacidad

craneofacial, con variables motoras, de discapacidad cervical y variables psicológicas.

El enfoque bioconductual para el tratamiento, el diagnóstico y la valoración del DCF

reconoce la importancia de los factores psicosociales, como antecedentes de dolor, los

estados emocionales en curso, el estatus cognitivo, las creencias de salud, y las

habilidades de afrontamiento, que interactúan con las alteraciones fisiológicas en la

determinación de la experiencia del dolor para los pacientes (Carlson, 2008; Shephard et

al., 2014).

50

51

OBJETIVOS

52

3. OBJETIVOS

El objetivo general de esta investigación es determinar la influencia biomecánica y

neurofisiológica de la región cervical sobre el dolor y la discapacidad craneofacial

crónica. Además se pretende identificar como determinados factores bioconductuales

influyen sobre la función craneomandibular, la discapacidad y el dolor craneofacial.

A continuación se detallan los objetivos específicos:

1- Evaluar la influencia de la postura craneocervical sobre la discapacidad

craneofacial, la dinámica mandibular y el umbral de dolor a la presión,

además se pretende analizar las diferencias de postura craneocervical entre

sujetos asintomáticos y pacientes con dolor cérvico-craneofacial (DCCF)

crónico.

Este objetivo se ha abordado en las publicaciones originales I y II:

I. La Touche R, París-Alemany A, von Piekartz H, Mannheimer JS,

Fernández-Carnero J, Rocabado M. The influence of cranio-cervical posture

on maximal mouth opening and pressure pain threshold in patients with

myofascial temporomandibular pain disorders. Clin J Pain. 2011

Jan;27(1):48-55

II. López-de-Uralde-Villanueva I, Beltran-Alacreu H, Paris-Alemany A,

Angulo-Díaz-Parreño S, La Touche R. Reliability, Standard Error, and

Minimal Detectable Change of Two Tests for Craniocervical Posture

53

Assessment in Asymptomatic Subjects and Chronic Neck/craniofacial Pain

Patients. 2014 (En revisión).

2- Determinar la influencia del dolor y la discapacidad cervical sobre la función

sensoriomotora trigeminal.

Este objetivo se ha abordado en las publicaciones originales III y V:

III. La Touche R, Fernández-de-Las-Peñas C, Fernández-Carnero J, Díaz-

Parreño S, Paris-Alemany A, Arendt-Nielsen L. Bilateral mechanical-pain

sensitivity over the trigeminal region in patients with chronic mechanical

neck pain. J Pain. 2010 Mar;11(3):256-63

V. La Touche R, Paris-Alemany A, Gil-Martínez A, Pardo-Montero J, Angulo-

Díaz-Parreño S, Fernández-Carnero J. The Influence of Neck Disability and

Pain Catastrophizing about Trigeminal Sensory-Motor System in Patients

with Headache Attributed to Temporomandibular Disorders. 2014 (En

revision)

3- Estudiar la asociación entre la discapacidad craneofacial y la discapacidad

cervical en pacientes con trastornos craneomandibulares, cefaleas y dolor

craneofacial crónico.

Este objetivo se ha abordado en las publicaciones originales II y IV:

II. López-de-Uralde-Villanueva I, Beltran-Alacreu H, Paris-Alemany A,

Angulo-Díaz-Parreño S, La Touche R. Reliability, Standard Error, and

54

Minimal Detectable Change of Two Tests for Craniocervical Posture

Assessment in Asymptomatic Subjects and Chronic Neck/craniofacial Pain

Patients. 2014 (En revisión).

IV. La Touche R, Pardo-Montero J, Gil-Martínez A, Paris-Alemany A,

Angulo-Díaz-Parreño S, Suárez-Falcón JC, Lara-Lara M, Fernández-Carnero

J. Craniofacial pain and disability inventory (CF-PDI): development and

psychometric validation of a new questionnaire. Pain Physician. 2014 Jan-

Feb;17(1):95-108.

4- Analizar la asociación de factores psicológicos como la depresión, el miedo

al movimiento y el catastrofismo ante el dolor con variable motoras, de dolor

y discapacidad cervical y craneofacial.

Este objetivo se ha abordado en las publicaciones originales III, IV y V:

III. La Touche R, Fernández-de-Las-Peñas C, Fernández-Carnero J, Díaz-

Parreño S, Paris-Alemany A, Arendt-Nielsen L. Bilateral mechanical-pain

sensitivity over the trigeminal region in patients with chronic mechanical

neck pain. J Pain. 2010 Mar;11(3):256-63

IV. La Touche R, Pardo-Montero J, Gil-Martínez A, Paris-Alemany A,

Angulo-Díaz-Parreño S, Suárez-Falcón JC, Lara-Lara M, Fernández-Carnero

J. Craniofacial pain and disability inventory (CF-PDI): development and

psychometric validation of a new questionnaire. Pain Physician. 2014 Jan-

Feb;17(1):95-108.

V. La Touche R, Paris-Alemany A, Gil-Martínez A, Pardo-Montero J, Angulo-

Díaz-Parreño S, Fernández-Carnero J. The Influence of Neck Disability and

Pain Catastrophizing about Trigeminal Sensory-Motor System in Patients

55

with Headache Attributed to Temporomandibular Disorders. 2014 (En

revision)

5- Determinar el efecto del tratamiento de fisioterapia aplicado en la región

cervical sobre la función mandibular y el dolor craneofacial.

Este objetivo se ha abordado en las publicaciones originales VI y VII:

VI. La Touche R, Fernández-de-las-Peñas C, Fernández-Carnero J,

Escalante K, Angulo-Díaz-Parreño S, Paris-Alemany A, Cleland JA. The

effects of manual therapy and exercise directed at the cervical spine on pain

and pressure pain sensitivity in patients with myofascial temporomandibular

disorders. J Oral Rehabil. 2009 Sep;36(9):644-52.

VII. La Touche R, París-Alemany A, Mannheimer JS, Angulo-Díaz-Parreño S,

Bishop MD, Lopéz-Valverde-Centeno A, von Piekartz H, Fernández-

Carnero J. Does mobilization of the upper cervical spine affect pain

sensitivity and autonomic nervous system function in patients with cervico-

craniofacial pain?: A randomized-controlled trial. Clin J Pain. 2013

Mar;29(3):205-15.

56

57

MATERIAL Y MÉTODOS

58

4. MATERIAL Y MÉTODOS

Se realizaron un total de 7 estudios con diferentes diseños metodológicos (Tabla 2). Los

pacientes fueron reclutados de dos clínicas odontológicas privadas de la Comunidad de

Madrid (Estudios VI y VII), dos clínicas privadas especializadas en dolor orofacial y

TCM (Estudios II, III, IV y V), una clínica universitaria de la Comunidad de Madrid

(Estudio I) y el Hospital Universitario La Paz de la Comunidad de Madrid (Estudio IV),

en los estudios donde se realizaron comparaciones con sujetos asintomáticos los

pacientes fueron reclutados en tres campus universitarios de la comunidad de Madrid

(Estudios II, III y V). Los procedimientos utilizados en las investigaciones de esta tesis

doctoral se realizaron bajo las directrices de la Declaración del Helsinki. Todos los

participantes de los estudios dieron su consentimiento informado por escrito antes de

comenzar con las investigaciones y estas fueron aprobadas previamente por los

respectivos comités de ética locales. Una visión general de los diseños de estudio,

características de la muestra, los métodos de recogida de datos e instrumentos de

medición se presentan en la Tabla 2.

Tabla 2. Descripción general de los diseños, características de la muestra, variables e

intervenciones.

Estudio I Estudio II Estudio III Estudio IV Estudio V Estudio VI Estudio VII

Tamaño de la

muestra

N=29

(19 mujeres; 10

hombres)

N=60 GE

(32 mujeres; 28

hombres)

N=53 GC

(30 mujeres; 23

hombres)

N=23 GE

(13 mujeres; 10

hombres)

N=23 GC

(15 mujeres; 8

hombres)

N=192

(132 mujeres; 60

hombres)

N=41 GE1

(26 mujeres; 15

hombres)

N=42 GE2

(25 mujeres; 17

hombres)

N=39 GC

(26 mujeres; 13

hombres)

N=19

(14 mujeres; 5

hombres)

N=16 GE

(10 mujeres; 5

hombres)

N=16 GC

(11 mujeres; 4

hombres)

Características de

los Participantes

Pacientes con TCM/

dolor miofascial

GE= pacientes con

TCM/ dolor miofascial

GE=dolor de

cuello crónico

Pacientes con

DCF

GE1=Cefalea

atribuida a TCM

Pacientes con

TCM/ dolor

Pacientes con

TCM/ dolor

59

crónico crónico y dolor de cuello

crónico mecánico

(DCCF)

GC=sujetos

asintomáticos

mecánico

GC=sujetos

asintomáticos

a.TCM/ dolor

miofascial crónico

b.TCM/ artralgia

c.Cefalea

atribuida por

TCM

d.Cefalea

tensional

e. Migraña

con moderada

discapacidad

cervical

GE2= Cefalea

atribuida a TCM

con leve

discapacidad

cervical

GC=Sujetos

asintomáticos

miofascial

crónico

miofascial

crónico y dolor

de cuello crónico

mecánico

(DCCF)

Media y Desviación

Típica de la Edad

34.69 ±10.83 GE=41,7±11,7

GC=38,1±10,5

GE=28±5

GC=28±6

46±13.06 GE1=44.31±10.9

GE2=40.95±12.8

9

GC=40.61±10.01

37±10 GE=33,19±9,49

GC=34,56±7,84

Diseño del Estudio Estudio prospectivo

transversal

Estudio prospectivo

transversal de fiabilidad

intra e inter-examinador

Estudio

prospectivo

transversal

Estudio

multicéntrico

prospectivo

transversal de un

diseño de un

cuestionario

Estudio

longitudinal de

casos y controles

Estudio

prospectivo de

casos

Ensayo clínico

aleatorio

controlado

Variables Somato-

sensoriales y

motoras

- UDP

- MAI

- EVA

-Postura de cabeza

-Distancia mentón-

esternón

- UDP

- END

- - UDP

-MAI

- EVA

- EVAF

-UDP

-MAI

- EVA

-UDP

-EVA

[Variable

simpáticas: CP,

FC, TC, FR]

Medidas de auto-

registro

IDC

IDD-CF

IDC

BDI

STAI

IDC

IDD-CF

HIT-6

ECD

TSK-11

IDC

HIT-6

ECD

- - IDC

- BDI

- STAI

Intervenciones - - - - - -TMO en la

región cervical

(a. Rol anterior

de la región

cervical

superior; b.

movilización

postero-anterior

de C5)

-ETCM

-TMO en la

región cervical

(movilización

antero-posterior

de la región

cervical superior)

Abreviaturas: TCM, trastornos craneomandibulares; DCF, dolor craneofacial; DCCF, dolor cérvico-craneofacial; UDP, umbral de

60

dolor a la presión; MAI, máxima apertura interincisal; EVA, escala visual analógica del dolor; END, escala numérica del dolor; GE,

grupo experimental; GC, grupo control; IDC, índice de dolor cervical; IDD-CF, inventario de dolor y discapacidad craneofacial;

BDI, inventario de depresión Beck; STAI, cuestionario de ansiedad estado-rasgo; HIT-6, cuestionario de impacto de la cefalea;

ECD; escala de catastrofismo ante el dolor; TSK-11, escala de Tampa de Kinesiofobia; EVAF, escala visual analógica de fatiga;

TMO, terapia manual ortopédica; ETCM, ejercicio terapéutico de control motor; CP, conductancia de la piel; FC, frecuencia

cardíaca; FR, frecuencia respiratoria; TC, temperatura cutánea.

4.1 Participantes

La muestra de los estudios I y VI estuvo conformada por pacientes que presentaban

TCM atribuido a dolor miofascial, esta denominación se extrae de los Criterios

diagnósticos de investigación para TCM (Dworkin and LeResche, 1992; Schiffman et

al., 2010), aunque es importante mencionar que además se establecieron otros criterios

de inclusión que se exponen a continuación: a) diagnóstico primario de dolor miofascial

de acuerdo a los Criterios diagnósticos de investigación para TCM; (Dworkin and

LeResche, 1992; Schiffman et al., 2010); b) dolor bilateral en los músculos masetero y

temporal; c) duración del dolor mayor a 6 meses; d) intensidad del dolor mayor a 30mm

según la escala visual analógica (EVA); y e) presencia de PGM en la musculatura

masticatoria. Los criterios de exclusión adoptados en estos estudios fueron los

siguientes: a) TCM atribuidos a disfunciones articulares o enfermedades degenerativos

de acuerdo a los Criterios diagnósticos de investigación para TCM (Dworkin and

LeResche, 1992; Schiffman et al., 2010); b) lesiones traumáticas como fracturas o

latigazo cervical; c) enfermedades sistémicas reumatológicas como fibromialgia y

artritis; c; dolor neuropático; y d) concomitancia con cefaleas primarias.

El estudio III contó con una muestra de pacientes con dolor de cuello crónico mecánico

inespecífico. Conceptualmente esta dolencia se define como una afectación que presenta

signos y síntomas de disfunción muscular como empeoramiento de dolor con el

mantenimiento de la postura, limitación del rango del movimiento y dolor a la palpación

de la musculatura cervical. Además los pacientes incluidos en este estudio tenían que

61

tener el dolor en un periodo superior a 6 meses. Los criterios de exclusión adoptados en

este estudio fueron los siguientes: a) dolor de cuello unilateral; b) enfermedades

reumáticas; c) latigazo cervical; d) cirugías previas de la región cervical; e) diagnóstico

de radiculopatía cervical; f) diagnóstico de TCM.

La muestra del estudio IV estuvo representada por pacientes con distintos tipos de DCF

como los siguientes, cefalea tensional, migraña, cefalea atribuida a TCM, artralgia y

dolor miofascial. Los criterios de inclusión fueron los siguientes: a) pacientes mayores

de 18 años; b) diagnóstico de dolor facial o cefalea de acuerdo a los criterios de la

Clasificación Internacional de las Cefaleas (IHS, 2013); c) diagnóstico de TCM de

acuerdo a los Criterios diagnósticos de investigación para TCM; (Dworkin and

LeResche, 1992; Schiffman et al., 2010); d) presencia de los síntomas dolorosos de más

de 6 meses; y e) buena compresión del idioma español. Los criterios de exclusión

adoptados en este estudio fueron los siguientes: a) dificultad en la compresión del

idioma español; b) deterioro cognitivo; y trastornos psiquiátricos.

El estudio V fue conformado por pacientes con cefalea atribuida a TCM de acuerdo a

los criterios de la Clasificación Internacional de las Cefaleas (IHS, 2013) y los criterios

clínicos y de investigación para TCM (Schiffman et al., 2014), además se incluyeron

los siguientes criterios de inclusión: a) presencia de dolor superior a 6 meses; b) dolor

en mandíbula, zona temporal, cara y cuello en reposo o en movimiento; c) ser mayor de

18 años; y d) discapacidad de cuello cuantificado de acuerdo al índice de discapacidad

cervical (IDC) (Andrade Ortega et al., 2010), por otra parte se debe mencionar que en

este estudio los pacientes se subdividieron de acuerdo a los niveles de discapacidad

cervical según el IDC (discapacidad leve y moderada) (Andrade Ortega et al., 2010).

Los criterios de exclusión adoptados en estos estudios fueron los siguientes: a) TCM

atribuidos a disfunciones articulares o enfermedades degenerativos de acuerdo los

62

Criterios diagnósticos de investigación para TCM (Dworkin and LeResche, 1992;

Schiffman et al., 2010); b) lesiones traumáticas como fracturas o latigazo cervical; c)

enfermedades sistémicas reumatológicas como fibromialgia y artritis; c; dolor

neuropático; d) concomitancia con cefaleas primarias; e) dolor de cuello unilateral; f)

procedimientos quirúrgicos previos en la región cervical; y g) radiculopatía cervical.

Los estudios II y VII contaron con una muestra de pacientes con DCCF crónico, estos

pacientes integran clínicamente una comorbilidad entre el dolor de cuello crónico

mecánico inespecífico (descrito en estudio III) y TCM atribuido a dolor miofascial

(descrito en los estudios I y VI). Definimos DCCF como un dolor de origen muscular

que presenta mecanismos disfuncionales como limitación del movimiento, movimientos

in-coordinados y debilidad y falta de resistencia en el cuello y la mandíbula, estos

síntomas pueden exacerbarse con posturas mantenidas generando dolor en la región

cervical y craneofacial. Los criterios de exclusión adoptados en estos estudios fueron los

mismos que en los estudios I, III y VI.

También es importante destacar que en los estudios II, III y V se realizaron

comparaciones con participantes asintomáticos.

4.2 Variables y Pruebas de Medición

En todos los estudios se registraron diversos tipos de variables sociodemográficas como

la edad, peso, altura, sexo y la duración de los síntomas, además en el estudio V se

cuantifico el nivel de estudios y el estado laboral. A parte de las variables

sociodemográficas en los estudios también se evaluaron variables somatosensoriales,

motoras y psicológicas mediante la utilización de diversos instrumentos y otras

herramientas de auto-registro especializadas. En la tabla 3 se presenta un resumen de la

variables e instrumentos de medición utilizadas en cada estudio.

Tabla 3. Variables e instrumentos utilizados en los estudios.

63

Variables Medidas Estudios

I II III IV V VI VII

Intensidad del dolor

a. Escala visual

analógica del dolor

b. Escala numérica de

dolor

X-a X-b X-a X-a X-a

Máxima apertura interincisal a. Escala therabite

b. Escala CMD

c.

X-a X-b X-a

Umbral de dolor a la presión Algométro

X X X X X

Postura craneocervical a. Distancia mentón

esternón medido con

un calibre digital.

b. Postura de cabeza

medido con CROM

X-ab

Percepción de fatiga Escala visual analógica de fatiga

X

Discapacidad cervical Índice de discapacidad cervical

X X X X X

Discapacidad craneofacial y

función mandibular

Inventario de dolor y

discapacidad craneofacial

X X

Síntomas depresivos Inventario de depresión Beck

X

Estado de ansiedad Cuestionario de ansiedad

estado/rasgo

X X

Miedo al movimiento Escala Tampa de Kinesiofobia

X

Catastrofismo ante el dolor Escala de catastrofismo ante el

dolor

X X

Impacto de la cefalea en la

vida diaria

Cuestionario de impacto de la

cefalea HIT-6

X X

64

4.2.1 Medidas de auto-registro

Catastrofismo ante el Dolor

Se utilizó la versión española de la escala de catastrofismo ante el dolor (ECD) para

evaluar el nivel de catastrofismo (García Campayo et al., 2008). La ECD está

compuesta por 13 ítems, cada ítem puntúa del 0 al 4. El rango de puntuación total se

encuentra de 0 a 52, donde puntuaciones mayores indican mayor nivel de catastrofismo.

Este instrumento presentó la misma estructura factorial original presentando tres

factores (rumiación, magnificación y desesperanza), así como unas adecuadas

propiedades psicométricas (García Campayo et al., 2008).

Miedo al Movimiento

La versión en español de la escala Tampa de kinesiofobia (TSK-11) mide el miedo al

dolor y al movimiento (Gómez-Pérez et al., 2011). La TSK-11 contiene 11 ítems en su

versión española, tras el análisis factorial se eliminaron algunos ítems de la versión

original que fueron psicométricamente pobres (Gómez-Pérez et al., 2011; Kori et al.,

1990). La puntuación total del TSK-11 se encuentra entre 11 – 44 puntos y cada ítem

presenta una escala likert que puntúa del 1 al 4 (1 = totalmente en desacuerdo, 4 =

totalmente de acuerdo). Puntuaciones más altas indican mayor miedo al movimiento y

al dolor. El TSK-11 tiene dos sub-escalas: evitación de actividad y daño, además esta

escala ha demostrado aceptables propiedades psicométricas (Gómez-Pérez et al., 2011).

Intensidad del Dolor

La intensidad del dolor se midió con la escala visual analógica del dolor (EVA). La

EVA consiste en una línea de 100 mm, en el que el lado izquierdo representa "ningún

dolor" y el lado derecho "el peor dolor imaginable". Los pacientes colocan una marca

donde se sentían que representan la intensidad del dolor. Se ha comprobado que este

instrumento tiene una buena fiabilidad (Bijur et al., 2001).

65

En la medición de la intensidad del dolor también se utilizó la escala numérica del dolor

(END), esta escala presenta 11 puntos posibles representados en números del 0 (sin

dolor) al 10 (máximo dolor). Se ha demostrado que END presenta una buena fiabilidad

y validez en pacientes crónicos (Jensen and McFarland, 1993; Jensen et al., 1999).

Percepción de Fatiga

La escala visual analógica de fatiga (EVAF) se utilizó para cuantificar la fatiga

percibida. La EVAF consiste en una línea vertical de 100 mm en la que la parte inferior

representa "ninguna fatiga" (0 mm), y la parte superior representa la "fatiga máxima"

(100 mm). El investigador registra el resultado en mm. Se ha comprobado que este

instrumento tiene una buena fiabilidad (Tseng et al., 2010).

Discapacidad Cervical

La versión española del índice de discapacidad cervical (IDC) es instrumento utilizado

para evaluar la discapacidad percibida en relación a la dolencia en el cuello (Andrade

Ortega et al., 2010; Vernon and Mior, 1991). Este cuestionario consta de 10 ítems, con

6 posibles respuestas que representa 6 niveles de capacidad funcional, que van desde 0

(sin discapacidad) a 5 (discapacidad total) puntos. Las puntuaciones más altas indican

mayor discapacidad percibida. El IDC ha demostrado propiedades psicométricas

aceptables (Andrade Ortega et al., 2010).

Impacto de la Cefalea en la Vida Diaria

La versión española del HIT-6 (Bjorner et al., 2003; Gandek et al., 2003) consiste en un

cuestionario de seis ítems que evalúa la gravedad y el impacto del dolor de cabeza en la

vida del paciente. Los resultados de HIT-6 están estratificados en cuatro clases basadas

en el grado de impacto: poco o ningún impacto (HIT-6 puntuación de: 36-49), impacto

moderado (HIT-6 puntuación de: 50-55), impacto sustancial (HIT-6 puntuación de: 56-

59), y el impacto severo (HIT-6 puntuación de: 60-78) (Bjorner et al., 2003). El HIT-6

66

ha demostrado propiedades psicométricas aceptables (Martin et al., 2004).

Síntomas de Ansiedad

La versión española del cuestionario de ansiedad estado-rasgo (STAI) es una medida de

auto-informe de 40 ítems, diseñado para evaluar los síntomas de la ansiedad (Spielberg

and Lushene, 1982). Consta de 2 escalas independientes, una escala de ansiedad estado

y una escala de ansiedad rasgo, con 20 puntos cada uno, lo que resulta en una

puntuación entre 20 y 80. Superiores puntuaciones indican un mayor nivel de ansiedad.

Las escalas de estado y rasgo evalúan la ansiedad como un estado emocional actual y

como un rasgo de la personalidad, respectivamente. El STAI ha demostrado

propiedades psicométricas aceptables en su versión en español (Spielberg and Lushene,

1982).

Síntomas Depresivos

Los síntomas depresivos se evaluaron con el Inventario de Depresión Beck (BDI-II),

este instrumento de auto-registro evalúa síntomas afectivos, cognitivos y somáticos de

depresión. Se ha comprobado en estudios con población general y clínica que el BDI-II

presenta adecuadas propiedades psicométricas (Penley et al., 2003; Wiebe and Penley,

2005)

4.2.2 Instrumentos de medición

Máxima Apertura Interincisal

La máxima apertura interincisal (MAI) es la capacidad de abrir la boca tan amplio

como se pueda sin dolor. Esta distancia se mide en milímetros entre el incisivo superior

y el incisivo inferior. La MAI se midió con la escala TheraBite (Model CPT 95851;

Atos Medical AB; Sweden) y con la escala craneomandibular (Escala CMD. Patente.

No. ES 1075174 U, INDCRAN: 2011. INDCRAN, Madrid, Spain) (Figura 12). El

procedimiento para medir la MAI ha demostrado una buena fiabilidad inter-evaluador

67

(ICC = 0,95 - 0,96) (Beltran-Alacreu et al., 2014).

Figura 12. Medición de máxima apertura interincisal con la escala CMD.

Umbral de Dolor a la Presión

Un algómetro digital (FDX 25, Wagner Instruments, Greenwich, CT, EE.UU.),

compuesto por un cabezal de goma (1 cm2) unido a un manómetro, se utilizó para medir

UDPs (Figura 13). La presión ejercida se mide en kilogramos (kg); por lo tanto, los

UDPs se expresaron en kg /cm2. El protocolo utilizado fue una secuencia de 3

mediciones, con un intervalo de 30 segundos entre cada una de las mediciones. Un

promedio de las 3 mediciones se calculó para obtener un único valor para cada uno de

los puntos medidos en cada una de las evaluaciones. Los UDPs se evaluaron en varios

puntos de la región craneofacial y craneomandibular (Figura 14). El dispositivo se

aplica perpendicular a la piel. Se pidió a los pacientes que levantasen la mano en el

momento en que la presión comenzara a cambiar a una sensación de dolor, y en ese

momento el evaluador dejó de aplicar presión. La presión aplicada en la prueba se

aumentó gradualmente a una velocidad de aproximadamente 1 kg/s. Este procedimiento

de algometría tiene alta fiabilidad intra-evaluador (ICC = 0,94 a 0,97) para la medición

68

de los UDPs (Walton et al., 2011).

Figura 13. Medición del umbral de dolor a la presión con el algómetro digital.

Figura 14. Puntos de áreas trigeminales y cervicales en donde se midieron los umbrales de dolor a la presión en los

diferentes estudios.

Postura Craneocervical

Utilizamos el dispositivo CROM para medir la postura de cabeza (PC). Este dispositivo

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tiene tres partes: a) una estructura plástica con forma de gafas; b) tres inclinómetros,

uno para cada plano de movimiento; y c) un brazo plástico para medir la de cabeza

hacia adelante y un localizador de vértebra (Figura 15). La medición de la PC está

graduada en el instrumento en 0,5 cm, que indican la distancia horizontal entre el puente

de la nariz y el localizador de vértebras. El localizador de vértebras tiene un nivel de

burbuja en la parte superior para ayudar a la colocación exacta. Los inclinómetros no se

utilizaron debido a los movimientos del cuello no se evaluaron.

Figura 15. Medición de la postura craneocervical

Para medir la distancia mentón-esternón (DME) se utilizó un calibre digital. El

dispositivo está hecho de plástico con una pantalla LCD de 5 dígitos y se puede medir

en pulgadas o en milímetros (mm) con un rango de 0,01 mm a 150 mm.

El evaluador explica en primer lugar que la medición se llevará a cabo mientras está

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acostado en una camilla. En este momento, el evaluador mostró los calibradores

digitales al tema y dijo: "Usted sentirá que el instrumento contactará con su esternón y

en la barbilla; en ese momento no se debe mover”. Una vez en su lugar, la medición fue

tomada de la escotadura yugular del esternón a la protuberancia de la barbilla (Figura

16). La medida fue tomada en dos ocasiones.

Figura 16. Medición de la distancia mentón-esternón.

4.3 Resumen de los Procedimientos

Estudio I

Se registraron inicialmente las variables sociodemográficas y la intensidad del dolor y

después se procedió a medir los UDPs y la MAI en tres posturas craneocervicales

inducidas experimentalmente (posición neutra craneocervical, retracción craneocervical

y protracción craneocervical)

Estudio II

Se seleccionaron a los pacientes y los sujetos asintomáticos del grupo control, después

se registraron las variables sociodemográficas y las medidas de auto-registro (IDC y

IDD-CF) y finalmente se realizaron las mediciones de la postura craneocervical.

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Estudio III

Se registraron las variables sociodemográficas y las medidas de auto-registro y después

se procedió a realizar mediciones del UDP en los puntos trigeminales.

Estudio IV

Se seleccionaron a los pacientes y después se procedió a registrar las variables

sociodemográficas y una batería de medidas de auto-registro de variables psicológicas,

dolor y discapacidad.

Estudio V

Una vez seleccionados los pacientes y el grupo control se procedió al registro de

variables sociodemográficas y las medidas de auto-registro, después de esa fase se

realizó el test masticatorio de provocación durante 6 minutos en donde se evaluó la

fatiga y la intensidad del dolor. Al finalizar el test masticatorio de provocación se

procedió a realizar las mediciones de la MAI y los UDPs.

Estudio VI

Se realizó un tratamiento sobre los pacientes seleccionados durante 10 sesiones, este

tratamiento estaba enfocado a la región cervical y específicamente se utilizó un

protocolo de estabilización cervical y un tratamiento de terapia manual sobre la región

cervical, además se realizaron mediciones de variables somatosensoriales y motoras

pre-intervención, post-intervención y tres meses después.

Estudio VII

Se seleccionaron un grupo de pacientes que se subdividen aleatoriamente en dos grupos,

un grupo recibe un tratamiento placebo y el otro un tratamiento manual sobre la región

cervical superior. Se realizaron mediciones de variables somatosensoriales y del sistema

nervioso simpático pre-intervención y post-intervención.

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4.4 Análisis Estadístico

En el análisis de datos se ha utilizado estadística descriptiva para mostrar los datos de

las variables continuas que se presentan como media ± desviación típica (DT), intervalo

de confianza del 95% (IC) y frecuencia relativa (porcentaje). Prueba de Chi-cuadrado,

se utilizó para comparar las diferencian entre las variables categóricas (nominales). Se

realizo la prueba de Kolmogorov Smirnov para comprobar la normalidad.

Se utilizó la t de Student para la comparar las variables continuas entre los dos grupos.

Cuando las comparaciones se realizaron con más de dos grupos o se intentó analizar la

interacción con otras variables se aplicó una ANOVA de una, dos o tres vías según

procediese, seguido de un test post hoc de Bonferroni para analizar las comparaciones

múltiples. En uno de los estudios se realizó un análisis con una ANCOVA de dos vías

para identificar múltiples interacciones entre variables.

Se calculó el tamaño del efecto (d de Cohen) para las variables principales estudiadas.

De acuerdo con el método de Cohen, la magnitud del efecto fue considerado como

pequeño (0,20 a 0,49), medio (0,50 a 0,79), y grande (0,8) (Cohen, 1988).

La estructura factorial se analizó mediante un análisis factorial exploratorio (es decir,

análisis de componentes principales, ACP) con la rotación Oblimin. El número de

factores para la extracción se basa en el criterio de valor propio de Kaiser (valor propio

≥1) y la evaluación del gráfico de sedimentación (Ferguson and Cox, 1993). La calidad

de los modelos de análisis factorial se evaluó mediante la prueba de Bartlett para la

esfericidad y la prueba de Kaiser-Meyer-Olkin (KMO). Prueba de Bartlett es una

medida de la probabilidad de que la matriz de correlación inicial es una matriz de

identidad y debe ser <0,05 (Bartlett, 1954). La prueba de KMO mide el grado de

multicolinealidad y varía entre 0 y 1 (debe ser mayor que 0,50-0,60) (Kaiser, 1974).

El efecto suelo-techo se midieron mediante el cálculo del porcentaje de pacientes que

73

indican los puntajes mínimos y máximos posibles en los cuestionarios. El efecto suelo-

techo se considera que está presente si más del 15% de los encuestados logró el mayor o

menor puntuación total posible (Terwee et al., 2007).

La fiabilidad intra e inter-evaluador se analizo mediante coeficiente de correlación intra-

clase (CCI). Niveles de fiabilidad se definieron en base a la siguiente clasificación:

buena fiabilidad: ICC ≥ 0,75; fiabilidad moderada: ICC ≥ 0,50 y <0,75; y escasa

fiabilidad: ICC <0,50 (Portney LG, 2009).

El error de medición se expresa como un error estándar de medición (EEM), que se

calcula como 𝐷𝑇 × √1 − 𝐶𝐶𝐼, donde DT es la de los valores de todos los participantes,

y el CCI es el coeficiente de fiabilidad (Weir, 2005). El error de medición es el error

sistemático y aleatorio de la puntuación de un paciente que no es atribuible a los

cambios reales en el constructo a medir (Mokkink et al., 2010). Capacidad de respuesta

se evaluó utilizando el mínimo cambio detectable (MCD). MCD expresa el cambio

mínimo necesario para identificar el 90% de confianza de que el cambio observado

entre las dos medidas refleja un cambio real y no un error de medición (Haley and

Fragala-Pinkham, 2006). Se calcula como 𝐸𝐸𝑀 × √2 × 1,96 (Haley and Fragala-

Pinkham, 2006).

La asociación entre las variables se determinó mediante el coeficiente de correlación de

Pearson. Un coeficiente de correlación de Pearson mayor que 0,60 indica una fuerte

correlación, un valor entre 0,30 y 0,60 indica una correlación moderada, y uno por

debajo de 0,30 indica una correlación baja o muy baja (Hinkle et al., 1988). También se

utilizó en uno de los estudios el coeficiente de correlación de Spearman.

Se realizó un análisis de regresión lineal múltiple para estimar la fuerza de las

asociaciones entre los resultados variables primarias (variables criterio) con las

secundarias (variables predictoras). Se calcularon los factores de inflación de varianza

74

(FIV) para determinar si existían problemas de multicolinealidad en cualquiera de los

modelos analizados.

La fuerza de asociación se examinó utilizando los coeficientes de regresión (β), los

valores de P y r2 ajustado. Coeficientes beta estandarizados fueron reportados para cada

variable de predicción incluida en los modelos finales reducidas para permitir una

comparación directa entre las variables predictoras en el modelo de regresión y la

variable criterio que se está estudiando. Para el análisis de regresión, se utilizó la regla

de 10 casos por variable con el fin de obtener estimaciones razonablemente estables de

coeficientes de regresión (Peduzzi et al., 1996).

En la tabla 4 se presenta un resumen de los test estadísticos utilizados en cada uno de

los estudios.

El programa estadístico para Ciencias Sociales (SPSS 21, SPSS Inc., Chicago, IL

EE.UU.) se utilizó para el análisis estadístico. El nivel de significación para todas las

pruebas se estableció a un nivel de P <0,05.

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Tabla 4. En esta tabla se puede observar las pruebas estadísticas utilizadas en cada uno

de los estudios.

Pruebas estadísticas Estudios

I II III IV V VI VII

- Análisis descriptivo X X X X X X X

- Pruebas de normalidad (test de Kolmogorov Smirnov) X X X X X X X

- t de student X X X

- ANOVA X X X X X

- ANCOVA X

- Calculo del tamaño del efecto (d) X X

- Análisis factorial exploratorio X

- Efecto suelo-techo X

- Coeficiente de correlación intra-clase X X X

- Error estándar de medición X X X X

- Mínimo cambio detectable X X

- Coeficiente de correlación de Pearson X X X

- Coeficiente de correlación de Spearman X

- Análisis de regresión lineal múltiple X X

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77

RESULTADOS

78

5. RESULTADOS

5.1 Estudio I

La Touche R, París-Alemany A, von Piekartz H, Mannheimer JS, Fernández-Carnero J,

Rocabado M. The influence of cranio-cervical posture on maximal mouth opening and

pressure pain threshold in patients with myofascial temporomandibular pain disorders. Clin

J Pain. 2011 Jan;27(1):48-55.

Objetivo del estudio

El objetivo de este estudio fue evaluar la influencia de la postura craneocervical sobre la

MAI y el UDP en pacientes TCM atribuidos a dolor miofascial.

Resultados

Las comparaciones indicaron diferencias significativas en los UDPs de los 3 puntos

musculares con inervación trigeminal [masetero (M1 y M2) y temporal anterior (T1)] entre

las 3 posturas de cabeza [M1 (F = 117.78, p <0,001), M2 (F = 129.04, p <0,001), y T1 (F =

195,44, p <0,001)]. También hubo diferencias significativas en la MAI medidas en las 3

posturas de cabeza (F = 208.06, p <0,001). La fiabilidad intra-evaluador en base a pruebas

realizadas día a día fue buena, presentando un coeficiente de correlación intra-clase en los

rangos de 0,89-0,94 y 0,92 hasta 0,94 para UDP y la MAI, respectivamente, entre las

diferentes posturas craneocervicales.

Conclusiones

Los resultados de este estudio muestran que la inducción experimental de diferentes

posturas craneocervicales influye en los valores de la MAI y los UDPS de la ATM y

músculos de la masticación que reciben inervación motora y sensitiva por el nervio

trigémino. Nuestros resultados proporcionan información que respalda la relación

biomecánica entre la región craneocervical y la dinámica de la ATM, así como las

modificaciones en el procesamiento nociceptivo trigeminal en diferentes posturas

craneocervicale.

The Influence of Cranio-cervical Posture on Maximal MouthOpening and Pressure Pain Threshold in Patients With

Myofascial Temporomandibular Pain Disorders

Roy La Touche, PT, MSc,*w z Alba Parıs-Alemany, PT, MSc,w Harry von Piekartz, PT, PhD,yJeffrey S. Mannheimer, PT, PhD, CCTT,J Josue Fernandez-Carnero, PT, PhD,w z

and Mariano Rocabado, PT, DPT#

Objective: The aim of this study was to assess the influence ofcranio-cervical posture on the maximal mouth opening (MMO)and pressure pain threshold (PPT) in patients with myofascialtemporomandibular pain disorders.

Materials and Methods: A total of 29 patients (19 females and 10males) with myofascial temporomandibular pain disorders, aged19 to 59 years participated in the study (mean years±SD;34.69±10.83 y). MMO and the PPT (on the right side) of patientsin neutral, retracted, and forward head postures were measured. A1-way repeated measures analysis of variance followed by 3 pair-wise comparisons were used to determine differences.

Results: Comparisons indicated significant differences in PPT at 3points within the trigeminal innervated musculature [masseter (M1and M2) and anterior temporalis (T1)] among the 3 head postures[M1 (F=117.78; P<0.001), M2 (F=129.04; P<0.001), and T1(F=195.44; P<0.001)]. There were also significant differencesin MMO among the 3 head postures (F=208.06; P<0.001). Theintrarater reliability on a given day-to-day basis was good with theinterclass correlation coefficient ranging from 0.89 to 0.94 and 0.92to 0.94 for PPT and MMO, respectively, among the different headpostures.

Conclusions: The results of this study shows that the experimentalinduction of different cranio-cervical postures influences the MMOand PPT values of the temporomandibular joint and musclesof mastication that receive motor and sensory innervation by thetrigeminal nerve. Our results provide data that supports thebiomechanical relationship between the cranio-cervical region andthe dynamics of the temporomandibular joint, as well as trigeminalnociceptive processing in different cranio-cervical postures.

Key Words: temporomandibular disorders, myofascial pain, posture,

cervical spine, orofacial pain

(Clin J Pain 2011;27:48–55)

Pain in the masticatory muscles and arthralgia of thetemporomandibular joints are some of the features of

the term temporomandibular disorders (TMD) that havebeen categorized into 3 major groups by the ResearchDiagnostic Criteria (RDC) that is most commonly used toclassify symptomatology of TMD.1,2 Myofascial pain, discdisplacements, and arthralgia/osteoarthrosis constitute thisdiagnostic grouping. TMD of myofascial origin is categor-ized by episodic pain with periods of exacerbation andremission.3 Nevertheless, some patients may suffer persis-tent pain, and their prognosis is determined by psycho-metric evaluation (Axis II of the RDC/TMD). Myofascialpain is frequently associated with the presence of triggerpoints (TrPs) and the discomfort is considered to representa taut and painful disturbance of muscle and fascia that canbe local or referred with tenderness and pressure uponpalpation.4,5

It is well known that cervical spine tissues can referpain to the head and orofacial region.6,7 Comorbidity ofTMD and cervical spine disorders is quite common andconsists of a composite of functional limitation, pain,tender points, and hyperalgesia indigenous to the upperquarter.8 Some authors believe that neuronal plasticity,local interactions, and general predisposing musculoskeletalfactors might be behind this coexistence, but the relation-ship between the orofacial and cervical region is stronglyrooted by dense neuromusculoskeletal and neurophysiolo-gic connections.8,9 The trigeminal brainstem sensorynuclear complex located within the suboccipital spine,represents the prime neurophysiologic region where theconvergence of sensory information from the first 3 cervicalspinal nerves converge with trigeminal afferents, whereassome fibers descend to lower segmental levels.10–15 There-fore ascending cervicogenic and descending trigeminalreferral is mediated through the trigeminal brainstemsensory nuclear complex.15,16 The convergence of differenttypes of afferent and efferent neurotransmission on thetrigeminal nucleus together with the good evidence forneuronal plasticity that is known to occur in chronic painstates17–19 may account for the concomitant pain anddysfunction of the cervical, temporomandibular joints, andmasticatory system because of changes in head posture.17,20

Forward positioning of the head may contribute toor occur concomitantly with TMD,21,22 cervicogenic head-ache,23 and tension-type headache.24 Some authors supportthe connection between TMD and head posture,20–22,25

whereas others do not.26,27 The mechanism whereby headposture might be related to craniofacial signs and symptomsis unclear. The neuroplastic changes associated withCopyright r 2010 by Lippincott Williams & Wilkins

Received for publication April 7, 2010; revised June 9, 2010; acceptedJune 14, 2010.

From the *School of Health Science, Department of Physical Therapy;wGroup for Musculoskeletal Pain and Motor Control ClinicalResearch; zOrofacial Pain Unit of the Policlınica Universitaria,Universidad Europea de Madrid, Villaviciosa de Odon; zDepart-ment of Physical Therapy, Occupational Therapy, Rehabilitationand Physical Medicine, Universidad Rey Juan Carlos, Alcorcon,Madrid, Spain; yFaculty of Business, Management and SocialScience, University of Applied Science Osnabruck, Osnabruck,Germany; JProgram in Physical Therapy, Columbia University,New York, NY; and #Faculty of Rehabilitation Science, UniversidadAndres Bello, Santiago, Chile.

Reprints: Roy La Touche, PT, MSc, Facultad de Ciencias de la Salud/Departamento de Fisioterapia, Universidad Europea de Madrid,C/Tajo s/n, 28670 Villaviciosa de Odon, Madrid, Espana (e-mail:[email protected]).

ORIGINAL ARTICLE

48 | www.clinicalpain.com Clin J Pain � Volume 27, Number 1, January 2011

convergent afferent inputs mentioned above might play aconsiderable role. Further, it is noteworthy that changes inhead posture can alter the position of the mandible28,29 andthe activity of the masticatory muscles.30 Higbie et al31

demonstrated increased mouth opening in a forward headposition as compared with the neutral or retracted headposition, in healthy individuals. Furthermore, postural anddeep cervical flexor training as well as cervical manualtherapy have been shown to improve TMD signs andsymptoms.21,32,33

Although Visscher et al27 did obtain a wide rangeof head postures in both patients with craniomandibulardysfunction and healthy ones, their results data did notsupport the suggestion that craniomandibular dysfunctionis related to abnormal head posture, even in the presence ofcervical spine dysfunction. On the basis of their findings,Olivo et al34 found that the association between head andcervical posture with intra-articular or muscular TMD isnot clear.

Given the conflict in the literature as to whether thereis an association between head posture might be relatedto craniofacial signs and symptoms; the aim of this study isto assess the influence of cranio-cervical posture on themaximal mouth opening (MMO) and pressure pain thresh-old (PPT) of the trigeminal region in patients withmyofascial TMD pain.

MATERIALS AND METHODS

PatientsTMD patients were recruited from November 2008 to

March 2009 and were referred from 3 private dental clinicsin Madrid, Spain. Patients were selected if they met all ofthe following criteria: (1) a primary diagnosis of myofascialpain as defined by the Axis I, category Ia and Ib (ie,myofascial pain with or without limited opening), of theRDC/TMD,2 (2) bilateral pain involving the masseter andtemporalis, (3) a duration of pain of at least 6 months, (4) apain intensity corresponding to a weekly average of at least30mm on a 100mm visual analog scale, and (5) a presenceof bilateral TrPs in both the masseter and temporalismuscles diagnosed following the criteria described bySimons et al.35 TrPs were diagnosed according to thefollowing criteria: (1) presence of a palpable taut band inskeletal muscle, (2) presence of a hypersensitive tender spotwithin the taut band, (3) local twitch response elicited bythe snapping palpation of the taut band, and (4) reproduc-tion of referred pain in response to TrP compression. Thesecriteria have shown good interrater reliability (k) rangingfrom 0.84 to 0.88.36

All patients included in the study were examined byan experienced TMD specialist, with more than 4 years ofclinical practice, from the University Center of ClinicalResearch of the Cranial-Cervical-Mandibular System,Faculty of Medicine, San Pablo CEU University.

Patients were excluded if they presented any signs,symptoms, or history of the following diseases: (1) intra-articular disc displacement, ostheoarthrosis, or arthritis ofthe temporomandibular joint (TMJ), according to cate-gories II and III of the RDC/TMD2; (2) history of trauma-tic injuries (eg, contusion, fracture, and whiplash injury);(3) systemic diseases: (fibromyalgia, systemic lupus erythe-matosus, and psoriatic arthritis); (4) neurologic disorders(eg, trigeminal neuralgia); (5) concomitant diagnosis ofany primary headache (tension type or migraine); and

(6) current or recent therapy for the disorder within theprevious 2 months.

Each participant received a thorough explanationabout the content and purpose of the treatment beforesigning an informed consent relative to the procedures. Allprocedures were approved by the local ethics committee inaccordance with the Helsinki Declaration.

Experimental ProceduresEach patient with myofascial TMD pain were

subjected to a protocol for assessing maximum activeopening and PPT in 3 different cranio-cervical postures asfollows and illustrated in Figure 1:

Neutral head posture (NHP) defined as the positionassumed when the individual was told to sit and maintaintheir head in a vertical position. This position was furtherconfirmed as neutral if the tragus of the ear and acromionwere bisected by a plumb line.Forward head posture (FHP) defined as anteriortranslation of the head with or without lower cervicalflexion. It is claimed that the FHP is associated with anincrease in upper-cervical extension.37,38

Retracted head posture (RHP) defined as posteriortranslation of the head over the trunk associated withupper cranio-cervical flexion and extension of the low-to-mid cervical spine.39

All measurements were conducted by 2 physiothera-pists who had experience in research evaluations, one incharge of placing the patient in the measurement positionand the other responsible for the recording of MMOand PPT. All patients underwent 3 measurements of eachvariable in the 3 head positions on 3 different days. Awashout period of 24 hours was incorporated between eachmeasurement day.

A software program was used to obtain blockedrandomization of the size to arrange the order of measure-ment (GraphPad Software, Inc, CA). An average of 15minutes per patient was required to perform the random-ized measurements of MMO and PPT in NHP, FHP, andRHP. Every patient maintained their head in each positionfor 5 seconds during these measurements.

Establishment of the Measurement PositionsA plumb line hanging from the ceiling and a cervical

range of motion (CROM) device (Performance AttainmentAssociates, 958 Lydia DR, Roseville, MN) was usedto determine each patients’ cranio-cervical postures. TheCROM instrument measured the degree of FHP or RHPand the active cervical range of movement. The CROMinstrument uses a clear plastic eyeglass-like frame with 2dial-angle meters, a head arm that includes a vertebrallocator and bubble leveller (Fig. 2). The head arm wasplaced in the frame of the CROM horizontally to the head.The base of the vertebral locator was placed on the C-7spinous process so that the bubble leveller was centeredwithin the 2 vertical lines on the dial with the examinerstanding to the left of the patient to read the sagittal planemeter (Fig. 2). When the sagittal plane meter read zero andwith the head arm horizontal (parallel to the floor), theintersection of the head arm and vertebral locator wasrecorded as the head posture measurement in centimeters.Excellent reliability has been showed for the measurementof FHP using the CROM instrument [intrarater reliability

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r 2010 Lippincott Williams & Wilkins www.clinicalpain.com | 49

(interclass correlation coefficient, ICC=0.93) and interraterreliability (ICC=0.83)].40

Cranio-cervical postures were measured in the sittingposition attained by instructing the patient to sit in acomfortable upright position with the thoracic spine incontact with the back of the chair. The feet were positionedflat on the floor with knees and hips at 90 degrees and armsresting freely alongside.

Forward and retruded head postures were achieved byinitial placement into the NHP using the plumb line asexplained earlier. Movement into a FHP was performedwith the CROM after verbal instruction to position thehead forward in a horizontal plane allowing the tragus to bealigned to a target plumb line placed 8 cm anterior to thebase plumb line. Each patient was instructed to continuallymaintain their eyes at the same horizontal level while being

told to “slide your jaw and head forward until the examinertells you to stop” upon reaching the target plum line (Fig. 1).

Movement into a RHP was also performed with theCROM by instruction to position the head posteriorly ina horizontal plane allowing the tragus to be aligned to thetarget plumb line placed 4 cm posterior to the base plumbline. Each patient was instructed to continually maintaintheir eyes at the same horizontal level while being told to“slide your jaw and head backward until the examiner tellsyou to stop” upon reaching the target plum line (Fig. 1).

Measurement of MMOThe MMO was measured with a TheraBite range of

motion scale (Model CPT 95851; Atos Medical AB;Sweden) (Fig. 2). The patients were told to: “Open yourmouth as wide as possible without causing pain or

FIGURE 1. Measurement of maximum mouth opening with TheraBite, controlling the head position with the CROM device and plumline: A, retracted head posture. B, Forward head position. Measurement of pressure pain thresholds at masseter and temporalis muscleswith a mechanical algometer, controlling head position with CROM device: C, forward head position. D, Neutral head position. CROMindicates cervical range of motion.

FIGURE 2. Description and representation of measurement devices: TheraBite scale (A); CROM device: plastic eyeglass-like frame with 2dial-angle meters (B), head arm (C), and vertebral locator and bubble leveller (D).

La Touche et al Clin J Pain � Volume 27, Number 1, January 2011

50 | www.clinicalpain.com r 2010 Lippincott Williams & Wilkins

discomfort.” Interincisal distance was then recorded byplacing one end of the TheraBite scale against the incisaledge of one central mandibular incisor with the other endagainst the incisal edge of the opposing maxillary centralincisor (Fig. 1). Earlier research has shown excellentintrarater (0.92 to 0.97) and interrater (0.92 to 0.93)reliability when assessing MMO in 3 different cranio-cervical positions.33

Measurement of PPTThe PPT was defined as the amount of pressure that

a patient would initially perceive as painful.41 PPTs havebeen assessed with a mechanical pressure algometer (PainDiagnosis and Treatment Inc, Great Neck, NY) whichwas used in this study. The instrument consists of a 1 cmdiameter hard rubber tip, attached to the plunger of apressure (force) gauge. The dial of the gauge is calibratedin kg/cm2 and the range of the algometer is 0 to 10 kgwith 0.1 kg divisions. Earlier research has shown that thereliability of pressure algometry is as high as [ICC=0.91(95% confidence interval, CI 0.82-0.97)].42

Before the evaluation, 3 specific cutaneous regionsoverlying the masseter and temporalis were marked with apencil. Algometric measurements were then performed at 2masseteric sites and 1 temporalis site as delineated by:masseter muscle (M1 and M2) and temporalis muscle (T1)(Fig. 3). During the measurements, the algometer was heldperpendicular to the skin (Fig. 1) and the patient was toldto immediately alert the assessor when the pressure turned

into a sensation of pain, at which point the mechanicalstimulus was stopped. Three consecutive measurementswere obtained by the same assessor, with a pause of 30seconds between measurements. The mean of 3 measureswas calculated and used for analysis. All measurementswere performed on the right side because of the disturbanceinduced by the dial-angle meter of the CROM at the leftside (Fig. 1).

Statistical AnalysisData are expressed as mean, SD, and 95% CI. The

Kolmogorov-Smirnov test was used to determine the normaldistribution of the variables (P<0.05). A 1-way repeatedmeasures analysis of variance (ANOVA) followed by 3 pair-wise comparisons was used to determine differences in MMOand PPT among the 3 different head postures. Post-hoccomparisons were conducted with the Bonferroni test.Intrarater reliability of repeated measures was determinedfrom the ICC by means of the 2-way model, the 95% CI,and the standard error of the measurement (SEM). Thestrength of the ICC was interpreted as <0.50=poor; 0.50<0.75=moderate; 0.75 <0.90=good; and >0.90=excel-lent. The ICC and SEM convey different information aboutreliability of a measure. The analysis was conducted at 95%CI and P value less than 0.05 was considered to bestatistically significant. Statistical analyses were carried outusing the Statistical Package for Social Sciences, Version 15.0(SPSS, Chicago, IL).

RESULTSThe general demographic data and pain-related data

are shown in Table 1. Figure 4 represents the study samplesize and the reasons for exclusion of the patients. All thepatients who started the study were analyzed, and therewere no dropouts or losses.

FIGURE 3. Pressure pain threshold measurement sites attemporalis and masseter muscles. T1: located 3 cm above theline between the lateral edge of the eye and the anterior part ofthe helix on the anterior fibers of temporalis muscle. M1: located2.5 cm anterior to the tragus and 1.5 cm inferiorly. M2: located1 cm superior and 2 cm anterior from the mandibular angle.

TABLE 1. General Data of the Analyzed Patients

Demographic and Clinical Data Mean SD

Age (y) 34.69 10.83Weight (kg) 68.83 7.87Height (cm) 166.72 8.52Duration of pain (mo) 9 2.44VAS (mm) 39.7 1.78

SD indicates standard deviation; VAS, visual analog scale.

51 patients screened

Causes for exclusion

29 patients included(19 females)(10 males)

22 patients excluded

29 patients analysed0 losses or dropouts

FIGURE 4. Flow diagram of the patients in this study. RDCindicates Research Diagnostic Criteria; TMD, temporomandibulardisorders.

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MMOThe intrarater reliability on a given day-to-day basis

was excellent with ICC ranging from 0.92 to 0.94 for MMOamong the 3 cranio-cervical postures. Reliability coeffi-cients, ICC associated 95% CI, and SEM values for MMOare presented in Table 2. A 1-way repeated measuresANOVA followed by 3 pair-wise comparisons indicated asignificant difference in MMO among the 3 cranio-cervicalpostures (F=208.06; P<0.001). Post-hoc results revealedthat the MMO was higher in FHP compared with the NHP(difference between means=2.81 cm) and the RHP (differ-ence between means=6.81 cm) (P<0.001). Furthermore,the MMO of the NHP was higher when compared with theRHP (difference between means=4cm) (P<0.001). Table 2summarizes MMO assessed among the 3 cranio-cervicalpostures.

PPTThe intrarater reliability on a given day-to-day basis

was good with ICC ranging from 0.89 to 0.94 for PPTamong the 3 cranio-cervical postures. Reliability coeffi-cients, ICC associated 95% CI, and SEM values for PPTare presented in Table 3. A 1-way repeated measuresANOVA followed by 3 pair-wise comparisons indicated asignificant difference in PPT of the 3 measurement pointsamong the 3 cranio-cervical postures [M1 (F=117.78;P<0.001); M2 (F=129.04; P<0.001); and T1 (F=195.44;P<0.001)]. Results of the post-hoc test for multiplecomparisons between PPT among the 3 cranio-cervicalpostures are presented in Figure 5. Table 4 summarizes thePPT among the 3 head postures.

DISCUSSIONThe experimental posture model used in this study

showed that MMO and PPT values become modifiedamong the induced cranio-cervical postures. MMO andPPT values in the NHP were between those obtained in theFHP and RHP. We observed the highest MMO in the FHP

and the lowest in the RHP. However, the PPT values didnot correspond with those obtained for the MMO as theywere lower in the FHP. In addition, the intrarater reliabilityof the model used to assess MMO and PPT was good.

MMOThe results obtained in the assessment of MMO in

the 3 different postures (NHP 40.8mm, RHP 36.8mm, andFHP 43.7mm) correspond with the results obtained byHigbie et al31 with healthy individuals (NHP 41.5mm,RHP 36.2mm, and FHP 44.5mm). The coincident valuessupport the existence of a functional integration betweenthe anatomic and biomechanical relationship of thetemporomandibular and cranio-cervical regions that hasbeen tested earlier by static and dynamic means. Erikssonet al43 and Zafar et al44 have demonstrated parallel andcoordinated head-neck movements during concomitant jawmovements. Haggman-Henrikson et al45 found a limitationof jaw movement and a shorter duration of jaw opening/closing cycles when experimental fixation of the neck wasperformed.

The variations of MMO in different head positions canbe explained by different actions of the masticatory andcervical muscles as well as intra-articular variations ofcondylar motion. Visscher et al46 found small changes inthe intra-articular distance of the TMJ when it wasmeasured in different cranio-cervical postures. RecentlyOhmure et al47 observed posterior condylar positioning inthe presence of a forced FHP, which may be a predisposingfactor toward intrinsic TMJ disorders resulting fromcumulative muscular and ligamental microtrauma ofabnormal postural origin.48 However, this factor has yetto be supported by clinical research.49,50 Olmos, et al51

demonstrated that after a TMJ treatment in symptomatic

TABLE 2. Descriptive and Intrarater Reliability Statistics forMeasurements of MMO in Patients With Myofascial TMD Pain(N=29) in the 3 Cranio-cervical Postures

Posture Mean±SD 95% CI ICC 95% CI for ICC SEM

NHP 40.8±3.12 39.69-42.07 0.93 0.89-0.96 0.78RHP 36.8±3.6 35.69-38.25 0.93 0.85-0.96 0.92FHP 43.7±2.93 42.58-44.81 0.94 0.90-0.97 0.68

CI indicates confidence interval; FHP, forward head posture; ICC,intraclass correlation coefficient; MMO, maximal mouth opening; NHP,neutral head posture; RHP, retracted head posture; SEM, standard error ofthe measurement; TMD, temporomandibular disorders.

TABLE 3. Descriptive Statistics for Measurements of PPT (kg/cm2) in Patients With Myofascial TMD Pain (N=29)

NHP RHP FHP

Measurement Points Mean±SD 95% CI Mean±SD 95% CI Mean±SD 95% CI

M1 2.2±0.61 1.97-2.44 1.91±0.52 1.71-2.11 1.73±0.48 1.55-1.92M2 2.4±0.61 2.17-2.64 2.1±0.55 1.91-2.35 1.91±0.55 1.7-2.12T1 2.43±0.58 2.2-2.65 2±0.58 1.84-2.28 1.82±053 1.62±2

CI indicates confidence interval; FHP, forward head posture; NHP, neutral head posture; PPT, pressure pain threshold; RHP, retracted head posture; SD,standard deviation; TMD, temporomandibular disorders.

3,50

NHP* * ** *

*2,50

3,00 RHPFHP

** * *

1,00

1,50

2,00

PP

T (

kg/c

m2 )

0,00

0,50

T1M1 M2

FIGURE 5. Comparison of the means of pressure pain thresholds(PPT) measures at masseter and temporalis muscles in relation to3 cranio-cervical postures: neutral head posture (NHP), retractedhead posture (RHP), and forward head posture (FHP). Error barsindicate SD and *P < 0.001.

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52 | www.clinicalpain.com r 2010 Lippincott Williams & Wilkins

patients there seemed to be an increase in the retrodiscalspace and decrease in the distance between the shoulder andexternal auditory meatus. Therefore, an improved condylefossa relationship was apparent as the resting condylarposition became more anterior in conjunction with areduction of the FHP.

Recent evidence and the results of this study support theexistence of a relationship between the biomechanical actionof the cranio-cervical region and jaw movements, but ourresults do not show the degree of clinical implication that thedifferent postures have specific to intrinsic TMJ disorders.

PPTOur findings show that PPT values modify depending

upon the head posture in which they are measured. Thisvariability could be because of increased excitability ofthe trigeminal muscular nociceptors induced by differentcranio-cervical postures within which the PPT was mea-sured. In relation to orofacial nociception, an interactionbetween somatosensory processing and sensory-motorfunction is supported by our data.52

The results of our research cannot determine thereason by which the PPT decreases in the RHP and FHP ascompared with the NHP values. However, if our datais added to the findings of others it may lead to thedevelopment of different theories that offer additionalexplanations. We suggest that the PPT variations may bebecause of experimental biomechanical modifications ofmuscle and soft tissue that were produced when the patientstried to hold the FHP and the RHP, which generatedaugmented electromyography (EMG) activity and masti-catory reflexes. Modification of the activity produced ateach of the aforementioned postures could be causing PPTalteration. Furthermore, increased jaw-reflex activity maybe triggered by enhanced fusimotor drive, thereby elevatingmuscle spindle discharge resulting in reflex facilitation.Elevated fusimotor drive may in turn lead to increased TMJstiffness and pain. Earlier research has supported thepremise that experimental pain can augment masticatoryreflex activity.53–56

A recent study has shown that masseteric EMGactivity increases in the presence of a forced FHP.48 Inaddition, EMG changes in the suprahyoid muscles havebeen observed in experimentally induced FHP.57 However,in direct contrast, earlier studies have found increasedmasticatory EMG activity in head extension,58 which isa component of the RHP. Johansson and Sojka59 haveproposed a model to explain the spread of muscle painbased on the g-motoneuron system in which muscle stiffnessand pain are increased by enhanced activity of primarymuscle spindle afferents. This hypothesis may explain someof the results of this study, however, such thoughts are only

theoretical reflections and future research needs to provewhether postural changes truly alter the nociceptive trigem-inal mechanism.

Study LimitationsThe results of this study must be taken with caution

because the objective measurements were performed inan experimentally forced posture and not a natural one. Itwould also be interesting to determine in future researchwhether the PPT is modified with different natural posturesand whether postural alterations may affect or may be anaggravating factor in the development of orofacial pain. Itis also important to state that our participant sample onlyincluded patients with myofascial TMD. Therefore, it isimperative that future research apply the same method-ology with healthy individuals and other cohorts of TMDto determine whether the results can be replicated.

Clinical ImplicationsThe anatomic and physiological interaction between

the cranio-cervical and temporomandibular regions asshowed in this research supports the concept of a functionaltrigeminocervical coupling during jaw activities that influ-ences the inherent modifications that we observed in MMOand PPT. This factor must be taken into account duringpatient evaluation to control for variations in measurement.

The methodology that we used can result in a morestructured assessment of the MMO and PPT in neutralposition, within which we observed that average values wereobtained with excellent intrarater reliability. Postural treat-ment has already been shown to be useful for reducing TMDmyofascial pain and improving MMO.33,60 We have demon-strated experimentally that pain thresholds at the trigeminalarea can be modified only by changing the cranio-cervicalposture. As PPT values diminish in FHP and RHP, it wouldbe useful to consider new therapeutic strategies to improvethe cranio-cervical posture toward a NHP and futureresearch should determine whether postural treatments canhelp to modulate pain in myofascial TMD patients.

CONCLUSIONSThe results of this study shows that the experimental

induction of different cranio-cervical postures influencesthe MMO and PPT values of masticatory and joint func-tion of the temporomandibular complex. Our observationssupport the concept of a biomechanical relationship andinteraction within the trigeminocervical complex as well asinherent nociceptive processing in different cranio-cervicalpostures. Why or how postural modifications influence thePPT and MMO values are issues that are beyond the scopeof this study.

TABLE 4. Intrarater Reliability Statistics for Measurements of PPT in Patients With Myofascial TMD Pain (N=29) in the 3 Cranio-cervicalPostures

NHP RHP FHP

Measurement Points ICC 95% CI for ICC SEM ICC 95% CI for ICC SEM ICC 95% CI for ICC SEM

M1 0.93 0.87-0.96 0.16 0.9 0.82-0.94 0.16 0.93 0.87-0.96 0.12M2 0.91 0.84-0.95 0.18 0.92 0.86-0.96 0.16 0.92 0.87-0.96 0.15T1 0.89 0.82-0.94 0.19 0.94 0.89-0.97 0.14 0.92 0.86-0.96 0.13

CI indicates confidence interval; FHP, forward head posture; ICC, intraclass correlation coefficient; NHP, neutral head posture; PPT, pressure painthreshold; RHP, retracted head posture; SD, standard deviation; SEM, standard error of the measurement; TMD, temporomandibular disorders.

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ACKNOWLEDGMENT

The authors thank Dr Greg Murray (Professor ofDentistry, Jaw Function and Orofacial Pain Research Unit,Faculty of Dentistry, University of Sydney, Australia) for hishelpful contribution in this article.

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87

5.2 Estudio II

López-de-Uralde-Villanueva I, Beltran-Alacreu H, Paris-Alemany A, Angulo-Díaz-Parreño S,

La Touche R. Reliability, Standard Error, and Minimal Detectable Change of Two Tests for

Craniocervical Posture Assessment in Asymptomatic Subjects and Chronic Neck/craniofacial

Pain Patients. (En revisión).

Objetivo del Estudio

Nuestro objetivo fue examinar la fiabilidad de dos mediciones para evaluar la postura

craneocervical (PC y DME). Además, se evaluó una posible asociación entre las variables

registradas. Como objetivo final, tenemos la intención de evaluar si existen diferencias en la

postura craneocervical entre sujetos asintomáticos y pacientes con dolor cérvico- craneofacial.

Resultados

La fiabilidad intra-evaluador de la medición de PC fue alta para los sujetos asintomáticos y

pacientes DCCF (CCI = 0,93 y 0,81, respectivamente) y para DME (rango CCI entre 0,78-0,99).

La fiabilidad intra-evaluador se mantuvo alta cuando se evaluó 9 días más tarde. Los resultados

de fiabilidad inter-evaluador fue alta para la PC (rango CCI entre 0,94 a 0,96) y fue justa para la

DME (rango CCI entre 0,78 a 0,79). El EEM de PC fue de 0,41 hasta 0,75 cm, mientras que el

MCD fue 0,96 a 1,74 cm. El SEM para la DME fue 1,61 a 7,06 mm, mientras que el MCD fue

3,76 a 16,47 mm. Se observó una correlación positiva moderada en ambos grupos entre HP y

SCD (sujetos asintomáticos, r = 0,447; pacientes con DCCF, r = 0,52). Análisis realizado con

una t de student mostró diferencias estadísticamente significativas entre los grupos para las

medidas de la postura craneocervical, pero estas diferencias eran muy pequeñas. Se encontró

una correlación positiva fuerte entre la discapacidad cervical y la craneofacial.

Conclusiones

Las mediciones para evaluar la postura craneocervical son fiables cuando se realizan por uno o

por dos evaluadores en sujetos asintomáticos o pacientes con DCCF.

1

Reliability, Standard Error, and Minimal Detectable Change of Two Tests for

Craniocervical Posture Assessment in Asymptomatic Subjects and Chronic

Neck/craniofacial Pain Patients

Ibai López-de-Uralde-Villanueva, PT, MSc1-4

, Hector Beltran-Alacreu, PT, MSc 2,3

,

Alba Paris-Alemany, PT, MSc1-4

, Santiago Angulo-Díaz-Parreño, MSc2,3,5

, Roy La

Touche, PT, MSc1-4

,

1. Department of Physiotherapy, Faculty of Health Science, The Center for

Advanced Studies University La Salle, Universidad Autónoma de Madrid,

Aravaca, Madrid, Spain.

2. Research Group on Movement and Behavioral Science and Study of Pain, The

Center for Advanced Studies University La Salle, Universidad Autónoma de

Madrid.

3. Institute of Neuroscience and Craniofacial Pain (INDCRAN), Madrid, Spain

4. Hospital La Paz Institute for Health Research, IdiPAZ. Madrid, Spain.

Madrid, Spain

5. Faculty of Medicine, Universidad San Pablo CEU, Madrid, Spain

Address for reprint requests / Corresponding author:

Roy La Touche

Facultad de Ciencias de la Salud

Centro Superior de Estudios Universitarios La Salle.

Calle la Salle, 10

28023 Madrid

SPAIN

Telephone number: + 34 91 7401980 (EXT.256)

Fax number:

Email address: [email protected]

The study protocol was approved by the local ethics committee of the Center for

Advanced Studies University La Salle, Madrid (Spain).

2

Reliability, Standard Error, and Minimal Detectable Change of Two Tests for

Craniocervical Posture Assessment in Asymptomatic Subjects and Chronic

Neck/craniofacial Pain Patients

ABSTRACT

PURPOSE:

Is recommended to quantifying the craniocervical posture as part of the assessment of

patients with neck and craniofacial pain to facilitate diagnosis and determine

treatment strategies. There is insufficient research regarding the intra-rater and inter-

rater reliability of craniocervical posture measurement using a CROM device and a

Digital Calliper.

OBJETIVE:

Determine the intra-rater and inter-rater reliability of two craniocervical posture

measurements on asymptomatic subjects and chronic neck/craniofacial pain (chronic

cervico-craniofacial pain, CCFP).

METHODS:

Two-groups repeated measures for inter- and intra-rater reliability study. 53

asymptomatic adult subjects and 60 CCFP patients who volunteered for the study.

Two raters measured head posture (HP) and the sternomental distance (SMD) using

the CROM device and Digital Calliper respectively.

RESULTS:

Intra-rater reliability of the HP measurement was high for asymptomatic subjects and

CCFP patients (Intraclass Correlation Coefficients (ICC)=0.93 and 0.81 respectively)

and for SMD (ICC range between 0.78-0.99), the intra-rater reliability remained high

3

when evaluated 9 days later. Inter-rater reliability was high for HP (ICC range

between 0.94-0.96) and fair for SMD (ICC range between 0.78-0.79). The HP

standard error of measurement (SEM) was 0.41–0.75cm while the minimal detectable

change (MDC) was 0.96–1.74cm. The SMD SEM was 1.61-7.06mm while the MDC

was 3.76-16.47mm. A moderate positive correlation for both groups was observed

between HP and SCD (asymptomatic subjects, r=0.447; CCFP patients, r=0.52).

Analysis with an independent t-test showed statistically significant differences

between groups for measures of craniocervical posture, but these differences were

very small. No statistically significant correlations between the HP and SMD with the

disabilities variables. Neck disability is strong positively correlated with the

craniofacial disability (r=0.79, p<0.001, n=60).

CONCLUSION:

The CROM device and Digital Calliper were reliable means of measuring HP and

SMD when performed by two or one raters in asymptomatic subjects and CCFP

patients.

KEYWORDS:

Reliability, Posture, Reproducibility of Results, Rehabilitation, Measurement, Neck

Pain, Temporomandibular disorders

INTRODUCTION

The optimal position of the head is the one in which the cranium is not inclined,

retracted, rotated, or extended. This position minimizes the muscle forces needed to

compensate the tendency of the head to tilt forward.[1] Currently, many professions

(office workers, clerks, carriers, etc.) require workers to spend much of their work day

sitting. In this situation one may adopt an excessive forward head posture (FHP).[2]

4

This head posture (HP) may occur due to a front translation of the head, a flexion of

the lower cervical spine, or both, and is also associated with an increase in extension

of the upper cervical spine.[3] It has been suggested that FHP increases the

compressive forces of the cervical zygapophyseal joint and those in the rear of the

vertebrae,[4] causing changes in the length and strength of the connective tissue

leading to stretching of the anterior neck structures and shortening of the posterior

neck muscles, all leading to pain.[5]

It is recommended that HP is quantified as part of the examination of patients with

neck pain to facilitate the diagnosis and determine treatment strategies. In addition, it

is very important to monitor a patient’s progress.[5] This growing interest around the

importance of the HP by researchers and clinicians is due to the belief that FHP is

associated with the development and persistence of certain disorders, such as cervical

headaches and migraines,[6] myofascial pain syndrome,[7] and woman with

craniofacial pain.[8] Regarding the association between the FHP and pain, there are

numerous studies with conflicting results: some showed differences in the HP of

patients with neck pain versus asymptomatic subjects,[9] while others do not.[10]

Attempts have been made to quantify FHP in many ways, both objectively and

subjectively. Subjective methods are described by some authors,[11] while objective

methods use photographs (to measure the tragus-C7-horizontal angle),[12]

radiographic images,[13] or the Cervical Range of Motion instrument (CROM),[14]

among others.

The CROM was designed to measure cervical range of motion but it can also measure

protraction and retraction of the head.[14] In the trial conducted by Garret et al.[14],

HP was measured in a sitting position with the CROM. The authors found high intra-

5

examiner reliability (ICC=0.93) while inter-examiner reliability was good

(ICC=0.83).

Another measurement that may be of interest is the sternomental distance (SMD). We

hypothesize a direct association between the SMD and the HP. We found only two

studies that evaluated the SMD, but they did not association it with HP.[15, 16]

There is little evidence concerning the reliability of intra-examiner and inter-examiner

measurement of HP using the CROM, therefore our purpose was to examine this

reliability and of using a Digital Calliper to measure the SMD. In addition, we

assessed a possible association between the variables recorded by these instruments

and as ultimate objective, we intend to assess whether there are differences in

craniocervical posture between asymptomatic subjects and patients with chronic

cervico-craniofacial pain (CCFP).

METHODS

Study design

We employed two-group repeated measures for intra- and inter-rater reliability

design. This study was planned and conducted in accordance with the Guidelines for

Reporting Reliability and Agreement Studies (GRRAS).[17]

Sample size

Sample size was calculated using the method described by Walter et al.[18]. This

method is recommended for estimating of sample size based on the Intraclass

Correlation Coefficient (ICC). The minimally acceptable ICC value (ρ1 = 0.7) versus

an alternative ICC reflecting the expected value (ρ1 = 0.8) was chosen. To obtain a

power of 80% (β = 0.2) and significance level of 5%, we determined that a sample of

at least 53 healthy subjects was required for intra-rater and inter-rater reliability (two

sets of 2 measurements were performed each day for two days). In addition, under the

6

same conditions, we determined that a sample of at least 57 symptomatic subjects was

required for intra-rater reliability (1 set of 2 measurements were performed each day

for three days). To estimate sample size we used the Power Analysis & Sample Size

Software (PASS 12).

Subjects

Two convenience samples of asymptomatic subjects were obtained from our

university campus and the local community through flyers, posters, and social media.

To participate in this study, the asymptomatic subjects were required to be between

18 and 65 years of age and must not have experienced: (1) neck or face pain during

data collection, or (2) a history of neck or face pain in the prior six months.

The second convenience sample of symptomatic subjects consisted in chronic

cervico-craniofacial pain patients. The sample was recruited two private clinics

specialized in spine, craniofacial pain and temporomandibular disorders (TMD)

(Madrid, Spain). A diagnosis of CCFP of muscular origin was the first inclusion

criterion. We defined CCFP of muscular origin as the presence of mechanical signs of

dysfunction and muscular pain (e.g. limited movement, uncoordinated movement,

weakness and lack of endurance in the neck and jaw) that were exacerbated by

maintained postures and movement, generating pain at the cervical and craniofacial

regions [19]. The specific inclusion criteria were: a) signs of disability and pain in the

orofacial and craniomandibular region, according to the Craniofacial pain and

disability inventory (CF-PDI) [20]; b) a primary diagnosis of myofascial pain

following Axis 1 (myofascial pain) of the Research Diagnostic Criteria for

Temporomandibular Disorders[21]; c) ≥ 6 months with the presence of the pain; d) ≥

5 points on the Neck Disability Index (NDI)[22]; f) bilateral pain of the temporal,

masseter, suboccipital and trapezius muscles. Patients were excluded if they had any

7

"red flags,"[23] a rheumatologic disease, any type of cancer, cervical radiculopathy,

myelopathy, a history of cervical surgery or whiplash trauma. The study was

conducted in accordance with the Declaration of Helsinki and was approved by the

local ethics committee. Prior to their participation, subjects gave written informed

consent.

Evaluators

The assessments were made by two physical therapists with more than three years of

clinical experience using the CROM to measure range of movement (ROM) and head

posture (HP) in clinical practice. Both therapists received a 120-minute training

session on how to use the Digital Calliper and how to measure the SMD.

Instrumentation

In this study we used the CROM equipped to measure the HP. The device used was

the CROM 3. It has the appearance of eyeglasses and is made from a lightweight

plastic with three inclinometers, one for each plane of motion. It is adjusted using a

hook-and-loop strap. The part of the device used to measure HP includes the forward

head arm and the vertebra locator. The forward head arm is equipped with a ruler

marked in 0.5 cm units, indicating the horizontal distance between the bridge of the

nose and the vertebra locator. The vertebra locator has a leveler bubble on top to

assist with accurate positioning. In this study the inclinometers were not used because

neck movements were not evaluated.

The digital calliper was used to quantify the SMD. The device is made of plastic with

a 5-digit LCD display, and can measure in inches or millimeters (mm) and with a

range of 0.01 mm to 150 mm. It also includes a ruler provided with a nonius, for

accurate measurement of lengths or angles. The one used for measuring length

comprised of a rule divided into equal parts on which a nonius slides such that n-1

8

divisions of the rule are divided into n equal parts of the nonius. It has two tips for

controlling internal and external measurements. The digital calliper is used for direct

measurement. Also, it is a fast and accurate instrument.

Procedures

The assessments were made between May and June of 2012 in our university

laboratory for asymptomatic subjects and between July and September of 2014 for

symptomatic subjects. Each healthy subject visited the laboratory on two different

occasions separated by a space of 48 hours. On the first day, rater A performed the

first assessment followed by rater B. On the second day, rater B performed the first

assessment followed by rater A. Moreover, each symptomatic subject visited the

laboratory on three different occasions separated by a space of 48 hours (between trial

1 and trial 2) and 9 days (between trial 2 and trial 3). In symptomatic subjects, the

assessment always was performed by the same rater. In both samples of subjects, each

rater used a data collection sheet on which to record the measurements. Before the

assessments, subjects removed eyeglasses, caps, and any jewelry. The measurements

in this study were taken twice, and the order in which they were performed was as

follows:

1. Head Posture

To quantify HP, the subjects were told to stay in the starting position: sitting in a chair

with a back rest, feet flat on the floor, and arms hanging alongside the body. The

evaluator placed the CROM on the subject’s head like a pair of eyeglasses and

adjusted it with the strap. The evaluator then located the spinous process of C7 and

placed the vertebra locator on it, adjusting the pressure until the subject indicated that

the pressure of the device was felt. Once the subject felt the pressure over C7, the

9

evaluator stated, “From this moment you should not move”. This was performed as a

means for the subject to become familiar with the test.

Then the subject was asked to stand up and then sit back into the starting position.

The evaluator standing to the left side of the subject, found the spinous process of C7

and placed the vertebra locator such that it formed a 90° angle with the head arm of

the CROM with the bubble indicating the instrument was level (Figure 1. A). This

measurement was made twice, and between the first and the second measurements the

subjects were asked to stand up and sit back into the starting position again,

whereupon the evaluator completed the procedure.

2. Sternomental Distance

The evaluator first explained to the subject that the measurement would take place

while lying on a couch. Also at this time the evaluator showed the Digital Calliper to

the subject and said: “You will notice contact on your sternum and on your chin; at

the moment you notice that you should not move.” When the subject understood the

statement and gave the evaluator permission to proceed, the subject was asked to lie

in a supine position on the couch, looking at the ceiling. When the subject was in

position the evaluator gave the instruction: “Don’t move your head.” Once in place,

the measurement was taken from the jugular notch of the sternum to the chin

protuberance (Figure 1. B). The measurement was taken twice between the subject

was instructed to roll to a right lateral position and then return to the supine position.

DATA ANALYSIS

Data were analysed with the SPSS statistical package (SPSS v.20.0; SPSS, Inc,

Chicago, IL). The Kolmogorov-Smirnov test was used to analyze the normal

distribution of the variables (P>0.05).

10

The intra-rater and inter-rater reliability was evaluated using the Intraclass Correlation

Coefficient (ICC). Reliability levels were defined based on the following

classification: good reliability, ICC ≥ 0.75; moderate reliability, ICC ≥ 0.50 and

<0.75; and poor reliability, <0.50 [24].

Bland-Altman analysis were performed by calculating the mean difference between

two measurements and the standard deviation (SD) of the difference.[25] A 95% of

the differences is expected to be less than two SDs. The closer the mean difference

was to 0 and the smaller the SD of this difference, the better was the agreement.[25]

The Bland–Altman analysis was used to compare the values of HP and SMD obtained

by the two raters separately. Similarly, comparisons were made to confirm the

reproducibility by analyzing the measurements values obtained on two trials. Bland-

Altman analysis was performed using MedCalc for Windows, version 12.5.0.0

(MedCalc Software, Mariakerke, Belgium).

Measurement error is expressed as a standard error of measurement (SEM), which is

calculated as , where SD is the SD of values from all participants and

ICC is the reliability coefficient.[26] Measurement error is the systematic and random

error of a patient’s score that is not attributable to true changes in the construct to be

measured.[27]

Responsiveness was assessed using the Minimal Detectable Change (MDC). The

MDC90 expresses the minimal change required to be 90% confident that the observed

change between the two measures reflects real change and not measurement error.[28]

It is calculated as .[28]

The Pearson correlation coefficient was used to analyze the association between HP

and SMD in the two samples of subjects, also used to analyze the correlations

between the variables of disability with the data HP and SMD in patients with CCFP.

11

A Pearson correlation coefficient greater then 0.60 indicated a strong correlation,

between 0.30 and 0.60 indicated a moderate correlation, and below 0.30 indicated a

low or very low correlation.[29]

Finally, the independent t-test was used for the analysis of HP and SMD variables

(using the mean of the trial 1 and 2), comparing the collection data for the two

samples.

RESULTS

The asymptomatic subjects sample consisted of 53 participants, 30 of whom were

women; the subjects were between 18 and 53 years of age (mean=38.1, SD=10.5

years). The symptomatic subjects sample consisted of 60 CCFP patients, 32 of whom

were women; the subjects were between 19 and 61 years of age (mean=41.7, SD=11.7

years). No statistically significant differences between the general characteristics of

both groups are presented. The group of symptomatic subjects presented a mean of

14.78 ±4.04 of neck disability and 16.30±7.11 of craniofacial disability. All variables

were normally distributed according to the Kolmogorov-Smirnov test (P>0.05). No

subjects were excluded from the study based on the inclusion and exclusion criteria.

Asymptomatic subjects

The ICC value for intra-rater reliability of single measures separated by a space of 48

hours was 0.93 for HP and ranged from 0.95 to 0.99 for SMD. Descriptive statistics,

ICCs and associated 95% CIs, SEMs and MDC90 between each evaluator´s trials are

presented in Table 1.

ICC values for interrater reliability of single measures ranged from 0.78 to 0.79 for

SMD and from 0.94 to 0.96 for HP. Descriptive statistics, ICCs and associated 95%

CIs, SEMs, and MDC90 between each rater´s trials are presented in Table 1.

12

The Bland-Almand analysis for the intra-rater and inter-rater performances are shown

for assessement of HP and SMD in Table 2. The mean differences in all Bland-

Almand analysis were close to zero, suggesting that appropriate intra-rater and inter-

rater reliability. Inter-rater performances of SMD at the 95% confidence intervals

showed large variability, would indicate error and suggesting that SMD assessment is

reliable but not precise (Table 2).

The scatter diagram (Figure 2. A) shows a moderate positive correlation between HP

and the SMD (r=0.44, p=0.001, n=53).

Chronic cervico-craniofacial pain patients

The ICC value for intra-rater reliability of single measures separated by a space of 48

hours was 0.88 for HP and 0.79 for SMD. When the singles measures were separated

by a space of 9 days, the ICC value for intra-rater reliability was 0.81 for HP and 0.76

for SMD. Descriptive statistics, ICCs and associated 95% CIs, SEMs and MDC90

between trials are presented in Table 3.

The Bland-Almand analysis for the intra-rater performances are shown for

assessement of HP and SMD in Table 4. The mean differences in all Bland-Almand

analysis were close to zero, suggesting that appropriate intra-rater and inter-rater

reliability. Inter-rater performances of SMD at the 95% confidence intervals showed

large variability, would indicate error and suggesting that SMD assessment is reliable

but not precise. (Table 4).

The scatter diagram (Figure 2. B) shows a moderate positive correlation between HP

and the SMD (r=0.56, p<0.001, n=60). No statistically significant correlations

between the HP and SMD with the disabilities variables. Neck disability is strong

positively correlated with the craniofacial disability (r=0.79, p<0.001, n=60).

13

Asymptomatic subjects versus chronic cervico-craniofacial pain patients

The independent t-test for comparison between the asymptomatic and symptomatic

samples, using the mean of the trial 1 and 2 (separated by 48 hours), found

statistically significant differences for HP and SMD (p<0.05). Descriptive statistics,

mean differences and associated 95% CIs between the two samples are presented in

Table 5.

DISCUSSION

The evaluation of HP is a variable to consider evaluating in clinical practice due to its

influence on the pathophysiology of the cervical region.[4, 30] Our results show

strong intra- and inter-rater reliability when measuring HP with the CROM device. As

for the examination of the SMD, results obtained with the Digital Calliper reflected

strong reliability.

Recently, several studies have measured HP using different methods and

instruments,[1, 11–13] but disadvantages were low reliability,[11, 31] high cost, and

difficulty in transporting the equipment.[13, 32, 33] Furthermore, where a

radiological diagnosis was used, the risk of radiation exposure to the subject must be

considered.

In the literature we found only one study in which the intra- and inter-rater

reliabilities were evaluated in measuring HP using CROM; results showed a good

intra and inter-rater reliability.[14] If we compare this data with our own, we find

strong intra-rater reliability in both investigations, while our inter-rater reliability was

superior to that obtained by Garrett et al.[14] for asymptomatic subjects but not for

CCFP patients. Both investigations followed a rigorous standardized protocol using

similar samples. An important aspect to note is that the time did not influence the

14

intra-rater reliability and the results were very similar at 48 hours and 9 days later. It

has been suggested that a range of 2 to 14 days is generally acceptable for analyzing

test reliability.[34]

As we mentioned, the SMD measured by the Digital Calliper showed high intra-rater

reliability where it showed acceptable inter-rater reliability. Again, we find only one

article that mentions the SMD, but that investigation was designed to generate a

prediction rule for the degree of difficulty when performing a laryngoscopy.[15, 16]

The SMD measurement used in a study by Al Ramadhani et al.[15], was of 142.8

(SD=1.50), whereas we found SMD to be between 107.5 and 113.57 of our study.

This difference could be explained by the fact that their measurement protocol was

performed measuring the cervical extension. It is also worth mentioning that the

measure was performed using a ruler with an accuracy of 5 mm rather than a Digital

Calliper with a resolution of 0.01 mm. We feel this fact supports a contention that our

investigation is more rigorous and reliable.

We found the intra-rater MDC of HP varied from 1.27 cm to 1.74 cm but that the

inter-rater MDC was between 0.96 cm and 1.30 cm. We also found that the intra-rater

MDC of the SMD was between 3.76 mm and 14.55 mm while the inter-rater MDC

was between 16.13 mm and 16.47 mm. Is considered MDC the smallest quantity

above the SEM, although it should not be assumed that this change has reached the

threshold of clinically significant improvement.[35]

With regard to the comparison of the means of the 2 measurements of the

craniocervical posture, the results show that there are statistically significant

differences between both groups, with higher measures in the group of CCFP,

however you have to take into account that the differences are very small and exceed

slightly the MDC in the HP measurement (mean difference -1.27 cm), nor for the

15

SMD (mean difference -5.01 mm), other studies have found similar results to ours,

finding very small differences between measurements of craniocervical posture in

asymptomatic subjects versus symptomatic subjects with neck pain [30] and

TMD.[36] We did not find association between measurements of craniocervical

posture and disability variables, this result is supported by recent evidence [36, 37],

being this issue controversial.[38] We have found a strong correlation between neck

disability and craniofacial disability (r=0.79), other studies have also found similar

results to our findings. [20, 36]

Furthermore, the Pearson correlation coefficient between HP and the SMD is 0.447

for asymptomatic subject and 0.56 for symptomatic subjects, suggesting a moderate

correlation. We believe this is the first study to determine this association; we found

that the previous studies measuring the SMD do not correlate it to HP. Thus, we can

assume that there is a relationship between HP in the sitting position and SMD in

supine position in healthy subjects.

Limitations

This study has several limitations that must be discussed. We agree with Garret et

al.[14] that a limitation exists in the head arm of the CROM in that it is marked in

increments of 0.5 cm, making it hard to determine a measurement when the indicator

is between two marks. We believe that the reliability and data collection could be

improved if the head arm was marked in mm. Lastly, we calculated the MDC but not

the minimal clinically relevant change (MCRC), which we believe is of special

interest in clinical practice. We must remember that the MDC is not the same as the

MCRC, which is the grade of clinically significant improvement and is normally

associated with an external criteria that indicates when that change has occurred.[35]

We have not calculated the MCRC, so we do not know the grade of clinically

16

significant improvement. Future randomized controlled trials should identify

interventions that influence the HP and SMD, this could help assess the performance

of this test when subjected to clinical interventions and also with those results could

calculate the MCRC.

CONCLUSIONS

The CROM and the Digital Calliper are reliable instruments for measuring HP and the

SMD in healthy subjects and CCFP patients. Furthermore, there is a moderate

correlation between HP and the SMD and strong correlation between neck disability

and craniofacial disability. We did not find association between measurements of

craniocervical posture and disability variables. We also believe further studies should

consider the MCRC and the influence of longer periods between examinations on the

measures.

17

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20

FIGURES AND LEGENDS

Figure 1. A) Placement of CROM with the head arm for the measure of Head Posture

with the vertebra locator. B) Evaluator taking measure from the jugular notch of the

sternum to the chin protuberance to quantitative the Sternomental Distance.

21

Figure 2. Scatter Diagram showing correlation between Head Posture and the

Sternomental Distance. A) Scatter diagram for asymptomatic subjects (n=53); B)

scatter diagram for chronic cervico-craniofacial pain patients (n=60).

22

Table 1. Intra-rater and Inter-rater reliability and descriptive statistics for

measurements in asymptomatic subjects.

Abbreviations: CI, confidence interval; ICC 3,1, intraclass correlation coefficient,

model 3,1; HP, head posture; MDC90, minimal detectable change at the 90%

confidence level; SMD, sternomental distance; SD, standard deviation; SEM,

standard error of the measurement.

Rater A Rater B

Trial 1

(Mean

± SD)

Trial 2

(Mean

± SD)

ICC

3,1

95%

CI for

ICC

SEM MDC90 Trial 1

(Mean

± SD)

Trial 2

(Mean

± SD)

ICC

3,1

95%

CI for

ICC

SEM MDC90

HP (cm) 18.97 ±

2.47

19.07

± 2.19

0.93 0.88 –

0.96

0.60 1.40 18.77

± 2.35

18.96

± 2.19

0.93 0.89 –

0.96

0.55 1.30

SMD

(mm)

108.50

± 16.55

109.03

±

16.14

0.99

0.98 –

0.99

1.61 3.76 105.07

±

14.55

107.54

±

14.21

0.95 0.85 –

0.97

2.75 6.42

Trial 1

Trial 2

Rater A

(Mean

± SD)

Rater

B

(Mean

± SD)

ICC

3,1

95%

CI for

ICC

SEM MDC90 Rater

A

(Mean

± SD)

Rater

B

(Mean

± SD)

ICC

3,1

95%

CI for

ICC

SEM MDC90

HP (cm) 18.97 ±

2.47

18.77

± 2.35

0.94 0.90 –

0.96

0.56 1.30 19.07

± 2.19

18.96

± 2.19

0.96 0.93 –

0.98

0.41 0.96

SMD

(mm)

108.50

± 16.55

105.07

±

14.55

0.78 0.63 –

0.87

7.06 16.47 109.03

±

16.14

107.54

±

14.21

0.79 0.66 –

0.87

6.91 16.13

23

Table 2. Statistical metrics from Bland-Altman analysis of the intra-rater and inter-

rater measurements in asymptomatic subjects.

Intra-rater

Rater A Rater B

Mean

differences

± SD

95% CI for

mean

differences

LOA (Lower

limit-Upper

limit)

Mean

differences

± SD

95% CI for

mean

differences

LOA (Lower

limit-Upper

limit)

HP (cm) -0.10 ± 0.85 -0.34 to 0.15 -1.76 to 1.57 -0.19 ± 0.79 -0.41 to 0.04 -1.73 to 1.36

SMD (mm) -0.53 ± 2.28 -1.18 to 0.12 -4.99 to 3.94 -2.47 ± 3.89 -3.58 to -1.37 -10.10 to 5.16

Inter-rater

Trial 1 Trial 2

HP (cm)

0.19 ± 0.79 -0.03 to 0.42 -1.35 to 1.74 0.10 ± 0.59 -0.06 to 0.27 -1.05 to 1.25

SMD (mm) 3.43 ± 9.99 0.59 to 6.27 -16.14 to 23 1.49 ± 9.78 -1.29 to 4.26 -17.68 to 20.65

Abbreviations: CI, confidence interval; HP, head posture; LOA, limits of agreement;

SMD, sternomental distance; SD, standard deviation.

24

Table 3. Intra-rater reliability and descriptive statistics for measurements in chronic

cervico-craniofacial pain patients.

Abbreviations: CI, confidence interval; ICC 3,1, intraclass correlation coefficient,

model 3,1; HP, head posture; MDC90, minimal detectable change at the 90%

confidence level; SMD, sternomental distance; SD, standard deviation; SEM,

standard error of the measurement.

Rater A

Trial 1

(Mean

± SD)

Trial 2

(Mean

± SD)

Trial 3

(Mean

± SD)

48 hours between trials

(Trial 1-Trial 2)

9 days between trials

(Trial 2-Trial 3)

ICC

3,1

95% CI

for ICC

SEM MDC90 ICC

3,1

95% CI

for ICC

SEM MDC90

HP (cm) 20.40 ±

1.50

20.23

± 1.58

20.03 ±

1.84

0.88 0.80 –

0.92

0.54 1.27 0.81 0.70 –

0.88

0.75 1.74

SMD

(mm)

111.53

± 12.41

113.57

±

11.83

112.73

± 13.78

0.79

0.67 –

0.87

5.60 13.07 0.76 0.63 –

0.85

6.24 14.55

25

Table 4. Statistical metrics from Bland-Altman analysis of the intra-rater

measurements in chronic cervico-craniofacial pain patients.

Intra-rater

48 hours (Trial 1 – Trial 2) 9 days (Trial 2 – Trial 3)

Mean

differences

± SD

95% CI for

mean

differences

LOA (Lower

limit-Upper

limit)

Mean

differences

± SD

95% CI for

mean

differences

LOA (Lower

limit-Upper

limit)

HP (cm) 0.17 ± 0.77 -0.03 to 0.37 -1.34 to 1.67 0.21 ± 1.06 -0.06 to 0.48 -1.86 to 2.28

SMD (mm) -2.03 ± 7.92 -4.08 to 0.01 -17.56 to 13.49 0.83 ± 8.82 -1.45 to 3.11 -16.46 to 18.12

Abbreviations: CI, confidence interval; HP, head posture; LOA, limits of agreement;

SMD, sternomental distance; SD, standard deviation.

26

Table 5. Comparison between the asymptomatic subjects and chronic cervico-

craniofacial pain patients samples for measurements.

Asymptomatic

subjects (Mean ± SD)

CCFP patients (Mean

± SD)

Mean differences (95% CI)

HP (cm) 18.95 ± 2.25 20.32 ± 1.49 -1.37 (-2.11 to -0.63)**

SMD (mm) 107.54 ± 14.53 112.55 ± 11.46 -5.01 (-9.92 to -0.1)*

Abbreviations: CI, confidence interval; HP, head posture; SMD, sternomental

distance; SD, standard deviation.

* p<0.05

** p<0.01

114

5.3 Estudio III

La Touche R, Fernández-de-Las-Peñas C, Fernández-Carnero J, Díaz-Parreño S, Paris-

Alemany A, Arendt-Nielsen L. Bilateral mechanical-pain sensitivity over the trigeminal region

in patients with chronic mechanical neck pain. J Pain. 2010 Mar;11(3):256-63

Objetivos del estudio

El objetivo del presente estudio fue investigar la sensibilización del trigémino en pacientes con

dolor de cuello crónico mecánico, además se observaron la interacción de los resultados con

variables psicológicos, como la depresión y la ansiedad.

Resultado

Los resultados mostraron que los niveles de UDPS son significativamente menores

bilateralmente sobre los puntos musculares del masetero, temporal, los del trapecio superior, y

también los puntos medidos en las articulaciones cigapofisiarias de C5-C6 (P <0,001), pero no

sobre los puntos del músculo tibial anterior (P = 0,4) en pacientes con dolor de cuello crónico

mecánico, en comparación con los controles. La magnitud de la disminución de los UDPs fue

mayor en la región cervical, en comparación con la región del trigeminal (P <0,01). Los UDPs

en los músculos maseteros se correlacionaron negativamente tanto a la duración de los síntomas

de dolor y la intensidad del dolor (P <0,001). Además se encontraron correlaciones positivas

entre la intensidad de dolor con la discapacidad de cuello y los síntomas depresivos.

Conclusiones

Nuestros resultados revelaron la presencia de hiperalgesia mecánica en la región trigeminal en

pacientes con dolor de cuello crónico mecánico, lo que sugiere la difusión de la sensibilización a

la región del trigémino en esta población de pacientes. Los resultados de este estudio sugieren

que existe la presencia de un proceso de sensibilización del NCT en esta población. Este

hallazgo tiene implicaciones para el desarrollo de estrategias de gestión.

The Journal of Pain, Vol 11, No 3 (March), 2010: pp 256-263Available online at www.sciencedirect.com

Bilateral Mechanical-Pain Sensitivity Over the Trigeminal Region in

Patients With Chronic Mechanical Neck Pain

Roy La Touche,*y Cesar Fernandez-de-las-Penas,zx{ Josue Fernandez-Carnero,zx{

Santiago Dıaz-Parreno,*y Alba Paris-Alemany,*y and Lars Arendt-Nielsenz

*Faculty of Medicine, Department of Physical Therapy.yUniversity Center for Clinical Research of the Craneal-Cervical-Mandibular System, Universidad San Pablo CEU,Madrid, Spain.zDepartment of Physical Therapy, Occupational Therapy, Rehabilitation and Physical Medicine.xEsthesiology Laboratory, Universidad Rey Juan Carlos, Alcorcon, Madrid, Spain.{Centre for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University,Aalborg, Denmark.

ReceivedAddressde Ciencs/n, 2892

1526-590

ª 2010 b

doi:10.10

256

Abstract: The aim of this study was to investigate bilateral pressure-pain sensitivity over the tri-

geminal region, the cervical spine, and the tibialis anterior muscle in patients with mechanical chronic

neck pain. Twenty-three patients with neck pain (56% women), aged 20 to 37 years old, and 23

matched controls (aged 20 to 38 years) were included. Pressure pain thresholds (PPTs) were bilaterally

assessed over masseter, temporalis, and upper trapezius muscles, the C5-C6 zygapophyseal joint, and

the tibialis anterior muscle in a blinded design. The results showed that PPT levels were significantly

decreased bilaterally over the masseter, temporalis, and upper trapezius muscles, and also the C5-C6

zygapophyseal joint (P < .001), but not over the tibialis anterior muscle (P = .4) in patients with

mechanical chronic neck pain when compared to controls. The magnitude of PPT decreases was

greater in the cervical region as compared to the trigeminal region (P < .01). PPTs over the masseter

muscles were negatively correlated to both duration of pain symptoms and neck-pain intensity (P <

.001). Our findings revealed pressure-pain hyperalgesia in the trigeminal region in patients with

mechanical chronic neck pain, suggesting spreading of sensitization to the trigeminal region in

this patient population.

Perspective: This article reveals the presence of bilateral pressure-pain hypersensitivity in the

trigeminal region in patients with idiopathic neck pain, suggesting a sensitization process of the tri-

gemino-cervical nucleus caudalis in this population. This finding has implications for development of

management strategies.

ª 2010 by the American Pain Society

Key words: Neck pain, trigeminal sensitization, pressure pain threshold.

Chronic mechanical neck pain is a significant clinicalproblem. It seems that the prevalence of neck painis as high as the prevalence of low back pain. A sys-

tematic review reported a 1-year prevalence for neckpain ranging from 16.7 to 75.1%, with a mean of37.2%.11 A best-evidence synthesis showed an incidencerate for self-reported neck pain in the general popula-tion between 146 and 213 per 1,000 patients per year.21

Nearly half of neck-pain patients develop chronic symp-

May 31, 2009; Revised June 29, 2009; Accepted July 22, 2009.reprint requests to Cesar Fernandez de las Penas, Facultadias de la Salud, Universidad Rey Juan Carlos, Avenida de Atenas2 Alcorcon, Madrid, Spain. E-mail: [email protected]

0/$36.00

y the American Pain Society

16/j.jpain.2009.07.003

toms,4 and many will continue to exhibit moderatedisability at long-term follow-up.17 The economicburden associated with the management of neck painis second only to low back pain in annual workers’ com-pensation costs in the United States.44

Although the aetiology of insidious mechanical neckpain is under debate, it is clear that neck pain is multifac-torial in nature, with both physical and psychosocial con-tributors.38 In recent years, there has been an increasinginterest in the study of nociceptive-pain processing indifferent musculoskeletal-pain conditions. For instance,pressure pain thresholds5,32 have been extensively usedfor investigating mechanical pain hypersensitivity inseveral chronic pain conditions, eg, whiplash,36 fibro-myalgia,9 unilateral migraine,14 repetitive strain injury,18

tension-type headache,13 osteoarthritis,1 low back

La Touche et al 257

pain,27 or carpal tunnel syndrome.15 Nevertheless, thephenomenon of sensory hypersensitivity has been rela-tively recently investigated in mechanical nontraumaticneck pain.37

Scott et al33 found that the hypersensitivity present inindividuals with idiopathic neck pain seems to be con-fined to the neck area with little evidence of spread tomore remote body regions, eg, the tibialis anterior mus-cle, as opposite happens in chronic whiplash. The pres-ence of hypersensitivity restricted to the neck regionmay reflect segmental local sensitization, but not wide-spread central sensitization, in patients with idiopathicneck pain.

Several studies have reported that patients with neckpain also suffered from symptoms in the orofacialregion,7,8,23 and headaches.29 The expansion of symp-toms from the neck area to the trigeminal region maybe related to the convergence of the nociceptive sec-ond-order neurons receiving both trigeminal and cervi-cal inputs into the trigemino-cervical nucleus caudalisin the spinal gray matter of the spinal cord.25 To thebest of our knowledge, no previous study has investi-gated the pressure hypersensitivity over the trigeminalregion in chronic mechanical neck pain. Further, Rhudyand Meagher31 demonstrated that psychological states,particularly anxiety and depression, induce an increasedeffect on pressure-pain sensitivity. Therefore, the aim ofthe present study was to investigate trigeminal sensitiza-tion in patients with chronic mechanical neck pain con-trolling psychological aspects, such as depression andanxiety.

Methods

SubjectsPatients presenting with mechanical insidious neck

pain referred by their primary-care physicians to a spe-cialized physical-therapy clinic between September2007 and February 2008 were screened for possible eligi-bility criteria. Mechanical neck pain was defined as gen-eralized neck and/or shoulder pain with symptomsprovoked by neck postures, neck movement, or palpa-tion of the cervical musculature. Symptoms had to be bi-lateral and present for at least 6 months. Patients wereexcluded if they exhibited any of the following: 1) unilat-eral neck pain; 2) diagnosis of fibromyalgia;43 3) previouswhiplash; 4) cervical spine surgery; 5) clinical diagnosis ofcervical radiculopathy or myelopathy; 6) history of previ-ous physical-therapy intervention for the cervical region;7) presence of severe degenerative arthritis (confirmedby cervical radiography taken for all patients over theage of 30 years); 8) less than 18 years; 9) diagnosis ofany TMD, according to the Research Diagnostic Criteriafor TMD (RDC/TMD)10; or 10) concomitant diagnosis ofprimary headache.

Demographic and Clinical DataDemographic data including age, gender, height,

weight, location, and nature of the symptoms was col-lected. An 11-point numerical point rate scale22 (NPRS;

0 = no pain, 10 = maximum pain) was used to assess cur-rent level of neck pain. Patients also completed the NeckDisability Index (NDI) to measure perceived disability,42

the Beck Depression Inventory (BDI-II) to assess symp-toms of depression,2 and the State-Trait Anxiety Inven-tory (STAI) for assessing state and trait anxiety.34

The NDI consist of 10 questions measured on a 6-pointscale (0 = no disability, 5 = full disability).42 The numericscore for each item is summed for a score varying from0 to 50, where higher scores reflect greater disability.The NDI has demonstrated to be a reliable (intraclass cor-relation coefficients ranging from .50 to .98)24 and validself-assessment of disability in chronic neck pain.19,39

The BDI-II is a 21-item self-report measure assessingaffective, cognitive, and somatic symptoms of depres-sion.2 Patients choose from a group of sentences thatbest describe how they have been feeling in the past 2weeks. Higher scores indicate higher levels of depressivesymptoms.2 The BDI-II showed good internal consistency(alpha coefficient .90) and adequate divergent validity.41

The STAI is a self-report assessment device whichincludes separate measures of state and trait anxiety.34

In the present study, the trait-anxiety subscale whichdenotes relatively stable anxiety proneness and refersto a general tendency to respond with anxiety to per-ceived threats in the environment was used. Participantsuse a 4-point response scale ranging from ‘‘almost never’’to ‘‘almost always’’, indicating the extent to which theyexperience each emotion. The State-Trait questionnairehas shown good internal consistency (a = .83). Higherscores indicate greater trait anxiety.34

Finally, healthy controls were recruited from volunteerwho responded to a local announcement and were ex-cluded if they exhibited a history of neck, facial, orhead pain (infrequent episodic tension-type headachewas permitted), any systemic disease or any history oftraumatic event (whiplash).

The study was conducted in accordance with the Hel-sinki Declaration, and all subjects provided informed con-sent which was approved by the local ethics committee.

Sample Size DeterminationThe sample-size determination and power calculations

were performed with an appropriate software (Tamanode la Muestra, v.1.1, Universidad de Medicina, Madrid,Spain). The calculations were based on detecting, atthe least, significant clinical differences of 20% on pres-sure pain threshold (PPT) between both groups,28 withan alpha level of .05 and a desired power of 80%, andan estimated interindividual coefficient of variation forPPT measures of 20%. This generated a sample size ofat least 16 participants per group.

PPT AssessmentPPT is defined as the minimal amount of pressure

where a sensation of pressure first changes to pain.40 Amechanical pressure algometer (Pain Diagnosis andTreatment Inc, Great Neck, NY) was used in this study.The device consists of a round rubber disk (1 cm2)attached to a pressure gauge. The gauge displays values

258 Trigeminal Pain Sensitivity in Neck Pain

in kg/cm2, ranging from 0 to 10 kg. The mean of 3 trials(intraexaminer reliability) was calculated and used forthe main analysis. A 30-second resting period wasallowed between each trial. The reliability of pressure al-gometry has been found to be high in both asymptom-atic subjects6 (ICC .91 [95% CI .82–.97]) and neck painpatients45 (ICC .78–.93; 95% CI .53–.97).

Study ProtocolThe study protocol was the same for neck-pain pa-

tients and healthy controls. All examinations weredone in a quiet, draught-free, temperature- and humid-ity-controlled laboratory (24�C 6 1�C, relative humidity25–35%). All participants were restricted from vigorousexercise from the day prior to the examination. Noneof the patients were taking any preventive drug at thetime the study was performed. Participants were not al-lowed to take analgesics or muscle relaxants throughthe 72 hours prior to the examination. PPTs were mea-sured bilaterally over masseter and temporalis muscles,the articular pillar of C5-C6 zygapophyseal joint (basedon palpation of C6-C7 spinous processes), the upper tra-pezius muscle (midway between C7 and acromion), andtibialis anterior muscle (upper one-third of the musclebelly) by an assessor blinded to the subject’s condition.The masseter and temporalis muscles were chosen as tri-geminal areas, the articular pillar of C5-C6 and the uppertrapezius muscle were chosen as the most common sitesof involvement in idiopathic neck pain, and the tibialisanterior was chosen as a remote distant site. The orderof assessment was randomized between the participants.

Pressure Pain Threshold DataManagement

In the current study, the magnitude of sensitizationwas investigated by assessing the differences of absoluteand relative PPT values between both groups. For rela-tive values, we calculated a ‘‘PPT Index,’’ dividing thePPT of each patient at each point by the mean of PPTscore of the control group at the same point. PPT indiceswere only calculated in those PPT levels significantly dif-ferent between patients and controls. A greater PPT In-dex (%) indicates lower degree of sensitization.

Statistical AnalysisData were analysed with the SPSS statistical package

(SPSS v.16.0; SPSS, Inc, Chicago, IL). Results are expressedas mean, standard deviation (SD), and 95% confidenceinterval (95% CI). The Kolmogorov-Smirnov test wasused to analyze the normal distribution of the variables(P > .05). Quantitative data without a normal distribution(ie, pain history, current level of pain, and NDI) were an-alyzed with nonparametric tests, whereas data witha normal distribution (PPT levels, BDI-II, and STAI) wereanalyzed with parametric tests. The intraclass correlationcoefficient (ICC) was used to evaluate the intraexaminerreliability of PPT data. A 2-way ANCOVA was used to in-vestigate the differences in PPT assessed over each point(masseter, temporalis, upper trapezius, tibialis anteriormuscles, and the C5-C6 zygapophyseal joint) with side

(dominant or nondominant) as within-subject factorand group (patients or controls) as the between-subjectfactor. A 2-way ANCOVA test was used for assessing thedifferences in PPT Index with side (dominant, nondomi-nant) as within-patient factor, point (masseter, tempora-lis, upper trapezius, tibialis anterior muscles, and theC5-C6 joint) as between-patient factor, and age, sex,BDI-II, and STAI scores as covariates. Post hoc compari-sons were conducted with the Bonferroni test. Finally,the Spearman’s rho (rs) test was used to analyze the asso-ciation between PPTs and the clinical variables relating tosymptoms, disability, anxiety, and depression. The statis-tical analysis was conducted at a 95% confidence leveland a P value less than .05 was considered statisticallysignificant.

Results

Demographic and Clinical Data of thePatients

Forty consecutive patients presenting with neck painbetween January and May 2009 were screened for possi-ble eligibility criteria. Seventeen patients were excluded:concomitant diagnosis RDC/TMD (n = 8), migraine (n = 5),and previous whiplash (n = 4). Finally, 23 patients (10men and 13 women) with mechanical neck pain, aged20 to 37 years (mean, 28 6 5 years; mean weight, 70 6

10 kg; mean height, 168 6 10 cm), and 23 matched con-trols, aged 20 to 38 years old (mean, 28 6 6 years; meanweight, 66 6 11 kg; mean height, 168 6 9 cm) were in-cluded. No significant differences between both groupsfor age (P = .9), weight (P = .3) and height (P = .8) werefound. Patients with neck pain showed greater levels(P < .001) of depression (BDI-II, 7.5 6 3) and anxiety(STAI, 22.4 6 3.2) as compared to controls (BDI-II, 3 6 3;STAI, 10 6 8, respectively).

Within the patient group, mean duration of neck painhistory was 10 6 4.6 months (95% CI 7.8–11.7 months),the mean intensity (NPRS) of neck pain was 3.6 6 1.5(95% CI 3.2–4.8), the mean NDI was 18.5 6 3.3 (95% CI17–20), the mean BDI-II was 7.5 6 1.6 (95% CI 6–9), andthe STAI was 22 6 3 (95% CI 21–24). Furthermore, posi-tive correlations between duration of pain history withcurrent level of pain (rs = .55, P = .007 [Fig 1A]) andBDI-II (rs =.58, P = .004 [Fig 1B]) were found: the longerthe duration of the symptoms, the greater the intensityof the perceived pain and the greater the self-reporteddepression. Further, current level of pain was also posi-tively correlated to disability (rs = .57, P = .004 [Fig 2A])and to BDI-II (rs = .64; P = .001, [Fig 2B]): the greater theintensity of the perceived pain, the greater the self-re-ported disability and the greater the self-reporteddepression.

Pressure Pain Sensitivity Over theTrigeminal Region

The intraexaminer repeatability of PPTreadings for themasseter and temporalis muscle was .9 and .92 for themost painful side and .91 for the contralateral side. Thestandard error of measurement (SEM) was .14 kg/cm2

Figure 1. Scatter plots of relationships between duration of history of neck pain and NPRS values (A) and between history ofneck pain and Beck Depression Inventory (B) A positive linear regression line is fitted to the data (NPRS: numerical pain rate scale,range 0 to 10).

La Touche et al 259

for the most painful side and .11 kg/cm2 for the contra-lateral side.

The ANOVA revealed significant differences betweenboth groups, but not between sides, for PPT levels overthe masseter (group: F = 257.3, P < .001; side: F = .58,P = .447) and temporalis (group: F = 124.8, P < .001;side: F = .06, P = .803) muscles. Over both muscles, pa-tients showed bilateral lower PPT levels than healthycontrols (P < .001). Table 1 summarizes PPT assessedover the masseter and temporalis muscles for both sideswithin each study group.

Pressure Pain Sensitivity Over theCervical Region

The intraexaminer repeatability of PPT over the C5-C6joint and the upper trapezius muscle was .91 for the mostpainful side and .89 for the contralateral side, respec-tively. The SEM was .11 and .13 kg/cm2 for the most pain-ful side and .15 kg/cm2 for the contralateral side.

The ANOVA revealed significant differences betweenboth groups, but not between sides, for PPT levels overthe upper trapezius muscle (group: F = 355.9, P < .001;side: F = .03, P = .851), and the C5-C6 zygapophyseal joint(group: F = 291.5, P < .001; side: F = .08, P = .776). Again,

Figure 2. Scatter plots of relationships between duration of NPRS pvalues and Beck Depression Inventory (B) A positive linear regression0 to 10).

patients showed bilateral lower PPT levels in both pointsas compared to healthy controls (P < .001). Table 1 showsPPT over the upper trapezius muscle and the C5-C6 zyga-pophyseal joint for both sides within each group.

Pressure Pain Sensitivity Over the TibialisAnterior Muscle

The intraexaminer repeatability of PPT over tibialis an-terior muscle was .93 for the most painful side and .91 forthe contralateral side, whereas the SEM was .18 and .2kg/cm2, respectively.

The ANOVA did not find significant differencesbetween groups and sides for PPT levels over the tibialisanterior muscle (group: F = 1.49, P = .461; side: F = .05, P =.824). Table 1 shows PPT over the tibialis anterior musclefor both sides within each group.

There was no effect of age, BDI-II, or STAI score on PPTlevels (P > .2), although there was an effect of sex at thetibialis anterior with females having lower PPTs (F = 8.8,P = .005) than males.

Pressure Pain Threshold IndicesThe ANOVA revealed significant differences for PPT

indices between sites (F = 8.7, P < .001), but not between

ain values and Neck Disability Index (A) and between NPRS painline is fitted to the data (NPRS: numerical pain rate scale, range

Table 1. Pressure Pain Thresholds (PPTs) in Patients With Mechanical Neck Pain (n = 23) andMatched Control Subjects (n = 23). Mean Values 6 Standard Deviation and 95% ConfidenceIntervals in Parenthesis (kg/cm2)

MECHANICAL NECK PAIN HEALTHY CONTROLS

DOMINANT SIDE NON-DOMINANT SIDE DOMINANT SIDE NON-DOMINANT SIDE

Trigeminal Area

Masseter* 2 6 .4 (1.8–2.2) 2 6 .5 (1.8–2.2) 3.4 6 .5 (3.2–3.6) 3.5 6 .4 (3.3–3.7)

Temporalis* 2.2 6 .5 (1.9–2.5) 2.1 6 .5 (1.9–2.4) 3.7 6 .6 (3.4–3.9) 3.6 6 .8 (3.4–3.9)

Joint

C5–C6* 1.7 6 .4 (1.5–1.9) 1.6 6 .3 (1.4–1.8) 3.2 6 .4 (3.1–3.4) 3.2 6 .6 (3.1–3.5)

Muscle

Upper trapezius* 1.8 6 .4 (1.6–2) 1.8 6 .3 (1.6–2) 3.8 6 .7 (3.6–4) 3.7 6 .5 (3.5–3.9)

Tibialis anterior 5.0 6 .8 (4.6–5.3) 5 6 .9 (4.6–5.4) 5.2 6 .7 (4.9–5.6) 5.3 6 .8 (5–5.7)

*Indicates significant difference between neck pain and control subjects (ANOVA, P < .001).

260 Trigeminal Pain Sensitivity in Neck Pain

sides (F = .03, P = .859). The post hoc analysis showedsignificant differences between both masseter and tem-poralis muscles with the upper trapezius muscle (P < .001)and between the temporalis muscles with the C5-C6 joint(P = .02). In such a way, the cervical region (upper trape-zius muscle and C5-C6 joint) showed lower PPT indices(greater degree of sensitization) compared to the tri-geminal region (masseter and temporalis muscles) forboth sides (Fig 3).

Pressure Sensitivity and Clinical Featuresin Patients with Mechanical Neck Pain

Finally, a significant negative correlation between his-tory of symptoms and PPT levels over both masseter mus-cles (dominant side: rs = –.64, P < .001 [Fig 4A];nondominant side: rs = –.42, P = .04 [Fig 4B]) was found:the longer the duration of the symptoms, the lower thePPT levels over both masseter muscles. In addition, cur-rent level of pain intensity was also negatively correlatedwith bilateral PPT levels over the masseter muscles (dom-inant side: rs = –.62, P < .001 [Fig 5A]; nondominant side:rs = –.51, P = .02 [Fig 5B]): the greater the pain intensity,the lower the bilateral PPT levels. No significant correla-tions between NDI, BDI-II, and PPT levels were found.

Figure 3. Pressure pain threshold indices in both trigeminaland cervical points. The boxes represent the mean and percen-tile scores, and the error bars represent the standard deviation.

DiscussionThis study showed bilateral pressure-pain hyperalgesia

in both the trigeminal and cervical region, but not overthe tibialis anterior muscle, in patients with mechanicalchronic neck pain as compared to healthy controls. Thedecrease in PPT levels over the trigeminal region was as-sociated with the intensity and duration of pain symp-toms, supporting a role of the peripheral nociceptiveinput as an important factor driving the developmentof spreading sensitization.

Current results of cervical, but not widespread, pressure-pain hypersensitivity in patients with idiopathic neck painare very similar to those previously found by Scott et al.33

The findings from both studies support the idea that me-chanical nontraumatic neck pain is characterized by pres-sure-pain hyperalgesia in the cervical spine, probably

reflecting peripheral nociceptor sensitization. Further-more, our study increases evidence that pressure-pain hy-peralgesia is not only restricted to cervical joints (C5–C6 orC2–C3 as previously reported) but also to cervical muscles(upper trapezius). This is expected since the upper trape-zius muscle receives nerve innervation from the C2–C4level. Nevertheless, lower PPT levels over the upper trape-zius may also be related to muscle spasm residing in theneck muscles in this patient population.

The present study demonstrated that patients withmechanical chronic neck pain also have pressure-pain hy-peralgesia in the trigeminal region. This finding may re-flect a sensitization process of the trigemino-cervicalnucleus caudalis due to the convergence of inputs from

Figure 4. Scatter plot of the relationship between duration of history of neck pain and PPT levels in both dominant (A) and nondom-inant (B) masseter muscles (n = 23). A negative linear regression line is fitted to the data (PPT: pressure pain threshold, kg/cm2).

La Touche et al 261

the trigeminal and cervical regions. In fact, neck-pain pa-tients included in the current study were completelyasymptomatic in the orofacial region, which supportsthat the pressure-pain hyperalgesia found over masseterand temporalis muscles reflects a sensitization process.Nevertheless, it seems that there is a greater sensitizationdegree in the cervical spine. This is supported by the factthat the magnitude of PPT changes was higher over theupper trapezius muscle (48–49%) and C5-C6 zygapophy-seal joint (51–53%) when compared to the magnitude ofPPT changes over the masseter (57–58%) and temporalis(60%) muscles. Nevertheless, there is no consensus aboutthe PPT that are needed to consider differences as realchanges.37 Different studies6,35,45 have suggested thatdifferences ranging from 123 kPa to 200 kPa (1.2–2 kg)are needed to consider real differences. In the currentstudy, differences between trigeminal (1.4–1.5 kg) andcervical regions (1.5–2 kg) were placed within this inter-val, so differences between both groups can be consid-ered as real.

Our results increase the evidence that nontraumaticneck pain is characterized by segmental, but not wide-spread, sensitization mechanisms that are mostlyrestricted to the trigemino-cervical region. The involve-ment of segmental sensitization mechanisms has beenreported in several local pain syndromes, eg repetitivestrain injury,18 chronic tension-type headache,13 low

Figure 5. Scatter plot of the relationship between duration of NPRinant (B) masseter muscles (n = 23). A negative linear regression line

back pain,27 osteoarthritis,1 carpal tunnel syndrome,15

and unilateral shoulder pain.16 The existence of sensiti-zation mechanisms in local pain syndromes suggeststhat sustained peripheral noxious input to the centralnervous system plays a role in the initiation and mainte-nance of sensitization process.26 This is supported by thefact that central sensitization is a dynamic conditioninfluenced by multiple factors, including activity of pe-ripheral nociceptive inputs.20 For instance, in insidiousmechanical neck pain, where there is no sudden nocicep-tive barrage to the central nervous system as in patientswith whiplash syndrome, a prolonged, continued noci-ceptive barrage from different cervical structures, eg,muscles12 or facet joints,3 may be capable of leading toimpairment in the nociceptive processing of the trige-mino-cervical nucleus caudalis. This was supported bythe fact that duration of symptoms was positively relatedto current level of pain and PPT levels over the massetermuscle. On the contrary, Scott et al33 found that durationof pain symptoms was not related to PPT levels over thecervical spine. It should be considered that patients in-cluded in the study by Scott et al have a greater durationof symptoms (mean: 51.5 6 40 months), were more dis-abled (NDI: 29 ± 16), and had greater levels of anxiety(STAI: 40.6 ± 11) than patients included in the presentstudy (duration of symptoms: 10 ± 4.6 months; NDI,18.5 6 3.3; STAI, 22.4 6 3.2), which may explain

S pain values and PPT levels in both dominant (A) and nondom-is fitted to the data (PPT: pressure pain threshold, kg/cm2).

262 Trigeminal Pain Sensitivity in Neck Pain

differences between both studies. Finally, we do notknow if sensitization mechanisms found in this studyare mediated via a deregulation of second-order neu-rons in a segmental fashion or via glia30 and other im-mune cells that reside in the trigeminal-cervical region.Future studies are needed to further elucidate the mech-anisms involved in trigemino-cervical sensitization inneck pain.

It has been suggested that anxiety and depression mayinfluence pressure-pain hypersensitivity.31 Our resultswere independent of levels of depression (BDI-II) andthe state anxiety (STAI). Additionally, patients includedin the present study showed scores < 8 points in theBDI-II, which are considered normal.2 Our results agreewith those previously reported by Scott et al33 in whichanxiety appears not to influence pressure-pain sensitivityin patients with insidious mechanical neck pain. Never-

theless, further studies investigating the influence ofpsychological factors are required.

ConclusionBilateral pressure-pain hyperalgesia was detected in

both trigeminal and cervical regions in patients with me-chanical chronic neck pain. The decrease in pressure painthresholds in the trigeminal region was associated withthe intensity and duration of the neck-pain symptoms,supporting a role of the peripheral nociceptive input asa driving factor for inducing sensitization. Our study fur-ther supports that nontraumatic neck pain shows sensiti-zation in the trigemino cervical region, which has clinicalimplications in terms of spreading symptomatology tothis body area.

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123

5.4 Estudio IV

La Touche R, Pardo-Montero J, Gil-Martínez A, Paris-Alemany A, Angulo-Díaz-Parreño S,

Suárez-Falcón JC, Lara-Lara M, Fernández-Carnero J. Craniofacial pain and disability

inventory (CF-PDI): development and psychometric validation of a new questionnaire. Pain

Physician. 2014 Jan-Feb;17(1):95-108.

Objetivo del estudio

El propósito de este estudio es presentar el desarrollo, el análisis de la estructura factorial y

propiedades psicométricas de un nuevo cuestionario auto-administrado (Inventario de dolor y

discapacidad craneofacial; IDD-CF), dirigido a medir el dolor, la discapacidad y el estado

funcional de la mandíbula y la región craneofacial.

Resultados

La versión final del IDD-CF consta de 21 ítems, el análisis factorial exploratorio reveló dos

factores ("El dolor y la discapacidad" y "el estado funcional de mandíbula"), ambos factores con

valor propio mayor que uno, que explican 44,77% de la varianza. No se observaron efectos

suelo o techo. Se confirmó una alta consistencia interna de la IDD-CF (α de Cronbach: 0,88) y

también para las dos subescalas (0,80 a 0,86 α de Cronbach). Basándose en el resultado de CCI

=0,90 (IC del 95% 0,86 hasta 0,93) fue considerado como una excelente fiabilidad test-retest. El

EEM y el MCD se calcularon como 2,4 y 7 puntos respectivamente. En la puntuación total

IDD-CF se observó una correlación moderada con la mayoría de los cuestionarios evaluados (r

= desde 0,36 hasta 0,52) y una fuerte correlación con el IDC (r = 0,65, p <0,001). El IDC, la

EVA y la TSK-11 fueron predictores del IDD-CF.

Conclusiones

El IDD-CF mostró buenas propiedades psicométricas. Con base en los hallazgos de este estudio,

el IDD-CF se puede utilizar en la investigación y la práctica clínica para la evaluación de los

pacientes con DCF.

Background: Orofacial pain, headaches, and neck pain are very common pain conditions in the general population and might be associated in their pathophysiology, although this is not yet clarified. The development and validation of a prediction inventory is important to minimize risks. Most recent questionnaires have not focused on pain, but pain is the common symptom in temporomandibular disorders, headaches, and neck pain. It is necessary to provide tools for these conditions.

Objectives: The purpose of this study is to present the development and analysis of the factorial structure and psychometric properties of a new self-administered questionnaire (Craniofacial Pain and Disability Inventory [CF-PDI]) designed to measure pain, disability, and functional status of the mandibular and craniofacial regions.

Study Design: Multicenter, prospective, cross-sectional, descriptive survey design. A secondary analysis of the reliability of the measures was a longitudinal, observational study.

Setting: A convenience sample was recruited from a hospital and 2 specialty clinics in Madrid, Spain.

Methods: The study sample consisted of 192 heterogeneous chronic craniofacial pain patients. A sub-sample of 106 patients was asked to answer the questionnaire a second time, to assess the test-retest reliability. The development and validation of the CF-PDI were conducted using the standard methodology, which included item development, cognitive debriefing, and psychometric validation. The questionnaire was assessed for the following psychometric properties: internal consistency (Cronbach’s α); floor and ceiling effects; test-retest reliability (Intraclass Correlation Coefficient [ICC]; Bland and Altman method); construct validity (exploratory factor analysis); responsiveness (standard error of measurement [SEM] and minimal detectable change [MDC]); and convergent validity (Pearson correlation coefficient), by comparing visual analog scale (VAS), the Tampa Scale for Kinesiophobia (TSK-11), the Pain Catastrophizing Scale (PCS), the Neck Disability Index (NDI), and the Headache Impact Test-6 (HIT-6). Multiple linear regression analysis was used to estimate the strength of the associations with theoretically similar constructs.

Results: The final version of the CF-PDI consists of 21 items. Exploratory factor analysis revealed 2 factors (“pain and disability” and “jaw functional status”), both with an eigenvalue greater than one, explaining 44.77% of the variance. Floor or ceiling effects were not observed. High internal consistency of the CF-PDI (Cronbach’s α: 0.88) and also of the 2 subscales (Cronbach’s α: 0.80 – 0.86) was confirmed. ICC was found to be 0.90 (95% confidence interval [CI] 0.86 – 0.93), which was considered to be excellent test-retest reliability. The SEM and MDC were 2.4 and 7 points, respectively. The total CF-PDI score showed a moderate correlation with most of the assessed questionnaires (r = 0.36 – 0.52) and a strong correlation with the NDI (r = 0.65; P < 0.001). The NDI, VAS, and TSK-11 were predictors of CF-PDI.

Limitations: Only self-reported measures were considered for convergent validity. Future research should use physical tests to explore the clinical signs relating to pain and disability.

Prospective Evaluation

Craniofacial Pain and Disability Inventory (CF-PDI): Development and Psychometric Validation of a New Questionnaire

From: 1Department of Physiotherapy, Faculty of Health Science, The Center

for Advanced Studies University La Salle. Universidad Autónoma de Madrid, Aravaca, Madrid, Spain;

2Research Group on Movement and Behavioral Science and Study of Pain,

The Center for Advanced Studies University La Salle, Universidad

Autónoma de Madrid; 3Institute of Neuroscience and Craniofacial Pain

(INDCRAN), Madrid, Spain; 4Hospital La Paz Institute for Health Research (IdiPAZ), Madrid, Spain; 5Faculty of

Medicine, Universidad San Pablo CEU, Madrid, Spain; 6Department

of Methodology of the Behavioural Sciences, Faculty of Psychology,

Universidad Nacional de Educación a Distancia, Madrid, Spain;

7Department of Neurology, Hospital Universitario La Paz, Madrid, Spain;

8Department of Physical Therapy, Occupational Therapy, Rehabilitation

and Physical Medicine, Universidad Rey Juan Carlos, Alcorcón, Madrid,

Spain

Address Correspondence: Roy La Touche

Facultad de Ciencias de la SaludCentro Superior de Estudios

Universitarios La SalleCalle la Salle, 10  

28023 Madrid SPAINEmail: [email protected]

Disclaimer: There was no external funding in the preparation of this

manuscript. Conflict of interest: Each author certifies that he or she, or a

member of his or her immediate family, has no commercial

association (i.e., consultancies, stock ownership, equity interest, patent/licensing arrangements, etc.) that

might pose a conflict of interest in connection with the submitted

manuscript.

Manuscript received: 06-21-2013 Accepted for publication: 08-25-2013

Free full manuscript:www.painphysicianjournal.com

Roy La Touche, PT, MSc1-3, Joaquín Pardo-Montero PhD1-3, Alfonso Gil-Martínez PT, MSc1-4, Alba Paris-Alemany PT, MSc2,3, Santiago Angulo-Díaz-Parreño MSc2,5, Juan Carlos Suárez-Falcón PhD6, Manuel Lara-Lara, MD7, and Josué Fernández-Carnero, PT, PhD2,8

www.painphysicianjournal.com

Pain Physician 2014; 17:95-108 • ISSN 1533-3159

Conclusion: The CF-PDI showed good psychometric properties. Based on the findings of this study, the CF-PDI can be used in research and clinical practice for the assessment of patients with craniofacial pain.

Key words: Craniofacial pain, temporomandibular disorders, headache, neck pain, disability, development, questionnaire, reliability, psychometric validation, minimal detectable change

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96 www.painphysicianjournal.com

disability or dysfunction but not on pain, even though pain is the common symptom in TMD, headaches, and neck pain. Additionally, pain is been addressed by other validated scales (19).

For clinical practice and research, it is necessary to have tools to measure neck pain and the associated dis-ability (20). In addition, the development and validation of a prediction inventory allows the minimization of risks and helps prevent the development of the disease.

The purpose of this study is to present the de-velopment and analysis of the factorial structure and psychometric properties of a new self-administered questionnaire (Craniofacial Pain and Disability Inven-tory [CF-PDI]) designed to measure pain, disability, and functional status of the mandibular and craniofacial regions.

Methods

The development and validation of the CF-PDI was conducted in a standardized manner, using an accepted measure development methodology that included 3 phases (21): a) item development and identification of domains; b) pilot testing on a small number of patients with

cognitive debriefing; and c) psychometric validation.

Item DevelopmentItems were generated through a multi-step process

(21): 1) literature review; 2) patient interviews and focus group; 3) examination by the research group; 4) item writing and selection; and 5) examination of the inventory by independent

experts.

The relevant scientific literature search was con-ducted using electronic databases (Medline, Embase, CINAHL). The extracted information was related to the diagnosis, pathophysiology, comorbidities, and psycho-

Chronic orofacial pain and temporomandibular disorders (TMD) are commonly associated but may also arise from other sources (1). Orofacial

pain is a common pain condition associated with the hard and soft tissues of the face and mouth. Its prevalence in the general population is approximately 13% (2). Headache and neck pain are also 2 of the most common symptoms seen in the general population (3,4).

TMD, headaches, and neck pain are related dis-eases and share signs and symptoms (5-7). Some clinical evidence of the interconnection between the cervical spine and TMD has been demonstrated (8). Plesh et al (9) showed that 53% of patients with TMD had severe headache and 54% had neck pain. Besides, 59% with TMD reported at least 2 comorbid pains, and women reported more comorbid pain than men (9). This rela-tionship between headache and a causative disorder is a criterion for secondary headache diagnoses (10).

Although it has been suggested that TMD and headaches may be related in their pathophysiology (7,11) and that headache could be a possible risk factor for the development of neck pain (12), the pathophysi-ological mechanisms underlying these pain conditions are still not fully clarified. However, a biopsychosocial approach to the etiology, assessment, and treatment of chronic pain is widely advocated (13).

Nearly 60% of both men and women reported recent pain of moderate-to-severe intensity, with a quarter of them indicating interference or termination of work-related activities (14). Therefore, the correct diagnosis of these diseases is very important to reduce their huge economic impact (15,16).

A useful scale is the Jaw Functional Limitation Scale (JFLS), which consists of 3 constructs comprising a total of 20 items identified along a global scale (17). At present, there are no questionnaires in Spanish to as-sess these characteristics. This fact is especially relevant considering that Spain is one of the European Union countries with a high cost for these disabilities (18).

Moreover, most questionnaires have focused on

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Psychometric Validation of the Craniofacial Pain and Disability Inventory

social and disability factors associated with craniofacial pain. We found 5 published questionnaires that assess orofacial pain and jaw function (22-26). All of them were only validated in the English language. On the ba-sis of the existing literature, a semi-structured interview guide was developed focusing on the following 3 main areas: 1) perception of physical and psychosocial health in

relation to craniofacial pain; 2) patient-perceived physical impacts of the condition

(including impacts on general physical functioning and specific jaw function); and

3) perception of disability and pain associated with their condition.

A total of 13 patients with chronic craniofacial pain underwent the semi-structured interview and 5 patients with the same condition participated in the focus group. Both processes ended with the question: “Do you think there are any other aspects of craniofacial pain we have not discussed?” The research group proceeded to ana-lyze and compare the information extracted from semi-structured interviews, focus group, and review of the relevant literature to generate the construct concept of the CF-PDI and subsequently to write the items. A list of 30 draft items was generated. The research group then selected 22 items based on a finely structured consensus process (27) to not omit any necessary concepts.

The 22 items of the inventory were subjected to an external assessment by a group of experts in cra-niofacial pain (3 physiotherapists, one dentist, and one medical doctor). The 5 experts assessed whether each of the items had a relationship with the conditions of craniofacial pain and TMD, through a 3-level Likert scale (complete disagreement, neither agreement nor disagreement, and complete agreement).

Cognitive DebriefingCognitive debriefing of the preliminary CF-PDI

was conducted with a small number of patients to as-sess their interpretations of the questions (24 patients with craniofacial pain in the pilot test). Patients were selected from 3 different educational levels (primary school, secondary school, and university) and the total response time for all items of the CF-PDI was calculated. These patients were asked to complete the preliminary CF-PDI, and were then interviewed about its compre-hensiveness, relevance, and clarity of expression. This led to some minor alterations to the questionnaire.

Psychometric Validation

Sample/PatientsThis study employed a prospective, cross-sectional,

descriptive design. A consecutive convenience sample was recruited from outpatients of the Hospital Univer-sitario La Paz (Madrid, Spain) and 2 private clinics spe-cializing in craniofacial pain and TMD (Madrid, Spain). Patients were selected if they met all of the following criteria: 1) headache and facial pain, the diagnosis of which was made according to the guidelines of the In-ternational Classification of Headache Disorders (10); 2) headache or facial pain attributed to TMD (10), the di-agnosis of which was based on the Research Diagnostic Criteria for TMD (28,29) to classify patients with painful TMD (myofascial pain, temporomandibular joint [TMJ] arthralgia, or TMJ osteoarthritis); 3) pain history of at least 6 months prior to the study; 4) at least 18 years of age; and 5) good understanding of the Spanish language. The exclusion criteria were as follows: cogni-tive impairment; the presence of psychiatric limitations that impede participation in the study assessments; and poor knowledge of the Spanish language. To assess the test-retest reliability of the CF-PDI, a sub-sample of 106 patients whose clinical conditions were stable were asked to answer the inventory a second time, after an interval of 12 days.

The study was conducted in accordance with the Declaration of Helsinki and was approved by the local ethics committee of the Hospital Universitario La Paz (PI-1241). Prior to their participation, subjects gave written informed consent.

After consenting to the study, recruited patients were given a battery of questionnaires to complete on the day of the visit. These included various self-reports for demographic and pain-related variables, including the CF-PDI to be validated, a visual analog scale (VAS) for pain intensity, and the validated Spanish versions of the Tampa Scale for Kinesiophobia (TSK-11), the Pain Catastrophizing Scale (PCS), the Neck Disability Index (NDI), and the impact associated with headache was assessed using the Headache Impact Test-6 (HIT-6). The sociodemographic questionnaire collected information about gender, date of birth, marital status, living ar-rangements, education level, and work status.

Pain intensity was measured with the VAS. The VAS consists of a 100 mm line, on the left side of which represents “no pain” and the right side represents “the worst pain imaginable.” The patients placed a mark on

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the line where they felt best represented their pain intensity (30).

The Spanish version of the TSK-11 is a self-reported questionnaire that assesses fear of re-injury due to movement (31). The TSK-11 is an 11-item questionnaire that eliminates psychometrically poor items from the original version of the TSK (32) to create a shorter ques-tionnaire with comparable internal consistency. The TSK-11 has a 2-factor structure: activity avoidance and harm, and has demonstrated acceptable psychometric properties (31).

The Spanish version of the PCS assesses the degree of pain catastrophization (33,34). The PCS has 13 items and a 3-factor structure: rumination, magnification, and helplessness. The theoretical range is between 0 and 52, with lower scores indicating less catastrophizing. The PCS has demonstrated acceptable psychometric proper-ties (33).

The Spanish version of the NDI measures perceived neck disability (20,35). This questionnaire consists of 10 items, with 6 possible answers that represent 6 levels of functional capacity, ranging from 0 (no disability) to 5 (complete disability) points. The NDI has demonstrated acceptable psychometric properties (20).

The Spanish version of the HIT-6 (36,37) is a 6-item questionnaire that measures the severity and impact of headache on the patient’s life. The HIT-6 has demon-strated acceptable psychometric properties (38).

Statistical AnalysisSocio-demographic and clinical variables of the pa-

tients were analyzed. Analysis of variance (ANOVA) was used to test for differences in socio-demographic and clinical characteristics between the groups of patients.

Weighted kappa statistics (39) were calculated to assess the percentage agreement between external expert evaluators. Kappa statistics were calculated for each item. The Kappa coefficient varies from -1 (com-plete disagreement) to +1 (complete agreement), with 0 representing neither agreement nor disagreement.

Factor AnalysisThe factor structure was investigated using an

explorative factor analysis (ie, principal component analysis [PCA]) with Oblimin rotation. The number of factors for extraction was based on Kaiser’s eigenvalue criterion (eigenvalue ≥1) and evaluation of the scree plot (40). The quality of the factor analysis models was assessed using Bartlett’s test for sphericity and the Kai-ser-Meyer-Olkin (KMO) test. Bartlett’s test is a measure

of the probability that the initial correlation matrix is an identity matrix and should be < 0.05 (41). The KMO test measures the degree of multicollinearity and varies between 0 and 1 (should be greater than 0.50 – 0.60) (42).

Reliability For reliability, internal consistency and reproduc-

ibility were examined. Internal consistency was estimat-ed using Cronbach’s α and item total correlation coef-ficients. For a questionnaire to be internally consistent, α levels should be above 0.7 (43).

The test-retest reliability (repeatability) was evalu-ated using the Intraclass Correlation Coefficient (ICC). An ICC value above 0.70 is considered acceptable (44). We also constructed a Bland Altman Plot by calculating the mean difference between 2 measurements and the standard deviation (SD) of the difference (45). In this plot, 95% of the differences are expected to be less than 2 SDs.

Floor and Ceiling EffectsPotential floor and ceiling effects were measured

by calculating the percentage of patients indicating the minimum or maximum possible scores in the question-naires. Floor and ceiling effects are considered to be present if more than 15% of respondents achieved the highest or lowest possible total score (44).

Responsiveness AnalysesMeasurement error is the systematic and random

error of a patient’s score that is not attributable to true changes in the construct to be measured (46). Measure-ment error is expressed as a standard error of measure-ment (SEM), which is calculated as:

SD where SD is the SD of values from all participants

and ICC is the reliability coefficient (47,48). Ostelo et al (49) suggested that the percentage of the SEM in rela-tion to the total score of a questionnaire is an impor-tant indicator of agreement, and can be interpreted as follows: ≤ 5% very good; > 5% and ≤ 10% good; > 10% and ≤ 20% doubtful; and > 20% negative. Responsive-ness was assessed with the Minimal Detectable Change (MDC). The MDC expresses the minimal magnitude of change required to be 95% confident that the observed change between the 2 measures reflects real change and not just measurement error (50). It is calculated as SEM × × 1.96 (50,51).

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Convergent Validity The convergent validity was assessed by the Pear-

son correlation coefficient between the CF-PDI and the other questionnaires: VAS, TSK-11, PCS, NDI, and HIT-6. A strong correlation was considered to be over 0.60; a moderate correlation between 0.30 and 0.60; and a low (very low) correlation below 0.30 (44).

Linear RegressionMultiple linear regression analysis was used to esti-

mate the strength of the associations with theoretically similar constructs, so multiple linear regression analyses were also performed including CF-PDI as a criterion variable to estimate the strength of the association between CF-PDI and NDI, PVAS, TSK, and PCS as pre-dictor variables. As a measure of multicollinearity, the variance inflation factor (VIF) is presented (VIF < 10 indicates no problem with multicollinearity).

All statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS), version 20 (IBM company, USA) except for the SEM and MDC values, which were calculated using Microsoft Excel. The critical value for significance was P < 0.05.

Results

Item Development and Cognitive DebriefingA total of 18 patients with chronic craniofacial

pain participated in the focus group and were also interviewed in May 2011 and July 2011, and 30 items were pooled as potential questions. After a review by the research group, some questions were added, and 22 items covering 4 aspects (quality of life, jaw functional status, avoidance behavior, and pain) were finally gen-erated. There was agreement among the expert evalu-ators who reviewed the items, with a kappa coefficient of 0.83. The greatest disagreement occurred in items 8 and 20.

A pilot test for cognitive debriefing was performed in 24 patients in September 2011 to examine the con-tent validity of the preliminary questionnaire in regards to relevance and clarity of the language. The mean ± SD age of the patients was 45.7 ± 13.5 years (range: 19 – 61), and 17 of the participants were women (70.8%). The time required to answer all the questions was 8.4 ± 3.1 minutes (range: 5.4 – 12.6). More than 96% of the patients could easily answer the questionnaire.

Characteristics of the SampleThe final study sample consisted of 192 heteroge-

neous chronic craniofacial pain patients (68.8% women, one patient was of unknown gender) aged 19 – 78 years (mean ± SD: 46.00 ± 13.06). The vast majority of patients (28.1%) had myofascial pain diagnoses; other patients suffered from TMJ arthralgia (15.1%), headache or fa-cial pain attributed to TMD (myofacial pain/TMJ osteo-arthritis or arthralgia) (24.5%), combined tension-type headache and myofascial pain (16.7%), and migraine (15.6 %). The mean time of pain was 130.46 ± 151.44 months (range: 15 – 888), and 19 patients (9.9%) had received disability benefits. Educational levels in our sample were primary (23.4%), secondary (36.5%), and university graduates (25.0%); there was no information for 15.1% of our sample.

Distribution of Total CF-PDI ScoresThe distribution of CF-PDI scores did not differ

significantly from a normal symmetric distribution (skewness = 0.43, SE = 0.18; kurtosis = -0.36; SE = 0.35), Kolmogorov-Smirnov Z = 1.11 (P = 0.172). There were no significant differences in scoring between men (19.46 ± 9.04) and women (20.52 ± 9.22). There was no significant association between CF-PDI scores and age, marital status, average duration of pain, education level, or work status.

Only the type of diagnosis showed differences in the median score of CF-PDI, headache or facial pain attributed to the TMD (myofacial pain/TMJ osteoarthri-tis or arthralgia) group presented higher scores 28.62 ± 7.10; TMJ arthralgia, 14.2 ± 5.24; migraine, 17.93 ± 12.30; myofascial pain, 18.17 ± 6.44; combined tension-type headache and myofascial pain, 19.00 ± 7.05. The distribution of CF-PDI total scores and other principal scales are shown in Table 1.

Table 1. Descriptive statistics and estimates of internal consistency (N = 192).

Instrument Mean (SD) Range Alpha

CF–PDI 20.24 (9.15) 2–48 0.88

Pain and Disability 15.43 (6.77) 1–34 0.86

Jaw Functional Status 4.81 (3.57) 0–14 0.80

HIT–6 54.48 (7.67) 36–74 0.85

NDI 16.96 (6.00) 0–42 0.74

TSK–11 25.40 (7.08) 11–44 0.88

PCS 23.86 (8.90) 7–52 0.84

VAS 52.94 (13.83) 15–85 –––

CF-PDI, craniofacial pain and disability inventory; VAS, visual analogue scale; TSK-11, Tampa Scale for Kinesiophobia; PCS, pain catastrophizing scale; NDI, Neck Dibility Index; HIT-6, headache impact test-6

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Internal ConsistencyCronbach’s α coefficient was 0.88 (95% CI = 0.86 –

0.91), indicating a high degree of internal consistency. The item-to-total correlation coefficients ranged from 0.32 to 0.73; no item dominated with an especially high correlation and no item appeared to be redun-dant. The previous item 20, “How long have you had pain?” was deleted in the final version and it increased slightly the Cronbach’s α coefficient. This item showed a strong positive skew, refers to the time of pain in our population, and shows limited information because all patients suffered from chronic pain. It was removed it; other results in Table 2.

Factor AnalysisIn order to explore the factorial structure of the

instrument, a PCA without rotation was conducted on the scores of our sample. We also attempted to con-struct one-, 2-, and 3-factor structures. A 2-factor solu-tion emerged in our sample using a PCA that explained 40.8% of the variance. The KMO was found to be 0.85, which exceeds the recommended minimum value of 0.60. Bartlett’s Test of Sphericity was highly significant (Chi square = 1467.10 P < 0.001), supporting the suit-ability of the data for PCA.

When factor loading smaller than 0.30 was sup-pressed, but there were no cases. The first factor (30.43% of the explanatory variance) was composed of 14 items (1, 2, 3, 4, 5, 6, 7, 8, 16, 17, 18, 19, 20 (previously 21), and 21 (previously 22); the second factor (10.39% of the explanatory variance) was composed of 7 items (9, 10, 11, 12, 13, 14, and 15). With these results and a visual inspection of the scree plot, a 2-factor solution was considered suitable (Fig. 1).

Regarding factor analysis, item 9 was not clearly classified into the assumed factor (with loadings un-der 0.35 in each of them). The results showed similar weights for both factors. Despite the unexpected load-ing of this item, the CF-PDI still showed appropriate internal consistency; therefore, we incorporated it into the jaw functional status domain for theoretical rea-sons. Results of the PCA are shown in Table 3.

Floor and Ceiling EffectsNo floor or ceiling effects were identified for the

whole scale. Only 9.3% of the respondents scored the lowest possible score of 0 in the jaw functional status subscale, and none of the craniofacial pain patients scored the highest possible score of 63 points on the CF-PDI.

Table 2. Corrected item-total between CF-PDI items (N = 192)

Scale mean if item deleted

Corrected item-total correlation

Squared multiple correlation

Cronbach's α if item deleted

1 18.65 0.73 0.63 0.87

2 18.72 0.46 0.37 0.88

3 18.58 0.54 0.55 0.88

4 19.61 0.47 0.56 0.88

5 19.82 0.53 0.51 0.88

6 19.88 0.34 0.31 0.88

7 19.19 0.50 0.36 0.88

8 19.56 0.35 0.23 0.88

9 19.49 0.32 0.21 0.88

10 19.30 0.59 0.57 0.87

11 19.34 0.53 0.54 0.88

12 19.41 0.41 0.48 0.88

13 19.70 0.55 0.54 0.88

14 19.79 0.40 0.50 0.88

15 19.83 0.43 0.46 0.88

16 18.29 0.64 0.56 0.87

17 18.58 0.57 0.46 0.87

18 19.33 0.44 0.30 0.88

19 19.30 0.44 0.37 0.88

20 19.22 0.47 0.36 0.88

21 19.19 0.38 0.25 0.88

Fig. 1. Scree plot of the 21 items of the CF-PDI.

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Psychometric Validation of the Craniofacial Pain and Disability Inventory

Test-Retest ReliabilityThe response to the CF-PDI provided by a random

subsample of 106 patients (gender women: 70, 66.7%; age: 45.6 ± 12.9 years; duration of the disorders: 69.0 ± 46.2 months) showed satisfactory temporal stability of

the scale after 12 days. ICC based on absolute agree-ment measures was 0.90 (95% CI: 0.86 – 0.93). The con-structed Bland and Altman plot for test-retest agree-ment showed a good reliability for total CF-PDI score

Table 3. Items of CF-PDI distribution and factor loadings according to principal component analysis with Oblimin rotation including Kaiser correction (N = 192).

Factor 1 Factor 2

1 ¿Presenta dolor en la cara? Do you feel any pain in your face? 0.79 0.45

2 ¿Se ha visto afectada su calidad de vida por esta dolencia? Is your quality of life affected by this pain? 0.58 0.21

3 Intensidad de dolor en la cara. Pain intensity on your face. 0.68 0.23

4 Le incapacita su dolor a la hora de tener relaciones afectuosas del tipo: besos, abrazos, relaciones sexuales… Does the pain make you unable to have emotional relationships, such as: kisses, embraces, or sexual relationships?

0.69 0.06

5 ¿Tiene dolor al reír? Do you feel any pain when you laugh? 0.68 0.19

6 ¿Su dolencia hace que evite el sonreír, hablar o masticar?Does your condition make you avoiding smiling, talking or chewing? 0.44 0.13

7. ¿Tiene dolor en la mandíbula?Do you feel any pain in your jaw? 0.53 0.38

8 ¿Escucha algún ruido al mover la mandíbula?Do you hear any noise when you move your jaw? 0.40 0.23

9. ¿Nota que su mandíbula se le sale o se le traba?Do you feel your jaw getting out of place or getting stuck? 0.33 0.31

10. Intensidad de dolor al masticarPain intensity when chewing 0.47 0.72

11. ¿Siente cansancio en la mandíbula, al hablar o al comer?Do you feel any tiredness in your jaw when you talk or eat? 0.38 0.73

12. ¿Tiene dificultad para abrir la boca?Do you have any trouble when you open your mouth? 0.23 0.73

13. Intensidad de dolor al hablarPain intensity when talking. 0.40 0.74

14. ¿Tiene miedo de mover la mandíbula?Do you fear moving your jaw? 0.20 0.73

15. Alimentación.Nutrition 0.24 0.72

16. ¿Con qué frecuencia tiene dolor en el cuello?How often have you got any neck pain? 0.76 0.31

17.¿Con qué frecuencia tiene dolor de cabeza?How often do you have a headache? 0.61 0.41

18. ¿Con qué frecuencia tiene dolor de oído?How often do you have an earache? 0.47 0.34

19. ¿Qué siente al tocarse la zona dolorosa?What do you feel when you touch the painful area? 0.53 0.23

20 ¿Su dolor le altera el sueño?Does the pain disrupts your sleep? 0.59 0.21

21 ¿El dolor le interfiere a la hora de desempeñar su actividad laboral?Does the pain interfere in your work? 0.38 0.36

and 2 subscales (Figs. 2-4). The results of reliability and responsiveness analy-ses are summarized in Table 4.

Convergent ValidityThe total CF-PDI score was signifi-

cantly associated with all the assessed questionnaires (Table 5), but the cor-relation with the NDI, was the most important in our sample.

Linear RegressionThe resulting beta coefficients,

ranging from 0.50 to 0.17, indicate independent contribution of each scale to the prediction of CF-PDI, the criteri-on variable. NDI, VAS, and TSK-11 were predictors of CF-PDI, significance < 0.05 (as illustrated by the higher standard-ized coefficients [beta] and P-values). NDI was the most important variable (Table 6). PCS and HIT-6 were excluded as predictor variables this time.

discussion The present study describes a

methodical approach to the develop-ment and validation of a new self-ad-ministered questionnaire to measure disability, pain, and functional status of the mandibular and craniofacial region in patients with craniofacial pain. Our results demonstrate that the CF-PDI is psychometrically valid and reliable. In addition, the instrument has proven to be easy to complete, and only requires a relatively short time to administer. The CF-PDI was de-veloped in Spain for Spanish patients with craniofacial pain and TMD. How-ever, since the CF-PDI does not contain items that are specifically related to Spanish culture, it could be translated and used internationally.

The design of the CF-PDI was based on a biopsychosocial approach. This conceptual model, recommended by the International Classification of Functioning Disability and Health (52,53), can assess the disease from a

Fig. 2. Bland Altman plot illustrating the test-retest reliability of the CF-PDI. A total of 106 patients participated in the test-retest assessment. The central line representing the mean difference between test and retest scores, which was - 2.22, and the 95% limits of agreement are presented as flanking lines.

Fig. 3. Bland Altman plot illustrating the test-retest reliability of the Pain and Disability subscale. A total of 106 patients participated in the test-retest assessment. The central line representing the mean difference between test and retest scores, which was -1,73, and the 95% limits of agreement are presented as flanking lines.

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Psychometric Validation of the Craniofacial Pain and Disability Inventory

Fig. 4. Bland Altman plot illustrating the test-retest reliability of the Jaw Functional Status subscale. A total of 106 patients participated in the test-retest assessment. The central line representing the mean difference between test and retest scores, which was -0.49, and the 95% limits of agreement are presented as flanking lines.

Table 4. Descriptive statistics, test-retest reliability, and responsiveness results (N = 106)

DomainsTest Retest

ICC 95% CI SEM MDCMean SD Mean SD

CF-PDI 20.57 8.42 22.79 7.80 0.90 0.86-0.93 2.48 6.87

Pain and Disability 15.37 6.13 17.10 5.26 0.86 0.81-0.90 2.10 5.82

Jaw Functional Status 5.20 3.39 5.69 3.93 0.86 0-80-0.90 1.35 3.75

CF-PDI, craniofacial pain and disability inventory; SD, standard deviation; ICC, intraclass correlation coefficient; 95% CI, 95% confidence interval; SEM, standard error of measurement; MDC, minimal detectable change

broader perspective, and provides an understanding of health, functioning, and disability. In addition, research sup-ports that clinical diagnosis is sometimes insufficient to explain patients’ pain and disability (54-56).

The scree plot and exploratory fac-tor analysis revealed a 2-factor solution. Both factors had eigenvalues greater than 1. PCA indicated that a satisfactory percentage of total variance (40.8%) was explained by the 2 factors. The CF-PDI contains 21 items divided into 2 subscales according to their content and exploratory factor analysis: “pain and disability” and “jaw functional status.”

High internal consistency was shown for the CF-PDI (Cronbach’s α: 0.88) and also for the 2 subscales (Cron-bach’s α: 0.80 – 0.86). These data are similar to the results from other research questionnaires used to assess facial pain and mandibular function (22-25,57,58).

Table 5. Pearson Correlation Coefficient of our principles scales (N = 192).

CF-PDI Pain and Disability Jaw Functional Status

VAS 0.46** 0.50** 0.23**

NDI 0.65** 0.69** 0.37**

PCS 0.46** 0.50** 0.25**

PCS rumiation 0.34** 0.35** 0.22**

PCS magnification 0.51** 0.52** 0.32**

PCS Helplessness 0.39** 0.45** 0.16*

TSK-11 0.40** 0.41** 0.26**

HIT6 0.38** 0.46** 0.09

** P < 0.01; * P < 0.05Abbreviations: CF-PDI, craniofacial pain and disability inventory; VAS, visual analogue scale; TSK-11, Tampa Scale for Kinesiophobia; PCS, pain catastrophizing scale; NDI, Neck Disability Index; HIT-6, headache impact test-6

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In this study, we choose a retest interval of 12 days (approximately), in order to avoid variations in clinical status and patients remembering their previous an-swers. A longer interval for a test-retest study of health may be inappropriate as fluctuations in the patient’s health status can occur (59). In relation to this, Streiner and Norman suggested that a retest interval of 2 to 14 days is generally acceptable (60).

The test-retest reliability for the total CF-PDI score was considered to be excellent (ICC: 0.90; 95% CI: 0.86 – 0.93). Also, we were able to verify that the test-retest reliability was high for each subscale.

The measurement of SEM was 2.4 points, corre-sponding to 11.7% of the mean CF-PDI values and 3.8% of the maximum possible score. Based on the SEM, the MDC was 7 points (34.5% of mean values). Considering that the score of the questionnaire ranges from 0 to 63 points, 7 points represents 11.1% of the maximum pos-sible score, which means that the CF-PDI is able to de-

tect very small changes. Changes higher than the MDC can be interpreted as real and not due to measurement error, with an acceptable probability level. These results may help to calculate the sample size of future studies aiming to assess the effectiveness of craniofacial pain interventions.

Construct validity was evidenced by significant cor-relations between the CF-PDI with all the questionnaires and scales used in the validation process. A moderate correlation between CF-PDI with the HIT-6 and the VAS (r = 0.38 – 0.46) was observed. In addition, the PCS and TSK-11 showed moderate correlation with the CF-PDI and the pain and disability subscale (r = 0.36 – 0.52). This is consistent with recent evidence demonstrating that patients with craniofacial pain or craniomandibular dis-orders report higher levels of catastrophizing (61-63). Furthermore, pain-related catastrophizing has been associated with the progression of pain intensity and signs of disability in chronic craniofacial pain (64-68).

Table 6. Multiple linear regression models with CF-PDI (A), pain and disability (B), and jaw functional status (C) as criterion variable, and NDI, VAS, TSK-11, PCS as predictor variables (N = 192).

Criterion variable Predictor variablesRegression coefficient

(B)

Standardized coefficient (β)

Significance (P) VIF

A. CF-PDI

NDIVASTSK-11

0.770.130.22

0.500.190.17

0.0000.0010.004

1.371.261.17

Excluded variables

PCS-TotalHIT-6

----

0.080.01

0.2530.905

1.621.46

B. Pain and Disability

NDIPCS-MagnificationVAS

0.550.680.10

0.490.250.21

0.0000.0000.000

1.371.261.17

Excluded variables

PCS-TotalTSK-11HIT-6PCS-RumiationPCS-Helplessness

----------

-0.500.090.08-0.06-0.00

0.4800.0980.1590.3140.968

0.400.770.680.700.61

C. Jaw Functional Status

NDIPCS-magnification

0.170.28

0.290.20

0.0000.007

1.221.22

Excluded variables

PCS-TotalTSK-11HIT-6PCS-RumiationPCS-HelplessnessVAS

------------

-0.130.09-0.13-0.00-0.160.06

0.2070.2580.0760.9680.0590.436

2.491.291.331.421.651.26

CF-PDI, craniofacial pain and disability inventory; VAS, visual analogue scale; TSK-11, Tampa Scale for Kinesiophobia; PCS, pain catastrophizing scale; NDI, Neck Dibility Index; HIT-6, headache impact test-6, VIF, variance inflation factor

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Previous research demonstrated the relationship between fear of jaw movements and craniofacial pain (69,70), but only limited evidence supports it. However, there is higher evidence showing that pain-related fear is associated with reduced activities in daily life and is also a strong predictor of disability in other chronic musculoskeletal disorders (71-75).

Pain catastrophizing and pain-related fear are 2 constructs that have been linked to the chronicity of musculoskeletal pain through the “fear avoidance model” (76). Based on the results of multiple linear regression analysis, pain intensity (VAS: β = 0.19, P = 0.001) and fear of pain and movement (TSK-11: β = 0.17, P = 0.004) were predictors of CF-PDI. For jaw functional status, and pain and disability, the variable predictor was pain catastrophizing (PCS-Magnification: β = 0.25, P < 0.001; β = 0.20, P = 0.007).

The principal predictor for CF-PDI and the 2 sub-scales was the variable of neck disability (NDI: β = 0.29 – 0.50, P < 0.001). In addition, a strong correlation was observed between CF-PDI and pain and disability factor with NDI (r = 0.65 – 0.69). This is in line with the results of Olivo et al (77) who described a strong relationship between neck disability and jaw disability (r = 0.82). Several studies have reported the high prevalence and comorbidity between orofacial pain, TMD, headache, and neck pain (65,78-81). Our findings suggest the importance of taking into account the neck disability questionnaires when assessing patients with craniofa-cial pain.

Limitations Our study has several limitations. First, there is

a gender disproportion as the sample had a smaller proportion of men. However, our findings showed no significant differences in scoring between genders. The evidence suggests that the prevalence of craniofacial pain is higher in women (82).

The second limitation of this study is that we did not assess the CF-PDI in healthy subjects; the sample consisted of patients with chronic pain. Further

studies will need to be performed to assess the dis-criminant power of the CF-PDI for specific diagnostic entities.

The sample size was sufficient to test the new in-strument’s reliability, convergence validity, and explor-atory factor analysis. However, it was too small to be able to carry out confirmatory factor analysis. Kline has suggested a sample size of 10 – 15 subjects per item to perform this statistical analysis (83). It should be noted that statisticians disagree on the issue of appropriate sample size for confirmatory factor analyses. In relation to this, DeVellis stated that as the sample size becomes larger, the relative number of respondents per item can diminish (84), and that a sample of 200 is adequate in most studies (85).

Another limitation is that only self-reported mea-sures were considered for convergent validity. Future research should use physical tests to explore the clinical signs relating to pain and disability, and assess whether these are associated with the CF-PDI.

The last limitation of the study is the cross-sectional design, which prevented us from investigating the abili-ty of the CF-PDI to detect responsiveness to change over time. Although in this study we investigated in a short period of time the reproducibility and the MDC, a longi-tudinal study or one with an experimental design with a follow-up period would be required to understand how CF-PDI scores change over time. Furthermore, such a study would allow us to obtain information such as the Minimum Clinically Important Difference.

conclusion Evidence has shown that the CF-PDI has a good

structure, internal consistency, reproducibility, and construct validity, and provides an objective tool for as-sessing pain and disability in craniofacial pain patients. Neck disability showed a strong association with the CF-PDI, and is also a significant predictor of the construct. Based on the findings of this study, the CF-PDI could be used in research and clinical practice for the assessment of treatment outcomes.

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138

5.5 Estudio V

La Touche R, Paris-Alemany A, Gil-Martínez A, Pardo-Montero J, Angulo-Díaz-Parreño S,

Fernández-Carnero J. The Influence of Neck Disability and Pain Catastrophizing about

Trigeminal Sensory-Motor System in Patients with Headache Attributed to Temporomandibular

Disorders. (En revisión)

Objetivos de estudio

Nuestro objetivo fue estudiar la influencia de la discapacidad y el dolor de cuello sobre las

variables sensoriales y motoras del trigémino en pacientes con cefalea atribuida a TCM.

Resultados

Los resultados de EVAF fueron mayores a 6 minutos (media 51,7, IC 95%: 50,15-53,26) y 24

horas después (21.08, IC 95%: 18,6-23,5) para las pruebas en el grupo que muestran

discapacidad moderada cuello en comparación con el grupo de discapacidad leve cuello (6

minutos, 44,16, IC del 95%: 42,65 a 45,67 / 24 horas después, 14,3; IC del 95%: 11,9-16,7) y el

grupo de control (6 minutos, 29.92, IC 95% 28,29-31,55 / 24 horas después, 4,65; IC del 95%:

2.5 a 7.24). El análisis muestra una disminución en el MAI sin dolor inmediatamente después de

las pruebas de todos los grupos y se observó que esta disminución sólo se mantuvo en el grupo

de discapacidad moderada 24 horas después de la prueba. Los UDPs de la región del trigémino

se redujeron inmediatamente en todos los grupos, mientras que a las 24 horas se observó una

disminución sólo en los grupos de pacientes. Los UDPs de la región cervical disminuyeron sólo

en el grupo con discapacidad cuello moderado 24 horas después de la prueba. La correlación

negativa más fuerte se encontró entre MAI sin dolor inmediatamente después de la prueba y el

IDC en ambos grupos: grupo de discapacidad leve (r = -0.49, P <0,001) y grupo de discapacidad

moderada (r = -0.54, P <0,001).

Conclusiones

Nuestros resultados sugieren que la discapacidad y dolor de cuello tienen una influencia en las

variables sensomotrices evaluados en pacientes con cefalea atribuida a TCM.

1

The Influence of Neck Disability and Pain Catastrophizing about Trigeminal

Sensory-Motor System in Patients with Headache Attributed to

Temporomandibular Disorders

Roy La Touche,1-4, Alba Paris-Alemany 1-4, Alfonso Gil-Martínez1-4, Joaquín Pardo-

Montero1-4, Santiago Angulo-Díaz-Parreño, Josué Fernández-Carnero,2,4,6.

1. Department of Physiotherapy, Faculty of Health Science, The Center for Advanced Studies

University La Salle. Universidad Autónoma de Madrid, Aravaca, Madrid, Spain.

2. Motion in Brains Research Group, The Center for Advanced Studies University La Salle,

Universidad Autónoma de Madird.

3. Institute of Neuroscience and Craniofacial Pain (INDCRAN), Madrid, Spain

4. Hospital La Paz Institute for Health Research, IdiPAZ. Madrid, Spain.

Madrid, Spain

5. Faculty of Medicine, Universidad San Pablo CEU, Madrid, Spain

6. Department of Physical Therapy, Occupational Therapy, Rehabilitation and Physical

Medicine, Universidad Rey Juan Carlos, Alcorcón, Madrid, Spain.

Address for reprint requests / Corresponding author:

Roy La Touche

Facultad de Ciencias de la Salud

Centro Superior de Estudios Universitarios La Salle.

Calle la Salle, 10

28023 Madrid

SPAIN

Telephone number: + 34 91 7401980 (EXT.256)

Fax number:

Email address: [email protected]

2

ABSTRACT

OBJECTIVE: Our purpose was to investigate the influence that neck pain and disability

may have on trigeminal sensory-motor variables in patients with headache attributed to

TMD.

METHODS: An experimental case-control study comprising 83 patients with headache

attributed to TMD and 39 healthy controls was done. Patients were grouped according

to their scores on the neck disability index (NDI) (mild and moderate neck disability).

Initial assessment included the visual analogue scale (VAS), pain catastrophizing scale,

NDI and the Headache Impact Test-6. The protocol consisted of baseline measurements

of pressure pain thresholds (PPT) for mechanical pain sensitivity in the trigeminal and

cervical region and the pain-free maximum mouth opening (MMO), performance of the

provocation chewing test, immediately after data collection and 24 hours after. During

the provocation chewing test, patients were assessed for subjective feelings of fatigue

(VAFS) and pain intensity, immediately and 24 hours after completion.

RESULTS: The VAFS were higher at 6 minutes (mean 51.7; 95% CI: 50.15-53.26) and

24 hours after (21.08; 95% CI: 18.6-23.5) for tests in the group showing moderate neck

disability compared with the mild neck disability group (6 minutes, 44.16; 95% CI

42.65-45.67/ 24 hours after, 14.3; 95% CI: 11.9-16.7) and the control group (6 minutes,

29.92; 95% CI 28.29-31.55/ 24 hours after, 4.65; 95% CI: 2.05-7.24). The analysis

shows a decrease in the pain-free MMO immediately after the tests for all groups and

this decrease was observed only in the group of moderate disability 24 hours after the

test. PPTs of the trigeminal region were decreased immediately in all groups, whereas at

24 hours a decrease was observed only in the groups of patients. PPTs of the cervical

region decreased only in the group with moderate neck disability 24 hours after the test.

The strongest negative correlation was found between pain-free MMO immediately

3

after the test and NDI in both groups: mild (r=-0.49; P<0.001) and moderate (r=-0.54;

P<0.001) neck disability group.

CONCLUSION: Neck pain and disability have an influence on the sensory-motor

variables evaluated in patients with headache attributed to TMD.

KEYWORDS: Temporomandibular disorders, headache, neck pain, pain

catastrophizing, disability.

4

.INTRODUCTION

Temporomandibular disorders (TMD), headaches and neck pain are very closely

related diseases[1]. Several studies have reported the overlapping signs and symptoms

among patients with TMD, headaches and neck pain, respectively[2, 3]. It has been

shown that neck pain complaints were also significantly associated with TMD[4, 5] and

that psychosocial factors have an influence on the presence of head, neck and orofacial

pain[3].

The prevalence of temporomandibular joint (TMJ) symptoms, orofacial pain,

neck pain and headache was assessed in 1339 non-patients. Often painless TMJ

symptoms were found in 10% of subjects, orofacial pain in 7%, headache in 15% and

neck pain in 39%[3]. Plesh et al. showed that 53% of patients with TMD had severe

headache and 54% had neck pain[6]. It has been suggested that TMD and headaches

may be involved in their pathophysiology[7, 8] and this headache could be a possible

risk factor for developing neck pain[9].

Recent research has shown a strong relationship between craniomandibular

disability and pain with cervical disability[10, 11]. Several experimental studies have

described functional connections between the craniofacial and cervical afferent fibres

via patterns of neural convergence of the trigeminal nucleus and the upper cervical

nociceptive neurons, which form a functional unit, the trigeminocervical complex[12–

18]. In relation to this, it has been observed in experimental studies that the pain

induced by the infiltration of algogenic substances in the masticatory or cervical

muscles can bi-directionally modify the activity of the stretch reflexes[13, 15]. Also, in

basic research, a reflex relationship has been observed between the activity of the

nociceptors of the TMJ and the activity of the fusimotor-muscle spindle system of the

cervical muscles[17]. This information is useful for proposing theories about the

5

influence of the cervical region over the possible nociceptive and sensory-motor

mechanisms involved in masticatory fatigue, pain and alterations in motor behaviour. At

present, there is insufficient information demonstrating the influence of neck pain and

disability in the sensory-motor activity in patients with trigeminal headache attribute to

TMD. This could be a key issue, since improvements could be made by changing the

diagnostic and therapeutic approach to these patients. We used the primary hypothesis

that neck disability is a factor influencing masticatory sensory-motor activity in patients

with headache attributed to TMD.

Headache attributed to TMD is classified as a secondary headache caused by a

disorder that affects the temporomandibular region[19]. The pain may be unilateral or

bilateral and is represented in the facial region, at the masseter and temporal region[19].

An important criterion for clinical diagnosis is that the headache occurs or is aggravated

by provocative manoeuvres (such as the palpatory pressure on the TMJ and masticatory

muscles) and/or mandibular active or passive movements[19, 20]. Recently, it has been

found that the diagnostic criteria that have greater sensitivity and specificity for this

type of headache are: 1) the provocation of pain by palpation of the temporalis muscle

or jaw movements and 2) the fact that pain changes with the movements of the jaw in

the function or parafunction[20, 21].

From the clinical point of view, it is important to identify changes in motor

behaviour that may be present in patients suffering TMD, especially knowing that a

percentage of these patients develop painful chewing[22, 23], difficulty performing jaw

movements[24] and masticatory fatigue[25, 26].

During the last decades, the relationship between masticatory muscle pain and

disordered jaw motor behaviour has been studied widely; see for example the review by

Svensson and Graven-Nielsen[27]. Pain may influence the characteristics of the

6

masticatory sensory-motor system[28]. Furthermore, Kurita et al. found a positive

correlation between chewing ability and TMJ pain and reduced mouth opening[29].

According to some researchers, fatigue and fatigue-related symptoms are reported

significantly more often by chronic TMD patients than by healthy volunteers[30]. In

addition, a recent study in patients with chronic orofacial pain demonstrated that fatigue

is mediated by psychosocial factors[31]. In this connection, Brandini et al. found a

positive association in TMD patients between mandibular kinematic variables and

psychological factors such as stress and depression[32].

Research or assessments based on a biobehavioural approach may offer a better

alternative for identifying patients with chronic TMD[33]; a biobehavioural approach to

the assessment and treatment of chronic pain is widely accepted[34]. A key point to

note about patients with headache attributed to TMD is that an association between

emotional functioning and increased frequency of headache has been found[35]. This

and previous findings lead us to propose integrating the assessment of psychological

factors with pain and disability associated with trigeminal sensory-motor variables in

this research. A significant amount of scientific evidence has shown the influence of

pain catastrophizing on several variables related to TMD[36–41]. This suggests the

hypothesis that pain catastrophizing has an association or is a predictor of some of the

trigeminal sensory-motor variables studied in this research.

The primary objective of this research is to investigate the influence that pain and

disability of the neck may have on trigeminal sensory-motor variables in patients with

headache attributed to TMD, and as a secondary objective we propose identifying

whether the psychological or disability variables have any association with the studied

sensory-motor variables.

7

MATERIALS AND METHODS

Study Design

This was an experimental case-control study. The assessor of sensory-motor

measurements was blinded. One researcher administered the participant appointments

and questionnaires, and also instructed the participant not to say anything that could

reveal their pain, disability trait or state. The reporting of the study follows the

“Strengthening the Reporting of Observational studies in Epidemiology” (STROBE

statement) [42].

After receiving detailed information about the experiment, the volunteers gave

their written informed consent. All of the procedures used in this study were planned

under the ethical norms of the Helsinki Declaration and were approved by the local

ethics committee.

Participants

A consecutive convenience sample of 83 patients with chronic headache

attributed to TMD and 39 healthy controls were recruited for the study. The sample was

recruited from outpatients of a Public Health Centre (Madrid, Spain) and two private

clinics specializing in craniofacial pain and TMD (Madrid, Spain). Patients were

selected if they met all of the following criteria: 1) Headache and facial pain attributed

to TMD, diagnosis was made according to the guidelines of the International

Classification of Headache Disorders[19]; 2) TMD diagnosis based on the Research

Diagnostic Criteria for TMD[43, 44] to classify patients with painful TMD (myofascial

pain, TMJ arthralgia and TMJ osteoarthritis); 3) pain symptoms history of at least the 6

months previous to the study; 4) pain in the jaw, temples, face, neck, pre-auricular area,

or in the ear during rest or function; 5) neck pain and disability and quantified according

to neck disability index (NDI)[45]; and 6) At least 18 years of age.

8

There were 83 patients categorized into two groups according to their scores on the

NDI[45]: 1) mild neck disability (NDI 5-14), and; 2) moderate neck disability (NDI 15-

24). The criteria for exclusion were: 1) a history of traumatic injuries (e.g., contusion,

fracture, or whiplash injury); 2) presence of fibromyalgia or other chronic pain disorder;

3) neuropathic pain (e.g., trigeminal neuralgia); 4) unilateral neck pain; 5) cervical spine

surgery, and; 6) clinical diagnosis of cervical radiculopathy or myelopathy.

Healthy controls were recruited from our academic university campus and the

local community through flyers, posters, and social media. Healthy participants were

examined and were included in the study only if they had no history of craniofacial

pain, headache or neck pain and had been free of any other painful disorders for the six

months prior to the experiment. All subjects had complete dentition, did not use any

medication, had no dental pathology and none were regular gum chewers. Subjects who

reported oral parafunctions (i.e., tooth grinding, tooth clenching) were excluded.

Experimental Protocol

After consenting for the study, recruited patients were given a battery of

questionnaires to complete on the first day of the experiment. These included various

self-reports for sociodemographic, psychological and pain-related variables, including

the visual analogue scale (VAS) for pain intensity and the validated Spanish versions of

the pain catastrophizing scale (PCS), the NDI and the impact associated with headache

was assessed using the Headache Impact Test-6 (HIT-6). The experimental protocol

consisted of baseline measurements, a provocation chewing test, and data collection

immediately after, and 24 hours after, the provocation chewing test. Participants

underwent standardized measurement of pressure pain thresholds (PPT) for mechanical

pain sensitivity at the trigeminal and cervical region and the pain-free maximum mouth

opening (MMO). The PPT and MMO measures have been employed in previous

9

studies[46] and are further described below. During the performance of the provocation

chewing test, data were collected regarding the subjective feelings of fatigue and pain

intensity every minute, immediately and 24 hours after completion.

Provocation Chewing Test

The provocation chewing test consisted of 6 minutes of unilateral chewing of eight

grams of hard gum; this protocol was modified from Karibe et al.[47]. Chewing gum

was employed to elicit pain and muscle fatigue. The participants performed the test in

the sitting position, which was attained by instructing the patient to sit in a comfortable

upright position, with the thoracic spine in contact with the back of the chair, but

without contact of the craniocervical region with the seat. The feet were positioned flat

on the floor with knees and hips at 90 degrees and arms resting freely alongside.

Tests were carried out by exclusively using the right side for chewing; the

metronome was set at 80 beats per minute to indicate chewing rate, as documented in a

previous study[48]. The participants were instructed to chew gum initially for 60

seconds to soften its initial hardness, then after 70 seconds of rest, the signal was given

to start the test.

Questionnaires

The Spanish version of the PCS assesses the degree of pain catastrophizing[49, 50]. The

PCS has 13 items and a 3-factor structure: rumination, magnification and helplessness.

The theoretical range is between 0 and 52, with lower scores indicating less

catastrophizing. The PCS has demonstrated acceptable psychometric properties[50].

The Spanish version of the NDI measures perceived neck disability[45, 51]: This

questionnaire consists of 10 items, with 6 possible answers that represents 6 levels of

functional capacity, ranging from 0 (no disability) to 5 (complete disability) points. The

addition of all of the points obtained from each of the items gave the level of disability,

10

with higher scores indicating greater perceived disability. The NDI has demonstrated

acceptable psychometric properties[51].

The Spanish version of the HIT-6[52, 53] consists of a six-item questionnaire measuring

the severity and impact of headache on the patient’s life. The results of HIT-6 are

stratified into four grade-based classes: little or no impact (HIT-6 score: 36-49),

moderate impact (HIT-6 score: 50-55), substantial impact (HIT-6 score: 56-59), and

severe impact (HIT-6 score: 60-78)[52]. The HIT-6 has demonstrated acceptable

psychometric properties[54].

Pain intensity

Pain intensity was measured with the VAS. The VAS consists of a 100 mm line, on

which the left side represents “no pain” and the right side “the worst pain imaginable”.

The patients placed a mark where they felt it represented their pain intensity[55].

The VAS scale was used to quantify two different situations:

a) Habitual and spontaneously perceived pain intensity.

b) Pain intensity perceived at different times during the course of the chewing

provocation test and at 24h after completion.

Subjective perception of fatigue.

The visual analogue fatigue scale (VAFS) was used to quantify fatigue at

different times during the course of the chewing provocation test and at 24h after

completion. The VAFS consists of a 100-mm vertical line on which the bottom

represents “no fatigue” (0 mm), and the top represents “maximum fatigue” (100

mm)[56]. The researcher registered the mark in mm.

Pressure pain thresholds

11

A digital algometer (FDX 25, Wagner Instruments, Greenwich, CT, USA),

comprised of a rubber head (1 cm2) attached to a pressure gauge, was used to measure

PPTs. Force was measured in kilograms (kg); therefore, thresholds were expressed in

kg/cm2. The protocol used was a sequence of 3 measurements, with an interval of 30

seconds between each of the measurements. An average of the 3 measurements was

calculated to obtain a single value for each of the measured points in each of the

assessments. PPTs were assessed at one point in the masseter muscle (2.5 cm anterior to

the tragus and 1.5 cm inferior to the zygomatic arch), one point in the temporalis muscle

(anterior fibres of the muscle; 3 cm superior to the zygomatic arch in the middle point

between the end of the eye and the anterior part of the helix of the ear), in the

suboccipital muscles (2 cm inferior and lateral to the external occipital protuberance)

and in the upper trapezius muscle (2.5 cm above the superior medial angle of the

scapula). The device was applied perpendicular to the skin. The patients were asked to

raise their hands at the moment the pressure started to change to a pain sensation, at

which point the assessor stopped applying pressure. Compression pressure was

gradually increased at a rate of approximately 1 kg/s. This algometric method has high

intra-rater reliability (ICC=0.94-0.97) for measuring PPT[57].

Pain-free MMO

MMO was measured with the patients in a supine position. The patients were

asked to open their mouths as wide as they could without pain. The distance between

the superior incisor and the opposite inferior incisor was measured in mm with a

Craniomandibular scale (CMD scale. Pat. No. ES 1075174 U, INDCRAN: 2011.

INDCRAN, Madrid, Spain). The inter-rater reliability of this procedure has been found

to be high (ICC = 0.95 – 0.96)[58].

12

Sample size

The sample size was estimated with the G*Power Program 3.1.7 for Windows

(G*Power© from University of Dusseldorf, Germany)[59]. The sample size calculation

was considered a power calculation to detect between-group differences in the primary

outcome measures (fatigue and pain intensity). To obtain 80% statistical power (1-β

error probability) with an α error level probability of 0.05, using analysis of variance

(ANOVA) of repeated measures, within-between interaction and an medium effect size

of 0.3, we considered 3 groups and 7 measurements for primary outcomes. This

generated a sample size of 31 participants per group. Allowing a dropout rate of 20%

and aiming to increase the statistical power of the results, we planned to recruit at least a

minimum of 112 participants to provide sufficient power to detect significant group

differences.

Statistical Analysis

The Statistical Package for Social Sciences (SPSS 21, SPSS Inc., Chicago, IL

USA) software was used for statistical analysis. The independent t-test and one-way

ANOVA was used for analysis of the self-report psychological and pain-related

variables (NDI, PCS and HIT-6), as well as pain duration and the subjects’

sociodemographic data (age, weight, height), comparing the baseline data for the three

groups. Results are presented as mean, standard deviation (±SD), range and 95%

confidence interval (CI).

For primary outcome variables (fatigue and pain intensity), we performed a 3-

way repeated-measures ANOVA, including within-between interaction factors. The

factors analysed were group (i.e., moderate neck disability group, mild neck disability

group and healthy group), sex (i.e., female and male) and time (measurement per minute

13

during the test and after 24 hours). The hypothesis of interest was the group vs. time

interaction.

The 2-way repeated-measures models of ANOVA were used to test the effect of

the task on the outcome secondary variables (i.e., PPTs and pain-free MMO). The

factors analysed were group and time (baseline, immediately after and after 24 hours),

and also the interactions group vs. time interactions were analysed. In the analysis,

repeated-measures ANOVAs, when the assumption of sphericity was violated (as

assessed using the Mauchly sphericity test), the number of degrees of freedom against

which the F-ratio was tested was corrected by the value of the Greenhouse–Geisser

adjustment. Post hoc analysis with Bonferroni corrections was performed in the case of

significant ANOVA findings for multiple comparisons between variables. Effect-sizes

(Cohen’s d) were calculated for outcome secondary variables. According to Cohen’s

method, the magnitude of the effect was classified as small (0.20 to 0.49), medium (0.50

to 0.79), and large (≥0.8)[60].

The relationship between pain-related measures after completion of the chewing

provocation test and self-reports for pain-related and psychological measures were

examined using Pearson correlation coefficients. Multiple linear regression analysis was

performed to estimate the strength of the associations between the results of VAS

[model 1], VAFS [model 2] and pain-free MMO [model 3] (criterion variables) after 24

hours following completion of the provocation chewing test and NDI, PCS, HIT-6 and

VAS were used as predictor variables. Variance inflation factors (VIFs) were calculated

to determine whether there were any multi-collinearity issues in any of the three models.

The strength of association was examined using regression coefficients (β), P

values and adjusted R2. Standardized beta coefficients were reported for each predictor

14

variable included in the final reduced models to allow for direct comparison between

the predictor variables in the regression model and the criterion variable being studied.

For regression analysis, the 10 cases per variable rule was applied in order to obtain

reasonably stable estimates of the regression coefficients[61]. The significance level for

all tests was set to P < 0.05.

RESULTS

Baseline characteristics of sociodemographic, psychological and pain-related variables

of the sample are summarized in Table 1. Finally, the total study sample consisted of

122 participants (77 females and 45 males). Table 1 shows no statistically significant

differences among the three groups in relation to sociodemographic variables. There

were no differences in the duration of pain and perceived pain intensity on a regular or

spontaneous basis in specific groups of patients, but differences were observed in NDI,

PCS and Hit-6 (p<0.05). The different diagnosis for TMD of the included patients were

as follows: 28 patients (33.7%) were diagnosed with myofascial pain, 8 patients (9.6%)

with arthralgia, 13 patients (15.6%) with osteoarthritis and 34 patients (40.9%) with a

combined diagnosis (myofascial pain with arthralgia or osteoarthritis).

In the group of healthy participants, there were no withdrawals during the

provocation chewing test; in the group of patients with moderate neck disability, nine

participants (21.9%) withdrew between minutes 5 and 6 of the test as well as six

participants in the group of patients with mild neck disability (14.2%). All of the

participants were evaluated 24 hours after the test.

Gender Differences in Response to Provocation Chewing Test

The interaction of group vs. sex showed significant differences in VAS

(F=10.86; P<0.001), VAFS (F=4.06; P=0.02) and PPTs of the trapezius muscle

15

(F=3.96; P=0.022). Post hoc analysis showed higher values of VAS and VAFS in

women compared to men for the three groups (P<0.05). PPTs in the trapezius muscle

values were lower in women than in men (P<0.05) for the two groups of patients; in the

control group there was no difference in this value. No differences (group vs. sex

interaction) were observed for the other variables.

Pain and Fatigue

The ANOVA revealed a significant group vs. time interaction (F=35.77;

P<0.001), and significant differences for the group factor (F=416.65; P<0.001)

regarding the VAS results during the provocation chewing test. VAS behaviour during

the tests can be seen in Figure 1-A. Post hoc analysis revealed that higher values on the

VAS during provocation chewing test for the moderate neck disability group compared

to the mild neck disability group and the control group. The results obtained 24 hours

after the test showed no differences between the groups of patients, but there were

differences with the control group (Figure 2-A).

For fatigue perceived during tests, the ANOVA showed a significant effect for

group vs. time interaction (F=13.05; P<0.001) and for the group factor (F=371.12;

P<0.001). VAFS behaviour during the tests can be seen in Figure 1-B. VAFS values

were higher at 6 minutes and 24 hours after the test in the group of moderate neck

disability compared with the other two groups. The post hoc analysis shows the

differences between the three groups (Figure 2-B).

Pain-free MMO

Regarding the pain-free MMO ANOVA revealed a significant effect for group

vs. time interaction (F=2.75; P=0.02) and for the group factor (F=65.74; P<0.001). The

post hoc analysis shows a decrease in the pain-free MMO immediately after the tests for

16

the three groups, but this decrease was observed only in the group of moderate disability

at 24 hours after the test (Table 2).

Pressure pain thresholds

The PPTs for all points of the trigeminal and cervical region showed statistically

significant differences by ANOVA in the group vs. time interaction and group factor

(P<0.001). According to the post hoc analysis of the PPT masseter muscle, the results

showed a decrease in all groups for measurements both immediately and 24 hours after

the test (P<0.05); however, this decrease was greater in the group showing moderate

neck disability (d>0.8). Changes in temporalis muscle PPT’s were observed in both

measures for the group of moderate neck disability (P<0.001; d>0.8). In the group of

mild neck disability, changes were only observed immediately after the test (P=0.002;

d=0.19). No changes were observed in the group of healthy subjects (P>0.05).

For PPT in the cervical region (trapezius muscle and suboccipital muscles), the

post hoc analysis shows a decrease of values measures immediately and 24 hours after

the test (P<0.001) for group of moderate neck disability. This decrease in PPT can be

considered large for the suboccipital region (d>0.9) and small-medium for the trapezius

muscle (d=0.27 and 0.61). In the group with mild neck disability, changes were

observed only in the trapezius muscle PPT measurement immediately after the test

(P=0.028; d=0.09) and no statistically significant differences were observed in any of

the PPT measurements in the cervical region in the group of healthy subjects (P>0.05).

Correlations Analysis

Table 3 shows the results of correlation analysis examining the bivariate

relationships among self-reports for pain-related and psychological measures and

MMO, VAS and VAFS measured immediately and 24 hours after the tests for the

17

groups with moderate and mild neck disability. The strongest correlations were found in

the analysis for the group with moderate neck disability, where the pain-free MMO

immediately after the test was negatively associated with NDI (r=-0.54; P<0.001). For

the mild neck disability group, the greater correlation was between the MMO results

after 24 hours and NDI, which had a negative association (r=-0.49; P<0.001).

Multiple linear regression analysis

A linear regression analysis was performed to evaluate contributors to VAFS,

VAS and pain-free MMO after 24 hours regarding all of the self-report results for pain-

related and psychological measures in the patient groups with moderate and mild neck

disability; the results are presented in Table 4.

In the first model, the criterion variable VAFS was predicted by pain

catastrophizing (for both groups), explaining 17% and 12% of variance, respectively.

The following variables, VAS (moderate neck disability, β=-0.001; P=0.10, mild neck

disability, β=-0.053; P=0.72), HIT-6 (moderate neck disability, β=0.004; P=-0.97, mild

neck disability, β=-0.071; P=0.63), and NDI (moderate neck disability, β=-0.082;

P=0.59, mild neck disability, β=-0.070; P=0.67) were not significant predictors.

In the second model, the VAS after 24 hours was predicted by HIT-6 (moderate

neck disability group) and pain catastrophizing (mild neck disability group), explaining

22% and 14% of the variance, respectively. The VAS (moderate neck disability, β=-

0.27; P=0.06, mild neck disability, β=-0.13; P=0.41), NDI (moderate neck disability,

β=0.19; P=0.17, mild neck disability, β=0.24; P=0.13) and PCS (moderate neck

disability, β=0.16; P=0.25) and HIT-6 (mild neck disability, β=-0.054; P=0.71) were not

significant predictors.

18

In a third model, the pain-free MMO was predicted by NDI for both groups;

these models accounted for between 14% and 21% of the variance. The PCS (moderate

neck disability, β=0.20; P=0.19, mild neck disability, β=0.13; P=0.39), the VAS

(moderate neck disability, β=-0.34; P=0.85, mild neck disability, β=-0.26; P=0.13) and

HIT6 (moderate neck disability, β=-0.24; P=-0.066, mild neck disability, β=0.20;

P=0.64) were not significant predictors.

DISCUSION

The results of this study demonstrate that a protocol of masticatory provocation

can induce pain, fatigue and other trigeminal sensory-motor changes in patients with

headache attributed to temporomandibular disorders. Our findings are consistent with

previous studies which have also observed sensory changes induced experimentally by

the masticatory provocation test[47, 62–64]. The duration of the masticatory

provocation test used in our study was similar to other investigations[47, 63, 65].

However, some studies have used longer and also shorter durations for the masticatory

test, reporting significant changes in both situations for both patients and healthy

subjects[48, 62, 64, 66–68]. It is important to mention that group changes were found in

the healthy subjects, but these were smaller than in the other groups, this could be

explained by the observation that exercise can induce pain and increased

hyperalgesia[69]. In addition, other authors have suggested that experimentally-induced

pain during the test may be due to masticatory muscle ischemia followed by the

accumulation of metabolic products in these muscles[70–72]. We also need to take into

account that there is sufficient evidence to suggest fatigue as a factor that increases the

pain perception[73].

19

In this regard, our findings show strong positive correlations between fatigue

and perceived pain associated with the masticatory provocation test in the three assessed

groups. These results may explain in a general way the observed sensory-motor

changes, although they are not sufficient to justify neither the between-groups

differences nor the influence of cervical disability. Reflections and discussion of these

issues are presented in the following section in an effort to clarify and achieve a better

understanding of the matter.

One of the hypotheses proposed in this study is that cervical disability has an

influence over the trigeminal sensory-motor variables, modifying them. The results

obtained support this hypothesis because we observed greater changes in the moderate

cervical disability group immediately and 24 hours after the test. In addition, it was

hypothesized that the psychosocial factors would have a relationship with the results of

the masticatory provocation test and specifically with the pain and fatigue variables.

This relationship was proved after observing an association with pain catastrophizing.

Gender Differences

Regarding pain perception and fatigue during the test, our data show that gender

influences the results of the three groups: women presented with the greater perception

of pain intensity and masticatory fatigue. These results are consistent with previous

studies of experimentally-induced pain in patients[63] and healthy subjects[47, 68];

however, other investigations have not observed the interaction of gender factors with

experimentally-induced pain or masticatory fatigue [65, 74]. This research has not been

designed to identify the physiologic or psychological mechanisms which may explain

the differences in the results of men and women, although it is important to state that

there are many studies which present evidence-based results regarding the response that

20

women have to other painful clinical situations, adding the evidence of experimentally-

induced pain studies which indicate that women have a greater pain sensitivity than men

regarding several somatosensory tests[75].

Influence of the cervical disability over the trigeminal sensory-motor activity.

In this study, we have identified that patients with mild to moderate cervical

disability present a greater perception levels of pain and fatigue compared with healthy

subjects. It is important to mention that the group with moderate cervical disability

presented the greatest changes at the sensorial variables measured along the test,

immediately after and 24 hours after the test, with the exception of the pain intensity

perception after 24 hours, in which no statistically significant differences were found

between groups.

Although there are many studies that have used a provocative test to induce

masticatory pain and fatigue, we have only found one study similar to ours, in which

Haggman-Henrikson et al.[63] observed that patients with whiplash-associated

disorders presented greater masticatory pain and fatigue induced by the test compared to

TMD patients and healthy subjects.

We note recent scientific evidence that injuries to the cervical region may alter

the masticatory motor control and normal mandibular open-close function[76–78]. The

findings of this study may be related to this issue, because our results show that the

masticatory provocation test reduces the pain-free MMO at the end of the test, as seen in

the three groups assessed; these results are similar to previous studies[47, 72]. However,

we need to point out that the reduction was greater in both patient’s groups and it was

maintained at 24 hours only in the moderate cervical disability group. Also, it is

21

important to highlight that the regression analysis showed that cervical disability is a

predictor of the pain-free MMO (after 24 hours) in both groups of patients.

At present, the scientific evidence suggests the existence of cervical and

trigeminal motor patterns that act in a coordinated manner in the performance of

masticatory activities (chewing)[79–82], plus recent studies also support that the neck

muscles are activated during jaw-clenching tasks tasks assessed electromyographically

[83–85] and it seems that the activity of the neck muscles is increased as the demand for

masticatory work is greater[86]. Although most of these studies have been performed in

healthy subjects, we believe that these data are useful to try to explain some of the

results of this research. In this sense, we propose the theory that the masticatory motor

patterns are more altered with the presence of greater cervical pain or disability. This

situation would generate the activation of maladaptive compensatory mechanisms that

might alter the behaviour, recruitment and coordination of the neck and mandibular

motor systems, thus generating higher levels of fatigue and pain during the provocation

test and retaining these feelings 24 hours later.

This same theory could explain the results of decreased PPTs at the trigeminal and

cervical regions, noting that the PPTs changes were higher in the patient groups and that

most changes in the cervical PPTs at 24 hours occurred in the group of moderate

cervical disability. As a contributing factor to this situation, the presence of neck pain

must be considered, as this can lead to lower values of trigeminal PPTs compared to

healthy subjects [87]. Although we believe that there may be a direct relationship

between the trigeminal sensory-motor changes with cervical pain and disability, we

must also consider the possibility that the changes seen in patients would have been

mainly influenced by pre-established neuroplastic changes in the central nervous

system. Patients with chronic pain may be more susceptible to develop a central

22

sensitization process[88]. Wolf et al. suggest that in painful conditions where there is a

comorbidity, such as in the sample of patients in this study, it can be a determining

factor in the pathophysiology of central sensitization[89]. In relation to this, Gaff-

Radford proposed that in central sensitization, changes appear in afferent pathways that

enable the communication of cervical and orofacial nociceptive neurons in the

trigeminal nucleus[90]. In addition, there are many studies in TMD patients that have

found peripheral and central mechanisms compatible with a process of central

sensitization[91–97].

Influence of pain catastrophizing over trigeminal sensory-motor activity.

In this research, we have used self-reports of psychological and pain-related

variables to identify possible associations with sensory-motor variables. Through linear

regression analysis, we have observed that pain catastrophizing and the impact of

headache on the quality of life (HIT-6) were associated with the pain perception and

fatigue variables 24 hours after performing the masticatory provocation test.

Specifically, analysing the pain catastrophizing as a psychological factor resulted in a

predictor for fatigue at 24 hours after the test in the moderate cervical disability group,

and in the mild cervical disability group it was a predictor for perceived cervical

disability and fatigue after 24 hours. Pain catastrophizing is defined as a cognitive factor

that implies a mental negative perception or exaggeration of the perceived threat of

either a real or anticipated pain experience[98, 99]. It has been described that in patients

with TMD, catastrophizing contributes to the chronification of pain and disability [100].

It has also been associated with a greater use of health system services, with greater

clinical findings at assessment associated with a negative mood[40, 41] and with

alterations of the functional mandibular status[10]. Regarding the perceived fatigue and

pain catastrophizing, we did not find any clinical or experimental trials that have

23

examined their association in patients with craniofacial pain and TMD; but we found

one study researching the relationship of pain catastrophizing with masticatory

kinematic variables (i.e., amplitude, velocity, frequency cycle) which were measured

with a procedure using very short exposure times (15 seconds of chewing)[32]. In this

study, no associations of the kinematic variables measured with respect to catastrophism

were observed; however, we must take into account that the purpose of that study was

not to induce pain or fatigue to observe the response, as we did in this research. It is

important to note that a recent systematic review concluded that there is an association

between catastrophizing and fatigue and that the former influences the latter

proportionately; these results were observed in various clinical populations[101]. This

has also been demonstrated in other musculoskeletal disorders where pain

catastrophizing is associated with motor disturbances, such as decreased function,

performance of activities of daily living and limitation of exercise capacity[102–104].

The relationship between psychological factors, motor activity and pain seems to

be present in various cases of musculoskeletal pain, but the explanation for this is

complex and limited so far. Peck et al.[105] and Murray and Peck[106] have proposed a

possible explanation for this and have created a new Integrated Pain Adaptation Model

(IPAM). This model basically explains that the influence of pain on motor activity

depends on the interaction of multidimensional characteristics (biological and

psychosocial) of pain with the sensory-motor system of an individual, which results in a

new motor recruitment strategy in order to minimize pain. However, this motor

response may be associated with the appearance of another pain or worsening of the

existing pain[105, 106]. This model is based on the multidimensional features (sensory

discriminative, affective-emotional, cognitive) of the pain experience and how it affects

the sensory-motor system through the peripheral and central connections that this

24

system has with the autonomous nervous system, the limbic system and other higher

centres[105, 107].

Clinical and scientific implications

According to the results of this research, we found that neck pain and disability

can influence sensory and motor variables of the masticatory system. These findings

lead us to reflect on the importance of including a clinically specific assessment of the

cervical region in the diagnostic protocols for TMD and headache attributed to TMD. It

is noteworthy that the most commonly used diagnostic and classification methods for

patients with TMD do not include a specific assessment of neck pain and disability[20,

44, 108]. A diagnostic criterion observed recently in patients with headache attributed to

TMD is that mandibular movement, function or parafunction modify headache in the

temporal region[21]. We have observed an association between cervical disability with

pain-free MMO and have also found that patients with greater neck disability have

increased fatigue and pain induced by the masticatory test. These findings lead us to

assume that the cervical region may have an important role for this type of headache,

but this has to be confirmed in future research, as these data can be extrapolated only to

patients with this type of headache who also associate neck disability.

From the point of view of treatment, we propose an approach to reduce cervical

pain and disability as part of the overall therapeutic strategy, as this could be beneficial

to reduce the negative sensory symptoms and improve masticatory motor control. We

believe that this approach should be investigated in future studies, but it must be taken

into account that we have recent evidence that therapeutic exercise and manual therapy

to the cervical region produce positive effects on pain modulation in trigeminal areas

and improving pain-free MMO[46, 109].

25

In this study and other longitudinal or transversal studies, we have shown the

influence of psychosocial factors on patients with TMD[36, 110, 111]; specifically, our

results show an association between catastrophizing and perceived fatigue induced by

the masticatory activity. This finding shows the interaction between sensory-type

variables with psychological variables, which should be considered a crucial issue when

performing the assessment or designing of therapeutic interventions. In patients with

chronic pain, it is essential to recognize psychosocial factors that may be perceived as

obstacles to recovery[112]; achieving a reduction of pain catastrophizing is the best

predictor of successful rehabilitation in pain conditions[113].

The integration of a biopsychosocial perspective in clinical reasoning and

decision-making could be a key point in the management of pain and motor

rehabilitation of patients with headache attributed to TMD. It has been shown that

cognitive-behavioural therapy reduces pain intensity, depressive symptoms, improves

chewing function[114], reduces pain catastrophizing in patients with chronic TMD[115]

and, furthermore, it has been found that it causes neuroplastic adaptive changes

associated with decreased pain catastrophism in cases of chronic pain[116]. Prescribing

therapeutic exercise may be a good alternative to take into consideration; it has been

observed that exercise causes a reduction of catastrophizing and depressive symptoms;

these results were similar to cognitive behavioural therapy in patients with chronic

lower back pain[117].

Limitations

The results of this study should be discussed with the consideration that there are

several limitations. Although the sample size was calculated to have adequate power

and further losses were less than 20%, the results were not compared with a group with

26

headache attributed to TMD but without the presence of neck pain and disability. To

extrapolate the results to a clinical population would require similar but future studies to

be implemented using patient sample protocols with and without neck pain and

disability. Another limitation to consider is that pain catastrophizing was assessed as the

only psychological variable. It would be interesting to investigate the association of

other variables such as anxiety, depression, kinesiophobia and self-efficacy with

trigeminal sensory-motor variables.

As the only motor variable measured in this research was pain-free MMO, other

kinematic variables should be taken into consideration in future research as they may

provide more information. Moreover, we believe that measuring motor variables of the

cervical region could also be useful to analyse possible correlations with masticatory

variables.

CONCLUSION

The results of this study suggest that neck pain and disability have an influence

on the sensory-motor variables evaluated in patients with headache attributed to TMD.

In particular, it was observed that patients with moderate neck disability showed greater

changes immediately and 24 hours after the masticatory provocation test. Our data

provide new evidence about the possible neurophysiologic mechanisms of interaction

between the craniocervical region and the craniomandibular region. Regarding pain

catastrophizing, an association with perceived masticatory fatigue in both patient groups

was observed. These findings support the need to recognize the interaction between

sensory-motor and psychological aspects of headache attributed to TMD rather than

being assessed in isolation.

27

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

RL, AP, AG, JF participated in the study design, manuscript preparation and editing and

data acquisition. JP, SA, RL participated in the performed the statistical analysis,

database management and manuscript preparation. All authors read and approved the

final manuscript.

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Figure 1. Data represent mean value and error bars with 95% confidence intervals of

the mean of the pain intensity score (A), and the visual analogue fatigue scale scores

(B). Recorded during the 6 min and 24 hours after provocation chewing test. Level of

significance (multiple comparisons for each group): Moderate disability, *P<0.05;

**P<0.01; Mild disability, °P<0.05; °°P<0.01; and Healthy, ^P<0.05; ^^P<0.01.

Figure 2. Comparison between groups of the pain intensity (A) and perceived fatigue

(B) immediately (6 min) and 24 hours after the provocation chewing test. Data represent

mean value, error bars with 95% confidence intervals of the mean and effect size (d).

Level of significance: *P<0.05; **P<0.01.

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Table 1. Summary of Demographic, Pain and Psychological Variables

Moderate Neck Disability (N=41)

Mild Neck Disability (N=42)

Healthy (N=39)

t / F P Value

Variables Mean±SD Range Mean±SD Range Mean±SD Range Sex (female/male) 26/15 - 25/17 - 26/13 - - -

Weight (kg)

69.56±12.47 51-103 67.76±14.03 50-97 64.84±10.2 48-90 1.4 0.23

Heigth (cm)

167.56±12.4

7

152-183 165.54±12.09 150-185 169.97±8.51 156-189 1.98 0.14

Age (years)

44.31±10.9 22-59 40.95±12.89 19-60 40.61±10.01 30-65 1.3 0.27

Pain duration

(months)

19.73±12.66 6-60 22.19±13.36 6-48 - - -0.8 0.39

NDI (points) 17.58±2.69 15-24 11.42±2.48 7-14 - - 10.8 0.01

PCS (points) 17.09±3.75 7-23 15.8±4.02 7-22 5.46±1.75 2-9 143 0.01

HIT-6 (points) 55.31±4.9 49-65 53.16±4.74 43-59 - - 2 0.04

VAS (mm) 40.75±9.17 21-58 37.04±9.16 19-54 - - 1.8 0.06

Abbreviations: NDI, Neck Disability Index; PCS, Pain Catastrophizing Scale; HIT-6, headache impact test-6; Visual Analog Scale, VAS; SD, standard deviation

39

Table 2. Descriptive data and multiple comparisons of the assessed variables

** p < 0.01; *p < 0.05 Abbreviations: MMO, maximal mouth opening; PPT, pressure pain threshold; SD, standard deviation

Mean±SD Mean difference (95% CI) Effect size (d)

Group Baseline Immediately after

After 24 hours a) Base vs. Immediately b) Base vs. 24 h.

MMO (mm)

Moderate Neck Disability

42.43±2.75 40.65±2.01 41.85±2.19 a) 1.89 (1.39 to 2.39)**;d=0.74 b) 0.6 (0.02 to 1.17)*;d=0.26

Mild Neck Disability

43.61±2.87 42±2.18 43.26±2.68 a) 1.56 (1.09 to 2.07)**; d=0.63 b) 0.36 (-0.01 to 0.75); d=0.12

Healthy 50±4.46 49.05±3.95 49.87±4.57

a) 0.76 (0.24 to 1.29)*; d=0.22 b) 0.09 (-0.32 to 0.51); d=0.02

PPT. Masseter Moderate Neck Disability

1.9±0.21 1.02±0.17 0.88±0.2 a) 0.89 (0.79 to 0.99)** d=4.66 b) 1.03 (0.94 to 1.13)** d=5.03

Mild Neck Disability

2.01±0.34 1.44±0.28 1.57±0.34 a) 0.57 (0.48 to 0.67)** d=1.82 b) 0.44 (0.35 to 0.53)** d=1.29

Healthy 2.85±0.58 2.39±0.52 2.7±0.51

a) 0.45 (0.35 to 0.56)** d=0.84 b) 0.13 (0.03 to 0.23)* d=0.27

PPT. Temporalis Moderate Neck Disability

1.99±0.19 1.55±0.25 1.62±0.23 a) 0.44 (0.39 to 0.49)** d=2.06 b) 0.37 (0.25 to 0.49)** d=1.77

Mild Neck Disability

2.12±0.35 2.05±0.37 2.04±0.45 a) 0.07 (0.02 to 0.12)** d=0.19 b) 0.09 (-0.02 to 0.2) d=0.20

Healthy 3.31±0.83 3.26±0.82 3.27±0.84

a) 0.04 (-0.001to 0.1) d=0.06 b) 0.06 (-0.05 to 0.19) d=0.04

PPT. Suboccipital

Moderate Neck Disability

2.39±0.44 1.65±0.36 1.47±0.32 a) 0.78 (0.7 to 0.85)** d=1.86 b) 0.95 (0.83 to 1.07)** d=2.42

Mild Neck Disability

2.14±0.57 2.06±0.55 2.22±0.57 a) 0.07 (-0.00 to 0.15) d=0.14 b) -0.11 (-0.23 to 0.00)* d=0.14

Healthy 3.15±0.56

3.09±0.55 3.18 ±0.59

a) 0.06 (-0.01 to 0.14) d=0.1 b) -0.01 (-0.13 to 0.11) d=0.05

PPT. Trapezius Moderate Neck Disability

2.62±0.49 2.33±0.47 2.49±0.45 a) 0.28 (0.24 to 0.33)** d=0.61 b) 0.14 (0.08 to 0.2)** d=0.27

Mild Neck Disability

2.68±0.62 2.62±0.63 2.63±0.58 a) 0.04 (0.00 to 0.09)* d=0.09 b) 0.04 (-0.01 to 0.1) d=0.08

Healthy 3.54±1 3.51±0.97 3.53±0.94 a)0.01 (-0.03 to 0.06) d=0.03 b) -0.01 (-0.05 to 0.07) d=0.01

40

Table 3. Pearson's correlation coefficient between the different variables analyzed in the study

Groups VAS 6min. VAS 24h. VAFS 6min.

VAFS 24h. MMO Immediately After

MMO 24h

Moderate Neck Disability

NDI 0.49** 0.28 0.40** 0.07 -0.54** -0.40**

Mild Neck Disability

0.02 0.37* 0.02 0.21 -0.48** -0.49**

Moderate Neck Disability

PCS 0.10 0.24 0.17 0.44** 0.03 0.04

Mild Neck Disability

0.08 0.40** 0.01 0.38* -0.17 -0.09

Moderate Neck Disability

HIT-6 0.41** 0.48** 0.27 0.07 -0.12 -0.31*

Mild Neck Disability

-0.11 -0.03 0.30 -0.04 -0.13 -0.12

Moderate Neck Disability

VAS -0.08 0.39* 0.49** 0.16 -0.23 -0.25

Mild Neck Disability

-0.08 0.17 -0.17 0.11 -0.39* -0.47**

** p < 0.01; *p < 0.05 Abbreviations: NDI, Neck Disability Index; PCS, pain catastrophizing scale; HIT-6, headache impact test-6; VAS, visual analog scale; VAFS, visual analog fatigue scale; MMO, maximal mouth opening

41

Table 4. Multiple linear regression analysis

Moderate Neck Disability

criterion variable

predictor variables

Regression coefficient (B)

Standardized coefficient (β)

Significance (p)

VIF Adjusted R2

VAFS24 PCS 0.84 0.44 0.004 1.00 0.17

VAS24 HIT-6 0.93 0.48 0.001 1.00 0.22

MMO24 NDI -0.35 -0.40 0.01 1.12 0.14

Mild Neck Disability

VAFS24 PCS 0.98 0.38 0.013 1.00 0.12

VAS24 PCS 0.67 0.40 0.009 1.00 0.14

MMO24 NDI -0.53 -0.49 0.001 1.00 0.21

Abbreviations: NDI, Neck Disability Index; PCS, pain catastrophizing scale; HIT-6, headache impact test-6; VAS, visual analog scale; VAFS, visual analog fatigue scale; MMO, maximal mouth opening; 24, 24 hours after of tests

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182

5.6 Estudio VI

La Touche R, Fernández-de-las-Peñas C, Fernández-Carnero J, Escalante K, Angulo-Díaz-

Parreño S, Paris-Alemany A, Cleland JA. The effects of manual therapy and exercise directed at

the cervical spine on pain and pressure pain sensitivity in patients with myofascial

temporomandibular disorders. J Oral Rehabil. 2009 Sep;36(9):644-52.

Objetivos del estudio

Nuestro objetivo fue investigar los efectos de la terapia manual y el ejercicio dirigido a la

columna cervical en la intensidad del dolor, la MAI y los UDPs de músculos masticatorios en

pacientes con TCM.

Resultados

El modelo mixto de ANOVA 2X3 reveló un efecto significativo en el factor tiempo (F = 77,8; P

<0,001), pero no para el factor lado (F = 0,2; P = 0,7) para los cambios en los UDPs sobre el

músculo masetero y más músculo temporal (tiempo: F = 66,8; P <0,001; lado: F = 0,07; P =

0,8). Las pruebas post hoc revelaron diferencias significativas entre pre-intervención y la post-

intervención y período de seguimiento (P <0,001), pero no entre la post-intervención y el

periodo seguimiento (P = 0,9) para ambos músculos. Los tamaños del efecto eran grandes (d>

1,0) para ambos períodos de seguimiento en los UDPS musculares. El ANOVA encontró un

efecto significativo de tiempo (F = 78,6; P <0,001) los cambios en la intensidad del dolor y la

MAI sin dolor (F = 17,1; P <0,001). Se encontraron diferencias significativas entre la pre-

intervención y dos periodos post-intervención (P <0.001), pero no entre la medida post-

intervención y el periodo de seguimiento (P> 0.7). Dentro del grupo tamaños del efecto eran

grandes (d> 0,8) para los resultados post-intervención y los períodos de seguimiento.

Conclusión

La aplicación de tratamiento dirigido a la columna vertebral cervical puede ser beneficioso en la

disminución de la intensidad del dolor, el aumento de los UDPS en los músculos de la

masticación y en la MAI libre de dolor en pacientes con TCM.

The effects of manual therapy and exercise directed at the

cervical spine on pain and pressure pain sensitivity in

patients with myofascial temporomandibular disorders

R. LA TOUCHE*, †, C. FERNANDEZ-DE-LAS-PENAS‡, §, J . FERNANDEZ-CARNERO‡, §,

K. ESCALANTE¶, S. ANGULO-DIAZ-PARRENO†, A. PARIS-ALEMANY† &

J. A. CLELAND** , ††, ‡‡*Faculty of Medicine, Department of Physical Therapy, Universidad San Pablo CEU, Madrid, †University

Center for Clinical Research of the Craneal-Cervical-Mandibular System of Universidad San Pablo CEU, Madrid, ‡Department of Physical

Therapy, Occupational Therapy, Rehabilitation and Physical Medicine, Universidad Rey Juan Carlos, Alcorcon, Madrid, §Esthesiology

Laboratory of Universidad Rey Juan Carlos, Alcorcon, Madrid, ¶Faculty of Psychology, Department of Personality Assessment and Psychology

Treatment, Universidad Complutense, Madrid, Spain, **Department of Physical Therapy, Franklin Pierce University, Concord, ††Physical

Therapist, Rehabilitation Services, Concord Hospital, Concord, NH and ‡‡Faculty, Manual Therapy Fellowship Program, Regis University,

Denver, CO, USA

SUMMARY No studies have investigated the effects of

the treatments directed at the cervical spine in

patients with temporomandibular disorders (TMD).

Our aim was to investigate the effects of joint

mobilization and exercise directed at the cervical

spine on pain intensity and pressure pain sensitivity

in the muscles of mastication in patients with TMD.

Nineteen patients (14 females), aged 19–57 years,

with myofascial TMD were included. All patients

received a total of 10 treatment session over a 5-

week period (twice per week). Treatment included

manual therapy techniques and exercise directed at

the cervical spine. Outcome measures included

bilateral pressure pain threshold (PPT) levels over

the masseter and temporalis muscles, active pain-

free mouth opening (mm) and pain (Visual Ana-

logue Scale) and were all assessed pre-intervention,

48 h after the last treatment (post-intervention) and

at 12-week follow-up period. Mixed-model ANOVAS

were used to examine the effects of the intervention

on each outcome measure. Within-group effect sizes

were calculated in order to assess clinical effect. The

2 · 3 mixed model ANOVA revealed significant effect

for time (F = 77Æ8; P < 0Æ001) but not for side (F = 0Æ2;

P = 0Æ7) for changes in PPT over the masseter muscle

and over the temporalis muscle (time: F = 66Æ8;

P < 0Æ001; side: F = 0Æ07; P = 0Æ8). Post hoc revealed

significant differences between pre-intervention

and both post-intervention and follow-up periods

(P < 0Æ001) but not between post-intervention and

follow-up period (P = 0Æ9) for both muscles. Within-

group effect sizes were large (d > 1Æ0) for both

follow-up periods in both muscles. The ANOVA

found a significant effect for time (F = 78Æ6;

P < 0Æ001) for changes in pain intensity and active

pain-free mouth opening (F = 17Æ1; P < 0Æ001). Sig-

nificant differences were found between pre-inter-

vention and both post-intervention and follow-up

periods (P < 0Æ001) but not between the post-

intervention and follow-up period (P > 0Æ7).

Within-group effect sizes were large (d > 0Æ8) for

both post-intervention and follow-up periods. The

application of treatment directed at the cervical

spine may be beneficial in decreasing pain intensity,

increasing PPTs over the masticatory muscles and an

increasing pain-free mouth opening in patients with

myofascial TMD.

KEYWORDS: cervical spine, temporomandibular dis-

order, pressure pain sensitivity

Accepted for publication 25 June 2009

ª 2009 Blackwell Publishing Ltd doi: 10.1111/j.1365-2842.2009.01980.x

Journal of Oral Rehabilitation 2009 36; 644–652

Introduction

Temporomandibular disorder (TMD) is a term which

includes several conditions involving the temporoman-

dibular joint and the muscles of mastication. The most

common symptoms of TMD include pain located over

the facial region and tenderness to palpation of the

masticatory structures. Some studies have shown

prevalence rate of TMD to be between 3% and 15%

in the Western population (1), with an incidence

between 2% and 4% (2). A recent survey determined

that the overall prevalence of TMD was 6Æ3% for

women and 2Æ8% for men (3).

It appears that an intimate functional relationship

exists between the mandibular and the head-neck

systems, as suggested by their anatomical and bio-

mechanical inter-relationships, although current

evidence is conflicting (4). Several epidemiological

studies have reported that patients with TMD often

experience symptoms of neck pain and that patients

with neck pain also suffered from symptoms in the

orofacial region (5–8). In addition, Eriksson et al. (9)

reported that mouth opening was accompanied by

head-neck extension and mouth closing by head-neck

flexion, with a precise temporal coordination between

jaw-neck movements dependent on the speed of the

movement (10).

The neuro-anatomical basis for the relationship

between the head and neck may be related to the

trigemino-cervical nucleus caudalis in the spinal grey

matter of the spinal cord at the C1–C3 level, where

there is a convergence on the nociceptive second order

neurons receiving trigeminal and cervical inputs (11).

The topographic arrangement of the trigeminal nucleus

caudalis allows the interchange of nociceptive infor-

mation between the cervical spine and the trigeminal

nerve (12). Studies have demonstrated that stimulation

of trigeminal-innervated structures evoked painful

sensations in the neck and vice versa (13, 14). In

addition, it has been reported that injection of an

inflammatory irritant into deep paraspinal tissues

results in a sustained activation of both jaw and neck

muscles (15, 16).

Several localized therapeutic modalities are often

used in the management of TMD, including mobiliza-

tion (17–19) or exercises (20, 21) of the temporoman-

dibular joint. As there is a connection between the neck

and the temporomandibular region, it can be hypo-

thesized that interventions targeted to the cervical spine

may also have an effect on patients with TMD.

Catanzariti et al. (22) suggested that neck pain patients

may respond to intervention applied to the temporo-

mandibular joint and that techniques applied to the

cervical spine may also have effect on the temporo-

mandibular system. To the best of our knowledge no

previous studies have investigated the effects of treat-

ment directed solely at the cervical spine in patients

with TMD. The purpose of this study was to investigate

the effects of joint mobilization directed at the cervical

spine plus an exercise protocol targeting the deep

cervical flexor muscles on intensity of pain and pressure

pain sensitivity in the muscles of mastication in patients

with myofascial TMD.

Materials and methods

Patients

Consecutive patients referred from four private dental

clinics between October 2007 and June 2008 partici-

pated in this study. Participants were eligible to partic-

ipate if they met the following criteria: (i) a primary

diagnosis of myofascial pain according to Axis I,

category Ia and Ib (i.e. myofascial pain with or without

limited opening) of the Research Diagnostic Criteria for

TMD (RDC ⁄ TMD) (23); (ii) bilateral pain involving the

masseter and temporal regions; (iii) presence of at least

one trigger point (TrP) in the masseter or temporalis

muscles; (iv) pain symptoms history of at least the

3 months previous to the study; and (v) intensity of the

pain of at least 30 mm on a 100 mm Visual Analogue

Scale (VAS). Trigger points were diagnosed following

the criteria described by Simons et al. (24): (i) presence

of a palpable taut band in a skeletal muscle; (ii)

presence of a hypersensitive tender spot within the

taut band; (iii) local twitch response elicited by the

snapping palpation of the taut band; and (iv) repro-

duction of the referred pain pattern of the TrP in

response to palpation. These criteria have demonstrated

good inter-examiner reliability (j) ranging from 0Æ84 to

0Æ88 (25).

Participants were excluded if they presented with any

of the following: (i) sign or symptoms of disc displace-

ment, arthrosis, or arthritis of the temporomandibular

joint, according to categories II and III of the

RDC ⁄ TMD; (ii) history of traumatic injuries (e.g.

fracture, whiplash); (iii) fibromyalgia syndrome (26);

(iv) diagnosis of systemic disease (rheumatoid arthritis,

C E R V I C A L S P I N E I N M Y O F A S C I A L T E M P O R O M A N D I B U L A R D I S O R D E R 645

ª 2009 Blackwell Publishing Ltd

systemic lupus erythematosus, or psoriatic arthritis); (v)

presence of neurological disorders (e.g. trigeminal

neuralgia); (vi) concomitant diagnosis of any primary

headache (tension-type headache or migraine); (vii)

subjects who had received any form of treatment

(physiotherapy, splint therapy and acupuncture) with-

in 3 months of the study. The study was conducted in

accordance with the Helsinki Declaration, and all

participants provided informed consent which was

approved by the local ethics committee.

Pain intensity

The VAS was used to record the patient’s level of pain at

baseline, 48 h after the last treatment (post-interven-

tion) and at 12-week follow-up period. The VAS is a

10 cm line anchored with a ‘0’ at one end representing

‘no pain’ and ‘10’ at the other end representing ‘the

worst pain imaginable’. Patients placed a mark along

the line corresponding to the intensity of their symp-

toms, which was scored to the nearest millimetre. The

VAS has been shown to be a reliable and valid

instrument for measuring pain intensity (27). It exhib-

its a minimal clinically important difference (MCID)

between 9 and 11 mm (28, 29).

Pressure pain threshold assessment

Pressure pain threshold (PPT) is defined as the amount

of pressure where the sense of pressure first changes to

pain (30). A mechanical pressure algometer (Pain

Diagnosis and Treatment Inc, Great Neck, NY, USA)

was used. This device consisted of a round rubber disc

(1 cm2) attached to a pressure (force) gauge. The gauge

displayed values in kilograms. As the surface of the

rubber tip was 1 cm2, the readings were expressed in

kg cm)2. The mean of three trials (intra-examiner

reliability) was calculated and used for the main

analysis. A 30-second resting period was allowed

between trials. The reliability of pressure algometry

was found to be high (ICC = 0Æ91 [95% confidence

intervals (CI): 0Æ82–0Æ97] (31). Pressure pain threshold

was assessed over bilateral masseter and the temporalis

muscles. The masseter point was located 1 cm superior

and 2 cm anterior from the mandibular angle, and the

temporal point was located on the anterior fibres of

temporal muscle, 2 cm above the zygomatic arch in the

middle part between lateral edge of the eye and the

anterior part of the helix. Pressure pain threshold levels

were assessed at pre-intervention, 48 h after the last

treatment (post-intervention) and at 12-week follow-

up period.

Active pain-free mouth opening

In a supine position, participants were asked to ‘open

the mouth as wide as possible without causing pain’. At

the end position of pain-free mouth opening, the

distance between upper-lower central incisors was

measured in millimetres. The intra-tester reliability of

this procedure was found to be high (ICC = 0Æ9–0Æ98)

(32). The mean of three trials was calculated and used

for the main analysis. Active pain-free mouth opening

was assessed pre-intervention, 48 h after the last

treatment (post-intervention) and at 12-week follow-

up period.

Treatment protocol

The treatment protocol included only interventions

directed at the cervical spine. The treatment techniques

were applied by the same physical therapist with

6 years of experience specializing in manipulative

therapy. All patients received a total of 10 sessions

over a 5-week period (twice a week). During the 10

treatment sessions all patients were treated with the

following techniques:

1 Upper cervical flexion mobilization: The patient was

supine with the cervical spine in a neutral position. The

therapist brought about a contact of the occipital bone

with the first finger and medial aspect of the hand, and

other hand over the frontal region of the patient’s head.

The mobilizing force was delivered by flexing the upper

cervical region using a combination of cephalic traction

with the occipital hand and caudal pressure with the

frontal hand (Fig. 1). The mobilization was applied at a

slow rate of one oscillation per 2 s (0Æ5 Hz) for a total

time of 10 min. This rate of mobilization was previously

used in another study (33).

2 C5 central posterior-anterior mobilization (34): The

patient was prone with the cervical spine in a neutral

position. The therapist placed the tips of his thumbs on

the posterior surface of the C5 spinous process, while the

other fingers rested gently around the patients’ neck

(Fig. 2). A grade III (large amplitude movement that

moved into the resistance limiting the range of move-

ment) posterior-anterior technique was applied centrally

to the C5 spinous process. The mobilization was applied

R . L A T O U C H E et al.646

ª 2009 Blackwell Publishing Ltd

at a rate of two oscillations per second (2 Hz). The

mobilizations were performed for a total of 9 min,

divided into 3-min intervalswith a 1 min rest in between.

3 Cranio-cervical flexor stabilization exercise: With the

aim to focus on the deep flexor muscles of the cervical

region, we followed the protocol described by Jull et al.

(35). Patients performed a cranio-cervical flexion exer-

cise in the supine position, which involved flexion of

the cranium (head) on the cervical spine (neck) while

ensuring that the back of the head remained in contact

with the supporting surface, in an effort to facilitate

activation of the deep cranio-cervical flexor muscula-

ture (particularly the longus capitis muscle) with

minimal activity of the superficial cervical flexors

(sternocleidomastoid and scalene muscles) (Fig. 3).

The contraction was graded through feedback from a

pressure biofeedback device (Stabilizer; Chattanooga

Group Inc., Chattanooga, TN, USA) that monitored the

flattening of the cervical lordosis due to the cranio-

cervical flexion movement from contraction of the deep

cervical flexor muscles (36). Falla et al. (37) demon-

strated that the cranio-cervical flexion test was accom-

panied by increased electromyographic activity in the

deep cervical flexor muscles. Additionally, increases in

the electromyographic activity of the deep cervical

flexors did not occur during other neck or jaw move-

ments, supporting the specificity of this test (38).

Patients first performed the correct cranio-cervical

flexion action with the following instructions: gently

nod your head as though you were saying ‘yes’ (Fig. 3).

The therapist monitored the superficial muscles by

palpation and identified the target level of the biofeed-

back where the patient could hold 10 s without use of

superficial neck flexor muscles, and without a quick or

jerky movement. Once the subject could perform the

movement correctly, the target level was established

and training began at this point. The baseline pressure

in the biofeedback device was 20 mmHg and the

patient was instructed to contract the deep neck flexors

to reach five pressure targets in increments of 2 mmHg

(35). The pressure increments were determined by

the level the patient could hold comfortably while

Fig. 1. Upper cervical flexion mobilization. Within one hand over

the occipital bone and the other hand over the frontal region of

the patient’s head, the therapist applies a mobilization force

inducing an upper cervical flexion using a combination of cephalic

traction with the occipital hand and caudal pressure with the

frontal hand.

Fig. 2. C5 central posterior-anterior mobilization. The therapist

placed the thumbs over the posterior surface of the C5 spinous

process and a posterior-anterior mobilization force is applied.

Fig. 3. Cranio-cervical flexor stabilization exercise.

C E R V I C A L S P I N E I N M Y O F A S C I A L T E M P O R O M A N D I B U L A R D I S O R D E R 647

ª 2009 Blackwell Publishing Ltd

maintaining a 10-second contraction with no pain.

Participants sustained the contraction for 10 repetitions

of 10-second duration, with a 10-second rest interval

between each contraction. Once this target was

achieved, the exercise progressed to the next pressure

target, repeating the process at the new pressure target,

first increasing the holding time and then the repeti-

tions. This exercise protocol has been used in previous

studies in patients with neck pain (39–41).

Statistical analysis

Statistical analysis was conducted with the SPSS 14.5

package.* Mean, s.d., or 95% CI of the values were

presented. The Kolmogorov–Smirnov test showed a

normal distribution of the data (P > 0Æ05). A 2 · 3

mixed model analysis of variance (ANOVA) with time

(pre-intervention, post-intervention and follow-up)

and side (right or left) as the within-subjects variables

was used to examine the effects of the treatment on PPT

over the masseter or the temporalis muscles. A one-way

repeated measure ANOVA with time (pre-intervention,

post-intervention and follow-up) as within-subject

variable was used to investigate the effects of the

treatment on spontaneous pain and active mouth

opening. The Bonferroni test was used for post hoc

analysis. Within-group effect size was calculated using

Cohen’s coefficient (d) (42). An effect size greater than

0Æ8 was considered large; around 0Æ5, moderate; and less

than 0Æ2, small. A P-value less than 0Æ05 was considered

as statistically significant for all analyses.

Results

A total of 19 patients, 14 females and 5 males, aged 19–

57 years old (mean age � s.d.: 37 � 10 years) partici-

pated. All subjects were right hand dominant. None of

the patients started drug therapy during the time of the

study. In this sample of patients with TMD the average

duration of symptoms was 9Æ2 months (95% CI: 7Æ7–

10Æ6 months), and the mean intensity of spontaneous

pain was 55Æ53 (95% CI: 51Æ4–59Æ6).

Pressure pain threshold levels

The 2 · 3 mixed model ANOVA revealed a significant

effect for time (F = 77Æ8; P < 0Æ001) but not for side

(F = 0Æ2; P = 0Æ7) for changes in PPT over the masseter

muscle. Post hoc testing revealed significant differences

between pre-intervention and both post-intervention

and follow-up periods (P < 0Æ001). However, no signif-

icant difference was identified between the post-inter-

vention and follow-up period (P = 0Æ9) for both

masseter muscles. Within-group effect sizes were large

(d > 1Æ0) for both follow-up periods in bilateral masse-

ter muscles. Table 1 details pre-intervention, post-

intervention, follow-up, and change scores of PPT

levels bilateral in both masseter and temporalis

muscles.

The mixed model ANOVA also found a significant effect

for time (F = 66Æ8; P < 0Æ001) but not for side (F = 0Æ07;

P = 0Æ8) for changes in PPT levels over the temporalis

muscle. The post hoc analysis found significant differ-

ences between pre-intervention and both post-inter-

vention and follow-up periods (P < 0Æ001). However,

no significant difference was identified between the

Table 1. Changes in pressure pain thresholds (kg cm)2) over the

masseter and temporalis muscles

Pressure pain threshold (kg cm)2)

in the right masseter muscle

Pre-intervention 2Æ8 � 0Æ7 (2Æ5 ⁄ 3Æ1)

Post-intervention 3Æ9 � 0Æ5 (3Æ7 ⁄ 4Æ2)

Follow-up 3Æ9 � 0Æ6 (3Æ6 ⁄ 4Æ2)

Pre- ⁄ post-differences 1Æ1 � 0Æ8 (0Æ8 ⁄ 1Æ6)

Pre ⁄ follow-up differences 1Æ1 � 0Æ7 (0Æ7 ⁄ 1Æ4)

Pressure pain threshold (kg cm)2)

in the left masseter muscle

Pre-intervention 2Æ3 � 0Æ6 (1Æ9 ⁄ 2Æ6)

Post-intervention 3Æ6 � 0Æ8 (3Æ4 ⁄ 3Æ9)

Follow-up 3Æ5 � 0Æ7 (3Æ1 ⁄ 3Æ8)

Pre- ⁄ post-differences 1Æ3 � 0Æ7 (1Æ0 ⁄ 1Æ6)

Pre ⁄ follow-up differences 1Æ2 � 0Æ8 (0Æ8 ⁄ 1Æ5)

Pressure pain threshold (kg cm)2)

in the right temporalis muscle

Pre-intervention 2Æ4 � 0Æ6 (2Æ1 ⁄ 2Æ7)

Post-intervention 3Æ7 � 0Æ5 (3Æ4 ⁄ 3Æ9)

Follow-up 3Æ5 � 0Æ7 (3Æ2 ⁄ 3Æ8)

Pre- ⁄ post-differences 1Æ3 � 0Æ7 (0Æ9 ⁄ 1Æ6)

Pre ⁄ follow-up differences 1Æ1 � 0Æ7 (0Æ7 ⁄ 1Æ4)

Pressure pain threshold (kg cm)2)

in the left temporalis muscle

Pre-intervention 3Æ0 � 0Æ7 (2Æ7 ⁄ 3Æ3)

Post-intervention 3Æ9 � 0Æ6 (3Æ6 ⁄ 4Æ2)

Follow-up 4Æ0 � 0Æ6 (3Æ6 ⁄ 4Æ3)

Pre- ⁄ post-differences 0Æ9 � 1Æ0 (0Æ4 ⁄ 1Æ4)

Pre ⁄ follow-up differences 1Æ0 � 0Æ8 (0Æ6 ⁄ 1Æ4)

Scores are expressed as mean � s.d. (95% confidence interval).*SPSS, Chicago, IL, USA.

R . L A T O U C H E et al.648

ª 2009 Blackwell Publishing Ltd

post-intervention and follow-up period (P = 0Æ9) for

both muscles. Within-group effect sizes were large

(d > 0Æ9) for both follow-up periods in bilateral tempo-

ralis muscles.

Pain

The ANOVA found a significant effect for time (F = 78Æ6;

P < 0Æ001) for changes in pain. Post hoc revealed

significant differences between pre-intervention and

both post-intervention and follow-up periods

(P < 0Æ001). However, no significant difference was

identified between the post-intervention and follow-up

period (P = 0Æ9). Within-group effect sizes were large

(d > 3Æ0) for both post-intervention and follow-up

periods. Table 2 shows pre-intervention, post-interven-

tion, follow-up and differences in scores of pain.

Active pain-free mouth opening

The ANOVA found a significant effect for time (F = 17Æ1;

P < 0Æ001) for changes in active mouth opening. Post

hoc analysis found significant differences between pre-

intervention and both post-intervention (P < 0Æ001)

and follow-up periods (P = 0Æ006). However, no signif-

icant difference was identified between the post-inter-

vention and follow-up period (P = 0Æ7). Within-group

effect sizes were large for both post-intervention

(d > 1Æ0) and follow-up (d > 0Æ8) periods. Table 2 sum-

marizes pre-intervention, post-intervention and follow-

up and change scores for VAS and active pain-free

mouth opening.

Discussion

The results of our study demonstrated that patients

with myofascial TMD treated with manual therapy and

exercise directed at the cervical spine experienced an

immediate decrease (48 h after 10 treatment sessions)

in facial pain, an increase in PPTs over the masticatory

muscles and an increase in pain-free mouth opening.

Additionally, these changes were maintained 12 weeks

after discharge. However, as this was a single cohort

design we could not say if these outcomes were the

result of treatment directed at the cervical spine or

some other variable.

The effect sizes were large for all of outcomes at both

immediate and the 12-week follow-up period. Addi-

tionally, it should be noted that the reduction in pain

was not only statistically significant but also clinically

meaningful as it exceeded the MCID on the VAS,

identified as 9–11 mm (28, 29). The relatively narrow

CI provide greater assurance when making clinical

decisions regarding the treatment effect identified in

this study (43). It should also be noted that even the

lower bound estimates for the 95% CI fell above the

MCID and provided evidence that cervical spine inter-

ventions might be beneficial in the management of

patients with TMD. Mellick and Mellick (44) reported

that treatment of the cervical spine with intra-muscular

injections was effective for reducing symptoms in

patients with orofacial pain. However, our study is the

first to provide preliminary evidence that manual

therapy and exercise directed at the cervical spine

may be beneficial in decreasing facial pain in these

patients.

The increases in PPT levels over both masseter and

temporalis muscles suggests that a hypoalgesic effects

may be induced by treatment of the cervical spine.

Previous evidence suggests that the hypoalgesic effects

occur after manual therapy interventions because of

the activation of the descending inhibitory pathways

(45, 46). It has been demonstrated that joint mobiliza-

tion of the cervical spine produced an increase of 25%

in PPTs in patients with lateral epicondylalgia (47) and

in patients with neck pain (48). In fact, O’Leary et al.

(49) found that the application of the cranio-cervical

flexor exercise protocol used in the current study

induced an immediate local hypoalgesic response in

patients with neck pain. Although the activation of

descending inhibitory pathways following the applica-

tion of manual procedures has not been demonstrated

Table 2. Changes in spontaneous pain (VAS) and active mouth

opening (mm)

Spontaneous orofacial pain

(Visual Analogue Scale)

Pre-intervention 55Æ5 � 8Æ6 (51Æ4 ⁄ 59Æ6)

Post-intervention 20Æ9 � 7Æ1 (17Æ5 ⁄ 24Æ4)

Follow-up 18Æ7 � 7Æ1 (15Æ3 ⁄ 22Æ1)

Pre- ⁄ post-differences )34Æ6 � 8Æ9 ()38Æ9 ⁄ )30Æ3)

Pre ⁄ follow-up differences )36Æ8 � 12Æ0 ()42Æ6 ⁄ )31Æ1)

Active mouth opening (mm)

Pre-intervention 38Æ3 � 5Æ0 (35Æ8 ⁄ 40Æ7)

Post-intervention 42Æ8 � 2Æ7 (41Æ5 ⁄ 44Æ1)

Follow-up 43Æ1 � 2Æ9 (41Æ7 ⁄ 44Æ5)

Pre- ⁄ post-differences 4Æ5 � 3Æ8 (2Æ8 ⁄ 6Æ4)

Pre ⁄ follow-up differences 4Æ8 � 5Æ8 (2Æ1 ⁄ 7Æ6)

Scores are expressed as mean � s.d. (95% confidence interval).

C E R V I C A L S P I N E I N M Y O F A S C I A L T E M P O R O M A N D I B U L A R D I S O R D E R 649

ª 2009 Blackwell Publishing Ltd

in patients with TMD this neurophysiological mecha-

nism seems plausible for explaining the bilateral hypo-

algesic effects that occurred in the trigeminal region

with interventions targeted to the cervical spine.

Nevertheless, as no signs of neck dysfunctions and ⁄ or

neck symptoms reported by the patients with TMD

were included in this study, it was difficult to establish a

relationship between the treatment of the cervical spine

and the orofacial effects found in the current study. As

we have discussed, it may be that the effects of cervical

interventions are more generalized rather than specific

for the trigeminal area. Future studies should investi-

gate these neurophysiological mechanisms between the

cervical spine and the orofacial region in patients with

myofascial TMD.

We also found an increase of 4Æ5 mm in pain-free

mouth opening after the treatment of the cervical

spine, which was slightly superior to the results of some

studies investigating changes in active mouth opening

after the treatment of masseter muscle TrPs which

ranged from 2 mm (50) to 4 mm (51). A recent study

has reported that the application of a thrust manipu-

lation targeted to the upper cervical spine resulted in an

increase in active mouth opening (3Æ5 mm) in women

with mechanical neck pain (52). As the application of

cervical interventions induced similar improvements in

mouth opening when compared with treatment of the

masseter muscle, perhaps cervical techniques might be

used as a complementary approach to manage pain in

patients with myofascial TMD. In addition, in patients

with allodynic responses in the facial region, in whom

the manual application of local interventions are often

extremely painful, an indirect approach directed to the

upper cervical spine may be beneficial.

One possible explanation for the increase in pain-free

mouth opening may be related to changes in the

positional afferent inputs of the cervical spine induced

by the protocol. Some studies have demonstrated that

position of the upper cervical spine modifies range of

motion of the mouth (53, 54) Others have shown that

the position of the cervical spine is influenced by the

masticatory muscles (55, 56). De Laat et al. (57) found

that a high percentage of patients with TMD also have

limited movement of the upper cervical spine. There-

fore, it is possible that the protocol applied in the

current study can improve the biomechanical adapta-

tion of the cervical spine with relation to the tempo-

romandibular joint, increasing pain-free mouth

opening. It is also plausible that the reduction in

spontaneous pain in the orofacial region will also

increase pain-free mouth opening.

Our study had several limitations. First, the sample

size was small. Second, we did not include a control

group, so we could not infer a direct cause and effect

relationship between the outcomes and the interven-

tions directed at the cervical spine. It is plausible that

the improvements seen in the patients may be related

to the passage of time. However, we would expect this

to be unlikely given the current duration of symptoms

(9Æ2 months). Furthermore, it was not possible to assess

gender differences because the size of the sample was

small. Future randomized controlled trials with a

greater number of participants and including a control

group which received traditional treatment for myo-

fascial TMD should be conducted in order to further

elucidate the effectiveness interventions directed at the

cervical spine for patients with TMD.

Conclusions

The results of our study demonstrated that patients

with myofascial TMD treated manual therapy and

exercise directed at the cervical spine might be bene-

ficial in decreasing facial pain, increasing PPTs over the

masticatory muscles and increasing pain-free mouth

opening. Furthermore, these changes were maintained

12 weeks after discharge in our population. The effect

sizes were large for all of outcomes at both the 48 h and

12 weeks follow-up periods. Future randomized studies

should investigate the potential of a cause and effect

relationship.

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Correspondence: Roy La Touche Arbizu, Facultad de Medicina,

Universidad San Pablo CEU, Calle Tutor, 35, 28008 Madrid, Spain.

E-mail: [email protected]

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192

5.7 Estudio VII

La Touche R, París-Alemany A, Mannheimer JS, Angulo-Díaz-Parreño S, Bishop MD,

Lopéz-Valverde-Centeno A, von Piekartz H, Fernández-Carnero J. Does mobilization of

the upper cervical spine affect pain sensitivity and autonomic nervous system function

in patients with cervico-craniofacial pain?: A randomized-controlled trial. Clin J Pain.

2013 Mar;29(3):205-15.

Objetivos del estudio

Los objetivos de este estudio fueron investigar los efectos de la movilización antero-

posterior de la región cervical superior en la modulación del dolor en las regiones

craneofacial y cervical y su influencia en el sistema nervioso simpático.

Resultados

Los UDPs en las regiones craneofacial y cervical aumentó significativamente (P

<0,001) y la intensidad del dolor disminuyó significativamente (P <0,001) en el grupo

de tratamiento en comparación con placebo. La movilización produjo una respuesta

simpatoexcitatoria demostrado por un aumento significativo de la conductancia de la

piel, la frecuencia respiratoria y la frecuencia cardíaca (p <0,001), pero no en la

temperatura de la piel (P = 0,071), después de la aplicación de la técnica en

comparación con el placebo.

Conclusiones

Este estudio proporciona una evidencia preliminar del efecto hipoalgésico a corto plazo

de la movilización articular de la región cervical en las regiones craneofacial y cervical

de pacientes con DCCF de origen miofascial, lo que sugiere que la movilización puede

causar una modulación nociceptiva inmediata en el CTC. Se observó una respuesta

simpatoexcitatoria, lo que podría estar relacionado con el efecto hipoalgésico inducido

por la técnica, aspecto a ser confirmado en estudios futuros.

Does Mobilization of the Upper Cervical Spine Affect PainSensitivity and Autonomic Nervous System Function

in Patients With Cervico-craniofacial Pain?

A Randomized-controlled Trial

Roy La Touche, PT, MSc,*wz Alba Parıs-Alemany, PT, MSc,zJeffrey S. Mannheimer, PT, PhD, CCTT,y Santiago Angulo-Dıaz-Parreno, MSc,wz8

Mark D. Bishop, PT, PhD,z# Antonio Lopez-Valverde-Centeno, MD, PhD,**Harry von Piekartz, PT, PhD,ww and Josue Fernandez-Carnero, PT, PhDwzz

Objectives: The aims were to investigate the effects of anterior-posterior upper cervical mobilization (APUCM) on pain modu-lation in craniofacial and cervical regions and its influence on thesympathetic nervous system.

Methods: Thirty-two patients with cervico-craniofacial pain ofmyofascial origin were randomly allocated into experimental orplacebo groups. Each patient received 3 treatments. Outcomemeasures included bilateral pressure pain thresholds assessed atcraniofacial and cervical points preintervention, after the secondintervention and after the final treatment. Pain intensity andsympathetic nervous system variables (skin conductance, breathingrate, heart rate, and skin temperature) were assessed before andimmediately after each intervention.

Results: The pressure pain thresholds in the craniofacial and cer-vical regions significantly increased (P<0.001) and pain intensitysignificantly decreased (P<0.001) in the treatment group com-pared with placebo. APUCM also produced a sympathoexcitatoryresponse demonstrated by a significant increase in skin con-ductance, breathing rate, and heart rate (P<0.001), but not in skintemperature (P=0.071), after application of the technique com-pared with placebo.

Discussion: This study provided preliminary evidence of a short-term hypoalgesic effect of APUCM on craniofacial and cervicalregions of patients with cervico-craniofacial pain of myofascialorigin, suggesting that APUCM may cause an immediate noci-ceptive modulation in the trigeminocervical complex. We also ob-served a sympathoexcitatory response, which could be related to

the hypoalgesic effect induced by the technique, but this aspectshould be confirmed in future studies.

Key Words: manual therapy, neck pain, temporomandibular

disorders, orofacial pain, craniofacial pain

(Clin J Pain 2013;29:205–215)

Discomfort resulting from temporomandibular disorders(TMDs) is representative of many chronic craniofacial

pain (CCFP) conditions.1 TMD demographics usuallyconsist of working women in the 3rd decade of life withhigh stress levels.2 TMDs are characterized by a focal site oftenderness that provokes nociceptive input and, whenchronic, contributes to the development of central sensiti-zation. Patients with TMDs are known to have greatertemporal summation of pain, suggesting hyperexcitabilityof the central nociceptive system.3,4 More specifically,chronic muscular TMD pain is associated with a generaldysfunction of the central nociceptive system that is con-comitant with central nociceptive neuronal hyperexcitabilityand dysfunction of the descending inhibitory pain systems.5

Women have a 3 times greater risk of experiencing chronicmasticatory myofascial pain than men.6 Patients with TMDsof myofascial origin are also characterized by a general hy-persensibility to mechanical pain stimuli, presenting lowercraniofacial pressure pain thresholds (PPT) of both thepainful and nonpainful side compared with healthy controls.7

Some studies suggest a functional relationship betweenthe jaw and head-neck with regard to craniofacial and cer-vical spine and a concomitance between craniofacial painand neck pain.2,8–10 Patients with craniofacial pain are attwice the risk of experiencing neck pain than the generalpopulation.2 Restricted segmental movements of the uppercervical vertebrae (C0-C3) with a greater percentage of up-per trapezius and sternocleidomastoid tender points exist inpatients with TMDs compared with a control group.11

In addition, Eriksson et al8 demonstrated coordi-nated articular patterns of movement between the temporo-mandibular, atlanto-occipital, and cervical joints, joints thatalso have known sensory-motor interaction via the trige-minocervical complex (TCC). Disturbance of this con-nection between jaw and head-neck movements has beenidentified in patients with whiplash-associated disorders.12

Spinal manual therapy (SMT) is used by physicaltherapists (PTs) to treat chronic musculoskeletal pain.13

Received for publication June 21, 2011; revised February 14, 2012;accepted February 17, 2012.

From the *Department of Physical Therapy, La Salle UniversityCenter, Faculty of Health Science, Aravaca; wResearch Group ofMusculoskeletal Pain and Motor Control, Universidad Europea deMadrid, Villaviciosa de Odon; zInstitute of Neuroscience andCraniofacial Pain (INDCRAN); 8Faculty of Experimental Science,Universidad San Pablo CEU; zzDepartment of Physical Therapy,Occupational Therapy, Rehabilitation and Physical Medicine,Universidad Rey Juan Carlos, Alcorcon, Madrid; **Departmentof Surgery, Faculty of Medicine and Dentistry, Universidad deSalamanca, Salamanca, Spain; yProgram in Physical Therapy,Columbia University, NY; zDepartment of Physical Therapy;#Center for Pain Research and Behavioral Health, University ofFlorida, Gainesville, FL; and wwFaculty of Business, Managementand Social Science, University of Applied Science, Osnabruck,Germany.

The authors declare no conflict of interest.Reprints: Roy La Touche, PT, MSc, INDCRAN, C/Canos del Peral

11, Bajo Izquierdo, 28013 Madrid, Spain (e-mail: [email protected]).

Copyright r 2012 by Lippincott Williams & Wilkins

ORIGINAL ARTICLE

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Various techniques such as passive manipulation and mo-bilization, active mobilization, neuromuscular facilitation,and articular glides are included under the general term ofSMT.14–17 Many SMTs have demonstrated hypoalgesiceffects. This hypoalgesic effect is not antagonized by na-loxone and does not exhibit tolerance,18 supporting thetheory that SMTs activate a nonopioid inhibitory system.In addition, a concomitant activation of the sympatheticnervous system (SNS) occurs after SMT, with the degree ofactivation depending on the technique.19,20

Many studies have investigated the effects of SMT onlower cervical pain,14–16,21 but there is no randomized-controlled trial in which SMT is used to diminish cranio-facial pain. George et al22 compared cervical manipulationwith a soft tissue technique at the cervical-cranial junctionto improve mouth opening in healthy controls, but no sig-nificant results were obtained. Another study examined amanual therapy and therapeutic exercise protocol appliedat the cervical spine, to treat craniofacial pain of myofascialorigin in a cohort intervention study, which resulted in anincrease in the PPT in the masticatory muscles and in-creased mouth opening.23

Consequently, the aims of this study were to extendprevious work by investigating the neurophysiologicaleffects of SMT in patients with CCFP of myofascial origin.Specifically, we studied passive anterior-posterior uppercervical mobilization (APUCM). We expected pain sensi-tivity in the craniofacial and cervical regions to decrease inresponse to treatment. In addition, we expected to observethe sympathetic influence of this technique on skin con-ductance (SC), breathing rate (BR), heart rate (HR), and skintemperature (ST).

MATERIALS AND METHODS

Selection and Description of ParticipantsThirty-two patients with CCFP of myofascial origin

referred from 2 private dental clinics and 3 universities inMadrid, Spain, were recruited from January 2009 to May2010. We defined the term CCFP of myofascial origin aspain and dysfunction located at the cervical and mastica-tory muscles. Patients were selected if they met all of thefollowing criteria: (1) a primary diagnosis of myofascialpain as defined by axis I, category Ia and Ib (eg, myofascialpain with or without limited opening of the mouth) of theResearch Diagnostic Criteria for Temporomandibular Dis-orders24; (2) bilateral pain involving the masseter, temporalis,upper trapezius, and suboccipital muscles; (3) a duration ofpain of at least 3 months; (4) a pain intensity correspondingto a weekly average of at least 30mm on a 100-mm visualanalog scale (VAS); (5) neck and/or shoulder pain withsymptoms provoked by neck postures or neck movement;(6) Neck Disability Index (NDI)25,26 Z15 points; and (7)presence of bilateral trigger points (TrPs) in masseter, tem-poralis, upper trapezius, and suboccipital muscles. TrPs werediagnosed according to the following criteria27: (1) presenceof a palpable taut band in the skeletal muscle; (2) presence ofa hypersensitive tender spot within the taut band; (3) localtwitch response elicited by the snapping palpation of the tautband; and (4) reproduction of referred pain in response toTrP compression.

All patients in the study were examined by a physi-otherapist with 7 years of experience managing craniofacialand cervical disorders. Patients were excluded if they pre-sented any signs, symptoms, or history of the following

diseases: (1) intra-articular temporomandibular disk displace-ment, osteoarthrosis, or arthritis of the temporomandibularjoint, according to categories II and III of the ResearchDiagnostic Criteria for Temporomandibular Disorders24,28;(2) history of traumatic injuries (eg, contusion, fracture, orwhiplash injury); (3) systemic diseases such as fibromyalgia,systemic erythematous lupus, or psoriatic arthritis; (4) neu-rological disorders (eg, trigeminal neuralgia); (5) concomitantmedical diagnosis of any primary headache (tension type ormigraine); (6) unilateral neck pain; (7) cervical spine surgery;(8) clinical diagnosis of cervical radiculopathy or myelopathy;and (9) history of previous physical therapy intervention forthe cervical region. Each participant received a thorough ex-planation of the content and purpose of the treatment beforesigning an informed consent form related to the procedures,which was approved by the local ethics committee in ac-cordance with the Helsinki Declaration.

Research DesignA randomized, double-blind placebo-controlled study

was performed. Patients were blind to which interventionthey received, and an independent assessor, blind to inter-vention assignment made the measurements and registeredthe data. Patients were randomly allocated to either treat-ment intervention or sham intervention. Randomizationwas performed by a computer generated random-sequencetable created with Graphpad software (GraphPad SoftwareInc., CA) before the beginning of the study. The random-ization sequence used a balanced block design in whichrandomization occurred in blocks of 2.

Sample Size CalculationA pilot study was performed with 5 patients in the

treatment group and 5 patients in the sham group to cal-culate the sample size. We used data indicative of the per-cent change in the PPT of the 2 assessed points: 1 at themasseter muscle and 1 at the trapezius muscle.

Sample sizes were calculated to obtain a power of 80%to detect changes in the bilateral contrast of the null hy-pothesis of equal means between the 2 groups, with 5%significance, taking into account the possibility that the SDsof the groups could be different. According to the samplecalculations which took into account the fact that the cal-culation was based on 2 different variables, we obtained 2possible results: 14 patients in each group or 16 patients ineach group. We decided to include 16 patients per group toanticipate the possible loss of patients.

Demographic and Clinical DataEach of the participants completed a questionnaire

to determine if they met the criteria for inclusion or ex-clusion. This questionnaire included demographic data,screening questions for TMDs from the American Acad-emy of Orofacial Pain,29 a body chart on which patientsmarked the location of their pain, and several questionsabout the characteristics of their pain such as “whendid it start?,” “what makes your pain worse?,” “what makesit better?,” and “what kind of pain is it?” To meetthe criteria to participate in the study, patients had to passan initial physical examination performed by a single in-vestigator to rule out the presence of nerve root com-pression.

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Instrumentation and Measurements

Self-reported VariablesPatients completed the Beck Depression Inventory

(BDI),30 the State-Trait Anxiety Inventory (STAI),31 andthe NDI25,26 to quantify their psychophysical state. TheBDI is a 21-item self-report instrument intended to assessthe existence and severity of symptoms of depression. Thereis a 4-point scale for each item ranging from 0 to 3. The resultsof each item, corresponding to a symptom of depression, aresummed to yield a single score for the BDI. A total score of0 to 13 is considered minimal, 14 to 19 mild, 20 to 28 mod-erate, and 29 to 63 severe depression. The BDI showed goodinternal consistency (a coefficient 0.86).30

The STAI31 is a 40-item self-report questionnaire de-signed to assess symptoms of anxiety. It consists of 2 in-dependent scales, a state anxiety scale and a trait anxietyscale, with 20 items each, resulting in a score between 20and 80. Higher scores indicate greater levels of anxiety. Thestate and trait scales explore anxiety as a current emotionalstate and as a personality trait, respectively.

The NDI,25,26 which measures perceived neck disability,consists of 10 items that assess different functional activitiesand uses a 6-point scale ranging from 0 (no disability) to 5(complete disability). The overall score (out of 100) is ob-tained by adding the score for each item and multiplyingby 2. A higher score indicates greater pain and disability. Thevalidity, reliability, and responsiveness of the NDI have beendemonstrated.26

Pain IntensityThe VAS was used to measure pain intensity of the

cervico-craniofacial region at rest and before and after eachtreatment. The VAS is comprised of a 100mm horizontalline in which the left side represents “no pain” and the rightside represents “worst pain.” The patient placed a mark onthe line at the point that they felt represented the intensityof their pain at the time. Pain intensity was quantified bythe assessor in millimeters. This scale has proven its reli-ability and validity for measuring pain intensity.32

Pressure Pain ThresholdPPT is defined as the minimum amount of pressure

needed to provoke a pain sensation.33 We used a digitalalgometer (Model FDX 10; Wagner Instruments, Greenwich,CT) comprised of a rubber head (1 cm2) attached toa pressure gauge, which measures in kg with thresholds ex-pressed in kg/cm2. The protocol consisted of 3 measurementswith an interval of 30 seconds between each measurement.The average of the 3 measurements was calculated to obtain asingle value for each one of the measured points in each ofthe assessments. This algometric method has high reliability(ICC=0.91, 95% CI, 0.82-0.97) for measuring PPT.34 PPTswere assessed bilaterally at 2 points in the masseter muscle(M1 and M2), 2 points in temporalis muscle (T1 and T2),suboccipital muscles, C5 zygapophyseal joint, and uppertrapezius muscle. The device was applied perpendicular to theskin, and the patients were asked to raise their hand themoment when the pressure started to change to a pain sen-sation, at which point the assessor stopped applying pressure.This procedure was performed 3 times: before the firsttreatment session (pretreatment outcome), after the secondtreatment session, and after the third treatment session(2 posttreatment outcomes).

Anatomic references for the algometric measurementsincluded the following: M1—2.5 cm anterior to the tragusand 1.5 cm inferior to the zygomatic arch; M2—1 cm su-perior and 2 cm anterior from the angle of the jaw; T1(anterior fibers of the muscle)—3 cm superior to the zy-gomatic arch in the middle point between the end of the eyeand the anterior part of the helix of the ear; T2 (middlefibers of the muscle)—2.5 cm superior from the helix of theear; suboccipital muscles—2 cm inferior to the occipitalcondyles; C5 zygapophyseal joint—2 cm lateral to the spi-nous process of C6; trapezius muscle—2.5 cm above thesuperior medial angle of the scapula.

Changes in the SNSSeveral characteristics were measured to assess the

SNS: SC, HR, BR, and ST. Measurements were taken be-fore and after each of the 3 treatment sessions. The re-cording device used was I-330-C2+ 6-channel biofeedbacksystem (J&J Engineering Inc., Poulsbo, WA) the MC-6SYsensor was used to measure SC and ST. During the meas-urements 2 electrodes were placed on the tip of the secondand third fingers of the left hand to measure the SC with thetemperature sensor attached to the tip of the fourth fingeralso at the left hand. The MC-5D electrodes used to meas-ure HR were applied longitudinally at the anterior and ra-dial aspect of the wrists and held with bracers. To measureBR, an MC-3MY breathing sensor was placed around thechest like a belt passing over the xiphoid process.

ProcedureThe experiment consisted of 3 treatment sessions. Each

patient received 3 sessions over 2 weeks, and the entire ex-periment lasted approximately 8 months.

The evaluator was a PT with extensive experience intaking the experimental measurements. During the first as-sessment, pretreatment data were obtained; after measuringthe PPT and VAS, the sensors were applied, and the patientwas instructed to lie down on a couch and relax. The roomtemperature was controlled at 251C. After 10 minutes (timedetermined for the patient to come to a normal baseline),the first record of the sympathetic parameters was regis-tered. The patient was then randomly assigned to 1 of the 2intervention groups, and the therapeutic technique wasapplied. Immediately after finishing the technique, SNSvariables were measured, and 5 minutes after the technique,VAS results were registered again. In the second and thirdtreatment session, the SNS variables and VAS were meas-ured using the same protocol (pretreatment and posttreat-ment data), but PPTs were taken only 5 minutes after theend of the treatment (posttreatment data). Therefore, weobtained 3 pretreatment and 3 posttreatment measurementsof SNS and VAS parameters and 1 pretreatment and 2posttreatment measurements (after the second and thirdsessions) of PPT.

Treatment TechniqueAPUCM directly influences the 3 upper cervical seg-

ments (C0-C3). The patient was placed in a supine positionwith a neutral position of the cervical spine. The PT heldthe occipital region of the patient with both hands to stabilizeand maintain the position of the upper cervical structures,while applying a posterior directed force on the frontal re-gion of the patient (anterior to posterior force) with the an-terior part of the shoulder. The mobilization was applied at aslow rate of 1 oscillation per 2 seconds (0.5Hz) controlled

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with an MA-30 digital metronome (Korg Inc., Japan). Thisoscillation rate has been used previously with a differentmanual therapy technique.19 The total time of mobilizationwas 6 minutes. Mobilization was applied in 3 intervals of2 minutes, with 30 seconds of rest in between, resulting in atotal of 7 minutes.

Sham TechniqueTo simulate the treatment technique, the PT applied

the same grips used with the treatment technique: 2 handsunder the occipital bone with the anterior part of 1 shoulderpositioned anterior to the frontal bone, with the patient insupine position. However, mobilization was not applied tothe cervical spine. The contact with the patient was held for3 intervals of 2 minutes with 30 seconds of rest in between.

Both techniques (treatment and sham) were applied bythe same PT, and each participant received the followingexplanation about the intervention: “A physical therapistwill apply a technique on your neck with one hand placedon the posterior part of your neck and the other one onyour forehead. The purpose is to obtain changes in yourneck and craniofacial pain.”

StatisticsStatistical analysis was performed with SPSS version

15.0. A Kolmogorow-Smirnov test was used to determinewhether the sample was consistent with a normal distri-bution (P>0.05). Student t test was used to analyze self-reported psycophysical variables (NDI, STAI, and BDI)and pain duration by comparing the preintervention datafor the treatment and sham groups.

The SNS variables (ST, HR, BR, SC) and VAS weretested with a 2�3 repeated measures analysis of variance(ANOVA); the factors analyzed were time (pre-post) andgroup (treatment and sham). Time�group interactions werealso analyzed. Post hoc analysis with Bonferroni correctionswas performed for specific comparisons between variables.

To determine differences between sessions in VAS andSNS variables, a 2-way ANOVA was used, which analyzedintersession factor and group� intersession interaction(presession 1, presession 2, presession 3). The percentchange for the SNS variables and VAS was obtained rela-tive to the percent change between each session and thepercent of the total of the means in both groups. A 1-wayANOVA was used to analyze the percent change in groupfactor and time factor between sessions (% change session1, % change session 2, % change session 3). The percentchange of the total of the means of the 3 sessions in thetreatment and placebo groups was analyzed with a Studentt test.

A 3�3 mixed-model ANOVAwas used to determine thePPT variables (M1, M2, T1, T2, suboccipital, C5, trapezius);the factors were group (treatment or sham), time (pre, post 1,and post 2) and side (right and left). Bonferroni correctionswere used for post hoc analysis of specific comparisons be-tween variables. Student t test determined the percent changebetween groups between the first session (pretreatment) andlast session (posttreatment 2) outcomes. Throughout allanalyses, statistical significance was set at P<0.05.

RESULTSThirty-two patients (21 females and 11 males) with

CCFP of myofascial origin were included in this study. Nopatients dropped out during the study, and no adverseevents occurred with the APUCM. The t test did not revealany significant differences between groups with regard todemographic details and clinical data (P>0.05), as shownin Table 1. A normal distribution was confirmed with theKolmogorov-Smirnov test (P>0.05).

Pain IntensityThe ANOVA revealed a significant group�time inter-

action (F=135.81; P<0.001), and significant differencesfor the time factor (F=261.7; P<0.001) and group factor(F=32.59; P=0.003) regarding the VAS results. Post hocanalysis also revealed significant differences for the treatmentgroup (P<0.001), but not for the sham group (P=0.3) forthe descriptive data shown in Table 2. A 2-way repeated-measures ANOVA found significant intersession differences(F=11.86; P<0.001) and a group� intersession interaction(F=17.09; P<0.001), indicating that the change fromsession to session was larger for 1 group.

Regarding the percentage of change, a 2-way repeated-measures ANOVA revealed significant differences for groupfactor (F=94.24; P<0.001) and time factor (F=11.3;P<0.001), represented in Figure 1A. The t test also re-vealed significant differences between the percent change ofthe total of the means for the treatment and sham groups(t= �10.03; P<0.001).

Pain Sensitivity

Craniofacial RegionAnalysis of the PPT within the craniofacial region was

performed by a 3�3 mixed-model ANOVA, which revealeda significant effect of time factor [M1 (F=83.65; P<0.001);M2 (F=67.44; P<0.001); T1 (F=98.05; P<0.001); T2(F=18.81; P<0.001)], group factor [M1 (F=12.27; P=0.001); M2 (F=18.35; P<0.001); T1 (F=16; P<0.001);T2 (F=15.85; P<0.001)] and group� time interaction [M1(F=59.65; P<0.001); M2 (F=48.45; P<0.001); T1

TABLE 1. Descriptive Data of the 2 Intervention Groups: Treatment and Sham Groups

Treatment (N=16) Sham (N=16)

Mean SD Mean SD Mean Difference

95% CI for

Mean Difference t P

Age 33.19 9.49 34.56 7.84 �1.37 �7.64 to 4.68 �0.48 0.65NDI 15.69 3.26 16.75 3.94 �1.06 �3.67 to 1.54 �0.83 0.41Pain duration 11.31 6.74 10.69 5.79 0.62 �5.16 to 3.91 �0.28 0.78BDI 13.63 3.64 12.38 4.41 1.25 �2.67 to 3.17 �0.17 0.86STAI 25.75 5.63 24.75 4.66 1 �2.73 to 4.73 �0.54 0.58

BDI indicates Beck Depression Inventory; CI, confidence interval; NDI, Neck Disability Index; STAI, State-Trait Anxiety Inventory; t, t test value.

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F=83.57; P<0.001); T2 (F=16.48; P<0.001)], but notfor side factor [M1 (F=0.94; P=0.76); M2 (F=0.13;P=0.72); T1 (F=0.009; P=0.92); T2 (F=0.64; P=0.43)]. Post hoc testing revealed significant differences be-tween the 3 sessions for the treatment group (P<0.001) butnot for the sham group (P>0.05) at all craniofacial points;descriptive data are shown in Table 3.

The t test revealed significant differences in the percentchange in PPT at the right and left craniofacial points. Figure 2shows the percent change in PPT from the pretreatment andfinal posttreatment assessment.

Cervical RegionA 3�3 mixed-model ANOVA revealed a significant

time effect of the suboccipital musculature (F=96.33; P<0.001), C5 zygapophyseal joint (F=52.37; P<0.001),trapezius muscle (F=57.41; P<0.001), and a group�timeinteraction at the suboccipital region (F=64.12; P<0.001),C5 zygapophyseal joint (F=46.84; P<0.001), and tra-pezius muscle (F=65.3; P<0.001). However, this was notthe case for side factor [suboccipital muscles (F=1.22; P=0.27); C5 zygapophyseal joint (F=1.8; P=0.18); trapeziusmuscle (F=1.57; P=0.22)]. Post hoc analysis revealedsignificant differences in the PPT for the 3 sessions of thetreatment group (P<0.001), but not the sham group(P>0.05), at each cervical point. Descriptive data of PPTfor the cervical region are shown in Table 3.

The t test revealed significant differences in the percentchange in PPT in the right and left cervical points for thetreatment group. Figure 3 shows the percent change in PPTof these measurements from pretreatment and final post-treatment points.

SNS

Skin ConductanceThe ANOVA revealed a significant group�time in-

teraction (F=107.55; P<0.001), an effect of time (F=118; P<0.001), and an effect of group (F=10.45; P=0.003) for changes in SC. Post hoc analysis revealed sig-nificant differences in the treatment group (P<0.001), but

not the sham group (P=0.73). The descriptive data of theSC are shown in Table 2. A 1-way repeated-measuresANOVA found no significant intersession differences (F=0.001; P=0.97) or group by intersession interaction (F=0.32; P=0.57).

ANOVA revealed significant differences in the percentchange between treatment sessions for the group factor(F=31.02; P<0.001), but not the time factor (F=0.72;P=0.48), as shown in Figure 4A. The t test revealed sig-nificant differences between percent change of the totalof the means of treatment and sham groups (t=6.11;P<0.001).

Breathing RateANOVA revealed a significant group�time interaction

(F=8.91; P=0.006) and a main effect of group (F=4.36;P=0.045), but not time (F=0.22; P=0.63), for changesin BR. Post hoc analysis revealed significant differences forthe treatment group (P=0.02), but not the sham group(P=0.08). The descriptive data of the BR are shownin Table 2. A 1-way repeated-measures ANOVA found nosignificant differences for intersession (F=0.13; P=0.87)or for group� intersession interaction (F=0.29; P=0.74).

TABLE 2. Descriptive Statistics for Sympathetic Nervous System Parameters and Pain Intensity, for Pretreatment and PosttreatmentAssessments

Mean±SD

Session 1 Session 2 Session 3

Pre Post Pre Post Pre Post

SCTreatment 1.84±0.61 3.33±0.43 2.10±0.78 3.45±0.38 1.88±0.59 3.4±0.53Sham 2.2±0.58 2.25±0.61 2.21±0.61 2.27±0.55 2.15±0.58 2.20±0.57

HRTreatment 69.56±6.3 73.16±5 71.25±4.39 75.1±2.88 72.05±6.84 77.12±4.12Sham 67.87±7.35 63.81±7.56 67.31±6 63.31±6.73 69.37±5.09 66.12±7.01

RRTreatment 15.31±2.76 16.31±4.13 15.63±1.9 18.38±3.7 15.88±2.56 16.7±3.6Sham 16.58±2.37 14.9±2.99 15.38±1.4 14.28±2.7 15.45±2.2 13.95±2.6

STTreatment 31.45±3.45 28.42±4.39 32.44±3.21 27.53±5.1 30.46±3.67 27.18±4.33Sham 31.71±3.19 29.11±4.07 32.03±2.7 29.56±3.76 31.06±3.26 28.57±3.61

VASTreatment 43.88±7.3 29.66±8.97 31.06±8.83 18.31±9.18 29.31±11.8 14.75±11.8Sham 42.38±9.41 41.5±7.9 45.13±7.9 42.56±6.88 44.31±8.51 42±9.05

BR indicates breathing rate; HR, heart rate; SC, skin conductance; ST, skin temperature; VAS, visual analog scale.

0

10

-20

-10

Treatment

-50

-40

-30

Ch

ang

e in

VA

S (

%)

Sham

-70

-60

-80Session 1 Session 2 Session 3

FIGURE 1. Visual analog scale (VAS) percentage change betweenthe 3 sessions (mean of preintervention and postintervention) fortreatment and sham groups.

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A 1-way ANOVA revealed significant differences inpercent change of BR for the group factor (F=11.34;P=0.002) but not for time (F=1.03; P=0.36) as shownin Figure 4B. The t test revealed significant differences be-tween the percent change of the total of the means for thetreatment and sham groups (t=3.07; P=0.004).

Heart RateANOVA revealed a significant group� time inter-

action (F=54.14; P<0.001) and a main effect of group(F=19.4; P<0.001), but not time (F=0.14; P=0.71),for changes in HR. Post hoc analysis revealed significantdifferences in the treatment group (P<0.001) and the shamgroup (P<0.001); HR data are shown in Table 2. A 1-wayrepeated-measures ANOVA found no significant inter-session differences (F=1.5; P=0.23) or group� interses-sion interaction (F=0.45; P=0.63).

Regarding the percent change in HR, a 1-way re-peated-measures ANOVA revealed significant differencesfor group factor (F=53.66; P<0.001), but not time factor

(F=1.02; P=0.36), as shown in Figure 4C. Significantdifferences between the percent change of the total of themeans for the treatment and sham groups (t=7.37; P<0.001) were observed.

Skin TemperatureThe ANOVA did not reveal any significant group�

time interaction (F=3.49; P=0.071), time factor effect(F=1.62; P=0.2), or group factor effect (F=0.53; P=0.46) for changes in ST. The descriptive data of the ST areshown in Table 2. A 1-way repeated-measures ANOVAfound no significant intersession differences (F=2.84;P=0.06) or group� intersession interaction (F=0.25;P=0.77).

Regarding percent change in ST, a 1-way repeated-measures ANOVA did not reveal a significant difference ingroup factor (F=3.25; P=0.08) or time factor (F=2.74; P=0.07), as shown in Figure 4D. The t test did notreveal a significant difference in the percent change of the

TABLE 3. Descriptive Statistics of PPT Assessed Pretreatment, Posttreatment 1 After the Second Session, and Posttreatment 2 After theThird Session, Taken Bilaterally

Treatment Sham

Right Left Right Left

Pre Post 1 Post 2 Pre Post 1 Post 2 Pre Post 1 Post 2 Pre Post 1 Post 2

Orofacial region

M1 2.13±0.37 3.03±0.5 3.46±0.45 2.12±0.43 2.91±0.53 3.5±0.44 2.29±0.54 2.32±0.48 2.39±0.55 2.28±0.37 2.31±0.62 2.42±0.6

M2 2.12±0.44 2.88±0.44 3.4±0.38 2.09±0.39 2.94±0.36 3.59±0.45 2.18±0.49 2.27±0.56 2.37±0.63 2.12±0.61 2.21±0.45 2.15±0.66

T1 2.76±0.49 3.52±0.5 4.11±0.55 2.69±0.5 3.66±0.54 4.19±0.53 2.81±0.47 2.85±0.46 2.97±0.32 2.89±0.51 2.78±0.57 2.82±0.59

T2 2.97±0.48 3.59±0.51 3.95±0.58 2.8±0.56 3.77±0.47 3.98±0.66 3.04±0.46 2.91±0.61 3.06±0.55 2.86±0.58 2.9±0.46 2.97±0.46

Cervical region

Suboccipital 2.36±0.34 3.33±0.29 3.95±0.22 2.28±0.35 3.38±0.32 3.99±0.22 2.31±0.44 2.43±0.52 2.48±0.63 2.25±0.39 2.35±0.49 2.41±0.54

C5 2.47±0.42 3.09±0.65 3.63±0.52 2.46±0.45 3.26±0.69 3.69±0.49 2.52±0.44 2.55±0.38 2.6±0.4 2.64±0.44 2.74±0.61 2.63±0.43

Trapezius 2.61±0.38 3.51±0.42 4.13±0.67 2.66±0.37 3.62±0.41 4.24±0.5 2.85±0.29 2.82±0.44 2.87±043 2.69±0.4 2.53±0.56 2.6±0.58

Mean±SD.PPT indicates pressure pain thresholds.

100.00

120.00 Treatment/Right SideTreatment/Left SideSham/Right SideSham/Left Side

60.00

80.00

40.00

0.00

20.00

Ch

ang

e in

PP

T (

%)

M1 M2 T1 T2

-20.00

FIGURE 2. Percent change in pressure pain thresholds (PPTs) ofthe craniofacial region (M1 and M2 points of masseter muscleand T1 and T2 of temporal muscle) for treatment and sham in-terventions at right and left sides (mean of preintervention andfinal postintervention). Error bars represent 95% confidence in-tervals of the mean.

Treatment/Right SideTreatment/Left SideSham/Right SideSham/Left Side

Ch

ang

e in

PP

T (

%)

120.00

80.00

100.00

60.00

40.00

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-20.00

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FIGURE 3. Percent change in pressure pain thresholds (PPTs) ofthe cervical region (suboccipital muscles, C5, and trapeziusmuscles) for treatment and sham interventions on the right andleft sides (mean of preintervention and final postintervention).Error bars represent 95% confidence intervals of the mean.

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total of the means for the treatment and sham groups(t= �1.82; P=0.079).

DISCUSSIONOur findings demonstrate that the APUCM technique

applied at a rate of 0.5Hz significantly increased SNS ac-tivity and produced short-term hypoalgesic effects. We arenot aware of any previous studies that have measured hy-poalgesic effects in the cervical and craniofacial regionsusing APUCM. We therefore contend that this is the firsttime that this specific manual mobilization technique ap-plied at the aforementioned frequency has been investigated,and our data indicate significant differences between theexperimental and control groups.

An increase in PPT was observed after the second in-tervention compared with the presession data and after thethird intervention compared with the first posttreatment as-sessment, which is indicative of a maintained increase overthe successive sessions. With regard to pain intensity, it isimportant to note the decrease in the VAS after each ses-sion, which was maintained from one session to the next andindicates a 41.7% decrease in pain intensity from the 3 ap-plications. A change in the SNS, as evidenced by changes inSC, BR, and HR, was noted after each session, but this trendreversed and was not maintained from one session to the next.Upon comparing the first, second, and third pretreatment

outcomes, it was apparent that the SNS values returned toa normal state of SNS activity. We suggest that the effectproduced by the technique could be due to the influence oftransient sympathoexcitation on pain mechanisms. Our con-tention is that the physiological effects produced by theAPUCM technique influence the suboccipital posterior sym-pathetic network and TCC and act to inhibit or gate my-ofascial pain within the cervico-craniofacial region.

Clinical EffectivenessThe results of clinical pain intensity measured by the

VAS indicate a decrease in the patients’ experience of painat rest with significant differences between treatment andsham groups. Patients who received the intervention re-ported a decrease of 29.13mm in VAS between the pre-treatment and third posttreatment assessment. Todd et al35

have stated that a minimal clinically significant change inVAS may be at least �13mm, whereas more recently, Birdand Dickson36 have contended that a clinically significantVAS change depends on the baseline VAS of the participantand that a change of �13mm would be clinically significantfor a baseline VAS<34mm, a change of �17mm for abaseline VAS between 34 and 67mm, and a change of�28mm for a baseline VAS>67mm. The more specificguidelines of Bird and Dickson are supported by Emshoffand colleagues in a study of chronic TMD pain patients.

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FIGURE 4. Percent change between the 3 sessions (mean of preintervention and postintervention) for treatment and sham groups. A,skin conductance; (B) heart rate; (C) breathing rate; (D) skin temperature.

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They established that to be clinically significant, patientswith a higher pain baseline must demonstrate a greater VASreduction than those with a lower baseline, and the minimalchange should be of �19.5mm or �37.9% of the VAS.37

Our findings are clinically significant according to theguidelines of Todd et al, Bird and Dickson, or Emshoffet al.35–37

SNS ResponsePrevious studies have noted similar effects in the variables

that we measured after SMT in the cervical region.15,17,19,20,38

We observed an increase of 83.75% in SC, which is similar tothat observed by Chiu and Wright19 and Sterling et al15 whoobserved increases of approximately 50% to 60% and 16%,respectively. Studies in which SMT was applied to other bodylocations also noted similar changes in SC. A 16.85% increasein SC was observed after a thoracic mobilization applied toT4,39 and a 13.5% increase in SC was observed after lumbarmobilization.40

A similar effect was noted for HR. We observed an in-crease of 6.06% compared with previous studies that reportedchanges of 10.5%,38 13%,20 and 4.5%.17 A significant changein HR in the sham group was also noted. HR decreased by�5.5% in the sham group, which could indicate that thetreatment can increase HR, whereas the sham application issimilar to a touch massage technique that results in a decreaseof SNS activity.41

Previous studies of BR have reported increases of44%38 and 36%.20 In our study, we observed a 10.4% in-crease in BR in the experimental group. This discrepancycould be due to the type of mobilization that we applied.Previous studies that used lateral cervical glides or poste-rior-anterior mobilization techniques at a frequency of2Hz. A significant change was not obtained in ST despitea downward trend in both treatment and sham groups, asnoted by Chiu and Wright.19 However, a significant de-crease of 2.5% in ST was obtained in another study.15

The results of Sterling et al15 correlate with our datawith respect to the tendency of ST to decrease and the notedchange in SC. Furthermore, significant changes in bloodpressure, which we did not record, have been observed byPaungmali et al,17 Vicenzino et al,20 and McGuiness et al.38

These results confirm that gentle manual mobilizationtechniques on the cervical spine can confer positive phys-iological effects.

Hypoalgesic EffectsOur data indicate that the APUCM technique pro-

duces hypoalgesic effects, as demonstrated by PTT meas-urements made by an algometer, and support a significantdifference between the treatment and sham groups. Sterlinget al15 demonstrated that a unilateral posterior-anteriormobilization applied on the side of pain increased the PPTby 23% on the side of treatment in patients with chronicidiopathic neck pain. We observed increases in PPTbetween 64% and 77% for the masseter muscle points,between 38% and 59% at temporal muscle points and be-tween 47% and 79% for the cervical points after 3 treat-ments of APUCM. The greater change in PPT observed inour study and others may be because our study investigatedshort-term outcomes (3 treatment sessions) instead of im-mediate outcomes (1 treatment session), due to the appliedtechnique and the frequency of mobilization and is in-dicative of a real bilateral hypoalgesic effect at both regions.

Previous research has investigated the effect of spinalmobilization on cervical and lumbar regions and reportedpositive results.15,20,40,42 Sterling et al15 noted a differencebetween the improved PPT in the painful side and thenonpainful side, indicating a unilateral effect from a uni-lateral technique. Our study demonstrates a bilateral in-crease in PPT in both cervical and craniofacial regions. Thisdifference could be due to the central application of thetechnique in this study as opposed to the unilateral appli-cation of Sterling et al.

Manual Therapeutic NeurophysiologyResearch in SMT has focused on the neurophysio-

logical effects of manual manipulation and mobilizationswith data suggesting activation of descendent pain inhibitorysystems upon short-term (initial) hypoalgesic effects.43–45

Skyba et al46 showed that mobilization of the hyperalgesicknee joint in rats produced an antihyperalgesic effect. Thiseffect, which maintained after spinal blockage of opioid orGABA receptors, could be due to descending serotoninergicor noradrenergic inhibitory mechanisms via corticospinalprojections from the periacueductal gray matter (PAG).46

Implications relate to noradrenaline, a PGA neurotransmitterthat is more effective at inhibiting mechanical nociceptionthan thermal nociception, which seems to be serotoninergi-cally mediated.47,48 Others have demonstrated that SMTmight be the ideal stimulus for PAG mediated nonopioidanalgesia, hypoalgesia, sympathoexcitatory effects, and changesin motor activity.15,17,20,49 In the present study, we obtainedboth a sympathoexcitation and hypoalgesic effect after theAPUCM technique, which supports the fact that the d-PAG isinfluenced by the SMT technique.

One controversial issue surrounding manual therapy iswhether a localized segmental and/or extrasegmental effectis produced by SMT. Previous research has shown thatSMT improves symptoms distal to the segment where it isapplied; that is, manipulation applied at the thoracic spinehas positive effects when performed on patients with frommechanical neck pain,14,21 and cervical SMT can result inhypoalgesia at the elbow.50 However, other clinical studieshave shown only segmental effects causing diminished neckpain and PPT after ipsilateral cervical mobilization.15,16

We applied a mobilization technique at the upper cer-vical spine and observed changes in the craniofacial andcervical region as well as hypoalgesic effects further awayfrom the segment to which it was applied, suggesting thatmanual therapy has a general central or at least supra-medullar effect. A physiological or sympathoexcitatoryeffect has also been demonstrated in the upper extremityafter cervical or thoracic SMT,15,39 and in the lower ex-tremities after lumbar mobilization.40

It is clear that SMT activates central structures that con-currently activate sympathoexcitatory and hypoalgesic effectsas demonstrated in our research and in that of others.15,20 Thepresence of an extrasegmental effect may indicate activation ofthe d-PAG and could be mediated by various descending paininhibitory pathways and associated tracts of the TCC thatallow for afferent and efferent transmission between the cer-vical and craniofacial regions.51,52

Nociceptive Modulation and the TCCThe increase in PPT caused by the APUCM technique

on the craniofacial region provides additional clinical

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support for pain modulatory mechanisms in the TCC.A review performed in 1998 outlined neurophysiologicalcoupling between craniofacial and cervical systems.53

It has been observed that manual therapeutic applica-tions to the cervical region provoked a pain reducing effectin the head and face. Mellick and Mellick54 and Mellicket al55 observed that applying a bilateral intramuscular in-jection of small amounts of 0.5% bupivacaine at the cervicalregion caused a decrease in facial pain and headaches. Inaddition, Carlson et al56 demonstrated that an infiltration of2% lidocaine on an active TrP of the trapezius muscle sig-nificantly reduced pain and electromyographical activity ofthe ipsilateral masseter.

The only previous study of manual interventions to thecervical spine to manage craniofacial pain was performedby La Touche et al. This study reported similar results toour study: improved PPT at the masseter and temporalismuscles after a manual therapy protocol directed to thecervical spine combined with a deep neck flexors train-ing program.23

Convergence pathways between cervical and trigemi-nal sensory afferents in the TCC are fully supported.52,57,58

Stimulation of an upper cervical root, such as manipulationof the greater occipital nerve has produced changes in theTCC neurons. This supports the concept that perception ofcranial pain is due to a functional convergence betweentrigeminal and cervical fibers in the TCC59,60 and provides apotential rationale for the relationship between headachesand arm and trunk pain.61

Direct stimulation of the greater occipital nerve (cer-vical input) increases metabolic activity of the TCC62 andtrigeminal nociceptors release neuropeptides, such as sub-stance P, from laminas I and II that diffuse to laminas III toV depending on the intensity of the stimulus.63 The TCCitself is formed by the upper cervical dorsal horns and thetrigeminal nucleus caudalis, which allows nociceptive inputto be transmitted from the TCC to higher centers.64 Painmodulatory structures such as the PAG, dorsolateral pon-tomesencephalic tegmentum, and rostral ventromedial me-dulla control the TCC-mediated generation of antinociceptiveor pronociceptive states.57,58,65

In summary, we propose a neurobiomechanical hypo-thesis to explain the possible mechanism by which a manualtherapeutic technique causes a hypoalgesic effect in cranio-facial and cervical regions. This technique primarily influen-ces the upper cervical region (C1-C3), which is anatomicallyrelated to the occipital bone. We believe that an anterior-posterior glide of the upper cervical structures provokes animproved arthrokinematic relationship of the target regionthereby generating improved pain-free range of movementand concomitant suboccipital muscle relaxation. A secondaryeffect might reduce mechanical forces on the upper cervicalneurovascular structures, thereby interrupting or inhibitinginput and reducing TCC sensitization by activating de-scendent pain inhibitory systems.

In addition, the TCC is the main nucleus that receivesnociceptive information from the face, head, and neck.66

Neurons inside the nuclei are considered multimodal neu-rons and can receive 2 or more inputs from different ori-gins, such as cervical nerve roots, when manual therapy isbeing applied. The input generated from the cervical regioncan alter the nociceptive processing in the TCC and, as aresult, produce a hypoalgesic effect at the facial region.Finally, another possible mechanism to explain the effect ofour manual intervention is that descending pain inhibitory

systems can be activated by SMT on the cervical spine byspinal noradrenergic and serotoninergic pathways from thedorsolateral pons and rostral ventral medulla.45,46

Study LimitationsAlthough the results of our research are positive, we

only measured short-term changes without follow-up testing.We only measured SC and ST on the right side. Other studiesinvestigating sympathetic activation after SMT treatmentonly measured one side of the body, usually the treated side.Perry and colleagues applied a unilateral lumbar mobilizationand measured sympathetic activity at both lower extremities.They only observed significant activation in the treated sidebut did observe a tendency toward sympathetic activation inthe untreated side.40 It would have been interesting to observeif central mobilization activates SNS with the same intensityin both upper extremities and if it has any effect on lowerextremities. It also could have been interesting to measure SCand ST directly on the facial region. We did not measure distalPPT; therefore, due to a lack of information, we cannot pro-vide a complete discussion about the general or segmental ef-fect of the APUCM technique.

This is the first time this type of mobilization at afrequency of 0.5Hz has been used in a clinical randomized-controlled trial. Because different techniques require differ-ent frequencies of application to provoke stronger changes,it would be of interest to test the same mobilization at dif-ferent frequencies of application.

Clinical ImplicationsWe have demonstrated that craniofacial pain can be

modulated through an upper cervical treatment (mobilization).The presence of craniofacial pain is a predictor factor for neckpain.9,67 It is interesting to treat this type of patient with atechnique that has proven effects at the craniofacial segmentthat can also treat a possible neck dysfunction. This techniquemight be contraindicated in patients with craniocervical hy-permobility syndrome due to the movement the APUCMprovokes at the upper cervical spine and the risk this entails.68

Chronic pain can be maintained by SNS modulationthrough the peripheric adrenorreceptor excitation of cat-echolamine.69 Chronic TMD patients seem to present adysregulation of b-adrenergic activity, which contributes toaltered cardiovascular and catecholamine responses.70 Thedysregulation of SNS can contribute to the severity andmaintenance of pain. The influence of APUCM on SNSactivity makes this technique an interesting tool to treatpatients with CCFP of myofascial origin and patients withfacial allodynia, in which other techniques applied directlyon the face would be contraindicated.

CONCLUSIONSWe demonstrate that APUCM reduces pain intensity

and increases PPT in the cervical and craniofacial regions.APUCM also causes sympathoexcitation, which confirms asympathetic effect. These results indicate an influence of themobilization on the CNS (medullar or supramedullar effect).This study provides preliminary evidence of the short-termhypoalgesic effect on the craniofacial and cervical regions ofpatients with CCFP of myofascial origin, suggesting thatAPUCM may cause an immediate nocioceptive modulationat the TTC.

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205

DISCUSIÓN

206

6. DISCUSIÓN

Los hallazgos mostrados en esta tesis coinciden con una gran cantidad de estudios

recientes publicados en las últimas dos décadas. En estas investigaciones de carácter

básico y clínico se ha comprobado como las estructuras cervicales pueden influir sobre

características sensoriales y motoras de la regiones craneofacial y craneomandibular y

viceversa (Armijo-Olivo and Magee, 2007, 2013; Dessem and Luo, 1999; Eriksson et

al., 2004, 2007; Ge et al., 2004; Giannakopoulos, Hellmann, et al., 2013;

Giannakopoulos, Schindler, et al., 2013; Häggman-Henrikson and Eriksson, 2004;

Häggman-Henrikson et al., 2013; Haggman-Henrikson et al., 2004; Hellmann et al.,

2012; Hellström et al., 2002; Hu et al., 2005; Olivo et al., 2010; Svensson et al., 2005;

Torisu et al., 2014). La investigación básica en torno a la neurofisiología del CTC ha

servido para establecer hipótesis y teorías relacionadas con los mecanismos

nociceptivos periféricos y centrales implicados en (Bartsch and Goadsby, 2002, 2003a;

Bereiter et al., 2005; Chiang et al., 1998, 2005; Hu et al., 1993; Lam et al., 2009; Salter,

2004; Sessle et al., 1986; Yu et al., 1995): 1) las comorbilidades entre las dolencias

cervicales y craneofaciales; 2) en la concomitancia motora entre la región

craneomadibular y craneocervical; 3) en las respuestas motoras alteradas; y 4) en las

posibles intervenciones terapéuticas sobre la región cervical que pudieran influir sobre

la región craneofacial. Los resultados de las investigaciones presentadas en esta tesis

ofrecen algunos hallazgos importantes que fortalecen la investigación previa en relación

con esto cuatro puntos. A continuación se discute en profundidad los resultados

obtenidos según los objetivos planteados en la tesis.

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6.1 Diferencias de Género en la Variables Somatosensoriales.

En el análisis del efecto del género sobre variables somatosensoriales en pacientes con

DCCF hay que partir de una premisa epidemiológica y es que como está representado

en nuestros estudios, la prevalencia de estas dolencias es mayor en la población

femenina (Adèrn et al., 2014; Carlsson, 1999; LeResche, 1997; Macfarlane, Blinkhorn,

Davies, Kincey, et al., 2002). Hemos encontrado en el estudio III (La Touche et al.,

2010) y en el estudio V (La Touche, Paris-Alemany, et al., 2014) influencias del género

sobre variables somatosensoriales.

En relación al estudio V (La Touche, Paris-Alemany, et al., 2014) los resultados

mostraron que la percepción del dolor y la fatiga durante el test masticatorio de

provocación estuvo influenciada por el género en los tres grupos evaluados, se observó

que las mujeres presentan una mayor percepción de intensidad de dolor y fatiga

masticatoria, estos resultados coinciden con estudios previos de dolor inducido

experimentalmente realizados con pacientes (Haggman-Henrikson et al., 2004) y

sujetos sanos (Karibe et al., 2003; Plesh et al., 1998), sin embargo es importante

mencionar que otras investigaciones no han observado la interacción del factor genero

sobre el dolor o la fatiga masticatoria inducida experimentalmente (Koutris et al., 2013;

van Selms et al., 2005). El estudio V no está diseñado con el objetivo de identificar los

mecanismos fisiológicos o psicológicos que puedan explicar las diferencias en los

resultados entre mujeres y hombres, sin embargo es importante destacar que la

evidencia de estudios experimentales relacionados con dolor inducido indica que las

mujeres presentan mayor sensibilidad al dolor que los hombres en diferentes pruebas

somatosensoriales (Fillingim et al., 2009). Finalmente destacar que en el estudio III (La

Touche et al., 2010), solo se identificó una interacción con el género en los UDPS del

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músculo tibial anterior, mostrando unos valores significativamente menores en mujeres

respecto a la población masculina del estudio.

6.2 Postura Craneocervical, Dinámica Mandibular y Dolor Craneofacial.

Dos investigaciones (I, (La Touche et al., 2011) y II (Lopez-de-Uralde-Villanueva et

al., 2014) de esta tesis han estudiado la influencia de la postura craneocervical sobre la

función mandibular y las posibles interacciones con mecanismos nociceptivos

trigeminales. Los resultados demuestran que las posturas craneocervicales inducidas

experimentalmente producen modificaciones en MAI presentándose menor o mayor

rango articular según la postura en que se realice el gesto (La Touche et al., 2011), estos

hallazgos también fueron comprobados por Higbie y cols. en 1999 (Higbie et al., 1999).

Además, evidencia previa refuerza estos hallazgos, ya que se han descrito las

modificaciones intra-articulares que se producen en ATM con diferentes posturas

craneocervicales o movimientos cervicales (Ohmure et al., 2008; Solow and Tallgren,

1976; Visscher et al., 2000).

Otro resultado que consideramos relevante en el estudio I, fue que los UDPS de áreas

trigeminales se vieron modificados según las diferentes posturas craneocervicales

siendo el menor UDP registrado en la postura de protracción. Este resultado es difícil

discutirlo ya que no hay estudios similares en esta línea, nosotros plantemos

teóricamente que esto puede suceder debido a cambios o ajustes que realiza el sistema

nervioso bajo diferentes condiciones del entorno y demandas de la región cervical,

creemos que estos ajustes se producen en mecanismos sensoriales pero también en los

motores. En relación a esto, debemos mencionar que contamos con evidencia previa que

describe que los movimientos cervicales o las posturas craneocervicales inducidas

experimentalmente modifican la actividad de la musculatura masticatoria

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incrementándola (Ballenberger et al., 2012; Forsberg et al., 1985; McLean, 2005;

Ohmure et al., 2008).

En el estudio II (Lopez-de-Uralde-Villanueva et al., 2014) se encontraron diferencias en

la postura craneocervical medido con dos instrumentos entre el grupo de pacientes con

DCCF y los sujetos asintomáticos, sin embargo es fundamental tener en cuenta que esos

cambios fueron muy pequeños y en una de la mediciones no superó el MCD y en la otra

los superó pero por muy poco, estos resultados se han encontrado prácticamente con las

mismas similitudes en investigaciones realizadas en pacientes con dolor de cuello

(Silva et al., 2009) y con TCM (Armijo-Olivo et al., 2011) comparada con sujetos

asintomáticos. Por otra parte, cabe mencionar que no se encontró asociación entre la

postura craneocervical con las variables de discapacidad cervical y craneofacial, datos

de otras investigaciones apoyan este resultado (Armijo-Olivo et al., 2011; Cheung et al.,

2010) aunque otros lo contradicen (Lau et al., 2010). La relación entre la postura y los

TCM es controvertida y no está clara según datos extraídos de dos revisiones

sistemáticas recientes (Armijo Olivo et al., 2006; Rocha et al., 2013), además ambas

revisiones coinciden en recalcar que los estudios analizados en relación a esta temática

presentan serias dificultades metodológicas y complica la posibilidad de extraer

conclusiones.

6.3 Influencia del Dolor y la Discapacidad Cervical sobre la Actividad

Sensoriomotora Trigeminal.

En los estudios III (La Touche et al., 2010) y V (La Touche, Paris-Alemany, et al.,

2014) se han obtenido resultados importantes entorno a la influencia del dolor y la

discapacidad de cuello sobre la región craneofacial, específicamente en el estudio V

hemos identificado que los pacientes con moderada y leve discapacidad cervical

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presentan mayores niveles de percepción de dolor y fatiga frente a los sujetos sanos

sometidos al test de provocación masticatorio, es importante mencionar que entre los

grupos de pacientes, el de moderada discapacidad cervical fue el que presentó mayores

cambios en las variables sensoriales medidas durante el test, inmediatamente después y

las 24 horas, La única excepción de esto ha sido en el resultado de la percepción de

intensidad dolor a las 24 horas en que entre ambos grupos no se presentaron diferencias

estadísticamente significativas. A pesar de que existen muchos estudios que utilizan los

test provocación masticatorias para inducir dolor y fatiga (Christensen et al., 1996; Dao

et al., 1994; Farella et al., 2001; Gavish et al., 2002; Karibe et al., 2003; Koutris et al.,

2009; Plesh et al., 1998), solo hemos encontrado un estudio similar al nuestro (estudio

V), (La Touche, Paris-Alemany, et al., 2014), en este Haggman-Henrikson y cols.

(Haggman-Henrikson et al., 2004) observaron que los pacientes con latigazo cervical

presentaron mayores niveles de dolor y fatiga masticatoria inducida por el test que los

pacientes con TCM y sujetos asintomáticos. Diversos estudios experimentales y clínicos

han descrito conexiones funcionales entre las regiones craniofacial y cervical a través de

patrones de convergencia neural en el CTC (Dessem and Luo, 1999; Ge et al., 2004;

Hellström et al., 2002; Hu et al., 2005; Svensson et al., 2005; Torisu et al., 2013; Wang

et al., 2004), en relación con esto se ha observado en estudios experimentales que el

dolor inducido por la infiltración de sustancias algógenas en músculos masticatorios o

cervicales modifican de forma bidireccional la actividad de los reflejos de estiramiento

(Ge et al., 2004; Wang et al., 2004) además, en investigaciones básicas con animales se

ha observado una relación refleja entre la actividad de los nociceptores de la ATM y

actividad del sistema fusimotor de los músculos de cuello (Hellström et al., 2002), esta

información es útil para plantear teorías acerca de la influencia de la región cervical

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sobre los posibles mecanismos nociceptivos (sensoriales) y motores implicados en el

dolor y la fatiga masticatoria.

Contamos con evidencia científica reciente que demuestra que lesiones sobre la región

cervical pueden alterar el control motor masticatorio y la función mandibular normal de

apertura-cierre (Eriksson et al., 2004, 2007; Zafar et al., 2006), los hallazgos de estudio

V se pueden relacionar con esta cuestión ya que nuestros resultados muestran que el test

de provocación masticatorio reduce la MAI libre de dolor al finalizar el test en los tres

grupos, este resultados son similares a la de otros estudios (Karibe et al., 2003;

Svensson et al., 2001), sin embargo hay que tomar en cuenta que esta disminución fue

mayor en los grupos de pacientes y se mantuvo a las 24 horas únicamente en el grupo de

moderada discapacidad cervical, además es importante destacar que el análisis de

regresión mostró que la discapacidad cervical es un predictor de la MAI libre de dolor

(después de 24 horas) en los dos grupos de pacientes. Planteamos la teoría de que los

patrones motores masticatorios estén más alterados a medida que se tenga mayor dolor

o discapacidad cervical, esta situación generaría la activación de mecanismos

compensatorios des-adaptativos que alterarían la conducta, el reclutamiento y la

coordinación de los sistemas motores del cuello y la mandíbula generando mayores

niveles de fatiga y dolor durante los test de provocación y manteniendo estas

sensaciones 24 horas después. Esta misma teoría podría servir para explicar los

resultados de la disminución de los umbrales del dolor a la presión de regiones

trigeminales y cervicales, cabe destacar que los cambios UDPs fueron mayores en los

grupos de pacientes y que la mayoría de cambios en los UDPs de la región cervical a las

24 horas se produjeron en el grupo de moderada discapacidad cervical, como factor

coadyuvante a este situación hay que considerar que la presencia de dolor cuello puede

provocar menores valores de UDPs en puntos trigeminales en comparación con sujetos

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sanos como se observó en el estudio III (La Touche et al., 2010). Aunque consideramos

que puede haber una relación directa entre los cambios sensoriomotores trigeminales

con el dolor y la discapacidad cervical, también tenemos que tener en cuenta la

posibilidad de que en los pacientes los cambios se hubieran visto influenciados

mayoritariamente por la presencia de cambios neuroplásticos ya establecidos a nivel

central; se conoce actualmente que los pacientes con dolor crónico pueden tener mayor

susceptibilidad de presentar un proceso de sensibilización central (Henry et al., 2011),

Wolf y cols. sugieren que en condiciones dolorosas en donde existe una comorbilidad

como es el caso de la muestra de pacientes de este estudio, puede ser un factor

determinante en la pato-fisiología de la sensibilización central (Woolf, 2011). En

relación con esto, Gaff-Radford propone que en la sensibilización central se producen

cambios en las vías aferentes que hacen posible la comunicación de las neuronas

nociceptivas cervicales y orofaciales en el núcleo trigeminal (Graff-Radford, 2012). A

esto hay que añadir que son muchos los estudios que han encontrado en pacientes con

TCM mecanismos periféricos y centrales compatibles con un proceso de sensibilización

central (Anderson et al., 2011; Ayesh et al., 2007; Chaves et al., 2013; Feldreich et al.,

2012; Park et al., 2010; Raphael et al., 2009; Sarlani et al., 2004), sin embargo es

importante destacar que en el grupo de pacientes con dolor de cuello crónico mecánico

del estudio III solo se encontraron diferencias en UDPs en áreas trigeminales y

cervicales pero no en zonas distales, estos nos lleva a pensar que en este tipo de

pacientes hay una posible sensibilización central especifica del CTC.

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6.4. Asociación entre la Discapacidad Cervical y la Discapacidad

Craneofacial/craneomandibular.

En los estudios II (Lopez-de-Uralde-Villanueva et al., 2014) y IV (La Touche, Pardo-

Montero, et al., 2014) se demostró una correlación positiva fuerte-moderada entre la

discapacidad cervical y la discapacidad craneofacial (r=0,79 y r=0,65 respectivamente),

es posible que el resultado del estudio II fuese mejor por la especificidad de la muestra

de pacientes con DCCF seleccionados, hay que tomar en cuenta que la muestra del

estudio IV la conformaron pacientes con diversos tipos de DCF en donde posiblemente

la discapacidad y estatus funcional mandibular no tenga tanto peso, pero esta es una

suposición que se tendrá que comprobar futuras investigaciones. Los resultados de los

estudios II y IV son apoyados por la investigación de Olivo y cols., en esta se encontró

una correlación positiva muy fuerte entre las dos variables de discapacidad (r=0,82)

(Olivo et al., 2010).

6.5 Factores Bioconductuales Implicados en las Alteraciones Sensoriomotoras

Trigeminales y la Discapacidad Craneofacial.

En los estudios III (La Touche et al., 2010), IV (La Touche, Pardo-Montero, et al.,

2014) y V (La Touche, Paris-Alemany, et al., 2014) se utilizaron medidas de auto-

registro relacionadas con el dolor, la discapacidad y factores psicológicos para analizar

las posibles asociaciones con variables sensoriomotoras.

En el estudio V, el análisis de regresión lineal múltiple mostró que el catastrofismo del

dolor y el impacto de la cefalea sobre la calidad de vida (HIT-6) se asociaron a las

variables de percepción de dolor y fatiga 24 horas después de haber realizado el test de

provocación masticatoria. Específicamente en el estudio V el catastrofismo ante el dolor

fue un factor psicológico analizado y mostró ser un predictor de la fatiga a las 24 horas

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en el grupo de moderada discapacidad cervical y en el grupo de leve discapacidad

cervical también fue predictor para la fatiga y la intensidad de dolor percibido 24 horas

después del test provocación masticatorio. El catastrofismo ante dolor se define como

un factor cognitivo que implica una percepción mental negativa o exagerada de la

amenaza percibida tanto real como anticipada de la experiencia de dolor (Sullivan et al.,

2001; Turner and Aaron, 2001).

En cuanto a la fatiga percibida y el catastrofismo no encontramos estudios clínicos o

experimentales en los que hayan estudiado la asociación en pacientes con DCF o TCM,

pero si hemos encontrado dos estudios sobre la relación del catastrofismo del dolor con

variables cinemáticas masticatorias (Akhter et al., 2014; Brandini et al., 2011). En el

estudio realizado por Akhter y cols. se investigó el efecto de un dolor experimental

agudo en una muestra dividida en sujetos con poco catastrofismo y alto catastrofismo,

los resultados de esta investigación mostraron que la intensidad del dolor percibida fue

más alta en los sujetos con mayor catastrofismo y además en este mismo grupo se

observó una velocidad más lenta y mayor variabilidad en los movimientos mandibulares

repetidos, los autores de este estudio sugieren que los cambios en la coordinación

motora son un ejemplo de conducta de evitación que afectan la función del sistema

motor mandibular (Akhter et al., 2014). En la otra investigación, Brandini y cols.

estudiaron variables cinemáticas masticatorias durante un procedimiento de exposición

muy corto (15 segundos) en pacientes con TMC atribuidas a dolor miofascial, en este

estudio no se observaron asociaciones de las variables cinemáticas medidas con

respecto al catastrofismo, sin embargo hay que tomar en cuenta que el propósito del

estudio no era inducir dolor o fatiga para observar la respuesta como si lo hemos hecho

en el estudio V (La Touche, Pardo-Montero, et al., 2014).

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Se debe destacar que en una revisión sistemática muy reciente se concluye que hay una

asociación entre el catastrofismo y la fatiga y que el primero influye proporcionalmente

sobre la segunda y estos resultados se observaron en diversas poblaciones clínicas

(Lukkahatai and Saligan, 2013), también se ha demostrado que en otras dolencias

musculoesqueléticas el catastrofismo del dolor se vio asociado a alteraciones motoras

como la disminución del funcionamiento y rendimiento de las actividades de la vida

diaria y limitación de la capacidad para realizar ejercicio (Meeus et al., 2012; Nijs et al.,

2008, 2012). Además este constructo se ha asociado con una mayor utilización de los

servicios de salud, con la aparición de mayores hallazgos clínicos en la valoración, con

un estado de ánimo negativo (Turner et al., 2001; Turner, Brister, et al., 2005) y con

una alteración estatus funcional mandibular (La Touche, Pardo-Montero, et al., 2014)

como hemos comparado en el estudio IV.

En el estudio IV se evaluó la validez del constructo realizando un análisis de

correlaciones entre la discapacidad craneofacial medida con el IDD-CF con otras

medidas de auto-registro psicológicas y de discapacidad. Se observó una correlación

moderada entre IDD-CF con el HIT-6 y la EVA (r = 0,38 hasta 0,46). Además, ECD y

TSK-11 mostraron una correlación moderada con el IDD-CF y con la sub-escala de

dolor y la discapacidad (r = 0,36 hasta 0,52). Esto es coherente con los datos recientes

que demuestran que los pacientes con DCF y TCM reportaron mayores niveles de

catastrofismo (Campbell et al., 2010; Fillingim et al., 2011; Quartana et al., 2010).

Además el catastrofismo ante el dolor se ha asociado con la progresión hacia altos

niveles de intensidad del dolor y de discapacidad en pacientes con DCF crónica

(Buenaver et al., 2008, 2012; Holroyd et al., 2007; Rantala et al., 2003; Velly et al.,

2011).

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Evidencia previa ha demostrado la relación entre el miedo a los movimientos de la

mandíbula y el DCF (Rollman et al., 2012; Visscher et al., 2010), pero la evidencia

hasta el momento se consideraba limitada. Sin embargo, hay estudios que demuestran

que el miedo al dolor y al movimiento se asocia a una disminución de las actividades de

la vida diaria y también ha sido identificado como un fuerte predictor de discapacidad

en otros trastornos musculoesqueléticos crónicos (Buer and Linton, 2002; Crombez et

al., 1999; Kamper et al., 2012; Vlaeyen et al., 1999; Walton and Elliott, 2013). El

catastrofismo ante el dolor y el miedo relacionado con el dolor son dos constructos que

se han vinculado a la cronicidad del dolor musculoesquelético a través del "Modelo de

miedo-evitación" (Leeuw et al., 2007). En el estudio IV se realizó un análisis de

regresión lineal múltiple en donde se identificó que la intensidad del dolor (EVA: β =

0,19; P = 0,001) y el miedo al dolor y al movimiento (TSK-11: β = 0,17; P = 0,004)

fueron predictores del DCF. Para el estado funcional de la mandíbula y la discapacidad

craneofacial el predictor fue el catastrofismo del dolor (ECD-magnificación: β = 0,25; P

<0,001; β = 0,20; P = 0,007).

La relación entre los factores psicosociales, la actividad motora y el dolor parece estar

presente en diversos casos de dolor musculoesquelético, sin embargo la explicación para

la misma es compleja y limitada hasta el momento. Peck y cols. (Peck et al., 2008) y

Murray y Peck (Murray and Peck, 2007) han planteado una posible explicación y para

ello han generado un nuevo modelo explicativo denominado Modelo integrado de

adaptación al dolor (MIAD). Este modelo explica básicamente que la influencia del

dolor sobre la actividad motora depende de la interacción de las características

multidimensionales (biológicas y psicosociales) del dolor con el sistema sensoriomotor

de un individuo que termina generando una nueva estrategia de reclutamiento motor con

el objetivo de minimizar el dolor, sin embargo esta respuesta motora puede asociarse a

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la aparición de otra dolencia o al empeoramiento del dolor existente (Murray and Peck,

2007; Peck et al., 2008). Este modelo se apoya en el carácter multidimensional

(sensorial discriminativa, afectiva-emocional, cognitiva) que presenta la experiencia de

dolor y cómo este influye sobre el sistema sensoriomotor a través de las conexiones

periféricas y centrales que tiene este sistema con el sistema nervioso autónomo, el

sistema límbico y otros centros superiores (Craig, 2003; Peck et al., 2008).

Recientes estudios de neuroimagen han comprobado como el catastrofismo ante el dolor

(rumiación y desesperanza) puede influir sobre diversas áreas de la corteza cerebral en

pacientes con TCM (Kucyi et al., 2014; Salomons et al., 2012). Salomons y cols.

(Salomons et al., 2012) encontraron en pacientes con TCM una correlación entre la

desesperanza (sub-escala de la ECD) y el grosor cortical del área motora suplementaria

(AMS) y la corteza cingulada media (CCM), los autores de esa investigación sugieren

que la activación de esas áreas en los pacientes con TCM podrían tener una implicación

en aspectos cognitivos de la conducta motora incluyendo las alteraciones de la respuesta

motora, hay que tomar en cuenta que el AMS neurofisiologicamente está implicada en

la planificación del acto motor (Nachev et al., 2007, 2008) y el CCM se ha asociado con

la selección óptima de respuestas motoras en condiciones de incertidumbre (Shackman

et al., 2011). En relación a los pacientes con TCM que presentaron altos niveles de

rumiación (sub-escala de la ECD), Kucyi y cols. (Kucyi et al., 2014) encontraron una

correlación positiva de aumento de la conectividad funcional del córtex prefrontal

medial con la corteza cingulada posterior, el tálamo medial, la corteza retroespinal y la

sustancia gris periacueductal/periventricular, estos resultados indican que la rumiación

ante el dolor podría influir sobre áreas relacionadas con aspectos afectivos y

emocionales de la experiencia dolorosa y con áreas del sistema inhibitorio descendente

del dolor. Parece ser que los cambios funcionales o estructurales en áreas cerebrales no

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solo se presentan en pacientes catastrofistas con TCM, también en otro estudio de

neuroimagen, pero en este caso en pacientes con fibromialgia que presentaban

considerables niveles de catastrofismo, se observó un incremento de actividad en áreas

cerebrales relacionadas con la anticipación del dolor, la atención al dolor, aspectos

emocionales del dolor y el control motor (Gracely et al., 2004), similares resultados se

han encontrado en otras dolencias musculoesqueléticas (Brown et al., 2014).

En el estudio III (La Touche et al., 2010) no se encontraron asociaciones entre los UDPs

de áreas trigeminales o cervicales con las medidas de síntomas depresivos o de

ansiedad. Introducir en esta investigación la valoración de estos síntomas lo

consideramos de gran interés teniendo en cuenta que estos dos factores emocionales se

han relacionado con diferentes situaciones de dolor (Castillo et al., 2013; Roddy et al.,

2013; Simons et al., 2014), a pesar de esto no hemos encontrado ningún tipo de

asociación de los síntomas de ansiedad con otras variables relacionadas con el dolor y la

discapacidad de este estudio. En relación con los síntomas depresivos sí encontramos

una asociación positiva con la intensidad (rho=0,65; P= 0,001) y la cronicidad del dolor

(rho=0,54; P=0.004) y este es un hecho que es recogido por una amplia parte de la

literatura científica (Salama-Hanna and Chen, 2013; Yalcin and Barrot, 2014).

6.6 Efecto del Tratamiento en la Región Cervical sobre el Dolor Craneofacial.

Los resultados de los estudios VI y VII (La Touche et al., 2009, 2012) demuestran que

el tratamiento de fisioterapia en la región cervical produce cambios en los UDPs de

áreas trigeminales y además una disminución en la intensidad del dolor de forma

inmediata y a corto plazo (3 meses), este es un hallazgo que consideramos relevante

teniendo en cuenta que son las primeras investigaciones que estudian estas

intervenciones sobre pacientes con TCM. Otros estudios en pacientes con cefaleas han

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encontrado resultados similares en cuanto a la modulación del dolor con métodos

aplicados en la región cervical como técnicas de neuro-estimulación periférica del

nervio occipital (Jasper and Hayek, 2008; Lee and Huh, 2013; Saper et al., 2011; Serra

and Marchioretto, 2012; Silberstein et al., 2012; Slavin et al., 2006), infiltraciones

locales (Ashkenazi and Levin, 2007; Mellick and Mellick, 2003, 2008; Mellick et al.,

2006; Saracco et al., 2010) o tratamientos de terapia manual (Castien et al., 2011, 2012,

2013; Espí-López and Gómez-Conesa, 2014; Espí-López et al., 2014; van Ettekoven

and Lucas, 2006; Hall et al., 2007; Mongini et al., 2012; Ylinen et al., 2010).

Otro resultado a destacar, en relación al estudio VI (La Touche et al., 2009) es que el

tratamiento sobre la región cervical basado en terapia manual y ejercicio mejora la MAI

libre de dolor. Este hallazgo es interesante ya que estudios experimentales previos

demostraron que una fijación inducida experimentalmente sobre la región cervical altera

la dinámica mandibular disminuyendo el movimiento y la coordinación mandibular

(Häggman-Henrikson et al., 2006). A partir de estos datos, nosotros planteamos

teóricamente que la mejora de la función de la región cervical a través del tratamiento

de fisioterapia puede evocar mecanismos de modulación del dolor en el CTC que

regularían los efectos nociceptivos periféricos y centrales mejorando a su vez la

dinámica mandibular y las estrategias motoras concomitantes cérvico-

craneomandibulares.

6.7 Implicaciones Científicas y Clínicas

De acuerdo al conjunto de resultados de los estudios de esta tesis podemos afirmar que

la discapacidad y el dolor cervical pueden influir sobre variables sensoriales y motoras

del sistema masticatorio; estos hallazgos nos llevan a reflexionar acerca de la

importancia de incluir a nivel clínico una valoración específica de la región cervical

para los protocolos diagnósticos de los TCM. Cabe destacar que los métodos

220

diagnósticos y de clasificación más utilizados para los pacientes con TCM no incluyen

una valoración especifica del dolor y la discapacidad cervical (Benoliel et al., 2011;

Schiffman et al., 2010, 2014). Un criterio diagnóstico recientemente observado en los

pacientes con cefalea atribuida a TCM es que los movimientos mandibulares, la función

o la parafunción modifican el dolor sobre la región temporal (Schiffman et al., 2012).

Nosotros hemos observado la asociación de la discapacidad cervical con la MAI libre de

dolor, además hemos identificado que los pacientes con mayor discapacidad cervical

presentan mayor fatiga y dolor inducido por el test masticatorio. Estos hallazgos nos

llevan a suponer que la región cervical puede tener un papel importante sobre este tipo

de cefalea, pero esto tiene que confirmarse en futuras investigaciones ya que estos datos

se pueden extrapolar únicamente a los pacientes con cefalea atribuida a TCM que

además presentaban dolor y discapacidad de cuello. Sabemos en la actualidad que la

prevalencia de dolor de cuello en los pacientes con TCM es muy alta, pero no sabemos

en la actualidad la influencia que tiene la región cervical en aquellos pacientes que no

presentan dolor cuello.

Desde el punto de vista del tratamiento, el plantear un abordaje para reducir el dolor y

la discapacidad cervical como parte de la estrategia terapéutica global podría ser

beneficioso para reducir los síntomas sensoriales negativos y mejorar el control motor

masticatorio, consideramos que este planteamiento debe seguir siendo investigado en

futuros estudios. Parte de los hallazgos de esta tesis demuestran que tratamientos de

fisioterapia basados en terapia manual y ejercicio terapéutico sobre la región cervical

producen efectos positivos sobre la modulación del dolor en áreas trigeminales y sobre

la mejora de la MAI libre de dolor (La Touche et al., 2009, 2012), con los cual

consideramos que es positivo integrarlos en los protocolos actuales para este tipo de

pacientes.

221

En varios de los estudios de esta tesis y en otros estudios longitudinales o transversales

se ha observado la influencia de factores psicosociales sobre pacientes con TCM (Chen

et al., 2013; Fillingim et al., 2011, 2013). Específicamente nuestros resultados muestran

una asociación entre el catastrofismo y la kinesiofobia con variables funcionales, de

discapacidad y DCF, estos hallazgos ponen en manifiesto la interacción entre variables

de tipo sensorial con variables psicológicas y esto debería considerarse como una

cuestión determinante a la hora de plantear la valoración o de diseñar las intervenciones

terapéuticas; en pacientes con dolor crónico es fundamental reconocer factores

psicosociales que pueden ser percibidos como obstáculos para la recuperación (Main,

2013): se ha observado que lograr una disminución del catastrofismo del dolor es un

buen predictor de éxito de la rehabilitación en condiciones de dolor (Sullivan, 2013).

La integración de una perspectiva bioconductual en el razonamiento clínico y en la toma

de decisiones podría ser un punto clave en el manejo del dolor y la reeducación motora

en pacientes con DCF y TCM. Se ha demostrado que el tratamiento cognitivo-

conductual disminuye la intensidad del dolor, los síntomas depresivos, mejora la

función masticatoria (Turner et al., 2006), reduce el catastrofismo en pacientes que

sufren TCM crónicos (Turner, Mancl, et al., 2005) y además se ha observado que en

casos de dolor crónico provoca cambios neuroplásticos adaptativos asociados a una

disminución del catastrofismo del dolor (Seminowicz et al., 2013). Prescribir ejercicio

terapéutico puede ser una buena alternativa a tener en cuenta: en relación a esto se ha

observado que el ejercicio en pacientes con dolor lumbar crónico produce una reducción

del catastrofismo y de los síntomas depresivos y estos resultados fueron similares al

tratamiento cognitivo-conductual (Smeets et al., 2006)

222

6.8 Limitaciones y Futuras Investigaciones

Los resultados de esta tesis se han discutido con la consideración de que hay varias

limitaciones que hemos tenido en cuenta y que presentamos a continuación. En los

estudios que conforman esta tesis se han tenido en cuenta algunas variables relacionadas

con la discapacidad y el dolor en la región cervical, sin embargo consideramos que aún

es necesario cuantificar más aspectos de las posibles alteraciones funcionales de la

región cervical como por ejemplo, los rangos de movimiento, la resistencia muscular, la

propiocepción craneocervical y analizar si estas alteraciones pueden tener alguna

relevancia clínica sobre las alteraciones motoras craneomandibulares o sobre el DCF;

sería necesario que futuros estudios precisaran aún más estos aspectos ya que podrían

generar nuevos datos que puedan servir para plantear alternativas diagnósticas y

terapéuticas.

Otra limitación a tener en cuenta, es que en los estudios en donde se ha planteado

intervenciones terapéuticas (VI, VII) solo se han medido los efectos inmediatos y a

corto plazo. Futuros estudios deberían investigar si estas intervenciones tienen un efecto

mantenido a medio y a largo plazo, por otra parte sería necesario realizar estudios de

efectividad de este tipo de intervenciones frente a tratamientos farmacológicos, férulas

oclusales o inclusive otros tratamientos de fisioterapia basados en agentes físicos o

tratamientos de electroterapia.

En esta tesis se han identificado algunos factores psicológicos que han presentado

asociación con la función mandibular y con la discapacidad y el DCF. Desde el

planteamiento neurobiológico de la experiencia multidimensional del dolor (sensorial-

discriminativa, emocional-afectiva, cognitiva) creemos que el haber incluido estas

variables es un acierto ya que ofrece una perspectiva más global de la problemática. A

223

pesar de esto y haciendo una reflexión profunda consideramos que hay otras variables

que son necesarias identificar como por ejemplo la autoeficacia o el tipo de estrategias

de afrontamiento ante el dolor, entre otras. Además sería necesario que los factores

psicológicos identificados como relevantes se sigan estudiando pero con diseños tipo

cohorte, de esta forma se podría establecer relaciones causa efecto. Finalmente y en

relación con la anterior reflexión, creemos que es importante realizar ensayos clínicos

aleatorizados controlados con un enfoque bioconductual donde las intervenciones que se

utilicen se establecieran de forma multimodal para de esta forma intentar influir sobre

variables psicosociales, sensoriales y motoras.

224

225

CONCLUSIONES

226

7. CONCLUSIONES.

1. Las posturas craneocervicales inducidas experimentalmente modifican la

dinámica mandibular y alteran los umbrales de dolor a la presión en áreas

trigeminales en pacientes con trastornos craneomandibulares.

2. Existen pequeñas diferencias en la postura craneocervical entre pacientes con

dolor cérvico-craneofacial y sujetos asintomáticos, pero no se encontraron

asociaciones entre la postura craneocervical y la discapacidad cervical y

craneofacial.

3. Los pacientes con cefalea atribuida a trastornos craneomandibulares con

moderada discapacidad cervical presentan mayores niveles de intensidad de

dolor y fatiga en el test de provocación masticatorio, así como menores umbrales

de dolor a la presión trigeminales y cervicales y una disminución de la máxima

apertura interincisal libre de dolor a las 24 horas posteriores al test de

provocación masticatorio, que los pacientes con leve discapacidad cervical y

sujetos asintomáticos.

4. Los pacientes con dolor de cuello crónico mecánico presentan una hiperalgesia

mecánica en áreas cervicales y trigeminales pero no en áreas extra-trigeminales,

por tanto la sensibilización central en el complejo trigeminocervical podría ser

un mecanismo involucrado en el mantenimiento del dolor de estos pacientes.

5. Existe una asociación entre la discapacidad cervical y la discapacidad

craneofacial en pacientes con dolor craneofacial.

6. La discapacidad cervical es un predictor de la disminución de la máxima

apertura interincisal libre de dolor.

7. La kinesiofobia y catastrofismo ante el dolor son predictores del dolor, la

discapacidad craneofacial y el estatus funcional mandibular.

227

8. El catastrofismo ante el dolor es un predictor de la fatiga masticatoria en

pacientes con cefalea atribuida a trastornos craneomandibulares.

9. Los síntomas depresivos presentan una asociación con la cronicidad y la

intensidad del dolor en pacientes con dolor de cuello crónico mecánico.

10. Las intervenciones fisioterápicas de terapia manual y ejercicio terapéutico sobre

la región cervical provocan efectos hipoalgesicos en áreas cervicales y

trigeminales y mejoran la máxima apertura interincisal libre del dolor en

pacientes con trastornos craneomandibulares.

228

229

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I

UNIVERSIDAD REY JUAN CARLOS

FACULTAD DE CIENCIAS DE LA SALUD

TESIS DOCTORAL

Aspectos neurofisiológicos y biomecánicos de la región

cervical sobre el dolor cérvico-craneofacial:

Implicaciones del tratamiento y el diagnóstico

Departamento Bioquímica, Fisiología y Genética Molecular, Farmacología y

Nutrición, Anatomía y Embriología Humana e Histología Humana y Anatomía

Patológica

Roy La Touche Arbizu

MADRID, 2014

II

Facultad de Ciencias de la Salud Departamento de Bioquímica, Fisiología y Genética Molecular,

Farmacología y Nutrición, Anatomía y Embriología Humana e Histología Humana y Anatomía Patológica

III Avda. de Atenas s/n E 28922 Alcorcón Madrid España Tel. 34 91 4888855 Fax 34 91 4888831

Don Carlos Goicoechea García, Profesor Titular de Farmacología del Dpto. de

Bioquímica, Fisiología y Genética Molecular, Farmacología y Nutrición, Anatomía y

Embriología Humana e Histología Humana y Anatomía Patológica y D. Josué

Fernández Carnero, Profesor Colaborador del Dpto. de Fisioterapia, Terapia

Ocupacional, Rehabilitación y Medicina Física de la Universidad Rey Juan Carlos,

CERTIFICAN:

Que el Trabajo de investigación titulado “Aspectos neurofisiológicos y biomecánicos

de la región cervical sobre el dolor cérvico-craneofacial: Implicaciones del tratamiento

y el diagnóstico” ha sido realizado por Don. Roy La Touche Arbizu (D.N.I.: 50349803

C) bajo nuestra supervisión y dirección y cumple con los requisitos necesarios para

optar al grado de Doctor.

Y para que así conste a los efectos oportunos, firmamos el presente certificado en

Madrid, a 3 de Noviembre de 2014

Fdo. D. C. Goicoechea García Fdo. D. J. Fernández-Carnero

IV

V

A mis papás, Hilda y Melvin por su amor incondicional, esfuerzo constante y sacrificios

realizados durante toda la vida para que yo pudiera llegar hasta aquí, sin ellos este

proyecto no se hubiera podido realizar, gracias por ser mi ejemplo de vida y por las

enseñanzas en torno al esfuerzo, la perseverancia y la paciencia

A mis 5 hermanos y a todos mis sobrinos por estar ahí y comprender mi ausencia en

momentos importantes, a pesar de la distancia siempre están en mi mente y en mi

corazón

VI

VII

AGRADECIMIENTOS

Este proyecto al que he dedicado tiempo y esfuerzo, no se hubiera podido

concluir sin la inestimable ayuda y colaboración de muchas personas que han aportado

sus esfuerzos desinteresadamente en las investigaciones que conforman esta tesis, a

todos ellos quisiera expresarles mi más sincera gratitud.

En mi primer lugar quisiera agradecer a mis dos directores de tesis, el Dr. Carlos

Goicoechea García y el Dr. Josué Fernández Carnero por su ayuda y orientación durante

la elaboración de este trabajo.

Al Dr. Carlos Goicochea García quisiera agradecerle especialmente la

motivación que me ofreció para realizar la tesis una vez que terminé el Máster en

Estudio y Tratamiento del Dolor que él dirigía. Tanto el Dr. Carlos Goicochea como

Dra. Mª Isabel Martín Fontelles y todo su equipo han sido referentes para mí por su

dedicación, rigurosidad, humildad y vocación en la investigación del tratamiento del

dolor. Conocerles y que hayan sido mis profesores ha sido un privilegio que me ha

ayudado a orientar mi actividad investigadora y profesional. Siempre estaré agradecido

con ellos…

Al Dr. Josué Fernández Carnero tengo muchas cosas que agradecerle y algunas

van más allá de este mismo proyecto. Durante todos los años que he tardado en finalizar

este proyecto Josué siempre ha estado detrás de cada paso que di, aportando nuevas

ideas, motivándome y dedicando toda su capacidad y conocimiento en cada una de las

investigaciones. Para mí es un premio haberle conocido y poder establecer una

verdadera relación de amistad, tengo el orgullo de decir que además de conseguir

terminar la tesis he conseguido un gran amigo. Gracias al profesor, gracias al tutor y

sobre todo gracias al amigo que has sido durante estos años.

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Haciendo una retrospectiva de lo que han sido estos años y el proceso para llegar

a conseguir este proyecto, tengo que reconocer que hay personas que han facilitado mi

adaptación a un país diferente al mío, pero el que considero un gran país del cual ya

formo parte, y en este sentido quiero agradecer especialmente al Dr. José Antonio

Martín Urrialde de la Universidad San Pablo CEU, quien me tendió una mano

desinteresadamente y me ayudó en todo momento para venir y estar en España y

conseguir finalmente este sueño. Muchas gracias por todo y más…

Hay varios profesores e investigadores de reconocido prestigio internacional que

han participado en algunas de las investigaciones de esta tesis, quiero agradecer su

colaboración al Dr. Mariano Rocabado Seaton de la Universidad Andrés Bello de Chile,

al Dr. Jeffrey Mannheimer de Columbia University de Estados Unidos de América, al

Dr. Harry Von Piekartz de la University of Applied Science Osnabruck de Alemania y

al Dr. Mark Bishop de la University of Florida de Estados Unidos de América.

Agradezco a mis compañeros y amigos del grupo de investigación Motion in

Brains de CSEU La Salle, los profesores Joaquín Pardo, Alfonso Gil, Ibai López de

Uralde y Héctor Beltrán por su colaboración en las últimas investigaciones de esta tesis.

Quiero agradecer a mi amigo el profesor Santiago Angulo Díaz-Parreño de la

Universidad San Pablo CEU por su ayuda y enseñanzas entorno al tratamiento y análisis

estadístico, su aporte a las investigaciones de esta tesis es incalculable. Muchas gracias

amigo por tu conocimiento, dedicación y amistad…

Si el título de doctor se pudiera compartir yo lo haría con mi pareja Alba París,

ella ha sido mi punto de apoyo en todo momento, ha entendido mi dedicación a la

investigación y ha estado implicada en todas los estudios que conforman esta tesis, su

aporte e implicación científica ha sido excepcional y sus palabras de motivación, su

IX

amor y cariño han sido suficientes para seguir adelante cuando se presentaron las

dificultades. Gracias mi vida por todo y porque cada día es único a tu lado…

A mis cinco hermanos, John, Vivian, Marco, Mayela y Dennis, y todos mis

sobrinos a los que amo mucho y añoro a diario, quiero dedicar esta tesis. Ellos han

sabido comprender mis muchas ausencias en momentos especiales en los que aunque

hubiera querido estar no me ha sido posible, sé que ellos se alegran de los éxitos que he

podido conseguir y yo me alegro de que sean mi familia del cual estoy muy orgulloso

de cada uno de ellos.

Finalmente quiero dedicar este proyecto a mis papás Hilda y Melvin que son

personas excepcionales, bondadosas, esforzadas a las cuales yo tengo una gran

admiración. Ambos con sus actos me han enseñado lecciones de vida impagables, son

pocas las palabras de gratitud que podría escribir en estas frases para expresar mi

profundo agradecimiento, todo y cada una de las cosas he podido conseguir se lo debo a

ellos.

Mi mamá lamentablemente no ha podido ver concluida esta fase profesional que

finalizo con esta tesis, a pesar de esto, en su memoria he querido darle este pequeño

homenaje que en su día le hice la promesa que lo finalizaría con el máximo esfuerzo.

Ella me apoyó en todo momento, sobre todo en los momentos difíciles y me arropó con

sus palabras de amor constantes. Gracias Mami te recuerdo todos los días y te voy a

querer siempre, esto es para ti…

A mi papá Melvin le debo muchas cosas, su vida es ejemplar y ha estado dedicada al

esfuerzo y trabajo por sus seis hijos, su vida es ejemplo de lucha diaria y en todo

momento, sea cual sea la adversidad. La honradez, la dignidad, la constancia y el

esfuerzo son principios que he podido aprender de mi papá, estos me han servido para

entender que el camino hacia un objetivo no siempre es fácil y que las metas no son lo

X

más importante sino el esfuerzo que dediques a ello. Gracias Papi por todo, te quiero

mucho y esto para ti…

En toda investigación clínica los pacientes son determinantes y sin duda alguna

lo más importante, quiero agradecer a todos los pacientes que amablemente accedieron

a participar en los estudios que conforman esta tesis, espero que el conocimiento que

hemos generado sirva de alguna manera para mejorar la atención que reciban o en

motivar a otros investigadores que continúen con estas líneas. Gracias a todos los

pacientes con dolor craneofacial, muchas gracias…

XI

ÍNDICE GENERAL

RESUMEN…………………………………………………………………………...XV

Lista de publicaciones originales………………………………………………...…XIX

Abreviaturas………………………………………………………………..…...…..XXI

1. INTRODUCCIÓN…………………………………………………………………..1

1.1 Aspectos Básicos del Dolor…………………………………………………....2

1.1.1 Proceso de sensibilización periférica………………………………….....4

1.1.2 Proceso de sensibilización central…………………………………….....6

1.2 Dolor Musculoesquelético Crónico…………………………………………...7

1.2.1 Epidemiología…………………………………………………………....7

1.3 Dolor Cervical Crónico………………………………………………………..8

1.3.1 Epidemiología…………………………………………………………..10

1.4 Dolor Craneofacial de Origen Musculoesquelético……………….………..12

1.4.1 Trastornos craneomandibulares………………………………………...12

1.4.2 Epidemiología…………………………………………………………..14

1.4.3 Epidemiología y comorbilidad entre trastornos craneomandibulares,

cefalea y dolor de cuello………………………………………………..16

1.5 Dolor Referido de la Región Cervical hacia la Región

Craneofacial…………………………………………………………………..18

1.6 Aspectos Anatomofuncionales de la Región Craneomandibular y la Región

Craneocervical………………………………………………………………..20

1.6.1 Modelos biomecánicos de la región craneomandibular/craneocervical..21

1.6.2 Estudios in-vivo de la relación craneomandibular/craneocervical……..23

1.6.3 Influencia de la región craneocervical sobre la dinámica mandibular…23

XII

1.6.4 Sinergias neuromusculares cervicales y masticatorias…………….……24

1.6.5 Cinemática y concomitancia craneocervical/craneomandibular………..27

1.7 Neurofisiología del Dolor Cérvico-craneofacial…………………………….28

1.7.1 Sistema sensorial trigeminal…………………………………………....29

1.7.2 Neuroanatomía de los segmentos cervicales superiores………………..35

1.7.3 Complejo trigeminocervical…………………………………………....37

1.7.4 Sensibilización del complejo trigeminocervical………………………..39

1.8 Modulación del Dolor en el Complejo Trigeminocervical…………………41

1.8.1 Influencia de las aplicaciones terapéuticas sobre el dolor craneofacial..43

2. JUSTIFICACIÓN DEL TRABAJO REALIZADO……………………………..47

3. OBJETIVOS……………………………………………………………….……….51

4. MATERIAL Y MÉTODOS……………………………………………………….57

4.1 Participantes……………………………………………………………….….60

4.2 Variables y Pruebas de Medición…………………………………………....62

4.2.1 Medidas de auto-registro…………………………………………….64

4.2.2 Instrumentos de medición…………………………………………...66

4.3 Resumen de los Procedimientos……………………………………………..70

4.4 Análisis Estadístico…………………………………………………………...72

5. RESULTADOS…………………………………………………………………….77

5.1 Estudio I…………………………………………………………………….....78

5.2 Estudio II……………………………………………………………………...87

5.3 Estudio III………………………………………………...………….……...114

5.4 Estudio IV…………………………………………………………………....123

5.5 Estudio V………………………………………………………………….…138

5.6 Estudio VI………………………………………………………………..…..182

XIII

5.7 Estudio VII……………………………………………………………..……192

6. DISCUSIÓN………………………………………………………………………205

6.1 Diferencias de Género en las Variables Somatosensoriales………….…...207

6.2 Postura Craneocervical, Dinámica Mandibular y

Dolor Craneocervical……………………………………………….………208

6.3 Influencia del Dolor y la Discapacidad Cervical sobre la Actividad

Sensoriomotora Trigeminal………………………………………………...209

6.4 Asociación entre la Discapacidad Cervical y la Discapacidad

Craneofacial/craneomandibular…………………………………………...213

6.5 Factores Bioconductuales Implicados en las Alteraciones Sensoomotoras

Trigeminales y la Discapacidad Craneofacial……………………………..213

6.6 Efecto del Tratamiento en la Región Cervical

sobre el Dolor Craneofacial…………………………………….…………..218

6.7 Implicaciones Científicas y Clínicas………………………………………..219

6.8 Limitaciones y Futuras Investigaciones…………………………………....222

7. CONCLUSIONES……………………………………………………………..…225

8. BIBLIOGRAFÍA………………………………………………………………....229

XIV

XV

RESUMEN

Introducción: El dolor craneofacial (DCF) de origen musculoesquelético, representa la

causa más común de DCF de origen no dental y puede afectar a la musculatura

masticatoria, la articulación temporomandibular y otras estructuras orofaciales. Entre

los diferentes tipos de DCF de origen musculoesquelético el más prevalente son los

denominados trastornos craneomandibulares (TCM) atribuidos o relacionados con el

dolor miofascial. Diversos estudios han descrito la presencia de comorbilidades entre la

cefalea, el dolor de cuello y los TCM, además se ha comprobado que el dolor de cuello

se asocia significativamente con los TCM y que la gravedad de estos se incrementa con

la gravedad del dolor de cuello. Evidencia científica reciente sugiere la existencia de

mecanismos neurofisiológicos trigeminocervicales implicados en las alteraciones

motoras craneomandibulares y en el DCF, a pesar de esto se necesitan más estudios

clínicos que aporten información más precisa en cuanto a la posible repercusión clínica

de características sensoriales y motoras cervicales que afectan a pacientes con DCF.

Objetivo general: Determinar la influencia biomecánica y neurofisiológica de la región

cervical sobre la discapacidad y el DCF, además se pretende identificar como

determinados factores bioconductuales influyen sobre la función craneomandibular, la

discapacidad y el DCF.

Métodos: Se realizaron 4 estudios transversales, un estudio de casos y controles, una

serie de casos y un ensayo clínico aleatorio controlado que incluyeron a pacientes con

dolor de cuello crónico mecánico, pacientes con TCM atribuido a dolor miofascial,

pacientes con dolor cérvico-craneofacial (DCCF) y pacientes con cefalea atribuida a

TCM. En tres de los estudios se realizaron comparaciones con sujetos asintomáticos.

En los estudios se evaluaron características sensoriales, motoras y factores psicológicos

implicados en el DCF mediante:

XVI

- Medidas de auto-registro psicológicas, de dolor y discapacidad (inventario de

dolor y discapacidad craneofacial, IDD-CF; índice de dolor de cuello, IDC;

inventario de depresión BECK, BDI; escala de catastrofismo ante el dolor, ECD;

escala tampa de kinesiofobia, TSK-11; Escala visual analógica del dolor, EVA;

escala visual analógica de la fatiga, EVAF).

- Mediciones de los umbrales de dolor a la presión (UDPs) en áreas trigeminales,

cervicales y extra-trigeminales mediante algometría digital.

- Medición de la máxima apertura interincisal (MAI) libre de dolor.

- Mediciones de la postura craneocervical.

En todos los estudios se realizó un análisis descriptivo e inferencial, y en algunos casos

se utilizaron análisis complementarios a los contrastes de significación como el tamaño

del efecto o el mínimo cambio detectable para determinar la relevancia clínica de los

resultados.

Resultados:

En la comparación de los resultados de los sujetos asintomáticos con respecto a los

pacientes se presentaron los siguientes hallazgos: 1) hay diferencias estadísticamente

significativas en la postura craneocervical en los pacientes con DCCF frente a los

sujetos asintomáticos, sin embargo estas diferencias son pequeñas; 2) Se identificó que

los pacientes con dolor de cuello crónico mecánico presentan hiperalgesia mecánica en

áreas trigeminales y cervicales pero no en otras áreas anatómicas a distancia; 3) Los

pacientes con cefalea atribuida a TCM con moderada discapacidad cervical presentaron

mayores niveles de dolor y fatiga masticatoria, y menores UDPS en áreas trigeminales y

cervicales y menor MAI libre de dolor. En las comparaciones intra-grupos se encontró

una fuerte correlación entre la discapacidad cervical y la discapacidad

craneofacial/craneomandibular en pacientes con TCM atribuido a dolor miofascial. Se

XVII

comprobó que distintas posturas craneocervicales inducidas experimentalmente

modifican la dinámica mandibular y alteran los UDPs de áreas trigeminales y

cervicales. Por otra parte, se identificó que el catastrofismo ante el dolor y la

kinesiofobia fueron predictores del estado funcional mandibular y de la discapacidad y

DCF. Finalmente, en los estudios en donde se realizó una intervención en pacientes con

TMC atribuido a dolor miofascial y en pacientes con DCCF se comprobó que el

ejercicio terapéutico en combinación de terapia manual o únicamente la aplicación de

terapia manual sobre la región cervical producen un efecto inmediato y a corto plazo en

la mejora MAI libre de dolor, una disminución de la intensidad de dolor y un aumento

de los UDPS en áreas trigeminales y cervicales.

Conclusiones:

Los resultados obtenidos en esta tesis sugieren la influencia de mecanismos

neurofisiológicos y biomecánicos de la región cervical sobre la función mandibular, las

alteraciones somatosensoriales en áreas trigeminales y sobre la discapacidad

craneofacial. Se ha demostrado que factores bioconductuales como el catastrofismo ante

el dolor y la kinesiofobia deben ser tomados en cuenta ya que son predictores de las

alteraciones funcionales craneomandibulares y el DCF. A nivel terapéutico se presentan

los primeros hallazgos sobre el efecto del tratamiento de fisioterapia específico sobre la

región cervical en la mejora de la dinámica mandibular y en la modulación del DCF.

Esta tesis aporta nuevos datos que pueden contribuir clínicamente al diagnóstico, la

valoración y el tratamiento de los TCM y el DCF.

XVIII

XIX

LISTA DE PUBLICACIONES ORIGINALES

Esta tesis está basada en las siguientes publicaciones originales que forman parte de una

línea de investigación que estudia los mecanismos neurofisiológicos, biomecánicos y

bioconductuales de la región cervical en pacientes con dolor craneofacial, las cuales se

presentan de forma completa en el apartado de resultados. En diferentes apartados del

texto se hace referencia a las publicaciones originales mediante números romanos:

I. La Touche R, París-Alemany A, von Piekartz H, Mannheimer JS,

Fernández-Carnero J, Rocabado M. The influence of cranio-cervical posture

on maximal mouth opening and pressure pain threshold in patients with

myofascial temporomandibular pain disorders. Clin J Pain. 2011

Jan;27(1):48-55

II. López-de-Uralde-Villanueva I, Beltran-Alacreu H, Paris-Alemany A,

Angulo-Díaz-Parreño S, La Touche R. Reliability, Standard Error, and

Minimal Detectable Change of Two Tests for Craniocervical Posture

Assessment in Asymptomatic Subjects and Chronic Neck/craniofacial Pain

Patients. (En revisión).

III. La Touche R, Fernández-de-Las-Peñas C, Fernández-Carnero J, Díaz-

Parreño S, Paris-Alemany A, Arendt-Nielsen L. Bilateral mechanical-pain

sensitivity over the trigeminal region in patients with chronic mechanical

neck pain. J Pain. 2010 Mar;11(3):256-63

IV. La Touche R, Pardo-Montero J, Gil-Martínez A, Paris-Alemany A, Angulo-

Díaz-Parreño S, Suárez-Falcón JC, Lara-Lara M, Fernández-Carnero J.

Craniofacial pain and disability inventory (CF-PDI): development and

XX

psychometric validation of a new questionnaire. Pain Physician. 2014 Jan-

Feb;17(1):95-108.

V. La Touche R, Paris-Alemany A, Gil-Martínez A, Pardo-Montero J, Angulo-

Díaz-Parreño S, Fernández-Carnero J. The Influence of Neck Disability and

Pain Catastrophizing about Trigeminal Sensory-Motor System in Patients

with Headache Attributed to Temporomandibular Disorders. (En revision)

VI. La Touche R, Fernández-de-las-Peñas C, Fernández-Carnero J, Escalante K,

Angulo-Díaz-Parreño S, Paris-Alemany A, Cleland JA. The effects of

manual therapy and exercise directed at the cervical spine on pain and

pressure pain sensitivity in patients with myofascial temporomandibular

disorders. J Oral Rehabil. 2009 Sep;36(9):644-52.

VII. La Touche R, París-Alemany A, Mannheimer JS, Angulo-Díaz-Parreño S,

Bishop MD, Lopéz-Valverde-Centeno A, von Piekartz H, Fernández-

Carnero J. Does mobilization of the upper cervical spine affect pain

sensitivity and autonomic nervous system function in patients with cervico-

craniofacial pain?: A randomized-controlled trial. Clin J Pain. 2013

Mar;29(3):205-15.

XXI

ABREVIATURAS

ATM Articulación temporomandibular

BDI Inventario de depresión Beck

CP Conductancia de la piel

CTC Complejo trigeminocervical

DCCF Dolor cérvico-craneofacial

DCF Dolor craneofacial

DMC Dolor musculoesquelético crónico

ECD Escala de catastrofismo ante el dolor

EMG Electromiografía

END Escala numérica del dolor

ETCM Ejercicio terapéutico de control motor

EVA Escala visual analógica del dolor

EVAF Escala visual analógica de fatiga

FC Frecuencia cardíaca

FR Frecuencia respiratoria

GC Grupo control

GE Grupo experimental

HIT-6 Cuestionario de impacto de la cefalea

IDC Índice de dolor cervical

IDD-CF Inventario de dolor y discapacidad craneofacial

MAI Máxima apertura interincisal

MC Migraña crónica

ME Migraña episódica

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MIAD Modelo integrado de adaptación al dolor

NE Neuronas nociceptivas específicas

NMDA N-metil-D-aspartato

PMG Puntos gatillos miofasciales

RDA Neuronas de rango dinámico amplio

SDM Síndrome de dolor miofascial

STAI Cuestionario de ansiedad estado-rasgo

SVc Sub-núcleo trigeminal caudal

SVi Sub-núcleo trigeminal interpolar

SVo Sub-núcleo trigeminal oral

TC Temperatura cutánea.

TCM Trastornos craneomandibulares

TMO Terapia manual ortopédica

TSK-11 Escala de Tampa de Kinesiofobia

UDP Umbral de dolor a la presión

VPM Núcleo ventral posteromedial del tálamo

1

INTRODUCCIÓN

2

1. INTRODUCCIÓN

1.1 Aspectos Básicos del Dolor

En el modelo biomédico general, el dolor ha sido considerado como un síntoma

producido por un daño tisular, de manera que la experiencia de dolor se ha

simplificado a que, si no había daño no había dolor, si había daño tendría que

haber dolor y a mayor daño mayor dolor. El conocimiento sobre el dolor

evolucionó a partir de la compresión del procesamiento neurofisiológico del dolor

a nivel medular. Melzack y Wall (Melzack and Wall, 1965) tuvieron una

destacada labor en esta cuestión al proponer la teoría de la regulación del umbral

también conocida como la teoría de la puerta de entrada, básicamente esta teoría

explicaba el mecanismo en que el dolor estaba representado neuralmente en el asta

dorsal de la médula espinal, donde se podía facilitar o inhibir la puerta de entrada

de estímulos dolorosos hacia centros superiores. Esta teoría cobró mucha

importancia hace unas décadas a pesar de no poder explicar fisiológicamente la

situación del dolor crónico (Melzack, 1993), sin embargo lo que si permitió fue la

consideración de los factores psicológicos como parte integral del procesamiento

del dolor.

La teoría de regulación del umbral evolucionó hacia la teoría de la neuromatriz, en

esta se amplía el concepto del dolor integrando las influencias que puedan tener las

funciones cognitivas del cerebro, los sistemas de regulación del estrés y los

estímulos sensoriales (Melzack, 1999), además se expone que el dolor es una

experiencia multidimensional compuesta por la interacción de tres dimensiones:

3

- Dimensión sensorial-discriminativa: identifica, evalúa, valora y modifica

todos aquellos factores relacionados con la percepción sensorial del dolor

(intensidad, localización, cualidad, factores temporales y espaciales)

- Dimensión motivacional-afectiva: comporta el aspecto emocional del

dolor. En esta dimensión estarían implicadas estructuras troncoenfálicas y

límbicas.

- Dimensión cognitivo-evaluativa: analiza e interpreta el dolor en función de

la sensación y lo que puede ocurrir.

En la actualidad el dolor se mira desde la óptica del paradigma biopsicosocial, con

lo cual los factores fisiológicos, psicológicos y sociales son tomados en cuenta, así

lo muestra la descripción de dolor definida por la Asociación Internacional para el

Estudio del Dolor:

“Es una experiencia sensorial y emocional desagradable asociada a un daño

tisular real o potencial, o descrita en términos del daño” (Merskey and Bogduk,

1994).

Existen diversas clasificaciones del dolor basadas en el origen, la evolución, los

mecanismos fisiológicos y en la estructura anatómica implicada. Con frecuencia y

desde un punto de vista clínico el dolor musculoesquéletico se clasifica en agudo y

crónico, esta clasificación toma en cuenta la evolución del dolor desde el punto de

vista del tiempo y los aspectos neurofisiológicos relacionados con la génesis y el

mantenimiento.

El dolor agudo tiene un curso temporal relacionado con los procesos de reparación

(Chapman et al., 2011) y representa una señal de alarma disparada por los

sistemas protectores del organismo (Loeser and Treede, 2008). La ineficacia en el

4

tratamiento o en la recuperación del dolor agudo puede generar que este se

mantenga en el tiempo convirtiéndose en un dolor crónico y adquiriendo las

complicaciones que este presenta.

Se define el dolor crónico como “el que persiste más allá del tiempo normal de

reparación de los tejidos, que se supone en el dolor no maligno es de 3 meses…,

pero para fines de investigación se prefiere elegir un tiempo de 6 meses” (Merskey

y Bogduk, 1994). El tiempo (días, meses…) en el que se tiene dolor es el

parámetro más utilizado para definir la diferencia entre el dolor agudo y el dolor

crónico, esta clasificación tiene sus limitaciones teniendo en cuenta que el dolor

crónico presenta una naturaleza multifactorial (Turk and Rudy, 1988). En este

sentido Von Korff y Dunn (Von Korff and Dunn, 2008), han comprobado que un

modelo de clasificación de los pacientes basado en los niveles de discapacidad,

calidad vida, intensidad de dolor, síntomas depresivos y toma de medicamentos

tiene mayor valor predictivo que solo la clasificación basada en el tiempo de dolor

(Von Korff and Dunn, 2008).

1.1.1 Proceso de sensibilización periférica

Desde el punto de vista de la neurofisiología, el dolor agudo es considerado como

una respuesta sensorial de la activación del sistema nociceptivo a consecuencia de

un daño tisular que produce una respuesta inflamatoria que sensibiliza los

nociceptores periféricos (Loeser and Treede, 2008; Woolf, 2004); la

sensibilización se produce a consecuencia de la acción de mediadores químicos de

origen inflamatorio que se liberan en el área del daño tisular, tales como la

sustancia P y el péptido relacionado con el gen de la calcitonina que se liberan en

la periferia y se unen a otros mediadores como neutrófilos, mastocitos y basófilos;

esta unión produce a su vez la liberación de sustancias pro-inflamatorias

5

(citoquinas, bradiquinina, histamina) que favorecen la síntesis de la enzima

ciclooxigenasa-2 (COX-2) que conduce a la producción y secreción

de prostaglandinas (Woolf, 2004). Este mediador actúa como un sensibilizador

que altera la sensibilidad al dolor por el incremento de la capacidad de respuesta

de los nociceptores periféricos (Woolf, 2004).

La sensibilización periférica se define como un proceso en donde hay una

reducción del umbral y una amplificación de la capacidad de respuesta de los

nociceptores, que se produce cuando las terminales periféricas de las neuronas

sensoriales primarias de alto umbral están expuestos a mediadores de inflamación

en el tejido dañado (Chen et al., 1999; Guenther et al., 1999; Hucho and Levine,

2007).

Es un hecho más que contrastado que la sensibilización periférica contribuye a la

sensibilización del sistema nociceptivo y provoca dolor e hipersensibilidad en las

áreas en donde se produce inflamación (hiperalgesia primaria) (Latremoliere and

Woolf, 2009), este fenómeno representa una acción protectora del organismo con

el fin de evitar el uso de estructuras dañadas (Nijs et al., 2010). A la sensación

dolorosa que se extiende más allá del área de la lesión y abarca zonas no afectadas

por la lesión original, se la conoce como hiperalgesia secundaria, pero este no es

un proceso únicamente de carácter periférico, lleva implícitos mecanismos

centrales (Latremoliere and Woolf, 2009; Woolf, 2011).

El proceso de sensibilización periférica se asocia a una alteración en la

sensibilidad térmica, pero no se observa una alteración de la sensibilización

mecánica que parece ser una característica importante de la sensibilización central

(Latremoliere and Woolf, 2009; Woolf, 2004).

6

1.1.2 Proceso de sensibilización central

El dolor crónico está asociado a cambios neuroplásticos sobre mecanismos

periféricos y centrales, estos cambios pueden mantener la percepción de dolor a

pesar de la ausencia de un daño potencial (Woolf and Costigan, 1999); por otra

parte, la característica defensiva propia del dolor agudo no está presente en esta

condición.

Un estímulo doloroso mantenido crónicamente produce una excitación excesiva de

las neuronas medulares y supramedulares, la producción de este proceso hace que

aparezca el mecanismo de la sensibilización central (Latremoliere and Woolf,

2009). La sensibilización central se manifiesta como una reducción prolongada del

umbral y un aumento en la sensibilidad y extensión de las áreas receptoras del asta

dorsal de la medula espinal (Ji et al., 2003), además se ha observado una

ineficiencia en los mecanismos inhibitorios encargados de la modulación del dolor

(Meeus et al., 2008).

Desde el punto de vista clínico la sensibilización central puede provocar que la

percepción de un estímulo no doloroso se convierta en un estímulo doloroso

(alodinia), por otra parte los estímulos dolorosos serían percibidos como una

sensación de dolor desproporcionado (hiperalgesia). Se ha sugerido que la

sensibilización central puede ser el mecanismo por el cual los factores

psicológicos y somáticos se correlacionan desde el punto de vista neurobiológico.

Además, se plantea que el distrés psicológico resultante del proceso de dolor

crónico contribuye al mecanismo de sensibilización central, lo que produce una

amplificación del dolor (Curatolo et al., 2006).

7

1.2 Dolor Musculoesquelético Crónico

Se considera dolor musculoesquelético crónico (DMC) cuando el dolor se

mantiene entre 3 y 6 meses (Walsh et al., 2008). El DMC se producen alteraciones

neurales, somáticas, cognitivas y conductuales (Walsh et al., 2008), que generan

una disminución de la calidad de vida del paciente y de su desempeño laboral.

El dolor musculoesquelético es descrito usualmente por los pacientes como una

sensación firme y de presión, de características difusas y que a menudo se

acompaña de hiperalgesia muscular profunda o alodinia (Graven-Nielsen, 2006),

este tipo de dolor puede manifestarse de forma localizada, regional y generalizado

(Graven-Nielsen and Arendt-Nielsen, 2010). El síndrome de dolor miofascial

(SDM), es un ejemplo de una condición de dolor regional muscular que se

caracteriza por la presencia de bandas tensas y dolor referido característico

causado por puntos gatillo miofasciales (PGM) (Simons, 1996).

La transición de dolor agudo musculoesquelético localizado a dolor crónico

generalizado está probablemente relacionada con la progresión de la

sensibilización periférica y central (Graven-Nielsen and Arendt-Nielsen, 2010). La

neurofisiología del DMC podría explicarse a través del proceso de sensibilización

central (Graven-Nielsen and Arendt-Nielsen, 2010).

1.2.1 Epidemiología

El dolor crónico es muy prevalente en la población general (Elliott et al., 1999) y

genera impacto negativo sobre la calidad de vida, el desempeño laboral y la

interacción psicosocial del paciente (Becker et al., 1997; Breivik et al., 2006).

8

El DMC se ha convertido en el principal motivo de consulta de dolor crónico en

atención primaria en la geografía española (Batlle-Gualda et al., 1998; Català et

al., 2002).

En una reciente revisión se ha descrito que la prevalencia del DMC se encuentra

entre el 13.5% y 47% de la población general y la del DMC generalizado varía

entre 11.4% y 24% (Cimmino et al., 2011).

En relación al SDM se ha sugerido que es el tipo de dolor más prevalente de entre

los de origen musculoesquelético (Simons, 1996), pero no hay datos precisos en

cuanto a la prevalencia de este en relación a la población general; a pesar de esto

en la actualidad clínica se tiene muy en cuenta al SDM, aún más conociendo que

en muchas investigaciones se ha demostrado que los PG son muy prevalentes en

diversos trastornos musculoesqueléticos como la cefalea tensional crónica

(Couppé et al., 2007), el dolor orofacial (Fernández-de-Las-Peñas et al., 2010), los

dolores relacionados con el raquis (Chen and Nizar, 2011), el dolor de hombro

(Bron et al., 2011) o la epicondilalgia lateral (Fernández-Carnero et al., 2007).

1.3 Dolor Cervical Crónico

La Neck Pain Task Force define el dolor cervical como un evento episódico a lo largo

de la vida que presenta una recuperación variable entre los diferentes episodios

(Guzman et al., 2009).

El dolor cervical frecuentemente denominado como no específico, de tejidos blandos o

dolor cervical mecánico se puede definir como aquel localizado en el territorio situado

entre la línea nucal superior y la línea de la espina de la escápula, en la parte posterior

del cuerpo, y en la parte anterior por encima del borde superior de la clavícula y el

esternón dejando fuera el contorno facial; con o sin irradiación a la cabeza, tronco y

9

miembros superiores (Guzman et al., 2009). Los signos de irradiación del dolor son

contemplados por esta definición, en relación con esto Bogduk (Bogduk, 2003) sugiere

que los signos de irradiación hacia la extremidad superior no deben asumirse como

parte del dolor cervical ya que estos son más propios del dolor cervical radicular y

fisiopatológicamente estas dos condiciones son muy distintas, además añade que la

confusión de estas dos entidades clínicas puede llevar a errores en el diagnóstico y

planteamientos de investigación y tratamiento poco adecuados (Bogduk, 2003).

Más acorde con la sugerencia de Bogduk (Bogduk, 2003) es la definición propuesta por

Merskey y Bogduk (Merskey and Bogduk, 1994), en esta, el dolor cervical se define

como el dolor que surge en una región limitada superiormente por la línea nucal

superior, lateralmente por los márgenes laterales del cuello, e inferiormente por una

línea imaginaria transversal a través de la apófisis espinosa T1.

El dolor cervical puede considerarse como un síntoma muy frecuente en la mayoría de

trastornos que afectan al cuadrante superior, aunque rara vez es síntoma de la presencia

de tumor, infección u otra afección grave (Bogduk, 2003). El dolor cervical puede

coexistir junto a otros trastornos musculoesqueléticos (Harris et al., 2006). Y puede

estar provocado o asociado a una patología local o una enfermedad sistémica tales como

lesiones de la piel, alteraciones de la laringe, tumores, infección, fracturas y

dislocaciones, traumatismos, mielopatías, artritis reumatoide u otras enfermedades

reumáticas (Haldeman et al., 2008).

El dolor cervical tiene una etiología multifactorial, con factores de riesgo no

modificables como la edad y el sexo (Hogg-Johnson et al., 2009). En estudios

realizados en población general relacionados con la edad, se ha observado que los

sujetos más jóvenes tienen mejor pronóstico de recuperación de la discapacidad cervical

(Hogg-Johnson et al., 2009). También se ha demostrado que otros trastornos

10

musculoesqueléticos y problemas psicológicos pueden considerarse factores de riesgo

del dolor cervical, y frecuentemente se asocian a él (Carroll et al., 2008; Hogg-Johnson

et al., 2009).

Entre los factores psicológicos asociados a un mal pronóstico de dolor cervical que se

han descrito son los estados de angustia, sufrimiento, enfado o frustración en respuesta

al dolor (Hill et al., 2004), en contraposición a esto se ha observado que el positivismo

y la alta autoestima estuvieron asociados con un mejor pronóstico (Haldeman et al.,

2008).

Existe mucha literatura que avala que los cambios degenerativos cervicales van

unidos a la presencia de dolor cervical persistente e incapacitante, pero no hay evidencia

de que los cambios degenerativos obtenidos con RMN cervical se correlacionen con

síntomas de dolor cervical. Tampoco hay evidencia suficiente para demostrar que la

degeneración de disco sea un factor de riesgo para tener dolor de cuello (Nordin et al.,

2008).

Un factor positivo es el hecho de practicar ejercicio, se ha visto que si se practicaba

ejercicio físico, ante la presencia de un dolor de cuello, éste tendrá mejor pronóstico que

si el paciente es sedentario (Hogg-Johnson et al., 2009), e incluso otro estudio sugiere

que el ejercicio puede tener un efecto protector contra el dolor cervical (van den Heuvel

et al., 2005).

Entre los factores predictivos relacionados con el dolor crónico se han encontrado, el

acoso laboral, trastornos de sueño, el índice de masa corporal en la mujeres, el trabajo

relacionado con el agotamiento emocional en los hombres, presentar dolor cervical

agudo con anterioridad y dolor crónico lumbar (Kääriä et al., 2012).

1.3.1 Epidemiología

El dolor de cuello es una de las condiciones de dolor más frecuente, la prevalencia de

11

dolor de cuello en la población general se ha estimado entre 10% y 15%, siendo más

común en mujeres que en hombres (Borghouts et al., 1999). En un reciente estudio de la

prevalencia de dolor en el cuello en la población española se ha estimado que indica un

19.5% anual entre los adultos españoles (Fernández-de-las-Peñas et al., 2011).

Un 70% aproximadamente de las personas, puede que experimenten un dolor cervical

en algún momento de sus vidas (Côté et al., 1998). En la población que sufre dolor

cervical se ha encontrado que a la hora de cualificarlo se representa en forma de

pirámide, en la que la base es conformada por un gran número de casos de dolor leve,

por encima pocos casos que consultan por su dolor y en la punta solo unos pocos casos

de dolor invalidante (Côté et al., 1998; Hogg-Johnson et al., 2009). Cote y cols.

encontraron que el 39.4 % de los individuos han tenido dolor cervical en los últimos 6

meses (Côté et al., 1998).

La literatura sugiere que entre el 50-80% de la población general que ha experimentado

dolor cervical, lo volverán a sufrir entre 1 -5 años más tarde y la mayor parte no se

recuperan totalmente del problema (Carroll et al., 2008). En general en la literatura se

dividen los grupos de edad en dos grandes grupos: jóvenes y mayores, siendo los de

peor pronóstico estos últimos. Hill y cols. (Hill et al., 2004) realizaron un estudio en el

que los sujetos se dividen en tres grupos de edades; se observó que en el grupo de edad

de entre 45-59 años, existe una tendencia 4 veces mayor a que el dolor cervical se

cronifique, recurra o sea continuo comparado con edades menores y mayores.

Más de 1/3 de los pacientes desarrollan síntomas crónicos que durarán más de 6 meses

(Côté et al., 2008). Entre un 15-32% de los individuos continúan experimentando

síntomas 5 años después del primer episodio de dolor de cuello (Enthoven et al., 2004;

Pernold et al., 2005). Después de 10 años, aproximadamente un 32% de los que

experimentan un primer episodio continuarán presentando síntomas moderados o

12

graves y un 79% mejoran del dolor pero no desaparece completamente (Gore et al.,

1987).

1.4 Dolor Craneofacial de Origen Musculoesquelético

El dolor craneofacial (DCF) es una denominación general que es utilizada para describir

la presencia de dolor en la cara, cabeza y estructuras asociadas, puede estar originado

por una variedad de condiciones, estructuras o etiologías (Armijo Olivo et al., 2006;

Kapur et al., 2003). El DCF se puede clasificar en neuropático, neurovascular y

musculoesquéletico (Benoliel et al., 2011). El DCF de origen musculoesquelético,

representa la causa más común de DCF de origen no dental y puede afectar la

musculatura masticatoria, la articulación temporomandibular (ATM) y estructuras

orofaciales (Okeson and de Leeuw, 2011). Los signos y síntomas más prevalentes que

se han observado en los pacientes con DCF son: dolor al abrir la boca, dolor a la

palpación muscular y dolor articular (Macfarlane et al., 2001), y por orden de

porcentaje, las áreas de expansión del dolor que se han descrito como más prevalentes

son: alrededor de los ojos, alrededor de la región temporal, en la zona anterior a la oreja

y en la ATM y alrededores de esta (Macfarlane, Blinkhorn, Davies, Kincey, et al.,

2002). Los factores psicológicos están muy presentes en el DCF y se han observado

múltiples comorbilidades con otras dolencias y patologías (Macfarlane et al., 2001).

El DCF de origen musculoesquelético según la Asociación Internacional para el Estudio

del Dolor se clasifica en cefalea tensional crónica, trastornos craneomandibulares

(TCM) dolorosos, TCM causados por artritis o artrosis, distonías y discinesias faciales y

traumatismos craneofaciales (Merskey and Bogduk, 1994).

1.4.1 Trastornos craneomandibulares

El término TCM se refiere a una serie de signos y síntomas que afectan a la musculatura

masticatoria, la ATM y estructuras asociadas o ambas (Okeson and de Leeuw, 2011;

13

Okeson, 1997), se considera un proceso patológico multifactorial causado posiblemente

por hiperactividad muscular o por parafunciones, lesiones traumáticas, influencias

hormonales y cambios a nivel articular (Liu and Steinkeler, 2013). Estos trastornos se

caracterizan por: (a) dolor orofacial y/o en la ATM o en los músculos masticatorios; (b)

alteraciones en el movimiento mandibular y/o limitación del rango de movimiento

mandibular; y (c) presencia de ruidos articulares durante la función mandibular (Liu

and Steinkeler, 2013; Okeson and de Leeuw, 2011).

Los factores psicosociales tienen un papel relevante en los TCM, en un reciente estudio

cohorte se identificó que el estrés, la afectividad negativa y las estrategias de

afrontamiento ante el dolor presentan una repercusión importante sobre los TMD

(Fillingim et al., 2011), por otra parte, Kindler y cols. (Kindler et al., 2012)

encontraron que los síntomas depresivos están más presentes en pacientes con TCM

articulares mientras la ansiedad estuvo más asociado con TCM de origen muscular.

Características psicológicas incluyendo la somatización, depresión y la ansiedad

relacionados con el género parecen tener un impacto significativo en la prevalencia de

TCM (Licini et al., n.d.). Evidencia reciente describe que las pacientes femeninas con

TCM presentan mayor percepción de intensidad del dolor y sensibilidad muscular a la

palpación que pacientes masculinos (Schmid-Schwap et al., 2013).

Existen diversos criterios diagnósticos para clasificar los TCM (Benoliel et al., 2011;

Schiffman et al., 2010), sin embargo la clasificación más utilizada en la actualidad son

los Criterios diagnósticos de investigación para TCM (en inglés, Research Diagnostic

Criteria for Temporomandibular Disorders; RDC/TMD) (Dworkin and LeResche, 1992;

Schiffman et al., 2010), estos criterios presentan una fiabilidad y validez contrastada

englobado en un protocolo sistematizado de valoración, diagnóstico y clasificación de

los subtipos más comunes de TCM (Look et al., 2010). Los Criterios diagnósticos de

14

investigación para TCM establecen la clasificación en dos grandes secciones definidos

en dos ejes: Eje I: Diagnóstico del dolor; y el Eje II Estatus psicosocial (Schiffman et

al., 2014). Es importante destacar que estos criterios han sido recientemente revisados y

el Eje I de diagnóstico ha sido dividido en dos grandes grupos de trastornos, TCM

relacionados con dolor y trastornos del disco y patología degenerativa de la ATM

(Tabla 1) (Schiffman et al., 2014).

Tabla 1. Clasificación diagnóstica de los trastornos craneomandibulares (Schiffman et

al., 2014).

Trastornos craneomandibulares

relacionados con dolor

Trastornos del disco y patología

degenerativa de la articulación

temporomandibular.

Mialgia Luxación del disco con reducción

Mialgia local Luxación del disco con reducción y con

bloqueos intermitentes

Dolor miofascial Luxación del disco sin reducción y con

limitación de la apertura

Dolor miofascial referido Luxación del disco sin reducción y sin

limitación de la apertura

Artralgia Trastornos degenerativos

Cefalea atribuida a trastornos

craneomandibulares

Subluxación

1.4.2 Epidemiología

El DCF es una dolencia muy prevalente en la población general en torno a un 17-26%

de los cuales el 11,7% llega a convertirse en condición crónica (Macfarlane, Blinkhorn,

15

Davies, Ryan, et al., 2002). En relación al sexo es más prevalente en mujeres y el rango

de edad donde se presenta con mayor frecuencia es entre los 18-25 años y los 56-65

años (Macfarlane, Blinkhorn, Davies, Kincey, et al., 2002). La presencia de dolor en la

región temporomandibular se produce en aproximadamente un 10% de la población

adulta (LeResche, 1997). Las mujeres presentan en general más signos y síntomas de

TCM y además estos son frecuentes y más severos que en los hombres (Adèrn et al.,

2014; Carlsson, 1999; LeResche, 1997), por otra parte las mujeres tienen menos

probabilidades de recuperarse de sus síntomas (Wänman, 1996) y son más propensas a

buscar tratamiento (Carlsson, 1999). En un reciente estudio se encontró que el 26.8% de

mujeres con TCM evaluadas se clasificaron como trastornos moderados frente a un

9.3% de TCM graves (Campos et al., 2014). En pacientes ancianos se encontró mayor

prevalencia de TCM en mujeres y los trastornos se clasificaron en un 43% leves, 13%

moderados y 4.5% en graves (Camacho et al., 2014).

De Kanter y cols. en un meta-análisis de 51 estudios epidemiológicos encontraron una

prevalencia del 30% de síntomas de TCM (De Kanter et al., 1993), en otro estudio se

observó el 10% de la población estudiada presentaba TCM y de estos el 50% presentó

más de un signo de TCM (Gesch et al., 2004). Se ha observado una mayor prevalencia

de signos y síntomas en edades intermedias (Carlsson, 1999; Yekkalam and Wänman,

2014), Yekkalan y Wanman en un estudio reciente encontraron mayor prevalencia de

signos entre los sujetos de 35 y 50 años (Yekkalam and Wänman, 2014) y la evidencia

muestra una prevalencia menor en edades adultas (Carlsson, 1999; Matsuka et al., 1996;

Yekkalam and Wänman, 2014). Manfredini y cols. en un estudio epidemiológico con

pacientes con TCM encontraron que el 56.4% de los pacientes presentaron un

diagnóstico de dolor muscular, el 42% de luxación del disco y 57.5% otros trastornos

articulares (Manfredini et al., 2012).

16

En cuanto a la incidencia, Kamisaka y cols. realizaron un estudio longitudinal en un

espacio temporal de 4 años y encontraron una incidencia del 6% para el dolor en la

ATM y un 12.9% para ruidos articulares en la ATM, en esta misma investigación se

encontró en los sujetos menores de 40 años un mayor riesgo de presentar ruidos en

ATM y las mujeres presentaban un aumento en el riesgo de perpetuación de dolor en la

ATM (Kamisaka et al., 2000).

1.4.3 Epidemiología y comorbilidad entre trastornos craneomandibulares, cefalea

y dolor de cuello

Los TCM, las cefaleas y el dolor de cuello son trastornos muy relacionados (Sipilä et

al., 2002; Storm and Wänman, 2006; Wiesinger et al., 2007). Varios estudios han

informado que los signos y síntomas se superponen entre los pacientes con TCM,

cefaleas y dolor en el cuello respectivamente (Anderson et al., 2011; Rantala et al.,

2003), se ha demostrado que el dolor de cuello se asocia significativamente con los

TCM y que la gravedad de éstos se incrementa con la gravedad del dolor de cuello

(Ciancaglini et al., 1999; Nilsson et al., 2013; Wiesinger et al., 2009), adicionalmente,

se ha comprobado que los factores psicosociales a su vez están relacionados con la

presencia de cefalea, dolor de cuello y dolor orofacial (Rantala et al., 2003). Stuginski-

Barbosa investigaron recientemente los signos de TCM en pacientes con migraña

crónica (MC) y episódica (ME), en esta investigación se identificó que el 73% de los

pacientes con MC presentaron dolor a la palpación en la musculatura masticatoria, 63%

presentaron dolor a la palpación articular y 64% presentaron dolor a la palpación del

cuello (Stuginski-Barbosa et al., 2010), otras estudios similares, pero realizados en

pacientes adolecentes con cefalea han observado una alta comorbilidad con los TCM

dolorosos, además se encontró una asociación significativa con el dolor de cuello

(Nilsson et al., 2013), además en pacientes adolescentes con TCM, encontraron que los

17

pacientes que presentaban alteraciones musculares y alteraciones musculares y

articulares tuvieron mayores niveles de dolor mandibular y orofacial, cefalea, dolor de

cuello y dificultad para comer alimentos blandos (Karibe et al., 2010).

Se ha sugerido que los TCM, las cefaleas y el dolor de cuello pueden tener una base

fisiopatológica similar (Ashina et al., 2006; Marklund et al., 2010; Svensson, 2007), por

otra parte se ha identificado que la cefalea podría ser un factor de riesgo de sufrir dolor

de cuello (Leclerc et al., 1999).

Rantala y cols. describió que de entre 1339 sujetos evaluados la prevalencia de signos

relacionados con la ATM fue del 10%, el dolor orofacial fue del 7%, la cefalea del 15%

y el dolor de cuello el 39% (Rantala et al., 2003), por otra parte, Plesh y cols. mostró

que el 53% de los pacientes con TCM que presentaron dolor de cabeza severo, el 54%

tenía dolor de cuello (Plesh et al., 2011). Un estudio realizado con 487 mujeres Sami

encontró que un 17% de estas presentó dolor en la regiones mandibular y orofacial que

además lo asociaban a una limitación de su calidad de vida, y en este mismo estudio se

describe que la duración del dolor en la región mandibular, las molestias al realizar la

apertura, el dolor de cuello y un nivel educativo bajo estaban relacionados cuando los

síntomas de TCM influían en la vida cotidiana (Mienna and Wanman, 2012), en

relación con esto dato, Weber y cols. encontraron que el 88,24% de los pacientes con

TCM presentaron a su vez dolor cervical, en esta investigación se sugiere que esta

situación está generada principalmente por factores neurofisiológicos y no por factores

biomecánicos como la postura (Weber et al., 2012).

La prevalencia del latigazo cervical en pacientes con TCM ha sido estudiada en una

revisión sistemática reciente (Häggman-Henrikson et al., 2014), en esta se describe que

la prevalencia del latigazo cervical en pacientes con TCM varía entre 8,4% a un 70%,

este resultado se comparó con la población general sin TCM en donde la prevalencia de

18

latigazo cervical se encuentra entre 1,7% y 13%, además en esta revisión se señala que

los pacientes con TCM con antecedentes de haber sufrido un latigazo cervical presentan

más signos de alteración de la ATM como limitación de la apertura bucal, más dolor

articular, cefalea y síntomas de estrés. Los autores de esta revisión sugieren que el

latigazo cervical puede ser un iniciador y/o un factor agravante, así como una condición

comórbida con los TCM (Häggman-Henrikson et al., 2014)

1.5 Dolor Referido de la Región Cervical hacia la Región Craneofacial

Diversas estructuras de la región cervical pueden provocar dolor referido hacia la región

craneofacial, la literatura científica describe que las articulaciones cervicales, los

ligamentos y los músculos son estructuras relevantes a tener en cuenta en la

identificación de los patrones del dolor que pueden afectar al cráneo, la región

craneomandibular y la región orofacial. Son muchos los estudios que demuestran que

los PGM del trapecio, el esplenio, el esternocleidomastoideo y los músculos sub-

occipitales producen dolor referido hacia la región craneofacial en pacientes con TCM y

cefaleas (Alonso-Blanco et al., 2012; Fernández-de-Las-Peñas et al., 2006, 2010;

Fricton et al., 1985; Wright, 2000). Muchos de estos patrones de dolor referido

evocados por PGM fueron descritos por Simons y cols. (Simons et al., 1999) (Figura

1).

19

Figura 1. Representación modificada de los patrones de dolor referido hacia la región craneofacial provocado por

PGM de músculos de la región cervical.

A nivel de las estructuras articulares de la región cervical, la investigación relacionada

con la infiltración de sustancias algógenas y estudios relacionados con el diagnóstico

estructural han identificado patrones o mapas de dolor referido hacia la región

craneofacial, específicamente Dreyfuss y cols. comprobaron en sujetos sanos que la

infiltración de sustancias algógenas sobre la articulación atlanto-occipital y la

articulación atlanto-axial lateral provocaban patrones de dolor referido sobre la región

cervical superior y la cabeza (Dreyfuss et al., 1994), también Dwyer y cols. con un

procedimiento similar en sujetos sanos identificaron que las articulaciones

zigoapofisarias C2-C3 provocan patrones de dolor referido hacia la región cervical y la

cabeza (Dwyer et al., 1990), estos patrones fueron confirmados con gran similitud en

pacientes (Aprill et al., 1990; Cooper et al., 2007). Se ha sugerido que el patrón de dolor

de las articulaciones zigoapofisarias C3-C4 ocasionalmente puede estar relacionado con

20

la cefalea cevicogénica (Cooper et al., 2007), sin embargo en el caso del disco

intervertebral C2-C3 sí se ha identificado como una fuente importante de dolor referido

hacia la cabeza en pacientes con cefalea cervicogénica (Schofferman et al., 2002)

(Figura 2).

Figura 2. Representación, según la evidencia científica de los patrones de dolor referido de estructuras articulares

cervicales hacia áreas craneocervicales (Aprill et al., 1990; Cooper et al., 2007; Dreyfuss et al., 1994; Dwyer et al.,

1990).

Destacar como hallazgo científico reciente, que Watson y Drummond encontraron

patrones de dolor referido hacia la cabeza muy similares al valorar la articulación

atlanto-occipital y las articulaciones zigoapofisarias C2-C3 en pacientes con migraña y

cefalea tensional (Watson and Drummond, 2012).

1.6 Aspectos Anatomofuncionales de la Región Craneomandibular y la Región

Craneocervical

La asociación entre la región craneomandibular y la región craneocervical ha sido

estudiada en las últimas décadas desde diversos paradigmas, incluyendo enfoques

anatómicos, biomecánicos, neurofisiológicos, y patofisiológicos (Armijo Olivo et al.,

2006), en este apartado se pretende hacer una descripción detallada de la evidencia

21

disponible relacionada con las posibles relaciones entre estas regiones tomando en

cuenta los enfoques anatómicos y biomecánicos desde la función normal.

1.6.1 Modelos biomecánicos de la relación cranemandibular/craneocervical

Uno de los primeros planteamientos teóricos de la dinámica craneomandibular

/craneocervical fue el desarrollado por Brodie (Brodie, 1950), este autor desarrolló un

esquema gráfico (Figura 3), que explicaba cómo la postura erguida de la cabeza se

mantenía mediante el equilibrio neuromuscular de los músculos anteriores y posteriores

de la región craneocervical y cervical. Otro postulado importante que proponía este

modelo es que una actividad mandibular como el apretar isométricamente tendría que

estar equilibrada por la activación de los músculos cervicales cuando la cabeza está

erguida (Brodie, 1950; Thompson and Brodie, 1942), Rocabado desarrolló un modelo

similar al anterior, en este se señala que la estabilidad craneomandibular se mantiene

entre el equilibrio de las fuerzas anteriores (músculos masticatorios, músculos supra e

infrahiodeos, y los músculos cervicales anteriores) y posteriores (músculos cervicales

posteriores), ambos grupos musculares junto a otras estructuras de la región

craneomandibular trabajan de forma sinérgica en una cadena funcional; por otra parte

este autor sugiere que la posición de la mandíbula y del hueso hiodes depende de la

curvatura cervical (Rocabado, 1983).

22

Figura 3. Esta figura representa el esquema diseñado por Brodie, para explicar el equilibrio mecánica neuromuscular

entre las regiones craneocervical y craneomandibular (Brodie, 1950; Thompson and Brodie, 1942).

Resultados de estudios basados en modelos matemáticos apoyan en gran medida las

tesis teóricas anteriormente descritas (Gillies et al., 1998; Suzuki et al., 2003), un

ejemplo de esto es el estudio de Suzuki y cols. en este se generó un sistema mecánico de

análisis dinámico del sistema estomatognático en condiciones de normalidad, se

observó como resultado principal que la actividad muscular de la región cervical influye

sobre la actividad mecánica de la mandíbula, además sugieren que los músculos

cervicales coordinan y resisten los cambios en la postura de la cabeza durante los

movimientos mandibulares (Suzuki et al., 2003). Otro de los modelos biomecánicos

relacionados con la dinámica mandibular, señala que el movimiento de extensión

craneocervical facilita la apertura mandibular y sugieren que esta situación se da para

lograr una mejor activación de los músculos que realizan la apertura y para generar una

posición más favorable para el movimiento (Koolstra and van Eijden, 2004).

23

1.6.2 Estudios in-vivo de la relación craneomandibular/craneocervical

La mayoría de estudios in-vivo en torno a las hipótesis de la relación

craneomandibular/craneocervical se han realizado con electromiografía (EMG), análisis

cinemático y estudios radiológicos; estas investigaciones se han diseñado con el

objetivo de comprobar la influencia mutua de ambas regiones en la dinámica articular

mandibular, en la estabilidad postural y en los aspectos funcionales más generales en los

que participa la ATM y las estructuras asociadas, como por ejemplo la deglución y la

masticación.

1.6.3 Influencia de la región craneocervical sobre la dinámica mandibular

En cuanto a la dinámica mandibular, Visscher y cols. demostraron pequeñas

variaciones en la posición del cóndilo mandibular según la postura craneocervical, sus

hallazgos mostraron que la distancia intra-articular en la ATM en el movimiento de

cierre es menor con retracción craneocervical y mayor con protrusión craneocervical

(Visscher et al., 2000), en relación con esto, Omure y cols. observaron que al inducir

experimentalmente la posición de protrusión craneocervical, el cóndilo mandibular se

posteriorizaba en comparación a la posición neutra (Ohmure et al., 2008), estos

hallazgos confirmarían las observaciones de Solow y Tallegren que en 1976 ya

describieron que el movimiento de extensión craneocervical se asocia a una retrusión

mandibular (Solow and Tallgren, 1976). Otro de los aspectos importantes que se han

investigado sobre la dinámica de la ATM es que la apertura mandibular se ve

directamente influenciada por la posición craneocervical, observándose un aumento de

la apertura mandibular en la posición de protracción craneocervical y una disminución

en la posición de retracción craneocervical cuando se comparan con la posición neutra

(Higbie et al., 1999). Un esquema de la relación de la postura craneocervical y la

dinámica intra-articular de la ATM es representada en la figura 4.

24

Figura 4. Este esquema representa el efecto de la postura de protracción craneocervical sobre la dinámica mandibular

y la musculatura masticatoria según la evidencia científica de estudios experimentales. La imagen A señala un

aumento de la actividad electromiográfica cuando se induce la postura de protracción craneocervical. La imagen B

representa una posteriorización del cóndilo mandibular asociado a la postura de protracción craneocervical.

1.6.4 Sinergias neuromusculares cervicales y masticatorias

La electromiografía ha sido uno de los instrumentos más utilizados para investigar las

acciones coordinadas, sinérgicas o asociadas entre la musculatura de la región

craneomandibular (musculatura masticatoria) y la musculatura del cuello. Diversos

estudios han comprobado la activación del músculo esternocleidomastoideo durante el

apretamiento (Clark et al., 1993; Davies, 1979; Hochberg et al., 1995; Rodríguez et al.,

2011; So et al., 2004; Venegas et al., 2009; Yoshida, 1988) (Figura 5) y el

rechinamiento dentario (Rodríguez et al., 2011; Venegas et al., 2009), en relación con

esto Clark y cols. describieron que para lograr un 5% de la contracción del

esternocleidomastoideo durante el apretamiento dentario se necesita una activación del

A

B

25

50% del músculo masetero (Clark et al., 1993), evidencia reciente demuestra que

durante la masticación se produce una acción concomitante entre los músculos masetero

y esternocleidomastoideo y el nivel activación de estos músculos se modula de acuerdo

a la demanda del elemento que se esté masticando (Häggman-Henrikson et al., 2013);

otras investigaciones realizadas con electromiografía profunda y superficial han

comprobado que durante diversas tareas de apretamiento dentario varios músculos de la

región cervical (esternocleidomastoideo, semiespinales del cuello y la cabeza,

multífidos cervical, elevador de la escápula, esplenio de la cabeza) son activados y este

reclutamiento se produce en torno al 2% y al 14% de la contracción voluntaria máxima

(Giannakopoulos, Hellmann, et al., 2013; Giannakopoulos, Schindler, et al., 2013;

Hellmann et al., 2012). Al contrario de la mayoría de los estudios que se han realizado

con la función de apretamiento dentario, Armijo-Olivo y Magee estudiaron la apertura

mandibular realizada contra resistencia, los resultados mostraron un aumento similar de

la actividad electromiográfica de los músculos masetero, temporal, esplenio de la

cabeza y de las fibras superiores del músculo trapecio. (Armijo-Olivo and Magee,

2007).

A B

26

Figura 5. Esta figura representa un esquema diseñado según la evidencia científica que muestra que el apretamiento

dentario modifica la actividad electromiográfico de músculos cervicales (A). En la figura B se muestra una

concomitancia entre los movimientos craneocervicales y craneomandibulares (el movimiento de apertura bucal se

asocia un movimiento de extensión craneocervical y el movimiento de cierre al movimiento de flexión

craneocervical).

Un hallazgo importante a destacar es que se ha observado que en posiciones de reposo

mandibular se produce un descenso en la actividad electromiográfica de los músculos

trapecio y esternocleidomastoideo (Ceneviz et al., 2006), sin embargo parece ser que los

diferentes tipos de oclusión no influyen sobre la actividad eletromiográfica de la

musculatura del cuello (Ferrario et al., 2006). La figura 5 representa un esquema de la

elevación de la actividad electromiográfica de los músculos cervicales durante el

apretamiento dentario.

En cuanto a la influencia del movimiento craneocervical sobre la actividad

electromiográfica de la musculatura masticatoria, Funakoshi y cols. observaron que se

producía una gran activación del músculo temporal y una moderada activación del

músculo masetero al realizar una extensión craneocervical (Funakoshi et al., 1976), a

diferencia de este estudio, Ballenberger y cols. investigaron la influencia de los

movimientos de la región cervical superior (rotación, extensión, flexión e inclinación

lateral) y encontraron diferencias estadísticamente significativas sobre la actividad

electromiográfica del músculo masetero pero no sobre el músculo temporal, además en

este estudio se señala que la actividad electromiográfica se incrementa más en extensión

que la flexión craneocervical (Ballenberger et al., 2012), en relación con esto, Forsberg

y cols. determinaron que el incremento de actividad de masetero durante la extensión

craneocervical se produce entre 10º y los 20º (Forsberg et al., 1985). Estudios en donde

se ha inducido experimentalmente la posición de protracción craneocervical han

descrito un aumento de la actividad de los músculos masetero (McLean, 2005; Ohmure

27

et al., 2008), digástrico (Ohmure et al., 2008) y geniogloso (Milidonis et al., 1993).

1.6.5 Cinemática y concomitancia craneocervical/craneomandibular

Los estudios que valoran específicamente la cinemática craneomandibular/

craneocervical han encontrado patrones de movimiento con un alto nivel de

coordinación espacio-temporal (Eriksson et al., 1998, 2000; Kohno, Matsuyama, et al.,

2001; Zafar, 2000; Zafar et al., 2000, 2002), estos hallazgos sugieren que las funciones

mandibulares comprenden acciones sincronizadas de la ATM y la región

craneocervical (articulación atlanto-occipital y las articulaciones vertebrales cervicales),

y esta coordinación es mayor en los movimientos más rápidos (Zafar et al., 2000) y en

general el movimiento craneocervical es sincrónico o se anticipa al movimiento

mandibular (Eriksson et al., 2000). Entre los movimientos que presentan una

concomitancia se encuentra, el de apertura mandibular que se acompaña de una

extensión craneocervical y el movimiento de cierre que se acompaña de una flexión

craneocervical (Eriksson et al., 1998) (Figura 5). Resultados similares se han obtenido

en otros estudios (Kohno, Kohno, et al., 2001; Torisu et al., 2002; Yamabe et al., 1999);

es importante destacar que Eriksson y cols. comprobaron que el movimiento

craneocervical es mayor en la apertura (entorno al 50%) y significativamente menor en

el cierre mandibular (entorno al 30-40%) (Eriksson et al., 1998). Un estudio reciente ha

demostrado que el movimiento concomitante de extensión craneocervical al realizar la

apertura mandibular fue significativamente mayor en los niños que en los adultos, los

autores de esta investigación sugieren que esa situación se genera en los niños como

mecanismos para aumentar la magnitud de la apertura mandibular (Kuroda et al., 2011).

Dos de las funciones orales en donde participa la ATM son la fonación y la masticación,

el movimiento de la región craneocervical también está implicado en estas funciones

28

(Häggman-Henrikson and Eriksson, 2004; Miyaoka et al., 2004), específicamente se ha

demostrado que el movimiento de flexo-extensión craneocervical acompaña los ciclos

masticatorios, pero además de acuerdo a como sea el tamaño del bolo alimenticio que se

mastique, el movimiento de extensión craneocervical se ve modificado (Häggman-

Henrikson and Eriksson, 2004); en cuanto a la fonación se ha observado que diversas

tareas en donde se articulan palabras y se realiza apertura-cierre están asociada a

movimientos de la región craneocervical (Miyaoka et al., 2004).

En la actualidad contamos con evidencia científica muy abundante que demuestra las

relaciones anatomofuncionales entre la regiones craneomandibular y la craneocervical,

sin embargo esta información no es suficiente para demostrar los aspectos

neurofisiológicas implicados en ambas funciones; resultados de investigación básica en

conejos han descrito mecanismos neurales supramedulares implicadas en las acciones

rítmicas cervicales y craneomandibulares (Igarashi et al., 2000), otros autores han

teorizado que las acciones concomitantes son comandos pre-programados a nivel central

(Torisu et al., 2001; Zafar, 2000) y que las funciones vienen moduladas por

mecanismos sensoriomotores trigeminocervicales (Eriksson et al., 1998; Zafar, 2000).

El conocimiento entorno a la neurofisiología trigeminocervical puede ayudar a

comprender las situaciones comorbilidad del dolor de cuello y el DCF o las alteraciones

disfuncionales motoras craneocervicales/craneomandibulares; estos aspectos

neurofisiológicos se desarrollan en el siguiente apartado.

1.7 Neurofisiología del Dolor Cérvico-craneofacial

La base neurofisiológica del dolor referido de la región cervical hacia el área

craneofacial se puede explicar mediante un fenómeno anatómico y fisiológico de

convergencia de aferencias nociceptivas trigeminales y cervicales que confluyen en el

núcleo trigeminal espinal y en los segmentos cervicales superiores (Bartsch and

29

Goadsby, 2003a, 2003b; Bartsch, 2005; Piovesan et al., 2003), este centro de

procesamiento del dolor se ha denominado complejo trigeminocervical (CTC). Este

complejo es el responsable de transmitir información sensorial visceral e información

nociceptiva de la cabeza y la región orofacial hacia otros centros superiores como el

tálamo, el hipotálamo y la corteza somatosensorial primaria (Benjamin et al., 2004;

Malick and Burstein, 1998; Malick et al., 2000, 2001) (Figura 6) e inclusive tiene

conexiones neurales con áreas del diencéfalo y el tronco encefálico relacionadas con la

modulación del dolor (Akerman et al., 2011).

1.7.1 Sistema sensorial trigeminal

El sistema sensorial trigeminal lo conforman: a) el nervio trigémino (y sus tres

divisiones: oftálmica, V1; maxilar, V2; y mandibular, V3); b) el ganglio del trigémino

(Gasser); c) la raíces nerviosas trigeminales; y d) los componentes centrales

trigeminales del tronco encefálico (los núcleos trigeminales, los tractos trigeminales y

las vías tálamo-trigeminales) (Sessle, 2005b; Waite and Ashwell, 2004) (Figura 6). El

nervio trigémino es el más grande de los nervios craneales y es considerado un nervio

mixto ya que tiene una división sensorial y una motora (Majoie et al., 1995; Sanders,

2010), además es importante destacar que proporciona la inervación sensorial principal

de la cara, la cavidad oral y parte de cráneo (Majoie et al., 1995; Sessle, 2005a).

30

Figura 6. La imagen representa la organización neuroanatómica del sistema trigeminal desde la periferia hasta las

conexiones neurofisiológicas a nivel central. S1, corteza somatensorial primaria; VMP, núcleo ventral posteromedial

del tálamo; NTE, núcleo trigeminal espinal; GT ganglio trigeminal.

El ganglio de Gasser es una estructura fina, considerado como un análogo craneal de los

ganglios de la raíz dorsal en el sistema nervioso periférico, pero es significativamente

más grande anatómicamente (Dixon, 1963; Kerr, 1963; Moses, 1967). La mayoría de

los cuerpos celulares de aferencias primarias trigeminales procedentes de la tres

divisiones del nervio trigémino (V1, V2 y V3) residen en el ganglio de Gasser, en donde

se encuentran organizadas de manera somatotópica (Borsook et al., 2003; Byers and

Närhi, 1999; Jacquin et al., 1986; Leiser and Moxon, 2006), pero hay que tomar en

cuenta que los cuerpos celulares de algunas aferencias periodontales y de los husos

musculares residen en el núcleo mesencefálico (Capra and Dessem, 1992).

Las fibras aferentes primarias trigeminales terminan en los tejidos craneofaciales como

31

terminaciones nerviosas libres y funcionan como nociceptores, estos pueden activarse

con estímulos nocivos mecánicos, térmicos y químicos. Su activación puede resultar en

la excitación de fibras de pequeño diámetro y de conducción lenta (A-delta o C) (Sessle,

1999, 2005b, 2011; Takemura et al., 2006). Una serie de componentes neuroquímicos

(por ejemplo, la sustancia P, 5-HT, prostaglandinas, bradiquininas) están involucrados

en la activación de estas terminaciones periféricas por estimulación nociva o en su

sensibilización periférica; la sensibilidad de las terminaciones puede aumentar después

de una lesión leve, y esta sensibilización de las terminaciones nociceptivas es un

mecanismo periférico que ayuda a proteger los tejidos lesionados de repetidos agravios

(Sessle, 2000, 2005b, 2011).

La división V1 inerva la región nasal y peri-orbital (incluyendo la córnea y la

conjuntiva), la duramadre supratentorial, así como la frente y la parte superior de la

cabeza que se superpone con el dermatoma C2. La división V2 suministra inervación al

área cigomática, el labio superior, una parte de la cavidad nasal y oral (incluyendo los

dientes del maxilar y su periodonto asociado), y la división V3 inerva a las estructuras

extra e intra-orales restantes en el tercio inferior de la cara (incluyendo los dientes de la

mandíbula y su periodonto), el labio inferior, la piel de la mejilla, y dos tercios

anteriores de la lengua, el mentón, la ATM, además de la piel cubre la mandíbula y el

lado de la cabeza (parte de la región temporal) a excepción de el ángulo de la mandíbula

que es la parte del dermatoma C2 (Majoie et al., 1995; Sanders, 2010). Las fibras

eferentes motoras del V3 inervan los cuatro músculos de la masticación (masetero,

temporal y pterigoideo medial y lateral), el músculo milohiodeo, el fascículo anterior

del músculo digástrico, el músculo tensor del tímpano y el músculo tensor del velo

palatino (Kamel and Toland, 2001; Majoie et al., 1995). En la figura 7 se representan

gráficamente los dermatomas trigeminales (Figura 7).

32

Figura 7. Representación gráfica de los dermatomas trigeminales y cervicales.

El nervio trigémino tiene cuatro núcleos centrales en el tronco encefálico (un núcleo

motor y 3 sensoriales): a) el núcleo mesencefálico trigeminal, que media la

propiocepción; b) el núcleo sensitivo principal, que media la sensación táctil

(principalmente tacto epicrítico y en menor medida tacto protopático); c) el núcleo

motor que proporciona inervación motora: y d) el núcleo espinal trigeminal, que media

el dolor, la sensibilidad térmica y táctil (Majoie et al., 1995; Sessle, 2000) (Figura 8).

El núcleo espinal trigeminal consiste en la división de tres sub-núcleos: a) oral (SVo);

b) interpolar (SVi); y c) caudal (SVc) (Sessle, 1999, 2000, 2005b, 2011). Los sub-

núcleos SVo y SVi se asocian con la transmisión de la percepción táctil; por otra parte,

están implicados principalmente en mecanismos nociceptivos orofaciales relacionados

especialmente con el dolor intra-oral y peri-oral (Dallel et al., 1988, 1990; Raboisson et

al., 1995). Los núcleos trigeminales se representan en la figura 8.

33

Figura 8. Representación gráfica de los núcleos trigeminales, también se muestra la subdivisión del núcleo trigeminal

espinal en sus 3 sub-núcleos: SVo, sub-núcleo trigeminal oral; SVi, sub-núcleo trigeminal interpolar; SVc, sub-

núcleo trigeminal caudal.

El sub-núcleo SVc se extiende desde el nivel de la OBEX (bulbo raquídeo) hasta el

nivel de C3 de la médula espinal cervical. Este sub-núcleo es el homólogo de la

sustancia gelatinosa del asta de posterior de la medula espinal ya que sus neuronas

tienen morfología celular similar, así como las conexiones sinápticas, y sus funciones.

Dado que el sub-núcleo SVc se encuentra inmediatamente superior a la sustancia

gelatinosa de los niveles de la médula espinal cervical, también se le denomina como el

"asta dorsal medular" (Sessle and Hu, 1991; Sessle, 1987; Sessle et al., 1986). El sub-

núcleo SVc es considerado como la principal área relacionada con la información

nociceptiva de los tejidos craneofaciales superficiales y profundos (Dubner and Bennett,

1983; Ebersberger et al., 2001; Schepelmann et al., 1999; Sessle and Hu, 1991; Sessle,

34

1987, 2005b).

En las láminas superficiales y profundas del SVc predominan dos tipos de neuronas

nociceptivas (neuronas nociceptivas específicas [NE] y neuronas de rango dinámico

amplio [RDA]), estas neuronas trasmiten información aferente nociceptiva hacia centros

superiores (núcleo ventral posteromedial del tálamo [VPM]) (Sessle, 1987, 2000,

2005a, 2011). Las neuronas NE sólo responden a estímulos nocivos (por ejemplo,

pellizcar, estímulos térmicos nocivos) aplicados a un campo receptivo craneofacial

localizado y reciben impulsos aferentes de fibras de diámetro pequeño (fibras A delta

y/o C); las neuronas RDA son excitadas por estímulos no nocivos (por ejemplo

estímulos táctiles), así como por estímulos nocivos, y pueden recibir impulsos aferentes

de fibras de gran diámetro (fibras A) y de pequeño diámetro (fibras C) (Sessle, 1999).

La mayoría de neuronas NE y RDA, también pueden ser excitadas por otros tipos de

entradas aferentes periféricas de diversas regiones como las meninges, tejido vascular,

los dientes, la ATM o en los músculos masticatorios (Burstein et al., 1998; Dostrovsky

et al., 1991; Sessle, 1996, 1999, 2000). Los extensos patrones convergentes de entradas

aferentes que son característicos de la ATM o de la duramadre son activados por

neuronas NE y RDA en el SVc, este fenómeno podría explicar la mala localización del

dolor profundo, así como la difusión del dolor referido que es condición típica de

dolencias que implican la ATM y la musculatura asociada (Sessle, 1999, 2011).

Las neuronas trigeminales somatosensoriales del tronco encefálico proyectan a otras

estructuras de esta misma región anatómica como la formación reticular y los núcleos

motores de otros nervios craneales; estas conexiones proporcionan respuestas

autonómicas y motoras ante estímulos craneofaciales (Sessle, 1987, 1996, 1999).

Específicamente las neuronas del SVc proyectan hacia el núcleo VPM del tálamo a

través de una vía multisináptica denominada tracto lemnisco trigeminal dorsal (tracto

35

trigeminotalámico dorsal) (Dougherty and Willis, 1992; Dougherty et al., 1992; Sessle,

1999; Sherman et al., 1997) (Figura 9). Las neuronas nociceptivas del núcleo VPM

tienen conexiones con la corteza somatosensorial (Sherman et al., 1997), representando

la dimensión sensorial-discriminativa del dolor. También se ha observado otras

conexiones como por ejemplo con la corteza cingulada anterior, situando a estos

circuitos neurales como parte de la dimensión afectivo-emocional del dolor (Sessle and

Hu, 1991; Sessle, 1999).

Figura 9. Representación gráfica del tracto trigeminotalámico dorsal. GT, ganglio trigeminal; NTE, núcleo

trigeminal espinal; SVc; sub-núcleo trigeminal caudal; VPM, Núcleo ventral posteromedial del tálamo; S1, corteza

somatosensorial primaria.

1.7.2 Neuroanatomía de los segmentos cervicales superiores

La médula espinal cervical superior incluye los segmentos espinales C1 y C2 en donde

emergen periféricamente los tres primeros nervios cervicales que se distribuyen en un

ramo dorsal, un ramo ventral y los nervios sinovertebrales (Alix and Bates, 1999;

36

Bogduk, 1981), estos nervios inervan a nivel motor y sensitivo diversas estructuras de la

parte posterior de la cabeza y el cuello (Bogduk, 2001) que pueden generar dolor

referido hacia la cabeza y la región orofacial (Johnston et al., 2013). El nervio C1

presenta un ganglio de la raíz dorsal ectópico, se ha observado que en algunos casos

(20%) este nervio carece de raíz dorsal y en estos casos las células ganglionares se

pueden encontrar entre las raíces del nervio espinal accesorio (Ouaknine and Nathan,

1973). Este nervio carece de distribución sensitiva cutánea, sin embargo a través de su

rama dorsal inerva sensitivamente a nivel profundo los músculos cortos del triángulo

suboccipital (Bogduk, 1982), su ramo ventral pasa por detrás y debajo de articulación

atlanto-occipital a la que suministra inervación (Bogduk, 2001)

El nervio C2 da inervación sensitiva a las articulaciones atlantoaxoideas laterales y

mediales; la duramadre de la fosa craneal posterior y de la médula espinal superior; y la

arteria carótida y vertebral. La rama ventral de este nervio inerva los músculos

paravertebrales, el músculo esternocleidomastoideo y el trapecio y la rama dorsal los

músculos semiespinales de la cabeza y el músculo esplenio de la cabeza. El nervio

sinovertebral de C2 se une a los de C1 y C3 para suministrar inervación a los

ligamentos transversal, alar y a la membrana tectoria (Bogduk, 2001). La rama ventral

de C3 se une al plexo cervical e inerva los músculos paravertebrales. La rama medial

del ramo dorsal de C3 inerva el músculo semiespinoso cervical y el músculo multifidus

y además inerva las articulaciones cigapofisiarias de C2-C3. El nervio sinovertebral de

C3 inerva el disco intervertebral C2-3 en su cara posterior (Bogduk, 2001; Bogduk et

al., 1988).

A nivel cutáneo la inervación sensitiva de la región craneocervical la suministran los

nervios occipital menor, occipital mayor y el nervio auricular mayor (Poletti, 1991; Shin

et al., 2007), estos tres nervios sensitivos más la zona cutánea que inervan conformarían

37

los dermatomas de la región craneocervical, estos dermatomas (C2, C3) tienen una

representación que incluye la parte posterior del cráneo (cuero cabelludo), el ángulo de

mandíbula, la región sub-occipital, la parte posterior de la oreja y la garganta (Poletti,

1991). Es importante destacar que la mayor distribución cutánea del nervio C2 está

representada por el nervio occipital mayor (Poletti, 1991).

1.7.3 Complejo trigeminocervical

El CTC es una unidad anatómica-funcional que forman las astas dorsales de los dos

segmentos superiores de la médula cervical y el SVc del núcleo espinal trigeminal

(Becker, 2010; Hoskin et al., 1999; Hu et al., 2005; Piovesan et al., 2003). Estudios

anatómicos en animales han encontrado que el CTC se extiende hasta el segmento

cervical C2-C3 (Goadsby and Hoskin, 1997; Kaube et al., 1993; Strassman et al., 1994).

En el CTC se produce una convergencia de neuronas nociceptivas de segundo orden que

reciben aferencias nociceptivas primarias trigeminales y de los tres primeros nervios

cervicales (Bartsch and Goadsby, 2003b; Bartsch, 2005; Bogduk, 2001; Goadsby et al.,

2008; Hu et al., 1995, 2005; Piovesan et al., 2003) (Figura 10). Evidencia científica de

estudios básicos en animales ha demostrado este fenómeno de convergencia (Bartsch

and Goadsby, 2002, 2003a; Hu et al., 1993; Sessle et al., 1986; Yu et al., 1995), y

también se tiene evidencia de este mecanismo en seres humanos (Busch et al., 2006;

Piovesan et al., 2001).

38

Figura 10. Representación gráfica del complejo trigeminocervical (CTC).

El CTC puede ser sensibilizado por aferencias nociceptivas primarias provenientes del

músculo masetero y de la ATM (Cairns et al., 2001, 2002; Nishimori et al., 1986;

Shigenaga et al., 1988), además se ha descrito que las aferencias primarias nociceptivas

provenientes de la piel y de los músculos cervicales son capaces de excitar neuronas del

CTC (Bartsch and Goadsby, 2003a; Le Doaré et al., 2006; Sessle et al., 1986), sin

embargo parece ser que la principal contribución aferente cervical hacia este complejo

neural está mediada por la raíz de C2, representada periféricamente por el nervio

occipital mayor (Bartsch, 2005), en relación con esto, Goadsby y cols. demostraron que

la activación de las fibras aferentes del nervio occipital mayor aumentan la actividad

metabólica de neuronas del CTC (Goadsby et al., 1997), por otra parte, Le Doare y cols.

observaron que los receptores N-metil-D-aspartato (NMDA) glutamatérgicos están

39

implicados en estas sinapsis (Le Doaré et al., 2006), varios estudios han demostrado que

los receptores NMDA son importantes en el desarrollo de la sensibilización central del

SVc (Chiang et al., 1998; Yu et al., 1996), así como los receptores de la neuroquinina y

purinérgicos (Dubner and Ren, 2004). Recientemente se ha comprobado en modelo

animal, que la lesión sobre un nervio espinal superior provoca alodinia mecánica y la

hiperalgesia térmica en la piel de la cara, los resultados de esta investigación también

sugieren que la fosforilación de la kinasa de regulación extracelular en el SVc y en las

neuronas de C1-C2 y la activación de las células astrogliales están involucradas en el

dolor orofacial extraterritorial producido después de una lesión (Kobayashi et al., 2011).

Xie describe que en la sensibilización central trigeminal las células gliales tienen una

importante implicación incluyendo la interacción con los receptores NMDA

glutamatérgicos y purinérgicos (Xie, 2008).

1.7.4 Sensibilización central del complejo trigeminocervical

Neurofisiológicamente la recepción de entradas de aferencias nociceptivas en el sistema

nervioso central forma parte de la sensibilización central que es un proceso fundamental

en el desarrollo y mantenimiento del dolor referido y el dolor crónico (Arendt-Nielsen

et al., 2000; Salter, 2004). En la sensibilización central trigeminal se produce una

expansión de los campos receptivos profundos y cutáneos neuronales, y además se han

observado otros cambios en las propiedades de las neuronas del trigeminales y en las

vías nociceptivas medulares (Bereiter et al., 2005; Chiang et al., 1998, 2005; Lam et al.,

2009; Salter, 2004; Vernon et al., 2009), específicamente se ha demostrado que la

aplicación experimental de una “sopa inflamatoria” en la duramadre puede inducir una

sensibilización central de las neuronas trigeminales nociceptivas de segundo orden en el

SVc, generando una mayor capacidad de respuesta a la estimulación cutánea de la

región facial y en la duramadre (Burstein et al., 1998), en relación con este hallazgo,

40

Bartsch y Goadsby encontraron que la estimulación del nervio occipital mayor podía

causar una sensibilización central con un aumento de la excitabilidad de la entrada de la

duramadre (Bartsch and Goadsby, 2002), además, se ha observado que la activación de

los nociceptores meníngeos por mediadores pro-inflamatorios sensibilizan a las

neuronas de primer orden en el ganglio trigeminal (Strassman et al., 1996) y las

neuronas de segundo orden trigeminovasculares en el CTC (Burstein et al., 1998).

En el proceso de sensibilización central se producen salidas eferentes que involucran

conexiones entre motoneuronas y aferencias nociceptivas neuronales que su vez generan

respuestas motoras (Bartsch, 2005; Sessle, 2002). Evidencia científica basada en

estudios realizados con modelos animales han demostrado que la estimulación química

nociceptiva de estructuras profundas paravertebrales musculares de la región cervical

evocan efectos reflejos, incluyendo un aumento de la actividad electromiográfica en los

músculos masticatorios y cervicales ipsilaterales (Hu et al., 1993, 1996; Shin et al.,

2005) y alteraciones en los reflejos de apertura mandibular (Makowska et al., 2005).

Similares resultados se han observado en la estimulación nociceptiva de las meninges

posteriores de la rata (Hu et al., 1995). Por otra parte, se ha demostrado que la inyección

de bradiquinina en el músculo masetero en conejos provoca un aumento de la actividad

fusimotora de los husos musculares paravertebrales de la región cervical, estos

hallazgos sugieren que existe una potente conexión refleja entre el sistema trigeminal y

el sistema neuromuscular cervical (Hellström et al., 2000, 2002), resultados similares se

han descrito en estudios realizados en sujetos sanos, en donde se observó que un dolor

provocado experimentalmente en el músculo masetero provoca un aumento de la

actividad electromiográfica en los músculos esternocleidomastoideo y el esplenio del

cuello (Svensson et al., 2004), además de un aumento del reflejo de estiramiento de

estos músculos (Wang et al., 2004); otra de las manifestaciones motoras a nivel

41

mandibular que se han observado es la limitación momentánea de la apertura

mandibular después de provocar un dolor experimental en el músculo trapecio mediante

la infiltración de suero salino hipertónico (Komiyama et al., 2005). Un hallazgo

importante observado recientemente es que al provocar un dolor experimental sobre el

músculo masetero se produce una alteración del control motor de las acciones

integradas de la región craneocervical y craneomandibular al realizar los movimientos

de apertura y cierre (Wiesinger et al., 2013).

La sensibilización central del CTC se manifiesta clínicamente con un aumento de las

áreas de expansión del dolor en territorios trigeminales y cervicales, una mala

localización del dolor, hiperalgesia, alodinia mecánica (Katsarava et al., 2002; Kaube et

al., 2002; Sessle, 1999, 2002, 2011) y una disfunción de la activación del sistema

inhibitorio descendente (King et al., 2009; Maixner et al., 1998; Sarlani et al., 2004)

1.8 Modulación del Dolor en el Complejo Trigeminocervical

La recepción de los estímulos nociceptivos por las neuronas de segundo orden del CTC

está modulada por proyecciones inhibitorias descendentes de estructuras del tronco

encefálico, el diencéfalo y la corteza somatosensorial (Akerman et al., 2011; Bartsch

and Goadsby, 2003b; Sessle, 1999, 2000), se ha demostrado que la manipulación de las

neuronas ventrolaterales de la sustancia gris periacueductal (Bartsch, Knight, et al.,

2004; Knight and Goadsby, 2001; Knight et al., 2002), el núcleo magno del rafe

(Edelmayer et al., 2009) y el bulbo rostroventral (Lambert et al., 2008) pueden modular

la actividad nociceptiva evocada en el CTC, evidencia previa ha demostrado que la

estimulación de estas áreas produce un importante efecto inhibitorio anti-nociceptivo

(Fields et al., 1991) (Figura 11), sin embargo es importante destacar que la activación

del bulbo rostroventral también puede facilitar la hiperalgesia, el dolor neuropático y el

dolor crónico (Porreca et al., 2002; Ren and Dubner, 2002; Sugiyo et al., 2005; Venegas

42

et al., 2009). Otros estudios en donde se ha estimulado químicamente la región posterior

del hipotálamo han demostrado que esta región también influye en la modulación

nociceptiva del CTC (Bartsch et al., 2005; Bartsch, Levy, et al., 2004).

Figura 11. Representación gráfica del sistema inhibitorio descendente y las estructuras implicadas en la modulación

de la actividad nociceptiva. SVc, sub-núcleo trigeminal cervical; NTE, núcleo trigeminal espinal; BRV, bulbo

rostroventral; vlPAG; área ventrolateral de la sustancia gris periacueductal; HT, hipotálamo; S1, corteza

somatosensorial primaria.

En el proceso de activación del sistema inhibitorio descendente se producen diversos

mecanismos que incluyen la participación de los receptores opioides y de

neurotransmisores como el GABA y la serotonina (5-HT) (Sessle, 1999, 2002). El SVc

recibe proyecciones serotoninérgicas y encefalinérgicas del núcleo magno del rafe

(Beitz, 1982; Beitz et al., 1987) que tienen una actuación en la modulación del dolor

(Mason and Fields, 1989). Por otra parte, se ha demostrado que en la médula espinal y

en el SVc el principal neurotransmisor que actúa en la actividad eferente inhibitoria en

43

el bulbo rostroventral es la 5-HT (Beitz, 1982; Clatworthy et al., 1988; Fields et al.,

1991), en relación con esto, Okamato y cols. comprobaron en un modelo animal de

dolor inflamatorio persistente de la ATM que los receptores 5-HT3 en el CTC están

involucrados en los circuitos inhibitorios serotoninérgicos centrales que modulan la

actividad nociceptiva profunda y superficial (Okamoto et al., 2005).

Acciones terapéuticas relacionadas con los cambios del comportamiento, intervenciones

farmacológicas y otros tratamientos que actúan a nivel estructural, influyen sobre

mecanismos tronco encefálicos relacionados con la modulación descendente del dolor

craniofacial (Sessle, 2002).

1.8.1 Influencia de las aplicaciones terapéuticas sobre el dolor craneofacial

A partir de los resultados de estudios experimentales sobre mecanismos

neurofisiológicos implicados en la modulación de dolor en el CTC, muchos

investigadores han planteado estrategias terapéuticas para influir sobre estructuras de la

región cervical y a su vez modular el dolor de cabeza y orofacial. Las intervenciones

sobre el nervio occipital han sido de las más utilizadas en las últimas décadas, son

varios los estudios que se sugieren que la neuro-estimulación periférica del nervio

occipital es efectiva en la disminución del dolor orofacial y la cefalea en un porcentaje

importante de los pacientes en los que se aplica este tratamiento (Jasper and Hayek,

2008; Lee and Huh, 2013; Saper et al., 2011; Serra and Marchioretto, 2012; Silberstein

et al., 2012; Slavin et al., 2006). Siguiendo con las intervenciones sobre el nervio

occipital, hay que destacar que Leroux y Ducros en una recientemente revisión de

ensayos clínicos y series de casos, describen que la infiltración mediante cortico-

esteroides con o sin adición de anestésicos locales sobre el nervio occipital en pacientes

con cefalea en racimos produce efectos inmediatos en la disminución de la frecuencia

de los ataques, sin embargo varios estudios describen que el dolor local tras la

44

intervención es un efecto secundario muy común pero no considerado grave (Leroux

and Ducros, 2013), en otra revisión narrativa se sugiere que la infiltración del nervio

occipital mayor presenta efectos positivos sobre los pacientes con migraña pero se

señala que estos datos se interpreten con precaución ya que se han extraído de estudios

con pobres diseños metodológicos (Ashkenazi and Levin, 2007). Posterior a esta

revisión, se publicaron dos ensayos clínicos aleatorizados en donde se pretendía

comprobar el efecto de una infiltración del nervio occipital mayor y de puntos gatillo de

músculos paravertebrales y del trapecio utilizando anestésicos locales con y sin cortico-

esteroides en pacientes con migraña, los resultados de ambas investigaciones

demostraron la efectividad de ambas intervenciones en la reducción del dolor de cuello

y el dolor de cabeza pero no hubo diferencia en la comparación de los dos tratamientos

(Ashkenazi et al., 2008; Saracco et al., 2010). Evidencia científica proveniente de

estudios de series de casos retrospectivos describen que la infiltración intramuscular de

bupivacaina en la musculatura paravertebral reduce el dolor en pacientes adultos

(Mellick and Mellick, 2003, 2008; Mellick et al., 2006) y en niños (Mellick and

Pleasant, 2010) que presentan dolor orofacial y/o cefalea.

La evidencia sobre la administración de bupivacaina intratecal en la región cervical para

dolores refractarios cervicales, de cabeza y orofaciales es limitada, sin embargo las

series de casos publicadas describen una eficacia en la analgesia producida y una

disminución de la utilización de fármacos opiáceos (Appelgren et al., 1996; Lundborg

et al., 2009) por otra parte, los efectos adversos descritos fueron pocos y la mayoría de

los casos transitorios (Lundborg et al., 2009).

Intervenciones específicas de fisioterapia aplicadas al tratamiento de la región cervical

para modular el dolor en pacientes con cefalea han sido muy investigadas en las últimas

dos décadas, específicamente se debe destacar que un gran número de ensayos clínicos

45

muestran que la terapia manual, el ejercicio terapéutico o la combinación de ambas

enfocadas a tratar estructuras musculoesqueléticas de la región cervical han demostrado

efectividad en las disminución de la intensidad y la frecuencia del dolor en pacientes

con cefalea tensional y cefalea cervicogénica (Castien et al., 2011, 2012, 2013; Espí-

López and Gómez-Conesa, 2014; Espí-López et al., 2014; van Ettekoven and Lucas,

2006; Hall et al., 2007; Mongini et al., 2012; Ylinen et al., 2010).

46

47

JUSTIFICACIÓN

48

2. JUSTIFICACIÓN DEL TRABAJO REALIZADO

La región orofacial y el cráneo, que a su vez incluyen estructuras orales y dentales

representan una de las zonas anatómicas más complejas del organismo, esta situación

conlleva a una difícil compresión de los mecanismos fisiopatológicos de los trastornos

que afectan a la región craneofacial como por ejemplo los TCM, las cefaleas y el dolor

orofacial (Fricton, 2014). La comprensión de la clínica, la patogénesis y el tratamiento

es esencial para ayudar a los pacientes que presentan estos problemas (Graff-Radford,

2007).

Es manifiesto que en la últimas décadas se ha incrementado de manera exponencial la

investigación en torno al DCF, estos estudios en su mayoría se han enfocado en estudiar

los mecanismos biológicos periféricos y centrales relacionados con la transmisión y

modulación nociceptiva, así como los sistemas de clasificación del paciente y los

factores psicosociales implicados (Hargreaves, 2011), los resultados de algunas

investigaciones en esta línea sugieren, que áreas extra-trigeminales como la región

cervical parecen tener un papel relevante en la fisiopatología de las cefaleas y el dolor

orofacial (Graff-Radford, 2012), a pesar de esto, consideramos que aún es necesario

contar con más estudios que apoyen los hallazgos demostrados y que además terminen

de identificar con mayor exactitud las implicaciones biomecánicas y neurofisiológicas

de la región cervical sobre el DCF, por otra parte, creemos que es importante aclarar

cómo estos datos se pueden utilizar para el diagnóstico clínico y el planteamiento

terapéutico de fisioterapia. En los últimos años el tratamiento de fisioterapia ha

adquirido un estatus importante en el tratamiento de los TCM y el DCF (Aggarwal and

Keluskar, 2012), sin embargo no contamos con evidencia científica suficiente que

demuestre la relevancia o el papel del tratamiento de fisioterapia sobre la región cervical

en los pacientes con TCM, este es uno de los motivos centrales que justifica esta tesis

49

doctoral y que nos lleva a plantear diversos objetivos entorno a esta cuestión.

La evidencia científica contemporánea nos ha llevado a la reflexión sobre las

limitaciones que presentan los estudios y los abordajes clínicos basados en modelos

mecanicistas o que toman en cuenta únicamente la dimensión sensorial-discriminativa

del DCF (Reid and Greene, 2013), en una parte de esta tesis hemos intentado contestar

interrogantes desde un punto de vista más integral utilizando un enfoque bioconductual

en el que planteamos las posibles interacciones entre el dolor y la discapacidad

craneofacial, con variables motoras, de discapacidad cervical y variables psicológicas.

El enfoque bioconductual para el tratamiento, el diagnóstico y la valoración del DCF

reconoce la importancia de los factores psicosociales, como antecedentes de dolor, los

estados emocionales en curso, el estatus cognitivo, las creencias de salud, y las

habilidades de afrontamiento, que interactúan con las alteraciones fisiológicas en la

determinación de la experiencia del dolor para los pacientes (Carlson, 2008; Shephard et

al., 2014).

50

51

OBJETIVOS

52

3. OBJETIVOS

El objetivo general de esta investigación es determinar la influencia biomecánica y

neurofisiológica de la región cervical sobre el dolor y la discapacidad craneofacial

crónica. Además se pretende identificar como determinados factores bioconductuales

influyen sobre la función craneomandibular, la discapacidad y el dolor craneofacial.

A continuación se detallan los objetivos específicos:

1- Evaluar la influencia de la postura craneocervical sobre la discapacidad

craneofacial, la dinámica mandibular y el umbral de dolor a la presión,

además se pretende analizar las diferencias de postura craneocervical entre

sujetos asintomáticos y pacientes con dolor cérvico-craneofacial (DCCF)

crónico.

Este objetivo se ha abordado en las publicaciones originales I y II:

I. La Touche R, París-Alemany A, von Piekartz H, Mannheimer JS,

Fernández-Carnero J, Rocabado M. The influence of cranio-cervical posture

on maximal mouth opening and pressure pain threshold in patients with

myofascial temporomandibular pain disorders. Clin J Pain. 2011

Jan;27(1):48-55

II. López-de-Uralde-Villanueva I, Beltran-Alacreu H, Paris-Alemany A,

Angulo-Díaz-Parreño S, La Touche R. Reliability, Standard Error, and

Minimal Detectable Change of Two Tests for Craniocervical Posture

53

Assessment in Asymptomatic Subjects and Chronic Neck/craniofacial Pain

Patients. 2014 (En revisión).

2- Determinar la influencia del dolor y la discapacidad cervical sobre la función

sensoriomotora trigeminal.

Este objetivo se ha abordado en las publicaciones originales III y V:

III. La Touche R, Fernández-de-Las-Peñas C, Fernández-Carnero J, Díaz-

Parreño S, Paris-Alemany A, Arendt-Nielsen L. Bilateral mechanical-pain

sensitivity over the trigeminal region in patients with chronic mechanical

neck pain. J Pain. 2010 Mar;11(3):256-63

V. La Touche R, Paris-Alemany A, Gil-Martínez A, Pardo-Montero J, Angulo-

Díaz-Parreño S, Fernández-Carnero J. The Influence of Neck Disability and

Pain Catastrophizing about Trigeminal Sensory-Motor System in Patients

with Headache Attributed to Temporomandibular Disorders. 2014 (En

revision)

3- Estudiar la asociación entre la discapacidad craneofacial y la discapacidad

cervical en pacientes con trastornos craneomandibulares, cefaleas y dolor

craneofacial crónico.

Este objetivo se ha abordado en las publicaciones originales II y IV:

II. López-de-Uralde-Villanueva I, Beltran-Alacreu H, Paris-Alemany A,

Angulo-Díaz-Parreño S, La Touche R. Reliability, Standard Error, and

54

Minimal Detectable Change of Two Tests for Craniocervical Posture

Assessment in Asymptomatic Subjects and Chronic Neck/craniofacial Pain

Patients. 2014 (En revisión).

IV. La Touche R, Pardo-Montero J, Gil-Martínez A, Paris-Alemany A,

Angulo-Díaz-Parreño S, Suárez-Falcón JC, Lara-Lara M, Fernández-Carnero

J. Craniofacial pain and disability inventory (CF-PDI): development and

psychometric validation of a new questionnaire. Pain Physician. 2014 Jan-

Feb;17(1):95-108.

4- Analizar la asociación de factores psicológicos como la depresión, el miedo

al movimiento y el catastrofismo ante el dolor con variable motoras, de dolor

y discapacidad cervical y craneofacial.

Este objetivo se ha abordado en las publicaciones originales III, IV y V:

III. La Touche R, Fernández-de-Las-Peñas C, Fernández-Carnero J, Díaz-

Parreño S, Paris-Alemany A, Arendt-Nielsen L. Bilateral mechanical-pain

sensitivity over the trigeminal region in patients with chronic mechanical

neck pain. J Pain. 2010 Mar;11(3):256-63

IV. La Touche R, Pardo-Montero J, Gil-Martínez A, Paris-Alemany A,

Angulo-Díaz-Parreño S, Suárez-Falcón JC, Lara-Lara M, Fernández-Carnero

J. Craniofacial pain and disability inventory (CF-PDI): development and

psychometric validation of a new questionnaire. Pain Physician. 2014 Jan-

Feb;17(1):95-108.

V. La Touche R, Paris-Alemany A, Gil-Martínez A, Pardo-Montero J, Angulo-

Díaz-Parreño S, Fernández-Carnero J. The Influence of Neck Disability and

Pain Catastrophizing about Trigeminal Sensory-Motor System in Patients

55

with Headache Attributed to Temporomandibular Disorders. 2014 (En

revision)

5- Determinar el efecto del tratamiento de fisioterapia aplicado en la región

cervical sobre la función mandibular y el dolor craneofacial.

Este objetivo se ha abordado en las publicaciones originales VI y VII:

VI. La Touche R, Fernández-de-las-Peñas C, Fernández-Carnero J,

Escalante K, Angulo-Díaz-Parreño S, Paris-Alemany A, Cleland JA. The

effects of manual therapy and exercise directed at the cervical spine on pain

and pressure pain sensitivity in patients with myofascial temporomandibular

disorders. J Oral Rehabil. 2009 Sep;36(9):644-52.

VII. La Touche R, París-Alemany A, Mannheimer JS, Angulo-Díaz-Parreño S,

Bishop MD, Lopéz-Valverde-Centeno A, von Piekartz H, Fernández-

Carnero J. Does mobilization of the upper cervical spine affect pain

sensitivity and autonomic nervous system function in patients with cervico-

craniofacial pain?: A randomized-controlled trial. Clin J Pain. 2013

Mar;29(3):205-15.

56

57

MATERIAL Y MÉTODOS

58

4. MATERIAL Y MÉTODOS

Se realizaron un total de 7 estudios con diferentes diseños metodológicos (Tabla 2). Los

pacientes fueron reclutados de dos clínicas odontológicas privadas de la Comunidad de

Madrid (Estudios VI y VII), dos clínicas privadas especializadas en dolor orofacial y

TCM (Estudios II, III, IV y V), una clínica universitaria de la Comunidad de Madrid

(Estudio I) y el Hospital Universitario La Paz de la Comunidad de Madrid (Estudio IV),

en los estudios donde se realizaron comparaciones con sujetos asintomáticos los

pacientes fueron reclutados en tres campus universitarios de la comunidad de Madrid

(Estudios II, III y V). Los procedimientos utilizados en las investigaciones de esta tesis

doctoral se realizaron bajo las directrices de la Declaración del Helsinki. Todos los

participantes de los estudios dieron su consentimiento informado por escrito antes de

comenzar con las investigaciones y estas fueron aprobadas previamente por los

respectivos comités de ética locales. Una visión general de los diseños de estudio,

características de la muestra, los métodos de recogida de datos e instrumentos de

medición se presentan en la Tabla 2.

Tabla 2. Descripción general de los diseños, características de la muestra, variables e

intervenciones.

Estudio I Estudio II Estudio III Estudio IV Estudio V Estudio VI Estudio VII

Tamaño de la

muestra

N=29

(19 mujeres; 10

hombres)

N=60 GE

(32 mujeres; 28

hombres)

N=53 GC

(30 mujeres; 23

hombres)

N=23 GE

(13 mujeres; 10

hombres)

N=23 GC

(15 mujeres; 8

hombres)

N=192

(132 mujeres; 60

hombres)

N=41 GE1

(26 mujeres; 15

hombres)

N=42 GE2

(25 mujeres; 17

hombres)

N=39 GC

(26 mujeres; 13

hombres)

N=19

(14 mujeres; 5

hombres)

N=16 GE

(10 mujeres; 5

hombres)

N=16 GC

(11 mujeres; 4

hombres)

Características de

los Participantes

Pacientes con TCM/

dolor miofascial

GE= pacientes con

TCM/ dolor miofascial

GE=dolor de

cuello crónico

Pacientes con

DCF

GE1=Cefalea

atribuida a TCM

Pacientes con

TCM/ dolor

Pacientes con

TCM/ dolor

59

crónico crónico y dolor de cuello

crónico mecánico

(DCCF)

GC=sujetos

asintomáticos

mecánico

GC=sujetos

asintomáticos

a.TCM/ dolor

miofascial crónico

b.TCM/ artralgia

c.Cefalea

atribuida por

TCM

d.Cefalea

tensional

e. Migraña

con moderada

discapacidad

cervical

GE2= Cefalea

atribuida a TCM

con leve

discapacidad

cervical

GC=Sujetos

asintomáticos

miofascial

crónico

miofascial

crónico y dolor

de cuello crónico

mecánico

(DCCF)

Media y Desviación

Típica de la Edad

34.69 ±10.83 GE=41,7±11,7

GC=38,1±10,5

GE=28±5

GC=28±6

46±13.06 GE1=44.31±10.9

GE2=40.95±12.8

9

GC=40.61±10.01

37±10 GE=33,19±9,49

GC=34,56±7,84

Diseño del Estudio Estudio prospectivo

transversal

Estudio prospectivo

transversal de fiabilidad

intra e inter-examinador

Estudio

prospectivo

transversal

Estudio

multicéntrico

prospectivo

transversal de un

diseño de un

cuestionario

Estudio

longitudinal de

casos y controles

Estudio

prospectivo de

casos

Ensayo clínico

aleatorio

controlado

Variables Somato-

sensoriales y

motoras

- UDP

- MAI

- EVA

-Postura de cabeza

-Distancia mentón-

esternón

- UDP

- END

- - UDP

-MAI

- EVA

- EVAF

-UDP

-MAI

- EVA

-UDP

-EVA

[Variable

simpáticas: CP,

FC, TC, FR]

Medidas de auto-

registro

IDC

IDD-CF

IDC

BDI

STAI

IDC

IDD-CF

HIT-6

ECD

TSK-11

IDC

HIT-6

ECD

- - IDC

- BDI

- STAI

Intervenciones - - - - - -TMO en la

región cervical

(a. Rol anterior

de la región

cervical

superior; b.

movilización

postero-anterior

de C5)

-ETCM

-TMO en la

región cervical

(movilización

antero-posterior

de la región

cervical superior)

Abreviaturas: TCM, trastornos craneomandibulares; DCF, dolor craneofacial; DCCF, dolor cérvico-craneofacial; UDP, umbral de

60

dolor a la presión; MAI, máxima apertura interincisal; EVA, escala visual analógica del dolor; END, escala numérica del dolor; GE,

grupo experimental; GC, grupo control; IDC, índice de dolor cervical; IDD-CF, inventario de dolor y discapacidad craneofacial;

BDI, inventario de depresión Beck; STAI, cuestionario de ansiedad estado-rasgo; HIT-6, cuestionario de impacto de la cefalea;

ECD; escala de catastrofismo ante el dolor; TSK-11, escala de Tampa de Kinesiofobia; EVAF, escala visual analógica de fatiga;

TMO, terapia manual ortopédica; ETCM, ejercicio terapéutico de control motor; CP, conductancia de la piel; FC, frecuencia

cardíaca; FR, frecuencia respiratoria; TC, temperatura cutánea.

4.1 Participantes

La muestra de los estudios I y VI estuvo conformada por pacientes que presentaban

TCM atribuido a dolor miofascial, esta denominación se extrae de los Criterios

diagnósticos de investigación para TCM (Dworkin and LeResche, 1992; Schiffman et

al., 2010), aunque es importante mencionar que además se establecieron otros criterios

de inclusión que se exponen a continuación: a) diagnóstico primario de dolor miofascial

de acuerdo a los Criterios diagnósticos de investigación para TCM; (Dworkin and

LeResche, 1992; Schiffman et al., 2010); b) dolor bilateral en los músculos masetero y

temporal; c) duración del dolor mayor a 6 meses; d) intensidad del dolor mayor a 30mm

según la escala visual analógica (EVA); y e) presencia de PGM en la musculatura

masticatoria. Los criterios de exclusión adoptados en estos estudios fueron los

siguientes: a) TCM atribuidos a disfunciones articulares o enfermedades degenerativos

de acuerdo a los Criterios diagnósticos de investigación para TCM (Dworkin and

LeResche, 1992; Schiffman et al., 2010); b) lesiones traumáticas como fracturas o

latigazo cervical; c) enfermedades sistémicas reumatológicas como fibromialgia y

artritis; c; dolor neuropático; y d) concomitancia con cefaleas primarias.

El estudio III contó con una muestra de pacientes con dolor de cuello crónico mecánico

inespecífico. Conceptualmente esta dolencia se define como una afectación que presenta

signos y síntomas de disfunción muscular como empeoramiento de dolor con el

mantenimiento de la postura, limitación del rango del movimiento y dolor a la palpación

de la musculatura cervical. Además los pacientes incluidos en este estudio tenían que

61

tener el dolor en un periodo superior a 6 meses. Los criterios de exclusión adoptados en

este estudio fueron los siguientes: a) dolor de cuello unilateral; b) enfermedades

reumáticas; c) latigazo cervical; d) cirugías previas de la región cervical; e) diagnóstico

de radiculopatía cervical; f) diagnóstico de TCM.

La muestra del estudio IV estuvo representada por pacientes con distintos tipos de DCF

como los siguientes, cefalea tensional, migraña, cefalea atribuida a TCM, artralgia y

dolor miofascial. Los criterios de inclusión fueron los siguientes: a) pacientes mayores

de 18 años; b) diagnóstico de dolor facial o cefalea de acuerdo a los criterios de la

Clasificación Internacional de las Cefaleas (IHS, 2013); c) diagnóstico de TCM de

acuerdo a los Criterios diagnósticos de investigación para TCM; (Dworkin and

LeResche, 1992; Schiffman et al., 2010); d) presencia de los síntomas dolorosos de más

de 6 meses; y e) buena compresión del idioma español. Los criterios de exclusión

adoptados en este estudio fueron los siguientes: a) dificultad en la compresión del

idioma español; b) deterioro cognitivo; y trastornos psiquiátricos.

El estudio V fue conformado por pacientes con cefalea atribuida a TCM de acuerdo a

los criterios de la Clasificación Internacional de las Cefaleas (IHS, 2013) y los criterios

clínicos y de investigación para TCM (Schiffman et al., 2014), además se incluyeron

los siguientes criterios de inclusión: a) presencia de dolor superior a 6 meses; b) dolor

en mandíbula, zona temporal, cara y cuello en reposo o en movimiento; c) ser mayor de

18 años; y d) discapacidad de cuello cuantificado de acuerdo al índice de discapacidad

cervical (IDC) (Andrade Ortega et al., 2010), por otra parte se debe mencionar que en

este estudio los pacientes se subdividieron de acuerdo a los niveles de discapacidad

cervical según el IDC (discapacidad leve y moderada) (Andrade Ortega et al., 2010).

Los criterios de exclusión adoptados en estos estudios fueron los siguientes: a) TCM

atribuidos a disfunciones articulares o enfermedades degenerativos de acuerdo los

62

Criterios diagnósticos de investigación para TCM (Dworkin and LeResche, 1992;

Schiffman et al., 2010); b) lesiones traumáticas como fracturas o latigazo cervical; c)

enfermedades sistémicas reumatológicas como fibromialgia y artritis; c; dolor

neuropático; d) concomitancia con cefaleas primarias; e) dolor de cuello unilateral; f)

procedimientos quirúrgicos previos en la región cervical; y g) radiculopatía cervical.

Los estudios II y VII contaron con una muestra de pacientes con DCCF crónico, estos

pacientes integran clínicamente una comorbilidad entre el dolor de cuello crónico

mecánico inespecífico (descrito en estudio III) y TCM atribuido a dolor miofascial

(descrito en los estudios I y VI). Definimos DCCF como un dolor de origen muscular

que presenta mecanismos disfuncionales como limitación del movimiento, movimientos

in-coordinados y debilidad y falta de resistencia en el cuello y la mandíbula, estos

síntomas pueden exacerbarse con posturas mantenidas generando dolor en la región

cervical y craneofacial. Los criterios de exclusión adoptados en estos estudios fueron los

mismos que en los estudios I, III y VI.

También es importante destacar que en los estudios II, III y V se realizaron

comparaciones con participantes asintomáticos.

4.2 Variables y Pruebas de Medición

En todos los estudios se registraron diversos tipos de variables sociodemográficas como

la edad, peso, altura, sexo y la duración de los síntomas, además en el estudio V se

cuantifico el nivel de estudios y el estado laboral. A parte de las variables

sociodemográficas en los estudios también se evaluaron variables somatosensoriales,

motoras y psicológicas mediante la utilización de diversos instrumentos y otras

herramientas de auto-registro especializadas. En la tabla 3 se presenta un resumen de la

variables e instrumentos de medición utilizadas en cada estudio.

Tabla 3. Variables e instrumentos utilizados en los estudios.

63

Variables Medidas Estudios

I II III IV V VI VII

Intensidad del dolor

a. Escala visual

analógica del dolor

b. Escala numérica de

dolor

X-a X-b X-a X-a X-a

Máxima apertura interincisal a. Escala therabite

b. Escala CMD

c.

X-a X-b X-a

Umbral de dolor a la presión Algométro

X X X X X

Postura craneocervical a. Distancia mentón

esternón medido con

un calibre digital.

b. Postura de cabeza

medido con CROM

X-ab

Percepción de fatiga Escala visual analógica de fatiga

X

Discapacidad cervical Índice de discapacidad cervical

X X X X X

Discapacidad craneofacial y

función mandibular

Inventario de dolor y

discapacidad craneofacial

X X

Síntomas depresivos Inventario de depresión Beck

X

Estado de ansiedad Cuestionario de ansiedad

estado/rasgo

X X

Miedo al movimiento Escala Tampa de Kinesiofobia

X

Catastrofismo ante el dolor Escala de catastrofismo ante el

dolor

X X

Impacto de la cefalea en la

vida diaria

Cuestionario de impacto de la

cefalea HIT-6

X X

64

4.2.1 Medidas de auto-registro

Catastrofismo ante el Dolor

Se utilizó la versión española de la escala de catastrofismo ante el dolor (ECD) para

evaluar el nivel de catastrofismo (García Campayo et al., 2008). La ECD está

compuesta por 13 ítems, cada ítem puntúa del 0 al 4. El rango de puntuación total se

encuentra de 0 a 52, donde puntuaciones mayores indican mayor nivel de catastrofismo.

Este instrumento presentó la misma estructura factorial original presentando tres

factores (rumiación, magnificación y desesperanza), así como unas adecuadas

propiedades psicométricas (García Campayo et al., 2008).

Miedo al Movimiento

La versión en español de la escala Tampa de kinesiofobia (TSK-11) mide el miedo al

dolor y al movimiento (Gómez-Pérez et al., 2011). La TSK-11 contiene 11 ítems en su

versión española, tras el análisis factorial se eliminaron algunos ítems de la versión

original que fueron psicométricamente pobres (Gómez-Pérez et al., 2011; Kori et al.,

1990). La puntuación total del TSK-11 se encuentra entre 11 – 44 puntos y cada ítem

presenta una escala likert que puntúa del 1 al 4 (1 = totalmente en desacuerdo, 4 =

totalmente de acuerdo). Puntuaciones más altas indican mayor miedo al movimiento y

al dolor. El TSK-11 tiene dos sub-escalas: evitación de actividad y daño, además esta

escala ha demostrado aceptables propiedades psicométricas (Gómez-Pérez et al., 2011).

Intensidad del Dolor

La intensidad del dolor se midió con la escala visual analógica del dolor (EVA). La

EVA consiste en una línea de 100 mm, en el que el lado izquierdo representa "ningún

dolor" y el lado derecho "el peor dolor imaginable". Los pacientes colocan una marca

donde se sentían que representan la intensidad del dolor. Se ha comprobado que este

instrumento tiene una buena fiabilidad (Bijur et al., 2001).

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En la medición de la intensidad del dolor también se utilizó la escala numérica del dolor

(END), esta escala presenta 11 puntos posibles representados en números del 0 (sin

dolor) al 10 (máximo dolor). Se ha demostrado que END presenta una buena fiabilidad

y validez en pacientes crónicos (Jensen and McFarland, 1993; Jensen et al., 1999).

Percepción de Fatiga

La escala visual analógica de fatiga (EVAF) se utilizó para cuantificar la fatiga

percibida. La EVAF consiste en una línea vertical de 100 mm en la que la parte inferior

representa "ninguna fatiga" (0 mm), y la parte superior representa la "fatiga máxima"

(100 mm). El investigador registra el resultado en mm. Se ha comprobado que este

instrumento tiene una buena fiabilidad (Tseng et al., 2010).

Discapacidad Cervical

La versión española del índice de discapacidad cervical (IDC) es instrumento utilizado

para evaluar la discapacidad percibida en relación a la dolencia en el cuello (Andrade

Ortega et al., 2010; Vernon and Mior, 1991). Este cuestionario consta de 10 ítems, con

6 posibles respuestas que representa 6 niveles de capacidad funcional, que van desde 0

(sin discapacidad) a 5 (discapacidad total) puntos. Las puntuaciones más altas indican

mayor discapacidad percibida. El IDC ha demostrado propiedades psicométricas

aceptables (Andrade Ortega et al., 2010).

Impacto de la Cefalea en la Vida Diaria

La versión española del HIT-6 (Bjorner et al., 2003; Gandek et al., 2003) consiste en un

cuestionario de seis ítems que evalúa la gravedad y el impacto del dolor de cabeza en la

vida del paciente. Los resultados de HIT-6 están estratificados en cuatro clases basadas

en el grado de impacto: poco o ningún impacto (HIT-6 puntuación de: 36-49), impacto

moderado (HIT-6 puntuación de: 50-55), impacto sustancial (HIT-6 puntuación de: 56-

59), y el impacto severo (HIT-6 puntuación de: 60-78) (Bjorner et al., 2003). El HIT-6

66

ha demostrado propiedades psicométricas aceptables (Martin et al., 2004).

Síntomas de Ansiedad

La versión española del cuestionario de ansiedad estado-rasgo (STAI) es una medida de

auto-informe de 40 ítems, diseñado para evaluar los síntomas de la ansiedad (Spielberg

and Lushene, 1982). Consta de 2 escalas independientes, una escala de ansiedad estado

y una escala de ansiedad rasgo, con 20 puntos cada uno, lo que resulta en una

puntuación entre 20 y 80. Superiores puntuaciones indican un mayor nivel de ansiedad.

Las escalas de estado y rasgo evalúan la ansiedad como un estado emocional actual y

como un rasgo de la personalidad, respectivamente. El STAI ha demostrado

propiedades psicométricas aceptables en su versión en español (Spielberg and Lushene,

1982).

Síntomas Depresivos

Los síntomas depresivos se evaluaron con el Inventario de Depresión Beck (BDI-II),

este instrumento de auto-registro evalúa síntomas afectivos, cognitivos y somáticos de

depresión. Se ha comprobado en estudios con población general y clínica que el BDI-II

presenta adecuadas propiedades psicométricas (Penley et al., 2003; Wiebe and Penley,

2005)

4.2.2 Instrumentos de medición

Máxima Apertura Interincisal

La máxima apertura interincisal (MAI) es la capacidad de abrir la boca tan amplio

como se pueda sin dolor. Esta distancia se mide en milímetros entre el incisivo superior

y el incisivo inferior. La MAI se midió con la escala TheraBite (Model CPT 95851;

Atos Medical AB; Sweden) y con la escala craneomandibular (Escala CMD. Patente.

No. ES 1075174 U, INDCRAN: 2011. INDCRAN, Madrid, Spain) (Figura 12). El

procedimiento para medir la MAI ha demostrado una buena fiabilidad inter-evaluador

67

(ICC = 0,95 - 0,96) (Beltran-Alacreu et al., 2014).

Figura 12. Medición de máxima apertura interincisal con la escala CMD.

Umbral de Dolor a la Presión

Un algómetro digital (FDX 25, Wagner Instruments, Greenwich, CT, EE.UU.),

compuesto por un cabezal de goma (1 cm2) unido a un manómetro, se utilizó para medir

UDPs (Figura 13). La presión ejercida se mide en kilogramos (kg); por lo tanto, los

UDPs se expresaron en kg /cm2. El protocolo utilizado fue una secuencia de 3

mediciones, con un intervalo de 30 segundos entre cada una de las mediciones. Un

promedio de las 3 mediciones se calculó para obtener un único valor para cada uno de

los puntos medidos en cada una de las evaluaciones. Los UDPs se evaluaron en varios

puntos de la región craneofacial y craneomandibular (Figura 14). El dispositivo se

aplica perpendicular a la piel. Se pidió a los pacientes que levantasen la mano en el

momento en que la presión comenzara a cambiar a una sensación de dolor, y en ese

momento el evaluador dejó de aplicar presión. La presión aplicada en la prueba se

aumentó gradualmente a una velocidad de aproximadamente 1 kg/s. Este procedimiento

de algometría tiene alta fiabilidad intra-evaluador (ICC = 0,94 a 0,97) para la medición

68

de los UDPs (Walton et al., 2011).

Figura 13. Medición del umbral de dolor a la presión con el algómetro digital.

Figura 14. Puntos de áreas trigeminales y cervicales en donde se midieron los umbrales de dolor a la presión en los

diferentes estudios.

Postura Craneocervical

Utilizamos el dispositivo CROM para medir la postura de cabeza (PC). Este dispositivo

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tiene tres partes: a) una estructura plástica con forma de gafas; b) tres inclinómetros,

uno para cada plano de movimiento; y c) un brazo plástico para medir la de cabeza

hacia adelante y un localizador de vértebra (Figura 15). La medición de la PC está

graduada en el instrumento en 0,5 cm, que indican la distancia horizontal entre el puente

de la nariz y el localizador de vértebras. El localizador de vértebras tiene un nivel de

burbuja en la parte superior para ayudar a la colocación exacta. Los inclinómetros no se

utilizaron debido a los movimientos del cuello no se evaluaron.

Figura 15. Medición de la postura craneocervical

Para medir la distancia mentón-esternón (DME) se utilizó un calibre digital. El

dispositivo está hecho de plástico con una pantalla LCD de 5 dígitos y se puede medir

en pulgadas o en milímetros (mm) con un rango de 0,01 mm a 150 mm.

El evaluador explica en primer lugar que la medición se llevará a cabo mientras está

70

acostado en una camilla. En este momento, el evaluador mostró los calibradores

digitales al tema y dijo: "Usted sentirá que el instrumento contactará con su esternón y

en la barbilla; en ese momento no se debe mover”. Una vez en su lugar, la medición fue

tomada de la escotadura yugular del esternón a la protuberancia de la barbilla (Figura

16). La medida fue tomada en dos ocasiones.

Figura 16. Medición de la distancia mentón-esternón.

4.3 Resumen de los Procedimientos

Estudio I

Se registraron inicialmente las variables sociodemográficas y la intensidad del dolor y

después se procedió a medir los UDPs y la MAI en tres posturas craneocervicales

inducidas experimentalmente (posición neutra craneocervical, retracción craneocervical

y protracción craneocervical)

Estudio II

Se seleccionaron a los pacientes y los sujetos asintomáticos del grupo control, después

se registraron las variables sociodemográficas y las medidas de auto-registro (IDC y

IDD-CF) y finalmente se realizaron las mediciones de la postura craneocervical.

71

Estudio III

Se registraron las variables sociodemográficas y las medidas de auto-registro y después

se procedió a realizar mediciones del UDP en los puntos trigeminales.

Estudio IV

Se seleccionaron a los pacientes y después se procedió a registrar las variables

sociodemográficas y una batería de medidas de auto-registro de variables psicológicas,

dolor y discapacidad.

Estudio V

Una vez seleccionados los pacientes y el grupo control se procedió al registro de

variables sociodemográficas y las medidas de auto-registro, después de esa fase se

realizó el test masticatorio de provocación durante 6 minutos en donde se evaluó la

fatiga y la intensidad del dolor. Al finalizar el test masticatorio de provocación se

procedió a realizar las mediciones de la MAI y los UDPs.

Estudio VI

Se realizó un tratamiento sobre los pacientes seleccionados durante 10 sesiones, este

tratamiento estaba enfocado a la región cervical y específicamente se utilizó un

protocolo de estabilización cervical y un tratamiento de terapia manual sobre la región

cervical, además se realizaron mediciones de variables somatosensoriales y motoras

pre-intervención, post-intervención y tres meses después.

Estudio VII

Se seleccionaron un grupo de pacientes que se subdividen aleatoriamente en dos grupos,

un grupo recibe un tratamiento placebo y el otro un tratamiento manual sobre la región

cervical superior. Se realizaron mediciones de variables somatosensoriales y del sistema

nervioso simpático pre-intervención y post-intervención.

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4.4 Análisis Estadístico

En el análisis de datos se ha utilizado estadística descriptiva para mostrar los datos de

las variables continuas que se presentan como media ± desviación típica (DT), intervalo

de confianza del 95% (IC) y frecuencia relativa (porcentaje). Prueba de Chi-cuadrado,

se utilizó para comparar las diferencian entre las variables categóricas (nominales). Se

realizo la prueba de Kolmogorov Smirnov para comprobar la normalidad.

Se utilizó la t de Student para la comparar las variables continuas entre los dos grupos.

Cuando las comparaciones se realizaron con más de dos grupos o se intentó analizar la

interacción con otras variables se aplicó una ANOVA de una, dos o tres vías según

procediese, seguido de un test post hoc de Bonferroni para analizar las comparaciones

múltiples. En uno de los estudios se realizó un análisis con una ANCOVA de dos vías

para identificar múltiples interacciones entre variables.

Se calculó el tamaño del efecto (d de Cohen) para las variables principales estudiadas.

De acuerdo con el método de Cohen, la magnitud del efecto fue considerado como

pequeño (0,20 a 0,49), medio (0,50 a 0,79), y grande (0,8) (Cohen, 1988).

La estructura factorial se analizó mediante un análisis factorial exploratorio (es decir,

análisis de componentes principales, ACP) con la rotación Oblimin. El número de

factores para la extracción se basa en el criterio de valor propio de Kaiser (valor propio

≥1) y la evaluación del gráfico de sedimentación (Ferguson and Cox, 1993). La calidad

de los modelos de análisis factorial se evaluó mediante la prueba de Bartlett para la

esfericidad y la prueba de Kaiser-Meyer-Olkin (KMO). Prueba de Bartlett es una

medida de la probabilidad de que la matriz de correlación inicial es una matriz de

identidad y debe ser <0,05 (Bartlett, 1954). La prueba de KMO mide el grado de

multicolinealidad y varía entre 0 y 1 (debe ser mayor que 0,50-0,60) (Kaiser, 1974).

El efecto suelo-techo se midieron mediante el cálculo del porcentaje de pacientes que

73

indican los puntajes mínimos y máximos posibles en los cuestionarios. El efecto suelo-

techo se considera que está presente si más del 15% de los encuestados logró el mayor o

menor puntuación total posible (Terwee et al., 2007).

La fiabilidad intra e inter-evaluador se analizo mediante coeficiente de correlación intra-

clase (CCI). Niveles de fiabilidad se definieron en base a la siguiente clasificación:

buena fiabilidad: ICC ≥ 0,75; fiabilidad moderada: ICC ≥ 0,50 y <0,75; y escasa

fiabilidad: ICC <0,50 (Portney LG, 2009).

El error de medición se expresa como un error estándar de medición (EEM), que se

calcula como 𝐷𝑇 × √1 − 𝐶𝐶𝐼, donde DT es la de los valores de todos los participantes,

y el CCI es el coeficiente de fiabilidad (Weir, 2005). El error de medición es el error

sistemático y aleatorio de la puntuación de un paciente que no es atribuible a los

cambios reales en el constructo a medir (Mokkink et al., 2010). Capacidad de respuesta

se evaluó utilizando el mínimo cambio detectable (MCD). MCD expresa el cambio

mínimo necesario para identificar el 90% de confianza de que el cambio observado

entre las dos medidas refleja un cambio real y no un error de medición (Haley and

Fragala-Pinkham, 2006). Se calcula como 𝐸𝐸𝑀 × √2 × 1,96 (Haley and Fragala-

Pinkham, 2006).

La asociación entre las variables se determinó mediante el coeficiente de correlación de

Pearson. Un coeficiente de correlación de Pearson mayor que 0,60 indica una fuerte

correlación, un valor entre 0,30 y 0,60 indica una correlación moderada, y uno por

debajo de 0,30 indica una correlación baja o muy baja (Hinkle et al., 1988). También se

utilizó en uno de los estudios el coeficiente de correlación de Spearman.

Se realizó un análisis de regresión lineal múltiple para estimar la fuerza de las

asociaciones entre los resultados variables primarias (variables criterio) con las

secundarias (variables predictoras). Se calcularon los factores de inflación de varianza

74

(FIV) para determinar si existían problemas de multicolinealidad en cualquiera de los

modelos analizados.

La fuerza de asociación se examinó utilizando los coeficientes de regresión (β), los

valores de P y r2 ajustado. Coeficientes beta estandarizados fueron reportados para cada

variable de predicción incluida en los modelos finales reducidas para permitir una

comparación directa entre las variables predictoras en el modelo de regresión y la

variable criterio que se está estudiando. Para el análisis de regresión, se utilizó la regla

de 10 casos por variable con el fin de obtener estimaciones razonablemente estables de

coeficientes de regresión (Peduzzi et al., 1996).

En la tabla 4 se presenta un resumen de los test estadísticos utilizados en cada uno de

los estudios.

El programa estadístico para Ciencias Sociales (SPSS 21, SPSS Inc., Chicago, IL

EE.UU.) se utilizó para el análisis estadístico. El nivel de significación para todas las

pruebas se estableció a un nivel de P <0,05.

75

Tabla 4. En esta tabla se puede observar las pruebas estadísticas utilizadas en cada uno

de los estudios.

Pruebas estadísticas Estudios

I II III IV V VI VII

- Análisis descriptivo X X X X X X X

- Pruebas de normalidad (test de Kolmogorov Smirnov) X X X X X X X

- t de student X X X

- ANOVA X X X X X

- ANCOVA X

- Calculo del tamaño del efecto (d) X X

- Análisis factorial exploratorio X

- Efecto suelo-techo X

- Coeficiente de correlación intra-clase X X X

- Error estándar de medición X X X X

- Mínimo cambio detectable X X

- Coeficiente de correlación de Pearson X X X

- Coeficiente de correlación de Spearman X

- Análisis de regresión lineal múltiple X X

76

77

RESULTADOS

78

5. RESULTADOS

5.1 Estudio I

La Touche R, París-Alemany A, von Piekartz H, Mannheimer JS, Fernández-Carnero J,

Rocabado M. The influence of cranio-cervical posture on maximal mouth opening and

pressure pain threshold in patients with myofascial temporomandibular pain disorders. Clin

J Pain. 2011 Jan;27(1):48-55.

Objetivo del estudio

El objetivo de este estudio fue evaluar la influencia de la postura craneocervical sobre la

MAI y el UDP en pacientes TCM atribuidos a dolor miofascial.

Resultados

Las comparaciones indicaron diferencias significativas en los UDPs de los 3 puntos

musculares con inervación trigeminal [masetero (M1 y M2) y temporal anterior (T1)] entre

las 3 posturas de cabeza [M1 (F = 117.78, p <0,001), M2 (F = 129.04, p <0,001), y T1 (F =

195,44, p <0,001)]. También hubo diferencias significativas en la MAI medidas en las 3

posturas de cabeza (F = 208.06, p <0,001). La fiabilidad intra-evaluador en base a pruebas

realizadas día a día fue buena, presentando un coeficiente de correlación intra-clase en los

rangos de 0,89-0,94 y 0,92 hasta 0,94 para UDP y la MAI, respectivamente, entre las

diferentes posturas craneocervicales.

Conclusiones

Los resultados de este estudio muestran que la inducción experimental de diferentes

posturas craneocervicales influye en los valores de la MAI y los UDPS de la ATM y

músculos de la masticación que reciben inervación motora y sensitiva por el nervio

trigémino. Nuestros resultados proporcionan información que respalda la relación

biomecánica entre la región craneocervical y la dinámica de la ATM, así como las

modificaciones en el procesamiento nociceptivo trigeminal en diferentes posturas

craneocervicale.

The Influence of Cranio-cervical Posture on Maximal MouthOpening and Pressure Pain Threshold in Patients With

Myofascial Temporomandibular Pain Disorders

Roy La Touche, PT, MSc,*w z Alba Parıs-Alemany, PT, MSc,w Harry von Piekartz, PT, PhD,yJeffrey S. Mannheimer, PT, PhD, CCTT,J Josue Fernandez-Carnero, PT, PhD,w z

and Mariano Rocabado, PT, DPT#

Objective: The aim of this study was to assess the influence ofcranio-cervical posture on the maximal mouth opening (MMO)and pressure pain threshold (PPT) in patients with myofascialtemporomandibular pain disorders.

Materials and Methods: A total of 29 patients (19 females and 10males) with myofascial temporomandibular pain disorders, aged19 to 59 years participated in the study (mean years±SD;34.69±10.83 y). MMO and the PPT (on the right side) of patientsin neutral, retracted, and forward head postures were measured. A1-way repeated measures analysis of variance followed by 3 pair-wise comparisons were used to determine differences.

Results: Comparisons indicated significant differences in PPT at 3points within the trigeminal innervated musculature [masseter (M1and M2) and anterior temporalis (T1)] among the 3 head postures[M1 (F=117.78; P<0.001), M2 (F=129.04; P<0.001), and T1(F=195.44; P<0.001)]. There were also significant differencesin MMO among the 3 head postures (F=208.06; P<0.001). Theintrarater reliability on a given day-to-day basis was good with theinterclass correlation coefficient ranging from 0.89 to 0.94 and 0.92to 0.94 for PPT and MMO, respectively, among the different headpostures.

Conclusions: The results of this study shows that the experimentalinduction of different cranio-cervical postures influences the MMOand PPT values of the temporomandibular joint and musclesof mastication that receive motor and sensory innervation by thetrigeminal nerve. Our results provide data that supports thebiomechanical relationship between the cranio-cervical region andthe dynamics of the temporomandibular joint, as well as trigeminalnociceptive processing in different cranio-cervical postures.

Key Words: temporomandibular disorders, myofascial pain, posture,

cervical spine, orofacial pain

(Clin J Pain 2011;27:48–55)

Pain in the masticatory muscles and arthralgia of thetemporomandibular joints are some of the features of

the term temporomandibular disorders (TMD) that havebeen categorized into 3 major groups by the ResearchDiagnostic Criteria (RDC) that is most commonly used toclassify symptomatology of TMD.1,2 Myofascial pain, discdisplacements, and arthralgia/osteoarthrosis constitute thisdiagnostic grouping. TMD of myofascial origin is categor-ized by episodic pain with periods of exacerbation andremission.3 Nevertheless, some patients may suffer persis-tent pain, and their prognosis is determined by psycho-metric evaluation (Axis II of the RDC/TMD). Myofascialpain is frequently associated with the presence of triggerpoints (TrPs) and the discomfort is considered to representa taut and painful disturbance of muscle and fascia that canbe local or referred with tenderness and pressure uponpalpation.4,5

It is well known that cervical spine tissues can referpain to the head and orofacial region.6,7 Comorbidity ofTMD and cervical spine disorders is quite common andconsists of a composite of functional limitation, pain,tender points, and hyperalgesia indigenous to the upperquarter.8 Some authors believe that neuronal plasticity,local interactions, and general predisposing musculoskeletalfactors might be behind this coexistence, but the relation-ship between the orofacial and cervical region is stronglyrooted by dense neuromusculoskeletal and neurophysiolo-gic connections.8,9 The trigeminal brainstem sensorynuclear complex located within the suboccipital spine,represents the prime neurophysiologic region where theconvergence of sensory information from the first 3 cervicalspinal nerves converge with trigeminal afferents, whereassome fibers descend to lower segmental levels.10–15 There-fore ascending cervicogenic and descending trigeminalreferral is mediated through the trigeminal brainstemsensory nuclear complex.15,16 The convergence of differenttypes of afferent and efferent neurotransmission on thetrigeminal nucleus together with the good evidence forneuronal plasticity that is known to occur in chronic painstates17–19 may account for the concomitant pain anddysfunction of the cervical, temporomandibular joints, andmasticatory system because of changes in head posture.17,20

Forward positioning of the head may contribute toor occur concomitantly with TMD,21,22 cervicogenic head-ache,23 and tension-type headache.24 Some authors supportthe connection between TMD and head posture,20–22,25

whereas others do not.26,27 The mechanism whereby headposture might be related to craniofacial signs and symptomsis unclear. The neuroplastic changes associated withCopyright r 2010 by Lippincott Williams & Wilkins

Received for publication April 7, 2010; revised June 9, 2010; acceptedJune 14, 2010.

From the *School of Health Science, Department of Physical Therapy;wGroup for Musculoskeletal Pain and Motor Control ClinicalResearch; zOrofacial Pain Unit of the Policlınica Universitaria,Universidad Europea de Madrid, Villaviciosa de Odon; zDepart-ment of Physical Therapy, Occupational Therapy, Rehabilitationand Physical Medicine, Universidad Rey Juan Carlos, Alcorcon,Madrid, Spain; yFaculty of Business, Management and SocialScience, University of Applied Science Osnabruck, Osnabruck,Germany; JProgram in Physical Therapy, Columbia University,New York, NY; and #Faculty of Rehabilitation Science, UniversidadAndres Bello, Santiago, Chile.

Reprints: Roy La Touche, PT, MSc, Facultad de Ciencias de la Salud/Departamento de Fisioterapia, Universidad Europea de Madrid,C/Tajo s/n, 28670 Villaviciosa de Odon, Madrid, Espana (e-mail:[email protected]).

ORIGINAL ARTICLE

48 | www.clinicalpain.com Clin J Pain � Volume 27, Number 1, January 2011

convergent afferent inputs mentioned above might play aconsiderable role. Further, it is noteworthy that changes inhead posture can alter the position of the mandible28,29 andthe activity of the masticatory muscles.30 Higbie et al31

demonstrated increased mouth opening in a forward headposition as compared with the neutral or retracted headposition, in healthy individuals. Furthermore, postural anddeep cervical flexor training as well as cervical manualtherapy have been shown to improve TMD signs andsymptoms.21,32,33

Although Visscher et al27 did obtain a wide rangeof head postures in both patients with craniomandibulardysfunction and healthy ones, their results data did notsupport the suggestion that craniomandibular dysfunctionis related to abnormal head posture, even in the presence ofcervical spine dysfunction. On the basis of their findings,Olivo et al34 found that the association between head andcervical posture with intra-articular or muscular TMD isnot clear.

Given the conflict in the literature as to whether thereis an association between head posture might be relatedto craniofacial signs and symptoms; the aim of this study isto assess the influence of cranio-cervical posture on themaximal mouth opening (MMO) and pressure pain thresh-old (PPT) of the trigeminal region in patients withmyofascial TMD pain.

MATERIALS AND METHODS

PatientsTMD patients were recruited from November 2008 to

March 2009 and were referred from 3 private dental clinicsin Madrid, Spain. Patients were selected if they met all ofthe following criteria: (1) a primary diagnosis of myofascialpain as defined by the Axis I, category Ia and Ib (ie,myofascial pain with or without limited opening), of theRDC/TMD,2 (2) bilateral pain involving the masseter andtemporalis, (3) a duration of pain of at least 6 months, (4) apain intensity corresponding to a weekly average of at least30mm on a 100mm visual analog scale, and (5) a presenceof bilateral TrPs in both the masseter and temporalismuscles diagnosed following the criteria described bySimons et al.35 TrPs were diagnosed according to thefollowing criteria: (1) presence of a palpable taut band inskeletal muscle, (2) presence of a hypersensitive tender spotwithin the taut band, (3) local twitch response elicited bythe snapping palpation of the taut band, and (4) reproduc-tion of referred pain in response to TrP compression. Thesecriteria have shown good interrater reliability (k) rangingfrom 0.84 to 0.88.36

All patients included in the study were examined byan experienced TMD specialist, with more than 4 years ofclinical practice, from the University Center of ClinicalResearch of the Cranial-Cervical-Mandibular System,Faculty of Medicine, San Pablo CEU University.

Patients were excluded if they presented any signs,symptoms, or history of the following diseases: (1) intra-articular disc displacement, ostheoarthrosis, or arthritis ofthe temporomandibular joint (TMJ), according to cate-gories II and III of the RDC/TMD2; (2) history of trauma-tic injuries (eg, contusion, fracture, and whiplash injury);(3) systemic diseases: (fibromyalgia, systemic lupus erythe-matosus, and psoriatic arthritis); (4) neurologic disorders(eg, trigeminal neuralgia); (5) concomitant diagnosis ofany primary headache (tension type or migraine); and

(6) current or recent therapy for the disorder within theprevious 2 months.

Each participant received a thorough explanationabout the content and purpose of the treatment beforesigning an informed consent relative to the procedures. Allprocedures were approved by the local ethics committee inaccordance with the Helsinki Declaration.

Experimental ProceduresEach patient with myofascial TMD pain were

subjected to a protocol for assessing maximum activeopening and PPT in 3 different cranio-cervical postures asfollows and illustrated in Figure 1:

Neutral head posture (NHP) defined as the positionassumed when the individual was told to sit and maintaintheir head in a vertical position. This position was furtherconfirmed as neutral if the tragus of the ear and acromionwere bisected by a plumb line.Forward head posture (FHP) defined as anteriortranslation of the head with or without lower cervicalflexion. It is claimed that the FHP is associated with anincrease in upper-cervical extension.37,38

Retracted head posture (RHP) defined as posteriortranslation of the head over the trunk associated withupper cranio-cervical flexion and extension of the low-to-mid cervical spine.39

All measurements were conducted by 2 physiothera-pists who had experience in research evaluations, one incharge of placing the patient in the measurement positionand the other responsible for the recording of MMOand PPT. All patients underwent 3 measurements of eachvariable in the 3 head positions on 3 different days. Awashout period of 24 hours was incorporated between eachmeasurement day.

A software program was used to obtain blockedrandomization of the size to arrange the order of measure-ment (GraphPad Software, Inc, CA). An average of 15minutes per patient was required to perform the random-ized measurements of MMO and PPT in NHP, FHP, andRHP. Every patient maintained their head in each positionfor 5 seconds during these measurements.

Establishment of the Measurement PositionsA plumb line hanging from the ceiling and a cervical

range of motion (CROM) device (Performance AttainmentAssociates, 958 Lydia DR, Roseville, MN) was usedto determine each patients’ cranio-cervical postures. TheCROM instrument measured the degree of FHP or RHPand the active cervical range of movement. The CROMinstrument uses a clear plastic eyeglass-like frame with 2dial-angle meters, a head arm that includes a vertebrallocator and bubble leveller (Fig. 2). The head arm wasplaced in the frame of the CROM horizontally to the head.The base of the vertebral locator was placed on the C-7spinous process so that the bubble leveller was centeredwithin the 2 vertical lines on the dial with the examinerstanding to the left of the patient to read the sagittal planemeter (Fig. 2). When the sagittal plane meter read zero andwith the head arm horizontal (parallel to the floor), theintersection of the head arm and vertebral locator wasrecorded as the head posture measurement in centimeters.Excellent reliability has been showed for the measurementof FHP using the CROM instrument [intrarater reliability

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(interclass correlation coefficient, ICC=0.93) and interraterreliability (ICC=0.83)].40

Cranio-cervical postures were measured in the sittingposition attained by instructing the patient to sit in acomfortable upright position with the thoracic spine incontact with the back of the chair. The feet were positionedflat on the floor with knees and hips at 90 degrees and armsresting freely alongside.

Forward and retruded head postures were achieved byinitial placement into the NHP using the plumb line asexplained earlier. Movement into a FHP was performedwith the CROM after verbal instruction to position thehead forward in a horizontal plane allowing the tragus to bealigned to a target plumb line placed 8 cm anterior to thebase plumb line. Each patient was instructed to continuallymaintain their eyes at the same horizontal level while being

told to “slide your jaw and head forward until the examinertells you to stop” upon reaching the target plum line (Fig. 1).

Movement into a RHP was also performed with theCROM by instruction to position the head posteriorly ina horizontal plane allowing the tragus to be aligned to thetarget plumb line placed 4 cm posterior to the base plumbline. Each patient was instructed to continually maintaintheir eyes at the same horizontal level while being told to“slide your jaw and head backward until the examiner tellsyou to stop” upon reaching the target plum line (Fig. 1).

Measurement of MMOThe MMO was measured with a TheraBite range of

motion scale (Model CPT 95851; Atos Medical AB;Sweden) (Fig. 2). The patients were told to: “Open yourmouth as wide as possible without causing pain or

FIGURE 1. Measurement of maximum mouth opening with TheraBite, controlling the head position with the CROM device and plumline: A, retracted head posture. B, Forward head position. Measurement of pressure pain thresholds at masseter and temporalis muscleswith a mechanical algometer, controlling head position with CROM device: C, forward head position. D, Neutral head position. CROMindicates cervical range of motion.

FIGURE 2. Description and representation of measurement devices: TheraBite scale (A); CROM device: plastic eyeglass-like frame with 2dial-angle meters (B), head arm (C), and vertebral locator and bubble leveller (D).

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discomfort.” Interincisal distance was then recorded byplacing one end of the TheraBite scale against the incisaledge of one central mandibular incisor with the other endagainst the incisal edge of the opposing maxillary centralincisor (Fig. 1). Earlier research has shown excellentintrarater (0.92 to 0.97) and interrater (0.92 to 0.93)reliability when assessing MMO in 3 different cranio-cervical positions.33

Measurement of PPTThe PPT was defined as the amount of pressure that

a patient would initially perceive as painful.41 PPTs havebeen assessed with a mechanical pressure algometer (PainDiagnosis and Treatment Inc, Great Neck, NY) whichwas used in this study. The instrument consists of a 1 cmdiameter hard rubber tip, attached to the plunger of apressure (force) gauge. The dial of the gauge is calibratedin kg/cm2 and the range of the algometer is 0 to 10 kgwith 0.1 kg divisions. Earlier research has shown that thereliability of pressure algometry is as high as [ICC=0.91(95% confidence interval, CI 0.82-0.97)].42

Before the evaluation, 3 specific cutaneous regionsoverlying the masseter and temporalis were marked with apencil. Algometric measurements were then performed at 2masseteric sites and 1 temporalis site as delineated by:masseter muscle (M1 and M2) and temporalis muscle (T1)(Fig. 3). During the measurements, the algometer was heldperpendicular to the skin (Fig. 1) and the patient was toldto immediately alert the assessor when the pressure turned

into a sensation of pain, at which point the mechanicalstimulus was stopped. Three consecutive measurementswere obtained by the same assessor, with a pause of 30seconds between measurements. The mean of 3 measureswas calculated and used for analysis. All measurementswere performed on the right side because of the disturbanceinduced by the dial-angle meter of the CROM at the leftside (Fig. 1).

Statistical AnalysisData are expressed as mean, SD, and 95% CI. The

Kolmogorov-Smirnov test was used to determine the normaldistribution of the variables (P<0.05). A 1-way repeatedmeasures analysis of variance (ANOVA) followed by 3 pair-wise comparisons was used to determine differences in MMOand PPT among the 3 different head postures. Post-hoccomparisons were conducted with the Bonferroni test.Intrarater reliability of repeated measures was determinedfrom the ICC by means of the 2-way model, the 95% CI,and the standard error of the measurement (SEM). Thestrength of the ICC was interpreted as <0.50=poor; 0.50<0.75=moderate; 0.75 <0.90=good; and >0.90=excel-lent. The ICC and SEM convey different information aboutreliability of a measure. The analysis was conducted at 95%CI and P value less than 0.05 was considered to bestatistically significant. Statistical analyses were carried outusing the Statistical Package for Social Sciences, Version 15.0(SPSS, Chicago, IL).

RESULTSThe general demographic data and pain-related data

are shown in Table 1. Figure 4 represents the study samplesize and the reasons for exclusion of the patients. All thepatients who started the study were analyzed, and therewere no dropouts or losses.

FIGURE 3. Pressure pain threshold measurement sites attemporalis and masseter muscles. T1: located 3 cm above theline between the lateral edge of the eye and the anterior part ofthe helix on the anterior fibers of temporalis muscle. M1: located2.5 cm anterior to the tragus and 1.5 cm inferiorly. M2: located1 cm superior and 2 cm anterior from the mandibular angle.

TABLE 1. General Data of the Analyzed Patients

Demographic and Clinical Data Mean SD

Age (y) 34.69 10.83Weight (kg) 68.83 7.87Height (cm) 166.72 8.52Duration of pain (mo) 9 2.44VAS (mm) 39.7 1.78

SD indicates standard deviation; VAS, visual analog scale.

51 patients screened

Causes for exclusion

29 patients included(19 females)(10 males)

22 patients excluded

29 patients analysed0 losses or dropouts

FIGURE 4. Flow diagram of the patients in this study. RDCindicates Research Diagnostic Criteria; TMD, temporomandibulardisorders.

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MMOThe intrarater reliability on a given day-to-day basis

was excellent with ICC ranging from 0.92 to 0.94 for MMOamong the 3 cranio-cervical postures. Reliability coeffi-cients, ICC associated 95% CI, and SEM values for MMOare presented in Table 2. A 1-way repeated measuresANOVA followed by 3 pair-wise comparisons indicated asignificant difference in MMO among the 3 cranio-cervicalpostures (F=208.06; P<0.001). Post-hoc results revealedthat the MMO was higher in FHP compared with the NHP(difference between means=2.81 cm) and the RHP (differ-ence between means=6.81 cm) (P<0.001). Furthermore,the MMO of the NHP was higher when compared with theRHP (difference between means=4cm) (P<0.001). Table 2summarizes MMO assessed among the 3 cranio-cervicalpostures.

PPTThe intrarater reliability on a given day-to-day basis

was good with ICC ranging from 0.89 to 0.94 for PPTamong the 3 cranio-cervical postures. Reliability coeffi-cients, ICC associated 95% CI, and SEM values for PPTare presented in Table 3. A 1-way repeated measuresANOVA followed by 3 pair-wise comparisons indicated asignificant difference in PPT of the 3 measurement pointsamong the 3 cranio-cervical postures [M1 (F=117.78;P<0.001); M2 (F=129.04; P<0.001); and T1 (F=195.44;P<0.001)]. Results of the post-hoc test for multiplecomparisons between PPT among the 3 cranio-cervicalpostures are presented in Figure 5. Table 4 summarizes thePPT among the 3 head postures.

DISCUSSIONThe experimental posture model used in this study

showed that MMO and PPT values become modifiedamong the induced cranio-cervical postures. MMO andPPT values in the NHP were between those obtained in theFHP and RHP. We observed the highest MMO in the FHP

and the lowest in the RHP. However, the PPT values didnot correspond with those obtained for the MMO as theywere lower in the FHP. In addition, the intrarater reliabilityof the model used to assess MMO and PPT was good.

MMOThe results obtained in the assessment of MMO in

the 3 different postures (NHP 40.8mm, RHP 36.8mm, andFHP 43.7mm) correspond with the results obtained byHigbie et al31 with healthy individuals (NHP 41.5mm,RHP 36.2mm, and FHP 44.5mm). The coincident valuessupport the existence of a functional integration betweenthe anatomic and biomechanical relationship of thetemporomandibular and cranio-cervical regions that hasbeen tested earlier by static and dynamic means. Erikssonet al43 and Zafar et al44 have demonstrated parallel andcoordinated head-neck movements during concomitant jawmovements. Haggman-Henrikson et al45 found a limitationof jaw movement and a shorter duration of jaw opening/closing cycles when experimental fixation of the neck wasperformed.

The variations of MMO in different head positions canbe explained by different actions of the masticatory andcervical muscles as well as intra-articular variations ofcondylar motion. Visscher et al46 found small changes inthe intra-articular distance of the TMJ when it wasmeasured in different cranio-cervical postures. RecentlyOhmure et al47 observed posterior condylar positioning inthe presence of a forced FHP, which may be a predisposingfactor toward intrinsic TMJ disorders resulting fromcumulative muscular and ligamental microtrauma ofabnormal postural origin.48 However, this factor has yetto be supported by clinical research.49,50 Olmos, et al51

demonstrated that after a TMJ treatment in symptomatic

TABLE 2. Descriptive and Intrarater Reliability Statistics forMeasurements of MMO in Patients With Myofascial TMD Pain(N=29) in the 3 Cranio-cervical Postures

Posture Mean±SD 95% CI ICC 95% CI for ICC SEM

NHP 40.8±3.12 39.69-42.07 0.93 0.89-0.96 0.78RHP 36.8±3.6 35.69-38.25 0.93 0.85-0.96 0.92FHP 43.7±2.93 42.58-44.81 0.94 0.90-0.97 0.68

CI indicates confidence interval; FHP, forward head posture; ICC,intraclass correlation coefficient; MMO, maximal mouth opening; NHP,neutral head posture; RHP, retracted head posture; SEM, standard error ofthe measurement; TMD, temporomandibular disorders.

TABLE 3. Descriptive Statistics for Measurements of PPT (kg/cm2) in Patients With Myofascial TMD Pain (N=29)

NHP RHP FHP

Measurement Points Mean±SD 95% CI Mean±SD 95% CI Mean±SD 95% CI

M1 2.2±0.61 1.97-2.44 1.91±0.52 1.71-2.11 1.73±0.48 1.55-1.92M2 2.4±0.61 2.17-2.64 2.1±0.55 1.91-2.35 1.91±0.55 1.7-2.12T1 2.43±0.58 2.2-2.65 2±0.58 1.84-2.28 1.82±053 1.62±2

CI indicates confidence interval; FHP, forward head posture; NHP, neutral head posture; PPT, pressure pain threshold; RHP, retracted head posture; SD,standard deviation; TMD, temporomandibular disorders.

3,50

NHP* * ** *

*2,50

3,00 RHPFHP

** * *

1,00

1,50

2,00

PP

T (

kg/c

m2 )

0,00

0,50

T1M1 M2

FIGURE 5. Comparison of the means of pressure pain thresholds(PPT) measures at masseter and temporalis muscles in relation to3 cranio-cervical postures: neutral head posture (NHP), retractedhead posture (RHP), and forward head posture (FHP). Error barsindicate SD and *P < 0.001.

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patients there seemed to be an increase in the retrodiscalspace and decrease in the distance between the shoulder andexternal auditory meatus. Therefore, an improved condylefossa relationship was apparent as the resting condylarposition became more anterior in conjunction with areduction of the FHP.

Recent evidence and the results of this study support theexistence of a relationship between the biomechanical actionof the cranio-cervical region and jaw movements, but ourresults do not show the degree of clinical implication that thedifferent postures have specific to intrinsic TMJ disorders.

PPTOur findings show that PPT values modify depending

upon the head posture in which they are measured. Thisvariability could be because of increased excitability ofthe trigeminal muscular nociceptors induced by differentcranio-cervical postures within which the PPT was mea-sured. In relation to orofacial nociception, an interactionbetween somatosensory processing and sensory-motorfunction is supported by our data.52

The results of our research cannot determine thereason by which the PPT decreases in the RHP and FHP ascompared with the NHP values. However, if our datais added to the findings of others it may lead to thedevelopment of different theories that offer additionalexplanations. We suggest that the PPT variations may bebecause of experimental biomechanical modifications ofmuscle and soft tissue that were produced when the patientstried to hold the FHP and the RHP, which generatedaugmented electromyography (EMG) activity and masti-catory reflexes. Modification of the activity produced ateach of the aforementioned postures could be causing PPTalteration. Furthermore, increased jaw-reflex activity maybe triggered by enhanced fusimotor drive, thereby elevatingmuscle spindle discharge resulting in reflex facilitation.Elevated fusimotor drive may in turn lead to increased TMJstiffness and pain. Earlier research has supported thepremise that experimental pain can augment masticatoryreflex activity.53–56

A recent study has shown that masseteric EMGactivity increases in the presence of a forced FHP.48 Inaddition, EMG changes in the suprahyoid muscles havebeen observed in experimentally induced FHP.57 However,in direct contrast, earlier studies have found increasedmasticatory EMG activity in head extension,58 which isa component of the RHP. Johansson and Sojka59 haveproposed a model to explain the spread of muscle painbased on the g-motoneuron system in which muscle stiffnessand pain are increased by enhanced activity of primarymuscle spindle afferents. This hypothesis may explain someof the results of this study, however, such thoughts are only

theoretical reflections and future research needs to provewhether postural changes truly alter the nociceptive trigem-inal mechanism.

Study LimitationsThe results of this study must be taken with caution

because the objective measurements were performed inan experimentally forced posture and not a natural one. Itwould also be interesting to determine in future researchwhether the PPT is modified with different natural posturesand whether postural alterations may affect or may be anaggravating factor in the development of orofacial pain. Itis also important to state that our participant sample onlyincluded patients with myofascial TMD. Therefore, it isimperative that future research apply the same method-ology with healthy individuals and other cohorts of TMDto determine whether the results can be replicated.

Clinical ImplicationsThe anatomic and physiological interaction between

the cranio-cervical and temporomandibular regions asshowed in this research supports the concept of a functionaltrigeminocervical coupling during jaw activities that influ-ences the inherent modifications that we observed in MMOand PPT. This factor must be taken into account duringpatient evaluation to control for variations in measurement.

The methodology that we used can result in a morestructured assessment of the MMO and PPT in neutralposition, within which we observed that average values wereobtained with excellent intrarater reliability. Postural treat-ment has already been shown to be useful for reducing TMDmyofascial pain and improving MMO.33,60 We have demon-strated experimentally that pain thresholds at the trigeminalarea can be modified only by changing the cranio-cervicalposture. As PPT values diminish in FHP and RHP, it wouldbe useful to consider new therapeutic strategies to improvethe cranio-cervical posture toward a NHP and futureresearch should determine whether postural treatments canhelp to modulate pain in myofascial TMD patients.

CONCLUSIONSThe results of this study shows that the experimental

induction of different cranio-cervical postures influencesthe MMO and PPT values of masticatory and joint func-tion of the temporomandibular complex. Our observationssupport the concept of a biomechanical relationship andinteraction within the trigeminocervical complex as well asinherent nociceptive processing in different cranio-cervicalpostures. Why or how postural modifications influence thePPT and MMO values are issues that are beyond the scopeof this study.

TABLE 4. Intrarater Reliability Statistics for Measurements of PPT in Patients With Myofascial TMD Pain (N=29) in the 3 Cranio-cervicalPostures

NHP RHP FHP

Measurement Points ICC 95% CI for ICC SEM ICC 95% CI for ICC SEM ICC 95% CI for ICC SEM

M1 0.93 0.87-0.96 0.16 0.9 0.82-0.94 0.16 0.93 0.87-0.96 0.12M2 0.91 0.84-0.95 0.18 0.92 0.86-0.96 0.16 0.92 0.87-0.96 0.15T1 0.89 0.82-0.94 0.19 0.94 0.89-0.97 0.14 0.92 0.86-0.96 0.13

CI indicates confidence interval; FHP, forward head posture; ICC, intraclass correlation coefficient; NHP, neutral head posture; PPT, pressure painthreshold; RHP, retracted head posture; SD, standard deviation; SEM, standard error of the measurement; TMD, temporomandibular disorders.

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ACKNOWLEDGMENT

The authors thank Dr Greg Murray (Professor ofDentistry, Jaw Function and Orofacial Pain Research Unit,Faculty of Dentistry, University of Sydney, Australia) for hishelpful contribution in this article.

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39. Lentell G, Kruse M, Chock B, et al. Dimensions of the cervicalneural foramina in resting and retracted positions usingmagnetic resonance imaging. J Orthop Sports Phys Ther. 2002;32:380–390.

40. Garrett TR, Youdas JW, Madson TJ. Reliability of measuringforward head posture in a clinical setting. J Orthop Sports PhysTher. 1993;17:155–160.

41. Svensson P, Arendt-Nielsen L, Nielsen H, et al. Effect ofchronic and experimental jaw muscle pain on pressure painthresholds and stimulus response curves. J Orofac Pain.1995;9:347–356.

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42. Chesterson LS, Sim J, Wright CC, et al. Inter-rater reliabilityof algometry in measuring pressure pain thresholds in healthyhumans, using multiple raters. Clin J Pain. 2007;23:760–766.

43. Eriksson PO, Zafar H, Nordh E. Concomitant mandibular andhead-neck movements during jaw opening-closing in man.J Oral Rehabil. 1998;25:859–870.

44. Zafar H, Nordh E, Eriksson PO. Temporal coordinationbetween mandibular and head-neck movements during jawopening-closing tasks in man. Arch Oral Biol. 2000;45:675–682.

45. Haggman-Henrikson B, Nordh E, Zafar H, et al. Headimmobilization can impair jaw function. J Dent Res. 2006;85:1001–1005.

46. Visscher CM, Huddleston Slater JJ, Lobbezoo F, et al.Kinematics of the human mandible for different head postures.J Oral Rehabil. 2000;27:299–305.

47. Ohmure H,Miyawaki S, Nagata J, et al. Influence of forward headposture on condylar position. J Oral Rehabil. 2008;35:795–800.

48. Rocabado M. Arthrokinematics of the temporomandibularjoint. Dent Clin North Am. 1983;27:573–594.

49. Hackney J, Bade D, Clawson A. Relationship between forwardhead posture and diagnosed internal derangement of thetemporomandibular joint. J Orofac Pain. 1993;7:386–390.

50. MunhozWC, Marques AP, de Siqueira JT. Evaluation of bodyposture in individuals with internal temporomandibular jointderangement. Cranio. 2005;23:269–277.

51. Olmos SR, Kritz-Silverstein D, Halligan W, et al. The effect ofcondyle fossa relationships on head posture. Cranio. 2005;23:48–52.

52. Sessle BJ. Mechanisms of oral somatosensory and motorfunctions and their clinical correlates. J Oral Rehabil. 2006;33:243–261.

53. Svensson P, Macaluso GM, De Laat A, et al. Effects of localand remote muscle pain on human jaw reflexes evoked by faststretches at different clenching levels. Exp Brain Res.2001;139:495–502.

54. Wang K, Svensson P, Arendt-Nielsen L. Effect of tonic musclepain on short-latency jaw-stretch reflexes in humans. Pain.2000;88:189–197.

55. Wang K, Arendt-Nielsen L, Svensson P. Excitatory actions ofexperimental muscle pain on early and late components ofhuman jaw stretch reflexes. Arch Oral Biol. 2001;46:433–442.

56. Wang K, Arendt-Nielsen L, Svensson P. Capsaicin-inducedmuscle pain alters the excitability of the human jawstretchreflex. J Dent Res. 2002;81:650–654.

57. Milidonis MK, Kraus SL, Segal RL, et al. Genioglossi muscleactivity in response to changes in anterior/neutral headposture. Am J Orthod Dentofacial Orthop. 1993;103:39–44.

58. Funakoshi M, Fujita N, Takehana S. Relations betweenocclusal interference and jaw muscle activities in response tochanges in head position. J Dent Res. 1976;55:684–690.

59. Johansson H, Sojka P. Pathophysiological mechanisms in-volved in genesis and spread of muscular tension in occupa-tional muscle pain. Med Hypotheses. 1991;135:196–203.

60. Komiyama O, Kawara M, Arai M, et al. Posture correction aspart of behavioural therapy in treatment of myofascial painwith limited opening. J Oral Rehabil. 1999;26:428–435.

Clin J Pain � Volume 27, Number 1, January 2011 Influence of Cranio-cervical Posture on TMD Pain

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87

5.2 Estudio II

López-de-Uralde-Villanueva I, Beltran-Alacreu H, Paris-Alemany A, Angulo-Díaz-Parreño S,

La Touche R. Reliability, Standard Error, and Minimal Detectable Change of Two Tests for

Craniocervical Posture Assessment in Asymptomatic Subjects and Chronic Neck/craniofacial

Pain Patients. (En revisión).

Objetivo del Estudio

Nuestro objetivo fue examinar la fiabilidad de dos mediciones para evaluar la postura

craneocervical (PC y DME). Además, se evaluó una posible asociación entre las variables

registradas. Como objetivo final, tenemos la intención de evaluar si existen diferencias en la

postura craneocervical entre sujetos asintomáticos y pacientes con dolor cérvico- craneofacial.

Resultados

La fiabilidad intra-evaluador de la medición de PC fue alta para los sujetos asintomáticos y

pacientes DCCF (CCI = 0,93 y 0,81, respectivamente) y para DME (rango CCI entre 0,78-0,99).

La fiabilidad intra-evaluador se mantuvo alta cuando se evaluó 9 días más tarde. Los resultados

de fiabilidad inter-evaluador fue alta para la PC (rango CCI entre 0,94 a 0,96) y fue justa para la

DME (rango CCI entre 0,78 a 0,79). El EEM de PC fue de 0,41 hasta 0,75 cm, mientras que el

MCD fue 0,96 a 1,74 cm. El SEM para la DME fue 1,61 a 7,06 mm, mientras que el MCD fue

3,76 a 16,47 mm. Se observó una correlación positiva moderada en ambos grupos entre HP y

SCD (sujetos asintomáticos, r = 0,447; pacientes con DCCF, r = 0,52). Análisis realizado con

una t de student mostró diferencias estadísticamente significativas entre los grupos para las

medidas de la postura craneocervical, pero estas diferencias eran muy pequeñas. Se encontró

una correlación positiva fuerte entre la discapacidad cervical y la craneofacial.

Conclusiones

Las mediciones para evaluar la postura craneocervical son fiables cuando se realizan por uno o

por dos evaluadores en sujetos asintomáticos o pacientes con DCCF.

1

Reliability, Standard Error, and Minimal Detectable Change of Two Tests for

Craniocervical Posture Assessment in Asymptomatic Subjects and Chronic

Neck/craniofacial Pain Patients

Ibai López-de-Uralde-Villanueva, PT, MSc1-4

, Hector Beltran-Alacreu, PT, MSc 2,3

,

Alba Paris-Alemany, PT, MSc1-4

, Santiago Angulo-Díaz-Parreño, MSc2,3,5

, Roy La

Touche, PT, MSc1-4

,

1. Department of Physiotherapy, Faculty of Health Science, The Center for

Advanced Studies University La Salle, Universidad Autónoma de Madrid,

Aravaca, Madrid, Spain.

2. Research Group on Movement and Behavioral Science and Study of Pain, The

Center for Advanced Studies University La Salle, Universidad Autónoma de

Madrid.

3. Institute of Neuroscience and Craniofacial Pain (INDCRAN), Madrid, Spain

4. Hospital La Paz Institute for Health Research, IdiPAZ. Madrid, Spain.

Madrid, Spain

5. Faculty of Medicine, Universidad San Pablo CEU, Madrid, Spain

Address for reprint requests / Corresponding author:

Roy La Touche

Facultad de Ciencias de la Salud

Centro Superior de Estudios Universitarios La Salle.

Calle la Salle, 10

28023 Madrid

SPAIN

Telephone number: + 34 91 7401980 (EXT.256)

Fax number:

Email address: [email protected]

The study protocol was approved by the local ethics committee of the Center for

Advanced Studies University La Salle, Madrid (Spain).

2

Reliability, Standard Error, and Minimal Detectable Change of Two Tests for

Craniocervical Posture Assessment in Asymptomatic Subjects and Chronic

Neck/craniofacial Pain Patients

ABSTRACT

PURPOSE:

Is recommended to quantifying the craniocervical posture as part of the assessment of

patients with neck and craniofacial pain to facilitate diagnosis and determine

treatment strategies. There is insufficient research regarding the intra-rater and inter-

rater reliability of craniocervical posture measurement using a CROM device and a

Digital Calliper.

OBJETIVE:

Determine the intra-rater and inter-rater reliability of two craniocervical posture

measurements on asymptomatic subjects and chronic neck/craniofacial pain (chronic

cervico-craniofacial pain, CCFP).

METHODS:

Two-groups repeated measures for inter- and intra-rater reliability study. 53

asymptomatic adult subjects and 60 CCFP patients who volunteered for the study.

Two raters measured head posture (HP) and the sternomental distance (SMD) using

the CROM device and Digital Calliper respectively.

RESULTS:

Intra-rater reliability of the HP measurement was high for asymptomatic subjects and

CCFP patients (Intraclass Correlation Coefficients (ICC)=0.93 and 0.81 respectively)

and for SMD (ICC range between 0.78-0.99), the intra-rater reliability remained high

3

when evaluated 9 days later. Inter-rater reliability was high for HP (ICC range

between 0.94-0.96) and fair for SMD (ICC range between 0.78-0.79). The HP

standard error of measurement (SEM) was 0.41–0.75cm while the minimal detectable

change (MDC) was 0.96–1.74cm. The SMD SEM was 1.61-7.06mm while the MDC

was 3.76-16.47mm. A moderate positive correlation for both groups was observed

between HP and SCD (asymptomatic subjects, r=0.447; CCFP patients, r=0.52).

Analysis with an independent t-test showed statistically significant differences

between groups for measures of craniocervical posture, but these differences were

very small. No statistically significant correlations between the HP and SMD with the

disabilities variables. Neck disability is strong positively correlated with the

craniofacial disability (r=0.79, p<0.001, n=60).

CONCLUSION:

The CROM device and Digital Calliper were reliable means of measuring HP and

SMD when performed by two or one raters in asymptomatic subjects and CCFP

patients.

KEYWORDS:

Reliability, Posture, Reproducibility of Results, Rehabilitation, Measurement, Neck

Pain, Temporomandibular disorders

INTRODUCTION

The optimal position of the head is the one in which the cranium is not inclined,

retracted, rotated, or extended. This position minimizes the muscle forces needed to

compensate the tendency of the head to tilt forward.[1] Currently, many professions

(office workers, clerks, carriers, etc.) require workers to spend much of their work day

sitting. In this situation one may adopt an excessive forward head posture (FHP).[2]

4

This head posture (HP) may occur due to a front translation of the head, a flexion of

the lower cervical spine, or both, and is also associated with an increase in extension

of the upper cervical spine.[3] It has been suggested that FHP increases the

compressive forces of the cervical zygapophyseal joint and those in the rear of the

vertebrae,[4] causing changes in the length and strength of the connective tissue

leading to stretching of the anterior neck structures and shortening of the posterior

neck muscles, all leading to pain.[5]

It is recommended that HP is quantified as part of the examination of patients with

neck pain to facilitate the diagnosis and determine treatment strategies. In addition, it

is very important to monitor a patient’s progress.[5] This growing interest around the

importance of the HP by researchers and clinicians is due to the belief that FHP is

associated with the development and persistence of certain disorders, such as cervical

headaches and migraines,[6] myofascial pain syndrome,[7] and woman with

craniofacial pain.[8] Regarding the association between the FHP and pain, there are

numerous studies with conflicting results: some showed differences in the HP of

patients with neck pain versus asymptomatic subjects,[9] while others do not.[10]

Attempts have been made to quantify FHP in many ways, both objectively and

subjectively. Subjective methods are described by some authors,[11] while objective

methods use photographs (to measure the tragus-C7-horizontal angle),[12]

radiographic images,[13] or the Cervical Range of Motion instrument (CROM),[14]

among others.

The CROM was designed to measure cervical range of motion but it can also measure

protraction and retraction of the head.[14] In the trial conducted by Garret et al.[14],

HP was measured in a sitting position with the CROM. The authors found high intra-

5

examiner reliability (ICC=0.93) while inter-examiner reliability was good

(ICC=0.83).

Another measurement that may be of interest is the sternomental distance (SMD). We

hypothesize a direct association between the SMD and the HP. We found only two

studies that evaluated the SMD, but they did not association it with HP.[15, 16]

There is little evidence concerning the reliability of intra-examiner and inter-examiner

measurement of HP using the CROM, therefore our purpose was to examine this

reliability and of using a Digital Calliper to measure the SMD. In addition, we

assessed a possible association between the variables recorded by these instruments

and as ultimate objective, we intend to assess whether there are differences in

craniocervical posture between asymptomatic subjects and patients with chronic

cervico-craniofacial pain (CCFP).

METHODS

Study design

We employed two-group repeated measures for intra- and inter-rater reliability

design. This study was planned and conducted in accordance with the Guidelines for

Reporting Reliability and Agreement Studies (GRRAS).[17]

Sample size

Sample size was calculated using the method described by Walter et al.[18]. This

method is recommended for estimating of sample size based on the Intraclass

Correlation Coefficient (ICC). The minimally acceptable ICC value (ρ1 = 0.7) versus

an alternative ICC reflecting the expected value (ρ1 = 0.8) was chosen. To obtain a

power of 80% (β = 0.2) and significance level of 5%, we determined that a sample of

at least 53 healthy subjects was required for intra-rater and inter-rater reliability (two

sets of 2 measurements were performed each day for two days). In addition, under the

6

same conditions, we determined that a sample of at least 57 symptomatic subjects was

required for intra-rater reliability (1 set of 2 measurements were performed each day

for three days). To estimate sample size we used the Power Analysis & Sample Size

Software (PASS 12).

Subjects

Two convenience samples of asymptomatic subjects were obtained from our

university campus and the local community through flyers, posters, and social media.

To participate in this study, the asymptomatic subjects were required to be between

18 and 65 years of age and must not have experienced: (1) neck or face pain during

data collection, or (2) a history of neck or face pain in the prior six months.

The second convenience sample of symptomatic subjects consisted in chronic

cervico-craniofacial pain patients. The sample was recruited two private clinics

specialized in spine, craniofacial pain and temporomandibular disorders (TMD)

(Madrid, Spain). A diagnosis of CCFP of muscular origin was the first inclusion

criterion. We defined CCFP of muscular origin as the presence of mechanical signs of

dysfunction and muscular pain (e.g. limited movement, uncoordinated movement,

weakness and lack of endurance in the neck and jaw) that were exacerbated by

maintained postures and movement, generating pain at the cervical and craniofacial

regions [19]. The specific inclusion criteria were: a) signs of disability and pain in the

orofacial and craniomandibular region, according to the Craniofacial pain and

disability inventory (CF-PDI) [20]; b) a primary diagnosis of myofascial pain

following Axis 1 (myofascial pain) of the Research Diagnostic Criteria for

Temporomandibular Disorders[21]; c) ≥ 6 months with the presence of the pain; d) ≥

5 points on the Neck Disability Index (NDI)[22]; f) bilateral pain of the temporal,

masseter, suboccipital and trapezius muscles. Patients were excluded if they had any

7

"red flags,"[23] a rheumatologic disease, any type of cancer, cervical radiculopathy,

myelopathy, a history of cervical surgery or whiplash trauma. The study was

conducted in accordance with the Declaration of Helsinki and was approved by the

local ethics committee. Prior to their participation, subjects gave written informed

consent.

Evaluators

The assessments were made by two physical therapists with more than three years of

clinical experience using the CROM to measure range of movement (ROM) and head

posture (HP) in clinical practice. Both therapists received a 120-minute training

session on how to use the Digital Calliper and how to measure the SMD.

Instrumentation

In this study we used the CROM equipped to measure the HP. The device used was

the CROM 3. It has the appearance of eyeglasses and is made from a lightweight

plastic with three inclinometers, one for each plane of motion. It is adjusted using a

hook-and-loop strap. The part of the device used to measure HP includes the forward

head arm and the vertebra locator. The forward head arm is equipped with a ruler

marked in 0.5 cm units, indicating the horizontal distance between the bridge of the

nose and the vertebra locator. The vertebra locator has a leveler bubble on top to

assist with accurate positioning. In this study the inclinometers were not used because

neck movements were not evaluated.

The digital calliper was used to quantify the SMD. The device is made of plastic with

a 5-digit LCD display, and can measure in inches or millimeters (mm) and with a

range of 0.01 mm to 150 mm. It also includes a ruler provided with a nonius, for

accurate measurement of lengths or angles. The one used for measuring length

comprised of a rule divided into equal parts on which a nonius slides such that n-1

8

divisions of the rule are divided into n equal parts of the nonius. It has two tips for

controlling internal and external measurements. The digital calliper is used for direct

measurement. Also, it is a fast and accurate instrument.

Procedures

The assessments were made between May and June of 2012 in our university

laboratory for asymptomatic subjects and between July and September of 2014 for

symptomatic subjects. Each healthy subject visited the laboratory on two different

occasions separated by a space of 48 hours. On the first day, rater A performed the

first assessment followed by rater B. On the second day, rater B performed the first

assessment followed by rater A. Moreover, each symptomatic subject visited the

laboratory on three different occasions separated by a space of 48 hours (between trial

1 and trial 2) and 9 days (between trial 2 and trial 3). In symptomatic subjects, the

assessment always was performed by the same rater. In both samples of subjects, each

rater used a data collection sheet on which to record the measurements. Before the

assessments, subjects removed eyeglasses, caps, and any jewelry. The measurements

in this study were taken twice, and the order in which they were performed was as

follows:

1. Head Posture

To quantify HP, the subjects were told to stay in the starting position: sitting in a chair

with a back rest, feet flat on the floor, and arms hanging alongside the body. The

evaluator placed the CROM on the subject’s head like a pair of eyeglasses and

adjusted it with the strap. The evaluator then located the spinous process of C7 and

placed the vertebra locator on it, adjusting the pressure until the subject indicated that

the pressure of the device was felt. Once the subject felt the pressure over C7, the

9

evaluator stated, “From this moment you should not move”. This was performed as a

means for the subject to become familiar with the test.

Then the subject was asked to stand up and then sit back into the starting position.

The evaluator standing to the left side of the subject, found the spinous process of C7

and placed the vertebra locator such that it formed a 90° angle with the head arm of

the CROM with the bubble indicating the instrument was level (Figure 1. A). This

measurement was made twice, and between the first and the second measurements the

subjects were asked to stand up and sit back into the starting position again,

whereupon the evaluator completed the procedure.

2. Sternomental Distance

The evaluator first explained to the subject that the measurement would take place

while lying on a couch. Also at this time the evaluator showed the Digital Calliper to

the subject and said: “You will notice contact on your sternum and on your chin; at

the moment you notice that you should not move.” When the subject understood the

statement and gave the evaluator permission to proceed, the subject was asked to lie

in a supine position on the couch, looking at the ceiling. When the subject was in

position the evaluator gave the instruction: “Don’t move your head.” Once in place,

the measurement was taken from the jugular notch of the sternum to the chin

protuberance (Figure 1. B). The measurement was taken twice between the subject

was instructed to roll to a right lateral position and then return to the supine position.

DATA ANALYSIS

Data were analysed with the SPSS statistical package (SPSS v.20.0; SPSS, Inc,

Chicago, IL). The Kolmogorov-Smirnov test was used to analyze the normal

distribution of the variables (P>0.05).

10

The intra-rater and inter-rater reliability was evaluated using the Intraclass Correlation

Coefficient (ICC). Reliability levels were defined based on the following

classification: good reliability, ICC ≥ 0.75; moderate reliability, ICC ≥ 0.50 and

<0.75; and poor reliability, <0.50 [24].

Bland-Altman analysis were performed by calculating the mean difference between

two measurements and the standard deviation (SD) of the difference.[25] A 95% of

the differences is expected to be less than two SDs. The closer the mean difference

was to 0 and the smaller the SD of this difference, the better was the agreement.[25]

The Bland–Altman analysis was used to compare the values of HP and SMD obtained

by the two raters separately. Similarly, comparisons were made to confirm the

reproducibility by analyzing the measurements values obtained on two trials. Bland-

Altman analysis was performed using MedCalc for Windows, version 12.5.0.0

(MedCalc Software, Mariakerke, Belgium).

Measurement error is expressed as a standard error of measurement (SEM), which is

calculated as , where SD is the SD of values from all participants and

ICC is the reliability coefficient.[26] Measurement error is the systematic and random

error of a patient’s score that is not attributable to true changes in the construct to be

measured.[27]

Responsiveness was assessed using the Minimal Detectable Change (MDC). The

MDC90 expresses the minimal change required to be 90% confident that the observed

change between the two measures reflects real change and not measurement error.[28]

It is calculated as .[28]

The Pearson correlation coefficient was used to analyze the association between HP

and SMD in the two samples of subjects, also used to analyze the correlations

between the variables of disability with the data HP and SMD in patients with CCFP.

11

A Pearson correlation coefficient greater then 0.60 indicated a strong correlation,

between 0.30 and 0.60 indicated a moderate correlation, and below 0.30 indicated a

low or very low correlation.[29]

Finally, the independent t-test was used for the analysis of HP and SMD variables

(using the mean of the trial 1 and 2), comparing the collection data for the two

samples.

RESULTS

The asymptomatic subjects sample consisted of 53 participants, 30 of whom were

women; the subjects were between 18 and 53 years of age (mean=38.1, SD=10.5

years). The symptomatic subjects sample consisted of 60 CCFP patients, 32 of whom

were women; the subjects were between 19 and 61 years of age (mean=41.7, SD=11.7

years). No statistically significant differences between the general characteristics of

both groups are presented. The group of symptomatic subjects presented a mean of

14.78 ±4.04 of neck disability and 16.30±7.11 of craniofacial disability. All variables

were normally distributed according to the Kolmogorov-Smirnov test (P>0.05). No

subjects were excluded from the study based on the inclusion and exclusion criteria.

Asymptomatic subjects

The ICC value for intra-rater reliability of single measures separated by a space of 48

hours was 0.93 for HP and ranged from 0.95 to 0.99 for SMD. Descriptive statistics,

ICCs and associated 95% CIs, SEMs and MDC90 between each evaluator´s trials are

presented in Table 1.

ICC values for interrater reliability of single measures ranged from 0.78 to 0.79 for

SMD and from 0.94 to 0.96 for HP. Descriptive statistics, ICCs and associated 95%

CIs, SEMs, and MDC90 between each rater´s trials are presented in Table 1.

12

The Bland-Almand analysis for the intra-rater and inter-rater performances are shown

for assessement of HP and SMD in Table 2. The mean differences in all Bland-

Almand analysis were close to zero, suggesting that appropriate intra-rater and inter-

rater reliability. Inter-rater performances of SMD at the 95% confidence intervals

showed large variability, would indicate error and suggesting that SMD assessment is

reliable but not precise (Table 2).

The scatter diagram (Figure 2. A) shows a moderate positive correlation between HP

and the SMD (r=0.44, p=0.001, n=53).

Chronic cervico-craniofacial pain patients

The ICC value for intra-rater reliability of single measures separated by a space of 48

hours was 0.88 for HP and 0.79 for SMD. When the singles measures were separated

by a space of 9 days, the ICC value for intra-rater reliability was 0.81 for HP and 0.76

for SMD. Descriptive statistics, ICCs and associated 95% CIs, SEMs and MDC90

between trials are presented in Table 3.

The Bland-Almand analysis for the intra-rater performances are shown for

assessement of HP and SMD in Table 4. The mean differences in all Bland-Almand

analysis were close to zero, suggesting that appropriate intra-rater and inter-rater

reliability. Inter-rater performances of SMD at the 95% confidence intervals showed

large variability, would indicate error and suggesting that SMD assessment is reliable

but not precise. (Table 4).

The scatter diagram (Figure 2. B) shows a moderate positive correlation between HP

and the SMD (r=0.56, p<0.001, n=60). No statistically significant correlations

between the HP and SMD with the disabilities variables. Neck disability is strong

positively correlated with the craniofacial disability (r=0.79, p<0.001, n=60).

13

Asymptomatic subjects versus chronic cervico-craniofacial pain patients

The independent t-test for comparison between the asymptomatic and symptomatic

samples, using the mean of the trial 1 and 2 (separated by 48 hours), found

statistically significant differences for HP and SMD (p<0.05). Descriptive statistics,

mean differences and associated 95% CIs between the two samples are presented in

Table 5.

DISCUSSION

The evaluation of HP is a variable to consider evaluating in clinical practice due to its

influence on the pathophysiology of the cervical region.[4, 30] Our results show

strong intra- and inter-rater reliability when measuring HP with the CROM device. As

for the examination of the SMD, results obtained with the Digital Calliper reflected

strong reliability.

Recently, several studies have measured HP using different methods and

instruments,[1, 11–13] but disadvantages were low reliability,[11, 31] high cost, and

difficulty in transporting the equipment.[13, 32, 33] Furthermore, where a

radiological diagnosis was used, the risk of radiation exposure to the subject must be

considered.

In the literature we found only one study in which the intra- and inter-rater

reliabilities were evaluated in measuring HP using CROM; results showed a good

intra and inter-rater reliability.[14] If we compare this data with our own, we find

strong intra-rater reliability in both investigations, while our inter-rater reliability was

superior to that obtained by Garrett et al.[14] for asymptomatic subjects but not for

CCFP patients. Both investigations followed a rigorous standardized protocol using

similar samples. An important aspect to note is that the time did not influence the

14

intra-rater reliability and the results were very similar at 48 hours and 9 days later. It

has been suggested that a range of 2 to 14 days is generally acceptable for analyzing

test reliability.[34]

As we mentioned, the SMD measured by the Digital Calliper showed high intra-rater

reliability where it showed acceptable inter-rater reliability. Again, we find only one

article that mentions the SMD, but that investigation was designed to generate a

prediction rule for the degree of difficulty when performing a laryngoscopy.[15, 16]

The SMD measurement used in a study by Al Ramadhani et al.[15], was of 142.8

(SD=1.50), whereas we found SMD to be between 107.5 and 113.57 of our study.

This difference could be explained by the fact that their measurement protocol was

performed measuring the cervical extension. It is also worth mentioning that the

measure was performed using a ruler with an accuracy of 5 mm rather than a Digital

Calliper with a resolution of 0.01 mm. We feel this fact supports a contention that our

investigation is more rigorous and reliable.

We found the intra-rater MDC of HP varied from 1.27 cm to 1.74 cm but that the

inter-rater MDC was between 0.96 cm and 1.30 cm. We also found that the intra-rater

MDC of the SMD was between 3.76 mm and 14.55 mm while the inter-rater MDC

was between 16.13 mm and 16.47 mm. Is considered MDC the smallest quantity

above the SEM, although it should not be assumed that this change has reached the

threshold of clinically significant improvement.[35]

With regard to the comparison of the means of the 2 measurements of the

craniocervical posture, the results show that there are statistically significant

differences between both groups, with higher measures in the group of CCFP,

however you have to take into account that the differences are very small and exceed

slightly the MDC in the HP measurement (mean difference -1.27 cm), nor for the

15

SMD (mean difference -5.01 mm), other studies have found similar results to ours,

finding very small differences between measurements of craniocervical posture in

asymptomatic subjects versus symptomatic subjects with neck pain [30] and

TMD.[36] We did not find association between measurements of craniocervical

posture and disability variables, this result is supported by recent evidence [36, 37],

being this issue controversial.[38] We have found a strong correlation between neck

disability and craniofacial disability (r=0.79), other studies have also found similar

results to our findings. [20, 36]

Furthermore, the Pearson correlation coefficient between HP and the SMD is 0.447

for asymptomatic subject and 0.56 for symptomatic subjects, suggesting a moderate

correlation. We believe this is the first study to determine this association; we found

that the previous studies measuring the SMD do not correlate it to HP. Thus, we can

assume that there is a relationship between HP in the sitting position and SMD in

supine position in healthy subjects.

Limitations

This study has several limitations that must be discussed. We agree with Garret et

al.[14] that a limitation exists in the head arm of the CROM in that it is marked in

increments of 0.5 cm, making it hard to determine a measurement when the indicator

is between two marks. We believe that the reliability and data collection could be

improved if the head arm was marked in mm. Lastly, we calculated the MDC but not

the minimal clinically relevant change (MCRC), which we believe is of special

interest in clinical practice. We must remember that the MDC is not the same as the

MCRC, which is the grade of clinically significant improvement and is normally

associated with an external criteria that indicates when that change has occurred.[35]

We have not calculated the MCRC, so we do not know the grade of clinically

16

significant improvement. Future randomized controlled trials should identify

interventions that influence the HP and SMD, this could help assess the performance

of this test when subjected to clinical interventions and also with those results could

calculate the MCRC.

CONCLUSIONS

The CROM and the Digital Calliper are reliable instruments for measuring HP and the

SMD in healthy subjects and CCFP patients. Furthermore, there is a moderate

correlation between HP and the SMD and strong correlation between neck disability

and craniofacial disability. We did not find association between measurements of

craniocervical posture and disability variables. We also believe further studies should

consider the MCRC and the influence of longer periods between examinations on the

measures.

17

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20

FIGURES AND LEGENDS

Figure 1. A) Placement of CROM with the head arm for the measure of Head Posture

with the vertebra locator. B) Evaluator taking measure from the jugular notch of the

sternum to the chin protuberance to quantitative the Sternomental Distance.

21

Figure 2. Scatter Diagram showing correlation between Head Posture and the

Sternomental Distance. A) Scatter diagram for asymptomatic subjects (n=53); B)

scatter diagram for chronic cervico-craniofacial pain patients (n=60).

22

Table 1. Intra-rater and Inter-rater reliability and descriptive statistics for

measurements in asymptomatic subjects.

Abbreviations: CI, confidence interval; ICC 3,1, intraclass correlation coefficient,

model 3,1; HP, head posture; MDC90, minimal detectable change at the 90%

confidence level; SMD, sternomental distance; SD, standard deviation; SEM,

standard error of the measurement.

Rater A Rater B

Trial 1

(Mean

± SD)

Trial 2

(Mean

± SD)

ICC

3,1

95%

CI for

ICC

SEM MDC90 Trial 1

(Mean

± SD)

Trial 2

(Mean

± SD)

ICC

3,1

95%

CI for

ICC

SEM MDC90

HP (cm) 18.97 ±

2.47

19.07

± 2.19

0.93 0.88 –

0.96

0.60 1.40 18.77

± 2.35

18.96

± 2.19

0.93 0.89 –

0.96

0.55 1.30

SMD

(mm)

108.50

± 16.55

109.03

±

16.14

0.99

0.98 –

0.99

1.61 3.76 105.07

±

14.55

107.54

±

14.21

0.95 0.85 –

0.97

2.75 6.42

Trial 1

Trial 2

Rater A

(Mean

± SD)

Rater

B

(Mean

± SD)

ICC

3,1

95%

CI for

ICC

SEM MDC90 Rater

A

(Mean

± SD)

Rater

B

(Mean

± SD)

ICC

3,1

95%

CI for

ICC

SEM MDC90

HP (cm) 18.97 ±

2.47

18.77

± 2.35

0.94 0.90 –

0.96

0.56 1.30 19.07

± 2.19

18.96

± 2.19

0.96 0.93 –

0.98

0.41 0.96

SMD

(mm)

108.50

± 16.55

105.07

±

14.55

0.78 0.63 –

0.87

7.06 16.47 109.03

±

16.14

107.54

±

14.21

0.79 0.66 –

0.87

6.91 16.13

23

Table 2. Statistical metrics from Bland-Altman analysis of the intra-rater and inter-

rater measurements in asymptomatic subjects.

Intra-rater

Rater A Rater B

Mean

differences

± SD

95% CI for

mean

differences

LOA (Lower

limit-Upper

limit)

Mean

differences

± SD

95% CI for

mean

differences

LOA (Lower

limit-Upper

limit)

HP (cm) -0.10 ± 0.85 -0.34 to 0.15 -1.76 to 1.57 -0.19 ± 0.79 -0.41 to 0.04 -1.73 to 1.36

SMD (mm) -0.53 ± 2.28 -1.18 to 0.12 -4.99 to 3.94 -2.47 ± 3.89 -3.58 to -1.37 -10.10 to 5.16

Inter-rater

Trial 1 Trial 2

HP (cm)

0.19 ± 0.79 -0.03 to 0.42 -1.35 to 1.74 0.10 ± 0.59 -0.06 to 0.27 -1.05 to 1.25

SMD (mm) 3.43 ± 9.99 0.59 to 6.27 -16.14 to 23 1.49 ± 9.78 -1.29 to 4.26 -17.68 to 20.65

Abbreviations: CI, confidence interval; HP, head posture; LOA, limits of agreement;

SMD, sternomental distance; SD, standard deviation.

24

Table 3. Intra-rater reliability and descriptive statistics for measurements in chronic

cervico-craniofacial pain patients.

Abbreviations: CI, confidence interval; ICC 3,1, intraclass correlation coefficient,

model 3,1; HP, head posture; MDC90, minimal detectable change at the 90%

confidence level; SMD, sternomental distance; SD, standard deviation; SEM,

standard error of the measurement.

Rater A

Trial 1

(Mean

± SD)

Trial 2

(Mean

± SD)

Trial 3

(Mean

± SD)

48 hours between trials

(Trial 1-Trial 2)

9 days between trials

(Trial 2-Trial 3)

ICC

3,1

95% CI

for ICC

SEM MDC90 ICC

3,1

95% CI

for ICC

SEM MDC90

HP (cm) 20.40 ±

1.50

20.23

± 1.58

20.03 ±

1.84

0.88 0.80 –

0.92

0.54 1.27 0.81 0.70 –

0.88

0.75 1.74

SMD

(mm)

111.53

± 12.41

113.57

±

11.83

112.73

± 13.78

0.79

0.67 –

0.87

5.60 13.07 0.76 0.63 –

0.85

6.24 14.55

25

Table 4. Statistical metrics from Bland-Altman analysis of the intra-rater

measurements in chronic cervico-craniofacial pain patients.

Intra-rater

48 hours (Trial 1 – Trial 2) 9 days (Trial 2 – Trial 3)

Mean

differences

± SD

95% CI for

mean

differences

LOA (Lower

limit-Upper

limit)

Mean

differences

± SD

95% CI for

mean

differences

LOA (Lower

limit-Upper

limit)

HP (cm) 0.17 ± 0.77 -0.03 to 0.37 -1.34 to 1.67 0.21 ± 1.06 -0.06 to 0.48 -1.86 to 2.28

SMD (mm) -2.03 ± 7.92 -4.08 to 0.01 -17.56 to 13.49 0.83 ± 8.82 -1.45 to 3.11 -16.46 to 18.12

Abbreviations: CI, confidence interval; HP, head posture; LOA, limits of agreement;

SMD, sternomental distance; SD, standard deviation.

26

Table 5. Comparison between the asymptomatic subjects and chronic cervico-

craniofacial pain patients samples for measurements.

Asymptomatic

subjects (Mean ± SD)

CCFP patients (Mean

± SD)

Mean differences (95% CI)

HP (cm) 18.95 ± 2.25 20.32 ± 1.49 -1.37 (-2.11 to -0.63)**

SMD (mm) 107.54 ± 14.53 112.55 ± 11.46 -5.01 (-9.92 to -0.1)*

Abbreviations: CI, confidence interval; HP, head posture; SMD, sternomental

distance; SD, standard deviation.

* p<0.05

** p<0.01

114

5.3 Estudio III

La Touche R, Fernández-de-Las-Peñas C, Fernández-Carnero J, Díaz-Parreño S, Paris-

Alemany A, Arendt-Nielsen L. Bilateral mechanical-pain sensitivity over the trigeminal region

in patients with chronic mechanical neck pain. J Pain. 2010 Mar;11(3):256-63

Objetivos del estudio

El objetivo del presente estudio fue investigar la sensibilización del trigémino en pacientes con

dolor de cuello crónico mecánico, además se observaron la interacción de los resultados con

variables psicológicos, como la depresión y la ansiedad.

Resultado

Los resultados mostraron que los niveles de UDPS son significativamente menores

bilateralmente sobre los puntos musculares del masetero, temporal, los del trapecio superior, y

también los puntos medidos en las articulaciones cigapofisiarias de C5-C6 (P <0,001), pero no

sobre los puntos del músculo tibial anterior (P = 0,4) en pacientes con dolor de cuello crónico

mecánico, en comparación con los controles. La magnitud de la disminución de los UDPs fue

mayor en la región cervical, en comparación con la región del trigeminal (P <0,01). Los UDPs

en los músculos maseteros se correlacionaron negativamente tanto a la duración de los síntomas

de dolor y la intensidad del dolor (P <0,001). Además se encontraron correlaciones positivas

entre la intensidad de dolor con la discapacidad de cuello y los síntomas depresivos.

Conclusiones

Nuestros resultados revelaron la presencia de hiperalgesia mecánica en la región trigeminal en

pacientes con dolor de cuello crónico mecánico, lo que sugiere la difusión de la sensibilización a

la región del trigémino en esta población de pacientes. Los resultados de este estudio sugieren

que existe la presencia de un proceso de sensibilización del NCT en esta población. Este

hallazgo tiene implicaciones para el desarrollo de estrategias de gestión.

The Journal of Pain, Vol 11, No 3 (March), 2010: pp 256-263Available online at www.sciencedirect.com

Bilateral Mechanical-Pain Sensitivity Over the Trigeminal Region in

Patients With Chronic Mechanical Neck Pain

Roy La Touche,*y Cesar Fernandez-de-las-Penas,zx{ Josue Fernandez-Carnero,zx{

Santiago Dıaz-Parreno,*y Alba Paris-Alemany,*y and Lars Arendt-Nielsenz

*Faculty of Medicine, Department of Physical Therapy.yUniversity Center for Clinical Research of the Craneal-Cervical-Mandibular System, Universidad San Pablo CEU,Madrid, Spain.zDepartment of Physical Therapy, Occupational Therapy, Rehabilitation and Physical Medicine.xEsthesiology Laboratory, Universidad Rey Juan Carlos, Alcorcon, Madrid, Spain.{Centre for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University,Aalborg, Denmark.

ReceivedAddressde Ciencs/n, 2892

1526-590

ª 2010 b

doi:10.10

256

Abstract: The aim of this study was to investigate bilateral pressure-pain sensitivity over the tri-

geminal region, the cervical spine, and the tibialis anterior muscle in patients with mechanical chronic

neck pain. Twenty-three patients with neck pain (56% women), aged 20 to 37 years old, and 23

matched controls (aged 20 to 38 years) were included. Pressure pain thresholds (PPTs) were bilaterally

assessed over masseter, temporalis, and upper trapezius muscles, the C5-C6 zygapophyseal joint, and

the tibialis anterior muscle in a blinded design. The results showed that PPT levels were significantly

decreased bilaterally over the masseter, temporalis, and upper trapezius muscles, and also the C5-C6

zygapophyseal joint (P < .001), but not over the tibialis anterior muscle (P = .4) in patients with

mechanical chronic neck pain when compared to controls. The magnitude of PPT decreases was

greater in the cervical region as compared to the trigeminal region (P < .01). PPTs over the masseter

muscles were negatively correlated to both duration of pain symptoms and neck-pain intensity (P <

.001). Our findings revealed pressure-pain hyperalgesia in the trigeminal region in patients with

mechanical chronic neck pain, suggesting spreading of sensitization to the trigeminal region in

this patient population.

Perspective: This article reveals the presence of bilateral pressure-pain hypersensitivity in the

trigeminal region in patients with idiopathic neck pain, suggesting a sensitization process of the tri-

gemino-cervical nucleus caudalis in this population. This finding has implications for development of

management strategies.

ª 2010 by the American Pain Society

Key words: Neck pain, trigeminal sensitization, pressure pain threshold.

Chronic mechanical neck pain is a significant clinicalproblem. It seems that the prevalence of neck painis as high as the prevalence of low back pain. A sys-

tematic review reported a 1-year prevalence for neckpain ranging from 16.7 to 75.1%, with a mean of37.2%.11 A best-evidence synthesis showed an incidencerate for self-reported neck pain in the general popula-tion between 146 and 213 per 1,000 patients per year.21

Nearly half of neck-pain patients develop chronic symp-

May 31, 2009; Revised June 29, 2009; Accepted July 22, 2009.reprint requests to Cesar Fernandez de las Penas, Facultadias de la Salud, Universidad Rey Juan Carlos, Avenida de Atenas2 Alcorcon, Madrid, Spain. E-mail: [email protected]

0/$36.00

y the American Pain Society

16/j.jpain.2009.07.003

toms,4 and many will continue to exhibit moderatedisability at long-term follow-up.17 The economicburden associated with the management of neck painis second only to low back pain in annual workers’ com-pensation costs in the United States.44

Although the aetiology of insidious mechanical neckpain is under debate, it is clear that neck pain is multifac-torial in nature, with both physical and psychosocial con-tributors.38 In recent years, there has been an increasinginterest in the study of nociceptive-pain processing indifferent musculoskeletal-pain conditions. For instance,pressure pain thresholds5,32 have been extensively usedfor investigating mechanical pain hypersensitivity inseveral chronic pain conditions, eg, whiplash,36 fibro-myalgia,9 unilateral migraine,14 repetitive strain injury,18

tension-type headache,13 osteoarthritis,1 low back

La Touche et al 257

pain,27 or carpal tunnel syndrome.15 Nevertheless, thephenomenon of sensory hypersensitivity has been rela-tively recently investigated in mechanical nontraumaticneck pain.37

Scott et al33 found that the hypersensitivity present inindividuals with idiopathic neck pain seems to be con-fined to the neck area with little evidence of spread tomore remote body regions, eg, the tibialis anterior mus-cle, as opposite happens in chronic whiplash. The pres-ence of hypersensitivity restricted to the neck regionmay reflect segmental local sensitization, but not wide-spread central sensitization, in patients with idiopathicneck pain.

Several studies have reported that patients with neckpain also suffered from symptoms in the orofacialregion,7,8,23 and headaches.29 The expansion of symp-toms from the neck area to the trigeminal region maybe related to the convergence of the nociceptive sec-ond-order neurons receiving both trigeminal and cervi-cal inputs into the trigemino-cervical nucleus caudalisin the spinal gray matter of the spinal cord.25 To thebest of our knowledge, no previous study has investi-gated the pressure hypersensitivity over the trigeminalregion in chronic mechanical neck pain. Further, Rhudyand Meagher31 demonstrated that psychological states,particularly anxiety and depression, induce an increasedeffect on pressure-pain sensitivity. Therefore, the aim ofthe present study was to investigate trigeminal sensitiza-tion in patients with chronic mechanical neck pain con-trolling psychological aspects, such as depression andanxiety.

Methods

SubjectsPatients presenting with mechanical insidious neck

pain referred by their primary-care physicians to a spe-cialized physical-therapy clinic between September2007 and February 2008 were screened for possible eligi-bility criteria. Mechanical neck pain was defined as gen-eralized neck and/or shoulder pain with symptomsprovoked by neck postures, neck movement, or palpa-tion of the cervical musculature. Symptoms had to be bi-lateral and present for at least 6 months. Patients wereexcluded if they exhibited any of the following: 1) unilat-eral neck pain; 2) diagnosis of fibromyalgia;43 3) previouswhiplash; 4) cervical spine surgery; 5) clinical diagnosis ofcervical radiculopathy or myelopathy; 6) history of previ-ous physical-therapy intervention for the cervical region;7) presence of severe degenerative arthritis (confirmedby cervical radiography taken for all patients over theage of 30 years); 8) less than 18 years; 9) diagnosis ofany TMD, according to the Research Diagnostic Criteriafor TMD (RDC/TMD)10; or 10) concomitant diagnosis ofprimary headache.

Demographic and Clinical DataDemographic data including age, gender, height,

weight, location, and nature of the symptoms was col-lected. An 11-point numerical point rate scale22 (NPRS;

0 = no pain, 10 = maximum pain) was used to assess cur-rent level of neck pain. Patients also completed the NeckDisability Index (NDI) to measure perceived disability,42

the Beck Depression Inventory (BDI-II) to assess symp-toms of depression,2 and the State-Trait Anxiety Inven-tory (STAI) for assessing state and trait anxiety.34

The NDI consist of 10 questions measured on a 6-pointscale (0 = no disability, 5 = full disability).42 The numericscore for each item is summed for a score varying from0 to 50, where higher scores reflect greater disability.The NDI has demonstrated to be a reliable (intraclass cor-relation coefficients ranging from .50 to .98)24 and validself-assessment of disability in chronic neck pain.19,39

The BDI-II is a 21-item self-report measure assessingaffective, cognitive, and somatic symptoms of depres-sion.2 Patients choose from a group of sentences thatbest describe how they have been feeling in the past 2weeks. Higher scores indicate higher levels of depressivesymptoms.2 The BDI-II showed good internal consistency(alpha coefficient .90) and adequate divergent validity.41

The STAI is a self-report assessment device whichincludes separate measures of state and trait anxiety.34

In the present study, the trait-anxiety subscale whichdenotes relatively stable anxiety proneness and refersto a general tendency to respond with anxiety to per-ceived threats in the environment was used. Participantsuse a 4-point response scale ranging from ‘‘almost never’’to ‘‘almost always’’, indicating the extent to which theyexperience each emotion. The State-Trait questionnairehas shown good internal consistency (a = .83). Higherscores indicate greater trait anxiety.34

Finally, healthy controls were recruited from volunteerwho responded to a local announcement and were ex-cluded if they exhibited a history of neck, facial, orhead pain (infrequent episodic tension-type headachewas permitted), any systemic disease or any history oftraumatic event (whiplash).

The study was conducted in accordance with the Hel-sinki Declaration, and all subjects provided informed con-sent which was approved by the local ethics committee.

Sample Size DeterminationThe sample-size determination and power calculations

were performed with an appropriate software (Tamanode la Muestra, v.1.1, Universidad de Medicina, Madrid,Spain). The calculations were based on detecting, atthe least, significant clinical differences of 20% on pres-sure pain threshold (PPT) between both groups,28 withan alpha level of .05 and a desired power of 80%, andan estimated interindividual coefficient of variation forPPT measures of 20%. This generated a sample size ofat least 16 participants per group.

PPT AssessmentPPT is defined as the minimal amount of pressure

where a sensation of pressure first changes to pain.40 Amechanical pressure algometer (Pain Diagnosis andTreatment Inc, Great Neck, NY) was used in this study.The device consists of a round rubber disk (1 cm2)attached to a pressure gauge. The gauge displays values

258 Trigeminal Pain Sensitivity in Neck Pain

in kg/cm2, ranging from 0 to 10 kg. The mean of 3 trials(intraexaminer reliability) was calculated and used forthe main analysis. A 30-second resting period wasallowed between each trial. The reliability of pressure al-gometry has been found to be high in both asymptom-atic subjects6 (ICC .91 [95% CI .82–.97]) and neck painpatients45 (ICC .78–.93; 95% CI .53–.97).

Study ProtocolThe study protocol was the same for neck-pain pa-

tients and healthy controls. All examinations weredone in a quiet, draught-free, temperature- and humid-ity-controlled laboratory (24�C 6 1�C, relative humidity25–35%). All participants were restricted from vigorousexercise from the day prior to the examination. Noneof the patients were taking any preventive drug at thetime the study was performed. Participants were not al-lowed to take analgesics or muscle relaxants throughthe 72 hours prior to the examination. PPTs were mea-sured bilaterally over masseter and temporalis muscles,the articular pillar of C5-C6 zygapophyseal joint (basedon palpation of C6-C7 spinous processes), the upper tra-pezius muscle (midway between C7 and acromion), andtibialis anterior muscle (upper one-third of the musclebelly) by an assessor blinded to the subject’s condition.The masseter and temporalis muscles were chosen as tri-geminal areas, the articular pillar of C5-C6 and the uppertrapezius muscle were chosen as the most common sitesof involvement in idiopathic neck pain, and the tibialisanterior was chosen as a remote distant site. The orderof assessment was randomized between the participants.

Pressure Pain Threshold DataManagement

In the current study, the magnitude of sensitizationwas investigated by assessing the differences of absoluteand relative PPT values between both groups. For rela-tive values, we calculated a ‘‘PPT Index,’’ dividing thePPT of each patient at each point by the mean of PPTscore of the control group at the same point. PPT indiceswere only calculated in those PPT levels significantly dif-ferent between patients and controls. A greater PPT In-dex (%) indicates lower degree of sensitization.

Statistical AnalysisData were analysed with the SPSS statistical package

(SPSS v.16.0; SPSS, Inc, Chicago, IL). Results are expressedas mean, standard deviation (SD), and 95% confidenceinterval (95% CI). The Kolmogorov-Smirnov test wasused to analyze the normal distribution of the variables(P > .05). Quantitative data without a normal distribution(ie, pain history, current level of pain, and NDI) were an-alyzed with nonparametric tests, whereas data witha normal distribution (PPT levels, BDI-II, and STAI) wereanalyzed with parametric tests. The intraclass correlationcoefficient (ICC) was used to evaluate the intraexaminerreliability of PPT data. A 2-way ANCOVA was used to in-vestigate the differences in PPT assessed over each point(masseter, temporalis, upper trapezius, tibialis anteriormuscles, and the C5-C6 zygapophyseal joint) with side

(dominant or nondominant) as within-subject factorand group (patients or controls) as the between-subjectfactor. A 2-way ANCOVA test was used for assessing thedifferences in PPT Index with side (dominant, nondomi-nant) as within-patient factor, point (masseter, tempora-lis, upper trapezius, tibialis anterior muscles, and theC5-C6 joint) as between-patient factor, and age, sex,BDI-II, and STAI scores as covariates. Post hoc compari-sons were conducted with the Bonferroni test. Finally,the Spearman’s rho (rs) test was used to analyze the asso-ciation between PPTs and the clinical variables relating tosymptoms, disability, anxiety, and depression. The statis-tical analysis was conducted at a 95% confidence leveland a P value less than .05 was considered statisticallysignificant.

Results

Demographic and Clinical Data of thePatients

Forty consecutive patients presenting with neck painbetween January and May 2009 were screened for possi-ble eligibility criteria. Seventeen patients were excluded:concomitant diagnosis RDC/TMD (n = 8), migraine (n = 5),and previous whiplash (n = 4). Finally, 23 patients (10men and 13 women) with mechanical neck pain, aged20 to 37 years (mean, 28 6 5 years; mean weight, 70 6

10 kg; mean height, 168 6 10 cm), and 23 matched con-trols, aged 20 to 38 years old (mean, 28 6 6 years; meanweight, 66 6 11 kg; mean height, 168 6 9 cm) were in-cluded. No significant differences between both groupsfor age (P = .9), weight (P = .3) and height (P = .8) werefound. Patients with neck pain showed greater levels(P < .001) of depression (BDI-II, 7.5 6 3) and anxiety(STAI, 22.4 6 3.2) as compared to controls (BDI-II, 3 6 3;STAI, 10 6 8, respectively).

Within the patient group, mean duration of neck painhistory was 10 6 4.6 months (95% CI 7.8–11.7 months),the mean intensity (NPRS) of neck pain was 3.6 6 1.5(95% CI 3.2–4.8), the mean NDI was 18.5 6 3.3 (95% CI17–20), the mean BDI-II was 7.5 6 1.6 (95% CI 6–9), andthe STAI was 22 6 3 (95% CI 21–24). Furthermore, posi-tive correlations between duration of pain history withcurrent level of pain (rs = .55, P = .007 [Fig 1A]) andBDI-II (rs =.58, P = .004 [Fig 1B]) were found: the longerthe duration of the symptoms, the greater the intensityof the perceived pain and the greater the self-reporteddepression. Further, current level of pain was also posi-tively correlated to disability (rs = .57, P = .004 [Fig 2A])and to BDI-II (rs = .64; P = .001, [Fig 2B]): the greater theintensity of the perceived pain, the greater the self-re-ported disability and the greater the self-reporteddepression.

Pressure Pain Sensitivity Over theTrigeminal Region

The intraexaminer repeatability of PPTreadings for themasseter and temporalis muscle was .9 and .92 for themost painful side and .91 for the contralateral side. Thestandard error of measurement (SEM) was .14 kg/cm2

Figure 1. Scatter plots of relationships between duration of history of neck pain and NPRS values (A) and between history ofneck pain and Beck Depression Inventory (B) A positive linear regression line is fitted to the data (NPRS: numerical pain rate scale,range 0 to 10).

La Touche et al 259

for the most painful side and .11 kg/cm2 for the contra-lateral side.

The ANOVA revealed significant differences betweenboth groups, but not between sides, for PPT levels overthe masseter (group: F = 257.3, P < .001; side: F = .58,P = .447) and temporalis (group: F = 124.8, P < .001;side: F = .06, P = .803) muscles. Over both muscles, pa-tients showed bilateral lower PPT levels than healthycontrols (P < .001). Table 1 summarizes PPT assessedover the masseter and temporalis muscles for both sideswithin each study group.

Pressure Pain Sensitivity Over theCervical Region

The intraexaminer repeatability of PPT over the C5-C6joint and the upper trapezius muscle was .91 for the mostpainful side and .89 for the contralateral side, respec-tively. The SEM was .11 and .13 kg/cm2 for the most pain-ful side and .15 kg/cm2 for the contralateral side.

The ANOVA revealed significant differences betweenboth groups, but not between sides, for PPT levels overthe upper trapezius muscle (group: F = 355.9, P < .001;side: F = .03, P = .851), and the C5-C6 zygapophyseal joint(group: F = 291.5, P < .001; side: F = .08, P = .776). Again,

Figure 2. Scatter plots of relationships between duration of NPRS pvalues and Beck Depression Inventory (B) A positive linear regression0 to 10).

patients showed bilateral lower PPT levels in both pointsas compared to healthy controls (P < .001). Table 1 showsPPT over the upper trapezius muscle and the C5-C6 zyga-pophyseal joint for both sides within each group.

Pressure Pain Sensitivity Over the TibialisAnterior Muscle

The intraexaminer repeatability of PPT over tibialis an-terior muscle was .93 for the most painful side and .91 forthe contralateral side, whereas the SEM was .18 and .2kg/cm2, respectively.

The ANOVA did not find significant differencesbetween groups and sides for PPT levels over the tibialisanterior muscle (group: F = 1.49, P = .461; side: F = .05, P =.824). Table 1 shows PPT over the tibialis anterior musclefor both sides within each group.

There was no effect of age, BDI-II, or STAI score on PPTlevels (P > .2), although there was an effect of sex at thetibialis anterior with females having lower PPTs (F = 8.8,P = .005) than males.

Pressure Pain Threshold IndicesThe ANOVA revealed significant differences for PPT

indices between sites (F = 8.7, P < .001), but not between

ain values and Neck Disability Index (A) and between NPRS painline is fitted to the data (NPRS: numerical pain rate scale, range

Table 1. Pressure Pain Thresholds (PPTs) in Patients With Mechanical Neck Pain (n = 23) andMatched Control Subjects (n = 23). Mean Values 6 Standard Deviation and 95% ConfidenceIntervals in Parenthesis (kg/cm2)

MECHANICAL NECK PAIN HEALTHY CONTROLS

DOMINANT SIDE NON-DOMINANT SIDE DOMINANT SIDE NON-DOMINANT SIDE

Trigeminal Area

Masseter* 2 6 .4 (1.8–2.2) 2 6 .5 (1.8–2.2) 3.4 6 .5 (3.2–3.6) 3.5 6 .4 (3.3–3.7)

Temporalis* 2.2 6 .5 (1.9–2.5) 2.1 6 .5 (1.9–2.4) 3.7 6 .6 (3.4–3.9) 3.6 6 .8 (3.4–3.9)

Joint

C5–C6* 1.7 6 .4 (1.5–1.9) 1.6 6 .3 (1.4–1.8) 3.2 6 .4 (3.1–3.4) 3.2 6 .6 (3.1–3.5)

Muscle

Upper trapezius* 1.8 6 .4 (1.6–2) 1.8 6 .3 (1.6–2) 3.8 6 .7 (3.6–4) 3.7 6 .5 (3.5–3.9)

Tibialis anterior 5.0 6 .8 (4.6–5.3) 5 6 .9 (4.6–5.4) 5.2 6 .7 (4.9–5.6) 5.3 6 .8 (5–5.7)

*Indicates significant difference between neck pain and control subjects (ANOVA, P < .001).

260 Trigeminal Pain Sensitivity in Neck Pain

sides (F = .03, P = .859). The post hoc analysis showedsignificant differences between both masseter and tem-poralis muscles with the upper trapezius muscle (P < .001)and between the temporalis muscles with the C5-C6 joint(P = .02). In such a way, the cervical region (upper trape-zius muscle and C5-C6 joint) showed lower PPT indices(greater degree of sensitization) compared to the tri-geminal region (masseter and temporalis muscles) forboth sides (Fig 3).

Pressure Sensitivity and Clinical Featuresin Patients with Mechanical Neck Pain

Finally, a significant negative correlation between his-tory of symptoms and PPT levels over both masseter mus-cles (dominant side: rs = –.64, P < .001 [Fig 4A];nondominant side: rs = –.42, P = .04 [Fig 4B]) was found:the longer the duration of the symptoms, the lower thePPT levels over both masseter muscles. In addition, cur-rent level of pain intensity was also negatively correlatedwith bilateral PPT levels over the masseter muscles (dom-inant side: rs = –.62, P < .001 [Fig 5A]; nondominant side:rs = –.51, P = .02 [Fig 5B]): the greater the pain intensity,the lower the bilateral PPT levels. No significant correla-tions between NDI, BDI-II, and PPT levels were found.

Figure 3. Pressure pain threshold indices in both trigeminaland cervical points. The boxes represent the mean and percen-tile scores, and the error bars represent the standard deviation.

DiscussionThis study showed bilateral pressure-pain hyperalgesia

in both the trigeminal and cervical region, but not overthe tibialis anterior muscle, in patients with mechanicalchronic neck pain as compared to healthy controls. Thedecrease in PPT levels over the trigeminal region was as-sociated with the intensity and duration of pain symp-toms, supporting a role of the peripheral nociceptiveinput as an important factor driving the developmentof spreading sensitization.

Current results of cervical, but not widespread, pressure-pain hypersensitivity in patients with idiopathic neck painare very similar to those previously found by Scott et al.33

The findings from both studies support the idea that me-chanical nontraumatic neck pain is characterized by pres-sure-pain hyperalgesia in the cervical spine, probably

reflecting peripheral nociceptor sensitization. Further-more, our study increases evidence that pressure-pain hy-peralgesia is not only restricted to cervical joints (C5–C6 orC2–C3 as previously reported) but also to cervical muscles(upper trapezius). This is expected since the upper trape-zius muscle receives nerve innervation from the C2–C4level. Nevertheless, lower PPT levels over the upper trape-zius may also be related to muscle spasm residing in theneck muscles in this patient population.

The present study demonstrated that patients withmechanical chronic neck pain also have pressure-pain hy-peralgesia in the trigeminal region. This finding may re-flect a sensitization process of the trigemino-cervicalnucleus caudalis due to the convergence of inputs from

Figure 4. Scatter plot of the relationship between duration of history of neck pain and PPT levels in both dominant (A) and nondom-inant (B) masseter muscles (n = 23). A negative linear regression line is fitted to the data (PPT: pressure pain threshold, kg/cm2).

La Touche et al 261

the trigeminal and cervical regions. In fact, neck-pain pa-tients included in the current study were completelyasymptomatic in the orofacial region, which supportsthat the pressure-pain hyperalgesia found over masseterand temporalis muscles reflects a sensitization process.Nevertheless, it seems that there is a greater sensitizationdegree in the cervical spine. This is supported by the factthat the magnitude of PPT changes was higher over theupper trapezius muscle (48–49%) and C5-C6 zygapophy-seal joint (51–53%) when compared to the magnitude ofPPT changes over the masseter (57–58%) and temporalis(60%) muscles. Nevertheless, there is no consensus aboutthe PPT that are needed to consider differences as realchanges.37 Different studies6,35,45 have suggested thatdifferences ranging from 123 kPa to 200 kPa (1.2–2 kg)are needed to consider real differences. In the currentstudy, differences between trigeminal (1.4–1.5 kg) andcervical regions (1.5–2 kg) were placed within this inter-val, so differences between both groups can be consid-ered as real.

Our results increase the evidence that nontraumaticneck pain is characterized by segmental, but not wide-spread, sensitization mechanisms that are mostlyrestricted to the trigemino-cervical region. The involve-ment of segmental sensitization mechanisms has beenreported in several local pain syndromes, eg repetitivestrain injury,18 chronic tension-type headache,13 low

Figure 5. Scatter plot of the relationship between duration of NPRinant (B) masseter muscles (n = 23). A negative linear regression line

back pain,27 osteoarthritis,1 carpal tunnel syndrome,15

and unilateral shoulder pain.16 The existence of sensiti-zation mechanisms in local pain syndromes suggeststhat sustained peripheral noxious input to the centralnervous system plays a role in the initiation and mainte-nance of sensitization process.26 This is supported by thefact that central sensitization is a dynamic conditioninfluenced by multiple factors, including activity of pe-ripheral nociceptive inputs.20 For instance, in insidiousmechanical neck pain, where there is no sudden nocicep-tive barrage to the central nervous system as in patientswith whiplash syndrome, a prolonged, continued noci-ceptive barrage from different cervical structures, eg,muscles12 or facet joints,3 may be capable of leading toimpairment in the nociceptive processing of the trige-mino-cervical nucleus caudalis. This was supported bythe fact that duration of symptoms was positively relatedto current level of pain and PPT levels over the massetermuscle. On the contrary, Scott et al33 found that durationof pain symptoms was not related to PPT levels over thecervical spine. It should be considered that patients in-cluded in the study by Scott et al have a greater durationof symptoms (mean: 51.5 6 40 months), were more dis-abled (NDI: 29 ± 16), and had greater levels of anxiety(STAI: 40.6 ± 11) than patients included in the presentstudy (duration of symptoms: 10 ± 4.6 months; NDI,18.5 6 3.3; STAI, 22.4 6 3.2), which may explain

S pain values and PPT levels in both dominant (A) and nondom-is fitted to the data (PPT: pressure pain threshold, kg/cm2).

262 Trigeminal Pain Sensitivity in Neck Pain

differences between both studies. Finally, we do notknow if sensitization mechanisms found in this studyare mediated via a deregulation of second-order neu-rons in a segmental fashion or via glia30 and other im-mune cells that reside in the trigeminal-cervical region.Future studies are needed to further elucidate the mech-anisms involved in trigemino-cervical sensitization inneck pain.

It has been suggested that anxiety and depression mayinfluence pressure-pain hypersensitivity.31 Our resultswere independent of levels of depression (BDI-II) andthe state anxiety (STAI). Additionally, patients includedin the present study showed scores < 8 points in theBDI-II, which are considered normal.2 Our results agreewith those previously reported by Scott et al33 in whichanxiety appears not to influence pressure-pain sensitivityin patients with insidious mechanical neck pain. Never-

theless, further studies investigating the influence ofpsychological factors are required.

ConclusionBilateral pressure-pain hyperalgesia was detected in

both trigeminal and cervical regions in patients with me-chanical chronic neck pain. The decrease in pressure painthresholds in the trigeminal region was associated withthe intensity and duration of the neck-pain symptoms,supporting a role of the peripheral nociceptive input asa driving factor for inducing sensitization. Our study fur-ther supports that nontraumatic neck pain shows sensiti-zation in the trigemino cervical region, which has clinicalimplications in terms of spreading symptomatology tothis body area.

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123

5.4 Estudio IV

La Touche R, Pardo-Montero J, Gil-Martínez A, Paris-Alemany A, Angulo-Díaz-Parreño S,

Suárez-Falcón JC, Lara-Lara M, Fernández-Carnero J. Craniofacial pain and disability

inventory (CF-PDI): development and psychometric validation of a new questionnaire. Pain

Physician. 2014 Jan-Feb;17(1):95-108.

Objetivo del estudio

El propósito de este estudio es presentar el desarrollo, el análisis de la estructura factorial y

propiedades psicométricas de un nuevo cuestionario auto-administrado (Inventario de dolor y

discapacidad craneofacial; IDD-CF), dirigido a medir el dolor, la discapacidad y el estado

funcional de la mandíbula y la región craneofacial.

Resultados

La versión final del IDD-CF consta de 21 ítems, el análisis factorial exploratorio reveló dos

factores ("El dolor y la discapacidad" y "el estado funcional de mandíbula"), ambos factores con

valor propio mayor que uno, que explican 44,77% de la varianza. No se observaron efectos

suelo o techo. Se confirmó una alta consistencia interna de la IDD-CF (α de Cronbach: 0,88) y

también para las dos subescalas (0,80 a 0,86 α de Cronbach). Basándose en el resultado de CCI

=0,90 (IC del 95% 0,86 hasta 0,93) fue considerado como una excelente fiabilidad test-retest. El

EEM y el MCD se calcularon como 2,4 y 7 puntos respectivamente. En la puntuación total

IDD-CF se observó una correlación moderada con la mayoría de los cuestionarios evaluados (r

= desde 0,36 hasta 0,52) y una fuerte correlación con el IDC (r = 0,65, p <0,001). El IDC, la

EVA y la TSK-11 fueron predictores del IDD-CF.

Conclusiones

El IDD-CF mostró buenas propiedades psicométricas. Con base en los hallazgos de este estudio,

el IDD-CF se puede utilizar en la investigación y la práctica clínica para la evaluación de los

pacientes con DCF.

Background: Orofacial pain, headaches, and neck pain are very common pain conditions in the general population and might be associated in their pathophysiology, although this is not yet clarified. The development and validation of a prediction inventory is important to minimize risks. Most recent questionnaires have not focused on pain, but pain is the common symptom in temporomandibular disorders, headaches, and neck pain. It is necessary to provide tools for these conditions.

Objectives: The purpose of this study is to present the development and analysis of the factorial structure and psychometric properties of a new self-administered questionnaire (Craniofacial Pain and Disability Inventory [CF-PDI]) designed to measure pain, disability, and functional status of the mandibular and craniofacial regions.

Study Design: Multicenter, prospective, cross-sectional, descriptive survey design. A secondary analysis of the reliability of the measures was a longitudinal, observational study.

Setting: A convenience sample was recruited from a hospital and 2 specialty clinics in Madrid, Spain.

Methods: The study sample consisted of 192 heterogeneous chronic craniofacial pain patients. A sub-sample of 106 patients was asked to answer the questionnaire a second time, to assess the test-retest reliability. The development and validation of the CF-PDI were conducted using the standard methodology, which included item development, cognitive debriefing, and psychometric validation. The questionnaire was assessed for the following psychometric properties: internal consistency (Cronbach’s α); floor and ceiling effects; test-retest reliability (Intraclass Correlation Coefficient [ICC]; Bland and Altman method); construct validity (exploratory factor analysis); responsiveness (standard error of measurement [SEM] and minimal detectable change [MDC]); and convergent validity (Pearson correlation coefficient), by comparing visual analog scale (VAS), the Tampa Scale for Kinesiophobia (TSK-11), the Pain Catastrophizing Scale (PCS), the Neck Disability Index (NDI), and the Headache Impact Test-6 (HIT-6). Multiple linear regression analysis was used to estimate the strength of the associations with theoretically similar constructs.

Results: The final version of the CF-PDI consists of 21 items. Exploratory factor analysis revealed 2 factors (“pain and disability” and “jaw functional status”), both with an eigenvalue greater than one, explaining 44.77% of the variance. Floor or ceiling effects were not observed. High internal consistency of the CF-PDI (Cronbach’s α: 0.88) and also of the 2 subscales (Cronbach’s α: 0.80 – 0.86) was confirmed. ICC was found to be 0.90 (95% confidence interval [CI] 0.86 – 0.93), which was considered to be excellent test-retest reliability. The SEM and MDC were 2.4 and 7 points, respectively. The total CF-PDI score showed a moderate correlation with most of the assessed questionnaires (r = 0.36 – 0.52) and a strong correlation with the NDI (r = 0.65; P < 0.001). The NDI, VAS, and TSK-11 were predictors of CF-PDI.

Limitations: Only self-reported measures were considered for convergent validity. Future research should use physical tests to explore the clinical signs relating to pain and disability.

Prospective Evaluation

Craniofacial Pain and Disability Inventory (CF-PDI): Development and Psychometric Validation of a New Questionnaire

From: 1Department of Physiotherapy, Faculty of Health Science, The Center

for Advanced Studies University La Salle. Universidad Autónoma de Madrid, Aravaca, Madrid, Spain;

2Research Group on Movement and Behavioral Science and Study of Pain,

The Center for Advanced Studies University La Salle, Universidad

Autónoma de Madrid; 3Institute of Neuroscience and Craniofacial Pain

(INDCRAN), Madrid, Spain; 4Hospital La Paz Institute for Health Research (IdiPAZ), Madrid, Spain; 5Faculty of

Medicine, Universidad San Pablo CEU, Madrid, Spain; 6Department

of Methodology of the Behavioural Sciences, Faculty of Psychology,

Universidad Nacional de Educación a Distancia, Madrid, Spain;

7Department of Neurology, Hospital Universitario La Paz, Madrid, Spain;

8Department of Physical Therapy, Occupational Therapy, Rehabilitation

and Physical Medicine, Universidad Rey Juan Carlos, Alcorcón, Madrid,

Spain

Address Correspondence: Roy La Touche

Facultad de Ciencias de la SaludCentro Superior de Estudios

Universitarios La SalleCalle la Salle, 10  

28023 Madrid SPAINEmail: [email protected]

Disclaimer: There was no external funding in the preparation of this

manuscript. Conflict of interest: Each author certifies that he or she, or a

member of his or her immediate family, has no commercial

association (i.e., consultancies, stock ownership, equity interest, patent/licensing arrangements, etc.) that

might pose a conflict of interest in connection with the submitted

manuscript.

Manuscript received: 06-21-2013 Accepted for publication: 08-25-2013

Free full manuscript:www.painphysicianjournal.com

Roy La Touche, PT, MSc1-3, Joaquín Pardo-Montero PhD1-3, Alfonso Gil-Martínez PT, MSc1-4, Alba Paris-Alemany PT, MSc2,3, Santiago Angulo-Díaz-Parreño MSc2,5, Juan Carlos Suárez-Falcón PhD6, Manuel Lara-Lara, MD7, and Josué Fernández-Carnero, PT, PhD2,8

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Pain Physician 2014; 17:95-108 • ISSN 1533-3159

Conclusion: The CF-PDI showed good psychometric properties. Based on the findings of this study, the CF-PDI can be used in research and clinical practice for the assessment of patients with craniofacial pain.

Key words: Craniofacial pain, temporomandibular disorders, headache, neck pain, disability, development, questionnaire, reliability, psychometric validation, minimal detectable change

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disability or dysfunction but not on pain, even though pain is the common symptom in TMD, headaches, and neck pain. Additionally, pain is been addressed by other validated scales (19).

For clinical practice and research, it is necessary to have tools to measure neck pain and the associated dis-ability (20). In addition, the development and validation of a prediction inventory allows the minimization of risks and helps prevent the development of the disease.

The purpose of this study is to present the de-velopment and analysis of the factorial structure and psychometric properties of a new self-administered questionnaire (Craniofacial Pain and Disability Inven-tory [CF-PDI]) designed to measure pain, disability, and functional status of the mandibular and craniofacial regions.

Methods

The development and validation of the CF-PDI was conducted in a standardized manner, using an accepted measure development methodology that included 3 phases (21): a) item development and identification of domains; b) pilot testing on a small number of patients with

cognitive debriefing; and c) psychometric validation.

Item DevelopmentItems were generated through a multi-step process

(21): 1) literature review; 2) patient interviews and focus group; 3) examination by the research group; 4) item writing and selection; and 5) examination of the inventory by independent

experts.

The relevant scientific literature search was con-ducted using electronic databases (Medline, Embase, CINAHL). The extracted information was related to the diagnosis, pathophysiology, comorbidities, and psycho-

Chronic orofacial pain and temporomandibular disorders (TMD) are commonly associated but may also arise from other sources (1). Orofacial

pain is a common pain condition associated with the hard and soft tissues of the face and mouth. Its prevalence in the general population is approximately 13% (2). Headache and neck pain are also 2 of the most common symptoms seen in the general population (3,4).

TMD, headaches, and neck pain are related dis-eases and share signs and symptoms (5-7). Some clinical evidence of the interconnection between the cervical spine and TMD has been demonstrated (8). Plesh et al (9) showed that 53% of patients with TMD had severe headache and 54% had neck pain. Besides, 59% with TMD reported at least 2 comorbid pains, and women reported more comorbid pain than men (9). This rela-tionship between headache and a causative disorder is a criterion for secondary headache diagnoses (10).

Although it has been suggested that TMD and headaches may be related in their pathophysiology (7,11) and that headache could be a possible risk factor for the development of neck pain (12), the pathophysi-ological mechanisms underlying these pain conditions are still not fully clarified. However, a biopsychosocial approach to the etiology, assessment, and treatment of chronic pain is widely advocated (13).

Nearly 60% of both men and women reported recent pain of moderate-to-severe intensity, with a quarter of them indicating interference or termination of work-related activities (14). Therefore, the correct diagnosis of these diseases is very important to reduce their huge economic impact (15,16).

A useful scale is the Jaw Functional Limitation Scale (JFLS), which consists of 3 constructs comprising a total of 20 items identified along a global scale (17). At present, there are no questionnaires in Spanish to as-sess these characteristics. This fact is especially relevant considering that Spain is one of the European Union countries with a high cost for these disabilities (18).

Moreover, most questionnaires have focused on

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social and disability factors associated with craniofacial pain. We found 5 published questionnaires that assess orofacial pain and jaw function (22-26). All of them were only validated in the English language. On the ba-sis of the existing literature, a semi-structured interview guide was developed focusing on the following 3 main areas: 1) perception of physical and psychosocial health in

relation to craniofacial pain; 2) patient-perceived physical impacts of the condition

(including impacts on general physical functioning and specific jaw function); and

3) perception of disability and pain associated with their condition.

A total of 13 patients with chronic craniofacial pain underwent the semi-structured interview and 5 patients with the same condition participated in the focus group. Both processes ended with the question: “Do you think there are any other aspects of craniofacial pain we have not discussed?” The research group proceeded to ana-lyze and compare the information extracted from semi-structured interviews, focus group, and review of the relevant literature to generate the construct concept of the CF-PDI and subsequently to write the items. A list of 30 draft items was generated. The research group then selected 22 items based on a finely structured consensus process (27) to not omit any necessary concepts.

The 22 items of the inventory were subjected to an external assessment by a group of experts in cra-niofacial pain (3 physiotherapists, one dentist, and one medical doctor). The 5 experts assessed whether each of the items had a relationship with the conditions of craniofacial pain and TMD, through a 3-level Likert scale (complete disagreement, neither agreement nor disagreement, and complete agreement).

Cognitive DebriefingCognitive debriefing of the preliminary CF-PDI

was conducted with a small number of patients to as-sess their interpretations of the questions (24 patients with craniofacial pain in the pilot test). Patients were selected from 3 different educational levels (primary school, secondary school, and university) and the total response time for all items of the CF-PDI was calculated. These patients were asked to complete the preliminary CF-PDI, and were then interviewed about its compre-hensiveness, relevance, and clarity of expression. This led to some minor alterations to the questionnaire.

Psychometric Validation

Sample/PatientsThis study employed a prospective, cross-sectional,

descriptive design. A consecutive convenience sample was recruited from outpatients of the Hospital Univer-sitario La Paz (Madrid, Spain) and 2 private clinics spe-cializing in craniofacial pain and TMD (Madrid, Spain). Patients were selected if they met all of the following criteria: 1) headache and facial pain, the diagnosis of which was made according to the guidelines of the In-ternational Classification of Headache Disorders (10); 2) headache or facial pain attributed to TMD (10), the di-agnosis of which was based on the Research Diagnostic Criteria for TMD (28,29) to classify patients with painful TMD (myofascial pain, temporomandibular joint [TMJ] arthralgia, or TMJ osteoarthritis); 3) pain history of at least 6 months prior to the study; 4) at least 18 years of age; and 5) good understanding of the Spanish language. The exclusion criteria were as follows: cogni-tive impairment; the presence of psychiatric limitations that impede participation in the study assessments; and poor knowledge of the Spanish language. To assess the test-retest reliability of the CF-PDI, a sub-sample of 106 patients whose clinical conditions were stable were asked to answer the inventory a second time, after an interval of 12 days.

The study was conducted in accordance with the Declaration of Helsinki and was approved by the local ethics committee of the Hospital Universitario La Paz (PI-1241). Prior to their participation, subjects gave written informed consent.

After consenting to the study, recruited patients were given a battery of questionnaires to complete on the day of the visit. These included various self-reports for demographic and pain-related variables, including the CF-PDI to be validated, a visual analog scale (VAS) for pain intensity, and the validated Spanish versions of the Tampa Scale for Kinesiophobia (TSK-11), the Pain Catastrophizing Scale (PCS), the Neck Disability Index (NDI), and the impact associated with headache was assessed using the Headache Impact Test-6 (HIT-6). The sociodemographic questionnaire collected information about gender, date of birth, marital status, living ar-rangements, education level, and work status.

Pain intensity was measured with the VAS. The VAS consists of a 100 mm line, on the left side of which represents “no pain” and the right side represents “the worst pain imaginable.” The patients placed a mark on

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the line where they felt best represented their pain intensity (30).

The Spanish version of the TSK-11 is a self-reported questionnaire that assesses fear of re-injury due to movement (31). The TSK-11 is an 11-item questionnaire that eliminates psychometrically poor items from the original version of the TSK (32) to create a shorter ques-tionnaire with comparable internal consistency. The TSK-11 has a 2-factor structure: activity avoidance and harm, and has demonstrated acceptable psychometric properties (31).

The Spanish version of the PCS assesses the degree of pain catastrophization (33,34). The PCS has 13 items and a 3-factor structure: rumination, magnification, and helplessness. The theoretical range is between 0 and 52, with lower scores indicating less catastrophizing. The PCS has demonstrated acceptable psychometric proper-ties (33).

The Spanish version of the NDI measures perceived neck disability (20,35). This questionnaire consists of 10 items, with 6 possible answers that represent 6 levels of functional capacity, ranging from 0 (no disability) to 5 (complete disability) points. The NDI has demonstrated acceptable psychometric properties (20).

The Spanish version of the HIT-6 (36,37) is a 6-item questionnaire that measures the severity and impact of headache on the patient’s life. The HIT-6 has demon-strated acceptable psychometric properties (38).

Statistical AnalysisSocio-demographic and clinical variables of the pa-

tients were analyzed. Analysis of variance (ANOVA) was used to test for differences in socio-demographic and clinical characteristics between the groups of patients.

Weighted kappa statistics (39) were calculated to assess the percentage agreement between external expert evaluators. Kappa statistics were calculated for each item. The Kappa coefficient varies from -1 (com-plete disagreement) to +1 (complete agreement), with 0 representing neither agreement nor disagreement.

Factor AnalysisThe factor structure was investigated using an

explorative factor analysis (ie, principal component analysis [PCA]) with Oblimin rotation. The number of factors for extraction was based on Kaiser’s eigenvalue criterion (eigenvalue ≥1) and evaluation of the scree plot (40). The quality of the factor analysis models was assessed using Bartlett’s test for sphericity and the Kai-ser-Meyer-Olkin (KMO) test. Bartlett’s test is a measure

of the probability that the initial correlation matrix is an identity matrix and should be < 0.05 (41). The KMO test measures the degree of multicollinearity and varies between 0 and 1 (should be greater than 0.50 – 0.60) (42).

Reliability For reliability, internal consistency and reproduc-

ibility were examined. Internal consistency was estimat-ed using Cronbach’s α and item total correlation coef-ficients. For a questionnaire to be internally consistent, α levels should be above 0.7 (43).

The test-retest reliability (repeatability) was evalu-ated using the Intraclass Correlation Coefficient (ICC). An ICC value above 0.70 is considered acceptable (44). We also constructed a Bland Altman Plot by calculating the mean difference between 2 measurements and the standard deviation (SD) of the difference (45). In this plot, 95% of the differences are expected to be less than 2 SDs.

Floor and Ceiling EffectsPotential floor and ceiling effects were measured

by calculating the percentage of patients indicating the minimum or maximum possible scores in the question-naires. Floor and ceiling effects are considered to be present if more than 15% of respondents achieved the highest or lowest possible total score (44).

Responsiveness AnalysesMeasurement error is the systematic and random

error of a patient’s score that is not attributable to true changes in the construct to be measured (46). Measure-ment error is expressed as a standard error of measure-ment (SEM), which is calculated as:

SD where SD is the SD of values from all participants

and ICC is the reliability coefficient (47,48). Ostelo et al (49) suggested that the percentage of the SEM in rela-tion to the total score of a questionnaire is an impor-tant indicator of agreement, and can be interpreted as follows: ≤ 5% very good; > 5% and ≤ 10% good; > 10% and ≤ 20% doubtful; and > 20% negative. Responsive-ness was assessed with the Minimal Detectable Change (MDC). The MDC expresses the minimal magnitude of change required to be 95% confident that the observed change between the 2 measures reflects real change and not just measurement error (50). It is calculated as SEM × × 1.96 (50,51).

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Convergent Validity The convergent validity was assessed by the Pear-

son correlation coefficient between the CF-PDI and the other questionnaires: VAS, TSK-11, PCS, NDI, and HIT-6. A strong correlation was considered to be over 0.60; a moderate correlation between 0.30 and 0.60; and a low (very low) correlation below 0.30 (44).

Linear RegressionMultiple linear regression analysis was used to esti-

mate the strength of the associations with theoretically similar constructs, so multiple linear regression analyses were also performed including CF-PDI as a criterion variable to estimate the strength of the association between CF-PDI and NDI, PVAS, TSK, and PCS as pre-dictor variables. As a measure of multicollinearity, the variance inflation factor (VIF) is presented (VIF < 10 indicates no problem with multicollinearity).

All statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS), version 20 (IBM company, USA) except for the SEM and MDC values, which were calculated using Microsoft Excel. The critical value for significance was P < 0.05.

Results

Item Development and Cognitive DebriefingA total of 18 patients with chronic craniofacial

pain participated in the focus group and were also interviewed in May 2011 and July 2011, and 30 items were pooled as potential questions. After a review by the research group, some questions were added, and 22 items covering 4 aspects (quality of life, jaw functional status, avoidance behavior, and pain) were finally gen-erated. There was agreement among the expert evalu-ators who reviewed the items, with a kappa coefficient of 0.83. The greatest disagreement occurred in items 8 and 20.

A pilot test for cognitive debriefing was performed in 24 patients in September 2011 to examine the con-tent validity of the preliminary questionnaire in regards to relevance and clarity of the language. The mean ± SD age of the patients was 45.7 ± 13.5 years (range: 19 – 61), and 17 of the participants were women (70.8%). The time required to answer all the questions was 8.4 ± 3.1 minutes (range: 5.4 – 12.6). More than 96% of the patients could easily answer the questionnaire.

Characteristics of the SampleThe final study sample consisted of 192 heteroge-

neous chronic craniofacial pain patients (68.8% women, one patient was of unknown gender) aged 19 – 78 years (mean ± SD: 46.00 ± 13.06). The vast majority of patients (28.1%) had myofascial pain diagnoses; other patients suffered from TMJ arthralgia (15.1%), headache or fa-cial pain attributed to TMD (myofacial pain/TMJ osteo-arthritis or arthralgia) (24.5%), combined tension-type headache and myofascial pain (16.7%), and migraine (15.6 %). The mean time of pain was 130.46 ± 151.44 months (range: 15 – 888), and 19 patients (9.9%) had received disability benefits. Educational levels in our sample were primary (23.4%), secondary (36.5%), and university graduates (25.0%); there was no information for 15.1% of our sample.

Distribution of Total CF-PDI ScoresThe distribution of CF-PDI scores did not differ

significantly from a normal symmetric distribution (skewness = 0.43, SE = 0.18; kurtosis = -0.36; SE = 0.35), Kolmogorov-Smirnov Z = 1.11 (P = 0.172). There were no significant differences in scoring between men (19.46 ± 9.04) and women (20.52 ± 9.22). There was no significant association between CF-PDI scores and age, marital status, average duration of pain, education level, or work status.

Only the type of diagnosis showed differences in the median score of CF-PDI, headache or facial pain attributed to the TMD (myofacial pain/TMJ osteoarthri-tis or arthralgia) group presented higher scores 28.62 ± 7.10; TMJ arthralgia, 14.2 ± 5.24; migraine, 17.93 ± 12.30; myofascial pain, 18.17 ± 6.44; combined tension-type headache and myofascial pain, 19.00 ± 7.05. The distribution of CF-PDI total scores and other principal scales are shown in Table 1.

Table 1. Descriptive statistics and estimates of internal consistency (N = 192).

Instrument Mean (SD) Range Alpha

CF–PDI 20.24 (9.15) 2–48 0.88

Pain and Disability 15.43 (6.77) 1–34 0.86

Jaw Functional Status 4.81 (3.57) 0–14 0.80

HIT–6 54.48 (7.67) 36–74 0.85

NDI 16.96 (6.00) 0–42 0.74

TSK–11 25.40 (7.08) 11–44 0.88

PCS 23.86 (8.90) 7–52 0.84

VAS 52.94 (13.83) 15–85 –––

CF-PDI, craniofacial pain and disability inventory; VAS, visual analogue scale; TSK-11, Tampa Scale for Kinesiophobia; PCS, pain catastrophizing scale; NDI, Neck Dibility Index; HIT-6, headache impact test-6

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Internal ConsistencyCronbach’s α coefficient was 0.88 (95% CI = 0.86 –

0.91), indicating a high degree of internal consistency. The item-to-total correlation coefficients ranged from 0.32 to 0.73; no item dominated with an especially high correlation and no item appeared to be redun-dant. The previous item 20, “How long have you had pain?” was deleted in the final version and it increased slightly the Cronbach’s α coefficient. This item showed a strong positive skew, refers to the time of pain in our population, and shows limited information because all patients suffered from chronic pain. It was removed it; other results in Table 2.

Factor AnalysisIn order to explore the factorial structure of the

instrument, a PCA without rotation was conducted on the scores of our sample. We also attempted to con-struct one-, 2-, and 3-factor structures. A 2-factor solu-tion emerged in our sample using a PCA that explained 40.8% of the variance. The KMO was found to be 0.85, which exceeds the recommended minimum value of 0.60. Bartlett’s Test of Sphericity was highly significant (Chi square = 1467.10 P < 0.001), supporting the suit-ability of the data for PCA.

When factor loading smaller than 0.30 was sup-pressed, but there were no cases. The first factor (30.43% of the explanatory variance) was composed of 14 items (1, 2, 3, 4, 5, 6, 7, 8, 16, 17, 18, 19, 20 (previously 21), and 21 (previously 22); the second factor (10.39% of the explanatory variance) was composed of 7 items (9, 10, 11, 12, 13, 14, and 15). With these results and a visual inspection of the scree plot, a 2-factor solution was considered suitable (Fig. 1).

Regarding factor analysis, item 9 was not clearly classified into the assumed factor (with loadings un-der 0.35 in each of them). The results showed similar weights for both factors. Despite the unexpected load-ing of this item, the CF-PDI still showed appropriate internal consistency; therefore, we incorporated it into the jaw functional status domain for theoretical rea-sons. Results of the PCA are shown in Table 3.

Floor and Ceiling EffectsNo floor or ceiling effects were identified for the

whole scale. Only 9.3% of the respondents scored the lowest possible score of 0 in the jaw functional status subscale, and none of the craniofacial pain patients scored the highest possible score of 63 points on the CF-PDI.

Table 2. Corrected item-total between CF-PDI items (N = 192)

Scale mean if item deleted

Corrected item-total correlation

Squared multiple correlation

Cronbach's α if item deleted

1 18.65 0.73 0.63 0.87

2 18.72 0.46 0.37 0.88

3 18.58 0.54 0.55 0.88

4 19.61 0.47 0.56 0.88

5 19.82 0.53 0.51 0.88

6 19.88 0.34 0.31 0.88

7 19.19 0.50 0.36 0.88

8 19.56 0.35 0.23 0.88

9 19.49 0.32 0.21 0.88

10 19.30 0.59 0.57 0.87

11 19.34 0.53 0.54 0.88

12 19.41 0.41 0.48 0.88

13 19.70 0.55 0.54 0.88

14 19.79 0.40 0.50 0.88

15 19.83 0.43 0.46 0.88

16 18.29 0.64 0.56 0.87

17 18.58 0.57 0.46 0.87

18 19.33 0.44 0.30 0.88

19 19.30 0.44 0.37 0.88

20 19.22 0.47 0.36 0.88

21 19.19 0.38 0.25 0.88

Fig. 1. Scree plot of the 21 items of the CF-PDI.

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Test-Retest ReliabilityThe response to the CF-PDI provided by a random

subsample of 106 patients (gender women: 70, 66.7%; age: 45.6 ± 12.9 years; duration of the disorders: 69.0 ± 46.2 months) showed satisfactory temporal stability of

the scale after 12 days. ICC based on absolute agree-ment measures was 0.90 (95% CI: 0.86 – 0.93). The con-structed Bland and Altman plot for test-retest agree-ment showed a good reliability for total CF-PDI score

Table 3. Items of CF-PDI distribution and factor loadings according to principal component analysis with Oblimin rotation including Kaiser correction (N = 192).

Factor 1 Factor 2

1 ¿Presenta dolor en la cara? Do you feel any pain in your face? 0.79 0.45

2 ¿Se ha visto afectada su calidad de vida por esta dolencia? Is your quality of life affected by this pain? 0.58 0.21

3 Intensidad de dolor en la cara. Pain intensity on your face. 0.68 0.23

4 Le incapacita su dolor a la hora de tener relaciones afectuosas del tipo: besos, abrazos, relaciones sexuales… Does the pain make you unable to have emotional relationships, such as: kisses, embraces, or sexual relationships?

0.69 0.06

5 ¿Tiene dolor al reír? Do you feel any pain when you laugh? 0.68 0.19

6 ¿Su dolencia hace que evite el sonreír, hablar o masticar?Does your condition make you avoiding smiling, talking or chewing? 0.44 0.13

7. ¿Tiene dolor en la mandíbula?Do you feel any pain in your jaw? 0.53 0.38

8 ¿Escucha algún ruido al mover la mandíbula?Do you hear any noise when you move your jaw? 0.40 0.23

9. ¿Nota que su mandíbula se le sale o se le traba?Do you feel your jaw getting out of place or getting stuck? 0.33 0.31

10. Intensidad de dolor al masticarPain intensity when chewing 0.47 0.72

11. ¿Siente cansancio en la mandíbula, al hablar o al comer?Do you feel any tiredness in your jaw when you talk or eat? 0.38 0.73

12. ¿Tiene dificultad para abrir la boca?Do you have any trouble when you open your mouth? 0.23 0.73

13. Intensidad de dolor al hablarPain intensity when talking. 0.40 0.74

14. ¿Tiene miedo de mover la mandíbula?Do you fear moving your jaw? 0.20 0.73

15. Alimentación.Nutrition 0.24 0.72

16. ¿Con qué frecuencia tiene dolor en el cuello?How often have you got any neck pain? 0.76 0.31

17.¿Con qué frecuencia tiene dolor de cabeza?How often do you have a headache? 0.61 0.41

18. ¿Con qué frecuencia tiene dolor de oído?How often do you have an earache? 0.47 0.34

19. ¿Qué siente al tocarse la zona dolorosa?What do you feel when you touch the painful area? 0.53 0.23

20 ¿Su dolor le altera el sueño?Does the pain disrupts your sleep? 0.59 0.21

21 ¿El dolor le interfiere a la hora de desempeñar su actividad laboral?Does the pain interfere in your work? 0.38 0.36

and 2 subscales (Figs. 2-4). The results of reliability and responsiveness analy-ses are summarized in Table 4.

Convergent ValidityThe total CF-PDI score was signifi-

cantly associated with all the assessed questionnaires (Table 5), but the cor-relation with the NDI, was the most important in our sample.

Linear RegressionThe resulting beta coefficients,

ranging from 0.50 to 0.17, indicate independent contribution of each scale to the prediction of CF-PDI, the criteri-on variable. NDI, VAS, and TSK-11 were predictors of CF-PDI, significance < 0.05 (as illustrated by the higher standard-ized coefficients [beta] and P-values). NDI was the most important variable (Table 6). PCS and HIT-6 were excluded as predictor variables this time.

discussion The present study describes a

methodical approach to the develop-ment and validation of a new self-ad-ministered questionnaire to measure disability, pain, and functional status of the mandibular and craniofacial region in patients with craniofacial pain. Our results demonstrate that the CF-PDI is psychometrically valid and reliable. In addition, the instrument has proven to be easy to complete, and only requires a relatively short time to administer. The CF-PDI was de-veloped in Spain for Spanish patients with craniofacial pain and TMD. How-ever, since the CF-PDI does not contain items that are specifically related to Spanish culture, it could be translated and used internationally.

The design of the CF-PDI was based on a biopsychosocial approach. This conceptual model, recommended by the International Classification of Functioning Disability and Health (52,53), can assess the disease from a

Fig. 2. Bland Altman plot illustrating the test-retest reliability of the CF-PDI. A total of 106 patients participated in the test-retest assessment. The central line representing the mean difference between test and retest scores, which was - 2.22, and the 95% limits of agreement are presented as flanking lines.

Fig. 3. Bland Altman plot illustrating the test-retest reliability of the Pain and Disability subscale. A total of 106 patients participated in the test-retest assessment. The central line representing the mean difference between test and retest scores, which was -1,73, and the 95% limits of agreement are presented as flanking lines.

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Fig. 4. Bland Altman plot illustrating the test-retest reliability of the Jaw Functional Status subscale. A total of 106 patients participated in the test-retest assessment. The central line representing the mean difference between test and retest scores, which was -0.49, and the 95% limits of agreement are presented as flanking lines.

Table 4. Descriptive statistics, test-retest reliability, and responsiveness results (N = 106)

DomainsTest Retest

ICC 95% CI SEM MDCMean SD Mean SD

CF-PDI 20.57 8.42 22.79 7.80 0.90 0.86-0.93 2.48 6.87

Pain and Disability 15.37 6.13 17.10 5.26 0.86 0.81-0.90 2.10 5.82

Jaw Functional Status 5.20 3.39 5.69 3.93 0.86 0-80-0.90 1.35 3.75

CF-PDI, craniofacial pain and disability inventory; SD, standard deviation; ICC, intraclass correlation coefficient; 95% CI, 95% confidence interval; SEM, standard error of measurement; MDC, minimal detectable change

broader perspective, and provides an understanding of health, functioning, and disability. In addition, research sup-ports that clinical diagnosis is sometimes insufficient to explain patients’ pain and disability (54-56).

The scree plot and exploratory fac-tor analysis revealed a 2-factor solution. Both factors had eigenvalues greater than 1. PCA indicated that a satisfactory percentage of total variance (40.8%) was explained by the 2 factors. The CF-PDI contains 21 items divided into 2 subscales according to their content and exploratory factor analysis: “pain and disability” and “jaw functional status.”

High internal consistency was shown for the CF-PDI (Cronbach’s α: 0.88) and also for the 2 subscales (Cron-bach’s α: 0.80 – 0.86). These data are similar to the results from other research questionnaires used to assess facial pain and mandibular function (22-25,57,58).

Table 5. Pearson Correlation Coefficient of our principles scales (N = 192).

CF-PDI Pain and Disability Jaw Functional Status

VAS 0.46** 0.50** 0.23**

NDI 0.65** 0.69** 0.37**

PCS 0.46** 0.50** 0.25**

PCS rumiation 0.34** 0.35** 0.22**

PCS magnification 0.51** 0.52** 0.32**

PCS Helplessness 0.39** 0.45** 0.16*

TSK-11 0.40** 0.41** 0.26**

HIT6 0.38** 0.46** 0.09

** P < 0.01; * P < 0.05Abbreviations: CF-PDI, craniofacial pain and disability inventory; VAS, visual analogue scale; TSK-11, Tampa Scale for Kinesiophobia; PCS, pain catastrophizing scale; NDI, Neck Disability Index; HIT-6, headache impact test-6

Pain Physician: January/February 2014; 17:95-108

104 www.painphysicianjournal.com

In this study, we choose a retest interval of 12 days (approximately), in order to avoid variations in clinical status and patients remembering their previous an-swers. A longer interval for a test-retest study of health may be inappropriate as fluctuations in the patient’s health status can occur (59). In relation to this, Streiner and Norman suggested that a retest interval of 2 to 14 days is generally acceptable (60).

The test-retest reliability for the total CF-PDI score was considered to be excellent (ICC: 0.90; 95% CI: 0.86 – 0.93). Also, we were able to verify that the test-retest reliability was high for each subscale.

The measurement of SEM was 2.4 points, corre-sponding to 11.7% of the mean CF-PDI values and 3.8% of the maximum possible score. Based on the SEM, the MDC was 7 points (34.5% of mean values). Considering that the score of the questionnaire ranges from 0 to 63 points, 7 points represents 11.1% of the maximum pos-sible score, which means that the CF-PDI is able to de-

tect very small changes. Changes higher than the MDC can be interpreted as real and not due to measurement error, with an acceptable probability level. These results may help to calculate the sample size of future studies aiming to assess the effectiveness of craniofacial pain interventions.

Construct validity was evidenced by significant cor-relations between the CF-PDI with all the questionnaires and scales used in the validation process. A moderate correlation between CF-PDI with the HIT-6 and the VAS (r = 0.38 – 0.46) was observed. In addition, the PCS and TSK-11 showed moderate correlation with the CF-PDI and the pain and disability subscale (r = 0.36 – 0.52). This is consistent with recent evidence demonstrating that patients with craniofacial pain or craniomandibular dis-orders report higher levels of catastrophizing (61-63). Furthermore, pain-related catastrophizing has been associated with the progression of pain intensity and signs of disability in chronic craniofacial pain (64-68).

Table 6. Multiple linear regression models with CF-PDI (A), pain and disability (B), and jaw functional status (C) as criterion variable, and NDI, VAS, TSK-11, PCS as predictor variables (N = 192).

Criterion variable Predictor variablesRegression coefficient

(B)

Standardized coefficient (β)

Significance (P) VIF

A. CF-PDI

NDIVASTSK-11

0.770.130.22

0.500.190.17

0.0000.0010.004

1.371.261.17

Excluded variables

PCS-TotalHIT-6

----

0.080.01

0.2530.905

1.621.46

B. Pain and Disability

NDIPCS-MagnificationVAS

0.550.680.10

0.490.250.21

0.0000.0000.000

1.371.261.17

Excluded variables

PCS-TotalTSK-11HIT-6PCS-RumiationPCS-Helplessness

----------

-0.500.090.08-0.06-0.00

0.4800.0980.1590.3140.968

0.400.770.680.700.61

C. Jaw Functional Status

NDIPCS-magnification

0.170.28

0.290.20

0.0000.007

1.221.22

Excluded variables

PCS-TotalTSK-11HIT-6PCS-RumiationPCS-HelplessnessVAS

------------

-0.130.09-0.13-0.00-0.160.06

0.2070.2580.0760.9680.0590.436

2.491.291.331.421.651.26

CF-PDI, craniofacial pain and disability inventory; VAS, visual analogue scale; TSK-11, Tampa Scale for Kinesiophobia; PCS, pain catastrophizing scale; NDI, Neck Dibility Index; HIT-6, headache impact test-6, VIF, variance inflation factor

www.painphysicianjournal.com 105

Psychometric Validation of the Craniofacial Pain and Disability Inventory

Previous research demonstrated the relationship between fear of jaw movements and craniofacial pain (69,70), but only limited evidence supports it. However, there is higher evidence showing that pain-related fear is associated with reduced activities in daily life and is also a strong predictor of disability in other chronic musculoskeletal disorders (71-75).

Pain catastrophizing and pain-related fear are 2 constructs that have been linked to the chronicity of musculoskeletal pain through the “fear avoidance model” (76). Based on the results of multiple linear regression analysis, pain intensity (VAS: β = 0.19, P = 0.001) and fear of pain and movement (TSK-11: β = 0.17, P = 0.004) were predictors of CF-PDI. For jaw functional status, and pain and disability, the variable predictor was pain catastrophizing (PCS-Magnification: β = 0.25, P < 0.001; β = 0.20, P = 0.007).

The principal predictor for CF-PDI and the 2 sub-scales was the variable of neck disability (NDI: β = 0.29 – 0.50, P < 0.001). In addition, a strong correlation was observed between CF-PDI and pain and disability factor with NDI (r = 0.65 – 0.69). This is in line with the results of Olivo et al (77) who described a strong relationship between neck disability and jaw disability (r = 0.82). Several studies have reported the high prevalence and comorbidity between orofacial pain, TMD, headache, and neck pain (65,78-81). Our findings suggest the importance of taking into account the neck disability questionnaires when assessing patients with craniofa-cial pain.

Limitations Our study has several limitations. First, there is

a gender disproportion as the sample had a smaller proportion of men. However, our findings showed no significant differences in scoring between genders. The evidence suggests that the prevalence of craniofacial pain is higher in women (82).

The second limitation of this study is that we did not assess the CF-PDI in healthy subjects; the sample consisted of patients with chronic pain. Further

studies will need to be performed to assess the dis-criminant power of the CF-PDI for specific diagnostic entities.

The sample size was sufficient to test the new in-strument’s reliability, convergence validity, and explor-atory factor analysis. However, it was too small to be able to carry out confirmatory factor analysis. Kline has suggested a sample size of 10 – 15 subjects per item to perform this statistical analysis (83). It should be noted that statisticians disagree on the issue of appropriate sample size for confirmatory factor analyses. In relation to this, DeVellis stated that as the sample size becomes larger, the relative number of respondents per item can diminish (84), and that a sample of 200 is adequate in most studies (85).

Another limitation is that only self-reported mea-sures were considered for convergent validity. Future research should use physical tests to explore the clinical signs relating to pain and disability, and assess whether these are associated with the CF-PDI.

The last limitation of the study is the cross-sectional design, which prevented us from investigating the abili-ty of the CF-PDI to detect responsiveness to change over time. Although in this study we investigated in a short period of time the reproducibility and the MDC, a longi-tudinal study or one with an experimental design with a follow-up period would be required to understand how CF-PDI scores change over time. Furthermore, such a study would allow us to obtain information such as the Minimum Clinically Important Difference.

conclusion Evidence has shown that the CF-PDI has a good

structure, internal consistency, reproducibility, and construct validity, and provides an objective tool for as-sessing pain and disability in craniofacial pain patients. Neck disability showed a strong association with the CF-PDI, and is also a significant predictor of the construct. Based on the findings of this study, the CF-PDI could be used in research and clinical practice for the assessment of treatment outcomes.

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138

5.5 Estudio V

La Touche R, Paris-Alemany A, Gil-Martínez A, Pardo-Montero J, Angulo-Díaz-Parreño S,

Fernández-Carnero J. The Influence of Neck Disability and Pain Catastrophizing about

Trigeminal Sensory-Motor System in Patients with Headache Attributed to Temporomandibular

Disorders. (En revisión)

Objetivos de estudio

Nuestro objetivo fue estudiar la influencia de la discapacidad y el dolor de cuello sobre las

variables sensoriales y motoras del trigémino en pacientes con cefalea atribuida a TCM.

Resultados

Los resultados de EVAF fueron mayores a 6 minutos (media 51,7, IC 95%: 50,15-53,26) y 24

horas después (21.08, IC 95%: 18,6-23,5) para las pruebas en el grupo que muestran

discapacidad moderada cuello en comparación con el grupo de discapacidad leve cuello (6

minutos, 44,16, IC del 95%: 42,65 a 45,67 / 24 horas después, 14,3; IC del 95%: 11,9-16,7) y el

grupo de control (6 minutos, 29.92, IC 95% 28,29-31,55 / 24 horas después, 4,65; IC del 95%:

2.5 a 7.24). El análisis muestra una disminución en el MAI sin dolor inmediatamente después de

las pruebas de todos los grupos y se observó que esta disminución sólo se mantuvo en el grupo

de discapacidad moderada 24 horas después de la prueba. Los UDPs de la región del trigémino

se redujeron inmediatamente en todos los grupos, mientras que a las 24 horas se observó una

disminución sólo en los grupos de pacientes. Los UDPs de la región cervical disminuyeron sólo

en el grupo con discapacidad cuello moderado 24 horas después de la prueba. La correlación

negativa más fuerte se encontró entre MAI sin dolor inmediatamente después de la prueba y el

IDC en ambos grupos: grupo de discapacidad leve (r = -0.49, P <0,001) y grupo de discapacidad

moderada (r = -0.54, P <0,001).

Conclusiones

Nuestros resultados sugieren que la discapacidad y dolor de cuello tienen una influencia en las

variables sensomotrices evaluados en pacientes con cefalea atribuida a TCM.

1

The Influence of Neck Disability and Pain Catastrophizing about Trigeminal

Sensory-Motor System in Patients with Headache Attributed to

Temporomandibular Disorders

Roy La Touche,1-4, Alba Paris-Alemany 1-4, Alfonso Gil-Martínez1-4, Joaquín Pardo-

Montero1-4, Santiago Angulo-Díaz-Parreño, Josué Fernández-Carnero,2,4,6.

1. Department of Physiotherapy, Faculty of Health Science, The Center for Advanced Studies

University La Salle. Universidad Autónoma de Madrid, Aravaca, Madrid, Spain.

2. Motion in Brains Research Group, The Center for Advanced Studies University La Salle,

Universidad Autónoma de Madird.

3. Institute of Neuroscience and Craniofacial Pain (INDCRAN), Madrid, Spain

4. Hospital La Paz Institute for Health Research, IdiPAZ. Madrid, Spain.

Madrid, Spain

5. Faculty of Medicine, Universidad San Pablo CEU, Madrid, Spain

6. Department of Physical Therapy, Occupational Therapy, Rehabilitation and Physical

Medicine, Universidad Rey Juan Carlos, Alcorcón, Madrid, Spain.

Address for reprint requests / Corresponding author:

Roy La Touche

Facultad de Ciencias de la Salud

Centro Superior de Estudios Universitarios La Salle.

Calle la Salle, 10

28023 Madrid

SPAIN

Telephone number: + 34 91 7401980 (EXT.256)

Fax number:

Email address: [email protected]

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ABSTRACT

OBJECTIVE: Our purpose was to investigate the influence that neck pain and disability

may have on trigeminal sensory-motor variables in patients with headache attributed to

TMD.

METHODS: An experimental case-control study comprising 83 patients with headache

attributed to TMD and 39 healthy controls was done. Patients were grouped according

to their scores on the neck disability index (NDI) (mild and moderate neck disability).

Initial assessment included the visual analogue scale (VAS), pain catastrophizing scale,

NDI and the Headache Impact Test-6. The protocol consisted of baseline measurements

of pressure pain thresholds (PPT) for mechanical pain sensitivity in the trigeminal and

cervical region and the pain-free maximum mouth opening (MMO), performance of the

provocation chewing test, immediately after data collection and 24 hours after. During

the provocation chewing test, patients were assessed for subjective feelings of fatigue

(VAFS) and pain intensity, immediately and 24 hours after completion.

RESULTS: The VAFS were higher at 6 minutes (mean 51.7; 95% CI: 50.15-53.26) and

24 hours after (21.08; 95% CI: 18.6-23.5) for tests in the group showing moderate neck

disability compared with the mild neck disability group (6 minutes, 44.16; 95% CI

42.65-45.67/ 24 hours after, 14.3; 95% CI: 11.9-16.7) and the control group (6 minutes,

29.92; 95% CI 28.29-31.55/ 24 hours after, 4.65; 95% CI: 2.05-7.24). The analysis

shows a decrease in the pain-free MMO immediately after the tests for all groups and

this decrease was observed only in the group of moderate disability 24 hours after the

test. PPTs of the trigeminal region were decreased immediately in all groups, whereas at

24 hours a decrease was observed only in the groups of patients. PPTs of the cervical

region decreased only in the group with moderate neck disability 24 hours after the test.

The strongest negative correlation was found between pain-free MMO immediately

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after the test and NDI in both groups: mild (r=-0.49; P<0.001) and moderate (r=-0.54;

P<0.001) neck disability group.

CONCLUSION: Neck pain and disability have an influence on the sensory-motor

variables evaluated in patients with headache attributed to TMD.

KEYWORDS: Temporomandibular disorders, headache, neck pain, pain

catastrophizing, disability.

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.INTRODUCTION

Temporomandibular disorders (TMD), headaches and neck pain are very closely

related diseases[1]. Several studies have reported the overlapping signs and symptoms

among patients with TMD, headaches and neck pain, respectively[2, 3]. It has been

shown that neck pain complaints were also significantly associated with TMD[4, 5] and

that psychosocial factors have an influence on the presence of head, neck and orofacial

pain[3].

The prevalence of temporomandibular joint (TMJ) symptoms, orofacial pain,

neck pain and headache was assessed in 1339 non-patients. Often painless TMJ

symptoms were found in 10% of subjects, orofacial pain in 7%, headache in 15% and

neck pain in 39%[3]. Plesh et al. showed that 53% of patients with TMD had severe

headache and 54% had neck pain[6]. It has been suggested that TMD and headaches

may be involved in their pathophysiology[7, 8] and this headache could be a possible

risk factor for developing neck pain[9].

Recent research has shown a strong relationship between craniomandibular

disability and pain with cervical disability[10, 11]. Several experimental studies have

described functional connections between the craniofacial and cervical afferent fibres

via patterns of neural convergence of the trigeminal nucleus and the upper cervical

nociceptive neurons, which form a functional unit, the trigeminocervical complex[12–

18]. In relation to this, it has been observed in experimental studies that the pain

induced by the infiltration of algogenic substances in the masticatory or cervical

muscles can bi-directionally modify the activity of the stretch reflexes[13, 15]. Also, in

basic research, a reflex relationship has been observed between the activity of the

nociceptors of the TMJ and the activity of the fusimotor-muscle spindle system of the

cervical muscles[17]. This information is useful for proposing theories about the

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influence of the cervical region over the possible nociceptive and sensory-motor

mechanisms involved in masticatory fatigue, pain and alterations in motor behaviour. At

present, there is insufficient information demonstrating the influence of neck pain and

disability in the sensory-motor activity in patients with trigeminal headache attribute to

TMD. This could be a key issue, since improvements could be made by changing the

diagnostic and therapeutic approach to these patients. We used the primary hypothesis

that neck disability is a factor influencing masticatory sensory-motor activity in patients

with headache attributed to TMD.

Headache attributed to TMD is classified as a secondary headache caused by a

disorder that affects the temporomandibular region[19]. The pain may be unilateral or

bilateral and is represented in the facial region, at the masseter and temporal region[19].

An important criterion for clinical diagnosis is that the headache occurs or is aggravated

by provocative manoeuvres (such as the palpatory pressure on the TMJ and masticatory

muscles) and/or mandibular active or passive movements[19, 20]. Recently, it has been

found that the diagnostic criteria that have greater sensitivity and specificity for this

type of headache are: 1) the provocation of pain by palpation of the temporalis muscle

or jaw movements and 2) the fact that pain changes with the movements of the jaw in

the function or parafunction[20, 21].

From the clinical point of view, it is important to identify changes in motor

behaviour that may be present in patients suffering TMD, especially knowing that a

percentage of these patients develop painful chewing[22, 23], difficulty performing jaw

movements[24] and masticatory fatigue[25, 26].

During the last decades, the relationship between masticatory muscle pain and

disordered jaw motor behaviour has been studied widely; see for example the review by

Svensson and Graven-Nielsen[27]. Pain may influence the characteristics of the

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masticatory sensory-motor system[28]. Furthermore, Kurita et al. found a positive

correlation between chewing ability and TMJ pain and reduced mouth opening[29].

According to some researchers, fatigue and fatigue-related symptoms are reported

significantly more often by chronic TMD patients than by healthy volunteers[30]. In

addition, a recent study in patients with chronic orofacial pain demonstrated that fatigue

is mediated by psychosocial factors[31]. In this connection, Brandini et al. found a

positive association in TMD patients between mandibular kinematic variables and

psychological factors such as stress and depression[32].

Research or assessments based on a biobehavioural approach may offer a better

alternative for identifying patients with chronic TMD[33]; a biobehavioural approach to

the assessment and treatment of chronic pain is widely accepted[34]. A key point to

note about patients with headache attributed to TMD is that an association between

emotional functioning and increased frequency of headache has been found[35]. This

and previous findings lead us to propose integrating the assessment of psychological

factors with pain and disability associated with trigeminal sensory-motor variables in

this research. A significant amount of scientific evidence has shown the influence of

pain catastrophizing on several variables related to TMD[36–41]. This suggests the

hypothesis that pain catastrophizing has an association or is a predictor of some of the

trigeminal sensory-motor variables studied in this research.

The primary objective of this research is to investigate the influence that pain and

disability of the neck may have on trigeminal sensory-motor variables in patients with

headache attributed to TMD, and as a secondary objective we propose identifying

whether the psychological or disability variables have any association with the studied

sensory-motor variables.

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MATERIALS AND METHODS

Study Design

This was an experimental case-control study. The assessor of sensory-motor

measurements was blinded. One researcher administered the participant appointments

and questionnaires, and also instructed the participant not to say anything that could

reveal their pain, disability trait or state. The reporting of the study follows the

“Strengthening the Reporting of Observational studies in Epidemiology” (STROBE

statement) [42].

After receiving detailed information about the experiment, the volunteers gave

their written informed consent. All of the procedures used in this study were planned

under the ethical norms of the Helsinki Declaration and were approved by the local

ethics committee.

Participants

A consecutive convenience sample of 83 patients with chronic headache

attributed to TMD and 39 healthy controls were recruited for the study. The sample was

recruited from outpatients of a Public Health Centre (Madrid, Spain) and two private

clinics specializing in craniofacial pain and TMD (Madrid, Spain). Patients were

selected if they met all of the following criteria: 1) Headache and facial pain attributed

to TMD, diagnosis was made according to the guidelines of the International

Classification of Headache Disorders[19]; 2) TMD diagnosis based on the Research

Diagnostic Criteria for TMD[43, 44] to classify patients with painful TMD (myofascial

pain, TMJ arthralgia and TMJ osteoarthritis); 3) pain symptoms history of at least the 6

months previous to the study; 4) pain in the jaw, temples, face, neck, pre-auricular area,

or in the ear during rest or function; 5) neck pain and disability and quantified according

to neck disability index (NDI)[45]; and 6) At least 18 years of age.

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There were 83 patients categorized into two groups according to their scores on the

NDI[45]: 1) mild neck disability (NDI 5-14), and; 2) moderate neck disability (NDI 15-

24). The criteria for exclusion were: 1) a history of traumatic injuries (e.g., contusion,

fracture, or whiplash injury); 2) presence of fibromyalgia or other chronic pain disorder;

3) neuropathic pain (e.g., trigeminal neuralgia); 4) unilateral neck pain; 5) cervical spine

surgery, and; 6) clinical diagnosis of cervical radiculopathy or myelopathy.

Healthy controls were recruited from our academic university campus and the

local community through flyers, posters, and social media. Healthy participants were

examined and were included in the study only if they had no history of craniofacial

pain, headache or neck pain and had been free of any other painful disorders for the six

months prior to the experiment. All subjects had complete dentition, did not use any

medication, had no dental pathology and none were regular gum chewers. Subjects who

reported oral parafunctions (i.e., tooth grinding, tooth clenching) were excluded.

Experimental Protocol

After consenting for the study, recruited patients were given a battery of

questionnaires to complete on the first day of the experiment. These included various

self-reports for sociodemographic, psychological and pain-related variables, including

the visual analogue scale (VAS) for pain intensity and the validated Spanish versions of

the pain catastrophizing scale (PCS), the NDI and the impact associated with headache

was assessed using the Headache Impact Test-6 (HIT-6). The experimental protocol

consisted of baseline measurements, a provocation chewing test, and data collection

immediately after, and 24 hours after, the provocation chewing test. Participants

underwent standardized measurement of pressure pain thresholds (PPT) for mechanical

pain sensitivity at the trigeminal and cervical region and the pain-free maximum mouth

opening (MMO). The PPT and MMO measures have been employed in previous

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studies[46] and are further described below. During the performance of the provocation

chewing test, data were collected regarding the subjective feelings of fatigue and pain

intensity every minute, immediately and 24 hours after completion.

Provocation Chewing Test

The provocation chewing test consisted of 6 minutes of unilateral chewing of eight

grams of hard gum; this protocol was modified from Karibe et al.[47]. Chewing gum

was employed to elicit pain and muscle fatigue. The participants performed the test in

the sitting position, which was attained by instructing the patient to sit in a comfortable

upright position, with the thoracic spine in contact with the back of the chair, but

without contact of the craniocervical region with the seat. The feet were positioned flat

on the floor with knees and hips at 90 degrees and arms resting freely alongside.

Tests were carried out by exclusively using the right side for chewing; the

metronome was set at 80 beats per minute to indicate chewing rate, as documented in a

previous study[48]. The participants were instructed to chew gum initially for 60

seconds to soften its initial hardness, then after 70 seconds of rest, the signal was given

to start the test.

Questionnaires

The Spanish version of the PCS assesses the degree of pain catastrophizing[49, 50]. The

PCS has 13 items and a 3-factor structure: rumination, magnification and helplessness.

The theoretical range is between 0 and 52, with lower scores indicating less

catastrophizing. The PCS has demonstrated acceptable psychometric properties[50].

The Spanish version of the NDI measures perceived neck disability[45, 51]: This

questionnaire consists of 10 items, with 6 possible answers that represents 6 levels of

functional capacity, ranging from 0 (no disability) to 5 (complete disability) points. The

addition of all of the points obtained from each of the items gave the level of disability,

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with higher scores indicating greater perceived disability. The NDI has demonstrated

acceptable psychometric properties[51].

The Spanish version of the HIT-6[52, 53] consists of a six-item questionnaire measuring

the severity and impact of headache on the patient’s life. The results of HIT-6 are

stratified into four grade-based classes: little or no impact (HIT-6 score: 36-49),

moderate impact (HIT-6 score: 50-55), substantial impact (HIT-6 score: 56-59), and

severe impact (HIT-6 score: 60-78)[52]. The HIT-6 has demonstrated acceptable

psychometric properties[54].

Pain intensity

Pain intensity was measured with the VAS. The VAS consists of a 100 mm line, on

which the left side represents “no pain” and the right side “the worst pain imaginable”.

The patients placed a mark where they felt it represented their pain intensity[55].

The VAS scale was used to quantify two different situations:

a) Habitual and spontaneously perceived pain intensity.

b) Pain intensity perceived at different times during the course of the chewing

provocation test and at 24h after completion.

Subjective perception of fatigue.

The visual analogue fatigue scale (VAFS) was used to quantify fatigue at

different times during the course of the chewing provocation test and at 24h after

completion. The VAFS consists of a 100-mm vertical line on which the bottom

represents “no fatigue” (0 mm), and the top represents “maximum fatigue” (100

mm)[56]. The researcher registered the mark in mm.

Pressure pain thresholds

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A digital algometer (FDX 25, Wagner Instruments, Greenwich, CT, USA),

comprised of a rubber head (1 cm2) attached to a pressure gauge, was used to measure

PPTs. Force was measured in kilograms (kg); therefore, thresholds were expressed in

kg/cm2. The protocol used was a sequence of 3 measurements, with an interval of 30

seconds between each of the measurements. An average of the 3 measurements was

calculated to obtain a single value for each of the measured points in each of the

assessments. PPTs were assessed at one point in the masseter muscle (2.5 cm anterior to

the tragus and 1.5 cm inferior to the zygomatic arch), one point in the temporalis muscle

(anterior fibres of the muscle; 3 cm superior to the zygomatic arch in the middle point

between the end of the eye and the anterior part of the helix of the ear), in the

suboccipital muscles (2 cm inferior and lateral to the external occipital protuberance)

and in the upper trapezius muscle (2.5 cm above the superior medial angle of the

scapula). The device was applied perpendicular to the skin. The patients were asked to

raise their hands at the moment the pressure started to change to a pain sensation, at

which point the assessor stopped applying pressure. Compression pressure was

gradually increased at a rate of approximately 1 kg/s. This algometric method has high

intra-rater reliability (ICC=0.94-0.97) for measuring PPT[57].

Pain-free MMO

MMO was measured with the patients in a supine position. The patients were

asked to open their mouths as wide as they could without pain. The distance between

the superior incisor and the opposite inferior incisor was measured in mm with a

Craniomandibular scale (CMD scale. Pat. No. ES 1075174 U, INDCRAN: 2011.

INDCRAN, Madrid, Spain). The inter-rater reliability of this procedure has been found

to be high (ICC = 0.95 – 0.96)[58].

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Sample size

The sample size was estimated with the G*Power Program 3.1.7 for Windows

(G*Power© from University of Dusseldorf, Germany)[59]. The sample size calculation

was considered a power calculation to detect between-group differences in the primary

outcome measures (fatigue and pain intensity). To obtain 80% statistical power (1-β

error probability) with an α error level probability of 0.05, using analysis of variance

(ANOVA) of repeated measures, within-between interaction and an medium effect size

of 0.3, we considered 3 groups and 7 measurements for primary outcomes. This

generated a sample size of 31 participants per group. Allowing a dropout rate of 20%

and aiming to increase the statistical power of the results, we planned to recruit at least a

minimum of 112 participants to provide sufficient power to detect significant group

differences.

Statistical Analysis

The Statistical Package for Social Sciences (SPSS 21, SPSS Inc., Chicago, IL

USA) software was used for statistical analysis. The independent t-test and one-way

ANOVA was used for analysis of the self-report psychological and pain-related

variables (NDI, PCS and HIT-6), as well as pain duration and the subjects’

sociodemographic data (age, weight, height), comparing the baseline data for the three

groups. Results are presented as mean, standard deviation (±SD), range and 95%

confidence interval (CI).

For primary outcome variables (fatigue and pain intensity), we performed a 3-

way repeated-measures ANOVA, including within-between interaction factors. The

factors analysed were group (i.e., moderate neck disability group, mild neck disability

group and healthy group), sex (i.e., female and male) and time (measurement per minute

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during the test and after 24 hours). The hypothesis of interest was the group vs. time

interaction.

The 2-way repeated-measures models of ANOVA were used to test the effect of

the task on the outcome secondary variables (i.e., PPTs and pain-free MMO). The

factors analysed were group and time (baseline, immediately after and after 24 hours),

and also the interactions group vs. time interactions were analysed. In the analysis,

repeated-measures ANOVAs, when the assumption of sphericity was violated (as

assessed using the Mauchly sphericity test), the number of degrees of freedom against

which the F-ratio was tested was corrected by the value of the Greenhouse–Geisser

adjustment. Post hoc analysis with Bonferroni corrections was performed in the case of

significant ANOVA findings for multiple comparisons between variables. Effect-sizes

(Cohen’s d) were calculated for outcome secondary variables. According to Cohen’s

method, the magnitude of the effect was classified as small (0.20 to 0.49), medium (0.50

to 0.79), and large (≥0.8)[60].

The relationship between pain-related measures after completion of the chewing

provocation test and self-reports for pain-related and psychological measures were

examined using Pearson correlation coefficients. Multiple linear regression analysis was

performed to estimate the strength of the associations between the results of VAS

[model 1], VAFS [model 2] and pain-free MMO [model 3] (criterion variables) after 24

hours following completion of the provocation chewing test and NDI, PCS, HIT-6 and

VAS were used as predictor variables. Variance inflation factors (VIFs) were calculated

to determine whether there were any multi-collinearity issues in any of the three models.

The strength of association was examined using regression coefficients (β), P

values and adjusted R2. Standardized beta coefficients were reported for each predictor

14

variable included in the final reduced models to allow for direct comparison between

the predictor variables in the regression model and the criterion variable being studied.

For regression analysis, the 10 cases per variable rule was applied in order to obtain

reasonably stable estimates of the regression coefficients[61]. The significance level for

all tests was set to P < 0.05.

RESULTS

Baseline characteristics of sociodemographic, psychological and pain-related variables

of the sample are summarized in Table 1. Finally, the total study sample consisted of

122 participants (77 females and 45 males). Table 1 shows no statistically significant

differences among the three groups in relation to sociodemographic variables. There

were no differences in the duration of pain and perceived pain intensity on a regular or

spontaneous basis in specific groups of patients, but differences were observed in NDI,

PCS and Hit-6 (p<0.05). The different diagnosis for TMD of the included patients were

as follows: 28 patients (33.7%) were diagnosed with myofascial pain, 8 patients (9.6%)

with arthralgia, 13 patients (15.6%) with osteoarthritis and 34 patients (40.9%) with a

combined diagnosis (myofascial pain with arthralgia or osteoarthritis).

In the group of healthy participants, there were no withdrawals during the

provocation chewing test; in the group of patients with moderate neck disability, nine

participants (21.9%) withdrew between minutes 5 and 6 of the test as well as six

participants in the group of patients with mild neck disability (14.2%). All of the

participants were evaluated 24 hours after the test.

Gender Differences in Response to Provocation Chewing Test

The interaction of group vs. sex showed significant differences in VAS

(F=10.86; P<0.001), VAFS (F=4.06; P=0.02) and PPTs of the trapezius muscle

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(F=3.96; P=0.022). Post hoc analysis showed higher values of VAS and VAFS in

women compared to men for the three groups (P<0.05). PPTs in the trapezius muscle

values were lower in women than in men (P<0.05) for the two groups of patients; in the

control group there was no difference in this value. No differences (group vs. sex

interaction) were observed for the other variables.

Pain and Fatigue

The ANOVA revealed a significant group vs. time interaction (F=35.77;

P<0.001), and significant differences for the group factor (F=416.65; P<0.001)

regarding the VAS results during the provocation chewing test. VAS behaviour during

the tests can be seen in Figure 1-A. Post hoc analysis revealed that higher values on the

VAS during provocation chewing test for the moderate neck disability group compared

to the mild neck disability group and the control group. The results obtained 24 hours

after the test showed no differences between the groups of patients, but there were

differences with the control group (Figure 2-A).

For fatigue perceived during tests, the ANOVA showed a significant effect for

group vs. time interaction (F=13.05; P<0.001) and for the group factor (F=371.12;

P<0.001). VAFS behaviour during the tests can be seen in Figure 1-B. VAFS values

were higher at 6 minutes and 24 hours after the test in the group of moderate neck

disability compared with the other two groups. The post hoc analysis shows the

differences between the three groups (Figure 2-B).

Pain-free MMO

Regarding the pain-free MMO ANOVA revealed a significant effect for group

vs. time interaction (F=2.75; P=0.02) and for the group factor (F=65.74; P<0.001). The

post hoc analysis shows a decrease in the pain-free MMO immediately after the tests for

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the three groups, but this decrease was observed only in the group of moderate disability

at 24 hours after the test (Table 2).

Pressure pain thresholds

The PPTs for all points of the trigeminal and cervical region showed statistically

significant differences by ANOVA in the group vs. time interaction and group factor

(P<0.001). According to the post hoc analysis of the PPT masseter muscle, the results

showed a decrease in all groups for measurements both immediately and 24 hours after

the test (P<0.05); however, this decrease was greater in the group showing moderate

neck disability (d>0.8). Changes in temporalis muscle PPT’s were observed in both

measures for the group of moderate neck disability (P<0.001; d>0.8). In the group of

mild neck disability, changes were only observed immediately after the test (P=0.002;

d=0.19). No changes were observed in the group of healthy subjects (P>0.05).

For PPT in the cervical region (trapezius muscle and suboccipital muscles), the

post hoc analysis shows a decrease of values measures immediately and 24 hours after

the test (P<0.001) for group of moderate neck disability. This decrease in PPT can be

considered large for the suboccipital region (d>0.9) and small-medium for the trapezius

muscle (d=0.27 and 0.61). In the group with mild neck disability, changes were

observed only in the trapezius muscle PPT measurement immediately after the test

(P=0.028; d=0.09) and no statistically significant differences were observed in any of

the PPT measurements in the cervical region in the group of healthy subjects (P>0.05).

Correlations Analysis

Table 3 shows the results of correlation analysis examining the bivariate

relationships among self-reports for pain-related and psychological measures and

MMO, VAS and VAFS measured immediately and 24 hours after the tests for the

17

groups with moderate and mild neck disability. The strongest correlations were found in

the analysis for the group with moderate neck disability, where the pain-free MMO

immediately after the test was negatively associated with NDI (r=-0.54; P<0.001). For

the mild neck disability group, the greater correlation was between the MMO results

after 24 hours and NDI, which had a negative association (r=-0.49; P<0.001).

Multiple linear regression analysis

A linear regression analysis was performed to evaluate contributors to VAFS,

VAS and pain-free MMO after 24 hours regarding all of the self-report results for pain-

related and psychological measures in the patient groups with moderate and mild neck

disability; the results are presented in Table 4.

In the first model, the criterion variable VAFS was predicted by pain

catastrophizing (for both groups), explaining 17% and 12% of variance, respectively.

The following variables, VAS (moderate neck disability, β=-0.001; P=0.10, mild neck

disability, β=-0.053; P=0.72), HIT-6 (moderate neck disability, β=0.004; P=-0.97, mild

neck disability, β=-0.071; P=0.63), and NDI (moderate neck disability, β=-0.082;

P=0.59, mild neck disability, β=-0.070; P=0.67) were not significant predictors.

In the second model, the VAS after 24 hours was predicted by HIT-6 (moderate

neck disability group) and pain catastrophizing (mild neck disability group), explaining

22% and 14% of the variance, respectively. The VAS (moderate neck disability, β=-

0.27; P=0.06, mild neck disability, β=-0.13; P=0.41), NDI (moderate neck disability,

β=0.19; P=0.17, mild neck disability, β=0.24; P=0.13) and PCS (moderate neck

disability, β=0.16; P=0.25) and HIT-6 (mild neck disability, β=-0.054; P=0.71) were not

significant predictors.

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In a third model, the pain-free MMO was predicted by NDI for both groups;

these models accounted for between 14% and 21% of the variance. The PCS (moderate

neck disability, β=0.20; P=0.19, mild neck disability, β=0.13; P=0.39), the VAS

(moderate neck disability, β=-0.34; P=0.85, mild neck disability, β=-0.26; P=0.13) and

HIT6 (moderate neck disability, β=-0.24; P=-0.066, mild neck disability, β=0.20;

P=0.64) were not significant predictors.

DISCUSION

The results of this study demonstrate that a protocol of masticatory provocation

can induce pain, fatigue and other trigeminal sensory-motor changes in patients with

headache attributed to temporomandibular disorders. Our findings are consistent with

previous studies which have also observed sensory changes induced experimentally by

the masticatory provocation test[47, 62–64]. The duration of the masticatory

provocation test used in our study was similar to other investigations[47, 63, 65].

However, some studies have used longer and also shorter durations for the masticatory

test, reporting significant changes in both situations for both patients and healthy

subjects[48, 62, 64, 66–68]. It is important to mention that group changes were found in

the healthy subjects, but these were smaller than in the other groups, this could be

explained by the observation that exercise can induce pain and increased

hyperalgesia[69]. In addition, other authors have suggested that experimentally-induced

pain during the test may be due to masticatory muscle ischemia followed by the

accumulation of metabolic products in these muscles[70–72]. We also need to take into

account that there is sufficient evidence to suggest fatigue as a factor that increases the

pain perception[73].

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In this regard, our findings show strong positive correlations between fatigue

and perceived pain associated with the masticatory provocation test in the three assessed

groups. These results may explain in a general way the observed sensory-motor

changes, although they are not sufficient to justify neither the between-groups

differences nor the influence of cervical disability. Reflections and discussion of these

issues are presented in the following section in an effort to clarify and achieve a better

understanding of the matter.

One of the hypotheses proposed in this study is that cervical disability has an

influence over the trigeminal sensory-motor variables, modifying them. The results

obtained support this hypothesis because we observed greater changes in the moderate

cervical disability group immediately and 24 hours after the test. In addition, it was

hypothesized that the psychosocial factors would have a relationship with the results of

the masticatory provocation test and specifically with the pain and fatigue variables.

This relationship was proved after observing an association with pain catastrophizing.

Gender Differences

Regarding pain perception and fatigue during the test, our data show that gender

influences the results of the three groups: women presented with the greater perception

of pain intensity and masticatory fatigue. These results are consistent with previous

studies of experimentally-induced pain in patients[63] and healthy subjects[47, 68];

however, other investigations have not observed the interaction of gender factors with

experimentally-induced pain or masticatory fatigue [65, 74]. This research has not been

designed to identify the physiologic or psychological mechanisms which may explain

the differences in the results of men and women, although it is important to state that

there are many studies which present evidence-based results regarding the response that

20

women have to other painful clinical situations, adding the evidence of experimentally-

induced pain studies which indicate that women have a greater pain sensitivity than men

regarding several somatosensory tests[75].

Influence of the cervical disability over the trigeminal sensory-motor activity.

In this study, we have identified that patients with mild to moderate cervical

disability present a greater perception levels of pain and fatigue compared with healthy

subjects. It is important to mention that the group with moderate cervical disability

presented the greatest changes at the sensorial variables measured along the test,

immediately after and 24 hours after the test, with the exception of the pain intensity

perception after 24 hours, in which no statistically significant differences were found

between groups.

Although there are many studies that have used a provocative test to induce

masticatory pain and fatigue, we have only found one study similar to ours, in which

Haggman-Henrikson et al.[63] observed that patients with whiplash-associated

disorders presented greater masticatory pain and fatigue induced by the test compared to

TMD patients and healthy subjects.

We note recent scientific evidence that injuries to the cervical region may alter

the masticatory motor control and normal mandibular open-close function[76–78]. The

findings of this study may be related to this issue, because our results show that the

masticatory provocation test reduces the pain-free MMO at the end of the test, as seen in

the three groups assessed; these results are similar to previous studies[47, 72]. However,

we need to point out that the reduction was greater in both patient’s groups and it was

maintained at 24 hours only in the moderate cervical disability group. Also, it is

21

important to highlight that the regression analysis showed that cervical disability is a

predictor of the pain-free MMO (after 24 hours) in both groups of patients.

At present, the scientific evidence suggests the existence of cervical and

trigeminal motor patterns that act in a coordinated manner in the performance of

masticatory activities (chewing)[79–82], plus recent studies also support that the neck

muscles are activated during jaw-clenching tasks tasks assessed electromyographically

[83–85] and it seems that the activity of the neck muscles is increased as the demand for

masticatory work is greater[86]. Although most of these studies have been performed in

healthy subjects, we believe that these data are useful to try to explain some of the

results of this research. In this sense, we propose the theory that the masticatory motor

patterns are more altered with the presence of greater cervical pain or disability. This

situation would generate the activation of maladaptive compensatory mechanisms that

might alter the behaviour, recruitment and coordination of the neck and mandibular

motor systems, thus generating higher levels of fatigue and pain during the provocation

test and retaining these feelings 24 hours later.

This same theory could explain the results of decreased PPTs at the trigeminal and

cervical regions, noting that the PPTs changes were higher in the patient groups and that

most changes in the cervical PPTs at 24 hours occurred in the group of moderate

cervical disability. As a contributing factor to this situation, the presence of neck pain

must be considered, as this can lead to lower values of trigeminal PPTs compared to

healthy subjects [87]. Although we believe that there may be a direct relationship

between the trigeminal sensory-motor changes with cervical pain and disability, we

must also consider the possibility that the changes seen in patients would have been

mainly influenced by pre-established neuroplastic changes in the central nervous

system. Patients with chronic pain may be more susceptible to develop a central

22

sensitization process[88]. Wolf et al. suggest that in painful conditions where there is a

comorbidity, such as in the sample of patients in this study, it can be a determining

factor in the pathophysiology of central sensitization[89]. In relation to this, Gaff-

Radford proposed that in central sensitization, changes appear in afferent pathways that

enable the communication of cervical and orofacial nociceptive neurons in the

trigeminal nucleus[90]. In addition, there are many studies in TMD patients that have

found peripheral and central mechanisms compatible with a process of central

sensitization[91–97].

Influence of pain catastrophizing over trigeminal sensory-motor activity.

In this research, we have used self-reports of psychological and pain-related

variables to identify possible associations with sensory-motor variables. Through linear

regression analysis, we have observed that pain catastrophizing and the impact of

headache on the quality of life (HIT-6) were associated with the pain perception and

fatigue variables 24 hours after performing the masticatory provocation test.

Specifically, analysing the pain catastrophizing as a psychological factor resulted in a

predictor for fatigue at 24 hours after the test in the moderate cervical disability group,

and in the mild cervical disability group it was a predictor for perceived cervical

disability and fatigue after 24 hours. Pain catastrophizing is defined as a cognitive factor

that implies a mental negative perception or exaggeration of the perceived threat of

either a real or anticipated pain experience[98, 99]. It has been described that in patients

with TMD, catastrophizing contributes to the chronification of pain and disability [100].

It has also been associated with a greater use of health system services, with greater

clinical findings at assessment associated with a negative mood[40, 41] and with

alterations of the functional mandibular status[10]. Regarding the perceived fatigue and

pain catastrophizing, we did not find any clinical or experimental trials that have

23

examined their association in patients with craniofacial pain and TMD; but we found

one study researching the relationship of pain catastrophizing with masticatory

kinematic variables (i.e., amplitude, velocity, frequency cycle) which were measured

with a procedure using very short exposure times (15 seconds of chewing)[32]. In this

study, no associations of the kinematic variables measured with respect to catastrophism

were observed; however, we must take into account that the purpose of that study was

not to induce pain or fatigue to observe the response, as we did in this research. It is

important to note that a recent systematic review concluded that there is an association

between catastrophizing and fatigue and that the former influences the latter

proportionately; these results were observed in various clinical populations[101]. This

has also been demonstrated in other musculoskeletal disorders where pain

catastrophizing is associated with motor disturbances, such as decreased function,

performance of activities of daily living and limitation of exercise capacity[102–104].

The relationship between psychological factors, motor activity and pain seems to

be present in various cases of musculoskeletal pain, but the explanation for this is

complex and limited so far. Peck et al.[105] and Murray and Peck[106] have proposed a

possible explanation for this and have created a new Integrated Pain Adaptation Model

(IPAM). This model basically explains that the influence of pain on motor activity

depends on the interaction of multidimensional characteristics (biological and

psychosocial) of pain with the sensory-motor system of an individual, which results in a

new motor recruitment strategy in order to minimize pain. However, this motor

response may be associated with the appearance of another pain or worsening of the

existing pain[105, 106]. This model is based on the multidimensional features (sensory

discriminative, affective-emotional, cognitive) of the pain experience and how it affects

the sensory-motor system through the peripheral and central connections that this

24

system has with the autonomous nervous system, the limbic system and other higher

centres[105, 107].

Clinical and scientific implications

According to the results of this research, we found that neck pain and disability

can influence sensory and motor variables of the masticatory system. These findings

lead us to reflect on the importance of including a clinically specific assessment of the

cervical region in the diagnostic protocols for TMD and headache attributed to TMD. It

is noteworthy that the most commonly used diagnostic and classification methods for

patients with TMD do not include a specific assessment of neck pain and disability[20,

44, 108]. A diagnostic criterion observed recently in patients with headache attributed to

TMD is that mandibular movement, function or parafunction modify headache in the

temporal region[21]. We have observed an association between cervical disability with

pain-free MMO and have also found that patients with greater neck disability have

increased fatigue and pain induced by the masticatory test. These findings lead us to

assume that the cervical region may have an important role for this type of headache,

but this has to be confirmed in future research, as these data can be extrapolated only to

patients with this type of headache who also associate neck disability.

From the point of view of treatment, we propose an approach to reduce cervical

pain and disability as part of the overall therapeutic strategy, as this could be beneficial

to reduce the negative sensory symptoms and improve masticatory motor control. We

believe that this approach should be investigated in future studies, but it must be taken

into account that we have recent evidence that therapeutic exercise and manual therapy

to the cervical region produce positive effects on pain modulation in trigeminal areas

and improving pain-free MMO[46, 109].

25

In this study and other longitudinal or transversal studies, we have shown the

influence of psychosocial factors on patients with TMD[36, 110, 111]; specifically, our

results show an association between catastrophizing and perceived fatigue induced by

the masticatory activity. This finding shows the interaction between sensory-type

variables with psychological variables, which should be considered a crucial issue when

performing the assessment or designing of therapeutic interventions. In patients with

chronic pain, it is essential to recognize psychosocial factors that may be perceived as

obstacles to recovery[112]; achieving a reduction of pain catastrophizing is the best

predictor of successful rehabilitation in pain conditions[113].

The integration of a biopsychosocial perspective in clinical reasoning and

decision-making could be a key point in the management of pain and motor

rehabilitation of patients with headache attributed to TMD. It has been shown that

cognitive-behavioural therapy reduces pain intensity, depressive symptoms, improves

chewing function[114], reduces pain catastrophizing in patients with chronic TMD[115]

and, furthermore, it has been found that it causes neuroplastic adaptive changes

associated with decreased pain catastrophism in cases of chronic pain[116]. Prescribing

therapeutic exercise may be a good alternative to take into consideration; it has been

observed that exercise causes a reduction of catastrophizing and depressive symptoms;

these results were similar to cognitive behavioural therapy in patients with chronic

lower back pain[117].

Limitations

The results of this study should be discussed with the consideration that there are

several limitations. Although the sample size was calculated to have adequate power

and further losses were less than 20%, the results were not compared with a group with

26

headache attributed to TMD but without the presence of neck pain and disability. To

extrapolate the results to a clinical population would require similar but future studies to

be implemented using patient sample protocols with and without neck pain and

disability. Another limitation to consider is that pain catastrophizing was assessed as the

only psychological variable. It would be interesting to investigate the association of

other variables such as anxiety, depression, kinesiophobia and self-efficacy with

trigeminal sensory-motor variables.

As the only motor variable measured in this research was pain-free MMO, other

kinematic variables should be taken into consideration in future research as they may

provide more information. Moreover, we believe that measuring motor variables of the

cervical region could also be useful to analyse possible correlations with masticatory

variables.

CONCLUSION

The results of this study suggest that neck pain and disability have an influence

on the sensory-motor variables evaluated in patients with headache attributed to TMD.

In particular, it was observed that patients with moderate neck disability showed greater

changes immediately and 24 hours after the masticatory provocation test. Our data

provide new evidence about the possible neurophysiologic mechanisms of interaction

between the craniocervical region and the craniomandibular region. Regarding pain

catastrophizing, an association with perceived masticatory fatigue in both patient groups

was observed. These findings support the need to recognize the interaction between

sensory-motor and psychological aspects of headache attributed to TMD rather than

being assessed in isolation.

27

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

RL, AP, AG, JF participated in the study design, manuscript preparation and editing and

data acquisition. JP, SA, RL participated in the performed the statistical analysis,

database management and manuscript preparation. All authors read and approved the

final manuscript.

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37

Figure 1. Data represent mean value and error bars with 95% confidence intervals of

the mean of the pain intensity score (A), and the visual analogue fatigue scale scores

(B). Recorded during the 6 min and 24 hours after provocation chewing test. Level of

significance (multiple comparisons for each group): Moderate disability, *P<0.05;

**P<0.01; Mild disability, °P<0.05; °°P<0.01; and Healthy, ^P<0.05; ^^P<0.01.

Figure 2. Comparison between groups of the pain intensity (A) and perceived fatigue

(B) immediately (6 min) and 24 hours after the provocation chewing test. Data represent

mean value, error bars with 95% confidence intervals of the mean and effect size (d).

Level of significance: *P<0.05; **P<0.01.

38

Table 1. Summary of Demographic, Pain and Psychological Variables

Moderate Neck Disability (N=41)

Mild Neck Disability (N=42)

Healthy (N=39)

t / F P Value

Variables Mean±SD Range Mean±SD Range Mean±SD Range Sex (female/male) 26/15 - 25/17 - 26/13 - - -

Weight (kg)

69.56±12.47 51-103 67.76±14.03 50-97 64.84±10.2 48-90 1.4 0.23

Heigth (cm)

167.56±12.4

7

152-183 165.54±12.09 150-185 169.97±8.51 156-189 1.98 0.14

Age (years)

44.31±10.9 22-59 40.95±12.89 19-60 40.61±10.01 30-65 1.3 0.27

Pain duration

(months)

19.73±12.66 6-60 22.19±13.36 6-48 - - -0.8 0.39

NDI (points) 17.58±2.69 15-24 11.42±2.48 7-14 - - 10.8 0.01

PCS (points) 17.09±3.75 7-23 15.8±4.02 7-22 5.46±1.75 2-9 143 0.01

HIT-6 (points) 55.31±4.9 49-65 53.16±4.74 43-59 - - 2 0.04

VAS (mm) 40.75±9.17 21-58 37.04±9.16 19-54 - - 1.8 0.06

Abbreviations: NDI, Neck Disability Index; PCS, Pain Catastrophizing Scale; HIT-6, headache impact test-6; Visual Analog Scale, VAS; SD, standard deviation

39

Table 2. Descriptive data and multiple comparisons of the assessed variables

** p < 0.01; *p < 0.05 Abbreviations: MMO, maximal mouth opening; PPT, pressure pain threshold; SD, standard deviation

Mean±SD Mean difference (95% CI) Effect size (d)

Group Baseline Immediately after

After 24 hours a) Base vs. Immediately b) Base vs. 24 h.

MMO (mm)

Moderate Neck Disability

42.43±2.75 40.65±2.01 41.85±2.19 a) 1.89 (1.39 to 2.39)**;d=0.74 b) 0.6 (0.02 to 1.17)*;d=0.26

Mild Neck Disability

43.61±2.87 42±2.18 43.26±2.68 a) 1.56 (1.09 to 2.07)**; d=0.63 b) 0.36 (-0.01 to 0.75); d=0.12

Healthy 50±4.46 49.05±3.95 49.87±4.57

a) 0.76 (0.24 to 1.29)*; d=0.22 b) 0.09 (-0.32 to 0.51); d=0.02

PPT. Masseter Moderate Neck Disability

1.9±0.21 1.02±0.17 0.88±0.2 a) 0.89 (0.79 to 0.99)** d=4.66 b) 1.03 (0.94 to 1.13)** d=5.03

Mild Neck Disability

2.01±0.34 1.44±0.28 1.57±0.34 a) 0.57 (0.48 to 0.67)** d=1.82 b) 0.44 (0.35 to 0.53)** d=1.29

Healthy 2.85±0.58 2.39±0.52 2.7±0.51

a) 0.45 (0.35 to 0.56)** d=0.84 b) 0.13 (0.03 to 0.23)* d=0.27

PPT. Temporalis Moderate Neck Disability

1.99±0.19 1.55±0.25 1.62±0.23 a) 0.44 (0.39 to 0.49)** d=2.06 b) 0.37 (0.25 to 0.49)** d=1.77

Mild Neck Disability

2.12±0.35 2.05±0.37 2.04±0.45 a) 0.07 (0.02 to 0.12)** d=0.19 b) 0.09 (-0.02 to 0.2) d=0.20

Healthy 3.31±0.83 3.26±0.82 3.27±0.84

a) 0.04 (-0.001to 0.1) d=0.06 b) 0.06 (-0.05 to 0.19) d=0.04

PPT. Suboccipital

Moderate Neck Disability

2.39±0.44 1.65±0.36 1.47±0.32 a) 0.78 (0.7 to 0.85)** d=1.86 b) 0.95 (0.83 to 1.07)** d=2.42

Mild Neck Disability

2.14±0.57 2.06±0.55 2.22±0.57 a) 0.07 (-0.00 to 0.15) d=0.14 b) -0.11 (-0.23 to 0.00)* d=0.14

Healthy 3.15±0.56

3.09±0.55 3.18 ±0.59

a) 0.06 (-0.01 to 0.14) d=0.1 b) -0.01 (-0.13 to 0.11) d=0.05

PPT. Trapezius Moderate Neck Disability

2.62±0.49 2.33±0.47 2.49±0.45 a) 0.28 (0.24 to 0.33)** d=0.61 b) 0.14 (0.08 to 0.2)** d=0.27

Mild Neck Disability

2.68±0.62 2.62±0.63 2.63±0.58 a) 0.04 (0.00 to 0.09)* d=0.09 b) 0.04 (-0.01 to 0.1) d=0.08

Healthy 3.54±1 3.51±0.97 3.53±0.94 a)0.01 (-0.03 to 0.06) d=0.03 b) -0.01 (-0.05 to 0.07) d=0.01

40

Table 3. Pearson's correlation coefficient between the different variables analyzed in the study

Groups VAS 6min. VAS 24h. VAFS 6min.

VAFS 24h. MMO Immediately After

MMO 24h

Moderate Neck Disability

NDI 0.49** 0.28 0.40** 0.07 -0.54** -0.40**

Mild Neck Disability

0.02 0.37* 0.02 0.21 -0.48** -0.49**

Moderate Neck Disability

PCS 0.10 0.24 0.17 0.44** 0.03 0.04

Mild Neck Disability

0.08 0.40** 0.01 0.38* -0.17 -0.09

Moderate Neck Disability

HIT-6 0.41** 0.48** 0.27 0.07 -0.12 -0.31*

Mild Neck Disability

-0.11 -0.03 0.30 -0.04 -0.13 -0.12

Moderate Neck Disability

VAS -0.08 0.39* 0.49** 0.16 -0.23 -0.25

Mild Neck Disability

-0.08 0.17 -0.17 0.11 -0.39* -0.47**

** p < 0.01; *p < 0.05 Abbreviations: NDI, Neck Disability Index; PCS, pain catastrophizing scale; HIT-6, headache impact test-6; VAS, visual analog scale; VAFS, visual analog fatigue scale; MMO, maximal mouth opening

41

Table 4. Multiple linear regression analysis

Moderate Neck Disability

criterion variable

predictor variables

Regression coefficient (B)

Standardized coefficient (β)

Significance (p)

VIF Adjusted R2

VAFS24 PCS 0.84 0.44 0.004 1.00 0.17

VAS24 HIT-6 0.93 0.48 0.001 1.00 0.22

MMO24 NDI -0.35 -0.40 0.01 1.12 0.14

Mild Neck Disability

VAFS24 PCS 0.98 0.38 0.013 1.00 0.12

VAS24 PCS 0.67 0.40 0.009 1.00 0.14

MMO24 NDI -0.53 -0.49 0.001 1.00 0.21

Abbreviations: NDI, Neck Disability Index; PCS, pain catastrophizing scale; HIT-6, headache impact test-6; VAS, visual analog scale; VAFS, visual analog fatigue scale; MMO, maximal mouth opening; 24, 24 hours after of tests

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182

5.6 Estudio VI

La Touche R, Fernández-de-las-Peñas C, Fernández-Carnero J, Escalante K, Angulo-Díaz-

Parreño S, Paris-Alemany A, Cleland JA. The effects of manual therapy and exercise directed at

the cervical spine on pain and pressure pain sensitivity in patients with myofascial

temporomandibular disorders. J Oral Rehabil. 2009 Sep;36(9):644-52.

Objetivos del estudio

Nuestro objetivo fue investigar los efectos de la terapia manual y el ejercicio dirigido a la

columna cervical en la intensidad del dolor, la MAI y los UDPs de músculos masticatorios en

pacientes con TCM.

Resultados

El modelo mixto de ANOVA 2X3 reveló un efecto significativo en el factor tiempo (F = 77,8; P

<0,001), pero no para el factor lado (F = 0,2; P = 0,7) para los cambios en los UDPs sobre el

músculo masetero y más músculo temporal (tiempo: F = 66,8; P <0,001; lado: F = 0,07; P =

0,8). Las pruebas post hoc revelaron diferencias significativas entre pre-intervención y la post-

intervención y período de seguimiento (P <0,001), pero no entre la post-intervención y el

periodo seguimiento (P = 0,9) para ambos músculos. Los tamaños del efecto eran grandes (d>

1,0) para ambos períodos de seguimiento en los UDPS musculares. El ANOVA encontró un

efecto significativo de tiempo (F = 78,6; P <0,001) los cambios en la intensidad del dolor y la

MAI sin dolor (F = 17,1; P <0,001). Se encontraron diferencias significativas entre la pre-

intervención y dos periodos post-intervención (P <0.001), pero no entre la medida post-

intervención y el periodo de seguimiento (P> 0.7). Dentro del grupo tamaños del efecto eran

grandes (d> 0,8) para los resultados post-intervención y los períodos de seguimiento.

Conclusión

La aplicación de tratamiento dirigido a la columna vertebral cervical puede ser beneficioso en la

disminución de la intensidad del dolor, el aumento de los UDPS en los músculos de la

masticación y en la MAI libre de dolor en pacientes con TCM.

The effects of manual therapy and exercise directed at the

cervical spine on pain and pressure pain sensitivity in

patients with myofascial temporomandibular disorders

R. LA TOUCHE*, †, C. FERNANDEZ-DE-LAS-PENAS‡, §, J . FERNANDEZ-CARNERO‡, §,

K. ESCALANTE¶, S. ANGULO-DIAZ-PARRENO†, A. PARIS-ALEMANY† &

J. A. CLELAND** , ††, ‡‡*Faculty of Medicine, Department of Physical Therapy, Universidad San Pablo CEU, Madrid, †University

Center for Clinical Research of the Craneal-Cervical-Mandibular System of Universidad San Pablo CEU, Madrid, ‡Department of Physical

Therapy, Occupational Therapy, Rehabilitation and Physical Medicine, Universidad Rey Juan Carlos, Alcorcon, Madrid, §Esthesiology

Laboratory of Universidad Rey Juan Carlos, Alcorcon, Madrid, ¶Faculty of Psychology, Department of Personality Assessment and Psychology

Treatment, Universidad Complutense, Madrid, Spain, **Department of Physical Therapy, Franklin Pierce University, Concord, ††Physical

Therapist, Rehabilitation Services, Concord Hospital, Concord, NH and ‡‡Faculty, Manual Therapy Fellowship Program, Regis University,

Denver, CO, USA

SUMMARY No studies have investigated the effects of

the treatments directed at the cervical spine in

patients with temporomandibular disorders (TMD).

Our aim was to investigate the effects of joint

mobilization and exercise directed at the cervical

spine on pain intensity and pressure pain sensitivity

in the muscles of mastication in patients with TMD.

Nineteen patients (14 females), aged 19–57 years,

with myofascial TMD were included. All patients

received a total of 10 treatment session over a 5-

week period (twice per week). Treatment included

manual therapy techniques and exercise directed at

the cervical spine. Outcome measures included

bilateral pressure pain threshold (PPT) levels over

the masseter and temporalis muscles, active pain-

free mouth opening (mm) and pain (Visual Ana-

logue Scale) and were all assessed pre-intervention,

48 h after the last treatment (post-intervention) and

at 12-week follow-up period. Mixed-model ANOVAS

were used to examine the effects of the intervention

on each outcome measure. Within-group effect sizes

were calculated in order to assess clinical effect. The

2 · 3 mixed model ANOVA revealed significant effect

for time (F = 77Æ8; P < 0Æ001) but not for side (F = 0Æ2;

P = 0Æ7) for changes in PPT over the masseter muscle

and over the temporalis muscle (time: F = 66Æ8;

P < 0Æ001; side: F = 0Æ07; P = 0Æ8). Post hoc revealed

significant differences between pre-intervention

and both post-intervention and follow-up periods

(P < 0Æ001) but not between post-intervention and

follow-up period (P = 0Æ9) for both muscles. Within-

group effect sizes were large (d > 1Æ0) for both

follow-up periods in both muscles. The ANOVA

found a significant effect for time (F = 78Æ6;

P < 0Æ001) for changes in pain intensity and active

pain-free mouth opening (F = 17Æ1; P < 0Æ001). Sig-

nificant differences were found between pre-inter-

vention and both post-intervention and follow-up

periods (P < 0Æ001) but not between the post-

intervention and follow-up period (P > 0Æ7).

Within-group effect sizes were large (d > 0Æ8) for

both post-intervention and follow-up periods. The

application of treatment directed at the cervical

spine may be beneficial in decreasing pain intensity,

increasing PPTs over the masticatory muscles and an

increasing pain-free mouth opening in patients with

myofascial TMD.

KEYWORDS: cervical spine, temporomandibular dis-

order, pressure pain sensitivity

Accepted for publication 25 June 2009

ª 2009 Blackwell Publishing Ltd doi: 10.1111/j.1365-2842.2009.01980.x

Journal of Oral Rehabilitation 2009 36; 644–652

Introduction

Temporomandibular disorder (TMD) is a term which

includes several conditions involving the temporoman-

dibular joint and the muscles of mastication. The most

common symptoms of TMD include pain located over

the facial region and tenderness to palpation of the

masticatory structures. Some studies have shown

prevalence rate of TMD to be between 3% and 15%

in the Western population (1), with an incidence

between 2% and 4% (2). A recent survey determined

that the overall prevalence of TMD was 6Æ3% for

women and 2Æ8% for men (3).

It appears that an intimate functional relationship

exists between the mandibular and the head-neck

systems, as suggested by their anatomical and bio-

mechanical inter-relationships, although current

evidence is conflicting (4). Several epidemiological

studies have reported that patients with TMD often

experience symptoms of neck pain and that patients

with neck pain also suffered from symptoms in the

orofacial region (5–8). In addition, Eriksson et al. (9)

reported that mouth opening was accompanied by

head-neck extension and mouth closing by head-neck

flexion, with a precise temporal coordination between

jaw-neck movements dependent on the speed of the

movement (10).

The neuro-anatomical basis for the relationship

between the head and neck may be related to the

trigemino-cervical nucleus caudalis in the spinal grey

matter of the spinal cord at the C1–C3 level, where

there is a convergence on the nociceptive second order

neurons receiving trigeminal and cervical inputs (11).

The topographic arrangement of the trigeminal nucleus

caudalis allows the interchange of nociceptive infor-

mation between the cervical spine and the trigeminal

nerve (12). Studies have demonstrated that stimulation

of trigeminal-innervated structures evoked painful

sensations in the neck and vice versa (13, 14). In

addition, it has been reported that injection of an

inflammatory irritant into deep paraspinal tissues

results in a sustained activation of both jaw and neck

muscles (15, 16).

Several localized therapeutic modalities are often

used in the management of TMD, including mobiliza-

tion (17–19) or exercises (20, 21) of the temporoman-

dibular joint. As there is a connection between the neck

and the temporomandibular region, it can be hypo-

thesized that interventions targeted to the cervical spine

may also have an effect on patients with TMD.

Catanzariti et al. (22) suggested that neck pain patients

may respond to intervention applied to the temporo-

mandibular joint and that techniques applied to the

cervical spine may also have effect on the temporo-

mandibular system. To the best of our knowledge no

previous studies have investigated the effects of treat-

ment directed solely at the cervical spine in patients

with TMD. The purpose of this study was to investigate

the effects of joint mobilization directed at the cervical

spine plus an exercise protocol targeting the deep

cervical flexor muscles on intensity of pain and pressure

pain sensitivity in the muscles of mastication in patients

with myofascial TMD.

Materials and methods

Patients

Consecutive patients referred from four private dental

clinics between October 2007 and June 2008 partici-

pated in this study. Participants were eligible to partic-

ipate if they met the following criteria: (i) a primary

diagnosis of myofascial pain according to Axis I,

category Ia and Ib (i.e. myofascial pain with or without

limited opening) of the Research Diagnostic Criteria for

TMD (RDC ⁄ TMD) (23); (ii) bilateral pain involving the

masseter and temporal regions; (iii) presence of at least

one trigger point (TrP) in the masseter or temporalis

muscles; (iv) pain symptoms history of at least the

3 months previous to the study; and (v) intensity of the

pain of at least 30 mm on a 100 mm Visual Analogue

Scale (VAS). Trigger points were diagnosed following

the criteria described by Simons et al. (24): (i) presence

of a palpable taut band in a skeletal muscle; (ii)

presence of a hypersensitive tender spot within the

taut band; (iii) local twitch response elicited by the

snapping palpation of the taut band; and (iv) repro-

duction of the referred pain pattern of the TrP in

response to palpation. These criteria have demonstrated

good inter-examiner reliability (j) ranging from 0Æ84 to

0Æ88 (25).

Participants were excluded if they presented with any

of the following: (i) sign or symptoms of disc displace-

ment, arthrosis, or arthritis of the temporomandibular

joint, according to categories II and III of the

RDC ⁄ TMD; (ii) history of traumatic injuries (e.g.

fracture, whiplash); (iii) fibromyalgia syndrome (26);

(iv) diagnosis of systemic disease (rheumatoid arthritis,

C E R V I C A L S P I N E I N M Y O F A S C I A L T E M P O R O M A N D I B U L A R D I S O R D E R 645

ª 2009 Blackwell Publishing Ltd

systemic lupus erythematosus, or psoriatic arthritis); (v)

presence of neurological disorders (e.g. trigeminal

neuralgia); (vi) concomitant diagnosis of any primary

headache (tension-type headache or migraine); (vii)

subjects who had received any form of treatment

(physiotherapy, splint therapy and acupuncture) with-

in 3 months of the study. The study was conducted in

accordance with the Helsinki Declaration, and all

participants provided informed consent which was

approved by the local ethics committee.

Pain intensity

The VAS was used to record the patient’s level of pain at

baseline, 48 h after the last treatment (post-interven-

tion) and at 12-week follow-up period. The VAS is a

10 cm line anchored with a ‘0’ at one end representing

‘no pain’ and ‘10’ at the other end representing ‘the

worst pain imaginable’. Patients placed a mark along

the line corresponding to the intensity of their symp-

toms, which was scored to the nearest millimetre. The

VAS has been shown to be a reliable and valid

instrument for measuring pain intensity (27). It exhib-

its a minimal clinically important difference (MCID)

between 9 and 11 mm (28, 29).

Pressure pain threshold assessment

Pressure pain threshold (PPT) is defined as the amount

of pressure where the sense of pressure first changes to

pain (30). A mechanical pressure algometer (Pain

Diagnosis and Treatment Inc, Great Neck, NY, USA)

was used. This device consisted of a round rubber disc

(1 cm2) attached to a pressure (force) gauge. The gauge

displayed values in kilograms. As the surface of the

rubber tip was 1 cm2, the readings were expressed in

kg cm)2. The mean of three trials (intra-examiner

reliability) was calculated and used for the main

analysis. A 30-second resting period was allowed

between trials. The reliability of pressure algometry

was found to be high (ICC = 0Æ91 [95% confidence

intervals (CI): 0Æ82–0Æ97] (31). Pressure pain threshold

was assessed over bilateral masseter and the temporalis

muscles. The masseter point was located 1 cm superior

and 2 cm anterior from the mandibular angle, and the

temporal point was located on the anterior fibres of

temporal muscle, 2 cm above the zygomatic arch in the

middle part between lateral edge of the eye and the

anterior part of the helix. Pressure pain threshold levels

were assessed at pre-intervention, 48 h after the last

treatment (post-intervention) and at 12-week follow-

up period.

Active pain-free mouth opening

In a supine position, participants were asked to ‘open

the mouth as wide as possible without causing pain’. At

the end position of pain-free mouth opening, the

distance between upper-lower central incisors was

measured in millimetres. The intra-tester reliability of

this procedure was found to be high (ICC = 0Æ9–0Æ98)

(32). The mean of three trials was calculated and used

for the main analysis. Active pain-free mouth opening

was assessed pre-intervention, 48 h after the last

treatment (post-intervention) and at 12-week follow-

up period.

Treatment protocol

The treatment protocol included only interventions

directed at the cervical spine. The treatment techniques

were applied by the same physical therapist with

6 years of experience specializing in manipulative

therapy. All patients received a total of 10 sessions

over a 5-week period (twice a week). During the 10

treatment sessions all patients were treated with the

following techniques:

1 Upper cervical flexion mobilization: The patient was

supine with the cervical spine in a neutral position. The

therapist brought about a contact of the occipital bone

with the first finger and medial aspect of the hand, and

other hand over the frontal region of the patient’s head.

The mobilizing force was delivered by flexing the upper

cervical region using a combination of cephalic traction

with the occipital hand and caudal pressure with the

frontal hand (Fig. 1). The mobilization was applied at a

slow rate of one oscillation per 2 s (0Æ5 Hz) for a total

time of 10 min. This rate of mobilization was previously

used in another study (33).

2 C5 central posterior-anterior mobilization (34): The

patient was prone with the cervical spine in a neutral

position. The therapist placed the tips of his thumbs on

the posterior surface of the C5 spinous process, while the

other fingers rested gently around the patients’ neck

(Fig. 2). A grade III (large amplitude movement that

moved into the resistance limiting the range of move-

ment) posterior-anterior technique was applied centrally

to the C5 spinous process. The mobilization was applied

R . L A T O U C H E et al.646

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at a rate of two oscillations per second (2 Hz). The

mobilizations were performed for a total of 9 min,

divided into 3-min intervalswith a 1 min rest in between.

3 Cranio-cervical flexor stabilization exercise: With the

aim to focus on the deep flexor muscles of the cervical

region, we followed the protocol described by Jull et al.

(35). Patients performed a cranio-cervical flexion exer-

cise in the supine position, which involved flexion of

the cranium (head) on the cervical spine (neck) while

ensuring that the back of the head remained in contact

with the supporting surface, in an effort to facilitate

activation of the deep cranio-cervical flexor muscula-

ture (particularly the longus capitis muscle) with

minimal activity of the superficial cervical flexors

(sternocleidomastoid and scalene muscles) (Fig. 3).

The contraction was graded through feedback from a

pressure biofeedback device (Stabilizer; Chattanooga

Group Inc., Chattanooga, TN, USA) that monitored the

flattening of the cervical lordosis due to the cranio-

cervical flexion movement from contraction of the deep

cervical flexor muscles (36). Falla et al. (37) demon-

strated that the cranio-cervical flexion test was accom-

panied by increased electromyographic activity in the

deep cervical flexor muscles. Additionally, increases in

the electromyographic activity of the deep cervical

flexors did not occur during other neck or jaw move-

ments, supporting the specificity of this test (38).

Patients first performed the correct cranio-cervical

flexion action with the following instructions: gently

nod your head as though you were saying ‘yes’ (Fig. 3).

The therapist monitored the superficial muscles by

palpation and identified the target level of the biofeed-

back where the patient could hold 10 s without use of

superficial neck flexor muscles, and without a quick or

jerky movement. Once the subject could perform the

movement correctly, the target level was established

and training began at this point. The baseline pressure

in the biofeedback device was 20 mmHg and the

patient was instructed to contract the deep neck flexors

to reach five pressure targets in increments of 2 mmHg

(35). The pressure increments were determined by

the level the patient could hold comfortably while

Fig. 1. Upper cervical flexion mobilization. Within one hand over

the occipital bone and the other hand over the frontal region of

the patient’s head, the therapist applies a mobilization force

inducing an upper cervical flexion using a combination of cephalic

traction with the occipital hand and caudal pressure with the

frontal hand.

Fig. 2. C5 central posterior-anterior mobilization. The therapist

placed the thumbs over the posterior surface of the C5 spinous

process and a posterior-anterior mobilization force is applied.

Fig. 3. Cranio-cervical flexor stabilization exercise.

C E R V I C A L S P I N E I N M Y O F A S C I A L T E M P O R O M A N D I B U L A R D I S O R D E R 647

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maintaining a 10-second contraction with no pain.

Participants sustained the contraction for 10 repetitions

of 10-second duration, with a 10-second rest interval

between each contraction. Once this target was

achieved, the exercise progressed to the next pressure

target, repeating the process at the new pressure target,

first increasing the holding time and then the repeti-

tions. This exercise protocol has been used in previous

studies in patients with neck pain (39–41).

Statistical analysis

Statistical analysis was conducted with the SPSS 14.5

package.* Mean, s.d., or 95% CI of the values were

presented. The Kolmogorov–Smirnov test showed a

normal distribution of the data (P > 0Æ05). A 2 · 3

mixed model analysis of variance (ANOVA) with time

(pre-intervention, post-intervention and follow-up)

and side (right or left) as the within-subjects variables

was used to examine the effects of the treatment on PPT

over the masseter or the temporalis muscles. A one-way

repeated measure ANOVA with time (pre-intervention,

post-intervention and follow-up) as within-subject

variable was used to investigate the effects of the

treatment on spontaneous pain and active mouth

opening. The Bonferroni test was used for post hoc

analysis. Within-group effect size was calculated using

Cohen’s coefficient (d) (42). An effect size greater than

0Æ8 was considered large; around 0Æ5, moderate; and less

than 0Æ2, small. A P-value less than 0Æ05 was considered

as statistically significant for all analyses.

Results

A total of 19 patients, 14 females and 5 males, aged 19–

57 years old (mean age � s.d.: 37 � 10 years) partici-

pated. All subjects were right hand dominant. None of

the patients started drug therapy during the time of the

study. In this sample of patients with TMD the average

duration of symptoms was 9Æ2 months (95% CI: 7Æ7–

10Æ6 months), and the mean intensity of spontaneous

pain was 55Æ53 (95% CI: 51Æ4–59Æ6).

Pressure pain threshold levels

The 2 · 3 mixed model ANOVA revealed a significant

effect for time (F = 77Æ8; P < 0Æ001) but not for side

(F = 0Æ2; P = 0Æ7) for changes in PPT over the masseter

muscle. Post hoc testing revealed significant differences

between pre-intervention and both post-intervention

and follow-up periods (P < 0Æ001). However, no signif-

icant difference was identified between the post-inter-

vention and follow-up period (P = 0Æ9) for both

masseter muscles. Within-group effect sizes were large

(d > 1Æ0) for both follow-up periods in bilateral masse-

ter muscles. Table 1 details pre-intervention, post-

intervention, follow-up, and change scores of PPT

levels bilateral in both masseter and temporalis

muscles.

The mixed model ANOVA also found a significant effect

for time (F = 66Æ8; P < 0Æ001) but not for side (F = 0Æ07;

P = 0Æ8) for changes in PPT levels over the temporalis

muscle. The post hoc analysis found significant differ-

ences between pre-intervention and both post-inter-

vention and follow-up periods (P < 0Æ001). However,

no significant difference was identified between the

Table 1. Changes in pressure pain thresholds (kg cm)2) over the

masseter and temporalis muscles

Pressure pain threshold (kg cm)2)

in the right masseter muscle

Pre-intervention 2Æ8 � 0Æ7 (2Æ5 ⁄ 3Æ1)

Post-intervention 3Æ9 � 0Æ5 (3Æ7 ⁄ 4Æ2)

Follow-up 3Æ9 � 0Æ6 (3Æ6 ⁄ 4Æ2)

Pre- ⁄ post-differences 1Æ1 � 0Æ8 (0Æ8 ⁄ 1Æ6)

Pre ⁄ follow-up differences 1Æ1 � 0Æ7 (0Æ7 ⁄ 1Æ4)

Pressure pain threshold (kg cm)2)

in the left masseter muscle

Pre-intervention 2Æ3 � 0Æ6 (1Æ9 ⁄ 2Æ6)

Post-intervention 3Æ6 � 0Æ8 (3Æ4 ⁄ 3Æ9)

Follow-up 3Æ5 � 0Æ7 (3Æ1 ⁄ 3Æ8)

Pre- ⁄ post-differences 1Æ3 � 0Æ7 (1Æ0 ⁄ 1Æ6)

Pre ⁄ follow-up differences 1Æ2 � 0Æ8 (0Æ8 ⁄ 1Æ5)

Pressure pain threshold (kg cm)2)

in the right temporalis muscle

Pre-intervention 2Æ4 � 0Æ6 (2Æ1 ⁄ 2Æ7)

Post-intervention 3Æ7 � 0Æ5 (3Æ4 ⁄ 3Æ9)

Follow-up 3Æ5 � 0Æ7 (3Æ2 ⁄ 3Æ8)

Pre- ⁄ post-differences 1Æ3 � 0Æ7 (0Æ9 ⁄ 1Æ6)

Pre ⁄ follow-up differences 1Æ1 � 0Æ7 (0Æ7 ⁄ 1Æ4)

Pressure pain threshold (kg cm)2)

in the left temporalis muscle

Pre-intervention 3Æ0 � 0Æ7 (2Æ7 ⁄ 3Æ3)

Post-intervention 3Æ9 � 0Æ6 (3Æ6 ⁄ 4Æ2)

Follow-up 4Æ0 � 0Æ6 (3Æ6 ⁄ 4Æ3)

Pre- ⁄ post-differences 0Æ9 � 1Æ0 (0Æ4 ⁄ 1Æ4)

Pre ⁄ follow-up differences 1Æ0 � 0Æ8 (0Æ6 ⁄ 1Æ4)

Scores are expressed as mean � s.d. (95% confidence interval).*SPSS, Chicago, IL, USA.

R . L A T O U C H E et al.648

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post-intervention and follow-up period (P = 0Æ9) for

both muscles. Within-group effect sizes were large

(d > 0Æ9) for both follow-up periods in bilateral tempo-

ralis muscles.

Pain

The ANOVA found a significant effect for time (F = 78Æ6;

P < 0Æ001) for changes in pain. Post hoc revealed

significant differences between pre-intervention and

both post-intervention and follow-up periods

(P < 0Æ001). However, no significant difference was

identified between the post-intervention and follow-up

period (P = 0Æ9). Within-group effect sizes were large

(d > 3Æ0) for both post-intervention and follow-up

periods. Table 2 shows pre-intervention, post-interven-

tion, follow-up and differences in scores of pain.

Active pain-free mouth opening

The ANOVA found a significant effect for time (F = 17Æ1;

P < 0Æ001) for changes in active mouth opening. Post

hoc analysis found significant differences between pre-

intervention and both post-intervention (P < 0Æ001)

and follow-up periods (P = 0Æ006). However, no signif-

icant difference was identified between the post-inter-

vention and follow-up period (P = 0Æ7). Within-group

effect sizes were large for both post-intervention

(d > 1Æ0) and follow-up (d > 0Æ8) periods. Table 2 sum-

marizes pre-intervention, post-intervention and follow-

up and change scores for VAS and active pain-free

mouth opening.

Discussion

The results of our study demonstrated that patients

with myofascial TMD treated with manual therapy and

exercise directed at the cervical spine experienced an

immediate decrease (48 h after 10 treatment sessions)

in facial pain, an increase in PPTs over the masticatory

muscles and an increase in pain-free mouth opening.

Additionally, these changes were maintained 12 weeks

after discharge. However, as this was a single cohort

design we could not say if these outcomes were the

result of treatment directed at the cervical spine or

some other variable.

The effect sizes were large for all of outcomes at both

immediate and the 12-week follow-up period. Addi-

tionally, it should be noted that the reduction in pain

was not only statistically significant but also clinically

meaningful as it exceeded the MCID on the VAS,

identified as 9–11 mm (28, 29). The relatively narrow

CI provide greater assurance when making clinical

decisions regarding the treatment effect identified in

this study (43). It should also be noted that even the

lower bound estimates for the 95% CI fell above the

MCID and provided evidence that cervical spine inter-

ventions might be beneficial in the management of

patients with TMD. Mellick and Mellick (44) reported

that treatment of the cervical spine with intra-muscular

injections was effective for reducing symptoms in

patients with orofacial pain. However, our study is the

first to provide preliminary evidence that manual

therapy and exercise directed at the cervical spine

may be beneficial in decreasing facial pain in these

patients.

The increases in PPT levels over both masseter and

temporalis muscles suggests that a hypoalgesic effects

may be induced by treatment of the cervical spine.

Previous evidence suggests that the hypoalgesic effects

occur after manual therapy interventions because of

the activation of the descending inhibitory pathways

(45, 46). It has been demonstrated that joint mobiliza-

tion of the cervical spine produced an increase of 25%

in PPTs in patients with lateral epicondylalgia (47) and

in patients with neck pain (48). In fact, O’Leary et al.

(49) found that the application of the cranio-cervical

flexor exercise protocol used in the current study

induced an immediate local hypoalgesic response in

patients with neck pain. Although the activation of

descending inhibitory pathways following the applica-

tion of manual procedures has not been demonstrated

Table 2. Changes in spontaneous pain (VAS) and active mouth

opening (mm)

Spontaneous orofacial pain

(Visual Analogue Scale)

Pre-intervention 55Æ5 � 8Æ6 (51Æ4 ⁄ 59Æ6)

Post-intervention 20Æ9 � 7Æ1 (17Æ5 ⁄ 24Æ4)

Follow-up 18Æ7 � 7Æ1 (15Æ3 ⁄ 22Æ1)

Pre- ⁄ post-differences )34Æ6 � 8Æ9 ()38Æ9 ⁄ )30Æ3)

Pre ⁄ follow-up differences )36Æ8 � 12Æ0 ()42Æ6 ⁄ )31Æ1)

Active mouth opening (mm)

Pre-intervention 38Æ3 � 5Æ0 (35Æ8 ⁄ 40Æ7)

Post-intervention 42Æ8 � 2Æ7 (41Æ5 ⁄ 44Æ1)

Follow-up 43Æ1 � 2Æ9 (41Æ7 ⁄ 44Æ5)

Pre- ⁄ post-differences 4Æ5 � 3Æ8 (2Æ8 ⁄ 6Æ4)

Pre ⁄ follow-up differences 4Æ8 � 5Æ8 (2Æ1 ⁄ 7Æ6)

Scores are expressed as mean � s.d. (95% confidence interval).

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in patients with TMD this neurophysiological mecha-

nism seems plausible for explaining the bilateral hypo-

algesic effects that occurred in the trigeminal region

with interventions targeted to the cervical spine.

Nevertheless, as no signs of neck dysfunctions and ⁄ or

neck symptoms reported by the patients with TMD

were included in this study, it was difficult to establish a

relationship between the treatment of the cervical spine

and the orofacial effects found in the current study. As

we have discussed, it may be that the effects of cervical

interventions are more generalized rather than specific

for the trigeminal area. Future studies should investi-

gate these neurophysiological mechanisms between the

cervical spine and the orofacial region in patients with

myofascial TMD.

We also found an increase of 4Æ5 mm in pain-free

mouth opening after the treatment of the cervical

spine, which was slightly superior to the results of some

studies investigating changes in active mouth opening

after the treatment of masseter muscle TrPs which

ranged from 2 mm (50) to 4 mm (51). A recent study

has reported that the application of a thrust manipu-

lation targeted to the upper cervical spine resulted in an

increase in active mouth opening (3Æ5 mm) in women

with mechanical neck pain (52). As the application of

cervical interventions induced similar improvements in

mouth opening when compared with treatment of the

masseter muscle, perhaps cervical techniques might be

used as a complementary approach to manage pain in

patients with myofascial TMD. In addition, in patients

with allodynic responses in the facial region, in whom

the manual application of local interventions are often

extremely painful, an indirect approach directed to the

upper cervical spine may be beneficial.

One possible explanation for the increase in pain-free

mouth opening may be related to changes in the

positional afferent inputs of the cervical spine induced

by the protocol. Some studies have demonstrated that

position of the upper cervical spine modifies range of

motion of the mouth (53, 54) Others have shown that

the position of the cervical spine is influenced by the

masticatory muscles (55, 56). De Laat et al. (57) found

that a high percentage of patients with TMD also have

limited movement of the upper cervical spine. There-

fore, it is possible that the protocol applied in the

current study can improve the biomechanical adapta-

tion of the cervical spine with relation to the tempo-

romandibular joint, increasing pain-free mouth

opening. It is also plausible that the reduction in

spontaneous pain in the orofacial region will also

increase pain-free mouth opening.

Our study had several limitations. First, the sample

size was small. Second, we did not include a control

group, so we could not infer a direct cause and effect

relationship between the outcomes and the interven-

tions directed at the cervical spine. It is plausible that

the improvements seen in the patients may be related

to the passage of time. However, we would expect this

to be unlikely given the current duration of symptoms

(9Æ2 months). Furthermore, it was not possible to assess

gender differences because the size of the sample was

small. Future randomized controlled trials with a

greater number of participants and including a control

group which received traditional treatment for myo-

fascial TMD should be conducted in order to further

elucidate the effectiveness interventions directed at the

cervical spine for patients with TMD.

Conclusions

The results of our study demonstrated that patients

with myofascial TMD treated manual therapy and

exercise directed at the cervical spine might be bene-

ficial in decreasing facial pain, increasing PPTs over the

masticatory muscles and increasing pain-free mouth

opening. Furthermore, these changes were maintained

12 weeks after discharge in our population. The effect

sizes were large for all of outcomes at both the 48 h and

12 weeks follow-up periods. Future randomized studies

should investigate the potential of a cause and effect

relationship.

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43. Noteboom JT, Allison SC, Cleland JA, Whitman JM. A primer

on selected aspects of evidence-based practice to questions of

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practice, and self-evaluation. J Orthop Sports Phys Ther.

2008;38:485–501.

44. Mellick LB, Mellick GA. Treatment of acute orofacial pain

with lower cervical intramuscular bupivacaine injections:

a 1-year retrospective review of 114 patients. J Orofac Pain.

2008;22:57–64.

45. Souvlis T, Vicenzino B, Wright A. Neuro-physiological effects

of spinal manual therapy. In: Boyling JD, Jull G, eds. Grieves’

modern manual therapy: the vertebral column, 3rd ed.

Edinburgh: Churchill-Livingstone; 2004:367–379.

46. Wright A. Pain-relieving effects of cervical manual therapy.

In: Grant R, ed. Physical therapy of the cervical and thoracic

spine. New York: Churchill-Livingstone; 2002:217–238.

47. Vicenzino B, Collins D, Wright A. The initial effects of a

cervical spine manipulative physiotherapy treatment on the

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effects on pain, sympathetic nervous system activity and

motor activity. Man Ther. 2001;6:72–81.

49. O’Leary S, Falla D, Hodges PW, Jull G, Vicenzino B. Specific

therapeutic exercise of the neck induces immediate local

hypoalgesia. J Pain. 2007;8:832–839.

50. Rodrıguez-Blanco C, Fernandez-de-las-Penas C, Hernandez-

Xumet JE, Pena-Algaba C, Fernandez-Rabadan M, Lillo-de-la-

Quintana MC. Changes in active mouth opening following a

single treatment of latent myofascial trigger points in the

masseter muscle involving post-isometric relaxation or

strain ⁄ counter-strain. J Bodyw Mov Ther. 2006;10:197–205.

51. Ibanez-Garcıa J, Alburquerque-Sendın F, Rodrıguez-Blanco C,

Girao D, Atienza-Meseguer A, Planella-Abella S et al. Changes

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que-Sendın F, Cleland JA, Bosca-Gandıa JJ. The immediate

effects of atlanto-occipital joint manipulation on active

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fusion on occlusion. Cranio. 1994;12:38–46.

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Correspondence: Roy La Touche Arbizu, Facultad de Medicina,

Universidad San Pablo CEU, Calle Tutor, 35, 28008 Madrid, Spain.

E-mail: [email protected]

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5.7 Estudio VII

La Touche R, París-Alemany A, Mannheimer JS, Angulo-Díaz-Parreño S, Bishop MD,

Lopéz-Valverde-Centeno A, von Piekartz H, Fernández-Carnero J. Does mobilization of

the upper cervical spine affect pain sensitivity and autonomic nervous system function

in patients with cervico-craniofacial pain?: A randomized-controlled trial. Clin J Pain.

2013 Mar;29(3):205-15.

Objetivos del estudio

Los objetivos de este estudio fueron investigar los efectos de la movilización antero-

posterior de la región cervical superior en la modulación del dolor en las regiones

craneofacial y cervical y su influencia en el sistema nervioso simpático.

Resultados

Los UDPs en las regiones craneofacial y cervical aumentó significativamente (P

<0,001) y la intensidad del dolor disminuyó significativamente (P <0,001) en el grupo

de tratamiento en comparación con placebo. La movilización produjo una respuesta

simpatoexcitatoria demostrado por un aumento significativo de la conductancia de la

piel, la frecuencia respiratoria y la frecuencia cardíaca (p <0,001), pero no en la

temperatura de la piel (P = 0,071), después de la aplicación de la técnica en

comparación con el placebo.

Conclusiones

Este estudio proporciona una evidencia preliminar del efecto hipoalgésico a corto plazo

de la movilización articular de la región cervical en las regiones craneofacial y cervical

de pacientes con DCCF de origen miofascial, lo que sugiere que la movilización puede

causar una modulación nociceptiva inmediata en el CTC. Se observó una respuesta

simpatoexcitatoria, lo que podría estar relacionado con el efecto hipoalgésico inducido

por la técnica, aspecto a ser confirmado en estudios futuros.

Does Mobilization of the Upper Cervical Spine Affect PainSensitivity and Autonomic Nervous System Function

in Patients With Cervico-craniofacial Pain?

A Randomized-controlled Trial

Roy La Touche, PT, MSc,*wz Alba Parıs-Alemany, PT, MSc,zJeffrey S. Mannheimer, PT, PhD, CCTT,y Santiago Angulo-Dıaz-Parreno, MSc,wz8

Mark D. Bishop, PT, PhD,z# Antonio Lopez-Valverde-Centeno, MD, PhD,**Harry von Piekartz, PT, PhD,ww and Josue Fernandez-Carnero, PT, PhDwzz

Objectives: The aims were to investigate the effects of anterior-posterior upper cervical mobilization (APUCM) on pain modu-lation in craniofacial and cervical regions and its influence on thesympathetic nervous system.

Methods: Thirty-two patients with cervico-craniofacial pain ofmyofascial origin were randomly allocated into experimental orplacebo groups. Each patient received 3 treatments. Outcomemeasures included bilateral pressure pain thresholds assessed atcraniofacial and cervical points preintervention, after the secondintervention and after the final treatment. Pain intensity andsympathetic nervous system variables (skin conductance, breathingrate, heart rate, and skin temperature) were assessed before andimmediately after each intervention.

Results: The pressure pain thresholds in the craniofacial and cer-vical regions significantly increased (P<0.001) and pain intensitysignificantly decreased (P<0.001) in the treatment group com-pared with placebo. APUCM also produced a sympathoexcitatoryresponse demonstrated by a significant increase in skin con-ductance, breathing rate, and heart rate (P<0.001), but not in skintemperature (P=0.071), after application of the technique com-pared with placebo.

Discussion: This study provided preliminary evidence of a short-term hypoalgesic effect of APUCM on craniofacial and cervicalregions of patients with cervico-craniofacial pain of myofascialorigin, suggesting that APUCM may cause an immediate noci-ceptive modulation in the trigeminocervical complex. We also ob-served a sympathoexcitatory response, which could be related to

the hypoalgesic effect induced by the technique, but this aspectshould be confirmed in future studies.

Key Words: manual therapy, neck pain, temporomandibular

disorders, orofacial pain, craniofacial pain

(Clin J Pain 2013;29:205–215)

Discomfort resulting from temporomandibular disorders(TMDs) is representative of many chronic craniofacial

pain (CCFP) conditions.1 TMD demographics usuallyconsist of working women in the 3rd decade of life withhigh stress levels.2 TMDs are characterized by a focal site oftenderness that provokes nociceptive input and, whenchronic, contributes to the development of central sensiti-zation. Patients with TMDs are known to have greatertemporal summation of pain, suggesting hyperexcitabilityof the central nociceptive system.3,4 More specifically,chronic muscular TMD pain is associated with a generaldysfunction of the central nociceptive system that is con-comitant with central nociceptive neuronal hyperexcitabilityand dysfunction of the descending inhibitory pain systems.5

Women have a 3 times greater risk of experiencing chronicmasticatory myofascial pain than men.6 Patients with TMDsof myofascial origin are also characterized by a general hy-persensibility to mechanical pain stimuli, presenting lowercraniofacial pressure pain thresholds (PPT) of both thepainful and nonpainful side compared with healthy controls.7

Some studies suggest a functional relationship betweenthe jaw and head-neck with regard to craniofacial and cer-vical spine and a concomitance between craniofacial painand neck pain.2,8–10 Patients with craniofacial pain are attwice the risk of experiencing neck pain than the generalpopulation.2 Restricted segmental movements of the uppercervical vertebrae (C0-C3) with a greater percentage of up-per trapezius and sternocleidomastoid tender points exist inpatients with TMDs compared with a control group.11

In addition, Eriksson et al8 demonstrated coordi-nated articular patterns of movement between the temporo-mandibular, atlanto-occipital, and cervical joints, joints thatalso have known sensory-motor interaction via the trige-minocervical complex (TCC). Disturbance of this con-nection between jaw and head-neck movements has beenidentified in patients with whiplash-associated disorders.12

Spinal manual therapy (SMT) is used by physicaltherapists (PTs) to treat chronic musculoskeletal pain.13

Received for publication June 21, 2011; revised February 14, 2012;accepted February 17, 2012.

From the *Department of Physical Therapy, La Salle UniversityCenter, Faculty of Health Science, Aravaca; wResearch Group ofMusculoskeletal Pain and Motor Control, Universidad Europea deMadrid, Villaviciosa de Odon; zInstitute of Neuroscience andCraniofacial Pain (INDCRAN); 8Faculty of Experimental Science,Universidad San Pablo CEU; zzDepartment of Physical Therapy,Occupational Therapy, Rehabilitation and Physical Medicine,Universidad Rey Juan Carlos, Alcorcon, Madrid; **Departmentof Surgery, Faculty of Medicine and Dentistry, Universidad deSalamanca, Salamanca, Spain; yProgram in Physical Therapy,Columbia University, NY; zDepartment of Physical Therapy;#Center for Pain Research and Behavioral Health, University ofFlorida, Gainesville, FL; and wwFaculty of Business, Managementand Social Science, University of Applied Science, Osnabruck,Germany.

The authors declare no conflict of interest.Reprints: Roy La Touche, PT, MSc, INDCRAN, C/Canos del Peral

11, Bajo Izquierdo, 28013 Madrid, Spain (e-mail: [email protected]).

Copyright r 2012 by Lippincott Williams & Wilkins

ORIGINAL ARTICLE

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Various techniques such as passive manipulation and mo-bilization, active mobilization, neuromuscular facilitation,and articular glides are included under the general term ofSMT.14–17 Many SMTs have demonstrated hypoalgesiceffects. This hypoalgesic effect is not antagonized by na-loxone and does not exhibit tolerance,18 supporting thetheory that SMTs activate a nonopioid inhibitory system.In addition, a concomitant activation of the sympatheticnervous system (SNS) occurs after SMT, with the degree ofactivation depending on the technique.19,20

Many studies have investigated the effects of SMT onlower cervical pain,14–16,21 but there is no randomized-controlled trial in which SMT is used to diminish cranio-facial pain. George et al22 compared cervical manipulationwith a soft tissue technique at the cervical-cranial junctionto improve mouth opening in healthy controls, but no sig-nificant results were obtained. Another study examined amanual therapy and therapeutic exercise protocol appliedat the cervical spine, to treat craniofacial pain of myofascialorigin in a cohort intervention study, which resulted in anincrease in the PPT in the masticatory muscles and in-creased mouth opening.23

Consequently, the aims of this study were to extendprevious work by investigating the neurophysiologicaleffects of SMT in patients with CCFP of myofascial origin.Specifically, we studied passive anterior-posterior uppercervical mobilization (APUCM). We expected pain sensi-tivity in the craniofacial and cervical regions to decrease inresponse to treatment. In addition, we expected to observethe sympathetic influence of this technique on skin con-ductance (SC), breathing rate (BR), heart rate (HR), and skintemperature (ST).

MATERIALS AND METHODS

Selection and Description of ParticipantsThirty-two patients with CCFP of myofascial origin

referred from 2 private dental clinics and 3 universities inMadrid, Spain, were recruited from January 2009 to May2010. We defined the term CCFP of myofascial origin aspain and dysfunction located at the cervical and mastica-tory muscles. Patients were selected if they met all of thefollowing criteria: (1) a primary diagnosis of myofascialpain as defined by axis I, category Ia and Ib (eg, myofascialpain with or without limited opening of the mouth) of theResearch Diagnostic Criteria for Temporomandibular Dis-orders24; (2) bilateral pain involving the masseter, temporalis,upper trapezius, and suboccipital muscles; (3) a duration ofpain of at least 3 months; (4) a pain intensity correspondingto a weekly average of at least 30mm on a 100-mm visualanalog scale (VAS); (5) neck and/or shoulder pain withsymptoms provoked by neck postures or neck movement;(6) Neck Disability Index (NDI)25,26 Z15 points; and (7)presence of bilateral trigger points (TrPs) in masseter, tem-poralis, upper trapezius, and suboccipital muscles. TrPs werediagnosed according to the following criteria27: (1) presenceof a palpable taut band in the skeletal muscle; (2) presence ofa hypersensitive tender spot within the taut band; (3) localtwitch response elicited by the snapping palpation of the tautband; and (4) reproduction of referred pain in response toTrP compression.

All patients in the study were examined by a physi-otherapist with 7 years of experience managing craniofacialand cervical disorders. Patients were excluded if they pre-sented any signs, symptoms, or history of the following

diseases: (1) intra-articular temporomandibular disk displace-ment, osteoarthrosis, or arthritis of the temporomandibularjoint, according to categories II and III of the ResearchDiagnostic Criteria for Temporomandibular Disorders24,28;(2) history of traumatic injuries (eg, contusion, fracture, orwhiplash injury); (3) systemic diseases such as fibromyalgia,systemic erythematous lupus, or psoriatic arthritis; (4) neu-rological disorders (eg, trigeminal neuralgia); (5) concomitantmedical diagnosis of any primary headache (tension type ormigraine); (6) unilateral neck pain; (7) cervical spine surgery;(8) clinical diagnosis of cervical radiculopathy or myelopathy;and (9) history of previous physical therapy intervention forthe cervical region. Each participant received a thorough ex-planation of the content and purpose of the treatment beforesigning an informed consent form related to the procedures,which was approved by the local ethics committee in ac-cordance with the Helsinki Declaration.

Research DesignA randomized, double-blind placebo-controlled study

was performed. Patients were blind to which interventionthey received, and an independent assessor, blind to inter-vention assignment made the measurements and registeredthe data. Patients were randomly allocated to either treat-ment intervention or sham intervention. Randomizationwas performed by a computer generated random-sequencetable created with Graphpad software (GraphPad SoftwareInc., CA) before the beginning of the study. The random-ization sequence used a balanced block design in whichrandomization occurred in blocks of 2.

Sample Size CalculationA pilot study was performed with 5 patients in the

treatment group and 5 patients in the sham group to cal-culate the sample size. We used data indicative of the per-cent change in the PPT of the 2 assessed points: 1 at themasseter muscle and 1 at the trapezius muscle.

Sample sizes were calculated to obtain a power of 80%to detect changes in the bilateral contrast of the null hy-pothesis of equal means between the 2 groups, with 5%significance, taking into account the possibility that the SDsof the groups could be different. According to the samplecalculations which took into account the fact that the cal-culation was based on 2 different variables, we obtained 2possible results: 14 patients in each group or 16 patients ineach group. We decided to include 16 patients per group toanticipate the possible loss of patients.

Demographic and Clinical DataEach of the participants completed a questionnaire

to determine if they met the criteria for inclusion or ex-clusion. This questionnaire included demographic data,screening questions for TMDs from the American Acad-emy of Orofacial Pain,29 a body chart on which patientsmarked the location of their pain, and several questionsabout the characteristics of their pain such as “whendid it start?,” “what makes your pain worse?,” “what makesit better?,” and “what kind of pain is it?” To meetthe criteria to participate in the study, patients had to passan initial physical examination performed by a single in-vestigator to rule out the presence of nerve root com-pression.

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Instrumentation and Measurements

Self-reported VariablesPatients completed the Beck Depression Inventory

(BDI),30 the State-Trait Anxiety Inventory (STAI),31 andthe NDI25,26 to quantify their psychophysical state. TheBDI is a 21-item self-report instrument intended to assessthe existence and severity of symptoms of depression. Thereis a 4-point scale for each item ranging from 0 to 3. The resultsof each item, corresponding to a symptom of depression, aresummed to yield a single score for the BDI. A total score of0 to 13 is considered minimal, 14 to 19 mild, 20 to 28 mod-erate, and 29 to 63 severe depression. The BDI showed goodinternal consistency (a coefficient 0.86).30

The STAI31 is a 40-item self-report questionnaire de-signed to assess symptoms of anxiety. It consists of 2 in-dependent scales, a state anxiety scale and a trait anxietyscale, with 20 items each, resulting in a score between 20and 80. Higher scores indicate greater levels of anxiety. Thestate and trait scales explore anxiety as a current emotionalstate and as a personality trait, respectively.

The NDI,25,26 which measures perceived neck disability,consists of 10 items that assess different functional activitiesand uses a 6-point scale ranging from 0 (no disability) to 5(complete disability). The overall score (out of 100) is ob-tained by adding the score for each item and multiplyingby 2. A higher score indicates greater pain and disability. Thevalidity, reliability, and responsiveness of the NDI have beendemonstrated.26

Pain IntensityThe VAS was used to measure pain intensity of the

cervico-craniofacial region at rest and before and after eachtreatment. The VAS is comprised of a 100mm horizontalline in which the left side represents “no pain” and the rightside represents “worst pain.” The patient placed a mark onthe line at the point that they felt represented the intensityof their pain at the time. Pain intensity was quantified bythe assessor in millimeters. This scale has proven its reli-ability and validity for measuring pain intensity.32

Pressure Pain ThresholdPPT is defined as the minimum amount of pressure

needed to provoke a pain sensation.33 We used a digitalalgometer (Model FDX 10; Wagner Instruments, Greenwich,CT) comprised of a rubber head (1 cm2) attached toa pressure gauge, which measures in kg with thresholds ex-pressed in kg/cm2. The protocol consisted of 3 measurementswith an interval of 30 seconds between each measurement.The average of the 3 measurements was calculated to obtain asingle value for each one of the measured points in each ofthe assessments. This algometric method has high reliability(ICC=0.91, 95% CI, 0.82-0.97) for measuring PPT.34 PPTswere assessed bilaterally at 2 points in the masseter muscle(M1 and M2), 2 points in temporalis muscle (T1 and T2),suboccipital muscles, C5 zygapophyseal joint, and uppertrapezius muscle. The device was applied perpendicular to theskin, and the patients were asked to raise their hand themoment when the pressure started to change to a pain sen-sation, at which point the assessor stopped applying pressure.This procedure was performed 3 times: before the firsttreatment session (pretreatment outcome), after the secondtreatment session, and after the third treatment session(2 posttreatment outcomes).

Anatomic references for the algometric measurementsincluded the following: M1—2.5 cm anterior to the tragusand 1.5 cm inferior to the zygomatic arch; M2—1 cm su-perior and 2 cm anterior from the angle of the jaw; T1(anterior fibers of the muscle)—3 cm superior to the zy-gomatic arch in the middle point between the end of the eyeand the anterior part of the helix of the ear; T2 (middlefibers of the muscle)—2.5 cm superior from the helix of theear; suboccipital muscles—2 cm inferior to the occipitalcondyles; C5 zygapophyseal joint—2 cm lateral to the spi-nous process of C6; trapezius muscle—2.5 cm above thesuperior medial angle of the scapula.

Changes in the SNSSeveral characteristics were measured to assess the

SNS: SC, HR, BR, and ST. Measurements were taken be-fore and after each of the 3 treatment sessions. The re-cording device used was I-330-C2+ 6-channel biofeedbacksystem (J&J Engineering Inc., Poulsbo, WA) the MC-6SYsensor was used to measure SC and ST. During the meas-urements 2 electrodes were placed on the tip of the secondand third fingers of the left hand to measure the SC with thetemperature sensor attached to the tip of the fourth fingeralso at the left hand. The MC-5D electrodes used to meas-ure HR were applied longitudinally at the anterior and ra-dial aspect of the wrists and held with bracers. To measureBR, an MC-3MY breathing sensor was placed around thechest like a belt passing over the xiphoid process.

ProcedureThe experiment consisted of 3 treatment sessions. Each

patient received 3 sessions over 2 weeks, and the entire ex-periment lasted approximately 8 months.

The evaluator was a PT with extensive experience intaking the experimental measurements. During the first as-sessment, pretreatment data were obtained; after measuringthe PPT and VAS, the sensors were applied, and the patientwas instructed to lie down on a couch and relax. The roomtemperature was controlled at 251C. After 10 minutes (timedetermined for the patient to come to a normal baseline),the first record of the sympathetic parameters was regis-tered. The patient was then randomly assigned to 1 of the 2intervention groups, and the therapeutic technique wasapplied. Immediately after finishing the technique, SNSvariables were measured, and 5 minutes after the technique,VAS results were registered again. In the second and thirdtreatment session, the SNS variables and VAS were meas-ured using the same protocol (pretreatment and posttreat-ment data), but PPTs were taken only 5 minutes after theend of the treatment (posttreatment data). Therefore, weobtained 3 pretreatment and 3 posttreatment measurementsof SNS and VAS parameters and 1 pretreatment and 2posttreatment measurements (after the second and thirdsessions) of PPT.

Treatment TechniqueAPUCM directly influences the 3 upper cervical seg-

ments (C0-C3). The patient was placed in a supine positionwith a neutral position of the cervical spine. The PT heldthe occipital region of the patient with both hands to stabilizeand maintain the position of the upper cervical structures,while applying a posterior directed force on the frontal re-gion of the patient (anterior to posterior force) with the an-terior part of the shoulder. The mobilization was applied at aslow rate of 1 oscillation per 2 seconds (0.5Hz) controlled

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r 2012 Lippincott Williams & Wilkins www.clinicalpain.com | 207

with an MA-30 digital metronome (Korg Inc., Japan). Thisoscillation rate has been used previously with a differentmanual therapy technique.19 The total time of mobilizationwas 6 minutes. Mobilization was applied in 3 intervals of2 minutes, with 30 seconds of rest in between, resulting in atotal of 7 minutes.

Sham TechniqueTo simulate the treatment technique, the PT applied

the same grips used with the treatment technique: 2 handsunder the occipital bone with the anterior part of 1 shoulderpositioned anterior to the frontal bone, with the patient insupine position. However, mobilization was not applied tothe cervical spine. The contact with the patient was held for3 intervals of 2 minutes with 30 seconds of rest in between.

Both techniques (treatment and sham) were applied bythe same PT, and each participant received the followingexplanation about the intervention: “A physical therapistwill apply a technique on your neck with one hand placedon the posterior part of your neck and the other one onyour forehead. The purpose is to obtain changes in yourneck and craniofacial pain.”

StatisticsStatistical analysis was performed with SPSS version

15.0. A Kolmogorow-Smirnov test was used to determinewhether the sample was consistent with a normal distri-bution (P>0.05). Student t test was used to analyze self-reported psycophysical variables (NDI, STAI, and BDI)and pain duration by comparing the preintervention datafor the treatment and sham groups.

The SNS variables (ST, HR, BR, SC) and VAS weretested with a 2�3 repeated measures analysis of variance(ANOVA); the factors analyzed were time (pre-post) andgroup (treatment and sham). Time�group interactions werealso analyzed. Post hoc analysis with Bonferroni correctionswas performed for specific comparisons between variables.

To determine differences between sessions in VAS andSNS variables, a 2-way ANOVA was used, which analyzedintersession factor and group� intersession interaction(presession 1, presession 2, presession 3). The percentchange for the SNS variables and VAS was obtained rela-tive to the percent change between each session and thepercent of the total of the means in both groups. A 1-wayANOVA was used to analyze the percent change in groupfactor and time factor between sessions (% change session1, % change session 2, % change session 3). The percentchange of the total of the means of the 3 sessions in thetreatment and placebo groups was analyzed with a Studentt test.

A 3�3 mixed-model ANOVAwas used to determine thePPT variables (M1, M2, T1, T2, suboccipital, C5, trapezius);the factors were group (treatment or sham), time (pre, post 1,and post 2) and side (right and left). Bonferroni correctionswere used for post hoc analysis of specific comparisons be-tween variables. Student t test determined the percent changebetween groups between the first session (pretreatment) andlast session (posttreatment 2) outcomes. Throughout allanalyses, statistical significance was set at P<0.05.

RESULTSThirty-two patients (21 females and 11 males) with

CCFP of myofascial origin were included in this study. Nopatients dropped out during the study, and no adverseevents occurred with the APUCM. The t test did not revealany significant differences between groups with regard todemographic details and clinical data (P>0.05), as shownin Table 1. A normal distribution was confirmed with theKolmogorov-Smirnov test (P>0.05).

Pain IntensityThe ANOVA revealed a significant group�time inter-

action (F=135.81; P<0.001), and significant differencesfor the time factor (F=261.7; P<0.001) and group factor(F=32.59; P=0.003) regarding the VAS results. Post hocanalysis also revealed significant differences for the treatmentgroup (P<0.001), but not for the sham group (P=0.3) forthe descriptive data shown in Table 2. A 2-way repeated-measures ANOVA found significant intersession differences(F=11.86; P<0.001) and a group� intersession interaction(F=17.09; P<0.001), indicating that the change fromsession to session was larger for 1 group.

Regarding the percentage of change, a 2-way repeated-measures ANOVA revealed significant differences for groupfactor (F=94.24; P<0.001) and time factor (F=11.3;P<0.001), represented in Figure 1A. The t test also re-vealed significant differences between the percent change ofthe total of the means for the treatment and sham groups(t= �10.03; P<0.001).

Pain Sensitivity

Craniofacial RegionAnalysis of the PPT within the craniofacial region was

performed by a 3�3 mixed-model ANOVA, which revealeda significant effect of time factor [M1 (F=83.65; P<0.001);M2 (F=67.44; P<0.001); T1 (F=98.05; P<0.001); T2(F=18.81; P<0.001)], group factor [M1 (F=12.27; P=0.001); M2 (F=18.35; P<0.001); T1 (F=16; P<0.001);T2 (F=15.85; P<0.001)] and group� time interaction [M1(F=59.65; P<0.001); M2 (F=48.45; P<0.001); T1

TABLE 1. Descriptive Data of the 2 Intervention Groups: Treatment and Sham Groups

Treatment (N=16) Sham (N=16)

Mean SD Mean SD Mean Difference

95% CI for

Mean Difference t P

Age 33.19 9.49 34.56 7.84 �1.37 �7.64 to 4.68 �0.48 0.65NDI 15.69 3.26 16.75 3.94 �1.06 �3.67 to 1.54 �0.83 0.41Pain duration 11.31 6.74 10.69 5.79 0.62 �5.16 to 3.91 �0.28 0.78BDI 13.63 3.64 12.38 4.41 1.25 �2.67 to 3.17 �0.17 0.86STAI 25.75 5.63 24.75 4.66 1 �2.73 to 4.73 �0.54 0.58

BDI indicates Beck Depression Inventory; CI, confidence interval; NDI, Neck Disability Index; STAI, State-Trait Anxiety Inventory; t, t test value.

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F=83.57; P<0.001); T2 (F=16.48; P<0.001)], but notfor side factor [M1 (F=0.94; P=0.76); M2 (F=0.13;P=0.72); T1 (F=0.009; P=0.92); T2 (F=0.64; P=0.43)]. Post hoc testing revealed significant differences be-tween the 3 sessions for the treatment group (P<0.001) butnot for the sham group (P>0.05) at all craniofacial points;descriptive data are shown in Table 3.

The t test revealed significant differences in the percentchange in PPT at the right and left craniofacial points. Figure 2shows the percent change in PPT from the pretreatment andfinal posttreatment assessment.

Cervical RegionA 3�3 mixed-model ANOVA revealed a significant

time effect of the suboccipital musculature (F=96.33; P<0.001), C5 zygapophyseal joint (F=52.37; P<0.001),trapezius muscle (F=57.41; P<0.001), and a group�timeinteraction at the suboccipital region (F=64.12; P<0.001),C5 zygapophyseal joint (F=46.84; P<0.001), and tra-pezius muscle (F=65.3; P<0.001). However, this was notthe case for side factor [suboccipital muscles (F=1.22; P=0.27); C5 zygapophyseal joint (F=1.8; P=0.18); trapeziusmuscle (F=1.57; P=0.22)]. Post hoc analysis revealedsignificant differences in the PPT for the 3 sessions of thetreatment group (P<0.001), but not the sham group(P>0.05), at each cervical point. Descriptive data of PPTfor the cervical region are shown in Table 3.

The t test revealed significant differences in the percentchange in PPT in the right and left cervical points for thetreatment group. Figure 3 shows the percent change in PPTof these measurements from pretreatment and final post-treatment points.

SNS

Skin ConductanceThe ANOVA revealed a significant group�time in-

teraction (F=107.55; P<0.001), an effect of time (F=118; P<0.001), and an effect of group (F=10.45; P=0.003) for changes in SC. Post hoc analysis revealed sig-nificant differences in the treatment group (P<0.001), but

not the sham group (P=0.73). The descriptive data of theSC are shown in Table 2. A 1-way repeated-measuresANOVA found no significant intersession differences (F=0.001; P=0.97) or group by intersession interaction (F=0.32; P=0.57).

ANOVA revealed significant differences in the percentchange between treatment sessions for the group factor(F=31.02; P<0.001), but not the time factor (F=0.72;P=0.48), as shown in Figure 4A. The t test revealed sig-nificant differences between percent change of the totalof the means of treatment and sham groups (t=6.11;P<0.001).

Breathing RateANOVA revealed a significant group�time interaction

(F=8.91; P=0.006) and a main effect of group (F=4.36;P=0.045), but not time (F=0.22; P=0.63), for changesin BR. Post hoc analysis revealed significant differences forthe treatment group (P=0.02), but not the sham group(P=0.08). The descriptive data of the BR are shownin Table 2. A 1-way repeated-measures ANOVA found nosignificant differences for intersession (F=0.13; P=0.87)or for group� intersession interaction (F=0.29; P=0.74).

TABLE 2. Descriptive Statistics for Sympathetic Nervous System Parameters and Pain Intensity, for Pretreatment and PosttreatmentAssessments

Mean±SD

Session 1 Session 2 Session 3

Pre Post Pre Post Pre Post

SCTreatment 1.84±0.61 3.33±0.43 2.10±0.78 3.45±0.38 1.88±0.59 3.4±0.53Sham 2.2±0.58 2.25±0.61 2.21±0.61 2.27±0.55 2.15±0.58 2.20±0.57

HRTreatment 69.56±6.3 73.16±5 71.25±4.39 75.1±2.88 72.05±6.84 77.12±4.12Sham 67.87±7.35 63.81±7.56 67.31±6 63.31±6.73 69.37±5.09 66.12±7.01

RRTreatment 15.31±2.76 16.31±4.13 15.63±1.9 18.38±3.7 15.88±2.56 16.7±3.6Sham 16.58±2.37 14.9±2.99 15.38±1.4 14.28±2.7 15.45±2.2 13.95±2.6

STTreatment 31.45±3.45 28.42±4.39 32.44±3.21 27.53±5.1 30.46±3.67 27.18±4.33Sham 31.71±3.19 29.11±4.07 32.03±2.7 29.56±3.76 31.06±3.26 28.57±3.61

VASTreatment 43.88±7.3 29.66±8.97 31.06±8.83 18.31±9.18 29.31±11.8 14.75±11.8Sham 42.38±9.41 41.5±7.9 45.13±7.9 42.56±6.88 44.31±8.51 42±9.05

BR indicates breathing rate; HR, heart rate; SC, skin conductance; ST, skin temperature; VAS, visual analog scale.

0

10

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-10

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-50

-40

-30

Ch

ang

e in

VA

S (

%)

Sham

-70

-60

-80Session 1 Session 2 Session 3

FIGURE 1. Visual analog scale (VAS) percentage change betweenthe 3 sessions (mean of preintervention and postintervention) fortreatment and sham groups.

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A 1-way ANOVA revealed significant differences inpercent change of BR for the group factor (F=11.34;P=0.002) but not for time (F=1.03; P=0.36) as shownin Figure 4B. The t test revealed significant differences be-tween the percent change of the total of the means for thetreatment and sham groups (t=3.07; P=0.004).

Heart RateANOVA revealed a significant group� time inter-

action (F=54.14; P<0.001) and a main effect of group(F=19.4; P<0.001), but not time (F=0.14; P=0.71),for changes in HR. Post hoc analysis revealed significantdifferences in the treatment group (P<0.001) and the shamgroup (P<0.001); HR data are shown in Table 2. A 1-wayrepeated-measures ANOVA found no significant inter-session differences (F=1.5; P=0.23) or group� interses-sion interaction (F=0.45; P=0.63).

Regarding the percent change in HR, a 1-way re-peated-measures ANOVA revealed significant differencesfor group factor (F=53.66; P<0.001), but not time factor

(F=1.02; P=0.36), as shown in Figure 4C. Significantdifferences between the percent change of the total of themeans for the treatment and sham groups (t=7.37; P<0.001) were observed.

Skin TemperatureThe ANOVA did not reveal any significant group�

time interaction (F=3.49; P=0.071), time factor effect(F=1.62; P=0.2), or group factor effect (F=0.53; P=0.46) for changes in ST. The descriptive data of the ST areshown in Table 2. A 1-way repeated-measures ANOVAfound no significant intersession differences (F=2.84;P=0.06) or group� intersession interaction (F=0.25;P=0.77).

Regarding percent change in ST, a 1-way repeated-measures ANOVA did not reveal a significant difference ingroup factor (F=3.25; P=0.08) or time factor (F=2.74; P=0.07), as shown in Figure 4D. The t test did notreveal a significant difference in the percent change of the

TABLE 3. Descriptive Statistics of PPT Assessed Pretreatment, Posttreatment 1 After the Second Session, and Posttreatment 2 After theThird Session, Taken Bilaterally

Treatment Sham

Right Left Right Left

Pre Post 1 Post 2 Pre Post 1 Post 2 Pre Post 1 Post 2 Pre Post 1 Post 2

Orofacial region

M1 2.13±0.37 3.03±0.5 3.46±0.45 2.12±0.43 2.91±0.53 3.5±0.44 2.29±0.54 2.32±0.48 2.39±0.55 2.28±0.37 2.31±0.62 2.42±0.6

M2 2.12±0.44 2.88±0.44 3.4±0.38 2.09±0.39 2.94±0.36 3.59±0.45 2.18±0.49 2.27±0.56 2.37±0.63 2.12±0.61 2.21±0.45 2.15±0.66

T1 2.76±0.49 3.52±0.5 4.11±0.55 2.69±0.5 3.66±0.54 4.19±0.53 2.81±0.47 2.85±0.46 2.97±0.32 2.89±0.51 2.78±0.57 2.82±0.59

T2 2.97±0.48 3.59±0.51 3.95±0.58 2.8±0.56 3.77±0.47 3.98±0.66 3.04±0.46 2.91±0.61 3.06±0.55 2.86±0.58 2.9±0.46 2.97±0.46

Cervical region

Suboccipital 2.36±0.34 3.33±0.29 3.95±0.22 2.28±0.35 3.38±0.32 3.99±0.22 2.31±0.44 2.43±0.52 2.48±0.63 2.25±0.39 2.35±0.49 2.41±0.54

C5 2.47±0.42 3.09±0.65 3.63±0.52 2.46±0.45 3.26±0.69 3.69±0.49 2.52±0.44 2.55±0.38 2.6±0.4 2.64±0.44 2.74±0.61 2.63±0.43

Trapezius 2.61±0.38 3.51±0.42 4.13±0.67 2.66±0.37 3.62±0.41 4.24±0.5 2.85±0.29 2.82±0.44 2.87±043 2.69±0.4 2.53±0.56 2.6±0.58

Mean±SD.PPT indicates pressure pain thresholds.

100.00

120.00 Treatment/Right SideTreatment/Left SideSham/Right SideSham/Left Side

60.00

80.00

40.00

0.00

20.00

Ch

ang

e in

PP

T (

%)

M1 M2 T1 T2

-20.00

FIGURE 2. Percent change in pressure pain thresholds (PPTs) ofthe craniofacial region (M1 and M2 points of masseter muscleand T1 and T2 of temporal muscle) for treatment and sham in-terventions at right and left sides (mean of preintervention andfinal postintervention). Error bars represent 95% confidence in-tervals of the mean.

Treatment/Right SideTreatment/Left SideSham/Right SideSham/Left Side

Ch

ang

e in

PP

T (

%)

120.00

80.00

100.00

60.00

40.00

20.00

-20.00

0.00

Sub-occipital C5 Trapezius

FIGURE 3. Percent change in pressure pain thresholds (PPTs) ofthe cervical region (suboccipital muscles, C5, and trapeziusmuscles) for treatment and sham interventions on the right andleft sides (mean of preintervention and final postintervention).Error bars represent 95% confidence intervals of the mean.

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total of the means for the treatment and sham groups(t= �1.82; P=0.079).

DISCUSSIONOur findings demonstrate that the APUCM technique

applied at a rate of 0.5Hz significantly increased SNS ac-tivity and produced short-term hypoalgesic effects. We arenot aware of any previous studies that have measured hy-poalgesic effects in the cervical and craniofacial regionsusing APUCM. We therefore contend that this is the firsttime that this specific manual mobilization technique ap-plied at the aforementioned frequency has been investigated,and our data indicate significant differences between theexperimental and control groups.

An increase in PPT was observed after the second in-tervention compared with the presession data and after thethird intervention compared with the first posttreatment as-sessment, which is indicative of a maintained increase overthe successive sessions. With regard to pain intensity, it isimportant to note the decrease in the VAS after each ses-sion, which was maintained from one session to the next andindicates a 41.7% decrease in pain intensity from the 3 ap-plications. A change in the SNS, as evidenced by changes inSC, BR, and HR, was noted after each session, but this trendreversed and was not maintained from one session to the next.Upon comparing the first, second, and third pretreatment

outcomes, it was apparent that the SNS values returned toa normal state of SNS activity. We suggest that the effectproduced by the technique could be due to the influence oftransient sympathoexcitation on pain mechanisms. Our con-tention is that the physiological effects produced by theAPUCM technique influence the suboccipital posterior sym-pathetic network and TCC and act to inhibit or gate my-ofascial pain within the cervico-craniofacial region.

Clinical EffectivenessThe results of clinical pain intensity measured by the

VAS indicate a decrease in the patients’ experience of painat rest with significant differences between treatment andsham groups. Patients who received the intervention re-ported a decrease of 29.13mm in VAS between the pre-treatment and third posttreatment assessment. Todd et al35

have stated that a minimal clinically significant change inVAS may be at least �13mm, whereas more recently, Birdand Dickson36 have contended that a clinically significantVAS change depends on the baseline VAS of the participantand that a change of �13mm would be clinically significantfor a baseline VAS<34mm, a change of �17mm for abaseline VAS between 34 and 67mm, and a change of�28mm for a baseline VAS>67mm. The more specificguidelines of Bird and Dickson are supported by Emshoffand colleagues in a study of chronic TMD pain patients.

120

140

160TreatmentA B

C D

Sham

30

40TreatmentSham

60

80

100

0

10

20

-20

0

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40

Ch

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Ski

n C

on

du

ctan

ce (

%)

-20

-10

0

Ch

ang

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Bre

ath

ing

Rat

e (%

)15 Treatment

-40

Session 1 Session 2 Session 3

Session 1 Session 2 Session 3

Treatment

0

5

10Sham

Sham

-10

-5

-15

Session 1 Session 2 Session 3

Ch

ang

e in

Hea

rt R

ate

(%)

0

-10

-5

-20

-15

-25

Session 1 Session 2 Session 3

Ch

ang

e in

Ski

n T

emp

erat

ure

(%

)

FIGURE 4. Percent change between the 3 sessions (mean of preintervention and postintervention) for treatment and sham groups. A,skin conductance; (B) heart rate; (C) breathing rate; (D) skin temperature.

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They established that to be clinically significant, patientswith a higher pain baseline must demonstrate a greater VASreduction than those with a lower baseline, and the minimalchange should be of �19.5mm or �37.9% of the VAS.37

Our findings are clinically significant according to theguidelines of Todd et al, Bird and Dickson, or Emshoffet al.35–37

SNS ResponsePrevious studies have noted similar effects in the variables

that we measured after SMT in the cervical region.15,17,19,20,38

We observed an increase of 83.75% in SC, which is similar tothat observed by Chiu and Wright19 and Sterling et al15 whoobserved increases of approximately 50% to 60% and 16%,respectively. Studies in which SMT was applied to other bodylocations also noted similar changes in SC. A 16.85% increasein SC was observed after a thoracic mobilization applied toT4,39 and a 13.5% increase in SC was observed after lumbarmobilization.40

A similar effect was noted for HR. We observed an in-crease of 6.06% compared with previous studies that reportedchanges of 10.5%,38 13%,20 and 4.5%.17 A significant changein HR in the sham group was also noted. HR decreased by�5.5% in the sham group, which could indicate that thetreatment can increase HR, whereas the sham application issimilar to a touch massage technique that results in a decreaseof SNS activity.41

Previous studies of BR have reported increases of44%38 and 36%.20 In our study, we observed a 10.4% in-crease in BR in the experimental group. This discrepancycould be due to the type of mobilization that we applied.Previous studies that used lateral cervical glides or poste-rior-anterior mobilization techniques at a frequency of2Hz. A significant change was not obtained in ST despitea downward trend in both treatment and sham groups, asnoted by Chiu and Wright.19 However, a significant de-crease of 2.5% in ST was obtained in another study.15

The results of Sterling et al15 correlate with our datawith respect to the tendency of ST to decrease and the notedchange in SC. Furthermore, significant changes in bloodpressure, which we did not record, have been observed byPaungmali et al,17 Vicenzino et al,20 and McGuiness et al.38

These results confirm that gentle manual mobilizationtechniques on the cervical spine can confer positive phys-iological effects.

Hypoalgesic EffectsOur data indicate that the APUCM technique pro-

duces hypoalgesic effects, as demonstrated by PTT meas-urements made by an algometer, and support a significantdifference between the treatment and sham groups. Sterlinget al15 demonstrated that a unilateral posterior-anteriormobilization applied on the side of pain increased the PPTby 23% on the side of treatment in patients with chronicidiopathic neck pain. We observed increases in PPTbetween 64% and 77% for the masseter muscle points,between 38% and 59% at temporal muscle points and be-tween 47% and 79% for the cervical points after 3 treat-ments of APUCM. The greater change in PPT observed inour study and others may be because our study investigatedshort-term outcomes (3 treatment sessions) instead of im-mediate outcomes (1 treatment session), due to the appliedtechnique and the frequency of mobilization and is in-dicative of a real bilateral hypoalgesic effect at both regions.

Previous research has investigated the effect of spinalmobilization on cervical and lumbar regions and reportedpositive results.15,20,40,42 Sterling et al15 noted a differencebetween the improved PPT in the painful side and thenonpainful side, indicating a unilateral effect from a uni-lateral technique. Our study demonstrates a bilateral in-crease in PPT in both cervical and craniofacial regions. Thisdifference could be due to the central application of thetechnique in this study as opposed to the unilateral appli-cation of Sterling et al.

Manual Therapeutic NeurophysiologyResearch in SMT has focused on the neurophysio-

logical effects of manual manipulation and mobilizationswith data suggesting activation of descendent pain inhibitorysystems upon short-term (initial) hypoalgesic effects.43–45

Skyba et al46 showed that mobilization of the hyperalgesicknee joint in rats produced an antihyperalgesic effect. Thiseffect, which maintained after spinal blockage of opioid orGABA receptors, could be due to descending serotoninergicor noradrenergic inhibitory mechanisms via corticospinalprojections from the periacueductal gray matter (PAG).46

Implications relate to noradrenaline, a PGA neurotransmitterthat is more effective at inhibiting mechanical nociceptionthan thermal nociception, which seems to be serotoninergi-cally mediated.47,48 Others have demonstrated that SMTmight be the ideal stimulus for PAG mediated nonopioidanalgesia, hypoalgesia, sympathoexcitatory effects, and changesin motor activity.15,17,20,49 In the present study, we obtainedboth a sympathoexcitation and hypoalgesic effect after theAPUCM technique, which supports the fact that the d-PAG isinfluenced by the SMT technique.

One controversial issue surrounding manual therapy iswhether a localized segmental and/or extrasegmental effectis produced by SMT. Previous research has shown thatSMT improves symptoms distal to the segment where it isapplied; that is, manipulation applied at the thoracic spinehas positive effects when performed on patients with frommechanical neck pain,14,21 and cervical SMT can result inhypoalgesia at the elbow.50 However, other clinical studieshave shown only segmental effects causing diminished neckpain and PPT after ipsilateral cervical mobilization.15,16

We applied a mobilization technique at the upper cer-vical spine and observed changes in the craniofacial andcervical region as well as hypoalgesic effects further awayfrom the segment to which it was applied, suggesting thatmanual therapy has a general central or at least supra-medullar effect. A physiological or sympathoexcitatoryeffect has also been demonstrated in the upper extremityafter cervical or thoracic SMT,15,39 and in the lower ex-tremities after lumbar mobilization.40

It is clear that SMT activates central structures that con-currently activate sympathoexcitatory and hypoalgesic effectsas demonstrated in our research and in that of others.15,20 Thepresence of an extrasegmental effect may indicate activation ofthe d-PAG and could be mediated by various descending paininhibitory pathways and associated tracts of the TCC thatallow for afferent and efferent transmission between the cer-vical and craniofacial regions.51,52

Nociceptive Modulation and the TCCThe increase in PPT caused by the APUCM technique

on the craniofacial region provides additional clinical

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support for pain modulatory mechanisms in the TCC.A review performed in 1998 outlined neurophysiologicalcoupling between craniofacial and cervical systems.53

It has been observed that manual therapeutic applica-tions to the cervical region provoked a pain reducing effectin the head and face. Mellick and Mellick54 and Mellicket al55 observed that applying a bilateral intramuscular in-jection of small amounts of 0.5% bupivacaine at the cervicalregion caused a decrease in facial pain and headaches. Inaddition, Carlson et al56 demonstrated that an infiltration of2% lidocaine on an active TrP of the trapezius muscle sig-nificantly reduced pain and electromyographical activity ofthe ipsilateral masseter.

The only previous study of manual interventions to thecervical spine to manage craniofacial pain was performedby La Touche et al. This study reported similar results toour study: improved PPT at the masseter and temporalismuscles after a manual therapy protocol directed to thecervical spine combined with a deep neck flexors train-ing program.23

Convergence pathways between cervical and trigemi-nal sensory afferents in the TCC are fully supported.52,57,58

Stimulation of an upper cervical root, such as manipulationof the greater occipital nerve has produced changes in theTCC neurons. This supports the concept that perception ofcranial pain is due to a functional convergence betweentrigeminal and cervical fibers in the TCC59,60 and provides apotential rationale for the relationship between headachesand arm and trunk pain.61

Direct stimulation of the greater occipital nerve (cer-vical input) increases metabolic activity of the TCC62 andtrigeminal nociceptors release neuropeptides, such as sub-stance P, from laminas I and II that diffuse to laminas III toV depending on the intensity of the stimulus.63 The TCCitself is formed by the upper cervical dorsal horns and thetrigeminal nucleus caudalis, which allows nociceptive inputto be transmitted from the TCC to higher centers.64 Painmodulatory structures such as the PAG, dorsolateral pon-tomesencephalic tegmentum, and rostral ventromedial me-dulla control the TCC-mediated generation of antinociceptiveor pronociceptive states.57,58,65

In summary, we propose a neurobiomechanical hypo-thesis to explain the possible mechanism by which a manualtherapeutic technique causes a hypoalgesic effect in cranio-facial and cervical regions. This technique primarily influen-ces the upper cervical region (C1-C3), which is anatomicallyrelated to the occipital bone. We believe that an anterior-posterior glide of the upper cervical structures provokes animproved arthrokinematic relationship of the target regionthereby generating improved pain-free range of movementand concomitant suboccipital muscle relaxation. A secondaryeffect might reduce mechanical forces on the upper cervicalneurovascular structures, thereby interrupting or inhibitinginput and reducing TCC sensitization by activating de-scendent pain inhibitory systems.

In addition, the TCC is the main nucleus that receivesnociceptive information from the face, head, and neck.66

Neurons inside the nuclei are considered multimodal neu-rons and can receive 2 or more inputs from different ori-gins, such as cervical nerve roots, when manual therapy isbeing applied. The input generated from the cervical regioncan alter the nociceptive processing in the TCC and, as aresult, produce a hypoalgesic effect at the facial region.Finally, another possible mechanism to explain the effect ofour manual intervention is that descending pain inhibitory

systems can be activated by SMT on the cervical spine byspinal noradrenergic and serotoninergic pathways from thedorsolateral pons and rostral ventral medulla.45,46

Study LimitationsAlthough the results of our research are positive, we

only measured short-term changes without follow-up testing.We only measured SC and ST on the right side. Other studiesinvestigating sympathetic activation after SMT treatmentonly measured one side of the body, usually the treated side.Perry and colleagues applied a unilateral lumbar mobilizationand measured sympathetic activity at both lower extremities.They only observed significant activation in the treated sidebut did observe a tendency toward sympathetic activation inthe untreated side.40 It would have been interesting to observeif central mobilization activates SNS with the same intensityin both upper extremities and if it has any effect on lowerextremities. It also could have been interesting to measure SCand ST directly on the facial region. We did not measure distalPPT; therefore, due to a lack of information, we cannot pro-vide a complete discussion about the general or segmental ef-fect of the APUCM technique.

This is the first time this type of mobilization at afrequency of 0.5Hz has been used in a clinical randomized-controlled trial. Because different techniques require differ-ent frequencies of application to provoke stronger changes,it would be of interest to test the same mobilization at dif-ferent frequencies of application.

Clinical ImplicationsWe have demonstrated that craniofacial pain can be

modulated through an upper cervical treatment (mobilization).The presence of craniofacial pain is a predictor factor for neckpain.9,67 It is interesting to treat this type of patient with atechnique that has proven effects at the craniofacial segmentthat can also treat a possible neck dysfunction. This techniquemight be contraindicated in patients with craniocervical hy-permobility syndrome due to the movement the APUCMprovokes at the upper cervical spine and the risk this entails.68

Chronic pain can be maintained by SNS modulationthrough the peripheric adrenorreceptor excitation of cat-echolamine.69 Chronic TMD patients seem to present adysregulation of b-adrenergic activity, which contributes toaltered cardiovascular and catecholamine responses.70 Thedysregulation of SNS can contribute to the severity andmaintenance of pain. The influence of APUCM on SNSactivity makes this technique an interesting tool to treatpatients with CCFP of myofascial origin and patients withfacial allodynia, in which other techniques applied directlyon the face would be contraindicated.

CONCLUSIONSWe demonstrate that APUCM reduces pain intensity

and increases PPT in the cervical and craniofacial regions.APUCM also causes sympathoexcitation, which confirms asympathetic effect. These results indicate an influence of themobilization on the CNS (medullar or supramedullar effect).This study provides preliminary evidence of the short-termhypoalgesic effect on the craniofacial and cervical regions ofpatients with CCFP of myofascial origin, suggesting thatAPUCM may cause an immediate nocioceptive modulationat the TTC.

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DISCUSIÓN

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6. DISCUSIÓN

Los hallazgos mostrados en esta tesis coinciden con una gran cantidad de estudios

recientes publicados en las últimas dos décadas. En estas investigaciones de carácter

básico y clínico se ha comprobado como las estructuras cervicales pueden influir sobre

características sensoriales y motoras de la regiones craneofacial y craneomandibular y

viceversa (Armijo-Olivo and Magee, 2007, 2013; Dessem and Luo, 1999; Eriksson et

al., 2004, 2007; Ge et al., 2004; Giannakopoulos, Hellmann, et al., 2013;

Giannakopoulos, Schindler, et al., 2013; Häggman-Henrikson and Eriksson, 2004;

Häggman-Henrikson et al., 2013; Haggman-Henrikson et al., 2004; Hellmann et al.,

2012; Hellström et al., 2002; Hu et al., 2005; Olivo et al., 2010; Svensson et al., 2005;

Torisu et al., 2014). La investigación básica en torno a la neurofisiología del CTC ha

servido para establecer hipótesis y teorías relacionadas con los mecanismos

nociceptivos periféricos y centrales implicados en (Bartsch and Goadsby, 2002, 2003a;

Bereiter et al., 2005; Chiang et al., 1998, 2005; Hu et al., 1993; Lam et al., 2009; Salter,

2004; Sessle et al., 1986; Yu et al., 1995): 1) las comorbilidades entre las dolencias

cervicales y craneofaciales; 2) en la concomitancia motora entre la región

craneomadibular y craneocervical; 3) en las respuestas motoras alteradas; y 4) en las

posibles intervenciones terapéuticas sobre la región cervical que pudieran influir sobre

la región craneofacial. Los resultados de las investigaciones presentadas en esta tesis

ofrecen algunos hallazgos importantes que fortalecen la investigación previa en relación

con esto cuatro puntos. A continuación se discute en profundidad los resultados

obtenidos según los objetivos planteados en la tesis.

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6.1 Diferencias de Género en la Variables Somatosensoriales.

En el análisis del efecto del género sobre variables somatosensoriales en pacientes con

DCCF hay que partir de una premisa epidemiológica y es que como está representado

en nuestros estudios, la prevalencia de estas dolencias es mayor en la población

femenina (Adèrn et al., 2014; Carlsson, 1999; LeResche, 1997; Macfarlane, Blinkhorn,

Davies, Kincey, et al., 2002). Hemos encontrado en el estudio III (La Touche et al.,

2010) y en el estudio V (La Touche, Paris-Alemany, et al., 2014) influencias del género

sobre variables somatosensoriales.

En relación al estudio V (La Touche, Paris-Alemany, et al., 2014) los resultados

mostraron que la percepción del dolor y la fatiga durante el test masticatorio de

provocación estuvo influenciada por el género en los tres grupos evaluados, se observó

que las mujeres presentan una mayor percepción de intensidad de dolor y fatiga

masticatoria, estos resultados coinciden con estudios previos de dolor inducido

experimentalmente realizados con pacientes (Haggman-Henrikson et al., 2004) y

sujetos sanos (Karibe et al., 2003; Plesh et al., 1998), sin embargo es importante

mencionar que otras investigaciones no han observado la interacción del factor genero

sobre el dolor o la fatiga masticatoria inducida experimentalmente (Koutris et al., 2013;

van Selms et al., 2005). El estudio V no está diseñado con el objetivo de identificar los

mecanismos fisiológicos o psicológicos que puedan explicar las diferencias en los

resultados entre mujeres y hombres, sin embargo es importante destacar que la

evidencia de estudios experimentales relacionados con dolor inducido indica que las

mujeres presentan mayor sensibilidad al dolor que los hombres en diferentes pruebas

somatosensoriales (Fillingim et al., 2009). Finalmente destacar que en el estudio III (La

Touche et al., 2010), solo se identificó una interacción con el género en los UDPS del

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músculo tibial anterior, mostrando unos valores significativamente menores en mujeres

respecto a la población masculina del estudio.

6.2 Postura Craneocervical, Dinámica Mandibular y Dolor Craneofacial.

Dos investigaciones (I, (La Touche et al., 2011) y II (Lopez-de-Uralde-Villanueva et

al., 2014) de esta tesis han estudiado la influencia de la postura craneocervical sobre la

función mandibular y las posibles interacciones con mecanismos nociceptivos

trigeminales. Los resultados demuestran que las posturas craneocervicales inducidas

experimentalmente producen modificaciones en MAI presentándose menor o mayor

rango articular según la postura en que se realice el gesto (La Touche et al., 2011), estos

hallazgos también fueron comprobados por Higbie y cols. en 1999 (Higbie et al., 1999).

Además, evidencia previa refuerza estos hallazgos, ya que se han descrito las

modificaciones intra-articulares que se producen en ATM con diferentes posturas

craneocervicales o movimientos cervicales (Ohmure et al., 2008; Solow and Tallgren,

1976; Visscher et al., 2000).

Otro resultado que consideramos relevante en el estudio I, fue que los UDPS de áreas

trigeminales se vieron modificados según las diferentes posturas craneocervicales

siendo el menor UDP registrado en la postura de protracción. Este resultado es difícil

discutirlo ya que no hay estudios similares en esta línea, nosotros plantemos

teóricamente que esto puede suceder debido a cambios o ajustes que realiza el sistema

nervioso bajo diferentes condiciones del entorno y demandas de la región cervical,

creemos que estos ajustes se producen en mecanismos sensoriales pero también en los

motores. En relación a esto, debemos mencionar que contamos con evidencia previa que

describe que los movimientos cervicales o las posturas craneocervicales inducidas

experimentalmente modifican la actividad de la musculatura masticatoria

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incrementándola (Ballenberger et al., 2012; Forsberg et al., 1985; McLean, 2005;

Ohmure et al., 2008).

En el estudio II (Lopez-de-Uralde-Villanueva et al., 2014) se encontraron diferencias en

la postura craneocervical medido con dos instrumentos entre el grupo de pacientes con

DCCF y los sujetos asintomáticos, sin embargo es fundamental tener en cuenta que esos

cambios fueron muy pequeños y en una de la mediciones no superó el MCD y en la otra

los superó pero por muy poco, estos resultados se han encontrado prácticamente con las

mismas similitudes en investigaciones realizadas en pacientes con dolor de cuello

(Silva et al., 2009) y con TCM (Armijo-Olivo et al., 2011) comparada con sujetos

asintomáticos. Por otra parte, cabe mencionar que no se encontró asociación entre la

postura craneocervical con las variables de discapacidad cervical y craneofacial, datos

de otras investigaciones apoyan este resultado (Armijo-Olivo et al., 2011; Cheung et al.,

2010) aunque otros lo contradicen (Lau et al., 2010). La relación entre la postura y los

TCM es controvertida y no está clara según datos extraídos de dos revisiones

sistemáticas recientes (Armijo Olivo et al., 2006; Rocha et al., 2013), además ambas

revisiones coinciden en recalcar que los estudios analizados en relación a esta temática

presentan serias dificultades metodológicas y complica la posibilidad de extraer

conclusiones.

6.3 Influencia del Dolor y la Discapacidad Cervical sobre la Actividad

Sensoriomotora Trigeminal.

En los estudios III (La Touche et al., 2010) y V (La Touche, Paris-Alemany, et al.,

2014) se han obtenido resultados importantes entorno a la influencia del dolor y la

discapacidad de cuello sobre la región craneofacial, específicamente en el estudio V

hemos identificado que los pacientes con moderada y leve discapacidad cervical

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presentan mayores niveles de percepción de dolor y fatiga frente a los sujetos sanos

sometidos al test de provocación masticatorio, es importante mencionar que entre los

grupos de pacientes, el de moderada discapacidad cervical fue el que presentó mayores

cambios en las variables sensoriales medidas durante el test, inmediatamente después y

las 24 horas, La única excepción de esto ha sido en el resultado de la percepción de

intensidad dolor a las 24 horas en que entre ambos grupos no se presentaron diferencias

estadísticamente significativas. A pesar de que existen muchos estudios que utilizan los

test provocación masticatorias para inducir dolor y fatiga (Christensen et al., 1996; Dao

et al., 1994; Farella et al., 2001; Gavish et al., 2002; Karibe et al., 2003; Koutris et al.,

2009; Plesh et al., 1998), solo hemos encontrado un estudio similar al nuestro (estudio

V), (La Touche, Paris-Alemany, et al., 2014), en este Haggman-Henrikson y cols.

(Haggman-Henrikson et al., 2004) observaron que los pacientes con latigazo cervical

presentaron mayores niveles de dolor y fatiga masticatoria inducida por el test que los

pacientes con TCM y sujetos asintomáticos. Diversos estudios experimentales y clínicos

han descrito conexiones funcionales entre las regiones craniofacial y cervical a través de

patrones de convergencia neural en el CTC (Dessem and Luo, 1999; Ge et al., 2004;

Hellström et al., 2002; Hu et al., 2005; Svensson et al., 2005; Torisu et al., 2013; Wang

et al., 2004), en relación con esto se ha observado en estudios experimentales que el

dolor inducido por la infiltración de sustancias algógenas en músculos masticatorios o

cervicales modifican de forma bidireccional la actividad de los reflejos de estiramiento

(Ge et al., 2004; Wang et al., 2004) además, en investigaciones básicas con animales se

ha observado una relación refleja entre la actividad de los nociceptores de la ATM y

actividad del sistema fusimotor de los músculos de cuello (Hellström et al., 2002), esta

información es útil para plantear teorías acerca de la influencia de la región cervical

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sobre los posibles mecanismos nociceptivos (sensoriales) y motores implicados en el

dolor y la fatiga masticatoria.

Contamos con evidencia científica reciente que demuestra que lesiones sobre la región

cervical pueden alterar el control motor masticatorio y la función mandibular normal de

apertura-cierre (Eriksson et al., 2004, 2007; Zafar et al., 2006), los hallazgos de estudio

V se pueden relacionar con esta cuestión ya que nuestros resultados muestran que el test

de provocación masticatorio reduce la MAI libre de dolor al finalizar el test en los tres

grupos, este resultados son similares a la de otros estudios (Karibe et al., 2003;

Svensson et al., 2001), sin embargo hay que tomar en cuenta que esta disminución fue

mayor en los grupos de pacientes y se mantuvo a las 24 horas únicamente en el grupo de

moderada discapacidad cervical, además es importante destacar que el análisis de

regresión mostró que la discapacidad cervical es un predictor de la MAI libre de dolor

(después de 24 horas) en los dos grupos de pacientes. Planteamos la teoría de que los

patrones motores masticatorios estén más alterados a medida que se tenga mayor dolor

o discapacidad cervical, esta situación generaría la activación de mecanismos

compensatorios des-adaptativos que alterarían la conducta, el reclutamiento y la

coordinación de los sistemas motores del cuello y la mandíbula generando mayores

niveles de fatiga y dolor durante los test de provocación y manteniendo estas

sensaciones 24 horas después. Esta misma teoría podría servir para explicar los

resultados de la disminución de los umbrales del dolor a la presión de regiones

trigeminales y cervicales, cabe destacar que los cambios UDPs fueron mayores en los

grupos de pacientes y que la mayoría de cambios en los UDPs de la región cervical a las

24 horas se produjeron en el grupo de moderada discapacidad cervical, como factor

coadyuvante a este situación hay que considerar que la presencia de dolor cuello puede

provocar menores valores de UDPs en puntos trigeminales en comparación con sujetos

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sanos como se observó en el estudio III (La Touche et al., 2010). Aunque consideramos

que puede haber una relación directa entre los cambios sensoriomotores trigeminales

con el dolor y la discapacidad cervical, también tenemos que tener en cuenta la

posibilidad de que en los pacientes los cambios se hubieran visto influenciados

mayoritariamente por la presencia de cambios neuroplásticos ya establecidos a nivel

central; se conoce actualmente que los pacientes con dolor crónico pueden tener mayor

susceptibilidad de presentar un proceso de sensibilización central (Henry et al., 2011),

Wolf y cols. sugieren que en condiciones dolorosas en donde existe una comorbilidad

como es el caso de la muestra de pacientes de este estudio, puede ser un factor

determinante en la pato-fisiología de la sensibilización central (Woolf, 2011). En

relación con esto, Gaff-Radford propone que en la sensibilización central se producen

cambios en las vías aferentes que hacen posible la comunicación de las neuronas

nociceptivas cervicales y orofaciales en el núcleo trigeminal (Graff-Radford, 2012). A

esto hay que añadir que son muchos los estudios que han encontrado en pacientes con

TCM mecanismos periféricos y centrales compatibles con un proceso de sensibilización

central (Anderson et al., 2011; Ayesh et al., 2007; Chaves et al., 2013; Feldreich et al.,

2012; Park et al., 2010; Raphael et al., 2009; Sarlani et al., 2004), sin embargo es

importante destacar que en el grupo de pacientes con dolor de cuello crónico mecánico

del estudio III solo se encontraron diferencias en UDPs en áreas trigeminales y

cervicales pero no en zonas distales, estos nos lleva a pensar que en este tipo de

pacientes hay una posible sensibilización central especifica del CTC.

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6.4. Asociación entre la Discapacidad Cervical y la Discapacidad

Craneofacial/craneomandibular.

En los estudios II (Lopez-de-Uralde-Villanueva et al., 2014) y IV (La Touche, Pardo-

Montero, et al., 2014) se demostró una correlación positiva fuerte-moderada entre la

discapacidad cervical y la discapacidad craneofacial (r=0,79 y r=0,65 respectivamente),

es posible que el resultado del estudio II fuese mejor por la especificidad de la muestra

de pacientes con DCCF seleccionados, hay que tomar en cuenta que la muestra del

estudio IV la conformaron pacientes con diversos tipos de DCF en donde posiblemente

la discapacidad y estatus funcional mandibular no tenga tanto peso, pero esta es una

suposición que se tendrá que comprobar futuras investigaciones. Los resultados de los

estudios II y IV son apoyados por la investigación de Olivo y cols., en esta se encontró

una correlación positiva muy fuerte entre las dos variables de discapacidad (r=0,82)

(Olivo et al., 2010).

6.5 Factores Bioconductuales Implicados en las Alteraciones Sensoriomotoras

Trigeminales y la Discapacidad Craneofacial.

En los estudios III (La Touche et al., 2010), IV (La Touche, Pardo-Montero, et al.,

2014) y V (La Touche, Paris-Alemany, et al., 2014) se utilizaron medidas de auto-

registro relacionadas con el dolor, la discapacidad y factores psicológicos para analizar

las posibles asociaciones con variables sensoriomotoras.

En el estudio V, el análisis de regresión lineal múltiple mostró que el catastrofismo del

dolor y el impacto de la cefalea sobre la calidad de vida (HIT-6) se asociaron a las

variables de percepción de dolor y fatiga 24 horas después de haber realizado el test de

provocación masticatoria. Específicamente en el estudio V el catastrofismo ante el dolor

fue un factor psicológico analizado y mostró ser un predictor de la fatiga a las 24 horas

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en el grupo de moderada discapacidad cervical y en el grupo de leve discapacidad

cervical también fue predictor para la fatiga y la intensidad de dolor percibido 24 horas

después del test provocación masticatorio. El catastrofismo ante dolor se define como

un factor cognitivo que implica una percepción mental negativa o exagerada de la

amenaza percibida tanto real como anticipada de la experiencia de dolor (Sullivan et al.,

2001; Turner and Aaron, 2001).

En cuanto a la fatiga percibida y el catastrofismo no encontramos estudios clínicos o

experimentales en los que hayan estudiado la asociación en pacientes con DCF o TCM,

pero si hemos encontrado dos estudios sobre la relación del catastrofismo del dolor con

variables cinemáticas masticatorias (Akhter et al., 2014; Brandini et al., 2011). En el

estudio realizado por Akhter y cols. se investigó el efecto de un dolor experimental

agudo en una muestra dividida en sujetos con poco catastrofismo y alto catastrofismo,

los resultados de esta investigación mostraron que la intensidad del dolor percibida fue

más alta en los sujetos con mayor catastrofismo y además en este mismo grupo se

observó una velocidad más lenta y mayor variabilidad en los movimientos mandibulares

repetidos, los autores de este estudio sugieren que los cambios en la coordinación

motora son un ejemplo de conducta de evitación que afectan la función del sistema

motor mandibular (Akhter et al., 2014). En la otra investigación, Brandini y cols.

estudiaron variables cinemáticas masticatorias durante un procedimiento de exposición

muy corto (15 segundos) en pacientes con TMC atribuidas a dolor miofascial, en este

estudio no se observaron asociaciones de las variables cinemáticas medidas con

respecto al catastrofismo, sin embargo hay que tomar en cuenta que el propósito del

estudio no era inducir dolor o fatiga para observar la respuesta como si lo hemos hecho

en el estudio V (La Touche, Pardo-Montero, et al., 2014).

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Se debe destacar que en una revisión sistemática muy reciente se concluye que hay una

asociación entre el catastrofismo y la fatiga y que el primero influye proporcionalmente

sobre la segunda y estos resultados se observaron en diversas poblaciones clínicas

(Lukkahatai and Saligan, 2013), también se ha demostrado que en otras dolencias

musculoesqueléticas el catastrofismo del dolor se vio asociado a alteraciones motoras

como la disminución del funcionamiento y rendimiento de las actividades de la vida

diaria y limitación de la capacidad para realizar ejercicio (Meeus et al., 2012; Nijs et al.,

2008, 2012). Además este constructo se ha asociado con una mayor utilización de los

servicios de salud, con la aparición de mayores hallazgos clínicos en la valoración, con

un estado de ánimo negativo (Turner et al., 2001; Turner, Brister, et al., 2005) y con

una alteración estatus funcional mandibular (La Touche, Pardo-Montero, et al., 2014)

como hemos comparado en el estudio IV.

En el estudio IV se evaluó la validez del constructo realizando un análisis de

correlaciones entre la discapacidad craneofacial medida con el IDD-CF con otras

medidas de auto-registro psicológicas y de discapacidad. Se observó una correlación

moderada entre IDD-CF con el HIT-6 y la EVA (r = 0,38 hasta 0,46). Además, ECD y

TSK-11 mostraron una correlación moderada con el IDD-CF y con la sub-escala de

dolor y la discapacidad (r = 0,36 hasta 0,52). Esto es coherente con los datos recientes

que demuestran que los pacientes con DCF y TCM reportaron mayores niveles de

catastrofismo (Campbell et al., 2010; Fillingim et al., 2011; Quartana et al., 2010).

Además el catastrofismo ante el dolor se ha asociado con la progresión hacia altos

niveles de intensidad del dolor y de discapacidad en pacientes con DCF crónica

(Buenaver et al., 2008, 2012; Holroyd et al., 2007; Rantala et al., 2003; Velly et al.,

2011).

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Evidencia previa ha demostrado la relación entre el miedo a los movimientos de la

mandíbula y el DCF (Rollman et al., 2012; Visscher et al., 2010), pero la evidencia

hasta el momento se consideraba limitada. Sin embargo, hay estudios que demuestran

que el miedo al dolor y al movimiento se asocia a una disminución de las actividades de

la vida diaria y también ha sido identificado como un fuerte predictor de discapacidad

en otros trastornos musculoesqueléticos crónicos (Buer and Linton, 2002; Crombez et

al., 1999; Kamper et al., 2012; Vlaeyen et al., 1999; Walton and Elliott, 2013). El

catastrofismo ante el dolor y el miedo relacionado con el dolor son dos constructos que

se han vinculado a la cronicidad del dolor musculoesquelético a través del "Modelo de

miedo-evitación" (Leeuw et al., 2007). En el estudio IV se realizó un análisis de

regresión lineal múltiple en donde se identificó que la intensidad del dolor (EVA: β =

0,19; P = 0,001) y el miedo al dolor y al movimiento (TSK-11: β = 0,17; P = 0,004)

fueron predictores del DCF. Para el estado funcional de la mandíbula y la discapacidad

craneofacial el predictor fue el catastrofismo del dolor (ECD-magnificación: β = 0,25; P

<0,001; β = 0,20; P = 0,007).

La relación entre los factores psicosociales, la actividad motora y el dolor parece estar

presente en diversos casos de dolor musculoesquelético, sin embargo la explicación para

la misma es compleja y limitada hasta el momento. Peck y cols. (Peck et al., 2008) y

Murray y Peck (Murray and Peck, 2007) han planteado una posible explicación y para

ello han generado un nuevo modelo explicativo denominado Modelo integrado de

adaptación al dolor (MIAD). Este modelo explica básicamente que la influencia del

dolor sobre la actividad motora depende de la interacción de las características

multidimensionales (biológicas y psicosociales) del dolor con el sistema sensoriomotor

de un individuo que termina generando una nueva estrategia de reclutamiento motor con

el objetivo de minimizar el dolor, sin embargo esta respuesta motora puede asociarse a

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la aparición de otra dolencia o al empeoramiento del dolor existente (Murray and Peck,

2007; Peck et al., 2008). Este modelo se apoya en el carácter multidimensional

(sensorial discriminativa, afectiva-emocional, cognitiva) que presenta la experiencia de

dolor y cómo este influye sobre el sistema sensoriomotor a través de las conexiones

periféricas y centrales que tiene este sistema con el sistema nervioso autónomo, el

sistema límbico y otros centros superiores (Craig, 2003; Peck et al., 2008).

Recientes estudios de neuroimagen han comprobado como el catastrofismo ante el dolor

(rumiación y desesperanza) puede influir sobre diversas áreas de la corteza cerebral en

pacientes con TCM (Kucyi et al., 2014; Salomons et al., 2012). Salomons y cols.

(Salomons et al., 2012) encontraron en pacientes con TCM una correlación entre la

desesperanza (sub-escala de la ECD) y el grosor cortical del área motora suplementaria

(AMS) y la corteza cingulada media (CCM), los autores de esa investigación sugieren

que la activación de esas áreas en los pacientes con TCM podrían tener una implicación

en aspectos cognitivos de la conducta motora incluyendo las alteraciones de la respuesta

motora, hay que tomar en cuenta que el AMS neurofisiologicamente está implicada en

la planificación del acto motor (Nachev et al., 2007, 2008) y el CCM se ha asociado con

la selección óptima de respuestas motoras en condiciones de incertidumbre (Shackman

et al., 2011). En relación a los pacientes con TCM que presentaron altos niveles de

rumiación (sub-escala de la ECD), Kucyi y cols. (Kucyi et al., 2014) encontraron una

correlación positiva de aumento de la conectividad funcional del córtex prefrontal

medial con la corteza cingulada posterior, el tálamo medial, la corteza retroespinal y la

sustancia gris periacueductal/periventricular, estos resultados indican que la rumiación

ante el dolor podría influir sobre áreas relacionadas con aspectos afectivos y

emocionales de la experiencia dolorosa y con áreas del sistema inhibitorio descendente

del dolor. Parece ser que los cambios funcionales o estructurales en áreas cerebrales no

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solo se presentan en pacientes catastrofistas con TCM, también en otro estudio de

neuroimagen, pero en este caso en pacientes con fibromialgia que presentaban

considerables niveles de catastrofismo, se observó un incremento de actividad en áreas

cerebrales relacionadas con la anticipación del dolor, la atención al dolor, aspectos

emocionales del dolor y el control motor (Gracely et al., 2004), similares resultados se

han encontrado en otras dolencias musculoesqueléticas (Brown et al., 2014).

En el estudio III (La Touche et al., 2010) no se encontraron asociaciones entre los UDPs

de áreas trigeminales o cervicales con las medidas de síntomas depresivos o de

ansiedad. Introducir en esta investigación la valoración de estos síntomas lo

consideramos de gran interés teniendo en cuenta que estos dos factores emocionales se

han relacionado con diferentes situaciones de dolor (Castillo et al., 2013; Roddy et al.,

2013; Simons et al., 2014), a pesar de esto no hemos encontrado ningún tipo de

asociación de los síntomas de ansiedad con otras variables relacionadas con el dolor y la

discapacidad de este estudio. En relación con los síntomas depresivos sí encontramos

una asociación positiva con la intensidad (rho=0,65; P= 0,001) y la cronicidad del dolor

(rho=0,54; P=0.004) y este es un hecho que es recogido por una amplia parte de la

literatura científica (Salama-Hanna and Chen, 2013; Yalcin and Barrot, 2014).

6.6 Efecto del Tratamiento en la Región Cervical sobre el Dolor Craneofacial.

Los resultados de los estudios VI y VII (La Touche et al., 2009, 2012) demuestran que

el tratamiento de fisioterapia en la región cervical produce cambios en los UDPs de

áreas trigeminales y además una disminución en la intensidad del dolor de forma

inmediata y a corto plazo (3 meses), este es un hallazgo que consideramos relevante

teniendo en cuenta que son las primeras investigaciones que estudian estas

intervenciones sobre pacientes con TCM. Otros estudios en pacientes con cefaleas han

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encontrado resultados similares en cuanto a la modulación del dolor con métodos

aplicados en la región cervical como técnicas de neuro-estimulación periférica del

nervio occipital (Jasper and Hayek, 2008; Lee and Huh, 2013; Saper et al., 2011; Serra

and Marchioretto, 2012; Silberstein et al., 2012; Slavin et al., 2006), infiltraciones

locales (Ashkenazi and Levin, 2007; Mellick and Mellick, 2003, 2008; Mellick et al.,

2006; Saracco et al., 2010) o tratamientos de terapia manual (Castien et al., 2011, 2012,

2013; Espí-López and Gómez-Conesa, 2014; Espí-López et al., 2014; van Ettekoven

and Lucas, 2006; Hall et al., 2007; Mongini et al., 2012; Ylinen et al., 2010).

Otro resultado a destacar, en relación al estudio VI (La Touche et al., 2009) es que el

tratamiento sobre la región cervical basado en terapia manual y ejercicio mejora la MAI

libre de dolor. Este hallazgo es interesante ya que estudios experimentales previos

demostraron que una fijación inducida experimentalmente sobre la región cervical altera

la dinámica mandibular disminuyendo el movimiento y la coordinación mandibular

(Häggman-Henrikson et al., 2006). A partir de estos datos, nosotros planteamos

teóricamente que la mejora de la función de la región cervical a través del tratamiento

de fisioterapia puede evocar mecanismos de modulación del dolor en el CTC que

regularían los efectos nociceptivos periféricos y centrales mejorando a su vez la

dinámica mandibular y las estrategias motoras concomitantes cérvico-

craneomandibulares.

6.7 Implicaciones Científicas y Clínicas

De acuerdo al conjunto de resultados de los estudios de esta tesis podemos afirmar que

la discapacidad y el dolor cervical pueden influir sobre variables sensoriales y motoras

del sistema masticatorio; estos hallazgos nos llevan a reflexionar acerca de la

importancia de incluir a nivel clínico una valoración específica de la región cervical

para los protocolos diagnósticos de los TCM. Cabe destacar que los métodos

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diagnósticos y de clasificación más utilizados para los pacientes con TCM no incluyen

una valoración especifica del dolor y la discapacidad cervical (Benoliel et al., 2011;

Schiffman et al., 2010, 2014). Un criterio diagnóstico recientemente observado en los

pacientes con cefalea atribuida a TCM es que los movimientos mandibulares, la función

o la parafunción modifican el dolor sobre la región temporal (Schiffman et al., 2012).

Nosotros hemos observado la asociación de la discapacidad cervical con la MAI libre de

dolor, además hemos identificado que los pacientes con mayor discapacidad cervical

presentan mayor fatiga y dolor inducido por el test masticatorio. Estos hallazgos nos

llevan a suponer que la región cervical puede tener un papel importante sobre este tipo

de cefalea, pero esto tiene que confirmarse en futuras investigaciones ya que estos datos

se pueden extrapolar únicamente a los pacientes con cefalea atribuida a TCM que

además presentaban dolor y discapacidad de cuello. Sabemos en la actualidad que la

prevalencia de dolor de cuello en los pacientes con TCM es muy alta, pero no sabemos

en la actualidad la influencia que tiene la región cervical en aquellos pacientes que no

presentan dolor cuello.

Desde el punto de vista del tratamiento, el plantear un abordaje para reducir el dolor y

la discapacidad cervical como parte de la estrategia terapéutica global podría ser

beneficioso para reducir los síntomas sensoriales negativos y mejorar el control motor

masticatorio, consideramos que este planteamiento debe seguir siendo investigado en

futuros estudios. Parte de los hallazgos de esta tesis demuestran que tratamientos de

fisioterapia basados en terapia manual y ejercicio terapéutico sobre la región cervical

producen efectos positivos sobre la modulación del dolor en áreas trigeminales y sobre

la mejora de la MAI libre de dolor (La Touche et al., 2009, 2012), con los cual

consideramos que es positivo integrarlos en los protocolos actuales para este tipo de

pacientes.

221

En varios de los estudios de esta tesis y en otros estudios longitudinales o transversales

se ha observado la influencia de factores psicosociales sobre pacientes con TCM (Chen

et al., 2013; Fillingim et al., 2011, 2013). Específicamente nuestros resultados muestran

una asociación entre el catastrofismo y la kinesiofobia con variables funcionales, de

discapacidad y DCF, estos hallazgos ponen en manifiesto la interacción entre variables

de tipo sensorial con variables psicológicas y esto debería considerarse como una

cuestión determinante a la hora de plantear la valoración o de diseñar las intervenciones

terapéuticas; en pacientes con dolor crónico es fundamental reconocer factores

psicosociales que pueden ser percibidos como obstáculos para la recuperación (Main,

2013): se ha observado que lograr una disminución del catastrofismo del dolor es un

buen predictor de éxito de la rehabilitación en condiciones de dolor (Sullivan, 2013).

La integración de una perspectiva bioconductual en el razonamiento clínico y en la toma

de decisiones podría ser un punto clave en el manejo del dolor y la reeducación motora

en pacientes con DCF y TCM. Se ha demostrado que el tratamiento cognitivo-

conductual disminuye la intensidad del dolor, los síntomas depresivos, mejora la

función masticatoria (Turner et al., 2006), reduce el catastrofismo en pacientes que

sufren TCM crónicos (Turner, Mancl, et al., 2005) y además se ha observado que en

casos de dolor crónico provoca cambios neuroplásticos adaptativos asociados a una

disminución del catastrofismo del dolor (Seminowicz et al., 2013). Prescribir ejercicio

terapéutico puede ser una buena alternativa a tener en cuenta: en relación a esto se ha

observado que el ejercicio en pacientes con dolor lumbar crónico produce una reducción

del catastrofismo y de los síntomas depresivos y estos resultados fueron similares al

tratamiento cognitivo-conductual (Smeets et al., 2006)

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6.8 Limitaciones y Futuras Investigaciones

Los resultados de esta tesis se han discutido con la consideración de que hay varias

limitaciones que hemos tenido en cuenta y que presentamos a continuación. En los

estudios que conforman esta tesis se han tenido en cuenta algunas variables relacionadas

con la discapacidad y el dolor en la región cervical, sin embargo consideramos que aún

es necesario cuantificar más aspectos de las posibles alteraciones funcionales de la

región cervical como por ejemplo, los rangos de movimiento, la resistencia muscular, la

propiocepción craneocervical y analizar si estas alteraciones pueden tener alguna

relevancia clínica sobre las alteraciones motoras craneomandibulares o sobre el DCF;

sería necesario que futuros estudios precisaran aún más estos aspectos ya que podrían

generar nuevos datos que puedan servir para plantear alternativas diagnósticas y

terapéuticas.

Otra limitación a tener en cuenta, es que en los estudios en donde se ha planteado

intervenciones terapéuticas (VI, VII) solo se han medido los efectos inmediatos y a

corto plazo. Futuros estudios deberían investigar si estas intervenciones tienen un efecto

mantenido a medio y a largo plazo, por otra parte sería necesario realizar estudios de

efectividad de este tipo de intervenciones frente a tratamientos farmacológicos, férulas

oclusales o inclusive otros tratamientos de fisioterapia basados en agentes físicos o

tratamientos de electroterapia.

En esta tesis se han identificado algunos factores psicológicos que han presentado

asociación con la función mandibular y con la discapacidad y el DCF. Desde el

planteamiento neurobiológico de la experiencia multidimensional del dolor (sensorial-

discriminativa, emocional-afectiva, cognitiva) creemos que el haber incluido estas

variables es un acierto ya que ofrece una perspectiva más global de la problemática. A

223

pesar de esto y haciendo una reflexión profunda consideramos que hay otras variables

que son necesarias identificar como por ejemplo la autoeficacia o el tipo de estrategias

de afrontamiento ante el dolor, entre otras. Además sería necesario que los factores

psicológicos identificados como relevantes se sigan estudiando pero con diseños tipo

cohorte, de esta forma se podría establecer relaciones causa efecto. Finalmente y en

relación con la anterior reflexión, creemos que es importante realizar ensayos clínicos

aleatorizados controlados con un enfoque bioconductual donde las intervenciones que se

utilicen se establecieran de forma multimodal para de esta forma intentar influir sobre

variables psicosociales, sensoriales y motoras.

224

225

CONCLUSIONES

226

7. CONCLUSIONES.

1. Las posturas craneocervicales inducidas experimentalmente modifican la

dinámica mandibular y alteran los umbrales de dolor a la presión en áreas

trigeminales en pacientes con trastornos craneomandibulares.

2. Existen pequeñas diferencias en la postura craneocervical entre pacientes con

dolor cérvico-craneofacial y sujetos asintomáticos, pero no se encontraron

asociaciones entre la postura craneocervical y la discapacidad cervical y

craneofacial.

3. Los pacientes con cefalea atribuida a trastornos craneomandibulares con

moderada discapacidad cervical presentan mayores niveles de intensidad de

dolor y fatiga en el test de provocación masticatorio, así como menores umbrales

de dolor a la presión trigeminales y cervicales y una disminución de la máxima

apertura interincisal libre de dolor a las 24 horas posteriores al test de

provocación masticatorio, que los pacientes con leve discapacidad cervical y

sujetos asintomáticos.

4. Los pacientes con dolor de cuello crónico mecánico presentan una hiperalgesia

mecánica en áreas cervicales y trigeminales pero no en áreas extra-trigeminales,

por tanto la sensibilización central en el complejo trigeminocervical podría ser

un mecanismo involucrado en el mantenimiento del dolor de estos pacientes.

5. Existe una asociación entre la discapacidad cervical y la discapacidad

craneofacial en pacientes con dolor craneofacial.

6. La discapacidad cervical es un predictor de la disminución de la máxima

apertura interincisal libre de dolor.

7. La kinesiofobia y catastrofismo ante el dolor son predictores del dolor, la

discapacidad craneofacial y el estatus funcional mandibular.

227

8. El catastrofismo ante el dolor es un predictor de la fatiga masticatoria en

pacientes con cefalea atribuida a trastornos craneomandibulares.

9. Los síntomas depresivos presentan una asociación con la cronicidad y la

intensidad del dolor en pacientes con dolor de cuello crónico mecánico.

10. Las intervenciones fisioterápicas de terapia manual y ejercicio terapéutico sobre

la región cervical provocan efectos hipoalgesicos en áreas cervicales y

trigeminales y mejoran la máxima apertura interincisal libre del dolor en

pacientes con trastornos craneomandibulares.

228

229

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