ORIGINAL ARTICLE

Consensus on Hypotonia via Delphi Process

Pragashnie Naidoo & Robin W. E. Joubert

Received: 11 August 2012 /Accepted: 21 March 2013# Dr. K C Chaudhuri Foundation 2013

AbstractObjectives To generate consensus on the assessment ofhypotonia in the pediatric population, more specifically withrespect to the clinical characteristics and first line tests andmethods to be used to assess these characteristics.Methods Consensus methodology was used. A sample ofexperts was recruited based on specific inclusion criteria. Atwo-round Delphi process was conducted electronically,which was based on a prior literature appraisal and surveyamongst a cohort of clinicians. An a priori threshold marginerror of 70±5 % was pre-determined, with Cronbach’s αmeasuring the level of internal consistency.Results The 2-round iteration was useful in establishingconsensus on clinical characteristics and tests /methods in theassessment of low muscle tone in the pediatric population (2–5 y age band). Twenty-four clinical characteristics, organizedinto 11 clusters were determined as relevant for inclusion.For each characteristic, one test (as a first line assessmentmethod) had been identified with consensus after two rounds.Additionally, consensus on the importance of collateralsources was determined. The ranking order of importance ofcharacteristics however revealed variations.Conclusions The results of this study have displayed thatDelphi, if executed with available guidelines, may be auseful technique in moving towards consensus on issuesthat may be contentious and have assisted in providinginitial data to move towards consensus on the assessmentof hypotonia in children.

Keywords Hypotonia . Assessment . Delphi

Introduction

The assessment of muscle tone forms an integral part of theneurological examination of infants and children. Variations inmuscle tone can also be a sign of both benign and seriousconditions [1], and is viewed as a sign of neurological change[2, 3]. Early detection of variations or alteration in muscle toneis important in establishing a diagnosis correctly and promptly[2]. Although the need to measure muscle tone has beenquestioned, ensuringmore valid and objective clinical methodswill assist in comparable results against a standard or guidelineas well as assist in determining the progress of individuals whoreceive therapeutic interventions to address low muscle tone[4]. A search of the literature indicated a gap in the assessmentof hypotonia with respect to objective measures and thescientific community is yet to gain consensus on these[5, 6]. A survey conducted with occupational therapists,physiotherapists, pediatricians and pediatric neurologistsin South Africa revealed that the 2–5 y age band poses thegreatest challenge in assessment of low muscle tone.Thepurpose of this study was thus to obtain consensus on theclinical criteria andmethods that can be used in the assessmentof hypotonia in this age band. From a literature review,assessment of hypotonia appears to have previously not beenresearched using formal consensus techniques. Formalconsensus methods have become increasingly visible as toolsfor solving problems in health and medicine and in defininglevels of agreement in controversial areas. They are also saidto be useful in reducing bias, and enhancing the lucidity of thejudgmental approach that is often required to define diagnosticor assessment criteria, in the absence of an available goldstandard [7].

Material and Methods

A two-round Delphi technique, preceded by a critical appraisalof the literature and a survey, was used. Participants were

P. Naidoo (*) : R. W. E. JoubertDiscipline of Occupational Therapy, School of Health SciencesUniversity of KwaZulu-Natal (Westville Campus),Private Bag X54001,Durban 4000, South Africae-mail: naidoopg@ukzn.ac.za

Indian J PediatrDOI 10.1007/s12098-013-1018-7

recruited from the clinical disciplines of pediatrics, pediatricneurology, occupational therapy and physiotherapy as theyhave a similar clientele’, and are responsible in the assessmentof muscle tone and in implementation or referrals of interven-tion. A systematic method was utilized for identifying the“experts.” Opinion leaders (gathered by their contributionand attendance at three national pediatric conferences between2010/2011) and clinical researchers in pediatrics (determinedvia the training Universities in South Africa as well as by eachof the specific professional bodies) were considered.

Non–probability purposive sampling was used. Individualswere not selected in an attempt to represent the generalpopulation, but rather in their ability to expertly contribute tothe research questions [8]. Expertise was documented in aself-report.

In order to use the Delphi technique maximally, theauthor collated findings of a literature appraisal, and anelectronic survey (in review and not described in this paper),to inform the Round 1 questionnaire. The Delphi process ishighlighted in Fig. 1 and the questionnaire appears inAppendix 1. Results of Round 1 were collated and assisted inthe development of Round 2.

Prior to round 1, experts were sent an informationpackage, a description of Delphi technique and a consent

letter. Following the implementation of Round 1 and dataanalysis, results were pooled and feedback provided tothe panel with the round 2 questionnaires, electronically.Membership of the panel was not disclosed to the participants(quasi-anonymity). Communication within rounds occurredvia e-mail.

Data was analysed using SPSS 18. The extent withwhich each participant agreed with the stated issue(numerical/categorical scale) and the level of agreementbetween each other (descriptive statistics) were determined.Cronbach’s αwas utilized as a measure of internal consistencyof the group; where cronbach’s α is close to 1.0, it canbe argued that there is consistency in the responses ofthe panel [9]. An a priori consensus thresholdof 70 %(± 5 %) was selected, because of the small number ofpanelists, and one that was considered an acceptablethreshold as noted in a previous study [10]. Analysisand feedback to panelists prior to round 2 includedpercentages of agreement on each item, based on thea priorithreshold, as well as the overall cronbach αscore. Items on which agreement had not been settledhad been highlighted and panelists were encouraged tore-consider their stance on those items that consensuswas not reached on and to re-rate items.

Fig. 1 Outline of Delphiprocess employed in the study

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Tab

le1

Delph

ipaneldemog

raph

ics

ProfGrp

Age

M/F

Years

ofExp

erience

Years

ofExp

erience

(Pediatrics)

PracticeSettin

gHighestLevel

ofEdu

catio

nAvg

Cases

p/wk

Pub

lication

Record

Areas

ofInterest

GeographicArea

P1

Ped

aNeuro

38F

147

HospitalAcademic

MPhil;FCPediatrics

Pediatric

Neurology

11–15

4PaediatricNeurology

KwaZ

uluNatal

P2

OT

31F

1111

Academic

Private

MECIb&

SIPTc

<5

0Occup

ation-Centred

Practice

(Paeds)

CapeTow

n

P3

OT

28F

55

NGO/NPO

Private

Adv

Diploma;

NDT

(Basic

Peds);NDT

(Babies)

5–10

0PaediatricNeurology

Gauteng

P4

OT

35F

1010

Academic

MECIb

<5

2PaediatricOT

KwaZ

ulu-Natal

P5

PT

28F

66

Private

MSc(PedsPhy

sio)

>20

1Prematureinfant

developm

ent

Gauteng

P6

OT

41F

189

Academic

PhD

(OT);MSc(O

T)

NDT(Basic

Peds)

11–15

10Playin

Con

text;The

politics

ofhu

man

occupatio

nCapeTow

n

P7

PT

34F

118

Academic

MScM

ED

(Neurodev)

NDT(Basic/Adv

anced)

<5

0PaediatricPhy

siotherapy

FreeState/Kwa-Zulu

Natal

P8

OT

43F

2121

Private

SIPTc ;MSc(O

T)

Neurosciences;

NDTBasic

Pediatric;

Adv

ancedNDTBabies

16–20

0PaediatricNeurology

KwaZ

ulu-Natal

P9

OT

31F

97

Academic

Private

MSc(OT)Neurosciences

<5

1PaediatricNeurology

Gauteng

P10

Ped

43F

1811

Academic

Hospital

MScM

ED

(Neurodev)

Griffith

sandBayley

Develop

mentalScales

>20

1PaediatricNeurodevelopm

ent

KwaZ

ulu-Natal

P11

OT

33F

115

Academic

MSc(OT);NDT(Basic)

<5

1Edu

catio

n,Neurology

CapeTow

n

aPediatric

neurolog

ist

bMasters

inearlychild

hood

interventio

ncSensory

integrationandpraxistests

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Results

A summary of the demographic information of participantsis highlighted in Table 1. Eleven “experts” from a widegeographical area within South Africa formed the finalpanel. Experience ranged from 5 to 21 y. All experts possessedone or more tertiary qualification, with 10 of the panelistshaving a master’s degree in a pediatric-related field. A numberof panelists (n=8) functioned within an academic setting.Some of the panelists had published in the area of pediatrics,more specifically in the areas of pediatric neurology,neurodevelopment, specific learning disabilities, earlychildhood development and epilepsy.

Of the 24 clinical characteristics listed in Round 1 (n=10),agreement on 22 characteristics (≥70 %) were noted. Twocharacteristics, viz. co-contraction and pronated feet, fellbelow the threshold (i.e., 60 % agreement). These twocharacteristics were thus flagged for the Round 2 Delphisurvey (Fig. 2). In Round 2 (n=9), 78 % of participantsdisagreed that pronated feet should be included as a clinicalcharacteristic, whilst 78 % agreed that co-contraction shouldbe included. For this question, the concept of consensuswas defined as the consistency of opinions amongst thepanelists. Cronbach’s α for the 24 items was 0.86,suggesting that the items had relatively high internalconsistency.

Clinical characteristics were grouped into 11 clusters, viz.reflexes, palpation, motor skills, muscle strength, balance,range of motion, endurance, antigravity positions, posture,excessive drooling and hypotonic facies, to ensure ease inranking of items. Panelists were then required to rank, inorder of importance, those criteria that may be used in theassessment of hypotonia. In Round 1, except for posture, inwhich 70 % of the panelists agreed to it as being the mostimportant clinical characteristic cluster, variation in theother clusters were noted. Further analysis in determiningthe top two, top three and top five clinical characteristicclusters were undertaken. These are represented in Fig. 3(a).Greater variation was noted in administration of the samequestion in Round 2 when panelists were asked to reconsidertheir stance.

The authors were additionally interested to determine thetests and methods of assessments that would be consideredas the first line assessment for each of the 24 characteristicslisted above. The ≥70±5 % threshold was applied. Eighttests/methods were listed that were determined from thepreceding phases of this study, viz. general observation,reflex testing, palpation, manual muscle testing, range ofmotion, antigravity tests, assessment of posture, developmentalassessment and functional assessment. A percentage of ≥70 %agreement on a single test was noted in only 8 of the 24characteristics. The remaining 16 characteristics with the

0

10

20

30

40

50

60

70

80

90

100Fig. 2 Level of agreementfor each clinical characteristicround 1 (n=10). x-axis =clinical characteristics y-axis =level (%) of agreement

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8 options of tests and methods were redistributed to thepanelists in Round 2. Combined results of Round 1 and 2are presented in Fig. 4 graphically. A scatter plot has beenused to depict the results. Following Round 2, consensus forall criteria was reached within the threshold.

Level of Agreement on collateral sources that assist inAssessment: Panelists were required to indicate the level ofagreement, in inclusion of other aspects in the evaluation ofhypotonia, viz. initial interview, parental history, birth anddevelopment history, scholastic performance, developmentalmilestones, functional ability and play activity. Consensus(>70 %) amongst panelists were noted in ALL aspects listed.This was thus not repeated in round 2.

Discussion

The discussion will focus on the clinical characteristics andtests. The literature has both supported and refuted theinclusion the above-mentioned clinical criteria and methodsand tests, in the assessment of hypotonia as well as theirimportance in the diagnostic process. These are describedwithin the 11 clusters described above.

Reflexes The literature supports the use of the deep tendonreflexes as being a valuable aspect of the physical examination.Diminished or absent reflexes are said to be strongly indicativeof disorders of the lower motor unit and also peripheraldisorders [3, 11, 12].

Palpation The current definition of hypotonia indicates thatit is “diminished resistance to passive movement,” [13]hence inclusion of this characteristic is undoubtedly relevantin the establishment of hypotonia in a child.

Motor Skills Contradictory evidence was present within theliterature. In one study, hypotonia was considered to not berelated to motor delays at specific developmental periods[14]. Other studies indicate that delayed achievement ofmotor milestones may be the predominant difficulty in olderinfants and children with hypotonia [15], and that reducedaxial tone may lead to a delay in acquisition of motormilestones [1]. Whether hypotonia itself is evidenced bymotor delay remains unclear. This relationship requiresfurther clarity.

Muscle Strength The literature supports the testing of musclestrength. Distinction needs to however be made fromthe child with hypotonia with weakness and withoutweakness [1, 12] as there are varying implications [1,16]. Most of the literature reports that hypotonia andgeneralized muscle weakness are correlated [17, 18],however children with central motor problems, may havesignificant hypotonia, but have reasonable strength [17]. Giventhe variability of responses between the panelists and theliterature, the authors suggest caution in making assumptionsthat children with hypotonia may present with weakness.As this may be contributory to the diagnostic processes,the challenge for clinicians is to link muscle tone withstrength in a way that is objective.

Balance A review of the literature, did not reveal anystudies that considered the relationship of balance tohypotonia. However, inclusion of balance as a clinicalcharacteristic in the assessment of hypotonia was agreedon by 100 % of panelists. The authors suggest that the

a

b

Top 2

Top 3

Top 5

Top 2

Top 3

Top 5

Fig. 3 a Ranking of importance of clinical characteristic clusters round 1(n=10). b Ranking of importance of clinical characteristic clusters round2 (n=9). x-axis = clinical characteristics y-axis = % of agreement

Indian J Pediatr

reason for agreement on balance, by the panelists, is thefact that children who present with hypotonia, oftendisplay clumsiness [18], which may inevitably appearto affect their ability to maintain their balance. However,this relationship requires further investigation.

Range of Motion Many authors have acknowledged theassociation between hypermobile joints and hypotonia[14, 15, 17]. Some authors have also indicated that jointlaxity may be as a result of genetic defects [14], how-ever other authors suggest that joint laxity may be theresult of hypotonia [19]. Although there is evidence toindicate that hypotonia and hypermobility frequentlyoccur together, the exact nature of this relationship andcontributing factors remains unclear.

Endurance In one study [6], 92.5 % of the sample of 80occupational and physiotherapists, agreed on decreasedactivity tolerance as being a common symptom in childrenwith hypotonia. In a follow-up study [5], the same authors,again indicated that a high percentage (68 %) of pediatricoccupational and physiotherapists in a sample of 268therapists, presented this aspect as being indicative ofhypotonia. Crawford (1992) [15], however indicates that

fatigue is challenging to examine in an infant or youngchild as it requires sustained and maximal effort, whichis difficult to elicit in young children. The authors,however cautions against the use of this characteristicwithout substantive evidence.

Antigravity Positions A relationship between muscle powerand ability to assume antigravity positions exist [11, 20],in the younger child. Authors of papers on assessment ofhypotonia have emphasized the value of antigravity po-sitions in the neurological assessment of floppy children[1, 11, 12, 16]. Moreover, reduced ability in maintainingantigravity postures in the hypotonic child is often saidto be a sensitive and specific sign for neuromusculardisorders [17].

Posture Postural assessment has been emphasized by manyauthors of papers on hypotonia [5, 11, 17, 19, 20].

Drooling A child who has hypotonia may exhibit oral-motordysfunction that may result in excessive drooling. Droolingmay also be an indicator of weakness, where there is poorswallowing ability (indicated by drooling) and oropharyngealpooling of secretions [16].

6062646668707274767880828486889092949698

100 Increased Flexibility

Diminished Resistance to Passive Movement

Delayed Motor Skills

Leaning on External Supports

Rag-doll Postures

Difficulty in Supine and Prone Postures

Hypermobile Joints

Postural Fixations

Postural Asymmetry

Decreased Activity/Task Tolerance

Diminished or Absent Reflexes

Winging of the Scapula Posture

"W or M" Sitting Postures

Co-contraction

Frog-like Postures

Reduced Balance

Postural Alignment

Pronated Feet

Protruding Abdomen

Increased Kypho-lordosis

Excessive Drooling

Poor Endurance

Muscle Weakness

Fig. 4 Combined results of preferred test/method for each characteristic (n=10 round 1; n=9 round 2). x-axis = preferred test/method y-axis = %of agreement

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Hypotonic Facies The presence of “myopathic” facies and apaucity of facial expressions are common in hypotonic infants[17]. These may also include open mouth with tented upperlip, poor lip seal when sucking, ptosis and restricted ocularmovements [20].

Conclusions

There appears to be no gold standard for the clinicalassessment of hypotonia in children. The 2-round Delphiprocess described in this paper was useful in establishingconsensus on clinical characteristics and tests/methodsin the assessment of low muscle tone within the 2–5 yage range. These findings have been correlated with

relevant literature supporting its inclusion in the diagnosticand assessment process. This paper thus provides a startingpoint in moving clinicians towards more comprehensiveand objective measures of testing hypotonia in childrenwithin the 2–5 y age range, based on an expert opinionvia consensus.

Acknowledgements The authors would like to thank Mr SathieshGovender, data scientist, of I and S Transdata, for his assistance in dataanalysis.

Conflict of Interest None.

Role of Funding Source None.

Appendix 1. Delphi round 1 questionnaire

CLINICAL CHARACTERISTIC /SYMPTOM / SIGN

DISAGREESTRONGLY

DISAGREESLIGHTLY

AGREESLIGHTLY

AGREESTRONGLY

1. Increased flexibility

2. Diminished resistance to passive movement

3. Delayed Motor skills

4. Leaning on external supports

5. Rag-doll postures

6. Difficulty in supine and prone postures

7. Hypermobile joints

8. Postural fixations

9. Postural asymmetry

10. Decreased activity/task tolerance

11. Diminished or absent reflexes

12. Winging of the scapula posture

13. “W” or “M” sitting postures

14. Co-contraction

15. Frog-like postures

16. Reduced balance

17. Postural alignment

18. Pronated feet

19. Protruding abdomen

20. Increased kypho-lordosis

21. Excessive drooling

22. Poor endurance

23. Hypotonic facies

24. Muscle weakness

Q1. For each of the characteristics below, please indicate if you agree or disagree, as to whether that characteristic willassist a clinician in determining if a child (aged between 2 and 5 y) has hypotonia. Please mark your response with an X.

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Bygeneral

Observatio

nReflex

testing

Palpatio

nManualMuscle

Strength

Range

ofMov

ement

Antigravity

Tests

Assessm

entof

Posture

Develop

mental

Assessm

ent

Fun

ctional

Assessm

ent

Non

e/do

n’t

know

1.Increasedflexibility

2.Dim

inishedresistance

topassivemov

ement

3.Delayed

motor

skills

4.Leaning

onexternal

supp

orts

5.Rag-dollpo

stures

6.Difficulty

insupine

andpron

epo

stures

7.Hyp

ermob

ilejoints

8.Posturalfixatio

ns

9.10

Posturalasym

metry

10.Decreased

activ

ity/task

tolerance

11.Dim

inishedor

absent

reflexes

12.Winging

ofthescapulapo

sture

13.“W

”or

“M”sitting

postures

14.Co-contraction

15.Frog-lik

epo

stures

16.Reduced

balance

17.Posturalalignm

ent

18.Pronatedfeet

19.Protrud

ingabdo

men

20.Increasedky

pho-lordosis

21.Excessive

droo

ling

22.Poo

rendu

rance

23.Hyp

oton

icfacies

24.Muscleweakn

ess

Q2.

For

each

characteristic

listed,

please

indicate

which

method

ofassessmentor

test

would

best

assist

youin

theclinical

setting

indeterm

iningifachild

has

hypotonia?

Pleasemark(X

)ONERESPONSEONLY.

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Thank you for taking the time to complete this survey

CHARACTERISTIC CATEGORIES RANK ORDER

1. REFLEXES (Diminished or absent)

2. PALPATION

Diminished resistance to passive movement

3. DELAYED MOTOR SKILLS

4. MUSCLE STRENGTH (Weakness)

Co-contraction

5. BALANCE (reduced/impaired)

6. RANGE OF MOTION

Increased flexibility

Hypermobile Joints

7. ENDURANCE (reduced)

Decreased activity or task tolerance

8. ANTIGRAVITY POSITIONS

Supine Flexion and Prone Extension Postures

9. POSTURE

“W” or “M” sitting

Winging of the scapula

Postural Fixations

Postural Asymmetry

Increased kypho-lordosis

Pronated feet

Protruding Abdomen

Frog-like Postures

Leaning on External Supports

10. EXCESSIVE DROOLING

11. HYPOTONIC FACIES

Q3. Which categories of characteristics would you consider to be most important when determining if a child hashypotonia. Please rank them in order of importance from 1 (most important) to 11 (least important).

Q4. Thinking now about the clinical assessment of hypotonia in children, irrespective of underlying cause, and holisticmanagement, please could you tell me how important it is for each of these to assist in drawing your final clinical opinion?.

Please mark oneanswer for eachstatement

Not at allimportant(1)

SomewhatImportant(2)

Important(3)

Veryimportant(4)

1. Initial Interview

2. Parental history

3. Birth andDevelopmentalHistory

4. Referral to otherprofessionals

5. ScholasticPerformance(if available)

6. DevelopmentalMilestones

7. Functional Ability

8. Play Activity

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