The extend of orthodontically induced inflammatory root resoption ...

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TRESO

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THE EXTENT OF ORTHODONTICALLY INDUCED INFLAMMATORY ROOT RESORPTION FOLLOWING TRANSVERSE AND VERTICAL JIGGLING

MOVEMENT WITH HEAVY FORCES FOR 12 WEEKS: A MICRO‐CT STUDY

CAROLYN NG ii

DEDICATION

To my loving husband Andrew

For all your patience, love and support on this journey with me,

To my parents Gloria and Ming

For all your inspiration, encouragement and guidance,

To Selena and Jonathan

For all your insight and companionship,

To all my dearest family and friends

For all your thoughts and prayers,

“With God all things are possible”

Matthew 19:26



CAROLYN NG iii

ACKNOWLEDGEMENTS

“I can do everything through Him who gives me strength.” Philippians 4:13

Professor M Ali Darendeliler, Head of Department, Discipline of Orthodontics, University of Sydney

for all your supervision and support throughout this thesis,

Professor Turk, and his team, Department of Orthodontics, Ondokuz Mayis University and Assistant

Professor Fethiye Cakmak, Department of Orthodontics, University of Bulent Ecevit, for all your

collaboration with this study, and your assistance in the collection of the samples,

Dr Oyku Dalci, Senior Lecturer, Discipline of Orthodontics, University of Sydney for your advice and

supervision of the project,

Dr Matthew Foley, Australian Centre for Microscopy and Microanalysis, University of Sydney, for

your help and expertise with the micro‐CT processing and analysis,

Associate Professor Peter Petocz, Department of Statistics, Macquarie University Sydney, for your

help and expertise regarding the statistical analysis of the project,

To the postgraduate students from the Department of Orthodontics at the University of Sydney for

your dedication, effort, and guidance which have helped shape this research,

Finally, to all my tutors and dedicated role models within the Orthodontic Department, Discipline of

Orthodontics, University of Sydney, for all your nurturing patience, support and expertise throughout

this new stage in my career.



CAROLYN NG iv

Table of Contents

DECLARATION ....................................................................................................................................... i

DEDICATION ........................................................................................................................................ ii

ACKNOWLEDGEMENTS ....................................................................................................................... iii

ABBREVIATIONS ................................................................................................................................ viii

1. INTRODUCTION ........................................................................................................................... 1

2. LITERATURE REVIEW ................................................................................................................... 3

2.1 Cementum ................................................................................................................................. 3

2.1.1 Characteristics of Cementum ............................................................................ 3

2.1.2 Development, Structure and Function of Cementum ........................................ 4

2.2 Orthodontically Induced Inflammatory Root Resorption ........................................................... 8

2.2.1 History & Definition .......................................................................................... 8

2.2.3 Incidence & Prevalence ..................................................................................... 9

2.2.4 Classification, Grading and Diagnosis ................................................................ 9

2.2.5 Biochemical Assays ......................................................................................... 12

2.2.5.1 Saliva ....................................................................................................... 12

2.2.5.2 Gingival Crevicular Fluid .......................................................................... 13

2.2.5.3 Urinary Excretion Products ...................................................................... 13

2.2.5.4 Serum ...................................................................................................... 13

2.2.6 Aetiology......................................................................................................... 14

2.2.6.1 Biologic Risk Factors ................................................................................ 14

2.2.6.1.1 Genetic Factors................................................................................. 14

2.2.6.1.2 Environmental Factors ...................................................................... 15

2.2.6.1.2.1 Systemic .................................................................................... 15

2.2.6.1.2.2 Local .......................................................................................... 17



CAROLYN NG v

2.2.6.2 Mechanical Risk Factors ........................................................................... 19

2.2.6.2.1 Force Magnitude .............................................................................. 19

2.2.6.2.2 Treatment Duration .......................................................................... 20

2.2.6.2.3 Appliances and Treatment Philosophy ............................................. 20

2.2.6.2.4 Distance, Type and Direction of Tooth Movement ........................... 22

2.2.6.2.5 Pattern of Force Application ............................................................. 24

2.2.7 Pathogenesis ................................................................................................... 25

2.2.7.1 Mechanism of resorption: histopathology and biochemical mediators ... 25

2.2.7.2 Resistance and Repair .............................................................................. 26

2.2.8 Prognosis and Prevention, Management ........................................................ 28

2.3 Research Methods for Investigation and Evaluation of OIIRR .................................................. 31

2.3.1 Radiography (2D) ............................................................................................ 31

2.3.2 Histologic Analysis (2D) ................................................................................... 32

2.3.3 Scanning Electron Microscopy (2D) ................................................................. 32

2.3.4 X‐ray Micro‐Computed Tomography (3D) ....................................................... 33

3. REFERENCES .............................................................................................................................. 37

4. MANUSCRIPT ............................................................................................................................ 57

4.1 Abstract ................................................................................................................................... 59

4.2 Introduction ............................................................................................................................. 60

4.3 Material and Methods ............................................................................................................. 61

4.3.1 Sample ............................................................................................................ 61

4.3.2 Appliance Design ............................................................................................ 62

4.3.3 Specimen Collection ....................................................................................... 62

4.3.4 Specimen Analysis........................................................................................... 63

4.3.5 Statistical Analysis ........................................................................................... 63

4.4 Results ..................................................................................................................................... 64



CAROLYN NG vi

4.5 Discussion ................................................................................................................................ 64

4.6 Conclusion ............................................................................................................................... 72

4.7 Acknowledgement ................................................................................................................... 72

4.8 References ............................................................................................................................... 73

4.9 Figures ..................................................................................................................................... 76

Figure 1: Experiment protocol ................................................................................ 77

Figure 2: Mean resorption values for heavy jiggling forces.Error! Bookmark not defined.

Figure 3: Mean resorption values for each vertical third region. ............................. 78

Figure 4: Mean resorption values for each root surface.Error! Bookmark not defined.

4.10 Tables ...................................................................................................................................... 81

Table 1: Force Direction: ANOVA Findings ................... Error! Bookmark not defined.

Table 2: Force Direction: Mean Resorption Values (mm)Error! Bookmark not defined.

Table 3: Vertical Third Regions: ANOVA Findings ......... Error! Bookmark not defined.

Table 4: Vertical Third Regions: Mean Resorption Values (mm)Error! Bookmark not defined.

Table 5: Vertical Third Region: Overall Mean Resorption Values (mm) per Force Direction

.................................................................................... Error! Bookmark not defined.

Table 6: Vertical Third Region vs. Force Direction: Mean Resorption Values (mm)Error!

Bookmark not defined.

Table 7: Tooth Surface: ANOVA Findings ..................... Error! Bookmark not defined.

Table 8: Tooth Surface: Mean Resorption Values (mm)Error! Bookmark not defined.

Table 9: Tooth Surface: Overall Mean Resorption Values (mm) by Force DirectionError!

Bookmark not defined.

Table 10: Tooth Surface vs. Force Direction: Mean Resorption Values (mm)Error! Bookmark

not defined.

5. Future Directions ...................................................................................................................... 85

6. Appendices ............................................................................................................................... 86



CAROLYN NG vii

6.1 Sample Distribution ................................................................................................................. 86

6.2 Specimen Collection Sequence ................................................................................................ 87

6.3 Specimen Analysis Sequence ................................................................................................... 88

6.4 Total Volumetric Resorption per Tooth .................................................................................... 89

6.5 Total Volumetric Resorption per Region .................................................................................. 89

6.6 Total Volumetric Resorption per Surface ................................................................................. 90



CAROLYN NG viii

ABBREVIATIONS

2D Two Dimensional

3D Three Dimensional

AAC Acellular Afibrillar Cementum

AEFC Acellular Extrinsic Fibre Cementum

AIFC Acellular Intrinsic Fibre Cementum

ALT‐RAMEC Alternating Rapid Maxillary Expansion And Contraction

cAMP Cyclic Adenosine Monophosphate

CIFC Cellular Intrinsic Fibre Cementum

CEJ Cemento‐Enamel Junction

CMSC Cellular Mixed Stratified Cementum

DCJ Dentinocemental Junction

ERM Epithelial Rests Of Malassez

FEM Finite Element Model

HERS Hertwig’s Epithelial Root Sheath

Hz Hertz

IL‐1 Interleukin‐1

IL‐1b Interleukin‐1 Beta

IO Instrumental Orthodontitis

IDO1 Instrumental and Detrimental Orthodontitis Grade 1

IDO2 Instrumental and Detrimental Orthodontitis Grade 2

Micro‐CT Micro Computed Tomography

MM Millimetres

NSAID Non‐Steroidal Anti‐Inflammatory Drug

OIIRR Orthodontically Induced Inflammatory Root Resorption

OPG Osteoprotegrin

PA Periapical Radiograph

PDL Periodontal Ligament

PGE2 Prostaglandin E2

RANK Receptor Activator Of Nuclear Factor Kappa Beta

RANKL Receptor Activator Of Nuclear Factor Kappa Beta Ligand

SEM Scanning Electron Microscopy

TIFF Tagged Image File Format

TMA Beta‐Titanium Molybdenum Alloy

TNF Tumour Necrosis Factor

TNFRSF11A Tumour Necrosis Factor Receptor Super‐Family 11 Alpha

TRAP Tartrate Resistant Acid Phosphatase

XMT X‐Ray Microtomography



CAROLYN NG 1

1. INTRODUCTION

Orthodontically induced inflammatory root resorption (OIIRR) is the term given to the

unavoidable pathologic loss of root structure that occurs as a consequence of orthodontic tooth

movement.1 In 2014, the localised aseptic inflammation produced by orthodontic force application

has been considered under a new term, Orthodontitis, which also encompasses the various types of

OIIRR within the groups of Instrumental‐Orthodontitis (IO) and Instrumental‐Detrimental

Orthodontitis (IDO).2

The incidence of OIIRR in adults has been reported at 25‐76% after at least 12months of

treatment,3‐7 while in adolescents it has been reported at 5‐18%.4, 8‐10 When graded scales are used,

OIIRR is usually classified as minor or moderate in most orthodontic patients.10‐13 Severe resorption,

exceeding 4mm or one‐third of the original root length is reported to be seen in 1% to 5% of teeth.6, 8,

10‐12, 14‐16

A reduced root length subsequent to OIIRR could potentially compromise the longevity of

affected teeth by complicating restorative treatment planning, and placing affected teeth at greater

risk of loss secondary to periodontal disease or trauma. Fortunately, in the majority of cases, the

extent of root loss is mild and inconsequential to the long term survival and functionality of the

affected teeth or dentition. 17, 18

Since the relationship between root resorption and orthodontic treatment was proposed in

1914,19 OIIRR has been studied extensively, both radiographically and histologically. As a result of

these studies, OIIRR is recognized as having a multifactorial aetiology, and risk factors for OIIRR are

classified as either biologic or mechanical in origin. Biologic factors include both genetic and

environmental factors, which may be further divided into either systemic or localised factors.

Mechanical factors pertain mainly to various characteristics of orthodontic force application.



CAROLYN NG 2

Alternating patterns of orthodontic force application or “jiggling forces” have long been

implicated in OIIRR.8, 20‐22 This study follows on from a forthcoming prospective x‐ray

microtomography study investigating the effect of light (25g) and heavy (225g) jiggling forces in

comparison with unidirectional light and heavy forces on human premolars.23 To supplement this

investigation, this study aims to compare the effect of controlled heavy (225g) jiggling forces

occurring in 4 weekly cycles in the transverse and vertical plane over a 12 week period utilising x‐ray

micro‐tomography for qualitative and quantitative volumetric analysis. In doing so, this study aims

to elucidate the effect of this pattern of force application in the process of OIIRR; in continuance of

root resorption research conducted by the Orthodontic Department in the Faculty of Dentistry at The

University of Sydney.



CAROLYN NG 3

2. LITERATURE REVIEW

2.1 Cementum

The principal tissue of the tooth that is concerned with orthodontically induced inflammatory

root resorption is cementum. Together with the periodontal ligament, alveolar bone and gingiva,

cementum forms a structural and functional unit, which surrounds and supports the teeth,

collectively known as the periodontium.24 The primary function of cementum is to anchor the

principal collagen fibres of the periodontal ligament to the root surface. It is described as a

specialised, complex, and responsive tissue that is slowly formed throughout life, allows for continual

reattachment of the periodontal ligament fibres and is capable of repair, regeneration and pulpal

protection following damage to the root surface.24‐28 These dynamic features of cementum are

critically involved in orthodontic tooth movement as well as orthodontically induced inflammatory

root resorption, and as such, an overview of its characteristics, development, structure and function

provides a contextual background for root resorption studies.

2.1.1 Characteristics of Cementum

Cementum is pale yellow in appearance with a dull surface. When compared with dentine,

cementum is softer and more permeable24 with a lower elastic modulus,29 which, together with

hardness, is reported to decrease from the cervical to the apical area when measured on premolar

teeth.30 On a respective wet‐weight or volume basis, cementum is composed of 65% or 45%

inorganic hydroxyapatite crystals and amorphous calcium phosphate, 23% or 33% organic Type I

collagen (90%) and Type III collagen (5%) and non‐collagenous proteins (bone sialoprotein and

osteopontin), proteoglycans and glycosoaminoglycans, and 12% or 22% water.26 The hydroxyapatite

crystals are thin and plate‐like, approximately 55nm wide and 8nm thick, with an increased capacity

for absorption of trace elements. 27, 31, 32 Fluoride has been found in relatively high concentrations

(0.9%) in cementum, which increased with age, in association with exposure, and was predominantly

localized in the surface layers with limited diffusion.33 As with the physical properties, the structure



CAROLYN NG 4

and degree of mineralisation of cementum is not uniform throughout the tissue. Although,

cementum has many chemical properties similar to bone; it is avascular, lacks innervation, does not

undergo physiologic resorption or remodelling,25, 34 and is also less readily resorbed.24 Possible

reasons for the reduced susceptibility to resorption when compared with bone may be attributed to:

differences in the properties between bone and cementum, protective features of pre‐cementum, an

increased density of Sharpey’s fibres and the presence of the epithelial cell rests of Malassez (ERM)

on the root surface.24, 27, 35, 36

2.1.2 Development, Structure and Function of Cementum

During the late bell stage of tooth development, when the enamel organ is at its final size

and dentine formation reaches the cervix of the tooth, the internal and external enamel epithelia

converge and proliferate together as a double layered sheet, known as Hertwig’s Epithelial Root

Sheath (HERS), to map out the shape of the tooth root/s.37 The formation of cementum is temporally

and spatially related to root dentine formation as it is restricted to a narrow band encircling the

forming root, 200‐300nm coronal to the advancing root edge, and continues apically as the root

elongates.26 Due to a process of reciprocal epithelial‐mesenchymal interactions, HERS induces the

peripheral cells of the dental papilla to differentiate and begin formation of radicular mantle dentine.

Before mineralization of this pre‐dentine matrix reaches the lining of the inner epithelial cells, HERS

disintegrates into isolated bundles of cells surrounded by a basement membrane, known as epithelial

cell rests of Malassez (ERM), and allows fibroblast‐like cells of the adjacent dental follicle to contact

the unmineralised pre‐dentine matrix. These follicular ectomesenchymal cells receive a reciprocal

inductive signal from the dentine and/or the surrounding HERS cells and differentiate into

cementoblasts. HERS cells have also been implicated in contributing to the differentiation of

cementoblasts.38 Following differentiation, cementoblasts produce a cementum matrix, and implant

collagen fibrils (1‐2um in diameter) into the predentine, enabling an intimate interdigitation of

collagen fibrils at the dentinocemental junction (DCJ). Once the cementum matrix is established on



CAROLYN NG 5

the root surface, a mineralising front, originating in the root dentine, reaches or just surpasses the

fibrillar DCJ, resulting in mineralisation of the cementum matrix. In this way, mineralisation of the

cementum matrix is not controlled by the cementoblasts but rather the presence of hydroxyapatite

crystals in the adjacent dentine, and possibly as well as the adjacent periodontal fibroblasts that are

rich in alkaline phosphatase.24 Mineralisation proceeds in a slow linear fashion and calcospherites are

not observed in cementum. This initial zone of cementum formation has been described as a

primary acellular intrinsic fibre cementum (AIFC), 24, 27 which is formed slowly with incremental lines

in close proximity, and attains a thickness of approximately 10um. Eventually, with increasing

thickness, collagen fibres of Sharpey from the periodontal ligament become attached to the surface

of the cementum layer and a zone of primary acellular extrinsic fibre cementum (AEFC) is formed.

These Sharpey’s fibre bundles are round or ovoid and are approximately 5‐7um in diameter. This

cementum increases slowly and evenly in thickness at rates of 2‐2.5um per year, attains a thickness

of approximately 15um, and covers the cervical two‐thirds of the root. This period of cementogenesis

has been termed the pre‐functional stage26 as this cementum is formed prior to occlusal loading, and

is characterized by the slow rate of formation and an acellular structure. Sharpey’s fibres in AEFC

fulfil the function of providing attachment of the tooth to the surrounding bone.

Upon eruption of the tooth, and following formation of primary cementum in the cervical

portion of the root, secondary cellular cementum appears in the apical region of the root as well as in

furcation areas of multi‐rooted teeth. It is also found to be present in resorption lacunae.25 This type

of cementum is associated with an increased rate of cementum formation. Large basophilic cells rich

in rough endoplasmic reticulum differentiate from cells in the adjacent dental follicle, and secrete

ground substance and collagen, which forms the intrinsic fibres (1‐2um) of cellular intrinsic fibre

cementum (CIFC).26 These fibres are oriented parallel to the root surface. As with bone, a multipolar

mode of matrix secretion by cementoblasts results in a thin (5um thick) layer of unmineralised

cementum at the surface; and cementoblasts become incorporated into the forming matrix, as

cementocytes, which necessitates the generation of new cementoblasts from stem cells within the



CAROLYN NG 6

PDL. Mineralisation of the deep layers of precementum occurs in a linear manner, however, this

cellular cementum is overall less mineralised than primary cementum. CIFC has an adaptive and

reparative function with no role in tooth attachment.27

In some regions of the root AEFC and CIFC may be present in alternating layers, resulting in

variations in the amount of PDL attachment to the tooth. This type of cementum has been termed

cellular mixed stratified cementum (CMSC). In some cases, regions of AIFC may also be found in

these areas of CMSC.39 This type of cementum has been implicated in adaptation and repair.

A type of afibrillar acellular cementum (AAC) that is sparsely distributed and consists of well

mineralised ground substance may be seen on cervical enamel or intervening between fibrillar

cementum and dentine. This type of cementum usually forms when the reduced enamel epithelium

overlying the enamel on an unerupted tooth is damaged or lost, allowing adjacent connective tissue

cells of the dental follicle to contact the enamel surface and become induced into differentiating into

cementoblasts. 24, 27



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The complex structure of cementum is summarised in table 1, which demonstrates the

variable nature in fibre origin , distribution and function.

Table 1:

Characteristics of Cementum.25, 27

CHARACTERISTICS OF CEMENTUM

Type Fibre Origin Distribution Function

Acellular (Primary)

AIFC Intrinsic

Cervical margin to apical third in

unerupted teeth or inner 10um AEFC of

erupted teeth

Attaches Cementum to Dentine

Acellular (Primary)

AEFC

Extrinsic Sharpey’s Fibres

(with some intrinsic fibres initially)

Cervical margin to apical third

Attaches PDL to tooth for anchorage to the alveolar bone

Cellular (Secondary)

CIFC (+ AIFC) Intrinsic

Middle to apical third, furcations and resorption lacunae

Adaptation and Repair

Mixed (Alternating

AEFC + CIFC/AIFC Intrinsic + Extrinsic

Apical portion and furcations

Adaptation

Acellular Afibrillar

AAC ‐

Spurs and patches over enamel and

dentine None



CAROLYN NG 8

2.2 Orthodontically Induced Inflammatory Root Resorption

2.2.1 History & Definition

Root resorption may be classified as either physiological or pathological. In the permanent

dentition, physiologic root resorption is usually a result of physiological changes that occur over time,

whereas, pathological root resorption usually results from trauma, disease or iatrogenic causes.27

Reports on pathologic root resorption of permanent teeth began in 1856 by Bates,40 and its

association with orthodontic treatment was established in 1914 by Ottolengui,19 with major concerns

reported in a radiographic investigation in 1927 by Ketcham.41 In a literature review by Becks and

Marshall42 in 1932, it was concluded that the destruction and uptake of formed tissues by the blood

or lymph system in medical or dental literature should be termed resorption, as opposed to

absorption, which by its derivation, means to “absorb again.”43

The term Orthodontically Induced Inflammatory Root Resorption was introduced in 2002 by

Brezniak and Wasserstein44 to describe a transient inflammatory45, 46 external surface resorption,46, 47

which is an iatrogenic44 and unavoidable pathological consequence1, 48 of orthodontic tooth

movement. More recently, a new classification has been proposed that encompasses the term

Orthodontically Induced Inflammatory Root Resorption under the title of Orthodontitis, which

describes an aseptic local inflammation in the PDL produced by orthodontic forces.2



CAROLYN NG 9

2.2.3 Incidence & Prevalence

As explained by Harris,49 the reported frequency of OIIRR is variable in the literature and

largely results from the diverse and poorly defined criteria used to identify resorption. This

subsequently results in an unreliable prediction of the prevalence of OIIRR when the findings are

applied to a general population. However, a recent systematic review by Weltman50 summarises that

the incidence of OIIRR reported histologically is greater than 90% in orthodontically treated teeth,51,

52 while radiographically it has been reported as 15% before treatment and 73% after treatment.6

The average amount of OIIRR detected radiographically is less than 2.5mm,5, 8, 53‐55 varying from 6% to

13% for different teeth.56 When graded scales are used, OIIRR is usually classified as minor or

moderate in most orthodontic patients.10‐13 Severe resorption, exceeding 4mm or a third of the

original root length is reported to be seen in 1% to 5% of teeth.6, 8, 10‐12, 14‐16

2.2.4 Classification, Grading and Diagnosis

Histologically, there are three degrees of severity of OIIRR as defined by Brezniak and

Wasserstein:1

1. Cemental or surface resorption with remodelling: outer cemental layers are resorbed

and are fully regenerated or remodelled, a process resembling trabecular bone

remodelling.

2. Dentinal resorption with repair (deep resorption): Cementum and the outer layers of

dentine are resorbed and repaired with cementum material. The final shape of the root

may or may not be identical to the original form.

3. Circumferential apical root resorption. Full irreversible resorption of the hard tissue

components of the root apex with root shortening. Repair occurs only within the

cemental layers.



CAROLYN NG 10

Radiographically, Malmgren9 compared pre‐ and post‐ orthodontic treatment radiographs

and registered root resorption lesions with index scores based on a four point scale as shown in

Figure 1. Using this index teeth with root resorption may be classified in levels ranging from 1 to 4.

Figure 1: Root resorption index for quantitative assessment of root resorption. 9

‐ Grade 1: Irregular root contour

‐ Grade 2: Less than 2mm of apical root resorption

‐ Grade 3: Root resorption amounting to from 2mm to one third of the original root length

‐ Grade 4: Root resorption exceeding one third of the original root length



CAROLYN NG 11

A clinical diagnosis of OIIRR is currently achieved with radiographs. It is often desirable to

screen for root resorption from routine orthodontic radiographic records (orthopantomogram and

lateral cephalogram) and supplement findings with periapical films of selected teeth. The

advantages and disadvantages of various radiographic methods for diagnosis of OIIRR are explained

in table 2.

CLINICAL METHODS FOR DIAGNOSIS OF OIIRR

Method Advantages Disadvantages

Orthopantomogram (OPG)

Low radiation dose when compared to full mouth PA

series.57

Magnification and improper patient positioning within the focal trough may result in exaggeration by 20%

when pre and post OPG are used. 58‐60 Maxillary anterior teeth outside the focal trough are likely to appear

short.57

Peri‐apical Films (PA)

Lowest radiation exposure when used selectively. Less distortion and

superimposition errors58 particularly when parallel techniques are used.57

Lateral Cephalogram (LC)

Useful for upper incisors.57 Overlapping roots obscures diagnosis Risk of 5‐12° enlargement factor.57

Cone Beam Computed Tomography (CBCT)

High detection and quantification.61‐63

More costly and higher levels of radiation when used routinely.58

Table 2: Clinical Methods for Diagnosis of OIIRR.



CAROLYN NG 12

The recent classification of Orthodontitis has the following categories which are used to

describe OIIRR:2

Instrumental Orthodontitis (IO): This category describes controlled bone modelling as well

as bone and reversible cemental remodelling which occurs during orthodontic tooth movement.

Instrumental and Detrimental Orthodontitis Grade 1 (IDO1): This category describes the

changes in the effect on cementum from a remodeling process to a modeling process, whereby

resorption progresses into the dentine with irreversible minor to moderate root shortening and

scattered lacunae on the root surfaces.

Instrumental and Detrimental Orthodontitis Grade 2 (IDO2): This category describes the

progression of OIIRR resulting in tooth mobility, sensitivity and severe root shortening in radiographs.

The consequences of IDO2 require treatment, which depends on the stage of identification and

severity. Treatment may vary from fixed retention/splinting affected teeth with unaffected teeth, to

extractions and implant replacement, in extremely rare cases.

2.2.5 Biochemical Assays

Recent research has focussed on identifying biologic markers in saliva, gingival crevicular

fluid, blood serum and urine, and relating these factors to the risk of OIIRR. If successful, these

techniques could be easily implemented in identifying at risk patients prior or during orthodontic

treatment and allow treatment to be modified accordingly.

2.2.5.1 Saliva

In saliva, an increase in the cytokines: interleukin‐7, interleukin‐10, interleukin‐12p70 and

interferon gamma, as well as a decrease in interleukin‐4 has been identified in patients with

moderate to severe OIIRR.64



CAROLYN NG 13

2.2.5.2 Gingival Crevicular Fluid

Elevated levels of dentine phosphoproteins has been reported in the gingival crevicular fluid

of exfoliating primary teeth and teeth undergoing orthodontic treatment when compared with the

GCF of untreated permanent teeth.65 An increase in dentine phosphophoryn and dentine sialoprotein

concentration has also be identified in the GCF of severe root resorption patients, which promotes

the use of dentine phosphophoryn and dentine sialoprotein as biologic markers for identifying at risk

patients, and monitoring root resorption during orthodontic treatment.66 Matrix proteins and

cytokines have also been confirmed in GCF of patients with OIIRR, along with an increased receptor

activator of nuclear factor kappa B ligand (RANKL) to osteoprotegerin (OPG) ratio, reflecting an

increase in bone resorption activity. 67 Studies are currently being undertaken to investigate changes

in the cytokine profile of GCF after application of heavy orthodontic forces and compare the cytokine

profile between patients showing high and low volumes of OIIRR. Preliminary results indicate that

higher levels of anti‐resorptive cytokines IL‐4 and GM‐CSF in low root resorption cases may indicate a

role in reducing the level of OIIRR.68

2.2.5.3 Urinary Excretion Products

Currently, research is being undertaken to profile the protein composition (proteome) of

root dentine in search for useful biomarkers for OIIRR.69 Dentine proteins are resolved by gel

electrophoresis and bands of interest identified by mass spectrometry. From this, several dentine‐

specific proteins have been proposed as biomarkers for OIIRR (e.g. dentine phosphoprotein and

related breakdown products), which are currently being investigated for excretion in urine during

physiologic root loss during the transitional dentition, in the eventual hope of identifying real time

OIIRR in susceptible patients.70

2.2.5.4 Serum

Elevated levels of salivary sIgA in serum before treatment have been associated with more

severe root resorption after 6months of treatment.71 Several studies have demonstrated the role of



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osteoprotegerin and receptor activator of nuclear factor kappa B ligand in osteoclastogenesis,72, 73

while other studies have explored the possibility of their role in OIIRR.74, 75 Subsequently, several

authors are investigating the levels of RANKL and OPG in serum and GCF to determine a possible link

between the relative concentrations of these biomarkers and OIIRR.76, 77

2.2.6 Aetiology

The precise aetiology of OIIRR is unknown and at this stage, appears to be multifactorial. The

literature has identified multiple risk factors that can be grouped into biological or mechanical

factors. Mechanical factors are of particular interest to clinicians as they may be controlled to reduce

the risk of OIIRR.

2.2.6.1 Biologic Risk Factors

Biologic risk factors associated with OIIRR are directly related to the patient and are not

associated with mechanical aspects of orthodontic treatment. They may be further divided into a

genetic or environmental origin.

2.2.6.1.1 Genetic Factors

Individual susceptibility, heritable genetic factors and ethnicity are the main intrinsic genetic

factors that have been linked with OIIRR. Both gender,5, 56, 78‐81 and age at the start of treatment18, 44,

81‐88 have generally been found to have little correlation with OIIRR.

Individual susceptibility to root resorption is an important factor in determining the risk of

root resorption.89 During compression of the PDL, within the microenvironment of the periodontal

ligament, an individual’s tendency for root resorption may be a result of individual disturbances or

peculiarities in the complex relationship between an individual’s hormones, body type and metabolic

rate, which modifies an individual’s cellular metabolism and hence an individual’s reaction to disease,

trauma or aging.90 OIIRR varies among individuals and within the same individual at various times, 22



CAROLYN NG 15

with some individuals demonstrating severe resorption even in the absence of orthodontic

treatment.89, 91

Identification of familial or genetic predispositions to OIIRR may enable clinicians to

accurately counsel patients about their individual risk and manage those at risk by altering their

treatment as needed. Since Newman in 1975, many studies have attempted to identify genetic

causes of OIIRR.92‐98 In a study of 103 sibling pairs, the reported heritability for resorption of maxillary

incisor roots and mandibular first molars was 70%.95 In a sample of 16 monozygotic and 10 dizygotic

twin pairs, a concordance estimate for OIIRR was found to be 49.2% in monozygotic twins and 28.3%

in dizygotic twins.93 More recently, studies have investigated the following two pathways by which

genetic factors may influence OIIRR: 1) Activation control of osteoclasts through the ATP/P2XR7/IL‐

1B inflammation modulation pathway and 2) RANK/RANKL/OPG osteoclast activation control

pathway.98 The TNFRSF11A gene, which encodes for receptor activator of nuclear factor‐kappa B

(RANK) and allele 1 at the IL‐1B gene, which decreases production of cytokine IL‐1 in‐vivo, have been

identified to play a role in increasing the risk of OIIRR.94, 96

In the United States, patients of Asian descent have been reported to exhibit less root

resorption than patients of Caucasian or Hispanic descent, 5 while no differences in resorption were

detected between patients from the Netherlands, United States or Kuwait.99

2.2.6.1.2 Environmental Factors

2.2.6.1.2.1 Systemic

Systemic environmental factors considered in the risk of OIIRR include: asthma and allergies,

endocrine and hormonal imbalances, nutrition, medications and alcohol consumption.

A higher incidence of OIIRR in maxillary molars has been reported in both patients 12 and

animals100 with asthma and allergies.101‐103 It has been proposed that the increased presence of

inflammatory mediators in the maxillary sinus penetrate the periodontal ligament of adjacent teeth



CAROLYN NG 16

and act synergistically to increase the OIIRR process, resulting in root blunting of maxillary molars.12,

44

Endocrine and hormonal imbalances found in hypothyroidism, hyperparathyroidism, Paget’s

disease and other metabolic disorders have been associated with altered resistance to root

resorption. 8, 104‐106 Some animal studies report that OIIRR appears to be increased in conditions with

increased bone turnover rate, e.g. hyperparathyroidism106 and osteoporosis.107 Conversely, in an

alternate rat model the risk of OIIRR has also been suggested to increase in subjects with decreased

bone turnover rate, e.g. hypothyroidism.108

There are conflicting reports in the literature regarding nutritional deficiencies and the risk of

OIIRR. Some authors have reported that calcium and vitamin D deficiency in rats has been associated

with increased parathyroid hormone and osteoclast levels and more severe OIIRR, 42, 106 while other

authors have reported that secondary hyperparathyroidism was correlated with increased bone

turnover and less OIIRR,109 and the marked variation in resorption levels in teeth of the same

individual throws doubt on the role of diet or hormone balance as a primary cause of OIIRR.8

The effect of a number of pharmacologic agents on OIIRR have been investigated in the

literature. Non‐Steroidal Anti‐Inflammatory Drugs (NSAIDs) 110‐112 and supplementation with

hormone L‐thyroxin in rats113 and humans114 has been associated with reduced OIIRR. Conversely,

corticosteroids have been associated with an increased risk of OIIRR1 particularly with short term

use, and careful monitoring of patients undergoing acute corticosteroid treatment, particularly in the

management of asthma or allergies, has been suggested.115 Bisphosphonates have also been found

to increase the vulnerability of the root surface to OIIRR,116, 117 while chronic alcohol consumption

during treatment has been found to increase root resorption through vitamin D hydroxylation in the

liver and altered calcium homeostasis.100, 118



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2.2.6.1.2.2 Local

The following localised factors have been investigated as possible aetiological factors for

OIIRR: habits, pre‐existing resorption, previous trauma, dental morphologies/anomalies or agenesis,

endodontic treatment, periodontal status, alveolar bone density and turnover rate, dental age and

developmental stage and malocclusion.

Nail biting habits91, 92, 119, finger sucking habits beyond the age of seven years53 and tongue

thrust82, 92 have been associated with an increased risk of OIIRR. When treatment was delayed until

after adverse habits were discontinued, no increased OIIRR was found during treatment.8

Pre‐existing resorption has been reported as a clear indicator of increased risk of severe

OIIRR during treatment.9, 86, 91, 92

Previous trauma may be a predictive of an increased risk of OIIRR.8, 53, 120 It has been

reported that the distribution of root resorption in patients with only a history of trauma was 6.7%,

while those with a history of orthodontic treatment was 7.8%, and those with orthodontic treatment

and a history of trauma was almost four times higher, at 27.8%.121 Traumatized teeth that exhibit

signs of resorption prior to treatment tend to undergo more resorption during orthodontic

treatment than teeth without such signs,9 and the extent of external root resorption following

trauma is related to the severity of the injury.122 Damage to the periodontal ligament or cementum

during traumatic injuries may be responsible for the increased risk of OIIRR.9, 46

Abnormal root morphology and length, dental anomalies, agenesis and ectopia have been

reported to be associated with increased OIIRR.5, 10, 54, 92, 99, 123‐126 Features of abnormal root

morphology include pipette‐shape, thin, pointed, dilacerated, blunt or bottle‐shaped, while features

of dental anomalies include invagination of incisors, peg shaped lateral incisors or taurodontism. The

increased risk of OIIRR may be associated with greater forces being applied to the roots during

orthodontic treatment.10, 127 Interestingly, these findings of increased OIIRR are not consistent

throughout the literature.13, 128, 129



CAROLYN NG 18

Endodontic treatment has been reported to be both a preventive factor for OIIRR 54, 130 as

well as a causative factor for OIIRR, although this finding may be confounded by a history of trauma

that was found in the majority of cases analysed.131 It has been proposed that an increased density

and hardness of the dentine in endodontically treated teeth is responsible for resistance against

OIIRR.17, 132

Both periodontal disease 102 and a hypofunctional periodontium133‐135 have been associated

with increased risk of OIIRR. Concomitant inflammation in a diseased periodontium is expected to

reinforce the inflammatory process associated with OIIRR during tooth movement. In the absence of

occlusal function, the periodontium exhibits progressive atrophic changes in all functional structures,

such as the functional arrangement of Sharpey’s Fibres, fibroblastic proliferation, vascularity, and

distribution of Ruffini’s nerve endings and proteoglycans. Accelerated root destruction has been

proposed to result from the narrow periodontal space and derangement of the functional fibres

providing an inadequate cushioning effect and stress distribution, resulting in increased

concentration of compression zones. Interestingly, a study in rats found that although root size and

PDL structure may be reduced due to disuse atrophy resulting from defective occlusal function, they

may be recovered following re‐establishment of occlusal stimuli.135

It has been reported that increased bone turnover108 and decreased bone density90, 109, 132, 136

may allow faster remodelling of bone and less remodelling of root tissue and consequently less

OIIRR. It has been suggested that in patients where decreased bone turnover rates are expected,

reactivation of appliance forces should be performed less frequently and the risk of OIIRR carefully

evaluated.108 However, the radiographic bone density and morphology of the dentoalveolar complex

have been reported to have little correlation to OIIRR.137

Teeth with incomplete root formation at the onset of orthodontic treatment have been

reported to have a higher protection or resistance against OIIRR when compared to teeth with

completed root formation,8, 84, 138, 139 a finding which favours early orthodontic treatment. However,



CAROLYN NG 19

application of these findings should be tempered by the incidence of root dilaceration caused by

orthodontic treatment, reported at 8%. 139

Although no malocclusion is immune to OIIRR1 certain types of malocclusion have been

reported to have a higher prevalence of root resorption. Class III patients were found to have a

higher prevalence of root resorption, which may be related to forward tipping of maxillary incisors

with root apices against the lingual cortical plate during dentoalveolar compensation of a Class III jaw

relationship.140 Class II Division 1 patients were found to have increased OIIRR when compared to

Class I patients, however it was unrelated to the degree of tooth movement or treatment time.141

Malocclusions that require extractions have also been found to have greater resorption than those

that do not require extractions.5 Open‐bite cases have recently been reported to have more teeth

with abnormal root shape and OIIRR when compared to normal overbite cases.134 Deep bite cases

were reported to have greater incisor and maxillary first molar distal root OIIRR.81 Importantly, the

amount of OIIRR is positively associated with the amount of orthodontic tooth movement, which is a

function of the severity of the malocclusion. 86, 94, 142

2.2.6.2 Mechanical Risk Factors

Orthodontic tooth movement has been reported to account for approximately 10 to 30% of

the total variation in OIIRR.

2.2.6.2.1 Force Magnitude

The severity of OIIRR is directionally proportional to the magnitude of the applied force. 48, 52,

143‐148 Numerous three‐dimensional quantitative studies on human maxillary first premolars have

demonstrated an increased amount of OIIRR with increased force levels,149‐152 and in a rigorous

systematic review of the literature, Weltman in 2010 concluded that heavy force application

produced significantly more OIIRR than light force application or control groups.50 Heavy forces that

induce excessive hyalinisation interferes with the repair of root resorption craters, resulting in an

increased prevalence of OIIRR. 48, 51, 90, 136, 144 Two histologic studies have failed to detect a significant



CAROLYN NG 20

difference in the frequency or severity of OIIRR between light and heavy forces, however these

findings were attributed to large individual variations in the subject sample and may hence be

related to the employed methodology. 50, 153, 154

2.2.6.2.2 Treatment Duration

The severity of OIIRR is directly related to treatment duration, thus the longer the force

application the more severe the OIIRR.22, 46, 48, 155 Paetyangkul et al152 reported a statistically

significant increase in the amount of OIIRR in heavy force groups (225g) between 4, 8 and 12 weeks

and, as well as in light force groups (25g) at 12 weeks when compared to 4 and 8 weeks of force

application. Artun et al156 reported the risk of one or more teeth undergoing more than 1.0mm of

OIIRR from 6 to 12months of treatment is 3.8 times higher than that in the first 6months of

treatment. At 3‐9months after initiation of fixed appliance treatment, Smale et al99 reported

approximately 4% of patients had an average OIIRR of ≥1.5mm in maxillary incisors and 15.5% had

more than one maxillary incisor with OIIRR ≥2mm. Levander and Malmgren10 reported 35% of teeth

showed OIIRR after 6‐9months of treatment, which later increased to 56% at 19months of treatment.

In the management of Class II malocclusions, Brin et al13 reported a greater proportion of incisors

with moderate‐severe OIIRR in one‐phase treatment when compared with two‐phase treatment.

2.2.6.2.3 Appliances and Treatment Philosophy

Some studies have reported differences in OIIRR between different orthodontic appliances.

The Begg appliance has been reported to have more OIIRR than edgewise appliances, which may be

attributed to excessive palatal root uprighting in stage three of the Begg technique.157 Bioefficient

therapy, utilizing heat activated and superelastic wires, a different bracket design and smaller

rectangular stainless steel wires during incisor retraction and finishing, has been reported to have

less OIIRR when compared with standard and straight‐wire edgewise systems.11 When serial

panoramic radiographs were used to compare the effects of a preadjusted edgewise appliance, the

Speed appliance and the Tip‐Edge appliance in 114 extraction and non‐extraction cases, statistically



CAROLYN NG 21

significant OIIRR was detected on the following teeth treated with: the preadjusted appliance: 12, 11,

21 and 26 (0.76‐1.68mm); the Speed appliance: 26, 31, 41, 42 (1.11‐2.35mm); and the Tip‐Edge

appliance: 31 (1.12mm).158 However, many studies have also found no statistical difference among

various orthodontic appliances and bracket systems (Tweed, Begg, edgewise and self‐ligating,

sectional and continuous mechanics),56, 81, 142, 159 which may be attributed to individual variation and

difficulties in applying split‐mouth study designs as malocclusions are often asymmetrical.48

Removable appliances are generally considered less detrimental than fixed appliances in

causing OIIRR8, 53 due to the intermittent pattern of force application.48 Barbagallo et al160 found the

degree of OIIRR from clear sequential thermoplastic aligners was comparable to light buccally

directed forces of 25g, however heavy 225g forces induced twice as much OIIRR.

Some authors have reported greater OIIRR in extraction treatment,155, 157 with up to 3.72

times increased incidence of OIIRR.157 These findings should be applied with caution as emphasis

should be placed on the amount of tooth displacement required rather than the decision to extract.48

Extractions to resolve an increased overjet may require more maxillary incisor displacement than

extractions to resolve severe crowding, resulting in increased treatment duration and increased

OIIRR.155, 161‐165

The effect of ultrasound and vibration on OIIRR has been investigated. Low Intensity Pulsed

Ultrasound (LIPUS) has been reported to enhance repair of OIIRR lesions associated with continuous

orthodontic force resulting in lower resorption areas and craters.166 A buccally directed vibration of

113Hz applied for 10min per day has been found to result in 33% less OIIRR volumes, which may play

a role in prevention or repair of OIIRR.167

Rapid maxillary expansion appliances have been associated with increased OIIRR on anchor

teeth, studied by scanning electron microscopy after extraction, particularly on the buccal

surfaces.168 However, no differences are detectable in periapical films when rapid and slow

expansion appliances are compared. 155



CAROLYN NG 22

2.2.6.2.4 Distance, Type and Direction of Tooth Movement

The distance, type and direction of tooth movement are important mechanical factors

affecting the incidence and distribution of OIIRR.

The severity of OIIRR has been shown to be positively related to the distance of tooth

movement, with maxillary incisors, having the highest risk of OIIRR, moving the greatest distance. 155,

161, 162, 169, 170

Teeth may be moved by rotation, tipping of the crown, torqueing of the root or bodily

translation through the bone. Heavy rotational forces produce predictably more OIIRR than light

rotational forces, with concentration of lesions at the buccodistal and linguomesial surfaces171 or

regions corresponding to prominent zones of the roots.172 A greater angle of crown tipping (15°)

produces more OIIRR than a smaller angle of crown tip (2.5°)173 with a greater concentration of

lesions at the buccal‐cervical region and lingual apical region when a buccally directed force is

applied. 152, 160, 174 When buccal root torque was applied to maxillary first premolars, there was no

difference detected in the total root resorption volumes between a small angle (2.5°) and a large

angle (15°), while concentration of the lesions occurred at the buccoapical, mid‐buccal and

palatocervical regions.175 Labial root torque on a maxillary incisor root apex has been reported to

produce 12.7% apical OIIRR annually.176 Bodily tooth movement has been reported to have no

discernible influence on OIIRR.142 A recent rat study reported that OIIRR was more pronounced in

teeth undergoing tipping movements as opposed to bodily tooth movement, and although the

amount of tooth movement decreased when extremely heavy forces were applied, OIIRR increased

in both tipping and bodily tooth movement groups. 177

The direction of tooth movement may be either intrusive or extrusive in nature. Intrusive

forces have been reported to elicit an increased incidence of OIIRR, with light (25g) and heavy (225g)

force groups producing approximately 11 and 68 times greater OIIRR volumes than control groups



CAROLYN NG 23

(0g) respectively, and a significant concentration of lesions at the mesio‐apical and distoapical

regions.150 Clinically, utility arches have been reported to result in 1.84mm of root shortening for

maxillary incisors and 0.61mm for mandibular incisors with no significant correlation between

resorption and the amount of intrusion.126 Following marginal bone loss, the amount of OIIRR after

intrusion has been reported to vary between 1 to 3mm.178 Conversely, heavy extrusive forces have

been reported to produce greater OIIRR than light extrusive forces with the distal surfaces of the

roots more affected than other surfaces.151 However, extrusive forces have also been reported to

produce less OIIRR than intrusive forces.179

Jiggling forces have generally been accepted to be responsible for OIIRR.180, 181 Jiggling was

first described by Oppenheim20 and defined as “small intermittent movements along the tooth axis

originating from biting forces when antagonizing teeth oppose extrusive forces,”20, 21 or a tooth

oscillating along a line of movement.145 Jiggling forces are thought to be produced during

orthodontic treatment when there are occlusal interferences,8, 20 when deformation of light

archwires occurs during function with concomitant use of intermaxillary elastics,8 and following

dental relapse that occurs after removal of palatal expanders.145 Restorative build‐ups on first

premolars, used to increase the vertical dimension by 2 mm for 4 weeks, have been found to have

increased OIIRR during the active bite‐increase period, which may be due to the premature contacts

that transmit excessive uncontrolled vertical forces.182 Two animal studies have investigated the

effects of jiggling on OIIRR. Kim and Son (1994) found no histological or radiographic difference in the

pattern of OIIRR in a feline model when alternating mesial and distal forces were applied in 3 day

cycles over 6, 12, 18 and 24 days when compared to unidirectional mesial forces; 183 while Matsuda

et al found that weekly cycles of alternating buccal and lingual jiggling forces produced more OIIRR in

Wistar rats than two or four weekly cycles, which continued to increase as the duration of applied

jiggling forces lengthened.184 Interestingly, Baumrind (1996) also advised, “resorption in the absence

of overt root displacement seems… consistent with the purported role of “jiggling” during orthodontic

treatment.”18



CAROLYN NG 24

More importantly, the literature shows the distribution of OIIRR lesions reflects the location

of pressure zones on the periodontium. Rudolph et al185 demonstrated in a finite element study that

when tipping movements occur, stress concentrations exist at the alveolar crest and root apex,

whereas when bodily tooth movements occur, there is more even distribution along the root surface.

Purely intrusive, extrusive and rotational movements were found to result in stress concentration at

the apex. Furthermore, OIIRR occurs preferentially at the apical region because the variable

orientation of periodontal fibres in this region enables increased stress concentration,186 the acellular

cementum covering the apical third of the root is more friable and prone to injury,18, 80, 186 and the

perpetual challenge of aligning forces through the centre of resistance of a tooth in all three planes

to achieve a true bodily translation, results in undesirable stress concentrations in the apical third of

the tooth.80

2.2.6.2.5 Pattern of Force Application

The pattern of force application may be either continuous or intermittent. The effect of

applying forces continuously or intermittently on OIIRR in the literature is unclear. One view is that

an intermittent pattern of force application allows resorbed cementum to repair with less resultant

OIIRR. 48, 124, 187‐193 The alternate view is that there is no difference in the amount of OIIRR between

intermittent and continuous force applications.194 More importantly, even though continuous forces

cause more OIIRR, they are more efficient at orthodontic tooth movement than intermittent forces.

In the case where intermittent forces are beneficial, various studies have attempted to determine an

appropriate length of pause between force applications, 192, 193 with a regime of 18 days‐on and 3

days‐off scheme producing significantly less OIIRR when compared with a 3‐week continuous force

application, albeit with a slower mean tooth movement rate. 192



CAROLYN NG 25

2.2.7 Pathogenesis

2.2.7.1 Mechanism of resorption: histopathology and biochemical mediators

The process of OIIRR is characterised by the following features:1

1. Application of orthodontic force to the tooth,

2. In areas of high stress concentration, exceeding the capillary blood pressure (20‐25g/cm2),

overcompression of the periodontium occurs with collapse of the local blood supply,195

3. Formation of aseptic necrosis occurs in the periodontal membrane and bone, which has a glass‐

like hyalinised histologic appearance,195‐197

4. An inflammatory process is initiated at the periphery of the hyalinised zone, in adjacent vital

parts of the PDL. The following hormones are involved in orchestrating this initial inflammatory

process via synthesis of signalling molecule prostaglandin E2 (PGE2) and an intracellular “second

messenger” cyclic adenosine monophosphate (cAMP): IL‐1a, IL‐1b and TNF,198

5. At the periphery, viable resident macrophages and fibroblast‐like cells begin phagocytosis of

cellular and connective tissue remnants of the periodontal membrane and precementum, while

mono‐nucleated tartrate resistant acid phosphatase (TRAP) ‐ negative fibroblast‐like cells

continue to remove the necrotic hyaline tissue and surface layers of precementum and

mineralised acellular cementum,199, 200

6. The cementoblast lining and cementoid on the root surface becomes damaged during resorption

of the hyaline zone or as a result of orthodontic pressure, and the underlying mineralized

cementum becomes exposed,199

7. Blood‐borne TRAP‐positive multi‐nucleated giant cells (MNGC) infiltrate and remove the main

part of the necrotic tissue and upon reaching the contaminated and damaged root surface,

continue resorption of the cementum surface.201 Although these MNGCs lack ruffled borders and

have many morphological traits similar to odontoclasts and osteoclasts, and are assumed to be

derived from the mono‐nucleated phagocytic system,201



CAROLYN NG 26

8. It has been suggested that, in areas where the cementum has been partly or fully removed, new

odontoclasts differentiate, appearing as multi‐nucleated TRAP‐positive cells with ruffled borders

and clear zones, as they are found only within root resorption lacunae in contact with resorbed

dentine surfaces.201 The following osteoblast‐derived factors are involved in the differentiation

and activation of osteoclasts: receptor activator of nuclear factor kappa β ligand promotes

osteoclast formation, while osteoprotegerin (OPG) down‐regulates osteoclastogenesis,202 and

may similarly be involved in the regulation of odontoclast activity.203 An increased production of

RANKL, decreased production of OPG and a stimulated osteoclast formation has been detected

in the compressed PDL cells obtained from patients with severe apical root resorption,75 while

increased levels of RANKL and OPG have been detected in rats in the environment of root

resorption following the application of heavy forces,74

9. The inflammatory resorptive process continues until no necrotic tissue is present and/or when

there is relief of compression.204 Resorption of the alveolar bone wall204 as well as resorption

lacunae on the root surface,1 expanding the amount of root surface under compression,

contributes to decompression of the periodontal membrane. As the local stress concentration

abates, stimulation of the inflammatory process is reduced and spontaneous repair of resorption

lacunae in cementum is permitted. 204

2.2.7.2 Resistance and Repair

The precementum and cementoblast lining of the root surface have been recognized as

providing a protective barrier against root resorption204 which may be attributed to potent anti‐

collagenases 35 that inhibit the extracellular removal of the cementoid lining and prevent access and

stimulation of clastic cells by the underlying mineralised tooth structure. Some authors have

explored the role of remodelled cementum in providing additional protective effects when reporting

on findings of patients having less OIIRR following orthodontic retreatment.1 However, it should be



CAROLYN NG 27

noted that patients seeking retreatment in general need less tooth movement to correct the

malocclusion, and these findings of less OIIRR should be evaluated with care. 4

Once the necrotic tissue is cleared and as the local stress concentration reduces,90 below the

limit of systolic capillary blood pressure of 20‐26g/cm3, 205 repair of OIIRR lesions commences.

During this process, cementoblasts rich in rough endoplasmic reticulum and dense bodies indicating

synthesis of fibrillar collagen material, migrate into the lesions206 and begin deposition of acellular

cementum which is later replaced by cellular cementum, 207 and a new periodontal ligament is

established.136, 168, 206, 208 This new PDL is comparable to that found in control specimens.206 Thus the

risk of tooth loss due to OIIRR is not high. 17, 209, 210 Some authors have reported that repair is

initiated from the periphery,206, 211 while others have reported repair initiating from the central zone.

168, 207, 212

Repair of OIIRR lesions has been described in four phases:211

I. Lag Phase: End of resorption and beginning of repair: With dissipation of residual forces

differentiation of cementoblasts occurs.

II. Incipient Phase: 14 days later: a transitional phase between no apposition and active

deposition.

III. Peak phase: 14‐28 days later: Short spurt in matrix formation and incorporation of extrinsic

fibres into the intrinsic cementum matrix.

IV. Steady Deposit phase: 42‐56 days: steady deposition of mixed fibrillar cementum.

Repair of OIIRR lesions has been reported to occur during the application of light forces and

simultaneously with OIIRR continuing in a different zone of a lesion. 204 The onset of repair has been

reported in histological studies of human premolars, to occur as early as the first week of retention,88

and the amount of repair increases with increased time in retention.88, 154, 168 After 5‐6 weeks, the

process slows down and reaches a steady phase with up to 75‐82% of the resorptive areas



CAROLYN NG 28

undergoing repair at 6‐ 8 weeks of retention, with great individual variation in healing potential

reported. 88, 207

After analysing the repair process in a rat model, OIIRR at the end of treatment has been

proposed to result from a series of repetitive resorption and healing cycles throughout the treatment

period, and hence the time span between each orthodontic adjustment may allow healing to

occur.213 Consequently, it has been suggested that frequent reactivation of orthodontic appliances as

well as re‐establishing new or additional mechanical loading before the repair process overcomes the

resorption process, may result in severe root resorption. Longer time intervals between orthodontic

reactivations may enable more healing to take place. For these reasons, when heavy orthodontic

forces are applied, more than 12 weeks between each force application have been recommended.

In terms of the level of force application, Cheng et al214 evaluated cementum repair at 4 and

8 weeks of retention after 4 weeks of continuous light and heavy orthodontic forces and reported

that light orthodontic forces had the least OIIRR crater volume following passive retention.

2.2.8 Prognosis and Prevention, Management

There are no reports of iatrogenic tooth loss as a result of severe OIIRR.215 A reduced root

length subsequent to OIIRR could potentially compromise the longevity of affected teeth by

complicating restorative treatment planning and placing them at greater risk of loss secondary to

periodontal disease or trauma. Fortunately, in the majority of cases, the extent of root loss is mild

and inconsequential to the long term survival and functionality of the affected teeth or dentition. 17,

18 Furthermore, OIIRR does not progress after appliance removal. 8, 17, 210, 216, 217

The most adverse outcome from OIIRR reported in the literature is hypermobility.215 At a

mean follow‐up examination of 14 years, only 1% of teeth examined exhibited apical root resorption

of more than one third the root length and 2% of patients reported hypermobility.17 At long term



CAROLYN NG 29

follow‐up 5‐15 years after active treatment, maxillary incisors with severe OIIRR and remaining root

lengths less than or equal to 9mm are at increased risk of tooth mobility; the risk is less if the

remaining length is >9mm.218 Increasing mobility can be expected with age in teeth with extremely

resorbed roots, while teeth with root length ≥10mm and a healthy periodontium have been reported

to remain stable.219 Root shortening of 0‐3mm has been reported to equate to 0‐1mm of crestal

bone loss, with 4mm of apical root loss translating to 20% loss of total attachment.220 Consequently,

patients that are susceptible to marginal periodontal breakdown may be at higher risk of losing

severely resorbed teeth prematurely. Despite these findings, it is encouraging to note that OIIRR

levels over 50% of the root length has not been found to be adequate reason for extraction and

prosthetic replacement.215



CAROLYN NG 30

The following recommendations have been made for clinically reducing the risk of OIIRR:48

Identify risk factors with a thorough medical and family history, 5, 93

Habit cessation,82, 119

Commencement of treatment when incisors have open apices,84, 136

Efficient treatment planning and mechanics to minimise treatment duration,10, 51, 124, 156

Light forces: especially for intrusion, maxillary incisor palatal torque and premolar de‐

rotation,51, 52, 90, 136

Intermittent forces to allow periods of rest and repair,181, 187, 191

Increased intervals between appointments (repair),136

Avoid sustained jiggling: e.g. intermaxillary elastics,53

Radiographic assessment at 6 months into treatment (or 3 months in high risk individuals)14,

109 and

Enable repair by pausing treatment for up to 3 months if resorption is detected.142

There has been recent interest in the role of fluoride and the prevention of OIIRR. Foo et al

found that fluoride reduces the average volume of root resorption craters in rats.221 Gonzales et al

found that fluoride reduces the depth and roughness of resorption craters in rats exposed to fluoride

in drinking water from birth, suggesting an increased resistance to demineralisation.222 Karadeniz et

al reported patients residing in regions of high fluoride concentration in public water supplies

(>2ppm) have been found to have significantly reduced volume of OIIRR craters when heavy buccal

tipping forces are applied.223 This effect was not significant with light forces. This study indicated

that fluoride may reduce the acidic effect of clastic activity and decreased cementum solubility.



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Interestingly, another study by the same group found that high fluoride intake from public water

supplies did not have a beneficial effect on the severity of OIIRR after 4‐weeks orthodontic force

application and 12 weeks of passive retention.224

The following guidelines has been recommended for managing OIIRR clinically:48

Pause treatment with passive arch wires for 2‐3 months, cease force application for 4‐6

months or in extreme cases terminate treatment124, 155

Reassess treatment objectives to reduce further damage: compromise or terminate early,

Continue radiographic examination until resorption has ceased,44 especially in severe OIIRR

cases. If OIIRR continues to worsen, sequential root canal therapy with calcium hydroxide

may be considered,225

Appropriate counselling and regular review,155

Ensure that final radiographs at take at the time of fixed appliance removal,44

Retention of teeth with severely resorbed roots should be carefully considered to avoid

adverse occlusal trauma that may exacerbate the root resorption.44

2.3 Research Methods for Investigation and Evaluation of OIIRR

2.3.1 Radiography (2D)

Various radiographic techniques have been employed to document the incidence, prevalence

and severity of OIIRR following orthodontic treatment.14, 41, 57, 58, 92, 180, 226, 227 Radiographic techniques

employed include: periapical bisecting or paralleling angle, orthopantomogram, cephalogram and

laminogram films. While these films are useful in recording the amount of root shortening, there are

several limitations, explored previously, relating to: the two dimensional nature of the analysis,

distortion and variable magnification factors.57‐60 Periapical paralleling techniques provide the least



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distortion and superimposition errors when compared with orthopantomograms and lateral

cephalograms.22, 57 Due to these limitations alternate forms of investigation have been employed.

2.3.2 Histologic Analysis (2D)

Histological analysis, by way of hard tissue sectioning, staining and analysis by light

microscopy, are conducted for research purposes where all stages of resorption can be observed.21,

51, 88, 102, 109, 136, 153, 154, 186, 189, 190, 194, 199, 207, 227‐231 This analysis provides only a two‐dimensional analysis

and is limited by the ability to ensure that all craters are accurately identified, isolated, processed

and analysed. Issues relating to variable tooth morphology further complicate preparation of the

samples and accurate isolation of the lesions. Furthermore, samples are destroyed by this process

and no further records of the original structure are maintained for subsequent analysis.

2.3.3 Scanning Electron Microscopy (2D)

In an effort to improve the identification and evaluation of OIIRR lesions, scanning electron

microscopy has been employed, which utilises minimal specimen preparation to provide enhanced

visual assessment of the root surface. 52, 148, 168, 187, 232, 233 234 Despite providing detailed information

about resorption lacunae and the mineralised structure, SEM has been described as a difficult

method of examining root resorption because sputtering of specimens with a carbon coating is

necessary, and the desired image view must be chosen before an image is created;235 furthermore,

parallax errors due to convexity in the tooth surface may manifest, resulting in errors in

measurement.60

To enable 3‐dimensional mapping and volumetric analysis of the craters, stereo SEM imaging

was developed.60, 149, 236 This method involves collection of two SEM images of a lesion to create a

stereopair with a 6‐degree difference in perspective, which is then converted to an 8‐bit greyscale

depth map to enable volumetric analysis of the lesion. Although highly accurate and reproducible,

this technique is still relatively time consuming and technique sensitive.



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2.3.4 X‐ray Micro‐Computed Tomography (3D)

Computed axial tomography uses computer‐processed x‐rays to produce tomographic slices

of a scanned object. X‐ray micro‐computed tomography (XMT) is a high resolution version of

computerized axial tomography enabling analysis in the order of micrometres. Digital geometry

processing is then used to combine a series of tomographic images taken around a single axis of

rotation to generate a three‐dimensional reconstruction of the scanned object.

The resolution of medical computed axial tomography can only be obtained to a fraction of a

millimetre, owing to limitations in radiation exposure. In order to obtain a higher resolution, the

exposure must be increased 10,000‐fold in order to achieve a tenfold improvement in resolution.

With smaller specimen sizes, lower x‐ray energies are required, enabling only 1000‐fold increases in

exposure for a tenfold improvement in resolution. Consequently, in order to obtain imaging on a

micrometre scale, XMT is best suited to small inanimate specimens, and can only be considered a

non‐destructive technique, rather than a non‐invasive technique, as only biopsy specimens are suited

for analysis.237

XMT has been employed in several aspects of dentistry and include: measurement of enamel

thickness and tooth measurement,238‐243 analysis of root canal morphology,244‐256 evaluation of root

canal preparation,257‐268 evaluation of craniofacial skeletal structure and development,269‐273 micro

finite element modelling, 274‐279 dental tissue engineering,280‐282 mineral density of dental hard

tissues283‐293 and applications in dental implantology.294‐303

The SkyScan 1172 high resolution commercial laboratory (absorption) XMT system (SkyScan,

Aartselaar, Belgium) is a cone beam system that is suited to specimen sizes with a diameter up

to 16mm and enables reconstruction sizes of <1um, 2um, 5 or 8um.304 Following scanning,

SkyScan Nrecon package (Version 1.4.2; SkyScan, Aartselaar, Belgium) is used to reconstruct

cross‐section images from tomography projection images utilizing the Feldkamp algorithm.305



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The reconstructed cross‐section images may then be imported into a variety of 3D

reconstruction and visualisation software packages for volumetric analysis and imaging. The

following findings have been reported from human studies utilizing XMT with the SkyScan 1172

system to investigate OIIRR:

1. The mean volumes of OIIRR craters in light (25g) and heavy (225g) force groups were

approximately 11 and 68 times greater than in control groups respectively and the mesial and

distal surfaces had the greatest resorption volumes.150

2. OIIRR sites were significantly increased in groups receiving orthodontic tooth movement, and

fluoride has been found to reduce the size of resorption craters, although the effect is variable

and not statistically significant.221

3. Clear removable thermoplastic aligners have similar effects on root cementum as light (25g)

orthodontic force with fixed appliances.160

4. The volume of OIIRR craters on maxillary and mandibular first premolars induced by buccally

directed forces for 12 weeks was directly proportional to the magnitude of the force, with

maxillary premolars more susceptible to OIIRR than mandibular premolars.152

5. Intermittent forces of 226cN produced less OIIRR than continuous forces of 226cN over an 8

week period, with the buccal‐cervical region having the most lesions.193

6. Unerupted and nonimpacted maxillary third molars exhibited the greatest OIIRR on the mesial

root surface adjacent to erupted second molars. They also exhibited slightly greater cube‐root

volumes of resorption per tooth when compared with erupted first premolars not subjected to

orthodontic forces, and similar cube‐root volumes of resorption per tooth as first premolars

subjected to light (25g) buccal and intrusive orthodontic forces. These findings suggested that

OIIRR may occur as part of hard tissue remodelling and turnover, eruption or transmission of

masticatory forces through the dentition to the alveolar bone.306

7. When used in combination with light microscopy, XMT has been reported to improve the

efficiency and accuracy of histologic techniques.212



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8. The amount of OIIRR in the left and right sides of both jaws was similar when heavy buccal forces

are applied. Thus, it is expected that a split mouth technique may be used with teeth from one

side of the jaw serving as controls.307

9. When comparing 2.5° and 15° of buccal root torque, higher magnitudes of torque can cause

more OIIRR, particularly in the apical region, which is clinical significant because it can adversely

affect the crown‐to‐root ratio.175

10. With high fluoride intake and heavy force application (225g) less OIIRR was found in all root

surfaces and root thirds.223

11. A 15° distal root tip bend causes more OIIRR than a 2.5° distal root tip bend. Greater OIIRR can be

found in areas under pressure compared with areas under tension. 173

12. Heavy rotational forces cause more OIIRR than light rotation forces. Compression areas (buccal –

distal and lingual mesial surfaces in this study) showed significantly higher OIIRR than other areas

at all levels of the root.171

13. Greater OIIRR volumes were observed after heavy (225g) extrusive forces when compared with

light (25g) forces. The distal surfaces of the root were significantly more affected than other root

surfaces and may be influenced by root morphology and initial angulation of the tooth. There

was no significant difference in the amount of OIIRR in the vertical thirds of the root for either

force groups.151

14. Intermittent forces result in less tooth movement and OIIRR than continuous forces. With

intermittent forces, when a pause is given, OIIRR decreases irrespective of the timing of

reactivation. With continuous forces, 2 weekly reactivations produced faster tooth movement

with similar OIIRR when compared with intermittent forces.192

15. In split‐mouth study of 30 maxillary first premolar teeth, there was no statistical difference

between control teeth and teeth exposed to vibration of 30Hz or 20grams with AcceleDent in

terms of OIIRR volume and distribution, when 150g buccal directed forces are applied.

Furthermore, a regression analysis revealed that patients with a higher level of individual



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susceptibility to OIIRR may potentially benefit more from the use of vibration than those less

susceptible.308

16. In another split‐mouth study of 28 maxillary first premolar teeth, exposure to vibration with 113

Hz and produced 33% less OIIRR than control teeth when exposed to 150g buccally directed

forces.167

17. High fluoride intake from public water supplies did not have a statistically beneficial effect on the

severity of OIIRR after application of 4 weeks orthodontic forces and 12 weeks of passive

retention.224

18. Restorative build‐ups, used to increase the vertical dimension by 2mm over a 4 week period,

caused OIIRR along the sides of the teeth during the active bite increase period. No significant

differences existed in the amount of OIIRR among the different surfaces or regions and there was

no correlation between age, sex, volume of OIIRR and pain.182



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90. Rygh, P., Orthodontic root resorption studied by electron microscopy. Angle Orthodontist, 1977. 47(1): p. 1‐16.

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100. Davidovitch, Z., Godwin, S.L., Park, Y.G., Taverne, A.A.R., Dobeck, J.M., Lilly, C.M. and De Sanctis, G.T., The etiology of root resorption, in Orthodontic Treatment: Management of Unfavorable Sequelae., J.A. McNamara and C.A. Trotman, Editors. 1996, University of Michigan Press: Ann Arbor, MI. p. 93‐117.

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106. Engstrom, C., Granstrom, G. and Thilander, B., Effect of orthodontic force on periodontal tissue metabolism. A histologic and biochemical study in normal and hypocalcemic young rats. American Journal of Orthodontics & Dentofacial Orthopedics, 1988. 93(6): p. 486‐95.

107. Sirisoontorn, I., Hotokezaka, H., Hashimoto, M., Gonzales, C., Luppanapornlarp, S., Darendeliler, M.A. and Yoshida, N., Tooth movement and root resorption; The effect of ovariectomy on orthodontic force application in rats. Angle Orthodontist, 2011. 81(4): p. 570‐577.

108. Verna, C., Dalstra, M. and Melsen, B., Bone turnover rate in rats does not influence root resorption induced by orthodontic treatment. European Journal of Orthodontics, 2003. 25(4): p. 359.

109. Goldie, R.S. and King, G.J., Root resorption and tooth movement in orthodontically treated, calcium‐deficient, and lactating rats. American Journal of Orthodontics, 1984. 85(5): p. 424‐430.

110. Villa, P.A., Oberti, G., Moncada, C.A., Vasseur, O., Jaramillo, A., Tobon, D. and Agudelo, J.A., Pulp‐dentine complex changes and root resorption during intrusive orthodontic tooth movement in patients prescribed nabumetone. Journal of Endodontics, 2005. 31(1): p. 61‐66.

111. Gonzales, C., Hotokezaka, H., Matsuo, K.I., Shibazaki, T., Yozgatian, J.H., Darendeliler, M.A. and Yoshida, N., Effects of steroidal and nonsteroidal drugs on tooth movement and root resorption in the rat molar. Angle Orthodontist, 2009. 79(4): p. 715‐726.

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113. Poumpros, E., Loberg, E. and Engström, C., Thyroid function and root resorption. Angle Orthodontist, 1994. 64(5): p. 389‐93.

114. Loberg, E.L. and Engstrom, C., Thyroid administration to reduce root resorption. Angle Orthodontist, 1994. 64(5): p. 395‐9; discussion 399‐400.

115. Verna, C., Hartig, L.E., Kalia, S. and Melsen, B., Influence of steroid drugs on orthodontically induced root resorption. Orthodontics & Craniofacial Research, 2006. 9(1): p. 57‐62.



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116. Alatli, I. and Hammarstrom, L., Root surface defects in rat molar induced by 1‐hydroxyethylidene‐1,1‐bisphosphonate. Acta Odontologica Scandinavica, 1996. 54(1): p. 59‐65.

117. Alatli, I., Hellsing, E. and Hammarstrom, L., Orthodontically induced root resorption in rat molars after 1‐hydroxyethylidene‐1,1‐bisphosphonate injection. Acta Odontologica Scandinavica, 1996. 54(2): p. 102‐8.

118. Davidovitch, Z., Etiological factors in force‐induced root resorption, in Biological Mechanisms of Tooth Eruption, Resorption, and Replacement by Implants, Z. Davidovitch, Editor 1998, Harvard Society for the Advancement of Orthodontics: Boston, Mass. p. 349‐355.

119. Odenrick, L. and Brattstrom, V., Nailbiting: frequency and association with root resorption during orthodontic treatment. Journal of Orthodontics, 1985. 12(2): p. 78‐81.

120. Brin, I., Ben Bassat, Y., Heling, I. and Brezniak, N., Profile of an orthodontic patient at risk of dental trauma. Dental Traumatology, 2000. 16(3): p. 111‐115.

121. Brin, I., Ben‐Bassat, Y., Heling, I. and Engelberg, A., The influence of orthodontic treatment on previously traumatized permanent incisors. European Journal of Orthodontics, 1991. 13(5): p. 372‐377.

122. Andreasen, J. and Andreasen, F., Root resorption following traumatic dental injuries. Proceedings of the Finnish Dental Society. Suomen Hammaslääkäriseuran toimituksia, 1992. 88: p. 95.

123. Kjaer, I., Morphological characteristics of dentitions developing excessive root resorption during orthodontic treatment. European Journal of Orthodontics, 1995. 17(1): p. 25‐34.

124. Levander, E., Malmgren, O. and Eliasson, S., Evaluation of root resorption in relation to two orthodontic treatment regimes. A clinical experimental study. European Journal of Orthodontics, 1994. 16(3): p. 223.

125. Thongudomporn, U. and Freer, T.J., Anomalous dental morphology and root resorption during orthodontic treatment: a pilot study. Australian Orthodontic Journal, 1998. 15(3): p. 162‐7.

126. McFadden, W.M., Engstrom, C., Engstrom, H. and Anholm, J.M., A study of the relationship between incisor intrusion and root shortening. American Journal of Orthodontics & Dentofacial Orthopedics, 1989. 96(5): p. 390‐6.

127. Oyama, K., Motoyoshi, M., Hirabayashi, M., Hosoi, K. and Shimizu, N., Effects of root morphology on stress distribution at the root apex. European Journal of Orthodontics, 2007. 29(2): p. 113‐7.

128. Lee, R.Y., Artun, J. and Alonzo, T.A., Are dental anomalies risk factors for apical root resorption in orthodontic patients? American Journal of Orthodontics & Dentofacial Orthopedics, 1999. 116(2): p. 187‐95.

129. Kook, Y.A., Park, S. and Sameshima, G.T., Peg‐shaped and small lateral incisors not at higher risk for root resorption. American journal of orthodontics and dentofacial orthopedics, 2003. 123(3): p. 253‐258.

130. Spurrier, S.W., Hall, S.H., Joondeph, D.R., Shapiro, P.A. and Riedel, R.A., A comparison of apical root resorption during orthodontic treatment in endodontically treated and vital teeth. American Journal of Orthodontics & Dentofacial Orthopedics, 1990. 97(2): p. 130‐4.

131. Wickwire, N.A., Mc Neil, M.H., Norton, L.A. and Duell, R.C., The effects of tooth movement upon endodontically treated teeth. Angle Orthodontist, 1974. 44(3): p. 235‐42.



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132. Reitan, K., Biomedical principles and reactions., in Orthodontics: current principals and techniques., R.L. Vanarsdall and T.M. Graber, Editors. 1985, Mosby: St. Louis. p. 101‐92.

133. Sringkarnboriboon, S., Matsumoto, Y. and Soma, K., Root resorption related to hypofunctional periodontium in experimental tooth movement. Journal of Dental Research, 2003. 82(6): p. 486‐90.

134. Motokawa, M., Terao, A., Kaku, M., Kawata, T., Gonzales, C., Darendeliler, M.A. and Tanne, K., Open bite as a risk factor for orthodontic root resorption. European Journal of Orthodontics, 2013. 35(6): p. 790‐795.

135. Motokawa, M., Terao, A., Karadeniz, E.I., Kaku, M., Kawata, T., Matsuda, Y., Gonzales, C., Darendeliler, M.A. and Tanne, K., Effects of long‐term occlusal hypofunction and its recovery on the morphogenesis of molar roots and the periodontium in rats. Angle Orthodontist, 2012. 83(4): p. 597‐604.

136. Reitan, K., Initial tissue behavior during apical root resorption. Angle Orthodontist, 1974. 44(1): p. 68‐82.

137. Otis, L.L., Hong, J.S.H. and Tuncay, O.C., Bone structure effect on root resorption. Orthodontics & Craniofacial Research, 2004. 7(3): p. 165‐177.

138. Rudolph, C.E., An evaluation of root resorption occurring during orthodontic treatment. Journal of Dental Research, 1940. 19(4): p. 367‐71.

139. Rosenberg, H.N., An evaluation of the incidence and amount of apical root resorption and dilaceration occurring in orthodontically treated teeth, having incompletely formed roots at the beginning of Begg treatment. American Journal of Orthodontics, 1972(61): p. 524‐5.

140. Kaley, J. and Phillips, C., Factors related to root resorption in edgewise practice. Angle Orthodontist, 1991. 61(2): p. 125‐32.

141. Taner, T., Ciger, S. and Sencift, Y., Evaluation of apical root resorption following extraction therapy in subjects with Class I and Class II malocclusions. European Journal of Orthodontics, 1999. 21(5): p. 491‐6.

142. Parker, R.J. and Harris, E.F., Directions of orthodontic tooth movements associated with external apical root resorption of the maxillary central incisor. American Journal of Orthodontics & Dentofacial Orthopedics, 1998. 114(6): p. 677‐683.

143. Dellinger, E.L., A histologic and cephalometric investigation of premolar intrusion in the Macaca speciosa monkey. American Journal of Orthodontics, 1967. 53(5): p. 325‐55.

144. King, G. and Fischlschweiger, W., The effect of force magnitude on extractable bone resorptive activity and cemental cratering in orthodontic tooth movement. Journal of Dental Research, 1982. 61(6): p. 775‐79.

145. Vardimon, A., Graber, T., Voss, L. and Lenke, J., Determinants controlling iatrogenic external root resorption and repair during and after palatal expansion. Angle Orthodontist, 1991. 61(2): p. 113‐122.

146. Casa, M.A., Faltin, R.M., Faltin, K., Sander, F.G. and Arana‐Chavez, V.E., Root resorptions in upper first premolars after application of continuous torque moment. Journal of Orofacial Orthopedics/Fortschritte der Kieferorthopädie, 2001. 62(4): p. 285‐295.

147. Darendeliler, M., Kharbanda, O., Chan, E., Srivicharnkul, P., Rex, T., Swain, M., Jones, A. and Petocz, P., Root resorption and its association with alterations in physical properties, mineral contents and resorption craters in human premolars following application of light and heavy controlled orthodontic forces. Orthodontics & Craniofacial Research, 2004. 7(2): p. 79‐97.



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148. Faltin, R.M., Arana‐Chavez, V.E., Faltin, K., Sander, F.G. and Wichelhaus, A., Root resorptions in upper first premolars after application of continuous intrusive forces. Intra‐individual study. Journal of Orofacial Orthopedics, 1998. 59(4): p. 208‐19.

149. Chan, E.K.M., Darendeliler, M.A., Petocz, P. and Jones, A.S., A new method for volumetric measurement of orthodontically induced root resorption craters. European Journal of Oral Sciences, 2004. 112(2): p. 134‐9.

150. Harris, D.A., Jones, A.S. and Darendeliler, M.A., Physical properties of root cementum: part 8. Volumetric analysis of root resorption craters after application of controlled intrusive light and heavy orthodontic forces: a microcomputed tomography scan study. American Journal of Orthodontics & Dentofacial Orthopedics, 2006. 130(5): p. 639‐647.

151. Jiménez Montenegro, V.C., Jones, A., Petocz, P., Gonzales, C. and Darendeliler, M.A., Physical properties of root cementum: Part 22. Root resorption after the application of light and heavy extrusive orthodontic forces: A microcomputed tomography study. American Journal of Orthodontics and Dentofacial Orthopedics, 2012. 141(1): p. e1‐e9.

152. Paetyangkul, A., Turk, T., Elekdag‐Turk, S., Jones, A.S., Petocz, P. and Darendeliler, M.A., Physical properties of root cementum: part 14. The amount of root resorption after force application for 12 weeks on maxillary and mandibular premolars: a microcomputed‐tomography study. American Journal of Orthodontics & Dentofacial Orthopedics, 2009. 136(4): p. 492.e1‐9; discussion 492‐3.

153. Owman‐Moll, P., Kurol, J. and Lundgren, D., Effects of a doubled orthodontic force magnitude on tooth movement and root resorptions. An inter‐individual study in adolescents. European Journal of Orthodontics, 1996. 18(1): p. 141.

154. Owman‐Moll, P., Kurol, J. and Lundgren, D., The effects of a four‐fold increased orthodontic force magnitude on tooth movement and root resorptions. An intra‐individual study in adolescents. European Journal of Orthodontics, 1996. 18(3): p. 287‐94.

155. Sameshima, G.T. and Sinclair, P.M., Predicting and preventing root resorption: Part II. Treatment factors. American Journal of Orthodontics & Dentofacial Orthopedics, 2001. 119(5): p. 511‐515.

156. Artun, J., Smale, I., Behbehani, F., Doppel, D., Hof, M. and Kuijpers‐Jagtman, A., Apical root resorption six and 12 months after initiation of fixed orthodontic appliance therapy. Angle Orthodontist, 2005. 75(6): p. 919.

157. McNab, S., Battistutta, D., Taverne, A. and Symons, A.L., External apical root resorption following orthodontic treatment. Angle Orthodontist, 2000. 70(3): p. 227‐32.

158. Armstrong, D., Kharbanda, O.P., Petocz, P. and Darendeliler, M.A., Root resorption after orthodontic treatment. Australian Orthodontic Journal, 2006. 22(2): p. 153‐160.

159. Alexander, S.A., Levels of root resorption associated with continuous arch and sectional arch mechanics. American Journal of Orthodontics & Dentofacial Orthopedics, 1996. 110(3): p. 321‐4.

160. Barbagallo, L.J., Jones, A.S., Petocz, P. and Darendeliler, M.A., Physical properties of root cementum: Part 10. Comparison of the effects of invisible removable thermoplastic appliances with light and heavy orthodontic forces on premolar cementum. A microcomputed‐tomography study. American Journal of Orthodontics & Dentofacial Orthopedics, 2008. 133(2): p. 218‐27.

161. Hollender, L., Ronnerman, A. and Thilander, B., Root resorption, marginal bone support and clinical crown length in orthodontically treated patients. European Journal of Orthodontics, 1980. 2(4): p. 197‐205.



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162. Sharpe, W., Reed, B., Subtelny, J.D. and Polson, A., Orthodontic relapse, apical root resorption, and crestal alveolar bone levels. American Journal of Orthodontics & Dentofacial Orthopedics, 1987. 91(3): p. 252‐8.

163. Kennedy, D.B., Joondeph, D.R., Osterberg, S.K. and Little, R.M., The effect of extraction and orthodontic treatment on dentoalveolar support. American Journal of Orthodontics, 1983. 84(3): p. 183‐190.

164. Kinsella, P., Some aspects of root resorption in orthodontics. New Zealand Orthodontic Journal, 1973. 43: p. 247‐255.

165. Sjolien, T. and Zachrisson, B.U., Periodontal bone support and tooth length in orthodontically treated and untreated persons. American Journal of Orthodontics, 1973. 64(1): p. 28‐37.

166. El‐Bialy, T., El‐Shamy, I. and Graber, T.M., Repair of orthodontically induced root resorption by ultrasound in humans. American Journal of Orthodontics and Dentofacial Orthopedics, 2004. 126(2): p. 186‐193.

167. Grove, J.L., The Effect Of Mechanical Vibration (113 Hz Applied to Maxillary First Premolars) On Root Resorption Associated With Orthodontic Force: A Micro‐CT Study [Thesis], 2011, University of Sydney Australia.

168. Barber, A.F. and Sims, M.R., Rapid maxillary expansion and external root resorption in man: a scanning electron microscope study. American Journal of Orthodontics, 1981. 79(6): p. 630‐52.

169. DeShields, R.W., A Study of Root Resorption in Treated Class II, Division I Malocclusions. Angle Orthodontist, 1969. 39(4): p. 231‐245.

170. Goldson, L. and Henrikson, C.O., Root resorption during Begg treatment; a longitudinal roentgenologic study. American Journal of Orthodontics, 1975. 68(1): p. 55‐66.

171. Wu, A.T.J., Turk, T., Colak, C., Elekda ‐Turk, S., Jones, A.S., Petocz, P. and Darendeliler, M.A., Physical properties of root cementum: Part 18. The extent of root resorption after the application of light and heavy controlled rotational orthodontic forces for 4 weeks: A microcomputed tomography study. American Journal of Orthodontics & Dentofacial Orthopedics, 2011. 139(5): p. e495‐e503.

172. Jimenez‐Pellegrin, C. and Arana‐Chavez, V.E., Root resorption in human mandibular first premolars after rotation as detected by scanning electron microscopy. American Journal of Orthodontics & Dentofacial Orthopedics, 2004. 126(2): p. 178‐184.

173. King, A.D., Turk, T., Colak, C., Elekdag‐Turk, S., Jones, A.S., Petocz, P. and Darendeliler, M.A., Physical properties of root cementum: Part 21. Extent of root resorption after the application of 2.5° and 15° tips for 4 weeks: A microcomputed tomography study. American Journal of Orthodontics and Dentofacial Orthopedics, 2011. 140(6): p. e299‐e305.

174. Paetyangkul, A., Türk, T., Elekdağ‐Türk, S., Jones, A.S., Petocz, P., Cheng, L.L. and Darendeliler, M.A., Physical properties of root cementum: Part 16. Comparisons of root resorption and resorption craters after the application of light and heavy continuous and controlled orthodontic forces for 4, 8, and 12 weeks. American journal of orthodontics and dentofacial orthopedics, 2011. 139(3): p. e279‐e284.

175. Bartley, N., Türk, T., Colak, C., Elekda ‐Türk, S., Jones, A., Petocz, P. and Darendeliler, M.A., Physical properties of root cementum: Part 17. Root resorption after the application of 2.5° and 15° of buccal root torque for 4 weeks: A microcomputed tomography study. American Journal of Orthodontics & Dentofacial Orthopedics, 2011. 139(4): p. e353‐e360.



CAROLYN NG 48

176. Goldin, B., Labial root torque: effect on the maxilla and incisor root apex. American Journal of Orthodontics & Dentofacial Orthopedics, 1989. 95(3): p. 208‐219.

177. Nakano, T., Hotokezaka, H., Hashimoto, M., Sirisoontorn, I., Arita, K., Kurohama, T., Darendeliler, M.A. and Yoshida, N., Effects of different types of tooth movement and force magnitudes on the amount of tooth movement and root resorption in rats. Angle Orthodontist, 2014.

178. Melsen, B., Agerbæk, N. and Markenstam, G., Intrusion of incisors in adult patients with marginal bone loss. American Journal of Orthodontics and Dentofacial Orthopedics, 1989. 96(3): p. 232‐241.

179. Han, G., Huang, S., Von den Hoff, J.W., Zeng, X. and Kuijpers‐Jagtman, A.M., Root resorption after orthodontic intrusion and extrusion: an intraindividual study. Angle Orthodontist, 2005. 75(6): p. 912.

180. Dermaut, L. and De Munck, A., Apical root resorption of upper incisors caused by intrusive tooth movement: a radiographic study. American Journal of Orthodontics and Dentofacial Orthopedics, 1986. 90(4): p. 321‐326.

181. Vlaskalic, V., Boyd, R.L. and Baumrind, S., Etiology and sequelae of root resorption. Seminars in Orthodontics, 1998. 4(2): p. 124‐31.

182. Cakmak, F., Turk, T., Karadeniz, E.I., Elekdag‐Turk, S. and Darendeliler, M.A., Physical properties of root cementum: Part 24. Root resorption of the first premolars after 4 weeks of occlusal trauma. American Journal of Orthodontics and Dentofacial Orthopedics, 2014. 145(5): p. 617‐625.

183. Kim, Y.H. and Son, W.S., Root resorption and bone resorption by jiggling force in cat premolars. Korean Journal of Orthodontics, 1994. 24(3): p. 621‐630.

184. Matsuda Y, M.M., Kaku M, Kawata T, Fujita T, Ohtani J, et al., Histochemical analysis of root resorption in rats by jiggling forces. . Abstract, available at http://iadr.confex.com/iadr/japan10/preliminaryprogram/abstract_143030.htm.

185. Rudolph, D.J., Willes, P.M.G. and Sameshima, G.T., A finite element model of apical force distribution from orthodontic tooth movement. Angle Orthodontist, 2001. 71(2): p. 127‐31.

186. Henry, J.L. and Weinmann, J.P., The pattern of resorption and repair of human cementum. Journal of the American Dental Association, 1951. 42(3): p. 270‐90.

187. Acar, A., Canyürek, U., Kocaaga, M. and Erverdi, N., Continuous vs. discontinuous force application and root resorption. Angle Orthodontist, 1999. 69(2): p. 159.

188. Maltha, J. and Dijkman, G., Discontinuous forces cause less extensive root resorption than continuous forces. European Journal of Orthodontics, 1996. 18: p. 420.

189. Oppenheim, A., Human tissue response to orthodontic intervention of short and long duration. American Journal of Orthodontics and Oral Surgery, 1942. 28(5): p. 263‐301.

190. Reitan, K., Effects of force magnitude and direction of tooth movement on different alveolar bone types. Angle Orthodontist, 1964. 34(4): p. 244‐255.

191. Weiland, F., Constant versus dissipating forces in orthodontics: the effect on initial tooth movement and root resorption. European Journal of Orthodontics, 2003. 25(4): p. 335‐42.

192. Aras, B., Cheng, L.L., Turk, T., Elekdag‐Turk, S., Jones, A.S. and Darendeliler, M.A., Physical properties of root cementum: Part 23. Effects of 2 or 3 weekly reactivated continuous or intermittent orthodontic forces on root resorption and tooth movement: A microcomputed



CAROLYN NG 49

tomography study. American Journal of Orthodontics and Dentofacial Orthopedics, 2012. 141(2): p. e29‐e37.

193. Ballard, D.J., Jones, A.S., Petocz, P., Darendeliler, M.A. and Baccetti, T., Physical properties of root cementum: part 11. Continuous vs intermittent controlled orthodontic forces on root resorption. A microcomputed‐tomography study. American Journal of Orthodontics & Dentofacial Orthopedics, 2009. 136(1): p. 8.e1‐8; discussion 8‐9.

194. Owman‐Moll, P., Kurol, J. and Lundgren, D., Continuous versus interrupted continuous orthodontic force related to early tooth movement and root resorption. Angle Orthodontist, 1995. 65(6): p. 395‐401; discussion 401‐2.

195. Schwarz, A.M., Tissue changes incidental to orthodontic tooth movement. International Journal of Orthodontia, 1932. 18: p. 331‐352.

196. Sandstedt, C., Einige beiträge zur theorie der zahnregulierung. Nord Tandlaeg. Tidskr, 1904. 5: p. 236‐256.

197. Sandstedt, C., Einige beiträge zur theorie der zahnregulierung. Nord Tandlaeg. Tidskr., 1905. 6: p. 1‐25.

198. Davidovitch, Z., Nicolay, O.F., Ngan, P.W. and Shanfeld, J.L., Neurotransmitters, cytokines, and the control of alveolar bone remodeling in orthodontics. Dental Clinics of North America, 1988. 32(3): p. 411‐35.

199. Brudvik, P. and Rygh, P., The initial phase of orthodontic root resorption incident to local compression of the periodontal ligament. European Journal of Orthodontics, 1993. 15(4): p. 249‐263.

200. Brudvik, P. and Rygh, P., Non‐clast cells start orthodontic root resorption in the periphery of hyalinized zones. European Journal of Orthodontics, 1993. 15(6): p. 467.

201. Brudvik, P. and Rygh, P., Multi‐nucleated cells remove the main hyalinized tissue and start resorption of adjacent root surfaces. European Journal of Orthodontics, 1994. 16(4): p. 265‐273.

202. Lacey, D., Timms, E., Tan, H.‐L., Kelley, M., Dunstan, C., Burgess, T., Elliott, R., Colombero, A., Elliott, G. and Scully, S., Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell, 1998. 93(2): p. 165‐176.

203. Sasaki, T., Differentiation and functions of osteoclasts and odontoclasts in mineralized tissue resorption. Microscopy research and technique, 2003. 61(6): p. 483‐495.

204. Brudvik, P. and Rygh, P., Transition and determinants of orthodontic root resorption‐repair sequence. European Journal of Orthodontics, 1995. 17(3): p. 177‐188.

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CAROLYN NG 51

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285. Anderson, P., Elliott, J., Bose, U. and Jones, S., A comparison of the mineral content of enamel and dentine in human premolars and enamel pearls measured by X‐ray microtomography. Archives of Oral Biology, 1996. 41(3): p. 281‐290.

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CAROLYN NG 58

Carolyn Lian Tat Ng, BDSc

Post‐graduate student

Discipline of Orthodontics

Faculty of Dentistry

University of Sydney, Australia

Tamer Türk, DDS, PhD

Professor

Department of Orthodontics


University of Ondokuz Mayis, Turkey

Peter Petocz, PhD

Associate Professor, Statistician

Department of Statistics

Macquarie University, Australia

Selma Elekdag‐Türk

Associate Professor



University of Ondokuz Mayis, Turkey

Oyku Dalci, DDS, PhD

Senior Lecturer




Fethiye Cakmak

Assistant professor



University of Bulent Ecevit, Turkey.

M. Ali Darendeliler, BDS, PhD, Dip Ortho, Certif.

Orth, Priv. Doc

Professor and Chair




Matthew Foley, BSc, PhD

Image Analysis and Computed Tomography Specialist

Australian Centre for Microscopy & Microanalysis


Address for Correspondence:

M. Ali Darendeliler


Level 2, 2 Chalmers Street

Surry Hills, NSW 2010

Australia

Phone +61 2 93518314

Fax +61 2 9351 8336

Email: [email protected]



CAROLYN NG 59

4.1 Abstract

Introduction: Jiggling tooth movements may be responsible for root resorption in the

absence of overt root displacement. This study aims to quantify and compare the effects of

controlled heavy transverse buccal and palatal, and vertical extrusive and intrusive jiggling forces

applied over a 12 week period on root resorption, and to localize the sites of prevalence in

premolars.

Method: Ten patients who required bilateral maxillary first premolar extractions as part of

their orthodontic treatment participated in this study. The total sample consisted of 20 maxillary first

premolars. Heavy (225g) forces were applied to the right or left first premolar with the direction of

force alternating along either the transverse or vertical plane every 4 weeks over a 12 week

period. After the experimental period, the teeth were extracted without root damage and analysed

with micro computed tomography. Each specimen was studied in 3 dimensions with specifically

designed software to measure the volume of each crater.

Results: Heavy vertical forces produced marginally more root resorption than heavy

transverse forces with median total crater volumes of 1.51mm3 and 0.92mm3, respectively (p=0.032).

There was also a significant difference in the total root resorption on each root surface caused by

heavy vertical and transverse forces (p<0.001) with greater resorption on the distal root surface of

premolars undergoing heavy vertical jigging forces. The cervical, middle or apical thirds of the root

for both heavy vertical and transverse jiggling forces did not show any significant difference in root

resorption.

Conclusion: Heavy vertical jiggling forces produced more root resorption than heavy

transverse jiggling forces. Clinicians should especially avoid mechanics that apply vertical jiggling

forces as these maybe more detrimental.



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Key Words: Root resorption, jiggling, heavy forces, transverse, vertical, micro‐computed

tomography, volumetric analysis.

4.2 Introduction

Jiggling forces have generally been accepted to be responsible for Orthodontically Induced

Inflammatory Root Resorption (OIIRR).1, 2 Jiggling was first described by Oppenheim3 and defined as

“small intermittent movements along the tooth axis originating from biting forces when antagonizing

teeth oppose extrusive forces,”3, 4 or a tooth oscillating along a line of movement.5 Jiggling forces

are thought to be produced during orthodontic treatment when there are occlusal interferences;3, 6

when deformation of light archwires occurs during function with concomitant use of intermaxillary

elastics;6 and following dental relapse that occurs after removal of palatal expanders.5 Restorative

build‐ups on first premolars, used to increase the vertical dimension by 2mm for 4 weeks, have been

found to have increased OIIRR during the active bite‐increase period, which may be due to the

premature contacts that transmit excessive uncontrolled vertical forces.7 Two animal studies have

investigated the effects of jiggling on OIIRR. Kim and Son (1994) found no histological or radiographic

difference in the pattern of OIIRR in a feline model when alternating mesial and distal forces were

applied in 3 day cycles over 6, 12, 18 and 24 days when compared to unidirectional mesial forces; 8

while Matsuda et al found that weekly cycles of alternating buccal and lingual jiggling forces

produced more OIIRR in Wistar rats than two or four weekly cycles, which continued to increase as

the duration of applied jiggling forces lengthened.9 However, Baumrind in 1996 also advised,

“resorption in the absence of overt root displacement seems entirely consistent with the purported

role of “jiggling” during orthodontic treatment...”10

The severity of OIIRR is directionally proportional to the magnitude of the applied force. 5, 11‐

17 Numerous three‐dimensional quantitative studies on human maxillary first premolars have

demonstrated an increased amount of OIIRR with increased force levels,18‐21 and in a rigorous

systematic review of the literature, Weltman in 2010 concluded that heavy force application



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produced significantly more OIIRR than light force application or control groups.22 Heavy forces that

induce excessive hyalinisation interferes with the repair of root resorption craters, resulting in an

increased prevalence of OIIRR.11, 13, 23‐25

There are several x‐ray microcomputed tomography (XMT) studies analysing the effect of

heavy and light forces on OIIRR on human premolars.19‐21 The volume of root resorption produced

over a 12 week period by heavy buccal forces has been found to be 2.25 times greater than light

forces.21 Over a 4 week period, the volume of root resorption produced by heavy intrusive and

extrusive forces have been found to be approximately 619 and 320 times greater than light forces,

respectively.

This study aims to quantify and compare the effects of controlled heavy transverse buccal

and palatal, and vertical extrusive and intrusive jiggling forces applied over a 12 week period on root

resorption, and to localise the sites of prevalence in premolars. It was hypothesized that: heavy

vertical jiggling forces would result in greater root resorption volumes than transverse forces; the

pattern of root resorption, in terms of the root surfaces and vertical third regions between the

transverse and vertical jiggling force groups, would differ based on the location of force

concentration; and heavy jiggling forces would result in clinically significant or severe root shortening

in both the transverse and vertical groups.

4.3 Material and Methods

4.3.1 Sample

The sample consisted of 20 maxillary first premolars extracted from 10 orthodontic patients

(7 girls, 3 boys), requiring removal of these teeth as part of their orthodontic treatment at Ondokuz

Mayis University, Turkey. The mean age of these patients was 14 years and 7 months, (11 years and

9months to 17 years and 7 months). Patients were selected according to a strict selection criteria

described previously,26 with sufficient room for the proposed tooth movements to be carried out.



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Ethics approvals were obtained from Zonguldak Karaelmas University (now known as University of

Bulent Ecevit) Clinical Research Ethics Committee in Turkey (2012/06) and the University of Sydney

Human Research Ethics Committee (2013/1095). Written and verbal informed consent was obtained

from the participants and their parents or guardians. This study was also registered in the Australian

and New Zealand Clinical Trials Registry.

Heavy (225g) forces, measured using a strain gauge (Dentaurum, Germany), were applied to

a randomly selected right or left first premolar with the direction of force alternating along either the

transverse (bucco‐palatal) or vertical (intrusive‐extrusive) plane every 4 weeks over a 12 week

period. In transverse plane, the premolar was moved buccally for four weeks, palatally for four

weeks and buccally again for another 4 weeks. In the vertical plane, the premolar was intruded for

four weeks, extruded for four weeks and intruded again for another 4 weeks. All patients were

treated by the same operator.

4.3.2 Appliance Design

SPEED™ orthodontic brackets with a 0.022 inch slot (Strite Industries, Cambridge, Ontario,

Canada) were bonded to the maxillary first molars and premolars. A 0.017 x 0.025 inch Titanium

Molybdenum Alloy wire was used to apply transverse and vertical forces. A transpalatal arch

connecting the upper first molars was included in the setup with occlusal stops to prevent occlusal

interferences (Figure 1).

4.3.3 Specimen Collection

After the experimental period, the teeth were extracted without root damage and placed in

individual containers of 10% buffered formalin. Any residual periodontal ligament and soft tissue was

removed by placement in an ultrasonic bath for 10 minutes followed by gently rubbing the root with

damp gauze. The teeth were then immersed in 70% ethanol for 30min for disinfection and bench

dried for at least 24 hours.



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4.3.4 Specimen Analysis

A desktop microcomputed tomography x‐ray system (SkyScan 1172, Aartselaar, Belgium) was

used to produce multiple high resolution tomography projection images of the tooth. The x‐ray

tube operated at 59kV with a current of 167μA, and without filters. The rotation step of the tooth

was at 0.200° and images were saved as 16 bit Tagged Image File Format (TIFF) files. Axial slice‐by‐

slice reconstruction was achieved using Nrecon (version 1.4.2, Aartselaar, Belgium), which is

SkyScan's reconstruction software. Avizo Fire Version 8 (FEI Visualisation Sciences Group, Burlington,

MA, USA) was used for 3D reconstruction and visualisation of the dataset. Craters were manually

isolated, duplicated and volumetrically calculated using a convex hull macro within Fiji, an image

processing package comprising of Image J 1.47g, Java and Java 3D. This macro was developed by Dr

Matthew Foley at the Australian Centre for Microscopy & Microanalysis at the University of

Sydney. Once the craters were duplicated, the macro applies a 2D convex hull algorithm to each

axial slice and calculates the number of pixels within the isolated crater. The macro then adds the

total number of pixels across all slices and multiplies this value by the voxel volume, determined by

the resolution (17.6μm), to calculate the total volume of the crater.

Craters were grouped according to their location on the root surface (buccal, lingual, mesial,

distal) and according to their location in the vertical regions of the tooth (cervical, middle, apical).

The total number of cross‐sectional slices from the CEJ to the apex for each tooth was divided into

thirds to determine the different vertical regions. Craters were allocated based on which region that

corresponded to the majority of slices.

4.3.5 Statistical Analysis

Statistical analysis was performed using commercial software (SPSS for Windows, version 21,

SPSS Inc., Chicago Ill). In order to create a model that satisfied the assumptions of the analysis, the

scale of measurement was converted from volume (cubic millimetres) to cube‐root‐volume



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(millimetres). In doing so, the forces were compared to equivalent radii of the craters. This method

has been used in similar studies.19, 27 For statistically significant results, the mean values were

transformed back to the volumetric scale, which adjusts for patient and other factors used in the

analysis, and effectively translates to the median values for the sample.

The statistical analysis was conducted using a Univariate Analysis of Variance (ANOVA) with a

modified Bonferroni adjustment for each of the cube‐root volumes as response‐variables: patient

was assigned as a random factor (which links the two teeth from each person); and force, surface,

region and their interactions as fixed factors. Due to the large number of tests examined, a

significance level of 0.01 has been used, and p‐values between 0.01 and 0.05 were considered

marginally significant, in order to have some protection against type 1 errors (falsely rejecting a true

null hypothesis).

Craters were measured three times for 15% of the sample, 2 and 3 months after the initial

analysis, to determine the overall standard error of measurement.

4.4 Results

Heavy vertical jiggling forces produced more resorption than transverse forces at 1.15mm

(1.51mm3) and 0.97mm (0.92mm3), respectively (Figure 2). This difference was marginally significant,

p = 0.032.

The mean cube‐root volumes for the different force and region combinations is shown in

Table 2 and is depicted in the profile plot in Figure 3. Heavy vertical jiggling forces produced more

resorption than transverse jiggling forces, however this difference was not statistically significant (p =

0.127). Cervical regions appeared to have more resorption than middle or apical regions, however

these differences were also not statistically significant (p = 0.06). Although the trend of resorption

values across the different vertical regions appear to be different for vertical and transverse forces in

Figure 3, these differences were not found to be statistically significant (p=0.438).



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The mean cube‐root volumes for the different forces and surface combinations is shown in



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Table 3 and is depicted in the profile plot in Figure 4. There was no overall difference

(p=0.66) in the amount of root resorption between vertical and transverse forces. Irrespective of the

type of force applied, the distal surfaces had the highest amount of root resorption (0.755mm or

0.430mm3) followed by the mesial (0.646mm or 0.270mm3), buccal (0.527mm or 0.146mm3) and

lingual (0.410mm or 0.069mm3). These differences between surfaces were statistically significant

(p<0.001). Vertical jiggling forces produced both the greatest and the least amount of resorption,

which were found on the distal and lingual surfaces respectively (p<0.001). The difference in the

trends of resorption volumes across the different root surfaces for vertical and transverse forces in

Figure 4 is statistically significant (p<0.001).

Overall the statistical analysis revealed both statistically significant and marginally significant

differences in root resorption between patients for all analyses conducted. Consequently patients

were included as a random factor in the analysis which links the data obtained from the left and right

sides of the mouth.

The overall standard error of measurement was found to be 0.0442mm3 and the coefficient

of variance was 7.1%.

4.5 Discussion

Jiggling forces have long been implicated in OIIRR.3, 4, 6, 28 Previous animal8, 9, 29 and human

studies4 exploring the role of jiggling in OIIRR do not provide 3D quantitative conclusions on the

amount of resorption. Additionally, due to the substantive methodological differences between

these studies the results are also incomparable. Studies that discuss the effect of jiggling forces on

OIIRR in humans have been of a short intermittent duration, caused by either the use of

intermaxillary elastics, active removable appliances or occlusal interferences.3, 4, 6, 7 Furthermore,

while these studies report on the effects of jiggling in the transverse5 and vertical4, 7 plane, there are

no studies to date comparing the amount of OIIRR caused by controlled jiggling forces between the

transverse and vertical planes of space.



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This study follows up from a forthcoming prospective XMT study investigating the effect of

light and heavy jiggling forces in comparison with unidirectional light and heavy forces on human

premolars.30 To supplement this investigation, this study aims to compare the effect of controlled

heavy jiggling forces occurring in 4 weekly cycles in the transverse and vertical plane over a 12 week

period.

It is expected that vertical jigging forces would have a higher force per unit area and thus

cause more tissue necrosis and OIIRR;11, 31 a finding that is supported by this study. Vertical jiggling

forces produced a significant 65% more resorption than transverse jiggling forces. Clinically, these

findings indicate that round tripping with heavy vertical forces should be avoided in patients with

pre‐existing root resorption, emphasizing the importance of efficient treatment planning.

Although the patient groups in previous root resorption studies analysed by XMT are not

comparable, Harris et al19 found that heavy intrusive orthodontic forces produced a median average

resorption volume of 9.41 x 10‐4mm3, while Jimenez Montenegro et al20 found that heavy extrusive

orthodontic forces produced a median resorption average volume of 6.33 x 10‐3mm3; however, the

heavy forces in both of these studies were applied for only 4 weeks. These values are much less than

the median resorption values found for vertical (1.51mm3) and transverse (0.92mm3) forces in this

study. Conversely, Paetyangkul et al21 reported heavy buccal forces applied over a 12 week period

resulted in a median average of 17.31mm3. This volume of OIIRR is 18 times greater than that found

in the transverse jiggling group of this study.

In terms of the vertical thirds of the root, although there was no statistical difference in the

mean cube‐root volume of resorption between horizontal and vertical force groups, and between

the different regions, there appears to be a general trend for the heavy vertical force group to exhibit

greater resorption in the cervical third. Given that purely intrusive and extrusive forces are difficult

to obtain without any mesiodistal tipping using the type of spring design in this study, the finding of

greater resorption in the cervical third appears to be concordant with a finite element study



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demonstrating that the principal stress from a tipping force is located at the alveolar crest.32 The lack

of statistical difference between regions is also concordant with results published in other similar

XMT studies.19, 20

Apical cementum is characterised by cellular intrinsic fibre cementum which has an adaptive

and reparative function, with no role in tooth attachment.33 Apical cementum also has a reduced

hardness and elastic modulus in comparison with cervical cementum,34, 35 while the deficiency of

Sharpey’s fibres in cellular cementum is assumed to make repaired and apical cementum more

vulnerable to resorption.36, 37 Consequently, the lack of statistical significance between the different

vertical thirds found in this study and in other similar XMT studies may indicate that the hardness,

elastic modulus and composition of cementum is unrelated to the distribution of OIIRR. Alternately,

the findings in this study may be confounded by the alternating nature of the applied forces that may

have enabled repair of the OIIRR lesions in the apical third, masking the effect of the heavy forces

and reducing the discrepancy in OIIRR volumes between the different regions. Furthermore, the

chosen sample size may be inadequate to elicit statistical differences in the vertical thirds26 and

factor for variations in individual susceptibility, while the treatment duration of the study may also

be inadequate to produce a noticeable difference; Matsuda et al9 found that the amount of root

resorption area caused by jiggling forces in rats increased with increased time lapse of the

experiment.

In this study, the distal root surface was found to have statistically more resorption in the

heavy vertical jiggling group. This may be due to distal placement of the centre of rotation during

extrusive and intrusive movements, caused by the design of the springs, resulting in uncontrolled

distal tipping with greater tooth‐to‐bone contact along the distal surface, facilitating root resorption.

This finding is concordant with those reported in similar micro‐CT studies of vertical forces.19, 20

Additional factors that predispose the distal surfaces to greater root resorption include the original



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tooth position affecting the axial direction of applied forces20 and a distally inclined/dilacerated root

morphology.1, 20, 38, 39

Although, a new algorithm was written for this convex hull calculation, as explained by other

XMT studies, there continues to be a limitation of underestimated crater volume on convex surfaces

and overestimation of crater volumes on concave surfaces, which is mitigated because the crater

volume measurement is based on direct imaging of the tooth as a fully three dimensional object.19

In the process of calculating resorption volumes, there are two points in the process whereby

voxel data is intentionally removed, which may affect the resultant reading on repeated

measurements. When the teeth are scanned by SkyScan 1172 XMT unit, a series of high resolution

projections of the tooth are produced with varying degrees of radiopacity. On reconstruction into

cross‐sectional slices, in SkyScan’s Nrecon software package, the images undergo a process of beam

hardening and artefact reduction, and a user‐defined greyscale range within the image is selected for

the desired reconstruction. Through this process, pixels outside of this greyscale range are omitted

from the cross‐sectional slices, which is attributed to the extremes of being completely opaque or

transparent. Typically this greyscale range should be selected based on the best imaging that can be

achieved across the whole sample. Variations in this range may occur due to individual variations in

tooth mineralisation and radiopacity. The cross‐sectional slices are then compiled as a three‐

dimensional image of the tooth and is inspected for resorption craters in Avizo Fire. Once the

resorption craters have been identified, the collection of cross‐sectional slices are imported into Fiji

(an image processing package based on Image J) and binarisation of the images in the stack of slices

occurs following selection of an appropriate greyscale threshold with black set as background and

white set as tooth structure. Once again, this greyscale threshold is selected based on the best

imaging threshold that applies across the whole sample. Once a crater is identified and isolated, a

range of x, y and z coordinates are then selected that define the location of the crater. Although the

coordinates of the crater have been defined; to get to this stage, there have been two time points (at



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reconstruction and on binarisation) whereby voxel data is omitted from the final sample from which

crater volumes are calculated. Selection of different greyscale ranges and different greyscale

thresholds may result in omission of different voxels in the final sample when the process is

repeated, which effectively translates as variability in the number of craters and/or total volume of

OIIRR.

To measure the reliability of the method, 15% of the sample underwent the process of

reconstruction, conversion to binary scale and analysis, three times, 2 and 3 months after the initial

analysis, to produce an overall standard error of measurement of 0.0442mm3 and a coefficient of

variance of 7.1%. The sample size chosen for repeat analysis follows that used in a previous micro‐CT

study.20 The importance of repeating the process from reconstruction to volumetric analysis ensures

that discrepancies in greyscale range and threshold selection are factored into the error of

measurement. If the teeth do not undergo the whole process from reconstruction to volumetric

analysis on repeat measurements, then there is unlikely to be a significant difference in the standard

error of measurement as the x, y, z coordinates of a binary image are unlikely to deviate from the

initial analysis. The standard error of measurement in this study is similar to that reported in a

similar XMT study on OIIRR.40

Volumetric root resorption results obtained by different XMT studies are often not

comparable because of variations in the scanning environment, x‐ray beam properties and the

operator involved in establishing image reconstruction and volumetric analysis parameters. The use

of a calibrated phantom at the time of scanning each tooth would enable the entire sample to be

calibrated and measured according to a defined greyscale range and threshold. When subsequent

samples and studies are scanned with the same calibrated block it is expected that there may be

greater standardisation and comparability between studies and samples. However, there is a

practical issue of space optimisation in the chamber when inadequate space is available for the



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sample alone. Furthermore there may be considerations relating to degradation of the calibrated

phantom on repeated analysis.

The force characteristics employed by this study were chosen to reflect those used in routine

clinical orthodontic treatment. Although the experimental period was short, the transverse force

group may have a force pattern similar to that used in alternating rapid maxillary expansion and

contraction (ALT‐RAMEC) protocols advocated by Liou41, 42 for disarticulation of circumaxillary sutures

for maxillary protraction in cleft and Class III patients. Alternately, the vertical force group may have

a force pattern similar to that used in correction of deep bite Class II division 2 malocclusions,

whereby maxillary incisors are intruded to reduce the deep bite and allow Class II correction,

extruded during incisor palatal‐root torque expression and re‐intruded again to re‐establish optimal

overbite. The findings from this study indicate that the latter form of mechanics, when used with

heavy forces, is more damaging than the former, which typically uses heavy forces, and as such,

should be avoided in patients with clinical signs of increased risk for OIIRR. Considerations for

efficient mechanotherapy with light forces is especially important in management of patients with

malocclusions that may result in alternating vertical intermittent forces. Further treatment

considerations may include the avoidance of intermaxillary elastics on light archwires and prevention

of premature occlusal contacts in the final stages of incisor retraction to avoid occlusal

interferences.6

This findings of this study also suggest that combined tooth‐borne and bone‐borne

expansion appliances may be a desirable option to reduce the transverse loading on the teeth during

ALT‐RAMEC expansion protocols. Vardimon5 demonstrated in an animal model that bone‐borne

direct magnetic expansion resulted in less OIIRR than indirect tooth‐borne magnetic expansion, and

there was less OIIRR after 4months retention and 2 months relapse due to repair of the OIIRR lesions.



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4.6 Conclusion

Heavy vertical jiggling forces produced greater OIIRR volumes than heavy transverse jiggling

forces, neither of which appear to result in severe root shortening. Vertical jiggling forces produced

greater OIIRR lesions on the distal surface of the root, which may be related to the type of spring

design used. Clinicians should avoid mechanics that apply vertical jiggling forces as these maybe

more detrimental.

4.7 Acknowledgement

The authors would like to thank the ASO Foundation for Research and Education for their

kind financial support and acknowledge the role of the Australian Microscopy and Microanalysis

Facility in this research.



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4.8 References

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3. Stuteville, O., Injuries caused by orthodontic forces and the ultimate results of these injuries. American Journal of Orthodontics and Oral Surgery, 1938. 24(2): p. 103‐119.

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16. Faltin, R.M., Arana‐Chavez, V.E., Faltin, K., Sander, F.G. and Wichelhaus, A., Root resorptions in upper first premolars after application of continuous intrusive forces. Intra‐individual study. Journal of Orofacial Orthopedics, 1998. 59(4): p. 208‐19.

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30. Eross, E., Turk, T., Elekda ‐Türk, S., Cakmak, F., Jones, A., Papadopoulou A.K. and Darendeliler, M.A., Extent of root resorption after the application of light and heavy bucco‐palatal forces for 12 weeks: A microcomputed tomography study. PhD Thesis, School of Semmelweis University, Budapest, Hungary, 2014.

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32. Rudolph, D.J., Willes, P.M.G. and Sameshima, G.T., A finite element model of apical force distribution from orthodontic tooth movement. Angle Orthodontist, 2001. 71(2): p. 127‐31.

33. Nanci, A. and Ten Cate, A.R., Ten Cate's oral histology: development, structure, and function. 6th ed, ed. P. Rudolph 2003, St Louis: Mosby.

34. Srivicharnkul, P., Kharbanda, O.P., Swain, M.V., Petocz, P. and Darendeliler, M.A., Physical properties of root cementum: Part 3. Hardness and elastic modulus after application of light and heavy forces. American Journal of Orthodontics & Dentofacial Orthopedics, 2005. 127(2): p. 168‐76; quiz 260.

35. Malek, S., Darendeliler, M.A. and Swain, M.V., Physical properties of root cementum: Part I. A new method for 3‐dimensional evaluation. American Journal of Orthodontics & Dentofacial Orthopedics, 2001. 120(2): p. 198‐208.

36. Vardimon, A.D., Graber, T.M., Voss, L.R. and Lenke, J., Determinants controlling iatrogenic external root resorption and repair during and after palatal expansion. Angle Orthodontist, 1991. 61(2): p. 113‐122.

37. Jones, S. and Boyde, A., The resorption of dentine and cementum in vivo and in vitro. Biological mechanisms of tooth eruption and root resorption. Ohio: Columbus, 1988: p. 335‐354.

38. Oyama, K., Motoyoshi, M., Hirabayashi, M., Hosoi, K. and Shimizu, N., Effects of root morphology on stress distribution at the root apex. European Journal of Orthodontics, 2007. 29(2): p. 113‐7.

39. Aoki, K., [Morphological studies on the roots of maxillary premolars in Japanese]. Shika gakuho. Dental science reports, 1990. 90(2): p. 181‐199.

40. Cheng, L.L., Türk, T., Elekdag‐Türk, S., Jones, A.S., Petocz, P. and Darendeliler, M.A., Physical properties of root cementum: Part 13. Repair of root resorption 4 and 8 weeks after the application of continuous light and heavy forces for 4 weeks: A microcomputed‐tomography study. American Journal of Orthodontics and Dentofacial Orthopedics, 2009. 136(3): p. 320. e1‐320. e10.

41. Liou, E., Effective maxillary orthopedic protraction for growing Class III patients: a clinical application simulates distraction osteogenesis. Progress in Orthodontics, 2005. 6(2): p. 154‐71.

42. Liou, E.J.W. and Tsai, W.C., A new protocol for maxillary protraction in cleft patients: repetitive weekly protocol of alternate rapid maxillary expansions and constrictions. The Cleft Palate‐Craniofacial Journal, 2005. 42(2): p. 121‐127.

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4.9 Figures

Figure 2: Experiment protocol ................................................................................................ 77

Figure 3: Mean resorption values for heavy jiggling forces. ..... Error! Bookmark not defined.

Figure 4: Mean resorption values for each vertical third region. .......................................... 78

Figure 5: Mean resorption values for each root surface. .......... Error! Bookmark not defined.

THE EXTE

CAROLYN N

A

for four

weeks, e

sides.

NT OF ORTHODO

NG

A randomly

weeks and

extruded for


F

selected righ

buccally for

r four weeks

CED INFLAMMAT

T WITH HEAVY FO

Figure 1: E

ht or left firs

four weeks,

and intrude


Experimen

st premolar w

, while the c

ed for four w

ORPTION FOLLOW

WEEKS: A MICRO

nt protoco

was moved

contralateral

weeks. 225g

WING TRANSVER

O‐CT STUDY

ol

buccally for

l premolar w

of heavy for

SE AND VERTICA

four weeks,

was intruded

rce was used

L JIGGLING

77

palatally

d for four

d on both

THE EXTE

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bl

()

NT OF ORTHODO

NG

Figure

Cube‐Root Volume (mm)


e 2: Mean

CED INFLAMMAT

T WITH HEAVY FO

n resorptio


on values

Jiggling

ORPTION FOLLOW

WEEKS: A MICRO

for heavy

g Force

WING TRANSVER

O‐CT STUDY

y jiggling f

SE AND VERTICA

forces.

L JIGGLING

78



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Figure 3: Mean resorption values for each vertical third region.

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

Cervical Middle Apical

Estimated M

arginal M

ean

s Cube‐Root Volume (mm)

Vertical Third Region

TransverseVertical



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Figure 4: Mean resorption values for each root surface.

0

0.2

0.4

0.6

0.8

1

1.2

Mesial Distal Buccal Lingual

Estimated M

arginal M

ean

s Cube‐Root Volume (mm)

Tooth Surface

Transverse

Vertical



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4.10 Tables

Table 1: Force Direction: Mean Resorption Values (mm) ...................................................... 82

Table 2: Vertical Third Region vs. Force Direction: Mean Resorption Values (mm) .............. 82

Table 3: Tooth Surface vs. Force Direction: Mean Resorption Values (mm) ......................... 84



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Table 1: Force Direction: Mean Resorption Values (mm)

Mean Resorption Values (mm)

Force

Direction

M

ean

S

D

Transverse 0

.972

0

.049

Vertical 1

.147

0

.049

Table 2: Vertical Third Region vs. Force Direction: Mean Resorption Values (mm)

Vertical Third

Region

Force

Direction

Tra

nsverse

V

ertical

Mesial 0.6

27

0

.665

Distal 0.5

08

1

.001



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Buccal 0.6

25

0

.429

Lingual 0.5

38

0

.282



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Table 3: Tooth Surface vs. Force Direction: Mean Resorption Values (mm)

Vertical Third

Region

Force

Direction

Tra

nsverse

V

ertical

Mesial 0.6

27

0

.665

Distal 0.5

08

1

.001

Buccal 0.6

25

0

.429

Lingual 0.5

38

0

.282



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5. Future Directions

It is expected that the differences in cementum hardness between the apical and cervical

regions and the mosaic nature of cementum composition would result in regional differences in

resorption and repair. Consequently, from a methodological perspective, further OIIRR studies that

incorporate both hardness testing and XMT analysis may assist with determining possible reasons for

the lack of variation in OIIRR for the different vertical thirds. Larger sample sizes that enable greater

levels of stratification in terms of the timing of repair may also assist with achieving a greater

spectrum of OIIRR volumes across the different vertical thirds. With adequate sample sizes,

histologic and XMT studies may be conducted in tandem with hardness testing and XMT studies to

further elucidate the role of cementum composition in OIIRR. There are obvious ethical

considerations pertaining to extended intervention periods, however with well‐planned study

designs, larger scale studies may be more easily implemented with the current study protocols.

Unfortunately, due to magnification and corresponding radiation exposure issues relating to

XMT in comparison with cone beam computed tomography, scanning with CBCT technology before

and after application of orthodontic forces is unlikely to yield adequate data except in cases where

severe OIIRR has occurred.



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6. Appendices

6.1 Sample Distribution

10 participants

Randomly assigned first premolar

Transverse Jiggling

225g

Buccal 4 wks

Palatal 4 wks

Buccal 4 weeks

Extraction

&

Analysis

Vertical

Jiggling

225g

Intrusion 4 wks

Extrusion 4 wks

Intrusion 4 wks

Extraction

&

Analysis

THE EXTE

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6.2 Sp

1

NT OF ORTHODO

NG

pecimen C

10% bufferedFormalin


Collection

10minUltraso

Bath

d

CED INFLAMMAT

T WITH HEAVY FO

Sequence

n nic


Gentle removal ofPDL with

damp gauz

ORPTION FOLLOW

WEEKS: A MICRO

70% Etdisinfe

f

e

WING TRANSVER

O‐CT STUDY

2Be

hanol ection

SE AND VERTICA

24 Hours ench Dry

L JIGGLING

87

THE EXTE

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6.3 Sp

S

images o

images.

identific

using a c

NT OF ORTHODO

NG

pecimen A

SkyScan 117

of the tooth.

Avizo Fire

ation of cra

convex hull m

Sky


Analysis Se

72 scanner w

. SkyScan Nr

was used f

ters. Craters

macro within

yScan1172

CED INFLAMMAT

T WITH HEAVY FO

equence

was used to

recon softwa

for the 3D r

s were man

n Fiji, an imag

N2


produce mu

are package

reconstructio

nually isolate

ge processin

Nrecon

SkyHig

ORPTION FOLLOW

WEEKS: A MICRO

ultiple high re

was used to

on of the t

ed, duplicate

g package co

yScan1172

h-resolution

WING TRANSVER

O‐CT STUDY

esolution to

o reconstruct

tooth to allo

ed and volu

omprising of

Micro-

SE AND VERTICA

mography p

t axial cross‐

ow visualiza

metrically c

f Image J.

L JIGGLING

88

rojection

‐sectional

tion and

alculated



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6.4 Total Volumetric Resorption per Tooth

Total volume of resorption per Tooth (mm3)

Subject Transverse (T) Vertical (V)

1 0.031 0.024

2 0.075 0.142

3 0.019 0.070

4 0.072 0.041

5 0.071 0.080

6 0.029 0.049

7 0.027 0.060

8 0.067 0.166

9 0.050 0.078

10 0.042 0.069

6.5 Total Volumetric Resorption per Region

Total volume of resorption per vertical third (mm3)

Subject Cervical Middle Apical

T V T B T V

1 0.076 0.101 0.007 0.031 0.025 0.010

2 0.170 0.046 0.040 0.273 0.028 0.069

3 0.040 0.897 0.018 0.018 0.013 0.025

4 0.254 0.000 0.030 0.072 0.032 0.009

5 0.090 0.144 0.092 0.061 0.033 0.029

6 0.069 0.284 0.018 0.029 0.013 0.027

7 0.031 0.347 0.019 0.075 0.049 0.019

8 0.133 0.469 0.044 0.037 0.060 0.108

9 0.079 0.348 0.024 0.030 0.042 0.069

10 0.089 0.167 0.030 0.039 0.036 0.022

Total 1.031 2.803 0.322 0.666 0.329 0.388

Mean 0.103 0.311 0.032 0.067 0.033 0.039

SD 0.067 0.259 0.024 0.075 0.015 0.032

T= transverse, V = Vertical



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6.6 Total Volumetric Resorption per Surface

Total volume of resorption per surface (mm3)

Subject Buccal Distal Lingual Mesial

T V T B T V T V

1 0.039 0.015 0.018 0.029 0.038 0.016 0.024 0.036

2 0.035 0.005 0.109 0.235 0.095 0.001 0.064 0.066

3 0.007 0.040 0.013 0.116 0.018 0.000 0.040 0.020

4 0.067 0.006 0.060 0.036 0.038 0.003 0.143 0.080

5 0.097 0.022 0.115 0.091 0.003 0.001 0.033 0.092

6 0.023 0.029 0.010 0.087 0.048 0.201 0.036 0.017

7 0.036 0.020 0.020 0.094 0.025 0.000 0.028 0.032

8 0.092 0.015 0.040 0.493 0.051 0.040 0.040 0.076

9 0.035 0.050 0.000 0.174 0.165 0.019 0.039 0.083

10 0.055 0.033 0.043 0.210 0.126 0.042 0.027 0.047

Total 0.486 0.233 0.428 1.565 0.608 0.324 0.474 0.549

Mean 0.049 0.023 0.048 0.156 0.061 0.040 0.047 0.055

SD 0.029 0.015 0.040 0.136 0.052 0.067 0.035 0.028

T= transverse, V = Vertical

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