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Pathomechanics of Calcaneal Apophysitis Simon Christopher McSweeney BHlthSci (Pod) MSc (Pod Med) Submitted in fulfilment of the requirement for the degree of Doctor of Philosophy School of Clinical Sciences Faculty of Health Queensland University of Technology 2019

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Page 1: Pathomechanics of Calcaneal Apophysitis...Pathomechanics of Calcaneal Apophysitis Simon Christopher McSweeney BHlthSci (Pod) MSc (Pod Med) Submitted in fulfilment of the requirement

Pathomechanics of Calcaneal Apophysitis

Simon Christopher McSweeney

BHlthSci (Pod) MSc (Pod Med)

Submitted in fulfilment of the requirement for the degree of

Doctor of Philosophy

School of Clinical Sciences

Faculty of Health

Queensland University of Technology

2019

Page 2: Pathomechanics of Calcaneal Apophysitis...Pathomechanics of Calcaneal Apophysitis Simon Christopher McSweeney BHlthSci (Pod) MSc (Pod Med) Submitted in fulfilment of the requirement

KEYWORDS

Achilles tendon properties, biomechanics. calcaneal apophysitis, children, dynamic ankle

movement, foot mobility, foot movement, foot stiffness, instrumented treadmill, kinematic,

kinetic, paediatric gait analysis, paediatric heel pain, quantitative ultrasound, regional

plantar pressure, reliability, sever’s apophysitis, sever’s disease, temporospatial gait

parameters, transmission-mode ultrasonography, vertical ground reaction force, visual

analogue pain scale.

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ABSTRACT

Calcaneal apophysitis (CA) is a common cause of activity-related heel pain in children,

which is widely regarded as an overuse injury of the cartilaginous-layer of the calcaneal

apophysis. Foot mobility and heightened ground reaction force have been purported to be

clinically associated with the development of the injury. Additional variables clinically

thought to be associated with CA include altered functional properties of the Achilles

tendon and ankle range of movement. There is a paucity of research, however, evaluating

the presence of these potential risk factors and, of the few investigated, scientific support is

often contradictory. The present research aimed to better understand factors clinically

associated with CA through a series of quasi-experimental case-control studies that

investigated foot mobility and stiffness, vertical ground reaction force, functional Achilles

tendon properties and dynamic ankle movement during walking and running in children

with and without the condition.

Since the measurement techniques adopted for the individual experiments in this program

of research have not been widely used in children with CA, the thesis has also

methodologically identified, quantified and described inherent limitations and potential

errors of using these clinical measures in children. The findings indicate that while the

reliability of measures of foot mobility and stiffness were similar to those reported in

adults, foot mobility values in children (8 ± 2 mm) were smaller than those previously

reported in adults (≈18 mm). A follow-up exploratory investigation, in which clinical foot

mobility measures were compared to those obtained from radiographic skin markers in a

small sub-sample of children (n=3), suggested that clinical measures of foot mobility likely

reflect a varied combination of soft tissue distortion and osseous movement in children. In

a further methodological study evaluating the reliability of gait parameters derived from an

instrumented treadmill that incorporated a pressure platform, it was observed that

conventional measures of ground reaction force and temporospatial parameters were highly

repeatable (SEM typically <5%) in children during both walking and running at self-

selected speeds. Finally, consistent with previously consolidated repeatability analyses

reported for adults, the within-subject repeatability of measuring ultrasound velocity of the

Achilles tendon and also ankle electrogoniometric measures in children during running was

highly reproducible from one gait cycle to the next.

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In the experimental component of this thesis, a series of quasi-experimental case-control

studies were performed to analyze foot mobility and stiffness, vertical ground reaction

force, functional Achilles tendon properties and dynamic ankle movement during gait in

children with and without CA. Collectively, these studies have shown that foot mobility

and stiffness, peak vertical ground reaction force during walking and running, and peak

ultrasound velocity in the Achilles tendon during running, a measure of the instantaneous

material stiffness of the tendon, may not clinically differ in children with and without CA.

However, children with CA were characterized by a consistently higher cadence than those

without heel pain specifically during running (≈ 5%). Children with CA also had greater

ankle dorsiflexion (≈ 4°) than those without CA during running despite adopting a similar

foot strike pattern. While these findings may question the rationale behind current

treatments aimed at modifying foot mobility and improving functional Achilles tendon

properties through enhanced ankle dorsiflexion in CA, self-reported pain was inversely

related to peak ankle dorsiflexion and positively related to peak vertical ground reaction

force during running. Hence symptom improvement during running may be linked to

heightened ankle dorsiflexion and lower peak vertical ground reaction force. Although

further research is required, this thesis has provided greater insight into factors associated

with CA in children, and raises a number of questions for further clinical consideration.

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Table of Contents KEYWORDS ............................................................................................................................... 2

ABSTRACT ................................................................................................................................. 3

LIST OF PUBLICATIONS, PAPERS SUBMITTED FOR PUBLICATION AND ADDITIONAL MANUSCRIPTS ................................................................................................ 7

Published Journal Papers.......................................................................................................... 7

Published Conference Abstract ................................................................................................ 7

Submitted Journal Paper .......................................................................................................... 7

Additional Manuscripts ............................................................................................................ 7

LIST OF TABLES ....................................................................................................................... 8

LIST OF FIGURES ..................................................................................................................... 9

LIST OF ABBREVIATIONS .................................................................................................... 11

STATEMENT OF ORIGINAL AUTHORSHIP ....................................................................... 12

ACKNOWLEDGEMENTS ....................................................................................................... 13

CHAPTER 1 INTRODUCTION ............................................................................................... 14

CHAPTER 2 LITERATURE REVIEW .................................................................................... 16

2.1 DESCRIPTION OF CONDITION .................................................................................. 16

2.2 PATHOPHYSIOLOGY ................................................................................................... 17

2.3 SIGNS AND SYMPTOMS.............................................................................................. 19

2.4 DIAGNOSTIC CLINICAL INVESTIGATIONS ............................................................ 20

2.5 AETIOLOGY ................................................................................................................... 22

2.6 DIFFERENTIAL DIAGNOSES ...................................................................................... 34

2.7 DESCRIPTION OF MANAGEMENT ............................................................................ 35

2.8 SUMMARY ..................................................................................................................... 36

CHAPTER 3 RESEARCH AIMS & RATIONALE.................................................................. 38

3.1 AIM 1: Identify whether children with CA possess a more mobile and compliant (less stiff) foot than children without CA. ............................................................................................... 38

3.2 AIM 2: Compare peak vertical ground reaction forces during walking and running in children with and without CA. ............................................................................................... 38

3.3 AIM 3: Assess functional properties of the Achilles tendon in children with and without CA during running. ...................................................................................................................... 39

CHAPTER 4 FOOT MOBILITY MAGNITUDE AND STIFFNESS IN CHILDREN WITH AND WITHOUT CALCANEAL APOPHYSITIS ............................................................................. 40

4.1 ABSTRACT ..................................................................................................................... 41

4.2 INTRODUCTION............................................................................................................ 42

4.3 METHODS ...................................................................................................................... 43

4.4 RESULTS ........................................................................................................................ 46

4.5 DISCUSSION .................................................................................................................. 48

4.6 CONCLUSION ................................................................................................................ 50

4.7 REFERENCES ................................................................................................................. 51

CHAPTER 5 RADIOGRAPHIC FOOT MOBILITY MAGNITUDE IN CHILDREN: AN EXPLORATORY STUDY ........................................................................................................ 54

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5.1 INTRODUCTION............................................................................................................ 55

5.2 METHODS ...................................................................................................................... 55

5.3 RESULTS ........................................................................................................................ 60

5.4 DISCUSSION and CONCLUSION ................................................................................. 61

5.5 REFERENCES ................................................................................................................. 62

CHAPTER 6 RELIABILITY OF AN INSTRUMENTED TREADMILL FOR

CHARACTERIZING GAIT IN CHILDREN............................................................................ 63

6.1 ABSTRACT ..................................................................................................................... 64

6.2 INTRODUCTION............................................................................................................ 65

6.3 METHODS ...................................................................................................................... 65

6.4 RESULTS ........................................................................................................................ 67

6.5 DISCUSSION .................................................................................................................. 71

6.6 CONCLUSION ................................................................................................................ 72

6.7 REFERENCES ................................................................................................................. 73

CHAPTER 7 VERTICAL GROUND REACTION FORCES DURING GAIT IN CHILDREN

WITH AND WITHOUT CALCANEAL APOPHYSITIS ........................................................ 75

7.1 ABSTRACT ..................................................................................................................... 76

7.2 INTRODUCTION............................................................................................................ 77

7.3 METHODS ...................................................................................................................... 77

7.4 RESULTS ........................................................................................................................ 82

7.5 DISCUSSION .................................................................................................................. 84

7.6 CONCLUSION ................................................................................................................ 85

7.7 REFERENCES ................................................................................................................. 86

CHAPTER 8 ULTRASOUND VELOCITY IN THE ACHILLES TENDON OF CHILDREN WITH AND WITHOUT CALCANEAL APOPHYSITIS DURING RUNNING .................... 89

8.1 ABSTRACT ..................................................................................................................... 90

8.2 INTRODUCTION............................................................................................................ 91

8.3 METHODS ...................................................................................................................... 92

8.4 RESULTS ........................................................................................................................ 96

8.5 DISCUSSION ................................................................................................................ 102

8.6 CONCLUSION .............................................................................................................. 103

8.7 REFERENCES ............................................................................................................... 105

CHAPTER 9 GENERAL DISCUSSION ................................................................................ 109

9.1 METHODOLOGICAL ISSUES .................................................................................... 110

9.2 CALCANEAL APOPHYSITIS ..................................................................................... 112

9.3 LIMITATIONS .............................................................................................................. 116

9.4 FUTURE RESEARCH .................................................................................................. 117

9.5 CONCLUSION .............................................................................................................. 118

REFERENCES ........................................................................................................................ 119

APPENDIX A .......................................................................................................................... 128

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LIST OF PUBLICATIONS, PAPERS SUBMITTED FOR PUBLICATION AND

ADDITIONAL MANUSCRIPTS

Published Journal Papers

McSweeney SC, Reed L, Wearing S. Foot Mobility Magnitude and Stiffness in

Children With and Without Calcaneal Apophysitis. Foot Ankle Int. 2018;39(5):585-590.

An eprint record for this work has been added to QUT ePrints. The URL for the eprint record

is https://eprints.qut.edu.au/118616/.

McSweeney S, Reed LF, Wearing SC. Vertical ground reaction forces during gait in

children with and without calcaneal apophysitis. Gait Posture. 2019;71:126-130.

An eprint record for this work has been added to QUT ePrints. The URL for the eprint record

is https://eprints.qut.edu.au/128840/.

Published Conference Abstract

McSweeney SC, Reed LF, Wearing S. The effect of sex on measures of foot mobility

and stiffness in children and adolescents. Footwear Sci. 2017;9(s1):s138-s139.

An eprint record for this work has been added to QUT ePrints. The URL for the eprint record

is https://eprints.qut.edu.au/118614/.

Submitted Journal Paper

Reliability of an instrumented treadmill for characterizing gait in children (Chapter 6).

Submitted to Gait and Posture journal.

Additional Manuscripts

Radiographic foot mobility magnitude in children: an exploratory study (Chapter 5).

Ultrasound velocity in the Achilles tendon of children with and without calcaneal

apophysitis during running (Chapter 8).

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LIST OF TABLES

Table 2.1 Proposed intrinsic & extrinsic risk factors reported in calcaneal apophysitis 24

Table 2.2 Ankle joint (AJ) dorsiflexion (DF) in children with calcaneal apophysitis 29

Table 2.3 Foot alignment in children with calcaneal apophysitis 29

Table 2.4 BMI measurement in children with calcaneal apophysitis 33

Table 2.5 Summary of studies described encompassing treatment in children with

calcaneal apophysitis 33

Table 2.6 Differential diagnoses of calcaneal apophysitis 34

Table 4.1 Anthropometric data for children with and without calcaneal apophysitis 44

Table 4.2 Intra-rater reliability (ICC), standard error of the measurement (SEM),

and minimal detectable change (MDC95%) scores 46

Table 4.3 Foot dimensions during double-limb stance 47

Table 4.4 Change in foot dimensions, foot mobility magnitude and foot stiffness

with loading 47

Table 5.1 Anthropometric data for the three participants 55

Table 5.2 Radiographic foot dimensions during double-limb stance 60

Table 5.3 Changes in soft tissue and osseous radiographic foot dimensions with

loading 60

Table 6.1 Mean (SD) temporospatial and kinetic gait parameters during barefoot

walking on an instrumented treadmill 68

Table 6.2 Mean (SD) temporospatial and kinetic gait parameters during barefoot

running on an instrumented treadmill 69

Table 7.1 Anthropometric data for children with and without calcaneal apophysitis 78

Table 7.2 Mean (SD) temporospatial and kinetic gait parameters during barefoot

walking and running on an instrumented treadmill 83

Table 8.1 Mean (SD) maxima, minima and range in transmission ultrasound

velocity in the right Achilles tendon during barefoot running on an

instrumented treadmill 98

Table 8.2 Mean (SD) temporospatial and kinetic gait parameters during barefoot

running on an instrumented treadmill 99

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LIST OF FIGURES

Figure 2.1 Anatomical margins of the hindfoot in children 18

Figure 2.2 Radiographic representation of the paediatric calcaneus 18

Figure 2.3 Tensional and impact forces in calcaneal apophysitis 23

Figure 2.4 Illustration of histological section of the physis. Separation of bony

trabeculae of the calcaneal apophysis by un-calcified cartilage 25

Figure 2.5 Flow chart illustrating clinically associated risk factors and

postulated mechanisms in calcaneal apophysitis 37

Figure 4.1 Custom-built foot platform used to measure foot mobility magnitude

and foot stiffness under quasi-static loading conditions. The platform

was mounted on a force platform 44

Figure 5.1(a) Anteroposterior foot radiograph demonstrating the

measurement margins for MFWrs (red) and MFWrb (yellow) 58

Figure 5.1(b) Lateral foot radiograph demonstrating the measurement

margins for AHrs and FLrs (red) and AHrb and FLrb (yellow) 58

Figure 5.2 Lateral foot radiographs during NWB (upper) and DLS (lower).

Arrows indicate the position of the radio-opaque dorsal arch

height skin marker. Note both osseous movement and soft

tissue deformation occur 59

Figure 6.1 Typical vertical ground reaction force curves during one gait

cycle of walking (gray line) and running (black line) taken from a

single participant. Note that vertical ground reaction force during

walking was characterized by two maxima (F1, F3), and the local

minimum (F2), whereas only one maxima (F3) was apparent

during running 66

Figure 6.2 Bland and Altman plot for cadence during walking (gray) and running

(black) in children. Bias (solid line) and upper and lower limits of

agreement (dashed lines) for between trials (within-session) 70

Figure 7.1 Vertical ground reaction force, regional plantar pressure and

temporospatial gait parameters during barefoot walking and running

estimated via an instrumented treadmill system 79

Figure 7.2 Each electronic footprint was masked into hindfoot, midfoot and

forefoot segments using proprietary software. The maximum plantar

pressure in each segment was recorded for each footfall and averaged

over 10 seconds of steady-state barefoot walking and running 81

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Figure 8.1(a) Five-element ultrasound probe utilized for ultrasound velocity

measurement in the Achilles tendon. The probe comprises a

1-MHz Emitter (blue*) and four collinear, regularly spaced

receivers (red*) 93

Figure 8.1(b) Ultrasound probe attached to the right Achilles tendon of a child 93

Figure 8.2 Ensemble histories for ultrasound velocity recorded in the

right Achilles tendon of a child with CA (gray line) and one healthy

child (black line) during barefoot running at a matched gait speed.

Each child displayed a RFS pattern 95

Figure 8.3 Mean peak ankle dorsiflexion (DF) and plantarflexion (PF)

for children with CA (gray) and healthy participants (black) during

barefoot running on an instrumented treadmill. Error bars reflect

the standard deviation. *Indicates a statistically significant

difference between children with and without CA 100

Figure 8.4 Scatter plot with trend lines showing the relationships between

self-reported pain (abscissa) with peak ankle dorsiflexion

(left ordinate, gray dots) and self-reported pain with peak

vertical ground reaction force (right ordinate, black dots)

during running 101

Figure 9.1 Flow chart illustrating considerations for the current mechanistic

model of calcaneal apophysitis 115

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LIST OF ABBREVIATIONS

AH - Arch Height

AHI - Arch Height Index

AP - Anteroposterior

BMI - Body Mass Index

BW - Body Weight

CA - Calcaneal Apophysitis

CT - Computed Tomography

DF - Dorsiflexion

DLS - Double Limb Stance

F1 - Force Maxima 1

F2 - Force Maxima 2

FFS - Forefoot Foot Strike

FL - Foot Length

Fm - Force Minima

FMM - Foot Mobility Magnitude

FS - Foot Stiffness

Hz - Hertz

kPa - Kilopascals

kV - Kilovolt

LAT - Lateral

mAs - Milliampere-seconds

MFS - Midfoot Foot Strike

MFW - Midfoot Width

MHz - MegaHertz

mm - Millimetre

MRI - Magnetic Resonance Imaging

m/s - Meter Per Second

ms - Millisecond

NWB - Nonweightbearing

PF - Plantarflexion

PFLR - Peak Force Loading Rate

RFS - Rearfoot Foot Strike

US - Ultrasound

VAS - Visual Analog Scale

VFS - Varied Foot Strike

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STATEMENT OF ORIGINAL AUTHORSHIP

The work contained in this thesis has not been previously submitted to meet requirements for

an award at this or any other higher education institution. To the best of my knowledge and

belief, the thesis contains no material previously published or written by another person

except where due reference is made.

Signature:

Date: _________________________ 23 July 2019

QUT Verified Signature

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ACKNOWLEDGEMENTS

Undertaking this PhD under Professor Scott Cameron Wearing has been one of the most

fortunate and privileged opportunities of my life. A part of me will forever feel in debt to

Professor Wearing for the learning experience that he has provided during my candidature,

the challenges he has driven me with, and the distinguished standard of scientific research

practice that he has expected of me from the outset of this journey. This standard defines him.

I am truly inspired by your overt intelligence Professor Wearing. Thank you for taking me on

as your student, I have been blessed.

My sincere thanks must also be extended to Associate Professor Lloyd Reed, whose

contributions to this thesis and critical review of many manuscripts in preparation for journal

submissions have been invaluable. A/Professor Reed, I respect you as one of the genuine

experts in the field of Podiatric science. I am honored to have had you as a mentor in my

supervisory team.

To Professor Vivienne Tippett, thank you dearly for your timely enthusiasm and

encouragement as an associate supervisor during my candidature. Your insightful advice and

opinion particularly during the writing milestones of this research were instrumental to the

development of this thesis.

The assistance of Mathias Wulf and Dr Derrick Maxwell during the data collection phases of

this PhD must also be recognized. Mathias, our unspoken camaraderie has seen us work so

efficiently together. Thank you for being a fantastic colleague. Dr Maxwell, your technical

assistance with the development of experimental equipment and accessories pertinent to this

research is duly noted. Thank you for supporting Professor Wearing’s team of research

candidates.

Finally, to my family. Thank you for your unconditional support and patience as I have

undergone this experience of a lifetime. This PhD is dedicated to you.

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CHAPTER 1 INTRODUCTION

Calcaneal apophysitis (CA) is a common cause of activity-related heel pain in children,

resulting in discomfort at the secondary growth centre of the calcaneus either during or

directly after physical activity. 1, 2 Typically, the condition affects children between the ages

of 7 and 15 years prior to skeletal maturity. 3-7 There is a reported incidence of between 2 and

5 cases per thousand children in the general population, 8 with the prevalence even greater in

physically active children and those participating in sport (2-16%). 4 The injury has been

described under various names within the literature, including Sever’s disease and Sever’s

apophysitis. 4, 9

CA is thought to result from injury to the apophysis, secondary to repetitive microtrauma

arising from heel strike, or tension or shear arising from altered loading in the Achilles

tendon. 3, 4 Loading is required for the development of strong connective tissues, however too

much loading (magnitude, rate, frequency) may cause microdamage, which is often referred

to as the so called mechanostat theory. 10 To date, empirical evidence demonstrating altered

loading and tendon properties in CA is limited.

Although repetitive loading associated with heel strike, tendon load, and factors that

influence both of these variables have been anecdotally implicated in development of CA,

ultimately, the causes of this condition are not completely understood. 9 Two purported

mechanisms have been suggested to be clinically implicated in the development of the

condition, namely;

(1) heightened ground reaction forces arising during walking and running gait. 11, 12

(2) excessive tension at the insertion of the Achilles tendon into the apophysis secondary

to either an overactive or short triceps surae-Achilles tendon muscle complex; or the

influence of biomechanical foot malalignment. 1, 9, 11, 13-16

While there is emerging evidence that plantar pressures may be heightened in paediatric feet

with CA, 17 further research assessing vertical ground reaction force in symptomatic children

and a matched control group during dynamic activities such as walking and running is

required. Additionally, investigations into the significance of other associated risk factors,

such as foot mobility, functional Achilles tendon properties and dynamic ankle range of

movement may provide greater insight into the potential involvement of excessive tensile

force within the Achilles tendon of children with CA.1, 18, 19

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This research aimed to better understand potential factors anecdotally implicated with CA. In

particular, foot mobility and stiffness, vertical ground reaction force, functional Achilles

tendon properties, and dynamic ankle range of movement in children with and without CA

were investigated. The rationale linking these factors is detailed in the literature review and

outlined in Chapter 3.

This thesis comprises of methodological and an experimental components. A series of quasi-

experimental case-control studies, evaluating foot mobility and stiffness, vertical ground

reaction force; functional Achilles tendon properties and sagittal ankle movement during gait

in children with and without CA have been undertaken, with reliability analyses for each of

these measurement techniques described within each chapter. A small exploratory

investigation of radiographic foot mobility was also undertaken.

Chapter 4 presents the findings of a published manuscript comparing foot mobility and

stiffness measurements in children with and without CA. Chapter 5 explores radiographic

measures of foot mobility magnitude (FMM) in a small subset of children, providing an

evaluation of the contribution of soft tissue distortion to clinical FMM measurement. Chapter

6 reports the within-session reliability of an instrumented treadmill for characterizing gait in

children. Chapter 7 compares vertical ground reaction force in children with and without CA

during walking and running. Chapter 8 outlines the use of transmission-mode ultrasound to

compare Achilles tendon properties in children with and without CA specifically during

running. Additionally, the chapter also evaluates differences in dynamic ankle movement in

these children during running. The findings of these studies are collectively discussed in

Chapter 9, in which potential directions for future research are also outlined.

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CHAPTER 2 LITERATURE REVIEW

This chapter provides a description of CA and presents a review of the accessible literature

pertaining to this condition. The review has considered all levels of evidence relating to CA

with the exclusion of non-English language reports. Literature searches have included the

databases of EMBASE, MEDLINE, CINAHL, PubMed, Biomed Central, Science Direct,

Scopus, Ebscohost and Google scholar. Reference listings of located articles were also

searched for evaluation.

2.1 DESCRIPTION OF CONDITION

CA is a paediatric foot condition involving pain of the calcaneal apophysis; a secondary

growth center into which the Achilles tendon directly inserts. 3, 13, 20 CA was first described

by Haglund in 1907, 21 and further characterized in the literature as an inflammatory disorder

by Sever in 1912. 1 The condition is considered to be the most common cause of heel pain

among children, and usually involves boys between the ages of 7 and 15 years. 3-7

Fibrocartilage and hyaline cartilage at the apophyseal margin of the calcaneus is widely

thought to be susceptible to micro-damage from repetitive loading associated with heel strike,

tension within the Achilles tendon or shearing resulting from their combination; ultimately

leading to pain. 22 Involvement of the cartilaginous physis accounts for the age-specificity of

the injury, with cessation of symptoms occurring following osseous fusion of the calcaneal

growth centers at adolescence. 1

The prevalence of CA is believed to be between 2% and 16% of all musculoskeletal

complaints reported in children seeking treatment, 9 with approximately 60-65% of cases

presenting bilaterally. 23, 24 These estimates have been mainly derived from European and

American populations subsequent to retrospective review of clinical notes within sports

medicine clinics. Thus, the true incidence of CA within an entire population is yet to be

determined. However, a higher prevalence is thought to be evident among active paediatric

patients. 23, 25, 26

CA is recognized as a benign, self-limiting injury, as calcaneal cartilage at the physis

eventually ossifies with time to form bone. 27 Although the condition is self-limiting, previous

research has demonstrated that the heel pain associated with CA may adversely affect the

health-related quality of life of children. 28 Children with CA (n = 67) have been reported to

have significantly lower ‘happiness’ (≈ 15%) and ‘sport/physical function’ (≈ 32%) subscale

scores than children without CA (control group n = 236) based on self-reported response to

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the Pediatric Orthopedic Surgeons of North America ‘Musculoskeletal Quality of Life’

questionnaire. 28 Additionally, social impacts of CA and the influence of the condition in the

school environment have been described; as have child and parent perceptions of health

related quality of life associated with CA. 19, 29 Interestingly, this later research has suggested

that children with CA experiencing higher pain levels associated with the condition report

less impact of CA at school and during play, possibly attributed to their competitive

motivation and the ability to endure pain during physical activity. 19 Consistent with this

finding, children with CA have also been found to have a differing perception of health-

related quality of life impact compared to their parent’s perception, with parents reporting a

greater impact of the condition relative to their affected children, prior to a convergence of

agreement subsequent to symptom treatment. 29 It is recognized, however, that such findings

could also be influenced by the fact that CA is indeed an intermittent condition. 29

2.2 PATHOPHYSIOLOGY

2.2.1 Anatomy of the developing calcaneus

The calcaneus is the largest tarsal bone of the foot and is positioned at the most plantar-

posterior aspect of the hindfoot (FIGURE. 2.1 & 2.2). 9 This bone articulates superiorly with

the talus at the subtalar joint, and distally with the cuboid to constitute a segment of the

midtarsal joint. 9 The calcaneus acts as an attachment for a number of tendons, ligaments and

muscles including: the insertion point for the gastrocnemius, soleus and plantaris musculature

via the Achilles tendon; the origin of the intrinsic plantar foot muscles including abductor

hallucis, flexor digitorum brevis, quadratus plantae, abductor digiti minimi, extensor

digitorum brevis and the plantar fascia as well as the dorsally located extensor hallucis brevis

muscle. 30 The ligamentous attachment sites include: calcaneofibular ligament (laterally),

calcaneocuboid ligament (inferiorly), cervical ligament, talocalcaneal interosseous ligament,

lateral, intermediate, and medial roots of the inferior extensor retinaculum (superiorly), and

plantar calcaneonavicular ligament (anteriorly). 9, 30 The Achilles tendon and plantar fascia

insert into the distal-posterior and plantar-medial prominences of the calcaneus, respectively.

30 In children, the ossification of the calcaneus primarily occurs at two centres, the body and

the apophysis which are separated by the physis. 31 The calcaneal apophysis is located

proximal to the interface of the physis and possesses its own, slower-growing growth plate,

separate from the physeal plate. 3, 13 The calcaneal apophysis, a secondary osseous growth

center, develops in children between the ages of 5-15 years, usually fusing with the calcaneal

body at approximately 13 years in females and 15 years in males. 31-34 Hence, the calcaneal

physis and apophysis are situated in regions of high stress and are primarily influenced by

loading in the Achilles tendon and plantar fascia alike. 22

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FIGURE 2.1 Anatomical margins of the hindfoot in children.

FIGURE 2.2. Radiographic representation of the paediatric calcaneus.

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2.3 SIGNS AND SYMPTOMS

Literature has suggested that a typical clinical presentation of CA usually encompasses a

physically-active 10-12 year old male presenting at the commencement of a sporting season.

14, 23, 25, 35 Additionally, it is reportedly more common in boys with a 2-3:1, male:female ratio,

36, 37 and is frequently associated with running and jumping in sports, such as soccer, which

are noted to produce the highest levels of pain experienced by these children. 33 As the

majority of the aforementioned studies have reported from sports medicine clinical settings,

such findings could also potentially reflect participant bias and must therefore be considered

with due caution. Symptoms are believed to coincide with periods of growth and increased

physical activity, and upon clinical examination patients will often report non-radiating pain

involving apophyseal margins of the calcaneus or regional tenderness at the distal Achilles

tendon. 23, 25, 35 The natural progression of symptoms generally lasts for longer than 8 weeks.

38, 39 Additionally, it is often clinically reported that children display limited ankle joint

dorsiflexion range of motion and/or an accompanying biomechanical foot malalignment of

variable nature; a limp may also be present in symptomatic children following exercise. 1, 14-

16, 23, 33, 35, 40-42 The pain experienced often limits the child’s physical capabilities and may

subsequently interfere with activities of daily living in young athletes. 17 These clinical traits

have mainly arisen from previous authors’ observational surmise, or largely from data that

has involved multiple practitioners’ assessments and retrospective analysis of clinical notes. 1,

15, 16, 33 The methods utilized to measure and classify such traits often have not been described

in detail, nor has broader comment been drawn towards the reliability or validity of the

specific methods adopted to quantify ankle joint dorsiflexion range measurement or foot

posture data. 7 A more rigorous and robust evaluation of the clinical traits associated with CA

may further assist the scrutiny and understanding of the aetiologies and consequences related

to this injury.

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2.4 DIAGNOSTIC CLINICAL INVESTIGATIONS

The most well-described clinical test used to diagnose CA involves manual, medial-lateral

compression of the posterior calcaneus at the growth plate margin, and is commonly referred

to as the ‘squeeze test’. 5 43 A positive test is characterized by pain over the growth plate, but

can also elicit symptoms from the metaphyseal region. Additional positive clinical findings

include: (1) tenderness on palpation coursing the medial tubercle of the calcaneum (thought

to represent inflammation due to tractional forces at the plantar fascia), and (2) replication of

symptoms during barefoot one-legged heel standing. A functional variation of the palpation

test, heel standing is thought to increase force in the Achilles tendon and also heighten

pressure at the plantar calcaneus similar to that experienced during heel strike. 33, 44, 45 In a

study of 45 children attending a sports medicine clinic, 30 with heel pain (case group) and 15

without (control group), Perhamre et al. 5 reported that the sensitivity for one-leg heel

standing was 100%, 97% for the squeeze test, and 80% for the palpation test compared to a

diagnosis identified from the participants history. 5 The pain during these three tests

reportedly correlated ‘well’ with the self-reported ‘pain’ produced in the patients’ specific

sports activities, however pain was not quantifiably defined. Although the three clinical tests

all showed 100% specificity, it is acknowledged that there is a need to validate a ‘gold

standard’ to which these clinical tests can be compared. 5

Throughout the literature the use of medical imaging approaches, such as radiography, as aids

in the diagnosis of CA is controversial. Previously, the diagnosis of CA has been partly based

on radiographic findings involving the calcaneal apophysis. 5 Sclerosis and fragmentation of

the apophysis have been thought to represent signs of inflammation. 5 Accordingly, some

imaging studies have shown reductions in radiographic bone density and increases in

magnetic resonance imaging (MRI) signal intensity as characteristic features of apophysitis. 3,

46, 47 However, these changes have also been commonly observed in children without heel

pain; 48 leading many authors to caution against the use of imaging in the diagnosis of the

condition. 40, 48, 49 Although advanced imaging techniques, such as MRI or computed

tomography (CT), may be useful in ruling out conditions that mimic CA, including calcaneal

stress fracture, neoplasm, bone cyst or the presence of foreign bodies, 16, 34, 40, 50-52 such

abnormalities are uncommon and reportedly occur in as little as 1-4% of cases. 49, 52

The controversy regarding the radiographic appearance of apophyseal fragmentation in

symptomatic and asymptomatic children continues. The majority of authors believe that

osseous apophyseal fissures are normal findings and do not reflect pathologic changes due to

heel pain. 3, 53 Conversely, Volpon and de Carvalho Filho showed that there was a difference

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in the amount of fragmentation between symptomatic boys and a control group following

their assessment of lateral radiographs of the respective cohorts. 46 However, the number of

apophyseal fragments that are considered normal or abnormal is unclear.54 Ethnicity,

hormonal changes, hyperemia and trauma have been suggested to affect normal development

and imaging interpretation of the calcaneal apophysis but awaits scientific confirmation. 48, 55

Furthermore, some investigators claim that fragmentation is a normal physiological process

that takes place during calcaneal growth and does not truly reflect a pathological condition. 54

It would appear, therefore, that radiologic identification of CA in the absence of clinical

information is inconclusive. 54 Moreover, the inter-observer and intra-observer reliability of

diagnosing CA using the radiographic criteria of increased sclerosis and fragmentation has

previously been questioned by authors, with interpretation of fragmentation ultimately

deemed subjective. 54 Hence, radiographic findings that consistently assist the diagnosis of

CA remain elusive, 9 leading many authors to conclude that radiography is not necessary in

CA. 49, 52, 54

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2.5 AETIOLOGY

The dominant theory regarding the aetiology of CA is that it represents a mechanical overuse

injury, subsequent to repetitive microtrauma at the apophysis, followed by inflammation. 2, 20,

23, 40, 56-58 Repetitive tensile, compressive or shear stress is thought to increase micromotion

between the apophysis and calcaneal body, resulting in micro-damage and inflammation of

the chondral bone plate (FIGURE 2.3). This micromotion has specifically been attributed to

traction within the Achilles tendon or alternatively repetitive loading associated with heel

strike amid periods of heightened physical activity and rapid growth. 1, 2 The calcaneal

apophysis is believed to be susceptible to injury due to the rapid proliferation of chondrocytes

in growth centers that results in a point of mechanical weakness. This weakness is promoted

by a mismatch in bone mineralization relative to bone growth during pubescent development,

rendering the bone temporarily more porous and prone to injury. 59, 60

It is believed that excessive tensile, compressive or shear force at the apophysis arises from

the Achilles tendon and opposing plantar fascia and plantar intrinsic foot musculature

secondary to either an overactive or short triceps surae-Achilles tendon muscle complex; 23, 33,

61 or the influence of biomechanical foot malalignment. 1, 9, 11, 13-16 (FIGURE 2.3). In contrast,

the magnitude and rise in vertical ground reaction force during heel strike have also been

suggested to cause direct microtrauma to the apophysis resulting in CA, and in severe cases

has been reported to lead to calcaneal stress fracture 3 (FIGURE 2.3). In support of such a

concept, higher plantar pressures beneath the heel have been reported during stance and

walking in children with CA when compared to those without heel pain. 17, 27 However, the

relevance of elevated plantar pressures under static loading is not clear, especially as the

condition has been clinically linked with more ballistic activities such as running and

jumping in high impact sports..33 Whether vertical ground reaction forces associated with

running are elevated in children with CA has not been evaluated.

There are several risk factors proposed to be associated with CA. These risk factors have

been summarized in Table 2.1 and may be classified as intrinsic or extrinsic.

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FIGURE 2.3. Tensional and impact force in calcaneal apophysitis.

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Table 2.1. Proposed intrinsic and extrinsic risk factors reported in CA.

Intrinsic Extrinsic

Triceps surae muscle-tendon unit tightness 3, 25, 62 Trauma (indirect) 1, 15, 63, 64

Ankle equinus 7, 17, 19, 23, 27, 35, 40, 42 Improper footwear 65

Biomechanical foot mal-alignment 7, 19, 40, 66 Surface properties 65, 66

Overweight 7, 19, 66 High activity level 7, 65, 66

High subcalcaneal plantar pressures 17, 27

2.5.1 Triceps surae muscle-tendon unit tightness

Triceps surae muscle-tendon unit tightness is thought to heighten tension in the Achilles

tendon, resulting in traction and microdamage of the apophysis. 3, 25, 62 Liberson et al 22

examined the calcaneal apophysis of 35 children with CA and 52 children without heel pain

using histology (FIGURE 2.4), radiography and CT. They reported fibrous bands in the

cartilage that were oriented perpendicular to the plane of the physis. The authors suggested

the bands reflected the orientation of stress in the tissue, consistent with biomechanical theory

relating bending or compression under repetitive stresses of either traction and/or ground

reaction force during heel strike. 1, 22, 23, 67, 68 Although poorly understood, pain is thought to

reflect an inability of the tissue to withstand these stresses, resulting in an increased rate of

re-modelling of the tissue. It has been hypothesized that children encountering growth spurts

may experience a significant imbalance in the ratio of muscle-tendon unit length to bone

length about the ankle leading to the development of CA. 2, 13, 35 Essentially, the relatively

shortened muscle-tendon unit is thought to place greater traction at the insertion to the

apophysis. 3 To date however, there are no published studies providing empirical evidence

demonstrating altered tendon load in children with CA.

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FIGURE 2.4. Illustration of histological section of the physis. Separation of bony trabeculae

of the calcaneal apophysis by un-calcified cartilage. Reproduced from: Liberson A, Lieberson

S, Mendes DG, Shajrawi I, Haim YB, Boss JH. Remodeling of the calcaneus apophysis in the

growing child. Journal of Pediatric Orthopaedics B. 1995;4(1):74-79 with permission. 22

Fibrocartilage

Hyaline cartilage

Bone trabeculae

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2.5.2 Reduced ankle joint dorsiflexion/equinus

A relatively shortened triceps surae muscle-tendon unit is considered to place greater traction

on the apophysis at the insertional margin, 3 and is believed to contribute to reductions in

ankle joint dorsiflexion range of motion, or so called “ankle equinus”. 69 According to Root et

al., 70 ankle equinus represents insufficient ankle joint dorsiflexion for normal gait and results

in lower extremity compensation, pathology or a combination of both. Clinical literature

generally suggests that normal gait requires greater than 10 degrees of ankle dorsiflexion

(measured statically) with the knee extended. 69-71 In adults, ankle equinus has been clinically

associated with many foot and ankle pathologies including: plantar fasciitis, hallux abducto-

valgus, Achilles tendinopathy, Charcot’s midfoot collapse, and diabetic ulcerations. 72 In the

absence of bony deformity, neurologic abnormality or spastic conditions; ankle equinus is

thought to be a key clinical indicator of calf tightness in children, and by implication

increased tension on the calcaneal apophysis. 3, 62 As ankle equinus may also be a common

entity within asymptomatic individuals, 73 further investigation into ankle joint range of

movement could provide greater insight as to whether this factor affects children suffering

CA.

The theory that ankle equinus is linked to CA is supported by a clinical investigation

performed by Szames et al, 42 which evaluated 79 cases of CA in 53 patients. The research

found that 82% of the children with CA possessed an ankle equinus due to muscular

tightness. Although insightful, the study did not provide specific details on how

measurements were conducted or graded, and multiple raters (of unknown experience) were

involved in data collection without mention of a reliability assessment. Unfortunately, these

issues are consistently evident across the literature related to CA. 23, 40, 42 Accordingly, many

previous studies investigating ankle joint dorsiflexion in children with CA have involved

varied measuring formats (i.e non- weightbearing instrumented, non- weightbearing

goniometric supine, weightbearing lunge) for quantifying foot dorsiflexion on the leg,

possibly influencing the accuracy of results. 7, 17, 19, 27 Only one of these studies has mentioned

the application of a defined moment (torque) when measuring ankle range to objectify the

examination technique7, 74 (TABLE 2.2.). Other factors complicating the accuracy of ankle

dorsiflexion measurement may include instrumentation positioning, uncontrolled motion of

the subtalar joint, midfoot deformity, incomplete relaxation of ankle plantarflexor muscles

during testing or pain response of symptomatic subjects, and locating specific reproducible

anatomical landmarks on the foot/leg when coordinating measurements. 75-79 Additionally,

the relationship between static and dynamic ankle joint dorsiflexion measurement and ankle

motion during gait appears questionable, with previous research finding no correlations

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between the respective measurement formats. 80, 81 Furthermore, interpretation of static ankle

joint measurements in this specific instance must be given due diligence, considering that CA

has been previously associated with dynamic activities. 33 Notably, previous research has

reported greater ankle dorsiflexion in children with CA as measured by the weight-bearing

‘lunge’ test. 19, 82 However, as the lunge test does not reflect the magnitude of ankle

dorsiflexion during dynamic activity, 81 and CA is common in children that run and jump, 33

the clinical significance of such a finding is not clear.

2.5.3 Biomechanical foot mal-alignment

Biomechanical mal-alignment of the foot is commonly, though anecdotally, linked with CA.9

It is widely asserted that a ‘pronated’ foot type elongates the medial longitudinal arch,

placing a stretch on the plantar fascia and Achilles tendon. 1, 15, 16 This is thought to result in

an imbalance in tension between the Achilles tendon and plantar fascia/plantar intrinsic foot

musculature resulting in potential shearing at the Achilles tendinous-apophyseal margin. 1, 15,

16 Although unsubstantiated by empirical evidence, 83 it has also been suggested that a

‘pronated’ foot type may also contribute to over activity of the gastrocnemius-soleal complex

(net inverter muscles) in order to stabilize the talocrural (ankle) joint and resist the eversion

of the calcaneus. 84 Again, over-activity of the gastrocnemius-soleal complex would

theoretically increase tension in the Achilles tendon and subsequent traction at the calcaneal

apophysis. 84 Additionally, a ‘pronated’ foot type is thought to result in greater foot mobility,

85 and clinical treatment of this condition is often focused on reducing foot motion by means

of padding, strapping and/or foot orthoses. 9, 19, 25, 42, 86 Indeed, Sever in 1912 1 comments on

both foot motion and pronation in these children, yet despite being implicated for over 100

years, no studies to our knowledge have investigated foot mobility in children with and

without CA.

As summarized in Table 2.3, the more recently published works of Scharfbillig et al., 7 James

et al.; 19 and Sartorelli et al.; 66 are the few studies in the literature to date that have provided

evidence of biomechanical foot alignment measurement.87, 88 The three studies all utilized

versions of the Foot Posture Index 87 to assess clinical foot alignment in children of relevant

age with CA. James et al. 19 reported that static weight bearing foot posture was more

pronated (mean Foot Posture Index-6 score 4.43 ± 2.72) in children suffering CA compared

to normative values (mean Foot Posture Index-6 score 3.74 ± 2.34). However, contrary to

these findings, Sartorelli et al. 66 in a large population-based cohort, found no difference in

Foot Posture Index (unspecified version) 87 values of children with and without CA. While

the specific Foot Posture Index version and derived values were not disclosed for

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interpretation, the authors concluded that a pronated foot posture as determined by the Foot

Posture Index (unspecified version) should not be considered a risk factor for the condition.

Although Scharfbillig et al. 7 noted that forefoot frontal plane position bilaterally (as per

traditional foot measurements adopted by Podiatrists) was significantly greater in non-planar

(varus and valgus) magnitude for children suffering CA, suggesting a possible link between

forefoot malalignment and the condition, they also found no significant between-group

differences in Foot Posture Index-8 in the study. It must be highlighted that there is an

inability to validate segments of the eight item Foot Posture Index scale. 89 The original

authors recommend use of the six item Foot Posture Index tool 90 in replacement of the eight

item scale, and hence due diligence must be taken when contrasting results from the differing

versions. Notably, Scharfbillig et al. 7 report a lack of consistency on the scoring algorithm of

the Foot Posture Index for measuring all types of feet, questioning the tool’s overall clinical

applicability. Nonetheless, the variation in results from these aforementioned studies

highlight the need to interpret this purported risk factor with caution; and ultimately indicate

a need for further research.

Whilst passive static clinical measures of foot structure, such as the Foot Posture Index, may

not reflect foot function during dynamic activity, 91 clinical static tests of foot mobility and

stiffness allow for quantification of the effect of loading, albeit quasistatic, on foot structure

and are considered clinically important with respect to the predisposition of lower limb

musculoskeletal injuries. 92, 93 Although the relationship between foot mobility and dynamic

foot function during gait in adults is controversial, 91 relatively little is known about foot

mobility and stiffness in children, and the usefulness of these measurements in predicting

injuries in paediatric populations. Furthermore, there appears a need to investigate measures

of foot mobility and stiffness in children as foot motion is thought to be clinically implicated

in the development of injury, such as CA 1.

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Table 2.2. Ankle joint (AJ) dorsiflexion (DF) in children with calcaneal apophysitis.

Reference Study Design Diagnosis Sample Size Age (years) AJ DF measure Findings

Micheli et al. 1987 23 Retrospective Squeeze Test 62 cases 11.6 # Unspecified Mean peak AJ DF on cases affected limbs ≈ 5°

Krantz, 1965 40 Retrospective Uncomfirmed 36 cases; 64 controls 6-13 Unspecified Non-quantitative commentary - generally limited ankle flexion in cases

Szames et al. 1990 42 Retrospective Uncomfirmed 53 cases 11# Unspecified Non-quantitative commentary - ankle equinus in 82% of cases due to muscular tightness

Scharfbillig et al. 2011 7 Case Control Squeeze Test 67 cases; 236 controls 10.9 ± 1.5 Modified Lidcombe Cases Left 11.0°* (5.7) Right 11.9° (5.9); Controls Left 12.8° (5.7) Right 13.2° (5.8)

Becerro et al. 2011 27 Case Control Squeeze Test 22 cases; 24 controls 10.5 ± 0.8 Clinical Goniometry Less AJ DF in cases*; Nb - quantitative ° value undisclosed

Becerro et al. 2014 17 Case Control Squeeze Test 28 cases; 28 controls 10.8 ± 1.5 Clinical Goniometry Cases 6.9°* (1.0); Controls 17.7° (1.95)

James et al. 2015 19 Cross-sectional Squeeze Test 124 cases 10.9 ± 1.5 Lunge test Cases 28.8°* (4.3); Pop. norm 25.4° (8.5)

# no SD reported; *Indicates a statistically significant difference between children with and without CA (P < .05)

Table 2.3. Foot alignment in children with calcaneal apophysitis.

Reference Study Design Diagnosis Sample Size Age (years) Foot measure Findings

Krantz, 1965 40 Retrospective Uncomfirmed 36 cases; 64 controls 6-13 Roentgenologic General commentary - 'medium to high' arches in cases (i.e calcaneal pitch > 20°)

James et al. 2015 19 Cross-sectional Squeeze Test 124 measured cases 10.9 ± 1.5 FPI 6 point scale Cases 4.4* (2.7); Pop. norm 3.7 (2.3)

Sartorelli et al. 2017 66 Population Cohort Squeeze Test 430 athletic children 6-14 FPI (unspecified version) General commentary - FPI should not be considered a risk factor

Scharfbillig et al. 2011 7 Case Control Squeeze Test 67 cases; 236 controls 10.9 ± 1.5 Traditional measures; FPI-8 Forefoot angle - Cases Left 5.5°* (1.7) Right 5.5°* (1.7); Controls Left 4.3° (2.2) Right 4.3° (2.2)

FPI - Cases Left 5.8 (4.1) Right 5.8 (4.2); Controls Left 5.8 (3.95) Right 6.0 (4.0)

*Indicates a statistically significant difference between children with and without CA (P < .05)

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2.5.4 Trauma (indirect/extrinsic)

Authors have anecdotally acknowledged that varied causes of foot and ankle trauma that

result in a direct impact to the calcaneal apophysis may precede CA symptoms. It is believed

that such trauma can induce heightened shear and compressive stress upon the calcaneal

apophysis with such associated injury. 1, 15, 63, 64

2.5.5 Infection

Infection is noted to be an uncommon risk factor for CA and may be loosely considered to

weaken the physeal area. However, it must be highlighted that authors usually refer to

infective inflammation as a differential diagnosis to be considered during clinical assessment,

rather than a causative factor. 13, 23, 33, 41, 42

2.5.6 Body Mass Index influence

While several studies have drawn comment that CA commonly occurs in ‘overweight’

children, many of these studies do not detail how weight-status was classified or limits to

which it was controlled in matched healthy children. 1, 63, 94, 95 Although speculative, it has

been suggested that excess body weight could increase tension on the calcaneal apophysis as

the gastrocnemius-soleal complex may exert more force to lift a greater body mass, or

alternatively greater body mass may increase peak ground reaction force during heel-toe

walking and running. 9 A higher body mass is also associated with greater Achilles tendon

stiffness, 96 which is important considering that heightened Achilles tendon stiffness has been

implicated in CA. 18 Additionally, ‘overweight’ and obesity has been associated with low-

grade chronic systemic inflammation, 97-101 and CA has been classified as an inflammatory

disorder in the past. 1 In their population based cohort study of 430 athletic children,

Sartorelli et al 66 found that Body Mass Index (BMI) was not associated with an increased

risk, but rather the prevalence was heightened in younger children (TABLE 2.4). Contrary to

this, a recent cross-sectional study by James et al 19 demonstrated that children with CA were

more likely to have a greater BMI, increased weight, greater waist circumference, and

increased height than that of normative values derived from healthy children in the general

population. However, it is not clear as to whether children with CA in this study had a high

BMI prior-to or post-development of CA. It could be considered logical to suggest that

children with a high body mass/weight possess higher peak ground reaction forces during

activity, which may lead to the development of CA. Contrary to this, it may also be feasible

that the pain caused by CA results in inactivity of the child and subsequent weight gain.

Additionally, an increased BMI could simply be linked to hormonal and endocrine changes,

or purely reflects lower physical activity. 102

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Interestingly, Scharfbillig et al 7 acknowledged that BMI should be interpreted with caution

in children of this age, secondary to children being prone to large changes in weight and

height nearing the onset of puberty. The authors argued that, these anthropometric values

may not accurately reflect the weight and height of the individual at the exact time at which

the injury occurred prior to clinical and research assessment. 103 Additionally, these

anthropometric measures may not accurately reflect body composition or adiposity. Although

Scharfbillig et al 7 found no statistically significant between-group differences in BMI in their

case control study, comparison of their reported BMI data against published thresholds for

overweight adjusted for age, 104 suggested that children in their research suffering from CA

were overweight or near close to it. However, this may also reflect a sampling bias, and

hence the results should be interpreted with caution.

2.5.7 High vertical ground reaction forces at the apophysis

Vertical ground reaction forces or increased plantar pressures at the calcaneal area may cause

repetitive microtrauma to the apophysis during the heel strike phase of gait.3, 17 In a series of

case-control studies, Becerro et al. observed that children with CA have higher maximum

peak plantar pressure (kPa) beneath the heel during standing (CA cases 339 ± 27 vs healthy

controls 83 ± 2) and self-selected speed walking (CA cases 880 ± 78; healthy controls 88 ±

112). 17, 27 Relative to other previous research that has reported peak plantar pressures at the

heels (≈ 230-270 kPa) of healthy children of similar age (7-11 years) during barefoot level

walking at self-selected speeds, 105 interestingly, the healthy control participants in their work

appeared to have exceedingly low plantar pressure values beneath the heel. Caution may be

required when interpreting these results. Additionally, a limitation of this work was that

despite gait velocity being self-selected, no between-group comparison of walking speed was

described. 17 Moreover, although these authors evaluated children with CA under static

conditions and walking, CA has been clinically linked with more ballistic activities such as

running and jumping in high impact sports, 33 and vertical loading during running is yet to be

investigated in these children.

Animal studies have suggested that if external loading rates are not moderated sufficiently,

then tissue damage may occur. 106, 107 In a study encompassing 14 symptomatic children with

recalcitrant heel pain unresponsive to treatment, Ogden et al. 3 found traumatic stress fracture

of the immature trabecular bone of the calcaneus when visualized with MRI. It was noted that

increased signal intensity evident in the secondary ossification center effectively remained

unchanged after resolution of contiguous metaphyseal bone bruising. These authors

furthermore suggested that repeated and intense impact forces may be responsible for the

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damage to trabecular bone. 3 However, no diagnostic criteria for the condition is described in

this study, and there is a lack of descriptive thoroughness regarding bony bruising in the

metaphysis. Additionally, increase signal on fluid sensitive sequences, in either the

metaphysis equivalent of the posterior calcaneus or the secondary ossification centers have

also been commonly observed in children without heel pain; 48 leading many authors to

caution against the use of imaging in the diagnosis and interpretation of the condition. 48, 49

2.5.8 Footwear, surface properties and activity levels

Clemow et al. 65 anecdotally suggested that children most susceptible to CA are usually

highly active, wear poorly fitting footwear and run frequently on hard surfaces. Interestingly,

football has been found to be one of the more common sports played by children suffering

this condition. 11, 14, 23, 25, 35, 41, 84 While running is a key component of football, and has also

been anecdotally linked to CA, football boots typically offer minimal heel elevation and are

thought to place greater load on the Achilles tendon than traditional running shoes. 84

Accordingly, through freeze-frame video analysis and F-Scan pressure testing (Tekscan INC.,

Boston MA), Walter and Ng 108 found that compared to non-cleated shoes, studded soccer

boots placed children’s feet in a dorsiflexed position during full foot contact at stance phase

of gait whilst running. It was purported that this positioning increased the amount of tension

within the Achilles tendon and also elevated average rearfoot plantar pressure by ≈ 276 kPa

compared to the non-cleated shoes.

Contrary to previous authors, 1, 11, 14, 25, 35, 63, 109 Scharfbillig et al 7 did not identify self-

reported exercise duration as a risk factor for CA in their prospective case-control study.

Rather the authors suggested that earlier studies may have overstated this aspect of the risk

factor profile, secondary to patient recruitment being sought from dedicated sporting clinics

and a lack of controlled comparison group from the same population. Interestingly, Sartorelli

et al 66 found the onset of the condition to be more frequent in athletic children who self-

reported lower-levels of physical activity, and identified no association of symptoms with

sex, type of terrain, or sport when measured via a bespoke questionnaire.

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Table 2.4. BMI measurement in children with calcaneal apophysitis.

Reference Study Design Age Diagnosis Sample Size Findings

Sartorelli et al. 2017 66 Population based Cohort 6-14^ Squeeze Test 430 athletic children General commentary - BMI should not be considered a risk factor

James et al. 2015 19 Cross-sectional 10.8 ± 1.5 Squeeze Test 124 cases Cases 19.3* (3.1); Pop. norm 18.3 (3.4)

Scharfbillig et al. 2011 7 Case Control 10.9 ± 1.5 Squeeze Test 67 cases; 236 controls Cases 19.8 (3.0); Controls 19.4 (3.8)

^ Only range reported. *Indicates a statistically significant difference between children with and without CA (P < .05)

Table 2.5. Summary of studies described encompassing treatment in children with calcaneal apophysitis.

Reference Study Design Diagnosis Sample Size Treatments Outcome measures

Micheli, 1987 23 Retrospective Squeeze Test 85 Stretch & strength; Heel lifts; Orthoses Unspecified pain-response rating: Return to sport

Wooten, 1990 110 Case series Squeeze Test 5 Ice; Stretch; Padding; Oral anti-inflammatory drugs Ordinal pain scale; ROM; Strength (p-values)

Kvist, 1991 25 Retrospective Squeeze Test 67 Rest; Ice; Stretch; Heel lifts; Orthoses; Massage Unspecified pain scale & Activity capability rating

Leri, 2004 111 Case report Squeeze Test 1 Rest; Ice; Stretch; Mobilisation Unspecified pain-response rating

White, 2006 112 Case report Squeeze Test 1 Rest; Ice; Stretch; Heel lifts; NSAIDS; Heat; Mobilisation Unspecified VAS; Lower extremity functional screen; Strength; ROM

Hunt, 2007 62 Case series Squeeze Test 11 Taping Ordinal pain scale (p-values)

Perhamre, 2012 84 Randomized Trial Squeeze Test 30 Orthoses Borg CR-10 Pain; Engstrom's activity index (p-values)

Perhamre, 2011 113 Randomized Trial Squeeze Test 51 Heel wedge; Orthoses Borg CR-10 Pain; Engstrom's activity index (p-values)

Perhamre, 2011 24 Randomized Trial Squeeze Test 35 Heel wedge; Orthoses Borg CR-10 Pain (p-values & IQR)

James, 2016 114 Randomized Trial Squeeze Test 124 Orthoses; Heel lifts; Footwear Oxford ankle foot questionnaire; Faces pain scale; Lunge test (p-values)

Wiegerinck, 2015 115 Randomized Trial Squeeze Test 98 Heel lifts; Eccentric exercises; Rest Face pain scale; Oxford ankle foot questionnaire (p-values)

Kuyucu, 2017 116 Randomized Trial Undetailed clinical exam; Radiological 22 Taping American Orthopaedic Foot and Ankle Society scores; VAS (p-values)

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2.6 DIFFERENTIAL DIAGNOSES

Plausible differential diagnoses of CA for clinical consideration are listed in Table 2.6.

Table 2.6. Differential diagnoses of calcaneal apophysitis.

Intrinsic

Achillobursitis 1, 23, 25 Foreign bodies 117

Retrocalcaneal exostosis or bursitis 23, 25, 33

Plantar fasciitis 1, 15, 23, 25

Entrapment inferior calcaneal nerve 118

Ruptures tendon or ligaments 23, 25, 33, 119

Tuberculosis 1, 15 Fractures and stress fractures 23, 25, 33

Rheumatoid arthritis 23, 25, 41 Tarsal tunnel syndrome 23, 25, 33

Cysts and tumors 23, 25, 119

Osteomyelitis 23, 25, 41

Contusions 23, 25, 33

Tarsal coalition. 23, 33, 119

In these situations, a thorough subjective history and clinical assessment of the injury,

location of pain, type/description of pain, changes/pattern of symptoms over time will usually

aid pathological differentiation alongside subsequent referral for radiological evaluation by

practitioners if deemed necessary. 52 Whilst each condition may produce heel pain in

adolescents, the symptom patterns differ to that of CA. 9 Although there are many possible

confounding diagnoses for paediatric heel pain, there are none that specifically mimic the

positive squeeze test of CA without a wider spectrum of symptoms. Thus, the diagnosis of

CA is one that may be achieved with relative clarity once other possible differential

diagnoses are excluded. 9

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2.7 DESCRIPTION OF MANAGEMENT

To date the recommended treatment regimen for CA is highly variable and based largely on

anecdote. The range of interventions discussed and advocated within the literature typically

includes: modified rest or cessation of sport, heel lifts, foot orthoses, footwear modification

or replacements, triceps surae and plantar fascial stretching, extensor muscle strengthening,

night splints, calcaneal padding or strapping mechanisms, therapeutic ultrasound, non-

steroidal anti-inflammatory drugs, icing, steroid injections, immobilization casting or

crutches, and surgical removal of the calcaneal apophysis itself. 9, 27 The broad range of

treatment interventions used in the management of CA are not guided by a definitive

understanding of the causative mechanisms. A greater understanding of the mechanism of

injury of this condition would help to direct clinical and future research approaches toward

preventative measures, diagnostic aids and management protocols.

To the best of the author’s knowledge, Leeb et al. performed the first qualitative systematic

review of the literature encompassing treatment options for patients with CA. 120 The review

article included 29 studies published between 2008-2011, following the last literature review

detailing CA by Scharfbillig et al. 9 Articles included in the analysis were related to

radiographic diagnosis and treatment of the condition, and predominately involved case

studies or case-series. Despite the use of multiple treatment plans, the authors conclude that

there appears to be no gold standard diagnostic criteria or treatment algorithm for best

practice. Moreover the authors recommended that further evaluation of plausible treatment

methods was required due to a lack of randomized clinical trials. 120 This may be viewed as

debatable, considering the underlying mechanisms for the injury remain unclear and

randomized clinical trials should be informed by mechanistic studies. 121 Since then, a more

focused systematic review has been performed by James et al. 122 assessing the treatment

options for CA as quantified by the outcome measures of pain reduction and maintenance of

physical activity. Nine articles fit the inclusion criteria for their systematic review, which

included three randomized control trials, two retrospective case reviews, and two case

reports. The authors concluded that although many treatment options are reported in the

literature, few are examined against a control group or alternate treatment option.

Additionally, there was limited evidence to support the use of heel raises and foot orthoses in

children suffering heel pain related to CA. Kuyucu et al.116 provided the first prospective

randomized trial on the efficacy of kinesio taping in CA, and concluded that kinesio taping

may be utilized effectively for the restoration of ankle function of athletes with CA, but its

role in pain management was equivocal (TABLE 2.5).

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As there is minimal literature analyzing the cause or mechanism underlying this injury, it is

not surprising to find a variety of treatment approaches prescribed within the literature. The

literature advocates treatments that are thought to unload the Achilles tendon and reduce

loading beneath the heel, usually by means of padding, strapping, heel lifts or foot orthoses. 6,

9, 19, 25, 39, 42, 86 Other authors emphasize the significance of accommodating foot mal-

alignment as another main treatment strategy. 33, 42 To date, however, “best practice”

management plans are lacking. Furthermore, the efficacy of treatment options such as taping,

heel lifts and orthotics are based on the clinical assumption that CA is the result of either

increased traction at the calcaneal apophysis from the Achilles tendon or from increased load

at the plantar surface of the heel, which have not been rigorously tested. 122, 123

More recent studies performed by James et al. 114 and Wiegerinck et al. 115 have indicated that

various treatments for CA may produce modest short-term improvements in pain scores of

symptomatic children. Namely, as evidenced in a 12-month factorial randomized comparative

effectiveness trial, heel raises and prefabricated foot orthoses have been shown to improve

pain scores and dysfunction in the initial stage of managing symptoms, where neither a main

effect of footwear nor a shoe insert by footwear interaction was apparent. 114 Although, foot

orthoses appear to offer no additional benefit over simple heel lifts for relieving pain

associated with CA over a 3 month duration. 114, 115 Hence, a mechanistic approach to

understanding factors related to CA may aid in identifying appropriate treatments for

symptom relief in CA and remains an area for further research.

2.8 SUMMARY

In summary, a review of the literature has highlighted intrinsic and extrinsic factors thought

to precipitate CA in children. Tension in the Achilles tendon and loading beneath the heel

appear to be commonly proposed mechanisms for CA. Diagnosis is generally made by

clinical examination with no consensus on diagnostic criteria for medical imaging. There is

weak evidence that treatments targeting reduction of stress in the Achilles tendon and impact

forces beneath the heel may be effective in providing symptomatic relief. However, there is a

need for further empirical evidence specifically investigating the purported mechanisms and

associated factors of this condition recapitulated in FIGURE 2.5.

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Intrinsic factors

Extrinsic factors

gggg

Postulated mechanisms

FIGURE 2.5. Flow chart illustrating clinically associated risk factors and postulated mechanisms in calcaneal apophysitis.

Trauma (indirect)

Surface properties

Footwear

Activity levels

Tension

Achilles

Triceps surae tightness

Biomechanical foot malalignment

Ankle joint range of motion

Altered Achilles tendon properties

Body Mass Index

Vertical ground reaction force

Peak plantar pressures

Impact

CA Microdamage

Physis

Pain

Inflammation

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CHAPTER 3 RESEARCH AIMS & RATIONALE

A review of the literature has demonstrated that relatively little is known about

biomechanical factors associated with CA in children. Although foot mobility/stiffness,

vertical ground reaction force, functional Achilles tendon properties and dynamic ankle joint

range of motion have all been anecdotally implicated in CA, 1, 11, 17-19, 84 there is a lack of

scientific evidence supporting their involvement in the condition. This thesis aimed to better

understand whether these factors were associated with CA. The general aim and rationale for

each study are detailed below.

3.1 AIM 1: Identify whether children with CA possess a more mobile and compliant (less

stiff) foot than children without CA.

Tension within the plantar fascia and plantar intrinsic foot musculature is thought to be

influenced by mobility and stiffness of the foot, 124 which in turn has the potential to

influence loading across the calcaneal physis. 3, 20, 22 Hence, foot mobility has been

hypothesized to play an important role in CA. 1 In support of such a concept, a ‘pronated’

foot posture, which is thought to result in a more mobile foot (vertical, medial-lateral and

global foot mobility), 85 has been implicated in the development of CA by some, 19 but not all

studies. 7, 66 Despite foot mobility being implicated in CA by Sever over 100 years ago, 1 to

the best of the authors’ knowledge no published research to date has specifically evaluated

the magnitude of foot mobility and stiffness in children with and without CA. Chapter 4

addressed this aim by evaluating the foot mobility magnitude and quasi-static measures of

foot stiffness in children with and without CA.

3.2 AIM 2: Compare peak vertical ground reaction forces during walking and running in

children with and without CA.

Elevated vertical ground reaction force at heel strike is believed to be clinically associated

with the development of CA. 2, 23, 25 Previous research has shown that CA is characterized by

higher maximum and average peak pressures beneath the symptomatic heel during static

stance and walking. 17, 27 However, CA has been clinically linked with ballistic activities,

such as running and jumping, rather than relatively low-impact activities such as walking. 33

Vertical ground reaction force and plantar pressures during running have yet to be

investigated in this cohort and are of particular importance, as ground reaction forces are

known to be influenced by gait speed. 125, 126 The study detailed in Chapter 6 was designed to

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investigate vertical ground reaction forces and peak plantar pressures during walking and

running in children with and without CA.

3.3 AIM 3: Assess functional properties of the Achilles tendon in children with and without

CA during running.

Micro-damage of the physis is generally considered pathognomonic of CA and, in part, is

clinically thought to reflect a change in the functional properties of the Achilles tendon with

growth. 18, 84 However, evidence that tendon properties may be altered in children with CA is

lacking. While estimates of Achilles tendon properties in children are commonly undertaken

by means of indirect measurement techniques under quasistatic loading conditions, 18, 96

transmission mode ultrasound is emerging as an alternative method for the non-invasive

measurement of tendon properties in vivo during dynamic activities. 127 Axial transmission

velocity of ultrasound in tendon is dependent on its instantaneous elastic modulus (material

stiffness), and proportional to the applied tensile load. 127-129 Evaluation of functional Achilles

tendon properties in CA particularly during more ballistic activities such as running is

important, as they have been clinically implicated in the development of the condition, 33 and

may reveal differences in tendon properties that are not evident with static maximum

voluntary contractions. Chapter 7 outlines the use of transmission-mode ultrasound to assess

the functional properties of the Achilles tendon specifically during running in children with

and without CA. Additionally, the study has also provided valuable insight into potential

differences in dynamic ankle movement between these cohorts.

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CHAPTER 4 FOOT MOBILITY MAGNITUDE AND STIFFNESS IN CHILDREN

WITH AND WITHOUT CALCANEAL APOPHYSITIS

Forming the first part of the experimental phase of this research, this study was designed to

address research aim 1 (Chapter 3) and evaluated the magnitude of foot mobility and stiffness

in children with and without CA. The chapter has been reformatted from the published

article:

McSweeney SC, Reed L, Wearing S: Foot Mobility Magnitude and Stiffness in Children

With and Without Calcaneal Apophysitis. Foot Ankle Int 2018, 39(5):585-590.

Contributions of co-authors:

S. McSweeney: contributed to study conception and design, data collection, data analysis and

interpretation, and preparation of the manuscript.

L. Reed: contributed to study conception and design, data analysis and interpretation, and

preparation of the manuscript.

S. Wearing: contributed to study conception and design, data analysis and interpretation, and

preparation of the manuscript.

The co-authors have certified that:

1. they meet the criteria for authorship in that they have participated in the conception, execution, or

interpretation, of at least that part of the publication in their field of expertise (as described);

2. they take public responsibility for their part of the publication, except for the responsible author who

accepts overall responsibility for the publication;

3. there are no other authors of the publication according to these criteria;

4. potential conflicts of interest have been disclosed to (a) granting bodies, (b) the editor or publisher of

journals, and (c) the head of the responsible academic unit, and

5. they agree to the use of the publication in the student’s thesis and its publication on the QUT’s ePrints site

consistent with any limitations set by publisher requirements.

Simon McSweeney 12 December 2018

Lloyd Reed 12 December 2018

Scott Wearing 12 December 2018

QUT Verified Signature

QUT Verified Signature

QUT Verified Signature

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4.1 ABSTRACT

Background: This study evaluated quasi-static measures of foot mobility magnitude (FMM)

and foot stiffness (FS) in children, aged 8 to 14 years, with and without CA.

Methods: Between 2016 and 2017, FMM and FS measurements were captured on 41

children (22 cases and 19 controls) using a custom-built foot assessment platform. The

platform incorporated a portable force plate which allowed quantification of vertical force

during double limb stance (DLS).

Results: There was no significant difference in FS in children with and without CA (P =

.459). FMM was significantly greater (+19%) in children with CA than in those without (P =

.045). The mean difference in FMM between groups (1.4 mm), however, did not exceed the

minimum detectable change (MDC95%) for the measurement (± 2.5 mm).

Conclusion: Differences in FMM in children with CA were small and within the observed

error of measurement. Clinical measures of FS did not differ in children with and without CA

during quasistatic loading. Further research evaluating the level of uncertainty of the

measurement techniques in children and under dynamic loading conditions is recommended.

Clinical Relevance: These findings question the rationale behind interventions which aim to

modify quasistatic foot mobility and stiffness in children with CA.

Level of Evidence: Level III

Keywords: Sever’s disease; heel pain; paediatric; foot movement.

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4.2 INTRODUCTION

Calcaneal apophysitis (CA) is the most common cause of activity-related heel pain in

growing children, with a reported prevalence of 2-16%.10 Also known as Sever’s disease, the

condition is typically self-limiting in nature but may result in debilitating discomfort of the

secondary growth centre of the calcaneus prior to skeletal maturity.24, 34 The cause of CA is

unknown, but repetitive microtrauma arising from impact pressure, tension, or shear is

thought to damage the chondral plate separating the body of the calcaneus from the

apophysis, resulting in inflammation.15, 26 Heightened tension in the Achilles tendon, which

inserts posteriorly onto the calcaneal apophysis, has often been implicated clinically in the

development of the condition.2, 28 Similarly, tension within the plantar fascia, which

originates near the epiphysis and stabilizes the medial longitudinal arch of the foot has the

potential to influence loading across the chondral plate.15, 19, 26 Foot mobility and stiffness

may, therefore, play an important role in CA. In support of such a concept, a ‘pronated’ foot

posture, which is thought to result in a more mobile foot,8 has been implicated in the

development of CA by some,13 but not all studies.32 Moreover, clinical treatment of this

condition is often aimed at reducing foot motion by means of padding, strapping and/ or foot

orthoses.13, 17, 20, 32, 36 To the best of the authors’ knowledge, however, no published research

to date has evaluated the magnitude of foot mobility and stiffness in children with and

without CA.

The aim of the present study, therefore, was to investigate foot mobility magnitude and

stiffness in children with and without CA under quasistatic loading conditions. It was

hypothesized that children with CA would possess a more mobile and less stiff foot than

healthy age-matched children.

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4.3 METHODS

4.3.1 Participants

Twenty-two consecutive cases of CA and nineteen healthy children without heel pain, aged

8-14 years, were recruited from the greater Brisbane metropolitan area via direct referral from

health-care providers. Data collection was typically aligned with school holiday periods and

took place between March 2016 and July 2016 and; January 2017 through June 2017. Case

participants were primarily recruited prior to those in the control group. The clinical

diagnosis of CA was made from established clinical criteria, including a comprehensive

subjective history and clinical examination, in which symptoms were replicated with medial

and lateral compression of the calcaneal apophysis (squeeze test).13, 25, 27, 38, 39 In all cases,

symptoms were typically provoked by physical activity and had been present for a duration

greater than 8 weeks. The mean (± SD) age, height, and body mass of participants is

displayed in Table 4.1. Of the 22 children with CA, 19 were male and 3 were female. The

right foot was characterized as the most painful limb in 17 cases and the left foot in 5.

Children with CA reported a median pain rating of 5 cm (range, 1-8 cm) on a standard 10-cm

visual analogue pain scale.

Participants in the control group were matched on age, sex and body mass index (BMI), and

free of lower limb pain and pathology (Table 4.1). Exclusion criteria for all participants

included poorly defined irregular calcaneal symptoms, history of fracture, tumour or surgery

of the foot within the last 12 months, overt orthopaedic abnormalities of the foot and lower

limb and a medical history of autoimmune, neurological, vascular, metabolic or endocrine

disorders. Current or past treatment did not influence exclusion criteria. Sample size was

calculated a priori and was based on previously published data reported for healthy adults.23,

41 Participant numbers were sufficient to detect a 10% difference in foot mobility magnitude

(FMM) and foot stiffness (FS) with an ɑ of .05, and β of .20. All participants provided

written informed consent with their accompanying guardians before participation in the

study, which received approval from the university human research ethics committee.

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Table 4.1. Anthropometric data for children with and without calcaneal apophysitis.

Variable Calcaneal Apophysitis Healthy Control t Value P Value d

n 22 19

Age (y) 11 ± 1 10 ± 2 0.51 .613 0.63

Height (cm) 149 ± 10 146 ± 15 0.59 .560 0.24

Body Mass (kg) 41 ± 8 43 ± 14 0.41 .686 0.18

BMI (kg/m2) 18 ± 2 19 ± 4 0.96 .344 0.32

d, Cohen’s effect size statistic; n, sample size

4.3.2 Equipment

Clinical measures of foot mobility and foot stiffness were made using a custom-built foot

assessment platform (Figure 4.1). The platform was similar to that outlined elsewhere,22 but

was modified to incorporate three in-built ruler-gauges and a portable force platform (PS-

2142, PASCO, Roseville, CA). The 37-cm x 37-cm force platform had a full scale of 1100 N,

and a measurement resolution of 0.1N.

Figure 4.1 Custom-built foot platform used to measure foot mobility magnitude and foot

stiffness under quasi-static loading conditions. The platform was mounted on a force

platform.

4.3.3 Protocol

Participants reported to the laboratory wearing lightweight, comfortable clothing. The skin on

the medial, dorsal and lateral aspect of the foot was marked with indelible ink at 50% of the

measured FL during quiet double-limb stance (DLS).22 Foot length (FL), midfoot width

(MFW) and arch-height (AH) were subsequently measured during nonweightbearing (NWB)

and DLS using previously established methods.22 AH was defined as the distance of the

dorsal foot marker to the support surface,21 while MFW was defined as the distance between

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the medial and lateral foot markers.22 FL was defined as the distance from the most posterior

aspect of the calcaneus to the most distal aspect of the longest digit.22 In accordance with

previous research,22 NWB measurements were taken once participants reported ‘first contact’

of their plantar foot with the support surface, and were undertaken with the assistance of a

height-adjustable chair. During DLS participants were requested to stand erect with their feet

positioned approximately 15 cm apart, with an allowance to freely position the non-test limb,

and their bodyweight equally distributed on both limbs. Foot position was consistent with that

described previously for measures of foot mobility in adults,23 with the assumed base of

support comparable to intermalleolar distances previously reported in children of similar

age.37 Vertical ground reaction force was recorded during DLS at a rate of 100Hz. All

measurements were undertaken by a single operator (SCM) and repeated, after approximately

20 minutes, to establish measurement reliability.

4.3.4 Data Reduction and Statistical Analysis

As outlined previously,4 arch height index (AHI), a measure of static foot structure, was

calculated as the ratio of AH to FL. Foot mobility magnitude (FMM) was calculated

according to the equation outlined by McPoil et al. (Eq 1),22 where dAH and dMFW reflect

the change in arch height and midfoot width between DLS and NWB, respectively.

FMM = √dAH2 + dMFW2 (Eq 1)

Foot stiffness (FS) was calculated according to the equation outlined by Zifchock et al. (Eq

2),41 in which dF represents the change in measured force (kgf) between DLS and NWB, and

dAHI represents the corresponding change in arch height index (AHI), the ratio of AH to FL.

FS = dF/dAHI (Eq 2)

Statistical analysis was performed using IBM-SPSS statistical software (Version 21 for

Windows IBM Corp. Armonk, NY, USA). All data were evaluated for normality using the

Shapiro Wilkes test. Student t-tests were used to evaluate potential between-group differences

in body anthropometry (age, height, weight, BMI), AHI, FMM, FS and changes in foot

dimensions with loading (dFL, dMFW, dAH). Effect size was estimated with Cohen’s d

statistic, in which the mean difference between the groups was divided by the pooled

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standard deviation.7 Values of d between 0.2 and 0.5 represent a small effect, between 0.5

and 0.8 a medium effect, and higher than 0.8 a large effect.7 An alpha level of .05 was used

for all tests of significance.

Measurement reliability was assessed using intraclass correlation coefficients (ICC 2,1).35 ICC

values less than 0.20 were considered slight; between 0.21 and 0.40 fair; 0.41 and 0.60

moderate; 0.61 and 0.80 substantial; and almost perfect if greater than 0.80.18 As ICC values

are relative measures of reliability and not directly transferable to different populations,31 the

standard error of measurement (SEM) was also calculated according to the equation: SEM =

SDd/√2 , where SDd represents the standard deviation of difference scores.40 The minimal

detectable change (MDC 95%) was additionally determined according to the equation:

MDC95% = 1.96 × SDd, where 1.96 reflects the z-score associated with the amount of

change required for an observed difference to be considered “true” rather than measurement

error.33, 40

4.4 RESULTS

ICC values for all measures exceeded 0.80. MDC95% values for dFL, dAH, dMFW and

FMM were typically less than 3 mm, while those for dAHI, dF and FS were 0.01, 27N and

357 kgf/AHI units, respectively (Table 4.2).

Table 4.2. Intra-rater reliability (ICC), standard error of the measurement (SEM), and

minimal detectable change (MDC95%) scores (n = 20).

Variable ICC CI95% BIAS SEM MDC95%

dAH (mm) 0.87 0.67-0.95 0 1 2

dMFW (mm) 0.89 0.72-0.95 0 1 2

dFL (mm) 0.96 0.89-0.98 0 0 1

dF (N) 0.98 0.97-0.99 -5 10 27

dAHI 0.84 0.61-0.93 0.00 0.00 0.01

FMM (mm) 0.81 0.52-0.92 0.1 0.9 2.5

FS (kgf/AHI) 0.97 0.93-0.99 36 129 357

As demonstrated in Table 4.3, there was no statistically significant difference in FL, MFW

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and AH in children with and without CA during stance. Similarly, there was no statistically

significant difference in static AHI between groups (t33= 0.416, P = .679, d = 0.000) during

stance (Table 4.3).

Table 4.3. Foot dimensions during double-limb stance.

Variable Calcaneal Apophysitis Healthy Control t Value P Value d

FL (mm) 237 ± 19 228 ± 22 1.49 .144 0.44

AH (mm) 61 ± 5 59 ± 6 1.07 .291 0.36

MFW (mm) 80 ± 7 78 ± 9 0.55 .609 0.25

AHI 0.26 ± 0.02 0.26 ± 0.02 0.41 .679 0.00

d, Cohen’s effect size statistic

There was no statistically significant difference in FS, dFL, dAH, dMFW or dAHI during

loading in children with and without CA (Table 4.4). Children with CA, however, tended to

have a greater reduction in dorsal arch height with loading (40%) than children without heel

pain (t37 = 1.950, P = .058, d = 1.000). FMM was significantly greater (+19%) in children

with CA than in those without (t37 = 2.066, P = .045, d = 0.654). The mean difference in dAH

(2 mm) and FMM (1 mm) between groups, however, did not exceed the MDC95% for either

measurement (Table 4.2).

Table 4.4. Change in foot dimensions, foot mobility magnitude and foot stiffness with

loading.

Variable Calcaneal Apophysitis Healthy Control t Value P Value d

dAH (mm) 7 ± 2 5 ± 2 1.95 .058 1.00

dMFW (mm) 5 ± 2 5 ± 2 0.82 .417 0.00

dFL (mm) 4 ± 2 3 ± 2 0.61 .544 0.50

dF (N) 214 ± 48 213 ± 68 0.03 .978 0.01

dAHI 0.03 ± 0.01 0.03 ± 0.01 1.50 .142 0.00

FMM (mm) 8.7 ± 2.5 7.3 ± 1.7 2.07 .045* 0.65

FS (kgf/AHI) 777 ± 357 893 ± 584 0.75 .459 0.24

d, Cohen’s effect size statistic; *statistically significant difference (P < .05)

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4.5 DISCUSSION

The present study evaluated quasi-static measures of FMM and FS in children with and

without CA. Contrary to our hypothesis, we observed no significant difference in FS in

children with and without CA, suggesting that quasistatic foot stiffness was similar between

groups. Children with apophysitis, in contrast, tended to have a greater reduction in dorsal

arch height (≈ 2 mm) with weightbearing and a significantly greater FMM (≈ 1 mm) than

those without heel pain. Although the differences reflect moderate to large effects according

to Cohen’s convention, they were equal to or less than the minimum detectable change for

each measure (≈ 2 and 3 mm, respectively) and within measurement error. Hence, there was

no meaningful difference in foot mobility or stiffness in children with and without CA. These

findings, therefore, question the rationale behind current treatment interventions, such as foot

orthoses, which aim to modify foot mobility and stiffness in children with CA in order to

relieve symptoms associated with heel pain.13, 17, 36 The finding is also consistent with

previous research which has shown that foot orthoses offer no benefit over simple heel lifts

for relieving pain associated with CA.12

Reliability coefficients (ICC) for FMM and FS in the current study were similar to those

reported previously in adults.22, 30 However, the minimal detectable change (MDC95%) in

dAH and FMM in the current study (2-3 mm) was equal to or greater than mean difference in

these parameters in children with and without heel pain (≈ 2 mm). They were also greater

than the difference in dAH and FMM (≈ 2 mm) reported in adults with and without

patellofemoral pain.23 Hence, the findings of the current study also raise the possibility that

measures of FMM in children may not be sufficiently sensitive to detect small differences in

foot mobility magnitude, such as those reported in adults with knee pain.

It is notable that mean FS scores for children in the current study (830 ± 473 kgf/AHI

units) were consistent with the lower limits of those reported in healthy adults (range,

940 – 2840 kgf/AHI units); suggesting adults may have a stiffer foot structure.41 In

contrast, the mean FMM in children (8 ± 2 mm) was approximately 2-times lower than

that reported previously in adults (≈ 18 mm); suggesting adults have a more mobile foot.22

Although it is possible that adults have more mobile feet than children, it is also

possible that measures of FMM may be subject to scalar, developmental or

maturational factors.6 It is recommended, therefore, that further research be directed

toward identifying factors that influence FMM measurement, and establish the need

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for age- or size-specific norms, before FMM can be routinely used for assessment of

foot mobility.

This study has a number of limitations which should be considered when interpreting the

results. First, FMM and FS were evaluated under quasistatic loading conditions and

may, therefore, not be representative of foot mobility and compliance under dynamic

loading conditions, such as those experienced in running and jumping.3, 9, 11 Second,

clinical measures of FMM and FS, as employed in the current study, undoubtedly reflect a

combination of osseous movement and soft tissue distortion with loading. The relative

contribution of osseous and soft tissue movement to measures of FMM and FS are

unknown, but may be highly variable,14 and presents a new avenue for future

research. Third, standard clinical criteria were used for the diagnosis of CA in this

study. Although these criteria are well established within the literature,5 it is

recognized that advanced imaging techniques may be useful in ruling out other

conditions that mimic CA.29 Such abnormalities are, however, uncommon and

reportedly occur in as little as 1-4% of cases.16, 29 Finally, while the age range of the

cohort investigated in the current study (8-14 years) is consistent with that reported

previously in children with CA, 10, 32 potential sex and hormonal effects on measures of FMM

and FS were not investigated. Nonetheless, the findings of the current study identified no

meaningful difference in FMM or FS in children with and without CA when evaluated

under quasistatic loading conditions. Although further research characterizing

measurement errors of FMM in children is recommended, the findings do not support the use

of interventions that aim to modify quasistatic foot mobility and stiffness in children with

CA.

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4.6 CONCLUSION

The current study found that differences in foot mobility magnitude in children with and

without CA were small and within the observed measurement error. Accordingly, clinical

measures of foot stiffness did not differ in children with and without CA during quasistatic

loading. While further research evaluating the level of uncertainty of the measurement

techniques in children and under dynamic loading conditions is recommended, the findings of

the current study question the rationale behind treatment protocols that aim to modify foot

mobility and stiffness in children with CA.

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4.7 REFERENCES

1. Bland JM, Altman DG. Measuring agreement in method comparison studies. Stat

Methods Med Res. 1999;8(2):135-160.

2. Bolgla LA, Malone TR. Plantar fasciitis and the windlass mechanism: a biomechanical

link to clinical practice. J Athl Train. 2004;39(1):77.

3. Buldt AK, Murley GS, Levinger P, Menz HB, Nester CJ, Landorf KB. Are clinical

measures of foot posture and mobility associated with foot kinematics when walking? J

Foot Ankle Res. 2015;8(1):1-12.

4. Butler RJ, Hillstrom H, Song J, Richards CJ, Davis IS. Arch height index measurement

system: establishment of reliability and normative values. J Am Podiatr Med Assoc.

2008;98(2):102-106.

5. Cassas KJ, Cassettari-Wayhs A. Childhood and adolescent sports-related overuse

injuries. Am Fam Physician. 2006;73(6):1014-1022.

6. Cheng JC, Leung SS, Leung AK, Guo X, Sher A, Mak AF. Change of Foot Size With

Weightbearing; A Study of 2829 Children 3 to 18 Years of Age. Clin Orthop Relat Res.

1997;342:123-131.

7. Cohen J. Statistical power analysis for the behavioral sciences. Hilsdale. NJ: Lawrence

Earlbaum Associates. 1988;2.

8. Cornwall MW, McPoil TG. Relationship between static foot posture and foot mobility. J

Foot Ankle Res. 2011;4(4):1-9.

9. Dicharry JM, Franz JR, Croce UD, Wilder RP, Riley PO, Kerrigan DC. Differences in

static and dynamic measures in evaluation of talonavicular mobility in gait. J Orthop

Sports Phys Ther. 2009;39(8):628-634.

10. Hendrix CL. Calcaneal apophysitis (Sever disease). Clin Podiatr Med Surg.

2005;22(1):55-62.

11. Hollander K, Scholz T, Braumann K-M, Zech A. Correlation between static and dynamic

foot arch measurement in children–preliminary study of the Barefoot LIFE project. Gait

Posture. 2016;49(suppl 2):178.

12. James AM, Williams CM, Haines TP. Effectiveness of footwear and foot orthoses for

calcaneal apophysitis: a 12-month factorial randomised trial. Br J Sports Med.

2016;50(20):1268-1275.

13. James AM, Williams CM, Luscombe M, Hunter R, Haines TP. Factors associated with

pain severity in children with calcaneal apophysitis (Sever Disease). J Pediatr.

2015;167(2):455-459.

14. Johannsen F, Hansen P, Stallknecht S, et al. Can positional MRI predict dynamic

changes in the medial plantar arch? An exploratory pilot study. J Foot Ankle Res.

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52

2016;9(1):35.

15. Kaeding CC, Whitehead R. Musculoskeletal injuries in adolescents. Prim Care.

1998;25(1):211-223.

16. Kose O. Do we really need radiographic assessment for the diagnosis of non-specific

heel pain (calcaneal apophysitis) in children? Skeletal Radiol. 2010;39(4):359-361.

17. Kvist M, Heinonem O. Calcaneal apophysitis (Sever's disease)—a common cause of heel

pain in young athletes. Scand J Med Sci Sports. 1991;1(4):235-238.

18. Landis JR, Koch GG. The measurement of observer agreement for categorical data.

Biometrics. 1977;33(1):159-174.

19. Liberson A, Lieberson S, Mendes DG, Shajrawi I, Haim YB, Boss JH. Remodeling of

the calcaneus apophysis in the growing child. J Pediatr Orthop B. 1995;4(1):74-79.

20. MacLean CL, Davis IS, Hamill J. Influence of running shoe midsole composition and

custom foot orthotic intervention on lower extremity dynamics during running. J Appl

Biomech. 2009;25(1):54-63.

21. McPoil TG, Cornwall MW, Vicenzino B, et al. Effect of using truncated versus total foot

length to calculate the arch height ratio. Foot. 2008;18(4):220-227.

22. McPoil TG, Vicenzino B, Cornwall MW, Collins N, Warren M. Reliability and

normative values for the foot mobility magnitude: a composite measure of vertical and

medial-lateral mobility of the midfoot. J Foot Ankle Res. 2009;2(1):6.

23. McPoil TG, Warren M, Vicenzino B, Cornwall MW. Variations in foot posture and

mobility between individuals with patellofemoral pain and those in a control group. J Am

Podiatr Med Assoc. 2011;101(4):289-296.

24. Micheli LJ, Fehlandt Jr AF. Overuse tendon injuries in pediatric sports medicine. Sports

Med Arthrosc. 1996;4(2):190-195.

25. Naaktgeboren K, Dorgo S, Boyle JB. Growth plate injuries in children in sports: A

review of Sever's disease. Strength Cond J. 2017;39(2):59-68.

26. Ogden JA, Ganey TM, Hill JD, Jaakkola JI. Sever’s injury: a stress fracture of the

immature calcaneal metaphysis. J Pediatr Orthop. 2004;24(5):488-492.

27. Perhamre S, Lazowska D, Papageorgiou S, Lundin F, Klässbo M, Norlin R. Sever’s

injury: a clinical diagnosis. J Am Podiatr Med Assoc. 2013;103(5):361-368.

28. Perhamre S, Lundin F, Klässbo M, Norlin R. A heel cup improves the function of the

heel pad in Sever's injury: effects on heel pad thickness, peak pressure and pain. Scand J

Med Sci Sports. 2012;22(4):516-522.

29. Rachel JN, Williams JB, Sawyer JR, Warner WC, Kelly DM. Is radiographic evaluation

necessary in children with a clinical diagnosis of calcaneal apophysitis (sever disease)? J

Pediatr Orthop. 2011;31(5):548-550.

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30. Richards C, Card K, Song J, Hillstrom H, Butler R, Davis I. A novel arch height index

measurement system (AHIMS): intra-and inter-rater reliability. Proceedings of American

Society of Biomechanics Annual Meeting Toledo. 2003.

31. Rohner-Spengler M, Mannion AF, Babst R. Reliability and minimal detectable change

for the figure-of-eight-20 method of measurement of ankle edema. J Orthop Sports Phys

Ther. 2007;37(12):199-205.

32. Scharfbillig RW, Jones S, Scutter SD. Sever’s disease: what does the literature really tell

us? J Am Podiatr Med Assoc. 2008;98(3):212-223.

33. Schmitt JS, Di Fabio RP. Reliable change and minimum important difference (MID)

proportions facilitated group responsiveness comparisons using individual threshold

criteria. J Clin Epidemiol. 2004;57(10):1008-1018.

34. Sever J. Apophysitis of the os calcis. NY Med J. 1912;95:1025.

35. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol

Bull. 1979;86(2):420.

36. Szames S, Forman W, Oster J, Eleff J, Woodward P. Sever's disease and its relationship

to equinus: a statistical analysis. Clin Podiatr Med Surg. 1990;7(2):377-384.

37. Thijs Y, Bellemans J, Rombaut L, Witvrouw E. Is high-impact sports participation

associated with bowlegs in adolescent boys? Med Sci Sports Exerc. 2012;44(6):993-998.

38. Toomey EP. Plantar heel pain. Foot Ankle Clin. 2009;14(2):229-245.

39. Walling AK, Grogan DP, Carty CT, Ogden JA. Fractures of the calcaneal apophysis. J

Orthop Trauma. 1990;4(3):349-355.

40. Weir JP. Quantifying test-retest reliability using the intraclass correlation coefficient and

the SEM. J Strength Cond Res. 2005;19(1):231-240.

41. Zifchock RA, Davis I, Hillstrom H, Song J. The effect of gender, age, and lateral

dominance on arch height and arch stiffness. Foot Ankle Int. 2006;27(5):367-372.

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CHAPTER 5 RADIOGRAPHIC FOOT MOBILITY MAGNITUDE IN CHILDREN:

AN EXPLORATORY STUDY

This small exploratory study was pursued as a subsequent investigation to the first

component of the experimental research phase of this thesis. The preliminary investigation

primarily aimed to evaluate the contribution of soft tissue distortion to clinical FMM

measurement. The chapter has been compiled in a ‘Short Communication’ format.

Contributions of co-authors:

S. McSweeney: contributed to study conception and design, data collection, data analysis and

interpretation, and preparation of the manuscript.

L. Reed: contributed to study conception and design, data analysis and interpretation, and

preparation of the manuscript.

S. Wearing: contributed to study conception and design, data analysis and interpretation, and

preparation of the manuscript.

The co-authors have certified that:

1. they meet the criteria for authorship in that they have participated in the conception, execution, or

interpretation, of at least that part of the chapter in their field of expertise (as described);

2. they take public responsibility for their part of the chapter, except for the responsible author who accepts

overall responsibility for the chapter;

3. there are no other authors of the chapter according to these criteria;

4. potential conflicts of interest have been disclosed to (a) granting bodies, (b) the editor or publisher of

journals, and (c) the head of the responsible academic unit, and

5. they agree to the use of the chapter in the student’s thesis and its publication on the QUT’s ePrints site

consistent with any limitations set by publisher requirements.

Simon McSweeney 12 December 2018

Lloyd Reed 12 December 2018

Scott Wearing 12 December 2018

QUT Verified Signature

QUT Verified Signature

QUT Verified Signature

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5.1 INTRODUCTION

Foot mobility magnitude (FMM) is a clinical measure of the change in foot shape with

weightbearing, which has been advocated to be a potentially useful predictor of lower limb

injury in adults. 1 Defined as the root mean square of the change in arch height (AH) and

midfoot width (MFW) under nonweightbearing and weightbearing condition, FMM

purportedly reflects the mobility of the osseous segments of the foot. 2 While the reliability of

clinical measures of FMM has been established in adults, 2 and is reported for the first time in

children in Chapter 4, the potentially confounding effect of soft tissue distortion to the

measurement has not been considered. This pilot study explored the potential relation

between clinical and non-contact measures of FMM and the relative contribution of soft

tissue distortion to FMM in a small subset of participants.

5.2 METHODS

A convenience subsample of three male children (2 with CA, 1 healthy) were recruited from

participants of a larger study outlined in Chapter 4, which included 22 consecutive cases of

CA and 19 healthy children without heel pain, aged 8-14 years. The age, height, and body

mass of the three participants is displayed in Table 5.1. No child reported a history of

fracture, tumour or surgery of the foot within the last 12 months, overt orthopaedic

abnormalities of the foot, or medical conditions that could affect the foot and lower limb. All

participants provided written, informed consent with their accompanying guardians prior to

participation in the research. The pilot investigation received approval from the university

human research ethics committee (QUT Ethics Approval Number: 1500001041) and was

undertaken according to the principles outlined in the Declaration of Helsinki.

Table 5.1 Anthropometric data for the 3 participants.

Variable p1 p2 p3

Age (y) 11 14 11

Height (cm) 148 166 154.5

Body Mass (kg) 46.5 70 58

BMI (kg/m2) 21 25 24

p, Participant

Spherical (diameter 1.5mm) radiopaque markers (E-Z-Mark, Bracco Diagnostics Inc.,

Princeton, N) were fixed to the skin of the right foot at the anatomical sites corresponding to

clinical FMM measurement described in detail in Chapter 4.3.3. In brief, skin markers were

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positioned on the medial, lateral and dorsal foot at 50% of foot length measured during quiet

double-limb stance (DLS), the most posterior aspect of the calcaneus and the most anterior

aspect of the longest digit. 2

Lateral (LAT) and anteroposterior (AP) radiographs were acquired during double limb

support (DLS) and under non-weightbearing (NWB) conditions as per published clinical

FMM measurement protocol. 2 During DLS participants were requested to stand erect with

their bodyweight equally distributed on both limbs and NWB measurements were taken once

participants reported ‘first contact’ of their plantar foot with the support surface, 2 undertaken

with the assistance of a height-adjustable chair. During the trial, positioning of the X-ray tube

and image intensifier remained consistent for each set of images, with the distance from the

X-ray tube to the foot and exposure setting providing a 1:1 ratio (i.e no magnification). For

the LAT images, the central X-ray beam was directed at 90 degrees to long axis of the foot

and centred on the base of the fifth metatarsal. 3 AP images were acquired with the central X-

ray beam orientated 30 degrees to the vertical axis 3 and directed to the base of the third

metatarsal. The distance from the X-ray tube to the foot was 100 cm with an exposure setting

of 2.5 mAs at 66 kV. To correct for potential distortion, a rectilinear calibration grid

described elsewhere 4 was positioned within the field of view, and orientated such that it was

coincident with the long axis of the foot for LAT images and perpendicular to the central x-

ray beam for AP images.

5.2.1 Data reduction and statistical analysis

Radiographs were analysed using Matlab (Matlab R2012a, MathWorks, Natick,

Massachusetts, USA). Following a two-dimensional direct linear transformation of the

calibration grid, 4, 5 the centre of each radiographic skin marker and the corresponding soft-

tissue-bone interface were manually digitized for each image (Figures 5.1a, b and 5.2).

Radiographic-based measures of AH, MFW and FL were then defined using two approaches.

The first approach mimicked clinical measures, in that the distance between radio-opaque

skin markers (MFWrs, FLrs) or between radio-opaque skin markers and the support surface

(AHrs) were calculated. In the second approach, bone-to-bone distances were calculated.

AHrb was defined as the distance between the dorsal bone surface corresponding to the

clinical measurement site and a line connecting the plantar surface of the calcaneus and the

head of the first metatarsal.

As per the methods for clinical FMM measurement outlined in Chapter 4, FMM from skin-

mounted radiographic markers and radiographic bone measurements was calculated

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according to the equation outlined by McPoil et al.,2 where dAHxx and dMFWxx reflect the

change in arch height and midfoot width between DLS and NWB, respectively.

FMMxx = √dAH2 + dMFW2

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FIGURE 5.1(a) Anteroposterior foot radiograph demonstrating the respective measurement

margins for MFWrs (red) and MFWrb (yellow).

FIGURE 5.1(b) Lateral foot radiograph demonstrating the respective measurement margins

for AHrs and FLrs (red) and AHrb and FLrb (yellow).

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FIGURE 5.2 Lateral foot radiographs during NWB (upper) and DLS (lower). Arrows

indicate the position of the radio-opaque dorsal arch height skin marker. Note both osseous

movement and soft tissue deformation occur.

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5.3 RESULTS

Table 5.2 displays the differences in radiographic skin-marker and bone-bone AH, MFW and

FL measurements for each participant during stance.

Table 5.2. Radiographic foot dimensions during double-limb stance.

Variable (mm) p1 p2 p3

AHrs 66 82 72

AHrb 42 52 45

MFWrs 90 88 80

MFWrb 60 65 58

FLrs 267 270 250

FLrb 251 250 235

p, Participant

Table 5.3. Changes in soft tissue and osseous radiographic foot dimensions with loading.

Variable (mm) p1 p2 p3

dAHrs 7 3 3

dAHrb 5 1 0

dMFWrs 12 4 1

dMFWrb 4 2 1

dFLrs 6 9 1

dFLrb 5 5 0

FMMrs 14 5 3

FMMrb 6 3 1

p, Participant

As demonstrated in Table 5.3, the difference in radiographic skin-marker FMM and bone-

bone FMM scores for each participant ranged from 2-8 mm. The relative differences in

dAHrs-dAHrb, dMFWrs-dMFWrb and dFLrs-dFLrb ranged from 2-3 mm, 0-8 mm and 1-4

mm respectively.

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5.4 DISCUSSION and CONCLUSION

FMM has been increasingly used as a clinical measure of foot mobility. However, both

osseous realignment and distortion of the soft tissues of the foot are known to occur with

weightbearing. 6 The clinical measurement of FMM not only includes potential error arising

from caliper measurement (chapter 4) but also likely reflects a combination of osseous

movement and soft tissue distortion with loading. In this small pilot investigation the

contribution of soft tissue distortion to FMM measurement was highly variable between

participants. Considering foot mobility is known to influence the management of varied foot

ailments in the clinical setting, 2 the findings of this preliminary investigation duly consider

and caution the interpretation (osseous vs soft tissue movement) of clinical FMM

measurement as a composite measure of foot mobility, raising doubts as to its accuracy. This

small initial exploratory investigation has furthermore identified a need for continued

research within these realms of clinical foot science and highlights the importance of

validating this measurement procedure for application in the clinical setting.

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5.5 REFERENCES

1. Cornwall MW, McPoil TG. Relationship between static foot posture and foot mobility. J

Foot Ankle Res. 2011;4(1):4.

2. McPoil TG, Vicenzino B, Cornwall MW, Collins N, Warren M. Reliability and

normative values for the foot mobility magnitude: a composite measure of vertical and

medial-lateral mobility of the midfoot. J Foot Ankle Res. 2009;2(1):6.

3. Davids JR, Gibson TW, Pugh LI. Quantitative segmental analysis of weight-bearing

radiographs of the foot and ankle for children: normal alignment. J Pediatr Orthop.

2005;25(6):769-776.

4. Wearing SC, Smeathers JE, Yates B, Sullivan PM, Urry SR, Dubois P. Errors in

measuring sagittal arch kinematics of the human foot with digital fluoroscopy. Gait

Posture. 2005;21(3):326-332.

5. Baltzopoulos V. A videofluoroscopy method for optical distortion correction and

measurement of knee-joint kinematics. Clin Biomech (Bristol, Avon). 1995;10(2):85-92.

6. Nigg BM, MacIntosh BR, Mester J. Biomechanics and biology of movement: Human

Kinetics; 2000.

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CHAPTER 6 RELIABILITY OF AN INSTRUMENTED TREADMILL FOR

CHARACTERIZING GAIT IN CHILDREN

Forming part of the methodological componentry of the thesis, this study was designed as a

prelude to the experiment presented in Chapter 7, and evaluated the within-session reliability

of an instrumented treadmill for characterizing gait in children. The chapter contains a

formatted manuscript submitted to Gait and Posture journal.

Contributions of co-authors:

S. McSweeney: contributed to study conception and design, data collection, data analysis and

interpretation, and preparation of the manuscript.

L. Reed: contributed to study conception and design, data analysis and interpretation, and

preparation of the manuscript.

S. Wearing: contributed to study conception and design, data analysis and interpretation, and

preparation of the manuscript.

The co-authors have certified that:

1. they meet the criteria for authorship in that they have participated in the conception, execution, or

interpretation, of at least that part of the publication in their field of expertise (as described);

2. they take public responsibility for their part of the publication, except for the responsible author

who accepts overall responsibility for the publication;

3. there are no other authors of the publication according to these criteria;

4. potential conflicts of interest have been disclosed to (a) granting bodies, (b) the editor or publisher

of journals, and (c) the head of the responsible academic unit, and

5. they agree to the use of the publication in the student’s thesis and its publication on the QUT’s

ePrints site consistent with any limitations set by publisher requirements.

Simon McSweeney 12 December 2018

Lloyd Reed 12 December 2018

Scott Wearing 12 December 2018

QUT Verified Signature

QUT Verified Signature

QUT Verified Signature

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64

6.1 ABSTRACT

Background: Instrumented treadmills that incorporate pressure platforms have increasingly

been used to characterize gait in children. Although the measurement performance of

pressure platforms is known to be influenced by footprint size, published evidence on the

reliability of such systems for children’s gait is lacking. The present study evaluated the

within–session reliability of temporospatial gait parameters and vertical ground reaction

forces measured in healthy children during barefoot walking and running on a capacitance–

based instrumented treadmill system.

Methods: Temporospatial gait parameters, including cadence, step length, stride duration,

stance and swing phase durations, and the magnitude and timing of conventional vertical

ground reaction force peaks were determined on two occasions for 17 healthy children (mean

age, 11 ± 2 years; height, 148.4 ± 9.3 cm; and mass, 43.3 ± 10 kg) during walking and

running at preferred speed on an instrumented treadmill. Intra class correlation coefficients

(ICC) and standard error of measurement (SEM) were calculated as indices of reliability. The

minimum detectable change (MDC95%) was also calculated.

Results: ICC values ranged from 0.94-0.99 for all variables. When expressed as a percentage

of mean values, the SEM was <5% for all gait parameters assessed during walking and

running. Peak vertical ground reaction force loading rate displayed the greatest variability

(SEM ≈ 4%). MDC95% values for gait parameters were typically higher during running than

walking, and were ±4 % of the gait cycle for temporal parameters, ±3 cm for step length and

±11 % bodyweight for peak vertical ground reaction force.

Conclusions: Children’s gait parameters varied by <5 % between test occasions and were

typically more consistent during walking than running. The findings provide a reference for

clinicians of the magnitude of gait changes that can be reliably detected in children by an

instrumented treadmill that incorporates a pressure platform.

Keywords: Paediatric; gait analysis; repeatability; kinematic; kinetic.

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6.2 INTRODUCTION

Instrumented treadmills incorporating pressure platforms are emerging as an efficient method

to quantify gait in children and adolescents [1]. These systems, which capture pressure-based

electronic footprints, have the advantage of allowing rapid measurement of basic

temporospatial gait parameters and ground reaction force over a large number of steps. Such

treadmills have been used to monitor gait patterns in children with cerebral palsy [2] and

Down syndrome [3, 4], and in the assessment of interventions designed to improve gait

patterns in children [1, 5]. Although previous reliability studies involving the use of

instrumented treadmills in adults have reported errors (within–subject coefficient of

variation) of less than 10% for most gait parameters [6, 7], the reliability of such measures in

children is yet to be determined.

While many factors may affect the reliability of capacitance-based treadmill measurement

[8], it is particularly important to establish the reliability of these systems in children, as they

have smaller footprint areas and lower peak pressures than adults, both of which are known to

adversely influence the accuracy of pressure measurement systems [9, 10]. The aim of this

study, therefore, was to evaluate the within–session reliability of temporospatial gait

parameters and vertical ground reaction force in healthy children while walking and running

on a capacitance–based treadmill system at self–selected speed.

6.3 METHODS

Seventeen healthy children (12 males and 5 females) walked and ran barefoot on an

instrumented treadmill (FDM–THM–S, Zebris Medical GmbH, Isny, Germany) on two

occasions. Children had a mean (± SD) age, height, and body mass of 11 ± 2 years, 148.4 ±

9.3 cm, and 43.3 ± 10 kg, respectively. No child reported a history of balance disorders or

medical conditions likely to affect their ability to walk and run on a treadmill. All participants

provided written informed consent with their accompanying guardians before participating in

the study, which received approval from the university human research ethics committee.

The instrumented treadmill system is described in detail elsewhere [6]. In brief, the treadmill

contained a capacitance-based pressure platform that incorporated 7168 sensors; each

approximately 0.85 x 0.85 cm in size. The belt of the treadmill had a contact surface of 150 x

50 cm and its speed could be adjusted in increments of 0.1 km.h-1 up to a maximum speed of

22 km.h-1.

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Following anthropometric assessment, children were provided a treadmill acclimatization

session, which included at least six minutes of steady-state barefoot walking and running at

self-selected speeds [11]. Given that variability in stride and step parameters are typically

lowest at self-selected speeds [12], participants were instructed to adjust the speed of the

treadmill to their ‘‘comfortable’’ walking and running pace [6]. Pressure data were then

subsequently recorded over 30 seconds of steady-state barefoot walking and running,

respectively. All data were collected at a sampling rate of 120 Hz. Gait trials were

subsequently repeated in a second session, approximately 15 minutes later, at identical

walking and running speeds to the first session, to evaluate the within-session reliability of

gait parameters.

Pressure data were exported from the treadmill in ASCII format. Ground reaction force was

normalized to body weight and the magnitude and timing of conventional vertical ground

reaction force peaks were identified for each step (Figure 6.1). Peak force loading rate

(PFLR), defined as the maximum force differential during the first 20 ms of stance, was

calculated using previously outlined methods [13]. Basic temporospatial gait parameters

including cadence, step length, stride duration, stance and swing phase durations were also

calculated. With the exception of stride duration, all temporal data were expressed as a

percentage of the gait cycle. Mean values were calculated for all steps recorded within the 30-

s data capture period, which equated to an average of 29 ± 4 steps during barefoot walking

and 44 ± 5 steps during barefoot running.

FIGURE 6.1. Typical vertical ground reaction force curves during one gait cycle of walking

(gray line) and running (black line) taken from a single participant. Note that vertical ground

0

0.5

1

1.5

2

2.5

3

0 20 40 60 80

Ver

tica

l G

rou

nd

Rea

ctio

n F

orc

e (B

W)

Time (% Gait Cycle)

Walk

Run

F3

F1F3

F2

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reaction force during walking was characterized by two maxima (F1, F3), and the local

minimum (F2), whereas only one maxima (F3) was apparent during running.

Statistical analysis was performed using IBM-SPSS statistical software (Version 21 for

Windows IBM Corp. Armonk, NY, USA). All data were evaluated for normality using the

Shapiro Wilkes test. A 2 (gait) x 2 (trial) repeated measure ANOVA model was used to

investigate main effects for ‘trial’ and its interaction with ‘gait’ for cadence, step length,

stride duration, stance phase duration, swing phase duration, peak force, and PFLR. In each

case, measurement trial (trial 1, 2) and gait (walk, run) were treated as within-subject factors.

An alpha level of .05 was used for all tests of significance. As there was no statistically

significant difference between limbs, only data for the right limb have been presented.

Measurement reliability was assessed using intraclass correlation coefficients (ICC 2,1) [14].

As ICC values are relative measures of reliability and not directly transferable to different

populations [15], the standard error of measurement (SEM) was also calculated according to

the equation: SEM = SDd/√2 , where SDd represents the standard deviation of difference

scores [16]. The minimal detectable change (MDC95%), an index of measurement

sensitivity, was additionally calculated according to the equation: MDC95% = 1.96 × SDd,

where 1.96 reflects the z-score associated with the desired level of confidence [16].

6.4 RESULTS

The average gait speed of participants during treadmill walking and running was 1.01 ± 0.22

m.s-1 (range 0.72-1.50 m.s-1) and 1.90 ± 0.26 m.s-1 (range 1.52-2.41 m.s-1), respectively.

Statistically significant main effects of gait condition were observed for all temporospatial

and ground reaction force parameters. There were, however, no statistically significant

differences in peak ground reaction force or temporospatial gait parameters between repeated

walking (Table 6.1) and running (Table 6.2) trials.

ICC values for all gait parameters ranged between 0.94 and 0.99. When expressed as a

percentage of the mean, the SEM was less than 5% for all vertical ground reaction force and

temporospatial gait parameters assessed during walking and running. As demonstrated for

cadence (Figure 6.2), MDC95% values during running for all variables were typically higher

(approximately double) than those during walking.

.

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TABLE 6.1 Mean (SD) temporospatial and kinetic gait parameters during barefoot walking on an instrumented treadmill (BW, body weight).

Variable Trial 1 Trial 2 ICC CI95% SEM (%) BIAS MDC95%

Cadence (strides/sec) 0.98 0.97 0.99 (0.97-0.99) 0.01 0.01 0.04

(0.12) (0.13) (1)

Step length (m) 0.64 0.64 0.99 (0.97-0.99) 0.01 0.00 0.02

(0.08) (0.07) (2)

Stride duration (sec) 1.04 1.05 0.99 (0.98-0.99) 0.02 -0.01 0.04

(0.14) (0.14) (2)

Stance phase duration (%) 62 62 0.99 (0.97-0.99) 0 0 1

(2) (2) (0)

Swing phase duration (% ) 38 38 0.99 (0.97-0.99) 0 0 1

(2) (2) (0)

First force peak (BW) 1.2 1.2 0.97 (0.93-0.99) 0.0 0.0 0.1

(0.1) (0.1) (2)

Time first force peak (%) 28 28 0.94 (0.85-0.98) 1 0 4

(4) (4) (4)

Minima force (BW) 0.9 0.9 0.99 (0.99-0.99) 0.0 0.0 0.0

(0.1) (0.1) (1)

Time minima force (%) 49 50 0.91 (0.76-0.97) 1 -1 3

(3) (2) (2)

Second force peak (BW) 1.2 1.2 0.98 (0.95-0.99) 0.0 0.0 0.0

(0.1) (0.1) (1)

Time second force peak (%) 74 74 0.95 (0.86-0.98) 1 0 3

(3) (3) (1)

Peak force loading rate (BW·s-1) 116 117 0.99 (0.98-0.99) 5 -1 13 (42) (40) (4)

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TABLE 6.2 Mean (SD) temporospatial and kinetic gait parameters during barefoot running on an instrumented treadmill (BW, body weight).

Variable Trial 1 Trial 2 ICC CI95% SEM (%) BIAS MDC95%

Cadence (strides/sec) 1.48 1.49 0.98 (0.97-0.99) 0.02 -0.01 0.06

(0.15) (0.15) (1)

Step length (m) 0.58 0.57 0.98 (0.95-0.99) 0.01 0.01 0.03

(0.06) (0.06) (2)

Stride duration (sec) 0.68 0.68 0.99 (0.98-0.99) 0.01 0.00 0.03

(0.07) (0.07) (1)

Stance phase duration (%) 46 45 0.99 (0.97-0.99) 1 0 2

(6) (6) (2)

Swing phase duration (%) 54 55 0.99 (0.97-0.99) 1 0 2

(6) (6) (2)

Peak force (BW) 2.1 2.1 0.99 (0.96-0.99) 0.0 0.0 0.1

(0.2) (0.2) (2)

Time peak force (%) 35 35 0.95 (0.86-0.98) 1 0 3

(4) (3) (3)

Peak force loading rate (BW·s-1) 287 287 0.99 (0.97-0.99) 11 0 32 (86) (89) (4)

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FIGURE 6.2. Bland and Altman plot for cadence during walking (gray) and running (black)

in children. Bias (solid line) and upper and lower limits of agreement (dashed lines) for

between trials (within-session).

-0.10

-0.08

-0.06

-0.04

-0.02

0.00

0.02

0.04

0.06

0.08

0.10

0.60 0.80 1.00 1.20 1.40 1.60 1.80

Wit

hin

-ses

sio

n d

iffe

rence

in C

aden

ce (

Str

ide/

sec)

Average Cadence (Stride/sec)

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6.5 DISCUSSION

The present study evaluated the reliability of a capacitance–based treadmill system to

estimate temporospatial and peak vertical ground reaction force parameters in healthy

children while walking and running at self–selected speed. According to the criteria of Landis

and Koch [14], ICC values for all temporospatial and kinetic gait parameters were ‘almost

perfect’ during walking and running. The SEM was <5 % for all gait parameters assessed

during walking and running. Consistent with previous research in adults [17], MDC95%

values during running, however, were typically higher and approximately double those of

walking.

The minimum detectable change for temporal parameters was less than ±4 % when expressed

as a percentage of the gait cycle, ±3 cm for step length and ±11 % for ground reaction force

peaks when normalized to body weight during walking and running. These values are

generally less than, or consistent with, those reported in adults during walking [6, 7, 18].

Although previous research has suggested that the repeatability of temporospatial data may

be lower in children than adults during overground gait [18]; several factors such as age,

instrumentation, and the specific measurement protocol adopted are known to influence the

reliability of temporospatial gait parameters [19]. For instance, rather than allow participants

to self-select their gait speed during each of the two measurement occasions, as used

previously in adults [6], gait speeds during the second measurement trial in the current study

were set by researchers so as to be identical to those adopted by participants in the first

session. Nevertheless, it is interesting to note that the MDC95% values reported for

temporospatial parameters in the current study are inclusive of significant differences

reported in step length, cadence, and timing of vertical ground reaction force peaks reported

by previous footwear and intervention studies; in which an identical system was used to

characterize children’s gait [1, 3, 4]. While MDC95% values observed in the present study

raise questions as to the clinical significance of such findings, they also highlight the need for

researchers and clinicians to evaluate the measurement characteristics of instrumented

treadmills in a variety of populations and over a range of gait speeds.

This study has a number of limitations. The reliability of gait parameters was determined in

healthy children (aged 8-14 years) at self–selected gait speeds. It is well documented that

speed and variability in basic gait parameters display a quadratic relationship with gait speed

in young adults, in which gait variability increases at speeds slower or faster than preferred

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[10, 11, 13]. Therefore, reliability indices and MDC95% for gait parameters in the current

study may not be transferrable to other cohorts walking and running at gait speeds other than

their self-selected “comfortable” speed [3, 4, 8]. Moreover, treadmill systems are known to

induce temporal and spatial constraints on gait [8]. Hence, the reliability of gait parameters in

this study may not be representative of over-ground or unconstrained gait outside of the

laboratory setting [18]. Nonetheless, the findings of the current study provide clinicians and

researchers with an indication of the reliability and sensitivity of a capacitance–based

treadmill system to detect changes in common temporospatial gait parameters and vertical

ground reaction forces in healthy children during walking and running at self–selected speed.

6.6 CONCLUSION

The findings of the current study describe the reliability and sensitivity of a capacitance–

based instrumented treadmill for characterizing gait in children. Although the SEM for all

gait parameters derived from the treadmill system were <5%, peak ground reaction force and

temporospatial gait parameters were typically less consistent during running than walking.

The minimum change that can be detected with 95% confidence by the instrumented

treadmill ranged between ±1% and ±4% for temporal parameters, ±2cm and ±3cm for step

length, and ±3% and ±11% for peak vertical ground reaction force during walking and

running, respectively.

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6.7 REFERENCES

1. Hollander K, Riebe D, Campe S, Braumann KM, Zech A. Effects of footwear on

treadmill running biomechanics in preadolescent children. Gait Posture. 2014;40(3):381-

5.

2. Romkes J, Brunner R: An electromyographic analysis of obligatory (hemiplegic cerebral

palsy) and voluntary (normal) unilateral toe-walking. Gait Posture. 2007;26(4):577-86.

3. Wu J, Ajisafe T. Kinetic patterns of treadmill walking in preadolescents with and without

Down syndrome. Gait Posture. 2014;39(1):241-6.

4. Wu J, Beerse M, Ajisafe T, Liang H. Walking dynamics in preadolescents with and

without Down syndrome. Phys Ther. 2015;95(5):740-9.

5. Romkes J, Hell AK, Brunner R. Changes in muscle activity in children with hemiplegic

cerebral palsy while walking with and without ankle–foot orthoses. Gait Posture. 2006;

24(4):467-74.

6. Reed LF, Urry SR, Wearing SC. Reliability of spatiotemporal and kinetic gait parameters

determined by a new instrumented treadmill system. BMC Musculoskelet Disord. 2013;

14(1):1-10.

7. Faude O, Donath L, Roth R, Fricker L, Zahner L. Reliability of gait parameters during

treadmill walking in community-dwelling healthy seniors. Gait Posture. 2012; 36(3):444-

448.

8. Stolze H, Kuhtz-Buschbeck J, Mondwurf C, Boczek-Funcke A, Jöhnk K, Deuschl G,

Illert M. Gait analysis during treadmill and overground locomotion in children and

adults. Electroencephalogr Clin Neurophysiol. 1997;105(6):490-7.

9. Hennig EM, Rosenbaum D. Pressure distribution patterns under the feet of children in

comparison with adults. Foot Ankle. 1991;11(5):306-11.

10. Urry SR, Wearing SC. A comparison of footprint indexes calculated from ink and

electronic footprints. J Am Podiatr Med Assoc. 2001;91(4):203-9.

11. Lavcanska V, Taylor NF, Schache AG. Familiarization to treadmill running in young

unimpaired adults. Hum Mov Sci. 2005;24(4):544-57.

12. Jordan K, Newell KM. The structure of variability in human walking and running is

speed-dependent. Exerc Sport Sci Rev. 2008;36(4):200-4.

13. Revill AL, Perry SD, Edwards AM, Dickey JP. Variability of the impact transient during

repeated barefoot walking trials. J Biomech. 2008;41(4):926-30.

14. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol

Bull. 1979;86(2):420.

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15. Rohner-Spengler M, Mannion AF, Babst R. Reliability and minimal detectable change

for the figure-of-eight-20 method of measurement of ankle edema. J Orthop Sports Phys

Ther. 2007;37(12):199-205.

16. Weir JP. Quantifying test-retest reliability using the intraclass correlation coefficient and

the SEM. J Strength Cond Res. 2005;19(1):231-40.

17. Nüesch C, Overberg J-A, Schwameder H, Pagenstert G, Mündermann A. Repeatability

of spatiotemporal, plantar pressure and force parameters during treadmill walking and

running. Gait Posture. 2018;62:117-23.

18. Stolze H, Kuhtz-Buschbeck J, Mondwurf C, Jöhnk K, Friege L. Retest reliability of

spatiotemporal gait parameters in children and adults. Gait Posture. 1998;7(2):125-30.

19. Cousins SD, Morrison SC, Drechsler WI. The reliability of plantar pressure assessment

during barefoot level walking in children aged 7-11 years. J Foot Ankle Res.

2012;5(1):8.

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CHAPTER 7 VERTICAL GROUND REACTION FORCES DURING GAIT IN

CHILDREN WITH AND WITHOUT CALCANEAL APOPHYSITIS

Forming the second component of the experimental phase of this research, this study

addressed the second research aim and investigated vertical ground reaction forces and peak

plantar pressures during walking and running gait in children with and without CA. The

chapter has been reformatted from the published article:

McSweeney S, Reed LF, Wearing SC. Vertical ground reaction forces during gait in children

with and without calcaneal apophysitis. Gait Posture. 2019;71:126-130.

Contributions of co-authors:

S. McSweeney: contributed to study conception and design, data collection, data analysis and

interpretation, and preparation of the manuscript.

L. Reed: contributed to study conception and design, data analysis and interpretation, and

preparation of the manuscript.

S. Wearing: contributed to study conception and design, data analysis and interpretation, and

preparation of the manuscript.

The co-authors have certified that:

1. they meet the criteria for authorship in that they have participated in the conception, execution, or

interpretation, of at least that part of the publication in their field of expertise (as described);

2. they take public responsibility for their part of the publication, except for the responsible author

who accepts overall responsibility for the publication;

3. there are no other authors of the publication according to these criteria;

4. potential conflicts of interest have been disclosed to (a) granting bodies, (b) the editor or publisher

of journals, and (c) the head of the responsible academic unit, and

5. they agree to the use of the publication in the student’s thesis and its publication on the QUT’s

ePrints site consistent with any limitations set by publisher requirements.

Simon McSweeney 12 December 2018

Lloyd Reed 12 December 2018

Scott Wearing 12 December 2018

QUT Verified Signature

QUT Verified Signature

QUT Verified Signature

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7.1 ABSTRACT

Background: Heightened vertical loading beneath the foot has been anecdotally implicated

in the development of activity-related heel pain of the calcaneal apophysis in children but is

supported by limited evidence.

Research question: This study investigated whether vertical loading patterns during walking

and running differed in children with and without CA.

Methods: Vertical ground reaction force, peak plantar pressure (forefoot, midfoot, heel) and

temporospatial gait parameters (cadence, step length, stride, stance and swing phase

durations) were determined in children with (n=14) and without (n=14) CA. Measures were

acquired during barefoot walking and running at matched self-selected speed using an

instrumented treadmill, sampling at 120 Hz. Statistical comparisons between groups were

made using repeated measure ANOVAs.

Results: There were no significant between group differences in vertical ground reaction

force peaks or regional peak plantar pressures. However, when normalised to stature, cadence

was significantly higher (≈ 5%) and step length shorter (≈ 5%) in children with CA than those

without, but only during running (P <.05). Maximum pressure beneath the rearfoot during

running was significantly correlated with self-reported pain in children with CA.

Significance: Peak vertical force and plantar pressures did not differ significantly in children

with and without CA during walking or running. However, children with CA adopted a

higher cadence than children without heel pain during running. While the findings suggest

that children with CA may alter their cadence to lower pressure beneath the heel and, hence

pain, they also highlight the benefit of evaluating running rather than walking gait in children

with CA.

Keywords: Sever’s disease; heel pain; paediatric; ground reaction force

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7.2 INTRODUCTION

Calcaneal apophysitis (CA) is a common cause of activity-related heel pain in children,

which is characterized by pain involving the secondary growth centre of the calcaneus [1].

Although poorly understood, the condition is widely considered to be a mechanical overuse

injury of the chondral physis in children, with elevated vertical ground reaction force often

raised as one of several factors anecdotally suggested to be linked to its development [1-3].

Previous research has reported that children with CA have 4 to 10 times higher peak plantar

pressure (kPa) beneath the heel during standing (CA cases 339 ± 27; healthy controls 83 ± 2)

and walking (CA cases 880 ± 78; healthy controls 88 ± 11) at self-selected speed than

asymptomatic children, suggesting that plantar loading of the heel may be important in CA

[4]. Surprisingly, despite its well-known clinical link to more dynamic activities such as

running and jumping [5], vertical loading beneath the heel during such activities is yet to be

investigated in CA. This is important because ground reaction forces are known to be

influenced by gait speed and changes to basic temporospatial gait parameters [6, 7]. The aim

of the present study, therefore, was to evaluate peak plantar pressures and vertical ground

reaction force parameters during walking and running in children with and without CA.

Consistent with previous research investigating heel pain in children and adults [4, 8, 9], it

was hypothesized that vertical ground reaction forces during walking and running would be

higher in children with CA than in those without.

7.3 METHODS

7.3.1 Participants

Fourteen children with clinical signs and symptoms of CA and 14 healthy children without

heel pain participated in the study. Children were 8-14 years of age and recruited from the

greater Brisbane metropolitan area via public advertisements and direct referral from health-

care providers and local sporting clubs. CA was diagnosed by a healthcare professional with

more than 10-years clinical experience using established criteria, which included a

comprehensive medical history and physical replication of clinical symptoms with medial

and lateral compression of the calcaneal apophysis (squeeze test) [10, 11]. Healthy

participants were individually matched on age (± 3 yrs), and were free of lower limb pain and

pathology on examination. Exclusion criteria for all participants included poorly-defined

calcaneal symptoms, a self-reported history of calcaneal fracture, tumour or surgery of the

foot within the last 12 months, and a self-reported medical history of autoimmune,

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neurological, vascular, metabolic or endocrine disorders. No participant presented with a

lower extremity rotational or angular abnormalities beyond previously reported ‘normal’

values [12]. Current or past treatment for CA were not exclusion criteria in this study.

The mean (± SD) age, height and weight of participants is displayed in Table 7.1. Of the

fourteen children with CA, twelve were male and two were female. Eleven children presented

with bilateral symptoms, one with symptoms involving only the left foot and two only the

right foot. For the purpose of this study, only the right foot was considered in children

presenting with bilateral symptoms. In all cases, symptoms had been present for a duration of

at least 8 weeks and were exacerbated by physical activity. The median duration of symptoms

intermittently experienced by participants prior to assessment was 21 months (range, 6-48

months). Children reported a median heel pain of 3 cm (range, 1-7 cm) on a standard 10-cm

visual analogue pain scale (VAS), anchored by the terms “no pain” and “worst pain”.

Table 7.1. Anthropometric data for children with and without calcaneal apophysitis.

Variable Calcaneal Apophysitis Healthy Control

n 14 14

Sex (Males: Females) 12:2 10:4

Age (y) 11 ± 1 12 ± 2

Height (cm) 152 ± 10 157 ± 13

Body Mass (kg) 44 ± 8 50 ± 16

n, sample size.

Participant numbers were estimated a priori based on previously published ground reaction

force data reported for children during treadmill walking [13], and were sufficient to detect a

10% difference in peak vertical ground reaction force (1.03 ± 0.07 BW) at an alpha (ɑ) level

of .05 and beta (β) of .20. All participants provided written informed assent with their

accompanying guardians providing consent before participating in the study. The methods

used in the study received approval from the University Human Research Ethics Committee

(Ethics Approval: 1500001041).

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7.3.2 Equipment

An instrumented treadmill system (FDM–THM–S, Zebris Medical GmbH, Isny, Germany)

was used to measure vertical ground reaction force, regional plantar pressure and

temporospatial gait parameters during barefoot walking and running at self-selected speed

(Figure 7.1). The treadmill contained a capacitance-based pressure platform with a sensing

area of 108.4 x 47.4 cm. The platform incorporated 7168 pressure transducers, each

approximately 0.85 x 0.85 cm in size. The belt of the treadmill had a contact surface of 150 x

50 cm, and its speed could be adjusted between 0.2 and 22 km.h-1, in increments of 0.1 km.h-

1. Reported coefficients of variation for repeated measures of temporospatial gait parameters

in adults is typically below 10% using the system [14, 15], but have not been established for

paediatric cohorts.

FIGURE 7.1. Vertical ground reaction force, regional plantar pressure and temporospatial

gait parameters during barefoot walking and running were estimated via an instrumented

treadmill system.

7.3.3 Protocol

Participants reported to the laboratory wearing lightweight, comfortable clothing. Following

anthropometric measures of weight and height, children undertook a treadmill acclimatization

session which involved a minimum of six minutes of steady-state barefoot treadmill walking

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and running at a self-selected ‘‘comfortable” speed [16, 17]. After a further three minutes,

plantar pressure and ground reaction force data were then recorded over 10 seconds of

steady-state barefoot walking and running at a sampling rate of 120 Hz [16]. Gait speeds of

children without heel pain were individually matched to the self-selected gait speed of

children with CA to mitigate potentially confounding effects of speed on vertical ground

reaction force and temporospatial gait parameters [18.19].

7.3.4 Data Reduction and Statistical Analysis

As variations in foot strike pattern have been shown to influence peak vertical ground

reaction forces in adults [19, 20], foot strike patterns during walking and running were

determined by visual inspection of each electronic footprint acquired over the 10 second data

capture period [21-24]. Foot strike patterns were defined based on previous classifications

[23, 25] and the following definitions were adopted: a rearfoot foot strike (RFS) was defined

as a pattern in which the heel made initial ground contact before the ball of the foot; a

forefoot foot strike (FFS) was defined as a pattern in which the forefoot made initial ground

contact; a midfoot foot strike (MFS) was defined as a pattern in which the middle to upper-

middle 1/3 of the foot made initial ground contact before the remaining sole of the foot.

Children that did not display the same consistent footfall pattern (RFS, FFS, or MFS) for

more than 70% of foot strikes within the data capture period were classified as having a

‘varied’ (VFS) foot strike pattern.

Pressure data were exported in ASCII format and custom computer code (Matlab R2012a,

MathWorks, Natick, Massachusetts, USA) was subsequently used to determine key

temporospatial gait parameters. Walking velocity, cadence and step length were normalised

to body height using non-dimensional methods outlined elsewhere [26]. Vertical ground

reaction force was normalized to body weight and the magnitude and timing of conventional

vertical ground reaction force peaks during walking (two dominant peaks) and running (one

dominant peak) was identified for each step. Peak force loading rate, defined as the peak

instantaneous force differential during the stance phase of gait, was also calculated using

previously outlined methods [27]. Maximum pressure footprints were divided into rearfoot,

midfoot and forefoot areas (Figure 7. 2), and peak regional pressures were subsequently

determined [28].

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FIGURE 7.2. Each electronic footprint was masked into hindfoot, midfoot and forefoot

segments using proprietary software. The maximum plantar pressure in each segment was

recorded for each footfall and averaged over 10 seconds of steady-state barefoot walking and

running.

Statistical analysis was performed using IBM-SPSS statistical software (Version 21 for

Windows IBM Corp. Armonk, NY, USA). All data were evaluated for normality using the

Shapiro Wilk test. As outcome variables were determined to be normally distributed, means

and standard deviations have been used as summary statistics. Paired t-tests were used to

evaluate potential between-group differences in body anthropometry (height and weight).

Foot strike frequency distributions during running were compared between groups using the

maximum likelihood ratio Chi-square test. A 2 (gait) x 2 (group) mixed ANOVA model was

used to investigate main effects for ‘group’ and its interactions with ‘gait’ for vertical ground

reaction force, regional plantar pressure and temporospatial gait parameters. Whereby,

‘group’ (case, control) was treated as the between-subjects factor, and ‘gait’ (walk, run) was

treated as the within-subject factor. Underlying assumptions regarding the uniformity of the

variance–covariance matrix were assessed using Mauchly test of sphericity. When the

assumption of uniformity was violated, an adjustment to the degrees of freedom of the F-ratio

was made using Greenhouse–Geisser Epsilon, thereby making the F-test more conservative.

Post hoc t-tests were used to investigate significant gait by group interactions. Potential

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relationships among pain, vertical ground reaction force, regional plantar pressure and

temporospatial gait parameters were investigated using scatter plots and Pearson product-

moment correlations. An alpha level of .05 was used for all tests of significance.

7.4 RESULTS

Mean absolute walking speed was 1.07 ± 0.23 m/s in children with CA and 1.06 ± 0.25 m/s in

children without heel pain, while absolute running speed was 1.89 ± 0.23 m/s and 1.91 ± 0.21

m/s, respectively. All participants adopted a RFS pattern during walking. Chi-square analysis

revealed there were no significant differences in the frequency of foot strike patterns in

children with (RFS 10; FFS 2; MFS 1; VFS 1) and without CA (RFS 11; FFS 1; MFS 0; VFS

2) during running (P = .549).

There was no significant difference in vertical ground reaction force or regional plantar

pressure between groups during walking or running (Table 7.2). There was, however, a

significant interaction between ‘group’ and ‘gait’ for normalised step length (F1,26 = 5.559, P

= .026); whereby children with CA had a shorter step length than children without heel pain

during running but not walking. Similarly, cadence, when normalised to body height, was

significantly higher in children with CA than those without heel pain but only during running

(t24=2.38, P = .025).

VAS pain scores for children with CA were significantly correlated only with the maximum

pressure beneath the rearfoot during running (r, 0.77, P = .04) but not walking.

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TABLE 7.2. Mean (SD) temporospatial and kinetic gait parameters during barefoot

walking and running on an instrumented treadmill.

Walk Run

Healthy

Control

Calcaneal

Apophysitis

Healthy

Control

Calcaneal

Apophysitis

n 14 14 14 14

Velocity (statures/sec) 0.27 0.28 0.49 0.49 (0.06) (0.06) (0.04) (0.05)

Cadence (dimensionless) 0.38 0.38 0.55 0.58* (0.04) (0.04) (0.03) (0.03)

Step length (statures) 0.35 0.36 0.44 0.42* (0.04) (0.05) (0.03) (0.04)

Stride duration (sec) 1.08 1.05 0.73 0.68 (0.11) (0.11) (0.04) (0.05)

Stance phase duration (% GC) 62 62 48 46 (1) (2) (4) (4)

Swing phase duration (% GC) 38 38 52 54 (1) (2) (4) (4)

First force peak (BW) 1.3 1.2 2.2 2.2 (0.3) (0.1) (0.5) (0.2)

Time first force peak (% SPD) 28 27 36 37 (3) (4) (3) (4)

Minima force (BW) 1.0 0.9 - -

(0.3) (0.1)

Time minima force (% SPD) 48 47 - -

(4) (3)

Second force peak (BW) 1.3 1.2 - -

(0.3) (0.1)

Time second force peak (% SPD) 74 75 - -

(3) (4)

Peak force loading rate (BW·s-1) 0.28 0.31 0.59 0.60 (0.08) (0.08) (0.20) (0.15)

Maximum Pressure Rearfoot (kPa) 230 240 262 242 (66) (34) (67) (89)

Maximum Pressure Midfoot (kPa) 157 145 158 157 (43) (25) (37) (30)

Maximum Pressure Forefoot (kPa) 265 237 268 252 (74) (37) (64) (65)

BW, body weight; GC, gait cycle; SPD, stance phase duration. kPa, kilopascal.

*Indicates a statistically significant difference between children with and without calcaneal

apophysitis for the given gait speed (P < .05).

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7.5 DISCUSSION

This study evaluated loading beneath the foot in children with and without CA during

treadmill walking and running. Contrary to our hypothesis, neither maximum pressure

beneath the heel nor vertical ground reaction force parameters differed significantly between

groups during treadmill walking and running. Although the findings are at odds with previous

studies evaluating plantar pressures during standing and walking [4, 8], children with CA in

the current study had a significantly higher cadence during running than children without heel

pain.

The observation that children with CA in this research were characterized by an increased

cadence when normalized to height during running (≈5%) is consistent with an overuse

repetitive injury model [29], in which an increase in the repetition of loading is one

mechanism thought to result in the accumulation of fatigue damage at the calcaneal physis

[30]. However, it is also possible that children with CA may have adopted a higher cadence

to ameliorate peak loads and pain beneath the heel during running. In support of such a

concept, an increase in cadence as little as 5% in adults has been reported to lower heel

loading during running by 2.2% over time [31]. Further, in the current study, self-reported

pain in children with CA was moderately correlated with peak rearfoot pressure during

running; suggesting a potential antalgic gait response at the higher gait speed. It should be

noted, however, that self-reported pain was not significantly correlated with cadence in

children with CA during treadmill running.

Previous research has suggested that foot strike patterns may also influence the magnitude of

peak vertical ground reaction force parameters during running in adults [32, 33]. In the

current study, there was no significant difference in the frequency of foot strike patterns in

children with and without heel pain. The majority of children (75 %) adopted a RFS pattern

during barefoot treadmill running, which is similar to previous research involving children

and adolescent populations of similar age, in which the prevalence of RFS during barefoot

treadmill/overground running was ≈ 62 % [32, 34].

There are some limitations in the current study which should be considered when interpreting

the results. Firstly, this is a cross sectional study and hence causal relationships cannot be

drawn. While it is possible that children with heel pain make gait adjustments in order to

maintain consistent loading beneath the foot and potentially avoid pain [35], it is also

possible that these differences in gait may contribute to the development of CA through more

frequent loading. Future research evaluating loading beneath the foot during running with

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manipulation of cadence or longitudinal studies monitoring loading with resolution of CA

would seem useful approaches to provide further insight into potential causality. Secondly,

there is some evidence that treadmills may induce minor changes in temporospatial and

kinetic gait parameters in healthy children when compared to overground walking [36].

While children with and without CA participated in the same structured treadmill

familiarization process in the current study, it is possible the differences observed in cadence

may not be directly transferable to overground gait conditions. Finally, although the age

range of children investigated in the current study is consistent with that reported previously

in CA [37, 38], pubertal status is known to influence neuromotor performance in adolescence

[39]. Hence it is recommended that potential effects of pubertal status and sex be considered

in future investigations when matching participants.

7.6 CONCLUSION

The present research identified no significant differences in peak vertical ground reaction

force or peak plantar pressures in children with and without CA during walking or running.

However, children with CA adopted a higher cadence than children without heel pain during

running. While the findings suggest that children with CA may alter their cadence to

modulate loading beneath the heel and, hence pain, they also highlight the importance of

assessing running as opposed to walking gait patterns in children with painful CA.

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7.7 REFERENCES

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[2] L.J. Micheli, M.L. Ireland, Prevention and management of calcaneal apophysitis in

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[5] C.C. Madden, M.B. Mellion, Sever's disease and other causes of heel pain in adolescents,

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[6] M. Diop, A. Rahmani, A. Belli, V. Gautheron, A. Geyssant, J. Cottalorda, Influence of

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[8] R. Becerro de Bengoa Vallejo, M.E. Losa Iglesias, D. Rodriguez Sanz, J.C. Prados

Frutos, P. Salvadores Fuentes, J.L. Chicharro, Plantar pressures in children with and

without Sever’s disease, J Am Podiatr Med Assoc 101(1) (2011) 17-24.

[9] A.P. Ribeiro, S.M.A. João, R.C. Dinato, V.D. Tessutti, I.C.N. Sacco, Dynamic patterns

of forces and loading rate in runners with unilateral plantar fasciitis: A cross-sectional

study, PloS one 10(9) (2015) e0136971.

[10] A.M. James, C.M. Williams, M. Luscombe, R. Hunter, T.P. Haines, Factors associated

with pain severity in children with calcaneal apophysitis (Sever Disease), J Pediatr

167(2) (2015) 455-459.

[11] S. Perhamre, D. Lazowska, S. Papageorgiou, F. Lundin, M. Klässbo, R. Norlin, Sever’s

Injury: a clinical diagnosis, J Am Podiatr Med Assoc 103(5) (2013) 361-368.

[12] C.M. Rerucha, C. Dickison, D.C. Baird, C.R. Darnall, Lower extremity abnormalities in

children, Am Fam Physician 96(4) (2017) 226-233.

[13] J. Wu, T. Ajisafe, Kinetic patterns of treadmill walking in preadolescents with and

without Down syndrome, Gait Posture 39(1) (2014) 241-246.

[14] L.F. Reed, S.R. Urry, S.C. Wearing, Reliability of spatiotemporal and kinetic gait

parameters determined by a new instrumented treadmill system, BMC Musculoskelet

Disord 14(1) (2013) 1-10.

[15] O. Faude, L. Donath, R. Roth, L. Fricker, L. Zahner, Reliability of gait parameters during

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treadmill walking in community-dwelling healthy seniors, Gait Posture 36(3) (2012)

444-448.

[16] S.C. Wearing, L. Reed, S.L. Hooper, S. Bartold, J.E. Smeathers, T. Brauner, Running

shoes increase achilles tendon load in walking: an acoustic propagation study, Med Sci

Sports Exerc 46(8) (2014) 1604-1609.

[17] V. Lavcanska, N.F. Taylor, A.G. Schache, Familiarization to treadmill running in young

unimpaired adults, Hum Mov Sci 24(4) (2005) 544-557.

[18] T. Oberg, A. Karsznia, K. Oberg, Basic gait parameters: reference data for normal

subjects, 10-79 years of age, J Rehabil Res Devel. 30 (1993) 210-223.

[19] M.H Schwartz, A. Rozumalski, J.P. Trost, The effect of walking speed on the gait of

typically developing children, J Biomech 41(8) (2008) 1639-1650.

[20] D. Liddle, K. Rome, T. Howe, Vertical ground reaction forces in patients with unilateral

plantar heel pain—a pilot study, Gait Posture 11(1) (2000) 62-66.

[21] A.H. Gruber, K. Boyer, J.F. Silvernail, J. Hamill, Comparison of classification methods

to determine footfall pattern, Footwear Sci 5(sup1) (2013) S103-S104.

[22] A.R. Altman, I.S. Davis, A kinematic method for footstrike pattern detection in barefoot

and shod runners, Gait Posture 35(2) (2012) 298-300.

[23] D.E. Lieberman, What we can learn about running from barefoot running: an

evolutionary medical perspective, Exerc Sport Sci Rev 40(2) (2012) 63-72.

[24] M.E. Kasmer, X.-c. Liu, K.G. Roberts, J.M. Valadao, Foot-strike pattern and

performance in a marathon, Int J Sports Physiol Perform 8(3) (2013) 286-292.

[25] B. Breine, P. Malcolm, V. Segers, J. Gerlo, R. Derie, T. Pataky, et al., Magnitude and

spatial distribution of impact intensity under the foot relates to initial foot contact pattern,

J Appl Biomech 33(6) (2017) 431-436.

[26] B.W. Stansfield, S.J. Hillman, M.E. Hazlewood, A.M. Lawson, A.M. Mann, I.R.

Loudon, et al., Normalisation of gait data in children, Gait Posture 17 (2003) 81-87.

[27] A.L. Revill, S.D. Perry, A.M. Edwards, J.P. Dickey, Variability of the impact transient

during repeated barefoot walking trials, J Biomech 41(4) (2008) 926-930.

[28] S.C. Wearing, J.E. Smeathers, S.R. Urry, A comparison of two analytical techniques for

detecting differences in regional vertical impulses due to plantar fasciitis, Foot Ankle Int

23 (2002) 148-154.

[29] B.L. Sih, W. Shen, J.H. Stuhmiller, Overuse Injury Assessment Model, US Army

Medical Research and Materiel Command Jaycor Technical Report J3181-03-192, San

Diego, CA, 2003.

[30] A. Herbaut, P. Chavet, M. Roux, N. Guéguen, F. Barbier, E. Simoneau-Buessinger, The

influence of shoe aging on children running biomechanics, Gait Posture 56 (2017) 123-

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128.

[31] J. Wellenkotter, S. Meardon, T. Kernozek, T. Suchomel, The effects of running cadence

manipulation on plantar loading, J Orthop Sports Phys Ther 43(1) (2013) A140-A141.

[32] D.E. Lieberman, M. Venkadesan, W.A. Werbel, A.I. Daoud, S. D'Andrea, I.S. Davis, et

al., Foot strike patterns and collision forces in habitually barefoot versus shod runners,

Nature 463 (7280) (2010) 531-535.

[33] H. Rice, M. Patel, Manipulation of foot strike and footwear increases Achilles tendon

loading during running, Am J Sports Med 45(10) (2017) 2411-2417.

[34] P.Á.L. Román, F.R. Balboa, F.G. Pinillos, Foot strike pattern in children during shod-

unshod running, Gait Posture 58 (2017) 220-222.

[35] S.E. Robbins, A.M. Hanna, G.J. Gouw, Overload protection: avoidance response to

heavy plantar surface loading, Med Sci Sports Exerc 20(1) (1988) 85-92.

[36] A. Rozumalski, T.F. Novacheck, C.J. Griffith, K. Walt, M.H. Schwartz, Treadmill vs.

overground running gait during childhood: a qualitative and quantitative analysis, Gait

Posture 41 (2015) 613-618.

[37] R.W. Scharfbillig, S. Jones, S.D. Scutter, Sever’s disease: what does the literature really

tell us?, J Am Podiatr Med Assoc 98(3) (2008) 212-223.

[38] C.L. Hendrix, Calcaneal apophysitis (Sever disease), Clin Pod Med Surg 22(1) (2005)

55-62.

[39] F.B Ortega, J.R. Ruiz, M.J. Castillo, L.A. Moreno, A. Urzanqui, M. González-Gross, et

al., AVENA Study Group. Health-related physical fitness according to chronological and

biological age in adolescents. The AVENA study, J Sports Med Phys Fitness 48 (2008)

371-9.

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CHAPTER 8 ULTRASOUND VELOCITY IN THE ACHILLES TENDON OF

CHILDREN WITH AND WITHOUT CALCANEAL APOPHYSITIS DURING

RUNNING

Forming the third section of the experimental phase of this research, this study addressed

research aim 3 (chapter 3) to assess the mechanical properties of the Achilles tendon and

dynamic ankle movement in children with and without CA during running. The chapter

contains a manuscript compiled in an ‘original research article’ format.

Contributions of co-authors:

S. McSweeney: contributed to study conception and design, data collection, data analysis and

interpretation, and preparation of the manuscript.

L. Reed: contributed to study conception and design, data analysis and interpretation, and

preparation of the manuscript.

S. Wearing: contributed to study conception and design, data analysis and interpretation, and

preparation of the manuscript.

The co-authors have certified that:

1. they meet the criteria for authorship in that they have participated in the conception, execution, or

interpretation, of at least that part of the chapter in their field of expertise (as described);

2. they take public responsibility for their part of the chapter, except for the responsible author who accepts

overall responsibility for the chapter;

3. there are no other authors of the chapter according to these criteria;

4. potential conflicts of interest have been disclosed to (a) granting bodies, (b) the editor or publisher of

journals, and (c) the head of the responsible academic unit, and

5. they agree to the use of the chapter in the student’s thesis and its publication on the QUT’s ePrints site

consistent with any limitations set by publisher requirements.

Simon McSweeney 12 December 2018

Lloyd Reed 12 December 2018

Scott Wearing 12 December 2018

QUT Verified Signature

QUT Verified Signature

QUT Verified Signature

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8.1 ABSTRACT

Background:

Micro-damage of the developmental physis is generally considered pathognomonic of

calcaneal apophysitis (CA). Altered properties of the Achilles tendon with growth have been

clinically implicated in development of the injury. However to date, there has been minimal

research characterizing functional properties of the Achilles tendon in CA. This study used

transmission-mode ultrasound, a measure of the instantaneous elastic properties of tendon, to

compare the functional properties of the Achilles tendon in children with and without CA

during running.

Methods: A custom-built transmission-mode ultrasound system was used to characterise the

axial transmission velocity of ultrasound in the right Achilles tendon of children with (n = 9;

mean ± SD age 11±1 years) and without (n = 9; mean ± SD age 12±2 years) CA during

barefoot running at self-selected speed. Sagittal ankle movement, temporospatial gait

parameters and peak vertical ground reaction forces were also determined using an

electrogoniometer and instrumented treadmill system, respectively. Paired t-tests were used

to evaluate potential between-group differences in peak ultrasound velocity, sagittal ankle

movement, vertical ground reaction force and temporospatial gait parameters, including

cadence, step length and stance duration. Self-reported pain was assessed with a standard

VAS pain scale. Scatter plots and Pearson product-moment correlations were used to

investigate potential relationships among biomechanical parameters and pain.

Results: There were no statistically significant differences in peak ultrasound velocity in the

Achilles tendon or peak vertical ground reaction force between groups. However, children

with CA adopted a higher cadence (t16 = 3.097, P = .00, d = 1.50), shorter stance phase

duration (t16 = 2.026, P = .05, d = 1.00), and had greater peak ankle dorsiflexion (t13 = 2.424,

P = .03, d = 1.56) during running than children without heel pain. Self-reported pain was

negatively correlated with peak ankle dorsiflexion (r, -0.95, P <.01) and positively correlated

with peak vertical ground force (r = 0.89, P =.01) in children with CA.

Conclusion: Despite children with CA having a higher cadence and greater ankle

dorsiflexion than those without heel pain, peak ultrasound velocity, and hence the

instantaneous material stiffness of the Achilles tendon was not significantly different in

children with and without CA. Ankle joint dorsiflexion and peak vertical ground reaction

force during running were, however, associated with self-reported pain in CA, and represent

an avenue for future research in these children.

Keywords: Sever’s disease; quantitative ultrasound; speed of sound; paediatric gait.

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8.2 INTRODUCTION

Calcaneal apophysitis (CA) is a common cause of activity-related heel pain in children and is

widely regarded as an overuse injury of the cartilaginous-layer of the calcaneal apophysis. 1

Although poorly understood, micro-damage of the physis is generally considered

pathognomonic and, in part, is believed to reflect a change in the functional properties of

Achilles tendon with growth. 2, 3 While altered mechanical properties of the Achilles tendon

have been implicated in overuse achillodynia in adults, 4 evidence that tendon properties may

also be altered in children with traction apophysitis of the calcaneus is lacking.

Estimates of Achilles tendon properties in children are commonly undertaken using indirect

measurement techniques during quasistatic isometric loading conditions. 2, 5 Although

insightful, this approach has been found to overestimate tendon properties by as much 50%

when compared with direct estimates. 6 Transmission mode ultrasound is emerging as an

alternative method for the non-invasive measurement of tendon properties during activities of

daily living. 7 The operational principle of the transmission technique is described in detail

elsewhere, 8 but is governed by the observation that the axial transmission velocity of

ultrasound in tendon is dependent on its instantaneous elastic modulus (material stiffness),

which in turn, is related to the applied tensile load. 7, 9, 10 Hence, by taking advantage of the

nonlinear properties of tendon, the technique is capable of evaluating tendon properties

during dynamic activities 7, 11, 12 and has been shown to be sufficiently sensitive to detect

changes in instantaneous Achilles tendon properties with gait speed, 11 tendon injury, 13 and

footwear intervention. 14, 15 Moreover, the technique is particularly attractive for evaluating

Achilles tendon properties in CA, as it can be used during relatively high impact activities,

such as running, which clinically have been linked to the development of CA.16

The primary aim of the current study, therefore, was to use transmission-mode ultrasound to

assess the functional properties of the Achilles tendon during running in children with and

without CA. Given that axial transmission velocity of ultrasound is related to the

instantaneous material stiffness of tendon, 17 and that heightened tendon stiffness has been

implicated in traction apophysitis, 2 it was hypothesised that ultrasound velocity in the

Achilles tendon would be higher in children with CA than in children without heel pain.

Additionally, as axial transmission velocity of ultrasound in the Achilles tendon is also

closely coupled with sagittal movement of the ankle joint, 12 it was hypothesised that axial

transmission velocity of ultrasound in children with CA would be accompanied by lower

ankle dorsiflexion during running. 18

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8.3 METHODS

8.3.1 Participants

Eighteen children, aged 8-14 years (nine cases and nine healthy children), were recruited via

direct referral from health-care providers and local sporting clubs. CA was clinically

diagnosed based on established criteria, including a comprehensive medical history and

clinical examination, in which symptoms were replicated with medial and lateral compression

of the calcaneal apophysis (squeeze test). 19, 20 Exclusion criteria for all participants included

poorly-defined calcaneal symptoms, a history of calcaneal fracture, tumour or surgery of the

foot within the last 12 months, overt orthopaedic abnormalities of the foot or lower limb and

a medical history of autoimmune, neurological, vascular, metabolic or endocrine disorders.

Current or past treatment for CA were not exclusion criteria for this study. Of the nine

children with CA, eight were male and one was female (mean ± SD age 11±1 years; height

155±11 cm; weight 45±7 kg). All children with CA presented with bilateral pain. For the

purpose of this study, only the right foot was considered. Heel pain was exacerbated by

physical activity and had been present for at least 8 weeks in all cases. The median duration

of symptoms experienced by participants prior to assessment was 13 months (range, 6-48

months). The six male and three female participants that formed the control group were

individually matched on age (± 3 years) and were free of lower limb pain and pathology

(mean ± SD age 12±2 years; height 158±14 cm; weight 51±18 kg).

In the absence of published measures of ultrasound velocity in a paediatric cohort, participant

numbers for this preliminary investigation in children were based on previously published

data for the Achilles tendon in healthy adults during running (peak ultrasound velocity 2285

± 113 m/s). 12 Participant numbers in the current study were sufficient to detect a 5%

difference in peak ultrasound velocity of the tendon at an alpha (ɑ) level of .05 and beta (β) of

.20. All participants provided written informed consent with their accompanying guardians

before participating in the study, which received approval from the university human research

ethics committee.

8.3.2 Equipment

Ultrasound velocity was measured in the right Achilles tendon using a custom-built

ultrasound system described elsewhere. 11, 14 The ultrasound probe consisted of a 1-MHz

broadband pulse emitter and four regularly spaced receivers (Figure 8.1a). Received

ultrasound signals were digitized at 20 MHz, and the time of flight of the first arriving

transient between receivers was determined. The transmission velocity of ultrasound was

subsequently calculated given the known distance between receivers and the measured time

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of flight. The mean within-subject coefficient of variation for ultrasound velocity maxima

and minima in human Achilles tendon during running has been reported to range between 0.5

and 1.6%. 12

(a) (b)

FIGURE 8.1 (a). Five-element ultrasound probe utilized for ultrasound velocity

measurement in the Achilles tendon. The probe comprises a 1-MHz Emitter (blue*) and four

collinear, regularly spaced receivers (red*). (b) Ultrasound probe attached to the right

Achilles tendon of a child.

A flexible twin-axis strain-gauge electrogoniometer (SG110A, Penny and Giles, Biometrics,

Gwent, UK) was used to measure sagittal ankle movement during running. The

electrogoniometer has been widely used to assess ankle kinematics during gait 21 and has a

reported accuracy of 1.5 % over a measurement range of 100° with a measurement resolution

of 1°. 22

Temporospatial gait parameters and vertical ground reaction forces were determined during

running at self-selected speed using an instrumented treadmill system (FDM–THM–S, Zebris

Medical GmbH, Isny, Germany). The treadmill contained a capacitance-based pressure

platform (108.4 x 47.4 cm) positioned beneath a treadmill belt, which had a contact surface of

150 x 50 cm. The pressure platform had a spatial resolution of approximately 0.85 cm.

Reported coefficients of variation for most repeated measurements of temporospatial gait

*

*

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parameters are reportedly less than 10 % in adults, 23, 24 but have not been reported for

paediatric cohorts.

Heel pain was assessed with a standard 10-cm visual analogue pain scale (VAS) anchored by

the terms “no pain” and “worst pain.” 25 Visual analogue scales have been widely used for the

assessment of pain in children; 26 and are reportedly reliable (ICC 0.85-0.87) for use in

children 5 years of age and older. 27-30

8.3.3 Protocol

Following anthropometric assessment of weight and height, the skin overlying the posterior

Achilles tendon and lateral aspect of the right shank was prepared and cleaned using standard

alcohol abrading methods. 31 The ultrasound probe was then positioned over the midline of

the posterior aspect of the Achilles tendon, with the emitter placed 1 cm above the calcaneal

attachment. The probe was attached using a semi-adhesive coupling gel and further secured

using a non-restrictive brace (EVA 30 closed-cell foam) and elasticized straps (Figure 8.1b).

The end-blocks of the electrogoniometer were then fixed to the skin overlying the lateral

calcaneus and the distal aspect of the fibula of the right ankle, using double-sided adhesive

and surgical tape. 14 Prior to testing, children underwent a treadmill acclimatization session,

which involved a minimum of six minutes of steady-state treadmill running at self-selected

“comfortable” speed. 32 After a further three minutes, ultrasound velocity in the right Achilles

tendon, sagittal ankle movement, temporospatial gait parameters and vertical ground reaction

forces were then recorded during “steady-state” running at self-selected gait speed. Gait

speeds of children without heel pain were individually matched to those with CA (within ≈ 7

%). 33, 34 All data were acquired over 10 seconds of steady-state barefoot running at a

sampling rate of 120 Hz. 14

8.3.4 Data Reduction and Statistical Analysis

As variations in foot strike pattern have been shown to influence peak vertical ground

reaction forces in adults,33, 35 foot strike patterns were determined by visual inspection of each

electronic footprint acquired over the 10 second data capture period.36-39 Foot strike patterns

were defined based on previous research classifications 38, 40 and the following definitions

were adopted: a rearfoot foot strike (RFS) was defined as a pattern in which the heel made

initial ground contact before the ball of the foot; a forefoot foot strike (FFS) was defined as a

pattern in which the forefoot made initial ground contact; a midfoot foot strike (MFS) was

defined as pattern in which the middle to upper-middle 1/3 of the foot made initial ground

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contact before the remaining sole of the foot. Children that did not display the same

consistent footfall pattern (RFS, FFS, or MFS) for more than 70% of footstrikes within the

data capture period were classified as having a ‘varied’ (VFS) foot strike pattern.

Maximum (max) and minimum (min) ultrasound transmission velocities in the Achilles

tendon were determined for each gait cycle during the 10 second data capture period (Figure

8.2). Similarly peak ankle plantarflexion (PF) and dorsiflexion (DF) were also identified for

each gait cycle. Mean values were subsequently calculated over all recorded gait cycles for

each participant, and used in later statistical analysis. An average of 14 ± 1 gait cycles were

analyzed for each participant.

FIGURE 8.2. Ensemble histories for ultrasound velocity recorded in the right Achilles

tendon of a child with CA (gray line) and one healthy child (black line) during barefoot

running at a matched gait speed. Each child displayed a RFS pattern.

Pressure data were exported from the treadmill system in ASCII format and custom computer

code (Matlab R2012a, MathWorks, Natick, Massachusetts, USA) was used to determine key

temporospatial gait parameters including cadence, stride length, stride duration, and stance

and swing phase durations (% gait cycle). Vertical ground reaction force was normalized to

body weight and the magnitude and timing of the peak vertical ground reaction force was

identified for each step. Peak force loading rate, defined as the peak instantaneous force

differential during the stance phase of gait, was also calculated using previously outlined

methods. 41

1500

1600

1700

1800

1900

2000

2100

0 20 40 60 80 100

Ult

raso

un

d v

elo

city

(m

/s)

Gait Cycle %

Max Max

Min

Min

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Statistical analysis was performed using IBM-SPSS statistical software (Version 21 for

Windows IBM Corp. Armonk, NY, USA). All data were evaluated for normality using the

Shapiro Wilkes test. As outcome variables were determined to be normally distributed, means

and standard deviations have been used as summary statistics. Paired t-tests were used to

evaluate potential differences in body height and weight between groups. Foot strike

frequency distributions during running were compared between groups using the maximum

likelihood ratio Chi-square test. Paired t-tests were also used to evaluate potential between-

group differences in ultrasound velocity in the Achilles tendon, sagittal ankle movement,

temporospatial and vertical ground reaction force parameters. Effect size was estimated with

Cohen’s d statistic, in which the mean difference between the groups was divided by the

pooled standard deviation. 42 Values of d between 0.2 and 0.5 represent a small effect,

between 0.5 and 0.8 a medium effect, and higher than 0.8 a large effect. 42 Potential

relationships among pain, ultrasound velocity in the Achilles tendon, sagittal ankle

movement, temporospatial and vertical ground reaction force parameters were investigated

using scatter plots and Pearson product-moment correlations. An alpha level of .05 was used

for all tests of significance.

8.4 RESULTS

Maximum likelihood ratio Chi-square test analysis revealed that there were no significant

differences in the frequency of foot strike patterns in children with (RFS 5; FFS 1; MFS 1;

VFS 2) and without CA (RFS 8; FFS 1; MFS 0; VFS 0) during running (P = .183).

During running the within-subject repeatability of ultrasound velocity and ankle

electrogoniometric measures was highly reproducible from one gait cycle to the next. The

mean within-subject coefficient of variation for ultrasonic maxima and minima ranged

between 0.1 and 1.4%. Additionally, the mean within-subject coefficient of variation for peak

ankle plantarflexion and dorsiflexion was 2° and 1° respectively. There were no statistically

significant differences in maximum and minimum ultrasound velocity in the Achilles tendon,

peak vertical ground reaction force or peak force loading rate between groups (Table 8.1 &

8.2). There was, however, a significant between-group difference in cadence (t16 = 3.097, P =

.00, d = 1.50), stride duration (t16 = 3.137, P = .00, d = 1.25), stance phase duration (t16 =

2.026, P = .05, d = 1.00), swing phase duration (t16 = 2.026, P = .05, d = 1.00), and peak

ankle dorsiflexion (t13 = 2.424, P = .03, d = 1.56) (Table 8.2) (Figure 8.3). Children with CA

had a higher cadence with a shorter stance phase duration and longer swing phase duration,

and greater peak ankle dorsiflexion than children without heel pain.

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Pain assessment was captured on six of the nine case participants who completed the self-

report. Children with heel pain reported a median ‘pain rating’ of 3 cm (range, 1-7 cm). VAS

pain score was negatively correlated with peak dorsiflexion (r = -0.92, P = 0.00) during

running and positively correlated with peak vertical ground reaction force (r = 0.88, P = 0.02)

(Figure 8.4).

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TABLE 8.1. Mean (SD) maxima, minima and range in transmission ultrasound velocity in the right Achilles tendon during barefoot running on an

instrumented treadmill.

Healthy Control (n =9) Calcaneal Apophysitis (n=9) d

Maximum US velocity (m·s-1) 2102 2070 0.41

(93) (56)

Minimum US velocity (m·s-1) 1830 1819 0.11

(121) (55)

Range (Max-Min US velocity m·s-1) 272 251 0.32

(89) (20)

d, Cohen’s effect size statistic

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TABLE 8.2. Mean (SD) temporospatial and kinetic gait parameters during barefoot running on an instrumented treadmill.

Healthy Control (n =9) Calcaneal Apophysitis (n=9) d

Velocity (m/sec) 2.0 2.0 0.00

(0.2) (0.2)

Cadence (strides/sec) 1.39 1.51* 1.50

(0.08) (0.08)

Stride length (m) 1.42 1.30 0.66

(0.17) (0.19)

Stride duration (sec) 0.72 0.67* 1.25

(0.04) (0.04)

Stance phase duration (% GC) 48 45* 1.00

(3) (3)

Swing phase duration (% GC) 52 55* 1.00

(3) (3)

Force peak (BW) 2.1 2.2 0.50

(0.2) (0.2)

Time force peak (% SPD) 36 36 0.00

(4) (4)

Peak force loading rate (BW·s-1) 0.52 0.61 0.55 (0.13) (0.19)

BW, body weight; GC, gait cycle; SPD, stance phase duration; d, Cohen’s effect size statistic.

*Indicates a statistically significant difference between children with and without CA for the given gait speed (P ≤ .05).

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FIGURE 8.3. Mean peak ankle dorsiflexion (DF) and plantarflexion (PF) for children with

CA (gray) and healthy participants (black) during barefoot running on an instrumented

treadmill. Error bars reflect the standard deviation. *Indicates a statistically significant

difference between children with and without CA (P ≤ .05).

20

15

10

5

0

5

10

15

20S

ag

itta

l a

nk

le a

ng

le (

° )

DF

PF

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FIGURE 8.4. Scatter plot with trend lines showing the relationships between self-reported

pain (abscissa) with peak ankle dorsiflexion (left ordinate, gray dots) and self-reported pain

with peak vertical ground reaction force (right ordinate, black dots) during running (n=6).

*Note that six of the nine case participants completed self-report pain.

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8.5 DISCUSSION

This study used transmission-mode ultrasound to investigate Achilles tendon properties in

children with and without CA during treadmill running. Contrary to our hypothesis, we

observed no significant differences in ultrasound velocity in the Achilles tendon of children

with and without heel pain, suggesting that heightened instantaneous material stiffness of the

Achilles tendon was not characteristic of CA. Notably, peak ultrasound velocity values in the

Achilles tendon of children in the present study (≈ 1819–2102 m/s), were lower than those

previously reported in healthy adults (≈ 1950–2311 m/s) during instrumented treadmill

running at similar speeds. 12 While this observation may indicate that the instantaneous

material stiffness of Achilles tendon (which is proportional to applied tensile load) may be

lower in children compared to adults, previous research has suggested that tendon mechanical

properties are matched to the force producing capacity of the muscle, implying that the

instantaneous material stiffness of tendon is strength dependent. 43 Strength gains as a result

of maturation 44 may therefore potentially explain the difference in peak ultrasound velocity

between children of the present work, relative to that reported previously in adults. 12

Children with CA had significantly greater peak ankle dorsiflexion (≈ 4°) during running than

children without heel pain. While previous research has also reported greater ankle

dorsiflexion in children with CA when measured with the weight-bearing ‘lunge’ test, 19, 45

the finding is in direct contrast to other studies assessing passive ankle dorsiflexion range of

motion in children with CA. 46, 47 It is noteworthy that pain associated with CA in the current

study was negatively correlated (r2 = 90%) with peak ankle dorsiflexion during running.

Hence, while CA was characterised by greater ankle dorsiflexion during running, greater

ankle dorsiflexion was parenthetically associated with lower levels of self-reported pain.

Although the present experimental design does not allow for a mechanistic explanation for

the observed relationship, Finni et al. 48 proposed that the internal loading of a muscle–tendon

unit, and hence the instantaneous material stiffness of the tendon, is dependent on both the

amplitude of movement of the joint and contraction intensity of the corresponding muscle.

Given that the triceps surae muscle complex is thought to primarily control the amount of

dorsiflexion at the ankle joint during running; 49 it is possible that children with CA may not

activate the triceps surae to the same intensity as children without heel pain. Although it may

be argued that the lower peak ultrasound velocity observed in the Achilles tendon of children

with CA is consistent with such a concept, it should be noted that in the current study the

difference in ultrasound velocity between groups was not statistically significant.

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Alternatively, it is also possible that greater ankle dorsiflexion in children with CA may be

associated with greater flexion at the knee. Greater knee flexion would assist in maintaining

triceps surae muscle-tendon unit length and is consistent with the observation that ultrasound

velocity within the Achilles tendon did not differ between groups. Although this study did not

evaluate knee or hip kinematics, it is recommended that future research evaluate the relative

roles of knee and hip movement and muscle activity on Achilles tendon loading profiles in

these children.

This study has a number of limitations. Firstly, while this research specifically characterized

the instantaneous material properties of the Achilles tendon as a whole, it did not quantify the

morphology of the tendon which may influence its structural properties. The technique, in its

current form, does not allow quantification of component (fascicular) properties of the

Achilles tendon. 50 Secondly, it is known that rearfoot pronation is coupled with ankle

dorsiflexion, 51-53 and may result in significantly more recordable dorsiflexion arising from

midfoot movement during assessment of the ankle. In this study, utilizing an

electrogoniometer attached to the calcaneus minimized this effect. Depending on the model,

quantification of rearfoot movement in 3D may provide more insight into potential

mechanisms underlying the observations in this study. As the triceps surae is a biarticular

muscle, quantification of knee joint movement may also prove insightful for future research.

Thirdly, it is noted that six of the nine case participants in this research completed self-report

pain, and hence, the significant findings relating pain to peak ankle dorsiflexion and peak

vertical ground reaction force during running in children with CA seemingly requires further

investigation in larger cohorts. Finally, participants in the present study were matched on age

(±3 years). Although it is controversial as to whether growth-related changes in Achilles

tendon properties may occur over this time frame, 2, 5 careful matching of children on

pubertal status, sex, and height may need to be considered in future investigations.

Nonetheless, the findings of the current study suggest that the instantaneous material

properties of the Achilles tendon are not heightened in CA but rather heightened cadence and

greater ankle dorsiflexion during running are characteristic of the condition.

8.6 CONCLUSION

Peak ultrasound velocity in the Achilles tendon was not significantly different in children

with and without CA, suggesting that heightened material stiffness of the tendon is not

characteristic of the condition. However, children with CA have a higher cadence and greater

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ankle dorsiflexion during running than children without heel pain. Self-reported pain was

inversely related to peak ankle dorsiflexion and positively related to peak vertical ground

reaction force during running. How greater ankle joint dorsiflexion is coupled with increased

cadence but in the absence of increased loading in the Achilles tendon represents an exciting

new avenue for future research.

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53. Tiberio D, Bohannon R, Zito M. Effect of subtalar joint position on the measurement of

maximum ankle dorsiflexic. Clin Biomech (Bristol, Avon). 1989;4(3):189-191.

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CHAPTER 9 GENERAL DISCUSSION

CA is a paediatric foot condition involving pain of the calcaneal apophysis; a cartilaginous

growth center onto which the Achilles tendon inserts. 3, 13, 20 The condition commonly affects

children between the ages of 7 and 15 years, prior to skeletal maturity. 3-7 Classified as an

overuse syndrome, CA is thought to result from repetitive microtrauma of the apophysis,

arising secondary to heel strike or tension within the Achilles tendon, or both, during periods

of heightened physical activity and rapid growth. 1, 2 However, few studies have evaluated

biomechanical factors related to CA, particularly during relatively high-impact activities,

such as running, to which the condition has been often clinically linked. 33 This thesis, aimed

to evaluate several biomechanical factors clinically implicated with the injury. Foot mobility

and stiffness, vertical ground reaction force, Achilles tendon properties, and dynamic ankle

range of movement in children with and without CA were evaluated for the first time to our

knowledge.

This chapter discusses the methodological issues, clinical implications, limitations of the

work as a whole and provides recommendations for future research.

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9.1 METHODOLOGICAL ISSUES

While the reliability of measures of FMM and FS in children were similar to those reported

previously in adults, 130, 131 mean FMM scores in children were substantially lower than

that of adult FMM scores reported previously, suggesting that children may have less

flexible feet than adults 130 In contrast, FS scores for children were consistent with the

lower limits of those reported for adults, suggesting that adults have a stiffer foot

structure than children. 132 As FMM is determined from displacements and not

normalized to body size, it was concluded that FMM may be subject to scalar,

developmental or maturational factors.133 Subsequently, a small exploratory

investigation of radiographic FMM was undertaken (Chapter 5). The exploratory

study found that the contribution of soft tissue deformation to FMM measurement

was substantial but also highly variable between individuals. This initial work duly

considers and cautions the broader interpretation (osseous vs soft tissue movement) of

clinical FMM measurement as a composite measure of foot mobility, and raises doubts as to

its accuracy. Further research is clearly needed to validate this measurement

procedure for application in the clinical setting. Notably, the importance of

establishing limits of agreement for FMM measurement was highlighted in Chapter

4, which insightfully found the small but statistically significant between-group

difference in FMM of children with and without CA to fall within the observed

measurement error.

As shown in Chapter 6, the within day repeatability of children’s temporospatial gait

parameters and vertical ground reaction forces during instrumented treadmill walking and

running at self-selected speeds were highly repeatable (SEM typically <5%). Considering the

use of instrumented treadmill systems for characterizing children’s gait in both the clinical

and research settings is ever-increasing, 134 it is surprising that published evidence on the

reliability of such systems for measuring children’s gait is lacking. The study presented in

Chapter 6 addressed this apparent deficit in the literature. Furthermore, the work has provided

clinicians and researchers with an indication of the reliability and sensitivity of these

instrumented treadmill systems to detect changes in common gait parameters in children

during walking and running. Moreover, the study fundamentally assisted the interpretation of

statistically significant between-group differences in cadence during walking and running of

children with and without CA later evidenced in Chapter 7 and 8 of this thesis.

Finally, the within-subject repeatability of measuring ultrasound velocity of the Achilles

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tendon and also ankle electrogoniometric measures in children was found to be highly

reproducible from one gait cycle to the next during the experiment described in Chapter 8. It

was particularly important to establish these reliability estimates considering transmission

mode ultrasound is less commonly used in biomechanics and has not been published in

children to date. Additionally, differences in dynamic ankle movement between children with

and without CA, as determined by a flexible strain-gauge electrogoniometer, were evaluated

for the first time to our knowledge in this paediatric cohort.

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9.2 CALCANEAL APOPHYSITIS

This thesis aimed to evaluate several of the commonly purported biomechanical risk factors

clinically linked to CA. As such, the work has provided greater insight into the specific

factors of foot mobility and stiffness, vertical ground reaction force, Achilles tendon

properties and dynamic ankle movement during running in children with the condition. In

doing so it has raised a number of questions for further clinical consideration.

As described in Chapter 1, CA is widely regarded to be an overuse injury in which repetitive

micro-movement between the calcaneal apophysis and body results in microtrauma and

inflammation of the chondral bone plate of the apophysis. 2, 20, 23, 40, 56-58 The mechanisms

clinically attributed to injury development are traction within the Achilles tendon and the

opposing plantar fascia and/ or repetitive loading associated with heel strike amid periods of

increased physical activity. 1, 2 With reference to Figure 9.1, interestingly, the results of the

present research challenge several of the associated factors commonly linked to the

development of CA and unequivocally highlight the complexity of this paediatric injury.

It is particularly noteworthy to acknowledge that Sever 1 himself identified altered foot

mobility in children with CA more than 100 years ago. To the best of our knowledge,

however, the present body of research is the first to date that has specifically evaluated the

magnitude of foot mobility and stiffness in these children. Interestingly, the findings of this

investigation demonstrated no meaningful difference in quasi-static measures of FMM or FS

in children with and without the condition, questioning the rationale behind conventional

clinical interventions which typically aim to modify FMM and FS in children with CA.19, 25, 42

As there are many factors (i.e timing, location and magnitude of forces acting on the body)

beyond quasi-static mobility that may moderate or facilitate the foot to move in the context of

walking, running and jumping, 135 it was important to further evaluate dynamic gait

parameters in these children, during conditions that impart higher extrinsic forces on the

body. 135

Despite being frequently clinically linked to the development of CA, 2, 18, 23, 25, 84 until the

present body of work, no research had examined vertical ground reaction forces during gait in

children with and without the condition, nor had there previously been any investigations

quantitatively assessing Achilles tendon properties or dynamic ankle range of movement

specifically during running in this paediatric cohort. This was particularly remarkable, given

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the well-known clinical link between dynamic activities such as running and jumping and

children suffering CA. 33 Hence, the subsequent experimental studies in this program of

research aimed to address these knowledge gaps.

Differences in dynamic peak vertical ground reaction force parameters and also maximum

plantar pressures beneath the heel were evaluated during walking and, for the first time,

during running. Evaluation of plantar pressures and vertical ground reaction force during

walking was undertaken as it allowed direct comparison to previous work evaluating plantar

pressures in children with CA. 17 In contrast to the previous study, which encompassed over

ground walking with a ‘two step’ gait protocol and no detail of the participants self-selected

walking speeds, the current research has collectively shown that dynamic peak vertical

ground reaction force parameters and maximum plantar pressures were not different in

children with and without symptomatic CA. Despite this, both peak rearfoot pressure

(Chapter 7) and peak vertical ground reaction force (Chapter 8) were positively related to

pain specifically during running. Hence, it could be argued that dynamic peak vertical ground

reaction force parameters and maximum plantar pressures beneath the heel are in fact

aggravating factors for the condition of CA (FIGURE 9.1), rather than inciting factors as

widely clinically purported.

Non-invasive transmission-mode ultrasound technology was utilized for the assessment of

mechanical properties of the Achilles tendon in children with and without CA specifically

during running. This is of notable significance considering the technique permitted an

evaluation of functional Achilles tendon properties in CA, which are clinically implicated in

the development of the injury, rather than adopting conventional indirect measurements under

quasi-static loading conditions. Additionally, differences specifically in dynamic ankle

movement between children with and without CA were also investigated building upon the

current body of knowledge encompassing ankle movement in these children, which has

conventionally been assessed through static measurements. With reference to Figure 9.1, the

findings of the research have demonstrated that peak ultrasound velocity in the Achilles

tendon during running, a measure of the instantaneous material stiffness of the tendon, was

not clinically different in children with and without CA. However, children with CA had

greater ankle dorsiflexion (≈ 4°) than those without heel pain during running despite adopting

a similar foot strike pattern. While this later finding is contrary to common clinical dogma,

self-reported pain in children with CA in the present work was inversely associated with peak

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ankle dorsiflexion during running. On the assumption that increased ankle dorsiflexion does

not represent a treatment effect, it could be argued that heightened dynamic ankle motion

may be a risk factor for the condition or possibly a method to modify pain. Additionally,

consistent with the observation that ultrasound velocity within the Achilles tendon did not

differ between groups, it is speculated that children with CA possibly increase flexion of the

knee during running in order to maintain triceps surae muscle-tendon unit length with greater

ankle dorsiflexion.

Together, the findings of this program of research may question the rationale behind current

treatments aimed at modifying foot mobility and improving functional Achilles tendon

properties through enhanced ankle dorsiflexion in CA. Moreover, the findings suggest that

symptom severity in these children during running may be linked to heightened ankle

dorsiflexion, lower peak vertical ground reaction force and peak plantar pressure. Finally, of

the two studies that evaluated cadence in this thesis, both demonstrated a consistently higher

cadence in children with CA during running. Given the cross-sectional nature of these

studies, it is unclear if higher cadence reflects gait adaptations in people with CA or a pre-

existing risk factor for the development of the repetitive over use injury. The findings of this

thesis further highlight the importance of assessing gait patterns in children with CA, and

highlight the need for systematic prospective studies that evaluate lower extremity

biomechanics during dynamic activities, such running, in this paediatric cohort.

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Intrinsic factors

Extrinsic factors

gggg

Postulated mechanisms

FIGURE 9.1. Flow chart illustrating considerations for the current mechanistic model of calcaneal apophysitis.

Trauma (indirect)

Surface properties

Footwear

Activity levels

Tension

Achilles

Triceps surae tightness

Biomechanical foot malalignment

Ankle joint range of motion

Altered Achilles tendon properties

Body Mass Index

Vertical ground reaction force*

Peak plantar pressures*

Impact

CA Microdamage

Physis

Pain

Inflammation

Aggravating

factors?

*Dynamic Ankle dorsiflexion?

*Knee flexion?

*Cadence?

Trait considerations

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9.3 LIMITATIONS

This research has a number of limitations. The most notable being the cross sectional study

design does not permit causal relationships to be drawn. Future research, evaluating

associated factors of this condition in children with the resolution of symptoms linked to CA

would seem warranted. Additionally, although current or past treatment for CA were not

exclusion criteria for the studies in this thesis, and participants were at varied stages of

chronic injury, all cases presented with active heel pain at the time of testing. Secondly, this

research aimed to investigate intrinsic biomechanical factors related to CA, and there is a

need for further evaluation of proposed extrinsic factors in subsequent work to gain greater

appreciation of the underlying mechanisms for the injury. Thirdly, the exploratory pilot study

in Chapter 5 suggests that as currently undertaken, clinical measures of FMM and FS may

reflect a combination of both osseous movement and soft tissue deformation with loading.

The relative contribution of soft tissue deformation is likely to be highly variable from

individual to individual and raises questions as to the appropriate clinical

interpretation and application of such measurements. This is further compounded by

the observation that FMM values observed in children (Chapter 4) are 2 times

smaller than those reported in adults. Hence, it is recommended that continued

research be directed toward identifying factors that influence FMM measurement,

and establish the need for age- or size-specific norms, before FMM can be routinely

used for assessment of foot mobility. Accordingly, radiographic FMM analysis in a

larger cohort would seem warranted. Moreover, the relation between quasistatic foot

mobility and stiffness with functional mobility during dynamic tasks such as running

is currently unknown.

Fourthly, ultrasound velocity in the Achilles tendon is difficult to interpret clinically

and would benefit from measuring the effect of tendon dimensions and muscle

activity, which were not quantified in children participating in this research. While

the results of the present research found no significant differences in the functional

properties of the Achilles tendon in children with and without CA, it is recommended that

future studies incorporate an additional quasi-static experimental set-up, in which

tendon properties are evaluated over a range of applied loads and standardized

positions to help delineate inherent between-tendon differences in material

properties. Similarly, while ankle joint dorsiflexion, as quantified in the present

research, provides an indication of the functional range of the joint required to

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undertake a given activity, its interpretation may benefit from the inclusion of a

measure of the total range of motion available at the ankle joint. Moreover,

considering that only ankle joint kinematics were measured in the present research, it

is important to note that the gastrocnemius muscle is bi-articular, crossing both the

ankle and knee joints. Hence the relative timing and magnitude of knee and hip

movement would likely be important for future investigations.

9.4 FUTURE RESEARCH

This thesis has provided greater insight into several factors associated with CA. Ultimately

the aetiology of CA remains poorly understood, and continued research investigating

the pathomechanics of this overuse injury is needed to support evidence-based

rehabilitative therapy. More rigorous and robust evaluations of the clinical traits associated

with CA, may further assist the scrutiny and understanding of the aetiologies and

consequences related to this injury. The present research would indicate that particular

attention should now be drawn to better understanding the significance of cadence

and dynamic ankle joint dorsiflexion in these children. Accordingly, in light of the

observation of the current research that running rather than walking tended to

exaggerate key temporospatial differences in the gait of these children, a prospective

evaluation of running biomechanics encompassing measures of 3D foot, ankle and

lower limb joint kinematics and contact forces, muscle activity and passive joint

range of motion in a larger cohort of children with and without CA is recommended.

Prospective analysis of these gait parameters in children with resolution of symptoms

of CA would also seem warranted to evaluate potential causality. Alternatively,

assessing clinical prognostic factors associated with CA through a longitudinal study

of healthy children who develop the condition is advocated, albeit difficult,

considering the reported incidence of CA is between 2 and 5 cases per thousand

children in the general population. 8

There is a need for continued research investigating the level of uncertainty of the

measurement techniques of paediatric foot mobility and stiffness. Additionally, a dynamic

assessment of foot mobility in children with and without CA is also recommended, and

would further build upon the work presented in this thesis. Exploring relationships

between ultrasound velocity in the Achilles tendon with tendon dimensions and

biomechanical gait parameters during running in this paediatric cohort is advocated.

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Finally, further attention directed towards other components of running activity such

as intensity, frequency, recovery and footwear properties should also be considered

with respect to this paediatric injury too.

9.5 CONCLUSION

This thesis has analyzed a number of clinical factors that have been anecdotally implicated in

CA. While repetitive loading associated with heel strike, tendon load, and factors that

influence both of these variables continue to be purportedly linked to the development of CA,

ultimately, the causes of this condition remain elusive. Through a series of quasi-

experimental studies, the thesis has contributed to the existing scientific knowledge in the

literature to date pertaining to this paediatric injury. The work has provided evidence

indicating that heightened foot mobility is not characteristic of CA. In contrast to previous

research, it has shown that peak vertical ground reaction force under the rearfoot was not

significantly different in children with CA, but may be related to pain and is potentially an

aggravating factor. Similarly, it has shown for the first time that the Achilles tendon of

children with CA does not have higher peak ultrasound velocity and hence instantaneous

material stiffness than that of children without heel pain during the relatively high-impact

activity of running, and that dynamic ankle dorsiflexion is greater in children with CA and

associated with lower levels of self-reported pain. The novel discoveries in this thesis raise a

number of insightful considerations for further research, such as the significance of cadence,

functional ankle movement, and the suspected influence of knee and hip kinematics

in children suffering the condition. This thesis has provided greater insight into proposed

factors associated with CA in children, advocating ongoing deliberation of the current

mechanistic model for CA in both the clinical and research fields.

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APPENDIX A

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University Human Research Ethics Committee (UHREC)

HUMAN RESEARCH ETHICS APPROVAL CERTIFICATENHMRC Registered Committee Number EC00171

Date of Issue: 6/1/16 (supersedes all previously issued certificates)

Prof Scott WearingDear

This approval certificate serves as your written notice that the proposal has met the requirements of the National

Statement on Ethical Conduct in Human Research and has been approved on that basis. You are therefore

authorised to commence activities as outlined in your application, subject to any specific and standard conditions

detailed in this document.

Project Details

Category of Approval:

Approved From: 24/12/2021

Approval Number: 1500001041

Negligible-Low Risk

Project Title:

Approved Until:24/12/2015 (subject to annual reports)

Pathomechanics of Sever's Apophysitis

Chief Investigator: Prof Scott Wearing

Investigator Details

Other Staff/Students:

Investigator Name Type Role

A/Prof Lloyd Reed Internal QUT Associate Supervisor

Mr Simon McSweeney Student Doctoral (Research)

Conditions of Approval

Specific Conditions of Approval:

No special conditions placed on approval by the UHREC. Standard conditions apply.

Standard Conditions of Approval:

1. Conduct the project in accordance with QUT policy, the National Statement on Ethical Conduct in Human

Research (http://www.nhmrc.gov.au/guidelines/publications/e72), the Australian Code for the Responsible

Conduct of Research (http://www.nhmrc.gov.au/guidelines/publications/r39 ), any associated legislation,

guidelines or standards;

2. Gain UHREC approval for any proposed variation (http://www.orei.qut.edu.au/human/var/) to the project

prior to implementation;

3. Respond promptly to the requests and instructions of UHREC;

4. Declare all actual, perceived or potential conflicts of interest;

5. Immediately advise the Office of Research Ethics and Integrity (http://www.orei.qut.edu.au/human/adv/) if:

o any unforeseen development or events occur that might affect the continued ethical acceptability of the

project;

o any complaints are made, or expressions of concern are raised, in relation to the project;

o the project needs to be suspended or modified because the risks to participants now outweigh the

benefits;

o a participant can no longer be involved because the research may harm them; and

6. Report on the progress of the approved project at least annually, or at intervals determined by UHREC. The

Committee may also choose to conduct a random audit of your project.

If any details within this Approval Certificate are incorrect please advise the Research Ethics Unit within 10 days

of receipt of this certificate.End of Document

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