The acute adaptations of normal and pathological human achilles tendons to eccentric and concentric exercise

THE ACUTE ADAPTATIONS OF NORMAL AND PATHOLOGICAL HUMAN ACHILLES
TENDONS TO ECCENTRIC AND CONCENTRIC EXERCISE

Thesis submitted in fulfilment of the
requirements for the award:

Doctor of Philosophy

2011

Nicole Lorraine Grigg
BAppSc (Human Movement)
BHlthSc (Hons) (Human Movement)

Institute of Health and Biomedical Innovation
School of Human Movement Studies
Queensland University of Technology


KEY WORDS
Achilles Tendon, Tendinopathy, Eccentric Exercise, Rehabilitation, Treatment,
Diametral

Strain,

Morphology,

Tendon

Thickness,

Ultrasound,

Sonography,

Echogenicity, Time-Dependent Conditioning, Walking, Electromyography, Ground
Reaction Force, Power Spectral Density, Frequency, Motor Output Variability, Triceps
Surae, Steadiness.

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ABSTRACT
Eccentric exercise is the conservative treatment of choice for mid-portion Achilles
tendinopathy. While there is a growing body of evidence supporting the medium to long
term efficacy of eccentric exercise in Achilles tendinopathy treatment, very few studies
have investigated the short term response of the tendon to eccentric exercise. Moreover,
the mechanisms through which tendinopathy symptom resolution occurs remain to be
established. The primary purpose of this thesis was to investigate the acute adaptations
of the Achilles tendon to, and the biomechanical characteristics of, the eccentric exercise
protocol used for Achilles tendinopathy rehabilitation and a concentric equivalent. The
research was conducted with an orientation towards exploring potential mechanisms
through which eccentric exercise may bring about a resolution of tendinopathy
symptoms. Specifically, the morphology of tendinopathic and normal Achilles tendons
was monitored using high resolution sonography prior to and following eccentric and
concentric exercise, to facilitate comparison between the treatment of choice and a
similar alternative. To date, the only proposed mechanism through which eccentric

exercise is thought to result in symptom resolution is the increased variability in motor
output force observed during eccentric exercise. This thesis expanded upon prior work
by investigating the variability in motor output force recorded during eccentric and
concentric exercises, when performed at two different knee joint angles, by limbs with
and without symptomatic tendinopathy.

The methodological phase of the research focused on establishing the reliability of
measures of tendon thickness, tendon echogenicity, electromyography (EMG) of the
Triceps Surae and the standard deviation (SD) and power spectral density (PSD) of the
vertical ground reaction force (VGRF). These analyses facilitated comparison between
the error in the measurements and experimental differences identified as statistically
significant, so that the importance and meaning of the experimental differences could be
established. One potential limitation of monitoring the morphological response of the
Achilles tendon to exercise loading is that the Achilles tendon is continually exposed to
additional loading as participants complete the walking required to carry out their
necessary daily tasks. The specific purpose of the last experiment in the methodological

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Achilles Tendon Adaptation to Exercise


phase was to evaluate the effect of incidental walking activity on Achilles tendon
morphology. The results of this study indicated that walking activity could decrease
Achilles tendon thickness (negative diametral strain) and that the decrease in thickness
was dependent on both the amount of walking completed and the proximity of walking
activity to the sonographic examination. Thus, incidental walking activity was identified
as a potentially confounding factor for future experiments which endeavoured to monitor

changes in tendon thickness with exercise loading.

In the experimental phase of this thesis the thickness of Achilles tendons was monitored
prior to and following isolated eccentric and concentric exercise. The initial pilot study
demonstrated that eccentric exercise resulted in a greater acute decrease in Achilles
tendon thickness (greater diametral strain) compared to an equivalent concentric
exercise, in participants with no history of Achilles tendon pain. This experiment was
then expanded to incorporate participants with unilateral Achilles tendinopathy. The
major finding of this experiment was that the acute decrease in Achilles tendon thickness
observed following eccentric exercise was modified by the presence of tendinopathy,
with a smaller decrease (less diametral strain) noted for tendinopathic compared to
healthy control tendon. Based on in vitro evidence a decrease in tendon thickness is
believed to reflect extrusion of fluid from the tendon with loading. This process would
appear to be limited by the presence of pathology and is hypothesised to be a result of
the changes in tendon structure associated with tendinopathy. Load induced fluid
movement may be important to the maintenance of tendon homeostasis and structure as
it has the potential to enhance molecular movement and stimulate tendon remodelling.
On this basis eccentric exercise may be more beneficial to the tendon than concentric
exercise. Finally, EMG and motor output force variability (SD and PSD of VGRF) were
investigated while participants with and without tendinopathy performed the eccentric
and concentric exercises. Although between condition differences were identified as
statistically significant for a number of force variability parameters, the differences were
not greater than the limits of agreement for repeated measures. Consequently the
meaning and importance of these findings were questioned. Interestingly, the EMG
amplitude of all three Triceps Surae muscles did not vary with knee joint angle during

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the performance of eccentric exercise. This raises questions pertaining to the functional
importance of performing the eccentric exercise protocol at each of the two knee joint
angles as it is currently prescribed. EMG amplitude was significantly greater during
concentric compared to eccentric muscle actions. Differences in the muscle activation
patterns may result in different stress distributions within the tendon and be related to
the different diametral strain responses observed for eccentric and concentric muscle
actions.

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TABLE OF CONTENTS
KEY WORDS ...................................................................................................................... II
ABSTRACT ........................................................................................................................ III
TABLE OF CONTENTS ........................................................................................................ 6
LIST OF FIGURES ............................................................................................................. 12
LIST OF TABLES ............................................................................................................... 15
LIST OF ABBREVIATIONS ................................................................................................. 16
LIST OF PUBLICATIONS ................................................................................................... 18
STATEMENT OF AUTHORSHIP ......................................................................................... 19
ACKNOWLEDGEMENTS .................................................................................................... 20
1.0

INTRODUCTION ..................................................................................................... 22

2.0

LITERATURE REVIEW........................................................................................... 26

2.1

Introduction ..................................................................................................... 26

2.2

Achilles Tendon Anatomy............................................................................... 26

2.2.1

Musculature ............................................................................................... 26

2.2.2

Fibre Architecture ...................................................................................... 28

2.2.3

Vascularity ................................................................................................. 29

2.2.4

Summary..................................................................................................... 30

2.3

Tendon .............................................................................................................. 31

2.3.1

Composition and Structure ........................................................................ 31

2.3.2

Mechanical Properties ............................................................................... 36

2.3.3

The Influence of Structure on Mechanical Properties ............................... 40

2.4

Load Induced Changes in Tendon Morphology and Interstitial Fluid Flow .
........................................................................................................................... 41

2.4.1

In Vitro Evidence and Proposed Mechanisms ........................................... 41

2.4.2

In Vivo Observations .................................................................................. 46

2.5

Tendinopathy ................................................................................................... 48

2.5.1

Pathophysiology ......................................................................................... 49

2.5.2

Aetiology .................................................................................................... 52

2.6

Treatment for Tendinopathy .......................................................................... 55

2.7

Evidence for the Efficacy of Eccentric Exercise: A Systematic Review ..... 56

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2.7.1

Introduction ................................................................................................ 56

2.7.2

Method........................................................................................................ 56

2.7.3

Results ........................................................................................................ 58

2.7.4

Discussion .................................................................................................. 64

2.8

Characteristics of Eccentric and Concentric Exercise ................................. 68

2.8.1

Force Fluctuations ..................................................................................... 68

2.8.2

EMG: Within Muscle Characteristics ........................................................ 72

2.8.3

EMG: Between Muscle Characteristics ..................................................... 75

2.9
3.0

Summary .......................................................................................................... 76
RESEARCH AIMS AND OBJECTIVES ...................................................................... 78

3.1

Methodological Phase...................................................................................... 79

3.2

Experimental Phase ......................................................................................... 80

4.0

THE RELIABILITY

OF

SONOGRAPHIC MEASUREMENT

FOR

MONITORING

TENDON THICKNESS AND ECHOGENICITY ..................................................................... 81
4.1

Abstract ............................................................................................................ 81

4.2

Introduction ..................................................................................................... 82

4.3

Method .............................................................................................................. 83

4.3.1

Participants ................................................................................................ 83

4.3.2

Procedure ................................................................................................... 84

4.3.3

Sonographic Imaging ................................................................................. 85

4.3.4

Sonographic Image Analysis ...................................................................... 86

4.3.5

Data Analysis ............................................................................................. 86

4.4

Results............................................................................................................... 87

4.5

Discussion ......................................................................................................... 92

4.6

Conclusions ...................................................................................................... 94

5.0

ERRORS

IN THE MEASUREMENT OF

ELECTROMYOGRAPHIC

AND

GROUND

REACTION FORCE PARAMETERS DURING TRICEPS SURAE EXERCISE ......................... 95
5.1

Abstract ............................................................................................................ 95

5.2

Introduction ..................................................................................................... 95

5.3

Method .............................................................................................................. 96

5.3.1

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Procedure ................................................................................................... 96

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5.3.2

Instrumentation .......................................................................................... 97

5.3.3

Data Analysis ............................................................................................. 99

5.3.4

Statistical Analysis ................................................................................... 101

5.4

Results............................................................................................................. 101

5.5

Discussion ....................................................................................................... 102

5.6

Conclusion ...................................................................................................... 103

6.0

INCIDENTAL

WALKING ACTIVITY IS SUFFICIENT TO INDUCE TIME-DEPENDENT

CONDITIONING OF THE ACHILLES TENDON .................................................................. 104

6.1

Abstract .......................................................................................................... 104

6.2

Introduction ................................................................................................... 105

6.3

Methods .......................................................................................................... 106

6.3.1

Participants .............................................................................................. 106

6.3.2

Procedure ................................................................................................. 107

6.3.3

Sonographic Imaging ............................................................................... 107

6.3.4

Image Analysis ......................................................................................... 108

6.3.5

Activity Data Reduction ........................................................................... 109

6.3.6

Statistical Analysis ................................................................................... 110

6.4

Results............................................................................................................. 110

6.5

Discussion ....................................................................................................... 112

6.6

Conclusion ...................................................................................................... 114

7.0

ECCENTRIC CALF MUSCLE EXERCISE PRODUCES A GREATER ACUTE REDUCTION

IN ACHILLES TENDON THICKNESS THAN CONCENTRIC EXERCISE

............................... 115

7.1

Abstract .......................................................................................................... 115

7.2

Introduction ................................................................................................... 116

7.3

Methods .......................................................................................................... 118

7.3.1

Participants .............................................................................................. 118

7.3.2

Procedure ................................................................................................. 118

7.3.3

Exercise Protocol ..................................................................................... 118

7.3.4

Sonographic Imaging ............................................................................... 119

7.3.5

Image Analysis ......................................................................................... 119

7.3.6

Statistical Analysis ................................................................................... 120

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7.4

Results............................................................................................................. 120

7.5

Discussion ....................................................................................................... 122

7.6

Conclusion ...................................................................................................... 125

8.0

THE DIAMETRAL STRAIN RESPONSE ELICITED

BY

ECCENTRIC EXERCISE

IS

REDUCED IN TENDINOPATHY ........................................................................................ 126
8.1

Abstract .......................................................................................................... 126

8.2

Introduction ................................................................................................... 127

8.3

Method ............................................................................................................ 130

8.3.1

Participants .............................................................................................. 130

8.3.2

Procedure ................................................................................................. 131

8.3.3

Exercise Protocol ..................................................................................... 131

8.3.4

Biomechanics ........................................................................................... 132

8.3.5

Sonographic Imaging ............................................................................... 133

8.3.6

Biomechanical Analysis ........................................................................... 134

8.3.7

Sonographic Image Analysis .................................................................... 134

8.3.8

Statistical Analysis ................................................................................... 136

8.4

Results............................................................................................................. 137

8.4.1

Baseline Tendon Characteristics ............................................................. 137

8.4.2

Biomechanics ........................................................................................... 138

8.4.3

Achilles Tendon Diametral Strain............................................................ 141

8.4.4

Diametral Strain and Dorsiflexion Angle ................................................ 145

8.4.5

Achilles Tendon Echogenicity .................................................................. 145

8.5

Discussion ....................................................................................................... 145

8.5.1

Baseline Tendon Characteristics ............................................................. 145

8.5.2

Achilles Tendon Diametral Strain............................................................ 146

8.5.3

Biomechanics of Exercise Performance .................................................. 148

8.5.4

The Time Course of Achilles Tendon Diametral Strain ........................... 149

8.5.5

Achilles Tendon Echogenicity .................................................................. 150

8.5.6

Limitations ............................................................................................... 150

8.6

Conclusions .................................................................................................... 151

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9.0

THE FREQUENCY POWER SPECTRA OF GROUND REACTION FORCE RECORDED

DURING ECCENTRIC EXERCISE IS ALTERED IN ACHILLES TENDINOPATHY............... 152
9.1

Abstract .......................................................................................................... 152

9.2

Introduction ................................................................................................... 153

9.3

Method ............................................................................................................ 155

9.3.1

Participants .............................................................................................. 155

9.3.2

Procedure ................................................................................................. 156

9.3.3

Exercise Protocol ..................................................................................... 156

9.3.4

Instrumentation ........................................................................................ 157

9.3.5

Data Analysis ........................................................................................... 159

9.3.6

Statistical Analysis ................................................................................... 161

9.4

9.4.1

Knee Joint Angle ...................................................................................... 162

9.4.2

SD of the VGRF........................................................................................ 162

9.4.3

PSD of the VGRF ..................................................................................... 163

9.4.4

EMG ......................................................................................................... 168

9.5

Discussion ....................................................................................................... 170

9.5.1

Knee Joint Angle ...................................................................................... 170

9.5.2

Eccentric versus Concentric Exercise ...................................................... 172

9.5.3

Limb ......................................................................................................... 174

9.5.4

Limitations ............................................................................................... 176

9.6
10.0

Results............................................................................................................. 162

Conclusions .................................................................................................... 176
GENERAL DISCUSSION ........................................................................................ 178

10.1 Methodological Issues ................................................................................... 179
10.2 Experimental Findings................................................................................... 181
10.2.1

Acute Morphological Adaptations to Eccentric and Concentric Exercise ....
.................................................................................................................. 181

10.2.2

Biomechanical Characteristics of Eccentric and Concentric Exercise ... 184

10.3 Limitations ..................................................................................................... 186
10.4 General Conclusions...................................................................................... 186
10.5 Future Research ............................................................................................ 187

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11.0

APPENDICES ........................................................................................................ 190

Appendix 1: EMG and VGRF Reliability Data .................................................... 190

12.0

REFERENCES ....................................................................................................... 192

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LIST OF FIGURES
Figure 2.1: Tendon hierarchal structure, adapted and modified from (Ker, 2007; Wang,
2006). ............................................................................................................... 34
Figure 2.2: Matrix to fibril stress transfer and distribution, adapted from Ker (1999). .. 37
Figure 2.3: Typical tendon stress strain curve, adapted from Wang, (2006). ................. 39
Figure 4.1: Sonographic images of the Achilles tendons of control (left) and
symptomatic (right) limbs, with the measurement site (40 mm) identified by
the magenta line, the grey scale profile plotted in yellow and the anterior and
posterior tendon borders identified by the green lines. ................................... 86
Figure 4.2: Bland and Altman plots illustrating the bias and 95% limits of agreement for
the sonographic measurements of sagittal Achilles tendon thickness (mm) at
the 20 (left) and 40 (right) mm sites for control),( asymptomatic (

) and

symptomatic ( ) limbs..................................................................................... 89
Figure 4.3: Bland and Altman plots illustrating the bias and 95% limits of agreement for
the mean tendon grey-scale (U) at the 20 (left) and 40 (right) mm sites for
control ( ), asymptomatic ( ) and symptomatic ( ) limbs. ............................ 91

Figure 5.1: Force plate block configuration. ................................................................... 98
Figure 5.2: Modified Helen Hayes marker system. ........................................................ 99
Figure 5.3: An example of the VGRF frequency power spectra for two exercise
repetitions in one participant. ........................................................................ 100
Figure 6.1: Sagittal diameter (d) of the Achilles tendon measured at a standard reference
point 2 cm from the superior aspect of the calcaneus (c). ............................. 108
Figure 6.2: Relationship between Achilles tendon diametral strain and total activity, for
each individual, normalised to a percentage of the maximum possible activity
within each 0–12 (∆) and 12–24 ( ) hour period......................................... 111
Figure 6.3: Relationship between Achilles tendon diametral strain and total weighted
activity, for each individual, normalised to a percentage of the maximum
possible activity within each 0–12 ( ) and 12–24 ( ) hour period. .............. 111

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Figure 7.1: Mean Achilles tendon sagittal thickness normalised for pre-exercise values
following eccentric ( ) and concentric (

) calf muscle exercise. Error bars

represent 95% confidence intervals. Exponential fit representative of the
eccentric recovery time course (-). For clarity, data points have been shifted
either side of the specified time points, at which they were observed. ......... 122
Figure 8.1: Sonographic images of the Achilles tendons of control (left) and
symptomatic (right) limbs, with the measurement site (40 mm) identified by

the magenta line, the grey scale profile plotted in yellow and the anterior and
posterior tendon borders identified by the green lines. ................................. 135
Figure 8.2: Mean load duration (s) for control, asymptomatic and symptomatic limbs
during the performance of eccentric () and concentric (

) exercise. Error

bars represent 95% confidence intervals. *significantly different from control
limb (p < .05) ................................................................................................. 139
Figure 8.3: Mean maximum sagittal ankle joint angles for control, asymptomatic and
symptomatic limbs during the performance of concentric ( ) and eccentric
( ) loading exercises and mean minimum sagittal ankle joint angles for
control, asymptomatic and symptomatic limbs during the performance of
concentric (∆) and eccentric ( ) loading exercises. Error bars represent 95%
confidence intervals. *significantly different from control limb (p < .05) .... 141
Figure 8.4: Mean Achilles tendon diametral strain (%) at the 20 mm site, following
concentric (triangle) and eccentric (square) exercise for control (no shading),
asymptomatic (solid grey) and symptomatic (solid black) limbs. Error bars
represent 95% confidence intervals. .............................................................. 144
Figure 8.5: Mean Achilles tendon diametral strain (%) at the 40 mm site, prior to and
following concentric (triangle) and eccentric (square) exercise for control (no
shading), asymptomatic (solid grey) and symptomatic (solid black) limbs.
Error bars represent 95% confidence intervals. ............................................. 144
Figure 9.1: Force plate block configuration. ................................................................. 158

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Achilles Tendon Adaptation to Exercise

Figure 9.2: Mean SD of the VGRF for control ( ), asymptomatic (

) and symptomatic

( ) limbs during the performance of eccentric and concentric exercise.
*significantly different from the eccentric condition (p < .05). .................... 163
Figure 9.3: Mean power within the 9 (top) and 10 (bottom) Hz window for eccentric ( )
and concentric ( ) muscle actions across the six exercise sets. Error bars
represent 95% confidence intervals. *significantly different from eccentric
exercise set one, two and three (p < .05) ....................................................... 165
Figure 9.4: Mean power within the 9 (top), 10 (middle) and 11 (bottom) Hz window for
control ( ), asymptomatic (

) and symptomatic ) ( limbs during the

performance of eccentric and concentric muscle actions. Error bars represent
95% confidence intervals. *significantly different from eccentric exercise (p <
.05) ................................................................................................................. 167
Figure 9.5: Mean EMG amplitude (V) of LG (top), MG (middle) and SOL (bottom)
during concentric ( ) and eccentric () exercise across exercise sets 1 -6.
Error bars represent 95% confidence intervals. *significantly different from
concentric exercise set one, two and three (p < .05)...................................... 169

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LIST OF TABLES
Table 2.1: Intervention study characteristics including mean ± SD (range) for participant
age and symptom duration............................................................................... 61
Table 2.2: Mean ± SD pain scores from the eight contrasts. .......................................... 63
Table 4.1: Bias and 95% limits of agreement for sagittal thickness measurement of the
Achilles tendon expressed as diametral strain (%). ......................................... 90
Table 5.1: 95% limits of agreement for the EMG amplitude of the MG, LG and SOL
muscles, the power (N2/Hz) within each frequency window and the standard
deviation (N) of the VGRF. ........................................................................... 102
Table 7.1: Mean (standard deviation) sagittal thickness (mm) of Achilles tendons
allocated to eccentric or concentric exercise protocols. ................................ 121
Table 8.1: Mean (SE) baseline (PRE) Achilles tendon thickness (mm) and echogenicity
(0-200 U) of control, asymptomatic and symptomatic limbs at the 20 and 40
mm measurement sites................................................................................... 138
Table 8.2: Mean (SE) maximum and minimum sagittal knee joint angles (degrees)
across exercise sets. ....................................................................................... 140
Table 8.3: Mean (SE) tendon echogenicity (0-200 U) across all time points and muscle
actions for control, asymptomatic and symptomatic limbs at the 20mm and
40mm measurement sites............................................................................... 145
Table 9.1: Mean (SE) maximum and minimum sagittal knee joint angles (degrees) across
exercise sets.................................................................................................... 162
Table 9.2: Mean (SE) power spectral density (N2/Hz) of eccentric and concentric muscle
actions for the frequency windows 2-6 Hz. .................................................... 164
Table 11.1: Bias and 95% limits of agreement for EMG amplitude (V). ..................... 190
Table 11.2: Bias and 95% limits of agreement for the power (N2/Hz) within each
frequency window and for the standard deviation (SD) of the VGRF. ......... 191

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LIST OF ABBREVIATIONS
1-RM

One repetition Maximum

3-4SET

Sonographic imaging conducted between the third and fourth exercise
sets

8hPOST

Sonographic imaging conducted 8 hours after exercise completion

24hPOST

Sonographic imaging conducted 24 hours after exercise completion

A_max

Maximum sagittal ankle joint angle (maximum dorsiflexion)

A_min

Minimum sagittal ankle joint angle (maximum plantarflexion)

ADC

Apparent Diffusion Coefficient

AIC

Akaike’s Information Criterion

ASIS

Anterior Superior Iliac Spine

CV

Coefficient of Variation

ECM

Extracellular matrix

EMG

Electromyography

FOAS

Foot and Ankle Outcome Score

GAG

Glycosaminoglycan

HP

Hydroxylysylpyridinolone (enzymatic collagen cross link)

IMMPOST

Sonographic imaging conducted immediately upon the completion of
exercise

K_max

Maximum sagittal knee joint angle

K_min

Minimum sagittal knee joint angle

LG

Lateral Gastrocnemius

LP

Lysylpyridinoline (enzymatic collagen cross link)

MG

Medial Gastrocnemius

MMP

Matrix Metalloproteinase

MRI

Magnetic resonance Imaging

MVC

Maximum Voluntary Contraction

NRS

Numerical Rating Scale

NSAIDs

Non-steroidal Anti-inflammatory Drugs

PEG 2

Prostaglandin E 2

PRE

Sonographic imaging conducted prior to exercise

PSD

Power Spectral Density

S\V

Surface Area to Volume Ratio

SD

Standard Deviation

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SE

Standard Error

SOL

Soleus

TIME

Duration of exercise repetition loading

VAS

Visual Analogue Scale

VEGF

Vascular Endothelial Growth Factor

VGRF

Vertical Ground Reaction Force

VISA-A

Victorian Institute of Sport Assessment Achilles

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LIST OF PUBLICATIONS
Published Papers
Grigg, N. L., Wearing, S. C., & Smeathers, J. E. (2009). Eccentric calf muscle exercise
produces a greater acute reduction in Achilles tendon thickness than concentric
exercise. British Journal of Sports Medicine, 43(4), 280-283.

Grigg, N. L., Stevenson, N. J., Wearing, S. C., & Smeathers, J. E. (2010). Incidental
walking activity is sufficient to induce time-dependent conditioning of the
Achilles tendon. Gait & Posture, 31(1), 64-67.
Grigg, N. L., Smeathers, J. E., & Wearing, S. C. (2010). Concurrent Validity of the Polar
s3 Stride Sensor for Measurement of Walking Stride Velocity. Research
Quarterly for Exercise and Sport, In Press.
Conference Proceedings and Presentations
Grigg, N., Smeathers, J., & Grimshaw, P. (2007). Unanticipated cutting in female netball
players: Valgus knee angle and the potential for non-contact ligament injury.
Australian Conference of Science and Medicine in Sport. Adelaide, Australia.
Grigg, N. L., Smeathers, J. E., Wearing, S. C., & Urry, S. R. (2008). Tendon
rehabilitation: isolated eccentric loading invokes a greater reduction in Achilles
tendon thickness than concentric exercise. Australian Conference of Science
and Medicine in Sport. Hamilton Island, Australia.
Stevenson, N., Smeathers, J., Grigg, N., & Wearing, S. (2008). Modeling activity
dependent diametral strain in Achilles tendon. Australian Conference of Science
and Medicine in Sport. Hamilton Island, Australia.
Grigg, N. L., Stevenson, N. J., Smeathers, J. E., & Wearing, S. C. (2009). Incidental
activity induces time-dependent conditioning of the Achilles tendon. XXII
Congress of the International Society of Biomechanics. Cape Town, South
Africa.

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STATEMENT OF 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:

____________________

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ACKNOWLEDGEMENTS
First and foremost to my supervisors Dr James Smeathers and Associate Professor Scott
Wearing, thank you, just doesn’t seem quite enough. Thank you for sharing your
knowledge in such an elegant and patient manner. I couldn’t have asked for better
supervisors. The time and effort you have put into my work and the way in which you
have fostered my learning, to facilitate my development as a scientist, is appreciated
ever so much. I have been privileged to work with two people who possess such
intelligence and good nature. To James, Cara calls you my intellectual friend, the
impromptu and informal conversations we had on regular occasions, particularly in
2010, were informative and helpful. I’m grateful for the time you have made for me. To

Scott, you have not only been an amazing academic mentor but a good friend. As a
trusted friend you really did help me through the toughest time of my short life to date
and for that I will always be grateful.

To all the people who provided technical support to the project: Diana Battistutta and
Dimitrios Vagenas for their assistance with all matters statistical; Tim Gurnett for his
assistance with the evolution of the MATLAB code used for image analysis and John
O’Toole for helping with the MATLAB code used to quantify the power spectral density
of the vertical ground reaction force. At this point I must mention the one and only Dr
Nathan Stevenson. Nathan developed the original MATLAB code for image analysis.
More recently, Nathan developed the code which facilitated segmentation of EMG, force
and kinematic data into individual exercise repetitions and provided the code for the
EMG analysis. It was an absolute honour and privilege to work with Nathan, not only
because of his wonderful MATLAB skills but his infectious personally. I have such fond
memories of the times during which we worked together.

To Michael Cole, Cara Graepel, Jamie Sheard, Feng Qui, Amanda Rojek, Melissa
Tucker, Manas Sivaramakrishnan and Tara Fernandez, you guys have been like a safety
harness, you have kept me safe and allowed me to enjoy the experience, as I rode the
rollercoaster which was PhD. Thank you. It has been a lot of fun.

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Finally I would like to thank all the kind people who participated in the research. Their
generous donation of time allowed this research to be completed, my personal goals to

be achieved and information added to the body of knowledge.

Nicole L Grigg

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1.0 INTRODUCTION
The Achilles tendon is the largest and strongest tendon in the human body, acting to
transmit force produced by the Triceps Surae muscle group to the calcaneus, a
transmission necessary for locomotory movement (O'Brien, 2005). Consequently the
Achilles tendon is exposed to high tensile loads with extreme frequency. The peak
tensile force within the Achilles tendon during the stance phase of the walking gait cycle
is approximately two times bodyweight (1430 N) (Finni, Komi & Lukkariniemi, 1998)
and Achilles tendon forces during running and jumping can be up to eight times
bodyweight (3100-5330 N) (Magnusson & Kjaer, 2003). Although forces encountered
by the Achilles tendon are high, with respect to the strength of the tendon, the loads
encountered usually equate to less than one third of the ultimate tensile stress (100 MPa)
and induce strains of less than 4% (Wang, Iosifidis & Fu, 2006). While the original
tendon length will be restored after exposure to strains of up to 4%, it is likely that even
at low strain levels, the fibrils and collagen cross-links will sustain routine damage. The
tendon must, therefore, continually undergo a process of remodelling to maintain
structural homeostasis and mechanical integrity (Ker, 2007; Wang et al., 2006).

With continuous remodelling comes the potential for the process to fail and the tendon
to become degenerative. Achilles tendon degeneration resulting in symptoms such as
pain and a sensation of stiffness particularly at the onset of loading and clinical signs
including local tenderness, swelling, reduced ankle dorsiflexion and increased tendon

thickness and hypoechogenicity evident on ultrasound imaging, is commonly termed
tendinopathy (Abate et al., 2009; Alfredson & Cook, 2007; Fredberg & StengaardPedersen, 2008; Kingma, de Knikker, Wittink & Takken, 2007; Kjaer, 2004; Wang et
al., 2006). Whilst the pathogenesis of tendinopathy is poorly understood, the condition is
believed to arise from exposure to repetitive high magnitude loading without sufficient
time for remodelling between loading sessions, and the interaction between loading and
certain physiological and or environmental factors (Abate et al., 2009; Fredberg &
Stengaard-Pedersen, 2008; Wang et al., 2006).

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The lack of understanding as to the pathogenesis of tendinopathy has led to the
development of an array of conservative treatment options (Alfredson & Cook, 2007;
Rees, Wilson & Wolman, 2006; Wang et al., 2006). Eccentric exercise is one such
treatment and is reported to be the treatment of choice for Achilles tendinopathy (Rees,
Maffulli & Cook, 2009). In contrast to many other treatment options eccentric exercise
has been the subject of many scientific investigations. Such investigations have almost
exclusively focused on the improvement of symptoms or changes in some physiological
characteristics following the completion of a 12 week eccentric exercise program.
Overall, the available evidence suggests that eccentric exercise is beneficial in the
treatment of tendinopathy, due to methodological limitations however, the level of
evidence for the suggested efficacy remains relatively low (Kingma et al., 2007;
Wasielewski & Kotsko, 2007; Woodley, Newsham-West & Baxter, 2007). Importantly,
the mechanisms through which eccentric exercise may produce a reduction in
tendinopathy symptoms have received little attention within the literature and still
remain to be determined. Understanding how eccentric exercise reduces the symptoms

of Achilles tendinopathy is of critical importance, as this understanding may enhance the
effectiveness and efficiency of existing eccentric exercise protocols and lead to the
development of new treatments.

While the medium to long term effects of eccentric training on Achilles tendinopathy
symptoms has been investigated extensively, the short term response of the tendon to
eccentric exercise has received little attention within the literature. Direct measurement
of how the tendon responds to eccentric exercise and contrasting this response with that
of a control condition may provide a more objective measure of the tendons response to
eccentric exercise than a patients’ perception of symptoms. Moreover, some insight into
the underlying mechanisms for eccentric exercise efficacy may be gained by directly
measuring the response of the tendon to eccentric exercise and a control condition. An
equivalent concentric exercise protocol provides the ideal contrast, as there is a small
amount of evidence to suggest that concentric exercise is less effective in reducing
tendinopathy symptoms than eccentric exercise (Mafi, Lorentzon & Alfredson, 2001;
Niesen-Vertommen, Taunton, Clement & Mosher, 1992), and the two exercises would

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be expected to expose the tendon to similar tensile loads. In addition, characteristics of
the exercises including muscle activation and motor output force variability maybe
monitored, in order to identify characteristics unique to eccentric exercise.

The aim of this thesis was, therefore, to examine the acute morphological response of
normal and tendinopathic human Achilles tendons to both isolated eccentric and

concentric Triceps Surae exercise, using sonographic imaging. Furthermore, the
biomechanical characteristics of these exercises were examined via surface
electromyography (EMG) and monitoring fluctuations in the motor output force.

The body of the thesis is divided into two sections; (1) the methodological section in
which the errors associate with sonographic imaging, EMG, motor output force and
incidental walking activity were quantified; (2) the experimental section in which the
morphological response to, and characteristics of, eccentric and concentric exercise were
quantified in participants with and without Achilles tendinopathy.

The methodological section spans three chapters. Chapter 4 investigates the intraobserver reliability for the measurement of anterior-posterior Achilles tendon thickness
from sagittal sonographic images, incorporating errors associated with image capture
and digitisation. Chapter 4 also investigates the reliability of image echogenicity
quantification which is mostly dependent on the capture of the image. Chapter 5
explores the error associated with quantification of EMG and force parameters over
multiple exercise repetitions. The two reliability chapters provide estimates of the level
of error associated with each of the measurement variables. Thus, any differences
observed across experimental conditions can be compared to the level of error, allowing
the meaning of the difference to be identified independently from the statistical findings.
The third chapter in the methodological section (Chapter 6) examines the effect of a
potential confounding factor, that of incidental walking activity, on the Achilles tendon
diametral strain. It was necessary to understand whether the loading associated with
incidental walking was sufficient to modify the Achilles tendon diameter. If this was the

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case, incidental walking would be a source of error in future studies, and would need to
be controlled or accounted for.

The experimental section of the thesis also consists of three chapters. Chapter 7 reports
the findings of a pilot experiment conducted to determine whether the morphological
response of the Achilles tendon was dependent on exercise mode i.e. isolated eccentric
or isolated concentric exercise. The pilot experiments revealed that eccentric and
concentric exercises did elicit different morphological responses and thus informed the
design of subsequent experiments within the experimental section. Chapter 8 examines
the morphological response to eccentric and concentric exercise in participants with and
without Achilles tendinopathy to determine whether pathological tendons responded in a
similar manner to healthy tendons. Chapter 9 considers the electromyographic and motor
output force characteristics of the eccentric and concentric exercises in order to evaluate
the potential mechanistic differences between the two exercises and whether these
characteristics of exercise performance were dependent on the presence of tendinopathy.

Findings from the individual studies are collectively discussed, in light of the research
limitations and with reference to directions for future research, within Chapter 10.

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