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 Nicole L Grigg Page | ii Achilles Tendon Adaptation to Exercise 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 Nicole L Grigg Page | iii 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 Nicole L Grigg Page | iv Achilles Tendon Adaptation to Exercise 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 Nicole L Grigg Page | v Achilles Tendon Adaptation to Exercise TABLE OF CONTENTS KEY WORDS II ABSTRACT III TABLE OF CONTENTS 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 Nicole L Grigg Page | Achilles Tendon Adaptation to Exercise 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 Nicole L Grigg Procedure 96 Page | Achilles Tendon Adaptation to Exercise 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 Nicole L Grigg Page | Achilles Tendon Adaptation to Exercise 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 Nicole L Grigg Page | Achilles Tendon Adaptation to Exercise 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 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