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HAMSTRING STRAIN INJURY
The role of strength & voluntary activation
Matthew N. Bourne
B. App Sci. HMS. (Hons)
2016
Doctor of Philosophy
(Thesis by publication)
School of Exercise and Nutrition Sciences
Faculty of Health
Queensland University of Technology
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Table of Contents
Table of Contents ..................................................................................................................... ii
Abstract ................................................................................................................................... iv
List of Figures ........................................................................................................................... x
List of Tables ......................................................................................................................... xii
List of Abbreviations ............................................................................................................ xiii
Statement of Original Authorship ......................................................................................... xiv
Chapter 1: INTRODUCTION ............................................................................. 1
Chapter 2: LITERATURE REVIEW ................................................................. 3
2.1 Definition of hamstring strain injury .............................................................................. 3
2.2 Incidence of hamstring strain injury in sport .................................................................. 3
2.3 Recurrence of hamstring strain injury in sport ............................................................... 4
2.4 Hamstring anatomy ......................................................................................................... 5
2.5 Mechanism(s) of injury................................................................................................. 11 2.5.1 Hamstring function during high-speed running and propensity for injury ......... 12
2.6 Proposed risk factors for hamstring strain injury .......................................................... 13 2.6.1 Unalterable risk factors ...................................................................................... 14 2.6.2 Alterable risk factors .......................................................................................... 16
2.7 Factors underpinning high rates of hamstring strain injury recurrence ........................ 28
2.8 Mechanism(s) for chronic strength deficits following hamstrings strain injury ........... 30
2.9 Neuromuscular Inhibition ............................................................................................. 31 2.9.1 Evidence for incomplete activation in maximal voluntary contractions ............ 33 2.9.2 Mechanism(s) underpinning neural inhibition ................................................... 37 2.9.3 The impact of resistance training on skeletal muscle activation ........................ 38 2.9.4 The impact of pain and injury on skeletal muscle activation ............................. 40 2.9.5 Evidence for neuromuscular inhibition following hamstring strain injury ........ 41 2.9.6 Impact of neuromuscular inhibition on hamstring muscle morphology and
architecture ......................................................................................................... 43 2.9.7 Neuromuscular inhibition as a mechanism for high rates of hamstring strain injury
recurrence ........................................................................................................... 45
Chapter 3: PROGRAM OF RESEARCH ........................................................ 48
Chapter 4: STUDY 1 – ECCENTRIC STRENGTH AND HAMSTRING INJURY RISK IN RUGBY UNION: A PROSPECTIVE COHORT STUDY.................... 53
4.1 ABSTRACT ................................................................................................................. 55
4.2 INTRODUCTION ........................................................................................................ 57
4.3 METHODS ................................................................................................................... 59
4.4 RESULTS ..................................................................................................................... 64
4.5 DISCUSSION ............................................................................................................... 75
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Chapter 5: STUDY 2 – REDUCED ACTIVATION OF PREVIOUSLY INJURED BICEPS FEMORIS LONG HEAD MUSCLES IN RUNNING ........................... 81
5.1 Linking Paragraph ........................................................................................................ 83
5.2 ABSTRACT ................................................................................................................. 84
5.3 INTRODUCTION ........................................................................................................ 85
5.4 METHODS ................................................................................................................... 87
5.5 RESULTS ..................................................................................................................... 94
5.6 DISCUSSION ............................................................................................................. 100
Chapter 6: STUDY 3 – IMPACT OF EXERCISE SELECTION ON HAMSTRING MUSCLE ACTIVATION ...................................................................................... 105
6.1 Linking Paragraph ...................................................................................................... 107
6.2 ABSTRACT ............................................................................................................... 109
6.3 INTRODUCTION ...................................................................................................... 110
6.4 METHODS ................................................................................................................. 112
6.5 RESULTS ................................................................................................................... 121
6.6 DISCUSSION ............................................................................................................. 129
Chapter 7: STUDY 4 – ADAPTABILITY OF HAMSTRING ARCHITECTURE AND MORPHOLOGY TO TARGETED RESISTANCE TRAINING ............ 137
7.1 Linking Paragraph ...................................................................................................... 139
7.2 ABSTRACT ............................................................................................................... 140
7.3 INTRODUCTION ...................................................................................................... 141
7.4 METHODS ................................................................................................................. 143
7.5 RESULTS ................................................................................................................... 153
7.6 DISCUSSION ............................................................................................................. 163
Chapter 8: GENERAL DISCUSSION, LIMITATIONS & CONCLUSION169
Bibliography ............................................................................................................ 173
Appendices ............................................................................................................... 195
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Abstract
Hamstring strain injuries (HSIs) are endemic in sports involving high-speed running. These
injuries typically occur when athletes run at maximal or near maximal speeds and upwards of
80% affect the biceps femoris long head (BFLH). High rates of injury recurrence (16-54%) are
also concerning, particularly given the tendency for re-injuries to be more severe than the
initial insult. These observations suggest that more is to be learnt about the mechanisms
underpinning first-time and recurrent HSIs, while also suggesting that prophylactic programs
should specifically target the BFLH. This thesis aimed to, firstly, explore the role of eccentric
strength and between-limb imbalance in HSI occurrence, and determine if previously injured
hamstrings display altered neuromuscular function during high-speed running. The second
aim of this thesis was to characterise the activation patterns and the malleability of hamstring
muscle architecture and morphology to different strengthening exercises, in an attempt to
improve HSI prevention programs by better targeting the site of injury.
The aim of study 1 was to determine if lower levels of eccentric knee-flexor strength or
greater between-limb imbalances in eccentric strength are risk-factors for HSI. This study
found that athletes with between-limb imbalance in eccentric knee-flexor strength of ≥ 15%
and ≥ 20% increased the risk of HSI 2.4 fold (RR = 2.4, 95% CI = 1.1 to 5.5, p = 0.033) and
3.4 fold (RR = 3.4, 95% CI = 1.5 to 7.6, p = 0.003), respectively. Furthermore, the risk of re-
injury was augmented in players with strength imbalances (p < 0.001).
Study 2 aimed to determine: 1) the spatial patterns of hamstring muscle activation during
high-speed overground running in limbs with and without a prior HSI and; 2) whether
previously injured hamstring muscles exhibit lasting deficits in cross-sectional area (CSA).
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Ten elite male athletes with a history of unilateral BFLH strain injury underwent functional
magnetic resonance imaging before and immediately after a repeat-sprint running protocol.
This study demonstrated that previously injured BFLH muscles displayed a significantly lower
percentage increase in transverse relaxation time after the running protocol, compared to
uninjured contralateral BFLH muscles (mean difference = 12.0%, p < 0.001). However, no
between-limb differences in CSA were observed for any hamstring muscles.
The purpose of Study 3 was to determine the extent to which different strength training
exercises selectively activate the commonly injured BFLH muscle. Part 1 employed surface
electromyography (EMG) to measure hamstring activation during 10 common exercises and
found that, in eccentric contractions, the largest BF/MH normalised EMG (nEMG) ratio was
observed in the 45° hip extension exercise (HE) and the lowest was observed in the Nordic
hamstring (NHE) and bent-knee bridge exercises. Part 2 used fMRI to explore the spatial
patterns of hamstring activation in the 45° HE and NHE and revealed that the BFLH was
significantly more active in the 45° HE than the NHE (p < 0.001).
Based on the results from Study 3, Study 4 aimed to evaluate changes in hamstring muscle
volume, anatomical cross-sectional area (ACSA) and BFLH fascicle length following 10-
weeks of NHE or HE training, or a period of no training (CON). This study found that BFLH
fascicles were significantly longer in the NHE and HE groups after 5 (p < 0.001) and 10
weeks of training (p < 0.001) but remained unchanged for the CON group (p > 0.05). The HE
group displayed a greater percentage increase in BFLH volume than the NHE (p < 0.037) and
CON (p < 0.001) groups. Similarly, BFLH ACSA increased more in the HE group than the
NHE (p = 0.047) and CON groups (p < 0.001). Both exercises induced similar (p > 0.05)
increases in semitendinosus volume and ACSA which were greater than those observed for
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the CON group (all p ≤ 0.002). However, only the NHE group exhibited increased BF short
head ACSA, and only the HE group displayed increased semimembranosus volume (p =
0.007) and ACSA (p = 0.015), compared to the CON group.
This program of research has contributed new knowledge relating to factors which may
predispose to, and manifest as a result of HSI, while also providing novel data which may be
used to inform injury preventive and rehabilitation practices. This thesis has provided
evidence 1) that between-limb imbalance in eccentric knee flexor strength is a risk factor for
HSI; 2) that previously injured hamstrings display a reduced activation capacity following a
return to sport; 3) that different strengthening exercises elicit unique patterns of hamstring
muscle activation; and 4) that training with different exercises results in heterogeneous
architectural and morphological adaptations in the hamstrings. These data highlight the
potential importance of ameliorating eccentric strength imbalances and restoring voluntary
activation, particularly following HSI, while also providing an evidence base from which to
form decisions regarding exercise selection in prophylactic programs.
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List of publications related to thesis
1. Bourne, MN., Opar, DA., Williams, MD., & Shield, AJ. (2015). Eccentric Knee-
flexor Strength and Hamstring Injury Risk in Rugby Union: A prospective study. Am
J Sports Med, 43(11):2663-70. doi: 10.1177/0363546515599633.
2. Bourne, MN., Williams, MD., Opar, DA., Al Najjar, A., & Shield, AJ. (2016).
Impact of exercise selection on hamstring muscle activation. Br J Sports Med,
Accepted.
Manuscripts currently under peer review
1. Bourne, MN., Duhig, SJ., Timmins, RG., Williams, MD., Opar, DA., Al Najjar, A.,
Kerr, G., & Shield, AJ. (2016). Impact of the Nordic hamstring and hip extension
exercises on hamstring architecture and morphology: implications for injury
prevention. Br J Sports Med, Under Review.
Other relevant publications
1. Bourne, MN., Opar,DA., Williams,MD., Al Najjar, A, & Shield, AJ (2015). Muscle
activation patterns in the Nordic hamstring exercise: Impact of prior strain injury.
Scand J Med Sci Sports doi: 10.1111/sms.12494.
2. Timmins, R., Bourne, MN., Shield, A., Williams, M., Lorenzon, C., & Opar, D.
(2015). Short biceps femoris fascicles and eccentric knee flexor weakness increase the
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risk of hamstring injury in elite football (soccer): a prospective cohort study. Br J
Sports Med, [Epub ahead of print].
3. Timmins, RG., Bourne, MN., Shield, AJ., Williams, MD., Lorenzen, C., & Opar, DA
(2015). Biceps femoris architecture and strength in athletes with a prior ACL
reconstruction. Med Sci Sports Exerc, [Epub ahead of print].
Grants awarded during candidature
1) Institute of Health and Biomedical Innovation
Bourne MN, Shield AJ. (2015) The effect of gender on hamstring muscle activity
during selected rehabilitation exercises.
$8000
2) Queensland Academy of Sport Centre of Excellence
Bourne MN, Shield AJ. (2014) Impact of exercise selection of biceps femoris
activation and hypertrophy.
$36 800
List of conference presentations
1) Bourne, MN, Opar, DA, Williams, MD, Shield, AJ. Eccentric Strength and
Hamstring Injury Risk in Rugby Union: A Prospective corhort study. World Congress
on Science and Football. Copenhagen, 2015.
2) Bourne, MN, Opar DA, Williams MD, Al Najjar A, Shield AJ. Reduced activation
of biceps femoris long head muscles in running following strain injury. Sports
Medicine Australia. Canberra, 2014.
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3) Bourne, MN, Opar DA, Williams MD, Al Najjar A, Shield AJ. Impact of previous
strain injury on hamstring muscle activation during high-speed overground running.
International Olympic Committee World Congress for the Prevention of Injury and
Illness in Sport. Monaco, 2014
4) Bourne, MN, Opar DA, Williams MD, Al Najjar A, Shield AJ. Previously injured
biceps femoris long head muscles display reduced activation during high-speed
overground running: an fMRI investigation. IHBI Inspires, Gold Coast, 2014.
5) Bourne, MN, Opar DA, Williams MD, Al Najjar A, Shield AJ. Hamstring muscle
activation during the Nordic hamstring exercise and the impact of previous strain
injury: an fMRI study. XXII International Conference on Sports Rehabilitation and
Traumatology: Football Medicine Strategies for Muscle and Tendon Injuries. London,
2013.
6) Bourne, MN, Opar DA, Williams MD, Al Najjar A, Shield AJ The impact of
previous strain injury on hamstring muscle activation during the Nordic hamstring
exercise. American College of Sports Medicine Annual Meeting. Indianapolis, 2013.
7) Bourne, MN, Opar DA, Williams MD, Al Najjar A, Shield AJ Spatial activation
patterns of the knee flexors during the Nordic hamstring exercise: an fMRI study.
Sports Medicine Australia. Phuket, 2013.
8) Bourne, MN, Preventing hamstring strain injuries in elite athletes. Queensland
Academy of Sport Injury Management Seminar. Brisbane, 2013.
9) Bourne, MN. The role of neuromuscular inhibition in hamstring strain injury
recurrence. IHBI Inspires. Brisbane, 2013.
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List of Figures
Figure 2-1. Phases of the running gait cycle ............................................................. 12
Figure 2-2. Comparison of knee flexion torque-velocity relationships between previously injured hamstrings, contralateral uninjured hamstrings and reference values from uninjured control subjects ........................................ 29
Figure 2-3. The torque/force-velocity relationships of electrically stimulated (red) and voluntarily activated (blue) skeletal muscle ................................................. 32
Figure 2-4. A simplified scheme of the afferent synaptic inputs to alpha (ά) and gamma (γ) motoneurones .......................................................................................... 38
Figure 2-5. Percentage change in fMRI T2 relaxation times of each hamstring muscle for both the previously injured (inj) and uninjured (uninj) limbs ................ 42
Figure 2-6. MRI image illustrating a previously injured BFLH (right limb) and uninjured contralateral BFLH (left limb) ...................................................... 44
Figure 2-7. Architectural characteristics of the injured BFLH ................................... 45
Figure 2-8. Conceptual model for the development of neuromuscular inhibition following hamstring strain injury ................................................................. 47
Figure 4-1. The Nordic hamstring exercise ............................................................... 61
Figure 4-2. The relationship between eccentric knee flexor strength imbalances and probability of future hamstring strain injury ................................................ 72
Figure 5-1. Mean percentage change in fMRI T2 relaxation times after running for each hamstring muscle in previously injured (Inj) and uninjured (Uninj) limbs ...................................................................................................................... 95
Figure 5-2. A. Parametric map of transverse (T2) relaxation times for the previously injured and uninjured contralateral limbs of a single participant ............... 96
Figure 5-3. Mean CSAs (cm2) of each hamstring muscle for both the previously injured (Inj) and uninjured (Uninj) contralateral limbs ........................................... 97
Figure 5-4. Percentage change in fMRI T2 relaxation times of each hamstring muscle in the uninjured limb ..................................................................................... 98
Figure 6-1. The 10 examined exercises .................................................................... 116
Figure 6-2. Biceps femoris (BF) to medial hamstring (MH) normalised EMG (nEMG) relationship for the (a) concentric and (b) eccentric phases of each exercise .................................................................................................................... 124
Figure 6-3. Percentage change in fMRI T2 relaxation times of each hamstring muscle following the 45° hip extension exercise .................................................... 125
Figure 6-4. Percentage change in fMRI T2 relaxation times of each hamstring muscle following the Nordic hamstring exercise .................................................... 127
Figure 6-5. Ratio of biceps femoris long head (BFLH) to semitendinosus (ST) (BFLH/ST) percentage change in fMRI T2 relaxation times following the 45° hip extension and the Nordic hamstring exercise ............................................................. 128
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Figure 7-1. (a) The 450 hip extension (HE) exercise and (b) the Nordic hamstring exercise (NHE) ............................................................................................ 146
Figure 7-2. T1-weighted image (transverse relaxation time = 750ms; echo time = 12ms, slice thickness = 10mm), depicting the regions of interest for each hamstring muscle. ....................................................................................... 151
Figure 7-3. Biceps femoris long head (BFLH) fascicle lengths before (baseline), during (mid-training) and after (post-training) the intervention period ................ 154
Figure 7-4. Percentage change in volume (cm3) for each hamstring muscle after the intervention. ................................................................................................ 156
Figure 7-5. Percentage change in anatomical cross sectional area (ACSA) (cm2) for each hamstring muscle after the intervention. ............................................ 159
Figure 7-6. Eccentric knee flexor force measured during the Nordic strength test before (baseline) and after (post-training) the intervention period ....................... 161
Figure 7-7. Hip extension three-repetition maximum (3RM) before (baseline) and after (post ............................................................................................................ 162
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List of Tables
Table 2-1. Morphometric and architectural data of the hamstring muscles ............... 9
Table 4-1. Pre-season Nordic hamstring exercise force variables for each level of competition and player position. .................................................................. 66
Table 4-2. Pre-season Nordic hamstring exercise force variables for hamstring strain injured and uninjured rugby union players. ................................................. 68
Table 4-3. Univariate relative risk of suffering a future hamstring strain injury ...... 70
Table 4-4. Multivariate logistic regression model using prior hamstring strain injury (HSI) and between-limb imbalance in eccentric knee flexor strength .......... 73
Table 5-1. Hamstring strain injury details for all participants (n=10) ..................... 89
Table 6-1. Mean normalised EMG (nEMG) amplitudes for the biceps femoris (BF) and medial hamstring (MH) muscles during the concentric and eccentric phases of 10 hamstring strengthening exercises ........................................................ 122
Table 7-1. Training program variables ................................................................... 147
Table 7-2. Participant characteristics ..................................................................... 153
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List of Abbreviations
BFLH biceps femoris long head
BFSH biceps femoris short head
CI confidence interval
CSA cross-sectional area
EMG electromyography
fMRI functional magnetic resonance imaging
HSI hamstring strain injury
kg kilograms of body mass
MRI magnetic resonance imaging
MTU musculotendinous unit
MVIC maximal voluntary isometric contraction
N newtons of force
NHE Nordic hamstring exercise
ROI region of interest
RR risk ratio
SD standard deviation
SE standard error
SM semimembranosus
ST semitendinosus
T2 transverse relaxation time
VA voluntary activation
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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: QUT Verified Signature
Date: July 2016
Chapter 1: INTRODUCTION 1
Chapter 1: INTRODUCTION
Hamstring strain injury (HSI) is characterised by a partial to complete disruption of muscle
fibres in the hamstring muscle group and it represents the most common injury in sports
involving high-speed running (Brooks, Fuller, Kemp, & Reddin, 2005c, 2006; Drezner,
Ulager, & Sennet, 2005; Ekstrand, Hagglund, & Walden, 2011b; Orchard, James, & Portus,
2006; Woods et al., 2004). Comparatively high rates of HSI recurrence (Brooks, et al., 2006;
Heiser, Weber, Sullivan, Clare, & Jacobs, 1984; Orchard & Seward, 2010; Woods, et al.,
2004) are perhaps the most concerning aspect of these injuries, as re-injuries are typically
more severe (Brooks, et al., 2006; Ekstrand, et al., 2011b; Koulouris, Connell, Brukner, &
Schneider-Kolsky, 2007) and demand greater periods of convalescence (Koulouris, et al.,
2007) than first-time insults.
Despite significant efforts in recent years to reduce the burden of HSI in sport, longitudinal
data from the elite Australian football league (Orchard & Seward, 2002; Seward, Orchard,
Hazard, & Collinson, 1993), professional rugby union (Brooks, Fuller, Kemp, & Reddin,
2005a, 2005b; Brooks, et al., 2006), elite level soccer (Hagglund, Walden, & Ekstrand, 2009;
Woods, et al., 2004) and athletics (Opar et al., 2013), suggest that HSI rates have not declined
over several years. This is particularly concerning in light of evidence that other common
injuries such as ankle sprains in soccer (Ekstrand & Gillquist, 1983) and posterior cruciate
ligament injuries in Australian football (Orchard & Seward, 2010), have shown reduced
injury rates following the implementation of preventive measures. These data suggest that the
effectiveness of conventional HSI prevention and rehabilitation practices might be overstated
and that there is more to be learnt about the mechanisms underpinning injury occurrence.
Chapter 1: INTRODUCTION 2
Significant time lost from training and competition, from first time and recurrent HSIs
(Brooks, et al., 2006; Orchard & Seward, 2011; Woods, et al., 2004), is not only challenging
for the athlete, but also imparts a significant financial burden on professional sporting clubs.
For example, HSIs were estimated to cost English premier league clubs £74.4 million in
wages paid to unavailable players during the 1999-2000 seasons (Woods, Hawkins, Hulse, &
Hodson, 2002). In the elite Australian football league, HSI cost clubs AUD$1.5m in ‘lost
wages’ throughout the 2009 competitive season (Opar, Williams, & Shield, 2012) and
between 2002 and 2012, the average yearly cost of HSIs per Australian football club
increased by 71% (Hickey, Shield, Williams, & Opar, 2013). Over the same time period the
average financial cost of a single HSI increased by 56% from AUD$25 603 in 2003 to AUD
$40 021 in 2012, despite little change in the rate of injuries during that period (Hickey, et al.,
2013).
Given the performance and economic based implications of HSI, further exploration of the
mechanisms responsible for this injury is warranted. This review aims to provide the reader
with a summary of HSI literature through an overview of HSI prevalence in sport, a
description of anatomical and morphological factors which predispose this muscle group to
injury, and a discussion of the proposed causes and risk factors for HSI. It will conclude by
proposing a conceptual framework for the role of neuromuscular inhibition in HSI recurrence
and suggest some novel direction for future research.
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Chapter 2: LITERATURE REVIEW
2.1 DEFINITION OF HAMSTRING STRAIN INJURY
HSI is characterised by a partial to complete disruption of muscle fibres in the hamstring
muscle group and is typically associated with the instantaneous onset of posterior thigh pain
(Heiderscheit, Sherry, Silder, Chumanov, & Thelen, 2010). HSI or rupture occurs most often
at the proximal aponeurosis of the BFLH (Askling, Tengvar, Saartok, & Thorstensson, 2007;
De Smet & Best, 2000; Garrett, 1990) but can also affect the proximal bony origin,
musculotendinous junction (MTJ), muscle belly or the point of distal bony insertion of any of
the hamstring muscles (Agre, 1985). The severity of injury appears to be dependent on the
location, the magnitude of force applied, the physical integrity of the muscle at the time of
injury (Agre, 1985) and the magnitude of strain experienced (Askling, Saartok, &
Thorstensson, 2006). The American Medical Association has identified three grades of
severity (Craig, 1973): grade 1 injuries involve a minor tear of only a few muscle fibres with
minimal loss of function; grade 2 injuries are more severe partial tears of the muscle-tendon
unit (MTU) signified by some loss of function; and grade 3 injuries involve a complete
rupture of the MTU and severe functional deficits.
2.2 INCIDENCE OF HAMSTRING STRAIN INJURY IN SPORT
HSI is common in a range of sports including athletics (Bennell & Crossley, 1996; D'Souza,
1994; Drezner, et al., 2005; Opar, Drezner, et al., 2013), American football (Elliott, Zarins,
Powell, & Kenyon, 2011; Feeley et al., 2008), Australian football (Gabbe, Finch,
Wajswelner, & Bennell, 2002; Orchard & Seward, 2002, 2010; Seward, Orchard, Hazard, &
Collinson, 1993b), rugby union (Brooks, et al., 2005a, 2005b) and soccer (Ekstrand,
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Hagglund, & Walden, 2010, 2011a; Woods, et al., 2002; Woods, et al., 2004). Within
athletics, HSI accounts for 75% of all lower limb strains and represents 24.1% of all injures
in the sport (Opar, Drezner, et al., 2013). In the American National Football League, HSI
represents 11.6% of all injuries and is the most severe injury subtype with, on average, 8.3
days lost per incident (Feeley, et al., 2008). HSI is the most common injury in the elite
Australian football league (Gabbe, et al., 2002; Orchard & Seward, 2002, 2010; Seward, et
al., 1993). On average, six new injuries per club per season over the past 10 years have been
attributed to HSI, representing 16% of all injuries sustained in the sport (Orchard & Seward,
2010). HSI accounted for 28% of all AFL games missed in the 2009 season, which is far
more than quadriceps strains (7.8%) or groin strains (17.9%) (Orchard & Seward, 2010).
Large-scale studies in English professional rugby union (Brooks, et al., 2005a, 2005b) have
reported that hamstring strains account for 6–15% of all injuries suffered during match play
and result in, on average, 17 days of absence from training and/or playing. This contrasts with
12 days lost following quadriceps or hip flexor strain and 10 days lost as a result of hip
adductor strain injury (Brooks, et al., 2005c). HSIs are the single most common injury in
soccer and account for 12% of all injuries in this game (Ekstrand, et al., 2010, 2011a; Woods,
et al., 2002; Woods, et al., 2004). This is more than quadriceps strains (7%), groin injuries
(9%) and ankle sprains (7%) (Ekstrand, et al., 2011a) and equates roughly to a squad of 25
incurring 7 HSIs each season. Further, HSI represents the most common type of severe injury
(those resulting in >28 days of absence from training and playing) (Ekstrand, et al., 2011a).
2.3 RECURRENCE OF HAMSTRING STRAIN INJURY IN SPORT
Arguably the most concerning aspect of HSIs is their tendency to re-occur (Brooks, et al.,
2006; Croisier, 2004; Heiser, et al., 1984; Orchard & Seward, 2002, 2010, 2011; Seward, et
al., 1993; Woods, et al., 2004), often with greater severity than the original insult (Brooks, et
5
al., 2006) (Brooks, et al., 2006; Ekstrand, et al., 2011b). Two decades ago, Seward et al.
(Seward, et al., 1993) reported that 34% of all HSIs in professional Australian football, rugby
union and rugby league players were recurrences of previous injuries. Heiser and colleagues
(Heiser, et al., 1984) noted similar recurrence rates in American football (31.7%) close to 30
years ago. More recent epidemiological studies suggest that recurrent HSI is still an issue as
27% of all HSIs across a 20-year period in elite Australian football were recurrent injuries
(Orchard & Seward, 2011). In elite rugby union, 21.3% of all HSIs were reported to be
recurrences of previous injuries (Brooks, et al., 2006). Interestingly, HSI recurrence rates in
Australian football have declined moderately in recent years with the reduction attributed to
more cautious treatment and increased convalescence rather than to improved rehabilitation
practices (Orchard & Seward, 2010). However, HSI recurrence rates remain significantly
higher than groin strain recurrences (23.3%) and quadriceps strain recurrences (17%)
(Orchard & Seward, 2011) in elite Australian footballers. High recurrence rates across a
number of sports suggest that conventional rehabilitation practices are not fully addressing
the underlying risk factors leading to HSI or the maladaptations associated with the previous
insult.
2.4 HAMSTRING ANATOMY
The hamstring muscle compartment collectively describes a group of three muscles located
on the posterior thigh—semimembranosus (SM), semitendinosus (ST), and biceps femoris
(BF); BF is further divided into a long head (BFLH) and a short head (BFSH). With the
exception of BFSH, the hamstrings are biarticular muscles because they cross both the
posterior aspects of the knee and hip joints. This organisation allows the biarticular
hamstrings to perform flexion at the knee and extension of the hip during concentric
contraction. Although these muscles share relatively common actions, they exhibit significant
6
differences in morphology, architecture and function (Markee et al., 1955). A thorough
understanding of the anatomical and architectural characteristics of these muscles, as well as
differences in their patterns of innervation, is necessary to comprehend the potential impact
hamstring structure may play in HSI occurrence.
Semitendinosus ST constitutes one-half of the medial hamstrings and morphologically is considered a single
muscle, although it may be termed digastric given the presence of a tendinous inscription
dividing the muscle belly into superior and inferior portions (Markee, et al., 1955).
Proximally, its long fibres originate from three distinct locations: the posteromedial portion
of the ischial tuberosity; the medial border of the proximal BFLH tendon; and an aponeurosis
which arises from the proximal tendon of the BFLH (Woodley & Mercer, 2005). Distally,
fibres converge into a tendon which then inserts onto the proximal medial surface of the tibia
(Marieb & Hoehn, 2007). ST has a dual innervation (a result of its digastric structure) with
each nerve originating from the tibial portion of the sciatic nerve (Markee, et al., 1955). The
uppermost nerve arises from the tibial division almost opposite the ischial tuberosity and
innervates motor units proximal to the tendinous inscription. The second nerve comes from
the tibial division at the level of the upper and middle thirds of the thigh and supplies the
inferior portion of the muscle. Architecturally, ST demonstrates characteristics of a strap-like
muscle with long and thin fibres, which are the longest of all the hamstring muscles (Table 2-
1) (Woodley & Mercer, 2005).
Semimembranosus SM is the second of the medial hamstrings and is a single muscle with a bipennate
architectural arrangement (Markee, et al., 1955). Its proximal tendon originates from the
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lateral facet of the posterior ischial tuberosity (Marieb & Hoehn, 2007). Distally, the tendon
has multiple attachment sites; one portion inserts on the posterior medial surface of the
medial tibial condyle and a second segment expands to the medial condyle of the femur, the
capsule of the knee joint and proximally onto the medial collateral ligament (Markee, et al.,
1955). SM is innervated by a single nerve branch arising from the tibial portion of the sciatic
nerve; it shares the same nerve as that which supplies the distal section of ST. This nerve
travels inferiorly, dispersing into five branches in succession, the first of which lies near the
proximal origin and last of which lies near the distal aponeurosis (Markee, et al., 1955).
Architecturally, SM displays the greatest physiological cross-sectional area (PCSA) of all
hamstring muscles (Table 2-1) (Woodley & Mercer, 2005).
Biceps femoris BF is a two-segment muscle with both a short (BFSH) and a long head (BFLH). BFSH is the
only single joint muscle of the hamstring group, acting only to flex the knee during
concentric contraction. Its fibres originate from three locations: the lateral lip of the linear
aspera; the upper two-thirds of the lateral supracondylar line; and the lateral intermuscular
septum (Marieb & Hoehn, 2007). Distally, its parallel fibres converge on a common tendon
with that of BFLH, which inserts onto the head of fibula and lateral condyle of the femur
(Marieb & Hoehn, 2007). BFSH is innervated by nerve branches originating from the sciatic
nerve or common peroneal nerves, depending on anatomical variations (Markee, et al., 1955;
Woodley & Mercer, 2005). Structurally, BFSH has the smallest PCSA relative to all other
hamstring muscles (Table 2-1) (Woodley & Mercer, 2005), although it comprises the longest
mean fascicle lengths.
8
BFLH, a bipennate and biarticular muscle (Marieb & Hoehn, 2007), originates partly from a
common tendon with ST, which originates from the medial portion of the superior half of the
ischial tuberosity (Woodley & Mercer, 2005). BFLH also attaches directly to the
sacrotuberous ligament. The long proximal tendon passes distally until it forms a narrow
aponeurotic musculotendinous junction; BFLH fibres emerge on the lateral border of this
tendon along with some ST fascicles (Woodley & Mercer, 2005). Distally, the large muscle
belly passes inferolaterally to converge onto a common tendon with BFSH, inserting on the
superior extremity of the head of the fibula and the lateral femoral condyle (Markee, et al.,
1955; Woodley & Mercer, 2005). BFLH is innervated by the tibial division of the sciatic
nerve, which divides into an upper and lower portion and supplies the deep and superficial
motor units, respectively (Markee, et al., 1955). Architecturally, BFLH displays the second
greatest PCSA (behind SM) of all the hamstring muscles (Table 2-1) (Woodley & Mercer,
2005).
9
Table 2-1. Morphometric and architectural data of the hamstring muscles (SM, Semimembranosus; ST, Semitendinosus; BFlh, Biceps femoris
long head; BFsh, Biceps femoris short head). Adapted from Woodley and Mercer (2005).
11
2.5 MECHANISM(S) OF INJURY
HSI occurs most often as a result of trauma to the MTU (Craig, 1973). This may be in the
form of forceful eccentric contraction or from excessive stretch of the MTU (Agre, 1985). A
number of potential mechanisms have been proposed for HSIs however, there is no clear
consensus in the literature. High degrees of muscular strain, defined as the change in length
of the muscle during movement (Garrett, 1990), and high degrees of muscular stress,
quantified as force per unit of cross-sectional area (CSA) (Garrett, 1990) are both present
during forceful eccentric contractions. However, it is unclear which of these is the major
contributor to HSI (Garrett, 1990). Garrett and colleagues (1987) examined the effects of
strain on in situ animal muscles that were stimulated maximally and submaximally and then
stretched to the point of MTU strain-induced failure. The resultant load–deformation curves
demonstrated that, regardless of the stimulation level, all muscles failed at the same MTU
length (Garrett, Safran, Seaber, Glisson, & Ribbeck, 1987). These data imply that strain, not
stress, is the primary determinant of strain injury occurrence. However, various authors have
noted that HSI is most likely to occur during the terminal swing phase of running (Brooks, et
al., 2005c; Ekstrand, et al., 2011a; Woods, et al., 2002; Yu et al., 2008) where stress is high
(Schache, Dorn, Blanch, Brown, & Pandy, 2012) but strain is moderate (Thelen, Chumanov,
Best, Swanson, & Heiderscheit, 2005). Clearly, there is some degree of both stress and strain
whenever muscles are active and it is likely that with lower levels of stress, a higher level of
strain is needed to cause rupture, while at higher levels of stress comparatively lower levels
of strain will bring about injury (Opar, et al., 2012).
12
2.5.1 Hamstring function during high-speed running and propensity for injury
The running gait cycle for each leg can be divided into two major phases: a stance phase
comprising the initial contact, mid-stance and take-off; and a swing phase comprising initial,
mid and terminal-swing of each leg (Figure 2-1) (Subotnick, 1985). During the mid and
terminal-swing phases, the hamstrings primarily contract eccentrically to decelerate hip
flexion and knee extension (Montgomery, Pink, & Perry, 1994). With increasing running
speed, the duration of the terminal swing phase is reduced (Agre, 1985), increasing the
angular velocity at both the hip and knee which requires increased torque generation by the
hamstrings to control the movement at each joint (Agre, 1985). The biomechanical demands
of high-speed running may explain the propensity of HSI to occur during sprint running
compared with slow-speed running (jogging).
Figure 2-1. Phases of the running gait cycle
To date, there have only been two case-studies which captured the time-occurrence and
biomechanical response to an HSI during running. Each of these studies concluded that injury
occurred while the hamstrings were actively lengthening during the terminal-swing phase of
the running cycle (Heiderscheit et al., 2005; Schache, Wrigley, Baker, & Pandy, 2009). This
might be explained by evidence that the biarticular SM, ST and BFLH all produce peak force
13
while lengthening during the late-swing phase of running (Chumanov, Heiderscheit, &
Thelen, 2007, 2011; Schache, et al., 2012; Thelen et al., 2005). Schache and colleagues
(2012) suggest that during this phase, the BFLH exhibits the greatest peak strain, ST exhibits
the fastest lengthening velocity, and SM displays the greatest peak force, produces the most
power and completes the greatest amount of work. Given the reported pre-eminence of
muscle strain in HSI (Opar, et al., 2012), the differences in peak muscle length during
terminal-swing has received significant interest (Chumanov, et al., 2007, 2011; Schache, et
al., 2012; Thelen, Chumanov, Hoerth, et al., 2005); BFLH increases in length by 9.5% relative
to the MTU length in the anatomical position in contrast with 7.4% lengthening by SM and
8.1% by ST (Chumanov, et al., 2007, 2011; Schache, et al., 2012; Thelen, Chumanov,
Hoerth, et al., 2005). That BFLH experiences the greatest strain magnitude may explain its
propensity for injury relative to the other hamstring (Connell et al., 2004; Koulouris, et al.,
2007), however, whether these small differences can account for discrepant injury rates is yet
to be determined.
2.6 PROPOSED RISK FACTORS FOR HAMSTRING STRAIN INJURY
Several unalterable and alterable risk factors for HSI have been proposed in the literature.
Unalterable risk factors include previous HSI (Arnason et al., 2004; Bennell et al., 1998;
Gabbe, Bennell, Finch, Wajswelner, & Orchard, 2006; Hagglund, Walden, & Ekstrand, 2006;
Orchard, 2001; Verrall, Slavotinek, Barnes, Fon, & Spriggins, 2001), increasing age
(Arnason, et al., 2004; Gabbe, Bennell, & Finch, 2006; Verrall, et al., 2001) and ethnicity
(Brooks, et al., 2006; Verrall, et al., 2001; Woods, et al., 2004). Alterable risk factors include
muscular weakness (Aagaard, Simonsen, Magnusson, Larsson, & Dyhre-Poulsen, 1998;
Arnason, Andersen, Holme, Engebretsen, & Bahr, 2008; Askling, Karlsson, & Thorstensson,
2003; Brockett, Morgan, & Proske, 2001; Burkett, 1970; Croisier, Forthomme, Namurois,
14
Vanderthommen, & Crielaard, 2002; Croisier, Ganteaume, Binet, Genty, & Ferret, 2008c;
Friden & Lieber, 1992; Gabbe, Bennell, Finch, et al., 2006; Garrett, et al., 1987; Lee, Reid,
Elliott, & Lloyd, 2009; Mair, Seaber, Glisson, & Garrett, 1996; Orchard, Marsden, Lord, &
Garlick, 1997b; Petersen, Thorborg, Nielsen, Budtz-Jørgensen, & Hölmich, 2011; Sugiura,
Saito, Sakuraba, Sakuma, & Suzuki, 2008; Yamamoto, 1993; Yeung, Suen, & Yeung, 2009),
poor flexibility (Bradley & Portas, 2007; Henderson, Barnes, & Portas, 2009; McHugh et al.,
1999; Witvrouw, Danneels, Asselman, D'Have, & Cambier, 2003), fatigue (Brooks, et al.,
2006; Heiser, et al., 1984; Mair, et al., 1996; Opar, et al., 2012; Woods, et al., 2004), poor
lumbopelvic control (Chumanov, et al., 2007; Sherry & Best, 2004) and short BFLH fascicle
lengths (Timmins, Bourne, et al., 2015). A comprehensive understanding of each of these risk
factors is necessary for identifying individuals most susceptible to HSI and re-injury.
2.6.1 Unalterable risk factors
Previous injury Previous HSI appears to be the best independent predictor of future HSI (Bennell, et al.,
1998a; Gabbe, Bennell, Finch, et al., 2006; Hagglund, et al., 2006; Orchard, 2001; Verrall, et
al., 2001). Prospective studies in elite soccer players have found that players who sustained a
HSI in the previous season were up to 11.6 times more likely to experience a recurrent injury
in the following season (Arnason, et al., 2004; Hagglund, et al., 2006). Similarly, elite
(Gabbe, Bennell, Finch, et al., 2006; Orchard, 2001) and community-level (Verrall,
Slavotinek, Barnes, & Fon, 2003) Australian footballers with a history of HSI are at
significantly greater risk of future HSI. The mechanism(s) by which previous HSI increases
future injury risk is unclear, but is likely to reflect a number of maladaptations following HSI
(Opar, et al., 2012) or the persistence of pre-existing risk factors (Bradley & Portas, 2007;
Brockett, Morgan, & Proske, 2004; Croisier, et al., 2002; Jonhagen, Nemeth, & Eriksson,
15
1994; Silder, Heiderscheit, Thelen, Enright, & Tuite, 2008; Silder, Reeder, & Thelen, 2010;
Witvrouw, et al., 2003). Because of a lack of prospective data on these maladaptations, it is
unknown whether these changes result from the injury or whether they were present before,
and were possibly the cause of, the original insult.
Age Increasing age has been identified as a significant predictor of future HSI in Australian
football (Gabbe, Bennell, & Finch, 2006; Opar et al., 2014) and soccer players (Timmins,
Bourne, et al., 2015; Verrall, et al., 2001). The risk of HSI appears to increase by 10% per
year in elite Icelandic soccer players (Arnason, et al., 2004). Older elite Australian football
players (>25 years) are more than four times more likely to experience an injury than are
younger players (<20 years) (Gabbe, Bennell, & Finch, 2006). Similar findings have been
found in community-level AFL, with older players (>23 years) up to four times more likely to
incur an HSI than younger players (<23 years) (Gabbe, Finch, Bennell, & Wajswelner, 2005).
Relatively little is known about the mechanism(s) responsible for the age-related changes that
heighten HSI risk. However, recently we (Opar, et al., 2014; Timmins, Bourne, et al., 2015)
have provided evidence to suggest that this risk might be modulated by one or more
modifiable risk factors. For example, older (>23 years) elite Australian footballers are only at
an elevated risk of HSI if the athlete also has low levels of eccentric knee flexor strength.
Further, in professional soccer players, higher levels of eccentric knee flexor strength and
longer BFLH fascicles appear to offset the elevated risk of HSI associated with increasing age
(Timmins, Bourne, et al., 2015). Others have suggested that age-related reductions in hip
flexor flexibility and increased body mass index (BMI) (Gabbe, Bennell, & Finch, 2006), or
hypertrophy of the lumbosacral ligament (Orchard et al., 2004) may explain the increased
16
susceptibility to HSI. Further work is required to advance our knowledge about how
increasing age influences HSI risk.
2.6.2 Alterable risk factors
Alterable risk factors refer to those functional characteristics that can be modified with
training. For the purposes of this review these will include: muscular weakness or imbalances
in strength (Aagaard, et al., 1998; Arnason, et al., 2008; Askling, et al., 2003; Brockett, et al.,
2001; Burkett, 1970; Croisier, et al., 2002; Croisier, et al., 2008c; Friden & Lieber, 1992;
Gabbe, Bennell, Finch, et al., 2006; Garrett, et al., 1987; Lee, et al., 2009; Mair, et al., 1996;
Orchard, et al., 1997b; Petersen, et al., 2011; Sugiura, et al., 2008; Yamamoto, 1993; Yeung,
et al., 2009); poor flexibility (Bradley & Portas, 2007; Henderson, et al., 2009; McHugh, et
al., 1999; Witvrouw, et al., 2003); fatigue (Brooks, et al., 2006; Heiser, et al., 1984; Mair, et
al., 1996; Opar, et al., 2012; Woods, et al., 2004); and poor lumbopelvic control (Chumanov,
et al., 2007; Sherry & Best, 2004).
Weakness and strength imbalances For the purposes of this review, strength imbalances are between-leg asymmetries in knee
flexor strength and/or a low ratio of knee flexor to knee extensor strength, otherwise known
as the hamstring-to-quadriceps (H:Q) ratio.
Early in situ studies demonstrated that maximally stimulated muscles can tolerate more stress
than those stimulated submaximally (Garrett, et al., 1987; Mair, et al., 1996). A heightened
ability to tolerate stress enables these muscles to absorb more energy before strain injury
occurs (Mair, et al., 1996). Assuming that these in situ results reflect in vivo function, one can
17
infer that stronger muscles are more resistant to strain injury than are weaker muscles
(Garrett, et al., 1987).
Between-limb strength imbalances The concept of a relationship between leg-to-leg (bilateral) strength asymmetries and injury
risk is a logical assumption given the evidence suggesting that weakness may predispose to
strain injury. Between-limb strength imbalances of the knee flexors have been associated
with an increased risk of HSI in several sports (Burkett, 1970; Croisier, et al., 2002; Croisier,
et al., 2008c; Orchard, Marsden, Lord, & Garlick, 1997a). Although the underlying
mechanism remains unknown, it has been proposed that biomechanical alterations arise from
these imbalances and may increase the strain experienced by the weaker hamstrings during
running, thereby increasing HSI risk (Croisier, et al., 2008c).
The largest study examining bilateral strength asymmetries, by Croisier and colleagues
(2008c), used isokinetic dynamometry to determine whether asymmetry could predict future
HSI. The study tested 462 professional soccer players during the preseason period to assess
hamstring strength asymmetry using a standardised concentric and eccentric isokinetic
protocol. At the end of the competitive season, athletes who did not present with strength
imbalances in the pre-season or those who underwent an intervention to correct imbalances
and then completed a subsequent re-test, displayed similarly low incidence rates of HSI
(Croisier, et al., 2008c). In comparison, those with detected asymmetry who chose not to
undergo the intervention were up to four times more likely to suffer an HSI (Croisier, et al.,
2008c). However, it should be acknowledged that only severe injuries (> 30 days to return to
sport) were reported in this study and epidemiological data (Ekstrand, et al, 2011) suggests
that the average return to play time from HSI in professional football is significantly less than
18
this and severe injuries (> 28 days) constitute only a very small percentage (~10%) of total
injuries in this cohort. These data suggest the possibility that a large number of HSIs were not
reported by Croisier and colleagues (2008c) and renders it impossible to determine if athletes
with less severe injuries were also at a greater risk of injury is they presented with isokinetic
strength imbalances. It should also be acknowledged that isokinetic testing was conducted by
multiple clinicians at various sites, using different equipment and different cut-points to
determine pass or fail (Croisier, et al, 2008c) and the reliability of such measures is unclear.
Given these limitations, the results of Croisier and colleagues’ study (2008c) should be
interpreted with caution. Nevertheless, prospective studies of elite-level sprinters with no
history of HSI have also demonstrated that athletes with isokinetically derived knee flexor
asymmetries were more likely to sustain a strain injury in the following 12-24 months
(Sugiura, et al., 2008; Yamamoto, 1993). Similarly, isokinetic strength testing of Australian
footballers showed that players who exhibited unilateral hamstring muscle weakness in the
preseason were significantly more likely to experience HSI throughout the following season
(Orchard, et al., 1997b). Although little is known about the degree of knee flexor asymmetry
required to elevate HSI risk, various guidelines have been suggested. Early research found
that asymmetries of more than 10% are associated with an increased risk of HSI in American
footballers (Burkett, 1970) and track and field athletes (Heiser, et al., 1984). More recent
evidence has shown that Australian footballers with asymmetries of 8% or greater (Orchard,
et al., 1997b) and soccer players with imbalances exceeding 15% (Croisier, et al., 2008c) are
at increased risk of HSI. It should be noted that some prospective studies have found no
relationship between isokinetic strength imbalances and hamstring injury risk (Bennell, et al.,
1998a; Yeung, et al., 2009). However, the size and therefore statistical power of these studies
is almost always inadequate to rule out a link between strength imbalance and risk (Bahr &
Holme, 2003).
19
Future research should continue to explore the risk factors for HSI with an emphasis on
defining the level of knee flexor strength imbalance associated with an increased risk of HSI
across different sports. The strength asymmetries among other muscles which act during
terminal swing, for example the hip flexors, should also be explored because these are known
to affect hamstring mechanics during running (Lee, et al., 2009). Implementation of practical
field-based measures of between-limb hamstring strength may also help to reduce injury rates
in sport.
20
H:Q ratio Throughout the terminal swing phase of running (Figure 2.3), the hamstrings act primarily as
a ‘brake’ by rapidly decelerating the extending knee and flexing hip. This exposes the
hamstrings to moderate degrees of strain and high degrees of stress, which may increase their
susceptibility to injury (Garrett, 1990). The H:Q ratio is calculated as the peak (concentric or
eccentric) hamstring strength divided by peak concentric quadriceps stength (Aagaard, et al.,
1998). Theoretically, an individual with relatively stronger knee extensors and comparatively
weaker knee flexors may have a lesser ability to overcome the inertia imparted on the shank
by the quadriceps during the swing phase. Initially, the H:Q ratio was measured using
concentric knee flexor and concentric knee extensor strength and this is now termed the
conventonal hamstring:quadriceps ratio (H:Qconv) (Burkett, 1970; Orchard, et al., 1997a).
However, this method has been criticised for disregarding the eccentrically biased role of the
hamstrings during high-speed running. As a result, a ‘functional ratio’ involving eccentric
hamstring to concentric quadriceps strength (H:Qfunc) has been proposed (Aagaard, et al.,
1998) and popularised (Croisier, et al., 2008c; Gabbe, Bennell, Finch, et al., 2006; Sugiura, et
al., 2008; Yeung, et al., 2009).
Early small-scale research examining the H:Qconv and its relationship with HSI risk in
Australian footballers found that players with H:Qconv ratios of <0.61 were at significantly
increased risk of sustaining an HSI in the following competitive season (Orchard, et al.,
1997a). Similar studies exploring the H:Qconv ratios in American footballers concluded that
those with a ratio of <0.50 were more likely to experience an HSI during the season (Heiser,
et al., 1984). The most statistically powerful research available (n=462) found that low
H:Qfunc ratios (<0.80–0.89) and low H:Qconv ratios (<0.45–0.47) were associated with a
significantly increased incidence of HSI (Croisier, et al., 2008c). However, there are
21
conflicting data, and several authors have reported no relationship between H:Q ratios and
increased HSI risk (Yeung, et al., 2009; Bennell, et al., 1998). Yeung and colleauges (2009),
for example, found no significant relationship between either H:Qconv or H:Qfunc and
subsequent HSI in sprinters. Bennell and colleagues (Bennell, et al., 1998) also reported no
significant association between either the H:Qconv or the H:Qfunc ratio and future HSI in
Australian footballers. However, these and many studies investigating H:Q ratios have used
relatively small sample sizes and different methodologies. Bahr and colleagues (2003) argue
that this presents an obvious limitation and that sample sizes of >300 are necessary to
accurately detect small-sized associations between H:Q ratios and HSI risk. This must be
considered when interpreting the current literature and future research should explore these
relationships using larger-scale prospective studies.
In prospective studies which examine eccentric hamstring strength and associated strength
ratios as a risk factor for future HSI, isokinetic dynamometry has been the chosen strength
testing methodology (Bennell et al., 1998; Croisier, Ganteaume, Binet, Genty, & Ferret,
2008b; Sugiura, Saito, Sakuraba, Sakuma, & Suzuki, 2008; Yeung, et al., 2009). Whilst
isokinetic dynamometry is considered the gold standard tool for assessing eccentric
hamstring strength, its wide spread application is limited due to the device being largely
inaccessible and expensive to purchase. Further to this, the time taken to complete an
assessment of an individual athlete (up to 20 minutes) normally at an off-site location is often
prohibitive, particularly in elite sporting environments (Opar, Piatkowski, Williams, &
Shield, 2013a). Our group has recently developed a field testing device for the assessment of
eccentric hamstring strength to overcome the limitations of isokinetic dynamometry (Opar,
Piatkowski, et al., 2013a). This device measures eccentric knee flexor force during the
performance of the Nordic hamstring exercise. We recently employed this device in a large-
22
scale prospective study conducted in the elite AFL (n=210) during the 2013 competitive
season (Opar, et al., 2014). Footballers were tested during the pre-season and at three time-
points throughout the season and injury data were collected prospectively. Results
demonstrated that limbs that went on to sustain a HSI were significantly weaker than the
limbs of uninjured athletes at the start and end of preseason, and players with a ‘two-limb
average’ eccentric strength lower than 256 N at the start of preseason or 279 N at the end of
preseason were at 2.7 and 4.3 fold greater risk of sustaining an HSI compared to players
above these thresholds. However, the ‘protective’ effect of extra strength appeared to
diminish at around ~350-400 N. This suggests that there might be no relationship between
strength and HSI risk in running-based sports that are typically characterised by higher levels
of strength, for example rugby union, and this should be a focus of future investigations.
Angle of peak knee flexor torque (T-JA) Previously injured hamstrings have been reported to generate peak torque at greater knee
joint angles (shorter hamstring muscle lengths) compared with the uninjured contralateral
limb (Brockett, et al., 2004). As described in section 2.4.1, if the optimum angle for torque
generation is at a shorter relative muscle length, more of that muscle’s working range is on
the descending limb of the force–length relationship and the muscle may be more susceptibile
to damage (Morgan, 1990). It is suspected that those who generate peak torque at shorter
muscle lengths would be more prone to accumulated microscopic damage in the form of
sarcomere over-extension (also known as sarcomere ‘popping’), which may, if it accumulates
sufficiently, give rise to macroscopic strain injury (Brockett, et al., 2004).
Early retrospective work by Brockett and colleagues (2004) found that athletes with a history
of unilateral HSI produced peak knee flexor torque at markedly shorter muscle lengths than
23
uninjured athletes. In a group of elite Australian footballers and sub-elite track and field
athletes, peak torque was shifted by 12.1° ± 2.7° towards a more flexed knee in the
previously injured limb when compared to the uninjured contralateral limb (Brockett, et al.,
2004). However, given the retrospective nature of this study, one cannot determine whether
the altered angle of peak torque was the cause or result of the injury. A subsequent small and
therefore underpowered prospective study of national and international-level sprinters found
no relationship between the angle of peak knee flexor torque and the incidence of HSI
throughout the competitive season (Yeung, et al., 2009). A larger scale study is required to
ascertain whether the angle of peak torque is a significant predictor of HSI risk.
Biceps femoris long head (BFLH) fascicle length
Recently, Timmins et al., (2014) demonstrated that athletes with a history of HSI display
shorter BFLH fascicles coupled with increased pennation angles in their previously injured
limb when compared to their uninjured contralateral limb. A subsequent prospective study in
elite soccer players demonstrated that short BFLH fascicles (<10.56cm) increased the risk of
HSI four-fold (Timmins, Bourne, et al., 2015). Moreover, longer fascicles appeared to off-set
the increased risk of HSI associated with increasing age and prior HSI, which were
previously considered to be non-modifiable risk factors. Reduced fascicle lengths most likely
result from the shedding of in-series sarcomeres (Lieber & Friden, 2000), although it is
difficult to determine whether this causes or results from injury. Fewer serial sarcomeres
would be expected to shift the muscles force-length relationship to the left, thereby increasing
its susceptibility to muscle damage at longer lengths. Fortunately, muscle architecture has the
potential to be altered with appropriately structured resistance training. For example,
Timmins et al., (2015) recently demonstrated a significant increase in BFLH fascicle length
coupled with a reduction in pennation angle in response to six weeks of eccentric-only
24
isokinetic knee flexor training. However, few athletes train exclusively with isokinetic
devices and further work is needed to determine the adaptability of muscle architecture to
different strength training interventions.
Flexibility Increased flexibility has long been considered important in injury prevention, despite little
prospective evidence (Witvrouw, et al., 2003; Worrell, Smith, & Winegardner, 1994). It has
been proposed that high forces produced during eccentric contractions are absorbed by the
active contractile components and the passive in-series elements of muscle (Bennell, et al.,
1998a). Early research suggested that greater compliance of the passive elastic structures may
increase the energy absorption capabilities of the MTU (Worrell, et al., 1994), thereby
reducing the loads placed on the active contractile elements of the muscle and mitigating the
risk of strain injury (Garrett, et al., 1987; Garrett, 1990). However, large-scale prospective
studies using objective measures of flexibility have identified no relationship between
flexibility and future HSI in either elite Australian Football players (Gabbe, Bennell, Finch, et
al., 2006; Orchard, et al., 1997b) or elite American footballers (Burkett, 1970). However,
these studies used only the sit-and-reach test to measure flexibility, which is limited by its
inability to identify between-leg differences because both legs are tested simultaneously.
Furthermore, the test can be influenced by lumbar spine flexibility and upper to lower limb
length ratios. Subsequent studies using the toe-touch test, also found no relationship between
poor flexibility and injury risk in elite Australian footballers (Bennell, Tully, & Harvey,
1999). Moreover, there is no correlation between active (Gabbe, et al., 2005) and passive
(Arnason, et al., 2004) knee flexor stiffness and HSI incidence in Australian footballers
(Gabbe, et al., 2005) or professional soccer players (Arnason, et al., 2004). By contrast, a
prospective study by Witvrouw and colleagues (Witvrouw, et al., 2003) found that elite
25
soccer players (n=146) who exhibited a passive straight-leg raise of less than 90° were at
significantly greater risk of a subsequent HSI. However, the use of the straight-leg raise has
been criticised for being more indicative of neural extensibility than hamstring muscle
flexibility (Devlin, 2000).
Despite an unclear relationship between reduced flexibility and subsequent HSI risk, there is
some evidence to suggest that individuals with a history of HSI are less flexible than
uninjured people (McHugh, et al., 1999; Witvrouw, et al., 2003). Several studies have
demonstrated that sprinters (Jonhagen, et al., 1994), American footballers (Worrell & Perrin,
1992) and elite soccer players (Ekstrand & Gillquist, 1983) with a history of HSI exhibit
ongoing deficits in hamstring flexibility. This may be a result of scar tissue formation, a
known maladaptation to previous HSI (Silder, et al., 2010), however these studies are again
limited by the use of a retrospective study design (Bahr & Holme, 2003). In addition, the
subjective measures of flexibility used in these studies lack validity (Opar, et al., 2012),
which may affect their interpretation (Bahr & Holme, 2003)
Fatigue Fatigue is commonly implicated as a potential cause of HSI (Heiser, et al., 1984; Mair, et al.,
1996). Epidemiological evidence shows an increased incidence of HSI during the latter stages
of practice or competition (Brooks, et al., 2006; Woods, et al., 2004). Fatigue reduces the
capacity of the muscle to generate contractile force, which limits the energy-absorbing ability
of the MTU in vivo (Mair, et al., 1996). Muscular fatigue occurs through both central and
peripheral mechanisms. Central fatigue can be defined as a reduction of maximum force
generating capacity due to a diminished capacity to voluntarily activate a muscle (Shield &
Zhou, 2004), whereas peripheral fatigue is a reduction in the maximum capacity of the
26
muscle itself caused by a number of changes occurring distal to the neuromuscular junction
(Aagaard et al., 2000).
In situ animal studies were the first to suggest that the energy-absorbing capability of a
muscle is diminished in a fatigued state and that this is related to a reduction in contractile
strength (Garrett, et al., 1987; Mair, et al., 1996). While both fatigued and non-fatigued
muscles failed at the same relative muscle length (Mair, et al., 1996) the non-fatigued in situ
muscle is able to absorb more energy before stretch-induced MTU failure, which suggests
that fatigue may limit a muscle’s ability to prevent over lengthening.
Fatigue has also been shown to induce a number of proprioceptive changes in humans (Allen,
Leung, & Proske, 2010; Brown, Child, Donnelly, Saxton, & Day, 1996; Skinner, Wyatt,
Hodgdon, Conard, & Barrack, 1986). Allen and colleagues (Allen, et al., 2010) recently
demonstrated that after fatiguing exercise of the knee flexors, subjects perceived their knee to
be in a more flexed position than it actually was. The authors suggested that alterations at the
level of the sensorimotor cortex were responsible (Allen, et al., 2010). In a separate study,
hamstring fatigue led to alterations in hamstring muscle kinematics during running (Pinniger,
Steele, & Groeller, 2000). Following a fatiguing intermittent running protocol and knee
flexor resistance training session, subjects displayed a significant reduction in hip flexion and
a concomitant increase in knee extension during the swing phase of high-speed overground
running (Pinniger, et al., 2000). Concurrent sEMG demonstrated an increase in the duration
of hamstring electromyographical activity throughout the swing phase of gait (Pinniger, et al.,
2000). An inability to sense knee position accurately may cause an underestimation of
hamstring length, potentially increasing susceptibility to repeated over-lengthening which
may require greater muscle activity to correct.
27
Interestingly, hamstring fatigue following intermittent running has been reported to be
confined primarily to reductions in eccentric strength (Greig, 2008; Opar, Williams, Porter, &
Raj, 2009). This eccentric-specific decline was prevalent without any deficits in concentric
knee flexor or extensor strength and exhibited a high degree of individual variability (Greig,
2008; Opar, et al., 2009). These findings are particularly interesting given the propensity for
HSI to occur during forceful eccentric contractions (Brockett, et al., 2004; Croisier, 2004;
Garrett, 1990).
Lumbopelvic stability Poor neuromuscular control of the lumbopelvic region, specifically the uniarticular hip
flexors (psoas major and minor and iliacus) is a recently proposed factor in HSI (Sherry &
Best, 2004). Shortening of the uniarticular hip flexors during the early swing phase of
running has been shown to induce significant stretch on the contralateral hamstrings, most
notably the BFLH, through increased anterior pelvic tilt (Chumanov, et al., 2007). Chumanov
(Chumanov, et al., 2007) proposed that perturbations in coordination of the uniarticular hip
flexors increase strain on the biarticular hamstrings during running, particularly as speeds
increase (Chumanov, et al., 2007). To date, research on lumbopelvic stability is limited to
biomechanical models of joint kinematics, and further randomised controlled trials are
required to establish the validity of this theory.
28
2.7 FACTORS UNDERPINNING HIGH RATES OF HAMSTRING STRAIN INJURY RECURRENCE
HSI is known to trigger a number of structural and functional maladaptations which may
augment the risk of re-injury. Of particular interest to this review is the interrelationship
between previous HSI and muscular weakness. Previously injured hamstrings have been
reported to possess significant deficits in eccentric strength, in the presence of smaller or
absent concentric strength deficits when compared to the uninjured contralateral limb (Figure
2-2) (Croisier, 2004; Croisier, et al., 2002; Dauty, Potiron-Josse, & Rochcongar, 2003;
Jonhagen, et al., 1994; Lee, et al., 2009). Croisier and colleagues (2002) were the first to
suggest that isokinetically-derived strength imbalances increase the risk of hamstring strain
re-injury. The comprehensive testing battery determined that 18 of 26 athletes with a previous
HSI who experienced ongoing hamstring pain also exhibited knee flexor strength
asymmetries (Croisier, et al., 2002). These strength imbalances were defined as leg to leg
differences in knee flexor strength of >15%, concentric knee flexor to concentric knee
extensor strength (H:Qconv) <0.47, and eccentric knee flexor to concentric knee extensor
strength (H:Qfunc) <0.80 (Croisier, et al., 2002). Of interest was the preferential reduction of
eccentric peak torque (~22%) compared with concentric torque (~11%) (Figure 2-2)
(Croisier, et al., 2002). Athletes with predetermined strength deficits were prescribed
individualised rehabilitation programs to restore a normalised isokinetic strength profile and
correction of these abnormalities resulted in a marked reduction in pain and discomfort.
Furthermore, none of the athletes sustained a clinically diagnosed HSI in the 12 months
following the intervention and all were successfully able to return to their pre-injury levels of
competition (Croisier, et al., 2002).
29
Figure 2-2. Comparison of knee flexion torque-velocity relationships between previously
injured hamstrings, contralateral uninjured hamstrings and reference values from uninjured
control subjects. Note the greater deficit in eccentric compared to concentric strength in
previously injured hamstrings (Croisier & Crielaard, 2000).
While it is possible that strength deficits may be present prior to the original insult (Croisier,
et al., 2008c; Sugiura, et al., 2008; Yeung, et al., 2009), evidence suggests that bilateral
asymmetries are amplified following HSI. For example, Sugiara et al. (Sugiura, et al., 2008)
reported that eccentric strength deficits of ~4.5% were predictive of future HSI in uninjured
elite sprinters, while Croisier et al. (2002) identified much larger deficits of 22-24% in
previously injured elite soccer players. Compounding the issue further is the observation that
these deficits appear to be long-lasting, with several studies identifying deficits months to
years’ post-injury (Croisier, et al., 2002; Dauty, et al., 2003; Jonhagen, et al., 1994; Lee, et
al., 2009).
30
2.8 MECHANISM(S) FOR CHRONIC STRENGTH DEFICITS FOLLOWING HAMSTRINGS STRAIN INJURY
Given several lines of supportive evidence, previously injured hamstrings appear to be
considerably weaker during eccentric contractions compared to uninjured hamstrings
(Croisier, 2004; Croisier, et al., 2002; Jonhagen, et al., 1994; Lee, et al., 2009). However, the
mechanism(s) responsible for greater eccentric strength loss, compared with concentric
strength loss following HSI, remains to be determined. Recently it has been proposed that
chronic deficits in hamstring voluntary activation, which can be defined as the completeness
of skeletal muscle activation during voluntary contractions (Shield & Zhou, 2004), may
manifest following HSI as a result of persistent neuromuscular inhibition (Opar, et al.,
2012).The role of neuromuscular inhibition after other injuries is well established. For
example, substantial and long-lasting deficits in quadriceps maximal activation have been
observed following traumatic knee injury (Hurley, 1997; Urbach, Nebelung, Becker, &
Awiszus, 2001). Likewise, injury to the ankle joint has been linked to reductions in plantar
flexor activation (Hurley, 1997). In addition, experimentally induced joint and muscle pain
has been shown to reduce voluntary drive to nearby muscles as well as alter inter-muscular
coordination patterns (Diederichsen et al., 2009). The presence of significant eccentric
strength deficits combined with smaller or absent losses in concentric strength is suggestive
of a severe contraction mode-specific decline in voluntary activation (Croisier & Crielaard,
2000). Previous investigations from this student’s Honours project demonstrated significant
muscle-specific reductions in activation of previously injured hamstring muscles, relative to
uninjured contralateral hamstring muscles during a common rehabilitation exercise (Bourne,
D., Williams, Al-Nijjar, & Shield, 2015). Furthermore, evidence of hamstring remodelling 5-
23 months post-HSI, specifically, atrophy of the previously injured muscle (most likely via
limited activation) and concomitant hypertrophy of synergists (Silder, et al., 2008), suggests a
31
chronic de-loading of the previously injured muscle and the existence of compensatory
activation strategies (Silder, et al., 2008).
2.9 NEUROMUSCULAR INHIBITION
Discrepancies between the force-velocity relationships of isolated, electrically stimulated
muscles (in vitro) and voluntarily activated muscle (in vivo) indicate the inability of healthy
but untrained individuals, to maximally activate certain muscles during eccentric contractions
(Figure 2-3) (Westing, Cresswell, & Thorstensson, 1991; Westing, Seger, Karlson, &
Ekblom, 1988). The force-velocity relationship of electrically stimulated human muscle
demonstrates that during concentric contractions maximal force generation declines as the
rate of shortening increases (Katz, 1939; Westing, et al., 1988), while eccentric contractions
are characterised by markedly higher maximal forces that plateau at levels up to 100% greater
than peak isometric force (Katz, 1939; Westing, et al., 1991).
32
Figure 2-3. The torque/force-velocity relationships of electrically stimulated (red) and
voluntarily activated (blue) skeletal muscle. Note the divergence in maximal eccentric
force/torque, indicating the existence of a tension-limiting mechanism(s) during volitional
eccentric contractions.
Although the force-velocity curves of electrically stimulated and voluntarily activated
skeletal muscle display similarities in their concentric and isometric portions (Thorstensson,
Grimby, & Karlsson, 1976; Westing, et al., 1988), clear differences can be noted in the
eccentric portion of these relationships (Edman, Elzinga, & Noble, 1978; Katz, 1939).
Specifically, during eccentric contractions voluntarily activated muscle fails to reach the
levels of maximal force obtained by isolated muscle (Edman, et al., 1978; Westing, et al.,
1988) (Figure 2-3). This evidence suggests that voluntarily activated muscles are not fully
activated during active lengthening despite maximal voluntary effort (Westing, et al., 1991).
The divergence of the voluntarily activated force-velocity curve from that observed for
33
isolated muscle appears to be the result of a tension-limiting mechanism(s) that acts to reduce
the extent of force produced during eccentric contractions (Babault, Pousson, Michaut,
Ballay, & Hoecke, 2002; Westing, et al., 1991). By limiting the development of excessive
force within the MTU, this mechanism may protect the musculoskeletal system from an
injury that could result if the muscle was to be fully activated (Babault, et al., 2002; Westing,
et al., 1991).
2.9.1 Evidence for incomplete activation in maximal voluntary contractions
Studies exploring voluntary activation of the knee extensors and flexors through the use of
the interpolated twitch technique (Amiridis et al., 1996; Babault, et al., 2002; Beltman,
Sargeant, Mechelen, & Haan, 2004; Westing, et al., 1991) and sEMG (Aagaard, et al., 2000;
Amiridis, et al., 1996; Onishi et al., 2002; Ono, Higashihara, & Fukubayashi, 2011; Ono,
Okuwaki, & Fukubayashi, 2010; Westing, et al., 1991) have demonstrated incomplete
activation during maximal eccentric (Kellis & Baltzopoulos, 1998) and slow concentric
(Aagaard, et al., 2000) contractions.
Twitch interpolation is the most commonly used method for assessing the completeness of
skeletal muscle activation (Belanger & McComas, 1981; Shield & Zhou, 2004). Twitch
interpolation typically involves the application of a supramaximal electrical stimulus to an
active muscle(s), during voluntary isometric and/or dynamic contractions (Shield & Zhou,
2004). While some studies suggest that maximal voluntary activation is possible during
concentric contractions of muscles such as the biceps brachii (Gandevia, 1998), there is
evidence for deficits in maximal activation during eccentric actions of the knee extensors
(Babault, et al., 2002; Beltman, et al., 2004). For instance, Babault (2002) compared knee
extensor activity during maximal isometric, concentric and eccentric isokinetic contractions
34
and reported voluntary activation levels of 95.2% during isometric contractions, in contrast
with 88.3% and 89.7% for maximal eccentric and concentric contractions, respectively. A
subsequent study employing a similar protocol reported even greater activation deficits
during eccentric contractions (79%), compared with concentric (92%) and isometric (93%)
contractions (Beltman, et al., 2004). These results suggest that activation of the knee
extensors is reduced primarily during eccentric contractions, however to date no studies have
validated the interpolated twitch technique for assessing this in the knee flexors.
Surface EMG provides a global measure of the electrical contributions made by the active
motor units (MUs), as detected by electrodes placed on the skin overlying the active muscle
(Farina, Merletti, & Enoka, 2004). This technique provides further evidence for incomplete
activation during maximal voluntary contractions, as sEMG amplitude is reduced during
eccentric and slow concentric contractions, when compared to faster concentric contractions
(Aagaard, et al., 2000; Amiridis, et al., 1996; Kellis & Baltzopoulos, 1998; Westing, et al.,
1991). Interestingly, this reduction in sEMG is seen despite an increased torque-generating
capacity associated with eccentric contractions (Katz, 1939; Westing, et al., 1991) (Figure 2-
3). For instance, Kellis and Baltzopoulos (1998) measured sEMG of the knee extensors and
flexors during maximal eccentric and concentric isokinetic contractions at a range of
velocities. Results demonstrated that normalised EMG of both extensor and flexor muscle
groups was significantly lower during eccentric contractions, when compared to their
respective concentric values (Kellis & Baltzopoulos, 1998). Similarly, Westing et al. (1991)
explored the sEMG-velocity relationship of the knee extensors and found that sEMG
amplitudes were significantly reduced during eccentric contractions when compared to
concentric contractions, despite greater torque values at all eccentric testing velocities. This
35
evidence is suggestive of neuromuscular inhibition of the knee flexors and extensors during
maximal voluntary eccentric contractions.
Limitations of inferring activation strategies from surface electromyography (sEMG) While sEMG is the only tool currently used in the assessment of knee flexor voluntary
activation, it should be acknowledged that this technique has a number of limitations. The
amplitude of sEMG is proportional to the net motor unit (MU) activity and therefore reflects
the recruitment and discharge rates of active MUs (Farina, et al., 2004). While this is
theoretically an index of the extent of muscle voluntary activation, sEMG amplitude is
influenced by several other factors including electrode location (Farina, Cescon, & Merletti,
2002), subcutaneous tissue (Farina, et al., 2004), the distribution of MU conduction velocities
(Arendt-Nielsen & Zwarts, 1989) and the degree to which MU firing is synchronous (Yao,
Fuglevand, & Enoka, 2000). Indeed, the coefficient of variation for repeated sEMG
measurements has been reported to be as high as 23% (Veiersted, 1991). Furthermore, while
sEMG displays excellent temporal resolution, its spatial resolution is relatively poor. Given,
the anatomical complexity of the hamstring muscle group (Woodley & Mercer, 2005), and
the observation that the hamstrings display non-uniform activation during running (Schache,
et al., 2012) and during different strengthening exercises (Ono, et al., 2011; Ono, et al.,
2010), it is possible that sEMG is limited in its capacity to assess activation in this muscle
group. Fine wire EMG overcomes some of these limitations and has been used previously to
assess the hamstring EMG-joint angle relationship (Onishi, et al., 2002). While it should be
acknowledged that this technique potentially allows for a more accurate spatiotemporal
assessment of electromyographical activity (Ciccotti, Kerlan, Perry, & Pink, 1994), its use
not widespread because of its invasive nature.
36
Assessing spatial activation via functional magnetic resonance imaging (fMRI)
Functional magnetic resonance imaging (fMRI) is a unique technique that allows for a high-
resolution spatial assessment of the size and functional characteristics of muscles. For two
decades this method has been established to noninvasively assess patterns and quantify the
extent of skeletal muscle activation during exercise (Adams, Duvoisin, & Dudley, 1992;
Foley, Jayaraman, Prior, Pivarnik, & Meyer, 1999; Jayaraman et al., 2004; Kinugasa,
Kawakami, & Fukunaga, 2006; Mendiguchia et al., 2004; Ono, et al., 2011; Ono, et al.,
2010). The premise of using fMRI to assess voluntary activation is that exercise increases the
proton transverse (spin-spin) (T2) relaxation time of skeletal muscle in fMRI images (T2
1/2<20 min) (Jayaraman, et al., 2004) and this shift has been shown to increase proportionately
with exercise intensity (Adams, et al., 1992; Adams, Harris, Woodard, & Dudley, 1993;
Fisher, Meyer, Adams, Foley, & Potchen, 1990; Fleckenstein et al., 1991). Exercise-induced
increases in T2 relaxation times are proportional to EMG measures of neuromuscular
activation (Adams, et al., 1992) and to isometric torque evoked by electrical stimulation of
skeletal muscle (Adams, et al., 1993). Functional MRI also provides high-resolution
assessment of muscle cross-section and volume. Given the complexity of muscle architecture
and neural innervations, fMRI presents a unique advantage in its ability to sample the entire
length of the muscle. Recently, fMRI has been used to assess spatial patterns of knee flexor
muscle activation during different hamstring strengthening exercises (Mendiguchia, Arcos, et
al., 2013a; Mendiguchia, Garrues, et al., 2013; Ono, et al., 2011; Ono, et al., 2010). Further,
this student’s Honours project was the first to use fMRI to explore the impact of previous HSI
on spatial activation patterns of the hamstring muscles (Bourne, et al., In review).
37
2.9.2 Mechanism(s) underpinning neural inhibition
Currently, the precise mechanism(s) responsible for inhibition of hamstring motoneuron
activation remain unclear (Aagaard, et al., 2000). It is known that maximal voluntary
activation is moderated by both reflex sensory (afferent) pathways and central descending
pathways (Gandevia, 1998). Sensory afferent pathways originate from muscle spindles
(group Ia and II), Golgi tendon organs (group Ib) and group III and IV afferents from the skin
and joint receptors (Figure 2-4). It has been postulated that the reduction in maximal
voluntary activation observed during eccentric and slow concentric contractions is most
likely a result of inhibitory feedback from Golgi Tendon organs (group IIb afferents) and
excitatory feedback from group Ia muscle spindles (Aagaard, et al., 2000). This is because
these afferents converge onto the entire motoneuron pool from both agonist (homonymous
afferent pathways) and antagonist muscles (heteronymous pathways) and therefore possess
the greatest ability to monitor tension throughout the entire MTU (Gordon, 1991) and
throughout the entire physiological range of force graduation (Houk, Crago, & Rymer, 1980).
However, conflicting evidence suggests that sensory output from group IIb afferents in
particular, is maximised at approximately 20-50% of MVC which would indicate that their
involvement at higher levels of force development is limited (Rymer, Houk, & Crago, 1979).
Indeed, it is now recognised that group IIb afferents may also exert excitatory effects on the
muscles they innervate in certain movement contexts (Rio, Kidgell, Purdam, Gaida, Moseley,
Pearce & Cook, 2015; Pratt, 1995). Reflex pathways from joint and ligament receptors (group
II and III afferents) may also inhibit motoneuron activation in conditions of high tensile
loading (Aagaard, et al., 2000). Certainly, evidence of an inhibitory reflex pathway from the
human ACL to the quadriceps muscles has been reported previously (Dyhre-Poulsen &
Krogsgaard, 2000).
38
Figure 2-4. A simplified scheme of the afferent synaptic inputs to alpha (ά) and gamma (γ)
motoneurones (MN). Open and filled circles represent excitatory and inhibitory neurones,
respectively. Shown are the type Ia and type II afferents from the muscle spindles, type Ib
afferents from Golgi tendon organs and type III and IV afferents from the agonist muscle and
the skin and joint structures (From Gandevia, 1998).
2.9.3 The impact of resistance training on skeletal muscle activation
It appears that resistance training may modulate the mechanism(s) responsible for limiting
voluntary activation during high force contractions (Aagaard, et al., 2000; Amiridis, et al.,
1996). For instance, heavy progressive-intensity resistance training has been shown to
increase maximal voluntary activation of quadriceps in untrained men (Aagaard, et al., 2000).
In this study (Aagaard, et al., 2000) pre-training EMG activity of the quadriceps was
considerably lower during maximal voluntary eccentric and slow concentric contractions,
when compared to fast concentric contractions. However, following a 14-week (38 sessions)
39
period of high-intensity resistance training, inhibition of quadriceps activation was either
reduced or completely removed. In addition, the increase in activation was accompanied by
significant increases in quadriceps strength during slow concentric and eccentric contractions
(Aagaard, et al., 2000). In a separate isokinetic knee extension investigation (Amiridis, et al.,
1996), elite-level high jumpers displayed significantly greater maximal activation of
quadriceps during eccentric contractions when compared to healthy untrained individuals,
suggesting that long-term conditioning to high-force loading may inhibit the tension-limiting
mechanism(s) in human quadriceps. More recently, Rio et al (2015) employed EMG and
transcranial magnetic stimulation on six athletes with patella tendinopathy, to determine the
effect of an acute bout of isometric resistance exercise for the quadriceps on corticospinal
excitability. Following isometric exercise, these athletes displayed a significant reduction in
corticospinal inhibition to the quadriceps, which was accompanied by an increase in
isometric knee extensor strength and a concurrent reduction in pain. These changes, which
persisted for at least 45 min after the cessation of the training stimulus, highlight the
effectiveness of resistance training on modulating voluntary drive, and demonstrate that the
time-course of these adaptations may be quite rapid (Rio, et al, 2015).
The role of resistance training in modulating the tension-regulating mechanism(s) of skeletal
muscle can be further explained by the fact that strength increases significantly more than
muscle CSA in the early weeks of resistance training (Higbie, Cureton, Warren, & Prior,
1996; Narici, Roi, Landoni, Minetti, & Cerretelli, 1989). Following short bouts of resistance
training, several studies have reported an increase in MU firing rates (Van Cutsem,
Duchateau, & Hainaut, 1998), enhanced reflex potentiation (motoneurone excitability)
(Milner-Brown & Lee, 1975; Sale, Upton, McComas, & MacDougall, 1983), and increased
EMG activity during MVC’s (Hakkinen, Alen, & Komi, 1985; Hakkinen & Komi, 1986;
40
Komi & Buskirk, 1972; Narici, et al., 1989). These adaptations have also been shown to be
reversed with detraining (Hakkinen, et al., 1985; Narici, et al., 1989). Other studies have
demonstrated a reduction of the bilateral deficit (Häkkinen et al., 1996) and cross-education
from trained limbs to untrained contralateral limbs (Hortobagyi et al., 1996; Moritani &
DeVries, 1979; Weir, Housh, Housh, & Weir, 1995). All of these findings are suggestive of
positive adaptations in neural control of muscle function as a consequence of training.
2.9.4 The impact of pain and injury on skeletal muscle activation
The pain-adaptation model proposed by Lund, Donga, Widmer and Stohler (1991) suggests a
relationship between musculoskeletal pain and motor activity. This theory suggests that in
painful conditions, voluntary activation of agonistic muscles is reduced, while voluntary
activation of antagonistic muscles is increased (Lund, et al., 1991). For example, following
ACL rupture, significant and long-term deficits in quadriceps activity have been observed
(Hurley, 1997; Urbach, et al., 2001) and in one study these alterations persisted despite the
return of joint stability two years after reconstruction (Urbach, et al., 2001). Deficits in
quadriceps activation have also been reported in individuals with knee (Hurley, 1997) and hip
(Suetta et al., 2007) osteoarthritis (OA), patella tendinopathy (Rio, et al, 2015) and anterior
knee pain (Suter, Herzog, & Bray, 1998) and those with lower back pain (Suter & Lindsay,
2001). Similar reductions in voluntary activation have been reported for the plantar flexors
following traumatic ankle injury (Behm & St-Pierre, 1997).
Experimentally-induced pain has also been shown to inhibit muscle activation and impair
coordination patterns during static and dynamic motor functions. Intramuscular injection of
hypertonic saline is associated with reduced torque production and movement velocity
41
(Svensson, Houe, & Arendt-Nielsen, 1997), reduced sEMG amplitude (Graven-Nielsen,
Svensson, & Arendt-Nielsen, 1997; Svensson, et al., 1997) and a decline in MU firing rates
(Sohn, Graven‐Nielsen, Arendt‐Nielsen, & Svensson, 2000) in the painful muscle. For
example, saline injections into the supraspinatus muscle have been shown to reduce agonist
(deltoid and upper trapezius) activity and increase antagonist muscle activity (latissimus dorsi
and lower trapezius) during shoulder elevation (Diederichsen, et al., 2009). Hodges and
colleagues (2009) demonstrated similar reductions in quadriceps activation following saline
injections into the infrapatellar fat pad. In this study participants displayed delayed activation
of vastus medialis obliquus during stair climbing, relative to the ipsilateral pain-free vastus
lateralis. They also displayed a reduction in vastus lateralis activation when compared to the
homologous vastus lateralis in the pain-free contralateral limb (Hodges, et al, 2009). Such
adaptations lend further support to the notion that voluntary activation is inhibited to avoid
pain provocation from muscle contraction.
2.9.5 Evidence for neuromuscular inhibition following hamstring strain injury
Findings from this student’s Honours project (Appendix A) suggest that previously injured
hamstring muscles display long-lasting deficits in activation compared to uninjured
contralateral muscles during a common eccentric conditioning exercise, known as the Nordic
hamstring exercise (NHE) (Bourne, et al, 2015) (Figure 2-5). During a bout of NHEs
previously injured muscles (mean time of 9.8 months post-injury) were approximately 40%
less active than homonymous BFLH muscles in the uninjured contralateral limb as assessed by
fMRI (Figure 2-5). These observations support recent findings from our laboratory of
reduced levels of sEMG activity in previously injured BF muscles when compared to the
uninjured contralateral BF muscles during eccentric but not concentric isokinetic contractions
42
(Opar, Williams, Timmins, Dear, & Shield, 2013a). This potentially explains the
mechanism(s) for why previously injured hamstrings display considerable deficits in
eccentric strength in the presence of smaller or absent concentric strength deficits (Croisier,
2004; Croisier, et al., 2002; Jonhagen, et al., 1994; Lee, et al., 2009).
Figure 2-5. Percentage change in fMRI T2 relaxation times of each hamstring muscle for
both the previously injured (inj) and uninjured (uninj) limbs. Values are expressed as a mean
percentage change compared to the values at rest. * indicates a significant difference
between limbs for individual muscles (p<0.05). Error bars depict standard deviation. BFLH,
biceps femoris long head; BFSH, biceps femoris short head; ST, semitendinosus; SM,
semimembranosus.
43
2.9.6 Impact of neuromuscular inhibition on hamstring muscle morphology and architecture
Previously injured hamstrings have been reported to exhibit chronic alterations in hamstring
muscle and tendon morphology (Silder, et al., 2008). Silder and colleagues (2008) conducted
MRI on 14 athletes with a history of HSI 5-23 months post injury and five uninjured controls
to investigate between-limb differences in hamstring morphology following injury. Athletes
who had previously strained the BFLH (n=13) displayed significant reductions in BFLH muscle
volumes (Figure 2-6) and this residual atrophy was often accompanied by concomitant
hypertrophy of the ipsilateral BFSH. The authors suggested that these morphological
differences may have been influenced by several factors including the severity of the insult,
the frequency, intensity and modality of exercises employed in rehabilitation, as well as the
intensity of training upon return to competition (Silder, et al., 2008). However, it was
concluded that chronic hypertrophy of BFSH was most likely an exercise-induced
compensation for atrophy of BFLH, in an effort to conserve global knee flexion strength
(Silder, et al., 2008). This evidence is strongly supportive of persistent neuromuscular
inhibition of the previously injured BFLH.
44
Figure 2-6. MRI image illustrating a previously injured BFLH (right limb) and uninjured
contralateral BFLH (left limb). Note the atrophy of the previously injured BFLH with
corresponding hypertrophy of the BFSH, relative to the uninjured contralateral limb (Silder et
al., 2008).
Neuromuscular inhibition following HSI has also been reported to account for fascicular
shortening in the previously injured muscle (Fyfe, Opar, Williams, & Shield, 2013b).
Timmins et al. (2014) have recently reported that previously injured BFLH muscles display
significantly shorter fascicles, coupled with increased pennation angles, compared to
homologous muscles in the uninjured contralateral limb. The authors proposed that a reduced
capacity to activate the previously injured muscle throughout the rehabilitation process
(particularly during eccentric contractions) (Opar, Williams, et al., 2013a), may result in a
shedding of serial sarcomeres. This reduction in serial sarcomeres should result in a leftward
shift of the BFLH’s force-length relationship (Reeves, Narici, & Maganaris, 2004), which may
increase its susceptibility to damage at longer lengths such as those experienced in the
terminal-swing phase of high-speed running (Brockett, et al., 2001). The restoration of BFLH
fascicle lengths is an important component of rehabilitation, in light of recent evidence
showing that professional soccer players with short BFLH fascicles are four times more likely
to suffer an HSI than those with longer fascicles (Timmins, Bourne, et al., 2015).
45
Figure 2-7. Architectural characteristics of the injured BFLH and the contralateral uninjured
BFLH in the previously injured group at all contraction intensities (p<0.05).
2.9.7 Neuromuscular inhibition as a mechanism for high rates of hamstring strain injury recurrence
Recently, our group proposed a novel conceptual framework for the development of
neuromuscular inhibition following an HSI and its potential role in HSI recurrence (Figure 8)
(Fyfe, Opar, Williams, & Shield, 2013a; Opar, et al., 2012). Given the known relationships
between experimentally-induced pain and deficits in maximal voluntary activation of local
musculature, it is logical to expect a degree of acute neuromuscular inhibition immediately
following an HSI. We hypothesise that the pain associated with the initial insult triggers an
acute alteration of neural control designed to protect the injured muscle fibres and fascicles
and connective tissues from further damage. A reduced ability to activate the previously
46
injured muscle, particularly during eccentric actions and at longer muscle lengths, would
result in a number of acute and potentially chronic changes to muscle structure and function,
including a reduction of peak eccentric torque (Graven‐Nielsen, Lund, Arendt‐Nielsen,
Danneskiold‐Samsøe, & Bliddal, 2002), a loss of serial sarcomeres (Brockett, et al., 2004),
and potentially, resultant atrophy of the injured muscle (Silder, et al., 2008). Although
deficits in activation appear to be an acute response to the pain associated with injury,
compensatory activation strategies ‘learned’ during rehabilitation may result in a chronic ‘re-
wiring’ of neural pathways (Hodges & Tucker, 2011). These changes are likely to occur at
multiple levels of the nervous system in an effort to redistribute motor activity within and
between muscles (Hodges & Tucker, 2011). Indeed, the resolution of experimentally-induced
pain or injury does not automatically trigger a return to initial motor patterns (Hodges &
Tucker, 2011), and it is possible that these pain-induced patterns may become ingrained
during rehabilitation and may still persist even when athletes are deemed fit to return to
competition. If neuromuscular inhibition is not addressed during the rehabilitative process
then the athlete is left weaker during eccentric contractions and more susceptible to muscle
damage and together, these factors are likely to predispose them to a heightened risk of re-
injury.
47
Figure 2-8. Conceptual model for the development of neuromuscular inhibition following
hamstring strain injury and its potential role in injury recurrence. * Particularly at long
muscle lengths, # biceps femoris (BF) specific (Fyfe et al., 2013).
48
Chapter 3: PROGRAM OF RESEARCH
The goals of this program of research are to 1) further examine the role of eccentric knee
flexor strength and between-limb imbalances in hamstring injury occurrence; 2) explore the
neuromuscular mechanism(s) which may underpin high rates of HSI recurrence; and 3) in an
effort to improve HSI prevention strategies, characterise the activation patterns and the
architectural and morphological adaptations of the hamstrings to difference strength training
exercises.
One major aim of this program of research is to further examine the association between
eccentric hamstring strength and injury risk in sport. Recently our group has developed a
novel field testing device for the assessment of eccentric hamstring strength which overcomes
some of the limitations of isokinetic dynamometry (Opar, Piatkowski, Williams, & Shield,
2013). Using the commonly employed NHE, the device is able to record maximal eccentric
hamstring strength and between limb imbalances in less than two minutes. In two recent large
scale prospective studies conducted by our group, elite Australian footballers (Opar, et al.,
2014) and professional soccer players (Timmins, Bourne, et al., 2015) who displayed
eccentric hamstring weakness during the NHE, were ~4 times more likely to suffer a future
HSI compared to stronger athletes. It is therefore of practical importance to prospectively
explore these relationships in other sports with high incidence rates of HSI so as to reduce the
burden of this troublesome injury. It is also important to further explore the effects of
previous hamstring injury on knee flexor strength.
49
We recently proposed that high rates of HSI recurrence might be partly explained by chronic
neuromuscular inhibition of the BF (Fyfe, et al., 2013; Opar, et al., 2012) which has been
observed during eccentric but not concentric knee flexor efforts (Bourne, et al.,2015; Opar,
Williams, et al., 2013a). These contraction mode-specific deficits in BF activation persist
despite rehabilitation and return to sport and may mediate preferentially eccentric hamstring
weakness (Croisier & Crielaard, 2001; Croisier, et al., 2002; Jonhagen, et al., 1994), reduced
rates of knee flexor torque development (Opar, Williams, Timmins, Dear, & Shield, 2013b),
persistent BFLH atrophy (Silder, et al., 2008), and altered BFLH architecture (Timmins et al.,
2015) – all of which have been observed months to years after an HSI. These activation
deficits that persist throughout rehabilitation would reduce the injured muscle’s loading,
particularly during eccentric contractions at longer muscle lengths (Opar, Williams, et al.,
2013a; Sole, Milosavljevic, Nicholson, & Sullivan, 2011a, 2011b) and this likely
compromises hypertrophy and sarcomerogenesis (Brockett, et al., 2001), both of which are
thought to be important in allowing muscles to adapt to the demands of sprinting and
strengthening exercises. While inhibition of BF muscles appears to be a robust and persistent
phenomenon in previously injured athletes, to date it has only been explored during eccentric
isokinetic tasks (Opar, Williams, et al., 2013a; Sole, et al., 2011a) and the NHE (Bourne, et
al., 2015). It remains to be seen whether activation deficits are also present during the
presumably injurious (Brooks, et al., 2005c; Ekstrand, et al., 2011a; Woods, et al., 2002; Yu,
et al., 2008) terminal-swing phase of high speed running.
With respect to the restoration of neuromuscular function following an HSI, heavy,
progressive intensity resistance training has been shown to improve activation of skeletal
muscle (Aagaard, et al., 2000; Amiridis, et al., 1996; Carolan & Cafarelli, 1992; Deschenes &
Kraemer, 2002; Dudley, Tesch, Miller, & Buchanan, 1991). While no studies have measured
50
voluntary hamstring activation following a period of strength training, interventions aimed at
improving eccentric hamstring strength appear very effective in reducing the incidence of
both first-time and recurrent HSIs (Arnason, et al., 2008; Askling, et al., 2003; Askling,
Tengvar, & Thorstensson, 2013; Croisier, et al., 2008c; Petersen, Thorborg, Nielsen, Budtz-
Jørgensen, & Hölmich, 2011). However, different exercises appear to target different
hamstring muscles and different portions of those muscles and the BF is not always heavily
recruited (Bourne, et al., 2015; Zebis et al., 2012). As BFLH injuries represent up to 80% of
all hamstring strains (Connell et al., 2004; Koulouris, et al., 2007), an improved
understanding of which exercises preferentially activate and stimulate adaptations in the
BFLH, will be paramount in designing interventions aimed at improving eccentric strength
and activation in this muscle.
Objectives
The major questions to be addressed in this program of research include:
1) Are eccentric strength deficits or between-limb imbalances predictive of future
HSI in athletes?
2) Do athletes with a history of HSI display altered patterns of muscle activation
during high-speed overground running?
3) What is the optimal exercise to improve voluntary activation and strength in the
commonly injured biceps femoris long head (BFLH)?
51
4) How does hamstring architecture and morphology adapt to a targeted progressive
intensity resistance training intervention?
53
Chapter 4: STUDY 1 – ECCENTRIC STRENGTH AND HAMSTRING INJURY RISK IN RUGBY UNION: A PROSPECTIVE COHORT STUDY
Publication statement
This chapter is comprised of the following paper published in the American Journal of Sports
Medicine:
Bourne, MN., Opar, DA., Williams, MD., & Shield, AJ. (2015). Eccentric Knee-flexor
Strength and Hamstring Injury Risk in Rugby Union: A prospective study. Am J Sports Med,
43(11):2663-70. doi: 10.1177/0363546515599633.
54
Statement of Contribution of Co-Authors for Thesis by Published Paper
The authors listed below 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;
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 or other publications, and (c) the head of the responsible academic unit
5. They agree to the use of the publication in the student’s thesis and its publication on the Australasian Research Online database consistent with any limitations set by publisher requirements.
Contributor
Statement of contribution*
Matthew Bourne Experimental design, ethical approval, data collection and analysis, statistical analysis, manuscript preparation
08/03/2016 David Opar Aided in experimental design and manuscript preparation
Morgan Williams Assisted with statistical analysis and manuscript preparation Anthony Shield Aided in experimental design and manuscript preparation
Principal Supervisor Confirmation
I have sighted email from all co-authors confirming their certifying authorship.
Dr Anthony Shield ____________________ ______________
55
4.1 ABSTRACT
BACKGROUND: Hamstring strain injuries represent the most common cause of lost
playing time in rugby union. Eccentric knee-flexor weakness and between-limb imbalances in
eccentric knee-flexor strength are associated with a heightened risk of hamstring injury in
other sports; however these variables have not been explored in rugby union. PURPOSE: To
determine if lower levels of eccentric knee-flexor strength or greater between-limb imbalance
in this parameter during the Nordic hamstring exercise are risk-factors for hamstring strain
injury in rugby union. STUDY DESIGN: Cohort study; level of evidence, 3. METHODS:
This prospective study was conducted over the 2014 Super Rugby and Queensland Rugby
Union seasons. In total, 178 rugby union players (age, 22.6 ± 3.8 years; height, 185 ± 6.8 cm;
mass, 96.5 ± 13.1 kg) had their eccentric knee-flexor strength assessed using a custom-made
device during the pre-season. Reports of previous hamstring, quadriceps, groin, calf and
anterior cruciate ligament injury were also obtained. The main outcome measure was
prospective occurrence of hamstring strain injury. RESULTS: Twenty players suffered at
least one hamstring strain during the study period. Players with a history of hamstring strain
injury had 4.1 fold (RR = 4.1, 95% CI = 1.9 to 8.9, p = 0.001) greater risk of subsequent
hamstring injury than players without such history. Between-limb imbalance in eccentric
knee-flexor strength of ≥ 15% and ≥ 20% increased the risk of hamstring strain injury 2.4
fold (RR = 2.4, 95% CI = 1.1 to 5.5, p = 0.033) and 3.4 fold (RR = 3.4, 95% CI = 1.5 to 7.6,
p = 0.003), respectively. Lower eccentric knee flexor strength and other prior injuries were
not associated with increased risk of future hamstring strain. Multivariate logistic regression
revealed that the risk of re-injury was augmented in players with strength imbalances.
CONCLUSION: Previous hamstring strain injury and between-limb imbalance in eccentric
knee-flexor strength were associated with an increased risk of future hamstring strain injury
56
in rugby union. These results support the rationale for reducing imbalance, particularly in
players who have suffered a prior hamstring injury, to mitigate the risk of future injury.
57
4.2 INTRODUCTION
Rugby union is a physically demanding contact game with one of the highest reported
incidences of match injuries of all sports (Brooks, et al., 2005c; Fuller, Sheerin, & Targett,
2013; Williams, Trewartha, Kemp, & Stokes, 2013). The unique nature of the sport exposes
athletes of varying anthropometric characteristics (Zemski, Slater, & Broad, 2015) to frequent
bouts of high-intensity running, kicking, and unprotected collisions, interspersed with periods
of lower intensity aerobic work (Duthie, Pyne, & Hooper, 2003). Hamstring strain injury
represents the most common cause of lost playing and training time at the professional level
(Brooks, et al., 2005a, 2005b) and a significant portion of these injuries re-occur, resulting in
extended periods of convalescence (Brooks, et al., 2006).
Despite the prevalence of HSIs in rugby union (Brooks, et al., 2005a), efforts to identify risk
factors and to optimise injury prevention strategies are limited (Brooks, et al., 2006; Upton,
Noakes, & Juritz, 1996). It is generally agreed that the aetiology of HSI is multifactorial
(Mendiguchia, Alentorn-Geli, & Brughelli, 2012) and injuries result from the interaction of
several modifiable (Burkett, 1970; Croisier, et al., 2002; Croisier, et al., 2008c; Heiser, et al.,
1984; Opar, et al., 2014; Orchard, et al., 1997b; Sugiura, et al., 2008) and non-modifiable
(Arnason, et al., 2004; Gabbe, Bennell, & Finch, 2006; Hagglund, et al., 2006; Verrall, et al.,
2001) risk factors. In rugby union (Brooks, et al., 2006), as well as several other sports
(Askling, et al., 2007; Opar, et al., 2014; Woods, et al., 2004), HSIs most frequently result
from high-speed running which potentially explains why the incidence of HSI is significantly
higher for backline rugby players (Brooks, et al., 2006), who perform longer and more
frequent sprints than forwards. During running, the biarticular hamstrings play a crucial role
in decelerating the forward swinging shank during terminal-swing (Yu, et al., 2008) and in
generating horizontal force upon ground contact (Mann, Moran, & Dougherty, 1986). Given
58
the active lengthening role of the hamstrings it has been proposed that eccentric weakness
(Opar, et al., 2014) or between-limb imbalances in eccentric strength may predispose to HSI,
and both factors have been associated with the risk of HSI in other sports (Croisier, et al.,
2008c; Fousekis, Tsepis, Poulmedis, Athanasopoulos, & Vagenas, 2011; Heiser, et al., 1984;
Yamamoto, 1993). Furthermore, interventions aimed at improving eccentric strength with the
Nordic hamstring exercise reduce the incidence and severity of HSIs in soccer (Arnason, et
al., 2008; Petersen, et al., 2011) while professional rugby union teams employing the exercise
have been reported to suffer fewer HSIs than those which do not (Brooks, et al., 2006). Still,
the role of eccentric strength in HSI occurrence remains a controversial issue with
contradictory results reported in the literature (Bennell, et al., 1998a; Zvijac, Toriscelli,
Merrick, & Kiebzak, 2013) and a recent meta-analysis suggested that isokinetically-derived
measures of strength do not represent a risk factor for HSI (Freckleton & Pizzari, 2013).
Nevertheless, the authors are not aware of any study that has examined the relationship
between eccentric knee-flexor strength, between-limb imbalance, and HSI incidence in rugby
union. Given the unique anthropometric characteristics of rugby union players (Zemski, et al.,
2015) and the diverse physical demands of the game (Duthie, et al., 2003; Williams, et al.,
2013), it may not be appropriate to generalise the findings from other sports to this cohort.
It has been shown that eccentric knee flexor strength can be reliably measured during the
performance of the Nordic hamstring exercise (Opar, Piatkowski, et al., 2013a). In a recent
prospective study of elite Australian footballers (Opar, et al., 2014), players with low Nordic
strength measures in the pre-season training period were significantly more likely to sustain
an HSI in the subsequent competitive season. However, it remains to be seen if the same
measures can identify rugby union players at risk of future HSI.
59
An improved understanding of risk factors for HSI in rugby union represents the first step
(van Mechelen, Hlobil, & Kemper, 1992) towards optimising injury prevention strategies and
reducing the high rates of HSI occurrence in the sport (Brooks, et al., 2005a, 2005b). The aim
of this study was to determine whether pre-season eccentric knee-flexor strength and
between-limb imbalance in strength measured during the Nordic hamstring exercise, were
predictive of future HSI in rugby union players. In addition, given the multifactorial aetiology
of HSI (Mendiguchia, Alentorn-Geli, et al., 2012) and the potential for various risk factors to
interact (Thorborg, 2014), a secondary aim was to determine the association between
measures of eccentric strength, imbalance and other previously identified risk factors, such as
prior HSI (Brooks, et al., 2006; Thorborg, 2014). The a priori hypotheses were that
subsequently injured players would display lower levels of eccentric knee-flexor strength and
greater between-limb imbalances in this measure than players who remained free from HSI.
4.3 METHODS
Participants & study design
This prospective cohort study was approved by the Queensland University of Technology’s
Human Research Ethics Committee and was completed during the 2014 Super 15 and
Queensland Rugby Union (QRU) seasons. In total, 194 male rugby players (age, 22.6 ± 3.8
years; height, 185 ± 6.7 cm; weight, 97 ± 13.1 kg) from three professional Super 15 clubs
(n=75) and two local QRU clubs (n=119) provided written informed consent to participate.
The QRU clubs included players in both sub-elite (n=79) and U’19 premier-grade teams
(n=40). Prior to the commencement of data collection, retrospective injury details were
collected for all players which included their history of hamstring, quadriceps and calf strain
injuries and chronic groin pain within the preceding 12 months as well as history of anterior
cruciate ligament (ACL) injury at any stage in their career. Demographic (age) and
60
anthropometric (height, body mass) data were also collected in addition to player position
(forward, back). For all Super 15 players these data were obtained from team medical staff
and the national Australian Rugby Union registry. All sub-elite players completed a standard
injury history form with their team physiotherapist and injuries were confirmed with
information from each club’s internal medical reporting system. Subsequently, players had
their eccentric knee flexor strength assessed at a single time point within the 2014 pre-season
(Super 15, November 2013; sub-elite, January 2014). At the discretion of team medical staff,
some players (n=16) were excluded from strength testing because they had an injury or
illness at the time of testing that precluded them from performing maximal resistance
exercise
Eccentric knee-flexor strength assessment
The assessment of eccentric knee-flexor strength during the Nordic hamstring exercise has
been reported previously (Opar, Piatkowski, et al., 2013a; Opar, et al., 2014). Participants
knelt on a padded board, with the ankles secured immediately superior to the lateral
malleolus by individual ankle braces which were attached to custom made uniaxial load cells
(Delphi Force Measurement, Gold Coast, Australia) with wireless data acquisition
capabilities (Mantracourt, Devon, UK) (Figure 1). The ankle braces and load cells were
secured to a pivot which allowed the force generated by the knee flexors to always be
measured through the long axis of the load cells. Immediately prior to testing, players were
provided with a demonstration of the Nordic hamstring exercise from investigators and
received the following instructions: gradually lean forward at the slowest possible speed
while maximally resisting this movement with both limbs while keeping the trunk and hips in
a neutral position throughout, and the hands held across the chest (Opar, et al., 2014).
Subsequently, players completed a single warm-up set of three repetitions followed by one
61
set of three maximal repetitions of the bilateral Nordic hamstring exercise. All trials were
closely monitored by investigators to ensure strict adherence to proper technique and players
received verbal encouragement throughout each repetition to encourage maximal effort. A
repetition was deemed acceptable when the force output reached a distinct peak (indicative of
maximal eccentric strength), followed by a rapid decline in force which occurred when the
athlete was no longer able to resist the effects of gravity acting on the segment above the
knee joint. All eccentric strength testing was performed in a rested state, prior to the
commencement of scheduled team training.
Figure 4-1. The Nordic hamstring exercise performed on the testing device (progressing
from right to left). Participants were instructed to lower themselves to the ground as slowly
as possible by performing a forceful eccentric contraction of their knee flexors. Participants
only performed the eccentric portion of the exercise and after ‘catching their fall’, were
instructed to use their arms to push back into the starting position (not shown here). The
ankles are secured independently.
Data analysis
Force data for the left and right limbs were transferred to a personal computer at 100Hz
through a wireless USB base station receiver (Mantracourt, Devon, UK). Eccentric strength,
determined for each leg from the peak force during the best of three repetitions of the NHE,
62
was reported in absolute terms (N) and relative to bodyweight (N.kg-1). For the uninjured
group, between limb imbalance in peak eccentric knee-flexor force was calculated as a
left:right limb ratio and for the injured group, as an uninjured:injured limb ratio. The between
limb imbalance ratio was converted to a percentage difference as per previous work (Opar, et
al., 2014) using log transformed raw data followed by back transformation.
Prospective hamstring strain injury reporting
An HSI was defined as acute pain in the posterior thigh which caused immediate cessation of
training or match play and damage to the hamstring muscle-tendon unit (Opar, et al., 2014)
which was later confirmed with magnetic resonance imaging (for all Super 15 players) or
clinical examination by the team physiotherapist (for all sub-elite and U’19 players). For all
injuries that satisfied the inclusion criteria, team medical staff provided the following details
to investigators: limb injured (left / right), muscle injured (biceps femoris long or short
head/semimembranosus/semitendinosus, injury severity (grade 1-3), injury mechanism (ie,
running, kicking, collision, change of direction), the date of injury and whether it was a
recurrence and the total time taken to resume full training and competition.
Statistical analysis
All statistical analyses were performed using JMP 10.02 (SAS Institute, Inc). Mean and
standard deviations (SD) of age, height, weight, eccentric knee-flexor strength for the left and
right limb and between-limb imbalance (%) in strength were determined. Because the player
and not the leg was the unit of measure in some analyses, it was necessary to have a single
measure of eccentric knee-flexor strength for each athlete and this was determined by
averaging the peak forces from each limb (two-limb-average strength). Univariate analysis
was used to compare age, height, weight and between-limb imbalance between the injured
63
and uninjured groups. Eccentric knee-flexor strength of the injured limb was compared to the
uninjured contralateral limb and to the average of the left and right limbs from the uninjured
control group. In addition, eccentric knee-flexor strength was compared between elite, sub-
elite and U’19 players and between player positions (forwards vs. backs). All univariate
comparisons were made using independent samples t tests with Bonferroni corrections to
control for Type 1 error.
To calculate univariate relative risk (RR) and 95% confidence intervals (95% CI), players
were grouped according to:
whether they did or did not have a history of
o HSI in the previous 12 months
o quadriceps strain injury in the previous 12 months
o chronic groin pain in the previous 12 months
o calf strain injury in the previous 12 months
o or ACL injury at any stage;
Two-limb-average eccentric knee-flexor strength above or below 267.9N or 3.18N.kg-1
(these cut-offs were determined using receiver operator characteristic (ROC) curves
based on the force and relative force values that maximised the difference between
sensitivity and 1 – specificity).
between-limb eccentric strength imbalance above or below a 10, 15 or 20% cut-off;
whether they were above or below the 25th, 50th and 75th percentiles for:
64
o age
o height
o weight
Any variable associated with subsequent HSI according to univariate analysis was entered
into a univariate logistic regression model to determine its predictive value as a risk factor for
future HSI. Furthermore, given the multifactorial nature of HSI, a multivariate logistic
regression model was constructed (using prior HSI and between-limb imbalance) to explore
the potential interaction between risk factors (Opar, et al., 2014) and eliminate any
confounding effects (Orchard, 2001). Alpha was set at p<0.05 and for all univariate analyses
the difference between limbs and groups is reported as mean difference and 95% CI.
4.4 RESULTS
Cohort and prospective hamstring strain injury details
In total, 178 players (age, 22.6 ± 3.8 years; height, 185 ± 6.8 cm; weight, 96.5 ± 13.1 kg) had
their eccentric knee-flexor strength assessed in the pre-season period. Of these, 75 were elite
(age, 24.4 ± 3.1 years; height, 186 ± 7.2 cm; weight, 101 ± 11.3 kg), 65 were sub-elite (age,
21.3 ± 3.7 years; height, 184 ± 6.4 cm; weight, 93 ± 13.4 kg) and 38 were in the U’19
division (age, 18.1 ± 0.8 years; height, 183 ± 6.8 cm; weight, 91 ± 14.9 kg).
Twenty athletes suffered at least one HSI during the 2014 competitive season (age, 22.8 ± 3.2
years; height, 185.6 ± 5.5 cm; weight, 97.4 ± 12.4 kg) and 158 remained free of HSI (age,
22.5 ± 3.8 years; height, 184.9 ± 7.0 cm; weight, 96.4 ± 13.3 kg). No significant differences
were observed in terms of age, height or body mass between the subsequently injured and
uninjured players (p>0.05). Hamstring strains resulted in an average of 21 days (range = 7 to
65
49 days) absence from full training and match play. Forty-five percent were recurrences from
the previous season and 25% of those reported during the observation period recurred. Of the
20 injuries, 80% affected the BF as the primary site of injury and 85% resulted from high-
speed running. The majority of HSIs were sustained by backs (60%) compared to forwards
(40%). No injuries were sustained during the assessment of eccentric knee-flexor strength.
Comparison of strength between playing level and position
Eccentric strength measures for each level of play and player position can be found in Table
4-1. In terms of eccentric strength, there was no significant difference between elite and sub-
elite players (mean difference = 21N, 95% CI = -7.8 to 49.9N, p = 0.154) or between elite
and U’19 players (mean difference = 24.1N, 95% CI = -6.90 to 55.0 N, p = 0.126) however,
sub-elite players were significantly stronger than U’19 players (mean difference 45.1N, 95%
CI = 8.1 to 82.0N, p = 0.017). When expressed relative to bodyweight, both sub-elite (mean
difference = 0.35, 95% CI = 0.08 to 0.63, p = 0.013) and U’19 players (mean difference =
0.38N, 95% CI = 0.07 to 0.70, p = 0.017) were significantly stronger than elite players
although no difference was observed between sub-elite and U’19 players (mean difference = -
0.03, 95% CI = -0.4 to 0.34, p = 0.870). In absolute terms, forward line players were
significantly stronger than backs (mean difference = 35.3N, 95% CI = 10.11 to 60.5N, p=
0.006) however, no difference was observed when strength was normalised to bodyweight
(mean difference = -0.1, 95% CI = -0.35 to 0.16, p = 0.583).
66
Table 4-1. Pre-season Nordic hamstring exercise force variables for each level of competition and player position.
Data is presented as mean ± standard deviation. * Indicates significantly different from the U’19 group; ** indicates significantly different from
both the U’19 and sub-elite groups; # indicates a significant difference between forwards and backs.
Playing
group
n Absolute eccentric knee flexor
strength (N)
Relative eccentric knee flexor
strength (N.kg-1)
Elite
Sub-elite
U’19
75 366.9 ± 76.9 3.65 ± 0.71**
65
38
387.9 ± 96.3*
342.8 ± 81.5
4.00 ± 0.93
4.03 ± 0.92
Forward
Back
82
96
388.5 ± 95.5#
353.1 ± 74.9#
3.81 ± 0.92
3.9 ± 0.80
67
Univariate analysis of factors associated with hamstring strain injury
Eccentric knee-flexor strength and between-limb imbalances for the injured and uninjured
groups can be found in Table 4-2. Limbs that went on to be injured were significantly weaker
in pre-season than uninjured contralateral limbs both in absolute terms (mean difference =
55.1N, 95% CI = 11.65 to 98.5N, p = 0.016) and when normalised to body mass (mean
difference = 0.55 N.kg-1, 95% CI = 0.13 to 0.98N.kg-1, p = 0.013). Players who went on to
sustain an HSI displayed higher levels of between-limb imbalance than those players who
remained free from HSI (mean difference = -7.4%, 95% CI = -12.4 to -2.4%, p = 0.004).
However, there was no difference between the subsequently injured limb and the average of
the left and right limbs from the uninjured group either in absolute strength (mean difference
= -14.9N, 95% CI = -55.5 to 25.6N, p = 0.470) or strength relative to body mass (mean
difference = -0.07 N.kg-1, 95% CI = -0.48 to 0.33 N.kg-1, p = 0.710). No significant
differences were observed in age (mean difference = 0.18yrs, 95% CI = -1.5 to 1.9yrs, p =
0.235), height (mean difference = 0.86cm, 95% CI = -2.3 to 4.1cm, p = 0.457), or weight
(mean difference = 0.97kg, 95% CI = -5.2 to 7.4kg, p = 0.632) between the injured and
uninjured groups.
68
Table 4-2. Pre-season Nordic hamstring exercise force variables for hamstring strain injured and uninjured rugby union players.
Data is presented as mean ± standard deviation. * Indicates significant differences between limbs in the injured group (p<0.05). # Significant
differences between injured and uninjured players.
Group Limb Absolute eccentric knee flexor
strength (N)
Relative eccentric knee flexor
strength (N.kg-1)
Between-limb imbalance (%)
Injured
Injured
(n=20)
355.1 ± 80.5* 3.65 ± 0.67*
Uninjured
(n=20)
410.1 ± 132.4*
4.21 ± 1.14*
17.37 ± 16.1#
Uninjured Average of
left and right
(n=158)
367.7 ± 85.0 3.85 ± 0.87 10.02 ± 9.8#
69
Relative risk
Players with a history of HSI in the previous 12 months had 4.1 (RR = 4.1, 95% CI = 1.9 to
8.9, p = 0.001) times greater risk of suffering a subsequent HSI than players with no HSI in
the same period (Table 4-3). Between-limb imbalance in eccentric knee-flexor strength of ≥
15% increased the risk of HSI 2.4 fold (RR = 2.4, 95% CI = 1.1 to 5.5, p = 0.033) while an
imbalance ≥ 20% increased that risk 3.4 fold (RR = 3.4, 95% CI = 1.5 to 7.6, p = 0.003).
However, players with two-limb-average eccentric knee-flexor strength of less than 267.9N
were not at elevated risk of HSI (RR = 0.17, 0.0 to 2.7, p = 0.204) compared to stronger
players (area under the ROC curve = 0.52; specificity= 0.86; sensitivity = 1.0). Similarly,
having normalised strength values of less than 3.18N.kg-1 did not increase the risk of HSI
(RR = 0.97, 95%CI = 0.3 to 2.7, p = 0.957).
70
Table 4-3. Univariate relative risk of suffering a future hamstring strain injury (HSI) using
eccentric strength and between-limb imbalance, injury history and demographic data as risk
factors.
Risk factor n % from
each group
that
sustained
HSI
Relative risk
(95%CI)
P
Prior injury
HSI 30 30.0 4.1 (1.9 to 8.9) 0.001
No HSI 164 7.3 0.24 (0.1 to 0.5)
ACL 16 12.5 1.17 (0.3 to 4.6) 0.538
No ACL 178 10.7 0.85 (0.2 to 3.3)
Calf strain 7 14.3 1.33 (0.2 to 8.5) 0.56
No calf strain 186 10.8 0.75 (0.1 to 4.8)
Quadriceps strain 10 10.0 0.92 (0.1 to 6.2) 0.691
No quadriceps strain 184 10.9 1.09 (0.2 to 7.3)
Chronic groin pain 12 8.3 0.76 (0.1 to 5.2) 0.758
No chronic groin pain 182 11.0 1.32 (0.2 to 9.0)
Pre-season eccentric hamstring
strength
<267.9N 22 0 0.17 (0.01 to 2.7) 0.204
≥267.9N 156 12.8 6.0 (0.4 to 96.0)
<3.18N.kg-1 36 11.1 0.97 (0.3 to 2.7) 0.957
≥3.18N.kg-1 140 11.4 1.03 (0.4 to 2.9)
Pre-season between-limb imbalance
<10% 113 9.7 0.70 (0.3 to 1.6) 0.403
≥10% 65 13.8 1.42 (0.6 to 3.3)
<15% 133 8.3 0.41 (0.2 to 0.9) 0.033
≥15% 45 20.0 2.42 (1.1 to 5.5)
<20% 149 8.1 0.29 (0.1 to 0.7) 0.003
≥20% 29 27.6 3.43 (1.5 to 7.6)
71
Age (years)
≤19 48 6.2 0.60 (0.2 to 2.0) 0.397
>19 146 11.6 1.67 (0.5 to 5.5)
≤22 95 10.2 1.04 (0.4 to 2.2) 0.922
>22 99 10.1 0.96 (0.5 to 2.5)
≤25 149 10.7 1.2 (0.4 to 3.4) 0.723
>25 45 8.9 0.83 (0.3 to 2.4)
Height (cm)
≤180 57 7.0 0.56 (0.2 to 1.6) 0.273
>180 135 12.6 1.79 (0.6 to 5.1)
≤185 113 9.7 0.77 (0.3 to 1.7) 0.523
>185 79 12.7 1.3 (0.6 to 2.9)
≤189 148 10.1 0.74 (0.3 to 1.8) 0.511
>189 44 13.6 1.3 (0.5 to 3.3)
Weight (kg)
≤87 48 6.3 0.5 (0.15 to 1.6) 0.249
>87 144 12.5 2.0 (0.6 to 6.5)
≤96.45 95 10.5 1.0 (0.5 to 2.2) 0.979
>96.45 97 11.3 0.99 (0.5 to 2.2)
≤105.25 143 11.2 1.10 (0.4 to 2.8) 0.849
>105.25 49 10.2 0.91 (0.4 to 2.4)
* Indicates a significant difference (p<0.05) in the relative risk of future HSI between
groups. 95%CI, 95% confidence interval; HSI, hamstring strain injury; ACL, anterior
cruciate ligament; N, newtons; cm, centimetre; kg, kilograms.
Logistic regression
Players with a history of HSI in the previous 12 months were, according to the odds ratio, 5.3
times more likely (OR = 5.3, 95%CI = 1.84 to 15.0, p = 0.003) to suffer a subsequent HSI
than players who had remained injury free in that time. In addition, a relationship was
observed between the magnitude of between-limb imbalance in eccentric knee-flexor strength
72
and the risk of subsequent HSI; where, for every 10% increase in between-limb imbalance,
the odds of HSI increased by a factor of 1.34 (95%CI = 1.03 to 1.75, p = 0.028) (Figure 4-2).
Multivariate logistic regression revealed a significant (p < 0.001) relationship between both
prior HSI and between-limb imbalance and the risk of subsequent HSI (Table 4-4), however,
no interaction effect was observed between these variables. This model suggests that for
players with a history of HSI, the risk of re-injury is amplified when they also have between-
limb imbalances in eccentric knee flexor strength (Figure 4-2).
Figure 4-2. The relationship between eccentric knee flexor strength imbalances and
probability of future hamstring strain injury (HSI) for players with and without a history of
HSI in the previous 12 months. Errors bars depict 95% confidence intervals.
73
Table 4-4. Multivariate logistic regression model using prior hamstring strain injury (HSI) and between-limb imbalance in eccentric knee flexor
strength as input variables
AUC, area under the curve
ChiSquare p AUC Sensitivity 1-Specificity
Whole Model 16.00 <0.001 0.69 0.6 0.21
Prior HSI 9.33 0.002
Between-limb imbalance (%) 4.71 0.030
75
4.5 DISCUSSION
The aim of this study was to determine if rugby union players with lower levels of eccentric
strength or larger between-limb imbalances in this measure, as determined during the Nordic
hamstring exercise, were at increased risk of HSI. Higher levels of between-limb imbalance
were found to significantly increase the risk of subsequent HSI and this was amplified in
athletes who had suffered the same injury in the previous 12 months. However, while the
limbs that went on to be injured were significantly weaker than the uninjured contralateral
limbs in pre-season testing, weaker players were no more likely to suffer injury than stronger
players when strength was determined by averaging the peak eccentric forces from left and
right limbs.
The observation that higher levels of between-limb strength imbalance increase an athlete’s
risk of HSI is consistent with previous reports (Croisier, et al., 2008; Fousekis, et al., 2011;
Heiser, et al., 1984; Orchard, et al., 1997b; Yamamoto, 1993). Croisier and colleagues (2008)
reported that professional soccer players with isokinetically-derived knee-flexor strength
imbalances in pre-season had a 4.66 fold greater risk of subsequent HSI than athletes without
such imbalances. More recently, Fousekis and colleagues found that elite soccer players with
imbalances in eccentric knee-flexor strength ≥ 15% in the pre-season had a significantly
greater (OR = 3.88) risk of HSI than athletes with no asymmetry (Fousekis, et al., 2011).
Still, contradictory results have been reported in Australian footballers (Bennell, et al., 1998a;
Opar, et al., 2014) and it remains unclear as to the exact mechanism(s) by which significant
imbalances increase the risk of HSI. It is plausible that between-limb imbalances in eccentric
knee-flexor strength may alter running biomechanics (Chumanov, et al., 2007) or reduce the
capacity of the weaker limb to decelerate the forward swinging shank during terminal-swing
76
(Opar, et al., 2012). However, it should also be noted that the assessment of between-limb
imbalance in the current study was performed during a bilateral Nordic hamstring exercise,
whereas typical assessments involve maximal unilateral contractions performed on an
isokinetic dynamometer (Bennell, et al., 1998a; Fousekis, et al., 2011). For this reason, direct
comparisons to previous work should be made with caution. A bilateral Nordic hamstring
exercise was employed in the current study as previous work has shown that this is more a
more reliable test of eccentric knee-flexor strength than unilateral Nordics (Opar, Piatkowski,
et al., 2013a).
The finding that weaker players were no more likely to sustain an HSI than stronger players
is in line with a recent systematic review and meta-analysis which suggested that
isokinetically-derived measures of strength were not a risk factor for HSI in sport (Freckleton
& Pizzari, 2013). However, the results of the current study differ from a recent investigation
(Opar, et al., 2014) using the Nordic hamstring test which reported that elite Australian
footballer’s with eccentric strength < 256N at the start of preseason and < 279N at the end of
preseason had a 2.7 and 4.3 fold greater risk of HSI, respectively. The disparity between
studies might reflect the vastly different anthropometric characteristics of rugby union
(Zemski, et al., 2015) and Australian football players (Bilsborough et al., 2014), or the unique
physical demands of each sport (Duthie, et al., 2003; Seward, & Orchard, 2013). However, it
is also important to consider that the rugby players in the current study were substantially
stronger than the Australian footballer’s studied previously (Opar, et al., 2014). It is possible
that the protective benefits conferred by greater levels of eccentric strength may plateau at
higher ends of the strength spectrum as they appear to in Australian footballer’s (see Figures
1 & 2 in Opar et al.) (Opar, et al., 2014). It should also be acknowledged that while some
studies have found an association between low levels of knee-flexor strength and subsequent
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HSI (Heiser, et al., 1984; Opar, et al., 2014; Yamamoto, 1993), prior injury is also associated
with knee-flexor weakness (Croisier, et al., 2002; Opar, Piatkowski, et al., 2013a; Opar,
Williams, et al., 2013a; Timmins, Shield, et al., 2014), and this may confound results
(Orchard, 2001).
The current study supports prior HSI as a risk factor for re-injury which is consistent with
earlier observations in rugby union (Brooks, et al., 2006; Upton, et al., 1996) Australian
football (Bennell, et al., 1998a; Freckleton, Cook, & Pizzari, 2014; Orchard, et al., 1997b;
Warren, Gabbe, Schneider-Kolsky, & Bennell, 2010) and soccer (Arnason, et al., 2004).
While the mechanism(s) explaining why prior HSI augments the risk of re-injury remain(s)
unclear, this study revealed a significant relationship between prior HSI and between-limb
imbalance in eccentric knee-flexor strength. This novel finding suggests that rugby union
players with a history of HSI have a significantly greater risk of re-injury if they return to
training and match play with one limb weaker than the other (Figure 4-2). For example, an
athlete with a prior HSI and a 30% between-limb imbalance in eccentric strength is twice as
likely to suffer a recurrence as a previously injured athlete with no imbalance. In light of this
interaction, there is a growing body of evidence to suggest that between-limb imbalance in
knee-flexor strength (Croisier, et al., 2002; Croisier, et al., 2008c; Jonhagen, et al., 1994;
Orchard, et al., 1997b) is a risk-factor for HSI recurrence. These data highlight the
multifactorial nature of HSIs and suggest that the amelioration of between-limb imbalances in
eccentric knee-flexor strength should be a focus of rehabilitative strategies following HSI.
There are some limitations that should be acknowledged in the current study. Firstly, the
assessment of eccentric knee-flexor strength and between-limb imbalance was only
performed at a single time point in the pre-season period. While this is consistent with other
prospective studies exploring the impact of strength variables on HSI risk (Croisier,
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Ganteaume, Binet, Genty, & Ferret, 2008a; Fousekis, et al., 2011; Heiser, et al., 1984;
Orchard, et al., 1997b; Yamamoto, 1993), it is important to consider that strength may change
over the pre-season and in-season periods (Opar, et al., 2014). The assessment of strength at
multiple time points may provide a more robust measure of player risk however, the
geographic diversity of the Super 15 competition precluded follow-up assessments by the
investigators. Eccentric strength was measured as a force output (N) rather than a joint torque
(Nm) which makes direct comparison to isokinetically-derived measures difficult. Further,
this mode of testing does not allow for an assessment of the angle at which the knee flexors
produce maximum torque (Brockett, et al., 2004), and did not permit force to be expressed
relative to quadriceps (Croisier, et al., 2008c) or hip flexor (Yeung, et al., 2009) strength,
which may provide additional information on an athlete’s risk of HSI. The lack of player
exposure data also prevents HSI rates being expressed relative to the amount of training and
match-play that athletes were undertaking. Future work should seek to clarify the effect of
total exposure time (particularly to high-speed running) on the incidence of HSI in rugby
union players (Brooks, et al., 2006). Finally, it should be acknowledged that the area under
the curve (AUC) for the multivariate logistic regression model was 0.69 and while it
displayed a moderate to high ability to identify those athletes at risk of HSI (sensitivity =
0.6), the specificity (0.2) of the model was low and this should be considered when
interpreting the current data.
In conclusion, this study suggests that both between-limb imbalances in eccentric knee-flexor
strength and prior HSI are associated with an increased risk of future HSI in rugby union.
However, lower levels of eccentric knee-flexor strength and a recent history of other lower
limb injuries do not significantly increase the risk of future HSI in this cohort. This study,
along with previous findings (Opar, et al., 2014), highlights the multifactorial nature of HSI
79
and supports the rationale for reducing imbalance, particularly in players who have suffered a
prior injury within the previous 12 months.
81
Chapter 5: STUDY 2 – REDUCED ACTIVATION OF PREVIOUSLY INJURED BICEPS FEMORIS LONG HEAD MUSCLES IN RUNNING
Publication statement
This chapter is comprised of the following paper which was submitted for review at Medicine
and Science in Sports and Exercise:
Bourne, MN., Opar, DA., Williams, MD., Al Najjar, A., Kerr, G., & Shield, AJ. (2015).
Reduced activation of previously injured biceps femoris long head muscles in running. Med
Sci Sports Ex, Submitted.
82
Statement of Contribution of Co-Authors for Thesis by Published Paper
The authors listed below 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;
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 or other publications, and (c) the head of the responsible academic unit
5. They agree to the use of the publication in the student’s thesis and its publication on the Australasian Research Online database consistent with any limitations set by publisher requirements.
Contributor
Statement of contribution*
Matthew Bourne Experimental design, ethical approval, data collection and analysis, statistical analysis, manuscript preparation
08/03/2016 David Opar Aided in experimental design and manuscript preparation
Aiman Al Najjar Aided in data collectionMorgan Williams Assisted with statistical analysis and manuscript preparation
Graham Kerr Assisted with manuscript preparation Anthony Shield Aided in experimental design and manuscript preparation
Principal Supervisor Confirmation
I have sighted email from all co-authors confirming their certifying authorship.
Dr Anthony Shield ____________________ ______________
83
5.1 LINKING PARAGRAPH
The study in Chapter 4 demonstrated that athletes with between-limb imbalances in eccentric
knee flexor strength, and those with a history of HSI, are at a significantly elevated risk of
future HSI. Moreover, for those athletes who have been injured previously, the risk of re-
injury is amplified when they return to sport with between-limb strength imbalances. This
study highlighted the multifactorial nature of HSI and supports the rationale for reducing
strength imbalances, particularly in those players who have a history of injury. However, the
mechanism(s) underpinning these strength imbalances are poorly understood. Using fMRI,
we have recently found that previously injured hamstring muscles are activated less
completely than uninjured contralateral muscles during the Nordic hamstring exercise
(Bourne, et al, 2015). However, it remains to be seen if these deficits also exist during the
presumably injurious task of high-speed overground running.
84
5.2 ABSTRACT
PURPOSE: It is unknown whether elite athletes with a history of strain injury display altered
patterns of hamstring muscle activation during maximal speed sprinting, or reduced muscle
size. The goals of this study were to determine: 1) the spatial patterns of hamstring muscle
activation during high-speed overground running in limbs with and without a prior hamstring
strain injury and; 2) whether previously injured hamstring muscles exhibit lasting deficits in
cross-sectional area (CSA). METHODS: Ten elite male athletes with a history of unilateral
biceps femoris long head (BFLH) strain injury underwent functional magnetic resonance
imaging before and immediately after a repeat-sprint running protocol. Transverse relaxation
times of the BFLH and short head, semitendinosus, and semimembranosus were measured
before and immediately after exercise and CSA was measured at rest. RESULTS: Previously
injured BFLH muscles displayed a significantly lower percentage increase in transverse
relaxation time after the running protocol than uninjured contralateral BFLH muscles (mean
difference = 12.0%, p < 0.001). In the uninjured control limb the biceps femoris short head
was significantly less active than the BFLH (mean difference = 18.1%, p < 0.001) and the
semitendinosus (mean difference = 18.1%, p < 0.001). No participant reported any pain in the
posterior thigh before or after exercise. No between-limb differences in CSA were observed
for any hamstring muscles. CONCLUSION: Elite athletes with a prior strain injury to the
BFLH display altered patterns of muscle activation in their previously injured limbs during
maximal speed overground running; these differences exist in the absence of pain and
atrophy and despite a full return to pre-injury levels of training and competition.
85
5.3 INTRODUCTION
Hamstring strains are endemic in sports that involve high-speed overground running and
represent the most common injury in track and field (Opar, Drezner, et al., 2013), Australian
rules football (Orchard, et al., 2013) and soccer (Ekstrand, et al., 2011b) and the most
prevalent non-contact injury in rugby union (Brooks, et al., 2006). High rates of recurrence
are arguably the most concerning aspect of these injuries, particularly given the tendency for
recurrences to result in more time-loss than the initial insult (Koulouris, et al., 2007).
Hamstring strain injury is commonly suffered when athletes run at maximal speeds (Askling,
et al., 2007) and ~80% of these injuries effect the BFLH (Connell et al., 2004; Koulouris, et
al., 2007). Studies employing surface electromyography (sEMG) suggest that the hamstrings
are most active (Thelen, Chumanov, Hoerth, et al., 2005) during the ostensibly injurious
(Schache, et al., 2009; Thelen, Chumanov, Hoerth, et al., 2005) late-swing, where they
actively lengthen to decelerate the forward swinging shank. However, while these studies
have provided important insight into the temporal patterns of hamstring muscle use during
high-speed running, the contribution of individual hamstring muscles is not well understood.
Further, it remains unclear as to whether the spatial patterns of muscle activation are altered
following an HSI.
Fyfe and colleagues (Fyfe, et al., 2013b) have proposed that high rates of HSI recurrence
might be partly explained by chronic neuromuscular inhibition of the previously injured
muscle. In support of this, reduced sEMG activity has been observed in previously injured BF
muscles during maximal (Opar, Williams, et al., 2013a) and rapid (Opar, Williams, et al.,
2013b) eccentric isokinetic knee flexor contractions. Further, previously injured hamstring
muscles were found to be significantly less active than uninjured contralateral muscles during
86
the performance of the bilateral eccentric Nordic hamstring exercise (Bourne, et al, 2015). It
is plausible that activation deficits, that persist long after rehabilitation and the return to
training and competition, might mediate preferential eccentric knee flexor weakness
(Croisier, et al., 2008c; Lee, et al., 2009), reduced rates of eccentric knee flexor torque
development (Opar, Williams, et al., 2013b), lasting BFLH atrophy (Silder, et al., 2008) and a
chronic shortening of BFLH fascicles (Timmins, Shield, et al., 2014), all of which have been
reported for previously injured hamstring muscles. However, these activation deficits have
only been noted during single joint exercises that do not replicate the high-velocity and multi-
joint demands of high-speed overground running.
An improved understanding of the spatial patterns of hamstring muscle activation during
high-speed running, particularly in previously injured limbs, will be important in optimising
rehabilitation programs and may have implications for understanding the mechanisms of
running-induced HSI. Functional magnetic resonance imaging (fMRI) is a validated (Adams,
Duvoisin, & Dudley, 1992; Cagnie et al., 2011; Fleckenstein, Canby, Parkey, & Peshock,
1988) and highly reliable (Cagnie et al., 2008; Cagnie, et al., 2011) measure of skeletal
muscle activation during exercise that allows for a concurrent assessment of muscle
morphology. The premise of using fMRI to assess muscle activation is based on signal
intensity changes in fMR images resulting from a transient increase in the transverse (T2)
relaxation time of muscle water following exercise (Cagnie, et al., 2011). These T2 shifts
increase proportionately to exercise intensity (Fleckenstein, et al., 1988) and are consistent
with electromyographical measures of muscle activity (Adams, et al., 1992; Cagnie, et al.,
2011). However, the unique ability of fMRI to non-invasively assess deep muscles at
multiple sites within a single scan overcomes several spatial limitations associated with EMG
(Adams et al., 1992). As such, fMRI has become a popular tool for the assessment of muscle
87
use during exercise (Bourne, et al, 2015; Cagnie, et al., 2008; Mendiguchia et al., 2012; Ono,
et al., 2011; Schuermans, Van Tiggelen, Danneels, & Witvrouw, 2014; Sloniger, Cureton,
Prior, & Evans, 1997) with great potential to demonstrate aberrant activation patterns
following injury (Bourne, et al, 2015; Patten, Meyer, & Fleckenstein, 2003).
This study employed fMRI on elite athletes with a history of unilateral HSI to the BFLH who
had since undergone apparently successful rehabilitation and returned to their pre-injury level
of competition. The primary purpose of this investigation was to determine the spatial
patterns of hamstring muscle activation during high-speed overground running in limbs with
and without a history of HSI. A secondary aim was to determine whether previously injured
hamstrings exhibit chronic alterations in muscle morphology. We hypothesised that the
hamstrings of uninjured limbs would be activated non-uniformly during high-speed running
and that previously injured muscles would show reduced activation, and reduced cross-
sectional area (CSA), relative to uninjured contralateral muscles.
5.4 METHODS
Experimental Design
This observational study employed a cross-sectional design in which all participants
completed a single testing session. Prior to testing, participants provided a detailed injury
history to investigators with reference to imaging findings and clinical notations from the
practitioner who diagnosed and treated their most recent HSI. Subsequently, participants
underwent an fMRI scan of their thighs before and immediately after a repeat-sprint running
protocol. Participants were asked to rate their level of perceived pain in the posterior thigh
before and after running using a visual analogue scale (VAS).
88
Participants
Ten elite male athletes (age, 23.2 ± 5.3 years; height, 184.9 ± 4.2 cm; weight, 82.2 ± 5.4 kg)
currently competing in a running based sport and who had suffered a unilateral grade II strain
injury to the BFLH within the previous 12 months (mean time of 8.7 ± 3.2 months since the
last insult) were recruited (Table 5-1). A sample size of 10 was deemed sufficient to detect an
effect size of 1.0 in T2 relaxation time and CSA between muscles and limbs, at a power of
0.80 and with p<0.05 (Bourne, et al, 2015). All athletes had returned to their pre-injury levels
of training and competition (involved in 18 ± 4 hours of structured training per week) with
eight participants competing at a national to international level in track and field, one
competing at a state level in rugby union (backline) and one at a state level in soccer at the
time of testing. Participants completed an injury history questionnaire with reference to
clinical notes provided by their physical therapist. All had their diagnosis confirmed with
MRI (n=8) or ultrasound (n=2) at the time of injury and had subsequently completed a
standard progressive intensity rehabilitation program (Heiderscheit, et al., 2010) under the
guidance of their physical therapist. Participants were free of orthopaedic abnormalities of the
lower limbs, had no history of neurological or motor disorders and had no other soft tissue
injuries to the thighs at the time of testing. All completed a cardiovascular risk factor
questionnaire (Appendix B) to ensure it was safe for them to perform intense exercise and a
standardised MRI screening questionnaire (Appendix C) provided by the imaging facility to
make certain that it was safe for them to enter the magnetic field. All athletes provided
written informed consent to participate in this study, which was approved by the Queensland
University of Technology Human Research Ethics Committee and the University of
Queensland Medical Research Ethics Committee.
89
Table 5-1. Hamstring strain injury details for all participants (n=10)
Participant Muscle
injured
Dominant
limb injured
Severity of
last injury
(grade 1-3)
Months
since last
injury
Rehabilitation
period
(weeks)
1 BFLH Yes 2 9 10
2 BFLH No 2 12 8
3 BFLH No 2 4 10
4 BFLH Yes 2 12 6
5 BFLH No 2 7 8
6 BFLH Yes 2 4 4
7 BFLH No 2 8 8
8 BFLH No 2 12 10
9 BFLH Yes 2 7 10
10 BFLH Yes 2 12 8
Rehabilitation was defined by a return to pre-injury levels of training and competition. BFLH,
biceps femoris long head.
Experimental Session
Repeat-sprint running protocol
Participants completed three sets of six maximal intensity 40m sprints (with an additional
10m acceleration and 15m deceleration distance) on a flat grass sports field adjacent to the
imaging facility. Participants were provided with 30s of rest between sprints and one minute
rest between sets. Investigators verbally encouraged maximal effort throughout each interval.
Participants ran towards the entrance of the imaging facility on the final repetition of the
90
running protocol and were returned to the scanner immediately (<30s) following the cessation
of exercise. Localiser adjustments began within 98 ± 8s (mean ± SD) and post-exercise T2-
weighted imaging began within 2min of exercise.
Functional magnetic resonance imaging
All fMRI scans were performed using a Siemens 3-Tesla (3T) TrioTim imaging system with
a spinal coil. The participant was positioned supine in the magnet bore with their knees fully
extended and hips in neutral and straps were positioned around both limbs to prevent any
undesired movement. Consecutive T2- and contiguous T1-weighted transaxial MR images
were taken of both limbs beginning at the level of the iliac crest and finishing distal to the
tibial plateau. All images were collected using a 180 x 256 image matrix and a 400 x
281.3mm field of view. T2-weighted images were used to assess the extent of hamstring
activation during exercise and were acquired pre- and immediately post-exercise using a Car-
Purcel-Meiboom-Gill (CPMG) spin-echo pulse sequence (transverse relaxation time =
2000ms; echo time = 10, 20, 30, 40, 50 and 60ms; number of excitations = 1; slice thickness
= 10mm; interslice gap = 10mm) (Bourne, et al, 2015). T1-weighted spin-echo images were
acquired only during the pre-exercise scan (transverse relaxation time = 1180ms; echo time =
12ms; field of view = 400 x 281.3 mm; number of excitations = 1; slice thickness = 10mm;
interslice gap = 0mm); these images have substantially greater contrast than T2-weighted
images and were used to accurately assess muscle CSA. The total acquisition time for pre-
exercise images was 15 minutes and 10s and for post-exercise images, 10 minutes.
To minimise any inhomogeneity in MR images caused by dielectric resonances at 3T, a B1
filter was applied to all scans (de Sousa, Vignaud, Fleury, & Carlier, 2011); this is a post-
processing image filter that improves the image signal intensity profile without affecting the
91
image contrast. In addition, participants were asked to avoid strength training of the lower
limbs for 72 hours prior to scanning as muscle damage may augment resting T2 values.
Lastly, to reduce the effects of intramuscular fluid shifts before the pre-exercise scans,
participants were seated for a minimum of 15 minutes before data acquisition (Bourne, et al,
2015).
Visual analogue scale
Before and immediately following the cessation of the repeat-sprint running protocol,
participants were asked to rate their level of pain and discomfort in the posterior thigh (if any)
on a VAS. Participants were instructed to choose a number between 0 (no pain) and 10
(unbearable pain).
Data analysis
All fMR images were transferred to a personal computer in the DICOM file format and
image analysis software (Sante Dicom Viewer and Editor, Cornell University) was used for
subsequent analysis. The analysis of T2 relaxation time and muscle CSA was performed on
each hamstring muscle (BFLH, BFSH, ST and SM) for both the previously injured and
uninjured contralateral limbs in 10mm thick slices corresponding to 30, 40, 50, 60 and 70%
of the distance between the inferior margin of the ischial tuberosity (0%) and the superior
border of the tibial plateau (100%) (Ono, et al., 2011). The T2 relaxation times of each
hamstring muscle were measured in T2-weighted images acquired before and after exercise
to evaluate the degree of muscle activation during the repeat-sprint running protocol. At each
slice, the signal intensities of the BFLH, BFSH, ST and SM were measured in both limbs using
10mm2 rectangular regions of interest (ROI) (Mendiguchia, Garrues, et al., 2012) in each
muscle (total of eight ROIs in each slice). Each ROI was placed in a homogenous region of
92
muscle tissue, with great care taken to avoid aponeurosis, tendon, bone and blood vessels and
was selected at the same coordinates within each muscle for the pre- and post-exercise scans.
An ROI approach was deemed most appropriate as this method allowed investigators to avoid
any areas of residual scar tissue associated with prior HSI (Silder, et al., 2008). The signal
intensity reflected the mean value of all pixels within the ROI and was determined for each
ROI across six echo times (10, 20, 30, 40, 50 and 60ms). T2 relaxation time for each ROI
was then calculated by fitting signal intensity values at each echo time to a mono-exponential
decay model using a least squares algorithm:
[(SI= M exp(echo time / T2) (Bourne, et al, 2015; Ono, et al., 2011)
where SI is the signal intensity at a specific echo time, and M represents the pre-exercise
fMRI signal intensity. To assess the degree of muscle activation during exercise, the mean
percentage change in T2 for each ROI was calculated as:
[(mean post-exercise T2 / mean pre-exercise T2) x 100].
To provide a meaningful measure of whole-muscle activation, the percentage change in T2
relaxation time for each hamstring muscle was evaluated using the average value of all ROIs
(at all five thigh levels). Previous studies have demonstrated excellent intertester reliability of
T2 relaxation time measures with intra-class correlation coefficients ranging from 0.87 to
0.94 (Cagnie, et al., 2008; Cagnie, et al., 2011).
Muscle CSAs obtained from pre-exercise T1-weighted images were analysed to examine
differences in hamstring muscle morphology in limbs with and without a history of strain
injury to the BFLH. The muscle boundaries of BFLH, BFSH, ST and SM were traced manually
on each limb (at slices 30, 40, 50, 60 and 70% of thigh length)(24) and CSA was calculated
as the total cm2 within each trace. For each muscle, the average CSA of all slices in the
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previously injured limb was compared with that of the uninjured contralateral limb to
evaluate between-limb differences following injury.
Statistical Analysis
All statistical analyses were performed using JMP version 10.02 (SAS Institute Inc, 2012). A
repeated measures design linear mixed model fitted with the restricted maximum likelihood
(REML) method was used to compare transient exercise-induced percentage changes in T2
relaxation times and resting values of CSA for each muscle in the previously injured and
uninjured contralateral limbs. Muscle (BFLH, BFSH, ST or SM), limb (injured/uninjured) and
muscle by limb interaction were the fixed factors with participant identity (ID), participant ID
by muscle and participant ID by limb as the random factors. When the muscle by limb
interaction was significant (p<0.05) for the percentage change in T2 relaxation time or for
CSA, post-hoc t-tests with Bonferroni corrections were used to report the mean difference
between limbs for each muscle with 95% confidence intervals (95%CI). To determine the
spatial activation patterns of healthy uninjured hamstrings, the percentage change in T2
relaxation time was compared between each hamstring muscle in the uninjured limb. Again,
when a significant main effect was detected, post hoc t tests with Bonferroni corrections were
used to report the mean difference (and 95% CI) between muscles. The adjusted alpha level
for all post hoc t tests was set at p < 0.005.
To assess the potential impact of acute posterior thigh pain on between-limb differences in
muscle activation, VAS scores obtained from participants before and after the repeat-sprint
running protocol were reported descriptively as means ± SD. Finally, given the potential for
muscle activation to improve over time, the magnitude of between-limb differences in T2
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relaxation time were correlated with the time since injury and duration of the rehabilitation
period using the coefficient of determination.
5.5 RESULTS
Comparison of muscle activation between previously injured and uninjured
contralateral limbs
The between-limb analysis of muscle activation revealed a significant muscle by limb
interaction (p < 0.001). Previously injured BFLH muscles displayed a smaller running-induced
percentage increase in T2 relaxation time (Figure 5-1 & 5-2A) than the homonymous muscles
in the uninjured contralateral limb (mean difference = 12.0%, 95% CI = 2.4 to 21.6%, p <
0.001). In contrast, there were no significant differences in the percentage change in T2
relaxation times for ST (mean difference = 7.4%, 95% CI = -2.2% to 17.0%, p = 0.022), BFSH
(mean difference = 2.9%, 95% CI = -6.7 to 12.5%, p = 0.334) or SM (mean difference = -
2.6%, 95% CI = -12.5 to 7.3%, p = 0.396) muscles in injured and uninjured limbs (Figure 5-
1).
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Figure 5-1. Mean percentage change in fMRI T2 relaxation times after running for each
hamstring muscle in previously injured (Inj) and uninjured (Uninj) limbs. * indicates a
significant between limb difference for individual muscles (p<0.005). Error bars depict 95%
CIs. BFLH, biceps femoris long head; BFSH, biceps femoris short head; ST, semitendinosus;
SM, semimembranosus.
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Figure 5-2. A. Parametric map of transverse (T2) relaxation times for the previously injured
and uninjured contralateral limbs of a single participant, acquired immediately following the
high-speed running protocol. Colour spectrum illustrates the absolute T2 value in
milliseconds (ms). Note the divergence between the previously injured and uninjured
contralateral limbs. 2B. Typical T1-weighted image at 50% of thigh length (transverse
relaxation time = 1180ms; echo time = 12ms; slice thickness = 10mm), depicting the regions
of interest for each hamstring muscle. For both A & B, the right side of the image
corresponds to the participant’s left side as per radiology convention. BFLH, biceps femoris
long head; BFSH, biceps femoris short head; ST, semitendinosus; SM, semimembranosus.
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Comparison of muscle cross-sectional area between previously injured and uninjured
contralateral limbs
For muscle CSA, the interaction of muscle by limb was not significant (p = 0.345) when
comparing homonymous muscles in uninjured and previously injured limbs. There were no
significant between-limb differences in CSAs of homonymous muscles (BFLH mean
difference = -0.7 cm2, 95% CI = -2.6 to 1.2 cm2, p = 0.248; BFSH mean difference = -0.3 cm2,
95% CI = -2.1 to 1.50 cm2, p = 0.589); ST mean difference = -0.6 cm2, 95% CI = -2.5 to 1.3
cm2, p = 0.303); SM mean difference = -0.6 cm2, 95% CI = -2.4 to 1.2 cm2, p = 0.293)
(Figure 5-3).
Figure 5-3. Mean CSAs (cm2) of each hamstring muscle for both the previously injured (Inj)
and uninjured (Uninj) contralateral limbs (BFLH, biceps femoris long head; BFSH, biceps
femoris short head; ST, semitendinosus; SM, semimembranosus). Error bars depict 95% CIs.
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Spatial activation patterns of the uninjured limb
For the analysis of muscle activation in the uninjured limb, there was a significant main effect
for muscle (p<0.001) (Figure 5-4). Post-hoc t-tests revealed that BFSH was significantly less
active than BFLH (mean difference = 18.1%, 95% CI = 3.3 to 32.9%, p < 0.001) and ST
(mean difference = 18.1%, 95% CI = 3.3 to 32.9%, p < 0.001). No significant differences in
the percentage change in T2 relaxation time were observed for BFSH vs. SM (mean difference
= 9.8%, 95% CI = -5.0 to 24.6%, p = 0.048), SM vs. BFLH (mean difference = 8.3%, 95% CI
= -6.5 to 23.1%, p = 0.090), SM vs. ST (mean difference = 8.3%, 95% CI = -6.5 to 23.1%, p
= 0.090), or ST vs. BFLH (mean difference = 0.0%, 95% CI = -9.7 to 9.7% p = 0.999).
Figure 5-4. Percentage change in fMRI T2 relaxation times of each hamstring muscle in the
uninjured limb. Values are expressed as a mean percentage change compared to the values
at rest. * indicates significantly different from BFSH (p<0.005). Error bars depict 95% CIs.
BFLH, biceps femoris long head; BFSH, biceps femoris short head; ST, semitendinosus; SM,
semimembranosus.
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Pain and discomfort
No participant reported any pain in the posterior thigh before or immediately following the
repeat-sprint running protocol (mean VAS scores pre- and post-exercise = 0.0 ± 0).
Time elapsed since injury and injury severity There was no relationship between the time elapsed since injury and the magnitude of
between-limb differences in the percentage change in T2 relaxation time for BFLH (R2 =
0.001) or ST (R2 = 0.02). Furthermore, there was no correlation between the duration of
rehabilitation and the extent of between-limb differences in T2 change for BFLH (R2 = 0.05)
or ST (R2 = 0.002).
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5.6 DISCUSSION
This study is the first to use fMRI to map the spatial activation patterns of hamstring muscles
during high-speed overground running in a homogenous group of highly trained athletes. The
results suggest that healthy uninjured hamstrings were activated somewhat uniformly during
sprinting, with the exception of BFSH. However, previously injured BFLH muscles were
activated ~50% less than homonymous contralateral muscles with no history of injury. These
differences were present after rehabilitation, the return to pre-injury levels of training and
competition and in the absence of pain.
Evidence for altered activation patterns in previously injured hamstring muscles is in line
with previous findings (Bourne, et al, 2015; Daly, McCarthy Persson, Twycross-Lewis,
Woledge, & Morrissey, 2015; Opar, Williams, et al., 2013a, 2013b; Sole, et al., 2011a). A
recent fMRI investigation showed that previously injured hamstrings were significantly less
active than uninjured contralateral muscles during the Nordic hamstring exercise (Bourne, et
al, 2015). As in the current study, these activation deficits were present long after a return to
sport (~10 months post-injury) and were present without discrepancies in muscle CSA
(Bourne, et al, 2015). Earlier work employing sEMG and isokinetic dynamometry reported
inhibition during eccentric actions in previously injured BF muscles (Opar, Williams, et al.,
2013a, 2013b) many months after a return to sport, which suggests that this is likely a robust
phenomenon. Most recently, reduced BF electromyographic activity relative to other hip and
trunk muscles has been reported during treadmill running at 20km.h-1 in athletes with a
unilateral history of HSI (Daly, et al., 2015). However, only the current study provides
insights into the activation patterns of all the hamstring muscles in previously injured and
uninjured limbs during overground running. Furthermore, the observation of activation
deficits in BFLH muscles during high-speed running has direct implications for clinical
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practice because this is the activity most often associated with injury (Askling, et al., 2007;
Koulouris, et al., 2007; Schache, et al., 2009) and this muscle is the most common site of
injury (Connell, et al., 2004; Koulouris, et al., 2007), It is also noteworthy that pain-free high-
speed running is often used as a clinical marker for return to play (Heiderscheit, et al., 2010),
although the activation deficits observed in this cohort persisted in the absence of pain and
despite a complete return to pre-injury levels of training and competition. In the current
study, a moderate effect size (0.6) was observed for the comparison between ST muscles in
previously injured and uninjured limbs which raises the prospect that this study was
insufficiently powered to identify this unexpected difference. Future work should determine
whether or not BFLH injury is associated with reduced ipsilateral ST use.
The current results do diverge from one recent fMRI investigation (Schuermans, et al., 2014).
Schuermans and colleagues (Schuermans, et al., 2014) reported an increased percentage
change in T2 relaxation and more symmetrical muscle use in previously injured hamstrings
relative to uninjured hamstrings following ~255s of exhaustive leg curl exercise. The authors
proposed that the higher T2 shift represented a greater metabolic demand on the active tissue
during sub-maximal exercise and by extension, a reduced strength endurance capacity of
previously injured hamstrings. However, the prone leg curl exercise in this study
(Schuermans, et al., 2014) was performed with submaximal loads (5kg) and only involved
movement at the knee, which may not reflect the high-intensity and high-velocity multi-joint
demands of sprinting. It is possible that previously injured hamstrings may respond very
differently to submaximal loading, given that prior observations of reduced hamstring
activation have been noted during high-velocity (Daly, et al., 2015; Sole, et al., 2011a) or
maximal eccentric efforts (Bourne, et al, 2015; Opar, Williams, et al., 2013a, 2013b).
However, in the work by Schuermans and colleagues (Schuermans, et al., 2014) injuries were
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self-reported and heterogeneous in terms of location and severity which may have
confounded the results. Further, the analysis of muscle activation was limited to a 35mm
region in the distal thigh, which may not reflect whole-muscle use as accurately as the current
investigation.
It has been proposed that the acute pain and discomfort associated with HSI results in
centrally-mediated neural changes that chronically reduce activation of previously injured
muscles (Fyfe, et al., 2013b; Opar, et al., 2012). While acute inhibition is a normal response
to pain and injury that may protect the injured structures from further damage (Lund, et al.,
1991), it may also result in a permanent redistribution of motor activity within and between
muscles (Hodges & Tucker, 2011) if not adequately addressed in rehabilitation. Activation
deficits in previously injured hamstrings during high-speed running may reduce the ability of
these muscles to generate high levels of force (Daly, et al., 2015; Opar, Williams, et al.,
2013a, 2013b), particularly during the seemingly injurious (Schache, et al., 2009; Thelen,
Chumanov, Hoerth, et al., 2005) terminal-swing phase of running where hamstring stresses
are greatest (Chumanov, et al., 2011; Nagano, Higashihara, Takahashi, & Fukubayashi, 2014;
Schache, Dorn, Blanch, Brown, & Pandy, 2012). Prior hamstring injury has also been
reported to result in deficits in horizontal ground reaction forces during high speed running
(Brughelli, Cronin, Mendiguchia, Kinsella, & Nosaka, 2010; Mendiguchia et al., 2014).
Whether our athletes had similar deficits is unknown, although the observation of reduced
muscle activation offers a potential explanation for lasting deficits in force production.
The current study found no evidence of atrophy in previously injured hamstring muscles as
has been reported previously (Bourne, et al, 2015). Sanfilippo and colleagues (Sanfilippo,
Silder, Sherry, Tuite, & Heiderscheit, 2013) also found no evidence of atrophy in previously
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injured BFLH muscles six months following the completion of a standardised hamstring
rehabilitation program. However, chronically reduced BFLH volume and an apparently
compensatory hypertrophy of the ipsilateral BFSH has been reported after BFLH strains
(Silder, Heiderscheit, Thelen, Enright, & Tuite, 2008). These divergent findings may reflect
differences in training practices and competition level. It is also possible that alterations to
muscle architecture following HSI may reduce the sensitivity of CSA measures to muscle
size. Timmins and colleagues (Timmins, Shield, et al., 2014) recently reported that
previously injured BFLH muscles exhibited significantly shorter fascicles and greater
pennation angles than homonymous muscles in the uninjured contralateral limb. This increase
in pennation angle would tend to counter any effects of muscle atrophy on measures of
muscle thickness, so measures of CSA or thickness may not be as sensitive to atrophy as are
measures of muscle volume. Further work is required to understand the effect of prior HSI on
hamstring morphology, particularly in highly trained athletes. This study and previous work
(Bourne, et al, 2015; Sanfilippo, et al., 2013) suggest that structured, progressive intensity
rehabilitation programs may be effective at maintaining muscle cross-sections after HSI
while not adequately addressing activation deficits.
The current results suggest that in limbs with no history of HSI, the two-joint hamstring
muscles are activated rather uniformly during sprint running while BFSH is activated
significantly less than the BFLH and ST. Sloniger and colleagues (Sloniger, et al., 1997) have
previously reported very similar levels of BF, ST and SM muscle use according to T2 fMRI
changes after exhaustive treadmill running in recreationally active females, which is largely
in line with findings of the current investigation. However, Sloniger and colleagues (Sloniger,
et al., 1997) did not differentiate between the long and short heads of BF, which appear to
display distinct activation magnitudes during running.
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With regard to limitations of the current study, it is acknowledged that the retrospective
nature of this experiment means that it is not possible to determine whether activation deficits
in previously injured muscles were the cause or result of injury. Future prospective studies
should seek to clarify whether poor hamstring activation is associated with an increased risk
of HSI, although the expense of fMRI renders this methodology impractical for such study
designs. Also, given the absence of a control group without a history of HSI in either limb, it
is impossible to know whether participants had normal patterns of muscle activation in their
uninjured limbs. It is also important to consider that the T2 response to an exercise stimulus
is highly dynamic and can be influenced by a range of factors such as the metabolic capacity
and vascular dynamics of the active tissue (Patten, et al., 2003). We attempted to minimise
these factors through strict inclusion criteria (ie. recruiting male athletes of a similar age with
homogenous injury location and comparable training status), however, it was assumed that
these factors would not differ significantly between previously injured and uninjured
muscles.
This study provides novel insights into hamstring muscle use during high-speed running in
athletes with a unilateral history of BFLH injury. Future work should aim to clarify whether
the inhibition observed here causes or results from HSI. Identifying the methods by which
this deficit can be ameliorated should also be prioritised.
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Chapter 6: STUDY 3 – IMPACT OF EXERCISE SELECTION ON HAMSTRING MUSCLE ACTIVATION
Publication statement
This chapter is comprised of the following paper which has been accepted for publication at
the British Journal of Sports Medicine:
Bourne, MN., Williams, MD., Opar, DA., Al Najjar, A., & Shield, AJ. (2016). Impact of
exercise selection on hamstring muscle activation. Br J Sports Med, Accepted.
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Statement of Contribution of Co-Authors for Thesis by Published Paper
The authors listed below 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;
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 or other publications, and (c) the head of the responsible academic unit
5. They agree to the use of the publication in the student’s thesis and its publication on the Australasian Research Online database consistent with any limitations set by publisher requirements.
Contributor
Statement of contribution*
Matthew Bourne Experimental design, ethical approval, data collection and analysis, statistical analysis, manuscript preparation
08/03/2016 David Opar Aided in experimental design and manuscript preparation
Aiman Al Najjar Aided in data collectionMorgan Williams Assisted with statistical analysis and manuscript preparation Anthony Shield Aided in experimental design and manuscript preparation
Principal Supervisor Confirmation
I have sighted email from all co-authors confirming their certifying authorship.
Dr Anthony Shield ____________________ ______________
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6.1 LINKING PARAGRAPH
Fyfe et al. (2013) have recently proposed that high rates of HSI recurrence might be partly
explained by chronic neuromuscular inhibition which results in a reduced capacity to
voluntarily activate the BFLH muscle. Indeed, Chapter 5 demonstrated that previously injured
BFLH muscles were activated ~50% less than homonymous contralateral muscles with no
history of injury during the presumably injurious (Thelen, Chumanov, Hoerth, et al., 2005)
task of high-speed running. These observations are consistent with findings from this
student’s Honours project showing that previously injured hamstrings were significantly less
active than uninjured contralateral muscles during the NHE (Bourne, et al, 2015). Earlier
work employing sEMG and isokinetic dynamometry also reported inhibition during eccentric
actions in previously injured BF muscles (Opar, Williams, et al., 2013a, 2013b) which
suggests that this is a robust phenomenon. Persistent neuromuscular inhibition of BFLH
muscles, many months after rehabilitation and a full return to training and competition, may
help to explain observations of persistent atrophy (Silder, et al., 2008) and altered architecture
(Timmins, Shield, et al., 2014) in this muscle following injury. These data suggest the
possibility that conventional rehabilitation practices may not be adequately targeting the
previously injured BFLH.
Heavy resistance training offers a practical and potent stimulus for improving voluntary
activation (Akima et al., 1999) and evoking hypertrophy (Kraemer, et al., 2002) of skeletal
muscle. However, there is an emerging body of evidence (Mendiguchia, Arcos, et al., 2013b;
Mendiguchia, Garrues, et al., 2012; Ono, et al., 2011; Zebis et al., 2013) to suggest that
different exercises target different portions of the hamstring muscle group and it is possible
that some exercises employed in rehabilitation do not optimally target the injured muscle. An
improved understanding of the spatial patterns of hamstring muscle activation during
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different exercises may help practitioners to better tailor rehabilitation programs to the site of
injury.
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6.2 ABSTRACT
To determine the extent to which different strength training exercises selectively activate the
commonly injured biceps femoris long head (BFLH) muscle. METHODS: This two-part
observational study recruited 24 recreationally active males. Part 1 explored the amplitudes
and the ratios of lateral to medial hamstring (BF/MH) normalised electromyography (nEMG)
during the concentric and eccentric phases of 10 common strength training exercises. Part 2
used functional magnetic resonance imaging (fMRI) to determine hamstring T2 relaxation
time changes during two exercises which i) most selectively, and ii) least selectively activated
the BF in part 1. RESULTS: Eccentrically, the largest BF/MH nEMG ratio was observed in
the 45° hip extension exercise and the lowest was observed in the Nordic hamstring (NHE)
and bent-knee bridge exercises. Concentrically, the highest BF/MH nEMG ratio was
observed during the lunge and 45° hip extension and the lowest was observed for the leg curl
and bent-knee bridge. fMRI revealed a greater BFLH to semitendinosus activation ratio in the
45° hip extension than the NHE (p < 0.001). The T2 increase after hip extension for BFLH,
semitendinosus and semimembranosus muscles were greater than that for BFSH (p < 0.001).
During the NHE, the T2 increase was greater for the semitendinosus than for the other
hamstrings (p ≤ 0.002). CONCLUSION: This investigation highlights the non-uniformity of
hamstring activation patterns in different tasks and suggests that hip extension exercise more
selectively activates the BFLH while the NHE preferentially recruits the semitendinosus.
These findings have implications for strength training interventions aimed at preventing
hamstring injury.
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6.3 INTRODUCTION
Hamstring ‘tears’ are commonly experienced by athletes involved in running-based sports.
They are the most prevalent injury in track and field (Opar, Drezner, et al., 2013), Australian
Rules football (Orchard & Seward, 2002; Orchard, et al., 2013), and soccer (Ekstrand, et al.,
2011b) and up to 30% recur within 12 months (Orchard & Best, 2002). Upwards of 80% of
HSIs involve BFLH muscle (Koulouris, et al., 2007; Opar, et al., 2014; Timmins, Bourne, et
al., 2015) and most injuries are thought to occur during the late swing phase of high-speed
running (Schache, et al, 2009). During this phase of the gait cycle, the BFLH reaches its peak
length and develops maximal force while undergoing a forceful eccentric contraction to
decelerate the shank for foot strike (Chumanov, et al, 2007), and it is thought that these
conditions may at least partly explain its propensity for injury. It has also been reported that
prior BFLH injury is associated with a degree of neuromuscular inhibition (Opar, et al, 2013a;
Bourne, et al, 2015) and prolonged atrophy (Silder, et al, 2008), which suggests that current
rehabilitation practices do not adequately restore function to this muscle.
While the aetiology of HSI is multifactorial, it has been proposed that hamstring weakness is
a risk factor for future strain injury (Croisier, et al., 2008a; Opar, et al., 2014; Thorborg,
2014) and interventions aimed at increasing strength, particularly eccentric knee flexor
strength, have been effective in reducing HSI rates in several sports (Arnason, et al., 2008;
Askling, Tengvar, Tarassova, & Thorstensson, 2014; Askling, et al., 2013; Petersen, et al.,
2011; van der Horst, Smits, Petersen, Goedhart, & Backx, 2015). However, despite an
increased focus on hamstring strength in prophylactic programs (Heiderscheit, et al., 2010),
exercise selection is often implemented on the basis of clinical recommendations and
assumptions rather than empirical evidence (Guex & Millet, 2013; Malliaropoulos et al.,
2012). There is currently a small body of work on the activation patterns of the hamstrings
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during commonly employed exercises. Studies using functional magnetic resonance imaging
(fMRI) have shown that activation differs within and between hamstring muscles during
different tasks (Bourne, et al, 2015; Mendiguchia, Arcos, et al., 2013a; Mendiguchia,
Garrues, et al., 2012; Ono, et al., 2011; Ono, et al., 2010). For example, the semitendinosus
(ST) appears to be selectively activated during the Nordic hamstring exercise (NHE)
(Bourne, et al, 2015) and the eccentric prone leg curl (Ono, et al., 2010), while the
semimembranosus (SM) is preferentially recruited during the stiff leg deadlift (Ono, et al.,
2011). Surface electromyography (sEMG) has also been used in the analysis of hamstring
exercises (Ditroilo, De Vito, & Delahunt, 2013; Ono, et al., 2011; Ono, et al., 2010;
Schoenfeld et al., 2015; Zebis, et al., 2013). However, these studies are sometimes
contradictory and are often inconsistent with the results from fMRI (Bourne, et al, 2015;
Mendiguchia, Arcos, et al., 2013a; Mendiguchia, Garrues, et al., 2012; Ono, et al., 2011;
Ono, et al., 2010; Zebis, et al., 2013). The lack of complete agreement between fMRI and
sEMG might reflect the different physiological basis of each technique (Cagnie, et al., 2011).
Surface EMG amplitude is sensitive to the electrical activity generated by active motor units
and is detected by electrodes overlying the skin (Farina, et al., 2004). This provides valuable
information on the neural strategies involved during muscle activation with high temporal
resolution, but is prone to cross talk (Farina, et al., 2004) and cannot discriminate between
closely approximated segments of muscles (Adams, et al., 1992) such as the medial
hamstrings (semimembranosus and semitendinosus). By contrast, fMRI reflects the metabolic
activity associated with exercise (Cagnie, et al., 2011). Muscle activation is associated with a
transient increase in the transverse (T2) relaxation time of tissue water, which can be
interpreted from signal intensity changes in fMR images. These T2 shifts, which increase in
proportion to exercise intensity (Fisher, Meyer, Adams, et al., 1990; Fleckenstein, et al.,
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1988), can be mapped in cross-sectional images of muscles and therefore provide
significantly greater spatial clarity than sEMG (Adams, et al., 1992; Cagnie, et al., 2011).
An improved understanding of the patterns of hamstring muscle activation during common
strength training exercises may enable practitioners to make better informed decisions
regarding exercise selection in injury prevention and rehabilitation programs. The purpose of
this two-part study was to determine which exercises most selectively activate the BFLH. Part
1 used sEMG to determine the amplitude and ratio of lateral to medial hamstring activation
during 10 commonly employed exercises. Based on these findings, part 2 employed fMRI to
map muscle activation during two exercises that appeared to a) most selectively; and b) least
selectively activate the BF according to sEMG. We hypothesised that the patterns of
hamstring muscle activation would be non-uniform between exercises and that higher levels
of BF activity would be observed during hip-extension exercise (Ono, et al., 2011).
6.4 METHODS
Participants Twenty-four recreationally active male athletes (age, 24.4 ± 3.3 years, height, 181.8 ± 6.1 cm,
weight, 85.2 ± 13.4 kg) participated in this study. Eighteen athletes (age, 23.9 ± 3.1, height,
180.6 ± 5.9, weight, 86.0 ± 14.8) participated in part 1 and ten athletes (age, 24.6 ± 4.0,
height, 183.5 ± 7.0, weight, 83.5 ± 8.7) participated in part 2. A priori sample size estimates
were based on 1) the capacity to detect a 10% difference in the ratio of BF to MH (BF/MH)
sEMG amplitude between exercises (Zebis, et al., 2013); and 2) an effect size of 1.0 in T2
relaxation time between muscles (Bourne, et al, 2015), at a power of 0.80 and with p<0.05.
Participants were free from soft tissue and orthopaedic injuries to the trunk, hips and lower
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limbs at the time of testing and had no known history of cardiovascular, metabolic or
neurological disorders. Participants had not suffered an HSI in the previous 12 months and
had no history of anterior cruciate ligament injury. Prior to testing, all participants completed
a cardiovascular screening questionnaire (Appendix B) to make sure it was safe for them to
perform intense exercise and those who were involved in part 2 also completed a standard
MRI screening questionnaire (Appendix C) to ensure it was safe for them to enter the
magnetic field. All participants provided written, informed consent for this study, which was
approved by the Queensland University of Technology Human Research Ethics Committee
and the University of Queensland Medical Research Ethics Committee.
Study Design
This cross-sectional study involved two parts. In the first we explored the sEMG amplitudes
and ratios of BF to medial hamstring (MH) sEMG activity during ten commonly employed
strength training exercises. Based on these findings, part 2 involved an fMRI investigation of
two exercises which appeared to a) most selectively, and b) least selectively activate the BF
muscle during eccentric contractions.
PART 1
Prior to testing participants were familiarised with the exercises used in this investigation. All
were shown a demonstration of each exercise (Figure 1) and performed several practice
repetitions while receiving verbal feedback from the investigators. Once the participant could
complete the exercise with appropriate technique, the loads were progressively increased
until an approximate 12RM load was determined (unless the exercise was already
supramaximal, ie. NHE and glute-ham-raise). On the day of testing, participants reported to
the laboratory and were prepared for sEMG measurement. The testing session began with two
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maximal voluntary isometric contractions (MVICs) for the hamstrings (see below).
Subsequently, participants completed a single set of six repetitions of each exercise, each
with the predetermined 12RM load, in randomised order. All data were sampled from a
random limb, which was the exercised limb during all unilateral movements and all testing
sessions were supervised by the same investigator (MNB) to ensure consistency of
procedures.
Electromyography
Bipolar pre-gelled Ag/AgCl sEMG electrodes (10mm diameter, 15mm interelectrode
distance) were used to record electromyographical activity from the BF and MH. The skin of
the participants was shaved, lightly abraded and cleaned with alcohol before electrodes were
placed on the posterior thigh, midway between the ischial tuberosity and tibial epicondyles.
Electrodes were oriented parallel to the line between these two landmarks, as per SENIAM
guidelines (Hermens, Freriks, Disselhorst-Klug, & Rau, 2000), and secured with tape to
minimise motion artefact. The reference electrode was placed on the ipsilateral head of the
fibula. Muscle bellies of the BF and MH were identified via palpation and correct placement
was confirmed by observing active external and internal rotation of the knee in 90° of flexion
(Opar, Williams, et al., 2013a; Timmins et al., 2014). During all exercise trials, hip and knee
joint angles were measured simultaneously with sEMG data using two digital goniometers.
The hip sensor’s axis of rotation was aligned with the greater trochanter of the femur and the
knee sensor was positioned superficial to the lateral femoral epicondyle.
Maximal voluntary contraction
Surface EMG activity was recorded during MVICs of the hamstrings using a custom-made
device which was fitted with two uniaxial load cells (Opar, Piatkowski, et al., 2013a),
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Participants lay prone with their hips in 0° of flexion and knees fully extended (180°), with
their ankles secured in immoveable yokes and were asked to perform forceful knee flexion
while investigators provided strong verbal encouragement. After 1-2 warm-up contractions,
participants completed two 3-4sec MVICs, with 30-sec of rest separating each attempt. The
contraction that elicited the highest average amplitude for the BF and MH was used to
represent the maximal EMG amplitude.
Data analysis
All sEMG and joint angle data were sampled at 1 kHz through a 16-bit PowerLab 26T AD
unit (ADInstruments, New South Wales, Australia) (amplification = 1000; common mode
rejection ratio = 10dB) and analysed using LabChart 8.0 (AD Instruments, New South Wales,
Australia). Raw sEMG data were filtered using a Bessel filter (frequency bandwidth = 10-
500Hz) and then full wave rectified. Joint angle data were used to determine the concentric
(lifting) and eccentric (lowering) phases of each repetition for each exercise. For each phase,
the filtered sEMG signal was normalised to values obtained during MVIC and these
normalised sEMG (nEMG) values were averaged across the six repetitions.
Exercise Protocol
The 10 exercises were chosen based on a review of the scientific literature (Mendiguchia,
Garrues, et al., 2012; Ono, et al., 2011; Schoenfeld, et al., 2015; Zebis, et al., 2013). They
included the bilateral and unilateral stiff-leg deadlift, hip hinge, lunge, unilateral bent and
straight knee bridges, leg curl, 45° hip extension, glute-ham-raise and the NHE (Figure 6-1).
Unless the exercise was explosive (hip hinge) or supramaximal and eccentric-only (NHE and
glute-ham raise) participants completed both the concentric and eccentric phases of each
exercise using a 12-RM load at a constant pace (2 s up and 2 s down).
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Figure 6-1. The 10 examined exercises. (a) bilateral stiff-leg deadlift, (b) hip hinge, (c)
unilateral stiff-leg deadlift, (d) lunge, (e) unilateral bent knee bridge, (f) unilateral straight
knee bridge, (g) leg curl, (h) 45° hip extension, (i) glute-ham-raise, (j) Nordic hamstring
exercise (NHE).
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Statistical analysis
Data were analysed using JMP version 10.02 (SAS Institute Inc, 2012). Descriptive statistics
were calculated for mean nEMG amplitudes of BF and MH for the concentric and eccentric
phases of each exercise and an activation ratio was determined by dividing the average BF
nEMG amplitude by the average MH nEMG amplitude (BF/MH); ratios >1.0 indicated that
the BF was more active than the MH muscles. For both the concentric and eccentric phases,
repeated measures linear mixed models fitted with the restricted maximum likelihood method
were used to determine differences between exercises. For this analysis, exercise was the
fixed factor and participant identity the random factor. When a significant main effect was
observed for exercise, post hoc t-tests with Bonferroni corrections were used to identify the
source and reported as mean differences with 95% CIs. For these analyses, the Bonferroni
adjusted p value was set at <0.002.
PART 2
A cross-sectional design was used to map the spatial patterns of hamstring muscle activation
during the 45° hip extension and NHE. These exercises were chosen because they a) most
selectively (45° hip extension) and b) least selectively (NHE) activated the BF muscle during
eccentric contractions according to sEMG. Participants completed two separate exercise
sessions, separated by at least six days (14 ± 5 days), with each session involving one of the
aforementioned exercises. Functional MRI scans of both thighs were acquired before and
immediately after each exercise bout. All testing sessions were supervised by the same
investigator (MNB).
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Exercise Protocol
A depiction of the 45° hip extension and NHE can be found in Figure 6-1. All exercise was
completed using the same equipment as that used in part 1. Participants completed five sets of
10 repetitions of each exercise with one-minute rest intervals between sets (Ono, et al., 2011),
The higher volume of exercise (compared to part 1) was necessary because transient T2
changes reflect fluid shifts associated with glycolysis and have a higher detection threshold
than sEMG (Cagnie, et al., 2011), All subjects completed 50 repetitions successfully. During
the rest periods, participants remained in a seated position (for the hip extension exercise) or
lay prone (NHE) to minimise activation of the hamstrings. The 45° hip extension exercise
was performed unilaterally with a starting load corresponding to each participant’s
approximate 12-RM (median = 10 kg; range = 10 to 20 kg). However if the participant could
no longer complete the exercise with the allocated load, the weight was gradually reduced by
increments of 5kg until it could be completed at the desired speed (2 s up and 2 s down),
which was controlled by an electronic metronome. The NHE was performed bilaterally with
body weight only. Participants received verbal support from the investigators throughout all
exercise sessions to promote maximal effort. All participants were returned to the scanner
immediately following the cessation of exercise and post-exercise scans began within 148.6 ±
24 s (mean ± SD).
Functional muscle magnetic resonance imaging (fMRI)
All fMRI scans were performed using a 3-Tesla (Siemens TrioTim, Germany) imaging
system with a spinal coil. The participant was positioned supine in the magnet bore with their
knees fully extended and hips in neutral and straps were secured around both limbs to prevent
any undesired movement. Consecutive T2-weighted axial images were acquired of both limbs
beginning at the level of the iliac crest and finishing distal to the tibial plateau using a 180 x
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256 image matrix. Images were acquired before and immediately after exercise using a Car-
Purcel-Meiboom-Gill (CPMG) spin-echo pulse sequence and the following parameters:
transverse relaxation time (TR) = 2540 ms; echo time (TE) = 8, 16, 24, 32, 40, 48 and 56 ms;
number of excitations = 1; slice thickness = 10 mm; interslice gap = 10 mm; field of view =
400 x 281.3 mm). The total acquisition time for each scan was 6 min 24 s. A localiser
adjustment (20 s) was applied prior to the first sequence of each scan to standardise the field
of view and to align collected images between the pre- and post- exercise scans (Bourne, et
al, 2015). To minimise any inhomogeneity in MR images caused by dielectric resonances at
3T, a post-processing (B1) filter was applied to all scans (de Sousa, et al., 2011); this is a
post-processing image filter that improves the image signal intensity profile without affecting
the image contrast. In addition, to ensure that the signal intensity profile of T2-weighted
images was not disrupted by anomalous fluid shifts, participants were seated for a minimum
of 15 min (Ono, et al., 2011) before data acquisition.
For each exercise session, the T2 relaxation times of each hamstring muscle were measured
in T2-weighted images acquired before and after exercise to evaluate the degree of muscle
activation during exercise. All fMRI scans were transferred to a Windows computer in the
digital imaging and communications in medicine (DICOM) file format. The T2 relaxation
times of each hamstring muscle (BFLH, BFSH, ST and SM) were measured in five axial slices,
corresponding to 30, 40, 50, 60 and 70% of thigh length; these values were determined
relative to the distance between the inferior margin of the ischial tuberosity (0%) and the
superior border of the tibial plateau (100%) (Bourne, et al, 2015; Ono, et al., 2011). Image
analysis software (Sante Dicom Viewer and Editor, Cornell University) was used to measure
the signal intensity of each hamstring muscle in the exercised limb in both the pre- and post-
exercise scans. The signal intensity was measured in each slice using a circular region of
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interest (ROI) (Mendiguchia, Garrues, et al., 2012) which was placed in a homogenous
region of contractile tissue in each muscle belly (avoiding fat, aponeurosis, tendon, bone and
blood vessels). The size of each ROI varied (0.2 to 5.6 cm2) based on the cross-sectional area
and the amount of homogeneous tissue available in each slice. The signal intensity reflected
the mean value of all pixels within the ROI and was measured across seven echo times (8, 16,
24, 32, 40, 48, 56ms). To calculate the T2 relaxation time for each ROI, the signal intensity
value at each echo time was fitted to a mono-exponential decay model using a least squares
algorithm:
[(SI= M exp(echo time / T2)] (Ono, et al., 2011)
where SI is the signal intensity at a specific echo time, and M represents the pre-exercise
fMRI signal intensity. To assess the extent to which each ROI was activated during exercise,
the mean percentage change in T2 was calculated as:
[(mean post-exercise T2 / mean pre-exercise T2) x 100].
To provide a meaningful measure of whole-muscle activation, the percentage change in T2
relaxation time for each hamstring muscle was evaluated using the ROIs (at all five thigh
levels). Previous studies have demonstrated excellent reliability of T2 relaxation time
measures with intra-class correlation coefficients ranging from 0.87 to 0.94 (Cagnie, et al.,
2008; Cagnie, et al., 2011).
Statistical analysis
Repeated measures linear mixed models fitted with the restricted maximum likelihood
(REML) method were used to determine the spatial activation patterns of the hamstring
muscles during the 45° hip extension and NHE. The percentage change in T2 relaxation time
was compared between each hamstring muscle (BFLH, BFSH, ST and SM) for both exercises.
For this analysis, muscle was the fixed factor and both participant identity and participant
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identity x muscle the random factors. When a significant main effect was detected for muscle,
post hoc t tests with Bonferroni corrections were used to determine the source; the adjusted p
value was set at 0.008. Given that the two examined exercises differed in intensity and
contraction mode(s), it was not appropriate to directly compare the magnitude of the T2 shifts
between exercises.(Patten, et al., 2003) Instead, repeated measures linear mixed models fitted
with the REML method were used to determine differences in the ratio of BF to ST (BFLH/ST
and BFSH/ST) and SM to ST (SM/ST) percentage change in T2 relaxation time between
exercises. For these analyses exercise was the fixed factor and participant identity the random
factor. When a main effect was found for exercise, post hoc t tests were again used to
determine the source and reported as mean difference (and 95% CI). Alpha was set at p<0.05
for these analyses.
6.5 RESULTS
Levels of hamstring muscle activation
Means and standard errors for the average nEMG amplitudes of the BF and MH muscles
during the 10 exercises can be found in Table 6-1. Average BF muscle activity ranged from
21.4% (lunge) to 99.3% (unilateral straight knee bridge) MVIC during the concentric phase
and 10.7% (hip hinge) to 71.9% (NHE) during the eccentric phase. Average MH muscle
activity ranged from 18.1% (lunge) to 120.7% (leg curl) during the concentric phase and
11.6% (hip hinge) to 101.8% (NHE) during the eccentric phase.
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Table 6-1. Mean normalised EMG (nEMG) amplitudes for the biceps femoris (BF) and
medial hamstring (MH) muscles during the concentric and eccentric phases of 10 hamstring
strengthening exercises. Data are expressed as means (standard error).
Normalised sEMG Exercise Muscle Concentric Eccentric Bilateral stiff leg deadlift BF 54.6 (7.6) 21.4 (4.9)
MH 49.3 (8.0) 18.2 (5.5) Hip hinge BF 44.9 (7.4) 10.7 (4.8)
MH 45.7 (7.8) 11.6 (5.4) Unilateral stiff leg deadlift BF 51.9 (7.6) 26.7 (4.9)
MH 57.5 (8.0) 27.7 (5.5) Lunge BF 21.4 (7.4) 13.9 (4.8)
MH 18.1 (7.8) 16.9 (5.4) Unilateral bent-knee bridge BF 41.9 (7.4) 23.1 (4.8)
MH 57.4 (7.8) 24.5 (4.6) Unilateral straight-knee bridge BF 99.3 (7.4) 55.8 (4.8)
MH 90.6 (7.8) 54.9 (5.4) Unilateral leg curl BF 87.6 (7.4) 43.7 (4.8)
MH 120.7 (7.8) 54.6 (5.4) 45° hip extension BF 75.6 (7.4) 48.5 (4.8)
MH 61.2 (7.8) 37.1 (5.4) Glute-ham-raise BF - 57.7 (5.1)
MH - 78.2 (5.7) Nordic hamstring exercise BF - 71.9 (4.8)
MH - 101.8 (5.4)
The concentric BF/MH activation ratio for each exercise can be found in Figure 6-2a. A
significant main effect was detected between exercises (p < 0.001) with post hoc t tests
showing that the BF/MH ratio was greater during the lunge than the leg curl (mean difference
= 0.81, 95% CI = 0.48 to 1.14, p < 0.001) and bent-knee bridge (mean difference = 0.74, 95%
CI = 0.41 to 1.06, p < 0.001). Similarly, the BF/MH ratio was greater in the 45° hip extension
exercise than the leg curl (mean difference = 0.62, 95% CI = 0.30 to 0.95, p < 0.001) and
bent-knee bridge (mean difference = 0.55, 95% CI = 0.22 to 0.87, p = 0.001).
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Eccentric biceps femoris to medial hamstring (BF:MH) activation ratio
The eccentric BF/MH activation ratio for each exercise can be found in Figure 6-2b. A
significant main effect was observed for exercise (p < 0.001) with post hoc analyses revealing
that the BF/MH ratio was significantly greater in the 45° hip extension than the NHE (mean
difference = 0.69, 95% CI = 0.40 to 0.99, p < 0.001), bent-knee bridge (mean difference =
0.69, 95% CI = 0.40 to 0.99, p<0.001), leg curl (mean difference = 0.60, 95% CI = 0.30 to
0.89, p < 0.001) and the glute-ham raise (mean difference = 0.56, 95% CI = 0.25 to 0.87, p <
0.001). No other between-exercise differences were observed once adjusted for multiple
comparisons (p > 0.002).
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Figure 6-2. Biceps femoris (BF) to medial hamstring (MH) normalised EMG (nEMG)
relationship for the (a) concentric and (b) eccentric phases of each exercise. (SDL) Bilateral
stiff-leg deadlift, (HH) hip hinge, (USDL) unilateral stiff-leg deadlift, (L) lunge, (bKb)
unilateral bent knee bridge, (SKB) unilateral straight knee bridge, (LC) leg curl, (HE) 45°
hip extension, (GHR) glute-ham-raise, (NHE) Nordic hamstring exercise. Exercises to the left
of the 45° line exhibited higher levels of BF than MH nEMG and exercises to the right
displayed higher levels of MH than BF nEMG.
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Percentage change in T2 relaxation time following the 45° hip extension exercise A significant main effect was observed for muscle (p < 0.001) with post hoc t tests revealing
that the exercise-induced T2 changes in the BFSH were significantly lower than those
observed for the BFLH (mean difference = 60.65%, 95% CI = 41.25 to 80.06%, p < 0.001),
ST (mean difference = 77.99%, 95% CI = 58.40 to 97.59%, p < 0.001) and SM muscles
(mean difference = 49.81%, 95% CI = 30.12 to 69.52%, p < 0.001) (Figure 6-3). The T2
change for ST was significantly greater than SM (mean difference = 28.17%, 95% CI = 9.24
to 47.11%, p = 0.005) however, no difference was observed between the BFLH and SM (p =
0.245) or between the BFLH and ST muscles (p = 0.067).
Figure 6-3. Percentage change in fMRI T2 relaxation times of each hamstring muscle
following the 45° hip extension exercise. Values are expressed as mean percentage change
compared to values at rest. ** indicates significantly different from ST, BFLH and SM
(p<0.001). * indicates significantly different from ST (p=0.005). Error bars depict standard
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error. BFLH, biceps femoris long head; BFSH, biceps femoris short head; ST, semitendinosus;
SM, semimembranosus.
Percentage change in T2 relaxation time following the Nordic hamstring exercise A
main effect was detected for muscle (p < 0.001). Post hoc analyses showed that the T2
changes induced by exercise within the ST were significantly larger than those observed for
the BFLH (mean difference = 29.84%, 95% CI = 20.51 to 39.16%, p < 0.001), BFSH (mean
difference = 16.19%, 95% CI = 6.39 to 25.99%, p = 0.002) and SM (mean difference =
29.94%, 95% CI = 20.43 to 39.44%, p < 0.001) muscles (Figure 6-4). In addition, the T2
increase observed for BFSH was significantly greater than for the BFLH (mean difference =
13.65%, 95% CI = 3.88 to 23.40%, p = 0.008) and SM (mean difference = 13.75, 95% CI =
3.81 to 23.68, p = 0.008) muscles. No difference was observed between the BFLH and SM
muscles (p = 0.982).
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Figure 6-4. Percentage change in fMRI T2 relaxation times of each hamstring muscle
following the Nordic hamstring exercise. Values are expressed as mean percentage change
compared to values at rest. ** indicates significantly different from BFLH, BFSH and SM
(p≤0.002). * indicates significantly different from BFLH and SM (p=0.008) Error bars depict
standard error. BFLH, biceps femoris long head; BFSH, biceps femoris short head; ST,
semitendinosus; SM, semimembranosus.
Comparison of hamstring activation ratios between exercises
When comparing the BFLH/ST ratio a significant main effect was observed for exercise (p <
0.001) with post hoc analyses revealing a significantly greater ratio during 45° hip extension
exercise than during the NHE (mean difference = 0.73, 95% CI = 0.59 to 0.87, p < 0.001)
(Figure 6-5).
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Figure 6-5. Ratio of biceps femoris long head (BFLH) to semitendinosus (ST) (BFLH/ST)
percentage change in fMRI T2 relaxation times following the 45° hip extension and the
Nordic hamstring exercise (NHE). * indicates a significant difference between exercises
(p<0.001). Error bars depict standard error.
A significant main effect was also detected for exercise when comparing the BFSH/ST ratio (p
< 0.001). Post hoc t tests demonstrated that this ratio was significantly greater during the
NHE than during the 45° hip extension exercise (mean difference = 0.42, 95% CI = 0.24 to
0.62, p < 0.001).When comparing the SM/ST ratio a significant main effect was detected for
exercise (p < 0.001) with post hoc t tests showing relatively higher ratios during the 45° hip
extension than during the NHE (mean difference = 0.51, 95% CI = 0.39 to 0.64, p < 0.001).
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6.6 DISCUSSION
The primary aim of this study was to determine movements that most selectively activate the
commonly injured BFLH. The results support the hypothesis that hamstring activation patterns
differ markedly between exercises and provide evidence to suggest that hip extension
exercise more selectively targets the BFLH than the NHE.
The NHE has been shown, in a number of studies, (Arnason, et al., 2008; Petersen, et al.,
2011; van der Horst, et al., 2015), to reduce HSIs in soccer players as long as compliance is
adequate (Goode et al., 2015). However, we (Bourne, et al, 2015) and others (Mendiguchia,
Arcos, et al., 2013a) have previously reported that the NHE preferentially activates the ST
and this might be interpreted as evidence that the exercise is sub-optimal to protect against
running-related strain injury. In this study, we have provided EMG evidence which shows,
despite the relatively selective activation of the ST, that the lateral hamstrings were still
strongly activated during the NHE. Indeed, BF nEMG was higher during the NHE than
during the eccentric phase of any other exercise and the evidence for this exercise’s
protective effects (Arnason, et al., 2008; Petersen, et al., 2011; van der Horst, et al., 2015)
suggests that eccentric actions alone in a training program are sufficient to make the
hamstrings more resistant to strain injury. High levels of BF nEMG during the NHE are
consistent with previous investigations (Zebis, et al., 2013) and are the result of the
supramaximal intensity of the exercise, which potentially explains why high levels of BF
nEMG were also observed in the eccentric glute-ham raise. High levels of BF nEMG in
concentric actions were observed in several other exercises including the straight-knee
bridge, leg curl and the 45° hip extension which corroborates previous observations (Zebis, et
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al., 2013). However, the importance of hamstring activation patterns during concentric
actions remains unclear from the perspective of injury prevention.
While high levels of nEMG are an important stimulus for improving strength and voluntary
activation (Kraemer, et al., 2002), exercise selectivity may still have important implications
for rehabilitation. For example, inhibition of previously injured BF muscles during eccentric
actions has been reported many months after rehabilitation (Opar, et al, 2013a, 2013b;
Bourne, et al, 2015), and it has been proposed (Fyfe, et al, 2013) that these deficits might
partly explain observations of persistent eccentric knee flexor weakness (Opar, et al, 2013a),
BFLH atrophy (Silder, et al, 2008) and a chronic shortening of BFLH fascicles (Timmins, et al,
2015). These data (Bourne, et al, 2015; Timmins, et al, 2015; Opar, et al, 2013a, 2013b;
Silder, et al, 2008) are consistent with the possibility that conventional rehabilitation
strategies may not adequately target the commonly injured BFLH. Previous studies have
shown that the ratio of lateral to medial hamstring (BF/MH) sEMG varies with foot rotation
(Lynn & Costigan, 2009) and differs between exercises (Zebis, et al., 2013). In the current
study, the eccentric phase of the 45° hip extension exercise exhibited the greatest BF/MH
nEMG ratio (1.5 ± 0.1) while the NHE (0.8 ± 0.1) and bent-knee bridge exercises (0.8 ± 0.1)
displayed the lowest ratios. These observations were confirmed in the subsequent fMRI
analysis whereby the ratio of BFLH to ST in the 45° hip extension exercise (0.96 ± 0.09) was
markedly higher than that observed for the NHE (0.23 ± 0.08). It is also noteworthy that the
eccentric phase of other hip-oriented exercises (straight-knee bridge, unilateral and bilateral
stiff-leg deadlift and hip hinge) displayed BF/MH nEMG ratios >1.0. In contrast, the
eccentric phase of exercises that involved significant movement at the knee (leg curl, glute-
ham-raise, bent-knee bridge and NHE) had higher levels of medial hamstring nEMG (BF/MH
ratio <1.0). These data suggest the possibility that hamstring activation strategies during
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eccentric efforts might be partly dependent on the joints involved in each movement. During
concentric contractions, the most selective BF activation was observed in the lunge exercise
which corroborates a previous fMRI investigation (Mendiguchia, Garrues, et al., 2012).
However, it is important to consider that the lunge also exhibited the lowest BF nEMG
amplitude (21.4 ± 7.4%) of any exercise which likely renders it an inadequate stimulus for
improving strength or hypertrophy in this muscle (Kraemer, et al., 2002). Interestingly, the
exercise that least selectively activated the BF during concentric contractions was the leg
curl, which mimics the joint positions and hamstring muscle-tendon lengths experienced in
the NHE.
The mechanism for higher levels of BFLH activity during hip extension-oriented movements
remains unclear, however, it is possible that hamstring muscle moment arms play a role. For
example, the BFLH exhibits a larger moment arm at the hip than at the knee (Thelan, et al ,
2005) and therefore possesses a greater mechanical advantage at this joint. As a result, the
BFLH undergoes significantly more shortening during hip extension than knee flexion. By
comparison, the ST displays a larger sagittal plane moment arm at the knee than both BFLH
and SM (Thelan, et al , 2005), which may explain its preferential recruitment during
movements at this joint, such as the NHE and leg curl exercises. It is also noteworthy that the
ST is a fusiform muscle with long fibre lengths and many sarcomeres in series, which
potentially makes it well-suited to forceful eccentric contractions (Lieber, et al, 2000) such as
those experienced in the NHE. Further work is needed to clarify the mechanisms
underpinning these unique strategies of hamstring activation during hip and knee movements.
The current findings are different to some others that have investigated hamstring activation
patterns during different tasks. For example, Zebis and colleagues (2013) recently reported
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that both the NHE and the prone isokinetic leg curl were performed with very similar levels
of ST and BFLH nEMG. However, in the current investigation, the NHE and leg curl exercises
resulted in more selective activation of the medial hamstrings and, in the case of the NHE, the
fMRI results also suggest selective use of the ST muscle. Differences between these studies
may conceivably be related to participant sex (females (Zebis, et al., 2013) versus males in
the current study) and electrode placement. However, it is also important to consider that
sEMG does not have the spatial resolution of fMRI and cannot reliably distinguish between
neighbouring muscles (Adams, et al., 1992), such as the long and short heads of BF or the ST
and SM, which appear to display distinct activation magnitudes (Bourne, et al, 2015; Ono, et
al., 2011; Ono, et al., 2010). These data highlight the limitations of relying exclusively on
sEMG to infer strategies of hamstring muscle activation during exercise and suggest the need
for more spatially robust methods in future work.
In interpreting the results of this study, it is important to consider that sEMG and fMRI
techniques measure different aspects of muscle activity. The absence of T2 relaxation time
changes in people with McCardle’s disease (Fleckenstein et al., 1991) suggests that fMRI is
sensitive to glycolysis (Meyer & Prior, 2000) and it is thought that the osmotic fluid shifts
which persist after exercise and give rise to T2 changes are a consequence of the
accumulation of glycolytic metabolites (Patten, et al., 2003). Fortunately, the proportion of
Type II glycolytic fibres does not appear to vary across the hamstring muscles (Garrett,
Califf, & Bassett, 1984) so this is unlikely to be a confounding factor. However, exercise
induced changes in T2 will be influenced by contraction mode because concentric work is
markedly less efficient than eccentric work against the same loads (Shellock, Fukunaga,
Mink, & Edgerton, 1991) As a consequence, the differences in T2 relaxation time changes
after the 45° hip extension exercise which involved concentric and eccentric actions and the
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almost entirely eccentric NHE do not reflect only the levels of voluntary muscle activation.
Instead, fMRI can offer insights into the relative metabolic activity and reliance upon
different hamstring muscles in each exercise. According to fMRI, the NHE involves
preferential ST use with modest use of the other hamstrings, while the 45° hip extension
exercise appears to heavily recruit both the BFLH and ST muscles. These observations are
largely consistent with the sEMG component of this study, which also suggested higher
activation of the medial than lateral hamstrings in the NHE and more even activation of the
medial and lateral hamstrings in the 45° hip extension.
Characterising the activation patterns of the hamstrings during different tasks is an important
first step in identifying exercises worthy of further investigation however, electrical or
metabolic activity of muscles should not be the only factors considered in exercise selection.
Further work is required to understand how the hamstrings adapt to these exercises and
adaptation is influenced by a range of factors, such as contraction mode (Roig et al., 2009;
Timmins, Ruddy, et al., 2015) and range of motion (Lieber & Friden, 2000), which were not
a part of the current investigation. For example, there is little reason to believe that concentric
or concentrically-biased exercise is effective in HSI prevention or rehabilitation programs
(Askling, et al., 2014; Askling, et al., 2013; Mjolsnes, Arnason, Osthagen, Raastad, & Bahr,
2004). Indeed, there is evidence that concentric training may shorten BFLH fascicles
(Timmins, Ruddy, et al., 2015) and shift knee flexor torque-joint angle relationships towards
shorter muscle lengths (Kilgallon, Donnelly, & Shafat, 2007) and neither of these adaptations
are considered beneficial for HSI prevention (Brockett, et al., 2004; Timmins, Bourne, et al.,
2015). Because eccentric and concentric training programs appear to have opposing effects
on fascicle lengths (Timmins, Ruddy, et al., 2015), it is possible that exercises combining
contraction modes may have minimal or at least blunted effects on muscle architecture.
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Future studies are needed to assess the impact of certain exercises on known or proposed risk
factors for HSI such as eccentric strength (Opar, et al., 2014) and fascicle lengths (Timmins,
Bourne, et al., 2015), and only then will there be sufficient evidence to justify use of those
exercises in intervention studies aimed at reducing the risk of injury.
Given the high cost of fMRI, it was not possible to include all participants in both parts of the
experiment. Therefore, comparing the results of part 1 and 2 should be done with caution.
Furthermore, all of our participants were recreationally active men so it remains to be seen
whether these findings can be applied to more highly trained athletes. We have previously
shown that recreationally active young men with a history of unilateral hamstring strain
exhibited less T2 change in previously injured muscles than in their uninjured homologous
muscles from the contralateral limb after performing the Nordic exercise (Bourne, et al.,
2015). Therefore, more research will be needed to establish whether the patterns of selective
muscle activation observed in the current study are also evident in athletes with a history of
strain injury. Lastly, it should be acknowledged that the T2 response to an exercise stimulus
is highly dynamic and can be influenced by a range of factors such as the metabolic capacity
and vascular dynamics of the active tissue (Patten, et al., 2003). We attempted to minimise
this by recruiting only male participants with a similar age and training status.
The current study suggests that the patterns of hamstring muscle activation are heterogeneous
between different strength exercises. We have provided sEMG evidence to suggest that,
during eccentric contractions, hip extension exercise more selectively activates the lateral
hamstrings while knee flexion-oriented exercises may preferentially recruit the medial
hamstrings. However, despite being the least selective activator of the BF, the NHE still
elicited higher levels of BF nEMG than any other exercise which may help to explain how it
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confers HSI-preventive benefits (Arnason, et al., 2008; Petersen, et al., 2011; van der Horst,
et al., 2015). The results of the fMRI investigation largely confirm our initial sEMG
observations, however, they also show that the BFLH, BFSH, ST and SM all display distinct
patterns of muscle use during different tasks. Collectively, the results of this study highlight
the limitations of relying on a single method to infer strategies of muscle activation and
suggest that the hip extension exercise may be useful for improving strength and voluntary
activation of the commonly injured BFLH. Future work is needed to determine the effect of
this and other exercises on hamstring architecture and morphology.
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Chapter 7: STUDY 4 – ADAPTABILITY OF HAMSTRING ARCHITECTURE AND MORPHOLOGY TO TARGETED RESISTANCE TRAINING
Publication statement
This chapter is comprised of the following paper which is currently under review at the
British Journal of Sports Medicine:
Bourne, MN., Duhig, SJ., Timmins, RG., Williams, MD., Opar, DA., Al Najjar, A., Kerr, G.,
& Shield, AJ. (2016). Impact of Nordic hamstring and hip extension training on hamstring
muscle architecture and morphology. Br J Sports Med, Under Review.
138
Statement of Contribution of Co-Authors for Thesis by Published Paper
The authors listed below 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;
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 or other publications, and (c) the head of the responsible academic unit
5. They agree to the use of the publication in the student’s thesis and its publication on the Australasian Research Online database consistent with any limitations set by publisher requirements.
Contributor
Statement of contribution*
Matthew Bourne Experimental design, ethical approval, data collection and analysis, statistical analysis, manuscript preparation
08/03/2016 Steven Duhig Aided in experimental design and data collection
Ryan Timmins Assisted in data collection David Opar Aided in experimental design and manuscript preparation
Aiman Al Najjar Assisted with data collection Morgan Williams Assisted with statistical analysis and manuscript preparation
Graham Kerr Assisted with experimental design and manuscript preparation Anthony Shield Aided in experimental design and manuscript preparation
Principal Supervisor Confirmation
I have sighted email from all co-authors confirming their certifying authorship.
Dr Anthony Shield ____________________ ______________
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7.1 LINKING PARAGRAPH
The result of Chapter 6 demonstrated that hip extension exercise more selectively activates
the BFLH while the NHE preferentially recruits the semitendinosus. These findings have
implications for strength training interventions aimed at preventing hamstring injury.
However, it remains to be seen how hamstring muscle architecture and morphology adapts to
these exercises after a period of training. Indeed, adaptation is influenced by a range of
factors, such as contraction mode (Roig, et al., 2009; Timmins, Ruddy, et al., 2015) and range
of motion (Lieber & Friden, 2000), which were not explored in Chapter 6.
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7.2 ABSTRACT
The architectural and morphological adaptations of the hamstrings in response to training
with different exercises have not been explored. PURPOSE: To evaluate changes in
hamstring muscle volume, anatomical cross-sectional area (ACSA) and biceps femoris long
head (BFLH) fascicle length following 10-weeks of Nordic hamstring exercise (NHE) or hip
extension (HE) training. METHODS: Thirty recreationally active male athletes (age, 22.0 ±
3.6 years, height, 180.4 ± 7 cm, weight, 80.8 ± 11.1 kg) were randomly allocated to one of
three groups: 1) HE training (n=10), NHE training (n=10), or no training (CON) (n=10).
BFLH fascicle length was assessed before, during (5 weeks) and after the intervention with
two-dimensional ultrasound. Muscle volumes and ACSAs of the hamstring muscles were
determined before and after training via magnetic resonance imaging. RESULTS: Compared
to baseline, BFLH fascicles were longer in the NHE and HE groups at mid- (p < 0.001) and
post-training (p < 0.001) but remained unchanged for the CON group (p > 0.05). The
percentage change in BFLH volume was greater for the HE than the NHE (p<0.037) and CON
(p < 0.001) groups. Similarly, BFLH ACSA increased more in the HE group than the NHE (p
= 0.047) and CON groups (p < 0.001). Both exercises induced similar (p > 0.05) increases in
semitendinosus volume and ACSA which were greater than those observed for the CON
group (all p ≤ 0.002). However, only the NHE group exhibited increased BF short head
ACSA, and only the HE group displayed increased semimembranosus volume (p = 0.007)
and ACSA (p = 0.015), compared to the CON group. CONCLUSION: NHE and HE training
both stimulate significant increases in BFLH fascicle length however, HE training may be
more effective for promoting hypertrophy in the BFLH and semimembranosus than the NHE,
which appears to selectively develop the semitendinosus and BF short head. Future studies
should seek to clarify whether HE exercise is effective in reducing hamstring strain injury in
sport.
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7.3 INTRODUCTION
Hamstring ‘tears’ are endemic in sports involving high-speed running and upwards of 80% of
these injuries involve the BFLH (Bourne, Opar DA, Williams, & Shield, In Press; Koulouris,
et al., 2007; Opar, et al., 2014; Verrall, et al., 2003). Hamstring strains represent the most
common injury in athletics (Opar, Drezner, et al., 2013), Australian Rules football (Orchard
& Seward, 2002; Orchard, et al., 2011), and soccer (Ekstrand, et al., 2011b) and as many as
30% reoccur within 12 months (Orchard & Best, 2002). These findings highlight the need for
improved hamstring injury prevention programs while also suggesting the possibility that
these programs should specifically target the BFLH.
There has been significant interest in exploring the patterns of muscle activity in hamstring
exercises (Bourne, et al, 2015; Bourne et al., In review; Mendiguchia, Arcos, et al., 2013a;
Ono, et al., 2011; Ono, et al., 2010; Zebis, et al., 2013), but there is little research examining
the architectural and morphological adaptations of these muscles to different exercise
interventions. The Nordic hamstring exercise (NHE) has proven effective in increasing
eccentric knee flexor strength (Mjolsnes, et al., 2004) and reducing injuries (Arnason, et al.,
2008; Petersen, et al., 2011; van der Horst, et al., 2015) in soccer, although there is
disagreement in the literature as to which hamstring muscles are most active during this
exercise (Bourne, et al, 2015; Bourne, In review; Ditroilo, et al., 2013; Mendiguchia, Arcos,
et al., 2013a). We have previously reported that the NHE preferentially activates the ST
(Bourne, et al, 2015; Bourne, In review), however, we have also observed high levels of BFLH
activity in this exercise (Bourne, In review) which suggests that it may nevertheless provide a
powerful stimulus for adaptation within this most commonly injured muscle (Bourne, et al.,
In press; Koulouris, et al., 2007; Opar, et al., 2014; Verrall, et al., 2003). Eccentric exercise
has been proposed to increase muscle fascicle lengths via sarcomerogenesis (Brockett, et al.,
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2001; Lynn, Talbot, & Morgan, 1998) and Timmins and colleagues (2015) have recently
observed such an adaptation after eccentric knee flexor training on an isokinetic
dynamometer while also noting that concentric training caused fascicle shortening despite
occurring at long muscle lengths. Furthermore, we have recently reported that soccer players
with shorter BFLH fascicles (<10.56cm) were at fourfold greater risk of hamstring strain
injury than players with longer fascicles (Timmins, Bourne, et al., 2015). Given the
effectiveness of the predominantly eccentric NHE in hamstring injury prevention and
rehabilitation (Arnason, et al., 2008; Petersen, et al., 2011; van der Horst, et al., 2015), it is of
interest to examine the impact of this and alternative exercises on BFLH fascicle lengths and
morphology.
We have recently observed that the 45° hip extension (HE) exercise resulted in more uniform
activation of the two-joint hamstrings and greater BFLH activity than the NHE (Bourne, In
review). HE exercises are also performed at longer hamstring lengths than the NHE and it has
been suggested that this may make them more effective in hamstring injury prevention than
the NHE (Guex & Millet, 2013). However, HE and most other hamstring exercises are
typically performed with both eccentric and concentric phases and it remains to be seen how
the combination of contraction modes will affect fascicle length by comparison with an
almost purely eccentric exercise like the NHE. Nevertheless, the greater activation of BFLH
during HE (Bourne, et al, 2015; Bourne, In review) may provide a greater stimulus for
muscle hypertrophy, which might have implications for rehabilitation practices given
observations of persistent atrophy in this muscle following injury (Silder, et al., 2008).
The purpose of this study was to evaluate changes in BFLH architecture and hamstring muscle
volume and anatomical cross-sectional area (ACSA) following 10-week resistance training
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programs consisting exclusively of HE or the NHE. We tested the hypothesis that the HE
exercise would elicit greater increases in BFLH fascicle length than the NHE. Furthermore,
given recent observations (Bourne, In review), we hypothesised that HE training would
stimulate more BFLH hypertrophy than the NHE, while those training with the NHE would
experience more selective hypertrophy of the ST muscle.
7.4 METHODS
Participants
Thirty recreationally active male athletes (age, 22.0 ± 3.6 years, height, 180.4 ± 7 cm, weight,
80.8 ± 11.1 kg) provided written informed consent to participate in this study. Participants
were free from soft tissue and orthopaedic injuries to the trunk, hips and lower limbs and had
no known history of hamstring strain, anterior cruciate ligament or other traumatic knee
injury. Before enrolment in the study, all participants completed a cardiovascular screening
questionnaire (Appendix B) and a standard MRI questionnaire (Appendix C) to ensure it was
safe for them to enter the magnetic field. This study was approved by the Queensland
University of Technology Human Research Ethics Committee and the University of
Queensland Medical Research Ethics Committee.
Study design
This randomised controlled study was conducted between April and June, 2015.
Approximately one week before the intervention commenced, participants underwent MR
and 2D ultrasound imaging of their posterior thighs to determine hamstring muscle size and
BFLH architecture, respectively. After scanning, all participants were familiarised with the
NHE and 45° HE exercise and subsequently underwent strength assessments on each
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exercise. After all of the pre-training assessments had been completed, participants were
allocated to one of three groups: NHE, HE or control (CON). Allocation of participants to
groups was performed using stratified pseudo-random methods on the basis of baseline BFLH
fascicle lengths because this ensured that this parameter did not differ significantly between
groups before the intervention. The NHE and HE groups completed a 10-week progressive
strength training program consisting exclusively of their allocated exercise (Table 1). The
CON group were advised to continue their regular physical activity levels but not to engage
in any resistance training for the lower body. At the beginning of every training session,
participants in both training groups reported their level of perceived soreness in the posterior
thigh using a 1-10 numeric pain rating scale. All CON participants were required to report to
the laboratory at least once per week. For all participants, BFLH architecture was re-assessed
five weeks into the intervention and within 3-5 days of the final training session. MRI scans
were acquired for all participants <7 days after the final training session. Strength testing was
conducted after all imaging had been completed.
Training intervention
Nordic hamstring exercise (NHE)
An illustration of the NHE can be found in Figure 1 (see also video supplement). Participants
knelt on a padded board, with the ankles secured immediately superior to the lateral
malleolus by individual ankle braces which were attached to uniaxial load cells (Figure 1).
The ankle braces and load cells were secured to a pivot which allowed the force generated by
the knee flexors to be measured through the long axis of the load cells. From the initial
kneeling position with their ankles secured in padded yokes, arms on the chest and hips
extended, participants lowered their bodies as slowly as possible to a prone position (Bourne,
et al, 2015). Participants performed only the lowering (eccentric) portion of the exercise and
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were instructed to use their arms and flex at the hips and knees to push back into the starting
position so as to minimise concentric knee flexor activity. When participants developed
sufficient strength to completely stop the movement in the final 10-20⁰ of the range of
motion, they were instructed to hold a weight plate (range = 2.5 kg to 20 kg) to their chest
(centred to the xiphoid process) to ensure the exercise was still of supramaximal intensity.
Hip extension exercise (HE)
Participants were positioned in a 45° hip extension machine (BodySolid, IL, USA) with their
trunk erect and hip joints extended and superior to the level of support pad (Figure 2; see also
video supplement). The ankle of the exercised limb was ‘hooked’ under an ankle pad and the
unexercised limb was allowed to rest above its ankle restraint. Participants held one or more
circular weight plate(s) to the chest (centred to the xiphoid process) and were instructed to
flex their hip until they reached a point approximately 90° from the starting position. Once
participants had reached this position they were instructed to return to the starting position by
extending their hip, while keeping their trunk in a rigid neutral position throughout. Both
limbs were trained in alternating fashion with 30s of rest provided between each set. The load
held to the chest was progressively increased throughout the training period whenever the
prescribed repetitions and sets could be completed with appropriate technique.
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Figure 7-1. (a) The 450 hip extension (HE) exercise and (b) the Nordic hamstring exercise
(NHE), progressive from left to right.
Hamstring training program
Participants in both intervention groups completed a progressive intensity training program
consisting of 20 supervised exercise sessions (two per week) over the 10 week period (Table
1). Each session was followed by at least 48 hours of recovery and participants were
prohibited from engaging in any other resistance training for the lower body. The training
program was based on the approximate loads, repetitions and sets employed in previous
interventions using the NHE (Mjolsnes, et al., 2004; Petersen, et al., 2011; van der Horst, et
al., 2015), although the volume (number of repetitions) was reduced in the final two weeks to
accommodate increases in exercise intensity. All sessions were conducted in the same
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laboratory, employed the same exercise equipment and were supervised by the same
investigators (MNB and SJD) to ensure consistency of procedures.
Table 7-1. Training program variables Week Frequency Sets Repetitions
1 2 2 6
2 2 3 6
3 2 4 8
4 2 4 10
5-8
9
10
2
2
2
5
6
5
8-10
6
5
Strength assessments
Before and <7 days after the intervention, all participants underwent an assessment of their
maximal eccentric knee-flexor strength during three repetitions of the NHE, and their 3-
repetition maximum (3-RM) strength on the 45° hip extension machine. All strength tests
were conducted by the same investigators (MNB, SJD and AJS) with tests completed at
approximately the same time of day before and after the intervention.
Nordic eccentric strength test
The assessment of eccentric knee flexor force using the NHE has been reported previously
(Bourne, et al., In press; Opar, Piatkowski, et al., 2013a; Opar, et al., 2014; Timmins, Bourne,
et al., 2015). Participants completed a single warm-up set of five repetitions followed, one
minute later, by a set of three maximal repetitions of the bilateral NHE. A repetition was
deemed acceptable when the force output reached a distinct peak (indicative of maximal
eccentric strength), followed by a rapid decline when the athlete was no longer able to resist
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the effects of gravity. Eccentric strength was determined for each leg from the peak force
produced during the three repetitions of the NHE and was reported in absolute terms (N).
Hip extension strength test
All strength assessments on the 45° hip extension machine were conducted unilaterally.
Participants initially warmed up by performing 8-10 repetitions on each leg using body
weight only. Subsequently, the loads were progressively increased until investigators
determined the maximal load that could be lifted 3 times.
BFLH architecture assessment
BFLH fascicle length was determined from ultrasound images taken along the longitudinal
axis of the muscle belly utilising a two-dimensional, B-mode ultrasound (frequency, 12Mhz;
depth, 8 cm; field of view, 14 x 47 mm) (GE Healthcare Vivid-i, Wauwatosa, U.S.A).
Participants were positioned prone on a plinth with their hips in neutral and knees fully
extended, while images were acquired from a point midway between the ischial tuberosity
and the knee joint fold, parallel to the presumed orientation of BFLH fascicles. After the
scanning site was determined, the distance of the site from various anatomical landmarks
were recorded to ensure its reproducibility for future testing sessions. These landmarks
included the ischial tuberosity, head of the fibula and the posterior knee joint fold at the mid-
point between BF and ST tendon. On subsequent visits the scanning site was determined and
marked on the skin and then confirmed by replicated landmark distance measures. Images
were obtained from both limbs following at least five minutes of inactivity. To gather
ultrasound images, the linear array ultrasound probe, with a layer of conductive gel was
placed on the skin over the scanning site, aligned longitudinally and perpendicular to the
posterior thigh. Care was taken to ensure minimal pressure was placed on the skin by the
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probe as this may influence the accuracy of the measures (Klimstra, Dowling, Durkin, &
MacDonald, 2007). The orientation of the probe was manipulated slightly by the sonographer
(RGT) if the superficial and intermediate aponeuroses were not parallel.
Ultrasound images were analysed using MicroDicom software (Version 0.7.8, Bulgaria). For
each image, 6 points were digitised as described by Blazevich and colleagues.(Blazevich,
Gill, & Zhou, 2006) Following the digitising process, muscle thickness was defined as the
distance between the superficial and intermediate aponeuroses of the BFLH. A fascicle of
interest was outlined and marked on the image. Fascicle length was determined as the length
of the outlined fascicle between aponeuroses and was reported in absolute terms (cm). As the
entire fascicles were not visible in the probe’s field of view, their lengths were estimated
using the following equation:
FL=sin (AA+90°) x MT/sin(180°-(AA+180°-PA)).
Where FL=fascicle length, AA=aponeurosis angle, MT=muscle thickness and PA=pennation
angle. (Blazevich, et al., 2006; Kellis, Galanis, Natsis, & Kapetanos, 2009)
All images were collected and analysed by the same investigator (RGT) who was blinded to
participant identity and training group allocation. The assessment of BFLH architecture using
the aforementioned procedures by this investigator (RGT) is highly reliable (intraclass
correlations >0.90) (Timmins, Shield, et al., 2014).
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Magnetic resonance imaging
All MRI scans were performed using a 3-Tesla (Siemens TrioTim, Germany) imaging system
with a spinal coil. The participant was positioned supine in the magnet bore with the knees
fully extended and hips in neutral, and straps were placed around both limbs to prevent any
undesired movement. Contiguous T1-weighted axial MR images (transverse relaxation time:
750ms; echo time: 12ms; field of view: 400mm; slice thickness: 10mm; interslice distance:
0mm) were taken of both limbs beginning at the iliac crest and finishing distal to the tibial
condyles. A localiser adjustment (20s) was applied prior to the acquisition of T1-weighted
images to standardise the field of view. In addition, to minimise any inhomogeneity in MR
images caused by dielectric resonances at 3T, a post-processing (B1) filter was applied to all
scans (de Sousa, et al., 2011). The total scan duration was 3min 39sec.
Muscle volumes and anatomical cross-sectional areas (ACSAs) of the BFLH and short head
(BFSH), semitendinosus (ST) and semimembranosus (SM) muscles were determined for both
limbs using manual segmentation. Muscle boundaries were identified and traced on each
image in which the desired structure was present using image analysis software (Sante Dicom
Viewer and Editor, Cornell University) (Figure 2). Volumes were determined for each muscle
by multiplying the summed CSAs (from all the slices containing the muscle of interest) by
the interslice distance (Silder, et al., 2008). ACSA was determined by locating the 10mm
slice with the greatest CSA and averaging this along with the two slices immediately cranial
and caudal (five slices). All traces (pre- and post-training) were completed by the same
investigator (MNB) who was blinded to participant identity and training group in all post-
testing.
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Figure 7-2. T1-weighted image (transverse relaxation time = 750ms; echo time = 12ms, slice
thickness = 10mm), depicting the regions of interest for each hamstring muscle. The right
side of the image corresponds to the participant’s left side as per radiology convention.
BFLH, biceps femoris long head; BFSH, biceps femoris short head; ST, semitendinosus; SM,
semimembranosus.
Statistical analysis
All statistical analyses were performed using SPSS version 22.0.0.1 (IBM Corporation,
Chicago, IL). Where appropriate, data were screened for normal distribution using the
Shapiro-Wilk test and homoscedasticity using Levene’s test. Repeated measures split plot
ANOVAs were used to determine training-induced changes in BFLH architecture, hamstring
muscle volumes and ACSA, and strength, for each group. For the analysis of BFLH
architecture, the within-subject variable was time (baseline, mid-training, post-training) and
the between-subject variable was group (HE, NHE, CON). Because BFLH architecture did not
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differ between limbs (dominant vs non-dominant) at any time point (p>0.05), the left and
right limbs were averaged to provide a single value for each participant. To determine
differences in the percentage change in hamstring muscle volume and ACSA between
groups, the within-subject variable was muscle (BFLH, BFSH, ST, SM) and the between-subject
variable was group (HE, NHE, CON). To explore changes in Nordic and 45° hip extension
strength the within-subject variable was (baseline and post-training) and the between-subject
variable was group (HE, NHE, CON). For all analyses, when a significant main effect was
detected, post hoc independent t tests with Bonferroni corrections were used to determine
which comparisons differed. The mean differences were reported with their 95% confidence
intervals (CIs). Ratings of perceived soreness (NPRS) throughout the training period were
analysed and reported descriptively (mean ± SD) for each group.
Sample size
A priori sample size estimates were based on anticipated differences in BFLH fascicle length
following the training intervention. A sample size of 10 in each group was calculated to
provide sufficient statistical power (80%) to detect an effect size of 1.0 with p < 0.05. Effect
size estimates were based on two previous studies (Potier, Alexander, & Seynnes, 2009;
Timmins, Ruddy, et al., 2015) which reported a 13-34% increase in BFLH fascicle length
following eccentric hamstring training, with an effect size range of 1.1-1.9.
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7.5 RESULTS
No significant differences were observed in age, height or body mass between the three
groups (p>0.05) (Table 2). Compliance rates were excellent for both training groups (HE:
100%; NHE: 99.5%).
Table 7-2. Participant characteristics
Group Age (years) Height (cm) Mass (kg)
HE 23.1±4.1 180±6.3 81.6±9.7
NHE 21.6±3.2 182.8±8.7 85.0±10.9
CON 21.3±3.7 178.5±5.4 75.9±11.8
Biceps femoris long head (BFLH) architecture
A significant group x time interaction effect was observed for fascicle length during the
training period (p < 0.001). Post hoc analyses revealed BFLH fascicle length was significantly
longer in the NHE group at mid- (mean difference = 1.23cm, 95% CI = 0.84 to 1.63cm, p <
0.001) and post-training (mean difference = 2.22cm, 95% CI = 1.74 to 2.69cm, p < 0.001)
compared to baseline (Figure 7-3). The HE group also displayed significantly longer fascicles
at mid- (mean difference = 0.75cm, 95% CI = 0.35 to 1.15cm, p < 0.001) and post-training
(mean difference = 1.33cm, 95% CI = -0.86 to 1.80cm, p < 0.001) than baseline. The CON
group remained unchanged relative to baseline values at all time points (p > 0.05). The NHE
group displayed significantly longer fascicles than the CON group at mid- (mean difference =
1.50cm, 95% CI = 0.58 to 2.41cm, p = 0.001) and post-training (mean difference = 2.40cm,
95% CI = 1.28 to 3.53cm, p < 0.001). The HE group exhibited significantly longer fascicles
than the CON group at mid- (mean difference = 1.14cm, 95% CI = 0.22 to 2.05cm, p = 0.011)
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and post-training (mean difference = 1.63cm, 95% CI = 0.51 to 2.76cm, p = 0.003). No
significant differences were observed between training groups at either baseline, mid- or
post-training points (p>0.05).
Figure 7-3. Biceps femoris long head (BFLH) fascicle lengths before (baseline), during (mid-
training) and after (post-training) the intervention period for the hip extension (HE), Nordic
hamstring exercise (NHE) and control (CON) groups. Fascicle length is expressed in
absolute terms (cm) with error bars depicting standard error (SE). * indicates p<0.05
compared to baseline (week 0). ** signifies p<0.001 compared to baseline. # indicates
p<0.05 compared to the control group.
Hamstring muscle volumes
A significant main effect was detected for the muscle x group interaction for hamstring
muscle volume changes (p < 0.001). HE training stimulated a greater increase in volume for
the ST than the BFSH (mean difference = 5.61%, 95% CI = 1.12% to 10.10%, p = 0.009). No
other significant between-muscle differences were noted for volume changes after HE
training (p > 0.05 for all pairwise comparisons) or in the CON group (p > 0.05). After NHE
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training, the percentage change in volume was greater for the BFSH than the BFLH (mean
difference = 9.56%, 95% CI = 4.30 to 14.80%, p < 0.001) and SM (mean difference =
10.33%, 95% CI = 5.33 to 15.34%, p < 0.001). Similarly, ST volume increased more than
BFLH (mean difference = 15.28%, 95% CI = 10.69 to 19.87%, p < 0.001) and SM (mean
difference = 16.06%, 95% CI = 10.96 to 21.16%, p < 0.001) (Figure 7-4a).
BFLH volume increased significantly more in the HE than the NHE (mean difference =
6.72%, 95% CI = 0.32 to 13.11%, p = 0.037) and CON groups (mean difference = 12.10%,
95% CI = 5.71 to 18.50%, p < 0.001), and no significant difference was observed between the
NHE and CON groups (mean difference = 5.39%, 95% CI = -1.01 to 111.78%, p = 0.122)
(Figure 7-4b). BFSH volume increased more in the HE (mean difference = 8.51%, 95% CI =
0.17 to 16.85%, p = 0.044) and NHE groups (mean difference = 15.29%, 95% CI = 6.95 to
23.63%, p < 0.001) than in the CON group. Both the NHE (mean difference = 21.21%, 95%
CI = 11.55 to 30.88%, p < 0.001) and HE (mean difference = 14.32%, 95% CI = 4.65 to
23.98%, p = 0.002) training groups exhibited a greater increase in ST volume than the CON
group. No significant difference in ST volume change was noted between NHE and HE
groups (mean difference = 6.90%, 95% CI = -2.77 to 16.56%, p = 0.239). The percentage
change in volume for the SM was significantly greater for the HE group than for CON (mean
difference = 8.95%, 95% CI = 2.21 to 115.69%, p = 0.007), while no difference was observed
between the NHE and CON group changes (mean difference = 3.38%, 95% CI = -3.36 to
10.12%, p = 0.636) for this muscle.
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Figure 7-4. Percentage change in volume (cm3) for each hamstring muscle after the
intervention. Values are expressed as a mean percentage change compared to the values at
baseline with error bars representing standard error (SE). (a) Depicts pairwise comparisons
for each muscle and (b) shows pairwise comparisons for each group. For all comparisons, *
indicates p<0.05 and ** signifies that p<0.001. BFLH, biceps femoris long head; BFSH,
biceps femoris short head; ST, semitendinosus; SM, semimembranosus.
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Peak hamstring muscle cross-sectional areas (CSA)
A significant main effect was detected for the muscle x group interaction (p < 0.001). After
HE training, the change in ACSA observed for the ST was significantly greater than the BFLH
(mean difference = 6.46, 95% CI = 0.84 to 12.10%, p = 0.017), BFSH (mean difference =
9.98%, 95% CI = 4.25 to 15.71%, p < 0.001) and SM (mean difference = 6.73%, 95% CI =
1.54 to 11.92%, p = 0.006) (Figure 7-5a). No other pairwise between-muscle differences in
ACSA change were noted after HE training (all p>0.05). After NHE training, the change in
ACSA was greater for BFSH than BFLH (mean difference = 9.30%, 95% CI = 3.47 to 15.12%,
p = 0.001) and SM (mean difference = 9.50%, 95% CI = 4.92 to 14.08, p < 0.001), while ST
ACSA increased more than BFLH (mean difference = 14.14%, 95% CI = 8.52 to 19.76%, p <
0.001) and SM (mean difference = 14.35%, 95% CI = 9.15 to 19.54%, p < 0.001) (Figure 7-
5a).
The percentage change in BFLH ACSA was greater in the HE training group than in the NHE
(mean difference = 5.24%, 95% CI = 0.061 to 10.41, p = 0.047) and CON groups (mean
difference = 8.90%, 95% CI = 3.73 to 14.07%, p < 0.001), while no difference was observed
between the NHE and CON groups (mean difference = 3.67%, 95% CI = -1.51 to 8.84%, p =
0.245) (Figure 7-5b). BFSH ACSA increased significantly more in the NHE than the CON
group (mean difference = 13.26%, 95% CI = 4.98 to 21.54%, p = 0.001), while no difference
was observed between changes exhibited by the HE and CON groups (mean difference =
5.69%, 95% CI = -2.59 to 0.70%, p = 0.273). The percentage change in ST ACSA was
significantly greater in the NHE (mean difference = 17.60%, 95% CI = 7.60 to 27.61%, p <
0.001) and HE (mean difference = 15.16%, 95% CI = 5.15 to 25.17%, p = 0.002) groups than
the CON group, however no significant difference was noted between changes in the NHE
and HE groups (mean difference = 2.4%, 95% CI = -7.57 to 12.45%, p = 1.000). The
percentage increase in SM ACSA was greater in the HE than the CON group (mean
158
difference = 7.19%, 95% CI = 1.21 to 13.18%, p = 0.015), but was not significantly greater in
NHE than CON (mean difference = 2.02%, 95% CI = -3.97 to 8.01%, p = 1.000). No
significant difference in SM ACSA change was noted between the HE and NHE groups
(main difference = 5.17%, 95% CI = -8.2 to 11.16%, p = 0.109) (Figure 7-5b).
159
Figure 7-5. Percentage change in anatomical cross sectional area (ACSA) (cm2) for each
hamstring muscle after the intervention. Values are expressed as a mean percentage change
compared to the values at baseline with error bars representing standard error (SE). (a)
Depicts pairwise comparisons for each muscle and (b) shows pairwise comparisons for each
group. For all comparisons, * indicates p<0.05 and ** signifies that p<0.001. BFLH, biceps
femoris long head; BFSH, biceps femoris short head; ST, semitendinosus; SM,
semimembranosus.
160
Strength
A significant group x time interaction effect was observed for the Nordic eccentric strength
test (p < 0.001) (Figure 7-6). Post hoc t tests demonstrated that the NHE (mean difference =
97.38N, 95% CI = 65.51 to 129.26N, p < 0.001) and HE (mean difference = 110.47N, 95%
CI = 76.87 to 144.07N, p < 0.001) groups were significantly stronger at post-training
compared to baseline while the CON group did not change (mean difference = 8.91N, 95%
CI = -42.51to 24.69N, p = 0.590). No groups differed at baseline (p > 0.461) however at post-
training, the NHE (mean difference = 123.436N, 95% CI = 39.93 to 206.93N, p = 0.003) and
HE (mean difference = 94.27N, 95% CI = 8.60 to 179.94N, p = 0.028) groups were
significantly stronger than the CON group. No significant difference was observed between
training groups at post-training (mean difference = 29.16N, 95% CI = -54.34 to 112.66N, p =
1.000).
161
Figure 7-6. Eccentric knee flexor force measured during the Nordic strength test before
(baseline) and after (post-training) the intervention period for the hip extension (HE), Nordic
hamstring exercise (NHE) and control (CON) groups. Force is reported in absolute terms (N)
with error bars depicting standard error (SE). * indicates p<0.001 compared to baseline
(week 0). # signifies p<0.05 compared to the control group.
A significant group x time interaction effect was also observed for 3-RM strength as assessed
during the 45⁰ HE strength test (p < 0.001) (Figure 7-7). Post hoc analyses demonstrated that
the HE (mean difference = 41.00kg, 95% CI = 35.97 to 46.03kg, p < 0.001) and NHE groups
(mean difference = 26.00kg, 95% CI = 20.97 to 31.03kg, p < 0.001) improved significantly
from baseline whereas the CON group did not change (mean difference = 3.50kg, 95% CI = -
1.53 to 8.53kg, p = 0.165). No groups differed significantly at baseline (p > 0.091) however
at post-training, both the HE (mean difference = 43.50kg, 95% CI = 30.93 to 56.07kg, p <
0.001) and NHE groups (mean difference = 32.0kg, 95% CI = 19.43 to 44.57kg, p < 0.001)
were significantly stronger than CON. No difference was observed between training groups
(mean difference = 11.50kg, 95% CI = -1.07 to 24.07kg, p = 0.082).
162
Figure 7-7. Hip extension three-repetition maximum (3RM) before (baseline) and after (post
training) the intervention period for the hip extension (HE), Nordic hamstring exercise
(NHE) and control (CON) groups. Force is reported in absolute terms (kg) with error bars
depicting standard error (SE). ** indicates p<0.001 compared to baseline (week 0). #
signifies p<0.001 compared to the control group.
163
7.6 DISCUSSION
This study is the first to explore the architectural and morphological adaptations of the
hamstrings in response to different strength training exercises. These data suggest that both
the HE and NHE stimulate significant increases in BFLH fascicle length. However, HE
training appears to elicit more hypertrophy in the BFLH than does the NHE, which
preferentially develops the ST and BFSH muscles. Both exercises resulted in significant
strength increases which were equally evident in the NHE and HE strength tests.
Fascicle lengthening is one possible mechanism by which the NHE (Arnason, et al., 2008;
Petersen, et al., 2011; van der Horst, et al., 2015) and other eccentric or long length hamstring
exercises (Askling, et al., 2014) protect muscles from injury. We have recently shown,
prospectively, that professional soccer players with fascicles <10.56cm were ~4 times more
likely to suffer a hamstring strain than athletes with longer fascicles and that the probability
of injury was reduced by ~74% for every 0.5cm increase in fascicle length (Timmins,
Bourne, et al., 2015). In the current study, participants increased their fascicle lengths from
~10.6cm prior to training, to 12.8 and 12.0cm in the NHE and HE groups, respectively,
which would likely result in significant reductions in hamstring injury risk.
Despite its success in reducing hamstring strain injuries, the adoption of the NHE in elite
European soccer has been reported to be poor with only ~11% of Norwegian premier league
and UEFA teams deemed to have adequately implemented the NHE programs that have
proven effective in randomised controlled trials (Arnason, et al., 2008; Petersen, et al., 2011;
van der Horst, et al., 2015). Some conditioning coaches and researchers (Guex & Millet,
2013) believe that the exercise does not challenge the hamstrings at sufficient lengths to
optimise injury prevention benefits. However, this study shows, for the first time, that the
164
limited excursion of the hamstrings during the NHE does not prevent the exercise from
increasing BFLH fascicle length. Indeed, the exercise resulted in greater fascicle lengthening
than the HE, although the current study lacked the statistical power to distinguish between the
two. Together with observations that long length concentric hamstring training can shorten
muscle fascicles (Timmins, Ruddy, et al., 2015), the current findings are consistent with the
possibility that the combination of concentric and eccentric contractions somewhat dampens
the elongation of BFLH fascicles. The advantage of the NHE may be its almost purely
eccentric or eccentrically-biased nature. Further work is needed to clarify whether
eccentrically-biased or purely eccentric HE exercise may yield greater improvements in BFLH
fascicle length than the combined concentric and eccentric contraction modes used in this
investigation.
Observations of increased fascicle length following eccentric hamstring exercise are largely
consistent with previous literature. For example, Potier and colleagues (Potier, et al., 2009)
reported a 34% increase in BFLH fascicle length following eight weeks of eccentric leg curl
exercise, while Timmins and colleagues (Timmins, Ruddy, et al., 2015) reported a 16%
increase in BFLH fascicle length after six weeks of eccentrically-biased training on an
isokinetic dynamometer (Timmins, Ruddy, et al., 2015), These adaptations most likely result
from the addition of in-series sarcomeres, as has been shown to occur within the rat vastus
intermedius muscle after five days of downhill running (Lynn & Morgan, 1994). It has been
proposed that this increase in serial sarcomeres accounts for both a rightward shift in a
muscle’s force-length relationship (Reeves, et al., 2004), while also reducing its
susceptibility to damage (Brockett, et al., 2001; Lynn, et al., 1998). However, theoretically, it
is also possible that fascicles lengthen as a product of increased tendon or aponeurotic
165
stiffness. Further research is needed to clarify the precise mechanism(s) responsible for these
architectural changes.
To the authors’ knowledge, this is the first study to explore the morphological adaptations of
the hamstrings to different strengthening exercises. These data suggest that the NHE and HE
exercises induce different patterns of hamstring muscle hypertrophy, with the former
preferentially stimulating ST and BFSH growth and the latter resulting in significantly more
hypertrophy of the BFLH and more homogenous growth of all two-joint hamstring muscles.
We have previously noted transient T2 relaxation time changes after 50 repetitions of each of
these exercises that almost exactly fitted this pattern (Bourne, et al., 2016), so it appears that
the acute changes observed via functional MRI match quite well the hypertrophic effects
observed after 10 weeks of training. However, neither muscle volume nor ACSA have been
identified as risk factors for hamstring strain injury, so the exact significance of these
findings is unknown. Indeed, we have previously reported that BFLH muscle thickness
measured via ultrasound is not a risk factor for hamstring injury in elite soccer (Timmins,
Bourne, et al., 2015). Nevertheless, BFLH muscle atrophy has been noted as long as 5-23
months after injury in recreational athletes (Silder, et al., 2008), so unilateral HE exercises
may prove more beneficial than the NHE at redressing this deficit in rehabilitation.
Interestingly, reduced muscle volumes of the ST have been observed 12-72 months after
anterior cruciate ligament injury (Nomura, Kuramochi, & Fukubayashi, 2015) and the results
of the current investigation suggest that the NHE may be valuable in rehabilitation of this
injury. Future intervention studies analogous to those employing the NHE previously
(Arnason, et al., 2008; Gabbe, Branson, & Bennell, 2006; Petersen, et al., 2011; van der
Horst, et al., 2015), should seek to clarify whether HE training is effective in reducing
hamstring strain injuries.
166
Hamstring strengthening is an important component of injury prevention strategies (Guex &
Millet, 2013; Malliaropoulos, et al., 2012; Opar, et al., 2012). Indeed, several large scale
interventions employing the NHE have shown ~65% reductions in hamstring strain injury
rates in soccer (Arnason, et al., 2008; Petersen, et al., 2011; van der Horst, et al., 2015) and
recent prospective findings in elite Australian football (Opar, et al., 2014) and soccer
(Timmins, Bourne, et al., 2015) suggest that eccentric strength improvements like those
reported here and previously (Mjolsnes, et al., 2004) are at least partly responsible for these
protective benefits. For example, elite athletes in these sports who generated less than < 279
N (Australian football) and < 337 N (soccer) of knee flexor force at the ankles during the
NHE strength test were ~4 times more likely to sustain hamstring injuries than stronger
counterparts (Opar, et al., 2014; Timmins, Bourne, et al., 2015). In this study, our recreational
level athletes were able to generate, on average, 460N and 431N after NHE and HE training,
respectively, after 10 weeks of training, making them substantially stronger than these elite
Australian football (Opar, et al., 2014) and soccer players (Timmins, Bourne, et al., 2015).
Significant improvements in 3-RM HE strength were also observed for both training groups,
which suggests that hamstring strengthening, at least in recreationally trained athletes, is not
highly specific to the chosen exercise. While the benefits of high levels of HE strength
remain unclear from the perspective of injury prevention, the observed effects of HE training
on BFLH fascicle lengths and eccentric knee flexor strength suggest the potential for this
exercise to reduce hamstring injury risk and this possibility should be explored in future
investigations.
The authors acknowledge that there are some limitations associated with the current study.
Firstly, muscle architecture was only assessed in the BFLH and it may not be appropriate to
generalise these findings to other knee flexors, given that each hamstring muscle displays
167
unique architectural characteristics (Woodley & Mercer, 2005). Further, the assessment of
fascicle length using two-dimensional ultrasound requires some degree of estimation, because
the entire length of the BFLH is not always visible. While the estimation equation used in this
study has been validated against cadaveric samples (Kellis, et al., 2009), there is still the
potential for error, and future studies employing extended field of view ultrasound methods
may be needed to completely eliminate this. Lastly, all of the athletes in this study were
recreational level males of a similar age, and it remains to be seen if these results are
applicable to other populations. However, our participants were, on average, as strong as elite
Australian football players (Opar, et al., 2014) and stronger than professional soccer players
(Timmins, Bourne, et al., 2015) at the start of the study. Furthermore, our cohort displayed
average fascicle lengths before training that were within one standard deviation of the values
reported in elite soccer players previously (Timmins, Bourne, et al., 2015), so it is unlikely
that they were unrepresentative of higher-level athletes, in these parameters at least.
This is the first study to demonstrate that training with different exercises elicits unique
architectural and morphological adaptations within the hamstring muscle group. We have
provided evidence to suggest that both NHE and HE training are effective in lengthening
BFLH fascicles. However, HE training appears to be more effective for promoting
hypertrophy in the commonly injured BFLH than the NHE, which preferentially develops the
ST and BFSH muscles. These data may help to explain the mechanism(s) by which the NHE
confers injury preventive benefits and also provide compelling evidence to warrant the
further exploration of HE-oriented exercises in hamstring strain injury prevention protocols.
Future prospective studies are needed to ascertain whether HE training interventions are
effective in reducing the incidence of hamstring strain injury in sport and whether or not the
combination of HE and NHE is more effective than the NHE alone.
169
Chapter 8: GENERAL DISCUSSION, LIMITATIONS & CONCLUSION
This program of research aimed to 1) further examine the role of eccentric knee flexor
strength and between-limb imbalances in eccentric strength, in hamstring strain injury (HSI)
occurrence; 2) explore the neuromuscular maladaptations that may manifest following HSI
and underpin high rates of injury recurrence; and 3) characterise the activation patterns and
the architectural and morphological adaptations of the hamstrings to difference strength
training exercises. Study 1 demonstrated that between-limb imbalances in eccentric knee
flexor strength and prior HSI both increased the risk of future strain injury in rugby union
players. Moreover, for those athletes who had been injured previously, their risk of re-injury
was augmented if they had returned to competition with strength imbalances. Study 2
provided novel evidence to suggest that elite athletes with a history of strain injury to the
BFLH have a reduced capacity to activate the previously injured muscle during high-speed
running, for many months following a return to sport. In light of these findings, it was
important to understand how training practices can be improved to redress strength
imbalances and to better target the commonly injured BFLH in prophylactic programs. Study 3
demonstrated that the hamstrings are activated non-uniformly during various strength training
exercises and that hip extension tasks more selectively activate the BFLH than the Nordic
hamstring exercise (NHE), which preferentially recruits the semitendinosus. Study 4 built
upon these findings by exploring the architectural and morphological adaptations of the
hamstrings to 10 weeks of hip extension or NHE training. This study provided evidence to
suggest that both NHE and hip extension training stimulate significant increases in BFLH
fascicle length however, hip extension exercise may be more effective for promoting
hypertrophy in BFLH than the NHE, which selectively develops the semitendinosus muscle.
170
The prospective findings from Study 1 highlight the importance of ameliorating between-
limb imbalances in eccentric strength, particularly following HSI, to reduce the risk of future
injury. It might be expected that these imbalances would be addressed in the rehabilitation
process however, the retrospective findings from Study 2 ((and previous observations
(Bourne, et al, 2015; Opar, Williams, et al., 2013a)), suggest the possibility that conventional
HSI rehabilitation strategies may not be effectively restoring strength and voluntary
activation to the commonly injured BFLH. Indeed, it has been proposed (Fyfe, et al., 2013b)
that these activation deficits may mediate the preferentially eccentric weakness (Opar,
Williams, et al., 2013a), reduced rates of knee flexor torque development (Opar, Williams, et
al., 2013b), BFLH atrophy (Silder, et al., 2008) and reduced fascicle lengths (Timmins, Shield,
et al., 2014) that have been reported in the literature. Further work is required to determine
whether neuromuscular inhibition is the cause or result of prior HSI, and if indeed it
represents a risk factor for injury recurrence.
An improved understanding of the patterns of hamstring muscle activation during common
strength training exercises may enable practitioners to make better informed decisions
regarding exercise selection in injury prevention and rehabilitation programs. Using sEMG
and fMRI, study 3 demonstrated that the commonly employed NHE only moderately
activates the BFLH relative to the semitendinosus muscle. In contrast, hip extension exercise
appeared to most selectively activate the BFLH which suggests that it might provide a more
effective stimulus for stimulating adaptations in this muscle. Study 4 corroborated this
hypothesis by demonstrating that 10 weeks of hip extension training elicited significantly
more hypertrophy to the BFLH than a volume-matched program using the NHE. However,
both exercises promoted significant lengthening of BFLH fascicles, which may help to explain
how the NHE (Arnason, et al., 2008; Petersen, et al., 2011; van der Horst, et al., 2015) and
171
other long-length hamstring exercises (Askling, et al., 2014; Askling, et al., 2013) protect
against hamstring injury. These data also provide compelling evidence to warrant the further
exploration of hip extension exercise in hamstring strain injury prevention protocols.
There are some limitations associated with program of research. With respect to Study 1, the
assessment of eccentric knee-flexor strength and between-limb imbalance was only
performed at a single time point in the pre-season period and it is important to consider that
strength may change throughout the pre-season and in-season periods. Further, given that we
only employed rugby union players, the results may not be generalizable to other sports or
populations. Study 2 was retrospective in nature and it remains to be seen if the observed
activation deficits were the cause or result of the athletes’ prior HSI. Moreover, given the
absence of an uninjured control group, it is difficult to determine whether participants had
normal patterns of muscle activation in their uninjured limbs. The techniques used to assess
voluntary hamstring activation in Study 2 and 3 also have limitations. For example, sEMG is
prone to cross talk (Farina, et al., 2004) and cannot discriminate between closely
approximated segments of muscles (Adams, et al., 1992). Functional MRI largely overcomes
this spatial limitation however the T2 response to an exercise stimulus is highly dynamic and
can be influenced by a range of factors such as the metabolic capacity and vascular dynamics
of the active tissue. With respect to Study 4, the assessment of muscle architecture was only
performed on the BFLH. This was justified on the basis that the BFLH was the most frequently
injured muscle in Study 1, however, the adaptability of muscle architecture in other
hamstring muscles is worthy of future investigation. Further, the assessment of fascicle
length using two-dimensional ultrasound requires some degree of estimation, because the
entire length of the BFLH is not always visible. While the estimation equation used in this
study has been validated against cadaveric samples, (Kellis, et al., 2009) there is still the
172
potential for error, and future studies employing extended field of view ultrasound methods
may be needed to completely eliminate this.
In conclusion, this program of research has provided prospective data on risk factors for HSI
and has retrospectively explored maladaptations which may manifest as a result of injury. In
addition, it has provided novel data on the activation patterns and the architectural and
morphological adaptations of the hamstrings to different strength training exercises. The
findings from studies 1 & 2 highlight the importance of ameliorating strength and voluntary
activation deficits, particularly following HSI, while data from studies 3 & 4 provide an
evidence base from which to form decisions regarding exercise selection in prophylactic
programs.
Bibliography 173
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Appendices 195
Appendices
Appendix A.
Muscle activation patterns in the Nordic hamstring exercise: Impact of prior strain
injury
Publication statement
This appendix is comprised of the following paper which was published in the Scandinavian
Journal of Medicine and Science in Sports during this student’s candidature:
Bourne, M., Opar,DA, Williams,MD, Al Najjar, A, Shield, AJ (2015). Muscle activation
patterns in the Nordic hamstring exercise: Impact of prior strain injury. Scand J Med Sci
Sports. [Epub ahead of print]
Appendices 196
ABSTRACT
This study aimed to determine: 1) the spatial patterns of hamstring activation during the
Nordic hamstring exercise (NHE); 2) whether previously injured hamstrings display
activation deficits during the NHE; and, 3) whether previously injured hamstrings exhibit
altered cross-sectional area. Ten healthy, recreationally active males with a history of
unilateral hamstring strain injury underwent functional magnetic resonance imaging (fMRI)
of their thighs before and after 6 sets of 10 repetitions of the NHE. Transverse (T2) relaxation
times of all hamstring muscles (biceps femoris long head, (BFLH); biceps femoris short head
(BFSH); semitendinosus (ST); semimembranosus (SM)), were measured at rest and
immediately after the NHE and cross-sectional area (CSA) was measured at rest. For the
uninjured limb, the ST’s percentage increase in T2 with exercise was 16.8, 15.8 and 20.2%
greater than the increases exhibited by the BFLH, BFSH and SM, respectively (p<0.002 for
all). Previously injured hamstring muscles (n=10) displayed significantly smaller increases in
T2 post-exercise than the homonymous muscles in the uninjured contralateral limb (mean
difference -7.2%, p=0.001). No muscles displayed significant between limb differences in
CSA. During the NHE, the ST is preferentially activated and previously injured hamstring
muscles display chronic activation deficits compared to uninjured contralateral muscles.
Appendices 197
INTRODUCTION
Hamstring strains are the most prevalent of all injuries in sports that involve high speed
running (Woods et al., 2004; Drezner et al., 2005; Orchard et al., 2006; Brooks et al., 2006a;
Brooks et al., 2006b; Ekstrand et al., 2011) and 80% or more of these insults involve the
biceps femoris muscle (BF) (Verrall et al., 2003; Askling et al., 2007; Koulouris et al., 2007;
Silder et al., 2008). High rates of hamstring muscle strain injury (HSI) recurrence (Heiser et
al., 1984; Woods et al., 2004; Orchard et al., 2006; Brooks et al., 2006b) are also
troublesome, particularly because re-injuries typically result in greater periods of
convalescence than first-time occurrences (Brooks et al., 2006; Ekstrand et al., 2011). These
observations highlight the need for improved hamstring prevention and rehabilitation
practices while also suggesting that these exercise programs should specifically target
(activate) the BF.
The importance of eccentric conditioning in HSI prevention is reasonably well recognised
(Stanton & Purdham., 1989; Brockett et al., 2001; Askling et al., 2013) and intuitively
appealing in light of evidence that hamstring stresses are highest when actively lengthening
in the presumably injurious (Thelen et al., 2005; Schache et al., 2009), terminal swing phase
of sprinting (Schache et al., 2009; Chumanov et al., 2011). The Nordic hamstring exercise
(NHE), the most widely investigated of these eccentric movements, has been reported to
reduce first time (Arnason et al., 2008; Petersen et al., 2011) and recurrent (Petersen et al.,
2011) HSIs in large scale interventions in soccer. Furthermore, rugby union teams employing
the NHE appear to have significantly lower HSI rates than those that do not (Brooks et al.,
2006b). Despite the observed benefits of the NHE in reducing injury risk, relatively little is
known about the patterns of hamstring muscle activation during this task. One study has
reported a non-uniform pattern of hamstring activation during the NHE in male soccer
Appendices 198
referees (Mendiguchia et al., 2013). However, there is a need to extend these observations,
particularly to athletes with a history of HSI, given the prominent role of the NHE in
prevention and rehabilitation programs.
Fyfe et al. (2013) have recently proposed that the high rates of HSI recurrence might be
partly explained by chronic neuromuscular inhibition which results in a reduced capacity to
voluntarily activate the BF muscle during eccentric but not concentric knee flexor efforts
(Opar et al., 2013a; Opar et al., 2013b). These contraction mode-specific deficits in BF
activation can persist despite rehabilitation and return to sport and may mediate preferentially
eccentric hamstring weakness (Jonhagen et al., 1994; Croisier et al., 2000; Croisier et al.,
2002), reduced rates of knee flexor torque development (Opar et al., 2013b) and persistent BF
long head (BFLH) atrophy (Silder et al., 2008), all of which have been observed months to
years after HSI. It has been proposed that reduced activation of the BF during active
lengthening may diminish the stimuli that would otherwise promote adaptation to the
demands of running and strength exercises employed in rehabilitation and training (Opar et
al., 2012; Fyfe et al., 2013). However, the aforementioned activation deficits have only been
noted during eccentric isokinetic tasks and it remains to be seen whether they also exist
during the performance of exercises like the NHE.
Further insight into muscle activation patterns during the NHE in uninjured and previously
injured muscles will be critical in better understanding how this exercise confers HSI-
preventative benefits. Functional magnetic resonance imaging (fMRI) allows for assessment
of muscle size and this technique is also increasingly employed to investigate muscle
activation patterns during exercise (Akima et al., 1999; Mendiguchia et al., 2013; Ono et al.,
2011). Functional MRI enables the measurement of T2 relaxation times of imaged skeletal
Appendices 199
muscles and these values, increase in proportion with exercise intensity (Fleckenstein et al.,
1988) and in parallel with electromyographic measures of muscle activation (Adams et al.,
1992). Fortunately, the changes in T2 relaxation times last for 20-30 minutes after intense
physical activity (Patten et al., 2003) so post-exercise fMRI scans can reveal the extent to
which muscles have been activated even after exercise ceases. In addition, because T2
relaxation times are mapped out across cross-sectional images of muscles, fMRI is able to
determine differences in activation within and between muscles and this excellent spatial
resolution overcomes several limitations of surface electromyography (sEMG) (Adams et al.,
1992).
The purpose of this study was to use fMRI to determine: 1) the spatial patterns of hamstring
activation during the NHE; 2) whether previously injured hamstrings display activation
deficits compared to homonymous muscles in the uninjured limb during the NHE; and, 3)
whether previously injured hamstrings exhibit reduced cross sectional areas (CSAs)
compared to homonymous muscles in the uninjured limb. We hypothesised that the
hamstrings of uninjured limbs would be activated non-uniformly during the NHE and that
previously injured hamstring muscles would display reduced activation and reduced CSA,
compared to homonymous muscles in the uninjured limb.
METHODS
Experimental Design
This study used a cross-sectional design in which all participants visited the laboratory on
two occasions. During the first, participants were familiarised with the NHE and had baseline
anthropometric measures taken. Experimental testing, completed at least seven days later,
involved the performance of a NHE session with pre- and post-exercise fMRI scans to
Appendices 200
compare the extent of hamstring muscle activation during the NHE and to assess hamstring
muscle CSA between limbs.
Participants
Ten healthy and recreationally active males, aged 18-25 (age, 21.6 ± 1.9 years; height, 180.1
± 7.4 cm; weight, 81.3 ± 6.5 kg) with a history of unilateral HSI within the previous 24
months were recruited. A sample size of 10 was calculated to provide sufficient statistical
power (≥0.80) to avoid a type II error given a presumed effect size of 1.0 for the differences
in exercise induced T2 relaxation time changes between muscles of the same limb and
between homonymous muscles in opposite limbs when p<0.05. Since this investigation was
the first to explore between limb differences in T2 relaxation times following a HSI, the
effect size was estimated based on a previous fMRI study (Ono et al., 2010) that reported an
approximate change (mean ± standard deviation) in T2 of 42±4% in ST, 7±1% in SM and
11±6% in BFLH following eccentric knee flexor exercise using 120% of the 1-repetition
maximum load. Participants completed an injury history questionnaire with reference to
clinical notes provided by their physical therapist which detailed the location, grade and
rehabilitation period of their most recent HSI as well as the total number of HSIs that they
had sustained. Participants had all returned to full training and competition schedules, were
free of orthopaedic abnormalities of the lower limbs and had no history of neurological or
motor disorders. All completed a cardiovascular risk factor questionnaire prior to testing.
Additionally, all participants completed a standardised MRI screening questionnaire provided
by the imaging facility to ensure that it was safe for them to undergo scanning. Participants
were instructed to avoid strength training of the lower body and to abstain from anti-
inflammatory medications for the week preceding experimental testing. This study was
Appendices 201
approved by the Queensland University of Technology Human Research Ethics Committee
and the University of Queensland Human Ethics Committee.
Familiarisation Session
A familiarisation session was conducted approximately 8 days (±1 day) before experimental
testing. Upon arrival at the laboratory, the participant’s height and mass were recorded before
they received a demonstration and instructions on the performance of the NHE. From the
initial kneeling position with their ankles secured in padded yokes, arms crossed on the chest
and hips extended, participants were instructed to lower their bodies as slowly as possible to a
prone position (Figure 1). Participants performed only the lowering (eccentric) portion of the
exercise and after ‘catching their fall’, were instructed to use their arms to push back into the
starting position so as to minimise concentric knee flexor activity. Verbal feedback was
provided to correct any technique faults while participants completed several practice
repetitions (typically three sets of six repetitions).
Figure 1. The Nordic hamstring exercise, progressing from left to right.
Experimental Session
Nordic hamstring exercise protocol
Appendices 202
Each participant completed 6 sets of 10 repetitions of the NHE with 1-minute rest intervals
between sets. During the 1min rest, the participant lay in the prone position. Investigators
verbally encouraged maximal effort throughout each repetition. Participants were returned to
the scanner immediately (<15s) following the exercise protocol and post-exercise T2-
weighted scans began within 90 ± 16s (mean ± SD) following localiser adjustments.
Functional magnetic resonance imaging
All fMRI scans were performed using a Siemens 3-Tesla (3T) TrioTim imaging system with
a spinal coil. The participant was positioned supine in the magnet bore with the knees fully
extended and hips in neutral, while contiguous MR images were taken of both limbs,
beginning immediately superior to the iliac crest and finishing immediately distal to the tibial
plateau. Transaxial T2-weighted images were acquired before and immediately after the NHE
protocol using a CPMG spin-echo pulse sequence (transverse relaxation time = 2000ms; echo
time = 10, 20, 30, 40, 50 and 60ms; number of excitations = 1; slice thickness = 10mm;
interslice gap = 10mm). All T2-weighted images were collected using a 180 x 256 image
matrix and a 400 x 281.3mm field of view. T1-weighted axial spin-echo images were also
obtained but only during the pre-exercise scan (transverse relaxation time = 1180ms; echo
time = 12ms; field of view = 400 x 281.3 mm; number of excitations = 1; slice thickness =
10mm; interslice gap = 10mm). The total acquisition time for pre-exercise images was 15min
10s and for post-exercise images, 10min. Given the high field strength of 3T, a B1 filter was
applied to minimise any inhomogeneity in MR images caused by dielectric resonances (De
Souza, 2011). Further, to minimise the effects of intramuscular fluid shifts before the pre-
exercise scans, the participant was seated for a minimum of 15 minutes before data
acquisition.
Appendices 203
Data analysis
All T1- and T2-weighted fMR images were transferred to a personal computer in the DICOM
file format and image analysis software (Sante Dicom Viewer and Editor, Cornell University)
was used for subsequent analysis. To evaluate the degree of muscle activation during the
NHE protocol, the T2 relaxation times of each hamstring muscle were measured before and
immediately after exercise for both the previously injured and uninjured contralateral limb.
To quantify T2 relaxation times, the signal intensity of each hamstring muscle (BFLH, BFSH,
SM and ST) was measured using a 5 mm² region of interest (ROI) in three slices
corresponding to 40%, 50% and 60% respectively, of the distance between the inferior
margin of the ischial tuberosity (0%) and the superior border of the tibial plateau (100%)
(Ono et al., 2010). For BFSH, a single 5mm² ROI was selected at 50% of thigh length because
it was not always possible to identify this muscle in more cranial or caudal slices. All ROIs
were selected in the centre of the muscle belly with great care taken to avoid scar and
connective tissue, fatty deposits, aponeurosis, tendon, bone and blood vessels. The signal
intensity reflected the mean value of all pixels within the ROI and was determined for each
ROI across six echo times (10, 20, 30, 40, 50 and 60ms). The signal intensity at each echo
time was then graphed to a mono-exponential time curve using a least squares algorithm
[(SI= M exp(echo time / T2), where SI is the signal intensity at a specific echo time, and M
represents the pre-exercise fMRI signal intensity] to extrapolate the T2 relaxation times for
each ROI. The absolute T2 relaxation times at all three thigh levels (40%, 50% and 60%)
were averaged to provide a mean T2 value for each muscle (BFLH, BFSH, ST, SM) before and
after exercise. To assess muscle activation during the NHE protocol, the averaged post-
exercise T2 value for each muscle was expressed as a percentage change relative to the pre-
exercise value (Fleckenstein et al., 1988; Ono et al., 2011). Muscle cross-sectional area
obtained from pre-exercise T1-weighted images was analysed to determine differences in
Appendices 204
hamstring muscle CSA in limbs with and without a history of HSI. The muscle boundaries of
BFLH, SM and ST were identified and traced manually at slices 40%, 50% and 60% of the
distance between the inferior margin of the ischial tuberosity (0%) and superior border of the
tibial plateau (100%) (Ono et al., 2010) while BFSH was only traced at 50% of thigh length
for reasons described previously. Muscle CSA was calculated as the total number of cm2
within each trace and was averaged across the three slices to provide a mean value for each
muscle. The averaged CSA of previously injured muscles was compared with homonymous
muscles in the uninjured contralateral limb to evaluate between-limb differences following an
HSI.
Statistical Analysis
To determine the spatial activation patterns in healthy (uninjured) limbs, a repeated measures
design linear mixed model fitted with the restricted maximum likelihood (REML) method
was used. Exercise-induced percentage changes in T2 relaxation times were compared for
each hamstring muscle in the 10 limbs without prior HSI. Muscle (BFLH, BFSH, ST or SM)
was the fixed factor with participant as a random factor. When a significant main effect was
detected, Bonferroni corrections were used for post-hoc testing and reported as mean
difference with 95% CIs.
The between-limb analyses of muscle activation and CSA were carried out on all participants.
Paired t-tests were used to compare exercise-induced percentage changes in T2 relaxation
times and pre-exercise muscle CSA’s of the 10 previously injured muscles (7 BFLH, 2 ST, 1
SM) to the homonymous muscles in the uninjured limbs. For these analyses, T2 relaxation
times and CSA were reported as uninjured limb versus injured limb mean differences both
with 95% CIs. Bonferroni corrections were again used for post-hoc testing and significance
Appendices 205
was set at p<0.05. Finally, given the possibility that changes in activation patterns and CSA
after injury may be muscle-specific, the between-limb analyses (injured v uninjured) were
repeated using only the seven participants who had injured their biceps femoris muscles.
RESULTS
Participant injury histories
All participants had a history of unilateral HSI within the previous 24 months, with an
average time of 9.8 months (± 8.7 months) since the last insult. At the time of injury, all
participants had their HSI diagnosis confirmed with MRI (n=7) or ultrasound (n=3). The
details of all participants HSI histories can be found in Table 1.
Table 1. Hamstring strain injury (HSI) details of all participants (n=10).
Participant Injured
Limb
Dominant
Limb
Location Number
of HSIs
Months
since last
HSI
Grade of
last HSI
(1-3)
Rehabilitation
period (wks)
1 Right Yes ST 1 5 2 8
2 Left No BFlh 4 24 2 6
3 Right Yes BFlh 1 3 2 8
4 Right Yes BFlh 2 12 2 32
5 Right Yes BFlh 1 21 2 24
6 Left No ST 2 24 2 24
7 Left No BFlh 1 6 2 10
8 Right Yes BFlh 1 3 2 8
9 Right Yes SM 2 3 2-3 8
10 Right Yes BFlh 5 12 2 8
Appendices 206
Spatial activation of the uninjured limb following the NHE
In the uninjured limbs, there was a significant main effect for muscle with respect to exercise-
induced T2 changes following the NHE protocol (p<0.001). Post-hoc tests revealed that the
T2 changes induced by exercise within the ST were significantly larger than those observed
for the BFLH (ST vs. BFLH mean difference = 16.8%, 95% CI = 7.1 to 26.4%, p=0.001), BFSH
(ST vs. BFSH mean difference = 15.8%, CI = 6.1 to 25.4%, p=0.002) and SM (ST vs. SM
mean difference = 20.2%, 95% CI = 10.6 to 29.9%, p<0.001) (Figure 2). All other between-
muscle comparisons in the percentage change of T2 relaxation times were small and non-
significant (BFLH vs. BFSH, mean difference = 1.0%, 95% CI = -8.7 to 10.6%, p=0.834; BFLH
vs. SM, mean difference = 3.4%, 95% CI = -6.2 to 13.1%, p=0.467; BFSH vs. SM, mean
difference = 4.5%, 95% CI = -5.2 to 14.1%, p=0.351).
Appendices 207
Figure 2. Percentage change in functional MRI T2 relaxation times of each hamstring muscle
for all 10 uninjured limbs. Values are expressed as a percentage change compared to the
values at rest. * indicates p<0.05 when compared to ST with the error bars displaying
standard deviation. BFLH, biceps femoris long head; BFSH, biceps femoris short head; ST,
semitendinosus; SM, semimembranosus.
Between-limb comparisons of muscle activation in previously injured hamstring
muscles
The 10 previously injured hamstring muscles displayed a significantly lower percentage
increase in T2 relaxation time (mean difference = -7.2%, 95% CI = -3.8 to -10.7%, p=0.001)
(Figure 3) after the NHE than the uninjured homonymous muscles in the contralateral limbs.
Appendices 208
Figure 3. Percentage change in fMRI T2 relaxation times of each hamstring muscle for both
the previously injured (inj) and uninjured (uninj) limbs. Values are expressed as a percentage
change compared to the values at rest. * indicates p<0.05 when compared to ST with the error
bars displaying standard deviation. BFLH, biceps femoris long head; BFSH, biceps femoris
short head; ST, semitendinosus; SM, semimembranosus.
Between-limb comparison of hamstring muscle cross-sectional area
There were no statistically significant between-limb differences in CSA between the 10
homonymous muscles in the previously injured and uninjured limbs (mean difference = -
0.29cm2, CI = 1.21 to -1.80cm2, p=0.670 (Figure 4).
Figure 4. CSA (cm2) of each hamstring muscle (BFLH, biceps femoris long head; BFSH,
biceps femoris short head; ST, semitendinosus; SM, semimembranosus) for both the
Appendices 209
previously injured (Inj) and uninjured (Uninj) contralateral limbs. Values are expressed as
means and p<0.05 for all paired comparisons. Error bars depict standard deviation.
When only BFLH injuries were considered (n=7), the previously injured BFLH’s displayed a
significantly lower percentage increase in T2 relaxation time (mean difference = -7.9%, 95%
CI = -3.0 to -12.9%, p=0.008) after the NHE than the contralateral uninjured BFLH. However,
no additional significant between-limb differences were observed for the other muscles (BFSH
mean difference = -0.6%, 95% CI = -7.0 to 5.8, p=0.837; ST mean difference = 4.7%, 95%
CI = - 6.1 to 15.6, p=0.382; SM mean difference = 2.7%, 95% CI = -3.7 to 9.1, p=0.400).
Previously injured BFLH muscles did not display any significant deficits in CSA when
compared to uninjured contralateral BFLH muscles (mean difference = -0.26cm2, CI = -2.52 to
1.99cm2, p=0.785).
DISCUSSION
The results of this study suggest that in healthy, uninjured limbs, the ST is activated
significantly more than other hamstring muscles during the NHE. Furthermore, previously
injured hamstring muscles are activated less completely than the homonymous uninjured
muscles in the opposite limbs, although these activation deficits are not associated with any
significant differences in muscle CSA.
Selective recruitment of ST during the NHE is an interesting finding. Maximum force-
generating capacity of skeletal muscle is dependent on its physiological CSA (Lieber et al.,
2000), and as such, pennate muscles are generally stronger than fusiform muscles.
Nonetheless, the results of this study suggest that ST, which is long, thin and fusiform
(Woodley & Mercer., 2005), is more active during the NHE than BFLH and SM, which are
Appendices 210
bulkier pennate muscles. These findings are consistent with a recent fMRI investigation of
the NHE (Mendiguchia et al., 2013) which reported a greater percentage change in T2 for ST
(14-20%) than for BFLH (6-7%) and non-significant changes in the SM. Interestingly,
Mendiguchia and colleagues (2013) also reported a significant T2 increase in the distal BFSH
which remained elevated for 72 hours however, it is important to consider that this delayed
increase in T2 is representative of muscle damage and sites of preferential damage may not
reflect sites of preferential activation (Bourne et al., 2013). In contrast to the current
investigation, recent work employing sEMG in female athletes reported no significant
difference in the extent to which BFLH and ST muscles were activated during the NHE (Zebis
et al., 2013). However, sEMG is prone to cross-talk from neighbouring muscles (Adams et
al., 1992) and this may account to some extent for the divergent results.
While the mechanism for selective recruitment of ST during the NHE remains unclear, it is
possible that differences between hamstring muscle moment arms play a role. At the knee, ST
has a larger sagittal plane moment arm than BF and SM (Thelen et al., 2005) and it
consequently possesses the greatest mechanical advantage which may explain its preferential
recruitment during movements at this joint. Indeed, preferential ST recruitment has
previously been observed during eccentric knee flexor exercise using a leg curl machine (Ono
et al., 2010) so this strategy appears to be characteristic of hamstring recruitment associated
with knee movements when the hip joint angle is fixed. These observations suggest the
possibility that the NHE, with its modest activation of BFLH in comparison to ST, may not be
the optimal exercise for the prevention of running related strain injury. However, despite this
possibility, some large-scale intervention studies have shown that the NHE is effective in
reducing first time and recurrent HSIs (Arnason et al., 2008; Petersen et al., 2011; Van der
Horst et al., 2014). These benefits may be mediated via improvements in eccentric knee
Appendices 211
flexor strength (Mjølsnes et al., 2004) and/or a shift of the hamstring torque-joint angle
relationship to longer muscle lengths (Brockett et al., 2001). It is possible that even a
relatively mild training stimulus is sufficient to protect the BFLH from strain injury or that
activation of this muscle progressively increases with regular training and the progressive
overload that has been employed in effective intervention programs (Arnason et al., 2008;
Petersen et al., 2011). Increased muscle use has previously been observed, via fMRI, after
two weeks of knee extensor (Akima et al., 1999) and 12 weeks of neck extensor training
(Conley et al., 1997), so it is reasonable to expect that several weeks of NHE training would
result in athletes activating the BF and SM muscles more completely than we have observed
here. Another possibility is that NHE interventions do preferentially stimulate ST adaptations
and that the BFLH is effectively protected in running by an enhanced load bearing capacity of
its agonist. Nevertheless, there is evidence that BFLH is more selectively activated in the stiff
leg deadlift exercise (Ono et al., 2011) so further exploration of the injury prevention benefits
of this and other hip-oriented hamstring exercises is warranted.
Observations of reduced hamstring activation during the NHE after strain injury are
consistent with other findings. Opar et al. (2013a) recently reported inhibition of previously
injured BF muscles during eccentric knee flexor contractions using surface electromyography
and isokinetic dynamometry. However, by assessing hamstring activation during the NHE,
the present findings have more direct implications for conventional rehabilitation practices.
Importantly, these activation deficits persist despite apparently successful rehabilitation and a
return to pre-injury levels of training and match play, which corroborates previous work
(Opar et al., 2013a).
Appendices 212
The existence of reduced voluntary activation in previously injured hamstring muscles
suggests the possibility of a muscle- and possibly contraction mode-specific tension-limiting
mechanism(s) at one or more levels of the central nervous system. Neuromuscular inhibition,
evident in the form of reduced strength and voluntary activation of surrounding skeletal
muscles has been shown to occur after a range of musculoskeletal injuries including anterior
cruciate ligament rupture (Urbach et al., 2001) and ankle fractures (Stevens et al., 2006).
Recently, it has been suggested that the acute pain associated with a HSI may result in
chronic neural inhibition that may compromise hamstring rehabilitation (Fyfe et al., 2013).
Short-lasting inhibition constitutes a well-accepted protective strategy to minimise discomfort
and preserve the injured structures from further damage (Hodges et al., 2010; Opar et al.,
2012). However, activation deficits that persist throughout rehabilitation would reduce the
injured muscle’s loading, particularly during eccentric contractions and this may compromise
hypertrophy and sarcomerogenesis (Timmins et al., 2014; Brockett et al., 2001), both of
which are thought to be important in allowing muscles to adapt to the demands of sprinting.
Evidence of persistent inhibition, many months after conventional rehabilitation and a full
return to training and competition also suggests that inadequate attention has been paid to
increasing voluntary activation of the previously injured muscle (Fyfe et al., 2013). Heavy
resistance training offers a practical and potent stimulus for improving voluntary activation of
skeletal muscle (Akima et al., 1999; Conley et al., 1997). However, in light of recent
evidence (Mendiguchia et al., 2013; Ono et al., 2010; Zebis et al., 2013) that different
exercises target different portions of the hamstring muscle group, it is possible that some
exercises employed in rehabilitation do not optimally target the injured muscle. An improved
understanding of the spatial patterns of hamstring muscle activation during different exercises
may help practitioners to better tailor rehabilitation programs to the site of injury and should
be a focus of future investigations.
Appendices 213
Despite the presence of activation deficits, the current study found no evidence of atrophy in
previously injured hamstring muscles. These findings differ from an earlier investigation that
reported chronic atrophy of previously injured BFLH muscles and compensatory hypertrophy
of the ipsilateral BFSH 5-23 months following an HSI in recreational athletes (Silder et al.,
2008). However, subsequent work from the same group found no evidence of atrophy six
months after completion of standardised hamstring rehabilitation (Sanfilippo et al., 2013) and
this suggests that different rehabilitation and training practices might at least partially explain
the disparate results. Methodological differences between the current study and that of
previous work may also explain some of the discrepancies. The current investigation assessed
hamstring muscle CSA at 40, 50 and 60% of thigh length, whereas previous investigations
(Silder et al., 2008; Sanfilippo et al., 2013) assessed the volume of each hamstring muscle-
tendon unit. Timmins and colleagues (2014) recently reported that ultrasound measures of
biceps femoris muscle architecture revealed significantly shorter fascicles coupled with
greater pennation angles and no significant differences in muscle thickness between
previously injured muscles and uninjured homonymous muscles in the opposite limb. This
increase in pennation angle would tend to counter any effects of muscle atrophy on measures
of muscle thickness, so measures of cross-section or thickness may not be as sensitive to
atrophy as are measures of muscle volume.
Participants in this study had received their injuries in the 3 to 24 months prior to being tested
so it might be argued that this group is not particularly homogenous in terms of stage of
recovery. However, when the activation deficits on the injured limbs were plotted against
time since injury, no relationship was observed (R2= 0.03) and all participants had resumed
full training and competition schedules. Furthermore, there are numerous reports in the
literature suggesting that the deficits in eccentric hamstring strength (Jonhagen et al., 1994;
Appendices 214
Croisier et al., 2002; Lee et al., 2009) and muscle volume (Silder et al., 2008) persist long
after strain injury. For example, Lee and colleagues (2009) reported deficits in eccentric knee
flexor performance in a group of athletes with an average time since injury of 19 ± 12.5
months. Furthermore, Silder et al. (2008) provided evidence of BFLH atrophy 5-23 months
following injury. These observations are consistent with an argument that some effects of
hamstring strain are particularly persistent (Fyfe et al., 2013).
It should be acknowledged that some limitations are present in the current study. Firstly,
because of the retrospective design, we do not know whether activation deficits in previously
injured hamstring muscles are the cause or the result of prior HSI. Furthermore, given the
absence of a control group with no history of HSI in either limb, it is not possible to know
with certainty whether the participants in this study have normal patterns of muscle activation
in their uninjured legs. However, similar preferential recruitment of ST has been reported
during the NHE (Mendiguchia et al., 2013) and during eccentric knee flexor exercise (Ono et
al., 2010) so this pattern of activation is likely to be a robust phenomenon. Finally, it is
important to consider that T2 changes are multifactorial and can be influenced by
confounding factors such as the metabolic capacity and vascular dynamics of the active tissue
(Patten et al., 2003). Such factors have been proposed to account for the high variability in
exercise-induced T2 changes between individuals (Patten et al., 2003). To minimise this
effect we recruited a homogenous male population with limited ranges in age and levels of
physical activity. Furthermore, participants were instructed to avoid strength training of the
lower body and to abstain from anti-inflammatory medications for the week preceding
experimental testing.
Appendices 215
Conclusion
The current study provides novel insight into the spatial activation patterns of the hamstring
muscles during the NHE and how these are altered by prior strain injury. We have provided
evidence that ST is selectively activated during the NHE and that previously injured
hamstring muscles are less active compared to uninjured homonymous muscles in the
contralateral limb. However, these activation deficits are not associated with any significant
between-limb differences in muscle CSA. The sub-optimal activation of the BFLH during the
NHE may suggest the need to investigate the protective effects of alternative hamstring
exercises for the prevention of running related HSI. Furthermore, the observation of
persistent activation deficits in previously injured hamstring muscles suggests that
conventional rehabilitation practices are not addressing the mechanism(s) underpinning
neuromuscular inhibition following HSI (Fyfe et al., 2013). These findings provide evidence
for altered muscle use during eccentric hamstring exercise which should be a focus of future
investigations.
Perspective
This study demonstrated that during the performance of the NHE, the ST muscle is activated
significantly more than the BF and SM. This may have implications for the use of this
exercise in HSI prevention protocols given that the vast majority of HSIs involve the BF as
the primary site of injury (Verrall et al., 2003; Askling et al., 2007; Koulouris et al., 2007;
Silder et al., 2008). Furthermore, previously injured hamstring muscles were activated
significantly less than uninjured contralateral muscles during the NHE, in the absence of
diminished cross-sectional areas and despite apparently successful rehabilitation and a return
to full training and competition. From a practical point of view, these activation deficits may
compromise the rehabilitation process and would likely render the athlete weaker,
Appendices 216
particularly during eccentric contractions, following a return to sport. Future work should
seek to clarify whether these activation deficits are a risk factor for hamstring strain re-injury.
Acknowledgements
We thank the Queensland Academy of Sport’s Centre of Excellence for Applied Sport
Science Research, for funding this investigation. The authors also acknowledge the facilities,
and the scientific and technical assistance of the National Imaging Facility at the Centre for
Advanced Imaging, University of Queensland.
Appendices 217
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Appendices 221
Appendix B. Cardiovascular & Injury History Questionnaires
CARDIOVASCULAR RISK FACTOR QUESTIONNAIRE
To be eligible to participate in the experiment you are required to complete the following questionnaire which is designed to assess the risk of you experiencing any harm during the course of the study. A full and honest disclosure of your medical history is vital for your own safety. Name: ________________________________________________Date of Birth: ______________ Age: __________years Weight: __________kg Height: __________cm Give a brief description of your average weekly activity pattern: Please tick / answer the appropriate responses for the following questions: 1. Are you overweight? Yes No
Don’t Know
2. Do you smoke? Yes No Don’t Know
3. Does your family have a history of premature (<70 years) cardiovascular problems (eg. heart attack, stroke)? Yes No Don’t Know
4. Are you asthmatic? Yes No Don’t Know
5. Are you diabetic? Yes No Don’t Know
6. Do you have high blood cholesterol levels? Yes No Don’t Know
7. Do you have high blood pressure? Yes No Don’t Know
Appendices 222
8. Do you have low blood pressure? Yes No Don’t Know
9. Do you have a heart murmur Yes No Don’t Know
10. Do you have, or have you ever had, any blood-clots in any of your blood vessels (eg. deep-vein thrombosis)? Yes No Don’t Know
11. Do you have, or have you ever had, any tendency to bleed for long periods after cutting yourself? Yes No Don’t Know
12. Are you currently using any medication Yes No
If so, what is the medication?
13. Have you ever experienced any of the following during exertion (exercise or physical labour) or at rest?
Light headedness or dizziness
Pain in the chest, neck, jaw or arm
Numbness or pins-and-needles in any part of your body
Loss of consciousness
14. Do you think you have any medical complaint or any other reason which you know of that may prevent you from safely participating in intense exercise?
Yes No
If yes, please elaborate.
I, ________________________________________________, believe that the answers to these
questions are true and correct.
Signed: ________________________________________________ Date: ________________________
Appendices 223
INJURY QUESTIONNAIRE
Section 1: Participant details Participant ID: __________________ Date of birth: ________________ Sport: ________________________ Level: ______________________ 1a) Which is your preferred foot (i.e. to kick with)?
Left Right Both 1b) For how long have you played your chosen sport? __________years 1c) On average how many hours per week do you train:
On your own: __________hours per week With the team (if appropriate): __________hours per week
Section 2: Hamstring injury particulars
Note: Please fill out a section for each hamstring injury suffered in chronological order, from the first injury suffered to the most recent.
First Hamstring Injury 2a) What date did this hamstring injury occur? _____ / _____ / _____ 2b) What were you doing when the injury occurred?
Sprinting Kicking Picking up the ball Other
If other, please specify: ____________________________________________________________
2c) Were you: Training on your own Training with the team Competing 2d) On which leg did the injury occur? Left Right 2e) Who diagnosed this injury?
Doctor Physiotherapist Other
If other, please specify: ____________________________________________________________ 2f) Were any imaging investigations performed on this injury?
Appendices 224
MRI Ultrasound Other
If other, please specify: ____________________________________________________________ 2g) What was the severity of the strain?
Grade I Grade II Grade III Unsure Section 3: Rehabilitation particulars First Hamstring Injury 3a) Did you have any scheduled rehabilitation for this injury?
Yes No 3b) Who prescribed your rehabilitation?
Rehabilitation/conditioning coach Physiotherapist Other
If other, please specify: ____________________________________________________________ 3c) What was the length of your rehabilitation (the time taken to resume full competition
following injury)?
3d) Describe in as much detail as possible the type of rehabilitation employed:
For those who have suffered only one hamstring this is the end of the questionnaire. When more than one hamstring injury has occurred please continue to complete this questionnaire for the relevant number of hamstring strains you have had.
Appendices 225
Second Hamstring Injury 2a) What date did this hamstring injury occur? _____ / _____ / _____ 2b) What were you doing when the injury occurred?
Sprinting Kicking Picking up the ball Other
If other, please specify: ____________________________________________________________
2c) Were you: Training on your own Training with the team Competing 2d) On which leg did the injury occur? Left Right 2e) Who diagnosed this injury?
Doctor Physiotherapist Other
If other, please specify: ____________________________________________________________ 2f) Were any imaging investigations performed on this injury?
MRI Ultrasound Other
If other, please specify: ____________________________________________________________ 2g) What was the severity of the strain?
Grade I Grade II Grade III Unsure Rehabilitation Particulars 3a) Did you have any scheduled rehabilitation for this injury?
Yes No 3b) Who prescribed your rehabilitation?
Rehabilitation/conditioning coach Physiotherapist Other
If other, please specify: ____________________________________________________________ 3c) What was the length of your rehabilitation (the time taken to resume full competition
following injury)?
3d) Describe in as much detail as possible the type of rehabilitation employed:
Appendices 226
Third Hamstring Injury 2a) What date did this hamstring injury occur? _____ / _____ / _____ 2b) What were you doing when the injury occurred?
Sprinting Kicking Picking up the ball Other
If other, please specify: ____________________________________________________________
2c) Were you: Training on your own Training with the team
Competing 2d) On which leg did the injury occur? Left Right 2e) Who diagnosed this injury?
Doctor Physiotherapist Other
If other, please specify: ____________________________________________________________
2f) Were any imaging investigations performed on this injury?
MRI Ultrasound Other
If other, please specify: ____________________________________________________________
2g) What was the severity of the strain?
Grade I Grade II Grade III Unsure
Rehabilitation Particulars 3a) Did you have any scheduled rehabilitation for this injury?
Yes No 3b) Who prescribed your rehabilitation?
Rehabilitation/conditioning coach Physiotherapist Other
If other, please specify: ____________________________________________________________
3c) What was the length of your rehabilitation (the time taken to resume full competition
following injury)?
3d) Describe in as much detail as possible the type of rehabilitation employed:
Appendices 227
Fourth Hamstring Injury 2a) What date did this hamstring injury occur? _____ / _____ / _____ 2b) What were you doing when the injury occurred?
Sprinting Kicking Picking up the ball Other
If other, please specify: ____________________________________________________________
2c) Were you: Training on your own Training with the team
Competing 2d) On which leg did the injury occur? Left Right 2e) Who diagnosed this injury?
Doctor Physiotherapist Other
If other, please specify: ____________________________________________________________
2f) Were any imaging investigations performed on this injury?
MRI Ultrasound Other
If other, please specify: ____________________________________________________________ 2g) What was the severity of the strain?
Grade I Grade II Grade III Unsure
Rehabilitation Particulars 3a) Did you have any scheduled rehabilitation for this injury?
Yes No 3b) Who prescribed your rehabilitation?
Rehabilitation/conditioning coach Physiotherapist Other
If other, please specify: ____________________________________________________________
3c) What was the length of your rehabilitation (the time taken to resume full competition
following injury)?
Appendices 228
3d) Describe in as much detail as possible the type of rehabilitation employed:
Appendices 229
Appendix C. Magnetic Resonance Imaging Screening Form
Appendices 230