Impact of prior hamstring strain injury & biofeedback on eccentric &

isometric knee flexor strength

Casey K.E Sims B. Exercise & Movement Science

Master of Applied Science (research)

Submitted in fulfilment of the requirement for the degree of

Master of Applied Science (research)

School of Exercise and Nutrition Sciences

Faculty of Health

Queensland University of Technology

2019

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Abstract

Hamstring strain injury (HSI) is the most prevalent non-contact injury in running-based

sports, and there have been considerable efforts to understand the aetiology of primary and

recurrent injuries. Rehabilitation and prevention programs have emerged from these

investigations with eccentric biased exercises, particularly the Nordic hamstring exercise

(NHE), showing powerful effects on injury rates, hamstring muscle architecture and eccentric

strength. The NHE is utilised reasonably widely in elite sport, however, there is minimal

understanding of the most effective way to prescribe the exercise. Successful randomised

controlled trials have employed as many as 3 sets of 10-12 repetitions per training session,

although it is uncommon to employ so many repetitions per set in elite sport and it is possible

that lower repetition schemes may induce less strength loss and allow more work to be

performed. Furthermore, the effects of a prior hamstring injury and performance feedback

(biofeedback) on the forces produced during the NHE are not known. Finally, a range of

strength tests has been employed to assess knee flexor strength and the torque-joint angle

relationship after a hamstring injury and this series of studies aimed to assess the value of

various bilateral and unilateral tests of dynamic and isometric strength.

Study 1 aimed to compare knee flexor forces and medial and lateral hamstring surface

electromyography (sEMG) during the performance of 30 repetitions of the NHE performed as

either 3 sets of 10 repetitions or 5 sets of 6 repetitions with knee flexor forces recorded via load

cells at the ankles. Fourteen recreationally active males participated in two sessions with

randomised presentation order of the two set and repetition schemes. There was no difference

between the average of the peak forces across 30 repetitions for the two prescriptions (mean

difference = 0.77N, 95% CI = -5.90 to 5.74; p = 0.97). Peak forces declined slightly between

the first and last two repetitions of both the 5x6 (mean change = -85.1N or 11.3%, 95%CI = -

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166.24 to -3.957N; p = 0.04) and the 3x10 scheme (mean change = -69.3N or 9.3%, 95% CI =

-131.23 to - 7.38N; p = 0.03) but there was no significant difference between the extent of these

changes. Normalised BF sEMG was significantly lower during the 3x10 than the 5x6

prescription (mean difference = 0.15, 95% CI = 0.164 to 0.125; p <0.01).

The aims of Study 2 were to: 1) assess the effects of previous HSI on knee flexor force

production during 30 repetitions of the NHE (3 sets of 10 repetitions); 2) To assess the effects

of real-time visual force biofeedback on the knee-flexor forces and medial and lateral hamstring

sEMG; and, 3) To assess biceps femoris long head (BFlh) muscle architecture in previously

injured limbs. Twelve males with a history of unilateral HSI presented to the laboratory on

three occasions. All had reported to be fully recovered from their injuries as determined by a

full return to sport and training. The first visit was to scan the BFlh via 2D ultrasound. The

second and third visits involved the performance of 3 sets of 10 repetitions of the NHE, once

with real-time visual biofeedback of knee flexor forces at each ankle presented throughout the

session and once without feedback of any sort. Previously injured BFlh muscles had shorter

fascicles (mean difference = -0.74cm, 95% CI = -0.3 to -0.011; p = 0.0001) and larger pennation

angles (mean difference = 1.110, 95% CI = 0.43 to 1.84; p = 0.005) than uninjured contralateral

muscles. There were no significant effects of previous injury (mean difference = -2.5N, 95%

CI = -46.7 to 41.7; p = 0.910) or biofeedback (-9.91N, 95% CI = -72.48 to 52.64; p= 0.751) on

the average of the peak knee-flexor force outputs across the 30 repetitions. There was no

significant effects of feedback (mean difference = -9.91N, 95% CI = -72.48 to 52.64; p = 0.751)

or previous injury (mean difference = -2.50N, 95% CI = -46.7 to 41.7; p = 0.910) on sEMG;

however, the average normalised lateral hamstring sEMG across the 30 repetitions was

significantly lower than that of the medial hamstrings (mean difference = 28.30%, 95% CI = -

49.51 to -7.10; p= 0.01).

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Study 3 aimed to: 1) determine the association between a prior HSI and knee flexor

joint angle of peak torque (JAPT) and the sEMG – knee angle relationship, or muscle

architecture; and, 2) to compare knee flexor strength and sEMG during the NHE, Razor Curl

and bilateral and unilateral isometric maximal voluntary contractions. Eight recreationally

active males with a unilateral history of HSI visited the laboratory on three occasions. The first

visit was to acquire BFlh architecture measures via 2D ultrasound. The second visit involved

isometric testing (to construct a torque-joint angle relationship for the knee flexors) on an

isokinetic dynamometer and the final visit involved a testing battery of the NHE, Razor curl

and prone unilateral and bilateral isometric contractions with maximum forces determined via

loads cells as per the previous studies. Muscle architecture measures showed significantly

shorter BFlh muscles fascicles (mean difference = -0.74cm, 95% CI = -0.27 to -1.23; p= 0.008)

and greater pennation angles (mean difference = 1.470, 95% CI = 1.0 to 1.93; p = <0.001) in

previously injured than uninjured limbs. Previously injured limbs did not differ in terms of

normalised isometric torque output in the seated isometric tests compared to the contralateral

uninjured limbs across the five angles tested on the dynamometer (mean difference = -0.03Nm,

95% CI = -0.34 to 0.29; p = 0.854) and no significant between-limb differences in force were

noted at any joint angle (p > 0.7 for all comparisons). The previously injured limbs were not

weaker than uninjured limbs in the NHE (mean difference = -7.4N, 95% CI = -28.8 to 14.1; p

= 0.44)), Razor curl (mean difference = 27.6N, 95% CI = 12.6 to -67.7; p = 0.149). The

difference between bilateral and unilateral strength was significant for the uninjured limbs

(mean difference = 29.7N, 95% CI =10.6 to 48.8; p = 0.008), but not the previously injured

limbs (mean difference = 13.0N, 95% CI = -5.2 to 31.1; p = 0.136).

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Despite the force output being higher in the Razor curl than the NHE, sEMG was higher

in the NHE for both the lateral (mean difference = 27.5%, 95% CI = 17.9 to 27.0; p = <0.001)

and medial hamstrings (mean difference = 25.3%, 95% CI = 12.4 to 38.2; p = 0.002). The

medial hamstrings were significantly more active than the lateral in both exercises (NHE mean

difference = 32.4%, 95% CI = 7.0 to 57.9; p = 0.02; Razor curl mean difference = 34.6, 95%CI

= 8.1 to 61.2; p = 0.018).

The program of research has presented some novel data that contributes to evolving

knowledge of HSI. For individuals familiar with the NHE, there appears to be small and similar

levels of force loss, as determined by peak forces across an exercise session, regardless of

whether 30 repetitions are arranged in sets of 6 or 10 repetitions. Limbs with a history of

relatively mild hamstring strains appear to have no significant eccentric or isometric strength

deficits, no increase in strength loss during 30 repetitions of the NHE exercise and no

differences in the knee-flexor JAPT despite exhibiting differences in muscle architecture by

comparison with contralateral uninjured limbs.

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Table of Contents Abstract ............................................................................................................................... 3

List of Figures...................................................................................................................... 9

List of tables ...................................................................................................................... 11

List of abbreviations ......................................................................................................... 12

STATEMENT OF ORIGINAL AUTHORSHIP ............................................................. 13

ACKNOWLEDGMENTS ................................................................................................. 13

Chapter 1: INTRODUCTION .......................................................................................... 14

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

2.1 Incidence of Hamstring Injury in Sport ................................................................. 16

2.1.2 American Football ........................................................................................... 16

2.1.3 Soccer .............................................................................................................. 17

2.1.4 AUSTRALIAN Football .................................................................................. 17

2.1.5 RUGBY Union ................................................................................................ 18

2.1.6 TRACK And Field ........................................................................................... 18

2.2 Recurrent Hamstring Strain Injury......................................................................... 19

2.3 Mechanism of Injury ............................................................................................. 20

2.4 Risk Factors .......................................................................................................... 22

2.4.1 Non-Modifiable Risk Factors ........................................................................... 22

2.4.2 Modifiable Risk Factors ................................................................................... 24

2.5 Factors in Hamstring Strain Injury Recurrence ...................................................... 30

2.5.1 Neuromuscular Inhibition ................................................................................ 31

2.5.2 Scar tissue formation........................................................................................ 33

2.6 Hamstring Injury Prevention ................................................................................. 34

2.6.1 Flexibility ........................................................................................................ 34

2.6.2 Eccentric and Eccentrically-biased Strength Training ....................................... 34

2.7 Assessing deficits in hamstring function after injury ............................................. 37

2.8 Biofeedback .......................................................................................................... 38

2.8.1 Proposed Mechanism of biofeedback in strength rehabilitation ........................ 39

2.9 The gapS in current literature. ............................................................................... 42

CHAPTER 3: KNEE-FLEXOR FATIGUE DURING THE NORDIC HAMSTRING EXERCISE ........................................................................................................................ 45

3.1 Research Objectives .................................................................................................. 45

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3.1.2 Objectives............................................................................................................... 45

3.1.3 PARTICIPANTS .................................................................................................... 45

3.1.4 Methodology .......................................................................................................... 45

3.1.5 Data Analysis: ........................................................................................................ 47

3.1.6 Statistical analysis .................................................................................................. 48

3.2 Results....................................................................................................................... 49

3.3 Discussion ................................................................................................................. 58

Linking Paragraph ........................................................................................................... 62

CHAPTER 4: The Effects of Biofeedback and Previous Hamstring Injury on Eccentric Strength During a Nordic Hamstring Training Session .................................................. 63

4.1 Research Design ........................................................................................................ 63

4.1.2 Objectives............................................................................................................... 63

4.1.3 Participants ............................................................................................................. 63

4.1.4 Methodology .......................................................................................................... 63

4.1.5 Data Analysis ......................................................................................................... 67

4.1.6 Statistical analysis .................................................................................................. 68

4.2 Results....................................................................................................................... 70

4.3 Discussion ................................................................................................................. 81

4.4 Conclusion ................................................................................................................ 84

Linking paragraph ........................................................................................................... 84

CHAPTER 5: The Effect of Previous Hamstring Strain Injury on Isometric and Dynamic Strength Profiles of the Knee-Flexors ............................................................... 85

5.1 Research Design ........................................................................................................ 85

5.1.1 Objectives............................................................................................................... 85

5.1.2 ParticipantS ............................................................................................................ 85

5.1.3 Methodology .......................................................................................................... 86

5.1.4 Data Analysis ........................................................................................................ 89

5.1.5 Statistical Analysis ................................................................................................. 90

5.2 Results....................................................................................................................... 91

5.3 Discussion ............................................................................................................... 100

5.4 Conclusion .............................................................................................................. 105

CONCLUSION ............................................................................................................... 106

CHAPTER 6: REFERENCES ........................................................................................ 108

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List of Figures

FIGURE 1: Changes in VMO/VL sEMG ratio for an exercise group and an exercise +

biofeedback group in patellofemoral pain sufferers with and without sEMG biofeedback. There

was a significant improvement only in the exercise + biofeedback group ........................... 40

FIGURE 2: Prone isometric test on hamstring testing device. Participants pull their legs up

against the restraints around ankle .................................................................................... 46

FIGURE 3: Nordic hamstring exercise on hamstring testing device. Participants pull against

ankle restraints as they resist falling .................................................................................. 46

FIGURE 4: Average of summed eccentric knee-flexor forces of all 30 repetitions for the 3x10

and 5x6 protocols ............................................................................................................... 50

FIGURE 5: Eccentric knee flexor forces in the first two and last two repetitions of the 3x10

and 5x6 protocols .............................................................................................................. 51

FIGURE 6: Averaged summed eccentric knee-flexor force per repetition for each exercise

prescription ........................................................................................................................ 52

FIGURE 7: Averaged knee angle at peak summed force for each exercise prescription ..... 53

FIGURE 8: Averaged knee angle velocity at peak summed force for each exercise prescription

.......................................................................................................................................... 54

FIGURE 9: Average normalised sEMG for all 30 repetitions of the protocols ................... 56

FIGURE 10: Normalised Surface EMG for 30 repetitions for the 3 x 10 and 5 x 6 protocols,

for the BF and MH ............................................................................................................. 57

FIGURE 11: Nordic hamstring exercise on hamstring testing device. Participants pull against

ankle restraints as they resist falling .................................................................................. 65

FIGURE 12: Nordic hamstring exercise with feedback displayed on a laptop in front of

participant performed on hamstring testing device. Participants pull against ankle restraints

as they resist falling ........................................................................................................... 65

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FIGURE 13: Left leg (red in the top trace), right leg (blue in the middle trace) and left and

right leg forces both shown within the one trace (bottom) for three consecutive repetitions of

the Nordic hamstring exercise. ........................................................................................... 66

FIGURE 14: Knee flexor strength comparison between limbs (N) of all NHE repetitions

performed. ......................................................................................................................... 72

FIGURE 15: Knee-Flexor Eccentric Force Across Time for NHE ..................................... 73

FIGURE 16: Average summed eccentric knee-flexor force per repetition of the NHE ........ 74

FIGURE 17 Comparison between feedback conditions for all 30 repetitions combined ..... 75

FIGURE 18: Averages of prone knee-flexor isometric contractions pre and post NHE exercise .......................................................................................................................................... 76

FIGURE 19: The effect of feedback on normalised sEMG for injured vs uninjured and medial

vs lateral hamstrings .......................................................................................................... 78

FIGURE 20: Normalised sEMG for medial and lateral hamstrings during 30 NHE repetitions

with and without feedback. ................................................................................................ 73

FIGURE 21: Isometric knee-flexor dynamometry. ............................................................. 85

FIGURE 22: Nordic hamstring exercise on hamstring testing device. Participants pull against

ankle restraints as they resist falling .................................................................................. 86

FIGURE 23: Razor curl test on hamstring testing device. participants pull against ankle

restraints as they resist falling ............................................................................................ 86

FIGURE 24: Normalised Torque – knee joint angle data for previously injured and uninjured

limbs as measured by isometric dynamometry .................................................................... 90

FIGURE 25: Normalised sEMG during isometric seated knee flexor dynamometry ........... 91

FIGURE 26: Eccentric knee-flexor force for NHE and Razor Curl .................................... 92

FIGURE 27: Comparison between exercises for normalised sEMG for injured vs uninjured

and medial vs lateral hamstrings. ....................................................................................... 93

FIGURE 28: Prone isometric force during unilateral and bilateral contractions. .............. 94

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FIGURE 29: Comparison between exercises for normalised sEMG for injured vs uninjured

and medial vs lateral hamstrings. ....................................................................................... 95

List of tables

Table 1: Participant anthropometric information .............................................................. 49

Table: Maximal Voluntary Contractions (Prone) – Descriptive Statistics ........................ 49

Table 3: Architectural characteristics of biceps femoris long head muscles in previously injured and uninjured limbs. ............................................................................................. 71

Table 4: Pre and Post Exercise Isometric Contractions – Descriptive Statistics ............... 77

Table 5: Hamstring injury history information for all participants. ................................... 89

Table 6: Architectural characteristics of biceps femoris long head muscles in previously injured and uninjured limbs. ............................................................................................. 90

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List of abbreviations

AFL Australian Football Leauge

BF Biceps Femoris

BFlh Biceps Femoris long head

BFsh Biceps Femoris short head

CI Confidence Interval

EMG Electromyography

EMGBF Electromyography Biofeedback

H:Q Hamstrings to Quadriceps

HIS Hamstring Strain Injury

IAAF

International Amateur Athletics

Federation

JAPT Joint Angle of Peak Torque

MH Medial Hamstring

MRI Magnetic Resonance Imagery

MVC Maximal Voluntary Contraction

MVIC

Maximal Voluntary Isometric

Contraction

NFL National Football League

NHE Nordic Hamstring Exercise

ROM Range of Motion

RR Relative Risk

sEMG Surface Electromyography

UEFA Union of European Football Associations

VL Vastus lateralis

VMO Vastus medialis oblique

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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: February 2019

ACKNOWLEDGMENTS

Firstly I’d like to thank my main supervisor Associate Professor Tony Shield for his

unwavering patience and support for the duration of this research program. From reading

countless drafts to answering even the smallest questions, he was there and always willing to

help. In addition associate supervisor Dr Geoffrey Minett for his timely and extremely helpful

feedback and direction to steer onto the right path. I’d also like to thank the Hamstring Strain

Injury Research Team for all their help in the laboratory and guidance in completing this thesis.

Lastly, a thank you to the participants for their contribution to this work and without them, this

wouldn’t have been possible.

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Chapter 1: INTRODUCTION

Sporting injuries are common and considerable efforts have been made to quantify their

effects on team success and finances (Eirale, Tol, Farooq, Smiley, & Chalabi, 2013; Ekstrand,

Gillquist, Möller, Oberg, & Liljedahl, 1983; Hägglund, Waldén, Magnusson et al., 2013;

Hickey, Shield, Williams, & Opar, 2014). Sporting injuries not only cause physical trauma and

time out of competition for athletes, but they also affect team performance, finances, academic

performance, psychological states (Andrew et al., 2014; Bliekendaal, Goossens, & Stubbe,

2017; Hickey et al., 2014; Merkel, 2013; Stubbe et al., 2015). However, the lack of injury

reporting in recreational sport and physical activity may result in a large underestimation of

injury prevalence (Kreisfeld, Harrison, & Pointer, 2014) and personal costs (Marshall &

Guskiewicz, 2003). The impacts of sporting injuries have prompted research that is required to

better understand their mechanisms and the factors that expose athletes to risk. The findings of

such research will hopefully lead to improved rehabilitation and injury prevention programs.

Hamstring strains are the most prevalent non-contact injuries in running-based sports (Opar,

Williams, & Shield, 2012). Despite considerable research interest, there have been either small

increases or small decreases in HSI prevalence in European soccer or Australian rules football

(AFL) in the past 20 years (Ekstrand, Waldén, & Hägglund, 2016; Hägglund, Waldén, &

Ekstrand, 2009; Hawkins & Fuller, 1999; Orchard & Seward, 2011; Orchard, Seward, &

Orchard, 2012a, 2012b). Further, the rate of HSI recurrence remains at ~23 - 60% across

different sporting populations (Brooks, Fuller, Kemp, & Reddin, 2006; Opar, Drezner et al.,

2014; Orchard, Seward, & Orchard, 2013a). These injury trends come with significant financial

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implications, with each HSI estimated to cost AFL clubs approximately AUD 40, 021 in 2012

(Hickey et al., 2014).

One common feature of injury rehabilitation programs is that they attempt to ameliorate

the deficits seen after injury in the hope of preventing recurrences (Croisier, Forthomme,

Namurois, Vanderthommen, & Crielaard, 2002; Croisier, Ganteaume, Binet, Genty, & Ferret,

2008). Hamstring injury rehabilitation strategies have previously been based on known post-

injury deficits such as those observed in eccentric strength and flexibility (Arnason, Andersen,

Holme, Engebretsen, & Bahr, 2008b; Petersen et al., 2011; van der Horst, Smits, Petersen,

Goedhart, & Backx, 2015a). However, there is a paucity of evidence regarding post-injury

deficits in knee-flexor strength-endurance and the torque-joint angle relationship (JAPT), and

an improved understanding of these may assist in the development of more successful

rehabilitation programs.

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CHAPTER 2: LITERATURE REVIEW

This review aims to provide the reader with an overview of current hamstring literature,

by outlining the prevalence in sport and the aetiology of HSI. An overview of the

morphological and functional consequences of injury and their potential implications on the

hamstring muscle group will be provided.

2.1 INCIDENCE OF HAMSTRING INJURY IN SPORT

Sports characterised by high-speed running, such as American football (NFL),

Australian football (AFL), football (Soccer), rugby union, and track and field each demonstrate

a high incidence of HSI. This not only impacts the athletes, but carries significant financial

ramifications for their respective clubs and organisations (Brooks, Fuller, Kemp, & Reddin,

2005a; Brooks et al., 2006; Brooks & Kemp, 2008; Brooks, Fuller, Kemp, & Reddin, 2005b;

Brophy, 2016; Dalton, Kerr, & Dompier, 2015; Dick, Putukian, Agel, Evans, & Marshall,

2007; Edouard, Branco, & Alonso, 2016; Edouard, Depiesse, Branco, & Alonso, 2014;

Ekstrand, Hägglund, & Waldén, 2009; Ekstrand et al., 2016; Elliott, Zarins, Powell, & Kenyon,

2011; Gabbe, Finch, Wajswelner, & Bennell, 2002; Malliaropoulos et al., 2010; Orchard &

Seward, 2002; Orchard & Seward, 2011; Orchard et al., 2012a, 2012b, 2013a; Woods et al.,

2004).

2.1.2 AMERICAN FOOTBALL

A 10-year injury surveillance across all National Football League (NFL) registered

teams was conducted between 1989 and 1998 (Elliott et al., 2011). During this period, 1716

HSIs were reported at a rate of 0.77 per 1000 athlete exposures (one athlete exposure = one

athlete exposed to either a training session or a game) with 16.5% of injuries being recurrences.

HSIs accounted for an annual average of 2222 days lost to injury. HSI also plagues elite college

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American football with Dalton and colleagues (2016) reporting HSI contributing to 35.5% of

all injuries across five seasons (Dalton et al., 2015). In another ten-year surveillance study

focused on NFL preseason and training camps, the authors found HSI to be the second most

frequent injury behind knee sprains (Feeley et al., 2008). HSIs during preseason and training

camps accounted for an average of 8.3 days lost to injury.

2.1.3 SOCCER

HSIs are also the most frequently observed injury in association soccer (Ekstrand et al.,

2009; Ekstrand et al., 2016; Hägglund, Waldén, & Ekstrand, 2006; Hägglund et al., 2009;

Hägglund, Waldén, & Ekstrand, 2013; Woods et al., 2004). HSI represented approximately

12% of all injuries recorded in professional European soccer with Woods and Colleagues

(2004) reporting five to six injuries per club per season resulting in approximately 90 days

away from training and matches per club. Ekstrand and colleagues (2011) reported that HSIs

represent 12% of all injuries in UEFA competition with an average of four to six hamstring

strain injuries per club resulting in approximately 82 days away from matches and training

sessions per club per season. During the nine consecutive seasons of European professional

soccer (2001- 2010), 26 clubs reported 900 HSIs amongst a total of 2123 lower limb muscle

strain injuries (Hägglund, Waldén, Magnusson et al., 2013). Out of these HSIs, 53% required

an eight to 28-day recovery, and 13% required more than 28 days (Hägglund, Waldén,

Magnusson et al., 2013).

2.1.4 AUSTRALIAN FOOTBALL

The AFL routinely reports HSI as the highest frequency and most prevalent injury

(Brophy, 2016; Gabbe et al., 2002; Gabbe, Bennell, Finch, Wajswelner, & Orchard, 2006;

Orchard et al., 2012a, 2012b, 2013a). In 2012(a) Orchard, Seward and Orchard published

results from 21 years of injury surveillance reporting HSI to be the most frequently occurring

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injury, with six new injuries per club per season (Orchard & Seward, 2002; Orchard & Seward,

2008; Orchard & Seward, 2010, 2011; Orchard et al., 2012a, 2012b, 2013a; Orchard, Seward,

& Orchard, 2013b). The accumulated recovery times for each club due to HSI resulted in 20

missed matches (3.8 games per HSI) during the standard 22 match season. At the community

level of Australian football, HSI was the most commonly reported injury, accounting for 10 -

13.7% of all injuries (Ekegren et al., 2015; Gabbe et al., 2002).

2.1.5 RUGBY UNION

The incidence of HSI in elite English Rugby Union is second only to thigh hematomas;

however, HSI recovery time is threefold that of haematomas (Brooks et al., 2005a; Brooks et

al., 2006; Brooks & Kemp, 2008; Brooks et al., 2005b). The incidence of HSI is similar to AFL

and elite European soccer, with each club sustaining approximately seven HSIs per year

resulting in an accumulated 123 days of lost playing time (Brooks et al., 2006; Ekstrand et al.,

2016; Orchard et al., 2013b). Most of the HSIs occur during matches rather than training, with

researchers noting a higher incidence of injury in the last quarter of a match (Brooks et al.,

2006).

2.1.6 TRACK AND FIELD

Track and field competitors are at significantly greater risk of sustaining a HSI than any

other injury (Alonso et al., 2012; Alonso et al., 2010; Edouard et al., 2016; Edouard et al., 2014;

Opar, Drezner et al., 2014). At the 2009 and 2011 International Amateur Athletics Federation

(IAAF) World Championships, Alonso and colleagues analysed injury data from all countries

that had a team of 15 or more (Alonso et al., 2012; Alonso et al., 2010). While HSI was not

specifically identified, thigh injury accounted for 23.3% of all injuries, and it is known from

other track and field studies that hamstring injuries are >5 times more common than quadriceps

strains (Opar, Drezner et al., 2014). Thigh strain was also the blanket term used in an all injury

analysis of high school track and field competitors in the United States, with boys and girls

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both displaying incidence rates of 35.5% and 26.6% respectively (Dalton et al., 2015).

Additionally, a three-year injury surveillance study of 48 473 athletes at the Penn Relays

Athletics Carnival found HSI accounted for 24.1% of all injuries and 75% of all lower limb

injuries (Opar, Drezner et al., 2014).

Track and Field athletes, on average, face longer recuperation periods after hamstring

injury than competitors in other sports (Askling, Saartok, & Thorstensson, 2006). In elite

soccer, rugby union and AFL, a single club with 5-7 injuries per club collectively loses 90-123

days, or approximately 18 days per injury (Ekstrand, Hägglund, & Waldén, 2011; Orchard &

Seward, 2002; Orchard et al., 2013b; Woods et al., 2004). For a track and field athlete, the

median recovery is 112 days (16 weeks) with a variance between 6 – 50 weeks (Askling et al.,

2006). The extended recovery could be attributed to track and field athletes relying purely on

high speed running compared to the other sports where skilful players may be able to return to

competition before they fully recover their ability to sprint maximally.

2.2 RECURRENT HAMSTRING STRAIN INJURY

In addition to a high incidence, HSI also exhibits high recurrence rates in running-based

sports (Brooks et al., 2006; Croisier, 2004; Ekstrand et al., 2011; Orchard & Seward, 2002;

Orchard & Seward, 2011; Orchard et al., 2013b; Woods et al., 2004). The AFL has

demonstrated an average recurrence rate of 23% over ten seasons from 2001-10 (Orchard &

Seward, 2011). Similarly, during the 2002-2004 seasons of the English professional rugby

union competition, recurrent injuries accounted for 23% of the total HSIs (Brooks et al., 2006).

Recurrent injuries were typically more severe than the original injuries as they resulted in

significantly more time away from training and competition (Brooks et al., 2006). In athletics,

the Penn Relays Carnival attracted 48,698 participants over a three-year period (2002-2004),

with 26% of all reported injuries being HSIs and 60% of these being recurrences (Opar, Drezner

et al., 2014). Despite the high recurrence rates across multiple sports, the AFL has reported a

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decline from 27% to 15% in recurrent HSIs across a ten year period (2003-2012). This has been

attributed to a more conservative (slower) approach to return to sport in recent times (Orchard

& Seward, 2011).

Multiple factors are thought to contribute to initial HSI, and it is likely that most injuries

result from interactions between modifiable and non-modifiable risk factors. High recurrence

rates suggest that current rehabilitation practices are not preparing the hamstring muscles

adequately for a return to play and competition. Current evidence suggests having a prior HSI

is the strongest predictor of sustaining a future HSI (Gabbe, Bennell et al., 2006; Hägglund et

al., 2006; Orchard, 2001). This review will examine risk factors for HSI; however, there will

be a focus on the possible roles of the knee-flexor fatiguability, torque-joint angle relationship

and between-limb imbalances in eccentric strength, all of which have been proposed to

contribute to re-injury risk (Bourne, Opar, & Shield, 2014; Bourne, Opar, Williams, Al Najjar,

& Shield, 2015; Croisier & Crielaard, 2000; Croisier et al., 2008; Opar, Williams, Timmins,

Dear, & Shield, 2013a, 2013b; Timmins, Bourne, Shield, Williams, Lorenzen et al., 2015; Tol

et al., 2014).

2.3 MECHANISM OF INJURY

To address the inadequacies of HSI rehabilitation an understanding of the mechanism

of injury is required. Hamstring injuries are typically classified as either ‘sprint’ or ‘stretch’

injuries. The main focus of this literature review and programme of research is sprint type

injuries, due to their high incidence and recurrence rates in running-based sports (Opar et al.,

2012).

HSI rates in running sports have prompted analyses of running to determine the likely timing

of injury (Chumanov, Heiderscheit, & Thelen, 2007, 2011; Higashihara, Nagano, Ono, &

Fukubayashi, 2016; Yu et al., 2008). With the assumption that high force eccentric actions at

longer muscle lengths are likely to be detrimental, the terminal swing phase is suggested as the

21

most likely time in the gait cycle for HSI to occur (Chumanov et al., 2011; Schache, Dorn,

Blanch, Brown, & Pandy, 2012; Schache, Kim, Morgan, & Pandy, 2010). In this stage of the

gait cycle the hamstrings experience active lengthening (eccentric actions), although some

modelling studies also suggest active lengthening in the early stance phase to be potentially

injurious (Chumanov et al., 2011; Schache et al., 2012; Schache et al., 2010; Yu et al., 2008).

Biomechanical analyses suggest the hamstring muscle group exhibits peak electromyographic

(EMG) activity during the terminal swing and early stance phases (Chumanov et al., 2011;

Schache et al., 2012; Schache et al., 2010; Yu et al., 2008). Additionally, hamstring strain

(length) is higher in the late swing than any other phase of gait (Thelen et al., 2005). Modelling

studies suggest that the biceps femoris long head (BFlh) is stretched the most out of all the

hamstring muscles, reaching 109-112% of its ‘upright-standing’ length compared to

semimembranosus (107.4%) and semitendinosus (108.1%) (Chumanov et al., 2007; Schache

et al., 2012; Thelen et al., 2005).

High eccentric activation levels can be attributed to the simultaneous muscle

lengthening and deceleration of the extending knee and flexing hip during the terminal swing

phase. It has been argued that the combination of the high force (stress) eccentric actions and

the moderate lengths of the muscle-tendinous units make the terminal swing phase riskier than

early stance, which is characterised by high levels of activity but shorter muscle-tendon units

(Chumanov et al., 2011; Dolman, Verrall, & Reid, 2014; Thelen et al., 2005; Yu et al., 2008).

The argument that the terminal swing phase is the most likely time of injury is supported, to an

extent, by two serendipitous HSIs that have been observed during biomechanical analyses of

sprint running (Heiderscheit et al., 2005; Schache et al., 2010). In both studies, the late swing

phase was determined to be the most likely time for each strain to have occurred given the

22

onset of disrupted gait and presumptions about the lag times required to sense and respond to

these injuries.

2.4 RISK FACTORS

A number of modifiable and non-modifiable risk factors have been suggested to

contribute to HSIs. Understanding each risk factor may assist in identifying at-risk individuals

or in developing effective intervention strategies.

2.4.1 NON-MODIFIABLE RISK FACTORS

Age

Increasing age in elite sport has proven to be an independent risk factor for HSI

(Arnason et al., 2004; Gabbe, Finch, Bennell, & Wajswelner, 2005; Henderson, Barnes, &

Portas, 2010; Timmins, Bourne, Shield, Williams, Lorenzen et al., 2015; Verrall, Slavotinek,

Barnes, Fon, & Spriggins, 2001; Woods et al., 2004). Investigations in soccer have shown that

athletes beyond 23 years of age were at a significantly higher risk of injury than younger players

(Woods et al., 2004). Henderson and colleagues (2009) have also reported that the odds for

European soccer players sustaining a hamstring injury increased 1.8 fold per year. Studies of

AFL players found players older than 23 years of age to be more prone to HSI than younger

players (Orchard, 2001). Another investigation found that players 25 years of age and older

suffered twice as many HSIs compared to those 20 years and younger (Gabbe, Bennell et al.,

2006). For AFL players, every one-year increase in age has been reported to increase the risk

of HSI 1.3 fold (Verrall et al., 2001).

It is unknown why older athletes are at increased risk of injury. Investigators have

proposed alterations to muscle volume, fibres, and fibre type (Gabbe, Bennell et al., 2006;

Orchard, Farhart, & Leopold, 2004), but there is no evidence for any of these. Other proposals

attribute injury rates to age-related hypertrophy of the lumbosacral ligament, which has been

23

proposed to potentially entrap the L5/S1 nerve root (Orchard et al., 2004). Again, there is no

evidence for this. Further studies are required to determine the mechanisms that are responsible

for increased HSI rates in older athletes.

Previous Injury

Previous injury is the greatest predictor of future HSI in elite sport (Gabbe, Branson et

al., 2006; Hägglund et al., 2006; Orchard, 2001; Verrall et al., 2001). One study of soccer

players indicated that those who had previously sustained a HSI were 11.6 times more likely

to sustain another in the following season than players without such a history (Arnason et al.,

2004; Hägglund et al., 2006). AFL players with a previous HSI are 2.4 times more likely to

suffer re-injury (Gabbe, Bennell et al., 2006; Orchard, 2001; Orchard et al., 2013b). HSIs have

been suggested to elicit structural and functional deficits, with some still apparent months and

years after an athlete returns to play. These deficits include presistent reductions in eccentric

strength (Croisier et al., 2002; Croisier et al., 2008; Gabbe, Bennell et al., 2006; Jonhagen,

Nemeth, & Eriksson, 1994; Lee, Reid, Elliott, & Lloyd, 2009; Orchard, 2001; Orchard et al.,

2013b; Timmins, Bourne, Shield, Williams, Lorenzen et al., 2015) and voluntary activation of

the hamstrings (Bourne, Opar, Williams, Al Najjar et al., 2015; Opar, Williams et al., 2013a;

Opar, Williams et al., 2014b; Silder, Reeder, & Thelen, 2010; Timmins et al., 2014a), residual

scar tissue (Connell et al., 2004; Silder, Heiderscheit, Thelen, Enright, & Tuite, 2008; Silder et

al., 2010) and possibly shortened fascicles within the often injured long head of the biceps

femoris (Timmins, Bourne, Shield, Williams, Lorenzen et al., 2015; Timmins, Shield,

Williams, Lorenzen, & Opar, 2015). It is also possible that prior injury alters running

mechanics and that these changes result in an elevated propensity towards injury (Lee et al.,

2009; Schache, Wrigley, Baker, & Pandy, 2009). High recurrence rates may indicate that

24

rehabilitation fails to address these deficits in hamstring function or that other unidentified pre-

existing causative factors persist.

2.4.2 MODIFIABLE RISK FACTORS

Flexibility

Reduced hip extensor/knee-flexor range has been proposed as a risk factor for muscle

strain injury (Witvrouw, Danneels, Asselman, D’Have, & Cambier, 2003). Specific to HSI,

increased flexibility has been proposed to increase the amount of energy the passive contractile

components can absorb during forceful eccentric contraction (Bennell et al., 1998). Increased

strain absorbed by passive components, it is argued, may reduce the load on contractile tissue

during the terminal swing/early stance phase of gait, reducing the risk of strain injury (Garrett

et al., 1990; Witvrouw et al., 2003). Several approaches have been used to quantify flexibility

including sit and reach (Gabbe, Bennell et al., 2006; Orchard, Marsden, Lord, & Garlick, 1997),

active (Gabbe, Branson et al., 2006; Gabbe et al., 2005) and passive knee extension tests

(Arnason et al., 2008a), and single leg raises (Yeung, Suen, & Yeung, 2009). Collectively, the

tests above have produced confounding results with a meta-analysis showing no significant

relationship between range of motion (ROM) and HSI (Freckleton & Pizzari, 2012).

Fatigue

An increased susceptibility to HSI in fatigued athletes has been suggested by evidence

from laboratory and sporting environments. For example, multiple epidemiological studies

have reported that a majority of HSIs occur in the later portions of training and gameplay in

soccer and rugby union (Brooks et al., 2006; Ekstrand et al., 2009, 2011; Hawkins & Fuller,

1999; Woods et al., 2004). Laboratory testing on isolated animal muscles has provided insight

into the role of fatigue on a muscle’s capability to withstand forces during active lengthening

(Mair, Seaber, Glisson, & Garrett, 1996). Muscles fatigued by electrical stimulation were

25

shown to absorb 8 – 30% less energy before rupture, compared to unfatigued muscles (Mair et

al., 1996). In the human context of high speed running, it could be implied that a fatigued

muscle may not have the capacity to absorb energy during the eccentric actions of the terminal

swing phase and this may result in overlengthening of the fatigued hamstrings, leading to strain

injury.

Fatigue caused by repeated dynamic knee-flexor efforts in humans has been found to

alter the running mechanics of the lower limb, leading to increases in knee extension and

decreased hip extension (Pinniger, Steele, & Groeller, 2000). Similarly Small and colleagues

(2009) saw similar alternations to running mechanics in knee extension and hip extension

angles with fatigue after a simulated football match. While these kinematic changes may cancel

the other’s effects on hamstring length, it has been proposed that fatigue-induced deficits in

proprioception may contribute to the reduced control of lower limbs and thereby increase the

risk of a hamstring injury (Pinniger et al., 2000). Others have observed that fatiguing isokinetic

knee-flexor protocols cause humans to underestimate hamstring length (Allen, Leung, &

Proske, 2010).

Greig (2008) and Small & McNaughton et al., (2009) replicated the intermittent running

demands of a soccer match and found reduced knee-flexor torque in the eccentric contraction

mode only. These findings are supported by Timmins et al., (2014), who showed reductions in

both eccentric strength and biceps femoris long head (BFlh) (sEMG) activity during maximal

eccentric knee flexor contractions after repeated overground sprinting. Hamstring fatigue,

particularly in eccentric contraction modes, may elevate the risk of HSI given the suggested

links between eccentric strength and the risk of HSI.

Knee-flexor Strength

The combination of high levels of force and active lengthening during the terminal

swing phase of the gait cycle has been suggested to be particularly hazardous to the hamstring

26

muscle group (Chumanov et al., 2011; Croisier et al., 2008; Opar, Williams et al., 2014b; Opar

et al., 2012; Sugiura, Saito, Sakuraba, Sakuma, & Suzuki, 2008; Thelen et al., 2005; van Dyk

et al., 2016). These findings have prompted some authors to suggest that having a greater

capacity to absorb energy during eccentric contractions could protect the hamstring muscle

group during active lengthening. Investigations using animal muscles showed maximally

stimulated muscles were able to withstand a greater amount of stress than those stimulated sub-

maximally and could, therefore, withstand greater loads before failing (Mair et al., 1996).

Together these findings suggest a theoretical basis for the benefits of increasing eccentric

strength for the reduction of hamstring injury risk.

Isokinetic testing on dynamometers has not shown a consistent relationship between

knee-flexor strength and hamstring injury rates (Bennell et al., 1998; Freckleton & Pizzari,

2012; Green, Bourne, & Pizzari, 2017; van Dyk et al., 2016). The most powerful study to date

involved the isokinetic testing of 614 professional players over four years (van Dyk et al.,

2016). Findings from this study showed eccentric strength to be a weak risk factor for a

hamstring injury which was unable to be used in the identification of at-risk athletes.

Recently, eccentric strength has been tested by instrumenting the Nordic hamstring

exercise via load cells connected to ankle restraints (Opar, Piatkowski, Williams, & Shield,

2013). Low levels of Nordic eccentric knee-flexor strength have been suggested to predispose

AFL and Australian Soccer Players (A-League) players to HSI. In an AFL cohort, weaker

athletes (eccentric strength <279 N in late pre-season) were 4.4 times more likely to sustain a

HSI compared to stronger players (Opar, Williams et al., 2014a). However, no relationship

between Nordic strength and hamstring injury rates were reported in studies of Australian male

Rugby union players (Bourne, Opar, Williams, & Shield, 2015) or elite Qatari soccer players

27

(van Dyk et al., 2017) It is evident that there is no clear consensus on the relationship between

strength and the risk of hamstring injury.

A lower hamstring to quadriceps strength (H:Q) ratio has been proposed to be a risk

factor for HSI given the assumption that it signifies the capacity of the hamstrings to overcome

the angular momentum created during the swing phase of running gait (Croisier et al., 2008;

Opar et al., 2012). Deficits in hamstring eccentric strength during the terminal swing could

cause the forward swinging shank to move to a position that is beyond the mechanical limits

of these muscles (Aagaard, Simonsen, Magnusson, Larsson, & Dyhre-Poulsen, 1998; Croisier

et al., 2008). The H:Q ratio is measured using an isokinetic dynamometer and originally

involved concentric contractions of both quadriceps and hamstrings. However, the terminal

swing phase of gait involves eccentric actions of the hamstrings (Chumanov et al., 2011). As a

consequence, the functional H:Q ratio, which compares eccentric knee-flexor to concentric

knee extensor strength is now considered more appropriate (Croisier et al., 2002; Croisier et

al., 2008; Yeung et al., 2009).

Croisier and colleagues (2008) have reported that a mixture of knee-flexor performance

indices including the conventional H:Q ratio, the functional H:Q ratio and bilateral knee-flexor

asymmetries of >15%, all measured at a range of speeds, were associated with a greater risk of

a hamstring strain injury if the players did not undertake efforts to correct the imbalances.

These soccer players were part of a large cohort (n=462), and 5.7% of players who underwent

retesting went on to sustain a severe (>4-week recovery) hamstring injury while 16.7% of

players who chose not to attempt correction or to be reassessed sustained a severe injury

(Croisier et al., 2008). Results from an AFL study using the H:Qconv test found 0.5 to 0.6 to

be a cut-off for significant injury risk (Orchard et al., 1997). Likewise, sprinters were at a 17.4

fold risk of injury with a ratio of <0.6 (Yeung et al., 2009). However, except for the study by

Croisier and colleagues (2008), most of the studies above examining H:Q ratios were small to

28

medium in scale. As a consequence of these limitations and the aforementioned negative

findings, the value of the H:Q ratio is at best uncertain (Freckleton & Pizzari, 2012; Green et

al., 2017; van Dyk et al., 2016).

Fascicle Length

It has been proposed that human hamstring muscles with fewer in-series sarcomeres (or

shorter fascicles) are more prone to strain injury (Brockett, Morgan, & Proske, 2001) and only

recently has this proposal been tested. In a prospective study of elite Australian male soccer

players, Timmins and colleagues (2015a) showed a four-fold increase in injury in players

whose BFLH fascicles were shorter than 10.56 cm compared to players with longer fascicles.

This study also showed that older and previously injured players with longer fascicles were at

no greater risk of hamstring injury than young and previously uninjured players. At present,

this study is the only one of its type, and more investigations in this area are required to confirm

the role of BFLH fascicle length in HSI.

Joint Angle of Peak Torque

A post HSI shift in the knee-flexor joint angle of peak torque (JAPT) towards shorter

muscle lengths, presumably as the result of the injured muscles losing in-series sarcomeres,

has been widely cited in the literature (Brockett et al., 2001; Brockett, Morgan, & Proske, 2004;

Brughelli, Cronin, Mendiguchia, Kinsella, & Nosaka, 2010; Brughelli, Nosaka, & Cronin,

2009; Heiderscheit, Sherry, Silder, Chumanov, & Thelen, 2010). However, the evidence for

shifted JAPT is based on observations of between limb differences in only 10 participants from

two studies (Brockett et al., 2001; Brughelli et al., 2009). Furthermore, there are no published

observations of hamstring fascicle lengths shortening as a result of a hamstring injury, and the

29

retrospective nature of JAPT studies means that it is not possible to establish that the initial

hamstring injuries caused these differences.

It has been argued that sarcomeres within myofibrils lengthen in a non-uniform fashion

and therefore become unstable during eccentric actions beyond the lengths required for optimal

force generation (Gordon, Huxley, & Julian, 1966; Morgan, 1990; Proske & Morgan, 2001;

Verrall et al., 2001). According to the theory, the longer sarcomeres become weaker than the

shorter and are therefore thought to overextend or ‘pop’ as a result. This sarcomere damage is

argued to be a normal part of delayed onset muscle soreness (Proske & Morgan, 2001) and it

typically remains microscopic in nature. However, in athletes who frequently run at high speed,

it has been argued that this microscopic damage may accumulate across a training session or

multiple training sessions and eventually result in macrotrauma in the form of a strain injury

(Brockett et al., 2004; Morgan, 1990; Proske & Morgan, 2001). If a previously injured muscle

has a shorter optimal length as a consequence of having fewer in-series sarcomeres, it may

perform more work with its sarcomeres acting beyond their optimal length and therefore be

more prone to injury (Brockett et al., 2004; Morgan, 1990).

Neuromuscular inhibition has been proposed as an additional explanation for a shift in

injured knee-flexor JAPT and its failure to return to normal throughout the rehabilitation

process (Fyfe, Opar, Williams, & Shield, 2013; Sole, Milosavljevic, Nicholson, & Sullivan,

2011). Neuromuscular inhibition, which has been shown to be persistent after hamstring strain

injury (Bourne, Opar, Williams, Al Najjar et al., 2015; Opar, Williams et al., 2013a, 2013b) is

suggested to occur to prevent the hamstring muscle group generating high eccentric forces at

longer muscle lengths. However, in late rehabilitation exercises are performed with the goal of

restoring strength at long lengths. It has been proposed that inhibited muscles may create

30

insufficient eccentric forces at long lengths to stimulate sarcomerogenesis which might be

required to restore normal fascicle lengths and JAPT (Fyfe et al., 2013).

The argument that hamstring injury causes a shift in the JAPT has some limitations.

Firstly, it has not been established that strain injury to one or two of the seven major knee-

flexor muscles can result in a shift in knee-flexor JAPT (Timmins, Shield, Williams, & Opar,

2016). A 12.1 ± 2.7° shift in the angle of optimal knee flexion torque was reported in the largest

study of nine participants (Brockett et al., 2001), which is very hard to attribute to previous

damage to one or two muscles. Secondly, the paucity of evidence for this ‘shift’ suggests a

need for further investigation to support the claims that is has a role in elevating the risk of

hamstring strain injury or that it is a result of such injury. The subsequent studies aim to address

the limitations of the JAPT measure in the literature and provide a better understanding of this

measure.

2.5 FACTORS IN HAMSTRING STRAIN INJURY RECURRENCE

Despite significant research efforts, as many as 30% of HSIs in footballers re-occur in

the same season (Ekstrand et al., 2016; Orchard et al., 2013a). The most definitive risk factor

for future HSI is previous HSI (Arnason et al., 2004; Gabbe, Bennell et al., 2006; Orchard,

2001). This suggests that rehabilitation is either not successfully addressing the original

causative factors for injury, or that one or more structural and functional maladaptations occur

following injury and this or these predispose athletes to recurrent injury. Previously injured

hamstrings have been reported to exhibit significant deficits in strength and flexibility (Maniar,

Shield, Williams, Timmins, & Opar, 2016), and the loss of strength is often significantly greater

in eccentric than concentric tests (Croisier & Crielaard, 2000; Croisier et al., 2002; Croisier et

al., 2008; Jonhagen et al., 1994; Lee et al., 2009; Opar, Williams et al., 2013a). There is also

some evidence of shorter fascicles in injured versus uninjured BFlh muscles (Timmins, Bourne,

31

Shield, Williams, & Opar, 2015; Timmins, Bourne, Shield, Williams, Lorenzen et al., 2015;

Timmins, Shield et al., 2015) and increased fatigue, in the form of slower sprint speeds, in

athletes with prior HSI (Røksund et al., 2017).

2.5.1 NEUROMUSCULAR INHIBITION

Neuromuscular inhibition has been proposed as the cause of eccentric strength deficits

after HSI (Fyfe et al., 2013; Opar et al., 2012). For this review, voluntary activation is defined

as the completeness of skeletal muscle activation during maximal voluntary contractions

(Shield & Zhou, 2004). After a muscle or joint injury, acute changes in maximal voluntary

muscle activation and strength have been identified (Akima, Hioki, & Furukawa, 2008a;

Bourne et al., 2014; Bourne, Opar, Williams, Al Najjar et al., 2015; Callaghan & Oldham,

2004; Croisier & Crielaard, 2000; Croisier et al., 2002; Heiderscheit et al., 2010; Hurley &

Newham, 1993; Opar, Williams et al., 2013a, 2013b; Silder et al., 2010; Timmins et al., 2014b;

Urbach, Nebelung, Becker, & Awiszus, 2001). These changes are proposed to serve as a

protective mechanism and reduce the loads on recently injured and sensitised muscle or joint

tissues (Gabler, Kitzman, & Mattacola, 2013; Hopkins & Ingersoll, 2010; Sole et al., 2011).

However, these deficits are not always reversed by rehabilitation and return to play and may

persist, resulting in a chronically reduced capacity to voluntarily activate the previously injured

muscle(s) (Fyfe et al., 2013; Gabler et al., 2013; Hopkins & Ingersoll, 2010).

Neuromuscular inhibition has been reported in other lower limb injuries, particularly in

relation to deficits in quadriceps strength after a knee injury (Akima, Hioki, & Furukawa,

2008b; Ingersoll, Grindstaff, Pietrosimone, & Hart, 2008; Urbach et al., 2001). There is also

some recent evidence for the existence of hamstring muscle inhibition after HSI. Deficits in

hamstring sEMG (when normalised to concentric sEMG of the same muscles) during maximal

eccentric contractions in previously injured BF muscles compared to the medial and uninjured

32

contralateral BF muscles, have been reported (Opar, Williams et al., 2013a). Opar and

colleagues (2013b) also noted reduced rates of hamstring sEMG and knee-flexor torque

development in previously injured limbs during maximal eccentric actions performed on a

dynamometer.

These observations are consistent with the evidence gathered using functional magnetic

resonance imaging (fMRI) (Bourne, Opar, Williams, Al Najjar et al., 2015). Previously

hamstring injured participants were required to perform 60 repetitions of the NHE and the

activation of previously injured muscles (as measured by changes in T2 relaxation times) was

markedly smaller in the previously injured BFlh compared to contralateral homonymous

muscles (Bourne et al., 2015b). Indirect evidence for injury-induced hamstring muscle

inhibition also comes from a study that has reported that muscle-specific atrophy of previously

injured BFlh muscles coexists with relatively hypertrophied BFsh muscles by contrast with

uninjured contralateral muscles (Silder et al., 2008). Importantly, all of the above observations

were made in athletes who had undergone rehabilitation and resumed full training and

competition in their chosen sports. This suggests that the deficits in voluntary activation are

persistent, although the retrospective nature of these observations prevents any conclusion that

injury causes inhibition.

Neuromuscular inhibition is suggested to sabotage rehabilitation from HSI (Fyfe et al.,

2013). The acute de-loading of muscle tissue and the reduction in muscle excursion in the early

days after injury are proposed to cause reductions in strength and fascicle lengths. Cautious

practices in the early and middle stages of rehabilitation reduce the exposure to high forces and

longer muscle lengths (Sherry et al., 2015) in an attempt to minimise the formation of scar

tissue (Heiderscheit et al., 2010). When the muscles eventually get exposed to moderate and

high eccentric forces and longer muscle lengths in late rehabilitation, the expected outcomes

are increased fascicle lengths (via sarcomerogenesis) and the return of strength to pre-injury

33

levels (Fyfe et al., 2013; Sole et al., 2011). However, unresolved inhibition is proposed to limit

the strength of eccentric hamstring contractions (Bourne et al., 2014), particularly at longer

muscle lengths (Sole et al., 2011), and this is proposed to rob the previously injured hamstring

muscle(s) of the stimuli for fascicle lengthening and the recovery of eccentric strength (Fyfe et

al., 2013; Opar et al., 2012).

While the model proposed by Fyfe and colleagues (2013) remains to be thoroughly

tested, there is some evidence that is consistent with it. For example, AFL players with a history

of at least one hamstring strain in the previous season have been reported to exhibit markedly

lower eccentric strength improvements across the course of the subsequent preseason training

period than players who were not injured in that time frame (Opar, Williams et al., 2014a).

Furthermore, previously injured athletes have been reported to exhibit shorter BFLH fascicles

in their injured than uninjured limbs despite the return to full training and competition

schedules (Timmins, Shield et al., 2015). More recently, smaller pre-season increases in BFLH

fascicle lengths have been reported in previously injured than contralateral uninjured limbs and

players with no history of hamstring strain (Timmins, Bourne, Williams, & Opar, 2018).

Further work will be needed, however, to establish that hamstring muscle inhibition is the

underlying cause of these observations.

2.5.2 SCAR TISSUE FORMATION

Scar tissue formation has been proposed to contribute to future HSI due to its impact

on the lengthening mechanics of adjacent muscle tissue (Silder et al., 2008). Post HSI, scar

tissue forms, often at the muscle-tendon junction, with the adjacent muscle fibres experiencing

greater strain compared to the contralateral limb. Tissue morphological adaptations are also

said to be persistent after injury with Silder and colleagues (2008) observing scar tissue in

34

previously injured limbs 5- 23 months post-injury. The changes in muscle-tendon junction

stiffness and the consequently higher levels of muscle strain suggest a greater risk of re-injury.

2.6 HAMSTRING INJURY PREVENTION

With the identification of modifiable risk factors, interventions are developed in the

hope of reducing injury. In the case of the hamstrings, these interventions have focused most

on improving flexibility and eccentric strength.

2.6.1 FLEXIBILITY

More flexible hamstrings have been proposed to be less prone to strain injury although

it should be acknowledged that the evidence for this is sparse (Bennell, Tully, & Harvey, 1999).

A large-scale non-randomised intervention to increase the flexibility of elite European soccer

players found no significant difference in injury rates between teams that did and did not

participate in flexibility training (Arnason et al., 2008a). The study by Arnason and colleagues

(2008) assigned a partner based flexibility training intervention three times a week to players

during the pre-season, and this was reduced to once or twice a week during the playing season.

Similarly, Malliaroplolous and colleagues (2004) reported no reduction in HSI rates in a group

of recreational runners who undertook a 16-week program of warm up, cool down and

stretching procedures (Malliaropoulos, Papalexandris, Papalada, & Papacostas, 2004).

2.6.2 ECCENTRIC AND ECCENTRICALLY-BIASED STRENGTH TRAINING

For the sake of this review, eccentrically-biased strength training is any form of

resistance training in which the forces created or the loads encountered by the hamstring

muscles during the eccentric portion of a lift or exercise are higher than those encountered in

the concentric phase. Many studies have explored the effect of eccentric conditioning on

35

hamstring injury rates in sport (Arnason et al., 2008a; Askling et al., 2014; Askling, Tengvar,

& Thorstensson, 2013; Petersen et al., 2011; Seagrave et al., 2014; van der Horst et al., 2015a).

Askling and colleagues (2013) administered a ten-week leg curl training programme (using a

flywheel device) to 15 of the 30 elite Swedish soccer players participating. Flywheel training

is proposed to allow for eccentric overload because it is possible to decelerate the flywheel

across a shorter range of motion then is used to accelerate it. Across the following season,

players in the intervention group suffered fewer hamstring strains (3 injuries in 15 players) than

those in the control group (10 injuries in 15 players). This study’s small size and the very high

rates of injury reported for control players (66%) are, however, reasons for concern regarding

the reproducibility of these results.

A number of subsequent large-scale studies employing the NHE have reported benefits

of eccentric conditioning, particularly when compliance is adequate (Arnason et al., 2008a;

Petersen et al., 2011; Seagrave et al., 2014; van der Horst et al., 2015b). In the first of these

studies, Arnason and colleagues (2008), reported that Icelandic and Norwegian soccer teams

that completed a 10-week progressive intensity NHE program in pre-season and then continued

to incorporate a lower volume of the exercise in-season, experienced 65% fewer hamstring

strains than teams that did not (RR = 0.35, 95%CI = 0.2-0.6). In a subsequent investigation,

Petersen and colleagues (2011) randomly assigned 461 of 942 sub-elite Danish soccer players

into a ten-week Nordic hamstring training programme during pre-season. Players who

completed the training suffered 71% fewer first-time and 85% fewer recurrent hamstring

injuries than players in the control group. More recent work by van der Horst and colleagues

(2015) randomly allocated 292 of 597 sub-elite Danish soccer players to a 13-week NHE

36

programme. This study reported that players who completed the intervention experienced 69%

fewer HSIs that those who did not (OR = 0.3, 95% CI = 0.1-0.7).

Contrary to the findings above, two prospective studies employing the NHE have found

no significant effect on hamstring injury rates (Engebretsen, Myklebust, Holme, Engebretsen,

& Bahr, 2008; Gabbe, Branson et al., 2006). However, both of these studies were confounded

by very poor rates of player compliance. For example, Engebretson and colleagues (2008),

assigned 85 of 161 elite to sub-elite Norwegian soccer players to a 10-week Nordic hamstring

protocol and reported no reduction in injury rates as a consequence of the intervention (RR,

1.6; 95% CI = 0.8-2.9). However, in this study, only 20% of players in the intervention group

completed the injury prevention programme. Gabbe and colleagues (2006), also observed no

benefit of the Nordic exercise on hamstring injury rates in 114 of 220 community level

Australian Rules Football players (RR = 1.2, 95%CI = 0.5-2.8). However, the training

programme employed in this study was not designed to improve eccentric strength as only five

sessions were planned over a 12-week period (Engebretsen et al., 2008). Furthermore, less than

one in 10 players completed the intervention. A recent meta-analysis on eccentric interventions

was conducted on randomised controlled trials with eccentric hamstring interventions (Goode

et al., 2015). This analysis included the Askling et al. (2003), Engebretsen et al. (2008), Gabbe

et al. (2006), and Petersen et al. (2011) studies. Overall, the results suggested no significant

effect of eccentric hamstring training, although significant heterogeneity was observed and a

significant positive effect of eccentric hamstring training became evident when compliance

was accounted for (Goode et al., 2015).

Eccentric conditioning has also proven effective in several rehabilitation protocols. In

2013, Askling and colleagues (2013), assigned 75 previously injured Swedish soccer players

to either an L Protocol (exercises at longer hamstring muscle lengths called ‘the diver’ and one

with an eccentric bias known as , ‘the glider’) or the C Protocol (conventional and short-length

37

exercises ‘contract/relax stretching’, ‘cable hip extension’, ‘pelvic tilt’). Participants in the L

Protocol had a shorter return to play time compared to participants in the C protocol with 28 ±

15 days and 51 ±21 days respectively, although, the C Protocol group recorded only one injury

compared with zero injuries after the L protocol. The major difference between the L and C

protocols was therefore in return to play time, rather than reinjury rate. Eccentric hamstring

exercise, often in the form of the NHE, has also been part of successfully trialled rehabilitation

programs reported by Mendiguchia and colleagues (2017) and Silder and colleagues (2013).

However, the multifaceted nature of these programs prevents firm conclusions from being

made as to the contribution of the eccentric hamstring exercises.

2.7 ASSESSING DEFICITS IN HAMSTRING FUNCTION AFTER INJURY

Rehabilitation for HSI has historically been directed by observations of pain and altered

hamstring function post-injury. For example deficits observed in eccentric strength and

flexibility have prompted the development of protocols that focus on these (Arnason et al.,

2008a; Askling, Karlsson, & Thorstensson, 2003; Askling et al., 2013; Malliaropoulos et al.,

2004; Mendiguchia et al., 2017; Mjølsnes, Arnason, Raastad, & Bahr, 2004; Petersen et al.,

2011; van der Horst et al., 2015a). There is still a gap in the literature regarding strength-

endurance deficits post-injury. Previous work by Freckleton and colleagues suggested poor hip

extensor endurance, as measured by a supine bridge test, may be a risk factor for future HIS

(Freckleton, Pizzari, Cook, & Young, 2011). However, the effects of HSI on eccentric knee

flexor strength-endurance are unknown. If such deficits are present after HSI, it would seem

wise to incorporate exercises with positive effects on this performance parameter.

As mentioned previously, knee-flexor strength deficits have sometimes been observed

in eccentric contraction modes with little to no effect on concentric contractions. Post-injury

eccentric knee-flexor strength deficits have been exhibited in both isokinetic and NHE tests,

38

yet the long-term effects of injury on isometric strength is less thoroughly researched (Charlton

et al., 2018). It is possible that isometric tests could be employed more frequently than eccentric

tests because the former result in little to no muscle soreness by comparison with eccentric

ones (Charlton et al., 2018). While this may be advantageous in busy training schedules, it is

possible the deficits in isometric strength may, like concentric deficits, be smaller than those

observed in eccentric tests. The value of isometric testing in previously injured muscles

requires further investigation to ascertain its worth in rehabilitation and return to play protocols.

2.8 BIOFEEDBACK

Biofeedback, otherwise known as augmented feedback, real-time and extrinsic

feedback has been used in the rehabilitation of many injuries. Biofeedback in rehabilitation

involves quantifying physiological and biomechanical measurements in real-time and

presenting information that might otherwise be unknown to patients or athletes. In some cases,

biofeedback is used to make research participants or patients aware of factors that are under

control of the autonomic nervous system (Giggins, Persson, & Caulfield, 2013; Onate,

Guskiewicz, & Sullivan, 2001). Biofeedback has been utilised to aid rehabilitation otherwise

delayed by atherogenic muscle inhibition, or between limb imbalances in muscle activation

39

(Ekblom & Eriksson, 2012; Gabler et al., 2013; Giggins et al., 2013; Hopkins & Ingersoll,

2010; Hopper, Berg, Andersen, & Madan, 2003; Lepley, Gribble, & Pietrosimone, 2012).

There are many modes of biofeedback that can be used to rehabilitate inhibited muscles, such

as visual force readings, audio, and tactile feedback but most common is electromyographical

biofeedback (EMGBF) (Gabler et al., 2013; Giggins et al., 2013).

2.8.1 PROPOSED MECHANISM OF BIOFEEDBACK IN STRENGTH

REHABILITATION

The exact neuromuscular mechanism(s) by which biofeedback alters performance are

not fully understood, but many believe that feedback allows the patient to better understand

muscular and strength deficits, allowing them to focus on different aspects of motor control

(Gabler et al., 2013; Lucca & Recchiuti, 1983; Pietrosimone, McLeod, & Lepley, 2012). The

awareness of the deficits may motivate the patient/athlete and consequentially increase

activation of the affected muscles (Gabler et al., 2013; Giggins et al., 2013; Lepley et al., 2012;

Lucca & Recchiuti, 1983).

Biofeedback in rehabilitation is thought to alter the cortical control used in the

generation of force (Croce, 1986; Gabler et al., 2013; Kleim et al., 2002). Cortical topography

excitability studies have shown post-injury decreases in the activity of the area of the cortex

responsible for activation of muscles surrounding injured joints after periods of immobilisation

or reduced voluntary activation (Liepert, Tegenthoff, & Malin, 1995; Roberts et al., 2007). This

process appears to be reversed after specific training (activity-dependent) for the affected

muscle area (Cooke & Bliss, 2006; Gabler et al., 2013; Kleim et al., 2002) and it is possible

that biofeedback-enhanced rehabilitation may have a role in optimising these changes.

There is evidence for positive effects of biofeedback in the rehabilitation of strength in

the injured and in the training of uninjured persons (Giggins et al., 2013). For example,

40

biofeedback in the form EMG has been used to increase quadriceps strength after knee injuries

(Akkaya et al., 2012; Ekblom & Eriksson, 2012; Giggins et al., 2013; Hopkins & Ingersoll,

2010; Kirnap, Calis, Turgut, Halici, & Tuncel, 2005; Lepley et al., 2012). Post-operative or

post-injury reductions in the vastus medialis oblique (VMO) activation have been noted, and

biofeedback programs have been reported to increase the VMO/VL EMG ratio during knee

extension exercises (Draper & Ballard, 1991; Ng, Zhang, & Li, 2008; Wise, Fiebert, & Kates,

1984). Increasing the VMO/VL sEMG ratio between the aforementioned muscles is proposed

to reduce symptoms of patellofemoral pain, reduce the risk of re-injury after ACL

reconstruction and arthroscopic meniscectomy (Ingersoll & Knight, 1991; Kirnap et al., 2005).

FIGURE 1: Changes in VMO/VL sEMG ratio for an exercise group and an exercise + biofeedback group in patellofemoral pain sufferers with and without sEMG biofeedback. There was a significant improvement only in the exercise + biofeedback group (Ng et al., 2008).

Kinrap and colleagues (2005) added EMG biofeedback of VMO and VL muscles to the

post arthroscopic meniscectomy rehabilitation for 20 patients. The feedback group (n=20)

exhibited a significant increase in maximum isometric strength and increased scores on the

Tegner-Lysholm knee function test compared to the traditional rehabilitation control group

(n=20). Patellofemoral pain patients also benefited from biofeedback correction of voluntary

41

activation levels between VMO to VL (Ng et al., 2008). The pre- and post-testing involved

collecting EMG data from participants as they conducted six hours of activities of daily living.

The biofeedback group displayed a significantly greater VMO/VL ratio compared to baseline,

while the non-biofeedback group had insignificant changes as seen in Figure 1.

The results of Ng et al. (2008) and Kinrap et al. (2005) are consistent with others aiming

to selectively increase muscle activation or strength in affected lower limbs to aid in the

rehabilitation process (Akkaya et al., 2012; Draper & Ballard, 1991; Ingersoll & Knight, 1991;

Jeyanthi, Natesan, & Manivannan, 2014; Wise et al., 1984). Nevertheless, there is some

evidence to refute the efficacy of biofeedback in a clinical setting with further research with

larger sample sizes are required to determine the efficacy of biofeedback in rehabilitation

(Giggins et al., 2013; Lepley et al., 2012). Furthermore, the application of biofeedback to HSI

is limited or non-existent.

Biofeedback has not been limited to rehabilitation of injured limbs. Healthy subjects

have also used biofeedback to increase strength, power and muscle activation (Croce, 1986;

Draper & Ballard, 1991; Ekblom & Eriksson, 2012; Hobbel & Rose, 1993; Hopper et al., 2003;

Kellis & Baltzopoulos, 1998; Randell, Cronin, Keogh, Gill, & Pedersen, 2011). Isokinetic knee

flexion and extension movements were examined amongst in 15 female subjects with

biofeedback applied to the vastii muscles in an attempt to increase strength, motor output and

activation (Ekblom & Eriksson, 2012). The biofeedback group displayed significantly greater

increases in knee extensor strength in both eccentric and concentric muscle contractions modes

than the control group, and this effect was particularly pronounced for eccentric strength

(Ekblom & Eriksson, 2012).

The findings are consistent with a study of similar participants that supported the

efficacy of visual feedback in increasing acute force productions in eccentric knee flexion and

extension movements (Hopper et al., 2003). Eccentric muscle activation measured by EMG

42

feedback and eccentric strength exhibit a more pronounced benefit from real-time feedback

than concentric and isometric muscle activation (Ekblom & Eriksson, 2012; Kellis &

Baltzopoulos, 1998).

A more recent study examining the transfer effects of biofeedback in training to sports

specific testing found significant improvements compared to a training only group (Randell et

al., 2011). Rugby union players were split into two groups and received peak velocity feedback

during squat jump training. At the end of a six-week training block a variety of sprint and

jumping tests were conducted with more pronounced improvements in the 10, 20 and 30 m

sprint trials in the experimental than the control group (1.3% vs. 0.1%, 0.9% vs. 0.1% and 1.4%

vs. -0.3% respectively (Randell et al., 2011). Randell and colleagues (2011) suggest the use of

biofeedback led to greater adaptations and effects than training alone and that this could

translate into an increase in sporting performance.

Overall, biofeedback can be used to increase strength, power, and activation both

bilaterally and unilaterally in the lower limb muscles. The efficacy of biofeedback in healthy

and unhealthy populations supports its value in addition to traditional rehabilitation exercises.

It remains to be seen if biofeedback can be successfully applied to hamstring strain injury

training and rehabilitation, particularly in athletes already accustomed to performing eccentric

exercises.

2.9 THE GAPS IN CURRENT LITERATURE.

The loss of eccentric strength and reductions in fascicle length after HSI have been

proposed to contribute to high rates of hamstring injury recurrence (Fyfe et al., 2013). It has

additionally been proposed that a shift in the knee flexor JAPT also occurs after HSI (Brockett

et al., 2001; Brughelli et al., 2010; Brughelli et al., 2009; Friden & Lieber, 1992; Fyfe et al.,

2013; Morgan, 1990), however, the evidence for this is extremely limited (Brockett et al., 2001;

43

Brughelli et al., 2009) and the dynamic method employed to determine JAPT is questionable

because it is sensitive to the rate of torque development and not determined entirely by the

force-length relationships of the hamstring muscles (Timmins et al., 2016). Additionally Yeung

and colleagues (2009), prospectively investiageted the role of JAPT in sprinters and resported

that JAPT had no bearing on injury risk. A review into the JAPT measure and the effect of

previous injury has suggested more investigation is required to understand the relationship

between JAPT and hamstring strain injury (Timmins, 2016). To this author’s knowledge, shifts

in the knee flexors’ isometric torque-joint angle relationship have not been demonstrated after

HSI.

The NHE is typically performed with the assistance of a partner restraining the ankles,

or with an external restraint on the ankles (Arnason et al., 2008a; Petersen et al., 2011; van der

Horst et al., 2015b). Despite the success of the exercise in reducing recurring injury rates

(Arnason et al., 2008a; Petersen et al., 2011; van der Horst et al., 2015b) it does not give the

performer feedback about between-limb imbalances or force outputs. When performed without

feedback it is possible that participants may rely heavily on a stronger limb with relatively little

activation of previously injured hamstring muscles. Recent developments have seen a novel

device (Opar, Piatkowski et al., 2013) give NHE participants instantaneous feedback of their

force outputs throughout the exercise. The acute benefits of biofeedback on eccentric and

isometric strength are yet to be examined in either uninjured or previously injured athletes after

a hamstring injury, and it is possible that using feedback during the NHE could impact the

performance of the exercise and thereby influence its benefits.

Another concern with the NHE is the extent to which it causes fatigue, however, the

only study to have examined this to date employed participants who were not accustomed to

the exercise (Marshall, Lovell, Knox, Brennan & Siegler, 2015). The effect of prior HSI on

strength loss during the NHE is also unknown. The main intervention studies that are the basis

44

for the NHEs implementation reach prescriptions of three sets of 10–12 repetitions (Mjølsnes,

Arnason, Raastad, & Bahr, 2004; Petersen, Thorborg, Nielsen, Budtz-Jørgensen, & Hölmich,

2011; van der Horst, Smits, Petersen, Goedhart, & Backx, 2015), however, the prescription of

more than six repetitions per set is unusual in high level sport. It remains to be seen what

influence that set and repetition prescriptions (e.g. 3 x 10 v 5 x 6) have on strength loss during

NHE sessions. It is possible that the performance of fewer repetitions per set will allow for

higher forces and torques to be maintained across training sessions, although this possibility

has not been tested.

The main objectives of this program of research are:

1) To investigate the proposed post HSI shifts in JAPT should they occur, and determine

if these shifts can be observed by isometric measures.

2) Can tests which were formally exercises be conducted utilising a instrument Nordic

Hamstring Device, and are these tests sensitive to the observed alterations in isometric

and eccentric strength post HSI?

3) Monitor the real-time effects of the NHE on force output, knee angle, knee angle

velocity and sEMG during 30 repetitions of the NHE performed in sets of medium or

high repetitions and investigate whether the protocols differentiate in the above

variables.

4) Observed in real-time the effects of prior HSI on performance of the NHE across 30

repetitions.

5) Implement visual biofeedback of force traces during the NHE and observe it’s effect

on NHE performance in those with a history of prior HSI.

45

CHAPTER 3: KNEE-FLEXOR FATIGUE DURING THE NORDIC HAMSTRING EXERCISE

3.1 RESEARCH OBJECTIVES

3.1.2 OBJECTIVES

1) To observe the knee flexor force production and sEMG output during the

performance of 30 repetitions of the NHE when performed in two different prescriptions (3

sets of 10 repetitions and 5 sets of 6 repetitions)

3.1.3 PARTICIPANTS

Fourteen recreationally active, adult males who were participating in moderate to high

levels of physical activity twice or more per week and who had previously used the NHE in

their training programs were recruited for this study. Participants completed an injury

questionnaire and were free of lower limb pathologies, and none had a history of HSI or serious

knee injury. A cardiovascular screening questionnaire was also completed before participation.

All gave informed consent to participate in this study which was approved by the Queensland

University of Technology Human Research Ethics Committee (approval number 1600000767).

3.1.4 METHODOLOGY

Participants, who were already familiar with the exercise and protocols from previous

participation (within the previous 6 months) in the research group’s projects, visited the

laboratory on two occasions three weeks apart. For both visits, the participants initially

performed a warm-up consisting of five minutes of self-paced submaximal cycling. They then

performed two isometric maximal voluntary contractions of the knee-flexor muscles in a prone

position (knees fully extended), with one minute rest between repetitions (Figure 2 below). The

46

isometric contractions were performed for the subsequent normalisation of sEMG obtained

from the NHE.

FIGURE 2: Prone isometric test on hamstring testing device. Participants pulled their legs up against the restraints around the ankle .

FIGURE 3: Nordic hamstring exercise on hamstring testing device. Participants pulled against ankle restraints to slow their fall as much as possible.

Participants then performed 30 repetitions of the NHE, arranged into five sets of six

repetitions on one laboratory visit and three sets of ten repetitions on the other visit. Three

minutes of rest was allocated between sets. The presentation order of the exercise prescription

(3×10 or 5×6) was randomised (see figure 4). Participants were self-paced throughout the

repetitions and not required to adhere to a metronome or other pacing device.

An electrogoniometer (PRV6 5K potentiometer) fixed to the left knee measured knee

angle throughout the exercise sessions . The knee-flexor forces at the ankles were measured

47

with uniaxial load cells (MLP-1K, Transducer Techniques, CA, USA) attached in-series to

ankle straps. The middle of each ankle strap was aligned with the lateral malleoli, and the ankle

restraints were vertical and perpendicular to the shank. Surface electromyographic (sEMG)

information was collected via bipolar pre-gelled Ag/AgCl sEMG electrodes (10 mm diameter,

20 mm inter-electrode distance) placed over the bellies of the semitendinosus and biceps

femoris muscle on the posterior thigh half way between the ischial tuberosity and tibial

epicondyles. The reference electrode was placed on the ipsilateral head of the fibula.

All sEMG, force and joint angle data was sampled at 1000 Hz via a 16-bit PowerLab

26T AD unit (amplification = 1000; common mode rejection ratio = 110 dB) and analysed

using LabChart 7 (ADInstruments, New South Wales, Australia). Raw sEMG data was Bessel

filtered (frequency bandwidth = 10–500 Hz) and then full-wave rectified and smoothed over

100ms windows. Knee angle data were low pass filtered at 4 Hz. All data was then transferred

to a personal computer.

3.1.5 DATA ANALYSIS:

The peak forces (N) for each repetition of the NHE for each participant were derived

by taking the maximum or peak value for the summed forces (left + right limb) for each

repetition. The corresponding knee angle and knee angle velocity at these peak forces were

also determined. The data were exported into Microsoft Excel and SPSS for statistical analysis.

Surface Electromyography

Smoothed rectified sEMG data was averaged over 0.5 seconds before the peak forces

in all dynamic exercise efforts (NHE). The sEMG data obtained from the NHE was then

normalised to that obtained from the prone maximal isometric contractions at the knee angle

48

of 00. For all prone isometric contractions, sEMG data was averaged over the 0.5 seconds

surrounding the peak force of each contraction, (0.25 seconds either side of the peak).

3.1.6 STATISTICAL ANALYSIS

Strength Measures

Statistical analysis was performed using SPSS version 23.0.1 (IBM Corporation,

Chicago IL). The normality of the data was assessed with the Shapiro-Wilks test. Sphericity

was assessed via Mauchly's Test of sphericity and when sphericity wasn’t observed the Huynh-

Feldt correction was used.

For the purposes of analysing force decline within sets, the average of the first two and

the last two repetitions was used. To ascertain the differences in force output across the thirty

repetitions, the average of repetitions 1 & 2 and 29 & 30 were employed. The effects of time

(strength loss) and session type (3x10, 5x6) on peak eccentric knee-flexor force were

determined by two way repeated measures analyses of variance (ANOVA). The same analyses

were conducted for knee angles and knee angle velocities of peak force. When significant main

effects were detected, post hoc t-tests with Bonferroni corrections were employed for pair-wise

comparisons. The mean differences were reported with their 95% confidence intervals (CIs).

For sEMG data, the effects of time (strength loss) and session type (3x10, 5x6) and

muscle (lateral, medial) were determined by a three-way repeated measures analysis of

variance (ANOVA). When significant main effects were detected, post hoc t-tests with

Bonferroni corrections were employed for pair-wise comparisons. The mean differences were

reported with their 95% confidence intervals (CIs).

49

3.2 RESULTS

Participants

The anthropometric characteristics of the participants are detailed in Table 1.

Table 1 :Participant Anthropometric Information

Age (Years) Height (cm) Body Mass (kg)

Mean 23.50 178.00 74.60

SD 4.00 6.50 17.20

Strength Measures

Table 2: Maximal Voluntary Contractions (Prone) – Descriptive Statistics

3x10 Protocol Mean (N) SD (N) CoV

Left Limb 348.05 99.10 28.47

Right Limb 369.60 100.96 27.32

Combined 752.80 171.08 22.73

5x6 Protocol

Left Limb 319.96 95.58 29.87

Right Limb 547.43 204.12 37.29

Combined 672.10 207.11 30.82

SD = Standard deviation CoV = Coefficient of variance

There were no observed differences in the average of summed peak eccentric knee-

flexor forces across 30 repetitions between the two exercise protocols, (mean difference = -

50

0.77N, 95% CI = -5.90 to 5.74; p= 0.97) as seen in Figure 5. There were significant declines in

strength between the first repetitions (1 & 2) and the last repetitions (29 & 30) with both

protocols, with a mean decline of -85.1N (11.3%), (95% CI = -166.24 to -3.957; p = 0.04)

during the 3x10 protocol and -69.3N (9.3%), (95% CI = -131.23 to -7.38; p = 0.03) during

the 5x6 protocol.

FIGURE 4: Average of summed eccentric knee-flexor forces for all 30 repetitions for the 3x10 and 5x6 protocols. Bars represent means and error bars represent the standard deviation.

0

100

200

300

400

500

600

700

800

900

Sum

med

Ecc

entr

ic K

nee-

Flex

or F

orce

(N)

Protocol

3 x 10 repetitions5 x 6 repetitions

51

FIGURE 5: Eccentric knee flexor forces in the first two and last two repetitions of the 3x10 and 5x6 protocols. Bars represent means and error bars represent the standard deviation. * p = 0.04, ** p = 0.03 for the differences between the forces generated in the first and last two repetitions for each protocol.

* **

52

FIGURE 6: Averaged summed eccentric knee-flexor force per repetition for each exercise prescription Bars represent group means, error bars represent the standard deviation (SD)

0

100

200

300

400

500

600

700

800

900

1000

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30

Sum

med

Ecc

entr

ic K

nee F

lexo

r Fo

rce

(N)

Repetitions

3 x 10repetitions

5 x 6repetitions

53

Knee angle at peak summed force

The summed knee flexor forces reached their peaks at 40o ± 15o and 45o ± 12o in the first

two repetitions of the 5x6 and 3x10 protocols, respectively. The corresponding knee angles in

the final two repetitions were 47o ± 15o and 49o ± 15o of the 5x6 and 3x10 protocols,

respectively. There was no significant main effect for protocol on knee angles of peak force

(mean difference = 3o; 95% CI = -3o to 9o, p = 0.345). There was no main effect for time on

knee angle of peak force (mean difference = 5o; 95% CI = -1o to 11o, p = 0.091). However, for

the final two repetitions of the 5x6 protocol, knee angle of peak force was significantly more

flexed than the first two reps (mean difference = -7o, 95% CI = -11o to -2o, p = 0.013). No

significant difference in knee flexion angle was observed between the first and last two

repetitions of the 3x10 protocol (mean difference = -3o, 95% CI = -13o to 6o, p = 0.438).

FIGURE 7: Averaged knee angle at peak summed force for each exercise prescription Bars represent group means, error bars represent the standard deviation (SD) * = 0.013

0

10

20

30

40

50

60

70

First Repetitions Last Repetitions

Kne

e Ang

le a

t Sum

med

pea

k fo

rce

(deg

rees

/seco

nd) 3x10

Repetitions

5x6Repetitions

*

54

FIGURE 8: Averaged knee angle velocity at peak summed force for each exercise prescription - Bars represent group means, error bars represent the standard deviation (SD) * = 0.001 ** = 0.004

Knee angle velocity at peak summed force

The summed knee flexor forces reached their peaks whilst falling at a velocity -20o.s-1±

16o.s-1 and -17o.s-1 ± 8o.s-1 in the first two repetitions of the 5x6 and 3x10 protocols,

respectively. The corresponding velocities in the final two repetitions were -40o.s-1 ± 14o.s-1 and

-38o.s-1 ± 38o.-1 of the 5x6 and 3x10 protocols, respectively. There was no significant main

effect for protocol on knee angles of peak force (mean difference = 2o; 95% CI = -13o to 17o,

p = 0.722). There was a main effect for time on the velocity at peak summed force (mean

difference = 20o.s-1; 95% CI = 8o.s-1 to 33o.s-1, p = 0.004). More specifically, the 5x6 protocol

showed a significant increase in the velocity at peak summed force between the first two

repetitions and the last two repetitions (mean difference = 20o.s-1; 95% CI = 10o.s-1 to 31o.s-1,

p = 0.001). However, despite it being very similar in size, the increase in velocity observed

-55

-45

-35

-25

-15

-5

First Repetitions Last RepetitionsVe

loci

ty a

t Sum

med

Pea

k Fo

rce

(deg

rees

/seco

nd)

3x10Repetitions

5x6Repetitions

** *

55

within the 3x10 protocol was not statistically significant (mean difference = 21o.s-1; 95% CI =

-0.1o.s-1 to 42o.s-1, p = 0.051).

Surface Electromyography

Normalised sEMG, as an average across all 30 repetitions, was not significantly

different for the medial hamstrings between the 3x10 (0.92 ± 0.05) and 5x6 (0.94 ± 0.05)

protocols (mean difference = 0.02, 95% CI = -0.048 to 0.001; p = 0.054). In contrast, the

normalised BFlh EMG was significantly lower for the 3x10 (0.71 ± 0.03) compared to 5x6

(0.85 ± 0.04) protocol across the 30 repetitions (mean difference = 0.14, 95% CI = 0.164 to

0.125; p <0.01) (see Figures 9 and 10).

56

FIGURE 9: Average normalised sEMG for all 30 repetitions of the 3x10 and 5x6 protocols. Bars represent means and error bars represent standard deviation. MH = Medial Hamstrings, BF = Biceps Femoris. * p < 0.01.

0

0.2

0.4

0.6

0.8

1

1.2

Bflh nEMG MH nEMG

nEM

G

3x10 repetitions

5x6 repetitions

*

57

FIGURE 10: Normalised Surface EMG for 30 repetitions for the 3 x 10 and 5 x 6 protocols, for the BF and MH. Error bars are omitted for the sake of clarity.

0

0.2

0.4

0.6

0.8

1

1.2

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30

nEM

G

Repetitions

3 x10 BicepsFemoris

3x10 MedialHamstrings

5 x6 BicepsFemoris

5x6 MedialHamstrings

58

3.3 DISCUSSION

Despite the prescription of 3 sets of ~10 repetitions of the NHE in randomised

controlled trials (RCTs) (Mjølsnes et al., 2004; Petersen et al., 2011; van der Horst et al., 2015),

it is more common for supramaximal eccentric exercise to involve fewer repetitions per set

(e.g.3-6 repetitions) in athlete training programs. However, the results of the current study

suggest, contrary to the hypothesis, that there are minimal differences in knee extensor torque

and muscle forces between training sessions involving sets of 10 and 6 repetitions per set when

a total of 30 repetitions is completed. Furthermore, the knee angles of peak force did not change

significantly for either protocol and were not significantly different between the protocols. The

knee angle velocity at the summed peak force did increase significantly throughout both

protocols but it did not change to a different extent between protocols.

McNeil and colleagues (2004) have reported that work to rest ratios have minimal

impact on dorsiflexor torque output when eccentric contractions are performed and the current

results, for the knee-flexors, are consistent with this. Presumably, this is because muscle

damage rather than metabolic stress is the main cause of reduced performance with repeated

eccentric contractions which are energy efficient (McNeil, Allman, Symons, Vandervoort, &

Rice, 2004; Warren, Ingalls, Lowe, & Armstrong, 2002). Compared to isometric and concentric

contractions, repeated eccentric contractions are unique in their capacity to induce muscle

damage and they also produce higher forces per active muscle fibre at a low metabolic cost

(Lieber & Fridén, 2002; McNeil et al., 2004; Newham, Mills, Quigley, & Edwards, 1983;

Warren et al., 2002). Conventional fatigue from metabolic stress is proposed to be the largest

contributor to impaired performance in repeated concentric and isometric contractions whereas

muscle damage is observed to be the main contributor to impaired performance after repeated

eccentric contractions (Warren et al., 2002). The proposed mechanism behind muscle damage

59

induced fatigue post eccentric activity is the disruption and consequential dysfunction of the

excitation-contraction coupling mechanism (Warren et al., 2002). Strength losses caused by

fatiguing concentric or isometric activities are observed during and immediately post exercise,

and they tend to recover rapidly upon cessation of activity. By contrast, the loss in maximal

torque generating capacity caused by repeated eccentric contractions may be small to moderate

acutely and develop later and last significantly longer, even up to 96 hours (McNeil et al.,

2004). In conventional exercise involving significant concentric or isometric contractions, the

work to rest ratios significantly influence muscle fatigue (Bigland-Ritchie, Rice, Garland, &

Walsh, 1995; McNeil et al., 2004). However, eccentric contractions seem to be largely

unaffected by rest periods between the repeated efforts, further reinforcing that muscle damage

is the main contributor to observed strength loss or lack thereof (McNeil et al., 2004; Teague

& Schwane, 1995). In the current study, which employed participants who were familiar

(within the previous month) with the performance of the NHE, the decline in peak forces was

very modest, and this suggests that either exercise session induced minimal muscle damage.

The results of this study provide novel insight into the effects of fatigue on performance

of the NHE. The two protocols used, 3 sets of 10 repetitions and 5 sets of 6 repetitions, had no

significantly different effects on strength loss. This suggests the possibility that neither protocol

has obvious advantages over the other, although the higher repetition option would allow 30

repetitions to be performed in a shorter time frame.

Prior to this work no study had assessed the strength losses incurred during NHE

without confounding effects from testing protocols such as repeated eccentric or concentric

efforts. One group has investigated the acute fatiguing effects of the NHE by having

participants perform 6 sets of 5 repetitions and assessing strength between sets with concentric

and eccentric efforts. Marshall and colleagues (2015), found after the first set of NHE, a

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significant 7.9 - 17% reduction in eccentric torque with no further significant reductions for

the subsequent sets (Marshall, Lovell, Knox, Brennan, & Siegler, 2015). The authors did note

that significant differences from pre-exercise values were found during eccentric actions in the

later 60 degrees of the range of motion and throughout concentric actions. As only eccentric

forces were measured in the current study, it is not possible to know whether the participants

experienced a loss of concentric strength.

In the current study, peak knee flexor forces declined to a small extent across the 30

maximal repetitions of the NHE while the velocity at which these forces were reached changed

more significantly. Given the shape of the force-velocity curve for slow and medium speed

eccentric actions, it seems likely that reductions in force generating capacity were counteracted

by increases in knee angle velocity. Lengthening actions at approximately -20o.1 are typically

weaker than those performed at -40 to -60o.1, and these velocities were observed in the current

investigation. This effect of velocity may lead to under estimation of the strength loss incurred

during the NHE (Westing, Serger, Kalson, Ekblom, 1998).

One statistically significant difference between the two exercise protocols was the level

of normalised BFlh sEMG. While the normalised MH sEMG did not differ between protocols,

there was a lower BFlh EMG in the 3 sets of 10 protocol than the 5 sets of 6 protocol. The

practical significance of this difference, given that forces were not different between protocols,

is unclear. However, this may suggest some potential advantages to performing fewer

repetitions per set in this exercise, but more investigation is required before this can be stated

with certainty. Any potential advantages of a lower repetition prescription should be

investigated because 3 sets of 10 are prescribed in weeks 5 to 10 of the hamstring prevention

programs employed in the Nordic hamstring RCTs (Petersen et al., 2011; van der Horst et al.,

2015b). It is thought that at least some of the benefits of eccentric training are mediated by

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architectural changes such as the addition of in-series sarcomeres (and resulting lengthening of

fascicles) within the BFlh (Bourne et al., 2016). Higher levels of BFlh activation with the lower

repetition range employed in this study might, on their own suggest some advantages for injury

prevention programs but more work is needed to substantiate this, and the lack of a difference

in force outputs is difficult to reconcile with the differences in sEMG.

The optimal placement of hamstring injury prevention exercises within training

sessions isn’t known, but some injury prevention programs such as the FIFA 11+ prescribe

NHE in addition to 11 other exercises during the warm-up period (Bizzini et al., 2013;

Impellizzeri et al., 2013). While the FIFA 11+ plus program doesn’t prescribe 30 repetitions,

it does call for up to 12 repetitions in a single set. If there is an element of hamstring fatigue or

weakness from the NHE in addition to the other exercises performed, it is possible that these

muscles may be placed at risk in the following training session. The BFlh goes through the

greatest amount of strain of all hamstring muscles (Chumanov et al., 2011; Schache et al., 2012;

Thelen et al., 2005) during the late swing phase of gait with the hamstring muscle group acting

eccentrically to decelerate the forward swinging shank (Chumanov et al., 2011; Dolman et al.,

2014; Thelen et al., 2005). If the hamstring muscle group is weakened, it would potentially

reduce the capacity to decelerate the shank. Reduced deceleration capacity may stretch muscle

fibres and their sarcomeres beyond optimal lengths, resulting in an accumulation of

microscopic tears which could potentially accumulate and then result in HSI. The current

results suggest, however, that strength loss from a single set of 10 repetitions or two sets of six

repetitions is minimal in athletes who are accustomed to performing this exercise.

Having the capacity to measure eccentric strength during the NHE and the muscle

activation via sEMG, in real-time, has provided some insight into the acute fatigue effects of

the NHE on the hamstring muscle group. However, there are some limitations to this

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investigation that should be acknowledged. The current study utilised sEMG to attain insight

into muscle activation and this method is prone to cross-talk so that some of the signal is

actually ‘noise’ from adjacent muscles. Functional magnetic resonance imaging (fMRI) would

allow a measure of muscle activation with better spatial resolution, but this technique does not

provide a measure of muscle activation changes across time in the way that sEMG can. Another

limitation arises from the recruitment of recreationally active participants because it is not clear

whether these results would translate to elite sporting populations. However, the current

participants were accustomed to performing this exercise, and they had similar or even slightly

better eccentric strength than elite athletes in previous studies from this group (Opar et al.,

2105; Timmins et al., 2016).

While further investigation into the appropriate prescription and programming of the

NHE is needed, the current findings suggest that strength loss is minimal in recreational athletes

who are familiar with the exercise and that the prescription of 6 or 10 repetitions does not

appear to significantly influence the knee flexor forces or the degree of strength loss exhibited

during exercise sessions.

LINKING PARAGRAPH

We now know the effects of the NHE on healthy recreational athletes without a history

of HSI. However, it is not clear whether athletes with a history of HSI will display the same

responses. Previous history of HSI has been shown to increase the degree of force loss in bouts

of concentric knee-flexor exercise (Lord, Ma'ayah, & Blazevich, 2018), but we do not currently

know the effect of prior HSI on eccentric strength decline during exercise such as the NHE.

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CHAPTER 4: The Effects of Biofeedback and Previous Hamstring Injury on Eccentric Strength During a Nordic Hamstring Training Session

4.1 RESEARCH DESIGN

4.1.2 OBJECTIVES

1) To assess the effects of previous HSI on knee-flexor force production and hamstrings

sEMG during the performance of 30 repetitions of the NHE.

2) To assess the effects of real-time visual force biofeedback on knee-flexor forces and

hamstring muscle activation during the performance of 30 repetitions of the NHE.

3) To assess the biceps femoris architecture (fascicle length, fascicle length, and

pennation angle) in previous injured compared to the uninjured contralateral limb.

4.1.3 PARTICIPANTS

Fourteen recreationally active adult males with a history of unilateral HSI were

recruited for this investigation. Two participants were excluded from data collection after

familiarisation because of injuries sustained during participation in sporting activities unrelated

to this study. The sample size was chosen based upon previous and similar research conducted

in the laboratory. The participants gave informed consent to participate in the study which was

approved by the Queensland University of Technology Human Research Ethics Committee

(approval number 1600000767).

4.1.4 METHODOLOGY

Participants visited the laboratory on three occasions with the first and second visit

separated by one week and the second and third visit separated by three weeks. During the first

64

session, participants had ultrasound images taken midway along the longitudinal axis of the

BFlh muscle belly to assess fascicle length and pennation angle.

Images were taken using two-dimensional B-mode ultrasound (frequency, 12 MHz;

depth, 8 cm; field of view, 14×47 mm) (GE Healthcare Vivid-i, Wauwatosa, USA). The

scanning site was determined as the halfway point between the ischial tuberosity and the knee

joint fold, along the line of the BFlh. All architectural assessments were performed with

participants in a prone position and the hip neutral following at least five minutes of inactivity.

Following the ultrasound scans, participants warmed up by cycling at a submaximal pace for

five minutes. Participants then performed three to six repetitions of the NHE (NHE), under the

instruction of the investigator, to familiarise themselves with the appropriate technique

requirements of the exercise.

On the second and third visits to the laboratory, participants performed three sets of ten

repetitions of the NHE, once with (Figure 10) and once without visual feedback (Figure. 9) of

force production at the ankle. The order of presentation was randomised. The exercise

prescription of three sets of ten repetitions was chosen from the study in Chapter 3. The

prescription showed minimal changes in force out puts comparative to the alternate prescription

and is a common prescription observed in RCTs previously conducted by Mjolsnes et al.,

(2014) and Petersen et al., (2015). Upon arrival at the laboratory, participants initially

performed a warm-up consisting of five minutes of sub-maximal ad self-paced cycling.

Participants then performed two isometric maximal voluntary contractions of the knee-flexor

muscles in a prone position with one-minute rest between repetitions. Three maximal

repetitions of the Nordic Hamstring Curl were then performed followed by a five-minute rest,

after which participants completed three sets of ten repetitions of the NHE with one minute

rests between sets. Two prone, maximal isometric voluntary contractions of the knee-flexors

65

were performed after the NHE, one immediately after the final repetition of the NHE and the

other one minute later.

FIGURE 11: Nordic hamstring exercise on hamstring testing device. Participants pull against ankle restraints as they resist falling.

FIGURE 12: Nordic hamstring exercise with feedback displayed on a laptop in front of participant performed on hamstring testing device. Participants pull against ankle restraints as they resist falling.

An electronic goniometer (PRV6 5K potentiometer) fixed to the left knee measured

knee angle throughout the exercise sessions. The knee-flexor forces at the ankles were

measured with uniaxial load cells (MLP-1K, Transducer Techniques, CA, USA) attached in-

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series to ankle straps. The middle of each ankle strap was aligned with the lateral malleoli, and

the ankle restraints were vertical and perpendicular to the shank.

Surface electromyographic (sEMG) information was collected from the lateral and medial

hamstrings via bipolar pre-gelled Ag/AgCl sEMG electrodes (10 mm diameter, 20 mm inter-

electrode distance) placed over the appropriate muscle bellies halfway between the ischial

tuberosity and tibial epicondyles. The reference electrode was placed on the ipsilateral head of

the fibula.

All sEMG, force and joint angle data were sampled at 1000 Hz via a 16-bit PowerLab

26T AD unit (amplification = 1000; common mode rejection ratio = 110 dB) and analysed

using LabChart 7 (ADInstruments, New South Wales, Australia). Raw sEMG data were filtered

using a Bessel filter (frequency bandwidth=10–500 Hz) and then full-wave rectified and

smoothed over 100ms windows. Knee angle data were low pass filtered at 4 Hz. All data was

then transferred to a personal computer.

During the feedback session, participants were shown force traces from their left and

right legs superimposed in a single channel in real time (Figure 11) on a 1 7inch monitor for

easier reading. The overlay trace was derived from the real time left and right force traces

superimposed upon each other in the Labchart 7 software (ADInstruments, New South Wales,

Australia). Participants were instructed to “activate the injured limb to match its force trace to

your uninjured limb, without sacrificing the strength of your uninjured limb”. The force data

was presented to the participants at eye level via a computer screen.

67

FIGURE 13: Left leg (red in the top trace), right leg (blue in the middle trace) and left and right leg forces both shown within the one trace (bottom) for three consecutive repetitions of the Nordic hamstring exercise.

4.1.5 DATA ANALYSIS

Strength Measures

The peak forces (N) for each repetition of the NHE for each participant were derived

by taking the maximum value for the left and right limb at the peak of summed force for each

repetition. The data was then exported into Microsoft Excel and SPSS for statistical analysis.

Data for the prone maximal isometric contractions (MVIC) was the average force obtained

from the 0.5 seconds of data surrounding the peak force (0.25 seconds either side of the peak)

from each contraction. All isometric contractions were performed twice with the results

averaged. For the purposes of reviewing changes in force across the 30 repetitions of the NHE,

the first two repetitions and the last two repetitions of each set were averaged and are denoted

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by S1 (start or first two repetitions of set 1), E1 (end or last two repetitions of set 1), S2, E2,

S3 and E3.

Between limb asymmetry in force was derived from the point of peak summed force.

The injured limb’s force was compared to the uninjured limb’s force as a raw value and as a

percentage value.

Surface Electromyography

sEMG data were averaged across the 0.5 seconds of data before the peak in all dynamic

exercise efforts (NHE). The sEMG data obtained from the NHE was then normalised to that

obtained from the pre-exercise maximal isometric contractions. For all prone isometric

contractions, sEMG data were averaged across the 0.5 second period surrounding the peak

force. All isometric contractions were performed twice, and the average of the two contractions

was used for analysis.

Muscle Architecture

The MicroDicom software (Version 0.7.8) was used for analysing the ultrasound

images collected. Due to the limited view of the ultrasound probe a muscle fascicle of interest

was outlines and the muscle fascicle length was determined using the equation: FL=sin

(AA+90°) x MT/sin(180°-(AA+180°-PA)). Muscle Thickness (MT was defined by the as the

distance between the superficial and intermediate aponeuroses of the BFLH). The ultrasound

technician was blinded to all participants’ previous injury data.

4.1.6 STATISTICAL ANALYSIS

Strength Measures

Statistical analysis was performed using SPSS version 23.0.1 (IBM Corporation,

Chicago IL). The normality of the data was assessed with the Shapiro-Wilks test. Sphericity

69

was assessed via Mauchly's test and when sphericity was not observed the Huynh-Feldt

correction was used.

A repeated measures time (start of set 1 (S1), end of set 1 (E1), S2, E2, S3, E3) by leg

(injured v uninjured) by feedback condition analysis of variance (ANOVA) was employed to

assess whether there were differences in knee flexor force production.

Prone isometric strength was analysed via a time (Pre 1, Pre 2, Post 1, Post 2), limb

(injured vs uninjured) and condition (feedback vs no feedback) repeated measures analysis of

variance (ANOVA). When significant main effects were detected, post hoc t-tests with

Bonferroni corrections were employed for pair-wise comparisons. The mean differences were

reported with their 95% confidence intervals (CIs).

Surface Electromyography

Analysis of the prone isometric exercises was performed by a limb (injured vs

uninjured) by time (Pre-, post 0 and post 1 minute) by muscle (lateral and medial) repeated

measures analysis of variance (ANOVA).

Smoothed rectified sEMG data was averaged over 0.5 seconds before the peak forces

in all dynamic exercise efforts (NHE). The sEMG data obtained from the NHE was then

normalised to that obtained from the prone maximal isometric contractions at the knee angle

of 00. For all prone isometric contractions, sEMG data was averaged over the 0.5 seconds

surrounding the peak force of each contraction, (0.25 seconds either side of the peak).

When significant main effects were detected from ANOVAs, post hoc t-tests with

Bonferroni corrections were employed for pair-wise comparisons. The mean differences were

reported with their 95% confidence intervals (CIs).

70

Muscle Architecture

Measures of muscle architecture (fascicle length, muscle thickness, and pennation

angle) were analysed by comparing the injured to uninjured limbs via paired sample t-tests.

The mean differences were reported with their 95% confidence intervals (CIs).

4.2 RESULTS

Participants

All participants (age 23.5 ± 1.8 years, height 179.2 ± 5.7cm, body mass 83.1 ± 6.8 kg)

had a history of unilateral HSI to their right limb only, within the past 24 months. The average

time since the most recent insult was 8.3 ± 6.4 months with an average recovery time of 4.8 ±

2.9 weeks. Details of the participant’s injury information can be found in Table 2.

71

Table 3: Hamstring injury history information for all participants

Participant Injured Limb

Muscle injured

Number of HSIs

Months Since last HSI

Grade of last HSI

Rehabilitation time (weeks)

1 Right ST 2 18 2 10

2 Right BFlh 1 2 1 5

3 Right BFlh 2 2 1 5

4 Right BFlh 1 2 1 2

5 Right BFlh 3 12 2 4

6 Right BFlh 1 2 1 4

7 Right BFlh 3 18 1 4

8 Right BFlh 1 5 1 12

9 Right BFlh 2 12 1 3

10 Right BFlh 3 6 2 5

11 Right BFlh 1 18 1 3

12 Right BFlh 2 8 1 2

BFlh: Biceps Femoris Long Head ST: Semitendinosus

Rehabilitation time was defined by the length of time that it took to return to full training or

competition. The severity (grade) was determined by the American Medical Association's

guidelines (Craig, 1973)

72

Biceps femoris long head architecture

BFlh fascicles were significantly shorter (mean difference = -0.74 cm, 95% CI = -0.3

to -1.13; p = 0.001) and pennation angles significantly higher (mean difference = 1.11o, 95%

CI = 0.43 to 1.84; p = 0.005) in previously injured than the uninjured limbs. Muscle thickness

was not significantly different between limbs (mean difference = 0.014cm, 95% CI =-0.09 to

0.12; p = 0.769) (see Table 3).

Table 4. Architectural characteristics of biceps femoris long head muscles in previously injured and uninjured limbs.

Injured Limb Uninjured Limb p-value

BFlh Fascicle Length (cm) 9.25 ± 0.87 9.99 ± 0.64 0.001

Pennantion Angle (degrees) 16.39 ± 0.82 15.25 ± 1.05 0.005

Muscle Thickness (cm) 2.61 ± 0.33 2.63 ± 0.27 0.769

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Strength measures during exercise

There was no observed effect of previous injury on the knee-flexor force output across

the 30 repetitions of the NHE according to the mean forces obtained from the 30 repetitions

(Figure 13; mean difference = -2.50N, 95% CI =-46 .7 to 41.7; p = 0.910). There were

significant reductions in the mean knee-flexor force output over with time, although these did

not differ between injured and uninjured limbs. The mean force output declined from time point

1 (repetitions 1 & 2) to time point 4 (repetitions 19 & 20) with a mean difference of 27.8N

(95% CI = 17.8 to 41.3; p = <0.001). A statistically significant difference in mean force output

was observed between the 1st time point and time points 5 (repetition 21 & 22) (mean

difference = 35N, 95% CI= 17.8 to 52.1; p = <0.001) and 6 (repetitions 29 & 30) (mean

difference = 43.6N, 95% CI = 28.8 to 58.3; p = <0.001), respectively. There was also a

significant reduction in knee-flexor force between time point 3 (repetition 11 & 12) and 4

(repetitions 19 & 20) (mean difference = 15.2N (95% CI = 6.8 to 24.3; p = <0.001).

FIGURE 14: Knee flexor strength comparison between limbs (N) of all NHE repetitions performed. Bars represent group means, error bars represent standard deviation (SD).

0

50

100

150

200

250

300

350

400

Kne

e-Fl

exor

For

ce (N

)

UninjuredInjured

74

FIGURE 15: Knee-flexor eccentric force across time for NHE Bars represent group means, error bars represent standard deviation (SD) * = P <0.001

0

50

100

150

200

250

300

350

400

450

Time Point 1 (Rep 1&2)

Time Point 2 (Rep 9& 10)

Time Point 3 (Rep11 & 12)

Time Point 4 (Rep19 &20)

Time Point 5 (Rep21 &22)

Time Point 6 (Rep29 & 30)

Ecc

entr

ic K

nee-

Felx

or F

orce

(N)

No Feedback

Uninjured

No Feedback Injured

Feedback Uninjured

Feedback Injured

Total

*

*

*

*

75

FIGURE 16: Average summed eccentric knee-flexor force per repetition of the NHE Bars represent group means, error bars represent standard deviation (SD)

0

50

100

150

200

250

300

350

400

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30

Sum

med

Ecc

entr

ic K

nee-

Flex

or F

orce

(N)

Repetitions

NoFeedbackUninjuredNoFeedbackInjuredFeedbackUninjured

FeedbackInjured

76

Effect of feedback

There was no observed effect of real-time feedback throughout the NHE protocol on

peak knee-flexor forces across the 30 repetitions in the previously injured (mean difference =-

9.918N, 95% CI = -72.48 to 52.64; p = 0.751) or uninjured limbs (mean difference = 2.47N,

95% CI = -60.08 to 65.42; p = 0.937).

FIGURE 17: Comparison between feedback conditions for all 30 repetitions combined. Bars represent group means, error bars represent standard deviations (SD)

0

50

100

150

200

250

300

350

400

Ecce

ntri

c K

nee-

Flex

or F

orce

(N)

No FeedbackFeedback

77

Table 4: Pre and Post Exercise Isometric Contractions – Descriptive Statistics

Uninjured Limb (N) COV

Injured Limb (N) COV

No Feedback Condition

Pre Exercise Repetition 1 290.52 ± 71.69 24.6 283.56 ± 50.7 17.9

Pre Exercise Repetition 2 297.78 ± 52.25 17.55 289.91 ± 50.16 17.33

Post Exercise Repetition 1 256.91 ± 54.06 17.33 262.26 ± 53.54 20.42

Post Exercise Repetition 2 284.00 ± 54.73 19.27 276.96 ± 46.36 16.74

Feedback Condition

Pre Exercise Repetition 1 277.28, 58.84 21.22 284.40 ± 53.53 18.82

Pre Exercise Repetition 1 300.81 ,68.07 22.63 300.29 ± 51.77 17.44

Post Exercise Repetition 1 276.67 ,67.44 24.37 283.27 ± 45.51 16.06

Post Exercise Repetition 1 294.39, 76.49 25.98 290.66 ± 53.55 18.42

COV = Coefficient of variation

Isometric knee-flexor strength immediately post-exercise was not significantly

different from pre-exercise values (mean difference = -21.9, 95% CI -59.7 to 15.9; p=0.539).

However, there was a small and significant increase in isometric force between the two post-

exercise contractions (mean difference 20.8N, 95% CI = 4.5 to 37.2; p= 0.011). More

specifically, the uninjured limb showed a significant increase between the second and first post-

exercise contractions (mean difference = 26.5N, 95% CI = 10.5 to 42.6; p=0.002), while the

injured limb did not (mean difference = 15.2, 95% CI = 6.1 to 36.5; p= 0.259). The use of

feedback had no observed effect the knee-flexor isometric forces averaged across the four tests

(Pre 1, Pre 2, Post 1, Post 2) performed (mean difference -8.3N, 95% CI = -35.9 to 19.4; p=

0.523).

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FIGURE 18: Averages of prone knee-flexor isometric contractions pre and post NHE exercise. Bars represent group means, error bars represent standard deviation (SD)

Surface Electromyography

When averaged across the entire 30 repetitions, the normalised sEMG activity from the

lateral hamstring muscles was significantly lower than the medial hamstring muscle group

(mean difference = -28.30, 95% CI = -49.51 to -7.10; p = 0.01). Previous injury had no observed

effect on the normalised sEMG in either the lateral (mean difference = -1.13, 95% CI =-22.43

to 20.15; p = 0.90) or medial (mean difference = -18.49, 95% CI =-49.13 to 12.14; p = 0.90)

hamstring muscles, in either feedback condition. The use of feedback had no effect on the

normalised sEMG on either lateral (mean difference = -4.46, 95% CI = -29.58 to 20.65; p =

0

50

100

150

200

250

300

350

400

First PRE ISO Second PREISO

First POSTISO

Second POSTISO

Isom

etri

c K

nee-

Flex

or F

orce

(N)

Uninjured NoFeedbackInjured NoFeedbackUninjuredFeedbackInjuredFeedback

79

0.70) or medial hamstrings for all repetitions (mean difference = -2.13, 95% CI = -29.73 to

20.65; p = 0.703).

FIGURE 19: The effect of feedback on normalised sEMG for injured vs uninjured and medial vs lateral hamstrings. Bars represent group means, Error bars represent standard deviation (SD)

80

0

20

40

60

80

100

120

140

160

Repetition 1&2 Repetition 9&10 Repetition11&12

Repetition19&20

Repetition21&22

Repetition29&30

norm

alise

d sE

MG

(%)

FIGURE 18: Normalised sEMG for medial and lateral hamstrings during 30 NHE repetitions with and without feedback.

LL Lateral No FeedbackLL Medial No FeebackRL Lateral No FeedbackRL Medial No FeedbackLL Lateral FeedbackLL Medial FeedbackRL Lateral FeedbackRL Medial Feedback

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4.3 DISCUSSION

The use of the NHE is now relatively common in strength and conditioning programs

(Oakley, Jennings, & Bishop, 2017). The NHE has proven effective in reducing the incidence

and recurrence rate of HSIs in football populations (Arnason et al., 2008a; Mjølsnes et al.,

2004; Petersen et al., 2011; van der Horst et al., 2015b), although this exercise is typically

performed with a partner holding the exerciser’s ankles. As a consequence, the movement is

typically performed without performance feedback, and this may potentially limit the value of

the exercise, particularly if athletes under-perform or if previously injured athletes rely

predominantly on their uninjured limb. Biofeedback has been employed in rehabilitation for

other lower limb injuries such as ACL rupture, patellofemoral pain, and knee arthroscopy;

however, as far as the author is aware, it has not been applied in hamstring injury rehabilitation.

The results of the current study revealed no significant effects of visual biofeedback on

strength or muscle activation during a single exercise session in recreational athletes with a

unilateral history of HSI. However, the current literature on the use of feedback predominantly

focuses on its use in longitudinal rehabilitation programs (Giggins et al., 2013), which could

potentially allow participants more opportunity to learn how to utilise biofeedback and

consequently alter their muscle activation patterns. The acute nature of the current study

potentially did not allow participants to learn how to simultaneously perform the exercise while

also interpreting and applying the information they received through feedback despite the

participants completing a familiarisation and having a larger 17 inch screen in front of them to

make the force traces easy to read whilst participating in the protocol. While no study has

specifically targeted previous HSIs through feedback, most studies examining the knee

extensors performed their protocols on an isokinetic dynamometer (Croce, 1986; Ekblom &

Eriksson, 2012; Kirnap et al., 2005; Ng et al., 2008; Randell et al., 2011). The seated

dynamometer would allow for no upper body movement and potentially make reading,

82

interpreting and applying biofeedback easier for participants, compared to the constant upper

body movement associated with the NHE.

Another limitation of the current study is the lack of significant strength deficit in

previously injured limbs. Previous injury had no effect on force output compared to the

contralateral uninjured limb across the 30 repetitions. The lack of strength deficit in the injured

limb is inconsistent with previous studies which have shown reduced eccentric strength and

muscle activation in the previously injured compared to uninjured contralateral limbs (Bourne,

Opar, Williams, Al Najjar et al., 2015; Opar, Williams et al., 2014b; Timmins, Bourne, Shield,

Williams, Lorenzen et al., 2015). Differences in injury severity may explain the results, as

previous studies typically recruited participants with grade two or three injuries compared to

the less severe grade one injuries that nine of the 12 participants had experienced in this study.

The participants did provide their injury history via recall due to their sub-elite status and lack

of uniform reporting procedures from a professional such as a team doctor or physiotherapist.

Screening procedures ensured that all participants who were involved in the study had injuries

diagnosed by a medical professional and sought subsequent treatment. There is a possibility

that grade one injuries suffered by the current participants did not evoke a great neuromuscular

inhibitory response. Significant deficits in fascicle length and increased pennation angles in

previously injured BFlh muscles have been reported after more severe injuries (Timmins,

Bourne, Shield, Williams, Lorenzen et al., 2015; Timmins, Shield et al., 2015) and it has been

assumed by some that injury may have caused these, probably because this has been proposed

previously (Brockett et al., 2004). Unfortunately, it is not possible to know whether the shorter

fascicles predate initial injuries or occur as a consequence of them.

Lower fascicle lengths suggest a reduction in the number of in-series sarcomeres and

this does not directly influence maximum force generating capacity when isometric

measurements are employed as observed within this study. Furthermore, if there was any

83

reduction in muscle PCSA within this previously injured muscle (the BFLH) it should be

considered that there are numerous other knee flexors that generate torque (eg semitendinosus,

semimembranosus, biceps femoris short head, gracilis, sartorius and gastrocnemius). Mild

losses in BFLH PCSA would therefore have limited effects on knee flexor torque and there is

the possibility that other muscles may have exhibited compensatory hypertrophy since injury,

as has been reported previously (Silder et al., 2009)

The present results suggest that visual biofeedback of force output has no impact on the

strength loss during an exercise session involving 30 repetitions of the NHE. With or without

biofeedback, the significant finding from the NHE protocol performed here was the reduction

in knee-flexor force output over time, suggesting the protocol has a fatiguing effect on the

knee-flexors. The presence of strength loss across the repetitions is consistent with findings of

Marshall and colleagues (2015) who investigated 30 repetitions of the NHE in soccer players

and measured strength between sets of the NHE with eccentric and concentric efforts. The

findings of this study demonstrated strength loss during the performance of the NHE without

the potential confounding effects of other eccentric and concentric efforts. Additionally the

current investigation did examine the repetitions and subsequent variables at the peak of

summed force as opposed to the segments of the repetition as a whole. Whilst the peak summed

force knee angle was low amongst our participants it only captured information a specific point

of time and not across knee angles associated with HSI.

The EMG results highlighted the heterogeneity of muscle activation during the NHE,

with the preferential recruitment of the medial hamstrings, similar to that observed in study one

in this thesis and by Bourne and colleagues (2017) using fMRI. Despite preferentially targeting

the medial hamstrings, which are not the most commonly injured hamstring muscles during

high-speed running, the exercise still elicits high levels of activation in the lateral muscles, and

this supports its place within injury prevention programs. The author acknowledges there are

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limitations to this study. The lack of training in using feedback could have prevented the

participants from engaging with the information presented and utilising it to their greatest

capacity. The acute nature of the study didn’t allow participants the chance to learn and adapt

to having feedback while also completing the exercise. By contrast with the significant and

persistent strength deficits that have been published after more severe HSIs, the injuries in the

participants in this study, may have been more readily rehabilitated or simply recovered

spontaneously. It remains to be seen whether the use of feedback during the NHE over longer

periods of time would be more or less beneficial for more severely injured athletes.

4.4 CONCLUSION

Mild hamstring injuries do not appear to result in any lasting weakness or an

exaggerated loss of eccentric strength across 30 repetitions of the NHE. Furthermore,

biofeedback of force does not result in any acute changes in performance during the

performance of a NHE exercise session.

LINKING PARAGRAPH

The bilateral and eccentric NHE test is now used relatively widely in elite level sports.

However, it is unclear whether or not this test is more or less sensitive to the effects of prior

injury than unilateral and isometric tests of the knee flexors. It is also possible to perform a

razor curl on the same device designed to assess the NHE, and it is not known whether this

popular exercise is more sensitive to the effects of previous injury. The next study is designed

to assess the potential value of other isometric and bilateral tests of hamstring strength in

addition to changes in the isometrically derived knee flexor torque-joint angle curve after HSI.

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CHAPTER 5: The Effect of Previous Hamstring Strain Injury on Isometric and Dynamic Strength Profiles of the Knee-Flexors

5.1 RESEARCH DESIGN

5.1.1 OBJECTIVES

The aims of this investigation were to;

1. Confirm whether or not prior hamstring strain injury is associated with a shift in the

JAPT.

2. Determine whether this shift is associated with surface EMG activity of the hamstrings

at long muscle lengths.

3. To compare knee-flexor strength and medial and lateral hamstrings surface EMG

activity during the NHE, the razor curl and bilateral and unilateral isometric maximal

voluntary contractions in previously injured and uninjured limbs.

4) To assess the biceps femoris architecture (fascicle length, fascicle length, and

pennation angle) in previous injured compared to the uninjured contralateral limb.

5.1.2 PARTICIPANTS

Eight recreationally active adult males with a history of unilateral HSI were recruited

for this study. Participants completed a cardiovascular risk screening form and an injury

questionnaire with the information provided detailing the injury location, grade and

rehabilitation period of their most recent hamstring strains occurring within the past 18 months

(7.7 ± 7.2 months). All had made a full return to competition and training and were free from

any other lower limb pathologies. Participants gave informed consent to participate in the study

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which was approved by the Queensland University of Technology Human Research Ethics

Committee (approval number 1600000479).

5.1.3 METHODOLOGY

Participants completed a familiarisation session in which they performed isometric

contractions while seated on a dynamometer. During the first session, participants had

ultrasound images taken midway along the longitudinal axis of the BFlh muscle belly to assess

fascicle length and pennation angle.

Images were taken using two-dimensional B-mode ultrasound (frequency, 12 MHz;

depth, 8 cm; field of view, 14×47 mm) (GE Healthcare Vivid-i, Wauwatosa, USA). The

scanning site was determined as the halfway point between the ischial tuberosity and the knee

joint fold, along the line of the BFlh. All architectural assessments were performed with

participants in a prone position and the hip neutral following at least five minutes of inactivity.

Following the ultrasound scans, participants warmed up by cycling at a submaximal pace for

five minutes. Participants then performed three to six repetitions of the NHE (NHE), Razor

curl (RC), under the instruction of the investigator, to familiarise themselves with the

appropriate technique requirements of the exercise.

Seven days after familiarisation participants visited the laboratory for testing. The

remaining participants did not complete a familiarisation session due to previous exposure to

the testing methods in the laboratory. After completing 5 minutes of submaximal and self-

paced pedalling on a cycle ergometer, participants were then seated on a dynamometer (Biodex

System 3, New York, USA) to perform maximal voluntary isometric contractions of the knee-

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flexor and extensors at knee angles of 10, 30, 50, 70 and 90 degrees from full knee extension

(Figure 20).

FIGURE 21: Isometric knee-flexor dynamometry.

Two knee extensor and two knee-flexor contractions were performed at each joint angle

with one minute rest between efforts and a randomised presentation order of joint angles. For

all dynamometer testing, surface electromyographic (sEMG) information was collected via

bipolar pre-gelled Ag/AgCl sEMG electrodes (10 mm diameter, 20 mm inter-electrode

distance) placed on the posterior thigh half way between the ischial tuberosity and tibial

epicondyles. The reference electrode was placed on the ipsilateral head of the fibula. The lower

limbs were tested in randomised order.

Seven days after the first testing session participants returned to the laboratory for

further eccentric and isometric hamstring strength tests, this time on a device developed by the

research group. After a five minute cycling warm-up, the participants performed two maximal

voluntary isometric contractions of the knee-flexors in the prone position with two minutes rest

between contractions. They then performed unilateral maximal voluntary isometric

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contractions on each leg with a two minute rest period between repetitions. Finally, they

performed three maximal repetitions of NHE with no rest between repetitions, followed by a

two-minute rest and then three maximal repetitions of a razor curl, again without rest between

repetitions. Knee-flexor forces at the ankles were measured with uniaxial load cells (MLP-1K,

Transducer Techniques, CA, USA) attached in-series to ankle straps. The middle of each ankle

strap was aligned with the lateral malleoli, and the ankle restraints were vertical and

perpendicular to the shank. Surface electromyographic (sEMG) data was collected from lateral

and medial hamstrings as described for the first testing session and knee angle measurements

were made using a custom-made electronic goniometer (PRV6 5K potentiometer) fixed to the

left knee.

FIGURE 22: Nordic hamstring exercise on hamstring testing device. Participants

pull against ankle restraints as they resist falling

FIGURE 23: Razor curl test on hamstring testing device. Participants pull against ankle restraints as they resist falling while attempting to fully extend their knees and hips with their faces held close to the ground.

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All sEMG, force and joint angle data were sampled at 1000 Hz via a 16-bit PowerLab

26T AD unit (amplification = 1000; common mode rejection ratio = 110 dB) and analysed

using LabChart 7 (ADInstruments, New South Wales, Australia). Raw sEMG data were filtered

using a Bessel filter (frequency bandwidth=10–500 Hz) and then full-wave rectified and

smoothed over 100ms windows. Knee angle data were low pass filtered at 4 Hz. All data was

then transferred to a personal computer.

5.1.4 DATA ANALYSIS

Strength Measures

The peak forces (N) for each repetition of the NHE and razor curl for each participant

were derived by taking the maximum value for the left and right limb at the moment of the

peak of summed force for each repetition. This process was repeated for all individual

repetitions for each participant. The data was then exported into Microsoft Excel and SPSS for

statistical analysis.

For both seated and prone maximal isometric contractions (MVIC), data were obtained

from the 0.5 seconds of data surrounding the instant of peak force for each contraction (0.25

seconds either side of the peak). All isometric contractions were performed twice with the

results averaged for each contraction angle. For MVICs performed on the dynamometer,

torques for each participant were normalised to those obtained at 900 from full extension.

Surface Electromyography

Surface EMG (sEMG) data was derived by taking and averaging the 0.5 seconds of

data before the peak forces in all dynamic exercises (NHE, and Razor Curl). For all isometric

contractions, both seated and prone, sEMG data was derived by sampling the 0.5 seconds

surrounding the peak force. Surface EMG for the Nordic, razor curl, and prone isometric tests

were normalised to the MVIC contraction values in the prone position. All isometric

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contractions were performed twice at each position and knee angle; as such the average of the

two contractions was used for analysis. For MVICs performed on the dynamometer, sEMG

values for each participant were normalised to that obtained at 900 from full extension as they

cannot be normalised to the prone positioning due to the change in muscle length, and hip

position.

Muscle Architecture

The MicroDicom software (Version 0.7.8) was used for analysing the ultrasound

images collected. Due to the limited view of the ultrasound probe a muscle fascicle of interest

was outlines and the muscle fascicle length was determined using the equation: FL=sin

(AA+90°) x MT/sin(180°-(AA+180°-PA)). Muscle Thickness (MT was defined by the as the

distance between the superficial and intermediate aponeuroses of the BFLH). The ultrasound

technician was blinded to all participants’ previous injury data.

5.1.5 STATISTICAL ANALYSIS

Statistical analysis was performed using SPSS version 23.0.1 (IBM Corporation,

Chicago IL,). When appropriate, the normality of the data was assessed with the Shapiro-Wilks

test. Sphericity was assessed via Mauchly's Test of sphericity. When sphericity wasn’t

observed, the Huynh-Feldt correction was used.

For the seated dynamometry torques and normalised sEMG results, joint angle (10, 30,

50, 70, 900) by limb (injured vs uninjured) repeated measures analyses of variance (ANOVA)

were used. When significant main effects were detected, post hoc t-tests with Bonferroni

corrections were employed for pair-wise comparisons. Prone isometric results were analysed

via a laterality (bilateral vs. unilateral) by leg limb (injured vs uninjured) repeated measures

ANOVA. The force outputs for the injured versus the uninjured limb in both the Nordic

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Hamstring and Razor curl tests were compared via an exercise (NHE vs. Razor Curl) by limb

(injured vs uninjured) repeated measures ANOVA. When significant main effects were

detected, post hoc t-tests with Bonferroni corrections were employed to determine the

significant pair-wise comparisons. The mean differences were reported with their 95%

confidence intervals (CIs).

Muscle Architecture

Measures of muscle architecture (fascicle length, muscle thickness, and pennation

angle) were analysed by comparing the injured to uninjured limbs via paired sample t-tests.

The mean differences were reported with their 95% confidence intervals (CIs).

5.2 RESULTS

All participants (age 23.5 ± 2.1 years, height 178.2 ± 5.8cm, and body mass 84.6 ± 7.3

kg) had a history of unilateral HSI within the past 18 months. The average time since the most

recent insult was 7.7 ± 7.2 months with a mean return to play time of 6 ± 3.6 weeks. Details of

the participant’s injury information can be found in Table 4.

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Table 5: Hamstring injury history information for all participants.

Participant Injured Limb

Muscle injured

Number of HSIs

Months Since last HSI

Grade of last HSI

Rehabilitation time (weeks)

1 Right ST 2 18 2 10

2 Right BFlh 1 2 1 5

3 Right BFlh 2 2 1 5

4 Right BFlh 1 2 1 2

5 Right BFlh 3 12 2 4

6 Right BFlh 1 2 1 4

7 Right BFlh 3 18 1 4

8 Right BFlh 1 5 1 12

BFlh: Biceps Femoris Long Head ST: Semitendinosus

Rehabilitation was defined by a return training and match. The severity (grade) was determined by the American Medical Association's guidelines (Craig, 1973).

Biceps femoris long head architecture

BFlh fascicles were significantly shorter (mean difference = -0.74 cm, 95% CI = -0.27

to -1.23; p = 0.008) and pennation angles significantly higher (mean difference = 1.47o, 95%

CI = 1.0 to 1.93; p <0.001) in previously injured than the uninjured limbs. Muscle thickness

was not significantly different between limbs (mean difference = -0.04cm, 95% CI = -0.18 to

0.10; p = 0.546) (see Table 5).

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Table 6. Architectural characteristics of biceps femoris long head muscles in previously injured and uninjured limbs.

Injured Limb Uninjured Limb p-value

BFlh Fascicle Length 9.17 ± 0.98 9.92 ± 0.68 0.008

Pennantion Angle 16.47 ± 0.82 14.99 ± 0.96 <0.001

Muscle Thickness 2.60 ± 0.38 2.57 ± 0.29 0.546

Torque Joint-Angle relationship

Previously injured limbs were not weaker than the contralateral uninjured limbs in

normalised isometric torque across the five angles tested on the dynamometer (mean difference

= -0.03Nm, 95% CI = -0.34 to 0.29; p = 0.854) and no significant between-limb differences in

force were noted at any joint angle (p > 0.7 for all comparisons).

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FIGURE 24: Normalised Torque – knee joint angle data for previously injured and uninjured limbs as measured by isometric dynamometry.

Surface electromyography joint-angle relationship

Surface EMG for the isometric contractions performed on the dynamometer was

normalised to the result obtained from the test at 900 of knee flexion. Comparisons between

previously injured and uninjured limbs showed no significant main effect of injury history

(mean difference = 3.7%, 95% CI = -11.8 to 19.2; p = 0.512). When compared across joint

angles, the medial hamstrings were significantly more active, in terms of normalised sEMG,

than lateral hamstrings (mean difference = 23.2%, 95%CI = 12.1 to 34.3, p = 0.002), although

this effect was statistically significant in the uninjured limbs (mean difference = 30.8%, 95%

CI = 12.5 to 49.1; p = 0.005) but not the previously injured limbs (mean difference = 15.5%,

95%CI = -0.8 to 31.9; p = 0.060).

0

0.5

1

1.5

2

2.5

10 30 50 70 90

Nor

mal

ised

Torq

ue (N

m)

Angle (degrees)

InjuredUninjured

95

FIGURE 25: Normalised sEMG during isometric seated knee flexor dynamometry Error bars are omitted for the sake of clarity.

Dynamic strength tests

Previously injured limbs were not weaker than contralateral uninjured limb in either the

NHE (mean difference = -7.4N, 95% CI = -28.8 to 14.1; p = 0.444) or the razor curl test (mean

difference = 27.6N, 95% CI= 12.6 to -67.7; p = 0.149).

0

20

40

60

80

100

120

140

10 30 50 70 90

Nor

mal

ised

EMG

(%)

Degrees

InjuredLateral

InjuredMedial

UninjuredLateral

UninjuredMedial

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FIGURE 26 Eccentric knee-flexor force for NHE and Razor Curl Bars represent group means, error bars represent standard deviation (SD)

Dynamic sEMG measures

Previous injury had no effect on the normalised sEMG during either the NHE or razor

curl (mean difference = 9.8%, 95% CI = -23.3 to 43.0; p = 0.506). Normalised sEMG was

higher in the NHE than the razor curl for both lateral (mean difference = 27.5%, 95% CI = 17.9

to 27.0; p = <0.001) and medial hamstrings (mean difference = 25.3%, 95% CI = 12.4 to 38.2;

p = 0.002) and the medial hamstrings were significantly more active than the lateral in both

exercises (NHE mean difference = 32.4%, 95% CI = 7.0 to 57.9; p = 0.02; Razor curl mean

difference = 34.6, 95% CI = 8.1 to 61.2; p = 0.018).

0

100

200

300

400

500

600

NHE Razor Curl

Forc

e (N

)

UninjuredInjured

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FIGURE 27: Comparison between exercises for normalised sEMG for injured vs uninjured and medial vs lateral hamstrings.Bars represent group means, error bars represent standard deviations (SD. * p = 0.001, *** p =0.02, **** p= 0.001

Bilateral and unilateral prone isometric strength measures

From the maximal isometric testing in a prone position, the combined force generated

from the bilateral test was compared to the summed forces of the two unilateral tests. A bilateral

deficit was observed with unilateral knee-flexor forces 21.3N (4%) (95% CI = 5.1 to 37.6; p =

0.017) higher than the bilateral forces. The difference between bilateral and unilateral strength

was significant for the uninjured limbs (mean difference = 29.7N, 95% CI =10.6 to 48.8; p =

0

20

40

60

80

100

120

140

160

180

200

NHE Razor Curl

Nor

mal

ised

sEM

G (%

)

UninjuredLateral

UninjuredMedial

InjuredLateral

InjuredMedial

**

**** *** **** ****

98

0.008), but not the previously injured limbs (mean difference = 13.0N, 95% CI = -5.2 to 31.1;

p = 0.136).

FIGURE 28: Prone isometric force during unilateral and bilateral contractions. Bars represent group means, error bars represent standard deviation (SD). * p = 0.001

Bilateral and unilateral prone isometric sEMG measures

There was no significant difference in normalised sEMG between bilateral and

unilateral isometric contractions (mean difference = 2.6%, 95% CI = -4.8 to 10.1; p = 0.427).

However, there was a main effect of injury on unilateral normalised sEMG with lower levels

of activity in previously injured limbs (mean difference = 11.0%, 95% CI = 1.1 to 20.9; p =

0.035). There was a significant exercise by limb by muscle interaction for normalised sEMG

351322

0

50

100

150

200

250

300

350

400

450

Unilateral Bilateral

Forc

e (N

)

Exercise

UninjuredInjured

*

99

for lateral hamstrings with uninjured limbs exhibiting significantly higher activity than

previously injured limbs during the unilateral test (mean difference = 14.6%, 95% CI = 4.5 to

24.8; p = 0.011).

FIGURE 29: Comparison between isometric tests for normalised sEMG for injured vs uninjured and medial vs lateral hamstrings. Bars represent group means, error bars represent standard deviations (SD). * p= 0.035, ** p = 0.011.

0

20

40

60

80

100

120

140

Bilateral Test Unilateral Test

Nor

mal

ised

sEM

G (%

)

UninjuredLateral

UninjuredMedial

InjuredLateral

InjuredMedial

**

*

100

5.3 DISCUSSION

To this author’s knowledge, this is the first study to investigate JAPT in athletes with a

history of HSI via isometric measurements. One goal of this study was to examine whether

prior HSI was associated with a shift in the knee-flexor angle of peak torque. Such a shift has

been reported in the literature, although a total of only ten participants across two studies have

been shown to exhibit such changes (Brockett et al., 2001, 2004; Brughelli et al., 2009). The

results from the current isometric tests show that previously injured, and contralateral limbs

were both stronger at 10 degrees from full extension than at any other tested angle and, unlike

previous reports (Alonso, McHugh, Mullaney, & Tyler, 2009; Brockett et al., 2001, 2004;

Brughelli et al., 2009) injured and uninjured limbs in the current study did not display a peak

in torque across the range of joint angles tested. In this study, the torque-joint angle relationship

was determined across a range of isometric tests at different knee angles whereas Brockett et

al., (2001 and 2004) and Brughelli et al., (2009) employed concentric tests performed at 60

degrees per second across an approximately 90 degree range of motion. This dynamic test is

flawed in that the rate of force development influences the torques that are achieved in the first

10-20° of the flexion movement and this, therefore, influences the joint angle of peak torque.

The isometric method employed in the current study is not adversely affected by rates of force

development as each contraction lasts 3-4 seconds. It has previously been shown that hamstring

injury can result in reductions in the rate of eccentric force development (Opar, Williams et al.,

2013b) and if this is also true for concentric actions it may explain previous reports of shifts in

the joint-angle of peak knee-flexor torque. The reliability of dynamic assessments of the

torque-joint angle relationship has also been questioned (Timmins, Shield, Williams, & Opar,

2016).

It has been assumed that changes in fascicle length in previously injured hamstrings

brought about the previously reported shifts in dynamic torque-joint angle relationships

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(Brockett et al., 2001, 2004; Brughelli et al., 2009). This study, however, has shown no shift in

this relationship despite statistically significant differences in fascicle length. This is consistent

with the argument that fascicle length changes within the long head of biceps femoris may be

insufficient to create shifts in the joint angle of peak torque (Timmins et al., 2016). Previously

observed shifts in the dynamic knee-flexor torque-joint angle relationship could also potentially

be explained by neuromuscular inhibition which, after a hamstring injury, appears to be isolated

to longer muscle lengths (Opar, Williams et al., 2013b; Sole et al., 2011). In the current study,

the participants had less severe injuries than those in previous studies, and there was no

evidence of reduced knee-flexor strength at longer muscle lengths (Timmins et al., 2016). A

rather large range in the time since injury was evident amongst the cohort tested. Regardless

of the time of injury the between participant variance in force and fascicle lengths was minimal,

as we have noted previously (Bourne et al., 2015). The large range in times-since-injury is also

consistent with other research looking at athletes with previous injury history (Bourne et al.,

2015, Tol et al., 2014).

Timmins and colleagues (2015 & 2017) have previously reported reduced BFlh fascicle

lengths and increased pennation angles in previously injured limbs compared to uninjured

contralateral limbs. Furthermore, this group has reported that fascicle lengths are relatively

unresponsive to training in the previously injured limbs of Australian rules football players

(Timmins, Bourne, Williams, & Opar, 2017). The current study shows that these architectural

deficits can exist despite mild to non-existent strength differences between injured and

uninjured limbs. It should also be acknowledged that muscle thicknesses were virtually

identical in the previously injured and uninjured BFlh muscles. Additionally, the BFlh

represents approximately 32% of the total physiological cross-section area of the hamstrings

(Sugisaki, Kobayashi, Tsuchie, & Kanehisa, 2017), and the gastrocnemius, gracilis, and

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sartorius muscles are also knee-flexors. As a consequence, small changes in the strength of this

previously injured muscle would be unlikely to influence knee-flexor torques to a great extent.

There are a range of knee-flexor strength tests available in clinical and laboratory

settings, and it is of interest to know if any of these are more sensitive to effects of prior HSI

than others. In the current study, the participants performed unilateral isometric tests, the NHE,

a razor curl, and bilateral and unilateral prone isometric knee-flexor MVCs. Of these, tests

conducted on isokinetic dynamometers are almost always unilateral while the NHE test is

typically bilateral and it is unknown whether bilateral or unilateral tests are more sensitive to

the effects of prior HSI. The results of the present investigation are unclear on this matter

because of the lack of strength deficits in the recruited participants. This author had anticipated

some strength deficits in previously injured limbs as these have been reported previously (Opar,

Williams et al., 2013a; Sole et al., 2011; Timmins, Bourne, Shield, Williams, & Opar, 2015).

However, it has been proposed that neuromuscular inhibition may be limited to more severe

hamstring strains (Fyfe et al., 2013) and most of the present participants had suffered relatively

minor (grade 1) injuries whereas the participants in a number of previous studies had grade 2

or higher injuries (e.g. Bourne et al., 2015 and Opar et al., 2013 a&b). In the present study,

there were no significant differences in knee-flexor strength between previously injured and

uninjured limbs regardless of how strength was measured. As a consequence, it was not

possible to determine whether any of the strength tests were more sensitive to the effects of

prior injury than the others. Whether or not this is true for more severe injuries remains to be

seen.

Despite a lack of difference in strength measures between limbs, there were deficits in

normalised sEMG of the lateral hamstrings in previously injured limbs during prone isometric

strength tests. This deficit has been reported previously for eccentric knee-flexor strength tests

by Opar et al., (2013a), who also showed a lack of difference in medial hamstring activity

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between injured and uninjured limbs. Bourne and colleagues (2015b) have also previously

reported deficits in BFlh muscle activation, as determined by functional MRI changes in T2

relaxation time during the NHE in previously injured muscles. However, in the current study,

no such difference was noted in the seated isometric MVCs or during the dynamic NHE and

razor curl. The reason for this inconsistency is not apparent, however, the process of

normalising sEMG is rather arbitrary, and differences in normalisation between tests may

contribute to the discrepancy. It should also be acknowledged that no significant differences in

sEMG were noted in two of the three tests conducted and it is possible that the reduced lateral

hamstring sEMG may have been a false-positive finding.

Differences between the knee flexion forces and hamstring muscle activation levels

may have some significance for exercise selection in injury prevention programs. The razor

curl exercise is emerging as a popular alternative to the NHE, and much like the NHE it appears

to be a medial hamstring dominant exercise as illustrated by sEMG data in the present study.

While the lateral hamstrings are the muscles most prone to injury, greater activation of the

medial muscles is proposed to be advantageous in providing a protective mechanism for the

lateral hamstrings (Schuermans, Van Tiggelen, Danneels, & Witvrouw, 2014). The razor curl,

however, exhibited lower levels of hamstring activation overall compared to the NHE, despite

exhibiting similar and even higher force outputs. The reduced levels of muscle activation could

be attributed to the simultaneous knee extension during the exercise, similar to those observed

during the squat and leg press exercises (Ploutz-Snyder, Convertino, & Dudley, 1995). Recent

unpublished data also suggests that the razor curl is ineffective in altering BFlh fascicle lengths

(Pollard et al., 2018)

(https://drive.google.com/open?id=1pazSfGizEFA_cafNfCOOZFuLjNPIJiq2).

There are some limitations to the current investigation. Firstly, the number of participants,

while comparable to a number of similar studies (Brockett et al., 2001, 2004; Brughelli et al.,

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2009) was low, and this raises the question of how reproducible the findings are. This study

had a small participant cohort due to the stricter criteria on previous lower limb pathologies.

This study required participants to only exhibit a unilateral hamstring injury in the absence of

all other lower limb pathologies. Timmins and colleagues (2016), when reviewing the JAPT

literature highlighted the limitation in assuming that changes in one muscle contribute to larger

deficits in knee flexion torque despite multiple muscles contributing to this movement. As such,

investigating those with only a hamstring strain would help with the current understanding

surrounding the impact of HSI on the JAPT without confounding factors. Between limb

differences in hamstring force outputs were compared to previous studies which had a minimal

detectable change of 76N and 60N for the left and right limbs, respectively, in healthy

participants. As highlighted earlier, the participants could have had their strength sufficiently

rehabilitated and or not suffered a severe enough injury for neuromuscular inhibition to occur.

However, there is minimal literature investigating the effects of low grade hamstring injuries

to which the current results can be compared. The author acknowledges that there is a

likelihood of a type II error due to the low statistical power of the current study and this

reinforces the need for further research with larger cohorts to understand the effect of previous

injury on the JAPT.

Another limitation was the self-reporting of injuries from participants and the lack of

detailed information regarding their rehabilitation. A small proportion of hamstring strains in

sport are associated with negative findings on MRI and it is possible that some participants in

the current study may have fitted into this category (Gibbs, Cross, Cameron, & Houang, 2004).

The use of sEMG is also problematic in determining levels of muscle activity due to potential

crosstalk from neighbouring muscles. This effect is minimised by placing recording electrodes

for the one muscle close together, and the inter-electrode distances of 20mm employed in the

current study are likely to minimise crosstalk. It should be noted, however, that the current

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results for the NHE are consistent with those from fMRI studies which show preferential

activation of the semitendinosus over the biceps femoris long head (Bourne et al., 2015 and

2017).

The retrospective nature of this study does not allow determination of whether the

deficits observed in injured limbs, such as those for fascicle lengths, were present before the

initial injury or were caused by it. There is evidence that BFlh fascicle length is an independent

risk factor for HSI (Timmins, Shield et al., 2015; Timmins et al., 2016) but there is no current

evidence that fascicle lengths decrease as a result of HSI. In the future, it may be of value to

follow, for extended periods of time, large cohorts of previously uninjured athletes to determine

the impact of injuries as they occur.

5.4 CONCLUSION

Isometric testing in seated and prone positions in people with a previous low-grade

hamstring strain injury showed no significant shifts in the torque-joint angle relationship or any

strength deficits in previously injured limbs when compared to the contralateral limbs.

Similarly, the dynamic NHE and razor curl tests showed no strength deficits in previously

injured limbs. This study suggests that previous low-grade injury is associated with BFlh

fascicle length deficits and elevated pennation angles without any effects on isometric or

eccentric strength.

106

CONCLUSION

This program of research aimed to improve our understanding of the acute effects of eccentric

and isometric contractions on knee-flexor force output and sEMG and to ascertain whether

prior low grade injury effects these measures and if the use of biofeedback can alter measures.

Study 1 further enforced the need to investigate the appropriate prescriptions of

rehabilitation exercises. Despite the 30 repetitions of the NHE showing no differences in torque

output regardless of prescription (3x10 vs. 5x6). In a practical setting this suggests that neither

protocol has an obvious advantage over the other, although the 3x10 repetition protocol can be

performed in a shorter time frame compared to the 5x6 protocol. Differences in the BFlh sEMG

did highlight the needs to prescribe exercises such as the NHE appropriately, to retain its shown

benefits but without putting the muscle at subsequent risk of injury in the following sessions.

The effects of force loss observed in Study 1 were still unknown to affect previously

injured muscles in the same fashion. Study 2 aimed to investigate the effect that previous injury

has on the performance of the NHE at a higher volume. In addition, Study 2 aimed to assess

the use of biofeedback during the exercise and its subsequent effects on performance. While

previous injury and feedback did not affect the NHE performance. The structural differences

in the muscles bring to attention an avenue of future enquiry into enhancing rehabilitation

programs that ameliorate the functional deficits but the structural deficits such as those

observed in Study 2.

Finally, Study 3 aimed to evaluate the value of other tests for hamstring strength testing

of varying contraction modes and laterality in addition to muscle architecture. Muscle

architecture measures exhibited significant alterations to fascicle length and pennation angle

when comparing the previously injured limb to the uninjured limb. Despite alterations to the

107

structure of the muscle, the function as measured by strength appears to be unaffected. The

strength test results were mixed, but the differences between injured to uninjured limbs and

between the lateral and medial muscles again highlighted the need to create and implement

effective rehabilitation and preventative strategies that target the muscles capacity activate and

enhance the structure of the muscle as well as the architecture.

Moving forward, this program of research has added some insight into the acute effects

of lower grade hamstring has on ability to perform various hamstring tests and exercise

protocols in the presence of structural deficits. Future research should aim to elaborate on these

findings and look forward into enhancing current hamstring protocols to ensure both structure

and function are restored to pre-injury levels and reduce the risk of future HSI for athletes.

Additionally, further research will need to investigate if the same protocols and tests effect

those in elite sport similarly or differently to the sub-elite populations tested within this

research programme.

Overall the findings from this program of research have provided some novel insights

that have contributed to the existing knowledge of hamstring strain injury. Low-grade

hamstring strain showed no lasting deficits on JAPT, eccentric, and or isometric strength

despite significant between limb differences in muscle architecture when measured by fascicle

length and pennation angle. The findings provided insight into the acute effects the respective

testing and exercise protocols have on the hamstring muscle group and may inform

practitioners moving forward when making decisions for their programming needs.

108

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