anterior cruciate ligament reconstruction & the hamstrings · prevention protocols given that...

ANTERIOR CRUCIATE LIGAMENT

RECONSTRUCTION &

THE HAMSTRINGS

Implications for injury prevention & rehabilitation

Daniel J. Messer

B. App Sci. HMS.

Masters by 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

2018

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Table of Contents

Table of Contents ......................................................................................................... ii

Abstract ....................................................................................................................... iv

List of Figures ............................................................................................................. ix

List of Tables ................................................................................................................ x

List of Abbreviations .................................................................................................. xi

Statement of Original Authorship .............................................................................. xii

Acknowledgements ................................................................................................... xiii

INTRODUCTION ............................................................................. 1

LITERATURE REVIEW ................................................................. 4

2.1 Knee joint anatomy ......................................................................................................... 4 2.1.1 Hamstrings............................................................................................................ 5 2.1.2 Quadriceps ............................................................................................................ 7 2.1.3 Anterior cruciate ligament .................................................................................... 8

2.2 Definition of hamstring strain injury .............................................................................. 8

2.3 Incidence of hamstring strain injury ............................................................................... 9

2.4 Recurrence of hamstring strain injury .......................................................................... 10

2.5 Mechanism(s) of hamstring strain injury ...................................................................... 10

2.6 Proposed risk factors for hamstring strain injury .......................................................... 12 2.6.1 Non-modifiable risk factors ................................................................................ 12 2.6.2 Modifiable risk factors ....................................................................................... 14 2.6.3 Interaction between modifiable and non-modifiable risk factors ....................... 18

2.7 Definition of anterior cruciate ligament injury ............................................................. 18

2.8 Incidence of anterior cruciate ligament injury .............................................................. 19

2.9 Recurrence of anterior cruciate ligament injury ........................................................... 21

2.10 Mechanism(s) of anterior cruciate ligament injury ....................................................... 21

2.11 Proposed risk factors for of anterior cruciate ligament injury ..................................... 23 2.11.1 Non-modifiable risk factors ............................................................................. 24 2.11.2 Modifiable risk factors ..................................................................................... 27

2.12 Consequences of of anterior cruciate ligament injury .................................................. 34 2.12.1 ACL reconstruction .......................................................................................... 34 2.12.2 Hamstring grafts .............................................................................................. 35 2.12.3 Rehabilitation and return to sport .................................................................... 37 2.12.4 Long term consequences .................................................................................. 39

2.13 Anterior cruciate ligament injury and risk of future injury........................................... 39

2.14 Assessing spatial patterns of muscle activation via functional magnetic resonance imaging ................................................................................................................................... 41

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PROGRAM OF RESEARCH ........................................................ 43

STUDY 1 – HAMSTRING MUSCLE USE IN FEMALES DURING HIP-EXTENSION AND THE NORDIC HAMSTRING EXERCISE ................. 45

4.1 Linking paragraph ......................................................................................................... 46

4.2 ABSTRACT ................................................................................................................. 48

4.3 INTRODUCTION ........................................................................................................ 49

4.4 METHODS ................................................................................................................... 50

4.5 RESULTS ..................................................................................................................... 56

4.6 DISCUSSION ............................................................................................................... 61

STUDY 2 – A HISTORY OF ANTERIOR CRUCIATE LIGAMENT INJURY INCREASES THE RISK OF HAMSTRING STRAIN INJURY ACROSS FOOTBALL CODES IN AUSTRALIA ................................................................. 65


5.2 ABSTRACT ................................................................................................................. 67

5.3 INTRODUCTION ........................................................................................................ 68

5.4 METHODS ................................................................................................................... 70

5.5 RESULTS ..................................................................................................................... 74

5.6 DISCUSSION ............................................................................................................... 78

STUDY 3 – HAMSTRING MUSCLE ACTIVATION, MORPHOLOGY AND STRENGTH DURING ECCENTRIC EXERCISE 1 TO 6 YEARS AFTER ANTERIOR CRUCIATE LIGAMENT RECONSTRUCTION WITH SEMITENDINOSUS GRAFT ................................................................................. 84


6.2 ABSTRACT ................................................................................................................. 86

6.3 INTRODUCTION ........................................................................................................ 88

6.4 METHODS ................................................................................................................... 89

6.5 RESULTS ..................................................................................................................... 98

6.6 DISCUSSION ............................................................................................................. 105

GENERAL DISCUSSION & CONCLUSION ........................... 110

Bibliography ............................................................................................................ 113

Appendices ............................................................................................................... 148

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Abstract Both anterior cruciate ligament (ACL) and hamstring strain injuries (HSI) account for a

significant amount of lost time in a range of football codes. Both are associated with high

recurrence rates, while a history of each injury is a very strong predictor of the same injury

in the future. ACL injuries are immediately debilitating and can lead to chronic deficits in

medial hamstring volumes (Konrath et al., 2016; Nomura, Kuramochi, & Fukubayashi,

2015; Snow, Wilcox, Burks, & Greis, 2012), knee flexor (Konrath et al., 2016; Nomura et

al., 2015; Snow et al., 2012) and medial rotator strength (Konrath et al., 2016), knee stability

(Abourezk et al., 2017), altered gait (Abourezk et al., 2017; Tashman, Collon, Anderson,

Kolowich, & Anderst, 2004) and early onset knee osteoarthritis (Beynnon, Johnson, Abate,

Fleming, & Nichols, 2005). Following ACL injury, ACL reconstruction (ACLR) surgery is

widely considered to be required in sports involving rapid jumping and pivoting.

However, there appears to be no difference in subjective and objective outcomes after ACLR

and those treated with rehabilitation alone (Frobell, Roos, Roos, Ranstam, & Lohmander,

2010; Frobell et al., 2013). It has been suggested that a history of a significant knee

injury is a risk factor for future HSI, although the evidence for this assertion is limited.

The prevention of ACL injuries may require a better understanding of the muscle activation

patterns during hamstring strengthening exercises. This thesis aimed to, firstly, examine

the muscle activation patterns of women, without a history of lower limb injury, during

two common hamstring exercises and, secondly, examine the impact of a prior ACLR

on a) the risk of subsequent HSI, and b) hamstring muscle size, eccentric strength and

patterns of muscle use during a common rehabilitation exercise.

The purpose of study 1 was to assess the hamstring muscle activation patterns in

women. Six recreationally active women with no history of lower limb injury underwent

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functional magnetic resonance imaging (fMRI) on both thighs before and immediately

after 5 sets of 6 bilateral eccentric contractions of the 45º hip-extension or Nordic

hamstring exercises. This study showed, a higher biceps femoris long head to

semitendinosus activation ratio during the 45° hip-extension than the Nordic exercise (p =

0.028). The hip-extension exercise was found to more evenly activate the biarticular

hamstrings while the Nordic exercise preferentially recruited the semitendinosus (ST)

muscle. These observations fit with the muscle activation pattern previously reported for

recreational male athletes.

The aim of study 2 was to determine the impact of a prior ACL injury, HSI or both on 1)

the risk of future HSI; and 2) eccentric knee flexor strength and between-limb imbalance

during the Nordic hamstring exercise. This study showed that athletes with a history of a

HSI in the previous 12 months had a 2.4-fold (RR = 2.4; 95 % CI = 1.5 to 3.9; p < 0.001)

greater risk of subsequent HSI and those with a history ACL injury had a 3.2-fold (RR =

3.2; 95 % CI = 1.9 to 5.2; p < 0.001) greater risk of subsequent HSI than athletes without

such history. Meanwhile, athletes with a prior ACL injury and a history of HSI in the

previous 12 months had a 5.7-fold (RR = 5.7; 95 % CI = 3.2 to 9.5; p < 0.001) increased

risk of HSI. The results showed that athletes with a history of ACL injury and recent (12

months) history of HSI were significantly weaker (mean difference = -106 N; 95 % CI =

-165 to -46 N; p < 0.001) and displayed larger between-limb imbalances (mean difference

= 28 %; 95 % CI = 14 to 41 %; p < 0.001) than those without such history, while those

with a prior ACL injury were not weaker than players without a prior ACL injury.

Study 3 aimed to determine the effect of ACLR from a hamstring graft on 1)

hamstring muscle activation during eccentric exercise; 2) hamstring muscle volumes,

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anatomical cross-sectional areas (ASCAs) and lengths and; 3) eccentric hamstring

strength. Fourteen recreationally active men (n = 5) and women (n = 9) with a history of

unilateral ACLR from a hamstring tendon graft were recruited. All were at least 12 months

post-surgery. Each participant underwent fMRI of their thighs before and after they

performed five sets of 10 repetitions of the Nordic hamstring exercise. ST muscle

activation, as indicated by changes in T2 relaxation times, was significantly reduced in

limbs with a previous ACLR compared to uninjured contralateral limbs (mean

difference = -9.9 %; 95 % CI = -3.8 to -16.0 %; p = 0.004; d = 0.93). None of the other

hamstring muscles exhibited differences in activation between injured and uninjured

limbs. ST muscle volume (mean difference = -80.9 cm3; 95 % CI = -57.1 to -104.7 cm3; p <

0.001; d = 1.52), ACSA (mean difference = -3.5 cm2; 95 % CI = -1.9 to -5.0 cm2; p <

0.001; d = 0.89) and length (mean difference = -7.2 cm; 95 % CI = -4.8 to -9.5 cm; p <

0.001; d = 1.99) were significantly lower in the injured limb. Semimembranosus (mean

difference = 9.7 cm3; 95 % CI = 5.5 to 14.0 cm3; p < 0.001; d = 0.20) and biceps femoris

short head (mean difference = 5.9 cm3; 95 % CI = 0.6 to 11.0 cm3; p = 0.032; d = 0.25)

muscle volumes were slightly, but statistically significantly larger in injured limbs. No

difference in eccentric hamstring strength was found between limbs during the Nordic

hamstring exercise (mean difference = -21 N, 95 % CI = 33 to -74 N, p = 0.550, d = 0.26).

This program of research has provided novel data to suggest that the hamstring activation

patterns in women are similar to those previously reported in men. Additionally, it has

provided prospective data on the impact of ACL injury and HSI on the future risk of

hamstring injury and provided novel data on the activation patterns and morphology of the

hamstrings following ACLR. Future studies are needed to ascertain whether training

interventions are effective in increasing ST muscle size and activation after ACLR and

subsequent rehabilitation and whether there are exercises that can significantly compensate

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for the loss of medial rotation strength, perhaps via targeting the semimembranosus. In

addition, future work on the hip extension exercise should be included in hamstring injury

prevention protocols given that this exercise may be more useful than the Nordic hamstring

exercise and other hamstring exercises at activating the commonly injured biceps femoris

long head muscle. These data highlight the maladaptations that occur after ACL injury and

subsequent reconstruction, while also providing evidence to form decisions regarding

exercise selection in ACL and hamstring injury prevention and rehabilitation programs.

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List of publications

1) Messer, DJ. (2017). Review of the literature: a review investigating the impact

hamstring strain injury and anterior cruciate ligament reconstruction have on eccentric

knee flexor strength and future hamstring injury risk. Journal of Australian Strength and

Conditioning, Accepted.

2) Messer, DJ., Bourne MN., Williams MD., Al Najjar, A., Shield, AJ. (2018). Hamstring

muscle use in females during hip extension and the Nordic hamstring exercise: an fMRI

study. Journal of Orthopaedic and Sport Physical Therapy, Accepted.

Manuscripts currently under peer review

1) Messer, DJ., Bourne, MN., Williams, MD., Timmins, RG., Shield, AJ. Hamstring

muscle activation, morphology and strength during eccentric exercise 1 to 6 years

after anterior cruciate ligament reconstruction with semitendinosus graft. Knee

Surgery, Sports Traumatology, Arthroscopy, Under Review.

Grants awarded during candidature

1) Institute of Health and Biomedical Innovation

a) Messer DJ., Shield AJ. (2015). The effect of eccentric exercise on knee flexor muscle

activation patterns in females.

$8000

b) Messer DJ., Shield AJ. (2016). Knee flexor muscle function and structure after

anterior cruciate ligament reconstruction.

$7000

List of conference presentations

1) Messer, DJ., Bourne, MB., Williams, MD., Al Najjar, A., Shield, AJ. Hamstring muscle

use during hip extension and the Nordic hamstring exercise: an fMRI study. Sports

Medicine Australia Conference. Melbourne, 2016.

2) Messer, DJ., Williams, MD., Bourne, MB., Timmins, RG., Opar, DA., Duhig, SJ.,

Shield, AJ. A history of anterior cruciate ligament injury increases the risk of hamstring

strain injury across football codes in Australia. IOC World Conference. Monaco, 2017.

ix

List of Figures

Figure 4-1. (A) 45° hip-extension exercise and; (B) Nordic hamstring exercise. ...... 53

Figure 4-2. Percentage change in fMRI T2 relaxation times of each knee flexor

muscle following the (A) 45° hip-extension exercise (B) Nordic hamstring

exercise. ........................................................................................................ 58

Figure 4-3. 45° hip-extension exercise and; (B) Nordic hamstring exercise.

Region of interest selection in a T2-weighted image (1) before and; (2)

after exercise.. ............................................................................................... 60

Figure 4-4. The BFLH to ST ratio (BFLH/ST) percentage change in fMRI T2

relaxation times following the 45° hip-extension and the Nordic

hamstring exercise.. ...................................................................................... 61

Figure 5-1. The Nordic hamstring exercise performed on the testing device

(progressing from right to left).. ................................................................... 72

Figure 5-2. Participant recruitment and inclusion in the study. ................................ 75

Figure 5-3. Eccentric knee flexor strength (N) (bars) and between-limb imbalance

(%) (line) as measured by the Nordic hamstring device for each group. ..... 78

Figure 6-1. The Nordic hamstring exercise, progressing from right to left. .............. 92

Figure 6-2. (A) Region of interest selection in a T2-weighted image and (B) T1-

weighted mDixon water only image.. ........................................................... 97

Figure 6-3. Percentage change in fMRI T2 relaxation times of each hamstring

muscle following the Nordic hamstring exercise.. ........................................ 99

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List of Tables

Table 4-1. The average T2 relaxation time values measured before (T2 Pre) and

immediately after (T2 Post) the 45° hip-extension and Nordic hamstring

exercise and the average T2 increase (%) of each muscle (relative to the

T2 relaxation time at rest). ........................................................................... 59

Table 5-1. Relative risk of future hamstring strain injury (HSI) ................................ 75

Table 5-2. Regression analysis of future risk of hamstring strain injury (HSI) ......... 76

Table 6-1. T2-weighted and mDixon slice positioning and image acquisition

parameters .................................................................................................... 94

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List of Abbreviations

ACL anterior cruciate ligament

ACLR anterior cruciate ligament reconstruction

BFLongHead biceps femoris long head

BFShortHead biceps femoris short head

CI confidence interval

EMG electromyography

fMRI functional magnetic resonance imaging

HSI hamstring strain injury

H:Q ratio hamstring-to-quadriceps ratio

NHE Nordic hamstring exercise

ROI region of interest

RR relative risk

SM semimembranosus

ST semitendinosus

T2 transverse relaxation time

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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: May 2018

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Acknowledgements

I would like to express my sincere gratitude to my supervisor and the rest of my research

team for the continuous support during my Masters study and related research. A special

mention goes to Dr. Anthony Shield, Dr. Matthew Bourne and Dr. Morgan Williams, for

their insightful comments and encouragement throughout writing this thesis and in my life in

general.

Chapter 1: INTRODUCTION 1

INTRODUCTION

During the time course of an athlete’s career, there is a high risk of suffering a significant

knee or lower limb injury during sports participation (Darrow, Collins, Yard, & Comstock,

2009; Majewski, Susanne, & Klaus, 2006). Both anterior cruciate ligament (ACL) and

hamstring strain injuries (HSI) account for a significant amount of lost time in a range of

football codes (Bjordal, Arnly, Hannestad, & Strand, 1997; Ekstrand, Hagglund, & Walden,

2011a; Orchard & Seward, 2002) and both are associated with high recurrence rates (Arnason

et al., 2004; Ekstrand, Hagglund, & Walden, 2011b) and a history of each injury is a very

strong predictor of the same injury in the future (Hagglund, Walden, & Ekstrand, 2006;

Verrall, Slavotinek, Barnes, Fon, & Spriggins, 2001). It has also been suggested that a history

of a significant knee injury, including an ACL injury, is a risk factor for future HSI (Verrall

et al., 2001), although the evidence for this assertion is limited.

In Australia and the United States combined there are reportedly 100,000 to 300,000 ACL

injuries each year (Boden, Griffin, & Garrett, 2000; Prodromos, Han, Rogowski, Joyce, &

Shi, 2007) and many of these occur in 15-25-year-old athletes participating in sport (Hewett,

Myer, & Ford, 2006; LaBella et al., 2014). Most ACL tears are non-contact injuries that

occur during landing, changes of direction or deceleration while hip adduction, internal

femoral rotation, external tibial rotation and knee valgus is often identifiable at the time of

injury (Besier, Lloyd, & Ackland, 2003; Cochrane, Lloyd, Buttfield, Seward, & McGivern,

2007). ACL injuries in athletes are immediately debilitating and typically require ACL

reconstruction (ACLR) surgery. This procedure usually involves one of two autogenous

grafts harvested from either the ipsilateral semitendinosus (ST) and gracilis or the patellar

tendon (Ardern, Webster, Taylor, & Feller, 2010; Aune, Holm, Risberg, Jensen, & Steen,


2001; Gobbi & Francisco, 2006; Paterno et al., 2010; Pinczewski, Deehan, Salmon, Russell,

& Clingeleffer, 2002; Pinczewski et al., 2007). Given the reduced risk of developing anterior

knee pain after hamstring grafts (Ejerhed, Kartus, Sernert, Kohler, & Karlsson, 2003), the

vast majority of ACLRs in elite Australian sport involve the ST tendon (Aglietti, Buzzi,

Zaccherotti, & De Biase, 1994; Ejerhed et al., 2003). However, the ST muscle provides

support to the ACL by resisting external tibial rotation and anterior tibial translation (Ejerhed

et al., 2003; Nomura et al., 2015), and the impact of ST tendon grafts on the long term

function of this muscle is unclear (Burks, Crim, Fink, Boylan, & Greis, 2005).

HSI has less lifetime impact than ACL injury but still costs sports organisations millions of

dollars (Verrall, Kalairajah, Slavotinek, & Spriggins, 2006; Woods, Hawkins, Hulse, &

Hodson, 2002). For example, in the Australian football league, HSIs cost each club an

average of AUD$1.5m per season in wages paid to side-lined players (Orchard, Seward, &

Orchard, 2013). It is also possible that the common hamstring graft reconstruction technique

leaves athletes more prone to HSI. Even in the absence of ACL injury and reconstruction, it

has been suggested that the relative activation of the biceps femoris long head (BFLongHead)

and ST vary between individuals and that athletes who display relatively low levels of ST

muscle activation and a relatively heavy use of the BFLongHead are at greater risk of future

hamstring strain injury (Schuermans, Van Tiggelen, Danneels, & Witvrouw, 2014, 2016). It

seems likely that athletes, who lose significant ST function as a consequence of ACLR,

would also be at increased risk of HSI.

Some serious long-term consequences of ACLR include the almost guaranteed development

of knee osteoarthritis (Lohmander, Englund, Dahl, & Roos, 2007), along with an increased

risk of subsequent graft failure (Kvist, 2004) and knee replacement later in life (Carr et al.,


2012; Culliford et al., 2012; Khan et al., 2018; Mather et al., 2013). A number of

observational studies (Konrath et al., 2016; Nomura et al., 2015; Takeda, Kashiwaguchi,

Matsuura, Higashida, & Minato, 2006) have reported decrements in concentric (Tengman et

al., 2014) and eccentric (Tengman et al., 2014; Thomas, Villwock, Wojtys, & Palmieri-

Smith, 2013) knee flexor strength in the years following ACLR surgery in addition to

reduced ST muscle size (Nomura et al., 2015) and altered BFLongHead muscle architecture

(Timmins, Shield, Williams, Lorenzen, & Opar, 2015). It has been suggested that after a

significant knee injury, such as an ACL injury, the biomechanics of the lower limb are

altered, and these changes increase the risk of future HSI (Verrall et al., 2001).

As there is limited evidence on the impact of ACL injury and subsequent reconstruction on

knee flexor function and risk of future HSI, further investigation of the long-term

consequences of this injury is warranted. This review aims to provide the reader with a

summary of HSI literature through an overview of HSI prevalence in sport and discussion of

the proposed risk factors for injury. Following this, there is a summary of the literature

surrounding ACL injury, including, an overview of ACL injury prevalence in sport, a

discussion of the proposed risk factors for injury and long-term consequences of injury and

subsequent reconstruction. It will conclude with a discussion of the impact of ACL injury on

the risk of future injury.

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LITERATURE REVIEW

2.1 KNEE JOINT ANATOMY

The knee is the largest joint in the human body and is formed from three bones, a strong

network of ligaments and muscles and two joints, the tibiofemoral and patellofemoral joint

(Levangie & Norkin, 2011). The tibiofemoral joint is the articulation between the distal

femur and the proximal tibia whereas the patellofemoral joint is the articulation between the

posterior patella and the anterior portion of the distal femur (Levangie & Norkin, 2011). The

knee is responsible for supporting the weight of the human body and redistributing joint loads

during a range of static and dynamic actions (Arnoczky, 1983; Smith et al., 2012). Within the

knee are the menisci which cover two-thirds of the articular surface of the tibial plateau.

These serve as shock absorbers for 50 % to 70 % of the loads produced during movement

(Arnoczky, 1983; Levangie & Norkin, 2011). The passive stability of the knee is the

responsibility of four ligaments; medial collateral ligament, lateral collateral ligament,

posterior cruciate ligament and the anterior cruciate ligament. Collectively, these ligaments

resist knee varus and valgus stresses, anterior or posterior displacement of the tibia relative to

the femur, medial or lateral rotation of the tibia relative to the femur and excessive knee

extension (Levangie & Norkin, 2011). Each ligament’s influence is dependent on the position

of the knee and the capacity of active and passive structures to control joint stresses. The

dynamic restraints of the knee joint include the quadriceps, hamstrings and other knee flexor

muscles, which are located on the anterior and posterior aspect of the thigh. Collectively

these muscles work to control and stabilize the knee joint (Arnoczky, 1983).

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2.1.1 Hamstrings

The hamstring muscle complex describes a group of three muscles located on the posterior

thigh – semitendinosus, semimembranosus (SM), and biceps femoris; which is further

divided into a long and a short head (Woodley & Mercer, 2005). With the exclusion of biceps

femoris short head (BFShortHead), the hamstrings are biarticular muscles because they cross

both the posterior aspects of the hip and knee joints (Koulouris & Connell, 2005), which

allow the long hamstrings to perform flexion at the knee and extension of the hip during

concentric contraction. Collectively, the hamstrings’ common actions are hip extensors and

knee flexors; however, each muscle exhibits significant differences in morphology (e.g.,

physiological cross sectional area), architecture (e.g., fascicle length and pennation angles)

and function (e.g., activation patterns) (Markee et al., 1955; Woodley & Mercer, 2005).

Physiological cross sectional area refers to the cross section of a muscle perpendicular to its

muscle fibres whereas anatomical cross sectional area is the cross section of a muscle

perpendicular to its longitudinal axis. As major flexors of the knee, the hamstrings provide

the greatest active restraint against anterior tibial translation shear forces (Blackburn,

Norcross, Cannon, & Zinder, 2013; Ford, Myer, Toms, & Hewett, 2005; Myer et al., 2009).

A comprehensive understanding of hamstring anatomy, architecture and function are

necessary to determine the role these muscles play in HSI and ACL injury prevention and

rehabilitation.

Medial hamstrings

Semitendinosus

The ST is a single digastric muscle with a tendinous inscription which divides the muscle

belly into superior and inferior portions (Koulouris & Connell, 2005; Markee et al., 1955).

Proximally, the muscle fibres of ST originate from three distinct locations: the posteromedial

6

portion of the ischial tuberosity; the medial border of the proximal BFLongHead tendon; and an

aponeurosis from the proximal tendon of the BFLongHead (Woodley & Mercer, 2005). Distally,

the ST muscle fibres form a long tendon which inserts onto the proximal medial surface of

the tibia (Woodley & Mercer, 2005). ST is innervated by two nerves originating from the

tibial portion of the sciatic nerve (Koulouris & Connell, 2005; Markee et al., 1955). The

superior nerve innervates motor units proximal to the tendinous inscription, while the inferior

nerve innervates the inferior portion of the muscle. The ST architecture is strap-like muscle

with long and thin fibres and is the longest of all the hamstrings (Woodley & Mercer, 2005).

Semimembranosus

SM is a single muscle with bipennate architecture (Markee et al., 1955). Proximally, the SM

tendon originates from the lateral side of the posterior ischial tuberosity (Woodley & Mercer,

2005). Distally, the SM tendon has multiple insertions, including, the posterior surface of the

medial tibial condyle, the capsule of the knee joint and the proximal medial collateral

ligament (Koulouris & Connell, 2005; Markee et al., 1955). SM is innervated by a nerve

branch originating from the tibial portion of the sciatic nerve while sharing the same nerve

branch as the inferior portion of the ST. The SM displays the greatest physiological cross-

sectional area of all the hamstring muscles (Woodley & Mercer, 2005)

Lateral hamstrings

Biceps femoris

Biceps femoris is a double headed muscle. The long head is a bipennate and biarticular

muscle which originates from the medial portion of the superior half of the ischial tuberosity

(Woodley & Mercer, 2005). BFLongHead displays a long proximal tendon that passes distally

until it forms a narrow aponeurotic musculotendinous junction with muscle fibres arising on

7

the lateral border of this tendon along with some ST fascicles (Markee et al., 1955; Woodley

& Mercer, 2005). Distally, the BFLongHead muscle belly passes inferiorly and laterally to join

with BFShortHead and insert onto the fibula head and lateral tibial condyle (Markee et al., 1955;

Woodley & Mercer, 2005). BFLongHead is innervated by the tibial portion of the sciatic nerve

(Koulouris & Connell, 2005; Markee et al., 1955) and displays the second largest

physiological cross sectional area of all the hamstring muscles (Woodley & Mercer, 2005).

The BFShortHead is a single joint muscle which functions to flex the knee during concentric

contraction. It has muscle fibres that originate from three locations, including, the lateral lip

of the linea aspera; the upper two-thirds of the lateral supracondylar line and the lateral

intermuscular septum (Woodley & Mercer, 2005). Distally, the muscle fibres of the

BFShortHead form a common tendon with BFLongHead which inserts onto the fibula head and

lateral tibial condyle (Markee et al., 1955; Woodley & Mercer, 2005). The BFShortHead is

innervated by the sciatic and peroneal nerves (Woodley & Mercer, 2005) and displays the

longest mean fascicle lengths and smallest physiological cross sectional areas of all the

hamstring muscles (Woodley & Mercer, 2005).

2.1.2 Quadriceps

The quadriceps femoris muscle group is located on the anterior thigh and divided into four

separate muscles, including the rectus femoris, vastus lateralis, vastus medialis and vastus

intermedius (Levangie & Norkin, 2011). A tendon connects the quadriceps to the patella,

which is attached to the tibia via the patellar tendon. All of the quadriceps muscles extend the

knee during a concentric contraction, while the rectus femoris also flexes the hip during

concentric contraction (Levangie & Norkin, 2011). The quadriceps are ACL-antagonists

because contraction of these muscles increases ACL loads by pulling the tibia forward

8

relative to the femur (Aagaard, Simonsen, Magnusson, Larsson, & Dyhre-Poulsen, 1998;

Solomonow et al., 1987).

2.1.3 Anterior cruciate ligament

The ACL’s role is to provide stability to the knee joint, resist anterior and rotational forces of

the tibia relative to the femur and prevent knee hyperextension (Arnoczky, 1983; Beynnon et

al., 1995; Bjordal et al., 1997). As major flexors of the knee, the hamstrings provide the

greatest active restraint against anterior tibial translation shear forces (Blackburn et al., 2013;

Ford et al., 2005; Myer et al., 2009). The ACL runs from the posteromedial aspect of the

lateral femoral condyle in the intercondylar notch to the anterior intercondylar area of the

tibia as a collection of individual fascicles (Alentorn-Geli et al., 2009a; Arnoczky, 1983;

Levangie & Norkin, 2011; Tengman et al., 2014). The ACL’s fascicles are divided into

anteromedial and posterolateral bands, and the knee angle determines the degree of tension

transmitted through each (Arnoczky, 1983). For example, the ACL is slack when the knee is

flexed and taut when the knee is extended (Arnoczky, 1983). The ACL helps to stabilize the

knee in one of two ways: 1) as a passive restraint to excessive translational and rotational

movement; and 2) via proprioceptors within the ligament, that send afferent signals to the

brain and spinal cord which generally excite hamstrings while inhibiting quadriceps motor

neurons (Levangie & Norkin, 2011; Takeda, Xerogeanes, Livesay, Fu, & Woo, 1994).

2.2 DEFINITION OF HAMSTRING STRAIN INJURY

A HSI is defined as a partial or complete disruption of muscle fibres in the hamstring muscle

group and is commonly associated with immediate pain in the posterior thigh (Heiderscheit,

Sherry, Silder, Chumanov, & Thelen, 2010). The most common site of HSI, particularly

during high speed running, is the biceps femoris long head at the proximal musculotendinous

junction (Askling, Tengvar, Saartok, & Thorstensson, 2007). However, injury can occur at

9

the musculotendinous junction, muscle belly or distal insertion of any hamstring muscle

(Agre, 1985). The severity of a HSI is dependent on the location, the level of force applied,

the physical state of the muscle at the time of injury (Agre, 1985) and level of strain

experienced (Askling, Saartok, & Thorstensson, 2006). While there are a range of injury

classification or grading systems, HSIs are often classified using three grades of severity,

where; grade 1 injury involves a minor tear of a few muscles fibres with minimal loss of

function; grade 2 injury involves more severe partial tears of the muscle-tendon unit and

some loss of function; and grade 3 injury involves a complete rupture of the muscle-tendon

unit and severe loss of function (Agre, 1985). HSIs are usually confirmed via a clinical

diagnosis, however, magnetic resonance imaging (MRI) has increasingly been utilized in

professional sport to confirm the specific details of the injury (Greenky & Cohen, 2017). MRI

scans allow the clinician to determine the specific muscle involved, the location of the injury

and the size and extent of the injury (muscle or tendon) (Greenky & Cohen, 2017).

2.3 INCIDENCE OF HAMSTRING STRAIN INJURY

HSIs are most common in field and court based sports, including, athletics (Opar et al.,

2014), American football (Liu, Garrett, Moorman, & Yu, 2012), rugby union (Brooks, Fuller,

Kemp, & Reddin, 2006), soccer (Ekstrand et al., 2011a, 2011b; Woods et al., 2004) and

Australian football (Orchard & Seward, 2002). In the Australian football league, HSI

accounts for 16 % of all time-loss injuries with an average of six new injuries per club per 22

game season over the past 10 years (Orchard & Seward, 2010). These findings are consistent

with large scale studies completed in professional rugby union where HSIs account for 6 % to

15 % of all injuries suffered during match play (Brooks, Fuller, Kemp, & Reddin, 2005a,

2005b) and in professional soccer where they account for 12 % of all injuries with an average

of eight new injuries per club per season (Ekstrand et al., 2011b).

10

2.4 RECURRENCE OF HAMSTRING STRAIN INJURY

HSIs are associated with a high rate of recurrence (Brooks et al., 2006; Croisier, 2004;

Orchard & Seward, 2002; Orchard & Seward, 2010; Woods et al., 2004), and these

incidences are typically more severe than the initial injury (Brooks et al., 2006; Ekstrand et

al., 2011a). Early research by Seward and colleagues (1993) showed that 34 % of HSIs

sustained in professional Australian football and rugby codes were recurrences (Seward,

Orchard, Hazard, & Collinson, 1993). Recent research in Australian football has shown that

HSI recurrence rates remain a major problem (Orchard et al., 2013), although the rate has

declined in recent years, presumably because of a more cautious approach to treatment and

greater recovery time following injury (Orchard & Seward, 2010). The high recurrence rates

in several sports suggest rehabilitation practices are suboptimal for reducing the risk of future

HSI.

2.5 MECHANISM(S) OF HAMSTRING STRAIN INJURY

HSIs usually involve damage to the muscle tendon unit and are thought to be caused by

forceful eccentric contraction or from an excessive stretch of the muscle tendon unit (Agre,

1985). The proposed mechanisms for HSIs include kicking, tackling, cutting, stooping while

running and excessive stretching (Brooks et al., 2006; Ekstrand & Gillquist, 1983; Verrall,

Slavotinek, Barnes, & Fon, 2003; Woods et al., 2004). However, the majority of HSIs in

running based sports occur during high-speed activities (Bourne, Opar, Williams, & Shield,

2015; Brooks et al., 2006; Opar et al., 2015a; Timmins et al., 2016b; Woods et al., 2004).

During eccentric contractions at medium to long muscle lengths, there are moderate to high

levels of muscle strain (muscle length) (Garrett, 1990). Strong eccentric actions also expose

muscle-tendon units to high degrees of muscle stress, measured as force per unit of cross

sectional area (Garrett, 1990).

11

Some argue that HSI is most likely to occur during the terminal swing phase of running

(Brooks et al., 2005a; Ekstrand et al., 2011a; Woods et al., 2002; Yu et al., 2008) where high

stress (Schache, Dorn, Blanch, Brown, & Pandy, 2012) and moderate strain (Thelen,

Chumanov, Best, Swanson, & Heiderscheit, 2005) is placed on the muscle. There are only

two case studies in which HSI during running has been observed, and both studies suggest

that HSI occurred when the hamstrings were actively lengthening during the terminal swing

phase of running (Heiderscheit et al., 2005; Schache, Wrigley, Baker, & Pandy, 2009).

During the terminal swing phase, the biarticular hamstrings, BFLongHead, ST and SM, all

produce peak force while lengthening (Chumanov, Heiderscheit, & Thelen, 2007; Schache et

al., 2012). However, Schache and colleagues (2012) suggest that the biomechanical load and

therefore the contribution of each of these muscles during this phase are different. The

authors found BFLongHead exhibits the largest peak strain, ST displays the greatest lengthening

velocity, and SM produces the highest peak force, generates the most power and performs the

largest amount of work during the terminal swing phase of running (Schache et al., 2012).

Some authors have investigated differences in peak muscle length during the terminal swing

phase (Chumanov et al., 2007; Chumanov, Heiderscheit, & Thelen, 2011; Thelen,

Chumanov, Hoerth, et al., 2005) and found BFLongHead increases in length by 9.5 %, SM by

7.4 % and ST by 8.1 % relative to the muscle tendon unit length in the anatomical position

(Chumanov et al., 2007, 2011; Thelen, Chumanov, Hoerth, et al., 2005). The BFLongHead

experiences the greatest strain and this may explain why this muscle is most commonly

injured compared to SM and ST during high-speed running (Koulouris, Connell, Brukner, &

Schneider-Kolsky, 2007). The hamstrings undergo some level of stress and strain when they

are active and therefore whenever the magnitude of either is high enough a HSI will occur

(Opar, Williams, & Shield, 2012).

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2.6 PROPOSED RISK FACTORS FOR HAMSTRING STRAIN INJURY

There are several non-modifiable and modifiable risk factors for HSI reported in the

literature. Non-modifiable risk factors include a history of HSI (Arnason et al., 2004; Gabbe,

Bennell, Finch, Wajswelner, & Orchard, 2006; Hagglund et al., 2006; Verrall et al., 2001)

and increasing age (Arnason et al., 2004; Gabbe, Bennell, & Finch, 2006; Hagglund et al.,

2006; Woods et al., 2004). Modifiable risk factors include poor flexibility (Bradley & Portas,

2007; Henderson, Barnes, & Portas, 2010; Witvrouw, Danneels, Asselman, D'Have, &

Cambier, 2003), hamstring muscle weakness (Aagaard et al., 1998; Askling, Karlsson, &

Thorstensson, 2003; Brockett, Morgan, & Proske, 2001; Croisier, Ganteaume, Binet, Genty,

& Ferret, 2008; Orchard, Marsden, Lord, & Garlick, 1997; Petersen, Thorborg, Nielsen,

Budtz-Jorgensen, & Holmich, 2011; Yeung, Suen, & Yeung, 2009), muscle fatigue (Brooks

et al., 2006; Ekstrand et al., 2011a; Woods et al., 2004) and short BFLongHead fascicles

(Timmins et al., 2016b). A thorough understanding of the abovementioned risk factors is

necessary for determining the training strategies required to reduce the risk of initial HSI or

re-injury in athletes.

2.6.1 Non-modifiable risk factors

Previous injury

A history of HSI is a very strong predictor of future HSI (Gabbe, Bennell, Finch, et al., 2006;

Hagglund et al., 2006; Orchard, 2001; Verrall et al., 2001). One prospective study in elite

soccer players has shown that players who suffered a HSI in the previous season were 11.6

times more likely to sustain a recurrent HSI in the subsequent season (Arnason et al., 2004).

This relative risk (RR) is high, but generally consistent with others in both recreational and

elite footballers (Gabbe, Bennell, Finch, et al., 2006; Hagglund et al., 2006; Orchard, 2001;

Verrall et al., 2003).

13

The mechanism(s) increasing the risk of future HSI in individuals with a history of this injury

remain unclear; however, it is likely to occur from the contribution of a number of

maladaptation’s following HSI (Fyfe, Opar, Williams, & Shield, 2013; Opar et al., 2012) or

the persistence of risk factors that contributed to the initial injury (Croisier, Forthomme,

Namurois, Vanderthommen, & Crielaard, 2002; Silder, Heiderscheit, Thelen, Enright, &

Tuite, 2008; Witvrouw et al., 2003).

There have been a number of retrospective observations made in relation to the

maladaptations following injury, such as; the formation of non-functional scar tissue which

impacts muscle tissue lengthening mechanics (Silder, Reeder, & Thelen, 2010), reduced

flexibility (Jonhagen, Nemeth, & Eriksson, 1994), chronic reductions in eccentric strength

(Croisier et al., 2002; Jonhagen et al., 1994; Lee, Reid, Elliott, & Lloyd, 2009), chronic

atrophy of the injured muscle (Silder et al., 2008), alterations in the angle of peak torque

(Brockett, Morgan, & Proske, 2004) and lower limb biomechanics (Verrall et al., 2001),

however, given the lack of prospective evidence it is difficult to determine if these factors are

the cause of or the result of initial injury (Opar et al., 2012).

Increasing age

Previous investigations have identified increasing age as a risk factor for HSI in Australian

footballers (Gabbe, Bennell, & Finch, 2006; Gabbe, Bennell, Finch, et al., 2006; Orchard,

Seward, McGivern, & Hood, 2001; Verrall et al., 2001) and soccer players (Arnason et al.,

2004; Henderson et al., 2010; Woods et al., 2004). Both elite and sub-elite Australian

footballers and soccer players older than 23 to 24 years have been reported to be at an

increased risk of HSI than younger players (Gabbe, Bennell, Finch, et al., 2006). In one study

14

of elite football players, the risk of future HSI was found to increase by 10 % each year of

age (Arnason et al., 2004).

Several studies have attempted to identify the mechanism(s) responsible for why older

athletes are at an increased risk of future HSI (Gabbe, Bennell, & Finch, 2006; Gabbe,

Bennell, Finch, et al., 2006; Opar et al., 2015b). One identified reduced hip flexor flexibility

and increased body weight as age-related changes that were related to HSI risk in Australian

footballers older than 25 years, although the associated relative risks were very small (Gabbe,

Bennell, & Finch, 2006). Others have suggested that age-related reductions in knee flexor

strength may account for increased injury rates (Gabbe, Bennell, Finch, et al., 2006), but

these assertions were based on cross-sectional studies that included older participants than

those who play elite sport (Doherty, 2001; Kirkendall & Garrett, 1998).

2.6.2 Modifiable risk factors

Poor flexibility

It has been suggested that during eccentric contractions high forces are produced which are

absorbed by the active contractile components and passive in-series elements of muscle

(Bennell et al., 1998). Earlier work proposed that the compliance of passive elastic

components may improve the musculotendinous junction’s ability to absorb energy which

would reduce loads placed on the active contractile components of muscle and reduce the risk

of strain injury (Garrett, 1990; Garrett, Safran, Seaber, Glisson, & Ribbeck, 1987).

Despite the theory, there is conflicting evidence around flexibility as a risk factor for future

HSI. A prospective study by Witvrouw and colleagues (2003) found that players with lower

levels of hamstring flexibility had significantly higher rates of HSI compared to players

without a HSI. However, three other prospective studies have shown that hamstring

15

flexibility was not associated with subsequent injury (Arnason, Andersen, Holme,

Engebretsen, & Bahr, 2008; Engebretsen, Myklebust, Holme, Engebretsen, & Bahr, 2010;

Henderson et al., 2010). Interestingly, there has been no relationship identified between

flexibility and risk of future HSI in elite Australian footballers (Gabbe, Bennell, Finch, et al.,

2006; Orchard et al., 1997). Despite the mixed evidence that poor flexibility contributes to

hamstring injury, studies have shown ongoing (Jonhagen et al., 1994; Warren, Gabbe,

Schneider-Kolsky, & Bennell, 2010) or transient (Maniar, Shield, Williams, Timmins, &

Opar, 2016) deficits in hamstring flexibility in players with a history of HSI which may be

due to scar tissue formation, a known maladaptation to previous HSIs (Silder et al., 2008).

Hamstring muscle weakness and between limb strength imbalance

Strength deficits (Burkett, 1970) and between limb imbalances (Zakas, 2006) have previously

been suggested as risk factors for future HSI (Opar et al., 2012). For this review, between-

limb imbalance refers to knee flexor weakness, between-leg asymmetry in knee flexor

strength and/or a low knee flexor to knee extensor strength ratio, commonly known as the

hamstring-to-quadriceps (H:Q) ratio.

Croisier and colleagues (2008) completed the largest prospective study investigating bilateral

strength asymmetries using isokinetic dynamometry to determine if between-limb asymmetry

of greater than 15 % and low eccentric hamstrings to concentric quadriceps strength ratios

(the functional H:Q ratio) could predict future risk of HSI (Croisier et al., 2008). This study

included 462 elite soccer players who had hamstring strength assessments during the

preseason using a standardised concentric and eccentric isokinetic dynamometer protocol. At

the conclusion of the competitive season, players who did not display large strength

imbalances or low functional H:Q ratios in the pre-season and those who completed a training

16

intervention to reduce imbalances and then performed a subsequent re-test, demonstrated low

incidence rates of HSI (Croisier et al., 2008). By contrast, players with between limb

asymmetry or low functional H:Q ratios who did not follow a strength training intervention

had four times greater risk of HSI (Croisier et al., 2008).

In Australian football, players who were weaker in pre-season concentric isokinetic tests of

hamstring strength had a significantly greater risk of HSI during the competitive season

(Orchard et al., 1997). Early evidence revealed that between-limb asymmetries greater than

10 % were a strong predictor of future HSI in American footballers and track and field

athletes (Burkett, 1970; Heiser, Weber, Sullivan, Clare, & Jacobs, 1984). Evidence from

isokinetic strength assessments completed during pre-season suggests that Australian

footballers with between-limb asymmetries greater than 8 % (Orchard et al., 1997) and elite

soccer players with more than 15 % between-limb asymmetries (Croisier et al., 2008) were

at an increased risk of future HSI. Recently, Bourne and colleagues (2015) investigated

eccentric hamstring strength using the NordBord™ and found that Rugby players who

displayed greater than 15 % to 20 % between limb imbalances in eccentric knee flexor

strength were at a 2.4 to 3.4-fold greater risk of HSI. It is noteworthy that some prospective

studies have shown no association between isokinetic knee flexor strength and risk of future

HSI (Bennell et al., 1998; Yeung et al., 2009). The level of between-limb knee flexor strength

imbalance and the contribution of other muscles during the terminal swing phase are areas of

future research given these are known to influence running mechanics (Lee et al., 2009).

Muscle fatigue

Fatigue is often proposed as a potential cause of HSI (Heiser et al., 1984; Mair, Seaber,

Glisson, & Garrett, 1996) and several studies have shown that the incidence of HSIs is higher

17

during the later stages of training or competition (Brooks et al., 2006; Ekstrand et al., 2011b;

Garrett, 1990; Woods et al., 2004). Garrett and colleagues (1987) were the first to investigate

the effect of fatigue on muscle lengthening in in situ animal muscles. In this study, muscle

was found to absorb twice as much energy when activated and stretched until failure

compared to passively stretched muscle (Garrett et al., 1987). Mair and colleagues (1996)

found muscles that were pre-fatigued using electrical stimulation absorbed less energy before

failure compared to unfatigued muscles. These findings demonstrate that the energy-

absorbing capability of a muscle is diminished in a fatigued state (Mair et al., 1996).

Fatigue has been found to cause proprioceptive changes in humans (Allen, Leung, & Proske,

2010; Skinner, Wyatt, Hodgdon, Conard, & Barrack, 1986). For example, Allen and

colleagues (2010) showed that fatiguing the knee flexors caused participants to perceive their

knee to be in a more flexed position than it was and proposed that alterations at the level of

the sensorimotor cortex were responsible. Furthermore, there is evidence to show that a

fatiguing intermittent running protocol and knee flexor resistance training session caused

participants to display increased knee extension and reduced hip flexion during the terminal

swing phase of running (Pinniger, Steele, & Groeller, 2000). Any increase in knee extension

during the terminal swing phase would generate greater strain on the hamstrings. However, a

concomitant decrease in hip flexion was also reported in this study (Pinniger et al., 2000), so

the significance of this change on injury risk is uncertain. If hamstring length were

underestimated, this could potentially result in repeated over-lengthening of the hamstrings

during running. Studies have shown that intermittent running protocols specific to the

demands of competitive soccer, result in significant reductions in eccentric hamstring torque

without reductions in concentric knee flexor or extensor strength (Greig, 2008; Small,

McNaughton, Greig, Lohkamp, & Lovell, 2009). These findings are of interest given the

18

likelihood that HSIs occur during forceful eccentric contractions (Brockett et al., 2004;

Croisier, 2004).

Short BFLongHead head fascicles

Timmins and colleague’s (2016) prospective study in elite Australian soccer players showed

that BFLongHead fascicles shorter than 10.56 cm were associated with 4.1 times (95 % CI, 1.9

to 8.7) increased risk of HSI. The study also reported that the risk of HSI in older players or

those with a prior history of HSI is reduced when players have longer BFLongHead fascicles.

Reduced fascicle lengths are most likely caused by losing in-series sarcomeres (Lieber &

Friden, 2000) which may increase the BFLongHead muscles susceptibility to muscle damage at

longer lengths.

2.6.3 Interaction between modifiable and non-modifiable risk factors

As mentioned above, recent evidence suggests that the effects of age on HSI risk may be

countered by changes to one or more modifiable risk factors (Opar et al., 2015b; Timmins et

al., 2016b). For example, elite Australian footballers older than 23 years are at a heightened

risk of HSI if they display low levels of eccentric knee flexor strength, but the effects of age

are significantly smaller in stronger players (Opar et al., 2015a; Timmins et al., 2016b). More

recently, Timmins and colleagues (2016b) found that higher levels of eccentric knee flexor

strength and longer BFLongHead fascicles reduced the risk of HSI in older elite soccer players.

However, further investigations are needed to improve the understanding of increasing age

and HSI risk.

2.7 DEFINITION OF ANTERIOR CRUCIATE LIGAMENT INJURY

ACL injuries are characterised as partial or complete tears and defined using three grades of

severity, including; grade 1 involves minor micro-tears of the ligament with minimal loss of

19

function; grade 2 involves more severe tears of the ligament with some loss of function; and

grade 3 involves a complete rupture of the ligament and major loss of function (Levangie &

Norkin, 2011). A complete tear (grade 3) is the most common and is typically associated with

additional damage to other knee structures, including; joint cartilage, cancellous bone,

meniscus and other collateral ligaments (Arnoczky, 1983). The severity of injury is

dependent on the magnitude and direction of forces applied to the knee joint at the time of

injury (Alentorn-Geli et al., 2009a). When the ACL ruptures, a loud ‘pop’ is often heard with

an immediate sense of the knee giving way or buckling when weight is applied to the joint,

then the knee begins to swell due to the bleeding associated with the damaged blood vessels

of the ligament (Spindler & Wright, 2008). To determine the severity of the injury, a clinician

will complete a physical examination using the Lachman test and the pivot shift test.

Additionally, MRI is typically required to confirm an ACL tear, however, this is usually

identified during the physicians physical examination (Spindler & Wright, 2008).

2.8 INCIDENCE OF ANTERIOR CRUCIATE LIGAMENT INJURY

ACL injuries are debilitating and usually result in a lengthy period out of sport and are

sometimes career ending (Roi, Nanni, & Tencone, 2006; Walden, Hagglund, Magnusson, &

Ekstrand, 2016). Collectively, there are reportedly 100,000 to 300,000 ACL injuries each

year in Australia and the United States (Boden, Griffin, et al., 2000; Prodromos, Han, et al.,

2007) and many occur in men and women between 15 and 25 years of age (Renstrom et al.,

2008). Recently, a large prospective study in men’s professional soccer by Walden and

colleagues (2017) reported an ACL injury rate of 0.4 per club per season. The ACL injury

rate in men’s professional soccer is not declining despite several randomised controlled trials

demonstrating that neuromuscular training programs can reduce ACL injury rates in sub-elite

men’s and women’s handball, soccer, basketball and volleyball (Hewett, Lindenfeld,

20

Riccobene, & Noyes, 1999; Silvers-Granelli et al., 2015; Walden, Atroshi, Magnusson,

Wagner, & Hagglund, 2012).

Low compliance with evidence-based exercises for reducing hamstring strain injuries has

been identified in professional soccer (Bahr, Thorborg, & Ekstrand, 2015) and the same may

be true for exercises aimed at reducing ACL injuries. In the Australian Football League, ACL

injury has accounted for 12.1 games missed per club per season over the past 10 years,

second only to hamstring strain injury (21.1 games per club per season) (Orchard et al.,

2013). Furthermore, the incidence rate of one new ACL injury per club per season is low

(Orchard et al., 2013), although, an ACL injury typically requires a minimum of 9 to 12

months out of sport for complete recovery (Ardern, Webster, Taylor, & Feller, 2011a;

Ardern, Webster, Taylor, & Feller, 2011b; Webster, Feller, & Whitehead, 2017), so these

injuries are markedly more severe than hamstring strains as they result in a longer time out of

sport and have more severe long term implications such as knee osteoarthritis. The highest

frequencies of ACL injury are in intermittent-sprint team sports that involve pivoting, cutting,

sudden deceleration, jumping and landing (Bahr & Krosshaug, 2005; Boden, Dean, Feagin, &

Garrett, 2000; Renstrom et al., 2008). Women are 2-8 times more likely to sustain an ACL

injury than males (Adirim & Cheng, 2003; Arendt & Dick, 1995) and there are a range of

possible reasons why women are more susceptible to injury. It appears that anatomical

(Hewett et al., 2006; Landry, McKean, Hubley-Kozey, Stanish, & Deluzio, 2007; Silvers &

Mandelbaum, 2011) and sex hormone level differences (Habelt, Hasler, Steinbruck, &

Majewski, 2011; Hewett et al., 2006; Huston, Greenfield, & Wojtys, 2000; Renstrom et al.,

2008) contribute to the heightened ACL injury risk in women.

21

2.9 RECURRENCE OF ANTERIOR CRUCIATE LIGAMENT INJURY

A history of ACL injury is associated with an increased risk of a new knee injury (Faude,

Junge, Kindermann, & Dvorak, 2006; Walden, Hagglund, & Ekstrand, 2006) and long-term

morbidity such as osteoarthritis (Lohmander, Ostenberg, Englund, & Roos, 2004). Athletes

involved in sports that require pivoting and jumping, very often require ACLR to restore knee

joint stability before they can return to sport (Hewett, Di Stasi, & Myer, 2013). There is a

general belief that ACLR is required to return to sport, however, even the best level of

evidence does not support this claim (Frobell et al., 2010; Frobell et al., 2013). In elite soccer,

the ACL injury recurrence (graft failure) rate is 7 % to 35 % (Arnason, Gudmundsson, Dahl,

& Johannsson, 1996; Hawkins & Fuller, 1999; Hawkins, Hulse, Wilkinson, Hodson, &

Gibson, 2001; Walden, Hagglund, & Ekstrand, 2005) while in Australian footballers a prior

ACLR has been identified as a strong risk factor for future ACL injury (Orchard et al., 2001).

Moreover, the risk of secondary ACL injury in young adults (<25 years) is reportedly 20 % to

40 % which is significantly high (Webster & Feller, 2016; Webster, Feller, Kimp, &

Whitehead, 2018). The consequences of a second ACL injury and subsequent ACLR are

typically worse than for index injuries (Hewett et al., 2013; Spindler et al., 2013). The

augmented risk of new knee injury in athletes with a history of ACL injury could be

explained by altered kinematics and diminished proprioception after initial injury (Hewett et

al., 2013; Hewett et al., 1999).

2.10 MECHANISM(S) OF ANTERIOR CRUCIATE LIGAMENT INJURY

The ACL is commonly injured via a non-contact mechanism during sports participation

(Alentorn-Geli et al., 2009a; Ardern et al., 2011a; Griffin et al., 2000; Silvers &

Mandelbaum, 2007) and typically this occurs during pivoting, cutting, sudden deceleration,

jumping and landing movements (Bahr & Krosshaug, 2005; Boden, Dean, et al., 2000;

22

Renstrom et al., 2008). ACL injury may also occur via direct contact with an object or

another player (Alentorn-Geli et al., 2009a; Griffin et al., 2000; Hewett et al., 2006), though

usually occurs during foot strike with the ground with concurrent low knee flexion angle,

knee joint rotation and knee valgus or collapse (Alentorn-Geli et al., 2009a; Serpell, Scarvell,

Ball, & Smith, 2012). Knee valgus is hazardous as it increases the load on the ACL while

also stressing other knee joint structures such as the medial collateral ligament and meniscus

(Habelt et al., 2011; Hewett et al., 2005).

The prevalence of meniscal tear during ACL injury is 55 % to 65 % (Noyes & Barber-

Westin, 2012; Smith & Barrett, 2001), while some authors report more lateral meniscal tears

(Bellabarba, Bush-Joseph, & Bach, 1997) and others more medial meniscal tears (Smith &

Barrett, 2001) at the time of injury, although, medial meniscal tears appear to be more

common in ACL deficient knees (Smith & Barrett, 2001; Wickiewicz, 1990). The lateral

meniscus is loosely attached to the tibial plateau and provides little to no stabilisation in the

knee although the medial meniscus is firmly attached to the tibia and provides significant

stabilisation in the knee (Smith & Barrett, 2001). These anatomical differences are proposed

to expose the lateral and medial menisci to different forces and different mechanisms of

injury (Smith & Barrett, 2001).

The balance of muscle activation between the hamstrings and quadriceps has been suggested

to play an important role in ACL injury prevention (Besier et al., 2003; Zebis, Andersen,

Bencke, Kjaer, & Aagaard, 2009). There are studies that suggest high knee joint loads

experienced when landing and an imbalance between weak knee flexors and strong knee

extensors contribute to dynamic knee instability during side-cutting and landing tasks

(Hewett et al., 2006; McLean, Huang, & van den Bogert, 2005). The active hamstrings

23

function to unload the ACL as they take on a significant share of the forces created by

anterior tibial translation. As a consequence, it has been proposed that strengthening of this

muscle group may be important for the prevention of ACL injury (Serpell et al., 2012). It is

well established that non-contact ACL injuries are multifactorial (Griffin et al., 2000; LaBella

et al., 2014). However, it is of further interest to investigate the influence of hamstring

function on ACL injury prevention and rehabilitation.

2.11 PROPOSED RISK FACTORS FOR ANTERIOR CRUCIATE LIGAMENT

INJURY

There are several non-modifiable and modifiable risk factors for ACL injury reported in the

literature. Non-modifiable risk factors include a previous ACL injury (Bahr & Bahr, 1997;

Gianotti, Marshall, Hume, & Bunt, 2009; Messina, Farney, & DeLee, 1999), sex (Arendt &

Dick, 1995; Myklebust, Maehlum, Holm, & Bahr, 1998), anatomical differences (Chaudhari,

Zelman, Flanigan, Kaeding, & Nagaraja, 2009; Myer, Ford, Paterno, Nick, & Hewett, 2008;

Shelbourne, Davis, & Klootwyk, 1998; Uhorchak et al., 2003), female sex hormone levels

(Hewett, Zazulak, & Myer, 2007; Myklebust et al., 1998; Renstrom et al., 2008; Slauterbeck

et al., 2002), environment (e.g., playing surface) (Orchard & Seward, 2002) and equipment

(e.g., knee bracing) (Griffin et al., 2000). Modifiable risk factors include characteristics that

can be modified with training. For this review, these will include deficits in strength and

activation of hip and knee muscles, H:Q ratio (Ahmad et al., 2006; Myer et al., 2009),

proprioception (Friden, Roberts, Ageberg, Walden, & Zatterstrom, 2001; Renstrom et al.,

2008), knee valgus (Hewett et al., 2005; Zazulak, Hewett, Reeves, Goldberg, & Cholewicki,

2007) and muscle fatigue (Zebis et al., 2011).

24

2.11.1 Non-modifiable risk factors

Previous injury

A history of ACL injury is a strong risk factor for subsequent re-injury (Bahr & Bahr, 1997;

Gianotti et al., 2009; Messina et al., 1999) and this is due to many factors, including; sub-

optimal surgery, muscular weakness and imbalances, weakening of ligaments, altered

kinematics and diminished proprioception after initial injury (Hewett et al., 2013; Hewett et

al., 1999; Murphy, Connolly, & Beynnon, 2003). Some studies have found that the risk of

future ACL injury is higher for the contralateral uninjured limb compared than the previously

injured limb (Boden, Dean, et al., 2000; Hewett et al., 2006). The incidence of ACL injury

within two years of ACLR and subsequent return to sport was 6-fold higher in athletes with a

history of ACL injury compared to uninjured athletes (Paterno, Rauh, Schmitt, Ford, &

Hewett, 2012). Furthermore, it appears the greatest risk for re-injury is 12 to 24 months after

ACLR, and this is typically when athletes return to competitive sport (Paterno et al., 2012;

Paterno, Rauh, Schmitt, Ford, & Hewett, 2014). A history of ACL injury results in deficits in

proprioception and range of motion which may alter the coordination of previously learnt

movements (Paterno et al., 2012, 2014). Walden and colleagues (2006) showed that 50 % of

athletes with a history of ACL injury and subsequent reconstruction go on to suffer an

overuse knee injury such as bursitis, tendinitis or patellofemoral pain syndrome. This

suggests greater care should be taken from early to late stage rehabilitation to ensure

successful recovery before players return to competition in their respective sports (Walden et

al., 2015). It may be that after ACLR, persistent neuromuscular and biomechanical risk

factors occur which render athletes at greater risk of future re-injury (Alentorn-Geli et al.,

2009a; Hewett et al., 1999; Hewett et al., 2006; Mandelbaum et al., 2005).

25

Sex

Many studies have shown that more ACL injuries occur in females than males (Arendt &

Dick, 1995; Dugan, 2005; Hewett et al., 1999; Hewett et al., 2006). The massive increase in

sport participation for women over the past 30 years has resulted in a greater number of ACL

injuries, hence it seems likely that the number of injuries will continue to increase (Griffin et

al., 2000). A range of neuromuscular, biomechanical and hormonal changes occur during

adolescence which is believed to be, in some way, responsible for this increased risk of injury

in women (Ford et al., 2005; Griffin et al., 2000; Hewett et al., 2006). During adolescence,

males and females grow in both height and weight, and this produces a higher centre of mass

and larger joint forces (Alentorn-Geli et al., 2009a; Hewett et al., 2005; McLean, Walker, &

van den Bogert, 2005). However, between the ages of 12 to 18, females do not experience the

same increases in power, strength and coordination as males (Alentorn-Geli et al., 2009a;

Hewett et al., 2006; Uhorchak et al., 2003) and this may affect the ability of females to

control dynamic lower body movements (Hewett et al., 2006). It has previously been

suggested there are no difference in ACL injury rates in pre-pubertal (<12 years old) athletes;

however, once puberty commences (>12 years old) females exhibit higher injury rates than

males (Ford et al., 2005).

Epidemiological research has shown that the highest incidences of ACL injuries occur in 15-

25-year-old athletes (Bahr & Engebretsen, 2011; Hewett et al., 2005; Myer, Ford, Brent, &

Hewett, 2007), and females, particularly adolescents (Hewett et al., 2005), have a 2 to 8 fold

greater risk of non-contact ACL injury than males (Adirim & Cheng, 2003; Arendt & Dick,

1995).

26

Anatomical differences

A range of anatomical factors have been suggested to increase the risk of ACL injury in

females (Hewett et al., 2006). These include femoral intercondylar notch width, ACL size,

quadriceps angle, hip width, flexibility and joint laxity (Hewett et al., 2006; Landry et al.,

2007; Silvers & Mandelbaum, 2011).

Females are known to display smaller femoral notch widths relative to the size of the ACL

compared to males (Dugan, 2005; Ford et al., 2005; Silvers & Mandelbaum, 2011). Narrower

intercondylar notches have been shown in a meta-analysis to be associated with ACL injury

risk (Zeng et al., 2013) and are argued to predispose females to an increased ACL injury risk

because of their correlation with smaller and weaker ACL’s (Griffin et al., 2000; Hewett et

al., 2006; Peterson & Krabak, 2014). Further, smaller intercondylar notches may place

excessive stretch on the ACL under high loads (Alentorn-Geli et al., 2009a; Hewett et al.,

2006). However, the impact narrow femoral intercondylar notch widths has on ACL injury

rates has not been determined (Arendt & Dick, 1995; Griffin et al., 2000; Hewett et al., 2006;

Malinzak, Colby, Kirkendall, Yu, & Garrett, 2001).

Many studies have investigated the quadriceps angle and found a direct correlation with ACL

injury incidences in female athletes (Dugan, 2005; Hewett et al., 2005; Myer et al., 2009).

Previously, the quadriceps angle has been defined as the angle between the line connecting

the anterior superior iliac spine and the middle of the patella, and the line connecting the

tibial tubercle and the same reference point of the patella (Dugan, 2005). Naturally, females

have wider hips relative to their height, and because the distance between their feet during

standing is not greater than that of males, there is an increased angle between the long axis of

the femur and tibia (Myer, Ford, & Hewett, 2005).

27

2.11.2 Modifiable risk factors

Deficits in muscle strength and activation of hip and knee muscles

The initiation of movement and the provision of stability in the lower body involves

coordinated muscle activation (Griffin et al., 2000). As mentioned previously, females

display quadriceps dominance and relatively lower activation of the hamstrings during side-

cutting and jump-landing tasks compared to men (Griffin et al., 2000; Zebis et al., 2008).

There are also likely differences between trunk and hip muscle strength and control between

male and female athletes that may contribute to the sex differences in ACL injury rates

(Griffin et al., 2000; Hewett et al., 2006). Hip strength is known to play a significant role in

the control of frontal plane knee motion (Jacobs, Uhl, Mattacola, Shapiro, & Rayens, 2007;

Stearns & Powers, 2014). Accordingly, weakness of hip abductor muscles may increase ACL

injury risk by predisposing athletes to greater hip adduction and internal rotation that increase

medial knee motion and knee abduction moments (Jacobs et al., 2007; Stearns & Powers,

2014). Females are known to display deficits in hip extensor strength and reduced activation

of hip muscles (Griffin et al., 2000; Osborne, Quinlan, & Allison, 2012). Athletes with

stronger hip abduction may reduce the load on the ACL and risk of future ACL injury (Jacobs

et al., 2007; Stearns & Powers, 2014).

H:Q ratio

The H:Q ratio is defined as the peak concentric or eccentric knee flexion torque divided by

the peak concentric knee extensor torque (Aagaard et al., 1998). The earliest uses of the H:Q

ratio involved concentric knee flexor and concentric knee extensor strength, which is now

referred to as the conventional H:Q ratio (Myer et al., 2009). This technique came under

scrutiny as it failed to consider that the hamstrings actively lengthen while decelerating the

flexing hip and extending knee during running (Myer et al., 2009). As a consequence, the

28

functional ratio, which involves measures of eccentric knee flexion to concentric knee

extension strength has become more widely accepted (Aagaard et al., 1998). Both the

hamstrings and quadriceps are active restraints of the knee which work together to protect

knee ligaments and other joint structures. Furthermore, the balance of strength and activation

of the hamstring and quadriceps muscles are critical to maintaining knee stability with a

number of studies reporting that a reduced H:Q ratio increases the risk of ACL injury

(Holcomb, Rubley, Lee, & Guadagnoli, 2007; Myer et al., 2009; Soderman, Alfredson,

Pietila, & Werner, 2001).

Deficits in hamstring muscle activation

Because the hamstrings help to unload the ACL during anterior tibial translation, altered

hamstring function may increase the risk of future ACL injury. The medial and lateral

hamstrings have different actions at the knee joint in the frontal plane so the interplay

between these muscles may be a risk factor for ACL injury. Most often in field sports, non-

contact ACL injuries occur when changing direction while running (Cochrane et al., 2007;

Serpell et al., 2012). Surface electromyography (sEMG) studies have shown that both

hamstring and quadriceps activity increases significantly in ‘cutting’ movements (Besier et

al., 2003; Besier, Lloyd, Ackland, & Cochrane, 2001; Zebis et al., 2009). Furthermore, the

balance between hamstring and quadriceps muscles have been proposed to identify athletes

with an increased risk of ACL injury (Besier et al., 2003; Zebis et al., 2009). These studies

demonstrate reduced hamstring to quadriceps activity likely to reduce knee flexion and

subsequently increase ground reaction force and anterior tibial translation at the knee joint

(Besier et al., 2003; Hewett, Myer, & Ford, 2001; Myer et al., 2009; Zebis et al., 2009).

Evidence suggests that high activation of the medial hamstrings during side-cutting tasks may

29

protect the ACL from external shear forces which are known to produce anterior tibial

translation and knee valgus moments (Lloyd & Buchanan, 2001; Myer et al., 2009).

Myer and colleagues (2009) prospective study on the relationship between hamstrings to

quadriceps strength ratio reported that a low H:Q ratio and reduced hamstring strength were

risk factors for ACL injury in female athletes. Conversely, a four-year prospective study

involving 895 male and female military cadets reported that the H:Q ratio was not a risk

factor for ACL injury (Uhorchak et al., 2003). These findings are supported by others (Vacek

et al., 2016).

The medial and lateral hamstrings contribute differently to knee stability. For example, the

medial hamstrings (ST and SM) are responsible for medial rotation and varus stress at the

knee, while the lateral hamstrings (BFLongHead and BFShortHead) are responsible for external

rotation and knee valgus (Besier et al., 2003; Besier et al., 2001; Zebis et al., 2009). If the

contribution of the medial or lateral hamstrings is compromised then the hamstring activation

relative to quadriceps activation will be reduced which may increase the risk of ACL injury.

Females display significantly greater activation of the lateral hamstrings compared to males

when decelerating from a jump-landing task (Rozzi, Lephart, Gear, & Fu, 1999) which

increases knee valgus loading, a common mechanism of ACL injury. Given the medial

hamstrings contribute to knee varus loading, any deficits in the function of the medial

hamstrings may increase knee valgus and thereby increase the risk of ACL injury in females

(Rozzi et al., 1999). It has been argued that the ST may be particularly important for the

prevention of ACL injury because contraction of this muscle has the potential to reduce

dynamic knee valgus and external rotation (Buchanan, Kim, & Lloyd, 1996). Hewett and

30

colleagues’ (2005) prospective study on drop-jump landings reported that dynamic knee

valgus displayed during a landing phase predisposed female athletes to an ACL injury.

Similarly, Zebis and colleagues (2009) studied a side-cutting task and suggested that low

activation of ST and higher levels of activation of vastus lateralis, when measured using

sEMG, may increase the risk of ACL injury. The Nordic hamstring exercise has been shown

to selectively activate the ST in male athletes (Bourne, Opar, Williams, Al Najjar, & Shield,

2016; Bourne, Williams, et al., 2017; Mendiguchia, Arcos, et al., 2013) and is commonly

employed in ACL injury prevention programs (Sugimoto, Myer, Foss, & Hewett, 2015).

High levels of muscle activation are an important stimulus for improving strength and

voluntary activation (Kraemer et al., 2002) and strengthening of the hamstrings to reduce

anterior shear force produced by the quadriceps may protect the ACL.

Proprioception

The receiving of sensory input from muscles, tendons and joints and the capacity of the

central nervous system to process and act appropriately on the basis of this information is

known as proprioception or neuromuscular control (Hewett, Paterno, & Myer, 2002).

Neuromuscular training is a process which involves learning how to move more effectively

(Mandelbaum et al., 2005), while neuromuscular control involves the activation of dynamic

restraints surrounding a joint in response to sensory stimuli (Griffin et al., 2000; Hewett et al.,

2005). This control requires proficient communication between the afferent and efferent

pathways of the central nervous system (Blackburn et al., 2013; Ford et al., 2005). Many

intervention studies have employed neuromuscular training programs in an attempt to reduce

ACL injury risk (Heidt, Sweeterman, Carlonas, Traub, & Tekulve, 2000; Mandelbaum et al.,

2005; Myklebust et al., 2003). Multiple systematic reviews and meta-analyses have examined

the effectiveness of neuromuscular training programs by comparing the number of ACL

31

injuries between the intervention and control groups. These studies have consistently reported

that neuromuscular training programs effectively reduce ACL injury rates in female athletes

(Grimm, Jacobs, Kim, Denney, & Shea, 2015; Myer, Sugimoto, Thomas, & Hewett, 2013;

Taylor, Waxman, Richter, & Shultz, 2015). By contrast, the same results are often not found

in males (Engebretsen, Myklebust, Holme, Engebretsen, & Bahr, 2008; Taylor et al., 2015;

van Beijsterveldt et al., 2012).

Lower baseline strength and power capacities in females may explain why they appear to

benefit more than males from training interventions (Myer et al., 2013; Sugimoto, Myer,

McKeon, & Hewett, 2012). Unfortunately, the term ‘neuromuscular training’ is excessively

broad and ill-defined. There is no type of physical exercise that fit under this umbrella term.

The injury prevention literature also includes many diverse neuromuscular training programs,

making it difficult to determine which components of these programs provide the greatest

prophylactic effects (Taylor et al., 2015). Regardless, the effectiveness of the neuromuscular

training program appear to be influenced by the age of participants, type and number of

exercises, the level of compliance and dosage of the program (Myer et al., 2013; Sugimoto,

Myer, Foss, & Hewett, 2014).

Knee valgus

Both knee valgus angle and moments during drop landings have been identified as predictors

of ACL injury (Hewett et al., 2005). Knee valgus has been suggested to be related to muscle

weakness at the trunk, hip or knee joints (Alentorn-Geli et al., 2009a; Ekegren, Miller,

Celebrini, Eng, & Macintyre, 2009; Myer, Ford, & Hewett, 2005; Powers, 2010). Inadequate

strength and activation of hip muscles can result in dysfunction in all three planes of motion

32

(frontal, transverse and sagittal) and thereby have consequences to distal segments of the

lower limb (Powers, 2010).

As mentioned previously, dynamic knee valgus occurs as a consequence of excessive hip

adduction and internal hip rotation which causes the knee to shift medially to the weight

bearing foot (Powers, 2010). Medial displacement of the knee joint also causes external

rotation of the tibia relative to the femur and pronation of the foot (Powers, 2010; Schmitz,

Shultz, & Nguyen, 2009). It has been argued that hip adduction weakness is the primary

factor for dynamic knee valgus positions (Powers, 2010; Stearns & Powers, 2014), although,

deficits in strength and activation of the hamstrings have also been proposed to contribute

significantly to dynamic knee valgus (Zebis et al., 2008; Zebis et al., 2013).

Muscle fatigue

Muscle fatigue has been suggested as a risk factor for ACL injury (Walden et al., 2016; Zebis

et al., 2011). Fatigued, muscles are unable to adequately absorb energy and this may increase

the loads on other structures and ligaments of the knee joint (Alentorn-Geli et al., 2009a;

Gehring, Melnyk, & Gollhofer, 2009; Greig, 2008). The effects of fatigue on ACL injury risk

factors are inconsistent (Barber-Westin & Noyes, 2017). Studies have shown that men and

women display different responses during a fatiguing task and that the magnitude of sex

differences is task specific (Hunter, 2009). In professional soccer, fatigue seems to be an

unlikely risk factor for ACL ruptures, because most injuries are sustained in the first half or

soon after players enter a match (Walden et al., 2015). More prospective studies investigating

the effects of fatigue on ACL injury risk are warranted.

33

Female sex hormone levels

The variability of sex hormone concentrations during the female menstrual cycle has

previously been suggested as a risk factor for ACL injury (Habelt et al., 2011; Hewett et al.,

2006; Huston et al., 2000; Renstrom et al., 2008). Recent evidence suggests that women who

take oral contraceptive pills may lower their risk of ACL injury by 20 % (Herzberg et al.,

2017). It is suggested that higher estrogen concentrations during the mid-stage of the

menstrual cycle may reduce the tensile strength of the ACL, while also hindering motor skills

that influence the protective neuromuscular mechanisms of the knee (Boden, Griffin, et al.,

2000). Others have argued that hormone fluctuations may impair the structure and function of

the ACL, proprioceptive feedback loops and load bearing capabilities of the ACL (Dugan,

2005). These findings are inconsistent (Myklebust et al., 1998) with further investigation

necessary to determine the effect of hormone fluctuations on the structural properties of the

ACL (Boden, Griffin, et al., 2000).

Environmental

Weather conditions

Orchard and colleagues (2002) have shown that more ACL injuries are sustained during dry

than wet conditions for reasons discussed below.

Shoe-surface interaction

The relationship between shoe type and playing surface has previously been identified as a

risk factor for ACL injury specifically when there is a high level of friction between an

athlete’s shoes and the playing surface (Orchard, 2002). It has been argued that greater shoe-

surface friction and torsional resistance in dry conditions cause a greater number of ACL

injuries (Orchard, 2002; Orchard et al., 2001). It is noteworthy that higher levels of friction

34

between shoe type and playing surface also produce higher levels of sport performance

(Malisoux, Gette, Urhausen, Bomfim, & Theisen, 2017).

Knee bracing

Knee bracing has been proposed to improve proprioception (Griffin et al., 2000) and thereby

reduce the risk of ACL injuries (Griffin et al., 2000; Hewett et al., 2006). However, there is

no conclusive evidence to show that knee braces prevent ACL injuries.

2.12 CONSEQUENCES OF ANTERIOR CRUCIATE LIGAMENT INJURY

2.12.1 ACL reconstruction

ACLR is widely considered to be required in sports involving rapid jumping and

pivoting, and a range of different procedures have previously been investigated with some

authors finding surgical (Fink, Hoser, Hackl, Navarro, & Benedetto, 2001) or non-surgical

(Giove, Miller, Kent, Sanford, & Garrick, 1983) treatments more beneficial than the other.

Many surgeons recommend surgery, yet the decision is heavily influenced by the severity of

the injury, age and activity level of the patient and cost of surgery and rehabilitation

(Arnason, Birnir, Guethmundsson, Guethnason, & Briem, 2014; Macaulay, Perfetti, &

Levine, 2012). There is a general belief that ACLR is required to return to sport, however,

even the best level of evidence does not support this claim (Frobell et al., 2010; Frobell et al.,

2013). Nevertheless, rehabilitation without surgery has also been shown to be a good

alternative for management of an ACL injury (Weiler, Monte-Colombo, Mitchell, & Haddad,

2015), although this does not eliminate the possibility of future surgical treatment (Myklebust

& Bahr, 2005). Moreover, ACLR surgery usually involves either an allograft, which involves

a tissue graft that is surgically transplanted from one person to another, or an autograft, which

35

involves a tissue graft that is surgically transplanted from one part of a person’s body to

another (Macaulay et al., 2012; Prodromos, Joyce, & Shi, 2007). The benefits of allografts

include the absence of harvest site morbidity and lower postoperative pain (Kaeding et al.,

2011; Macaulay et al., 2012). However, the risk of postoperative graft failure is 2 to 4 times

greater when allografts are used compared to autografts (Krych, Jackson, Hoskin, & Dahm,

2008; Prodromos, Joyce, et al., 2007). A meta-analysis reported an odds ratio of 5.03 times

greater risk of graft failure when patients were treated with allografts compared to autografts

(Krych et al., 2008). Given these data, autografts are the preferred surgical choice, and their

other benefits include improved joint stability, lower risk of infection and earlier return to

sport (Bonasia & Amendola, 2012).

The two most common autografts are from either the ipsilateral ST and gracilis or patellar

tendon (Aune et al., 2001; Gobbi & Francisco, 2006; Paterno et al., 2010; Pinczewski et al.,

2002; Pinczewski et al., 2007). Patellar tendon grafts have been the most popular surgical

choice, though hamstring tendon grafts have recently become more common (Ejerhed et al.,

2003). Interestingly, there is no gold standard treatment for ACL injury and graft selection is

often heavily biased by surgeon opinion (Bonasia & Amendola, 2012; Macaulay et al., 2012).

Notably, regardless of the chosen graft, deficits in eccentric and concentric knee extensor

(Knezevic, Mirkov, Kadija, Nedeljkovic, & Jaric, 2014; Konishi et al., 2007) and flexor

(Kramer, Nusca, Fowler, & Webster-Bogaert, 1993; Tengman et al., 2014) strength persist

long term and in some cases are found 25 years following surgery (Tengman et al., 2014).

2.12.2 Hamstring grafts

The most common ACLR surgical procedure in Australia is the quadrupled hamstring graft

(Bonasia & Amendola, 2012; Chechik et al., 2013). A surgeon performs this procedure using

an arthroscope and small incisions made where the semitendinosus and/or gracilis tendons are

36

located and harvested. Once harvested, the tendons are arranged into four strips and are

stitched together. The surgeon then prepares the knee and drills holes in the tibia and the

femur to place the graft. Several studies have shown that hamstring grafts, involving the

surgical removal of the distal ST tendon are associated with significant muscle atrophy and

retraction of the muscle belly (Burks et al., 2005; Konrath et al., 2016; Nomura et al., 2015).

Studies which report no muscle atrophy of the ST in the reconstructed limbs compared to the

contralateral uninjured limbs may be heavily influenced by different scanning parameters

used to assess the morphology of the muscle (Burks et al., 2005). It also seems possible some

scan sites have been too far distal to the ST muscle belly to detect muscle atrophy (Burks et

al., 2005). Nomura and colleagues (2014) showed that the length and volume of ST were 3.5

cm shorter and 26 % lower, respectively, in the ACLR limb compared to the uninjured

contralateral limb in a group of recreationally active athletes. These results are similar to

earlier studies (Choi et al., 2012; Simonian et al., 1996). It appears other knee flexor muscles

do not compensate for ST muscle atrophy and this may contribute to greater deficits in

hamstring strength following surgery (Nomura et al., 2015). Previously, Snow and colleagues

(2012) reported persistent atrophy of the ST and gracilis in the previously ACLR limb 9 to 11

years after ACLR from a ST graft in a group of sedentary people, and this was associated

with compensatory hypertrophy of the BFLongHead when compared to the contralateral

uninjured limb.

Some studies report hamstring strength is restored following ACLR and extensive

rehabilitation (Lipscomb, Johnston, Snyder, Warburton, & Gilbert, 1982; Simonian et al.,

1996) and others have shown deficits in hamstring strength remain after rehabilitation

(Hiemstra, Webber, MacDonald, & Kriellaars, 2007; Tadokoro et al., 2004). Arnason and

colleagues (2013) found medial hamstring activation patterns, when assessed using sEMG

37

during a knee-based exercise, are significantly altered 1 to 6 years after surgery. Previously,

one study used functional magnetic resonance imaging (fMRI) to assess knee flexor muscle

use during an isokinetic exercise and found no significant difference in muscle activation

patterns in the ST and gracilis muscles between previously ACLR and uninjured limbs

(Takeda et al., 2006).

2.12.3 Rehabilitation and return to sport

A recent meta-analysis of 69 studies which included 7556 patients, reported that 82 % of

athletes return to a lower level of sport, while only 55 % returned to competitive sport 3 years

following ACLR (Ardern, Taylor, Feller, & Webster, 2014). In an earlier review, Ardern and

colleagues (2011) reported that only 44 % of patients returned to competitive sport. More

recently, a 15-year prospective study in men’s professional football by Hagglund and

colleagues (2016) showed that 85 % of players returned to training and 65 % of players

returned to competitive play within three years following ACLR. Rehabilitation and return to

sport outcome measures are widely discussed in the literature (Bradley, Klimkiewicz, Rytel,

& Powell, 2002; Lyman et al., 2009) and a number of outcome measures are used in

rehabilitation programs to determine the time course for when athletes can return to sport

(Bauer, Feeley, Wawrzyniak, Pinkowsky, & Gallo, 2014; Myer, Paterno, Ford, Quatman, &

Hewett, 2006; Myklebust & Bahr, 2005; Webster et al., 2017). For many years, isokinetic

dynamometry has been considered the gold standard measure of the strength and dynamic

stability of the knee joint and is frequently used for the evaluation of the success of the

rehabilitation program (Cvjetkovic et al., 2015). This method provides an objective measure

of both concentric and eccentric knee flexor and extensor strength (Aagaard et al., 1998).

However, the optimal time or set of criteria for when athletes are allowed to return to sport

following ACLR remains uncertain (Ardern et al., 2014; Webster et al., 2017). Typically,

athletes require 9 to 12 months recovery before making a return to competitive sport (Ardern

38

et al., 2014; Ardern et al., 2011a). Recent work by Webster and colleagues (2017) reported

that only one-third of athletes had returned to their pre-injury competitive sport 12 months

after ACLR while another one-third had only returned to training.

Functional objective parameters are often used to determine an athlete’s readiness to return to

sport (Bauer et al., 2014). Almost all rehabilitation protocols after ACLRs involve distinct

goal-based phases where progression is determined by successful attainment of specific

outcome measures. For example, the primary goals in phase one (1-2 weeks) are typically to

reduce knee swelling and improve knee range of motion before the start of phase two where

basic strength and range of motion exercises are introduced. Two recent studies have shown

that the ACL reinjury risk can be significantly reduced if the return to sport criteria has been

met (Grindem, Snyder-Mackler, Moksnes, Engebretsen, & Risberg, 2016; Kyritsis, Bahr,

Landreau, Miladi, & Witvrouw, 2016). Kyritsis and colleagues (2016) demonstrated that

athletes who did not meet the discharge criteria before returning to professional sport were

four times more likely to sustain an ACL injury than those who met the return to sport

criteria. In addition, it appears that a low H:Q ratio is associated with an increased risk of

ACL injury (Kyritsis et al., 2016).

The psychological impact of ACLR, including the fear of re-injury has been an additional

area for recent investigation (Kvist, Ek, Sporrstedt, & Good, 2005). The traumatic nature of

an ACL injury is often followed by psychological effects such as negative emotions,

depression and reduced self-confidence (Kvist et al., 2005). Moreover, negative emotions

surrounding re-injury are a large obstacle for any athlete’s mind to block out during

rehabilitation and recovery from ACLR (Kvist et al., 2005; Webster et al., 2017). It has been

proposed that athletes adopt alternative movement patterns as a protective mechanism against

39

excessive joint forces for the previously ACLR limb and this may increase future lower limb

injury risk (Paterno et al., 2012, 2014). Neuromuscular inhibition of thigh muscles, caused by

the trauma to the previously ACLR limb, is highly likely to increase the risk of re-injury

(Saunders, McLean, Fox, & Otago, 2014). Furthermore, harvesting the ST tendon may

significantly increase the risk of future ACL re-injury (or graft failure) and HSI.

2.12.4 Long term consequences

The early onset of knee osteoarthritis commonly occurs after ACL injury irrespective of

whether surgical or non-surgical treatments are used (Chaudhari, Briant, Bevill, Koo, &

Andriacchi, 2008; Ferretti, Conteduca, De Carli, Fontana, & Mariani, 1991; Lohmander et al.,

2007; Lohmander et al., 2004). Currently, there are no effective means of preventing joint

degeneration (Chaudhari et al., 2008; Ferretti et al., 1991; Kvist, 2004). Osteoarthritis is a

degeneration process initiated by changes in mechanical and biological properties of the

cartilage within the knee joint over time (Chaudhari et al., 2008). It is associated with pain,

stiffness and functional impairment around the knee joint (Lohmander et al., 2004). The

cause of osteoarthritis remains unclear (Chaudhari et al., 2008), though it appears the

preservation of the menisci is the key factor in preventing detrimental knee articular changes

in previously ACL injured limbs (Ferretti et al., 1991). Normally, advanced osteoarthritis

requires knee replacement, and this can significantly hinder knee function and quality of life

(Ferretti et al., 1991; Lohmander et al., 2004).

2.13 ANTERIOR CRUCIATE LIGAMENT INJURY AND RISK OF FUTURE

INJURY

The severe consequences of ACL injury (Arnason et al., 2014) and high rate of re-injury

(Sugimoto et al., 2016) suggest that injury prevention and rehabilitation practices are

suboptimal. The literature has focused heavily on improving treatment methods ahead of

40

prevention practices (Alentorn-Geli et al., 2009b). Typically, ACL injury prevention training

programs are targeted toward altering the neuromuscular and biomechanical risk factors

associated with injury (Griffin et al., 2006), and almost all such studies have included one or

more of the following type of exercise: strength, plyometric, proprioceptive, balance and/or

trunk muscle training (Alentorn-Geli et al., 2009a; Engebretsen et al., 2008; Hewett et al.,

1999; Mandelbaum et al., 2005; Myer, Ford, Palumbo, & Hewett, 2005). However, the

problem with including multiple components is that there is uncertainty regarding the specific

ingredient(s) responsible for reducing ACL injury rates after compliance with the training

program. Of all components previously investigated, it appears plyometric training is the

most effective training stimulus for reducing ACL injury rates (Alentorn-Geli et al., 2009b;

Sugimoto et al., 2016; Sugimoto et al., 2015). The goal of training programs is to improve the

way athletes move during their respective sport, and often this involves an emphasis on

deceleration, jumping, landing and cutting movements (Alentorn-Geli et al., 2009b; Griffin et

al., 2000).

Most often, training programs aim to improve strength of the trunk, hip and knee muscles to

reduce future risk of ACL injury (Alentorn-Geli et al., 2009b; Griffin et al., 2000; Griffin et

al., 2006). However, little research exists to support the use of hip muscle strengthening

programs to alter the neuromuscular and biomechanical risk factors of ACL injury. Perhaps

unsurprisingly, strengthening the hip muscles and improving the ability to control excessive

anterior pelvic tilt for athletes has resulted in a greater control of the lower extremity during

foot plant upon landing (Chimera, Swanik, Swanik, & Straub, 2004).

Previously, it has been suggested that strong medial hamstrings may play an important role in

preventing external rotation of the knee which is arguably the primary cause of knee valgus

41

and subsequent ACL injury (Arnason et al., 2014; Zebis et al., 2013). Bourne and colleagues

(2017b) and others (Mendiguchia, Arcos, et al., 2013; Mendiguchia, Garrues, et al., 2013)

have shown that the Nordic hamstring exercise selectively recruits the ST over the other long

head hamstring muscles. Bourne and colleagues (2017a) have also recently shown that ST

growth alone accounts for ~53 % of total hamstring hypertrophy after 10 weeks of training

with the Nordic hamstring exercise. A stronger or a more activated semitendinosus may aid

in reducing excessive external knee rotation and knee valgus moments during movements and

reduce the risk of ACL injury (Olsen, Myklebust, Engebretsen, Holme, & Bahr, 2005;

Sugimoto et al., 2015; Sugimoto et al., 2012). This exercise may be advantageous in both

hamstring and ACL injury prevention and rehabilitation programs.

2.14 ASSESSING SPATIAL PATTERNS OF MUSCLE ACTIVATION VIA

FUNCTIONAL MAGNETIC RESONANCE IMAGING

Functional magnetic resonance imaging (fMRI) is a unique technique that allows for a high-

resolution spatial assessment of the size and functional characteristics of muscles. This

analytical method was formed to noninvasively assess patterns and quantify the magnitude of

skeletal muscle activation during exercise (Adams, Duvoisin, & Dudley, 1992; Ardern et al.,

2010; Ono, Higashihara, & Fukubayashi, 2010; Ono, Okuwaki, & Fukubayashi, 2010). The

fMRI technique is used to assess voluntary activation and exercise has been shown to

increase the proton transverse (spin-spin) T2 relaxation time of skeletal muscle in fMRI

images (Jayaraman et al., 2004) and this shift in T2 relaxation time has been shown to

increase proportionately with exercise intensity (Adams et al., 1992; Fleckenstein et al.,

1991). The exercise-induced increases in T2 relaxation time are proportional to sEMG

measures of muscle activation (Adams et al., 1992). fMRI also provides a high-resolution

42

assessment of muscle cross sectional area and volume. Recently, fMRI has been used to

assess spatial patterns of hamstring muscle activation (Bourne, Williams, et al., 2017) and

muscle morphology (Bourne, Duhig, et al., 2017) during different hamstring strengthening

exercises.

43

PROGRAM OF RESEARCH

The goals of this program of research were to:

1) Examine the muscle activation patterns of women, without a history of lower limb injury,

during two common hamstring exercises

2) Examine the impact of a prior ACLR on

a. The risk of subsequent HSI

b. Hamstring muscle size, eccentric strength and patterns of muscle use during a

common rehabilitation exercise

Previous studies suggest that different strength exercises target different hamstring muscles

(Bourne, Williams, et al., 2017; Mendiguchia, Alentorn-Geli, & Brughelli, 2011;

Mendiguchia, Garrues, et al., 2013; Ono, Higashihara, & Fukubayashi, 2011; Zebis et al.,

2013). However, there is a discrepancy between studies that have used sEMG to assess

hamstring muscle activation patterns. Therefore, it was of further interest to use fMRI to

assess the patterns of hamstring muscle activation as it is a better method than sEMG. No

previous study has used fMRI to assess the patterns of hamstring muscle activation during

two different hamstring exercises in women. An improved understanding of the patterns of

hamstring muscle use during different exercises may be important for improving lower limb

injury prevention programs, particularly in women, who are at a greater risk of ACL injury.

Previous work has shown that deficits in eccentric knee flexor strength during the

performance of the Nordic hamstring exercise are associated with a 4.3 to 4.4-fold increased

44

risk of future hamstring injury in elite Australian rules footballers (Opar et al., 2015a) and

professional soccer players (Timmins et al., 2016b), although no such relationship was noted

for Rugby players (Bourne et al., 2015). Meanwhile, athletes with a history of ACL injury or

HSI display similar eccentric knee flexor weakness and shorter BFLongHead fascicle lengths in

previously injured limbs compared to the uninjured contralateral limbs (Opar et al., 2015a;

Timmins et al., 2016b). These findings suggest that a prior ACL injury and HSI may both

significantly increase the risk of future HSI. It is therefore of importance to prospectively

explore the effects of a prior ACL injury requiring reconstruction on the risk of future HSI.

In more recent years, hamstring grafts have become the popular graft choice for ACLR

surgery because of their ease of harvest, greater tensile strength, reduced knee extensor

strength deficit and lower risk of developing anterior knee pain and osteoarthritis (Ardern et

al., 2010; Freedman, D'Amato, Nedeff, Kaz, & Bach, 2003; West & Harner, 2005). It is

unclear whether or how hamstring muscle activation patterns are altered after ACLR.

Therefore, it is of interest to further explore the patterns of hamstring muscle use during a

common rehabilitation exercise. Once we better understand risk factors for injury (ACL or

hamstring) we should be able to design better rehabilitation programs.

45

STUDY 1 – HAMSTRING

MUSCLE USE IN FEMALES

DURING HIP-EXTENSION AND

THE NORDIC HAMSTRING

EXERCISE

Messer, DJ., Bourne, MB., Williams, MD., Al Najjar, A., Shield, AJ. (2018). Hamstring

muscle use in females during hip-extension and the Nordic hamstring exercise. Journal of

Orthopaedic and Sport Physical Therapy, Accepted.

46

4.1 LINKING PARAGRAPH

There is a large body of evidence (Bourne, Williams, et al., 2017; Mendiguchia et al., 2011;

Mendiguchia, Garrues, et al., 2013; Ono et al., 2011; Zebis et al., 2013) to suggest that

different strength exercises target different hamstring muscles. However, there is a

discrepancy between studies that have used sEMG to assess patterns of hamstring muscle

activation. For example, Bourne and colleagues (2017b) have shown that the Nordic

hamstring exercise selectively activates the ST, while Zebis and colleagues (2013) reported

that the Nordic hamstring exercise and prone isokinetic leg curl exercise were performed with

similar levels of ST and BFLongHead muscle activation when assessed using sEMG. However,

sEMG has poor spatial resolution and is not able to discriminate between closely

approximated muscles, such as the long and short heads of biceps femoris or either of the

medial hamstrings. Furthermore, the study by Bourne and colleagues (2017b) employed male

athletes while that of Zebis and colleagues (2013) employed females. Therefore, it was of

further interest to use fMRI to assess the patterns of hamstring muscle activation in females

as this method has better spatial resolution than sEMG. No previous study has used fMRI to

assess the patterns of hamstring muscle activation during hamstring exercises in women.

Understanding the muscle activation patterns of different hamstring strengthening exercises

may allow rehabilitation programs to target specific muscle deficits. For example, BFLongHead

exhibits prolonged atrophy after this muscle suffers strain injury (Silder et al., 2008).

Furthermore, a better understanding of hamstring muscle activation patterns may also allow

the development of better injury prevention programs. For example, Zebis and colleagues

(2013) have proposed that the ST may play a particularly important role in preventing ACL

injury given that this muscle functions to prevent excessive anterior tibial translation and

knee valgus, which are both movements commonly associated with ACL injury (Buchanan et

al., 1996; Hewett, Stroupe, Nance, & Noyes, 1996; Zebis et al., 2013). Therefore,

47

understanding the patterns of hamstring muscle activation may be of particular value in

reducing ACL injury in women as they are significantly more likely to sustain such injuries.

48

4.2 ABSTRACT

BACKGROUND: Understanding hamstring muscle activation patterns in resistance training

exercises may have implications for the design of strength training and injury prevention

programs. Unfortunately, surface electromyography studies have reported conflicting results

with regard to hamstring muscle activation patterns in women. PURPOSE: To determine the

spatial patterns of hamstring muscle activity during the 45º hip-extension and Nordic

hamstring exercises, in females using functional magnetic resonance imaging. STUDY

DESIGN: Cross-sectional. METHODS: Six recreationally active females with no history of

lower limb injury underwent functional magnetic resonance imaging (fMRI) on both thighs

before and immediately after 5 sets of 6 bilateral eccentric contractions of the 45º hip-

extension or Nordic exercises. Using fMRI, the transverse (T2) relaxation times were

measured from pre- and post- exercise scans and the percentage increase in T2 was used as an

index of muscle activation. RESULTS: fMRI revealed a significantly higher biceps femoris

long head (BFLongHead) to semitendinosus ratio during the 45° hip-extension than the Nordic

exercise (p = 0.028). The T2 increase after 45° hip-extension was greater for BFLongHead (p <

0.001), semitendinosus and semimembranosus (p = 0.001) than that of biceps femoris short

head (BFShortHead). During the Nordic exercise, the T2 increase for semitendinosus was greater

than that of BFShortHead (p < 0.001) and BFLongHead (p = 0.001). CONCLUSION: While both

exercises involve high levels of semitendinosus activation in women, the Nordic exercise

preferentially recruits that muscle while the hip extension more evenly activates all of the

biarticular hamstrings. These findings may have implications for the design of hamstring and

ACL injury prevention programs.

49

4.3 INTRODUCTION

Understanding patterns of hamstring muscle activation in different exercises may have

implications for strength training and hamstring and knee injury prevention programs.

Hamstring muscle activation has been examined in a range of resistance training exercises via

surface electromyography (sEMG) (Bourne, Williams, et al., 2017; Ono, Okuwaki, et al.,

2010; Zebis et al., 2013) and via functional magnetic resonance imaging (fMRI) (Bourne,

Williams, et al., 2017; Mendiguchia, Garrues, et al., 2013; Ono, Okuwaki, et al., 2010). The

fMRI technique offers high levels of spatial resolution and potentially provides greater clarity

as to the relative contribution of individual muscles than sEMG which is prone to cross-talk

(Adams et al., 1992; Cagnie et al., 2011). As far as we are aware, however, fMRI has not

previously been employed to assess hamstring activation in females. Furthermore, there are

currently disparities between sEMG studies that have employed male (Bourne, Williams, et

al., 2017) and female (Zebis et al., 2013) participants. For example, Bourne and colleagues

(2017) recently utilised a combination of sEMG and fMRI techniques and reported that knee

movements such as the Nordic hamstring exercise (NHE) and leg curl selectively activated

(Bourne, Williams, et al., 2017) the semitendinosus (ST) and biceps femoris short head

(BFShortHead) muscles, while the hip-extension exercises more uniformly recruited the

biarticular hamstrings in men (Bourne, Williams, et al., 2017). In contrast, Zebis and

colleagues (2013) have reported preferential sEMG activation of the biceps femoris long head

(BFLongHead) in the NHE and various forms of leg curls in women. These discrepancies could

potentially be due to small differences in EMG electrode placement and can potentially be

resolved with fMRI measures of hamstring muscle activation in women.

fMRI is a non-invasive form of imaging that allows for quantification of muscle activation

during exercise (Mendiguchia, Arcos, et al., 2013). The technique is based on changes in the

50

T2 relaxation time of tissue water (Cagnie et al., 2011; Mendiguchia, Arcos, et al., 2013;

Schuermans et al., 2014) which can be inferred from signal intensity changes in fMR images.

The T2 relaxation times of muscles change in proportion to exercise intensity and mirror the

changes in sEMG while also overcoming the limitations in spatial resolution of sEMG

(Adams et al., 1992; Cagnie et al., 2011).

The purpose of this study was to determine the spatial patterns of hamstring muscle use in

females, during the 45º hip-extension and Nordic hamstring exercises. On the basis of

previous work in males (Bourne, Williams, et al., 2017), we hypothesized that that the 45º

hip-extension exercise would display a higher BFLongHead to semitendinosus activation ratio

than the Nordic hamstring exercise.

4.4 METHODS

Participants

Six recreationally active females (age, 22.5 ± 5.9 years, height, 170.5 ± 7.5 cm, weight, 59 ±

6.9 kg) participated in this study. Participants were free from injuries to the trunk, hips and

lower limbs at the time of testing and had no known history of cardiovascular, metabolic or

neurological disorders. Participants had no history of hamstring strain injury or ACL injury.

All completed a cardiovascular risk factor questionnaire (Appendix A) to ensure it was safe

for them to perform intense exercise and a standardised MRI screening questionnaire

(Appendix B) provided by the imaging facility to make certain that it was safe for them to

enter the magnetic field. Prior to testing, participants provided written informed consent to

participate in the study, which was approved by the Queensland University of Technology

Ethics Committee and the University of Queensland Medical Research Ethics Committee.

51

Study Design

A cross-sectional design was used to determine the spatial patterns of hamstring muscle use

during the 45º hip-extension and Nordic hamstring exercises. These exercises were chosen on

the basis of previous work, which reported that out of 10 common exercises, the 45º hip-

extension most selectively activated the BFLongHead, while the Nordic most selectively

recruited the semitendinosus (Bourne, Williams, et al., 2017). At least 7 days (± 1 day) before

experimental testing, all participants were familiarized with each exercise and had

anthropometric measures taken. Experimental testing involved two separate sessions

separated by at least 14 days (14 ± 4 days). Each session involved fMRI on both thighs before

and immediately after one of the aforementioned exercises. All testing sessions were

supervised by the same investigator to ensure consistency of procedures (DJM).

Exercise protocol

An illustration of the 45° hip-extension and Nordic exercises can be found in Figure 4-1.

Participants performed only the eccentric or lowering phase of each exercise. Participants

were instructed to perform each eccentric repetition at the slowest possible speed and were

loudly encouraged to provide maximum effort during each repetition. During the

familiarisation session, the Nordic hamstring exercise was performed, with body mass only,

on a device described previously which enabled forces at the ankle to be assessed (Opar,

Piatkowski, Williams, & Shield, 2013; Opar et al., 2015a, 2015b). The ankle braces and load

cells attached to the device allowed the forces generated by the knee flexors to be measured

through the long axis of the load cells. In an attempt to approximately equate the intensity of

the hip-extension and the Nordic hamstring exercises, participants performed three maximal

eccentric repetitions (falling at the slowest possible speed) and concentric repetitions (with

the assistance of an elastic band attached across the chest and held by the investigator above

52

and behind the participant) of the Nordic hamstring exercise and the forces measured at each

participant’s ankles formed an eccentric to concentric ratio. During the Nordic, participants

displayed forces that were ~20 % greater during eccentric repetitions than concentric

repetitions. Subsequently, participants were given an approximate 10-RM load (the heaviest

load that can be lifted 10 times), in the form of weight plates held on the chest for the hip-

extension exercise (median = 15 kg; range = 10-20 kg). They then performed the exercise

with the allocated load and the weight was gradually increased or reduced until a 10-RM load

was found. Using Holten’s equation, × 100% ÷ 80% , where X = the 10-RM load,

we were able to estimate the 1-RM hip-extension load required to match the supramaximal

intensity of the Nordic (120 % of the estimated hip-extension 1RM).

In each subsequent exercise session, participants performed 5 sets of 6 repetitions with 1-

minute rest intervals between sets. Participants were loudly encouraged by investigators to

foster maximal effort during these tests. During the rest period, participants rested in a seated

position (45° hip-extension) or lay prone (Nordic) to minimize activation of the knee flexors.

Immediately after the completion of exercise, participants were returned to the scanner for

post-exercise scans which commenced within 135.4 ± 20s (mean ± SD).

53

Figure 4-1. (A) 45° hip-extension exercise and; (B) Nordic hamstring exercise.

Functional muscle magnetic resonance imaging (fMRI)

All fMRI scans were performed using a 3-Tesla (Siemens TrioTim, Germany) imaging

system with a spinal coil. Participants lay supine in the magnet bore with knees fully

extended and hips in a neutral position with straps secured around both limbs to prevent

undesired movements. A 180 x 256mm body image matrix was positioned over the anterior

thighs and aligned with the centre of the 400 x 281.3mm field of view (FoV), which included

both limbs and spanned the distance between the femoral head and the tibial plateau.

Consecutive T2-weighted axial images were acquired of both limbs before and immediately

following exercise using a Car-Purcel-Meiboom-Gill (CPMG) spin-echo pulse sequence and

the following parameters: transverse relaxation time (TR) = 2540ms; echo time (TE) = 8, 16,

24, 32, 40, 48 and 56ms; number of excitations = 1; slice thickness = 10mm; interslice gap =

A

B

54

10mm). All participants had two CPMG spin-echo pulse sequences to capture the entire

length of the thigh muscles and the total acquisition time for each sequence was 6min 25s. A

localiser adjustment (20s) was applied prior to the first sequence of each scan (pre- and post-

exercise) to standardise the field of view and to align collected images between the pre- and

post- exercise scans (Bourne, Opar, & Shield, 2014). A post-processing (B1) filter was

applied in order to minimise any inhomogeneity in MR images caused by dielectric

resonances at 3T (Ono et al., 2011). Participants were seated for a minimum of 15 minutes

prior to pre-exercise scans, and were asked to avoid strength training of the lower limbs for

72 hours prior to data acquisition to ensure that the signal intensity profile of pre-exercise

T2-weighted images was not affected by anomalous fluid shifts (Ono et al., 2011).

Measurement of T2 relaxation times

The T2 relaxation times of each hamstring muscle (BFLongHead; BFShortHead; ST; and

semimembranosus, SM) were measured in T2-weighted images acquired before and after

exercise sessions to evaluate muscle activation during exercise. All images were transferred

to a Windows computer in the digital imaging and communications in medicine (DICOM)

file format. The T2 relaxation time for all hamstring muscles was measured in five axial

slices which corresponded to 30, 40, 50, 60 and 70 % of thigh length (defined as the distance

between the inferior margin of the ischial tuberosity (0 %) and the superior border of the

tibial plateau (100 %)) (Bourne et al., 2014; Ono et al., 2011). Image analysis software (Sante

Dicom Viewer and Editor, Cornell University) was used to measure the signal intensity of

each muscle in both limbs in pre- and post-exercise scans. The signal intensity was measured

in each slice using a 9-40 mm2 circular region of interest (ROI) (Mendiguchia, Arcos, et al.,

2013; Mendiguchia, Garrues, et al., 2013) which was placed in a homogenous area of

contractile tissue in the centre of each muscle belly (avoiding aponeurosis, fat, tendon, bone

55

and blood vessels). The signal intensity represented the mean value of all pixels within the

ROI and was measured across seven echo times (8, 16, 24, 32, 40, 48, and 56 ms). For each

ROI, T2 relaxation time was calculated using the signal intensity value at each TE which was

fitted to a mono-exponential decay model using a least squares algorithm:

[(SI = M ´ exp(echo time / T2)] (Ono et al., 2011)

where SI is the signal intensity at a specific echo time, and M represents the pre-exercise

fMRI signal intensity. To determine the extent to which each ROI was activated during

exercise, the mean percentage change in T2 was calculated as:

[(mean post-exercise T2 / mean pre-exercise T2) x 100].

The percentage change in T2 relaxation time for each hamstring muscle was evaluated using

the average value of all ROIs at all five thigh levels, which provided a measure of whole-

muscle activation. Previous studies have demonstrated excellent intertester reliability of T2

relaxation time measures with intra-class correlation coefficients ranging from 0.87 to 0.94

(Cagnie et al., 2011; Ono et al., 2011).

Statistical analysis

The pre- and post-exercise T2 values for each exercise session were reported as mean ± SD.

A repeated measures linear mixed model fitted with the restricted maximum likelihood

(REML) method was used to compare the spatial patterns of hamstring muscle activation

during the 45º hip-extension and Nordic exercises. For each exercise, the log transformed

percentage change in T2 relaxation time was compared between each hamstring muscle; for

this analysis, muscle was the fixed factor and both participant identity and participant identity

× muscle the random factors. When a significant main effect was detected for muscle or

exercise, post hoc t tests with Bonferroni corrections were used to identify the source and

reported as mean differences with 95 % CIs. The adjusted α was set at p < 0.003 for these

56

analyses. The 45° hip-extension and Nordic hamstring exercises differed in terms of

movement velocity and hamstring excursion, so it was not appropriate to compare the

magnitude of T2 shifts between exercises. To determine differences in the extent of lateral to

medial hamstring activity between exercises, a repeated measures linear mixed model fitted

with the REML method was used to compare the differences in the ratio of BFLongHead to

semitendinosus percentage change in T2 relaxation time. For this analysis, exercise was the

fixed factor and participant identity the random factor. When a main effect was found for

exercise, post hoc t tests were again used to identify the source and reported as mean

difference (95 % CI); α was set at p < 0.05 for this analysis and Cohen’s d was reported as a

measure of the effect size.

4.5 RESULTS

T2 relaxation time percentage change following the 45° hip-extension exercise

A significant effect for muscle was noted with regard to T2 changes after hip-extension

exercise (p < 0.001). Post hoc analyses revealed the exercise-induced T2 increases for

BFShortHead were significantly less than for semitendinosus (mean difference in the log

transformed %T2 changes = 0.94; 95 % CI = 0.5 to 1.3; p < 0.001; d = 0.8),

semimembranosus, (mean difference = 0.67; 95 % CI = 0.2 to 1.1; p = 0.001; d = 0.6) and

BFLongHead (mean difference = 0.73; 95 % CI = 0.3 to 1.1; p < 0.001; d = 0.8) (Figure 4-2A).

An example of pre- and post-exercise T2 images is shown in Figure 4-3A. No statistically

significant differences were observed between any other muscle pairs (p > 0.003). The

absolute T2 values before and after the 45° hip-extension exercise and average percentage T2

increase for each muscle are displayed in Table 4-1.

57

T2 relaxation time percentage change following the Nordic hamstring exercise

A significant effect for muscle was noted with regard to T2 changes after the Nordic

hamstring exercise (p < 0.001). Post hoc analyses demonstrated that the exercise-induced T2

increase for semitendinosus was significantly greater than for BFShortHead (mean difference =

0.84; 95 % CI = 0.4 to 1.2; p < 0.001; d = 0.7) and BFLongHead (mean difference = 0.59; 95 %

CI = 0.2 to 0.9; p = 0.001; d = 0.5) (Figure 4-2B). Figure 4-3B shows an example of pre- and

post-exercise T2 images for the Nordic hamstring exercise. No statistically significant

differences were observed between any other muscle pairs (p > 0.003). The absolute T2

values before and after the Nordic hamstring exercise and average percentage T2 increase for

each muscle are displayed in Table 4-1.

58

Figure 4-2. Percentage change in fMRI T2 relaxation times of each knee flexor muscle

following the (A) 45° hip-extension exercise (B) Nordic hamstring exercise. Values are

displayed as the mean percentage change compared to values at rest. (A) * Indicates

significantly different from BFSH (p < 0.001) ** Indicates significantly different from BFLH (p

< 0.001) and SM (p = 0.001). (B) *Indicates significantly different from BFSH (p < 0.001)

and BFLH (p = 0.001). Data are presented as mean values (± 95 % CI). BFLH, biceps femoris

long head; BFSH, biceps femoris short head; ST, semitendinosus; SM, semimembranosus.

**

*A

*

B

59

Table 4-1. The average T2 relaxation time values measured before (T2 Pre) and immediately after (T2 Post) the 45° hip-extension and Nordic

hamstring exercise and the average T2 increase (%) of each muscle (relative to the T2 relaxation time at rest).

45° Hip-extension Nordic hamstring exercise

T2 Pre (ms) T2 Post (ms) T2 Increase (%) T2 Pre (ms) T2 Post (ms) T2 Increase (%)

BFLH 43.21 (± 4.33) 54.99 (± 11.67) 25.45 (± 16.94) 42.09 (± 2.08) 53.81 (± 4.38) 25.39 (± 13.69)

BFSH 42.35 (± 1.25) 46.58 (± 4.55) 10.46 (± 6.91) 41.60 (± 2.02) 51.18 (± 4.90) 22.46 (± 15.82)

ST 42.21 (± 1.86) 63.14 (± 8.06) 37.13 (± 19.11) 41.50 (± 1.29) 68.41 (± 9.77) 57.99 (± 32.39)

SM 42.22 (± 2.76) 56.20 (± 2.88) 24.90 (± 13.00) 41.36 (± 1.88) 56.39 (± 7.83) 33.27 (± 19.24)

Data are presented as mean values (± SD).

BFLH, biceps femoris long head; BFSH, biceps femoris short head; ST, semitendinosus; SM, semimembranosus.

60

Figure 4-3. (A) 45° hip-extension exercise and; (B) Nordic hamstring exercise. Region of

interest selection in a T2-weighted image (1) before and; (2) after exercise. BFLH, biceps

femoris long head; BFSH, biceps femoris short head; ST, semitendinosus; SM,

semimembranosus.

3.3 Comparison of biceps femoris long head to semitendinosus ratio between exercises

A significant main effect was observed for exercise (p = 0.028) when comparing the

BFLongHead to semitendinosus ratio (Figure 4-4). A significantly lower ratio was found during

the Nordic exercise compared to the 45° hip-extension exercise (mean difference = -0.20; 95

% CI = -0.37 to -0.03; p = 0.028).

A1

BFLH SM

A2 B2

B1

BFLH

ST

SM

ST

61

Figure 4-4. The BFLH to ST ratio (BFLH/ST) percentage change in fMRI T2 relaxation times

following the 45° hip-extension and the Nordic hamstring exercise. Column bars depict the

average BFLH to ST ratio for exercise and dashed lines demonstrate the participants BFLH to

ST ratio response between exercises. *Indicates a significant difference between exercises (p

= 0.028). BFLH, biceps femoris long head; ST, semitendinosus; Nordic, Nordic hamstring

exercise.

4.6 DISCUSSION

This is the first study to have used fMRI to explore the impact of exercise selection on

hamstring muscle activation in females. The findings are consistent with a previous study of

males (Bourne, Williams, et al., 2017) in showing high levels of semitendinosus activation

during both the eccentric 45° hip-extension and Nordic exercises, although the Nordic

exercise preferentially targets the semitendinosus while the hip-extension more evenly

activates the three biarticular hamstrings. Given the high spatial resolution of the fMRI

technique, these findings provide some clarity regarding hamstring activation patterns in two

*

62

common hamstring exercises which has not been produced by sometimes conflicting sEMG

studies (Bourne, Williams, et al., 2017; Zebis et al., 2013). These findings may also have

implications for design of strength training and injury prevention programs aimed at reducing

hamstring strain and anterior cruciate ligament injuries.

Explosive lower body movements are frequently performed during competitive sport, and

these activities impart significant loads on the ACL (Johansson, Sjölander, & Sojka, 1990;

Zebis et al., 2013). Given that the hamstrings represent the primary form of muscular support

for this ligament (Hewett et al., 1999), strengthening of these muscles is increasingly

prioritised in ACL injury prevention programs (Hewett et al., 1996; Wilkerson et al., 2004). It

has previously been proposed that the semitendinosus may play a more significant role than

the other hamstrings in unloading the ACL (Zebis et al., 2009), given that this muscle

functions to prevent excessive anterior tibial translation and knee valgus, which are both

movements commonly associated with ACL injury (Buchanan et al., 1996; Hewett et al.,

1996; Zebis et al., 2013). Accordingly, exercises that selectively activate the semitendinosus,

like the Nordic hamstring exercise, may be important in ACL injury prevention protocols.

Prior BFLongHead strain injury is associated with persistent deficits in muscle activation

(Bourne et al., 2016; Opar, Williams, Timmins, Dear, & Shield, 2013), BFLongHead fascicle

lengths (Timmins et al., 2016b), and muscle volume (Silder et al., 2008). These deficits

appear to persist even after a successful return to sport (Fyfe et al., 2013), which suggest that

conventional rehabilitation programs are ineffective in restoring optimal structure and

function to this most commonly injured muscle. Given that the acute T2 patterns observed

after a single exercise bout (Bourne, Williams, et al., 2017) closely match the hypertrophic

63

adaptations experienced as a consequence of 10 weeks of training (Bourne, Duhig, et al.,

2017), the results of the current study suggest that the Nordic hamstring exercise is unlikely

to be the optimal stimulus for restoring BFLongHead volume in cases of atrophy. Instead, the

hip-extension exercise which elicited a higher BFLongHead to semitendinosus activation ratio

may be a useful alternative for redressing these deficits and this should be a focus of future

work.

The mechanism for the non-uniformity of muscle activation in different exercises is not fully

understood, however, morphological and architectural differences might be at least partly

responsible (Bourne, Williams, et al., 2017; Ono, Okuwaki, et al., 2010). For example, the

semitendinosus displays a larger moment arm at the knee than the hip (Thelen, Chumanov,

Hoerth, et al., 2005), and may therefore be preferentially activated during movements

involving knee flexion (Thelen, Chumanov, Hoerth, et al., 2005). In contrast, the BFLongHead

moment arm is greater at the hip than the knee (Thelen, Chumanov, Hoerth, et al., 2005).

Moreover, semitendinosus is long, thin and fusiform and possesses many sarcomeres in

series, which may be better suited to contractions at long muscle lengths (Ono et al., 2011).

Participants were healthy, recreationally active females so we cannot assume that similar

results would occur in highly trained female athletes or those with a history of hamstring or

knee pathology. Furthermore, the T2 response following exercise is influenced by a range of

factors, such as the metabolic capacity of the active tissue, which is likely to differ between

individuals (Adams et al., 1992; Cagnie et al., 2011). We attempted to minimise any

variability by recruiting only female participants with a similar age and training status.

Despite our attempts to approximately standardise the exercise intensity, the 45° hip

extension and Nordic hamstring exercises differed in terms of movement velocity and

64

hamstring excursion, so it was not appropriate to compare the absolute magnitudes of T2

shifts between exercises. However, our findings can offer insights into the relative metabolic

activity and reliance on different hamstring muscles during the eccentric contraction of both

exercises.

Females display different spatial patterns of hamstring muscle activation during hip- and

knee-based strength exercises. The semitendinosus muscle displays high levels of muscle

activation during both the eccentric 45° hip-extension and Nordic exercises. Hip-extension

exercise more evenly activates the biarticular hamstrings while the Nordic exercise

preferentially targets the semitendinosus. As a consequence, the 45° hip-extension exercise

displayed a BFLongHead to semitendinosus activation ratio that was approximately 20 percent

higher than the Nordic exercise. These findings may have implications for the design of

hamstring and ACL injury prevention programs.

65

STUDY 2 – A HISTORY OF

ANTERIOR CRUCIATE

LIGAMENT INJURY INCREASES

THE RISK OF HAMSTRING

STRAIN INJURY ACROSS

FOOTBALL CODES IN

AUSTRALIA

Messer, DJ., Williams, MD., Bourne, MN., Opar, DA., Timmins, RG., Duhig, SJ., Shield,

AJ. A history of anterior cruciate ligament injury increases the risk of hamstring strain injury

across football codes in Australia.

66


It has been reported that a history of a significant knee injury, involving the ACL, medial

collateral ligaments, the menisci or cartilage, is a risk factor for HSI, although the evidence

for this is limited (Verrall et al., 2001). The goal of this study was to examine whether a

history of ACLR was associated with an elevated risk of future hamstring strain injury. This

study involved a secondary analysis of data collected in three previous prospective hamstring

injury risk factor studies of male Australian rules football (Opar et al., 2015a), soccer

(Timmins et al., 2016b) and rugby (Bourne et al., 2015) players. By combining the results of

each study, sufficient statistical power was obtained to examine relationships between prior

ACLR and future HSI. Therefore, it was of interest to observe eccentric knee flexor strength

during the Nordic hamstring exercise after ACL injury and subsequent ACLR.

67

5.2 ABSTRACT

BACKGROUND: The burden of anterior cruciate ligament (ACL) and hamstring strain

injuries (HSI) is considerable across football codes in Australia. Once injured, the likelihood

of reoccurrence of the same type of injury is high. While it has been proposed that a previous

ACL injury increases the risk of future HSI, there is currently no evidence for this.

PURPOSE: To determine the impact of a prior ACL injury, HSI or both on 1) the risk of

future HSI; and 2) eccentric knee flexor strength and between-limb imbalance during the

Nordic hamstring exercise. STUDY DESIGN: Prospective study, secondary analysis.

METHODS: In total, 538 elite to sub-elite male athletes (age, 23.5 ± 4.5 years; height, 184.8

± 7.8 cm; mass, 87.6 ± 12.4 kg) had their eccentric knee flexor strength assessed during the

Nordic hamstring exercise during preseason training. Injury history and demographic data

were also collected. The main outcome measure was the prospective occurrence of HSIs.

RESULTS: Eighty-three athletes suffered at least one HSI during the subsequent competitive

season. Athletes with a history of ACL injury had a 3.2-fold (95 % CI = 1.9 to 5.2; p < 0.001)

greater risk of subsequent HSI than athletes without such history. Athletes with a prior ACL

injury and a history of HSI in the previous 12 months had 5.7-fold (95 % CI = 3.2 to 9.5; p <

0.001) increased risk of HSI. The previously injured limbs from athletes with a history of

ACL injury and hamstring strain were significantly weaker (mean difference = -106 N; 95 %

CI = -165 to -46 N; p < 0.001) and displayed larger between-limb imbalances (mean

difference = 28 %; 95 % CI = 14 to 41 %; p < 0.001) than those without such history.

CONCLUSION: Athletes with a prior ACL injury are at an increased risk of future HSI, and

this risk is augmented if coupled with a previous HSI. Athletes with a history of ACL injury

and HSI display lower levels of eccentric knee flexor strength and larger between-limb

imbalances.

68

5.3 INTRODUCTION

ACL injuries and HSIs account for a significant amount of lost playing time in a range of

football codes (Ekstrand et al., 2011a; Opar et al., 2015a; Orchard & Seward, 2002). They

have high recurrence rates (Arnason et al., 2004; Ekstrand et al., 2011b) and a history of each

injury is a very strong predictor of the same type of injury in the future (Hagglund et al.,

2006). It has also been suggested that a history of a significant knee injury is a risk factor for

HSI (Verrall et al., 2001), although the evidence for a link between past ACLR and future

hamstring injury is limited.

In Australia, ACL injuries cost professional sporting organisations an estimated AUD$17 000

- 25 000 per athlete for surgery and rehabilitation (Orchard, Seward, McGivern, & Hood,

1999; Orchard et al., 2001), and these injuries are associated with development of early onset

osteoarthritis and anterior knee pain later in life (Lohmander et al., 2007). Similarly, HSIs

cost sport organisations millions of dollars (Verrall et al., 2006; Woods et al., 2002). For

example, in the Australian football league they cost each club an average of AUD$1.5 million

per season in wages paid to side-lined players (Orchard et al., 2013). In elite sport, ACL

reconstructions are almost always considered essential for restoring adequate knee joint

stability (Ardern et al., 2011a; Liow, McNicholas, Keating, & Nutton, 2003), and they

usually involve one of two autogenous grafts harvested from either the ipsilateral ST and

gracilis or the patellar tendon (Ardern et al., 2010; Paterno et al., 2010; Pinczewski et al.,

2007). Both techniques have significant long-term effects on knee muscle strength (Konrath

et al., 2016; Makihara, Nishino, Fukubayashi, & Kanamori, 2006), proprioception (Katayama

et al., 2004) and coordination (Yosmaoglu, Baltaci, Kaya, Ozer, & Atay, 2011) which may

increase the prospects of injury recurrence and contribute to an elevated risk of HSI.

69

Given the reduced risk of developing anterior knee pain after hamstring grafts (Ejerhed et al.,

2003), the vast majority of ACLRs in elite Australian sport involve the ST tendon (Aglietti et

al., 1994; Ejerhed et al., 2003). Most studies report deficits in quadriceps and hamstring

strength after ACLR, and in many cases, these deficits persist well after the cessation of

rehabilitation (Pinczewski et al., 2007; Yasuda, Tsujino, Ohkoshi, Tanabe, & Kaneda, 1995).

A number of observational studies (Konrath et al., 2016; Nomura et al., 2015; Takeda et al.,

2006) have reported decrements in concentric (Tengman et al., 2014) and eccentric (Tengman

et al., 2014; Thomas et al., 2013) knee flexor strength in the years following surgery as well

as reduced muscle size (Nomura et al., 2015) and altered muscle architecture of the ST

(Timmins et al., 2015). However, these studies are almost always constrained by small

sample sizes, and several investigations have found conflicting results regarding the recovery

of strength after rehabilitation (Aglietti et al., 1994; Ejerhed et al., 2003).

Late-preseason deficits in eccentric knee flexor strength during the Nordic hamstring exercise

are associated with a 4.3 to 4.4-fold increased risk of future hamstring injury in elite

Australian rules footballers (Opar et al., 2015a) and professional soccer players (Timmins et

al., 2016b), although no such relationship was noted for Rugby players (Bourne et al., 2015).

Moreover, athletes with a history of ACL injury or HSI have been found to display similar

eccentric knee flexor weakness and shorter BFLongHead fascicle lengths in the previously

injured limb compared to the uninjured contralateral limb (Opar, Piatkowski, et al., 2013;

Timmins et al., 2016a). These findings suggest that a prior ACL injury and HSI may both

significantly increase the risk of future HSI.

The purposes of this study were to determine the impact of a prior ACL injury, HSI or both

on 1) the risk of future HSI; and 2) eccentric knee flexor strength and between-limb

70

imbalance as measured during the Nordic hamstring exercise. We hypothesised that athletes

with prior ACL injury and/or HSI would be at an increased risk of future HSI when compared

to those with no such injury history.

5.4 METHODS

Participants and study design

This study involved a secondary analysis of data collected in three previously published

prospective studies (Bourne et al., 2015; Opar et al., 2015a; Timmins et al., 2016b). Ethics

approval for these studies was granted by the Queensland University of Technology Human

Research Ethics Committee and Australian Catholic University Human Research Ethics

Committee and were completed between 2013 and 2015. A total of 538 male athletes,

including, 229 elite Australian Football League (AFL) players, 131 elite A-League Soccer

players and 178 elite and sub-elite Rugby Union players had their eccentric knee flexor

strength assessed at the beginning of their sport’s preseason (see Figure 5-2). All three studies

required team medical staff to complete a previous injury questionnaire that included, for all

athletes; a history of hamstring, quadriceps, and calf strain injuries and chronic groin pain

within the previous 12 months and a history of ACL injury at any stage in the athlete’s career.

These injury reports were confirmed with information from each club’s internal medical

recording system. The type of ACLR was not recorded for the entire AFL cohort or some of

the Rugby players. Our study deals with the effects of ACLR on subsequent hamstring injury

rather than the effects of any specific reconstruction technique.

Experimental design

Eccentric knee flexor strength

The assessment of eccentric knee flexor strength using the Nordic hamstring testing device

71

(Figure 5-1) has been reported previously (Bourne et al., 2016; Opar, Piatkowski, et al., 2013;

Opar et al., 2015a; Timmins et al., 2016b). Athletes knelt over a padded board, with ankles

secured immediately superior to the lateral malleolus by individual ankle braces, which were

attached to custom made uniaxial load cells (Delphi Force Measurement, Gold Coast,

Australia) with wireless data acquisition capabilities (Mantracourt, Devon, UK). The ankle

braces and load cells were secured to a pivot, which allowed the force generated by the knee

flexors to be measured through the long axis of the load cells. Following a warm up set,

athletes performed one set of three maximal repetitions of the bilateral Nordic hamstring

exercise. Athletes were instructed to lean forward at the slowest possible speed while

maximally resisting this movement with both limbs and keeping the trunk and hips in a

neutral position throughout, with the hands held in line with the chest. Athletes were loudly

encouraged to provide maximum effort during each repetition. A repetition was considered

acceptable when the force output reached a distinct peak (indicative of maximal eccentric

strength), followed by a rapid decline in force, which occurred when the athlete was no

longer able to resist the effects of gravity acting on the segment above the knee joint.

72

Figure 5-1. The Nordic hamstring exercise performed on the testing device (progressing

from right to left). Athletes were instructed to lower themselves to the ground as slowly as

possible by performing a forceful eccentric contraction of their knee flexors. Athletes only

performed the eccentric portion of the exercise and, after ‘‘catching their fall,’’ were

instructed to use their arms to push back into the starting position (not shown here). (Image

from Bourne et al., 2015).

Data analysis

Force data for each limb were transferred to a personal computer at 100 Hz through a

wireless USB base station receiver (Mantracourt, Devon, UK). Eccentric knee flexor

strength, determined for each leg from the peak force during the best of 3 repetitions of the

Nordic hamstring exercise, was reported in absolute terms (N). For athletes with no history of

lower limb injury, a between-limb imbalance in peak eccentric knee flexor force was

calculated as a right:left limb ratio and, for athletes with a prior ACL injury or HSI as an

uninjured:injured limb ratio. The between-limb imbalance ratio was converted to a

percentage difference as per previous work (Bourne et al., 2015; Opar et al., 2015a) using

log-transformed raw data, followed by back transformation. Negative percentage imbalances

specify that the left limb was stronger than the right limb in athletes with no history of lower

limb injury or that the previously injured limb was stronger than the uninjured limb in

73

athletes with a prior ACL injury or HSI. Participants were categorised into groups based on

their injury histories (see Figure 5-2) and were excluded if they had insufficient injury history

or strength testing data.

Statistical analyses

All statistical analyses were performed using JMP 10.2.0 Statistical Discovery Software

(SAS Inc., Cary, North Carolina, USA). Where appropriate, data were screened for normal

distribution using the Shapiro-Wilk test and homoscedasticity using Levene’s test. Means and

standard deviations (SDs) of age, height, body mass, eccentric knee flexor strength for the

left and right limbs, and between limb imbalance (%) in strength were determined. To

calculate univariate relative risk (RR) and 95 % CIs of future HSI, athletes were grouped

according to whether they had a history of ACL injury, HSI or both and were compared to

those without a history of injury with RR significance assessed using a two-tailed Fisher’s

exact test. To assess the risk of future HSI a multivariate logistic regression model was

formed using the following factors; prior HSI, prior ACL injury, eccentric knee flexor

strength, between limb imbalance and body mass. All post-hoc comparisons were made using

independent-samples t tests with Bonferroni corrections to control for type 1 errors and

reported as the mean difference (95 % CIs): α was set at p < 0.05. The eccentric knee flexor

strength of the injured limb in athletes with a history of ACL injury and/or HSI were

compared with the uninjured contralateral limb and the average of the left and right limbs in

athletes with no history of ACL injury or HSI. Analyses of covariance (ANCOVA) were

performed to assess the effect of prior ACL injury, HSI or both on i) eccentric knee flexor

strength using body mass as the covariate, and ii) between limb imbalance using the

uninjured limb peak force as the covariate. Pearson’s correlation (R2) was used to assess the

74

magnitude of eccentric knee flexor strength deficits with time since ACL injury and was

reported with the 95 % CIs.

5.5 RESULTS

Details of Cohort and Prospective HSIs

In total, 538 athletes (age, 23.5 ± 4.5 years; height, 184.8 ± 7.8 cm; mass, 87.6 ± 12.4 kg) had

sufficient injury history and strength data and were included in this investigation (Figure 5-2).

Athletes with a life-time history of ACL injury were 55 ± 35 months post injury. Eighty-three

athletes suffered at least one HSI during the subsequent competitive season (age, 24.8 ± 4.4

years; height, 184.0 ± 7.4 cm; mass, 85.6 ± 11.1 kg), and 455 athletes did not (age 23.2 ± 4.5

years; height 185.0 ± 7.8 cm; mass 88.0 ± 12.6 kg). Subsequently injured athletes were

significantly older than uninjured athletes (mean difference = 1.6 ± 4.5 years; 95 % CI = 0.9

to 2.2; p = 0.003; d = 0.36). No significant differences were observed for height (mean

difference = 0.9 ± 7.6 cm; 95 % CI = -0.2 to 2.1; p = 0.28; d = 0.12) or mass (mean difference

= 2.3 ± 11.8 kg; 95 % CI = -0.5 to 4.1; p = 0.09; d = 0.19) between the subsequently injured

and uninjured athletes. Of these 83 athletes to suffer prospective hamstring injuries 34 were

AFL, 21 were rugby and 28 were soccer players.

75

Figure 5-2. Participant recruitment and inclusion in the study. 1) No prior ACL injury at any

stage and no HSI within the previous 12 months, 2) At least one HSI in the previous 12

months, 3) At least one ACL injury requiring reconstructive surgery at any stage in the

athlete’s life.

Risk of future hamstring strain injury

Relative risk

The impact of prior HSI, ACL injury or both on the relative risk of future HSI is reported in

Table 5-1.

Table 5-1. Relative risk of future hamstring strain injury (HSI)

Group n % from each group that

sustained a subsequent

HSI

Relative risk (95

% CI)

Significance

No Previous Injury1 400 10

Prior HSI2 80 25 2.4 (1.5 to 3.9) p < 0.001

Prior ACL Injury3 46 33 3.2 (1.9 to 5.2) p < 0.001

Prior ACL Injury3 and

HSI2

12 58 5.7 (3.2 to 9.5) p < 0.001

CI, confidence interval; HSI, hamstring strain injury; ACL, anterior cruciate ligament. 1) No prior ACL injury at

any stage and no HSI within the previous 12 months, 2) At least one HSI in the previous 12 months, 3) At least

one ACL injury requiring reconstructive surgery at any stage in the athlete’s life.

3 cohorts (n=538)

AFL (n=229) Soccer (n=131) Rugby (n=178)

Previous HSI2 (n=80)

Prior ACL injury3 and Previous HSI2 (n=12)

Prior ACL injury3 (n=46)

No previous injury1 (n=400)

Subsequent HSI (n=41)




76

Multivariate logistic regression

The multivariate logistic regression revealed that a history of ACL injury or HSI in the

previous 12 months were significant risk factors for future HSI (Table 5-2). Athletes with a

lifetime history of ACL injury exhibit an odds ratio of 4.5 (95 % CI = 2.3 to 8.8) while HSI in

the previous 12 months displayed an odds ratio of 2.6 (95 % CI = 1.4 to 4.6). Body mass and

the peak eccentric strength of the previously injured limb (ACL or HSI) had no significant

effect on risk of future HSI once previous injury was controlled for.

Table 5-2. Regression analysis of future risk of hamstring strain injury (HSI)

Eccentric Knee Flexor Strength and Between-limb Imbalance

Body mass had a significant effect on eccentric knee flexor strength (r2 = 0.11; p < 0.001),

where heavier athletes were stronger than lighter athletes. The eccentric knee flexor strength

of the uninjured contralateral limb had a significant effect on between-limb imbalance (r2 =

0.22; p < 0.001) where stronger athletes displayed smaller between-limb imbalances. The

eccentric knee flexor strength and between-limb imbalance for each group can be seen in

Figure 5-3. Eccentric knee flexor strength of the injured limb was used for athletes with a

history ACL injury and/or HSI, and the two-limb average was used for athletes with no

previous injury. Athletes with a lifetime history of ACL injury and HSI in the previous 12

months were significantly weaker (mean difference = -106 N; 95 % CI = -165 to -46 N; p <

0.001) and displayed larger between-limb imbalances (mean difference = 28 %; 95 % CI = 14

Risk factor Odds ratio 95 % CI Significance

Prior ACL Injury 4.5 2.3 to 8.8 p < 0.001

Prior HSI 2.6 1.4 to 4.6 p = 0.002

Body Mass 0.9 0.9 to 1.0 p = 0.076

Previously Injured Limb (ACL or HSI) 1.0 0.9 to 1.0 p = 0.358

CI, confidence interval; HSI, hamstring strain injury; ACL, anterior cruciate ligament

77

to 41 %; p < 0.001) than those without such history. Athletes with a lifetime history of ACL

injury and no HSI in the previous 12 months were not weaker than those without a history of

injury (mean difference = -21 N; 95 % CI = -53 to 11 N; p = 0.392), and the between limb

imbalances of these two groups did not differ significantly (mean difference = 4 %; 95 % CI

= -3 to 11 %; p = 0.435).

Athletes who had at least one HSI in the previous 12 months were not weaker than those with

no history of injury in that time-frame (mean difference = 18 N; 95 % CI = -6 to 43 N; p =

0.198), however the between limb imbalances of these two groups did differ (mean difference

= -8 N; 95 % CI = -13 to -2 N; p = 0.004). There was no correlation (r2 < 0.01; 95 % CI = -

0.02 to 0.02) between time since ACL injury and the magnitude of eccentric knee flexor

strength deficits.

78

Figure 5-3. Eccentric knee flexor strength (N) (bars) and between-limb imbalance (%) (line)

as measured by the Nordic hamstring device for each group. Eccentric knee flexor strength of

the injured limb was used for athletes with a history of ACL injury and HSI and the average

of the left and right limbs were used for athletes with no previous injury. Force is reported in

absolute terms (N) with error bars depicting the 95 % CI. # Indicates significantly different to

all groups (p < 0.001) in between limb imbalance. * Indicates significantly different to all

groups (p < 0.026) in eccentric knee flexor strength.

5.6 DISCUSSION

The aims of this study were to determine the effect of a prior ACL injury, HSI or both on 1)

the risk of future HSI; and 2) eccentric knee flexor strength and between-limb imbalance as

measured during the Nordic hamstring exercise. Our data show, for the first time, that a prior

#

*

79

ACL injury requiring reconstruction significantly increases the risk of subsequent HSI.

Interestingly, a lifetime history of ACL injury and subsequent reconstruction appears to have

an even larger impact on the likelihood of future HSI than did a recent history (12 months) of

HSI.

The factors that explain high hamstring injury rates after ACL injury are uncertain.

Proprioceptive and strength deficits (Kramer et al., 1993; Tengman et al., 2014; Timmins et

al., 2016a) seem to be reasonable hypotheses, but the current results suggest that poor

eccentric strength is an unlikely explanation for high hamstring injury rates in athletes with

prior ACLR. Opar and colleagues (2015a) and Timmins and colleagues (2016b) have shown

that weakness in the Nordic hamstring exercise was associated with an elevated risk of HSI in

elite Australian Rules Football and Soccer cohorts, respectively. Deficits in knee flexor

strength after ACLR have been noted previously (Kramer et al., 1993; Tengman et al., 2014;

Timmins et al., 2016a), although the current study showed no significant differences in knee

flexor strength between athletes with and without a prior history of ACLR, unless ACLR was

coupled with a recent history (12 months) of HSI. These findings suggest that there are

factors other than strength (e.g., muscle activation and size) which contribute to the elevated

risk of HSI.

A between limb imbalance in eccentric knee flexor strength has been reported to be

associated with future HSI (Bourne et al., 2015). For example, Bourne and colleagues (2015)

have previously reported that elite and sub-elite rugby union players are 2.4 and 3.4-fold

more likely to sustain a hamstring injury if they have 15 % and 20 % between-limb

imbalance in eccentric knee flexor strength respectively (Bourne et al., 2015). In this study,

however, athletes with a history of ACLR did not have significantly greater between-limb

80

imbalances than those with no history of injury. Another potential explanation for the

increases in hamstring injury risk is BFLongHead fascicle lengths. Timmins and colleagues

(2016a) have shown that athletes with previous ACLRs from hamstring grafts exhibit ~15 %

deficits in BFLongHead fascicle lengths in their previously injured limbs. More recently, the

same group have shown, in the soccer cohort that formed a part of this study, that shortened

BFLongHead fascicles are associated with a heightened risk of a hamstring strain in elite

Australian soccer players (Timmins et al., 2016b). Unfortunately, fascicle lengths were not

determined for the two other cohorts employed in this analysis.

Schuermans and colleagues (2014) have shown that athletes with a relatively high reliance on

BFLongHead and low use of ST, as determined by transverse (T2) relaxation time changes

observed via functional MRI in a fatiguing knee flexor exercise, appear to be at greater risk

of HSI (Schuermans et al., 2016). Hamstring tendon grafts have become the common surgical

choice for ACLR in Australian football players and have been found to be associated with

chronic deficits to the ST muscle volume (Burks et al., 2005; Nishino, Sanada, Kanehisa, &

Fukubayashi, 2006; Nomura et al., 2015), muscle length (Burks et al., 2005; Nishino et al.,

2006; Nomura et al., 2015), and patterns of muscle use (Tadokoro et al., 2004) making it

likely that following surgery athletes rely to a relatively greater extent on the BFLongHead

during running. Unfortunately, we do not have all the details of surgical graft type for the

ACLR recipients in this study, so it is not possible to report what proportion of athletes had

undergone ST and/or gracilis grafts, as opposed to patellar tendon grafts. In the soccer cohort,

however, 13 of 16 ACLR’s involved ST and, in our experience, this procedure is the standard

in a significant majority (>80 %) of AFL and rugby clubs in Australia. It seems reasonable to

suggest, therefore, that semitendinosus grafts had been performed on a vast majority of the

ACLR recipients in this study.

81

Typically, knee flexor muscle strength is well monitored during rehabilitation. However,

selective medial hamstring weakness, assessed via internal rotation of the flexed knee, has

been found up to 2 years after ACLR surgery (Armour et al., 2004). Furthermore, Arnason

and colleagues (2014) reported significant reductions in medial knee flexor muscle activation

in limbs with a prior ACLR during Nordic and leg curl exercise when assessed using sEMG.

The current study, however, explored eccentric knee flexor strength during the Nordic

hamstring exercise and we do not know whether medial knee flexor activation deficits were

observed in athletes with a history of ACLR. The observations of limited strength deficits

after ACLR are consistent with some (Lipscomb et al., 1982; Simonian et al., 1996; Tashiro,

Kurosawa, Kawakami, Hikita, & Fukui, 2003) but not all previous findings (Coombs &

Cochrane, 2001; Timmins et al., 2016a). However, the discrepant findings may be explained

by the contraction mode of the knee flexor strength tests, the time since injury and surgical

procedure and the nature of the rehabilitation programs employed. Bourne and colleagues

(2016; 2017) have previously shown that the Nordic hamstring exercise preferentially recruits

the ST muscle, which suggests the possibility that this exercise may be more sensitive than

other tests (i.e., isokinetic dynamometry) for assessing the function of this muscle.

Nevertheless, the current findings are that eccentric knee flexor strength is not significantly

reduced after ACLR, perhaps because the average time since surgery for players in this study

was ~4.5 years. However, given that the semitendinosus offers significant muscular support

for the ACL, it is likely that reduced function of these muscles would increase the loads

experienced by the ACL during running, landing and cutting movements.

In the current study, athletes with a life-time history of ACL injury and recent history (12

months) of HSI were weaker and had larger between-limb imbalance than those without a

history of injury. It is plausible that neuromuscular inhibition of the knee flexor muscles may

82

occur after ACLR and it has been observed after HSI (Opar, Williams, et al., 2013). Previous

work using fMRI has also shown that previously injured knee flexor muscles are significantly

less active than uninjured contralateral muscles during performance of the Nordic hamstring

exercise (Bourne et al., 2016). However, future work is needed to determine the

mechanism(s) for future HSI in athletes with a history of ACL injury and subsequent

reconstruction.

It is important to acknowledge some limitations associated with the current study. The major

limitation is the lack of information regarding the graft types for some of the athletes. This

could not be overcome because the original studies were prospective risk factor investigations

of hamstring injury and did not collect this information for all participants. Furthermore, de-

identification of athlete data prevented us from finding out retrospectively. Further

information regarding graft type may have allowed a comparison of the effects of

semitendinosus and patellar grafts on subsequent hamstring injury risk. Another limitation of

the study is related to strength measurements during the Nordic hamstring exercise. Results

of this strength test are influenced to some degree by athlete body mass (Buchheit, Cholley,

Nagel, & Poulos, 2016) and height, so any differences between injured and uninjured athletes

in these parameters would potentially have impacted on the strength comparisons that were

made. To minimise the effect of body mass, it was used as a covariate in the analysis of

covariance. Furthermore, body mass and height did not differ significantly between players

who did and did not sustain hamstring strain injury during the period of observation, so any

negative impacts were minimised.

Our results demonstrate that athletes with a prior ACL injury and HSI display the lowest

levels of eccentric knee flexor strength and largest between-limb imbalances compared to

83

athletes with no such injury. Furthermore, a history of ACL injury was the strongest predictor

of future HSI followed by a HSI in the previous 12 months. Athletes are 2.4, 3.2 and 5.7-fold

more likely to sustain a hamstring injury if they have had a HSI in the previous 12 months,

prior ACL injury or both, respectively. Future work is needed to determine why a history of

ACLR predisposes for future HSI in athletes and how this risk is best minimised.

84

STUDY 3 – HAMSTRING

MUSCLE ACTIVATION,

MORPHOLOGY AND STRENGTH

DURING ECCENTRIC EXERCISE

1 TO 6 YEARS AFTER ANTERIOR

CRUCIATE LIGAMENT

RECONSTRUCTION WITH

SEMITENDINOSUS GRAFT

Messer, DJ., Bourne, MN., Williams, MD., Timmins, RG., Shield, AJ. (2018). Hamstring

muscle activation, morphology and strength during eccentric exercise 1 to 6 years after

anterior cruciate ligament reconstruction with semitendinosus graft. Journal of Knee Surgery,

Sports Traumatology, Arthroscopy, Under Review.

85


Study 2 demonstrated that male footballers with a prior ACL injury have an increased risk of

future HSI and this is augmented if coupled with a previous HSI. Those with a life time

history of ACL injury and recent history (12 months) of HSI display lower levels of eccentric

knee flexor strength, larger between-limb imbalances and an increased risk of future HSI than

those without such history. Given the vast majority of ACLR surgeries in Australia involve a

hamstring graft from the ST tendon the long-term impact of surgery on the structure and

function of this and other hamstring muscles is unclear. Previously, Timmins and colleagues

(2016a & 2016b) reported that athletes with a prior history of ACL injury or HSI displayed

similar eccentric knee flexor weakness and shorter BFLongHead fascicle lengths in previously

injured limbs compared to the uninjured contralateral limbs. This suggests, given that short

fascicles and weak hamstrings are potential risk factors for a future hamstring injury, that

there should be a greater focus on regaining eccentric knee flexor strength during

rehabilitation after ACLR. The results from Chapter 2 showed no significant difference in

eccentric hamstring strength between athletes with and without a prior history of ACLR.

However, there is some disagreement in the literature on this matter (Nakajima, Maruyama,

Shitoto, Yamauchi, & Nakajima, 1996; Nomura et al., 2015; Timmins et al., 2016a). It is

possible that factors other than strength (e.g., muscle activation) may contribute to the

elevated risk of HSI. Therefore, it was of interest to further investigate hamstring muscle

function (e.g., strength and activation) and morphology (e.g., size) after ACLR and

subsequent rehabilitation.

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6.2 ABSTRACT

BACKGROUND: Harvest of the semitendinosus (ST) tendon for anterior cruciate ligament

reconstruction (ACLR) causes persistent atrophy of this muscle even after a return to sport,

although it is unclear if hamstring activation patterns are altered during eccentric exercise.

PURPOSE: To explore the pattern of hamstring muscle activation during intense eccentric

exercise in individuals with a previous unilateral ACLR involving ST autograft. Secondary

goals were to examine hamstring muscle volumes and anatomical cross-sectional areas

(ACSAs), ST muscle length and eccentric knee flexor strength. STUDY DESIGN: Case

series. METHODS: Fourteen recreationally active participants who had successfully

returned to sport from unilateral ACLR using ST tendon graft (median = 49 months, range =

12-78 months) were recruited. Participants underwent functional magnetic resonance imaging

(fMRI) of their thighs before and after 50 repetitions of the Nordic hamstring exercise

(NHE). Transverse (T2) relaxation times were measured at rest and immediately after

exercise and percentage T2 change was used as an index of hamstring activation. Muscle

volumes were determined from MR images and distal ST tendons were evaluated via

ultrasound. Eccentric knee flexor strength was determined during the NHE. RESULTS:

Exercise-induced T2 change was lower for ST muscles in surgical than control limbs (95 %

CI = -3.8 to -16.0 %; p = 0.004). Both ST muscle volume (95 % CI = -57.1 to -104.7 cm3; p <

0.001) and ACSA (95 % CI = -1.9 to -5.0 cm2; p < 0.001) were markedly lower in surgical

limbs. Semimembranosus (95 % CI = 5.5 to 14.0 cm3; p < 0.001) and biceps femoris short

head (95 % CI = 0.6 to 11.0 cm3; p = 0.032) volumes were slightly higher in surgical limbs.

No between-limb difference in eccentric knee flexor strength was observed (-21 N, 95 % CI =

33 to -74 N, p = 0.550). CONCLUSION: ST activation is significantly reduced during

eccentric knee flexor exercise 1 to 6 years after ACLR with ST graft. Diminished ST

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activation may partially explain this muscle’s persistent atrophy post ACLR and have

implications for the design of more effective rehabilitation programs.

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6.3 INTRODUCTION

Anterior cruciate ligament (ACL) ruptures are debilitating injuries that can lead to chronic

deficits in medial hamstring volumes (Konrath et al., 2016; Nomura et al., 2015; Snow et al.,

2012), knee flexor (Konrath et al., 2016; Nomura et al., 2015; Snow et al., 2012) and internal

rotator strength (Konrath et al., 2016), knee stability (Abourezk et al., 2017), altered gait

(Abourezk et al., 2017; Tashman et al., 2004) and early onset knee osteoarthritis (Beynnon et

al., 2005). ACL reconstruction (ACLR) surgery is widely considered necessary to restore

knee stability for sports participation (Arnason et al., 2014) and it often involves autografts

from the semitendinosus (ST), with or without the gracilis. However, despite the fact that ST

tendons have been reported to eventually regenerate and make attachments to the tibia or

other knee flexor muscle sheaths in a majority of cases (Konrath et al., 2016; Nomura et al.,

2015; Takeda et al., 2006), surgery typically results in long lasting ST muscle atrophy along

with the aforementioned strength deficits.

Persistent deficits in hamstring muscle size and strength following ACLR with ST graft may

be at least partly explained by chronic neuromuscular inhibition of the donor muscle. For

example, medial hamstring surface electromyographic (sEMG) activity is diminished in

limbs with previous ACLR during eccentric knee flexor exercise (Arnason et al., 2014) and

hopping (Briem, Ragnarsdottir, Arnason, & Sveinsson, 2016). However, limitations in spatial

resolution of sEMG means that it is not possible to determine whether only the ST muscle

activity has changed. Functional magnetic resonance imaging (fMRI) offers a high resolution

means of assessing spatial patterns of muscle use during exercise (Cagnie et al., 2011), and,

as far as we are aware, has only once been employed to examine the hamstrings after ACLR

involving ST grafts (Takeda et al., 2006). Takeda and colleagues (2006) assessed hamstring

muscle use after concentric exercise for the knee flexors 7-32 months after surgery and

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reported almost identical ST muscle activation between surgical and control limbs. However,

neuromuscular inhibition of the hamstrings may be larger in supramaximal eccentric than

concentric contractions (Opar, Williams, et al., 2013) and fMRI has never been applied to

eccentric exercise after ST grafts.

The primary purpose of this investigation was to explore the pattern of hamstring muscle

activation during intense eccentric exercise in individuals with a previous unilateral ACLR

involving ST autograft. Secondary goals were to examine hamstring muscle volumes and

anatomical cross-sectional areas (ACSAs), ST muscle length and eccentric knee flexor

strength. We hypothesised that in comparison with contralateral uninjured limbs, limbs with a

previous ACLR would display i) deficits in ST activation (according to T2 changes assessed

via fMRI) during the eccentric Nordic hamstring exercise (NHE); ii) smaller ST muscle

volumes, ACSAs and lengths; and iii) lower eccentric knee flexor strength.

6.4 METHODS

Participants

Fourteen recreationally active participants (5 men, mean age, 27.2 ± 4.0 years; mean height,

181.4 ± 3.2 cm; mean body mass, 80.4 ± 6.1 kg; and 9 women, mean age, 25.0 ± 5.3 years;

mean height, 168.9 ± 5.3 cm; mean body mass, 65.3 ± 12.5 kg), with a history of unilateral

ACLR were recruited for this study. The median time of participants post-surgery was 49

months (range = 12-78 months) at the time of testing. All had undergone rehabilitation under

the supervision of a qualified physiotherapist and had returned to their pre-injury levels of

training and competition. Inclusion criteria were: (i) aged between 18 and 35 years, (ii)

history of unilateral ACLR autograft from the ipsilateral semitendinosus, and (iii) ≥12

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months post ACLR surgery. Exclusion criteria were (i) any contraindications to MRI, (ii)

complex knee injuries with additional ligament surgery or meniscal injury, and (iii) any

history of hamstring injury to the operated or non-operated contralateral limb. Prior to testing,

all participants completed a cardiovascular screening questionnaire (Appendix A) to ensure it

was safe for them to exercise, and a standardised MRI questionnaire (Appendix C) to make

certain it was safe for them to enter the magnetic field. All participants provided written

informed consent to participate in this study, which was approved by the Queensland

University of Technology Human Research Ethics Committee 1600000882.

Familiarisation

Participants performed a familiarisation session of the NHE at least 5 days (range = 5-12

days) before experimental testing. Upon arrival at the laboratory, participants were provided

with a demonstration of the NHE (Figure 6-1). Subsequently, participants performed several

practice repetitions (typically two sets of five repetitions) whilst receiving verbal feedback

from investigators. All testing sessions were supervised by the same investigator (DJM) to

ensure consistency of procedures.

Experimental procedures

Upon arriving at the imaging facility, participants were seated at rest for at least 15 minutes

before data collection. Panoramic ultrasound images were then acquired for the hamstrings

on both limbs. Finally, participants underwent an fMRI scan of their thighs before and

immediately after performing the NHE.

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Exercise protocol and eccentric strength testing

Participants performed the NHE on the Nordbord (Vald Performance, Brisbane, Australia)

(Figure 6-1) and were instructed to lower themselves to the ground as slowly as possible

while maintaining their trunk and hips in a neutral position, with their hands held in line with

their chest. Participants only performed the lowering (eccentric) phase of the exercise and

were instructed to use their arms and to flex their knees and hips to return to the start position

so as to minimise concentric knee flexor activity. Participants completed five sets of 10

repetitions of the NHE with one-minute rests between sets. During the rest periods,

participants lay prone to minimise activation of the knee flexors. Investigators provided

strong verbal support throughout the exercise session to encourage maximal effort. All

participants completed the 50 repetitions and were returned to the scanner immediately

following the cessation of exercise (< 1 min); post-exercise scans began within 189.7 ± 24s

(mean ± SD).

The NordBord measures forces at the ankles via load cells (sampling at 50Hz) that are

attached to ankle hooks placed immediately superior to the lateral malleoli. Eccentric strength

was determined for each limb from the peak force (N) produced during the first set (10

repetitions) of the exercise session.

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Figure 6-1. The Nordic hamstring exercise, progressing from right to left.

Ultrasound Imaging

The distal ST tendons and adjacent muscle fascicles of both limbs were imaged via grey-scale

ultrasound (US) images taken with an iU22 Philips scanner (Philips Healthcare, Eindhoven,

Netherlands) equipped with a high resolution L12MHz linear transducer. All scanning was

performed by a single sonographer with >20 years of musculoskeletal experience.

Participants lay in the prone position to allow the posterior thigh to be examined in the

longitudinal and transverse planes. A standardised, pre-programmed general musculoskeletal

setting was selected for the grey-scale US scanning protocol, with the inclusion of optimised

scanning parameters, such as; depth, frequency, focal zone and Colour Doppler setting.

Distal ST muscles and their tendons were compared for the absence or presence of grey scale

abnormality (normal/abnormal). The sonographer made notes based on the following criteria;

1) integrity of distal semitendinosus tendon and appearance of adjacent muscle fascicles

compared to those from semimembranosus and biceps femoris long head (normal, partial loss

of fibrillary pattern or echogenic complete loss of fibrillary pattern), 2) absence or presence

of the surgical tendon scar (absent, thinned, normal reconstituted or hypertrophic), 3)

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observation of maturity of tendon scar (echogenic, mixed, hypoechoic or fluid), 4) colour

doppler imaging indicative of vascularity of the post-surgical harvest site graded using the

semi-quantitative method (none 0%, scant 1-24%, mild 25-49%, moderate 50-74% or severe

75-100%). All images and worksheets were recorded and stored with the picture archiving

and communication system (PACs).

MRI

All MRI scans were performed using a 3-Tesla imaging system (Phillips Ingenia, ©

Koninklijke Phillips N.V). Participants were positioned supine in the magnet bore with their

knees fully extended, hips in neutral and straps secured around both limbs to prevent

undesired movement. Scans of both lower limbs began at the level of the femoral head and

finished immediately distal to the tibial plateau. Participants were positioned in the centre of

the magnet bore with a 32-channel spinal coil placed over the anterior thighs. Prior to

exercise, participants underwent two MRI scanning sequences to generate T2-weighted and

mDixon axial images. T2-weighted imaging was repeated immediately after exercise. T2-

weighted images were acquired using a Car-Purcel-Meiboom-Gill spin echo pulse sequence

(Table 6-1). A localiser adjustment (20s) was applied before the first sequence of each scan to

standardise the field of view and align collected images consistently in the pre- and post-

exercise scans (Bourne et al., 2016). A post-processing (B1) filter was also applied to

minimise any inhomogeneity in MR images caused by dielectric resonances at 3T (Ono et al.,

2011). To ensure the signal intensity profile of T2-weighted images was not disturbed by

abnormal fluid shifts, participants were instructed to avoid strength training of the lower

limbs for 72 hours prior to data acquisition and were seated for 15 min (Ono, Higashihara, et

al., 2010) before pre-exercise imaging. Axial mDixon images were taken using a T1-

weighted 3-dimensional (3D) fast field echo (FFE) sequence (Table 1). The images were

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acquired in 4 stations (water only, fat only, in-phase and out-of-phase) with 180 slices per

station. The FFE sequence provided smooth 3-D images allowing for excellent visibility of

the muscles’ outer margins for manual segmentation.

Table 6-1. T2-weighted and mDixon slice positioning and image acquisition parameters

Scan position and acquisition parameters T2-weighted mDixon

Slice thickness (mm) 10 3.6

Interslice gap (mm) 10 0

Field of view (mm) 220 x 360 350 x 450

Relaxation time (ms) 2500 3.2

Echo time (ms) 8, 16, 24, 32, 40, 48 1.1, 2.1

Number of echoes 6 2

Field of view (mm) 220 x 360 350 x 450

Voxel size (mm) 0.9 x 0.9 x 10 1.8 x 1.8 x 3.6

Total acquisition time for each scan (sec)

348 28

Muscle activation

To determine the extent of hamstring muscle activation during the NHE, T2 relaxation times

were measured in consecutive multi-echo T2-weighted images acquired before and after

exercise. All images were transferred to a Windows computer in the digital imaging and

communications in medicine (DICOM) file format. For all hamstring muscles, the T2

relaxation time was measured in five axial slices that corresponded to 30, 40, 50, 60 and 70 %

of thigh length (defined as the distance between the inferior margin of the ischial tuberosity

(0 %) and the superior border of the tibial plateau (100 %)) (Bourne et al., 2014; Ono et al.,

2011). In the pre- and post- exercise scans, the signal intensity of each hamstring muscle in

both limbs was measured using image analysis software (Sante Dicom Viewer and Editor,

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Cornell University). The signal intensity was measured in each slice using a 0.5-10 cm2

circular region of interest (ROI) (Mendiguchia, Arcos, et al., 2013), which was placed in a

homogenous area of contractile tissue in the centre of each muscle belly (avoiding

aponeurosis, fat, tendon, bone and blood vessels). The size of each ROI varied due to the

cross-sectional area and amount of homogeneous muscle tissue identifiable in each slice of

interest. The signal intensity represented the mean value of all pixels within the ROI and was

measured across six echo times (8, 16, 24, 32, 40 and 48 ms). To calculate the T2 relaxation

time for each ROI, the signal intensity value at each echo time was fitted to a mono-

exponential decay model using a least squares algorithm:

[(SI = M ´ exp(echo time / T2)] (Ono et al., 2011)

where SI is the signal intensity at a specific echo time, and M represents the pre-exercise

fMRI signal intensity. Next, to determine the extent to which each ROI was activated during

exercise, the mean percentage change in T2 was calculated as:

[(mean post-exercise T2 / mean pre-exercise T2) x 100].

For each hamstring muscle, the percentage change in T2 relaxation time was evaluated using

the average value of all ROIs at all five thigh levels, which provided a measure of whole-

muscle activation. Previous studies have shown excellent intertester reliability of T2

relaxation time measures with intra-class correlation coefficients ranging from 0.87 to 0.94

(Cagnie et al., 2011; Ono et al., 2011).

Muscle volume, anatomical cross-sectional area and muscle length

Muscle volume, anatomical cross-sectional area (ACSA) and muscle length for each of the

hamstrings (biceps femoris long head (BFLH), biceps femoris short head (BFSH), ST and

semimembranosus (SM)) were determined for both limbs from mDixon images using manual

segmentation. Muscle boundaries were identified and traced on each image where the desired

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structure was present using image analysis software (Sante DICOM Viewer and Editor,

Cornell University) (Figure 6-2). Volumes were determined for each muscle by multiplying

the summed cross-sectional areas (CSAs) (from all slices containing the muscle of interest)

by the slice thickness (Silder et al., 2008). Maximum ACSA was determined by finding the

3.6 mm slice with the greatest CSA and averaging this along with the two slices immediately

cranial and caudal (5 slices). To determine muscle length, the total number of slices for each

muscle of interest were summed and then multiplied by the slice thickness to represent the

total length of each respective muscle belly. All traces were performed by the same

investigator (DJM) who was blinded to participant identity throughout all analyses.

Statistical analysis

Data were analysed using JMP Version 10.02 (SAS Institute, 2012). Hamstring muscle

volume, ACSA, length and pre- and post-exercise T2 values were reported as means ± SDs.

Clinical interpretation of ultrasound images was reported descriptively. A repeated measures

linear mixed model fitted with the restricted maximum likelihood (REML) method was used

to compare transient exercise-induced percentage changes in T2 relaxation times and resting

values of muscle volume, maximum ACSA and muscle length for each hamstring muscle.

For this analysis, muscle (BFLH, BFSH, ST, SM), limb (injured/uninjured) and muscle by limb

interaction were the fixed factors with participant identity (ID), participant ID by muscle and

participant ID by limb as the random factors. For this analysis, muscle (BFLH, BFSH, ST, SM),

limb (surgical/control) and muscle by limb interaction were the fixed factors with participant

identity (ID), participant ID by muscle and participant ID by limb as the random factors.

When a significant main effect was detected post hoc Student’s t tests with Bonferroni

corrections were used to determine which comparisons differed. Student’s t tests were used

for between-limb comparisons of muscle volumes and ACSAs for the total lateral (BFLH +

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BFSH) and medial (ST + SM) hamstrings, the whole hamstrings and eccentric knee flexor

strength. Comparisons were reported as mean differences with 95 % CIs and α was set at p <

0.05. For all analyses, Cohen’s d was reported as a measure for the effect size, with the levels

of effect being deemed small (d = 0.20), medium (d = 0.50) or large (d = 0.80) as

recommended by Cohen (1988).

Figure 6-2. (A) Region of interest selection in a T2-weighted image and (B) T1-weighted

mDixon water only image. BFLH, biceps femoris long head; BFSH, biceps femoris short head;

ST, semitendinosus; SM, semimembranosus.

BFLH

BFLHST ST

SM SM

BFSH

BFSH

A

BFSH

BFSH

BFLH

BF

LHST STSM SM

B

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6.5 RESULTS

Power calculations

As this is the first study to explore hamstring muscle activation during eccentric exercise in

individuals following ACLR, it was not possible to base sample size estimates on previously

reported effect sizes. However, previous studies exploring differences in strength and ST

muscle volume have reported effect sizes of 1.0 to 1.97 when comparing surgical to non-

surgical limbs (Konrath et al., 2016). Therefore, we conservatively based our sample size

estimates on anticipated effect sizes of 0.7 and a sample size of 14 was deemed sufficient to

provide a statistical power of ≥ 0.8.

Between limb comparisons

T2 relaxation time changes following eccentric exercise

A muscle by limb interaction was found (p < 0.001) for the percentage change in T2

relaxation time following the NHE. The average exercise-induced T2 change in ST muscles

was 34 % lower in previously surgical (19.3 ± 7.9 %) than in control limbs (29.2 ± 8.4 %)

(mean difference = -9.9 %; 95 % CI = -3.8 to -16.0 %; p = 0.004; d = 0.93). No significant

differences in T2 changes were observed between the surgical and control limbs for SM

(mean difference = -2.2 %; 95 % CI = -10.0 to 6.1 %; p >0.999; d = 0.33), BFLH (mean

difference = -0.9 %; 95 % CI = -5.8 to 4.1 %; p = 0.712; d = 0.24) or BFSH (mean difference

= 0.6 %; 95 % CI = -2.4 to 3.5 %; p = 0.683; d = 0.10) (Figure 6-3).

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Figure 6-3. Percentage change in fMRI T2 relaxation times of each hamstring muscle

following the Nordic hamstring exercise. Values are displayed as the mean percentage

change compared to values at rest. * Indicates significant difference between limbs (p =

0.004). Data are presented as mean values (± SD). BFLH, biceps femoris long head; BFSH,

biceps femoris short head; ST, semitendinosus; SM, semimembranosus.

Hamstring muscle volumes

A muscle by limb interaction was detected for muscle volume (p < 0.001). ST volume was 45

% lower in surgical (98.4 ± 54.3 cm3) than control limbs (179.4 ± 51.6 cm3) (mean difference

= -80.9 cm3; 95 % CI = -57.1 to -104.7 cm3; p < 0.001; d = 1.52). SM volume was 5 % larger

in surgical than control limbs (mean difference = 9.7 cm3; 95% CI = 5.5 to 14.0 cm3; p <

0.001; d = 0.20). BFSH volume was 7 % larger in the surgical than control limbs (mean

difference = 5.9 cm3; 95 % CI = 0.6 to 11.0 cm3; p = 0.032; d = 0.25) and BFLH volume was 4

% larger in the surgical than control limbs (mean difference = 7.5 cm3; 95 % CI = -1.4 to 16.0

cm3; p = 0.092; d = 0.17) although this was not statistically significant (Figure 6-4A).

*

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Medial hamstring muscle volume was 18 % lower in surgical (307.1 ± 91.8 cm3) than control

limbs (378.4 ± 89.6 cm3) (mean difference = -71.3 cm3; 95 % CI = -48.9 to -93.6 cm3; p <

0.001; d = 0.78) (Figure 6-4A). Lateral hamstring volume did not differ significantly between

surgical (260.1 ± 62.1 cm3) and control limbs (247.1 ± 62.3 cm3) (mean difference = 13.4

cm3; 95 % CI = -8.9 to 35.7cm3; p = 0.232; d = 0.21). Total hamstring muscle volume was 9

% lower in surgical (567.5 ± 147.6 cm3) than control limbs (625.3 ± 148.4 cm3) (mean

difference = -57.9 cm3; 95% CI = -38.0 to -77.6 cm3; p < 0.001; d = 0.39).

Hamstring muscle ACSA

A main effect was detected for muscle ACSA between limbs (p < 0.001). ACSA of the ST

was 28 % lower in surgical (8.9 ± 4.0 cm2) than control limbs (12.4 ± 3.7 cm2) (mean

difference = -3.5 cm2; 95 % CI = -1.9 to -5.0 cm2; p < 0.001; d = 0.89), while ACSA of BFSH

was 9 % larger in the surgical (8.4 ± 2.5 cm2) than control limbs (7.7 ± 2.5 cm2) (mean

difference = 0.7 cm2; 95 % CI = 0.2 to 1.2 cm2; p = 0.008; d = 0.28) (Figure 6-4B). No

significant between-limb differences were observed for SM (mean difference = 0.4 cm2; 95 %

CI = -8.2 to 9.1 cm2; p = 0.920; d = 0.15) or BFLH ACSA (mean difference = 0.3 cm2; 95 %

CI = -46.8 to 47.3 cm2; p > 0.999; d = 0.07).

The combined ACSA for the medial hamstrings was 11% lower for the surgical (24.5 ±

6.1cm2) than the control (27.5 ± 6.3cm2) limbs (mean difference = -3.1cm2; 95% CI = -

1.2cm2 to -4.9cm2; p = 0.001; d = 0.49) (Figure 6-4B). The combined ACSA for the lateral

hamstrings was 5 % greater in surgical (23.6 ± 5.8 cm2) than control limbs (22.6 ± 6.1 cm2),

although this difference was not statistically significant (mean difference = 1.0 cm2; 95 % CI

= -0.8 to 2.8 cm2; p = 0.269; d = 0.17). The combined total of all hamstring muscle ACSAs

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was not significantly different in surgical (48.1 ± 11.3 cm2) and control limbs (50.1 ± 11.8

cm2) (mean difference = -2.1 cm2; 95 % CI = -5.4 to 1.2 cm2; p = 0.194; d = 0.17).

Hamstring muscle length

A main effect was detected for muscle length between limbs (p < 0.001). ST muscles were 23

% shorter in surgical (23.4 ± 5.0 cm) than control limbs (30.5 ± 1.8 cm) (mean difference = -

7.2 cm; 95 % CI = -4.8 to -9.5 cm; p < 0.001; d = 1.99) (Figure 6-4C). No between-limb

length differences were observed for the remaining homonymous hamstring muscle pairs (all

p values > 0.05; all d values < 0.10).

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B

**

C

*# *

*

*

*

*#

*

*

A

*#

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Figure 6-4. (A) Mean volumes, (B) ACSAs and (C) lengths of hamstring muscles in injured

and uninjured contralateral limbs. Values were measured at rest. Data are presented as

mean values (± SD). For between limb muscle comparisons, * indicates (p < 0.001), **

indicates (p = 0.001) and *# signifies (p < 0.04). BFLH, biceps femoris long head; BFSH,

biceps femoris short head; ST, semitendinosus; SM, semimembranosus. ST, semitendinosus;

Hams, hamstrings; Medial Hams, medial hamstrings; Lateral Hams, lateral hamstrings; Inj,

injured limb; Uninj, uninjured contralateral limb.

Comparison of tendon and muscle structure of semitendinosus between limbs

Of the 14 surgical ST tendons, seven showed partial and four showed a complete loss of

fibrillary pattern while three appeared normal under ultrasound. All ST tendons from control

limbs appeared normal (Figure 6-5A). Distal ST muscle fascicles were abnormal only in the

surgical limbs. Ultrasound of the tendon harvest site showed variable degrees of scarring,

(Figure 6-5B) while ten surgical tendons exhibited no vascularity in the region of the scar,

three displayed ‘scant’ and one displayed ‘mild’ vascularity.

A

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Figure 6-5. Example ultrasound images of the semitendinosus (A) distal tendon in the

sagittal view and (B) distal muscle belly in the transverse view, in the injured and uninjured

contralateral limbs.

Eccentric knee flexor strength

Eccentric knee flexor strength, as determined from the highest forces generated in the first set

of the NHE, did not differ significantly between surgical (289 ± 87 N) and control limbs (310

± 71 N) (mean difference = -21 N, 95 % CI = 33 to -74 N, p = 0.550, d = 0.26) (Figure 6-6).

Three participant’s strength tests were not recorded due to equipment failure during testing.

C D

B

INJURED A

B INJURED UNINJURED

UNINJURED

B

A

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Figure 6-6. Peak eccentric knee flexor force measured at the ankles during the Nordic

hamstring exercise. Bars depict the average peak knee flexor force, while the jitter dots

represent each participant’s response. Strength is reported in absolute terms (N).

6.6 DISCUSSION

To our knowledge, this is the first fMRI study to explore hamstring muscle activation during

eccentric exercise in recipients of ACLR involving ST grafts. One to six years after surgical

intervention, the graft donor ST is activated significantly less than the homonymous muscle

in the control limb during the NHE, an exercise known to place particularly high demands on

this muscle (Bourne, Williams, et al., 2017). Significant deficits in ST muscle size and length

and ultrasound evidence consistent with chronic ST tendon deloading were also apparent in

the surgical limbs. BFSH volume and ACSA and SM volume were slightly higher in surgical

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than control limbs and there were only minor deficits in total hamstrings volume (9%) while

the total hamstrings ACSA was not significantly different. These modest differences in total

muscle size may explain the statistically insignificant between-limb difference eccentric knee

flexor strength, despite large deficits in ST ACSA (~28%).

One previous study used fMRI to evaluate hamstring activation after ACLR (Takeda et al.,

2006) and it showed no difference in exercise-induced T2 changes in the ST muscles of

surgical and contralateral limbs after concentric isokinetic knee flexion exercise. It is possible

that the greater demands imposed by the supramaximal eccentric exercise in this study were

able to reveal muscle activation deficits while concentric exercise as employed by Takeda

and colleagues (2006) could not. It should also be noted that Takeda and colleagues (2006)

only measured the T2 changes in a single fMR image that was 1cm distal to the middle of

each hamstring muscle. By comparison, the T2 changes in the current study were measured in

five slices between 30 and 70 % of the distance down the thigh.

Deficits in ST volume and maximum ACSA after ACLR involving ST grafts have previously

been reported (Konrath et al., 2016; Nomura et al., 2015; Snow et al., 2012). In contrast to

our study, Konrath and colleagues (2016) reported that BFLH muscles were and BFSH muscles

were not larger in surgical than control limbs. We observed that BFSH muscles in the surgical

limbs were larger than those in the control limbs, while there was no significant between-

limb difference in BFLH size. It is possible that the larger BF muscles in surgical limbs have

experienced compensatory hypertrophy after ST tendon grafts, although this is obviously

impossible to prove in retrospective studies like these. Differences in relative hamstring

muscle volumes between studies (Konrath et al., 2016; Nomura et al., 2015; Snow et al.,

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2012) may reflect variable rehabilitation strategies or subsequent training of the participants

in each study. Alternatively, the diversity of relative hamstring volumes may simply reflect

differences that pre-dated surgery. Like Konrath and colleagues (2016), we observed that SM

volume but not ACSA was larger in surgical than control limbs and that the summed volumes

and ACSAs of the medial hamstrings were significantly in deficit in surgical limbs. These

observations have implications for internal knee rotation strength, which has been reported to

be in deficit long after ACLR with ST grafts (Konrath et al., 2016).

The persistent deficit in medial hamstring muscle mass after ACLR with ST graft is a

concern given the role of these muscles in countering external tibial rotation torques and knee

valgus moments (Buchanan et al., 1996), both of which are thought to be risk factors for ACL

injury and re-injury (Alentorn-Geli et al., 2009a; Paterno et al., 2010). Given the devastating

effects of ST tendon grafts, it may be beneficial to develop rehabilitation strategies that target

the SM, the only other internal rotator of the knee that also acts as a hip extensor. Bourne and

colleagues (2017) reported that 10 weeks of hip extension strength training resulted in

significant SM hypertrophy while training with the NHE (in which overload is largely limited

to the knee) did not. So hip-extension exercises may be particularly effective in compensating

for the medial hamstrings size deficits that we and others have reported (Konrath et al.,

2016). In uninjured athletes, the ST muscle has been shown to hypertrophy significantly in

response to both hip extensor and knee flexor strength training (specifically, the NHE), with a

trend towards greater responses after the knee-oriented exercise (Bourne, Duhig, et al., 2017).

However, it is doubtful that similar benefits occur after ST grafts, because the persistent

deficits in ST muscle size shown here and by others (Konrath et al., 2016; Nomura et al.,

2015) are evident 1 to 6 years after surgery despite the completion of standard rehabilitation

programs and successful return to sport. The present findings of relatively low levels of post-

108

surgical ST activation in the demanding NHE also suggest that this muscle receives a limited

stimulus for adaptation, even during a supramaximal exercise which is known to

preferentially target this muscle (Bourne, Duhig, et al., 2017; Bourne, Williams, et al., 2017).

It should also be considered that ST tendon regeneration after ACLR may take approximately

18 months (Papandrea, Vulpiani, Ferretti, & Conteduca, 2000) and may not occur at all in 10

to 50 % of patients (Konrath et al., 2016; Nomura et al., 2015; Snow et al., 2012).

Rehabilitation during this time and for individuals with no tendon regeneration would

presumably not load the ST significantly. Future studies may examine the effectiveness of

hip-extension exercises in promoting SM hypertrophy, improving knee internal rotation

strength and altering dynamic lower limb function during running gait after ACLR with ST

grafts.

Contrary to our hypothesis, there were no significant differences in eccentric knee flexor

strength between surgical and control limbs, although there was considerable between-subject

variability. The literature regarding knee flexor strength after ACLR is mixed, with most

studies reporting persistent deficits (Nakajima et al., 1996; Nomura et al., 2015; Timmins et

al., 2016a) and others showing none.(Simonian et al., 1996) The study by Timmins and

colleagues (2016a) is the most similar to ours because it also assessed eccentric forces during

the NHE. By contrast, they observed a ~14 % strength deficit in surgical limbs, with an effect

size approximately twice as big as the one reported here (d = 0.51 v 0.26).

One limitation of the present study is its lack of a measure of internal knee rotation strength.

It should also be acknowledged that skeletal muscle’s T2 response to exercise is influenced

by a range of factors, including the metabolic capacity of the active tissue (Cagnie et al.,

109

2011; Patten, Meyer, & Fleckenstein, 2003). It is feasible that some differences in the T2

changes between injured and uninjured limbs may relate more to changes in metabolic

characteristics of tenotomised muscles, than to changes in muscle activation. However, it can

be argued that such metabolic changes are secondary to reduced muscle activation. Finally,

while there was no control group (without a history of ACLR) in this study, the activation

patterns of the uninjured control limbs are very similar to those that have been observed in

healthy uninjured limbs (Bourne et al., 2016; Bourne, Williams, et al., 2017; Messer, Bourne,

Williams, & Shield, 2017).

In conclusion, this is the first fMRI study to show ST activation is significantly reduced

during eccentric exercise 1 to 6 years after ACLR with ST graft. Diminished ST activation

may partially explain this muscle’s persistent atrophy and have implications for the design of

more effective rehabilitation programs.

110

GENERAL DISCUSSION &

CONCLUSION

Both ACL and hamstring injuries are major problems in sport and despite some progress in

the development of injury prevention and rehabilitation practices, the incidence and

recurrence rates of each are still high. Recent trends in elite male professional football

suggest that ACL (Walden et al., 2016) and hamstring injury rates (Ekstrand, Walden, &

Hagglund, 2016) are not declining, although results may vary in different sports and at

different levels of competition.

The results from this program of research suggest that it is possible to preferentially target

specific hamstring muscles with different exercises in women (Study 1) as shown previously

in men (Bourne, Williams, et al., 2017). Once we better understand risk factors for injury

(ACL or hamstring) the current work may allow us to design better rehabilitation programs.

For example, targeting the ST may be beneficial for hamstring injury prevention in certain

circumstances and it appears that the Nordic hamstring exercise does this better than the hip

extension exercise. Moreover, the semitendinosus has been argued to play a particularly

important role in preventing ACL injury given that this muscle functions to prevent excessive

anterior tibial translation and knee valgus, which are both movements commonly associated

with ACL injury. By contrast, reversing biceps femoris long head atrophy, occasionally

reported after hamstring strain injuries, would be better achieved by the hip extension

exercise.

111

The current work suggests the need for improvements in ACLR rehabilitation programs

because athletes are at significantly elevated risk of hamstring strain injury (Study 2) despite

successfully returning to sport, often with ~12 months of rehabilitation. Despite some recent

progress, hamstring rehabilitation programs must also be improved in light of evidence that

recurrence rates are still high in sport (Brooks et al., 2006; Croisier, 2004; Orchard &

Seward, 2002; Orchard & Seward, 2010; Woods et al., 2004). Study 2 demonstrated that

athletes with a prior ACL injury had a significantly greater risk of future HSI than athletes

without such a history, despite there being no significant differences in peak eccentric knee

flexor forces during the Nordic hamstring test. Moreover, for those athletes with a prior

ACLR, their risk of future HSI was augmented if they had also suffered a recent (12 months)

HSI.

The results from Study 3 provided novel evidence to suggest that despite successful

rehabilitation and return to sport, large deficits in ST muscle size and activation persist long

after ACLR and successful return to sport. The relatively poor activation of this muscle

suggests that it may be relatively unresponsive to the Nordic hamstring exercise and possibly

all others during rehabilitation. Whether or not alternative exercises can compensate better

for the dysfunctional ST is not yet known. Moreover, exercises that target the other medial

rotator, semimembranosus, may gain a place in future rehabilitation programs to offset

deficits in internal tibial rotator strength, although neither of the exercises investigated in

Study 1 appear to preferentially activate the semimembranosus muscle.

In conclusion, this program of research has provided novel data to suggest that the hamstring

activation patterns in women are similar to those previously reported in men. Additionally, it

has provided prospective data on the impact of ACL injury and HSI on the future risk of

112

hamstring injury and provided novel data on the activation patterns and morphology of the

hamstrings following ACLR. Future studies are needed to ascertain whether training

interventions are effective in increasing ST muscle size and activation after ACLR and

subsequent rehabilitation and whether there are exercises that can significantly compensate

for the loss of medial rotation strength, perhaps via targeting the semimembranosus. In

addition, future work on the hip extension exercise should be included in hamstring injury

prevention protocols given that this exercise may be more useful than the Nordic hamstring

exercise and other hamstring exercises at activating the commonly injured BFLongHead muscle.

These data highlight the maladaptations that occur after ACL injury and subsequent

reconstruction, while also providing evidence to form decisions regarding exercise selection

in ACL and hamstring injury prevention and rehabilitation programs.

113

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Appendices

Appendix A. Cardiovascular Questionnaire

CARDIOVASCULAR RISK FACTOR QUESTIONNAIRE

To be eligible to participate in the experiment you are required to complete the following

questionnaire which is designed to assess the risk of you experiencing any harm during the course of

the study. A full and honest disclosure of your medical history is vital for your own safety.

Name: ________________________________________________Date of Birth: ______________

Age: __________years Weight: __________kg Height: __________cm

Give a brief description of your average weekly activity pattern:

Please tick / answer the appropriate responses for the following questions:

1. Are you overweight? Yes No Don’t Know

2. Do you smoke? Yes No Don’t Know

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3. Does your family have a history of premature

(<70 years) cardiovascular problems (eg. heart

attack, stroke)? Yes No

Don’t Know

4. Are you asthmatic? Yes No Don’t Know

5. Are you diabetic? Yes No Don’t Know

6. Do you have high blood cholesterol levels? Yes No Don’t Know

7. Do you have high blood pressure? Yes No Don’t Know

8. Do you have low blood pressure? Yes No Don’t Know

9. Do you have a heart murmur Yes No Don’t Know

10. Do you have, or have you ever had, any blood-

clots in any of your blood vessels (eg. deep-

vein thrombosis)? Yes No

Don’t Know

11. Do you have, or have you ever had, any

tendency to bleed for long periods after cutting

yourself? Yes No

Don’t Know

12. Are you currently using any medication Yes No

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If so, what is the medication?

13. Have you ever experienced any of the following during exertion (exercise or physical labour)

or at rest?

Light headedness or dizziness

Pain in the chest, neck, jaw or arm

Numbness or pins-and-needles in any part of your body

Loss of consciousness

14. Do you think you have any medical complaint or any other reason which you know of that

may prevent you from safely participating in intense exercise?

Yes No

If yes, please elaborate.

I, ________________________________________________, believe that the answers to these

questions are true and correct.

Signed: ________________________________________________

Date: ________________________

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Appendix B. Magnetic Resonance Imaging Screening Form

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Appendix C. Magnetic Resonance Imaging Screening Form

anterior cruciate ligament reconstruction & the hamstrings · prevention protocols given that...

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