Anterior cruciate ligament (ACL) injuries are debilitating and result in a significant amount of time out from training and competition (5,29,30). In addition, a history of severe knee injury (including ACL injury) increases the risk of a future hamstring strain injury (HSI) (38). However, there has been little scientific investigation into why an athlete is at an increased risk of HSI after an ACL injury (38). Reconstruction of the ACL after an injury is highly invasive and typically involves one of two types of autogenous grafts harvested from either the semitendinosus/gracilis (ST) or patella tendon (8). These procedures, independent of graft type, have been reported to result in long-term deficits in eccentric and concentric knee extensor (16,17,36) and flexor (19,35,36) strength up to 25 yrs after the reconstruction. Despite the known link between previous ACL injury and future HSI risk, research into compromised function of the knee flexors after ACL reconstruction has mostly focused on strength (19,36) and rate of force development (16). Investigations into structural differences of the hamstrings after ACL reconstruction have shown differences in hamstring muscle volume, with the gracilis and ST of the surgically repaired limb being significantly smaller and the biceps femoris long head (BFlh) being larger when compared with those in the contralateral uninjured limb (33). However, the presence of other deficits in hamstring structure and/or function after ACL reconstruction are largely unknown.
Of all the hamstring muscles, the BFlh is the most commonly injured (18,24). Therefore, a greater understanding of the factors that might alter the risk of HSI in this muscle is needed. Recently, it has been shown that limbs with a previous BFlh strain injury display architectural differences when compared with the contralateral uninjured BFlh (37). Most notably, the previously injured BFlh displays shorter fascicles compared with those in the contralateral uninjured muscle (37). It is well accepted that limbs with a previous HSI display low levels of eccentric strength, which may be the result (13,27,34) or cause (24) of injury. Because a previous ACL injury is considered a risk factor for future HSI in athletes (18,38) and considering the evidence, which has shown reductions in eccentric strength in limbs with a previous ACL injury (19,35,36), it is of interest to determine whether alterations in hamstring architecture exist, given that eccentric contractions are thought to be a powerful stimulus for in-series sarcomerogenesis (3) and hypertrophy (31). Because the BFlh is the most commonly injured of the knee flexor muscles, it is also of interest to know whether limbs with a previous ACL injury can lead, indirectly, to alterations in BFlh architecture.
The purposes of this study were to 1) determine whether a limb with a previous ACL injury displays reduced eccentric knee flexor strength during the Nordic hamstring exercise when compared with the contralateral uninjured limb and a healthy control group and 2) determine whether the architectural characteristics of the BFlh of the previous ACL-injured limb is different from those of the contralateral limb without a history of ACL injury and a healthy control group. It was hypothesized that the previous ACL-injured limb will exhibit reduced eccentric strength and will present with shorter BFlh fascicles when compared with those in the contralateral uninjured limb.
Sixty-seven males (n = 67) were recruited to participate in this case–control study. Fifty-two (n = 52) elite athletes (age, 22.6 ± 4.6 yr; height, 1.77 ± 0.05 m; body mass, 74.4 ± 5.9 kg) with no history of lower limb injury in the past 12 months and no history at all of ACL injury were recruited as a control group. Fifteen elite (n = 15) athletes with a unilateral ACL injury history (age, 24.5 ± 4.2 yr; height, 1.86 ± 0.06 m; body mass, 84.2 ± 8.1 kg) were recruited to participate and form the group with ACL injury. All athletes in both groups were currently competing at national- or international-level in soccer or Australian football. Inclusion criteria for the group with ACL injury were (i) age between 18 and 35 yr, (ii) date of surgery between 2004 and 2013, (iii) ACL reconstruction autograft from the ipsilateral ST, (iv) no history of HSI in the past 12 months, and (v) returned to preinjury levels of competition and training. All athletes with an ACL injury reported standard rehabilitation progression as directed by the physiotherapist of their respective clubs (21) and reported the use of some eccentric hamstring conditioning at the time of assessment (10). The athletes with an ACL injury (nine soccer players and six Australian Rules Football players) were recruited to assess the differences in the BFlh architectural characteristics, maximal voluntary isometric contraction (MVIC) knee flexor strength, and average peak force during the Nordic hamstring exercise of their ACL-injured limb and the contralateral uninjured limb. All participants provided a written informed consent before testing, which was undertaken at the Australian Catholic University, Fitzroy, Victoria, Australia. Ethical approval for the study was granted by the Australian Catholic University human research ethics committee.
The test–retest reliability of real-time two-dimensional ultrasound–derived measures of muscle thickness, pennation angle, and estimates of BFlh fascicle length at rest and during different isometric contraction intensities has previously been investigated (37). Nordic hamstring exercise strength was assessed using a custom-made device (25). All participants (group with ACL injury and control group) had their BFlh architectural characteristics as well as their eccentric and MVIC knee flexor strength assessed during a single session. All athletes were assessed during early preseason in their chosen sport (soccer, June to July 2014; Australian Rules Football, November to December 2014).
BFlh architecture assessment
Muscle thickness, pennation angle, and estimates of BFlh fascicle length were determined from ultrasound images (Fig. 1) taken along the longitudinal axis of the muscle belly using a two-dimensional B-mode ultrasound (frequency, 12 MHz; depth, 8 cm; field of view, 14 × 47 mm) (Vivid i; GE Healthcare, WI). The scanning site was determined as the halfway point between the ischial tuberosity and the knee joint fold, along the line of the BFlh. Once the scanning site was determined, the distance of the site from various anatomical landmarks was recorded to ensure reproducibility of the scanning site for future testing sessions. These landmarks included the ischial tuberosity, fibula head, and the posterior knee joint fold at the midpoint between BF and ST tendon. All architectural assessments were performed with participants in a prone position and the hip in a neutral position after at least 5 min of inactivity. Assessments at rest were always performed first, followed by the isometric contraction protocol. Assessment of BFlh architecture at rest was performed with the knee at 0° (fully extended). Assessment of BFlh architecture during isometric contractions was always performed with the knee at 0° of knee flexion and was preceded by MVIC in a custom-made device (25). Participants were positioned prone on top of a padded board with both the hip and knee fully extended. The ankles were secured superior to the lateral malleolus by individual ankle braces, which were secured atop custom-made uniaxial load cells (Delphi Force Measurement, Gold Coast, Australia) fitted with wireless data acquisition capabilities (Mantracourt, Devon, United Kingdom). Participants were then instructed to contract maximally over a 5-s period, and the instantaneous peak force was used to determine the MVIC. The active architectural assessment was performed in the same device at 25% of MVIC with the participants shown the real-time visual feedback of the force produced to ensure that target contraction intensities were met.
To gather ultrasound images, the linear array ultrasound probe, with a layer of conductive gel, was placed on the skin over the scanning site, aligned longitudinally and perpendicular to the posterior thigh. Care was taken to ensure minimal pressure was placed on the skin by the probe because this may influence the accuracy of the measures (15). Finally, the orientation of the probe was manipulated slightly by the sonographer if the superficial and intermediate aponeuroses were not parallel. Reliability of the sonographer when assessing the BFlh architectural characteristics has been reported previously (37).
Once the images were collected, analysis was undertaken offline (MicroDicom version 0.7.8; Bulgaria). For each image, six points were digitized as described by Blazevich et al. (1). After the digitizing process, muscle thickness was defined as the distance between the superficial and intermediate aponeuroses of BFlh. A fascicle of interest was outlined and marked on the image (Fig. 1). The angle between this fascicle and the intermediate aponeurosis was measured and given as the pennation angle. The aponeurosis angle for both aponeuroses was determined as the angle between the line marked as the aponeurosis and an intersecting horizontal line across the captured image (1,14). Fascicle length was estimated from the length of the outlined fascicle between aponeuroses. Because the entire fascicle was not visible in the field of view of the probe, its length was estimated via the following validated equation from Blazevich et al. (1) and Kellis et al. (14):
where FL stands for fascicle length, AA stands for aponeurosis angle, MT stands for muscle thickness, and PA stands for pennation angle.
Fascicle length was reported in absolute terms (cm) and also relative to muscle thickness (fascicle length/muscle thickness). The same assessor (R. G. T.) collected and analyzed all scans and was blinded to participant identifiers during the analysis.
Eccentric hamstring strength
The assessment of eccentric hamstring strength using the Nordic hamstring exercise field testing device has been reported previously (25). Participants were positioned in a kneeling position over a padded board, with the ankles secured superior to the lateral malleolus by individual ankle braces, which were secured atop custom-made uniaxial load cells (Delphi Force Measurement, Gold Coast, Australia) fitted with wireless data acquisition capabilities (Mantracourt, Devon, United Kingdom). The ankle braces and load cells were secured to a pivot, which allowed the force to always be measured through the long axis of the load cells. After a warm-up set, participants were asked to perform one set of three continuous maximal bilateral repetitions of the Nordic hamstring exercise. Participants were instructed to gradually lean forward at the slowest possible speed while maximally resisting this movement with both lower limbs while keeping the trunk and hips in a neutral position throughout and the hands held across the chest. After each attempt, a visual analog scale was given to assess the level of pain that was experienced. None of the participants reported any pain during testing. Verbal encouragement was given throughout the range of motion to ensure maximal effort. The peak force for each of the three repetitions was averaged for all statistical comparisons.
While positioned in the custom-made device, shank length (m) was determined as the distance from the lateral tibial condyle to the midpoint of the brace, which was placed around the ankle. This measure of shank length was used to convert the force measurements (N) to torque (N·m). Knee flexor eccentric and MVIC strength force data were transferred to a personal computer at 100 Hz through a wireless USB base station (Mantracourt, Devon, United Kingdom). The peak force value during the MVIC and the three Nordic hamstring exercise repetitions for each of the limbs (left and right) were analyzed using custom-made software. Eccentric knee flexor strength, reported in absolute terms (N and N·m) and relative to body mass (N·kg−1 and N·m·kg−1), was determined as the average of the peak forces from the three repetitions for each limb, resulting in a left and right limb measure (25). Knee flexor MVIC strength, reported in absolute terms (N and N·m) and relative to body mass (N·kg−1 and N·m·kg−1), was determined as the peak force produced during a 5-s maximal effort for each limb.
All statistical analyses were performed using SPSS version 18.104.22.168 (IBM Corporation, Chicago, IL). Where appropriate, data were screened for normal distribution using the Shapiro–Wilk test and homoscedasticity of the data using the Levene test. Reliability of the assessor (R. G. T.) and processes used for the determination of the BFlh architectural characteristics have previously been reported (37).
At both contraction intensities, a split plot-design ANOVA, with the within-subject variable being limb (left/right or uninjured/ACL injured, depending on the group) and the between-subject variable being group (control group or group with ACL injury) was used to compare BFlh architecture, MVIC, and Nordic hamstring exercise strength variables. For the control group, all architectural and strength measurements from the left and right limbs were averaged, as the limbs did not differ (P > 0.05) (Table 1) in order to allow a single control group measure. Where significant limb–group interactions were detected, post hoc t-tests with Bonferroni adjustments to the alpha level were used to identify which comparisons differed.
Further between group analyses were undertaken to determine the extent of the between-limb asymmetry in BFlh architecture, MVIC, and Nordic hamstring exercise strength in the control group and in the group with ACL injury. The control group between-limb asymmetry was determined as the right limb minus the left and then converted to an absolute value (34,37), whereas in the group with ACL injury, asymmetry was determined as the uninjured limb minus the ACL-injured limb. Independent t-tests were used to assess differences in the extent of the between-limb asymmetry in the control group compared with that in the group with ACL injury. Bonferroni corrections were used to account for inflated type 1 error due to the multiple comparisons made for each dependent variable. Significance was set at P < 0.05, and where possible, Cohen d (4) was reported for the effect size of the comparisons, with the levels of effect being deemed small (d = 0.20), medium (d = 0.50), or large (d = 0.80) as recommended by Cohen (4).
Power analysis was undertaken a priori using G-Power (7). The analysis was based on the anticipated differences between the ACL-injured limb and the contralateral uninjured limb in the group with ACL injury. Estimates of effect size were based on previous research investigating differences between limbs in athletes with unilateral HSI history (37). This previous study reported differences in BFlh fascicle length between the previously injured limb and the contralateral uninjured limb to have an effect size of 1.34 when assessed at rest. Therefore, an effect size of 0.8 was deemed reasonable as a starting point. Power was set at 80% with an alpha of 0.05, returning a calculated sample size of 15. As a cross-reference to confirm this sample size calculation, previous studies that have used similar designs have used samples from 13 to 15 (27,28,34,37).
The participants in the group with ACL injury were 10.1 ± 8.1 kg heavier and 6.1 ± 0.06 cm taller compared with those in the control group (P < 0.05). All athletes from the group with ACL injury had experienced at least one ACL injury in the past 9 yr (median time since surgery, 3.5 yr (range, 1–9 yr)).
BFlh architectural comparisons
A significant limb–group interaction effect was found for fascicle length and fascicle length relative to muscle thickness at both contraction intensities (P = 0.004). Post hoc analysis showed that fascicle length and fascicle length relative to muscle thickness were significantly shorter in the BFlh of the ACL-injured limb compared with that in the contralateral uninjured limb in the group with ACL injury at both contraction intensities (P < 0.05; d range, 0.87–1.31) (Table 1; Fig. 2). A significant limb–group interaction effect was detected at both contraction intensities (P = 0.003) for pennation angle. Post hoc analysis showed that pennation angle was greater in the injured limb compared with that in the contralateral uninjured limb in the group with ACL injury at both contraction intensities (P < 0.05; d range, 0.87–0.93) (Table 1; Fig. 2). Comparisons of muscle thickness displayed no significant main effects (P > 0.05; d range, 0.27–0.42) (Table 1; Fig. 2); however, when comparing the ACL-injured limb with the contralateral uninjured limb, at rest, there was a small effect size (d = 0.42) (Table 1; Fig. 2) where the uninjured limb was thicker than the injured. No significant differences in any BFlh architectural characteristics were found when comparing either limb in the group with ACL injury with the average of both limbs in the control group (P > 0.05; d range, 0.11–0.21).
Comparing the extent of between-limb asymmetry in all the BFlh architectural characteristics in the control group with the group with ACL injury, the asymmetry in fascicle length, fascicle length relative to muscle thickness, and pennation angle were greater in the group with ACL injury (P < 0.05; d range, 0.86–1.13) (Fig. 3) (see Table, Supplemental Digital Content 1, Between-limb asymmetry of the biceps femoris architectural characteristics and knee flexor strength measures of the ACL-injured group to the control group absolute difference, http://links.lww.com/MSS/A582).
Knee flexor strength measures
A significant limb–group interaction effect was found for average peak force during the Nordic hamstring exercise (P = 0.001). Post hoc analysis showed that the ACL-injured limb (269.9 ± 81.4 N) was 13.7% weaker than the contralateral uninjured limb (312.9 ± 85.1 N) in the group with ACL injury (between-limb difference, 43.0 N; 95% confidence interval (CI), 7.2 N–78.7 N; P = 0.022; d = 0.51) (Table 2). Independent of whether it was relative to body weight or an absolute measure of force or torque, the ACL-injured limb was weaker than the average of both limbs in the control group (P < 0.05; d range, 0.58–0.74). There were no significant relative or absolute differences in force or torque between the uninjured limb in the group with ACL injury and the average of both limbs in the control group (mean difference, 7.1 N; 95% CI, −39.4 N to 53.5 N; P = 0.763; d = 0.08).
Between-limb asymmetry during the Nordic hamstring exercise was greater in the group with ACL injury (between-group difference, 36.0 N; 95% CI, 12.2 N–59.7 N; P = 0.003; d = 0.71) (see Table, Supplemental Digital Content 1, Between-limb asymmetry of the biceps femoris architectural characteristics and knee flexor strength measures of the ACL-injured group to the control group absolute difference, http://links.lww.com/MSS/A582).
Comparisons of knee flexor MVIC strength of the ACL-injured limb with that of the contralateral uninjured limb and the average of both limbs in the control group displayed no significant differences (P > 0.05; d range, 0.34–0.45).
Finally, no significant differences were found when comparing the extent of between-limb asymmetry in knee flexor MVIC between the group with ACL injury and control group (between group difference, −3.8 N; 95% CI, −34.7 N to 27.1N; P = 0.807; d = −0.07) (see Table, Supplemental Digital Content 1, Between-limb asymmetry of the biceps femoris architectural characteristics and knee flexor strength measures of the ACL-injured group to the control group absolute difference, http://links.lww.com/MSS/A582).
The major findings were that elite athletes with a unilateral ACL injury, which was reconstructed with a graft from the ipsilateral ST, had shorter fascicles and greater pennation angles in the BFlh of the previously ACL-injured limb than those in the contralateral uninjured limb both at rest and during a 25% MVIC. Furthermore, between-limb asymmetry of fascicle length and pennation angle was greater in the previous group with ACL injury than those in the control group. Moreover, eccentric strength during the Nordic hamstring exercise was significantly lower in the previous ACL-injured limb when compared with that in the contralateral uninjured limb (d = 0.51), whereas comparisons of isometric knee flexor strength displayed a small difference between limbs as determined by effect size (d = 0.31). In addition, the group with a previous ACL injury had greater between-limb asymmetry in eccentric knee flexor strength compared with that in the control group. To the authors’ knowledge, this is the first study that has investigated the BFlh architectural differences in a limb with a previous ACL injury, reconstructed from the ipsilateral ST, in comparison with uninjured limbs (both from the contralateral limb and the control group). In addition, no previous work has examined the between-limb differences in eccentric strength during the Nordic hamstring exercise in individuals with a history of unilateral ACL injury.
Observations of shorter muscle fascicles and greater pennation angles have been reported in previously strain-injured BFlh compared with the contralateral uninjured limb (37). However, no earlier study had investigated the effect that a previous ACL injury has on hamstring muscle architecture. Athletes in the current study with a previous ACL injury, reconstructed from the ST, have somewhat comparable BFlh fascicle lengths in their injured limb, at rest (10.13 ± 1.39 cm) (Table 1), and at 25% of MVIC (9.08 ± 1.38 cm) (Table 1) compared with previously strain-injured BFlh (rest, 10.40 ± 1.12 cm; 25% of MVIC, 9.50 ± 1.10 cm) (37). In addition, the extent of between-limb asymmetry in BFlh fascicle length in the athletes from the current study, when assessed at rest (13.7%; 1.61 ± 0.31 cm) and 25% of MVIC (12.9%; 1.35 ± 0.25 cm) is comparable with that in individuals with a unilateral history of BFlh strain injury (rest, 12.9%; 1.54 ± 0.12 cm; 25% of MVIC, 10.9%; 1.17 ± 0.10 cm) (37). The similarities in BFlh fascicle length and between-limb asymmetry in individuals with two different injuries are of great interest because history of both ACL injury and HSI increases the risk of future HSI (18,38). However, the maladaptations that influence the increase in HSI risk in individuals with a previous ACL injury are unknown. It has been hypothesized that possessing shorter muscle fascicles, with fewer in-series sarcomeres, may result in increased susceptibility to eccentrically induced muscle damage (2,22). Therefore, the shorter BFlh fascicle length in the limb with a history of ACL injury may increase its susceptibility to muscle damage during powerful eccentric contractions that occur during periods of high-speed running. This increased susceptibility to muscle damage may then contribute to the increased HSI risk in individuals with a history of ACL injury.
Although speculative from the current data, changes in muscle activation throughout the entire knee range of motion may contribute to variations in muscle architecture in individuals with a history of ACL injury. Certainly, individuals with a previous HSI display less BFlh activation at long muscle lengths, which hypothetically might be mediated by the pain associated with the initial injury (11,27,34). Investigations into experimentally induced pain have shown alterations in muscle activation, mechanical behavior, and motor unit discharge rates in an apparent effort to reduce stress (force per unit area) and protect the painful structures from further discomfort (11,12,20). Therefore, the pain associated with an ACL injury, as well as the surgical reconstruction, may alter knee flexor muscle activation so as to protect the knee from further discomfort. If these alterations in muscle activation are accentuated at long knee flexor muscle lengths, this may then result in architectural maladaptations of the knee flexors. However, reductions in fascicle length can occur despite compensatory increases in BFlh muscle volume in the ACL-injured limb (33) because changes in muscle architecture can occur independent of muscle size (23). What is still to be determined is why and/or how ACL reconstruction using the ipsilateral ST might influence BFlh architecture. Reductions in activation and eccentric strength may have contributed to the architectural alterations within the BFlh; however, other factors may influence these changes. Without architectural data of the other knee flexor muscles (see limitations section), it is impossible to know whether these architectural deficits are evident in all the hamstring muscles in the previous ACL-injured limb. It is unlikely, however, that there is a unique stimulus to the BFlh compared with the medial hamstrings. Future research should investigate whether the architectural differences, found in the BFlh, exist in the neighboring knee flexors.
In this study, individuals with a unilateral ACL injury reconstructed from the ipsilateral ST displayed a significantly lower amount of eccentric strength during the Nordic hamstring exercise in the previously ACL-injured limb when compared with those in the contralateral uninjured limb (15.9%; d = 0.51), despite smaller differences in MVIC strength (5.1%; d = 0.31). Similar between-limb differences in eccentric knee flexor strength (16.9%) are evident in individuals with a unilateral ACL injury when assessed via isokinetic dynamometry more than 20 yr after the injury (36). With respect to the link between previous ACL injury and HSI, elite Australian footballers who subsequently went on to sustain a HSI were approximately 14% weaker compared with those that remained injury free when assessed prospectively (24). This is a similar magnitude of weakness seen in the previously ACL-reconstructed limb compared with that in the contralateral uninjured limb in the current study. Given that approximately 60% of HSI occur during high-speed running, these low levels of eccentric strength may suggest a reduced ability to decelerate the lower limb during the terminal swing phase of high-speed running (24,26). This, coupled with the previously hypothesized increased susceptibility for muscle damage due to shorter muscle fascicles (2,9), may increase the risk of a future strain injury of the BFlh in individuals with a previous ACL injury during high-speed running or other repetitive eccentric contractions. In addition, the lower levels of eccentric strength, without any differences in MVIC, in the previously ACL-injured limb may be due to a maladaptive tension limiting mechanism (9). As the stresses and strains on the musculoskeletal structures are greater during eccentric contractions compared with those during isometric efforts (6), the lower levels of force during the Nordic hamstring exercise may act to reduce tissue loading in the ACL-injured limb.
We acknowledge that there are limitations associated with the study. First, the investigation of the muscle architectural characteristics only occurred in the BFlh, and therefore, the extent to which the other knee flexors may also be altered is unknown. Indeed, previous research suggests that compensatory adaptations may occur where intermuscular coordination is altered to accommodate the injured muscle (32). We have attempted imaging of the ST, and initial data did not display acceptable reproducibility. Previous studies have also reported lower reliability when assessing ST when compared with BFlh with intraclass correlations of 0.77 and 0.91, respectively (14). In addition, as the BFlh is the most commonly injured hamstring muscle (18,24), we believe that the findings reported in BFlh architectural differences between limbs with and without ACL reconstruction are of importance. Future work should examine whether these architectural differences are present in the other knee flexors, particularly in the harvested ST. Second, the retrospective nature of the study limits the determination of whether the differences in muscle architecture and eccentric strength existed before the ACL injury and reconstruction or were the result of the incident. Prospective investigations are required to determine any existence of a causal relation and should be the focus of future research. Finally, the current study only included athletes with an ACL injury reconstructed with a graft from the ipsilateral ST. Future research should aim to investigate the architectural variations in athletes with a non-ST graft.
In conclusion, the current study provided evidence that BFlh fascicle length, pennation angle, and eccentric knee flexor strength during the Nordic hamstring exercise in individuals with a unilateral ACL injury, which was reconstructed from the ipsilateral ST, is significantly different from limbs without a history of ACL injury. Despite the retrospective nature of these findings, they provide significant insight into the architectural and eccentric strength asymmetries of the BFlh, which exist in those who have a history of ACL injury. These differences should be considered when attempting to limit the risk of future HSI in those with a history of ACL injury. Much work is still required to determine whether hamstring muscle architecture and eccentric knee flexor strength play a role in the etiology of an ACL injury.
Dr. Anthony Shield and Dr. David Opar are listed as coinventors on an international patent application filed for the experimental device (PCT/AU2012/001041.2012).
This study was partially funded by a Faculty of Health Research grant from the Australian Catholic University.
The results of this study do not constitute endorsement by the American College of Sports Medicine.
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