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Abstract
Objective To determine which strength training exercises selectively activate the biceps femoris long head (BFLongHead) muscle.
Methods We recruited 24 recreationally active men for this two-part observational study. Part 1: We explored the amplitudes and the ratios of lateral (BF) to medial hamstring (MH) normalised electromyography (nEMG) during the concentric and eccentric phases of 10 common strength training exercises. Part 2: We used functional MRI (fMRI) to determine the spatial patterns of hamstring activation during two exercises which (1) most selectively and (2) least selectively activated the BF in part 1.
Results Eccentrically, the largest BF/MH nEMG ratio occurred in the 45° hip-extension exercise; the lowest was in the Nordic hamstring (Nordic) and bent-knee bridge exercises. Concentrically, the highest BF/MH nEMG ratio occurred during the lunge and 45° hip extension; the lowest was during the leg curl and bent-knee bridge. fMRI revealed a greater BF(LongHead) to semitendinosus activation ratio in the 45° hip extension than the Nordic (p<0.001). The T2 increase after hip extension for BFLongHead, semitendinosus and semimembranosus muscles was greater than that for BFShortHead (p<0.001). During the Nordic, the T2 increase was greater for the semitendinosus than for the other hamstring muscles (p≤0.002).
Summary We highlight the heterogeneity of hamstring activation patterns in different tasks. Hip-extension exercise selectively activates the long hamstrings, and the Nordic exercise preferentially recruits the semitendinosus. These findings have implications for strategies to prevent hamstring injury as well as potentially for clinicians targeting specific hamstring components for treatment (mechanotherapy).
- Hamstrings
- Injury prevention
- Physiotherapy
- MRI
- Exercise rehabilitation
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Introduction
Hamstring strain injuries (HSIs) are commonly experienced by athletes involved in running-based sports. They are the most prevalent injury in track and field,1 Australian Rules football2 and soccer,3 and up to 30% recur within 12 months.4 Upwards of 80% of HSIs involve the biceps femoris long head (BFLongHead) muscle,5–7 and most injuries are thought to occur during the late swing phase of high-speed running.8 During this phase of the gait cycle, the BFLongHead reaches its peak length and develops maximal force while undergoing a powerful eccentric contraction to decelerate the shank for foot strike,9 and this may, at least partly, explain its propensity for injury. Prior BFLongHead injury is associated with a degree of neuromuscular inhibition10 ,11 and prolonged atrophy,12 which suggests that current rehabilitation practices do not adequately restore function to this muscle.
Hamstring weakness is a risk factor for future strain injury6 ,13 ,14 and interventions aimed at increasing strength, particularly eccentric knee flexor strength, have reduced HSI rates in several sports.15–18 However, despite an increased focus on hamstring strength in injury preventive programmes,19 exercise prescription in the clinic often does not always rely on empirical evidence.20 ,21 There is currently a very small body of work on the activation patterns of the hamstrings during commonly employed exercises.
Functional MRI (fMRI) studies have shown that activation differs within and between hamstring muscles during different tasks.11 ,22–24 For example, the semitendinosus appears to be selectively activated during the Nordic hamstring exercise (Nordic)11 and the eccentric prone leg curl,24 while the semimembranosus is preferentially recruited during the stiff leg/deadlift.23
Surface electromyography (sEMG) has also been used to analyse hamstring exercises.23–26 Results have been contradictory and are often inconsistent with the findings from fMRI.11 ,22–25 ,27 The disagreement between fMRI and sEMG might reflect the different physiological basis of each technique.28 sEMG amplitude is sensitive to the electrical activity generated by active motor units, and is detected by electrodes overlying the skin.29 This provides valuable information on the neural strategies involved during muscle activation with high temporal resolution, but is prone to cross-talk29 and cannot discriminate between closely approximated segments of muscles,30 such as the long and short heads of BF, or either of the medial hamstrings (semimembranosus and semitendinosus). By contrast, fMRI reflects the metabolic activity associated with exercise.28 Muscle activation is associated with a transient increase in the transverse (T2) relaxation time of tissue water, which can be detected from signal intensity changes in fMR images. These T2 shifts, which, like sEMG, increase in proportion to exercise intensity,31 ,32 can be mapped in cross-sectional images of muscles and, therefore, provide significantly greater spatial clarity than sEMG.28 ,30
If the patterns of hamstring muscle activation during common strength training exercises were better characterised, it would enable clinicians to better prescribe exercises for injury prevention and rehabilitation programmes. These data may also inform the design of training studies aimed at investigating the chronic adaptations induced by different exercises. Thus, the purpose of this two-part study was to determine the extent to which different exercises selectively activate the commonly injured BFLongHead. Part 1 used sEMG to determine the amplitude and ratio of lateral (BF) to medial hamstring (MH) activation during 10 commonly employed exercises. Based on these findings, part 2 employed fMRI to map muscle activation during two exercises that appeared to (1) most selectively and (2) least selectively activate the BF according to sEMG. We hypothesised that the patterns of hamstring muscle activation would differ between exercises and, on the basis of previous work,23 that more selective activation of the BFLongHead would occur during hip-extension exercise.
Methods
Participants
Twenty-four recreationally active male athletes (age, 24.4±3.3 years; height, 181.8±6.1 cm; weight, 85.2±13.4 kg) participated in this study. Eighteen athletes (age, 23.9±3.1; height, 180.6±5.9; weight, 86.0±14.8) participated in part 1 and 10 athletes (age, 24.6±4.0; height, 183.5±7.0; weight, 83.5±8.7) participated in part 2. A priori sample size estimates were based on (1) the capacity to detect a 10% difference in the ratio of BF to MH (BF/MH) sEMG amplitude between exercises25 and (2) an effect size of 1.0 in the percentage change in T2 relaxation time between muscles,11 at a power of 0.80 and with p<0.05. Participants were free from soft tissue and orthopaedic injuries to the trunk, hips and lower limbs at the time of testing, and had no known history of cardiovascular, metabolic or neurological disorders. Participants had no history of HSI in the previous 18 months, and had never suffered an anterior cruciate ligament injury. Prior to testing, all participants completed a cardiovascular screening questionnaire to make sure it was safe for them to perform intense exercise, and those who were involved in part 2 also completed a standard MRI screening questionnaire to ensure it was safe for them to enter the magnetic field. All participants provided written, informed consent for this study, which was approved by the Queensland University of Technology Human Research Ethics Committee and the University of Queensland Medical Research Ethics Committee.
Study design
This cross-sectional study involved two parts. In the first, we explored the sEMG amplitudes and ratios of BF to MH sEMG activity during 10 commonly employed strength training exercises. On the basis of these findings, part 2 involved an fMRI investigation of two exercises which appeared to (1) most selectively and (2) least selectively activate the BF muscle during eccentric contractions.
Part 1
Prior to experimental testing, participants were familiarised with the exercises used in this investigation. All were shown a demonstration of each exercise (figure 1), and performed several practice repetitions while receiving verbal feedback from the investigators. Once the participant could complete the exercise with appropriate technique, the loads were progressively increased until an ∼12-RM load (the heaviest load that can be lifted 12 times) was determined (unless the exercise was already supramaximal, ie, Nordic and glute-ham raise). On the day of testing, participants reported to the laboratory and were prepared for sEMG measurement. The testing session began with two maximal voluntary isometric contractions (MVICs) for the hamstrings. Subsequently, participants completed a single set of six repetitions of each exercise, each with the predetermined 12RM load, in randomised order. All data were sampled from a randomly selected limb (dominant or non-dominant), which was the exercised limb during all unilateral movements, and all testing sessions were supervised by the same investigator (MNB) to ensure consistency of procedures.
The 10 examined exercises: (A) bilateral stiff-leg deadlift, (B) hip hinge, (C) unilateral stiff-leg deadlift, (D) lunge, (E) unilateral bent-knee bridge, (F) unilateral straight knee bridge, (G) leg curl, (H) 45° hip extension, (I) glute-ham raise, (J) Nordic hamstring exercise.
Exercise protocol
The 10 exercises were chosen based on a review of the scientific literature.23 ,25 ,27 They included the bilateral and unilateral stiff-leg deadlift, hip hinge, lunge, unilateral bent and straight knee bridges, leg curl, 45° hip extension, glute-ham raise and the Nordic. Unless the exercise was explosive (hip hinge) or supramaximal and eccentric only (Nordic and glute-ham raise), participants completed both the concentric and eccentric phases of each exercise using a 12-RM load at a constant pace (∼2 s up and ∼2 s down).
Electromyography
Bipolar pregelled Ag/AgCl sEMG electrodes (10 mm in diameter, 15 mm interelectrode distance) (Ambu, BlueSensor N) were used to record electromyographical activity from the BF and MH. The skin of the participants was shaved, lightly abraded and cleaned with alcohol before electrodes were placed on the posterior thigh, midway between the ischial tuberosity and tibial epicondyles. Electrodes were oriented parallel to the line between these two landmarks, as per Surface EMG for non-invasive assessment of muscles (SENIAM) guidelines,33 and secured with tape to minimise motion artefact. The reference electrode was placed on the ipsilateral head of the fibula. Muscle bellies of the BF and MH were identified via palpation, and correct placement was confirmed by observing active external and internal rotation of the knee in 90° of flexion.10 During all exercise trials, hip and knee joint angles were measured simultaneously with sEMG data using two digital goniometers. The hip sensor's axis of rotation was aligned with the greater trochanter of the femur, and the knee sensor was positioned superficial to the lateral femoral epicondyle.
Maximal voluntary contraction
Surface EMG activity was recorded during MVICs of the hamstrings using a custom-made device which was fitted with two uniaxial load cells.34 Participants lay prone with their hips in 0° of flexion and knees fully extended (180°), with their ankles secured in immoveable yokes, and were asked to perform forceful knee flexion while investigators provided strong verbal encouragement. After 1–2 warm-up contractions, participants completed two 3–4 s MVICs, with 30 s of rest separating each attempt. The contraction that elicited the highest average amplitude for the BF and MH was used to represent the maximal EMG amplitude.
Data analysis
All sEMG and joint angle data were sampled at 1 kHz through a 16-bit PowerLab 26T AD unit (AD Instruments, New South Wales, Australia) (amplification=1000; common mode rejection ratio=110 dB) and analysed using LabChart 8.0 (AD Instruments, New South Wales, Australia). Raw sEMG data were filtered using a Bessel filter (frequency bandwidth=10–500 Hz), and then full-wave rectified. Joint angle data were used to determine the concentric and eccentric phases of each repetition for each exercise. For each phase, the filtered sEMG signal was normalised to values obtained during MVIC, and these normalised sEMG (nEMG) values were averaged across the six repetitions.
Statistical analysis
Data were analysed using JMP V.10.02 (SAS Institute, 2012). Descriptive statistics were calculated for mean nEMG amplitudes of BF and MH for the concentric and eccentric phases of each exercise, and an activation ratio was determined by dividing the average BF nEMG amplitude by the average MH nEMG amplitude (BF/MH); ratios >1.0 indicated that the BF was more active than the MH muscles. For both the concentric and eccentric phases, repeated measures linear mixed models fitted with the restricted maximum likelihood method were used to determine differences between exercises. For this analysis, exercise was the fixed factor, and participant identity the random factor. When a significant main effect was observed for exercise, post hoc t tests with Bonferroni corrections were used to identify the source and reported as mean differences with 95% CIs. For these analyses, the Bonferroni adjusted p value was set at <0.002.
Part 2
A cross-sectional design was used to map the spatial patterns of hamstring muscle activation during the 45° hip extension and Nordic exercises. These exercises were chosen because they (1) most selectively (45° hip extension) and (2) least selectively (Nordic) activated the BF muscle during eccentric contractions according to sEMG. Participants completed two separate exercise sessions, separated by at least 6 days (14±5 days), with each session involving one of the aforementioned exercises. Functional MRI scans of both thighs were acquired before and immediately after each exercise bout. All testing sessions were supervised by the same investigator (MNB).
Exercise protocol
A depiction of the 45° hip extension and the Nordic exercises can be found in figure 1. All exercises were completed using the same equipment as that used in part 1. Participants completed five sets of 10 repetitions of each exercise with 1 min rest intervals between sets. The higher volume of exercise (compared to part 1) was necessary because transient T2 changes reflect fluid shifts associated with glycolysis and have a higher detection threshold than sEMG.28 All subjects completed 50 repetitions successfully. During the rest periods, participants remained in a seated position (for the hip-extension exercise), or lay prone (Nordic hamstring exercise) to minimise activation of the hamstrings. The 45° hip-extension exercise was performed unilaterally (with the limb chosen randomly), with a starting load corresponding with each participant's approximate 12RM (median=10 kg; range=10–20 kg). However, if the participant could no longer complete the exercise with the allocated load, the weight was gradually reduced by increments of 5 kg until it could be completed at the desired speed (2 s up and 2 s down), which was controlled by an electronic metronome. The Nordic was performed bilaterally with body weight only. Participants received verbal support from the investigators throughout all exercise sessions to promote maximal effort. All participants were returned to the scanner immediately following the cessation of exercise, and postexercise scans began within 148.6±24 s (mean±SD).
Functional muscle MRI
All fMRI scans were performed using a 3 T (Siemens TrioTim, Germany) imaging system with a spinal coil. The participant was positioned supine in the magnet bore with their knees fully extended and hips in neutral, and straps were secured around both limbs to prevent any undesired movement. Consecutive T2-weighted axial images were acquired of both limbs beginning at the level of the iliac crest and finishing distal to the tibial plateau using a 180×256 image matrix. Images were acquired before and immediately after exercise using a Car-Purcel-Meiboom-Gill spin-echo pulse sequence and the following parameters: transverse relaxation time (TR)=2540 ms; echo time (TE)=8, 16, 24, 32, 40, 48 and 56 ms; number of excitations=1; slice thickness=10 mm; interslice gap=10 mm; field of view=400×281.3 mm). The total acquisition time for each scan was 6 min 24 s. A localiser adjustment (20 s) was applied prior to the first sequence of each scan to standardise the field of view and to align collected images between the pre-exercise and postexercise scans.11 To minimise any inhomogeneity in MRI caused by dielectric resonances at 3 T, a (B1) filter was applied to all scans; this is a postprocessing image filter that improves the image signal intensity profile without affecting the image contrast. In addition, to ensure that the signal intensity profile of T2-weighted images was not disrupted by anomalous fluid shifts, participants were instructed to avoid any exhaustive resistance training of the lower limbs in the week preceding testing, and were seated for a minimum of 15 min23 before pre-exercise imaging.
For each exercise session, the T2 relaxation times of each hamstring muscle were measured in T2-weighted images acquired before and after exercise to evaluate the degree of muscle activation during exercise. All fMRI scans were transferred to a Windows computer in the digital imaging and communications in medicine (DICOM) file format. The T2 relaxation times of each hamstring muscle (BFLongHead, BFShortHead, semitendinosus and semimembranosus) were measured in five axial slices, corresponding to 30%, 40%, 50%, 60% and 70% of thigh length; these values were determined relative to the distance between the inferior margin of the ischial tuberosity (0%) and the superior border of the tibial plateau (100%).11 ,23 Image analysis software (Sante Dicom Viewer and Editor, Cornell University) was used to measure the signal intensity of each hamstring muscle in the exercised limb in both the pre-exercise and postexercise scans. The signal intensity was measured manually in each slice using a circular region of interest (ROI)27 which was placed in a homogeneous region of contractile tissue in each muscle belly (avoiding fat, aponeurosis, tendon, bone and blood vessels). The size of each ROI varied (0.2–5.6 cm2) based on the cross-sectional area and the amount of homogeneous tissue available in each slice. The signal intensity reflected the mean value of all pixels within the ROI, and was measured across seven TEs (8, 16, 24, 32, 40, 48, 56 ms). To calculate the T2 relaxation time for each ROI, the signal intensity value at each TE was fitted to a monoexponential decay model using a least squares algorithm:23
where SI is the signal intensity at a specific TE and M represents the pre-exercise fMRI signal intensity. To assess the extent to which each ROI was activated during exercise, the mean percentage change in T2 was calculated as:
To provide a meaningful measure of whole-muscle activation, the percentage change in T2 relaxation time for each hamstring muscle was evaluated using ROIs from all five thigh levels. Previous studies have demonstrated excellent reliability of T2 relaxation time measures with intraclass correlation coefficients ranging from 0.87 to 0.94.28 ,35
Statistical analysis
Absolute T2 values before and after each exercise session were reported descriptively as mean±SD. Repeated measures linear mixed models fitted with the restricted maximum likelihood (REML) method were used to determine the spatial activation patterns of the hamstring muscles during the 45° hip extension and Nordic exercises. The percentage change in T2 relaxation time was compared between each hamstring muscle (BFLongHead, BFShortHead, semitendinosus and semimembranosus) for both exercises. 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, post hoc t tests with Bonferroni corrections were used to determine the source; the adjusted α was set at p<0.008. Given that the two examined exercises differed in intensity and contraction mode(s), it was not appropriate to directly compare the magnitude of the T2 shifts between exercises.36 Instead, repeated measures linear mixed models fitted with the REML method were used to determine differences in the ratio of BF to semitendinosus (BFLongHead/semitendinosus and BFShortHead/semitendinosus) and semimembranosus to semitendinosus (semimembranosus/semitendinosus) percentage change in T2 relaxation time between exercises. For these analyses, exercise was the fixed factor, and participant identity the random factor. When a main effect was found for exercise, post hoc t tests were again used to determine the source and reported as mean difference (and 95% CI); α was set at p<0.05 for these analyses.
Results
Levels of hamstring muscle activation
Average BF muscle activity ranged from 21.4% (lunge) to 99.3% (unilateral straight-knee bridge) MVIC during the concentric phase, and 10.7% (hip hinge) to 71.9% (Nordic) during the eccentric phase. Average MH muscle activity ranged from 18.1% (lunge) to 120.7% (leg curl) during the concentric phase, and 11.6% (hip hinge) to 101.8% (Nordic) during the eccentric phase.
Concentric biceps femoris to medial hamstring (BF:MH) activation ratio
The concentric BF/MH activation levels for each exercise can be found in figure 2A. A significant main effect was detected between exercises (p<0.001), with post hoc t tests showing that the BF/MH ratio was greater during the lunge than the leg curl (mean difference=0.8, 95% CI 0.5 to 1.1, p<0.001), and bent-knee bridge (mean difference=0.7, 95% CI 0.4 to 1.1, p<0.001). Similarly, the BF/MH ratio was greater in the 45° hip-extension exercise than the leg curl (mean difference=0.6, 95% CI 0.3 to 1.0, p<0.001), and bent-knee bridge (mean difference=0.6, 95% CI 0.2 to 0.9, p=0.001).
Biceps femoris (BF) to medial hamstring (MH) nEMG relationship for the (A) concentric and (B) eccentric phases of each exercise. Exercises to the left of and above the 45° line exhibited higher levels of BF than MH nEMG, and exercises to the right and below the line displayed higher levels of MH than BF nEMG. bKB, unilateral bent-knee bridge; GHR, glute-ham raise; HE, 45° hip extension; HH, hip hinge; L, lunge; LC, leg curl; nEMG, normalised electromyography; NHE, Nordic hamstring exercise; SDL, bilateral stiff-leg deadlift; SKB, unilateral straight knee bridge; USDL, unilateral stiff-leg deadlift.
Eccentric biceps femoris to medial hamstring (BF:MH) activation ratio
The eccentric BF/MH activation levels for each exercise can be found in figure 2B. A significant main effect was observed for exercise (p<0.001) with post hoc analyses revealing that the BF/MH ratio was significantly greater in the 45° hip extension than the Nordic (mean difference=0.7, 95% CI 0.4 to 1.0, p<0.001), bent-knee bridge (mean difference=0.7, 95% CI 0.4 to 1.0, p<0.001), leg curl (mean difference=0.6, 95% CI 0.3 to 0.9, p<0.001) and the glute-ham raise (mean difference=0.6, 95% CI 0.3 to 0.9, p<0.001) exercises. No other between-exercise differences were observed once adjusted for multiple comparisons (p>0.002).
Percentage change in T2 relaxation time following the 45° hip-extension exercise
A significant main effect was observed for muscle (p<0.001) with post hoc t tests revealing that the exercise-induced T2 changes in the BFShortHead were significantly lower than those observed for the BFLongHead (mean difference=60.7%, 95% CI 41.3% to 80.1%, p<0.001), semitendinosus (mean difference=78.0%, 95% CI 58.4% to 97.6%, p<0.001) and semimembranosus muscles (mean difference=49.8%, 95% CI 30.1% to 69.5%, p<0.001) (figure 3). The T2 change for semitendinosus was significantly greater than semimembranosus (mean difference=28.2%, 95% CI 9.2% to 47.1%, p=0.005); however, no difference was observed between the BFLongHead and semimembranosus (p=0.245) or between the BFLongHead and semitendinosus muscles (p=0.067). Absolute T2 values before and after the hip-extension exercise are reported in table 1.
T2 relaxation time values measured before (T2 pre) and immediately after (T2 post) the 45° hip extension and Nordic hamstring exercise sessions
Percentage change in fMRI T2 relaxation times of each hamstring muscle following the 45° hip-extension exercise. Values are expressed as mean percentage change compared to values at rest. *Indicates significantly different from ST, BFLH and SM (p<0.001). **Indicates significantly different from ST (p=0.005). Error bars depict SE. BFLH, biceps femoris long head; BFSH, biceps femoris short head; ST, semitendinosus; SM, semimembranosus.
Percentage change in T2 relaxation time following the Nordic hamstring exercise
A main effect was detected for muscle (p<0.001). Post hoc analyses showed that the T2 changes induced by exercise within the semitendinosus were significantly larger than those observed for the BFLongHead (mean difference=29.8%, 95% CI 20.5% to 39.2%, p<0.001), BFShortHead (mean difference=16.2%, 95% CI 6.4% to 26.0%, p=0.002) and semimembranosus (mean difference=29.9%, 95% CI 20.4% to 39.4%, p<0.001) muscles (figure 4). In addition, the T2 increase observed for BFShortHead was significantly greater than for the BFLongHead (mean difference=13.7%, 95% CI 3.9% to 23.4%, p=0.008) and semimembranosus (mean difference=13.8, 95% CI 3.8 to 23.7, p=0.008) muscles. No difference was observed between the BFLongHead and semimembranosus muscles (p=0.982). The absolute T2 values measured before and after the Nordic exercise are reported in table 1.
Percentage change in fMRI T2 relaxation times of each hamstring muscle following the Nordic hamstring exercise. Values are expressed as mean percentage change compared to values at rest. *Indicates significantly different from BFLH, BFSH and SM (p≤0.002). **Indicates significantly different from BFLH and SM (p=0.008) Error bars depict SE. BFLH, biceps femoris long head; BFSH, biceps femoris short head; ST, semitendinosus; SM, semimembranosus.
Comparison of hamstring activation ratios between exercises
When comparing the BFLongHead to semitendinosus ratio, a significant main effect was observed for exercise (p<0.001) with post hoc analyses revealing a significantly greater ratio during 45° hip-extension exercise than during the Nordic exercise (mean difference=0.7, 95% CI 0.6 to 0.9, p<0.001) (figure 5).
Ratio of BFLH to ST (BFLH/ST) percentage change in functional MRI T2 relaxation times following the 45° hip extension and the NHE. *Indicates a significant difference between exercises (p<0.001). Error bars depict SE. BFLH, biceps femoris long head; NHE, Nordic hamstring exercise; ST, semitendinosus.
A significant main effect was also detected for exercise when comparing the BFShortHead to semitendinosus ratio (p<0.001). Post hoc t tests demonstrated that this ratio was significantly greater during the Nordic than during the 45° hip-extension exercise (mean difference=0.42, 95% CI 0.24 to 0.62, p<0.001). When comparing the semimembranosus to semitendinosus ratio, a significant main effect was detected for exercise (p<0.001) with post hoc t tests showing relatively higher ratios during the 45° hip extension than during the Nordic (mean difference=0.51, 95% CI 0.39 to 0.64, p<0.001).
Discussion
This study revealed that hamstring activation patterns differ markedly between exercises. The findings suggest that hip-extension exercises more selectively target the BFLongHead than the Nordic hamstring exercise, which preferentially recruits the semitendinosus.
Magnitude of hamstring muscle activation
The Nordic hamstring exercise is effective15 ,16 ,18 in reducing HSIs in soccer players as long as compliance is adequate.37 ,38 However, we11 and others22 have previously reported that the Nordic preferentially activates the semitendinosus, and this might be interpreted as evidence that the exercise is suboptimal to protection against running-related strain injury which predominantly effects the BFLongHead. It is entirely possible that the Nordic confers injury-preventive benefits via an improved load-bearing capacity of the ST,39 however, in this study, we have provided EMG evidence which shows, despite the relatively selective activation of the semitendinosus, that the BF was still strongly activated during this exercise. Indeed, BF nEMG was higher during the Nordic than during the eccentric phase of any other exercise, and the evidence for this exercise's protective effects15 ,16 ,18 suggests that eccentric actions alone in a training programme are sufficient to make the hamstrings more resistant to strain injury. To some extent, these protective benefits might be mediated by the elongation of BFLongHead fascicles,40 which would be expected to improve the strength of this muscle at long lengths41 and reduce its susceptibility to exercise-induced damage.42 High levels of BF nEMG during the Nordic are consistent with previous investigations,25 and are the result of the supramaximal intensity of the exercise, which potentially explains why high levels of BF nEMG were also observed in the eccentric glute-ham raise. High levels of BF nEMG in concentric actions were observed in several other exercises including the straight-knee bridge, leg curl and the 45° hip extension which corroborates previous observations.25 However, the importance of hamstring activation patterns during concentric actions remains unclear from the perspective of injury prevention.
Exercise selectivity
While high levels of nEMG are an important stimulus for improving strength and voluntary activation,43 exercise selectivity may have important implications for rehabilitation. For example, inhibition of previously injured BF muscles during eccentric actions has been reported many months after rehabilitation,10 ,11 ,44 and it has been proposed45 that these deficits might partly explain observations of persistent eccentric knee flexor weakness,10 BFLongHead atrophy12 and a chronic shortening of BFLongHead fascicles.46 These data10–12 ,44 ,46 are consistent with the possibility that conventional rehabilitation strategies may not adequately target the commonly injured BFLongHead. The ratio of lateral to medial hamstring (BF/MH) nEMG varies with foot rotation47 and differs between exercises.25 In our study, the eccentric phase of the 45° hip-extension exercise exhibited the greatest BF/MH nEMG ratio (1.5±0.1) while the Nordic (0.8±0.1) and bent-knee bridge exercises (0.8±0.1) displayed the lowest ratios. These observations were confirmed in the subsequent fMRI analysis whereby the ratio of BFLongHead to semitendinosus in the 45° hip-extension exercise (0.96±0.09) was markedly higher than that observed for the Nordic (0.23±0.08). It is also noteworthy that the eccentric phase of other hip-oriented exercises (straight-knee bridge, unilateral and bilateral stiff-leg deadlift and hip hinge) displayed BF/MH nEMG ratios >1.0. By contrast, the eccentric phase of exercises that involved significant movement at the knee (leg curl, glute-ham raise, bent knee bridge and Nordic) had higher levels of medial hamstring nEMG (BF/MH ratio <1.0). These data suggest that hamstring activation strategies are partly dependent on the joints involved in each movement. During concentric contractions, the most selective BF activation was observed in the lunge exercise which corroborates a previous fMRI investigation.27 However, it is important to consider that the lunge also exhibited the lowest BF nEMG amplitude (21.4±7.4%) of any exercise which may render it a suboptimal stimulus for improving strength or evoking hypertrophy in this muscle.43 Interestingly, the exercise that least selectively activated the BF during concentric contractions was the leg curl, which mimics the joint positions and hamstring muscle-tendon lengths experienced in the Nordic exercise.
The mechanism for higher levels of BFLongHead activity during hip-extension-oriented movements remains unclear; however, it is possible that hamstring muscle moment arms play a role. For example, the BFLongHead exhibits a larger moment arm at the hip than at the knee,48 and therefore possesses a greater mechanical advantage at this joint. As a result, the BFLongHead undergoes significantly more shortening during hip extension than knee flexion.48 By comparison, the semitendinosus displays a larger sagittal plane moment arm at the knee than both BFLongHead and semimembranosus,48 which may explain its preferential recruitment during movements at this joint, such as the Nordic and leg curl exercises. It is also noteworthy that the semitendinosus is a fusiform muscle with long fibre lengths and many sarcomeres in series, which potentially makes it well suited to forceful eccentric contractions49 such as those experienced in the Nordic. Further work is needed to clarify the mechanisms underpinning these unique strategies of hamstring activation during hip and knee movements.
Our findings differ from some other investigations of hamstring activation patterns. Zebis et al 25 recently reported that both the Nordic and the prone isokinetic leg curl exercises were performed with very similar levels of semitendinosus and BFLongHead nEMG. However, in the current sEMG investigation, the Nordic and leg curl exercises resulted in more selective activation of the medial hamstrings and, in the case of the Nordic, the fMRI results also suggest selective use of the semitendinosus muscle. Differences between these studies may conceivably be related to participant sex (females25 vs males in the current study), electrode placement and the fact that this earlier work did not differentiate between the concentric and eccentric phases of each exercise. However, it is also important to consider that sEMG does not have the spatial resolution of fMRI, and cannot reliably distinguish between neighbouring muscles,30 such as the long and short heads of BF or the two medial hamstrings (semitendinosus and semimembranosus), which appear to display distinct activation magnitudes.11 ,23 ,24 These data highlight the limitations of relying exclusively on sEMG to infer strategies of hamstring muscle activation during exercise and suggest the need for more spatially robust methods in future work.
Practical considerations and implications
To interpret the results of this study, it is important to consider that sEMG and fMRI techniques measure different aspects of muscle activity. The absence of T2 relaxation time changes in people with McCardle's disease50 suggests that fMRI is sensitive to glycolysis, and it is thought that the osmotic fluid shifts which persist after exercise and give rise to T2 changes are a consequence of the accumulation of glycolytic metabolites.36 Fortunately, the proportion of Type II glycolytic fibres does not appear to vary across the hamstring muscles,51 so this is unlikely to be a confounding factor in this study. However, exercise-induced changes in T2 will be influenced by contraction mode because concentric work is characterised by higher levels of motor unit activation, nEMG amplitudes29 and is markedly less efficient than eccentric work against the same loads.52 As a consequence, the differences in T2 relaxation time changes after the 45° hip-extension exercise which involved concentric and eccentric actions, and the almost entirely eccentric Nordic exercise, do not reflect only the levels of voluntary muscle activation. Instead, fMRI can offer insights into the relative metabolic activity and reliance on different hamstring muscles in each exercise. According to the current fMRI results, the Nordic involves preferential semitendinosus use with modest use of the other hamstrings, while the 45° hip-extension exercise appears to heavily recruit both the BFLongHead and semitendinosus muscles. These observations are largely consistent with the sEMG component of this study, which also suggested higher activation of the medial than lateral hamstrings in the Nordic, and more even activation of the medial and lateral hamstrings in the 45° hip extension.
Characterising the activation patterns of the hamstrings during different tasks is an important first step in identifying exercises worthy of further investigation; however, electrical or metabolic activity of muscles should not be the only factors considered in exercise selection. Indeed, despite the BFLongHead being more active in hip extension, there is currently no evidence to suggest that training with this exercise actually leads to a reduction in the risk of HSI. Further work is required to understand how the hamstrings adapt to this and other exercises, and adaptation is influenced by a range of mechanical factors, such as contraction mode40 and range of motion,49 which were not a part of the current investigation. For example, there is little reason to believe that concentric or concentrically biased exercise is effective in HSI prevention or rehabilitation programmes.17 On the contrary, there is evidence that concentric training shortens BFLongHead fascicles40 and shifts knee flexor torque–joint angle relationships towards shorter muscle lengths,41 and neither of these adaptations are considered beneficial for HSI prevention.7 ,42 Since eccentric and concentric training programmes appear to have opposing effects on fascicle lengths40 and the torque-joint angle relationship,41 it is possible that exercises combining contraction modes may have minimal or at least blunted effects on muscle architecture.
Future studies are needed to assess the impact of certain exercises on known or proposed risk factors for HSI, such as eccentric strength6 and fascicle lengths,7 and only then will there be sufficient evidence to justify use of those exercises in intervention studies aimed at reducing the risk of injury. Based on the current findings, for example, it seems logical to compare the effects of training programmes, including the Nordic and the 45° hip-extension exercises, on the above-mentioned variables.
Limitations
Given the high cost of fMRI, it was not possible to include all participants in both parts of the experiment. Therefore, comparing the results of parts 1 and 2 should be done with caution. Furthermore, all our participants were recreationally active men, so it remains to be seen whether these findings can be applied to more highly trained athletes. We have previously shown that recreationally active young men with a history of unilateral hamstring strain exhibited less T2 change in previously injured muscles than in their uninjured homologous muscles from the contralateral limb after performing the Nordic exercise.22 Therefore, more research will be needed to establish whether the patterns of selective muscle activation observed in the current study are also evident in athletes with a history of strain injury.10 ,11 ,44 ,53 Last, it should be acknowledged that the T2 response to an exercise stimulus is highly dynamic and can be influenced by a range of factors, such as the metabolic capacity and vascular dynamics of the active tissue.28 ,36 We attempted to minimise this by recruiting only male participants with a similar age and training status.
Summary and conclusion
The patterns of hamstring muscle activation are heterogeneous across a range of different strength training exercises. We have provided sEMG evidence to suggest that, during eccentric contractions, hip-extension exercise more selectively activates the lateral hamstrings while knee flexion-oriented exercises preferentially recruit the medial hamstrings. However, despite being the least selective activator of the BF, the Nordic still elicited higher levels of BF nEMG during eccentric actions than any other exercise which may help to explain how it confers HSI-preventive benefits.15 ,16 ,18 Our fMRI investigation largely confirmed our initial sEMG observations, showing that, relative to the semitendinosus, the BFLongHead was ∼4 times more active in hip extension than in the Nordic exercise. These findings reinforce earlier observations22 ,23 and support the hypothesis that the BFLongHead, BFShortHead, semitendinosus and semimembranosus display distinct patterns of muscle use during different tasks. Collectively, the results of this study highlight the limitations of relying on a single method to infer strategies of muscle activation and suggest that the hip-extension exercise may be useful for improving strength and voluntary activation of the commonly injured BFLongHead.
What are the findings?
The hamstrings are activated differently during hip-based and knee-based tasks.
Hip-extension exercise more evenly activates the three long heads of the hamstrings, and the Nordic hamstring exercise preferentially recruits the semitendinosus.
How might it impact on clinical practice in the future?
Hamstring injury prevention and rehabilitation exercises can potentially be targeted to the site of injury.
Hip-extension exercise may be more useful than the Nordic hamstring exercise for selectively activating the commonly injured biceps femoris long head.
Acknowledgments
The authors would like to thank the Queensland Academy of Sport, Centre of Excellence for Applied Sport Science Research for funding this investigation. The authors also acknowledge the facilities, and the scientific and technical assistance of the National Imaging Facility at the Centre for Advanced Imaging, University of Queensland.
References
Footnotes
Twitter Follow Matthew Bourne @mbourne5 and Anthony Shield @das_shield
Contributors MNB was the principle investigator and was involved with study design, recruitment, analysis and manuscript writeup. MDW, DAO, GKK and AJS were involved with the study design, analysis and manuscript preparation. AA was involved in fMRI data acquisition. All authors had full access to all of the data (including statistical reports and tables) in the study and can take responsibility for the integrity of the data and the accuracy of the data analysis.
Funding This study was funded by the Queensland Academy of Sport, Centre of Excellence for Applied Sports Science Research.
Competing interests None declared.
Ethics approval All participants provided written, informed consent for this study, which was approved by the Queensland University of Technology Human Research Ethics Committee and the University of Queensland Medical Research Ethics Committee.
Provenance and peer review Not commissioned; externally peer reviewed.