Hamstring strain injuries (HSI) are the most prevalent injury type in many running based sports (7,12,29) and result in athlete unavailability (7,41), reduced performance on return to competition (37), and financial loss for sporting teams/organisations (17). An unresolved issue with HSI is the elevated risk of recurrence, with reported reinjury rates of 16%–54% (1,12,15,29).
To minimize the risk of hamstring strain reinjury, a greater understanding of the maladaptations associated with a previous insult is required. Retrospective reports have identified prolonged deficits in the rate of torque development (27), biceps femoris (BF) activation (26,34), BF muscle volume (33), changes in the angle of peak torque (6), and eccentric knee flexor strength (26) when tested via isokinetic dynamometry (26) as well as during the performance of the Nordic hamstring exercise (25) in previously injured hamstrings. Shifts in the angle of peak torque toward shorter muscle lengths have been proposed to be indicative of a reduction of in-series sarcomeres and muscle fascicle length (6). Lesser fascicle lengths after HSI, hypothesized previously (6,14), might be most troublesome for reinjury because these would increase muscle susceptibility to eccentrically induced microscopic muscle damage, which may be a precursor to macroscopic damage in the form of a muscle strain injury (23). However, it is not yet known if a previously strained biceps femoris long head (BFlh) displays shorter fascicles compared to an uninjured BFlh.
Of all the methods available for the in vivo assessment of muscle architecture (22), real-time two-dimensional B-mode ultrasound is the most cost-effective and time-efficient. Two-dimensional ultrasonography has been shown to be a valid (19) and reliable (8,11,30) measure of BFlh architecture at a number of different hip and knee joint angles (8) while the muscle is at rest (8,30). Yet, muscle architecture during graded isometric contraction is also of interest because architecture is altered significantly when the muscle is active (21,22) and is likely to have greater implications for understanding function. Currently, however, there is no reported reliability data in the literature for the assessment of BFlh architecture during graded isometric contractions.
The purposes of this study were 1) to determine the test–retest reliability of real-time two-dimensional ultrasound measures of BFlh architecture (muscle thickness, pennation angle, and fascicle length) at rest and during graded isometric contractions and 2) to determine whether a previously strained BFlh displays different architecture compared to an uninjured BFlh. It is hypothesized that the previously injured limb will present with a BFlh, displaying shorter fascicles and greater pennation angles compared to the contralateral uninjured BFlh.
Thirty-six males were recruited to participate in this case–control study. Twenty recreationally active males (age = 26.1 ± 7.4 yr, height = 1.80 ± 0.05 m, body mass = 78.1 ± 8.7 kg) with no history of HSI were recruited to determine the test–retest reliability of the ultrasound measures of BFlh architecture as well as to serve as the control group. Sixteen elite (competing at national or international level) athletes with a unilateral BFlh strain injury history within the last 18 months (age = 23.7 ± 3.3 yr, height = 1.85 ± 0.07 m, body mass = 83.6 ± 7.9 kg) were recruited to participate and form the previously injured group. The athletes (12 Australian Rules Football players, 2 soccer players, 1 field hockey player, and 1 track and field athlete), who had all returned to preinjury levels of training and competition, were recruited to assess the differences in architecture between their previously injured and uninjured BFlh. Previously injured participants supplied their clinical notes to the research team, and all had their diagnosis confirmed by magnetic resonance imaging. All previously injured athletes reported standard rehabilitation progression (16) and the use of some eccentric conditioning as guided by their physical therapist. All participants provided 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 fascicle length of BFlh at rest and during graded isometric contractions was determined across three testing sessions separated by at least 24 h. On the final visit, eccentric knee flexor strength during the Nordic hamstring exercise was also assessed using a custom-made device (25). Determining the impact of a previous strain injury on the BFlh architectural characteristics and eccentric knee flexor strength was performed during a single assessment session in the previously injured cohort.
BFlh architecture assessment.
Muscle thickness, pennation angle, and fascicle length of the BFlh was determined from ultrasound images 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; GE Healthcare Vivid-i, Wauwatosa, 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 semitendinosus tendon. On subsequent visits during the reliability study, the scanning site was determined and marked on the skin and then confirmed by replicated landmark distance measures. All architectural assessments were performed with participants in a prone position with a neutral hip position after at least 5 min of inactivity. Assessments at rest were always performed first followed by the graded isometric contraction protocol. Assessment of BFlh architecture at rest was performed with the knee at three different positions, 0°, 30°, and 60° of knee flexion, which were determined via a manual goniometer. Assessment of BFlh architecture during isometric contractions was always performed with the knee at 0° of knee flexion and preceded by a maximal voluntary isometric contraction (MVIC), performed in a custom-made device (25). The graded isometric contractions of the knee flexors were performed in the same device at 25%, 50%, and 75% of MVIC with the participants shown the real-time visual feedback of the force produced to ensure that target contraction intensities were met. Assessment of the MVIC of the knee flexors was undertaken in a prone position, with both the hip and knee fully extended (0°). Participants were instructed to contract maximally over a 5-s period, of which the peak force was used to determine the MVIC.
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 (20). Finally, the orientation of the probe was manipulated slightly by the sonographer (R.G.T.) if the superficial and intermediate aponeuroses were not parallel.
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. (5). 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. 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 (5,19). Fascicle length was determined as the length of the outlined fascicle between aponeuroses. Because the entire fascicle was not visible in the field of view, it was estimated via the following validated equation from Blazevich et al. (5) and Kellis et al. (19):
where FL = fascicle length, AA = aponeurosis angle, MT = muscle thickness and PA = 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 Nordic hamstring exercise 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, UK). 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 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.
All statistical analyses were performed using SPSS Version 220.127.116.11 (IBM Corporation, Chicago, IL). For the determination of reliability, descriptive statistics for the architectural variables of the control group were determined for the left and right limbs separately. Where appropriate, data were screened for normal distribution using the Shapiro–Wilk test and homoscedasticity of the data using Levene test. Intraclass correlation coefficient (ICC), typical error (TE), and TE as a coefficient of variation (%TE) were calculated to assess the extent of variation between the first to second and the second to third visits (39). On the basis of previous quantitative reliability literature, it was subjectively determined that an ICC ≥ 0.90 was regarded as high, between 0.80 and 0.89 was moderate, and ≤0.79 was poor (16,38). Minimum detectable change at a 95% confidence interval (MDC95) was calculated as TE × 1.96 × √2. In addition, a %TE of ≤10% was considered to represent an acceptable level of reliability (10).
At each contraction intensity, a split-plot design ANOVA, with the within-subject variable being limb (left/right or uninjured/injured, depending on group) and the between-subject variable being group (control or previously injured), was used to compare BFlh architecture and Nordic hamstring exercise strength variables. Control group data were used from the third trial. Where significant limb–group interactions were detected, post hoc t-tests with Bonferroni adjustments to the α 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 and Nordic hamstring exercise strength in the control and previously injured groups. The control group’s between-limb asymmetry was determined as the right limb minus the left limb and then converted to an absolute value (34), whereas in the previously injured group, asymmetry was determined as the uninjured limb minus the injured limb. t-Tests were used to assess differences in the extent of the between-limb asymmetry in the control compared to the previously injured group. Bonferroni corrections were used to account for inflated Type I error due to the multiple comparisons made for each dependent variable. Significance was set at P < 0.05, and where appropriate, Cohen’s d (9) 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 (1988).
All architectural variables examined displayed high reliability at rest (Table 1) and during graded isometric contractions (Table 2). For fascicle length, all ICCs were above 0.93 at rest and during isometric contractions, and all %TE were below 4.9% at rest and 3.7% during isometric contractions. For muscle thickness, all ICCs were above 0.95 at rest and above 0.96 during isometric contractions. All muscle thickness %TE were below 4.2% at rest and 3.8% during isometric contraction. For pennation angle, at rest all ICCs were above 0.95, and during isometric contractions, all ICCs were above 0.93, with all %TE below 3.2% and 2.6% at rest and during isometric contractions, respectively.
BFlh architectural comparisons.
Fascicle length, pennation angle, muscle thickness, and fascicle length relative to muscle thickness in the injured and uninjured limb of the previously injured group were not significantly different from the control group data at any contraction intensity (P > 0.05). A significant limb-by-group interaction effect was found for fascicle length and fascicle length relative to muscle thickness at all contraction intensities (P < 0.011). Post hoc analysis showed that fascicle length and fascicle length relative to muscle thickness were significantly shorter in the injured BFlh compared to the contralateral uninjured BFlh in the previously injured group at all contraction intensities (P < 0.05, d range = 0.58–1.34; Table 3, Fig. 1A, D). A significant interaction effect for limb-by-group was detected at all contraction intensities (P < 0.004) for pennation angle. Post hoc comparisons showed that pennation angle was significantly greater in the injured BFlh compared to the contralateral uninjured BFlh in the previously injured group (P < 0.05, d range = 0.62–0.88; Table 3, Fig. 1B). There were no significant main effects detected for comparisons of muscle thickness between the injured and uninjured BFlh in the previously injured group at any contraction intensity (P > 0.05, d = 0.18–0.43; Table 3, Fig. 1C). Furthermore, the control group showed no between-limb differences in any BFlh architectural characteristics at any contraction intensity (P > 0.05, d = 0.01−0.19, Table 3, Figure 2).
When comparing the extent of between-limb asymmetry in BFlh architecture of the control group to the previously injured group, the asymmetry in fascicle length, fascicle length relative to muscle thickness, and pennation angle was significantly greater in the previously injured group at all contraction intensities (P < 0.05, d = 0.75–1.19, Table 4, Fig. 2). There were no differences between groups in the extent of between-limb asymmetry in muscle thickness at any contraction intensity (P > 0.359, d < 0.31; Table 4, Fig. 2).
Eccentric Nordic hamstring exercise strength.
The control group showed no statistically significant difference between the right (295.1 ± 74.5 N) and left limb (281.4 ± 78.1 N) in average peak force during the Nordic hamstring exercise (between-limb difference = 4.8%; 13.7 N, 95% confidence interval [CI] = −0.17 to 27.67; P = 0.053; d = 0.18). In contrast, the injured limb (288.6 ± 84.8 N) was weaker than the contralateral uninjured (341.1 ± 100.2 N) limb in the previously injured group (between-limb difference = −15.4%; 52.5 N, 95% CI = −76.2 to −28.4; P < 0.001, d = 0.56). The previously injured group also displayed a larger between-limb asymmetry compared to the control group (P = 0.007, d = 1.01).
Maximal isometric knee flexor strength.
The knee flexor MVIC forces did not significantly differ between the right (273.8 ± 33.4 N) and left limbs (263.2 ± 33.5 N) of the control participants (between-limb difference = 3.8%; 10.6 N, 95% CI = −2.4 to 23.8; P = 0.106; d = 0.31) or between the injured (236.6 ± 53.1 N) and contralateral uninjured limbs (262.6 ± 51.4 N) in the previously injured group (between-limb difference = 9.9%; 26 N, 95% CI = −15.8 to 67.7; P = 0.205; d = 0.49). Furthermore, the extent of between-limb asymmetry during the knee flexor MVIC was not significantly different when comparing the control group and previously injured group (P = 0.467, d = 0.25).
Following the reliability study, a priori power analysis for the previously injured group was completed using G-Power (13). The analysis was based on the anticipated differences in fascicle length between the injured and uninjured limbs. The effect size was estimated based on the only study to date that has reported changes in BF fascicle length after eccentric training. That study reported a very large increase (effect size of approximately 1.9) of 33% in fascicle after the intervention. Therefore, an effect size of 0.8 was deemed reasonable as a starting point. Power was set at 80%, with an α level 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 sample sizes from 13 to 15 (26,27,34).
To the authors’ knowledge, this is the first study that describes the reliability of assessing the architecture of the BFlh muscle in vivo during graded isometric contractions. In addition, no previous work has examined architectural differences between previously injured and uninjured muscles. The major findings were that the use of two-dimensional ultrasound to assess in vivo BFlh architecture is highly reliable at rest and during isometric knee flexion, when performed by a skilled operator. In addition, in elite athletes with a unilateral history of BFlh strain injury, fascicles were shorter and pennation angles were greater in the previously injured limb compared to the contralateral uninjured limb. Moreover, between-limb asymmetry in fascicle length and pennation angle was greater in the previously injured group compared to the control group. Eccentric knee flexor force during the Nordic hamstring exercise was also significantly reduced in the previously injured limbs compared to the contralateral uninjured limb in the previously injured group. By contrast, isometric strength was not statistically different in previously injured limbs compared to the contralateral uninjured limb.
Observations of shorter muscle fascicles in the previously injured BFlh (Fig. 1A) support preceding literature, which inferred altered architectural characteristics through the use of isokinetic dynamometry (6). Brockett et al. (6) proposed that differences in the torque–joint angle relationship in those with a history of HSI were mediated by a reduction in the number of in-series sarcomeres. The current study supports their hypothesis; however, the extent to which injury and fascicle shortening in one of many knee flexor muscles can influence the knee flexor torque–joint angle relationship is not clear. Future work should examine whether architectural changes extend beyond the injured muscle into the neighboring knee flexors.
Changes to muscle activation patterns across the range of knee motion may also contribute to shifts in the torque–joint angle relationship. Inhibition of the previously injured hamstrings seems to be greatest at long muscle lengths (34), and this would be expected to shift torque–joint angle relationships to shorter lengths. It has also been argued that neuromuscular inhibition and its preferential effect on eccentric strength after hamstring injury (25,26) may also contribute to the persistence of architectural deficits (14). Fascicles may shorten in response to the reduced excursions experienced in the early stages of recuperation. As rehabilitation continues and the athlete returns to more intense training, it might be thought that progressively stronger eccentric contractions would act as a stimulus for sarcomerogenesis (30). However, inhibited muscles may fail to lengthen back to normal if they are minimally activated during active lengthening (26,34). The results of this study are consistent with a theoretical model proposed by Fyfe et al. (14) who proposed that reductions in fascicle lengths persist in those with a history of HSI, even after they return to full training and match play. Such maladaptations may contribute to the reinjury risk that is evident in sport, and it has been argued that fascicles with fewer in-series sarcomeres are more prone to damage caused by the powerful eccentric contractions (6,23).
In the current study, individuals with a unilateral history of HSI displayed no significant differences in muscle thickness when comparing the injured BFlh to the contralateral uninjured BFlh at any of the contraction intensities (Fig. 1C). However, previous investigations using magnetic resonance imaging have shown a significant reduction in muscle volume in those with a history of BFlh strain injury (33), although there are a number of potential explanations for this apparent discrepancy. Firstly, the greater pennation angle may counter any tendency for muscle thickness to be lower in the injured BFlh in comparison to the contralateral uninjured BFlh. As a consequence, some atrophy may have occurred and been effectively masked when muscle thickness was assessed. Secondly, atrophy, if it had occurred, may not be uniform along the length of the injured BFlh. It is known that changes in muscle thickness and anatomical cross-sectional area, after resistance training interventions, are variable along the length of a muscle (4), and there is no reason to suppose that atrophy is more uniform. It is therefore possible that the assessment of muscle thickness in the current study may have occurred at a point of the BFlh where the muscle displays limited atrophy.
Differences in the slopes of the fascicle length–contraction intensity relationships for previously injured and uninjured BFlh (Fig. 1A) suggest differences in tendon–aponeurosis compliance, specifically that the previously injured BFlh may have stiffer tendons and/or aponeurosis than the homonymous muscle in the uninjured limbs. This may be consequent to scar tissue accumulation at the site of the original injury, although it is impossible to rule out the possibility that discrepancies in stiffness may have predated the injuries. Regardless, elevated knee flexor muscle stiffness has been previously associated with an increased risk of HSI (38). Future work should focus on how tendon mechanics are altered after HSI.
The current data indicate that BFlh architectural characteristics are altered as a function of isometric force production. From rest to 75% of MVIC, pennation angle increased from 12.8° to 17.8°, with a concomitant reduction in fascicle length from 10.8 to 8.7 cm in the control group. Using cadaveric data of mean muscle lengths (36,40), the alterations in muscle architecture reported in this study equate to an approximate 14% decrease in muscle length (24). These results suggest that the aponeurosis and tendon of the uninjured BFlh exhibit significant compliance, and this supports the concept that they act as mechanical buffers to reduce the extent of damage caused within the myofibrils during high-intensity eccentric contractions (31). The current data may serve an additional purpose as previous computational models of the human BFlh have used the geometrical data obtained from cadaveric samples to determine variables such as force–length and force–velocity relationships and fiber force production (32,35).
Previous investigations have examined the reliability of ultrasonography to assess BFlh architecture at rest. These studies report a range of ICCs from 0.78 to 0.97 (8,11,30), which, at the upper end, is similar to values reported in the present study. In two of these studies, %TE for the assessment of the BFlh architecture is also reported, with values ranging from 2.15% to 9.7%, with the current study reporting values ranging from 1.6% to 4.9% (11,19). Only one study has investigated the reliability of ultrasonography of the BFlh during an MVIC (100% of maximum); however, the ICC reported was poor (0.78) (11). The current study examined the reliability of the BFlh architecture at 25%, 50%, and 75% of MVIC and found a high reliability of these measures (Table 2). Imaging maximal contractions is difficult because of the inability of participants to maintain a smooth contraction long enough to allow the images to be captured. The combined findings from this article and from previous work (11) suggest that the assessment of BFlh architecture during active contractions is reproducible but not for maximal contractions.
There are limitations in the current study. The validation of the ultrasound assessment technique through the use of cadaveric samples was not undertaken. However, all data obtained at rest are comparable to that in the existing in-vivo literature, which show valid comparisons to cadaveric data (2,3,8,18,19). The comparison of two different cohorts, with elite athletes in the previously injured group and recreationally active participants in the control group, might seem to be a limitation. However, all architectural comparisons show no difference between the control group average and the uninjured limb in the previously injured group, suggesting homogeneity between the groups. Finally, the retrospective nature of the study limits any determinations of whether the reported differences in muscle architecture and eccentric strength are the cause or the result of injury. Prospective investigations are required to determine whether these variables are associated with the risk of sustaining an HSI.
In summary, the current study reported the use of ultrasonography to be highly reliable for the assessment of the BFlh architectural characteristics, at rest and during graded isometric contractions. Furthermore, BFlh absolute fascicle length, pennation angle, and fascicle length relative to muscle thickness as well as knee flexor eccentric force during the Nordic hamstring exercise are all significantly different in those with a previous BFlh strain injury. Whether or not these differences exist before an injury or are a result of the incident, the findings of the current study provide significant insight into architectural asymmetries in previously injured individuals. Much work is required in this area to determine what role, if any, variations in BFlh architecture has in the etiology of HSI.
The authors report that this study was not funded and that no conflict of interest exists. Results of this study do not constitute endorsement of the American College of Sports Medicine.
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