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Original Research

The Use of MRI to Evaluate Posterior Thigh Muscle Activity and Damage During Nordic Hamstring Exercise

Mendiguchia, Jurdan1; Arcos, Asier L.2; Garrues, Mirian A.3; Myer, Gregory D.4,5,6,7; Yanci, Javier8; Idoate, Fernando9

Author Information
Journal of Strength and Conditioning Research: December 2013 - Volume 27 - Issue 12 - p 3426-3435
doi: 10.1519/JSC.0b013e31828fd3e7
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Abstract

Introduction

Hamstring muscle strains are the most prevalent muscle injuries reported in soccer (11–14,19,20). In addition to the prevalence of hamstring injuries, frustration can be intensified by prolonged symptoms, poor healing responses, and a high risk of reinjury at a rate of 12–31% (11,13,14,19,20). When sprinting, the hamstring muscles of the swing leg function concentrically as hip extensors to quickly swing the thigh back, whereas the same muscle group acts eccentrically as knee flexors to decelerate the forward swing leg (40,48). This last action was described as the probable contributing injury mechanism because of the increased peak hamstring musculotendinous stretch, activation, and active lengthening contraction of the hamstring muscles (23,40,41,47,48). The Nordic hamstring (NH) exercise involves the individual athlete kneeling on the ground with his or her ankle fixed, followed by slowly lowering himself or herself to the ground eccentrically contracting hamstring muscles and thought to replicate hamstring function during terminal swing phase. This exercise has been shown to increase both strength (concentric and eccentric) (10,34) and to shift the angle at which the peak torque is produced to a longer length (5,10,29). Together, these may explain why this has been widely and successfully used as a method to prevent hamstring injuries (2,3,6,15,36,37).

Since NH exercise was described in 2001 by Brockett et al. (5), 6 studies have documented the effects of this exercise (2,7,15,17,36,39) on hamstring injuries in elite soccer, rugby, and Australian rules football players. More than 1,000 athletes were monitored in these 6 studies, and each study reported significant reductions in injury rates (2,7,17,36,39). Despite the on-going use and success of NH exercise as a mean of preventing posterior thigh muscle injuries, the effect on site-specific activation of this exercise on different hamstring muscles of the leg is not known.

Magnetic resonance imaging (MRI) may be a sensitive method to display the physiological changes that occur in muscles activated during exercise, as it provides detailed anatomical analysis of associated soft tissues, which is lacking in electromyography experiments (8,18,25,29,30,46). The signal of magnetic resonance images arises from magnetic activity of hydrogen nuclei in tissue water and fat molecules and depends on the sequence parameters selected. Important pulse sequence parameters are repetition time (TR), echo time (TE), and flip angle. Varying the pulse sequence parameters, the images obtained depict differences in the spin-lattice (T1) or in the T2 (spin-spin) relaxation times. It is well known that exercise produces changes in the distribution of water both intracellularly and intercellularly in muscle cells, and this shift in water distribution produces increase in nuclear magnetic transverse (spin-spin) relaxation time (T2) of muscle. The transverse (spin-spin) relaxation time (T2) is a quantitative index of muscle activation and can noninvasively monitor the changes in the amount and distribution of water in skeletal muscle after intensive exercise (8,9). Furthermore, using this technique, detailed information regarding the morphological changes in individual muscles can be obtained by calculating the physiological cross-sectional areas (CSAs) after exercise. In the previous studies, it has been shown that T2 value increased after eccentric exercise (8,9,26,30,33,38,43,44,52). This was positively correlated with plasma creatine kinase activity, reflecting exercise-induced muscle damage (8,30–32,42), especially after the second day after exercise (30). Earlier studies have investigated the nonuniform response of T2 value changes between proximal and distal regions of different muscles after exercise (1,30,33,43). These findings may have interesting implications in terms of the time, course, and effects of different exercises on the hamstrings.

The purpose of this study was to use MRI to investigate muscle damage and intermuscle and intramuscle regional differences in transverse (spin-spin) relaxation time and CSA values at hamstring muscles. Specifically, we aimed to assess morphology and signal intensity changes in the upper thigh muscles using MRI immediately after and then 72 hours after the NH exercise. We hypothesized that (a) the degree of the response after the intensive exercise would be different, as represented by different changes in MRI measurements, such as the CSAs and T2 values, among hamstring muscles with preferentially distal loading pattern, and (b) the hamstring muscle group would demonstrate asymmetrical activation and damage between dominant and nondominant legs. The information derived from this investigation should enable the clinician, strength, and conditioning coach or rehabilitation specialist a better understanding of site-specific activation of the posterior thigh muscles. Specifically, determination of site and limb specific activation and damage can assist in exercise programming with NH, which in turn should guide better practices in injury rehabilitation and selective strengthening of the hamstrings muscles.

Methods

Experimental Approach to the Problem

This study used a repeated-measures research design to investigate the regional-specific differences of MRI measurements in the hamstring muscles after NH exercise in addition to possible differences between extremities. Magnetic resonance imaging of both thighs was performed at different length sections (4,7,8,10,12,14) of muscles’ biceps femoris short head (BFsh), biceps femoris long head (BFlh), semitendinosus (SMT), and semimembranosus (SMM) before, immediately after, and 72 hours after NH eccentric exercise.

Subjects

Eight male national-level soccer referees involved in regular weekly training, supervised by the same strength coach, were invited to participate in this study. Participants were excluded if they had an injury to their legs or back in the past 12 months or if they were unsuitable for MRI because of foreign metal bodies, electronic implants, or claustrophobia. Before the start of the investigation, each participant's height, body mass, age, fat mass, regular exercise program, and any previous injuries to the legs were recorded (Table 1). The participants had previous experience with resistance training for a range between 2 and 4 years and at the time of recruitment were training 4 days per week with previous limited exposure of NH during the year. However, once enrolled into the investigation, they are not allowed to do any NH exercise 8 weeks before the study onset. In addition, subjects were instructed to avoid strength training activities for the lower legs and not to use icing or anti-inflammatory medication for the week preceding and the week of the experiment. The study was approved by hospital's institutional ethics committee and conformed to the Declaration of Helsinki. Each subject (soccer referees) signed an informed consent form before the study and after reading benefits and cons of MRI and eccentric exercise.

T1-25
Table 1:
Physical characteristics of the subjects.*

Exercise Protocol

For the NH exercise, subjects began the movement from a kneeling position on the ground with the ankles fixed (foot neutral) by a partner and were instructed to slowly lower himself (within approximately 4 seconds) to the ground by eccentrically contracting the hamstring muscles without stopping until they reached the ground. Subjects were verbally encouraged to generate maximal force at the starting position and to resist maximally against the knee-extending action as they lower their torso throughout the range of motion while maintaining perfect neutral alignment between trunk and hip joints. When the participant's chest reached the ground, they were instructed to return passively to the initial position using their arms to push themselves back up and avoid concentric action of the posterior chain musculature.

Procedures

The subjects were assigned to the same NH exercise protocol. The protocol involved 5 sets of 8 repetitions with 2-minute rest between sets. Immediately after the completion of the exercise protocol, the subjects were prepared for the MRI scans.

Imaging Technique

All MRI measurements of the thigh were performed using a 1.5-T whole-body imager with surface phased-array coils (Magnetom Avanto; Siemens, Erlangen, Germany). For the MRI scans, subjects were positioned supine with their knee extended. Magnetic resonance imaging of the subjects' thighs was performed immediately before and within 3 minutes after the exercise and repeated 72 hours after. Once the subject was positioned inside the magnet, the thighs of both legs were kept parallel to the MRI table, and the feet were strapped together to prevent rotation. The length of the right femur (Lf), taken as the distance from the intercondylar notch of the femur to the superior boundary of the femoral head, was measured in the coronal plane. Subsequently, 15 axial scans of the thigh interspaced by a distance of 1 of 15 Lf were obtained from the level of 1 of 15 Lf to 15 of 15 Lf. Every image obtained was labeled at its location (i.e., slice 4 being closer to the coxofemoral joint and slice 12 closer to the knee). Great care was taken to reproduce the same individual Lf each time using the appropriate anatomical landmarks as previously described (21). For the final calculation of the signal intensity of each muscle, slices 4 of 15, 6 of 15, 8 of 15, 10 of 15, 12 of 15, and 14 of 15 were used for all muscles examined; the 3 cranial slices (closer to the hip) and the last distal slice (closer to the knee) were discarded because of the presence of image artifacts. T2-weighted transverse spin-echo MR axial images (TR = 3250 ms, TE = 32, 64, and 96 ms) were collected using a 256 × 256 image matrix, with a 320-mm field of view and 10-mm slice thickness.

The MRI data were evaluated to obtain values for anatomical and signal intensity of each hamstring muscle (BFlh, BFsh, SMM, and SMT). The MR images were transferred to a personal computer in the Digital Imaging and Communications in Medicine format and analyzed using image manipulation and analysis software (OSIRIX, University Hospital of Geneva, Switzerland). The same examiner performed the tracings. The CSA was calculated drawing a region of interest by tracing the outline of the muscles, avoiding visible aponeurosis, vessels, fat, membranes, and the femur. The signal intensity was measured from the same region for all 3 TEs. A transverse (spin-spin) relaxation time measurement sequence with 3 TEs was applied to measure the absolute T2 value. Images taken at different TEs were fitted to a monoexponential time curve to extract the T2 values based on the formula: signal intensity = M0 × exp (−TE/T2), where signal intensity represents the signal intensity at a given TE and M0 is the original MRI signal intensity. The percentage of relative change of the average T2 mean value and the CSA of each muscle at each level were calculated. Previous studies have shown high intertester reliability with intraclass correlation coefficients ranging from 0.87 to 0.94, respectively, for T2 measurements (8).

Statistical Analyses

The CSA and T2 absolute values were reported as mean ± SD. The first purpose of the study was to determine changes in absolute values of CSA and T2 of the muscles (SMM, SMT, BFlh, and BFsh) for all different sections (4,7,8,10,12,14) along time (from pre to post, 0–1; from pre to postdelay exercise, 0–2; and from post to postdelay exercise 1–2) at the dominant and at the nondominant limbs.

The intramuscular changes over time of both legs were compared using 1-way analysis of variance (ANOVA) with repeated measures (time with 3 levels pre, post, and postdelay exercise). The second purpose was to determine possible differences between extremities (dominant vs. nondominant) used in this bilateral exercise. The second comparison of interest was the interlimb pre, post, and post-delete changes in absolute values of CSA and T2 of the muscles (SMT, SMM, BFlh, and BFsh) for all the different sections (4,7,8,10,12,14). To disentangle the main effects, a 2-factor (time × muscle section) repeated-measures ANOVA was used; time has the same 3 levels and all muscle sections have 2 levels: dominant and nondominant limbs. Paired t-tests were used to determine significant pre-exercise differences between the dominant and nondominant limbs. Statistical significance was set at p < 0.05. At CSA values, group sample sizes of 8 and 8 achieve 100% power to detect a difference of 1,000 in a design with 3 repeated measurements having a compound symmetry covariance structure when the SD is 0.50. For T2 values, group sample sizes of 8 and 8 achieve 100% and over 95% power to detect a difference of 6,000 to 16 by 4 in a design with 3 repeated measurements having a compound symmetry covariance structure when the SD is 0.25–10.00 by 5. After the statistical analysis, each statistical significant result was assessed for power. Statistical power of the study was greater than 80% (from 82.2 to 100%), and all results less than 80% were excluded. We tested the bidirectional hypothesis that mean change could be positive or negative.

Results

Typical T2 of the dominant and nondominant limbs pre- and postdelay exercise can be observed in Figure 1. Statistical differences (p = 0.03) were found in CSA of BFsh at section 10 between dominant (3.70 ± 0.86) and nondominant limbs (2.64 ± 0.91) at the beginning of the study. Significant differences were also found in T2 at SMT in sections 10 (p = 0.04) and 12 (p = 0.03) between dominant (40.50 ± 2.11 and 44.19 ± 4.11) and nondominant limbs (43.07 ± 2.29 and 51.69 ± 7.55), respectively. The changes in absolute values for CSA technique pre, post, and post delay exercise of the different muscles (SMT, BFsh, and BFlh) from sections 4–14 for the dominant and nondominant limbs can be observed in Tables 1 and 2 and in Figures 2–5. The following is a summary of the main findings from these results.

F1-25
Figure 1:
Representative T2-weighted magnetic resonance images obtained at Lf10 level before (A), immediately after (B), and 72 hours (C) after the nordic hamstring eccentric exercise. The bright areas of the dominant left (arrowheads) and nondominant right biceps femoris short head (arrows) muscles for the images obtained 72 hours after the exercise persists on areas with increased T2 times. Notice the visible asymmetry in cross-sectional area and signal intensity increases between the dominant and nondominant legs.
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Table 2:
Inter- and intralimb changes in cross-sectional areas of BFlh.*
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Figure 2:
Biceps femoris short head changes intramuscle and interlimb in cross-sectional areas. Intramuscle significant differences, p < 0.05. * = from pre to post exercise; # = from pre to post-delay exercise.
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Figure 3:
Semitendinosus changes intra- and intermuscle in T2. Intramuscle significant differences, p < 0.05. * = from pre to post exercise and # = from post to post delay exercise. Intermuscle significant differences, δ = at pre-exercise; δδ = postexercise; and δδδ = postdelay exercise.
F4-25
Figure 4:
Biceps femoris long head changes intra- and intermuscle in T2. Intramuscle significant differences, p < 0.05. * = from pre- to postexercise. Intermuscle significant, δδ = at postexercise.
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Figure 5:
Biceps femoris short head changes intramuscle and interlimb in T2. Intramuscle significant differences, p < 0.05. * = from pre- to postexercise; # = from pre- to postdelay exercise.

Cross-sectional Area

In terms of SMT and SMM CSA, no significant changes were found in intramuscle or intermuscle in any section or time period. No significant differences were found related to BFlh CSA at the dominant and nondominant limbs in any section or time period, despite significant changes observed between dominant and nondominant limbs at section 10 at pre-exercise (p = 0.012) and postexercise (p = 0.010). These differences disappeared at 72 hours (p = 0.055) (Table 2). Significant differences were found related to BFsh CSA at the dominant and nondominant limbs in section 10. At the nondominant limb from pre- to postexercise (approximately 36%, p = 0.025) and at the dominant and nondominant limbs, respectively, from pre- to postdelay exercise (approximately 30 and 64%, p = 0.035 and p = 0.015). No significant changes were observed between the dominant and nondominant limbs in any section or time period (Figure 2).

Transverse Relaxation Signal Intensity

For the SMT, significant changes (approximately 13–19%) in the T2 values for the dominant limb from pre- to postexercise at sections 8 (p = 0.003) and 10 (p = 0.002) were identified (Figure 3). At nondominant limb, significant increases (approximately 14–20%) were found from pre- to postexercise at the same sections (at section 8, p = 0.002 and at section 10, p = 0.002), where it was also found to be significantly decreased (approximately 10, p = 0.004) from pre- to postdelay at section 10 (Figure 2). The changes found differed significantly within limbs at sections 8 (at postexercise, p < 0.008) and 10 (at pre-exercise, p = 0.002; postexercise, p = 0.001; and postdelay exercise, p = 0.000) (Figure 3).

No significant changes were found at SMM related to T2 neither intramuscle nor intermuscle in any section or time period. Significant T2 changes of BFlh were found at the nondominant limb measurement from pre- to postexercise (at sections 10 and 12 of approximately 6–7%; Figure 4). There were also significant differences between the dominant and nondominant limbs at section 10 that increased at 72 hours after exercise execution (p = 0.002) (Figure 4).

Significant T2 changes of BFsh at the dominant limb were found distally into the muscle at section 14 (p = 0.036) from pre- to postexercise. Although the nondominant limb found significant changes from pre- to postexercise at sections 10 (p = 0.016) and 14 (p = 0.010), there were also found significant changes (p = 0.017) from pre- to postdelay exercise at section 10 (approximately 23%), while there was not a intermuscle significant difference in any period or section (Figure 5).

Discussion

This study examined the differences of changes in MRI measurements, represented as CSA and T2 values, among hamstring muscles before and after NH exercise. Results showed that almost all the hamstring muscles, except SMM, exhibited a T2 increase immediately following NH exercise. Kubota et al. (30) suggested that the T2 increase that occurred immediately after eccentric leg curl exercise (ELC) reflects the increased blood flow and that the increase that occurred after the second day after exercise reflects severe muscle damage.

Conversely, the BFsh presented an increase of CSA and T2 values after the exercise and on the third day (72 hours after) after. Therefore, these results confirm our first hypothesis that the loading patterns of each hamstring muscle would be nonuniform with preferentially distal damaged pattern. Specifically, the current data indicate that the degree of response during eccentric NH exercise was not uniform among the hamstring muscles, and the distally located BFsh cranial (close to its origin) muscle region might be more sensitive to the tested movement as it is selectively damaged to a greater extent.

It is generally considered that the hamstring muscles are similarly activated during knee flexion exercise. However, results of this study showed that the BFsh muscle was particularly altered after the eccentric exercise as indicated in the MRI measurements. The rationale behind the selective damage of this muscle was that the morphological property and architectural characteristics of this muscle is such that it can effectively deal with the strain during NH exercise.

BFsh is a uniarticular hamstring muscle that crosses only knee joint and was found to have long fascicular length and the smallest physiological cross-sectional area in comparison with the other hamstring muscles (4,16,50,51). Therefore, and according to its architectural design, functional capacity of BFsh muscle is to generate forces over large length changes and can be categorized as an excursion muscle.

Because of its location, it has been suggested that BFsh contributes to knee joint flexion, together with BFlh. However, BFlh research has shown that changes in the fascicle length are more sensitive to changes in hip position with the knee position constant than to changes in knee position with the hip position constant (22,49). This difference may be related to the larger muscle moment arm at the hip resulting in greater excursion of the muscle with changing hip position. This can explain greater BFsh changes in signal intensity and CSA after NH exercise, where knee flexion excursion is high while hip and trunk are fixed, whereas no changes in the BFlh were seen after 72 hours. The fact that both biceps presented different nerve supplies could be another explanation.

Recently, different authors (30,31,33) have considered that SMT is selectively recruited and damaged in open kinetic chain knee flexion to accomplish eccentric knee flexion exercise during ELC. A possible explanation of the selective recruitment patterns of 2 different eccentric knee flexion exercises is the consideration of the fixed body parts in each of the exercises. During the NH exercise, the movement occurs at the thigh while the tibia remains fixed. In contrast, during the eccentric leg curl exercise, the femur is more fixed while the tibia is in motion.

BFsh presents architectural partitions and innervation patterns (50) and probably relates to the proposed functions of the muscle and its concrete proximal damage pattern (section 10) compared with distal (sections 12 and 14) during NH exercise.

As defined by attachment sites, fascicle orientation, and nerve supply, BFsh comprises 2 anatomical regions (cranial and caudal) (51) (Figure 6). Concretely, section 10 of BFsh shows increased signal intensity corresponding with fascicles of cranial region (closer to its origin) of the muscle with origin in the medial wall of the lateral intramuscular septum. In contrast, fascicles constituting more caudal region (closer to its insertion) that typically originated deep to those of superior region, arising from both the ventral aspect of the medial wall of the lateral intermuscular septum and from the linea aspera (51), do not show signal intensity changes. In comparison with the fascicles in superior region, these were oriented at an acute angle, passing posteriorly, inferiorly, and slightly laterally toward their distal insertion site (Figure 6).

F6-25
Figure 6:
Representative axial magnetic resonance imaging T2-weighted images obtained at the cranial (Lf10), middle (Lf12), and distal (LF14) levels of the left biceps femoris short head showing heterogenous increase in signal intensity (arrowheads) 72 hours after the nordic hamstring exercise. Modified and reprinted with permission of the publisher from Woodley, SJ and Mercer, SR. Hamstring muscles: Architecture and innervation. Cells Tissues Organs 179: 125–41, 2005. *Indicates areas without increased signal intensity within the biceps femoris short head muscle.

These results may lead to a better understanding of the role that BFsh has in movements at the knee joint and also how it functions in relation to BFlh, particularly as both muscles receive different nerve supplies. This can explain the hypertrophy found in the short head of the biceps femoris after diagnosing BFlh injury (45) and atrophy, as a possible compensation, which is enabled by the separate innervations of the long and short heads with training from this exercise. Specifically by allowing overall knee flexion strength preservation to prevent hamstring muscle injuries, especially during the late swing phase of sprinting where hamstring muscles needs to contract as knee flexors to decelerate the forward tibia.

In respect to our second hypothesis, this study shows greater significant intermuscular changes related to crosssectional areas and T2 signal intensity in the nondominant hamstring muscles in contrast to the dominant limb. Interlimb analysis revealed significant transverse (spin-spin) relaxation time signal intensity changes between the dominant and nondominant limbs at specific sections or time period of BFlh (section 10) and SMT (sections 8 and 10). This fact confirms our primary hypothesis that the damage patterns of each hamstring muscle would be nonuniform with preferentially distal recruitment pattern and suggest that NH exercise creates asymmetrical and nonuniform loading pattern between legs.

This result may be due mainly to 2 reasons: subjects can be supported or load more the nondominant leg during the exercise and/or, on the other hand, nondominant leg may be less adapted to the eccentric exercise than the dominant leg by reflecting changes to greater intensity. In this line, Clark et al. (10) reported that after 4 weeks of training with the NH, the asymmetry in the angle where peak torque is produced is increased. Although the NH has been shown able to successfully reduce hamstring injuries and concomitantly increase both strength and optimum length, the results of this study showed different activation patterns between limbs during its realization.

Practical Applications

This study used MRI to assess the relative damage to lower leg muscles after NH exercise. Despite the fact that different exercises can increase hamstring strength (24,27), various hamstring exercises do not result in a uniform response (training stimulus) for the same muscles and regions. From the results of this study and previous findings, it can be concluded that when the goal of a therapeutic intervention is to specifically strengthen the BFlh and SMM, hip dominant exercises such as deadlifts or lunges may be indicated to support the desired adaptations from training (33,35). In contrast, a progressive resistive training program that incorporates ELC or NH may be indicated as these exercises selectively and effectively activate and damage the SMT and BFsh muscles, respectively (33).

In conclusion, this study demonstrates that the NH exercise not only has the ability to increase strength and optimum length of hamstring muscles (5,10,28,34) but also is better suited for loading cranial BFsh muscle.

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Keywords:

eccentric; hamstring strengthening; hamstring strain; injury prevention; region-specific difference

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