Abstract
Objective
The purpose of this study was to investigate the relationship between hamstring flexibility and electromyography (EMG) muscle parameters in back and lower limb extensor muscles during a trunk flexion task.
Methods
Thirty healthy women aged 18 to 30 years with normal hip movement were recruited for this study. Hamstring muscle flexibility was measured with the 90-90 active straight leg raise test. Surface EMG activities were simultaneously recorded from the lumbar erector spinae, gluteus maximus, biceps femoris, semitendinosus, lateral gastrocnemius, and medial gastrocnemius muscles during forward bending. Muscle activity onset and offset, amplitude, and duration were calculated with technical computer software (MATLAB, version 1.6.0). Linear regression analysis was used to investigate the relationships between hamstring flexibility test results and EMG parameters during trunk flexion. In addition, the Friedman test was used to determine the recruitment activity pattern in women with low versus normal hamstring flexibility.
Results
During flexion, the back extensor muscles in individuals with lower hamstring flexibility test scores were activated and deactivated later, which can lead to delayed flexion-relaxation. Regression analysis did not disclose any significant correlations between hamstring flexibility and other EMG parameters (duration and amplitude) in back extensor muscles. Activation and deactivation recruitment patterns differed between the groups with normal and low hamstring flexibility.
Conclusion
The findings of this study suggest that hamstring flexibility plays an important role in the patterns of trunk and lower limb muscle activity onset, offset, and recruitment.
Key Indexing Terms: Electromyography
Introduction
Lumbar spine movements are controlled by a complex neuromuscular system involving both active (muscle) and passive components (vertebral bones, intervertebral disks, ligaments and fascia).1 Forward trunk bending is a common lumbar movement during daily living and sport activities.2 Biomechanics specialists and clinicians usually use electromyography (EMG) activity of the trunk muscles to assess lumbar spine function.2 Floyd and Silver investigated the function of the erector spinae during trunk flexion and extension with EMG techniques and reported complete relaxation of the erector spinae muscles in full trunk flexion (flexion-relaxation), which can cause rupture of the annulus fibrosus and intervertebral ligaments during trunk flexion.3
Flexibility is defined as the ability to extend the muscles through the complete joint range of motion.4 The hamstring muscle has an important role during functional activities such as high-speed running or sprinting and tends toward shortening among general populations and athletic ones.5 Restricted anterior pelvic rotation has been demonstrated in healthy individuals with poor hamstring flexibility (owing to the muscle's attachment to the ischial tuberosity).6,7 Regarding lumbopelvic rhythm, hamstring muscle tightness can apply additional loads and stress on the lumbar spine and thus indirectly affect spinal lordosis and kinematics.6 A systematic review has reported that decreases in hamstring flexibility can predict the development of low back pain.8 Also, Esola et al have reported that improving hamstring flexibility may allow greater hip motion and less stress on the lumbar spine during forward bending.9 In another study, Hashemirad et al proposed that the EMG activity pattern of the erector spinae muscles may be influenced by general and lumbar spine flexibility in healthy subjects. They reported that different flexibilities were associated with altered neuromuscular responses of the erector spinae muscles during a flexion-extension task and that individuals with greater general and lumbar flexibility had shorter flexion-relaxation periods.10 Although that study investigated the relationship between lumbar flexibility and EMG activity patterns in the erector spinae muscles during trunk flexion-extension, to our knowledge the relationship between lower extremity (hamstring) flexibility and EMG patterns in the back and lower limb muscles during dynamic trunk flexion tasks has not been investigated. Therefore, we hypothesized that if hamstring flexibility decreased, the pattern of EMG activity of the trunk and lower limb muscles would alter during a dynamic trunk forward flexion task. Regarding this issue, reduced hamstring muscle length may make healthy individuals more susceptible to the development of musculoskeletal disorders such as low back pain.
Materials and Methods
Participants
Thirty healthy female college students aged 18 to 30 years with normal hip movement were recruited from Shiraz University of Medical Science. The sample size calculation was determined based on a pilot study. Then using MedCalc software, with α = 0.05, β = 0.2, and power of 80%, a total sample size of 30 subjects was estimated in each group before the study commenced. The exclusion criteria were history of spinal or lower extremity pain or surgery, metabolic and neuromuscular diseases, and neurologic or orthopedic signs. All participants signed an informed consent form approved by the Ethics Committee of Shiraz University of Medical Sciences.
Instrumentation
Seven pairs of disposable surface silver/silver chloride electrodes (Medico Electrodes International Ltd, Noida, India) were used to collect EMG data (ME6000-Telemetry EMG, Kuopio, Finland) from the sampled muscles (Table 1). The data were amplified by 1000 with a bandpass frequency of 8 to 500 Hz, gain of 100 µv/div, and common mode rejection ratio of 110 dB; they were then digitized and stored with a 14-bit analog-to-digital converter.10 The sampling rate for all recordings was 1000 Hz.10
Table 1.
Electromyography Electrode Positioning
| Muscle | Position |
|---|---|
| Erector spinae | At the L3-4 level over the right erector spinae musculature (about 4 cm lateral from midline)10 |
| Gluteus maximus | 34% of the distance from the second sacral vertebra to the greater trochanter, starting from the second sacral vertebra11 |
| Biceps femoris | 35% of the distance from the ischial tuberosity to the lateral side of the popliteal fossa, starting from the ischial tuberosity11 |
| Semitendinosus | 36% of the distance from the ischial tuberosity to the medial side of the popliteal fossa, starting from the ischial tuberosity11 |
| Lateral gastrocnemius | 61% of the distance from the lateral side of the popliteus cavity to the lateral side of the Achilles tendon insertion, starting from the Achilles tendon11 |
| Medial gastrocnemius | 50% of the distance from the medial side of the popliteal fossa to the medial side of the Achilles tendon insertion, starting from the Achilles tendon11 |
Experimental Procedures
Hamstring flexibility measurement and electrode placement were done sequentially. To measure hamstring flexibility, the 90-90 active straight leg raise test was performed.12 Participants lay in supine position, with their hips in 90° flexion and knees bent, and the examiner grasped their legs behind the knees and stabilized the thigh in this position. Then the participants actively extended each knee, and the knee angle was measured. Knee angles smaller than 20° were considered to indicate normal hamstring flexibility, and knee angles greater than 20° were considered to indicate low hamstring flexibility.12
Before electrode placement, the areas were shaved, cleaned, and abraded with an alcohol pad to ensure good surface contact and low skin impedance. The surface electrodes were placed longitudinally over 7 muscles on the side of the body with low hamstring flexibility. Interelectrode center-to-center distance was 2.5 cm, and all electrodes were placed parallel to the muscle fibers.10 The muscles sampled and locations of the electrodes are listed in Table 1.
The participants were instructed to stand barefoot on the platform with their feet at shoulder width, their knees straight, and their gaze directed forward. They were then asked to bend their trunk forward as far as possible until the tip of the fingers reached the ground at a natural speed (neither too fast nor too slow) when they heard an auditory signal.13 The pattern of the movement during trunk flexion was checked visually by the same examiner, and the participant counted the numbers from 1 to 5 during the trunk flexion task.
When they reached the end point of forward flexion (static phase of the task) they were asked to hold this position for 5 seconds. Three trials with a 1-minute interval between were recorded. Maximum voluntary contraction (MVC) of all muscles was calculated for amplitude normalization. In this study, MVC is defined as the maximum force that can be produced with isometric contraction.14 Each test was repeated 3 times, and the best of the 3 efforts in a single test session was considered the MVC. The protocol for MVC measurement of each muscle was as follows14:
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Gluteus maximus: hip extension, hip flexed 90° (prone)
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Lateral hamstring (bicepts femoris) and medial hamstring: prone, with the knees in 30° flexion
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Lateral gastrocnemius: ankle plantar flexion, with the ankle, knee, and hip in neutral position (prone)
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Medial gastrocnemius: ankle plantar flexion, with the ankle in neutral position (prone)
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Erector spinae: back extension (prone)
Data Processing
The raw data were filtered with a bandpass filter of 20 to 450 Hz.15 The onset of muscle EMG activity (beginning of activation or inhibition) was defined as the moment when EMG amplitude was greater or smaller than the mean ± 2 standard deviations of baseline activity for at least 50 milliseconds.16 Muscle activity onset and offset, amplitude, and duration were determined with technical computer software (MATLAB, version 1.6.0). Muscle activity amplitude was normalized by MVC.
Statistical Analysis
Normality of the data was checked with the Kolmogorov-Smirnov test (P > .05). Multiple linear regression analysis was used to investigate the relationships between hamstring flexibility test results and EMG parameters. For further comparisons, the participants were divided into 2 groups—low and normal hamstring flexibility—and the Friedman test was used to characterize recruitment activity patterns in both groups.17 The alpha level was set at 0.05, and SPSS version 19.0 software (IBM Corp., Armonk, NY) was used for all statistical analyses.
Results
Thirty healthy female college students participated in this study; their mean (± SD) age was 23.3 ± 3.4 years, height was 162 ± 5.5 cm, body weight was 56.1 ± 7.6 kg, and body mass index was 21.3 ± 2.5 kg/m2. The relationships between hamstring flexibility and EMG parameters (onset and offset, amplitude, and duration) are shown in Tables 2, 3, and 4, respectively. Regression analysis showed a positive relationship between hamstring flexibility and EMG characteristics (onset and offset) in the back and lower limb muscles (Table 2). Muscle activation and deactivation were delayed in women with low hamstring muscle flexibility. After muscle ranking, it was shown that activation and deactivation recruitment patterns differed between the groups with normal and low hamstring flexibility (Fig 1): medial muscles (semitendinosus and medial gastrocnemius) activated earlier and deactivated later than lateral muscles (biceps femoris and lateral gastrocnemius) in the low flexibility group. In this study, it seems that medial muscles play the more important role in stability. As shown in Tables 3 and 4, there were no significant correlations between hamstring flexibility and EMG amplitude or duration.
Table 2.
Results of the Linear Regression Analysis of the Association Between the Active Straight Leg Raise Test and Electromyography Onset and Offset Activity
| Unstandardized B coefficient |
|||||
|---|---|---|---|---|---|
| Variable | B | SD | P | R2 | Model |
| Constant ASLR Constant ASLR Constant ASLR Constant ASLR Constant ASLR Constant ASLR Constant ASLR Constant ASLR Constant ASLR Constant ASLR Constant ASLR Constant ASLR |
−1.820 0.029 −0.457 0.033 −1.774 0.027 −0.084 0.019 −2.052 0.041 −0.044 0.028 −1.921 0.035 0.359 0.008 −1.642 0.036 0.255 0.035 −1.494 0.029 0.128 0.042 |
0.275 0.012 0.344 0.015 0.268 0.012 0.347 0.015 0.375 0.016 0.381 0.017 0.368 0.016 0.340 0.015 0.260 0.011 0.292 0.013 0.221 0.010 0.328 0.014 |
<.001 .022a .195 .037a <.001 .031a .810 .323 <.001 .019a .909 .100 <.001 .040a .301 .584 <.001 .004a .389 .011a <.001 .006a .700 .007a |
0.173 0.146 0.155 0.051 0.181 0.093 0.142 0.011 0.261 0.212 0.243 0.231 |
ES onset −1.820 +0.029 (ASLR) ES offset −0.457 +0.033 (ASLR) GMax onset −1.774 +0.027 (ASLR) GMax offset BF onset −2.052 +0.041 (ASLR) BF offset ST onset −1.921 +0.035 (ASLR) ST offset LG onset −1.642 +0.036 (ASLR) LG offset −0.255 +0.035 (ASLR) MG onset −1.494 +0.029 (ASLR) MG offset 0.128 +0.014 (ASLR) |
ASLR, active straight leg raise; BF, biceps femoris; ES, erector spinae; GMax, gluteus maximus; LG, lateral gastrocnemius; MG, medial gastrocnemius; SD, standard deviation; ST, semitendinosus.
Indicates statistical significance.
Table 3.
Results of the Linear Regression Analysis of the Association Between the Active Straight Leg Raise Test and Electromyography Amplitude
| Unstandardized B coefficient |
|||||
|---|---|---|---|---|---|
| Variable | B | SD | P | R2 | Model |
| Constant ASLR Constant ASLR Constant ASLR Constant ASLR Constant ASLR Constant ASLR |
0.393 0.008 0.314 0.005 0.198 0.004 0.205 −2.221 0.338 0.002 0.415 0.005 |
0.163 0.007 0.176 0.008 0.075 0.003 0.048 0.002 0.117 0.005 0.176 0.008 |
.023 .255 .085 .559 .014 .257 <.001 .992 .007 .767 .026 .529 |
0.046 0.012 0.046 0.000 0.003 0.014 |
ES amplitude GMax amplitude BF amplitude ST amplitude LG amplitude MG amplitude |
ASLR, active straight leg raise; BF, biceps femoris; ES, erector spinae; GMax, gluteus maximus; LG, lateral gastrocnemius; MG, medial gastrocnemius; SD, standard deviation; ST, semitendinosus.
Table 4.
Results of the Linear Regression Analysis of the Association Between the Active Straight Leg Raise Test and Electromyography Duration
| Unstandardized B coefficient |
|||||
|---|---|---|---|---|---|
| Variable | B | SD | P | R2 | Model |
| Constant ASLR Constant ASLR Constant ASLR Constant ASLR Constant ASLR Constant ASLR |
1.363 0.004 1.690 −0.008 2.008 −0.012 2.279 −0.026 1.898 −0.001 1.622 0.013 |
0.235 0.010 0.231 0.010 0.393 0.017 0.354 0.016 0.326 0.014 0.331 0.014 |
<.001 .708 <.001 .430 <.001 .474 <.001 .100 <.001 .957 <.001 .390 |
0.005 0.022 0.018 0.093 0.000 0.027 |
ES duration GMax duration BF duration ST duration LG duration MG duration |
ASLR, active straight leg raise; BF, biceps femoris; ES, erector spinae; GMax, gluteus maximus; LG, lateral gastrocnemius; MG, medial gastrocnemius; SD, standard deviation; ST, semitendinosus.
Fig 1.
Mean rank of activation and deactivation pattern in 2 groups of hamstring flexibility. BF, biceps femoris; ES, erector spinae; Gas. Lat, lateral gastrocnemius; Gas. Med, medial gastrocnemius; Gl. Max, gluteus maximus; Semi, semitendinosus.
Discussion
The results of the present study show that differences in hamstring flexibility were associated with difference in EMG activity onset in all extensor muscles, and with differences in offset in the erector spinae and gastrocnemius muscles. Regression analysis showed that in the group with low hamstring muscle flexibility, muscle activation and deactivation were delayed. This finding is in line with earlier findings published by Dolan and Adams18 and Hashemirad et al.10
Muscle hypoactivity is characterized by delayed, decelerated, or reduced contraction.19 By lowering hamstring muscle flexibility, pelvic anterior tilt may lead to hypoactivity in the gluteus maximus muscle. Because of the connection between the gluteus maximus and spinal extensor muscles via the thoracolumbar fascia, gluteus maximus hypoactivity can lead to erector spinae deconditioning. As a result, flexion-relaxation is delayed and the hypoactivated muscles may exert an additional load on the vertebral spine, which in turn can cause low back pain (LBP). In other words, weakening and decreased activity of the gluteus maximus can cause excessive activity of the erector spinae in performing functional movement.20 As a result, the erector spinae muscle hyperactivity due to gluteus maximus hypoactivity can increase the stress on the lumbar spine. This poor biomechanical relationship can gradually develop LBP. However, our findings are inconsistent with the results of Vogt et al, who reported earlier onsets in the lumbar spine and hip extensors during walking in persons with LBP. The discrepancies may be due to the maintenance of spinal stability in the presence of pain.21
Our regression analysis did not disclose any significant correlations between hamstring flexibility and the two other EMG parameters investigated here (duration and amplitude) in the back extensor muscles. Our results were inconsistent with the findings of Shin et al,22 who reported lower flexibility and lower amplitude during isometric trunk flexion in healthy men. The differences between these results may be attributable to the nature of the activity performed: participants in the former study performed a static activity, whereas the task performed in the present study was dynamic. Our results showed that in the group of women with normal hamstring flexibility, the gluteus maximus muscle was activated after the erector spinae, biceps femoris, and semitendinosus muscles, and deactivated before them during forward flexion. Sahrmann23 hypothesized that the erector spinae, hamstring, and gluteus maximus muscles were activated sequentially during forward flexion in healthy people. That study showed that the gluteus maximus and biceps femoris were activated earlier and deactivated later in its group with low hamstring flexibility. With respect to the earlier activation and later deactivation of the hip extensor muscles (gluteus maximus and hamstring muscles) in comparison to the erector spinae, the hip extensor muscles may actively brace the back longer than the erector spinae during forward bending. Vleeming et al proposed that the gluteus maximus is a hip extensor muscle that is connected with the lumbar paraspinal and hamstring muscles via the thoracolumbar fascia and the sacrotuberous ligament.24 The gluteus maximus thus plays an important role in transferring the load from the lumbar spine to the lower limbs and in compressing the sacroiliac joint.25 In the present study, early activation of the hamstring muscles in the group with low hamstring flexibility may be an alternative strategy to maintain lumbopelvic stability, which can in turn impair load transfer and cause LBP. Sakamoto et al26 showed that the early onset of hamstring muscle activity in individuals with sacroiliac joint dysfunction can be a compensatory mechanism for gluteus maximus weakness. In this connection, they suggested that because of its role in sacroiliac joint stability, weakness of the gluteus maximus can lead to LBP, and they showed that the early onset of hamstring muscle activity in individuals with sacroiliac joint dysfunction can be a compensatory mechanism for gluteus maximus weakness.26 According to the compressive load of the hamstring muscles on the sacroiliac joint, early activation of the hamstring muscles in the healthy group with low hamstring flexibility can apply an additional compressive load that can cause motor control impairments and LBP as time passes.
Limitations
This study has some limitations. First, there is no device to control the speed of movement during the trunk flexion task. Second, the results of this study cannot be generalized to men, because only women were recruited. Third, the hamstring muscle flexibility was investigated in healthy subjects without pathology; investigation of hamstring flexibility among groups with different athletic ability or musculoskeletal disorders, including LBP, may be suggested in future studies.
Conclusion
The findings of this study suggest that hamstring flexibility plays an important role in the patterns of trunk and lower limb muscle activity onset, offset, and recruitment.
Acknowledgments
Acknowledgements
We thank K. Shashok (AuthorAID in the Eastern Mediterranean) for improving the use of English in the manuscript.
Funding Sources and Conflicts of Interest
We appreciate the financial support from the Rehabilitation Faculty of Shiraz University of Medical Sciences and Health Services. The authors report no conflict of interest.
Contributorship Information
Concept development (provided idea for the research): S.N.
Design (planned the methods to generate the results): S.N., S.P., S.T.
Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): S.P., S.T.
Data collection/processing (responsible for experiments, patient management, organization, or reporting data): S.N.
Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the results): S.P., S.T., L.H.
Literature search (performed the literature search): S.N., L.H.
Writing (responsible for writing a substantive part of the manuscript): S.P., S.T., L.H.
Critical review (revised manuscript for intellectual content, this does not relate to spelling and grammar checking): S.P., S.T., L.H.
Practical Applications.
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The findings of this study highlight the importance of hamstring muscle length on electromyographic activity patterns of the trunk and lower limb muscles that should be taken into consideration as a potential contributing factor to motor control deficiencies.
Alt-text: Unlabelled box
References
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