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ISSN : 1225-8962(Print)
ISSN : 2287-982X(Online)
Physical Therapy Korea Vol.24 No.4 pp.1-10
DOI : https://doi.org/10.12674/ptk.2017.24.4.001

Comparison of the Flexion-Relaxation Ratio of the Hamstring Muscle and Lumbopelvic Kinematics During Forward Bending in Subjects With Different Hamstring Muscle Flexibility

Chang-ho Kim1, Gyeong-tae Gwak1, Oh-yun Kwon2,3
1Dept. of Physical Therapy, The Graduate School, Yonsei University
2Dept. of Physical Therapy, College of Health Science, Yonsei University
3Dept. of Ergonomic Therapy, The Graduate School of Health and Environment, Yonsei University
Corresponding author : Oh-yun Kwon kwonoy@yonsei.ac.kr
July 18, 2017 July 18, 2017 October 26, 2017

Abstract

Background:

Flexion-relaxation phenomenon (FRP) was a term which refers to a sudden onset of myoelectric silence in the erector spinae muscles of the back during standing full forward flexion. Hamstring muscle length may be related to specific pelvic and trunk movements. Many studies have been done on the FRP of the erector spinae muscles. However, no studies have yet investigated the influence of hamstring muscle flexibility on the FRP of the hamstring muscle and lumbopelvic kinematics during forward bending.

Objects:

The purpose of this study was to examine the flexion-relaxation ratio (FRR) of the hamstring muscles and lumbopelvic kinematics and compare them during forward bending in subjects with different hamstring muscle flexibility.

Methods:

The subjects of two different groups were recruited using the active knee extension test. Group 1-consisted of 13 subjects who had a popliteal angle under 30°; Group 2-consisted of 13 subjects who had a popliteal angel above 50°. The kinematic parameters during the trunk bending task were recorded using a motion analysis system and the FRRs of the hamstring muscles were calculated. Differences between the groups were identified with an independent t-test.

Results:

The subjects with greater hamstring length had significantly less lumbar spine flexion movement and more pelvic flexion movement. The subjects with greater pelvic flexion movement had a higher rate of flexion relaxation during full trunk bending (p<.05).

Conclusion:

The results of this study suggest that differences in hamstring muscle flexibility might cause changes in people’s hamstring muscle activity and lumbopelvic kinematics.


초록


    Introduction

    The hamstring muscle complex is composed of three muscles that arise from part of the ischial tuberosity. Hamstring shortness is a common finding in low back pain (LBP) patients (Nourbakhsh et al, 2002). Hamstring muscle extensibility may be associated with specific pelvic and trunk postures (Gajdosik et al, 1994). Because the hamstring muscles originate on the ischial tuberosity of the pelvis, a decreased extensibility will affect the range of motion and posture of the pelvis (Congdon et al, 2005; Dewberry et al, 2003). Decreased hamstring muscle extensibility reduces the pelvic flexion range of motion during forward bending movement with the knees straight (Gajdosik et al, 1992).

    Pelvic flexion range has been suggested to be related to LBP due to the anatomical proximity of the pelvic and lumbar areas, and many authors interested in LBP have examined the association between the pelvic and lumbar areas (Harris-Hayes et al, 2009). Inadequate pelvic mobility is related to greater LBP severity (Mellin, 1988). Restricted pelvic flexion movement can be a risk factor that contributes to musculoskeletal pain syndromes, and alters mechanical forces, possibly leading to overstress in the lumbopelvic area (Ellison et al, 1990; Shum et al, 2007; Wong and Lee, 2004). Previous studies have highlighted the relationship between active pelvic flexion and LBP (Childs et al, 2004; Cibulka et al, 1998; Cibulka, 1999; Ellison et al, 1990; Fairbank et al, 1984; Flynn et al, 2002; Mellin, 1990). Several investigators have proposed that hip range of motion (ROM) measurements should be involved in studies with interventions targeting the lumbar vertebrae (Flynn et al, 2002; Hicks et al, 2005). Forward bending activities done by individuals with greater flexibility in the lumbopelvic area than in the hip joint will lead to compensatory lumbar flexion at the relatively flexible lumbopelvic area (Sahrmann, 2002).

    The term flexion-relaxation phenomenon (FRP) was coined by Floyd and Silver (Floyd and Silver, 1955) to depict the tendency of the low back muscle to activate as an individual moves to bend forward, be quiet during full flexion, and reactivate during body extension, subsequently bringing the back to an upright standing posture (Schinkel-Ivy et al, 2014). The FRP has been known as a sign of lumbar neuromuscular alterations caused by LBP (Alschuler et al, 2009; Shirado et al, 1995). In the full flexion posture, the body weight is assisted mainly by a passively generated extension moment from the spinal ligaments, intervertebral discs, and passive components of the extensor muscle-tendon units (McGill. and Kippers, 1994). This process involves the shift of the play of the extension moment generator from the active component (muscle tissue) to the passive component (ligaments, discs and fascia) (Ning et al, 2011). In addition, recent research has reported that the FRP takes place during lifting (Dolan et al, 1994; Mathieu and Fortin, 2000; Toussaint et al, 1995), lateral bending (Raftopoulos et al, 1988), and sitting (Callaghan and Dunk, 2002). The FRP is changed by many factors, including the magnitude of applied load (Schultz et al, 1985), and the loading rate (Sarti et al, 2001), and differences have been announced between low back pain and healthy subjects (Ahern et al, 1988; Golding, 1952; Shirado et al, 1995). The FRP is also modified due to repeated trunk bending (Dickey et al, 2003). It was also found that an increase in knee flexion can decrease tension on the lumbar posterior tissues and result in a lag of the lumbar erector spinae muscle’s FRP (Shin et al, 2004).

    Eccentric hamstring actions are associated with the maintenance of the posterior pelvic tilt during forward bending. It may be likely that LBP patients have increased eccentric hamstring torque as an adaptive mechanism to stabilize the lumbo-pelvic region (Marshall et al, 2010).

    Hamstring is an important stability muscle of the lower limb and its flexibility is important for maintaining normal posture and movement (Vadivelan and Priyaraj, 2015). The decrease of hamstring muscle flexibility produces a decrease of pelvic mobility that leads to an invariable biomechanical change in the pressure distribution in spine (Vadivelan and Priyaraj, 2015). Therefore, lower hamstring flexibility has been associated with postural deviations, gait limitations, increased risk of falls, and susceptibility to musculoskeletal injuries (Mayora-Vega et al, 2015). Recent study has suggested that an activation pattern similar to FRP is shown by the hamstring muscles (McGorry et al, 2001).

    However, to the best of our knowledge, no studies have yet investigated the influence of hamstring muscle flexibility on the FRP of the hamstring muscle and lumbopelvic kinematics during forward bending. Therefore, the purpose of this study was to examine the flexion-relaxation ratio (FRR) of the hamstring muscles and lumbopelvic kinematics and compare them during forward bending in subjects with different hamstring muscle flexibility.

    Methods

    Subjects

    A total of 35 participants volunteered to participate in the pretest. They were screened by a skilled physical therapist. Twenty-six subjects (n=26; 6 women and 20 men) were recruited to participate in this study. The active knee extension (AKE) test (Gajdosik and Lusin, 1983) was used to assess hamstring muscle length. The Popliteal angle was defined as the degree of knee flexion from terminal knee extension. Complete knee extension means a popliteal angle of 0°, and the lack of knee extension was measured with a bubble inclinometer (Figure 1). The AKE testing procedure was explained to all participants. The AKE measurements were taken for both knees. The inclusion criterion was subjects who had a popliteal angle under 30° (Group 1) or above 50° (Group 2). The 9 subjects who had a popliteal angle from 31° to 49° were excluded. People with any known orthopedic or neurological disorders were excluded. The general characteristics of the subjects are shown in Table 1. This study was approved by the Yonsei University Wonju institutional review board (approval number: 1041849-201704-BM-020-01).

    Electromyography (EMG)

    Each subject’s skin was cleaned with an alcohol swab. The electrodes were placed over the skin of right and left hamstrings (biceps femoris, BF) at the midpoint of the distance between the ischial tuberosity and the fibular head (Leinonen et al, 2000). The raw EMG signals were band-pass filtered between 20 and 450 ㎐, and sampled at 1000 ㎐. The EMG signals were processed into the root-mean-square (RMS) moving window of the 300-㎳ duration of the EMG data. We calculated the FRR as the maximum EMG during forward flexion (a) divided by the minimum resting (fully flexed) EMG (b) (Ahern et al, 1988; Watson et al, 1997). Electromyography values were calculated as the 1 second average RMS EMG around the maximum EMG levels detected during flexion and at the minimum level detected during the rest time. Using EMG values as ratios has the benefit of providing a normalized EMG value, which might provide the ability to compare FRRs over time and across people. This method has moderate to excellent within and between session reliability (Watson et al, 1997).

    Kinematic data

    The EMG system (EMG, Noraxon Inc., AZ, USA) was synchronized with a motion analysis system. The motion analysis system (MyoMotion system, Noraxon Inc., St. AZ, USA) was used to record the kinematic data. MyoMotion sensors were attached to the subject’s lower thoracic spine, pelvis and both thighs at the center of the spinous processes of the twelfth thoracic and first sacral vertebrae, and at the midpoint between the lateral femoral epicondyle and the greater trochanter of the femur (Figure 2). The fascia over the spinous processes has a firm fix ation to bone (Lundberg, 1996), so skin movement will follow bone movement more closely than in other regions. All sensors were fastened to the skin overlying these bony landmarks using special fixation straps, double-sided adhesive tape, and elastic straps. The kinematic data consisted of the lumbar and pelvic flexion angles. In the sagittal plane, the Lumbar flexion angle was defined as the mediolateral-axis angle between the lumbar spine and the pelvis; the pelvic flexion angle was defined as the mediolateral- axis angle between the pelvis and the femur.

    Experimental protocol

    The trunk forward bending task (Kim et al, 2013) consisted of natural standing, bending (trunk flexion), hanging (trunk full flexion), returning, and relaxed standing periods. The subjects were allowed to practice the required movements to familiarize themselves with the experimental tasks. A counted time signal was used to pace the movement. The subjects stood on a line labeled on the floor with their arms by their sides and the their feet at pelvis-width apart. First, the subjects were required to stand naturally for 3 seconds and then to bend their trunk forward as far as possible without flexing their knees and let their arms hang freely for 3 seconds. Second, they were instructed to hang in the fully flexed position for 3 seconds with the metronome. Third, they were asked to go back to the upright position for 3 seconds. Finally, the subjects were required to sustain a natural standing position for 3 seconds (Figure 3). Each activity was repeated three times. The mean score was used in the kinematic and electromyographical data analysis.

    Statistical analysis

    The SPSS statistical package version 18.0 was used for the statistical analyses. All data were tested for normal distribution with the Shapiro-Wilk normality test (EMG and kinematic data of the hip and lumbar). All variables were confirmed to be normally distributed; thus, parametric statistics were used. The significance of the differences between the two groups was evaluated using the independent t-test. p values less than .05 were used for the statistical tests.

    Results

    The FRRs of the hamstring muscles and lumbopelvic kinematics between two groups

    In the subjects with greater hamstring muscle flexibility (Group 1), the pelvic flexion showed a more range of motion than the lumbar flexion. The FRRs of the hamstring muscles were significantly higher in the subjects with greater hamstring muscle flexibility group (3.85±1.78) than in the subjects with lower hamstring muscle flexibility group (.93±.11) (Table 2).

    Discussion

    Diverse methods have been suggested for the quantification of FRP, comprising 4 general categories of visual inspection, statistical, threshold, and ratio. Ratio criteria identified FRP with high sensitivity and may be appropriate for use in either research or clinical settings. (Schinkel-Ivy, 2013).

    The major results of this study indicate that the FRR of the hamstring muscle was significantly decreased in the lower hamstring muscle flexibility group when compared to the greater hamstring muscle flexibility group. In the subjects with lower hamstring muscle flexibility, the maximal lumbar flexion was greater and the maximal hip flexion was lower than in the other subjects. This study also confirmed that the FRP occurs in hamstrings during terminal hip flexion, which follows previously reported patterns (Sihvonen, 1997). The tightness of the hamstring muscles may have been overactivated during the hanging period, as a consequence of increased eccentric muscle activity.

    This study also shows that subjects with more flexible hamstring muscles have a large amount of biceps femoris muscle relaxation during the hanging period, and the tightened hamstring muscle is related to a greater muscle activation of the hamstrings during the hanging period. During the forward bending period, the values were 29.32±8.31 μV in the group 1 and 33.19±6.77 μV in the group 2, but this difference was not statistically significant (p>.05).

    Several authors have found that shortness of the hamstrings and lower pelvic flexion are related to the presence of LBP and have recommended using hamstring stretching to obtain more flexibility and boost the cooperation of the pelvic motion in trunk flexion-extension (Cailliet, 1995; Esola et al, 1996).

    It has been commonly assumed that when two body parts move, the more mobile body segment will move first, and this was described as compensatory relative flexibility by Sahrmann (2002). Two variations in the degree of lumbar to pelvic flexion motion and changes in hamstring flexibility have been demonstrated in LBP patients (Esola et al, 1996). It may be that a positive correlation exists between hamstring shortness and lumbar motion and negative correlation between hamstring shortness and hip motion.

    One of the three subsystems of the spinal stabilizing system is a passive system: the spinal column, which is comprised of ligaments (spinal ligaments, discs annulus and facet capsules), vertebrae and the remaining two are the active and neural systems: the spinal muscles and the neuromuscular control unit (Panjabi, 2006). Uncountable mechanoreceptors lie in the spinal ligaments (Edgar, 2007; Sekine et al, 2001), facet capsules (McLain, 1994; Yamashita et al, 1990) and disc annulus (Edgar, 2007). Passive systems are deformed by the application of repeated stretching or tensile stress; this deformation creates information from the mechanoreceptors encompassed within them and this information decreases muscle activity (Holm et al, 2002).

    The results of this study show how subjects with having lower hamstring flexibility are less movable at the pelvic level and more movable at the lumbar spine. In the higher movable condition of the lumbar spine in the lower hamstring flexibility group, the ligaments of the lumbar spine undergo lengthening and reduced tension. Therefore, passive structures rather than the spinal stabilizing muscles provide spinal stability and the ligaments of the lumbar spine may be overstretched. The lengthening of ligamentous structures can cause a meaningful reduction in the activation of the multifidus through mechanoreceptor desensitization (Solomonow et al, 1999).

    There is evidence from animal studies that the stimulation of the ligaments of the spine results in spinal muscle firing (Solomonow et al, 1999; Solomonow et al, 2002). Decreased sensitivity of the ligament mechanoreceptors results in decreased muscle activity. One study observed that the creep produced in viscoelastic tissues by the imposition of cyclic loading causes desensitization of the mechanoreceptors. Other studies have observed that creep developed in the viscoelastic structures indicates that micro-damage developed in the collagen fibers (Frank et al., 1985; Soslowskyet al., 2000), which creates a notable decrease in muscle activity and, as a consequence, greater susceptibility to instability and possible injury (Solomonow et al, 1999).

    The forward bending of the trunk allows pelvic anterior rotation in combination with lumbar flexion. The shortness of the hamstring muscle may have been eccentrically hyper-activated during the forward bending movement, which, in turn, posteriorly rotates the pelvis. A posterior pelvic rotation reduces the lumbar lordotic curve through the flexion of the lumbar spine, causes posterior movement of the nucleus pulposus, and increases the diameter of the intervertebral foramina (Neumann, 2002). Furthermore, shortened hamstring muscles are related to slumped sitting, because a slumped sitting posture can produce pelvic posterior tilting. Slumped sitting decreases the activation of the spinal stabilizing muscles (O’Sullivan et al, 2002) and aggravates loading on the intervertebral disc (Macintosh et al, 1993) and soft tissues. Generally, it is strongly accepted that passive postures like slumped sitting exacerbate chronic low back pain (O’Sullivan, 2000).

    This study has several limitations. Interpretations of the results of our study are limited to our subjects, who were all university students in their early 20s. The findings of this study cannot be generalized to the entire population. We consider the lack of LBP patients group is a limitation of our study. We hope that future studies will account for these limitations.

    Our results suggest that forward bending movements produce overuse of the lumbar spine in people with lower hamstring muscle flexibility, which produces mechanoreceptor desensitization in the ligaments of the spine and inactivity of the spinal stabilizing muscle, therefore, this might be connected to LBP. So, we suggest that clinicians attempt to recover normal hamstring muscle flexibility in the LBP patients. This possibility should be addressed in future studies of LBP patients.

    Conclusion

    This study has shown that significant differences were observed in the FRR of the hamstring muscles and lumbopelvic kinematics between the subjects with different hamstring muscle flexibility during forward bending movement. Hamstring muscle flexibility have an influence on lumbo-pelvic kinematics during trunk forward bending. The flexibility of the pelvis seems to influence the patterns of the activation of hamstring muscles during forward bending. Peculiarly, subjects that are more flexible in their hamstring muscles show a greater degree of flexion relaxation and pelvic flexion at maximum flexion.

    Figure

    PTK-24-1_F1.gif

    Active knee extension test (AKEtest).

    PTK-24-1_F2.gif

    Location of the electrodes and myomotion sensors.

    PTK-24-1_F3.gif

    Postures adopted during the forward bending tasks.

    Table

    General characteristics of the subjects

    amean±standard deviations.

    Maximal angular displacements and FRR of the hamstring muscle during the trunk bending task

    amean±standard deviations.

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