Journal of Electromyography and Kinesiology xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Journal of Electromyography and Kinesiology journal homepage: www.elsevier.com/locate/jelekin
Individuals with chronic low back pain demonstrate delayed onset of the back muscle activity during prone hip extension Tadanobu Suehiro a,b,⇑, Masatoshi Mizutani a, Hiroshi Ishida b, Kenichi Kobara b, Hiroshi Osaka b, Susumu Watanabe b a b
Graduate School of Health Sciences, Kibi International University, 8 Iga-machi, Takahashi City 716-8508, Japan Department of Rehabilitation, Faculty of Health Science and Technology, Kawasaki University of Medical Welfare, 288, Matsushima, Kurashiki City 701-0193, Japan
a r t i c l e
i n f o
Article history: Received 6 January 2015 Received in revised form 10 April 2015 Accepted 23 April 2015 Available online xxxx Keywords: Chronic low back pain Prone hip extension Muscle activity onset time Lumbopelvic stability Back muscle
a b s t r a c t Prone hip extension (PHE) is commonly used in the evaluation of the stability of the lumbopelvic region. There is little evidence of difference in muscle activity onset timing between healthy individuals and individuals with chronic low back pain (CLBP) during PHE. The purpose of this study was to determine if individuals with and without CLBP differ in the onset time of the trunk and hip extensor muscles activity during PHE. The participants were 20 patients with CLBP and 20 healthy individuals. Electromyography data of the erector spinae, multifidus, gluteus maximus, and semitendinosus were collected during PHE using a surface electromyograph. Relative differences in the onset times between each muscle and the prime mover (i.e., the semitendinosus) were calculated. The onsets of the bilateral multifidus and contralateral erector spinae were significantly delayed in the CLBP group compared with the healthy group (p < 0.001), despite the onset timings of leg movement not being significantly different between the groups. The onset times of the gluteus maximus and ipsilateral erector spinae showed no significant differences between the groups. These results suggest that individuals with CLBP use an altered, and possibly inadequate, trunk muscle recruitment pattern. Ó 2015 Elsevier Ltd. All rights reserved.
1. Introduction Lumbopelvic stability is defined as the ability to control lumbopelvic orientation and maintain intervertebral neutral zones (Richardson et al., 2004). The prone hip extension (PHE) test is commonly used for the evaluation of lumbopelvic stability of individuals with back pathologies, and excessive lumbopelvic movement and the timing of the muscle activity are assessed. Clinically, the lumbopelvic region is often observed to extend or rotate excessively during PHE in individuals with lumbopelvic dysfunctions (Sahrmann, 2002). Such reduced movement control and excessive lumbar spine motion induced pain in individuals with back pain (O’Sullivan, 2005; Sahrmann, 2002). Several previous studies have analyzed the timing of muscle recruitment during PHE in healthy individuals (Lehman et al., 2004; Nygren Pierce and Lee, 1990; Tateuchi et al., 2012; Vogt and Banzer, 1997). In three of these studies, however, PHE was performed at a low speed (Nygren Pierce and Lee, 1990; Tateuchi et al., 2012; Vogt and
⇑ Corresponding author at: 288, Matsushima, Kurashiki City 701-0193, Japan. Tel.: +81 86 462 1111; fax: +81 86 464 1109. E-mail address: [email protected] (T. Suehiro).
Banzer, 1997), while the remaining report did not specify the speed of limb movement (Lehman et al., 2004). Studies have found that performing the movement at a low speed reduces the frequency of response of the trunk muscles and increases the variability (Hodges and Richardson, 1997b, 1999). Therefore, a consistent pattern of muscle activation still needs to be established. Several studies have examined muscle activity onset time during PHE in individuals with low back pain (LBP). Bruno and Bagust (2007) reported that patients with LBP have a significantly delayed onset of gluteus maximus (GM) activity when performing PHE movements, compared to healthy individuals. In contrast, Guimarães et al. (2010) and Masse-Alarie et al. (2014) did not detect differences in the onset time of the trunk and hip extensor muscles during PHE between asymptomatic individuals and those with chronic LBP (CLBP). Thus, whether muscle activity onset times differ between healthy individuals and patients with LBP is still controversial. In addition, these previous studies did not investigate the lumbopelvic stabilizer muscles such as the multifidus (MF). An altered activity pattern of the MF has been detected in individuals with CLBP during self-perturbation (Silfies et al., 2009). It has also been reported that, when the MF onset is delayed in healthy subjects during PHE, the degree of anterior pelvic tilt
http://dx.doi.org/10.1016/j.jelekin.2015.04.013 1050-6411/Ó 2015 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Suehiro T et al. Individuals with chronic low back pain demonstrate delayed onset of the back muscle activity during prone hip extension. J Electromyogr Kinesiol (2015), http://dx.doi.org/10.1016/j.jelekin.2015.04.013
2
T. Suehiro et al. / Journal of Electromyography and Kinesiology xxx (2015) xxx–xxx
increases (Tateuchi et al., 2012), and the excessive lumbopelvic movements can lead to compression and extension stress on the vertebrae and surrounding soft tissue, causing LBP (Gardner-Morse et al., 1995; Richardson et al., 1999). Investigating the onset timing of MF activity in individuals with CLBP during PHE is important to gain insight into the potential cause of their decreased lumbopelvic stability. Furthermore, successful treatment of lumbopelvic instability is difficult, in part because the pathology of the muscle recruitment patterns in individuals with CLBP is not completely understood. Thus, the main purpose of this study was to compare the muscle activation patterns between healthy individuals and patients with CLBP and to investigate changes in the onset timing of the trunk and hip extensor muscles in individuals with CLBP during PHE. Given that the temporal pattern of muscle recruitment has been a matter of debate, we also aimed to clarify the onset timing of the trunk and hip extensor muscles in healthy subjects during PHE. It was hypothesized that individuals with CLBP would demonstrate a delayed onset of MF activity. The results of this study offer insight into the treatment of lumbopelvic instability in individuals with CLBP. 2. Methods 2.1. Participants The sample size in this study was determined from a pilot study with 10 subjects (5 with CLBP and 5 controls). G-power 3.1.7 software (Franz Faul, Univesitat Kiel, Germany) was used to calculate a required sample size of 20 subjects in each group with a significance level of 0.05, power of 0.9, and effect size of 1.08 (calculated using the mean and standard deviation from the pilot study). Forty participants (20 with CLBP and 20 controls) were recruited through poster advertisements, local clinics, and word of mouth from the Okayama Prefecture and Ehime Prefecture areas. Volunteers with CLBP were included in the study if they satisfied the following inclusion criteria: (1) were between the ages of 20 and 40 years and (2) had unilateral or bilateral CLBP, localized between the levels of the twelfth thoracic vertebra and the coccyx, for more than 3 months without pain referral to the lower extremities. Control individuals were matched to those with CLBP based on age, gender, and body mass index (BMI). Exclusion criteria for all participants included (1) presence of pain during PHE, (2) shortening of the hip flexors, (3) neurological disorders, (4) pain in the thoracic spine and/or lower limbs, (5) a history of fractures or surgery in the lumbar spine or hip joints, (6) pregnancy in the two previous years, (7) sacroiliac dysfunction, and (8) presence of suspected or diagnosed serious spine pathology (inflammatory spondyloarthropathies, fracture, malignancy, cauda equina syndrome, or infection). Subjects who had undergone physical therapy involving strengthening of the extensors of the trunk or hip and those taking analgesics were also excluded. This study was reviewed and approved by the Ethics Committee at the Kawasaki University of Medical Welfare, and signed informed consent was obtained from all subjects prior to participation in the study. 2.2. Pain assessment and electromyography technique Severity of current LBP was scored using a numeric rating scale (NRS) from 0 to 10, where 0 denoted no pain and 10 the worst possible pain. The NRS has acceptable reliability and validity (Roach et al., 1997; Ferreira-Valente et al., 2011). Severity of LBP was also evaluated using the Oswestry Low Back Pain Disability Index (ODI), a 10-item questionnaire most commonly utilized for determining
the extent of functional disability caused by LBP (Fairbank and Pynsent, 2000). Participants were prepped for surface electromyography (EMG) electrode placement using standard protocols, which included shaving and lightly abrading the skin with rubbing alcohol until slightly red. Disposable pre-gelled EMG Ag/AgCl electrodes (Blue Sensor, Mets, Inc., Tokyo, Japan) with a 2.5-cm center-to-center inter-electrode distance were applied, with individual electrodes and electrode pairs placed parallel to the muscle belly over the following muscles according to the SENIAM recommendations (http://www.seniam.org): the bilateral erector spinae (ES): at a 2 finger widths distance laterally from the spinous process of L1; the bilateral MF: at the level of the L5 spinous process on a line extending from the posterior superior iliac spine to the interspace between L1 and L2; the semitendinosus (ST) on the leg extension side: in the middle of the line between the ischial tuberosity and the medial epicondyle of the femur; the GM on the leg extension side: in the middle of the line between the sacrum and the greater trochanter. A reference electrode was placed on the second sacral vertebra. The abdominal muscles (e.g., the external oblique and transverse abdominis/internal oblique muscles) were excluded from the analysis in this study because it has been reported that the activities of these muscles during PHE in healthy individuals were less than 5% of the maximal voluntary isometric contractions (Tateuchi et al., 2012), and no differences were found between asymptomatic and CLBP individuals in the onset of any abdominal muscle (Masse-Alarie et al., 2014). Electrode placements were confirmed with palpation during manually resisted muscle contractions. EMG data were acquired using a surface electromyograph (Vital Recorder 2, Kissei Comtec, Nagano, Japan) with 1000-Hz sampling frequency. The onset of leg movement was measured using a pressure sensor (Foot switch, Kissei Comtec, Nagano, Japan) synchronized with the electromyograph. The pressure sensor was attached to the front of the ankle and operated at a sampling frequency of 1000 Hz. 2.3. Experimental procedure Participants were asked to lie prone with their arms at their sides and a neutral position of the pelvis and hip joints. Each participant was instructed to perform active hip extension from 0° to 10° while keeping the knee extended (Fig. 1). Individuals with unilateral CLBP performed the movement using the leg of the painful side, those with bilateral CLBP used the leg of the more painful side, and controls used the non-dominant leg to avoid comparison with superior members. The leg that the participant used for support when kicking a soccer ball was considered non-dominant. Fast limb movement has been reported to increase the frequency of EMG response of the trunk muscles and reduce variability (Hodges and Richardson, 1997b, 1999). Accordingly, participants were instructed to raise the leg as rapidly as possible when the light-emitting diode (LED) lamp placed in front of their eyes was turned on. This position was maintained until the command ‘‘relax’’ was given. The position of the limb was inspected visually during the PHE task to ensure that the subject maintained neutral hip rotation and knee extension. If visible hip rotation movement was observed, the corresponding data were excluded. Several practice trials were allowed prior to testing to familiarize participants with the required movements. Three trials were performed, with rest periods of 1 min between them, and the average value was used. 2.4. Data processing All electromyographic signals were passed through a band-pass filter (10–500 Hz). Full-wave rectification was subsequently performed. To determine the onset of muscle activity, a threshold of
Please cite this article in press as: Suehiro T et al. Individuals with chronic low back pain demonstrate delayed onset of the back muscle activity during prone hip extension. J Electromyogr Kinesiol (2015), http://dx.doi.org/10.1016/j.jelekin.2015.04.013
3
T. Suehiro et al. / Journal of Electromyography and Kinesiology xxx (2015) xxx–xxx
LED lamp
Pressure sensor
Fig. 1. Active prone hip extension from 0° to 10°. Each participant was instructed to start the movement immediately after the LED lamp was turned on. EMG data were collected synchronously with data from a pressure sensor attached to the front of the ankle, which was used to determine the onset of leg movement.
two standard deviations from the mean value observed at baseline was calculated using Microsoft Excel 2010 (Microsoft). The values of the electromyographic signal were observed, and the onset of muscle activity was defined as the time when the electromyographic signal exceeded this threshold for a period of 50 ms (Hodges and Bui, 1996; Kang et al., 2013; Sakamoto et al., 2009). To investigate the temporal firing pattern of the hip and trunk muscles, the relative differences in the onset times between each muscle and the prime mover (i.e., the ST) were calculated (Chance-Larsen et al., 2010; Lehman et al., 2004; Takasaki et al., 2009). The onset time difference between each muscle and the ST was calculated by the following equation:
Relative onset time ¼ muscle onset time ST onset time ðmsÞ: Accordingly, a negative value indicated that the target muscle fired before the ST, and vice versa. The reaction time between turning the LED lamp on and the onset of leg movement was also evaluated. 2.5. Statistical analysis Because histograms and Kolmogorov–Smirnov statistics demonstrated that all of the data were normally distributed, we used parametric statistical methods. Differences in demographic characteristics between the groups were investigated with independent samples t-tests and the chi-squared test. One-way analysis of variance with repeated measures was used to detect differences in relative muscle onset time within the control group. Post-hoc analyses were performed using the Bonferroni method for P values
Contents lists available at ScienceDirect
Journal of Electromyography and Kinesiology journal homepage: www.elsevier.com/locate/jelekin
Individuals with chronic low back pain demonstrate delayed onset of the back muscle activity during prone hip extension Tadanobu Suehiro a,b,⇑, Masatoshi Mizutani a, Hiroshi Ishida b, Kenichi Kobara b, Hiroshi Osaka b, Susumu Watanabe b a b
Graduate School of Health Sciences, Kibi International University, 8 Iga-machi, Takahashi City 716-8508, Japan Department of Rehabilitation, Faculty of Health Science and Technology, Kawasaki University of Medical Welfare, 288, Matsushima, Kurashiki City 701-0193, Japan
a r t i c l e
i n f o
Article history: Received 6 January 2015 Received in revised form 10 April 2015 Accepted 23 April 2015 Available online xxxx Keywords: Chronic low back pain Prone hip extension Muscle activity onset time Lumbopelvic stability Back muscle
a b s t r a c t Prone hip extension (PHE) is commonly used in the evaluation of the stability of the lumbopelvic region. There is little evidence of difference in muscle activity onset timing between healthy individuals and individuals with chronic low back pain (CLBP) during PHE. The purpose of this study was to determine if individuals with and without CLBP differ in the onset time of the trunk and hip extensor muscles activity during PHE. The participants were 20 patients with CLBP and 20 healthy individuals. Electromyography data of the erector spinae, multifidus, gluteus maximus, and semitendinosus were collected during PHE using a surface electromyograph. Relative differences in the onset times between each muscle and the prime mover (i.e., the semitendinosus) were calculated. The onsets of the bilateral multifidus and contralateral erector spinae were significantly delayed in the CLBP group compared with the healthy group (p < 0.001), despite the onset timings of leg movement not being significantly different between the groups. The onset times of the gluteus maximus and ipsilateral erector spinae showed no significant differences between the groups. These results suggest that individuals with CLBP use an altered, and possibly inadequate, trunk muscle recruitment pattern. Ó 2015 Elsevier Ltd. All rights reserved.
1. Introduction Lumbopelvic stability is defined as the ability to control lumbopelvic orientation and maintain intervertebral neutral zones (Richardson et al., 2004). The prone hip extension (PHE) test is commonly used for the evaluation of lumbopelvic stability of individuals with back pathologies, and excessive lumbopelvic movement and the timing of the muscle activity are assessed. Clinically, the lumbopelvic region is often observed to extend or rotate excessively during PHE in individuals with lumbopelvic dysfunctions (Sahrmann, 2002). Such reduced movement control and excessive lumbar spine motion induced pain in individuals with back pain (O’Sullivan, 2005; Sahrmann, 2002). Several previous studies have analyzed the timing of muscle recruitment during PHE in healthy individuals (Lehman et al., 2004; Nygren Pierce and Lee, 1990; Tateuchi et al., 2012; Vogt and Banzer, 1997). In three of these studies, however, PHE was performed at a low speed (Nygren Pierce and Lee, 1990; Tateuchi et al., 2012; Vogt and
⇑ Corresponding author at: 288, Matsushima, Kurashiki City 701-0193, Japan. Tel.: +81 86 462 1111; fax: +81 86 464 1109. E-mail address: [email protected] (T. Suehiro).
Banzer, 1997), while the remaining report did not specify the speed of limb movement (Lehman et al., 2004). Studies have found that performing the movement at a low speed reduces the frequency of response of the trunk muscles and increases the variability (Hodges and Richardson, 1997b, 1999). Therefore, a consistent pattern of muscle activation still needs to be established. Several studies have examined muscle activity onset time during PHE in individuals with low back pain (LBP). Bruno and Bagust (2007) reported that patients with LBP have a significantly delayed onset of gluteus maximus (GM) activity when performing PHE movements, compared to healthy individuals. In contrast, Guimarães et al. (2010) and Masse-Alarie et al. (2014) did not detect differences in the onset time of the trunk and hip extensor muscles during PHE between asymptomatic individuals and those with chronic LBP (CLBP). Thus, whether muscle activity onset times differ between healthy individuals and patients with LBP is still controversial. In addition, these previous studies did not investigate the lumbopelvic stabilizer muscles such as the multifidus (MF). An altered activity pattern of the MF has been detected in individuals with CLBP during self-perturbation (Silfies et al., 2009). It has also been reported that, when the MF onset is delayed in healthy subjects during PHE, the degree of anterior pelvic tilt
http://dx.doi.org/10.1016/j.jelekin.2015.04.013 1050-6411/Ó 2015 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Suehiro T et al. Individuals with chronic low back pain demonstrate delayed onset of the back muscle activity during prone hip extension. J Electromyogr Kinesiol (2015), http://dx.doi.org/10.1016/j.jelekin.2015.04.013
2
T. Suehiro et al. / Journal of Electromyography and Kinesiology xxx (2015) xxx–xxx
increases (Tateuchi et al., 2012), and the excessive lumbopelvic movements can lead to compression and extension stress on the vertebrae and surrounding soft tissue, causing LBP (Gardner-Morse et al., 1995; Richardson et al., 1999). Investigating the onset timing of MF activity in individuals with CLBP during PHE is important to gain insight into the potential cause of their decreased lumbopelvic stability. Furthermore, successful treatment of lumbopelvic instability is difficult, in part because the pathology of the muscle recruitment patterns in individuals with CLBP is not completely understood. Thus, the main purpose of this study was to compare the muscle activation patterns between healthy individuals and patients with CLBP and to investigate changes in the onset timing of the trunk and hip extensor muscles in individuals with CLBP during PHE. Given that the temporal pattern of muscle recruitment has been a matter of debate, we also aimed to clarify the onset timing of the trunk and hip extensor muscles in healthy subjects during PHE. It was hypothesized that individuals with CLBP would demonstrate a delayed onset of MF activity. The results of this study offer insight into the treatment of lumbopelvic instability in individuals with CLBP. 2. Methods 2.1. Participants The sample size in this study was determined from a pilot study with 10 subjects (5 with CLBP and 5 controls). G-power 3.1.7 software (Franz Faul, Univesitat Kiel, Germany) was used to calculate a required sample size of 20 subjects in each group with a significance level of 0.05, power of 0.9, and effect size of 1.08 (calculated using the mean and standard deviation from the pilot study). Forty participants (20 with CLBP and 20 controls) were recruited through poster advertisements, local clinics, and word of mouth from the Okayama Prefecture and Ehime Prefecture areas. Volunteers with CLBP were included in the study if they satisfied the following inclusion criteria: (1) were between the ages of 20 and 40 years and (2) had unilateral or bilateral CLBP, localized between the levels of the twelfth thoracic vertebra and the coccyx, for more than 3 months without pain referral to the lower extremities. Control individuals were matched to those with CLBP based on age, gender, and body mass index (BMI). Exclusion criteria for all participants included (1) presence of pain during PHE, (2) shortening of the hip flexors, (3) neurological disorders, (4) pain in the thoracic spine and/or lower limbs, (5) a history of fractures or surgery in the lumbar spine or hip joints, (6) pregnancy in the two previous years, (7) sacroiliac dysfunction, and (8) presence of suspected or diagnosed serious spine pathology (inflammatory spondyloarthropathies, fracture, malignancy, cauda equina syndrome, or infection). Subjects who had undergone physical therapy involving strengthening of the extensors of the trunk or hip and those taking analgesics were also excluded. This study was reviewed and approved by the Ethics Committee at the Kawasaki University of Medical Welfare, and signed informed consent was obtained from all subjects prior to participation in the study. 2.2. Pain assessment and electromyography technique Severity of current LBP was scored using a numeric rating scale (NRS) from 0 to 10, where 0 denoted no pain and 10 the worst possible pain. The NRS has acceptable reliability and validity (Roach et al., 1997; Ferreira-Valente et al., 2011). Severity of LBP was also evaluated using the Oswestry Low Back Pain Disability Index (ODI), a 10-item questionnaire most commonly utilized for determining
the extent of functional disability caused by LBP (Fairbank and Pynsent, 2000). Participants were prepped for surface electromyography (EMG) electrode placement using standard protocols, which included shaving and lightly abrading the skin with rubbing alcohol until slightly red. Disposable pre-gelled EMG Ag/AgCl electrodes (Blue Sensor, Mets, Inc., Tokyo, Japan) with a 2.5-cm center-to-center inter-electrode distance were applied, with individual electrodes and electrode pairs placed parallel to the muscle belly over the following muscles according to the SENIAM recommendations (http://www.seniam.org): the bilateral erector spinae (ES): at a 2 finger widths distance laterally from the spinous process of L1; the bilateral MF: at the level of the L5 spinous process on a line extending from the posterior superior iliac spine to the interspace between L1 and L2; the semitendinosus (ST) on the leg extension side: in the middle of the line between the ischial tuberosity and the medial epicondyle of the femur; the GM on the leg extension side: in the middle of the line between the sacrum and the greater trochanter. A reference electrode was placed on the second sacral vertebra. The abdominal muscles (e.g., the external oblique and transverse abdominis/internal oblique muscles) were excluded from the analysis in this study because it has been reported that the activities of these muscles during PHE in healthy individuals were less than 5% of the maximal voluntary isometric contractions (Tateuchi et al., 2012), and no differences were found between asymptomatic and CLBP individuals in the onset of any abdominal muscle (Masse-Alarie et al., 2014). Electrode placements were confirmed with palpation during manually resisted muscle contractions. EMG data were acquired using a surface electromyograph (Vital Recorder 2, Kissei Comtec, Nagano, Japan) with 1000-Hz sampling frequency. The onset of leg movement was measured using a pressure sensor (Foot switch, Kissei Comtec, Nagano, Japan) synchronized with the electromyograph. The pressure sensor was attached to the front of the ankle and operated at a sampling frequency of 1000 Hz. 2.3. Experimental procedure Participants were asked to lie prone with their arms at their sides and a neutral position of the pelvis and hip joints. Each participant was instructed to perform active hip extension from 0° to 10° while keeping the knee extended (Fig. 1). Individuals with unilateral CLBP performed the movement using the leg of the painful side, those with bilateral CLBP used the leg of the more painful side, and controls used the non-dominant leg to avoid comparison with superior members. The leg that the participant used for support when kicking a soccer ball was considered non-dominant. Fast limb movement has been reported to increase the frequency of EMG response of the trunk muscles and reduce variability (Hodges and Richardson, 1997b, 1999). Accordingly, participants were instructed to raise the leg as rapidly as possible when the light-emitting diode (LED) lamp placed in front of their eyes was turned on. This position was maintained until the command ‘‘relax’’ was given. The position of the limb was inspected visually during the PHE task to ensure that the subject maintained neutral hip rotation and knee extension. If visible hip rotation movement was observed, the corresponding data were excluded. Several practice trials were allowed prior to testing to familiarize participants with the required movements. Three trials were performed, with rest periods of 1 min between them, and the average value was used. 2.4. Data processing All electromyographic signals were passed through a band-pass filter (10–500 Hz). Full-wave rectification was subsequently performed. To determine the onset of muscle activity, a threshold of
Please cite this article in press as: Suehiro T et al. Individuals with chronic low back pain demonstrate delayed onset of the back muscle activity during prone hip extension. J Electromyogr Kinesiol (2015), http://dx.doi.org/10.1016/j.jelekin.2015.04.013
3
T. Suehiro et al. / Journal of Electromyography and Kinesiology xxx (2015) xxx–xxx
LED lamp
Pressure sensor
Fig. 1. Active prone hip extension from 0° to 10°. Each participant was instructed to start the movement immediately after the LED lamp was turned on. EMG data were collected synchronously with data from a pressure sensor attached to the front of the ankle, which was used to determine the onset of leg movement.
two standard deviations from the mean value observed at baseline was calculated using Microsoft Excel 2010 (Microsoft). The values of the electromyographic signal were observed, and the onset of muscle activity was defined as the time when the electromyographic signal exceeded this threshold for a period of 50 ms (Hodges and Bui, 1996; Kang et al., 2013; Sakamoto et al., 2009). To investigate the temporal firing pattern of the hip and trunk muscles, the relative differences in the onset times between each muscle and the prime mover (i.e., the ST) were calculated (Chance-Larsen et al., 2010; Lehman et al., 2004; Takasaki et al., 2009). The onset time difference between each muscle and the ST was calculated by the following equation:
Relative onset time ¼ muscle onset time ST onset time ðmsÞ: Accordingly, a negative value indicated that the target muscle fired before the ST, and vice versa. The reaction time between turning the LED lamp on and the onset of leg movement was also evaluated. 2.5. Statistical analysis Because histograms and Kolmogorov–Smirnov statistics demonstrated that all of the data were normally distributed, we used parametric statistical methods. Differences in demographic characteristics between the groups were investigated with independent samples t-tests and the chi-squared test. One-way analysis of variance with repeated measures was used to detect differences in relative muscle onset time within the control group. Post-hoc analyses were performed using the Bonferroni method for P values
