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Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain
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Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain Chih-Hsiu Cheng a, Andy Chien b,c, Wei-Li Hsu d, Ling-Wei Yen a, Yang-Hua Lin a, Hsin-Yi Kathy Cheng e,* a
Department of Physical Therapy and Graduate Institute of Rehabilitation Science, College of Medicine, Chang Gung University, Taoyuan, Taiwan, ROC Department of Physical Therapy and Graduate Institute of Rehabilitation Science, China Medical University, Taichung, Taiwan, ROC c Institute of Biomedical Engineering, National Taiwan University, Taipei, Taiwan, ROC d School and Graduate Institute of Physical Therapy, College of Medicine, National Taiwan University, Taipei, Taiwan, ROC e Graduate Institute of Early Intervention, College of Medicine, Chang Gung University, Taoyuan, Taiwan, ROC b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 8 November 2014 Received in revised form 17 February 2015 Accepted 20 February 2015
Purpose: Previous studies have identified sensorimotor disturbances and greater fatigability of neck muscles in patients with neck pain. The purpose of this study was to investigate the effect of neck pain and neck flexor fatigue on standing balance following postural perturbations. Methods: Twenty patients with chronic neck pain (CNP) (24.7 3.6 year-old) and 20 age-matched asymptomatic subjects (22.1 2.2 year-old) were recruited. Subjects stood barefoot on a force plate and experienced backward perturbations before and after neck flexor fatigue. Center of pressure, electromyography of cervical and lumbar muscles, and head/trunk accelerations were recorded. Two-way ANOVA (pain fatigue) was used for statistical analysis. Results: CNP group showed larger body sway during quiet standing but not during perturbed standing compared with asymptomatic adults. In both groups, neck flexor fatigue resulted in greater body sway during the quiet standing but smaller body sway during perturbed standing, increased neck muscle activations and decreased lumbar muscle activations, as well as increased time to maximal head acceleration. Conclusions: Disturbed balance control was observed in CNP patients during the quiet standing. However, a rigid strategy was used to minimize the postural sway and to protect the head against backward perturbations in both CNP and asymptomatic young adults after neck flexor fatigue. The results facilitate the understanding of how the subjects with chronic neck pain and with neck muscle fatigue deal with the challenging condition. Further studies are needed to verify if such phenomenon could be changed after the intervention of specific flexor muscle retraining and balance control exercises. ß 2015 Elsevier B.V. All rights reserved.
Keywords: Neck pain Muscle fatigue Standing balance
1. Introduction Chronic neck pain (CNP) is a common musculoskeletal disease with a reported 1-year prevalence ranging from 10.4% to 75.1% in the adult population worldwide [1]. It is one of the most common causes of long-term physical and psychosocial disabilities with a high recurrence rate [2,3]. Higher perceived neck disability and
* Corresponding author at: No. 259, Wen-Hwa 1st Rd, Kweishan, Taoyuan, Taiwan, ROC. Tel.: +886 3 2118800x3667; fax: +886 2 3366 8161. E-mail address: [email protected] (H.-Y. Cheng).
fear of movement in individuals with CNP may also lead to reduced physical activity [4]. Cervical spine, with abundant cervical mechanoreceptors, plays a critical role in the integration of multisensory afferent input involving the proprioception, vestibular, visual and somatosensory information [5]. The high densities of muscle spindles in the suboccipital muscles are integral in maintaining appropriate postural control [6,7]. The muscle spindles and mechanoreceptors in the cervical region relay somatosensory information to and from the central nervous system (CNS) via specific pathways. While individuals subject to vibration or induced fatigue of the neck muscles, these pathways are highlighted by the identification of
http://dx.doi.org/10.1016/j.gaitpost.2015.02.007 0966-6362/ß 2015 Elsevier B.V. All rights reserved.
Please cite this article in press as: Cheng C-H, et al. Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain. Gait Posture (2015), http://dx.doi.org/ 10.1016/j.gaitpost.2015.02.007
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postural deterioration such as the significant change in velocity and the direction of gain [8,9]. Postural control relies on the ability of the CNS to correctly identify and selectively focus on the multisensory afferent input. With pain, the performance of CNS in postural adjustments is greatly reduced as the input of pain has priority over other somatosensory stimuli [10]. Prolonged presence of pain can also affect postural stability and head movement control [11,12]. Similarly, the presence of muscle fatigue has been suggested to indirectly deteriorate the reliability of the proprioceptive signals due to altered muscle spindle afferent input [13]. With altered muscle contractile efficiency, the postural and cortical control is negatively influenced [14,15]. The purpose of this study was therefore to assess the influence of neck pain and induced neck flexor muscle fatigue on standing balance when subjected to external perturbation.
center of the electrode sensor for the RA was placed 3 cm lateral and 2 cm superior to the umbilicus, and that for the ES was placed at the L3 level and 3 cm lateral from the spinous processes [19]. Reference electrode is not needed using the Trigno system. The sampling rate of the EMG signals was 2 kHz. The acquired data were further digitally band-pass filtered between 20 Hz and 450 Hz, full-wave rectified, and smoothed with a low-pass filter (time constant of 100 ms; Butterworth 8th-order). The dynamic range of the three-axis accelerometer is 1.5 g and the resolution is 0.016 g/bit with a sampling frequency of 148.1 Hz. The changes of the acceleration were recorded at the head (on the top of the head), upper trunk (at the T3 level) and lower trunk (at the L3 level). All measurements including the force plate, loadcell, and EMG system were synchronized using the 32-channel 16-bit A/D board (NI USB-6218, National Instruments Co., USA). 2.3. Experimental procedure
2. Methods 2.1. Participants The CNP group comprised of 20 participants (age: 24.7 3.6, 11 males and 9 females). The inclusion criteria were: (1) non-traumatic pain in the neck region for more than 6 months in duration, (2) the pain should be ongoing and frequent (at least once a week), and (3) the intensity of the pain should be rated at least 3 on the Visual Analog Scale (VAS, 0–10). Participants were excluded if they have, (1) arthritis in the neck as confirmed by a health professional, (2) received spinal or lower limb surgery, (3) diagnosed with any neurological, vestibular and musculoskeletal disorders that may influence balance, and (4) have had falls of unknown origin within the last year. Twenty age-matched asymptomatic volunteers (age: 22.1 2.2, 8 males and 12 females) were also recruited provided they had no complaints of spinal or limb pain within the last year and had never experienced trauma or injuries to the cervical spine, head, and limb regions requiring medical treatments. Participants with neck pain were asked to indicate their level of pain and disability by completing the VAS and Neck Disability Index (NDI, 0–50), which were reported reliable and valid in Chinesespeaking population with neck pain [16]. The institutional medical research ethics committee approved the study. All the participants gave written informed consent before inclusion. 2.2. Instrumentation The postural sway of participants during standing balance assessment was measured using a force plate (Bertec 9090-15, Advanced Mechanical Technology Inc., Columbus, USA). A loadcell (ST3-20KG, Plastronic Technology Co., LTD., New Taipei City, Taiwan) attached to an adjustable stand was used to measure the force exerted during the maximal isometric contractions and the fatigue exercise. The wireless electromyography (EMG) system (Trigno Wireless System, Delsys Inc., Boston, USA) which can output EMG signals and three-axis acceleration data was used to record the muscle activations, the onset of the perturbation, and the acceleration of the segments synchronically. Surface EMG activities of right side sternocleidomastoid (SCM), splenius capitis (SPL), semispinalis capitis (SSC), rectus abdominis (RA), and erector spinae (ES) were measured. Based on the recommendations of the SENIAM, the skin surface was shaved of hair and cleaned with alcohol swabs before the wireless EMG sensors were applied. For SCM, the electrode sensor was placed lower one-third of the distance between the sternal notch and the mastoid process [17]. For SPL, the center of the electrode sensor was located at the intersection of the C7-ear line and the line of action of splenius muscles [18]. For SSC, the electrode sensor was centered at the C2 level over the belly of the muscle [18]. The
The assessment of the postural control contained several standing balance tests. Participants wore a custom designed harness on the upper torso to allow the attachment of a steel cable at the T9 level. This cable was linked to a weighted pulley system (Fig. 1). Participants were asked to stand upright on a force plate with arms by the side for 60 s, barefooted in narrow stance with two heels 3 cm apart and feet 30 degrees of abduction. The participants were tested either in quiet standing or with an external perturbation. The amplitude of the perturbation was 15% of participant’s body weight and participant would experience a backward perturbation with the release of the weight. After completing the balance tests under non-fatigue condition, participants had to perform maximal isometric contractions of the neck and lumbar muscles. For the maximal neck muscle contractions, the participant sat on a chair with the head neutrally positioned and his/her forehead pushed against a fixed loadcell to a plateau for 5 s in anterior, posterior, left, and right directions. For the maximal lumbar muscle contractions, the participant sat on a chair with arms crossed over the chest, and his/her trunk pushed against the loadcell for 5 s in anterior and posterior directions. The best of three measures was recorded. Before a new repetition, a 2min rest was taken to minimize the muscle fatigue. Participants were then asked to perform the neck flexor fatigue exercise. Same as the maximal neck muscle contraction condition, the participant maintained an isometric neck flexion at 60% of the maximal isometric contraction until arbitrarily stopped by the examiner. The stopping criteria were a score of seven on the exertion Borg scale (0–10) [20] or when they can no longer maintain the 60% exertion force. Verbal encouragement was given to the participant during the exercise. The fatigue exercise was repeated prior to each quiet and perturbed balance test for the fatigue condition. It was performed right next to the force plate and there was a short time-lag (less than 20 s) between the induced fatigue state and the balance tests [21]. Familiarization session (3 sets 10 s of balance protocols) was given to all participants before data collection to ensure quality of the measurements. Three trials were recorded in a predetermined random order. 2.4. Data analysis For the balance tests, the center of pressure (CoP) data were analyzed including the maximal anteroposterior and mediolateral displacement, and the sway area and mean velocity of CoP. One second out of the 5 s EMG signal during the maximal isometric contraction was used for the normalization of the EMG amplitude. The normalized averaged integration of EMG (NAIEMG) between the 70 ms and 200 ms after the perturbation was calculated to
Please cite this article in press as: Cheng C-H, et al. Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain. Gait Posture (2015), http://dx.doi.org/ 10.1016/j.gaitpost.2015.02.007
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Fig. 1. Illustration of the setup of the standing balance test with random perturbation.
examine the automatic postural adjustments [22]. The duration from the perturbation to the time when the maximal acceleration occurred at the head, upper trunk and lower trunk were obtained. The median frequency of EMG signal during the fatigue exercise was calculated as an objective indicator of fatigue. Normality of the descriptive data was assessed using the Shapiro–Wilk’s test. Two-way mixed design ANOVA was carried out to determine the interaction and differences between the two groups (neck pain factor) and muscle fatigue (fatigue factor). Pearson analysis was also used to analyze the correlation of VAS and NDI results with the parameters of the balance tests. A p < 0.05 was considered to be of statistical significance. 3. Results The assumption of normality was met for all the variables except age (p < 0.05). The CNP group generally showed mild to moderate neck pain and disability (VAS: 3.5 1.2; NDI: 12.2 3.0). During the fatigue exercise, the averaged slope of the median frequency of the SCM was 0.12 0.13 Hz/ms (amount of decrement was 32.6 15.8 Hz) in the patient group, and was 0.01 0.11 Hz/ms (amount of decrement was 50.1 22.2 Hz) in the control group. 3.1. Center of pressure No significant interaction between neck pain and fatigue factors was identified for any of the CoP measurements. During quiet standing, CNP group showed significantly increased maximal anteroposterior and mediolateral displacement, sway area, and mean velocity of the CoP (all p < 0.05) compared with the control group. The post-fatigue condition came with an increased maximal anteroposterior displacement (p < 0.001) compared with the pre-fatigue condition. During the perturbed standing, CNP group did not showed significant difference compared with the control group. The post-fatigue condition came with a decreased CoP sway area (p = 0.016) and decreased velocity (p = 0.043) compared with the pre-fatigue condition (Fig. 2, Table 1). 3.2. Muscle activation No significant interaction was found for all the muscles. The post-fatigue condition came with an increased SCM activation (p = 0.041) and decreased RA activation (p = 0.001) compared with the pre-fatigue condition. SSC activation showed similar trend to that of SCM, and ES showed similar trend to that of RA without significance (Fig. 3). 3.3. Segment acceleration No significant interaction was found for the time to maximal acceleration of the head, upper trunk, and lower trunk. The post-fatigue condition of the head
demonstrated a delayed time to maximal acceleration compared with the prefatigue condition (p < 0.001) (Fig. 4). 3.4. Correlation There were no significant correlations between any of the CoP measurements, muscle activation, and the time to maximal acceleration of the segments and VAS or NDI. Only the ‘RA activation in the post-fatigue condition’ demonstrated a moderate correlation with VAS (r = 0.54, p = 0.021).
4. Discussion The aim of this study was to investigate the influence of neck pain and induced neck flexor muscle fatigue on the standing balance when subjected to the external perturbation. Compared with the asymptomatic subjects, the results from the patients with neck pain showed greater body sway during quiet standing but not during perturbed standing tests. Compared with the pre-fatigue condition, the participants under the post-fatigue condition demonstrated: (1) greater body sway during quiet standing but smaller body sway during perturbed standing tests, (2) increased neck muscle activations and decreased lumbar muscle activations, and (3) increased time to maximal head acceleration. As a whole, these information revealed that the patients with chronic neck pain did show poor postural control compared with the asymptomatic controls during quiet standing. However, after neck muscle fatigue, both groups demonstrated comparable restricted postural control in perturbed condition. In summary, under the less challenging condition, the presence of pain alone appears to cause postural control disturbances. With muscle fatigue, both group employed a rigid strategy to guard and minimize head motions. This fatigue appears to have an overriding impact on the postural control over the presence of pain. The current results indicated no interaction between the pain and fatigue factors. The main effects revealed that muscle fatigue appears to have a predominant influence on the balance control regardless of pain status. One plausible explanation was that the participants were mostly young adults. It has been documented that healthy adults tend to adopt a rigid strategy against large perturbations [23]. This is the first study to show that muscle fatigue is a more prevailing factor over pain and could result in the
Please cite this article in press as: Cheng C-H, et al. Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain. Gait Posture (2015), http://dx.doi.org/ 10.1016/j.gaitpost.2015.02.007
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Fig. 2. Averaged anteroposterior and mediolateral of displacement, sway area, and velocity of center of pressure under (a) quiet standing, and (b) external perturbation before and after fatigue conditions in patients with chronic neck pain (CNP) and asymptomatic control. * indicates p < 0.05.
Please cite this article in press as: Cheng C-H, et al. Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain. Gait Posture (2015), http://dx.doi.org/ 10.1016/j.gaitpost.2015.02.007
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Table 1 Mean values with standard deviation of the center of pressure, muscle activation (normalized averaged integration of EMG, NAIEMG), and time to maximal acceleration before and after fatigue conditions in patients with chronic neck pain (CNP) and asymptomatic control. Control
CNP Pre-fatigue Center of pressure (under quiet standing) Anteroposterior displacement (mm) Mediolateral displacement (mm) Sway area (mm2) Velocity (mm/s)
Post-fatigue
Pre-fatigue
Post-fatigue
10.5 4.3 16.3 5.4 79.3 60.0 5.4 1.2
13.0 4.7 16.5 5.5 90.1 59.3 5.3 1.4
7.7 3.5 12.9 4.1 41.6 26.4 4.5 1.1
8.8 3.4 12.7 4.0 51.0 38.3 4.5 1.0
Center of pressure (under external perturbation) Anteroposterior displacement (mm) Mediolateral displacement (mm) Sway area (mm2) Velocity (mm/s)
28.2 4.9 13.4 4.7 336.4 160.4 36.2 6.8
27.1 6.2 12.6 4.5 278.6 122.4 34.0 7.3
25.5 2.5 13.4 5.4 293.6 117.1 34.5 5.4
24.7 2.7 12.3 4.1 255.1 112.0 33.1 4.0
Muscle activation (under external perturbation) Sternocleidomastoids Semispinalis capitis Rectus abdominis Erector spinae
0.08 0.05 0.45 0.24 0.38 0.22 0.36 0.25
0.09 0.07 0.46 0.23 0.30 0.22 0.29 0.19
0.05 0.03 0.37 0.19 0.56 0.34 0.40 0.31
0.07 0.05 0.42 0.25 0.43 0.33 0.31 0.22
Time to maximal acceleration (under external perturbation) Head (ms) 276.4 15.5 Upper trunk (ms) 189.2 16.5 Lower trunk (ms) 244.1 31.7
285.2 24.8 193.6 10.5 244.8 37.6
279.9 19.6 183.6 24.4 230.9 24.5
299.5 34.3 189.8 18.7 229.6 33.9
adaptation of a ‘‘stiffened’’ posture in young adults regardless of neck pain. Further investigation is warranted if such strategy also exhibited in the mid-aged and elderly with chronic neck pain. Patients with neck pain showed greater body sway compared with the asymptomatic subjects during the quiet standing test, but not under the perturbed standing test. In addition, patients with neck pain showed a trend of increased neck muscle activations under external perturbations. The results indicated that chronic neck pain, even in young adults, could pose challenges to the postural control system. However, when subjected to external
perturbations, the young patients were still capable of maintaining balance as the asymptomatic subjects. The results indicated that patients with neck pain employed high activations of both the neck flexor and extensor muscles in an attempt to maintain their head position when perturbed. Participants in the current study were subjected to a large pulling force which equates to 15% of body weight comparing with the 3% of body weight used in previous similar studies [24]. Since the perturbation with 20% of body weight would induce stepping reactions [25], the ‘‘head strategy’’ used by the young patients seemed to be sufficient to maintain the
Fig. 3. Muscle activation (normalized averaged integration of EMG, NAIEMG) of sternocleidomastoids (SCM), semispinalis capitis (SSC), rectus abdominis (RA) and erector spinae (ES) under external perturbation before and after fatigue conditions in patients with chronic neck pain (CNP) and asymptomatic control. * indicates p < 0.05.
Please cite this article in press as: Cheng C-H, et al. Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain. Gait Posture (2015), http://dx.doi.org/ 10.1016/j.gaitpost.2015.02.007
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Fig. 4. Time to maximal acceleration of the top of head, upper trunk (UT) and lower trunk (LT) under external perturbation before and after fatigue conditions in patients with chronic neck pain (CNP) and asymptomatic control. * indicates p < 0.05.
balance within in situ status. Furthermore, given the previous reports of greater body sway in trauma-induced neck pain patients [24], our study provided a comparable pattern of body sway in chronic neck pain patients. Most studies to date have focused on the impact of neck extensor fatigue on the balance control [26]. Given the high densities of muscle spindles in the neck flexors and their fatigability in patients with neck pain [6,27], this is the first study, to the best of our knowledge, to determine if neck flexor fatigue would affect the postural control. The induction of neck flexor fatigue in current study resulted in an increased body sway during quiet standing, but a decreased body sway during perturbed standing, regardless of neck pain status. After the neck flexor fatigue, both the patients and the asymptomatic subjects demonstrated an increased activation of the neck flexors but a decreased activation of the lumbar flexors. The time to maximal head acceleration was also delayed under the fatigue condition. These results indicated that the neck flexor fatigue would deteriorate the postural control during quiet standing, while the young subjects adopted a rigid strategy against the external perturbation. The increased activation of the neck flexor and the increased time to maximal head acceleration indicated a state of head stabilization, and the decreased activation of the lumbar flexor were to balance the trunk perturbations. The possible ‘‘headfirst’’ or ‘‘fatigued-segment’’ protection strategy could be crucial against external perturbations. Further studies are warranted to verify if such strategy works in the aged population. This study also compared the relationships between pain and disability level and the balance parameters. No significant correlations were found but one: a moderate correlation between the VAS and the ‘‘RA activation in the post-fatigue condition’’. Our finding is consistent with a previous study examining patients with traumatic neck pain and found measurements like VAS and NDI correlated poorly with the head proprioceptive function [28]. Another study with 127 subjects found that pain frequency had a higher association with head proprioceptive function while the influence of pain intensity was inconsistent [29]. 4.1. Limitation in this study Some limitations should be addressed. The ages of the participants were between 20 and 30 years old, whereas the population with neck pain are commonly middle-aged. In addition, the muscle fatigue status was self-reported. Though no objective
technique was employed to verify the true muscle fatigue status in the current study design, previous studies have shown that the median frequency slopes of contractions until subjective exhaustion present reliable results and 30–50 Hz decrement of the median frequency can indicate the fatigue of neck muscles [30].
5. Conclusions Current results provided evidence that the young subjects adopted a rigid strategy for neck and lumbar muscles during external perturbation with neck pain or neck flexor fatigue. The results facilitate the understanding of the strategies subjects with chronic neck pain would choose under challenging conditions. Further studies are needed to verify if similar strategy exists in the aged population. The results also inspire the development of specific exercise programs for improving balance control in patients with chronic neck pain. Acknowledgments We gratefully acknowledge all the participants and the supports of the Ministry of Science and Technology of the Republic of China and Chang Gung Memorial Hospital Research Program, to this research under the grants 101-2221-E-182-020-MY3 and CMRPD1D0121 respectively. Conflict of interest: The authors declare that they have no conflict of interest.
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Please cite this article in press as: Cheng C-H, et al. Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain. Gait Posture (2015), http://dx.doi.org/ 10.1016/j.gaitpost.2015.02.007
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Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain Chih-Hsiu Cheng a, Andy Chien b,c, Wei-Li Hsu d, Ling-Wei Yen a, Yang-Hua Lin a, Hsin-Yi Kathy Cheng e,* a
Department of Physical Therapy and Graduate Institute of Rehabilitation Science, College of Medicine, Chang Gung University, Taoyuan, Taiwan, ROC Department of Physical Therapy and Graduate Institute of Rehabilitation Science, China Medical University, Taichung, Taiwan, ROC c Institute of Biomedical Engineering, National Taiwan University, Taipei, Taiwan, ROC d School and Graduate Institute of Physical Therapy, College of Medicine, National Taiwan University, Taipei, Taiwan, ROC e Graduate Institute of Early Intervention, College of Medicine, Chang Gung University, Taoyuan, Taiwan, ROC b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 8 November 2014 Received in revised form 17 February 2015 Accepted 20 February 2015
Purpose: Previous studies have identified sensorimotor disturbances and greater fatigability of neck muscles in patients with neck pain. The purpose of this study was to investigate the effect of neck pain and neck flexor fatigue on standing balance following postural perturbations. Methods: Twenty patients with chronic neck pain (CNP) (24.7 3.6 year-old) and 20 age-matched asymptomatic subjects (22.1 2.2 year-old) were recruited. Subjects stood barefoot on a force plate and experienced backward perturbations before and after neck flexor fatigue. Center of pressure, electromyography of cervical and lumbar muscles, and head/trunk accelerations were recorded. Two-way ANOVA (pain fatigue) was used for statistical analysis. Results: CNP group showed larger body sway during quiet standing but not during perturbed standing compared with asymptomatic adults. In both groups, neck flexor fatigue resulted in greater body sway during the quiet standing but smaller body sway during perturbed standing, increased neck muscle activations and decreased lumbar muscle activations, as well as increased time to maximal head acceleration. Conclusions: Disturbed balance control was observed in CNP patients during the quiet standing. However, a rigid strategy was used to minimize the postural sway and to protect the head against backward perturbations in both CNP and asymptomatic young adults after neck flexor fatigue. The results facilitate the understanding of how the subjects with chronic neck pain and with neck muscle fatigue deal with the challenging condition. Further studies are needed to verify if such phenomenon could be changed after the intervention of specific flexor muscle retraining and balance control exercises. ß 2015 Elsevier B.V. All rights reserved.
Keywords: Neck pain Muscle fatigue Standing balance
1. Introduction Chronic neck pain (CNP) is a common musculoskeletal disease with a reported 1-year prevalence ranging from 10.4% to 75.1% in the adult population worldwide [1]. It is one of the most common causes of long-term physical and psychosocial disabilities with a high recurrence rate [2,3]. Higher perceived neck disability and
* Corresponding author at: No. 259, Wen-Hwa 1st Rd, Kweishan, Taoyuan, Taiwan, ROC. Tel.: +886 3 2118800x3667; fax: +886 2 3366 8161. E-mail address: [email protected] (H.-Y. Cheng).
fear of movement in individuals with CNP may also lead to reduced physical activity [4]. Cervical spine, with abundant cervical mechanoreceptors, plays a critical role in the integration of multisensory afferent input involving the proprioception, vestibular, visual and somatosensory information [5]. The high densities of muscle spindles in the suboccipital muscles are integral in maintaining appropriate postural control [6,7]. The muscle spindles and mechanoreceptors in the cervical region relay somatosensory information to and from the central nervous system (CNS) via specific pathways. While individuals subject to vibration or induced fatigue of the neck muscles, these pathways are highlighted by the identification of
http://dx.doi.org/10.1016/j.gaitpost.2015.02.007 0966-6362/ß 2015 Elsevier B.V. All rights reserved.
Please cite this article in press as: Cheng C-H, et al. Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain. Gait Posture (2015), http://dx.doi.org/ 10.1016/j.gaitpost.2015.02.007
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postural deterioration such as the significant change in velocity and the direction of gain [8,9]. Postural control relies on the ability of the CNS to correctly identify and selectively focus on the multisensory afferent input. With pain, the performance of CNS in postural adjustments is greatly reduced as the input of pain has priority over other somatosensory stimuli [10]. Prolonged presence of pain can also affect postural stability and head movement control [11,12]. Similarly, the presence of muscle fatigue has been suggested to indirectly deteriorate the reliability of the proprioceptive signals due to altered muscle spindle afferent input [13]. With altered muscle contractile efficiency, the postural and cortical control is negatively influenced [14,15]. The purpose of this study was therefore to assess the influence of neck pain and induced neck flexor muscle fatigue on standing balance when subjected to external perturbation.
center of the electrode sensor for the RA was placed 3 cm lateral and 2 cm superior to the umbilicus, and that for the ES was placed at the L3 level and 3 cm lateral from the spinous processes [19]. Reference electrode is not needed using the Trigno system. The sampling rate of the EMG signals was 2 kHz. The acquired data were further digitally band-pass filtered between 20 Hz and 450 Hz, full-wave rectified, and smoothed with a low-pass filter (time constant of 100 ms; Butterworth 8th-order). The dynamic range of the three-axis accelerometer is 1.5 g and the resolution is 0.016 g/bit with a sampling frequency of 148.1 Hz. The changes of the acceleration were recorded at the head (on the top of the head), upper trunk (at the T3 level) and lower trunk (at the L3 level). All measurements including the force plate, loadcell, and EMG system were synchronized using the 32-channel 16-bit A/D board (NI USB-6218, National Instruments Co., USA). 2.3. Experimental procedure
2. Methods 2.1. Participants The CNP group comprised of 20 participants (age: 24.7 3.6, 11 males and 9 females). The inclusion criteria were: (1) non-traumatic pain in the neck region for more than 6 months in duration, (2) the pain should be ongoing and frequent (at least once a week), and (3) the intensity of the pain should be rated at least 3 on the Visual Analog Scale (VAS, 0–10). Participants were excluded if they have, (1) arthritis in the neck as confirmed by a health professional, (2) received spinal or lower limb surgery, (3) diagnosed with any neurological, vestibular and musculoskeletal disorders that may influence balance, and (4) have had falls of unknown origin within the last year. Twenty age-matched asymptomatic volunteers (age: 22.1 2.2, 8 males and 12 females) were also recruited provided they had no complaints of spinal or limb pain within the last year and had never experienced trauma or injuries to the cervical spine, head, and limb regions requiring medical treatments. Participants with neck pain were asked to indicate their level of pain and disability by completing the VAS and Neck Disability Index (NDI, 0–50), which were reported reliable and valid in Chinesespeaking population with neck pain [16]. The institutional medical research ethics committee approved the study. All the participants gave written informed consent before inclusion. 2.2. Instrumentation The postural sway of participants during standing balance assessment was measured using a force plate (Bertec 9090-15, Advanced Mechanical Technology Inc., Columbus, USA). A loadcell (ST3-20KG, Plastronic Technology Co., LTD., New Taipei City, Taiwan) attached to an adjustable stand was used to measure the force exerted during the maximal isometric contractions and the fatigue exercise. The wireless electromyography (EMG) system (Trigno Wireless System, Delsys Inc., Boston, USA) which can output EMG signals and three-axis acceleration data was used to record the muscle activations, the onset of the perturbation, and the acceleration of the segments synchronically. Surface EMG activities of right side sternocleidomastoid (SCM), splenius capitis (SPL), semispinalis capitis (SSC), rectus abdominis (RA), and erector spinae (ES) were measured. Based on the recommendations of the SENIAM, the skin surface was shaved of hair and cleaned with alcohol swabs before the wireless EMG sensors were applied. For SCM, the electrode sensor was placed lower one-third of the distance between the sternal notch and the mastoid process [17]. For SPL, the center of the electrode sensor was located at the intersection of the C7-ear line and the line of action of splenius muscles [18]. For SSC, the electrode sensor was centered at the C2 level over the belly of the muscle [18]. The
The assessment of the postural control contained several standing balance tests. Participants wore a custom designed harness on the upper torso to allow the attachment of a steel cable at the T9 level. This cable was linked to a weighted pulley system (Fig. 1). Participants were asked to stand upright on a force plate with arms by the side for 60 s, barefooted in narrow stance with two heels 3 cm apart and feet 30 degrees of abduction. The participants were tested either in quiet standing or with an external perturbation. The amplitude of the perturbation was 15% of participant’s body weight and participant would experience a backward perturbation with the release of the weight. After completing the balance tests under non-fatigue condition, participants had to perform maximal isometric contractions of the neck and lumbar muscles. For the maximal neck muscle contractions, the participant sat on a chair with the head neutrally positioned and his/her forehead pushed against a fixed loadcell to a plateau for 5 s in anterior, posterior, left, and right directions. For the maximal lumbar muscle contractions, the participant sat on a chair with arms crossed over the chest, and his/her trunk pushed against the loadcell for 5 s in anterior and posterior directions. The best of three measures was recorded. Before a new repetition, a 2min rest was taken to minimize the muscle fatigue. Participants were then asked to perform the neck flexor fatigue exercise. Same as the maximal neck muscle contraction condition, the participant maintained an isometric neck flexion at 60% of the maximal isometric contraction until arbitrarily stopped by the examiner. The stopping criteria were a score of seven on the exertion Borg scale (0–10) [20] or when they can no longer maintain the 60% exertion force. Verbal encouragement was given to the participant during the exercise. The fatigue exercise was repeated prior to each quiet and perturbed balance test for the fatigue condition. It was performed right next to the force plate and there was a short time-lag (less than 20 s) between the induced fatigue state and the balance tests [21]. Familiarization session (3 sets 10 s of balance protocols) was given to all participants before data collection to ensure quality of the measurements. Three trials were recorded in a predetermined random order. 2.4. Data analysis For the balance tests, the center of pressure (CoP) data were analyzed including the maximal anteroposterior and mediolateral displacement, and the sway area and mean velocity of CoP. One second out of the 5 s EMG signal during the maximal isometric contraction was used for the normalization of the EMG amplitude. The normalized averaged integration of EMG (NAIEMG) between the 70 ms and 200 ms after the perturbation was calculated to
Please cite this article in press as: Cheng C-H, et al. Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain. Gait Posture (2015), http://dx.doi.org/ 10.1016/j.gaitpost.2015.02.007
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Fig. 1. Illustration of the setup of the standing balance test with random perturbation.
examine the automatic postural adjustments [22]. The duration from the perturbation to the time when the maximal acceleration occurred at the head, upper trunk and lower trunk were obtained. The median frequency of EMG signal during the fatigue exercise was calculated as an objective indicator of fatigue. Normality of the descriptive data was assessed using the Shapiro–Wilk’s test. Two-way mixed design ANOVA was carried out to determine the interaction and differences between the two groups (neck pain factor) and muscle fatigue (fatigue factor). Pearson analysis was also used to analyze the correlation of VAS and NDI results with the parameters of the balance tests. A p < 0.05 was considered to be of statistical significance. 3. Results The assumption of normality was met for all the variables except age (p < 0.05). The CNP group generally showed mild to moderate neck pain and disability (VAS: 3.5 1.2; NDI: 12.2 3.0). During the fatigue exercise, the averaged slope of the median frequency of the SCM was 0.12 0.13 Hz/ms (amount of decrement was 32.6 15.8 Hz) in the patient group, and was 0.01 0.11 Hz/ms (amount of decrement was 50.1 22.2 Hz) in the control group. 3.1. Center of pressure No significant interaction between neck pain and fatigue factors was identified for any of the CoP measurements. During quiet standing, CNP group showed significantly increased maximal anteroposterior and mediolateral displacement, sway area, and mean velocity of the CoP (all p < 0.05) compared with the control group. The post-fatigue condition came with an increased maximal anteroposterior displacement (p < 0.001) compared with the pre-fatigue condition. During the perturbed standing, CNP group did not showed significant difference compared with the control group. The post-fatigue condition came with a decreased CoP sway area (p = 0.016) and decreased velocity (p = 0.043) compared with the pre-fatigue condition (Fig. 2, Table 1). 3.2. Muscle activation No significant interaction was found for all the muscles. The post-fatigue condition came with an increased SCM activation (p = 0.041) and decreased RA activation (p = 0.001) compared with the pre-fatigue condition. SSC activation showed similar trend to that of SCM, and ES showed similar trend to that of RA without significance (Fig. 3). 3.3. Segment acceleration No significant interaction was found for the time to maximal acceleration of the head, upper trunk, and lower trunk. The post-fatigue condition of the head
demonstrated a delayed time to maximal acceleration compared with the prefatigue condition (p < 0.001) (Fig. 4). 3.4. Correlation There were no significant correlations between any of the CoP measurements, muscle activation, and the time to maximal acceleration of the segments and VAS or NDI. Only the ‘RA activation in the post-fatigue condition’ demonstrated a moderate correlation with VAS (r = 0.54, p = 0.021).
4. Discussion The aim of this study was to investigate the influence of neck pain and induced neck flexor muscle fatigue on the standing balance when subjected to the external perturbation. Compared with the asymptomatic subjects, the results from the patients with neck pain showed greater body sway during quiet standing but not during perturbed standing tests. Compared with the pre-fatigue condition, the participants under the post-fatigue condition demonstrated: (1) greater body sway during quiet standing but smaller body sway during perturbed standing tests, (2) increased neck muscle activations and decreased lumbar muscle activations, and (3) increased time to maximal head acceleration. As a whole, these information revealed that the patients with chronic neck pain did show poor postural control compared with the asymptomatic controls during quiet standing. However, after neck muscle fatigue, both groups demonstrated comparable restricted postural control in perturbed condition. In summary, under the less challenging condition, the presence of pain alone appears to cause postural control disturbances. With muscle fatigue, both group employed a rigid strategy to guard and minimize head motions. This fatigue appears to have an overriding impact on the postural control over the presence of pain. The current results indicated no interaction between the pain and fatigue factors. The main effects revealed that muscle fatigue appears to have a predominant influence on the balance control regardless of pain status. One plausible explanation was that the participants were mostly young adults. It has been documented that healthy adults tend to adopt a rigid strategy against large perturbations [23]. This is the first study to show that muscle fatigue is a more prevailing factor over pain and could result in the
Please cite this article in press as: Cheng C-H, et al. Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain. Gait Posture (2015), http://dx.doi.org/ 10.1016/j.gaitpost.2015.02.007
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Fig. 2. Averaged anteroposterior and mediolateral of displacement, sway area, and velocity of center of pressure under (a) quiet standing, and (b) external perturbation before and after fatigue conditions in patients with chronic neck pain (CNP) and asymptomatic control. * indicates p < 0.05.
Please cite this article in press as: Cheng C-H, et al. Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain. Gait Posture (2015), http://dx.doi.org/ 10.1016/j.gaitpost.2015.02.007
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Table 1 Mean values with standard deviation of the center of pressure, muscle activation (normalized averaged integration of EMG, NAIEMG), and time to maximal acceleration before and after fatigue conditions in patients with chronic neck pain (CNP) and asymptomatic control. Control
CNP Pre-fatigue Center of pressure (under quiet standing) Anteroposterior displacement (mm) Mediolateral displacement (mm) Sway area (mm2) Velocity (mm/s)
Post-fatigue
Pre-fatigue
Post-fatigue
10.5 4.3 16.3 5.4 79.3 60.0 5.4 1.2
13.0 4.7 16.5 5.5 90.1 59.3 5.3 1.4
7.7 3.5 12.9 4.1 41.6 26.4 4.5 1.1
8.8 3.4 12.7 4.0 51.0 38.3 4.5 1.0
Center of pressure (under external perturbation) Anteroposterior displacement (mm) Mediolateral displacement (mm) Sway area (mm2) Velocity (mm/s)
28.2 4.9 13.4 4.7 336.4 160.4 36.2 6.8
27.1 6.2 12.6 4.5 278.6 122.4 34.0 7.3
25.5 2.5 13.4 5.4 293.6 117.1 34.5 5.4
24.7 2.7 12.3 4.1 255.1 112.0 33.1 4.0
Muscle activation (under external perturbation) Sternocleidomastoids Semispinalis capitis Rectus abdominis Erector spinae
0.08 0.05 0.45 0.24 0.38 0.22 0.36 0.25
0.09 0.07 0.46 0.23 0.30 0.22 0.29 0.19
0.05 0.03 0.37 0.19 0.56 0.34 0.40 0.31
0.07 0.05 0.42 0.25 0.43 0.33 0.31 0.22
Time to maximal acceleration (under external perturbation) Head (ms) 276.4 15.5 Upper trunk (ms) 189.2 16.5 Lower trunk (ms) 244.1 31.7
285.2 24.8 193.6 10.5 244.8 37.6
279.9 19.6 183.6 24.4 230.9 24.5
299.5 34.3 189.8 18.7 229.6 33.9
adaptation of a ‘‘stiffened’’ posture in young adults regardless of neck pain. Further investigation is warranted if such strategy also exhibited in the mid-aged and elderly with chronic neck pain. Patients with neck pain showed greater body sway compared with the asymptomatic subjects during the quiet standing test, but not under the perturbed standing test. In addition, patients with neck pain showed a trend of increased neck muscle activations under external perturbations. The results indicated that chronic neck pain, even in young adults, could pose challenges to the postural control system. However, when subjected to external
perturbations, the young patients were still capable of maintaining balance as the asymptomatic subjects. The results indicated that patients with neck pain employed high activations of both the neck flexor and extensor muscles in an attempt to maintain their head position when perturbed. Participants in the current study were subjected to a large pulling force which equates to 15% of body weight comparing with the 3% of body weight used in previous similar studies [24]. Since the perturbation with 20% of body weight would induce stepping reactions [25], the ‘‘head strategy’’ used by the young patients seemed to be sufficient to maintain the
Fig. 3. Muscle activation (normalized averaged integration of EMG, NAIEMG) of sternocleidomastoids (SCM), semispinalis capitis (SSC), rectus abdominis (RA) and erector spinae (ES) under external perturbation before and after fatigue conditions in patients with chronic neck pain (CNP) and asymptomatic control. * indicates p < 0.05.
Please cite this article in press as: Cheng C-H, et al. Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain. Gait Posture (2015), http://dx.doi.org/ 10.1016/j.gaitpost.2015.02.007
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Fig. 4. Time to maximal acceleration of the top of head, upper trunk (UT) and lower trunk (LT) under external perturbation before and after fatigue conditions in patients with chronic neck pain (CNP) and asymptomatic control. * indicates p < 0.05.
balance within in situ status. Furthermore, given the previous reports of greater body sway in trauma-induced neck pain patients [24], our study provided a comparable pattern of body sway in chronic neck pain patients. Most studies to date have focused on the impact of neck extensor fatigue on the balance control [26]. Given the high densities of muscle spindles in the neck flexors and their fatigability in patients with neck pain [6,27], this is the first study, to the best of our knowledge, to determine if neck flexor fatigue would affect the postural control. The induction of neck flexor fatigue in current study resulted in an increased body sway during quiet standing, but a decreased body sway during perturbed standing, regardless of neck pain status. After the neck flexor fatigue, both the patients and the asymptomatic subjects demonstrated an increased activation of the neck flexors but a decreased activation of the lumbar flexors. The time to maximal head acceleration was also delayed under the fatigue condition. These results indicated that the neck flexor fatigue would deteriorate the postural control during quiet standing, while the young subjects adopted a rigid strategy against the external perturbation. The increased activation of the neck flexor and the increased time to maximal head acceleration indicated a state of head stabilization, and the decreased activation of the lumbar flexor were to balance the trunk perturbations. The possible ‘‘headfirst’’ or ‘‘fatigued-segment’’ protection strategy could be crucial against external perturbations. Further studies are warranted to verify if such strategy works in the aged population. This study also compared the relationships between pain and disability level and the balance parameters. No significant correlations were found but one: a moderate correlation between the VAS and the ‘‘RA activation in the post-fatigue condition’’. Our finding is consistent with a previous study examining patients with traumatic neck pain and found measurements like VAS and NDI correlated poorly with the head proprioceptive function [28]. Another study with 127 subjects found that pain frequency had a higher association with head proprioceptive function while the influence of pain intensity was inconsistent [29]. 4.1. Limitation in this study Some limitations should be addressed. The ages of the participants were between 20 and 30 years old, whereas the population with neck pain are commonly middle-aged. In addition, the muscle fatigue status was self-reported. Though no objective
technique was employed to verify the true muscle fatigue status in the current study design, previous studies have shown that the median frequency slopes of contractions until subjective exhaustion present reliable results and 30–50 Hz decrement of the median frequency can indicate the fatigue of neck muscles [30].
5. Conclusions Current results provided evidence that the young subjects adopted a rigid strategy for neck and lumbar muscles during external perturbation with neck pain or neck flexor fatigue. The results facilitate the understanding of the strategies subjects with chronic neck pain would choose under challenging conditions. Further studies are needed to verify if similar strategy exists in the aged population. The results also inspire the development of specific exercise programs for improving balance control in patients with chronic neck pain. Acknowledgments We gratefully acknowledge all the participants and the supports of the Ministry of Science and Technology of the Republic of China and Chang Gung Memorial Hospital Research Program, to this research under the grants 101-2221-E-182-020-MY3 and CMRPD1D0121 respectively. Conflict of interest: The authors declare that they have no conflict of interest.
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Please cite this article in press as: Cheng C-H, et al. Changes of postural control and muscle activation pattern in response to external perturbations after neck flexor fatigue in young subjects with and without chronic neck pain. Gait Posture (2015), http://dx.doi.org/ 10.1016/j.gaitpost.2015.02.007