- Email: [email protected]
Neck muscle vibration produces diverse responses in balance and gait speed between individuals with and without neck pain
Accepted Manuscript Neck muscle vibration produces diverse responses in balance and gait speed between individuals with and without neck pain Nipaporn Wannaprom, Julia Treleaven, Gwendolen Jull, Sureeporn Uthaikhup PII:
S2468-7812(18)30041-9
DOI:
10.1016/j.msksp.2018.02.001
Reference:
MSKSP 162
To appear in:
Musculoskeletal Science and Practice
Received Date: 20 September 2017 Accepted Date: 2 February 2018
Please cite this article as: Wannaprom, N., Treleaven, J., Jull, G., Uthaikhup, S., Neck muscle vibration produces diverse responses in balance and gait speed between individuals with and without neck pain, Musculoskeletal Science and Practice (2018), doi: 10.1016/j.msksp.2018.02.001. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Neck muscle vibration produces diverse responses in balance and gait speed between individuals with and without neck pain
Department of Physical Therapy, Faculty of Associated Medical Sciences, Chiang Mai
University, Thailand b
Division of Physiotherapy, School of Health and Rehabilitation Sciences, The University of
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Queensland, St Lucia, Brisbane, Australia
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a
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Nipaporn Wannaproma, Julia Treleavenb, Gwendolen Jullb, Sureeporn Uthaikhupa,*
*Corresponding author
Dr. Sureeporn Uthaikhup
Department of Physical Therapy, Faculty of Associated Medical Sciences, Chiang Mai University, Chiang Mai, Thailand, 50200 Phone: 0-5394-9249 Email: [email protected]
ACCEPTED MANUSCRIPT Abstract Background: Neck muscle vibration can influence cervical proprioception and sensorimotor function. It is hypothesized to affect motor performance differently in persons with and without neck pain.
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Study design: Cross-sectional study
Objective: To clarify the extent to which vibration-induced motor responses of neck muscles affect static standing balance and gait speed in persons with and without neck pain.
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Methods: Thirty participants with chronic neck pain and 30 healthy controls were recruited. Balance and gait were measured before and after 30 seconds of suboccipital neck muscle
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vibration. Balance was measured in a confortable stance with eyes closed using a swaymeter and gait using the timed 10 meter walk test.
Results: At baseline, neck pain participants had greater postural sway, particularly in the anterior-posterior direction and slower gait speed than healthy controls (p < 0.001).
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Immediately after vibration, neck pain participants displayed decreased postural sway, and increased gait speed (p < 0.001). Healthy controls had increased postural sway and decreased gait speed (p < 0.001).
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Conclusion: Neck muscle vibration improved standing balance and gait speed in participants
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with neck pain but reduced performance in healthy controls. The study supports the importance of cervical proprioceptive information in postural control. Use of vibration could be considered neck pain patients’ rehabilitation.
Keywords: balance, gait, neck pain, postural control, proprioception, vibration.
ACCEPTED MANUSCRIPT Neck muscle vibration produces diverse responses in balance and gait speed between
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individuals with and without neck pain
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ACCEPTED MANUSCRIPT 1. Introduction The maintenance of postural control and locomotion engages sensory information from the visual, vestibular, proprioceptive and somatosensory systems (Mergner and Rosemeier, 1998). Afferent signals from the cervical region, in particular the deep cervical
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muscles, are vital for proprioceptive information (Boyd-Clark et al., 2002; Kulkarni et al., 2001). The central nervous system interprets muscle proprioceptive information in relation to the status of the vestibular input to produce an accurate response for the maintenance of
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vertical posture (Hlavacka et al., 1996; Popov et al., 1999a). However, the information
al., 1993; Courtine et al., 2003).
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acquired and the interaction may vary between static and dynamic postural tasks (Britton et
Understanding the precise interaction between neck muscle proprioception and other sensory systems is important to facilitate improved management of balance and gait disturbances. The interaction is often studied via neck muscle vibration (Lund, 1980; Popov
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et al., 1999b; Roll et al., 1989b) as vibration is an adequate and reproducible stimulus for selectively activating muscle spindle primary endings and eliciting discharge in Ia afferent fibers (Roll et al., 1989a). There is some evidence that neck muscle vibration, like calf
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muscle vibration, primarily induces body movements in an anterior-posterior direction (Ivanenko et al., 1999; Patel et al., 2009) with resultant alterations in postural balance and
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gait (Bove et al., 2002; Courtine et al., 2003; Fransson et al., 2007; Gomez et al., 2009). Increased postural sway and a deviation of the trajectory during gait have been demonstrated after neck muscle vibration in healthy subjects (Bove et al., 2001; Bove et al., 2009; Kavounoudias et al., 1999). The vibration is thought to provoke alteration to cervical proprioceptive input (Bove et al., 2009). Nevertheless, some subjects with neck pain are thought to have already have abnormal cervical proprioceptive input which presents as impaired sensorimotor control (i.e. joint position error, impaired head-eye movement control
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ACCEPTED MANUSCRIPT and impaired balance) (Field et al., 2008; Storaci et al., 2006; Treleaven et al., 2003) Thus neck pain patient’s responses to cervical muscle vibration may be different. Recent studies support this notion. They show neck muscle vibration has opposite effects in patients and healthy subjects (Beinert et al., 2015; Muceli et al., 2011). Muceli et al.
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(2011) determined the effect of short-term neck muscle vibration, showing improved cervical force steadiness in patients with neck pain. Similarly, Beinert et al. (2015) demonstrated improved joint position sense and reduced dynamic postural sway after vibration in neck pain
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patients but reduced joint position sense acuity and likely increased postural sway in healthy controls. However, there was no effect of neck muscle vibration on static postural control in
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either group, which may be associated with task difficulty or the methodological approach (Beinert et al., 2015). Responses in gait to neck muscle vibration have not been determined, which could be important given that gait disturbance is not uncommon in association with neck pain (Poole et al., 2008; Stokell et al., 2011; Uthaikhup et al., 2014).
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The aim of this study was to clarify the extent of vibration-induced motor responses of neck muscles on both static standing balance and gait speed in persons with and without neck pain. It was hypothesized that after vibration, standing balance and gait speed would
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improve in persons with neck pain and decline in those without neck pain. Understanding the
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precise influence of neck vibration on postural stability and gait in individuals with neck pain may improve therapeutic interventions.
2. Methods
2.1. Participants Thirty participants with neck pain and 30 healthy controls of a similar age, weight and height were recruited for the study from local hospitals, physical therapy clinics, the university and community. To be eligible for the study, participants with neck pain had to
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ACCEPTED MANUSCRIPT have neck pain for more than 3 months, have no radicular pain, and have a score of at least 10/100 on the Neck Disability Index-Thai version (Uthaikhup et al., 2011). Inclusion criteria for the control group were no history of either neck pain, frequent intermittent headache or dizziness in the past 6 months. Participants were excluded from the study if they had a
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previous history of neck injury, known or suspected vestibular pathology, any neurological deficit, musculoskeletal problem(s) that could affect balance and gait speed tests, or were taking more than four medications (Huang et al., 2010). The participants were asked to
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refrain from consuming alcohol and taking analgesic/muscle relaxant medications on the day of testing.
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The study was approved by the research ethics committee (AMSEC-60EX-023) and was conducted in accordance with the declaration of Helsinki. All participants received information about the study and they provided informed consent prior to commencement of
2.2. Balance measure
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the study.
A swaymeter developed by Lord et al. (Lord et al., 2003) was used to measure postural
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sway in standing. The swaymeter is a reliable and valid device to assess postural sway
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(Sturnieks et al., 2011) and has been widely used in populations with balance impairment (Hinman et al., 2002; Lord et al., 2003; Thakker and Elumalai, 2015). The device comprises a 40-cm-long rod with a vertically mounted pen at its end. The rod was attached to the participants with a firm belt and it extended posteriorly at the level of the posterior superior iliac spines. Participants were asked to stand barefoot, as still as possible, for 30 seconds in comfortable stance (feet approximately shoulder width apart and arms at the sides) on a firm surface with eyes closed (Figure 1). The tip of the pen recorded participant’s postural sway on a millimeter graph paper fastened to the top of an adjustable-height table. The postural
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ACCEPTED MANUSCRIPT sway was computed in the maximum anterior-posterior (AP) and medial-lateral (ML) sway displacements and total sway area (AP x ML).
2.3. Gait speed measure
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Gait speed was measured using the timed 10 meter walk test. The participants walked barefoot along a 10-m walkway at their maximum speed. Time was recorded with a digital stopwatch over the intermediate 6 of the 10 meters to allow for acceleration and deceleration
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(Lindemann et al., 2008). At the start point, an examiner said that “I will say ready, set, go. When I say go, walk as fast as you safely can until I say stop” (Marques et al., 2016). Time
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starts when the toes of the leading foot cross the 2-meter mark and stops when the toes of the leading foot cross the 8-meter mark. Each participant performed the test twice (Bohannon, 1997). Gait speed was computed for each trial and the mean value was used for analysis.
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2.4. Neck muscle vibration
Neck muscle vibration was applied using a vibration device (Thrive MD-01, Thrive Co.,Ltd., Osaka, Japan) with a 5 cm diameter round head, a frequency of 100 Hz and an
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amplitude of 1.0 mm (Kamada et al., 2011). The vibrator was placed centrally on the skin
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above C2 spinous process (suboccipital region) for 30 seconds with sufficient pressure to maintain firm contact (Bove et al., 2009). The vibration head was kept in place throughout the session.
2.5. Experimental protocol The experiment consisted of two sessions: a balance session and a gait session, with 30 minute rest between each session. The experiment was performed in a standard order in both neck pain and control groups by an examiner who was blinded to the participant’s status.
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ACCEPTED MANUSCRIPT Session 1-balance: postural sway during standing with eyes closed was measured at baseline. Participants then sat on a chair and neck muscle vibration was applied over the suboccipital region for 30 seconds. Postural sway was measured again immediately after vibration. Any adverse effect was recorded during and after neck muscle vibration.
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Session 2-gait: the participants performed two trials of the timed 10 meter walk test for the baseline measurement. The participants once again sat on a chair and neck muscle vibration was applied over the suboccipital region for 30 seconds. Two trials of the timed 10
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meter walk test were measured again immediately after the vibration.
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2.6. Statistical analysis
Sample size calculation was based on our pilot study (5 neck pain subjects and 5 controls). According to the postural sway and gait speed data, a total sample size required for the study was 34 (effect size = 0.25, power = 0.8 and significant level = 0.05) and 54 (effect
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size = 0.16, power = 0.8 and significant level = 0.05), respectively. Independent t-tests were used to identify significant differences in demographic data between groups. Kolmogorov-Smirnov tests were used to determine the distribution of the
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outcome measures (p > 0.05). Two-way mixed model ANOVA was used to analyze between-
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groups (neck pain vs. control) and within-subjects (before vs. after vibration) factors for the balance and gait outcomes. Significance was defined as p < 0.05. All statistical analyses were conducted using SPSS statistical package.
3. Results 3.1. Participant demographics Demographic data for the neck pain and control groups are presented in Table 1. There were no significant differences in age, gender and body mass index between the groups
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ACCEPTED MANUSCRIPT (all p > 0.05). Three (10.0 %) participants with neck pain took pain killers to relieve pain and 14 (46.7%) received other treatment including modalities, massage and acupuncture.
3.2. Balance
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All participants received and tolerated vibration for 30 seconds and no adverse events were reported in either group.
The analyses of balance and gait revealed similar patterns of responses for each
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measure in each group.
Total sway area: The mixed model ANOVA revealed a significant interaction effect
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between group and time (F1, 58 = 63.3, p < 0.001). Prior to vibration, the neck pain group had a larger mean sway area than controls (p < 0.001). Following vibration, the neck pain group demonstrated a decreased area of postural sway (p < 0.001) while in the control group postural sway area increased (p < 0.01) (Figure 2). The net effect was that there was no
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between group difference in sway area after vibration (p > 0.05).
Sway displacement (anterior-posterior): The mixed model ANOVA revealed a significant interaction effect between group and time (F1,
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= 78.0, p < 0.001). Before
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vibration, again the neck pain group had larger AP sway displacement than the control group
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(p < 0.001). Following vibration, the neck pain group displayed decreased AP sway displacement (p < 0.001) while the control group had increased AP sway displacement (p < 0.001) (Figure 3). There was no difference between groups after vibration (p > 0.05). Sway displacement (medial-lateral): The mixed model ANOVA revealed a significant interaction effect between group and time (F1, 58 = 68.1, p < 0.001). Before vibration, the neck pain group had larger ML sway displacement than the control group (p < 0.001). After vibration, the neck pain group had decreased ML sway displacement (p < 0.001) and the
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ACCEPTED MANUSCRIPT control group had increased ML sway displacement (p < 0.001) (Figure 4). There was no between group difference after vibration (p > 0.05).
3.3. Gait speed
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All participants received vibration for 30 seconds and there were no adverse events in either group.
The mixed model ANOVA results revealed a significant interaction between group 58
= 35.1, p < 0.001). Before vibration, the neck pain group had slower gait
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and time (F1,
speed than healthy controls (p < 0.01). After vibration, gait speed in the neck pain group
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increased (p < 0.001) while it decreased in the control group (p < 0.001) (Figure 5). Again the net effect was that there was no between group difference in gait speed after vibration (p > 0.05).
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4. Discussion
The study demonstrated that neck muscle vibration improved standing balance and gait speed in participants with neck pain but reduced performance in healthy controls. This
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supports the notion that neck muscle vibration affects motor performance differently in
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persons with and without neck pain (Beinert et al., 2015; Muceli et al., 2011). Additionally, the results confirm the presence of impairments in standing balance and gait in association with neck pain (Field et al., 2008; Sjostrom et al., 2003; Uthaikhup et al., 2014) and the importance of proprioceptive information from the cervical spine in postural control. As expected, at baseline, participants with neck pain had greater postural sway particularly in the AP direction and slower gait speed than healthy controls, which is consistent with findings of previous studies demonstrating impaired balance (Field et al., 2008; Treleaven et al., 2005; Treleaven et al., 2008) and impaired gait characteristics in
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ACCEPTED MANUSCRIPT patients with neck pain (Poole et al., 2008; Uthaikhup et al., 2014). The results indicate that altered cervical proprioceptive information plays a particularly important role in controlling balance during standing and locomotion in such patients. A mismatch between altered
of the impaired balance and gait (Treleaven, 2008).
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cervical proprioceptive signals and normal vestibular and visual signals is a suggested cause
The results of this study indicate a positive effect of neck muscle vibration on both balance control in standing and gait in neck pain participants. These participants had reduced
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postural sway, predominantly in the AP direction during standing, and increased speed during walking following vibration. Similarly, a recent study demonstrated improved dynamic
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postural stability using the postural perturbation test under a single leg stance after neck muscle vibration in neck pain patients (Beinert et al., 2015). The integration of multisensory information is dynamically regulated to adapt to the available sensory inputs (Peterka, 2002; Peterka and Loughlin, 2004). When there is a large conflict of multisensory information, the
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vestibular input is trusted and its weight is increased while the proprioceptive weighting declines (Hwang et al., 2014; Mahboobin et al., 2009). Improved balance and gait performance displayed in our neck pain group may be explained by reweighting of sensory
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inputs following neck muscle vibration. Neck muscle vibration at frequency between 80-120
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Hz is a good stimulus for Ia afferent fibers originating in the muscle spindles (Burke et al., 1976; Roll and Vedel, 1982). Unreliable cervical proprioceptive input from muscle spindles may be suppressed by the reweighting process. Alternatively it is possible that in the presence of neck pain, deficits in balance and gait are due to decreased cervical proprioceptive input which is improved and normalized by adding vibration. In contrast to those with neck pain, the healthy control group had increased postural sway particularly in the AP direction and decreased gait speed in response to vibration. These results confirm previous research in healthy controls (Bove et al., 2001; Bove et al., 2009;
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ACCEPTED MANUSCRIPT Kavounoudias et al., 1999). Vibration may alter cervical proprioception and/or vestibular input in this group (Karnath, 1994) resulting in an imbalance in sensory afferent input and excessive sensory noise within the sensorimotor system (Beinert et al., 2015; Bove et al., 2009). Healthy participants may need to adapt their gait speed in the direction of vibration
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induced illusion (i.e. forward) to compensate for the postural instability created.
From the clinical perspective, the findings of the current study suggest that vibration may improve balance and gait in persons with neck pain. Neck muscle vibration is non-
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invasive and easy to apply and future research exploring the potential for its use in rehabilitation in patients who have impaired balance control during standing and gait is
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warranted. However, the exact approach needs further exploration. The current study is limited only to the immediate effect of neck muscle vibration. Further research should also determine whether neck muscle vibration causes any long-term benefits for patients with
5. Conclusion
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neck pain.
Neck muscle vibration affects motor performance differently in persons with and
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without neck pain. Participants with neck pain displayed significantly improved standing
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balance and gait speed whereas healthy participants showed an impaired standing balance and gait speed, immediately after vibration. The importance of cervical proprioceptive information in controlling balance during standing and walking should be taken into account for rehabilitation in patients with neck pain.
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ACCEPTED MANUSCRIPT Poole, E., Treleaven, J., Jull, G., 2008. The influence of neck pain on balance and gait parameters in community-dwelling elders. Man Ther. 13, 317-24. Popov, K.E., Kozhina, G.V., Smetanin, B.N., Shlikov, V.Y., 1999a. Postural responses to combined vestibular and hip proprioceptive stimulation in man. Eur J Neurosci. 11,
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ACCEPTED MANUSCRIPT Thakker, H., Elumalai, S., 2015. Static and dynamic postural stability in subjects with and without chronic low back pain. Int J Res Med Sci. 3, 2405-9. Treleaven, J., 2008. Sensorimotor disturbances in neck disorders affecting postural stability, head and eye movement control. Man Ther. 13, 2-11.
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Treleaven, J., LowChoy, N., Darnell, R., Panizza, B., Brown-Rothwell, D., Jull, G., 2008. Comparison of sensorimotor disturbance between subjects with persistent whiplashassociated disorder and subjects with vestibular pathology associated with acoustic neuroma. Arch Phys Med Rehabil. 89, 522-30.
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Uthaikhup, S., Sunkarat, S., Khamsaen, K., Meeyan, K., Treleaven, J., 2014. The effects of
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ACCEPTED MANUSCRIPT Figure legends Figure 1: Standing balance measure using a swaymeter.
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pain and control groups. (* p < 0.01, ** p < 0.001)
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Figure 2: Mean and standard error of total sway area before and after vibration for the neck
Figure 3: Mean and standard error of sway displacement (anterior-posterior) between the
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neck pain and controls groups at baseline and immediately after vibration. (** p < 0.001)
Figure 4: Mean and standard error of sway displacement (medial-lateral) the neck pain and
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controls groups at baseline and immediately after vibration. (** p < 0.001)
Figure 5: Mean and standard error of gait speed obtained from the neck pain and controls
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groups at baseline and immediately after vibration. (* p < 0.01, ** p < 0.001)
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ACCEPTED MANUSCRIPT Acknowledgement
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The study was supported by Faculty of Associated Medical Sciences, Chiang Mai University.
ACCEPTED MANUSCRIPT Table 1 Baseline characteristics of participants with neck pain and healthy controls. Controls (n = 30)
Age (years)
31.5 ± 10.5
29.5 ± 10.2
Gender (% female)
56.7
56.7
Weight (kg)
65.1 ± 15.6
Height (cm)
164.4 ± 10.0
Body mass index (kg/m2)
24.0 ± 5.0
Side of pain (% bilateral)
80.0
Neck pain intensity (0 – 10 VAS)
59.9 ± 11.9
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162.5 ± 10.0 22.7 ± 4.1
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22.3 ± 12.9
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5.1 ± 2.0
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29.6 ± 29.9
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Neck pain duration (months)
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Neck disability index (%)
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Neck pain (n = 30)
3.5 ± 2.2
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Pain on the testing day (%)
86.7
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26.7
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Dizziness (%)
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Neck pain frequency (days per week)
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Data are presented as mean ± sd unless otherwise indicated. NDI = Neck Disability Index, VAS = Visual Analogue Scale.
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Highlights Cervical proprioception is important for controlling balance and gait
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Greater AP postural sway and slower gait speed occurs with neck pain
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Vibration effects balance and gait positively in neck pain and negatively in controls
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Neck muscle vibration has potential for rehabilitation of neck pain
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S2468-7812(18)30041-9
DOI:
10.1016/j.msksp.2018.02.001
Reference:
MSKSP 162
To appear in:
Musculoskeletal Science and Practice
Received Date: 20 September 2017 Accepted Date: 2 February 2018
Please cite this article as: Wannaprom, N., Treleaven, J., Jull, G., Uthaikhup, S., Neck muscle vibration produces diverse responses in balance and gait speed between individuals with and without neck pain, Musculoskeletal Science and Practice (2018), doi: 10.1016/j.msksp.2018.02.001. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Neck muscle vibration produces diverse responses in balance and gait speed between individuals with and without neck pain
Department of Physical Therapy, Faculty of Associated Medical Sciences, Chiang Mai
University, Thailand b
Division of Physiotherapy, School of Health and Rehabilitation Sciences, The University of
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Queensland, St Lucia, Brisbane, Australia
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a
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Nipaporn Wannaproma, Julia Treleavenb, Gwendolen Jullb, Sureeporn Uthaikhupa,*
*Corresponding author
Dr. Sureeporn Uthaikhup
Department of Physical Therapy, Faculty of Associated Medical Sciences, Chiang Mai University, Chiang Mai, Thailand, 50200 Phone: 0-5394-9249 Email: [email protected]
ACCEPTED MANUSCRIPT Abstract Background: Neck muscle vibration can influence cervical proprioception and sensorimotor function. It is hypothesized to affect motor performance differently in persons with and without neck pain.
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Study design: Cross-sectional study
Objective: To clarify the extent to which vibration-induced motor responses of neck muscles affect static standing balance and gait speed in persons with and without neck pain.
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Methods: Thirty participants with chronic neck pain and 30 healthy controls were recruited. Balance and gait were measured before and after 30 seconds of suboccipital neck muscle
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vibration. Balance was measured in a confortable stance with eyes closed using a swaymeter and gait using the timed 10 meter walk test.
Results: At baseline, neck pain participants had greater postural sway, particularly in the anterior-posterior direction and slower gait speed than healthy controls (p < 0.001).
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Immediately after vibration, neck pain participants displayed decreased postural sway, and increased gait speed (p < 0.001). Healthy controls had increased postural sway and decreased gait speed (p < 0.001).
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Conclusion: Neck muscle vibration improved standing balance and gait speed in participants
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with neck pain but reduced performance in healthy controls. The study supports the importance of cervical proprioceptive information in postural control. Use of vibration could be considered neck pain patients’ rehabilitation.
Keywords: balance, gait, neck pain, postural control, proprioception, vibration.
ACCEPTED MANUSCRIPT Neck muscle vibration produces diverse responses in balance and gait speed between
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individuals with and without neck pain
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ACCEPTED MANUSCRIPT 1. Introduction The maintenance of postural control and locomotion engages sensory information from the visual, vestibular, proprioceptive and somatosensory systems (Mergner and Rosemeier, 1998). Afferent signals from the cervical region, in particular the deep cervical
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muscles, are vital for proprioceptive information (Boyd-Clark et al., 2002; Kulkarni et al., 2001). The central nervous system interprets muscle proprioceptive information in relation to the status of the vestibular input to produce an accurate response for the maintenance of
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vertical posture (Hlavacka et al., 1996; Popov et al., 1999a). However, the information
al., 1993; Courtine et al., 2003).
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acquired and the interaction may vary between static and dynamic postural tasks (Britton et
Understanding the precise interaction between neck muscle proprioception and other sensory systems is important to facilitate improved management of balance and gait disturbances. The interaction is often studied via neck muscle vibration (Lund, 1980; Popov
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et al., 1999b; Roll et al., 1989b) as vibration is an adequate and reproducible stimulus for selectively activating muscle spindle primary endings and eliciting discharge in Ia afferent fibers (Roll et al., 1989a). There is some evidence that neck muscle vibration, like calf
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muscle vibration, primarily induces body movements in an anterior-posterior direction (Ivanenko et al., 1999; Patel et al., 2009) with resultant alterations in postural balance and
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gait (Bove et al., 2002; Courtine et al., 2003; Fransson et al., 2007; Gomez et al., 2009). Increased postural sway and a deviation of the trajectory during gait have been demonstrated after neck muscle vibration in healthy subjects (Bove et al., 2001; Bove et al., 2009; Kavounoudias et al., 1999). The vibration is thought to provoke alteration to cervical proprioceptive input (Bove et al., 2009). Nevertheless, some subjects with neck pain are thought to have already have abnormal cervical proprioceptive input which presents as impaired sensorimotor control (i.e. joint position error, impaired head-eye movement control
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ACCEPTED MANUSCRIPT and impaired balance) (Field et al., 2008; Storaci et al., 2006; Treleaven et al., 2003) Thus neck pain patient’s responses to cervical muscle vibration may be different. Recent studies support this notion. They show neck muscle vibration has opposite effects in patients and healthy subjects (Beinert et al., 2015; Muceli et al., 2011). Muceli et al.
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(2011) determined the effect of short-term neck muscle vibration, showing improved cervical force steadiness in patients with neck pain. Similarly, Beinert et al. (2015) demonstrated improved joint position sense and reduced dynamic postural sway after vibration in neck pain
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patients but reduced joint position sense acuity and likely increased postural sway in healthy controls. However, there was no effect of neck muscle vibration on static postural control in
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either group, which may be associated with task difficulty or the methodological approach (Beinert et al., 2015). Responses in gait to neck muscle vibration have not been determined, which could be important given that gait disturbance is not uncommon in association with neck pain (Poole et al., 2008; Stokell et al., 2011; Uthaikhup et al., 2014).
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The aim of this study was to clarify the extent of vibration-induced motor responses of neck muscles on both static standing balance and gait speed in persons with and without neck pain. It was hypothesized that after vibration, standing balance and gait speed would
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improve in persons with neck pain and decline in those without neck pain. Understanding the
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precise influence of neck vibration on postural stability and gait in individuals with neck pain may improve therapeutic interventions.
2. Methods
2.1. Participants Thirty participants with neck pain and 30 healthy controls of a similar age, weight and height were recruited for the study from local hospitals, physical therapy clinics, the university and community. To be eligible for the study, participants with neck pain had to
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ACCEPTED MANUSCRIPT have neck pain for more than 3 months, have no radicular pain, and have a score of at least 10/100 on the Neck Disability Index-Thai version (Uthaikhup et al., 2011). Inclusion criteria for the control group were no history of either neck pain, frequent intermittent headache or dizziness in the past 6 months. Participants were excluded from the study if they had a
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previous history of neck injury, known or suspected vestibular pathology, any neurological deficit, musculoskeletal problem(s) that could affect balance and gait speed tests, or were taking more than four medications (Huang et al., 2010). The participants were asked to
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refrain from consuming alcohol and taking analgesic/muscle relaxant medications on the day of testing.
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The study was approved by the research ethics committee (AMSEC-60EX-023) and was conducted in accordance with the declaration of Helsinki. All participants received information about the study and they provided informed consent prior to commencement of
2.2. Balance measure
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the study.
A swaymeter developed by Lord et al. (Lord et al., 2003) was used to measure postural
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sway in standing. The swaymeter is a reliable and valid device to assess postural sway
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(Sturnieks et al., 2011) and has been widely used in populations with balance impairment (Hinman et al., 2002; Lord et al., 2003; Thakker and Elumalai, 2015). The device comprises a 40-cm-long rod with a vertically mounted pen at its end. The rod was attached to the participants with a firm belt and it extended posteriorly at the level of the posterior superior iliac spines. Participants were asked to stand barefoot, as still as possible, for 30 seconds in comfortable stance (feet approximately shoulder width apart and arms at the sides) on a firm surface with eyes closed (Figure 1). The tip of the pen recorded participant’s postural sway on a millimeter graph paper fastened to the top of an adjustable-height table. The postural
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ACCEPTED MANUSCRIPT sway was computed in the maximum anterior-posterior (AP) and medial-lateral (ML) sway displacements and total sway area (AP x ML).
2.3. Gait speed measure
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Gait speed was measured using the timed 10 meter walk test. The participants walked barefoot along a 10-m walkway at their maximum speed. Time was recorded with a digital stopwatch over the intermediate 6 of the 10 meters to allow for acceleration and deceleration
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(Lindemann et al., 2008). At the start point, an examiner said that “I will say ready, set, go. When I say go, walk as fast as you safely can until I say stop” (Marques et al., 2016). Time
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starts when the toes of the leading foot cross the 2-meter mark and stops when the toes of the leading foot cross the 8-meter mark. Each participant performed the test twice (Bohannon, 1997). Gait speed was computed for each trial and the mean value was used for analysis.
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2.4. Neck muscle vibration
Neck muscle vibration was applied using a vibration device (Thrive MD-01, Thrive Co.,Ltd., Osaka, Japan) with a 5 cm diameter round head, a frequency of 100 Hz and an
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amplitude of 1.0 mm (Kamada et al., 2011). The vibrator was placed centrally on the skin
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above C2 spinous process (suboccipital region) for 30 seconds with sufficient pressure to maintain firm contact (Bove et al., 2009). The vibration head was kept in place throughout the session.
2.5. Experimental protocol The experiment consisted of two sessions: a balance session and a gait session, with 30 minute rest between each session. The experiment was performed in a standard order in both neck pain and control groups by an examiner who was blinded to the participant’s status.
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ACCEPTED MANUSCRIPT Session 1-balance: postural sway during standing with eyes closed was measured at baseline. Participants then sat on a chair and neck muscle vibration was applied over the suboccipital region for 30 seconds. Postural sway was measured again immediately after vibration. Any adverse effect was recorded during and after neck muscle vibration.
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Session 2-gait: the participants performed two trials of the timed 10 meter walk test for the baseline measurement. The participants once again sat on a chair and neck muscle vibration was applied over the suboccipital region for 30 seconds. Two trials of the timed 10
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2.6. Statistical analysis
Sample size calculation was based on our pilot study (5 neck pain subjects and 5 controls). According to the postural sway and gait speed data, a total sample size required for the study was 34 (effect size = 0.25, power = 0.8 and significant level = 0.05) and 54 (effect
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size = 0.16, power = 0.8 and significant level = 0.05), respectively. Independent t-tests were used to identify significant differences in demographic data between groups. Kolmogorov-Smirnov tests were used to determine the distribution of the
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outcome measures (p > 0.05). Two-way mixed model ANOVA was used to analyze between-
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groups (neck pain vs. control) and within-subjects (before vs. after vibration) factors for the balance and gait outcomes. Significance was defined as p < 0.05. All statistical analyses were conducted using SPSS statistical package.
3. Results 3.1. Participant demographics Demographic data for the neck pain and control groups are presented in Table 1. There were no significant differences in age, gender and body mass index between the groups
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ACCEPTED MANUSCRIPT (all p > 0.05). Three (10.0 %) participants with neck pain took pain killers to relieve pain and 14 (46.7%) received other treatment including modalities, massage and acupuncture.
3.2. Balance
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All participants received and tolerated vibration for 30 seconds and no adverse events were reported in either group.
The analyses of balance and gait revealed similar patterns of responses for each
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measure in each group.
Total sway area: The mixed model ANOVA revealed a significant interaction effect
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between group and time (F1, 58 = 63.3, p < 0.001). Prior to vibration, the neck pain group had a larger mean sway area than controls (p < 0.001). Following vibration, the neck pain group demonstrated a decreased area of postural sway (p < 0.001) while in the control group postural sway area increased (p < 0.01) (Figure 2). The net effect was that there was no
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between group difference in sway area after vibration (p > 0.05).
Sway displacement (anterior-posterior): The mixed model ANOVA revealed a significant interaction effect between group and time (F1,
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= 78.0, p < 0.001). Before
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vibration, again the neck pain group had larger AP sway displacement than the control group
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(p < 0.001). Following vibration, the neck pain group displayed decreased AP sway displacement (p < 0.001) while the control group had increased AP sway displacement (p < 0.001) (Figure 3). There was no difference between groups after vibration (p > 0.05). Sway displacement (medial-lateral): The mixed model ANOVA revealed a significant interaction effect between group and time (F1, 58 = 68.1, p < 0.001). Before vibration, the neck pain group had larger ML sway displacement than the control group (p < 0.001). After vibration, the neck pain group had decreased ML sway displacement (p < 0.001) and the
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ACCEPTED MANUSCRIPT control group had increased ML sway displacement (p < 0.001) (Figure 4). There was no between group difference after vibration (p > 0.05).
3.3. Gait speed
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All participants received vibration for 30 seconds and there were no adverse events in either group.
The mixed model ANOVA results revealed a significant interaction between group 58
= 35.1, p < 0.001). Before vibration, the neck pain group had slower gait
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and time (F1,
speed than healthy controls (p < 0.01). After vibration, gait speed in the neck pain group
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increased (p < 0.001) while it decreased in the control group (p < 0.001) (Figure 5). Again the net effect was that there was no between group difference in gait speed after vibration (p > 0.05).
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4. Discussion
The study demonstrated that neck muscle vibration improved standing balance and gait speed in participants with neck pain but reduced performance in healthy controls. This
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supports the notion that neck muscle vibration affects motor performance differently in
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persons with and without neck pain (Beinert et al., 2015; Muceli et al., 2011). Additionally, the results confirm the presence of impairments in standing balance and gait in association with neck pain (Field et al., 2008; Sjostrom et al., 2003; Uthaikhup et al., 2014) and the importance of proprioceptive information from the cervical spine in postural control. As expected, at baseline, participants with neck pain had greater postural sway particularly in the AP direction and slower gait speed than healthy controls, which is consistent with findings of previous studies demonstrating impaired balance (Field et al., 2008; Treleaven et al., 2005; Treleaven et al., 2008) and impaired gait characteristics in
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ACCEPTED MANUSCRIPT patients with neck pain (Poole et al., 2008; Uthaikhup et al., 2014). The results indicate that altered cervical proprioceptive information plays a particularly important role in controlling balance during standing and locomotion in such patients. A mismatch between altered
of the impaired balance and gait (Treleaven, 2008).
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cervical proprioceptive signals and normal vestibular and visual signals is a suggested cause
The results of this study indicate a positive effect of neck muscle vibration on both balance control in standing and gait in neck pain participants. These participants had reduced
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postural sway, predominantly in the AP direction during standing, and increased speed during walking following vibration. Similarly, a recent study demonstrated improved dynamic
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postural stability using the postural perturbation test under a single leg stance after neck muscle vibration in neck pain patients (Beinert et al., 2015). The integration of multisensory information is dynamically regulated to adapt to the available sensory inputs (Peterka, 2002; Peterka and Loughlin, 2004). When there is a large conflict of multisensory information, the
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vestibular input is trusted and its weight is increased while the proprioceptive weighting declines (Hwang et al., 2014; Mahboobin et al., 2009). Improved balance and gait performance displayed in our neck pain group may be explained by reweighting of sensory
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inputs following neck muscle vibration. Neck muscle vibration at frequency between 80-120
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Hz is a good stimulus for Ia afferent fibers originating in the muscle spindles (Burke et al., 1976; Roll and Vedel, 1982). Unreliable cervical proprioceptive input from muscle spindles may be suppressed by the reweighting process. Alternatively it is possible that in the presence of neck pain, deficits in balance and gait are due to decreased cervical proprioceptive input which is improved and normalized by adding vibration. In contrast to those with neck pain, the healthy control group had increased postural sway particularly in the AP direction and decreased gait speed in response to vibration. These results confirm previous research in healthy controls (Bove et al., 2001; Bove et al., 2009;
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ACCEPTED MANUSCRIPT Kavounoudias et al., 1999). Vibration may alter cervical proprioception and/or vestibular input in this group (Karnath, 1994) resulting in an imbalance in sensory afferent input and excessive sensory noise within the sensorimotor system (Beinert et al., 2015; Bove et al., 2009). Healthy participants may need to adapt their gait speed in the direction of vibration
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induced illusion (i.e. forward) to compensate for the postural instability created.
From the clinical perspective, the findings of the current study suggest that vibration may improve balance and gait in persons with neck pain. Neck muscle vibration is non-
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invasive and easy to apply and future research exploring the potential for its use in rehabilitation in patients who have impaired balance control during standing and gait is
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warranted. However, the exact approach needs further exploration. The current study is limited only to the immediate effect of neck muscle vibration. Further research should also determine whether neck muscle vibration causes any long-term benefits for patients with
5. Conclusion
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neck pain.
Neck muscle vibration affects motor performance differently in persons with and
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without neck pain. Participants with neck pain displayed significantly improved standing
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balance and gait speed whereas healthy participants showed an impaired standing balance and gait speed, immediately after vibration. The importance of cervical proprioceptive information in controlling balance during standing and walking should be taken into account for rehabilitation in patients with neck pain.
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ACCEPTED MANUSCRIPT Fransson, P.A., Hjerpe, M., Johansson, R., 2007. Adaptation of multi-segmented body movements during vibratory proprioceptive and galvanic vestibular stimulation. J Vestib Res. 17, 47-62. Gomez, S., Patel, M., Magnusson, M., Johansson, L., Einarsson, E.J., Fransson, P., 2009.
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elaboration of body references. Prog Brain Res. 80, 113-23. Sjostrom, H., Allum, J.H., Carpenter, M.G., Adkin, A.L., Honegger, F., Ettlin, T., 2003. Trunk sway measures of postural stability during clinical balance tests in patients with
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ACCEPTED MANUSCRIPT Thakker, H., Elumalai, S., 2015. Static and dynamic postural stability in subjects with and without chronic low back pain. Int J Res Med Sci. 3, 2405-9. Treleaven, J., 2008. Sensorimotor disturbances in neck disorders affecting postural stability, head and eye movement control. Man Ther. 13, 2-11.
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Treleaven, J., Jull, G., Lowchoy, N., 2005. Standing balance in persistent whiplash: a comparison between subjects with and without dizziness. J Rehabil Med. 37, 224-9. Treleaven, J., Jull, G., Sterling, M., 2003. Dizziness and unsteadiness following whiplash
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Treleaven, J., LowChoy, N., Darnell, R., Panizza, B., Brown-Rothwell, D., Jull, G., 2008. Comparison of sensorimotor disturbance between subjects with persistent whiplashassociated disorder and subjects with vestibular pathology associated with acoustic neuroma. Arch Phys Med Rehabil. 89, 522-30.
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Uthaikhup, S., Paungmali, A., Pirunsan, U., 2011. Validation of Thai versions of the Neck Disability Index and Neck Pain and Disability Scale in patients with neck pain. Spine (Phila Pa 1976). 36, 1415-21.
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Uthaikhup, S., Sunkarat, S., Khamsaen, K., Meeyan, K., Treleaven, J., 2014. The effects of
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ACCEPTED MANUSCRIPT Figure legends Figure 1: Standing balance measure using a swaymeter.
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pain and control groups. (* p < 0.01, ** p < 0.001)
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Figure 2: Mean and standard error of total sway area before and after vibration for the neck
Figure 3: Mean and standard error of sway displacement (anterior-posterior) between the
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neck pain and controls groups at baseline and immediately after vibration. (** p < 0.001)
Figure 4: Mean and standard error of sway displacement (medial-lateral) the neck pain and
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controls groups at baseline and immediately after vibration. (** p < 0.001)
Figure 5: Mean and standard error of gait speed obtained from the neck pain and controls
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groups at baseline and immediately after vibration. (* p < 0.01, ** p < 0.001)
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ACCEPTED MANUSCRIPT Acknowledgement
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The study was supported by Faculty of Associated Medical Sciences, Chiang Mai University.
ACCEPTED MANUSCRIPT Table 1 Baseline characteristics of participants with neck pain and healthy controls. Controls (n = 30)
Age (years)
31.5 ± 10.5
29.5 ± 10.2
Gender (% female)
56.7
56.7
Weight (kg)
65.1 ± 15.6
Height (cm)
164.4 ± 10.0
Body mass index (kg/m2)
24.0 ± 5.0
Side of pain (% bilateral)
80.0
Neck pain intensity (0 – 10 VAS)
59.9 ± 11.9
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162.5 ± 10.0 22.7 ± 4.1
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22.3 ± 12.9
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5.1 ± 2.0
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29.6 ± 29.9
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Neck pain duration (months)
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Neck disability index (%)
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Neck pain (n = 30)
3.5 ± 2.2
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Pain on the testing day (%)
86.7
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26.7
0
Dizziness (%)
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Neck pain frequency (days per week)
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Data are presented as mean ± sd unless otherwise indicated. NDI = Neck Disability Index, VAS = Visual Analogue Scale.
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Highlights Cervical proprioception is important for controlling balance and gait
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Greater AP postural sway and slower gait speed occurs with neck pain
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Vibration effects balance and gait positively in neck pain and negatively in controls
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Neck muscle vibration has potential for rehabilitation of neck pain
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