THE EFFECT OF CERVICAL SPINE MANIPULATION ON POSTURAL SWAY IN PATIENTS WITH NONSPECIFIC NECK PAIN Alison R. Fisher, MOst, a Catherine J. Bacon, MSc, PhD, b c and Jamie V.H. Mannion, PGDipSci, MSc d
ABSTRACT Objective: This crossover study aimed to determine whether a single high-velocity, low-amplitude manipulation of the cervical spine would affect postural sway in adults with nonspecific neck pain. Methods: Ten participants received, in random order, 7 days apart, a high-velocity, low-amplitude manipulation applied to a dysfunctional spinal segment and a passive head-movement control. Four parameters of postural sway were measured before, immediately after, and at 5 and 10 minutes after each procedure. Results: Results showed no differences between interventions in change in any of the parameters. When changes before and immediately after each procedure were analyzed separately, only the control showed a significant change in the length of center of pressure path (an increase from median, 118 mm; interquartlie range, 93-137 mm to an increase to 132 mm; 112-147; P = .02). Conclusion: This study failed to show evidence that single manipulation of the cervical spine influenced postural sway. Given the ability of the postural control system to reweight the hierarchy of sensory information to compensate for inadequacies in any 1 component, it is possible that any improvements in the mechanisms controlling postural sway elicited by the manipulative intervention may have been concealed. (J Manipulative Physiol Ther 2015;38:65-73) Key Indexing Terms: Neck Pain; Central Nervous System; Cervical Manipulation; Neuronal Plasticity; Posture
ysfunction within components of the postural control system has been associated with an increase in postural sway and in energy expenditure required to maintain upright stance. 1,2 Therefore, it is a basic assumption of many measurements of postural equilibrium that the magnitude of postural sway is a reflection of the integrity of the postural control system. 3,4 Several studies have noted that individuals with both experimental 5
D
a Osteopath, Department of Osteopathy, Unitec Institute of Technology, Auckland, New Zealand. b Research Supervisor, Department of Osteopathy, Unitec Institute of Technology, Auckland, New Zealand. c Postdoctoral Research Fellow, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand. d Lecturer, Department of Osteopathy, Unitec Institute of Technology, Auckland, New Zealand. Submit requests for reprints to: Catherine J. Bacon, BSc, BPhed (Hons), MSc, PhD, Faculty of Medical and Health Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand. (e-mail: [email protected]). Paper submitted December 13, 2013; in revised form August 25, 2014; accepted September 1, 2014. 0161-4754 Copyright © 2015 by National University of Health Sciences. http://dx.doi.org/10.1016/j.jmpt.2014.10.014
and clinical 3,6,7 neck pain exhibit 130% to 170% greater postural sway, during normal stance with eyes open, when compared with asymptomatic controls. Neck pain is also associated with impairment in other measures of balance, and these have been recently reviewed. 8 The cervical region plays an important role in supplying proprioceptive information to the postural control system. This is reflected by the dense concentration of proprioceptive organs within cervical musculature and the extensive network of connections that cervical afferents form with numerous components of the postural control system. 9 The importance of cervical afferents to postural control has been eloquently demonstrated by experimental studies, which found that vibration of neck musculature in healthy individuals resulted in disrupted gait 10 and increased postural sway. 11 Somatic pain is associated with extensive neuroplastic changes in regions responsible for sensory processing and interpretation, motor planning, and emotional and behavioral responses. 12 It is thought that these changes may be responsible for the development and maintenance of functional impairments seen in neck pain sufferers. 13,14 Examples include altered processing of sensory information, 15 reduced kinesthetic sensibility of the cervical spine, 16 delayed feedforward activation of postural musculature, 17 reduced
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neuromuscular efficiency, 18 altered motor patterning, and increased fatigability of cervical musculature. 19 Such pain-induced disturbances to important components of the postural control system, in conjunction with altered cervical proprioceptive input, are thought to be significant contributing factors to the increased postural sway observed in individuals with neck pain. 3,20,21 High-velocity, low-amplitude (HVLA) spinal manipulation has long been used by manual therapists in the treatment of musculoskeletal complaints. 22,23 Cervical spine manipulation to individuals with neck pain has been shown to reduce pain levels locally and in peripheral sites, 24,25 increase force production by improving recruitment of inhibited musculature, 26-28 and improve kinesthetic performance. 29,30 Despite the evidence of promising therapeutic and sensorimotor effects of HVLA manipulation of patients with painful neck disorders, the mechanisms underlying this technique are still unclear. A series of studies by Haavik and Murphy 31-33 has demonstrated acute alterations in cortical activity in regions related to sensory processing and sensorimotor integration changes up to 30 minutes after cervical spine manipulation to dysfunctional segments in patients with neck pain. From these data, it has been proposed that improvements in neuromuscular performance after manipulation in patients with neck pain may result directly from the normalization of aberrant proprioceptive input associated with neck pain 21 or indirectly from the analgesic effects of the technique itself. 34 Thus, because postural sway responds immediately to disturbance of cervical afferents 11 and because neck manipulation has been shown to result in acute improvements in sensorimotor integration, 21 recent studies have hypothesized an effect of a single HVLA cervical spine manipulation on the postural sway of asymptomatic individuals. Two of these studies demonstrated significant reductions in postural sway after cervical spine manipulation with eyes open 35 and eyes closed. 36 By contrast, a study by Palmgren et al 29 reported no significant change in postural sway in measurements with both occluded vision and full vision. Although Haavik and Murphy have demonstrated relevant immediate changes in cortical function after manipulation in patients with neck pain, to date, no studies explore the potential for HVLA spinal manipulation to acutely influence postural sway in individuals with neck pain. In this study, we therefore investigate 1 mechanism for the observed effects of cervical spine manipulation on neck pain by examining the effect of a single HVLA manipulation to the cervical spine of individuals with neck pain on postural sway in the eyes open condition.
METHODS Participants Adults between the ages of 18 and 55 years with neck pain for at least the previous 4-week neck pain were invited to
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participate in this study in posters placed in a training osteopathy clinic at Unitec, Auckland, New Zealand, and on the participant recruitment Web site ResearchStudies.co.nz. To be eligible, participants were also required to have a dysfunctional segment within the cervical spine, defined as the presence of restricted intersegmental range of motion and tenderness on palpation of the joint. 37 Assessments of range of motion and tenderness have been shown to have good to excellent interexaminer reliability for cervical range of motion, 38,39 in contrast to palpable paravertebral muscular tissue texture change. 37,40 Participants were ineligible for the study if, in a medical screening questionnaire, they reported possible contraindications to cervical spine manipulation, 41 subjective symptoms of vertebrobasilar insufficiency, 42 or if, under examination, they exhibited signs or symptoms suggestive of the presence of vertebrobasilar insufficiency using a provocation test in accordance with Australian Physiotherapy Association clinical guidelines. 42,43 After expressing interest in the study, the aims and procedures involved in the study were explained verbally to prospective participants; and they were sent a formal information sheet and consent form. Written, informed consent was obtained from each participant. This study was approved by Unitec Research Ethics Committee (UREC 2011-1188) and registered with the Australian New Zealand Clinical Trials Registry (ACTRN12613001254785).
Experimental Protocol A randomized controlled trial design with crossover was used. Each participant attended 2 sessions, 1 week apart, in which they received either the cervical spine manipulation or a passive head movement control. The passive head movement was designed as a physiologic control for any possible changes occurring due to the vestibular or mechanical input from passively preparing the participants' heads for the cervical spine manipulation intervention. The order of treatments was determined via random generation of an odd or even number, using Web-based software (www.random.org), after enrolment at the time participants arrived for their first treatment session, so foreknowledge of upcoming allocation was prevented.
Procedures The procedures were performed by a registered osteopath, who had also conducted the screening examinations. The cervical spine manipulation intervention consisted of a single HVLA thrust to the identified dysfunctional segment. The passive head movement control involved the participant's head being gently and passively side bent and rotated into the position that the practitioner would normally manipulate. The participants' head was then returned to a neutral position.
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The participants were told that the study aimed to investigate the effects of 2 different techniques on postural sway. As a result, the participants were unaware that the cervical spine manipulation intervention was the technique of interest and that the passive head movement was designed as a control.
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sway variables at each of the 3 postprocedure time points were assessed for violation of assumptions of normality to evaluate the appropriateness of parametric statistics. 48 Analysis of variance (ANOVA) models and nonparametric equivalents were used to evaluate differences between procedures (manipulation intervention vs passive control) across the measurement time points. For all analyses, statistical significance was set to P b .05.
Measurements of Postural Sway and Pain Both baseline and postprocedure postural sway were measured using the Medicapteurs S-Plate platform (Balma, France) and associated S-Plate software, version 1.36. Center of pressure (COP) deviations derived from a force platform have been shown to be a reliable measure of postural sway. 44 Four variables of COP were measured: the length of COP path, the area covered by the COP path, and the average speed in both medial/lateral and anterior/ posterior directions. These measures have been previously shown to have the greatest reliability on this force platform (intraclass correlation coefficients on the first session ranging from 0.75 to 0.87). 45 Participants were asked to stand, without footwear, on the force plate as naturally as possible with their eyes open, on a template that aligned their feet to a position with their heels 10 cm apart and at an angle of 30° as measured along the medial border of the foot and looking at a marked point on the wall 90 cm in front of them. The investigator (a different person to the practitioner) was stationed behind them, out of sight to reduce possible body language transmission of expectation related to the outcome. The total duration of each measurement period was 75 seconds. This included 10 seconds before initiation of recording to allow the participant to settle into a standing posture, 60 seconds of data collection, and 5 seconds after the completion of the recording to allow for any anticipatory movement near the completion of data capture. To further reduce variability that might arise from trial-totrial fluctuation of performance, 2 baseline measures of postural sway were recorded. After this, the participant received their allocated procedure. The first postprocedure measurement of postural sway was taken immediately after administration of the procedure. Two subsequent measurements at 5 and 15 minutes postprocedure were made with the participant sitting quietly between measures. Participants rated their neck pain using an 11-point Numerical Rating Scale (NRS) before the baseline sway measurements were recorded and again after the first postprocedure measurement of sway. The NRS has been found to be valid, reliable, and appropriate for measuring pain intensity in clinical and research settings. 46,47
Statistical Analysis Data were analyzed using SPSS version 19 (SPSS and IBM company, Chicago IL). Changes from baseline for all
RESULTS Ten adults (7 men and 3 women) with a mean age of 37.2 years, ranging from 27 to 46 years, participated in this study. The sample size was calculated using G*Power3 49 based on a statistical power of 0.8 to detect a change in sway measures of 20 mm (effect size, 1.0) using reliability data from a previous study. 45 Analysis for any systematic change in the magnitude of sway measures between the first and second baseline measures was conducted to establish whether reporting an average of these 2 measures was justified. Paired t tests showed reductions in sway between the first and second measurements (P range from .003 to .1). To adjust for this systematic change but maintain the greater consistency afforded by duplicate baseline measures, the mean difference between the 2 measurements was subtracted from the first baseline measurement to adjust the first baseline measurement. An average of second baseline and this adjusted first baseline measurement was used for analysis. Change from baseline for all of the sway variables showed at least at 1 postprocedure time point that displayed skewness or kurtosis, which fell outside the 95% confidence interval for a normal distribution. Similarly, each change variable showed a significant Shapiro-Wilk statistic, which indicated a violation of normality, 48 for at least 1 postprocedure time point. To establish whether there were differences between the manipulation intervention and passive head movement control procedures in the pattern of change in sway variables over the 4 measurement points, 2-way (time point × procedure) ANOVAs were run for each sway variable (length of path, area of path, speed in anterior-posterior direction, and speed in medial-lateral direction). Parametric statistics were applied here because ANOVA is thought to be robust to moderate violations of normality with sample sizes between 10 and 20. 50 No significant interactions for any of the 4 ANOVAs were shown (Table 1), indicating a lack of difference in change between the manipulation intervention and passive head movement control condition (F[3,27], when sphericity assumption upheld, ranged from .4 to 1.0; P values from .4 to .6) (Fig 1). The findings did not change when a nonparametric equivalent was performed. For this, differences between conditions for each time point were calculated for each sway variable and analyzed as 4 single-factorial nonparametric Friedman ANOVAs. Again, no statistically
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Table 1. Effect Sizes of Changes in Sway Parameters From Before to Immediately After Cervical Spine Manipulation or Passive Head Movement and Their Correlations With Initial Levels and Changes in NRS Neck Pain Scores Cervical Manipulation ES
Initial NRS Sway Parameter Area of COP path (square millimeters) Length of path (millimeters) Average speed x-axis (millimeter per second) Average speed y-axis (millimeter per second)
0.28 0.05 0.30 0.38
Passive Head Movement Control
Correlations
ES Change in NRS
ρ
P
ρ
P
0.21 0.37 0.11 0.01
.6 .3 .8 1.0
− 0.10 − 0.24 − 0.03 − 0.01
.6 .3 .8 1.0
Correlations Initial NRS
0.80 0.12 0.66 0.55
Change in NRS
ρ
P
ρ
P
− 0.17 0.39 − 0.06 − 0.30
.6 .3 .9 .4
− 0.10 − 0.32 − 0.15 0.17
.8 .4 .7 .6
COP, center of pressure; ES, effect size: posttreatment measurement − pretreatment measurement/SD of difference; NRS, numerical rating scale. For average speed, x-axis is medial/lateral direction and y-axis is anterior/posterior direction. Corrrelation coefficients are Spearman ρ.
significant effects that would suggest an interaction between conditions and changes over time were found (χ 2[3] range from 1.4 to 2.3; P values from .5 to .7). Because an unexpected trend for an increase in sway after the passive head movement (control) condition was observed, an additional analysis was undertaken to determine whether there were changes in sway variables across measurements for the manipulation and passive movement procedures separately. Friedman ANOVAs showed no change over time shown for any of the sway variables for the manipulation intervention (χ 2[3] range from 2.8 to 3.5; P values from .3 to .5). For the passive control, these analyses showed changes over time for length of path in the passive condition (χ 2[3], 9.5; P = .02) and a trend toward this in the passive condition for area (χ 2[3], 7.4; P = .06) but no changes for the other 2 sway variables (χ 2[3] range from 2.5 to 4.9; P values from .2 to .5). Visual inspection of the figures for length of path and speed sway variables show that the largest change over time occurred from baseline to immediately after the intervention(Fig 1 B-D). Despite statistical significance of the main effect for length, the pairwise change did not attain statistical significance (P = .02) when Bonferroni correction was applied (P b .0083 for significance). Numeric pain scores decreased from precondition to postcondition for both the manipulative (3.5 ± 1.4-2.3 ± 1.3 points; mean ± SD) and passive (4.1 ± 1.9-3.6 ± 1.8 points) conditions (F[1,9], 11.8; P = .008 for effect of time), but the change did not attain 2.5, the threshold for numeric pain score estimated to be clinically important 51 and did not differ between conditions (F[1,9], 3.1; P = .1 for interaction of time and condition).
DISCUSSION The aim of the present study was to determine whether a single HVLA manipulation of dysfunctional cervical segments in participants with neck pain would influence
postural sway. No difference was shown between changes in sway for the manipulation compared with the passive control condition. These findings are in contrast to results from the few studies that have explored the effect of spinal manipulation on postural control. Although no studies have been identified that have investigated the effect of cervical spine manipulation on the postural sway of individuals with neck pain, 3 studies have been conducted on asymptomatic individuals. Two randomized controlled trials, Nolan 35 (n = 45) and Smith and Mehta 36 (n = 11, intervention + 10 control) reported improvements in postural sway measurements after a single HVLA cervical spine manipulation compared with a sham treatment using a detuned ultrasound 35 or lying supine. 36 By contrast, a crossover study of 6 asymptomatic participants, which compared the effects of bilateral manipulation and cervical facet joint blockade to C5/6, noted no significant changes in either intervention. 29 A possible explanation for the failure of the current study to show any changes in postural sway, after manipulation compared with passive control, is that neck pain may be associated with an adaptive reweighting of sensory information away from the cervical spine. Sensory reweighting has been shown to occur in situations, where information from various sensory modalities becomes unavailable (eyes closed) or inaccurate (compliant support surface). In these scenarios, the postural control system reorganizes the hierarchy of sensory information to maintain balance in a variety of environmental conditions. 52,53 In the present study of symptomatic participants, a similar reweighting of sensory information away from the cervical proprioceptive elements may have occurred, a phenomenon that was unlikely to occur in previous studies that recruited asymptomatic individuals. 35,36 As a result, cervical spinal manipulation may have had less effect on sway than seen in previous studies. Evidence of sensory reweighting in the postural control system has been observed in the elderly, 54,55 patients with lower back pain, 56,57 and in healthy individuals after alteration of proprioceptive sensory information. 53,58 If sensory reweighting had occurred in the participants in the present study, postural sway before the intervention would
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Fig 1. Change of the 4 COP parameters over time.Darker boxes (left in each pair) show the manipulation intervention, and lighter boxes (right in each pair) show the passive head movement control. Graphs as follows: area of COP path (A), length of COP path (B), average speed of COP path in medial/lateral direction (C), and average speed of COP path in anterior/posterior direction (D). Boxes show interquartile range with bars extending to 10th and 90th percentiles and outliers as dots.⁎Statistically significant overall Friedman ANOVA (χ 2[3], 9.5; P = .02) for differences between measures for the passive head movement procedure only for length of path measure (B). No differences between procedures or interaction between procedures and changes over time were shown.
not be expected to be different from that of asymptomatic adults of a similar age; and cervical spinal manipulation may have had less effect on sway than seen in previous studies. It is difficult to determine whether initial sway measurements were comparable with previously reported measures in asymptomatic adults. This difficulty lies in the large degree of heterogeneity between studies in terms of testing position, manipulation of sensory conditions such as vision, and the frequency and duration of data collection. In the current study, we did not blindfold participants because others have shown that blindfolding participants may not be necessary for manipulation-induced changes in postural sway to be observed. 29,35 However, if sensory reweighting away from cervical proprioceptive input toward other sensory modalities was a factor in masking the effects of the intervention in the current study, then measures to occlude one of these systems, such as vision, may have amplified any change in cervical proprioceptive performance elicited by the manipulative intervention. In the past, several studies have demonstrated that individuals with neck pain, 59 lower back pain, 55 and diabetic peripheral neuropathy 60 exhibit greater postural sway than healthy controls after the limitation of sensory modalities such as lower limb proprioception and vision. Future studies might compare the effects of cervical spine manipulation on sway in both eyes open and eyes closed conditions.
An alternative explanation for the present study's failure to detect any difference in postural sway between the manipulative and passive head movement interventions may be that the central changes that have been reported after cervical spine manipulation 32,33,61-63 had not yet manifested as changes in functional motor output in the 15 minutes separating the intervention and the final measurement in the present study. To date, most studies have focused on responses of the sensory and motor cortices as discrete regions, and so it is not yet clear whether there is a direct link between the changes in excitability of the sensory cortex and the corticomotor output during pain. Recently, Schabrun et al 64 used somatosensoryevoked potentials and transcranial magnetic stimulation to monitor cortical responses to experimental muscle pain. Their results demonstrated changes in the somatosensory cortex both during and after pain, whereas changes in the motor cortex emerged only after the pain had resolved. Baseline pain levels were restored within 15 minutes in all patients. 64 Because the present study collected data only for a 15-minute period, it is possible that this measurement period was insufficient to detect a response from the motor system in the form of greater changes in postural sway. Final possibilities are that the passive head movement may not have been a sufficient control for the hypothesized effects, particularly any effect that might have occurred indirectly through small alterations in perceived pain or mobility, or that
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there may have been a 1-week carryover effect from the cervical spine manipulation procedure to the passive head movement condition for those randomized to receive the manipulation first, which blunted any overall effect that may have been present. The passive head movement was designed as a physiologic control for any changes elicited by the cutaneous, muscular, or vestibular input that would occur as a result of the preparation phase of cervical spine manipulation. The design of this control is supported by findings that both muscle spindles and Golgi tendon organs increase their discharge rate significantly more in response to the thrust phase of the spinal manipulation than the preload forces. 23 These authors note that spindles within paraspinal tissues increase their resting discharge by up to 200% in the thrust phase compared with only 29% in the preload phase. 23 Golgi tendon organs rarely responded to preload at all but also increased their discharge rate in the thrust phase. 23 The same control condition as the present study was used by the research group of Haavik and Murphy 32,33,62,63 in a series of studies. In each of these studies, significant cortical findings were recorded in the cervical spine manipulation intervention but not as a result of the use of this control technique. 32,33,62,65 Abnormal cortical processing of sensory information has been proposed to be a significant factor in the development and persistence of impaired functional performance in individuals with spinal-region pain. 15,66 Therefore, in the current study, it was deemed plausible that the improvements noted by Haavik and Murphy 21 might result in subsequent improvement in postural sway. Our study showed no evidence that a single cervical spine manipulation maneuver improved postural sway. This is in contrast to the findings from the body of research of Haavik and Murphy 21,31-33,61-63,65 that suggests cervical spine manipulation improves sensory processing and early sensorimotor integration. Furthermore, the findings of this study are contrary to the small group of studies that have demonstrated improvements in sway after lumbar manipulation of individuals with lower back pain 67 and cervical spine manipulation of asymptomatic individuals. 35,36 The observation that no such improvements were seen in this study may reflect an underlying reorganization of the postural control system as part of the complex neuromuscular response to neck pain. Pain-mediated neurologic influences on cortical processing of sensorimotor input may be of relevance to the treatment and rehabilitation process. Clinicians should keep in mind that, although manipulation may alleviate symptoms, the resulting effect on postural control may not match that observed for asymptomatic individuals.
LIMITATIONS A limitation of the present study is that it was performed with a small number of relatively heterogeneous participants over a relatively short time frame. These factors may have
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impaired the ability of the study to detect smaller changes that may have reached significance in a larger study. Despite this, an inspection of the mean change after manipulation intervention does not show a trend toward decreasing postural sway. Contrary to expectations, of the 4 sway variables, 3 appeared to increase immediately after the interventions, particularly after the passive condition. The secondary finding from the results of the nonparametric, Friedman ANOVA showing changes in 1 sway measure for the passive condition needs to be interpreted very cautiously due to the post hoc nature of the hypothesis, the number of statistical tests used, and because no overall statistical difference in conditions was shown for the 2-way ANOVA. Another possible limiting factor was the heterogeneous nature of the participant group, in terms of factors such as the etiology of their neck pain, their treatment history, and the duration of their symptoms, which may have reduced the ability to demonstrate a consistent effect of manipulation on sway. Future studies might investigate the type of manipulation or the effect of manipulation under a greater variety of conditions, for example, by manipulating surface or visual input and by comparing the effects of cervical spine manipulation in symptomatic and asymptomatic individuals.
CONCLUSION This study showed no evidence that a single cervical spine manipulation maneuver improved postural sway in this sample of individuals with nonspecific neck pain. Further investigation, with due consideration to the above factors, may be warranted to gain further insight into the complex process of neurophysiologic adaptation to neck pain and to develop more effective treatment and rehabilitation protocols with which to manage these patients in clinical practice.
FUNDING SOURCES AND POTENTIAL CONFLICTS OF INTEREST Equipment for this study was supplied by Unitec Institute of Technology, Auckland, New Zealand. No conflicts of interest were reported for this study.
CONTRIBUTORSHIP INFORMATION Concept development (provided idea for the research): A.F. Design (planned the methods to generate the results): A.F., C.B., J.M. Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): C.B., J.M. Data collection/processing (responsible for experiments, patient management, organization, or reporting data): A.F.
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Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the results): C.B., A.F. Literature search (performed the literature search): A.F. Writing (responsible for writing a substantive part of the manuscript): A.F., C.B. Critical review (revised manuscript for intellectual content, this does not relate to spelling and grammar checking): C.B., J.M.
Practical Applications • The current study failed to detect any change in postural sway after a manipulative procedure when compared with a passive movement control procedure in participants with chronic nonspecific neck pain. • This might mean that the previously observed ability of manipulation procedures to alter postural sway may not apply in situations of nonspecific chronic pain. • Based upon the findings of our study, cervical spine manipulation as a treatment to improve postural sway does not appear justified.
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26. Suter E, McMorland G. Decrease in elbow flexor inhibition after cervical spine manipulation in patients with chronic neck pain. Clin Biomech (Bristol, Avon) 2002;17:541-4, http://dx.doi.org/ 10.1016/S0268-0033(02)00025-6. 27. Dunning J, Rushton A. The effects of cervical high-velocity low-amplitude thrust manipulation on resting electromyographic activity of the biceps brachii muscle. Man Ther 2009; 14:508-13, http://dx.doi.org/10.1016/j.math.2008.09.003. 28. Fernández-Carnero J, Fernández-de-las-Peñas C, Cleland JA. Immediate hypoalgesic and motor effects after a single cervical spine manipulation in subjects with lateral epicondylalgia. J Manipulative Physiol Ther 2008;31:675-81, http://dx.doi.org/ 10.1016/j.jmpt.2008.10.005. 29. Palmgren P, Lindeberg A, Nath S, Heikkilä H. Head repositioning accuracy and posturography related to cervical facet nerve blockade and spinal manipulative therapy in healthy volunteers: a time series study. J Manipulative Physiol Ther 2009;32:193-202, http://dx.doi.org/10.1016/j. jmpt.2009.02.003. 30. Palmgren P, Sandström P, Lundqvist F, Heikkilä H. Improvement after chiropractic care in cervicocephalic kinesthetic sensibility and subjective pain intensity in patients with nontraumatic chronic neck pain. J Manipulative Physiol Ther 2006;29:100-6, http://dx.doi.org/10.1016/ j.jmpt.2005.12.002. 31. Haavik H, Murphy B. Subclinical neck pain and the effects of cervical manipulation on elbow joint position sense. J Manipulative Physiol Ther 2011;34:88-97, http://dx.doi.org/ 10.1016/j.jmpt.2010.12.009. 32. Haavik-Taylor H, Murphy B. Cervical spine manipulation alters sensorimotor integration: a somatosensory evoked potential study. Clin Neurophysiol 2007;118:391-402, http:// dx.doi.org/10.1016/j.clinph.2006.09.014. 33. Haavik-Taylor H, Murphy B. Altered central integration of dual somatosensory input after cervical spine manipulation. J Manipulative Physiol Ther 2010;33:178-88, http://dx.doi.org/ 10.1016/j.jmpt.2010.01.005. 34. Ruhe A, Fejer R, Walker B. Does postural sway change in association with manual therapeutic interventions? A review of the literature. Chiropr Man Ther 2013;21:9, http://dx.doi. org/10.1186/2045-709X-21-9. 35. Nolan JH. The effect of cervical spine chiropractic manipulation on balance [Dissertation]. Johannesburg, South Africa: University of Johannesburg; 2009. 36. Smith L, Mehta M. The effects of upper cervical complex high velocity low amplitude thrust technique and sub-occipital muscle group inhibition techniques on standing balance. Int J Osteopath Med 2008;11:162, http://dx.doi.org/10.1016/j. ijosm.2008.08.020. 37. Fryer G, Morris T, Gibbons P. Paraspinal muscles and intervertebral dysfunction: part one. J Manipulative Physiol Ther 2004;27:267-74, http://dx.doi.org/10.1016/j.jmpt. 2004.02.006. 38. Boline PD, Haas M, Meyer JJ, Kassak K, Nelson C, Keating JC. Interexaminer reliability of eight evaluative dimensions of lumbar segmental abnormality: part II. J Manipulative Physiol Ther 1993;16:363-74. 39. Rheault W, Albright B, Beyers C, et al. Intertester reliability of the cervical range of motion device. J Orthop Sports Phys Ther 1992;15:147-50. 40. Gibbons P, Tehan P. Manipulation of the spine. Thorax and pelvis. 3rd ed. Elsevier Limited; 2010. 41. Arnold C, Bourassa R, Langer T, Stoneham G. Doppler studies evaluating the effect of a physical therapy screening protocol on vertebral artery blood flow. Man Ther 2004;9: 13-21, http://dx.doi.org/10.1016/S1356-689X(03)00087-0.
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42. Rivett D, Shirley D, Magarey M, Refshauge K. Clinical guidelines for assessing vertebrobasilar insufficiency in the management of cervical spine disorders. Australian Physiotherapy Association; 2006, [http://www.whitmorephysiotherapy. com/downloads/Level_3_Upper/APA_VBI_Guidelines.pdf]. 43. Field S, Treleaven J, Jull G. Standing balance: a comparison between idiopathic and whiplash-induced neck pain. Man Ther 2008;13:183-91, http://dx.doi.org/10.1016/j.math.2006.12.005. 44. Fryer G, Morris T, Gibbons P. Paraspinal muscles and intervertebral dysfunction: part two. J Manipulative Physiol Ther 2004;27:348-57, http://dx.doi.org/10.1016/j.jmpt. 2004.04.008. 45. Fisher ST. Intra- session and inter-session reliability of center-of-pressure based measures of postural sway within a normal population. [Thesis]. Auckland: Unitec Institute of Technology; 2010. 46. Ferreira-Valente MA, Pais-Ribeiro JL, Jensen MP. Validity of four pain intensity rating scales. Pain 2011;152:2399-404, http://dx.doi.org/10.1016/j.pain.2011.07.005. 47. Hjermstad MJ, Fayers PM, Haugen DF, et al. Studies comparing Numerical Rating Scales, Verbal Rating Scales, and Visual Analogue Scales for assessment of pain intensity in adults: a systematic literature review. J Pain Symptom Manage 2011;41: 1073-93, http://dx.doi.org/10.1016/j.jpainsymman.2010.08.016. 48. Field A. Discovering statistics using SPSS. . 3rd Ed. London: Sage Publications; 2009. 49. Erdfelder E, Faul F, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 2007;39: 175-91. 50. Stevens JP. Applied mulitivariate statistics for the social sciences, 4th Ed. Mahwah, NJ. London: Lawrence Erlbaum Associates; 2002. 51. Pool J, Ostelo R, Hoving J, Bouter L, De Vet H. Minimal clinically important change of the Neck Disability Index and the Numerical Rating Scale for patients with neck pain. Spine 2007;32:3047-51. 52. Peterka RJ. Sensorimotor integration in human postural control. J Neurophysiol 2002;88:1097-118, http://dx.doi.org/10.1152/ jn.00605.2001 [PubMed Central PMCID: PMC 12205132]. 53. Vuillerme N, Pinsault N, Vaillant J. Postural control during quiet standing following cervical muscular fatigue: effects of changes in sensory inputs. Neurosci Lett 2005;378:135-9, http://dx.doi.org/10.1016/j.neulet.2004.12.024. 54. Woollacott M, Shumway-Cook A, Nashner L. Aging and posture control: changes in sensory organization and muscular coordination. Int J Aging Hum Dev 1986;23:97-114, http:// dx.doi.org/10.2190/VXN3-N3RT-54JB-X16X. 55. Brumagne S, Cordo P, Verschueren S. Proprioceptive weighting changes in persons with low back pain and elderly persons during upright standing. Neurosci Lett 2004;366: 63-6, http://dx.doi.org/10.1016/j.neulet.2004.05.013. 56. Popa T, Bonifazi M, Della Volpe R, Rossi A, Mazzocchio R. Adaptive changes in postural strategy selection in chronic low back pain. Exp Brain Res 2007;177:411-8, http://dx.doi.org/ 10.1007/s00221-006-0683-4. 57. Peterka RJ, Loughlin PJ. Dynamic regulation of sensorimotor integration in human postural control. J Neurophysiol 2004; 91:410-23, http://dx.doi.org/10.1152/jn.00516.2003. 58. Claeys K, Brumagne S, Dankaerts W, Kiers H, Janssens L. Decreased variability in postural control strategies in young people with non-specific low back pain is associated with altered proprioceptive reweighting. Eur J Appl Physiol 2011; 111:115-23, http://dx.doi.org/10.1007/s00421-010-1637-x. 59. Madeleine P, Nielsen M, Arendt-Nielsen L. Characterization of postural control deficit in whiplash patients by means of
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linear and nonlinear analyses—a pilot study. J Electromyogr Kinesiol 2011;21:291-7, http://dx.doi.org/10.1016/j.jelekin. 2010.05.006. Simoneau G, Ulbrecht J, Derr J, Cavanagh P. Role of somatosensory input in the control of human posture. Gait Posture 1995;3:115-22, http://dx.doi.org/10.1016/0966-6362 (95)99061-O. Haavik-Taylor H, Murphy B. The effects of spinal manipulation on central integration of dual somatosensory input observed after motor training: a crossover study. J Manipulative Physiol Ther 2010;33:261-72, http://dx.doi.org/10. 1016/j.jmpt.2010.03.004. Haavik-Taylor H, Murphy B. Altered sensorimotor integration with cervical spine manipulation. J Manipulative Physiol Ther 2008;31:115-26, http://dx.doi.org/10.1016/j.jmpt.2007.12.011. Haavik-Taylor H, Murphy B. Transient modulation of intracortical inhibition following spinal manipulation. Chiropr J Aust 2007;37:106-16.
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64. Schabrun S, Jones E, Kloster J, Hodges P. Temporal association between changes in primary sensory cortex and corticomotor output during muscle pain. Neuroscience 2013;235:159-64, http://dx.doi.org/10.1016/j.neuroscience. 2012.12.072. 65. Haavik-Taylor H, Murphy B. Altered cortical integration of dual somatosensory input following the cessation of a 20 min period of repetitive muscle activity. Exp Brain Res 2007;178: 488-98, http://dx.doi.org/10.1007/s00221-006-0755-5. 66. Brumagne S, Janssens L, Janssens E, Goddyn L. Altered postural control in anticipation of postural instability in persons with recurrent low back pain. Gait Posture 2008;28: 657-62, http://dx.doi.org/10.1016/j.gaitpost.2008.04.015. 67. Childs JD, Piva SR, Erhard RE. Immediate improvements in side-to-side weight bearing and iliac crest symmetry after manipulation in patients with low back pain. J Manipulative Physiol Ther 2004;27:306-13, http://dx.doi.org/10.1016/j. jmpt.2004.04.004.
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ABSTRACT Objective: This crossover study aimed to determine whether a single high-velocity, low-amplitude manipulation of the cervical spine would affect postural sway in adults with nonspecific neck pain. Methods: Ten participants received, in random order, 7 days apart, a high-velocity, low-amplitude manipulation applied to a dysfunctional spinal segment and a passive head-movement control. Four parameters of postural sway were measured before, immediately after, and at 5 and 10 minutes after each procedure. Results: Results showed no differences between interventions in change in any of the parameters. When changes before and immediately after each procedure were analyzed separately, only the control showed a significant change in the length of center of pressure path (an increase from median, 118 mm; interquartlie range, 93-137 mm to an increase to 132 mm; 112-147; P = .02). Conclusion: This study failed to show evidence that single manipulation of the cervical spine influenced postural sway. Given the ability of the postural control system to reweight the hierarchy of sensory information to compensate for inadequacies in any 1 component, it is possible that any improvements in the mechanisms controlling postural sway elicited by the manipulative intervention may have been concealed. (J Manipulative Physiol Ther 2015;38:65-73) Key Indexing Terms: Neck Pain; Central Nervous System; Cervical Manipulation; Neuronal Plasticity; Posture
ysfunction within components of the postural control system has been associated with an increase in postural sway and in energy expenditure required to maintain upright stance. 1,2 Therefore, it is a basic assumption of many measurements of postural equilibrium that the magnitude of postural sway is a reflection of the integrity of the postural control system. 3,4 Several studies have noted that individuals with both experimental 5
D
a Osteopath, Department of Osteopathy, Unitec Institute of Technology, Auckland, New Zealand. b Research Supervisor, Department of Osteopathy, Unitec Institute of Technology, Auckland, New Zealand. c Postdoctoral Research Fellow, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand. d Lecturer, Department of Osteopathy, Unitec Institute of Technology, Auckland, New Zealand. Submit requests for reprints to: Catherine J. Bacon, BSc, BPhed (Hons), MSc, PhD, Faculty of Medical and Health Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand. (e-mail: [email protected]). Paper submitted December 13, 2013; in revised form August 25, 2014; accepted September 1, 2014. 0161-4754 Copyright © 2015 by National University of Health Sciences. http://dx.doi.org/10.1016/j.jmpt.2014.10.014
and clinical 3,6,7 neck pain exhibit 130% to 170% greater postural sway, during normal stance with eyes open, when compared with asymptomatic controls. Neck pain is also associated with impairment in other measures of balance, and these have been recently reviewed. 8 The cervical region plays an important role in supplying proprioceptive information to the postural control system. This is reflected by the dense concentration of proprioceptive organs within cervical musculature and the extensive network of connections that cervical afferents form with numerous components of the postural control system. 9 The importance of cervical afferents to postural control has been eloquently demonstrated by experimental studies, which found that vibration of neck musculature in healthy individuals resulted in disrupted gait 10 and increased postural sway. 11 Somatic pain is associated with extensive neuroplastic changes in regions responsible for sensory processing and interpretation, motor planning, and emotional and behavioral responses. 12 It is thought that these changes may be responsible for the development and maintenance of functional impairments seen in neck pain sufferers. 13,14 Examples include altered processing of sensory information, 15 reduced kinesthetic sensibility of the cervical spine, 16 delayed feedforward activation of postural musculature, 17 reduced
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neuromuscular efficiency, 18 altered motor patterning, and increased fatigability of cervical musculature. 19 Such pain-induced disturbances to important components of the postural control system, in conjunction with altered cervical proprioceptive input, are thought to be significant contributing factors to the increased postural sway observed in individuals with neck pain. 3,20,21 High-velocity, low-amplitude (HVLA) spinal manipulation has long been used by manual therapists in the treatment of musculoskeletal complaints. 22,23 Cervical spine manipulation to individuals with neck pain has been shown to reduce pain levels locally and in peripheral sites, 24,25 increase force production by improving recruitment of inhibited musculature, 26-28 and improve kinesthetic performance. 29,30 Despite the evidence of promising therapeutic and sensorimotor effects of HVLA manipulation of patients with painful neck disorders, the mechanisms underlying this technique are still unclear. A series of studies by Haavik and Murphy 31-33 has demonstrated acute alterations in cortical activity in regions related to sensory processing and sensorimotor integration changes up to 30 minutes after cervical spine manipulation to dysfunctional segments in patients with neck pain. From these data, it has been proposed that improvements in neuromuscular performance after manipulation in patients with neck pain may result directly from the normalization of aberrant proprioceptive input associated with neck pain 21 or indirectly from the analgesic effects of the technique itself. 34 Thus, because postural sway responds immediately to disturbance of cervical afferents 11 and because neck manipulation has been shown to result in acute improvements in sensorimotor integration, 21 recent studies have hypothesized an effect of a single HVLA cervical spine manipulation on the postural sway of asymptomatic individuals. Two of these studies demonstrated significant reductions in postural sway after cervical spine manipulation with eyes open 35 and eyes closed. 36 By contrast, a study by Palmgren et al 29 reported no significant change in postural sway in measurements with both occluded vision and full vision. Although Haavik and Murphy have demonstrated relevant immediate changes in cortical function after manipulation in patients with neck pain, to date, no studies explore the potential for HVLA spinal manipulation to acutely influence postural sway in individuals with neck pain. In this study, we therefore investigate 1 mechanism for the observed effects of cervical spine manipulation on neck pain by examining the effect of a single HVLA manipulation to the cervical spine of individuals with neck pain on postural sway in the eyes open condition.
METHODS Participants Adults between the ages of 18 and 55 years with neck pain for at least the previous 4-week neck pain were invited to
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participate in this study in posters placed in a training osteopathy clinic at Unitec, Auckland, New Zealand, and on the participant recruitment Web site ResearchStudies.co.nz. To be eligible, participants were also required to have a dysfunctional segment within the cervical spine, defined as the presence of restricted intersegmental range of motion and tenderness on palpation of the joint. 37 Assessments of range of motion and tenderness have been shown to have good to excellent interexaminer reliability for cervical range of motion, 38,39 in contrast to palpable paravertebral muscular tissue texture change. 37,40 Participants were ineligible for the study if, in a medical screening questionnaire, they reported possible contraindications to cervical spine manipulation, 41 subjective symptoms of vertebrobasilar insufficiency, 42 or if, under examination, they exhibited signs or symptoms suggestive of the presence of vertebrobasilar insufficiency using a provocation test in accordance with Australian Physiotherapy Association clinical guidelines. 42,43 After expressing interest in the study, the aims and procedures involved in the study were explained verbally to prospective participants; and they were sent a formal information sheet and consent form. Written, informed consent was obtained from each participant. This study was approved by Unitec Research Ethics Committee (UREC 2011-1188) and registered with the Australian New Zealand Clinical Trials Registry (ACTRN12613001254785).
Experimental Protocol A randomized controlled trial design with crossover was used. Each participant attended 2 sessions, 1 week apart, in which they received either the cervical spine manipulation or a passive head movement control. The passive head movement was designed as a physiologic control for any possible changes occurring due to the vestibular or mechanical input from passively preparing the participants' heads for the cervical spine manipulation intervention. The order of treatments was determined via random generation of an odd or even number, using Web-based software (www.random.org), after enrolment at the time participants arrived for their first treatment session, so foreknowledge of upcoming allocation was prevented.
Procedures The procedures were performed by a registered osteopath, who had also conducted the screening examinations. The cervical spine manipulation intervention consisted of a single HVLA thrust to the identified dysfunctional segment. The passive head movement control involved the participant's head being gently and passively side bent and rotated into the position that the practitioner would normally manipulate. The participants' head was then returned to a neutral position.
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The participants were told that the study aimed to investigate the effects of 2 different techniques on postural sway. As a result, the participants were unaware that the cervical spine manipulation intervention was the technique of interest and that the passive head movement was designed as a control.
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sway variables at each of the 3 postprocedure time points were assessed for violation of assumptions of normality to evaluate the appropriateness of parametric statistics. 48 Analysis of variance (ANOVA) models and nonparametric equivalents were used to evaluate differences between procedures (manipulation intervention vs passive control) across the measurement time points. For all analyses, statistical significance was set to P b .05.
Measurements of Postural Sway and Pain Both baseline and postprocedure postural sway were measured using the Medicapteurs S-Plate platform (Balma, France) and associated S-Plate software, version 1.36. Center of pressure (COP) deviations derived from a force platform have been shown to be a reliable measure of postural sway. 44 Four variables of COP were measured: the length of COP path, the area covered by the COP path, and the average speed in both medial/lateral and anterior/ posterior directions. These measures have been previously shown to have the greatest reliability on this force platform (intraclass correlation coefficients on the first session ranging from 0.75 to 0.87). 45 Participants were asked to stand, without footwear, on the force plate as naturally as possible with their eyes open, on a template that aligned their feet to a position with their heels 10 cm apart and at an angle of 30° as measured along the medial border of the foot and looking at a marked point on the wall 90 cm in front of them. The investigator (a different person to the practitioner) was stationed behind them, out of sight to reduce possible body language transmission of expectation related to the outcome. The total duration of each measurement period was 75 seconds. This included 10 seconds before initiation of recording to allow the participant to settle into a standing posture, 60 seconds of data collection, and 5 seconds after the completion of the recording to allow for any anticipatory movement near the completion of data capture. To further reduce variability that might arise from trial-totrial fluctuation of performance, 2 baseline measures of postural sway were recorded. After this, the participant received their allocated procedure. The first postprocedure measurement of postural sway was taken immediately after administration of the procedure. Two subsequent measurements at 5 and 15 minutes postprocedure were made with the participant sitting quietly between measures. Participants rated their neck pain using an 11-point Numerical Rating Scale (NRS) before the baseline sway measurements were recorded and again after the first postprocedure measurement of sway. The NRS has been found to be valid, reliable, and appropriate for measuring pain intensity in clinical and research settings. 46,47
Statistical Analysis Data were analyzed using SPSS version 19 (SPSS and IBM company, Chicago IL). Changes from baseline for all
RESULTS Ten adults (7 men and 3 women) with a mean age of 37.2 years, ranging from 27 to 46 years, participated in this study. The sample size was calculated using G*Power3 49 based on a statistical power of 0.8 to detect a change in sway measures of 20 mm (effect size, 1.0) using reliability data from a previous study. 45 Analysis for any systematic change in the magnitude of sway measures between the first and second baseline measures was conducted to establish whether reporting an average of these 2 measures was justified. Paired t tests showed reductions in sway between the first and second measurements (P range from .003 to .1). To adjust for this systematic change but maintain the greater consistency afforded by duplicate baseline measures, the mean difference between the 2 measurements was subtracted from the first baseline measurement to adjust the first baseline measurement. An average of second baseline and this adjusted first baseline measurement was used for analysis. Change from baseline for all of the sway variables showed at least at 1 postprocedure time point that displayed skewness or kurtosis, which fell outside the 95% confidence interval for a normal distribution. Similarly, each change variable showed a significant Shapiro-Wilk statistic, which indicated a violation of normality, 48 for at least 1 postprocedure time point. To establish whether there were differences between the manipulation intervention and passive head movement control procedures in the pattern of change in sway variables over the 4 measurement points, 2-way (time point × procedure) ANOVAs were run for each sway variable (length of path, area of path, speed in anterior-posterior direction, and speed in medial-lateral direction). Parametric statistics were applied here because ANOVA is thought to be robust to moderate violations of normality with sample sizes between 10 and 20. 50 No significant interactions for any of the 4 ANOVAs were shown (Table 1), indicating a lack of difference in change between the manipulation intervention and passive head movement control condition (F[3,27], when sphericity assumption upheld, ranged from .4 to 1.0; P values from .4 to .6) (Fig 1). The findings did not change when a nonparametric equivalent was performed. For this, differences between conditions for each time point were calculated for each sway variable and analyzed as 4 single-factorial nonparametric Friedman ANOVAs. Again, no statistically
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Table 1. Effect Sizes of Changes in Sway Parameters From Before to Immediately After Cervical Spine Manipulation or Passive Head Movement and Their Correlations With Initial Levels and Changes in NRS Neck Pain Scores Cervical Manipulation ES
Initial NRS Sway Parameter Area of COP path (square millimeters) Length of path (millimeters) Average speed x-axis (millimeter per second) Average speed y-axis (millimeter per second)
0.28 0.05 0.30 0.38
Passive Head Movement Control
Correlations
ES Change in NRS
ρ
P
ρ
P
0.21 0.37 0.11 0.01
.6 .3 .8 1.0
− 0.10 − 0.24 − 0.03 − 0.01
.6 .3 .8 1.0
Correlations Initial NRS
0.80 0.12 0.66 0.55
Change in NRS
ρ
P
ρ
P
− 0.17 0.39 − 0.06 − 0.30
.6 .3 .9 .4
− 0.10 − 0.32 − 0.15 0.17
.8 .4 .7 .6
COP, center of pressure; ES, effect size: posttreatment measurement − pretreatment measurement/SD of difference; NRS, numerical rating scale. For average speed, x-axis is medial/lateral direction and y-axis is anterior/posterior direction. Corrrelation coefficients are Spearman ρ.
significant effects that would suggest an interaction between conditions and changes over time were found (χ 2[3] range from 1.4 to 2.3; P values from .5 to .7). Because an unexpected trend for an increase in sway after the passive head movement (control) condition was observed, an additional analysis was undertaken to determine whether there were changes in sway variables across measurements for the manipulation and passive movement procedures separately. Friedman ANOVAs showed no change over time shown for any of the sway variables for the manipulation intervention (χ 2[3] range from 2.8 to 3.5; P values from .3 to .5). For the passive control, these analyses showed changes over time for length of path in the passive condition (χ 2[3], 9.5; P = .02) and a trend toward this in the passive condition for area (χ 2[3], 7.4; P = .06) but no changes for the other 2 sway variables (χ 2[3] range from 2.5 to 4.9; P values from .2 to .5). Visual inspection of the figures for length of path and speed sway variables show that the largest change over time occurred from baseline to immediately after the intervention(Fig 1 B-D). Despite statistical significance of the main effect for length, the pairwise change did not attain statistical significance (P = .02) when Bonferroni correction was applied (P b .0083 for significance). Numeric pain scores decreased from precondition to postcondition for both the manipulative (3.5 ± 1.4-2.3 ± 1.3 points; mean ± SD) and passive (4.1 ± 1.9-3.6 ± 1.8 points) conditions (F[1,9], 11.8; P = .008 for effect of time), but the change did not attain 2.5, the threshold for numeric pain score estimated to be clinically important 51 and did not differ between conditions (F[1,9], 3.1; P = .1 for interaction of time and condition).
DISCUSSION The aim of the present study was to determine whether a single HVLA manipulation of dysfunctional cervical segments in participants with neck pain would influence
postural sway. No difference was shown between changes in sway for the manipulation compared with the passive control condition. These findings are in contrast to results from the few studies that have explored the effect of spinal manipulation on postural control. Although no studies have been identified that have investigated the effect of cervical spine manipulation on the postural sway of individuals with neck pain, 3 studies have been conducted on asymptomatic individuals. Two randomized controlled trials, Nolan 35 (n = 45) and Smith and Mehta 36 (n = 11, intervention + 10 control) reported improvements in postural sway measurements after a single HVLA cervical spine manipulation compared with a sham treatment using a detuned ultrasound 35 or lying supine. 36 By contrast, a crossover study of 6 asymptomatic participants, which compared the effects of bilateral manipulation and cervical facet joint blockade to C5/6, noted no significant changes in either intervention. 29 A possible explanation for the failure of the current study to show any changes in postural sway, after manipulation compared with passive control, is that neck pain may be associated with an adaptive reweighting of sensory information away from the cervical spine. Sensory reweighting has been shown to occur in situations, where information from various sensory modalities becomes unavailable (eyes closed) or inaccurate (compliant support surface). In these scenarios, the postural control system reorganizes the hierarchy of sensory information to maintain balance in a variety of environmental conditions. 52,53 In the present study of symptomatic participants, a similar reweighting of sensory information away from the cervical proprioceptive elements may have occurred, a phenomenon that was unlikely to occur in previous studies that recruited asymptomatic individuals. 35,36 As a result, cervical spinal manipulation may have had less effect on sway than seen in previous studies. Evidence of sensory reweighting in the postural control system has been observed in the elderly, 54,55 patients with lower back pain, 56,57 and in healthy individuals after alteration of proprioceptive sensory information. 53,58 If sensory reweighting had occurred in the participants in the present study, postural sway before the intervention would
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Fig 1. Change of the 4 COP parameters over time.Darker boxes (left in each pair) show the manipulation intervention, and lighter boxes (right in each pair) show the passive head movement control. Graphs as follows: area of COP path (A), length of COP path (B), average speed of COP path in medial/lateral direction (C), and average speed of COP path in anterior/posterior direction (D). Boxes show interquartile range with bars extending to 10th and 90th percentiles and outliers as dots.⁎Statistically significant overall Friedman ANOVA (χ 2[3], 9.5; P = .02) for differences between measures for the passive head movement procedure only for length of path measure (B). No differences between procedures or interaction between procedures and changes over time were shown.
not be expected to be different from that of asymptomatic adults of a similar age; and cervical spinal manipulation may have had less effect on sway than seen in previous studies. It is difficult to determine whether initial sway measurements were comparable with previously reported measures in asymptomatic adults. This difficulty lies in the large degree of heterogeneity between studies in terms of testing position, manipulation of sensory conditions such as vision, and the frequency and duration of data collection. In the current study, we did not blindfold participants because others have shown that blindfolding participants may not be necessary for manipulation-induced changes in postural sway to be observed. 29,35 However, if sensory reweighting away from cervical proprioceptive input toward other sensory modalities was a factor in masking the effects of the intervention in the current study, then measures to occlude one of these systems, such as vision, may have amplified any change in cervical proprioceptive performance elicited by the manipulative intervention. In the past, several studies have demonstrated that individuals with neck pain, 59 lower back pain, 55 and diabetic peripheral neuropathy 60 exhibit greater postural sway than healthy controls after the limitation of sensory modalities such as lower limb proprioception and vision. Future studies might compare the effects of cervical spine manipulation on sway in both eyes open and eyes closed conditions.
An alternative explanation for the present study's failure to detect any difference in postural sway between the manipulative and passive head movement interventions may be that the central changes that have been reported after cervical spine manipulation 32,33,61-63 had not yet manifested as changes in functional motor output in the 15 minutes separating the intervention and the final measurement in the present study. To date, most studies have focused on responses of the sensory and motor cortices as discrete regions, and so it is not yet clear whether there is a direct link between the changes in excitability of the sensory cortex and the corticomotor output during pain. Recently, Schabrun et al 64 used somatosensoryevoked potentials and transcranial magnetic stimulation to monitor cortical responses to experimental muscle pain. Their results demonstrated changes in the somatosensory cortex both during and after pain, whereas changes in the motor cortex emerged only after the pain had resolved. Baseline pain levels were restored within 15 minutes in all patients. 64 Because the present study collected data only for a 15-minute period, it is possible that this measurement period was insufficient to detect a response from the motor system in the form of greater changes in postural sway. Final possibilities are that the passive head movement may not have been a sufficient control for the hypothesized effects, particularly any effect that might have occurred indirectly through small alterations in perceived pain or mobility, or that
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there may have been a 1-week carryover effect from the cervical spine manipulation procedure to the passive head movement condition for those randomized to receive the manipulation first, which blunted any overall effect that may have been present. The passive head movement was designed as a physiologic control for any changes elicited by the cutaneous, muscular, or vestibular input that would occur as a result of the preparation phase of cervical spine manipulation. The design of this control is supported by findings that both muscle spindles and Golgi tendon organs increase their discharge rate significantly more in response to the thrust phase of the spinal manipulation than the preload forces. 23 These authors note that spindles within paraspinal tissues increase their resting discharge by up to 200% in the thrust phase compared with only 29% in the preload phase. 23 Golgi tendon organs rarely responded to preload at all but also increased their discharge rate in the thrust phase. 23 The same control condition as the present study was used by the research group of Haavik and Murphy 32,33,62,63 in a series of studies. In each of these studies, significant cortical findings were recorded in the cervical spine manipulation intervention but not as a result of the use of this control technique. 32,33,62,65 Abnormal cortical processing of sensory information has been proposed to be a significant factor in the development and persistence of impaired functional performance in individuals with spinal-region pain. 15,66 Therefore, in the current study, it was deemed plausible that the improvements noted by Haavik and Murphy 21 might result in subsequent improvement in postural sway. Our study showed no evidence that a single cervical spine manipulation maneuver improved postural sway. This is in contrast to the findings from the body of research of Haavik and Murphy 21,31-33,61-63,65 that suggests cervical spine manipulation improves sensory processing and early sensorimotor integration. Furthermore, the findings of this study are contrary to the small group of studies that have demonstrated improvements in sway after lumbar manipulation of individuals with lower back pain 67 and cervical spine manipulation of asymptomatic individuals. 35,36 The observation that no such improvements were seen in this study may reflect an underlying reorganization of the postural control system as part of the complex neuromuscular response to neck pain. Pain-mediated neurologic influences on cortical processing of sensorimotor input may be of relevance to the treatment and rehabilitation process. Clinicians should keep in mind that, although manipulation may alleviate symptoms, the resulting effect on postural control may not match that observed for asymptomatic individuals.
LIMITATIONS A limitation of the present study is that it was performed with a small number of relatively heterogeneous participants over a relatively short time frame. These factors may have
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impaired the ability of the study to detect smaller changes that may have reached significance in a larger study. Despite this, an inspection of the mean change after manipulation intervention does not show a trend toward decreasing postural sway. Contrary to expectations, of the 4 sway variables, 3 appeared to increase immediately after the interventions, particularly after the passive condition. The secondary finding from the results of the nonparametric, Friedman ANOVA showing changes in 1 sway measure for the passive condition needs to be interpreted very cautiously due to the post hoc nature of the hypothesis, the number of statistical tests used, and because no overall statistical difference in conditions was shown for the 2-way ANOVA. Another possible limiting factor was the heterogeneous nature of the participant group, in terms of factors such as the etiology of their neck pain, their treatment history, and the duration of their symptoms, which may have reduced the ability to demonstrate a consistent effect of manipulation on sway. Future studies might investigate the type of manipulation or the effect of manipulation under a greater variety of conditions, for example, by manipulating surface or visual input and by comparing the effects of cervical spine manipulation in symptomatic and asymptomatic individuals.
CONCLUSION This study showed no evidence that a single cervical spine manipulation maneuver improved postural sway in this sample of individuals with nonspecific neck pain. Further investigation, with due consideration to the above factors, may be warranted to gain further insight into the complex process of neurophysiologic adaptation to neck pain and to develop more effective treatment and rehabilitation protocols with which to manage these patients in clinical practice.
FUNDING SOURCES AND POTENTIAL CONFLICTS OF INTEREST Equipment for this study was supplied by Unitec Institute of Technology, Auckland, New Zealand. No conflicts of interest were reported for this study.
CONTRIBUTORSHIP INFORMATION Concept development (provided idea for the research): A.F. Design (planned the methods to generate the results): A.F., C.B., J.M. Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): C.B., J.M. Data collection/processing (responsible for experiments, patient management, organization, or reporting data): A.F.
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Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the results): C.B., A.F. Literature search (performed the literature search): A.F. Writing (responsible for writing a substantive part of the manuscript): A.F., C.B. Critical review (revised manuscript for intellectual content, this does not relate to spelling and grammar checking): C.B., J.M.
Practical Applications • The current study failed to detect any change in postural sway after a manipulative procedure when compared with a passive movement control procedure in participants with chronic nonspecific neck pain. • This might mean that the previously observed ability of manipulation procedures to alter postural sway may not apply in situations of nonspecific chronic pain. • Based upon the findings of our study, cervical spine manipulation as a treatment to improve postural sway does not appear justified.
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