Gait & Posture 24 (2006) 349355 www.elsevier.

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Changes in coordination of postural control during dynamic stance in chronic low back pain patients
R. della Volpe a, T. Popa b, F. Ginanneschi b, R. Spidalieri b, R. Mazzocchio a,*, A. Rossi a
a

Sezione di Neurosiologia Clinica, Dipartimento di Scienze Neurologiche e del Comportamento, Universita di Siena, Policlinico Le Scotte, Viale Bracci, I-53100 Siena, Italy b Scuola di Dottorato in Scienze Neurologiche Applicate, Universita di Siena, Siena, Italy Received 20 August 2005; accepted 24 October 2005

Abstract The human postural system operates on the basis of integrated information from three independent sources: vestibular, visual and somatosensory. It is conceivable that a derangement of any of these systems will inuence the overall output of the postural system. The peripheral proprioceptive system or the central processing of proprioceptive information may be altered in chronic low back pain (CLBP). We therefore investigated whether patients with CLBP exhibited an altered postural control during quiet standing. Dynamic posturography was performed by 12 CLBP patients and 12 age-matched controls. Subjects task was to stand quietly on a computer-controlled movable platform under six sensory conditions that altered the available visual and proprioceptive information. While the control of balance was comparable between the two groups across stabilized support surface conditions (13), CLBP patients oscillated much more than controls in the anterior posterior (AP) direction in platform sway-referenced conditions (46). Control experiments ruled out that increased sway was due to pain interference. In CLBP patients, postural stability under challenging conditions is maintained by an increased sway in AP direction. This change in postural strategy may underlie a dysfunction of the peripheral proprioceptive system or the central integration of proprioceptive information. # 2005 Elsevier B.V. All rights reserved.
Keywords: Posturography; Balance; Back pain; Proprioception

1. Introduction The maintenance and control of balance, whether under static or dynamic conditions, is an essential requirement for physical and daily activities. In humans, the balancecontrolling system is believed to be phylogenetically old, and to operate relatively autonomously through the spinal and brainstem reex networks [1]. However, there is evidence that standing, rather than rely on mechano-reex mechanisms [2,3], may require activity of higher order structures [4,5]. Therefore, the control of erect posture may be more integrated into the movement control scheme than has been previously considered.

* Corresponding author. Tel.: +39 0577 233409; fax: +39 0577 40327. E-mail address: mazzocchio@unisi.it (R. Mazzocchio). 0966-6362/$ see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2005.10.009

The human postural system operates on the basis of the integrated information from three independent sensory sources: somatosensory, vestibular and visual inputs [6]. This information, which allows to assess the position and motion of the body in space, is constantly reweighted so as to generate the appropriate forces to control and maintain balance in a wide range of situations [6]. It is thus conceivable that a derangement to any of the three sensory systems will inuence the overall output of the postural system. The coordination of postural control may be affected in subjects with chronic low back pain (CLBP) [712]. The cause of this disturbance is not known. Specically, it is not clear whether changes in postural control are related to pain itself and to its stressful nature, so-called pain interference [9,10]. In humans, discharge from high-threshold nociceptive afferents interacts with spinal motor pathways [1315] as well as with primary somatosensory and motor

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cortex [16,17]. These complex actions are likely to contribute to adaptive changes in postural control [18,19]. In addition, proprioceptive impairment has been suspected as one of the possible causes for balance impairments in CLBP [2022]. The majority of studies have focused on the lumbar spine, while little attention has been paid to the possibility that a reduced proprioception from the lower limbs may contribute to an altered control of balance in CLBP patients. In normal adults, postural adjustments during quiet standing are generally achieved using an ankle strategy [23], in which the ankle torque maintains the center of force over the base of support. In this strategy, the muscles groups acting at the ankle joint are considered as the main musculature for the control of stability during quiet standing [24]. Patients with CLBP due to spondylolisthesis have been found to have abnormalities of the soleus H-reex [25,26] which depends on the activation of large-diameter mechano-receptive afferents (group Ia bres) in the muscle [27]. It is known that changes in Ia input may result in altered proprioception [28] and distortion of sensory maps [29]. In addition, altered processing of non-noxious afferent information from large-diameter afferent bres has been suspected to contribute to some aspects of pain [30,31]. The purpose of the present experiments was to investigate the possibility that patients with CLBP exhibited an altered postural control during quiet standing with respect to a control population, as assessed by dynamic posturography [32]. This method measures whole body performance during quiet standing and allows to differentiate the contribution of the vestibular, proprioceptive and visual system to balance control. The hypothesis was that changes in postural control associated with CLBP, rather than being caused by pain interference, probably reect an altered postural strategy
Table 1 Clinical and radiological ndings Patient no. 1 2 3 4 Age (years) 23 22 31 40 Sex m m m f Height (cm) 190 175 175 159 Back pain (years) 1 2 2 10 Leg pain No No No No Oswestry LBPDQ 1 (2%) 12 (24%) 5 (10%) 19 (38%)

underlying a dysfunction of the peripheral proprioceptive system or of the central processing of proprioceptive information.

2. Methods 2.1. Subjects Twelve CLBP patients participated in this study. Inclusion criteria were: (1) localized back pain, lasting more than 6 months and radiating no further than the buttock, (2) no previous history of sciatica or other radicular involvement and (3) normal neurological examination. Selfreported disability was assessed with the Oswestry Low Back Pain Disability Questionnaire [33]. None of the patients had any history of vestibular and neurological disease nor of hip/knee/ankle/foot problems. The patients underwent medical and neurological examinations. Clinical data were recorded according to standardized protocols. Special attention was given to symptoms and signs relevant to the dysfunction of the nerve roots (i.e., pain, changes in muscle strength, sensory changes and problems with bladder or bowel function). The duration of pain was registered. When possible, the patients were examined with plain radiographs, computed tomographic scans and magnetic resonance imaging of the lumbosacral spinal tract. The radiographs were read by experienced neuroradiologist who had no clinical information available. The clinical characteristics and radiological ndings are summarized in Table 1. Twelve age-matched controls participated in this study. Control subjects had not experienced any low back pain 6 months prior to testing and had no evidence of gait,

Sensory symptoms and signs No No No No

Motor symptoms and signs No No No No

X-rays n.p. n.p. n.p. deg L5S1

CT-scan MRI deg L4L5, deg L5S1 n.p. Normal deg L1L2, deg L4L5, deg L5S1 deg L4L5, deg L5S1 deg L2L3, deg L5S1 deg L5S1 Multiple disc protrusions deg L4L5, deg L5S1 n.p. n.p. n.p.

5 6 7 8 9 10 11 12

32 29 25 57 36 31 38 61

f m m m f f f m

167 184 188 178 165 170 172 176

5 8 9 10 5 1.5 5 4

No No No No No No No No

1 (2%) 2 (4%) 4 (8%) 6 (12%) 24 (48%) 7 (14%) 6 (12%) 7 (14%)

No No No No No No No No

No No No No No No No No

deg L5S1 n.p. Dorsal scoliosis listhesisL5 Spondylosis multiple deg n.p. n.p. n.p. deg L1L2

LBFDQ: Low Back Pain Disability Questionnaire; deg: degenerative; L: lumbar; S: sacral; n.p.: not performed.

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postural or musculo-skeletal abnormalities. Informed consent was obtained from each subject and the experimental procedure was approved by the local Ethics Commission. 2.2. Apparatus Postural stability was evaluated by an instrumented platform system (Equitest, Neurocom Int. Inc., Clackamas, OR, USA) which has been used in previous studies [32,34 36]. The system included a movable support surface (which rotated around an axis co-linear to the ankle joints) and a movable visual surround (a 1-m2 enclosure open at the back and bottom which rotated around an axis co-linear to the ankle joints). Strain gauges within the platform measured the tangential forces and the total vertical force exerted by the feet resting upon its surface (Fig. 1A). In this way, the center of pressure (COP) location, i.e., the point of application of the ground reaction force, was calculated. Forceplate movements are described in terms of X and Y. Movement forward and backward is measured along the Y-axis, and lateral movement is measured along the X-axis. The anteroposterior (AP) and mediolateral (ML) displacements (mm) of COP were stored for off-line analysis. 2.3. Platform test procedures Subjects stood barefoot with ankles directly above the X-axis of the force platform and feet equidistant from the Y-axis, their arms hanging loosely by their sides, facing the visual surround and maintaining optic xation straight ahead on a small cloud drawn at the center of the scenery. A safety harness was used to prevent falls. Subjects were asked to stand as still as possible for three trials of 20 s during six different test conditions (Fig. 1B). During the rst three test conditions, the platform support surface remained xed with respect to the Earth horizontal, but the visual surrounds were: (task 1) xed with respect to the Earth vertical, (task 2) the subjects eyes were closed and (task 3) in proportional to AP body sway (visual stabilization). During the three other conditions (tasks

46), the platform support surface rotated in proportional to AP body sway (support surface stabilization) and the rst three visual conditions were repeated. The gain of surface motion relative to that of the body sway was set to 1 (surface and body motion were in direct proportion). A trial was stopped by the operator when subjects exceeded their limits of stability and took a step, opened their eyes (if the condition required eyes closed) or touched the visual surround with their hands in order to maintain upright stance. 2.4. Dynamic posturography during experimental arm pain To study the impact of pain in general on postural performance, we elicited arm pain by intramuscular injection of levo-ascorbic acid (L-AS) deeply in the belly of the right biceps muscle in six healthy subjects (four males and two females from the healthy group) who served as their own control. The experimental procedure to activate nociceptive afferents has been described in detail in previous papers [1416,37] and is only briey described here. A 0.3-ml bolus (pH 6.3 at 24 8C) of L-AS was delivered via a 26 G needle over 5 s. To evaluate the effect of the injections, we asked the subjects to rate the pain sensation using an 11-point box scale: 0 = absence of pain, 10 = worst possible pain. Pain intensity was monitored at about 1-min intervals between each posturographic test condition. Posturographic testing was started 30 s after injection when pain level reached its peak (time 0 in Fig. 3). Three subjects were rst exposed to static (tasks 1 3) and then dynamic (tasks 46) conditions while in the remaining three the order was inverted. This ensured that the effects of pain equally inuenced the different conditions. 2.5. Data analyses The average COP velocity and the root mean square (RMS) of COP displacement in the AP and ML directions of

Fig. 1. Apparatus (A) and tasks (B) consisting of six different posturographic test conditions.

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the three trials performed in each of the six test conditions were calculated for each subject. 2.6. Statistical analysis Data were initially subjected to cluster analysis (distance measures: Euclidean; linkage method: centroid) and then tested for normal distribution (KolmogorovSmirnov) and homogeneity of variance (Levenes F). ANOVA with repeated measures on task (conditions 16) was performed to test for differences in average COP velocity and RMS of COP in AP and ML directions between healthy subjects and CLBP patients and between acute pain and no pain condition in healthy subjects. Post hoc analyses (Scheffe tests) were used when appropriate. The level of signicance was set at p < 0.05.

3. Results Duration of CLBP ranged from 1 year to 10 years (5.2 3.3 years). The level of discomfort and disability of

CLBP patients prior to the performance of the postural tests was on average low (see Table 1). Sensory and motor testing was normal. Radiological ndings mainly showed moderate degenerative changes of the lumbar discs with no sign of root compression. Fig. 2 compares the measures of sway in AP (A and B) and ML (C and D) directions between the healthy group and the CLBP group. Overall ANOVA showed a signicant increase in average COP velocity (Fig. 2A) and RMS of COP (Fig. 2B) in AP direction for the CLBP group (23.7 2.0 mm/s, F = 21.1, p < 0.0001, and 0.34 0.03 mm, F = 19.9, p < 0.0001, respectively) as compared to the healthy group (18.5 1.3 mm/s and 0.27 0.02 mm, respectively). There was a signicant interaction between both measures of sway and task, i.e., the different posturographic test conditions (F = 3.23, p = 0.01, and F = 3.35, p < 0.01). Post hoc testing revealed signicant differences for tasks 46 (see Table 2), corresponding to the dynamic stance conditions. On the other hand, there was no signicant increase in average COP velocity (Fig. 2C) and RMS of COP (Fig. 2D) in ML direction for the CLBP group as compared to the healthy group.

Fig. 2. Average COP velocity (A and C) and RMS of COP displacement (B and D) in anteriorposterior (AP) and mediallateral (ML) directions for the six different conditions between healthy controls and chronic low back pain (CLBP) patients. Note signicant increase in sway for the dynamic tasks (conditions 4 6) in AP direction for the CLBP group (*p < 0.05; see also Table 2). The small inset shows overall differences between the two groups for all the conditions (*p < 0.0001).

R. della Volpe et al. / Gait & Posture 24 (2006) 349355 Table 2 Anteriorposterior sway (mean 1S.E.) Task (test conditions) Average COP (velocity (mm/s) Control 1 2 3 4 5 6 8.89 0.37 10.32 0.57 10.83 0.92 16.12 0.81 35.56 2.12 29.45 2.30 CLBP 9.11 0.40 12.18 1.20 12.35 1.05 21.25 1.73* 47.84 4.98* 39.49 3.48* RMS of COP (mm) Control 0.15 0.00 0.16 0.01 0.17 0.01 0.24 0.01 0.50 0.03 0.41 0.03 CLBP

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0.15 0.01 0.19 0.01 0.19 0.01 0.31 0.03a 0.66 0.07* 0.55 0.05*

Mean measures of sway during the different posturographic conditions for both groups. a There was a tendency for an increased RMS of COP for task 4 ( p = 0.06). * p < 0.05.

Fig. 3A shows the time course of experimentally induced arm pain in six healthy subjects. As discussed in a previous paper [15], the nociceptive effect of L-AS is probably due to a drop in tissue pH [38]. Most subjects described pain at the injection site and extending along the muscle belly like a cramp. Pain level peaked by 30 s at about 5/10 on average and was down to 2/10 by the time the task was over. Fig. 3B compares average COP velocity (left) and RMS of COP (right) in AP (upper graphs) and ML (lower graphs) direction between pain and no-pain condition in the healthy subgroup. No signicant effect for either measure of sway was observed in both AP and ML directions.

4. Discussion The main result of the present study was that subjects with CLBP exhibited an increased sway in the AP direction during quiet standing, as assessed by dynamic posturography. This procedure, which has been extensively used in

clinical practice [39], evaluates utilization of visual, vestibular and proprioceptive sensors by manipulating the accuracy of visual and/or somatosensory inputs during quiet stance [36]. While the amount of sway was comparable between the CLBP group and the control group across static conditions (tasks 13, the absence or inaccuracy of visual references not interfering with maintenance of posture), performance under altered proprioceptive conditions, such as with support surface sway-referencing (task 4) and with absent or altered vision (tasks 5 and 6), produced the largest difference in the amount of sway between the CLBP and the control group. In other words, patients with CLBP oscillated much more than controls when proprioceptive input was altered and visual input was removed or inaccurate, suggesting greater dependence on visual input to control balance under challenging dynamic conditions. These ndings are in line with previous work showing the largest differences between CLBP patients and healthy subjects with tasks involving increased complexity in the absence of visual input [8,11,12]. However, we did not nd that absence

Fig. 3. (A) Time course of arm pain. The mean (continuous line) and standard deviation (dashed lines) of the intensity of pain elicited by intramuscular injection of levo-ascorbic acid into the right biceps muscle in six healthy subjects making part of the control group. Time 0 corresponds to the onset of posturographic assessment which started with static test conditions (tasks 13) for three subjects and with dynamic test conditions (tasks 46) for the remaining three. (B) Overall average COP velocity (left panel) and RMS of COP displacement (right panel) in anteriorposterior (AP) and mediallateral (ML) directions for all posturographic tasks between the pain condition and the no-pain condition (the same subjects served as their own control). No signicant difference in either measure of sway was found in AP and ML directions.

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of vision increased sway in AP direction under the Romberg condition (task 2) nor did we nd signicant differences in ML postural sway between the CLBP group and the control group. This discrepancy may be due to the lack of acute back pain prior to and during the performance of the test in our patients and to a lesser duration of CLBP in our population (5 years on average) as well as to different experimental testing conditions. Before concluding that body sway in AP direction is increased during quiet standing in CLBP patients, it is important to rule out that pain itself is not directly responsible for the observed modication of the control of balance. The absence of acute pain in our patients during testing conditions does not necessarily rule out the possibility of some activity arising from nociceptive afferents [40]. Muscle pain may cause marked reduction of position sense [16] possibly through increased presynaptic inhibition of muscle afferents at spinal level [14] and/ or by a down-regulation of cortical systems involved in proprioceptive processing [17,41]. The results from the experimental arm pain performed in a representative sample (50%) of the healthy subjects show that there was no direct inuence of pain on postural sway, as assessed by dynamic posturography. The time course and perceptual characteristics of acute arm pain elicited by injection of L-AS into the biceps muscle are consistent with a body of work using intramuscular injection at other anatomical sites [1317,37,42]. The protocol achieved moderate to marked pain of sufcient duration to perform all posturographic tasks. These ndings, therefore, make the possibility that nociception alone may produce an increase in body sway, as observed in the CLBP group, unlikely. We have demonstrated that in CLBP patients greater postural sway in AP direction becomes manifest during quiet standing as compared to healthy subjects, when challenging conditions are met. This nding may suggest a decreased ability to detect small motions of the platform during dynamic stance in CLPB patients. As a result, larger AP oscillations are generated to presumably remain within the range required for stability. The absence of increased sway under static stance conditions as well as during experimentally induced arm pain strongly reduces the possibility that sway changes are due to a general effect of pain [10]. We propose that these changes may be adaptive in nature, i.e., that they reect a change in postural control strategy, possibly due to a decreased sensitivity of the peripheral systems, as well as reduced exibility in central information processing [43]. It has been suggested that proprioceptive input is important for maintenance of balance [36,44] and that increased emphasis is placed upon vision for compensatory balance control under challenging conditions [8,11,12,36]. Indeed, our patients exhibited an increased sway in the response to platform sway-referencing (task 4), suggesting that visual information was increasingly relied upon. When an additional sensory conict was introduced, such as absent

or inaccurate vision (tasks 5 and 6), CLBP patients became more destabilized as compared with the healthy group. It has been argued that balance dysfunction in patients with CLBP may be due to altered proprioceptive feedback from the lumbar spine [8,20,21]. This suggestion has been made on the basis of trunk specic CLBP assessment rather than measures of whole body performance [11]. It is possible that a change in proprioceptive feedback from segments of the body other than the trunk may also inuence postural control in CLBP patients. Interestingly, an increased electrical threshold for activation of the largest sensory bres conveying proprioceptive information from the soleus muscle has been observed in a group of patients with CLBP due to spondylolisthesis [25,26]. Sensory dysfunction such as this may increase the threshold to movement detection at the level of the ankle joint. Ankle muscle input and, possibly, cutaneous input from the foot sole contribute to the control of human erect posture [45]. A loss of somatosensory information from the lower limbs, resulting from a disease or an experimental manipulation, has been shown to induce postural control abnormalities [39,46]. It appears then reasonable to suggest that when the proprioceptive system is stressed (for example, in platform sway-referenced conditions) small differences in sensory discrimination in the CLBP group, as compared to the healthy group, may become important for sway control. In conclusion, dynamic posturography was reliable and sensitive enough to distinguish CLBP patients as a group from a healthy population. CLBP patients showed an increased postural sway in the AP direction with a greater dependence on visual input under dynamic stance conditions. This may be an adaptive postural strategy to maintain equilibrium under conditions challenging stability. Further uses of dynamic posturography may include the development and guidance of CLBP treatment and evaluation of recovery progress.

Acknowledgements Dr. Raimondo della Volpe was nanced by a grant from University of Siena. We wish to thank Dr. Pietro Piu for statistical counseling. This work was in part nanced by a grant from the University of Siena (PAR 2003).

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