Altered postural control in anticipation of postural ... - Gait & Posture

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Gait & Posture 28 (2008) 657–662 www.elsevier.com/locate/gaitpost

Altered postural control in anticipation of postural instability in persons with recurrent low back pain Simon Brumagne *, Lotte Janssens, Evelien Janssens, Lieselotte Goddyn Musculoskeletal Research Unit, Department of Rehabilitation Sciences, Faculty of Kinesiology and Rehabilitation Sciences, University of Leuven, Tervuursevest 101, B-3001 Leuven, Brabant, Belgium Received 3 January 2007; received in revised form 1 April 2008; accepted 21 April 2008

Abstract Insight into the mechanisms of altered postural control in persons with low back pain (LBP) could lead to better interventions for patients with LBP. This study investigated (1) whether persons with recurrent LBP have an altered body inclination, and (2) whether anticipation of postural instability further alters body inclination. Thirty-three young healthy individuals and 56 young persons with recurrent LBP participated in this study. The upright standing posture was evaluated by means of two piezo-resistive electrogoniometers and a force platform for the conditions as follows: (1) quiet stance with and without vision, and (2) in anticipation of postural instability due to a ballistic arm movement or ankle muscle vibration. No differences in body inclination were observed when visual information was available between the two groups (P > 0.05). However, significant more forward inclination was seen in the persons with recurrent LBP when vision was occluded (+7.4%) and in anticipation of postural instability (+19%) (P < 0.05) compared to the healthy individuals. The results suggest that young persons with recurrent LBP have an altered body inclination that might be caused by anticipation of postural instability. The adopted forward inclined posture may potentially be a factor in the recurrence of LBP. # 2008 Elsevier B.V. All rights reserved. Keywords: Proprioception; Postural balance; Subjective vertical; Low back pain

1. Introduction Alterations in postural control have been reported in persons with low back pain (LBP). Compared with healthy controls, persons with LBP demonstrated a greater postural sway, an increased difficulty with adapting to changing conditions, and a decreased recovery of postural balance after perturbation [1–3]. Furthermore, persons with LBP seem to have altered proprioceptive sensitivity. Due to a less refined position sense of the lower back [4,5], reweighting of the proprioceptive input by increasing the gain at the ankle level seems to have taken place in persons with LBP [6,7], so that people with LBP tend to use less hip and low back movement for balance control in quiet standing [6–9].

* Corresponding author. Tel.: +32 16 329121; fax: +32 16 329197. E-mail address: [email protected] (S. Brumagne). 0966-6362/$ – see front matter # 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2008.04.015

The vertical orientation of the body in the upright standing position is maintained by a dynamic interplay of vision, proprioception, haptic contact cues, efferent control and internal models [10,11]. Sensory inflow is compared to the subjective vertical, the internal representation of verticality. On the basis of the comparison, compensatory reorientations of the body are performed with the aim of keeping the body longitudinal axis aligned with the vertical. The subjective vertical is also updated every time sensory inflow changes [12]. In patients with musculoskeletal impairments such as spasmodic torticollis (i.e., a pathological condition whereby torsion of the cervical spine due to neck muscle spasm occurs) changes in the reference system used in the control of body orientation have been demonstrated [13]. A small number of studies have reported alterations in the body inclination in relation to postural control in persons with LBP [1,2,6] despite the clinical relevance. However, the results have been inconsistent, with evidence supporting

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both a more anterior [6] and a more posterior [1,2] located center of mass (COM) compared to the neutral upright posture of healthy controls. The control of upright stance can change during conditions of increased postural anxiety. Adoption of postural strategies to maintain a tighter control of the COM by use of a stiffening strategy in response to increase perceived postural threat has been observed [14]. Although evidence for changes in balance control due to postural anxiety has been provided [15], all this evidence was obtained from a healthy young population. Since patients with LBP seem also to adopt a body stiffening strategy [7,9], the question arises whether the mechanism of anticipation of postural instability plays an important role in the altered postural control observed in persons with LBP. If so, adoption of an altered body inclination combined with a stiffening strategy (e.g., co-contraction of trunk muscles) when postural instability is anticipated could lead to more compressive forces on the spine [16]. Moreover, this postural strategy could reduce preparatory spinal movement [9,17], which may adversely affect spinal control. Consequently, the reduction in spinal movement counterproductively exposes the spine to greater resultant displacement, as recently observed in patients with recurrent LBP [9]. When the mechanisms of postural control in persons with and without LBP are better known, results could provide new insight into the choice of assessment and rehabilitation for postural control impairments in this patient population, e.g., postural tasks including anticipation of postural instability, learning differential control versus stiffening in demanding postural conditions. Accordingly, addressing these postural control mechanisms could be effective in the prevention of recurrence of LBP. The aim of this study was to examine whether possible changes in body inclination in persons with LBP could be identified as an aspect of postural control impairment and as a possible underlying mechanism of the high recurrence rate observed in patients with LBP. In addition, this study aims at investigating whether anticipation of postural instability further alters body inclination. Therefore, we evaluated body inclination in upright posture with and without vision in patients with recurrent LBP and healthy controls combined with anticipation of different degrees of postural perturbations such as ballistic arm movements or triceps surae muscle vibration. 2. Methods 2.1. Subjects Eighty-nine university students and personnel members participated in this study. A medical screening by a physician of the Sports Medical Advice Center, UZ Leuven was performed to include and exclude subjects in the study. Individuals with a history of vestibular disorder, neurological or respiratory disease, previous spinal surgery, acute radicular pathology or serious neck problems

Table 1 Characteristics of the subjects

Age (years) Height (cm) Weight (kg) PAI ODI-2 VAS LBP (years)

Persons with LBP (n = 56)

Healthy persons (n = 33)

22.7 1.1 174.5 9.3 62.4 7.7 9.0 2.3 9.2 5.4 1.5 1.8 4.0 3.1

23.2 1.2 173.9 7.2 65.0 8.2 8.9 2.4 0.0 0.0 0.0 0.0 0.0 0.0

NS NS NS NS

ODI-2 = Oswestry disability index; VAS = visual analogue scale for pain (0–10); PAI = physical activity index (0–15) [35]; LBP (years) = duration of low back pain in years. NS = not significant (P > 0.05).

were excluded. Subjects were included in the group with LBP when they had experienced non-specific LBP for more than 6 months, had at least three recurrent episodes, and had an Oswestry disability index (ODI-2) [18] score higher than six. The group with LBP included 56 subjects with LBP, while the ‘‘healthy’’ group consisted of 33 subjects who expressed an ODI-2 score and a visual analogue scale (VAS) for pain score equal to zero (Table 1). The study was approved by the local Ethics Committee of Biomedical Sciences of the K.U. Leuven, Belgium. All participants gave their written informed consent. 2.2. Experimental procedure Subjects stood barefoot on a force platform with their feet separated by the width of their hips and their hands at their sides. The position of the feet was marked on a plastic sheet attached to the force platform to enable standardization of the subsequent trials. They were instructed to remain still and relaxed. In the first trial, the subject was instructed to look straightforward to a white wall. In all other trials, vision was occluded by means of special liquid-crystal goggles (Translucent Technologies, Canada). When the subjects wore the goggles, they were asked to keep the eyes open and to keep the gaze in a straight-ahead direction [19]. Vision was suppressed to evaluate the contribution of proprioceptive signals in the control of body inclination. Body inclination (Angle in degrees) and postural sway characteristics were appraised in six consecutive conditions (Table 2). Actual trial duration was 60 s for trials 1 and 2, and 15 s for the anticipation of postural instability trials 3–5. Between each trial, rest periods of 2 min with vision and change of posture (i.e., stepping off the platform and moving around) were given to decrease post-vibration effects [20]. Different degrees of anticipation of postural instability were created by inducing distinct postural perturbations. Ballistic arm abduction movements were used to create an internal perturbation to postural stability (Condition 3) [17]. Muscle vibration was applied bilaterally to the triceps surae muscles to induce increased anticipation of postural instability (Conditions 4 and 5). When vibration, known as a potent stimulus for muscle spindles [21,22], is applied to the leg muscles during quiet standing, it can induce postural instability, sometimes to the point of falling [6,23]. Short (1–2 s) and longer (15 s) vibration stimuli were used to evaluate the effect of smaller and larger anticipation of postural instability, respectively. Activation and deactivation of the vibrators were manually controlled. The characteristics of vibration (frequency = 60 Hz, amplitude = 0.5 mm) were chosen to induce a maximal illusion of joint movement [21,22]. The respective postural


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Table 2 Experimental procedure Trial 1: quiet stance with vision Trial 2: quiet stance with vision occlusion Pre-trial 3: performing of ballistic arm bilateral arm movement ! rest (2 min) Trial 3: vision occlusion ! quiet stance with expectation of ballistic bilateral arm movement at 15 s and possibly postural instability (internal perturbation) Pre-trial 4: vision occlusion, short soleus muscle vibration (1–2 s) ! rest (2 min) Trial 4: vision occlusion, actual trial: quiet stance with expectation of short muscle vibration and possibly postural instability at 15 s Pre-trial 5: vision occlusion, long soleus muscle vibration (15 s) ! rest (2 min) Trial 5: vision occlusion, actual trial: quiet stance with expectation of long muscle vibration and possibly postural instability at 15 s Trial 6: estimation of limits of stability ! neutral stance ! maximal forward leaning ! neutral stance ! maximal backward leaning ! neutral stance Trials were performed in fixed order. Rest period included vision and stepping off the force platform.

perturbation was executed before the actual trial recording (trials 3–5) followed by a 2-min rest period. Just before the actual trial recording, subjects were told that they could expect the respective perturbation after 15 s. While both the LBP and healthy groups expressed on a numerical rating scale (0 = no fear of falling, 10 = maximal fear of falling) no or almost no fear for falling during Conditions 1 (0/10) and 2 (0.8 0.8, 0.6 0.8, respectively), and little during Condition 3 (1.6 2.2, 1.5 2.3, respectively), higher scores were expressed during Condition 4 (4.9 2.7, 4.6 2.3, respectively) and Condition 5 (6.3 2.8, 6.0 2.9, respectively), showing larger anticipation of postural instability from these postural perturbations. No significant differences in fear of falling scores were found between the two groups (P > 0.05).

trunk inclination and COP displacement (from trials 1 to 5) relative to the individual limits of stability. During all trials, minor variations were measured between accelerometer 1 and 2. Hence, for clarity, only data from the accelerometer 1 (Th1) are given. All data are presented as means standard deviation (S.D.). The significance level was set at P < 0.05. Statistical analysis was performed with Statistica, Version 7.1 (OK, USA).

3. Results No differences in body inclination were observed when visual information was available between the LBP groups

2.3. Instruments 2.3.1. Force platform and accelerometers Postural sway characteristics (mean center of pressure (COP) position and RMS values) of a standing subject were measured using a six-channel force platform (Bertec Corporation, OH, USA). To evaluate body inclination in space, two lightweight piezoresistive built-in amplified and temperature compensated accelerometers, model 3140-002 (ICSensors, UK) was used as electrogoniometers by measuring the static component of gravity [24]. The electrogoniometers were fixed with double-sided tape to the skin over the spinous processes of the first thoracic vertebra (Th1) and second sacral vertebra (S2) in upright posture and provided online information about the relative angle of the thorax and the sacrum in space. Force platform and accelerometer data were sampled at 500 Hz using a Micro 1401 data acquisition system and Spike2 software (Cambridge Electronic Design, UK) and low pass filtered with a cutoff frequency of 5 Hz (Fig. 1). 2.4. Statistical analysis To examine differences in characteristics of the subjects between the two groups a t-test was used (Table 1). Differences in mean and RMS values of COP displacements and differences in body inclination between trials and groups were evaluated using a repeated measures MANOVA. Where a significant main and interaction effect was found post hoc tests (Scheffe´) were performed to further analyze the detailed effects. The data from trial 6 (limits of stability) were only used to determine the changes of

Fig. 1. Experimental set-up.

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A significant interaction between group and the trials (trials 1–5) was demonstrated (F(3, 87) = 26.13, P < 0.001). Further post hoc analysis revealed a significant difference between the LBP group and the healthy group during the control vision occlusion trial (trial 2) (P < 0.05). Further differences (P < 0.05) were demonstrated for the different levels of anticipation of postural instability conditions (trials 3–5). Whereas the healthy individuals moved their trunk in the direction of the true gravitational vertical (positive values, Fig. 3) (trials 2–5), the persons with LBP leaned more forward when vision was occluded (trial 2) (+7.4%) and when postural instability (trials 3–5) was anticipated (+19%) (negative values, Fig. 3).

4. Discussion

Fig. 2. Raw center of pressure (COP) data of a representative person with LBP (A) and a healthy control subject (B). For clarity, only the COP data of the vision condition (black dots), vision occlusion condition (dark grey traces), and anticipation of long vibration (light grey traces) are displayed. Note that the mean position of the COP of the persons with LBP already is more anteriorly positioned in the control vision condition compared to the healthy subject.

and healthy persons (P > 0.05). However, a tendency was seen that persons with LBP had already a more anterior positioned mean COP compared to the healthy individuals in the vision condition (P = 0.06) (e.g., Fig. 2).

Fig. 3. Comparison of trunk inclination differences in degrees between the LBP group and healthy group during vision occlusion, anticipation of ballistic arm movement, anticipation of short vibration and long vibration conditions. Negative values represent forward trunk inclination and positive values represent backward trunk inclination, compared to the control vision condition.

The main finding of the current work is that young persons with LBP showed an altered body inclination during conditions that challenge postural control compared to healthy young persons by leaning more forward when postural instability was anticipated. An offset in the reference frame in the anterior direction might explain the findings that individuals with LBP have changed their trunk inclination when vision was occluded. This is in agreement with results in patients with spasmodic torticollis who have been observed to have changes in the reference system used in the control of body inclination [13]. When visual signals are unavailable, the body had to be oriented mainly on the basis of proprioceptive and vestibular signals. However, persons with LBP have been observed to have less refined position sense of the lower back [4,5]. Moreover, reweighting of the proprioceptive input by increasing the gain at the ankle level seems to have taken place in persons with LBP [6,7], so that persons with LBP tend to use an ankle strategy for balance control in quiet standing [6–8]. This strategy has been described as common during quiet standing, but inadequate when postural demands increase [6,7,25], particularly when proprioceptive signals from the ankles are challenged, such as standing on an unstable support surface [29]. Alternatively, it is possible that the adopted forward inclined posture is a purposeful protective mechanism to prevent postural instability. In a study of Popa et al. persons with chronic LBP showed significantly more forward inclined postures compared to healthy controls in expectation of a first backward platform translation, similar to the findings of our study [26]. However, after repeated perturbed trials the subjects with chronic LBP demonstrated less forward lean. This suggests that prior experience has a profound influence on postural strategy selection and that persons with chronic LBP can adapt to more optimal postures. Postural anxiety and fear of falling might be another explanation for the changes in body inclination in persons with LBP in the present work. In healthy subjects, the COP is


positioned posterior (closer to the ankle) to the middle of the support base (i.e., feet). As postural control is less accurate in persons with LBP, increasing the safety margins would lead to a more stable posture. Hence, a possible way to compensate for loss of stability is to position the body COP more in the middle of the support base, i.e., performing a forward inclination of the body. Such a forward displacement of the mean position of the COP is also reported in elderly subjects who reported fear of falling [27]. Another advantage of the forward inclination of the body is the proprioceptive benefit at the ankles. In a forward inclined body posture with the heels on the ground, the muscle spindles of the triceps surae are in an elongated position which increases their sensitivity [28]. A postural control strategy that is mainly based on proprioceptive input from the ankles profits thus by a similar change of position. In addition, it is possible that the changes of proprioceptive feedback from segments of the body other than the trunk (e.g., soleus muscles) in persons with LBP may necessitate, based on a similar mechanism, a more forward inclined posture [29,30]. Consequently, moving the mean COP more forward in anticipation of postural instability could be beneficial to maintain postural stability in the short-term for compensating for the possible loss of proprioceptive acuity at the low back and/or ankles. On the other hand, a more forward body inclination increases back muscle activation. Whereas the healthy subjects adopted a more vertical orientation, i.e., a more efficient posture which requires less energy, the adoption of a more forward inclined orientation requires more energy from the subject with LBP. Moreover, the adopted position and the increased back muscle activity could lead to undue loading of the spine [16,31] and might be more associated with the development of symptomatic spinal degenerative changes [32,33]. Increased and prolonged isometric back muscle activity could also have a strong effect on the internal representation of the body position and orientation [10]. As a result, the body scheme might be adapted, i.e., with a reference frame offset in the anterior direction. In contrast with the results of the current work, two studies reported a more posterior oriented COP in persons with LBP, compared to pain-free control subjects [1,2]. This discrepancy may be explained by the differences both in sensory conditions and in characteristics of the subjects. In the study of Mientjes and Frank the less anterior located COP in the LBP group was only observed during the vision condition and/or when the head was tilted backwards [2]. These studies also examined middle-aged patients with a history of LBP of 10 years, whereas the subjects of the current study were recruited from a young population with a shorter history of LBP. This might indicate that in the first stage of LBP body inclination is more forward inclined in complex balance conditions, and that in time body inclination might change in the posterior direction (e.g., sway back position). The authors of the two former studies hypothesized that the posterior oriented posture would relax

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the trunk extensors through lordosis, or that it is adopted as a result of reduced knee extension. The first hypothesis of these authors (i.e., relaxation of back muscles through a lordotic posture) could be still in accordance with the results of the current work since forward inclination of the body could increase the activity of the back muscles and to decrease the energy expenditure on the long run, a sway back position might be a solution. However, this posture might be optimal based on energy expenditure, but not for loading of the spine. This posture has been observed to be more associated with degenerative spondylolisthesis [33]. The alternative explanation for a more posterior oriented posture due to the adoption of less knee extension in persons with LBP is not in accordance with the observations of the current study. In our study, all persons with LBP locked their knees in an extended position. Moreover, the adoption of knee flexion (not locking of knees) has been described as a fundamental component of a multi-segmental balance strategy, whereas knee extension during standing, which will stretch the calf muscles and thus, enhance the input of the ankle muscle spindles [28], often indicates an ankle strategy [34]. Since individuals with LBP have been demonstrated to rely more on an ankle strategy to control balance [6–8], this would indicate a lesser support for the second explanation of these authors. Further analysis and comparison of body inclination in persons with and without LBP could be fruitful in understanding the postural control strategies used by persons with and without LBP. Several methodological issues warrant discussion. First, no randomization of the testing order was performed. Carryover and learning effects cannot be excluded, however, rest periods between the trials were provided to minimize carryover effects. In previous studies with similar testing protocol, when random testing order was compared to fixed testing order no different results were obtained (Brumagne et al., unpublished data). Because of data analysis convenience, a fixed testing order was chosen for this study. In addition, because the subjects were instructed to change position between trials and because of the short duration of vibration, post-effects due to vibration were minimized [20]. However, in future studies, electromyography of the ankle muscles could prove fruitful to monitor whether tonic activity of the ankle muscles plays a role in altered body inclination. Second, despite the accuracy and reliability of piezo-resistive accelerometers in measuring body inclination [24], 3D-motion analysis systems could provide more detailed information on position and movement of all body segments, so that it is possible to determine at which specific joint movement occurs in order to move the COP forward, which was not possible with the instruments used in our study. Third, we acknowledge that the results of this study cannot be generalized to a more typical LBP patient population, i.e., older age and more disabled. However, the findings of this study might shed light on the

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postural control mechanism of the high recurrence rate observed in persons with LBP. Therefore, future research comparing young persons with LBP with patients of older age and with higher disability would further test the proposed hypothesis. In conclusion, young persons with LBP tend to position their body COM more in the middle of the support base in anticipation of postural instability, however, at the possible expense of increased trunk muscle activity. This mechanism might be a factor in the high recurrence rate of LBP. In addition, it could prove fruitful to research whether the altered postural control can also be observed in an older and more disabled patient population, hopefully leading to a more complete understanding of the mechanisms of altered postural control and to better interventions for persons with LBP.

Acknowledgements This work was supported by grants from the Research Council K.U. Leuven (PDM/99/121) and Fund for Scientific Research-Flanders (1.5.104.03). Conflict of interest statement The authors disclose any financial and personal relationships with other people or organizations that could inappropriately influence their work.

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