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Effect of bracing or surgical treatments on balance control in idiopathic scoliosis: three case studies.

Introduction

Scoliosis is the most common spinal deformity among adolescents. (1) It can be congenital or have an early onset between birth and 3 years of age (infantile), develop between 2 and 10 (juvenile), or it even develops during adulthood as a degenerative scoliosis. Scoliosis takes place mostly during adolescence, the prevalence is approximately 2-3% in children ages 10 to 16 years, and is more frequent in females. (2, 3) Scoliosis is characterized or classically defined as a lateral deviation of the spine, but in fact, it is a three-dimensional (3D) deformation inducing geometric and morphologic changes in trunk and rib cage. (4)

Etiology

Harrington (5) has suggested that over 50 pathologies generate a secondary scoliosis. Among these pathologies, various neuromuscular diseases such as anterior poliomyelitis with trunk paralysis, multiple sclerosis, but also malformations such as congenital hemi-vertebra cause secondary scoliosis. Nonetheless, 80% of scoliosis is still considered as idiopathic. (5) It is unlikely, however, that the etiopathogenesis of idiopathic scoliosis results from a unique factor. In contrast, it is believed that various factors are involved and interact with various genetic predisposing factors. (6, 7) The current trend in scoliosis research is to detect biomarkers that could predict either spine deformation onset or progression risk. (6) The common factors that are being investigated could be aggregated into 6 groups: genetic, neurological, hormonal and metabolic, skeletal growth, biomechanical, environmental. (8) During the last decades, various studies have investigated whether AIS patients had perceptual or sensorimotor impairments. It has been reported that AIS patients have deficits in sensorimotor adaptation and balance control and perceptual impairments. (9)

Vestibular system and scoliosis

An efficient control of upright balance implies the detection of instability (i.e., its direction and amplitude) and the selection of appropriate motor commands to restore stability. (10, 11) Therefore, these processes require accurate sensory systems, optimal sensory processing and sensorimotor transformation. Altering the quality of sensory information allows studying the ability of the brain to re-weight the sensory signal and select the appropriate motor commands to ascertain proper balance control. Results from studies assessing balance control have demonstrated that AIS patients have poorer balance control than controls and manipulating the availability of visual information or the quality of lower limb sensory information increased their disequilibrium. (12-15) The role of ankle proprioception, for controlling balance, has been studied in AIS patients by co-vibrating the tendon of the ankle joint, which altered the sensory information, and led to greater instability of AIS patients than controls. (16) Furthermore, following a brief period of sensory deprivation it has been shown that reintegration of ankle proprioception, whether vision was available or not, led to larger variability of the CP velocity in AIS patients whereas the age-matched controls reduced their CP velocity variability. (17)

Another sensory system that is worth investigating as a potential factor for scoliosis onset is the vestibular apparatus. (18-20) For instance, the vestibular nuclei occupy a prominent position in the brainstem. Since the lateral vestibulospinal tract controls axial muscles (21), it is thought that alteration in the brainstem or the cortical network involved in sensorimotor transformation, during body growth (i.e., preadolescent and adolescent period) may translate into abnormal trunk muscles activation causing permanent spinal deformities. (19, 22) It has been reported that AIS patients, when asked to judge the amplitude of the whole body rotation, underestimated the amplitude of the angular displacement to a greater extent than controls. (18) However, in this last study, the vestibulo-ocular reflex (VOR) gain (defined as eye speed divided by head speed) of the AIS patients was similar to controls. These latest results promote the suggestion that it is the cortical mechanisms performing the sensory processing and sensorimotor transformation rather than the brainstem that is malfunctioning in AIS patients. (23-25)

One way to assess sensorimotor transformation capability is to manipulate sensory information and quantify its effect on motor control. For instance, the role of vestibular information on upright balance control can be evaluated using bipolar binaural galvanic vestibular stimulation (GVS). (22, 26-28) With the head in neutral position, GVS evokes body sway mainly along the frontal plane and the direction is toward the side of the anode. (29) By changing the polarity of the stimulation (i.e., anode on the right or left mastoid), body sway can be induced on the right or left. Using vestibular stimulation, abnormal vestibulomotor control has been observed in AIS patients; compared to controls AIS patients demonstrated larger body sway either during or immediately after GVS cessation. (30)

It has been suggested that scoliosis could be related to a delay in the development or a distortion of the body schema. (9, 31) Although attractive, this suggestion should be further investigated. Body schema refers to specific neural cortical networks holding an updated map of the body shape, dimension and posture. In other words, at the cortical level, the processing of the various sensory signals forms a sensory map of the body. (32) As an example, when using a tool to elongate the hand the brain needs to take into account the change in the body dynamics to ascertain proper movements. (33) In such a case, the body schema is updated; the participants perceive their arm as being longer. (34) Proprioception and vision are crucial for body schema updating, however, it has been recently suggested that vestibular information also contributes to body schema updating. (33, 35-37) For instance, it has been demonstrated that vestibular stimulation enhances somatosensory input and even modulates visual processing. (36, 38) Furthermore, it has been reported that patients with vestibular disorders might encounter distortions of their body schema. (37) Consequently, dysfunction in the mechanisms processing sensory information can cause asymmetry or a change in the amplitude of the vestibulomotor commands and alters the body schema. During rapid spine growth, this condition would lead to spine deformation and asymmetrical trunk proprioception promoting the updating of a distorted body schema (Fig. 1). (31, 34, 39)

The present study is part of a research programme assessing the vestibulomotor control of balance in AIS. The objective of the present study was to establish an experimental framework for testing whether spine deformation could be related to a distortion of the body schema. Since the body schema is continuously updated through sensory signals, it is possible that surgical intervention that drastically reduces spine deformation or bracing that creates proprioceptive rehabilitation, through torso proprioceptive cues, lead to a recalibration of the body schema. If this is the case, improvement in balance control either during or after sensory manipulation should be observed following spine surgery or long-term bracing. If this hypothesis is supported, it would indicate that the weight of proprioceptive information from the torso is larger than the weight of vestibular information (participants are tested in absence of vision) in the updating of body schema. An alternate hypothesis is that balance control improvement is caused by a decrease in the biomechanical forces acting on the spine due to a lessening of the spinal curvature. It has been demonstrated, however, that reintegration of sensory information altered balance in AIS patients which favours the first hypothesis. (17) In contrast, if body sway does not decrease following spine surgery or long-term bracing, it would suggest that the cortical mechanisms involved in sensorimotor transformation are impaired. In this case, although straightening the spine or bracing would improve torso proprioceptive cues, it would not be sufficient to recalibrate effectively the body schema.

Methods

Three participants were involved in this study. All of them gave their written informed consent according to Laval University biomedical ethics committee. Vestibular stimulations were delivered using a DS5 bipolar constant current stimulator (Digitimer Ltd, Garden City, UK). The skin behind the ears over the mastoid process was prepared bilaterally using electrode skin prep pad (Dynarex, Orangeburg NY, USA) before placing the PALS Platinum 3.2 cm electrodes (Axelgaard Manufacturing Co Ltd, Failbrook CA, USA). The electrodes were secured using 3M Transpore Tape 1527-1(3M). Participants performed the same tasks; they stood upright with their eyes closed and their feet 2 cm apart and with each foot standing on a force platform. Balance control was assessed using two force platforms (AMTI-model BP400600NC-1000, Watertown, MA, USA). The horizontal displacement of the torso along the frontal plane was evaluated using sensors (Polhemus--model Liberty 240/8, Colchester VT, USA) located at C7 and L5/S1. Because these measurements are influenced by either the height (i.e., L5/S1 and C7 displacement) or the weight (i.e., vertical force) of the participants, sensor horizontal displacement was normalized to participant's height and the vertical forces were normalized to participant's weight. For each trial, data acquisition started only when the participant's weight was evenly distributed according to the amplitude of each foot vertical force. Each trial was divided into four epochs. The first 2-seconds were used to assess baseline balance control prior to GVS (preGVS [2 0]). The following 2-seconds served to evaluate vestibulomotor control. A GVS of 1mA of amplitude and lasting 2 seconds was applied to assess vestibulomotor control (GVS [0 2]). For 15 trials, the anode was located on the left mastoid process (inducing a right to left body movement along the frontal plane) and for 15 trials the anode was located on the right mastoid process (inducing a left to right body movement along the frontal plane). The first second, following GVS, permitted to assess balance control during sensory reintegration ([2 3]) while the following 2-second was used to evaluate whether participants' balance control returned to baseline level (balance recovery [3 5]). The body sways of the two AIS patients were compared to normative data obtained from 15 age-related adolescents without spine deformities or neurological problems (control group--CTR). For the adult case, the control group is composed of 16 age-related young adults. AIS participants were evaluated twice; the second assessment occurred at least 12-month following the initial evaluation (hereafter, T0 and T1 are used to evoke the first and second evaluation). The same experimenter and the same material were used for both evaluations. From the force platform data, the Root Mean Square values (RMS) of the vertical forces were computed before vestibular stimulation (pre-GVS [-2 0] interval), during vestibular stimulation (GVS [0 2] interval), immediately after the cessation of the stimulation (sensory reintegration [2 3] interval), or later in time (balance recovery: post [3 5] interval). Normative data for the RMS vertical force value calculated in the two control groups are presented in Table 1.

Case 1: Effect of spine surgery on balance control

This case concerns a 17-year-old male. He was 14 years old when he first saw his orthopedic surgeon. The assessment of his balance control was performed when he was 15 year old. There were 3 other known cases of scoliosis in his family: his 2-year younger sister (mild scoliosis, Cobb angle = 20[degrees]), his mother (unknown Cobb angle), and his mother's sister (she probably had a severe spine deformation since she had had corrective spinal surgery). At the initial balance control assessment (T0), his Risser sign was 1 (i.e., index of osseous maturity based on iliac crest ossification, ranging from 0 to 5) and he had a 52[degrees] right thoracic curve and a 34[degrees] left lumbar curve. At the age of 16, he underwent surgery. Pre-surgery neurological routine examination did not report any findings. Motor conductance was normal in both lower limbs, sensory conductance was difficult to obtain on the right side but lumbar spine MRI was normal. The surgery consisted of reducing the curves and vertebrae rotations using transpedicular screws from the third thoracic to third lumbar vertebrae and two Harrington rods. Following the surgery (T1), 18-months later, he had an 18[degrees] right thoracic curve and a 14[degrees] left lumbar curve. His Risser sign was 5. Because spine deformation and surgical instrumentation necessarily constrained trunk mobility, the participant's trunk maximal voluntary range of motion along the frontal plane was quantified using the sensors located on the 5th lumbar vertebra (L5), and on the 7th cervical vertebra (C7). Right and left maximal voluntary trunk flexions were 30[degrees]and 38[degrees] before surgery (T0) and 23[degrees] and 27[degrees] following surgery (T1). Maximal torso deviations, due to vestibular stimulation, were smaller than his voluntary range of motion: 4[degrees] and 6[degrees] at T0 and 2[degrees] and 2[degrees] at T1 for right and left movements, respectively.

Before spine surgery, his balance instability was much larger than controls during and after vestibular stimulation; the vertical force RMS values were 2.4 times greater than controls during GVS ([0-2]) and 4.9 times immediately following GVS (i.e., sensory reintegration epoch, [2-3]) (Fig. 2). Following spine surgery (T1), however, his balance control slightly improved. For instance, his vertical force RMS values were both 1.3 times greater than controls for the GVS and sensory reintegration epochs, respectively. It is worth noting that, following spine surgery, his vertical force RMS values diverged slightly from controls during the GVS epoch mainly because the vertical force slightly increased toward the end of the interval whereas it leveled out for controls. Overall, for this AIS patient, it seems that the spine surgery improved his balance control.

Case 2: Effect of bracing on balance control

Case 2 is a 15-year-old girl and the sister of case 1. Her balance control assessments were performed the same day as her brother. At that time (T0), she was 13 when a 16[degrees] right thoracic curve and a 13[degrees] left lumbar curve were detected. At the time, her Risser sign was 2. Before the first balance control evaluation, the patient had been wearing a Providence brace for 2 months and was still wearing it 18-months later (i.e., at T1). Bracing did not change much her spine deformation; she had a 17[degrees] right thoracic curve and a 23[degrees] left lumbar curve and her Risser sign was 4. At initial evaluation (T0), during the vestibular stimulation, her balance control was impaired compared to controls; the vertical force RMS value was 2.4 times larger (Fig. 3). Furthermore, her vertical force RMS value was 3 times larger than controls immediately following GVS (i.e., sensory reintegration interval, [2 3]) and she could not recover her balance to the same extent as the controls (balance recovery interval, [3 5]). Eighteen months later (T1), during GVS, her vertical force RMS value was 2.6 larger than control. Although it seems that the amplitude of her vertical force slightly decreased; her balance control was still impaired compared to controls. Immediately following the cessation of GVS (i.e., sensory reintegration interval), her vertical force RMS value was 2.6 times greater than controls. Finally, it is worth noting that compared to controls, she had trouble recovering her balance; the amplitude of her vertical forces did not reach a steady state. Overall, the present results suggest that long-term torso proprioceptive cue provided by the brace partly improved (but still larger than controls) balance control while her lumbar deformation increased by 10[degrees]. This latest result suggests that the amplitude of the spine deformation is not necessary related to balance control impairment.

Case 3: Effect of spine surgery in adult on balance control

This participant is a 20-year-old woman. There are two other known cases of scoliosis in her family: her grandmother and her older sister underwent spine surgery. Her scoliosis has been diagnosed when she was 11. Between the diagnosis and the surgery, she had been braced. A first surgery was performed when she was 14 and a second surgery when she was 16. Before the first surgery, she had a 70[degrees] right thoracic curve and a 55[degrees] left lumbar curve. The last assessment of her spine deformation revealed that she still had a 35[degrees] right thoracic curve and a 30[degrees] left lumbar curve. The balance control assessment was realized following both spine surgeries. The analysis of the vertical force time-series during GVS revealed that her balance control was worse than controls; her vertical force RMS value was 2.3 larger than controls (Fig. 4). Furthermore, immediately following vestibular stimulation (i.e., sensory reintegration epoch [2 3]), her balance control was still worse than controls; her vertical force RMS value was 4.5 times larger. Across time (i.e., balance recovery epoch, [3 5]), however, her vertical forces drastically decreased but her RMS value was still 1.9 larger than controls. Overall, it is concluded that despite the absence of a complete reduction in her spine deformation, compared to controls, the cortical mechanisms performing sensorimotor transformation are impaired.

Discussion

Visual, proprioceptive and vestibular information contribute to the perception of the body shape, dimension and relative limb position with respect to each other (body representation). Since it has long been reported that AIS patients have sensory processing impairments (16, 17, 19, 40-43), it is plausible to suggest that AIS patients could have a distorted body representation. The aim of this study was to present an experimental framework to evaluate this suggestion. It was hypothesized that reducing spine deformation, through conventional treatment, should allow recalibrating body schema. As a result, reduction in spine deformation should translate into balance control improvement either during or following sensory manipulation.

Bracing or surgery effect

Results have demonstrated that for cases 1 and 2, either the spine surgery or bracing slightly improved balance control. For both cases, however, balance control was still impaired during or following vestibular stimulation. For these patients, altering the asymmetry in torso proprioception through spine surgery or providing torso proprioceptive cue via bracing partly improved balance control. The cortical mechanisms that update the body schema likely weight differently the sensory signals. (17, 44) Consequently, for some patients, straightening the spine or wearing a brace could partly reduce body representation distortion. For these individuals, alteration in the sensorimotor transformation of vestibular information would not be completely eliminated by the torso proprioception. In conclusion, it is speculated that for these two cases, improvement in balance control during sensory deprivation or sensory reintegration implies a better body representation.

For case 3, the reduction in spine deformation, through two surgeries, did not reduce her balance sway to the same extent as controls either during or immediately following sensory manipulation. Nonetheless, it is worth mentioning that she still had a spine deformation post-surgery (i.e., 35[degrees] right thoracic curve and a 30[degrees] left lumbar curve). Therefore, one may suggest that balance control impairment was related to biomechanical factor. The increase in vertical force immediately following vestibular stimulation rule out this suggestion as performing sensory reintegration led to balance control impairment. As a result, it seems that asymmetrical torso proprioceptive information (i.e., distorted body representation) led to suboptimal sensorimotor transformation and inefficient balance control.

Treatment of AIS

The recommendation from the Scoliosis Research Society (SRS) indicates that for curves between 25[degrees] and 40[degrees] patients should be braced. (45-47) For these curve severities, surgical treatment is not necessary as long as the curve remains below 45[degrees] even if it progresses despite bracing. Surgical treatment is recommended for patients that are still growing with curve greater than 45[degrees], or if the curve is larger than 45[degrees] and continues to progress even if growth has stopped. The purpose of surgical intervention is twofold: i) to prevent curve progression and ii) to reduce spine deformation. On the other hand, bracing only slows curve progression. Therefore, to be efficient, bracing must be prescribed as soon as possible. Bracing is considered an effective treatment with 72% of success ( i.e., the curve did not worsen) compared to 42% after observation. (48) Furthermore, there is a significant positive association between hours of bracing and treatment success; 12.9 daily hours of bracing entails a success rate of 90 %. (48)

Limitations and research recommendation

Undoubtedly, scoliosis onset or progression involves multiple factors. Alteration in the processing of sensory information or in the mechanisms performing sensorimotor transformation could be related to a genetic defect, for example. Therefore, alterations in sensorimotor transformation, for example due to a distortion in body representation, might be related to scoliosis onset or progression in some patients. This case series propose a tentative experimental framework to explore whether a potential link between body representation and scoliosis exists. This study has various limitations. Obviously, to better test the experimental framework and draw any conclusion, more AIS patients need to be tested before and after spine surgery to thoroughly verify whether reduction in spine deformation translate into a better body representation. Because of its complex aetiology, it is proposed that grouping AIS patients based on the severity of the spine deformation could mix patients with various causes (e.g., genetic, neurological dysfunction, hormonal). Consequently, an approach based on detecting the prevalence of a biomarker (e.g., vestibular impairment) should be used. (49)

The motor response evoked by GVS is reliable in healthy individuals and individuals with vestibular pathology over weeks (personal communication with the authors). (50) Although in the present study balance control was studied after several months, we are confident that this period did not affect our results since the motor responses evoked by GVS are unaffected up to 60 years old.

Conclusion

Overall, the present results suggest that reducing spine deformation does not necessary translate in balance control improvement. The three cases demonstrated different behaviour following conventional treatment. For instance, spine surgery improved to a great extent balance control in case 1 either during or following sensory manipulation. In contrast, bracing had a slight effect for case 2 while her lumbar deformation increased by 10[degrees]. For case 3, reduction in spine deformation through surgeries did not translate in balance control similar to controls. The absence of clear-cut results supports the idea that AIS is a multi-factorial pathology. Consequently, studying the effects of conventional treatment on balance control while manipulating sensory information (e.g., through GVS) could give some insights into the physiopathology of AIS patients with balance control impairment.

Acknowledgements

This project has been supported by Fondation Cotrel de l'Institut de France. JPP has been awarded a scholarship from Fonds de Recherche du Quebec en Sante, and has been supported by Fondation de Recherche Chiropratique du Quebec and European Chiropractic Union.

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Jean-Philippe Pialasse, DC, MSc, PhD(c) (a, b) Martin Simoneau, PhD (a, b)

(a) Faculte de medecine, Departement de kinesiologie, Universite Laval, 2300 Rue de la Terrasse, Quebec, Quebec, Canada G1V 0A6

(b) Centre de recherche du CHU de Quebec, Quebec, Quebec, Canada

Corresponding Author: Jean-Philippe Pialasse, PhD(c), 1(418)656-2131 extension 14784, jppialasse@pialasse.com Universite Laval, 2300 Rue de la Terrasse, Quebec, Quebec, Canada G1V 0A6

All participants gave their informed consent according to the Laval University Biomedical Ethics Committee.

This project has been partly supported by Fondation Cotrel de 1'Institut de France. JPP has been awarded a scholarship from Fond de Recherche du Quebec en Sante, and has been supported by Fondation de Recherche Chiropratique du Quebec and the European Chiropractic Union.

Table 1:
Root mean square (RMS) values of the vertical force before (pre),
during or after galvanic vestibular stimulation (GVS). These data are
from a group of healthy adolescent (n = 16) and a group of healthy
young adult (n = 15). Data are the means (standard deviation) of 15
trials per side.

                   [-2 0]           [0 2]                [2 3]
                  pre-GVS            GVS         Sensory Reintegration

Adolescents    0.27 (0.07) /    0.48 (0.11) /        0.64 (0.19) /
Right / Left    0.27 (0.07)      0.51 (0.18)          0.64 (0.20)

Young adults   0.23 (0.11) /    0.45 (0.16) /        0.61 (0.22) /
Right / Left    0.24 (0.10)      0.45 (0.13)          0.66 (0.24)

                    [3 5]
               Balance Recovery

Adolescents     0.52 (0.15) /
Right / Left     0.56 (0.16)

Young adults    0.46 (0.17) /
Right / Left     0.45 (0.12)
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Author:Pialasse, Jean-Philippe; Simoneau, Martin
Publication:Journal of the Canadian Chiropractic Association
Article Type:Case study
Geographic Code:1CQUE
Date:Apr 1, 2014
Words:5234
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