Gait & Posture 37 (2013) 82–87
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Impact of pre-operative regular physical activity on balance control compensation after vestibular schwannoma surgery Ge´rome C. Gauchard a,b,c,*, Ce´cile Parietti-Winkler a,b,c, Alexis Lion a,b, Claude Simon c, Philippe P. Perrin a,b,c a
National Institute for Health and Medical Research (Inserm), U 954, Thematic group ‘‘Neurodegenerative diseases, Neuroplasticity, Cognition’’, Faculty of Medicine, Vandoeuvre-le`sNancy, France Nancy University, Henri Poincare´ University, Balance Control & Motor Performance, UFR STAPS, Villers-le`s-Nancy, France c Department of ENT, University Hospital of Nancy, Nancy, France b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 30 August 2011 Received in revised form 31 May 2012 Accepted 16 June 2012
Vestibular compensation after unilateral vestibular deafferentation is modulated by certain individual characteristics, such as pre-operative visual neurosensory preference or vestibular pattern. Physical activity (PA) allows the implementation of new sensorimotor and behavioral strategies leading to an improvement of balance control. This study aimed to evaluate the effect of the level of PA before surgery on balance compensatory mechanisms in patients after vestibular schwannoma (VS) surgery. Thirty patients with VS, 15 considered as regularly physically active and 15 as sedentary participated in this study, including an evaluation of gaze control by videonystagmography and postural control by a sensory organization test. Patients considered as physically active before surgery presented the best pattern of postural compensation, with the classical decrease in postural performances at short term (i.e. eight days) and the increase in postural performances at middle and long terms (i.e. 90 and 180 days, respectively) after surgery. For the sedentary patients, the consequences of surgery were more difficult to manage at short term, even though this did not prevent the ability to compensate well later on. Preoperative practice of PA promotes the neuroplasticity of neural networks involved in motor learning, which allows to benefit of physical therapy more rapidly and efficiently. ß 2012 Elsevier B.V. All rights reserved.
Keywords: Vestibular schwannoma Balance control Unilateral vestibular deafferentation Physical activity Neuroplasticity
1. Introduction Some factors are known to modify the time-course of postural compensation after vestibular schwannoma (VS) surgery, such as the pre-operative vestibular pattern, the origin of the tumor on the vestibular nerve or the pre-operative preference of visual cues to control balance [1–3]. So far, no study was interested in the potential role of physical activity (PA) on compensatory mechanisms related to VS and its removal. Many studies have shown that PA, of any kind (leisure sport, gardening, do-it yourself (masonry, joinery, plumbing, electricity, etc.)), could influence postural mechanisms at any level of balance regulation and limit the risk of falling [4,5]. The effects of physical therapy on the pathophysiology of vestibular and postural compensation are better known. Vestibular exercises are known to speed up the rate of vestibular
compensation and limit the dispersion of vestibulo-ocular reflex (VOR) asymmetry [6], resulting in an improved postural stability through a diminished perception of disequilibrium and an increase in reliance on proprioceptive information [7]. However, while vestibular exercises performed before surgery improve vestibular compensation after surgery [8], exercises designed to rehabilitate patients should be sufficiently challenging to instigate learning processes [9]. Therefore, PA practice before VS surgery could limit the consequences of surgery on balance control, because of the implementation of new sensorimotor and behavioral strategies. This study aimed to examine the effects of a pre-operative PA practice on balance compensatory mechanisms at short, middle and long term in VS patients after surgery. 2. Methods 2.1. Patients
* Corresponding author at: Equilibration et Performance Motrice, UFR STAPS, Nancy Universite´, Universite´ Henri Poincare´, 30 rue du Jardin Botanique, 54600 Villers-le`s-Nancy, France. Tel.: +33 383 683 926; fax: +33 383 683 919. E-mail address:
[email protected] (G.C. Gauchard). 0966-6362/$ – see front matter ß 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.gaitpost.2012.06.011
This study involved 30 consenting patients (median age (Mage) = 51 years, interquartile range (IQR) = 16 years) with unilateral VS who were scheduled for surgical ablation.
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Each participant had clinical otoneurological examination, instrumental audiological and vestibular tests and magnetic resonance imaging (MRI) with gadolinium contrast. Tumors were measured from the pre-operative MRI performed between one to three months before surgery and classified according to Koos in four stages (stage I: size 10 mm confined to the internal auditory meatus; stage II: size 20 mm penetrating the cerebello-pontine angle; stage III: size 30 mm, filling in the cerebello-pontine angle but not compressing the brainstem; stage IV: size >30 mm, compressing the brainstem) [10]. Stage IV tumors have been excluded from this study because of potential brain stem involvement in postural dysfunction. All VS ablations were performed by the same surgeon using the translabyrinthine approach. Both inferior and superior vestibular nerves were resected in all subjects. After surgery, the patients were mobilised as early as possible and all underwent an active post-operative postural training program. The rehabilitation program was composed of different exercises designed to improve balance, mobility and coordination, beginning one day after surgery and ending just before being discharged from the hospital centre, i.e. for 8–10 consecutive days. The first two days consisted in the recovery of verticality, initially sitting posture and then standing posture, with and without ocular fixation. From the third day, balance and gait exercises were introduced, combining ocular fixation or head movements, forward and backward, with direction and speed changes. Eye-head fixation and coordination exercises were introduced in sitting position. From the fifth day, balance and gait exercises were performed in eyes closed condition too, and the eye-head coordination exercises were introduced during gait with random orders. Every patient completed a questionnaire and took part in an interview about his PA which has been defined according to three modalities: leisure sport, professional activities and/ or gardening/do-it yourself. Each patient has given information on the type of PA practiced, the period in the subject’s life when the PA was practiced (age of subject and duration of practice), the frequency (number of times per week) and intensity (number of hours per session). Accordingly, two groups were defined: - Fifteen participants (Group 1, 12 women, Mage = 45 years, IQR = 9 years) were considered as physically active patients. Among them, 14 declared practicing leisure sport (e.g. swimming, rambling, jogging, cycling, fitness, ski, football, Tai Chi or soft gymnastics), 2 working in physically trying conditions (packer, factory worker) and 5 practicing certain tasks in gardening (kitchen garden) or do-it-yourself (masonry, joinery, tiling) at an important activity level. - Fifteen participants (Group 2, nine women, Mage = 50 years, IQR = 8 years) were considered as sedentary patients. Every patient in this group had declared neither practicing leisure sport except walking or working in physically trying conditions. The activity level in gardening/do-it-yourself tasks was too low to be considered as PA.
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2.2. Gaze control evaluation Two tests were performed with videonystagmography (Synapsys, Marseille, France). (i) The bithermal caloric vestibular testing, which evaluates the vestibular sensitivity, showed before surgery three types of patterns: eight patients with an absent response on the side of the affected labyrinth (vestibular areflexy), 16 patients with a decreased response, on the side of the affected labyrinth, of more than 20% (vestibular hyporeflexy) and six patients with a normal symmetrical response (vestibular normoreflexy). In all patients, the contralateral vestibular activity was normal and the visual fixation inhibited the test-related nystagmus [5]. (ii) For the pendular rotary vestibular test (RVT), which reflects the degree of vestibular compensation, the patients were investigated in a rotary chair with eyes open in a dark room, consisting in seven sinusoidal oscillations (frequency: 0.22 Hz; maximal velocity: 308/s; maximal oscillation amplitude: 308). Fourier analyses were performed to calculate both the slow phase eye velocity and the chair velocity. The gain measurements of the VOR were determined by the ratio of the amplitudes of the eye velocity to those of the chair velocity. The directional preponderance measurements were determined by the mean slow phase eye velocity over the duration of the stimulus [5,11]. 2.3. Postural control evaluation During the sensory organization test (SOT, EquiTest1, Neurocom1, Oregon), the patient’s task is to maintain an upright stance, as stable as possible, during three 20 s trials in six conditions that combine three visual conditions with two platform conditions (Table 1). An equilibrium score (ES) was calculated by comparing the subject’s anterior-posterior sway during each 20 s SOT trial to the maximal theoretical sway limits of stability, which is based on the individual’s height and size of the base of support. Lower sways lead to a higher ES, indicating a better balance performance (a score of 100 represents no sway, while 0 indicates sway that exceeds the limits of stability, resulting in a fall). ES were calculated for every condition (C1ES to C6ES). Composite equilibrium score (CES) was calculated to evaluate global balance performances, by adding the average scores from conditions 1 to 2 and the ES from each trial of sensory conditions 3 to 6, and finally dividing that sum by the total number of trials (here 14), that would smooth the data across all conditions [11,12]. 2.4. Procedure Tests were carried out in the Laboratory for the Analysis of Posture, Equilibrium and Movement (LAPEM) of the University Hospital of Nancy (Ministry of Health agreement for research). All patients were submitted to VOR and posturography tests three days before surgery (BS) and three times after surgery, at short term (eight days, AS8), at middle term (90 days, AS90) and at long term (180 days, AS180).
Table 1 Sensory organisation test (EquiTest1, Neurocom1, Clackamas, Oregon, USA): description of the 6 conditions; SR: sway-referenced. Name
Situation
Available cues
Unavailable or perturbed cues
Sensory organisation test Condition 1 (C1) Condition 2 (C2) Condition 3 (C3) Condition 4 (C4) Condition 5 (C5) Condition 6 (C6)
Eyes open, fixed support Eyes closed, fixed support SR surround, fixed support Eyes open, SR support Eyes closed, SR support SR surround, SR support
Vision, vestibular, somatosensory Vestibular, somatosensory Vestibular, somatosensory Vision, vestibular Vestibular Vestibular
– No vision Vision perturbed Somatosensory cue perturbed No vision, somatosensory cue perturbed Vision and somatosensory cue perturbed
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2.5. Statistical analysis The statistics were done using non-parametric tests due to the lack of normality of the distribution and the relatively small sample size in both groups. For the intra-group comparisons between the four evaluation times (BS, AS8, AS90 and AS180), the Friedman (x2, overall heterogeneity) and Wilcoxon (z, pairwise comparisons) tests were used for VOR and SOT parameters. A probability level of p 0.05 was used as an indicator of statistically significant results for overall heterogeneity and Bonferroni procedure was applied to pairwise comparisons by adjusting ‘‘familywise alpha’’ to a significance level of p 0.05/6 = 0.0083 in accordance with the six possible comparisons. For the inter-group comparisons, Mann and Whitney test (z, pairwise comparison) were used for age, anthropometry, VOR and SOT parameters. The Yates corrected x2 or Fisher’s exact tests (distribution comparison, according to tests application conditions) were used for gender, tumor stage and localization and vestibular reflectivity parameters. A probability level of p 0.05 was used as an indicator of statistically significant results for pairwise comparisons. 3. Results For age, gender, height, weight, body mass index, tumor stage and localization, vestibular reflectivity and transient post-operative facial palsy parameters (Table 2), no significant difference was observed between the two groups. For the VOR testing (Fig. 1), results of physically active patients showed an increase in directional preponderance in AS8 compared to BS, and a decrease in AS90 and AS180. For the gain parameter, no significant heterogeneity was observed between the four evaluation times. Results of sedentary patients were similar to those of physically active patients both for directional preponderance and gain. Inter-group comparisons showed that no statistically significant difference was observed whatever the evaluation time for the gain and directional preponderance parameters. For the SOT analysis (Fig. 2), equilibrium scores of sedentary patients seemed to vary more between the four evaluation times than those in physically active patients. Indeed, a high statistical heterogeneity was observed for C5ES, C6ES and CES in both groups and also for C2ES, C3ES and C4ES in sedentary patients. Balance performances of physically active patients were increasing from BS
to AS90 for the main scores with a plateau between AS90 and AS180. Results of sedentary patients were decreasing between BS and AS8 for the main scores and increasing between AS8 and AS180; AS90 performances were midway. Inter-group comparisons showed that performances of physically active patients were better than those of sedentary patients, statistically significant differences or borderline significance being observed for C1ES, C2ES, C4ES, C5ES, C6ES and CES. No statistically significant differences were observed in BS between both groups. 4. Discussion This longitudinal study has shown that patients considered as physically active before surgery presented a different pattern of postural compensation after surgery. In these patients, no deterioration of postural performance was observed just after surgery and an improvement was noted at longer term. In the sedentary patients, postural control modifications followed a more classical time-course, characterised by degradation in postural performances immediately after surgery and a progressive restoration and an improvement of balance performances over time. On the other hand, VOR values were similar between physically active and sedentary patients whatever the evaluation time, showing a dissociation between vestibular and postural compensation. In a classical view of postural control, balance during quiet stance is supported by the use of an inverted pendulum model [13], and its regulation and adaptation to the environment is based on postural tone and on the postural reflexes, which are generated by the vestibular, visual and somatosensory systems and involve higher levels of control [14,15]. When postural situations are more complex, especially during sensory conflicts, the complementarity and the redundancy of the different sensory cues allow the postural system to adjust postural programs to maintain stance [16–18]. As balance control operates as a feedback and feedforward control system [14,19,20], perturbation techniques by sensory conflict could require adaptation and learning mechanisms to adjust balance and, therefore, implicate central structures beyond vestibular nuclei, such as the cerebellum and hippocampus, as during vibratory proprioceptive stimulation [8,9]. The higher the demand on cognitive processes to elaborate postural programs in these complex situations, the higher inter-individual variability is expected in the ability to compensate for sensory
Table 2 Characteristics of the groups constituted by patients considered as active (Group 1) or inactive (Group 2). Intergroup comparisons have been performed with the Mann and Whitney test for the quantitative parameters (expressed in median associated with the interquartile range (IQR)), such as age, height, weight and body mass index (BMI), and with the x2 or Fisher’s exact tests for the qualitative parameters (expressed in number of subject (n0 ) presenting the character), such as gender, tumor stage, vestibular reflectivity of the tumor side and transient post-operative facial palsy. NS = non significant. Group 1, n = 15 median (IQR)/percentage 45.9 (9.5) Age (years) Gender (%) Women 80.0 Men 20.0 Height (m) 1.65 (0.13) Weight (kg) 66.0 (10.5) 2 Body mass index (kg/m ) 24.0 (3.4) Tumor stage (%) Stage 1 6.7 Stage 2 40.0 Stage 3 53.3 Tumor localization (%) Right ear 40.0 Left ear 60.0 Vestibular reflectivity of the tumor side (%) Areflexy 26.7 Hyporeflexy 60.0 Normoreflexy 13.3
Group 2, n = 15 median (IQR)/percentage
Intergroup comparison
50.2 (8.5)
z = 1.4, NS
60.0 40.0 1.63 (0.17) 75.0 (19.5) 24.7 (3.2)
Fisher’s exact p = 0.268
20.0 13.3 66.7
x2 = 3.2, NS
33.3 66.7
x2 = 0.1, NS
26.7 46.6 26.7
x2 = 0.9, NS
z = 0.5, NS z = 1.0, NS z = 1.3, NS
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Physically active patients (PAP) Physically inactive patients (PIP)
Gain
0.75 0.5 0.25 0
BS
AS8
AS90
85
Intragroup comparisons BS vs. AS8 BS vs. AS90 BS vs. AS180 AS8 vs. AS90 AS8 vs. AS180 AS90 vs. AS180
PAP -------------
PIP -------------
Intragroup comparisons BS vs. AS8 BS vs. AS90 BS vs. AS180 AS8 vs. AS90 AS8 vs. AS180 AS90 vs. AS180
PAP ** NS NS * ** NS
PIP * NS NS * * NS
AS180
DP (º/s)
8 6 4 2 0
BS
AS8
AS90
AS180
Fig. 1. Vestibulo-ocular reflex (VOR) test – median values with first and third quartiles of the gain and directional preponderance (DP in8/s) observed just before (BS), eight (AS8), ninety (AS90) and one hundred and eighty (AS180) day after vestibular schwannoma surgery in physically active patients (PAP) (white bars) and physically inactive patient (PIP) (grey bars). Statistics for the intragroup comparisons: NS, non significant; (—), non-calculated; t (trend), p 0.0167; *p 0.0083; **p 0.00167 (after Bonferroni–Dunn correction).
losses [21,22], all the more since vestibular deafferentation results in cognitive impairment [23]. The practice of PA or sports highly implicates these learning mechanisms for specific motor skills in balance regulation at various levels [4,5]. This could explain why postural compensation does not parallel vestibular compensation. This dissociation is all the more important as higher cognitive processes are involved, such as those related to motor learning in PA. For physically active patients, postural performances after surgery remained unchanged in quiet stance or simple sensory conflict situations and are even improved during more complex sensory conflict situations. Surgery did not modify the postural performances at short term, despite the loss of remaining vestibular function. These patients have trained their postural control system more before surgery and the implementation of a compensated vestibular function at a later stage allowed an improvement of postural pattern. They have coped with more difficult tasks, both in terms of pure biodynamics and of feedforward models; they have trained their feed-back during disease, compensating for the vestibular loss prior to surgery. On the other hand, postural performances deteriorated at short term in sedentary patients, especially in challenging sensory situations when vestibular information is the only reliable information for postural regulation, revealing difficulty to solve sensory conflict. Later on, even though postural performances increased, they were still lower than those observed in physically active patients. Therefore, this study seems to show the beneficial effects of a preoperative practice of PA on postural compensation at short and at long term after surgery. At short term after surgery, posturographic evolution was completely different in the two groups of patients, although physical therapy during the first days after surgery was the same for all patients. Physical therapy, especially vestibular exercises, have proven their benefits after surgery on vestibular and postural functions [6,7], but PA of any kind (leisure sporting activities, gardening, do-it-yourself. . .) seems to add post-operative benefits when it is practiced before surgery. PA is protective against the risk of falling and leads to the development of proprioception and a modification of sensory hierarchy allowing a higher contribution of somatokinesthetic information compared to visual information [4,5,24]. A sensory organization favouring visual information to
organize balance control is a negative factor to postural compensation in the acute stage after surgery [3]. This partially explains the posturographic pattern of the sedentary patients, because of their potentially higher dependency on visual information due to sedentary life. On the other hand, as the reweighting of sensory information and increase in the use of both visual and proprioceptive sensory cues is an important part of vestibular compensation [25,26], PA could add its effects on sensory hierarchy to the neural remodeling generated by vestibular compensation; this would favor the use of proprioceptive information for balance control, allowing a better and faster postural compensation. Moreover, PA implies motor learning and, in this way, allows the development of new neural networks, especially in some areas of motor cortex [27], leading to new and more efficient sensorimotor and behavioural strategies. Therefore, whereas these whole mechanisms did not allow a postural gain before surgery in physically active patients, their existence could serve pre-operatively as a support for a more rapid and appropriate implementation of the rehabilitation-related mechanisms just after surgery. Moreover, psychological aspects could be involved. Patients disinclined to be physically active prior to surgery would be even more so after surgery, thus delaying central processes for postural compensation. If patients become dizzy after surgery, generally with spontaneous nystagmus [3], movement causes further dizziness leading to a disinclination to move, even when nystagmus has disappeared [28]. In that respect, mandatory physical therapy is helpful after surgery. On the other hand, at long term, vestibular compensation being organized and similar between the two groups, it seems that a sensory reweighting and an implementation of new neural networks related to PA allowed the development of more efficient postural strategies, especially in the more complex postural situations. However, this increase in performances could also reflect a learning effect to handle the postural testing itself due to consolidation of a short-term memory into a long-lasting memory and the recovery of a vestibular role in orienting and internal references associated with a fine-tuning of body scheme [8]. Nevertheless, to be useful, all balance measuring tools must be scientifically sound in terms of three basic psychometric properties: reliability, responsiveness (sensitivity to change), and
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Physically active patients (PAP) Physically inactive patients (PIP) * *
C1ES (%)
100 90 80 BS BS
AS8 AS8
AS90 AS90
Intragroup comparisons BS vs. AS8 BS vs. AS90 BS vs. AS180 AS8 vs. AS90 AS8 vs. AS180 AS90 vs. AS180
PAP -------------
PIP -------------
Intragroup comparisons BS vs. AS8 BS vs. AS90 BS vs. AS180 AS8 vs. AS90 AS8 vs. AS180 AS90 vs. AS180
PAP -------------
PIP -------------
AS180 AS180
100 *
C2ES (%)
* 90
80 BS
AS8 AS8
AS90 AS90
AS180 AS180
C3ES (%)
100 Intragroup comparisons BS vs. AS8 BS vs. AS90 BS vs. AS180 AS8 vs. AS90 AS8 vs. AS180 AS90 vs. AS180
90
80 BS
AS8 AS8
AS90 AS90
**
**
AS8 AS8
AS90 AS90
AS180 AS180
***
t
AS90 AS90
AS180 AS180
**
***
AS8 AS8
AS90 AS90
AS180 AS180
***
***
**
AS8 AS8
AS90 AS90
AS180 AS180
PAP -------------
PIP NS NS NS NS NS *
AS180 AS180
C4ES (%)
100 90 80 70 BS
C5ES (%)
100 ***
75 50 25 0 BS
AS8 AS8
C6ES (%)
100 ***
75 50 25 0 BS BS
CES (%)
100 75 50 25 0 BS
Intragroup comparisons BS vs. AS8 BS vs. AS90 BS vs. AS180 AS8 vs. AS90 AS8 vs. AS180 AS90 vs. AS180
PAP -------------
PIP NS NS NS * * NS
Intragroup comparisons BS vs. AS8 BS vs. AS90 BS vs. AS180 AS8 vs. AS90 AS8 vs. AS180 AS90 vs. AS180
PAP NS NS t t * NS
PIP * NS NS t * *
Intragroup comparisons BS vs. AS8 BS vs. AS90 BS vs. AS180 AS8 vs. AS90 AS8 vs. AS180 AS90 vs. AS180
PAP NS NS t * * NS
PIP NS NS NS NS t *
Intragroup comparisons BS vs. AS8 BS vs. AS90 BS vs. AS180 AS8 vs. AS90 AS8 vs. AS180 AS90 vs. AS180
PAP NS NS t * * NS
PIP * NS t * * *
Fig. 2. Sensory organization test – median values with first and third quartiles of the equilibrium scores (ES, in %) for the six conditions (C1ES, C2ES, C3ES, C4ES, C5ES and C6ES) and the composite equilibrium score (CES) observed just before (BS), eight (AS8), ninety (AS90) and one hundred and eighty (AS180) day after vestibular schwannoma surgery in physically active patients (PAP) (white bars) and physically inactive patient (PIP) (grey bars). Statistics for the intergroup comparisons: t (trend), p 0.10; *p 0.05; **p 0.01; ***p 0.001. Statistics for the intragroup comparisons: NS, non significant; (—), non-calculated; t (trend), p 0.0167; *p 0.0083 (after Bonferroni–Dunn correction).
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predictive validity [29]. In this respect, most of the equilibrium scores used here present a fair to high test-retest reliability and acceptable responsiveness [30]. Another aspect of this study is the relation between postural and pre-operative vestibular performances. Patients presenting an absence of vestibular function and being physically active might be less affected by surgery in terms of postural control because of less vestibular decompensation. While the effects of the pre-operative vestibular pattern, according to bithermal caloric vestibular testing (normoreflexy, hyporeflexy and areflexy), are already known on the postural compensation after surgery [1], a sub-analysis based on rotary vestibular testing and analysing the degree of vestibular compensation could add further information. A higher number of participants would allow further splitting into subgroups of vestibular function, but our current sample size would only allow underpowered statistics. Nevertheless, this could constitute a field of investigation in future studies. In conclusion, this study showed that patients considered as physically active before surgery presented the best pattern of postural compensation, characterized by the lack of the classical decrease in postural performances just after surgery and the increase in postural performances at a later stage. Physical inactivity made the consequences of surgery more difficult to manage in the acute stage, even though it did not prevent the ability to compensate well later on. In this respect, it can be proposed that pre-operative practice of PA promotes the neuroplasticity of neural networks involved in motor learning which allows to benefit of physical therapy more rapidly and adequately. Conflict of interest statement No conflict of interest. References [1] Parietti-Winkler C, Gauchard GC, Simon C, Perrin PP. Pre-operative vestibular pattern and balance compensation after vestibular schwannoma surgery. Neuroscience 2011;172:285–92. [2] Gouveris H, Akkafa S, Lippold R, Mann W. Influence of nerve of origin and tumor size of vestibular schwannoma on dynamic posturography findings. Acta Oto-laryngologica 2006;126:1281–5. [3] Parietti-Winkler C, Gauchard GC, Simon C, Perrin PP. Visual sensorial preference delays balance control compensation after vestibular schwannoma surgery. Journal of Neurology Neurosurgery and Psychiatry 2008;79:1287–94. [4] Gauchard GC, Chau N, Touron C, Benamghar L, Dehaene D, Perrin PP, et al. Individual characteristics in occupational accidents due to imbalance: a case– control study of the employees of a railway company. Occupational and Environmental Medicine 2003;60:330–5. [5] Gauchard GC, Gangloff P, Jeandel C, Perrin PP. Physical activity improves gaze and posture control in the elderly. Neuroscience Research 2003;45:409–17. [6] Enticott JC, O’leary SJ, Briggs RJ. Effects of vestibulo-ocular reflex exercises on vestibular compensation after vestibular schwannoma surgery. Otology and Neurotology 2005;26:265–9. [7] Herdman SJ, Clendaniel RA, Mattox DE, Holliday MJ, Niparko JK. Vestibular adaptation exercises and recovery: acute stage after acoustic neuroma resection. Otolaryngology Head and Neck Surgery 1995;113:77–87.
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