Posturographic Correlates of Postural Instability in Patients with Idiopathic Parkinson's Disease On and Off Medication

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1 Original Article Posturographic Correlates of Postural Instability in Patients with Idiopathic Parkinson's Disease On and Off Medication Gihan Abd-Ellatief Younis El-Tantawi 1, Ghada Abd-Elhadi Osman Achmawi 2 Departments of Physical Medicine, Rheumatology & Rehabilitation 1, Neurology 2, Alexandria University; Egypt ABSTRACT Background: Researches characterizing postural instability in idiopathic Parkinson's disease (IPD) provides insights into the possibly disturbed mechanisms for postural control. There is however paucity of researches that are interested in providing multisystem evaluation for detection of possible contribution of different systems to balance disturbance in IPD patients. Objective: To study posturographic correlates of postural instability in IPD off and on antiparkinsonian medication to determine the exact pathophysiologic mechanisms underlying their balance problems. Methods: Fifteen IPD patients (on and off state) were compared to ten healthy control subjects. Patients underwent clinical examination including Unified Parkinson Disease Rating Scale (UPDRS) and Hoehn Yahr Scale together with posturographic evaluation including sensory organization test, motor control test, and neurotesting (akinesia test, retropulsion test, and bradykinesia test). The posturographic parameters were compared to those of control group. Results: Compared to controls, IPD patients "off state" had significantly low composite equilibrium score and significantly low visual ratio and visual preference ratio of the sensory organization test. Elevated automatic postural thresholds were detected only to medium sized forward translation during motor control test. Significantly prolonged reaction and movement times together with defective pacing characterized patients movement during neurotesting. Partial improvement was found in all clinical subscales and in some of posturographic parameters in response to antiparkinsonian medication. Conclusion: Both sensory and motor components of balance are important contributors to postural instability in IPD. Visual dysfunction dominated sensory abnormality. Motor abnormalities contributing to postural disturbance may be the result of increased rigidity, defective timing components of balance, and defective force generation. (Egypt J Neurol Psychiat Neurosurg. 2010; 47(1): ) Key Words: Parkinson's disease, posturography, antiparkinsonian medications INTRODUCTION Maintaining balance is critical for movement execution and more especially locomotion. 1 Balance or postural stability, is a complicated process, which demands coordination of the sensory, motor, and central nervous systems. 2 Our understanding of the basis of instability comes from researches examining postural control in patients with specific neurological lesions such as Parkinson's disease. 2 Postural instability is a hallmark of Parkinson's disease and represents an incapacitating symptom. 3 Researches characterizing postural instability in IPD are providing insights into the possibly disturbed mechanisms for postural control in IPD. 4 There is however paucity of researches that are interested in providing multisystem evaluation for detection of possible contribution of different systems to balance disturbance in patients with IPD. 5-7 Correspondence to Ghada Achmawi, Department of neurology, Alexandria University, Egypt Tel: dr.ghadaabdelhadi@yahoo.com. The influence of antiparkinsonian treatment on balance control is additional point of concern and results were found to be controversial. 1,8-10 This study is carried out to assess posturographic correlates of postural instability in patients with IPD off and on antiparkinsonian medication to determine pathophysiologic mechanism(s) underlying their balance impairment. PATIENTS AND METHODS Fifteen patients with IPD (9 men and 6 women) were recruited from the Movement Disorders Clinic, Neurology Department, Faculty of Medicine. Ten healthy age- and sex-matched individuals were included as a control group. Mean age of patients was 61.79±2.9 years, that of controls was 60.2±2.7 years with no significant difference between both groups (P=0.4). Mean disease duration was 6.3±2.4 years. The diagnosis of IPD was made on the basis of the UK brain bank criteria for IPD. 11 Patients were excluded if evidence was found of other pathologies that might affect postural control. All patients were receiving carbidopa (25 mg)/l-dopa (250 mg) at 750- Egypt J Neurol Psychiat Neurosurg. Jan 2010 Vol 47 Issue 1 185

2 1000 mg/day orally. Patients were assessed clinically and posturographically twice (on and off antiparkinsonian medication). On state evaluation was carried out in the best clinical condition, about one hour after intake of antiparkinsonian medication. Drugs were withdrawn 12 hours in advance of the off state testing to allow sufficient time for the effects of medications to wear off and not affect the off-medication analysis. Clinical assessment of postural instability was determined by postural subcomponents of Unified Parkinson s Disease Rating Scale (UPDRS) 12 including item 22 (leg rigidity), item 28 (posture), item 29 (gait), and item 30 (postural stability). The degree of disease severity was determined by the Hoehn Yahr Staging. 13 Posturographic evaluation was carried out in the Department of Physical Medicine, Rheumatology, and Rehabilitation using computerized dynamic posturography Equitest system TM ; Neurocom International, Inc. Portland, OR. USA. Test prerequisites included the ability to stand erect independently with eyes open for a period of at least one minute. 14 Table (1) illustrates descriptions of posturographic tests and measures. 1- Sensory organization test (SOT) 14 (Table 1): Sensory organization test (SOT) evaluates the ability to make effective use of visual, vestibular, and somatosensory inputs to maintain balance. Patients were harnessed to prevent falls. The SOT protocol consists of 6 experimental conditions as described in Table1. The complete protocol consists of three trials for each of the six conditions, a total of 18 trials. Each trial lasts for 20 seconds. The patient under test was instructed to remain upright and as steady as possible during each trial. The equilibrium score for each sensory condition was calculated and the average of 3 trials for each condition was used in data analysis. The composite equilibrium score representing the overall level of performance on the SOT was calculated. In addition, sensory ratios (Somatosensory; SOM, visual; VIS, vestibular; VEST, and visual preference ratio; VIS PREF) were calculated to determine the specific nature of a patient's sensory balance problem. 2- Motor control test (MCT) 14,15 (Table 1): The test assesses the active forces exerted to regain balance following an unexpected external disturbance (horizontal translations of the force platform). The translations were delivered in 3 increasing intensities (small, medium, and large) in both directions (anteriorly and posteriorly). The latency (msec) and the response strength (degree/sec) of the active forces were measured. 3- Neurotesting: Variables obtained from neurotesting reflect timing components of balance. a- Akinesia test 15 (Table 1): This test evaluates the time to initiate a movement to a target (reaction time) and the time to move to the target (movement time).the screen in front of the patient is to be turned on. Patients were asked to center their center of gravity (COG) in a white circle seen on the screen until a target located outside the circle appears. When it appears, the patient had to shift his/her weight as quickly as possible to the target. There were 8 targets per test and the test was run three times. If the patient did not reach a target, no score was given and a missed target was considered. b. Bradykinesia and retropulsion tests 15 (Table 1): Bradykinesia and retropulsion tests evaluate the ability to make voluntary movements at a specific speed. As the bradykinesia test started, the screen was turned on and a sliding bar that moved from side to side between two vertical bars was shown on the screen. The sliding bar moves at 3 different paces: slow (3s), medium (2s), and fast (1s) paces and patients were instructed to have their COG keep pace with the moving bar at the pace indicated. The procedures of retropulsion test were the same as for the bradykinesia test, however, the sliding bar was moving forward and backward between two transverse bars. Measurements included the length of time it takes the patients to go between bars and the distance in degrees that the patient moved the COG between the two end-points. Statistical analysis: The statistical Package of Social Science (SPSS version 9.0) software was used to analyze the obtained data. Descriptive data was expressed as mean ± standard deviation. The independent samples t-test was used to assess the differences between posturographic scores of patients and those of controls. The paired samples t-test was used to assess differences in the mean of posturographic scores off and on medication. For nonparametric data (clinical scores), McNemar test was used to determine the significance of the treatment on the measured parameters. Spearman's rank correlation test was used to assess the relationship between posturographic parameters and clinical scores while off medications. 186 Egypt J Neurol Psychiat Neurosurg. Jan 2010 Vol 47 Issue 1

3 Table 1. Abbreviations and Description of posturographic tests and measures Expansion Sensory organization test (SOT): sensory condition 1 (C1) sensory condition 2 (C2) sensory condition 3 (C3) sensory condition 4 (C4) sensory condition 5 (C5) sensory condition 6 (C6) composite equilibrium score (Comp) Somatosensory ratio (SOM) visual ratio (VIS) vestibular ratio (VEST) visual preference ratio (VIS PREF) Motor control test (MCT): response latency response strength Neurotesting: Akinesia test reaction time (RT) movement time (MT) total path length Bradykinesia and retropulsion tests COG: center of gravity Description Evaluates the ability to make effective use of visual, vestibular, and somatosensory inputs separately and to suppress sensory information that is inappropriate Eyes open and fixed platform, normal standing Eyes closed and fixed platform, somatosensory input is the dominant input to balance Eyes open and visual sway, inaccurate (conflicting) visual input is delivered to the patient in the presence of somatosensory input Eyes open and platform sway, visual input is the dominant sensory input Eyes closed and platform sway, vestibular input is the dominant sensory input Eyes open and platform and visual sway, inaccurate (conflicting) visual input is delivered to the patient in absence of somatosensory input Represents the overall level of performance on the SOT C2/C1, represents somatosensory contribution to postural control C4/C1 represents visual contribution to postural control C5/C1, represents vestibular contribution to postural control C3+6/C2+5, represents the ability to rely on vision, even if inadequate Assesses the ability of the automatic motor system to quickly recover following an unexpected external disturbance Reflects the time to initiate the active force response Reflects the ability to produce a level of force appropriate for the degree to which the patient has been displayed for each translation. Reflects motor control and timing components of balance Evaluates the time to initiate a voluntary movement to a target and the time to move to the target The time from when the target first appears on the screen until the patient starts to move toward it The time from when the target appeared until the target is achieved minus RT Represents the length of the patient's COG trace from the time the target appeared until it was achieved or the trial was ended Evaluate the ability to make voluntary movements at a specific speed and the ability to maintain the prescribed speed RESULTS Clinical assessment: Clinical postural subcomponent scores of UPDRS and Hoehn Yahr Staging were abnormal in all patients both on and off states with significant improvement of all postural subcomponents "on state" (Table 2). Posturographic testing: a) Sensory organization test: Patients off medication had significantly low composite equilibrium score and significantly low scores under C4, C6, VIS, and VIS PREF (P<0.001) compared to controls (Table 3 and Figure 1a). Seven patients fell under C6, (Figure. 1a). The type of falls was identified as being free falls as they were not preceded by attempted corrections. On treatment, the composite equilibrium score and the mean scores of C4, VIS, and VIS PREF (71.4±7.7, 77.33±5.3, 0.82±0.04, 0.93±0.2 respectively) were significantly improved (P=0.05, P=0.038, P=0.035, P=0.034 respectively). b) Motor control test: There were significantly delayed response latency and significantly increased response strength scores (excessive force generation) for medium sized forward translation for both sides in patients "off state" compared to control group. (Table 4, Figure 1 b). On medications, response strength scores were significantly improved (decreased) for right (3.57±0.76, P=0.000) and left (4±0.55, P=0.001) sides to a level approaching that of control group (P=0.85, P=0.23 respectively) with no improvement as regards response latency scores for both right (130±6.79, P=0.13) and left sides (128.57±5.35, P=0.13). c) Neurotesting analysis: - Akinesia test: Times to initiate and execute movement (RT and MT) were significantly prolonged Egypt J Neurol Psychiat Neurosurg. Jan 2010 Vol 47 Issue 1 187

4 in patients "off state" compared to control group (P<0.001). Moreover, patients failed to reach many targets with significant increase in the number of missed targets as compared to controls (P<0.001) (Table 3, Figure 1c). On treatment, MT (4.29±1.01s) was significantly improved (decreased) (P<0.001), however, still greater than values for controls (P<0.001) with no improvement regarding other parameters. - Bradykinesia and retropulsion tests: Patient's movement off state was significantly slower than the control group at medium (2s) and fast (1s) paced speed (more challenging conditions) and the distances they moved were significantly less at all paced speeds for both tests (Table 3, Figures 1d and 1e). On treatment, the speed of movement was significantly improved at 2s paced speed during bradykinesia test (2.02±0.06, P=0.028) but to a level below that for control group (P=0.006). Distances moved were increased at all paced speeds but not to a significant level. During retropulsion test, distances moved were significantly increased at 3s, 2s, and 1s paced speeds (4.35±1.1, P=0.000; 4.21±1.48, P=0.001; 3.65±1.11, P=0.000 respectively) but to levels below that of control group (P=0.002, P=0.000, P=0.000 respectively) with no improvement as regards patients speed at all paced speeds. Correlation analysis: In off-medication state, rigidity and postural stability subcomponents of the UPDRS were the two clinical parameters found to correlate significantly with posturographic parameters (Table 5). MT measured during akinesia test was found to correlate positively with gait scores as well. Poor correlation was found between clinical scores and SOT parameters. In addition, Hoehn Yahr Staging was found to correlate poorly with posturographic parameters. Table 2: Distribution of patients according to UPDRS Scoring and Hoehn Yahr staging on and off antiparkinsonian medication. Variable Number of patients in various postural subcomponents of UPDRS P value Rigidity: Posture: Gait: Off state * On state 15 Off state * On state 7 8 Off state ** On state 15 Postural stability: Off state * On state 12 3 Number of patients in various Hoehn Yahr Staging Hoehn Yahr Staging: Off state * On state 12 3 UPDRS: Unified Parkinson Disease Rating Scale P is significant if 0.05 * Statistically significant. ** Highly significant 188 Egypt J Neurol Psychiat Neurosurg. Jan 2010 Vol 47 Issue 1

5 Table 3. SOT and Neurotesting scores in IPD patients (off medication) and controls. Variable IPD patients (off medications) (n=15) Control group (n=10) t-test 95% CI lower/upper P-value Sensory Organization test: Sensory condition: C1 93 ± ± / C ± ± / C3 89 ± ± / C ± ± / * C ± ± / C ± ± / * Comp 66.9 ± ± / * Sensory ratio: SOM.97 ± ± / VIS.76 ± ± / ** VEST.67 ± ± / VIS PREF.77 ± ± / ** Neurotesting: Akinesia test: - Reaction time (s) 2.1 ± ± / * - Movement. Time (s) 5.9 ± ± / * - Number of missed targets 2.79 ± ± / ** - Path length (degree) 8.4 ± ± / * Bradykinesia test: -Time length (s) to go between bars at: slow (3s) pace 2.9 ± ± / medium (2s) pace 1.93 ± ± / * fast (1s) pace 1.12 ± ± / Distance travelled (degree): slow (3s) pace 6.22 ± ± / * medium (2s) pace 5.79 ± ± / ** fast (1s) pace 4.01 ± ± / ** Retropulsion test: - Time length (s) to go between bars at: slow (3s) pace 2.9 ± ± / medium (2s) pace 2.14 ± ± / * fast (1s) pace 1.17 ±.15 1 ± /.2.033* -Distance travelled (degree): slow (3s) pace 2.9 ± ± / ** medium (2s) pace 3.04 ± ± / ** fast (1s) pace 1.81 ± ± / ** P is significant if *Statistically significant. ** Highly significant SOT: sensory organization test IPD: idiopathic Parkinson's disease C: condition Comp: composite equilibrium score SOM: Somatosensory ratio VIS: Visual ratio VEST: Vestibular ratio VIS PREF: Visual preference ratio s: second *Statistically significant. ** Highly significant Egypt J Neurol Psychiat Neurosurg. Jan 2010 Vol 47 Issue 1 189

6 Table 4. Response latency and response strength scores of MCT in IPD patients off medication and controls. Variable IPD patients (off medication) (n=15) Control group (n=10) t. test P value IPD patients (off medication) (n=15) Control group (n=10) t. test P-value Right leg Left leg Response Latency (msec): Backward translation: Medium-sized translation 113± ± ± Large-sized translation 131.2± ± ± ± Forward translation: Medium-sized translation 135.1± ± * 134± ± * Large-sized translation 130.6± ± ± ± Response strength: (degree/sec): Backward translation: Medium-sized translation 3.2± ± ± ± Large-sized translation 4.3± ± ± ± Forward translation: Medium-sized translation 5.19± ± * 5.41± ± * Large-sized translation 5.31± ± ± ± P is significant if *Statistically significant. ** Highly significant MCT: motor control test IPD: idiopathic Parkinson's disease ms: millisecond s: second 190 Egypt J Neurol Psychiat Neurosurg. Jan 2010 Vol 47 Issue 1

7 A B C D E Figure 1. Posturographic data analysis showing: significantly reduced composite equilibrium score scores with reduced scores under C4, C6, VIS, and VIS PREF during SOT (a), significantly increased response strength score (º/sec) to medium-sized forward translation during MCT (b), significantly increased path length with inability to reach many targets during akinesia test (c), and significantly reduced distances moved during retropulsion (d) and bradykinesia (e) tests in IPD patient off state compared to one control subject. Egypt J Neurol Psychiat Neurosurg. Jan 2010 Vol 47 Issue 1 191

8 Table 5. Correlations between clinical scores and posturographic parameters in the IPD patients off medication. Sensory organization test: Variables Unified Parkinson s Disease Rating Scale Hoehn Yahr Staging Rigidity Gait Postural stability rho P rho P rho P rho P Comp SOM VIS VEST VES PREF Motor control test: Medium-sized forward translation: Response latency: right leg ** ** ** left leg * * * Response strength: right leg * * * left leg * * * Neurotesting: Akinesia test: Reaction time Movement time ** * ** ** Number of missed targets * * * Distance traveled (path length) * * * Bradykinesia test: The length of time to go between transverse bars: at 3s paced speed at 2s paced speed at 1s paced speed Distance traveled: at 3s paced speed at 2s paced speed at 1s paced speed * * * * Retropulsion test: The length of time to go between transverse bars: at 3s paced speed at 2s paced speed ** ** at 1s paced speed Distance traveled: at 3s paced speed * * at 2s paced speed ** ** at 1s paced speed Only data of statistical significance are presented) ** Correlation is significant at the 0.01 level (2-tailed) * Correlation is significant at the 0.05 level (2-tailed) IPD: idiopathic Parkinson's disease Comp: composite equilibrium score SOM: somatosensory ratio VIS: visual ratio VEST: vestibular ratio VIS PREF: visual preference ratio 192 Egypt J Neurol Psychiat Neurosurg. Jan 2010 Vol 47 Issue 1

9 DISCUSSION The basal ganglia are part of motor central nervous system for control of movements and posture. 17 More recently, the sensory role of basal ganglia has been documented and the basal ganglia is now considered critical for integration of sensory information for postural control. 18 In this study, the sensory and motor components (both the automatic and voluntary aspects) of balance were assessed in patients with IPD. Impaired sensory organization In the present work, IPD patients had impaired sensory organization as shown by significantly low composite equilibrium score. The sensory balance problem was related to disturbed visual senses of balance and to inability to suppress visual input when inaccurate i.e. visual dependence. The involvement of the visual pathway but not the vestibular and/or the somatosensory pathways in the present study needs an explanation. Vision is known to play a direct and important role in stabilizing balance. 19 Dopamine was found to be an important neurotransmitter in the visual pathway. 20 Reduction in the level of dopamine in the retina, the lateral geniculate nucleus, and the visual cortex has been documented in PD 21 with subsequent impairment of retinal processing, spatial working visual memory, 22 and cortical visual processing. In the present work, dopamine depletion in the retina and/or visual cortex may be responsible for visual dysfunction and can be of functional impact on postural stability of the studied patients who may experience unsteadiness by irregular moving support surfaces or in environments containing many moving stimuli. 14 Actually, we had 7 patients who fell under C6. None of these falls was preceded by attempted corrections (free-falls). Free falls are known to be associated with the most severe forms of sensory dysfunction and indicate that patients are making little if any use of the information from the involved sensory system. 16 The presence of poor correlation between clinical scores and scores of SOT conditions and ratios is expected given that UPDRS scores and Hoehn Yahr Staging reflect motor aspects, whereas the SOT equilibrium scores reflect the sensory organizational process of postural control. Impaired automatic postural mechanisms In the present study, the integrity of the automatic motor system was assessed by measurement of the force generated to regain balance during MCT. Abnormalities included significantly delayed response latency and significantly increased response strength scores (excessive force generation) to medium-sized forward translation for both sides in patients "off state". Excessive force can contribute to balance impairment, where patients tend to over shoot the centered position and may oscillate. 16 A likely cause of MCT abnormalities is a lesion along the efferent branch of long loop pathway to flexor muscles. 14 In patients with PD, tonic hyperactivity (rigidity) of flexor muscles is characteristic and the contribution of axial rigidity to functional impairments of posture and locomotion in PD was shown by Wright and colleagues. 23 Abnormal forward alignment (stooping) may also be implicated and the influence of stooping on postural responses in normal and PD patients has been investigated and stooped posture was found to be a destabilizing posture. 24,25 Impaired motor control and timing components of balance Variables obtained from neurotesting reflect voluntary motor control and timing components of balance. 23 The results of akinesia test showed significant prolongation of RT reflecting movement initiation and MT reflecting movement execution in IPD patients off medication. Moreover, patients failed to reach many targets. Defective movement execution was also shown during bradykinesia and retropulsion tests where patients movements were slower than the control group and the distances they moved were less. Such findings are consistent with the fact that defective initiation of movement and slowed movement execution (bradykinesia) are principle deficits in IPD patients 26 who were found to react more slowly than healthy subjects in preparing expected responses 27,28 as well as executing simple, 29 complex, 30 and sequential rapid movements. 31 The presence of positive correlation between the rigidity score and movement time points to the possibility that, rigidity may contribute to postural instability in IPD by potentially contributing to bradykinesia. The effect of antiparkinsonian medications Patients' performance, both clinically and posturographically, was better in response to antiparkinsonian treatment. Improvement involved some but not all measured aspects of posture. This improvement was partial in some of the improved measures and complete in some of them. The composite equilibrium score was significantly improved over that "off state" with significant improvement of equilibrium scores of C4 and visual ratio, however, improvement was partial not reaching values of control group. Visual preference ratio significantly improved with values approaching those of control group. Given that, visual Egypt J Neurol Psychiat Neurosurg. Jan 2010 Vol 47 Issue 1 193

10 dysfunction was dominating, improvement in theses scores in response to dopaminergic drugs may be related to replacement of deficient dopamine in the retina and/or visual cortex which was reflected on patients' performance during the relevant sensory conditions of SOT. During MCT, response strength scores for medium-sized forward translation were partially improved. This may be related to significantly decreased rigidity and stooping. Partial improvement during MCT helps providing more stability in face of destabilizing perturbing conditions. Considering the results of neurotesting and their correlation with clinical scores, it could be suggested that, improved postural performance of patients in response to treatment is probably the result of reduction in rigidity and bradykinesia (motor component of posture). This finding comes in agreement with the result of other researchers who found that postural stability of PD patients is improved by decreasing rigidity 32 and bradykinesia. 23 This reduction in rigidity and bradykinesia should improve postural adjustments by increasing joint flexibility and reducing RT required for appropriate postural responses. 8 In view of the present findings, postural instability in PD is multifactorial. Understanding and identifying the underlying mechanism(s) of postural instability in patients with PD and their response to treatment will help focusing interventions to their specific problem(s) and will enhance the ability to effectively treat such patients. Interventions can be directed to improve disturbed visual function, 16,33,34 to modify postural responses and improve rate of force development, 33 and lastly to reduce bradykinesia. 35 Conclusion Both sensory and motor abnormalities are important contributors to postural instability in patients with IPD. Visual dysfunction dominated sensory abnormalities. Motor abnormalities contributing to postural disturbance may be the result of increasing rigidity, defective timing components of balance, and defective force generation. Improvement in response to antiparkinsonian medication was either partial or complete and involved some but not all measured aspects of postural control. REFERENCES 1. Bronte-Stewart HM, Yuriko Minn AY, Rodrigues K, Buckley EL, Nashner LM. Postural instability in idiopathic Parkinson's disease: the role of medication and unilateral pallidotomy. Brain. 2002; 125 (9): Shumway-cook A, Woollacott MH. Motor control. Theory and clinical applications. 2nd edition. Philadelphia, Baltimore, New York, London, Buenos Aires, Hong Kong, Sydney, Tokyo: Lippincott Williams & Wilkins; Louis ED, Tang MX, Alfaro BC, Mejia H, Marder K. Progression of Parkinsonian Signs in Parkinson Disease. Arch Neurol. 1999; 56: Brown P, Steiger M. Basal ganglia and gait disorders. In: Bronstein AM, Woollacott M, editors. Balance, posture, and gait. London: Arnold; 1996 p Roberts-Warrior D, Overby A, Jankovic J, Olson S, Lai EC, Krauss JK, et al. Postural control in Parkinson s disease after unilateral posteroventral pallidotomy. Brain. 2000; 123 (10): Toole T, Park S, Hirsch MA, Lehman DA, Maitland CG. The multicomponent nature of equilibrium in persons with Parkinsonism: a regression approach. J Neurol Transm Gen Sect. 1996; 103: Colnat-Coulbois S, Gauchard GC, Maillard L, Barroche G, Vespignani H, Auque J, et al. Bilateral subthalamic nucleus stimulation improves balance control in Parkinson's disease. J Neurol Neurosurg Psychiatry. 2005; 76: Bejjani BP, Gervais D, Arnulf I, Papadopoulos S, Demeret S, Bonnet A-M, et al. Axial parkinsonian symptoms can be improved: the role of levodopa and bilateral subthalamic stimulation. J Neurol Neurosurg Psychiatry. 2000; 68: Burn DJ. The effect of deep brain stimulation and levodopa on postural sway in subjects with Parkinson s disease. J Neurol Neurosurg Psychiat. 2002; 73 (3): Rocchi L, Chiari L, Horak FB. Effects of deep brain stimulation and levodopa on postural sway in Parkinson s disease. J Neurol Neurosurg Psychiat 2002; 73 (3): Gibb WR, Lees AJ. The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson s disease. J Neurol Neurosurg Psychiat. 1988; 51: Fahn S, Elton RL, UPDRS Development Committee. Unified Parkinson s Disease Rating Scale. In: Fahn S, Marsden CD, Calne DB, Goldstein M, editors. Recent Developments in Parkinson s Disease. Florham Park, NJ: Macmillan; p Hoehn MM, Yahr MD. Parkinsonism: onset, progression and mortality. Neurology 1967; 17 (5): Nashner LM. Posturographic testing: the handbook of balance functions testing, Jacobson GP, Newman CW, Kartush JM, editors. St Louis, Baltimore, Boston: Mosby-year book Inc.; p Nashner LM: EquiTest system operator's manual, version Clackamas, OR: NeuroCom International, Inc.; Nashner LM. Equitest System.Version 4.0. Data interpretation manual. Neurocom International Inc.; Egypt J Neurol Psychiat Neurosurg. Jan 2010 Vol 47 Issue 1

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12 عالقة تخطيط القوام بعدم استقرار الملخص العربى القوام فى مرض باركنيسون ذاتى العلة مع تقطع العالج 196 Egypt J Neurol Psychiat Neurosurg. Jan 2010 Vol 47 Issue 1