Movement Disorders Vol. 17, No. 4, 2002, pp.

663669 2002 Movement Disorder Society

Analysis of Sway in Parkinsons Disease Using a New Inclinometry-Based Method

Maria K. Viitasalo, MD,1 Ville Kampman,2 Kyo sti A. Sotaniemi, MD,1 Seppo Leppa vuori, TD,2 1 1 Vilho V. Myllyla , MD, and Juha T. Korpelainen, MD *
2 1 Department of Neurology, University of Oulu, Oulu, Finland Department of Laboratory of Microelectronics, University of Oulu, Oulu, Finland

Abstract: In order to analyze balance control, we developed a new inclinometry-based method to provide direct information about body sway in the side-to-side and forwardbackward directions. We tested the clinical utility of this method for analyzing balance in Parkinsons disease (PD), and studied the clinical correlates of the balance measures in PD. Postural sway was measured during quiet stance with eyes open and eyes closed in 28 PD patients and in 32 age- and sex-matched control subjects. Postural sway was modeled using side-to-side and forwardbackward directional sway movements, sway velocity, and sway area. The amount of postural sway in the PD patients was greater than in the control subjects, the higher level being most marked in patients with severe or long-

duration PD. All the side-to-side directional sway parameters were abnormal in the PD patients compared with the control subjects (P < 0.05), whereas the forwardbackward directional parameters did not differentiate the two groups. The most sensitive measures of sway were path length, velocity, and area. The duration and severity of PD seem to be particularly associated with the amount of side-to-side directional postural sway. This new inclinometric method appears to be useful in quantifying postural sway and evaluating balance impairment in PD. 2002 Movement Disorder Society Key words: postural sway; balance impairment; Parkinsons disease

Because of degeneration of dopaminergic nigrostriatal projections and other motor control centers, parkinsonian patients suffer from postural instability, stooped posture, and gait difficulties. Impairment of balance is an important feature of Parkinsons disease (PD), often leading to falls and injuries. It has recently been shown that PD patients have an increased risk of death strongly related to the presence of gait disturbances.1 Because postural instability is associated with advanced stages of PD with diminished functional ability and poor prognosis,2 an accurate method for analyzing balance is needed. In the clinical setting, balance evaluation in PD has mainly been based on bedside tests such as the patients ability to recover equilibrium when knocked off balance by pulling suddenly backwards on the shoulders, or fall*Correspondence to: Juha T. Korpelainen, Department of Neurology, University of Oulu, PO Box 5000, 90014 Oulun yliopisto, Finland. E-mail: juha.korpelainen@ppshp.fi Received 16 March 2001; Revised 17 July 2001; Accepted 25 July 2001 Published online 7 January 2002 in Wiley InterScience (www. interscience.wiley.com). DOI 10.1002/mds.10023

ing frequency, gait difficulties, and the need for postural support. However, these kinds of tests are inaccurate and their sensitivity and reliability is limited. In the laboratory, the amount of postural sway reflecting balance disorders in PD has previously been assessed indirectly by recording ground reaction forces as a subject stands on a platform equipped with force transducers. 37 This method has been used to evaluate postural stability under varying sensory conditions810 and to investigate postural reflexes.37,10 Movements of the center of gravity have also been measured with a platform-mounted potentiometer attached to the body.4,5,11 Other motion measuring instruments, for example infrared emitting diodes,12,13 have also been used for balance measurements in PD. However, all of these methods have severe limitations when quantifying balance disorders in a clinical setting. We developed an inclinometry-based method to provide direct information about body sway in the side-toside and forwardbackward directions. We tested the clinical utility of this method of recognizing balance im-

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TABLE 2. Concomitant diseases of Parkinsons disease patients and control subjects
Disease Cardiovascular disease Asthma Noninsulin-dependent diabetes mellitus Hypothyreosis Musculoskeletal disease Patients (n 28) 12 2 1 2 7 Controls (n 32) 12 6 0 4 6

pairment, assessed postural instability in PD by comparing the amount of sway of PD patients with that of healthy controls, and evaluated the clinical correlates of balance impairment in PD. SUBJECTS AND METHODS Subjects The protocol was approved by the Ethics Committee of the local Medical Faculty, and informed consent was obtained from each subject. Twenty-eight patients with PD (14 men and 14 women) and 32 age- and sexmatched control subjects participated in the study (Table 1). The severity of PD was evaluated by the Hoehn and Yahr stage14 and by the motor subscale of the Unified Parkinsons Disease Rating Scale (UPDRS).15 For further analyses, the patients were divided into subgroups according to their motor scores on the UPDRS subscale: Group 1, <10 (n7); Group 2, 1025 (n13); and Group 3, > 25 (n8). Subjects were further divided into two subgroups according to the duration of the disease: (1) 5 years or less (n18); (2) more than 5 years (n 10). The mean age of the patients of the subgroups and that of the controls was similar. All the PD patients were clinically examined and their postural sway was measured during the on-period at the moment when dyskinesia was not present. All the PD patients were on levodopa medication. Levodopa was used as a monotherapy in five cases and in combination with a dopamine agonist in 10 patients, with entacapone in 19 and with selegiline in eight. Twelve patients had a concomitant cardiovascular disease, either arterial hypertension or coronary heart disease. Seven patients had a musculoskeletal disease, two bronchial asthma, one noninsulin-dependent diabetes mellitus, and two had hypothyreosis (Table 2). Three of the patients used nitrates, three diuretics, six beta blockers, one a calcium channel blocker, two acetylsalicylic acid, one dipyridamole, one thyroxine, one benzodiazepine, one zopiclone, one hydroxyzine, and two had medication for bronchial asthma.
TABLE 1. Clinical characteristics of Parkinsons disease patients and control subjects
Characteristics Gender (M/F) Mean age, yr (range) Mean duration of PD, yr (range) Mean Hoehn and Yahr stage (S.D.) Mean UPDRS motor score (S.D.) Motor fluctuations or dyskinesias Patients (n 28) 14/14 64.9 (5083) 7.1 (217) 2.4 (0.8) 18.2 (10.1) 14 Controls (n 32) 16/16 63.1 (4677)

The control group consisted of 32 sex- and agematched subjects, who were spouses or acquaintances of the patients. Twelve had cardiovascular diseases, either arterial hypertension or coronary heart disease, and one had chronic atrial fibrillation. Six had musculoskeletal diseases, six had bronchial asthma, and four had hypothyreosis. One used nitrates, one digoxin, two diuretics, five beta blockers, one a calcium channel blocker, one an angiotensin converting enzyme inhibitor, four acetylsalicylic acid, one dipyridamole, one warfarin, four thyroxine, one benzodiazepine, one amitriptyline, and five medication for bronchial asthma. None of the control subjects had any difficulty in standing without support during the measurements. Methods Postural sway measurements were performed under standardized conditions. Every test was visually controlled by the same investigator. The measurements were taken during normal standing both with eyes open and eyes closed and they were repeated once. Each recording lasted 60 seconds. The mean value of the two consecutive recordings was used in the analysis. During the test, the subjects stood at attention, without shoes, with their feet together and arms beside the body. In the eyes-open test, subjects were asked to look straight ahead at a mark on the facing wall. The inclinometric device consisted of a belt fastened firmly at the level of the iliac crist, an inflexible measuring rod, an inclinometric module, a joint structure lying on the ground, a power unit, and a personal computer. The measuring rod transmitted movements of the body to the detecting inclinometric module located on its the lower end (Fig. 1). The bottom end of the rod was attached to a joint structure that was designed to avoid both the rod and the sensor module rotating around the longitudinal axis during the measurement. The height of the measuring rod was adjusted according to the height of the subject. The deviating movement (D) of the measuring rod was calculated separately for the side-to-side (x) and forwardbackward (y) directions using the equation Dx,y=tanx,y x h, where x,y is the measured inclination in the x or y direction, and h the selected calculation

UPDRS, Unified Parkinsons Disease Rating Scale.

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FIG. 1. A subjects waistline movement during standardized stance was analyzed using a belt, a measuring rod, and a two-axis inclinomentric sensor. The movement of the rod (Dx,y) was calculated using a constant height (h 80 cm) for all the subjects independent of the height of the belt.

height (Fig. 1). By combining these two calculated deflections (Dx,y), the movement of the rod was presented as an x-y coordinate. A two-axis electrolytic liquid-based inclinometric module including signal conditioning was used as a detecting sensor. The module had two output voltages proportional to the x- and y-axis inclination of the measuring rod. These two voltages were converted to digital data using two 12-bit analog to digital (A/D)-converters. The A/D-conversion frequency of both channels was 20 Hz. The converted data was filtered using an 8-order low-pass digital filter (cut frequency 3 Hz) to avoid highfrequency noise. Digital data were calculated for the

sway parameters and displayed between every A/Dconversion to provide a real-time display. A constant calculation height (h 0.8 m) was used for analyzing the sway parameters of all the subjects. By using this constant value h, any possible effect of the different heights of the subjects on the results was eliminated. Thus, all the calculated sway parameters represented the measuring rod movements on the horizontal plane at the height of 0.8 m. The measurement resolution of the inclinometric module was 0.006 degrees, and the repeatability was less than 0.02 degrees. Thus, the measurement repeatability of the rod movement at the 0.8-m level, for example, was less than 0.4 mm ([tan 0.03] 800 mm). The response time of the module to inclination change (1090%) was 40 ms. The recorded sway parameters were the total path length of postural sway movements (at the 0.8-m level), mean velocity, maximum deflection () for the x- and y -directional sway separately, 90% of the x - and y-directional sway, the standard deviation (S.D.) of the xand y-directional sway, and the total sway area. The path length was obtained by calculating the distance between the sequential location points of each sample, and after that, summing the values. The mean velocity was obtained by calculating the average of all the velocity values between sequential samples. The x and y were calculated by assessing the maximum and minimum xand y-directional deflections and subtracting the assessed values for each direction. Ninety percent x and y described the smallest possible difference where 90% of the calculated deflection points was located. The S.D. was calculated for both directions to provide statistical information about a subjects sway. Finally, the algorithm of the software approximated the outlines of the sway graph and calculated the total sway area on the graph (Fig. 2). The data were analyzed using SPSS for Windows software (SPSS, Chicago, IL). The Mann-Whitney twosample test was used to compare the measures of the control subjects with those of the PD patients. Pearson correlation coefficients were used to evaluate the clinical correlates of balance impairment in PD. RESULTS Table 3 shows the results of the sway measurements of both the PD patients and the control subjects. Significantly greater postural sway was detected in the PD patients than in the control subjects (eyes open test: velocity, P 0.003; path length, P 0.004; area, P 0.033; x, P 0.005; 90% x-direction, P 0.012; S.D. x-direction, P 0.011; eyes closed test: velocity, P 0.012; path length, P 0.013; area, P 0.016). No

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FIG. 2. Graph represents postural sway movements in a 77-year-old male patient (A) and in a 67-year-old male control subject (B) in the x and y coordinates.

differences in the y-directional (forwardbackward) sway parameters were found between PD patients and control subjects. The increase of postural sway was related to the duration of the PD, the amount of sway being most proTABLE 3. Postural sway in Parkinsons disease patients (n = 28) and control subjects (n = 32)
Variable Eyes open Velocity (cm/sec) Length (cm) Area (cm2) x (cm) y (cm) 90% x (cm) 90% y (cm) S.D. x (cm) S.D. y (cm) Eyes closed Velocity (cm/sec) Length (cm) Area (cm2) x (cm) y (cm) 90% x (cm) 90% y (cm) S.D. x (cm) S.D. y (cm) PD patients 0.50 0.15 29.95 9.37 1.60 0.91 2.01 0.59 1.85 0.61 1.29 0.39 1.23 0.42 0.41 0.12 0.40 0.14 0.74 0.26 44.68 15.34 3.17 1.62 2.65 0.76 2.47 0.68 1.71 0.53 1.62 0.45 0.56 0.20 0.53 0.15 Control subjects 0.40 0.11 24.02 6.74 1.23 0.95 1.64 0.46 1.77 0.77 1.07 0.31 1.28 0.62 0.34 0.11 0.41 0.20 0.60 0.16 35.80 9.81 2.38 1.47 2.36 0.83 2.31 0.68 1.53 0.55 1.50 0.50 0.48 0.17 0.48 0.17 P-value 0.003 0.004 0.033 0.005 0.218 0.012 0.673 0.011 0.534 0.013 0.013 0.016 0.066 0.346 0.164 0.254 0.132 0.131

nounced in patients with long-term disease (duration more than 5 years; Table 4). Comparing the results of the patients with long-term disease with those of the control subjects, a marked difference was found in most of the parameters (eyes open: velocity, P 0.004; path length, P 0.005; area, P 0.018; x, P 0.014; 90%
TABLE 4. Postural sway in patients with short-term Parkinsons disease (n = 18) and long-term (n = 10) Parkinsons disease and in control subjects (n = 32)
Variable Eyes open Velocity (cm/sec) Length (cm) Area (cm2) x (cm) y (cm) 90% x (cm) 90% y (cm) S.D. x (cm) S.D. y (cm) Eyes closed Velocity (cm/sec) Length (cm) Area (cm2) x (cm) y (cm) 90% x (cm) 90% y (cm) S.D. x (cm) S.D. y (cm) PD 5 yr 0.46 0.11 27.4 6.64 1.29 0.59 1.90 0.36* 1.54 0.29 1.21 0.31 1.01 0.21 0.38 0.09 0.32 0.06 0.74 0.25* 44.55 15.09* 3.05 1.56 2.66 0.93 2.49 0.76 1.73 0.63 1.55 0.43 0.54 0.20 0.51 0.15 PD > 5 yr 0.53 0.17** 31.36 10.50* 1.78 1.02* 2.07 0.69* 2.02 0.67 1.34 0.43* 1.35 0.47 0.42 0.14* 0.45 0.15 0.75 0.27* 44.75 15.91* 3.23 1.69* 2.64 0.68 2.46 0.65 1.70 0.49 1.66 0.47 0.57 0.20 0.53 0.15 Control subjects 0.40 0.11 24.02 6.74 1.23 0.95 1.64 0.46 1.77 0.77 1.07 0.31 1.28 0.62 0.34 0.11 0.41 0.20 0.60 0.16 35.80 9.81 2.38 1.47 2.36 0.83 2.31 0.68 1.53 0.55 1.50 0.50 0.48 0.17 0.48 0.17

Values are expressed as mean S.D. *P-values for the Mann-Whitney test comparing control subjects and patients with each other. x indicates maximum side-to-side deflection; y indicates forwardbackward deflection. 90% x, y indicates the smallest possible difference where 90% of the calculated deflection points were located. S.D. x, y indicates standard deviation of side-to-side and forwardbackward directional sway.

Values are expressed as mean S.D. *P < 0.05; **P < 0.01. P-values are for the Mann-Whitney test comparing control subjects with short-term PD and long-term PD. See Table 3 for abbreviations.

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TABLE 5. Postural sway in Parkinsons disease (PD) patient groups with a UPDRS motor score less than 10, 10 to 25, more than 25, and in control subjects
PD Variable Eyes open Velocity (cm/sec) Length (cm) Area (cm2) x (cm) y (cm) 90% x (cm) 90% y (cm) S.D. x (cm) S.D. y (cm) Eyes closed Velocity (cm/sec) Length (cm) Area (cm2) x (cm) y (cm) 90% x (cm) 90% y (cm) S.D. x (cm) S.D. y (cm) Group 1, <10 (n 7) 0.46 0.13 27.57 7.95 1.39 0.65 1.98 0.46 1.78 0.41 1.31 0.36 1.23 0.30 0.41 0.10 0.39 0.09 0.75 0.26 45.07 15.36 3.55 1.93 2.71 0.74 2.55 0.71 1.78 0.50 1.64 0.48 0.56 0.16 0.52 0.15 Group 2, 1025 (n 13) 0.49 0.13* 29.39 7.55* 1.48 0.79 1.98 0.70 1.80 0.89 1.25 0.45 1.20 0.52 0.40 0.14 0.41 0.18 0.69 0.19 41.04 11.49 2.73 1.39 2.57 0.84 2.32 0.68 1.66 0.59 1.56 0.51 0.56 0.25 0.51 0.18 Group 3, >25 (n 8) 0.55 0.21* 32.94 13.05* 1.99 1.23* 2.09 0.57* 1.99 0.66 1.34 0.35* 1.26 0.37 0.43 0.11* 0.41 0.12 0.84 0.34* 50.25 20.49* 3.54 1.72* 2.72 0.72 2.66 0.68 1.74 0.51 1.72 0.36 0.55 0.15 0.55 0.09 Control subjects (n 32) 0.40 0.11 24.02 6.74 1.23 0.95 1.64 0.46 1.77 0.77 1.07 0.31 1.28 0.62 0.34 0.11 0.41 0.20 0.60 0.16 35.80 9.81 2.38 1.47 2.36 0.83 2.31 0.68 1.53 0.55 1.50 0.50 0.48 0.17 0.48 0.17

Values are expressed as mean standard deviation. *P < 0.05. P-values are for the Mann-Whitney test comparing control subjects with Groups 1, 2, and 3. See Table 3 for abbreviations. UPDRS, Unified Parkinsons Disease Rating Scale.

x-direction, P 0.012; S.D. x-direction, P 0.013; eyes closed: velocity, P 0.048; path length, P 0.044; area, P 0.028). The difference between the PD patients with short-term disease (5 years or shorter) and the control subjects was significant (P < 0.05) for the parameters of sway area (eyes open), path length (eyes closed), and velocity (eyes closed). The results were not affected by age or gender. Table 5 presents the values of the control subjects and those of the PD patients with a UPDRS motor subscore less than 10 (Group 1), 10 to 25 (Group 2), and over 25 (Group 3). The sway parameters were higher in Group 3 than in the control group (eyes open: velocity, P 0.027; path length, P 0.033; area, P 0.036; x, P 0.022; 90% x-direction, P 0.030; S.D. x-direction, P 0.027; eyes closed: velocity, P 0.027; path length, P 0.027; area, P 0.020). Patients in Group 2 had higher (P < 0.05) values of sway velocity and path length than the control subjects, whereas the results of the patients of Group 1 did not differ from those of the control subjects. Amount of sway correlated also significantly with the Hoehn and Yahr stage and the UPDRS motor score items leg agility, arising from chair, posture, gait, postural stability, and body bradykinesia (Table 6), but not with the items tremor, rigidity, finger tabs, hand movements, and

TABLE 6. Pearson correlation coefficients between the variables velocity of postural sway, path length and sway area and the scores of the Hoehn and Yahr stage and various items of the UPDRS motor score in Parkinsons disease patients (n = 28) and in control subjects (n = 32)
Velocity Eyes open Hoehn and Yahr Leg agility (right) Leg agility (left) Arising from chair Posture Gait Postural stability Body bradykinesia Eyes closed Hoehn and Yahr Leg agility (right) Leg agility (left) Arising from chair Posture Gait Postural stability Body bradykinesia 0.447* 0.461* 0.459* 0.522** 0.534** 0.323 0.374* 0.387* 0.237 0.104 0.277 0.246 0.311 0.152 0.302 0.357 Length 0.441* 0.457* 0.482* 0.525** 0.534** 0.318 0.372* 0.381* 0.239 0.109 0.281 0.249 0.314 0.155 0.304 0.360 Area 0.501** 0.453* 0.409* 0.689*** 0.662*** 0.492** 0.528** 0.453* 0.303 0.105 0.166 0.287 0.393* 0.246 0.393* 0.326

*P < 0.05; **P < 0.01, ***P < 0.001. UPDRS, Unified Parkinsons Disease Rating Scale.

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M.K. VIITASALO ET AL. methods have been introduced.4,5,1113 Force platform studies have mainly been focused on altered reflex patterns35,7,10 and changes in center of foot pressure9,10 elicited by various stimuli. Postural sway during free quiet standing has been studied less frequently. One study comparing the predictive abilities of a wide range of balance tests and measures concluded that lateral instability may be a major predictor of future falling risk in elderly individuals.20 Our findings showed that postural sway, especially side-to-side directional sway, is increased in PD patients compared to that of control subjects. The commonly used force platform method analyses postural sway indirectly on the basis of ground reaction forces. However, its informative value is limited because of the assumption that a human body acts during quiet standing like a single pendulum21 where motions only occur around the ankle joint, and movements of the knee and hip joints as well as those of the upper body are ignored. Another problematic issue in the force platform method is how to solve the displacements of the center of gravity from the center of pressure. During the measurement, the center of pressure oscillates around the center of gravity position projection because of the subjects body segment dynamics. These facts may result in systematic errors, usually the overestimation of the center of gravity movements compared with actual ones.22,23 Unlike conventional platform posturography, our inclinometric method is not based on such assumptions as it directly measures absolute movements of the body, providing both momentary and cumulative values for sway parameters without complex mathematical and statistical estimations. This inclinometric device was also designed to avoid rotational artifacts by using a special joint structure, and to detect body movements at the level of the estimated center of gravity caused by multiple simultaneous motions of the lower extremity joints. Another advantage of this system is that it is lightweight and portable, and has a simple interface with the customized software. In conclusion, the present inclinometric device seems to be useful in detecting abnormalities of postural sway in PD. It appears to show that the amount of side-to-side directional sway is greater in PD patients than in healthy subjects, and this sway correlates with the severity and duration of the disease, and with the degree of bradykinesia, gait disorders, and lower extremity dysfunction. However, further studies with other patients suffering from balance disorders are needed to establish the wider clinical utility of this new method.

rapid alternating movements of hands. The correlations were stronger in the eyes open test than in the eyes closed test. DISCUSSION We have demonstrated that postural sway is markedly greater in PD patients than in healthy controls, and that it correlates with the duration and severity of PD and the clinical test scores for postural stability, body bradykinesia, gait disorders, posture, and lower extremity functions. Side-to-side directional sway seems to be pronounced in PD. The presented new inclinometry-based method for measuring postural stability proved to be useful in detecting differences in postural sway between PD patients and control subjects, the most sensitive parameters being velocity, path length, and total sway area. Although the pathophysiology underlying balance impairment in PD still remains obscure, several contributing factors are known. First, both selection and execution of postural reflexes seem to be disturbed in PD. Secondly, poor control of voluntary movements, partly due to bradykinesia, rigidity, and intrinsic muscle stiffness, and additional factors such as adverse effects of medication, orthostatic hypotension, and gait abnormalities may be involved.16 There are also reports5, 17 suggesting that gait disorders and postural instability may result from advanced nondopaminergic cerebral pathology and therefore these symptoms do not respond to levodopa. Impairment of balance in PD has been shown to be associated with a poor prognosis, a more rapidly progressive form of the disease, a higher mortality rate, and an increased prevalence of dementia.18 Here, postural sway was most markedly increased in PD patients with severe (UPDRS motor subscore > 25) or long-term disease. Among PD patients with moderate disease (motor score 1025), only the most sensitive sway parameters, i.e., velocity and path length, were increased, while the values of PD patients with mild disease were equal to those of the controls. Moreover, increased postural sway was observed in patients with high Hoehn and Yahr stage, impaired leg agility, slowness in arising from chair, stooped posture, gait disorders, impaired postural stability, or body bradykinesia. On the other hand, the amount of tremor, rigidity, or impaired movements of the higher extremity were not related to postural sway. Previous results concerning postural sway during quiet stance have been inconsistent. Some reports11,12,18,19 suggest that postural sway is pathognomic in PD, whereas others7 have not found differences between PD patients and control subjects. Methodological heterogeneity has been obvious. The prevailing method has been force platform posturography, although many other

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SWAY IN PARKINSONS DISEASE REFERENCES

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