Analysis of Sway in Parkinson’s Disease

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Analysis of Sway in Parkinsons Disease Using a NewInclinometry-Based Method

Maria K. Viitasalo, MD, 1 Ville Kampman, 2 Kyosti A. Sotaniemi, MD, 1 Seppo Leppavuori, TD, 2

Vilho V. Myllyla, MD, 1 and Juha T. Korpelainen, MD 1 *

1 Department of Neurology, University of Oulu, Oulu, Finland 2 Department of Laboratory of Microelectronics, University of Oulu, Oulu, Finland

Abstract: In order to analyze balance control, we developed anew inclinometry-based method to provide direct informationabout body sway in the side-to-side and forwardbackward

directions. We tested the clinical utility of this method foranalyzing balance in Parkinsons disease (PD), and studied theclinical correlates of the balance measures in PD. Postural swaywas measured during quiet stance with eyes open and eyesclosed in 28 PD patients and in 32 age- and sex-matched con-trol subjects. Postural sway was modeled using side-to-side andforwardbackward directional sway movements, sway veloc-ity, and sway area. The amount of postural sway in the PDpatients was greater than in the control subjects, the higherlevel being most marked in patients with severe or long-

duration PD. All the side-to-side directional sway parameterswere abnormal in the PD patients compared with the controlsubjects ( P < 0.05), whereas the forwardbackward directional

parameters did not differentiate the two groups. The most sen-sitive measures of sway were path length, velocity, and area.The duration and severity of PD seem to be particularly asso-ciated with the amount of side-to-side directional posturalsway. This new inclinometric method appears to be useful inquantifying postural sway and evaluating balance impairmentin PD. 2002 Movement Disorder Society

Key words: postural sway; balance impairment; Parkinsonsdisease

Because of degeneration of dopaminergic nigrostriatal

projections and other motor control centers, parkinsonianpatients suffer from postural instability, stooped posture,and gait difficulties. Impairment of balance is an impor-tant feature of Parkinsons disease (PD), often leading tofalls and injuries. It has recently been shown that PDpatients have an increased risk of death strongly relatedto the presence of gait disturbances. 1 Because posturalinstability is associated with advanced stages of PD withdiminished functional ability and poor prognosis, 2 an ac-curate method for analyzing balance is needed.

In the clinical setting, balance evaluation in PD hasmainly been based on bedside tests such as the patientsability to recover equilibrium when knocked off balanceby pulling suddenly backwards on the shoulders, or fall-

ing frequency, gait difficulties, and the need for postural

support. However, these kinds of tests are inaccurate andtheir sensitivity and reliability is limited. In the labora-tory, the amount of postural sway reflecting balance dis-orders in PD has previously been assessed indirectly byrecording ground reaction forces as a subject stands on aplatform equipped with force transducers. 37 Thismethod has been used to evaluate postural stability undervarying sensory conditions 810 and to investigate pos-tural reflexes. 37,10 Movements of the center of gravityhave also been measured with a platform-mounted po-tentiometer attached to the body. 4,5,11 Other motion mea-suring instruments, for example infrared emitting di-

odes,12,13

have also been used for balance measurementsin PD. However, all of these methods have severe limi-tations when quantifying balance disorders in a clinicalsetting.

We developed an inclinometry-based method to pro-vide direct information about body sway in the side-to-side and forwardbackward directions. We tested theclinical utility of this method of recognizing balance im-

*Correspondence to: Juha T. Korpelainen, Department of Neurol-ogy, University of Oulu, PO Box 5000, 90014 Oulun yliopisto, Finland.E-mail: [email protected]

Received 16 March 2001; Revised 17 July 2001; Accepted 25 July2001

Published online 7 January 2002 in Wiley InterScience (www.interscience.wiley.com). DOI 10.1002/mds.10023

Movement DisordersVol. 17, No. 4, 2002, pp. 663669 2002 Movement Disorder Society

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pairment, assessed postural instability in PD by compar-ing 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

SubjectsThe protocol was approved by the Ethics Committee

of the local Medical Faculty, and informed consent wasobtained from each subject. Twenty-eight patients withPD (14 men and 14 women) and 32 age- and sex-matched control subjects participated in the study (Table1). The severity of PD was evaluated by the Hoehn andYahr stage 14 and by the motor subscale of the UnifiedParkinson s Disease Rating Scale (UPDRS). 15 For fur-ther analyses, the patients were divided into subgroupsaccording to their motor scores on the UPDRS subscale:Group 1, 25 (n 8). Subjects were further divided intotwo subgroups according to the duration of the disease:(1) 5 years or less (n 18); (2) more than 5 years (n10). The mean age of the patients of the subgroups andthat of the controls was similar. All the PD patients wereclinically examined and their postural sway was mea-sured during the on-period at the moment when dyski-nesia was not present.

All the PD patients were on levodopa medication.Levodopa was used as a monotherapy in five cases andin combination with a dopamine agonist in 10 patients,with entacapone in 19 and with selegiline in eight.Twelve patients had a concomitant cardiovascular dis-

ease, either arterial hypertension or coronary heart dis-ease. Seven patients had a musculoskeletal disease, twobronchial asthma, one noninsulin-dependent diabetesmellitus, and two had hypothyreosis (Table 2). Three of the patients used nitrates, three diuretics, six beta block-ers, one a calcium channel blocker, two acetylsalicylicacid, one dipyridamole, one thyroxine, one benzodiaze-pine, one zopiclone, one hydroxyzine, and two had medi-cation for bronchial asthma.

The control group consisted of 32 sex- and age-matched subjects, who were spouses or acquaintances of the patients. Twelve had cardiovascular diseases, eitherarterial hypertension or coronary heart disease, and onehad chronic atrial fibrillation. Six had musculoskeletaldiseases, six had bronchial asthma, and four had hypo-thyreosis. One used nitrates, one digoxin, two diuretics,five beta blockers, one a calcium channel blocker, one anangiotensin converting enzyme inhibitor, four acetylsali-cylic acid, one dipyridamole, one warfarin, four thyrox-ine, one benzodiazepine , one amitriptyline, and fivemedication for bronchial asthma. None of the controlsubjects had any difficulty in standing without supportduring the measurements.

MethodsPostural sway measurements were performed under

standardized conditions. Every test was visually con-trolled by the same investigator. The measurements weretaken during normal standing both with eyes open andeyes closed and they were repeated once. Each recordinglasted 60 seconds. The mean value of the two consecu-

tive recordings was used in the analysis. During the test,the subjects stood at attention, without shoes, with theirfeet together and arms beside the body. In the eyes-opentest, subjects were asked to look straight ahead at a mark on the facing wall.

The inclinometric device consisted of a belt fastenedfirmly at the level of the iliac crist, an inflexible mea-suring rod, an inclinometric module, a joint structurelying on the ground, a power unit, and a personal com-puter. The measuring rod transmitted movements of thebody to the detecting inclinometric module located on itsthe lower end (Fig. 1). The bottom end of the rod wasattached to a joint structure that was designed to avoid

both the rod and the sensor module rotating around thelongitudinal axis during the measurement. The height of the measuring rod was adjusted according to the heightof the subject. The deviating movement ( D) of the mea-suring rod was calculated separately for the side-to-side( x ) and forward backward ( y) directions using the equa-tion D

x,y=tan

x,y x h, where

x,yis the measured inclination

in the x or y direction, and h the selected calculation

TABLE 1. Clinical characteristics of Parkinsons disease patients and control subjects

Characteristics Patients(n 28) Controls(n 32)

Gender (M/F) 14/14 16/16Mean age, yr (range) 64.9 (50 83) 63.1 (46 77)Mean duration of PD, yr (range) 7.1 (2 17) Mean Hoehn and Yahr stage (S.D.) 2.4 (0.8) Mean UPDRS motor score (S.D.) 18.2 (10.1) Motor fluctuations or dyskinesias 14

UPDRS, Unified Parkinson s Disease Rating Scale.

TABLE 2. Concomitant diseases of Parkinsons disease patients and control subjects

DiseasePatients

(n 28)Controls(n 32)

Cardiovascular disease 12 12Asthma 2 6

Noninsulin-dependent diabetes mellitus 1 0Hypothyreosis 2 4Musculoskeletal disease 7 6

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height (Fig. 1). By combining these two calculated de-flections ( D

x,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 de-

tecting sensor. The module had two output voltages pro-portional to the x- and y-axis inclination of the measur-ing rod. These two voltages were converted to digitaldata using two 12-bit analog to digital (A/D)-converters.The A/D-conversion frequency of both channels was 20Hz. The converted data was filtered using an 8-orderlow-pass digital filter (cut frequency 3 Hz) to avoid high-frequency noise. Digital data were calculated for the

sway parameters and displayed between every A/D-conversion to provide a real-time display.

A constant calculation height ( h 0.8 m) was usedfor analyzing the sway parameters of all the subjects. Byusing this constant value h, any possible effect of thedifferent heights of the subjects on the results was elimi-nated. Thus, all the calculated sway parameters repre-sented the measuring rod movements on the horizontalplane at the height of 0.8 m. The measurement resolutionof the inclinometric module was 0.006 degrees, and therepeatability was less than 0.02 degrees. Thus, the mea-surement repeatability of the rod movement at the 0.8-mlevel, for example, was less than 0.4 mm ([tan 0.03] 800 mm). The response time of the module to inclinationchange (10 90%) was 40 ms.

The recorded sway parameters were the total pathlength 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 x -and y-directional sway, and the total sway area. The pathlength was obtained by calculating the distance betweenthe sequential location points of each sample, and afterthat, summing the values. The mean velocity was ob-tained by calculating the average of all the velocity val-ues between sequential samples. The x and y werecalculated by assessing the maximum and minimum x -and y-directional deflections and subtracting the assessedvalues for each direction. Ninety percent x and y de-scribed the smallest possible difference where 90% of the calculated deflection points was located. The S.D.

was calculated for both directions to provide statisticalinformation about a subject s sway. Finally, the algo-rithm of the software approximated the outlines of thesway graph and calculated the total sway area on thegraph (Fig. 2).

The data were analyzed using SPSS for Windows soft-ware (SPSS, Chicago, IL). The Mann-Whitney two-sample test was used to compare the measures of thecontrol subjects with those of the PD patients. Pearsoncorrelation coefficients were used to evaluate the clinicalcorrelates of balance impairment in PD.

RESULTS

Table 3 shows the results of the sway measurements of both the PD patients and the control subjects. Signifi-cantly greater postural sway was detected in the PD pa-tients than in the control subjects (eyes open test: veloc-ity, 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, P0.012; path length, P 0.013; area, P 0.016). No

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

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differences in the y-directional (forward backward)sway parameters were found between PD patients andcontrol subjects.

The increase of postural sway was related to the du-ration of the PD, the amount of sway being most pro-

nounced in patients with long-term disease (durationmore than 5 years; Table 4). Comparing the results of thepatients with long-term disease with those of the controlsubjects, a marked difference was found in most of theparameters (eyes open: velocity, P 0.004; path length,P 0.005; area, P 0.018; x , P 0.014; 90%

TABLE 3. Postural sway in Parkinson s disease patients(n = 28) and control subjects (n = 32)

Variable PD patients Control subjects P-value

Eyes openVelocity (cm/sec) 0.50 0.15 0.40 0.11 0.003Length (cm) 29.95 9.37 24.02 6.74 0.004Area (cm 2 ) 1.60 0.91 1.23 0.95 0.033

x (cm) 2.01 0.59 1.64 0.46 0.005 y (cm) 1.85 0.61 1.77 0.77 0.218

90% x (cm) 1.29 0.39 1.07 0.31 0.01290% y (cm) 1.23 0.42 1.28 0.62 0.673S.D. x (cm) 0.41 0.12 0.34 0.11 0.011S.D. y (cm) 0.40 0.14 0.41 0.20 0.534

Eyes closedVelocity (cm/sec) 0.74 0.26 0.60 0.16 0.013Length (cm) 44.68 15.34 35.80 9.81 0.013Area (cm 2 ) 3.17 1.62 2.38 1.47 0.016

x (cm) 2.65 0.76 2.36 0.83 0.066 y (cm) 2.47 0.68 2.31 0.68 0.346

90% x (cm) 1.71 0.53 1.53 0.55 0.16490% y (cm) 1.62 0.45 1.50 0.50 0.254S.D. x (cm) 0.56 0.20 0.48 0.17 0.132S.D. y (cm) 0.53 0.15 0.48 0.17 0.131

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 forward-

backward deflection.90% x, y indicates the smallest possible difference where 90% of the

calculated deflection points were located. S.D. x, y indicates standarddeviation of side-to-side and forward backward directional sway.

TABLE 4. Postural sway in patients with short-termParkinson s disease (n = 18) and long-term (n = 10)Parkinson s disease and in control subjects (n = 32)

Variable PD 5 yr PD > 5 yr Controlsubjects

Eyes openVelocity (cm/sec) 0.46 0.11 0.53 0.17** 0.40 0.11Length (cm) 27.4 6.64 31.36 10.50* 24.02 6.74Area (cm 2 ) 1.29 0.59 1.78 1.02* 1.23 0.95

x (cm) 1.90 0.36* 2.07 0.69* 1.64 0.46 y (cm) 1.54 0.29 2.02 0.67 1.77 0.77

90% x (cm) 1.21 0.31 1.34 0.43* 1.07 0.3190% y (cm) 1.01 0.21 1.35 0.47 1.28 0.62S.D. x (cm) 0.38 0.09 0.42 0.14* 0.34 0.11S.D. y (cm) 0.32 0.06 0.45 0.15 0.41 0.20

Eyes closedVelocity (cm/sec) 0.74 0.25* 0.75 0.27* 0.60 0.16Length (cm) 44.55 15.09* 44.75 15.91* 35.80 9.81Area (cm 2 ) 3.05 1.56 3.23 1.69* 2.38 1.47

x (cm) 2.66 0.93 2.64 0.68 2.36 0.83 y (cm) 2.49 0.76 2.46 0.65 2.31 0.68

90% x (cm) 1.73 0.63 1.70 0.49 1.53 0.5590% y (cm) 1.55 0.43 1.66 0.47 1.50 0.50S.D. x (cm) 0.54 0.20 0.57 0.20 0.48 0.17S.D. y (cm) 0.51 0.15 0.53 0.15 0.48 0.17

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.

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.




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rapid alternating movements of hands. The correlationswere stronger in the eyes open test than in the eyes closedtest.

DISCUSSION

We have demonstrated that postural sway is markedlygreater in PD patients than in healthy controls, and that itcorrelates with the duration and severity of PD and theclinical test scores for postural stability, body bradyki-nesia, gait disorders, posture, and lower extremity func-tions. Side-to-side directional sway seems to be pro-nounced in PD. The presented new inclinometry-basedmethod for measuring postural stability proved to be use-ful in detecting differences in postural sway between PDpatients and control subjects, the most sensitive param-eters being velocity, path length, and total sway area.

Although the pathophysiology underlying balance im-pairment in PD still remains obscure, several contribut-ing factors are known. First, both selection and executionof postural reflexes seem to be disturbed in PD. Sec-ondly, poor control of voluntary movements, partly dueto bradykinesia, rigidity, and intrinsic muscle stiffness,and additional factors such as adverse effects of medi-cation, orthostatic hypotension, and gait abnormalitiesmay be involved. 16 There are also reports 5, 17 suggestingthat gait disorders and postural instability may resultfrom advanced nondopaminergic cerebral pathology andtherefore these symptoms do not respond to levodopa.Impairment of balance in PD has been shown to be as-sociated with a poor prognosis, a more rapidly progres-sive form of the disease, a higher mortality rate, and an

increased prevalence of dementia.18

Here, postural swaywas most markedly increased in PD patients with severe(UPDRS motor subscore > 25) or long-term disease.Among PD patients with moderate disease (motor score1025), only the most sensitive sway parameters, i.e.,velocity and path length, were increased, while the val-ues of PD patients with mild disease were equal to thoseof the controls. Moreover, increased postural sway wasobserved in patients with high Hoehn and Yahr stage,impaired leg agility, slowness in arising from chair,stooped posture, gait disorders, impaired postural stabil-ity, or body bradykinesia. On the other hand, the amountof 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 reports 11,12,18,19

suggest that postural sway is pathognomic in PD,whereas others 7 have not found differences between PDpatients and control subjects. Methodological heteroge-neity has been obvious. The prevailing method has beenforce platform posturography, although many other

methods have been introduced. 4,5,11 13 Force platformstudies have mainly been focused on altered reflexpatterns 3 5,7,10 and changes in center of foot pressure 9,10

elicited by various stimuli. Postural sway during freequiet standing has been studied less frequently.

One study comparing the predictive abilities of a widerange of balance tests and measures concluded that lat-eral instability may be a major predictor of future fallingrisk in elderly individuals. 20 Our findings showed thatpostural sway, especially side-to-side directional sway, isincreased in PD patients compared to that of controlsubjects.

The commonly used force platform method analysespostural sway indirectly on the basis of ground reactionforces. However, its informative value is limited becauseof the assumption that a human body acts during quietstanding like a single pendulum 21 where motions onlyoccur around the ankle joint, and movements of the kneeand hip joints as well as those of the upper body areignored. Another problematic issue in the force platformmethod is how to solve the displacements of the center of gravity from the center of pressure. During the measure-ment, the center of pressure oscillates around the centerof gravity position projection because of the subject sbody segment dynamics. These facts may result in sys-tematic errors, usually the overestimation of the center of gravity movements compared with actual ones. 22,23 Un-like conventional platform posturography, our inclino-metric method is not based on such assumptions as itdirectly measures absolute movements of the body, pro-

viding both momentary and cumulative values for swayparameters without complex mathematical and statisticalestimations. This inclinometric device was also designedto avoid rotational artifacts by using a special joint struc-ture, and to detect body movements at the level of theestimated center of gravity caused by multiple simulta-neous motions of the lower extremity joints. Anotheradvantage of this system is that it is lightweight andportable, and has a simple interface with the customizedsoftware.

In conclusion, the present inclinometric device seemsto be useful in detecting abnormalities of postural sway

in PD. It appears to show that the amount of side-to-sidedirectional sway is greater in PD patients than in healthysubjects, and this sway correlates with the severity andduration of the disease, and with the degree of bradyki-nesia, gait disorders, and lower extremity dysfunction.However, further studies with other patients sufferingfrom balance disorders are needed to establish the widerclinical utility of this new method.




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Analysis of Sway in Parkinson’s Disease