Sensitivity and specificity of a portable system measuring postural tremor

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Neurotoxicology and Teratology, Vol. 19, No. 2, pp. 95-104,1997 Copyright 0 1997 Elsevier Science Inc. Printkdk the USA. All rights reserved

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Sensitivity and Specificity of a Portable System Measuring Postural Tremor RODERICK

EDWARDS

AND

ANNE

BEUTER

Dkpartement de Kinanthropologie, Universit6 du Qutbec LiMont&al, C.P. 8888, succ. Centre-ville, Montrdal, PQ, Canada H3C 3P8

Received

2 May 1996; Accepted

31 July 1996

EDWARDS, R. AND A. BEUTER. Sensitivity and specificity of a portable system measuring postural tremor. NEUROTOXICOL TERATOL 19(2) 95-104, 1997.-A portable, accelerometric system measuring tremor was evaluated. That is, the validity and consistency of measurements as well as its ability to discriminate pathologic from physiological tremor were investigated. Control subjects and patients with Parkinson’s disease were tested with this portable system and with an independent system that gave precise displacement data using lasers. It was found that amplitude of postural tremor as measured by the two systems differed significantly, but further investigation revealed that this difference was due 1) to the difference between amplitude of acceleration and amplitude of displacement, and 2) to changes in tremor over the time between tests, rather than to any inaccuracy or unreliability in the portable system. The other characteristics of tremor reported by the portable system were also valid and reasonably reliable in test-retest experiments, with the exception of the “harmonic index,” which proved less stable. Most of the reported characteristics were distributed differently for the control group and for the patients with Parkinson’s disease, but the large overlaps between distributions would make diagnosis difficult when tremor is not very pronounced. These results suggest that until better discriminating measures of tremor are available, tremor tests should be repeated and combined with other tests of motor function. 0 1997 Elsevier Science Inc.

Tremor quantification

Neurological deficits

Portable system

sway. Traditionally,

neuromotor test batteries have included subsets of these items. Among these tests, tremor is probably one of the most difficult movements to record and analyse adequately (3). This is an especially important issue because it appears that tremor is relatively vulnerable to neurotoxic influences but the recorded changes are usually subtle and the variability in the normal population is high. Tremor is defined as involuntary and continuous oscillatory movements of body parts such as extremities, jaws, eyes, or head that are normally present in healthy subjects (i.e., physiological tremor) but may change as a function of fear, anxiety, cold, anger, or hypoglycaemia (i.e., enhanced physiological tremor) (16). Sometimes enhanced physiological tremor is perfectly normal (it is basically physiological tremor with a larger amplitude); however, at other times it may reflect metabolic disturbances or pathologies of the nervous system (8). Like all movement abnormalities, physiological tremor tends to fluctuate over time in a significant way that makes it

BEHAVIORAL testing of occupational populations based on neuropsychology and experimental psychology started in the 1960s and has continuously evolved since. For example, the number of tests has considerably expanded and tests have

become computerized (1). Recently researchers have become aware that subtle changes in neuromotor control might represent a pathognomonic sign of neurotoxicity. As a result, a few valid and reliable neuromotor test batteries have been developed. One of them, composed of the Tremor Analysis Test System and the Coordination Ability Test System developed in Denmark in 1992 by Danish Product Development (DPD) is now available commercially to quantify exposure to neurotoxic agents such as metals, solvents, or pesticides. A sample of 61 normal subjects was tested with the Tremor Analysis Test System for standardization by Dr. Sigurd Mikkelsen at the Clinic of Occupational Health, Copenhagen County Hospital [(4) p. 311. Typical items included in neuromotor evaluation include measures of reaction time, finger tapping, rapid alternating movements, tremor, hand dexterity, and postural

-

Kequests tor reprints should be addressed to Anne Beuter, DCpartement de Kinanthropologie, succ. Centre-ville, Montrtal, PQ, Canada H3C 3P8. Fax: (514) 987-6616.

9.5

UniversitC du QuCbec B MontrCal, C.P. 8888,

EDWARDS

96 harder to classify in normal and pathological types (8,9,11,13). Authors have attempted to classify tremor by aetiology, by behavioral characteristics, by frequency, by electromyography, by pharmacological response, or by origin (i.e., central vs. peripheral). Other tremors defined as psychogenic (14) psychotic (lo), and orthostatic (i.e., rapid, irregular, and asynchronous) (18) are usually excluded from these classifications (8). These last authors indicate that today no single classification scheme is available to be used diagnostically. One additional difficulty is that other movement abnormalities such as clonus. chorea, or tics may also have, like tremor. an oscillatory nature. Tools and methodologies used to quantify and analyse tremor generally lack standardisation and it is not unusual to find completely opposite conclusions in studies dealing with a similar problem (3). We decided to select a pathology characterized by relatively well-known symptoms and to examine critically the ability of a typical test to detect differences in the subjects’ performance. Therefore, the purpose of this study was to determine the sensitivity (detecting small differences in tremor), specificity (detecting differences specific to a particular condition), and consistency of a simple, portable accelerometer system (the DPD system). First. tremor amplitude in patients with Parkinson’s disease and in healthy normal control subjects was quantified using precise displacement data from a laser-based system (LB). Second, all subjects were classified into two groups (i.e.. low-tremor amplitude and high-tremor amplitude groups) and tested using the DPD system. Third. the five characteristics calculated by the DPD system were compared between high- and low-tremor amplitude groups and between groups defined by a neurological assessment of presence or absence of Parkinson’s disease symptoms. Finally. validity was tested by a simultaneous recording of tremor by the two systems and consistency was checked by testing another group of subjects twice using the DPD system.

The Danish Product Development

AND

BEUTER

Tremor Test (DPD)

This tremor test has been developed by Danish Product Development (Fig. 1). It measures postural tremor successively in each hand during about 8.2 s while subjects look at a light stylus that they hold horizontally 10 cm away from their navel. The stylus is sensitive in a plane perpendicular to the tube axis and is individually calibrated with a calibration file. Two axis microaccelerometers embedded in the tip of the stylus measure accelerations in orthogonal directions. Samples arc taken at 500 Hz but are subsampled at 31.25 Hz after being put through a low-pass filter (5). The raw accelerations, after calibration, are reported to be accurate to within l-10% (standard deviation) across the frequency range used [(4). p. 201. The stylus is connected to a personal computer via a datalogger. Fourier transforms are calculated from the two time ser-ies and combined by a Pythagorean sum to give a single power spectrum. Recorded data (time series and power spectrum) and group statistics can be visualized immediately and power spectrum data can be exported in ASCII format for further analysis. Measures derived from acceleration data are based on the Fourier power spectrum. which gives a power distribution of the data in the frequency domain. It is composed of 1 I6 discrete values in the 0.9-15 Hz range. each approximately 0.12 Hz apart. This spectrum is supposed to react to “deviant” tremor patterns.

Fifty-four subjects were included in the primary study, 21 of them in the early stages (I and II) (12) of Parkinson’s disease. Control subjects were selected in the same age range. All the subjects were assessed by a neurologist on the same day as the tremor recordings were taken. The clinical examination revealed that all of the control subjects were free of neurological disorders except one who had a moderate rssential tremor. and two others who were assessed as having mild essential tremor. These last two. however, had tremor indistinguishable from normal tremor in our recordings. All sub,jects performed the two types of test (DPD and LB) with each hand. The LB test was done twice in succession for each hand. with a 30-s tracking task between the two trials.

Limitatiot2s Tremor was measured using the DPD and LB systems within a period of about 1 h so some differences may be present due to changes in conditions over this time (e.g.. fatigue, anxiety). Changes in amplitude were sometimes observed visibly over periods of a few minutes. Also, patients were under medication and this may have contributed to hide some of the symptoms. but it is well known that tnedications have a limited effect on tremor (7). To what extent medications alter tremor characteristics aside from amplitude is unknown.

FIG.

I. The Danish Product

Development

Tremor

Test

POSTURAL

TREMOR

The specific parameters

MEASURING examined

(4) are as follows:

1. Tremor intensity (I) is the RMS of acceleration recorded in the 0.9-15 Hz band during the 8.192-s test period and is expressed in m/s*. This is usually called “amplitude” in the literature and we use the latter term throughout. 2. Centre Frequency (F50) is the median frequency of the acceleration in the 0.9-15 Hz band during the 8.2-s test period: 50% of the area under the spectrum is at frequencies above the centre frequency and 50% is below. Units are Hz or s I. Based on a test performed by DPD on 61 control subjects, the normal human means for left and right hand are 7.5 and 7.2 Hz, respectively. 3. Standard Deviation of Centre Frequency (SFSO) indicates the degree of irregularity of the tremor. Sixty-eight percent of the area under the spectrum lies within 1 SD of the centre frequency. A simple rhythmic tremor has a small SF50 indicating that most of the area is within a narrow frequency band. Based on a test performed by DPD on control subjects, the normal human means for left and right hand are 3.8 and 3.5 Hz, respectively. 4. Harmonic Index (HI) compares the tremor spectrum with that of a single harmonic oscillation, which has a HI = 1.OO. A tremor composed of a few dominating frequencies has a high HI. It is defined as the area above the normalized spectrum (i.e., the highest peak is set to a power of I) between 0.Y and 14.9 Hz and below a power of 1. Based on a test performed by DPD on control subjects, normal tremor has a HI centered around 0.88, reflecting its irregular character, but values up to 0.95 are not unusual. 5. Tremor Index (TI) is a single measure incorporating the four previous measures. Any value deviating significantly from the norm will contribute a smaller than usual amount to the TI. The method of calculation is as follows: Let the recorded value for each of the four characteristics be denoted K,. Let the normal human mean and SD for each characteristic be denoted hl, and S,. respectively. Then the TI is given by TI = F c(ai

97

SYSTEM

exp (- I (K, - MI)/S, I).

where I;is a scaling factor to make the mean Tl of the test sample of normal human subjects equal 100 and the ai are l/6 for all except amplitude, for which a, is 113. (There is also a fifth component. SHI, a measure of dispersion of the Harmonic Index. which was used in previous versions of the DPD system but is no longer reported. though it is still apparently used in the calculation of the TI).

Past studies have shown that a LB system (2) measuring displacement can be used to record human tremor with high precision. In the present study. the LB system was used to quantify the amplitude of postural tremor and to classify the subjects into two groups: one group of subjects whose tremor was larger (detrended RMS > 0.17 mm) and the other group whose tremor was smaller (detrended RMS < 0. I7 mm). The LB system is placed at a fixed distance from the finger tip. This system uses analog output sensors based on optical triangulation range measurement. The laser beam emitted from the light-emitting element (semiconductor laser) passes through the projector lens to a target. A part of the diffusereflected laser light passes through the receiver lens to a spot on the position-sensitive device. The position of the light spot varies actor-ding to the detected distance. The change in out-

put currents caused by a deflection of the light spot OIIthe position-sensitive device is used to determine distance. Because this deflection is independent of the volume of the incident light. a stable distance measurement can be made. Proctdures

Used with the Laser-Bused

System (LB)

The subject is comfortably seated in a chair with the elbow joints flexed at 90” and resting on a foam-padded support. The subject’s forearm is lying pronated on the padded support. The index finger is extended while the remaining fingers of the tested hand rest in a semiflexed position on a specially molded soft support. Interphalangeal joints of the index are blocked by a light splint (-7 g) and vertical displacement of the index at the metacarpo-phalangeal joint is measured at the center of the finger nail (-10 cm from the joint). Visual feedback is presented on an oscilloscope screen placed 80 cm in front of the subject. A line corresponding to the finger position is displayed on the screen and subjects arc asked to try to keep this line on a fixed reference line. The analog signals recorded from the laser are sampled at 200 H7 for 30 s using an acquisition system (Experimenter’s Workbench. DataWave Technologies, Longmont, CO). The displacement data from the lasers were detrended by subtracting cubic polynomials fitted to 200 points (which corresponds to 1 s) every 0.5 s, over five 1024-point segments. A gradual transition was made (by linear combination) between the overlapping parts of successive cubits. This was intended to capture the shape of the curve smoothly. The magnitudes of the five segments were then averaged in the Fourier domain and tremor amplitude was calculated as the RMS of displacement of the KY-15 Hz component of the detrended and averaged signal. This method was used to remove the low-frequency component of the signal (due to drift. breathing, and hear-tbeat). and was preferred to a low-pass filter because it also removed the contribution of these factors to higher frequency parts of the spectrum (due to the effect known as “leakage”). Though curve fitting is usually avoided in spectral analysis. as it can create small artifacts in the spectrum. here we are only calculating amplitude of tremor (essentially a time domain characteristic). RtSC!LIS

The distribution of tremor amplitudes recorded with the LB system for the 216 trials (54 subjects X 2 hands X 2 trials) had a bimodal form (Fig. 2). with a large group below about 0.17 mm and a smaller group with a mode above this value. This was used as a criterion for dividing the trials into lowand high-amplitude groups. A particular hand of a particular subject was deemed to belong to the high-amplitude group if either of the trials for that hand did. This gave 12 cases (subject. hand) in the high-amplitude group and 96 cases in the low-amplitude group for subsequent analysis using the DPD system. Note that the high-amplitude group includes four cases (out of 66) from the control group and the low-amplitudc group includes 34 cases (out of 42) from the patient group (including the nonaffected hand in particular).

Kesults for the five characteristics reported by the DPD system for each hand of each subject in the two groups (as defined by the LB system) arc summarized in Table 1 (means

98

EDWARDS

AND

I

I

I

I

I

I

-5

-4

-3

-2

-1

0

BEUTER

Log intensity (mm)

FIG. 2. Histogram of LB tremor amplitude from detrended displacement data (54 subjects x 2 hands x 2 trials). The arrow divides the high- and low-amplitude groups. (Note that the high-amplitude group includes trials from control subjects and the low-amplitude group includes trials from patients).

and SDS). Figure 3 gives a histogram of DPD amplitudes in the two groups. The high- and iow-tremor amplitudes as calculated by the DPD system are not neatly separated, although there is a significant difference in mean amplitude for the two groups. The other characteristics vary by differing amounts between the two groups. Centre frequency is distributed similarly for both groups. Harmonic index and tremor index show some separation, although the means are still within 1 SD of each other. Frequency dispersion separates the two groups slightly more. Therefore, the other three characteristics used in calculating the tremor index (centre frequency, frequency dispersion, and harmonic index), although somewhat correlated with amplitude, extract different information from the tremor. The differences in amplitude results from the DPD and LB systems, indicated by the large overlap in DPD amplitude be-

TABLE

1

DPD SYSTEM

Characteristic Amplitude Log(amplitude)* Centre freq. Freq. dispersion Harmonic index Tremor index

High-Amplitude Group (n = 12) 0.314 - 1.614 6.267 1.592 0.937 59.83

2 ? -c 5 k i

0.372 0.944 1.059 1.335 0.045 39.20

Low-Amplitude Group (n = 96) 0.095 -2.402 6.408 2.848 0.903 86.74

+ -t 2 ? z 5

0.036 0.291 1.083 1.048 0.050 27.80

Values are means t SDS of spectral characteristics, 54 subjects, both hands (high- vs. low-amplitude groups). *Amplitude is given because it is reported by the DPD system, but the distribution of log(amplitude) for our sample is closer to being Gaussian.

tween the high- and low-amplitude groups, suggested that further tests be done to check validity and consistency of the measuring systems. Validity Validity of the DPD system measurements was assessed by testing a small group of subjects simultaneously with the DPD and LB systems. Six subjects were tested four times each (two left, two right). The DPD stylus was held in the usual position and a light (
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