The development of a neurobehavioral test battery for use in hazard evaluations in occupational settings

Neurotoxicologyand Teratology,Vol. 12, pp. 509-514. ©Pergamon Press plc, 1990. Printed in the U.S.A.

0892-0362/90 $3.00 + .00

The Development of a Neurobehavioral Test Battery for Use in Hazard Evaluations in Occupational Settings I ANN M. WILLIAMSON

National Institute o f Occupational Health and Safety, P.O. Box 58, Sydney, Australia 2001

WILLIAMSON, A. M. The development of a neurobehavioral test battery for use in hazard evaluations in occupational settings. NEUROTOXICOL TERATOL 12(5) 509-514, 1990.--The interest in, and number of, neurobehavioral test batteries for use in occupational settings has increased markedly over the last decade. While this is a welcome development in furthering the cause for greater acceptance of these methods in hazard evaluation and toxicity testing, there are a number of issues that are not being addressed by many test battery designers and users. Without careful consideration of important issues concerning the use of the test batteries, such as the level of testing needed and the selection of appropriate tests, the specificity and sensitivity of tests chosen, the role of computers in test delivery, and the standardisation and interpretation of test results, it is likely that the credibility and utility of neurobehavioral testing will be jeopardised even at this early stage of development. In this paper, the development of a test battery for use in occupational health will be discussed with particular reference to the degree of success in addressing some of the issues described above. A test battery was designed using an information processing model of behavior generation as a base. A continuing programme of standardisation is being carried out on a range of working populations and current results will be discussed. The battery has also been used to evaluate the effects of occupational exposure to a number of hazardous substances including mercury, lead, and most recently, solvents, and to hazardous environments, specifically, underwater work. These results are summarised in terms of the ability of the test battery to detect the effects of particular hazards. Neurobehavioral test battery

Occupational evaluation

Toxicity testing

Humans

Behavioral toxicology

decrements at the subclinical level, since at this level tests may also pick up functional depression due to other factors like age, educational level or alcohol consumption. For neurobehavioral tests to be useful for detection of toxicant effects at low levels of exposure, these factors must either be controlled for, or their effects on test performance must be known, or both. In addition, it is desirable for test batteries to discriminate between the effects of various toxic substances, when applicable, by revealing a specific pattern of functional disturbance for each toxic substance. Finally, test batteries should provide leads for further investigation. Since no test battery that is currently available is likely to be useful for all toxicants in all situations, it is unlikely that a single test battery will be able to cover the full range of possible neurobehavioral functional effects. It is important, however, that it provide information for the direction of more detailed further investigation. This paper focuses on some of the efforts that have been made in addressing these issues in the development of a neurobehavioral test battery for use in hazard evaluation in occupational settings.

IN occupational health, neurobehavioral testing is a relatively recent addition for use in the evaluation of hazard. Its potential, however, is clearly being appreciated, and increasing numbers of batteries of tests are being developed and applied. While this is an important progression for the field, a number of issues have not been addressed in the design of many of these batteries. These pose problems which can compromise the utility of a given test battery. First, to be useful for neurobehavioral field studies, tests in a test battery must be sensitive enough to detect early functional impairments due to toxic exposure. Use of some of the classical neuropsychological tests like many of those from the WAIS (Wechsler Adult Intelligence Scale) (16) or the Halstead-Reitan (9) are effective for detecting gross head injuries, but may not be sensitive enough to detect early or more subtle functional changes. Since early functional changes are one of the major concerns in occupational toxicity testing, it is essential to use tests that can detect them. The second problem arises in attempting to detect performance

~The views expressed in this article are those of the author and do not necessarily reflect those of the National Occupational Health and Safety Commission.

509

510 DESCRIPTIONOF THE TESTBA'ITERY The test battery was designed to give a reasonably comprehensive coverage of the major areas of known neurobehavioral function and also to provide an integrated framework for the explanation of detected changes in functional status. The aim of the battery was not only to answer the question of whether a particular hazard affects the nervous system, but also to determine which function(s), in particular, is affected by that hazard. The design of many test batteries limits the interpretation of findings obtained with them to the results of effects on specific functions. For example, a number of studies have shown that occupational exposure to various organic solvents produces slowed reaction time, poorer manual dexterity, and memory impairments (5,10). While these findings suggest that chronic exposure to solvents affects nervous system function, they provide little further knowledge that would guide us to the actual mechanism of action of solvents. Behaviors like manual dexterity and memory are an amalgamation of a number of fundamental processes which can be traced to particular nervous processes. In order to produce either behavior, for example, a critical level of attention is required. If this level is not achieved, performance on tests for manual dexterity or memory will be reduced. Unless attention is measured separately, it is not possible to determine whether apparent deficits in dexterity and memory are simply due to poorer attention, since the subject must fully attend to the task in order to perform it at an optimum level. Under these conditions, the likelihood of gaining even partial understanding of the nature of the underlying physiological damage becomes virtually impossible. In an attempt to overcome such problems of interpretation, the tests for the battery to be discussed here were selected using an information processing model of human performance generation (17). The tests included in the battery have been described in detail elsewhere (18). Briefly, they include: 1) Critical flicker fusion (CFF): A visual perception test in which a light cycling on and off, usually between 70 and 20 Hz, is used to measure an individual's ability to discriminate the onset of flicker as the on-off rate is reduced. The fusion threshold in cycles per second is recorded for each eye. 2) Vigilance: A sustained attention task requiring the individual to track over a 20-minute period the illumination sequence of five lights and the infrequent occurrence (10% illuminations) of two lights illuminated simultaneously. The number of single and double targets tracked and the number of pauses in responding are recorded. 3) Hand steadiness test: A visual-motor coordination test in which the individual is required to hold a thin, metal stylus in a 5-mm diameter hole without touching the edges for 1 minute. The number and duration of touches to the upper and lower edges of the hole are recorded as off-target corrections and fatigue, respectively. 4) Simple reaction time test: A perceptual speed test in which the individual responds to the onset of a light as quickly as possible by pressing a button. Speed of response is measured (in msec). 5) Visual pursuit test: A psychomotor task requiring the individual to track a moving light within a circular pathway at each of two separate speeds. Time on target is recorded. 6) Sensory store memory test: Pairs of letters are presented tachistoscopically for brief periods to left, central and right visual fields. The individual's task is to recall what they have seen. The number of letters recalled at each position is recorded. 7) Sternberg memory test: A short-term memory test in which individuals are asked to remember a varying number of single digits (2, 3, 4, or 5 digits) and then respond positively (Yes button) if the digit was present in their to-be-remembered set or negatively (No button) if the digit was not present. Speed of response and the

WILLIAMSON

number of errors are recorded. 8) Paired associates, short-term memory test: This involves the recall of 5 pairs of three letter words in which all pairs are shown once, followed immediately by the first member of each pair. The individual's task is to complete each pair. The number of words correct on the first trial is recorded as a measure of short-term memory. The sequence is repeated until the subject correctly recalls all pairs and the number of trials to recall all words correctly is recorded as a measure of learning. 9) Paired associates, long-term memory test: This requires the individual to recall the five words learned earlier (about 90 minutes before) when presented once only with the first member of each pair. The number of words recalled correctly is recorded. Most of the tests can now be administered and analysed with the aid of an IBM microcomputer or clone (CFF, vigilance, hand steadiness, reaction time, and Sternberg memory tests). For the other tests, stimulus presentation and response generation occurred as described previously (18). "Computerisation" of these tests only extended to using the computer for generating stimuli which were then presented via a separate piece of hardware and for recording responses which were made on that hardware. The computer monitor and keyboard were not used for stimulus presentation and response generation, respectively, as there are some problems inherent in doing so. These include: less control over the subject's attention to the stimulus, added distractions in responding due to extraneous information on the keyboard, and the generally low level of computer familiarity in the populations that are commonly exposed to toxic substances at the workplace. The test battery also included a demographic questionnaire which covered age, sex, education level, ethnic background, present and previous occupations, details of daily routine such a waking time and bedtime, and the amount and frequency of consumption of alcohol and other drugs. STANDARDISATIONOF TESTS A continuing program of test standardisation is in progress. The following data are based on the first 228 nonexposed workers tested and are used to estimate confidence limits for nonexposed functional status for each test. Considerably more data will be collected in order to refine these estimates. However, some useful indications can be derived already for normal limits on each test and for the effects of confounding variables on test performance. Table 1 shows the results of multivariate linear regression analysis for the effect of 5 major possible confounding variables on performance on each test: age, education level, type of job, sex and the length of residence in Australia. This last variable is included because Australia has a high proportion of recent immigrants from non-English-speaking countries. It might be important, therefore, to take into account the subject's ability to understand the test instructions and, for verbal tests, to perform the test. Neither CFF nor the steadiness tests were significantly influenced by any of the five variables considered. Not surprisingly, age was shown to be a confounder for every other test although its effects as a single confounder were relatively small (<10% of variance explained in each case). Combinations with other confounders increased the proportion of variance to a maximum of 26% for parts of the sensory store memory test. All 5 possible confounders affected at least one test. Future analyses will include differences in daily routine and social use of drugs such as caffeine, cigarettes, and alcohol as predictors of test performance. This type of analysis provides a useful basis for designing studies in which the test battery is employed. It also demonstrates the need to consider age differences in case-control and cross-

TEST BATTERY DEVELOPMENT

511

TABLE 1

TABLE 2

RESULTS OF MULTIVARIATE LINEAR REGRESSION ANALYSIS FOR NEUROBEHAVIORAL TEST PERFORMANCE USING COMBINATIONS OF AGE, EDUCATION, JOB TYPE, SEX AND LENGTH OF RESIDENCE AS PREDICTOR VARIABLES

SUMMARY OF RESULTS FOR STUDY COMPARING MERCURY-EXPOSED WORKERS AND NONEXPOSED CONTROLS ON A RANGE OF NEUROBEHAVIORAL TESTS

Tests Test

Predictors

Variance Explained

Mercury-Exposed

Controls

Critical flicker fusion: (mean, s.d., both eyes, Hz/sec)

42.35 (9.04)

40.43 (7.20)

4.38* (0.57)

8.69 (1.74)

Critical flicker

None

na

Vigilance Pauses Errors (last half of test)

Vigilance: (mean, s.d., pauses in performance)

Age Age

9% 7%

Reaction time: (mean, msec)

Reaction time

Age

9%

Hand steadiness

None

na

Visual pursuit: (mean, s.d., time on target at 30 rpm)

Visual pursuit Slow tracking Fast tracking

Age, Sex Age, Sex, Job

14% 16%

Sensory store memory Left visual field Central visual field Right visual field

Age Age, Education, Sex Age, Sex

7% 26% 26%

Sternberg memory test Positive responses Negative responses

Age, Education None

16% na

Paired associates test Short-term memory Long-term memory

Job, Sex, Residence Age, Education, Residence

21% 24%

sectional studies and other potential confounders in studies where specific tests are used. It also provides an estimate of the extent to which these confounders affect performance on each test. A brief study of the reliability of the test measures has been made on a small group (n = 10) of nonexposed workers who were tested twice on all tests at an interval of at least 3 months. Test-retest results show good reliability (reliability coefficients greater than .8) for all tests except the hand steadiness test (reliability coefficients between .53 and .75). Further work is being carded out to confirm these findings using a larger sample size. These results assisted in design decisions for the next stage of development of the test battery. USING THE TEST BATTERY

Sensitivity: How Well Does the Test Battery Discriminate Between Exposed and Nonexposed Workers? An important consideration for a test battery designed for use in neurobehavioral toxicological studies is how well it discriminates between exposed and nonexposed workers. The battery discussed here was used in three case-control studies, each involving a different hazardous exposure. In each study, exposed and nonexposed workers were matched individually for age, sex, educational background, type of job, ethnic background and length of residence in Australia. Workers who were heavy users of alcohol, had a history of head injury or neurological disorder or who had a recent (in the past 24 hours) significant departure from their usual daily routine were excluded from testing. Inorganic mercury exposure. In the fLrSt study, the test battery performances of a small group of workers exposed to inorganic

Hand steadiness: (last 20 sec of test) Off-target touches (mean, s.d.) % time off target (mean, s.d.) Sternberg test: (results for lines of best fit) Motor component (intercepts) Positive set (yes) Negative set (no) Cognitive component (slopes) Positive set (yes) Negative set (no) Paired associates (means) Immediate recall Trials to criterion Delayed recall

375.00

347.00

5.06 (2.08)

7.04 (3.69)

52.50* (16.10) 32.50* (8.70)

26.00 (9.09) 10.20 (7.50)

695.60* 715.70"

429.70 14.70

61.50 82.90

71.50 57.90

2.33 2.88 3.74

3.78 1.75 3.75

*Statistically significant difference between mercury-exposed workers and their controls (p<0.05).

mercury (n = 12) were compared to individually matched nonexposed workers (18). The results of this study are summarised in Table 2. For 8 workers, mercury exposure occurred during the manufacture of a mercury-based fungicide and the remainder were exposed to mercury due to its use as an amalgam in gold refining. The results revealed significant impairments in motor and psychomotor functions and in short-term memory for the mercury group compared to the nonexposed group as evidenced by their inferior performance on hand steadiness, visual pursuit, and Sternberg memory tests and the short-term memory component of the paired associates test. Test performance was related to exposure such that workers who were actively using mercury at the time of testing showed the greatest impairments. These results are consistent with earlier findings of increased intentional tremor in workers exposed to inorganic mercury (21) and with the finding of impaired short-term memory (14). Lead exposure. The second study investigated the effect of occupational lead exposure by comparing the test performance of a group of 59 workers exposed to lead with that of an equal number of individually matched nonexposed workers (19). Thirtyone of the lead-exposed group worked in the battery manufacturing industry and the remainder in secondary lead smelting. The mean level of exposure for the group was 2.37 ~mol/1 (standard deviation = 0.64). Most workers had fairly short-term exposure to

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TABLE 3

TABLE 4

SUMMARISED RESULTS FOR A STUDY OF LEAD-EXPOSED WORKERS AND NONEXPOSED CONTROLS ON A RANGE OF NEUROBEHAVIORAL TESTS

SUMMARY OF RESULTS COMPARING PROFESSIONAL SHALLOW-WATER DIVERS AND THEIR CONTROLS FOR A RANGE OF NEUROBEHAVIORAL TESTS

Tests Critical flicker fusion: (mean, s.d., both eyes, Hz/sec) Vigilance: (mean, s.d., No. targets tracked for last 5-min period) Reaction time: (mean, s.d., msec)

Lead-Exposed

Controls

35.46* (4.77)

36.86 (5.23)

306.17" (92.11)

372.34 (79.50)

458.7" (146.5)

408.1 (92.5)

Visual pursuit: (30 rpm, mean, s.d.)

6.57* (3.30)

8.76 (4.60)

Hand steadiness: (last 20 sec test) Off-target touches (mean, s.d.) % time off target (mean, s.d.)

53.78* (15.80) 24.00* (6.90)

40.03 (9.70) 18.90 (7.10)

Sternberg test: (results for lines of best fit) Motor component (intercepts) Positive set (yes) Negative set (no) Cognitive components (slopes) Positive set (yes) Negative set (no) Paired associates (means) Immediate recall Trials to criterion Delayed recall

621.3* 631.49*

513.51 589.35

70.50* 83.30*

61.50 53.97

2.33* 2.88 3.74

3.78 1.75 3.75

*Statistically significant difference (p<0.05) between lead-exposed and control workers.

lead with nearly one-third being exposed for less than 1000 hours. Lead-exposed workers showed poorer performance on all tests with the exception of the long-term memory test (see Table 3). These results are consistent with those of a number of other studies (7,13) which found a range of neurobehavioral deficits in leadexposed workers. No relationship was found in this study between test performance and either measure of lead exposure, length of exposure or magnitude of body burden. The range of exposures was, however, very limited with no lead worker having blood lead levels exceeding the then current threshold limit value of 3.81 ixg/100 ml blood. Underwater exposure. The third case-control study was an investigation of the effects of multiple exposures to the underwater environment over a number of years as experienced by professional abalone divers. A group of abalone divers (n = 33) were compared with an equal number of individually matched nondiving controls (20). The abalone divers were relatively experienced (mean length of exposure = 5,205 hours) but were not exposed to particularly great depth. The mean maximum depth reported for a typical dive was 64.8 feet (s.d. = 16.8), however, most reported suffering decompression sickness, which often involved neurological symptoms, at some time in their diving career.

Tests

Divers

Controls

Critical flicker fusion: (mean, s.d., both eyes, Hz/sec)

34.80* (4.50)

37.70 (4.75)

not tested

not tested

345.20

378.10

not tested

not tested

55.10" (14.20) 21.65" (8.70)

39.70 (9.90) 19.60 (7.60)

Vigilance: Reaction time: (mean, msec) Visual pursuit: Hand steadiness: (last 20 sec of test) Off-target touches (mean, s.d.) % time off target Sternberg test: (results for lines of best fit) Motor component (intercept) Positive set (yes) Negative set (no) Cognitive component (slope) Positive set (yes) Negative set (no) Error (means, s.d.) Paired associates (means) Immediate recall Trials to criterion Delayed recall

468.50* 611.90*

564.20 640.10

66.10" 44.80 1.60" (1.10)

54.70 50.00 0.62 (0.95)

2.00 4.50 2.50

2.00 3.00 3.00

*Statistically significant difference (p<0.05) between divers and their controls.

For this study it was necessary to use a slightly modified version of the test battery due to time constraints. The vigilance and visual pursuit tests were replaced by the digit symbol test from the WAIS (16) and the Bourdon-Wiersma test from the Finnish Institute test battery (6). A summary of the results is shown in Table 4. Abalone divers showed poorer CFF thresholds, poorer hand steadiness, poorer digit symbol performance, were less able to learn new material, and, in the Sternberg memory test, made more errors and showed a lesser ability to cope with increasing memory loads compared to controls. These results are consistent with previous reports of visual effects due to decompression sickness in caisson workers (12) and reports of intentional tremor and poorer memory in divers with known histories of decompression sickness (11). More detailed analysis of the Sternberg test data in this study revealed that divers adopted a strategy of sacrificing accuracy for speed as shown by their increased speed in performing the task but increased error compared to controls. This finding may indicate a difference in approach to task performance in divers. It remains to be shown whether trading accuracy for speed is related to risk-taking attitudes or other properties common to inherently hazardous occupations. The test performance of divers was significantly correlated with their diving experience. Unsafe diving practices was a

TEST BATTERY DEVELOPMENT

513

TABLE 5 COMPARISONOF EFFECTSOF DIFFERENTHAZARDSON NEUROBEHAVIORALFUNCTION Exposure

CFF

VIG

RT

Inorganic Mercury

N.S.

N.S.

N.S.

Inorganic Lead Underwater Environments (Divers)

VP

HS

Steinberg Memory Motor Cognit. Errors

Paired Associates STM Trials LTM N.S.

N.S.

@

~ *

N.S.

N.S. ~

N.S.

[ ] Exposed group significantly different from controls. *Not tested. N.S. = No statistically significant difference. CFF=critical flicker fusion test, VIG=vigilance test, RT=reaction time test, VP=visual pursuit test, HS = hand steadiness test. Sternberg memory: Motor = motor component of test, Cognit. = cognitive component of test, Errors = errors made during test. Paired associates test: STM= immediate recall performance, Trials =trials to criteria, learning measure, LTM = delayed recall performance.

significant predictor of poor test performance. Length of exposure to the underwater environment adversely affected performance only when combined with unsafe practices like not decompressing when returning from depth. In summary, the test battery described here discriminates well between exposed and nonexposed workers. It also discriminates between exposure conditions within exposed groups and thus appears to be of useful sensitivity. The behavioral functions shown to be impaired for each toxic exposure discussed are consistent with findings from previous research.

Specificity: How Well Does the Battery Discriminate Between the Effects of Different Toxic Substances? The next desirable attribute of a useful test battery is its ability to identify specific neurotoxic hazards, that is, differentiate between compounds. Table 5 shows a comparison of the results of each of the studies described above. Each of the exposures produced a characteristic pattern of results. The hand steadiness test was affected across all hazards. Long-term memory was the only test not affected by any hazard. Divers showed a distinct pattern of neurobehavioral effects unlike those produced by the heavy metals lead and mercury. Each of the two heavy metals also produced distinctive patterns of neurobehavioral effects, thus the test battery has the capacity to detect specific toxic effects.

examination of the stage 1 results shows that two different conclusions can be drawn regarding the neurological impairments underlying the observed functional deficits caused by lead. The fact that so many functions were affected by lead exposure suggests that it affects a wide range of neurological processes. The structure of the test battery, however, permits an alternative interpretation. Namely, that since primary visual functions are affected (i.e., CFF), and the nature of stimulus presentation for virtually all tests in the battery is visual, the finding of functional deficits in almost all tests could be explained solely by the effects of lead on visual function. Consequently, a second study of lead exposure is in progress to determine whether lead is a general neurotoxicant, or whether it exerts specific effects on the visual

TABLE 6 TESTS USEDIN SECONDLEVELOF TESTINGFOR THE EFFECTSOF LEAD EXPOSURE Visual Sensory function Snellen test (8) Contrast sensitivity (4) Critical flicker fusion (18) Visual fields test (4)

OUTLOOKFOR USE OF THE TEST BATTERY The long-term utility of this test battery probably will depend on whether it provides data useful in elucidating the nature of neurological damage caused by occupational hazards. As the battery assesses functional status based on a model of information processing, the patterns of the effects of toxicants on test performance can hopefully be used to formulate hypotheses about the neurological substrates involved in toxicant-induced behavioral deficits. We may, therefore, come closer to answering the question of what a particular hazard does to the nervous system. The test battery is currently being employed in a second stage of testing for the effects of lead exposure. The results of the first stage of testing have been described earlier in this paper. Close

Auditory

Screening audiometry (22)

Sensory-motor function Simple auditory reaction time (18)

Simple visual reaction time (18) Memory function

Auditory Sternberg test (15)

Visual Steinberg test (15) Additional:

Buschke Memory test (selected and restricted reminding) (2)

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WILLIAMSON

system. Previous research in both monkeys (1) and humans (3) has shown optic neuropathy following lead exposure and supports the visual system hypothesis. To test this hypothesis, the battery has been developed further to include equivalent forms of the same tests using visual or auditory modalities for stimulus presentation and to include tests of the primary functional status of these two modalities. Equivalent forms of the reaction time, hand steadiness and Sternberg memory tests were also developed and are being used in the ongoing study. The components of the new test battery are summarized in Table 6. The "second level" approach should allow a clearer understanding of how lead affects the nervous system. It should also point the way to more specific tests for functional disturbances due to lead exposure. These might then be used as adjuncts to, or replacements for, the current, perhaps less specific, biochemical tests performed on lead workers. It is likely that for some hazards a second level of testing will not be required to determine the specific neurological deficits underlying an observed neurobehavioral effect. Nevertheless,

results obtained from the test battery may provide the data necessary to allow decisions about further testing to be made. CONCLUSIONS This initial evaluation of the use of a test battery in the behavioral assessment of the effects of exposure to various environmental influences has been very encouraging. We now have some understanding of the effects of some of the major confounding variables on the scores obtained from the battery. The battery not only allows assessment of a range of nervous functions but does so in a systematic way so that relationships between functions can be investigated and used to assess the validity of measurement. The battery discriminates between the effects of different neurotoxicants and therefore can be recommended for use in hazard evaluation in occupational settings. It might also find use in other settings such as in communities where exposure to pollutants has occurred. Finally, it is envisaged that the battery will be of use in categorizing various neurotoxic states and their causes.

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