Journal of Consulting and Clinical Psychology 1978, Vol. 46, No. 5, 913-923

Neuropsychological Stability in Multiple Sclerosis Robert J. Ivnik Mayo Clinic and Mayo Inundation Rochester, Minnesota The neuropsychological performances of 14 patients who had multiple sclerosis (MS) and who received repeated testings spaced over time by at least 1 year were compared with identical evaluations of 14 patients who had neurological involvement but not MS. Subjects in each group were individually matched on chronological age at first testing, length of test-retest interval, sex, and years of formal education. Performance decrements attributable to the demyelination process of MS were primarily manifested on tasks requiring motor proficiency or complex sensory discriminations. Tests of higher order cognitive functions (e.g., abstractions, speech perception) were less adversely affected, except for measures having significant motor components. Preliminary Minnesota Multiphasic Personality Inventory data are also presented. The results indicate relative preservation or only mild deterioration for most intellectual abilities despite worsened motor-sensory functioning.

In recent years, the psychological test performances of patients with multiple sclerosis (MS) have been experimentally differentiated from the performances of either patients with neurological involvement but not MS or normal control patients. Matthews, Cleeland, and Hopper (1970) compared the test scores of 30 patients who had MS with those of a neurological group that excluded MS subjects on an extensive battery of neuropsychological tests and found significantly poorer functioning for the patients with MS on tests that demanded motor skill, speed, and coordination. Reitan, Reed, and Dyken (1971) reported similar findings when patients who had MS were compared with a neurologically normal control group. Reitan et al. also noted less striking but statistically significant defi-

This research was completed while the author was a postdoctoral fellow in clinical neuropsychology at the Neuropsychology Laboratory, University of Wisconsin. The author is particularly appreciative of the assistance provided by J. Preston Harley and Charles G. Matthews during the course of manuscript preparation. Requests for reprints should be sent to Robert J. Ivnik, Department of Psychiatry and Psychology, Mayo Clinic, Rochester, Minnesota 55901.

cits on tests of verbal and auditory perception, measures of incidental recall for geometric figures and spatial relations, and tests of sensory-perceptual alertness. General information, verbal communication, and comprehension measures were least affected by MS. In each study, relatively good preservation of reasoning and logical-analytic skills was apparent. The validity of the studies by Matthews et al. and Reitan et al. is supported by Goldstein and Shelly's (1974) successful partial replication of each. Finally, Beatty and Gange (1977) provided correlative evidence suggesting that memory functions also may suffer the effects of demyelination, but this hypothesis at present is tentative and requires additional experimental verification. MS is a disease manifested by exacerbations and remissions of clinical symptoms associated with a slowly progressive deterioration of general functioning. Even though neuropsychological studies have defined distinguishing behavioral-performance features of the disease, the relationship between the extent of neuropsychological impairment and the clinical progression of the disease has not been described. To approach this question, Ivnik (1978) compared the neuropsychological performances of three groups of patients:

Copyright 1978 by the American Psychological Association, Inc. 0022-006X/78/4605-0913$00.7S

913

914

ROBERT J. IVNIK

Table 1 Neurological Diagnoses of 14 Non-MS Neurological Control Patients alien!

3 4 5 6 7 8 9 10 11 12

13 14

Diagnosis Left cerebral atrophy; history of alcohol abuse Major motor seizures secondary to subarachnoid hemorrhage Posttraumatic syndrome S/P encephalitis Somatosensory-evoked seizures of unknown etiology S/P ncurosurgical repair ol depressed skull fracture S/P neiirosurgical repair of epidural heinatoma S/P skull fracture with cerebral contusion Major motor seizures of unknown etiology Major motor seizures of unknown etiology Parkinson's disease Mixed seizure disorder of unknown etiology Partial-complex seizure of unknown etiology Mild mental retardation; radiculopathy; S/P myasthenic syndrome

Note. MS = multiple sclerosis; S/P = status/post.

those whose duration of MS was 1-5 years, 6-10 years, or greater than 10 years. Neuropsychological tests generated surprisingly few .significant findings. Ivnik observed that the individual rate at which MS progresses is so varied that large-group comparative statistics may be an inappropriate experimental design for examining the disease process. To more rigorously examine the stability of neuropsychological performances over time for patients with MS, the research reported herein contained repeated examinations of the subject population using each patient as his or her own control. Patients with MS who were seen for extensive ncuropsychological examinations on two occasions were compared with a population of patients with non-MS neurological involvement who also received repeated evaluations. Method Subjects The testing protocol of every patient with MS who had received repeated examinations in the

Neuropsychology Laboratory, University of Wisconsin, was reviewed. Only patients with definite diagnoses of MS were considered; patients described as "possible MS," "probable MS," "MS suspect," or in any other equivocal manner were excluded. The referring neurologist's judgment that the diagnosis was certain determined group inclusion. If a patient's diagnosis was equivocal at the time of initial testing but definite when reevaluated, he or she was included for further consideration. A minimal tcslrctcst interval of 1 year was required. Persons not receiving complete neuropsychological evaluations were excluded unless the missing data reflected a patient's physical disability due to the neurological illness. For example, if a patient's manipulative skills were so deteriorated that he or she was unable to perform the test of fine motor coordination, the patient was included in the study and the worst possible score was assigned for the missing lest. If, however, data were missing for reasons unrelated to the ability being assessed (e.g., a patient did not receive the Category Test of nonverbal abstraction abilities because of poor visual acuity), no theoretic data were supplied. There were few instances in which data were supplied, because one criterion for selection in the study was having completed most of the ncuropsychological measures. Determination of the non-MS neurological control group required review of all neuropsychological patient protocols on file. Persons with incomplete lest protocols, only one neuropsychological examination, or primary diagnoses of nonneurological conditions were excluded from further consideration. Each patient with MS was directly matched to a non-MS neurological control patient with regard to sex, chronological age when first tested, education, and number of months between testings. The decision to use only non-MS neurological patients as controls was made to distinguish the stability of MS from that of other neurological disorders. From a clinical viewpoint, a neurological control group comprised of diseases that are most frequently included in the differential diagnoses with MS (e.g., spinal cord lesions) would have been optimal, but practical concerns made this impossible. The final MS and neurological control groups included 14 patients each. Neurological diagnoses of control patients are shown in Table 1.

Neuropsychological Tests The following measures served as dependent variables in this study. Wechsler Adult Intelligence Scale (WA1S). Verbal, Performance, and Full Scale IQs (Wechsler, 1955) were compared for each experimental group. Individual WAIS subtcsl performances also were analyzed. Wide Range Achievement Test (WRAT). Word recognition, spelling, and arithmetic abilities were tested and scored for grade level equivalencies (Jastak & Jastak, 1965).

MULTIPLE SCLEROSIS Category Test. A test of abstraction - concept formation ability using 208 visual stimuli was presented on a screen (Halstead, 1947). The number of errors was recorded. Speech Perception Test, This is an auditory discrimination task in which the subject underlines on an answer sheet one of four nonsense syllables that most closely corresponds to the stimulus presented via a tape recorder (Halstead, 1947). The test was scored for number of errors. Tactual Performance Test ( T P T ) . A 10-block form board was given under a blindfolded condition. Average time (in minutes per block) for three consecutive trials (preferred hand, nonpreferred hand, both hands) was recorded, as was the total time for the three trials. The number of blocks that the subject could recall for shape (memory component) and correct location (location component) on a posttest drawing of the board and blocks was also noted (Halstead, 1947). Trail Making Test. A paper-and-pencil test was given in which on Part A a subject connects as rapidly as possible 25 numbered circles distributed on a sheet of paper (Armitage, 1946). On Part B, half of the circles are numbered and half are lettered, and the subject connects the circles by alternating between these two sequences. The number of seconds to complete each part was the dependent measure. Seashore Rhythm Test. A test of the subject's ability to make same-different discriminations between 30 pairs of rhythmic patterns was presented with a tape recorder (Seashore, Lewis, & Saetveit, 1960). The number of correct responses was recorded. Imperception Test. Standardized examination was given for eliciting tactile, auditory, and visual imperception or suppression (or both) errors (Reitan, 19S9b). Finger Agnosia Test. The patient was required to identify by touch alone fingers of his or her hand after they were lightly touched with a pencil point; 20 trials were given on each hand, and the number of errors was recorded (Reilan, 1959b). Fingertip Number Writing Test. The patient was blindfolded and was required to identify numbers written on his or her fingertips; 20 trials were given on each hand, with the number of errors being noted (Reitan, 1959b). Tactile Form Discrimination Test. The subject identified by touch alone one of four plastic shapes placed in his or her hand, indicating his or her response by pointing to a display panel. Time and error scores were recorded for each hand (Reitan, 1959b). Sandpaper Roughness Discrimination Test. The patient was blindfolded and was presented with four wooden blocks, each of which was covered with a different roughness of sandpaper. The subject was required to arrange (as quickly as possible) the sandpaper blocks in order of increasing roughness. Time and error scores were computed for each hand. Grooved Pegboard Test. A manipulative dexter-

915

Table 2 Means and Standard Deviations of Matching. Variables for MS Group and Non-MS Neurological Control Group Variable Chronological age at first testing Education (years) No. months between testings

MS

Control

38.0 ± 9.28 12. S ± 2.6S

37.0 ±9.32 12.1 ± 2.80

37.0 ± 28.6

34.4 ± 29.7

Note. MS = multiple sclerosis. Sex was directly matched. There were no significant differences. ity task using a pegboard containing 25 holes with randomly positioned slots (Lafayette Instrument Co., Model 4202) was given. Before they could be inserted, the pegs, with an edge along one side, needed to be rotated to match the hole. Time scores were recorded for each hand. Maze Coordination Test. A modified 2706 A Maze (Lafayette Instrument Co.) was placed on a stand in a vertical position at the subject's midlinc. The subject was required to go through the maze with an electric stylus, trying not to touch the sides. The stylus was attached to a time clock and counter. Cumulative time of contact with the maze and cumulative error scores were recorded for each hand. Static Steadiness Test. The subject inserted an electric stylus into the holes of a conventional holetype steadiness test (Lafayette Instrument Co., Model 4605 C). The subject was asked to keep the stylus in each hole for 15 sec. Cumulative time and counter scores were recorded for each hand. Finger Tapping Speed Test. The subject was required to tap (as fast as possible) his or her index finger on a counter apparatus. The mean of five 10sec trials was recorded for each hand (Halstead, 1947). Wisconsin Impairment Index. A composite score was computed for each subject, ranging from 0 to 1.0, based on the frequency with which the subject exceeded specified cutoff points on 10 tests routinely used in the neuropsychological examination. Six of 10 Impairment Index measures were represented by tests from Halstead's battery. The other four measures were (a) time score on Part A plus Part B of the Trail Making Test exceeding the cutoff point suggested by Reitan (1958); (b) two or more definite dysphasic symptoms on a modified and extended version of the Halstead-Wepman Aphasia Screening Test (Halstead & Wepman, 1949) ; (c) distorted reproductions of square, triangle, or Greek cross figures on the Aphasia Screening Test; and (d) occurrence of two or more errors on one body side in tests of tactile finger identification and fingertip number writing perception, or the presence of two or more lateralized errors on sensory imperception testing in tactile, auditory, or visual modalities.

ROBERT J. IVNIK

916 Table 3

Raw Score Descriptive Statistics on All Dependent Measures MS testingFirst Measure WAIS Full Verbal Performance

Control Second SD

M

SD

M

SD

10.8

99.7

10.8 12.8

104.1

13.3 13.4 14.6

98.4 99.4 96.6

15.7 18.6 15.3

100.4 100.9 99.7

15.0 17.4 13.1

2.5 2.8

11.0

2.4 3.1

9.9 10.5 9.7 10.5 9.4 9.7 6.8 9.4 9.8 9.2 8.7

2.6 3.4 4.0 2.8

10.5 10.1

2.6 2.8 4.3 2.9 3.6 3.2 2.0 2.3 3.0 2.4

9.5 7.4 6.0

4.5

SD

103.4 107.7 97.7

94.0

11.5 12.0 11.4 11.1 10.5 11.0 7.5 10.0 9.7 8.8 7.6

3.1

11.5 10.8 10.6 9.2 10.3 5.9 9.9 8.3 8.1 7.7

WRAT (grade level) Reading Spelling Arithmetic

11.8 8.7 7.8

4.2 3.0 2.9

11.3 8.6 7.6

.55 52.3

24.1

24.1 5.8 40.1 94.9

Second

M

M

WAIS subtests Information Comprehension Arithmetic Similarities Digit Span Vocabulary Digit Symbol Picture Completion Block Design Picture Arrangement Object Assembly

Impairment Index Category Test (errors) Seashore Rhythm Test (number correct) Speech Perception (errors) Trails A (seconds) Trails B (seconds)

First

3.2 2.1 1.5 2.6 2.4 1.8 1.6 2.7

.27 3.1 3.4

11.8 32.0

.68 51.1

23.4 6.1 55.6 178.2

3.7 2.7 2.5 2.6 2.6 2.5 3.1 2.3 3.3

3.7

2.8 3.4 .23

21.8 4.2 2.3

29.5 126.7

3.2 3.1 2.2 2.5 3.1 2.4 2.9

2.9 2.9

.23 .64 58.4 20.9

22.2 10.1 56.0 135.4

4.2

7.0 44.7 96.9

10.2 10.6 8.6 10.1 7.3 10.0 9.6 8.0 10.0

9.6 7.2 5.3

2.0

4.3 3.1

1.8

.53 .25 49.4 27.5

22.5 7.9 51.9 137.1

4.1 7.2 22.1 9.1

1.3 1.5 .8 31.4 6.3 3.3

1.2 1.7 1.1 29.0 2.0 2.5

TPT

Dominant (min/block) Nondominant (min/block) Both (min/block) Total Time (minutes) Memory Location Imperception Testing (errors) Tactile Auditory Visual Total Finger Agnosia (errors) Right Left Total

2.3 1.9 2.1

2.4 2.4 3.0

39.1

24.0

5.6 2.8

2.3 2.1

.36 .14 .14 .64

.84 .53

.53 1.15

3.0

3.3 1.6 47.6 5.9 2.1

3.2 3.2 2.5 28.6 1.6 1.4

1.9 1.9 1.8 45.9 5.7 2.1

.64 .86 .86 2.36

1.50 1.75 1.61 3.32

.29 .64 .07 1.00

1.6 1.2 2.79

1.3 1.5

1.8 1.7

1.1 1.4

1.6 2.2

2.79

2.89

2.42

3.34

1.5 2.5 2.6

35.5 2.9

2.4

.27 1.30

.86 .79 .29 1.93

2.9 1.6 3.89

1.2 1.1 2.29

.61 1.22

1.88 2.12 .61

3.87

2.0 2.0 3.75

MULTIPLE SCLEROSIS

917

Table 3 (continued) MS testing First Measure Fingertip Number Writing (errors) Right Left Total Sandpaper (sec) Right Left Total Sandpaper (errors) Right Left Total Tactile Forms (sec) Right Left Total Tactile Forms (errors) Right Left Total

Control First

Second

Second

M

SD

M

SD

M

SD

M

SD

2.9 2.6

5.6 4.1 9.7

6.2 5.6

10.5

2.9 2.0 4.9

2.8 3.9 6.5

2.2 1.1

5.5

4.1 4.0 8.1

3.4

2.8 2.0 4.6

33.7 43.3 78.6

8.2 20.1 30.1

52.7 55.4 109.1

28.0 31.8 70.0

47.9 39.4 90.6

25.0 20.0 51.1

38.6 35.5 71.1

17.0 13.7 30.7

.57 .71 1.28

28.8 31.1 60.1 .57 .86 1.43

0.94 1.68 2.30 23.6 23.1 44.6 .75 2.07 2.47

1.00 1.14 2.14 38.1 40.6 78.7 .79 1.86 2.64

1.30 1.92 3.58

1.14 1.00 2.14

25.7

25.9

28.8 53.2

21.6

1.42 2.63 3.30

47.5 .29 .07 .36

1.87

.57

1.88 3.63

.71 .71

7.3 6.4 13.0 .82 .27 1.08

20.2 17.4 40.6 .07 .00 .64

1.22 1.27 1.27 6.1 5.2 13.8 .27 .00 2.13

Finger Tapping (count) Dominant Nondominant

43.4 36.2

9.0 7.7

37.2 29.8

7.6 10.9

39.7 35.0

10.1 9.0

44.1 38.9

10.2 5.6

Dynamometer (kg) Dominant Nondominant

44.7 38.1

9.0 14.1

39.4 33.8

9.8 15.1

36.7 35.9

11.4 10.6

41.8 37.9

14.2

Pegboard (sec/peg) Dominant Nondominant

4.3 5.9

1.8

5.6 25.6

2.5 40.3

3.8

.9

3.9

4.2

1.2

3.6 4.0

.9 .9

4.31 14.61

4.24 25.65

6.21 22.06

34.01

4.39 6.75

6.57 5.70

2.39 4.65

3.41 6.80

Mazes (sec) Dominant Nondominant Mazes (count) Dominant Nondominant Static Steadiness (sec) Dominant Nondominant Static Steadiness (count) Dominant Nondominant

27.1 106.1 22.62 34.62

109.1 112.1

27.0 253.9 18.00 27.35 75.9 53.3

37.6

182.6 34.93 42.39

139.3 259.7

6.52

36.8 347.7

25.33 30.65

67.7 320.8

15.6

23.3 42.6

38.4

15.9 25.4

18.0 30.2

22.82 32.82

9.36 20.10

23.62 31.91

14.79 19.57

155.9 155.9

24.0

90.5 73.4

126.3 143.7

68.7 64.7

Note. WAIS = Wechsler Adult Intelligence Scale; WRAT = Wide Range Achievement Test; TPT = Tactual Performance Test.

ROBERT J. IVNIK

918 Minnesota Multiphasic (MMPI). Ten patients in pleted the MMPI at each were compared for each scale

Personality Inventory each group also comtesting. Their profiles as a related brief study.

Data Analysis Normative data for many of the above-described tests have been provided by Kiernan and Matthews (1976). The availability of these norms permits the transformation of raw scores on individual tests into T scores (M = 50, SD = 10), thereby providing a mechanism for comparing the experimental subjects' performances against "normal expectation." 7"-scorc conversions also allow for direct comparison of performance levels in various ability domains because raw score measurement units (e.g., kilograms for grip strength, IQ for intelligence) are transformed to a common scale. Further, these conversions provide the opportunity for a graphic display of the lest results. A disadvantage of Kiernan and Matthews' results is that normative data on sensory examinations were not included. The dependent

variables to which the T-score conversions apply include Verbal, Performance, and Full Scale IQs from the WAIS, Wisconsin Impairment Index, Category Test, Seashore Rhythm Test, Trail Making Test, Speech Perception Test, Tactual Performance Test, and all tests of motor-steadiness proficiency. Analyses of variance (ANOVA) ( 2 X 2 ) were computed with repeated measures on the second variable (i.e., testings). On measures for which the ANOVA identified a trend (.OS < p < .10) or a significant difference (p

Neuropsychological stability in multiple sclerosis.

Journal of Consulting and Clinical Psychology 1978, Vol. 46, No. 5, 913-923 Neuropsychological Stability in Multiple Sclerosis Robert J. Ivnik Mayo C...
749KB Sizes 0 Downloads 0 Views