Journal of Clinical and Experimental Neuropsychology

ISSN: 1380-3395 (Print) 1744-411X (Online) Journal homepage: https://www.tandfonline.com/loi/ncen20

Cognitive Decline Following Stroke: A

Comprehensive Study of Cognitive Decline
Following Stroke*

Jacqueline Hochstenbach , Theo Mulder , Jacques van Limbeek , Rogier

Donders & Henny Schoonderwaldt

To cite this article: Jacqueline Hochstenbach , Theo Mulder , Jacques van Limbeek ,
Rogier Donders & Henny Schoonderwaldt (1998) Cognitive Decline Following Stroke:
A Comprehensive Study of Cognitive Decline Following Stroke*, Journal of Clinical and
Experimental Neuropsychology, 20:4, 503-517, DOI: 10.1076/jcen.20.4.503.1471

To link to this article: https://doi.org/10.1076/jcen.20.4.503.1471

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Journal of Clinical and Experimental Neuropsychology 1380-3395/98/2004-503$12.00
1998, Vol. 20, No. 4, pp. 503-517 © Swets & Zeitlinger

Cognitive Decline Following Stroke:

A Comprehensive Study of Cognitive Decline
Following Stroke*
Jacqueline Hochstenbach1,2, Theo Mulder1,2, Jacques van Limbeek1,3, Rogier Donders4, and Henny
Schoonderwaldt2
1Sint Maartenskliniek-Research, Nijmegen, The Netherlands, 2Neurological Institute, University of Nijmegen,
3
Sint Maartenskliniek-Rehabilitation Centre, Nijmegen, and 4Centre for Biostatistics, University of Utrecht,
The Netherlands

ABSTRACT

General insight into the frequency and gravity of cognitive dysfunctions following stroke and its influenc-
ing factors is still lacking. With an extensive neuropsychological battery 229 patients who had suffered a
stroke were assessed. More than 70% of the patients showed a marked slowness of information processing,
whereas at least 40% of all patients had difficulty with memory, visuospatial and constructive tasks, lan-
guage skills, and arithmetic. A significant effect was found for side and type of stroke, gender, and the
presence of aphasia. No significant effect was found for cortical versus subcortical lesions, having one
versus multiple strokes, having lowered consciousness on admission, the presence of risk factors, a paresis
of the hand, or the interval between the stroke and the neuropsychological assessment.

Although stroke is one of the most prominent
neurological disorders, often leading to serious
and long-lasting sensorimotor and behavioral
disabilities, a general insight into the gravity and
frequency of cognitive impairments is still lack-
ing. Such an insight, however, is urgently
needed, first since it is well known that cogni-
tive dysfunctions may hinder functional recov-
ery and rehabilitation (Allen, 1984; Feigenson,
McDowell, Meese, McCarthy, & Greenberg,
1977; Feigenson, McCarthy, Greenberg, &
Feigenson, 1977; Galski, Bruno, Zorowitz, &
Walker, 1993; Novack, Haban, Graham, &
Satterfield, 1987; Sundet, Finset, & Reinvang,
1988; Tatemichi et al., 1994) and second, be-
cause this knowledge is needed for the improve-
ment of long-term disability-oriented care pro-
grams (Hochstenbach, Donders, Mulder, van
Limbeek, & Schoonderwaldt, 1996). However,
to date studies concerning an overall view of the
cognitive consequences following stroke are still
rare. The majority of publications on the neuro-
psychological consequences of stroke focus on
specific cognitive impairments such as neglect,
aphasia, or apraxia. The few studies which con-
cern a more general analysis, however, employ
mostly only short global screening tests, such as
the Mini-Mental State Examination (MMSE;
Galasko et al., 1990) and its variants (Babikian,
Wolfe, Linn, Knoefel, & Albert, 1990; Down-
hill, & Robinson, 1994; Ebrahim, Nouri, &
Barer, 1985; Friedman, 1991; Kappelle, Adams,
Heffner, & Tomer, 1994), the Neurobehavioral
Cognitive Status Examination (NCSE; Galski et
al., 1993; Mysiw, Beehan, & Gatens, 1989) or
the CAMCOG, which is part of the Cambridge

*
This work has been supported by a grant from the Health Research and Development Council, number 281706.
The helpful comments of Patricia Anderson are gratefully acknowledged.
Address correspondence to: Jacqueline Hochstenbach, Sint Maartenskliniek-Research, P.O.Box 9011, 6500 GM
Nijmegen, The Netherlands. E-mail: jh_aro@universal.nl
Accepted for publication June 18, 1998.
504 JACQUELINE HOCHSTENBACH ET AL.
Examination for Mental Disorders of the Elderly
(CAMDEX; Kwa et al., 1996). The value of
these studies is limited, because little insight can
be gained about the diversity and complexity of
the dysfunctions (Wade, 1993).
The aim of the present paper is twofold: (1) to
present an explorative, descriptive overview of
the frequency and severity of cognitive changes
which may take place after stroke, and (2) to
detemine whether a relationship exists between
the gravity of the dysfunctions and variables
such as anatomic location, type of vascular le-
sions, number of strokes, gender, aphasia, and
lowered consciousness on admission.
METHOD
Participants
The protocol was approved by the Medical Ethics
Board of each participating hospital, and all partic-
ipants gave their informed consent for the study. In
total 229 patients participated in the present study.
They were recruited from patients consecutively
admitted between September 1992 and August
1995 to three different hospitals in the Nijmegen
area: a university hospital, a rehabilitation centre,
and a regional hospital. Univariate analyses of
variance were used to investigate potential con-
founding by hospital: none of the analyses showed
significant differences. Patients were between 18
and 70 years of age, with the diagnosis of a stroke
confirmed by computed tomography of the brain.
By imposing an age limit of 70 years, the effects of
aging on cognitive functioning have been reduced.
Patients were excluded when they suffered from
any other major physical illnesses (life-threaten-
ing, neurological, or disabling diseases) or mental
disorders (under psychiatric treatment in the last
10 years), or when a reliable assessment of neuro-
psychological functions was not possible (e.g., in
patients with a persistent impairment in conscious-
ness like drowsiness). Aphasic patients were only
excluded if they were not able to respond ade-
quately to ‘yes’ or ‘no’ questions.
Sensory deficits, reflex pathology, or lowered
consciousness were scored on basis of the medical
reports, all at the time of admission in the acute
phase. The Medical Research Council scale (MRC;
Wade, 1992, p. 53) was used to determine the de-
gree of strength of the hands, arms, and legs. Be-
cause the interrater reliability of the MRC scale is
low and the interpretation of the scores indicating
degree of impairment is open to debate (Dvir,
1997), the 6-point scale was recoded to only distin-
guish between normal and affected muscle
strength. The number of previous strokes as well
as a series of risk factors were scored. Stroke char-
acteristics were determined by the CT scans. This
resulted in a group of 229 patients (140 men and
89 women) with a mean age of 55.9 years (SD =
11.19) and a mean educational level of 4.1 years
(SD = 1.5) (see Appendix). The mean interval be-
tween stroke and the neuropsychological assess-
ment was 72.2 days (SD = 49.7, range 5–293
days). Further clinical data of these patients are
presented in Table 1.
Because not all neuropsychological tests have
norms adequately stratified for age, a group of
healthy controls (n = 33) was included as a refer-
ence sample. The control group consisted of volun-
teers from the community (n = 18) and spouses of
stroke patients (n = 15). There were 12 males and
21 females. Mean age was 52.4 years (range 25-
73), with a mean level of education of 4.4 years
(SD = 1.5). None of the controls suffered from any
neurological or psychiatric illness. Five controls
were under medical treatment at the time of assess-
ment: one was being treated by an orthopedic sur-
geon; two by a lung specialist; and two had re-
cently visited both an internist and an ophthalmol-
ogist.
Neuropsychological Assessment
The following neuropsychological ‘‘domains’’
were assessed: orientation, memory, attention and
concentration, visuospatial and visuoconstructive
functions, language, and arithmetic.
For detailed information concerning the admin-
istered tests, the reader is referred to Lezak (1995).
In the present paper only a global description of
the tasks is given.
Orientation was determined by questions about
time, length of time, place, and person.
Memory performance was evaluated using the
Dutch version of the Rey Auditory-Verbal Learn-
ing Test (AVLT; Rey, 1964), the Wechsler Adult
Intelligence Scale (WAIS; Stinissen, Willems,
Coetsier, & Hulsman, 1970; Wechsler, 1955) In-
formation and Digit Span subtests, and the
Rivermead Behavioural Memory Test (RBMT;
Wilson, Cockburn, & Baddeley, 1985; Wilson,
Cockburn, Baddely, & Hiorns, 1989). From the
AVLT the scores for immediate recall, delayed
recall, and recognition were used. WAIS Informa-
tion subtest was used for examining (the reproduc-
tion of) general knowledge. The Digit Span sub-
test, which comprises two different tests (digits
forward and digits backward), reflects the memory
 COGNITIVE DECLINE FOLLOWING STROKE 505

Table 1. Clinical Data for 229 Stroke Patientsa.

n %
Stroke description
Type
Infarct 199 (86.9%)
Hemorrhage 130 (13.1%)
Side
Left 114 (49.8%)
Right 103 (45%)
Both 110 (4.4%)
Not applicable 112 (0.9%)
Brain
Cortical 137 (59.8%)
Subcortical 182 (35.8%)
Both 118 (3.5%)
SAHb 112 (0.9%)
Previous stroke 136 (15.7%)
Affected sensory system 198 (42.8%)
Affected reflexes 134 (58.7%)
Lowered consciousness 142 (19.3%)
Paresis
Arm 195 (85.2%)
Hand 192 (83.9%)
Leg 184 (80.3%)
Facialis 146 (63.8%)
Risk factors
Heart disease 152 (22.3%)
Atrial Fibrillation 114 (25.9%)
Myocardial infarction 122 (40.7%)
Other 118 (33.4%)
Vascular disease 170 (30.6%)
Carotic stenosis 131 (43.7%)
Hypercholesterolemia 111 (15.5%)
Arteriosclerosis 116 (8.5%)
AV malformation 115 (7.0%)
Other 118 (25.3%)
Diabetes mellitus 123 (10%)
Hypertension 168 (29.7%)
Contraception 110 (4.4%)
Obesity 112 (5.2%)
Smoking 170 (30.6%)

Note. SAH = Subarchnoid Hemorrhage; AV malformation = Arterio-Venous Malformation.

span of immediate verbal recall. The RBMT,
which consists of ecologically relevant tasks such
as remembering a newspaper article, a route, a
name, or an appointment, provides information
about the effects of impaired memory on activities
of daily life.
Attention was investigated with the Trail Mak-
ing Test, Parts A and B (TMT-A, TMT-B; Reitan,
1958) which involves motor speed and agility, and
the WAIS Digit Symbol subtest which involves
sustained, focused attention, and directed visual
shifting. For testing visual inattention a letter can-
cellation task, which according to Halligan and
Robertson (1994) is one of the most sensitive mea-
sures of neglect, was used, as well as one photo-
graph from the Picture Scanning subtest of the
Behavioural Inattention Task (BIT; Wilson, Cock-
burn, & Halligan, 1987). The scoring of the TMT-
A and TMT-B was slightly modified in order to
control for differences in response times and cor-
506 JACQUELINE HOCHSTENBACH ET AL.
rections made by the patient. Therefore, the num-
ber of correct connections made by the patients
was scored in addition to the time score.
Visuospatial and visuoconstructive functions
were assessed by the WAIS Block Design subtest,
the Bobertag (Bobertag, 1914; Karpov, Luria, &
Yarbuss, 1968), a structured clock test (with dif-
ferent levels of difficulty), a clock-drawing task
(Freedman, 1991), the copying task of the BIT, and
by Money’s Road Map Test (Money, 1976) for
left-right orientation. The Bobertag shows a draw-
ing of a complex social situation for which the par-
ticipant has to construct a logical story. The struc-
tured clock test consists of two parts: in the first
part the patient has to set the time in five circles
(clocks). In the second part the time has to be read
from 20 clocks which have a decreasing level of
difficulty. The first 5 clocks have only the two
hands, the next 5 clocks have markings for the
quarter hour, the following 5 clocks have markings
for every 5 minutes, and finally 5 digital clocks
were shown. For aphasics, a multiple choice ver-
sion was available.
Language was evaluated with the Similarities
subtest from the WAIS and several subtests from
the Dutch Aphasia Society (SAN; Deelman,
Liebrand, Koning-Haanstra, & van den Burg,
1987), concerning word comprehension, sentence
comprehension, verbal fluency (in the category
‘animals’), and naming. The Similarities subtest is
a test of verbal concept formation and provides a
sensitive measure of abstract thinking. When pa-
tients named a difference instead of a similarity,
they were given another chance instead of record-
ing an incorrect response. Different aspects of
writing were assessed as well. Only the results of
the task about writing-on-command have been
used in the present article as the other tasks (spon-
taneous writing and copying) were highly corre-
lated with this test (respectively, r = .88 and r =
.95). In order to decide whether writing was af-
fected or not, qualitative aspects such as scrib-
bling, spatial disorders, agrammatisms, spelling,
and other linguistic errors were taken into account.
Arithmetic skills were assessed by different as-
pects of handling money: recognizing, counting,
and arithmetic.
Testing length was tailored to the individual
abilities of the patients. This generally resulted in
three testing sessions to complete the assessment,
in order to avoid fatigue interference.
RESULTS
Table 2 gives a general overview of the tests
employed as well as the mean scores and the
standard deviations for the patients and the con-
trols. The stroke patients as a group have lower
scores indicating poorer performance than con-
trols. On almost all tests the performance of the
stroke patients differs from the performance of
the controls. The only exceptions are the WAIS
Information subtest, the immediate recall of a
story, the number of correct connections of
TMT-A, the picture scanning task, the clock
test, word comprehension, and recognizing
money. On these tests the scores differ only
minimally from the scores of the controls.
Table 2 gives only a general overview of the
mean scores, and therefore no insight is given
into the number of patients performing less well
and also no answer is given to the question
whether there is a relevant problem or not. In
Table 3 the percentage of patients with a prob-
lem are listed for each test. The percentages are
expressed in terms of statistical relevance as
well as in terms of clinical relevance. For statis-
tical relevance, the scores of the patients were
standardized into z scores by using the mean and
the standard deviation of the control group. A
standardized score of –2 (or 2 in those cases
where a higher score indicates a worse perfor-
mance), was taken as a cutoff point; that is, test
results which differed by more than 2 SDs from
the results of the controls were seen as clearly
pathological. However, a clinical criterion was
also employed, that is, the 15th percentile score
of the control group. Thus, all patients whose
scores fall below the 15th percentile of the con-
trol group (or above the 85th percentile score in
cases where a higher test score indicates a worse
performance) are classified as patients with a
deficit on that test.
From the percentages of dysfunction in the
15th percentile, it can be inferred that slowness
of information processing forms the main prob-
lem, that is to say, about 70% of the patients
showed difficulties in performing adequately
under conditions of time pressure (as can be de-
rived from the time scores on Tests 13, 15, 16,
17, 21 in Table 3). Even when using the more
 COGNITIVE DECLINE FOLLOWING STROKE 507

Table 2. Performance of Stroke Patients and Controls on Neuropsychological Tests.

Patients Controls

Measures n M SD n M SD
a
Orientation (0–4) 216 .36 .78 33 0 .00
Memory
AVLT immediate recall (0–75) 194 32.53 10.98 33 43.79 12.04
AVLT delayed recall (0–15) 191 6.08 3.34 33 9.76 3.43
AVLT recognition (0–15) 186 26.99 3.04 32 28.47 3.13
WAIS Information (0–22) 207 9.77 5.26 33 11.24 5.08
WAIS Digit Span (0–24) 213 9.02 3.56 32 11.72 2.40
Forward (0–12) 199 4.87 2.18 32 5.78 1.86
Backward (0–12) 199 4.10 1.97 32 5.94 1.41
RBMT profile score (0–24) 204 17.67 4.33 33 20.76 2.77
Story immediate recall (0–21) 205 6.65 3.82 33 7.65 3.48
Story delayed recall (0–21) 205 4.81 3.58 33 6.48 3.83
Attention
TMT-A correct (0–24) 222 23.59 2.02 33 23.97 .17
TMT-A time in s 223 86.34 55.84 33 39.03 14.82
TMT-B correct (0–24) 184 17.28 7.93 33 22.06 6.06
TMT-B time in s 185 203.28 133.09 33 84.21 31.96
WAIS Digit Symbol (0–115) 211 27.36 15.20 33 46.73 14.17
Letter cancellation
Time 220 166.75 99.16 32 88.03 27.36
Omissions left 221 2.57 4.40 33 .24 .50
Omissions right 221 1.47 2.85 33 .33 .85
Picture scanning (0–3) 222 2.49 .82 33 2.55 .56
Visuospatial/constructive
WAIS Block Design (0–26)
With time limit 225 7.51 5.49 33 17.39 5.78
No time limit 165 11.36 6.36 33 20.03 6.52
Bobertag (– 20–35) 200 14.48 7.07 33 18.06 6.36
Clock test (0–20) 222 15.65 9.11 32 18.19 1.23
Clock drawing (0–10) 223 7.82 2.42 32 9.75 .62
Copying (0–19) 222 11.73 3.87 33 15.67 2.31
Money’s Road Map
Time 197 129.4 79.97 32 79.19 41.27
Defaults (0–32) 197 7.65 5.96 33 4.85 5.14
Language and arithmetic
WAIS Similarities (0–26) 199 11.25 6.40 32 15.75 5.36
Word comprehension (0–18) 222 17.75 1.09 33 18 .00
Sentence comprehension (0–45) 222 42.36 4.31 33 44.64 .90
Verbal fluency (0–54) 219 21.52 10.52 33 33.58 6.42
Naming (0–18) 218 16.5 4.00 33 18 .00
Writing (0–1) 213 .33 .47 33 .03 .17
Recognizing money (0–12) 223 11.78 1.03 33 12 .00
Counting money (0–10) 223 8.85 2.13 33 9.94 .35
Arithmetic with money (0–20) 212 14.25 6.00 33 17.82 2.72

Note. AVLT = Auditory-Verbal Learning Test; WAIS = Wechsler Adult Intelligence Scale; RBMT = Rivermead
Behavioural Memory Test; TMT = Trail Making Test.
a
Numbers in parentheses indicate range of possible scores.
508 JACQUELINE HOCHSTENBACH ET AL.

Table 3. Percent of Stroke Patients Falling below 2 Standard Deviations or the 15th Percentilea.

Measures 2 SD 15th percentile

Orientation
1. Totalb –d –
Memory
2. AVLT Immediate recall 13.9 31.4
3. AVLT delayed recall 20.9 47.5
4. AVLT recognition 11 26.7
5. WAIS Information 4.4 20.3
6. WAIS Digit Span 34.7 50.2
7. Forward 14.1 34.6
8. Backward 40 58.5
9. RBMT 31.9 42.6
10. Story immediate recall 8.3 34.6
11. Story delayed recallc – 38.3
Attention
12. TMT-A correctb –e –
13. TMT-A time 50.2 68.2
14. TMT-B correct 25 56.2
15. TMT-B time 56.4 71.4
16. WAIS Digit Symbol 29.9 69.7
Letter cancellation
17. Time 51.4 72.3
18. Omissions left 35 49.5
19. Omissions right 26.2 43.9
20. Picture scanning 10 17.7
Visuospatial/constructive
WAIS Block Design
21. With time limit 46.7 80.2
22. No time limit 23.6 75.2
23. Bobertag 14 34.2
24. Clock test 46 50.5
25. Clock drawing 58.7 62.3
26. Copying 49.1 62.6
Money’s Road Map
27. Time 25.4 42.6
28. Defaults 15.2 34
Language and arithmetic
29. WAIS Similarities 25.1 41.1
30. Word comprehensionb –f –
31. Sentence comprehension 39 41
32. Verbal fluency 49.3 67.3
33. Namingb –g –
34. Writingb –h –
35. Recognizing moneyb –i –
36. Counting moneyb –j –
37. Arithmetic 30 46.1

Note. AVLT = Auditory-Verbal Learning Test; WAIS = Wechsler Adult Intelligence Scale; RBMT = Rivermead
Behavioural Memory Test; TMT = Trail Making Test.
a
Based on standardized residual scores.
b
For these tests almost all controls had a perfect score (see also Table 2), so it was not possible to determine
either correct SD or percentile scores.
c
Due to large variation in the scores of the control group it was not possible to obtain a score that would be 2 SD
lower than the mean of the group
d
22.2% of the patient group had a less than perfect score.
e
13.1% of the patient group had a less than perfect score.
f
10.4% of the patient group had a less than perfect score.
g
22.5% of the patient group had a less than perfect score.
h
32.9% of the patient group had a less than perfect score.
i
8.5% of the patient group had a less than perfect score
j
33.6% of the patient group had a less than perfect score.
 COGNITIVE DECLINE FOLLOWING STROKE
rigorous statistical cutoff criterion, more than
50% of the patients showed impairments in this
cognitive domain. Furthermore, the data show
clear attentional deficits. Left-sided neglect was
found in 50% (Test 18 in Table 3), and even
right-sided neglect was prominent (Test 19).
From the figures for other cognitive processes, it
can be concluded that at least 40% of all patients
had difficulty with visuospatial and constructive
tasks (Tests 21–28) and with language skills and
arithmetic. In the language domain especially
verbal fluency (Test 32) seems to cause diffi-
culty. The least affected domain seems to be
memory, but even there at least 30% showed a
significantly poorer performance than the con-
trols. Furthermore, results show that long-term
memory seems to be more affected than does
short-term memory (Test 3 vs. 2, 11 vs. 10) and
that recognition is least affected (Test 4). The
RBMT (Test 9) shows that 42.6% had difficulty
remembering everyday information.
Influence of Clinically Relevant Variables
Only the tests on which the stroke patients
performed less well than the controls were
taken as a starting point for further statistical
analysis. Orientation and writing were excluded
because of a ‘‘ceiling effect’’, caused by the fact
that the scores obtained by the patient group
were close to the perfect score. The test results
that were analyzed further were: the scores on
the AVLT immediate and delayed recall, WAIS
Digit Span, RBMT, TMT-A, TMT-B, WAIS
Digit Symbol, letter cancellation, WAIS Block
Design (with time limit), Bobertag, clock draw-
ing, copying, Money’s Road Map, WAIS Simi-
larities, sentence comprehension, verbal fluency,
and arithmetic with money. The results were
divided into two data clusters: a cluster derived
from tests where a verbal response was needed,
and a cluster derived from tests where such a
verbal response was not required. This was done
because a joint analysis of all tests would lead to
the undesirable effect that aphasic patients
would be dropped from the analysis because
they were not able to complete the tests requir-
ing a verbal response. Moreover, this grouping
of tests allows us to study the influence of apha-
sia on the ‘‘nonverbal response’’ tests. The
509
‘‘verbal response’’ tests were the AVLT,
RBMT, TMT-A, TMT-B, Bobertag, Money’s
Road Map, WAIS Similarities, sentence com-
prehension, verbal fluency, and arithmetic with
money. The TMT is included in the ‘‘verbal re-
sponse’’ tests because knowing the alphabet is a
sine qua non for the completion of the test. The
‘‘nonverbal response’’ tests were WAIS Digit
Span, letter cancellation, WAIS Block Design,
clock drawing, copying, and WAIS Digit Sym-
bol.
The MANOVA procedure from SPSS was
used to analyze the influence of a number of
variables. In both the analyses the educational
level and the age of the patients were used as
covariates. Although educational level is scored
on an ordinal scale, we chose to use it here as if
it was an interval one. There were 11 indepen-
dent variables:(1) gender, (2) type of stroke (in-
farct or hemorrhage), (3) side of stroke (left or
right), (4) cortical or subcortical stroke, (5) the
interval between the stroke and the neuropsy-
chological assessment (NPA), (6) single or mul-
tiple strokes, (7) level of consciousness on ad-
mission in the hospital, (8) inclusion in high risk
group (heart disease, vascular disease, diabetes,
hypertension, smoking), (9) presence or absence
of paresis of the hand (based on the scores on
muscle strength: affected or not), (10) presence
of receptive aphasia, or (11) an expressive apha-
sia. The variable ‘‘receptive aphasia’’ was based
on the scores for sentence comprehension,
which were dichotomized; the variable ‘‘expres-
sive aphasia’’ was based on the scores on verbal
fluency. These last two independent variables
were used only in the analysis of the results ob-
tained with the nonverbal response tests. The
interval between the stroke and the time of as-
sessment (variable 5) was divided into four cate-
gories: 3 to 37 days (n = 57), 37 to 70 days (n =
57), 70 to 95 days (n = 57), and more than 95
days (n = 58).
The effect of these independent variables was
tested in two multivariate analyses, one for the
tests which involved verbal responding, and one
for the nonverbal response tests. Because the
large number of possible interactions would
clearly hinder the adequate interpretation of the
results, only the main effects will be examined.
510 JACQUELINE HOCHSTENBACH ET AL.
The residual variance was used as the error
term.
Table 4 shows the significant results of the
multivariate analysis of the verbal response tests
(vr), whereas Table 5 shows the results of the
nonverbal response tests (nvr). Those variables
that proved to be significant in the univariate
tests are reported as well, together with the
means of the different patient groups.
The analysis of the vr tests shows that only
gender and the side of the stroke had a signifi-
cant multivariate effect. The analysis for gender
indicates that women performed better on mem-
ory tasks, but that men performed better than
women on visuospatial tasks. Performance was
better after right-sided lesions than after left-
sided lesions with the exceptions of WAIS
Block Design and the letter cancellation. The
analysis of the nvr tests showed a significant
effect for the type and the side of stroke. For the
vr tests no significant difference was found for
the type of stroke (F (14, 92) = .92, p = .543).
The results of the nvr tests further show a better
performance for three tests after an infarction
compared to the performance following a hem-
orrhage. Furthermore, no significant effect of
gender on the results of the nvr-tests was found
(F (8, 135) = 1.48, p = .171). The data also show
that aphasia had a disruptive effect on test per-
formance, even on tests where verbal responding
played a minor role.
No significant effect on neuropsychological
test scores was found for cortical versus subcor-
tical lesions (vr: F (14, 92) = 1.76, p = .058; nvr:
F (8, 135) = 1.04, p = .413), the interval between
stroke and NPA (vr: F (42, 272) = 1.26, p =
.145; nvr: F (24, 401) = 1.12, p = .314), single
versus multiple strokes (vr: F (14, 92) = 1.48, p
= .131; nvr: F (8, 135) = .53, p = .836), lowered
consciousness on admission (vr: F (14, 92) =
.81, p = .657; nvr: F (8, 135) = .97, p = .460),
the presence of risk factors (vr: F (14, 92) =
1.02, p = .443; nvr: F (8,135) = .95, p = .480), or
a paresis of the hand (vr: F (14, 92) = .95, p =
.505; nvr: F (8, 135) = 1.35, p = .226).
DISCUSSION
The main purpose of the present article is to give
a comprehensive overview of the gravity and
frequency of cognitive changes following
stroke. The data clearly show that stroke has a
massive effect on many cognitive processes.
Tatemichi et al. (1994), who defined failure by
a cutoff score in the fifth percentile (comparable
to 1.65 SD, which is less rigorous than the statis-
tical criterium chosen in this study), had basi-
cally the same results, although the percentages
of dysfunction in their study were lower. What-
ever the cutoff, the present data show that the
effects of stroke upon cognitive functioning lead
to far-reaching and dramatic changes, with a
general slowing in information processing and
attentional deficits being the most prominent.
The question now becomes relevant whether the
reduced performance on other tasks can be seen
as a consequence of this general slowing. Al-
though it seems plausible to assume that slow-
ness of information processing as a nonspecific
deficit will have some effect on other test re-
sults, it cannot explain the full range of deterio-
ration, as the present data reveal that, even with-
out time limits, patients with a stroke still have
considerable problems performing adequately
on a number of tests. Not only the effect of
slowness of information processing, but the ef-
fect of motor problems on neuropsychological
test performances, should be further elaborated.
The fact that we found no effect of hand paresis
does not mean that there is no such effect. Per-
haps it is a consequence of the relatively crude
measure (Dvir, 1997) and the use of a more sen-
sitive measure like the Purdue Pegboard might
indicate that some of the results are reflective of
motor disability required in task performance.
The distinction we made between tests requir-
ing a verbal response and tests requiring no such
response may seem a bit arbitrary since in fact
each test requires some involvement of language
(e.g., understanding the instructions). However,
although this division has its shortcomings, it
does offer the opportunity to analyze the results
of aphasic patients who otherwise would have
been omitted from the sample because of unob-
tainable data. Hence, the data of an important
Table 4. MANOVA Results for Verbal Response Tests, with Univariate Analyses to Indicate Significant Difference

Independent n F df p Univariate F df p M n M n
variables
Gender 119 4.50 14, 92 .000 1, 105 Male 71 Female 48

AVLT immediate recall 15.62 .000 31.08 37.69

AVLT delayed recall 14.29 .000 5.48 7.56
Money’s Road Map time 5.17 .025 106.31 137.46
Money’s Road Map de- 10.30 .002 5.11 8.25
faults

COGNITIVE DECLINE FOLLOWING STROKE

Side of the stroke 119 2.94 14, 92 .001 1, 105 Left 46 rRght 73

RBMT profile score 6.52 .012 17.17 19.14

AVLT immediate recall 15.90 .000 29.09 36.68
AVLT delayed recall 6.82 .010 5.24 7.00
WAIS Similarities 5.13 .026 11.41 13.48

Note. AVLT = Auditory-Verbal Learning Test; RBMT = Rivermead Behavioural Memory Test; WAIS = Wechsler Adult Intelligence Scale.

511
 512
Table 5. MANOVA Results for Nonverbal Response Tests, with Univariate Analyses to Indicate Significant Difference.

Independent n F df p Univariate F df p M n M n
variables

Type 158 2.46 8, 135 .016 1, 142 Infarct 138 Bleed- 20

ing
WAIS Block Design w.t.l. 10.47 .002 8.22 5.00
copying 10.44 .002 12.18 9.65
WAIS Digit Symbol 11.87 .001 27.44 20.25

Side of the 158 3.92 8, 135 .000 1, 142 Left 73 Right 85

stroke

JACQUELINE HOCHSTENBACH ET AL.

WAIS Digit Span 14.57 .000 7.62 10.12
letter cancellation o.l. 14.24 .000 1.37 3.65
WAIS Block Design w.t.l. 12.85 .000 8.82 6.94

Receptive 158 3.92 8, 135 .000 1, 142 Yes 92 No 66

aphasia
letter cancellation o.l. 13.78 .000 3.47 1.39
latter cancellation o.r. 8.57 .004 1.99 .44
WAIS Block Design w.t.l. 16.72 .000 6.09 10.21
clock drawing 13.61 .000 7.33 9.05
copying 8.27 .005 10.96 13.12
WAIS Digit Symbol 11.06 .001 22.67 31.91

Expressive 158 2.96 8, 135 .004 1, 142 Yes 75 No 83

aphasia
letter cancellation o.r. 8.28 .005 2.12 .64
WAIS Digit Symbol 22.14 .000 20.61 31.88

Note. WAIS = Wechsler Adult Intelligence Scale; w.t.l = with time limit; o.l. = omissions left; o.r. = omissions right; WAIS.
 COGNITIVE DECLINE FOLLOWING STROKE
subgroup of patients could be analyzed, showing
an overall effect of aphasia on the test results.
The rather general character of the cognitive
decline needs some further discussion. Indeed,
at first sight it may seem remarkable that the
relation between type of stroke, number and lo-
cation of strokes on the one hand, and the fre-
quency and gravity of cognitive disorders, on
the other hand, is so weak. However, as early as
1966 Luria indicated that higher mental func-
tions are the result of a complex and dynamic
interaction between a number of brain structures
united in functional systems and that these struc-
tures make their own contribution to the dy-
namic whole. A cognitive function, therefore,
should not be understood in terms of being a
direct property of a specialized group of cells,
located at a certain ‘‘spot’’ in the brain, but as
the end result of dynamic neural networks,
territorially scattered throughout the brain (for a
recent discussion see Alexandrov & Jarvilehto,
1993). This is an important argument, still rele-
vant for modern neuropsychology as it under-
scores the dynamic and integrated character of
the cerebral cortex. Many of the results of the
present study can be explained in light of these
arguments. Comparable results have been re-
ported by Hom and Reitan (1990) who came to
the same conclusion as Luria: Neuropsychologi-
cal functioning is dependent on the overall gen-
eral integrity of the brain (see also Lezak, 1995).
Table 5 shows that aphasia has a far-reaching
impact on general cognitive functioning. In light
of the above-mentioned arguments on the inte-
grated character of the brain, these results are
less striking. In accordance with Luria (1966),
language should be considered as the means by
which all other mental functions can be articu-
lated; no single complex form of human mental
activity can take place without the direct or indi-
rect participation of speech. Speech activity,
therefore, should not be limited to the processes
related to verbal communication, but should be
seen as a ‘‘higher regulator of human behav-
ior’’, enabling us to make abstractions and gen-
eralizations, or to encompass relationships and
associations between objects and events extend-
ing far beyond the limits of direct sensory per-
ception. Hence, the ‘‘linguistic organization’’ of
513
mental processes should be considered as the
combined work of both hemispheres.
During the last two decades a growing inter-
est can be observed in the relationship between
subcortical structures and cognitive processes.
Research in degenerative diseases like Parkin-
son’s and Huntington’s disease have shown that
subcortical structures are involved in a number
of cognitive processes. To our knowledge, little
or no research has been devoted to the differ-
ence between the effect of subcortical versus
cortical strokes on cognitive functioning. In the
present study no significant difference between
subcortical and cortical strokes was found.
However, more studies are needed to determine
the robustness of these findings.
We wanted to determine whether relevant
variables could be isolated with a predictive
‘‘power’’ for cognitive functioning. Most of
these independent variables have been distilled
from the literature on functional recovery. It has
been shown, for example, that functional out-
come following infarction is better than after
hemorrhage (Abu-Zeid, Choi, Hsu, & Maini,
1978; Allen, 1984; Bamford, Sandercock, Den-
nis, Burn, & Warlow, 1990; Bonita, Ford, &
Stewart, 1988; Foulkes, Wolf, Price, Mohr, &
Hier, 1988). De Haan, Limburg, van der
Meulen, Jacobs, and Aaronson (1995), however,
found no such difference for quality of life when
comparing patients with infratentorial infarc-
tions with those with hemorrhages, whereas
Mori, Sadoshima, Ibayashi, Iino, and Fujishima
(1994) found that the type of stroke did not in-
fluence the degree of cognitive dysfunctioning.
The present study indicated that only the results
of 3 of the 22 (sub)tests showed a significant
difference in favor of the infarction, which
raises the question whether it is correct to con-
clude that, in general, cognitive functioning af-
ter infarction is better than following hemor-
rhage.
Desmond, Tatemichi, Paik, and Stern (1993)
have shown that the presence of vascular risk
factors (like diabetes mellitus and hypercholes-
terolemia) in a stroke-free cohort of elderly per-
sons leads to cognitive decline. Furthermore, it
has been shown that vascular risk factors are
negative predictors for survival and functional
514 JACQUELINE HOCHSTENBACH ET AL.
recovery after stroke (Anderson, Jamrozik,
Broadhurst, & Stewart-Wynne, 1994; Lai, Alter,
Friday, & Sobel, 1995; Olsson, Viitanen,
Asplund, Eriksson, & Hagg, 1990; Sacco, Wolf,
Kannel, & McNamara, 1982). Although for
functional or sensorimotor recovery these risk
factors may play an important role, the present
study indicates that for the cognitive outcome
these risk factors have no significant influence.
Although several studies (Anderson, Boure-
strom, Greenberg, & Hildyard, 1974; Boure-
strom, 1976; Jongbloed, 1986; Katz, Ford,
Chinn, & Newill, 1966; Rankin, 1957) reported
that for functional recovery a previous stroke
was an adverse prognostic indicator, this finding
could not be confirmed for cognitive function-
ing. Finally, in studies about recovery it has also
been shown that during the first few months
most patients with stroke show considerable re-
covery of function, although the exact extent
and duration of this recovery is less certain
(Feigenson, McDowell, et al., 1977; Feigenson,
McCarthy, et al., 1977, Ferrucci et al., 1993;
Kotila, Waltimo, Niemi, Laaksonen, & Lem-
pinen, 1984; Ogden, Mee, & Henning, 1993;
Wade, Wood, & Langton Hewer, 1985, 1988).
In the present study, however, no significant
difference in cognitive functioning between pa-
tients who were assessed at different poststroke
intervals was found. Nevertheless, caution
should be taken, because it might well be that
the cognitive impairment observed in this study
would not be present to this extent, especially in
those patients who were tested soon after their
stroke. Moreover, it would be interesting to ex-
plore the extent of recovery at a 1- or 2-year fol-
low-up.
In summary, the results of this study show an
extensive general decline in cognitive function-
ing following stroke. The implication of the re-
sults for neurological rehabilitation are clear:
Focusing too much on specific problems can
lead to the underestimation of the general effects
of a brain lesion, which may hinder the design of
an optimal rehabilitation process.
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 COGNITIVE DECLINE FOLLOWING STROKE 517

APPENDIX

Dutch Educational System.

Level Years of education

1 (< 6 years elementary school)
2 6
3 8
4 9
5 10-11
6 12-18
7 (university) > 18