ORIGINAL ARTICLE

Post-stroke cognitive impairment is common even after successful

clinical recovery
H. Jokinen, S. Melkas, R. Ylikoski, T. Pohjasvaara, M. Kaste, T. Erkinjuntti and M. Hietanen

Clinical Neurosciences, Neurology, University of Helsinki and Helsinki University Hospital, Helsinki, Finland
EUROPEAN JOURNAL OF NEUROLOGY

Keywords:
cognition, cognitive
impairment,
neuropsychology, stroke
Received 20 January 2015
Accepted 6 April 2015
European Journal of
Neurology 2015, 22:
1288–1294
doi:10.1111/ene.12743
Background and purpose: Cognitive impairment is common after stroke, but
the prevalence and long-term significance of the diverse neuropsychological
deficits on functional outcome are still not well known. The frequency and
prognostic value of domain-specific cognitive impairments were investigated in
a large cohort of ischaemic stroke patients.
Methods: Consecutive patients (n = 409), aged 55–85 years, from the acute
stroke unit of the Helsinki University Hospital, Finland, were evaluated with
extensive clinical and neuropsychological assessments 3 months post-stroke.
Impairments within nine cognitive domains were determined according to age-
appropriate normative data from a random healthy population. Functional
disability was evaluated with the modified Rankin scale (mRS) 3 and
15 months post-stroke.
Results: In all, 83% patients showed impairment in at least one cognitive
domain, whereas 50% patients were impaired in multiple (≥3) domains. In
cases with excellent clinical recovery at 3 months (mRS = 0–1, no disability),
the occurrence of any cognitive impairment was 71%. Memory, visuoconstruc-
tional and executive functions were most commonly impaired. A substantially
smaller proportion of patients scored below the conventional or more stringent
cut-offs in the Mini-Mental State Examination (MMSE). Domain-specific cog-
nitive impairments were associated with functional dependence at 15 months
regardless of stroke severity and other confounders.
Conclusions: Cognitive impairment as evaluated with a comprehensive neuro-
psychological assessment is prevalent in stroke survivors even with successful
clinical recovery. Typically multiple domains and complex cognitive abilities
are affected. MMSE is not sensitive in detecting these symptoms. Post-stroke
cognitive impairment is strongly related to poor functional outcome.

differences in the sample characteristics, assessment

Introduction
Cognitive impairment is a common consequence of
stroke and one of the major determinants of poor
long-term outcome [1,2]. Even milder cognitive deficits
resulting from stroke can affect patients’ quality of
life, independent functioning and occupational abili-
ties. Earlier studies have reported varying prevalence
estimates for post-stroke cognitive impairment due to
Correspondence: H. Jokinen-Salmela, Unit of Neuropsychology,
Department of Neurology, Helsinki University Hospital,
PO Box 302, 00029 HUS, Helsinki, Finland (tel.: +358947173861;
fax: +358947174088; e-mail: hanna.jokinen@helsinki.fi).
methods, definitions of impairment and time interval
since stroke onset. Studies using short screening tests
of global cognitive dysfunction have typically yielded
relatively low prevalence rates, below 25% [3,4], whilst
more detailed neuropsychological assessments of
domain-specific cognitive impairments have suggested
higher occurrence, ranging from 35% to 92% [5–8].
Post-stroke cognitive impairment is not a unitary
syndrome but incorporates a variety of deficits in mul-
tiple domains such as attention, executive functions,
memory, language and visuoperceptual abilities. Tra-
ditionally, clinical outcomes in stroke studies have

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 POST-STROKE COGNITIVE IMPAIRMENT 1289

been evaluated with measures of physical recovery or Diagnostic and Statistical Manual of Mental Disorders
focal cortical syndromes such as aphasia and neglect, IV (DSM-IV) criteria [17] and pre-stroke cognitive
whilst the broad spectrum of cognitive changes has decline on the basis of all available history from the
been overlooked. Prospective follow-up studies of the patient and from the knowledgeable informant.
long-term functional impact of domain-specific cogni- In total, 409 patients participated in the neuropsy-
tive impairments are sparse [1,9,10]. Moreover, little is chological assessment described below after excluding
known about the occurrence of cognitive impairment cases with severe hearing or sight disabilities, reduced
in stroke patients with seemingly good clinical recov- level of consciousness, and those unwilling to partici-
ery and no physical handicap. pate. Compared to the included cases, the excluded
The aim of this study was to investigate the preva- cases (n = 77) were older (73.7 vs. 70.7 years,
lence of domain-specific cognitive impairments P = 0.002) and they had higher NIHSS (5.5 vs. 3.0,
3 months after ischaemic stroke in a large representa- P = 0.004) and lower MMSE scores (23.6 vs. 25.3,
tive cohort and in a subgroup of patients with excel- P = 0.035), but there were no significant differences in
lent clinical recovery (no significant disability). education or sex. The majority (n = 332, 81.2%) of
Cognitive impairment detected in an extensive the included patients had experienced a first-ever
neuropsychological assessment was compared to that stroke, 69 patients had a history of one previous
identified by the Mini-Mental State Examination stroke, and eight had more than one previous stroke.
(MMSE). Furthermore, the predictive value of the The characteristics of the patients are shown in
domain-specific cognitive deficits on functional disabil- Table 1.
ity was tested after 15 month follow-up. After 15 months, the evaluation of functional abili-
ties with mRS was repeated for 364 of 409 patients
either at a follow-up visit (n = 287) or by phone
Methods
(n = 77). At follow-up, 38 patients had died, six
patients refused to participate and one could not be
Subjects and study protocol
reached. At this stage, functional dependence was
In the Helsinki Stroke Aging Memory Study, 486 defined as mRS = 3–5 indicating moderate to severe
patients consecutively admitted to the acute stroke disability and need of assistance in daily activities.
unit of the Helsinki University Hospital, Finland, The study was approved by the Ethics Committee
were examined 3 months after ischaemic stroke. The of the Department of Clinical Neurosciences, Helsinki
baseline recruitment was conducted between Decem-
ber 1993 and March 1995, and the follow-up extended Table 1 Characteristics of the patients participating in the neuropsy-
to 15 years. The study procedure and the characteris- chological assessment in the Helsinki Stroke Aging Memory Study
tics of the patients have been described in full previ- (n = 409)
ously [11,12]. In summary, the examinations included Age, mean (SD) 70.7 (7.7)
comprehensive clinical neurological and neuropsycho- Sex, female, n (%) 207 (50.6)
logical assessments, and brain magnetic resonance Education, years, mean (SD) 9.2 (4.1)
Hypertension, n (%) 199 (48.7)
imaging. Of the vascular risk factors, hypertension
Diabetes, n (%) 96 (23.5)
was defined at the time of study inclusion as systolic Prior ischaemic stroke, n (%) 77 (18.8)
blood pressure ≥160 mmHg and diastolic blood pres- NIHSS score, n (%)
sure ≥95 mmHg. Diabetes was defined as previously 0 185 (45.2)
documented diagnosis, current use of insulin or oral 1–4 139 (34.0)
5–15 67 (16.4)
hypoglycaemic medication or fasting blood glucose
16–20 13 (3.4)
>7.0 mmol/l. The clinical severity of stroke was evalu- 21–42 5 (1.2)
ated with the National Institutes of Health Stroke mRS score, n (%)
Scale (NIHSS) [13], functional abilities with the modi- 0–1 152 (37.2)
fied Rankin Scale (mRS) [14] and post-stroke depres- 2–3 184 (45.0)
4–5 73 (17.8)
sive symptoms with the Beck Depression Inventory
MMSE, mean (SD) 25.4 (4.4)
(BDI) [15]. Excellent clinical recovery was defined as BDI, mean (SD) 9.5 (7.2)
mRS = 0–1 indicating no symptoms at all or no sig- Post-stroke dementia, DSM-IV, n (%) 68 (17.6)
nificant disability despite symptoms (able to perform Pre-stroke cognitive decline (%) 48 (11.7)
all usual duties and activities). Further, global cogni-
BDI, Beck Depression Inventory; DSM-IV, Diagnostic and Statisti-
tive status was evaluated with the MMSE using either cal Manual of Mental Disorders IV; MMSE, Mini-Mental State
<24/30 or <27/30 as the cut-off for cognitive impair- Examination; mRS, modified Rankin Scale; NIHSS, National Insti-
ment [16]. Dementia was diagnosed according to the tutes of Health Stroke Scale.

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Table 2 Neuropsychological test battery of the Helsinki Stroke

Aging Memory Study

Executive functions and attention

Trail making test, parts A and B
Stroop test, colour naming and interference
Wisconsin card sorting test
Verbal fluency, phonemic and semantic
Digit span, forward and backward
Memory
WMS-R logical memory, story A, immediate and delayed recall
WMS-R visual reproduction, immediate and delayed recall
Fuld object memory evaluation, 10-item learning test, 5 trials and
delayed recall
Visuoconstructional and spatial functions
WAIS-R block design
Figure copying test
Clock drawing test
Abstract thinking
WAIS-R similarities Figure 1 Number of cognitive domains impaired 3 months post-
Aphasia stroke in the Helsinki Stroke Aging Memory Study; total
Token test
n = 409
Boston naming test
Boston diagnostic aphasia examination, overall speech evaluation
visuoconstructional functions, 14 (3%) in aphasia, 50
Reading and writing
Samples (12%) in arithmetic, 37 (9%) in reading and writing,
Arithmetic 26 (6%) in agnosia and 43 (11%) in neglect. Missing
Arithmetic operations data occurred mainly due to patients’ inability to
Neglect complete the entire test battery.
Bells test
Agnosia
Poppelreuter Data analysis
See Appendix S1 for details and references. WAIS-R, Wechsler Comparisons between groups were made with the chi-
Adult Intelligence Scale revised; WMS-R, Wechsler Memory Scale
squared test, the independent samples t test or the
revised.
Mann Whitney U test, where appropriate. Factors
associated with cognitive impairments were studied
University Hospital, Finland. All subjects received with multiple logistic regression analyses entering
and signed an informed written consent. demographic characteristics, key risk factors and clini-
cal findings to the models simultaneously. The predic-
tive value of each domain-specific cognitive
Neuropsychological assessment
impairment on functional dependence (mRS = 3–5) in
The neuropsychological assessment was administered the 15-month follow-up was tested with logistic
by a trained neuropsychologist at a single session an regression analyses adjusting for confounders.
average of 105 (SD 14.8) days after the index stroke
[18]. The battery included 19 established cognitive
Results
tests grouped into nine cognitive domains (Table 2).
Standard instructions and scoring were used. Details
Cognitive impairment in the whole cohort
and the original references for the individual tests are
given in Appendix S1. Impairment within each In all, 339 of 409 (83%) patients showed impairment
domain was judged in three age groups using norma- in at least one cognitive domain. Eighty (20%)
tive data from a random Finnish population without patients had impairment in one domain, 56 (14%)
any neurological diseases [19]. Abnormality was patients in two and 203 (50%) patients in multiple
defined as a test performance 2 SD below the level of (≥3) domains (Fig. 1). Most frequently, impairments
the norm in domains assessed with a single test, or 1 were found in memory, and visuoconstructional and
SD below the normative level in several tests in executive functions, following deficits in language and
domains assessed with two or more tests [12,19]. other verbal functions with smaller proportions
Data on impairment were not available for 39 (Table 3). Neglect and agnosia were relatively uncom-
(10%) cases in executive functions/attention, 30 (7%) mon in this sample. The most frequent combinations
in memory, 43 (11%) in abstract thinking, 14 (3%) in of deficits were observed between memory and visuo-

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Table 3 Frequencies of impairment in each cognitive domain in the most frequent cognitive impairments. In bivariate
whole cohort and in a subgroup of patients with excellent clinical analysis, memory impairment was significantly associ-
recovery (mRS = 0–1) 3 months after ischaemic stroke in the Hel-
sinki Stroke Aging Memory Study
ated with lower education (8.8 vs. 10.0 years,
P = 0.005) and higher BDI score (10.5 vs. 8.0,
n (%) P = 0.001), but not with age, sex, hypertension, diabe-
All patients Patients with tes, prior stroke or NIHSS score. Visuoconstructional
Cognitive domain n = 409 mRS = 0–1 n = 152 deficits were related to higher age (72.1 vs. 68.7 years,
P < 0.001), female sex (56.9% vs. 42.5%, P = 0.004),
Memory functions 227 (60) 77 (52)
Visuoconstructional 216 (55) 54 (36)
lower education (8.6 vs. 10.0 years, P < 0.001) and
and spatial functions higher NIHSS score (3.5 vs.1.6, P < 0.001). Executive
Executive functions and 181 (49) 52 (34) dysfunction was associated with higher age (71.8 vs.
attention 69.1 years, P = 0.001), lower education (8.8 vs. 9.8
Aphasia 114 (29) 23 (15) years, P = 0.021) and prior stroke (22.1% vs. 13.8%,
Reading and writing 112 (30) 16 (11)
Abstract reasoning 106 (29) 26 (17)
P = 0.036), as well as higher NIHSS (3.2 vs. 1.5,
Arithmetic 71 (20) 12 (8) P < 0.001) and BDI scores (10.3 vs. 8.6, P = 0.025).
Neglect 29 (8) 2 (1) As analysed with multiple logistic regression entering
Agnosia 13 (3) 1 (1) all variables together, education and BDI score
Unequal numbers of cases are presented for each domain due to
remained as independent predictors of memory
missing data (see text for details). mRS, modified Rankin Scale. impairment [odds ratio (OR) 0.94, 95% confidence
interval (CI) 0.89–0.99, P = 0.027; OR 1.05, 95%
constructional functions (147 cases, 39%), executive CI 1.02–1.09, P = 0.003, respectively]. Age, education
and visuoconstructional functions (140 cases, 38%), and NIHSS score predicted visuoconstructional defi-
and executive functions and memory (133 patients, cits (OR 1.05, 95% CI 1.02–1.08, P = 0.001; OR 0.93,
37%). Relative to these, the other combinations 95% CI 0.88–0.98, P = 0.010; OR 1.14, 95% CI 1.06–
remained less frequent (<90 cases). Of the total sam- 1.22, P < 0.001, respectively), whereas age, prior
ple, 94 (24%) patients scored <24 and 192 (50%) stroke and NIHSS score predicted executive dysfunc-
patients scored <27 in the MMSE. tion (OR 1.04, 95% CI 1.01–1.07, P = 0.005;
OR 1.81, 95% CI 1.01–3.22, P = 0.046; OR 1.12,
95% CI 1.04–1.20, P = 0.002).
Cognitive impairment in a subgroup of patients with
excellent clinical recovery
Cognitive impairments associated with functional
In patients with excellent clinical recovery 3 months
dependence at 15-month follow-up
post-stroke (mRS = 0–1), any cognitive impairment
was found in 108 of 152 cases (71%). One domain In the whole cohort, all domain-specific cognitive
was affected in 38 (25%) cases, two in 22 (15%) cases impairments analysed one by one, except arithmetic
and multiple domains in 48 (32%) cases. Similarly to impairment, were significantly associated with func-
the whole cohort, the most common impairments and tional dependence (mRS = 3–5, n = 192, 44%) at the
combinations were found in memory, and visuocon- 15-month follow-up independently of age, sex, years
structional and executive functions (Table 3). of education and NIHSS (Table 4). After adding BDI
However, only nine (6%) patients of this subgroup score as another covariate, the results remained
scored <24 and 47 (31%) <27 in the MMSE. Com- unchanged. In addition to the cognitive impairments,
pared to the rest of the cohort (mRS >1), the patients poor functional outcome was significantly related to
with good clinical outcome were significantly younger age, BDI score and NIHSS score (P < 0.05). These
(68.6 vs. 72.0 years, P < 0.001), had higher education analyses were not run for neglect and agnosia because
(10.1 vs. 8.6 years, P < 0.001), were more often men of small numbers of cases.
(89 vs. 63, P = 0.004) and had lower NIHSS (0.4 vs.
4.5, P < 0.001). After excluding cases with a history
Discussion
of previous clinical stroke (n = 21), the frequency of
any cognitive deficits was still 69%. The prevalence and long-term functional significance
of domain-specific cognitive impairments were investi-
gated in a consecutive cohort of 409 middle-aged and
Factors associated with cognitive impairment
older patients 3 months after ischaemic stroke. In an
The demographic and clinical correlates of cognitive extensive neuropsychological assessment, cognitive
impairment were investigated by focusing on the three impairment was observed to be highly frequent both

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1292 H. JOKINEN ET AL.
Table 4 Cognitive impairments 3 months post-stroke as predictors
of functional dependence (modified Rankin Scale >2) at 15-month
follow-up in the Helsinki Stroke Aging Memory Study
Logistic regression
95% CI
Impairment OR (P value) for OR
Memory functions 2.2 (0.008) 1.2–3.9
Visuoconstructional and spatial functions 5.1 (<0.001) 2.7–9.1
Executive functions and attention 3.2 (<0.001) 1.8–5.7
Aphasia 2.1 (0.017) 1.1–3.9
Reading and writing 2.3 (0.011) 1.2–4.3
Abstract reasoning 2.3 (0.006) 1.3–4.2
Arithmetic 1.9 (0.063) 1.0–3.9
Statistical analyses are adjusted for age, sex, years of education and
stroke severity (National Institutes of Health Stroke Scale score).
OR, odds ratio; CI, confidence interval.
in the whole cohort (83%) and, strikingly so, also in a
subgroup of patients with excellent clinical recovery
and no functional disability at 3 months (71%). The
widely used screening test MMSE, with either the con-
ventional or more stringent cut-off, was only able to
detect much lower frequencies of cognitive dysfunc-
tion (24%–50% and 6%–31%, respectively). The
majority of the patients in both samples had impair-
ments in more than one cognitive domain. These defi-
cits were selectively associated with age, years of
education, depression, prior stroke and stroke sever-
ity. Independently of the confounding factors, the
domain-specific cognitive impairments were related to
functional disability at 15-month follow-up.
Our results support previous studies reporting a high
overall occurrence of cognitive impairment in detailed
evaluation of specific domains in a subacute stage of
stroke, i.e. up to 3 months after stroke onset [5–8,10].
However, direct comparison of studies is difficult due
to many methodological differences such as variation in
timing of assessment, evaluated cognitive domains and
test batteries, use of control group or normative data,
definition of impairment as well as dissimilar settings
and patient cohorts. In a pioneering study, Tatemichi
and co-workers found 78% of older stroke patients fail-
ing at least one cognitive test, whilst 35% were
impaired in four or more tests [5]. Recent studies have
reported even 76%–92% of patients demonstrating
impairment in one or more cognitive domains [7,8,10].
In addition to the overall prevalence of cognitive
impairment, there is also some variability in previous
studies in the proportions of the impaired domains.
Executive functions, attention and processing speed
are included in the most commonly impaired domains
in different studies [5–8,10,20,21]. As in our study,
impairments in long-term (episodic) memory [5,7] and
visuoconstructional and spatial functions [6,8] have
also been commonly reported. Taken together, cogni-
tive impairment seems to occur most frequently in
multiple cognitive domains, typically affecting com-
plex cognitive abilities, in which executive control
functions and focused attention have a major role.
These processes are also determining factors in com-
plex visuoconstructional functions and in effective
memory encoding and retrieval strategies. Impairment
in long-term memory, visuoconstruction and executive
functions, as well as combinations of these three defi-
cits, were the most common findings in our study.
Compared to these, impairments in abstract reason-
ing, language, reading, writing and arithmetic were
less common, although they still occurred in 20%–
30% of the patients. Neglect was relatively uncommon
occurring only in 8% of all patients, which contrasts
some of the earlier findings [6]. A simple cancellation
task was used in our assessment, which is widely used
in an acute setting but may not be sensitive in detect-
ing residual neglect in the post-acute stage.
An important result of the present study is the find-
ing that even the patients with the most favourable
clinical outcome (mRS = 0–1), thus having no appar-
ent functional disability, demonstrated a wide spec-
trum of cognitive deficits similar to the whole cohort.
Thus far, there have been few studies investigating
cognitive symptoms with detailed neuropsychological
assessments amongst clinically well-recovered patients.
These patients are typically discharged after short
acute care and are expected to return to their previous
lives without major difficulties. Planton and co-work-
ers have reported a 40% overall rate of cognitive
impairment 3 months post-stroke in 60 patients with
good clinical outcome (defined by mRS ≤ 2 and NI-
HSS ≤ 3) [22]. Furthermore, in a subgroup of stroke
patients with no apparent neurological symptoms (NI-
HSS = 0), Kauranen and co-workers observed cogni-
tive impairment in 41% of patients at 1–2 weeks’
evaluation and 32% of patients at 6 months’ follow-
up [23]. The patients of both these studies were youn-
ger compared to our study, which could explain their
lower figures. The likelihood of pre-stroke cognitive
decline is increased in the older age groups. Moreover,
these studies only enrolled patients who had experi-
enced their first symptomatic ischaemic stroke, whilst
all consecutive patients below the mRS cut-off (≤1)
were included here. Excluding patients with previous
stroke did not, however, essentially alter our results.
As far as is known, this is the largest neuropsycho-
logical study investigating post-stroke cognitive
impairment. A representative cohort of consecutive
patients from a unit responsible for acute stroke man-
agement in the city of Helsinki was collected prospec-
tively. In a stable post-acute stage of stroke, extensive
© 2015 EAN

neuropsychological assessments were carried out with
established clinical tests and performance was com-
pared with a single source age-matching normative
data. The relationship between cross-sectional neuro-
psychological data and functional outcome was
confirmed at 15 month follow-up. A minority of
patients were not able to complete all neuropsycholog-
ical tests, which may cause some selection bias in the
results and possible under-representation of cases with
the poorest cognitive outcome. Furthermore, a signifi-
cant proportion of patients in our cohort had low
NIHSS scores indicating that patients with mild to
moderate ischaemic stroke were over-represented
compared to those with severe stroke.
In conclusion, cognitive impairment was found in the
vast majority of late middle-aged and older patients
3 months after ischaemic stroke, and it was very fre-
quent even in patients with seemingly successful clinical
recovery and no functional disability. Typically, com-
plex cognitive abilities, including long-term memory
encoding and retrieval, focused attention and executive
functions as well as visuoconstructional abilities, were
compromised. These impairments were significantly
related to poor functional outcome during long-term
follow-up. MMSE proved to be insensitive in detecting
post-stroke cognitive impairment. The results empha-
size the importance of detailed cognitive assessment as
part of routine clinical evaluation of stroke patients.
Acknowledgements
The study was supported by grants from the Clinical
Research Institute and the Medical Research Fund of
the Helsinki University Central Hospital.
Disclosure of conflicts of interest
Dr Kaste reports grants from Helsinki University
Central Hospital and other support from Lundbeck
A/S, Siemens AG, Boehringer Ingelheim, Mitsubishi
Pharma Europe Ltd, outside the submitted work.
Supporting Information
Additional Supporting Information may be found in
the online version of this article:
Appendix S1. Neuropsychological test battery of the
Helsinki Stroke Aging Memory Study.
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