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for the Korean-Vascular Cognitive Impairment Harmonization Standards Study Group

Jae-Kwan Cha, Jong-Moo Park, Hee-Joon Bae, Yeonwook Kang and Byung-Chul Lee
Kyung-Ho Yu, Soo-Jin Cho, Mi Sun Oh, San Jung, Ju-Hun Lee, Joon-Hyun Shin, Im-Suck Koh,
Standards in a Multicenter Prospective Stroke Cohort in Korea
Cognitive Impairment Evaluated With Vascular Cognitive Impairment Harmonization
Print ISSN: 0039-2499. Online ISSN: 1524-4628
Copyright 2012 American Heart Association, Inc. All rights reserved.
is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Stroke
doi: 10.1161/STROKEAHA.112.668343
2013;44:786-788; originally published online December 27, 2012; Stroke.
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786
S
everal studies have elucidated the frequency and char-
acteristics of cognitive dysfunction in stroke patient
cohorts. However, most studies of poststroke cognitive impair-
ment have focused on dementia.
14
In 2006, the National
Institute of Neurological Disorders and Stroke and Canadian
Stroke Network proposed the Vascular Cognitive Impairment
Harmonization Standards (VCIHS), which could be used to
evaluate cognitive dysfunction in potential patients with vascular
cognitive impairment (VCI) in multicenter studies.
5,6
However,
no study has applied this neuropsychological test protocol to
poststroke survivors in a large-scale, multicenter stroke cohort.
The purpose of this study was to determine the frequency of
VCI and to investigate the usefulness of the Korean version of
the VCIHS neuropsychological (K-VCIHS-NP) protocol in a
multicenter, hospital-based stroke cohort study in Korea.
Methods
From October 2007 to August 2008, we screened 899 ischemic stroke
patients among who consecutively enrolled to the hospital-based
stroke registers of 12 university hospitals in South Korea.
7
The isch-
emic stroke was conrmed by magnetic resonance imaging within 7
days of symptom onset.
Of these patients, a total of 620 were enrolled within 2 weeks after
stroke for baseline evaluations. At 3 months after stroke, 506 patients
underwent a follow-up evaluation, and 353 patients completed the
60-minute K-VCIHS-NP protocol proposed by the National Institute
of Neurological Disorders and Stroke and Canadian Stroke Network
(Figure). Korean Mini-Mental Status Examination for evaluating
global cognitive dysfunctions and the Informant Questionnaire of
Cognitive Decline in the Elderly (IQCODE) for the premorbid history
of cognitive dysfunctions were also included. The tests and scales that
compose the K-VCIHS-NP protocol were validated and standardized
for Korean subjects (online-only Data Supplement Table I).
Dementia was diagnosed with reference to Diagnostic and
Statistical Manual of Mental Disorders, 4th Edition, criteria based on
cognitive functions that were categorized as impaired when a score
was below the 10th percentile for an individual domain and social
functioning status as assessed by the Instrumental Activities of Daily
Living scale. Patients were classied as having vascular dementia
(VaD), VCI with no dementia, and normal cognition. The detailed
methodology is described in the online-only Data Supplement.
Background and PurposeSince the Vascular Cognitive Impairment Harmonization Standards (VCIHS) neuropsychological
test protocol was proposed by the National Institute of Neurological Disorders and Stroke and Canadian Stroke Network,
no studies have applied this neuropsychological protocol to poststroke survivors in a large-scale, multicenter stroke
cohort. We determined the frequency of vascular cognitive impairment (VCI) and investigated the feasibility of using the
Korean version of the VCIHS neuropsychological protocol in a multicenter, hospital-based stroke cohort in Korea.
MethodsWe prospectively enrolled 620 subjects with ischemic stroke within 7 days of symptom onset among 899
patients who were consecutively admitted to 12 university hospitals in Korea. Neuropsychological assessments using the
60-minute Korean VCIHS neuropsychological protocol were administered at 3 months after stroke.
ResultsOf the 620 patients, 506 were followed up at 3 months after stroke. Of these, 353 (69.8%) were evaluated for
cognitive function using the 60-minute Korean VCIHS neuropsychological protocol. The frequency of VCI at 3 months
was 62.6%: VCI with no dementia in 49.9% and vascular dementia in 12.7%. Old age (P=0.014), poor functional outcomes
at 3 months (P=0.029), and stroke subtypes other than small vessel disease (P=0.004) were independent risk factors of VCI.
ConclusionsVCI, evaluated using the Korean VCIHS neuropsychological protocol, is substantial at 3 months after
ischemic stroke in Korea. The use of the 60-minute Korean VCIHS neuropsychological protocol was feasible in large-
scale multicenter studies. (Stroke. 2013;44:786-788.)
Key Words: neuropsychology stroke vascular dementia
Cognitive Impairment Evaluated With Vascular Cognitive
Impairment Harmonization Standards in a Multicenter
Prospective Stroke Cohort in Korea
Kyung-Ho Yu, MD, PhD; Soo-Jin Cho, MD, PhD; Mi Sun Oh, MD; San Jung, MD, PhD;
Ju-Hun Lee, MD; Joon-Hyun Shin, MD; Im-Suck Koh, MD; Jae-Kwan Cha, MD, PhD;
Jong-Moo Park, MD, PhD; Hee-Joon Bae, MD, PhD; Yeonwook Kang, PhD; Byung-Chul Lee, MD, PhD;
for the Korean-Vascular Cognitive Impairment Harmonization Standards Study Group
Received June 18, 2012; accepted October 18, 2012
From the Department of Neurology, Hallym University College of Medicine, South Korea; Department of Neurology, National Medical Center, South
Korea; Department of Neurology, Dong-A University Hospital, South Korea; Department of Neurology, Nowon Eulji Hospital, South Korea; Department
of Neurology, Seoul National University Bundang Hospital, South Korea; and Department of Psychology, Hallym University, Chunchon, South Korea.
The online-only Data Supplement is available at http://stroke.ahajournals.org/lookup/suppl/doi:10.1161/STROKEAHA.112.668343/-/DC1.
Correspondence to Byung-Chul Lee, MD, PhD, 896 Pyungchon Anyang-city, South Korea 430-070. E-mail: ssbrain@hallym.ac.kr
2013 American Heart Association, Inc.
Stroke is available at http://stroke.ahajournals.org DOI: 10.1161/STROKEAHA.112.668343
2012
46,100,127
Jennifer Schorr
Brief Reports
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Yu et al VCI Harmonization Standards in a Multicenter Study 787
Results
Of 620 patients enrolled in baseline evaluation, 267 missed
the cognitive assessment follow-up at 3 months, as depicted
in the Figure. Patients who were lost to follow-up were older,
less educated women, and had more hypertension, previous
stroke, severe stroke symptoms when admitted, and worse
prestroke functional and cognitive status (online-only Data
Supplement Table II).
The number of subjects with VCI at 3 months after stroke
was 221 (62.6%) of the 353 poststroke survivors who com-
pleted the K-VCIHS-NP protocol; VCI with no dementia was
apparent in 176 (49.9%), and VaD was apparent in 45 (12.7%).
As dened by the Korean Mini-Mental Status Examination
scores, the frequencies of VCI with no dementia and VaD were
9.9% (35/353) and 16.4% (58/353), consecutively. The propor-
tion of patients with recurrent stroke who experienced VaD was
twice that of rst-ever stroke patients (21.5% vs 10.8%; Table).
The frequency of prestroke cognitive decline evaluated using
Korean-IQCODE at the time of admission was 7.2% (25/346)
among patients who completed the 3-month follow-up. The fre-
quency of VaD among patients who had experienced prestroke
cognitive decline was 40% (10 of 25), which was 4-times
higher than the frequency among patients who did not have pre-
stroke cognitive decline (10.3%; 33/321). Old age (P=0.014),
poor functional outcomes at 3 months poststroke (P=0.029),
and stroke subtypes other than small vessel disease (P=0.004)
were independent risk factors of VCI (Online Table III).
Discussion
To the best of our knowledge, this is the rst large-scale,
multicenter study to evaluate the frequency of VCI using the
60-minute K-VCIHS-NP protocol proposed by the National
Institute of Neurological Disorders and Stroke and Canadian
Stroke Network.
A substantial percentage of patients in the prospective
acute stroke cohort were unable to undergo cognitive assess-
ment because of death, worsening of neurological or medi-
cal conditions, or failure to follow-up. In this study, of the
506 patients who were followed-up at 3 months after stroke,
353 patients (69.8%) were evaluated using the K-VCIHS-NP
protocol (Figure). This coverage rate of cognitive assessment
was slightly lower than the rates from previous studies, which
were reported to be 74.0% to 76.5%.
3,4,8
However, the previ-
ous cohort studies were not conducted in a multicenter setting,
and they applied individual neuropsychological tests, such as
the IQCODE or the Mini-Mental Status Examination.
2,57
A higher frequency of VCI at 3 months (62.6% in poststroke
survivors) was observed in this study. When the poststroke cog-
nitive impairments were dened using the Mini-Mental Status
Examination, the frequency of VCI was 37.1% (161/434) in
a previous cohort study in China
8
and 26.4% (93/353) in this
study. In another study, 55% of the patients showed abnor-
malities in 1 cognitive domain in a complementary neuro-
psychological battery.
9
This disparity might be explained by
the differences in study setting and in the extensiveness of the
neuropsychological protocols used.
2
In this study, of the 346 patients who completed the
K-IQCODE at the time of admission, only 25 (7.2%) had
Figure. Subject disposition.
Table. Frequency of Cognitive Impairment at 3 Months After
Stroke in Different Study Populations
Variable VaD VCIND Normal Cognition
All subjects, n=353 12.7% (45) 49.9% (176) 37.4% (132)
First-ever stroke, n=288 10.8% (31) 51.4% (148) 37.8% (109)
Recurrent stroke, n=65 21.5% (14) 43.1% (28) 35.4% (23)
Prestroke cognition, n=346
Declined cognition,
n= 25 (K-IQCODE 3.6)
40.0% (10) 52.0% (13) 8.0% (2)
Normal cognition,
n=321 (K-IQCOD E <3.6)
10.3% (33) 49.8% (160) 39.9% (130)
K-IQCODE indicates Korean-Informant Questionnaire of Cognitive Decline in
the Elderly; VaD, vascular dementia; and VCIND, vascular cognitive impairment
with no dementia.
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788 Stroke March 2013
experienced cognitive dysfunctions before stroke. Because
prestroke cognitive decline had to be retrospectively evaluated
using the K-IQCODE in this hospital-based study setting, the
prevalence of prestroke dementia could be underestimated.
However, the progression of patients from prestroke cognitive
decline to VaD observed in this study was similar to that of a
previous cohort study.
3
In conclusion, the 60-minute K-VCIHS-NP protocol might
be useful for evaluating cognitive impairments in poststroke
survivors in multicenter cohort studies.
Acknowledgments
Korean VCIHS study group members include Hee-Jun Bae, Jae-
Kwan Cha, Ki-Hyun Cho, Soo-Jin Cho, San Jung, Yeonwook Kang,
Dong-Eog Kim, Hahn-Young Kim, Oeun-Kyu Kim, Yong-Jae Kim,
Im-Suck Koh, Sun-Uck Kwon, Ju-Hun Lee, Seung- Hoon Lee, Soo-
Ju Lee, Mi Sun Oh, Jong-Moo Park, Joon-Hyun Shin, Kyung-Ho Yu
and Byung-Chul Lee.
Sources of Funding
This study was supported by a grant from the Korea Healthcare
Technology R&D Project, Ministry of Health and Welfare, Republic
of Korea (A102065), and Eisai Korea.
Disclosures
None.
References
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and predictors of dementia after ischemic stroke: the Chongqing stroke
study. J Neurol. 2004;251:421427.
2. Pendlebury ST, Rothwell PM. Prevalence, incidence, and factors associ-
ated with pre-stroke and post-stroke dementia: a systematic review and
meta-analysis. Lancet Neurol. 2009;8:10061018.
3. Serrano S, Domingo J, Rodrguez-Garcia E, Castro MD, del Ser T.
Frequency of cognitive impairment without dementia in patients with
stroke: a two-year follow-up study. Stroke. 2007;38:105110.
4. Tang WK, Chan SS, Chiu HF, Ungvari GS, Wong KS, Kwok TC, et al.
Frequency and determinants of poststroke dementia in Chinese. Stroke.
2004;35:930935.
5. Gorelick PB, Scuteri A, Black SE, Decarli C, Greenberg SM, Iadecola C,
et al. Vascular contributions to cognitive impairment and dementia: a state-
ment for healthcare professionals from the American Heart Association/
American Stroke Association. Stroke. 2011;42:26722713.
6. Hachinski V, Iadecola C, Petersen RC, Breteler MM, Nyenhuis DL,
Black SE, et al. National Institute of Neurological Disorders and Stroke-
Canadian Stroke Network vascular cognitive impairment harmonization
standards. Stroke. 2006;37:22202241.
7. Lee BC, Roh JK; Korean Stroke Registry. International experience in
stroke registries: Korean Stroke Registry. Am J Prev Med. 2006;31(6
Suppl 2):S243S245.
8. Zhou DH, Wang JY, Li J, Deng J, Gao C, Chen M. Frequency and
risk factors of vascular cognitive impairment three months after isch-
emic stroke in China: the Chongqing stroke study. Neuroepidemiology.
2005;24:8795.
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ment three months after stroke. Eur J Neurol. 2001;8:621627.
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SUPPLEMENTAL MATERIAL

Cognitive impairment evaluated with Vascular Cognitive Impairment Harmonization
Standards in a multicenter prospective stroke cohort in Korea

Supplemental Methods

Participants

From October 2007 to August 2008, we screened 899 ischemic stroke patients with
ischemic stroke among the consecutively enrolled to the multicenter hospital-based
stroke register
1
from 12 hospitals in South Korea. All subjects were patients with
ischemic stroke diagnosed using diffusion-weighted MRI within 7 days of symptom
onset.
Of these 899 patients, a total of 620 patients were enrolled for baseline assessment in
this study, after excluding 79 patients with severe concomitant medical or
neurological conditions (persistent impairment of consciousness or visual impairment),
14 with severe dysphasia, 8 who died within 2 weeks of stroke onset, 16 who were
referred to other hospitals, and 162 who refused to give informed consent. The
demographics, vascular risk factors, and clinical characteristics, including stroke
subtypes, the severity of neurological symptoms, and functional status, were evaluated
within 2 weeks after stroke onset during baseline evaluation. Of the 620 patients, 506
were followed up at 3 months after stroke onset, and 353 of them underwent
comprehensive cognitive evaluations. This study was approved by the Institutional
Review Board of each participating hospital, and all subjects provided written
informed consent.

Evaluation of cognitive functions

Three months after stroke, the patients cognitive functions were assessed using the
60-minute Korean version of the Vascular Cognitive Impairment Harmonization
Standards neuropsychological (K-VCIHS-NP) protocol proposed by the National
Institute of Neurological Disorders and Stroke and Canadian Stroke Network.
2, 3
The
original version consists of 4 cognitive domains: 1) executive / activation: Animal
naming, Controlled Oral Word Association Test (phonemic fluency), Digit Symbol
Coding, and Trail Making Test; 2) language: Boston Naming Test; 3) visuospatial:
Rey Complex Figure Test: Copy-; and 4) memory: Hopkins Verbal Learning Test. In
addition, Korean Mini-Mental Status Examination (K-MMSE) for evaluating global
cognitive dysfunctions and the Informant Questionnaire of Cognitive Decline in the
Elderly (IQCODE) for assessing the patients pre-morbid history of cognitive
dysfunctions were also included. All tests and scales in the original version were
validated and standardized in Korea (Table S1).
4-13


Diagnosis of dementia and cognitive impairment

Dementia was diagnosed according to the Diagnostic and Statistical Manual (DSM) of
Mental Disorders, Fourth Edition, criteria based on clinical interviews, cognitive
functions assessed using the 60-minute K-VCIHS-NP, and social functioning status
assessed on the scale of instrumental Activities of Daily Living (IADL) 3 months after
stroke onset.
Cognitive functions were categorized as impaired when a decline was observed in at
least 1 domain, where a score below the 10
th
percentile for an individual domain. For
frontal domains, which consisted of 4 tests, patients who scored below the 10
th

percentile on more than 2 tests were identified as having abnormal frontal functions.
Functional status and pre-stroke cognitive declines were classified as abnormal if the
scores were above 0.43 on the Korean instrumental ADL scale
5
and 3.6 on the K-
IQCODE,
12
in accordance with the validation studies conducted on the Korean
versions of these tests.
Patients were classified as having vascular dementia (VaD), vascular cognitive
impairment with no dementia (VCIND), and normal cognition. VaD was defined as
dementia in post-stroke survivors without regard to pre-stroke cognitive status, and
VCIND was defined as cognitive impairment after stroke that does not meet the
dementia criteria of DSM-IV. We also compared the rates of VCIND and VaD
defined by the K-VCIHS-NP protocol with the rates determined using more
established neuropsychological instruments, K-MMSE scores. The subjects had a
score below the 2
nd
percentile of the K-MMSE score of the norm group were defined
as VaD, and between the 2
nd
and 10
th
percentile were VCIND.
7, 14-17


Statistical Analysis

The differences in demographics and clinical variables between study participants and
patients who were excluded from the study were compared using the Chi-squared and
the Mann-Whitney tests according to the characteristics of variables. The clinical
determinants associated with VaD, VCIND, and normal cognition were assessed using
logistic regression models, controlling for age, sex, level of education, various
vascular risk factors, and other detailed clinical variables, including subtypes of
ischemic stroke. A two-sided p-value of less than 0.05 was defined as statistically
significant.



Supplemental Table 1. Korean version of the 60-minute Vascular Cognitive
Impairment Harmonization Standards-Neuropsychology Protocol proposed by the
National Institute of Neurological Disorders and Stroke and Canadian Stroke Network
Cognitive domains and
neuropsychological test
Korean version of
VCIHS-NP protocol
Sources
Executive/Activation
Animal naming (semantic fluency) Animal naming Kang, Y et al.
(2000)
8

Controlled Oral Word Association
Test (COWAT)
Korean-COWAT (!, ", #)
Kang, Y et al.
(2000)
8

Digit Symbol Coding Digit Symbol Coding Yum, TH et al.
(1992)
6

Trail Making Test Korean-Trail Making Test-
Elderlys version
Yi, H et al.
(2007)
18

List learning test strategies Seoul Verbal Learning Test Kang, Y et al.
(2003)
10

Language / Lexical Retrieval
Boston Naming Test Korean-Boston Naming test:
Short form A
Kang, Y et al.
(1999)
9

Visuospatial
Rey Complex Figure Test: Copy Rey Complex Figure Test:
Copy
Kang, Yet al.
(2003)
10

Memory
Hopkins Verbal Learning Test Seoul Verbal Learning Test Kang, Y et al.
(2003)
10

Others
Informant Questionnaire of
Cognitive Decline in the Elderly
(IQCODE): Short form
IQCODE-Korean Lee, DW et al.
(2005)
12

Mini-Mental State Examination
(MMSE)
Korean-MMSE Kang, Y
(2006)
7

Instrumental Activities of Daily
Living (ADL)
Korean-Instrumental ADL Kang, SJ et al.
(2002)
5

VCIHS-NP: Vascular Cognitive Impairment Harmonization Standards neuropsychological


Supplemental Table 2. Comparison of the clinical characteristics of patients whose
cognitive function was evaluated with those of patients who dropped out at the 3-
month follow-up

Baseline
assessment
(N=620)
Cognitive
function
evaluated
(N=353)
Dropped out
(N=267)
P
value
Age, years SD 65.6 12.5 63.9 12.4 67.9 12.3 <0.001
Sex (women), % (N) 44.4 (275) 38.8 (137) 51.7 (138) 0.002
Education, years SD 4.5 1.8 4.7 1.7 4.2 1.8 <0.001
Risk Factors, % (N)
Hypertension 66.3 (411) 62.9 (222) 70.8 (189) 0.046
Diabetes 32.9 (204) 32.6 (115) 33.3 (89) 0.871
Hyperlipidemia 24.5 (151) 22.9 (80) 26.6 (71) 0.310
Smoking 43.2 (268) 45.9 (162) 39.7 (106) 0.130
prior stroke 23.2 (144) 18.7 (66) 29.2 (78) 0.002
Atrial fibrillation 17.6 (109) 15.9 (56) 19.9 (53) 0.206
NIH Stroke Scale score at
admission (median*)
3 3 4 <0.001
Poor pre-morbid status, % (N)
(modified Rankin Score !3)
9.8 (61) 7.6 (27) 12.7 (34) 0.048
Pre-stroke IQCODE score,
median*
3.07
(N=594)
3.07
(N=346)
3.11
(N=248)
0.003
SD: standard deviation; N: number; NIH: National Institutes of Health; IQCODE:
Informant Questionnaire of Cognitive Decline in the Elderly; * Mann-Whitney U test



Supplemental Table 3. Clinical characteristics and determinants of cognitive
impairment in post-stroke survivors at 3 months after ischemic stroke


Uni-variable analysis Multi-variable analysis

Normal
cognition
(N=132)
VCI
(N=221)
P value
Adjusted
OR

P value
Men, % 60.7 61.7 0.860
0.77
(0.42-1.41)
0.395
Age, years (SD)
59.9
(13.2)
66.5
(11.7)
<0.001


1.03
(1.01-1.06)
0.014
Low education, $ 6 years % 35.1 46.0 0.055

Vascular risk factors

Hypertension, % 49.1 69.2 <0.001
*

1.71
(0.94-3.12)
0.082
Diabetes, % 25 36 0.039
*

1.47
(0.78-2.75)
0.234
Hyperlipidemia, % 27.7 20.6 0.142

Smoking, % 43.1 44.3 0.837

Prior stroke, % 16.1 20.2 0.350

Ischemic Stroke subtypes, %

Large artery atherosclerosis 28.8 46.1 0.002
*

1.42
(0.70-2.87)
0.331
Small vessel occlusion 40.5 21.3 <0.001
*

0.36
(0.18-0.72)
0.004
Cardioembolism 12.6 17.6 0.239

Other or undetermined causes 8 14.7 0.425

Neurological severity on
admission
by NIH Stroke Scale, mean (SD)
3.45
(3.76)
4.57
(4.65)
0.025


1.04
(0.97-1.13)
0.276
Poor functional status at 3
months by modified Rankin
Scale % 3, %
4.7 22.3 <0.001
*

3.59
(1.14-11.30)
0.029
NIH: National Institutes of Health; SD: Standard deviation; VCI: vascular cognitive
impairment,
* Chi-square test, Mann-Whitney test, OR: odds ratio (95% confidence interval)
after adjusting for age, sex, hypertension, diabetes, NIH Stroke scale, modified Rankin
Scale, large artery atherosclerosis, and small vessel occlusion



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healthcare professionals from the American Heart Association/American Stroke
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3. Hachinski V, Iadecola C, Petersen RC, Breteler MM, Nyenhuis DL, Black SE, et
al. National Institute of Neurological Disorders and Stroke-Canadian Stroke
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