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2014 - Lees R. Et Al - Test Accuracy of Cognitive Screening Tests For Diagnosis of Dementia and Cognitive Impairment in Stroke
2014 - Lees R. Et Al - Test Accuracy of Cognitive Screening Tests For Diagnosis of Dementia and Cognitive Impairment in Stroke
Background and Purpose—Guidelines recommend screening stroke-survivors for cognitive impairments. We sought to
collate published data on test accuracy of cognitive screening tools.
Methods—Index test was any direct, cognitive screening assessment compared against reference standard diagnosis of
(undifferentiated) multidomain cognitive impairment/dementia. We used a sensitive search statement to search multiple, cross-
disciplinary databases from inception to January 2014. Titles, abstracts, and articles were screened by independent researchers.
We described risk of bias using Quality Assessment of Diagnostic Accuracy Studies tool and reporting quality using Standards
for Reporting of Diagnostic Accuracy guidance. Where data allowed, we pooled test accuracy using bivariate methods.
Results—From 19 182 titles, we reviewed 241 articles, 35 suitable for inclusion. There was substantial heterogeneity:
25 differing screening tests; differing stroke settings (acute stroke, n=11 articles), and reference standards used
(neuropsychological battery, n=21 articles). One article was graded low risk of bias; common issues were case–control
methodology (n=7 articles) and missing data (n=22). We pooled data for 4 tests at various screen positive thresholds:
Addenbrooke’s Cognitive Examination-Revised (<88/100): sensitivity 0.96, specificity 0.70 (2 studies); Mini Mental
State Examination (<27/30): sensitivity 0.71, specificity 0.85 (12 studies); Montreal Cognitive Assessment (<26/30):
sensitivity 0.95, specificity 0.45 (4 studies); MoCA (<22/30): sensitivity 0.84, specificity 0.78 (6 studies); Rotterdam-
CAMCOG (<33/49): sensitivity 0.57, specificity 0.92 (2 studies).
Conclusions—Commonly used cognitive screening tools have similar accuracy for detection of dementia/multidomain
impairment with no clearly superior test and no evidence that screening tools with longer administration times perform
better. MoCA at usual threshold offers short assessment time with high sensitivity but at cost of specificity; adapted
cutoffs have improved specificity without sacrificing sensitivity. Our results must be interpreted in the context of modest
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3008
Lees et al Cognitive Screening in Stroke 3009
Collation and synthesis of the evidence around cognitive blinded to each others’ results. On review of paired data, disagree-
screening tools will help guide policy and practice and high- ment was resolved by group discussion.
We developed a sensitive search strategy in collaboration with an
light knowledge gaps. We sought to perform systematic review Information Scientist (CF) and with assistance from the Cochrane
and meta-analysis, describing accuracy of screening tools for Dementia and Cognitive Improvement Group. Search terms were
assessing dementia and multidomain cognitive impairment in developed using a concepts-based approach, using Medical Subject
stroke-survivors. Heading terms and other controlled vocabulary. Concepts of inter-
est were stroke, dementia, and cognitive assessment. Our cognitive
assessment concept included terms relating to cognitive tests used
Methods in stroke, based on previous survey data.9,10 We searched multiple,
We used systematic literature review and meta-analysis techniques international, cross-disciplinary electronic databases from inception
specific to test accuracy13 and followed best practice in reporting.14 to January 2014. (Full search strategy is detailed in the online-only
Data Supplement I–II.) We checked reference lists of relevant studies
Aims and reviews for further titles, repeating the process until no new titles
Coprimary aims were to describe the following: were found.
We screened all titles generated by initial searches for relevance, and
1. Accuracy of cognitive screening tests for clinical diagnosis of corresponding abstracts were assessed and potentially eligible studies
multidomain, cognitive impairment/dementia in stroke-survivors. reviewed as full manuscripts against inclusion criteria. As a check of in-
2. Accuracy of brief (<5 minutes completion time), cognitive screen- ternal validity, a random selection of 2000 titles from the original search
ing tests against more detailed neuropsychological assessments. was reassessed by a third author (TQ). We tested external validity of our
If data allowed, secondary objectives were to compare differing search by sharing lists of included articles with independent researchers
cutpoint scores used to define a threshold of test positivity and to (Acknowledgments). One author (TQ) identified exemplar articles rel-
compare the effects of heterogeneity with specific reference to test evant to the review question (online-only Data Supplement II), and we
context and diagnostic reference standard. assessed whether these titles were detected by search strategy.
Figure 1. Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) flow diagram. ACE-R indicates Addenbrooke’s
cognitive examination-revised; AMT, Abbreviated Mental Test; FN, false-negative; FP, false-positive; HSROC, Hierarchical Summary
ROC; MMSE, mini-mental state examination; MoCA, Montreal cognitive assessment; R-CAMCOG, Rotterdam-CAMCOG; ROC, received
operating characteristic; TN, true-negative; and TP, true-positive.
Lees et al Cognitive Screening in Stroke 3011
Table 1. Test Accuracy Data for Studies Where Reference Standard was
Clinical Diagnosis of Dementia
n n (%) With Index Test Summary
Study Included Dementia (Threshold) Results
Brookes34* 152 N/A BMET Discriminates AD/SVD
Cumming 201022 149 42 (28%) Cog4 Sens: 53% Spec: 84%
de Koning 200037 300 55 (19%) R-CAMCOG (33) Sens: 91% Spec: 90%
de Koning 200538 121 35 (29%) R-CAMCOG (33) Sens: 66% Spec: 94%
de Koning 52
300 55 (19%) CAMCOG (81) Sens: 91% Spec: 80%
MMSE (25) Sens: 80% Spec: 76%
Dong 201239 300 60 (25%) MoCA (21) Sens: 88% Spec: 64%
MMSE (24) Sens: 88% Spec: 67%
Hershey 42
63 13 (21%) CSCE (20) Sens: 85% Spec: 87%
Hobson43* 149 N/A PNB (55) Sens: 71% Spec: 93%
Srikanth24 67 8 (12%) MMSE (23) Sens: 14% Spec: 100%
Tang47 142 10 (12%) MDRS (22) Sens: 82% Spec: 90%
MMSE (18) Sens: 80% Spec: 88%
Wu49 206 95 (46%) MoCA (23) Sens: 65% Spec: 79%
Where >1 test threshold was described, we present the primary data. AD indicates Alzheimer’s
disease; BMET, brief memory and executive test; CSCSE, cognitive capacity screening examination;
MDRS, Mattis dementia rating scale; MMSE, mini-mental state examination; MoCA, Montreal cognitive
assessment; N/A, not applicable; PNB, preliminary neuropsychological battery; R-CAMCOG, Rotterdam-
CAMCOG; and SVD, small vessel disease.
*Case–control study, data not included in pooled analyses.
Accuracy of Screening Tools for Diagnosis of descriptions of training and expertise of assessors (n=25 arti-
Cognitive Impairment cles; online-only Data Supplement V)
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Accuracy of Brief Tools were partially successful in this aim. Although there is an
We found 3 suitable articles (n=294 participants; online-only extensive, cross-disciplinary literature describing cogni-
Data Supplement VIII).53–55 Two articles were graded high risk tive testing in stroke, number of articles using the classical
of bias and applicability concerns because of case–control test accuracy paradigm of index test versus reference (gold)
methodology and patient inclusion.53,55 standard was limited. Eligible articles were characterized by
substantial heterogeneity and risk of bias, and the potential to
Discussion describe summary analyses at individual test level was limited.
Previous systematic reviews of cognitive test accuracy have Accepting these caveats, we can still offer conclusions from
focused on older adults with narrative results only. Our aim our pooled analysis. There was no clearly superior cognitive
was to provide a stroke-specific, literature synthesis to allow screening test. Given the relative consistency in accuracy,
evidence-based recommendations on cognitive testing. We choice of test strategy should be informed by other factors,
Lees et al Cognitive Screening in Stroke 3013
such as purpose of testing, feasibility; acceptability, and There is no universally accepted gold standard for demen-
opportunity cost. Recent guidance and practice has tended tia. Rather than restricting to a particular pathological subtype,
to favor novel tests compared with the traditionally popular our focus was all cause dementia post stroke. We think this
MMSE.6,7,56 Although there may be good reasons to favor approach is in keeping with current clinical practice, where
other tests, our data do not suggest that MMSE is inferior for initial screening highlights potential cognitive issues that can
the diagnosis of multidomain impairment, albeit MMSE may subsequently be characterized with more detailed assess-
lack sensitivity for single domain impairment.15,46,56 There was ments. Literature describing screening tests for diagnosis of
a trend toward better clinical utility for Rotterdam-CAMCOG, specific dementia subtypes was limited, and we were only
but the small number of studies and corresponding wide confi- able to describe test accuracy for all cause (undifferentiated)
dence intervals precludes definitive recommendation. dementia. A priori, we decided to include multidomain impair-
Preferred test properties will depend on test purpose, par- ment based on neuropsychological assessment in our reference
ticularly the level of cognitive impairment to be detected. It standard, and this approach maximized potential for pooled
could be argued that for initial screening, sensitivity is pre- analysis and recognizes that clinical diagnosis in certain stroke
ferred compared with specificity. In this case, MoCA and situations is not always feasible or appropriate. We used mul-
Addenbrooke’s Cognitive Examination-Revised may be pre- tidomain rather than single domain impairment because this is
ferred. The high false-positive rate for multidomain impair- closest to current operational classifications of dementia. We
ment obtained using MoCA <26 is to be expected because this did not specify content of the neuropsychological assessment
threshold was chosen for detection of single domain impair- and recognize the substantial heterogeneity in batteries used.15
ment/mild cognitive impairment.15,46 Our findings suggest that There were many potential sources of heterogeneity (sample
an adjusted cut-off <22 has improved overall test properties for size, case–control methodology, investigator training); indeed
multidomain impairment in stroke as suggested previously.15,46 a degree of heterogeneity is expected in test accuracy meta-
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We were pragmatic in our choice of index test and refer- analyses. We were not able to assess all potentially contributory
ence standard. Our screening test rubric included relatively factors across the modest number of included studies and accept
short assessments (MoCA) through to fairly lengthy batteries that this limits our findings. We chose to focus on reference stan-
(Repeatable Battery for Assessment of Neuropsychological dard and timing of assessment as the most important possible
Status). We did not find significant improvements in sensitiv- sources of heterogeneity. We found that test properties varied
ity/specificity comparing shorter and longer screens (MoCA with timing and seemed to favor earlier assessment, albeit our
and Addenbrooke’s Cognitive Examination-Revised). This rubric of acute assessment included studies from first hours ≤14
may suggest that increasing the length of test batteries does days post ictus. Comparative analysis of test properties require
not necessarily improve the test accuracy. careful interpretation; a conservative interpretation would be
Table 3. Pooled Test Accuracy for 4 Cognitive Screening Tests Against a Reference Standard of Cognitive Impairment
Articles Cognitive Sensitivity Specificity Positive Likelihood Negative Likelihood Clinical
Test (Threshold) (Patients) Impairment, n (%) (95% CI) (95% CI) Ratio (95% CI) Ratio (95% CI) Utility Index
ACE-R (<88/100) 2 (192) 52 (27%) 96.2 (0.90–1.0) 0.70 (0.59–0.80) 3.19 (2.24–4.54)) 0.06 (0.01–0.22) +0.67
−0.67
MMSE (<25/30) 12 (1639) 483 (30%) 0.71 (0.60–0.80) 0.85 (0.80–0.89) 4.73 (3.63–6.17) 0.34 (0.25–0.47) +0.46
−0.70
MMSE (<27/30) 5 (445) 195 (44%) 0.88 (0.82–0.92) 0.62 (0.50–0.73) 2.33 (1.72–3.17) 0.19 (0.13–0.29) +0.65
−0.54
MoCA (<22/30) 6 (726) 289 (39%) 0.84 (0.76–0.89) 0.78 (0.69–0.84) 3.75 (2.77–5.08) 0.20 (0.15–0.29) +0.59
−0.63
MoCA (<26/30) 4 (326) 131 (40%) 0.95 (0.89–0.98) 0.45 (0.34–0.57) 1.73 (1.43–2.10) 0.10 (0.04–0.23) +0.60
−0.36
R-CAMCOG (<33/49) 2 (421) 90 (21%) 0.81 (0.57–0.93) 0.92 (0.87–0.95) 10.18 (6.41–16.18) 0.20 (0.07–0.52) +0.59
−0.86
For clinical utility index, +, positive; −, negative. ACE-R indicates Addenbrooke’s cognitive examination-revised; MMSE, mini-mental state examination; MoCA,
Montreal cognitive assessment; and R-CAMCOG, Rotterdam-CAMCOG.
3014 Stroke October 2014
B
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Figure 3. Summary received operating characteristic (ROC) curve and forest plot describing test accuracy studies of (A) Folstein’s mini-
mental state examination (MMSE) at threshold of <25/30; and (B) MMSE at threshold of <27/30. (Continued)
Lees et al Cognitive Screening in Stroke 3015
D
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Figure 3 (Continued). Summary ROC curve and forest plot describing test accuracy studies of (C) Montreal cognitive assessment (MoCA) at
threshold of <26/30; and (D) MoCA at threshold of <22/30. The filled circle represents the summary (pooled) test accuracy; unfilled circles repre-
sent individual articles. The solid line is the summary ROC curve; the broken line is the 95% confidence interval (CI) around the summary point.
3016 Stroke October 2014
that a test suitable for longer-term poststroke assessment may missing data, future studies may wish to describe feasibility
not be suitable for early assessment and that cognitive testing and acceptability of testing, as well as classical test accuracy
can (and should) be performed in the acute stroke unit. metrics.
Brief assessment tools are attractive for use in busy stroke
settings but only if they have acceptable accuracy. In this Conclusions
regard, the limited number of studies looking at brief assess- All our results must be interpreted with caution as included
ments is unfortunate. Based on data available, screening using studies had substantial heterogeneity and potential for bias.
clock drawing test or abbreviated mental test may have a role However, we can offer some practical advice to clinicians.
for initial assessment; but they should not be considered a sub- There is no clearly superior cognitive screening test approach
stitute for subsequent multidomain testing. and no evidence that newer or longer screening tests neces-
sarily offer better test accuracy than established screens with
Limitations of Included Studies shorter administration time. The strategy for cognitive testing
Our review highlights issues in the design and reporting of in stroke must be informed by the purpose of the test and by
cognitive test accuracy studies. There was little reporting of other metrics, such as feasibility, acceptability, and opportu-
missing or indeterminate data; however, we know that sub- nity cost. If the purpose of the initial screening is to pick-up
stantial numbers of stroke patients are unable to complete all potential cases to allow further assessment, then MoCA
multidomain screening tools. The same concern holds for a may be the preferable test because it offers high sensitivity
reference standard based on extensive neuropsychological with shorter administration time than other equally sensitive
testing. Limiting test accuracy data to those able to complete tests. For MoCA use in stroke, screen positive thresholds may
testing will bias results, tending to inflate test accuracy. We need to be adapted if the aim is to assess for dementia/mul-
would encourage use of the intention to diagnose approach, tidomain impairment, and test accuracy may vary with time
where the traditional 2×2 test accuracy table is expanded with since stroke event.
cells representing those unable to complete index test and ref-
erence standard.57 Acknowledgments
A related issue is around generalizability of the included We are grateful for expert assistance from Cochrane Dementia and
subjects. In our quality assessment, we scored several articles Cognitive Improvement Group to Cochrane authors who shared rel-
evant papers, specifically Dr Ingrid Arevalo Rodriguez, Dr Sarah
as inappropriate exclusion, including the studies that excluded Cullum/Dr Daniel Davis, and Professor Nadina Lincoln. We are
patients with moderate to severe aphasia or inability to consent. grateful to all study authors who responded to queries or shared data.
We recognize the challenges of cognitive testing in this group,
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