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Article

Journal of Geriatric Psychiatry


and Neurology
Cognitive Deficits in Healthy Elderly 1-7
ª The Author(s) 2016
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DOI: 10.1177/0891988716629858
on the Mini-Mental State Examination jgpn.sagepub.com

Kristen L. Votruba, PhD1, Carol Persad, PhD1,2, and Bruno Giordani, PhD1,2

Abstract
This study investigated whether healthy older adults with Mini-Mental State Examination (MMSE) scores above 23 exhibit cog-
nitive impairment on neuropsychological tests. Participants completed the MMSE and a neuropsychological battery including tests
of 10 domains. Results were compared to published normative data. On neuropsychological testing, participants performed well
on measures of naming and recall but showed mild to moderate impairment in working memory and processing speed and marked
impairment in inhibition, sustained attention, and executive functioning. Almost everyone (91%) scored at least 1 standard
deviation (SD) below the mean in at least 1 domain. The median number of domains in which individuals scored below 1 SD was
3.0 of 10.0, whereas over 21% scored below 1 SD in 5 domains or more. With the strictest of definitions for impairment, 20% of
this population scored below 2.0 SDs below the norm in at least 2 domains, a necessary condition for a diagnosis of dementia. The
finding that cognitive impairment, particularly in attention and executive functioning, is found in healthy older persons who
perform well on the MMSE has clinical and research implications in terms of emphasizing normal variability in performance and
early identification of possible impairment.

Keywords
Mini-Mental State Examination, neuropsychological testing, cognitive screening

Cognitive Deficits in Healthy Elderly cognitive functioning is typically reported at 24 of 30,5,6 and
Population With ‘‘Normal’’ MMSE Scores scores below 24 have been shown to detect dementia fairly
accurately.7,8 The MMSE and a more thorough cognitive eva-
Dementia, and perhaps even more so mild cognitive impair- luation using the Dementia Rating Scale did not differ with
ment (MCI), can be difficult to diagnose by general practi- respect to classification in nursing home settings that often
tioners, particularly when working with a well-educated consist of more severely impaired elderly individuals,7 and the
population with significant cognitive reserve capacities and MMSE discriminates well between Clinical Dementia Rating
limited time to do a comprehensive assessment. Nevertheless, (CDR) stages of 0.5, 1.0, 2.0, and 3.0.8 Further, studies have
detection of cognitive deterioration is important, as cognitive found that in nondemented community samples older than
impairment is a significant cause of morbidity and mortality in 65 years, participants usually score 24 and above.3,9
the United States even after controlling for medical health.1,2 However, the MMSE is not without its limitations. First, age
Further, pharmaceutical advancements have made early detec- is associated with a decline in MMSE scores10,11 as is lower
tion even more essential as efforts to slow the progression of education level.9-11 These factors can potentially lead to mis-
the disease early in the course have become available. The use identification of dementia in these individuals. For example, in
of sensitive and brief screening measures of cognitive function- participants aged 60 to 69 years with 0 to 4 years of education, a
ing is therefore becoming more critical in geriatric settings. score of 18 to 19 may be a more appropriate cut score for
The most commonly administered brief screen for cognitive
functioning is the Mini-Mental State Examination (MMSE),3
which was developed as a bedside test that could be used to 1
Neuropsychology Section, Department of Psychiatry, University of Michigan
detect cognitive impairment. The MMSE is a 10-minute screen Medical Center, Ann Arbor, MI, USA
2
that consists of 11 questions assessing a variety of domains Michigan Alzheimer’s Disease Center (MADC), Ann Arbor, MI, USA
including orientation, attention, memory, language, and
Corresponding Author:
visual-spatial abilities. It is proven to have good concurrent Kristen L. Votruba, University of Michigan, 2101 Commonwealth Blvd Suite C,
validity with other neuropsychological assessment instruments Ann Arbor, MI 48105, USA.
but is not highly specific.4 The standard cutoff score for normal Email: kvotruba@umich.edu

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2 Journal of Geriatric Psychiatry and Neurology

dementia, whereas in the same aged people with 13þ years of Table 1. Sources of Normative Data.
education, a cut score of 26 to 27 is more appropriate.12 There
Test Source of Normative Data
is also perhaps an overdiagnosis of dementia based on the
MMSE in African Americans, but the debate continues whether WAIS: Digit Span WAIS manual21
an education correction can correct for this bias.13 The MMSE WMS: LII MOANS norms18
is also criticized as insensitive to deficits in cognitive domains DRT: spatial Taylor et al16
such as psychomotor speed, problem solving, or attention, BNT MOANS norms18
TMT A and B MOANS norms18
areas of deficit that are commonly present in individuals with
Stroop Stroop manual19
subcortical dementias or dementia due to multiple sclerosis14 WCST Rhodes17
or HIV.15 Further, the MMSE is potentially not efficient in TOVA TOVA manual20
detecting early signs of cognitive impairment, as evidenced
by its poor performance in separating CDR stages 0 from Abbreviations: BNT, Boston Naming Test; DRT, Delayed Recognition Test; LII,
Logical Memory II (delayed recall); MOANS, Mayo Older Americans
0.58 and its poor discriminatory capacity in individuals with Normative Studies; TMT A and B, Trail Making Test, Parts A and B; TOVA,
MMSE scores ranging from 21 to 25.16 Further, the overall Test of Variables of Attention; WAIS, Wechsler Adult Intelligence Scale–
score on the MMSE has been shown to be equivalent in healthy Revised; WCST, Wisconsin Card Sort Test; WMS, Wechsler Memory Scale–
participants and patients with MCI.17 Revised.
The current study investigated the relationship between
MMSE scores in a nondemented population of older, healthy, an assistive device but without help from other; and (4) score
community-dwelling adults and the performance of these indi- below 15 on the Geriatric Depression Scale (GDS). All parti-
viduals when evaluated with more comprehensive neuropsy- cipants were given an examination by a geriatrician or nurse
chological testing. We report the percentage of healthy elderly clinician to rule out the presence of neurological disease, sig-
participants with an MMSE score greater than 23 that exhibit nificant visual impairment not corrected by glasses, recent limb
cognitive deficits and compare these results to what would be or spinal fracture, other musculoskeletal impairments, or per-
expected based on normal variation in general cognitive pro- sistent symptoms of vertigo, lightheadedness, or unsteadiness.
files. The aim of this analysis was to identify whether the
MMSE is adequate to rule out cognitive impairment in a
healthy elderly sample. This study may have implications for Procedure
geriatric centers that frequently see many ‘‘healthy’’ older Participants underwent a neuropsychological battery that
adults. If the MMSE can accurately be utilized in this setting, included measures of global mental status, intelligence, and
it could provide a quick and easy way to screen for neuropsy- mood as well as reaction time, memory (verbal and visual),
chological impairment and perhaps reduce health care costs by confrontation naming, working memory, processing speed,
eliminating unnecessary tests for patients who are cognitively sustained attention, inhibition, mental flexibility, and concept
intact. formation. After excluding participants with MMSE < 24 and
those who endorsed significant symptoms of depression (GDS
 15), descriptive statistics were computed for each of the 10
Methods domains listed previously according to the percentage of parti-
cipants who scored below a designated point (SDs below the
Participants mean compared to others of the same age). All normative data
This retrospective study included 204 community-dwelling, used were adjusted based on age or age and gender. These
independent, healthy, older adults (39 men and 165 women). sources are listed in Table 1. When possible, normative data
The mean age was 79.44 years (standard deviation [SD] ¼ 7.5; were obtained from the test manual or from the Mayo Older
range ¼ 60-102), and the mean education level was 13.62 years Americans Normative Studies (MOANS) norms, as the
(SD ¼ 2.9; range ¼ 6-20). Average Full Scale IQ, as measured MOANS norms are based on age and are shown to be reliable
by the Wechsler scales, was 108 (SD ¼ 8.6; range ¼ 86-127). and valid.18 Normative data for the delayed recognition test
Individuals were recruited from the Human Subjects Core of (DRT) came from the study by Taylor et al.19 With regard to
the University of Michigan Claude Pepper Older Adults Inde- the Wisconsin Card Sort Test (WCST), normative data were
pendence Center (OAIC); the Michigan Alzheimer’s Disease taken from a meta-analytic review of published normative data
Center Clinical Core normal, healthy cohort; or 1 of 5 local (Rhodes)20 in order to allow for the inclusion of the wide
senior congregate apartment complexes. Participants were part breadth of ages included in our sample (the manual only pro-
of a larger study examining mobility in older community- vides normative data up to age 79 years). When comparing the
dwelling individuals. Participants included in this study were normative data of younger individuals, the normative data of the
those who met the following criteria: (1) age equal to or greater WCST manual and the Rhodes20 were not significantly different.
than 60 years; (2) no clinical evidence of dementia and an The proportion of domains in which each individual scored
MMSE score above 23 (mean MMSE score was 28.3 + 1.6); below 1, 1.5, or 2.0 SDs from expected norms was calculated
(3) able to stand independently from a sitting position for at in order to compare these results to the variation in performance
least 5 minutes and able to walk independently, with or without that would be expected in a truly healthy sample.

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Votruba et al 3

Measures
Working memory: Digit Span subtest (Wechsler Adult Intelligence
Scales–Revised). The Digit Span subtest is a measure of simple
auditory attention that measures immediate forward and back-
ward repetition of digit series.21

Inhibition: Stroop Color and Word Test. This task is a measure of


attentional abilities, particularly rapid shifting and inhibition of
attentional set.22 The task has 3 trials: the first requires parti-
cipants to rapidly read words (red, green, or blue) printed in
black ink; the second requires participants to name the colors of
the ink (red, green, or blue) presented in a box; and the third
requires the participant to name the color, not the word (red,
green, or blue), printed in a different color ink than the word
itself (color–word condition). Participants are given 45 seconds
for each trial, and the total score reflects the number of words
completed within the time limit. The total score on the color–
word condition was used in these analyses, as it is thought to be
the most ‘‘pure’’ measure of an individual’s ability to alternate
attentional focus and inhibit prepotent responses.

Sustained attention: Test of Variables of Attention. This is a com-


puterized continuous performance test measuring sustained Figure 1. Percentage of participants below a given standard deviation
on a battery of neuropsychological tests (controlled for age). BNT
attention and impulsivity.23 It provides error rates for omis-
indicates Boston Naming Test; DRT, Delayed Recognition Test; LII,
sions, which is a measure of sustained attention abilities and Logical Memory II (delayed recall); TMT, Trail Making Test; TOVA,
error rates for commissions which measures impulsivity. The Test of Variables of Attention; WAIS, Wechsler Adult Intelligence
rate of omission errors was used in the current analyses. Scale; WMS, Wechsler Memory Scale; WCST, Wisconsin Card Sort
Test.
Verbal memory: Logical Memory subtests (Wechsler Memory Scale–
Revised). This is a memory test in which participants are asked the connection of consecutively numbered circles from 1 to
to recall short stories that are read to them immediately and 25 printed on a page.26 Higher scores reflect a longer time to
then recall these stories 30 minutes later (ie, delayed recall).24 complete this task (worse performance).
On both tasks, total scores range from 0 to 50.
Cognitive flexibility: Trail Making Test-B. Part B of the TMT
Visual memory: Digit Recognition Task (DRT). This test measures requires the consecutive connection of alternating numbered
memory recognition for spatial positions using a delayed and lettered circles as quickly as possible.26 Time to complete
nonmatch-to-sample paradigm.19 The task involves identifying Part B is often used as a measure of executive functioning
a new stimulus in a variable array each time it appears with abilities, particularly mental flexibility. As in Part A of the
scores ranging from 0 to 14. TMT, higher scores reflect slower (worse) performance.
Confrontation naming: Boston Naming Test. This test requires Concept formation: Wisconsin Card Sorting Test. In this task, a
participants to name 60 ink drawings of items ranging in famil- participant is given 128 cards on which are printed 1 to 4 sym-
iarity.25 When an individual is unable to name a drawing, the bols, in one of 4 colors.27 The individual’s task is to place his or
examiner gives a stimulus cue. If the participant is still unable her cards under one of 4 stimulus cards according to a principle
to give a correct name, a phonetic cue is provided. The total that the participant must deduce based on examiner feedback.
score is the number of items correctly named immediately or The number of times that the participant correctly categorizes a
with a semantic cue (range: 0-60). specific number of cards in a row (ie, categories generated) was
used in the analyses.
Reaction time: Test of Variables of Attention. In addition to doc-
umenting omission and commission errors (described previ-
ously), the Test of Variables of Attention (TOVA) provides a
measure of mean response time to target stimuli providing a
Results
good measure of reaction time.23 Figure 1 presents the percentage of participants classified as
normal by the MMSE who scored below various standards
Processing speed: Trail Making Test, Part A. The Trail Making compared to the mean on the cognitive measures. Scoring
Test, Part A (TMT-A) is a test of visuomotor tracking requiring below 1 SD indicates that these individuals were in the bottom

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4 Journal of Geriatric Psychiatry and Neurology

16th percentile compared to others of their age. Results are


further classified by those who scored below 1.5 and 2.0 SDs
below the mean compared to others their age. Scoring 1.5 SDs
below the norm indicates that these individuals performed at
approximately the seventh percentile compared to their same-
aged peers, whereas those scoring 2 or more SDs below the
mean compared to others their age are comparable to the sec-
ond percentile. Individuals scoring in this range are typically
considered impaired in a clinical evaluation and have signifi-
cant functional difficulties arising from their objective cogni-
tive deficits. As can be seen in Figure 1, mild impairment (ie, at
least 1.0 SDs below the mean) was common on measures of
working memory (digit span: 72.4%), sustained attention
(TOVA omissions: 23.6%), processing speed (TMT-A:
24.9%), inhibition (Stroop Color–Word: 40.0%), and executive
functioning (TMT-B: 35.3%; WCST categories completed: Figure 2. Participants scoring below 1.0, 1.5, and 2.0 standard
deviations (SDs) in multiple domains. The 10 total domains assessed:
65.8%). Scoring in the moderate range of impairment (ie, at
working memory, verbal memory, visual memory, naming, processing
least 1.5 SDs below the mean) in this healthy population was speed, cognitive flexibility, inhibition, sustained attention, reaction
not rare, particularly on measures of inhibition (Stroop: time, and concept formation. Average number of domains below 1.0
26.3%), sustained attention (TOVA: 20.9%), cognitive flexi- SD ¼ 2.89 (1.99); median: 3.0. Average number of domains below
bility (TMT-B: 22.8%), and concept formation (WCST correct 1.5 SD ¼ 1.44 (1.54); median: 1.0. Average number of domains below
categories: 44.6%). Severe impairment (at least 2.0 SDs below 2.0 SD ¼ 0.77 (1.14); median: 0.0.
the mean) was noted on measures of attention (TOVA omis-
sions: 18.1%) and executive functioning (TMT-B: 20.1%; conducted. With MMSE as the dependent variable, the specific
WCST categories completed: 13.0%). neuropsychological domains were entered as independent vari-
Importantly, some variability in neuropsychological profiles ables. The total model was significant, F11,136 ¼ 3.30, P < .01,
is to be expected and may reflect characteristic long-standing R2 ¼ .21. The squared semipartial correlations, which indicate
weaknesses. In fact, in their publications of a large base nor- the amount of unique variance attributable to the individual
mative data set, Heaton et al report that normal patients may predictors in the model, indicated that Logical Memory II was
show impairment (‘‘conservatively’’ recorded in their sample the only uniquely significant predictor of MMSE score
as 1 SD below the norm) on 10% to 12% of the measures in (sr2 ¼ .03). In contrast, when using neuropsychological tests
their test battery.28,29 Using the same criteria for impairment as as the dependent variable, the MMSE score predicted approx-
Heaton et al, our study shows that 91% of the elderly popula- imately 8.6% of the variance in the Logical Memory II subtest
tion with normal MMSE scores showed impairment in 10% of scores (F1,178 ¼ 17.87, P < .01, R2 ¼ .09), supporting the strong
the measures that we administered and over half of our sample relationship between MMSE and memory performance. Inter-
showed impairment in at least 30% of the measures that were estingly, despite critiques of the MMSE as being insensitive to
administered. Figure 2 presents the number of domains in deficits in executive functioning, the MMSE was best as pre-
which participants scored below 1, 1.5, and 2.0 SDs below the dicting scores on the TMT-B (F1,182 ¼ 37.38, P < .01, R2 ¼ .17)
mean. As mentioned, almost everyone in our sample scored at and the Stroop Color–Word test (F1,173 ¼ 27.90, P < .01, R2 ¼ .13).
least 1 SD below the mean in at least 1 domain within this brief
neuropsychological battery, and 73% of the sample scored
below 1 SD on at least 2 of the domains assessed, a necessary
Discussion
condition for a diagnosis of dementia. The average number of Several prior studies have suggested that in early dementia, a
domains in which individuals scored below 1 SD was 2.89 cut score of 24 of 30 on the MMSE is likely too low.9,30 For
(SD ¼ 1.99; median ¼ 3.0), while over 10% of the individuals example, Benedict and Brandt31 found that over half of indi-
scored below 1 SD in 5 domains or more. With stricter defini- viduals with amnesia scored above 24 on the MMSE, and
tions for impairment, the average number of domains in which Galasko and colleagues32 found that 24 of 74 individuals with
individuals scored below 1.5 SDs below the norm was 1.44 (SD probable Alzheimer disease (AD) scored above the typical cut
¼ 1.54; median ¼ 1.0), with 38.5% of the population scoring score of 24. It has even been shown that in some cases of
below 1.5 SDs below the norm in 2 domains or more. With the probable AD, individuals have been able to score perfectly
strictest of criteria (2.0 SDs below the norm indicating severe on the MMSE.33 These studies highlight the concerns about
impairment), 43% of this population scored below this level in using the MMSE as the sole representation of cognition in
1 cognitive domain and 20% of the population scored below patients with known diagnoses or medical problems. Addition-
this level in at least 2 domains. ally, reviews of what other factors (other than MMSE score)
In an attempt to delineate what neuropsychological tests should be incorporating into a diagnosis of AD or MCI have
may predict MMSE score, a multiple regression was varied. Relevant factors include patient history, objective test

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Votruba et al 5

performance, and longitudinal assessment of functional abil- example, new, recently published clinical criteria for MCI rec-
ities. Unfortunately, such longitudinal assessment is not always ommend that an MCI diagnosis be considered if performances
possible early in the disease course as many people experience on cognitive tests are approximately 1 to 1.5 SDs below expec-
cognitive difficulties for several years before seeking assis- tation,36 and consideration of AD is recommended if such
tance. Little research has investigated the very common (and impairment is noted in 2 or more cognitive domains on testing
often recommended) use of the MMSE in healthy older adults and there is evidence of impairment in functional activities.37
in the community who are coming in for routine medical check- Our results suggest that this level of impairment often exists
ups before presenting with cognitive complaints. Such routine even in healthy elderly individuals with normal MMSE scores.
assessment could promote earlier and comprehensive neurop- Although our population was admittedly predominantly
sychological assessments in patients identified as at risk for women and perhaps slightly more educated than the elderly
cognitive impairment and subsequently result in improved general population, possibly limiting the generalizability, our
knowledge regarding characterization of specific cognitive findings support the prior observation that almost half of
phenotypes, biomarker associations, stability of diagnoses, healthy individuals with only subjective cognitive complaints
and prediction of progression, as proposed by Bondi and (but no functional impairment) have objective cognitive
colleagues.34 impairment upon formal neuropsychological testing.38 Partici-
The findings of the current study clearly indicate that cog- pants in our study showed objective cognitive impairment even
nitive impairment often exists, even in healthy elderly individ- without any subjective cognitive complaints. Relying solely on
uals who perform well on the MMSE. Much of our sample of an MMSE score may lead one to be particularly prone to mis-
individuals who received ‘‘passing’’ scores on the MMSE identifying patients with MCI, which is important in terms of
showed substantial deficits in attention, processing speed, men- treatment implications, predictions of future trajectory of
tal flexibility, and concept formation upon more thorough neu- symptoms, and appropriate identification for research studies.
ropsychological testing. These findings make clear that a score What appears critical to understand in the case of individual
of 24 or above on the MMSE does not assure the lack of patients seen clinically is whether objective cognitive impair-
cognitive impairment and concurs with prior research claiming ments represent a change in functioning from some previously
that the MMSE may not be as accurate in identifying cognitive higher level and whether they interfere with everyday activi-
impairment in domains such as attention and executive func- ties. Therefore, in a clinical setting, it may be particularly
tioning.14,15 Interestingly, however, when we analyzed the clin- important to have observer- or family-based evaluations of
ical domains that predict poor performance on the MMSE, tests functional status.
of cognitive flexibility and response inhibition predicted the These findings have implications for both clinicians and
most unique variance in the overall MMSE score, even more researchers. Clinically, although we cannot always be certain
than memory. These results suggest that although the MMSE of the functional manifestations of scoring below the norm on a
may lack specific items sensitive to executive functioning, the cognitive test and this study did not link cognitive performance
overall score is often impacted substantially by deficits in these with functional abilities, we must be alert to the potentially
skills. important deficits that may be present in attention and execu-
Although Axelrod35 has described normal variation in neu- tive functioning in individuals with a normal MMSE score, as
ropsychological performance across multiple domains, in the dangers associated with deficits in these areas can be sig-
which most normal participants have 1 domain below 1 SD nificant (poor decision making and inability to respond appro-
from the mean, the findings reported in this study suggest that priately to novel situations). Executive functioning skills
in healthy elderly individuals, the frequency of scores substan- appear to nonspecifically impact overall MMSE score, as mea-
tially below expectation given an adequate MMSE score was sures of cognitive flexibility and response inhibition were the
much higher. In fact, in our sample, the typical participant most predictive of MMSE scores in this population.
scored below 1 SD in 3 of the 10 domains that were assessed Further, researchers must be mindful that creating a distinc-
and over 21% of the participants scored below 1 SD in 5 tion in research studies based on a cutoff score of 24 on the
domains or more. More strikingly, with stricter criteria, almost MMSE is a fairly arbitrary and perhaps inappropriate distinc-
40% of the population scored below 1.5 SDs below the norm in tion, as it doesn’t guarantee a lack of cognitive impairment
2 domains or more and 20% of the population scored below 2.0 when including groups of community-based, healthy individu-
SDs (which would be classified in the severely impaired range) als. Research findings could easily be improperly influenced by
in at least 2 domains. Therefore, these data show that it is inappropriate participant selection and categorization based on
critical for the primary care provider to understand that an these standards. Continued research investigating the demo-
MMSE score above 23 does not guarantee intact cognition and graphic and personal characteristics that influence MMSE
reinforces the holistic diagnostic process that incorporates scores and the associated cutoff scores that may indicate
patient history and reported functioning abilities. dementia or MCI is warranted. Also, similar studies following
The findings of this article, suggesting that a substantial healthy elderly participants’ longitudinal cognitive status may
proportion of individuals demonstrate values below norm- yield further information about the utility of various aspects of
based expectations, have relevance to the clinical/neuropsy- the MMSE that may predict future preservation or decline in
chological evaluation of both patients with MCI and AD. For cognitive abilities.

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6 Journal of Geriatric Psychiatry and Neurology

Acknowledgments 12. Crum RM, Anthony JC, Bassett SS, et al. Population-based norms
The authors thank the Human Subjects cores of the University of for the Mini-Mental State Examination by age and education
Michigan Claude Pepper Older Adults Independence Center (OAIC), level. JAMA. 1993;269(18):2386-2391.
the Michigan Alzheimer’s Disease Center, and the senior apartment 13. Lampley-Dallas VT. Neuropsychological screening tests in Afri-
complexes that assisted with participation. can Americans. J Natl Med Assoc. 2001;93(9):323-328.
14. Franklin GM, Heaton RK, Nelson CM, et al. Correlation of neu-
ropsychological and MRI findings in chronic/progressive multi-
Declaration of Conflicting Interests ple sclerosis. Neurology. 1988;38(12):1826-1829.
The author(s) declared no potential conflicts of interest with respect to 15. Dilley JW, Boccellari A, Davis A. The use of the Mini-Mental
the research, authorship, and/or publication of this article. State Exam as a cognitive screen in patients with AIDS. Abstracts
of the Fifth International Conference on AIDS; Montreal, Canada;
Funding 1989.
16. Kim SYH, Caine ED. Utility and limits of the Mini Mental State
The author(s) disclosed receipt of the following financial support for
the research, authorship, and/or publication of this article: This Examination in evaluating consent capacity in Alzheimer’s dis-
research was supported in part by grant AG10542-0121 from the ease. Psychiatr Serv. 2002;53(10):1322-1324.
National Institute on Aging. 17. Diniz BSO, Yassuda MS, Nunes PV, Radanovic M, Forlenza OV.
Mini-mental state examination performance in mild cognitive
impairment subtypes. Int Psychogeriatr. 2007;19(4):647-656.
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