Mini-Mental State Examination Item Scores as Predictors of Alzheimer's Disease: Incidence Data From the Kungsholmen Project, Stockholm

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1 Journal of Gerontology: MEDICAL SCIENCES 1997, Vol. 52A. No. 5, M299-M304 Copyright 1997 by The Gemntological Society of America Mini-Mental State Examination Item Scores as Predictors of Alzheimer's Disease: Incidence Data From the Kungsholmen Project, Stockholm Brent J. Small, 1 Matti Viitanen, 1 and Lars Backman 1,2 'Stockholm Gerontology Research Center and Department of Clinical Neuroscience and Family Medicine, Division of Geriatric Medicine, Karolinska Institute, Stockholm, Sweden. department of Psychology, Goteborg University, Goteborg, Sweden. Background. The present study examined the power of individual Mini-Mental State Examination (MMSE) items in predicting incidence of Alzheimer's disease (AD). In addition, 3-year longitudinal changes in MMSE items were contrasted between incident AD and nondemented persons. Methods. A population-based group of very old adults, years of age, were followed longitudinally. Of the original 327 participants, 32 were diagnosed with probable or possible AD after a 3-year follow-up interval and 189 remained nondemented. Cognitive performance was indexed by the individual item scores from the MMSE. These sample from multiple domains of cognitive functioning, including visuospatial skill, recent memory, orientation to time and place, language, and the ability to sustain attention. Results. Items dealing with delayed episodic memory and orientation to time were significant predictors of AD incidence, independent of age, gender, and years of education, as determined by logistic regression analyses. Longitudinally, changes in performance were largest among individuals diagnosed as incident AD, although the magnitude of change across items was highly variable. In particular, decline was relatively small for the delayed memory item, whereas most other measures showed dramatic decline in performance among individuals with incident AD. Conclusions. Individual MMSE items, especially those with some type of episodic memory referent, were the best predictors of incident cases of AD. Moreover, MMSE items displayed differential rates of change, particularly for the incident AD participants. THE Mini-Mental State Examination (MMSE; 1) is one of the most widely used instruments for screening cognitive impairment (2). It is composed of 20 items that assess multiple domains of cognitive functioning, including tests of visuospatial skill, recent memory, orientation to time and place, language, and the ability to sustain attention. The total score of the MMSE is out of a maximum of 30 points, and traditionally a cutoff of 23/24 is used in screening for cognitive impairment, such as dementia (2). In the present study, we examined the relationship between performance on the individual MMSE items and incidence of Alzheimer's disease (AD) over a 3-year followup interval. Several studies have found that individuals who have poorer baseline MMSE total scores are more likely to develop AD than their superior performing counterparts (3,4). What is less clear, however, is whether there is a differential relationship among the specific MMSE items and prediction of dementia. That is, do individuals who are going to develop AD lose their points equally across all domains of performance, or are some abilities more affected than others? We know, for example, that measures of episodic memory performance are particularly effective predictors of dementia incidence (5-8). The question remains whether specific MMSE items, related to memory or other abilities, show a differential relationship in the prediction of AD. This research question has some potentially interesting clinical implications. When making diagnostic decisions, clinicians may be encouraged to chart the areas in which patients "lose" their points on the MMSE. If particular items in the MMSE are differentially affected in preclinical stages of AD, or other syndromes, this information may aid in the subsequent diagnosis of these impairments. A related question concerns longitudinal changes in MMSE item performance in incident AD. It is becoming increasingly clear that episodic memory performance is among the first abilities to be affected in AD (5-11). On the other hand, verbal and visuospatial functioning are thought to decline somewhat later in the disease process (9-11). In the current study, we sought to examine whether a similar differential pattern of cognitive change could be observed with MMSE item scores corresponding to memory, verbal, and visuospatial performance. There is some evidence that MMSE items do follow a differential pattern of negative change in AD. Brooks et al. (12) found little evidence for longitudinal change in the delayed recall item of the MMSE, but more pronounced changes in factors related to language and orientation abilities. Thus, the second goal of the present study was to examine whether a differential pattern of change exists among the MMSE items for incident AD and nondemented persons. M299

2 M300 SMALL ETAL. The participants in the present study come from a longitudinal investigation of very old (75-95 years) adults residing in Stockholm, Sweden. The sample is unique in that little is known about the ability of cognitive performance measures to predict incident cases of AD in the very old, as most related studies have focused on younger samples of elderly adults (5-7). METHODS Subjects. The original population was taken from all inhabitants aged 75 years and older in the Kungsholmen parish of Stockholm (2,368 individuals) who were included in a population survey on aging and dementia. A detailed description of the population and methods used has been reported elsewhere (13,14). Three phases of the study have been completed. In phase 1, 1,810 individuals from the whole study population were administered a questionnaire, which included the MMSE, to detect suspected dementia cases. In phase 2, all those with an MMSE score below 24 (n = 314) arid a random sample, stratified by age and gender, of those with an MMSE score above 23 (n = 354) were assessed with extensive medical, neurological, and psychiatric examinations; social and family interviews; laboratory blood analyses; and a comprehensive cognitive test battery. In phase 3, all participants from phase 2 were invited back to be examined approximately 3 years later. The same clinical and psychological examination was administered at this time. The diagnostic criteria and procedure used to reach the clinical diagnosis of dementia, as well as type of dementia, at baseline and follow-up, are described in detail in Fratiglioni et al. (13) and involved multiple steps. In the first step, a preliminary diagnosis was made after a common discussion among the geriatricians who had examined the participant and reviewed their social and family history. Step 2 involved a second preliminary diagnosis of all participants by a physician expert in dementia. In step 3, the two preliminary diagnoses were compared and cases with discordant diagnoses were reviewed again by the physicians to ascertain causes of agreement and disagreement. This eliminated most of the discordant diagnoses; however, in those cases where disagreement persisted, the final diagnosis was made by a supervising physician. This process yielded a diagnosis of the presence or absence of dementia according to the criteria in the Diagnostic and Statistical Manual of Mental Disorders (15). Type of dementia was further defined according to standardized criteria (15). There were 225 persons with dementia, whereas 443 were found to be nondemented at that time. The present study focuses on the nondemented and incident AD cases between phase 2 (time 1) and phase 3 (time 2). From the nondemented participants, the following were excluded from the present analyses at baseline: 66 with MMSE scores below 24; 30 with psychiatric symptomatology (e.g., major depression, psychosis, schizophrenia, paranoia); 16 with a history of stroke; and 4 with Parkinson's disease. Of the remaining 327 nondemented participants, 32 were diagnosed as having probable or possible AD after the approximate 3-year (3.08 ±.60, mean ± SD) follow-up interval. In addition, 9 were diagnosed with dementia other than AD (e.g., vascular dementia, mixed vascular, unspecified), 61 individuals had died, and 36 participants dropped out (e.g., refused, moved, could not be located). For the present analyses, the final sample consisted of 189 nondemented and 32 incident AD persons. The baseline demographic characteristics of the nondemented and incident AD participants are presented in Table 1. Analyses indicated that two of the individual items were statistically reliable, age and MMSE score. Results indicated that the incident AD patients were older and had poorer MMSE scores at entry. Measures. The primary outcome measure was the MMSE (1). The Swedish version of the test was administered according to standardized procedures, arid the total score is out of a maximum of 30. In the present study, the question requiring individuals to spell a word backwards was not examined. Because of missing data, only the serial sevens measure was used to index the ability to sustain attention. In addition to the total score, 11 individual item scores were examined. They were orientation to time, orientation to place, word recall-immediate, serial sevens, word recall-delayed, naming, repetition, following commands, reading, writing, and design copy. Data analysis. To assess the power of the MMSE items to predict dementia incidence, a logistic regression analysis was conducted with diagnostic category (i.e., AD vs nondemented) as the outcome variable. In this analysis, age, gender, and years of education were controlled by including them as covariates in the model. The relative importance of the individual baseline MMSE items was assessed by stepwise forward logistic regression procedures, with alpha level set at.01. To facilitate comparisons of the power of each of the MMSE items in predicting dementia incidence, the scores were transformed into z- scores to maintain the same metric across variables. Longitudinal changes in MMSE item scores were assessed with a Diagnostic Group (AD, nondemented) X Time of Measurement repeated measures multivariate analysis of variance (MANOVA). To adjust for type I error rate, a modified Bonferroni procedure (16) with family wise alpha at.01 was employed for the univariate tests of significance. Variable Age Gender (% Female) Years of education MMSEf AD14 Table 1. Baseline Demographic Characteristics of Incident AD and Nondemented Participants Incident AD (n = 32) ± ± ± ±1.20 Nondemented (n=189) ±4.80* ± ±1.94** 1.63 ±1.05 Note: Data are given as mean ± SD. fmini-mental State Examination (1). JKatz ADL index (1 = independent, to 7 = dependent; ref. 24; due to missing data n = 219 (32 incident AD and 187 nondemented subjects). *p<.01; **/?<.001.

3 MMSE AND INCIDENCE OF ALZHEIMER'S DISEASE M301 RESULTS Prediction of incident AD. Table 2 shows the results of the logistic regression analysis predicting dementia status at time 2. Age, gender, and years of education were entered as a block and treated as covariates. Among the demographic characteristics, only age was statistically reliable. The negative regression coefficient indicated that older individuals were more likely to develop AD. Among the MMSE items assessed at baseline, two measures, word recall-delayed and orientation to time, were reliable predictors of dementia status at follow-up. In both cases, poorer performance at baseline was associated with an increased risk of AD. The odds ratios indicated that word recall-delayed was the most potent predictor of dementia incidence. Specifically, the probability of developing AD at the follow-up interval increased 3 times per decrease in SD unit at baseline. A decrease of 1 SD unit orientation to time was associated with a doubling of the risk of developing AD. Table 2. Results From Logistic Regression Predicting AD* with Age, Gender, and Years of Education as Covariates Variable Covariatesf Age Gender Years of education Significant predictors^ Word recall-delayed Orientation to time P Odds Ratio % CI p-value <.001 <.001 *AD outcome coded as 1; no dementia was coded as 2. ( Variables entered as a block. ^Variables entered by stepwise (forward) procedure. Variables are continuous and in z-score metric. Risk ratios represent relative risk of incident dementia per SD difference independent of all other variables in the model. Longitudinal changes in performance. Table 3 presents the means and SD for the MMSE items as a function of dementia status and time of measurement. Note that the sample size for the nondemented group has been reduced by one participant. This was due to the subject refusing testing at the second time of measurement because of fatigue. Diagnostic Group X Time of Measurement repeated measures MANOVAs were performed separately on the MMSE total score and on the group of individual item scores. Analyses on the total score revealed significant effects of group status, time of measurement, and a Group X Time of Measurement interaction. Inspection of the means revealed that the incident AD group declined by almost 8 points (7.81 ± 5.20; mean ± SD) over the followup interval, whereas the nondemented group declined by just over 1.5 points (1.68 ± 2.82). Among the individual MMSE items, there were significant effects of diagnostic group, time of measurement, and a Diagnostic Group X Time of Measurement interaction. Univariate analyses indicated significant diagnostic group differences, favoring the nondemented adults, on all of the MMSE items. The univariate analyses for time of measurement revealed longitudinal changes in performance on 10 of the 11 items. The time of measurement effect for word recall-delayed failed to reach statistical significance (p =.715). Finally, and most importantly, univariate analyses indicated significant Time of Measurement X Diagnostic Group interactions for 8 of the 11 MMSE items. The three items for which the interaction effect was not reliable were word recall-delayed (p =.186), design copy (p =.195), and follow commands (p =.007; not reliable at adjusted alpha level). Although the majority of the MMSE items showed reliable effects of diagnostic group, time of measurement, and their interaction, there was a great deal of variability in the magnitude of these relationships. One way to gauge this variability is to convert the change scores into standardized scores. This allows us to directly compare changes across different items because they have the same metric. Table 4 Table 3. Performance on MMSE Items as a Function of Dementia Diagnosis and Time of Measurement Incident AD Nondemented Variable* Time 1 («= 32) Time 2 (n = 32) Time 1 (n =188) ± ± ± ± ± ± ± ± ± ± ± ±.44 Time 2 (n= 188) Total score (30) Orientation to time (5) Orientation to place (5) Immediate memory (3) Serial sevens (5) Delayed memory (3) Naming (2) Repetition (1) Follow commands (3) Reading (1) Writing (1) Copy a design (1) ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±.50 Note: Data are given as mean ± SD. Numbers in parentheses refer to the highest possible score for each item.

4 M302 SMALL ETAL. Table 4. z-score Change on MMSE Subscales for Incident AD and Nondemented Participants Variable Total score Orientation to time Orientation to place Word recall-immediate Serial sevens Word recall-delayed Naming Repeat sentence Follow commands Reading Write sentence Copy design Note: Data are given as mean ± SD. Incident AD (n = 32) ± ± ± ± ± ± ± ± ± ± ± ± 1.52 Nondemented (n= 188) -.26 ± ± ± ± ±.11 ± -.19 ± -.28 ± -.18± 0.00 ±.22 ± -.44 ± displays the longitudinal changes in z-scores, created by using the averaged mean and SD across times of measurement for the nondemented and incident AD groups. There are several things that are readily apparent from this table. First, the Time of Measurement X Diagnostic Group interactions are obvious given the large negative changes in performance among the incident AD group, whereas the performance of the nondemented group changed very little over the retest interval. The second thing that is clear from Table 4 is the large variability in change across each of the domains of cognitive functioning. For the incident AD group, the greatest changes occurred for the MMSE total score and the two orientation measures. On the other hand, there was no reliable change in the delayed recall measure. A somewhat lower variability in change was observed in the nondemented group whereby the serial sevens measure exhibited the most negative change. By contrast, several other items exhibited no changes (e.g., word recall-immediate, reading) or even slight increases (e.g., word recalldelayed, write a sentence) for the nondemented group over the follow-up interval. DISCUSSION The results from the logistic regression analysis indicated that two of the individual MMSE items added to the prediction model of AD. Specifically, poorer performance on delayed word recall and orientation to time was associated with an increased risk of AD. Galasko et al. (4) reported similar findings in their attempt to discriminate between mild AD and nondemented persons on the basis of MMSE item performance. They noted that mild AD patients exhibited greater impairment on these MMSE items, as well as orientation to place, as compared to the nondemented group of adults. In the present study, we extend these findings by demonstrating that baseline performances on the delayed recall and orientation to time measures are sensitive predictors of AD even before a clinical diagnosis is possible. The results from the logistic regression analysis are also consistent with other studies (5-8) that have examined the prediction of AD incidence with more comprehensive cognitive batteries. Specifically, these studies have found that variables assessing episodic memory performance are the best predictors of AD incidence. Although two of the MMSE items were significant predictors of AD, the majority of variables were not related to the incidence of AD. Among the individual MMSE items, performance associated with attentional (serial sevens), verbal (naming, repeat sentence, reading), visuospatial (copy design), and primary memory (word recall-immediate) abilities failed to significantly predict dementia incidence. The nonsignificant effects are consistent with prior cross-sectional analyses from the same study population. Herlitz et al. (9) examined the predictive role of a comprehensive battery of cognitive tests in detecting early AD. They found that visuospatial measures, as well as indices of primary memory, failed to contribute to the discrimination between patients with mild AD and normal adults at time 1. Among the demographic variables (age, gender, and years of education), only age was significantly related to dementia incidence. The relationship with age was expected given the clear increase in the incidence of AD in older age groups (17,18). The lack of a significant relationship with gender is inconsistent with some studies (5,14), but consistent with others (18) that have examined this relationship. Recently, a report describing incidence of dementia using subjects from the same population as the present study (19) found a greater incidence of AD among women than in men. However, that study focused solely on data from phase 1, and the sample size was much larger than that of the present study, resulting in greater power to detect effects of the demographic characteristics on the incidence of AD. In addition, we observed no relationship between educational attainment and incidence of AD. This contrasts with results from other studies that have reported that greater educational attainment may serve as a protective factor for the development of dementia (20,21). One possibility for the negative finding in the present study was that there is limited variability in educational attainment, and this may have mitigated against finding such effects. However, other studies that have used large samples with greater variability in educational attainment have also found no relationship between years of education and incidence of AD (5,22). Thus, the lack of education effects in the present study may not simply result from the limited variability in our sample. The results from the mean-level longitudinal analyses indicated diagnostic group differences and negative longitudinal changes both in favor of the nondemented group for the majority of MMSE items. Moreover, significant Diagnostic Group X Time of Measurement interactions resulted from the performance of the AD group declining dramatically over the follow-up interval, whereas the nondemented group exhibited fewer changes in performance. Although significant decline was detected for the majority of variables, there was substantial variability in the magnitude of these changes. For example, among the incident AD persons, there was no evidence for longitudinal change in delayed word recall, but performance on the two orientation measures and the total score declined by more than 2 SD over the follow-up interval.

5 MMSEAND INCIDENCE OF ALZHEIMER'S DISEASE M303 The results indicating differential change among the MMSE items are consistent with prior studies that have used more elaborate cognitive batteries. Several longitudinal studies have found the most dramatic changes in the cognitive performance of mildly to moderately demented adults to occur in measures of verbal and visuospatial ability (10,11). Episodic memory functioning (e.g., word recall-delayed), on the other hand, exhibits fewer changes in performance because this ability is compromised early in the progression of the disease (23). In the present study, we found comparable results when the progression of dementia was charted from the preclinical to mild to moderate stages of impairment. However, one possibility for the lack of change in delayed word recall is that performance on this item was close to floor levels already at baseline and this may have prevented any future negative change. Although this may be possible, at least for the incident AD group, we feel that it does not detract from the fact that episodic memory is among the first abilities to decline in AD. The results of the present study have several clinical implications. For example, clinicians may be encouraged to focus on both the MMSE total scores, for screening and classification purposes, and the MMSE items scores, to determine which items the individuals perform most poorly on. In the present study, we found that the delayed memory and orientation to time measures were particularly effective predictors of incidence of AD. An interesting question would be to examine the predictive relationships between MMSE items and other dementing syndromes. If persons with different dementia etiologies have the same MMSE total score, but "lose" their points on different questions, this information could be useful in helping to diagnose dementia and differentiate between different dementing syndromes. Unfortunately, too few persons with dementia diagnoses other than AD precluded the examination of this research issue in the present study. Although the current study is informative regarding the role of MMSE items in predicting dementia incidence, and longitudinal changes over a 3-year follow-up interval, there are several limitations that must be acknowledged. Most notably is the size of the AD sample that was examined. Although the AD incidence rates are comparable to other studies (8,19), the small sample size may limit the power of the statistical tests to detect differences in performance. In addition, the proportion of men in the sample is somewhat limited. This may have led to the nonsignificant effects of gender in the logistic regression analyses as both groups were not evenly represented. In sum, the results of the present study indicated that individual items of the MMSE can act as significant predictors of dementia incidence. In particular, items with some form of memory referent, including word recall-delayed and orientation to time, were associated with an increased risk of developing AD. In addition, the results indicated that for the incident AD group, dramatic changes in cognitive performance across a 3-year follow-up period occurred for most domains of functioning although little change was observed for the episodic memory item (word recalldelayed). ACKNOWLEDGMENTS This research was supported by grants from the Swedish Council for Research in the Humanities and the Social Sciences to Lars Backman, and from the Swedish Council for Social Research to Bengt Winblad and Lars Backman. We thank all members of the Kungsholmen Project Study Group for collaboration and data collection. Address correspondence to Dr. Brent J. Small, Department of Gerontology-SOC 107, University of South Florida, 4202 E. Fowler Ave., Tampa, FL REFERENCES 1. Folstein MF, Folstein SE, McHugh PR. 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6 M304 SMALL ETAL. 22. Cobb JL, Wolf PA, Au R, White R, D'Agostino RB. The effect of education on the incidence of dementia and Alzheimer's disease in the Framingham Study. Neurology 1995;45: Storandt M, Morris JC, Rubin EH, Coben LA, Berg L. Progression of senile dementia of the Alzheimer type on a battery of psychometric tests. In: Backman L, ed. Memory functioning in dementia. Amsterdam: North-Holland, 1992: Katz S, Ford A, Moskowitz RW, Jackson BA, Jaffee MW. The index of ADL: standardized measure of biological and psychosocial function. JAMA 1975; 185: Received August 8, 1996 Accepted February 10, 1997 FREE PRECONFERENCES FOR ALL STUDENTS AND NEW MEMBERS OF THE GERONTOLOGICAL SOCIETY OF AMERICA Open preconference workshops designedfor all students andfor new GSA members will be offered at the Society's 50th Annual Scientific Meeting at the Convention Center in Cincinnati, OH. There is no charge for these sessions: preregistration is required; attendance is limited; membership is not mandatory. See the preliminary program or contact the Society for registration forms. SESSION #1 Perspectives in Gerontology: An Overview for All Disciplines Friday, November 14; 12:30-2:00pm, Room North 206 This overview session will introduce student and new members of GSA to the structure and function of the Society and its four sections: Biological Sciences, Clinical Medicine, Behavioral and Social Sciences and Social Research, Policy and Practice. Former section chairs, and representatives from the Minority Task Force and Student Organization of GSA will provide information about current research and professional activities of the Society. Presenters will also describe the ways in which student and new members can become involved in Society activities. Speakers: R. Applebaum, PhD (Miami Univ); J. Dwyer, PhD (Wayne State Univ); C. Fry, PhD (Loyola Univ); J. Johnson, MD (Univ of PA School of Medicine); M. Miranda, PhD (Cat State, Los Angeles); P. Wise, PhD (Univ ofky); C. Zwane, MS (Univ ofnc at Greensboro). SESSION #2 (Select One) Perspectives on the Biology of Aging Friday, November 14; 2:30-5:00pm - Room South 240 This session offers students, new investigators and others interested in the biological processes that influence the rates of aging, an overview of some areas of ongoing biogerontological research. Underlying concepts and various aspects of current biological research will be discussed along with the relationship of processes of aging and the etiology of disease. Aspects of public policy, funding of aging research and the interests of science will also be discussed. Speakers: H. Bertrand, PhD (Univ oftx at San Antonio); E. Masoro, PhD (Univ o/tx- HSC at San Antonio); R. Miller, PhD (Univ of Ml); R McDonald, PhD (Univ ofca - Davis). Perspectives in Behavioral and Social Sciences Research Friday, November 14; 2:30-5:00pm - Room North 214 This session is designed for graduate students and others new to the Society. Focus is on developing a career in gerontology, choosing an area of research, and the use of qualitative and quantitative methods in the study of aging. Speakers: P. Dilworth-Anderson, PhD (Univ of NC at Greensboro); L. Burton, PhD (PA State Univ); B. Dugan, PhD (Bowman Gray School of Medicine); M. Luborsky; PhD (Wayne State Univ); S. White-Means, PhD (Univ of Memphis). Perspectives in Clinical Medicine Research Friday, November 14; 2:30-5:00pm - Room South 241 Designed for graduate students and researchers who are at the beginning or mid-level of their research career, This session provides a multidisciplinary perspective on practice implications and emerging clinical research issues in a changing health care environment. Speakers: S. Travis, PhD (Univ of OK); M. Hobbins, DMD (Univ of TX - Houston Dental); J. Wyman, PhD, RN, FAAN (Univ ofmn); L Phillips, PhD, RN, FAAN (Univ ofaz); M. Bernard, MD (Univ of OK - HSC); J. Rogers, PhD (Univ of Pittsburgh). Perspectives in Social Research, Policy, and Practice Friday, November 14; 2:30-5:00pm - Room South 234 This session is designed for graduate students and others new to the Society. It will showcase a variety of research topics of interest to and pursued by SRPP Section members. Speakers will discuss their research or practice, including wnat inspired them to begin doing this research/practice and how their interests have evolved over time. Speakers: S. Geron, PhD (Boston Univ); R. Hudson, PhD (Boston Univ); R. Applebaum, PhD (Miami Univ - Scripps Gerontology Center); J. Gonyea, PhD (Boston Univ); M. Downs, PhD (Univ of Stirling, Scotland); V. Colder on, MS (UMASS/Boston). The Gerontological Society of America, 1275 K Street, NW, Suite 350, Washington, DC (202) FAX (202) geron@geron.org