Leisure Activities and the Risk of Dementia in the Elderly
Joe Verghese, M.D., Richard B. Lipton, M.D., Mindy J. Katz, M.P.H., Charles B. Hall, Ph.D., Carol A. Derby, Ph.D., Gail Kuslansky, Ph.D., Anne F. Ambrose, M.D., Martin Sliwinski, Ph.D., and Herman Buschke, M.D.
Background Participation in leisure activities has been associatedwith a lower risk of dementia. It is unclear whether increasedparticipation in leisure activities lowers the risk of dementiaor participation in leisure activities declines during the preclinicalphase of dementia.
Methods We examined the relation between leisure activitiesand the risk of dementia in a prospective cohort of 469 subjectsolder than 75 years of age who resided in the community anddid not have dementia at base line. We examined the frequencyof participation in leisure activities at enrollment and derivedcognitive-activity and physical-activity scales in which theunits of measure were activity-days per week. Cox proportional-hazardsanalysis was used to evaluate the risk of dementia accordingto the base-line level of participation in leisure activities,with adjustment for age, sex, educational level, presence orabsence of chronic medical illnesses, and base-line cognitivestatus.
Results Over a median follow-up period of 5.1 years, dementiadeveloped in 124 subjects (Alzheimer's disease in 61 subjects,vascular dementia in 30, mixed dementia in 25, and other typesof dementia in 8). Among leisure activities, reading, playingboard games, playing musical instruments, and dancing were associatedwith a reduced risk of dementia. A one-point increment in thecognitive-activity score was significantly associated with areduced risk of dementia (hazard ratio, 0.93 [95 percent confidenceinterval, 0.90 to 0.97]), but a one-point increment in the physical-activityscore was not (hazard ratio, 1.00). The association with thecognitive-activity score persisted after the exclusion of thesubjects with possible preclinical dementia at base line. Resultswere similar for Alzheimer's disease and vascular dementia.In linear mixed models, increased participation in cognitiveactivities at base line was associated with reduced rates ofdecline in memory.
Conclusions Participation in leisure activities is associatedwith a reduced risk of dementia, even after adjustment for base-linecognitive status and after the exclusion of subjects with possiblepreclinical dementia. Controlled trials are needed to assessthe protective effect of cognitive leisure activities on therisk of dementia.
The incidence of dementia increases with increasing age.1,2Although the prevention of dementia has emerged as a major publichealth priority, there is a paucity of potential preventivestrategies.3,4,5 Identifying protective factors is essentialto the formulation of effective interventions for dementia.Cross-sectional studies report associations between dementiaand reduced participation in leisure activities in midlife,as well as between cognitive status and participation in leisureactivities in old age.6,7 Katzman proposed that persons withhigher educational levels are more resistant to the effectsof dementia as a result of having greater cognitive reserveand increased complexity of neuronal synapses.8 Like education,participation in leisure activities may lower the risk of dementiaby improving cognitive reserve.9,10,11,12,13,14,15
In observational studies, elderly persons who had participatedto a greater extent in leisure activities had a lower risk ofdementia than those who had participated to a lesser extent.10,11,12,13,14,15Although these results suggest that leisure activities havea protective role, an alternative explanation is possible. Inmost types of dementia, there is a long period of cognitivedecline preceding diagnosis.16,17,18 Reduced participation inactivities during this preclinical phase of dementia may bethe consequence and not the cause of cognitive decline. Resolutionof this issue requires a long period of observation before diagnosisto enable researchers to disentangle the potential effects ofpreclinical dementia. Base-line cognitive status, educationallevel, and level of depression may confound the relation betweenleisure activities and dementia.10,11,12,13,14,15 Moreover,most studies have not assessed the associations between leisureactivities and particular types of dementia.10,11,12,13,14
The Bronx Aging Study provided us with the opportunity to studythe influence of leisure activities on the risk of dementiaover a long period19,20 while accounting for previously identifiedconfounders. This community-based study has followed a cohortof persons who did not have dementia at base line, with theuse of detailed clinical and neuropsychological evaluationsperformed at intervals for up to 21 years.19,20 We examinedthe influence of individual and composite measures of cognitiveand physical leisure activities on the risk of the developmentof dementia.
Methods
Study Population
The study design and recruitment methods of the Bronx AgingStudy have been described previously.19,20 Briefly, the studyenrolled English-speaking subjects between 75 and 85 years ofage who resided in the community. Criteria for exclusion includedsevere visual or hearing impairment and a previous diagnosisof idiopathic Parkinson's disease, liver disease, alcoholism,or known terminal illness. Subjects were screened to rule outthe presence of dementia at base line and were included if theymade eight or fewer errors on the Blessed Information–Memory–Concentrationtest.19,20,21 This test has a high test–retest reliability(0.86), and its results correlate well with the stages of Alzheimer'sdisease.22,23 At the inception of the study, the cohort wasmiddle-class, most subjects were white (91 percent), and themajority were female (64 percent). Written informed consentwas obtained at enrollment. The local institutional review boardapproved the study protocol.
The study enrolled 488 subjects between 1980 and 1983. Subjectsunderwent detailed clinical and neuropsychological evaluationsat enrollment and at follow-up visits every 12 to 18 months.The potential study period consisted of the 21-year period from1980 to 2001. We excluded 2 subjects without documented leisureactivities and 17 subjects who moved or declined to return forfollow-up. After these subjects had been excluded, 469 subjects(96.1 percent) were eligible. In 1992, 73 surviving subjectswere still having study visits in our current project, the EinsteinAging Study.
Clinical Evaluation
During the study, subjects were interviewed with the use ofa structured medical-history questionnaire and were examinedby study clinicians.19,20 Functional limitations on 10 basicand instrumental activities of daily living were rated on a3-point scale for each activity (range of total scores, 10 to30 points), with 1 point indicating "no limitation," 2 pointsindicating "does activity with difficulty," and 3 points indicating"unable."19,20 A spouse or family member accompanied most subjectsor was contacted for confirmation of the history.
Neuropsychological Evaluation
An extensive battery of neuropsychological tests was administeredat study visits.18,19,20 We examined performance on the BlessedInformation–Memory–Concentration test (range ofscores, 0 to 33),21 the verbal and performance IQ accordingto the Wechsler Adult Intelligence Scale,24 the Fuld Object-MemoryEvaluation (range of scores, 0 to 10),25 and the Zung depressionscale (range of scores, 0 to 100).26 These tests were used toinform the diagnosis of dementia at case conferences.
Leisure Activities
At base line, subjects were interviewed regarding participationin 6 cognitive activities (reading books or newspapers, writingfor pleasure, doing crossword puzzles, playing board games orcards, participating in organized group discussions, and playingmusical instruments) and 11 physical activities (playing tennisor golf, swimming, bicycling, dancing, participating in groupexercises, playing team games such as bowling, walking for exercise,climbing more than two flights of stairs, doing housework, andbabysitting). Subjects reported the frequency of participationas "daily," "several days per week," "once weekly," "monthly,""occasionally," or "never." We recoded these responses to generatea scale with one point corresponding to participation in oneactivity for one day per week. The units of the scales are thusactivity-days per week; the scales were designed to be intuitivelymeaningful to clinicians and elderly persons and to be usefulin the design of intervention studies or public health recommendations.For each activity, subjects received seven points for dailyparticipation; four points for participating several days perweek; one point for participating once weekly; and zero pointsfor participating monthly, occasionally, or never. We summedthe activity-days for each activity to generate a cognitive-activityscore, ranging from 0 to 42, and a physical-activity score,ranging from 0 to 77.
The estimates of the overall level of participation were consistentwith good test–retest reliability for scores obtainedon entry and at the next visit a year later on the cognitive-activityscale (Spearman r = 0.518, P=0.001) and the physical-activityscales (Spearman r = 0.410, P=0.001). There was no direct measurementof the time spent in activities, although participation wasverified by family members or friends. The scores were not correlatedwith age. Scores on the cognitive-activity scale correlatedwith scores on the Blessed test21 (Spearman r = –0.286,P=0.001), but not functional status (Spearman r = –0.042,P=0.77). Scores on the physical-activity scale correlated withfunctional status (Spearman r = –0.293, P=0.001) but notwith scores on the Blessed test (Spearman r = –0.021,P=0.65).21
Diagnosis of Dementia
At study visits, subjects in whom dementia was suspected onthe basis of the observations of members of the study staff,results of neuropsychological tests, or a worsening of the scoreson the Blessed test21 by four points or a total of more thanseven errors underwent a workup including computed tomographicscanning and blood tests.19,20 A diagnosis of dementia was assignedat case conferences attended by study neurologists, a neuropsychologist,and a geriatric nurse clinician, according to the criteria ofthe Diagnostic and Statistical Manual of Mental Disorders, thirdedition (DSM-III) or, after 1986, the revised third edition(DSM-III-R).27,28,29 Updated criteria for the diagnosis of dementiaand particular types of dementia were introduced after the studyhad begun.
To ensure uniformity of diagnosis, all cases were discussedagain at new diagnostic conferences held in 2001 and involvinga neurologist and a neuropsychologist who had not participatedin diagnostic conferences between 1980 and 1998.29 Dementiawas diagnosed according to the DSM-III-R criteria.28 Reducedparticipation in leisure activities was used to assess functionaldecline, but the leisure-activity scales were not availableto the raters assessing such decline. Disagreements betweenraters were resolved by consensus after the case was presentedto a second neurologist, with blinding maintained. Cases ofdementia were classified according to the criteria for probableor possible Alzheimer's disease published by the National Institutesof Neurological Disorders and Stroke and the Alzheimer's Diseaseand Related Disorders Association30 and the criteria for probable,possible, or mixed vascular dementia published by the Alzheimer'sDisease Research Centers of California.31
Statistical Analysis
Continuous variables were compared with use of either an independent-samplest-test or the Mann–Whitney U test, and categorical variableswere compared with use of the Pearson chi-square test.32 Inprimary analyses, we studied the association between cognitiveand physical activities and the risk of dementia and specifictypes of dementia using Cox proportional-hazards regressionanalysis to estimate hazard ratios, with 95 percent confidenceintervals.33 The time to an event was defined as the time fromenrollment to the date of a diagnosis of dementia or to thefinal contact or visit for subjects without dementia. All multivariatemodels reported include the following covariates unless otherwisespecified: age at enrollment, sex, educational level (high schoolor less vs. college-level education), presence or absence ofchronic medical illnesses, and base-line scores on the Blessedtest. Presence of the following self-reported chronic medicalillnesses was individually entered in the models: cardiac disease(angina, previous myocardial infarction, or cardiac failure),hypertension, diabetes mellitus, stroke, depression, and hypothyroidism.We also divided the study cohort into thirds on the basis oftheir scores on the two activity scales and determined the riskof dementia according to these groups. We examined the roleof individual leisure activities by comparing subjects who participatedin an activity several days or more per week (frequent participation)with subjects who participated weekly or less frequently (rareparticipation) and, in the full models, adjusted for participationin other leisure activities.
In secondary analyses, we examined the influence of base-linecognitive status and possible preclinical dementia. First, wesequentially excluded from the full models subjects in whomdementia developed during the first two, four, seven, and nineyears of follow-up in order to avoid confounding by a possibleinfluence of preclinical dementia on participation in leisureactivities. Second, we used linear mixed models controlled forage, sex, and educational level to assess the relation betweencognitive activities and base-line cognitive status and theannual rate of change in cognitive status.34 We analyzed verbalIQ as well as specific cognitive domains, including episodicmemory (with the Buschke Selective Reminding test [range ofscores, 0 to 72, with lower scores indicating worse memory]35and the Fuld Object-Memory Evaluation25) and executive function(with the Digit–Symbol Substitution subtest of the WechslerAdult Intelligence Scale [range of scores, 0 to 90, with lowerscores indicating worse cognition]).24 Each model included termsfor the cognitive-activity score, time, and the interactionbetween the two. The assumptions of the models were examinedanalytically and graphically and were adequately met.
Results
Demographic Characteristics
During 2702 person-years of follow-up (median follow-up, 5.1years), dementia developed in 124 subjects (Alzheimer's diseasein 61, vascular dementia in 30, mixed dementia in 25, and othertypes of dementia in 8). By the end of the study period, 361subjects had died, 88 subjects had dropped out (mean [±SD]follow-up, 6.6±4.9 years), and 20 subjects were stillactive. When the cohort was divided into thirds according tothe cognitive-activity score or the physical-activity score,no significant differences in the length of follow-up were foundamong these subgroups.
Table 1. Base-Line Characteristics of Subjects in Whom Dementia Developed and Subjects in Whom It Did Not.
A smaller proportion of the 361 subjects with a high-schooleducation or less than of the 108 subjects who had attendedcollege participated in reading (90 percent vs. 96 percent,P=0.05), writing (67 percent vs. 80 percent, P=0.01), doingcrossword puzzles (21 percent vs. 36 percent, P=0.001), andplaying musical instruments (7 percent vs. 15 percent, P=0.02).There was no difference according to educational level in theproportion of subjects who played board games or participatedin group discussions.
Leisure Activities
Among cognitive activities, reading, playing board games, andplaying musical instruments were associated with a lower riskof dementia (Table 2). Dancing was the only physical activityassociated with a lower risk of dementia. Fewer than 10 subjectsplayed golf or tennis, so the relation between these activitiesand dementia was not assessed.
Table 2. Risk of Development of Dementia According to the Frequency of Participation in Individual Leisure Activities at Base Line.
Cognitive Activities
When the cognitive-activity score was modeled as a continuousvariable (Table 3), the hazard ratio for dementia for a one-pointincrement in this score was 0.93 (95 percent confidence interval,0.89 to 0.96). Adjustment for the base-line score on the Blessedtest in a second model (Table 3) did not attenuate the association.Participation in cognitive activities was associated with areduced risk of Alzheimer's disease (hazard ratio, 0.93 [95percent confidence interval, 0.88 to 0.98]), vascular dementia(hazard ratio, 0.92 [95 percent confidence interval, 0.86 to0.99]), and mixed dementia (hazard ratio, 0.87 [95 percent confidenceinterval, 0.78 to 0.93]). The frequency of participation incognitive activities was related to the risk of dementia. Accordingto the model in which we adjusted for the base-line score onthe Blessed test, the hazard ratio for subjects with scoresin the highest third on the cognitive-activity scale, as comparedwith those with scores in the lowest third, was 0.37 (95 percentconfidence interval, 0.23 to 0.61) (Table 3).
Table 3. Risk of Dementia According to the Base-Line Scores on the Cognitive-Activity Scale and the Physical-Activity Scale.
In additional analyses, adjustment for intellectual status withthe use of the verbal IQ24 did not alter the association betweenparticipation in cognitive activities and the risk of dementia(hazard ratio, 0.92 [95 percent confidence interval, 0.87 to0.97]). Participation in cognitive activities was also associatedwith a reduced risk of dementia among the 361 subjects witha high-school education or less (hazard ratio, 0.94 [95 percentconfidence interval, 0.91 to 0.98]). The association of cognitiveactivities with dementia was not affected by adjustment forfunctional status, the restriction of the analyses to subjectswith scores of less than 5 on the Blessed test,21 or the exclusionof subjects who died during the first year after enrollment.
Physical Activities
The physical-activity score was not significantly associatedwith dementia, either when analyzed as a continuous variableor when the study cohort was divided into thirds according tothis score (Table 3).
Influence of Preclinical Dementia
The presence of preclinical dementia might reduce participationin leisure activities,6,7 leading to the overestimation of itsprotective influence. The association between the base-linecognitive-activity score and dementia was significant even afterthe exclusion of 94 subjects in whom dementia was diagnosedduring the first seven years after enrollment (hazard ratio,0.94 [95 percent confidence interval, 0.88 to 0.99]) (Table 4).The association was no longer significant after the exclusionof the 105 subjects in whom dementia was diagnosed during thefirst nine years after enrollment. However, only 19 subjectswere given a diagnosis of dementia after this point.
Table 4. Risk of Dementia per 1-Point Increment in the Base-Line Cognitive-Activity Score, with the Sequential Exclusion of Subjects in Whom Dementia Developed during the First Nine Years of Follow-up.
We used linear mixed models to examine the influence of participationin cognitive activities on the annual rate of change in cognitivefunction.34 In these models (Table 5), the term for the cognitive-activityscore represents the cross-sectional association between thecognitive activities and the scores on the selected tests administeredat enrollment. These results indicate that subjects with increasedparticipation in cognitive activities at entry had better overallcognitive status. Analysis with use of the term for time indicatesthat cognitive performance declines linearly as a function offollow-up time. The term for the interaction between the cognitive-activityscore and time represents the longitudinal effect of the base-linemeasure of participation in cognitive activities on the annualrate of decline in performance on the selected tests; this effectwas significant only for the tests of episodic memory. The estimatesshow that for a one-point increment in the cognitive-activityscore, the annual rate of decline in scores on the Buschke SelectiveReminding test is reduced by 0.043 point (P=0.02), and the annualrate of decline on the Fuld Object-Memory Evaluation is reducedby 0.006 point (P=0.04).
Table 5. Association of Participation in Cognitive Leisure Activities with Base-Line Cognitive Function and Rate of Change in Cognitive Function.
Discussion
This prospective, 21-year study demonstrates a significant associationbetween a higher level of participation in leisure activitiesat base line and a decreased risk of dementia — both forAlzheimer's disease and for vascular dementia. A one-point incrementin the cognitive-activity score, which corresponds to participationin an activity for one day per week, was associated with a reductionof 7 percent in the risk of dementia. The association betweencognitive activities and the risk of dementia remained robusteven after adjustment for potential confounding variables suchas age, sex, educational level, presence or absence of chronicmedical illnesses, and base-line cognitive status. Increasedparticipation in leisure activities was associated with a lowerrisk of dementia. Subjects with scores in the highest thirdon the cognitive-activity scale (more than 11 activity-days)had a risk of dementia that was 63 percent lower than that amongsubjects with scores in the lowest third.
We identified three possible explanations for the associationbetween greater participation in leisure activities and a decreasedrisk of dementia. First, the presence of preclinical dementiamay decrease participation in leisure activities. Second, unmeasuredconfounding may influence the results. Third, there may be atrue causal effect of cognitive activities. We used severalstrategies to test the hypothesis that reduced participationin leisure activities appears to be a risk factor for, but isin fact a consequence of, preclinical dementia. Adjustment forbase-line scores on cognitive tests, which predict dementia,did not alter the association between participation in cognitiveactivities and dementia. We have reported that an accelerateddecline in memory begins seven years before dementia is diagnosed.18The exclusion of subjects in whom dementia was diagnosed duringthe first seven years after enrollment should eliminate mostsubjects who had preclinical dementia at enrollment. However,participation in cognitive activities predicted dementia evenamong those in whom it developed more than seven years afterenrollment. Results from the linear mixed models that analyzedcognitive function over time corroborate the findings of previousstudies13,36 and show that increased participation in cognitiveactivities is associated with slower rates of cognitive decline,especially in terms of episodic memory.
Because of the observational nature of our study, there is apossibility of residual or unmeasured confounding. The observedassociation appears to be independent of educational level andintellectual level, which may influence the choice of leisureactivities. Perhaps reduced participation in leisure activitiesis an early marker of dementia that precedes the declines oncognitive tests.13 Alternatively, participation in leisure activitiesmay be a marker of behavior that promotes health. But the specificityof our findings for cognitive activities and not physical activitiesargues against this hypothesis. We did not study the effectof apolipoprotein E genotype, which may influence the ratesof cognitive decline.15,36 Hence, despite the magnitude andconsistency of the associations, our findings do not establisha causal relation between participation in leisure activitiesand dementia, and controlled trials are therefore needed.
If there is a causal role, participation in leisure activitiesmay increase cognitive reserve, delaying the clinical or pathologicalonset of dementia.8,37,38 Alternatively, participation in cognitiveactivities might slow the pathological processes of diseaseduring the preclinical phase of dementia. Our findings do notimply that subjects who were less active cognitively increasedtheir risk of dementia.
The role of individual leisure activities is not well known,since most studies have used composite measures. In a Frenchcohort, knitting, doing odd jobs, gardening, and traveling reducedthe risk of dementia.10 In the Nun Study, low density of ideasand low levels of grammatical complexity in autobiographieswritten in early life were associated with low cognitive testscores in later life.39 Reading, playing board games, playingmusical instruments, and dancing were associated with a lowerrisk of dementia in our cohort. There was no association between physical activity and the risk of dementia.Exercise is saidto have beneficial effects on the brain by promoting plasticity,increasing the levels of neurotrophic factors in the brain,and enhancing resistance to insults.40 Cognitive and physicalactivities overlap, and therefore it is not surprising thatprevious studies have disagreed on the role of physical activities.10,11,12,13,14,15Although physical activities are clearly important in promotingoverall health,41 their protective effect against dementia remainsuncertain.
Our study has several limitations. Ours was a cohort of volunteerswho resided in the community; whites and subjects older than75 years of age were overrepresented, as compared with the generalpopulation of those over 65 years of age, thus potentially limitingthe generalizability of our results. Although standard criteriaand well-established procedures were used to make diagnoses,some misclassification is inevitable. Time spent in each activitywas not directly measured, although the history was verifiedby family members or other informants. Duration and cognitivedemand are both important in the assessment of an activity.It is difficult to assign weights to the cognitive demands ofleisure activities, since such demands vary among activitiesand among the persons who engage in each activity. Leisure activitieswere arbitrarily classified as cognitive or physical. For instance,doing housework requires not only a certain functional statusbut also the ability to plan, prepare, and adapt to changesin circumstances and the environment. The leisure activitieswe studied reflect the interests of our cohort, and it is quitelikely that activities other than the ones we studied are alsoprotective.10,11,12,13,14,15
Supported by a grant (AGO3949-15) from the National Instituteon Aging.
Presented in part at the 127th annual meeting of the AmericanNeurological Association, New York, October 12–16, 2002.
Source Information
From the Einstein Aging Study (J.V., R.B.L., M.J.K., C.B.H., C.A.D., G.K., M.S., H.B.) and the Departments of Neurology (J.V., R.B.L., C.B.H., C.A.D., G.K., H.B.), Epidemiology and Social Medicine (R.B.L., C.B.H.), and Physical Medicine and Rehabilitation (A.F.A.), Albert Einstein College of Medicine, Bronx, N.Y.; and the Department of Psychology and the Center for Health and Behavior, Syracuse University, Syracuse, N.Y. (M.S.).
Address reprint requests to Dr. Verghese at the Einstein Aging Study, Albert Einstein College of Medicine, 1165 Morris Park Ave., Bronx, NY 10461, or at jverghes{at}aecom.yu.edu.
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