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Age and Ageing 1996.25201-205 Prevalence of Ageing-associated Cognitive Decline in an Elderly Population TUOMO HANNINEN, KEIJO KOIVISTO, KARI J. REINIKAINEN, EEVA-LIISA HELKALA, HILKKA SOININEN, LEENA MYKKANEN, MARKKU LAAKSO, PAAVO J. RIEKKINEN Summary Different diagnostic definitions have been proposed for use in the characterization of mild cognitive disorders associated with ageing. Previously, we reported a high (38.4%) prevalence of age-associated memory impairment (AAMI) using the National Institute of Mental Health criteria in an elderly population. Recently, a work group of the International Psychogeriatric Association proposed criteria for 'ageing-associated cognitive decline' (AACD). The objective of this study was to evaluate the prevalence of AACD in an elderly population. We examined 403 randomly selected subjects (68-78 years of age) with tests of memory, cognitive processing, attention, verbal and visuoconstructive functions and with a structured questionnaire for health status and subjective complaints of cognitive decline. In all, 26.6% of the subjects (24.4% of women, 30.1% of men) fulfilled the AACD criteria. The prevalence was slightly related to age and education. The rate was lowest in the oldest age group of 75-78 years (20.5%) and highest in the age group of 71-74 years (30.5%). Subjects with less than 4 years of education had the lowest (14.3%) and subjects with more than 6 years of education had the highest rate (29.4%) for AACD. However, the differences between these subgroups were not statistically significant. These results suggest that the prevalence of AACD is lower than that of AAMI. As AAMI tends to identify a very heterogeneous subject group, the AACD diagnosis, which takes into account age and education specific norms in its inclusion criteria, might prove superior to AAMI in differentiating a meaningful subgroup from an elderly population both for research purposes and in clinical settings. Introduction The decline in memory and other cognitive abilities during ageing is well documented [e.g. 1,2]. However, the diagnostic classifications aimed to characterize elderly individuals with different degrees of cognitive decline (but not demented) are not established. Recently, a working party of the International Psycho- geriatric Association (IPA) in collaboration with the World Health Organization (WHO) proposed diagnos- tic criteria for 'ageing-associated cognitive decline' (AACD) to categorize a group of subjects with cognitive decline falling short of dementia [3]. The criteria include the presence of subjective gradual cognitive decline (for at least 6 months) and objective evidence of abnormal performance in any principal domain of cognition, i.e. memory and learning, atten- tion and concentration, thinking, language or visuo- spatial functioning. The abnormality is defined as performance at least one standard deviation (SD) below the age and education norms in well standardized neuropsychological tests. Furthermore, there must be no evidence of any medical condition known to cause cerebral dysfunction. Thus, the AACD diagnosis identifies persons with subjective and objective evi- dence of cognitive decline which does not impair function to warrant a diagnosis of dementia. The criteria leave open the question of progression. For some subjects, AACD may precede dementia, whereas for others it may be a relatively stable condition. The AACD diagnosis is related to 'age-associated memory impairment' (AAMI), a condition character- ized in the criteria proposed by a working group of the National Institute of Mental Health [4]. However, the AAMI diagnosis is based on a less comprehensive evaluation which takes into account memory function only. The AAMI criteria also differ from the AACD criteria in that the subjects are classified as having AAMI if they score 1 SD below the mean of younger adults (not people of their own age) in a standardized memory test. In spite of many supporting reports [5—8] and the high prevalence of AAMI [9], the significance of this condition has remained controversial [10—12]. AACD has to be differentiated also from 'mild cognitive disorder' (MCD), a classification included in the research criteria for ICD-10 by WHO [13]. This diagnosis is used only when there is an indication of a disease or condition known to cause cerebral by guest on July 13, 2011 ageing.oxfordjournals.org Downloaded from

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Age and Ageing 1996.25201-205

Prevalence of Ageing-associated CognitiveDecline in an Elderly PopulationTUOMO HANNINEN, KEIJO KOIVISTO, KARI J. REINIKAINEN,EEVA-LIISA HELKALA, HILKKA SOININEN, LEENA MYKKANEN,MARKKU LAAKSO, PAAVO J. RIEKKINEN

SummaryDifferent diagnostic definitions have been proposed for use in the characterization of mild cognitive disordersassociated with ageing. Previously, we reported a high (38.4%) prevalence of age-associated memory impairment(AAMI) using the National Institute of Mental Health criteria in an elderly population. Recently, a work groupof the International Psychogeriatric Association proposed criteria for 'ageing-associated cognitive decline'(AACD). The objective of this study was to evaluate the prevalence of AACD in an elderly population. Weexamined 403 randomly selected subjects (68-78 years of age) with tests of memory, cognitive processing,attention, verbal and visuoconstructive functions and with a structured questionnaire for health status andsubjective complaints of cognitive decline. In all, 26.6% of the subjects (24.4% of women, 30.1% of men) fulfilledthe AACD criteria. The prevalence was slightly related to age and education. The rate was lowest in the oldestage group of 75-78 years (20.5%) and highest in the age group of 71-74 years (30.5%). Subjects with less than 4years of education had the lowest (14.3%) and subjects with more than 6 years of education had the highest rate(29.4%) for AACD. However, the differences between these subgroups were not statistically significant. Theseresults suggest that the prevalence of AACD is lower than that of AAMI. As AAMI tends to identify a veryheterogeneous subject group, the AACD diagnosis, which takes into account age and education specific norms inits inclusion criteria, might prove superior to AAMI in differentiating a meaningful subgroup from an elderlypopulation both for research purposes and in clinical settings.

IntroductionThe decline in memory and other cognitive abilitiesduring ageing is well documented [e.g. 1,2]. However,the diagnostic classifications aimed to characterizeelderly individuals with different degrees of cognitivedecline (but not demented) are not established.Recently, a working party of the International Psycho-geriatric Association (IPA) in collaboration with theWorld Health Organization (WHO) proposed diagnos-tic criteria for 'ageing-associated cognitive decline'(AACD) to categorize a group of subjects withcognitive decline falling short of dementia [3]. Thecriteria include the presence of subjective gradualcognitive decline (for at least 6 months) and objectiveevidence of abnormal performance in any principaldomain of cognition, i.e. memory and learning, atten-tion and concentration, thinking, language or visuo-spatial functioning. The abnormality is defined asperformance at least one standard deviation (SD)below the age and education norms in well standardizedneuropsychological tests. Furthermore, there must beno evidence of any medical condition known to causecerebral dysfunction. Thus, the AACD diagnosis

identifies persons with subjective and objective evi-dence of cognitive decline which does not impairfunction to warrant a diagnosis of dementia. Thecriteria leave open the question of progression. Forsome subjects, AACD may precede dementia, whereasfor others it may be a relatively stable condition.

The AACD diagnosis is related to 'age-associatedmemory impairment' (AAMI), a condition character-ized in the criteria proposed by a working group ofthe National Institute of Mental Health [4]. However,the AAMI diagnosis is based on a less comprehensiveevaluation which takes into account memory functiononly. The AAMI criteria also differ from the AACDcriteria in that the subjects are classified as havingAAMI if they score 1 SD below the mean of youngeradults (not people of their own age) in a standardizedmemory test. In spite of many supporting reports [5—8]and the high prevalence of AAMI [9], the significanceof this condition has remained controversial [10—12].

AACD has to be differentiated also from 'mildcognitive disorder' (MCD), a classification includedin the research criteria for ICD-10 by WHO [13].This diagnosis is used only when there is an indicationof a disease or condition known to cause cerebral

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T. HANNINEN ET AL.

dysfunction. Yet another related concept is included inDSM-IV [14] as 'age-related cognitive decline' anddefined as 'an objectively identified decline in cognitivefunctioning consequent to the ageing process that iswithin normal limits given the person's age'.

The purpose of this study was to evaluate theprevalence rate of AACD in a randomly selectedsample of elderly people by applying the criteriaproposed by the IPA working party. The associationsof age, sex and education with prevalence rates werealso evaluated. Furthermore, we examined the diag-nostic value of a neuropsychological test battery foridentifying AACD subjects.

Subjects and MethodsA random sample of 592 persons, 68-78 years of age, wasdrawn from the Kuopio population register. Of these subjects79 had died and 11 had moved outside the study area beforethey were contacted. Of the remaining 502 subjects, 403(80.3%) were evaluated. Of those not participating in thestudy, 17 were too ill to participate, 55 refused to participateand 27 could not be contacted. The study population has beendescribed previously as a part of a report on the prevalence ofAAMI [9]. The mean age of the participants was 71.3 years(SD 3.1, range 68-78). Women were somewhat older thanmen (71.9 vs. 71.0). The mean duration of formal educationwas 6.7 years (SD 3.4, range 0—18) with no difference betweenwomen and men. The proportions of women, 246 (61%), andmen, 157 (39%), are similar to those in the total population(64%/36%) for this age group in the study area. The mostfrequent previous diagnoses were coronary heart disease(34%), hypertension (33%), cardiac arrhythmia (17%) andtransient ischaemic attack (16%). The following diseases withpossible direct negative effect on cognitive functions wereconsidered as exclusion of AACD: stroke (7%), brainhaemorrhage (2%), diabetes (7%), psychiatric disorder (9%),malignancy (6%). The participants who scored poorly in theneuropsychological tests were invited to the further evalua-tion for possible dementia. A total of 23 (5.7%) subjectsfulfilled the DSM-III criteria of dementia (unpublished data)which also was an exclusion for AACD. Of the 403participants, 402 had data complete enough for the classifica-tion of AACD and are included in the analyses. All subjectsparticipating in the study gave their informed consent. TheEthics Committee of the University of Kuopio approved thestudy.

All participants underwent a structured interview fordemographic information, medical history, current medica-tion, smoking and alcohol consumption, and subjectiveassessment of memory disturbances and depression duringthe past year. Subjective complaints of memory loss wererecorded by the Memory Complaint Questionnaire (MAC-Q)[15], in which a score of 25 or over is considered as indicatingsubjective memory loss. A test battery of brief neuropsycho-logical tests was used to evaluate different cognitive domainsessential for the identification of AACD. The following scoresof tests were used: (1) Memory: The Buschke— Fuld SelectiveReminding Test (BSRT) [16], the score is the total recall in sixtrials (max. 60); (2) Attention: The Trail-Making Test,Version A (TMT-A) [17], the score is the time in seconds(max. time limit 150 s.); (3) Effortful cognitive processing: TheTrail-Making Test, Version C (TMT-C) [17, 18], the score isthe time in seconds (max. time limit 300 s.); (4) Verbal ability:The Verbal Fluency Test, animal category (VFT) [19]. the

score is the total number of names of animals produced during1 minute; and (5) Visuoconstructive function: Copying of thefigures of Russell's adaptation of the Visual Reproduction Test(CVRT) [20] from the Wechsler Memory Scale (WMS), thescore is the number of components present in the drawings(max. 21). The presentation of tests in detail, the validity of thebattery and the associations of age and sex with testperformance have been described previously [18]. Further-more, a neuropsychological battery including the Mini-MentalState Examination [21], the Benton Visual Reproduction Test[22] and the Paired Associated Learning sub-test from theWMS [23] was used to diagnose AAMI as reported earlier indetail [9].

The evaluations were carried out by a trained nurse,psychologist, or physician in the Memory Research Unit ofthe Department of Neurology in Kuopio University. Aninstructional manual was used to standardize the interviewand presentation of tests.

To determine the cut-off points for neuropsychologicaltests appropriate for different levels of education, a subgroupof 278 healthy subjects without diseases which couldpotentially affect cognitive functions was identified from thetotal sample. The cut-offs for the TMT-A and TMT-C werecalculated as the mean score plus 1 SD and for the BSRT,VFT and CVRT as the mean minus 1 SD in each of threeeducational subgroups of these healthy subjects: minimaleducation (3 years or less), elementary school education (4—6years) and secondary school or high school education (7 yearsor more). Previous studies have used these same categoriesbased on the Finnish educational programme for the subjects'age group [18, 24]. The prevalence of AACD was calculatedseparately for each educational subgroup. The association ofage with the prevalence of AACD was evaluated within threecategories: subjects of 67-70, 71—74 or 75-78 years of age.

The data were analysed by using the SPSS-PC + V.4.0.1software. The x2 test was used to evaluate the differences inAACD prevalence between the subgroups of the studypopulation. The results for continuous variables are given asa mean with SD.

ResultsSubjective complaints of cognitive decline in MAC-Qwere found in 79.8% (320/402) of the subjects. The cut-off points for neuropsychological tests as determined ina subgroup of 278 healthy subjects (without exclusiondiseases) in three different educational subgroups arepresented in Table I. According to these cut-off points,a total of 107 subjects out of 402 (26.6%) fulfilled theAACD criteria. The prevalence of AACD tended to behigher in men (30.1%) than in women (24.4%) (TableII). Age-specific prevalence rates were: 25.2% in the agegroup 68—70 years, 30.5% in the age group 71-74 years,and 20.5% in the age group 75-78 years. Theprevalence rates did not differ significantly in thevarious age groups. Education-specific prevalencerates varied in the three education groups, but thedifferences were not statistically significant. The sub-jects with 3 years or less of education had a prevalencerate of 14.3%, in subjects with 4—6 years of education itwas 26.2%, and in subjects with 7 years or moreeducation the prevalence rate was 29.4% (Table III).

No major differences were found in the ability of

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Table I. The education-specific scores, mean (SD), incriterion tests in a healthy subgroup (n = 278) of the studypopulation and cut-off points for AACD classification

Table III. Education-specific prevalence rates for AACDaccording to the International Psychogeriatric Associationworking party criteria in the study population

Education in years Education in years Number Rate %

Test0-3(n =

4-6(n= 138)

7 or more(n = 126)

BSRTCut-off

TMT-ACut-off

TMT-CCut-off

VFTCut-off

CVRTCut-off

28.5 (6.3)22

109.3 (37.4)147263.7(62.1)30015.3 (4.4)11

14.2 (3.4)11

32.6 (7.6)25

82.0(31.5)114

232.8 (72.0)300

16.3(5.1)1116.3 (2.4)14

35.6 (8.4)2763.0 (26.9)90

168.9 (79.0)248

19.4(5.6)14

17.4(2.3)15

neuropsychological tests to identify subjects withAACD. The BSRT identified 23.6% (89 out of 377subjects completing this test), the TMT-A identified19.9% (79/396), the T M T - C identified 23.3% (87/376),the VFT identified 19.3% (76/393) and the CVRTidentified 22.5% (89/396) of the subjects as havingAACD. Of those who were classified into AACDcategory, 60.7% (65/107) met the criteria due to one testonly. Subsequently, 21.5% (23/207), 11.2% (12/107),5.6% (6/107) and 0.9% (1/107) were classified as havingAACD with two, three, four or all five tests. For thosewho met the criteria in one test only, this test was theBSRT in 26.2% (17/65), VFT in 21.5% (14/65), CVRT

Table II. Age- and sex-specific prevalence rates for AACDaccording to the International Psychogeriatric Associationworking party criteria in the study population

Age group Number Rate %

Men68-7071-7475-78Total

Women68-7071-7475-78Total

Combined68-7071-7475-78Total

21/7521/595/22

47/156

20/8825/9215/6660/246

41/6346/15120/98

107/402

28.035.622.730.1

22.727.222.724.4

25.230.520.526.6

0-34-67 or moreTotal

4/2855/21048/163

107/402

14.326.229.426.6

in 20.0% (13/65), T M T - C in 20.0% (13/65), and T M T -A in 12.3% (8/65) of the cases.

Discussion

In the present study, the prevalence rate for AACD insubjects aged 68-78 years was 26.6% according to theIPA criteria. Sex, age and education seemed to havesome association with the prevalence of AACD,although the differences between subgroups were notsignificant. The prevalence was higher in men (30.1%)than in women (24.4%). The highest rate was found inthe group of 71—74-year-old subjects and the lowestrate in subjects aged 75—78 years. The subgroup withonly elementary education had the lowest rate and thebest educated subgroup had the highest rate.

To our knowledge, this is the first study on theepidemiology of AACD using the IPA criteria. How-ever, some studies have reported data concerning theepidemiology of a related concept, AAMI. Theprevalence of AAMI reported in previous studies hasbeen higher than the prevalence of AACD found in thepresent study. In our own study, the prevalence ofAAMI was 38.4% [9]. A study by Lane and Snowdon[7] reported a 34.9% prevalence rate for AAMI. In arecent Spanish study [25] the prevalence was muchlower: 7.1%. However, the definition of AAMI in thelatter study was different, resembling the definition ofMCD for which also a low prevalence rate, 4%, wasrecently reported [26]. Considering AAMI, someresearchers have estimated that most people over 50are affected to some degree [27]. It has been proposedthat AAMI might be an intermediary state in thecontinuum from normal ageing to Alzheimer's disease[28]. However, the condition has been suggested to berather stable [29] and in a population-based follow-upstudy it was shown to identify a very heterogeneoussubject group with only very slightly elevated incidenceof dementia [30]. Because of this markedly lowerprevalence rate, AACD might identify a more homo-geneous group of elderly individuals who have a higherrisk of developing dementia. However, this has to beconfirmed by follow-up studies with AACD subjects.

The finding of the present study that AACD is morefrequent in men (30.1%) than in women (24.4%) is inaccordance with a previous study of AAMI prevalencewhich also reported higher rates in men than in women

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[9]. The interpretation of the association of age with theprevalence is complicated. We found that the rate washighest in the intermediate subgroup of 71—74-year-oldsubjects. In a previous study, the prevalence of AAMIdeclined with age [9] while the prevalence of Alzheimer'sdisease has been shown to increase with age [31, 32].Thus, the time course of the changes of prevalence ratesfor AACD in the present study does not agree with thosereported in the AD and AAMI studies. However, weneed to note that the age range in our population wasrather narrow (68-78 years) and the differences inprevalence rates were small. Since the AACD criteriaproposed by the IPA do not include any age restrictions,further studies are needed to provide data about theprevalence of AACD in younger and older subjects.

The individuals with more education appeared to bemore frequently classified as having AACD. Thesubgroups divided according to education were notequal in size as the subgroup with minimal educationconsisted of only 28 subjects. Given the diverseduration of education which different individuals inthis age group have received, the classification is logicaland it has been utilized also in previous studies [18, 24].However, owing to the small size of the subgroup withminimal education in this study, it is difficult to drawdefinite conclusions about any effect of education on theprevalence of AACD.

In addition to epidemiological aspects, our resultselucidate the psychometric characteristics of AACD.We used a subgroup of healthy subjects from our studypopulation to establish the education specific norms forthese neuropsychological tests. In accordance withmany previous studies [18, 33, 34], we observed anassociation of education with test performance; the cut-off score for every neuropsychological test was highestin the best educated subjects. Thus, our resultsemphasize the need for well adjusted norms to beused in the neuropsychological tests in studies onAACD. This is further underscored by the effect ofcultural factors on psychometric tests and scales [24,35].

The AACD criteria require that there has to be asubjective report by the individuals that their cognitivefunction has declined. We found almost 80% of thesubjects reporting a deterioration when assessed withthe MAC-Q. The subjective complaints were proposedalso as a part of the AAMI diagnosis, but this hasremained a controversial issue in the AAMI literature[12]. For this study, it could be confounding that theMAC-Q is restricted only to memory. However, as theIPA working party pointed out, memory may be thecognitive domain about which elderly subjects mostfrequently complain [3]. Another characteristic of theMAC-Q which undoubtedly increases the number ofidentified subjects is that it asks the subjects to comparetheir present memory with their own memory in thepast, instead of some other standard, such as people oftheir own age. Thus, the frequency of subjectivecomplaints of cognitive decline in this study is morelikely to be exaggerated than understated, though

complaints in other cognitive domains than memorywere not surveyed. Furthermore, we need to note thatin the AACD criteria reports of decline by reliableinformants can be used instead of subjective com-plaints. In the present study, however, the reports byinformants were not evaluated. In further studiesinvolving AACD subjects, the methods for assessingsuch subjective or informant-based reports aboutcognitive decline need critical evaluation.

Each of the neuropsychological tests in the batteryassigned a similar number of subjects to the AACDcategory. The BSRT, a memory test, was the mostsensitive in classifying subjects as having AACD. Whenwe used only one test to assess each cognitive domain,about 60% of the AACD subjects met the classificationon the basis of one test only. This suggests that thenumber of tests in the battery is critical for theidentification of AACD. We may speculate that if thenumber of tests was increased also the frequency ofAACD cases would be elevated.

The selection of tests for the neuropsychologicalevaluation undoubtedly influences the prevalence ofAACD. In the present study, we selected a test batterywhich could provide as good an overall description ofcognition as possible by an easily administered briefexamination. To keep the test session short, weemployed only one test for each cognitive domain.However, each test employed can cover only one part ofthe wide spectrum of cognitive abilities. Although theVFT reflects naming skills, it gives only a limitedassessment of verbal abilities. It is also related tosemantic memory and attention. The CVRT is a test ofvisuoconstructive function but does not include spatialcomponents. In addition to attention, TMT-A involvesmotor function which may obscure the results espe-cially in elderly subjects. The TMT-C assesses effortfulprocessing and problem-solving in a stressing situation,but like the TMT-A it is dependent also on attentionand motor performance. Some other test which had notime-limiting and motor components would be betterthan the TMT-C to assess 'pure' problem-solving. TheBSRT has been considered as a quite accurate measureof memory. The major advantage of our test battery isthat all the tests are well known and widely used in bothresearch and clinical settings.

In conclusion, the present study reports the pre-valence of AACD to be lower than that of AAMI. Thissuggests that AACD might be better than AAMI indifferentiating those who have a genuine cognitivedecline that possibly justifies pharmacological inter-vention trials or who should be observed in follow-upstudies for the development of dementia from subjectswith 'normal' ageing. Therefore, AACD might alsoturn out to be clinically more relevant than AAMI.However, data from follow-up studies are neededbefore firm conclusions can be drawn about therelevance of this diagnostic category. Furthermore,this study emphasizes the need for obtaining carefullyadjusted norms in psychometric tests to be used inneuropsychological assessment of elderly populations.

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AcknowledgementThis study was supported by grants from the MedicalResearch Council of the Academy of Finland.

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Authors' addressesT. Hanninen, K. Koivisto, K. Reinikainen, E-L. Helkala,H. Soininen, P. J. RiekkinenDepartment of Neurology,

L. Mykkanen, M. LaaksoDepartment of Medicine,

University of Kuopio,P.O. Box 1627,70211 Kuopio, Finland

Received 20 August 1995

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