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[Original Article]

Alzheimer Disease & Associated DisordersIssue: Volume 17(3), July/September 2003, pp 139-145Copyright: © 2003 Lippincott Williams & Wilkins, Inc.Publication Type: [Original Article]ISSN: 0893-0341Accession: 00002093-200307000-00003Keywords: risk factors, education, electromagnetic field, EMF, Turkey

Risk Factors for Alzheimer Disease: A Population-Based Case-Control Study in Istanbul, TurkeyHarmanci, Hande MD; Emre, Murat MD; Gurvit, Hakan MD; Bilgic, Basar MD; Hanagasi, Hasmet MD; Gurol, Edip MD; Sahin, Huseyin MD; Tinaz, Sule MD

Author InformationFrom the Department of Public Health (Dr Harmanci), Marmara University Medical Faculty, and the Department of Neurology (Drs Emre, Gurvit, Bilgic, Hanagasi, Gurol,

Sahin, and Tinaz), Istanbul University, Istanbul Medical Faculty, Istanbul, Turkey.Received for publication August 7, 2002; accepted March 8, 2003.This project was supported by a non-restricted research grant from Novartis A.S Turkey.Reprints: Dr. Hande Harmanci, Marmara University Medical Faculty, Department of Public Health, Haydarpasa 81326, Istanbul, Turkey (e-mail:

hharmanci@marmara.edu.tr).

Summary:

The objective is to study risk factors for Alzheimer disease (AD) in Istanbul, Turkey. This is a population-basedcase-control study. We screened people over age 70 in the community for cognitive impairment. The screen positivesand a proportion of screen negatives underwent neurologic examination in the second phase. Cases were 57“probable” AD patients and controls were 127 cognitively normal individuals identified by neurologic examination.Odds ratios (OR) were calculated using multivariate logistic regression analysis. Having a university/college degreehad a protective effect on AD risk (OR = 0.10, 95% confidence interval [CI] = 0.02–0.50). Exposure to occupationalelectromagnetic field had an OR of 4.02 (95% CI = 1.02–15.78). Use of electricity for residential heating also showedelevated risk (OR = 2.77, 95% CI = 1.12–6.85). Our results suggest that having a higher education is protective from ADand that electromagnetic field exposure at work or at home is a significant risk factor.

Alzheimer disease (AD) is becoming a major public health problem as populations age and the proportion of theaged constitute a growing proportion of the population. The high prevalence 1–3 and incidence rates, 4–5 combinedwith the social and economic burden, rank AD high in the list of important health problems of the modern society.

A steady stream of studies has been published for the risk factors of AD for the last two decades. A review article6 groups these studies into four types: those that have examined familial and genetic factors (gender, family history,APOE, etc), clinical/illness-related risk factors (Down syndrome, thyroid disease, head injury, etc), exposure toenvironmental hazards (estrogen replacement therapy, nonsteroidal anti inflammatory drugs [NSAIDs], tobacco,alcohol, electromagnetic fields (EMFs), aluminum, etc.), and sociodemographic characteristics (education,occupation, rural area of residence, household characteristics, etc) as risk factors. Among those, only age andpositive family history are considered as definite risk factors.

Most of the publications on AD have come from the developed world. Developing countries have not been able toreport reliable data on dementias and AD, possibly because they have less resources for research and health servicesfor the care of the elderly. The Indo-U.S. study 7 is one of the few from a developing country, and it reports lowerprevalence figures compared with developed nations, with possible explanations of low overall life expectancy, shortsurvival with the disease, and low age-specific incidence potentially due to differences in the underlying distributionof risk and protective factors compared with populations with higher prevalence. One prospective study 8 examinesincidence rate differences between Nigerians and African Americans living in Illinois and reports significantdifferences between the two populations with Nigerians having lower incidence rates.

We here present the first AD risk factor study from Turkey as part of the Turkish Alzheimer Prevalence Study.

METHODS

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METHODS

This study was carried out in Kadikoy, Istanbul, Turkey. The sample for the cross-sectional part of this study wasdetermined as 1067 individuals 70 years of age or older randomly selected from population registries (records of themuhtars'1 list). After obtaining addresses from muhtars, all subjects were visited in their homes by a group of trainedinterviewers. Those who were not found at home were visited two more times. Assuming a community prevalence of50%, we determined that the sample size offered 95% confidence that the prevalence estimates would be within 3%of the true rate; 95.5% (n = 1019) of the sample population agreed to participate in the study.

The community prevalence study followed a two-stage design. Participants older than 70 years, living in thecommunity, were screened for cognitive impairment using the Turkish version 9 of the Mini Mental State Examination(MMSE) 10 and were asked to undergo a neurologic examination if the screening test indicated cognitive impairment.Cognitive impairment was defined as an MMSE score of <24 of 30 in the illiterate 11 and 25 of 30 in the literategroup; 223 of 1019 participants tested positive in the first phase; 69.5% of the screen positives (n = 223) accepted theclinical examination. We aimed to reach 5% of the cognitively normal screening population and include them in theclinical evaluation; we reached 8.3% at the end of the study (n = 58). A sensitivity analysis was done among 281participants who attended the clinical evaluation. Among the 57 participants who were diagnosed as “probable” ADduring clinical evaluation, 56 also tested positive with the MMSE. Among the 177 participants who were diagnosed asclinically normal during clinical evaluation, 56 also tested negative with the MMSE. Taking the clinical evaluation asthe golden standard, the sensitivity of the MMSE is 98.3% and the specificity is 31.6%.

Diagnostic criteria for dementia followed the Diagnostic and Statistical Manual of Mental Disorders12 to definedementia, as well as the National Institute of Neurologic and Communicative Disorders and Stroke and theAlzheimer's Disease and Related Disorders Association criteria for possible and probable AD. 13

Risk Factor Study

Of the 281 individuals examined by a team of three neurologists, 57 were diagnosed as “probable” AD, 11 as“possible” AD, 79 had other cognitive disorders, and 127 subjects were diagnosed as cognitively normal. We selectedthe “probable” AD subjects as cases (n = 57) and “cognitively normal” individuals as controls (n = 127).

Data Collection

Risk factor questionnaires were obtained by face-to-face in-home interviews between trained interviewers andproxy informants for both cases and controls. Proxy informants were defined as the spouse, adult children, and anyother people who have spent the majority of their adult lives living in the same residence as the subject. Wecollected data to test some of the major proposed risk factors in the literature (education, occupation, place ofresidency, alcohol use, history of stroke, history of general anesthesia, current use of NSAIDs) and added two others(history of tuberculosis and type of domestic heating) that we thought may be important in Turkey.

Independent Variables

Level of education was recorded as the school last graduated. Those who did not graduate from primary school(5 years), whether literate or illiterate, were grouped under “no schooling.” Some of the categories were combinedtogether to allow for bigger numbers to work with (no schooling category includes 27 illiterates and 20 literates;secondary education category includes 21 junior high school graduates and 35 high school graduates; and highereducation category includes 10 vocational school graduates and 19 university graduates). Job held for the longesttime was recorded as open-ended responses and later classified by the first author, blinded to the case or controlstatus, according to the ISCO-88 International Standard Classification of Occupations. 14 These occupations werethen blindly regrouped into medium to high EMF exposure according to the criteria proposed by Sobel et al., 15–16farmers, and others. Current use of NSAIDs was assessed by medicine chest examination in residence of participant byinterviewers unaware of the research hypotheses. Alcohol use was assessed as ever/never use; ever users were askedof the duration and amount of use. Participants were asked where they lived for the longest part of their lives andanswers were recorded as rural or urban by self-report. Type of primary residential heating in life was assessed bytwo questions: method for heating the house and method for heating the bath water. These two were regrouped intoone as use of electrical appliances in house or water heating versus use of other methods.

Analysis

The [chi]2 test is used for comparison of proportion of various risk factors, and Student t test is used to compare

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The [chi]2 test is used for comparison of proportion of various risk factors, and Student t test is used to comparemean ages between case and control groups. The strength of association between the putative risk factors and AD isdescribed by odds ratios (OR) and 95% confidence intervals (CI). 17 Crude ORs were calculated from univariate

frequency tables. Multiple logistic regression was used to obtain adjusted effect estimates. The likelihood ratio [chi]2

test was used for significance of odds ratios in the multivariate analyses. Two-sided significance tests and confidenceintervals were used.

RESULTS

Table 1 shows the distribution of various factors between cases and controls. The mean age (standard deviation)was 77.3 (6.0) for the cases and 76.1 (5.8) for the controls (p = 0.20). There were more women than men in bothcases and controls. Controls were significantly more educated than cases (21.3% of controls are college/universitygraduates compared with only 3.5% of cases).

TABLE 1. Distribution of Various Factors Between Case and Control Groups

Univariate and multivariate odds ratios for gender, level of education, occupational group, urban/ruralresidency, alcohol use, use of electricity for residential heating, history of tuberculosis, stroke and generalanesthesia, and current use of NSAIDs are given in Table 2.

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TABLE 2. Odds Ratios With 95% Confidence Intervals for Alzheimer Disease Associated With Various FactorsOR, oddsratio; CI, confidence interval.*Stepwise backward logistic regression analysis.

The crude ORs for education level were significantly associated with AD risk. We took the “no schooling” groupas the reference category and showed that having a university/college degree had a protective effect on AD risk witha crude OR of 0.12 (95% CI = 0.03–0.56). This association keeps quite stable in the multivariate model (OR = 0.10; 95%CI = 0.02–0.50).

Farmers and those with medium to high EMF exposure had crude ORs of 10.38 (95% CI = 1.13–95.31) and 3.98(95% CI = 1.05–14.42), respectively. Adjustment of ORs (multivariate modeling) increased the OR of the medium/highEMF-exposed group to 4.02 (95% CI = 1.02–15.78), resulted in a loss of significance in the farmers group, and resultedin a significant difference in use of electricity for residential heating (OR = 2.77; 95% CI = 1.12–6.85).

DISCUSSION

Cross-sectional case-control studies have largely been replaced by prospective cohort studies in the literaturedue to biases inherent in their design. However, they are sometimes the best that can be accomplished with limitedresources and are a very reasonable way of generating hypotheses for further study, particularly in populations beingstudied for the first time, which is the case in this study.

One of the major strengths of this study is that it is population based, with cases and controls drawn from thesame population. This allows for generalization of the study results to the population at large. Cases wereascertained by the use of established diagnostic criteria for dementia and AD. All controls were assessed by the sameteam and were diagnosed as cognitively normal. Exposures to risk factors were symmetrically ascertained in case andcontrol groups by non-health personnel-interviewers who were blind both to the hypotheses of the study and to the

diagnostic status of the subjects.

Four large incidence studies show an increased incidence of AD in women in the later years of life. Acollaborative study in Europe, 5 the EURODEM study, 18 the Rotterdam study, 19 and the PAQUID project 20 allindicate that incidences are similar up to the age 85 to 90 years. After this age, however, the incidence is higher inwomen. We did not find gender as one of the risk factors for AD. This is probably due to the fact that our sample isrelatively young with only 4 people older than 90 years and an average age (SD) of 77.3 years (6.0 years) for the casesand 76.1 years (5.8 years) for the controls. This may also be the reason that age did not appear as a risk factor in thisstudy.

The evidence about relationship between education and AD is mixed. Case-control 1 and longitudinal studies 20–23 provide evidence for an inverse association between education and AD. The Kungsholmen project 23 reports that alow level of education is related to an increased incidence of AD. The Rotterdam study 24 reports an inverse dose-response relation between education and AD. An East Boston study 21 reports a decrease of AD risk by approximately17% for each year of education. Still, the EURODEM 25 study reports increased risk with low levels of educationconfined to women only. One study 26 investigates whether loss to follow-up in incidence studies, and use of MMSEfor cognitive level screening, influence the association between level of education and AD risk. They conclude thatthese factors cannot completely explain the association and that a low level of education is indeed predictive ofincident AD. We found that having a university/college degree may be protective from acquiring AD. The exactmechanism of this protective effect is not known. Education may be a surrogate for socioeconomic status, whichitself may be a risk factor through worse living conditions, exposure to various environmental factors, etc. It ispossible that the association between level of education and AD reflects a general association of poor health withlower socioeconomic status. In a cohort study, 21 however, level of education was identified as a risk factorindependent of income and occupational prestige levels. Nevertheless, the authors propose that this may be due tothe ease of measurement of level of education compared with the other variables. Another proposed explanation for

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the ease of measurement of level of education compared with the other variables. Another proposed explanation forthe protective effect of education is the “reserve hypothesis,” which originated from the first large-scaleepidemiological survey of dementia reporting an inverse association of AD with education. 27 Simply put, the reservetheory suggests that education assumes some form of positive effect in brain development during childhood andadolescence, which then creates a “reserve” for later functional loss. This reserve requires that more pathology ispresent before memory begins to be affected. Patients with higher education are thought to be able to maximizeperformance through differential recruitment of brain networks, which may reflect the use of alternate cognitivestrategies. 28 One other explanation may be that educational attainment correlates to a greater or lesser extent withvirtually every cognitive test including the MMSE. In other words, people may perform poorly in a cognitive test notbecause of a hidden dementing disorder but because of a limited educational background. We controlled for this inour study by applying different cutoff points for the literate and illiterate groups in the MMSE. 11

Those who agreed to participate in the clinical evaluation were comparable in age and sex in both screen-positive and -negative subjects. There were, however, more people with higher levels of education amongparticipants in the screen-negative group compared with refusers in the same group. This limitation exists in thisstudy since power does not permit further analysis of this situation.

Starting with the first article by Sobel et al. in 1995, 15 a number of studies addressed the possibility of anassociation between EMF exposure and AD. Ahlbom pooled five of these articles in a meta-analysis aiming to identify

a more realistic risk estimate of AD in relation to EMF exposure. 29 This meta-analysis suggests that there is anassociation between EMF exposure and AD risk (pooled relative risk = 2.2, 95% CI = 1.5–3.2). The author, however,warns that this risk estimation is mainly confined to two studies whose cases are clinic-based and the populationsthat the controls are chosen from are undefined. This makes it impossible to control for selection bias. Another study30 investigating mortality due to neurodegenerative diseases and occupation demonstrates increased proportionatemortality ratios for AD among occupations that could have higher exposure to EMF. In our study, we found anincreased risk for the medium/high EMF-exposed group (OR = 4.02, 95% CI = 1.02–15.78) though with a wideconfidence interval due to small numbers. The strength of this result is in the nature of the study; it is populationbased and less prone to selection bias. The weakness, however, is the small numbers (Table 3) in the EMF-exposedgroup that did not allow for further analysis to test for any differences between groups of gender and duration ofoccupation. Another weakness is that EMF exposure classification data are not available for occupational groups inTurkey. Therefore, we applied the Sobel et al. (1995) criteria to our data, assuming that they are relevant for thisstudy group also.

TABLE 3. Occupations Classified as Likely to Have Medium or High EMF Exposure in Case and Control Groups

The Canadian Study of Health and Aging 31 reports an increased risk of AD for occupational exposure topesticides and fertilizers. The PAQUID cohort, 32 however, reports that occupational category has no major impacton the risk of AD; nevertheless, it indicates an increased risk of dementia with parkinsonism in farmers. Two studiesfrom Canada focus on the same problem through exposure to pesticides, defoliants, and fumigants. 33–34 One ofthese studies reports a null association between pesticide use and AD risk. 33 In this study, the exposure assessmentto pesticides was based on residential histories and the agriculture census histories. The authors state that among the265 active substances used in the area, only 38 were neurotoxic, and that it was impossible to differentiate betweenthem during data collection. Thus, their result should be interpreted cautiously. Tyas et al., however, demonstratean increased risk with use of defoliants and fumigants (which have neurologic effects) but not with the use ofpesticides and fertilizers, controlled for being a farmer. 34 They therefore suggest that exposure to these substancesand not just farming per se may be the real risk factor. In our study, being a farmer as the primary occupation in lifewas significantly associated with AD risk in the univariate analysis; however, it failed to reach statistical significancein the multivariate modeling. The small numbers in this group (4 cases and 1 control) limit any further analysis.Neurotoxic effects and AD risk of such exposures, nevertheless, need to be further studied with better measurementmethods, especially for a possible dose-effect relationship.

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methods, especially for a possible dose-effect relationship.

In the same line with being a farmer, rural place of residence has also been suggested as a risk factor. Studiesattempted to identify whether residence in a rural or an urban environment constituted a risk factor for AD. Onestudy reported a statistically significant excess of AD cases in the rural area as compared with the referencepopulation. 35 Another one stated that rural residence exerted a protective effect for dementia and AD. 36 Yetanother study looked at area of residence before the age of 18 years and hypothesized a protective association,however reporting a null result. 37 We did not find a significant association with primary place of residence and ADrisk. Rural residence is rather a crude variable possibly including more than one putative risk factor.

One of the interesting findings of this study is the positive association between use of electricity for residentialheating and AD risk. This is, to our knowledge, an unprecedented finding. We already discussed the occupational EMFexposure with respect to AD risk. If EMF exposure is a risk factor at work, it follows that it may be a risk factor athome. A main difference would be the dose of exposure, which is usually considerably higher in work environments.However, there is no evidence to prove that high-level exposure to EMF at work is any more a risk factor than low-level, long-term exposure at home. Unpublished analysis of the most recent Turkish Demographic and Health SurveyData (1998) shows the following distribution for residential heating: 11.0% by central heating, 3.8% by natural gasfurnace, 76.2% by wood/coal furnace, and 8.9% by other methods. Electricity seems to be grouped under “othermethods.”38

International Agency for Research on Cancer classifies EMF as a “possible human carcinogen” based onepidemiological studies suggesting residence near power lines resulted in a higher risk of leukemia in children. Onestudy using personal magnetic field measurements among women working outside of home and homemakers reportstime-weighted average exposure in various occupation groups. 39 The geometric mean (GM) of time-weightedaverage exposure was 0.265 microT (range 0.054–3.436) for those working in manufacturing and industrial facilities,0.133 microT (range 0.022–0.403) for homemakers, and 0.099 microT (0.035–0.673) for teachers and schooladministrators. This implies that residential EMF exposure may even be higher than in some occupations. In thisstudy, we classified homemakers as members of the low EMF exposure group. This may be a misclassification ifresidential EMF exposure is indeed a risk factor. Including an occupation × home heating interaction term in thelogistic regression model would have shed light on this issue. However, power does not permit for such a calculation.

Ahlbom et al. for the International Commission for Non-Ionizing Radiation Protection Standing Committee onEpidemiology state that exposure assessment is particularly difficult for EMF since the exposure is imperceptible andubiquitous and has multiple sources in our modern society. 29,40 The big difference of incidence and prevalencerates of AD in the developing and the developed world naturally raises the issue of whether there is some factor inthe industrialized civilization that is contributing to development of AD. This may very well be the widespread use ofelectricity and electrical appliances. This finding needs to be confirmed for strength of association, biologiccredibility, temporality, and dose-effect relationship by better exposure assessment and preferably by prospectivestudies. If confirmed, an opportunity for primary prevention of AD may be available, at least for a proportion ofcases.

In conclusion, our results suggest that having a higher education is protective from AD and that EMF exposure atwork or at home is a significant risk factor. Studies with prospective methodology with more precise exposureassessment procedures are necessary to better evaluate the results about EMF exposure as a risk factor for AD.

ACKNOWLEDGMENTS

The authors thank Dr. Lenore J. Launer for her valuable contribution to the design of the study and Kay Zahaskyfor translation editing of the manuscript.

FOOTNOTES

1A muhtar is an elected official responsible mainly of keeping records of the population living in a definedgeographical area. The records contain the following information: name, address, date and place of birth, mother'sand father's names. [Context Link]

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Key Words: risk factors; education; electromagnetic field; EMF; Turkey

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10/29/13 10:57 AMOvid: Risk Factors for Alzheimer Disease: A Population-Based Case-Control Study in Istanbul, Turkey.

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