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Dementia and Alzheimer Disease Incidence Rates Do Not Vary by Sex in Rochester, Minn
Steven D. Edland, PhD;
Walter A. Rocca, MD, MPH;
Ronald C. Petersen, MD, PhD;
Ruth H. Cha, MS;
Emre Kokmen, MD
Arch Neurol. 2002;59:1589-1593.
ABSTRACT
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Background Incidence rates of Alzheimer disease (AD) were higher in women than
in men in several recent European and Asian studies. Cohort studies in the
United States, on the other hand, have consistently reported no difference
in incidence across sex.
Objective To measure age- and sex-specific incidence rates of dementia and AD
for persons aged 50 years and older residing in Rochester, Minn, during 1985
to 1989.
Subjects and Methods Cases were ascertained through the medical records linkage system of
the Rochester Epidemiology Project, which encompasses the records of all medical
care providers (including outpatient clinics, hospitals, general practitioners,
and nursing homes) in Rochester. Computer indices of clinical diagnoses, histologic
diagnoses, and medical procedures were screened for indications of dementia.
All medical records of potential cases were reviewed and abstracted by a trained
nurse abstractor. A neurologist (E.K.) confirmed the presence of dementia
and established a differential diagnosis of AD using the criteria of the Diagnostic and Statistical Manual of Mental Disorders, Fourth
Edition, and estimated the year of onset.
Results A total of 482 incident cases of dementia were identified; 356 of them
(73.9%) had AD. For both dementia and AD, incidence rates increased steeply
with age, and there were no consistent differences between men and women.
The sex pattern for AD did not change after removing cases with silent bilateral
infarcts on imaging.
Conclusions Contrary to observations from European and Asian populations, women
were not at increased risk of incident AD in Rochester. Our findings, based
on a medical records linkage system, corroborate findings from several other
US studies that involved the direct contact of cohort members. The consistency
of findings across study designs suggests that sex or sex-related exposures
do not consistently play a major role in AD causation in American populations.
INTRODUCTION
WHILE CAUSAL genetic mutations, susceptibility genes, and environmental
risk factors for Alzheimer disease (AD) have been identified, these factors
collectively account for one half or less of all cases, and additional risk
factors will likely be identified.1 In some
studies, women have an increased incidence of AD compared with men, and it
has been hypothesized that being female is a risk factor for AD.2
Recent reports that estrogen replacement therapy may improve memory performance
and protect against AD suggest a biological basis for an increased risk of
AD in postmenopausal women.3-5
Epidemiologic evidence regarding sex as a risk factor for AD is ambiguous.
Some investigators have reported higher age-specific incidence rates of AD
in women than in men.6-7 Others
have found an increased risk, but only in the oldest ages.8
Still, others have found a trend toward an increased risk in women9-11 or no consistent pattern
by sex.12-16
Remarkably, those studies with positive findings are all from European6-9 and Asian10-11 populations, while no study from
the United States has found a significant effect of sex on risk of AD.12-15 A
problem with many of these investigations is their limited sample size, especially
in the oldest ages studied, where the greatest differences in incidence between
sexes have been reported.
We previously reported incidence rates in Rochester, Minn, for the 1975
through 1979 and 1980 through 1984 calendar periods and found no consistent
difference in the incidence of AD by sex.17
To further address the question of differential risk by sex in the same Rochester
population, we assessed the age- and sex-specific incidence rates of dementia
and AD for 1985 through 1989. Cases of dementia were ascertained using the
medical records linkage system of the Rochester Epidemiology Project, which
allowed us to efficiently study a population of approximately 14 400
persons over a 5-year period. To our knowledge, this is one of the largest
populations for which incident AD cases have been enumerated, and hence, this
study provides a powerful assessment of sex differences in the incidence of
AD.
METHODS
STUDY POPULATION
The study population has been described in detail elsewhere.17-19 In brief, Rochester
is the centrally located seat of Olmsted County and lies about 90 miles southeast
of Minneapolis. As of the 1990 census, 70 745 people lived in Rochester
and they were predominantly white. Twenty percent (n = 14 439) were aged
50 years or older, and among this group, 57% were women.19
CASE ASCERTAINMENT
We ascertained cases of dementia through the medical records linkage
system of the Rochester Epidemiology Project.17-19
Medical care for the population of Rochester and Olmsted County is provided
largely by the Mayo Clinic at the primary, secondary, and tertiary levels.
Additional health care providers (1 hospital, 1 outpatient clinic, several
general practitioners, and several nursing homes) in the community participate
in the Rochester Epidemiology Project, which provides the infrastructure for
indexing all medical information of the local population. Each provider in
the community employs a dossier system whereby all medical information for
each individual is accumulated in a single file. Medical diagnoses, surgical
interventions, and other key information from the dossier are routinely abstracted,
coded using the International Classification of Diseases,
Adapted Code for Hospitals (H-ICDA),20 and entered into computerized indices. Therefore,
each individual in the system can be searched for a given condition through
the computerized indices.
We searched these indices for 112 specific H-ICDA codes that might indicate dementia. Any subject with at least 1 of
the study codes was considered as a potential case. Cases of dementia in the
general population may remain undetected for a number of years but may be
diagnosed at some point during their natural history. To increase the likelihood
of capturing these individuals, the indices were searched for the study interval
and for 6 additional years (1990-1995). All medical records of each potential
case were screened by a trained nurse abstractor, and all entries in the medical
record relevant to dementia were flagged. The study neurologist (E.K.) confirmed
the presence of dementia, classified the dementia by type, and determined
the year of onset as previously described.21
To standardize and operationalize the diagnosis, each cardinal feature required
for a diagnosis of dementia was considered and documented separately (see
below).
To be included in the study, a patient was required to reside in Rochester
in the year of onset of dementia and for at least 1 preceding year. Patients
who moved to Rochester for the management of a preexisting dementing illness
were excluded. All study procedures were reviewed and approved by the Mayo
Clinic institutional review board. Persons obtaining medical care at the Mayo
Clinic and other medical services affiliated with the Rochester Epidemiology
Project are given the opportunity to deny access to their medical records
for research purposes; 10 subjects were excluded from our study for this reason.22
DIAGNOSTIC CRITERIA
We used the Diagnostic and Statistical Manual of Mental
Disorders, Fourth Edition (DSM-IV)23 criteria for dementia and AD. The DSM-IV criteria for dementia include 3 items: (1) memory impairment
as a prominent early feature, (2) at least 1 of aphasia, apraxia, agnosia,
or disturbance of executive function, and (3) loss of function representing
a significant decline from a previous level and sufficient to interfere with
social or occupational activities. Abstraction and interpretation of medical
records was standardized and operationalized to increase reliability. All
medical records, including physician and nurse notes, were reviewed, and all
available data pertinent to the DSM-IV criteria were
abstracted. Each item of the DSM-IV criteria was
documented separately, and a diagnosis of dementia was allowed only if all
3 items were present.
The differential diagnosis of AD from other types of dementia was likewise
based on all available clinical and laboratory data, using DSM-IV criteria (dementia with gradual onset and continuing decline
and absence of any other conditions that could explain the deficits).23 Autopsy information encoded in the Rochester Epidemiology
Project record linkage system was screened to identify potential cases of
dementia in the case-ascertainment phase of the study. Final diagnoses, however,
were based strictly on antemortem data.
DATA ANALYSIS
The numbers of persons at risk and person-years at risk were estimated
from census data with an adjustment for prevalent cases of dementia, as previously
described.17 Census data for Rochester by sex
and by single year of age were available for the census years 1980 and 1990.
Counts for the years between censuses were estimated by linear interpolation
(assuming a constant increment from one year to the next). These numbers were
adjusted downward by removing prevalent cases already affected by dementia
and therefore not at risk.17
Average annual incidence rates were reported by sex and by 5-year age
intervals up to age 99 years. Tabular summaries were reported as cases per
100 000 person-years, while graphical summaries were reported as cases
per 100 person-years. The few cases with onset of dementia at 100 years or
older were excluded from tables and graphs. Since the study covered the target
population completely (no sampling was involved), there is no statistical
uncertainty in the data, and we elected to report the rates without confidence
intervals.24-25
RESULTS
A total of 2819 persons age 50 years and older had 1 or more H-ICDA codes potentially indicative of dementia during the 1985 through
1995 screening period (study incidence period plus 6 additional years). Ten
of these individuals (0.4%) denied access to medical records for research
purposes and were excluded. Medical records for the balance of 2809 persons
were reviewed to confirm residency, the presence of dementia, and the year
of onset of symptoms. A total of 482 residents of Rochester aged 50 years
or older developed dementia during 1985 through 1989; 356 (73.9%) of them
developed AD. Three patients were older than 99 years at dementia onset (specifically
AD) and were not included in Table 1
and in Figure 1 and Figure 2. Fourteen persons had medical records suggestive of dementia
but remained undiagnosed because not all of the cardinal features required
for a DSM-IV diagnosis were documented. These persons
were not included in the incidence calculations.
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Age- and Sex-Specific Incidence Rates (per 100 000 Person-Years)
of Dementia and Alzheimer Disease in Rochester, Minn, 1985-1989*
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Figure 1. Age- and sex-specific incidence
rates of dementia (A) and Alzheimer disease (B) in Rochester, Minn, during
1985 through 1989.
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Figure 2. Age- and sex-specific incidence
rates of Alzheimer disease in Stockholm, Sweden (the Kungsholmen Project),6 in southwestern France (the PAQUID Study),8 in the pooled data from 8 European studies (the EURODEM
project),26 in Baltimore, Md (the Baltimore
Longitudinal Study of Aging),12 in Framingham,
Mass (the Framingham study),15 and in Rochester,
Minn (the current study). The pooled European figure includes data from the
Stockholm and southwestern France studies, also shown separately, as well
as data from Kuopio (Finland), Odense (Denmark), Rotterdam (the Netherlands),
Liverpool (England), Zaragoza (Spain), and Pamplona (Spain).26
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Table 1 presents the distribution
of incident cases, the corrected census counts (in the footnotes), and the
age- and sex-specific incidence rates of dementia and AD by 5-year age increments
(new cases per 100 000 person-years). For both dementia and AD, the incidence
increased continuously with age and was similar in men and women at all ages
(Figure 1). Up to age 80 years,
incidence rates for AD were essentially identical in men and women. From age
80 to 89 years, there was a slightly higher incidence rate in women than in
men (rate ratio = 1.14 in 80- to 84-year-olds; rate ratio = 1.28 in 85- to
89-year-olds). Among 90- to 94-year-olds, the incidence rate in women was
identical to that in men (rate ratio = 0.94). The population size of those
older than 95 years was too small for meaningful interpretation.
Several cases that were classified as AD by the DSM-IV criteria and included as AD in the current report had some indications
of cerebrovascular disease, that is, bilateral infarcts on imaging judged
to be sufficient to cause dementia in the absence of a clinical stroke. Exclusion
of these 31 cases of AD with imaging evidence of vascular lesions did not
modify the sex pattern. In addition, we reported separately incidence rates
of vascular dementia in the same Rochester population using several sets of
diagnostic criteria.27 Age-specific incidence
rates of vascular dementia did not differ substantively between men and women,
using either a narrower or a broader interpretation of the diagnostic criteria.27
COMMENT
We found no substantial difference between men and women in the incidence
of AD in the population of Rochester. Our findings contradict those from several
recent studies of European6-9,26
and Asian10-11 populations. On
the other hand, our findings are consistent with studies of populations in
the United States, which have consistently found no pattern of increased incidence
of AD in women.12-15
Findings from several European and US studies reporting age- and sex-specific
incidence rates are shown in Figure 2.
The European cohort studies consistently found that incidence rates in men
leveled off after about age 85 years, while rates in women continued to increase
beyond this age.26 A nonstatistically significant
trend in this direction was also observed in 2 Asian studies.10-11
Studies in the United States, on the other hand, have consistently found that
rates increased across age in both sexes, with no systematic differences in
rates between sexes. Studies in the United States included both prospective
cohort studies12-15
and the current study. There are potential limitations with both study designs.
For example, patients who do not seek medical care for their dementia before
they die cannot be detected through our medical records linkage system. Cohort
studies involving repeated contacts over time, on the other hand, have other
limitations. Usually, the size of the sample that can be studied at reasonable
cost is too small for investigators to obtain stable incidence estimates for
age and sex subgroups. In addition, the initial study sample may be distorted
by nonparticipation, and additional distortion may result from losses to follow-up.17 With either study design, differential ascertainment
of men or women affected by dementia is possible, thus introducing or masking
a sex difference. The consistency of findings across study designs in the
US studies suggests that the lack of a sex effect is not due to design-related
biases.
There are potential limitations to our study. As previously discussed,
patients with dementia who did not reach medical attention may have been missed;
therefore, underascertainment of disease is possible. The features of our
population and study design limit the extent of this potential bias, however.
The population is almost entirely middle-class, is well educated, and has
excellent access to medical care. This should enhance referral of cases with
moderate or severe dementia to the services included in the Rochester Epidemiology
Project. In addition, all health care providers in the city of Rochester (and
in Olmsted County) participate in the records linkage system and provide access
to all of their records.
To increase detection, we searched the system indices for the 6 years
following the study period. Subjects with dementia were likely to be diagnosed
at some point before death even though the disease was not recognized at the
onset or when the symptoms were mild. One hundred eight (22%) of the 482 incident
cases of dementia and 87 (24%) of the 356 incident cases of AD were diagnosed
only after the end of the incidence study period (after 1989). Hence, the
inclusion of 6 additional years of follow-up substantially reduced the potential
for underascertainment of cases. On the other hand, the age-specific incidence
of dementia and AD restricted to the cases identified through 1989 did not
vary by sex; therefore, the inclusion or exclusion of the cases with delayed
diagnosis from our overall incidence rate calculations did not modify the
sex patterns.
Underascertainment of dementia cases, if it occurred, should have differentially
underestimated the rate of disease in men. Because of their decreased longevity,
men with AD symptoms are presumably less likely than comparably affected women
to survive till their clinical symptoms are documented in medical records.
Therefore, men may have been less likely to be captured by our study. Capturing
fewer men would have decreased the observed incidence in men compared with
women, particularly in the oldest age categories, where mortality is high.
Despite this potential bias, we did not observe sex differences in incidence.
It is possible that the sex pattern observed for AD was influenced by
differences in the application of diagnostic criteria for other types of dementia,
primarily vascular dementia, between men and women. However, we found no difference
in age-specific incidence rates between men and women when considering dementia
overall or when considering vascular dementia alone, using either a broader
or a stricter interpretation of the diagnostic criteria.27
In addition, the sex pattern for AD did not change after removing patients
who had silent bilateral infarcts on imaging but not a clinical stroke. Therefore,
the lack of sex differences for AD in our study is not due to a difference
in the classification of dementia by type.
Our finding may have implications for etiologic research in AD and for
public health planning. The similar risk of AD in men and women in our population
and in other US populations suggests that hormonal factors or sex-related
social, cultural, or occupational factors do not consistently play a major
role in AD causation. Sex-related exposures may help to explain the sex effects
observed in other geographically defined populations. The importance of these
possible exposures to AD risk remains an area for future study.
AUTHOR INFORMATION
Accepted for publication April 30, 2002.
Author contributions: Study concept and design (Drs Rocca and Kokmen); acquisition of data (Drs Rocca, Petersen,
and Kokmen); analysis and interpretation of data (Drs Edland
and Rocca and Ms Cha); drafting of the manuscript (Drs Edland,
Rocca, and Kokmen); critical revision of the manuscript for important
intellectual content (Drs Rocca, Petersen, and Kokmen, and Ms Cha);
statistical expertise (Dr Rocca and Ms Cha); obtained funding (Drs Kokmen and Petersen); administrative, technical, and material
support (Dr Kokmen); study supervision (Drs Edland, Rocca,
Petersen, and Kokmen).
The study was supported by the grants AG 06786 and AG 08031 from the
National Institute on Aging, Bethesda, Md, and was made possible by the Rochester
Epidemiology Project (grant AR 30582 from the National Institutes of Health,
Bethesda). We thank nurse abstractors Virginia Hanson, RN, and Connie Neuman,
RN, for their assistance with medical records abstracting. We also thank Karen
Tennison for technical assistance with the manuscript and Roger Mueller, BS,
for database management and support.
Corresponding author and reprints: Steven D. Edland, PhD, Department
of Health Sciences Research, Mayo Clinic, 200 First St SW, Rochester, MN 55905
(e-mail: edland.steven{at}mayo.edu).
From the Departments of Health Sciences Research (Drs Edland, Rocca,
and Petersen, and Ms Cha) and Neurology (Drs Rocca, Petersen, and Kokmen),
Mayo Clinic and Mayo Foundation, Rochester, Minn. Dr Kokmen died in 2000.
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