(Stroke. 1997;28:491-499.)
© 1997 American Heart Association, Inc.
Articles |
Comparable Studies of the Incidence of Stroke and its Pathological Types
Results From an International Collaboration
From the Department of Clinical Neurosciences, University of Edinburgh (Scotland).
Correspondence to Dr Cathie Sudlow, Registrar in Medical Neurology, Department of Clinical Neurosciences, University of Edinburgh, Western General Hospital, Crewe Rd, Edinburgh EH4 2XU, Scotland.
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Abstract |
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Background and Purpose Comparing stroke rates in different parts of the world may increase our understanding of both etiology and prevention. However, comparisons are meaningful only if studies use standard definitions and methods, with comparably presented data. We compared the incidence of stroke and its pathological types (cerebral infarction, primary intracerebral hemorrhage, and subarachnoid hemorrhage) in recent studies from around the world.
Methods Studies with a midyear of 1984 or later, fulfilling standard criteria for a comparable, community-based study, provided original data for comparative analyses.
Results By mid-1995, data were available from 11 studies in Europe, Russia, Australasia, and the United States, comprising approximately 3.5 million person-years and 5575 incident strokes. Age- and sex-standardized annual incidence rates for subjects aged 45 to 84 years were similar (between approximately 300/100 000) and 500/100 000) in most places but were significantly lower in Dijon, France (238/100 000), and higher in Novosibirsk, Russia (627/100 000). In subjects aged 75 to 84 years, however, Novosibirsk no longer ranked higher than the other studies. The distribution of pathological types, when these were reliably distinguished, did not differ significantly between studies.
Conclusions The similarities in stroke incidence and pathological types are perhaps not surprising given that all the populations were westernized and mainly white. The higher rates in Novosibirsk, disappearing in the elderly, and the lower rates in Dijon have several potential explanations. These include methodological artifact and different patterns of population risk factors. Further work is needed to explore these possibilities and to extend our knowledge of stroke incidence to other parts of the world, especially developing countries.
Key Words: epidemiology • incidence • stroke, acute
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Introduction |
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Comparing rates of disease in different parts of the world and attempting to determine factors to explain any differences have often led to important knowledge about etiology and prevention. For stroke, however, there are problems in comparing rates on an international scale. Mortality statistics, when available, are a convenient starting point but are limited by inaccuracy, variable diagnostic and coding methods, and the absence of information on nonfatal strokes.1 2 In addition, stroke is not a single disease but a clinical syndrome with several different pathologies; these are not distinguished reliably in death certificates and some—lacunar strokes, for example—are rarely fatal. Stroke incidence (and case fatality) should be much more informative, but accurate data can be obtained only by rigorously conducted studies adhering to criteria that make their results comparable with each other. We believe that these criteria should be based on those of Malmgren et al,3 and they are discussed in detail elsewhere.2 The review of Malmgren et al, published in 1987, found only nine of a potential 65 studies whose incidence rates for all types of stroke combined could be reasonably compared.4 5 6 7 8 9 10 11 12 13 14 Such studies are therefore rare, and what we know of stroke incidence on a worldwide scale remains very limited, being largely confined to developed, westernized countries.
However, our knowledge of the worldwide situation is slowly growing as further comparable studies emerge. The ongoing WHO MONICA project has recently published stroke incidence figures from participating centers in Europe, Russia, and China.15 This is a landmark study in stroke epidemiology, but it has some limitations: many parts of the world are not represented; no center includes subjects aged >75 years (in whom the burden of stroke is greatest), and many stop at 65 years (thereby excluding approximately 75% of all strokes); the study is not designed to investigate accurately different pathological types of stroke; and many centers use the semiretrospective "cold pursuit" method of case finding, which is more suitable for monitoring time trends within individual studies (the main aim of the MONICA project) than for comparing rates between studies.
However, data from other potentially comparable incidence studies that were not initially established as part of an international effort can be used to contribute to the broadening knowledge of worldwide patterns of stroke incidence. Moreover, with the wider availability of CT scanning, an increasing number of studies can provide reliable information on the incidence of the different pathological types of stroke: CI, PICH, and SAH. This article presents the results of comparisons from a collaborative group of recent studies. Most of these monitored stroke in subjects aged up to and over 85 years. For studies with high rates of accurate diagnosis of pathological types of stroke, a comparison of the incidence rates of pathological types is included.
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Methods |
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Developing Standard Criteria
Based on the work of Malmgren et al,3 supplemented by the experiences of stroke incidence studies undertaken more recently, we established an updated set of criteria for comparable studies of stroke incidence. These are summarized in Table 1
and discussed fully in an earlier
report.2
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Study Selection
Stage 1: Search Strategy
We searched for studies performed recently (midyear of study
1984 or later) that might contribute to an up-to-date "snapshot"
of stroke incidence around the world. We used the American Library of
Medicine Medline and Popline databases and the Bath Information Data
Services' Embase to identify studies. Reference lists of stroke
incidence studies and relevant review articles were also examined.
Several journals with an interest in stroke epidemiology were inspected
prospectively during the last 12 years by one of the authors (C.P.W.).
Finally, we asked collaborators and international colleagues to inform
us of any potentially comparable studies.
Studies that are part of the WHO MONICA project,15 even if independently published, were not included in this comparison because they form a well-defined group that is being analyzed separately. Therefore, this is not a complete systematic review but rather an attempt to bring together currently available knowledge from independent groups of investigators.
Stage 2: Examining Written Reports of Studies
We examined the publications and available unpublished
manuscripts from all identified studies. Studies were excluded when it
was clear that the standard definitions and methods outlined in Table 1
had not been used, with one exception: the Mayo Clinic in Rochester,
Minn, has a unique records system, reliably documenting all medical
presentations from the level of primary care upward.16 In
this case only, we considered retrospective methods of case
identification to be as reliable (or nearly as reliable) as prospective
ones. Emphasis was placed on the importance of complete,
community-based case ascertainment. Studies that did not clearly
attempt to identify cases managed outside the hospital were excluded.
Stage 3: Seeking Information Not Included in Written Reports
For all potentially comparable studies, we not only used the
written reports but also sought unpublished details from the authors to
confirm the use of standard definitions and methods. This included one
of the authors (C.L.M.S.) visiting almost all the centers of
potentially "ideal" studies in late 1994. For each study, we
established the range of case-finding procedures and their relevance to
the local healthcare system, ensuring (as far as possible) that all
potential sources of cases had been identified. Our minimum criteria
for adequate case ascertainment methods are shown in Table 2.
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Stage 4: Data Collection
The studies selected provided original data in a standard
format, with actual numbers of first-ever-in-a-lifetime strokes and
population figures in 5-year age bands for men and women separately.
Ten-year age bands were used in two studies17 18 19 in which
5-year breakdowns for the denominator were unavailable. Most studies
had collected data on strokes for all age groups and could provide
information for subjects aged up to and over 85 years. We avoided
averaging data collected over periods of >5 years. For studies running
continuously or intermittently for >5 years, the most recent set of
data was used.
Stage 5: Selecting Studies for Comparisons of Pathological Types of
Stroke
Studies with a high rate of diagnosis of pathological types,
which used diagnostic definitions as outlined in Table 3
and discussed previously,2 provided data in the same
format as described above for each of the pathological types. We
considered a "definite" pathological diagnosis rate of >70% of
incident strokes (ie, <30% "undetermined" or "probable")
to be high enough to make the results reasonably representative of the
true distribution of pathological types. This effectively meant a
minimum CT scan rate of approximately 70%, because the number of cases
assigned a definite pathology purely on the basis of autopsy or other
investigations was small in all studies. When this condition was met,
we considered it acceptable for some of the cases without a definite
pathological type to be assigned a probable pathological type (CI or
PICH) based on a validated clinical score.2 For all
studies, we assumed that the vast majority of SAHs could be diagnosed
reliably with the use of mainly clinical and cerebrospinal fluid
criteria, making all strokes of undetermined pathology either PICH or
CI. This meant that as long as they used the criteria in Table 3,
studies with lower rates of CT scanning could provide separate
information on SAHs but not on other pathological types.
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The comparison included all studies selected as described above with data made available to us by mid-1995.
Data Analysis
Incidence rates were calculated from the data provided for each
study, and comparisons between studies were made with the use of direct
age standardization to Segi's European population.20 In
this comparison, the study populations resemble this notional
population structure more closely than Segi's world
population,20 which would be more appropriate for the
truly worldwide comparison that is not yet possible. The distribution
of ages in the population within the open-ended upper age band may vary
between studies, and therefore if this age band is included in
estimates of age-standardized rates, the results may not be comparable
between studies. Age-standardized rates for comparisons were therefore
based on closed bands: 45 to 84 or 45 to 74 years. Data combining both
men and women were standardized to a notional population with a
male-to-female ratio of 1:1 (direct sex standardization). For analysis
of rates of pathological types, in studies in which a clinical score
was used as described above, the definite and probable categories for
CI and PICH were combined.
We calculated confidence intervals by assuming a Poisson distribution of incident strokes over time.21 For the Auckland study, a more complex adaptation of the standard method had to be used because one quarter of the study population was used for monitoring out-of-hospital cases.22
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Results |
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Studies and Characteristics
From a total of 35 studies of stroke incidence (excluding WHO MONICA studies) of mid-year 1984 or later, published by the end of 1994 or unpublished but known to us at that stage, 11 were selected according to the methods described. Several important features of these are summarized in Table 4
. One of the studies
(Söderhamn, Sweden) is unpublished, but the methods are the same
as those used in previous studies by the same investigator in the same
location.4 13 An appendix listing all the studies reviewed
and reasons for exclusion can be obtained from the authors on request.
We continue to seek details from several very recent studies as part of
the ongoing collaborative effort.
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The Oxfordshire study population was not geographically discrete,
with the denominator based on the age/sex registers of general practice
populations.23 All the other studies defined their
population according to geographic boundaries of all or part of a town
or city, with denominator numbers derived from official census data.
Because the studies collected cases for a variable period of time, the
person-years studied are a variable multiple of the population size.
The total number of strokes is also an important determinant of the
statistical precision of incidence estimates. Table 4 also shows the
variability in hospital admission rates for stroke. In most studies, a
substantial minority were not admitted, demonstrating the importance of
a comprehensive out-of-hospital case-finding system. All the studies
fulfilled our minimum criteria for case ascertainment. However, there
were considerable differences in the way that these were achieved,
particularly the maintenance of contact with primary health care,
involving frequent general practice visits by study nurses or
neurologists in some studies and relying on regular written reminders
to general practitioners to refer all suspected stroke and TIA cases in
others. Most studies made use of hospital discharge lists as well as
admissions, and most used a variety of other case-finding methods,
depending on the local healthcare system. For example, emergency
ambulance calls were monitored daily in Novosibirsk,34 and
in several studies routine investigations of requests to CT scanning
and carotid ultrasound departments were made. All except the Rochester
study (see above) used prospective methods, with a study specialist
assessing the majority of potential stroke cases, usually within a few
days of the event. In the Rochester study all records for potential
stroke cases were reviewed by a study neurologist.
Incidence Rates
Our calculated incidence rates sometimes yielded different
results from those in existing publications. For example, ongoing case
finding in the Auckland study33 discovered some extra
cases not known about when the results of the study were first
published, although these were too few (four) to make any meaningful
difference to the results. The original publications of the Perth study
included 18 months of strokes,30 but in this analysis only
the first-year data were used to avoid the possible effect of seasonal
fluctuations in incidence rates. Published work from the Dijon study
included as CIs all cases of TIA with a visible infarct on CT
scan.24 25 Because we sought to compare rates of stroke as
defined by the WHO, with symptoms lasting beyond 24 hours, TIAs were
excluded in the Dijon data set used for this comparison. In a recent
publication by the Rochester group, incidence rates are estimated with
a denominator corrected for prevalent cases (ie, those no longer at
risk of a first-ever stroke are removed from the
denominator).27 No other study has been able to adjust for
prevalence in this way, and therefore for this comparison we have not
adjusted the Rochester population denominator.
Rates for All Types of Stroke Combined
The Warsaw study is not included here because SAHs were not
registered, and therefore total stroke rates are not
known.32 Fig 1 shows the incidence of all
types of stroke combined, in 10-year age bands from 45 to 54 up to 
85
years . Data are sex-standardized within each age band. As expected, a
rise in stroke incidence with age is seen for all studies, with the
vast majority of strokes occurring in those aged 65 years. The rate
of this rise varies between studies with especially wide variation in
those aged >85 years. Smaller population numbers in this age band
limit the precision of rate estimates, which have wide confidence
intervals. It is also an open-ended upper age band with potential
variability arising from different age distributions within this band
in each study.
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Fig 2 shows age- and sex-standardized incidence
rates for all types of stroke combined for subjects aged 45 to 84 years
and age-standardized incidence rates for men and women separately for
the same age group. When we allow for the statistical imprecision of
the estimates, the results suggest a similar annual stroke incidence
for most studies, with the age- and sex-standardized rate lying
somewhere between approximately 300/100 000 and 500/100 000. However,
Dijon, at 238/100 000, had a significantly lower rate, and
Novosibirsk, at 627/100 000, had a rate more than 2.5-fold that in
Dijon. Men had consistently higher incidence rates than women. The
tendency for rates to be lower in Dijon and higher in Novosibirsk was
maintained when the sexes were considered separately.
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If the oldest age group for which a closed age band is available (ie,
75 to 84 years) is considered, the variation in incidence rates between
countries, shown in Fig 3, is somewhat different. In
particular, Novosibirsk, which from Fig 2 had by far the highest
overall stroke incidence, no longer ranks the highest.
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Rates for Pathological Types
Studies suitable for comparison of pathological types defined as
in Table 3 are shown in Table 4. The Umbria and Oxfordshire
studies17 19 both used Guy's Hospital Stroke Diagnosis
Score35 to increase the pathological diagnosis rate.
Neither Auckland33 nor Novosibirsk34 had high
enough rates of CT scanning to be included in the comparison of all
pathological types, but they were included in the comparison of rates
of SAH and of all other types of stroke combined, shown in Fig 4. We were able to include the Warsaw study, in which no
SAHs were counted, in this part of the comparison.32 We
had to use the more restricted age group of 45 to 74 years here because
the Warsaw study did not have separate denominator age groups 80
years, and two other studies (Oxfordshire and Umbria) had denominator
numbers only in mid-decade 10-year age bands. The proportion of total
strokes in this age group that were SAHs varied between studies from
just over 2% to almost 9%. However, the numbers of SAHs were very
small, with wide confidence intervals around the incidence rates, so
that the variation seen in the figure could be simply due to chance.
The differences between studies in the rates of all other stroke types
combined followed a pattern similar to that seen in Fig 2, with
especially high rates in Novosibirsk and low rates in Dijon. All the
other studies, including the Warsaw study on this occasion, were very
similar.
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Eight studies were suitable for examining pathological types of stroke
separately. In the data set provided by the Rochester group, strokes in
the undetermined pathology category, which constituted a very small
proportion, were assumed to be CIs (because of their similar prognosis
at follow-up in this data set) and categorized as such. The age- and
sex-standardized rates for the group aged 45 to 84 years are shown in
Table 5. Except for CI, the numbers are small and the
confidence intervals are wide. If we allow for this, the percent
distribution of pathological types shown in Fig 5 is
similar for all the studies examined.
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Discussion |
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There is little variation to be found in the incidence of all types of stroke combined among the studies considered here. This is perhaps not surprising, given that all the populations studied were predominantly white with a westernized lifestyle. However, the study from France has strikingly low rates. This could simply be artifact, relating to methodological differences, most likely in case finding, but it raises the possibility that the so-called French paradox—low rates of cardiovascular disease in France, attributed by some to wine consumption36 37 —applies to stroke as well as to ischemic heart disease. Further reliable stroke incidence studies from this part of the world are needed to investigate this possibility. The much higher rates in Novosibirsk may also be due to methodological artifact or may indicate a real difference, reflecting a higher level of population risk factors for stroke. However, stroke rates in Novosibirsk do not rank as high in the elderly. The reasons are not clear. Perhaps case finding among older people in this population was less efficient. Another possibility is that there are fewer stroke-prone people in this age group because of earlier deaths from complications of ischemic heart disease in a population with a high prevalence of risk factors for both cardiovascular and cerebrovascular disease.
The approximately 2.5-fold difference between stroke incidence in Dijon and Novosibirsk is considerably less than the approximately 8-fold difference in mortality (from official statistics) between France and Russia.38 While it is possible that the much larger mortality difference could be due to higher case fatality in Russia, another potential explanation is that mortality statistics are simply not reliable enough to reflect accurately international variation in stroke incidence.
In regard to pathological types, no striking differences in distribution are seen, but the studies contributing to the analysis are again drawn from broadly similar types of population. Studies from the Far East show a similar overall incidence rate of stroke to other parts of the world when comparisons have been made. These include the WHO MONICA project,15 with a study from Beijing, China,39 and the review of Malmgren et al in 1987,3 which included an incidence study from Shibata, Japan, from the 1970s.6 However, most of the Far Eastern studies have suggested that the proportion of intracerebral hemorrhages is significantly higher (up to 35%) than in whites.6 39 40 41 42 43 44 Unfortunately, none of these studies fulfill our criteria for a comparable study, and therefore we cannot yet confirm that this excess of hemorrhages is real. This will require studies with comparable methods and high rates of accurate pathological diagnosis.
There is clearly a need to continue and extend this work to include
studies in the Middle East, Asia, Africa, and South America. In 1990,
official mortality statistics were available for only approximately one
third of deaths worldwide,45 and reliable information on
stroke incidence is available for only a tiny fraction. Fig 6 illustrates the paucity of our present knowledge about
stroke incidence around the world.
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); studies included in WHO MONICA stroke
incidence comparison
); and studies included in
current comparison (
).Future collaborative comparisons could also include a consideration of case fatality, which was estimated in many comparable incidence studies. This may eventually help us to determine whether international mortality differences are due to differences in incidence, case fatality, or both or are just an artifact. Attempting to determine reasons for any differences cannot be justified unless they are real. Only then can they possibly further our knowledge about the etiology and prevention of the third most common cause of death in the Western world.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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The worldwide visits for discussions with international investigators were made possible by the kind hospitality of colleagues and friends in Sweden, Denmark, Poland, Italy, France, Japan, Australia, New Zealand, and the United States, with generous financial support from the Edinburgh Stroke Research Fund, the Guarantors of Brain, the Royal College of Physicians of Edinburgh Myre Sim Bequest, Lilly Industries Limited, Bayer plc, and Boehringer Ingelheim Limited. We thank Jim Slattery for his helpful comments on earlier versions of the manuscript.
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Footnotes |
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A complete list of the participants in this research study appears at the end of this article.
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Appendix 1 |
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Collaborators were as follows: Auckland, New Zealand: R. Bonita, J. Broad; Dijon, France: M. Giroud, M. Lemesle; Frederiksberg, Denmark: H.S. Jorgensen; Oxfordshire, UK: M.S. Dennis, P.A.G. Sandercock, C.P. Warlow; Novosibirsk, Russia: V. Feigin, Y. Nikitin, A. Tarasov, T. Vinogradova; Perth, Australia: C. Anderson, P.W. Burvill, T.M. Chakera, G. Hankey, K. Jamrozik, E. Stewart-Wynne; Rochester, Minn: R. Brown, D. Wiebers, J. Whisnant; Söderhamn, Sweden: A. Terent; Umbria, Italy: M.-G. Celani, S. Ricci; Valle d'Aosta, Italy: G. D'Alessandro; and Warsaw, Poland: A. Czlonkowska, D. Ryglewicz.
Received August 20, 1996; revision received November 4, 1996; accepted November 19, 1996.
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A. G. Thrift, H. M. Dewey, R. A. L. Macdonell, J. J. McNeil, and G. A. Donnan Stroke Incidence on the East Coast of Australia : The North East Melbourne Stroke Incidence Study (NEMESIS) Stroke, September 1, 2000; 31(9): 2087 - 2092. [Abstract] [Full Text] [PDF]
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 J. Moncayo, G. Devuyst, G. Van Melle, and J. Bogousslavsky Coexisting Causes of Ischemic Stroke Arch Neurol, August 1, 2000; 57(8): 1139 - 1144. [Abstract] [Full Text] [PDF]
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T. Ingall, K. Asplund, M. Mahonen, and R. Bonita A Multinational Comparison of Subarachnoid Hemorrhage Epidemiology in the WHO MONICA Stroke Study Stroke, May 1, 2000; 31(5): 1054 - 1061. [Abstract] [Full Text] [PDF]
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G. R. Williams, J. G. Jiang, D. B. Matchar, and G. P. Samsa Incidence and Occurrence of Total (First-Ever and Recurrent) Stroke Stroke, December 1, 1999; 30(12): 2523 - 2528. [Abstract] [Full Text] [PDF]
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G. J. Hankey Stroke: How Large a Public Health Problem, and How Can the Neurologist Help? Arch Neurol, June 1, 1999; 56(6): 748 - 754. [Abstract] [Full Text] [PDF]
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 M.-G. Bousser Stroke in Women : The 1997 Paul Dudley White International Lecture Circulation, February 2, 1999; 99(4): 463 - 467. [Full Text] [PDF]
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G. P. Samsa, J. Bian, J. Lipscomb, and D. B. Matchar Epidemiology of Recurrent Cerebral Infarction : A Medicare Claims–Based Comparison of First and Recurrent Strokes on 2-Year Survival and Cost Stroke, February 1, 1999; 30(2): 338 - 349. [Abstract] [Full Text] [PDF]
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K. N. Vemmos, M. L. Bots, P. K. Tsibouris, V. P. Zis, D. E. Grobbee, G. S. Stranjalis, and S. Stamatelopoulos Stroke Incidence and Case Fatality in Southern Greece : The Arcadia Stroke Registry Stroke, February 1, 1999; 30(2): 363 - 370. [Abstract] [Full Text] [PDF]
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M. Lemesle, C. Milan, J. Faivre, T. Moreau, M. Giroud, and R. Dumas Incidence Trends of Ischemic Stroke and Transient Ischemic Attacks in a Well-Defined French Population From 1985 Through 1994 Stroke, February 1, 1999; 30(2): 371 - 377. [Abstract] [Full Text] [PDF]
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