(Stroke. 1996;27:550-558.)
© 1996 American Heart Association, Inc.
Articles |
Comparing Stroke Incidence Worldwide
What Makes Studies Comparable?
From the Department of Clinical Neurosciences, University of Edinburgh (Scotland).
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Abstract |
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 Top Abstract IntroductionWhy Measure Stroke Incidence?...Measuring Stroke Incidence: A...Measuring and Comparing...Conclusions References |
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Background Comparing stroke rates in different parts of the world and at different points in time may increase our understanding of the disease. Comparisons are only meaningful if they are based on studies that use similar definitions, methods, and data presentation.
Summary of Review We discuss the criteria that make such studies comparable, drawing on the experiences of recent studies performed around the world. If only those studies that fulfill the proposed criteria for comparison are considered, comparable data do not exist for vast areas of the world, including Africa, Asia, and South America. The importance of complete, community-based case ascertainment, including strokes managed outside the hospital, is emphasized. An approach for measuring and comparing the incidence of the pathological types of stroke (cerebral infarction, primary intracerebral hemorrhage, and subarachnoid hemorrhage) and subtypes of cerebral infarction is suggested.
Conclusions The "ideal" stroke incidence study does not exist, but studies closely approaching it will reveal the most reliable and comparable results. There is a need for further studies to fill the gaps in our knowledge of the worldwide incidence of stroke, particularly for developing countries.
Key Words: epidemiology • incidence • stroke
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Introduction |
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TopAbstractIntroductionWhy Measure Stroke Incidence?...Measuring Stroke Incidence: A...Measuring and Comparing...Conclusions References |
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Comparing stroke incidence in different countries and observing changes in incidence with time in a particular place may increase our understanding of the disease. To be comparable, studies of stroke incidence must use the same definitions, methods, and mode of data presentation. However well-conducted a study may be, unless it conforms in each of these three areas, comparison with other studies is not possible. The ideal approach is to develop standard criteria for these components of a stroke incidence study before establishing a series of comparable studies based on the prespecified criteria.
The first attempt to do this on an international scale is the World Health Organization (WHO) MONICA (Monitoring Trends and Determinants in Cardiovascular Disease) study, primarily designed to monitor trends in the incidence of myocardial infarction and stroke, together with the prevalence of various risk factors, in a number of different countries.1 A comparison of incidence and case-fatality rates from those countries monitoring stroke has recently been published.2 Although clearly a landmark study in international cardiovascular epidemiology, the MONICA study has limitations. The centers monitoring stroke are mainly European, extending into Eastern Europe, Russia, and China. This is the most extensive comparison yet, but large areas of the world were not included. In addition, a limited age range was covered, with most centers monitoring stroke up to age 65 years and none routinely collecting data on those older than 75 years, in whom the incidence (and caseload, at least in the areas studied) of stroke is highest. Finally, the MONICA study concentrates on total strokes and is not specifically designed to examine the incidence of pathological types, although some of the centers do have high enough rates of accurate pathological diagnosis for this.
A large number of independent studies have also measured stroke incidence. Most of them did not have comparative incidence as their sole or even main aim, and only a few are suitable for this purpose. In 1987, Malmgren and colleagues3 reviewed studies of stroke incidence from around the world. Of 65 studies, only nine met a set of standard criteria sufficiently to be considered comparable with each other.4 5 6 7 8 9 10 11 12 13 14 Since that time, several further studies approaching the original criteria of Malmgren et al have been published.15 16 17 18 19 20 21 22 23 24 25 26 27 The area of the world covered by these studies is still very limited, and reliable information remains sparse for nonwhite populations. Despite this deficiency, there is a broadening experience of studying the incidence of stroke in different environments and within different healthcare systems. Thus, an increasing number of studies may provide comparable incidence data to add to our knowledge of stroke incidence worldwide. It is important that these valuable data are not ignored simply because they are from studies that were not established as part of an international effort.
This article aims to extend and refine the original criteria of Malmgren et al in the light of further experiences of measuring stroke incidence, the identification of new problems and possible solutions, and the wider availability of imaging technology, which allows accurate pathological diagnosis. It discusses a set of standards for definitions, methods, and data presentation that individual studies of stroke incidence should fulfill to be considered comparable with one another. It does not attempt to cover all the practicalities of establishing such studies but highlights several important areas that may make comparisons difficult. It is based not only on an extensive review of the literature but also on a series of visits around the world in 1994 to meet with investigators in centers where stroke incidence has been studied for detailed discussions of study methods in the context of the particular local healthcare systems. Considering the successes and problems encountered should increase the ease with which further reliable studies can be established. We hope that this article will encourage those establishing stroke registers to consider the factors that will allow their data to contribute to the accumulating worldwide knowledge of stroke incidence. This is particularly true for the many developing countries for which reliable information simply does not exist.
The main concern of this article is to compare incidence studies in different parts of the world. Many of the issues also relate to studies of time trends in incidence. These may be assessed by continuous registration of strokes or by comparing the incidence measured during two or more discrete periods, separated by a number of years. In either case, internal consistency of methodology is essential so that any change detected is real. For comparison between studies in different locations, external consistency is also necessary.
The wider availability of CT scanning in a number of countries since the 1980s means that many more studies than were published at the time of the review of Malmgren et al can now make a reliable diagnosis of pathological type of stroke during life for the majority of cases. This may allow, for the first time, a reliable international comparison of the incidence of the individual pathological types of stroke (cerebral infarction, primary intracerebral hemorrhage, and subarachnoid hemorrhage). We include a discussion of the criteria that should make this possible.
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Why Measure Stroke Incidence? |
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TopAbstractIntroductionWhy Measure Stroke Incidence?...Measuring Stroke Incidence: A...Measuring and Comparing...Conclusions References |
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Limitations of Mortality Statistics
Mortality is the most readily available variable for comparing stroke rates between countries and monitoring changes with time, so why put enormous efforts into measuring incidence? Official mortality data may be convenient, but they rely on the accuracy of death certificates, which is questionable,28 29 and provide information about fatal cases of stroke only, telling us nothing about the significant proportion of stroke patients who survive, many with major disability. Furthermore, without knowledge of the accuracy of diagnostic methods they cannot tell us about the distribution of the different pathological types of stroke. Several possible explanations exist for the substantial differences in stroke mortality between countries and its trends with time. For example, the apparent recent decline in stroke mortality in many Western countries30 may reflect changes in diagnostic fashions and coding procedures or a real decline, explained by changes in incidence and/or case fatality. The latter may depend on the distribution of pathological types, disease severity, and management. A clearer, more complete picture is only obtained by examining incidence and case-fatality rates separately. If accurate, these measures allow more valid comparisons between countries, may yield data that can be used to follow trends with time, and assist in healthcare planning within communities.
Scope of Stroke Incidence Studies
Another advantage of
measuring incidence of stroke is the
potential of community-based studies to answer additional questions
based on an unbiased sample of incident cases (Table 1
).
These may include follow-up for outcome in terms of case fatality,
recurrence, and disability; case-control studies of various
risk factors; and assessment of stroke services. Expanding the yield
beyond the mere identification of cases helps to justify the intensive
effort put into the case-finding process. Careful study design is
crucial to ensure that the identified aims are achieved without the
collection of excess, useless data, which simply create extra work for
the investigators and may compromise the quality of the study. As for
incidence, the measurement of other variables should be
standardized for comparison. For case fatality, it is suggested that
the MONICA standard of 28-day case fatality be widely adopted.
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Measuring Stroke Incidence: A Discussion of Standard Criteria for a
Comparable Study (Table 2)
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TopAbstractIntroductionWhy Measure Stroke Incidence?...Measuring Stroke Incidence: A...Measuring and Comparing...Conclusions References |
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Standard Definitions
WHO Definition of Stroke
The WHO definition of stroke, "rapidly developing clinical signs of focal (at times global) disturbance of cerebral function, lasting more than 24 hours or leading to death with no apparent cause other than that of vascular origin,"31 is the broadly accepted standard. Some care is required with its interpretation. First, according to the definition, presentations of subarachnoid hemorrhage with sudden-onset headache, meningism, and no focal or global disturbance of cerebral function should be excluded. However, the definition is generally considered to include all cases of cerebral infarction, primary intracerebral hemorrhage, and subarachnoid hemorrhage. In practice, most investigators include all subarachnoid hemorrhages, and reports of studies should make this clear.
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Second, it is important to rely on the clinical criteria in the definition, with the distinction between stroke and transient ischemic attack (TIA) based on a duration of more (stroke) or less (TIA) than 24 hours. Advances in imaging technology have made us aware that a significant proportion of TIAs are associated with an appropriately located infarct visible on CT or MRI scan. Controversy exists regarding how these "cerebral infarcts with transient signs" should be classified and whether the presence of a visible infarct associated with a TIA alters prognosis.32 33 The availability and sensitivity of imaging technology vary enormously with place and time. Abandoning the clinical distinction between TIA and stroke for one based on imaging would create spurious variability between studies and compound the difficulties in comparing their results.
A similar problem is posed by "silent infarcts"—areas of presumed infarction visible radiologically with no associated symptomatic episode. Again, it would be inappropriate to include these as incident strokes, not only for the reasons outlined in the preceding paragraph but also because, in the absence of symptoms, it is impossible to know when the event leading to the abnormal scan appearance occurred.
First-Ever-in-a-Lifetime Strokes
If we wish comparisons to give us pointers to important
determinants of disease etiology, first-ever-in-a-lifetime
strokes are the preferred numerator because they most closely reflect
these factors. Some studies base their incidence estimates on the
number of first stroke events occurring within the study
period.31 34 These estimates do not exclude those who
had
a stroke before the start of the study, thereby including a number of
recurrent strokes that are not true incident cases. Others count all
strokes within the study period.35 Because there is no
consistent relationship between
first-ever-in-a-lifetime strokes, first-event strokes,
and all strokes,3 it is meaningless to compare incidence
measurements based on different definitions (Figure).
Including recurrent strokes in the numerator makes sense for assessing
the total burden of stroke for local healthcare planning. Thus, studies
examining stroke services may also register recurrent strokes but will
need available data on first-ever-in-a-lifetime strokes for
any etiologic comparisons.
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In addition, because many intercurrent illnesses can cause neurological deterioration, defining a recurrent stroke is often difficult in clinical practice, making first-ever-in-a-lifetime stroke a more accurate comparator. Its accuracy requires a careful history and review of all available past records for each potential case to ensure that subjects with previous strokes are not included as incident cases.
Standard Methods
Complete, Community-Based Case
Ascertainment
Malmgren et al3 found many studies
measuring
incidence in hospital-based populations. These never
represent the whole community because there will always be some
cases not admitted to the hospital (Table 3).
Furthermore, they cannot be used for comparisons of place or time:
hospitalization rates for stroke vary considerably between and even
within countries and are likely to vary with time as management
strategies change and new treatments for acute stroke
emerge.13 19 36 37 In the
Oxfordshire Community Stroke
Project, which was performed in the 1980s, 40% of incident stroke
patients were not admitted to the hospital.36 This
contrasts with the situation in Swedish studies from the same period
and later, which demonstrate admission rates of 95% or
more.4 13 38 There is also evidence that
hospital-based stroke registers are biased toward younger patients
with more severe strokes.36 The authors of some
community-based studies of stroke incidence were surprised by the
significant proportion of cases they found to be managed outside the
hospital (eg, 15% in both Warsaw, Poland, and Umbria,
Italy19 24 ), demonstrating that such cases must be
rigorously searched for without simply assuming that all will be
admitted to the hospital. It is because they are entirely hospital
based that many of the studies from developing countries are unsuitable
for international comparisons.39 40 41
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True community-based studies must therefore use several overlapping
sources of information to ensure complete case ascertainment. Possible
sources are shown in Table 4. The local healthcare
system will determine which of these are applicable.
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Sources must be surveyed with adequate frequency, covering a broad spectrum of possible presentations of stroke so that cases are not missed. For example, labels such as "collapse," "dizziness," "headache," "fits," or "confusion" may reveal stroke cases. The importance of assessing patients labeled as TIA cases (from both hospital and community) as potential stroke cases is demonstrated by results from the Oxfordshire Community Stroke Project: 7% of incident strokes were initially referred to the investigators as TIAs but in fact had symptoms lasting longer than 24 hours.14
Sources outside the hospital, in particular primary healthcare physicians and nursing institutions, should be involved in the study and contacted regularly to ensure complete referral of community cases. Hospital discharge lists and computer-linked records schemes provide a useful check for patients not identified by admission and ward checks. Reviewing death certificates is the only way of finding patients who die without a referral being made. Their importance, like that of other sources, will depend on local practice and culture. Most studies find death certificates an important contributor of cases. However, a recent study in Okinawa, Japan, which examined death certificates in only one subpopulation of the total, found an insignificant number of cases from this source not already ascertained from others.42 Gathering whatever information is available retrospectively from relatives, attending physicians, medical records, and/or autopsy findings is required before possible death certificate cases can be confirmed (or refuted) as first-ever, WHO-defined strokes.
Assessing Completeness of Case
Ascertainment
It would be helpful to have some quantitative way of
assessing the
completeness of case ascertainment. One approach is to perform a
cross-sectional survey of the population, or a sample of it, at
intervals (usually every one or few years) during the study to find out
whether cases have been missed.6 35 43
Because many stroke
cases are among the elderly and disabled, who may be housebound,
labor-intensive and therefore expensive survey methods are required
to ensure that such cases are not excluded. Cross-sectional surveys
may also miss those minor strokes that patients tend to forget with
time and that may only be included at all if registered at the time of
presentation.
Studies that run for a period of several years can assess their own case-finding efficiency. For example, they may note the number of stroke cases found that are recurrences with a first-ever-in-a-lifetime stroke missed at an earlier stage during the study period. In addition, a surprisingly high or low case-fatality rate may alert investigators to the possibility that either fatal or mild, out-of-hospital cases are being missed. Participating centers in the WHO MONICA study are subject to a number of quality-control procedures to assess the validity of their data. Checks for case ascertainment require centers with case-fatality or out-of-hospital case referral rates falling outside certain arbitrarily determined limits to reexamine their data.44
There is currently no perfect, objective indicator of completeness of case ascertainment. Subjective judgment based on knowledge of the appropriateness of case-finding methods to the study population may be as reliable and less likely to provide false reassurance. No one source of cases will be either infallible or all-encompassing. Multiple overlaps between sources may be regarded as an indication of good case-finding methods as long as multiply referred cases are not registered more than once.10 However, it would be wasteful to concentrate resources on a source with negligible yield. We feel that investigators should identify all possible sources in their location and justify the exclusion of any that are not used. For example, quality-control checks of the WHO MONICA study in northern Sweden, where hospital admission rates are very high, revealed that an intensified effort by general practitioners over a 1-month period to refer all cases did not significantly increase the incidence rates.38 The investigators therefore concentrate on hospital cases and death certificates for case finding.
An interesting possibility is the capture-recapture technique, initially developed for estimating the size of animal populations and now being used in some areas of human disease epidemiology.45 46 It recognizes that no survey has complete coverage and allows an estimate to be made of the number of cases not ascertained, with the use of information from two or more overlapping sources of cases of the disease being counted. Complex adaptations of the technique are required in humans to adjust for the nonindependence of sources and variability between subgroups.45 46 47 The information required to attempt such an analysis is not available for any of the stroke incidence studies of which we are aware, except perhaps the Auckland study.10 11 Until this technique has been developed in stroke epidemiology, we must continue to rely on those methods already in use.
However complete we judge case-finding methods to be, we can only expect to find those cases that are presented to the sources surveyed. The Oxfordshire Community Stroke Project found that of those patients whose stroke was preceded by a TIA, only about half had sought medical attention for their TIA.48 Similarly, some persons with mild strokes might never seek medical attention. This is particularly likely among the elderly, who may attribute symptoms of a stroke to age or some age-associated disease such as osteoarthritis. Any individual study may thus underestimate stroke incidence, and this effect may vary between studies because of differences between study populations in the interpretation of symptoms, perception of their severity, and accessibility and cost of health care. These factors are not easy to control or measure, but their potential contribution to differences in incidence rates between studies, particularly in regard to mild strokes, cannot be ignored.
Importance of Prospective Study Design
Stroke is a clinical diagnosis, making accurate clinical
assessment by an appropriately qualified specialist an essential part
of any incidence study. There is no "gold standard"
diagnostic method superior to clinical judgment. For
example, CT or MRI scanning cannot necessarily distinguish between a
stroke and the transient focal weakness that may follow a seizure. The
rate of error, as judged by CT scanning, in the clinical diagnosis of
stroke versus nonstroke varies from 1.5% to
16%19 49 50 51 52 53
and appears to be dependent on the degree of skill and training of the
assessor. In community-based stroke registers, in which patients
are assessed soon after onset of symptoms by a neurologist or stroke
specialist with the specific intent of monitoring stroke incidence, the
error rate is below 2%.19 49 Only truly prospective
studies that pursue cases as they occur—termed "hot
pursuit"—provide this degree of accuracy.
Retrospective collection of information ("cold pursuit") is more liable to cause blurring of the margin between TIAs and strokes than is the hot-pursuit method. One of the reasons for increased accuracy with prospective design is that a clinician managing an individual patient has a different agenda from a study epidemiologist or neurologist measuring incidence in the population. The clinician recognizes that making a precise distinction between a TIA lasting 20 hours and a minor stroke with resolution of symptoms by 30 hours is unnecessary because it will affect neither prognosis nor management. Because this information is not considered relevant, it may either be documented inaccurately or not recorded at all. For the investigator wishing to compare different studies of stroke incidence the distinction, albeit artificial, is important. A further example is the assessment of a patient's history. Previous strokes, minor ones in particular, are much more likely to be ascertained prospectively by a study neurologist or epidemiologist aware of the importance of including only first-ever-in-a-lifetime strokes in the incidence figures.
Many centers in the WHO MONICA study use the cold-pursuit approach, with review of records after hospital discharge and death certificates as the main sources of cases.1 This will provide valuable information about incidence trends as long as diagnostic methods remain constant. Cold-pursuit methods have the advantage of consuming considerably less time and resources than hot-pursuit ones. However, it may be invalid to compare studies using this method with each other or with those using the hot-pursuit method without knowing how overall case ascertainment is affected in any particular center. Centers best suited to cold pursuit will require a very reliable records system and should be able to demonstrate that hot-pursuit methods do not materially alter case ascertainment.
Studies based entirely on retrospective reviews of records depend on complete record ascertainment for the whole community and accurate documentation. These are rarely demonstrated, but exceptions may exist. For example, the Mayo Clinic has a records system that appears to be unique in its complete, reliably documented coverage of the whole Rochester community. In this particular case, as long as the information is appropriately accessed, retrospective methods may be considered as reliable as prospective methods.54
The Study Population
The best populations are well
defined (usually, but not always, on
a geographic basis) and stable, with limited in- and out-migration.
Investigators cannot manipulate populations: they simply have to be
opportunistic in selecting what is available. Relatively isolated
populations, for example, the inhabitants of Japan's Okinawa
islands42 or the Valle d'Aosta in northern
Italy,20 are particularly suitable. Such situations limit
the "cross-boundary effect" in which cases are either missed,
because they occur while a resident is outside the study area, or are
included erroneously when they occur in visitors who are not permanent
residents. Unstable populations, with frequent permanent changes of
residence into and out of the study area, are less reliable. However,
the more isolated a population is, the less
representative of its country it may be because of the
effects of such factors as a restricted gene pool and special dietary
habits. A sensibly selected population takes these various opposing
factors into account. Populations composed of healthy self-selected
volunteers or excluding certain disease states (for example, the
Framingham Study55 ) are not really suitable for a
comparable incidence study.
The size of the population is important because the larger the population, the more strokes are likely to occur within the monitoring period, and the confidence interval around estimates of incidence is dependent on the number of strokes contributing to the estimate.56 There is no perfect population size. Because most strokes occur in the elderly, populations with a high proportion of older people will yield more strokes for the same total population size than will younger populations. Monitoring too large a population is difficult without extensive resources and may lead to undercounting. Some investigators increase the number of stroke cases by monitoring the same population for several years (but ideally not more than 5; see below) for a single estimate based on the number of person-years observed.15 16 17 18 19 24 57 It is suggested that below approximately 250 cases the confidence interval becomes unacceptably wide. For populations with a Western European type of structure, this will require approximately 100 000 person-years of observation. Estimates of incidence from many cohort studies have limited precision because of small population size.55 58 59 It is emphasized that although they provide an idea of the statistical precision of the estimate, confidence intervals do not allow for methodological flaws such as incomplete case ascertainment.
The accuracy of determining the denominator must also be considered. Investing resources in obsessional case finding is inappropriate unless reliable and up-to-date information on the age and sex structure of the population is also available. For an appropriately large population (see above), minor inaccuracies have little effect on incidence rates but major ones must be avoided. Most studies use official census statistics, which are usually (but not always60 ) reliable in developed countries. Their unreliability in developing countries makes them inappropriate for estimating denominator size. Unfortunately, few populations will have census information for every year. Studies performed during the census year can use the census data as they stand.11 25 Those performed between censuses require an estimate of the denominator. Official updates of the census rely on information about births, deaths, and in- and out-migration.4 13 Because these are often inaccurate (Sweden, with accurate updates fortnightly, is an exception), investigators may prefer to rely on interpolation of census data, based on prior trends.15 The error can be estimated when subsequent census statistics become available. In general, it increases with the time from the last census. In populations in which the vast majority of people are registered with a general practitioner, the denominator may be based on the age/sex registers of general practices.14 One potential problem here is the existence of "ghosts": patients who have died or moved but who have not yet been removed from the practice list.
A further consideration is that incidence measurements should really be based on the population at risk. This implies that we should remove from the denominator any prevalent cases, ie, those who have already suffered a stroke. In practice, the information is simply not available to the vast majority of investigators so that adjustments for prevalence are not made. We can assume that the effect in the younger age groups in whom prevalence is low would be minimal. In older age groups the effect in those populations where it has been assessed appears to be significant (R. Brown, unpublished data, 1995).
Standard Data Presentation
Data collected over complete years
avoids confounding from the
possible effect of seasonal variations in incidence documented in
several community-based studies.61 62 63
From the
Rochester group's results, it appears that incidence rates can vary
secularly over periods of approximately 5 years.5 This
implies that rates should not be averaged over time intervals longer
than 5 years and that comparisons between different studies should be
confined to similar points in time.
Most stroke epidemiologists use mid-decade 10-year age bands (eg, 45 to 54, 55 to 64 years). It seems reasonable to retain this convention in publications. However, it is helpful to collect data for both numerator and denominator in narrower 5-year bands for two reasons. First, in some other areas of epidemiology the convention is to use 10-year age bands spanning a complete decade (eg, 50 to 59, 60 to 69 years).64 The availability of 5-year age bands allows comparisons between studies presenting data by nonmatching 10-year age bands, including those investigating the incidence of other diseases. Second, the distribution of ages within a 10-year age band may vary considerably between populations. Incidence rates in different studies can be compared either by looking at age-specific rates for a particular age band or by comparing age-standardized rates. The use of narrower age bands (5 rather than 10 years) reduces the effect on age-standardized rates of variability of age distribution within each age band, especially that occurring within the open-ended upper age group. Differences in incidence rates between populations may otherwise simply reflect a different distribution of ages within each age band. This effect was regarded by one reviewer as a potential explanation for the variation in incidence rates with time in the Rochester series.65 Thus, while it would be cumbersome to include rates for 5-year age groups in publications, it is helpful to have them available for comparisons with other studies and time trend studies. The population chosen for age standardization should be appropriate to the study populations. A comparison of stroke incidence rates among countries in Europe might use Segi's notional European population.66 Segi's world population would be more appropriate for a true worldwide comparison. Because of potential differences between the sexes, rates should be sex- as well as age-standardized. Age-specific rates should be presented separately for men and women.
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Measuring and Comparing Incidence of Pathological Types of Stroke |
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Main Pathological Types
The heterogeneity of stroke is a challenge for clinical epidemiologists. The standard WHO definition31 encompasses cerebral infarction, primary intracerebral hemorrhage, and subarachnoid hemorrhage. Our ability to distinguish the first two pathological types without neuroimaging (usually CT scanning, occasionally MRI) or, in fatal cases, autopsy, is limited.50 It is therefore not possible to draw firm conclusions about the incidence rates of pathological types of stroke in studies using mainly clinical criteria. In the Rochester series, the introduction of CT scanning caused an apparent increase in the rate of intracerebral hemorrhage because of the increased detection rate for small hemorrhages that would previously have been classified as infarcts.67 For many years, particularly high rates of primary intracerebral hemorrhage (22% to 36%) have been reported from countries in the Far East. These reports are from community-based studies with low CT scan rates,6 43 cohort studies with very small study populations,59 or hospital series that have high CT rates but that cannot be assumed to be representative of the whole community.68 69 Newer studies with both high rates of CT scanning and more complete case ascertainment42 are helping to resolve this issue, but there is still a lack of reliable, community-based information on pathological types from this part of the world. It is only when we have confirmation that the apparent excess of cerebral hemorrhages is real that searching for potential causes of this difference will be justified.
Definitions must be standardized for comparisons. We recommend the scheme used in the Oxfordshire Community Stroke Project.57 Appropriately timed CT scan (see below) or autopsy is required to distinguish infarct from intracerebral hemorrhage. The definition of subarachnoid hemorrhage is based on a typical clinical history with CT or lumbar puncture evidence of subarachnoid blood or angiographic demonstration of a source of bleeding. The distribution of pathologies can only be estimated accurately if the proportion with undetermined pathology is small. The problem of falling autopsy rates has been partly overcome in the Dijon Stroke Registry by postmortem CT scans (M. Giroud, unpublished data, 1994). It will never be possible to assign a definite pathological type to every incident case, but an acceptably accurate type can be ascribed to a proportion of cases without CT scan or autopsy. In line with the Oxfordshire Community Stroke Project, we consider it acceptable to use a well-validated clinical scoring system (such as the Guy's Hospital or Siriraj Score) for pathological diagnosis in those cases without CT scan or autopsy, provided the score is at one or the other extreme, giving a diagnostic accuracy for hemorrhage or infarct of 90% or more.70 71 72 For management of individual patients it is often important to be 100% certain about the distinction between infarct and hemorrhage, leading to criticism of these scores in clinical practice.73 However, it seems reasonable to use them for epidemiological studies as long as there is no consistent bias in one direction or the other. Two community-based studies have used clinical scores in combination with high (approximately 70%) CT rates in this way.19 57 Several others have high enough rates of CT scanning (above an arbitrarily selected level of approximately 70%) and autopsy diagnoses to make them suitable for examination of pathological types.16 20 21 23 24
The timing of neuroimaging is important. Several studies consider a CT scan within about 30 days of stroke to be reliable in distinguishing infarct from intracerebral hemorrhage.19 23 57 MR scanning may continue to be helpful after this stage,23 but its availability is often limited. Although it has been demonstrated that a number of small primary intracerebral hemorrhages may be indistinguishable from infarcts on CT scan as early as 2 weeks after onset,74 studies of serially scanned hemorrhages are not large enough to tell us what proportion of hemorrhages we may be misinterpreting as infarcts by performing scans after 2 weeks.75 The 30-day cutoff may still be reasonable for epidemiological purposes, but we do not know. Many centers now scan most cases very early, within 24 hours of onset. However, the issue is important for those countries with many stroke patients managed outside the hospital, with limited scanning facilities and long prescan waiting times.
With early scanning there is concern about misdiagnosis of some cases of hemorrhagic transformation of infarct as primary hemorrhage. There is increasing evidence that such transformation may occur very early, even within hours of stroke onset.76 For the moment this is another unresolved issue but one of which we need to be aware.
The ability of increasing numbers of community-based studies to provide accurate information on pathological types will enhance geographic comparisons. We will be able not only to compare the incidence of these types between countries but also to investigate more closely the difference in incidence between men and women. While it appears that the incidence of myocardial infarction is four to five times greater in men than in women, the incidence of total stroke varies much less between the sexes.77 One reason for this might be that greater differences are hidden until the pathological types are examined separately.
Subtypes of Cerebral Infarction
Cerebral infarction has a
number of possible etiologies with
differing patterns of clinical presentation and outcome.
There is no generally accepted way of classifying these subtypes. We
favor the classification developed by Bamford et al,78
dividing cerebral infarction on the basis of simple clinical criteria
into four subtypes: total anterior circulation infarction, partial
anterior circulation infarction, lacunar infarction, and posterior
circulation infarction. This classification is reasonably predictive of
etiology,79 prognosis,78 and the size and
site of cerebral infarction on CT scanning80 and has
reasonable interobserver agreement.81 Furthermore, it is
of particular value for epidemiological comparisons because, unlike
some classification systems,82 83 it does not require
a
large number of often invasive investigations. Even in centers with
easy access to such investigations, there remain many (40% to 50%)
infarcts of undetermined cause. Meticulous searching for a cause may be
clinically appropriate in individual cases, but for epidemiological
studies the exclusion of a large number of patients from assignment of
specific subtypes would make the overall analysis an
unrepresentative one.
A few studies fulfilling the core criteria for comparability have been able to apply this classification system to their cases of cerebral infarction.19 78 84 Others have been able to at least define lacunar infarction as a separate group16 24 with the use of the same clinical criteria.
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Conclusions |
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The above discussion is an attempt to create a framework for establishing future studies and for deciding which of the incidence studies performed to date are suitable for international comparisons. The worldwide visits that contributed so much to its content also led to the formation of a collaborative group of comparable studies of stroke incidence. Both qualitative and quantitative data are being collected and will be presented separately.
Table 2
summarizes the major standard criteria that make a
study of
stroke incidence comparable with others. The ideal study does not exist
in reality. However, to make sense of geographic and secular
comparisons, we should recognize that the studies that come close to
the ideal are the most likely to provide reliable and comparable
results. In comparing studies that use standard definitions and make a
concerted effort to search for out-of-hospital strokes, the
major source of potential error is still likely to be variable case
finding. Methods must vary between locations because of differences in
healthcare systems. Comparing the relative efficiency of these methods
is difficult. The possibility of comparing incidence of accurately
assigned pathological types and subtypes of cerebral infarction is an
interesting new prospect, based on advances in imaging technology that
are becoming increasingly widely available.
Our aim should be to use the lessons from previous incidence studies to design even better ones. The challenge is not only to explain the results that we have but also to find out what we can about stroke incidence in Africa, Asia, South America, and other areas about which so little is known but where so many of the world's people live. In developing countries, we might expect that, as life expectancy increases and the high-risk behaviors (eg, smoking, diet) of the Western lifestyle are increasingly adopted, strokes will be an escalating problem. Governments and makers of health policy are in no position to plan for the prevention of diseases that are an unknown quantity.
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Acknowledgments |
|---|
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 Martin Dennis, Peter Sandercock, and Mark Sudlow for their helpful comments on the manuscript.
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Footnotes |
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Reprint requests to Dr Cathie Sudlow, Registrar in Medical Neurology, Department of Clinical Neurosciences, University of Edinburgh, Western General Hospital, Crewe Rd, Edinburgh EH4 2XU, Scotland.
Received July 20, 1995; revision received December 19, 1995; accepted December 22, 1995.
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References |
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A. G. Thrift, H. M. Dewey, J. W. Sturm, S. L. Paul, A. K. Gilligan, V. K. Srikanth, R. A.L. Macdonell, J. J. McNeil, M. R. Macleod, and G. A. Donnan Greater Incidence of Both Fatal and Nonfatal Strokes in Disadvantaged Areas: The Northeast Melbourne Stroke Incidence Study Stroke, March 1, 2006; 37(3): 877 - 882. [Abstract] [Full Text] [PDF]
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M. Correia, M. R. Silva, R. Magalhaes, L. Guimaraes, and M. Carolina Silva Transient Ischemic Attacks in Rural and Urban Northern Portugal: Incidence and Short-Term Prognosis Stroke, January 1, 2006; 37(1): 50 - 55. [Abstract] [Full Text] [PDF]
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K. Carter, C. Anderson, M. Hacket, V. Feigin, P. A. Barber, J. B. Broad, R. Bonita, and on behalf of the Auckland Regional Community Strok Trends in Ethnic Disparities in Stroke Incidence in Auckland, New Zealand, During 1981 to 2003 Stroke, January 1, 2006; 37(1): 56 - 62. [Abstract] [Full Text] [PDF]
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R. Vibo, J. Korv, and M. Roose The Third Stroke Registry in Tartu, Estonia: Decline of Stroke Incidence and 28-Day Case-Fatality Rate Since 1991 Stroke, December 1, 2005; 36(12): 2544 - 2548. [Abstract] [Full Text] [PDF]
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R. Musolino, P. La Spina, S. Serra, P. Postorino, S. Calabro, R. Savica, G. Salemi, and G. Gallitto First-Ever Stroke Incidence and 30-Day Case Fatality in the Sicilian Aeolian Archipelago, Italy Stroke, December 1, 2005; 36(12): 2738 - 2741. [Abstract] [Full Text] [PDF]
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C. S. Anderson, K. N. Carter, M. L. Hackett, V. Feigin, P. A. Barber, J. B. Broad, R. Bonita, and on behalf of the Auckland Regional Community Strok Trends in Stroke Incidence in Auckland, New Zealand, During 1981 to 2003 Stroke, October 1, 2005; 36(10): 2087 - 2093. [Abstract] [Full Text] [PDF]
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S. L. Paul, J. W. Sturm, H. M. Dewey, G. A. Donnan, R. A.L. Macdonell, and A. G. Thrift Long-Term Outcome in the North East Melbourne Stroke Incidence Study: Predictors of Quality of Life at 5 Years After Stroke Stroke, October 1, 2005; 36(10): 2082 - 2086. [Abstract] [Full Text] [PDF]
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P. D. Syme, A. W. Byrne, R. Chen, R. Devenny, and J. F. Forbes Community-Based Stroke Incidence in a Scottish Population: The Scottish Borders Stroke Study Stroke, September 1, 2005; 36(9): 1837 - 1843. [Abstract] [Full Text] [PDF]
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S.A. Ogun, F.I. Ojini, B. Ogungbo, K.O. Kolapo, and M.A. Danesi Stroke in South West Nigeria: A 10-Year Review Stroke, June 1, 2005; 36(6): 1120 - 1122. [Abstract] [Full Text] [PDF]
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M. L. Hackett, C. Yapa, V. Parag, and C. S. Anderson Frequency of Depression After Stroke: A Systematic Review of Observational Studies Stroke, June 1, 2005; 36(6): 1330 - 1340. [Abstract] [Full Text] [PDF]
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E. Flossmann and P. M. Rothwell Family History of Stroke in Patients With Transient Ischemic Attack in Relation to Hypertension and Other Intermediate Phenotypes Stroke, April 1, 2005; 36(4): 830 - 835. [Abstract] [Full Text] [PDF]
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A. Tsiskaridze, M. Djibuti, G. van Melle, G. Lomidze, S. Apridonidze, I. Gauarashvili, B. Piechowski-Jozwiak, R. Shakarishvili, and J. Bogousslavsky Stroke Incidence and 30-Day Case-Fatality in a Suburb of Tbilisi: Results of the First Prospective Population-Based Study in Georgia Stroke, November 1, 2004; 35(11): 2523 - 2528. [Abstract] [Full Text] [PDF]
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J. W. Sturm, G. A. Donnan, H. M. Dewey, R. A. L. Macdonell, A. K. Gilligan, V. Srikanth, and A. G. Thrift Quality of Life After Stroke: The North East Melbourne Stroke Incidence Study (NEMESIS) Stroke, October 1, 2004; 35(10): 2340 - 2345. [Abstract] [Full Text] [PDF]
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V. K. Srikanth, J. F.I. Anderson, G. A. Donnan, M. M. Saling, E. Didus, R. Alpitsis, H. M. Dewey, R. A.L. Macdonell, and A. G. Thrift Progressive dementia after first-ever stroke: A community-based follow-up study Neurology, September 14, 2004; 63(5): 785 - 792. [Abstract] [Full Text] [PDF]
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V. L. Feigin and K. Carter Editorial Comment--Stroke Incidence Studies One Step Closer to the Elusive Gold Standard? Stroke, September 1, 2004; 35(9): 2045 - 2047. [Full Text] [PDF]
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A.J. Coull, L.E. Silver, L.M. Bull, M.F. Giles, P.M. Rothwell, and on behalf of the Oxford Vascular Study Direct Assessment of Completeness of Ascertainment in a Stroke Incidence Study Stroke, September 1, 2004; 35(9): 2041 - 2045. [Abstract] [Full Text] [PDF]
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M. Correia, M. R. Silva, I. Matos, R. Magalhaes, J. C. Lopes, J. M. Ferro, and M. C. Silva Prospective Community-Based Study of Stroke in Northern Portugal: Incidence and Case Fatality in Rural and Urban Populations Stroke, September 1, 2004; 35(9): 2048 - 2053. [Abstract] [Full Text] [PDF]
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C. S. Anderson, K. N. Carter, W. J. Brownlee, M. L. Hackett, J. B. Broad, and R. Bonita Very Long-Term Outcome After Stroke in Auckland, New Zealand Stroke, August 1, 2004; 35(8): 1920 - 1924. [Abstract] [Full Text] [PDF]
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J. Medin, A. Nordlund, and K. Ekberg Increasing Stroke Incidence in Sweden Between 1989 and 2000 Among Persons Aged 30 to 65 Years: Evidence From the Swedish Hospital Discharge Register Stroke, May 1, 2004; 35(5): 1047 - 1051. [Abstract] [Full Text] [PDF]
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U.G.R. Schulz, E. Flossmann, and P.M. Rothwell Heritability of Ischemic Stroke in Relation to Age, Vascular Risk Factors, and Subtypes of Incident Stroke in Population-Based Studies Stroke, April 1, 2004; 35(4): 819 - 824. [Abstract] [Full Text] [PDF]
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J. W. Sturm, G. A. Donnan, H. M. Dewey, R. A.L. Macdonell, A. K. Gilligan, and A. G. Thrift Determinants of Handicap After Stroke: The North East Melbourne Stroke Incidence Study (NEMESIS) Stroke, March 1, 2004; 35(3): 715 - 720. [Abstract] [Full Text] [PDF]
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U.G.R. Schulz and P.M. Rothwell Differences in Vascular Risk Factors Between Etiological Subtypes of Ischemic Stroke: Importance of Population-Based Studies Stroke, August 1, 2003; 34(8): 2050 - 2059. [Abstract] [Full Text] [PDF]
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S. Olindo, P. Cabre, R. Deschamps, C. Chatot-Henry, P. Rene-Corail, P. Fournerie, M. Saint-Vil, F. May, and D. Smadja Acute Stroke in the Very Elderly: Epidemiological Features, Stroke Subtypes, Management, and Outcome in Martinique, French West Indies Stroke, July 1, 2003; 34(7): 1593 - 1597. [Abstract] [Full Text] [PDF]
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R. Al-Shahi, J. J. Bhattacharya, D. G. Currie, V. Papanastassiou, V. Ritchie, R. C. Roberts, R. J. Sellar, and C. P. Warlow Prospective, Population-Based Detection of Intracranial Vascular Malformations in Adults: The Scottish Intracranial Vascular Malformation Study (SIVMS) Stroke, May 1, 2003; 34(5): 1163 - 1169. [Abstract] [Full Text] [PDF]
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R. Al-Shahi, J. J. Bhattacharya, D. G. Currie, V. Papanastassiou, V. Ritchie, R. C. Roberts, R. J. Sellar, and C. P. Warlow Scottish Intracranial Vascular Malformation Study (SIVMS): Evaluation of Methods, ICD-10 Coding, and Potential Sources of Bias in a Prospective, Population-Based Cohort Stroke, May 1, 2003; 34(5): 1156 - 1162. [Abstract] [Full Text] [PDF]
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P. Appelros, I. Nydevik, and M. Viitanen Poor Outcome After First-Ever Stroke: Predictors for Death, Dependency, and Recurrent Stroke Within the First Year Stroke, January 1, 2003; 34(1): 122 - 126. [Abstract] [Full Text] [PDF]
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J. W. Sturm, R. H. Osborne, H. M. Dewey, G. A. Donnan, R. A.L. Macdonell, and A. G. Thrift Brief Comprehensive Quality of Life Assessment After Stroke: The Assessment of Quality of Life Instrument in the North East Melbourne Stroke Incidence Study (NEMESIS) Stroke, December 1, 2002; 33(12): 2888 - 2894. [Abstract] [Full Text] [PDF]
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P. Appelros, I. Nydevik, A. Seiger, and A. Terent Predictors of Severe Stroke: Influence of Preexisting Dementia and Cardiac Disorders Stroke, October 1, 2002; 33(10): 2357 - 2362. [Abstract] [Full Text] [PDF]
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T. S. Field, M. D. Hill, and M. D. Connor Weather, Chinook, and Stroke Occurrence * Editorial Comment Stroke, July 1, 2002; 33(7): 1751 - 1758. [Abstract] [Full Text] [PDF]
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H.M. Dewey, A.G. Thrift, C. Mihalopoulos, R. Carter, R.A.L. Macdonell, J.J. McNeil, and G.A. Donnan Informal Care for Stroke Survivors: Results From the North East Melbourne Stroke Incidence Study (NEMESIS) Stroke, April 1, 2002; 33(4): 1028 - 1033. [Abstract] [Full Text] [PDF]
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J. W. Sturm, H. M. Dewey, G. A. Donnan, R. A.L. Macdonell, J. J. McNeil, and A. G. Thrift Handicap After Stroke: How Does It Relate to Disability, Perception of Recovery, and Stroke Subtype?: The North East Melbourne Stroke Incidence Study (NEMESIS) Stroke, March 1, 2002; 33(3): 762 - 768. [Abstract] [Full Text] [PDF]
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H. Ohkuma, S. Fujita, and S. Suzuki Incidence of Aneurysmal Subarachnoid Hemorrhage in Shimokita, Japan, From 1989 to 1998 Stroke, January 1, 2002; 33(1): 195 - 199. [Abstract] [Full Text] [PDF]
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P. L. Kolominsky-Rabas, M. Weber, O. Gefeller, B. Neundoerfer, and P. U. Heuschmann Epidemiology of Ischemic Stroke Subtypes According to TOAST Criteria: Incidence, Recurrence, and Long-Term Survival in Ischemic Stroke Subtypes: A Population-Based Study Stroke, December 1, 2001; 32(12): 2735 - 2740. [Abstract] [Full Text] [PDF]
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D. Smadja, P. Cabre, F. May, J.-L. Fanon, P. Rene-Corail, C. Riocreux, J.-C. Charpentier, P. Fournerie, M. Saint-Vil, and J. Ketterle ERMANCIA: Epidemiology of Stroke in Martinique, French West Indies: Part I: Methodology, Incidence, and 30-Day Case Fatality Rate Stroke, December 1, 2001; 32(12): 2741 - 2747. [Abstract] [Full Text] [PDF]
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L. Mihalka, V. Smolanka, B. Bulecza, S. Mulesa, and D. Bereczki A Population Study of Stroke in West Ukraine: Incidence, Stroke Services, and 30-Day Case Fatality Stroke, October 1, 2001; 32(10): 2227 - 2231. [Abstract] [Full Text] [PDF]
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H. M. Dewey, A. G. Thrift, C. Mihalopoulos, R. Carter, R. A.L. Macdonell, J. J. McNeil, and G. A. Donnan Cost of Stroke in Australia From a Societal Perspective: Results From the North East Melbourne Stroke Incidence Study (NEMESIS) Stroke, October 1, 2001; 32(10): 2409 - 2416. [Abstract] [Full Text] [PDF]
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C. Fieschi and A. Falcou Keynote address Neurology, September 1, 2001; 57(90002): S82 - 86. [Abstract] [Full Text]
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A. G. Thrift, H. M. Dewey, R. A.L. Macdonell, J. J. McNeil, and G. A. Donnan Incidence of the Major Stroke Subtypes: Initial Findings From the North East Melbourne Stroke Incidence Study (NEMESIS) Stroke, August 1, 2001; 32(8): 1732 - 1738. [Abstract] [Full Text] [PDF]
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R. G. J. Gibbs, R. Newson, R. Lawrenson, R. M. Greenhalgh, and A. H. Davies Diagnosis and Initial Management of Stroke and Transient Ischemic Attack Across UK Health Regions From 1992 to 1996 : Experience of a National Primary Care Database Stroke, May 1, 2001; 32(5): 1085 - 1090. [Abstract] [Full Text] [PDF]
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G. Engstrom, I. Jerntorp, H. Pessah-Rasmussen, B. Hedblad, G. Berglund, and L. Janzon Geographic Distribution of Stroke Incidence Within an Urban Population : Relations to Socioeconomic Circumstances and Prevalence of Cardiovascular Risk Factors Stroke, May 1, 2001; 32(5): 1098 - 1103. [Abstract] [Full Text] [PDF]
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 K. Tilling Capture-recapture methods--useful or misleading? Int. J. Epidemiol., February 1, 2001; 30(1): 12 - 14. [Full Text] [PDF]
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K N Vemmos, M L Bots, P K Tsibouris, V P Zis, C E Takis, D E Grobbee, and S Stamatelopoulos Prognosis of stroke in the south of Greece: 1 year mortality, functional outcome and its determinants: the Arcadia Stroke Registry J. Neurol. Neurosurg. Psychiatry, November 1, 2000; 69(5): 595 - 600. [Abstract] [Full Text] [PDF]
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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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Anonymous Epidemiology of Aneurysmal Subarachnoid Hemorrhage in Australia and New Zealand : Incidence and Case Fatality From the Australasian Cooperative Research on Subarachnoid Hemorrhage Study (ACROSS) Stroke, August 1, 2000; 31(8): 1843 - 1850. [Abstract] [Full Text] [PDF]
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Y. Morikawa, H. Nakagawa, Y. Naruse, M. Nishijo, K. Miura, M. Tabata, W. Hirokawa, S. Kagamimori, M. Honda, K. Yoshita, et al. Trends in Stroke Incidence and Acute Case Fatality in a Japanese Rural Area : The Oyabe Study Stroke, July 1, 2000; 31(7): 1583 - 1587. [Abstract] [Full Text] [PDF]
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R. Davenport and M. Dennis Neurological emergencies: acute stroke J. Neurol. Neurosurg. Psychiatry, March 1, 2000; 68(3): 277 - 288. [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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P. L. Kolominsky-Rabas, C. Sarti, P. U. Heuschmann, C. Graf, S. Siemonsen, B. Neundoerfer, A. Katalinic, E. Lang, K.-G. Gassmann, and T. R. von Stockert A Prospective Community-Based Study of Stroke in Germany—The Erlangen Stroke Project (ESPro) : Incidence and Case Fatality at 1, 3, and 12 Months Stroke, December 1, 1998; 29(12): 2501 - 2506. [Abstract] [Full Text] [PDF]
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A. Carolei, C. Marini, M. Di Napoli, G. Di Gianfilippo, P. Santalucia, M. Baldassarre, M. Giorgio De Matteis, and F. di Orio High Stroke Incidence in the Prospective Community-Based L'Aquila Registry (1994–1998) : First Year's Results Stroke, December 1, 1997; 28(12): 2500 - 2506. [Abstract] [Full Text]
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C.L.M. Sudlow and C.P. Warlow Comparable Studies of the Incidence of Stroke and its Pathological Types : Results From an International Collaboration Stroke, March 1, 1997; 28(3): 491 - 499. [Abstract] [Full Text]
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