(Stroke. 1997;28:793-798.)
© 1997 American Heart Association, Inc.
Articles |
Hospitalization and Case-Fatality Rates for Subarachnoid Hemorrhage in Canada From 1982 Through 1991
The Canadian Collaborative Study Group of Stroke Hospitalizations
From the Departments of Epidemiology and Biostatistics and of Family Medicine, University of Western Ontario, London, Ontario (T.Ø.); and the Division of Clinical Epidemiology, Royal Victoria Hospital, and the Department of Epidemiology and Biostatistics, McGill University, Montreal, Quebec (A.L., N.M.), Canada.
Correspondence to Truls Østbye, MD, MPH, Associate Professor, Department of Epidemiology and Biostatistics, University of Western Ontario, London, Ontario N6A 5C1, Canada. E-mail ostbye{at}uwo.ca
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Abstract |
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Background and Purpose Subarachnoid hemorrhage (SAH) has a different epidemiological profile from other types of stroke and a different etiology. Although there has been a general decline in overall stroke incidence since the 1950s, secular trends for SAH have been modest. In contrast to other stroke types, changes in incidence over the last few decades have been less clear. The purpose of this study was to estimate hospitalization and case-fatality rates of SAH according to age, sex, calendar year, and season.
Methods Data were obtained for each of Canada's 10 provinces for the 10 fiscal years 1982 through 1991. All hospitalizations of persons 15 years of age or older with a primary diagnosis at discharge coded 430 according to the International Classification of Diseases, 9th Revision, were included. Rates of SAH per 100 000 population were calculated for men and women for 5-year age groups, by calendar year, and by season. Annual age- and sex-specific (hospital) case-fatality rates up to 30 days were also calculated. Additionally, hospital deaths from this study were related to national SAH mortality statistics.
Results A total of 14 145 women and 8995 men were discharged with a primary diagnosis of SAH during the 10-year period. In contrast to other types of stroke, the rates of SAH were higher for women than for men at all ages. The age-standardized rates of SAH in 1991-1992 were 11.2 per 100 000 women and 8.0 per 100 000 men. For women, there was a 6% (95% confidence interval [CI], -12% to 0%) decline in hospitalization rates over that period; for men, the decline was 15% (95% CI, -21% to -8%). The peak season for SAH among women was winter; for men the peaks were in the fall and spring. For both sexes, the lowest occurrence was in the summer. Over this period, 30-day case-fatality rates declined somewhat (statistically significant only in the age group of 35 to 44 years). The number of deaths enumerated from hospital discharges was 20% to 50% lower than the number recorded on national mortality statistics, indicating that a proportion of SAH deaths occurred before (or after) the hospital stay.
Conclusions Although rates of hospitalization for SAH declined over this period, SAH remains an important neurological event affecting individuals at relatively young ages. The rates were higher for women than for men at all ages. Total (in-hospital) case-fatality rate remains high.
Key Words: Canada • epidemiology • hospitalization • mortality • subarachnoid hemorrhage
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Introduction |
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Subarachnoid hemorrhage occurs from the rupture of an artery or vein into the subarachnoid space. Aneurysms account for 70% to 80% of primary SAH, and arteriovenous malformations are responsible for 5% to 10%; 10% to 20% of patients have no anatomic abnormality observable by arteriography.1 In about one third of patients, SAH is an instantaneous, devastating occurrence.2 In all cases, SAH is a life-threatening event that needs aggressive medical or surgical management.
SAH is more common among women than men, and relative to other types of stroke, SAH is more common in younger persons. Reported incidence of SAH shows considerable geographic variation, from 3/100 000 per year in Libya3 to 37/100 000 in Finland,4 but even studies from within the same country have shown a wide range of incidence rates. Differences in study design (prospective, retrospective, or cross-sectional), the age structure of the study populations, sources of data (population- or hospital-based), completeness of case ascertainment, and the criteria used to define SAH may explain some of this variation. Although there has been a general decline in overall stroke incidence since the 1950s, reflecting changes in the prevalence of cardiovascular risk factors in the population,5 6 7 8 secular trends for SAH have been modest.9
Risk factors for SAH are not as well delineated as are the risk factors for other subtypes of stroke, and there are likely genetic influences.10 The two strongest modifiable risk factors are hypertension and smoking. For hypertension, RRs of 2.2 for men and 5.6 for women4 have been reported. Neaton et al11 reported a 29% increase in risk of SAH per 10 mm Hg increase in blood pressure in American men, and Yano et al12 found an RR of 1.7 per 20 mm Hg for Japanese men in Hawaii. For smoking, RRs between 1.3 and 3.0 have been reported.11 12 13 One study reported an RR of 4.7 for high alcohol consumption (>150 g/wk).14 The roles of cholesterol, adiposity, diabetes mellitus, and stress remain controversial in SAH.11 12 15 Of potential etiologic relevance are the circannual (seasonal) and circadian (diurnal) patterns that have been reported from various countries.16 17 18 19
The impact of SAH is considerable because it is very often fatal. Case-fatality rates (28-day) ranging from 22% to nearly 50% have been reported.20 21 22 23 Age has been found to be a predictor of survival after SAH,24 and men have had a better prognosis than women.20 Case-fatality rates have declined over the past few decades, likely due to advances in medical and surgical management.25
In Canada, data on hospitalizations for the entire population are available and have been used to describe the epidemiology of stroke.26 The epidemiology of SAH has never been described in Canada. The purpose of this study was to estimate hospitalization and case-fatality rates of SAH in Canada according to age, sex, calendar year, and season.
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Subjects and Methods |
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The methods for this study were similar to those previously reported for the study of hospitalizations for cerebral infarction and intracerebral hemorrhage in Canada.26 Briefly, data were obtained from the hospitalization database for each Canadian province for the 10 fiscal years 1982 through 1991. Hospitalizations with a primary discharge diagnosis of SAH, coded according to the ICD-9 as 430, were extracted. Previous validation studies from two Canadian provinces27 and the United States28 have indicated that SAH is accurately identified on hospital discharge data. For each province, records were obtained for all residents 15 years of age and over who were discharged (deceased or alive) from provincial acute-care hospitals. Persons discharged from long-term-care hospitals, from long-term-care units within acute-care hospitals, or rehabilitation hospitals, as well as out-of-province residents, were not included. Exclusions were made to eliminate redundant entries that occurred when a patient was transferred from one hospital to another for the management of the same hemorrhagic event.
Rates were calculated for men and women separately and for five age groups. Denominators for these rates were the numbers of persons in each age and sex stratum as determined from the 1981, 1986, and 1991 censuses of the entire Canadian population.29
Poisson regression30 was used to model the natural logarithm of the age- and sex-specific rates of hospital discharge for SAH as a function of year. The exponent of the regression coefficient for year (ßi) from each of the Poisson models was used as an estimate of the annual change in the rate of hospital discharge. A smoothed estimate of the total percent change in the stratum-specific rates over the 10 years of study was calculated using the following formula: 100x{[exp(10xßi)]-1}, where i indicates the ith age- and sex-specific stratum. The standard error of the regression coefficient was used to calculate 95% CIs.
To examine whether there was a circannual (seasonal) pattern of SAH,
the numbers of events occurring per month and season (adjusted for
number of days per month) were compared, using the admission date as a
proxy for the date of onset. A 
2 test was used to
test for differences in proportions of SAH among seasons (winter,
December through February; spring, March through May; summer, June
through August; autumn, September through November).
Annual age- and sex-specific, 30-day, in-hospital case-fatality rates were calculated as the proportion of all discharges in each stratum that ended in death within 30 days. For these rates, contiguous hospitalizations were combined into one discharge record. Logistic regression was used to determine whether there were differences in the in-hospital case-fatality rate according to age group or sex and over time.
Additionally, we compared the number of deaths enumerated from this data set on hospital discharges with the number of deaths recorded on the national SAH mortality statistics31 for the 5 most recent years.
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Results |
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The total number of hospital discharges for SAH over this 10-year period was 23 140 (14 145 women and 8995 men). The numbers of hospitalizations in Canada for SAH by age, sex, and fiscal year are shown in Table 1
. The estimated percent change in rate
over time by sex and age group is also given. These figures show that
for men the rates declined significantly over time across all age
groups except for the oldest category (65 years and over). For women,
the only significant decline was observed for the age group 35 to 44
years.
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Fig 1 shows the age-specific rates of SAH for men (A)
and women (B) in comparison with rates for cerebral infarction and
intracerebral hemorrhage previously reported
for the same time period.32 The rate of SAH for both men
and women increased with age and reached a plateau for men of 16.2 per
100 000 between ages 55 and 59 years; for women, a plateau of 24.4 per
100 000 was reached between ages 69 and 74 years.
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The annual age-standardized rates of SAH for men and women,
respectively, are presented in Fig 2. Over all
years, these rates were higher among women than men. For men, the
age-specific declines, which were relatively consistent across
age groups (see Table 1
), yielded an overall age-adjusted decline of
15% (95% CI, -21% to -8%). For women, the overall age-adjusted
decline was 6% (95% CI, -12% to 0%).
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Fig 3 shows that there were large and
statistically significant differences in the seasonal number of
admissions for SAH. The greatest number of admissions among women
occurred in the winter months; for men, peaks were observed in the fall
and spring. For both sexes, the lowest occurrence was in the summer,
notably July.
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Age-specific case-fatality rates for the first and last year of the
study are presented in Table 2, adjusted for
sex. Rates were presented adjusted for sex rather than
sex-specific because there were only minor differences between men and
women in the 30-day, in-hospital case-fatality rates. The estimated
percent change over the entire period, as calculated through the
regression coefficients obtained from logistic regression, is also
presented. In-hospital case-fatality rates declined for all
ages (except for the very oldest age group). The declines ranged from
8% in the 45- to 54-year-old age group to 26% in those aged 35 to 44
years. (The decline was statistically significant only in the 35- to
44-year age group.)
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In all age groups, most of the (in-hospital) deaths occurred during the first week after admission. Only in the two older age groups did the risk continue appreciably beyond 7 days.
Table 3 presents the numbers of deaths recorded
for SAH through routinely reported mortality statistics and the number
of deaths identified for SAH from the hospital discharge database. The
proportion of total mortality that was attributed to in-hospital deaths
is also presented. Table 3 indicates that younger persons,
especially men, have a lower proportion of deaths occurring in the
hospital. For example, for men aged 15 to 34 years, Statistics Canada
reported 181 deaths; 89 deaths were identified from the hospital
discharge database. Therefore, according to these data, 49.4% of
deaths occurred in the hospital, and 50.6% occurred either before or
after the hospital stay. For women aged 15 to 34 years, 71.6% of all
recorded deaths were identified by hospital discharge records;
28.4% were not identified by hospital discharge records.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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This Canadian study confirms that SAH has a different epidemiological pattern than other types of stroke, affecting relatively younger individuals. The rate of SAH was highest around age 55 years for men and age 60 for women. This contrasts with the rates for cerebral infarction and intracerebral hemorrhage, which increase exponentially with increasing age.26 SAH is the most common form of stroke until the fifth or sixth decade of life. This age pattern is likely caused by pathological mechanisms unrelated to normal aging,32 namely rupture of a congenital aneurysm or arteriovenous malformation of intracranial vessels.12
The seasonal pattern observed is consistent with that reported recently by Gallerani et al.18 19 Higher rates of SAH during the winter months have been associated with meteorological factors such as low humidity, low temperature,16 and short duration of sunshine (serotonergic mechanism).17 The winter excess has been linked to physiological responses to cold, such as increases in platelet and red cell counts,33 increased blood pressure34 and sympathetic nerve activity,35 and decreased factor VIII and increased fibrinolytic activity in blood.36
Different seasonal patterns in men and women have also been observed elsewhere.37 Different hormonal effects in men and women38 may be responsible for these sex differences in seasonal effects, for the somewhat different age distribution of cases, and for the overall difference in occurrence.
This study also showed that hospitalization for SAH declined from 1982 through 1991. This is consistent with the study by Harmsen et al,20 who observed a decrease in incidence in Sweden from 1971 to 1987. In contrast, other studies,39 40 including a recent meta-analysis9 covering three decades of data, showed stable incidence rates. The increased use of CT scans may have increased the accuracy with which SAH was differentiated from other conditions leading to blood in the cerebrospinal fluid. The net effect would reduce the number of other types of hemorrhage incorrectly classified as SAH. On the other hand, Yano et al12 argue that better diagnostic tools might have led to an apparent increase in the incidence of SAH through the inclusion of minor events. The complex relationship between modifiable risk factors, genetic predisposition, and diagnostic technology makes interpretation of the change over time difficult. Nevertheless, SAH remains an important contributor to morbidity and mortality for many adults in the prime of their life, and this condition therefore warrants ongoing population-based surveillance.
More aggressive surgical management25 could have
contributed to better in-hospital survival in the younger age groups
than in the older ones (Table 2). The trend toward improvement in
30-day survival is consistent with other
studies20 25 and may be associated with improved
management of secondary complications.41
It is unlikely that the trend toward a decline in in-hospital case-fatality rates can be attributed to an increase in posthospital deaths because of an increasing propensity for early discharge. The length of stay over this period was quite long and did not decline appreciably (21.1 days in 1982-1984 to 19.7 days in 1990-1992). In addition, SAH is rapidly fatal: the median time to death in the hospital was less than 5 days.
The discrepancy between the number of deaths identified through this examination of hospital discharges and the national mortality statistics is likely due to out-of-hospital deaths. It is not possible to discern whether these deaths occurred before or after hospitalization. Young men had the lowest proportion of deaths identified as occurring in the hospital. SAH in young men may be more severe than in women and more rapidly fatal; alternatively, women may present for care at an earlier phase in the symptomatology of SAH.
Hospital discharge data are a potentially valuable resource for
estimating rates of illness in the population, but this type of data
has some known limitations.39 Rates of hospitalization
consistently underestimate incidence primarily because cases
that are not hospitalized are not ascertained. For SAH, cases of sudden
death will be missed, but all other occurrences will be hospitalized.
Between 5% and 15% of all occurrences of SAH have been estimated to
end in sudden death.42 43 44 These deaths likely explain the
largest part of the difference between the number of in-hospital deaths
and total mortality for SAH. We believe death occurring shortly after
discharge from the acute-care hospital to be less of an issue (see
Table 3).
Another limitation in using administrative data for disease surveillance is that the accuracy of the diagnostic codes is not assured. However, previous studies have illustrated that SAH is well identified on hospital discharge data.27 28 Diagnostic investigations more frequently confirm the clinical diagnosis in cases of SAH than in cases of other types of stroke.45
Previous epidemiological investigations of SAH have mostly been relatively small hospital-based studies or studies from local stroke registries. In these studies, the source population has usually been ill defined, too small, or restricted in time; the numbers of events are therefore too small to yield stable estimates of rates. Often, SAH has been included with other stroke types and not been considered as a distinct entity. National population-based studies have been rare.45 Such studies are difficult and costly to perform without access to population-based data banks. Routinely collected healthcare data do not provide accurate estimates of the health of the population without universal healthcare coverage.46
Hospital discharge data have arguably been underutilized for monitoring SAH, relative to other diseases in general and other types of stroke in particular. The acute and serious nature of SAH, as well as the fact that SAH affects relatively younger individuals, means that hospitalization is almost always necessary and further implies that hospitalization data are well suited for ongoing surveillance. This is particularly true in countries that have universal health care, since coverage of the entire population is virtually complete.46
Conclusions
Although there has likely been a slight decrease in incidence over
the last decade, SAH remains an important health problem in Canada.
Despite recent advances in neurosurgical techniques,1 the
overall outcome after aneurysmal SAH remains poor. Further
reductions of the known risk factors of hypertension and smoking, as
well as earlier diagnosis and treatment, are desirable. Although there
are likely genetic and sex-related factors underlying SAH, these are at
present unknown,10 and epidemiological studies of
known and other environmental, lifestyle, and genetic risk factors need
to be carried out, since primary prevention is likely to be the
principal strategy to fight a disease with such a high
case-fatality rate.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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This study was funded through a grant from Health Canada: National Health Research Development Program 6605-392-57. The authors acknowledge the contribution of the other members of the Canadian Collaborative Study Group of Stroke Hospitalizations: Doreen Neville, Newfoundland; Susan Kirkland, Nova Scotia; Cam Mustard, Manitoba; Bruce Reeder, Saskatchewan; Michel Joffres, Alberta; and Gerhard Brauer, British Columbia. The authors would also like to thank David D'Andrea, McGill University, and Larry Svenson, Alberta Health.
Received October 28, 1996; revision received January 27, 1997; accepted January 27, 1997.
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References |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
- Day AL, Salcman M. Subarachnoid hemorrhage. Am Fam Physician. 1989;40:95-105.
- Subarachnoid hemorrhage. In: Toole JF, ed. Cerebrovascular Disorders. New York, NY: Raven Press Publishers; 1990:451-470.
- Ashok PP, Tadhakrishnan K, Sridharan E, El-Mangoush MA. Incidence and pattern of cerebrovascular disease in Benghazi, Libya. J Neurol Neurosurg Psychiatry. 1986;49:519-523. [Abstract]
- Knekt P, Reunanen A, Aho K, Heliövaara M, Rissanen A, Aromaa A, Impivaara O. Risk factors for subarachnoid hemorrhage in a longitudinal population study. J Clin Epidemiol. 1991;44:933-939. [Medline] [Order article via Infotrieve]
- Garraway WM, Whisnant JP, Furlan AJ, Phillips LH II, Kurland LT, O'Fallon WM. The declining incidence of stroke. N Engl J Med. 1979;300:449-452. [Abstract]
- Garraway WM, Whisnant JP, Drury I. The continuing decline in the incidence of stroke. Mayo Clin Proc. 1983;58:520-523. [Medline] [Order article via Infotrieve]
- Gillum RF, Gomez-Marin O, Kottke TE, Jacobs DR Jr, Prineas RJ, Folsom AR, Luepker RV, Blackburn H. Acute stroke in a metropolitan area, 1970 and 1980: the Minnesota Heart Survey. J Chronic Dis. 1985;38:891-898. [Medline] [Order article via Infotrieve]
-
Bonita R, Beaglehole R. Monitoring stroke: an
international challenge. Stroke. 1995;26:541-542.
[Free Full Text] -
Linn FHH, Rinkel GJE, Algra A, van Gijn J.
Incidence of subarachnoid hemorrhage: role of region,
year, and rate of computed tomography: a meta-analysis.
Stroke. 1996;27:625-629.
[Abstract/Free Full Text] -
Teunnissen LL, Rinkel GJE, Algra A, van Gijn J.
Risk factors for subarachnoid hemorrhage.
Stroke. 1996;27:544-549.
[Abstract/Free Full Text] - Neaton JD, Wentworth DN, Cutler J, Stamler J, Kuller L, for Multiple Risk Factor Intervention Trial Research Group. Risk factors for death from different types of stroke. Ann Epidemiol. 1993;3:493-499. [Medline] [Order article via Infotrieve]
- Yano K, Popper JS, Kagan A, Chyou P, Grove JS. Epidemiology of stroke among Japanese men in Hawaii during 24 years of follow-up: the Honolulu Heart Program. Health Rep. 1994;6:28-38. [Medline] [Order article via Infotrieve]
- Shinton R, Beevers G. Meta-analysis of relation between cigarette smoking and stroke. BMJ. 1989;298:789-794.
- Stampfer MJ, Colditz GA, Willett WC. A prospective study of moderate alcohol consumption and the risk of coronary disease and stroke in women. N Engl J Med. 1988;319:267-273. [Abstract]
-
Harmsen P, Rosengren A, Tsipogianni, Wilhelmsen
L. Risk factors for stroke in middle-aged men in Goteborg,
Sweden. Stroke. 1990;21:223-229.
[Abstract/Free Full Text] - Lejeune J-P, Vinchon M, Amouyel P, Escartin T, Escartin D, Christiaens J-L. Association of occurrence of aneurysmal bleeding with meteorologic variations in the North of France. Stroke. 1994;25:338-341. [Abstract]
- Vinall PE, Maislin G, Michele JJ, Deitch C, Simeone FA. Seasonal and latitudinal occurrence of cerebral vasospasm and subarachnoid hemorrhage in the northern hemisphere. Epidemiology. 1994;5:302-308. [Medline] [Order article via Infotrieve]
- Gallerani M, Trappella G, Manfredini R, Pasin M, Napolitano M, Migliore A. Acute intracerebral haemorrhage: circadian and circannual patterns of onset. Acta Neurol Scand. 1994;89:280-286. [Medline] [Order article via Infotrieve]
-
Gallerani M, Portaluppi F, Maida G, Chieregato A,
Calzolari F, Trapella G, Manfredini R. Circadian and circannual
rhythmicity in the occurrence of subarachnoid
hemorrhage. Stroke. 1996;27:1793-1797.
[Abstract/Free Full Text] -
Harmsen P, Tsipogianni A, Wilhelmsen L. Stroke
incidence rates were unchanged, while fatality rates declined, during
1971-1987 in Göteborg, Sweden. Stroke. 1992;23:1410-1415.
[Abstract/Free Full Text] -
Giroud M, Milan C, Beuriat P, Gras P, Essayagh E,
Arveux P, Dumas R. Incidence and survival rates during a
two-year period of intracerebral and
subarachnoid haemorrhages, cortical infarcts, lacunes
and transient ischaemic attacks: the Stroke Registry of Dijon,
1985-1989. Int J Epidemiol. 1991;20:892-899.
[Abstract/Free Full Text] - Bamford J, Sandercock P, Dennis M, Burn J, Warlow C. A prospective study of acute cerebrovascular disease in the community: the Oxfordshire Community Stroke Project, 1981-86. J Neurol Neurosurg Psychiatry. 1990;53:16-22. [Abstract]
-
Matsumoto N, Whisnant JP, Kurland LT, Okazaki H.
Natural history of stroke in Rochester, Minnesota, 1955 through 1969:
an extension of a previous study, 1945 through 1954.
Stroke. 1973;4:20-29.
[Abstract/Free Full Text] - Broderick JP, Brott T, Tomsick T, Miller R, Huster G. Intracerebral hemorrhage more than twice as common as subarachnoid hemorrhage. J Neurosurg. 1993;78:188-191. [Medline] [Order article via Infotrieve]
- Ingall TJ, Whisnant JP, Wiebers DO, O'Fallon WM. Has there been a decline in subarachnoid hemorrhage mortality? Stroke. 1989;20;718-724.
-
Mayo NE, Neville D, Kirkland S, Østbye T, Mustard CA,
Reeder B, Joffres M, Brauer G, Levy AR. Hospitalization and
case-fatality rates for stroke in Canada from 1982 through
1991. Stroke. 1996;27:1215-1220.
[Abstract/Free Full Text] - Mayo NF, Chockalingam A, Reeder BA, Philips S. Surveillance for stroke in Canada. Health Rep. 1994;6:62-72. [Medline] [Order article via Infotrieve]
- Leibson CL, Naessens JM, Brown RD, Whisnant JP. Accuracy of hospital discharge abstracts for identifying stroke. Stroke. 1994;25:2348-2355. [Abstract]
- Statistics Canada. Censuses 1981, 1986, 1991 of Canada. Age, Sex and Marital Status. Catalog No. 93-301. Ottawa, Ontario, Canada: Ministry of Supply and Services.
-
Frome EL, Checkoway H. Epidemiologic programs
for computers and calculators: use of Poisson regression models in
estimating incidence rates and ratios. Am J
Epidemiol. 1985;121:309-323.
[Abstract/Free Full Text] - Statistics Canada. Mortality: Summary List of Causes 199x. Catalog No. 84-902. Ottawa, Ontario, Canada: Ministry of Supply and Services.
- Melton LJ III. A `Gompertzian' view of osteoporosis. Calcif Tissue Int. 1990;46:285-286. [Medline] [Order article via Infotrieve]
- Keatinge WR, Coleshaw ERK, Cotter F. Increases in platelet and red cell counts, blood viscosity, and arterial pressure during mild surface cooling: factors in mortality from coronary and cerebral thrombosis in winter. BMJ. 1984;289:1045-1048.
- Brennan PJ, Greenberg G, Miall WE, Thompson SG. Seasonal variation in arterial blood pressure. BMJ. 1982;285:919-923.
- Hata T, Ogihara T, Maruyama A. The seasonal variation of blood pressure in patients with essential hypertension. Clin Exp Hypertens (A). 1982;4:341-354. [Medline] [Order article via Infotrieve]
-
Bull GM, Brozovic M, Chakrabarti R, Meade TW, Morton J,
North WR, Stirling Y. Relationship of air temperature to various
chemical, haematological, and haemostatic variables.
J Clin Pathol. 1979;32:16-20.
[Abstract/Free Full Text] - Cad D, Chen TL, Bronstein K, Brass LM. Seasonal fluctuation in the incidence of intracranial aneurysm rupture and its relationship to changing climatic conditions. J Neurosurg. 1994;81:525-530. [Medline] [Order article via Infotrieve]
-
Longstreth WT, Nelson LM, Koepsell TD, van Belle
G. Subarachnoid hemorrhage and hormonal factors
in women: a population-based case-control study. Ann
Intern Med. 1994;121:168-173.
[Abstract/Free Full Text] - Stegmayr B, Asplund K. Measuring stroke in the population: quality of routine statistics in comparison with a population-based stroke registry. Neuroepidemiology. 1992;11:204-213. [Medline] [Order article via Infotrieve]
-
Sarti C, Tuomilehto J, Salomaa V, Sivenius J, Kaarsalo
E, Narva EV, Salmi K, Torppa J.
Epidemiology of subarachnoid
hemorrhage in Finland from 1983 to 1985.
Stroke. 1991;22:848-853.
[Abstract/Free Full Text] - Broderick JP. Stroke trends in Rochester, Minnesota, during 1945 to 1984. Ann Epidemiol. 1993;3:476-479. [Medline] [Order article via Infotrieve]
-
Herman B, Leyten AC, van Luijk JH, Frenken C, Op de
Coul A, Schulte B. Epidemiology of
stroke in Tilburg, The Netherlands: the population-based Stroke
Incidence Register, II: incidence, initial clinical picture and medical
care, and three-week case fatality. Stroke. 1982;13:629-634.
[Abstract/Free Full Text] -
Bonita R, Thompson S. Subarachnoid
hemorrhage: epidemiology, diagnosis,
management, and outcome. Stroke. 1985;16:591-594.
[Abstract/Free Full Text] -
Phillips LH, Whisnant JP, O'Fallon WM, Sundt
TM. The unchanging pattern of subarachnoid
hemorrhage in a community. Neurology. 1980;30:1034-1040.
[Abstract/Free Full Text] -
Bonita R, Beaglehole R, North JDK.
Subarachnoid hemorrhage in New Zealand: an
epidemiological study. Stroke. 1983;14:342-347.
[Abstract/Free Full Text] - Greenfield L. Without universal coverage, health care use data do not provide population health. Milbank Q. 1996;74:33-36.[Medline] [Order article via Infotrieve]
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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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 D. Gaist, M. Væth, I. Tsiropoulos, K. Christensen, E. Corder, J. Olsen, and H. T. Sørensen Risk of subarachnoid haemorrhage in first degree relatives of patients with subarachnoid haemorrhage: follow up study based on national registries in Denmark BMJ, January 15, 2000; 320(7228): 141 - 145. [Abstract] [Full Text]
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W. D. Rosamond, A. R. Folsom, L. E. Chambless, C.-H. Wang, P. G. McGovern, G. Howard, L. S. Copper, and E. Shahar Stroke Incidence and Survival Among Middle-Aged Adults : 9-Year Follow-Up of the Atherosclerosis Risk in Communities (ARIC) Cohort Stroke, April 1, 1999; 30(4): 736 - 743. [Abstract] [Full Text] [PDF]
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