(Stroke. 1996;27:544-549.)
© 1996 American Heart Association, Inc.
Articles |
Risk Factors for Subarachnoid Hemorrhage
A Systematic Review
From the University Department of Neurology, Utrecht, Netherlands.
Correspondence to Laurien L. Teunissen, MD, University Department of Neurology, Heidelberglaan 100, 3584 CX Utrecht, Netherlands.
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Abstract |
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 Top Abstract IntroductionMethods Results Discussion References |
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Background and Purpose Knowledge of modifiable risk factors for subarachnoid hemorrhage (SAH) is important in terms of prevention. We therefore conducted a systematic review of studies on risk factors for SAH, with emphasis on sufficiently precise criteria for the diagnosis of SAH.
Methods To identify studies we performed a Medline search from 1966 to 1994 and searched the reference lists of all relevant publications. Studies were included only if they fulfilled predefined methodological criteria. Case-control studies were included if the diagnosis of SAH was proved by CT, angiography, or autopsy in at least 70% of patients. Longitudinal studies were included if the criteria for SAH were based on a review of the medical records.
Results Nine longitudinal studies and 11 case-control studies were included. Significant risk factors were as follows: (1) smoking (relative risk [RR] for longitudinal studies, 1.9; 95% confidence interval [CI], 1.5 to 2.3; odds ratio [OR] for case-control studies, 3.5; 95% CI, 2.9 to 4.3); (2) hypertension (RR, 2.8; 95% CI, 2.1 to 3.6; OR, 2.9; 95% CI, 2.4 to 3.7) and (3) drinking 150 g or more of alcohol per week (RR, 4.7; 95% CI, 2.1 to 10.5; OR, 1.5; 95% CI, 1.1 to 1.9). Use of oral contraceptives, hormone replacement therapy, hypercholesterolemia, and physical activity were not significantly related to the risk of SAH.
Conclusions We conclude that smoking, hypertension, and alcohol abuse are important risk factors for SAH. Reduction of exposure to these risk factors might result in a decreased incidence of SAH.
Key Words: gender • meta-analysis • risk factors • subarachnoid hemorrhage
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Introduction |
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TopAbstractIntroductionMethods Results Discussion References |
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In population-based studies, the case-fatality rate of SAH is still 40% to 50%1 2 3 despite continuing improvements in the management of patients with SAH.4 5 The predominant cause of death after SAH is the initial impact of the hemorrhage.2 Major improvement in terms of SAH can therefore be achieved only by reducing the incidence of aneurysmal rupture. To achieve primary prevention, knowledge of modifiable risk factors for SAH is pivotal. In a recently published set of guidelines for SAH, only smoking was accepted as a risk factor; the data on hypertension and oral contraceptives were considered inconsistent.6
Many studies on risk factors for SAH suffer from small numbers of patients and loose diagnostic criteria; in the majority of longitudinal studies, the diagnosis of SAH is not verified at all. Lack of verification of the diagnosis SAH may result in inclusion of many patients with intracerebral hemorrhage, since intracerebral hemorrhage occurs twice as often as SAH,7 and distinction between these two types of hemorrhage without CT scanning is erroneous in approximately 20% of patients.8 Since SAH and intracerebral hemorrhage may have different risk factors, series with a substantial proportion of patients in whom the diagnosis is not confirmed by CT, angiography, or autopsy may provide inaccurate data.
We therefore conducted a systematic review of all studies on risk factors for SAH to identify robust risk factors for SAH. We emphasized the use of sufficiently precise criteria for the diagnosis of SAH.
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Methods |
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TopAbstractIntroductionMethods Results Discussion References |
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To identify studies on risk factors for SAH, we performed a Medline search from 1966 through 1994. We also searched the reference lists of all relevant publications for additional studies on risk factors for SAH. In case of multiple publications on the same study population and risk factor, we used the most recent publication. To assess eligibility of the studies, two authors (L.L.T. and G.J.E.R.) independently assessed the studies according to a set of predefined criteria. In case of disagreement, the data were reviewed by the other authors. Inclusion criteria were as follows: (1) SAH had to be recognized and analyzed as a separate stroke entity and not be included in a hemorrhagic stroke group; (2) studies had to present crude data that could be recalculated in the analysis; (3) case and control subjects had to be comparable, without additional criteria for control subjects; and (4) for case-control studies the diagnosis of SAH had to be confirmed in more than 70% of the cases by the presence of subarachnoid blood on CT or by demonstration of an aneurysm during angiography or autopsy. For the longitudinal studies the diagnosis had to be based on a review of the medical records and not only on ICD codes. Case-control studies were distinguished in population-based and hospital-based studies.
We found data on the following risk factors: alcohol, smoking,
hypertension, hypercholesterolemia, physical
activity, oral contraceptives, and hormone replacement therapy. To
allow comparison of data from different studies, we recategorized some
of the risk factors. Alcohol consumption was recalculated in grams per
week. We divided alcohol use into three groups as follows: (1) no
alcohol consumption; (2) <150 g/wk; and (3) 
150 g/wk. One average
drink contains 12 g of alcohol. No alcohol consumption was taken as
reference in the comparison with the other two categories. For smoking,
case and control subjects were divided into three groups: (1) never
smokers; 2) former smokers; and (3) current smokers. Since not all
studies distinguished between never smokers and former smokers, we
performed a separate analysis with a dichotomy into (1) current
smokers and (2) previous smokers or nonsmokers. For hypertension and
hypercholesterolemia, case and control subjects
were divided according to the criteria used in the separate studies.
Insufficient data on type or dosage were available to recategorize oral
contraceptives and hormone replacement therapy. Case and control
subjects were divided in three groups: (1) never, (2) former, and (3)
current users. Since not all studies distinguished between never users
and former users, we performed a separate analysis with a
dichotomy into (1) current users and (2) never and former users.
Regional Differences
Since the incidence of SAH in Finland is
higher than anywhere
else,9 risk factors for SAH might also be different in
Finland. We therefore performed a separate analysis after
exclusion of all three Finnish
studies.10 11 12 These Finnish
case-control studies addressed
smoking,10 11 12
hypertension,11 12 and alcohol12 as risk
factors.
Data Analysis
RR and OR estimates from individual studies
were combined with
the Mantel-Haenszel method into combined estimates. For
case-control studies, population-based studies were considered
separately and in combination with hospital-based studies.
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Results |
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TopAbstractIntroductionMethods Results Discussion References |
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We included in the analyses 9 longitudinal studies11 13 14 15 16 17 18 19 20 and 11 case-control studies, of which 7 were population based10 21 22 23 24 25 26 and 4 hospital based.12 27 28 29 Details on the studies are given in Tables 1
and 2.
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Analysis of Studies
Smoking
Smoking was
assessed in 2 longitudinal studies,11 14
4 population-based case-control
studies,10 23 24 25 26
and 3 hospital-based case-control
studies.12 27 28
The risk of SAH for current smoking was increased in both the
longitudinal studies (RR, 1.9; 95% CI, 1.5 to 2.3), and the
case-control studies (OR, 3.5; 95% CI, 2.9 to 4.3). Ever smoking
also elevated the risk of SAH in the case-control studies (OR, 3.2;
95% CI, 2.5 to 4.1).12 23 27
(Figure).
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Hypertension
Hypertension
was assessed in 3 longitudinal
studies,11 16 18 4 population-based
case-control
studies,22 24 25 26 and 3
hospital-based case-control
studies.12 27 28 Hypertension
significantly increased the
risk of SAH in the longitudinal studies (RR, 2.8; 95% CI, 2.1 to 3.6)
as well as the case-control studies (OR, 2.9; 95% CI, 2.4 to 3.7)
(Figure
).
Alcohol
Risk implications
of alcohol intake were assessed in 2
longitudinal studies,19 20 1 population-based
case-control study,23 and 2 hospital-based
case-control studies.12 29 In the longitudinal
studies
the RR of SAH for drinking <150 g/wk was 2.8 (95% CI, 1.3 to 6.3),
and that for drinking 150 g/wk was 4.7 (95% CI, 2.1 to 10.5). In the
case-control studies, the OR for drinking 150 g/wk was 1.5 (95%
CI, 1.1 to 1.9), and that for drinking <150 g/wk was 0.8 (95% CI, 0.6
to 1.0) (Figure).
Oral Contraceptives
Use of oral contraceptives was assessed in 1 longitudinal
study17 and 5 case-control studies, all population
based.21 22 24 25 26
In the longitudinal study, based on only
eight cases, the risk for ever use of oral contraception was
inconclusive (RR, 5.4; 95% CI, 0.7 to 43.5). In the case-control
studies, the risks were not elevated for either current use (OR, 1.2;
95% CI, 0.8 to 1.9) or ever use (OR, 1.0; 95% CI, 0.8 to 1.3)
(Figure).
Hormone Replacement Therapy
In the single longitudinal study that addressed hormone
replacement as a risk factor for SAH,15 the risk was not
altered for either current use (RR, 0.6; 95% CI, 0.2 to 1.5) or ever
use (RR, 1.0; 95% CI, 0.5 to 1.9). In one small population-based
case-control study, the risks for current use (OR, 0.5; 95% CI,
0.2 to 1.0) and ever use (OR, 0.5; 95% CI, 0.3 to 1.0) tended to be
lower.22 (Figure).
Cholesterol
In 2 longitudinal studies16 18 and 1
hospital-based case-control study,28
hypercholesterolemia was studied as a possible
risk factor for SAH. Hypercholesterolemia did
not alter the risk of SAH in either the longitudinal studies (RR, 0.9;
95% CI, 0.4 to 1.9) or the case-control study (OR, 0.9; 95% CI,
0.5 to 1.7) (Figure).
Physical Activity
In a longitudinal study with 37 patients,13 physical
activity was almost significant as a protective factor (RR for
activity, 0.5; 95% CI, 0.3 to 1.0), despite a small number of
cases.
Regional Differences
In separate analyses
after exclusion of the Finnish
studies, smoking and hypertension were still significant risk factors
for SAH, but the use of alcohol at 150 g/wk was no longer
significantly associated with SAH.
Sex Differences
In separate analyses, the risks for alcohol use, smoking,
hypertension, and hypercholesterolemia were not
different for men and women (Table 3).
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Discussion |
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TopAbstractIntroductionMethods Results Discussion References |
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In our systematic review, we identified three significant risk factors for SAH in both case-control and longitudinal studies. RRs for smoking and hypertension were homogeneous between studies. An alcohol intake of
150 g/wk was also a significant
although less constant risk factor. The use of smaller amounts of
alcohol seemed to have a protective effect in the case-control
studies, but this effect was not supported by the longitudinal studies.
Our analysis therefore does not support a J-shaped
association between the dose of alcohol and the risk of SAH, as was
found for the association between alcohol and hemorrhagic stroke in
general.30 The results regarding alcohol are of course
influenced by the stratification we used. This restratification
explains why data we extracted from studies differ in some instances
from those in the original publications. For example, a single study
found that alcohol was a risk factor only when >400
g/wk,29 but this finding was not included in our
analysis because our stratification precludes subdivision into
categories of 150 to 400 and >400 g/wk. Also, we did not consider
drinking patterns in our analysis. There is some evidence that
binge drinking might increase the risk of SAH, but these studies did
not meet the predefined criteria and were therefore not
included.31 32 Another explanation for the higher
risk of
alcohol consumption is confounding, since smoking and alcohol use are
often combined and hypertension can be caused by smoking and alcohol
use.33 Since the individual studies did not always provide
information on combinations of risk factors in one patient, it was not
possible to study the effect of confounding in this systematic
review. A remarkable result of this review is the lack of evidence that oral contraceptives and cholesterol are risk factors for SAH. In two studies oral contraceptives were a significant risk factor for SAH,17 26 but the remaining four studies did not support this finding.21 22 24 25 In one of these four studies oral contraceptives even had a significant protective effect.24 The variation between the studies might be explained by different dosages of estrogen, but none of the studies provided information about type of oral contraceptive or amount of estrogen. In the two studies in which oral contraceptives were found to be a risk factor, the periods of follow-up were from 1969 to 1977 and from 1968 to 1987; in these periods the majority of patients used oral contraceptives with high estrogen levels. In all but one of the remaining studies, follow-up included a more recent period during which oral contraceptives with lower estrogen levels were used. The notion that estrogen use is a dose-dependent risk factor for SAH is further supported by the finding that hormone replacement therapy had a protective albeit nonsignificant effect on the risk for SAH.
This review is based on a total of 20 studies. Many other studies were not included in our analysis because they did not meet our predefined criteria. These include, among others, two often-cited Finnish studies on alcohol use and SAH, because they used estimated data of the general population as control.31 32 The well-known Framingham Study did not analyze SAH and intracerebral hemorrhage separately.34 Moreover, we have excluded many case-control studies in which fewer than 70% of the diagnoses of SAH were confirmed by CT, angiography, or autopsy and longitudinal studies in which medical records were not reviewed and diagnosis of SAH was based only on ICD codes. Additionally, many studies were excluded because it was impossible to recalculate the data into RRs. (A list of studies that were considered for this systematic review but did not meet our predefined criteria can be obtained on request from the authors.) For future studies of risk factors for aneurysmal SAH, we recommend CT scanning in as large a proportion of patients as possible and exclusion of patients with perimesencephalic hemorrhage. This benign subset of SAH is characterized by mild symptoms at onset, a typical pattern of hemorrhage on CT, absence of an aneurysm, an uneventful clinical course, and an excellent outcome.35 36 37 The risk factors for this nonaneurysmal type of SAH might be quite different from those for aneurysmal SAH. In the analysis we recommend reporting the RR of each risk factor separately in addition to the results of multivariate analysis. We divided the case-control studies into population-based and hospital-based studies, since hospital-based studies may contain a selected sample of the population with different risk factors. However, the analysis of population-based studies alone did not show important differences compared with the analysis of population-based and hospital-based studies together. The diagnostic criteria in the longitudinal studies were less strict than in the case-control studies. When longitudinal and case-control studies were compared, smoking and hypertension emerged as risk factors in every analysis, but for smoking the observed risk was higher in the case-control studies than in the longitudinal studies. Only two longitudinal studies considered alcohol as a risk factor, and in these studies alcohol was a stronger risk factor than in the case-control studies. Therefore, differences between longitudinal and case-control studies exist only in magnitude and not in the direction of the effect. An explanation for the different results obtained from longitudinal and case-control studies is that in longitudinal studies exposure status may be determined many years before the onset of the SAH, whereas in case-control studies exposures occur closer in time to stroke onset. The difference between longitudinal and case-control studies might also be explained by chance, since only two longitudinal studies considered smoking as a risk factor.
In a separate analysis after exclusion of the three Finnish
studies, alcohol intake of 150 g/wk was no longer a risk factor for
SAH. Although there might be loss of information caused by
stratification with this small number of studies, these data suggest
that alcohol abuse is more important a risk factor for SAH in Finland
than in other countries.
Our analysis of studies in which the diagnosis of SAH was verified in the majority of patients indicates that smoking, hypertension, and to a lesser extent alcohol abuse are significant risk factors for SAH. The decline in incidence of stroke in general, brought about by the reduction in these cardiovascular risk factors,38 39 has not been found for SAH: both a community study as well as a recent compilation disproved a decline in incidence of SAH over the last 30 years.9 40 The apparent lack of reduction in the incidence of SAH despite the reduction of its risk factors can be at least partly explained by the low incidence of SAH. The SAH incidence studies of the last few decades have been based on so few patients that even substantial reductions in incidence may not have been detected. Given an SAH incidence of 6/100 000 person-years,9 a prevalence of hypertension approximating 10%, and an RR of hypertension of 3, the incidence of SAH in patients without hypertension is 5/100 000 person-years and that of patients with hypertension 15/100 000 person-years. This means that hypertension should be effectively treated in 100 000 hypertensive patients to prevent 10 cases of SAH per year. The absence of a decline in SAH incidence might also be related to the presence of nonmodifiable risk factors, such as a familial, probably genetic factor,41 and a sex-related factor. SAH is more common in women, although smoking, hypertension, and alcohol use are more common in men, and the influence of the risk factors is equal in men and women. Since the genetic and sex-related risk factors are thus far unknown, the only method at present to decrease the incidence of SAH is the reduction of the major cardiovascular risk factors.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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We wish to express special thanks to F. Bominaar for her assistance in creating the Figure
and tables. Received October 2, 1995; revision received November 27, 1995; accepted November 27, 1995.
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References |
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TopAbstractIntroductionMethods Results Discussion References |
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1. Longstreth WT Jr, Nelson LM, Koepsell TD, van Belle G. Clinical course of spontaneous subarachnoid hemorrhage: a population-based study in King County, Washington. Neurology. 1993;43:712-718.
2. Broderick JP, Brott TG, Duldner JE, Tomsick T, Leach A. Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke. 1994;25:1342-1347. [Abstract]
3. Anderson CS, Jamrozik KD, Burvill PW, Chakera TMH, Johnson GA, Stewart-Wynne EG. Determining the incidence of different subtypes of stroke: results from the Perth Community Stroke Study, 1989-1990. Med J Aust. 1993;158:85-89. [Medline] [Order article via Infotrieve]
4.
Inagawa T, Tokuda Y, Ohbayashi N, Takaya M, Moritake
K. Study of aneurysmal subarachnoid
hemorrhage in Izumo City, Japan. Stroke. 1995;26:761-766.
5.
Fogelholm R, Hernesniemi J, Vapalahti M. Impact
of early surgery on outcome after aneurysmal
subarachnoid hemorrhage: a population-based
study. Stroke. 1993;24:1649-1654.
6. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Mayberg MR, Batjer HH, Dacey R, Diringer M, Haley C, Heros RC, Sternau LL, Torner J, Adams HP, Feinberg W, Thies W. Stroke. 1994;25:2315-2328. [Medline] [Order article via Infotrieve]
7. Broderick JP, Brott TG, 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]
8. van Gijn J, van Dongen KJ. Computed tomography in the diagnosis of subarachnoid haemorrhage and ruptured aneurysm. Clin Neurol Neurosurg. 1980;82:11-24. [Medline] [Order article via Infotrieve]
9. Linn FHH, Rinkel GJE, Algra A, van Gijn J. The true incidence of subarachnoid hemorrhage: influence of CT scanning and time trends. Neurology. 1995;45(suppl 4):A365. Abstract.
10.
Fogelholm R, Murros K. Cigarette smoking and
subarachnoid haemorrhage: a population-based
case-control study. J Neurol Neurosurg
Psychiatry.. 1987;50:78-80.
11. Knekt P, Reunanen A, Aho K, Heliovaara 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]
12.
Juvela S, Hillbom M, Numminen H, Koskinen P.
Cigarette smoking and alcohol consumption as risk factors for
aneurysmal subarachnoid hemorrhage.
Stroke. 1993;24:639-646.
13.
Abbott RD, Rodriquez BL, Burchfiel CM, Curb JD.
Physical activity in older middle-aged men and reduced risk of
stroke: the Honolulu Heart Program. Am J Epidemiol. 1994;139:881-893.
14.
Kawachi I, Colditz GA, Stampfer MJ, Willett WC, Manson
J, Rosner B, Speizer FE, Hennekens CH. Smoking cessation and
decreased risk of stroke in women. JAMA. 1993;269:232-236.
15. Stampfer MJ, Colditz GA, Willett WC, Manson JE, Rosner B, Speizer FE, Hennekens CH. Postmenopausal estrogen therapy and cardiovascular disease: ten-year follow-up from the Nurses' Health Study. N Engl J Med. 1991;325:756-762. [Abstract]
16. Iso H, Jacobs DR, Wentworth D, Neaton JD, Cohen JD. Serum cholesterol levels and six year mortality from stroke in 350,977 men screened for the Multiple Risk Factor Intervention Trial. N Engl J Med. 1989;320:904-910. [Abstract]
17. Vessey MP, Villard-Mackintosh L, McPherson K, Yeates D. Mortality among oral contraceptive users: 20 year follow up of women in a cohort study. BMJ. 1989;299:1487-1491.
18.
Yano K, Reed DM, Maclean CJ. Serum
cholesterol and hemorrhagic stroke in the Honolulu Heart
Program. Stroke. 1989;20:1460-1465.
19. Stampfer MJ, Colditz GA, Willett WC, Speizer FE, Hennekens CH. 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]
20.
Donahue RP, Abbott RD, Reed DM, Yano K. Alcohol
and hemorrhagic stroke: the Honolulu Heart Program.
JAMA. 1986;255:2311-2314.
21. Hannaford PC, Croft PR, Kay CR. Oral contraception and stroke: evidence from the Royal College of General Practitioners' Oral Contraception Study. Stroke. 1994;25:935-942. [Abstract]
22.
Longstreth WT Jr, 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.
23.
Longstreth WT, Nelson LM, Koepsell TD, van Belle
G. Cigarette smoking, alcohol use, and subarachnoid
hemorrhage. Stroke. 1992;23:1242-1249.
24.
Bonita R. Cigarette smoking, hypertension and
the risk of subarachnoid hemorrhage: a
population-based case-control study. Stroke. 1986;17:831-835.
25. Inman WHW. Oral contraceptives and fatal subarachnoid haemorrhage. Br Med J. 1979;2:1468-1470.
26. Petitti DB, Wingerd J. Use of oral contraceptives, cigarette smoking, and the risk of subarachnoid haemorrhage. Lancet. 1978;2:234-236. [Medline] [Order article via Infotrieve]
27. Adamson J, Humphries SE, Ostergaard JR, Voldby B, Richards P, Powell JT. Are cerebral aneurysms atherosclerotic? Stroke. 1994;25:963-966. [Abstract]
28. Canhão P, Pinto AN, Ferro H, Ferro JM. Smoking and aneurysmal subarachnoid haemorrhage: a case-control study. J Cardiovasc Risk. 1994;1:155-158. [Medline] [Order article via Infotrieve]
29. Gill JS, Shipley MJ, Tsementzis SA, Hornby RS, Gill SK, Hitchcock ER, Beevers DG. Alcohol consumption: a risk factor for hemorrhagic and non-hemorrhagic stroke. Am J Med. 1991;90:489-497. [Medline] [Order article via Infotrieve]
30. Van Gijn J, Stampfer MJ, Wolfe C, Algra A. The association between alcohol and stroke. In: Verschuren PM, ed. Health Issues Related to Alcohol Consumption. Brussels, Belgium: ILSI Press; 1993:43-79.
31.
Hillbom M, Kaste M. Does alcohol intoxication
precipitate aneurysmal subarachnoid
haemorrhage? J Neurol Neurosurg
Psychiatry.. 1981;44:523-526.
32.
Hillbom M, Kaste M. Alcohol intoxication: a risk
factor for primary subarachnoid hemorrhage.
Neurology.. 1982;32:706-711.
33. Keil U, Swales JD, Grobbee DE. Alcohol intake and its relation to hypertension. In: Verschuren PM, ed. Health Issues Related to Alcohol Consumption. Brussels, Belgium: ILSI Press; 1993:17-42.
34. Kannel WB, D'Agostino RB, Belanger AJ. Fibrinogen, cigarette smoking and risk of cardiovascular disease: insights from the Framingham Study. Am Heart J. 1987;113:1006-1010. [Medline] [Order article via Infotrieve]
35. Rinkel GJE, Wijdicks EFM, Vermeulen M, Hasan D, Brouwers PJAM, van Gijn J. The clinical course of perimesencephalic nonaneurysmal subarachnoid hemorrhage. Ann Neurol. 1991;29:463-468. [Medline] [Order article via Infotrieve]
36. Rinkel GJE, Wijdicks EFM, Vermeulen M, Ramos LMP, Tanghe HLJ, Hasan D, Meiners LC, van Gijn J. Nonaneurysmal perimesencephalic subarachnoid hemorrhage: CT and MR patterns that differ from aneurysmal rupture. AJNR Am J Neuroradiol.. 1991;12:829-834. AJR Am J Roentgenol. 1991;157:1325-1330. [Abstract]
37. Rinkel GJE, Wijdicks EFM, Hasan D, Kienstra G, Hageman L, Franke C, Vermeulen M, van Gijn J. Outcome in patients with subarachnoid hemorrhage and a negative angiography according to pattern of haemorrhage on computed tomography. Lancet. 1991;338:964-968. [Medline] [Order article via Infotrieve]
38. Sytkowski PA, Kannel WB, D'Agostino RB. Changes in risk factors and the decline in mortality from cardiovascular disease: the Framingham Heart Study. N Engl J Med. 1990;322:1635-1641. [Abstract]
39.
Vartiainen E, Sarti C, Tuomilehto J, Kuulasmaa
K. Do changes in cardiovascular risk factors
explain changes in mortality from stroke in Finland?
BMJ. 1995;310:901-904.
40.
Ingall TJ, Whisnant JP, Wiebers DO, O'Fallon
WM. Has there been a decline in subarachnoid
hemorrhage mortality? Stroke. 1989;20:718-724.
41.
Bromberg JEC, Rinkel GJE, Algra A, Greebe P, van Duyn
CM, Hasan D, Limburg M, ter Berg HWM, Wijdicks EFM, van Gijn J.
Subarachnoid hemorrhage in first and second degree
relatives. BMJ. 1995;311:288-289.
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Y. Wakugawa, Y. Kiyohara, Y. Tanizaki, M. Kubo, T. Ninomiya, J. Hata, Y. Doi, K. Okubo, Y. Oishi, K. Shikata, et al. C-Reactive Protein and Risk of First-Ever Ischemic and Hemorrhagic Stroke in a General Japanese Population: The Hisayama Study Stroke, January 1, 2006; 37(1): 27 - 32. [Abstract] [Full Text] [PDF]
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V. L. Feigin, G. J.E. Rinkel, C. M.M. Lawes, A. Algra, D. A. Bennett, J. van Gijn, and C. S. Anderson Risk Factors for Subarachnoid Hemorrhage: An Updated Systematic Review of Epidemiological Studies Stroke, December 1, 2005; 36(12): 2773 - 2780. [Abstract] [Full Text] [PDF]
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J. N. Struijs, M. L.L. van Genugten, S. M.A.A. Evers, A. J.H.A. Ament, C. A. Baan, and G. A.M. van den Bos Modeling the Future Burden of Stroke in the Netherlands: Impact of Aging, Smoking, and Hypertension Stroke, August 1, 2005; 36(8): 1648 - 1655. [Abstract] [Full Text] [PDF]
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 H. C. Kim, C. M. Nam, S. H. Jee, and I. Suh Comparison of Blood Pressure-Associated Risk of Intracerebral Hemorrhage and Subarachnoid Hemorrhage: Korea Medical Insurance Corporation Study Hypertension, August 1, 2005; 46(2): 393 - 397. [Abstract] [Full Text] [PDF]
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V. Feigin, V. Parag, C. M. M. Lawes, A. Rodgers, I. Suh, M. Woodward, K. Jamrozik, H. Ueshima, and on behalf of the Asia Pacific Cohort Studies Colla Smoking and Elevated Blood Pressure Are the Most Important Risk Factors for Subarachnoid Hemorrhage in the Asia-Pacific Region: An Overview of 26 Cohorts Involving 306 620 Participants Stroke, July 1, 2005; 36(7): 1360 - 1365. [Abstract] [Full Text] [PDF]
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A. Slowik, A. Borratynska, W. Turaj, J. Pera, T. Dziedzic, D. A. Figlewicz, M. Betlej, T. Krzyszkowski, R. Czepko, and A. Szczudlik {alpha}1-Antichymotrypsin Gene (SERPINA3) A/T Polymorphism as a Risk Factor for Aneurysmal Subarachnoid Hemorrhage Stroke, April 1, 2005; 36(4): 737 - 740. [Abstract] [Full Text] [PDF]
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 Y M Ruigrok, G J E Rinkel, C Wijmenga, and J van Gijn Anticipation and phenotype in familial intracranial aneurysms J. Neurol. Neurosurg. Psychiatry, October 1, 2004; 75(10): 1436 - 1442. [Abstract] [Full Text] [PDF]
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Y.B.W.E.M. Roos, G. Pals, P.M. Struycken, G.J.E. Rinkel, M. Limburg, J.C. Pronk, J.S.P. van den Berg, J.A.F.M. Luijten, P.L. Pearson, M. Vermeulen, et al. Genome-Wide Linkage in a Large Dutch Consanguineous Family Maps a Locus for Intracranial Aneurysms to Chromosome 2p13 Stroke, October 1, 2004; 35(10): 2276 - 2281. [Abstract] [Full Text] [PDF]
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B. Stegmayr, M. Eriksson, and K. Asplund Declining Mortality From Subarachnoid Hemorrhage: Changes in Incidence and Case Fatality From 1985 Through 2000 Stroke, September 1, 2004; 35(9): 2059 - 2063. [Abstract] [Full Text] [PDF]
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T. Mannami, H. Iso, S. Baba, S. Sasaki, K. Okada, M. Konishi, S. Tsugane, and for the Japan Public Health Center-Based Prospecti Cigarette Smoking and Risk of Stroke and its Subtypes Among Middle-Aged Japanese Men and Women: The JPHC Study Cohort I Stroke, June 1, 2004; 35(6): 1248 - 1253. [Abstract] [Full Text] [PDF]
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 Y.M. Ruigrok, G.J.E. Rinkel, A. Algra, T.W.M. Raaymakers, and J. van Gijn Characteristics of intracranial aneurysms in patients with familial subarachnoid hemorrhage Neurology, March 23, 2004; 62(6): 891 - 894. [Abstract] [Full Text] [PDF]
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C. S. Anderson, V. Feigin, D. Bennett, R.-B. Lin, G. Hankey, K. Jamrozik, and for the Australasian Cooperative Research on Subar Active and Passive Smoking and the Risk of Subarachnoid Hemorrhage: An International Population-Based Case-Control Study Stroke, March 1, 2004; 35(3): 633 - 637. [Abstract] [Full Text] [PDF]
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R. L. Macdonald Advances in Vascular Surgery Stroke, February 1, 2004; 35(2): 375 - 380. [Full Text] [PDF]
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D. Gaist, L. Pedersen, S. Cnattingius, and H. T. Sorensen Parity and Risk of Subarachnoid Hemorrhage in Women: A Nested Case-Control Study Based on National Swedish Registries Stroke, January 1, 2004; 35(1): 28 - 32. [Abstract] [Full Text] [PDF]
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D. Krex, H. Rohl, I. R. Konig, A. Ziegler, H. K. Schackert, and G. Schackert Tissue Inhibitor of Metalloproteinases-1, -2, and -3 Polymorphisms in a White Population With Intracranial Aneurysms Stroke, December 1, 2003; 34(12): 2817 - 2821. [Abstract] [Full Text] [PDF]
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S. Yamada, A. Koizumi, H. Iso, Y. Wada, Y. Watanabe, C. Date, A. Yamamoto, S. Kikuchi, Y. Inaba, H. Toyoshima, et al. Risk Factors for Fatal Subarachnoid Hemorrhage: The Japan Collaborative Cohort Study Stroke, December 1, 2003; 34(12): 2781 - 2787. [Abstract] [Full Text] [PDF]
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S. Juvela Prehemorrhage Risk Factors for Fatal Intracranial Aneurysm Rupture Stroke, August 1, 2003; 34(8): 1852 - 1857. [Abstract] [Full Text] [PDF]
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C. Anderson, C. Ni Mhurchu, D. Scott, D. Bennett, K. Jamrozik, and G. Hankey Triggers of Subarachnoid Hemorrhage: Role of Physical Exertion, Smoking, and Alcohol in the Australasian Cooperative Research on Subarachnoid Hemorrhage Study (ACROSS) Stroke, July 1, 2003; 34(7): 1771 - 1776. [Abstract] [Full Text] [PDF]
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 T. Vogel, R. Verreault, J.-F. Turcotte, M. Kiesmann, and M. Berthel Review Article. Intracerebral Aneurysms: A Review With Special Attention to Geriatric Aspects J. Gerontol. A Biol. Sci. Med. Sci., June 1, 2003; 58(6): M520 - 524. [Abstract] [Full Text] [PDF]
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T. Kurth, C. S. Kase, K. Berger, E. S. Schaeffner, J. E. Buring, and J. M. Gaziano Smoking and the Risk of Hemorrhagic Stroke in Men Stroke, May 1, 2003; 34(5): 1151 - 1155. [Abstract] [Full Text] [PDF]
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K. Okamoto, R. Horisawa, T. Kawamura, A. Asai, M. Ogino, T. Takagi, and Y. Ohno Family History and Risk of Subarachnoid Hemorrhage: A Case-Control Study in Nagoya, Japan Stroke, February 1, 2003; 34(2): 422 - 426. [Abstract] [Full Text] [PDF]
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H. Ohkuma, H. Tabata, S. Suzuki, and M. S. Islam Risk Factors for Aneurysmal Subarachnoid Hemorrhage in Aomori, Japan Stroke, January 1, 2003; 34(1): 96 - 100. [Abstract] [Full Text] [PDF]
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W T Longstreth Jr Coffee and subarachnoid haemorrhage J. Neurol. Neurosurg. Psychiatry, August 1, 2002; 73(2): 112 - 112. [Full Text]
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J Isaksen, A Egge, K Waterloo, B Romner, and T Ingebrigtsen Risk factors for aneurysmal subarachnoid haemorrhage: the Tromso study J. Neurol. Neurosurg. Psychiatry, August 1, 2002; 73(2): 185 - 187. [Abstract] [Full Text] [PDF]
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B. M. Kissela, L. Sauerbeck, D. Woo, J. Khoury, J. Carrozzella, A. Pancioli, E. Jauch, C. J. Moomaw, R. Shukla, J. Gebel, et al. Subarachnoid Hemorrhage: A Preventable Disease With a Heritable Component Stroke, May 1, 2002; 33(5): 1321 - 1326. [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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K. Okamoto, R. Horisawa, T. Kawamura, A. Asai, M. Ogino, T. Takagi, and Y. Ohno Menstrual and Reproductive Factors for Subarachnoid Hemorrhage Risk in Women: A Case-Control Study in Nagoya, Japan Stroke, December 1, 2001; 32(12): 2841 - 2844. [Abstract] [Full Text] [PDF]
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B. Zhang, S. Dhillon, I. Geary, W. M. Howell, F. Iannotti, I. N.M. Day, and S. Ye Polymorphisms in Matrix Metalloproteinase-1, -3, -9, and -12 Genes in Relation to Subarachnoid Hemorrhage Stroke, September 1, 2001; 32(9): 2198 - 2202. [Abstract] [Full Text] [PDF]
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T. Inagawa Trends in Incidence and Case Fatality Rates of Aneurysmal Subarachnoid Hemorrhage in Izumo City, Japan, Between 1980-1989 and 1990-1998 Stroke, July 1, 2001; 32(7): 1499 - 1507. [Abstract] [Full Text] [PDF]
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Y. M. Ruigrok, E. Buskens, and G. J. E. Rinkel Attributable Risk of Common and Rare Determinants of Subarachnoid Hemorrhage Stroke, May 1, 2001; 32(5): 1173 - 1175. [Abstract] [Full Text] [PDF]
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C. N. Mhurchu, C. Anderson, K. Jamrozik, G. Hankey, D. Dunbabin, W.T. Longstreth Jr, and L. M. Nelson Hormonal Factors and Risk of Aneurysmal Subarachnoid Hemorrhage : An International Population-Based, Case-Control Study Editorial Comment : The Gender Gap in Aneurysmal Subarachnoid Hemorrhage Stroke, March 1, 2001; 32(3): 606 - 612. [Abstract] [Full Text] [PDF]
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 P Sharma and M J Brown Neurovascular lessons from a pair of identical twins with cerebral aneurysms Postgrad. Med. J., March 1, 2001; 77(905): 197 - 198. [Abstract] [Full Text]
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 J. van Gijn and G. J. E. Rinkel Subarachnoid haemorrhage: diagnosis, causes and management Brain, February 1, 2001; 124(2): 249 - 278. [Abstract] [Full Text] [PDF]
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 C. G. Sobey Potassium Channel Function in Vascular Disease Arterioscler Thromb Vasc Biol, January 1, 2001; 21(1): 28 - 38. [Abstract] [Full Text] [PDF]
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J. B. Bederson, I. A. Awad, D. O. Wiebers, D. Piepgras, E. C. Haley Jr, T. Brott, G. Hademenos, D. Chyatte, R. Rosenwasser, and C. Caroselli Recommendations for the Management of Patients With Unruptured Intracranial Aneurysms : A Statement for Healthcare Professionals From the Stroke Council of the American Heart Association Stroke, November 1, 2000; 31(11): 2742 - 2750. [Full Text] [PDF]
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 |
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 J. B. Bederson, I. A. Awad, D. O. Wiebers, D. Piepgras, E. C. Haley Jr, T. Brott, G. Hademenos, D. Chyatte, R. Rosenwasser, and C. Caroselli Recommendations for the Management of Patients With Unruptured Intracranial Aneurysms : A Statement for Healthcare Professionals From the Stroke Council of the American Heart Association Circulation, October 31, 2000; 102(18): 2300 - 2308. [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. Mira, J. Aznar, A. Estelles, A. Vaya, P. Villa, and F. Ferrando State-of-the-Art Review : Congenital and Acquired Thrombotic Risk Factors in Women Using Oral Contraceptives: Clinical Aspects Clinical and Applied Thrombosis/Hemostasis, July 1, 2000; 6(3): 162 - 168. [Abstract] [PDF]
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J. M. Wardlaw and P. M. White The detection and management of unruptured intracranial aneurysms Brain, February 1, 2000; 123(2): 205 - 221. [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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J. M. Leppala, J. Virtamo, R. Fogelholm, D. Albanes, and O. P. Heinonen Different Risk Factors for Different Stroke Subtypes : Association of Blood Pressure, Cholesterol, and Antioxidants Stroke, December 1, 1999; 30(12): 2535 - 2540. [Abstract] [Full Text] [PDF]
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T. W. M. Raaymakers Aneurysms in relatives of patients with subarachnoid hemorrhage: Frequency and risk factors Neurology, September 1, 1999; 53(5): 982 - 982. [Abstract] [Full Text]
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J. S. P. van den Berg, G. Pals, F. Arwert, R. C. M. Hennekam, K. W. Albrecht, A. Westerveld, and M. Limburg Type III Collagen Deficiency in Saccular Intracranial Aneurysms : Defect in Gene Regulation? Stroke, August 1, 1999; 30(8): 1628 - 1631. [Abstract] [Full Text] [PDF]
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K. R. Evenson, W. D. Rosamond, J. Cai, J. F. Toole, R. G. Hutchinson, E. Shahar, and A. R. Folsom Physical Activity and Ischemic Stroke Risk : The Atherosclerosis Risk in Communities Study Stroke, July 1, 1999; 30(7): 1333 - 1339. [Abstract] [Full Text] [PDF]
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T. Uehara, M. Tabuchi, and E. Mori High frequency of unruptured intracranial aneurysms in female patients with ischaemic heart disease J. Neurol. Neurosurg. Psychiatry, April 1, 1998; 64(4): 536 - 538. [Abstract] [Full Text] [PDF]
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G. J. E. Rinkel, M. Djibuti, A. Algra, and J. van Gijn Prevalence and Risk of Rupture of Intracranial Aneurysms : A Systematic Review Stroke, January 1, 1998; 29(1): 251 - 256. [Abstract] [Full Text] [PDF]
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T. Ostbye, A. R. Levy, and N. E. Mayo Hospitalization and Case-Fatality Rates for Subarachnoid Hemorrhage in Canada From 1982 Through 1991 : The Canadian Collaborative Study Group of Stroke Hospitalizations Stroke, April 1, 1997; 28(4): 793 - 798. [Abstract] [Full Text]
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C. G. Sobey, D. D. Heistad, F. M. Faraci, and D. R. Harder Effect of Subarachnoid Hemorrhage on Cerebral Vasodilatation in Response to Activation of ATP-Sensitive K+ Channels in Chronically Hypertensive Rats Stroke, February 1, 1997; 28(2): 392 - 397. [Abstract] [Full Text]
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G. J.E. Rinkel, N. E.M. Prins, and A. Algra Outcome of Aneurysmal Subarachnoid Hemorrhage in Patients on Anticoagulant Treatment Stroke, January 1, 1997; 28(1): 6 - 9. [Abstract] [Full Text]
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F.H.H. Linn, G.J.E. Rinkel, A. Algra, and J. van Gijn Incidence of Subarachnoid Hemorrhage : Role of Region, Year, and Rate of Computed Tomography: A Meta-Analysis Stroke, April 1, 1996; 27(4): 625 - 629. [Abstract] [Full Text]
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