Skip main navigation

Risk Factors for Subarachnoid Hemorrhage

An Updated Systematic Review of Epidemiological Studies
Originally publishedhttps://doi.org/10.1161/01.STR.0000190838.02954.e8Stroke. 2005;36:2773–2780

Abstract

Background and Purpose— After a 1996 review from our group on risk factors for subarachnoid hemorrhage (SAH), much new information has become available. This article provides an updated overview of risk factors for SAH.

Methods— An overview of all longitudinal and case-control studies of risk factors for SAH published in English from 1966 through March 2005. We calculated pooled relative risks (RRs) for longitudinal studies and odds ratios (ORs) for case-control studies, both with corresponding 95% CIs.

Results— We included 14 longitudinal (5 new) and 23 (12 new) case-control studies. Overall, the studies included 3936 patients with SAH (892 cases in 14 longitudinal studies and 3044 cases in 23 case-control studies) for analysis. Statistically significant risk factors in longitudinal and case-control studies were current smoking (RR, 2.2 [1.3 to 3.6]; OR, 3.1 [2.7 to 3.5]), hypertension (RR, 2.5 [2.0 to 3.1]; OR, 2.6 [2.0 to 3.1]), and excessive alcohol intake (RR, 2.1 [1.5 to 2.8]; OR, 1.5 [1.3 to 1.8]). Nonwhite ethnicity was a less robust risk factor (RR, 1.8 [0.8 to 4.2]; OR, 3.4 [1.0 to 11.9]). Oral contraceptives did not affect the risk (RR, 5.4 [0.7 to 43.5]; OR, 0.8 [0.5 to 1.3]). Risk reductions were found for hormone replacement therapy (RR, 0.6 [0.2 to 1.5]; OR, 0.6 [0.4 to 0.8]), hypercholesterolemia (RR, 0.8 [0.6 to 1.2]; OR, 0.6 [0.4 to 0.9]), and diabetes (RR, 0.3 [0 to 2.2]; OR, 0.7 [0.5 to 0.8]). Data were inconsistent for lean body mass index (RR, 0.3 [0.2 to 0.4]; OR, 1.4 [1.0 to 2.0]) and rigorous exercise (RR, 0.5 [0.3 to 1.0]; OR, 1.2 [1.0 to 1.6]). In the studies included in the review, no other risk factors were available for the meta-analysis.

Conclusions— Smoking, hypertension, and excessive alcohol remain the most important risk factors for SAH. The seemingly protective effects of white ethnicity compared to nonwhite ethnicity, hormone replacement therapy, hypercholesterolemia, and diabetes in the etiology of SAH are uncertain.

Subarachnoid hemorrhage (SAH) comprises 1% to 7% of all strokes.1 Despite its relative rarity, the loss of productive life years in the general population from SAH is comparable to that of cerebral infarction, the most common stroke subtype.2 The main reasons for the huge impact of SAH are the relatively young age of onset and poor outcome.1,3,4 Although familial preponderance suggests a genetic influence, most instances of SAH can be attributed to lifestyle exposures.5 Hence, identification of modifiable risk factors for SAH is pivotal to reducing its incidence, which appears to have remained relatively stable in many countries6 over recent decades.3,7,8

Many etiological studies of SAH were based on small numbers and variable diagnostic criteria, and evaluations of only a single risk factor, often in a particular subgroup of patients, such as those admitted to hospitals. In this context, a systematic review of all published data can provide more reliable information on the relative importance of particular exposures. Ten years ago, we performed such a review,9 but the subsequent additional published epidemiological studies of SAH, including some previously unaddressed risk factors, have necessitated us to update these analyses.

Methods

Methods of literature search, inclusion criteria for studies, and diagnostic criteria for SAH were the same as that in the previous overview.9 In brief, the following key words or subject headings were used for the MEDLINE search from 1966 through March 2005: subarachnoid h(a)emorrhage, h(a)emorrhagic stroke(s), case-control, longitudinal, cohort, prospective, and risk factors. Bibliographies of retrieved articles were examined for further relevant publications. This method of cross-checking was continued until no further publications were found. Only studies published in English that reported crude data on risk factors for SAH were included in the meta-analysis. Crude data referred to the actual numbers of exposed and nonexposed subjects reported in the publication that allowed recalculation of the risk associated with the exposure. Studies confined to a particular subgroup of patients (eg, young subjects [except for studies of oral contraceptives] and familial ruptured aneurysms) were not included in the meta-analysis. Hospital-based and population-based case-control studies were analyzed separately and combined. For the longitudinal studies, the diagnosis had to be based on a review of the medical records and not only on International Classification of Diseases codes. For the case-control studies, SAH had to be confirmed in >70% of the cases by characteristic computed tomography, angiography, or autopsy findings. To assess eligibility of the studies and extract data for the meta-analysis, 3 authors (V.L.F., C.M.M.L., and G.J.E.R.) independently assessed the studies and cross-checked the data extracted. In case of disagreement, this was resolved by discussion between the reviewers. In case of multiple publications from 1 center, relevant data from most recent publication were extracted and included in the analysis. We also recorded whether the investigators had adjusted for major confounders in the original publication.

To allow comparison of data from different studies, risk factors were standardized across studies whenever possible. Alcohol consumption was categorized in 3 groups: (1) no alcohol consumption; (2) consumption of <150 g per week; and (3) consumption of ≥150 g per week. We assumed that 1 standard drink contains 12 g of ethanol. No alcohol consumption was taken as reference in the comparison with the other 2 categories. For smoking, case and control subjects were divided into never smokers, former smokers, current smokers, former/never smokers, and ever smokers (current and former smokers combined) depending on availability of the data. In addition to the list of risk factors analyzed in the previous overview,9 for this study, we also included data on body mass index (BMI), diabetes mellitus, and ethnicity. Lean BMI was defined as BMI <22 (BMI of ≥22 was used as the reference category). Ethnicity was dichotomized into white and nonwhite, and for hypertension (present versus absent), physical activity level (regular rigorous exercise versus no regular rigorous exercise), serum cholesterol level (hypercholesterolemia versus normal), and diabetes (present versus absent). For hormone replacement therapy and oral contraceptives, current users were compared with never and former users combined (if only ever users were reported in the original publication, they were compared with never users). For all risk factor categories, we accepted criteria from original publications. No individual data from the parent articles were available for analyses of data according to predefined criteria.

For longitudinal studies, pooled relative risk (RR) estimates were calculated by means of the inverse-variance weighting method.10 For case-control studies, odds ratio (OR) estimates were combined with the Mantel–Haenszel method into pooled estimates. For studies reporting risk factors separately for men and women, overall and gender-specific estimates were calculated, and additional stratified analyses by sex were performed whenever possible. If no evidence for statistical heterogeneity was observed for the Cochrane Q statistic (P<0.10), fixed-effect models were used; otherwise, we used random-effect models.11

Results

Based on the selection criteria, 5 longitudinal and 12 case-control studies published after the previous overview met our inclusion criteria (Figure 1). These were included in the meta-analysis in addition to the 9 longitudinal and 11 case-control studies included in the previous review9 (Tables 1 and 2). Most longitudinal studies were initiated in the 1970s and were restricted to the US, Japanese, UK, Korean, and Finnish populations. Of the 23 case-control studies, 10 (63% of SAH cases)12–21 were population based and 13 hospital based,22–34 covering a variety of populations: American (United States), Latin American (Chile, Colombia, Mexico, Brazil, and Jamaica), European (Norway, Germany, Hungary, Portugal, Denmark, Yugoslavia, Slovenia, Finland, and the United Kingdom), African (Kenya, Zambia, and Zimbabwe), and Australasian (China, Indonesia, Thailand, Australia, New Zealand, and Japan). Overall, 3936 cases of SAH (892 cases in longitudinal studies [9 223 763 person-years of follow-up] and 3044 cases in case-control studies) were available for the analysis, thus allowing 1984 more cases of SAH to be analyzed than in the previous overview.

Figure 1. Flowchart detailing the exclusion and inclusion criteria and numbers of studies excluded and included at each step of the literature search.

TABLE 1. Characteristics of Longitudinal Studies Included in the Analysis*

Study (in descending chronological order), Country, and Year of PublicationNo. of SAH CasesPerson- Years of Follow-UpBaseline Age or Mean Age, yFollow-Up PeriodDiagnostic CriteriaM/FAlcoholSmokingHTOCHRTHigh TCPhysical ActivityDiabetesBMI
*Studies listed in the ascending order of year of data collection and are additional to those in the previous overview.
†Diagnosis based on medical records, mostly on clinical grounds;
‡criteria of National Survey of Stroke (probable or definite);
#percentage of SAH cases diagnosed by computed tomography, angiography, or autopsy;
§63% SAH diagnosed by computed tomography, angiography, or autopsy.
M/F indicates separate data for men and women; M-F, data for men and women together; HT, hypertension; OC, oral contraceptive use; TC, total cholesterol.
Abbott41 (Japan 1994)37165 66045–681965–1990M+
Donahue42 (USA 1986)3296 07245–691965–1977M+
Yano43 (USA 1989)39144 10845–681965–1985§M++
Knekt44 (Finland 1991)187503 48520–691966–1988ICDM/F++++
Vessey45 (UK 1989)8271 26825–391968–1987#88%F+
Iso46 (USA 1989)552 169 97235–571973–1981M++
Sankai47 (Japan 2000)*71116 29740–691975–1993#83%M/F+
Stampfer48 (USA 1991)36337 85430–631976–1984F+
Stampfer49 (USA 1988)28334 38234–591976–1984F+
Kawachi50 (USA 1993)1081 404 07230–551976–1988F+
Klatsky51 (USA 2002)*1332 320 812mean 47.51978–1996M-F+
Kurth52 (USA 2003)*31385 41945+1982–2002M+
Suh53 (Korea 2001)*98619 46335–591993–1998#89%M+++++
Kurth52 (USA 2003)*29354 89945+1993–2003F+

TABLE 2. Characteristics of Case-Control Studies Included in the Analysis*

Study, Country and Year**Population- Based DesignNo. of SAH CasesSelection Period% CT% Ang% AutM/FAlcoholSmokingHTOCHRTHigh TCPhysical ActivityDiabetesBMI
*Studies listed in the ascending order of year of data collection and are additional to those in the previous overview.
†100% CT or angiography;
‡100% angiography or autopsy;
§99% CT, but unknown how many had SAH on CT.
** Study by the first author (in descending chronological order of data collection), country, and year of publication.
% CT, % Ang, and % Aut indicate percentage of SAH cases documented by computed tomography, angiography, or autopsy, respectively; M/F, separate data for men and women; M-F, data for men and women together; HT, hypertension; OC, oral contraceptive use; HRT, hormone replacement therapy; TC, total cholesterol.
Fogelholm20 (Finland 1987)+1141967–198081M/F+
Hannaford17 (UK 1994)+731968–1990F+
Petitti33 (USA 1978)111969–1977F++
Inman32 (UK 1979)1341976763F++
Bonita21 (NZ 1986)+1151982–198382M/F++
Gill31 (UK 1991)2081983–198499§96M-F+
Canhao29 (Portugal 1994)1411985–1990100M/F+++
Isaksen13 (Norway 2002)*+261986–1997M-F+
Longstreth18 (USA 1994)+1031987–19898264F++++
Longstreth19 (USA 1992)+1491987–19898264M-F++
Fann16 (USA 2000)*+1491987–19898264M-F+
Adamson28 (UK, Denmark 1994)961989–1991100M-F++
Juvela30 (Finland 1993)2781989–199192M/F+++
WHO34 (Africa/Asia/Europe/Latin America 1996)6081989–1993>804–10F+
Ohkuma22 (Japan 2003)*3901989–1998M-F+++++
Qureshi26 (USA 2001)*3231990–199797M-F++++
Okamoto25 (Japan 2001)*1241992–1997100F++
Okamoto23 (Japan 2003)*1241992–1997F++
Ni Mhurchu15 (ANZ 2001)*+2681995–1998F++
Anderson12,54 (ANZ 2003, 2004)*+4321995–1998M-F+++++
Kunze27 (Germany 2000)*561997–1998M-F+++
Kissela14 (USA 2002)*+1071997–200090M-F+++++
Kubota24 (Japan 2001)*127?100M-F++++

An overview of the RRs of the studied factors according to study design and gender is presented in Figure 2 and Table 3. In the table, current and ever smoking are compared separately with never smoking. The risk of former smoking (not listed in the table) was twice the risk of never smoking in longitudinal studies (RR, 1.9; 95% CI, 1.5 to 2.3) and in case-control studies (OR, 2.3; 95% CI, 2.2 to 2.4). Ever smoking was associated with a 2.2- to 3.1-fold increase when compared with never smoking, and current smoking had a 2.2- to 3.1-fold increased risk when compared with never and former smoking combined, with the most pronounced associations in case-control studies. In longitudinal studies, the risks of smoking for women were twice those for men, whereas in case-control studies, the risks were greater in men.

Figure 2. Risk of SAH occurrence (RRs for longitudinal studies, ORs for case-control studies, and 95% CIs) for smoking, hypertension, alcohol abuse, oral contraception, hormone replacement therapy, ethnicity, hypercholesterolemia, rigorous physical activity, lean BMI, and diabetes by study design. Studies are listed in the ascending order according to year of publication. Diamonds represent pooled estimates, and width of the diamonds represents 95% CIs.

Figure 2 (Continued)

TABLE 3. RRs and 95% CIs of Risk Factors for SAH by Gender and Study Design

Risk FactorWomenMenTotal
†Totals represent pooled estimates for all available studies reporting data for both men and women separately or combined; there were a different No. of studies that contributed data to the overall effect estimates and No. of studies that contributed data to the sex-specific estimates, thus affecting precision of the estimates.
Most significant risk factors of SAH by gender and study design.
Smoking
    Longitudinal
        Current44,46,50,52,532.2 (1.7–2.8)2.2 (1.7–3.0)2.2 (1.3–3.6)
        Ever46,50,52,532.7 (1.8–4.1)1.4 (0.9–2.1)2.2 (1.1–4.5)
    Case-control
        Current12,13,192.4 (1.4–4.0)5.2 (3.0–9.0)3.1 (2.7–3.5)
        Ever12–14,19–24,26–31,332.6 (2.0–3.5)3.4 (2.4–4.7)3.1 (2.5–3.9)
Hypertension
    Longitudinal43,44,46,533.3 (2.1–5.3)2.3 (1.8–3.0)2.5 (2.0–3.1)
    Case-control12,14,18,21–24,26–30,323.3 (2.6–4.3)2.1 (1.4–3.2)2.6 (2.0–3.1)
Alcohol intake
    Longitudinal
        <15042,47,49,51,532.7 (1.2–5.9)1.5 (0.9–2.5)1.1 (0.8–1.6)
        >15042,47,49,51,534.0 (0.8–19.1)2.2 (1.5–3.2)2.1 (1.5–2.8)
    Case-control
        <15012,14,19,22,26,30,310.6 (0.4–1.0)0.5 (0.3–0.8)0.8 (0.7–0.9)
        >15012,14,19,22,24,26,30,315.0 (1.9–14.3)4.5 (2.5–8.0)1.5 (1.3–1.8)
Oral contraceptives
    Longitudinal455.4 (0.7–43.5)
    Case-control15,17,18,21,32–340.8 (0.5–1.3)
Hormone replacement therapy
    Longitudinal480.6 (0.2–1.5)
    Case-control15,180.6 (0.4–0.8)
Hypercholesterolemia
    Longitudinal43,46,530.8 (0.6–1.3)
    Case-control22,24,291.2 (0.5–2.5)0.5 (0.2–1.9)0.6 (0.4–0.9)
Regular rigorous exercise
    Longitudinal410.5 (0.3–1.0)
    Case-control16,541.2 (1.0–1.6)
Lean BMI
    Longitudinal530.3 (0.2–0.4)
    Case-control14,181.1 (0.7–1.9)1.4 (1.0–2.0)
Nonwhite ethnicity
    Longitudinal461.8 (0.8–4.2)
    Case-control12,193.4 (1.0–11.9)
Diabetes
    Longitudinal440 (0.0–2.9)0.7 (0.1–4.7)0.3 (0.0–2.2)
    Case-control12,14,22,24,26,270.7 (0.5–0.8)

Hypertension increased the risk of SAH by ≈2.5× in longitudinal and case-control studies and was 30% more hazardous in women. Excessive (>150 g per week) alcohol consumption was associated with ≈2-fold increased risk of SAH in longitudinal and case-control studies, with a more hazardous effect in women.

Use of oral contraceptives did not significantly affect the risk of SAH in 1 small longitudinal study or in 7 case-control studies. Hormone replacement therapy was associated with nonsignificantly reduced risk of SAH in 1 longitudinal study and with 40% significantly reduced risk of SAH in 2 population-based case-control studies.

Hypercholesterolemia was associated with reduced risk of SAH but to a statistically significant level only in case-control studies (40% risk reduction), with no clear gender differences in the strength of the associations. One longitudinal study demonstrated a marginally nonsignificant protective effect of regular rigorous physical activity in men, whereas 2 case-control studies showed a slightly hazardous albeit nonsignificant effect of regular rigorous physical activity on the risk of SAH.

Lean BMI was associated with a 70% decreased risk of SAH in men in 1 longitudinal study, but it was associated with an increased risk, although not statistically significant, in 2 case-control studies. Nonwhite ethnicity was associated with 3.4-fold increased risk of SAH in 2 case-control studies and with ≈2-fold but not statistically significant risk of SAH in 1 longitudinal study. Diabetes was associated with reduced risk of SAH but to a statistically significant level in case-control studies only (30% risk reduction).

Discussion

This review was based on almost twice as many studies as in the previous review,9 and we have confirmed and extended the previous analyses. Smoking, hypertension, and excessive alcohol intake have statistically significant and consistent associations with an increased risk of SAH in case-control and longitudinal studies; because of the increase in the number of studies in this analysis, the estimates of association obtained are more precise. In addition to the previous overview, we found that the risk of SAH in former smokers is almost twice that of never smokers. Our previous research also showed that cardiovascular risk factors have the highest population-attributable risk associated with SAH.5 New information included in the current review has suggested that nonwhite ethnicity is associated with higher risk of SAH. In contrast, hormone replacement therapy and probably hypercholesterolemia appear to be risk-reducing factors. Use of oral contraceptives did not affect the risk of SAH, whereas data were inconsistent for lean BMI and regular rigorous physical activity.

Our findings concerning the nonsignificant effect of oral contraceptives on the risk of SAH do not confirm the increased risk found in another meta-analysis devoted to only oral contraceptives and SAH.35 The reason for the discrepancy might be the less stringent study selection criteria (especially for diagnosis of SAH) in the other review. The relatively high risk of SAH associated with nonwhite ethnicity found in this study was based only on 2 case-control studies and is probably linked with substantial differences in cardiovascular risk factor profiles (especially smoking and hypertension) between white and nonwhite populations.36,37 However, the extent and relative contribution of cardiovascular risk factors remain unclear because in our meta-analysis, we were not able to adjust the effect estimates for these confounders.

An unexpected and new finding in this review was that diabetes mellitus was associated with substantial reduction of the risk of SAH. This reduction was statistically significant in case-control studies but not in 1 longitudinal study available for the analysis. It is possible that patients with diabetes have a high risk of dying from other causes, and therefore the chances of developing SAH are smaller than in controls. A recent case-control study of SAH in Japan (not included in the present analysis because additional criteria [history of head trauma] were used for selection of controls) also demonstrated that diabetes mellitus was inversely associated with the risk of SAH.38 It has been suggested that lower or equivalent prevalence of diabetes mellitus in SAH patients than in the general population may be attributed to better medical treatment or altering lifestyle factors (eg, better dietary control) in the diabetic patients.39 However, the biological basis for inverse associations between diabetes mellitus and the risk of SAH is not well understood. Nevertheless, the size and consistency of the associations warrant further study.

Although the reduced risk of hypercholesterolemia for SAH was not statistically significant in longitudinal studies, it was in case-control studies. This reduced risk for SAH in patients with hypercholesterolemia is in line with findings for intracerebral hemorrhage.40 The predictive values of lean BMI were nonstatistically significant and were discordant between case-control and longitudinal studies. Despite known gender differences in the risk of SAH, only few epidemiological studies explored gender differences in risk factors for SAH. Our finding that most risk factors tend to be more hazardous in women than in men, although this difference is statistically nonsignificant, suggests that this may contribute to the higher incidence of SAH observed in women.

Although inferences from an overview without individual patient data are subject to limitations, our findings first reinforce the importance of smoking cessation, blood pressure control, and avoidance of excess in alcohol intake for SAH prevention, and second, they provide directions for further research into the pathogenesis of aneurysm formation and rupture.

C.M.M.L. is supported by a National Heart Foundation (New Zealand) fellowship.

Footnotes

Correspondence to Associate Professor Valery Feigin, Clinical Trials Research Unit, Faculty of Medicine and Health Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand. E-mail

References

  • 1 Feigin VL, Lawes CM, Bennett DA, Anderson CS. Stroke epidemiology: a review of population-based studies of incidence, prevalence, and case-fatality in the late 20th century. Lancet Neurol. 2003; 2: 43–53.CrossrefMedlineGoogle Scholar
  • 2 Johnston SC, Selvin S, Gress DR. The burden, trends, and demographics of mortality from subarachnoid hemorrhage. Neurology. 1998; 50: 1413–1418.CrossrefMedlineGoogle Scholar
  • 3 Linn FH, Rinkel GJ, 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.CrossrefMedlineGoogle Scholar
  • 4 Hackett ML, Anderson CS. Health outcomes 1 year after subarachnoid hemorrhage: an international population-based study. The Australian Cooperative Research on Subarachnoid Hemorrhage Study Group. Neurology. 2000; 55: 658–662.CrossrefMedlineGoogle Scholar
  • 5 Ruigrok YM, Buskens E, Rinkel GJ. Attributable risk of common and rare determinants of subarachnoid hemorrhage. Stroke. 2001; 32: 1173–1175.CrossrefMedlineGoogle Scholar
  • 6 Stegmayr B, Eriksson M, Asplund K. Declining mortality from subarachnoid hemorrhage: changes in incidence and case fatality from 1985 through 2000. Stroke. 2004; 35: 2059–2063.LinkGoogle Scholar
  • 7 Ingall TJ, Whisnant JP, Wiebers DO, O’Fallon WM. Has there been a decline in subarachnoid hemorrhage mortality? Stroke. 1989; 20: 718–724.CrossrefMedlineGoogle Scholar
  • 8 Sakurai Y, Li JH, Komatsu S, Saito H, Abe S, Yamada A, Nishikori M, Tsuji I, Hisamichi S. The secular trend in the incidence of subarachnoid hemorrhage in Miyagi, Japan: 1979–1990. Tohoku J Exp Med. 1995; 177: 89–92.CrossrefMedlineGoogle Scholar
  • 9 Teunissen LL, Rinkel GJ, Algra A, van Gijn J. Risk factors for subarachnoid hemorrhage: a systematic review. Stroke. 1996; 27: 544–549.CrossrefMedlineGoogle Scholar
  • 10 Petitti DB. Meta-Analysis, Decision Analysis, and Cost-Effectiveness Analysis. New York, NY: Oxford University Press; 1994.Google Scholar
  • 11 DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986; 7: 177–188.CrossrefMedlineGoogle Scholar
  • 12 Anderson CS, Feigin V, Bennett D, Lin RB, Hankey G, Jamrozik K. Australasian Cooperative Research on Subarachnoid Hemorrhage Study G roup. Active and passive smoking and the risk of subarachnoid hemorrhage: an international population-based case-control study. Stroke. 2004; 35: 633–637.LinkGoogle Scholar
  • 13 Isaksen J, Egge A, Waterloo K, Romner B, Ingebrigtsen T. Risk factors for aneurysmal subarachnoid hemorrhage: the Tromso Study. J Neurol Neurosurg Psychiatry. 2002; 73: 185–187.CrossrefMedlineGoogle Scholar
  • 14 Kissela BM, Sauerbeck L, Woo D, Khoury J, Carrozzella J, Pancioli A, Jauch E, Moomaw CJ, Shukla R, Gebel J, Fontaine R, Broderick J. Subarachnoid hemorrhage: a preventable disease with a heritable component. Stroke. 2002; 33: 1321–1326.LinkGoogle Scholar
  • 15 Ni Mhurchu C, Anderson C, Jamrozik K, Hankey G, Dunbabin D, Australasian Cooperative Research on Subarachnoid Hemorrhage Study (ACROSS) Group. Hormonal factors and risk of aneurysmal subarachnoid hemorrhage: an international population-based, case-control study. Stroke. 2001; 32: 606–612.CrossrefMedlineGoogle Scholar
  • 16 Fann JR, Kukull WA, Katon WJ, Longstreth WT Jr. Physical activity and subarachnoid haemorrhage: a population based case-control study. J Neurol Neurosurg Psychiatry. 2000; 69: 768–772.CrossrefMedlineGoogle Scholar
  • 17 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.CrossrefMedlineGoogle Scholar
  • 18 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.CrossrefMedlineGoogle Scholar
  • 19 Longstreth WT Jr, Nelson LM, Koepsell TD, van Belle G. Cigarette smoking, alcohol use, and subarachnoid hemorrhage. Stroke. 1992; 23: 1242–1249.CrossrefMedlineGoogle Scholar
  • 20 Fogelholm R, Murros K. Cigarette smoking and subarachnoid hemorrhage: a population-based case-control study. J Neurol Neurosurg Psychiatry. 1987; 50: 78–80.CrossrefMedlineGoogle Scholar
  • 21 Bonita R. Cigarette smoking, hypertension and the risk of subarachnoid hemorrhage: a population-based case-control study. Stroke. 1986; 17: 831–835.CrossrefMedlineGoogle Scholar
  • 22 Ohkuma H, Tabata H, Suzuki S, Islam MS. Risk factors for aneurysmal subarachnoid hemorrhage in Aomori, Japan. Stroke. 2003; 34: 96–100.LinkGoogle Scholar
  • 23 Okamoto K, Horisawa R, Kawamura T, Asai A, Ogino M, Takagi T, Ohno Y. Family history and risk of subarachnoid hemorrhage: a case-control study in Nagoya, Japan. Stroke. 2003; 34: 422–426.LinkGoogle Scholar
  • 24 Kubota M, Yamaura A, Ono J. Prevalence of risk factors for aneurysmal subarachnoid hemorrhage: results of a Japanese multicentre case control study for stroke. Br J Neurosurg. 2001; 15: 474–478.CrossrefMedlineGoogle Scholar
  • 25 Okamoto K, Horisawa R, Kawamura T, Asai A, Ogino M, Takagi T, Ohno Y. Menstrual and reproductive factors for subarachnoid hemorrhage risk in women: a case-control study in Nagoya, Japan. Stroke. 2001; 32: 2841–2844.CrossrefMedlineGoogle Scholar
  • 26 Qureshi AI, Suri MF, Yahia AM, Suarez JI, Guterman LR, Hopkins LN, Tamargo RJ. Risk factors for subarachnoid hemorrhage. Neurosurgery. 2001; 49: 607–612.MedlineGoogle Scholar
  • 27 Kunze AK, Annecke A, Wigger F, Lichy C, Buggle F, Schnippering H, Schnitzler P, Grau AJ. Recent infection as a risk factor for intracerebral and subarachnoid hemorrhages. Cerebrovasc Dis. 2000; 10: 352–358.CrossrefMedlineGoogle Scholar
  • 28 Adamson J, Humphries SE, Ostergaard JR, Voldby B, Richards P, Powell JT. Are cerebral aneurysms atherosclerotic? Stroke. 1994; 25: 963–966.CrossrefMedlineGoogle Scholar
  • 29 Canhao P, Pinto AN, Ferro H, Ferro JM. Smoking and aneurysmal subarachnoid haemorrhage: a case-control study. J Cardiovasc Risk. 1994; 1: 155–158.CrossrefMedlineGoogle Scholar
  • 30 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.CrossrefMedlineGoogle Scholar
  • 31 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.CrossrefMedlineGoogle Scholar
  • 32 Inman WH. Oral contraceptives and fatal subarachnoid haemorrhage. BMJ. 1979; 2: 1468–1470.CrossrefMedlineGoogle Scholar
  • 33 Petitti DB, Wingerd J. Use of oral contraceptives, cigarette smoking, and risk of subarachnoid haemorrhage. Lancet. 1978; 2: 234–235.CrossrefMedlineGoogle Scholar
  • 34 Haemorrhagic stroke, overall stroke risk, and combined oral contraceptives: results of an international, multicentre, case-control study. WHO Collaborative Study of Cardiovascular Disease and Steroid Hormone Contraception. Lancet. 1996; 348: 505–510.CrossrefMedlineGoogle Scholar
  • 35 Johnston SC, Colford JM Jr, Gress DR. Oral contraceptives and the risk of subarachnoid hemorrhage: a meta-analysis. Neurology. 1998; 51: 411–418.CrossrefMedlineGoogle Scholar
  • 36 Feigin VL, Rodgers A. Editorial comment–ethnic disparities in risk factors for stroke: what are the implications? Stroke. 2004; 35: 1568–1569.LinkGoogle Scholar
  • 37 Hajat C, Dundas R, Stewart JA, Lawrence E, Rudd AG, Howard R, Wolfe CD. Cerebrovascular risk factors and stroke subtypes: differences between ethnic groups. Stroke. 2001; 32: 37–42.CrossrefMedlineGoogle Scholar
  • 38 Inagawa T. Risk factors for aneurysmal subarachnoid hemorrhage in patients in Izumo City, Japan. J Neurosurg. 2005; 102: 60–67.CrossrefMedlineGoogle Scholar
  • 39 Adams HP Jr, Putman SF, Kassell NF, Torner JC. Prevalence of diabetes mellitus among patients with subarachnoid hemorrhage. Arch Neurol. 1984; 41: 1033–1035.CrossrefMedlineGoogle Scholar
  • 40 Ariesen MJ, Claus SP, Rinkel GJE, Algra A. Risk factors for intracerebral hemorrhage in the general population: a systematic review. Stroke. 2003; 34: 2060–2065.LinkGoogle Scholar
  • 41 Abbott RD, Rodriguez 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.CrossrefMedlineGoogle Scholar
  • 42 Donahue RP, Abbott RD, Reed DM, Yano K. Alcohol and hemorrhagic stroke. The Honolulu Heart Program. J Am Med Assoc. 1986; 255: 2311–2314.CrossrefMedlineGoogle Scholar
  • 43 Yano K, Reed DM, MacLean CJ. Serum cholesterol and hemorrhagic stroke in the Honolulu Heart Program. Stroke. 1989; 20: 1460–1465.CrossrefMedlineGoogle Scholar
  • 44 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.CrossrefMedlineGoogle Scholar
  • 45 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.CrossrefMedlineGoogle Scholar
  • 46 Iso H, Jacobs DR Jr, 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.CrossrefMedlineGoogle Scholar
  • 47 Sankai T, Iso H, Shimamoto T, Kitamura A, Naito Y, Sato S, Okamura T, Imano H, Iida M, Komachi Y. Prospective study on alcohol intake and risk of subarachnoid hemorrhage among Japanese men and women. Alcohol Clin Exp Res. 2000; 24: 386–389.CrossrefMedlineGoogle Scholar
  • 48 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 Eng J Med. 1991; 325: 756–762.CrossrefMedlineGoogle Scholar
  • 49 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 Eng J Med. 1988; 319: 267–273.CrossrefMedlineGoogle Scholar
  • 50 Kawachi I, Colditz GA, Stampfer MJ, Willett WC, Manson JE, Rosner B, Speizer FE, Hennekens CH. Smoking cessation and decreased risk of stroke in women. J Am Med Assoc. 1993; 269: 232–236.CrossrefMedlineGoogle Scholar
  • 51 Klatsky AL, Armstrong MA, Friedman GD, Sidney S. Alcohol drinking and risk of hemorrhagic stroke. Neuroepidemiology. 2002; 21: 115–122.CrossrefMedlineGoogle Scholar
  • 52 Kurth T, Kase CS, Berger K, Schaeffner ES, Buring JE, Gaziano JM. Smoking and the risk of hemorrhagic stroke in men. Stroke. 2003; 34: 1151–1155.LinkGoogle Scholar
  • 53 Suh I, Jee SH, Kim HC, Nam CM, Kim IS, Appel LJ. Low serum cholesterol and haemorrhagic stroke in men: Korea Medical Insurance Corporation Study. Lancet. 2001; 357: 922–925.CrossrefMedlineGoogle Scholar
  • 54 Anderson C, Ni Mhurchu C, Scott D, Bennett D, Jamrozik K, Hankey G. Triggers of subarachnoid hemorrhage: role of physical exertion, smoking, and alcohol in the Australasian Cooperative Research on Subarachnoid Hemorrhage Study (ACROSS). Stroke. 2003; 34: 1771–1776.LinkGoogle Scholar

eLetters(0)

eLetters should relate to an article recently published in the journal and are not a forum for providing unpublished data. Comments are reviewed for appropriate use of tone and language. Comments are not peer-reviewed. Acceptable comments are posted to the journal website only. Comments are not published in an issue and are not indexed in PubMed. Comments should be no longer than 500 words and will only be posted online. References are limited to 10. Authors of the article cited in the comment will be invited to reply, as appropriate.

Comments and feedback on AHA/ASA Scientific Statements and Guidelines should be directed to the AHA/ASA Manuscript Oversight Committee via its Correspondence page.