Worldwide Incidence of Aneurysmal Subarachnoid Hemorrhage According to Region, Time Period, Blood Pressure, and Smoking Prevalence in the Population: A Systematic Review and Meta-analysis

Nima Etminan; Han-Sol Chang; Katharina Hackenberg; Nicolien K de Rooij; Mervyn D I Vergouwen; Gabriel J E Rinkel; Ale Algra

doi:10.1001/jamaneurol.2019.0006

. 2019 Jan 19;76(5):588–597. doi: 10.1001/jamaneurol.2019.0006

Worldwide Incidence of Aneurysmal Subarachnoid Hemorrhage According to Region, Time Period, Blood Pressure, and Smoking Prevalence in the Population

A Systematic Review and Meta-analysis

Nima Etminan ^1,^✉, Han-Sol Chang ¹, Katharina Hackenberg ¹, Nicolien K de Rooij ², Mervyn D I Vergouwen ³, Gabriel J E Rinkel ³, Ale Algra ^3,⁴

¹Department of Neurosurgery, Mannheim University Hospital, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany

²Department of Rehabilitation, St Antonius Hospital, Nieuwegein, the Netherlands

³Brain Centre Rudolf Magnus, Department of Neurology and Neurosurgery, University Medical Centre Utrecht, Utrecht University, Utrecht, the Netherlands

⁴Julius Center for Health Sciences and Primary Care, University Medical Centre Utrecht, Utrecht University, Utrecht, the Netherlands

Accepted for Publication: December 7, 2018.

^✉

Corresponding Author: Nima Etminan, MD, Department of Neurosurgery, Mannheim University Hospital, Medical Faculty Mannheim, Heidelberg University, Theodor-Kutzer-Ufer 1-3, 68135 Mannheim, Germany (nima.etminan@medma.uni-heidelberg.de).

Published Online: January 19, 2019. doi:10.1001/jamaneurol.2019.0006

Author Contributions: Dr Etminan had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Drs Etminan and Chang contributed equally.

Study concept and design: Etminan, de Rooij, Rinkel, Algra.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: Etminan, Chang.

Critical revision of the manuscript for important intellectual content: All authors.

Statistical analysis: Chang, Algra.

Administrative, technical, or material support: Chang, Hackenberg.

Study supervision: Etminan, Algra.

Conflict of Interest Disclosures: None reported.

Meeting Presentation: This paper was presented at the German Society for Neurointensive and Emergency Medicine and the German Stroke Society 35th Annual Meeting; January 19, 2019; Berlin, Germany.

Additional Contributions: We sincerely thank Majid Ezzati, FMedSci, and Bin Zhou, PhD, as well as the Noncommunicable Disease Risk Factor Collaboration group (http://www.ncdrisc.org) for providing the detailed country-specific, age-specific, and sex-specific blood pressure data of the Noncommunicable Disease Risk Factor dataset. Contributors were not compensated for their work. We also thank the reviewers of our manuscript for their comments, some of which urged us to do additional analyses that yielded interesting and novel findings and ultimately helped us to improve the quality of our manuscript.

^✉

Corresponding author.

PMCID: PMC6515606 PMID: 30659573

Key Points

Question

What are the time trends and associated factors for the incidence of aneurysmal subarachnoid hemorrhage (SAH)?

Findings

In this systematic review and meta-analysis including 75 studies and 8176 patients, the crude global incidence of SAH declined from 10.2 per 100 000 person-years in 1980 to 6.1 in 2010, but large variation according to region, age, and sex exists. The global incidence of SAH decreased by 7.1% with every millimeter of mercury decrease in systolic blood pressure, 11.5% for every millimeter of mercury decrease in diastolic blood pressure, and 2.4% for every percentage decrease in smoking prevalence.

Meaning

Understanding determinants for regional differences and further reducing blood pressure and smoking prevalence may yield a diminished SAH burden.

This systematic review and meta-analysis assesses worldwide aneurysmal subarachnoid hemorrhage incidence according to region, age, sex, time period, blood pressure, and smoking prevalence.

Abstract

Importance

Subarachnoid hemorrhage (SAH) from ruptured intracranial aneurysms is a subset of stroke with high fatality and morbidity. Better understanding of a change in incidence over time and of factors associated with this change could facilitate primary prevention.

Objective

To assess worldwide SAH incidence according to region, age, sex, time period, blood pressure, and smoking prevalence.

Data Sources

We searched PubMed, Web of Science, and Embase for studies on SAH incidence published between January 1960 and March 2017. Worldwide blood pressure and smoking prevalence data were extracted from the Noncommunicable Disease Risk Factor and Global Burden of Disease data sets.

Study Selection

Population-based studies with prospective designs representative of the entire study population according to predefined criteria.

Data Extraction and Synthesis

Two reviewers independently extracted data according to PRISMA guidelines. Incidence of SAH was calculated per 100 000 person-years, and risk ratios (RRs) including 95% CIs were calculated with multivariable random-effects binomial regression. The association of SAH incidence with blood pressure and smoking prevalence was assessed with linear regression.

Main Outcomes and Measures

Incidence of SAH.

Results

A total of 75 studies from 32 countries were included. These studies comprised 8176 patients with SAH were studied over 67 746 051 person-years. Overall crude SAH incidence across all midyears was 7.9 (95% CI, 6.9-9.0) per 100 000 person-years; the RR for women was 1.3 (95% CI, 0.98-1.7). Compared with men aged 45 to 54 years, the RR in Japanese women older than 75 years was 2.5 (95% CI, 1.8-3.4) and in European women older than 75 years was 1.5 (95% CI, 0.9-2.5). Global SAH incidence declined from 10.2 (95% CI, 8.4-12.5) per 100 000 person-years in 1980 to 6.1 (95% CI, 4.9-7.5) in 2010 or by 1.7% (95% CI, 0.6-2.8) annually between 1955 and 2014. Incidence of SAH declined between 1980 and 2010 by 40.6% in Europe, 46.2% in Asia, and 14.0% in North America and increased by 59.1% in Japan. The global SAH incidence declined with every millimeter of mercury decrease in systolic blood pressure by 7.1% (95% CI, 5.8-8.4) and with every percentage decrease in smoking prevalence by 2.4% (95% CI, 1.6-3.3).

Conclusions and Relevance

Worldwide SAH incidence and its decline show large regional differences and parallel the decrease in blood pressure and smoking prevalence. Understanding determinants for regional differences and further reducing blood pressure and smoking prevalence may yield a diminished SAH burden.

Introduction

Subarachnoid hemorrhage (SAH) from a ruptured intracranial aneurysm accounts for 5% of all strokes and carries an exceptionally high disease-specific burden; half of patients with SAH are younger than 55 years, one-third die within the initial days to weeks after the hemorrhage, and most survivors have long-term disability or cognitive impairment.¹ On a community level, the loss of productive life-years after SAH is similar in magnitude to that of ischemic stroke. The crude incidence of SAH was previously estimated to be 9 per 100 000 person-years but varied considerably according to geographic location, age, and sex.² More recently, register-based or regional studies have reported conflicting data on reduction of SAH incidence over time.^3,4 If SAH incidence has indeed declined and potential determinants for such a decline could be detected on a population-based level, then this would have important implications for primary prevention strategies and thus reduction of the burden of disease in patients with SAH. We aimed to investigate worldwide and age-specific and sex-specific incidences of SAH according to region, age, sex, time period, blood pressure, and smoking prevalence in the population.^5,6

Methods

Search Strategy and Selection Criteria

To identify population-based studies on the incidence of SAH published between January 1960 and March 2017, we performed a systematic review of PubMed, Web of Science, and Embase using the keywords “subarachnoid hemorrhage” or “subarachnoid haemorrhage” and “incidence,” “epidemiology,” or “population,” building on our previous studies.^2,7 In addition, we cross-referenced the list of studies with the personal database of references of one of the authors (G.J.E.R.) to include missing studies. Our study followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Inclusion criteria were (1) a prospective study design, (2) the study population being representative of the studied population in general, (3) SAH reported as an individual entity, (4) the data including crude figures or enabling crude calculation of SAH incidence, (5) case findings permitting inclusion of all hospitals in the region and either involvement of general practitioners or review of death certificates by the study investigator(s), (6) diagnostic verification, including a neuroimaging rate greater than 80% or at least lumbar puncture or autopsy, (7) an upper age limit for the study not lower than 75 years, and (8) a lower age limit not greater than 25 years. Registry-based, hospital-based, and cohort studies, studies on nonaneurysmal SAH, and studies reporting data only for specific ethnic groups were excluded. In studies reporting on similar study populations or study periods, we only included the most recent study or the study with the greater amount of person-years or more sophisticated case finding methods.

Data Extraction

For studies published between October 2005 and March 2017, 2 reviewers (H.-S.C. and K.H.) assessed all newly retrieved studies independent from each other and registered the following items in a data extraction form: (1) size of study population; (2) study region; (3) midyear and study period; (4) number of patients with SAH; (5) case finding methods for SAH; (6) diagnostic criteria for SAH; and (7) age-specific and sex-specific incidence. For previously identified studies, we used data we had extracted in the same fashion.^2,7 Excellent diagnostics was defined as greater than 90% of patients with SAH being diagnosed with brain imaging (computed tomography [CT] or magnetic resonance imaging). In the event of disagreement on extracted data, the article was assessed by 2 other authors (N.E. and M.D.I.V.) independently from each other and discussed between the 4 authors until agreement was achieved. We used incidence rates relating to the entire population, without adjustment for age or sex. To determine the association of SAH incidence with age and sex, we collected age-specific and sex-specific incidence from the subset of studies that provided sufficient data. Study investigators were contacted for missing data on crude incidence of SAH when required. Since only 14% of studies included in our meta-analysis reported data on smoking or hypertension prevalence in patients with SAH and not for the entire reported population, we extracted age-specific, sex-specific, midyear-specific, and country-specific systolic and diastolic blood pressure values from the Noncommunicable Disease Risk Factor (NCD) data set⁵ and smoking prevalence data from the Global Burden of Disease Study⁶ to analyze their association with SAH incidence within the age-specific and sex-specific SAH incidence data set.

Data Analyses

For each of the included studies, the crude SAH incidence with corresponding 95% CIs was calculated with Poisson methods. For all subsequent analyses, we used random-effects binomial regression, with the number of SAHs and the number of person-years for each study as variables (RMA.GLMN module in R version 3.4.3 [The R Foundation]). Overall and regional incidences were estimated based on the models’ intercept; in addition, I² was calculated as a measure of variation, ie, heterogeneity, between the included studies.⁸ We considered an I² of 25% to 49% as low, 50% to 74% as moderate, and 75% or greater as high heterogeneity. To assess regional differences, we compared studies by continent or country. Next, we determined the association of age, sex, and time period with the incidence of SAH. In addition, we studied regional patterns of the association of age, sex, and time period with SAH incidence. To estimate current SAH incidence vs previous SAH incidence, we used the regression models and midyear cut-off of all studies (1996) within 15 years, which, after rounding, corresponded to 2010 (current SAH incidence) and 1980 (historic SAH incidence). In the age-specific and sex-specific data subset, we adjusted the time trend analyses for age and sex. In addition, we determined the association of blood pressure and smoking prevalence with SAH incidence. To describe patterns of blood pressure and smoking prevalence over time, we used linear regression analysis. Multivariable regression was used to estimate the (independent) contribution of continent, age, and sex as well as time trends to SAH incidence. Since our previous meta-analysis found a higher SAH incidence in Finland and Japan compared with the reference population,² we specifically analyzed the SAH incidence according to time for these countries. Included studies were reviewed for adherence to core and/or supplemental criteria for population-based stroke studies in relation to the midyear cutoff of all studies (1996).⁹ In sensitivity analyses, we restricted the time trend analysis to studies with at least 90% cranial scanning as well as studies with a midyear of study of 1985 at the earliest and with data on percentage of CT scanning.

Results

Data from 75 population-based studies and 84 study periods were included (eFigure 1 in the Supplement). For all 75 studies (range of midyears, 1955-2014), 55 (73%) fulfilled core criteria for population-based studies. For the 56 studies published after 1996, 48 studies (86%) fulfilled these criteria.

These studies described 8176 patients with SAH over 67 746 051 person-years from 32 countries and 6 continents. The median percentage of cranial imaging for detection of SAH was 91% (interquartile range, 78-97). Incidences of SAH by region, population size, study midyear, and case finding method as well as the diagnostic criteria for each study are listed in eTable 1 in the Supplement. Summary characteristics of the overall and age-specific and sex-specific data sets are provided in eTable 2 in the Supplement. Overall crude SAH incidence across all midyears was 7.9 (95% CI, 6.9-9.0) per 100 000 person-years (I² = 96.6%) (Figure 1^{10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51} and Figure 2^{52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85}).

Figure 2. — Crude SAH incidence per 100 000 person-years with 95% CIs are presented according to continent, country, and midyear. I² values are calculated per continent and overall including Europe (Figure 1).

SAH Incidence by Region and Time Trends

The crude worldwide SAH incidence (84 study periods) was 6.1 (95% CI, 4.9-7.5) per 100 000 person-years for 2010 and 10.2 (95% CI, 8.4-12.5) for 1980 and declined annually by 1.7% (95% CI, 0.6-2.8) between 1955 and 2014. Figure 1 and Figure 2 display the crude SAH incidences by continent and region. The SAH incidence for 2010 in Europe (45 study periods) was estimated to be 6.3 (95% CI, 4.9-8.1) per 100 000 person-years and declined annually by 1.7% (95% CI, 0.4-3.1) since 1972.^{10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51} For Finland (5 study periods), the SAH incidence was 16.6 (95% CI, 13.4-20.5) per 100 000 person-years, with no clear change over time (1972-1990); after 1990, no new studies fulfilling our inclusion criteria appeared. For Asia (13 study periods), the SAH incidence for 2010 was estimated to be 7.7 (95% CI, 2.8-21.7) per 100 000 person-years, and the annual decline was 2.0% (95% CI, −3.9 to 7.9) since 1977.^{52,53,54,55,56,57,58,59,60,61,62,63} Since 7 of 13 study periods from Asia were from Japan alone and there was a large heterogeneity between Japan and the remainder of Asia, data for Japan are presented separately. The SAH incidence in Japan was estimated to be 28.0 (95% CI, 25.3-31.0) per 100 000 person-years and increased annually by 1.6% (95% CI, 0.8-2.3) since 1977.^{52,53,54,55,56,57} In Asia excluding Japan, the SAH incidence for 2010 was estimated to be 3.7 (95% CI, 0.1-13.3) per 100 000 person-years, and the annual decline since 1984 was 1.3% (95% CI, −7.2 to 9.8).^{58,59,60,61,62,63} For North America (7 study periods), the SAH incidence for 2010 was estimated to be 6.9 (95% CI, 4.8-10.0) per 100 000 person-years, and the annual decline was 0.7% (95% CI, −0.4 to 1.8) since 1955.^73,74,75,76 Crude incidences for SAH, risk ratios (RRs) for SAH incidence, and time trends for all geographical locations, including Middle and South America (8 study periods),^{77,78,79,80,81,82,83,84} Australia and New Zealand (10 study periods),^{64,65,66,67,68,69,70,71,72} and Africa (Nigeria),⁸⁵ are summarized in Table 1. Continental and regional SAH incidences and time trends from studies reporting incidence data in the same population over several time periods are highlighted in eFigure 2 in the Supplement. In this subset of studies, there was a decrease in SAH incidence in most studies from Europe^{11,13,15,40,47,48,50,51} and the study from North America⁷⁴ and an increase in SAH incidence in the 2 studies from Japan.^53,86

Table 1. Subarachnoid Hemorrhage (SAH) Incidence, Risk Ratios (RRs), Midyear Range, and Time Trends by Region.

Geographic Location	No. of Study Periods	Overall SAH Incidence (95% CI)	I², %	RR of Overall Incidence (95% CI)	Time Trends
					Range of Midyears	SAH Incidence (95% CI)		Annual Change, % (95% CI)
					Range of Midyears	1980	2010	Annual Change, % (95% CI)
Global	84	7.9 (6.9 to 9.0)	96.6	NA	1955-2014	10.2 (8.4 to 12.5)	6.1 (4.9 to 7.5)	−1.7 (−2.8 to −0.6)
Europe overall	45	8.3 (7.2 to 9.5)	91.7	1 [Reference]	1972-2010	10.6 (8.5 to 13.3)	6.3 (4.9 to 8.1)	−1.7 (−3.1 to −0.4)
Europe without Finland	40	7.5 (6.6 to 8.6)	87.6	1 [Reference]^a	1972-2010	8.4 (6.4 to 11.1)	6.9 (5.4 to 8.8)	−0.7 (−2.2 to 0.8)
Finland	5	16.6 (13.4 to 20.5)^b	65.8	2.1 (1.5 to 3.1)^a	1972-1990	16.6 (13.4 to 20.6)	ND	−0.1 (−3.5 to 3.5)
Asia overall	13	10.4 (5.9 to 18.6)	99.5	1.4 (1.0 to 1.9)	1977-2010	14.3 (4.9 to 41.5)	7.7 (2.8 to 21.7)	−2.0 (−7.9 to 3.9)
Asia without Japan	6	4.3 (0.5 to 36.4)	95.5	0.6 (0.4 to 0.9)	1984-2010	5.5 (0.9 to 32.2)	3.7 (0.1 to 13.3)	−1.3 (−9.8 to 7.2)
Japan	7	22.5 (20.3 to 24.9)	78.5	2.6 (1.8 to 3.9)	1977-2006	17.6 (15.4 to 20.1)	28.0 (25.3 to 31.0)	1.6 (0.8 to 2.3)
Australia/New Zealand	10	8.5 (7.8 to 9.3)	0	0.9 (0.7 to 0.9)	1982-2010	9.4 (0.8 to 11.0)	7.4 (6.0 to 9.2)	−0.8 (−1.8 to 0.3)
North America	7	8.5 (7.1 to 10.2)	68.9	0.7 (0.6 to 0.8)	1955-2008	8.0 (7.2 to 10.1)	6.9 (4.8 to 10.0)	−0.7 (−1.8 to 0.4)
South/Middle America	8	4.8 (4.1 to 5.6)	7.4	0.5 (0.4 to 0.8)	1998-2014	3.3 (1.6 to 7.1)	5.1 (4.2 to 6.1)	1.4 (−1.5 to 4.3)
Africa	1	4.1 (2.6 to 6.3)	NA	0.5 (0.2 to 1.5)	2011	NA	NA	NA

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Abbreviations: NA, not applicable; ND, no data.

^{^a}

Europe without Finland; the RR for Finland is in comparison with this reference. For the remainder of the comparison, Europe as a whole including Finland is used as the reference value.

^{^b}

The overall Finnish SAH incidence is derived from incidence studies with a midyear range from 1972 to 1990.

The sensitivity analysis for the overall decline in the 40 studies that had at least 90% CT scanning^{14,18,20,21,22,23,24,27,28,29,30,32,34,35,37,39,44,49,51,53,54,56,57,58,59,62,66,68,69,71,72,75,76,77,78,79,80,81,82,84} demonstrated an annual decrease in SAH incidence of 2.1% (95% CI, −1.0 to 5.0). The 63 studies with a midyear of study after 1985 and data on percentage of CT scanning^{10,13,14,15,18,19,20,21,22,23,24,25,27,28,29,30,31,32,33,34,35,37,38,39,42,43,44,45,48,49,50,51,53,54,55,56,57,58,59,60,62,63,64,65,66,67,68,69,71,72,73,75,76,77,78,79,80,81,82,83,84} showed an annual decrease in SAH incidence of 1.4% (95% CI, −1.0 to 3.7) and an annual decrease in SAH incidence after adjustment for percentage of CT scanning of 1.3% (95% CI, −1.2 to 3.8).

SAH Incidence Stratified by Age, Sex, Region, and Time Trends

Twenty-nine studies^{10,19,20,27,28,29,32,34,36,43,51,52,53,57,58,64,66,67,72,73,77,78,79,83,84,85,86,87,88} with data on 34 study periods reported age-specific and sex-specific SAH incidence for 2133 patients with SAH over 17 029 016 person-years in 18 countries and 6 continents (eTable 2 in the Supplement). In this subset of studies, the overall incidence was 10.3 (95% CI, 9.0-11.9). Irrespective of geographical location, the incidence of SAH increased with increasing age but increased distinctly more in women older than 55 years (eFigure 3 and eTables 3 and 4 in the Supplement). The increase of SAH incidence associated with increasing age was higher in Japanese women older than 75 years (RR, 2.5; 95% CI, 1.8-3.4) than in European women older than 75 years (RR, 1.5; 95% CI, 0.9-2.5) compared with men aged 45 to 54 years from the same region.

The overall sex-specific incidence of SAH was 11.5 (95% CI, 9.5-13.9) per 100 000 person-years in women vs 9.3 (95% CI, 7.7-11.3) in men; the RR for women was 1.3 (95% CI, 0.98-1.7), which remained essentially the same after adjustment for midyear of study. In Europe, the SAH incidence was 12.5 (95% CI, 10.1-15.4) per 100 000 person-years in women and 10.7 (95% CI, 8.2-13.9) in men; the RR for women was 1.1 (95% CI, 0.8-1.5). In Japan, the incidence in women was 22.9 (95% CI, 15.7-33.5) per 100 000 person-years and in men was 19.5 (95% CI, 14.2-26.8); the RR for women was 1.3 (95% CI, 0.8-2.1). In Asia overall, the SAH incidence in women was 17.8 (95% CI, 12.4-25.7) per 100 000 person-years and in men was 14.8 (95% CI, 10.8-20.3); the RR for women was 1.3 (95% CI, 0.8-2.1) (eTable 4 in the Supplement). The annual decline in overall SAH incidence was 2.2% (95% CI, 0.7-3.7) in the sex-adjusted analysis and 2.3% (95% CI, 1.2-3.3) in the age-adjusted analysis (eTable 5 in the Supplement). This decline was more apparent in men (3.4%; 95% CI, 1.9-4.8) than women (1.3%; 95% CI, −0.3 to 2.8). After adjustment for age, SAH incidence in Europe tended to decline (annual decline, 0.7%; 95% CI, −1.3 to 2.7); this tendency was more visible in men. In Japan, there was an increase in crude SAH incidence (annual increase, 4.3%; 95% CI, 1.3-7.3) and sex-adjusted SAH incidence (annual increase, 4.2%; 95% CI, 1.3-7.2), which was no longer statistically significant after adjustment for age (annual increase, 0.9%; 95% CI, −0.6 to 2.4).

Association of Blood Pressure Levels and Smoking Prevalence With SAH Incidence by Region and Time Trends

Data on systolic and diastolic blood pressures were available for 18 countries and 34 study periods for which age-specific, sex-specific, midyear-specific, and country-specific SAH incidence data were available. Mean systolic and diastolic blood pressures, smoking prevalence, annual changes, and 1980 and 2010 estimates are given in Table 2. The annual changes in systolic and diastolic blood pressure by age category and sex between 1980 and 2010 are given in eTable 6 in the Supplement.

Table 2. Association of Mean Blood Pressure (BP) and Smoking Prevalence Time Trends With Subarachnoid Hemorrhage (SAH) Incidence^a.

Measure	Mean (Range)	Annual Change, % (95% CI)	1980 Estimate (Range)	2010 Estimate (Range)	Annual Decrease in SAH Incidence per Unit Decrease, % (95% CI)
Systolic BP, mm Hg	134.9 (106.4 to 161.8)	−0.2 (−0.3 to −0.1)	120.4 (118.6 to 122.2)	114.6 (112.9 to 116.3)	7.1 (5.8 to 8.4)
Diastolic BP, mm Hg	79.1 (65.1 to 88.1)	0.01 (−0.02 to 0.04)	70.6 (69.5 to 71.6)	70.8 (69.8 to 71.7)	11.5 (8.8 to 14.3)
Smoking prevalence, %	19.3 (0.3 to 72.9)	−0.5 (−0.6 to −0.4)	26.5 (22.7 to 30.3)	11.9 (8.4. to 15.4)	2.4 (1.6 to 3.3)

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^{^a}

All analyses are adjusted for age and sex.

With every millimeter of mercury decrease in systolic blood pressure, the overall age-adjusted and sex-adjusted incidence of SAH declined by 7.1% (95% CI, 5.8-8.4) (Table 2) (Figure 3A). With every millimeter of mercury decrease in diastolic blood pressure, the overall age-adjusted and sex-adjusted incidence of SAH declined by 11.5% (95% CI, 8.8-14.3). With every percentage decrease in smoking prevalence, the overall age-adjusted and sex-adjusted incidence of SAH decreased by 2.4% (95% CI, 1.6-3.3) (Figure 3B). The limited number of data points for individual countries did not permit robust analyses on the association of blood pressure and smoking prevalence with SAH incidence by country, age, sex, and time period.

Figure 3. — A, Time trends in SAH incidence in all studies by midyear are presented irrespective of age and sex (black dots). The black line indicates the regression/time trend of SAH incidence with markers for mean estimated incidence for 1980 and 2010. The blue line indicates mean systolic blood pressure levels in studies included in the age-specific and sex-specific analyses, with markers for mean estimated systolic blood pressure levels for 1980 and 2010. B, Time trends in SAH incidence in all studies by midyear are presented irrespective of age and sex (black dots). The black line indicates the regression/time trend of SAH incidence with markers for mean estimated incidence for 1980 and 2010. The red line indicates smoking prevalence in studies included in the age-specific and sex-specific analyses, with markers for smoking prevalence in 1980 and 2010.

Discussion

The crude global incidence of SAH has declined by 40% between 1980 and 2010, but there is large variation of SAH incidence according to age, sex, region, time period, blood pressure, and smoking prevalence. Between 1980 and 2010, SAH incidence declined by 40.6% in Europe, 46.2% in Asia, and 14.0% in North America. The global decrease in SAH incidence paralleled a global decrease in mean blood pressure and smoking prevalence. In Japan, the SAH incidence increased by 59.1% over the last 3 decades. The higher SAH incidence in women older than 55 years was striking in Japan and no longer statistically significant in Europe after adjustment.

A 2014 meta-analysis on worldwide stroke incidence including 56 population-based studies⁸⁹—to our knowledge, the most recent—did not detect a decrease in crude SAH incidence between 1980 and 2008. However, the overall proportion of studies reporting specific data on aneurysmal SAH incidence in that study may have been too limited to permit robust analysis of time trends. For Finland, a country with a previously reported high SAH incidence, no studies fulfilled our inclusion criteria after 1990, and therefore we could not assess a change over time. A recent register-based Finnish study,³ which also did not fulfill our inclusion criteria, reported an age-standardized decrease in SAH incidence by 24% between 1998 and 2012 along with a simultaneous decrease in smoking prevalence by 30%. The crude SAH incidence for 2010 in Finland was estimated in that study to be 9.1 per 100 000 person-years.³ This incidence is lower than our current estimate for the pre-1990 studies (ie, 16.6 per 100 000 person-years), which suggests that the incidence has also declined in Finland. Nevertheless, the estimated incidence from this registry study is still higher than the current SAH incidence in other European countries in our data.

There are several potential explanations for our findings of a decline in global SAH incidence over the last decades. First, the global SAH incidence may have declined because of a parallel decline in blood pressure and smoking prevalence in the underlying populations. Because of the nature of our study, we cannot draw causal conclusions, but it is highly likely that the evident decrease in the global prevalence of 2 major risk factors for SAH resulted in the decline of its incidence.⁹⁰ For smoking alone, such an association has been recently reported in a registry-based incidence study from Finland.³ However, it remains uncertain why the SAH incidence in Japan has increased substantially, despite the concomitant global decline. Hypothetically, this could be a consequence of the distinctly higher crude prevalence of smoking in Japan (26.1%) compared with the global population (19.3%) in our data set. Unfortunately, the limited age-specific, sex-specific, midyear-specific, and country-specific SAH incidence data did not permit further regression analyses in this respect.

Second, preventive repair of unruptured intracranial aneurysms (UIAs) could have resulted in a subsequent decrease of SAH incidence in the underlying populations. However, we consider it unlikely as the sole explanation because of the enormous number of interventions that should have been performed to reach such a reduction; to achieve a 10% reduction in SAH incidence, at least 15 million UIAs should have been treated preventively (assuming a UIA prevalence of 3% in the adult population and 165 million UIAs worldwide). In the United States alone, only about 12 000 Medicare patients underwent preventive aneurysm treatment in 1 decade.⁹¹ Third, a decrease in the prevalence of UIAs over the past decades could have resulted in a decline of SAH incidence, but such a trend was not found in the most recent pooled analysis.⁹²

Fourth, one could argue that our data on SAH incidence time trends are explained by the trend of increased proportions of CT scanning over time, which was the main explanation for the decline in SAH incidence almost 2 decades ago.⁸ However, our sensitivity analyses underline that the decline in SAH incidence in our study is genuine and is only partially explained by the increased use of CT scanning over time, especially because of the generally high proportion of cranial imaging (mean percentage of CT scanning, 89.6%) in studies published after 1985. Theoretically, a change in incidence over time within a population may also be caused by a change in proportions of race/ethnicity within that population over time. However, because none of the populations where incidence was studied in several time periods provided data on change in race/ethnicity over time within the population, we were not able to further analyze this aspect.

Strengths and Limitations

A strength of our study is that it comprises, to our knowledge, the most rigorous and geographically and chronologically dispersed data set on SAH incidence specifically and solely derived from population-based studies to date. We had strict inclusion criteria to ensure detection of patients dying before reaching the hospital. Since we also found little variation in case ascertainment and diagnostic criteria in our meta-analysis and since the proportion of patients who die suddenly is around 12%, it is unlikely that the large regional variation in incidence found in this systematic review is explained only by differences in case finding and diagnostic criteria between the studies.⁹³ Furthermore, our meta-analysis is the first to our knowledge to find an association of time trends of blood pressure and smoking prevalence with SAH incidence.

Our study had limitations. There were limited population-based data on SAH incidence for most of Africa and large Eastern populations, including China, Russia, and India. We chose the population-based study design over a registry-based design in favor of high-quality data and under the premise that study populations are representative of the population of that country. However, variations in SAH incidence on a regional level may exist, which may not be captured by the study population that represented a specific country. Further, a limitation of such an ecological study design is that one cannot study causal relationships on an individual patient level, and such a design harbors the risk of confounding relations. We minimized the risk of confounding by means of adjusted regression analyses. Nevertheless, we underline that our findings are no more than associations and that causal relationships between decline in blood pressure or smoking prevalence and SAH incidence can only be accurately studied when quantitative data for these risk factors become available on a population-based or individual patient level. Finally, not all patients with SAH included in the parent studies underwent angiography. On the one hand, this may have led to an overestimation of the incidence because instances of nonaneurysmal SAH may have been included. On the other hand, restricting to angiographically confirmed aneurysmal SAH inevitably induces an underestimation of the actual incidence because not all patients reach hospitals alive, and in the pre-CT angiography era, catheter angiography was only done if the patient was eligible for aneurysm treatment.

Conclusions

The association we found between blood pressure and smoking prevalence reduction with decrease in SAH incidence further supports control of these risk factors to reduce SAH burden. Future studies should address the regional differences in SAH incidence and its decline, regional differences in age-specific and sex-specific incidences, and their association with actual quantitative data on smoking. Explanations for these differences may help to further decrease SAH incidence. The reasons for the increasing incidence of SAH in Japan remain unclear.

Supplement.

eTable 1. Summary of all 75 included studies and 84 study periods, according to ascending midyear of study.

eTable 2. Characteristics of the overall and age-specific and sex-specific datasets.

eTable 3. Crude SAH incidence with 95% CIs and risk ratios for SAH in the age-specific and sex-specific dataset.

eTable 4. Overall and age-specific risk ratios in women vs men in the age-specific and sex-specific dataset (34 study periods).

eTable 5. Time trends in SAH incidence in the in the age-specific and sex-specific dataset (34 study periods).

eTable 6. Estimated blood pressures in 1980 and 2010 for women and men aged 45-54 years and 55-74 years including annual change from 1977 to 2014.

eFigure 1. Selection of studies.

eFigure 2. Regional time trends for studies reporting on consecutive SAH incidence for the same study population.

eFigure 3. Crude incidence of SAH in age-specific and sex-specific dataset overall, in Europe, and in Japan only.

Click here for additional data file.^{(629.4KB, pdf)}

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplement.

eTable 1. Summary of all 75 included studies and 84 study periods, according to ascending midyear of study.

eTable 2. Characteristics of the overall and age-specific and sex-specific datasets.

eTable 3. Crude SAH incidence with 95% CIs and risk ratios for SAH in the age-specific and sex-specific dataset.

eTable 4. Overall and age-specific risk ratios in women vs men in the age-specific and sex-specific dataset (34 study periods).

eTable 5. Time trends in SAH incidence in the in the age-specific and sex-specific dataset (34 study periods).

eTable 6. Estimated blood pressures in 1980 and 2010 for women and men aged 45-54 years and 55-74 years including annual change from 1977 to 2014.

eFigure 1. Selection of studies.

eFigure 2. Regional time trends for studies reporting on consecutive SAH incidence for the same study population.

eFigure 3. Crude incidence of SAH in age-specific and sex-specific dataset overall, in Europe, and in Japan only.

Click here for additional data file.^{(629.4KB, pdf)}

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PERMALINK

Worldwide Incidence of Aneurysmal Subarachnoid Hemorrhage According to Region, Time Period, Blood Pressure, and Smoking Prevalence in the Population

Nima Etminan, MD

Han-Sol Chang, MD

Katharina Hackenberg, MD

Nicolien K de Rooij, MD, PhD

Mervyn D I Vergouwen, MD, PhD

Gabriel J E Rinkel, MD, FRCPE

Ale Algra, MD, PhD

Key Points

Question

Findings

Meaning

Abstract

Importance

Objective

Data Sources

Study Selection

Data Extraction and Synthesis

Main Outcomes and Measures

Results

Conclusions and Relevance

Introduction

Methods

Search Strategy and Selection Criteria

Data Extraction

Data Analyses

Results

Figure 1. Crude Subarachnoid Hemorrhage (SAH) Incidence by Country and Midyear in Europe.

Figure 2. Crude Subarachnoid Hemorrhage (SAH) Incidence by Continent, Country, and Midyear.

SAH Incidence by Region and Time Trends

Table 1. Subarachnoid Hemorrhage (SAH) Incidence, Risk Ratios (RRs), Midyear Range, and Time Trends by Region.

SAH Incidence Stratified by Age, Sex, Region, and Time Trends

Association of Blood Pressure Levels and Smoking Prevalence With SAH Incidence by Region and Time Trends

Table 2. Association of Mean Blood Pressure (BP) and Smoking Prevalence Time Trends With Subarachnoid Hemorrhage (SAH) Incidencea.

Figure 3. Association of Time Trends of Blood Pressure and Smoking Prevalence With Subarachnoid Hemorrhage (SAH) Incidence.

Discussion

Strengths and Limitations

Conclusions

References

Associated Data

Supplementary Materials

ACTIONS

PERMALINK

RESOURCES

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Links to NCBI Databases

Table 2. Association of Mean Blood Pressure (BP) and Smoking Prevalence Time Trends With Subarachnoid Hemorrhage (SAH) Incidence^a.