Case fatality and functional outcome after spontaneous subarachnoid haemorrhage: A systematic review and meta-analysis of time trends and regional variations in population-based studies

Abstract

Introduction:

A previous systematic review of population-based studies from 1973 to 2002 found a decrease in case fatality for spontaneous subarachnoid haemorrhage, but could not find a sufficient number of studies to assess changes in functional outcome. Since then, treatment has advanced distinctly. We assessed whether case fatality has decreased further and whether functional outcome has improved.

Patients and methods:

We searched PubMed and Web of Science for new population-based studies using the same criteria as in our previous systematic review. We assessed changes in case fatality and functional outcome over time using linear regression.

Results:

We included 24 new studies with 827 patients and analysed 9542 patients described in 62 study periods between 1973 and 2017. Case fatality decreased by 0.3% (95% CI: −0.7 to 0.1) per year. In a sensitivity analysis excluding studies that did not provide 1-month outcome and outliers, the age and sex-adjusted decrease was 0.1% per year (95% CI: −0.9 to 0.6). The mean case fatality rate decreased from 47% (95% CI: 31–63) in the 1970s to 35% (95% CI: 30–39) in the 1990s, and remained stable in the 2000s (34%; 95% CI: 27–41) and 2010s (38%; 95% CI: 15–60). In 15 studies, the mean proportion of patients living independently increased by 0.2% per year (95%CI: −0.7 to 1.1) and the mean was 45% (95% CI: 39–50) in six studies that reported outcome after 12 months.

Discussion and conclusion:

From 1973 to 2017, the case-fatality rate of spontaneous subarachnoid haemorrhage declined overall by 13.5%, but remained stable over the last two decades. The data on time trends in functional outcome were inconclusive.

Graphical abstract

Keywords

Subarachnoid haemorrhage stroke case fatality functional outcome aneurysm

Introduction

Patients with spontaneous subarachnoid haemorrhage (SAH) have a poor prognosis. The majority dies within the initial days to weeks after the haemorrhage or remains dependent on help from others. In a previous meta-analysis of population-based studies on the outcome after spontaneous subarachnoid haemorrhage, the case fatality rate (CFR) decreased between 1973 and 2002 and was lower in Japan than in other regions in the world.¹ There were only a few studies that assessed the functional outcome of patients, which did not permit to determine whether the improved survival rate resulted in more patients becoming dependent on others or regaining their independence.

Since the previous publication of this systematic review, the management of patients with SAH has improved considerably. In 2002 the results of ISAT were published, showing a 7% absolute decrease in risk of poor outcome for coiling versus surgical clipping.² The results of this trial led to a steady increase in SAH patients treated by coiling.^3,4 Centralisation of care and development of comprehensive stroke centres may also have improved outcome, since large volume centres have better outcomes.⁵ This may in part be explained by higher proportions of patients treated endovascularly in such centres.⁶ We therefore updated the systematic review to assess whether case fatality rates have declined further and at a higher pace, and whether this concurs with an increased proportion of patients having a good clinical recovery. Further, we were interested to see whether we could find other regional differences in outcome after SAH than in the previous version.

Methods

Search strategy and selection criteria

Using the same literature search methods as in the previous review,¹ we updated the literature search in PubMed from July 2007 onwards up until May 2022. We also expanded our search and included a search in Web of Science for the same time period. We used the following keywords: (‘subarachnoid he[a]morrhage’) and ‘outcome’ or ‘mortality’ or ‘case fatality’ or ‘population’ or ‘epidemiology’) and (‘2007/7/1’; ‘2022/05/01’). Also: (‘stroke’) and ‘outcome’ or ‘mortality’ or ‘case fatality’ or ‘population’ or ‘epidemiology’) and (‘2007/7/1’; ‘2022/05/01’) (Figure 1).

Figure 1.

Preferred reporting items for systematic reviews and meta-analyses flow diagram.

For combinations with the keyword ‘stroke’, the reference list including the abstracts was downloaded. The key words ‘subarachnoid he[a]morrhage’ or ‘SAH’ were then searched in titles and abstracts using the Paperpile reference management software (Google Inc. 2022). Studies without either of these terms in the title or abstract were not considered for further evaluation. There was no language restriction.

Additional studies were identified by cross-checking the reference lists of matching studies. Finally, the available studies were compared with the personal database of one of the authors (GJER). This collection was prospectively built up over the last 25 years by daily searches in PubMed using the key words ‘subarachnoid h[a]emorrhage’, ‘aneurysm’ and ‘arteriovenous malformation’.

The inclusion criteria were as follows: (1) The study was published between 1965 and May 2022. (2) The study period did not exceed 10 years unless separate results were reported for each decade. (3) The study design was prospective and population-based and the study population was representative of the general population. All hospitals that provided care to the study population and all death certificates were reviewed or data on deaths were examined, or data on deaths of patients who were not hospitalised were obtained from the medical examiner. (4) The upper age limit for the study population was no younger than 74 years, and the lower limit was no older than 25 years. (5) In population-based studies of stroke in general, SAH was treated as a separate entity with defined criteria, and the case fatality rate or case morbidity was included or could be calculated. (6) The diagnosis of SAH could be verified for study purposes. (7) The incidence of SAH in the population studied was at least 3 per 100,000.

Studies from the previous review had the same inclusion criteria and were therefore eligible for inclusion (Figure 1). Since we applied the same methods as in the previous versions of the review, we did not pre-register the study protocol.

Statistical analysis

We calculated 95% confidence intervals (CI) for case fatality rates if these were not provided in the parent articles. When studies reported case fatality at multiple time points, 1-month outcome was used for the analysis. Linear regression weighted by the inverse of the standard error was performed. The standard error of the case fatality rate for each study was used to analyse the relationship between the case fatality rate and the mid-calendar year of the study. The results are expressed as the percentage change in the case fatality rate per calendar year with the corresponding 95% CI. In pre-defined sensitivity analyses we excluded studies with strikingly low or high case fatality rates, studies from regions with lower CFR than elsewhere and studies that did not provide case fatality data at 1 month. For those studies that provided data on age and sex, we used linear regression models to adjust for age and sex differences between studies.

Studies were also grouped by continent and the case fatality rates per continent were compared to those of each of the other continents. Linear regression for regional differences was performed and the single-factor analysis of variance was calculated using Scheffè’s post hoc test with correction of the alpha error. We performed a separate analysis for populations wherein case fatality was studied in two or more periods, separated by more than 5 years, updating a previous meta-analysis.⁷ We used linear regression analysis and the results are expressed as the absolute percentage change in case fatality per calendar year.

When studies provided data on clinical outcome at several time points, we used the time point that was reported by most studies (12 months), to assess changes in case morbidity over time. We dichotomised functional outcome into being able to live independently for help from others (modified Rankin Scale of <3 or Glasgow Outcome Scale > 3) versus being dependent on help for activities of daily life from others.

The statistical analyses were performed using MedCalc software (version 19.6) and SAS software (version 9.4). The random effect model was used in the meta-analysis. Forest plots were created to visualise the 95% CI results. A p-value of <.05 was considered statistically significant.

Results

We identified 24 new studies, which reported on 827 patients. One study from the previous systematic review was excluded, since an updated version of this study was available (Figure 2). In total, we analysed 56 studies, which reported on 9542 SAH patients described in 62 study periods between 1973 and 2017 (Table 1).^8–62 Most studies (n = 34; 57%) were conducted in Europe, and most patients were included (n = 5976) in Asia. A detailed list of studies per region and their main characteristics is provided in Supplemental Table 1. The median mid-calendar year of all studies was 1997.

Figure 2.

Case fatality rates per study.

Table 1.

Study characteristics.

··: data not available; SAH: subarachnoid haemorrhage; DBA: dead before arrival; CH: clinical history confirmed by lumbar puncture, CT or MRI scan, angiography, autopsy, or surgery; Guy’s: criteria from Guy’s Hospital, London, UK; NSS: National Stroke Survey; NINDS: National Institute of Neurological Disorders and Stroke; A: autopsy report; C: coroner; D: death certificates; E: emergency department; G: general practitioner; H: hospital records; M: media attention for the study during the recruitment phase; N: nursing home or rehabilitation centre; O: outpatient clinic; R: radiology requests; V: volunteers in door to door surveys.

Newly added studies are highlighted in colour.

Percentage of all stroke patients.

Outcome after 3 weeks.

Outcome after 2 months.

Outcome after 3 months.

Thirty-two studies reported on the age of the SAH patients. The overall mean age was 58 years (SD ±4.4) and was stable over time (Supplemental Table 2). In the 41 studies that reported on sex, the overall female proportion was 60%. Also the proportion of women was stable over time (Supplemental Table 2). There were no new studies that reported on age for men and women separately. The mean age ranged from 54 to 60 in different regions and the female sex ratio ranged between 56% and 67% over the different regions (Supplemental Table 1). None of the included studies separated patients with a proven aneurysm as a cause of the SAH from those without a proven aneurysm.

Case fatality and time-trends

Case fatality was assessed at 3 weeks in one study, at 1 month in 56 studies, at 2 months in one study and at 3 months in two studies. Case fatality ranged from 0% to 75% (Figure 2). The funnel plot shows three studies that break the symmetry of the plot (Supplemental Figure 1).

The overall reduction in case fatality was 13.5% (95% CI −29.6 to 2.7) between 1973 and 2017. Weighted linear regression analysis of all studies showed that case fatality rate decreased by 0.3% per year (95% CI −0.7 to 0.1). The mean case fatality rate from 1970 to 1979 was 47% (95% CI 31–63), from 1980 to 1989 it was 45% (95% CI 36–53), from 1990 to 1999 it was 35% (95% CI 30–39), from 2000 to 2009 it was 34% (95% CI 27–41) and 38% (95% CI 15–60) from 2010 to 2019 (Figure 3).

Figure 3.

Case fatality rates per decade. Case fatality rates per decade of the studies. Squares are means and bars are 95% CI.

After excluding studies with strikingly low or high case fatality rates (0%, 8.3% and 75%), case fatality ranged from 17% to 67% and decreased by 0.4% per year (95% CI −0.7 to −0.1). Further exclusion of studies that did not provide case fatality data at 1 month did not change the results (case fatality rate decreased by 0.4% per year (95% CI −0.7 to −0.1). Of all 9488 patients, 5711 came from three Japanese studies, which were reported in the previous meta-analysis with a median case fatality of 26.7%. After further excluding these Japanese studies, weighted linear regression analysis showed that the case fatality rate decreased by 0.5% per year (95% CI −0.8 to −0.1). Additional adjustment for age and sex in this subset led to a decrease of 0.3% per year (95% CI −1.1 to 0.4).

The mean case fatality rate without exclusion of specific studies and without adjustment of age and sex was in Europe 37% (95% CI 32–42), in Asia 34% (95% CI 28–40), in Australia and New Zealand 39% (95% CI 32–46), in North America 32% (95% CI n/a) and in Central and South America 41% (95% 24–59). The mean case fatality rate in Asia, excluding all Japanese studies, was 38% (95% CI 31–45). Figure 4 shows separated case fatality rates per continent. Linear regression analysis showed no significant continental differences in the case fatality rates.

Figure 4.

(a) Regional differences in case fatality. Boxes = interquartile range. Lines median. Bars = range. Squares = mean. (b) World heat map showing regional case fatality throughout the study period from 1973 to 2017. Each colour in a circle presents a distinct study or study period.

Two additional studies that assessed case fatality rates within a population at different time points were found since the previous review.⁷ The absolute risk reduction per year in Martinique from 1998 until 2012 was 0.5%, in Örebro (Sweden) from 1999 until 2017 it was 1.1%. The overall absolute risk reduction per year of nine studies that assessed case fatality rates at different timepoints within a population included in this systematic review was 0.9% (95% CI 0.4–1.5).

Functional outcome

Two studies reported functional outcome at 1 month, one study at 3 months, three studies at 6 months, four studies at 12 months and one at 44 and 60 months. Two studies reported functional outcomes at multiple time points (one ranging from one to 60 months and another one to 12 months). The total number of articles reporting on functional outcome was 15, which described 15 study periods including 2825 patients (Table 2); 8 new articles with 399 patients reporting on functional outcome were included. One study did not report the proportion of patients remaining dependent but only the combined proportion of death and being dependent,⁶¹ and one other reported only the median modified Rankin Scale without proportions of independent living patients and dependent living patients.⁶³

Table 2.

Functional outcome.

Study	Mid-year/region	Follow-up (months)	Stroke or SAH study	Number of SAH patients	Case fatality	mRS dependent	mRS independent
Lund¹¹	Sweden, 1983	2–12	SAH	78	37%	14%	49%
Oxfordshire¹²	UK, 1984	12	Stroke	33	48%	12%	39%
King County, WA¹⁶	USA, 1988	12	SAH	171	38%	11%	51%
Arcadia²⁵	Greece, 1994	1	Stroke	14	57%	7%	36%
Kumamoto (hospital)³¹	Japan, 1998	3	SAH	2115	25%	20%	55%
L’Aquila⁴⁰	Italy, 1996	12	Stroke	118	45%	10%	45%
Iquique³⁷	Chile, 2001	6	Stroke	15	46%	8%	46%
Auckland⁶¹	New Zealand, 2002	60	Stroke	27	..	17%^a	83%
Oxford⁴⁶	UK, 2005	12	Stroke	38	50%	11%	39%
Joinville⁴⁷	Brazil, 2005	6	Stroke	55	46%	2%	52%
Dublin⁴⁸	North Ireland, 2006	1	Stroke	26	46%	23%	31%
Aosta⁴⁹	Italy, 2006	44	Stroke	44	0%	27%	73%
Joinville⁶²	Brazil, 2009	12	Stroke	27	52%	4%	44%
Evros⁶³	Greece, 2011	12	Stroke	31	45%	6 (2–6)^b	..
Ñuble⁵⁷	Chile, 2015	6	Stroke	33	39%	12%	49%

SAH: subarachnoid haemorrhage; ··: data not available; mRS: modified Rankin Scale.

Dependent or died.

Median mRS and interquartile range.

Studies with a follow-up time of 12 months reported a range of the proportion of patients living independently from 39% to 51% and those remaining dependent from 4% to 14%. In the linear regression analysis of all studies from 1983 to 2015, the proportion of patients living independently increased by 0.2% (95% CI −0.7 to 1.1%) per year (Figure 5), and case morbidity did not change (0.0%) (95% CI −0.5% to 0.5%). Age and sex data were not available for functional outcome and therefore we could not adjust analyses on functional outcome for these factors.

Figure 5.

Mid-calendar year and proportions of patients who regained independence for daily life activities for studies reporting on functional outcome after spontaneous subarachnoid haemorrhage. Linear regression demonstrates a trend towards increase in the proportion of patients living independently after subarachnoid haemorrhage by 0.2% per year (95% CI −0.7 to 1.1).

Discussion

This systematic review included 24 new studies and one and a half decades of observations. The overall case fatality decreased but to a lesser extent than in the previous version. The decline in case fatality rate occurred mainly in the last decades of the 20th century, and seems to level off in the last two decades. The number of studies reporting on functional outcomes doubled in comparison with the previous version of the review. There was a trend towards an increase in the proportions of SAH patients who regained independence for activities of daily living, and no sign of increasing proportions of patients who remained dependent, but the data on the functional outcome were overall inconclusive.

In contrast to our finding of a stable case fatality rate over the last two decades, a hospital-based study found a statistically significant decrease in case fatality rates between 1999–2002 and 2009–2012, which was mainly attributed to a decrease in in-hospital rebleeding.⁶⁴ This hospital-based study did not include deaths before arrival the hospital. Because these sudden deaths from SAH are responsible for 10% to 15% of overall case fatality in SAH patients,⁶⁵ not taking into account these sudden deaths may in part explain the difference between this hospital-based study and population-based studies on case fatality rates over the last decades. A registry-based study in Finland, which captures also a large part of the sudden deaths from SAH, found an overall decrease in case fatality between 1998 and 2017, but when comparing the periods 1998–2000 and 2015–2017, case fatality rates decreased in women but increased in men, in particular in men older than 65 years of age.⁶⁶ In this registry-based study the proportion of women gradually increased during the study period, while the CFR decreased merely in women. In this systematic review the proportion of women did not increase and point estimates even suggested a decrease in the last two decades. Thus, the lack of a further decline in the CFR over the last two decades in our review may be partly explained by the stable proportion of women in the parent population-based studies.

In the subset of studies that assessed case fatality rates within one population at different time points we also found an overall decrease in case fatality over time, which strengthens our findings in the entire set of population-based studies. The two new studies with multiple assessments over time both had the first assessment in the 1990s and the newest in the 2010s. In both, the point estimates suggest a decline in case fatality rate over time. Similar findings were done in a recent systematic review on study populations with assessment of case fatality at different endpoints.⁶⁷ This study used different inclusion criteria and included 16 populations, 14 of which showed a decline in case fatality rates over time. Comparable to our findings in the overall data set, the decline in this review seemed stronger over the last two decades of the 20th century than over the first two decades of the 21st century.

There are several explanations for a lack of further decrease in case fatality on a population-based level over the last two decades. First, while the overall incidence of SAH is declining, the incidence of hospitalised elderly patients increases.^68,69 It is a challenge to improve outcomes in older patients, as underlined in the Finnish registry study.⁶⁶ Second, we hypothesised that the greater availability of coiling had led to a decrease in case fatality. In a study on 7658 aneurysmal SAH patients from 22 tertiary care hospitals from Europe, USA, and Australia, endovascular coiling did not result in lower 14-days case-fatality rates than neurosurgical clipping.⁷⁰ In clinical cohorts from the same study, also 90 days case fatality rates were higher after coiling than after clipping, but the proportion of patients with poor functional outcome were lower after coiling than after clipping. Thus, in clinical practice, that is, outside trials, the advent of coiling may have more impact on clinical outcome than on case fatality. Moreover, it is unclear whether new endovascular treatment options are widely used in all areas represented in this systematic review. Third, treatment in high-volume centres reduces case fatality in SAH patients,⁵ but data on (change in) the volume of the treatment centres was not available in the included studies. Lack of regional centralisation may have influenced results. Another explanation is that a plateau has been reached and no further reduction in CFR can be achieved. Still, around 10%–15% of patients with subarachnoid haemorrhage die before reaching the hospital, and even the best medical and surgical treatment cannot change the fate of these patients. The improvement achieved for patients admitted at hospitals may therefore not translate to an improvement of case fatality rates on a population-based level.

The range of patients living independently was very high. This may relate to different definitions of independent living between the studies or to differences between countries when a patient is considered able to live independently. Whatever the cause is, the wide range hampers proper assessment of the change in functional outcomes over time, even though the number of patients included in this analysis has doubled compared to the previous review. We also did not find studies with assessment of functional outcomes at different time points within one population, which further precludes assessment regarding time trends.

Our study has several strengths: We could include a considerable number of new and recent prospective, population-based studies into the meta-analyses, which enabled us to further estimate time trends of the case fatality rate in spontaneous SAH as well as functional outcomes over nearly five decades. Moreover, we used established, robust case-finding methods for the review. Our meta-analysis also has limitations. First, even though the number of new studies is large, the number of patients with SAH included in the new studies are in general smaller than in many studies already included in the previous version of the review. Second, for many confounders such as age, sex, or other potential risk factors for adverse functional outcomes, no additional data were available. Thus, we could not adjust for these factors. Both the relatively small numbers of patients and the lack of ability to adjust for risk factors are in part explained by the fact that most newly identified studies are population-based studies on stroke in general, with SAH as one of the subsets, instead of population-based studies on SAH in general. In the majority of studies on stroke in general, age and sex-specific data were not available for SAH patients separately. In both the previous and current systematic review we could not differentiate between aneurysmal and non-aneurysmal SAH because the underlying studies did not provide specific outcome data. We assume that most cases were of aneurysmal origin, but advocate that future studies report on the proportion of patients with proven aneurysms and separate outcomes for those with and without a proven aneurysm as cause for the SAH, as outcomes may be different.⁷¹

The lack of a further decline in case fatality on a population-based level over the last two decades, despite the overall reduction in case fatality over the last five decades, warrants further study. Although sudden deaths from SAH will prove difficult to eliminate, insight into the care provided and the case fatality per region could facilitate implementing strategies that proved successful in some regions into other regions. If further studies confirm the lack of further decline in case fatality, this would imply that further reduction in case fatality can only be achieved through prevention of aneurysm development and rupture. Future studies should also focus on functional outcome, using established outcome scales to facilitate comparability between the studies.

Supplemental Material

sj-docx-2-eso-10.1177_23969873241232823 – Supplemental material for Case fatality and functional outcome after spontaneous subarachnoid haemorrhage: A systematic review and meta-analysis of time trends and regional variations in population-based studies

Supplemental material, sj-docx-2-eso-10.1177_23969873241232823 for Case fatality and functional outcome after spontaneous subarachnoid haemorrhage: A systematic review and meta-analysis of time trends and regional variations in population-based studies by Andreas Ziebart, Judith Dremel, Svetlana Hetjens, Dennis J Nieuwkamp, Francisca HH Linn, Nima Etminan and Gabriel JE Rinkel in European Stroke Journal

Supplemental Material

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Supplemental material, sj-docx-3-eso-10.1177_23969873241232823 for Case fatality and functional outcome after spontaneous subarachnoid haemorrhage: A systematic review and meta-analysis of time trends and regional variations in population-based studies by Andreas Ziebart, Judith Dremel, Svetlana Hetjens, Dennis J Nieuwkamp, Francisca HH Linn, Nima Etminan and Gabriel JE Rinkel in European Stroke Journal

Supplemental Material

sj-jpg-1-eso-10.1177_23969873241232823 – Supplemental material for Case fatality and functional outcome after spontaneous subarachnoid haemorrhage: A systematic review and meta-analysis of time trends and regional variations in population-based studies

Supplemental material, sj-jpg-1-eso-10.1177_23969873241232823 for Case fatality and functional outcome after spontaneous subarachnoid haemorrhage: A systematic review and meta-analysis of time trends and regional variations in population-based studies by Andreas Ziebart, Judith Dremel, Svetlana Hetjens, Dennis J Nieuwkamp, Francisca HH Linn, Nima Etminan and Gabriel JE Rinkel in European Stroke Journal

Footnotes

Acknowledgements

None

Author contributions

Drs Rinkel and Ziebart conceptualised and designed the study. Drs Rinkel and Etminan coordinated and supervised the systematic review. Drs Ziebart and Dremel selected the articles, extracted the data. Dr Hetjens performed the data analysis and assessed the risk of bias. Drs Ziebart and Rinkel drafted the initial version of the manuscript. All authors critically reviewed and approved the final manuscript as submitted.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical approval

Not applicable.

Informed consent

Not applicable.

Guarantor

Gabriel JE Rinkel

ORCID iD

Andreas Ziebart

Supplemental material

Supplemental material for this article is available online.

References

Nieuwkamp

Setz

Algra

, et al. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol 2009; 8: 635–642.

Molyneux

Kerr

Stratton

, et al.; International Subarachnoid Aneurysm Trial (ISAT) Collaborative Group. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 2002; 360: 1267–1274.

Lin

Cahill

Frerichs

, et al. Treatment of ruptured and unruptured cerebral aneurysms in the USA: a paradigm shift. J Neurointerv Surg 2018; 10: i69–i76.

SVIN COVID-19 Global SAH Registry. Global impact of the COVID-19 pandemic on subarachnoid haemorrhage hospitalisations, aneurysm treatment and in-hospital mortality: 1-year follow-up. J Neurol Neurosurg Psychiatry 2022; 93: 1028–1038.

Lindgren

Burt

Bragan Turner

, et al. Hospital case-volume is associated with case-fatality after aneurysmal subarachnoid hemorrhage. Int J Stroke 2019; 14: 282–289.

Rush

Romano

Ashkanani

, et al. Impact of hospital case-volume on subarachnoid hemorrhage outcomes: a nationwide analysis adjusting for hemorrhage severity. J Crit Care 2017; 37: 240–243.

Lovelock

Rinkel

Rothwell

PM.

Time trends in outcome of subarachnoid hemorrhage population-based study and systematic review. Neurology 2010; 74: 1494–1501.

Numminen

Kotila

Waltimo

, et al. Declining incidence and mortality rates of stroke in Finland from 1972 to 1991. Results of three population-based stroke registers. Stroke 1996; 27: 1487–1491.

Herman

Leyten

van Luijk

, et al. Epidemiology of stroke in Tilburg, the Netherlands. The population-based stroke incidence register: 2. Incidence, initial clinical picture and medical care, and three-week case fatality. Stroke 1982; 13: 629–634.

10.

Truelsen

Bonita

Duncan

, et al. Changes in subarachnoid hemorrhage mortality, incidence, and case fatality in New Zealand between 1981-1983 and 1991-1993. Stroke 1998; 29: 2298–2303.

11.

Ljunggren

Säveland

Brandt

, et al. Aneurysmal subarachnoid hemorrhage. Total annual outcome in a 1.46 million population. Surg Neurol 1984; 22: 435–438.

12.

Bamford

Sandercock

Dennis

, et al. A prospective study of acute cerebrovascular disease in the community: the Oxfordshire Community Stroke Project–1981-86. 2. Incidence, case fatality rates and overall outcome at one year of cerebral infarction, primary intracerebral and subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry 1990; 53: 16–22.

13.

Norrving

Löwenhielm

Epidemiology of stroke in lund-orup, Sweden, 1983-85. Incidence of first stroke and age-related changes in subtypes. Acta Neurol Scand 1988; 78: 408–413.

14.

Chen

Román

, et al. Stroke in China (sino-MONICA-Beijing study) 1984–1986. Neuroepidemiology 1992; 11: 15–23.

15.

Jakovljević

Sivenius

Sarti

, et al. Socioeconomic inequalities in the incidence, mortality and prognosis of subarachnoid hemorrhage: the FINMONICA Stroke Register. Cerebrovasc Dis 2001; 12: 7–13.

16.

Longstreth

Nelson

Koepsell

, et al. Clinical course of spontaneous subarachnoid hemorrhage: a population-based study in King County, Washington. Neurology 43(4): 712.

17.

Ricci

Celani

La Rosa

, et al. SEPIVAC: a community-based study of stroke incidence in Umbria, Italy. J Neurol Neurosurg Psychiatry 1991; 54: 695–698.

18.

Anderson

Jamrozik

Broadhurst

, et al. Predicting survival for 1 year among different subtypes of stroke. Results from the Perth Community Stroke Study. Stroke 1994; 25: 1935–1944.

19.

D’Alessandro

Bottacchi

Di Giovanni

, et al. Temporal trends of stroke in Valle d’Aosta, Italy. Incidence and 30-day fatality rates. Neurol Sci 2000; 21: 13–18.

20.

Kimura

Takishita

Muratani

, et al. Demographic study of first-ever stroke and acute myocardial infarction in Okinawa, Japan. Intern Med 1998; 37: 736–745.

21.

Feigin

Wiebers

Nikitin

, et al. Stroke epidemiology in Novosibirsk, Russia: a population-based study. Mayo Clin Proc 1995; 70: 847–852.

22.

Lauria

Gentile

Fassetta

, et al. Incidence and prognosis of stroke in the Belluno province, Italy. First-year results of a community-based study. Stroke 1995; 26: 1787–1793.

23.

Kozák

Hayashi

Trends in the incidence of subarachnoid hemorrhage in Akita Prefecture, Japan. J Neurosurg 2007; 106: 234–238.

24.

Khan

Engstrom

Jerntorp

, et al. Seasonal patterns of incidence and case fatality of stroke in Malmo, Sweden: the STROMA study. Neuroepidemiology 2005; 24: 26–31.

25.

Vemmos

Bots

Tsibouris

, et al. Prognosis of stroke in the south of Greece: 1 year mortality, functional outcome and its determinants: the Arcadia Stroke Registry. J Neurol Neurosurg Psychiatry 2000; 69: 595–600.

26.

Ellekjær

Holmen

Indredavik

, et al. Epidemiology of stroke in Innherred, Norway, 1994 to 1996. Incidence and 30-day case-fatality rate. Stroke 1997; 28: 2180–2184.

27.

Kolominsky-Rabas

Sarti

Heuschmann

, et al. A prospective community-based study of stroke in Germany–the Erlangen Stroke Project (ESPro): incidence and case fatality at 1, 3, and 12 months. Stroke 1998; 29: 2501–2506.

28.

Di Carlo

Inzitari

Galati

, et al. A prospective community-based study of stroke in Southern Italy: the Vibo Valentia Incidence of Stroke Study (VISS). Cerebrovasc Dis 2003; 16: 410–417.

29.

Thrift

Dewey

Macdonell

RAL

, et al. Incidence of the major stroke subtypes: initial findings from the North East Melbourne stroke incidence study (NEMESIS). Stroke 2001; 32: 1732–1738.

30.

X. 25 ext Across Group, Hankey

Jamrozik

. 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 2000; 31: 1843–1850.

31.

Hamada

Morioka

Yano

, et al. Incidence and early prognosis of aneurysmal subarachnoid hemorrhage in Kumamoto Prefecture, Japan. Neurosurg 2004; 54: 31–37.

32.

Smadja

Cabre

May

, et al.; ERMANCIA Study Group. ERMANCIA: epidemiology of stroke in Martinique, French West Indies: Part I: methodology, incidence, and 30-day case fatality rate. Stroke 2001; 32: 2741–2747.

33.

Stegmayr

Eriksson

Asplund

Declining mortality from subarachnoid hemorrhage: changes in incidence and case fatality from 1985 through 2000. Stroke 2004; 35: 2059–2063.

34.

Zhang

L-F

Yang

Hong

, et al. Proportion of different subtypes of stroke in China. Stroke 2003; 34: 2091–2096.

35.

Appelros

Nydevik

Seiger

, et al. High incidence rates of stroke in Orebro, Sweden: further support for regional incidence differences within Scandinavia. Cerebrovasc Dis 2002; 14: 161–168.

36.

Syme

Byrne

Chen

, et al. Community-based stroke incidence in a Scottish population: the Scottish Borders Stroke Study. Stroke 2005; 36: 1837–1843.

37.

Lavados

Sacks

Prina

, et al. Incidence, 30-day case-fatality rate, and prognosis of stroke in Iquique, Chile: a 2-year community-based prospective study (PISCIS project). Lancet 2005; 365: 2206–2215.

38.

Tsiskaridze

Djibuti

van Melle

, et al. Stroke incidence and 30-day case-fatality in a suburb of Tbilisi: results of the first prospective population-based study in Georgia. Stroke 2004; 35: 2523–2528.

39.

Vibo

Korv

Roose

The Third Stroke Registry in Tartu, Estonia, from 2001 to 2003. Acta Neurol Scand 2007; 116: 31–36.

40.

Sacco

Totaro

Toni

, et al. Incidence, case-fatalities and 10-year survival of subarachnoid hemorrhage in a population-based registry. Eur Neurol 2009; 62: 155–160.

41.

Sarker

Heuschmann

Burger

, et al. Predictors of survival after haemorrhagic stroke in a multi-ethnic population: the South London Stroke Register (SLSR). J Neurol Neurosurg Psychiatry 2008; 79: 260–265.

42.

Thrift

Dewey

Sturm

, et al. Incidence of stroke subtypes in the North East Melbourne Stroke Incidence Study (NEMESIS): differences between men and women. Neuroepidemiology 2009; 32: 11–18.

43.

Correia

Magalhães

Silva

, et al. Stroke types in rural and urban northern Portugal: incidence and 7-year survival in a community-based study. Cerebrovasc Dis Extra 2013; 3: 137–149.

44.

Islam

Anderson

Hankey

, et al. Trends in incidence and outcome of stroke in Perth, Western Australia during 1989 to 2001: the Perth Community Stroke Study. Stroke 2008; 39: 776–782.

45.

Manobianca

Zoccolella

Petruzzellis

, et al. Low incidence of stroke in southern Italy: a population-based study. Stroke 2008; 39: 2923–2928.

46.

Luengo-Fernandez

Paul

Gray

, et al.; Oxford Vascular Study. Population-based study of disability and institutionalization after transient ischemic attack and stroke: 10-year results of the Oxford Vascular Study. Stroke 2013; 44: 2854–2861.

47.

Cabral

Goncalves

ARR

Longo

, et al. Incidence of stroke subtypes, prognosis and prevalence of risk factors in Joinville, Brazil: a 2 year community based study. J Neurol Neurosurg Psychiatry 2009; 80: 755–761.

48.

Kelly

Crispino

Sheehan

, et al. Incidence, event rates, and early outcome of stroke in Dublin, Ireland: the North Dublin population stroke study. Stroke 2012; 43: 2042–2047.

49.

Corso

Bottacchi

Giardini

, et al. Epidemiology of stroke in Northern Italy: the Cerebrovascular Aosta Registry, 2004-2008. Neurol Sci 2013; 34: 1071–1081.

50.

Palm

Urbanek

Rose

, et al. Stroke incidence and survival in Ludwigshafen am Rhein, Germany The Ludwigshafen Stroke Study (LuSSt). Stroke 2010; 41: 1865–1870.

51.

Shoeibi

Salehi

Thrift

, et al. One-year case fatality rate following stroke in the Mashhad stroke incidence study: a population-based study of stroke in Iran. Int J Stroke 2015; 10: 96–102.

52.

Pikija

Cvetko

Malojčić

, et al. A population-based prospective 24-month study of stroke: incidence and 30-day case-fatality rates of first-ever strokes in Croatia. Neuroepidemiology 2012; 38: 164–171.

53.

Janes

Gigli

D’Anna

, et al. Stroke incidence and 30-day and six-month case fatality rates in Udine, Italy: a population-based prospective study. Int J Stroke 2013; 8: 100–105.

54.

Tsivgoulis

Patousi

Pikilidou

, et al. Stroke incidence and outcomes in northeastern Greece: the Evros Stroke Registry. Stroke 2018; 49: 288–295.

55.

Olindo

Saint-Vil

Jeannin

, et al. One-year disability, death and recurrence after first-ever stroke in a black Afro-Caribbean population. Int J Stroke 2017; 12: 844–850.

56.

Bahit

Coppola

Riccio

, et al. First-ever stroke and transient ischemic attack incidence and 30-day case-fatality rates in a population-based study in Argentina. Stroke 2016; 47: 1640–1642.

57.

Lavados

Hoffmeister

Moraga

, et al. Incidence, risk factors, prognosis, and health-related quality of life after stroke in a low-resource community in Chile (ÑANDU): a prospective population-based study. Lancet Glob Health 2021; 9: e340–e351.

58.

Aked

Delavaran

Norrving

, et al. Temporal trends of stroke epidemiology in Southern Sweden: a population-based study on stroke incidence and early case-Fatality. Neuroepidemiology 2018; 50: 174–182.

59.

Minelli

Cabral

Ujikawa

, et al. Trends in the incidence and mortality of stroke in Matão, Brazil: the Matão Preventing Stroke (MAPS) study. Neuroepidemiology 2020; 54: 75–82.

60.

Appelros

Secular trends of stroke epidemiology in örebro, Sweden, 2017 compared to the trends in 1999: a population-based study. Cerebrovasc Dis 2019; 48: 149–156.

61.

Feigin

Barker-Collo

Parag

, et al.; ASTRO study group. Auckland Stroke Outcomes Study. Part 1: gender, stroke types, ethnicity, and functional outcomes 5 years poststroke. Neurology 2010; 75: 1597–1607.

62.

de Campos

Martins

Cabral

, et al. How many patients become functionally dependent after a stroke? A 3-year population-based study in Joinville, Brazil. PLoS One 2017; 12: e0170204.

63.

Tsivgoulis

Katsanos

Patousi

, et al. Stroke recurrence and mortality in northeastern Greece: the Evros Stroke Registry. J Neurol 2018; 265: 2379–2387.

64.

Vergouwen

Jong-Tjien-Fa

Algra

, et al. Time trends in causes of death after aneurysmal subarachnoid hemorrhage: a hospital-based study. Neurology 2016; 86: 59–63.

65.

Huang

van Gelder

JM.

The probability of sudden death from rupture of intracranial aneurysms: a meta-analysis. Neurosurg 2002; 51: 1101–1105.

66.

Asikainen

Korja

Kaprio

, et al. Case fatality in patients with aneurysmal subarachnoid hemorrhage in Finland: a nationwide register-based study. Neurology 2023; 100: e348–e356.

67.

Mahlamäki

Rautalin

Korja

Case fatality rates of subarachnoid hemorrhage are decreasing with substantial between-country variation: a systematic review of population-based studies between 1980 and 2020. Neuroepidemiology 2022; 56: 402–412.

68.

Etminan

Chang

Hackenberg

, et al. 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. JAMA Neurol 2019; 76: 588–597.

69.

Uhl

Huscher

Sommerfeld

, et al. Aneurysmal subarachnoid hemorrhage in Germany between 2005 and 2018: a nationwide observational study. Eur J Neurol 2022; 29: 3009–3016.

70.

Imperial Coll London, et al., Lindgren

Koivisto

Jääskeläinen

. In reply: outcome after clipping and coiling for aneurysmal subarachnoid hemorrhage in clinical practice in Europe, USA, and Australia. Neurosurg 2019; 84: E447–1026.

71.

G-D

Wang

Zhao

L-B

, et al. Clinical outcomes of diffuse angiogram-negative subarachnoid hemorrhage versus aneurysmal subarachnoid hemorrhage: a propensity score-matched analysis. J Am Heart Assoc 2024; 13: e031066.

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