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 | Cerebrovascular Disease | JAMA Neurology | JAMA Network
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Figure 1.  Crude Subarachnoid Hemorrhage (SAH) Incidence by Country and Midyear in Europe
Crude Subarachnoid Hemorrhage (SAH) Incidence by Country and Midyear in Europe

Crude SAH incidence per 100 000 person-years with 95% CIs are presented according to country and midyear in Europe.

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

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).

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

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.

Table 1.  Subarachnoid Hemorrhage (SAH) Incidence, Risk Ratios (RRs), Midyear Range, and Time Trends by Region
Subarachnoid Hemorrhage (SAH) Incidence, Risk Ratios (RRs), Midyear Range, and Time Trends by Region
Table 2.  Association of Mean Blood Pressure (BP) and Smoking Prevalence Time Trends With Subarachnoid Hemorrhage (SAH) Incidencea
Association of Mean Blood Pressure (BP) and Smoking Prevalence Time Trends With Subarachnoid Hemorrhage (SAH) Incidencea
1.
Nieuwkamp  DJ, Setz  LE, Algra  A, Linn  FH, de Rooij  NK, Rinkel  GJ.  Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis.  Lancet Neurol. 2009;8(7):635-642. doi:10.1016/S1474-4422(09)70126-7PubMedGoogle ScholarCrossref
2.
de Rooij  NK, Linn  FH, van der Plas  JA, Algra  A, Rinkel  GJ.  Incidence of subarachnoid haemorrhage: a systematic review with emphasis on region, age, gender and time trends.  J Neurol Neurosurg Psychiatry. 2007;78(12):1365-1372. doi:10.1136/jnnp.2007.117655PubMedGoogle ScholarCrossref
3.
Korja  M, Lehto  H, Juvela  S, Kaprio  J.  Incidence of subarachnoid hemorrhage is decreasing together with decreasing smoking rates.  Neurology. 2016;87(11):1118-1123. doi:10.1212/WNL.0000000000003091PubMedGoogle ScholarCrossref
4.
Mackey  J, Khoury  JC, Alwell  K,  et al.  Stable incidence but declining case-fatality rates of subarachnoid hemorrhage in a population.  Neurology. 2016;87(21):2192-2197. doi:10.1212/WNL.0000000000003353PubMedGoogle ScholarCrossref
5.
NCD Risk Factor Collaboration (NCD-RisC).  Worldwide trends in blood pressure from 1975 to 2015: a pooled analysis of 1479 population-based measurement studies with 19·1 million participants.  Lancet. 2017;389(10064):37-55. doi:10.1016/S0140-6736(16)31919-5PubMedGoogle ScholarCrossref
6.
GBD 2015 Tobacco Collaborators.  Smoking prevalence and attributable disease burden in 195 countries and territories, 1990-2015: a systematic analysis from the Global Burden of Disease Study 2015.  Lancet. 2017;389(10082):1885-1906. doi:10.1016/S0140-6736(17)30819-XPubMedGoogle ScholarCrossref
7.
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(4):625-629. doi:10.1161/01.STR.27.4.625PubMedGoogle ScholarCrossref
8.
Higgins  JP, Thompson  SG, Deeks  JJ, Altman  DG.  Measuring inconsistency in meta-analyses.  BMJ. 2003;327(7414):557-560. doi:10.1136/bmj.327.7414.557PubMedGoogle ScholarCrossref
9.
Sudlow  CL, Warlow  CP.  Comparing stroke incidence worldwide: what makes studies comparable?  Stroke. 1996;27(3):550-558. doi:10.1161/01.STR.27.3.550PubMedGoogle ScholarCrossref
10.
Pikija  S, Cvetko  D, Malojčić  B,  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(3):164-171. doi:10.1159/000336114PubMedGoogle ScholarCrossref
11.
Hansen  BS, Marquardsen  J.  Incidence of stroke in Frederiksberg, Denmark.  Stroke. 1977;8(6):663-665. doi:10.1161/01.STR.8.6.663PubMedGoogle ScholarCrossref
12.
Truelsen  T, Grønbaek  M, Schnohr  P, Boysen  G.  Stroke case fatality in Denmark from 1977 to 1992: the Copenhagen City Heart Study.  Neuroepidemiology. 2002;21(1):22-27. doi:10.1159/000048610PubMedGoogle ScholarCrossref
13.
Jørgensen  HS, Plesner  AM, Hübbe  P, Larsen  K.  Marked increase of stroke incidence in men between 1972 and 1990 in Frederiksberg, Denmark.  Stroke. 1992;23(12):1701-1704. doi:10.1161/01.STR.23.12.1701PubMedGoogle ScholarCrossref
14.
Vibo  R, Kõrv  J, Roose  M.  The Third Stroke Registry in Tartu, Estonia: decline of stroke incidence and 28-day case-fatality rate since 1991.  Stroke. 2005;36(12):2544-2548. doi:10.1161/01.STR.0000189633.33623.69PubMedGoogle ScholarCrossref
15.
Numminen  H, Kotila  M, Waltimo  O, Aho  K, Kaste  M.  Declining incidence and mortality rates of stroke in Finland from 1972 to 1991: results of three population-based stroke registers.  Stroke. 1996;27(9):1487-1491. doi:10.1161/01.STR.27.9.1487PubMedGoogle ScholarCrossref
16.
Sivenius  J, Heinonen  OP, Pyörälä  K, Salonen  J, Riekkinen  P.  The incidence of stroke in the Kuopio area of East Finland.  Stroke. 1985;16(2):188-192. doi:10.1161/01.STR.16.2.188PubMedGoogle ScholarCrossref
17.
Sarti  C, Tuomilehto  J, Salomaa  V,  et al.  Epidemiology of subarachnoid hemorrhage in Finland from 1983 to 1985.  Stroke. 1991;22(7):848-853. doi:10.1161/01.STR.22.7.848PubMedGoogle ScholarCrossref
18.
Biotti  D, Jacquin  A, Boutarbouch  M,  et al.  Trends in case-fatality rates in hospitalized nontraumatic subarachnoid hemorrhage: results of a population-based study in Dijon, France, from 1985 to 2006  [published correction appears in Neurosurgery. 2010;67(3):F878].  Neurosurgery. 2010;66(6):1039-1043. doi:10.1227/01.NEU.0000369512.58898.99PubMedGoogle ScholarCrossref
19.
Tsiskaridze  A, Djibuti  M, van Melle  G,  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(11):2523-2528. doi:10.1161/01.STR.0000144683.96048.98PubMedGoogle ScholarCrossref
20.
Kolominsky-Rabas  PL, Sarti  C, Heuschmann  PU,  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(12):2501-2506. doi:10.1161/01.STR.29.12.2501PubMedGoogle ScholarCrossref
21.
Palm  F, Urbanek  C, Rose  S,  et al.  Stroke incidence and survival in Ludwigshafen am Rhein, Germany: the Ludwigshafen Stroke Study (LuSSt).  Stroke. 2010;41(9):1865-1870. doi:10.1161/STROKEAHA.110.592642PubMedGoogle ScholarCrossref
22.
Stranjalis  G, Kalamatianos  T, Gatzonis  S, Loufardaki  M, Tzavara  C, Sakas  DE.  The incidence of the first-ever stroke in a Mediterranean island population: the isle of Lesvos Stroke Study.  Neuroepidemiology. 2014;43(3-4):206-212. doi:10.1159/000365849PubMedGoogle ScholarCrossref
23.
Hilmarsson  A, Kjartansson  O, Olafsson  E.  Incidence of first stroke: a population study in Iceland.  Stroke. 2013;44(6):1714-1716. doi:10.1161/STROKEAHA.111.000222PubMedGoogle ScholarCrossref
24.
Kelly  PJ, Crispino  G, Sheehan  O,  et al.  Incidence, event rates, and early outcome of stroke in Dublin, Ireland: the North Dublin Population Stroke Study.  Stroke. 2012;43(8):2042-2047. doi:10.1161/STROKEAHA.111.645721PubMedGoogle ScholarCrossref
25.
Ricci  S, Celani  MG, La Rosa  F,  et al.  A community-based study of incidence, risk factors and outcome of transient ischaemic attacks in Umbria, Italy: the SEPIVAC study.  J Neurol. 1991;238(2):87-90. doi:10.1007/BF00315687PubMedGoogle ScholarCrossref
26.
D’Alessandro  G, Di Giovanni  M, Roveyaz  L,  et al.  Incidence and prognosis of stroke in the Valle d’Aosta, Italy: first-year results of a community-based study.  Stroke. 1992;23(12):1712-1715. doi:10.1161/01.STR.23.12.1712PubMedGoogle ScholarCrossref
27.
Lauria  G, Gentile  M, Fassetta  G,  et al.  Incidence and prognosis of stroke in the Belluno province, Italy: first-year results of a community-based study.  Stroke. 1995;26(10):1787-1793. doi:10.1161/01.STR.26.10.1787PubMedGoogle ScholarCrossref
28.
Sacco  S, Totaro  R, Toni  D, Marini  C, Cerone  D, Carolei  A.  Incidence, case-fatalities and 10-year survival of subarachnoid hemorrhage in a population-based registry.  Eur Neurol. 2009;62(3):155-160. doi:10.1159/000226617PubMedGoogle ScholarCrossref
29.
Di Carlo  A, Inzitari  D, Galati  F,  et al.  A prospective community-based study of stroke in Southern Italy: the Vibo Valentia Incidence of Stroke Study (VISS): methodology, incidence and case fatality at 28 days, 3 and 12 months.  Cerebrovasc Dis. 2003;16(4):410-417. doi:10.1159/000072565PubMedGoogle ScholarCrossref
30.
D’Alessandro  G, Bottacchi  E, Di Giovanni  M,  et al.  Temporal trends of stroke in Valle d’Aosta, Italy: incidence and 30-day fatality rates.  Neurol Sci. 2000;21(1):13-18. doi:10.1007/s100720070113PubMedGoogle ScholarCrossref
31.
Musolino  R, La Spina  P, Serra  S,  et al.  First-ever stroke incidence and 30-day case fatality in the Sicilian Aeolian archipelago, Italy.  Stroke. 2005;36(12):2738-2741. doi:10.1161/01.STR.0000190907.88846.dfPubMedGoogle ScholarCrossref
32.
Manobianca  G, Zoccolella  S, Petruzzellis  A, Miccoli  A, Logroscino  G.  The incidence of major stroke subtypes in southern Italy: a population-based study.  Eur J Neurol. 2010;17(9):1148-1155. doi:10.1111/j.1468-1331.2010.02983.xPubMedGoogle ScholarCrossref
33.
Corso  G, Bottacchi  E, Giardini  G,  et al.  Community-based study of stroke incidence in the Valley of Aosta, Italy: CARe—Cerebrovascular Aosta Registry: years 2004-2005.  Neuroepidemiology. 2009;32(3):186-195. doi:10.1159/000195688PubMedGoogle ScholarCrossref
34.
Corso  G, Bottacchi  E, Giardini  G,  et al.  Epidemiology of stroke in northern Italy: the Cerebrovascular Aosta Registry, 2004-2008.  Neurol Sci. 2013;34(7):1071-1081. doi:10.1007/s10072-012-1185-8PubMedGoogle ScholarCrossref
35.
Janes  F, Gigli  GL, D’Anna  L,  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(suppl A100):100-105. doi:10.1111/ijs.12000PubMedGoogle ScholarCrossref
36.
Herman  B, Leyten  AC, van Luijk  JH, Frenken  CW, Op de Coul  AA, Schulte  BP.  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(5):629-634. doi:10.1161/01.STR.13.5.629PubMedGoogle ScholarCrossref
37.
Correia  M, Magalhães  R, Silva  MR, Matos  I, Silva  MC.  Stroke types in rural and urban northern Portugal: incidence and 7-year survival in a community-based study.  Cerebrovasc Dis Extra. 2013;3(1):137-149. doi:10.1159/000354851PubMedGoogle ScholarCrossref
38.
Caicoya  M, Rodríguez  T, Lasheras  C, Cuello  R, Corrales  C, Blázquez  B.  Stroke incidence in Asturias, 1990-1991  [in Spanish].  Rev Neurol. 1996;24(131):806-811.PubMedGoogle Scholar
39.
Díaz-Guzmán  J, Egido  JA, Gabriel-Sánchez  R, Barberá-Comes  G, Fuentes-Gimeno  B, Fernández-Pérez  C; IBERICTUS Study Investigators of the Stroke Project of the Spanish Cerebrovascular Diseases Study Group.  Stroke and transient ischemic attack incidence rate in Spain: the IBERICTUS study.  Cerebrovasc Dis. 2012;34(4):272-281. doi:10.1159/000342652PubMedGoogle ScholarCrossref
40.
Terént  A.  Increasing incidence of stroke among Swedish women.  Stroke. 1988;19(5):598-603. doi:10.1161/01.STR.19.5.598PubMedGoogle ScholarCrossref
41.
Norrving  B, Löwenhielm  P.  Epidemiology of stroke in Lund-Orup, Sweden, 1983-85: incidence of first stroke and age-related changes in subtypes.  Acta Neurol Scand. 1988;78(5):408-413. doi:10.1111/j.1600-0404.1988.tb03677.xPubMedGoogle ScholarCrossref
42.
Stegmayr  B, Eriksson  M, Asplund  K.  Declining mortality from subarachnoid hemorrhage: changes in incidence and case fatality from 1985 through 2000.  Stroke. 2004;35(9):2059-2063. doi:10.1161/01.STR.0000138451.07853.b6PubMedGoogle ScholarCrossref
43.
Khan  FA, Engstrom  G, Jerntorp  I, Pessah-Rasmussen  H, Janzon  L.  Seasonal patterns of incidence and case fatality of stroke in Malmo, Sweden: the STROMA study.  Neuroepidemiology. 2005;24(1-2):26-31. doi:10.1159/000081046PubMedGoogle ScholarCrossref
44.
Nilsson  OG, Lindgren  A, Ståhl  N, Brandt  L, Säveland  H.  Incidence of intracerebral and subarachnoid haemorrhage in southern Sweden.  J Neurol Neurosurg Psychiatry. 2000;69(5):601-607. doi:10.1136/jnnp.69.5.601PubMedGoogle ScholarCrossref
45.
Appelros  P, Nydevik  I, Seiger  A, Terént  A.  High incidence rates of stroke in Orebro, Sweden: further support for regional incidence differences within Scandinavia.  Cerebrovasc Dis. 2002;14(3-4):161-168. doi:10.1159/000065680PubMedGoogle ScholarCrossref
46.
Hallström  B, Jönsson  AC, Nerbrand  C, Norrving  B, Lindgren  A.  Stroke incidence and survival in the beginning of the 21st century in southern Sweden: comparisons with the late 20th century and projections into the future.  Stroke. 2008;39(1):10-15. doi:10.1161/STROKEAHA.107.491779PubMedGoogle ScholarCrossref
47.
Bamford  J, Sandercock  P, Dennis  M, Burn  J, Warlow  C.  A prospective study of acute cerebrovascular disease in the community: the Oxfordshire Community Stroke Project—1981-86. 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(1):16-22. doi:10.1136/jnnp.53.1.16PubMedGoogle ScholarCrossref
48.
Wolfe  CD, Rudd  AG, Howard  R,  et al.  Incidence and case fatality rates of stroke subtypes in a multiethnic population: the South London Stroke Register.  J Neurol Neurosurg Psychiatry. 2002;72(2):211-216. doi:10.1136/jnnp.72.2.211PubMedGoogle ScholarCrossref
49.
Syme  PD, Byrne  AW, Chen  R, Devenny  R, Forbes  JF.  Community-based stroke incidence in a Scottish population: the Scottish Borders Stroke Study.  Stroke. 2005;36(9):1837-1843. doi:10.1161/01.STR.0000177873.82478.1cPubMedGoogle ScholarCrossref
50.
Heuschmann  PU, Grieve  AP, Toschke  AM, Rudd  AG, Wolfe  CD.  Ethnic group disparities in 10-year trends in stroke incidence and vascular risk factors: the South London Stroke Register (SLSR).  Stroke. 2008;39(8):2204-2210. doi:10.1161/STROKEAHA.107.507285PubMedGoogle ScholarCrossref
51.
Lovelock  CE, Rinkel  GJ, Rothwell  PM.  Time trends in outcome of subarachnoid hemorrhage: population-based study and systematic review.  Neurology. 2010;74(19):1494-1501. doi:10.1212/WNL.0b013e3181dd42b3PubMedGoogle ScholarCrossref
52.
Tanaka  H, Ueda  Y, Date  C,  et al.  Incidence of stroke in Shibata, Japan: 1976-1978.  Stroke. 1981;12(4):460-466. doi:10.1161/01.STR.12.4.460PubMedGoogle ScholarCrossref
53.
Inagawa  T.  Trends in incidence and case fatality rates of aneurysmal subarachnoid hemorrhage in Izumo City, Japan, between 1980-1989 and 1990-1998.  Stroke. 2001;32(7):1499-1507. doi:10.1161/01.STR.32.7.1499PubMedGoogle ScholarCrossref
54.
Ohkuma  H, Fujita  S, Suzuki  S.  Incidence of aneurysmal subarachnoid hemorrhage in Shimokita, Japan, from 1989 to 1998.  Stroke. 2002;33(1):195-199. doi:10.1161/hs0102.101891PubMedGoogle ScholarCrossref
55.
Turin  TC, Kita  Y, Rumana  N,  et al.  Ambient air pollutants and acute case-fatality of cerebro-cardiovascular events: Takashima Stroke and AMI Registry, Japan (1988-2004).  Cerebrovasc Dis. 2012;34(2):130-139. doi:10.1159/000339680PubMedGoogle ScholarCrossref
56.
Hamada  J, Morioka  M, Yano  S, Kai  Y, Ushio  Y.  Incidence and early prognosis of aneurysmal subarachnoid hemorrhage in Kumamoto Prefecture, Japan.  Neurosurgery. 2004;54(1):31-37. doi:10.1227/01.NEU.0000097196.55204.0BPubMedGoogle ScholarCrossref
57.
Omama  S, Yoshida  Y, Ogasawara  K,  et al.  Incidence rate of cerebrovascular diseases in northern Japan determined from the Iwate Stroke Registry with an inventory survey system.  J Stroke Cerebrovasc Dis. 2013;22(8):e317-e322. doi:10.1016/j.jstrokecerebrovasdis.2012.12.011PubMedGoogle ScholarCrossref
58.
Zhang  J, Liu  G, Arima  H,  et al; CHERISH Investigators.  Incidence and risks of subarachnoid hemorrhage in China.  Stroke. 2013;44(10):2891-2893. doi:10.1161/STROKEAHA.113.002599PubMedGoogle ScholarCrossref
59.
Azarpazhooh  MR, Etemadi  MM, Donnan  GA,  et al.  Excessive incidence of stroke in Iran: evidence from the Mashhad Stroke Incidence Study (MSIS), a population-based study of stroke in the Middle East.  Stroke. 2010;41(1):e3-e10. doi:10.1161/STROKEAHA.109.559708PubMedGoogle ScholarCrossref
60.
Dalal  PM, Malik  S, Bhattacharjee  M,  et al.  Population-based stroke survey in Mumbai, India: incidence and 28-day case fatality.  Neuroepidemiology. 2008;31(4):254-261. doi:10.1159/000165364PubMedGoogle ScholarCrossref
61.
Epstein  L, Rishpon  S, Bental  E,  et al.  Incidence, mortality, and case-fatality rate of stroke in northern Israel.  Stroke. 1989;20(6):725-729. doi:10.1161/01.STR.20.6.725PubMedGoogle ScholarCrossref
62.
Abdul-Ghaffar  NU, el-Sonbaty  MR, el-Din Abdul-Baky  MS, Marafie  AA, al-Said  AM.  Stroke in Kuwait: a three-year prospective study.  Neuroepidemiology. 1997;16(1):40-47. doi:10.1159/000109669PubMedGoogle ScholarCrossref
63.
Feigin  VL, Wiebers  DO, Nikitin  YP, O’Fallon  WM, Whisnant  JP.  Stroke epidemiology in Novosibirsk, Russia: a population-based study.  Mayo Clin Proc. 1995;70(9):847-852. doi:10.1016/S0025-6196(11)63942-6PubMedGoogle ScholarCrossref
64.
Anderson  CS, Jamrozik  KD, Burvill  PW, Chakera  TM, Johnson  GA, Stewart-Wynne  EG.  Determining the incidence of different subtypes of stroke: results from the Perth Community Stroke Study, 1989-1990.  Med J Aust. 1993;158(2):85-89.PubMedGoogle ScholarCrossref
65.
Islam  MS, Anderson  CS, Hankey  GJ,  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(3):776-782. doi:10.1161/STROKEAHA.107.493643PubMedGoogle ScholarCrossref
66.
Thrift  AG, Dewey  HM, Macdonell  RA, McNeil  JJ, Donnan  GA.  Incidence of the major stroke subtypes: initial findings from the North East Melbourne Stroke Incidence Study (NEMESIS).  Stroke. 2001;32(8):1732-1738. doi:10.1161/01.STR.32.8.1732PubMedGoogle ScholarCrossref
67.
Thrift  AG, Dewey  HM, Sturm  JW,  et al.  Incidence of stroke subtypes in the North East Melbourne Stroke Incidence Study (NEMESIS): differences between men and women.  Neuroepidemiology. 2009;32(1):11-18. doi:10.1159/000170086PubMedGoogle ScholarCrossref
68.
Leyden  JM, Kleinig  TJ, Newbury  J,  et al.  Adelaide stroke incidence study: declining stroke rates but many preventable cardioembolic strokes.  Stroke. 2013;44(5):1226-1231. doi:10.1161/STROKEAHA.113.675140PubMedGoogle ScholarCrossref
69.
Newbury  J, Kleinig  T, Leyden  J,  et al.  Stroke Epidemiology in an Australian Rural Cohort (SEARCH).  Int J Stroke. 2017;12(2):161-168. doi:10.1177/1747493016670174PubMedGoogle ScholarCrossref
70.
Bonita  R, Thomson  S.  Subarachnoid hemorrhage: epidemiology, diagnosis, management, and outcome.  Stroke. 1985;16(4):591-594. doi:10.1161/01.STR.16.4.591PubMedGoogle ScholarCrossref
71.
Truelsen  T, Bonita  R, Duncan  J, Anderson  NE, Mee  E.  Changes in subarachnoid hemorrhage mortality, incidence, and case fatality in New Zealand between 1981-1983 and 1991-1993.  Stroke. 1998;29(11):2298-2303. doi:10.1161/01.STR.29.11.2298PubMedGoogle ScholarCrossref
72.
Feigin  V, Carter  K, Hackett  M,  et al; Auckland Regional Community Stroke Study Group.  Ethnic disparities in incidence of stroke subtypes: Auckland Regional Community Stroke Study, 2002-2003.  Lancet Neurol. 2006;5(2):130-139. doi:10.1016/S1474-4422(05)70325-2PubMedGoogle ScholarCrossref
73.
Cantu-Brito  C, Majersik  JJ, Sánchez  BN,  et al.  Hospitalized stroke surveillance in the community of Durango, Mexico: the Brain Attack Surveillance in Durango study.  Stroke. 2010;41(5):878-884. doi:10.1161/STROKEAHA.109.577726PubMedGoogle ScholarCrossref
74.
Brown  RD, Whisnant  JP, Sicks  JD, O’Fallon  WM, Wiebers  DO.  Stroke incidence, prevalence, and survival: secular trends in Rochester, Minnesota, through 1989.  Stroke. 1996;27(3):373-380.PubMedGoogle Scholar
75.
Longstreth  WT  Jr, Nelson  LM, Koepsell  TD, van Belle  G.  Clinical course of spontaneous subarachnoid hemorrhage: a population-based study in King County, Washington.  Neurology. 1993;43(4):712-718. doi:10.1212/WNL.43.4.712PubMedGoogle ScholarCrossref
76.
Labovitz  DL, Halim  AX, Brent  B, Boden-Albala  B, Hauser  WA, Sacco  RL.  Subarachnoid hemorrhage incidence among whites, blacks and Caribbean Hispanics: the Northern Manhattan Study.  Neuroepidemiology. 2006;26(3):147-150. doi:10.1159/000091655PubMedGoogle ScholarCrossref
77.
Bahit  MC, Coppola  ML, Riccio  PM,  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(6):1640-1642. doi:10.1161/STROKEAHA.116.013637PubMedGoogle ScholarCrossref
78.
Minelli  C, Fen  LF, Minelli  DP.  Stroke incidence, prognosis, 30-day, and 1-year case fatality rates in Matão, Brazil: a population-based prospective study.  Stroke. 2007;38(11):2906-2911. doi:10.1161/STROKEAHA.107.484139PubMedGoogle ScholarCrossref
79.
Cabral  NL, Gonçalves  AR, Longo  AL,  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(7):755-761. doi:10.1136/jnnp.2009.172098PubMedGoogle ScholarCrossref
80.
Cabral  NL, Cougo-Pinto  PT, Magalhaes  PS,  et al.  Trends of stroke incidence from 1995 to 2013 in Joinville, Brazil.  Neuroepidemiology. 2016;46(4):273-281. doi:10.1159/000445060PubMedGoogle ScholarCrossref
81.
Smadja  D, Cabre  P, May  F,  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(12):2741-2747. doi:10.1161/hs1201.099385PubMedGoogle ScholarCrossref
82.
Wolfe  CD, Corbin  DO, Smeeton  NC,  et al.  Estimation of the risk of stroke in black populations in Barbados and South London.  Stroke. 2006;37(8):1986-1990. doi:10.1161/01.STR.0000230578.10937.a6PubMedGoogle ScholarCrossref
83.
Alvarez  G, Cox  P, Pairoa  M, García  M, Delgado  I, Lavados  PM.  Incidence of subarachnoid haemorrhage in the Aconcagua Valley, Chile: a community-based, prospective surveillance project.  J Neurol Neurosurg Psychiatry. 2010;81(7):778-782. doi:10.1136/jnnp.2009.192971PubMedGoogle ScholarCrossref
84.
Lavados  PM, Sacks  C, Prina  L,  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(9478):2206-2215. doi:10.1016/S0140-6736(05)66779-7PubMedGoogle ScholarCrossref
85.
Okon  M, Adebobola  NI, Julius  S,  et al.  Stroke incidence and case fatality rate in an urban population.  J Stroke Cerebrovasc Dis. 2015;24(4):771-777. doi:10.1016/j.jstrokecerebrovasdis.2014.11.004PubMedGoogle ScholarCrossref
86.
Kita  Y, Turin  TC, Ichikawa  M,  et al.  Trend of stroke incidence in a Japanese population: Takashima Stroke Registry, 1990-2001.  Int J Stroke. 2009;4(4):241-249. doi:10.1111/j.1747-4949.2009.00293.xPubMedGoogle ScholarCrossref
87.
ACROSS Group.  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(8):1843-1850. doi:10.1161/01.STR.31.8.1843PubMedGoogle ScholarCrossref
88.
Vemmos  KN, Bots  ML, Tsibouris  PK,  et al.  Stroke incidence and case fatality in southern Greece: the Arcadia Stroke Registry.  Stroke. 1999;30(2):363-370. doi:10.1161/01.STR.30.2.363PubMedGoogle ScholarCrossref
89.
Feigin  VL, Forouzanfar  MH, Krishnamurthi  R,  et al; Global Burden of Diseases, Injuries, and Risk Factors Study 2010 (GBD 2010) and the GBD Stroke Experts Group.  Global and regional burden of stroke during 1990-2010: findings from the Global Burden of Disease Study 2010.  Lancet. 2014;383(9913):245-254. doi:10.1016/S0140-6736(13)61953-4PubMedGoogle ScholarCrossref
90.
Etminan  N, Rinkel  GJ.  Unruptured intracranial aneurysms: development, rupture and preventive management.  Nat Rev Neurol. 2016;12(12):699-713. doi:10.1038/nrneurol.2016.150PubMedGoogle ScholarCrossref
91.
Jalbert  JJ, Isaacs  AJ, Kamel  H, Sedrakyan  A.  Clipping and coiling of unruptured intracranial aneurysms among Medicare beneficiaries, 2000 to 2010.  Stroke. 2015;46(9):2452-2457. doi:10.1161/STROKEAHA.115.009777PubMedGoogle ScholarCrossref
92.
Vlak  MH, Algra  A, Brandenburg  R, Rinkel  GJ.  Prevalence of unruptured intracranial aneurysms, with emphasis on sex, age, comorbidity, country, and time period: a systematic review and meta-analysis.  Lancet Neurol. 2011;10(7):626-636. doi:10.1016/S1474-4422(11)70109-0PubMedGoogle ScholarCrossref
93.
Huang  J, van Gelder  JM.  The probability of sudden death from rupture of intracranial aneurysms: a meta-analysis.  Neurosurgery. 2002;51(5):1101-1105. doi:10.1097/00006123-200211000-00001PubMedGoogle ScholarCrossref
94.
Bamford  J, Dennis  M, Sandercock  P, Burn  J, Warlow  C.  The frequency, causes and timing of death within 30 days of a first stroke: the Oxfordshire Community Stroke Project.  J Neurol Neurosurg Psychiatry. 1990;53(10):824-829. doi:10.1136/jnnp.53.10.824PubMedGoogle ScholarCrossref
95.
Feigin  VL, Wiebers  DO, Whisnant  JP, O’Fallon  WM.  Stroke incidence and 30-day case-fatality rates in Novosibirsk, Russia, 1982 through 1992.  Stroke. 1995;26(6):924-929. doi:10.1161/01.STR.26.6.924PubMedGoogle ScholarCrossref
Original Investigation
January 19, 2019

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

Author Affiliations
  • 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
JAMA Neurol. 2019;76(5):588-597. doi:10.1001/jamaneurol.2019.0006
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.

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 110-51 and Figure 252-85).

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 1972.10-51 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 1977.52-63 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 1977.52-57 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).58-63 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 1955.73-76 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),77-84 Australia and New Zealand (10 study periods),64-72 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 Europe11,13,15,40,47,48,50,51 and the study from North America74 and an increase in SAH incidence in the 2 studies from Japan.53,86

The sensitivity analysis for the overall decline in the 40 studies that had at least 90% CT scanning14,18,20-24,27-30,32,34,35,37,39,44,49,51,53,54,56-59,62,66,68,69,71,72,75-82,84 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 scanning10,13-15,18-25,27-35,37-39,42-45,48-51,53-60,62-69,71-73,75-84 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 studies10,19,20,27-29,32,34,36,43,51-53,57,58,64,66,67,72,73,77-79,83-88 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.

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.

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.

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Article Information

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.

References
1.
Nieuwkamp  DJ, Setz  LE, Algra  A, Linn  FH, de Rooij  NK, Rinkel  GJ.  Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis.  Lancet Neurol. 2009;8(7):635-642. doi:10.1016/S1474-4422(09)70126-7PubMedGoogle ScholarCrossref
2.
de Rooij  NK, Linn  FH, van der Plas  JA, Algra  A, Rinkel  GJ.  Incidence of subarachnoid haemorrhage: a systematic review with emphasis on region, age, gender and time trends.  J Neurol Neurosurg Psychiatry. 2007;78(12):1365-1372. doi:10.1136/jnnp.2007.117655PubMedGoogle ScholarCrossref
3.
Korja  M, Lehto  H, Juvela  S, Kaprio  J.  Incidence of subarachnoid hemorrhage is decreasing together with decreasing smoking rates.  Neurology. 2016;87(11):1118-1123. doi:10.1212/WNL.0000000000003091PubMedGoogle ScholarCrossref
4.
Mackey  J, Khoury  JC, Alwell  K,  et al.  Stable incidence but declining case-fatality rates of subarachnoid hemorrhage in a population.  Neurology. 2016;87(21):2192-2197. doi:10.1212/WNL.0000000000003353PubMedGoogle ScholarCrossref
5.
NCD Risk Factor Collaboration (NCD-RisC).  Worldwide trends in blood pressure from 1975 to 2015: a pooled analysis of 1479 population-based measurement studies with 19·1 million participants.  Lancet. 2017;389(10064):37-55. doi:10.1016/S0140-6736(16)31919-5PubMedGoogle ScholarCrossref
6.
GBD 2015 Tobacco Collaborators.  Smoking prevalence and attributable disease burden in 195 countries and territories, 1990-2015: a systematic analysis from the Global Burden of Disease Study 2015.  Lancet. 2017;389(10082):1885-1906. doi:10.1016/S0140-6736(17)30819-XPubMedGoogle ScholarCrossref
7.
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(4):625-629. doi:10.1161/01.STR.27.4.625PubMedGoogle ScholarCrossref
8.
Higgins  JP, Thompson  SG, Deeks  JJ, Altman  DG.  Measuring inconsistency in meta-analyses.  BMJ. 2003;327(7414):557-560. doi:10.1136/bmj.327.7414.557PubMedGoogle ScholarCrossref
9.
Sudlow  CL, Warlow  CP.  Comparing stroke incidence worldwide: what makes studies comparable?  Stroke. 1996;27(3):550-558. doi:10.1161/01.STR.27.3.550PubMedGoogle ScholarCrossref
10.
Pikija  S, Cvetko  D, Malojčić  B,  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(3):164-171. doi:10.1159/000336114PubMedGoogle ScholarCrossref
11.
Hansen  BS, Marquardsen  J.  Incidence of stroke in Frederiksberg, Denmark.  Stroke. 1977;8(6):663-665. doi:10.1161/01.STR.8.6.663PubMedGoogle ScholarCrossref
12.
Truelsen  T, Grønbaek  M, Schnohr  P, Boysen  G.  Stroke case fatality in Denmark from 1977 to 1992: the Copenhagen City Heart Study.  Neuroepidemiology. 2002;21(1):22-27. doi:10.1159/000048610PubMedGoogle ScholarCrossref
13.
Jørgensen  HS, Plesner  AM, Hübbe  P, Larsen  K.  Marked increase of stroke incidence in men between 1972 and 1990 in Frederiksberg, Denmark.  Stroke. 1992;23(12):1701-1704. doi:10.1161/01.STR.23.12.1701PubMedGoogle ScholarCrossref
14.
Vibo  R, Kõrv  J, Roose  M.  The Third Stroke Registry in Tartu, Estonia: decline of stroke incidence and 28-day case-fatality rate since 1991.  Stroke. 2005;36(12):2544-2548. doi:10.1161/01.STR.0000189633.33623.69PubMedGoogle ScholarCrossref
15.
Numminen  H, Kotila  M, Waltimo  O, Aho  K, Kaste  M.  Declining incidence and mortality rates of stroke in Finland from 1972 to 1991: results of three population-based stroke registers.  Stroke. 1996;27(9):1487-1491. doi:10.1161/01.STR.27.9.1487PubMedGoogle ScholarCrossref
16.
Sivenius  J, Heinonen  OP, Pyörälä  K, Salonen  J, Riekkinen  P.  The incidence of stroke in the Kuopio area of East Finland.  Stroke. 1985;16(2):188-192. doi:10.1161/01.STR.16.2.188PubMedGoogle ScholarCrossref
17.
Sarti  C, Tuomilehto  J, Salomaa  V,  et al.  Epidemiology of subarachnoid hemorrhage in Finland from 1983 to 1985.  Stroke. 1991;22(7):848-853. doi:10.1161/01.STR.22.7.848PubMedGoogle ScholarCrossref
18.
Biotti  D, Jacquin  A, Boutarbouch  M,  et al.  Trends in case-fatality rates in hospitalized nontraumatic subarachnoid hemorrhage: results of a population-based study in Dijon, France, from 1985 to 2006  [published correction appears in Neurosurgery. 2010;67(3):F878].  Neurosurgery. 2010;66(6):1039-1043. doi:10.1227/01.NEU.0000369512.58898.99PubMedGoogle ScholarCrossref
19.
Tsiskaridze  A, Djibuti  M, van Melle  G,  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(11):2523-2528. doi:10.1161/01.STR.0000144683.96048.98PubMedGoogle ScholarCrossref
20.
Kolominsky-Rabas  PL, Sarti  C, Heuschmann  PU,  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(12):2501-2506. doi:10.1161/01.STR.29.12.2501PubMedGoogle ScholarCrossref
21.
Palm  F, Urbanek  C, Rose  S,  et al.  Stroke incidence and survival in Ludwigshafen am Rhein, Germany: the Ludwigshafen Stroke Study (LuSSt).  Stroke. 2010;41(9):1865-1870. doi:10.1161/STROKEAHA.110.592642PubMedGoogle ScholarCrossref
22.
Stranjalis  G, Kalamatianos  T, Gatzonis  S, Loufardaki  M, Tzavara  C, Sakas  DE.  The incidence of the first-ever stroke in a Mediterranean island population: the isle of Lesvos Stroke Study.  Neuroepidemiology. 2014;43(3-4):206-212. doi:10.1159/000365849PubMedGoogle ScholarCrossref
23.
Hilmarsson  A, Kjartansson  O, Olafsson  E.  Incidence of first stroke: a population study in Iceland.  Stroke. 2013;44(6):1714-1716. doi:10.1161/STROKEAHA.111.000222PubMedGoogle ScholarCrossref
24.
Kelly  PJ, Crispino  G, Sheehan  O,  et al.  Incidence, event rates, and early outcome of stroke in Dublin, Ireland: the North Dublin Population Stroke Study.  Stroke. 2012;43(8):2042-2047. doi:10.1161/STROKEAHA.111.645721PubMedGoogle ScholarCrossref
25.
Ricci  S, Celani  MG, La Rosa  F,  et al.  A community-based study of incidence, risk factors and outcome of transient ischaemic attacks in Umbria, Italy: the SEPIVAC study.  J Neurol. 1991;238(2):87-90. doi:10.1007/BF00315687PubMedGoogle ScholarCrossref
26.
D’Alessandro  G, Di Giovanni  M, Roveyaz  L,  et al.  Incidence and prognosis of stroke in the Valle d’Aosta, Italy: first-year results of a community-based study.  Stroke. 1992;23(12):1712-1715. doi:10.1161/01.STR.23.12.1712PubMedGoogle ScholarCrossref
27.
Lauria  G, Gentile  M, Fassetta  G,  et al.  Incidence and prognosis of stroke in the Belluno province, Italy: first-year results of a community-based study.  Stroke. 1995;26(10):1787-1793. doi:10.1161/01.STR.26.10.1787PubMedGoogle ScholarCrossref
28.
Sacco  S, Totaro  R, Toni  D, Marini  C, Cerone  D, Carolei  A.  Incidence, case-fatalities and 10-year survival of subarachnoid hemorrhage in a population-based registry.  Eur Neurol. 2009;62(3):155-160. doi:10.1159/000226617PubMedGoogle ScholarCrossref
29.
Di Carlo  A, Inzitari  D, Galati  F,  et al.  A prospective community-based study of stroke in Southern Italy: the Vibo Valentia Incidence of Stroke Study (VISS): methodology, incidence and case fatality at 28 days, 3 and 12 months.  Cerebrovasc Dis. 2003;16(4):410-417. doi:10.1159/000072565PubMedGoogle ScholarCrossref
30.
D’Alessandro  G, Bottacchi  E, Di Giovanni  M,  et al.  Temporal trends of stroke in Valle d’Aosta, Italy: incidence and 30-day fatality rates.  Neurol Sci. 2000;21(1):13-18. doi:10.1007/s100720070113PubMedGoogle ScholarCrossref
31.
Musolino  R, La Spina  P, Serra  S,  et al.  First-ever stroke incidence and 30-day case fatality in the Sicilian Aeolian archipelago, Italy.  Stroke. 2005;36(12):2738-2741. doi:10.1161/01.STR.0000190907.88846.dfPubMedGoogle ScholarCrossref
32.
Manobianca  G, Zoccolella  S, Petruzzellis  A, Miccoli  A, Logroscino  G.  The incidence of major stroke subtypes in southern Italy: a population-based study.  Eur J Neurol. 2010;17(9):1148-1155. doi:10.1111/j.1468-1331.2010.02983.xPubMedGoogle ScholarCrossref
33.
Corso  G, Bottacchi  E, Giardini  G,  et al.  Community-based study of stroke incidence in the Valley of Aosta, Italy: CARe—Cerebrovascular Aosta Registry: years 2004-2005.  Neuroepidemiology. 2009;32(3):186-195. doi:10.1159/000195688PubMedGoogle ScholarCrossref
34.
Corso  G, Bottacchi  E, Giardini  G,  et al.  Epidemiology of stroke in northern Italy: the Cerebrovascular Aosta Registry, 2004-2008.  Neurol Sci. 2013;34(7):1071-1081. doi:10.1007/s10072-012-1185-8PubMedGoogle ScholarCrossref
35.
Janes  F, Gigli  GL, D’Anna  L,  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(suppl A100):100-105. doi:10.1111/ijs.12000PubMedGoogle ScholarCrossref
36.
Herman  B, Leyten  AC, van Luijk  JH, Frenken  CW, Op de Coul  AA, Schulte  BP.  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(5):629-634. doi:10.1161/01.STR.13.5.629PubMedGoogle ScholarCrossref
37.
Correia  M, Magalhães  R, Silva  MR, Matos  I, Silva  MC.  Stroke types in rural and urban northern Portugal: incidence and 7-year survival in a community-based study.  Cerebrovasc Dis Extra. 2013;3(1):137-149. doi:10.1159/000354851PubMedGoogle ScholarCrossref
38.
Caicoya  M, Rodríguez  T, Lasheras  C, Cuello  R, Corrales  C, Blázquez  B.  Stroke incidence in Asturias, 1990-1991  [in Spanish].  Rev Neurol. 1996;24(131):806-811.PubMedGoogle Scholar
39.
Díaz-Guzmán  J, Egido  JA, Gabriel-Sánchez  R, Barberá-Comes  G, Fuentes-Gimeno  B, Fernández-Pérez  C; IBERICTUS Study Investigators of the Stroke Project of the Spanish Cerebrovascular Diseases Study Group.  Stroke and transient ischemic attack incidence rate in Spain: the IBERICTUS study.  Cerebrovasc Dis. 2012;34(4):272-281. doi:10.1159/000342652PubMedGoogle ScholarCrossref
40.
Terént  A.  Increasing incidence of stroke among Swedish women.  Stroke. 1988;19(5):598-603. doi:10.1161/01.STR.19.5.598PubMedGoogle ScholarCrossref
41.
Norrving  B, Löwenhielm  P.  Epidemiology of stroke in Lund-Orup, Sweden, 1983-85: incidence of first stroke and age-related changes in subtypes.  Acta Neurol Scand. 1988;78(5):408-413. doi:10.1111/j.1600-0404.1988.tb03677.xPubMedGoogle ScholarCrossref
42.
Stegmayr  B, Eriksson  M, Asplund  K.  Declining mortality from subarachnoid hemorrhage: changes in incidence and case fatality from 1985 through 2000.  Stroke. 2004;35(9):2059-2063. doi:10.1161/01.STR.0000138451.07853.b6PubMedGoogle ScholarCrossref
43.
Khan  FA, Engstrom  G, Jerntorp  I, Pessah-Rasmussen  H, Janzon  L.  Seasonal patterns of incidence and case fatality of stroke in Malmo, Sweden: the STROMA study.  Neuroepidemiology. 2005;24(1-2):26-31. doi:10.1159/000081046PubMedGoogle ScholarCrossref
44.
Nilsson  OG, Lindgren  A, Ståhl  N, Brandt  L, Säveland  H.  Incidence of intracerebral and subarachnoid haemorrhage in southern Sweden.  J Neurol Neurosurg Psychiatry. 2000;69(5):601-607. doi:10.1136/jnnp.69.5.601PubMedGoogle ScholarCrossref
45.
Appelros  P, Nydevik  I, Seiger  A, Terént  A.  High incidence rates of stroke in Orebro, Sweden: further support for regional incidence differences within Scandinavia.  Cerebrovasc Dis. 2002;14(3-4):161-168. doi:10.1159/000065680PubMedGoogle ScholarCrossref
46.
Hallström  B, Jönsson  AC, Nerbrand  C, Norrving  B, Lindgren  A.  Stroke incidence and survival in the beginning of the 21st century in southern Sweden: comparisons with the late 20th century and projections into the future.  Stroke. 2008;39(1):10-15. doi:10.1161/STROKEAHA.107.491779PubMedGoogle ScholarCrossref
47.
Bamford  J, Sandercock  P, Dennis  M, Burn  J, Warlow  C.  A prospective study of acute cerebrovascular disease in the community: the Oxfordshire Community Stroke Project—1981-86. 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(1):16-22. doi:10.1136/jnnp.53.1.16PubMedGoogle ScholarCrossref
48.
Wolfe  CD, Rudd  AG, Howard  R,  et al.  Incidence and case fatality rates of stroke subtypes in a multiethnic population: the South London Stroke Register.  J Neurol Neurosurg Psychiatry. 2002;72(2):211-216. doi:10.1136/jnnp.72.2.211PubMedGoogle ScholarCrossref
49.
Syme  PD, Byrne  AW, Chen  R, Devenny  R, Forbes  JF.  Community-based stroke incidence in a Scottish population: the Scottish Borders Stroke Study.  Stroke. 2005;36(9):1837-1843. doi:10.1161/01.STR.0000177873.82478.1cPubMedGoogle ScholarCrossref
50.
Heuschmann  PU, Grieve  AP, Toschke  AM, Rudd  AG, Wolfe  CD.  Ethnic group disparities in 10-year trends in stroke incidence and vascular risk factors: the South London Stroke Register (SLSR).  Stroke. 2008;39(8):2204-2210. doi:10.1161/STROKEAHA.107.507285PubMedGoogle ScholarCrossref
51.
Lovelock  CE, Rinkel  GJ, Rothwell  PM.  Time trends in outcome of subarachnoid hemorrhage: population-based study and systematic review.  Neurology. 2010;74(19):1494-1501. doi:10.1212/WNL.0b013e3181dd42b3PubMedGoogle ScholarCrossref
52.
Tanaka  H, Ueda  Y, Date  C,  et al.  Incidence of stroke in Shibata, Japan: 1976-1978.  Stroke. 1981;12(4):460-466. doi:10.1161/01.STR.12.4.460PubMedGoogle ScholarCrossref
53.
Inagawa  T.  Trends in incidence and case fatality rates of aneurysmal subarachnoid hemorrhage in Izumo City, Japan, between 1980-1989 and 1990-1998.  Stroke. 2001;32(7):1499-1507. doi:10.1161/01.STR.32.7.1499PubMedGoogle ScholarCrossref
54.
Ohkuma  H, Fujita  S, Suzuki  S.  Incidence of aneurysmal subarachnoid hemorrhage in Shimokita, Japan, from 1989 to 1998.  Stroke. 2002;33(1):195-199. doi:10.1161/hs0102.101891PubMedGoogle ScholarCrossref
55.
Turin  TC, Kita  Y, Rumana  N,  et al.  Ambient air pollutants and acute case-fatality of cerebro-cardiovascular events: Takashima Stroke and AMI Registry, Japan (1988-2004).  Cerebrovasc Dis. 2012;34(2):130-139. doi:10.1159/000339680PubMedGoogle ScholarCrossref
56.
Hamada  J, Morioka  M, Yano  S, Kai  Y, Ushio  Y.  Incidence and early prognosis of aneurysmal subarachnoid hemorrhage in Kumamoto Prefecture, Japan.  Neurosurgery. 2004;54(1):31-37. doi:10.1227/01.NEU.0000097196.55204.0BPubMedGoogle ScholarCrossref
57.
Omama  S, Yoshida  Y, Ogasawara  K,  et al.  Incidence rate of cerebrovascular diseases in northern Japan determined from the Iwate Stroke Registry with an inventory survey system.  J Stroke Cerebrovasc Dis. 2013;22(8):e317-e322. doi:10.1016/j.jstrokecerebrovasdis.2012.12.011PubMedGoogle ScholarCrossref
58.
Zhang  J, Liu  G, Arima  H,  et al; CHERISH Investigators.  Incidence and risks of subarachnoid hemorrhage in China.  Stroke. 2013;44(10):2891-2893. doi:10.1161/STROKEAHA.113.002599PubMedGoogle ScholarCrossref
59.
Azarpazhooh  MR, Etemadi  MM, Donnan  GA,  et al.  Excessive incidence of stroke in Iran: evidence from the Mashhad Stroke Incidence Study (MSIS), a population-based study of stroke in the Middle East.  Stroke. 2010;41(1):e3-e10. doi:10.1161/STROKEAHA.109.559708PubMedGoogle ScholarCrossref
60.
Dalal  PM, Malik  S, Bhattacharjee  M,  et al.  Population-based stroke survey in Mumbai, India: incidence and 28-day case fatality.  Neuroepidemiology. 2008;31(4):254-261. doi:10.1159/000165364PubMedGoogle ScholarCrossref
61.
Epstein  L, Rishpon  S, Bental  E,  et al.  Incidence, mortality, and case-fatality rate of stroke in northern Israel.  Stroke. 1989;20(6):725-729. doi:10.1161/01.STR.20.6.725PubMedGoogle ScholarCrossref
62.
Abdul-Ghaffar  NU, el-Sonbaty  MR, el-Din Abdul-Baky  MS, Marafie  AA, al-Said  AM.  Stroke in Kuwait: a three-year prospective study.  Neuroepidemiology. 1997;16(1):40-47. doi:10.1159/000109669PubMedGoogle ScholarCrossref
63.
Feigin  VL, Wiebers  DO, Nikitin  YP, O’Fallon  WM, Whisnant  JP.  Stroke epidemiology in Novosibirsk, Russia: a population-based study.  Mayo Clin Proc. 1995;70(9):847-852. doi:10.1016/S0025-6196(11)63942-6PubMedGoogle ScholarCrossref
64.
Anderson  CS, Jamrozik  KD, Burvill  PW, Chakera  TM, Johnson  GA, Stewart-Wynne  EG.  Determining the incidence of different subtypes of stroke: results from the Perth Community Stroke Study, 1989-1990.  Med J Aust. 1993;158(2):85-89.PubMedGoogle ScholarCrossref
65.
Islam  MS, Anderson  CS, Hankey  GJ,  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(3):776-782. doi:10.1161/STROKEAHA.107.493643PubMedGoogle ScholarCrossref
66.
Thrift  AG, Dewey  HM, Macdonell  RA, McNeil  JJ, Donnan  GA.  Incidence of the major stroke subtypes: initial findings from the North East Melbourne Stroke Incidence Study (NEMESIS).  Stroke. 2001;32(8):1732-1738. doi:10.1161/01.STR.32.8.1732PubMedGoogle ScholarCrossref
67.
Thrift  AG, Dewey  HM, Sturm  JW,  et al.  Incidence of stroke subtypes in the North East Melbourne Stroke Incidence Study (NEMESIS): differences between men and women.  Neuroepidemiology. 2009;32(1):11-18. doi:10.1159/000170086PubMedGoogle ScholarCrossref
68.
Leyden  JM, Kleinig  TJ, Newbury  J,  et al.  Adelaide stroke incidence study: declining stroke rates but many preventable cardioembolic strokes.  Stroke. 2013;44(5):1226-1231. doi:10.1161/STROKEAHA.113.675140PubMedGoogle ScholarCrossref
69.
Newbury  J, Kleinig  T, Leyden  J,  et al.  Stroke Epidemiology in an Australian Rural Cohort (SEARCH).  Int J Stroke. 2017;12(2):161-168. doi:10.1177/1747493016670174PubMedGoogle ScholarCrossref
70.
Bonita  R, Thomson  S.  Subarachnoid hemorrhage: epidemiology, diagnosis, management, and outcome.  Stroke. 1985;16(4):591-594. doi:10.1161/01.STR.16.4.591PubMedGoogle ScholarCrossref
71.
Truelsen  T, Bonita  R, Duncan  J, Anderson  NE, Mee  E.  Changes in subarachnoid hemorrhage mortality, incidence, and case fatality in New Zealand between 1981-1983 and 1991-1993.  Stroke. 1998;29(11):2298-2303. doi:10.1161/01.STR.29.11.2298PubMedGoogle ScholarCrossref
72.
Feigin  V, Carter  K, Hackett  M,  et al; Auckland Regional Community Stroke Study Group.  Ethnic disparities in incidence of stroke subtypes: Auckland Regional Community Stroke Study, 2002-2003.  Lancet Neurol. 2006;5(2):130-139. doi:10.1016/S1474-4422(05)70325-2PubMedGoogle ScholarCrossref
73.
Cantu-Brito  C, Majersik  JJ, Sánchez  BN,  et al.  Hospitalized stroke surveillance in the community of Durango, Mexico: the Brain Attack Surveillance in Durango study.  Stroke. 2010;41(5):878-884. doi:10.1161/STROKEAHA.109.577726PubMedGoogle ScholarCrossref
74.
Brown  RD, Whisnant  JP, Sicks  JD, O’Fallon  WM, Wiebers  DO.  Stroke incidence, prevalence, and survival: secular trends in Rochester, Minnesota, through 1989.  Stroke. 1996;27(3):373-380.PubMedGoogle Scholar
75.
Longstreth  WT  Jr, Nelson  LM, Koepsell  TD, van Belle  G.  Clinical course of spontaneous subarachnoid hemorrhage: a population-based study in King County, Washington.  Neurology. 1993;43(4):712-718. doi:10.1212/WNL.43.4.712PubMedGoogle ScholarCrossref
76.
Labovitz  DL, Halim  AX, Brent  B, Boden-Albala  B, Hauser  WA, Sacco  RL.  Subarachnoid hemorrhage incidence among whites, blacks and Caribbean Hispanics: the Northern Manhattan Study.  Neuroepidemiology. 2006;26(3):147-150. doi:10.1159/000091655PubMedGoogle ScholarCrossref
77.
Bahit  MC, Coppola  ML, Riccio  PM,  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(6):1640-1642. doi:10.1161/STROKEAHA.116.013637PubMedGoogle ScholarCrossref
78.
Minelli  C, Fen  LF, Minelli  DP.  Stroke incidence, prognosis, 30-day, and 1-year case fatality rates in Matão, Brazil: a population-based prospective study.  Stroke. 2007;38(11):2906-2911. doi:10.1161/STROKEAHA.107.484139PubMedGoogle ScholarCrossref
79.
Cabral  NL, Gonçalves  AR, Longo  AL,  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(7):755-761. doi:10.1136/jnnp.2009.172098PubMedGoogle ScholarCrossref
80.
Cabral  NL, Cougo-Pinto  PT, Magalhaes  PS,  et al.  Trends of stroke incidence from 1995 to 2013 in Joinville, Brazil.  Neuroepidemiology. 2016;46(4):273-281. doi:10.1159/000445060PubMedGoogle ScholarCrossref
81.
Smadja  D, Cabre  P, May  F,  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(12):2741-2747. doi:10.1161/hs1201.099385PubMedGoogle ScholarCrossref
82.
Wolfe  CD, Corbin  DO, Smeeton  NC,  et al.  Estimation of the risk of stroke in black populations in Barbados and South London.  Stroke. 2006;37(8):1986-1990. doi:10.1161/01.STR.0000230578.10937.a6PubMedGoogle ScholarCrossref
83.
Alvarez  G, Cox  P, Pairoa  M, García  M, Delgado  I, Lavados  PM.  Incidence of subarachnoid haemorrhage in the Aconcagua Valley, Chile: a community-based, prospective surveillance project.  J Neurol Neurosurg Psychiatry. 2010;81(7):778-782. doi:10.1136/jnnp.2009.192971PubMedGoogle ScholarCrossref
84.
Lavados  PM, Sacks  C, Prina  L,  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(9478):2206-2215. doi:10.1016/S0140-6736(05)66779-7PubMedGoogle ScholarCrossref
85.
Okon  M, Adebobola  NI, Julius  S,  et al.  Stroke incidence and case fatality rate in an urban population.  J Stroke Cerebrovasc Dis. 2015;24(4):771-777. doi:10.1016/j.jstrokecerebrovasdis.2014.11.004PubMedGoogle ScholarCrossref
86.
Kita  Y, Turin  TC, Ichikawa  M,  et al.  Trend of stroke incidence in a Japanese population: Takashima Stroke Registry, 1990-2001.  Int J Stroke. 2009;4(4):241-249. doi:10.1111/j.1747-4949.2009.00293.xPubMedGoogle ScholarCrossref
87.
ACROSS Group.  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(8):1843-1850. doi:10.1161/01.STR.31.8.1843PubMedGoogle ScholarCrossref
88.
Vemmos  KN, Bots  ML, Tsibouris  PK,  et al.  Stroke incidence and case fatality in southern Greece: the Arcadia Stroke Registry.  Stroke. 1999;30(2):363-370. doi:10.1161/01.STR.30.2.363PubMedGoogle ScholarCrossref
89.
Feigin  VL, Forouzanfar  MH, Krishnamurthi  R,  et al; Global Burden of Diseases, Injuries, and Risk Factors Study 2010 (GBD 2010) and the GBD Stroke Experts Group.  Global and regional burden of stroke during 1990-2010: findings from the Global Burden of Disease Study 2010.  Lancet. 2014;383(9913):245-254. doi:10.1016/S0140-6736(13)61953-4PubMedGoogle ScholarCrossref
90.
Etminan  N, Rinkel  GJ.  Unruptured intracranial aneurysms: development, rupture and preventive management.  Nat Rev Neurol. 2016;12(12):699-713. doi:10.1038/nrneurol.2016.150PubMedGoogle ScholarCrossref
91.
Jalbert  JJ, Isaacs  AJ, Kamel  H, Sedrakyan  A.  Clipping and coiling of unruptured intracranial aneurysms among Medicare beneficiaries, 2000 to 2010.  Stroke. 2015;46(9):2452-2457. doi:10.1161/STROKEAHA.115.009777PubMedGoogle ScholarCrossref
92.
Vlak  MH, Algra  A, Brandenburg  R, Rinkel  GJ.  Prevalence of unruptured intracranial aneurysms, with emphasis on sex, age, comorbidity, country, and time period: a systematic review and meta-analysis.  Lancet Neurol. 2011;10(7):626-636. doi:10.1016/S1474-4422(11)70109-0PubMedGoogle ScholarCrossref
93.
Huang  J, van Gelder  JM.  The probability of sudden death from rupture of intracranial aneurysms: a meta-analysis.  Neurosurgery. 2002;51(5):1101-1105. doi:10.1097/00006123-200211000-00001PubMedGoogle ScholarCrossref
94.
Bamford  J, Dennis  M, Sandercock  P, Burn  J, Warlow  C.  The frequency, causes and timing of death within 30 days of a first stroke: the Oxfordshire Community Stroke Project.  J Neurol Neurosurg Psychiatry. 1990;53(10):824-829. doi:10.1136/jnnp.53.10.824PubMedGoogle ScholarCrossref
95.
Feigin  VL, Wiebers  DO, Whisnant  JP, O’Fallon  WM.  Stroke incidence and 30-day case-fatality rates in Novosibirsk, Russia, 1982 through 1992.  Stroke. 1995;26(6):924-929. doi:10.1161/01.STR.26.6.924PubMedGoogle ScholarCrossref
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