Sex differences in incidence, pathophysiology, and outcome of primary intracerebral hemorrhage

Stroke

Volumn 46, Issue 3, 2015, Pages 886-892

  Gokhale, Sankalp ^a   Caplan, Louis R ^b   James, Michael L ^c  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Epidemiology; Gender; Intracerebral hemorrhage; Sex difference

Indexed keywords

AUSTRALIA AND NEW ZEALAND; BRAIN EDEMA; BRAIN HEMORRHAGE; CENTRAL AMERICA; CHINA; CLINICAL TRIAL (TOPIC); DEEP VEIN THROMBOSIS; EUROPE; HEMATOMA; HUMAN; INCIDENCE; JAPAN; MENOPAUSE; NORTH AMERICA; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SEIZURE; SEX DIFFERENCE; SOUTH AMERICA; AGED; ANIMAL; CEREBRAL HEMORRHAGE; ETHNIC GROUP; FEMALE; GEOGRAPHY; MALE; METABOLISM; MIDDLE AGED; PATIENT PARTICIPATION; RISK; TREATMENT OUTCOME;

HORMONE;

AGED; ANIMALS; CEREBRAL HEMORRHAGE; CLINICAL TRIALS AS TOPIC; ETHNIC GROUPS; FEMALE; GEOGRAPHY; HORMONES; HUMANS; INCIDENCE; MALE; MENOPAUSE; MIDDLE AGED; ODDS RATIO; PATIENT PARTICIPATION; SEX FACTORS; TREATMENT OUTCOME;

EID: 84929281636     PISSN: 00392499     EISSN: 15244628     Source Type: Journal    
DOI: 10.1161/STROKEAHA.114.007682     Document Type: Review

References (79)

1. Feigin VL, Lawes CM, Bennett DA, Barker-Collo SL, Parag V. Worldwide stroke incidence and early case fatality reported in 56 populationbased studies: a systematic review. Lancet Neurol. 2009;8:355-369. doi: 10.1016/S1474-4422 (09) 70025-0.
2. Flaherty ML, Woo D, Haverbusch M, Sekar P, Khoury J, Sauerbeck L, et al. Racial variations in location and risk of intracerebral hemorrhage. Stroke. 2005;36:934-937. doi: 10.1161/01. STR.0000160756.72109.95.
3. Mayer SA, Rincon F. Treatment of intracerebral haemorrhage. Lancet Neurol. 2005;4:662-672. doi: 10.1016/S1474-4422 (05) 70195-2.
4. Sivenius J, Tuomilehto J, Immonen-Räihä P, Kaarisalo M, Sarti C, Torppa J, et al; FINSTROKE study. Continuous 15-year decrease in incidence and mortality of stroke in Finland: the FINSTROKE study. Stroke. 2004;35:420-425. doi: 10.1161/01. STR.0000110220.63212.59.
5. Lovelock CE, Molyneux AJ, Rothwell PM; Oxford Vascular Study. Change in incidence and aetiology of intracerebral haemorrhage in Oxfordshire, UK, between 1981 and 2006: a population-based study. Lancet Neurol. 2007;6:487-493. doi: 10.1016/S1474-4422 (07) 70107-2.
6. van Asch CJ, Luitse MJ, Rinkel GJ, van der Tweel I, Algra A, Klijn CJ. Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis. Lancet Neurol. 2010;9:167-176. doi: 10.1016/S1474-4422 (09) 70340-0.
7. Islam MS, Anderson CS, Hankey GJ, Hardie K, Carter K, Broadhurst R, 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. doi: 10.1161/STROKEAHA.107.493643.
8. Benatru I, Rouaud O, Durier J, Contegal F, Couvreur G, Bejot Y, et al. Stable stroke incidence rates but improved case-fatality in Dijon, France, from 1985 to 2004. Stroke. 2006;37:1674-1679. doi: 10.1161/01. STR.0000226979.56456.a8.
9. Appelros P, Stegmayr B, Terént A. Sex differences in stroke epidemiology: a systematic review. Stroke. 2009;40:1082-1090. doi: 10.1161/STROKEAHA.108.540781.
10. 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;53:16-22.
11. Rothwell PM, Coull AJ, Silver LE, Fairhead JF, Giles MF, Lovelock CE, et al; Oxford Vascular Study. Population-based study of event-rate, incidence, case fatality, and mortality for all acute vascular events in all arterial territories (Oxford Vascular Study). Lancet. 2005;366:1773-1783. doi: 10.1016/S0140-6736 (05) 67702-1.
12. Bamford J, Sandercock P, Dennis M, Warlow C, Jones L, McPherson K, et al. A prospective study of acute cerebrovascular disease in the community: the Oxfordshire Community Stroke Project 1981-86. 1. Methodology, demography and incident cases of first-ever stroke. J Neurol Neurosurg Psychiatry. 1988;51:1373-1380.
13. 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;39:2204-2210. doi: 10.1161/STROKEAHA.107.507285.
14. Giroud M, Milan C, Beuriat P, Gras P, Essayagh E, Arveux P, et al. Incidence and survival rates during a two-year period of intracerebral and subarachnoid haemorrhages, cortical infarcts, lacunes and transient ischaemic attacks. The Stroke Registry of Dijon: 1985-1989. Int J Epidemiol. 1991;20:892-899.
15. Kolominsky-Rabas PL, Sarti C, Heuschmann PU, Graf C, Siemonsen S, Neundoerfer B, 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.
16. Fogelholm R, Nuutila M, Vuorela AL. Primary intracerebral haemorrhage in the Jyväskylä region, central Finland, 1985-89: incidence, case fatality rate, and functional outcome. J Neurol Neurosurg Psychiatry. 1992;55:546-552.
17. D'Alessandro G, Di Giovanni M, Roveyaz L, Iannizzi L, Compagnoni MP, Blanc S, et al. Incidence and prognosis of stroke in the Valle d'Aosta, Italy. First-year results of a community-based study. Stroke. 1992;23:1712-1715.
18. Lauria G, Gentile M, Fassetta G, Casetta I, Agnoli F, Andreotta G, et al. Incidence and prognosis of stroke in the Belluno province, Italy. Firstyear results of a community-based study. Stroke. 1995;26:1787-1793.
19. Di Carlo A, Inzitari D, Galati F, Baldereschi M, Giunta V, Grillo G, 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;16:410-417. doi: 10.1159/000072565.
20. D'Alessandro G, Bottacchi E, Di Giovanni M, Martinazzo C, Sironi L, Lia C, et al. Temporal trends of stroke in Valle d'Aosta, Italy. Incidence and 30-day fatality rates. Neurol Sci. 2000;21:13-18.
21. 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;24:26-31. doi: 10.1159/000081046.
22. Yesilot NF, Koyuncu BA, Coban O, Tuncay R, Bahar SZ. Gender differences in acute stroke: Istanbul medical school stroke registry. Neurol India. 2011;59:174-179. doi: 10.4103/0028-3886.79130.
23. Vemmos KN, Bots ML, Tsibouris PK, Zis VP, Grobbee DE, Stranjalis GS, et al. Stroke incidence and case fatality in southern Greece: the Arcadia stroke registry. Stroke. 1999;30:363-370.
24. Tveiten A, Ljøstad U, Mygland A, Thomassen L, Pripp AH, Naess H. Intracerebral hemorrhage in southern Norway-a hospital-based incidence study. Eur Neurol. 2012;67:240-245. doi: 10.1159/000336299.
25. 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;32:1732-1738.
26. Feigin V, Carter K, Hackett M, Barber PA, McNaughton H, Dyall L, 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;5:130-139. doi: 10.1016/S1474-4422 (05) 70325-2.
27. Thrift AG, Dewey HM, Sturm JW, Srikanth VK, Gilligan AK, Gall SL, 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. doi: 10.1159/000170086.
28. Labovitz DL, Halim A, Boden-Albala B, Hauser WA, Sacco RL. The incidence of deep and lobar intracerebral hemorrhage in whites, blacks, and Hispanics. Neurology. 2005;65:518-522. doi: 10.1212/01. wnl.0000172915.71933.00.
29. Kissela B, Schneider A, Kleindorfer D, Khoury J, Miller R, Alwell K, et al. Stroke in a biracial population: the excess burden of stroke among blacks. Stroke. 2004;35:426-431. doi: 10.1161/01. STR.0000110982.74967.39.
30. Rincon F, Mayer SA. The epidemiology of intracerebral hemorrhage in the United States from 1979 to 2008. Neurocrit Care. 2013;19:95-102. doi: 10.1007/s12028-012-9793-y.
31. Morikawa Y, Nakagawa H, Naruse Y, Nishijo M, Miura K, Tabata M, et al. Trends in stroke incidence and acute case fatality in a Japanese rural area: the Oyabe study. Stroke. 2000;31:1583-1587.
32. Inagawa T, Ohbayashi N, Takechi A, Shibukawa M, Yahara K. Primary intracerebral hemorrhage in Izumo City, Japan: incidence rates and outcome in relation to the site of hemorrhage. Neurosurgery. 2003;53:1283-1297, discussion 1297.
33. Kubo M, Kiyohara Y, Kato I, Tanizaki Y, Arima H, Tanaka K, et al. Trends in the incidence, mortality, and survival rate of cardiovascular disease in a Japanese community: the Hisayama study. Stroke. 2003;34:2349-2354. doi: 10.1161/01. STR.0000090348.52943. A2.
34. Ishikawa S, Kayaba K, Gotoh T, Nago N, Nakamura Y, Tsutsumi A, et al. Incidence of total stroke, stroke subtypes, and myocardial infarction in the Japanese population: the JMS Cohort Study. J Epidemiol. 2008;18:144-150.
35. Jiang B, Wang WZ, Chen H, Hong Z, Yang QD, Wu SP, et al. Incidence and trends of stroke and its subtypes in China: results from three large cities. Stroke. 2006;37:63-68. doi: 10.1161/01. STR.0000194955.34820.78.
36. Wang WJ, Lu JJ, Wang YJ, Wang CX, Wang YL, Hoff K, et al; China National Stroke Registry (CNSR). Clinical characteristics, management, and functional outcomes in Chinese patients within the first year after intracerebral hemorrhage: analysis from China National Stroke Registry. CNS Neurosci Ther. 2012;18:773-780. doi: 10.1111/j.1755-5949.2012.00367.x.
37. Lavados PM, Sacks C, Prina L, Escobar A, Tossi C, Araya F, 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. doi: 10.1016/S0140-6736 (05) 66779-7.
38. 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;38:2906-2911. doi: 10.1161/STROKEAHA.107.484139.
39. Ruiz-Sandoval JL, Chiquete E, Gárate-Carrillo A, Ochoa-Guzmán A, Arauz A, León-Jiménez C, et al; RENAMEVASC investigators. Spontaneous intracerebral hemorrhage in Mexico: results from a Multicenter Nationwide Hospital-based Registry on Cerebrovascular Disease (RENAMEVASC). Rev Neurol. 2011;53:705-712.
40. Ganti L, Jain A, Yerragondu N, Jain M, Bellolio MF, Gilmore RM, et al. Female gender remains an independent risk factor for poor outcome after acute nontraumatic intracerebral hemorrhage. Neurol Res Int. 2013;2013:219097. doi: 10.1155/2013/219097.
41. Wagner I, Volbers B, Kloska S, Doerfler A, Schwab S, Staykov D. Sex differences in perihemorrhagic edema evolution after spontaneous intracerebral hemorrhage. Eur J Neurol. 2012;19:1477-1481. doi: 10.1111/j.1468-1331.2011.03628.x.
42. Anderson CS, Huang Y, Wang JG, Arima H, Neal B, Peng B, et al; INTERACT Investigators. Intensive blood pressure reduction in acute cerebral haemorrhage trial (INTERACT): a randomised pilot trial. Lancet Neurol. 2008;7:391-399. doi: 10.1016/S1474-4422 (08) 70069-3.
43. Qureshi AI, Bliwise DL, Bliwise NG, Akbar MS, Uzen G, Frankel MR. Rate of 24-hour blood pressure decline and mortality after spontaneous intracerebral hemorrhage: a retrospective analysis with a random effects regression model. Crit Care Med. 1999;27:480-485.
44. Claassen J, Jetté N, Chum F, Green R, Schmidt M, Choi H, et al. Electrographic seizures and periodic discharges after intracerebral hemorrhage. Neurology. 2007;69:1356-1365. doi: 10.1212/01. wnl.0000281664.02615.6c.
45. De Reuck J, Hemelsoet D, Van Maele G. Seizures and epilepsy in patients with a spontaneous intracerebral haematoma. Clin Neurol Neurosurg. 2007;109:501-504. doi: 10.1016/j.clineuro.2007.04.001.
46. Kawase K, Okazaki S, Toyoda K, Toratani N, Yoshimura S, Kawano H, et al. Sex difference in the prevalence of deep-vein thrombosis in Japanese patients with acute intracerebral hemorrhage. Cerebrovasc Dis. 2009;27:313-319. doi: 10.1159/000202006.
47. Goldstein JN, Fazen LE, Wendell L, Chang Y, Rost NS, Snider R, et al. Risk of thromboembolism following acute intracerebral hemorrhage. Neurocrit Care. 2009;10:28-34. doi: 10.1007/s12028-008-9134-3.
48. Creutzfeldt CJ, Becker KJ, Weinstein JR, Khot SP, McPharlin TO, Ton TG, et al. Do-not-attempt-resuscitation orders and prognostic models for intraparenchymal hemorrhage. Crit Care Med. 2011;39:158-162. doi: 10.1097/CCM.0b013e3181fb7b49.
49. Brizzi M, Abul-Kasim K, Jalakas M, Selariu E, Pessah-Rasmussen H, Zia E. Early do-not-resuscitate orders in intracerebral haemorrhage; frequency and predictive value for death and functional outcome. A retrospective cohort study. Scand J Trauma Resusc Emerg Med. 2012;20:36. doi: 10.1186/1757-7241-20-36.
50. Zahuranec DB, Brown DL, Lisabeth LD, Gonzales NR, Longwell PJ, Smith MA, et al. Early care limitations independently predict mortality after intracerebral hemorrhage. Neurology. 2007;68:1651-1657. doi: 10.1212/01.wnl.0000261906.93238.72.
51. Fogelholm R, Murros K, Rissanen A, Avikainen S. Long term survival after primary intracerebral haemorrhage: a retrospective population based study. J Neurol Neurosurg Psychiatry. 2005;76:1534-1538. doi: 10.1136/jnnp. 2004.055145.
52. Nilsson OG, Lindgren A, Brandt L, Säveland H. Prediction of death in patients with primary intracerebral hemorrhage: a prospective study of a defined population. J Neurosurg. 2002;97:531-536. doi: 10.3171/jns.2002.97.3.0531.
53. Franke CL, van Swieten JC, Algra A, van Gijn J. Prognostic factors in patients with intracerebral haematoma. J Neurol Neurosurg Psychiatry. 1992;55:653-657.
54. Rodriguez-Luna D, Rubiera M, Ribo M, Coscojuela P, Piñeiro S, Pagola J, et al. Ultraearly hematoma growth predicts poor outcome after acute intracerebral hemorrhage. Neurology. 2011;77:1599-1604. doi: 10.1212/WNL.0b013e3182343387.
55. Kimura Y, Takishita S, Muratani H, Kinjo K, Shinzato Y, Muratani A, et al. Demographic study of first-ever stroke and acute myocardial infarction in Okinawa, Japan. Intern Med. 1998;37:736-745.
56. Zhang LF, Yang J, Hong Z, Yuan GG, Zhou BF, Zhao LC, et al; Collaborative Group of China Multicenter Study of Cardiovascular Epidemiology. Proportion of different subtypes of stroke in China. Stroke. 2003;34:2091-2096. doi: 10.1161/01. STR.0000087149.42294.8C.
57. Sheikh K, Bullock CM. Effect of measurement on sex difference in stroke mortality. Stroke. 2007;38:1085-1087. doi: 10.1161/01. STR.0000258103.15708.58.
58. Ayala C, Croft JB, Greenlund KJ, Keenan NL, Donehoo RS, Malarcher AM, et al. Sex differences in US mortality rates for stroke and stroke subtypes by race/ethnicity and age, 1995-1998. Stroke. 2002;33:1197-1201.
59. Zia E, Engström G, Svensson PJ, Norrving B, Pessah-Rasmussen H. Three-year survival and stroke recurrence rates in patients with primary intracerebral hemorrhage. Stroke. 2009;40:3567-3573. doi: 10.1161/STROKEAHA.109.556324.
60. Umeano O, Phillips-Bute B, Hailey CE, Sun W, Gray MC, Roulhac-Wilson B, et al. Gender and age interact to affect early outcome after intracerebral hemorrhage. PLoS One. 2013;8:e81664. doi: 10.1371/journal. pone.0081664.
61. Rodriguez-Luna D, Rubiera M, Ribo M, Coscojuela P, Pagola J, Piñeiro S, et al. Serum low-density lipoprotein cholesterol level predicts hematoma growth and clinical outcome after acute intracerebral hemorrhage. Stroke. 2011;42:2447-2452. doi: 10.1161/STROKEAHA.110.609461.
62. Burke JF, Brown DL, Lisabeth LD, Sanchez BN, Morgenstern LB. Enrollment of women and minorities in NINDS trials. Neurology. 2011;76:354-360. doi: 10.1212/WNL.0b013e3182088260.
63. Mendelow AD, Gregson BA, Fernandes HM, Murray GD, Teasdale GM, Hope DT, et al; STICH investigators. Early surgery versus initial conservative treatment in patients with spontaneous supratentorial intracerebral haematomas in the International Surgical Trial in Intracerebral Haemorrhage (STICH): a randomised trial. Lancet. 2005;365:387-397. doi: 10.1016/S0140-6736 (05) 17826-X.
64. Lyden PD, Shuaib A, Lees KR, Davalos A, Davis SM, Diener HC, et al; CHANT Trial Investigators. Safety and tolerability of NXY-059 for acute intracerebral hemorrhage: the CHANT Trial. Stroke. 2007;38:2262-2269. doi: 10.1161/STROKEAHA.106.472746.
65. Mayer SA, Brun NC, Begtrup K, Broderick J, Davis S, Diringer MN, et al; FAST Trial Investigators. Efficacy and safety of recombinant activated factor VII for acute intracerebral hemorrhage. N Engl J Med. 2008;358:2127-2137. doi: 10.1056/NEJMoa0707534.
66. Mendelow AD, Gregson BA, Rowan EN, Murray GD, Gholkar A, Mitchell PM; STICH II Investigators. Early surgery versus initial conservative treatment in patients with spontaneous supratentorial lobar intracerebral haematomas (STICH II): a randomised trial. Lancet. 2013;382:397-408. doi: 10.1016/S0140-6736 (13) 60986-1.
67. Herson PS, Koerner IP, Hurn PD. Sex, sex steroids, and brain injury. Semin Reprod Med. 2009;27:229-239. doi: 10.1055/s-0029-1216276.
68. Feldmann E, Broderick JP, Kernan WN, Viscoli CM, Brass LM, Brott T, et al. Major risk factors for intracerebral hemorrhage in the young are modifiable. Stroke. 2005;36:1881-1885. doi: 10.1161/01. STR.0000177480.62341.6b.
69. Chen TY, Tsai KL, Lee TY, Chiueh CC, Lee WS, Hsu C. Sex-specific role of thioredoxin in neuroprotection against iron-induced brain injury conferred by estradiol. Stroke. 2010;41:160-165. doi: 10.1161/STROKEAHA.109.562850.
70. Nakamura T, Xi G, Keep RF, Wang M, Nagao S, Hoff JT, et al. Effects of endogenous and exogenous estrogen on intracerebral hemorrhage-induced brain damage in rats. Acta Neurochir Suppl. 2006;96:218-221.
71. Lei B, Mace B, Bellows ST, Sullivan PM, Vitek MP, Laskowitz DT, et al. Interaction between sex and apolipoprotein e genetic background in a murine model of intracerebral hemorrhage. Transl Stroke Res. 2012;3:94-101. doi: 10.1007/s12975-012-0176-7.
72. Regan RF, Guo Y. Estrogens attenuate neuronal injury due to hemoglobin, chemical hypoxia, and excitatory amino acids in murine cortical cultures. Brain Res. 1997;764:133-140.
73. Gu Y, Xi G, Liu W, Keep RF, Hua Y. Estrogen reduces iron-mediated brain edema and neuronal death. Acta Neurochir Suppl. 2010;106:159-162. doi: 10.1007/978-3-211-98811-4-29.
74. Nakamura T, Hua Y, Keep RF, Park JW, Xi G, Hoff JT. Estrogen therapy for experimental intracerebral hemorrhage in rats. J Neurosurg. 2005;103:97-103. doi: 10.3171/jns.2005.103.1.0097.
75. Nguyen AP, Arvanitidis AP, Colbourne F. Failure of estradiol to improve spontaneous or rehabilitation-facilitated recovery after hemorrhagic stroke in rats. Brain Res. 2008;1193:109-119. doi: 10.1016/j. brainres.2007.11.054.
76. Auriat A, Plahta WC, McGie SC, Yan R, Colbourne F. 17beta-Estradiol pretreatment reduces bleeding and brain injury after intracerebral hemorrhagic stroke in male rats. J Cereb Blood Flow Metab. 2005;25:247-256. doi: 10.1038/sj.jcbfm.9600026.
77. Chen Z, Xi G, Mao Y, Keep RF, Hua Y. Effects of progesterone and testosterone on ICH-induced brain injury in rats. Acta Neurochir Suppl. 2011;111:289-293. doi: 10.1007/978-3-7091-0693-8-48.
78. Woo D, Rosand J, Kidwell C, McCauley JL, Osborne J, Brown MW, et al. The Ethnic/Racial Variations of Intracerebral Hemorrhage (ERICH) study protocol. Stroke. 2013;44:e120-e125. doi: 10.1161/STROKEAHA.113.002332.
79. Fisher M, Feuerstein G, Howells DW, Hurn PD, Kent TA, Savitz SI, et al; STAIR Group. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke. 2009;40:2244-2250. doi: 10.1161/STROKEAHA.108.541128.