Sex Differences in the Formation of Intracranial Aneurysms and Incidence and Outcome of Subarachnoid Hemorrhage: Review of Experimental and Human Studies
详细信息 查看全文
- 作者：Nefize Turan ; Robert Allen-James Heider…
- 关键词：Sex differences ; Intracranial aneurysm ; Subarachnoid hemorrhage
- 刊名：Translational Stroke Research
- 出版年：2016
- 出版时间：February 2016
- 年：2016
- 卷：7
- 期：1
- 页码：12-19
- 全文大小：523 KB
- 参考文献：1.Brisman JL, Song JK, Newell DW. Cerebral aneurysms. N Engl J Med. 2006;355(9):928–39. doi:10.1056/NEJMra052760 .CrossRef PubMed
2.Frosen J, Tulamo R, Paetau A, Laaksamo E, Korja M, Laakso A, et al. Saccular intracranial aneurysm: pathology and mechanisms. Acta Neuropathol. 2012;123(6):773–86. doi:10.1007/s00401-011-0939-3 .CrossRef PubMed
3.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(5):1197–201.CrossRef PubMed
4.Suarez JI, Tarr RW, Selman WR. Aneurysmal subarachnoid hemorrhage. N Engl J Med. 2006;354(4):387–96. doi:10.1056/NEJMra052732 .CrossRef PubMed
5.van Gijn J, Kerr RS, Rinkel GJ. Subarachnoid haemorrhage. Lancet. 2007;369(9558):306–18. doi:10.1016/S0140-6736(07)60153-6 .CrossRef PubMed
6.Alfano JM, Kolega J, Natarajan SK, Xiang J, Paluch RA, Levy EI, et al. Intracranial aneurysms occur more frequently at bifurcation sites that typically experience higher hemodynamic stresses. Neurosurgery. 2013;73(3):497–505. doi:10.1227/NEU.0000000000000016 .CrossRef PubMed
7.Tamura T, Jamous MA, Kitazato KT, Yagi K, Tada Y, Uno M, et al. Endothelial damage due to impaired nitric oxide bioavailability triggers cerebral aneurysm formation in female rats. J Hypertens. 2009;27(6):1284–92. doi:10.1097/HJH.0b013e328329d1a7 .CrossRef PubMed
8.Frosen J, Piippo A, Paetau A, Kangasniemi M, Niemela M, Hernesniemi J, et al. Remodeling of saccular cerebral artery aneurysm wall is associated with rupture: histological analysis of 24 unruptured and 42 ruptured cases. Stroke. 2004;35(10):2287–93. doi:10.1161/01.STR.0000140636.30204.da .CrossRef PubMed
9.Marbacher S, Marjamaa J, Bradacova K, von Gunten M, Honkanen P, Abo-Ramadan U, et al. Loss of mural cells leads to wall degeneration, aneurysm growth, and eventual rupture in a rat aneurysm model. Stroke. 2014;45(1):248–54. doi:10.1161/STROKEAHA.113.002745 .CrossRef PubMed
10.Laaksamo E, Tulamo R, Liiman A, Baumann M, Friedlander RM, Hernesniemi J, et al. Oxidative stress is associated with cell death, wall degradation, and increased risk of rupture of the intracranial aneurysm wall. Neurosurgery. 2013;72(1):109–17. doi:10.1227/NEU.0b013e3182770e8c .CrossRef PubMed
11.Inagawa T, Hirano A. Autopsy study of unruptured incidental intracranial aneurysms. Surg Neurol. 1990;34(6):361–5.CrossRef PubMed
12.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):626–36. doi:10.1016/S1474-4422(11)70109-0 .CrossRef PubMed
13.Harrod CG, Batjer HH, Bendok BR. Deficiencies in estrogen-mediated regulation of cerebrovascular homeostasis may contribute to an increased risk of cerebral aneurysm pathogenesis and rupture in menopausal and postmenopausal women. Med Hypotheses. 2006;66(4):736–56. doi:10.1016/j.mehy.2005.09.051 .CrossRef PubMed
14.Feigin VL, Rinkel GJ, Lawes CM, Algra A, Bennett DA, van Gijn J, et al. Risk factors for subarachnoid hemorrhage: an updated systematic review of epidemiological studies. Stroke J Cereb Circ. 2005;36(12):2773–80. doi:10.1161/01.STR.0000190838.02954.e8 .CrossRef
15.Juvela S, Poussa K, Porras M. Factors affecting formation and growth of intracranial aneurysms: a long-term follow-up study. Stroke. 2001;32(2):485–91.CrossRef PubMed
16.Kubo Y, Koji T, Kashimura H, Otawara Y, Ogawa A, Ogasawara K. Female sex as a risk factor for the growth of asymptomatic unruptured cerebral saccular aneurysms in elderly patients. J Neurosurg. 2014;121(3):599–604. doi:10.3171/2014.5.JNS132048 .CrossRef PubMed
17.Ostergaard JR, Hog E. Incidence of multiple intracranial aneurysms. Influence of arterial hypertension and gender. J Neurosurg. 1985;63(1):49–55. doi:10.3171/jns.1985.63.1.0049 .CrossRef PubMed
18.Ellamushi HE, Grieve JP, Jager HR, Kitchen ND. Risk factors for the formation of multiple intracranial aneurysms. J Neurosurg. 2001;94(5):728–32. doi:10.3171/jns.2001.94.5.0728 .CrossRef PubMed
19.Ghods AJ, Lopes D, Chen M. Gender differences in cerebral aneurysm location. Front Neurol. 2012;3:78. doi:10.3389/fneur.2012.00078 .PubMedCentral PubMed
20.Kongable GL, Lanzino G, Germanson TP, Truskowski LL, Alves WM, Torner JC, et al. Gender-related differences in aneurysmal subarachnoid hemorrhage. J Neurosurg. 1996;84(1):43–8. doi:10.3171/jns.1996.84.1.0043 .CrossRef PubMed
21.Jamous MA, Nagahiro S, Kitazato KT, Satomi J, Satoh K. Role of estrogen deficiency in the formation and progression of cerebral aneurysms. Part I: experimental study of the effect of oophorectomy in rats. J Neurosurg. 2005;103(6):1046–51. doi:10.3171/jns.2005.103.6.1046 .CrossRef PubMed
22.Jamous MA, Nagahiro S, Kitazato KT, Tamura T, Kuwayama K, Satoh K. Role of estrogen deficiency in the formation and progression of cerebral aneurysms. Part II: experimental study of the effects of hormone replacement therapy in rats. J Neurosurg. 2005;103(6):1052–7. doi:10.3171/jns.2005.103.6.1052 .CrossRef PubMed
23.Tada Y, Makino H, Furukawa H, Shimada K, Wada K, Liang EI, et al. Roles of estrogen in the formation of intracranial aneurysms in ovariectomized female mice. Neurosurgery. 2014;75(6):690–5. doi:10.1227/NEU.0000000000000528 . discussion 5.PubMedCentral CrossRef PubMed
24.Yasui N, Suzuki A, Nishimura H, Suzuki K, Abe T. Long-term follow-up study of unruptured intracranial aneurysms. Neurosurgery. 1997;40(6):1155–9. discussion 9–60.CrossRef PubMed
25.Wermer MJ, van der Schaaf IC, Algra A, Rinkel GJ. Risk of rupture of unruptured intracranial aneurysms in relation to patient and aneurysm characteristics: an updated meta-analysis. Stroke. 2007;38(4):1404–10. doi:10.1161/01.STR.0000260955.51401.cd .CrossRef PubMed
26.Greving JP, Wermer MJ, Brown Jr RD, Morita A, Juvela S, Yonekura M, et al. Development of the PHASES score for prediction of risk of rupture of intracranial aneurysms: a pooled analysis of six prospective cohort studies. Lancet Neurol. 2014;13(1):59–66. doi:10.1016/S1474-4422(13)70263-1 .CrossRef PubMed
27.Tada Y, Wada K, Shimada K, Makino H, Liang EI, Murakami S, et al. Estrogen protects against intracranial aneurysm rupture in ovariectomized mice. Hypertension. 2014;63(6):1339–44. doi:10.1161/HYPERTENSIONAHA.114.03300 .PubMedCentral CrossRef PubMed
28.Appelros P, Stegmayr B, Terent A. Sex differences in stroke epidemiology: a systematic review. Stroke. 2009;40(4):1082–90. doi:10.1161/STROKEAHA.108.540781 .CrossRef PubMed
29.Haberman S, Capildeo R, Rose FC. Sex differences in the incidence of cerebrovascular disease. J Epidemiol Community Health. 1981;35(1):45–50.PubMedCentral CrossRef PubMed
30.Korja M, Silventoinen K, Laatikainen T, Jousilahti P, Salomaa V, Hernesniemi J, et al. Risk factors and their combined effects on the incidence rate of subarachnoid hemorrhage—a population-based cohort study. PLoS One. 2013;8(9):e73760. doi:10.1371/journal.pone.0073760 .PubMedCentral CrossRef PubMed
31.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):1365–72. doi:10.1136/jnnp.2007.117655 .PubMedCentral CrossRef PubMed
32.Bonita R, Thomson S. Subarachnoid hemorrhage: epidemiology, diagnosis, management, and outcome. Stroke. 1985;16(4):591–4.CrossRef PubMed
33.Wong GK, Wun Tam YY, Zhu XL, Poon WS. Incidence and mortality of spontaneous subarachnoid hemorrhage in Hong Kong from 2002 to 2010: a Hong Kong hospital authority clinical management system database analysis. World Neurosurg. 2014;81(3–4):552–6. doi:10.1016/j.wneu.2013.07.128 .CrossRef PubMed
34.Risselada R, de Vries LM, Dippel DW, van Kooten F, van der Lugt A, Niessen WJ, et al. Incidence, treatment, and case-fatality of non-traumatic subarachnoid haemorrhage in the Netherlands. Clin Neurol Neurosurg. 2011;113(6):483–7. doi:10.1016/j.clineuro.2011.02.015 .CrossRef PubMed
35.Yamaguchi M, Sakurai H, Shimizu M, Tsushio Y, Nakagawa N, Masui T, et al. Analysis of complications and prognosis for different types of stroke patients registered between 1993 and 2000 in Aichi Prefecture. Nihon Koshu Eisei Zasshi. 2006;53(1):20–8.PubMed
36.Anderson CS, Feigin V, Bennett D, Lin RB, Hankey G, Jamrozik K. Active and passive smoking and the risk of subarachnoid hemorrhage: an international population-based case-control study. Stroke. 2004;35(3):633–7. doi:10.1161/01.STR.0000115751.45473.48 .CrossRef PubMed
37.Mhurchu CN, Anderson C, Jamrozik K, Hankey G, Dunbabin D. Hormonal factors and risk of aneurysmal subarachnoid hemorrhage: an international population-based, case-control study. Stroke. 2001;32(3):606–12.CrossRef PubMed
38.Okamoto K, Horisawa R, Kawamura T, Asai A, Ogino M, Takagi T, et al. Menstrual and reproductive factors for subarachnoid hemorrhage risk in women: a case-control study in Nagoya, Japan. Stroke. 2001;32(12):2841–4.CrossRef PubMed
39.Algra AM, Klijn CJ, Helmerhorst FM, Algra A, Rinkel GJ. Female risk factors for subarachnoid hemorrhage: a systematic review. Neurology. 2012;79(12):1230–6. doi:10.1212/WNL.0b013e31826aace6 .CrossRef PubMed
40.Kataoka H, Miyoshi T, Neki R, Yoshimatsu J, Ishibashi-Ueda H, Iihara K. Subarachnoid hemorrhage from intracranial aneurysms during pregnancy and the puerperium. Neurol Med Chir (Tokyo). 2013;53(8):549–54.CrossRef
41.Guida M, Altieri R, Palatucci V, Visconti F, Pascale R, Marra M, et al. Aneurysmal subarachnoid haemorrhage in pregnancy: a case series. Transl Med UniSa. 2012;2:59–63.PubMedCentral PubMed
42.Hamdan A, Barnes J, Mitchell P. Subarachnoid hemorrhage and the female sex: analysis of risk factors, aneurysm characteristics, and outcomes. J Neurosurg. 2014;121(6):1367–73. doi:10.3171/2014.7.JNS132318 .CrossRef PubMed
43.Gross BA, Rosalind Lai PM, Frerichs KU, Du R. Treatment modality and vasospasm after aneurysmal subarachnoid hemorrhage. World Neurosurg. 2014;82(6):e725–30. doi:10.1016/j.wneu.2013.08.017 .CrossRef PubMed
44.Rates of delayed rebleeding from intracranial aneurysms are low after surgical and endovascular treatment. Stroke. 2006;37(6):1437–42. doi:10.1161/01.STR.0000221331.01830.ce .
45.Kumar A, Brown R, Dhar R, Sampson T, Derdeyn CP, Moran CJ, et al. Early vs. delayed cerebral infarction after aneurysm repair after subarachnoid hemorrhage. Neurosurgery. 2013;73(4):617–23. doi:10.1227/NEU.0000000000000057 . discussion 23.CrossRef PubMed
46.Fisher CM, Roberson GH, Ojemann RG. Cerebral vasospasm with ruptured saccular aneurysm—the clinical manifestations. Neurosurgery. 1977;1(3):245–8.CrossRef PubMed
47.Vergouwen MD, Ilodigwe D, Macdonald RL. Cerebral infarction after subarachnoid hemorrhage contributes to poor outcome by vasospasm-dependent and -independent effects. Stroke. 2011;42(4):924–9. doi:10.1161/STROKEAHA.110.597914 .CrossRef PubMed
48.Vergouwen MD, Etminan N, Ilodigwe D, Macdonald RL. Lower incidence of cerebral infarction correlates with improved functional outcome after aneurysmal subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2011;31(7):1545–53. doi:10.1038/jcbfm.2011.56 .PubMedCentral CrossRef PubMed
49.Fergusen S, Macdonald RL. Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage. Neurosurgery. 2007;60(4):658–67. doi:10.1227/01.NEU.0000255396.23280.31 . discussion 67.CrossRef PubMed
50.Pegoli M, Mandrekar J, Rabinstein AA, Lanzino G. Predictors of excellent functional outcome in aneurysmal subarachnoid hemorrhage. J Neurosurg. 2015;122(2):414–8. doi:10.3171/2014.10.JNS14290 .CrossRef PubMed
51.Rivero Rodriguez D, Scherle Matamoros C, Fernandez Cue L, Miranda Hernandez JL, Pernas Sanchez Y, Perez NJ. Factors associated with poor outcome for aneurysmal subarachnoid haemorrhage in a series of 334 patients. Neurologia. 2015. doi:10.1016/j.nrl.2014.12.006 .PubMed
52.Jabbarli R, Reinhard M, Roelz R, Shah M, Niesen WD, Kaier K, et al. Early identification of individuals at high risk for cerebral infarction after aneurysmal subarachnoid hemorrhage: the BEHAVIOR score. J Cereb Blood Flow Metab. 2015. doi:10.1038/jcbfm.2015.81 .PubMed
53.Wunderle K, Hoeger KM, Wasserman E, Bazarian JJ. Menstrual phase as predictor of outcome after mild traumatic brain injury in women. J Head Trauma Rehabil. 2014;29(5):E1–8. doi:10.1097/HTR.0000000000000006 .CrossRef PubMed
54.Crago EA, Sherwood PR, Bender C, Balzer J, Ren D, Poloyac SM. Plasma estrogen levels are associated with severity of injury and outcomes after aneurysmal subarachnoid hemorrhage. Biol Res Nurs. 2014. doi:10.1177/1099800414561632 .PubMedCentral
55.Rincon F, Rossenwasser RH, Dumont A. The epidemiology of admissions of nontraumatic subarachnoid hemorrhage in the United States. Neurosurgery. 2013;73(2):217–22. doi:10.1227/01.neu.0000430290.93304.33 . discussion 2–3.CrossRef PubMed
56.Korja M, Silventoinen K, Laatikainen T, Jousilahti P, Salomaa V, Kaprio J. Cause-specific mortality of 1-year survivors of subarachnoid hemorrhage. Neurology. 2013;80(5):481–6. doi:10.1212/WNL.0b013e31827f0fb5 .PubMedCentral CrossRef PubMed
57.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):2059–63. doi:10.1161/01.STR.0000138451.07853.b6 .CrossRef PubMed
58.Friedrich V, Bederson JB, Sehba FA. Gender influences the initial impact of subarachnoid hemorrhage: an experimental investigation. PLoS One. 2013;8(11):e80101. doi:10.1371/journal.pone.0080101 .PubMedCentral CrossRef PubMed
59.Smith SL, Larson PG, Hall ED. A comparison of the effects of tirilazad on subarachnoid hemorrhage-induced blood
ain barrier permeability in male and female rats. J Stroke Cerebrovasc Dis. 1997;6(6):389–93.CrossRef PubMed
60.Macdonald RL. Delayed neurological deterioration after subarachnoid haemorrhage. Nat Rev Neurol. 2014;10(1):44–58. doi:10.1038/nrneurol.2013.246 .CrossRef PubMed
61.Miller BA, Turan N, Chau M, Pradilla G. Inflammation, vasospasm, and brain injury after subarachnoid hemorrhage. Biomed Res Int. 2014;2014:384342. doi:10.1155/2014/384342 .PubMedCentral PubMed
62.Lin CL, Dumont AS, Su YF, Dai ZK, Cheng JT, Tsai YJ, et al. Attenuation of subarachnoid hemorrhage-induced apoptotic cell death with 17 beta-estradiol. Laboratory investigation. J Neurosurg. 2009;111(5):1014–22. doi:10.3171/2009.3.JNS081660 .CrossRef PubMed
63.Wang Z, Zuo G, Shi XY, Zhang J, Fang Q, Chen G. Progesterone administration modulates cortical TLR4/NF-kappaB signaling pathway after subarachnoid hemorrhage in male rats. Mediat Inflamm. 2011;2011:848309. doi:10.1155/2011/848309 .
64.Yan F, Hu Q, Chen J, Wu C, Gu C, Chen G. Progesterone attenuates early brain injury after subarachnoid hemorrhage in rats. Neurosci Lett. 2013;543:163–7. doi:10.1016/j.neulet.2013.03.005 .CrossRef PubMed
65.Sun X, Ji C, Hu T, Wang Z, Chen G. Tamoxifen as an effective neuroprotectant against early brain injury and learning deficits induced by subarachnoid hemorrhage: possible involvement of inflammatory signaling. J Neuroinflammation. 2013;10:157. doi:10.1186/1742-2094-10-157 .PubMedCentral CrossRef PubMed
66.Chaichana KL, Pradilla G, Huang J, Tamargo RJ. Role of inflammation (leukocyte-endothelial cell interactions) in vasospasm after subarachnoid hemorrhage. World Neurosurg. 2010;73(1):22–41. doi:10.1016/j.surneu.2009.05.027 .CrossRef PubMed
67.Lin CL, Shih HC, Dumont AS, Kassell NF, Lieu AS, Su YF, et al. The effect of 17beta-estradiol in attenuating experimental subarachnoid hemorrhage-induced cerebral vasospasm. J Neurosurg. 2006;104(2):298–304. doi:10.3171/jns.2006.104.2.298 .CrossRef PubMed
68.Ding D, Starke RM, Dumont AS, Owens GK, Hasan DM, Chalouhi N, et al. Therapeutic implications of estrogen for cerebral vasospasm and delayed cerebral ischemia induced by aneurysmal subarachnoid hemorrhage. BioMed Res Int. 2014;2014:727428. doi:10.1155/2014/727428 .PubMedCentral PubMed
69.Chang CM, Su YF, Chang CZ, Chung CL, Tsai YJ, Loh JK, et al. Progesterone attenuates experimental subarachnoid hemorrhage-induced vasospasm by upregulation of endothelial nitric oxide synthase via Akt signaling pathway. BioMed Res Int. 2014;2014:207616. doi:10.1155/2014/207616 .PubMedCentral PubMed
70.Gurer B, Turkoglu E, Kertmen H, Karavelioglu E, Arikok AT, Sekerci Z. Attenuation of cerebral vasospasm and secondary injury by testosterone following experimental subarachnoid hemorrhage in rabbit. Acta Neurochir (Wien). 2014;156(11):2111–20. doi:10.1007/s00701-014-2211-9 . discussion 20.CrossRef
71.Zhao XD, Zhou YT. Effects of progesterone on intestinal inflammatory response and mucosa structure alterations following SAH in male rats. J Surg Res. 2011;171(1):e47–53. doi:10.1016/j.jss.2011.07.018 .CrossRef PubMed
72.Pedersen AT, Lidegaard O, Kreiner S, Ottesen B. Hormone replacement therapy and risk of non-fatal stroke. Lancet. 1997;350(9087):1277–83. doi:10.1016/S0140-6736(97)06005-4 .CrossRef PubMed
73.Bonita R. Cigarette smoking, hypertension and the risk of subarachnoid hemorrhage: a population-based case-control study. Stroke J Cereb Circ. 1986;17(5):831–5.CrossRef - 作者单位：Nefize Turan (1)
Robert Allen-James Heider (1)
Dobromira Zaharieva (1)
Faiz U. Ahmad (1)
Daniel L. Barrow (1)
Gustavo Pradilla (1)
1. Department of Neurological Surgery, Emory University School of Medicine, 1365 Clifton Rd. NE, Suite B6166, Atlanta, GA, 30322, USA - 刊物主题：Neurosciences; Neurology; Cardiology; Neurosurgery; Vascular Surgery;
- 出版者：Springer US
- ISSN：1868-601X
文摘
Intracranial aneurysms are defined as pathological dilatations of cerebral arteries and rupture of intracranial aneurysms leads to subarachnoid hemorrhage (SAH). The goal of this review was to outline the sex differences in the formation and progression of intracranial aneurysms as well as sex-related differences in incidence and outcome of SAH. The literature review was performed using PubMed with a combination of these search terms: “subarachnoid hemorrhage,” “incidence,” “outcome,” “sex,” “gender,” “male,” “female,” “experimental,” “mice,” and “rats.” Studies written in English were used. Female sex is thought to be a risk factor for aneurysm formation, especially in postmenopausal age populations, suggesting the potential protective involvement of sex steroids. Female sex is also considered a risk factor for SAH occurrence. Although incidence and mortality are confirmed to be higher in females in most studies, they elucidated no clear differences in the functional outcome among SAH survivors. The effect of gender on the pathophysiology of SAH is not very well understood; nevertheless, the majority of pre-clinical studies suggest a beneficial effect of sex steroids in experimental SAH. Moreover, conflicting results exist on the role and effect of hormone replacement therapies and oral contraceptive pills on the incidence and outcome of human SAH. Sex differences exist in the formation of aneurysms as well as the incidence and mortality of SAH. Potential therapeutic effects of sex steroids have been replicated in many animal studies, but their potential use in the treatment of acute SAH in human populations needs more future study. Keywords Sex differences Intracranial aneurysm Subarachnoid hemorrhage