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Sex Differences in the Formation of Intracranial Aneurysms and Incidence and Outcome of Subarachnoid Hemorrhage: Review of Experimental and Human Studies

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Abstract

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.

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References

  1. Brisman JL, Song JK, Newell DW. Cerebral aneurysms. N Engl J Med. 2006;355(9):928–39. doi:10.1056/NEJMra052760.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  4. Suarez JI, Tarr RW, Selman WR. Aneurysmal subarachnoid hemorrhage. N Engl J Med. 2006;354(4):387–96. doi:10.1056/NEJMra052732.

    Article  CAS  PubMed  Google Scholar 

  5. van Gijn J, Kerr RS, Rinkel GJ. Subarachnoid haemorrhage. Lancet. 2007;369(9558):306–18. doi:10.1016/S0140-6736(07)60153-6.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  11. Inagawa T, Hirano A. Autopsy study of unruptured incidental intracranial aneurysms. Surg Neurol. 1990;34(6):361–5.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  19. Ghods AJ, Lopes D, Chen M. Gender differences in cerebral aneurysm location. Front Neurol. 2012;3:78. doi:10.3389/fneur.2012.00078.

    PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  29. Haberman S, Capildeo R, Rose FC. Sex differences in the incidence of cerebrovascular disease. J Epidemiol Community Health. 1981;35(1):45–50.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

  32. Bonita R, Thomson S. Subarachnoid hemorrhage: epidemiology, diagnosis, management, and outcome. Stroke. 1985;16(4):591–4.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    PubMed Central  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  46. Fisher CM, Roberson GH, Ojemann RG. Cerebral vasospasm with ruptured saccular aneurysm—the clinical manifestations. Neurosurgery. 1977;1(3):245–8.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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  Google Scholar 

  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  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  59. Smith SL, Larson PG, Hall ED. A comparison of the effects of tirilazad on subarachnoid hemorrhage-induced blood-brain barrier permeability in male and female rats. J Stroke Cerebrovasc Dis. 1997;6(6):389–93.

    Article  CAS  PubMed  Google Scholar 

  60. Macdonald RL. Delayed neurological deterioration after subarachnoid haemorrhage. Nat Rev Neurol. 2014;10(1):44–58. doi:10.1038/nrneurol.2013.246.

    Article  CAS  PubMed  Google Scholar 

  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.

    PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    PubMed Central  PubMed  Google Scholar 

  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.

    PubMed Central  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

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  1. Department of Neurological Surgery, Emory University School of Medicine, 1365 Clifton Rd. NE, Suite B6166, Atlanta, GA, 30322, USA

    Nefize Turan, Robert Allen-James Heider, Dobromira Zaharieva, Faiz U. Ahmad, Daniel L. Barrow & Gustavo Pradilla

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Turan, N., Heider, R.AJ., Zaharieva, D. et al. Sex Differences in the Formation of Intracranial Aneurysms and Incidence and Outcome of Subarachnoid Hemorrhage: Review of Experimental and Human Studies. Transl. Stroke Res. 7, 12–19 (2016). https://doi.org/10.1007/s12975-015-0434-6

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