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Aneurysmal Subarachnoid Hemorrhage and Sex Differences: Analysis of Epidemiology, Outcomes, and Risk Factors

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Abstract

Background

The differences in outcomes after aneurysmal subarachnoid hemorrhage (aSAH) between the sexes have not been concretely determined. This study aimed to evaluate the differences in epidemiology, outcomes, and risk factors between male and female patients with aSAH.

Methods

We performed a multicenter, retrospective study of patients with aSAH from 2017 to 2020. We investigated the epidemiological differences between the two sexes. Propensity score matching (PSM) was used to compare short-term outcomes between the sexes. Binary logarithmic regression was performed to investigate the odds ratio (OR) for dependent survival in patients of different sexes.

Results

A total of 5,407 consecutive patients with aSAH were included in this study, and the female-to-male ratio was 1.8:1. The peak incidence of aSAH occurred in the 6th and 7th decades in males and females, respectively. There were more female patients with internal carotid artery or posterior communicating artery aneurysms (53.2%), and there were more male patients with anterior cerebral artery or anterior communicating artery aneurysms (43.2%). The incidence of multiple aneurysms was greater in female patients (21.5% vs. 14.2%, P < 0.001). There was no significant difference in outcomes before and after PSM at discharge. The dependent survival risk was related only to the clinical condition on admission in women. In addition, age > 50 years (OR 1.88, 95% confidence interval 1.17–3.02; P = 0.01) and hypertension (OR 1.81, 95% confidence interval 1.25–2.61; P = 0.002) were also risk factors for male patients.

Conclusions

There were more female patients with aneurysms than male patients in this study. Most aneurysm locations were different between the two groups. There was no significant difference in discharge outcomes before and after PSM. The risk factors for dependent survival were different between female and male patients.

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References

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  3. Fuentes AM, Stone McGuire L, Amin-Hanjani S. Sex differences in cerebral aneurysms and subarachnoid hemorrhage. Stroke. 2022;53(2):624–33. https://doi.org/10.1161/STROKEAHA.121.037147.

    Article  PubMed  Google Scholar 

  4. 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. https://doi.org/10.1136/jnnp.2007.117655.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Kaminogo M, Yonekura M, Shibata S. Incidence and outcome of multiple intracranial aneurysms in a defined population. Stroke. 2003;34(1):16–21. https://doi.org/10.1161/01.str.0000046763.48330.ad.

    Article  PubMed  Google Scholar 

  6. Juvela S. Risk factors for multiple intracranial aneurysms. Stroke. 2000;31(2):392–7. https://doi.org/10.1161/01.str.31.2.392.

    Article  PubMed  CAS  Google Scholar 

  7. 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. https://doi.org/10.1161/01.STR.0000260955.51401.cd.

    Article  PubMed  Google Scholar 

  8. Yang Y, Wang B, Ge X, et al. Natural course of ruptured but untreated intracranial aneurysms: a multicenter 2-year follow-up study. Stroke. 2023;54(8):2087–95. https://doi.org/10.1161/strokeaha.123.042530.

    Article  PubMed  CAS  Google Scholar 

  9. 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. https://doi.org/10.3171/2014.7.JNS132318.

    Article  PubMed  Google Scholar 

  10. Lindner SH, Bor AS, Rinkel GJ. Differences in risk factors according to the site of intracranial aneurysms. J Neurol Neurosurg Psychiatry. 2010;81(1):116–8. https://doi.org/10.1136/jnnp.2008.163063.

    Article  PubMed  CAS  Google Scholar 

  11. Locksley HB. Natural history of subarachnoid hemorrhage, intracranial aneurysms and arteriovenous malformations. Based on 6368 cases in the cooperative study. J Neurosurg. 1966;25(2):219–39. https://doi.org/10.3171/jns.1966.25.2.0219.

    Article  PubMed  CAS  Google Scholar 

  12. Aarhus M, Helland CA, Wester K. Differences in anatomical distribution, gender, and sidedness between ruptured and unruptured intracranial aneurysms in a defined patient population. Acta Neurochir (Wien). 2009;151(12):1569–74. https://doi.org/10.1007/s00701-009-0316-3.

    Article  PubMed  Google Scholar 

  13. Molenberg R, Thio CHL, Aalbers MW, et al. Sex hormones and risk of aneurysmal subarachnoid hemorrhage: a Mendelian randomization study. Stroke. 2022;53(9):2870–5. https://doi.org/10.1161/STROKEAHA.121.038035.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. McDowell MM, Zhao Y, Kellner CP, et al. Demographic and clinical predictors of multiple intracranial aneurysms in patients with subarachnoid hemorrhage. J Neurosurg. 2018;128(4):961–8. https://doi.org/10.3171/2017.1.JNS162785.

    Article  PubMed  Google Scholar 

  15. Horikoshi T, Akiyama I, Yamagata Z, Sugita M, Nukui H. Magnetic resonance angiographic evidence of sex-linked variations in the circle of willis and the occurrence of cerebral aneurysms. J Neurosurg. 2002;96(4):697–703. https://doi.org/10.3171/jns.2002.96.4.0697.

    Article  PubMed  Google Scholar 

  16. Lindekleiv HM, Valen-Sendstad K, Morgan MK, et al. Sex differences in intracranial arterial bifurcations. Gend Med. 2010;7(2):149–55. https://doi.org/10.1016/j.genm.2010.03.003.

    Article  PubMed  Google Scholar 

  17. Schupper AJ, Hardigan TA, Mehta A, et al. Sex and racial disparity in outcome of aneurysmal subarachnoid hemorrhage in the United States: a 20-year analysis. Stroke. 2023;54(5):1347–56. https://doi.org/10.1161/strokeaha.122.041488.

    Article  PubMed  Google Scholar 

  18. Turan N, Heider RA, Zaharieva D, Ahmad FU, Barrow DL, Pradilla G. Sex differences in the formation of intracranial aneurysms and incidence and outcome of subarachnoid hemorrhage: review of experimental and human studies. Transl Stroke Res. 2016;7(1):12–9. https://doi.org/10.1007/s12975-015-0434-6.

    Article  PubMed  Google Scholar 

  19. Acosta JN, Szejko N, Both CP, et al. Genetically determined smoking behavior and risk of nontraumatic subarachnoid hemorrhage. Stroke. 2021;52(2):582–7. https://doi.org/10.1161/strokeaha.120.031622.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Pegoli M, Mandrekar J, Rabinstein AA, Lanzino G. Predictors of excellent functional outcome in aneurysmal subarachnoid hemorrhage. J Neurosurg. 2015;122(2):414–8. https://doi.org/10.3171/2014.10.JNS14290.

    Article  PubMed  Google Scholar 

  21. Jabbarli R, Reinhard M, Roelz R, 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;35(10):1587–92. https://doi.org/10.1038/jcbfm.2015.81.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Larrew T, Pryor W 3rd, Weinberg J, et al. Aneurysmal subarachnoid hemorrhage: a statewide assessment of outcome based on risk factors, aneurysm characteristics, and geo-demography. J Neurointerv Surg. 2015;7(11):855–60. https://doi.org/10.1136/neurintsurg-2014-011359.

    Article  PubMed  Google Scholar 

  23. Galea JP, Dulhanty L, Patel HC, UK, Ireland Subarachnoid Hemorrhage Database C. Predictors of outcome in aneurysmal subarachnoid hemorrhage patients: observations from a multicenter data set. Stroke. 2017;48(11):2958–63. https://doi.org/10.1161/STROKEAHA.117.017777.

    Article  PubMed  Google Scholar 

  24. Rosenlrn J, Eskesen V, Schmidt K. Clinical features and outcome in females and males with ruptured intracranial saccular aneurysms. Br J Neurosurg. 1993;7(3):287–90. https://doi.org/10.3109/02688699309023811.

    Article  PubMed  CAS  Google Scholar 

  25. Tam AK, Ilodigwe D, Mocco J, et al. Impact of systemic inflammatory response syndrome on vasospasm, cerebral infarction, and outcome after subarachnoid hemorrhage: exploratory analysis of CONSCIOUS-1 database. Neurocrit Care. 2010;13(2):182–9. https://doi.org/10.1007/s12028-010-9402-x.

    Article  PubMed  Google Scholar 

  26. Lambert G, Naredi S, Eden E, Rydenhag B, Friberg P. Monoamine metabolism and sympathetic nervous activation following subarachnoid haemorrhage: influence of gender and hydrocephalus. Brain Res Bull. 2002;58(1):77–82. https://doi.org/10.1016/s0361-9230(02)00762-1.

    Article  PubMed  CAS  Google Scholar 

  27. Dasenbrock HH, Rudy RF, Rosalind Lai PM, et al. Cigarette smoking and outcomes after aneurysmal subarachnoid hemorrhage: a nationwide analysis. J Neurosurg. 2018;129(2):446–57. https://doi.org/10.3171/2016.10.JNS16748.

    Article  PubMed  Google Scholar 

  28. Bögli SY, Utebay D, Smits N, et al. Sex-related differences of invasive therapy in patients with aneurysmal subarachnoid hemorrhage. Acta Neurochir (Wien). 2022;164(11):2899–908. https://doi.org/10.1007/s00701-022-05345-0.

    Article  PubMed  Google Scholar 

  29. Hammer A, Steiner A, Ranaie G, et al. Impact of comorbidities and smoking on the outcome in aneurysmal subarachnoid hemorrhage. Sci Rep. 2018;8(1):12335. https://doi.org/10.1038/s41598-018-30878-9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Slettebø H, Karic T, Sorteberg A. Impact of smoking on course and outcome of aneurysmal subarachnoid hemorrhage. Acta Neurochir (Wien). 2020;162(12):3117–28. https://doi.org/10.1007/s00701-020-04506-3.

    Article  PubMed  Google Scholar 

  31. Broderick JP, Brott TG, Duldner JE, Tomsick T, Leach A. Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke. 1994;25(7):1342–7. https://doi.org/10.1161/01.str.25.7.1342.

    Article  PubMed  CAS  Google Scholar 

  32. Hawkins RI. Smoking, platelets and thrombosis. Nature. 1972;236(5348):450–2. https://doi.org/10.1038/236450a0.

    Article  PubMed  CAS  Google Scholar 

  33. Lasner TM, Weil RJ, Riina HA, et al. Cigarette smoking-induced increase in the risk of symptomatic vasospasm after aneurysmal subarachnoid hemorrhage. J Neurosurg. 1997;87(3):381–4. https://doi.org/10.3171/jns.1997.87.3.0381.

    Article  PubMed  CAS  Google Scholar 

  34. Weir BK, Kongable GL, Kassell NF, Schultz JR, Truskowski LL, Sigrest A. Cigarette smoking as a cause of aneurysmal subarachnoid hemorrhage and risk for vasospasm: a report of the Cooperative Aneurysm Study. J Neurosurg. 1998;89(3):405–11. https://doi.org/10.3171/jns.1998.89.3.0405.

    Article  PubMed  CAS  Google Scholar 

  35. Pobereskin LH. Influence of premorbid factors on survival following subarachnoid hemorrhage. J Neurosurg. 2001;95(4):555–9. https://doi.org/10.3171/jns.2001.95.4.0555.

    Article  PubMed  CAS  Google Scholar 

  36. Carandang RA, Barton B, Rordorf GA, Ogilvy CS, Sims JR. Nicotine replacement therapy after subarachnoid hemorrhage is not associated with increased vasospasm. Stroke. 2011;42(11):3080–6. https://doi.org/10.1161/STROKEAHA.111.620955.

    Article  PubMed  CAS  Google Scholar 

  37. Seder DB, Schmidt JM, Badjatia N, et al. Transdermal nicotine replacement therapy in cigarette smokers with acute subarachnoid hemorrhage. Neurocrit Care. 2011;14(1):77–83. https://doi.org/10.1007/s12028-010-9456-9.

    Article  PubMed  CAS  Google Scholar 

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Funding

This work was supported by the Tianjin Medical University General Hospital Clinical Research Program (Grant No. 22ZYYLCCG07) and the Natural Science Foundation of Tianjin, China (Grant No. 20JCZDJC00300).

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Author notes

  1. Chao Peng, Yan Zhao, and Fan Li are contributed equally to this work. They are co-first authors.

Authors and Affiliations

  1. Department of Neurosurgery, Tianjin Medical University General Hospital, Tianjin, People’s Republic of China

    Chao Peng, Yan Zhao, Bang-yue Wang, Jian Li, Heng-rui Zhang, Yi-fan Yang & Xin-yu Yang

  2. Department of Neurosurgery, Heji Hospital Affiliated to Changzhi Medical College, Changzhi, Shanxi Province, People’s Republic of China

    Fan Li, Tie-zhu Guo, Xiang-dong Wang & Xin-liang Ren

  3. Department of Neurosurgery, Heping Hospital Affiliated to Changzhi Medical College, Changzhi, Shanxi Province, People’s Republic of China

    Qing-guo Liu

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  1. Chao Peng
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Contributions

Manuscript writing: Chao Peng, Yan Zhao and Fan Li; Data collection: Chao Peng, Yan Zhao, Fan Li, Tie-zhu Guo, Xiang-dong Wang, and Bang-yue Wang; Data analysis: Chao Peng, Yan Zhao, Fan Li, Heng-rui Zhang, Yi-fan Yang, Qing-guo Liu and Xin-liang Ren; Study conception and design: Xin-yu Yang; Manuscript editing: Xin-yu Yang, Qing-guo Liu and Xin-liang Ren; Funding acquisition: Xin-yu Yang; Supervision: Xin-yu Yang. All the authors approved the final manuscript.

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Correspondence to Xin-yu Yang.

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This study protocol was examined and approved by the Medical Ethics Committee of Tianjin Medical University General Hospital (No. IRB2022-YX-175-01).

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Peng, C., Zhao, Y., Li, F. et al. Aneurysmal Subarachnoid Hemorrhage and Sex Differences: Analysis of Epidemiology, Outcomes, and Risk Factors. Neurocrit Care (2024). https://doi.org/10.1007/s12028-023-01929-5

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