Skip to main content

Advertisement

SpringerLink
Log in

Sex differences in patients with and without high-risk factors associated with aneurysmal subarachnoid hemorrhage

  • Original Article
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

Controversy remains regarding the appropriate screening for intracranial aneurysms or for the treatment of aneurysmal subarachnoid hemorrhage (aSAH) for patients without known high-risk factors for rupture. This study aimed to assess how sex affects both aSAH presentation and outcomes for aSAH treatment.

Method

A retrospective cohort study was conducted of all patients treated at a single institution for an aSAH during a 12-year period (August 1, 2007–July 31, 2019). An analysis of women with and without high-risk factors was performed, including a propensity adjustment for a poor neurologic outcome (modified Rankin Scale [mRS] score > 2) at follow-up.

Results

Data from 1014 patients were analyzed (69% [n = 703] women). Women were significantly older than men (mean ± SD, 56.6 ± 14.1 years vs 53.4 ± 14.2 years, p < 0.001). A significantly lower percentage of women than men had a history of tobacco use (36.6% [n = 257] vs 46% [n = 143], p = 0.005). A significantly higher percentage of women than men had no high-risk factors for aSAH (10% [n = 70] vs 5% [n = 16], p = 0.01). The percentage of women with an mRS score > 2 at the last follow-up was significantly lower among those without high-risk factors (34%, 24/70) versus those with high-risk factors (53%, 334/633) (p = 0.004). Subsequent propensity-adjusted analysis (adjusted for age, Hunt and Hess grade, and Fisher grade) found no statistically significant difference in the odds of a poor outcome for women with or without high-risk factors for aSAH (OR = 0.7, 95% CI = 0.4–1.2, p = 0.18).

Conclusions

A higher percentage of women versus men with aSAH had no known high-risk factors for rupture, supporting more aggressive screening and management of women with unruptured aneurysms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

aSAH:

Aneurysmal subarachnoid hemorrhage

mRS:

Modified Rankin Scale

References

  1. Algra AM, Klijn CJ, Helmerhorst FM et al (2012) Female risk factors for subarachnoid hemorrhage: a systematic review. Neurology 79(12):1230–1236

    Article  PubMed  Google Scholar 

  2. Alleyne CH Jr (2010) Aneurysmal subarachnoid hemorrhage: have outcomes really improved? Neurology 74(19):1486–1487

    Article  PubMed  Google Scholar 

  3. Backes D, Rinkel GJ, Laban KG et al (2016) Patient- and aneurysm-specific risk factors for intracranial aneurysm growth: a systematic review and meta-analysis. Stroke 47(4):951–957

    Article  PubMed  Google Scholar 

  4. Bijlenga P, Gondar R, Schilling S et al (2017) PHASES score for the management of intracranial aneurysm: a cross-sectional population-based retrospective study. Stroke 48(8):2105–2112

    Article  PubMed  Google Scholar 

  5. Black BK, Hicks SP (1952) The relation of hypertension to arterial aneurysms of the brain. U S Armed Forces Med J 3(12):1813–1818

    CAS  PubMed  Google Scholar 

  6. Blahova Z, Cibulkova J (1969) Personal experience with tooth arrangement according to Hallerin full dentures. Dtsch Stomatol 19(6):467–470

    CAS  PubMed  Google Scholar 

  7. Catapano JS, Zabramski JM, Baranoski JF et al (2019) The prognostic significance of a cast fourth ventricle in ruptured aneurysm patients with intraventricular hemorrhage in the Barrow Ruptured Aneurysm Trial (BRAT). Neurosurgery 85(2):E275–E283

    Article  PubMed  Google Scholar 

  8. Catapano JS, Ducruet AF, Frisoli FA, et al (2020) Predictors of the development of takotsubo cardiomyopathy in aneurysmal subarachnoid hemorrhage and outcomes in patients with intra-aortic balloon pumps. J Neurosurg 1–6

  9. Catapano JS, Rumalla K, Srinivasan VM et al (2021) Treatment of octogenarians and nonagenarians with aneurysmal subarachnoid hemorrhage: a 17-year institutional analysis. Acta Neurochir (Wien) 163(11):2941–2946

    Article  PubMed  Google Scholar 

  10. Centers for Disease C, Prevention (2012) Current cigarette smoking among adults - United States, 2011. MMWR Morb Mortal Wkly Rep. 61(44):889–894

  11. Centers for Disease C, Prevention (2012) Current tobacco use among middle and high school students--United States, 2011. MMWR Morb Mortal Wkly Rep. 61(31):581–585

  12. Chalouhi N, Chitale R, Jabbour P et al (2011) The case for family screening for intracranial aneurysms. Neurosurg Focus 31(6):E8

    Article  PubMed  Google Scholar 

  13. Chalouhi N, Starke RM, Correa T et al (2016) Differential sex response to aspirin in decreasing aneurysm rupture in humans and mice. Hypertension 68(2):411–417

    Article  CAS  PubMed  Google Scholar 

  14. Chason JL, Hindman WM (1958) Berry aneurysms of the circle of Willis; results of a planned autopsy study. Neurology 8(1):41–44

    Article  CAS  PubMed  Google Scholar 

  15. Chien A, Liang F, Sayre J et al (2013) Enlargement of small, asymptomatic, unruptured intracranial aneurysms in patients with no history of subarachnoid hemorrhage: the different factors related to the growth of single and multiple aneurysms. J Neurosurg 119(1):190–197

    Article  PubMed  Google Scholar 

  16. Cutler JA, Sorlie PD, Wolz M et al (2008) Trends in hypertension prevalence, awareness, treatment, and control rates in United States adults between 1988–1994 and 1999–2004. Hypertension 52(5):818–827

    Article  CAS  PubMed  Google Scholar 

  17. Etminan N, Brown RD Jr, Beseoglu K et al (2015) The unruptured intracranial aneurysm treatment score: a multidisciplinary consensus. Neurology 85(10):881–889

    Article  PubMed  PubMed Central  Google Scholar 

  18. Guresir E, Vatter H, Schuss P et al (2013) Natural history of small unruptured anterior circulation aneurysms: a prospective cohort study. Stroke 44(11):3027–3031

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Hasan DM, Mahaney KB, Brown RD Jr et al (2011) Aspirin as a promising agent for decreasing incidence of cerebral aneurysm rupture. Stroke 42(11):3156–3162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hilditch CA, Brinjikji W, Tsang A et al (2021) Application of PHASES and ELAPSS scores to ruptured cerebral aneurysms: how many would have been conservatively managed? J Neurosurg Sci 65(1):33–37

    Article  PubMed  Google Scholar 

  22. Huhtakangas J, Numminen J, Pekkola J et al (2021) Screening of unruptured intracranial aneurysms in 50 to 60-year-old female smokers: a pilot study. Sci Rep 11(1):23729

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  23. Inagawa T, Hirano A (1990) Autopsy study of unruptured incidental intracranial aneurysms. Surg Neurol 34(6):361–365

    Article  CAS  PubMed  Google Scholar 

  24. Inagawa T, Hirano A (1990) Ruptured intracranial aneurysms: an autopsy study of 133 patients. Surg Neurol 33(2):117–123

    Article  CAS  PubMed  Google Scholar 

  25. Inci S, Spetzler RF (2000) Intracranial aneurysms and arterial hypertension: a review and hypothesis. Surg Neurol 53(6):530–540

    Article  CAS  PubMed  Google Scholar 

  26. International Study of Unruptured Intracranial Aneurysms I (1998) Unruptured intracranial aneurysms–risk of rupture and risks of surgical intervention. N Engl J Med. 339(24):1725–1733

    Article  Google Scholar 

  27. Jellinger K (1977) Pathology of intracerebral hemorrhage. Zentralbl Neurochir 38(1):29–42

    CAS  PubMed  Google Scholar 

  28. Kassell NF, Torner JC, Haley EC Jr et al (1990) The international cooperative study on the timing of aneurysm surgery Part 1: Overall management results. J Neurosurg 73(1):18–36

    Article  CAS  PubMed  Google Scholar 

  29. Korja M, Lehto H, Juvela S (2014) Lifelong rupture risk of intracranial aneurysms depends on risk factors: a prospective Finnish cohort study. Stroke 45(7):1958–1963

    Article  PubMed  Google Scholar 

  30. Kwak R, Mizoi K, Katakura R, Suzuki J (1979) The correlation between hypertension in past history and the incidence of cerebral aneurysms. Tohoku J Exp Med 128(3):267–271

    Article  CAS  PubMed  Google Scholar 

  31. le Roux AA, Wallace MC (2010) Outcome and cost of aneurysmal subarachnoid hemorrhage. Neurosurg Clin N Am 21(2):235–246

    Article  PubMed  Google Scholar 

  32. Linn FH, Rinkel GJ, Algra A, van Gijn J (1996) Incidence of subarachnoid hemorrhage: role of region, year, and rate of computed tomography: a meta-analysis. Stroke 27(4):625–629

    Article  CAS  PubMed  Google Scholar 

  33. Maekawa H, Tada Y, Yagi K et al (2017) Bazedoxifene, a selective estrogen receptor modulator, reduces cerebral aneurysm rupture in ovariectomized rats. J Neuroinflammation 14(1):197

    Article  PubMed  PubMed Central  Google Scholar 

  34. McCormick WF, Schmalstieg EJ (1977) The relationship of arterial hypertension to intracranial aneurysms. Arch Neurol 34(5):285–287

    Article  CAS  PubMed  Google Scholar 

  35. Mehan WA Jr, Romero JM, Hirsch JA et al (2014) Unruptured intracranial aneurysms conservatively followed with serial CT angiography: could morphology and growth predict rupture? J Neurointerv Surg 6(10):761–766

    Article  PubMed  Google Scholar 

  36. Mensing LA, van Tuijl RJ, de Kort GA et al (2023) Screening for intracranial aneurysms in persons ⩾35 years with hypertension and atherosclerotic disease who smoke(d). Eur Stroke J 8(4):1071–1078

    Article  PubMed  PubMed Central  Google Scholar 

  37. Neulen A, Pantel T, Konig J et al (2021) comparison of unruptured intracranial aneurysm treatment score and PHASES score in subarachnoid hemorrhage patients with multiple intracranial aneurysms. Front Neurol 12:616497

    Article  PubMed  PubMed Central  Google Scholar 

  38. Pagiola I, Mihalea C, Caroff J et al (2020) The PHASES score: to treat or not to treat? Retrospective evaluation of the risk of rupture of intracranial aneurysms in patients with aneurysmal subarachnoid hemorrhage. J Neuroradiol 47(5):349–352

    Article  PubMed  Google Scholar 

  39. Pakarinen S (1967) Incidence, aetiology, and prognosis of primary subarachnoid haemorrhage. A study based on 589 cases diagnosed in a defined urban population during a defined period. Acta Neurol Scand 43(29):21–28

    Google Scholar 

  40. Rinkel GJ, Djibuti M, Algra A, van Gijn J (1998) Prevalence and risk of rupture of intracranial aneurysms: a systematic review. Stroke 29(1):251–256

    Article  CAS  PubMed  Google Scholar 

  41. Rose MJ (2011) Aneurysmal subarachnoid hemorrhage: an update on the medical complications and treatments strategies seen in these patients. Curr Opin Anaesthesiol 24(5):500–507

    Article  PubMed  Google Scholar 

  42. Stehbens WE (1963) Aneurysms and anatomical variation of cerebral arteries. Arch Pathol 75:45–64

    CAS  PubMed  Google Scholar 

  43. Stumpo V, Latour K, Trevisi G et al (2021) Retrospective application of UIATS recommendations to a multicenter cohort of ruptured intracranial aneurysms: how it would have oriented the treatment choices? World Neurosurg 147:e262–e271

    Article  PubMed  Google Scholar 

  44. Tabuchi S (2015) Relationship between postmenopausal estrogen deficiency and aneurysmal subarachnoid hemorrhage. Behav Neurol 2015:720141

    Article  PubMed  PubMed Central  Google Scholar 

  45. Tada Y, Wada K, Shimada K et al (2014) Estrogen protects against intracranial aneurysm rupture in ovariectomized mice. Hypertension 63(6):1339–1344

    Article  CAS  PubMed  Google Scholar 

  46. Tada Y, Makino H, Furukawa H et al (2014) Roles of estrogen in the formation of intracranial aneurysms in ovariectomized female mice. Neurosurgery 75(6):690–695

    Article  PubMed  Google Scholar 

  47. Thompson BG, Brown RD Jr, Amin-Hanjani S et al (2015) Guidelines for the management of patients with unruptured intracranial aneurysms: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 46(8):2368–2400

    Article  PubMed  Google Scholar 

  48. Woo D, Khoury J, Haverbusch MM et al (2009) Smoking and family history and risk of aneurysmal subarachnoid hemorrhage. Neurology 72(1):69–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Yokosuka K, Rutledge C, Kamio Y et al (2021) Roles of phytoestrogen in the pathophysiology of intracranial aneurysm. Stroke 52(8):2661–2670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the staff of Neuroscience Publications at Barrow Neurological Institute for assistance with manuscript preparation.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, 350 W. Thomas Rd, Phoenix, AZ, 85013, USA

    Joshua S. Catapano, Ethan A. Winkler, Robert F. Rudy, Christopher S. Graffeo, Stefan W. Koester, Visish M. Srinivasan, Tyler S. Cole, Jacob F. Baranoski, Lea Scherschinski, Ruchira M. Jha, Ashutosh P. Jadhav, Andrew F. Ducruet, Felipe C. Albuquerque & Michael T. Lawton

Authors
  1. Joshua S. Catapano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ethan A. Winkler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert F. Rudy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christopher S. Graffeo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stefan W. Koester
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Visish M. Srinivasan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tyler S. Cole
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jacob F. Baranoski
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lea Scherschinski
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ruchira M. Jha
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Ashutosh P. Jadhav
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Andrew F. Ducruet
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Felipe C. Albuquerque
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Michael T. Lawton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael T. Lawton.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Catapano, J.S., Winkler, E.A., Rudy, R.F. et al. Sex differences in patients with and without high-risk factors associated with aneurysmal subarachnoid hemorrhage. Acta Neurochir 166, 125 (2024). https://doi.org/10.1007/s00701-024-06021-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00701-024-06021-1

Keywords

Search

Navigation