Skip to main content
Log in

Associations of hemodynamics, morphology, and patient characteristics with aneurysm rupture stratified by aneurysm location

  • Diagnostic Neuroradiology
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

The mechanisms of cerebral aneurysm rupture are not fully understood. We analyzed the associations of hemodynamics, morphology, and patient age and gender with aneurysm rupture stratifying by location.

Methods

Using image-based models, 20 hemodynamic and 17 morphological parameters were compared in 1931 ruptured and unruptured aneurysms with univariate logistic regression. Rupture rates were compared between males and females as well as younger and older patients and bifurcation versus sidewall aneurysms for different aneurysm locations. Subsequently, associations between hemodynamics and morphology and patient as well as aneurysm characteristics were analyzed for aneurysms at five locations.

Results

Compared to unruptured aneurysms, ruptured aneurysms were characterized by a more irregular shape and were exposed to a more adverse hemodynamic environment described by faster flow, higher wall shear stress, more oscillatory shear, and more unstable and complex flows. These associations with rupture status were consistent for different aneurysm locations. Rupture rates were significantly higher in males at the internal carotid artery (ICA) bifurcation, ophthalmic ICA, and the middle cerebral artery (MCA) bifurcation. At the anterior communicating artery (ACOM) and MCA bifurcation, they were significantly higher for younger patients. Bifurcation aneurysms had significantly larger rupture rates at the MCA and posterior communicating artery (PCOM). In these groups with higher rupture rates, aneurysms were characterized by adverse hemodynamics and more complex shapes.

Conclusion

Hemodynamic and morphological differences between ruptured and unruptured aneurysms are consistent across locations. Adverse morphology and hemodynamics are related to rupture as well as younger age, male gender, and bifurcation aneurysms.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Abbreviations

CFD:

Computational fluid dynamics

ICA:

Internal carotid artery

VA:

Vertebral artery

ROC:

Receiver operating characteristic

ACOM:

Anterior communicating artery

ICA-OPH:

Ophthalmic segment of the ICA

ICA-BIF:

Internal carotid artery bifurcation

PCOM:

‘Posterior communicating artery

MCA:

Middle cerebral artery

MCA-DIST-PROX:

Without the MCA-bifurcation

WSS:

Wall shear stress

OSI:

Oscillatory shear index

References

  1. Vlak MH, Algra A, Brandenburg R, Rinkel GJ (2011) Prevalence of unruptured intracranial aneurysms, with emphasis on sex, age, comorbidity, country, and time period: a systematic review and meta-analysis. Lancet Neurol 10:626–636. https://doi.org/10.1016/s1474-4422(11)70109-0

    Article  PubMed  Google Scholar 

  2. Juvela S, Poussa K, Lehto H, Porras M (2013) Natural history of unruptured intracranial aneurysms: a long-term follow-up study. Stroke 44:2414–2421. https://doi.org/10.1161/strokeaha.113.001838

    Article  PubMed  Google Scholar 

  3. Rivero-Arias O, Gray A, Wolstenholme J (2010) Burden of disease and costs of aneurysmal subarachnoid haemorrhage (aSAH) in the United Kingdom. Cost Eff Resour Alloc 8:6. https://doi.org/10.1186/1478-7547-8-6

    Article  PubMed  PubMed Central  Google Scholar 

  4. Gabriel RA, Kim H, Sidney S, McCulloch CE, Singh V, Johnston SC, Ko NU, Achrol AS, Zaroff JG, Young WL (2010) Ten-year detection rate of brain arteriovenous malformations in a large, multiethnic, defined population. Stroke 41:21–26. https://doi.org/10.1161/STROKEAHA.109.566018

    Article  PubMed  Google Scholar 

  5. Longo M, Granata F, Racchiusa S, Mormina E, Grasso G, Longo GM, Garufi G, Salpietro FM, Alafaci C (2017) Role of hemodynamic forces in unruptured intracranial aneurysms: an overview of a complex scenario. World Neurosurg 105:632–642. https://doi.org/10.1016/j.wneu.2017.06.035

    Article  PubMed  Google Scholar 

  6. Xiang J, Natarajan SK, Tremmel M, Ma D, Mocco J, Hopkins LN, Siddiqui AH, Levy EI, Meng H (2011) Hemodynamic-morphologic discriminants for intracranial aneurysm rupture. Stroke 42:144–152

    Article  PubMed  Google Scholar 

  7. Miura Y, Ishida F, Umeda Y, Tanemura H, Suzuki H, Matsushima S, Shimosaka S, Taki W (2013) Low wall shear stress is independently associated with the rupture status of middle cerebral artery aneurysms. Stroke 44:519–521. https://doi.org/10.1161/STROKEAHA.112.675306

    Article  PubMed  Google Scholar 

  8. Jing L, Fan J, Wang Y, Li H, Wang S, Yang X, Zhang Y (2015) Morphologic and hemodynamic analysis in the patients with multiple intracranial aneurysms: ruptured versus unruptured. PLoS One 10:e0132494. https://doi.org/10.1371/journal.pone.0132494

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Lv N, Wang C, Karmonik C, Fang Y, Xu J, Yu Y, Cao W, Liu J, Huang Q (2016) Morphological and hemodynamic discriminators for rupture status in posterior communicating artery aneurysms. PLoS One 11:e0149906. https://doi.org/10.1371/journal.pone.0149906

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Ishibashi T, Murayama Y, Urashima M, Saguchi T, Ebara M, Arakawa H, Irie K, Takao H, Abe T (2009) Unruptured intracranial aneurysms: incidence of rupture and risk factors. Stroke 40:313–316. https://doi.org/10.1161/STROKEAHA.108.521674

    Article  PubMed  Google Scholar 

  11. Chung BJ, Mut F, Putman C, Hamzei-Sichani F, Brinjikji W, Kallmes D, Jimenez CM, Cebral JR (2018) Identification of hostile hemodynamics and geometries of cerebral aneurysms: a case-control study. AJNR Am J Neuroradiol. https://doi.org/10.3174/ajnr.A5764

  12. Mut F, Löhner R, Chien A, Tateshima S, Viñuela F, Putman C, Cebral JR (2011) Computational hemodynamics framework for the analysis of cerebral aneurysms. Int J Numer Method Biomed Eng 27:822–839

    Article  PubMed  PubMed Central  Google Scholar 

  13. Byrne G, Mut F, Cebral JR (2014) Quantifying the large-scale hemodynamics of intracanial aneurysms. AJNR Am J Neuroradiol 35:333–338 https://doi.org/10.3174/ajnr.A3678

    Article  PubMed  CAS  Google Scholar 

  14. Ma B, Harbaugh RE, Raghavan ML (2004) Three-dimensional geometrical characterization of cerebral aneurysms. Ann Biomed Eng 32:264–273

    Article  PubMed  Google Scholar 

  15. Raghavan ML, Ma B, Harbaugh RE (2005) Quantified aneurysm shape and rupture risk. J Neurosurg 102:355–362

    Article  PubMed  Google Scholar 

  16. Chung BJ, Doddasomayajula R, Mut F, Detmer F, Pritz MB, Hamzei-Sichani F, Brinjikji W, Kallmes DF, Jimenez CM, Putman CM, Cebral JR (2017) Angioarchitectures and hemodynamic characteristics of posterior communicating artery aneurysms and their association with rupture status. Am J Neuroradiol 38:2111–2118. https://doi.org/10.3174/ajnr.A5358

    Article  PubMed  CAS  Google Scholar 

  17. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300

    Google Scholar 

  18. R Core Team (2016) R: a language and environment for statistical computing. Version 3.3.3, R Foundation for Statistical Computing, Vienna, Austria

  19. Greving JP, Wermer MJ, Brown RD et al (2014) Development of the PHASES score for prediction of risk of rupture of intracranial aneurysms: a pooled analysis of six prospective cohort studies. Lancet Neurol 13:59–66. https://doi.org/10.1016/s1474-4422(13)70263-1

    Article  PubMed  Google Scholar 

  20. Backes D, Rinkel GJE, Greving JP, Velthuis BK, Murayama Y, Takao H, Ishibashi T, Igase M, terBrugge KG, Agid R, Jääskeläinen JE, Lindgren AE, Koivisto T, von und zu Fraunberg M, Matsubara S, Moroi J, Wong GKC, Abrigo JM, Igase K, Matsumoto K, Wermer MJH, van Walderveen MAA, Algra A, Vergouwen MDI (2017) ELAPSS score for prediction of risk of growth of unruptured intracranial aneurysms. Neurology 88:1600–1606. https://doi.org/10.1212/WNL.0000000000003865

    Article  PubMed  Google Scholar 

  21. Matsukawa H, Uemura A, Fujii M, Kamo M, Takahashi O, Sumiyoshi S (2013) Morphological and clinical risk factors for the rupture of anterior communicating artery aneurysms. J Neurosurg 118:978–983. https://doi.org/10.3171/2012.11.JNS121210

    Article  PubMed  Google Scholar 

  22. Wang G-X, Yu J-Y, Wen L, Zhang L, Mou KJ, Zhang D (2016) Risk factors for the rupture of middle cerebral artery bifurcation aneurysms using CT angiography. PLoS One 11:e0166654. https://doi.org/10.1371/journal.pone.0166654

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Juvela S, Porras M, Poussa K (2000) Natural history of unruptured intracranial aneurysms: probability of and risk factors for aneurysm rupture. J Neurosurg 93:379–387. https://doi.org/10.3171/jns.2000.93.3.0379

    Article  PubMed  CAS  Google Scholar 

  24. Wermer MJH, van der Schaaf IC, Algra A, Rinkel GJE (2007) Risk of rupture of unruptured intracranial aneurysms in relation to patient and aneurysm characteristics: an updated meta-analysis. Stroke 38:1404–1410. https://doi.org/10.1161/01.STR.0000260955.51401.cd

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  26. Kongable GL, Lanzino G, Germanson TP, Truskowski LL, Alves WM, Torner JC, Kassell NF, the Participants (1996) Gender-related differences in aneurysmal subarachnoid hemorrhage. J Neurosurg 84:43–48. https://doi.org/10.3171/jns.1996.84.1.0043

    Article  PubMed  CAS  Google Scholar 

  27. Mhurchu CN, Anderson C, Jamrozik K, Hankey G, Dunbabin D, Australasian Cooperative Research on Subarachnoid Hemorrhage Study (ACROSS) Group (2001) Hormonal factors and risk of aneurysmal subarachnoid hemorrhage: an international population-based, case-control study. Stroke 32:606–612

    Article  PubMed  CAS  Google Scholar 

  28. Jamous MA, Nagahiro S, Kitazato KT, Satomi J, Satoh K (2005) 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 103:1046–1051. https://doi.org/10.3171/jns.2005.103.6.1046

    Article  PubMed  CAS  Google Scholar 

  29. Jamous MA, Nagahiro S, Kitazato KT, Tamura T, Kuwayama K, Satoh K (2005) 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 103:1052–1057. https://doi.org/10.3171/jns.2005.103.6.1052

    Article  PubMed  CAS  Google Scholar 

  30. Qureshi AI, Malik AA, Saeed O, Defillo A, Sherr GT, Suri MFK (2016) Hormone replacement therapy and the risk of subarachnoid hemorrhage in postmenopausal women. J Neurosurg 124:45–50. https://doi.org/10.3171/2014.12.JNS142329

    Article  PubMed  CAS  Google Scholar 

  31. Lipton RB, Stewart WF, Diamond S, Diamond ML, Reed M (2001) Prevalence and burden of migraine in the United States: data from the American Migraine Study II. Headache 41:646–657

    Article  PubMed  CAS  Google Scholar 

  32. Juvela S, Lehto H (2015) Risk factors for all-cause death after diagnosis of unruptured intracranial aneurysms. Neurology 84:456–463. https://doi.org/10.1212/WNL.0000000000001207

    Article  PubMed  Google Scholar 

  33. Lindekleiv H, Sandvei MS, Njølstad I et al (2011) Sex differences in risk factors for aneurysmal subarachnoid hemorrhage: a cohort study. Neurology 76:637–643. https://doi.org/10.1212/WNL.0b013e31820c30d3

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Felicitas J. Detmer.

Ethics declarations

Funding

This study was funded by the National Institutes of Health/National Institute of Neurological Disorders and Stroke (NIH-NINDS) [R21NS094780].

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

For this type of study formal consent is not required.

Electronic supplementary material

ESM 1

(PDF 674 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Detmer, F.J., Chung, B.J., Jimenez, C. et al. Associations of hemodynamics, morphology, and patient characteristics with aneurysm rupture stratified by aneurysm location. Neuroradiology 61, 275–284 (2019). https://doi.org/10.1007/s00234-018-2135-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-018-2135-9

Keywords

Navigation