BACKGROUND: Understanding the risk factors leading to intracranial aneurysm (IA) rupture have still not been fully clarified. They are vital for proper medical guidance of patients harboring unruptured IAs. Clarifying the hemodynamics associated with the point of rupture could help could provide useful information about some of the risk factors. Thus far, few studies have studied this issue with often diverging conclusions. METHODS: We identified a point of rupture in patients operated for an IAs during surgery, using a combination of preoperative computed tomography (CT) and computed tomography angiography (CTA). Hemodynamic parameters were calculated both for the aneurysm sac as a whole and the point of rupture. In two cases, the results of CFD were compared with those of the experiment using particle image velocimetry (PIV). RESULTS: We were able to identify 6 aneurysms with a well-demarcated point of rupture. In four aneurysms, the rupture point was near the vortex with low wall shear stress (WSS) and high oscillatory shear index (OSI). In one case, the rupture point was in the flow jet with high WSS. In the last case, the rupture point was in the significant bleb and no specific hemodynamic parameters were found. The CFD results were verified in the PIV part of the study. CONCLUSION: Our study shows that different hemodynamic scenarios are associated with the site of IA rupture. The numerical simulations were confirmed by laboratory models. This study further supports the hypothesis that various pathological pathways may lead to aneurysm wall damage resulting in its rupture.

Department of Anatomy Faculty of Medicine Masaryk University Brno Brno Czechia

Department of Biochemistry Faculty of Medicine Masaryk University Brno Brno Czechia

Department of Neurosurgery Masaryk Hospital J E Purkyne University Ústí nad Labem Czechia

Faculty of Mathematics and Physics Mathematical Institute Charles University Prague Czechia

Faculty of Science and Engineering Bernoulli Institute University of Groningen Groningen Netherlands

Institute of Biophysics of the Czech Academy of Sciences Brno Czechia

Institute of Experimental Medicine of the Czech Academy of Sciences Prague Czechia

International Clinical Research Center St Anne's University Hospital Brno Brno Czechia

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Gabriel RA, Kim H, Sidney S, McCulloch CE, Singh V, Johnston SC, et al. . Ten-year detection rate of brain arteriovenous malformations in a large, multiethnic, defined population. Stroke. (2010) 41:21–6. doi: 10.1161/STROKEAHA.109.566018, PMID: PubMed DOI PMC

Dhar S, Tremmel M, Mocco J, Kim M, Yamamoto J, Siddiqui AH, et al. . Morphology parameters for intracranial aneurysm rupture risk assessment. Neurosurgery. (2008) 63:185–96. doi: 10.1227/01.NEU.0000316847.64140.81, PMID: PubMed DOI PMC

Xiang J, Natarajan SK, Tremmel M, Ma D, Mocco J, Hopkins LN, et al. . Hemodynamic-morphologic discriminants for intracranial aneurysm rupture. Stroke. (2011) 42:144–52. doi: 10.1161/STROKEAHA.110.592923, PMID: PubMed DOI PMC

Xiang J, Yu J, Choi H, Dolan Fox JM, Snyder KV, Levy EI, et al. . Rupture resemblance score (RRS): toward risk stratification of unruptured intracranial aneurysms using hemodynamic-morphological discriminants. J Neurointerv Surg. (2015) 7:490–5. doi: 10.1136/neurintsurg-2014-011218, PMID: PubMed DOI PMC

Jiang Y, Lu G, Ge L, Huang L, Wan H, Wan J, et al. . Rupture point hemodynamics of intracranial aneurysms: case report and literature review. Ann Vasc Surg. (2021) 1:100022. doi: 10.1016/j.avsurg.2021.100022 DOI

Zhang Y, Jing L, Zhang Y, Liu J, Yang X. Low wall shear stress is associated with the rupture of intracranial aneurysm with known rupture point: case report and literature review. BMC Neurol. (2016) 16:231. doi: 10.1186/s12883-016-0759-0, PMID: PubMed DOI PMC

Meng H, Tutino VM, Xiang J, Siddiqui A. High WSS or low WSS? Complex interactions of hemodynamics with intracranial aneurysm initiation, growth, and rupture: toward a unifying hypothesis. AJNR Am J Neuroradiol. (2014) 35:1254–62. doi: 10.3174/ajnr.A3558, PMID: PubMed DOI PMC

Staarmann B, Smith M, Prestigiacomo CJ. Shear stress and aneurysms: a review. Neurosurg Focus. (2019) 47:E2. doi: 10.3171/2019.4.FOCUS19225 PubMed DOI

Ujiie H, Tamano Y, Sasaki K, Hori T. Is the aspect ratio a reliable index for predicting the rupture of a saccular aneurysm? Neurosurgery. (2001) 48:495–502. doi: 10.1097/00006123-200103000-00007, PMID: PubMed DOI

Berg P, Roloff C, Beuing O, Voss S, Sugiyama S-I, Aristokleous N, et al. . The computational fluid dynamics rupture challenge 2013—phase II: variability of hemodynamic simulations in two intracranial aneurysms. J Biomech Eng. (2015) 137:121008. doi: 10.1115/1.4031794, PMID: PubMed DOI

Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, et al. . User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. NeuroImage. (2006) 31:1116–28. doi: 10.1016/j.neuroimage.2006.01.015, PMID: PubMed DOI

Fang Q, Boas DA. (2009). Tetrahedral mesh generation from volumetric binary and grayscale images. 2009 IEEE International Symposium on Biomedical Imaging: From Nano to Macro. Boston, MA: IEEE, 1142–1145

Magjarevic R, Poethke J, Spuler A, Petz C, Hege H-C, Goubergrits L, et al. . (2009). Cerebral aneurysm hemodynamics and a length of parent vessel. Dössel O., Schlegel W. C. World Congress on Medical Physics and Biomedical Engineering. September 7–12, 2009. Munich, Germany. (Berlin: Springer; ), 1608–1611

Chabiniok R, Hron J, Jarolímová A, Málek J, Rajagopal KR, Rajagopal K, et al. . Three-dimensional flows of incompressible Navier–Stokes fluids in tubes containing a sinus, with varying slip conditions at the wall. Int J Eng Sci. (2022) 180:103749. doi: 10.1016/j.ijengsci.2022.103749 DOI

Alnæs M, Blechta J, Hake J, Johansson A, Kehlet B, Logg A, et al. . The FEniCS project version 1.5. Arch Numer Softw. (2015) 3:9–23. doi: 10.11588/ANS.2015.100.20553 DOI

Abhyankar S, Brown J, Constantinescu EM, Ghosh D, Smith BF, Zhang H. (2018). PETSc/TS: a modern scalable ODE/DAE solver library. arXiv. Available at: http://arxiv.org/abs/1806.01437 (Accessed July 19, 2022) [Epub ahead of preprint].

Arnold DN, Brezzi F, Fortin M. A stable finite element for the stokes equations. Calcolo. (1984) 21:337–44. doi: 10.1007/BF02576171 DOI

Axier A, Rexiati N, Wang Z, Cheng X, Su R, Aikeremu R, et al. . Effect of hemodynamic changes on the risk of intracranial aneurysm rupture: a systematic review and meta-analysis. Am J Transl Res. (2022) 14:4638–47. PMID: PubMed PMC

Ayachit U. The ParaView Guide: A Parallel Visualization Application. Clifton Park, NY, USA: Kitware, Inc. (2015).

Schneider CA, Rasband WS, Eliceiri KW, Schindelin J, Arganda-Carreras I, Frise E, et al. . NIH image to ImageJ: 25 years of image analysis. Nat Methods. (2012) 9:671–5. doi: 10.1038/nmeth.2089, PMID: PubMed DOI PMC

Sullivan C, Kaszynski A. PyVista: 3D plotting and mesh analysis through a streamlined interface for the visualization toolkit (VTK). J Open Source Softw. (2019) 4:1450. doi: 10.21105/joss.01450 DOI

Hejčl A, Švihlová H, Sejkorová A, Radovnický T, Adámek D, Hron J, et al. . Computational fluid dynamics of a fatal ruptured anterior communicating artery aneurysm. J Neurol Surg A. (2017) 78:610–6. doi: 10.1055/s-0037-1604286, PMID: PubMed DOI

Cebral JR, Detmer F, Chung BJ, Choque-Velasquez J, Rezai B, Lehto H, et al. . Local hemodynamic conditions associated with focal changes in the intracranial aneurysm wall. AJNR Am J Neuroradiol. (2019) 40:510–6. doi: 10.3174/ajnr.A5970, PMID: PubMed DOI PMC

Kosierkiewicz TA, Factor SM, Dickson DW. Immunocytochemical studies of atherosclerotic lesions of cerebral berry aneurysms. J Neuropathol Exp Neurol. (1994) 53:399–406. doi: 10.1097/00005072-199407000-00012, PMID: PubMed DOI

Levesque MJ, Liepsch D, Moravec S, Nerem RM. Correlation of endothelial cell shape and wall shear stress in a stenosed dog aorta. Arteriosclerosis. (1986) 6:220–9. doi: 10.1161/01.ATV.6.2.220, PMID: PubMed DOI

Levesque MJ, Nerem RM. The elongation and orientation of cultured endothelial cells in response to shear stress. J Biomech Eng. (1985) 107:341–7. doi: 10.1115/1.3138567 PubMed DOI

Sejkorová A, Švihlová H, Ondra P, Kendall DD, Uthamaraj S, Lanzino G, et al. . Hemodynamic changes in four aneurysms leading to their rupture at follow-up periods. Ces Slov Neurol Neurochir. (2020) 83:621–6. doi: 10.48095/cccsnn2020621 DOI

Cebral JR, Sheridan M, Putman CM. Hemodynamics and bleb formation in intracranial aneurysms. AJNR Am J Neuroradiol. (2010) 31:304–10. doi: 10.3174/ajnr.A1819, PMID: PubMed DOI PMC

Beck J, Rohde S, El Beltagy M, Zimmermann M, Berkefeld J, Seifert V, et al. . Difference in configuration of ruptured and unruptured intracranial aneurysms determined by biplanar digital subtraction angiography. Acta Neurochir. (2003) 145:861–5. doi: 10.1007/s00701-003-0124-0, PMID: PubMed DOI

Suga M, Yamamoto Y, Sunami N, Abe T, Kondo A. Growth of asymptomatic unruptured aneurysms in follow-up study: report of three cases. No Shinkei Geka. (2003) 31:303–8. PMID: PubMed

Tsukahara T, Murakami N, Sakurai Y, Yonekura M, Takahashi T, Inoue T, et al. . Treatment of unruptured cerebral aneurysms; a multi-center study at Japanese national hospitals. Acta Neurochir Suppl. (2005) 94:77–85. doi: 10.1007/3-211-27911-3_12 PubMed DOI

Li B, Liu T, Liu J, Liu Y, Cao B, Zhao X, et al. . Reliability of using generic flow conditions to quantify aneurysmal haemodynamics: a comparison against simulations incorporating boundary conditions measured in vivo. Comput Methods Prog Biomed. (2022) 225:107034. doi: 10.1016/j.cmpb.2022.107034, PMID: PubMed DOI

Bordás R, Seshadhri S, Janiga G, Skalej M, Thévenin D. Experimental validation of numerical simulations on a cerebral aneurysm phantom model. Interv Med Appl Sci. (2012) 4:193–205. doi: 10.1556/imas.4.2012.4.4, PMID: PubMed DOI PMC

Brindise MC, Rothenberger S, Dickerhoff B, Schnell S, Markl M, Saloner D, et al. . Multi-modality cerebral aneurysm haemodynamic analysis: in vivo 4D flow MRI, in vitro volumetric particle velocimetry and in silico computational fluid dynamics. J R Soc Interface. (2019) 16:20190465. doi: 10.1098/rsif.2019.0465, PMID: PubMed DOI PMC

Buchmann NA, Yamamoto M, Jermy M, David T. Particle image velocimetry (PIV) and computational fluid dynamics (CFD) modelling of carotid artery haemodynamics under steady flow: a validation study. J Biomech Sci Eng. (2010) 5:421–36. doi: 10.1299/jbse.5.421 DOI

Li Y, Verrelli DI, Yang W, Qian Y, Chong W. A pilot validation of CFD model results against PIV observations of haemodynamics in intracranial aneurysms treated with flow-diverting stents. J Biomech. (2020) 100:109590. doi: 10.1016/j.jbiomech.2019.109590, PMID: PubMed DOI

Roloff C, Stucht D, Beuing O, Berg P. Comparison of intracranial aneurysm flow quantification techniques: standard PIV vs stereoscopic PIV vs tomographic PIV vs phase-contrast MRI vs CFD. J Neurointerv Surg. (2019) 11:275–82. doi: 10.1136/neurintsurg-2018-013921, PMID: PubMed DOI

Schneiders JJ, Marquering HA, van den Berg R, VanBavel E, Velthuis B, Rinkel GJE, et al. . Rupture-associated changes of cerebral aneurysm geometry: high-resolution 3D imaging before and after rupture. AJNR Am J Neuroradiol. (2014) 35:1358–62. doi: 10.3174/ajnr.A3866, PMID: PubMed DOI PMC