Peri-Aneurysmal Contact as a Risk Factor for Aneurysmal Rupture in Unruptured Intracranial Aneurysms: An Overview

Main Article Content

Toru Satoh, MD., PhD Yu Satoh, MD Yoichi Sawada, PhD

Abstract

The occurrence and growth of unruptured intracranial aneurysms are believed to be influenced by intraluminal factors of blood flow dynamics and pathological factors of the aneurysm wall. In addition to these, the deformation and rupture of aneurysms require consideration of physical extra-luminal factors due to contact between the aneurysm and surrounding structures including brain parenchyma, cranial nerves, arteries, veins, cranial base bone and dura mater. The extra-luminal factors of aneurysms were evaluated based on the presence of peri-aneurysmal contact. Peri-aneurysmal contact, depending on the type, location, and size of aneurysms, influenced the growth pattern of the aneurysm. Recently, with the imaging of magnetic resonance cisternography, it had become possible to non-invasively assess the anatomical relationship between the outer wall of aneurysms and the surrounding structures. Fusion images overlaying 3D magnetic resonance cisternography with 3D computed tomography angiography or 3D magnetic resonance angiography detailed the anatomical relationship of peri-aneurysmal contact, position of contact sites, and depth. We depicted the anatomical construction of peri-aneurysmal contact and bleb in unruptured intracranial aneurysms using fusion images and studied the intraluminal blood flow dynamics using computational fluid dynamics. As a result, peri-aneurysmal contact was observed to be involved as an independent variable in the process of bleb formation. It was suggested that factors extra-luminal to the aneurysm, such as peri-aneurysmal contact, might have a greater impact on bleb formation than intraluminal factors like blood flow dynamics. Peri-aneurysmal contact emerged as a noteworthy extra-luminal factor, particularly associated with bleb formation, presenting a substantial risk of rupture in unruptured intracranial aneurysms. These findings underscore the importance of considering the presence and extent of peri-aneurysmal contact alongside intraluminal and wall-related factors in future evaluations. The implications of this overview extend to the development of risk assessment protocols, providing valuable insights for guiding early intervention strategies and ultimately contributing to improved patient outcomes.

Keywords: Bleb formation, Computational fluid dynamics, Hemodynamics, Peri-aneurysmal contact, Unruptured intracranial aneurysm.

Article Details

How to Cite
SATOH, Toru; SATOH, Yu; SAWADA, Yoichi. Peri-Aneurysmal Contact as a Risk Factor for Aneurysmal Rupture in Unruptured Intracranial Aneurysms: An Overview. Medical Research Archives, [S.l.], v. 12, n. 2, feb. 2024. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/5021>. Date accessed: 23 nov. 2024. doi: https://doi.org/10.18103/mra.v12i2.5021.
Section
Research Articles

References

1. Rhoton AL Jr. Aneurysms. Neurosurgery. 2002;51[suppl 1]:121-158.

2. Vernooij MW, Ikram MA, Tanghe HL, Vincent AJPE, Hofman A, Krestin GP, Niessen WJ, Breteler MMB, van der Lugtet A. Incidental findings on brain MRI in the general population. N. Engl. J. Med. 2007;357(18):1821–1828. doi: 10.1056/NEJMoa070972.

3. Vlak MH, Algra A, Brandenburg R, Je Rinkelet G. 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): 626–636. doi: 10.1016/S1474-4422(11)70109-0.

4. UCAS Japan Investigators; Morita A, Kirino T, Hashi K, Aoki N, Fukuhara S, Hashimoto N, Nakayama T, Sakai M, Teramoto A, Tominari S, Yoshimoto T, CAS Japan Investigators. The natural course of unruptured cerebral aneurysms in a Japanese cohort. N. Engl. J. Med. 2012; 28;366(26):2474-82.
doi: 10.1056/NEJMoa1113260.

5. Murayama Y, Takao H, Toshihiro Ishibashi T, Saguchi T, Ebara M, Yuki I, Arakawa H, Irie K, Urashima M, Molyneux AJ. Risk analysis of unruptured intracranial aneurysms: prospective 10-year cohort study. Stroke. 2016;47(2):365–371. doi: 10.1161/STROKEAHA.115.010698. Epub 2016 Jan 7.

6. Ujiie H, Tachibana H, Hiramatsu O, Hazel AL, Matsumoto T, Ogasawara Y, Nakajima H, Hori T, Takakura K, Kajiya F. Effects of size and shape (aspect ratio) on the hemodynamics of saccular aneurysms; A possible index for surgical treatment of intracranial aneurysms. Neurosurgery. 1999;45(1):119-29; discussion 129-30. doi: 10.1097/00006123-199907000-00028.

7. Brisman JL, Song JK, Newell DW. Cerebral aneurysms. N. Engl. J. Med. 2006;31;355(9):928-39. doi: 10.1056/NEJMra052760.

8. Mocco J, Brown Jr RD, Torner JC, Capuano AW, Fargen KM, Raghavan ML, Piepgras DG, Meissner I, Huston III J. Aneurysm morphology and prediction of rupture: An international study of unruptured intracranial aneurysms analysis. Neurosurgery. 2018;82(4):491-496. doi: 10.1093/neuros/nyx226.

9. Estiman N, de Sousa DA, Tiseo C, Bourcier R, Desal H, Anttii Lindgren A, Timo KoivistoT, Netuka D, Peschillo S, Lémeret S, Avtar Lal A, Vergouwen MDI, Rinkel GJE. European Stroke Organisation (ESO) guidelines on management of unruptured intracranial aneurysms. European. Stroke. Journal. 2022, 7(3): LXXXI–CVI.

10. Lindgren AE, Koivisto T, Björkman J, von Und Zu Fraunberg M, Helin K, Jääskeläinen JE, Juhana Frösen J. Irregular shape of intracranial aneurysm indicates rupture risk irrespective of size in a population-based cohort. Stroke. 2016;47(5):1219-26. doi: 10.1161/STROKEAHA.115.012404. Epub 2016 Apr 12.

11. Kleinloog R, de Mul N, Verweij BH, Kleinloog R, Post JA Gabriel J E Rinkel GJ, Ruigrok YM. Risk factors for intracranial aneurysm rupture: A systematic review. Neurosurgery. 2018;;82(4):431-440.
doi: 10.1093/neuros/nyx238.

12. Seshaiyer P, Humphrey JD. On the potentially protective role of contact constraints on saccular aneurysms. J. Biomech. 2001;;34 (5):607-12. doi: 10.1016/s0021-9290(01)00002-1.

13. Sugiu K, Ugiu B, Jean B, Ruiz DSM, Martin J-B, Delavelle J, Rüfenachtet DA. Influence of the perianeurysmal environment on rupture of cerebral aneurysms. Preliminary observation. Interv. Neuroradiol. (Suppl 1) 2000;6:65–70.

14. Rúiz DSM, Tokunaga K, Dehdashti AR, Sugiu K, Delavelle J, Rüfenachtet DA. Is the rupture of cerebral berry aneurysms influenced by the perianeurysmal environment? Acta. Neurochir. Suppl. 2000;82: 31-34. https://doi. org/10.1159/000313441 (2002).

15. Satoh T, Omi M, Ohsako C, Katsumata A, Yoshimoto Y, Tsuchimoto S, Onoda K, Tokunaga T, Sugiu K, Date I. Influence of perianeurysmal environment on the deformation and bleb formation of the unruptured cerebral aneurysm: Assessment with fusion imaging of 3D MR cisternography and 3D MR angiography. AJNR Am. J. Neuroradiol. 2005;26(8):2010-2018.

16. Ruíz DSM, Yilmaz H, Dehdashti AR, Alimenti A, de Tribolet N, Rüfenacht DA. The perianeurysmal environment: Influence on saccular aneurysm shape and rupture. AJNR Am. J. Neuroradiol. 2006; 27(3):504-512.

17. Sfoza DM, Putman CM, Cebral JR. Hemodynamics of Cerebral Aneurysms. Annu. Re. Fluid. Mech. 1:41:91-107, Annu. Rev. Fluid. Mech. 2009; 41(1): 91107. doi:10.1146/annurev.fluid.40.111406.102126.

18. Sforza DM, Putman CM, Tateshima S, Viñuela F, Cebral JR. Effects of perianeurysmal environment during the growth of cerebral aneurysms: A case study. AJNR Am. J. Neuroradiol. 2012;33(6):1115-1120.
doi: 10.3174/ajnr.A2908. Epub 2012 Feb 2.

19. Wang F, Xue Z, Sun Z, Jiang J, Wu C, Xu B. Simulated effects of perianeurysmal bone on a cerebral aneurysm: A case study. Turk Neurosurg. 2018:28(5):805-810.
doi: 10.5137/1019-5149.JTN.20587-17.2.

20. Satoh T, Onoda K, Tsuchimoto S. Visualization of intaaneurysmal flow patterns with transluminal flow imaging of three-dimensional MR angiograms in conjunction with aneurysmal configurations. AJNR Am. J. Neuroradiol. 2003;24:1436‐1445.

21. Frösen L, Tulamo R, Paetau A, Laaksamo E, Korja M, Laakso A, Niemelä M, Hernesniemi J. Saccular intracranial aneurysm: pathology and mechanisms. Acta. Neuropathol. 2012 Jun;123(6):773-86. doi: 10.1007/s00401-011-0939-3.

22. Laaksamo E, Tulamo R, Liiman A, Baumann M, Friedlander RM, Hernesniemi J, Kangasniemi M, Niemelä M, Laakso A, Frösen J. 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.

23. Frösen J, Cebral J, Robertson AM, Aoki T. Flow-induced, inflammation-mediated arterial wall remodeling in the formation and progression of intracranial aneurysms. Neurosurg. Focus 2019;47, E21.
https://doi.org/10.3171/2019.5.FOCUS19234.

24. Kataoka H, Yagi T, Ikedo T, Imai H, Kawamura K,Yoshida K, Nakamura M, Aoki T, Miyamoto S. Hemodynamic and histopathological changes in the early phase of the development of an intracranial aneurysm. Neurol. Med. Chir. (Tokyo). 2020;60(7):319-328. doi: 10.2176/nmc.st.2020-0072.

25. Kakinuma K, Ezuka I, Yamada H, Harada A, Takahashi M. Late follow0up review of clipped cerebral aneurysms. Surg, Cereb. Stroke. (Jpn). 2002;30:88-92.

26. Kataoka K, Taneda M, Asai T, Yamada Y. Difference in nature of ruptured and unruptured cerebral aneurysm. Lancet. 2000;355(9199): 203. doi: 10.1016/S0140-6736(99)03881-7.

27. Satoh T, Omi M, Ohsako C, Katsumata A, Yoshimoto Y, Tsuchimoto S, Onoda, Tokunaga K, Sugiu K, Date I. Visualization of aneurysmal contours and perianeurysmal environment with conventional and transparent 3D MR cisternography. AJNR. Am. J. Neuroradiol. 2005;26(2):313–318.

28. Tateshima S, Murayama Y, Villablanca JP, Morino T, Takahashi T, Yamauchi T, Tanishita K, Vinuela F. Intraaneurysmal flow dynamics study featuring an acrylic aneurysm model manufactured using a computerized tomography angiogram as a mold. J. Neurosurg. 2001; 95(6):1020-7. doi: 10.3171/jns.2001.95.6.1020.

29. Tanaka R, Liew BS, Yamada Y, Sasaki K, Miyatani K, Komatsu F, Kawase T, Kato Y, Yuichi Hirose Y. Depiction of cerebral aneurysm wall by computational fluid dynamics (CFD) and preoperative illustration. Asian. J. Neuroosurg. 2022;17(1):43–49. doi: 10.1055/s-0042-1749148. eCollection 2022 Mar.

30. Cebral JR, Sheridan M, Putman CM. Hemodynamics and bleb formation in intracranial aneurysms. AJNR. Am. J. Neuroradiol. 2010;31(2):304-310. doi: 10.3174/ajnr.A1819. Epub 2009 Oct 1.

31. Satoh T, Yagi T, Sawada Y, Sugiu K, Yu Sato Y, Isao Date I. Association of bleb formation with peri-aneurysmal contact in unruptured intracranial aneurysms. Scientific Reports. 2022; 12(1):6075. doi: 10.1038/s41598-022-10064-8.

32. Sugiyama SI, Endo H, Omodaka S, Endo T, Kuniyasu Niizuma K, Rashad S, Nakayama T, Funamoto K, Ohta M, Tominaga T. Daughter sac formation related to blood inflow jet in an intracranial aneurysm. World. Neurosurg. 2016:96:396-402. doi: 10.1016/j.wneu.2016.09.040.

33. Russell JH, Kelson N, Barry M, et al. Computational fluid dynamic analysis of intracranial aneurysmal bleb formation. Neurosurgery. 2013;73(6):1061-8; discussion 1068-9. doi:10.1227/NEU.0000000000000137.

34. Salimi AFS, Mut F, Chung BJ, Robertson AM, Cebral JR. Hemodynamic conditions that favor bleb formation in cerebral aneurysms. J. Neurointerv. Surg. 2021;13(3):231-236. doi: 10.1136/neurintsurg-2020-016369.

35. Shojima M. Nemoto S, Morita A, Oshima M, Watanabe E, Saito N. Role of shear stress in the blister formation of cerebral aneurysms. Neurosurgery. 2010;67(5): 1268–1274. https://doi. org/10.1227/NEU.0b013 e3181 f2f442 (2010).

36. Machi P, Ouared R, Brina O, Bouillot P, Hasan Yilmaz H, Vargas MI, Gondar R, Bijlenga P, Lovblad O, Kulcsár Z. Hemodynamics of focal versus global growth of small cerebral aneurysms. Clin. Neuroradiol. 2019;29(2):285-293. doi: 10.1007/s00062-017-0640-6. Epub 2017 Dec 5.