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Published in: BMC Neurology 1/2022

Open Access 01-12-2022 | Intracranial Aneurysm | Research

Morphometry of cerebral arterial bifurcations harbouring aneurysms: a case-control study

Authors: K. Ćmiel-Smorzyk, E. Kawlewska, W. Wolański, A. Hebda, P. Ładziński, W. Kaspera

Published in: BMC Neurology | Issue 1/2022

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Abstract

Background

Conclusions from studies evaluating vessel dimensions and their deviations from values resulting from the principle of minimum work (PMW) on the formation of intracranial aneurysms (IAs) are still inconclusive. Our study aimed to perform a morphometric analysis of cerebral arterial bifurcations harbouring aneurysms.

Methods

The study comprised 147 patients with basilar artery (BA) and middle cerebral artery (MCA) aneurysms and 106 patients constituting the control group. The following morphometric parameters were evaluated: the radii of vessels forming the bifurcation, the junction exponent, the values of the bifurcation angles (Φ1 and Φ2 angles between the parent vessel trunk axis and the larger or smaller branches, respectively; α angle, the total bifurcation angle) and the difference between the predicted optimal and observed branch angles.

Results

The analysed parameters for internal carotid artery (ICA) bifurcations were not significantly different among the groups. The MCA and BA bifurcation angles and the radii of the parent MCA and BA vessels with aneurysms were significantly higher than those of the control group. The differences between the predicted optimal and observed branch angles were significantly higher for BA and MCA bifurcations with aneurysms compared to the control group. The mean junction exponent for bifurcations in the circle of Willis (i.e., ICA and BA bifurcations, respectively) and MCA bifurcations with aneurysms was significantly lower than the theoretical optimum and did not significantly differ among the groups. In a multilevel multivariate logistic regression analysis, the branch angles and the radius from the parent vessel were significant independent predictors of the presence of an IA. The ROC analysis indicated that the α angle was the best performer in discriminating between aneurysmal and nonaneurysmal bifurcations.

Conclusions

The dimensions of the arteries forming the circle of Willis do not follow the PMW. Deviation from the energetically optimum geometry for bifurcations beyond the circle of Willis (particularly, a larger radius of the parent artery and a wider total bifurcation angle) may lead to the formation of IAs. Further studies are warranted to investigate the significance of vessel dimensions and the bifurcation angle on the magnitude of shear stress in the walls of arterial bifurcations.
Literature
1.
go back to reference Hitchcock E, Gibson WT. A review of the genetics of intracranial berry aneurysms and implications for genetic counseling. J Genet Couns. 2017;26(1):21–31.PubMedCrossRef Hitchcock E, Gibson WT. A review of the genetics of intracranial berry aneurysms and implications for genetic counseling. J Genet Couns. 2017;26(1):21–31.PubMedCrossRef
2.
3.
go back to reference Meng H, Swartz DD, Wang Z, Hoi Y, Kolega J, Metaxa EM, et al. A model system for mapping vascular responses to complex hemodynamics at arterial bifurcations in vivo. Neurosurgery. 2006;59(5):1094–100 discussion 100-1.PubMedCrossRef Meng H, Swartz DD, Wang Z, Hoi Y, Kolega J, Metaxa EM, et al. A model system for mapping vascular responses to complex hemodynamics at arterial bifurcations in vivo. Neurosurgery. 2006;59(5):1094–100 discussion 100-1.PubMedCrossRef
4.
go back to reference Meng H, Wang Z, Hoi Y, Gao L, Metaxa E, Swartz DD, et al. Complex hemodynamics at the apex of an arterial bifurcation induces vascular remodeling resembling cerebral aneurysm initiation. Stroke. 2007;38(6):1924–31.PubMedPubMedCentralCrossRef Meng H, Wang Z, Hoi Y, Gao L, Metaxa E, Swartz DD, et al. Complex hemodynamics at the apex of an arterial bifurcation induces vascular remodeling resembling cerebral aneurysm initiation. Stroke. 2007;38(6):1924–31.PubMedPubMedCentralCrossRef
5.
go back to reference Alfano JM, Kolega J, Natarajan SK, Xiang J, Paluch RA, Levy EI, et al. Intracranial aneurysms occur more frequently at bifurcation sites that typically experience higher hemodynamic stresses. Neurosurgery. 2013;73(3):497–505.PubMedCrossRef Alfano JM, Kolega J, Natarajan SK, Xiang J, Paluch RA, Levy EI, et al. Intracranial aneurysms occur more frequently at bifurcation sites that typically experience higher hemodynamic stresses. Neurosurgery. 2013;73(3):497–505.PubMedCrossRef
6.
go back to reference Alnaes MS, Isaksen J, Mardal KA, Romner B, Morgan MK, Ingebrigtsen T. Computation of hemodynamics in the circle of Willis. Stroke. 2007;38(9):2500–5.PubMedCrossRef Alnaes MS, Isaksen J, Mardal KA, Romner B, Morgan MK, Ingebrigtsen T. Computation of hemodynamics in the circle of Willis. Stroke. 2007;38(9):2500–5.PubMedCrossRef
7.
go back to reference Ku DN, Giddens DP, Zarins CK, Glagov S. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis. 1985;5(3):293–302.PubMedCrossRef Ku DN, Giddens DP, Zarins CK, Glagov S. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis. 1985;5(3):293–302.PubMedCrossRef
8.
go back to reference Mantha A, Karmonik C, Benndorf G, Strother C, Metcalfe R. Hemodynamics in a cerebral artery before and after the formation of an aneurysm. AJNR Am J Neuroradiol. 2006;27(5):1113–8.PubMedPubMedCentral Mantha A, Karmonik C, Benndorf G, Strother C, Metcalfe R. Hemodynamics in a cerebral artery before and after the formation of an aneurysm. AJNR Am J Neuroradiol. 2006;27(5):1113–8.PubMedPubMedCentral
9.
go back to reference Shimogonya Y, Ishikawa T, Imai Y, Matsuki N, Yamaguchi T. Can temporal fluctuation in spatial wall shear stress gradient initiate a cerebral aneurysm? A proposed novel hemodynamic index, the gradient oscillatory number (GON). J Biomech. 2009;42(4):550–4.PubMedCrossRef Shimogonya Y, Ishikawa T, Imai Y, Matsuki N, Yamaguchi T. Can temporal fluctuation in spatial wall shear stress gradient initiate a cerebral aneurysm? A proposed novel hemodynamic index, the gradient oscillatory number (GON). J Biomech. 2009;42(4):550–4.PubMedCrossRef
10.
go back to reference Zimny M, Kawlewska E, Hebda A, Wolański W, Ładziński P, Kaspera W. Wall shear stress gradient is independently associated with middle cerebral artery aneurysm development: a case-control CFD patient-specific study based on 77 patients. BMC Neurol. 2021;21(1):281.PubMedPubMedCentralCrossRef Zimny M, Kawlewska E, Hebda A, Wolański W, Ładziński P, Kaspera W. Wall shear stress gradient is independently associated with middle cerebral artery aneurysm development: a case-control CFD patient-specific study based on 77 patients. BMC Neurol. 2021;21(1):281.PubMedPubMedCentralCrossRef
11.
go back to reference Ferguson GG. Physical factors in the initiation, growth, and rupture of human intracranial saccular aneurysms. J Neurosurg. 1972;37(6):666–77.PubMedCrossRef Ferguson GG. Physical factors in the initiation, growth, and rupture of human intracranial saccular aneurysms. J Neurosurg. 1972;37(6):666–77.PubMedCrossRef
12.
go back to reference Roach MR, Scott S, Ferguson GG. The hemodynamic importance of the geometry of bifurcations in the circle of Willis (glass model studies). Stroke. 1972;3(3):255–67.PubMedCrossRef Roach MR, Scott S, Ferguson GG. The hemodynamic importance of the geometry of bifurcations in the circle of Willis (glass model studies). Stroke. 1972;3(3):255–67.PubMedCrossRef
13.
go back to reference Ujiie H, Liepsch DW, Goetz M, Yamaguchi R, Yonetani H, Takakura K. Hemodynamic study of the anterior communicating artery. Stroke. 1996;27(11):2086–93 discussion 94.PubMedCrossRef Ujiie H, Liepsch DW, Goetz M, Yamaguchi R, Yonetani H, Takakura K. Hemodynamic study of the anterior communicating artery. Stroke. 1996;27(11):2086–93 discussion 94.PubMedCrossRef
14.
go back to reference Rossitti S. Shear stress in cerebral arteries carrying saccular aneurysms. A preliminary study Acta Radiol. 1998;39(6):711–7.PubMedCrossRef Rossitti S. Shear stress in cerebral arteries carrying saccular aneurysms. A preliminary study Acta Radiol. 1998;39(6):711–7.PubMedCrossRef
15.
go back to reference Murray CD. The Physiological principle of minimum work: I. the vascular system and the cost of blood volume. Proc Natl Acad Sci U S A. 1926;12(3):207–14.PubMedPubMedCentralCrossRef Murray CD. The Physiological principle of minimum work: I. the vascular system and the cost of blood volume. Proc Natl Acad Sci U S A. 1926;12(3):207–14.PubMedPubMedCentralCrossRef
17.
go back to reference Hutchins GM, Miner MM, Boitnott JK. Vessel caliber and branch-angle of human coronary artery branch-points. Circ Res. 1976;38(6):572–6.PubMedCrossRef Hutchins GM, Miner MM, Boitnott JK. Vessel caliber and branch-angle of human coronary artery branch-points. Circ Res. 1976;38(6):572–6.PubMedCrossRef
18.
go back to reference Zamir M, Chee H. Branching characteristics of human coronary arteries. Can J Physiol Pharmacol. 1986;64(6):661–8.PubMedCrossRef Zamir M, Chee H. Branching characteristics of human coronary arteries. Can J Physiol Pharmacol. 1986;64(6):661–8.PubMedCrossRef
19.
go back to reference Rossitti S, Löfgren J. Vascular dimensions of the cerebral arteries follow the principle of minimum work. Stroke. 1993;24(3):371–7.PubMedCrossRef Rossitti S, Löfgren J. Vascular dimensions of the cerebral arteries follow the principle of minimum work. Stroke. 1993;24(3):371–7.PubMedCrossRef
20.
go back to reference Baharoglu MI, Lauric A, Wu C, Hippelheuser J, Malek AM. Deviation from optimal vascular caliber control at middle cerebral artery bifurcations harboring aneurysms. J Biomech. 2014;47(13):3318–24.PubMedPubMedCentralCrossRef Baharoglu MI, Lauric A, Wu C, Hippelheuser J, Malek AM. Deviation from optimal vascular caliber control at middle cerebral artery bifurcations harboring aneurysms. J Biomech. 2014;47(13):3318–24.PubMedPubMedCentralCrossRef
21.
go back to reference Zhang XJ, Li CH, Hao WL, Zhang DH, Gao BL. The optimality principle decreases hemodynamic stresses for aneurysm initiation at anterior cerebral artery bifurcations. World Neurosurg. 2019;121:e379–e88.PubMedCrossRef Zhang XJ, Li CH, Hao WL, Zhang DH, Gao BL. The optimality principle decreases hemodynamic stresses for aneurysm initiation at anterior cerebral artery bifurcations. World Neurosurg. 2019;121:e379–e88.PubMedCrossRef
22.
23.
go back to reference Diagbouga MR, Morel S, Bijlenga P, Kwak BR. Role of hemodynamics in initiation/growth of intracranial aneurysms. Eur J Clin Investig. 2018;48(9):e12992.CrossRef Diagbouga MR, Morel S, Bijlenga P, Kwak BR. Role of hemodynamics in initiation/growth of intracranial aneurysms. Eur J Clin Investig. 2018;48(9):e12992.CrossRef
24.
go back to reference Tütüncü F, Schimansky S, Baharoglu MI, Gao B, Calnan D, Hippelheuser J, et al. Widening of the basilar bifurcation angle: association with presence of intracranial aneurysm, age, and female sex. J Neurosurg. 2014;121(6):1401–10.PubMedCrossRef Tütüncü F, Schimansky S, Baharoglu MI, Gao B, Calnan D, Hippelheuser J, et al. Widening of the basilar bifurcation angle: association with presence of intracranial aneurysm, age, and female sex. J Neurosurg. 2014;121(6):1401–10.PubMedCrossRef
25.
go back to reference Xu L, Zhang F, Wang H, Yu Y. Contribution of the hemodynamics of A1 dysplasia or hypoplasia to anterior communicating artery aneurysms: a 3-dimensional numerical simulation study. J Comput Assist Tomogr. 2012;36(4):421–6.PubMedCrossRef Xu L, Zhang F, Wang H, Yu Y. Contribution of the hemodynamics of A1 dysplasia or hypoplasia to anterior communicating artery aneurysms: a 3-dimensional numerical simulation study. J Comput Assist Tomogr. 2012;36(4):421–6.PubMedCrossRef
26.
go back to reference Lauric A, Hippelheuser JE, Malek AM. Induction of aneurysmogenic high positive wall shear stress gradient by wide angle at cerebral bifurcations, independent of flow rate. J Neurosurg. 2018;131(2):442–52.PubMedCrossRef Lauric A, Hippelheuser JE, Malek AM. Induction of aneurysmogenic high positive wall shear stress gradient by wide angle at cerebral bifurcations, independent of flow rate. J Neurosurg. 2018;131(2):442–52.PubMedCrossRef
27.
go back to reference Kaspera W, Ładziński P, Larysz P, Hebda A, Ptaszkiewicz K, Kopera M, et al. Morphological, hemodynamic, and clinical independent risk factors for anterior communicating artery aneurysms. Stroke. 2014;45(10):2906–11.PubMedCrossRef Kaspera W, Ładziński P, Larysz P, Hebda A, Ptaszkiewicz K, Kopera M, et al. Morphological, hemodynamic, and clinical independent risk factors for anterior communicating artery aneurysms. Stroke. 2014;45(10):2906–11.PubMedCrossRef
28.
go back to reference Kayembe KN, Sasahara M, Hazama F. Cerebral aneurysms and variations in the circle of Willis. Stroke. 1984;15(5):846–50.PubMedCrossRef Kayembe KN, Sasahara M, Hazama F. Cerebral aneurysms and variations in the circle of Willis. Stroke. 1984;15(5):846–50.PubMedCrossRef
29.
go back to reference Stehbens WE. Aneurysms and anatomical variation of cerebral arteries. Arch Pathol. 1963;75:45–64.PubMed Stehbens WE. Aneurysms and anatomical variation of cerebral arteries. Arch Pathol. 1963;75:45–64.PubMed
30.
31.
go back to reference Kaspera W, Ćmiel-Smorzyk K, Wolański W, Kawlewska E, Hebda A, Gzik M, et al. Morphological and hemodynamic risk factors for middle cerebral artery aneurysm: a case-control study of 190 patients. Sci Rep. 2020;10(1):2016.PubMedPubMedCentralCrossRef Kaspera W, Ćmiel-Smorzyk K, Wolański W, Kawlewska E, Hebda A, Gzik M, et al. Morphological and hemodynamic risk factors for middle cerebral artery aneurysm: a case-control study of 190 patients. Sci Rep. 2020;10(1):2016.PubMedPubMedCentralCrossRef
32.
go back to reference Can A, Ho AL, Dammers R, Dirven CM, Du R. Morphological parameters associated with middle cerebral artery aneurysms. Neurosurgery. 2015;76(6):721–6 discussion 6-7.PubMedCrossRef Can A, Ho AL, Dammers R, Dirven CM, Du R. Morphological parameters associated with middle cerebral artery aneurysms. Neurosurgery. 2015;76(6):721–6 discussion 6-7.PubMedCrossRef
33.
go back to reference Can A, Mouminah A, Ho AL, Du R. Effect of vascular anatomy on the formation of basilar tip aneurysms. Neurosurgery. 2015;76(1):62–6 discussion 6.PubMedCrossRef Can A, Mouminah A, Ho AL, Du R. Effect of vascular anatomy on the formation of basilar tip aneurysms. Neurosurgery. 2015;76(1):62–6 discussion 6.PubMedCrossRef
34.
go back to reference Can A, Ho AL, Emmer BJ, Dammers R, Dirven CM, Du R. Association between vascular anatomy and posterior communicating artery aneurysms. World Neurosurg. 2015;84(5):1251–5.PubMedCrossRef Can A, Ho AL, Emmer BJ, Dammers R, Dirven CM, Du R. Association between vascular anatomy and posterior communicating artery aneurysms. World Neurosurg. 2015;84(5):1251–5.PubMedCrossRef
35.
go back to reference Bor AS, Velthuis BK, Majoie CB, Rinkel GJ. Configuration of intracranial arteries and development of aneurysms: a follow-up study. Neurology. 2008;70(9):700–5.PubMedCrossRef Bor AS, Velthuis BK, Majoie CB, Rinkel GJ. Configuration of intracranial arteries and development of aneurysms: a follow-up study. Neurology. 2008;70(9):700–5.PubMedCrossRef
36.
go back to reference Sadatomo T, Yuki K, Migita K, Imada Y, Kuwabara M, Kurisu K. Differences between middle cerebral artery bifurcations with normal anatomy and those with aneurysms. Neurosurg Rev. 2013;36(3):437–45.PubMedCrossRef Sadatomo T, Yuki K, Migita K, Imada Y, Kuwabara M, Kurisu K. Differences between middle cerebral artery bifurcations with normal anatomy and those with aneurysms. Neurosurg Rev. 2013;36(3):437–45.PubMedCrossRef
37.
go back to reference Zhang XJ, Gao BL, Hao WL, Wu SS, Zhang DH. Presence of anterior communicating artery aneurysm is associated with age, bifurcation angle, and vessel diameter. Stroke. 2018;49(2):341–7.PubMedCrossRef Zhang XJ, Gao BL, Hao WL, Wu SS, Zhang DH. Presence of anterior communicating artery aneurysm is associated with age, bifurcation angle, and vessel diameter. Stroke. 2018;49(2):341–7.PubMedCrossRef
38.
go back to reference Zhang XJ, Gao BL, Li TX, Hao WL, Wu SS, Zhang DH. Association of Basilar Bifurcation Aneurysms with age, sex, and bifurcation geometry. Stroke. 2018;49(6):1371–6.PubMedCrossRef Zhang XJ, Gao BL, Li TX, Hao WL, Wu SS, Zhang DH. Association of Basilar Bifurcation Aneurysms with age, sex, and bifurcation geometry. Stroke. 2018;49(6):1371–6.PubMedCrossRef
39.
go back to reference Zhang XJ, Hao WL, Zhang DH, Gao BL. Asymmetrical middle cerebral artery bifurcations are more vulnerable to aneurysm formation. Sci Rep. 2019;9(1):15255.PubMedPubMedCentralCrossRef Zhang XJ, Hao WL, Zhang DH, Gao BL. Asymmetrical middle cerebral artery bifurcations are more vulnerable to aneurysm formation. Sci Rep. 2019;9(1):15255.PubMedPubMedCentralCrossRef
40.
go back to reference Zhang XJ, Hao WL, Zhang DH, Gao BL. Asymmetrical than symmetrical cerebral arterial bifurcations are more vulnerable to aneurysm presence. Sci Rep. 2019;9(1):17144.PubMedPubMedCentralCrossRef Zhang XJ, Hao WL, Zhang DH, Gao BL. Asymmetrical than symmetrical cerebral arterial bifurcations are more vulnerable to aneurysm presence. Sci Rep. 2019;9(1):17144.PubMedPubMedCentralCrossRef
41.
go back to reference Ingebrigtsen T, Morgan MK, Faulder K, Ingebrigtsen L, Sparr T, Schirmer H. Bifurcation geometry and the presence of cerebral artery aneurysms. J Neurosurg. 2004;101(1):108–13.PubMedCrossRef Ingebrigtsen T, Morgan MK, Faulder K, Ingebrigtsen L, Sparr T, Schirmer H. Bifurcation geometry and the presence of cerebral artery aneurysms. J Neurosurg. 2004;101(1):108–13.PubMedCrossRef
42.
go back to reference Zhang XJ, Li CH, Hao WL, Zhang DH, Ren CF, Gao BL. Enlarged anterior cerebral artery bifurcation angles may induce abnormally enhanced hemodynamic stresses to initiate aneurysms. World Neurosurg. 2018;120:e783–e91.PubMedCrossRef Zhang XJ, Li CH, Hao WL, Zhang DH, Ren CF, Gao BL. Enlarged anterior cerebral artery bifurcation angles may induce abnormally enhanced hemodynamic stresses to initiate aneurysms. World Neurosurg. 2018;120:e783–e91.PubMedCrossRef
43.
go back to reference Kasuya H, Shimizu T, Nakaya K, Sasahara A, Hori T, Takakura K. Angles between A1 and A2 segments of the anterior cerebral artery visualized by three-dimensional computed tomographic angiography and association of anterior communicating artery aneurysms. Neurosurgery. 1999;45(1):89–93 discussion -4.PubMed Kasuya H, Shimizu T, Nakaya K, Sasahara A, Hori T, Takakura K. Angles between A1 and A2 segments of the anterior cerebral artery visualized by three-dimensional computed tomographic angiography and association of anterior communicating artery aneurysms. Neurosurgery. 1999;45(1):89–93 discussion -4.PubMed
44.
go back to reference Ye J, Zheng P, Hassan M, Jiang S, Zheng J. Relationship of the angle between the A1 and A2 segments of the anterior cerebral artery with formation and rupture of anterior communicating artery aneurysm. J Neurol Sci. 2017;375:170–4.PubMedCrossRef Ye J, Zheng P, Hassan M, Jiang S, Zheng J. Relationship of the angle between the A1 and A2 segments of the anterior cerebral artery with formation and rupture of anterior communicating artery aneurysm. J Neurol Sci. 2017;375:170–4.PubMedCrossRef
45.
go back to reference Baharoglu MI, Lauric A, Safain MG, Hippelheuser J, Wu C, Malek AM. Widening and high inclination of the middle cerebral artery bifurcation are associated with presence of aneurysms. Stroke. 2014;45(9):2649–55.PubMedPubMedCentralCrossRef Baharoglu MI, Lauric A, Safain MG, Hippelheuser J, Wu C, Malek AM. Widening and high inclination of the middle cerebral artery bifurcation are associated with presence of aneurysms. Stroke. 2014;45(9):2649–55.PubMedPubMedCentralCrossRef
46.
go back to reference Zamir M, Bigelow DC. Cost of departure from optimality in arterial branching. J Theor Biol. 1984;109(3):401–9.PubMedCrossRef Zamir M, Bigelow DC. Cost of departure from optimality in arterial branching. J Theor Biol. 1984;109(3):401–9.PubMedCrossRef
Metadata
Title
Morphometry of cerebral arterial bifurcations harbouring aneurysms: a case-control study
Authors
K. Ćmiel-Smorzyk
E. Kawlewska
W. Wolański
A. Hebda
P. Ładziński
W. Kaspera
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2022
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-022-02559-8

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