Abstract
Background
The recanalization of posterior communicating artery (PCoA) aneurysms after endovascular treatment has been analyzed by various factors. However, the differences between adult and fetal types of posterior cerebral artery (PCA) have not been fully investigated. The main aim of this study was to investigate hemodynamic differences of PCoA aneurysms between adult and fetal types using computational fluid dynamics (CFD).
Methods
Fifty-five PCoA aneurysms were evaluated by 3D CT angiography and divided into unruptured aneurysms with adult-type or fetal-type PCAs (19 cases, UA group; 9 cases, UF group) and ruptured aneurysms with adult-type or fetal-type PCAs (17 cases, RA group; 10 cases, RF group). These native aneurysms were analyzed by CFD regarding morphological and hemodynamic characteristics. To evaluate simulated endovascular treatment of aneurysms, CFD was performed using porous media modeling.
Results
Morphologically, the RA group had significantly smaller parent artery diameter (2.91 mm vs. 3.49 mm, p=0.005) and higher size ratio (2.54 vs. 1.78, p=0.023) than the RF group. CFD revealed that the UA group had significantly lower oscillatory shear index (OSI) (0.0032 vs. 0.0078, p=0.004) than the UF group and that the RA group had lower WSS (3.09 vs. 11.10, p=0.001) and higher OSI (0.014 vs. 0.006, p=0.031) than the RF group, while the RF group presented significantly higher intra-aneurysmal flow velocity (0.19 m/s vs. 0.061 m/s, p=0.002) than the RA group. Porous media modeling of simulated treatment revealed higher residual flow volume in the fetal-type groups.
Conclusions
These results suggested that PCoA aneurysms with fetal-type PCAs had different morphological features and hemodynamic characteristics compared with those with adult-type PCAs, leading to high risks of recanalization.
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Data availability
All data relevant to the study are included in the article or uploaded as supplementary information.
Code availability
Not applicable.
References
Abdehkakha A, Hammond AL, Patel TR, Siddiqui AH, Dargush GF, Meng H (2021) Cerebral aneurysm flow diverter modeled as a thin inhomogeneous porous medium in hemodynamic simulations. Comput Biol Med. 139:104988. https://doi.org/10.1016/j.compbiomed.2021.104988
Akgiray Ö, Saatçı AM (2001) A new look at filter backwash hydraulics. Water Supply 1(2):65–72. https://doi.org/10.2166/ws.2001.0022
Augsburger L, Reymond P, Rufenacht DA, Stergiopulos N (2011) Intracranial stents being modeled as a porous medium: flow simulation in stented cerebral aneurysms. Ann Biomed Eng 39(2):850–863. https://doi.org/10.1007/s10439-010-0200-6
Beppu M, Tsuji M, Ishida F, Shirakawa M, Suzuki H, Yoshimura S (2020) Computational fluid dynamics using a porous media setting predicts outcome after flow-diverter treatment. AJNR Am J Neuroradiol. 41:2107–2113. https://doi.org/10.3174/ajnr.A6766
Campi A, Ramzi N, Molyneux AJ, Summers PE, Kerr RS, Sneade M, Yarnold JA, Rischmiller J, Byrne JV (2007) Retreatment of ruptured cerebral aneurysms in patients randomized by coiling or clipping in the international subarachnoid aneurysm trial (ISAT). Stroke 38:1538–1544. https://doi.org/10.1161/STROKEAHA.106.466987
Can A, Ho AL, Emmer BJ, Dammers R, Dirven CM, Du R (2015) Association between vascular anatomy and posterior communicating artery aneurysms. World Neurosurg 84(5):1251–1255. https://doi.org/10.1016/j.wneu.2015.05.078
Cho YD, Lee WJ, Kim KM, Kang HS, Kim JE, Han MH (2013) Stent-assisted coil embolization of posterior communicating artery aneurysms. AJNR 34(11):2171–2176. https://doi.org/10.3174/ajnr.A3541
Choi HH, Cho YD, Yoo DH, Lee HS, Kim SH, Jang D, Lee SH, Cho WS, Kang HS, Kim JE (2020) Impact of fetal-type posterior cerebral artery on recanalization of posterior communicating artery aneurysms after coil embolization: matched-pair case–control study. J Neurointerv Surg 12(8):783–787. https://doi.org/10.1136/neurintsurg-2019-015531
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. AJNR 38(11):2111–2118. https://doi.org/10.3174/ajnr.A5358
Chung J, Cheong JH, Kim JM, Lee DH, Yi HJ, Choi KS, Ahn JS, Park JC, Park W (2023) Is fetal-type posterior cerebral artery a risk factor for recurrence in coiled internal carotid artery-incorporating posterior communicating artery aneurysms? Analysis of conventional statistics, computational fluid dynamics, and random forest with hyper-ensemble approach. Neurosurgery 93(3):611–621. https://doi.org/10.1227/neu.0000000000002458
Corns R, Zebian B, Tait MJ, Walsh D, Hampton T, Deasy N, Tolias C (2013) Prevalence of recurrence and retreatment of ruptured intracranial aneurysms treated with endovascular coil occlusion. Br J Neurosurg 27(1):30–33. https://doi.org/10.3109/02688697.2012.701676
Crobeddu E, Lanzino G, Kallmes DF, Cloft HJ (2013) Review of 2 decades of aneurysm-recurrence literature, part 1: reducing recurrence after endovascular coiling. AJNR 34(2):266–270. https://doi.org/10.3174/ajnr.A3032
Daou B, Chalouhi N, Starke RM, Barros G, Ya'qoub L, Do J, Tjoumakaris S, Rosenwasser RH, Jabbour P (2016) Clipping of previously coiled cerebral aneurysms: efficacy, safety, and predictors in a cohort of 111 patients. J Neurosurg 125(6):1337–1343. https://doi.org/10.3171/2015.10.JNS151544
Ergun S (1952) Fluid flow through packed columns. Chem Eng Prog 48:85–94
Golshani K, Ferrell A, Zomorodi A, Smith TP, Britz GW (2010) A review of the management of posterior communicating artery aneurysms in the modern era. Surg Neurol Int 22(1):88. https://doi.org/10.4103/2152-7806.74147
Hassan T, Timofeev EV, Saito T, Shimizu H, Ezura M, Matsumoto Y, Takayama K, Tominaga T, Takahashi A (2005) A proposed parent vessel geometry–based categorization of saccular intracranial aneurysms: computational flow dynamics analysis of the risk factors for lesion rupture. J Neurosurg 103(4):662–680. https://doi.org/10.3171/jns.2005.103.4.0662
He Z, Wan Y (2018) Is fetal-type posterior cerebral artery a risk factor for intracranial aneurysm as analyzed by multislice CT angiography? Exp Ther Med 15(1):838–846. https://doi.org/10.3892/etm.2017.5504
Horikoshi T, Akiyama I, Yamagata Z, Sugita M, Nukui H (2002) Magnetic resonance angiographic evidence of sex-linked variations in the circle of Willis and the occurrence of cerebral aneurysms. J Neurosurg 96(4):697–703. https://doi.org/10.3171/jns.2002.96.4.0697
Ishida F, Tsuji M, Tanioka S, Tanaka K, Yoshimura S, Suzuki H, Esposito G, Regli L, Cenzato M, Kaku Y, Tanaka M, Tsukahara T (2021) Computational fluid dynamics for cerebral aneurysms in clinical settings. In: Trends in cerebrovascular surgery and interventions [Internet]. Springer, Cham (CH). https://doi.org/10.1007/978-3-030-63453-7_4
Jiang Y, Ge L, Di R, Lu G, Huang L, Li G, Leng X, Zhang S, Wan H, Geng D, Xiang J, Zhang XJ (2019) Differences in hemodynamic characteristics under high packing density between the porous media model and finite element analysis in computational fluid dynamics of intracranial aneurysm virtual treatment. Neurointerv Surg. 11(8):853–858. https://doi.org/10.1136/neurintsurg-2018-014218
Jou LD, Lee DH, Morsi H, Mawad ME (2008) Wall shear stress on ruptured and unruptured intracranial aneurysms at the internal carotid artery. AJNR Am J Neuroradiol 29(9):1761–1767. https://doi.org/10.3174/ajnr.A1180
Kim T, Oh CW, Bang JS, Ban SP, Lee SU, Kim YD, Kwon OK (2021) Higher oscillatory shear index is related to aneurysm recanalization after coil embolization in posterior communicating artery aneurysms. Acta Neurochir (Wien) 163(8):2327–2337. https://doi.org/10.1007/s00701-020-04607-z
Ku DN, Giddens DP, Zarins CK, Glagov S (1985) Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis. 5(3):293–302. https://doi.org/10.1161/01.atv.5.3.293
Luo B, Yang X, Wang S, Li H, Chen J, Yu H, Zhang Y, Zhang Y, Mu S, Liu Z, Ding G (2011) High shear stress and flow velocity in partially occluded aneurysms prone to recanalization. Stroke 42(3):745–753. https://doi.org/10.1161/STROKEAHA.110.593517
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(2):e0149906. https://doi.org/10.1371/journal.pone.0149906
Masanori T, Fujimaro I, Tomoyuki K, Kazuhiro F, Yoichi M, Masato S, Takanori S, Keiji F, Katsuhiro T, Hiroshi T, Yasuyuki U, Ryuta Y, Shinichi S, Hidenori S (2020) Double porous media modeling in computational fluid dynamics for hemodynamics of stent-assisted coiling of intracranial aneurysms: a technical case report. Brain Hemorrhages 1(1):85–88
Masanori T, Fujimaro I, Takenori S, Kazuhiro F, Yoichi M, Ryuta Y, Yasuyuki U, Naoki T, Hidenori S (2023) Computational fluid dynamics using dual-layer porous media modeling to evaluate the hemodynamics of cerebral aneurysm treated with FRED: a technical note. Brain Hemorrhages 4(1):39–43
Matthew DF, Noam A, Sung HL, David WH, David AS (2005) Characterization of volumetric flow rate waveforms in the normal internal carotid and vertebral arteries. Physiol Meas 26(4):477–488. https://doi.org/10.1088/0967-3334/26/4/013
Meng H, Tutino VM, Xiang J, Siddiqui A (2017) High WSS or low WSS? Complex interactions of hemodynamics with intracranial aneurysm initiation, growth, and rupture: toward a unifying hypothesis. AJNR Am J Neuroradiol 35(7):1254–1262. https://doi.org/10.3174/ajnr.A3558
Misaki K, Takao H, Suzuki T, Nishimura K, Kan I, Yuki I, Ishibashi T, Yamamoto M, Murayama Y (2017) Estimated pretreatment hemodynamic prognostic factors of aneurysm recurrence after endovascular embolization. Technol Health Care 25(5):843–850. https://doi.org/10.3233/THC-160495
Nambu I, Misaki K, Uchiyama N, Mohri M, Suzuki T, Takao H, Murayama Y, Futami K, Kawamura T, Inoguchi Y, Matsuzawa T, Nakada M (2019) High pressure in virtual postcoiling model is a predictor of internal carotid artery aneurysm recurrence after coiling. Neurosurgery 84(3):607–615. https://doi.org/10.1093/neuros/nyy073
Ojemann RG, Crowell RM (1988) Internal carotid artery aneurysms. Surgical management of cerebrovascular disease, 2nd edn. Williams and Wilkins, Baltimore, pp 179–198
Roy AK, Howard BM, Haussen DC, Osbun JW, Halani SH, Skukalek SL, Tong F, Nogueira RG, Dion JE, Cawley CM, Grossberg JA (2018) Reduced efficacy of the pipeline embolization device in the treatment of posterior communicating region aneurysms with fetal posterior cerebral artery configuration. Neurosurgery 82(5):695–700. https://doi.org/10.1093/neuros/nyx293
Sano T, Ishida F, Tsuji M, Furukawa K, Shimosaka S, Suzuki H (2017) Hemodynamic differences between ruptured and unruptured cerebral aneurysms simultaneously existing in the same location: 2 case reports and proposal of a novel parameter oscillatory velocity index. World Neurosurg 98:868.e5–868.e10. https://doi.org/10.1016/j.wneu.2016.12.047
Shaban A, Albright KC, Boehme AK, Martin-Schild S (2013) Circle of Willis variants: fetal PCA. Stroke Res Treat 2013:105937. https://doi.org/10.1155/2013/105937
Shiba M, Ishida F, Furukawa K, Tanemura H, Tsuji M, Shimosaka S, Suzuki H (2017) Relationships of morphologic parameters and hemodynamic parameters determined by computational fluid dynamics analysis with the severity of subarachnoid hemorrhage. JNET 11(10):512–519. https://doi.org/10.5797/jnet.oa.2016-0099
Songsaeng D, Geibprasert S, Willinsky R, Tymianski M, TerBrugge KG, Krings T (2010) Impact of anatomical variations of the circle of Willis on the incidence of aneurysms and their recurrence rate following endovascular treatment. Clin Radiol 65(11):895–901. https://doi.org/10.1016/j.crad.2010.06.010
Songsaeng D, Geibprasert S, ter Brugge KG, Willinsky R, Tymianski M, Krings T (2011) Impact of individual intracranial arterial aneurysm morphology on initial obliteration and recurrence rates of endovascular treatments: a multivariate analysis. J Neurosurg 114(4):994–1002. https://doi.org/10.3171/2010.8.JNS10241
Tanioka S, Ishida F, Kishimoto T, Tsuji M, Tanaka K, Shimosaka S, Toyoda M, Kashiwagi N, Sano T, Suzuki H (2019) Quantification of hemodynamic irregularity using oscillatory velocity index in the associations with the rupture status of cerebral aneurysms. J Neurointerv Surg 11(6):614–617. https://doi.org/10.1136/neurintsurg-2018-014489
Tanioka S, Ishida F, Yamamoto A, Shimizu S, Sakaida H, Toyoda M, Kashiwagi N, Suzuki H (2020) Machine learning classification of cerebral aneurysm rupture status with morphologic variables and hemodynamic parameters. Radiol Artif Intell. 2(1):e190077. https://doi.org/10.1148/ryai.2019190077
Tomoaki S, Nobuyuki G, Toshiharu N, Hiroshi A (2020) Assessing the hemodynamics in residual cavities of intracranial aneurysm after coil embolization with combined computational flow dynamics and silent magnetic resonance angiography. J Stroke Cerebrovasc Dis 29(12):105290. https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.105290
Tsuji M, Ishida F, Kishimoto T, Furukawa K, Miura Y, Shiba M, Sano T, Fukazawa K, Tanaka K, Tanemura H, Umeda Y, Yasuda R, Shimosaka S, Suzuki H (2020) Double porous media modeling in computational fluid dynamics for hemodynamics of stent-assisted coiling of intracranial aneurysms: a technical case report. Brain Hemorrhages 1(1):85–88. https://doi.org/10.1016/j.hest.2020.01.004
Umeda Y, Ishida F, Tsuji M, Furukawa K, Shiba M, Yasuda R, Toma N, Sakaida H, Suzuki H (2017) Computational fluid dynamics (CFD) using porous media modeling predicts recurrence after coiling of cerebral aneurysms. PLoS One 12:e0190222. https://doi.org/10.1371/journal.pone.0190222
van Raamt AF, Mali WP, van Laar PJ, van der Graaf Y (2006) The fetal variant of the circle of Willis and its influence on the cerebral collateral circulation. Cerebrovasc Dis 22:217–224. https://doi.org/10.1159/000094007
Wallace AN, Kayan Y, Austin MJ, Delgado Almandoz JE, Kamran M, Cross DT 3rd, Moran CJ, Osbun JW, Kansagra AP (2017) Pipeline embolization of posterior communicating artery aneurysms associated with a fetal origin posterior cerebral artery. Clin Neurol Neurosurg 160:83–87. https://doi.org/10.1016/j.clineuro.2017.06.014
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(1):144–152. https://doi.org/10.1161/STROKEAHA.110.592923
Xiang J, Tremmel M, Kolega J, Levy EI, Natarajan SK, Meng H (2012) Newtonian viscosity model could overestimate wall shear stress in intracranial aneurysm domes and underestimate rupture risk. J Neurointerv Surg 4(5):351–357. https://doi.org/10.1136/neurintsurg-2011-010089
Yamamoto H, Yabuta T, Negi Y, Horikawa D, Kawamura K, Tamura E, Tanaka K, Ishida F (2020) Measurement of human blood viscosity a using falling needle rheometer and the correlation to the Modified Herschel-Bulkley model equation. Heliyon 6(9):e04792. https://doi.org/10.1016/j.heliyon.2020.e04792
Yasuda R, Miura Y, Suzuki Y, Tsuji M, Shiba M, Toma N, Suzuki H (2022) Posterior communicating artery-incorporated internal carotid-posterior communicating artery aneurysms prone to recur after coil embolization. World Neurosurg 162:e546e552. https://doi.org/10.1016/j.wneu.2022.03.062
Yuan J, Huang C, Li Z, Jiang X, Zhao X, Lai N, Xia D, Wu D, Zhang B, Wang X, Fang X (2021) Hemodynamic characteristics associated with recurrence of middle cerebral artery bifurcation aneurysms after total embolization. Clin Interv Aging 6(16):2023–2032. https://doi.org/10.2147/CIA.S326635
Yuan J, Huang C, Li Z, Jiang X, Zhao X, Wu D, Lai N, Liu J, Zhang B, Qin F, Xia D, Fang X (2021) Hemodynamic and morphological parameters of ruptured mirror posterior communicating artery aneurysms. Front Neurol 27(12):653589. https://doi.org/10.3389/fneur.2021.653589
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Conceptualization: Katsuhiro Tanaka, Fujimaro Ishida
Data curation: Katsuhiro Tanaka, Kazuhiro Furukawa, Fujimaro Ishida
Formal analysis: Katsuhiro Tanaka, Kazuhiro Furukawa, Fujimaro Ishida
Methodology: Kazuhiro Furukawa, Fujimaro Ishida
Project administration: Katsuhiro Tanaka, Fujimaro Ishida
Software: Kazuhiro Furukawa, Fujimaro Ishida
Supervision: Fujimaro Ishida, Hidenori Suzuki
Validation: Katsuhiro Tanaka, Fujimaro Ishida
Visualization: Katsuhiro Tanaka, Fujimaro Ishida
Writing–original draft: Katsuhiro Tanaka
Writing–review and editing: Katsuhiro Tanaka, Fujimaro Ishida, Hidenori Suzuki
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Tanaka, K., Furukawa, K., Ishida, F. et al. Hemodynamic differences of posterior communicating artery aneurysms between adult and fetal types of posterior cerebral artery. Acta Neurochir 165, 3697–3706 (2023). https://doi.org/10.1007/s00701-023-05840-y
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DOI: https://doi.org/10.1007/s00701-023-05840-y