Quantitative evaluation of the effect of Circle of Willis structures on cerebral hyperperfusion: A multi-scale model analysis

• Autorzy: Huang Suqin , Li Bao , Liu Jincheng , Zhang Liyuan , Sun Hao , Guo Huanmei , Zhang Yanping , Liang Fuyou , Gong Yanjun , Liu Youjun

Identyfikatory

DOI

10.1016/j.bbe.2024.08.005

• Języki publikacji: EN

Abstrakty

EN

Cerebral hyperperfusion occurs in some patients after superficial temporal artery-middle cerebral artery bypass surgery. However, there is uncertainty about cerebral hyperperfusion after bypass for patients with different Circle of Willis (CoW) structures. This study established a lumped-parameter model coupled with one-dimensional model (0-1D), whilst a deep learning model for predicting pressure drop (DLM-PD) caused by stenosis and a cerebral autoregulation model (CAM) were introduced into the model. Based on this model, 9 CoW structural models before and after bypass were constructed, to investigate the effects of different CoW structures on cerebral hyperperfusion after bypass. The model and the results were further validated by clinical data. The MSE of mean flow rates from 0-1D model calculation and from clinical measurement was 1.4%. The patients exhibited hyperperfusion in three CoW structures after bypass: missing right anterior segment of the anterior cerebral artery (mRACA1) (13.96% hyperperfusion); mRACA1 and foetal-type right anterior segment of posterior cerebral artery (12.81%), and missing anterior communicating artery and missing left posterior communicating artery (112.41%). The error between the average flow ratio from the model calculations and from clinical measurements was less than 5%. This study demonstrated that the CoW structure had a significant impact on hyperperfusion after bypass. The general 0-1D model coupled with DLM-PD and CAM proposed in this study, could accurately simulate the hemodynamic environment of different CoW structures before and after bypass, which might help physicians identify high-risk patients with hyperperfusion before surgery, and promote the development of non-invasive diagnosis and treatment of cerebrovascular diseases.

Słowa kluczowe

EN

cerebral artery stenosis; cerebral artery bypass; 0–1D model; circle of Willis; cerebral hyperperfusion; deep learning model

PL

zwężenie tętnicy mózgowej; bajpas tętnicy mózgowej; koło Willisa; uczenie głębokie

• Wydawca: Nałęcz Institute of Biocybernetics and Biomedical Engineering of the Polish Academy of Sciences ; Elsevier
• Czasopismo: Biocybernetics and Biomedical Engineering
• Rocznik: 2024
• Tom: Vol. 44, no. 4
• Strony: 782--793
• Opis fizyczny: Bibliogr. 64 poz., rys., tab.

Twórcy

autor

Huang Suqin

• College of Chemistry and Life Science, Beijing University of Technology, Beijing 100124, China

autor

Li Bao

• College of Chemistry and Life Science, Beijing University of Technology, Beijing 100124, China

autor

Liu Jincheng

• National institute of metrology, Center for Medical Metrology, China

autor

Zhang Liyuan

• College of Chemistry and Life Science, Beijing University of Technology, Beijing 100124, China

autor

Sun Hao

• College of Chemistry and Life Science, Beijing University of Technology, Beijing 100124, China

autor

Guo Huanmei

• College of Chemistry and Life Science, Beijing University of Technology, Beijing 100124, China

autor

Zhang Yanping

• College of Chemistry and Life Science, Beijing University of Technology, Beijing 100124, China

autor

Liang Fuyou

• Department of Engineering Mechanics, School of Naval Architecture, Ocean and Civil Engineering, Shanghai Jiao Tong University, Shanghai 200240, China
• World-Class Research Center “Digital Biodesign and Personalized Healthcare”, Sechenov First Moscow State Medical University, Moscow 19991, Russia

autor

Gong Yanjun

• Department of Cardiology, Peking University First Hospital, Beijing 100034, China

autor

Liu Youjun

• College of Chemistry and Life Science, Beijing University of Technology, Beijing 100124, China

Bibliografia

• [1] Tong X, Yang QH, Ritchey MD, George MG, Jackson SL, Gillespie C, et al. The burden of cerebrovascular disease in the United States. Prev Chronic Dis 2019;16:9.
• [2] Lv B, Song G, Jing F, Li M, Zhou H, Li W, et al. Mortality from cerebrovascular diseases in China: exploration of recent and future trends. Chin Med J (Engl) 2024; 137:588-95.
• [3] Zhang H, Shang J, Li W, Gao D, Zhang J. Increased expression of VCAM1 on brain endothelial cells drives blood-brain barrier impairment following chronic cerebral hypoperfusion. ACS Chem Nerosci 2024.
• [4] Rajeev V, Chai YL, Poh L, Selvaraji S, Fann DY, Jo D-G, et al. Chronic cerebral hypoperfusion: a critical feature in unravelling the etiology of vascular cognitive impairment. Acta Neuropathol Commun 2023;11:93.
• [5] Wu X-B, Liu Y-A, Huang L-X, Guo X, Cai W-Q, Luo B, et al. Hemodynamics combined with inflammatory indicators exploring relationships between ischemic stroke and symptomatic middle cerebral artery atherosclerotic stenosis. Eur J Med Res 2023;28:378.
• [6] Zhang Y, Ya D, Yang J, Jiang Y, Li X, Wang J, et al. EAAT3 impedes oligodendrocyte remyelination in chronic cerebral hypoperfusion-induced white matter injury. CNS Neurosci Ther 2024;30:e14487.
• [7] Saceleanu VM, Toader C, Ples H, Covache-Busuioc R-A, Costin HP, Bratu B-G, et al. Integrative approaches in acute ischemic stroke: from symptom recognition to future innovations. Biomedicines 2023;11:2617.
• [8] Li L, Wang AJ, Wang CH, Zhang HB, Wu DS, Zhuang GL, et al. Superficial temporal artery-middle cerebral artery bypass in combination with encephalo-myosynangiosis in Chinese adult patients with moyamoya disease. Frontiers in Surgery 2023;10:8.
• [9] Aboukais R, Verbraeken B, Leclerc X, Gautier C, Vermandel M, Bricout N, et al. Protective STA-MCA bypass to prevent brain ischemia during high-flow bypass surgery: case series of 10 patients. Acta Neurochir 2019;161:1207-14.
• [10] Shi Z, Wu L, Wang Y, Zhang H, Yang Y, Hang C. Risk factors of postoperative cerebral hyperperfusion syndrome and its relationship with clinical prognosis in adult patients with moyamoya disease. Chinese Neurosurgical J 2023;9:190-8.
• [11] Kochi R, Kanoke A, Tashiro R, Uchida H, Endo H. Waveform analysis of superficial temporal artery-middle cerebral artery bypass graft in revascularization surgery for moyamoya disease. Cerebrovascular Diseases Extra 2024;14:39-45.
• [12] Lee K, Yoo R-E, Cho W-S, Choi SH, Lee SH, Kim KM, et al. Blood-brain barrier disruption imaging in postoperative cerebral hyperperfusion syndrome using DCEMRI. J Cereb Blood Flow Metab 2024;44:345-54.
• [13] Xu M, Yan P, Zhao Y, Wang H, Sun Q, Du Y. Neurosonological parameters may predict the risk of cerebral hyperperfusion syndrome after carotid artery stenting. World Neurosurg 2024.
• [14] Kurisu K, Ito M, Uchino H, Sugiyama T, Fujimura M. Long-term outcomes of combined revascularization surgery for moyamoya disease in the elderly: a single institute experience. Neurol. Med. Chir. 2024:2023-10219.
• [15] Liu Y, Zhu L, Hou B, Wang T, Xu D, Tan C, et al. Study on the correlation between the circle of Willis structure and collateral circulation in bilateral carotid artery occlusion. Neurol Sci 2021;42:5335-42.
• [16] Jones JD, Castanho P, Bazira P, Sanders K. Anatomical variations of the circle of Willis and their prevalence, with a focus on the posterior communicating artery: a literature review and meta-analysis. Clin Anat 2021;34:978-90.
• [17] Enyedi M, Scheau C, Baz RO, Didilescu AC. Circle of Willis: anatomical variations of configuration.A magnetic resonance angiography study.FoliaMorphol.2023;82:24-9.
• [18] Westphal LP, Lohaus N, Winklhofer S, Manzolini C, Held U, Steigmiller K, et al. Circle of Willis variants and their association with outcome in patients with middle cerebral artery-M1-occlusion stroke. Eur J Neurol 2021;28:3682-91.
• [19] Rangus I, Milles LS, Galinovic I, Villringer K, Audebert HJ, Fiebach JB, et al. Reclassifications of ischemic stroke patterns due to variants of the Circle of Willis. Int J Stroke 2022;17:770-6.
• [20] Tao T, Zhu W, Yu J, Li X, Wei W, Hu M, et al. Intraoperative evaluation of local cerebral hemodynamic change by laser speckle contrast imaging for predicting postoperative cerebral hyperperfusion during STA-MCA bypass in adult patients with moyamoya disease. J. Cereb. Blood Flow Metab. 2024 (0271678X241226483).
• [21] Hu M, Yu J, Zhang J, Chen J. Designing a flow-controlled STA-MCA anastomosis based on the Hagen-Poiseuille law for preventing postoperative hyperperfusion in adult moyamoya disease. Therapeutic Adv Chronic Disease 2023;14 (20406223231181492).
• [22] Lengyel B, Magyar-Stang R, Pál H, Debreczeni R, Sándor ÁD, Székely A, et al. Noninvasive tools in perioperative stroke risk assessment for asymptomatic carotid artery stenosis with a focus on the circle of willis. J Clin Med 2024;13:2487.
• [23] Davidson H, Scardino B, Gamage PT, Taebi A. Variations of middle cerebral artery hemodynamics due to aneurysm clipping surgery. J Eng Sci Medical Diagnostics and Therapy 2024;7:011008.
• [24] Coccarelli A, Van Loon R, Chien A. A computational pipeline to investigate longitudinal blood flow changes in the circle of willis of patients with stable and growing aneurysms. Ann Biomed Eng 2024;1-13.
• [25] Müller LO, Watanabe SM, Toro EF, Feijóo RA, Blanco PJ. An anatomically detailed arterial-venous network model. Cerebral and coronary circulation. Front. Physiol. 2023;14:1162391.
• [26] Li RC, Sughimoto K, Zhang XC, Wang SR, Liu H. Impacts of respiratory fluctuations on cerebral circulation: a machine-learning-integrated 0-1D multiscale hemodynamic model. Physiol Meas 2023;44:21.
• [27] McConnell FK, Payne S. The dual role of cerebral autoregulation and collateral flow in the circle of willis after major vessel occlusion. IEEE Trans Biomed Eng 2017;64:1793-802.
• [28] Feng Y, Fu R, Sun H, Wang X, Yang Y, Wen C, et al. Non-invasive fractional flow reserve derived from reduced-order coronary model and machine learning prediction of stenosis flow resistance. Artif Intell Med 2024;147:102744.
• [29] Liang FY, Takagi S, Himeno R, Liu H. Multi-scale modeling of the human cardiovascular system with applications to aortic valvular and arterial stenoses. Med Biol Eng Compu 2009;47:743-55.
• [30] Zhang XC, Haneishi H, Liu H. Impact of ductus arteriosus constriction and restrictive foramen ovale on global hemodynamics for term fetuses with d-TGA. Int J Numerical Methods in Biomedical Eng 2021;37:22.
• [31] Pfaller MR, Pham J, Verma A, Pegolotti L, Wilson NM, Parker DW, et al. Automated generation of 0D and 1D reduced-order models of patient-specific blood flow. Int J Numerical Methods in Biomedical Eng 2022;38:23.
• [32] Sun H, Liu JC, Feng YL, Xi XL, Xu K, Zhang LY, et al. Deep learning-based prediction of coronary artery stenosis resistance. American J Physiology-Heart and Circulatory Physiology 2022;323:H1194-205.
• [33] Sun H, Li B, Liu J, Xi X, Zhang L, Zhang Y, et al. Real-time model-based cerebral perfusion calculation for ischemic stroke. Comput Methods Programs Biomed 2024;243:107916.
• [34] Liang FY, Fukasaku K, Liu H, Takagi S. A computational model study of the influence of the anatomy of the circle of willis on cerebral hyperperfusion following carotid artery surgery. Biomed Eng Online 2011;10:22.
• [35] Kawano H, Yamada S, Watanabe Y, Ii S, Otani T, Ito H, et al. Aging and sex differences in brain volume and cerebral blood flow. Aging Dis 2024;14.
• [36] Takahashi T, Uwano I, Akamatsu Y, Chida K, Kobayashi M, Yoshida K, et al. Prediction of cerebral hyperperfusion following carotid endarterectomy using intravoxel incoherent motion magnetic resonance imaging. J Stroke Cerebrovasc Dis 2023;32:9.
• [37] Li N, Zhou F, Lu X, Chen H, Liu R, Chen S, et al. Impaired dynamic cerebral autoregulation as a predictor for cerebral hyperperfusion after carotid endarterectomy: a prospective observational study. World Neurosurg 2024;181:e312-21.
• [38] Tanaka H, Fujita N, Enoki T, Matsumoto K, Watanabe Y, Murase K, et al. Relationship between variations in the circle of Willis and flow rates in internal carotid and basilar arteries determined by means of magnetic resonance imaging with semiautomated lumen segmentation: reference data from 125 healthy volunteers. Am J Neuroradiol 2006;27:1770-5.
• [39] Zhang J, Yu J, Xin C, Fujimura M, Lau TY, Hu M, et al. A flow self-regulating superficial temporal artery-middle cerebral artery bypass based on side-to-side anastomosis for adult patients with moyamoya disease. J Neurosurg 2023;138:1347-56.
• [40] Alharbi Y. A 3D-0D computational model of the left ventricle for investigating blood flow patterns for cases of systolic anterior motion and after anterior mitral leaflet splitting. Appl Sci 2024;14:466.
• [41] Sun H, Li B, Zhang L, Zhang Y, Liu J, Huang S, et al. Numerical study of hemodynamic changes in the Circle of Willis after stenosis of the internal carotid artery. Comput Methods Programs Biomed 2024;243:107881.
• [42] Li J, Li D, Alaraj A, Du X, Wang K, Charbel FT. A patient-specific circle of Willis blood flow model in predicting outcomes of balloon test occlusion. J Neuroimaging 2024.
• [43] Luisi CA, Witter TL, Nikoubashman O, Wiesmann M, Steinseifer U, Neidlin M. Evaluating the accuracy of cerebrovascular computational fluid dynamics modeling through time-resolved experimental validation. Sci Rep 2024;14:8194.
• [44] Pradhan AM, Mut F, Cebral JR. A one-dimensional computational model for blood flow in an elastic blood vessel with a rigid catheter. Int J Numerical Methods in Biomedical Eng 2024:e3834.
• [45] Kizhisseri M, Gharaie S, Schluter J. An analytical method informed by clinical imaging data for estimating outlet boundary conditions in computational fluid dynamics analysis of carotid artery blood flow. Sci Rep 2023;13:14973.
• [46] Yan Q, Xiao DQ, Jia YS, Ai DN, Fan JF, Song H, et al. A multi-dimensional CFD framework for fast patient-specific fractional flow reserve prediction. Comput Biol Med 2024;168:12.
• [47] Zhang Y, He S, Jiang X, Fang H, Wang Z, Cao J, et al. Performance evaluation on full-scale proton exchange membrane fuel cell: Mutual validation of one-dimensional, three-dimensional and experimental investigations. Energ Conver Manage 2024;299:117905.
• [48] Lei X, Pan F, Liu H, He P, Zheng D, Feng J. An end-to-end deep learning framework for accurate estimation of intracranial pressure waveform characteristics. Eng Appl Artif Intel 2024;130:107686.
• [49] Beqiri E, García-Orellana M, Politi A, Zeiler FA, Placek MM, Fàbregas N, et al. Cerebral autoregulation derived blood pressure targets in elective neurosurgery. J Clin Monit Comput 2024;1-14.
• [50] Li B, Liu YJ, Liu JC, Sun H, Feng YL, Zhang Z, et al. Cerebral multi-autoregulation model based enhanced external counterpulsation treatment planning for cerebral ischemic stroke. J Cereb Blood Flow Metab 2023;43:1764-78.
• [51] Zhang JJ, Li SR, Fujimura M, Lau TY, Wu XL, Hu MA, et al. Hemodynamic analysis of the recipient parasylvian cortical arteries for predicting postoperative hyperperfusion during STA-MCA bypass in adult patients with moyamoya disease. J Neurosurg 2021;134:17-24.
• [52] Gyöngyösi Z, Belán I, Nagy E, Fülesdi Z, Farkas O, Végh T, et al. Incomplete circle of Willis as a risk factor for intraoperative ischemic events during carotid endarterectomies performed under regional anesthesia - a prospective case-series. Transl Neurosci 2023;14:20220293.
• [53] Sebök M, Höbner LM, Fierstra J, Schubert T, Wegener S, Kulcsár Z, et al. Flow-augmentation STA-MCA bypass for acute and subacute ischemic stroke due to internal carotid artery occlusion and the role of advanced neuroimaging with hemodynamic and flow-measurement in the decision-making: preliminary data. Quant Imaging Med Surg 2024;14:777.
• [54] Manjunath N, Dhanakshirur RR, Joshi S, Reddy NG, Raheja A, Devrajan Sebastian LJ, et al. Novel method of calculation of magnetic resonance imaging perfusion and comparison of single versus double barrel superficial temporal artery-middle cerebral artery bypass for revascularisation in moya moya disease. World Neurosurg 2024;181:e516-23.
• [55] Wang H, Shen L, Zhao C, Liu S, Wu G, Wang H, et al. The incomplete circle of Willis is associated with vulnerable intracranial plaque features and acute ischemic stroke. J Cardiovasc Magn Reson 2023;25:23.
• [56] de Athayde SR, Ferreira ZMCC, Portela MVV, Valentim M, Matielo MF, Nakamura ET, et al. The importance of the circle of willis in carotid interventions outcomes: a real-life study. Ann Vasc Surg 2024;101:127-33.
• [57] Gao F, Cong J, Duan Y, Zhao W, Zhu Z, Zheng Y, et al. Screening of postoperative cerebral hyperperfusion syndrome in moyamoya disease: a three-dimensional pulsed arterial-spin labeling magnetic resonance imaging approach. Front Neurosci 2023;17:1274038.
• [58] Banga PV, Varga A, Csobay-Novák C, Kolossváry M, Szántó E, Oderich GS, et al. Incomplete circle of Willis is associated with a higher incidence of neurologic events during carotid eversion endarterectomy withut shunting.JVascSurg2018;68:1764-71.
• [59] Lin E, Kamel H, Gupta A, RoyChoudhury A, Girgis P, Glodzik L. Incomplete circle of Willis variants and stroke outcome. Eur J Radiol 2022;153:110383.
• [60] Fan W, Shi W, Guo W, Zhang Y, Tan J, Yu B. Independent role of circle of Willis for peri-procedural evaluation of carotid endarterectomy in patients with severe carotid stenosis. Clin Neurol Neurosurg 2022;213:107102.
• [61] Ujiie H, Chiba R, Yamaguchi A, Nomura S, Shiiya H, Fujiwara-Kuroda A, et al. Developing a virtual reality simulation system for preoperative planning of robotic-assisted thoracic surgery. J Clin Med 2024;13:611.
• [62] Bellouche Y, Abdelli S, Hannachi S, Benic C, Nicol P-P, Le Ven F, et al. Hemodynamics of proximal coronary lesions in patient undergoing aortic valve replacement: patient-specific in silico study. Arch Cardiovasc Dis 2024;117:S64-5.
• [63] Zhang B, Chen X, Zhang X, Ding G, Ge L, Wang S. Computational modeling and simulation for endovascular embolization of cerebral arteriovenous malformations with liquid embolic agents. Acta Mechanica Sinica 2023;40:623042.
• [64] Rundfeldt HC, Lee CM, Lee H, Jung K-H, Chang H, Kim HJ. Cerebral perfusion simulation using realistically generated synthetic trees for healthy and stroke patients. Comput Methods Programs Biomed 2024;244:107956.

Uwagi

Opracowanie rekordu ze środków MNiSW, umowa nr POPUL/SP/0154/2024/02 w ramach programu "Społeczna odpowiedzialność nauki II" - moduł: Popularyzacja nauki (2025).