The Role of Circle of Willis Anatomy Variations in Cardio-embolic Stroke: A Patient-Specific Simulation Based Study
We describe a patient-specific simulation based investigation on the role of Circle of Willis anatomy in cardioembolic stroke. Our simulation framework consists of medical image-driven modeling of patient anatomy including the Circle, 3D blood flow simulation through patient vasculature, embolus transport modeling using a discrete particle dynamics technique, and a sampling based approach to incorporate parametric variations. A total of 24 (four patients and six Circle anatomies including the complete Circle) models were considered, with cardiogenic emboli of varying sizes and compositions released virtually and tracked to compute distribution to the brain. The results establish that Circle anatomical variations significantly influence embolus distribution to the six major cerebral arteries. Embolus distribution to MCA territory is found to be least sensitive to the influence of anatomical variations. For varying Circle topologies, differences in flow through cervical vasculature are observed. This incoming flow is recruited differently across the communicating arteries of the Circle for varying anastomoses. Emboli interact with the routed flow, and can undergo significant traversal across the Circle arterial segments, depending upon their inertia and density ratio with respect to blood. This interaction drives the underlying biomechanics of embolus transport across the Circle, explaining how Circle anatomy influences embolism risk.
KeywordsStroke Embolus Hemodynamics Circle of Willis Fluid–particle interaction
This work was supported by the American Heart Association Award: 13GRNT17070095. This research used the Savio computational cluster resource provided by the Berkeley Research Computing program at the University of California, Berkeley. NDJ acknowledges support from the Regent’s and Chancellor’s Research Fellowship at U.C. Berkeley. DM, NDJ, and SCS conceptualized the design of the study. DM developed the computational framework, performed the embolus dynamics, performed all statistical and data analysis, drafted the manuscript. NDJ devised the image-based modeling framework, computed all flow simulations, and contributed to embolus dynamics simulations. JN helped with data analysis, and contributed clinical and diagnostic connections to the simulation data. NDJ, SCS, and JN reviewed and edited the manuscript draft. Final manuscript version was in agreement with all Authors.
Conflict of interest
There are no conflicts of interest.
Electronic supplementary material 2 (MP4 28204 kb)
- 12.Gallo, D., Vardoulis, O., Monney, P., Piccini, D., Antiochos, P., Schwitter, J., Stergiopoulos, N., and Morbiducci, U. Cardiovascular morphometry with high-resolution 3D magnetic resonance: First application to left ventricle diastolic dysfunction. Med. Eng. Phys. 47:64–71, 2017.CrossRefPubMedGoogle Scholar
- 15.Hart, R.G., H.C. Diener, S.B. Coutts, J.D. Easton, C.B. Granger, M.J. O’Donnell, R.L. Sacco, S.J. Connolly, Cryptogenic Stroke/ESUS International Working Group, et al. Embolic strokes of undetermined source: the case for a new clinical construct. Lancet Neurol. 13(4):429–438, 2014.CrossRefGoogle Scholar
- 27.Krishnaswamy, A., J.P. Klein, and S.R. Kapadia. Clinical cerebrovascular anatomy. Catheter. Cardio. Intervent. 75(4):530–539, 2010.Google Scholar
- 28.Les, A.S., S.C. Shadden, C.A. Figueroa, J.M. Park, M.M. Tedesco, R.J. Herfkens, R.L. Dalman, and C.A. Taylor. Quantification of hemodynamics in abdominal aortic aneurysms during rest and exercise using magnetic resonance imaging and computational fluid dynamics. Ann. Biomed. Eng. 38(4):1288–1313, 2010.CrossRefPubMedGoogle Scholar
- 32.Marosfoi, M.G., N. Korin, M.J. Gounis, O. Uzun, S. Vedantham, E.T. Langan, A.L. Papa, O.W. Brooks, C. Johnson, A.S. Puri, et al. Shear-activated nanoparticle aggregates combined with temporary endovascular bypass to treat large vessel occlusion. Stroke 46(12):3507–3513, 2015.CrossRefPubMedGoogle Scholar
- 42.Smith, W.S., M.H. Lev, J.D. English, E.C. Camargo, M. Chou, S.C. Johnston, G. Gonzalez, P.W. Schaefer, W.P. Dillon, W.J. Koroshetz, and K.L. Furie. Significance of large vessel intracranial occlusion causing acute ischemic stroke and TIA. Stroke 40(12):3834–3840, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
- 45.Tanaka, H., N. Fujita, T. Enoki, K. Matsumoto, Y. Watanabe, K. Murase, and H. Nakamura. 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. 27(8):1770–1775, 2006.PubMedGoogle Scholar
- 48.Updegrove, A., N.M. Wilson, J. Merkow, H. Lan, A.L. Marsden, and S.C. Shadden. SimVascular: an open source pipeline for cardiovascular simulation. Ann. Biomed. Eng.:1–17, 2016.Google Scholar
- 49.Van Seeters, T., J. Hendrikse, G.J. Biessels, B.K. Velthuis, W.P.T.M. Mali, L.J. Kappelle, Y. van der Graaf, SMART Study Group, et al. Completeness of the circle of Willis and risk of ischemic stroke in patients without cerebrovascular disease. Neuroradiology 57(12):1247–1251, 2015.CrossRefPubMedPubMedCentralGoogle Scholar