Understanding the Role of Hemodynamics in the Initiation, Progression, Rupture, and Treatment Outcome of Cerebral Aneurysm from Medical Image-Based Computational Studies
About a decade ago, the first image-based computational hemodynamic studies of cerebral aneurysms were presented. Their potential for clinical applications was the result of a right combination of medical image processing, vascular reconstruction, and grid generation techniques used to reconstruct personalized domains for computational fluid and solid dynamics solvers and data analysis and visualization techniques. A considerable number of studies have captivated the attention of clinicians, neurosurgeons, and neuroradiologists, who realized the ability of those tools to help in understanding the role played by hemodynamics in the natural history and management of intracranial aneurysms. This paper intends to summarize the most relevant results in the field reported during the last years. 1. Introduction Stroke is the leading cause of long-term disability and the third cause of death in the Western World. Subarachnoid hemorrhage (SAH) is one of the most severe types of stroke, which usually occurs when an intracranial aneurysm ruptures [1]. SAH refers to a leakage of blood into the subarachnoid spaces, which is a continuous space between the supratentorial and infratentorial compartments. A greater concentration of the blood products around the site of bleed is usual. When hemorrhage extends into the adjacent parenchymal structures and ventricular system, it results in a higher morbidity and mortality rate [2]. Vasospasm, in which blood vessels constrict to restrict blood flow, is a serious consequence of SAH because it may cause ischemic brain injury and permanent brain damage due to lack of oxygen in parts of the brain [3]. Understanding of the underlying mechanisms that result in injury after SAH is limited. However, a number of studies indicate that apoptosis may play a major role in the pathogenesis of secondary brain injury after SAH [4]. Elevated intracranial pressure is an important consequence of aneurysmal SAH that often results in not only decreased cerebral perfusion but also secondary clinical decline [5]. Intracranial aneurysms tend to initiate at or near arterial bifurcations, mostly in the circle of Willis. The yearly risk of subarachnoid hemorrhage for an unruptured intracranial aneurysm is approximately 1% for lesions 7 to 10？mm in diameter. The optimal management of unruptured aneurysms is controversial, and current decision making is mainly based on aneurysm size and location, as derived from the International Study of Unruptured Intracranial Aneurysms (ISUIA) [6]. Current guidelines suggest that, with rare exceptions, all
References
[1]
S. Hwang, K. Kim, and T. Nam, “A pseudoaneurysm appeared after rebleeding,” Journal of Korean Neurosurgical Society, vol. 41, pp. 134–136, 2007.
[2]
P. J. Kirkpatrick, “Subarachnoid haemorrhage and intracranial aneurysms: what neurologists need to know,” Neurology in Practice, vol. 73, no. 1, pp. 28–33, 2002.
[3]
G. J. Velat, M. M. Kimball, J. D. Mocco, and B. L. Hoh, “Vasospasm after aneurysmal subarachnoid hemorrhage: review of randomized controlled trials and meta-analyses in the literature,” World Neurosurgery, vol. 76, no. 5, pp. 446–454, 2011.
[4]
W. J. Cahill, J. H. Calvert, and J. H. Zhang, “Mechanisms of early brain injury after subarachnoid hemorrhage,” Journal of Cerebral Blood Flow and Metabolism, vol. 26, no. 11, pp. 1341–1353, 2006.
[5]
W. J. Mack, R. G. King, A. F. Ducruet et al., “Intracranial pressure following aneurysmal subarachnoid hemorrhage: monitoring practices and outcome data,” Neurosurgical Focus, vol. 14, no. 4, p. e3, 2003.
[6]
D. O. Wiebers, “Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment,” Lancet, vol. 362, no. 9378, pp. 103–110, 2003.
[7]
R. J. Komotar, J. Mocco, and R. A. Solomon, “Guidelines for the surgical treatment of unruptured intracranial aneurysms: the first annual J. Lawrence pool memorial research symposium—controversies in the management of cerebral aneurysms,” Neurosurgery, vol. 62, no. 1, pp. 183–193, 2008.
[8]
W. E. Stehbens, “Pathology and pathogenesis of intracranial berry aneurysms,” Neurological Research, vol. 12, no. 1, pp. 29–34, 1990.
[9]
H. M. Finlay, P. Whittaker, and P. B. Canham, “Collagen organization in the branching region of human brain arteries,” Stroke, vol. 29, no. 8, pp. 1595–1601, 1998.
[10]
S. Inci and R. F. Spetzler, “Intracranial aneurysms and arterial hypertension: a review and hypothesis,” Surgical Neurology, vol. 53, no. 6, pp. 530–542, 2000.
[11]
W. E. Stehbens, “Etiology of intracranial berry aneurysms,” Journal of Neurosurgery, vol. 70, no. 6, pp. 823–831, 1989.
[12]
M. R. Crompton, “Mechanism of growth and rupture in cerebral berry aneurysms,” British Medical Journal, vol. 5496, pp. 1138–1142, 1966.
[13]
H. Nakatani, N. Hashimoto, Y. Kang et al., “Cerebral blood flow patterns at major vessel bifurcations and aneurysms in rats,” Journal of Neurosurgery, vol. 74, no. 2, pp. 258–262, 1991.
[14]
D. M. Sforza, C. M. Putman, and J. R. Cebral, “Hemodynamics of cerebral aneurysms,” Annual Review of Fluid Mechanics, vol. 41, pp. 91–107, 2009.
[15]
J. R. Cebral, M. A. Castro, J. E. Burgess, R. S. Pergolizzi, M. J. Sheridan, and C. M. Putman, “Characterization of cerebral aneurysms for assessing risk of rupture by using patient-specific computational hemodynamics models,” American Journal of Neuroradiology, vol. 26, no. 10, pp. 2550–2559, 2005.
[16]
M. A. Castro, C. M. Putman, M. J. Sheridan, and J. R. Cebral, “Hemodynamic patterns of anterior communicating artery aneurysms: a possible association with rupture,” American Journal of Neuroradiology, vol. 30, no. 2, pp. 297–302, 2009.
[17]
M. Castro, C. Putman, A. Radaelli, A. Frangi, and J. Cebral, “Hemodynamics and rupture of terminal cerebral aneurysms,” Academic Radiology, vol. 16, no. 10, pp. 1201–1207, 2009.
[18]
J. R. Cebral, M. Sheridan, and C. M. Putman, “Hemodynamics and bleb formation in intracranial aneurysms,” American Journal of Neuroradiology, vol. 31, no. 2, pp. 304–310, 2010.
[19]
M. Shojima, M. Oshima, K. Takagi et al., “Magnitude and role of wall shear stress on cerebral aneurysm: computational fluid dynamic study of 20 middle cerebral artery aneurysms,” Stroke, vol. 35, no. 11, pp. 2500–2505, 2004.
[20]
K. Fukazawa, F. Ishida, Y. Umeda et al., “Using computational fluid dynamics analysis to characterize local hemodynamic features of middle cerebral artery aneurysm rupture points,” World Neurosurgery, 2013.
[21]
M. Shojima, S. Nemoto, A. Morita, M. Oshima, E. Watanabe, and N. Saito, “Role of shear stress in the blister formation of cerebral aneurysms,” Neurosurgery, vol. 67, no. 5, pp. 1268–1274, 2010.
[22]
M. A. Castro, C. M. Putman, and J. R. Cebral, “Computational analysis of anterior communicating artery aneurysm shear stress before and after aneurysm formation,” Journal of Physics, vol. 332, no. 1, Article ID 012001, 2011.
[23]
Z. Kulcsár, á. Ugron, M. Marosfoi, Z. Berentei, G. Paál, and I. Szikora, “Hemodynamics of cerebral aneurysm initiation: the role of wall shear stress and spatial wall shear stress gradient,” American Journal of Neuroradiology, vol. 32, no. 3, pp. 587–594, 2011.
[24]
C. A. Taylor and J. D. Humphrey, “Open problems in computational vascular biomechanics: hemodynamics and arterial wall mechanics,” Computer Methods in Applied Mechanics and Engineering, vol. 198, no. 45-46, pp. 3514–3523, 2009.
[25]
G. M. Morales, I. Larrabide, A. J. Geers et al., “A virtual coiling technique for image-based aneurysm models by dynamic path planning,” IEEE Transactions on Medical Imaging, vol. 32, no. 1, pp. 119–129, 2013.
[26]
S.-H. Park, C.-Y. Lee, and M.-B. Yim, “The merits of endovascular coil surgery for patients with unruptured intracranial aneurysms,” Journal of Korean Neurosurgical Society, vol. 43, no. 6, pp. 270–274, 2008.
[27]
J. K. A. Hope, J. V. Byrne, and A. J. Molyneux, “Factors influencing successful angiographic occlusion of aneurysms treated by coil embolization,” American Journal of Neuroradiology, vol. 20, no. 3, pp. 391–399, 1999.
[28]
J. Raymond, T. Darsaut, I. Salazkin, G. Gevry, and F. Bouzeghrane, “Mechanisms of occlusion and recanalization in canine carotid bifurcation aneurysms embolized with platinum coils: an alternative concept,” American Journal of Neuroradiology, vol. 29, no. 4, pp. 745–752, 2008.
[29]
J. L. Brisman, J. K. Song, and D. W. Newell, “Cerebral aneurysms,” New England Journal of Medicine, vol. 355, no. 9, pp. 928–939, 2006.
[30]
M. T. Bhatti, K. R. Peters, C. Firment, and R. A. Mericle, “Delayed exacerbation of third nerve palsy due to aneurysmal regrowth after endovascular coil embolization,” Journal of Neuro-Ophthalmology, vol. 24, no. 1, pp. 3–10, 2004.
[31]
M. Piotin, L. Spelle, C. Mounayer et al., “Intracranial aneurysms: treatment with bare platinum coils—aneurysm packing, complex coils, and angiographic recurrence,” Radiology, vol. 243, no. 2, pp. 500–508, 2007.
[32]
J. Raymond, F. Guilbert, A. Weill et al., “Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils,” Stroke, vol. 34, no. 6, pp. 1398–1403, 2003.
[33]
M. Piotin, L. Spelle, C. Mounayer, C. Loureiros, A. Ghorbani, and J. Moret, “Intracranial aneurysms coiling with matrix: immediate results in 152 patients and midterm anatomic follow-up from 115 patients,” Stroke, vol. 40, no. 1, pp. 321–323, 2009.
[34]
P. Mitchell, R. Kerr, A. D. Mendelow, and A. Molyneux, “Could late rebleeding overturn the superiority of cranial aneurysm coil embolization over clip ligation seen in the International Subarachnoid Aneurysm Trial?” Journal of Neurosurgery, vol. 108, no. 3, pp. 437–442, 2008.
[35]
J. R. Cebral, F. M. F. Mut, M. R. M. Raschi et al., “Aneurysm rupture following treatment with flow-diverting stents: computational hemodynamics analysis of treatment,” American Journal of Neuroradiology, vol. 32, no. 1, pp. 27–33, 2011.
[36]
A. G. Radaelli, L. Augsburger, J. R. Cebral et al., “Reproducibility of haemodynamical simulations in a subject-specific stented aneurysm model—a report on the Virtual Intracranial Stenting Challenge 2007,” Journal of Biomechanics, vol. 41, no. 10, pp. 2069–2081, 2008.
[37]
J. Y. Ahn, I. B. Han, T. G. Kim et al., “Endovascular treatment of intracranial vertebral artery dissections with stent placement or stent-assisted coiling,” American Journal of Neuroradiology, vol. 27, no. 7, pp. 1514–1520, 2006.
[38]
G. Benndorf, U. Herbon, W. P. Sollmann, and A. Campi, “Treatment of a ruptured dissecting vertebral artery aneurysm with double stent placement: case report,” American Journal of Neuroradiology, vol. 22, no. 10, pp. 1844–1848, 2001.
[39]
R. Vanninen, H. Manninen, and A. Ronkainen, “Broad-based intracranial aneurysms: thrombosis induced by stent placement,” American Journal of Neuroradiology, vol. 24, no. 2, pp. 263–266, 2003.
[40]
M. A. Zenteno, L. M. Murillo-Bonilla, G. Guinto et al., “Sole stenting bypass for the treatment of vertebral artery aneurysms: technical case report,” Neurosurgery, vol. 57, no. 1, 2005.
[41]
P. K. Nelson, P. Lylyk, I. Szikora, S. G. Wetzel, I. Wanke, and D. Fiorella, “The pipeline embolization device for the intracranial treatment of aneurysms trial,” American Journal of Neuroradiology, vol. 32, no. 1, pp. 34–40, 2011.
[42]
G. Espinosa, L. Dzieciuchowicz, and L. Grochowicz, “Endovascular treatment of carotid stenosis associated with incidental intracranial aneurysm,” Annals of Vascular Surgery, vol. 23, no. 5, pp. 688-e1–688-e5, 2009.
[43]
L. J. Kappelle, M. Eliasziw, A. J. Fox, and H. J. M. Barnett, “Small, unruptured intracranial aneurysms and management of symptomatic carotid artery stenosis,” Neurology, vol. 55, no. 2, pp. 307–309, 2000.
[44]
G. Pappadà, “Incidence of asymptomatic berry aneurysms among patients undergoing carotid endarterectomy,” Journal of Neurosurgical Sciences, vol. 41, no. 3, pp. 257–262, 1997.
[45]
P. A. Rouleau, J. Huston III, J. Gilbertson, R. D. Brown Jr., F. B. Meyer, and T. C. Bower, “Carotid artery tandem lesions: frequency of angiographic detection and consequences for endarterectomy,” American Journal of Neuroradiology, vol. 20, no. 4, pp. 621–625, 1999.
[46]
H. P. Adams Jr., “Carotid stenosis and coexisting ipsilateral intracranial aneurysm. A problem in management,” Archives of Neurology, vol. 34, no. 8, pp. 515–516, 1977.
[47]
S. D. Navaneethan, V. S. Kannan, A. Osowo, R. Shrivastava, and S. Singh, “Concomitant intracranial aneurysm and carotid artery stenosis: a therapeutic dilemma,” Southern Medical Journal, vol. 99, no. 7, pp. 757–758, 2006.
[48]
L.-D. Jou, H. M. Shaltoni, H. Morsi, and M. E. Mawad, “Hemodynamic relationship between intracranial aneurysm and carotid stenosis: review of clinical cases and numerical analyses,” Neurological Research, vol. 32, no. 10, pp. 1083–1089, 2010.
[49]
M. A. Castro, N. L. Peloc, C. M. Putman, and J. R. Cebral, “Changes in cerebral aneurysm hemodynamics after virtual endarterectomy,” Mecánica Computacional, vol. 31, pp. 3797–3809, 2012.
[50]
C. A. Taylor, T. J. R. Hughes, and C. K. Zarins, “Finite element modeling of blood flow in arteries,” Computer Methods in Applied Mechanics and Engineering, vol. 158, no. 1-2, pp. 155–196, 1998.
[51]
J. S. Milner, J. A. Moore, B. K. Rutt, and D. A. Steinman, “Hemodynamics of human carotid artery bifurcations: computational studies with models reconstructed from magnetic resonance imaging of normal subjects,” Journal of Vascular Surgery, vol. 28, no. 1, pp. 143–156, 1998.
[52]
J. R. Cebral, M. A. Castro, O. Soto, R. L？hner, and N. Alperin, “Blood-flow models of the circle of Willis from magnetic resonance data,” Journal of Engineering Mathematics, vol. 47, no. 3-4, pp. 369–386, 2003.
[53]
D. A. Steinman, J. S. Milner, C. J. Norley, S. P. Lownie, and D. W. Holdsworth, “Image-based computational simulation of flow dynamics in a giant intracranial aneurysm,” American Journal of Neuroradiology, vol. 24, no. 4, pp. 559–566, 2003.
[54]
D. A. Steinman and C. A. Taylor, “Flow imaging and computing: large artery hemodynamics,” Annals of Biomedical Engineering, vol. 33, no. 12, pp. 1704–1709, 2005.
[55]
Q. Sun, A. Groth, M. Bertram et al., “Phantom-based experimental validation of computational fluid dynamics simulations on cerebral aneurysms,” Medical Physics, vol. 37, no. 9, pp. 5054–5065, 2010.
[56]
C. Karmonik, R. Klucznik, and C. Benndorf, “Blood flow in cerebral aneurysms: comparison of phase contrast magnetic resonance and computational fluid dynamics—preliminary experience,” RoFo Fortschritte auf dem Gebiet der Rontgenstrahlen und der Bildgebenden Verfahren, vol. 180, no. 3, pp. 209–215, 2008.
[57]
C. Karmonik, R. Klucznik, and G. Benndorf, “Comparison of velocity patterns in an AComA aneurysm measured with 2D phase contrast MRI and simulated with CFD,” Technology and Health Care, vol. 16, no. 2, pp. 119–128, 2008.
[58]
M. A. Castro, C. M. Putman, and J. R. Cebral, Computational Hemodynamics of Cerebral Aneurysms: Assessing the Risk of Rupture from Hemodynamic Patterns, VDM, Saarbrücken, Germany, 2008.
[59]
J. R. Cebral, C. M. Putman, M. T. Alley, T. Hope, R. Bammer, and F. Calamante, “Hemodynamics in normal cerebral arteries: qualitative comparison of 4D phase-contrast magnetic resonance and image-based computational fluid dynamics,” Journal of Engineering Mathematics, vol. 64, no. 4, pp. 367–378, 2009.
[60]
J. R. Cebral, R. S. Pergolizzi Jr., and C. M. Putman, “Computational fluid dynamics modeling of intracranial aneurysms: qualitative comparison with cerebral angiography,” Academic Radiology, vol. 14, no. 7, pp. 804–813, 2007.
[61]
P. van Ooij, A. Guédon, C. Poelma et al., “Complex flow patterns in a real-size intracranial aneurysm phantom: phase contrast MRI compared with particle image velocimetry and computational fluid dynamics,” NMR in Biomedicine, vol. 25, no. 1, pp. 14–26, 2012.
[62]
M. D. Ford, H. N. Nikolov, J. S. Milner et al., “PIV-measured versus CFD-predicted flow dynamics in anatomically realistic cerebral aneurysm models,” Journal of Biomechanical Engineering, vol. 130, no. 2, Article ID 021015, 9 pages, 2008.
[63]
J. R. Cebral, M. A. Castro, S. Appanaboyina, C. M. Putman, D. Millan, and A. F. Frangi, “Efficient pipeline for image-based patient-specific analysis of cerebral aneurysm hemodynamics: technique and sensitivity,” IEEE Transactions on Medical Imaging, vol. 24, no. 4, pp. 457–467, 2005.
[64]
A. J. Geers, I. Larrabide, A. G. Radaelli et al., “Patient-specific computational hemodynamics of intracranial aneurysms from 3D rotational angiography and CT angiography: an in vivo reproducibility study,” American Journal of Neuroradiology, vol. 32, no. 3, pp. 581–586, 2011.
[65]
L. Augsburger, P. Reymond, R. Ouared et al., “Influence of segmentation on morphological parameters and computed hemodynamics in cerebral aneurysms,” Journal of Biorheology, vol. 26, no. 1-2, pp. 44–57.
[66]
J. Jiang and C. Strother, “Computational fluid dynamics simulations of intracranial aneurysms at varying heart rates: a “patient-specific” study,” Journal of Biomechanical Engineering, vol. 131, no. 9, Article ID 91001, 11 pages, 2009.
[67]
A. Marzo, P. Singh, I. Larrabide et al., “Computational hemodynamics in cerebral aneurysms: the effects of modeled versus measured boundary conditions,” Annals of Biomedical Engineering, vol. 39, no. 2, pp. 884–896, 2011.
[68]
C. Karmonik, C. Yen, O. Diaz, R. Klucznik, R. G. Grossman, and G. Benndorf, “Temporal variations of wall shear stress parameters in intracranial aneurysms—importance of patient-specific inflow waveforms for CFD calculations,” Acta Neurochirurgica, vol. 152, no. 8, pp. 1391–1398, 2010.
[69]
C. Fisher and J. S. Rossmann, “Effect of non-Newtonian behavior on hemodynamics of cerebral aneurysms,” Journal of Biomechanical Engineering, vol. 131, no. 9, Article ID 91004, 9 pages, 2009.
[70]
L.-D. Jou and M. E. Mawad, “Timing and size of flow impingement in a giant intracranial aneurysm at the internal carotid artery,” Medical and Biological Engineering and Computing, vol. 49, no. 8, pp. 891–899, 2011.
[71]
K. M. Khanafer, P. Gadhoke, R. Berguer, and J. L. Bull, “Modeling pulsatile flow in aortic aneurysms: effect of non-Newtonian properties of blood,” Biorheology, vol. 43, no. 5, pp. 661–679, 2006.
[72]
V. L. Rayz, L. Boussel, M. T. Lawton et al., “Numerical modeling of the flow in intracranial aneurysms: prediction of regions prone to thrombus formation,” Annals of Biomedical Engineering, vol. 36, no. 11, pp. 1793–1804, 2008.
[73]
J. Xiang, M. Tremmel, J. Kolega, E. Levy, S. Natarajan, and H. Meng, “Newtonian viscosity model could overestimate wall shear stress in intracranial aneurysm domes and underestimated rupture risk,” Journal of NeuroInterventional Surgery, vol. 4, no. 5, pp. 351–357, 2011.
[74]
M. A. Castro, M. C. Ahumada Olivares, C. M. Putman, and J. R. Cebral, “Effects of Casson rheology on aneurysm wall shear stress,” Mecánica Computacional, vol. 31, pp. 3789–3796, 2012.
[75]
A. A. Valencia, A. M. Guzmán, E. A. Finol, and C. H. Amon, “Blood flow dynamics in saccular aneurysm models of the basilar artery,” Journal of Biomechanical Engineering, vol. 128, no. 4, pp. 516–526, 2006.
[76]
A. Valencia, J. Munizaga, R. Rivera, and E. Bravo, “Numerical investigation of the hemodynamics in anatomically realistic lateral cerebral aneurysms,” in Proceedings of the 32nd Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC '10), pp. 2616–2621, Buenos Aires, Argentina, September 2010.
[77]
V. Yaghmai, M. Rohany, A. Shaibani et al., “Pulsatility imaging of saccular aneurysm model by 64-slice ct with dynamic multiscan technique,” Journal of Vascular and Interventional Radiology, vol. 18, no. 6, pp. 785–788, 2007.
[78]
H. G. Boecher-Schwarz, K. Ringel, L. Kopacz, A. Heimann, and O. Kempski, “Ex vivo study of the physical effect of coils on pressure and flow dynamics in experimental aneurysms,” American Journal of Neuroradiology, vol. 21, no. 8, pp. 1532–1536, 2000.
[79]
J. Ueno, T. Matsuo, K. Sugiyama, and R. Okeda, “Mechanism underlying the prevention of aneurismal rupture by coil embolization,” Journal of Medical and Dental Sciences, vol. 49, no. 4, pp. 135–141, 2002.
[80]
C. Zhang, M. C. Villa Uriol, M. De Craene, J. M. Pozo, and A. F. Frangi, “Time-resolved 3D rotational angiography reconstruction: towards cerebral aneurysm pulsatile analysis,” The International Journal for Computer Assisted Radiology and Surgery, vol. 3, pp. S44–46, 2008.
[81]
L. Dempere-Marco, E. Oubel, M. Castro, C. Putman, A. Frangi, and J. Cebral, “Estimation of wall motion in intracranial aneurysms and its effects on hemodynamic patterns,” Lecture Notes in Computer Science, vol. 4191, pp. 438–445, 2006.
[82]
E. Oubel, J. R. Cebral, M. De Craene et al., “Wall motion estimation in intracranial aneurysms,” Physiological Measurement, vol. 31, no. 9, pp. 1119–1135, 2010.
[83]
M. A. Castro, M. C. Ahumada Olivares, C. M. Putman, and J. R. Cebral, “Intracranial aneurysm wall motion and wall shear stress from 4D computerized tomographic angiography images,” in Biomedical Applications in Molecular, Structural, and Functional Imaging, vol. 8672 of Proceedings of SPIE, Orlando, Fla, USA.
[84]
A. Firouzian, R. Manniesing, C. T. Metz et al., “Quantification of intracranial aneurysm morphodynamics from ECG-gated CT angiography,” Academic Radiology, vol. 20, pp. 52–58, 2013.
[85]
J. D. Humphrey, “Coupling haemodynamics with vascular wall mechanics and mechanobiology to understand intracranial aneurysms,” International Journal of Computational Fluid Dynamics, vol. 23, no. 8, pp. 569–581, 2009.
[86]
J. M. Dolan, J. Kolega, and H. Meng, “High wall shear stress and spatial gradients in vascular pathology: a review,” Annals of Biomedical Engineering, vol. 41, pp. 1411–1427, 2012.
[87]
A. Kamiya and T. Togawa, “Adaptive regulation of wall shear stress to flow change in the canine carotid artery,” The American journal of physiology, vol. 239, no. 1, pp. H14–H21, 1980.
[88]
F. Tronc, M. Wassef, B. Esposito, D. Henrion, S. Glagov, and A. Tedgui, “Role of NO in flow-induced remodeling of the rabbit common carotid artery,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 16, no. 10, pp. 1256–1262, 1996.
[89]
F. Tronc, Z. Mallat, S. Lehoux, M. Wassef, B. Esposito, and A. Tedgui, “Role of matrix metalloproteinases in blood flow-induced arterial enlargement: interaction with NO,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 20, no. 12, pp. E120–E126, 2000.
[90]
M. S. Aln？s, J. Isaksen, K.-A. Mardal, B. Romner, M. K. Morgan, and T. Ingebrigtsen, “Computation of hemodynamics in the circle of Willis,” Stroke, vol. 38, no. 9, pp. 2500–2505, 2007.
[91]
A. Mantha, C. Karmonik, G. Benndorf, C. Strother, and R. Metcalfe, “Hemodynamics in a cerebral artery before and after the formation of an aneurysm,” American Journal of Neuroradiology, vol. 27, no. 5, pp. 1113–1118, 2006.
[92]
M. D. Ford, Y. Hoi, M. Piccinelli, L. Antiga, and D. A. Steinman, “An objective approach to digital removal of saccular aneurysms: technique and applications,” The British Journal of Radiology, vol. 82, pp. S55–S61, 2009.
[93]
L. Boussel, V. Rayz, C. McCulloch et al., “Aneurysm growth occurs at region of low wall shear stress: patient-specific correlation of hemodynamics and growth in a longitudinal study,” Stroke, vol. 39, no. 11, pp. 2997–3002, 2008.
[94]
S. I. Sugiyama, H. Meng, K. Funamoto et al., “Hemodynamic analysis of growing intracranial aneurysms arising from a posterior inferior cerebellar artery,” World Neurosurgery, vol. 78, no. 5, pp. 462–468, 2012.
[95]
A. Valencia, H. Morales, R. Rivera, E. Bravo, and M. Galvez, “Blood flow dynamics in patient-specific cerebral aneurysm models: the relationship between wall shear stress and aneurysm area index,” Medical Engineering and Physics, vol. 30, no. 3, pp. 329–340, 2008.
[96]
D. M. Sforza, C. M. Putman, S. Tateshima, F. Vi？uela, and J. R. Cebral, “Effects of perianeurysmal environment during the growth of cerebral aneurysms: a case study,” American Journal of Neuroradiology, vol. 33, pp. 1115–1120, 2012.
[97]
J. Xu, Y. Yu, X. Wu et al., “Morphological and hemodynamic analysis of mirror posterior communicating artery aneurysms,” Plos One, vol. 8, no. 1, Article ID e55413, pp. 1–7, 2013.
[98]
M. A. Castro, C. M. Putman, and J. R. Cebral, “Computational fluid dynamics modeling of intracranial aneurysms: effects of parent artery segmentation on intra-aneurysmal hemodynamics,” American Journal of Neuroradiology, vol. 27, no. 8, pp. 1703–1709, 2006.
[99]
M. A. Castro, C. M. Putman, and J. R. Cebral, “Effects of parent vessel geometry on intraaneurysmal flow patterns,” in Medical Imaging 2006: Physiology, Function, and Structure from Medical Images, vol. 6143 of Proceedings of SPIE, San Diego, Calif, USA, February 2006.
[100]
Y. Miura, F. Ishida, Y. Umeda et al., “Low wall shear stress is independently associated with the rupture status of middle cerebral artery aneurysms,” Stroke, vol. 44, pp. 519–521, 2013.
[101]
J. Patti, F. Vi？uela, and A. Chien, “Distinct trends of pulsatility found at necks of ruptured and unruptured aneurysms,” Journal of Interventional Surgery, 2013.
[102]
A. Chien, S. Tateshima, J. Sayre, M. Castro, J. Cebral, and F. Vi？uela, “Patient-specific hemodynamic analysis of small internal carotid artery-ophthalmic artery aneurysms,” Surgical Neurology, vol. 72, no. 5, pp. 444–450, 2009.
[103]
J. R. Cebral and H. Meng, “Counterpoint: realizing the clinical utility of computational fluid dynamics—closing the gap,” American Journal of Neuroradiology, vol. 33, no. 3, pp. 396–398, 2012.
[104]
H. Meng, V. M. Tutino, J. Xiang, and A. Siddiqui, “High WSS or low WSS? Complex interactions of hemodynamics with intracranial aneurysm initiation, growth, and rupture: toward a unifying hypothesis,” American Journal of Neuroradiology, 2013.
[105]
T. Horiuchi, Y. Tanaka, and K. Hongo, “Surgical treatment for aneurysmal subarachnoid hemorrhage in the 8th and 9th decades of life,” Neurosurgery, vol. 56, no. 3, pp. 469–474, 2005.
[106]
E. H. Brilstra, G. J. E. Rinkel, Y. Van Der Graaf, W. J. J. Van Rooij, and A. Algra, “Treatment of intracranial aneurysms by embolization with coils: a systematic review,” Stroke, vol. 30, no. 2, pp. 470–476, 1999.
[107]
D. Perlmutter and A. L. Rhoton Jr., “Microsurgical anatomy of the anterior cerebral anterior communicating recurrent artery complex,” Journal of Neurosurgery, vol. 45, no. 3, pp. 259–272, 1976.
[108]
H. Kasuya, T. Shimizu, K. Nakaya, A. Sasahara, T. Hori, and K. Takakura, “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, vol. 45, no. 1, p. 89, 1999.
[109]
F. T. Charbel, D. Seyfried, B. Mehta, M. Dujovny, and J. I. Ausman, “Dominant A1: angiographic and clinical correlations with anterior communicating artery aneurysms,” Neurological Research, vol. 13, no. 4, pp. 253–256, 1991.
[110]
E. Tarulli and A. J. Fox, “Potent risk factor for aneurysm formation: termination aneurysms of the anterior communicating artery and detection of A1 vessel asymmetry by flow dilution,” American Journal of Neuroradiology, vol. 31, no. 7, pp. 1186–1191, 2010.
[111]
T. Hassan, A. A. Hassan, and Y. M. Ahmed, “Influence of parent vessel dominancy on fluid dynamics of anterior communicating artery aneurysms,” Acta Neurochirurgica, vol. 153, no. 2, pp. 305–310, 2011.
[112]
N. Hashimoto, H. Handa, I. Nagata, and F. Hazama, “Experimentally induced cerebral aneurysms in rats: V. Relation of hemodynamics in the circle of Willis to formation of aneurysms,” Surgical Neurology, vol. 13, no. 1, pp. 41–45, 1980.
[113]
L. Xu, F. Zhang, H. Wang, and Y. Yu, “Contribution of the hemodynamics of A1 dysplasia or hipoplasia to anterior communicating artery aneurysms: a 3-dimensional numerical simulation study,” Journal of Computer Assisted Tomography, vol. 36, no. 4, pp. 421–42610, 2012.
[114]
S. G. Imbesi and C. W. Kerber, “Analysis of slipstream flow in two ruptured intracranial cerebral aneurysms,” American Journal of Neuroradiology, vol. 20, no. 9, pp. 1703–1705, 1999.
[115]
M. A. Castro, C. M. Putman, and J. R. Cebral, “Patient-Specific computational modeling of cerebral aneurysms with multiple avenues of flow from 3D rotational angiography images,” Academic Radiology, vol. 13, no. 7, pp. 811–821, 2006.
[116]
M. A. Castro, C. M. Putman, and J. R. Cebral, “Patient-specific computational fluid dynamics modeling of anterior communicating artery aneurysms: a study of the sensitivity of intra-aneurysmal flow patterns to flow conditions in the carotid arteries,” American Journal of Neuroradiology, vol. 27, no. 10, pp. 2061–2068, 2006.
[117]
C. Karmonik, C. Yen, R. G. Grossman, R. Klucznik, and G. Benndorf, “Intra-aneurysmal flow patterns and wall shear stresses calculated with computational flow dynamics in an anterior communicating artery aneurysm depend on knowledge of patient-specific inflow rates,” Acta Neurochirurgica, vol. 151, no. 5, pp. 479–485, 2009.
[118]
S. Hodis, S. Uthamaraj, G. Lanzino, D. F. Kallmes, and D. Dragomir-Daescu, “Computational fluid dynamics simulation of an anterior communicating artery ruptured during angiography,” Journal of NeuroInterventional Surgery, 2013.
[119]
T. E. Darsaut, F. Bing, I. Salazkin, G. Gevry, and J. Raymond, “Flow diverters failing to occlude experimental bifurcation on curved sidewall aneurysms: an in vivo study in canines,” Journal of Neuroradiology, vol. 117, pp. 37–44, 2012.
[120]
G. R. Stuhne and D. A. Steinman, “Finite-element modeling of the hemodynamics of stented aneurysms,” Journal of Biomechanical Engineering, vol. 126, no. 3, pp. 382–387, 2004.
[121]
J. R. Cebral and R. L？hner, “Efficient simulation of blood flow past complex endovascular devices using an adaptive embedding technique,” IEEE Transactions on Medical Imaging, vol. 24, no. 4, pp. 468–476, 2005.
[122]
S. P. Ferns, M. E. S. Sprengers, W. J. Van Rooij et al., “Coiling of intracranial aneurysms: a systematic review on initial occlusion and reopening and retreatment rates,” Stroke, vol. 40, no. 8, pp. e523–e529, 2009.
[123]
W. J. Van Rooij and M. Sluzewski, “Endovascular treatment of large and giant aneurysms,” American Journal of Neuroradiology, vol. 30, no. 1, pp. 12–18, 2009.
[124]
D. Fiorella, P. Lylyk, I. Szikora et al., “Curative cerebrovascular reconstruction with the Pipeline embolization device: the emergence of definitive endovascular therapy for intracranial aneurysms,” Journal of NeuroInterventional Surgery, vol. 1, no. 1, pp. 56–65, 2009.
[125]
H. G. Morales, M. Kim, E. E. Vivas et al., “How do coil configuration and packing density influence intra-aneurysmal hemodynamics?” American Journal of Neuroradiology, vol. 32, no. 10, pp. 1935–1941, 2011.
[126]
S. Appanaboyina, F. Mut, R. L？hner et al., “Computational modelling of blood flow in side arterial branches after stenting of cerebral aneurysms,” International Journal of Computational Fluid Dynamics, vol. 22, no. 10, pp. 669–676, 2008.
[127]
D. Ma, G. F. Dargush, S. K. Natarajan, E. I. Levy, A. H. Siddiqui, and H. Meng, “Computer modeling of deployment and mechanical expansion of neurovascular flow diverter in patient-specific intracranial aneurysms,” Journal of Biomechanics, vol. 45, pp. 2256–2263, 2012.
[128]
I. Larrabide, M. L. Aguilar, H. G. Morales et al., “Intra-aneurysmal pressure and flow changes induced by flow diverters: relation to aneurysm size and shape,” American Journal of Neuroradiology, vol. 27, pp. 1–7, 2013.
[129]
L. M. Héman, L. M. Jongen, H. B. Van Der Worp, G. J. E. Rinkel, and J. Hendrikse, “Incidental intracranial aneurysms in patients with internal carotid artery stenosis: a CT angiography study and a metaanalysis,” Stroke, vol. 40, no. 4, pp. 1341–1346, 2009.
[130]
J. I. G. León, L. C. Aramendía, F. B. Marco, and J. C. V. Suárez, “Concomitant endovascular treatment of concomitant extracranial carotid stenosis and intracranial aneurysm: our experience,” Interventional Neuroradiology, vol. 15, no. 1, pp. 53–59, 2009.
[131]
E. Castro Reyes, F. Villoria, F. Fortea et al., “Simultaneous cerebral aneurysms and carotid disease: should the symptomatic lesion always be the first to be treated? A case report,” Interventional Neuroradiology, vol. 9, no. 2, pp. 213–218, 2003.
[132]
J. P. Archie Jr. and R. W. Feldtman, “Collateral cerebral vascular resistance in patients with significant carotid stenosis,” Stroke, vol. 13, no. 6, pp. 829–831, 1982.
[133]
B. A. Wasserman, R. J. Wityk, H. H. Trout III, and R. Virmani, “Low-grade carotid stenosis: looking beyond the lumen with MRI,” Stroke, vol. 36, no. 11, pp. 2504–2513, 2005.
[134]
M. J. Workman, H. J. Cloft, F. C. Tong et al., “Thrombus formation at the neck of cerebral aneurysms during treatment with Guglielmi detachable coils,” American Journal of Neuroradiology, vol. 23, no. 9, pp. 1568–1576, 2002.
[135]
V. L. Rayz, L. Boussel, L. Ge et al., “Flow residence time and regions of intraluminal thrombus deposition in intracranial aneurysms,” Annals of Biomedical Engineering, vol. 38, no. 10, pp. 3058–3069, 2010.
[136]
J. E. Cohen, E. Yitshayek, J. M. Gomori et al., “Spontaneous thrombosis of cerebral aneurysms presenting with ischemic stroke,” Journal of the Neurological Sciences, vol. 254, no. 1-2, pp. 95–98, 2007.
[137]
X. Wang and X. Li, “Biomechanical behaviour of cerebral aneurysm and its relation with the formation of intraluminal thrombus: a patient-specific modeling study,” Computer Methods in Biomechanics and Biomedical Engineering, 2012.
[138]
A. M. Malek, S. L. Alper, and S. Izumo, “Hemodynamic shear stress and its role in atherosclerosis,” Journal of the American Medical Association, vol. 282, no. 21, pp. 2035–2042, 1999.
[139]
V. Costalat, M. Sanchez, D. Ambard et al., “Biomechanical wall properties of human intracranial aneurysms resected following surgical clipping (IRRAs Project),” Journal of Biomechanics, vol. 44, no. 15, pp. 2685–2691, 2011.
[140]
M. Sánchez, D. Ambard, V. Costalat, S. Méndez, F. Jourdan, and F. Nicoud, “Biomechanical assessment of the individual risk of rupture of cerebral aneurysms: a proof of concept,” Annals of Biomedical Engineering, vol. 41, no. 1, pp. 28–40, 2012.
[141]
J. G. Isaksen, Y. Bazilevs, T. Kvamsdal et al., “Determination of wall tension in cerebral artery aneurysms by numerical simulation,” Stroke, vol. 39, no. 12, pp. 3172–3178, 2008.
[142]
G. Xiong, C. A. Figueroa, N. Xiao, and C. A. Taylor, “Simulation of blood flow in deformable vessels using subject-specific geometry and spatially varying wall properties,” International Journal for Numerical Methods in Biomedical Engineering, vol. 27, no. 7, pp. 1000–1016, 2011.
[143]
S. Balocco, O. Camara, E. Vivas et al., “Feasibility of estimating regional mechanical properties of cerebral aneurysms in vivo,” Medical Physics, vol. 37, no. 4, pp. 1689–1706, 2010.
[144]
Y. Bazilevs, M.-C. Hsu, Y. Zhang et al., “Computational vascular fluid-structure interaction: methodology and application to cerebral aneurysms,” Biomechanics and Modeling in Mechanobiology, vol. 9, no. 4, pp. 481–498, 2010.
[145]
A. Valencia, F. Mu？oz, S. Araya, R. Rivera, and E. Bravo, “Comparison between computational fluid dynamics, fluid-structure interaction and computational structural dynamics predictions of flow-induced wall mechanics in an anatomically realistic cerebral aneurysm model,” International Journal of Computational Fluid Dynamics, vol. 23, no. 9, pp. 649–666, 2009.
[146]
R. Torii, M. Oshima, T. Kobayashi, K. Takagi, and T. E. Tezduyar, “Numerical investigation of the effect of hypertensive blood pressure on cerebral aneurysm—dependence of the effect on the aneurysm shape,” International Journal for Numerical Methods in Fluids, vol. 54, no. 6-8, pp. 995–1009, 2007.
[147]
L. Antiga, B. A. Wasserman, and D. A. Steinman, “On the overestimation of early wall thickening at the carotid bulb by black blood MRI, with implications for coronary and vulnerable plaque imaging,” Magnetic Resonance in Medicine, vol. 60, no. 5, pp. 1020–1028, 2008.
[148]
D. A. Steinman, L. Antiga, and B. A. Wasserman, “Overestimation of cerebral aneurysm wall thickness by black blood MRI?” Journal of Magnetic Resonance Imaging, vol. 31, no. 3, p. 766, 2010.
[149]
J. D. Humphrey and C. A. Taylor, “Intracranial and abdominal aortic aneurysms: similarities, differences, and need for a new class of computational models,” Annual Review of Biomedical Engineering, vol. 10, pp. 221–246, 2008.
[150]
P. Di Achille and J. D. Humphrey, “Toward large-scale computational Fluid-Solid-Growth models of intracranial aneurysms,” Yale Journal of Biology and Medicine, vol. 85, pp. 217–228, 2012.
[151]
C. A. Taylor and D. A. Steinman, “Image-based modeling of blood flow and vessel wall dynamics: applications, methods and future directions: Sixth international bio-fluid mechanics symposium and workshop, March 28-30, 2008 Pasadena, California,” Annals of Biomedical Engineering, vol. 38, no. 3, pp. 1188–1203, 2010.
[152]
D. A. Steinman, D. A. Vorp, and C. R. Ethier, “Computational modeling of arterial biomechanics: insights into pathogenesis and treatment of vascular disease,” Journal of Vascular Surgery, vol. 37, no. 5, pp. 1118–1128, 2003.
[153]
W. Jeong and K. Rhee, “Hemodynamics of cerebral aneurysms: computational analyses of aneurysm progress and treatment,” Comp Math Meth Med, vol. 2012, Article ID 782801, 11 pages, 2012.
[154]
J. R. Cebral and M. Raschi, “Suggested connections between risk factors of intracranial aneurysms: a review,” Annals of Biomedical Engineering, vol. 41, no. 7, pp. 1366–1383, 2012.
[155]
C. A. Taylor and C. A. Figueroa, “Patient-specific modeling of cardiovascular mechanics,” Annual Review of Biomedical Engineering, vol. 11, pp. 109–134, 2009.
[156]
L. Augsburger, P. Reymond, E. Fonck et al., “Methodologies to assess blood flow in cerebral aneurysms: current state of research and perspectives,” Journal of Neuroradiology, vol. 36, no. 5, pp. 270–277, 2009.
[157]
P. R. Hoskins and D. Hardman, “Three-dimensional imaging and computational modelling for estimation of wall stresses in arteries,” The British Journal of Radiology, vol. 82, pp. S3–S17, 2009.
