Abstract
The evolution of intracranial aneurysms (IAs) is thought to be driven by progressive wall degradation in response to abnormal hemodynamics. Previous studies focused on the relationship between global hemodynamics and wall properties. However, hemodynamics, wall structure and mechanical properties of cerebral aneurysms can be non-uniform across the aneurysm wall. Therefore, the aim of this work is to introduce a methodology for mapping local hemodynamics to local wall structure in resected aneurysm specimens. This methodology combines image-based computational fluid dynamics, tissue resection, micro-CT imaging of resected specimens mounted on 3D-printed aneurysm models, alignment to 3D vascular models, multi-photon microscopy of the wall, and regional mapping of hemodynamics and wall properties. This approach employs a new 3D virtual marking tool for surgeons to delineate the location of the resected specimen directly on the 3D model, while in the surgical suite. The case of a middle cerebral artery aneurysm is used to illustrate the application of this methodology to the assessment of the relationship between local wall shear stress and local wall properties including collagen fiber organization and wall geometry. This methodology can similarly be used to study the relationship between local intramural stresses and local wall structure.
Similar content being viewed by others
References
Barbe, M. F., R. Adiga, O. Gordiienko, N. Pleshko, M. E. Selzer, and B. Krynska. Micro-computed tomography assessment of vertebral column defects in retinoic acid-induced rat model of myelomeningocele. Birth Defects Res. A Clin. Mol. Teratol. 100:453–462, 2014.
Broderick, J. P., R. D. Brown, Jr, L. Sauerbeck, R. Hornung, J. Huston, 3rd, D. Woo, C. Anderson, G. Rouleau, D. Kleindorfer, M. L. Flaherty, I. Meissner, T. Foroud, E. C. Moomaw, and E. S. Connolly. Greater rupture risk for familial as compared to sporadic unruptured intracranial aneurysms. Stroke 40:1952–1957, 2009.
Cebral, J. R., 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 Trans. Med. Imaging 24:457–467, 2005.
Cebral, J. R., M. A. Castro, C. M. Putman, and N. Alperin. Flow-area relationship in internal carotid and vertebral arteries. Physiol. Meas. 29:585–594, 2008.
Cebral, J. R., X. Duan, B. J. Chung, C. M. Putman, K. Aziz, and A. M. Robertson. Wall mechanical properties and hemodynamics of unruptured intracranial aneurysms. AJNR Am. J. Neuroradiol. 36:1695–1703, 2015.
Cebral, J. R., R. Pergolizzi, and C. M. Putman. Computational fluid dynamics modeling of intracranial aneurysms: qualitatively comparison with cerebral angiography. Acad. Radiol. 14:804–813, 2007.
Costalat, V., M. Sanchez, D. Ambard, L. Thines, N. Lonjon, F. Nicoud, H. Brunel, J. P. Lejeune, H. Dufour, P. Bouillot, J. P. Lhaldky, K. Kouri, F. Segnarbieux, C. A. Maurage, K. Lobotesis, M. C. Villa-Uriol, C. Zhang, A. F. Frangi, G. Mercier, A. Bonafe, L. Sarry, and F. Jourdan. Biomechanical wall properties of human intracranial aneurysms resected following surgical clipping (IRRAs Project). J. Biomech. 44:2685–2691, 2011.
Dempere-Marco, L., E. Oubel, M. A. Castro, C. M. Putman, A. F. Frangi, and J. R. Cebral. CFD analysis incorporating the influence of wall motion: application to intracranial aneurysms. Med. Image Comput. Comput. Assist. Interv. 9:438–445, 2006.
Erhart, P., C. Grond-Ginsbach, M. Hakimi, F. Lasitschka, S. Dihlmann, D. Bockler, and A. Hyhlik-Durr. Finite element analysis of abdominal aortic aneurysms: predicted rupture risk correlates with aortic wall histology in individual patients. J. Endovasc. Ther. 21:556–564, 2014.
Ford, M. D., H. N. Nikolov, J. S. Milner, S. P. Lownie, E. M. DeMont, W. Kalata, F. Loth, D. W. Holdsworth, and D. A. Steinman. PIV-measured versus CFD-predicted flow dynamics in anatomically realistic cerebral aneurysm models. J. Biomech. Eng. 130:021015–021011/021019, 2008.
Ford, M. D., G. R. Stuhne, H. N. Nikolov, D. F. Habets, S. P. Lownie, D. W. Holdsworth, and D. A. Steinman. Virtual angiography for visualization and validation of computational models of aneurysm hemodynamics. IEEE Trans. Med. Imaging 24:1586–1592, 2005.
Frosen, J. Smooth muscle cells and the formation, degeneration, and rupture of saccular intracranial aneurysm wall—a review of current pathophysiological knowledge. Transl. Stroke Res. 5:347–356, 2014.
Groen, H. C., T. van Walsum, S. Rozie, S. Klein, K. van Gaalen, F. J. Gijsen, P. A. Wielopolski, H. M. van Beusekom, R. de Crom, H. J. Verhagen, A. F. van der Steen, A. van der Lugt, J. J. Wentzel, and W. J. Niessen. Three-dimensional registration of histology of human atherosclerotic carotid plaques to in vivo imaging. J. Biomech. 43:2087–2092, 2010.
Hill, M. R., X. Duan, G. A. Gibson, S. Watkins, and A. M. Robertson. A theoretical and non-destructive experimental approach for direct inclusion of measured collagen orientation and recruitment into mechanical models of the artery wall. J. Biomech. 45:762–771, 2012.
Humphrey, J. D., and P. B. Canham. Structure, mechanical properties, and mechanics of intracranial saccular aneurysms. J. Elast. 61:49–81, 2000.
International Study of Unruptured Intracranial Aneurysms Investigators. Unruptured intracranial aneurysms–risk of rupture and risks of surgical intervention. N. Engl. J. Med. 339:1725–1733, 1998.
Juvela, S., M. Porras, and K. Poussa. Natural history of unruptured intracranial aneurysms: probability of and risk factors for aneurysm rupture. J. Neurosurg. 108:1052–1060, 2008.
Meng, H., D. D. Swart, Z. Wang, Y. Hoi, J. Kolega, E. M. Metaxa, M. P. Szymanski, J. Yamamoto, E. Sauvageau, and E. I. Levy. A model system for mapping vascular responses to complex hemodynamics at arterial bifurcations in vivo. Neurosurgery 59:1094–1101, 2006.
Morita, A., S. Fujiwara, K. Hashi, H. Ohtsu, and T. Kirino. Risk of rupture associated with intact cerebral aneurysms in the Japanese population: a systematic review of the literature from Japan.[see comment]. J. Neurosurg. 102:601–606, 2005.
Morita, A., T. Kimura, M. Shojima, T. Sameshima, and T. Nishihara. Unruptured intracranial aneurysms: current perspectives on the origin and natural course, and quest for standards in the management strategy. Neurol. Med. Chir. (Tokyo) 50:777–787, 2010.
Raschi, M., F. Mut, G. Byrne, C. M. Putman, S. Tateshima, F. Vinuela, T. Tanoue, K. Tanishita, and J. R. Cebral. CFD and PIV analysis of hemodynamics in a growing intracranial aneurysm. Int. J. Numer. Method Biomed. Eng. 28:214–228, 2012.
Rinkel, G. J., M. Djibuti, and J. van Gijn. Prevalence and risk of rupture of intracranial aneurysms: a systematic review. Stroke 29:251–259, 1998.
Robertson, A. M., X. Duan, M. R. Hill, K. Aziz, and J. R. Cebral. Diversity in the strength and structure of unruptured cerebral aneurysms. Ann. Biomed. Eng. 43:1502–1515, 2014.
Robertson, A. M., A. Sequeira, and M. V. Kameneva. Hemorheology. In: Hemodynamical Flows: Modeling, Analysis and Simulation, edited by G. P. Galdi, R. Rannacher, A. M. Robertson, and S. Turek. Birkhäuser: Basel, 2008.
Schneider, C. A., W. S. Rasband, and K. W. Eliceiri. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9:671–675, 2012.
Sforza, D., R. Löhner, C. M. Putman, and J. R. Cebral. Hemodynamic analysis of intracranial aneurysms with moving parent arteries: basilar tip aneurysms. IJNMBE Int. J. Num. Methods Biomed. Eng. 26:1219–1227, 2010.
Tremmel, M., J. Xiang, Y. Hoi, J. Kolega, A. H. Siddiqui, J. Mocco, and H. Meng. Mapping of vascular response to hemodynamics: applications to an aneurysm initiation model. Biomech. Model. Mechanobiol. 9:421–434, 2011.
Ujiie, H., H. Tachibana, O. Hiramatsu, A. L. Hazel, T. Matsumoto, Y. Ogasawara, H. Nakajima, T. Hori, K. Takakura, and F. Kajiya. Effects of size and shape (aspect ratio) on the hemodynamics of saccular aneurysms: a possible index for surgical treatment of intracranial aneurysms. Neurosurgery 45:119–129, 1999.
Wiebers, D. O., J. C. Torner, and I. Meissner. Impact of unruptured intracranial aneurysms on public health in the United States. Stroke 23:1416–1419, 1992.
Acknowledgments
This work was supported by NIH Grant R21NS080031. We thank Mary Barbe, Director of Micro-CT Core and Imaging Center at Temple University School of Medicine, for advice on biological tissue imaging; and George Stetton, Professor of Bioengineering, University of Pittsburgh, for valuable discussions on the virtual IA sample.
Author information
Authors and Affiliations
Corresponding author
Additional information
Associate Editor Andreas Anayiotos oversaw the review of this article.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10439_2016_1682_MOESM1_ESM.png
Overview of mapping strategy: 1) tissue marking and harvesting, 2) construction of vascular model, 3) 3D printing of vascular model, 4) mounting resected sample on 3D printed aneurysm model and micro-CT scanning, 5) alignment of virtual tissue sample to vascular model. Supplementary material 1 (PNG 1058 kb)
10439_2016_1682_MOESM2_ESM.png
Surgical procedure: exposure of the aneurysm (A), clip(s) placement (B, C), marking with surgical pen (D), aneurysm resection (E, F), and fresh resected sample with mark (G, H). Supplementary material 2 (PNG 3248 kb)
Rights and permissions
About this article
Cite this article
Cebral, J.R., Duan, X., Gade, P.S. et al. Regional Mapping of Flow and Wall Characteristics of Intracranial Aneurysms. Ann Biomed Eng 44, 3553–3567 (2016). https://doi.org/10.1007/s10439-016-1682-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10439-016-1682-7