Image-based modeling for better understanding and assessment of atherosclerotic plaque progression and vulnerability: Data, modeling, validation, uncertainty and predictions

Journal of Biomechanics

Volumn 47, Issue 4, 2014, Pages 834-846

  Tang, Dalin ^a,b   Kamm, Roger D ^c   Yang, Chun ^b,d   Zheng, Jie ^e   Canton, Gador ^f   Bach, Richard ^g   Huang, Xueying ^h   Hatsukami, Thomas S ⁱ   Zhu, Jian ^a   Ma, Genshan ^a   Maehara, Akiko ^j   Mintz, Gary S ^j   Yuan, Chun ⁱ  

^a SOUTHEAST UNIVERSITY   (China)

^b WORCESTER POLYTECHNIC INSTITUTE   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d China Information Technology Designing and Consulting Institute Co Ltd   (China)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f University of Washington   (United States)

^g WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h XIAMEN UNIVERSITY   (China)

ⁱ UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^j CARDIOVASCULAR RESEARCH FOUNDATION   (United States)

more..

Author keywords

Atherosclerosis; Fluid structure interaction; IVUS based modeling; MRI based modeling; Vulnerable plaques

Indexed keywords

FORECASTING; MEDICAL IMAGING;

ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CLINICAL PRACTICES; IMAGE-BASED MODELING; IMAGE-BASED MODELS; MODEL PREDICTION; SCREENING STRATEGY; VULNERABLE PLAQUES;

UNCERTAINTY ANALYSIS;

ACCURACY; ANGIOGRAPHY; ARTICLE; ATHEROSCLEROTIC PLAQUE; CALCULATION; CARDIAC IMAGING; COMPUTER ASSISTED TOMOGRAPHY; DISEASE COURSE; GEOMETRY; HISTOLOGY; HUMAN; IMAGE ANALYSIS; IMAGE PROCESSING; IMAGE QUALITY; INTRAVASCULAR ULTRASOUND; MATHEMATICAL MODEL; NEAR INFRARED SPECTROSCOPY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OPTICAL COHERENCE TOMOGRAPHY; OPTICAL COHERENCE TOMOGRAPHY DEVICE; PREDICTIVE VALUE; PRIORITY JOURNAL; RELIABILITY; RISK FACTOR; SENSITIVITY AND SPECIFICITY; SHEAR STRESS; SIMULATION; ULTRASOUND SCANNER; VALIDITY; WALL STRESS;

ATHEROSCLEROSIS; FLUID-STRUCTURE INTERACTION; IVUS-BASED MODELING; MRI-BASED MODELING; VULNERABLE PLAQUES;

DISEASE PROGRESSION; HUMANS; MAGNETIC RESONANCE IMAGING; MODELS, CARDIOVASCULAR; PLAQUE, ATHEROSCLEROTIC; PREDICTIVE VALUE OF TESTS; REPRODUCIBILITY OF RESULTS; UNCERTAINTY;

EID: 84894646086     PISSN: 00219290     EISSN: 18732380     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2014.01.012     Document Type: Article

References (83)

1. American Heart Association, 2005. Heart Disease and Stroke Statistics-2005 Update. http://www.americanheart.org/downloadable/heart/1105390918119HDSStats2005Update.p.
2. Arroyo L.H., Lee R.T. Mechanisms of plaque rupture: mechanical and biologic interactions. Cardiovasc. Res. 1999, 41(2):369-375.
3. Baldewsing R.A., Danilouchkine M.G., Mastik F., Schaa J.A, Serruys P.W., van der Steen A.F. An inverse method for imaging the local elasticity of atherosclerotic coronary plaques. IEEE Trans. Inf. Technol. Biomed. 2008, 12(3):277-289.
4. Barnett H.J., Eliasziw M., Meldrum H.E. Evidence based cardiology: prevention of ischaemic stroke. Br. Med. J. 1999, 318(7197):1539-1543.
5. Bluestein D., Alemu Y., Avrahami I., Gharib M., Dumont K., Ricotta J.J., Einav S. Influence of microcalcifications on vulnerable plaque mechanics using FSI modeling. J. Biomech. 2008, 41(5):1111-1118.
6. Bourantas C.V., Garcia-Garcia H.M., Farooq V., Maehara A., Xu K., Généreux P., Diletti R., Muramatsu T., Fahy M., Weisz G., Stone G.W., Serruys P.W. Clinical and angiographic characteristics of patients likely to have vulnerable plaques: analysis from the PROSPECT study. JACC Cardiovasc Imaging 2013, 6(12):1263-1272.
7. Canton G., Hippe D.S., Sun J., Kerwin W.S., Tang D., Yuan C. Characterization of distensibility, plaque burden and composition of the atherosclerotic carotid artery using magnetic resonance imaging. Med. Phys. 2012, 39(10):6247-6254.
8. Caplan J.D., Waxman S., Nesto R.W., Muller J.E. Near-infrared spectroscopy for the detection of vulnerable coronary artery plaques. J. Am. Coll. Cardiol. 2006, 47(8 Suppl.):C92-C96.
9. Cardoso, L., Weinbaum, S., 2013. Changing views of the biomechanics of vulnerable plaque rupture: a review. Ann. Biomed. Eng. [Epub ahead of print], PMID: 23842694 [PubMed - as supplied by publisher] PMCID: PMC3888649.
10. Cheng G.C., Loree H.M., Kamm R.D., Fishbein M.C., Lee R.T. Distribution of circumferential stress in ruptured and stable atherosclerotic lesions. A structural analysis with histopathological correlation. Circulation 1993, 87:1179-1187.
11. Finet G., Ohayon J., Rioufol G. Biomechanical interaction between cap thickness, lipid core composition and blood pressure in vulnerable coronary plaque: impact on stability or instability. Coron. Artery Dis. 2004, 15(1):13-20.
12. Fleg J.L., Stone G.W., Fayad Z.A., Granada J.F., Hatsukami T.S., Kolodgie F.D., Ohayon J., Pettigrew R., Sabatine M.S., Tearney G.J., Waxman S., Domanski M.J., Srinivas P.R., Narula J. Detection of high-risk atherosclerotic plaque: report of the NHLBI working group on current status and future directions. JACC Cardio Imaging 2012, 5(9):941-955.
13. Friedman M.H. Arteriosclerosis research using vascular flow models: from 2-D branches to compliant replicas. J. Biomech. Eng. 1993, 115:595-601.
14. Friedman M.H., Bargeron C.B., Deters O.J., Hutchins G.M., Mark F.F. Correlation between wall shear and intimal thickness at a coronary artery branch. Atherosclerosis 1987, 68:27-33.
15. Friedman M.H., Krams R., Chandran K.B. Flow interactions with cells and tissues: cardiovascular flows and fluid-structure interactions. Ann. Biomed Eng. 2010, 38(3):1178-1187.
16. Fuster V. The vulnerable atherosclerotic plaque: understanding, identification, and modification. AHA Monograph Series 1998, Futura Publishing, Armonk, NY. V. Fuster, J.F. Cornhill, R.E. Dinsmore, J.T. Fallon, W. Insull, P. Libby, S. Nissen, M.E. Rosenfeld, W.D. Wagner (Eds.).
17. Fuster V., Stein B., Ambrose J.A., Badimon L., Badimon J.J., Chesebro J.H. Atherosclerotic plaque rupture and thrombosis, evolving concept. Circulation 1990, 82:SII-47-59.
18. Gao H., Long Q., Das S.K., Halls J., Graves M., Gillard J.H., Li Z.Y. Study of carotid arterial plaque stress for symptomatic and asymptomatic patients. J. Biomech. 2011, 44(14):2551-2557.
19. Gardner C.M., Tan H., Hull E.L., Lisauskas J.B., Sum S.T., Meese T.M., Jiang C., Madden S.P., Caplan J.D., Burke A.P., Virmani R., Goldstein J., Muller J.E. Detection of lipid core coronary plaques in autopsy specimens with a novel catheter-based near-infrared spectroscopy system. JACC Cardiovasc. Imaging 2008, 1(5):638-648.
20. Garrett M.F., Laird N.M., Ware J.H. Applied Longitudinal Analysis 2004, Wiley-Interscience, Hoboken, NJ.
21. Gibson C.M., Diaz L., Kandarpa K., Sacks F.M., Pasternak R.C., Sandor T., Feldman C., Stone P.H. Relation of vessel wall shear stress to atherosclerosis progression in human coronary arteries. Arterioscler. Thromb. Vasc. Biol. 1993, 13(2):310-315.
22. Giddens D.P., Zarins C.K., Glagov S. The role of fluid mechanics in the localization and detection of atherosclerosis. J. Biomech. Eng. 1993, 115:588-594.
23. Gorelick P.B. Carotid endarterectomy: where do we draw the line?. Stroke 1990, 30:1745-1750.
24. Harloff A., Albrecht F., Spreer J., Stalder A.F., Bock J., Frydrychowicz A., Schöllhorn J., Hetzel A., Schumacher M., Hennig J., Markl M. 3D blood flow characteristics in the carotid artery bifurcation assessed by flow-sensitive 4D MRI at 3T. Magn. Reson. Med. 2009, 61(1):65-74.
25. Harloff A., Zech T., Frydrychowicz A., Schumacher M., Schöllhorn J., Hennig J., Weiller C., Markl M. Carotid intima-media thickness and distensibility measured by MRI at 3T versus high-resolution ultrasound. Eur. Radiol. 2009, 19(6):1470-1479.
26. Holzapfel G.A., Stadler M., Schulze-Bause C.A.J. A layer-specific three-dimensional model for the simulation of balloon angioplasty using Magnetic Resonance Imaging and mechanical testing. Ann. Biomed. Eng. 2002, 30(6):753-767.
27. Huang H., Virmani R., Younis H., Burke A.P., Kamm R.D., Lee R.T. The impact of calcification on the biomechanical stability of atherosclerotic plaques. Circulation 2001, 103:1051-1056.
28. Huang X., Yang C., Canton G., Ferguson M., Yuan C., Tang D. Quantifying effect of intraplaque hemorrhage on critical plaque wall stress in human atherosclerotic plaques using 3D FSI models. J. Biomech. Eng. 2012, 134(12):121004.
29. Huang X., Yang C., Yuan C., Liu F., Canton G., Zheng J., Woodard P.K., Sicard G.A., Tang D. Patient-specific artery shrinkage and 3D zero-stress state in multi-component 3D FSI models for carotid atherosclerotic plaques based on in vivo MRI data. Mol. Cell. Biomech. 2009, 6(2):121-134.
30. Joshi A.K., Leask R.L., Myers J.G., Ojha M., Butany J., Ethier C.R. Intimal thickness is not associated with wall shear stress patterns in the human right coronary artery. Arterioscler. Thromb. Vasc. Biol. 2004, 24(12):2408-2413.
31. Kelly-Arnold A., Maldonado N., Laudier D., Aikawa E., Cardoso L., Weinbaum S. Revised microcalcification hypothesis for fibrous cap rupture in human coronary arteries. Proc. Natl. Acad. Sci. USA 2013, 110(26):10741-10746.
32. Ku D.N., Giddens D.P., Zarins C.K., Glagov S. Pulsatile flow and atherosclerosis in the human carotid bifurcation: positive correlation between plaque location and low and oscillating shear stress. Arteriosclerosis 1985, 5:293-302.
33. Kural M.H., Cai M.C., Tang D., Gwyther T., Zheng J., Billiar K.L. Planar biaxial characterization of diseased human coronary and carotid arteries for computational modeling. J. Biomech. 2012, 45(5):790-798.
34. Le Floc'h S., Cloutier G., Saijo Y., Finet G., Yazdani S.K., Deleaval F., Rioufol G., Pettigrew R.I., Ohayon J. A four-criterion selection procedure for atherosclerotic plaque elasticity reconstruction based on in vivo coronary intravascular ultrasound radial strain sequences. Ultrasound Med. Biol. 2012, 38(12):2084-2097.
35. Lee S.W., Antiga L., Spence J.D., Steinman D.A. Geometry of the carotid bifurcation predicts its exposure to disturbed flow. Stroke 2008, 39(8):2341-2347.
36. Lin A.P., Bennett E., Wisk L.E., Gharib M., Fraser S.E., Wen H. Circumferential strain in the wall of the common carotid artery: Comparing displacement-encoded and cine MRI in volunteers. Magn. Reson. Med. 2008, 60(1):8-13.
37. Liu H., Cai M., Yang C., Zheng J., Bach R., Kural M.H., Billiar K.L., Muccigrosso D., Lu D., Tang D. IVUS-based computational modeling and planar biaxial artery material properties for human coronary plaque vulnerability assessment. Mol. Cell. Biomech. 2012, 9:77-93.
38. Liu H.F., Canton G., Yuan C., Yang C., Billiar K.L., Teng Z.Z., Hoffman A.H., Tang D. Using in vivo Cine and 3D multi-contrast MRI to determine human atherosclerotic carotid artery material properties and circumferential shrinkage rate and their impact on stress/strain predictions. J. Biomech. Eng. 2012, 134(1):011008.
39. Loree H.M., Kamm R.D., Stringfellow R.G., Lee R.T. Effects of fibrous cap thickness on peak circumferential stress in model atherosclerotic vessels. Circ. Res. 1992, 71:850-858.
40. Maehara A., Mintz G.S., Stone G.W. OCT versus IVUS: accuracy versus clinical utility. JACC Cardiovasc. Imaging 2013, 6(10):1105.
41. Maldonado N., Kelly-Arnold A., Vengrenyuk Y., Laudier D., Fallon J.T., Virmani R., Cardoso L., Weinbaum S. A mechanistic analysis of the role of microcalcifications in atherosclerotic plaque stability: potential implications for plaque rupture. Am. J. Physiol. Heart Circ. Physiol. 2012, 303(5):H619-H628.
42. Markl M., Wegent F., Zech T., Bauer S., Strecker C., Schumacher M., Weiller C., Hennig J., Harloff A. In vivo wall shear stress distribution in the carotid artery effect of bifurcation geometry, internal carotid artery stenosis, and recanalization therapy. Circ.-Cardiovasc. Imaging 2010, 3:647-655.
43. Naghavi M., Libby P., Falk E., Casscells S.W., Litovsky S., Rumberger J., Badimon J.J., Stefanadis C., Moreno P., Pasterkamp G., Fayad Z., Stone P.H., Waxman S., Raggi P., Madjid M., Zarrabi A., Burke A., Yuan C., Fitzgerald P.J., Siscovick D.S., de Korte C.L., Aikawa M., Juhani Airaksinen K.E., Assmann G., Becker C.R., Chesebro J.H., Farb A., Galis Z.S., Jackson C., Jang I.K., Koenig W., Lodder R.A., March K., Demirovic J., Navab M., Priori S.G., Rekhter M.D., Bahr R., Grundy S.M., Mehran R., Colombo A., Boerwinkle E., Ballantyne C., Insull W., Schwartz R.S., Vogel R., Serruys P.W., Hansson G.K., Faxon D.P., Kaul S., Drexler H., Greenland P., Muller J.E., Virmani R., Ridker P.M., Zipes D.P., Shah P.K., Willerson J.T. From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: Part I. Circulation 2003, 108(14):1664-1672.
44. Naghavi M., et al. From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: Part II. Circulation 2003, 108(15):1772-1778.
45. Nerem R.M. Vascular fluid mechanics, the arterial wall, and atherosclerosis. J. Biomech. Eng. 1992, 114:274-282.
46. Ohayon J., Dubreuil O., Tracqui P., Floc'h S.L., Rioufol G., Chalabreysse L., Thivolet F., Pettigrew R.I., Finet G. Influence of residual stress/strain on the biomechanical stability of vulnerable coronary plaques: potential impact for evaluating the risk of plaque rupture. Am. J. of Physiol. Heart Circ. Physiol. 2007, 293:H1987-H1996.
47. Ohayon J., Finet G., Gharib A.M., Herzka D.A., Tracqui P., Heroux J., Rioufol G., Kotys M.S., Elagha A., Pettigrew R.I. Necrotic core thickness and positive arterial remodeling index: emergent biomechanical factors for evaluating the risk of plaque rupture. Am. J. Physiol. Heart Circ. Physiol. 2008, 295(2):H717-H727.
48. Ohayon J., Gharib A.M., Garcia A., Heroux J., Yazdani S.K., Malvè M., Tracqui P., Martinez M.A., Doblare M., Finet G., Pettigrew R.I. Is arterial wall-strain stiffening an additional process responsible for atherosclerosis in coronary bifurcations? An in vivo study based on dynamic CT and MRI. Am. J. Physiol. Heart Circ. Physiol. 2011, 301(3):H1097-H1106.
49. Richardson P.D. Biomechanics of plaque rupture: progress, problems, and new frontiers. Ann. Biomed. Eng. 2002, 30(4):524-536.
50. Richardson P.D., Davies M.J., Born G.V. Influence of plaque configuration and stress distribution on fissuring of coronary atherosclerotic plaques. Lancet 1989, 21(2(8669)):941-944.
51. Samady H., Eshtehardi P., McDaniel M.C., Suo J., Dhawan S.S., Maynard C., Timmins L.H., Quyyumi A.A., Giddens D.P. Coronary artery wall shear stress is associated with progression and transformation of atherosclerotic plaque and arterial remodeling in patients with coronary artery disease. Circulation 2011, 124(7):779-788.
52. Speelman L., Akyildiz A.C., den Adel B., Wentzel J.J., van der Steen A.F., Virmani R., van der Weerd L., Jukema J.W., Poelmann R.E., van Brummelen E.H., Gijsen F.J. Initial stress in biomechanical models of atherosclerotic plaques. J. Biomech. 2011, 44(13):2376-2382.
53. Stary H.C., Blankenhorn D.H., Chandler A.B., Glagov S., Insull W., Richardson M., Rosenfeld M.E., Schaffer S.A., Schwartz C.J., Wagner W.D., Wissler R.W. A definition of the intima of human arteries and of its atherosclerosis-prone regions. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, AHA. Circulation 1992, 85:391-405.
54. Stary H.C., Chandler A.B., Glagov S., Guyton J.R., Insull W., Rosenfeld M.E., Schaffer S.A., Schwartz C.J., Wagner W.D., Wissler R.W. A definition of initial, fatty streak and intermediate lesions of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, AHA. Circulation 1994, 89:2462-2478.
55. Stary H.C., Chandler A.B., Dinsmore R.E., Fuster V., Glagov S., Insull W., Rosenfeld M.E., Schwartz C.J., Wagner W.D., Wissler R.W. A Definition of advanced types of atherosclerotic lesions and the histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, AHA. Circulation 1995, 92:1355-1374.
56. Steinman D.A. Image-based computational fluid dynamics modeling in realistic arterial geometries. Ann. Biomed. Eng. 2002, 30(4):483-497.
57. Stone G.W., Mintz G.S. Letter by Stone and Mintz regarding article, "unreliable assessment of necrotic core by virtual histology intravascular ultrasound in porcine coronary artery disease". Circ. Cardiovasc. Imaging 2010, 3(5):e4.
58. Stone P.H., Saito S., Takahashi S., Makita Y., Nakamura S., Kawasaki T., Takahashi A., Katsuki T., Nakamura S., Namiki A., Hirohata A., Matsumura T., Yamazaki S., Yokoi H., Tanaka S., Otsuji S., Yoshimachi F., Honye J., Harwood D., Reitman M., Coskun A.U., Papafaklis M.I., Feldman C.L., PREDICTION Investigators Prediction of progression of coronary artery disease and clinical outcomes using vascular profiling of endothelial shear stress and arterial plaque characteristics: the PREDICTION Study. Circulation 2012, 126(2):172-181.
59. Tang D. Modeling flow in healthy and stenosed arteries. Wiley Encyclopedia of Biomedical Engineering 2006, John Wiley & Sons, Inc., New Jersey, (Article 1525). M.A. Hoboekn (Ed.).
60. Tang D., Teng Z.Z., Canton G., Hatsukami T.S., Dong L., Huang X., Yuan C. Local critical stress correlates better than global maximum stress with plaque morphological features linked to atherosclerotic plaque vulnerability: an in vivo multi-patient study. Biomed. Eng. Online 2009, 8:15. 10.1186/1475-925X-8-15.
61. Tang D., Teng Z., Canton G., Yang C., Ferguson M., Huang X., Zheng J., Woodard P.K., Yuan C. Sites of rupture in human atherosclerotic carotid plaques are associated with high structural stresses: an in vivo MRI-based 3D fluid-structure interaction study. Stroke 2009, 40(10):3258-3263. (Featured article on MDlinx.com).
62. Tang D., Yang C., Kobayashi S., Zheng J., Woodard P.K., Teng Z., Billiar K., Bach R., Ku D.N. 3D MRI-based anisotropic FSI models with cyclic bending for human coronary atherosclerotic plaque mechanical analysis. J. Biomech. Eng. 2009, 131(6):061010.
63. Tang D., Yang C., Mondal S., Liu F., Canton G., Hatsukami T.S., Yuan C. A negative correlation between human carotid atherosclerotic plaque progression and plaque wall stress: in vivo MRI-based 2D/3D FSI models. J. Biomech. 2008, 41(4):727-736.
64. Tang D., Yang C., Zheng J., Woodard P.K., Saffitz J.E., Petruccelli J.D., Sicard G.A., Yuan C. Local maximal stress hypothesis and computational plaque vulnerability index for atherosclerotic plaque assessment. Ann. Biomed. Eng. 2005, 33(12):1789-1801.
65. Tang D., Yang C., Zheng J., Woodard P.K., Sicard G.A., Saffitz J.E., Yuan C. 3D MRI-based multi-component FSI models for atherosclerotic plaques, a 3-D FSI model. Ann. Biomed. Eng. 2004, 32(7):947-960.
66. Tearney G.J., Regar E., Akasaka T., Adriaenssens T., Barlis P., Bezerra H.G., Bouma B., Bruining N., Cho J.M., Chowdhary S., Costa M.A., de Silva R., Dijkstra J., Di Mario C., Dudek D., Falk E., Feldman M.D., Fitzgerald P., Garcia-Garcia H.M., Gonzalo N., Granada J.F., Guagliumi G., Holm N.R., Honda Y., Ikeno F., Kawasaki M., Kochman J., Koltowski L., Kubo T., Kume T., Kyono H., Lam C.C., Lamouche G., Lee D.P., Leon M.B., Maehara A., Manfrini O., Mintz G.S., Mizuno K., Morel M.A., Nadkarni S., Okura H., Otake H., Pietrasik A., Prati F., Räber L., Radu M.D., Rieber J., Riga M., Rollins A., Rosenberg M., Sirbu V., Serruys P.W., Shimada K., Shinke T., Shite J., Siegel E., Sonoda S., Suter M., Takarada S., Tanaka A., Terashima M., Thim T., Uemura S., Ughi G.J., van Beusekom H.M., van der Steen A.F., van Es G.A., van Soest G., Virmani R., Waxman S., Weissman N.J., Weisz G., International Working Group for Intravascular Optical Coherence Tomography (IWG-IVOCT) Consensus standards for acquisition, measurement, and reporting of intravascular optical coherence tomography studies: a report from the International Working Group for Intravascular Optical Coherence Tomography Standardization and Validation. J. Am. Coll. Cardiol. 2012, 59(12):1058-1072.
67. Teng Z., Canton G., Yuan C., Ferguson M., Yang C., Huang X., Zheng J., Woodard P.K., Tang D. 3D critical plaque wall stress is a better predictor of carotid plaque rupture sites than flow shear stress: an in vivo MRI-based 3D FSI study. J. Biomech. Eng. 2010, 132(3):031007.
68. Thim T., Hagensen M.K., Wallace-Bradley D., Granada J.F., Kaluza G.L., Drouet L., Paaske W.P., Bøtker H.E., Falk E. Unreliable assessment of necrotic core by virtual histology intravascular ultrasound in porcine coronary artery disease. Circ Cardiovasc. Imaging 2010, 3(4):384-391.
69. Underhill H.R., Hatsukami T.S., Fayad Z.A., Fuster V., Yuan C. MRI of carotid atherosclerosis: clinical implications and future directions. Nat. Rev. Cardiol. 2010, 7(3):165-173.
70. Vengrenyuk Y., Cardoso L., Weinbaum S. Micro-CT based analysis of a new paradigm for vulnerable plaque rupture: cellular microcalcifications in fibrous caps. Mol. Cell Biomech. 2008, 5(1):37-47.
71. Vengrenyuk Y., Carlier S., Xanthos S., Cardoso L., Ganatos P., Virmani R., Einav S., Gilchrist L., Weinbaum S. A hypothesis for vulnerable plaque rupture due to stress-induced debonding around cellular microcalcifications in thin fibrous caps. Proc. Natl. Acad. Sci. USA 2006, 103(40):14678-14683.
72. Virmani R., Kolodgie F.D., Burke A.P., Farb A., Schwartz S.M. Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol. 2000, 20(5):1262-1275.
73. Virmani R., Ladich E.R., Burke A.P., Kolodgie F.D. Histopathology of carotid atherosclerotic disease. Neurosurgery 2006, 59:S219-S227.
74. Wentzel J.J., Corti R., Fayad Z.A., Wisdom P., Macaluso F., Winkelman M.O., Fuster V., Badimon J.J. Does shear stress modulate both plaque progression and regression in the thoracic aorta? Human study using serial magnetic resonance imaging. J. Am. Coll. Cardiol. 2005, 45(6):846-854.
75. Williamson S.D., Lam Y., Younis H.F., Huang H., Patel S., Kaazempur-Mofrad M.R., Kamm R.D. On the sensitivity of wall stresses in diseased arteries to variable material properties. J. Biomech. Eng. 2003, 125:147-155.
76. Wu Z., Yang C., Tang D. In vivo serial MRI-based models and statistical methods to quantify sensitivity and specificity of mechanical predictors for carotid plaque rupture: location and beyond. J. Biomech. Eng. 2011, 133(6):064503.
77. Yang C., Bach R., Zheng J., El Naqa I., Woodard P.K., Teng Z.Z., Billiar K.L., Tang D. In vivo IVUS-based 3D fluid structure interaction models with cyclic bending and anisotropic vessel properties for human atherosclerotic coronary plaque mechanical analysis. IEEE Trans. Biomed. Eng. 2009, 56(10):2420-2428.
78. Yang C., Canton G., Yuan C., Ferguson M., Hatsukami T.S., Tang D. Advanced human carotid plaque progression correlates positively with flow shear stress: an in vivo MRI multi-patient 3D FSI study. J. Biomech. 2010, 43(13):2530-2538.
79. Yang C., Tang D., Yuan C., Hatsukami T.S., Zheng J., Woodard P.K. In vivo/ex vivo MRI-based 3D models with fluid-structure interactions for human atherosclerotic plaques compared with fluid/wall-only models. CMES: Comput. Model. Eng. Sci. 2007, 19(3):233-245.
80. Yuan C., Mitsumori L.M., Beach K.W., Maravilla K.R. Special review: carotid atherosclerotic plaque: noninvasive MR characterization and identification of vulnerable lesions. Radiology 2001, 221:285-299.
81. Yuan C., Mitsumori L.M., Ferguson M.S., Polissar N.L., Echelard D.E., Ortiz G., Small R., Davies J.W., Kerwin W.S., Hatsukami T.S. In vivo accuracy of multispectral MR imaging for identifying lipid-rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques. Circulation 2001, 104:2051-2056.
82. Zhang Y., Bajaj C., Sohn B.S. 3D finite element meshing from imaging data. Comput. Methods Appl. Mech. Eng. 2005, 194(48-49):5083-5106.
83. Zhang Y., Hughes T.J., Bajaj C.L. An automatic 3D mesh generation method for domains with multiple materials. Comput. Methods Appl. Mech. Eng. 2010, 199(5-8):405-415.