Skip to main content
Log in

3D MRI-Based Multicomponent FSI Models for Atherosclerotic Plaques

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

A three-dimensional (3D) MRI-based computational model with multicomponent plaque structure and fluid–structure interactions (FSI) is introduced to perform mechanical analysis for human atherosclerotic plaques and identify critical flow and stress/strain conditions which may be related to plaque rupture. Three-dimensional geometry of a human carotid plaque was reconstructed from 3D MR images and computational mesh was generated using Visualization Toolkit. Both the artery wall and the plaque components were assumed to be hyperelastic, isotropic, incompressible, and homogeneous. The flow was assumed to be laminar, Newtonian, viscous, and incompressible. The fully coupled fluid and structure models were solved by ADINA, a well-tested finite element package. Results from two-dimensional (2D) and 3D models, based on ex vivo MRI and histological images (HI), with different component sizes and plaque cap thickness, under different pressure and axial stretch conditions, were obtained and compared. Our results indicate that large lipid pools and thin plaque caps are associated with both extreme maximum (stretch) and minimum (compression when negative) stress/strain levels. Large cyclic stress/strain variations in the plaque under pulsating pressure were observed which may lead to artery fatigue and possible plaque rupture. Large-scale patient studies are needed to validate the computational findings for possible plaque vulnerability assessment and rupture predictions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  1. Bathe, K. J. Finite Element Procedures. New Jersey: Prentice-Hall, 1996.

    Google Scholar 

  2. Bathe, K. J., Ed. Theory and Modeling Guide, Vols. I&II. Watertown, MA: ADINA and ADINA-F, ADINA R&D, 2002.

    Google Scholar 

  3. Bathe, K. J., Ed. ADINA Verification Manual. Watertown, MA: ADINA R&D, 2002.

    Google Scholar 

  4. Beattie, D., C. Xu, R. P. Vito, S. Glagov, and M. C. Whang. Mechanical analysis of heterogeneous, atherosclerotic human aorta. J.Biomech.Eng. 120:602–607, 1998.

    Google Scholar 

  5. Berry, J. L., A. Santamarina, J. E. Moore, Jr., S. Roychowdhury, and W. D. Routh. Experimental and computational flow evaluation of coronary stents. Ann.Biomed.Eng. 28:386–398, 2000.

    Google Scholar 

  6. Bock, R. W., A. C. Gray-Weale, F. P. Mock, M. A. Stats, D. A. Robinson, L. Irwig, and R. J. Lusby. The natural history of asymptomatic carotid artery disease. J.Vasc.Surg. 17:160–171, 1993.

    Google Scholar 

  7. Boyle, J. J. Association of coronary plaque rupture and atherosclerotic inflammation. J.Pathol. 181:93–99, 1997.

    Google Scholar 

  8. Brossollet, L. J., and R. P. Vito. A new approach to mechanical testing and modeling of biological tissues, with application to blood vessels. J.Biomech.Eng. 118:433–439, 1996.

    Google Scholar 

  9. Burke, A. P., A. Farb, G. T. Malcom, Y. H. Liang, J. E. Smialek, and R. Virmani. Plaque rupture and sudden death related to exertion in men with coronary artery disease. JAMA 281:921–926, 1999.

    Google Scholar 

  10. Cai, J. M., T. S. Hatsukami, M. S. Ferguson, R. Small, N. L. Polissar, and C. Yuan. Classification of human carotid atherosclerotic lesions with in vivo multicontrast magnetic resonance imaging. Circulation 106:1368–1373, 2002.

    Google Scholar 

  11. Cheng, G. C., H. M. Loree, R. D. Kamm, M. C. Fishbein, and R. T. Lee. Distribution of circumferential stress in ruptured and stable atherosclerotic lesions, a structural analysis with histopathological correlation. Circulation 87:1179–1187, 1993.

    Google Scholar 

  12. Davies, M. J., and A. C. Thomas. Plaque fissuring-the cause of acute myocardial infarction, sudden ischemic death, and crecendo angina. Br.Heart J. 53:363–373, 1985.

    Google Scholar 

  13. Falk, E., P. K. Shah, and V. Fuster. Coronary plaque disruption. Circulation 92:657–671, 1995.

    Google Scholar 

  14. Fayad, Z. A., J. T. Fallon, M. Shinnar, S. Wehrli, H. M. Dansky, M. Poon, J. J. Badimon, S. A. Charlton, E. A. Fisher, J. L. Breslow, and V. Fuster. Noninvasive in vivo high-resolution MRI of atherosclerotic lesions in genetically engineered mice. Circulation 98:1541–1547, 1998.

    Google Scholar 

  15. Friedman, M. H. Arteriosclerosis research using vascular flow models: From 2-D branches to compliant replicas. J.Biomech.Eng. 115:595–601, 1993.

    Google Scholar 

  16. Fuster, V., B. Stein, J. A. Ambrose, L. Badimon, J. J. Badimon, and J. H. Chesebro. Atherosclerotic plaque rupture and throm-bosis, evolving concept. Circulation 82(Suppl. II):II-47–II-59, 1990.

    Google Scholar 

  17. Giddens, D. P., C. K. Zarins, and S. Glagov. Responses of arteries to near-wall fluid dynamic behavior. Appl.Mech.Rev. 43:S98–S102, 1990.

    Google Scholar 

  18. Giddens, D. P., C. K. Zarins, and S. Glagov. The role of fluid mechanics in the localization and detection of atherosclerosis. J.Biomech.Eng. 115:588–594, 1993.

    Google Scholar 

  19. Hafner, C. D. Minimizing the risks of carotid endarterectomy. J.Vasc.Surg. 1(3):392–397, 1984.

    Google Scholar 

  20. Hatsukami, T. S., R. Ross, N. L. Polissar, and C. Yuan. Visualization of fibrous cap thickness and rupture in human atherosclerotic carotid plaque in vivo with high-resolution magnetic resonance imaging. Circulation 102:959–964, 2000.

    Google Scholar 

  21. Huang, H., R. Virmani, H. Younis, A. P. Burke, R. D. Kamm, and R. T. Lee. The impact of calcification on the biomechanical stability of atherosclerotic plaques. Circulation 103:1051–1056, 2001.

    Google Scholar 

  22. Kaazempur-Mofrad, M. R., M. Bathe, H. Karcher, H. F. Younis, H. C. Seong, E. B. Shim, R. C. Chan, D. P. Hinton, A. G. Isasi, A. Upadhyaya, M. J. Powers, L. G. Griffith, and R. D. Kamm. Role of simulation in understanding biological systems. Comput.Struct. 81:715–726, 2003.

    Google Scholar 

  23. Kobayashi, S., D. Tsunoda, Y. Fukuzawa, H. Morikawa, D. Tang, and N. Ku. Flow and compression in arterial models of steno-sis with lipid core. Proceedings of 2003 ASME Summer Bio-engineering Conference, pp. 497–498, Miami, FL, June 25–29, 2003.

  24. Ku, D. N. Blood flowin arteries. Annu.Rev.Fluid Mech. 29:399–434, 1997.

    Google Scholar 

  25. Ku, D. N., D. P. Giddens, C. K. Zarins, and S. Glagov. Pulsatile flow and atherosclerosis in the human carotid bifurcation: Posi-tive correlation between plaque location and low and oscillating shear stress. Arteriosclerosis 5:293–302, 1985.

    Google Scholar 

  26. Ku, D. N., M. Zeigler, R. L. Binnes, and M. T. Stewart. A study of predicted and experimental wall collapse in models of highly stenotic arteries. In: Biofluid Mechanics: Blood Flow in Large Vessels, edited by Dieter Liepsch. New York: Springer-Verlag, 1990, pp. 409–416.

    Google Scholar 

  27. Lee, R. T., A. J. Grodzinsky, E. H. Frank, R. D. Kamm, and F. J. Schoen. Structure-dependent dynamic mechanical behavior of fibrous caps from human atherosclerotic plaques. Circulation 83(5):1764–1770, 1991.

    Google Scholar 

  28. Lee, R. T., and R. D. Kamm. Vascular mechanics for the cardiologist. J.Am.Coll.Cardiol. 23(6):1289–1295, 1994.

    Google Scholar 

  29. Lee, R. T., F. J. Schoen, H. M. Loree, M. W. Lark, and P. Libby. Circumferential stress and matrix metalloproteinase 1 in human coronary atherosclerosis. Implications for plaque rupture. Arterioscler.Thromb.Vasc.Biol. 16:1070–1073, 1996.

    Google Scholar 

  30. Lei, M., D. P. Giddens, S. A. Jones, F. Loth, and H. Bassiouny. Pulsatile flow in an end-to-side vascular graft model: Compar-ison of computations with experimental data. J.Biomech.Eng. 123:80–87, 2001.

    Google Scholar 

  31. Long, Q., X. Y. Xu, M. Bourne, and T. M. Griffith. Numerical study of blood flow in an anatomically realistic aorta–iliac bifur-cation generated from MRI data. Magn.Reson.Med. 43:565–576, 2000.

    Google Scholar 

  32. Long, Q., X. Y. Xu, K. V. Ramnarine, and P. Hoskins. Numerical investigation of physiologically realistic pulsatile flow through arterial stenosis. J.Biomech. 34:1229–1242, 2001.

    Google Scholar 

  33. Loree, H. M., R. D. Kamm, R. G. Stringfellow, and R. T. Lee. Effects of fibrous cap thickness on peak circumferential stress in model atherosclerotic vessels. Circ.Res. 71:850–858, 1992.

    Google Scholar 

  34. Loree, H. M., B. J. Tobias, L. J. Gibson, R. D. Kamm, D. M. Small, and R. T. Lee. Mechanical properties of model atheroscle-rotic lesion lipid pools. Arterioscler.Thromb. 14(2):230–234, 1994.

    Google Scholar 

  35. McCord, B. N. Fatigue of Atherosclerotic Plaque. PhD Thesis, Georgia Institute of Technology, 1992.

  36. Pedersen, P. C., J. Chakareski, and R. Lara-Montalvo. Ultra-sound characterization of arterial wall structures based on inte-grated backscatter profiles. Proceedings for the 2003 SPIE Med-ical Imaging Symposium, San Diego, CA, 2003, pp. 115–126.

  37. Perktold, K., G. Rappotsch, M. Hofer, G. Karner, and K. Andlinger. Effects of vessel wall compliance on flow and stress patterns in arterial bends and bifurcations. Adv.Bioeng.BED 33:329–330, 1996.

    Google Scholar 

  38. Peskin, C. S. Mathematical Aspects of Heart Physiology. Lecture notes of Courant Institute of Mathematical Sciences, New York, 1975.

  39. Peskin, C. S. Numerical analysis of blood flow in the heart. J.Comp.Phys. 25:220–252, 1977.

    Google Scholar 

  40. Peskin, C. S. A three-dimensional computational method for blood flow in the heart. J.Comp.Phys. 81:372–405, 1989.

    Google Scholar 

  41. Ravn, H. B., and E. Falk. Histopathology of plaque rupture. Cardiol.Clin. 17:263–270, 1999.

    Google Scholar 

  42. Schroeder, W., K. Martin, and B. Lorensen. The Visualization Toolkit, An Object-Oriented Approach To 3D Graphics, 2nd ed. New Jersey: Prentice-Hall, 1998.

    Google Scholar 

  43. Steinman, D. A., J. B. Thomas, H. M. Ladak, J. S. Milner, B. K. Rutt, and J. D. Spence. Reconstruction of carotid bifurcation hemodynamics and wall thickness using computational fluid dynamics and MRI. Magn.Reson.Med. 47(1):149–159, 2002.

    Google Scholar 

  44. Tang, D., C. Yang, S. Kobayashi, and D. N. Ku. Steady flow and wall compression in stenotic arteries: A 3-D thick-wall model with fluid–wall interactions. J.Biomech.Eng. 123:548–557, 2001.

    Google Scholar 

  45. Tang, D., C. Yang, S. Kobayashi, and D. N. Ku. Simulating cyclic artery compression using a 3-D unsteady model with fluid– structure interactions. Comput.Struct. 80:1651–1665, 2002.

    Google Scholar 

  46. Tang, D., C. S. Kobayashi, and D. N. Ku. Effect of a lipid pool on stress/strain distributions in stenotic arteries: 3D FSI models. J.Biomech.Eng., in press.

  47. Tang, D., C. Yang, H. F. Walker, S. Kobayashi, J. Zheng, and D. N. Ku. 2-D and 3-D multi-physics models for flow and non-linear stress/strain analysis of stenotic arteries with lipid cores. In: Computational Fluid and Solid Mechanics, edited by K. J. Bathe, Vol. 2. New York: Elsevier, 2003, pp. 1829–1832.

    Google Scholar 

  48. Tang, D., C. Yang, J. Zheng, and R. P. Vito. Effects of steno-sis asymmetry on blood flow and artery compression: A three-dimensional fluid–structure interaction model. Ann.Biomed.Eng. 31:1182–1193, 2003.

    Google Scholar 

  49. Toussaint, J. F., G. M. LaMuraglia, J. F. Southern, V. Fuster, and H. L. Kantor. MRimages of lipid, fibrous, calcified, hemorrhagic and thrombotic components of human atherosclerosis in vivo. Circulation 94:932–938, 1996.

    Google Scholar 

  50. van der Wal, A. C., A. E. Becker, C. M. van der Loos, and P. K. Das. Site of intimal rupture or erosion of thrombosed coro-nary atherosclerotic plaques is characterized by an inflammatory process irrespective of the dominant plaque morphology. Circulation 89:36–44, 1994.

    Google Scholar 

  51. Williamson, S. D., Y. Lam, H. F. Younis, H. Huang, S. Patel, M. R. Kaazempur-Mofrad, and R. D. Kamm. On the sensitivity of wall stresses in diseased arteries to variable material properties. J.Biomech.Eng. 125:147–155, 2003.

    Google Scholar 

  52. Yuan, C., B. W. Beath, L. H. Smith, and T. S. Hatsukami. Measurement of atherosclerotic carotid plaque size in vivo using high resolution Magnetic Resonance Imaging. Circulation 98:2666–2671, 1998.

    Google Scholar 

  53. Yuan, C., T. S. Hatsukami, and K. D. O'Brien. High resolution magnetic resonance imaging of normal and atherosclerotic human coronary arteries ex vivo: Discrimination of plaque tissue components. J.Med.Investig. 49(16):491–499, 2001.

    Google Scholar 

  54. Yuan, C., W. S. Kerwin, M. S. Ferguson, N. Polissar, S. X. Zhang, J. M. Cai, and T. S. Hatsukami. Contrast enhanced high resolu-tion MRI for atherosclerotic carotid artery tissue characterization. JMRI 15:62–67, 2002.

    Google Scholar 

  55. Yuan, C., L. M. Mitsumori, K. W. Beach, and K. R. Maravilla. Special review: Carotid atherosclerotic plaque: Noninvasive MR characterization and identification of vulnerable lesions. Radiology 221:285–299, 2001.

    Google Scholar 

  56. Yuan, C., L. M. Mitsumori, M. S. Ferguson, N. L. Polissar, D. E. Echelard, G. Ortiz, R. Small, J. W. Davies, W. S. Kerwin, and T. S. Hatsukami. In vivo accuracy of multispectral MR imaging for identifying lipid-rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques. Circulation 104:2051–2056, 2001.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tang, D., Yang, C., Zheng, J. et al. 3D MRI-Based Multicomponent FSI Models for Atherosclerotic Plaques. Annals of Biomedical Engineering 32, 947–960 (2004). https://doi.org/10.1023/B:ABME.0000032457.10191.e0

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:ABME.0000032457.10191.e0

Navigation