Biomechanical modeling and morphology analysis indicates plaque rupture due to mechanical failure unlikely in atherosclerosis-prone mice

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 304, Issue 3, 2013, Pages

  Campbell, Ian C ^a   Weiss, Daiana ^b   Suever, Jonathan D ^a   Virmani, Renu ^c   Veneziani, Alessandro ^a,d   Vito, Raymond P ^a   Oshinski, John N ^a,b   Taylor, W Robert ^a,b,e  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CVPATH INSTITUTE   (United States)

^d EMORY UNIVERSITY   (United States)

^e ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

Atherosclerosis; Biomechanics; Mouse model; Plaque rupture; Vulnerable plaque

Indexed keywords

ANGIOTENSIN II; APOLIPOPROTEIN E; LOW DENSITY LIPOPROTEIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROGENESIS; ATHEROSCLEROTIC PLAQUE; BIOMECHANICS; BRACHIOCEPHALIC TRUNK; CONTROLLED STUDY; LIPID DIET; MALE; MECHANICAL STRESS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

ANGIOTENSIN II; ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BIOMECHANICS; CALCINOSIS; COMPUTER SIMULATION; DIETARY FATS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; PHENOTYPE; PLAQUE, ATHEROSCLEROTIC; RECEPTORS, LDL; STRESS, MECHANICAL;

EID: 84873288114     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00620.2012     Document Type: Article

References (38)

1. Beattie D, Xu C, Vito R, Glagov S, Whang MC. Mechanical analysis of heterogeneous, atherosclerotic human aorta. J Biomech Eng 120: 602-607, 1998.
2. Bentzon JF, Falk E. Atherosclerotic lesions in mouse and man: is it the same disease? Curr Opin Lipidol 21: 434-440, 2010.
3. Bond AR, Jackson CL. The fat-fed apolipoprotein E knockout mouse brachiocephalic artery in the study of atherosclerotic plaque rupture. J Biomed Biotechnol 2011: 379069, 2011.
4. /~ mice-brief report. Arterioscler Thromb Vasc Biol 31: 1007-1010, 2011.
5. Calara F, Silvestre M, Casanada F, Yuan N, Napoli C, Palinski W. Spontaneous plaque rupture and secondary thrombosis in apolipoprotein E-deficient and LDL receptor-deficient mice. J Pathol 195: 257-263, 2001.
6. Cheng GC, Loree HM, Kamm RD, Fishbein MC, Lee RT. Distribution of circumferential stress in ruptured and stable atherosclerotic lesions. A structural analysis with histopathological correlation. Circulation 87: 1179-1187, 1993.
7. Chodorowski A, Mattsson U, Langille M, Hamarneh G. Color lesion boundary detection using live wire. In: Proceedings of SPIE Medical Imaging: Image Processing. Bellingham, WA: SPIE, 2005, vol. 5747, p. 1589-1596.
8. Daugherty A, Manning MW, Cassis LA. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest 105: 1605-1612, 2000.
9. Glagov S, Weisenberg E, Zarins CK, Stankunavicius R, Kolettis GJ. Compensatory enlargement of human atherosclerotic coronary arteries. N Engl J Med 316: 1371-1375, 1987.
10. Hallow KM, Taylor WR, Rachev A, Vito RP. Markers of inflammation collocate with increased wall stress in human coronary arterial plaque. Biomech Model Mechanobiol 8: 473-486, 2009.
11. Hansson GK, Heistad DD. Two views on plaque rupture. Arterioscler Thromb Vasc Biol 27: 697, 2007.
12. Hayenga HN, Trache A, Trzeciakowski J, Humphrey JD. Regional atherosclerotic plaque properties in ApoE-/- mice quantified by atomic force, immunofluorescence, and light microscopy. J Vasc Res 48: 495-504, 2011.
13. Holzapfel GA, Weizsacker HW. Biomechanical behavior of the arterial wall and its numerical characterization. Comput Biol Med 28: 377-392, 1998.
14. Humphrey JD, Rajagopal KR. A constrained mixture model for growth and remodeling of soft tissues. Math Mod Meth Appl S 12: 407-430, 2002.
15. Jackson CL. Defining and defending murine models of plaque rupture. Arterioscler Thromb Vasc Biol 27: 973-977, 2007.
16. Jawien J. The role of an experimental model of atherosclerosis: apoE-knockout mice in developing new drugs against atherogenesis. Curr Pharm Biotechnol; in press.
17. Jin SX, Shen LH, Nie P, Yuan W, Hu LH, Li DD, Chen XJ, Zhang XK, He B. Endogenous renovascular hypertension combined with low shear stress induces plaque rupture in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 32: 2372-2379, 2012.
18. Johnson J, Carson K, Williams H, Karanam S, Newby A, Angelini G, George S, Jackson C. Plaque rupture after short periods of fat feeding in the apolipoprotein E-knockout mouse: model characterization and effects of pravastatin treatment. Circulation 111: 1422-1430, 2005.
19. Li ZY, Howarth S, Trivedi RA, JMUKI, Graves MJ, Brown A, Wang L, Gillard JH. Stress analysis of carotid plaque rupture based on in vivo high resolution MRI. J Biomech 39: 2611-2622, 2006.
20. Maldonado N, Kelly-Arnold A, Vengrenyuk Y, Laudier D, Fallon JT, 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 303: H619-H628, 2012.
21. Ohayon J, Finet G, Gharib AM, Herzka DA, Tracqui P, Heroux J, Rioufol G, Kotys MS, Elagha A, Pettigrew RI. Necrotic core thickness and positive arterial remodeling index: emergent biomechanical factors for evaluating the risk of plaque rupture. Am J Physiol Heart Circ Physiol 295: H717-H727, 2008.
22. Ohayon J, Mesnier N, Broisat A, Toczek J, Riou L, Tracqui P. Elucidating atherosclerotic vulnerable plaque rupture by modeling cross substitution of ApoE-/- mouse and human plaque components stiffnesses. Biomech Model Mechanobiol 11: 801-813, 2012.
23. Rosenfeld ME, Polinsky P, Virmani R, Kauser K, Rubanyi G, Schwartz SM. Advanced atherosclerotic lesions in the innominate artery of the ApoE knockout mouse. Arterioscler Thromb Vasc Biol 20: 2587-2592, 2000.
24. Saraff K, Babamusta F, Cassis LA, Daugherty A. Aortic dissection precedes formation of aneurysms and atherosclerosis in angiotensin II-infused, apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 23: 1621-1626, 2003.
25. Sasaki T, Kuzuya M, Nakamura K, Cheng XW, Shibata T, Sato K, Iguchi A. A simple method of plaque rupture induction in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 26: 1304-1309, 2006.
26. Schwartz SM, Galis ZS, Rosenfeld ME, Falk E. Plaque rupture in humans and mice. Arterioscler Thromb Vasc Biol 27: 705-713, 2007.
27. Shoelson B. ClusterImg. Natick, MA: The MathWorks, 2006.
28. Suo J, Ferrara DE, Sorescu D, Guldberg RE, Taylor WR, Giddens DP. Hemodynamic shear stresses in mouse aortas: implications for atherogenesis. Arterioscler Thromb Vasc Biol 27: 346-351, 2007.
29. Tracqui P, Broisat A, Toczek J, Mesnier N, Ohayon J, Riou L. Mapping elasticity moduli of atherosclerotic plaque in situ via atomic force microscopy. J Struct Biol 174: 115-123, 2011.
30. van Ree JH, van den Broek WJ, Dahlmans VE, Groot PH, Vidgeon-Hart M, Frants RR, Wieringa B, Havekes LM, Hofker MH. Diet-induced hypercholesterolemia and atherosclerosis in heterozygous apolipoprotein E-deficient mice. Atherosclerosis 111: 25-37, 1994.
31. 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 103: 14678-14683, 2006.
32. Vengrenyuk Y, Kaplan TJ, Cardoso L, Randolph GJ, Weinbaum S. Computational stress analysis of atherosclerotic plaques in ApoE knockout mice. Ann Biomed Eng 38: 738-747, 2010.
33. Virmani R, Burke AP, Farb A, Kolodgie FD. Pathology of the vulnerable plaque. J Am Coll Cardiol 47: C13-18, 2006.
34. Weiss D, Kools JJ, Taylor WR. Angiotensin II-induced hypertension accelerates the development of atherosclerosis in apoE-deficient mice. Circulation 103: 448-454, 2001.
35. Weiss D, Sorescu D, Taylor WR. Angiotensin II and atherosclerosis. Am J Cardiol 87: 25C-32C, 2001.
36. Williamson SD, Lam Y, Younis HF, Huang H, Patel S, Kaazempur-Mofrad MR, Kamm RD. On the sensitivity of wall stresses in diseased arteries to variable material properties. J Biomech Eng 125: 147-155, 2003.
37. Yezzi AJ Jr, Prince JL. An Eulerian PDE approach for computing tissue thickness. IEEE Trans Med Imaging 22: 1332-1339, 2003.
38. Zadelaar S, Kleemann R, Verschuren L, de Vries-Van der Weij J, van der Hoorn J, Princen HM, Kooistra T. Mouse models for atherosclerosis and pharmaceutical modifiers. Arterioscler Thromb Vasc Biol 27: 1706-1721, 2007.