A robust rabbit model of human atherosclerosis and atherothrombosis

Journal of Lipid Research

Volumn 50, Issue 5, 2009, Pages 787-797

  Phinikaridou, Alkystis ^a   Hallock, Kevin J ^a   Qiao, Ye ^a   Hamilton, James A ^a,b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Boston University   (United States)

Author keywords

Lipids; Thrombosis; Vulnerable plaques

Indexed keywords

CHOLESTEROL; CHOLESTEROL ESTER; HISTAMINE; VIPER VENOM;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ATHEROSCLEROSIS; AORTA BALLOON; AORTA INJURY; ARTERY THROMBOSIS; ARTICLE; ATHEROSCLEROTIC PLAQUE; CHOLESTEROL DIET; CONTROLLED STUDY; HISTOPATHOLOGY; INFLAMMATION; MALE; MORPHOMETRICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RABBIT; THROMBOCYTE; THROMBUS; ANIMAL; AORTA; ATHEROSCLEROSIS; CORONARY ARTERY THROMBOSIS; DIET; DISEASE MODEL; HISTOLOGY; HUMAN; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; AORTA; ATHEROSCLEROSIS; CHOLESTEROL ESTERS; CORONARY THROMBOSIS; DIET; DISEASE MODELS, ANIMAL; HUMANS; MALE; RABBITS;

EID: 67649713425     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M800460-JLR200     Document Type: Article

References (59)

1. Davies, M. J. 1992. Anatomic features in victims of sudden coronary death. Coronary artery pathology. Circulation. 85: I19-I24.
2. Burke, A. P., A. Farb, G. T. Malcom, Y. H. Liang, J. Smialek, and R. Virmani. 1997. Coronary risk factors and plaque morphology in men with coronary disease who died suddenly. N. Engl. J. Med. 336: 1276-1282.
3. Boyle, J. J. 1997. Association of coronary plaque rupture and atherosclerotic inflammation. J. Pathol. 181: 93-99.
4. van der Wal, A. C., A. E. Becker, C. van der Loos, and P. Das. 1994. Site of intimal rupture or erosion of thrombosed coronary atherosclerotic plaques is characterized by an inflammatory process irrespective of the dominant plaque morphology. Circulation. 89: 36-44.
5. Moreno, P. R., K. R. Purushothaman, M. Sirol, A. P. Levy, and V. Fuster. 2006. Neovascularization in human atherosclerosis. Circulation. 113: 2245-2252.
6. Moreno, P. R., K. R. Purushothaman, V. Fuster, and W. N. O'Connor. 2002. Intimomedial interface damage and adventitial inflammation is increased beneath disrupted atherosclerosis in the aorta: implications for plaque vulnerability. Circulation. 105: 2504-2511.
7. Kolodgie, F. D., H. K. Gold, A. P. Burke, D. R. Fowler, H. S. Kruth, D. K. Weber, A. Farb, L. J. Guerrero, M. Hayase, R. Kutys, et al. 2003. Intraplaque hemorrhage and progression of coronary atheroma. N. Engl. J. Med.. 349: 2316-2325.
8. Pasterkamp, G., A. H. Schoneveld, D. J. Hijnen, D. P. de Kleijn, H. Teepen, A. C. van der Wal, and C. Borst. 2000. Atherosclerotic arterial remodeling and the localization of macrophages and matrix metalloproteases 1, 2 and 9 in the human coronary artery. Atherosclerosis. 150: 245-253.
9. Farb, A., A. P. Burke, A. L. Tang, T. Y. Liang, P. Mannan, J. Smialek, and R. Virmani. 1996. Coronary plaque erosion without rupture into a lipid core. A frequent cause of coronary thrombosis in sudden coronary death. Circulation. 93: 1354-1363.
10. Armstrong, M. L., and D. D. Heistad. 1990. Animal models of atherosclerosis. Atherosclerosis. 85: 15-23.
11. Drew, A. F. 2000. Atherosclerosis: Experimental Methods and Protocols. Humana Press, Totowa, NJ.
12. Lutgens, E., R. J. van Suylen, B. C. Faber, M. J. Gijbels, P. M. Eurlings, A. P. Bijnens, K. B. Cleutjens, S. Heeneman, and M. J. Daemen. 2003. Atherosclerotic plaque rupture: local or systemic process? Arterioscler. Thromb. Vasc. Biol. 23: 2123-2130.
13. Anitschkow, N., and S. Chalatow. 1913. Ueber experimentelle cholesterinsteatose und ihre bedeutung fur die entstehung einiger pathologischer prozesse. Centrbl. Allg. Pathol. Pathol. Anat. 24: 1-9.
14. Constantinides, P., N. Gutmann-Auersperg, and D. Hospes. 1958. Acceleration of intimal atherogenesis through prior medial injury. AMA Arch. Pathol. 66: 247-254.
15. Constantinides, P., J. Booth, and G. Carlson. 1960. Production of advanced cholesterol atherosclerosis in the rabbit. Arch. Pathol. 70: 80-92.
16. Constantinides, P., and R. N. Chakravarti. 1961. Rabbit arterial thrombosis production by systemic procedures. Arch. Pathol. 72: 197-208.
17. Vesselinovitch, D., R. W. Wissler, K. Fisher-Dzoga, R. Hughes, and L. Dubien. 1974. Regression of atherosclerosis in rabbits. I. Treatment with low-fat diet, hyperoxia and hypolipidemic agents. Atherosclerosis. 19: 259-275.
18. Weidinger, F. F., J. M. McLenachan, M. I. Cybulsky, J. T. Fallon, N. K. Hollenberg, J. P. Cooke, and P. Ganz. 1991. Hypercholesterolemia enhances macrophage recruitment and dysfunction of regenerated endothelium after balloon injury of the rabbit iliac artery. Circulation. 84: 755-767.
19. Abela, G. S., P. D. Picon, S. E. Friedl, O. C. Gebara, A. Miyamoto, M. Federman, G. H. Tofler, and J. E. Muller. 1995. Triggering of plaque disruption and arterial thrombosis in an atherosclerotic rabbit model. Circulation. 91: 776-784.
20. Johnstone, M. T., R. M. Botnar, A. S. Perez, R. Stewart, W. C. Quist, J. A. Hamilton, andW. J. Manning. 2001. In vivo magnetic resonance imaging of experimental thrombosis in a rabbit model. Arterioscler. Thromb. Vasc. Biol. 21: 1556-1560.
21. Botnar, R. M., A. Buecker, A. J. Wiethoff, E. C. Parsons, Jr., M. Katoh, G. Katsimaglis, R. M. Weisskoff, R. B. Lauffer, P. B. Graham, R. W. Gunther, et al. 2004. In vivo magnetic resonance imaging of coronary thrombosis using a fibrin-binding molecular magnetic resonance contrast agent. Circulation. 110: 1463-1466.
22. Wissler, R. W., and D. Vesselinovitch. 1974. Differences between Human and Animal Atherosclerosis. In Atherosclerosis III. G. Schettler and A. Weizel, editors. Springer, New York. 319-325.
23. Badimon, L. 2001. Atherosclerosis and thrombosis: lessons from animal models. Thromb. Haemost. 86: 356-365.
24. Rekhter, M. D., G. W. Hicks, D. W. Brammer, C. W. Work, J-S. Kim, D. Gordon, J. A. Keiser, and M. J. Ryan. 1998. Animal model that mimics atherosclerotic plaque rupture. Circ. Res. 83: 705-713.
25. Davey, M. G., and E. F. Luscher. 1965. Actions of some coagulant snake venoms on blood platelets. Nature. 207: 730-732.
26. Constantinides, P., and M. Robinson. 1969. Ultrastructural injury of arterial endothelium. Arch. Pathol. 88: 99-117.
27. Awano, K., M. Yokoyama, and H. Fukuzaki. 1989. Role of serotonin, histamine, and thromboxane A2 in platelet-induced contractions of coronary arteries and aortae from rabbits. J. Cardiovasc. Pharmacol. 13: 781-792.
28. Stary, H. C. 1989. Evolution and progression of atherosclerotic lesions in coronary arteries of children and young adults. Arteriosclerosis. 9: I19-I32.
29. Small, D. M. 1986. Handbook of Lipid Research: The Physical Chemistry of Lipids. From Alkanes to Phospholipids. D.J. Hanahan, editor. Plenum Press, New York and London.
30. Waugh, D. A., and D. M. Small. 1984. Identification and detection of in situ cellular and regional differences of lipid composition and class in lipid-rich tissue using hot stage polarizing light microscopy. Lab. Invest. 51: 702-714.
31. Stary, H. C., A. B. Chandler, R. E. Dinsmore, V. Fuster, S. Glagov, W. Insull, Jr., M. E. Rosenfeld, C. J. Schwartz, W. D. Wagner, and R. W. Wissler. 1995. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler. Thromb. Vasc. Biol. 15: 1512-1531.
32. Stary, H. C., A. B. Chandler, R. E. Dinsmore, V. Fuster, S. Glagov, W. Insull, Jr., M. E. Rosenfeld, C. J. Schwartz, W. D. Wagner, and R. W. Wissler. 1995. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation. 92: 1355-1374.
33. Burke, A. P., F. D. Kolodgie, A. Farb, D. Weber, and R. Virmani. 2002. Morphological predictors of arterial remodeling in coronary atherosclerosis. Circulation. 105: 297-303.
34. Pasterkamp, G., C. Borst, E. J. Gussenhoven, W. P. Mali, M. J. Post, S. H. The, J. A. Reekers, and F. G. van den Berg. 1995. Remodeling of de novo atherosclerotic lesions in femoral arteries: impact on mechanism of balloon angioplasty. J. Am. Coll. Cardiol. 26: 422-428.
35. Pasterkamp, G., A. H. Schoneveld, W. van Wolferen, B. Hillen, R. J. Clarijs, C. C. Haudenschild, and C. Borst. 1997. The impact of atherosclerotic arterial remodeling on percentage of luminal stenosis varies widely within the arterial system. A postmortem study. Arterioscler. Thromb. Vasc. Biol. 17: 3057-3063.
36. Shiomi, M., T. Ito, M. Hasegawa, K. Yoshida, and K. L. Gould. 2004. Novel insights into coronary lumen preservation during progression of coronary atherosclerosis in coronary atherosclerosis-prone rabbits. Coron. Artery Dis. 15: 419-426.
37. Constantinides, P. 1965. Experimental Atherosclerosis. Elsevier Publishing, New York.
38. Ross, R., and J. A. Glomset. 1976. The pathogenesis of atherosclerosis (first of two parts). N. Engl. J. Med. 295: 369-377.
39. Ross, R., and J. A. Glomset. 1976. The pathogenesis of atherosclerosis (second of two parts). N. Engl. J. Med. 295: 420-425.
40. Galis, Z. S., G. K. Sukhova, M. W. Lark, and P. Libby. 1994. Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J. Clin. Invest. 94: 2493-2503.
41. Virmani, R., A. P. Burke, A. Farb, and F. D. Kolodgie. 2006. Pathology of the vulnerable plaque. J. Am. Coll. Cardiol. 47: C13-C18.
42. Ma, H., K. S. Aziz, R. Huang, and G. S. Abela. 2006. Arterial wall cholesterol content is a predictor of development and severity of arterial thrombosis. J. Thromb. Thrombolysis. 22: 5-11.
43. Abela, G. S., and K. Aziz. 2006. Cholesterol crystals rupture biological membranes and human plaques during acute cardiovascular events-a novel insight into plaque rupture by scanning electron microscopy. Scanning. 28: 1-10.
44. Kumamoto, M., Y. Nakashima, and K. Sueishi. 1995. Intimal neovascularization in human coronary atherosclerosis: Its origin and pathophysiological significance. Hum. Pathol. 26: 450-456.
45. Moreno, P. R., K. R. Purushothaman, V. Fuster, D. Echeverri, H. Truszczynska, S. K. Sharma, J. J. Badimon, and W. N. O'Connor. 2004. Plaque neovascularization is increased in ruptured atherosclerotic lesions of human aorta: implications for plaque vulnerability. Circulation. 110: 2032-2038.
46. Glagov, S., E. Weisenberg, C. K. Zarins, R. Stankunavicius, and G. J. Kolettis. 1987. Compensatory enlargement of human atherosclerotic coronary arteries. N. Engl. J. Med. 316: 1371-1375.
47. Varnava, A. M., P. G. Mills, and M. J. Davies. 2002. Relationship between coronary artery remodeling and plaque vulnerability. Circulation. 105: 939-943.
48. Roberts, J. C. J., C. Moses, and R. H. Wilkins. 1959. Autopsy studies in atherosclerosis. I. Distribution and severity of atherosclerosis in patients dying without morphologic evidence of atherosclerotic catastrophe. Circulation. 20: 511-519.
49. Glagov, S., D. A. Rowley, and R. I. Kohut. 1961. Atherosclerosis of human aorta and its coronary and renal arteries. A consideration of some hemodynamic factors which may be related to the marked differences in atherosclerotic involvement of the coronary and renal arteries. Arch. Pathol. 72: 558-571.
50. Barakat, A. I., P. A. Uhthoff, and C. K. Colton. 1992. Topographical mapping of sites of enhanced HRP permeability in the normal rabbit aorta. J. Biomech. Eng. 114: 283-292.
51. Williams, J. K., G. K. Sukhova, D. M. Herrington, and P. Libby. 1998. Pravastatin has cholesterol-lowering independent effects on the artery wall of atherosclerotic monkeys. J. Am. Coll. Cardiol. 31: 684-691.
52. Aikawa, M., E. Rabkin, Y. Okada, S. J. Voglic, S. K. Clinton, C. E. Brinckerhoff, G. K. Sukhova, and P. Libby. 1998. Lipid lowering by diet reduces matrix metalloproteinase activity and increases collagen content of rabbit atheroma: a potential mechanism of lesion stabilization. Circulation. 97: 2433-2444.
53. Corti, R., J. I. Osende, J. T. Fallon, V. Fuster, G. Mizsei, H. Jneid, S. D. Wright, W. F. Chaplin, and J. J. Badimon. 2004. The selective peroxisomal proliferator-activated receptor-gamma agonist has an additive effect on plaque regression in combination with simvastatin in experimental atherosclerosis: in vivo study by high-resolution magnetic resonance imaging. J. Am. Coll. Cardiol. 43: 464-473.
54. Crisby, M., G. Nordin-Fredriksson, P. K. Shah, J. Yano, J. Zhu, and J. Nilsson. 2001. Pravastatin treatment increases collagen content and decreases lipid content, inflammation, metalloproteinases, and cell death in human carotid plaques: implications for plaque stabilization. Circulation. 103: 926-933.
55. Smilde, T. J., S. van Wissen, H. Wollersheim, M. D. Trip, J. J. Kastelein, and A. F. Stalenhoef. 2001. Effect of aggressive versus conventional lipid lowering on atherosclerosis progression in familial hypercholesterolaemia (ASAP): a prospective, randomised, double-blind trial. Lancet. 357: 577-581.
56. von Schacky, C., P. Angerer, W. Kothny, K. Theisen, and H. Mudra. 1999. The effect of dietary {omega}-3 fatty acids on coronary atherosclerosis: a randomized, double-blind, placebo-controlled trial. Ann. Intern. Med. 130: 554-562.
57. Johnstone, M. T., A. S. Perez, I. Nasser, R. Stewart, A. Vaidya, F. Al Ammary, B. Schmidt, G. Horowitz, J. Dolgoff, J. Hamilton, et al. 2004. Angiotensin receptor blockade with candesartan attenuates atherosclerosis, plaque disruption, and macrophage accumulation within the plaque in a rabbit model. Circulation. 110: 2060-2065.
58. Burke, A. P., F. D. Kolodgie, A. Farb, D. K. Weber, G. T. Malcom, J. Smialek, and R. Virmani. 2001. Healed plaque ruptures and sudden coronary death: evidence that subclinical rupture has a role in plaque progression. Circulation. 103: 934-940.
59. Qiao, Y., A. Farber, E. Semaan, and J. A. Hamilton. 2008. Images in cardiovascular medicine. Healing of an asymptomatic carotid plaque ulceration. Circulation. 118: e147-e148.