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Protein & Cell

ISSN 1674-800X

ISSN 1674-8018(Online)

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Prot Cell    0, Vol. Issue () : 189-201    https://doi.org/10.1007/s13238-011-1016-3      PMID: 21468891
REVIEW
Animal models for the atherosclerosis research: a review
Xiangdong Li(), Yuanwu Liu, Hua Zhang, Liming Ren, Qiuyan Li, Ning Li()
State Key Laboratory of Agrobiotechnology, China Agricultural University, Beijing 100193, China
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Abstract

Atherosclerosis is a leading cause of death worldwide, and its mechanisms are still unclear. However, various animal models have significantly advanced our understanding of the mechanisms involved in atherosclerosis and have allowed the evaluation of therapeutic options. The aim of this paper is to review those animal models (i.e., rabbits, mice, rats, guinea pigs, hamsters, avian, carnivores, swine, and, non-human primates) that have been used to study atherosclerosis. Though there is no single perfect animal model that completely replicates the stages of human atherosclerosis, cholesterol feeding and mechanical endothelial injury are two common features shared by most models of atherosclerosis. Further, with the development of genetically modified animals, these models are significantly broadening our understanding of the pathogenesis of atherosclerosis.

Keywords animal model      atherosclerosis     
Corresponding Author(s): Li Xiangdong,Email:xiangdongli@cau.edu.cn (X. Li); Li Ning,Email:ninglcau@cau.edu.cn (N. Li)   
Issue Date: 01 March 2011
 Cite this article:   
Xiangdong Li,Yuanwu Liu,Hua Zhang, et al. Animal models for the atherosclerosis research: a review[J]. Prot Cell, 0, (): 189-201.
 URL:  
https://academic.hep.com.cn/pac/EN/10.1007/s13238-011-1016-3
https://academic.hep.com.cn/pac/EN/Y0/V/I/189
Fig.1  Pathology of atherosclerotic disease.
Classification of the six types of artery wall lesion, modified from Stary et al. (1995).
Fig.1  Pathology of atherosclerotic disease.
Classification of the six types of artery wall lesion, modified from Stary et al. (1995).
Fig.2  Comparisons between lipoprotein cholesterol distribution between several animal models and humans (; ; ). HDL, high-density lipoprotein; LDL, low-density lipoprotein; VLOL, very low-density lipoprotein.
Fig.2  Comparisons between lipoprotein cholesterol distribution between several animal models and humans (; ; ). HDL, high-density lipoprotein; LDL, low-density lipoprotein; VLOL, very low-density lipoprotein.
AnimalsAdvantagesDisadvantages
RabbitsNaturally LDL-receptor-deficient strain, naturally hypertriglyceridemic strain, good size, easy to keep and handle, known to many investigators, good response to dietary cholesterol, and availability of transgenic linesLesion locations less similar to those in man, the majority of circulating cholesterol is HDL, very high plasma cholesterol needed to induce atherosclerosis, no advanced lesions, hepatic lipase deficient, no spontaneous atherosclerosis, and cholesterol storage syndrome on cholesterol feeding
MiceWell-defined genetics, easy breeding, short generation time, inbred availability, easy handling and housing, and availability of several transgenic linesHighly resistant to atherogenesis, high HDL, no CETP, and difficulties in frequent blood sampling and dissection of medium/small-size vessels
RatsEasy handling and housing, several strains of rats with heritable hyperlipidemia (some of which are associated with atherogenesis), and transgenic rats overexpressing human CETP produce atherosclerosisHighly resistant to atherogenesis, high HDL, and no CETP
HamstersHave plasma CETP, could develop hypercholesterolemia and early atherosclerosis of fatty streaks and complex plaques after various duration of diet induction, and easy to handleThe inconsistent and unrepeatable results of aortic lesions
Guinea pigsThe majority of circulating cholesterol is LDL, possess CETP, lipoprotein lipase, and LCAT, resignficant atherogenic inflammation with increased aortic cytokinesNo advanced atherosclerotic lesions, antibodies involved in atherogenic inflammation are rarely available, and not a good surgical model
AvianAtherosclerosis-susceptible strains, location and progress of lesions similar to those in humans, low cost and easy handling, sufficient size, good response to dietary cholesterol, short generation time, and relatively long life spanNon-mammalian, lack of apoE, B48, and chylomicron formation, viral infection seen associated with atherosclerosis, and considerable changes in lipoprotein metabolism during egg-laying
DogsSome physiological/anatomical similarities to humans, well-characterized lipoprotein profile, hematologic and metabolic similarities to humans, extensive literature on blood pressure-altering drugs and drug interactions, and prosthetic devicesAtherosclerosis-resistant species, high HDL, expensive, no advanced atherosclerotic lesions, poor response to dietary cholesterol, ethical concerns, large amount of experimental agents needed, and spontaneous bacteremias and viral infections
SwineSome physiological/anatomical similarities to humans, spontaneous atherosclerosis particularly in abdominal aorta, availability of miniature pigs, natural lipoprotein mutant strains, advanced vulnerable carotid atherosclerotic plaques, and surgical study of carotid artery stent techniquesHigh cholesterol diet (4%–5% w/w), longer time diet induction, very low baseline cholesterol level, difficulties in care, and high maintenance cost
Non-human primatesThe closest species to humans, some strains respond well to dietary cholesterol, spontaneous early stage atherosclerosis in some strains, familial LDL receptor de?ciency, and surgical angioplasty studySerious chronic kidney disease is the outcome of atherosclerosis research (resulting in high risk of premature death), variations in site of lesions, limited availability, expensive and difficult to house and handle, and ethical concerns
Tab.1  Advantages and disadvantages of certain animal species in human atherosclerosis research
1 Abela, G.S., Picon, P.D., Friedl, S.E., Gebara, O.C., Miyamoto, A., Federman, M., Tofler, G.H., and Muller, J.E. (1995). Triggering of plaque disruption and arterial thrombosis in an atherosclerotic rabbit model. Circulation 91, 776-784 .
pmid:7828306
2 Adams, C.W.M., Miller, N.E., Morgan, R.S., and Rao, S.N. (1982). Lipoprotein levels and tissue lipids in fatty-fibrous atherosclerosis induced in rabbits by two years’ cholesterol feeding at a low level. Atherosclerosis 44, 1-8 .
pmid:7115472
3 Aggarwal, D., Fernandez, M.L., and Soliman, G.A. (2006). Rapamycin, an mTOR inhibitor, disrupts triglyceride metabolism in guinea pigs. Metabolism 55, 794-802 .
pmid:16713440
4 Aggarwal, D., West, K.L., Zern, T.L., Shrestha, S., Vergara-Jimenez, M., and Fernandez, M.L. (2005). JTT-130, a microsomal triglyceride transfer protein (MTP) inhibitor lowers plasma triglycerides and LDL cholesterol concentrations without increasing hepatic triglycerides in guinea pigs. BMC Cardiovasc Disord 5, 30.
pmid:16188040
5 Aikawa, M., Rabkin, E., Voglic, S.J., Shing, H., Nagai, R., Schoen, F.J., and Libby, P. (1998). Lipid lowering promotes accumulation of mature smooth muscle cells expressing smooth muscle myosin heavy chain isoforms in rabbit atheroma. Circ Res 83, 1015-1026 .
pmid:9815149
6 Aliev, G., and Burnstock, G. (1998). Watanabe rabbits with heritable hypercholesterolaemia: a model of atherosclerosis. Histol Histopathol 13, 797-817 .
pmid:9690137
7 Anitschkow, N., and Chalatow, S. (1913). Uber experimentelle Cholesterinsteatose und ihre Bedeutung fur die Entstehung einiger pathologischer Prozesse. Centrbl Allg Pathol Pathol Anat 24, 1-9 .
8 Armstrong, M.L., and Heistad, D.D. (1990). Animal models of atherosclerosis. Atherosclerosis 85, 15-23 .
pmid:2282105
9 Armstrong, M.L., and Warner, E.D. (1971). Morphology and distribution of diet-induced atherosclerosis in rhesus monkeys. Arch Pathol 92, 395-401 .
pmid:5001046
10 Association, A.H. (2010). Heart Disease and Stroke Statistics-2009 Update (All Charts) [Accessed August 17, 2009]. Available at: http://wwwamericanheartorg/presenterjhtml?identifier=3018163.
11 Barakat, H.A., and St Clair, R.W. (1985). Characterization of plasma lipoproteins of grain- and cholesterol-fed White Carneau and Show Racer pigeons. J Lipid Res 26, 1252-1268 .
pmid:4067419
12 Bell, F.P., and Gerrity, R.G. (1992). Evidence for an altered lipid metabolic state in circulating blood monocytes under conditions of hyperlipemia in swine and its implications in arterial lipid metabolism. Arterioscler Thromb 12, 155-162 .
pmid:1543690
13 Bocan, T.M.A., Mueller, S.B., Mazur, M.J., Uhlendorf, P.D., Brown, E.Q., and Kieft, K.A. (1993). The relationship between the degree of dietary-induced hypercholesterolemia in the rabbit and atherosclerotic lesion formation. Atherosclerosis 102, 9-22 .
pmid:8257456
14 Bowman, T.A., and Hughes, H.C. (1984). Swine as an in vivo model for electrophysiologic evaluation of cardiac pacing parameters. Pacing Clin Electrophysiol 7, 187-194 .
pmid:6200843
15 Breslow, J.L. (1996). Mouse models of atherosclerosis. Science 272, 685-688 .
pmid:8614828
16 Brousseau, M.E., and Hoeg, J.M. (1999). Transgenic rabbits as models for atherosclerosis research. J Lipid Res 40, 365-375 .
pmid:10064724
17 Butkus, A., Ehrhart, L.A., and McCullagh, K.G. (1976). Plasma and aortic lipids in experimental canine atherosclerosis. Exp Mol Pathol 25, 152-162 .
pmid:992012
18 Chinellato, A., Ragazzi, E., Petrelli, L., Paro, M., Mironov, A., and Aliev, G. (1994). Effect of cholesterol-supplemented diet in heritable hyperlipidemic Yoshida rats: functional and morphological characterization of thoracic aorta. Atherosclerosis 106, 51-63 .
pmid:8018107
19 Chue, W.L., Campbell, G.R., Caplice, N., Muhammed, A., Berry, C.L., Thomas, A.C., Bennett, M.B., and Campbell, J.H. (2004). Dog peritoneal and pleural cavities as bioreactors to grow autologous vascular grafts. J Vasc Surg 39, 859-867 .
pmid:15071455
20 Clarkson, T.B., Lehner, N.D., Bullock, B.C., Lofland, H.B., and Wagner, W.D. (1976). Atherosclerosis in new world monkeys. Primates Med 9, 90-144 .
pmid:813212
21 Clarkson, T.B., Prichard, R.W., Netsky, M.G., and Lofland, H.B. (1959). Atherosclerosis in pigeons; its spontaneous occurrence and resemblance to human atherosclerosis. AMA Arch Pathol 68, 143-147 .
pmid:13669834
22 Cornhill, J.F., and Roach, M.R. (1974). Quantitative method for the evaluation of atherosclerotic lesions. Atherosclerosis 20, 131-136 .
pmid:4142392
23 Cornhill, J.F., and Roach, M.R. (1976). A quantitative study of the localization of atherosclerotic lesions in the rabbit aorta. Atherosclerosis 23, 489-501 .
pmid:57782
24 Dauber, D., Horlick, L., and Katz, L.N. (1949). The role of desiccated thyroid and potassium iodide in the cholesterol-induced atherosclerosis of the chicken. Am Heart J 38, 25-33 .
pmid:18153125
25 Dauber, D.V. (1944). Spontaneous atherosclerosis in chickens. AMA Arch Pathol 38, 46-51 .
26 David, T.E., Armstrong, S., Maganti, M., Butany, J., Feindel, C.M., and Bos, J. (2009). Postimplantation morphologic changes of glutaraldehyde-fixed porcine aortic roots and risk of aneurysm and rupture. J Thorac Cardiovasc Surg 137, 94-100 .
pmid:19154910
27 David, T.E., Puschmann, R., Ivanov, J., Bos, J., Armstrong, S., Feindel, C.M., and Scully, H.E. (1998). Aortic valve replacement with stentless and stented porcine valves: a case-match study. J Thorac Cardiovasc Surg 116, 236-241 .
pmid:9699575
28 Davies, M.K., and Hollman, A. (1998). Atherosclerosis and myocardial infarction. Heart 79, 218.
pmid:9602649
29 Dillard, A., Matthan, N.R., and Lichtenstein, A.H. (2010). Use of hamster as a model to study diet-induced atherosclerosis. Nutr Metab (Lond) 7, 89.
pmid:21143982
30 Duverger, N., Kruth, H., Emmanuel, F., Caillaud, J.M., Viglietta, C., Castro, G., Tailleux, A., Fievet, C., Fruchart, J.C., Houdebine, L.M., (1996). Inhibition of atherosclerosis development in cholesterol-fed human apolipoprotein A-I-transgenic rabbits. Circulation 94, 713-717 .
pmid:8772693
31 El-Khatib, F.H., Jiang, J., Gerrity, R.G., and Damiano, E.R. (2007). Pharmacodynamics and stability of subcutaneously infused glucagon in a type 1 diabetic Swine model in vivo. Diabetes Technol Ther 9, 135-144 .
pmid:17425438
32 Fabricant, C.G., Fabricant, J., Litrenta, M.M., and Minick, C.R. (1978). Virus-induced atherosclerosis. J Exp Med 148, 335-340 .
pmid:209124
33 Fan, J., McCormick, S.P.A., Krauss, R.M., Taylor, S., Quan, R., Taylor, J.M., and Young, S.G. (1995). Overexpression of human apolipoprotein B-100 in transgenic rabbits results in increased levels of LDL and decreased levels of HDL. Arterioscler Thromb Vasc Biol 15, 1889-1899 .
pmid:7583569
34 Fan, J., Shimoyamada, H., Sun, H., Marcovina, S., Honda, K., and Watanabe, T. (2001a). Transgenic rabbits expressing human apolipoprotein(a) develop more extensive atherosclerotic lesions in response to a cholesterol-rich diet. Arterioscler Thromb Vasc Biol 21, 88-94 .
pmid:11145938
35 Fan, J., Unoki, H., Kojima, N., Sun, H., Shimoyamada, H., Deng, H., Okazaki, M., Shikama, H., Yamada, N., and Watanabe, T. (2001b). Overexpression of lipoprotein lipase in transgenic rabbits inhibits diet-induced hypercholesterolemia and atherosclerosis. J Biol Chem 276, 40071-40079 .
pmid:11477088
36 Fan, J., Wang, J., Bensadoun, A., Lauer, S.J., Dang, Q., Mahley, R.W., and Taylor, J.M. (1994). Overexpression of hepatic lipase in transgenic rabbits leads to a marked reduction of plasma high density lipoproteins and intermediate density lipoproteins. Proc Natl Acad Sci U S A 91, 8724-8728 .
pmid:8078949
37 Fernandez, M.L., and Volek, J.S. (2006). Guinea pigs: a suitable animal model to study lipoprotein metabolism, atherosclerosis and inflammation. Nutr Metab (Lond) 3, 17.
pmid:16566831
38 Fernandez, M.L., Wilson, T.A., Conde, K., Vergara-Jimenez, M., and Nicolosi, R.J. (1999). Hamsters and guinea pigs differ in their plasma lipoprotein cholesterol distribution when fed diets varying in animal protein, soluble fiber, or cholesterol content. J Nutr 129, 1323-1332 .
pmid:10395594
39 Finking, G., and Hanke, H. (1997). Nikolaj Nikolajewitsch Anitschkow (1885-1964) established the cholesterol-fed rabbit as a model for atherosclerosis research. Atherosclerosis 135, 1-7 .
pmid:9395267
40 Fong, I.W. (2000). Emerging relations between infectious diseases and coronary artery disease and atherosclerosis. CMAJ 163, 49-56 .
pmid:10920732
41 Geary, R.L., Williams, J.K., Golden, D., Brown, D.G., Benjamin, M.E., and Adams, M.R. (1996). Time course of cellular proliferation, intimal hyperplasia, and remodeling following angioplasty in monkeys with established atherosclerosis. A nonhuman primate model of restenosis. Arterioscler Thromb Vasc Biol 16, 34-43 .
pmid:8548423
42 Gerrity, R.G. (1984). Atherogenesis in the swine Evans blue model. Vasa 13, 292-297 .
pmid:6516558
43 Gerrity, R.G., Goss, J.A., and Soby, L. (1985). Control of monocyte recruitment by chemotactic factor(s) in lesion-prone areas of swine aorta. Arteriosclerosis 5, 55-66 .
pmid:3966908
44 Gerrity, R.G., Naito, H.K., Richardson, M., and Schwartz, C.J. (1979). Dietary induced atherogenesis in swine. Morphology of the intima in prelesion stages. Am J Pathol 95, 775-792 .
pmid:453335
45 Gerrity, R.G., Natarajan, R., Nadler, J.L., and Kimsey, T. (2001). Diabetes-induced accelerated atherosclerosis in swine. Diabetes 50, 1654-1665 .
pmid:11423488
46 Ginzinger, D.G., Wilson, J.E., Redenbach, D., Lewis, M.E., Clee, S.M., Excoffon, K.J., Rogers, Q.R., Hayden, M.R., and McManus, B.M. (1997). Diet-induced atherosclerosis in the domestic cat. Lab Invest 77, 409-419 .
pmid:9389784
47 Glass, C.K., and Witztum, J.L. (2001). Atherosclerosis. the road ahead. Cell 104, 503-516 .
pmid:11239408
48 Go, A.S., Chertow, G.M., Fan, D., McCulloch, C.E., and Hsu, C.Y. (2004). Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med 351, 1296-1305 .
pmid:15385656
49 Go, A.S., Yang, J., Ackerson, L.M., Lepper, K., Robbins, S., Massie, B.M., and Shlipak, M.G. (2006). Hemoglobin level, chronic kidney disease, and the risks of death and hospitalization in adults with chronic heart failure: the Anemia in Chronic Heart Failure: Outcomes and Resource Utilization (ANCHOR) Study. Circulation 113, 2713-2723 .
pmid:16754803
50 Grove, D., and Pownall, H.J. (1991). Comparative specificity of plasma lecithin:cholesterol acyltransferase from ten animal species. Lipids 26, 416-420 .
pmid:1881237
51 Grundy, S.M., Howard, B., Smith, S. Jr, Eckel, R., Redberg, R., and Bonow, R.O. (2002). Prevention Conference VI: Diabetes and Cardiovascular Disease: executive summary: conference proceeding for healthcare professionals from a special writing group of the American Heart Association. Circulation 105, 2231-2239 .
pmid:11994261
52 Hajjar, D.P., Fabricant, C.G., Minick, C.R., and Fabricant, J. (1986). Virus-induced atherosclerosis. Herpesvirus infection alters aortic cholesterol metabolism and accumulation. Am J Pathol 122, 62-70 .
pmid:2934987
53 Hammad, S.M., Siegel, H.S., and Marks, H.L. (1998). Total cholesterol, total triglycerides, and cholesterol distribution among lipoproteins as predictors of atherosclerosis in selected lines of Japanese quail. Comp Biochem Physiol A Mol Integr Physiol 119, 485-492 .
pmid:11248992
54 Hancock, J.B., Forshaw, P.L., and Kaye, M.P. (1980). Gore-Tex (polytetrafluoroethylene) in canine coronary artery bypass. J Thorac Cardiovasc Surg 80, 94-101 .
pmid:6966722
55 Hansson, G.K. (2005). Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 352, 1685-1695 .
pmid:15843671
56 Hansson, G.K. (2009). Atherosclerosis—an immune disease: The Anitschkov Lecture 2007. Atherosclerosis 202, 2-10 .
pmid:18951547
57 Herrera, V.L.M., Makrides, S.C., Xie, H.X., Adari, H., Krauss, R.M., Ryan, U.S., and Ruiz-Opazo, N. (1999). Spontaneous combined hyperlipidemia, coronary heart disease and decreased survival in Dahl salt-sensitive hypertensive rats transgenic for human cholesteryl ester transfer protein. Nat Med 5, 1383-1389 .
pmid:10581080
58 Hoeg, J.M., Santamarina-Fojo, S., Bérard, A.M., Cornhill, J.F., Herderick, E.E., Feldman, S.H., Haudenschild, C.C., Vaisman, B.L., Hoyt, R.F. Jr, Demosky, S.J. Jr, (1996). Overexpression of lecithin:cholesterol acyltransferase in transgenic rabbits prevents diet-induced atherosclerosis. Proc Natl Acad Sci U S A 93, 11448-11453 .
pmid:8876155
59 Hoeg, J.M., Vaisman, B.L., Demosky, S.J. Jr, Santamarina-Fojo, S., Brewer, H.B. Jr, Remaley, A.T., Hoyt, R.F., and Feldman, S. (1993). Development of transgenic Watanabe Heritable Hyperlipidemic rabbits expressing human apolipoprotein A-I. Circulation 88, 1-2 .
60 Holvoet, P., Theilmeier, G., Shivalkar, B., Flameng, W., and Collen, D. (1998). LDL hypercholesterolemia is associated with accumulation of oxidized LDL, atherosclerotic plaque growth, and compensatory vessel enlargement in coronary arteries of miniature pigs. Arterioscler Thromb Vasc Biol 18, 415-422 .
pmid:9514410
61 Hughes, H.C. (1986). Swine in cardiovascular research. Lab Anim Sci 36, 348-350 .
pmid:3534437
62 Hunt, C.E., and Duncan, L.A. (1985). Hyperlipoproteinaemia and atherosclerosis in rabbits fed low-level cholesterol and lecithin. Br J Exp Pathol 66, 35-46 .
pmid:3970829
63 Ignatowski, A.C. (1908). Influence of animal food on the organism of rabbits. Izv Imp Voyenno-Med Akad Peter 16, 154-173 .
64 Ishii, A., Vi?uela, F., Murayama, Y., Yuki, I., Nien, Y.L., Yeh, D.T., and Vinters, H.V. (2006). Swine model of carotid artery atherosclerosis: experimental induction by surgical partial ligation and dietary hypercholesterolemia. AJNR Am J Neuroradiol 27, 1893-1899 .
pmid:17032861
65 Johnstone, M.T., Botnar, R.M., Perez, A.S., Stewart, R., Quist, W.C., Hamilton, J.A., and Manning, W.J. (2001). In vivo magnetic resonance imaging of experimental thrombosis in a rabbit model. Arterioscler Thromb Vasc Biol 21, 1556-1560 .
pmid:11557688
66 Joris, I., Zand, T., Nunnari, J.J., Krolikowski, F.J., and Majno, G. (1983). Studies on the pathogenesis of atherosclerosis. I. Adhesion and emigration of mononuclear cells in the aorta of hypercholesterolemic rats. Am J Pathol 113, 341-358 .
pmid:6650664
67 Kahlon, T., Chow, F., Irving, D., and Sayre, R. (1996). Cholesterol response and foam cell formation in hamsters fed two levels of saturated fat and various levels of cholesterol. Nutr Res 16, 1353-1368 .
68 Kahlon, T.S., Chow, F.I., Irving, D.W., and Sayre, R.N. (1997). Cholesterol response and fatty streak formation in hamsters fed two levels of saturated fat and various levels of cholesterol. Nutr Res 17, 1693-1707 .
69 Keech, A.C., Harper, R.W., Harrison, P.M., Pitt, A., and McLean, A.J. (1986). Pharmacokinetic interaction between oral metoprolol and verapamil for angina pectoris. Am J Cardiol 58, 551-552 .
pmid:3529913
70 Kent, W.C., and Whitney, J.E. (1982). Cholesterol kinetics in control and hypercholesterolemic foxhounds. Artery 11, 15-32
pmid:7171320.
71 Kita, T., Nagano, Y., Yokode, M., Ishii, K., Kume, N., Ooshima, A., Yoshida, H., and Kawai, C. (1987). Probucol prevents the progression of atherosclerosis in Watanabe heritable hyperlipidemic rabbit, an animal model for familial hypercholesterolemia. Proc Natl Acad Sci U S A 84, 5928-5931 .
pmid:3475709
72 Knopp, R.H. (1999). Drug treatment of lipid disorders. N Engl J Med 341, 498-511 .
pmid:10441607
73 Knopp, R.H., and Paramsothy, P. (2006). Treatment of hypercholesterolemia in patients with metabolic syndrome: how do different statins compare? Nat Clin Pract Endocrinol Metab 2, 136-137 .
pmid:16932272
74 Kolodgie, F.D., Katocs, A.S. Jr, Largis, E.E., Wrenn, S.M., Cornhill, J.F., Herderick, E.E., Lee, S.J., and Virmani, R. (1996). Hypercholesterolemia in the rabbit induced by feeding graded amounts of low-level cholesterol. Methodological considerations regarding individual variability in response to dietary cholesterol and development of lesion type. Arterioscler Thromb Vasc Biol 16, 1454-1464 .
pmid:8977449
75 Kovesdy, C.P., Trivedi, B.K., and Anderson, J.E. (2006). Association of kidney function with mortality in patients with chronic kidney disease not yet on dialysis: a historical prospective cohort study. Adv Chronic Kidney Dis 13, 183-188 .
pmid:16580621
76 Kritchevsky, D. (1995). Dietary protein, cholesterol and atherosclerosis: a review of the early history. J Nutr 125, 589S-593S .
pmid:7884538
77 Kritchevsky, D., Tepper, S.A., Williams, D.E., and Story, J.A. (1977). Experimental atherosclerosis in rabbits fed cholesterol-free diets. Part 7. Interaction of animal or vegetable protein with fiber. Atherosclerosis 26, 397-403 .
pmid:558766
78 Kusumi, Y., Scanu, A.M., McGill, H.C., and Wissler, R.W. (1993). Atherosclerosis in a rhesus monkey with genetic hypercholesterolemia and elevated plasma Lp(a). Atherosclerosis 99, 165-174 .
pmid:8503945
79 Lehner, N.D., Bullock, B.C., and Clarkson, T.B. (1967). Intranuclear inclusion disease of pigeons. J Am Vet Med Assoc 151, 939-941 .
pmid:4294041
80 Libby, P., and Aikawa, M. (2002). Stabilization of atherosclerotic plaques: new mechanisms and clinical targets. Nat Med 8, 1257-1262 .
pmid:12411953
81 Liedtke, A.J., Hughes, H.C., and Neely, J.R. (1975). An experimental model for studying myocardial ischemia. Correlation of hemodynamic performance and metabolism in the working swine heart. J Thorac Cardiovasc Surg 69, 203-211 .
pmid:1113538
82 Lindsay, S., and Chaikoff, I.L. (1966). Naturally occurring arteriosclerosis in nonhuman primates. J Atheroscler Res 6, 36-61 .
83 Lock, A.L., Horne, C.A.M., Bauman, D.E., and Salter, A.M. (2005). Butter naturally enriched in conjugated linoleic acid and vaccenic acid alters tissue fatty acids and improves the plasma lipoprotein profile in cholesterol-fed hamsters. J Nutr 135, 1934-1939 .
pmid:16046719
84 Lynch, S.M., Gaziano, J.M., and Frei, B. (1996). Ascorbic acid and atherosclerotic cardiovascular disease. Subcell Biochem 25, 331-367 .
pmid:8821982
85 Mahley, R.W., Weisgraber, K.H., and Innerarity, T. (1974). Canine lipoproteins and atherosclerosis. II. Characterization of the plasma lipoproteins associated with atherogenic and nonatherogenic hyperlipidemia. Circ Res 35, 722-733 .
pmid:4138629
86 Andrus, S.B., and Mann, G.V. (1956). Xanthomatosis and atherosclerosis produced by diet in an adult rhesus monkey. J Lab Clin Med 48, 533-550 .
pmid:13367592
87 Mann, G.V., Andrus, S.B., McNALLY, A., and Stare, F.J. (1953). Experimental atherosclerosis in Cebus monkeys. J Exp Med 98, 195-218 .
pmid:13084840
88 Marotti, K.R., Castle, C.K., Boyle, T.P., Lin, A.H., Murray, R.W., and Melchior, G.W. (1993). Severe atherosclerosis in transgenic mice expressing simian cholesteryl ester transfer protein. Nature 364, 73-75 .
89 McKenzie, J.E., Scandling, D.M., Ahle, N.W., Bryant, H.J., Kyle, R.R., and Abbrecht, P.H. (1996). Effects of soman (pinacolyl methylphosphonofluoridate) on coronary blood flow and cardiac function in swine. Fundam Appl Toxicol 29, 140-146 .
pmid:8838649
90 Mezdour, H., Jones, R., Dengremont, C., Castro, G., and Maeda, N. (1997). Hepatic lipase deficiency increases plasma cholesterol but reduces susceptibility to atherosclerosis in apolipoprotein E-deficient mice. J Biol Chem 272, 13570-13575 .
pmid:9153204
91 Miller, F.A., Perry, J.F. Jr, Thal, A., and Wangensteen, O.H. (1956). Direct suture anastomosis of the coronary arteries in the dog. Surgery 40, 1023-1029 .
pmid:13380675
92 Moghadasian, M.H. (1999). Clinical pharmacology of 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors. Life Sci 65, 1329-1337 .
pmid:10503952
93 Moghadasian, M.H., McManus, B.M., and Frohlich, J.J. (1997). Homocyst(e)ine and coronary artery disease. Clinical evidence and genetic and metabolic background. Arch Intern Med 157, 2299-2308 .
pmid:9361570
94 Mohrschladt, M.F., Westendorp, R.G.J., Gevers Leuven, J.A., and Smelt, A.H.M. (2004). Cardiovascular disease and mortality in statin-treated patients with familial hypercholesterolemia. Atherosclerosis 172, 329-335 .
pmid:15019543
95 Narayanaswamy, M., Wright, K.C., and Kandarpa, K. (2000). Animal models for atherosclerosis, restenosis, and endovascular graft research. J Vasc Interv Radiol 11, 5-17 .
pmid:10693708
96 Nishina, P.M., Verstuyft, J., and Paigen, B. (1990). Synthetic low and high fat diets for the study of atherosclerosis in the mouse. J Lipid Res 31, 859-869 .
pmid:2380634
97 Nistor, A., Bulla, A., Filip, D.A., and Radu, A. (1987). The hyperlipidemic hamster as a model of experimental atherosclerosis. Atherosclerosis 68, 159-173 .
pmid:3689479
98 Nojiri, C., Noishiki, Y., and Koyanagi, H. (1987). Aorta-coronary bypass grafting with heparinized vascular grafts in dogs. A preliminary study. J Thorac Cardiovasc Surg 93, 867-877 .
pmid:3494887
99 Ojerio, A.D., Pucak, G.J., Clarkson, T.B., and Bullock, B.C. (1972). Diet-induced atherosclerosis and myocardial infarction in Japanese quail. Lab Anim Sci 22, 33-39 .
pmid:4334434
100 Okamoto, K., Aoki, K., Nosaka, S., and Fukushima, M. (1964). Cardiovascular Diseases in the Spontaneously Hypertensive Rat. Jpn Circ J 28, 943-952 .
pmid:14254368
101 Oku, H., Ishikawa, M., Nagata, J., Toda, T., and Chinen, I. (1993). Lipoprotein and apoprotein profile of Japanese quail. Biochimica et Biophysica Acta- Lipids and Lipid Metabolism 1167, 22-28 .
102 Organization, W.H. (2011). Cardiovascular Diseases Fact Sheet. [Accessed August 17, 2009]. Available at: http://wwwwhoint/mediacentre/factsheets/fs317/en/printhtml.
103 Paigen, B., Morrow, A., Brandon, C., Mitchell, D., and Holmes, P. (1985). Variation in susceptibility to atherosclerosis among inbred strains of mice. Atherosclerosis 57, 65-73 .
pmid:3841001
104 P?tra?cu, I.V. (1987). Marek’s disease. XVII. Studies on virus induced-atherosclerosis. Virologie 38, 245-250 .
pmid:2830714
105 Plump, A.S., Smith, J.D., Hayek, T., Aalto-Set?l?, K., Walsh, A., Verstuyft, J.G., Rubin, E.M., and Breslow, J.L. (1992). Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 71, 343-353 .
pmid:1423598
106 Prescott, M.F., McBride, C.H., Hasler-Rapacz, J., Von Linden, J., and Rapacz, J. (1991). Development of complex atherosclerotic lesions in pigs with inherited hyper-LDL cholesterolemia bearing mutant alleles for apolipoprotein B. Am J Pathol 139, 139-147 .
pmid:1853929
107 Prichard, R.W., Clarkson, T.B., Goodman, H.O., and Lofland, H.B. (1964). Aortic Atherosclerosis in Pigeons and Its Complications. Arch Pathol 77, 244-257 .
pmid:14095741
108 Purcell-Huynh, D.A., Farese, R.V. Jr, Johnson, D.F., Flynn, L.M., Pierotti, V., Newland, D.L., Linton, M.F., Sanan, D.A., and Young, S.G. (1995). Transgenic mice expressing high levels of human apolipoprotein B develop severe atherosclerotic lesions in response to a high-fat diet. J Clin Invest 95, 2246-2257 .
pmid:7738190
109 Ramaswamy, M., Wallace, T.L., Cossum, P.A., and Wasan, K.M. (1999). Species differences in the proportion of plasma lipoprotein lipid carried by high-density lipoproteins influence the distribution of free and liposomal nystatin in human, dog, and rat plasma. Antimicrob Agents Chemother 43, 1424-1428 .
pmid:10348764
110 Rapacz, J., Hasler-Rapacz, J., Taylor, K.M., Checovich, W.J., and Attie, A.D. (1986). Lipoprotein mutations in pigs are associated with elevated plasma cholesterol and atherosclerosis. Science 234, 1573-1577 .
pmid:3787263
111 Rogers, K.A., and Karnovsky, M.J. (1988). A rapid method for the detection of early stages of atherosclerotic lesion formation. Am J Pathol 133, 451-455 .
pmid:3202115
112 Ross, R. (1993). The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362, 801-809 .
pmid:8479518
113 Ross, R. (1999). Atherosclerosis—an inflammatory disease. N Engl J Med 340, 115-126 .
pmid:9887164
114 Russell, J.C., Koeslag, D.G., Dolphin, P.J., and Amy, R.M. (1993). Beneficial effects of acarbose in the atherosclerosis-prone JCR:LA-corpulent rat. Metabolism 42, 218-223 .
pmid:8474319
115 Saltykow, S. (1908). Atherosklerose bei kaninchen nach weiderhotten staphylokokkeningjiktionen. Beitr Z Pathol Anat U Z Allg Pathol, Jena , 147-171 .
116 Sauvage, L.R., Berger, K.E., Wood, S.J., Yates, S.G. 2nd, Smith, J.C., and Mansfield, P.B. (1974). Interspecies healing of porous arterial prostheses: observations, 1960 to 1974. Arch Surg 109, 698-705 .
pmid:4279642
117 Scanu, A.M., Khalil, A., Neven, L., Tidore, M., Dawson, G., Pfaffinger, D., Jackson, E., Carey, K.D., McGill, H.C., and Fless, G.M. (1988). Genetically determined hypercholesterolemia in a rhesus monkey family due to a deficiency of the LDL receptor. J Lipid Res 29, 1671-1681 .
pmid:3244017
118 Schoen, F.J., and Levy, R.J. (2009). SnapShot: calcification of bioprosthetic heart valves. Biomaterials 30, 4445-4446 .
pmid:19623686
119 Shen, J., Herderick, E., Cornhill, J.F., Zsigmond, E., Kim, H.S., Kühn, H., Guevara, N.V., and Chan, L. (1996). Macrophage-mediated 15-lipoxygenase expression protects against atherosclerosis development. J Clin Invest 98, 2201-2208 .
pmid:8941635
120 Shih, J.C.H., Pullman, E.P., and Kao, K.J. (1983). Genetic selection, general characterization, and histology of atherosclerosis-susceptible and-resistant Japanese quail. Atherosclerosis 49, 41-53 .
pmid:6651912
121 Singh, V., Tiwari, R.L., Dikshit, M., and Barthwal, M.K. (2009). Models to study atherosclerosis: a mechanistic insight. Curr Vasc Pharmacol 7, 75-109 .
pmid:19149643
122 Skold, B.H., Getty, R., and Ramsey, F.K. (1966). Spontaneous atherosclerosis in the arterial system of aging swine. Am J Vet Res 27, 257-273 .
pmid:4161799
123 Spagnoli, L.G., Orlandi, A., Mauriello, A., Santeusanio, G., de Angelis, C., Lucreziotti, R., and Ramacci, M.T. (1991). Aging and atherosclerosis in the rabbit. 1. Distribution, prevalence and morphology of atherosclerotic lesions. Atherosclerosis 89, 11-24 .
pmid:1772469
124 St Clair, R.W. (1983). Metabolic changes in the arterial wall associated with atherosclerosis in the pigeon. Fed Proc 42, 2480-2485 .
pmid:6840299
125 St Clair, R.W. (1998). The contribution of avian models to our understanding of atherosclerosis and their promise for the future. Lab Anim Sci 48, 565-568 .
pmid:10090077
126 St John, L.C., and Bell, F.P. (1991). Arterial lipid biochemistry in the spontaneously hyperlipidemic Zucker rat and its similarity to early atherogenesis. Atherosclerosis 86, 139-144 .
pmid:1872908
127 Taylor, C.B., Cox, G.E., Counts, M., and Yogi, N. (1959). Fatal myocardial infarction in rhesus monkey with diet-induced hypercholesterolemia. Am J Pathol 35, 674.
128 Taylor, C.B., Cox, G.F., Hall-Taylor, B.J., and Nelson, L.G. (1954). Atherosclerosis in areas of vascular injury in monkeys with mild hypercholesterolemia. Circulation 10, 613.
129 Taylor, J.M., and Fan, J. (1997). Transgenic rabbit models for the study of atherosclerosis. Frontiers in Bioscience: a Journal and Virtual Library 2, 298-308 .
130 Taylor, R.G., and Lewis, J.C. (1986). Endothelial cell proliferation and monocyte adhesion to atherosclerotic lesions of white carneau pigeons. Am J Pathol 125, 152-160 .
pmid:3777132
131 Tyburczy, C., Major, C., Lock, A.L., Destaillats, F., Lawrence, P., Brenna, J.T., Salter, A.M., and Bauman, D.E. (2009). Individual trans octadecenoic acids and partially hydrogenated vegetable oil differentially affect hepatic lipid and lipoprotein metabolism in golden Syrian hamsters. J Nutr 139, 257-263 .
pmid:19106329
132 Véniant, M.M., Zlot, C.H., Walzem, R.L., Pierotti, V., Driscoll, R., Dichek, D., Herz, J., and Young, S.G. (1998). Lipoprotein clearance mechanisms in LDL receptor-deficient “Apo-B48-only” and “Apo-B100-only” mice. J Clin Invest 102, 1559-1568 .
pmid:9788969
133 Vyavahare, N., Ogle, M., Schoen, F.J., Zand, R., Gloeckner, D.C., Sacks, M., and Levy, R.J. (1999). Mechanisms of bioprosthetic heart valve failure: fatigue causes collagen denaturation and glycosaminoglycan loss. J Biomed Mater Res 46, 44-50 .
pmid:10357134
134 Wasan, K.M., Ramaswamy, M., Ng, S.P., Wong, W., Parrott, S.C., Ojwang, J.O., Wallace, T., and Cossum, P.A. (1998). Differences in the lipoprotein distribution of free and liposome-associated all-trans-retinoic acid in human, dog, and rat plasma are due to variations in lipoprotein lipid and protein content. Antimicrob Agents Chemother 42, 1646-1653 .
pmid:9660998
135 Watanabe, Y. (1980). Serial inbreeding of rabbits with hereditary hyperlipidemia (WHHL-rabbit). Atherosclerosis 36, 261-268 .
pmid:7406953
136 West, C.E., Deuring, K., Schutte, J.B., and Terpstra, A.H.M. (1982). The effect of age on the development of hypercholesterolemia in rabbits fed semipurified diets containing casein. J Nutr 112, 1287-1295 .
pmid:7201508
137 Wisselink, M.A., Koeman, J.P., Wensing, T., de Bruijne, J., and Willemse, T. (1994). Hyperlipoproteinaemia associated with atherosclerosis and cutaneous xanthomatosis in a cat. Vet Q 16, 199-202 .
pmid:7740743
138 Witztum, J.L., and Steinberg, D. (1991). Role of oxidized low density lipoprotein in atherogenesis. J Clin Invest 88, 1785-1792 .
pmid:1752940
139 Worthley, S.G., Helft, G., Fuster, V., Zaman, A.G., Fayad, Z.A., Fallon, J.T., and Badimon, J.J. (2000). Serial in vivo MRI documents arterial remodeling in experimental atherosclerosis. Circulation 101, 586-589 .
pmid:10673247
140 Yanni, A.E., Yatzidis, H.A., Kavantzas, N.G., Agapitos, E.V., Perrea, D.N., and Karayannacos, P.E. (2003). Dietary L-aspartate and L-glutamate inhibit fatty streak initiation in cholesterol-fed rabbit. Nutr Metab Cardiovasc Dis 13, 80-86 .
pmid:12929620
141 Zhang, S.H., Reddick, R.L., Piedrahita, J.A., and Maeda, N. (1992). Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 258, 468-471 .
pmid:1411543
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