Atherosclerosis
Volume 135, Issue 1 , Pages 1-7 , November 1997

Nikolaj Nikolajewitsch Anitschkow (1885–1964) established the cholesterol-fed rabbit as a model for atherosclerosis research

  • Gerald Finking

      Affiliations

    • Corresponding Author InformationCorresponding author. Present address: Abteilung Innere Medizin II, Medizinische Universitätsklinik und Poliklinik, Robert-Koch-Str. 8, D-89081 Ulm, Germany. Tel.: +49 731 5024384; fax: +49 731 5024442; e-mail: gerald.finking@medizin.uni-ulm.de
  • ,
  • Hartmut Hanke

Received 12 March 1997 ,Revised 26 June 1997 ,Accepted 2 July 1997.

References 

  1. Anitschkow N, Chalatow S. Ueber experimentelle cholesterinsteatose und ihre bedeutung für die entstehung einiger pathologischer prozesse. Centrbl Allg Pathol Pathol Anat. 1913;24:1–9
  2. Anitschkow N. Über die veränderungen der kaninchenaorta bei experimenteller cholesterinsteatose. Beitr Pathol Anat. 1913;56:379–404
  3. Bocan TM, Mueller SB, Mazur MJ, Uhlendorf PD, Brown EQ, Kieft KA. The relationship between the degree of dietary-induced hypercholesterolemia in the rabbit and atherosclerotic lesion formation. Atherosclerosis. 1993;102:9–22
  4. Constantinides P. The role of arterial wall injury in atherogenesis and arterial thrombogenesis. Zentralbl Pathol Anat. 1989;135:517–530
  5. Constantinides P, Gutmann-Auersperg N, Hospes D. Acceleration of intimal atherogenesis through prior medial injury. Arch Pathol. 1958;66:247–254
  6. Mahley RW, Innerarity TL, Brown MS, Ho YK, Goldstein JL. Cholesteryl ester synthesis in macrophages: stimulation by beta-very low density lipoproteins from cholesterol-fed animals of several species. J Lipid Res. 1980;21:970
  7. Wissler RW, Vesselinovitch D. Differences Between Human and Animal Atherosclerosis. In: Schettler G, Weizel A, editors. Atherosclerosis. New York: Springer, 1974:319–325.
  8. Garbarsch C, Matthiesen ME, Helin P, Lorenzen I. Spontaneous aortic arteriosclerosis in rabbits of the Danish country strain. Atherosclerosis. 1970;12:291–300
  9. Watanabe T, Hirata M, Yoshikawa Y, Nagafuchi Y, Toyoshima H. Role of macrophages in atherosclerosis. Sequential observations of cholesterol-induced rabbit aortic lesion by the immunoperoxidase technique using monoclonal antimacrophage antibody. Lab Invest. 1985;53:80–90
  10. Adams CW, Morgan RS. Regression of atheroma in the rabbit. Atherosclerosis. 1977;28:399–404
  11. Badimon JJ, Badimon L, Fuster V. Regression of atherosclerotic lesions by high density lipoprotein plasma fraction in the cholesterol-fed rabbit. J Clin Invest. 1990;85:1234–1241
  12. Zhu BQ, Sievers RE, Isenberg WM, Smith DL, Parmley WW. Regression of atherosclerosis in cholesterol-fed rabbits: effects of fish oil and verapamil. J Am Coll Cardiol. 1990;15:231–237
  13. Zhu BQ, Sievers RE, Sun YP, Isenberg WM, Parmley WW. Effect of lovastatin on suppression and regression of atherosclerosis in lipid-fed rabbits. J Cardiovasc Pharmacol. 1992;19:246–255
  14. Candipan RC, Wang BY, Buitrago R, Tsao PS, Cooke JP. Regression or progression. Dependency on vascular nitric oxide. Arterioscler Thromb Vasc Biol. 1996;16:44–50
  15. Haarbo J, Christiansen C. The impact of female sex hormones on secondary prevention of atherosclerosis in ovariectomized cholesterol-fed rabbits. Atherosclerosis. 1996;123:139–144
  16. Armstrong ML, Warner ED, Connor WE. Regression of coronary atheromatosis in rhesus monkeys. Circ Res. 1970;27:59–67
  17. Superko HR, Krauss RM. Coronary artery disease regression. Convincing evidence for the benefit of aggressive lipoprotein management. Circulation. 1994;90:1056–1069
  18. Gotto AM. Lipid lowering and coronary risk. Isr J Med Sci. 1996;32:355–359
  19. Davies MJ, Richardson PD, Woolf N, Katz DR, Mann J. Risk of thrombosis in human atherosclerotic plaques: role of extracellular lipid, macrophage, and smooth muscle cell content. Br Heart J. 1993;69:377–381
  20. Watanabe Y. Serial inbreeding of rabbits with hereditary hyperlipidemia (WHHL-rabbit). Atherosclerosis. 1980;36:261–268
  21. Goldstein JL, Kita T, Brown MS. Defective lipoprotein receptors and atherosclerosis. Lessons from an animal counterpart of familial hypercholesterolemia. N Engl J Med. 1983;309:288–296
  22. Buja LM, Kita T, Goldstein JL, Watanabe Y, Brown MS. Cellular pathology of progressive atherosclerosis in the WHHL rabbit. An animal model of familial hypercholesterolemia. Arteriosclerosis. 1983;3:87–101
  23. Rosenfeld ME, Tsukada T, Gown AM, Ross R. Fatty streak initiation in Watanabe Heritable Hyperlipemic and comparably hypercholesterolemic fat-fed rabbits. Arteriosclerosis. 1987;7:9–23
  24. Rosenfeld ME, Tsukada T, Chait A, Bierman EL, Gown AM, Ross R. Fatty streak expansion and maturation in Watanabe Heritable Hyperlipemic and comparably hypercholesterolemic fat-fed rabbits. Arteriosclerosis. 1987;7:24–34
  25. Rosenfeld ME, Ross R. Macrophage and smooth muscle cell proliferation in atherosclerotic lesions of WHHL and comparably hypercholesterolemic fat-fed rabbits. Arteriosclerosis. 1990;10:680–687
  26. Esper E, Runge WJ, Gunther R, Buchwald H. Natural history of atherosclerosis and hyperlipidemia in heterozygous WHHL (WHHL-Hh) rabbits. II. Morphologic evaluation of spontaneously occuring aortic and coronary lesions. J Lab Clin Med 1993;103–110.
  27. Armstrong ML, Heistad DD. Animal models of atherosclerosis. Atherosclerosis. 1990;85:15–23
  28. Massaro ER, Zilversmit DB. Controlling factors in the maintenance of plasma cholesterol concentration in the rabbit. J Nutr. 1977;107:596–605
  29. Van-Zutphen LF, Fox RR. Strain differences in response to dietary cholesterol by JAX rabbits: correlation with esterase patterns. Atherosclerosis. 1977;28:435–446
  30. Overturf ML, Smith SA, Hewett-Emmett D, Loose-Mitchell DS, Soma MR, Gotto AMJ, et al. Development and partial metabolic characterization of a dietary cholesterol-resistant colony of rabbits. J Lipid Res. 1989;30:263–273
  31. Ross R. The pathogenesis of atherosclerosis—an update. N Engl J Med. 1985;314:488–500
  32. Stary HC, Chandler AB, Glagov S, Guyton JR, Insull W, Rosenfeld ME, et al. A definition of initial, fatty streak, and intermediate lesions of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb. 1994;14:840–856
  33. McPherson DD, Sirna SJ, Hiratzka LF. Coronary arterial remodeling studied by high-frequency epicardial echocardiographie: an early compensatory mechanism in patients with obstructive coronary atherosclerosis. J Am Coll Cardiol. 1991;17:79–86
  34. Gown AM, Tsukada T, Ross R. Human atherosclerosis. II. Immunocytochemical analysis of the cellular composition of human atherosclerotic lesions. Am J Pathol. 1986;125:191–207
  35. Tsukada T, Rosenfeld M, Ross R, Gown AM. Immunocytochemical analysis of cellular components in atherosclerotic lesions. Use of monoclonal antibodies with the Watanabe and fat-fed rabbit. Arteriosclerosis. 1986;6:601–613
  36. Sanders M. Molecular and cellular concepts in atherosclerosis. Pharm Ther. 1994;61:109–153
  37. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801–809
  38. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W, et al. 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. 1995;92:1355–1374
  39. Stary HC, Blankenhorn DH, Chandler AB, Glagov S, Insull W, Richardson M, et al. 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, American Heart Association. Circulation. 1992;85:391–405
  40. McMillan GC, Duff GL. Mitotic activity in the aortic lesions of experimental cholesterol atherosclerosis of rabbits. Arch Pathol. 1948;46:179–182
  41. Stary HC, McMillan GC. Kinetics of cellular proliferation in experimental atherosclerosis. Radioautography with grain counts in cholesterol-fed rabbits. Arch Path. 1970;89:173–183
  42. Gratzner HG. Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science. 1982;218:474–475
  43. Aoyagi M, Yamamoto M, Wakimoto H, Azuma H, Hirakawa K, Yamamoto K. Immunohistochemical detection of Ki-67 in replicative smooth muscle cells of rabbit carotid arteries after balloon denudation. Stroke. 1995;26:2328–2332
  44. Zeymer U, Fishbein MC, Forrester JS, Cercek B. Proliferating cell nuclear antigen: Immunohistochemistry in rat aorta after balloon denudation. Am J Pathol. 1992;141:685–690
  45. Cybulsky MI, Gimbrone MAJ. Endothelial expression of a mononuclear leukocyte adhesion molecule during atherogenesis. Science. 1991;251:788–791
  46. Baumgartner HR, Studer A. Folgen des gefässkatheterismus am normo- und hypercholesterinaemischen kaninchen. Path Microbiol. 1966;29:393–405
  47. Weidinger FF, McLenachan JM, Cybulsky MI, Fallon JT, Hollenberg NK, Cooke JP, et al. Hypercholesterolemia enhances macrophage recruitment and dysfunction of regenerated endothelium after balloon injury of the rabbit iliac artery. Circulation. 1991;84:755–767
  48. Andersen HO, Holm P, Nordestgaard BG, Hansen BF, Kjeldsen K, Elinder LS, et al. Effect of the antioxidant probucol on transplant arteriosclerosis in aorta-allografted rabbits. J Mol Cell Cardiol. 1995;27:1561–1571
  49. Wilensky RL, March KL, Gradus Pizlo I, Sandusky G, Fineberg N, Hathaway DR. Vascular injury, repair, and restenosis after percutaneous transluminal angioplasty in the atherosclerotic rabbit. Circulation. 1995;92:2995–3005
  50. Bondjers G, Björkerud S. Arterial repair and atherosclerosis after mechanical injury. Part 4. Uptake and composition of cholesteryl ester in morphologically defined regions of atherosclerotic lesions. Atherosclerosis. 1972;15:273–284
  51. Reidy MA, Schwartz SM. Endothelial regeneration. (III). Time course of intimal changes after small defined injury to rat aortic endothelium. Lab Invest. 1981;44:301–308
  52. Betz E, Schlote W. Responses of vessel walls to chronical applied electrical stimuli. Basic Res Cardiol. 1979;74:10–20
  53. Kling D, Holzschuh T, Strohschneider T, Betz E. Enhanced endothelial permeability and invasion of leukocytes into the artery wall as initial events in experimental arteriosclerosis. Int Angiol. 1987;6:21–28
  54. Betz E, Hämmerle H. Arterienwandproliferate und zellkulturen als indikatoren für hemmstoffe der atherogenese. Funkt Biol Med. 1984;3:46–55
  55. Hanke H, Strohschneider T, Oberhoff M, Betz E, Karsch KR. Time course of smooth muscle cell proliferation in the intima and media of arteries following experimental angioplasty. Circ Res. 1990;67:651–659
  56. Soma MR, Donetti E, Parolini C, Mazzini G, Ferrari C, Fumagalli R, et al. HMG CoA reductase inhibitors. In vivo effects on carotid intimal thickening in normocholesterolemic rabbits. Arterioscler Thromb. 1993;13:571–578
  57. Israel O. Experimentelle untersuchung über den zusammenhang zwischen nierenkrankheiten und secundären veränderungen des circulationssystems. Virchow Arch Pathol Anat. 1881;86:299–321
  58. Campbell DJ, Day AJ, Skinner SL, Tume RK. The effect of hypertension on the accumulation of lipids and the uptake of (3H)cholesterol by the aorta of normal-fed and cholesterol-fed rabbits. Atherosclerosis. 1973;18:301–319
  59. Chobanian AV, Lichtenstein AH, Nilakhe V, Haudenschild CC, Drago R, Nickerson C. Influence of hypertension on atherosclerosis in the Watanabe rabbit. Hypertension. 1989;14:203–209
  60. Spence JD, Perkins DG, Kline RL, Adams MA, Haust MD. Hemodynamic modification of aortic atherosclerosis. Effects of propranolol vs hydralazine in hypertensive hyperlipidemic rabbits. Atherosclerosis. 1984;50:325–333
  61. Duff GL, McMillan GC. The effect of alloxan diabetes on experimental cholesterol atherosclerosis in the rabbit. I. The inhibition of experimental cholesterol atherosclerosis in alloxan diabetes. II. The effect of alloxan diabetes on the retrogression of experimental cholesterol atherosclerosis. J Exp Med. 1949;89:611–630
  62. Nordestgaard BG, Zilversmit DB. Large lipoproteins are excluded from the arterial wall in diabetic cholesterol-fed rabbits. J Lipid Res. 1988;29:1491–1500
  63. Nordestgaard BG, Zilversmit DB. Hyperglycemia in normotriglyceridemic, hypercholesterolemic insulin-treated diabetic rabbits does not accelerate atherogenesis. Atherosclerosis. 1988;72:37–47
  64. Voisard R, Jensch V, Baur R, Höher M, Hombach V. A coronary porcine organ culture system for studies of postangioplasty cell proliferation. Coron Art Dis. 1995;6:657–665
  65. Fingerle L, Kraft T. The induction of smooth muscle cell proliferation in vitro using an organ culture system. Int Angiol. 1987;6:65–72
  66. Wolburg-Buchholz K, Fallier-Becker P, Roth DR, Betz EL. Transfilter coculture system with vessel wall cells under the influence of monocytes and LDL: a model for in vitro plaque formation. In: Zilla P, Fasol R, Callow A, editors. Applied Cardiovascular Biology 1990–91. 1st ed. Karger: Basel, 1992:65–69.
  67. Ludden JB, Bruger M, Wright IS. Effect of testosterone propionate and estradiol dipropionate on experimental atherosclerosis in rabbits. Arch Pathol. 1942;33:58–62
  68. Riedel M, Rafflenbeul W, Lichtlen P. Ovarian sex steroids and atherosclerosis. Clin Invest. 1993;71:406–412
  69. Hayashi T, Fukuto JM, Ignarro LJ, Chaudhuri G. Basal release of nitric oxide from aortic rings is greater in female rabbits than in male rabbits: Implications for atherosclerosis. Proc Natl Acad Sci USA. 1992;89:11259–11263
  70. Gerhard M, Ganz P. How do we explain the clinical benefits of estrogen? From bedside to bench. Circulation. 1995;92:5–8
  71. Karas RH, Patterson BL, Mendelsohn ME. Human vascular smooth muscle cells contain functional estrogen receptor. Circulation. 1994;89:1943–1950
  72. Venkov CD, Rankin AB, Vaughan DE. Identification of authentic estrogen receptor in cultured endothelial cells. A potential mechanism for steroid hormone regulation of endothelial function. Circulation. 1996;94:727–733
  73. Losordo DW, Kearney M, Kim EA, Jekanowski J, Isner JM. Variable expression of the estrogen receptor in normal and atherosclerotic coronary arteries of premenopausal women. Circulation. 1994;89:1501–1510
  74. Lin AL, Gonzalez R, Carey KD, Shain SA. Estradiol-17-beta affects estrogen receptor distribution and elevates progesterone receptor content in baboon aorta. Arteriosclerosis. 1986;6:495–504
  75. Hanke H, Hanke S, Finking G, Muhic Lohrer A, Muck AO, Schmahl FW, et al. Different effects of estrogen and progesterone on experimental atherosclerosis in female versus male rabbits. Quantification of cellular proliferation by bromodeoxyuridine. Circulation. 1996;94:175–181
  76. Anthony MS, Clarkson TB, Hughes CL, Morgan TM, Burke GL. Soybean isoflavones improve cardiovascular risk factors without affecting the reproductive system of peripubertal rhesus monkeys. J Nutr. 1996;126:43–50
  77. Saltykow S. Atherosklerose bei Kaninchen nach wiederholter Staphylokokkeninjektion. In: Aschoff L, Marchand F, editors. Beitrage Pathology Anatomy. 43rd ed. Jena: Fischer, 1908:147–176.
  78. Klurfeld DM, Allison MJ, Gerszten E, Dalton HP. Alterations of host defenses paralleling cholesterol-induced atherogenesis. I. Interactions of prolonged experimental hypercholesterolemia and infections. J Med. 1979;10:35–48
  79. Melnick JL, Adam E, Debakey ME. Cytomegalovirus and atherosclerosis. Eur Heart J. 1993;14:30–38
  80. Visser MR, Vercellotti GM. Herpes simplex virus and atherosclerosis. Eur Heart J. 1993;14:39–42
  81. Mattila KJ. Viral and bacterial infections in patients with acute myocardial infarction. J Int Med. 1989;225:293–296
  82. Benditt EP, Benditt JM. Evidence for a monoclonal origin of human atherosclerotic plaques. Proc Nat Acad Sci USA. 1973;70:1753–1756
  83. Nieminen NS, Mattila K, Valtonen V. Infection and inflammation as risk factors for myocardial infarction. Eur Heart J. 1993;14:12–16
  84. Saikku P, Leinonen M, Tenkanen L, Linnanmäki E, Ekman M-R, Manninen V, et al. Chronic chlamydia pneumoniae infection as a risk factor for coronary heart disease in the Helsinki Heart Study. Ann Int Med. 1992;116:273–278
  85. Kuo C-c, Gown AM, Benditt EP, Grayston JT. Detection of Chlamydia pneumoniae in aortic lesions of atherosclerosis by immunocytological stain. Arterioscler Thromb. 1993;13:1501–1504
  86. Moazed TC, Kuo C-c, Patton DL, Grayston JT, Campbell LA. Experimental rabbit models of Chlamydia pneumoniae infection. Am J Pathol. 1996;148:667–676

PII: S0021-9150(97)00161-5

Atherosclerosis
Volume 135, Issue 1 , Pages 1-7 , November 1997