Why do animal models of post-angioplasty restenosis sometimes poorly predict the outcome of clinical trials?

Cardiovascular Research

Volumn 39, Issue 1, 1998, Pages 50-59

  Lafont, Antoine ^a   Faxon, David ^b  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; ANIMAL TISSUE; CONTROLLED STUDY; CORONARY ARTERY OBSTRUCTION; HISTOPATHOLOGY; MODEL; NONHUMAN; PRIORITY JOURNAL; RESTENOSIS; REVIEW; TRANSLUMINAL CORONARY ANGIOPLASTY; TREATMENT OUTCOME;

EID: 0032126369     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0008-6363(98)00109-6     Document Type: Review

References (136)

1. [1] Currier JW, Faxon DP. Restenosis after percutaneous transluminal coronary angioplasty: have we been aiming at the wrong target?. J Am Coll Cardiol 1995;25:516-520.
2. [2] Lafont A, Guérot C, Lemarchand P. Which gene for which restenosis?. Lancet 1995;346:1442-1443.
3. [3] Ferrell M, Fuster V, Gold HK, Chesebro JH. A dilemma for the 1990s. Choosing appropriate experimental animal model for the prevention of restenosis. Circulation 1992;85:1630-1631.
4. [4] Liu MW, Roubin GS, King SB. Restenosis after coronary angioplasty: potential biologic determinants and role of intimal hyperplasia. Circulation 1989;79:1374-1387.
5. [5] Muller D, Ellis S, Topol E. Experimental models of coronary artery restenosis. J Am Coll Cardiol 1992;19:418-432.
6. [6] Bauters C, Meurice T, Hamon M, et al. Mechanisms and prevention of restenosis: from experimental models to clinical practice. Cardiovasc Res 1996;31:835-846.
7. [7] Schwartz R. Animal models of human coronary restenosis. In Topol E, editor. Coronary and peripheral angioplasty. Saunders: 1994:365-381.
8. [8] Schwartz R, Huber K, Murphy J, et al. Restenosis and the proportional neointimal response to coronary artery injury: Results in a porcine model. J Am Coll Cardiol 1992;19:267-274.
9. [9] Santoian EC, King 3rd SB. Intravascular stents, intimal proliferation and restenosis. J Am Coll Cardiol 1992;19:877-879.
10. [10] Serruys PW, Macaya C, De Jaegere P, et al. A comparison of balloon-expandable-stent implantation with balloon angioplasty in patients with coronary artery disease. N Engl J Med 1994;331:489-495.
11. [11] Fischman DL, Leon MB, Bairn DS, et al. A randomized comparison of coronary stent placement and balloon angioplasty in the treatment of coronary artery disease. N Engl J Med 1994;331:496-501.
12. [12] Post MJ, de Smet BJ, van der Helm Y, Borst C, Kuntz RE. Arterial remodeling after balloon angioplasty or stenting in an atherosclerotic experimental model. Circulation 1997;96:996-1003.
13. [13] Lafont A, Guzman LA, Whitlow PL, et al. Restenosis after experimental angioplasty. Intimal, medial, and adventitial changes associated with constrictive remodeling. Circ Res 1995;76:996-1002.
14. [14] Kakuta T, Currier JW, Haudenschild CC, Ryan TJ, Faxon DP. Differences in compensatory vessel enlargement, not intimal formation, account for restenosis after angioplasty in the hypercholesterolemic rabbit model. Circulation 1994;89:2809-2815.
15. [15] Post MJ, Borst C, Pasterkamp G, Haudenschild CC. Arterial remodeling in atherosclerosis and restenosis: a vague concept of a distinct phenomenon. Atherosclerosis 1995;118:S115-S123.
16. [16] Guzman LA, Mick MJ, Arnold AM, Forudi F, Whitlow PL. Role of intimal hyperplasia and arterial remodeling after balloon angioplasty: an experimental study in the atherosclerotic rabbit model. Arterioscler Thromb Vasc Biol 1996;16:479-487.
17. [17] Andersen HG, Maeng M, Thorwest M, Falk E. Remodeling rather than neointimal formation explains luminal narrowing after deep vessel wall injury. Insights from a porcine coronary (re)stenosis model. Circulation 1996;93:1716-1724.
18. [18] Mintz GS, Popma JJ, Pichard AD, et al. Arterial remodeling after coronary angioplasty. A serial intravascular ultrasound study. Circulation 1996;94:35-43.
19. [19] Mintz GS, Popma JJ, Hong MK, et al. Intravascular ultrasound to discern device-specific effects and mechanisms of restenosis. Am J Cardiol 1996;78:18-22.
20. [20] Fishman JA, Ryan GB, Karnovsky MJ. Endothelial regeneration in the rat carotid artery and the significance of endothelial denudation in the pathogenesis of myointimal thickening. Lab Invest 1975;32:339-351.
21. [21] Clowes AW, Karnovsky MJ. Failure of certain antiplatelet drugs to affect myointimal thickening following arterial endothelial injury in the rat. Lab Invest 1977;36:452-464.
22. [22] Clowes AW, Karnovsky MJ. Suppression by heparin of smooth muscle cell proliferation in injured arteries. Nature 1977;265:625-626.
23. [23] Clowes AW, Reidy MA, Clowes MM. Kinetics of cellular proliferation after arterial injury. I. Smooth muscle cell growth in the absence of endothelium. Lab Invest 1983;49:327-333.
24. [24] Nam SC, Lee WM, Jarmolych J, Lee KT, Thomas WA. Rapid production of advanced atherosclerosis in swine by a combination of endothelial injury and cholesterol feeding. Exp Mol Pathol 1973;18:369-379.
25. [25] Blaton V, Peelers H. The nonhuman primates as models for studying human atherosclerosis: Studies on the chimpanzee, the baboon and the rhesus macacus. Adv Exp Med Biol 1976;67:33-64.
26. [26] Fingerle J, Au YPT, Clowes AW, Reidy MA. Intimal lesion formation in rat carotid arteries after endothelial denudation in absence of medial injury. Arteriosclerosis 1990;10:1082-1087.
27. [27] Clowes AW, Reidy MA, Clowes MM. Mechanisms of stenosis after arterial injury. Lab Invest 1983;49:208-215.
28. [28] Clowes AW, Schwartz SM. Significance of quiescent smooth muscle migration in the injured rat carotid artery. Circ Res 1985;56:139-145.
29. [29] Clowes AW, Clowes MM, Reidy MA. Kinetics of cellular proliferation aftr arterial injury. III. Endothelial and smooth muscle cell growth in chronically denuded vessels. Lab Invest 1986;54:295-303.
30. [30] Ye L, Mora R, Akhayani N, Haudenschild CC, Liau G. Growth factor and cytokine-regulated hyaluronan-binding protein TSG-6 is localized to the injury-induced rat neointima and confers enhanced growth in vascular smooth muscle cells. Circ Res 1997;81:289-296.
31. [31] Chen D, Krasinski K, Sylvester A, et al. Downregulation of cyclin-dependent kinase 2 activity and cyclin A promoter activity in vascular smooth muscle cells by p27 (KIP1), an inhibitor of neointima formation in the rat carotid artery. J Clin Invest 1997;99:2334-2341.
32. [32] Mills CJ, Northrup JL, Hullinger TG, et al. Temporal expression of c-fos mRNA following balloon injury in the rat common carotid artery. Cardiovasc Res 1996;32:954-961.
33. [33] Chang MW, Ohno T, Gordon D, et al. Adenovirus-mediated transfer of the herpes simplex virus thymidine kinase gene inhibits vascular smooth muscle cell proliferation and neointima formation following balloon angioplasty of the rat carotid artery. Mol Med 1995;1:172-181.
34. [34] Chang MW, Barr E, Lu MM, Barton K, Leiden JM. Adenovirus-mediated over-expression of the cyclin/cyclin-dependent kinase inhibitor, p21 inhibits vascular smooth muscle cell proliferation and neointima formation in the rat carotid artery model of balloon angioplasty. J Clin Invest 1995;96:2260-2268.
35. [35] Majesky MW, Schwartz SM, Clowes MM, Clowes AW Heparin regulates smooth muscle cell S phase entry in the injured rat carotid artery. Circ Res 1987;61:296-300.
36. [36] Ferns GA, Raines EW, Sprugel KH, et al. Inhibition of neointimal smooth muscle accumulation after angioplasty by an antibody to PDGF. Science 1991;253:1129-1132.
37. [37] Reidy MA, Silver M. Endothelial regeneration. VII. Lack of intimal proliferation after defined injury to rat aorta. Am J Pathol 1985;118:173-177.
38. [38] Powell J, Clozel J, Muller R, et al. Inhibitors of angiotensin-converting enzyme prevent myointimal proliferation after vascular injury. Science 1989;245:186-188.
39. [39] Wengrovitz M, Selassie LG, Gifford RRM, Thiele BL. Cyclosporin inhibits the development of medial thickening after experimental arterial thickening. J Vasc Surg 1990;12:1-7.
40. [40] Tiell ML, Sussman II, Gordon PB, Sanders RN. Suppression of fibroblast proliferation in vitro and of neointimal hyperplasia in vivo by the triazolopyrimidine, trapidil. Artery 1983;12:33-50.
41. [41] Lundergan C, Foegh ML, Vargas R, et al. Inhibition of myointimal proliferation of the rat carotid artery by the peptides, angiopeptin and BIM 23034. Atherosclerosis 1989;80:49-55.
42. [42] Sarembock IJ, LaVeau PJ, Sigal SL, et al. Influence of inflation pressure and balloon size on the development of intimal hyperplasia after balloon angioplasty: a study in the atherosclerotic rabbit. Circulation 1989;80:1029-1040.
43. [43] Wilensky RL, March KL, Gradus-Pizlo I, et al. Vascular injury, repair, and restenosis after percutaneous transluminal angioplasty in the atherosclerotic rabbit. Circulation 1995;92:2995-3005.
44. [44] Faxon DP, Weber VJ, Haudenschild C, et al. Acute effects of transluminal angioplasty in three models of atherosclerosis. Arteriosclerosis 1982;2:125-133.
45. [45] Faxon DP, Sanborn TA, Weber VJ, et al. Restenosis following transluminal angioplasty in experimental atherosclerosis. Arteriosclerosis 1984;4:189-195.
46. [46] Sarembock IJ, Gertz SD, Thome LM, et al. Effectiveness of hirulog in reducing restenosis after balloon angioplasty of atherosclerotic femoral arteries in rabbits. J VasC Res 1996;33:308-314.
47. [47] Ragosta M, Gimple LW, Gertz SD, et al. Specific factor Xa inhibition reduces restenosis after balloon angioplasty of atherosclerotic femoral arteries in rabbits. Circulation 1994;89:1262-1271.
48. [48] Lichtenstein AH, Chobanian AV. Effect of fish oil on atherogenesis in Watanabe heritable hyperlipidemic rabbit. Arteriosclerosis 1990;10:597-606.
49. [49] Ragosta M, Barry WL, Gimple LW, et al. Effect of thrombin inhibition with desulfatohirudin on early kinetics of cellular proliferation after balloon angioplasty in atherosclerotic rabbits. Circulation 1996;93:1194-1200.
50. [50] Fukuyama J, Ichikawa K, Hamano S, Shibata N. Tranilast suppresses the vascular intimaL hyperplasia after balloon injury in rabbits fed on a high-cholesterol diet. Eur J Pharmacol 1996;318:327-332.
51. [51] 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.
52. [52] Schneider JE, Berk BC, Gravanis MB, et al. Probucol decreases neointimal formation in a swine model of coronary artery balloon injury. A possible role for antioxidants in restenosis. Circulation 1993;88:628-637.
53. [53] Steg PG, Tahlil O, Aubailly N, et al. Reduction of restenosis after angioplasty in an atheromatous rabbit model by suicide gene therapy. Circulation 1997;96:408-411.
54. [54] Gellman J, Ezekowitz MD, Sarembock IJ, et al. Effect of lovastatin on intimal hyperplasia after balloon angioplasty: A study in an atherosclerotic hypercholesterolemic rabbit. J Am Coll Cardiol 1991;17:251-259.
55. [55] Gimple LW, Gertz SD, Haber HL, et al. Effect of chronic subcutaneous or intramural administration of heparin on femoral artery restenosis after balloon angioplasty in hypercholesterolemic rabbits. A quantitative angiographic and histopathological study. Circulation 1992;86:1536-1546.
56. [56] Lyle EM, Fujita T, Conner MW, et al. Effect of inhibitors of factor Xa or platelet adhesion, heparin, and aspirin on platelet deposition in an atherosclerotic rabbit model of angioplasty injury. J Pharmacol Toxicol Methods 1995;33:53-61.
57. [57] Bilazarian SD, Currier JW, Haudenschild CC, et al. Angiotensin converting enzyme inhibition reduces restenosis in experimental angioplasty (abstract). J Am Coll Cardiol 1991;17:268A.
58. [58] McKenney P, Currier J, Haudenschild C, Heyman D, Faxon D. Cyclosporin A does not inhibit restenosis in experimental angioplasty (abstract). Circulation 1991;84(suppl II):II-70.
59. [59] Liu MW, Roubin GS, Robinson KA, et al. Trapidil in preventing restenosis after balloon angioplasty in the atherosclerotic rabbit. Circulation 1990;81:1089-1093.
60. [60] Hong MK, Bhatti T, Matthews BJ, et al. The effect of porous infusion balloon-delivered angiopeptin on myointimal hyperplasia after balloon injury in the rabbit. Circulation 1993;88:638-648.
61. [61] Faxon DP, Sanborn TA, Haudenschild CC, Ryan TJ. Effect of antiplatelet therapy on restenosis after experimental angioplasty. Am J Cardiol 1984;53:72C-76C.
62. [62] Lafont AM, Chai YC, Cornhill JF, et al. Effect of alpha-tocopherol on restenosis after angioplasty in a model of experimental atherosclerosis. J Clin Invest 1995;95:1018-1025.
63. [63] Gellman J, Healey G, Chen Q, et al. The effect of very low dose irradiation on restenosis following balloon angioplasty. A study in the atherosclerotic rabbit (abstract). Circulation 1991;84(suppl II):II-331
64. [64] Robinson KA, Roubin GS, Siegel RJ, et al. Intra-arterial stenting in the atherosclerotic rabbit. Circulation 1988;78:646-653.
65. [65] Merritt R, Guruge BL, Miller DD, Chaitman BR, Bora PS. Moderate alcohol feeding attenuates postinjury vascular cell proliferation in rabbit angioplasty model. J Cardiovasc Pharmacol 1997;30:19-25.
66. [66] Anderson HV, Zaatari GS, Roubin GS, Leimgruber PP, Gruentzig AR. Steerable fiberoptic catheter delivery of laser energy in atherosclerotic rabbits. Am Heart J 1986;111:1065-1072.
67. [67] Rosenfeldt FL, Chi L, Black AJ, et al. Excimer laser angioplasty in the atherosclerotic rabbit: comparison with balloon angioplasty. Am Heart J 1992;124:349-355.
68. [68] Jang Y, Guzman LA, Lincoff AM, et al. Influence of blockade at specific levels of the coagulation cascade on restenosis in a rabbit atherosclerotic femoral artery injury model. Circulation 1995;92:3041-3050.
69. [69] Coats Jr. WD, Cheung DT, Han B, Currier JW, Faxon DP. Balloon angioplasty significantly increases collagen content but does not alter collagen subtype I/III ratios in the atherosclerotic rabbit iliac model. J Mol Cell Cardiol 1996;28:441-446.
70. [70] Coats Jr. WD, Whittaker P, Cheung DT, et al. Collagen content is significantly lower in restenotic versus nonrestenotic vessels after balloon angioplasty in the atherosclerotic rabbit model. Circulation 1997;95:1293-1300.
71. [71] Strauss BH, Chisholm RJ, Keeley FW, et al. Extracellular matrix remodeling after balloon angioplasty injury in a rabbit model of restenosis. Circ Res 1994;75:650-658.
72. [72] Strauss BH, Roubin R, Batchelor WB, et al. In vivo collagen turnover following experimental balloon angioplasty injury and the role of matrix metalloproteinases. Circ Res 1996;79:541-550.
73. [73] Gertz SD, Gimple LW, Banai S, et al. Geometric remodeling is not the principal pathogenetic process in restenosis after balloon angioplasty. Evidence from correlative angiographic-histomorphometric studies of atherosclerotic arteries in rabbits. Circulation 1994;90:3001-3008.
74. [74] Banai S, Shou M, Correa R, et al. Rabbit ear model of injury-induced arterial smooth muscle cell proliferation: Kinetics, reproducibility, and implications. Circ Res 1991;69:748-756.
75. [75] Losordo DW, Pickering JG, Takeshita S, et al. Use of the rabbit ear artery to serially assess foreign protein secretion after site-specific arterial gene transfer in vivo. Circulation 1994;89:785-792.
76. [76] Steele PM, Chesebro JH, Stanson AW, et al. Balloon angioplasty: natural history of the pathophysiological response to injury in a pig model. Circ Res 1985;57:105-112.
77. [77] Schwartz RS, Murphy JG, Edwards WD, et al. Restenosis after balloon angioplasty: Practical proliferation model in porcine coronary arteries. Circulation 1990;82:2190-2200.
78. [78] Weiner BH, Ockene IS, Jarmolych J, Fritz KE, Daoud AS. Comparison of pathologic and angiographic findings in a porcine preparation of coronary atherosclerosis. Circulation 1985;72:1081-1086.
79. [79] Schwartz R, Koval T, Edwards W, et al. Effect of external beam irradiation on neointimal hyperplasia after experimental coronary artery injury. J Am Coll Cardiol 1992;19:1106-1113.
80. [80] Reitman JS, Mahley RW, Fry DL. Yucatan miniature swine as a model for diet-induced atherosclerosis. Atherosclerosis 1982;43:119-132.
81. [81] Santoian ED, Schneider JE, Gravanis MB, et al. Angiopeptin inhibits intimal hyperplasia after angioplasty in porcine coronary arteries. Circulation 1993;88:11-14.
82. [82] Rodgers GP, Minor ST, Robinson K, et al. Adjuvant therapy for intracoronary stents: investigations in atherosclerotic swine. Circulation 1990;82:560-569.
83. [83] Gal D, Rondione AJ, Slovekai GA, et al. Atherosclerotic Yucatan microswine: an animal model with high-grade, fibrocalcific, nonfatty lesions suitable for testing catheter-based interventions. Am Heart J 1990;119:291-300.
84. [84] Fuster V, Lie TJ, Badimon L, et al. Spontaneous and diet-induced coronary atherosclerosis in normal swine and swine with von Willebrand disease. Arteriosclerosis 1985;5:67-73.
85. [85] Griggs TR, Reddick RL, Sultzer D, Brinkhous KM. Susceptibility to atherosclerosis in aortas and coronary arteries of swine with von Willebrand's disease. Am J Pathol 1981;102:137-145.
86. [86] Martinez-Gonzalez J, Badimon L. Human and porcine smooth muscle cells share similar proliferation dependence on the mevalonate pathway: implication for in vivo interventions in the porcine model. Eur J Clin Invest 1996;26:1023-1032.
87. [87] Chesebro JA, Lam JYT, Badimon L, Fuster V. Restenosis after arterial angioplasty: A hemorheologic response to injury. Am J Cardiol 1987;60:10B-16B.
88. [88] Ip JH, Fuster V, Israel D, et al. The role of platelets, thrombin and hyperplasia in restenosis after coronary angioplasty. J Am Coll Cardiol 1991;17:77B-88B.
89. [89] Mason R, Read M. Some species differences in fibrinolysis and blood coagulation. J Biomed Mater Res 1971;5:121-128.
90. [90] Murphy JG, Schwartz RS, Edwards WD, et al. Methotrexate and azathioprine fail to inhibit porcine coronary restenosis. Circulation 1990;82:III-429.
91. [91] Groves PH, Banning AP, Penny WJ, et al. Kinetics of smooth muscle cell proliferation and intimal thickening in a pig carotid model of balloon injury. Atherosclerosis 1995;117:83-96.
92. [92] Huckle WR, Drag MD, Acker WR, et al. Effects of subtype-selective and balanced angiotensin II receptor antagonists in a porcine coronary artery model of vascular restenosis. Circulation 1996;93:1009-1019.
93. [93] Huber KC, Schwartz RS, Edwards WD, et al. Effects of angiotensin converting enzyme inhibition on neointimal proliferation in a porcine coronary injury model. Am Heart J 1993;125:695-701.
94. [94] Burke SE, Lubbers NL, Gagne GD, et al. Selective antagonism of the ET(A) receptor reduces neointimal hyperplasia after balloon-induced vascular injury in pigs. J Cardiovasc Pharmacol 1997;30:33-41.
95. [95] Veinot JP, Edwards WD, Camrud AR, et al. The effects of lovastatin on neointimal hyperplasia following injury in a porcine coronary artery model. Can J Cardiol 1996;12:65-70.
96. [96] Nunes GL, Sgoutas DS, Redden RA, et al. Combination of vitamins C and E alters the response to coronary balloon injury in the pig. Arterioscler Thromb Vasc Biol 1995;15:156-165.
97. [97] Van Der Giessen WJ, Serruys PW, Van Beusekom HMM, et al. Coronary stenting with a new, radioopaque, balloon-expandable endoprosthesis in pigs. Circulation 1991;83:1788-1798.
98. [98] Carter AJ, Laird JR. Experimental results with endovascular irradiation via a radioactive stent. Int J Radiat Oncol Biol Phys 1996;36:797-803.
99. [99] Hata H, Ohara Y, Kuga T, et al. Vasoreactivity and restenosis after coronary angioplasty in the atherosclerotic pig model. Coron Artery Dis 1995;6:503-511.
100. [100] Weinberger J, Amols H, Ennis RD, et al. Intracoronary irradiation: dose-response for the prevention of restenosis in swine. Int J Radiat Oncol Biol Phys 1996;36:767-775.
101. [101] Filippo C, Abela GS, Fenech A, et al. Transluminal laser irradiation of coronary arteries in live dogs: an angiographic and morphologic study of acute effects. Am J Cardiol 1985;57:171-174.
102. [102] Roubin GS, Robinson KA, King SB, et al. Early and late results of intracoronary arterial stenting after coronary angioplasty in dogs. Circulation 1987;76:891-897.
103. [103] Schatz RA, Palmaz JC, Tio FO, et al. Balloon expandable intracoronary stents in the adult dog. Circulation 1987;76:450-456.
104. [104] Willerson JT, Yao SK, McNatt J, et al. Liposome-bound prostaglandin E1 often prevents cyclic flow variations in stenosed and endothelium-injured canine coronary arteries. Circulation 1994;89:1786-1791.
105. [105] Mondy JS, Williams JK, Adams MR, Dean RH, Geary RL. Structural determinants of lumen narrowing after angioplasty in atherosclerotic nonhuman primates. J Vasc Surg 1997;26:875-883.
106. [106] Rudel LL. Genetic factors influence the atherogenic response of lipoproteins to dietary fat and cholesterol in nonhuman primates. J Am Coll Nutr 1997;16:306-312.
107. [107] Geary RL, Williams JK, Golden D, et al. 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 1996;16:34-43.
108. [108] Bauters C, Hamon M, Van Belle E, et al. Restenosis after coronary angioplasty. Contribution of experimental models. Arch Mal Coeur Vaiss 1993;86:47-56.
109. [109] Karsch KR, Preisack MB, Baildon R, et al. Low molecular weight heparin (reviparin) in percutaneous transluminal coronary angioplasty. Results of a randomized, double-blind, unfractionated heparin and placebo-controlled, multicenter trial (REDUCE trial). Reduction of restenosis after PTCA, early administration of reviparin in a double-blind unfractionated heparin and placebo-controlled evaluation. J Am Coll Cardiol 1996;28:1437-1443.
110. [110] Cairns JA, Gill J, Morton B, et al. Fish oils and low-molecular-weight heparin for the reduction of restenosis after percutaneous transluminal coronary angioplasty. The EMPAR Study. Circulation 1996;94:1553-1560.
111. [111] Berger PB, Holmes Jr. DR, Ohman EM, et al. Restenosis, reocclusion and adverse cardiovascular events after successful balloon angioplasty of occluded versus nonoccluded coronary arteries. Results from the Multicenter American Research Trial with cilazapril after angioplasty to prevent transluminal coronary obstruction and restenosis. J Am Coll Cardiol 1996;27:1-7.
112. [112] Savage MP, Goldberg S, Bove AA, et al. Effect of thromboxane A2 blockade on clinical outcome and restenosis after successful coronary angioplasty. Multi-Hospital Eastern Atlantic Restenosis Trial. Circulation 1995;92:3194-3200.
113. [113] Ellis SG, Roubin GS, Wilentz J, Douglas JS, King SB. Effect of 18-24 hour heparin administration for prevention of restenosis after uncomplicated coronary angioplasty. Am Heart J 1989;117:777-782.
114. [114] Brack MJ, Ray S, Chauban A, et al. The subcutaneous Heparin and Angioplasty Restenosis Prevention (SHARP) trial. Results of a multicenter randomized trial investigating the effects of high dose unfractionated heparin on angiographic restenosis and clinical outcome. J Am Coll Cardiol 1995;26:947-954.
115. [115] Serruys PW, Herrman JP, Simon R, et al. A comparison of hirudin with heparin in the prevention of restenosis after coronary angioplasty. Helvetica investigators . N Engl J Med 1995;333:757-763.
116. [116] Nakamura Y, Yamaoka O, Uchida K, et al. Pravastatin reduces restenosis after coronary angioplasty of high grade stenotic lesions: results of SHIPS (SHIga Pravastatin Study). Cardiovasc Drugs Ther 1996;10:475-483.
117. [117] Foley DP, Bonnier H, Jackson G, et al. Prevention of restenosis after coronary balloon angioplasty: rationale and design of the Fluvastatin Angioplasty Restenosis (FLARE) Trial. The FLARE study group. Am J Cardiol 1994;73:50D-61D.
118. [118] Eriksen UH, Amtorp O, Bagger JP, et al. Randomized double-blind Scandinavian trial of angiopeptin versus placebo for the prevention of clinical events and restenosis after coronary balloon angioplasty. Am Heart J 1995;130:1-8.
119. [119] Maresta A, Balducelli M, Cantini L, et al. Trapidil (triazolopyrimidine), a platelet-derived growth factor antagonist, reduces restenosis after percutaneous transluminal coronary angioplasty. Results of the randomized, double-blind STARC study. Studio Trapidil versus Aspirin nella Restenosi Coronarica. Circulation 1994;90:2710-2715.
120. [120] Okamoto S, Inden M, Setsuda M, Konishi T, Nakano T. Effects of trapidil (triazolopyrimidine), a platelet-derived growth factor antagonist, in preventing restenosis after percutaneous transluminal coronary angioplasty. Am Heart J 1992;123:1439-1444.
121. [121] Bairati I, Roy L, Meyer F. Double-blind, randomized, controlled trial of fish oil supplements in prevention of recurrence of stenosis after coronary angioplasty. Circulation 1992;85:950-956.
122. [122] Lablanche JM, Grollier G, Lusson JR, et al. Effect of the direct nitric oxide donors linsidomine and molsidomine on angiographic restenosis after coronary balloon angioplasty. The ACCORD Study. Circulation 1997;95:83-89.
123. [123] Holmes Jr. DR, Garratt KN, Isner JM, et al. Effect of subintimal resection on initial outcome and restenosis for native coronary lesions and saphenous vein graft disease treated by directional coronary atherectomy. A report from the CAVEAT I and II investigators. Coronary Angioplasty Versus Excisional Atherectomy Trial. J Am Coll Cardiol 1996;28:645-651.
124. [124] Appelman YE, Piek JJ, Strikwerda S, et al. Randomised trial of excimer laser angioplasty versus balloon angioplasty for treatment of obstructive coronary artery disease. Lancet 1996;347:79-84.
125. [125] Barrett G, Mullins JJ. Transgenic animal models of cardiovascular disease. Curr Opin Biotechnol 1992;3:637-640.
126. [126] Waller BF, Pinkerton CA, Orr CM, et al. Morphological observations late (greater than 30 days) after clinically successful coronary balloon angioplasty. Circulation 1991;83:28-41.
127. [127] Lafont A, Durand E, Drechsel S, et al. Experimental evidence of remodeling after angioplasty in arterial remodeling. In: Lafont A, Topol E, editors. A critical factor in restenosis. Kluwer, Dordrecht: 1997:51-68.
128. [128] Tardif JC, Cote G, Lesperance J, et al. Probucol and multivitamins in the prevention of restenosis after coronary angioplasty. N Engl J Med 1997;337:365-372.
129. [129] Tardif JC, Cote G, Lesperance J, et al. Effects of probucol on vascular remodeling and tissue hyperplasia after coronary angioplasty: intravascular ultrasound results from the MVP randomized trial. Circulation 1997;96:I-154.
130. [130] Nabel EG, Pompili VJ, Plautz GE, Nabel GJ. Gene transfer and vascular disease. Cardiovasc Res 1994;28:445-455.
131. [131] Newman KD, Dunn PF, Owens JW, et al. Adenovirus-mediated gene transfer into normal rabbit arteries results in prolonged vascular cell activation, inflammation, and neointimal hyperplasia. J Clin Invest 1995;96:2955-2965.
132. [132] Lemarchand P, Jones M, Yamada I, Crystal RG. In vivo gene transfer and expression in normal uninjured blood vessels using replication-deficient recombinant adenovirus vectors. Circ Res 1993;72:1132-1138.
133. [133] Fischell TA, Carter AJ, Laird JR. The beta-particle-emitting radioisotope stent (isostent): animal studies and planned clinical trials. Am J Cardiol 1996;78:45-50.
134. [134] Waksman R. Local catheter-based intracoronary radiation therapy for restenosis. Am J Cardiol 1996;78:23-28.
135. [135] Bauters C, Amant C, Bodart JC, et al. D allele of the angiotensin I-converting enzyme is a major risk factor for restenosis after coronary stenting. Circulation 1997;96:56-60.
136. [136] Lawn RM, Wade DP, Hammer RE, et al. Atherogenesis in transgenic mice expressing human apolipoprotein(a) [see comments]. Nature 1992;360:670-672.