Cardiac allograft vasculopathy: Current concepts and treatment

Transplant International

Volumn 16, Issue 6, 2003, Pages 367-375

  Waller, Julian ^a,b   Brook, Nicholas R ^b   Nicholson, Michael L ^b  

^a Leicester General Hospital ^*  (United Kingdom)

^b LEICESTER GENERAL HOSPITAL   (United Kingdom)

Author keywords

Allograft vasculopathy; Chronic rejection; Immunosuppression

Indexed keywords

ANTIHYPERTENSIVE AGENT; ANTILIPEMIC AGENT; ANTIVIRUS AGENT; AZATHIOPRINE; CALCINEURIN INHIBITOR; CALCIUM CHANNEL BLOCKING AGENT; CHOLESTEROL; CYCLOSPORIN; CYTOKINE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; FINGOLIMOD; FK 506 BINDING PROTEIN; GANCICLOVIR; GROWTH FACTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; HYPERIMMUNE GLOBULIN; IMMUNOSUPPRESSIVE AGENT; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PLATELET DERIVED GROWTH FACTOR AA; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET DERIVED GROWTH FACTOR BB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PREDNISOLONE; RAPAMYCIN; SIMVASTATIN; STEROID; TACROLIMUS;

ALLOGRAFT; ANGIOCARDIOGRAPHY; ANIMAL MODEL; ATHEROSCLEROSIS; CARDIAC ALLOGRAFT VASCULOPATHY; CHRONIC GRAFT REJECTION; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CORONARY ARTERY BYPASS GRAFT; CORONARY ARTERY DISEASE; CYTOMEGALOVIRUS INFECTION; DISEASE ASSOCIATION; DISEASE SEVERITY; EXTRACELLULAR MATRIX; GRAFT REJECTION; GRAFT SURVIVAL; HEART TRANSPLANTATION; HISTOLOGY; HUMAN; HYPERLIPIDEMIA; HYPERTENSION; IMMUNOSUPPRESSIVE TREATMENT; INTRAVASCULAR ULTRASOUND; LIVER TOXICITY; MAJOR CLINICAL STUDY; NEPHROTOXICITY; NONHUMAN; ORGAN TRANSPLANTATION; PATHOGENESIS; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; RAT; REVIEW; RISK FACTOR; SURVIVAL RATE; VASCULAR DISEASE; VASCULAR SMOOTH MUSCLE;

HEART TRANSPLANTATION; HUMANS; IMMUNOSUPPRESSIVE AGENTS; RISK FACTORS; TRANSPLANTATION, HOMOLOGOUS; VASCULAR DISEASES;

EID: 0038011246     PISSN: 09340874     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-2277.2003.tb00316.x     Document Type: Review

References (102)

1. Bourge RC, Naftel DC, Constanzo-Nordin MR, Kirklin JK, Young JB, Kubo SH, Olivari M-T, Kasper EK (1993) The Transplant Cardiologists Research Database Group. Pre-transplantation risk factors for death after heart transplantations: a multi-institutional study. J Heart Lung Transplant 12:549-562
2. Morris RE (1993) Commentary on new xenobiotic immunosuppressants for transplantation: where are we, how did we get here, and where are we going? Clin Transplant 7:138-145
3. Petri WA Jr (1994) Infection in heart transplant recipients. Clin Infect Dis 18:141-146
4. International Society of Heart and Lung Transplantation (1999) 16th Annual Report
5. Billingham ME (1987) Cardiac transplant atherosclerosis. Transplant Proc 19 [Suppl 5]:19-25
6. Paul L (2000) Calcium channel blockers and angiotensin-converting enzyme inhibitors in the prevention of graft vasculopathy. J Heart Lung Transplant 19:409-413
7. Starnes VA, Stinson EB, Oyer PE, Valantine H, Baldwin JC, Hunt SA, Shumway NE (1987) Cardiac transplantation in children and adolescents. Circulation 76:V43-V47
8. Stark RP, McGinn AL, Wilson RF (1991) Chest pain in cardiac-transplant recipients. Evidence of sensory reinnervation after cardiac transplantation. N Engl J Med 324:1791-1794
9. Gao SZ, Schroeder JS, Hunt SA, Billingham ME, Valantine HA, Stinson EB (1989) Acute myocardial infarction in cardiac transplant recipients. Am J Coll Cardiol 64:1093-1097
10. Billingham ME (1992) Histopathology pf graft coronary disease. J Heart Lung Transplant 3:538-544
11. Johnson DE, Gao SZ, Schroeder JS, Hunt S, Alderman EL, Stinson E (1989) The spectrum of coronary pathological findings in human cardiac allografts. J Heart Lung Transplant 8:349-359
12. Keogh AM, Valantine HA, Hunt SA, Schroeder JS, McIntosh N, Oyer PE, Stinson EB (1992) Impact of proximal or mid vessel discrete coronary artery disease on survival after heart transplantation. J Heart Lung Transplant 11:892-901
13. Russell PS, Chase CM, Winn HJ, Colvin RB (1994) Coronary atherosclerosis in transplanted mouse hearts: I. Time course and immunogenetic and immunopathological considerations. J Am Pathol 144:260-269
14. Adams DH, Russel ME, Hancock WW, Sayegh MH, Wyner LR, Karnovsky MJ (1993) Chronic rejection in experimental cardiac transplantation: studies in the Lewis-F344 model. Immunol Rev 134:5-19
15. Cramer DV, Wu G-D, Chapman FA, Cajoulis E, Wang HK, Makowka L (1992) Lymphocyte subsets and histological changes associated with development of heart transplant arteriosclerosis. J Heart Lung Transplant 11:458-466
16. Constanzo-Nordin MR (1992) Cardiac allograft vasculopathy: relationship with acute cellular rejection and histocompatibility. J Heart Lung Transplant 11:90-104
17. Olivari MT, Homans DC, Wilson RF, Kubo SH, Ring WS (1989) Coronary artery disease in cardiac transplant patients receiving triple-drug immunosuppressive therapy. Circulation 80 [Suppl 3]:111-115
18. Schutz A, Kembes BM, Kugler C, Angermann C, Schad N, Rienmuller R, Fritsch S, Anthuber M, Neumaier P, Gokel JM (1990) The influence of rejection episodes on the development of coronary artery disease after heart transplantation. Eur J Cardiothorac Surg 40:300-307
19. Gao AZ, Shroeder JS, Hunt SA, Valantine HA, Hill IR, Stinson EB (1993) Influence of graft rejection on incidence of accelerated graft coronary artery disease: a new approach to analysis. J Heart Lung Transplant 12:1029-1035
20. Stovin PGI, Sharples LD, Schofield PM, Cary NRB, Mullins PA, English TAH, Wallwork J, Large SR (1993) Lack of association between endomyocardial evidence of rejection in the first six months and the later development of transplant-related coronary artery disease. J Heart Lung Transplant 12:110-116
21. Clowes AW, Clowes MM, Reidy MA (1983) Kinetics of cellular proliferation after arterial injury, I: smooth muscle cell growth in the absence of endothelium 49:327-333
22. Rabin BS, Griffith BP, Hardesty RL (1985) Vascular endothelial cell human leukocyte antigen-DR antigen and myocyte necrosis in human allograft rejection. J Heart Lung Transplant 4:293-295
23. Rose EA, Smith CR, Petrossian GA, Barr ML, Reemtsma K (1989) Humoral immune response after cardiac transplantation: correlation with fatal rejection and graft atherosclerosis. Surgery 106:203-207
24. Brasile L, Zerbe T, Rabin B, Clarke J, Abrams A, Cerilli J (1985) Identification of the antibody to vascular endothelial cells in patients undergoing cardiac transplantation. Transplantation 40:672-675
25. Zhao Xm, Yeoh TK, Hiebert M, Frist H, Miller GG (1993) The expression of acidic fibroblast growth factor (heparin binding growth 1) and cytokine genes in human cardiac allografts and T cells. Transplantation 56:1177-1182
26. Ardehali A, Drinkwater DC Jr, Laks H, Drake TA (1994) Cardiac allograft vasculopathy. Am Heart J 127:1498-1502
27. Dong C, Redenbach D, Wood S, Battistini B, Wilson JE, McManus BM (1996) The pathogenesis of cardiac allograft vasculopathy. Curr Opin Cardiol 11:183-190
28. Foegh ML (1993) Accelerated cardiac transplant atherosclerosis/chronic rejection in rabbits: inhibition by angiopeptin. Transplant Proc 25:2095-2097
29. Ventura HO, Milani RV, Lavie CJ, Smart FW, Stapleton DD, Toups TS, Price HL (1993) Cyclosporine-induced hypertension: efficacy of omega-3 fatty acids in patients after cardiac transplantation. Circulation 88 [Pt 2]:28128-28125
30. Jackson CL, Bush RC, Bowyer DE (1989) Mechanisms of anti-atherogenic actions of calcium channel antagonists. Atherosclerosis 80:17-26
31. McMurray HF, Chahwala SB (1992) Amlodipine exerts a potent antimigrational effect on aortic smooth muscle cells in culture. J Cardiovasc Pharmacol 20 [Suppl A]:54-56
32. McDonald P, Keogh A, Marshman D, et al. (1993) Two-year follow up of a prospective randomised controlled trial of diltiazem co-administration with cyclosporine after heart transplantation (abstract). J Heart Lung Transplant 12:80
33. Mehra MR, Ventura HO, Smart FW, Collins TJ, Ramee SR, Stapleton DD (1995) An intravascular ultrasound study of the influence of angiotensin-converting enzyme inhibitors and calcium entry channel blockers on the development of cardiac allograft vasculopathy. J Am Cardiol 75:853-854
34. Schroeder JS, Gao S-Z, Alderman EL, et al. (1993) A preliminary study of diltiazem in the prevention of coronary artery disease in heart-transplant recipients. N Engl J Med 328:164-170
35. Powell JS, Clozel J-P, Muller RKM, et al. (1989) Inhibitors of angiotensin-converting enzyme inhibitors prevent proliferation aften vascular injury. Science 245:186-188
36. Plissonier D, Amichot G, Duriez M, Legagneux J, Levy B, Michel J-B (1991) Effect of converting enzyme inhibition on allograft induced arterial wall injury and response. Hypertension 18 [Suppl 1]:47-54
37. Bell L, Madri JA (1990) Influence of the angiotensin system on endothelial and smooth muscle cell migration. Am J Pathol 137:7-12
38. Kagami S, Boder W, Miller D, Nobel N (1994) Angiotensin II stimulates extracellular matrix synthesis through induction of transforming growth factor-beta expression in rat glomerular mesangial cells. J Clin Invest 93:2427-2431
39. Gullestad L, Haywood G, Aass H, et al. (1998) Angiotensin II receptor subtype AT1 and AT2 expression after heart transplantation. Cardiovasc Res 38:340-347
40. Kobashigawa JA, Katznelson S, Laks H, et al. (1995) Effect of pravastatin on outcomes after cardiac transplantation. N Engl J Med 333:621-627
41. Wenke K, Meiser B, Thiery J, et al. (1997) Simvastatin reduces graft vessel disease and mortality after heart transplantation. Circulation 96:1398-1402
42. Grady KL, Constanzo-Nordin MR, Herold LS, Srinavasen S, Pifarre R (1991) Obesity and hyperlipidaemia after heart transplantation. J Heart Lung Transplant 10:449-454
43. Winters GL, Kendall TJ, Radio SJ, Wilson JE, Constanzo-Nordin MR, Switzer BL, Remmenga JA, McManus BM (1990) Post-transplant obesity hyperlipidaemia: major predictors of severity of coronary arteriopathy in failed human heart allografts. J Heart Lung Transplant 9:364-371
44. Becker DM, Chamberlain B, Swank R, Hedgewald MG, Girardet R, Baughman KL, Kwiterovich PO, Pearson TA, Ettinger WH, Renlund D (1988) Relationship between corticosteroid exposure and plasma lipid levels in heart transplant recipients. Am J Med 85:632-638
45. Superko HR, Haskel WL, DiRocco CD (1990) Lipoprotein and hepatic lipase activity and high-density lipoprotein subclasses after cardiac transplantation. Am J Cardiol 66:1131-1134
46. Wenke K, Meiser B, Thiery J, Nagel D, von Scheidt W, Steinbeck G, Seidel D, Reichart B. (1997) Simvastatin reduces graft vessel disease and mortality after heart transplantation. Circulation 96:1398-1402
47. Blankenhorn DH, Hodis DN (1993) Atherosclerosis: reversal with therapy. West J Med 159:2077-2079
48. Corsini A, Raiteri M, Soma MR, Gabbiani G, Paoletti R (1992) Simvastatin but not pravastatin has a direct inhibitory effect on rat and human myocyte proliferation. Clin Biochem 25:399-400
49. Cutts S, Bankhurst AD (1990) Reversal of lovastatin-mediated inhibition of natural killer cell toxicity by interleukin-2. J Cell Physiol 145:244-252
50. Kobashigawa JA, Katznelson S, Laks H, Johnson JA, Yeatnman L, Wang XM, Chia D, Terasaki PI, Sabad A, Cogert GA, Trosian K, Hamilton MA, Moriguchi JD, Kawata N, Hage A, Drinkwater DC, Stevenson LW (1995) Effect of pravastatin on outcomes after cardiac transplantation. N Engl J Med 333:621-627
51. Gratten MT, Moreno-Cabral CE, Starnes VA, Oyer PE, Stinson EB, Shumway NE (1989) Cytomegalovirus infection is associated with cardiac rejection and atherosclerosis. JAMA 261:3561
52. McDonald K, Rector TS, Braunlin EA, Kubo SH, Olivari MT (1989) Association of coronary artery disease in transplant recipients with cytomegalovirus infection. Am J Cardiol 64:359-362
53. Dummer S, Lee A, Breinig MK, Kormos R, Ho M, Griffith B (1994) Investigation of cytomegalovirus infection as a risk factor for coronary atherosclerosis in explanted hearts of patients undergoing heart transplantation. J Med Virol 44:305-309
54. Conraads V, Lahaye I, Rademakers F, Heuten H, Rodrigus I, Vrints C, Moulijn A (1998) Cardiac allograft vasculopathy. Aetiologic factors and therapeutic approaches. Acta Cardiol 1:37-43
55. Kendall TJ, Wilson JE, Radio SJ, Kandolf R, Gulizia JM, Winters GL, Constanzo-Nordin RR, Malcom GT, Thieszen SL, Miller LW, McManus BM (1992) Cytomegalovirus and other herpes viruses: do they have a role in the development of accelerated coronary arterial disease in human allografts? J Heart Lung Transplant 11:14-20
56. Lemstrom KB, Bruning JH, Bruggeman CA, Koskinen PK, Aho PT, Yilmaz S, Lautenschlager IT, Hayry PJ (1994) Cytomegalovirus infection-enhanced arteriosclerosis is prevented by DHPG prophylaxis in the rat. Circulation 90:1969-1978
57. Merigan TC, Renlund DG, Keay S, et al. (1992) A controlled trial of ganciclovir to prevent cytomegalovirus disease after heart transplantation. N Engl J Med 326:1182
58. Valantine HA, Gao SZ, Menon SG, et al. (2001) Impact of prophylactic immediate posttransplant ganciclovir on the development of transplant atherosclerosis: a post hoc analysis of a randomised, placebo-controlled study. Circulation 100:61
59. Valantine HA, Luikart H, Ramona D, Theodore J, Hunt S, Oyer P, Robbins R, Berry G, Reitz B (2001) Impact of cytomegalovirus hyperimmune globulin on outcome after cardiothoracic transplantation: a comparative study of combined prophylaxis with CMV hyperimmune globulin versus ganciclovir alone. Transplantation 72:1647-1652
60. Pflufelder PW, Boughner DR, Rudas L, Kostuk WJ (1993) Enhanced detection of cardiac allograft disease with intracoronary ultrasonographic imaging. Am Heart J 125:1583-1591
61. Johnson DE, Alderman EL, Schroeder JS, Gao SZ, Hunt S, De Campli WM, Stinson E, Billingham M (1991) Transplant coronary artery disease: histopathological correlations with angiographic morphology. J Am Coll Cardiol 17:449-457
62. Dressler FA, Miller LW (1992) Necropsy versus angiography: how accurate is angiography? J Heart Lung Transplant 11:56-59
63. Rickenbacher PR, Pinto FJ, Lewis NP, Hunt SA, Alderman EL, Shroeder JS, Stinson EB, Brown BW, Valantine HA (1995) Prognostic importance of intimal thickness as measured by intracoronary ultrasound after cardiac transplantation. Circulation 92:3445-3452
64. Klauss V, Rieber J, Uberfuhr P, Thiesen K, Mudra H (1995) Qualitative and quantitative assessment of cardiac allograft vasculopathy by intravascular ultrasound. Transplant Proc 27:1975-1976
65. Nissen SE, Yock P (2001) Intravascular ultrasound: novel pathophysiological insights and current clinical applications. Circulation 103:604-616
66. Mehra MR, Ventura HO, Stapleton DD, et al. (1995) Presence of severe intimal thickening by intravascular ultrasonography predicts cardiac events in cardiac allograft vasculopathy. Circulation 14:632-639
67. Morrison VA, Dunn DL, Manivel JC, GajI-Peczalska KJ, Peterson BA (1994) Clinical characteristics of post-transplant lymphoproliferative disorders. Am J Med 97:14-24
68. Oaks TE, Wallwork J (1993) Cardiac transplantation: a review. Br J Biomed Sci 50:200-211
69. Gamba A, Mammana C, Fiocchi R, Iamele L, Mamprin F (2000) Cyclosporine and coronary artery disease after heart transplantation. Compr Ther 26:121-126
70. Clipston NA, Crabtree GR (1992) Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357:695-697
71. Meiser BM, Uberfuhr, Fuchs A, Schmidt D, Pfeiffer M, Paulus D, Schulze C, Wildhirt S, von Scheidt W, Angermann CE, Klauss V, Martin S, Reichenspurner H, Kreuzer E, Reichart B (1998) Single-centre randomised trial comparing tacrolimus (FK506) and cyclosporine in the prevention of acute myocardial rejection. J Heart Lung Transplant 17:782-788
72. Pham SM, Kormos RL, Hattler BG, et al. (1996) A prospective trial of tacrolimus (FK506) in clinical heart transplantation: intermediate-term results. J Thorac Cardiovasc Surg 111:764-772
73. Rinaldi M, Pellegrini C, Martinelli L, Goggi C, Gavazzi A, Campana C, Arbustini E, Grossi, Regazzi M, Ippolitti G, Vigano M (1997) FK506 effectiveness in reducing acute rejection after heart transplantation: a prospective randomised study. J Heart Lung Transplant 10:1001-1009
74. Shibata T, Ogawa N, Koyoma I, Ksaneko N, Hokazono K, Omoto R (1993) Does FK506 accelerate the development of coronary artery disease in the transplant heart as well as in the native heart? Transplant Proc 25:1145-1148
75. Terada N, Lucas JJ, Szepsi A, et al. (1993) Rapamycin blocks cell cycle progression of activated T cells prior to events characteristic of the middle to late G1 phase of the cell cycle. J Cell Physiol 268:22825-22829
76. Aaguaard-Tillery KM, Jelinek D (1994) Inhibition of B lymphocyte cell cycle progression and proliferation by rapamycin. Cell Immunol 152:493-507
77. Mark SO, Jayaraman T, Go LO, et al. (1995) Rapamycin inhibits cell cycle regulators of proliferation in vascular smooth muscle cells. Circ Res 76:412-417
78. Mohasci PJ, Tuller D, Hullinger B, et al. (1997) Different inhibitory effects of immunosuppressive drugs on human and rat aortic smooth muscle and endothelial proliferation stimulated by platelet-derived growth factor of endothelial growth factor. J Heart Lung Transplant 6:484-492
79. Gregory CR, Pratt RE, Huie P, et al. (1993) Effect of treatment with cyclosporine, FK506, rapamycin, MMF, or deoxyspergualin on vascular smooth muscle cell proliferation in vitro and vivo. Transplant Proc 25:770-771
80. Poston RS, Billingham M, Grant Hoyt E, et al. (1999) Rapamycin reverses chronic graft vascular disease in a novel cardiac allograft model. Circulation 100:67-74
81. Ikonen TS, Gummert JF, Hayase M, Honda Y, Hausen B, Christians U, Barry GJ, Yock PG, Morris RE (2000) Sirolimus (rapamycin) halts and reverses progression of allograft vascular disease in non-human primates. Transplantation 70:969-975
82. Stepkowski SM, Tain L, Napoli KL, Ghobrial R, Wang ME, Chou TC, Kahan BD (1997) Synergistic mechanisms by which sirolimus and cyclosporine inhibit rat heart and kidney allograft rejection. Clin Exp Immunol 108:63-68
83. Waller JR, Nicholson ML (2001) The molecular mechanisms of renal allograft fibrosis. Br J Surg 88:1429-1441
84. Allison CA, Eugui EM, Sollinger HW (1993) Mycophenolate mofetil (RS 61443): mechanism of action and effects in transplantation. Transplant Rev 7:129-131
85. Kobashigawa JA, Renlund DG, Olsen SL, et al. (1992) Initial results of RS-61443 for refractory cardiac rejection (abstract). J Am Coll Cardiol 19:203
86. Ensley RD, Bristow MR, Olsen SL, et al. (1993)The use of mycophenolate mofetil (RS-61443) in human heart transplant recipients. Transplantation 56:75-82
87. Kobashigawa J, Miller L, Renlund D, Mentzer R, Alderman E, Bourge R, Costanzo M, Eisen H, Dureau G, Ratkovec R, Hummel M, Ipe D, Johnson J, Keogh A, Mamelok R, Mancini D, Smart F, Valantine H (1998) A randomized active-controlled trial of mycophenolate mofetil in heart transplant recipients. Mycophenolate Mofetil Investigators. Transplantation 66:507-515
88. Nikolova Z, Hof A, Baumlin Y, Hof RP (2001) Combined FTY 720/cyclosporine treatment promotes graft survival and lowers the peripheral lymphocyte count in a murine cardiac allotransplantation model. Transplantation 72:168-171
89. Chueh SC, Chen JR, Chen J, Lai MK (2001) FTY-729 prevents chronic rejection of rat heterotopic cardiac allografts. Transplant Proc 33:542-643
90. Stepkowski SM, Wang M, Qu X, Yu J, Okamato M, Tejpal N, Kahan BD (1998) Synergistic interaction of FTY-720 with cyclosporine or sirolimus to prolong heart allograft survival. Transplant Proc 30:2214-2216
91. Halle AA, DiSciascio G, Massin EK, Wilson RF, Johnson MR, Sullivan HJ, Bourge RC, Kleiman NS, Miller LW, Aversano TR (1995) Coronary angioplasty, atherectomy and bypass surgery in cardiac transplant recipients. J Am Coll Cardiol 26:120-128
92. Von Scheidt W, Uberfuhr P, Reichart B, Steinbeck G (1995) The role of PTCA in the management of focal critical lesions in transplant coronary artery disease. Transplant Proc 27:1936-1938
93. Wong PM, Piamsomboon C, Mathur A, Chastain HD, Singh DJ, Liu MW, Parks JM, Iyer S, Larry S, Baxley WA, Bourge RC, Roubin GS (1998) Efficacy of coronary stenting in the management of cardiac allograft vasculopathy. Am J Cardiol 82:239-241
94. Ensley RD, Hunt S, Taylor DO, Renlund DG, Menlove RL, Karwande SV, O'Connell JB, Barr ML, Michler RE, Copeland JG, Miller LW (1992) The Registry of the International Society of Heart and Lung Transplantation, and contributing investigators (1992) Predictors of survival after repeat heart transplantation. J Heart Lung Transplant 11:138-141
95. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa H, Makuuchi M, Hirata Y, Nagai R (2002) Haematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med 8:403-409
96. Lemstrom KB, Koskinen PK (1997) Expression and localisation of platelet-derived growth factor ligand and receptor protein during acute and chronic rejection of rat cardiac allografts. Circulation 96:1240-1249
97. Baumgartner I, Pieczek A, Manor O, et al. (1998) Constitutive expression of phVEGF 165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischaemia. Circulation 97:1114-1123
98. Losordo DW, Vale PR, Symes JF, et al. (1998) Gene therapy for myocardial angiogenesis: initial clinical results with direct myocardial injection of phVEGF as sole therapy for myocardial ischaemia. Circulation 98:2800-2804
99. Gao SZ, Alderman EL, Schroeder JS, et al. (1988) Accelerated coronary vascular disease in the heart transplant patient: coronary arteriographic findings. J Am Coll Cardiol 12:334-340
100. Miller GG, Davis SF, Atkinson JB, et al. (1999) Longitudinal analysis of fibroblast growth factor expression after transplantation and association with the severity of cardiac allograft vasculopathy. Circulation 100:2396-2399
101. Taraboletti G, Roberts D, Liotta LA, et al. (1990) Platelet thrombospondin modulates endothelial cell adhesion, motility and growth: a potential angiogenesis regulatory factor. J Cell Biol 111:765-772
102. Chen D, Asahara T, Krasinski K, et al. (1999) Antibody blockade of thrombospondin accelerates reendothelialisation and reduces neointima formation in balloon-injured rat carotid artery. Circulation 100:849-854