Cardiac allograft vasculopathy: Current knowledge and future direction

Clinical Transplantation

Volumn 25, Issue 2, 2011, Pages 175-184

  Colvin Adams, Monica ^a   Agnihotri, Adheesh ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Allograft vasculopathy; Coronary disease; Heart transplant; Immunology

Indexed keywords

BIOLOGICAL MARKER; BRAIN NATRIURETIC PEPTIDE; C REACTIVE PROTEIN; ENDOTHELIN; HLA ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN; VON WILLEBRAND FACTOR;

ANGIOCARDIOGRAPHY; BRAIN DEATH; CARDIAC ALLOGRAFT VASCULOPATHY; COMPUTED TOMOGRAPHIC ANGIOGRAPHY; CYTOMEGALOVIRUS INFECTION; DIABETES MELLITUS; DONOR; DYSLIPIDEMIA; GRAFT REJECTION; HLA MATCHING; HUMAN; HYPERTENSION; INTRAVASCULAR ULTRASOUND; MORTALITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; PREDICTOR VARIABLE; PRIORITY JOURNAL; REVIEW; RISK FACTOR; STRESS ECHOCARDIOGRAPHY;

HEART TRANSPLANTATION; HUMANS; TRANSPLANTATION, HOMOLOGOUS; VASCULAR DISEASES;

EID: 79953310537     PISSN: 09020063     EISSN: 13990012     Source Type: Journal    
DOI: 10.1111/j.1399-0012.2010.01307.x     Document Type: Review

References (121)

1. Billingham ME. Histopathology of graft coronary disease. J Heart Lung Transplant 1992: 11: S38.
2. Tuzcu EM, De Franco AC, Goormastic M et al. Dichotomous pattern of coronary atherosclerosis 1 to 9years after transplantation: insights from systematic intravascular ultrasound imaging. J Am Coll Cardiol 1996: 27: 839.
3. Rahmani M, Cruz RP, Granville DJ, McManus BM. Allograft vasculopathy versus atherosclerosis. Circ Res 2006: 99: 801.
4. Carrel A. Latent life of arteries. J Exp Med 1910: 12: 460.
5. Kosek JC, Hurley EJ, Lower RR. Histopathology of orthotopic canine cardiac homografts. Lab Invest 1968: 19: 97.
6. Thomson JG. Production of severe athero in a transplanted human heart. Lancet 1969: 2: 1088.
7. Kosek JC, Hurley EJ, Sewell DH, Lower RR. Histopathology of orthotopic canine cardiac homografts and its clinical correlation. Transplant Proc 1969: 1: 311.
8. Bieber CP, Stinson EB, Shumway NE, Payne R, Kosek J. Cardiac transplantation in man. VII. Cardiac allograft pathology. Circulation 1970: 41: 753.
9. Taylor DO, Stehlik J, Edwards LB et al. Registry of the International Society for Heart and Lung Transplantation: Twenty-sixth Official Adult Heart Transplant Report-2009. J Heart Lung Transplant 2009: 28: 1007.
10. Robbins RC, Barlow CW, Oyer PE et al. Thirty years of cardiac transplantation at Stanford University. J Thorac Cardiovasc Surg 1999: 117: 939.
11. Taylor DO, Edwards LB, Boucek MM et al. Registry of the International Society for Heart and Lung Transplantation: Twenty-fourth Official Adult Heart Transplant Report - 2007. J Heart Lung Transplant 2007: 26: 769.
12. Perrault LP, Mahlberg F, Breugnot C et al. Hypercholesterolemia increases coronary endothelial dysfunction, lipid content, and accelerated atherosclerosis after heart transplantation. Arterioscler Thromb Vasc Biol 2000: 20: 728.
13. Escobar A, Ventura HO, Stapleton DD et al. Cardiac allograft vasculopathy assessed by intravascular ultrasonography and nonimmunologic risk factors. Am J Cardiol 1994: 74: 1042.
14. Ballantyne CM, Podet EJ, Patsch WP et al. Effects of cyclosporine therapy on plasma lipoprotein levels. JAMA 1989: 262: 53.
15. Akhlaghi F, Jackson CH, Parameshwar J, Sharples LD, Trull AK. Risk factors for the development and progression of dyslipidemia after heart transplantation. Transplantation 2002: 73: 1258.
16. Eisen HJ, Tuzcu EM, Dorent R et al. Everolimus for the prevention of allograft rejection and vasculopathy in cardiac-transplant recipients. N Engl J Med 2003: 349: 847.
17. Morrisett JD, Abdel-Fattah G, Kahan BD. Sirolimus changes lipid concentrations and lipoprotein metabolism in kidney transplant recipients. Transplant Proc 2003: 35: 143S.
18. Kobashigawa JA, Katznelson S, Laks H et al. Effect of pravastatin on outcomes after cardiac transplantation. N Engl J Med 1995: 333: 621.
19. Hognestad A, Endresen K, Wergeland R et al. Plasma C-reactive protein as a marker of cardiac allograft vasculopathy in heart transplant recipients. J Am Coll Cardiol 2003: 42: 477.
20. Mehra MR, Raval NY. Metaanalysis of statins and survival in de novo cardiac transplantation. Transplant Proc 2004: 36: 1539.
21. Kwak B, Mulhaupt F, Myit S, Mach F. Statins as a newly recognized type of immunomodulator. Nat Med 2000: 6: 1399.
22. Radovancevic B, Poindexter S, Birovljev S et al. Risk factors for development of accelerated coronary artery disease in cardiac transplant recipients. Eur J Cardiothorac Surg 1990: 4: 309; discussion 13.
23. Costanzo MR, Naftel DC, Pritzker MR et al. Heart transplant coronary artery disease detected by coronary angiography: a multiinstitutional study of preoperative donor and recipient risk factors. Cardiac Transplant Research Database. J Heart Lung Transplant 1998: 17: 744.
24. Taylor DO, Barr ML, Radovancevic B et al. A randomized, multicenter comparison of tacrolimus and cyclosporine immunosuppressive regimens in cardiac transplantation: decreased hyperlipidemia and hypertension with tacrolimus. J Heart Lung Transplant 1999: 18: 336.
25. Reichart B, Meiser B, Vigano M et al. European Multicenter Tacrolimus (FK506) Heart Pilot Study: one-year results - European Tacrolimus Multicenter Heart Study Group. J Heart Lung Transplant 1998: 17: 775.
26. Schroeder JS, Gao SZ, Alderman EL et al. A preliminary study of diltiazem in the prevention of coronary artery disease in heart-transplant recipients. N Engl J Med 1993: 328: 164.
27. Bae JH, Rihal CS, Edwards BS et al. Association of angiotensin-converting enzyme inhibitors and serum lipids with plaque regression in cardiac allograft vasculopathy. Transplantation 2006: 82: 1108.
28. Erinc K, Yamani MH, Starling RC et al. The effect of combined angiotensin-converting enzyme inhibition and calcium antagonism on allograft coronary vasculopathy validated by intravascular ultrasound. J Heart Lung Transplant 2005: 24: 1033.
29. Martinez-Dolz L, Almenar L, Martinez-Ortiz L et al. Predictive factors for development of diabetes mellitus post-heart transplant. Transplant Proc 2005: 37: 4064.
30. Nieuwenhuis MG, Kirkels JH. Predictability and other aspects of post-transplant diabetes mellitus in heart transplant recipients. J Heart Lung Transplant 2001: 20: 703.
31. Depczynski B, Daly B, Campbell LV, Chisholm DJ, Keogh A. Predicting the occurrence of diabetes mellitus in recipients of heart transplants. Diabet Med 2000: 17: 15.
32. Mogollón Jiménez MV, Sobrino Márquez JM, Arizón Muñoz JM et al. Incidence and importance of de novo diabetes mellitus after heart transplantation. Transpl Proc 2008: 40: 3053.
33. Weir MR, Fink JC. Risk for posttransplant diabetes mellitus with current immunosuppressive medications. Am J Kidney Dis 1999: 34: 1.
34. Gunnarsson R, Lundgren G, Magnusson G, Ost L, Groth CG. Steroid diabetes - a sign of overtreatment with steroids in the renal graft recipient? Scand J Urol Nephrol Suppl 1980: 54: 135.
35. Pirsch JD, Miller J, Deierhoi MH, Vincenti F, Filo RS. A comparison of tacrolimus (FK506) and cyclosporine for immunosuppression after cadaveric renal transplantation. FK506 Kidney Transplant Study Group. Transplantation 1997: 63: 977.
36. European FK506 Multicentre Liver Study Group. Randomised trial comparing tacrolimus (FK506) and cyclosporin in prevention of liver allograft rejection. Lancet 1994: 344: 423.
37. Vincenti F, Jensik SC, Filo RS, Miller J, Pirsch J. A long-term comparison of tacrolimus (FK506) and cyclosporine in kidney transplantation: evidence for improved allograft survival at five years. Transplantation 2002: 73: 775.
38. Woodward RS, Schnitzler MA, Baty J et al. Incidence and cost of new onset diabetes mellitus among U.S. wait-listed and transplanted renal allograft recipients. Am J Transplant 2003: 3: 590.
39. Mayer AD, Dmitrewski J, Squifflet JP et al. Multicenter randomized trial comparing tacrolimus (FK506) and cyclosporine in the prevention of renal allograft rejection: a report of the European Tacrolimus Multicenter Renal Study Group. Transplantation 1997: 64: 436.
40. Pham SM, Kormos RL, Hattler BG et al. A prospective trial of tacrolimus (FK 506) in clinical heart transplantation: intermediate-term results. J Thorac Cardiovasc Surg 1996: 111: 764.
41. Meiser BM, Uberfuhr P, Fuchs A et al. Single-center randomized trial comparing tacrolimus (FK506) and cyclosporine in the prevention of acute myocardial rejection. J Heart Lung Transplant 1998: 17: 782.
42. Teebken OE, Struber M, Harringer W, Pichlmaier MA, Haverich A. Primary immunosuppression with tacrolimus and mycophenolate mofetil versus cyclosporine and azathioprine in heart transplant recipients. Transplant Proc 2002: 34: 1265.
43. Hathout EH, Chinnock RE, Johnston JK et al. Pediatric post-transplant diabetes: data from a large cohort of pediatric heart-transplant recipients. Am J Transplant 2003: 3: 994.
44. Raichlin ER, McConnell JP, Lerman A et al. Systemic inflammation and metabolic syndrome in cardiac allograft vasculopathy. J Heart Lung Transplant 2007: 26: 826.
45. Grattan MT, Moreno-Cabral CE, Starnes VA, Oyer PE, Stinson EB, Shumway NE. Cytomegalovirus infection is associated with cardiac allograft rejection and atherosclerosis. JAMA 1989: 261: 3561.
46. Mocarski ES Jr. Immune escape and exploitation strategies of cytomegaloviruses: impact on and imitation of the major histocompatibility system. Cell Microbiol 2004: 6: 707.
47. Koskinen PK. The association of the induction of vascular cell adhesion molecule-1 with cytomegalovirus antigenemia in human heart allografts. Transplantation 1993: 56: 1103.
48. Van Dorp WT, Jonges E, Bruggeman CA, Daha MR, Van Es LA, Van Der Woude FJ. Direct induction of MHC class I, but not class II, expression on endothelial cells by cytomegalovirus infection. Transplantation 1989: 48: 469.
49. Hosenpud JD, Chou SW, Wagner CR. Cytomegalovirus-induced regulation of major histocompatibility complex class I antigen expression in human aortic smooth muscle cells. Transplantation 1991: 52: 896.
50. Streblow DN, Kreklywich C, Yin Q et al. Cytomegalovirus-mediated upregulation of chemokine expression correlates with the acceleration of chronic rejection in rat heart transplants. J Virol 2003: 77: 2182.
51. Weis M, Kledal TN, Lin KY et al. Cytomegalovirus infection impairs the nitric oxide synthase pathway: role of asymmetric dimethylarginine in transplant arteriosclerosis. Circulation 2004: 109: 500.
52. Preiksaitis JK, Brennan DC, Fishman J, Allen U. Canadian Society of Transplantation Consensus Workshop on Cytomegalovirus Management in Solid Organ Transplantation Final Report. Am J Transplant 2005: 5: 218.
53. Potena L, Grigioni F, Magnani G et al. Prophylaxis versus preemptive anti-cytomegalovirus approach for prevention of allograft vasculopathy in heart transplant recipients. J Heart Lung Transplant 2009: 28: 461.
54. Hosenpud JD, Everett JP, Morris TE, Mauck KA, Shipley GD, Wagner CR. Cardiac allograft vasculopathy. Association with cell-mediated but not humoral alloimmunity to donor-specific vascular endothelium. Circulation 1995: 92: 205.
55. Costanzo-Nordin MR. Cardiac allograft vasculopathy: relationship with acute cellular rejection and histocompatibility. J Heart Lung Transplant 1992: 11: S90.
56. Vassalli G, Gallino A, Weis M et al. Alloimmunity and nonimmunologic risk factors in cardiac allograft vasculopathy. Eur Heart J 2003: 24: 1180; .
57. Raichlin E, Edwards BS, Kremers WK et al. Acute cellular rejection and the subsequent development of allograft vasculopathy after cardiac transplantation. J Heart Lung Transplant 2009: 28: 320.
58. Michaels PJ, Espejo ML, Kobashigawa J et al. Humoral rejection in cardiac transplantation: risk factors, hemodynamic consequences and relationship to transplant coronary artery disease. J Heart Lung Transplant 2003: 22: 58.
59. Mehra MR, Uber PA, Ventura HO, Scott RL, Park MH. The impact of mode of donor brain death on cardiac allograft vasculopathy: an intravascular ultrasound study. J Am Coll Cardiol 2004: 43: 806.
60. Szabo G, Buhmann V, Bahrle S, Vahl CF, Hagl S. Brain death impairs coronary endothelial function. Transplantation 2002: 73: 1846.
61. Yamani MH, Starling RC, Cook DJ et al. Donor spontaneous intracerebral hemorrhage is associated with systemic activation of matrix metalloproteinase-2 and matrix metalloproteinase-9 and subsequent development of coronary vasculopathy in the heart transplant recipient. Circulation 2003: 108: 1724; B.
62. Bendeck MP, Zempo N, Clowes AW, Galardy RE, Reidy MA. Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat. Circ Res 1994: 75: 539.
63. Pérez López S, Otero Hernández J, Vázquez Moreno N, Escudero Augusto D, ÁLvarez Menéndez F, Astudillo González A. Brain death effects on catecholamine levels and subsequent cardiac damage assessed in organ donors. J Heart Lung Transplant 2009: 28: 815.
64. Labarrere CA, Nelson DR, Faulk WP. Endothelial activation and development of coronary artery disease in transplanted human hearts. JAMA 1997: 278: 1169.
65. Valantine HA. Cardiac allograft vasculopathy: central role of endothelial injury leading to transplant "atheroma." Transplantation 2003: 76: 891.
66. Rogers NJ, Lechler RI. Allorecognition. Am J Transplant 2001: 1: 97.
67. Ciubotariu R, Liu Z, Colovai AI et al. Persistent allopeptide reactivity and epitope spreading in chronic rejection of organ allografts. J Clin Invest 1998: 101: 398.
68. Shoskes DA, Wood KJ. Indirect presentation of MHC antigens in transplantation. Immunol Today 1994: 15: 32.
69. Adams DH, Wyner LR, Karnovsky MJ. Experimental graft arteriosclerosis. II. Immunocytochemical analysis of lesion development. Transplantation 1993: 56: 794.
70. Zhang XP, Kelemen SE, Eisen HJ. Quantitative assessment of cell adhesion molecule gene expression in endomyocardial biopsy specimens from cardiac transplant recipients using competitive polymerase chain reaction. Transplantation 2000: 70: 505.
71. Nabel EG, Yang Z, Liptay S et al. Recombinant platelet-derived growth factor B gene expression in porcine arteries induce intimal hyperplasia in vivo. J Clin Invest 1993: 91: 1822.
72. Ross R, Raines EW, Bowen-Pope DF. The biology of platelet-derived growth factor. Cell 1986: 46: 155.
73. Heldin CH, Wasteson A, Westermark B. Platelet-derived growth factor. Mol Cell Endocrinol 1985: 39: 169.
74. Meliss RR, Pethig K, Steinhoff G et al. Platelet-derived growth factor rather than basic fibroblast growth factor and vascular endothelial cell growth factor is involved in adventitial narrowing causing vascular stenosis in end-stage cardiac allograft vasculopathy. Transplant Proc 1999: 31: 89.
75. Hosenpud JD, Morris TE, Shipley GD, Mauck KA, Wagner CR. Cardiac allograft vasculopathy. Preferential regulation of endothelial cell-derived mesenchymal growth factors in response to a donor-specific cell-mediated allogeneic response. Transplantation 1996: 61: 939.
76. Ross R. Mechanisms of atherosclerosis - a review. Adv Nephrol Necker Hosp 1990: 19: 79.
77. Blann AD, Woywodt A, Bertolini F et al. Circulating endothelial cells. Biomarker of vascular disease. Thromb Haemost 2005: 93: 228.
78. Werner N, Kosiol S, Schiegl T et al. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 2005: 353: 999.
79. Simper D, Wang S, Deb A et al. Endothelial progenitor cells are decreased in blood of cardiac allograft patients with vasculopathy and endothelial cells of noncardiac origin are enriched in transplant atherosclerosis. Circulation 2003: 108: 143.
80. Thomas HE, Parry G, Dark JH, Arthur HM, Keavney BD. Circulating endothelial progenitor cell numbers are not associated with donor organ age or allograft vasculopathy in cardiac transplant recipients. Atherosclerosis 2009: 202: 612.
81. Weis M, Von Scheidt W. Cardiac allograft vasculopathy: a review. Circulation 1997: 96: 2069.
82. Barbir M, Lazem F, Banner N, Mitchell A, Yacoub M. The prognostic significance of non-invasive cardiac tests in heart transplant recipients. Eur Heart J 1997: 18: 692.
83. Gao SZ, Alderman EL, Schroeder JS, Hunt SA, Wiederhold V, Stinson EB. Progressive coronary luminal narrowing after cardiac transplantation. Circulation 1990: 82: IV269.
84. O'Neill BJ, Pflugfelder PW, Singh NR, Menkis AH, McKenzie FN, Kostuk WJ. Frequency of angiographic detection and quantitative assessment of coronary arterial disease one and three years after cardiac transplantation. Am J Cardiol 1989: 63: 1221.
85. St Goar FG, Pinto FJ, Alderman EL et al. Intracoronary ultrasound in cardiac transplant recipients. In vivo evidence of "angiographically silent" intimal thickening. Circulation 1992: 85: 979.
86. Nissen S. Coronary angiography and intravascular ultrasound. Am J Cardiol 2001: 87: 15A.
87. Johnson DE, Alderman EL, Schroeder JS et al. Transplant coronary artery disease: histopathologic correlations with angiographic morphology. J Am Coll Cardiol 1991: 17: 449.
88. St Goar FG, Pinto FJ, Alderman EL et al. Detection of coronary atherosclerosis in young adult hearts using intravascular ultrasound. Circulation 1992: 86: 756.
89. Mehra MR, Ventura HO, Stapleton DD, Smart FW, Collins TC, Ramee SR. Presence of severe intimal thickening by intravascular ultrasonography predicts cardiac events in cardiac allograft vasculopathy. J Heart Lung Transplant 1995: 14: 632.
90. Rickenbacher PR, Pinto FJ, Lewis NP et al. Prognostic importance of intimal thickness as measured by intracoronary ultrasound after cardiac transplantation. Circulation 1995: 92: 3445.
91. Kobashigawa JA, Tobis JM, Starling RC et al. Multicenter intravascular ultrasound validation study among heart transplant recipients: outcomes after five years. J Am Coll Cardiol 2005: 45: 1532.
92. Tuzcu EM, Kapadia SR, Sachar R et al. Intravascular ultrasound evidence of angiographically silent progression in coronary atherosclerosis predicts long-term morbidity and mortality after cardiac transplantation. J Am Coll Cardiol 2005: 45: 1538.
93. Fang JC, Rocco T, Jarcho J, Ganz P, Mudge GH. Noninvasive assessment of transplant-associated arteriosclerosis. Am Heart J 1998: 135: 980.
94. Akosah KO, Mohanty PK, Funai JT et al. Noninvasive detection of transplant coronary artery disease by dobutamine stress echocardiography. J Heart Lung Transplant 1994: 13: 1024.
95. Akosah KO, McDaniel S, Hanrahan JS, Mohanty PK. Dobutamine stress echocardiography early after heart transplantation predicts development of allograft coronary artery disease and outcome. J Am Coll Cardiol 1998: 31: 1607.
96. Spes CH, Klauss V, Mudra H et al. Diagnostic and prognostic value of serial dobutamine stress echocardiography for noninvasive assessment of cardiac allograft vasculopathy: a comparison with coronary angiography and intravascular ultrasound. Circulation 1999: 100: 509.
97. Elhendy A, O'Leary EL, Xie F, McGrain AC, Anderson JR, Porter TR. Comparative accuracy of real-time myocardial contrast perfusion imaging and wall motion analysis during dobutamine stress echocardiography for the diagnosis of coronary artery disease. J Am Coll Cardiol 2004: 44: 2185.
98. Rodrigues AC, Bacal F, Medeiros CC et al. Noninvasive detection of coronary allograft vasculopathy by myocardial contrast echocardiography. J Am Soc Echocardiogr 2005: 18: 116.
99. Verhoeven PP, Lee FA, Ramahi TM et al. Prognostic value of noninvasive testing one year after orthotopic cardiac transplantation. J Am Coll Cardiol 1996: 28: 183.
100. Elhendy A, Van Domburg RT, Vantrimpont P et al. Prediction of mortality in heart transplant recipients by stress technetium-99m tetrofosmin myocardial perfusion imaging. Am J Cardiol 2002: 89: 964.
101. Hacker M, Tausig A, Romuller B et al. Dobutamine myocardial scintigraphy for the prediction of cardiac events after heart transplantation. Nucl Med Commun 2005: 26: 607.
102. Wilke N, Jerosch-Herold M, Wang Y et al. Myocardial perfusion reserve: assessment with multisection, quantitative, first-pass MR imaging. Radiology 1997: 204: 373.
103. Muehling OM, Wilke NM, Panse P et al. Reduced myocardial perfusion reserve and transmural perfusion gradient in heart transplant arteriopathy assessed by magnetic resonance imaging. J Am Coll Cardiol 2003: 42: 1054.
104. Suzuki K, Hamano K, Ito H, Fujimura Y, Esato K. The detection of chronic heart graft rejection by 31P NMR spectroscopy. Surg Today 1999: 29: 143.
105. Evanochko WT, Buchthal SD, Den Hollander JA et al. Cardiac transplant patients response to the (31)P MRS stress test. J Heart Lung Transplant 2002: 21: 522.
106. Caus T, Kober F, Marin P et al. Non-invasive diagnostic of cardiac allograft vasculopathy by 31P magnetic resonance chemical shift imaging. Eur J Cardiothorac Surg 2006: 29: 45.
107. Hacker M, Hoyer HX, Uebleis C et al. Quantitative assessment of cardiac allograft vasculopathy by real-time myocardial contrast echocardiography: a comparison with conventional echocardiographic analyses and [Tc99m]-sestamibi SPECT. Eur J Echocardiogr 2008: 9: 494.
108. Romeo G, Houyel L, Angel CY, Brenot P, Riou JY, Paul JF. Coronary stenosis detection by 16-slice computed tomography in heart transplant patients: comparison with conventional angiography and impact on clinical management. J Am Coll Cardiol 2005: 45: 1826.
109. Gibson CM, Cannon CP, Daley WL et al. TIMI frame count: a quantitative method of assessing coronary artery flow. Circulation 1996: 93: 879.
110. Fang JC, Kinlay S, Wexberg P et al. Use of the thrombolysis in myocardial infarction frame count for the quantitative assessment of transplant-associated arteriosclerosis. Am J Cardiol 2000: 86: 890.
111. Pijls NH, De Bruyne B, Peels K et al. Measurement of fractional flow reserve to assess the functional severity of coronary-artery stenoses. N Engl J Med 1996: 334: 1703.
112. Fearon WF, Takagi A, Jeremias A et al. Use of fractional myocardial flow reserve to assess the functional significance of intermediate coronary stenoses. Am J Cardiol 2000: 86: 1013, A10.
113. De Bruyne B, Hersbach F, Pijls NH et al. Abnormal epicardial coronary resistance in patients with diffuse atherosclerosis but "normal" coronary angiography. Circulation 2001: 104: 2401.
114. Fearon WF, Aarnoudse W, Pijls NH et al. Microvascular resistance is not influenced by epicardial coronary artery stenosis severity: experimental validation. Circulation 2004: 109: 2269.
115. Aarnoudse W, Fearon WF, Manoharan G et al. Epicardial stenosis severity does not affect minimal microcirculatory resistance. Circulation 2004: 110: 2137.
116. Labarrere CA, Lee JB, Nelson DR, Al-Hassani M, Miller SJ, Pitts DE. C-reactive protein, arterial endothelial activation, and development of transplant coronary artery disease: a prospective study. Lancet 2002: 360: 1462.
117. Eisenberg MS, Chen HJ, Warshofsky MK et al. Elevated levels of plasma C-reactive protein are associated with decreased graft survival in cardiac transplant recipients. Circulation 2000: 102: 2100.
118. Shaw SM, Williams SG. Is brain natriuretic peptide clinically useful after cardiac transplantation? J Heart Lung Transplant 2006: 25: 1396.
119. Mehra MR, Uber PA, Walther D et al. Gene expression profiles and B-type natriuretic peptide elevation in heart transplantation: more than a hemodynamic marker. Circulation 2006: 114: I21.
120. Labarrere CA, Nelson DR, Cox CJ, Pitts D, Kirlin P, Halbrook H. Cardiac-specific troponin I levels and risk of coronary artery disease and graft failure following heart transplantation. JAMA 2000: 284: 457.
121. Martínez-Dolz L, Almenar L, Reganon E et al. Follow-up study on the utility of von Willebrand factor levels in the diagnosis of cardiac allograft vasculopathy. J Heart Lung Transplant 2008: 27: 760.