Factors associated with the development of cardiac allograft vasculopathy - a systematic review of observational studies

Clinical Transplantation

Volumn 26, Issue 2, 2012, Pages

  Braga, J R ^a   Santos, I S O ^b   Mcdonald, M ^a   Shah, P S ^c   Ross, H J ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b Hospital de Messejana   (Brazil)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cardiac allograft vasculopathy; Heart transplantation; Risk factors; Systematic review

Indexed keywords

ANGIOCARDIOGRAPHY; ARTICLE; CARDIAC ALLOGRAFT VASCULOPATHY; CASE CONTROL STUDY; COHORT ANALYSIS; CYTOMEGALOVIRUS INFECTION; GRAFT RECIPIENT; GRAFT REJECTION; HEART FAILURE; HEART TRANSPLANTATION; HUMAN; INTRAVASCULAR ULTRASOUND; LIPID ANALYSIS; OBSERVATIONAL STUDY; ORGAN DONOR; PATIENT SELECTION; POSTOPERATIVE COMPLICATION; PRIORITY JOURNAL; RISK ASSESSMENT; SYSTEMATIC REVIEW;

CORONARY ANGIOGRAPHY; CORONARY DISEASE; HEART TRANSPLANTATION; HUMANS; RISK FACTORS;

EID: 84859848364     PISSN: 09020063     EISSN: 13990012     Source Type: Journal    
DOI: 10.1111/j.1399-0012.2011.01565.x     Document Type: Article

References (78)

1. Arnold JMO, Liu P, Demers C et al. Canadian Cardiovascular Society consensus conference recommendations on heart failure 2006: diagnosis and management. Can J Cardiol 2006: 22: 23.
2. Stehlik J, Edwards LB, Kucheryavaya AY et al. The Registry of the International Society for Heart and Lung Transplantation: twenty-seventh official adult heart transplant report-2010. J Heart Lung Transplant 2010: 29: 1089.
3. Ramzy D, Rao V, Brahm J, Miriuka S, Delgado D, Ross HJ. Cardiac allograft vasculopathy: a review. Can J Surg 2005: 48: 319.
4. Libby P, Tanaka H. The pathogenesis of coronary arteriosclerosis ("chronic rejection") in transplanted hearts. Clin Transplant 1994: 8: 313.
5. Stroup DF, Berlin JA, Morton SC et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 2000: 283: 2008.
6. Hayden JA, Côté P, Bombardier C. Evaluation of the quality of prognosis studies in systematic reviews. Ann Inter Med 2006: 144: 427.
7. Jones DR. Meta-analysis of observational epidemiological studies: a review. J R Soc Med 1992: 85: 165.
8. Aziz T, Hasleton P, Hann AW, Yonan N, Deiraniya A, Hutchinson IV. Transforming growth factor beta in relation to cardiac allograft vasculopathy after heart transplantation. J Thorac Cardiovasc Surg 2000: 119: 700.
9. 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.
10. Chang G, Denofrio D, Desai S et al. Lipoprotein(a) levels and heart transplantation atherosclerosis. Am Heart J 1998: 136: 329.
11. Brunner-La RoccaHP, Schneider J, Kunzli A, Turina M, Kiowski W. Cardiac allograft rejection late after transplantation is a risk factor for graft coronary artery disease. Transplantation 1998: 65: 538.
12. Gullestad L, Ross H, Myers J et al. Importance of decreased heart rate in predicting transplant coronary artery disease. Clin Transplant 1997: 11: 628.
13. Reed EF, Hong B, Ho E, Harris PE, Weinberger J, Suciu-Foca N. Monitoring of soluble HLA alloantigens and anti-HLA antibodies identifies heart allograft recipients at risk of transplant-associated coronary artery disease. Transplantation 1996: 61: 566.
14. Mehra MR, Ventura HO, Chambers R et al. Predictive model to assess risk for cardiac allograft vasculopathy: an intravascular ultrasound study. J Am Coll Cardiol 1995: 26: 1537.
15. 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.
16. Raichlin ER, Mcconnell JP, Lerman A et al. Systemic inflammation and metabolic syndrome in cardiac allograft vasculopathy. J Heart Lung Transplant 2007: 26: 826.
17. Densem CG, Hutchinson IV, Yonan N, Brooks NH. Donor and recipient-transforming growth factor-beta 1 polymorphism and cardiac transplant-related coronary artery disease. Transpl Immunol 2004: 13: 211.
18. Caforio AL, Tona F, Fortina AB et al. Immune and nonimmune predictors of cardiac allograft vasculopathy onset and severity: multivariate risk factor analysis and role of immunosuppression. Am J Transplant 2004: 4: 962.
19. Lietz K, John R, Mancini DM, Edwards NM. Outcomes in cardiac transplant recipients using allografts from older donors versus mortality on the transplant waiting list; implications for donor selection criteria. J Am Coll Cardiol 2004: 43: 1553.
20. Wang HJ, Ko WJ, Leea CM et al. Delayed occurrence of cardiac allograft vasculopathy in Chinese heart transplant recipients compared with their Western counterparts. Clin Transplant 2004: 18: 21.
21. Yamani MH, Lauer MS, Starling RC et al. Impact of donor spontaneous intracranial hemorrhage on outcome after heart transplantation. Am J Transplant 2004: 4: 257.
22. Haddad M, Pflugfelder PW, Guiraudon C et al. Angiographic, pathologic, and clinical relationships in coronary artery disease in cardiac allografts. J Heart Lung Transplant 2005: 24: 1218.
23. 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.
24. Tuzcu EM, Hobbs RE, Rincon G et al. Occult and frequent transmission of atherosclerotic coronary disease with cardiac transplantation: insights from intravascular ultrasound. Circulation 1995: 91: 1706.
25. Valantine HA, Gao SZ, Menon SG et al. Impact of prophylactic immediate posttransplant ganciclovir on development of transplant atherosclerosis: a post hoc analysis of a randomized, placebo-controlled study. Circulation 1999: 100: 61.
26. Gao HZ, Hunt SA, Alderman EL, Liang D, Yeung AC, Schroeder JS. Relation of donor age and preexisting coronary artery disease on angiography and intracoronary ultrasound to later development of accelerated allograft coronary artery disease. J Am Coll Cardiol 1997: 29: 623.
27. Densem CG, Hutchinson IV, Yonan N, Brooks NH. Influence of tumor necrosis factor-alpha gene-308 polymorphism on the development of coronary vasculopathy after cardiac transplantation. J Heart Lung Transplant 2001: 20: 1265.
28. Pethig K, Heublein B, Hoffmann A, Borlak J, Wahlers T, Haverich A. ACE-gene polymorphism is associated with the development of allograft vascular disease in heart transplant recipients. J Heart Lung Transplant 2000: 19: 1175.
29. Densem CG, Hutchinson IV, Cooper A, Yonan N, Brooks NH. Polymorphism of the transforming growth factor-beta 1 gene correlates with the development of coronary vasculopathy following cardiac transplantation. J Heart Lung Transplant 2000: 19: 551.
30. Czerny M, Sahin V, Fasching P et al. The impact of diabetes mellitus at the time of heart transplantation on long-term survival. Diabetologia 2002: 45: 1498.
31. Kauke T, Kaczmarek I, Dick A et al. Anti-MICA antibodies are related to adverse outcome in heart transplant recipients. J Heart Lung Transplant 2009: 28: 305.
32. Sanchez Lazaro IJ, Almenar Bonet L, Moro Lopez J et al. Influence of traditional cardiovascular risk factors in the recipient on the development of cardiac allograft vasculopathy after heart transplantation. Transplant Proc 2008: 40: 3056.
33. Kaczmarek I, Deutsch MA, Kauke T et al. Donor-specific HLA alloantibodies: long-term impact on cardiac allograft vasculopathy and mortality after heart transplant. Exp Clin Transplant 2008: 6: 229.
34. Arora S, Gullestad L, Wergeland R et al. Probrain natriuretic peptide and C-reactive protein as markers of acute rejection, allograft vasculopathy, and mortality in heart transplantation. Transplantation 2007: 83: 1308.
35. Subramanian AK, Quinn TC, Kickler TS, Kasper EK, Tucker PC. Correlation of Chlamydia pneumonia infection and severity of accelerated graft arteriosclerosis after cardiac transplantation. Transplantation 2002: 73: 761.
36. Wahlers T, Fieguth HG, Jurmann M et al. Graft coronary vasculopathy in cardiac transplantation - evaluation of risk factors by multivariate analysis. Eur J Cardiothorac Surg 1996: 10: 1.
37. Labarrere CA, Nelson DR, Pitts DE, Kirlin PC, Halbrook H. Immunohistochemical model to predict risk for coronary artery disease and failure in heart transplant patients. Am J Transplant 2001: 1: 251.
38. Labarrere CA, Torry RJ, Nelson DR et al. Vascular antithrombin and clinical outcome in heart transplant patients. Am J Cardiol 2001: 87: 425.
39. Labarrere CA, Nelson DR, Miller SJ et al. Value of serum-soluble intercellular adhesion molecule-1 for the noninvasive risk assessment of transplant coronary artery disease, post-transplant ischemic events, and cardiac graft failure. Circulation 2000: 102: 1549.
40. Labarrere CA, Nelson DR, Faulk WP. Myocardial fibrin deposits in the first month after transplantation predict subsequent coronary artery disease and graft failure in cardiac allograft recipients. Am J Med 1998: 105: 207.
41. Arora S, Andreassen A, Simonsen S et al. Prognostic importance of renal function 1year after heart transplantation for all-cause and cardiac mortality and development of allograft vasculopathy. Transplantation 2007: 84: 149.
42. Everett JP, Hershberger RE, Norman DJ et al. Prolonged cytomegalovirus infection with viremia is associated with development of cardiac allograft vasculopathy. J Heart Lung Transplant 1992: 11: S133.
43. Cunningham DA, Crisp SJ, Barbir M, Lazem F, Dunn MJ, Yacoub MH. Donor ACE gene polymorphism: a genetic risk factor for accelerated coronary sclerosis following cardiac transplantation. Eur Heart J 1998: 19: 319.
44. Martinez-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.
45. Miller WL, Edwards BS, Kremers WK et al. Elevated donor troponin levels are associated with a lower frequency of allograft vasculopathy. J Heart Lung Transplant 2005: 24: 2075.
46. 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.
47. Lindelow B, Bergh C, Lamm C, Andersson B, Waagstein F. Graft coronary artery disease is strongly related to the aetiology of heart failure and cellular rejections. Eur Heart J 1999: 20: 1326.
48. Drinkwater DC, Rudis E, Laks H et al. University of Wisconsin solution versus Stanford cardioplegic solution and the development of cardiac allograft vasculopathy. J Heart Lung Transplant 1995: 14: 891.
49. Gaudin PB, Rayburn BK, Hutchins GM et al. Peritransplant injury to the myocardium associated with the development of accelerated arteriosclerosis in heart transplant recipients. Am J Surg Pathol 1994: 18: 338.
50. Mangiavacchi M, Frigerio M, Gronda E et al. Acute rejection and cytomegalovirus infection: correlation with cardiac allograft vasculopathy. Transplant Proc 1995: 27: 1960.
51. McDonald K, Rector TS, Braunlin EA, Kubo SH, Olivari MT. Association of coronary artery disease in cardiac transplant recipients with cytomegalovirus infection. Am J Cardiol 1989: 64: 359.
52. Rickenbacher PR, Pinto FJ, Lewis NP et al. Correlation of donor characteristics with transplant coronary artery disease as assessed by intracoronary ultrasound and coronary angiography. Am J Cardiol 1995: 76: 340.
53. Arora S, Jenum PA, Aukrust P et al. Pre-transplant Toxoplasma gondii seropositivity among heart transplant recipients is associated with an increased risk of all-cause and cardiac mortality. J Am Coll Cardiol 2007: 50: 1967.
54. Rickenbacher PR, Kemna MS, Pinto FJ et al. Coronary artery intimal thickening in the transplanted heart: an in vivo intracoronary ultrasound study of immunologic and metabolic risk factors. Transplantation 1996: 61: 46.
55. Kobashigawa JA, Starling RC, Mehra MR et al. Multicenter retrospective analysis of cardiovascular risk factors affecting long-term outcome of de novo cardiac transplant recipients. J Heart Lung Transplant 2006: 25: 1063.
56. Vasilescu ER, Ho EK, De La Torre L et al. Anti-HLA antibodies in heart transplantation. Transpl Immunol 2004: 12: 177.
57. Zerbe T, Uretsky B, Kormos R et al. Graft atherosclerosis: effects of cellular rejection and human lymphocyte antigen. J Heart Lung Transplant 1992: 11: S104.
58. Mehra MR, Crespo-Leiro MG, Dipchand A, Ensminger SM, Hiemann NE, Kobashigawa JA. International Society for Heart and Lung Transplantation working formulation of a standardized nomenclature for cardiac allograft vasculopathy-2010. J Heart Lung Transplant 2010: 29: 717.
59. Costanzo MR, Dipchand A, Starling R et al. The International Society of Heart and Lung Transplantation guidelines for the care of heart transplant recipients. J Heart Lung Transplant 2010: 29: 914.
60. Johnson DE, Aldermann EL, Schroeder JS et al. Transplant coronary artery disease: histopathologic correlations with angiographic morphology. J Am Coll Cardiol 1991: 17: 449.
61. Deeks JJ, Higgins JPT, Altman DG. Analysing data and undertaking meta-analyses. In: Higgins JPT, Green S, eds. Cochrane Handbook for Systematic Reviews of Interventions Version 5.0.2 [updated September 2009]. The Cochrane Collaboration, 2009: Chapter 9, Section 9.4.11. Available from
62. Gao SZ, Alderman EL, Schroeder JS, Silverman JE, Hunt SA. Accelerated coronary vascular disease in the heart transplant patient: coronary arteriographic findings. JAMA 1988: 12: 334.
63. He JQ, Gaur LK, Stempien-Otero A et al. Genetic variants of the hemostatic system and development of transplant coronary artery disease. J Heart Lung Transplant 2002: 21: 629.
64. Kapadia SR, Nissen SE, Ziada KM et al. Impact of lipid abnormalities in development and progression of transplant coronary disease: a serial intravascular ultrasound study. J Am Coll Cardiol 2001: 38: 206.
65. Jurcevic S, Ainsworth ME, Pomerance A et al. Antivimentin antibodies are an independent predictor of transplant-associated coronary artery disease after cardiac transplantation. Transplantation 2001: 71: 886.
66. Bayliss J, Bailey M, Leet A, Stein AN, Thomson NM, Mclean CA. Late onset antibody-mediated rejection and endothelial localization of vascular endothelial growth factor are associated with development of cardiac allograft vasculopathy. Transplantation 2008: 86: 991.
67. Bayliss J, Maguire JA, Bailey M et al. Increased vascular endothelial growth factor mRNA in endomyocardial biopsies from allografts demonstrating severe acute rejection: a longitudinal study. Transpl Immunol 2008: 18: 264.
68. Kaczmarek I, Ertl B, Schmauss D et al. Preventing cardiac allograft vasculopathy: long-term beneficial effects of mycophenolate mofetil. J Heart Lung Transplant 2006: 25: 550.
69. Haji SA, Starling RC, Avery RK et al. Donor hepatitis-C seropositivity is an independent risk factor for the development of accelerated coronary vasculopathy and predicts outcome after cardiac transplantation. J Heart Lung Transplant 2004: 23: 277.
70. Raichlin E, Villarraga HR, Chandrasekaran K et al. Cardiac allograft remodeling after heart transplantation is associated with increased graft vasculopathy and mortality. Am J Transplant 2009: 9: 132.
71. Kittleson MM, Bead V, Fradley M et al. Elevated uric acid levels predict allograft vasculopathy in cardiac transplant recipients. J Heart Lung Transplant 2007: 26: 498.
72. Yamani MH, Taylor DO, Rodriguez ER et al. Transplant vasculopathy is associated with increased AlloMap gene expression score. J Heart Lung Transplant 2007: 26: 403.
73. Radovancevic B, Golino A, Vrtovec B et al. Is bridging to transplantation with a left ventricular assist device a risk factor for transplant coronary artery disease? J Heart Lung Transplant 2005: 24: 703.
74. Labarrere CA, Nelson DR, Cox CJ, Pitts D, Kirlin P, Halbrook H. Cardiac-specific troponin I levels and risks of coronary artery disease and graft failure following heart transplantation. J Am Med Assoc 2000: 284: 457.
75. Labarrere CA, Pitts D, Nelson DR, Faulk WP. Vascular tissue plasminogen activator and the development of coronary artery disease in heart-transplant recipients. N Engl J Med 1995: 333: 1111.
76. Ratkovec RM, Wray RB, Renlund DG et al. Influence of corticosteroid-free maintenance immunosuppression on allograft coronary artery disease after cardiac transplantation. J Thorac Cardiovasc Surg 1990: 100: 6.
77. Hammond EH, Yowell RL, Price GD et al. Vascular rejection and its relationship to allograft coronary artery disease. J Heart Lung Transplant 1992: 11: S111.
78. Arora S, Aukrust PI, Ueland T, Broch K, Simonsen S, Gude E. Elevated serum uric acid levels following heart transplantation predict all-cause and cardiac mortality. Eur J Heart Fail 2009: 11: 1005.