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Journal of Cardiovascular Translational Research
Published in: Journal of Cardiovascular Translational Research 2/2013

01-04-2013

Endothelial Dysfunction and Cardiac Allograft Vasculopathy

Authors: Monica Colvin-Adams, Nonyelum Harcourt, Daniel Duprez

Published in: Journal of Cardiovascular Translational Research | Issue 2/2013

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Abstract

Cardiac allograft vasculopathy remains a major challenge to long-term survival after heart transplantation. Endothelial injury and dysfunction, as a result of multifactorial immunologic and nonimmunologic insults in the donor and the recipient, are prevalent early after transplant and may be precursors to overt cardiac allograft vasculopathy. Current strategies for managing cardiac allograft vasculopathy, however, rely on the identification and treatment of established disease. Improved understanding of mechanisms leading to endothelial dysfunction in heart transplant recipients may provide the foundation for the development of sensitive screening techniques and preventive therapies.
Literature
1.
Topkara, V. K., Dang, N. C., John, R., Cheema, F. H., Barbato, R., Cavallo, M., et al. (2005). A decade experience of cardiac retransplantation in adult recipients. The Journal of Heart and Lung Transplantation, 24, 1745–1750.
2.
Aranda, J. M., Jr., & Hill, J. (2000). Cardiac transplant vasculopathy. Chest, 118, 1792–1800.
3.
Rickenbacher, P. R., Pinto, F. J., Chenzbraun, A., Botas, J., Lewis, N. P., Alderman, E. L., et al. (1995). Incidence and severity of transplant coronary artery disease early and up to 15 years after transplantation as detected by intravascular ultrasound. Journal of the American College of Cardiology, 25, 171–177.
4.
Stehlik, J., Edwards, L. B., Kucheryavaya, A. Y., Aurora, P., Christie, J. D., Kirk, R., et al. (2010). The registry of the International Society for Heart and Lung Transplantation: twenty-seventh official adult heart transplant report—2010. The Journal of Heart and Lung Transplantation, 29, 1089–1103.
5.
Stehlik, J., Edwards, L. B., Kucheryavaya, A. Y., Benden, C., Christie, J. D., Dobbels, F., et al. (2011). The registry of the international society for heart and lung transplantation: twenty-eighth adult heart transplant report–2011. The Journal of Heart and Lung Transplantation, 30, 1078–1094.
6.
Rahmani, M., Cruz, R., Granville, D., & McManus, B. (2006). Allograft vasculopathy versus atherosclerosis. Circulation Research, 99, 801–815.
7.
Furchgott, R., & Zawadzki, J. (1980). The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature, 288, 373–376.
8.
Verma, S., Buchanan, M. R., & Anderson, T. J. (2003). Endothelial function testing as a biomarker of vascular disease. Circulation, 108, 2054–2059.
9.
Drexler, H., Fischell, T. A., Pinto, F. J., Chenzbraun, A., Botas, J., Cooke, J. P., et al. (1994). Effect of l-arginine on coronary endothelial function in cardiac transplant recipients. Relation to vessel wall morphology. Circulation, 89, 1615–1623.
10.
Tiefenbacher, C. P., & Kreuzer, J. (2003). Nitric oxide-mediated endothelial dysfunction—is there need to treat? Current Vascular Pharmacology, 1, 123–133.
11.
Bahlmann, F., DeGroot, K., Duckert, T., Niemczyk, E., Bahlmann, E., Boehm, S., et al. (2003). Endothelial progenitor cell proliferation and differentiation is regulated by erythropoietin. Kidney International, 64, 1648–1652.
12.
Medawar, P. B. (1965). Transplantation of tissues and organs: introduction. British Medical Bulletin, 21, 97–99.
13.
Ross, R. (1993). The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature, 362, 801–809.
14.
Minami, E., Laflamme, M. A., Saffitz, J. E., & Murry, C. E. (2005). Extracardiac progenitor cells repopulate most major cell types in the transplanted human heart. Circulation, 112, 2951–2958.
15.
Kapessidou, Y., Habran, C., Buonocore, S., Flamand, V., Barvais, L., Goldman, M., et al. (2006). The replacement of graft endothelium by recipient-type cells conditions allograft rejection mediated by indirect pathway cd4+ t cells. Transplantation, 82, 582–591.
16.
O’Connell, J. B., Renlund, D. G., Bristow, M. R., & Hammond, E. H. (1991). Detection of allograft endothelial cells of recipient origin following abo-compatible, nonidentical cardiac transplantation. Transplantation, 51, 438–442.
17.
Glaser, R., Lu, M. M., Narula, N., & Epstein, J. A. (2002). Smooth muscle cells, but not myocytes, of host origin in transplanted human hearts. Circulation, 106, 17–19.
18.
Quaini, F., Urbanek, K., Beltrami, A. P., Finato, N., Beltrami, C. A., Nadal-Ginard, B., et al. (2002). Chimerism of the transplanted heart. The New England Journal of Medicine, 346, 5–15.
19.
Simper, D., Wang, S., Deb, A., Holmes, D., McGregor, C., Frantz, R., et al. (2003). 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, 108, 143–149.
20.
Hillebrands, J. L., Klatter, F. A., van den Hurk, B. M. H., Popa, E. R., Nieuwenhuis, P., & Rozing, J. (2001). Origin of neointimal endothelium and alpha-actin-positive smooth muscle cells in transplant arteriosclerosis. Journal of Clinical Investigation, 107, 1411–1422.
21.
Hu, Y., Davison, F., Ludewig, B., Erdel, M., Mayr, M., Url, M., et al. (2002). Smooth muscle cells in transplant atherosclerotic lesions are originated from recipients, but not bone marrow progenitor cells. Circulation, 106, 1834–1839.
22.
Sinclair, R. (1972). Origin of endothelium in human renal allografts. British Medical Journal, 4, 15–16.
23.
Lagaaij, E. L., Cramer-Knijnenburg, G. F., van Kemenade, F. J., van Es, L. A., Bruijn, J. A., & van Krieken, J. H. J. M. (2001). Endothelial cell chimerism after renal transplantation and vascular rejection. The Lancet, 357, 33–37.
24.
Atkinson, C., Horsley, J., Rhind-Tutt, S., Charman, S., Phillpotts, C. J., Wallwork, J., et al. (2004). Neointimal smooth muscle cells in human cardiac allograft coronary artery vasculopathy are of donor origin. The Journal of Heart and Lung Transplantation, 23, 427–435.
25.
Hruban, R., Long, P., Perlman, E., Hutchins, G., Baumgartner, W., Baughman, K., et al. (1993). Fluorescence in situ hybridization for the y-chromosome can be used to detect cells of recipient origin in allografted hearts following cardiac transplantation. The American Journal of Pathology, 142, 975.
26.
Shimizu, K., Sugiyama, S., Aikawa, M., Fukumoto, Y., Rabkin, E., Libby, P., et al. (2001). Host bone-marrow cells are a source of donor intimal smooth-muscle-like cells in murine aortic transplant arteriopathy. Nature Medicine, 7, 738–741.
27.
Li, J., Han, X., Jiang, J., Zhong, R., Williams, G. M., Pickering, J. G., et al. (2001). Vascular smooth muscle cells of recipient origin mediate intimal expansion after aortic allotransplantation in mice. The American Journal of Pathology, 158, 1943.
28.
Valantine, H. A. (2003). Cardiac allograft vasculopathy: central role of endothelial injury leading to transplant "atheroma". Transplantation, 76, 891–899.
29.
Caforio, A. L. P., Tona, F., Fortina, A. B., Angelini, A., Piaserico, S., Gambino, A., et al. (2004). Immune and nonimmune predictors of cardiac allograft vasculopathy onset and severity: multivariate risk factor analysis and role of immunosuppression. American Journal of Transplantation, 4, 962–970.
30.
Nagji, A. S., Hranjec, T., Swenson, B. R., Kern, J. A., Bergin, J. D., Jones, D. R., et al. (2010). Donor age is associated with chronic allograft vasculopathy after adult heart transplantation: Implications for donor allocation. The Annals of Thoracic Surgery, 90, 168–175.
31.
Pratschke, J., Neuhaus, P., & Tullius, S. (2005). What can be learned from brain–death models? Transplant International, 18, 15–21.
32.
Rogers, N., & Lechler, R. (2001). Allorecognition. American Journal of Transplantation, 1, 97–102.
33.
Adams, D., Russell, M., Hancock, W., Sayegh, M., Wyner, L., & Karnovsky, M. (1993). Chronic rejection in experimental cardiac transplantation: studies in the lewis-f344 model. Immunology Reviews, 134, 5–19.
34.
Ciubotariu, R., Colovai, A., Pennesi, G., Liu, Z., Smith, D., Berlocco, P., et al. (1998). Specific suppression of human cd4+ th cell responses to pig mhc antigens by cd8+ cd28− regulatory t cells. The Journal of Immunology, 161, 5193–5202.
35.
Salomon, R. N., Hughes, C., Schoen, F., Payne, D., Pober, J., & Libby, P. (1991). Human coronary transplantation-associated arteriosclerosis. Evidence for a chronic immune reaction to activated graft endothelial cells. The American Journal of Pathology, 138, 791.
36.
Zhang, X., Kelemen, S., & Eisen, H. (2000). Quantitative assessment of cell adhesion molecule gene expression in endomyocardial biopsy specimens from cardiac transplant recipients using competitive polymerase chain reaction. Transplantation, 70, 505–513.
37.
Nabel, E., Shum, L., Pompili, V., Yang, Z., San, H., Shu, H., et al. (1993). Direct transfer of transforming growth factor beta 1 gene into arteries stimulates fibrocellular hyperplasia. Proceedings of the National Academy of Sciences of the United States of America, 90, 10759–10763.
38.
Weis, M., & Cooke, J. (2003). Cardiac allograft vasculopathy and dysregulation of the no synthase pathway. Arteriosclerosis, Thrombosis, and Vascular Biology, 23, 567–575.
39.
Prasad, A., Zhu, J., Halcox, J. P. J., Waclawiw, M. A., Epstein, S. E., & Quyyumi, A. A. (2002). Predisposition to atherosclerosis by infections. Circulation, 106, 184–190.
40.
Valantine, H. A. (1999). Role of cmv in transplant coronary artery disease and survival after heart transplantation. Transplant Infectious Disease, 1(Suppl 1), 25–30.
41.
Speir, E., Yu, Z. X., Ferrans, V. J., Huang, E. S., & Epstein, S. E. (1998). Aspirin attenuates cytomegalovirus infectivity and gene expression mediated by cyclooxygenase-2 in coronary artery smooth muscle cells. Circulation Research, 83, 210–216.
42.
van Dorp, W., Jonges, E., Bruggeman, C., Daha, M., van Es, L., & van Der Woude, F. (1989). Direct induction of mhc class I, but not class II, expression on endothelial cells by cytomegalovirus infection. Transplantation, 48, 469–472.
43.
Koskinen, P. (1993). The association of the induction of vascular cell adhesion molecule-1 with cytomegalovirus antigenemia in human heart allografts. Transplantation, 56, 1103–1108.
44.
Hosenpud, J., Chou, S., & Wagner, C. (1991). Cytomegalovirus-induced regulation of major histocompatibility complex class i antigen expression in human aortic smooth muscle cells. Transplantation, 52, 896–903.
45.
Streblow, D., Kreklywich, C., Yin, Q., De La Melena, V., Corless, C., Smith, P., et al. (2003). Cytomegalovirus-mediated upregulation of chemokine expression correlates with the acceleration of chronic rejection in rat heart transplants. Journal of Virology, 77, 2182–2194.
46.
Weis, M., Kledal, T. N., Lin, K. Y., Panchal, S. N., Gao, S. Z., Valantine, H. A., et al. (2004). Cytomegalovirus infection impairs the nitric oxide synthase pathway: role of asymmetric dimethylarginine in transplant arteriosclerosis. Circulation, 109, 500–505.
47.
Simmonds, J., Fenton, M., Dewar, C., Ellins, E., Storry, C., Cubitt, D., et al. (2008). Endothelial dysfunction and cytomegalovirus replication in pediatric heart transplantation. Circulation, 117, 2657–2661.
48.
Petrakopoulou, P., Kübrich, M., Pehlivanli, S., Meiser, B., Reichart, B., von Scheidt, W., et al. (2004). Cytomegalovirus infection in heart transplant recipients is associated with impaired endothelial function. Circulation, 110, II-207–II-212.
49.
Grattan, M., Moreno-Cabral, C., Starnes, V., Oyer, P., Stinson, E., & Shumway, N. (1989). Cytomegalovirus infection is associated with cardiac allograft rejection and atherosclerosis. JAMA: The Journal of the American Medical Association, 261, 3561–3566.
50.
Potena, L., & Valantine, H. A. (2007). Cytomegalovirus-associated allograft rejection in heart transplant patients. Current Opinion in Infectious Diseases, 20, 425–431.
51.
Potena, L., Grigioni, F., Ortolani, P., Magnani, G., Marrozzini, C., Falchetti, E., et al. (2003). Relevance of cytomegalovirus infection and coronary-artery remodeling in the first year after heart transplantation: a prospective three-dimensional intravascular ultrasound study. Transplantation, 75, 839.
52.
Zakliczynski, M., Boguslawska, J., Wojniak, E., Zakliczynska, H., Ciesla, D., Nozynski, J., et al. (2011). In the era of the universal use of statins dyslipidemia’s are still common in heart transplant recipients: a cross-sectional study. Transplantation Proceedings, 43(8), 3071–3073.
53.
Stehlik, J., Edwards, L. B., Kucheryavaya, A. Y., Benden, C., Christie, J. D., Dobbels, F., et al. (2011). The registry of the International Society for Heart and Lung Transplantation: twenty-eighth adult heart transplant report—2011. The Journal of Heart and Lung Transplantation, 30, 10781094.
54.
Hilbrands, L. B., Demacker, P., Hoitsma, A. J., Stalenhoef, A., & Koene, R. (1995). The effects of cyclosporine and prednisone on serum lipid and (apo) lipoprotein levels in renal transplant recipients. Journal of the American Society of Nephrology, 5, 2073–2081.
55.
Kasiske, B., Tortorice, K., Heim-Duthoy, K., Awni, W., & Rao, K. (1991). The adverse impact of cyclosporine on serum lipids in renal transplant recipients. American Journal of Kidney Diseases: The Official Journal of the National Kidney Foundation, 17, 700.
56.
Lázaro, I., Bonet, L. A., López, J. M., Lacuesta, E. S., Martínez-Dolz, L., Ramón-Llín, J. A., et al. (2008). Influence of traditional cardiovascular risk factors in the recipient on the development of cardiac allograft vasculopathy after heart transplantation. Transplantation Proceedings, 40(9), 3056–3057.
57.
Escobar, A., Ventura, H. O., Stapleton, D. D., Mehra, M. R., Ramee, S. R., Collins, T. J., et al. (1994). Cardiac allograft vasculopathy assessed by intravascular ultrasonography and nonimmunologic risk factors. The American Journal of Cardiology, 74, 1042–1046.
58.
Eich, D., Thompson, J., Ko, D., Hastillo, A., Lower, R., Katz, S., et al. (1991). Hypercholesterolemia in long-term survivors of heart transplantation: an early marker of accelerated coronary artery disease. The Journal of heart and lung transplantation: the official publication of the International Society for Heart Transplantation., 10, 45.
59.
Kobashigawa, J. A., Moriguchi, J. D., Laks, H., Wener, L., Hage, A., Hamilton, M. A., et al. (2005). Ten-year follow-up of a randomized trial of pravastatin in heart transplant patients. The Journal of Heart and Lung Transplantation, 24, 1736–1740.
60.
Mehra M, Raval N. (2004). Metaanalysis of statins and survival in de novo cardiac transplantation. Transplantation Proceedings, 36, 1539–1541
61.
Mehra, M. R., Uber, P. A., Vivekananthan, K., Solis, S., Scott, R. L., Park, M. H., et al. (2002). Comparative beneficial effects of simvastatin and pravastatin on cardiac allograft rejection and survival. Journal of the American College of Cardiology, 40, 1609–1614.
62.
Wenke, K., Meiser, B., Thiery, J., Nagel, D., von Scheidt, W., Krobot, K., et al. (2003). Simvastatin initiated early after heart transplantation: 8-year prospective experience. Circulation, 107, 93–97.
63.
Weis, M., Pehlivanli, S., Meiser, B., & von Scheidt, W. (2001). Simvastatin treatment is associated with improvement in coronary endothelial function and decreased cytokine activation in patients after heart transplantation. Journal of the American College of Cardiology, 38, 814–818.
64.
Shimizu, K., Aikawa, M., Takayama, K., Libby, P., & Mitchell, R. N. (2003). Direct anti-inflammatory mechanisms contribute to attenuation of experimental allograft arteriosclerosis by statins. Circulation, 108, 2113–2120.
65.
Holm, T., Andreassen, A. K., Ueland, T., Kjekshus, J., Froland, S. S., Kjekshus, E., et al. (2001). Effect of pravastatin on plasma markers of inflammation and peripheral endothelial function in male heart transplant recipients. The American Journal of Cardiology, 87, 815–818. A819.
66.
Nieuwenhuis, M. G., & Kirkels, J. H. (2001). Predictability and other aspects of post-transplant diabetes mellitus in heart transplant recipients. The Journal of Heart and Lung Transplantation, 20, 703–708.
67.
Depczynski, B., Daly, B., Campbell, L., Chisholm, D., & Keogh, A. (2000). Predicting the occurrence of diabetes mellitus in recipients of heart transplants. Diabetic Medicine, 17, 15–19.
68.
Raichlin, E. R., McConnell, J. P., Lerman, A., Kremers, W. K., Edwards, B. S., Kushwaha, S. S., et al. (2007). Systemic inflammation and metabolic syndrome in cardiac allograft vasculopathy. The Journal of Heart and Lung Transplantation, 26, 826–833.
69.
Hirohata, A., Nakamura, M., Waseda, K., Honda, Y., Lee, D. P., Vagelos, R. H., et al. (2007). Changes in coronary anatomy and physiology after heart transplantation. The American Journal of Cardiology, 99, 1603–1607.
70.
Hollenberg, S. M., Klein, L. W., Parrillo, J. E., Scherer, M., Burns, D., Tamburro, P., et al. (2001). Coronary endothelial dysfunction after heart transplantation predicts allograft vasculopathy and cardiac death. Circulation, 104, 3091–3096.
71.
Fish, R. D., Nabel, E. G., Selwyn, A. P., Ludmer, P. L., Mudge, G. H., Kirshenbaum, J. M., et al. (1988). Responses of coronary arteries of cardiac transplant patients to acetylcholine. The Journal of Clinical Investigation, 81, 21–31.
72.
Davis, S. F., Yeung, A. C., Meredith, I. T., Charbonneau, F., Ganz, P., Selwyn, A. P., et al. (1996). Early endothelial dysfunction predicts the development of transplant coronary artery disease at 1 year posttransplant. Circulation, 93, 457–462.
73.
Hollenberg, S. M., Klein, L. W., Parrillo, J. E., Scherer, M., Burns, D., Tamburro, P., et al. (2004). Changes in coronary endothelial function predict progression of allograft vasculopathy after heart transplantation. The Journal of Heart and Lung Transplantation, 23, 265–271.
74.
Weis, M., Hartmann, A., Olbrich, H. G., Hör, G., & Zeiher, A. M. (1998). Prognostic significance of coronary flow reserve on left ventricular ejection fraction in cardiac transplant recipients. Transplantation, 65, 103.
75.
Fearon, W. F., Shah, M., Ng, M., Brinton, T., Wilson, A., Tremmel, J. A., et al. (2008). Predictive value of the index of microcirculatory resistance in patients with st-segment elevation myocardial infarction. Journal of the American College of Cardiology, 51, 560–565.
76.
Hillebrands, J. L., Klatter, F. A., van Dijk, W. D., & Rozing, J. (2002). Bone marrow does not contribute substantially to endothelial-cell replacement in transplant arteriosclerosis. Nature Medicine, 8, 194–195.
77.
Costanzo, M. R., Dipchand, A., Starling, R., Anderson, A., Chan, M., Desai, S., et al. (2010). The international society of heart and lung transplantation guidelines for the care of heart transplant recipients. The Journal of Heart and Lung Transplantation, 29, 914–956.
78.
Barbir, M., Lazem, F., Banner, N., Mitchell, A., & Yacoub, M. (1997). The prognostic significance of non-invasive cardiac tests in heart transplant recipients. European Heart Journal, 18, 692–696.
79.
Barbir, M., Lazem, F., Bowker, T., Ludman, P., Banner, N., Mitchell, A., et al. (1997). Determinants of transplant-related coronary calcium detected by ultrafast computed tomography scanning. The American Journal of Cardiology, 79, 1606–1609.
80.
Gao, S. Z., Alderman, E., Schroeder, J., Hunt, S., Wiederhold, V., & Stinson, E. (1990). Progressive coronary luminal narrowing after cardiac transplantation. Circulation, 82, IV269.
81.
St Goar, F., Pinto, F., Alderman, E., Valantine, H., Schroeder, J., Gao, S., et al. (1992). Intracoronary ultrasound in cardiac transplant recipients. In vivo evidence of “angiographically silent” intimal thickening. Circulation, 85, 979.
82.
O’Neill, B. J., Pflugfelder, P. W., Singh, N. R., Menkis, A. H., McKenzie, F. N., & Kostuk, W. J. (1989). Frequency of angiographic detection and quantitative assessment of coronary arterial disease one and three years after cardiac transplantation. The American Journal of Cardiology, 63, 1221–1226.
83.
Kobashigawa, J. A., Tobis, J. M., Starling, R. C., Tuzcu, E. M., Smith, A. L., Valantine, H. A., et al. (2005). Multicenter intravascular ultrasound validation study among heart transplant recipients: outcomes after five years. Journal of the American College of Cardiology, 45, 1532–1537.
84.
Tuzcu, E. M., Kapadia, S. R., Sachar, R., Ziada, K. M., Crowe, T. D., Feng, J., et al. (2005). Intravascular ultrasound evidence of angiographically silent progression in coronary atherosclerosis predicts long-term morbidity and mortality after cardiac transplantation. Journal of the American College of Cardiology, 45, 1538–1542.
85.
Jang, I. K., Bouma, B. E., Kang, D. H., Park, S. J., Park, S. W., Seung, K. B., et al. (2002). Visualization of coronary atherosclerotic plaques in patients using optical coherence tomography: comparison with intravascular ultrasound. Journal of the American College of Cardiology, 39, 604–609.
86.
Garrido IP, García-Lara J, Pinar E, Pastor-Pérez F, Sánchez-Mas J, Valdés-Chavarri M, Pascual-Figal DA (2012) Optical coherence tomography and highly sensitivity troponin t for evaluating cardiac allograft vasculopathy. The American Journal of Cardiology, 110, 655–661
87.
Mehra, M. R., Crespo-Leiro, M. G., Dipchand, A., Ensminger, S. M., Hiemann, N. E., Kobashigawa, J. A., et al. (2010). International society for heart and lung transplantation working formulation of a standardized nomenclature for cardiac allograft vasculopathy—2010. The Journal of Heart and Lung Transplantation, 29, 717–727.
88.
Gullestad, L., Simonsen, S., Ueland, T., Holm, T., Aass, H., Andreassen, A. K., et al. (1999). Possible role of proinflammatory cytokines in heart allograft coronary artery disease. The American Journal of Cardiology, 84, 999–1003.
89.
Spes, C. H., Klauss, V., Rieber, J., Schnaack, S. D., Tammen, A. R., Uberfuhr, P., et al. (1999). Functional and morphological findings in heart transplant recipients with a normal coronary angiogram: an analysis by dobutamine stress echocardiography, intracoronary doppler and intravascular ultrasound. The Journal of Heart and Lung Transplantation, 18, 391–398.
90.
Bacal, F., Moreira, L., Souza, G., Rodrigues, A. C., Fiorelli, A., Stolf, N., et al. (2004). Dobutamine stress echocardiography predicts cardiac events or death in asymptomatic patients long-term after heart transplantation: 4-year prospective evaluation. The Journal of Heart and Lung Transplantation, 23, 1238–1244.
91.
Eroglu, E., D’hooge, J., Sutherland, G. R., Marciniak, A., Thijs, D., Droogne, W., et al. (2008). Quantitative dobutamine stress echocardiography for the early detection of cardiac allograft vasculopathy in heart transplant recipients. Heart, 94, e3.
92.
Gregory, S. A., Ferencik, M., Achenbach, S., Yeh, R. W., Hoffmann, U., Inglessis, I., et al. (2006). Comparison of sixty-four-slice multidetector computed tomographic coronary angiography to coronary angiography with intravascular ultrasound for the detection of transplant vasculopathy. The American Journal of Cardiology, 98, 877–884.
93.
Sigurdsson, G., Carrascosa, P., Yamani, M. H., Greenberg, N. L., Perrone, S., Lev, G., et al. (2006). Detection of transplant coronary artery disease using multidetector computed tomography with adaptative multisegment reconstruction. Journal of the American College of Cardiology, 48, 772.
94.
Muehling, O. M., Wilke, N. M., Panse, P., Jerosch-Herold, M., Wilson, B. V., Wilson, R. F., et al. (2003). Reduced myocardial perfusion reserve and transmural perfusiongradient in heart transplant arteriopathyassessed by magnetic resonance imaging. Journal of the American College of Cardiology, 42, 1054.
95.
Colvin-Adams, M., Petros, S., Raveendran, G., Missov, E., Medina, E., & Wilson, R. (2011). Qualitative perfusion cardiac magnetic resonance imaging lacks sensitivity in detecting cardiac allograft vasculopathy. Cardiology Research., 2, 282–287.
96.
Schnetzler, B., Drobinski, G., Dorent, R., Camproux, A. C., Ghossoub, J. J., Thomas, D., et al. (2000). The role of percutaneous transluminal coronary angioplasty in heart transplant recipients. The Journal of Heart and Lung Transplantation, 19, 557–565.
97.
Treasure, C. B., Klein, J. L., Weintraub, W. S., Talley, J. D., Stillabower, M. E., Kosinski, A. S., et al. (1995). Beneficial effects of cholesterol-lowering therapy on the coronary endothelium in patients with coronary artery disease. The New England Journal of Medicine, 332, 481–487.
98.
Anderson, T. J., Uehata, A., Gerhard, M. D., Meredith, I. T., Knab, S., Delagrange, D., et al. (1995). Close relation of endothelial function in the human coronary and peripheral circulations. Journal of the American College of Cardiology, 26, 1235–1241.
99.
Blum, A., & Shamburek, R. (2009). The pleiotropic effects of statins on endothelial function, vascular inflammation, immunomodulation and thrombogenesis. Atherosclerosis, 203, 325–330.
100.
Laufs, U., La Fata, V., Plutzky, J., & Liao, J. K. (1998). Upregulation of endothelial nitric oxide synthase by hmg coa reductase inhibitors. Circulation, 97, 1129–1135.
101.
Valantine, H. (2005). Prevention of cardiac allograft vasculopathy with certican (everolimus): the Stanford University experience within the certican phase III clinical trial. The Journal of Heart and Lung Transplantation, 24, S191–S195. discussion S210-191.
102.
Eisen, H. J., Tuzcu, E. M., Dorent, R., Kobashigawa, J., Mancini, D., Valantine-von Kaeppler, H. A., et al. (2003). Everolimus for the prevention of allograft rejection and vasculopathy in cardiac-transplant recipients. The New England Journal of Medicine, 349, 847–858.
103.
Mancini, D., Pinney, S., Burkhoff, D., LaManca, J., Itescu, S., Burke, E., et al. (2003). Use of rapamycin slows progression of cardiac transplantation vasculopathy. Circulation, 108, 48–53.
104.
Raichlin, E., Prasad, A., Kremers, W. K., Edwards, B. S., Rihal, C. S., Lerman, A., et al. (2009). Sirolimus as primary immunosuppression is associated with improved coronary vasomotor function compared with calcineurin inhibitors in stable cardiac transplant recipients. European Heart Journal, 30, 1356.
105.
Keogh, A., Richardson, M., Ruygrok, P., Spratt, P., Galbraith, A., O’Driscoll, G., et al. (2004). Sirolimus in de novo heart transplant recipients reduces acute rejection and prevents coronary artery disease at 2 years: a randomized clinical trial. Circulation, 110, 2694–2700.
106.
Kuppahally, S., Al-Khaldi, A., Weisshaar, D., Valantine, H., Oyer, P., Robbins, R., et al. (2006). Wound healing complications with de novo sirolimus versus mycophenolate mofetil–based regimen in cardiac transplant recipients. American Journal of Transplantation, 6, 986–992.
107.
Aliabadi, A., Pohanka, E., Seebacher, G., Dunkler, D., Kammerstätter, D., Wolner, E., et al. (2008). Development of proteinuria after switch to sirolimus–based immunosuppression in long–term cardiac transplant patients. American Journal of Transplantation, 8, 854–861.
108.
Manito, N., Kaplinsky, E. J., Bernat, R., Roca, J., Castells, E., Serrano, T., et al. (2004). Fatal interstitial pneumonitis associated with sirolimus therapy in a heart transplant recipient. The Journal of Heart and Lung Transplantation, 23, 780–782.
109.
Bader, F. M., Kfoury, A. G., Gilbert, E. M., Barry, W. H., Humayun, N., Hagan, M. E., et al. (2006). Percutaneous coronary interventions with stents in cardiac transplant recipients. The Journal of Heart and Lung Transplantation, 25, 298–301.
110.
Benza, R. L., Zoghbi, G. J., Tallaj, J., Brown, R., Kirklin, J. K., Hubbard, M., et al. (2004). Palliation of allograft vasculopathy with transluminal angioplasty: a decade of experience. Journal of the American College of Cardiology, 43, 1973.
111.
Patel, V., Radovancevic, B., Springer, W., Frazier, O., Massin, E., Benrey, J., et al. (1997). Revascularization procedures in patients with transplant coronary artery disease1. European Journal of Cardio-Thoracic Surgery, 11, 895–901.
112.
Halle, A. A., DiSciascio, G., Massin, E. K., Wilson, R. F., Johnson, M. R., Sullivan, H. J., et al. (1995). Coronary angioplasty, atherectomy and bypass surgery in cardiac transplant recipients. Journal of the American College of Cardiology, 26, 120–128.
113.
Musci, M., Loebe, M., Wellnhofer, E., Meyer, R., Pasic, M., Hummel, M., et al. (1998). Coronary angioplasty, bypass surgery, and retransplantation in cardiac transplant patients with graft coronary disease. Thoracic and Cardiovascular Surgeon, 46, 268–274.
114.
Srivastava, R., Keck, B. M., Bennett, L. E., & Hosenpud, J. D. (2000). The results of cardiac retransplantation: an analysis of the joint international society for heart and lung transplantation/united network for organ sharing thoracic registry. Transplantation, 70, 606.
115.
Gao, S. Z., Schroeder, J. S., Hunt, S., & Stinson, E. B. (1988). Retransplantation for severe accelerated coronary artery disease in heart transplant recipients. The American Journal of Cardiology, 62, 876–881.
116.
Yeboah, J., Crouse, J., Hsu, F., Burke, G., & Herrington, D. (2007). Brachial flow-mediated dilation predicts incident cardiovascular events in older adults: the cardiovascular health study. Circulation, 115, 2390–2397.
117.
Kuvin, J. T., Patel, A. R., Sliney, K. A., Pandian, N. G., Rand, W. M., Udelson, J. E., et al. (2001). Peripheral vascular endothelial function testing as a noninvasive indicator of coronary artery disease. Journal of the American College of Cardiology, 38, 1843–1849.
118.
Roig, E., Cuppoletti, A., Masotti, M., Kianco, R., Vallejos, I., Sitges, M., et al. (2009). Assessment of peripheral endothelial-dependent vasodilatation within the first year after heart transplantation. The Journal of Heart and Lung Transplantation, 28, 299–304.
119.
Kubo, S. H., Rector, T. S., Bank, A. J., Tschumperlin, L. K., Raij, L., Brunsvold, N., et al. (1993). Effects of cardiac transplantation on endothelium-dependent dilation of the peripheral vasculature in congestive heart failure. The American Journal of Cardiology, 71, 88–93.
120.
Patel, A. R., Kuvin, J. T., Pandian, N. G., Smith, J. J., Udelson, J. E., Mendelsohn, M. E., et al. (2001). Heart failure etiology affects peripheral vascular endothelial function after cardiac transplantation. Journal of the American College of Cardiology, 37, 195–200.
121.
Holm, T., Aukrust, P., Andreassen, A. K., Ueland, T., Brosstad, F., Frøland, S. S., et al. (2000). Peripheral endothelial dysfunction in heart transplant recipients: possible role of proinflammatory cytokines. Clinical Transplantation, 14, 218–225.
122.
McVeigh, G. E., Burns, D. E., Finkelstein, S. M., McDonald, K. M., Mock, J. E., Feske, W., et al. (1991). Reduced vascular compliance as a marker for essential hypertension. American Journal of Hypertension, 4, 245–251.
123.
Duprez, D., Jacobs, D. J., Lutsey, P., Bluemke, D., Brumback, L., Polak, J., et al. (2011). Association of small artery elasticity with incident cardiovascular disease in older adults: the multi-ethnic study of atherosclerosis. American Journal of Epidemiology, 174, 528–536.
124.
Duprez, D., Jacobs, D., Jr., Lutsey, P., Herrington, D., Prime, D., Ouyang, P., et al. (2009). Race/ethnic and sex differences in large and small artery elasticity–results of the multi-ethnic study of atherosclerosis (mesa). Ethnicity & Disease, 19, 243.
125.
Baker, J. V., Duprez, D., Rapkin, J., Hullsiek, K. H., Quick, H., Grimm, R., et al. (2009). Untreated hiv infection and large and small artery elasticity. Journal of Acquired Immune Deficiency Syndromes (1999), 52, 25.
126.
Valappil, N. I., Jacobs, D. R., Duprez, D. A., Gross, M. D., Arnett, D. K., & Glasser, S. (2008). Association between endothelial biomarkers and arterial elasticity in young adults: the cardia study. Journal of the American Society of Hypertension, 2, 70–79.
127.
Colvin-Adams, M., Harcourt, N., Sonbol, Y., Raveendran, G., Pritzker, M., & Duprez, D. (2010). Heart transplantation is associated with impaired peripheral artery function and chronic endothelial dysfunction. The Journal of Heart and Lung Transplantation, 29, S74.
128.
Hognestad, A., Endresen, K., Wergeland, R., Stokke, O., Geiran, O., Holm, T., et al. (2003). Plasma C-reactive protein as a marker of cardiac allograft vasculopathy in heart transplant recipients. Journal of the American College of Cardiology, 42, 477–482.
129.
Andreassen, A. K., Nordoy, I., Simonsen, S., Ueland, T., Muller, F., Froland, S. S., et al. (1998). Levels of circulating adhesion molecules in congestive heart failure and after heart transplantation. The American Journal of Cardiology, 81, 604–608.
130.
Lin, Y., Weisdorf, D. J., Solovey, A., & Hebbel, R. P. (2000). Origins of circulating endothelial cells and endothelial outgrowth from blood. The Journal of Clinical Investigation, 105, 71–77.
131.
Gulati, R., Jevremovic, D., Peterson, T. E., Chatterjee, S., Shah, V., Vile, R. G., et al. (2003). Diverse origin and function of cells with endothelial phenotype obtained from adult human blood. Circulation Research, 93, 1023–1025.
132.
Ziche, M., & Morbidelli, L. (2000). Nitric oxide and angiogenesis. Journal of Neuro-Oncology, 50, 139–148.
133.
Morales-Ruiz, M., Fulton, D., Sowa, G., Languino, L., Fujio, Y., Walsh, K., et al. (2000). Vascular endothelial growth factor-stimulated actin reorganization and migration of endothelial cells is regulated via the serine/threonine kinase akt. Circulation Research, 86, 892–896.
134.
Aicher, A., Heeschen, C., Mildner-Rihm, C., Urbich, C., Ihling, C., Technau-Ihling, K., et al. (2003). Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nature Medicine, 9, 1370–1376.
135.
Papapetropoulos, A., Garcia-Cardena, G., Madri, J., & Sessa, W. (1997). Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. The Journal of Clinical Investigation, 100, 3131–3139.
136.
Werner, N., Kosiol, S., Schiegl, T., Ahlers, P., Walenta, K., Link, A., et al. (2005). Circulating endothelial progenitor cells and cardiovascular outcomes. The New England Journal of Medicine, 353, 999–1007.
137.
Vasa, M., Fichtlscherer, S., Adler, K., Aicher, A., Martin, H., Zeiher, A. M., et al. (2001). Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease. Circulation, 103, 2885–2890.
138.
Hill, J., Zalos, G., Halcox, J., Schenke, W., Waclawiw, M., Quyyumi, A., et al. (2003). Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. The New England Journal of Medicine, 348, 593–600.
139.
Thomas, H., Parry, G., Dark, J., Arthur, H., & Keavney, B. (2009). Circulating endothelial progenitor cell numbers are not associated with donor organ age or allograft vasculopathy in cardiac transplant recipients. Atherosclerosis, 202, 612–616.
140.
Lou, H., Kodama, T., Wang, Y. N., Katz, N., Ramwell, P., & Foegh, M. L. (1996). l-Arginine prevents heart transplant arteriosclerosis by modulating the vascular cell proliferative response to insulin-like growth factor-i and interleukin-6. The Journal of heart and lung transplantation: the official publication of the International Society for Heart Transplantation., 15, 1248.
141.
Lim, D. S., Mooradian, S. J., Goldberg, C. S., Gomez, C., Crowley, D. C., Rocchini, A. P., et al. (2004). Effect of oral l-arginine on oxidant stress, endothelial dysfunction, and systemic arterial pressure in young cardiac transplant recipients. The American Journal of Cardiology, 94, 828–831.
142.
Rybalkin, S., Yan, C., Bornfeldt, K., & Beavo, J. (2003). Cyclic gmp phosphodiesterases and regulation of smooth muscle function. Circulation Research, 93, 280–291.
143.
Hirata, K., Adji, A., Vlachopoulos, C., & O’Rourke, M. (2005). Effect of sildenafil on cardiac performance in patients with heart failure. The American Journal of Cardiology, 96, 1436–1440.
144.
Galie, N., Ghofrani, H., Torbicki, A., Barst, R., Rubin, L., Badesch, D., et al. (2005). Sildenafil citrate therapy for pulmonary arterial hypertension. The New England Journal of Medicine, 353, 2148–2157.
145.
Halcox, J., Nour, K., Zalos, G., Mincemoyer, R., Waclawiw, M., Rivera, C., et al. (2002). The effect of sildenafil on human vascular function, platelet activation, and myocardial ischemia. Journal of the American College of Cardiology, 40, 1232–1240.
146.
Schofield, R. S., Edwards, D. G., Schuler, B. T., Estrada, J., Aranda, J. M., Pauly, D. F., et al. (2003). Vascular effects of sildenafil in hypertensive cardiac transplant recipients. American Journal of Hypertension, 16, 874–877.
147.
Yousufuddin, M., Haji, S., Starling, R. C., Tuzcu, E. M., Ratliff, N. B., Cook, D. J., et al. (2004). Cardiac angiotensin ii receptors as predictors of transplant coronary artery disease following heart transplantation. European Heart Journal, 25, 377–385.
148.
Richter, M. H. C., Ricther, H. R., Olbrich, H. G., & Mohr, F. W. (2003). Two good reasons for an angiotensin–II type 1 receptor blockade with losartan after cadiac transplantation: reduction of incidence and severity of transplant vasculopathy. Transplant International, 16, 26–32.
149.
Steinhauff, S., Pehlivanli, S., Bakovic-Alt, R., Meiser, B. M., Becker, B. F., von Scheidt, W., et al. (2004). Beneficial effects of quinaprilat on coronary vasomotor function, endothelial oxidative stress, and endothelin activation after human heart transplantation. Transplantation, 77, 1859–1865.
150.
Hamblin, M., Chang, L., Fan, Y., Zhang, J., & Chen, Y. E. (2009). Ppars and the cardiovascular system. Antioxidants & Redox Signaling, 11, 1415–1452.
151.
Babaev, V. R., Yancey, P. G., Ryzhov, S. V., Kon, V., Breyer, M. D., Magnuson, M. A., et al. (2005). Conditional knockout of macrophage pparγincreases atherosclerosis in c57bl/6 and low-density lipoprotein receptor-deficient mice. Arteriosclerosis, Thrombosis, and Vascular Biology, 25, 1647–1653.
152.
Law, R. E., Meehan, W. P., Xi, X. P., Graf, K., Wuthrich, D. A., Coats, W., et al. (1996). Troglitazone inhibits vascular smooth muscle cell growth and intimal hyperplasia. The Journal of Clinical Investigation, 98, 1897.
153.
Duan, S. Z., Ivashchenko, C. Y., Russell, M. W., Milstone, D. S., & Mortensen, R. M. (2005). Cardiomyocyte-specific knockout and agonist of peroxisome proliferator-activated receptor-γ both induce cardiac hypertrophy in mice. Circulation Research, 97, 372–379.
154.
Hetzel, J., Balletshofer, B., Rittig, K., Walcher, D., Kratzer, W., Hombach, V., et al. (2005). Rapid effects of rosiglitazone treatment on endothelial function and inflammatory biomarkers. Arteriosclerosis, Thrombosis, and Vascular Biology, 25, 1804–1809.
155.
Murakami, K., Tobe, K., Ide, T., Mochizuki, T., Ohashi, M., Akanuma, Y., et al. (1998). A novel insulin sensitizer acts as a coligand for peroxisome proliferator-activated receptor-alpha (PPAR-alpha) and PPAR-gamma: effect of PPAR-alpha activation on abnormal lipid metabolism in liver of Zucker fatty rats. Diabetes, 47, 1841–1847.
156.
Sidhu, J. S., Cowan, D., & Kaski, J. C. (2004). Effects of rosiglitazone on endothelial function in men with coronary artery disease without diabetes mellitus. The American Journal of Cardiology, 94, 151–156.
157.
Werner, C., Kamani, C. H., Gensch, C., Böhm, M., & Laufs, U. (2007). The peroxisome proliferator-activated receptor-γ agonist pioglitazone increases number and function of endothelial progenitor cells in patients with coronary artery disease and normal glucose tolerance. Diabetes, 56, 2609–2615.
158.
Dormandy, J. A., Charbonnel, B., Eckland, D. J. A., Erdmann, E., Massi-Benedetti, M., Moules, I. K., et al. (2005). Secondary prevention of macrovascular events in patients with type 2 diabetes in the proactive study (prospective pioglitazone clinical trial in macrovascular events): a randomised controlled trial. The Lancet, 366, 1279–1289.
159.
Campia, U., Matuskey, L. A., & Panza, J. A. (2006). Peroxisome proliferator-activated receptor-γ activation with pioglitazone improves endothelium-dependent dilation in nondiabetic patients with major cardiovascular risk factors. Circulation, 113, 867–875.
160.
Hamblin, M., Chang, L., Zhang, H., Yang, K., Zhang, J., & Chen, Y. E. (2011). Vascular smooth muscle cell peroxisome proliferator-activated receptor-γ mediates pioglitazone-reduced vascular lesion formation. Arteriosclerosis, Thrombosis, and Vascular Biology, 31, 352–359.
161.
Kosuge, H., Haraguchi, G., Koga, N., Maejima, Y., Suzuki, J., & Isobe, M. (2006). Pioglitazone prevents acute and chronic cardiac allograft rejection. Circulation, 113, 2613–2622.
162.
Kelishadi, S. S., Azimzadeh, A. M., Zhang, T., Stoddard, T., Welty, E., Avon, C., et al. (2010). Preemptive cd20+ b cell depletion attenuates cardiac allograft vasculopathy in cyclosporine-treated monkeys. The Journal of Clinical Investigation, 120, 1275–1284.
163.
Avery, R. K. (2003). Cardiac-allograft vasculopathy. The New England Journal of Medicine, 349, 829–830.
Metadata
Title
Endothelial Dysfunction and Cardiac Allograft Vasculopathy
Authors
Monica Colvin-Adams
Nonyelum Harcourt
Daniel Duprez
Publication date
01-04-2013
Publisher
Springer US
Published in
Journal of Cardiovascular Translational Research / Issue 2/2013
Print ISSN: 1937-5387
Electronic ISSN: 1937-5395
DOI
https://doi.org/10.1007/s12265-012-9414-3

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