Immune-based monitoring for cytomegalovirus infection in solid organ transplantation: is it ready for clinical primetime?

References

• Reddehase MJ. Antigens and immunoevasins: opponents in cytomegalovirus immune surveillance. Nat Rev Immunol 2002;2(11):831-44
   PubMed Web of Science ®Google Scholar
• Beam E, Razonable RR. Cytomegalovirus in solid organ transplantation: epidemiology, prevention, and treatment. Curr Infect Dis Rep 2012;14(6):633-41
   PubMed Web of Science ®Google Scholar
• Bate SL, Dollard SC, Cannon MJ. Cytomegalovirus seroprevalence in the United States: the national health and nutrition examination surveys, 1988-2004. Clin Infect Dis 2010;50(11):1439-47
   PubMed Web of Science ®Google Scholar
• Greenberg PD, Riddell SR. Deficient cellular immunity--finding and fixing the defects. Science 1999;285(5427):546-51
   Google Scholar
• Torre-Cisneros J. Toward the individualization of cytomegalovirus control after solid-organ transplantation: the importance of the "individual pathogenic balance". Clin Infect Dis 2009;49(8):1167-8
   Google Scholar
• Humar A, Lebranchu Y, Vincenti F, et al. The efficacy and safety of 200 days valganciclovir cytomegalovirus prophylaxis in high-risk kidney transplant recipients. Am J Transplant 2010;10(5):1228-37
   PubMed Web of Science ®Google Scholar
• Paya C, Humar A, Dominguez E, et al. Efficacy and safety of valganciclovir vs. oral ganciclovir for prevention of cytomegalovirus disease in solid organ transplant recipients. Am J Transplant 2004;4(4):611-20
   PubMed Web of Science ®Google Scholar
• Einsele H, Hebart H, Kauffmann-Schneider C, et al. Risk factors for treatment failures in patients receiving PCR-based preemptive therapy for CMV infection. Bone Marrow Transplant 2000;25(7):757-63
   PubMed Web of Science ®Google Scholar
• Li CR, Greenberg PD, Gilbert MJ, et al. Recovery of HLA-restricted cytomegalovirus (CMV)-specific T-cell responses after allogeneic bone marrow transplant: correlation with CMV disease and effect of ganciclovir prophylaxis. Blood 1994;83(7):1971-9
   PubMed Web of Science ®Google Scholar
• Krause H, Hebart H, Jahn G, et al. Screening for CMV-specific T cell proliferation to identify patients at risk of developing late onset CMV disease. Bone Marrow Transplant 1997;19(11):1111-16
   PubMed Web of Science ®Google Scholar
• Manuel O, Pang XL, Humar A, et al. An assessment of donor-to-recipient transmission patterns of human cytomegalovirus by analysis of viral genomic variants. J Infect Dis 2009;199(11):1621-8
   PubMed Web of Science ®Google Scholar
• Razonable RR. Epidemiology of cytomegalovirus disease in solid organ and hematopoietic stem cell transplant recipients. Am J Health Syst Pharm 2005;62(8 Suppl 1):S7-13
   Google Scholar
• Goodrich JM, Bowden RA, Fisher L, et al. Ganciclovir prophylaxis to prevent cytomegalovirus disease after allogeneic marrow transplant. Ann Intern Med 1993;118(3):173-8
   PubMed Web of Science ®Google Scholar
• Humar A, Mazzulli T, Moussa G, et al. Clinical utility of cytomegalovirus (CMV) serology testing in high-risk CMV D+/R- transplant recipients. Am J Transplant 2005;5(5):1065-70
   PubMed Web of Science ®Google Scholar
• Cooper MA, Fehniger TA, Turner SC, et al. Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood 2001;97(10):3146-51
   PubMed Web of Science ®Google Scholar
• Caligiuri MA. Human natural killer cells. Blood 2008;112(3):461-9
   PubMed Web of Science ®Google Scholar
• Walzer T, Jaeger S, Chaix J, Vivier E. Natural killer cells: from CD3(-)NKp46(+) to post-genomics meta-analyses. Curr Opin Immunol 2007;19(3):365-72
   PubMed Web of Science ®Google Scholar
• Kuijpers TW, Baars PA, Dantin C, et al. Human NK cells can control CMV infection in the absence of T cells. Blood 2008;112(3):914-15
   PubMed Web of Science ®Google Scholar
• Munoz-Cobo B, Solano C, Benet I, et al. Functional profile of cytomegalovirus (CMV)-specific CD8+ T cells and kinetics of NKG2C+ NK cells associated with the resolution of CMV DNAemia in allogeneic stem cell transplant recipients. J Med Virol 2012;84(2):259-67
   PubMed Web of Science ®Google Scholar
• Jonjic S, Pavic I, Polic B, et al. Antibodies are not essential for the resolution of primary cytomegalovirus infection but limit dissemination of recurrent virus. J Exp Med 1994;179(5):1713-17
   Web of Science ®Google Scholar
• van Lier RA, ten Berge IJ, Gamadia LE. Human CD8(+) T-cell differentiation in response to viruses. Nat Rev Immunol 2003;3(12):931-9
   PubMed Web of Science ®Google Scholar
• Rowshani AT, Bemelman FJ, van Leeuwen EM, et al. Clinical and immunologic aspects of cytomegalovirus infection in solid organ transplant recipients. Transplantation 2005;79(4):381-6
   Web of Science ®Google Scholar
• Reddehase MJ, Weiland F, Munch K, et al. Interstitial murine cytomegalovirus pneumonia after irradiation: characterization of cells that limit viral replication during established infection of the lungs. J Virol 1985;55(2):264-73
   PubMed Web of Science ®Google Scholar
• Gandhi MK, Khanna R. Human cytomegalovirus: clinical aspects, immune regulation, and emerging treatments. Lancet Infect Dis 2004;4(12):725-38
   PubMed Web of Science ®Google Scholar
• Kalams SA, Walker BD. The critical need for CD4 help in maintaining effective cytotoxic T lymphocyte responses. J Exp Med 1998;188(12):2199-204
   PubMed Web of Science ®Google Scholar
• Rentenaar RJ, Gamadia LE, van DerHoek N, et al. Development of virus-specific CD4(+) T cells during primary cytomegalovirus infection. J Clin Invest 2000;105(4):541-8
   Google Scholar
• Zajac AJ, Blattman JN, Murali-Krishna K, et al. Viral immune evasion due to persistence of activated T cells without effector function. J Exp Med 1998;188(12):2205-13
   PubMed Web of Science ®Google Scholar
• Gamadia LE, Remmerswaal EB, Weel JF, et al. Primary immune responses to human CMV: a critical role for IFN-gamma-producing CD4+ T cells in protection against CMV disease. Blood 2003;101(7):2686-92
   PubMed Web of Science ®Google Scholar
• Egli A, Humar A, Kumar D. State-of-the-art monitoring of cytomegalovirus-specific cell-mediated immunity after organ transplant: a primer for the clinician. Clin Infect Dis 2012;55(12):1678-89
   PubMed Web of Science ®Google Scholar
• Egli A, Binet I, Binggeli S, et al. Cytomegalovirus-specific T-cell responses and viral replication in kidney transplant recipients. J Transl Med 2008;6:29
   PubMedGoogle Scholar
• Radha R, Jordan S, Puliyanda D, et al. Cellular immune responses to cytomegalovirus in renal transplant recipients. Am J Transplant 2005;5(1):110-17
   Google Scholar
• Shlobin OA, West EE, Lechtzin N, et al. Persistent cytomegalovirus-specific memory responses in the lung allograft and blood following primary infection in lung transplant recipients. J Immunol 2006;176(4):2625-34
   Google Scholar
• Lozza L, Lilleri D, Percivalle E, et al. Simultaneous quantification of human cytomegalovirus (HCMV)-specific CD4+ and CD8+ T cells by a novel method using monocyte-derived HCMV-infected immature dendritic cells. Eur J Immunol 2005;35(6):1795-804
   PubMed Web of Science ®Google Scholar
• Gerna G, Lilleri D, Fornara C, et al. Monitoring of human cytomegalovirus-specific CD4 and CD8 T-cell immunity in patients receiving solid organ transplantation. Am J Transplant 2006;6(10):2356-64
   Web of Science ®Google Scholar
• Maecker HT. Cytokine flow cytometry. Methods Mol Biol 2004;263:95-108
   Google Scholar
• Elkington R, Walker S, Crough T, et al. Ex vivo profiling of CD8+-T-cell responses to human cytomegalovirus reveals broad and multispecific reactivities in healthy virus carriers. J Virol 2003;77(9):5226-40
   Google Scholar
• Abate D, Saldan A, Forner G, et al. Optimization of interferon gamma ELISPOT assay to detect human cytomegalovirus specific T-cell responses in solid organ transplants. J Virol Methods 2014;196:157-62
   Google Scholar
• Giulieri S, Manuel O. QuantiFERON(R)-CMV assay for the assessment of cytomegalovirus cell-mediated immunity. Expert Rev Mol Diagn 2011;11(1):17-25
   PubMed Web of Science ®Google Scholar
• Lopez-Oliva MO, Martinez V, Buitrago A, et al. Pretransplant CD8 T-Cell response to IE-1 discriminates seropositive kidney recipients at risk of developing CMV infection posttransplant. Transplantation 2014;97(8)):839-45
   Google Scholar
• Bunde T, Kirchner A, Hoffmeister B, et al. Protection from cytomegalovirus after transplantation is correlated with immediate early 1-specific CD8 T cells. J Exp Med 2005;201(7):1031-6
   PubMed Web of Science ®Google Scholar
• Eid AJ, Brown RA, Arthurs SK, et al. A prospective longitudinal analysis of cytomegalovirus (CMV)-specific CD4+ and CD8+ T cells in kidney allograft recipients at risk of CMV infection. Transpl Int 2010;23(5):506-13
   Google Scholar
• Bestard O, Lucia M, Crespo E, et al. Pretransplant immediately early-1-specific T cell responses provide protection for CMV infection after kidney transplantation. Am J Transplant 2013;13(7):1793-805
   PubMed Web of Science ®Google Scholar
• Cantisan S, Lara R, Montejo M, et al. Pretransplant interferon-gamma secretion by CMV-specific CD8+ T cells informs the risk of CMV replication after transplantation. Am J Transplant 2013;13(3):738-45
   Google Scholar
• Sester M, Sester U, Gartner B, et al. Levels of virus-specific CD4 T cells correlate with cytomegalovirus control and predict virus-induced disease after renal transplantation. Transplantation 2001;71(9):1287-94
   Google Scholar
• Sester U, Gartner BC, Wilkens H, et al. Differences in CMV-specific T-cell levels and long-term susceptibility to CMV infection after kidney, heart and lung transplantation. Am J Transplant 2005;5(6):1483-9
   PubMed Web of Science ®Google Scholar
• Reusser P, Cathomas G, Attenhofer R, et al. Cytomegalovirus (CMV)-specific T cell immunity after renal transplantation mediates protection from CMV disease by limiting the systemic virus load. J Infect Dis 1999;180(2):247-53
   Google Scholar
• La Rosa C, Limaye AP, Krishnan A, et al. Longitudinal assessment of cytomegalovirus (CMV)-specific immune responses in liver transplant recipients at high risk for late CMV disease. J Infect Dis 2007;195(5):633-44
   PubMed Web of Science ®Google Scholar
• Pipeling MR, John ER, Orens JB, et al. Primary cytomegalovirus phosphoprotein 65-specific CD8+ T-cell responses and T-bet levels predict immune control during early chronic infection in lung transplant recipients. J Infect Dis 2011;204(11):1663-71
   Google Scholar
• Pipeling MR, West EE, Osborne CM, et al. Differential CMV-specific CD8+ effector T cell responses in the lung allograft predominate over the blood during human primary infection. J Immunol 2008;181(1):546-56
   Google Scholar
• Abate D, Saldan A, Fiscon M, et al. Evaluation of cytomegalovirus (CMV)-specific T cell immune reconstitution revealed that baseline antiviral immunity, prophylaxis, or preemptive therapy but not antithymocyte globulin treatment contribute to CMV-specific T cell reconstitution in kidney transplant recipients. J Infect Dis 2010;202(4)):585-94
   Google Scholar
• Chiereghin A, Gabrielli L, Zanfi C, et al. Monitoring cytomegalovirus T-cell immunity in small bowel/multivisceral transplant recipients. Transplant Proc 2010;42(1):69-73
   Google Scholar
• Costa C, Astegiano S, Terlizzi ME, et al. Evaluation and significance of cytomegalovirus-specific cellular immune response in lung transplant recipients. Transplant Proc 2011;43(4):1159-61
   Google Scholar
• Abate D, Fiscon M, Saldan A, et al. Human cytomegalovirus-specific T-cell immune reconstitution in preemptively treated heart transplant recipients identifies subjects at critical risk for infection. J Clin Microbiol 2012;50(6):1974-80
   Google Scholar
• Abate D, Saldan A, Mengoli C, et al. Comparison of cytomegalovirus (CMV) enzyme-linked immunosorbent spot and CMV quantiferon gamma interferon-releasing assays in assessing risk of CMV infection in kidney transplant recipients. J Clin Microbiol 2013;51(8):2501-7
   PubMed Web of Science ®Google Scholar
• Westall GP, Mifsud NA, Kotsimbos T. Linking CMV serostatus to episodes of CMV reactivation following lung transplantation by measuring CMV-specific CD8+ T-cell immunity. Am J Transplant 2008;8(8):1749-54
   PubMed Web of Science ®Google Scholar
• Lochmanova A, Lochman I, Tomaskova H, et al. Quantiferon-CMV test in prediction of cytomegalovirus infection after kidney transplantation. Transplant Proc 2010;42(9):3574-7
   Google Scholar
• Weseslindtner L, Kerschner H, Steinacher D, et al. Prospective analysis of human cytomegalovirus DNAemia and specific CD8+ T cell responses in lung transplant recipients. Am J Transplant 2012;12(8):2172-80
   Google Scholar
• Kumar D, Chernenko S, Moussa G, et al. Cell-mediated immunity to predict cytomegalovirus disease in high-risk solid organ transplant recipients. Am J Transplant 2009;9(5):1214-22
   PubMed Web of Science ®Google Scholar
• Manuel O, Husain S, Kumar D, et al. Assessment of cytomegalovirus-specific cell-mediated immunity for the prediction of cytomegalovirus disease in high-risk solid-organ transplant recipients: a multicenter cohort study. Clin Infect Dis 2013;56(6):817-24
   PubMed Web of Science ®Google Scholar
• Lisboa LF, Kumar D, Wilson LE, Humar A. Clinical utility of cytomegalovirus cell-mediated immunity in transplant recipients with cytomegalovirus viremia. Transplantation 2012;93(2):195-200
   PubMed Web of Science ®Google Scholar
• Weseslindtner L, Kerschner H, Steinacher D, et al. Association of human cytomegalovirus DNAaemia and specific granzyme B responses in lung transplant recipients. Clin Exp Immunol 2013;173(3):438-43
   Google Scholar
• Walker S, Fazou C, Crough T, et al. Ex vivo monitoring of human cytomegalovirus-specific CD8+ T-cell responses using QuantiFERON-CMV. Transpl Infect Dis 2007;9(2):165-70
   PubMed Web of Science ®Google Scholar
• Benmarzouk-Hidalgo OJ, Cisneros JM, Cordero E, et al. Therapeutic effect of the acquisition of cytomegalovirus-specific immune response during preemptive treatment. Transplantation 2011;91(8):927-33
   Google Scholar