De novo malignancies after organ transplantation: Focus on viral infections

Current Molecular Medicine

Volumn 13, Issue 7, 2013, Pages 1217-1227

  Piselli, P ^a   Busnach, G ^b   Fratino, L ^c   Citterio, F ^d   Ettorre, G M ^e   de Paoli, P ^c   Serraino, D ^c  

^a NATIONAL INSTITUTE FOR INFECTIOUS DISEASES L SPALLANZANI   (Italy)

^b OSPEDALE NIGUARDA CA GRANDA   (Italy)

^c CENTRO DI RIFERIMENTO ONCOLOGICO   (Italy)

^d CATHOLIC UNIVERSITY   (Italy)

^e SAN CAMILLO FORLANINI HOSPITAL   (Italy)

Author keywords

Cancer risk; Iatrogenic immunosuppression; Kaposi sarcoma; Non hodgkin lymphoma; Solid organ transplantation; Viral infection

Indexed keywords

ALPHA INTERFERON; AZATHIOPRINE; BLEOMYCIN; CALCINEURIN INHIBITOR; CYCLOPHOSPHAMIDE; CYCLOSPORIN; DACARBAZINE; DOXORUBICIN; INTERLEUKIN 6 ANTIBODY; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PREDNISONE; RITUXIMAB; STEROID; THIOPURINE METHYLTRANSFERASE; VINBLASTINE; VINCRISTINE; VIRUS DNA;

ALCOHOL ABUSE; AUTOIMMUNE DISEASE; BASAL CELL CARCINOMA; CANCER RISK; CELL CYCLE; COLON RESECTION; COLORECTAL CARCINOMA; ENTERITIS; EPSTEIN BARR VIRUS; HEMODIALYSIS; HEPATITIS C VIRUS; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN T CELL LEUKEMIA VIRUS 1; IATROGENIC DISEASE; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY CARCINOMA; KIDNEY POLYCYSTIC DISEASE; LYMPHOCYTE PROLIFERATION; MERKEL CELL TUMOR; NEOPLASM; NON MELANOMA SKIN CANCER; NONHODGKIN LYMPHOMA; ORGAN TRANSPLANTATION; OROPHARYNX TUMOR; POSTTRANSPLANT LYMPHOPROLIFERATIVE DISEASE; PRIMARY EFFUSION LYMPHOMA; PROPHYLAXIS; REVIEW; SCLEROSING CHOLANGITIS; SMOKING; SQUAMOUS CELL CARCINOMA; TUMOR VIRUS; ULCERATIVE COLITIS; VIRUS INFECTION; VIRUS LOAD; WART VIRUS;

EID: 84881339379     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/15665240113139990041     Document Type: Review

References (105)

1. Global Transplant data: Graphics and tables. Organ Donation and Tranplantation Activities. Available at: http://www.transplant-observatory.org [accessed Jan 24, 2012].
2. Shapiro R. End-stage renal disease in 2010: Innovative approaches to improve outcomes in transplantation. Nat Rev Nephrol 2011; 7: 68-70.
3. Merion RM. Current status and future of liver transplantation. Semin Liver Dis 2010; 30: 411-421.
4. Vajdic CM, McDonald SP, McCredie MR, et al. Cancer incidence before and after kidney transplantation. JAMA 2006; 296: 2823-2831.
5. Engels EA, Pfeiffer RM, Fraumeni JF, Jr, et al. Spectrum of cancer risk among US solid organ transplant recipients. JAMA 2011; 306: 1891-1901.
6. Doll R, Kinlen L. Immunosurveillance and cancer: epidemiological evidence. Br Med J 1970; 4: 420-2.
7. Penn I, Hammond W, Brettschneider L, Starzl TE. Malignant lymphomas in transplantation patients. Transplant Proc 1969; 1: 106-112.
8. Starzl TE, Penn I, Halgrimson CG. Immunosuppression and malignant neoplasms. N Engl J Med 1970; 283: 934.
9. Clemmesen J. Kaposi sarcoma in homosexual men: Is it a new disease? Lancet 1982; 2: 51-2.
10. Ziegler JL, Beckstead JA, Volberding PA, et al. Non-Hodgkin's lymphoma in 90 homosexual men. Relation to generalized lymphadenopathy and the acquired immunodeficiency syndrome. N Engl J Med 1984; 311: 565-570.
11. Dal Maso L, Serraino D, Franceschi S. Epidemiology of AIDS-related tumours in developed and developing countries. Eur J Cancer 2001; 37: 1188-1201.
12. Serraino D, Piselli P, Busnach G, et al. Risk of cancer following immunosuppression in organ transplant recipients and in HIV-positive individuals in southern Europe. Eur J Cancer 2007; 43: 2117-2123.
13. Grulich AE, van Leeuwen MT, Falster MO, Vajdic CM. Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet 2007; 370: 59-67.
14. Buell JF, Gross TG, Woodle ES. Malignancy after transplantation. Transplantation 2005; 80: S254-S264.
15. Vallejo GH, Romero CJ, de Vicente JC. Incidence and risk factors for cancer after liver transplantation. Crit Rev Oncol Hematol 2005; 56: 87-99.
16. Crespo-Leiro MG, Alonso-Pulpon L, Vazquez de Prada JA, et al. Malignancy after heart transplantation: incidence, prognosis and risk factors. Am J Transplant 2008; 8: 1031-9.
17. Piselli P, Serraino D, Segoloni G, et al. Risk of de novo cancers after transplantation: Results from a cohort of 7217 kidney transplant recipients, Italy 1997-2009. Eur J Cancer 2012 Oct 10. pii: S0959-8049(12)00727-7. doi: 10.1016/j.ejca.2012.09.013. [Epub ahead of print].
18. Miao Y, Everly JJ, Gross TG, et al. De novo cancers arising in organ transplant recipients are associated with adverse outcomes compared with the general population. Transplantation 2009; 87: 1347-1359.
19. de Martel C, Ferlay J, Franceschi S, et al. Gobal burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol 2012; 13: 607-615.
20. International Agency for Research on Cancer (IARC). Epstein-Barr virus and Kaposi's sarcoma herpesvirus/human herpesvirus 8. IARC Monogr Eval Carcinog Risks Hum. 1997; pp. 375-494.
21. Schulz TF. Cancer and viral infections in immunocompromised individuals. Int J Cancer 2009; 125: 1755-1763.
22. Biggar RJ, Henle W, Fleisher G, Bocker J, Lennette ET, Henle G. Primary Epstein-Barr virus infections in African infants. I. Decline of maternal antibodies and time of infection. Int J Cancer 1978; 22: 239-243.
23. Wensing B, Farrell PJ. Regulation of cell growth and death by Epstein-Barr virus. Microbes Infect 2000; 2: 77-84.
24. Snow AL, Martinez OM. Epstein-Barr virus: evasive maneuvers in the development of PTLD. Am J Transplant 2007; 7: 271-277.
25. Opelz G, Daniel V, Naujokat C, Dohler B. Epidemiology of pretransplant EBV and CMV serostatus in relation to posttransplant non-Hodgkin lymphoma. Transplantation 2009; 88: 962-967.
26. Dukers NH, Rezza G. Human herpesvirus 8 epidemiology: what we do and do not know. AIDS 2003; 17: 1717-1730.
27. Hoshida Y, Li T, Dong Z, et al. Lymphoproliferative disorders in renal transplant patients in Japan. Int J Cancer 2001; 91: 869-875.
28. Bouvard V, Baan R, Straif K, et al. A review of human carcinogens-Part B: biological agents. Lancet Oncol 2009; 10: 321-322.
29. Collett D, Mumford L, Banner NR, et al. Comparison of the Incidence of Malignancy in Recipients of Different Types of Organ: A UK Registry Audit. Am J Transplant 2010; 10: 1889-1896.
30. Villeneuve PJ, Schaubel DE, Fenton SS, et al. Cancer incidence among Canadian kidney transplant recipients. Am J Transplant 2007; 7: 941-948.
31. Rama I, Grinyo JM. Malignancy after renal transplantation: the role of immunosuppression. Nat Rev Nephrol 2010; 6: 511-519.
32. Ramsay HM, Fryer AA, Hawley CM, Smith AG, Harden PN. Non-melanoma skin cancer risk in the Queensland renal transplant population. Br J Dermatol 2002; 147: 950-956.
33. Webb MC, Compton F, Andrews PA, Koffman CG. Skin tumours posttransplantation: a retrospective analysis of 28 years experience at a single centre. Transplant Proc 1997; 29: 828-830.
34. Adami J, Gabel H, Lindelof B, et al. Cancer risk following organ transplantation: a nationwide cohort study in Sweden. Br J Cancer 2003; 89: 1221-1227.
35. Lindelof B, Sigurgeirsson B, Gabel H, Stern RS. Incidence of skin cancer in 5356 patients following organ transplantation. Br J Dermatol 2000; 143: 513-519.
36. Euvrard S, Kanitakis J, Claudy A. Skin cancers after organ transplantation. N Engl J Med 2003; 348: 1681-1691.
37. McGregor JM, Berkhout RJ, Rozycka M, et al. P53 mutations implicate sunlight in post-transplant skin cancer irrespective of human papillomavirus status. Oncogene 1997; 15: 1737-1740.
38. Rubel JR, Milford EL, Abdi R. Cutaneous neoplasms in renal transplant recipients. Eur J Dermatol 2002; 12: 532-535.
39. Geissler EK, Schlitt HJ. The relation between immunosuppressive agents and malignancy. Current Opinion in Organ Transplantation 2004; 9: 394-399.
40. Jensen P, Hansen S, Moller B, et al. Skin cancer in kidney and heart transplant recipients and different long-term immunosuppressive therapy regimens. J Am Acad Dermatol 1999; 40: 177-186.
41. Perrett CM, Walker SL, O'Donovan P, et al. Azathioprine treatment photosensitizes human skin to ultraviolet A radiation. Br J Dermatol 2008; 159: 198-204.
42. Guba M, von BP, Steinbauer M, et al. Rapamycin inhibits primary and metastatic tumor growth by antiangiogenesis: involvement of vascular endothelial growth factor. Nat Med 2002; 8: 128-135.
43. Morath C, Arns W, Schwenger V, et al. Sirolimus in renal transplantation. Nephrol Dial Transplant 2007; 22 Suppl 8: viii61-viii65.
44. Monaco AP. The role of mTOR inhibitors in the management of posttransplant malignancy. Transplantation 2009; 87: 157-163.
45. Geissler EK, Schlitt HJ. Transplantation: can sirolimus prevent skin cancer in transplant recipients? Nat Rev Nephrol 2010; 6: 639-641.
46. Harwood CA, Surentheran T, McGregor JM, et al. Human papillomavirus infection and non-melanoma skin cancer in immunosuppressed and immunocompetent individuals. J Med Virol 2000; 61: 289-297.
47. Zwald FO, Brown M. Skin cancer in solid organ transplant recipients: advances in therapy and management: part I. Epidemiology of skin cancer in solid organ transplant recipients. J Am Acad Dermatol 2011; 65: 253-261.
48. Feng H, Shuda M, Chang Y, Moore PS. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 2008; 319: 1096-1100.
49. Shuda M, Feng H, Kwun HJ, et al. T antigen mutations are a human tumor-specific signature for Merkel cell polyomavirus. Proc Natl Acad Sci USA 2008; 105: 16272-16372.
50. Opelz G, Dohler B. Lymphomas after solid organ transplantation: a collaborative transplant study report. Am J Transplant 2004; 4: 222-230.
51. Harris HL, Swerdlow SH, Frizzera G, Knowles DM. Post-trasplant lymphoproliferative disorders. In: Jaffe ES, Harris NL, Stein H, Vardiman JW, editors. WHO classification of tumours: pathology and genetrics of tumours of haematopoietic tissues. Lyon: IARC Press 2001; pp. 264-269.
52. Jagadeesh D, Woda BA, Draper J, Evens AM. Post transplant lymphoproliferative disorders: risk, classification, and therapeutic recommendations. Curr Treat Options Oncol 2012; 13: 122-136.
53. Swerdlow SH, Campo E, Harris NL, et al. Post-trasplant lymphoproliferative disorders. WHO classification of tumours of Haematopoietic and Lymphoid Tissues. Lyon: IARC Press 2008; pp. 343-350.
54. Hartmann C, Schuchmann M, Zimmermann T. Posttransplant lymphoproliferative disease in liver transplant patients. Curr Infect Dis Rep 2011; 13: 53-59.
55. Dror Y, Greenberg M, Taylor G, et al. Lymphoproliferative disorders after organ transplantation in children. Transplantation 1999; 67: 990-998.
56. Gulley ML, Tang W. Using Epstein-Barr viral load assays to diagnose, monitor, and prevent posttransplant lymphoproliferative disorder. Clin Microbiol Rev 2010; 23: 350-366.
57. Martinez OM, de Gruijl FR. Molecular and immunologic mechanisms of cancer pathogenesis in solid organ transplant recipients. Am J Transplant 2008; 8: 2205-2211.
58. Vakiani E, Basso K, Klein U, et al. Genetic and phenotypic analysis of B-cell post-transplant lymphoproliferative disorders provides insights into disease biology. Hematol Oncol 2008; 26: 199-211.
59. Capello D, Rossi D, Gaidano G. Post-transplant lymphoproliferative disorders: molecular basis of disease histogenesis and pathogenesis. Hematol Oncol 2005; 23: 61-67.
60. Nelson BP, Nalesnik MA, Bahler DW, Locker J, Fung JJ, Swerdlow SH. Epstein-Barr virus-negative post-transplant lymphoproliferative disorders: a distinct entity? Am J Surg Pathol 2000; 24: 375-385.
61. Burra P, Buda A, Livi U, et al. Occurrence of post-transplant lymphoproliferative disorders among over thousand adult recipients: any role for hepatitis C infection? Eur J Gastroenterol Hepatol 2006; 18: 1065-1070.
62. Cesarman E, Chang Y, Moore PS, Said JW, Knowles DM. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med 1995; 332: 1186-1191.
63. Caillard S, Agodoa LY, Bohen EM, Abbott KC. Myeloma, Hodgkin disease, and lymphoid leukemia after renal transplantation: characteristics, risk factors and prognosis. Transplantation 2006; 81: 888-895.
64. Jacobson CA, LaCasce AS. Lymphoma: risk and response after solid organ transplant. Oncology (Williston Park) 2010; 24: 936-944.
65. Gao SZ, Chaparro SV, Perlroth M, et al. Post-transplantation lymphoproliferative disease in heart and heart-lung transplant recipients: 30-year experience at Stanford University. J Heart Lung Transplant 2003; 22: 505-514.
66. Bustami RT, Ojo AO, Wolfe RA, et al. Immunosuppression and the risk of post-transplant malignancy among cadaveric first kidney transplant recipients. Am J Transplant 2004; 4: 87-93.
67. Zimmermann T, Hoppe-Lotichius M, Tripkovic V, et al. Liver transplanted patients with preoperative autoimmune hepatitis and immunological disorders are at increased risk for Post Transplant Lymphoproliferative Disease (PTLD). Eur J Intern Med 2010; 21: 208-215.
68. Parker A, Bowles K, Bradley JA, et al. Management of post-transplant lymphoproliferative disorder in adult solid organ transplant recipients - BCSH and BTS Guidelines. Br J Haematol 2010; 149: 693-705.
69. Donckier V, Sanchez-Fueyo A, Craciun L, et al. Induction of tolerance in solid organ transplantation: the rationale to develop clinical protocols in liver transplantation. Transplant Proc 2009; 41: 603-606.
70. Trappe RU, Choquet S, Reinke P, et al. Salvage therapy for relapsed posttransplant lymphoproliferative disorders (PTLD) with a second progression of PTLD after Upfront chemotherapy: the role of single-agent rituximab. Transplantation 2007; 84: 1708-1712.
71. Coiffier B. Treatment of post-transplant lymphomas. Oncology (Williston Park) 2010; 24: 950-951.
72. Pascual J. Post-transplant lymphoproliferative disorder-the potential of proliferation signal inhibitors. Nephrol Dial Transplant 2007; 22 Suppl 1: i27-i35.
73. Antman K, Chang Y. Kaposi's sarcoma. N Engl J Med 2000; 342: 1027-1038.
74. Lebbe C, Legendre C, Frances C. Kaposi sarcoma in transplantation. Transplant Rev (Orlando) 2008; 22: 252-261.
75. Chang Y, Cesarman E, Pessin MS, et al. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 1994; 266: 1865-1869.
76. Taylor GS, Blackbourn DJ. Infectious agents in human cancers: lessons in immunity and immunomodulation from gammaherpesviruses EBV and KSHV. Cancer Lett 2011; 305: 263-278.
77. Piselli P, Busnach G, Citterio F, et al. Risk of Kaposi sarcoma after solid-organ transplantation: multicenter study in 4,767 recipients in Italy, 1970-2006. Transplant Proc 2009; 41: 1227-1230.
78. Serraino D, Piselli P, Scuderi M, et al. Screening for human herpesvirus 8 antibodies in Italian organ transplantation centers. Clin Infect Dis 2005; 40: 203-205.
79. Zavos G, Bokos J, Papaconstantinou I, et al. Clinicopathological aspects of 18 Kaposi's sarcoma among 1055 Greek renal transplant recipients. Artif Organs 2004; 28: 595-599.
80. Garcia-Astudillo LA, Leyva-Cobian F. Human herpesvirus-8 infection and Kaposi's sarcoma after liver and kidney transplantation in different geographical areas of Spain. Transpl Immunol 2006; 17: 65-69.
81. Qunibi WY, Barri Y, Alfurayh O, et al. Kaposi's sarcoma in renal transplant recipients: a report on 26 cases from a single institution. Transplant Proc 1993; 25: 1402-1405.
82. El-Agroudy AE, El-Baz MA, Ismail AM, Ali-El-Dein B, El-Dein AB, Ghoneim MA. Clinical features and course of Kaposi's sarcoma in Egyptian kidney transplant recipients. Am J Transplant 2003; 3: 1595-1599.
83. Haberal AN, Suren D, Demirhan B, Bilezikci B, Celasun B, Haberal M. Evaluation of posttransplantation malignancies compared with de novo tumors. Transplant Proc 2007; 39: 1057-1062.
84. Shepherd FA, Maher E, Cardella C, et al. Treatment of Kaposi's sarcoma after solid organ transplantation. J Clin Oncol 1997; 15: 2371-2377.
85. Mbulaiteye SM, Engels EA. Kaposi's sarcoma risk among transplant recipients in the United States (1993-2003). Int J Cancer 2006; 119: 2685-2691.
86. Mendez JC, Procop GW, Espy MJ, Smith TF, McGregor CG, Paya CV. Relationship of HHV8 replication and Kaposi's sarcoma after solid organ transplantation. Transplantation 1999; 67: 1200-1201.
87. Frances C, Marcelin AG, Legendre C, et al. The impact of preexisting or acquired Kaposi sarcoma herpesvirus infection in kidney transplant recipients on morbidity and survival. Am J Transplant 2009; 9: 2580-2586.
88. Luppi M, Barozzi P, Guaraldi G, et al. Human herpesvirus 8-associated diseases in solid-organ transplantation: importance of viral transmission from the donor. Clin Infect Dis 2003; 37: 606-607.
89. Barozzi P, Luppi M, Facchetti F, et al. Post-transplant Kaposi sarcoma originates from the seeding of donor-derived progenitors. Nat Med 2003; 9: 554-561.
90. Parravicini C, Scalamogna C, Calattini S, et al. KSHV reactivation in post-transplant Kaposi sarcoma. Nat Med 2003; 9: 986.
91. Serraino D, Angeletti C, Carrieri MP, et al. Kaposi's sarcoma in transplant and HIV-infected patients: an epidemiologic study in Italy and France. Transplantation 2005; 80: 1699-1704.
92. Uldrick TS, Whitby D. Update on KSHV epidemiology, Kaposi Sarcoma pathogenesis, and treatment of Kaposi Sarcoma. Cancer Lett 2011; 305: 150-162.
93. Gutierrez-Dalmau A, Campistol JM. Immunosuppressive therapy and malignancy in organ transplant recipients: a systematic review. Drugs 2007; 67: 1167-1198.
94. Meric-Bernstam F, Gonzalez-Angulo AM. Targeting the mTOR signaling network for cancer therapy. J Clin Oncol 2009; 27: 2278-2287.
95. Stallone G, Schena A, Infante B, et al. Sirolimus for Kaposi's sarcoma in renal-transplant recipients. N Engl J Med 2005; 352: 1317-1323.
96. Boratynska M, Zmonarski SC, Klinger M. Reccurence of Kaposi's sarcoma after increased exposure to sirolimus. Int Immunopharmacol 2006; 6: 2018-2022.
97. Finkenstedt A, Graziadei IW, Oberaigner W, et al. Extensive surveillance promotes early diagnosis and improved survival of de novo malignancies in liver transplant recipients. Am J Transplant 2009; 9: 2355-2361.
98. Kliem V, Kolditz M, Behrend M, et al. Risk of renal cell carcinoma after kidney transplantation. Clin Transplant 1997; 11: 255-258.
99. Scandling JD. Acquired cystic kidney disease and renal cell cancer after transplantation: time to rethink screening? Clin J Am Soc Nephrol 2007; 2: 621-622.
100. Sint Nicolaas J, de Jonge V, Steyerberg EW, Kuipers EJ, van Leerdam ME, Veldhuyzen-van Zanten SJ. Risk of colorectal carcinoma in post-liver transplant patients: a systematic review and meta-analysis. Am J Transplant 2010; 10: 868-876.
101. Kulaylat MN, Dayton MT. Ulcerative colitis and cancer. J Surg Oncol 2010; 101: 706-712.
102. Oo YH, Gunson BK, Lancashire RJ, Cheng KK, Neuberger JM. Incidence of cancers following orthotopic liver transplantation in a single center: comparison with national cancer incidence rates for England and Wales. Transplantation 2005; 80: 759-764.
103. Talamini R, La VC, Levi F, Conti E, Favero A, Franceschi S. Cancer of the oral cavity and pharynx in nonsmokers who drink alcohol and in nondrinkers who smoke tobacco. J Natl Cancer Inst 1998; 90: 1901-1903.
104. Fung JJ, Jain A, Kwak EJ, Kusne S, Dvorchik I, Eghtesad B. De novo malignancies after liver transplantation: a major cause of late death. Liver Transpl 2001; 7: S109-S118.
105. Jimenez C, Manrique A, Marques E, et al. Incidence and risk factors for the development of lung tumors after liver transplantation. Transpl Int 2007; 20: 57-63.