Skin cancer in organ transplant recipients: More than the immune system

Journal of the American Academy of Dermatology

Volumn 71, Issue 2, 2014, Pages 359-365

  Wheless, Lee ^a   Jacks, Sarah ^a   Mooneyham Potter, Kathryn Anne ^a   Leach, Brian C ^a   Cook, Joel ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

calcineurin inhibitors; immunosuppression; mammalian target of rapamycin inhibitors; oncogenic viruses; organ transplant recipients; skin cancer

Indexed keywords

AZATHIOPRINE; CYCLOSPORIN; EVEROLIMUS; PREDNISONE; RAPAMYCIN; TACROLIMUS;

CANCER INCIDENCE; EXCISION REPAIR; GENE MUTATION; GRAFT RECIPIENT; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE SYSTEM; IMMUNOSUPPRESSIVE TREATMENT; KAPOSI SARCOMA; MERKEL CELL TUMOR; POLYOMA VIRUS; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SKIN CANCER; SKIN PIGMENTATION; SUN EXPOSURE; WART VIRUS;

CALCINEURIN INHIBITORS; IMMUNOSUPPRESSION; MAMMALIAN TARGET OF RAPAMYCIN INHIBITORS; ONCOGENIC VIRUSES; ORGAN TRANSPLANT RECIPIENTS; SKIN CANCER;

CALCINEURIN; CARCINOMA, BASAL CELL; CARCINOMA, SQUAMOUS CELL; DNA REPAIR; HUMANS; IMMUNOSUPPRESSIVE AGENTS; ORGAN TRANSPLANTATION; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; TOR SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84904743986     PISSN: 01909622     EISSN: 10976787     Source Type: Journal    
DOI: 10.1016/j.jaad.2014.02.039     Document Type: Review

References (67)

1. D. Berg, and C.C. Otley Skin cancer in organ transplant recipients: epidemiology, pathogenesis, and management J Am Acad Dermatol 47 2002 1 17
2. S. Euvrard, J. Kanitakis, and A. Claudy Skin cancers after organ transplantation N Engl J Med 348 2003 1681 1691
3. G. Tessari, and G. Girolomoni Nonmelanoma skin cancer in solid organ transplant recipients: update on epidemiology, risk factors, and management Dermatol Surg 38 2012 1622 1630
4. J. de Fijter Use of proliferation signal inhibitors in non-melanoma skin cancer following renal transplantation Nephrol Dial Transplant 22 Suppl 2007 i23 i26
5. F. Zwald, and M. Brown 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 65 2011 253 261
6. F. Zwald, and M. Brown Skin cancer in solid organ transplant recipients, advances in therapy and management, part II: management of skin cancer in solid organ transplant recipients J Am Acad Dermatol 65 2011 263 279
7. B. Muehleisen, S.B. Jiang, J.A. Gladsjo, M. Gerber, T. Hata, and R.L. Gallo Distinct innate immune gene expression profiles in non-melanoma skin cancer of immunocompetent and immunosuppressed patients PLoS One 7 2012 e40754
8. T. Hampton Skin cancer's ranks rise: immunosuppression to blame JAMA 294 2005 1476 1480
9. T. Mudigonda, M.M. Levender, J.L. O'Neill, C.E. West, D.J. Pearce, and S.R. Feldman Incidence, risk factors, and preventative management of skin cancers in organ transplant recipients: a review of single- and multicenter retrospective studies from 2006 to 2010 Dermatol Surg 39 2013 345 364
10. C. Kuschal, K.M. Thoms, S. Schubert, A. Schäfer, L. Boeckmann, and M.P. Schön et al. Skin cancer in organ transplant recipients: effects of immunosuppressive medications on DNA repair Exp Dermatol 21 2012 2 6
11. B. Aldabagh, J.G. Angeles, A.R. Cardones, and S.T. Arron Cutaneous squamous cell carcinoma and human papillomavirus: is there an association? Dermatol Surg 39 2013 1 23
12. A. Grulich, M.T. van Leeuwen, M.O. Falster, and C.M. Vajdic Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis Lancet 370 2007 59 67
13. S. Arron, L. Jennings, I. Nindl, F. Rosl, J.N. Bouwes Bavinck, and D. Seçkin et al. Viral oncogenesis and its role in nonmelanoma skin cancer Br J Dermatol 164 2011 1201 1213
14. G. Moulis, A. Sommet, J. Béné, F. Montastruc, L. Sailler, and J.L. Montastruc et al. Cancer risk of anti-TNF-α at recommended doses in adult rheumatoid arthritis: a meta-analysis with intention to treat and per protocol analyses PLoS One 7 2012 e48991
15. B. Krynitz, G. Edgren, B. Lindelöf, E. Baecklund, C. Brattström, and H. Wilczek et al. Risk of skin cancer and other malignancies in kidney, liver, heart and lung transplant recipients 1970 to 2008-a Swedish population-based study Int J Cancer 132 2013 1429 1438
16. C. Harwood, D. Mesher, J.M. McGregor, L. Mitchell, M. Leedham-Green, and M. Raftery et al. A surveillance model for skin cancer in organ transplant recipients: a 22-year prospective study in an ethnically diverse population Am J Transplant 13 2013 119 129
17. R. Gogia, M. Binstock, R. Hirose, W.J. Boscardin, M.M. Chren, and S.T. Arron Fitzpatrick skin phototype is an independent predictor of squamous cell carcinoma risk after solid organ transplantation J Am Acad Dermatol 68 2013 585 591
18. J. García, M.M. Suárez-Varela, J.J. Vilata, A. Marquina, L. Pallardó, and J. Crespo Risk factors for non-melanoma skin cancer in kidney transplant patients in a Spanish population in the Mediterranean region Acta Derm Venereol 93 2013 422 427
19. H. Kauffman, W.S. Cherikh, Y. Cheng, D.W. Hanto, and B.D. Kahan Maintenance immunosuppression with target-of-rapamycin inhibitors is associated with a reduced incidence of de novo malignancies Transplantation 80 2005 883 889
20. L. Mackintosh, C.C. Geddes, and R.M. Herd Skin tumors in the West of Scotland renal transplant population Br J Dermatol 168 2013 1047 1053
21. M. Silverberg, W. Leyden, E.M. Warton, C.P. Quesenberry Jr., E.A. Engels, and M.M. Asgari HIV infection status, immunodeficiency, and the incidence of non-melanoma skin cancer J Natl Cancer Inst 105 2013 350 360
22. N. Muñoz, F.X. Bosch, S. de Sanjosé, R. Herrero, X. Castellsagué, and K.V. Shah et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer N Engl J Med 348 2003 518 527
23. R. Alani, and K. Münger Human papillomaviruses and associated malignancies J Clin Oncol 16 1998 330 337
24. K. Zakrzewska, E. Regalbuto, F. Pierucci, R. Arvia, S. Mazzoli, and A. Gori et al. Pattern of HPV infection in basal cell carcinoma and in perilesional skin biopsies from immunocompetent patients Virol J 9 2012 309
25. M. Karagas, T. Waterboer, Z. Li, H.H. Nelson, K.M. Michael, and J.N. Bavinck et al. Genus beta human papillomaviruses and incidence of basal cell and squamous cell carcinomas of skin: population based case-control study BMJ 341 2010 c2986
26. B.J. Bouwes, M. Feltkamp, L. Struijk, and J. ter Schegget Human papillomavirus infection and skin cancer risk in organ transplant recipients J Investig Dermatol Symp Proc 6 2001 207 211
27. M. Ally, J.Y. Tang, and S.T. Arron Cutaneous human papillomavirus infection and basal cell carcinoma of the skin J Invest Dermatol 133 2013 1456 1458
28. M. Iannacone, T. Gheit, T. Waterboer, A.R. Giuliano, J.L. Messina, and N.A. Fenske et al. Case-control study of cutaneous human papillomavirus infection in basal cell carcinoma of the skin J Invest Dermatol 133 2013 1512 1520
29. M. Iannacone, W. Wang, H.G. Stockwell, K. O'Rourke, A.R. Giuliano, and V.K. Sondak et al. Sunlight exposure and cutaneous human papillomavirus seroreactivity in basal cell and squamous cell carcinomas of the skin J Infect Dis 206 2012 399 406
30. K. Connolly, P. Manders, P. Earls, and R.J. Epstein Papillomavirus- associated squamous skin cancers following transplant immunosuppression: one Notch closer to control Cancer Treat Rev 40 2014 205 214
31. B. Savani, S. Goodman, and A.J. Barrett Can routine posttransplant HPV vaccination prevent commonly occurring epithelial cancers after allogeneic stem cell transplantation? Clin Cancer Res 15 2009 2219 2221
32. M. Madeleine, L.G. Johnson, J.R. Daling, S.M. Schwartz, J.J. Carter, and D. Berg et al. Cohort profile: the skin cancer after organ transplant study Int J Epidemiol 42 2013 1669 1677
33. P. Coursaget, M. Samimi, J.T. Nicol, C. Gardair, and A. Touzé Human Merkel cell polyomavirus: virological background and clinical implications APMIS 121 2013 755 769
34. K. Paulson, J.G. Iyer, A. Blom, E.M. Warton, M. Sokil, and L. Yelistratova et al. Systemic immune suppression predicts diminished Merkel cell carcinoma-specific survival independent of stage J Invest Dermatol 133 2013 642 646
35. J. Girschik, K. Thorn, T.W. Beer, P.J. Heenan, and L. Fritschi Merkel cell carcinoma in Western Australia: a population-based study of incidence and survival Br J Dermatol 165 2011 1051 1057
36. K. Paulson, J.G. Iyer, and P. Nghiem Asymmetric lateral distribution of melanoma and Merkel cell carcinoma in the United States J Am Acad Dermatol 65 2011 35 39
37. A. Mogha, A. Fautrel, N. Mouchet, N. Guo, S. Corre, and H. Adamski et al. Merkel cell polyomavirus small T antigen mRNA level is increased following in vivo UV-radiation PLoS One 5 2010 e11423
38. C. Baez, M.A. Guimarães, R.A. Martins, A.C. Zalona, J.J. Cossatis, and M.G. Zalis et al. Detection of Merkel cell polyomavirus in oral samples of renal transplant recipients without Merkel cell carcinoma J Med Virol 85 2013 2016 2019
39. L. Dreyer, M. Faurschou, M. Mogensen, and S. Jacobsen High incidence of potentially virus-induced malignancies in systemic lupus erythematosus: a long-term followup study in a Danish cohort Arthritis Rheum 63 2011 3032 3037
40. L. Dreyer, L. Mellemkjær, A.R. Andersen, P. Bennett, U.E. Poulsen, and T. Juulsgaard Ellingsen et al. Incidences of overall and site specific cancers in TNFα inhibitor treated patients with rheumatoid arthritis and other arthritides-a follow-up study from the DANBIO registry Ann Rheum Dis 72 2013 79 82
41. I. Santana, N. Gomes Ado, L.D. Lyrio, M.F. Rios Grassi, and M.B. Santiago Systemic lupus erythematosus, human papillomavirus infection, cervical pre-malignant and malignant lesions: a systematic review Clin Rheumatol 30 2011 665 672
42. C. Sawyers The cancer biomarker problem Nature 452 2008 548 552
43. Y. Gu, J.X. Du, and M.L. Ma Sirolimus and non-melanoma skin cancer prevention after kidney transplantation: a meta-analysis Asian Pac J Cancer Prev 13 2012 4335 4339
44. R. Salgo, J. Gossmann, H. Schöfer, H.G. Kachel, J. Kuck, and H. Geiger et al. Switch to a sirolimus-based immunosuppression in long-term renal transplant recipients: reduced rate of (pre-)malignancies and nonmelanoma skin cancer in a prospective, randomized, assessor-blinded, controlled clinical trial Am J Transplant 10 2010 1385 1393
45. J. Alberú, M.D. Pascoe, J.M. Campistol, F.P. Schena, C. Rial Mdel, and M. Polinsky et al. Lower malignancy rates in renal allograft recipients converted to sirolimus-based, calcineurin inhibitor-free immunotherapy: 24-month results from the CONVERT trial Transplantation 92 2011 303 310
46. J. Campistol, J. Eris, R. Oberbauer, P. Friend, B. Hutchison, and J.M. Morales et al. Sirolimus therapy after early cyclosporine withdrawal reduces the risk for cancer in adult renal transplantation J Am Soc Nephrol 17 2006 581 589
47. S. Euvrard, E. Morelon, L. Rostaing, E. Goffin, A. Brocard, and I. Tromme et al. Sirolimus and secondary skin-cancer prevention in kidney transplantation N Engl J Med 367 2012 329 339
48. J.M. Hoogendijk-van den Akker, P.M. Harden, A.J. Hoitsma, C.M. Proby, R. Wolterbeek, and J.N. Bouwes Bavinck et al. Two-year randomized controlled prospective trial converting treatment of stable renal transplant recipients with cutaneous invasive squamous cell carcinomas to sirolimus J Clin Oncol 31 2013 1317 1323
49. I. Marcil, and R.S. Stern Risk of developing a subsequent nonmelanoma skin cancer in patients with a history of nonmelanoma skin cancer Arch Dermatol 136 2000 1524 1530
50. B. Muehleisen, A. Pazhenkottil, L.E. French, and G.F. Hofbauer Nonmelanoma skin cancer in organ transplant recipients: increase without delay after transplant and subsequent acceleration JAMA Dermatol 149 2013 618 620
51. P. Maurice, T. Fenton, N. Cross, I.A. Thomson, S.C. Rennie, and A.M. van Rij A dedicated dermatology clinic for renal transplant recipients: first 5 years of a New Zealand experience N Z Med J 126 2013 27 33
52. X. Wu, B.C. Nguyen, P. Dziunycz, S. Chang, Y. Brooks, and K. Lefort et al. Opposing roles for calcineurin and ATF3 in squamous skin cancer Nature 465 2010 368 372
53. M. Alam, and D. Ratner Cutaneous squamous-cell carcinoma N Engl J Med 344 2001 975 983
54. K. Kraemer Sunlight and skin cancer: another link revealed Proc Natl Acad Sci U S A 94 1997 11 14
55. K. Thoms, C. Kuschal, E. Oetjen, T. Mori, N. Kobayashi, and P. Laspe et al. Cyclosporin A, but not everolimus, inhibits DNA repair mediated by calcineurin: implications for tumorigenesis under immunosuppression Exp Dermatol 20 2011 232 236
56. C. Kuschal, K.M. Thoms, L. Boeckmann, P. Laspe, A. Apel, and M.P. Schön et al. Cyclosporin A inhibits nucleotide excision repair via downregulation of the xeroderma pigmentosum group A and G proteins, which is mediated by calcineurin inhibition Exp Dermatol 20 2011 795 799
57. W. Han, K. Soltani, M. Ming, and Y.Y. He Deregulation of XPC and CypA by cyclosporin A: an immunosuppression-independent mechanism of skin carcinogenesis Cancer Prev Res (Phila) 5 2012 1155 1162
58. H. Rezvani, A.L. Kim, R. Rossignol, N. Ali, M. Daly, and W. Mahfouf et al. XPC silencing in normal human keratinocytes triggers metabolic alterations that drive the formation of squamous cell carcinomas J Clin Invest 121 2011 195 211
59. S. de Feraudy, K. Ridd, L.M. Richards, P.Y. Kwok, I. Revet, and D. Oh et al. The DNA damage-binding protein XPC is a frequent target for inactivation in squamous cell carcinomas Am J Pathol 177 2010 555 562
60. K. Sully, O. Akinduro, M.P. Philpott, A.S. Naeem, C.A. Harwood, and V.E. Reeve et al. The mTOR inhibitor rapamycin opposes carcinogenic changes to epidermal Akt1/PKBα isoform signaling Oncogene 32 2013 3254 3262
61. E.D. Dommasch, K. Abuabara, D.B. Shin, J. Nguyen, A.B. Troxel, and J.M. Gelfand The risk of infection and malignancy with tumor necrosis factor antagonists in adults with psoriatic disease: a systematic review and meta-analysis of randomized controlled trials J Am Acad Dermatol 64 2011 1035 1050
62. G.R. Burmester, R. Panaccione, K.B. Gordon, M.J. McIlraith, and A.P. Lacerda Adalimumab: long-term safety in 23 458 patients from global clinical trials in rheumatoid arthritis, juvenile idiopathic arthritis, ankylosing spondylitis, psoriatic arthritis, psoriasis and Crohn's disease Ann Rheum Dis 72 2013 517 524
63. A. Kimball, J. Schenfeld, N.A. Accortt, M.S. Anthony, K.J. Rothman, and D. Pariser Incidence rates of malignancies and hospitalized infectious events in psoriasis patients with or without treatment and a general population in the US: 2005-2009 Br J Dermatol 170 2014 366 373
64. Ahmad I, Simanyi E, Guroji P, Tamimi IA, Delarosa HJ, Nagar A, et al. Toll-like receptor-4 deficiency enhances repair of UVR-induced cutaneous DNA damage by nucleotide excision repair mechanism. J Invest Dermatol doi:10.1038/jid2013.530. Published online December 10, 2013.
65. E. Demirkaya, I. Cok, E. Durmaz, O.K. Ulutas, N.A. Ayaz, and N. Besbas et al. Genotoxicity of anti-tumor necrosis factor therapy in patients with juvenile idiopathic arthritis Arthritis Care Res 62 2010 73 77
66. A. Faurschou Role of tumor necrosis factor-α in the regulation of keratinocyte cell cycle and DNA repair after ultraviolet-B radiation Dan Med Bull 57 2010 B4179
67. P. Voskamp, C.A. Bodmann, G.E. Koehl, H.G. Rebel, M.G. Van Olderen, and A. Gaumann et al. Dietary immunosuppressants do not enhance UV-induced skin carcinogenesis, and reveal discordance between p53-mutant early clones and carcinomas Cancer Prev Res (Phila) 6 2013 129 138