A surveillance model for skin cancer in organ transplant recipients: A 22-year prospective study in an ethnically diverse population

American Journal of Transplantation

Volumn 13, Issue 1, 2013, Pages 119-129

  Harwood, C A ^a,b   Mesher, D ^a   McGregor, J M ^a,b   Mitchell, L ^a   Leedham Green, M ^a   Raftery, M ^b   Cerio, R ^b   Leigh, I M ^a,b   Sasieni, P ^a   Proby, C M ^a,b  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b BARTS HEALTH NHS TRUST   (United Kingdom)

Author keywords

Basal cell carcinoma; melanoma; skin cancer; skin cancer prevention; skin cancer surveillance; squamous cell carcinoma; ultraviolet radiation

Indexed keywords

AZATHIOPRINE; CYCLOSPORIN; MYCOPHENOLIC ACID; PREDNISOLONE; TACROLIMUS;

ADOLESCENT; ADULT; AGE; AGED; ARTICLE; BASAL CELL CARCINOMA; CANCER EPIDEMIOLOGY; CANCER INCIDENCE; CANCER MORTALITY; CHILD; COHORT ANALYSIS; DERMATOFIBROSARCOMA PROTUBERANS; EVIDENCE BASED MEDICINE; FEMALE; GRAFT RECIPIENT; HUMAN; KAPOSI SARCOMA; KIDNEY TRANSPLANTATION; MAJOR CLINICAL STUDY; MALE; MELANOMA; MERKEL CELL TUMOR; MORBIDITY; PREDICTOR VARIABLE; PRIORITY JOURNAL; PROSPECTIVE STUDY; RADIATION EXPOSURE; RISK FACTOR; SCHOOL CHILD; SKIN CANCER; SKIN CARCINOMA; SKIN LYMPHOMA; TREATMENT DURATION; ULTRAVIOLET RADIATION; UNITED KINGDOM;

ADOLESCENT; ADULT; AGED; CHILD; ETHNIC GROUPS; FEMALE; GREAT BRITAIN; HUMANS; MALE; MIDDLE AGED; ORGAN TRANSPLANTATION; POPULATION SURVEILLANCE; PROSPECTIVE STUDIES; SKIN NEOPLASMS; YOUNG ADULT;

EID: 84871719483     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2012.04292.x     Document Type: Article

References (65)

1. Kasiske BL, Snyder JJ, Gilbertson DT, Wang C,. Cancer after kidney transplantation in the United States. Am J Transplant 2004; 4: 905-913.
2. Vajdic CM, McDonald SP, McCredie MR, et al.. Cancer incidence before and after kidney transplantation. JAMA 2006; 296: 2823-2831.
3. Webster AC, Craig JC, Simpson JM, Jones MP, Chapman JR,. Identifying high risk groups and quantifying absolute risk of cancer after kidney transplantation: A cohort study of 15,183 recipients. Am J Transplant 2007; 7: 2140-2151.
4. Wisgerhof HC, van der Geest LGM, de Fijter JW, et al.. Incidence of cancer in kidney-transplant recipients: A long-term cohort study in a single center. Cancer Epidemiol 2011; 35: 105-111.
5. 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.
6. Feltkamp M C, de Koning M N, Bavinck J N, Ter Schegget J,. Betapapillomaviruses: Innocent bystanders or causes of skin cancer. J Clin Virol. 2008: 43: 353-360.
7. Feng H, Shuda M, Chang Y, Moore PS,. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 2008; 319: 1096-1100.
8. Qunibi W, Akhtar M, Sheth K, et al.. Kaposi's sarcoma: The most common tumor after renal transplantation in Saudi Arabia. Am J Med 1988; 84: 225-232.
9. Yang TC, Shu KH, Cheng CH, Wu MJ, Lian JD,. Malignancy following renal transplantation. Zhonghua Yi Xue Za Zhi (Taipei) 1998; 61: 281-288.
10. Euvrard S, Kanitakis J, Claudy A,. Skin cancers after organ transplantation. N Engl J Med 2003; 348: 1681-1691.
11. Walder B, Robertson M, Jeremy D,. Skin cancer and immunosuppression. Lancet 1971; 2: 1282.
12. Proby CM, Wisgerhof HC, Casabonne D, Green AC, Harwood CA, Bouwes Bavinck JN,. The epidemiology of transplant-associated keratinocyte cancers in different geographical regions. Skin Cancer after organ transplantation. In:, Rosen T, ed. Cancer Treatment and Research 146. NY: Springer, 2009: pp. 75-95.
13. Berg D, Otley CC,. Skin cancer in organ transplant recipients: Epidemiology, pathogenesis, and management. J Am Acad Dermatol. 2002; 47: 1-17. Review.
14. Jensen AO, Svaerke C, Farkas D, Pedersen L, Kragballe K, Sàrensen HT,. Skin cancer risk among solid organ recipients: A nationwide cohort study in Denmark. Acta Derm Venereol 2010: 474-479.
15. Alama M, Brown RN, Silberc DH, et al.. Increased incidence and mortality associated with skin cancers after cardiac transplant. Am J Transplant 2011; 11: 1488-1497.
16. Hofbauer GFL, Bouwes Bavinck JN, Euvrard S,. Organ transplantation and skin cancer: Basic problems and new perspectives. Exp Dermatol 2010; 19: 473-482.
17. Hojo M, Morimoto T, Maluccio M, et al.. Cyclosporine induces cancer progression by a cell-autonomous mechanism. Nature 1999: 397: 530-534.
18. Yarosh DB, Pena AV, Nay SL, Canning MT, Brown DA,. Calcineurin inhibitors decrease DNA repair and apoptosis in human keratinocytes following ultraviolet B irradiation. J Invest Dermatol 2005; 125: 1020-1025.
19. Duncan FJ, Wulff BC, Tober KL, et al.. Clinically relevant immunosuppressants influence UVB-induced tumor size through effects on inflammation and angiogenesis. Am J Transplant 2007; 7: 2693-2703.
20. Norman KG, Canter JA, Shi M, Milne GL, Morrow JD, Sligh JE,. Cyclosporine A suppresses keratinocyte cell death through MPTP inhibition in a model for skin cancer in organ transplant recipients. Mitochondrion 2010; 94-101.
21. Wu X, Nguyen BC, Dziunycz P, et al.. Opposing roles for calcineurin and ATF3 in squamous skin cancer. Nature 2010; 465: 368-372.
22. Han W, Ming M, He TC, He YY,. Immunosuppressive cyclosporin A activates AKT in keratinocytes through PTEN suppression: Implications in skin carcinogenesis. J Biol Chem 2010; 285: 11369-11377.
23. Kuschal C, Thoms KM, Boeckmann L, 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 2011; 20: 795-799.
24. O'Donovan P, Perrett C, Zhang X, et al.. The immunosuppressant azathioprine and UVA light generate mutagenic oxidative DNA damage. Science 2005; 309: 1871-1874.
25. Perrett CM, Walker SL, O'Donovan P, et al.. Azathioprine photosensitises human skin to UV-A radiation. Br J Dermatol 2008; 159: 198-204.
26. Harwood CA, Attard NR, O' Donovan P, et al.. PTCH mutations in basal cell carcinomas from azathioprine-treated organ transplant recipients. Br J Cancer 2008; 99: 1276-1284.
27. Hofbauer GF, Attard NR, Harwood CA, et al.. Reversal of UVA skin photosensitivity and DNA damage in kidney transplant recipients by replacing azathioprine. Am J Transplant 2012; 12: 218-225.
28. Attard NR, Karran P,. UVA photosensitization of thiopurines and skin cancer in organ transplant Recipients. Photochem Photobiol Sci 2012; 11: 62-68.
29. Laing ME, Dicker P, Moloney FJ, et al.. Association of methylenetetrahydrofolate reductase polymorphism and the risk of squamous cell carcinoma in renal transplant patients. Transplantation 2007; 84: 113-116.
30. Proby CM, Harwood CA, Neale RE, et al.. A case-control study of betapapillomavirus infection and cutaneous squamous-cell carcinoma in organ transplant recipients. Am J Transplantation 2011; 11: 1498-1508.
31. National Institute for Health and Clinical Excellence. Improving outcomes for people with skin tumours including melanoma: The manual (2006 guidance).
32. Christenson LJ, Geusau A, Ferrandiz C, et al.. Specialty clinics for the dermatologic care of solid-organ transplant recipients. Dermatol Surg 2004; 30: 598-603. Review.
33. Stasko T, Brown MD, Carucci JA, et al.. International Transplant-Skin Cancer Collaborative; European Skin Care in Organ Transplant Patients Network. Guidelines for the management of squamous cell carcinoma in organ transplant recipients. Dermatol Surg 2004; 30: 642-650.
34. Ulrich C, Kanitakis J, Stockfleth E, Euvrard S,. Skin cancer in organ transplant recipients-where do we stand today ? Am J Transplant 2008; 11: 2192-8. Review.
35. KDIGO clinical practice guideline for the care of kidney transplant recipients. Kidney Disease: Improving Global Outcomes (KDIGO) Transplant Work Group. Chapter 18. Cancer of the Skin and Lip. Am J Transplant 2009; 9: S84-S85.
36. Zwald FO, Brown M,. 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 2011; 2: 263-279
37. Ismail F, Mitchell L, Casabonne D, Newton R, Proby CM, Harwood CA,. Specialist dermatology clinics for organ transplant recipients significantly improve compliance with photoprotection and levels of skin cancer awareness. Br J Dermatol 2006; 155: 916-925
38. Bouwes Bavinck JN, Euvrard S, Naldi L, et al.. Keratotoic skin lesions and other risk factors are associated with skin cancer in organ transplant recipients: A case-control study in The Netherlands, United Kingdom, Germany, France and Italy. J Invest Dermatol 2007; 127: 1647-1656.
39. Casabonne D, Lally A, Mitchell L, et al.. A case-control study of cutaneous squamous cell carcinoma among Caucasian organ transplant recipients: The role of antibodies against human papillomavirus (HPV) and other risk factors. Int J Cancer 2009; 125: 1935-1945.
40. Bordea C, Wojnarowska F, Millard PR, Doll H, Welsh K, Morris PJ,. Skin cancer in renal-transplant recipients occur more frequently than previously recognized in a temperate climate. Transplantation 2004; 77: 574-579.
41. Moloney FJ, Comber H, O'Lorcain P, O'Kelly P, Conlon PJ, Murphy GM,. A population-based study of skin cancer incidence and prevalence in renal transplant recipients. Br J Dermatol 2006; 154: 498-504.
42. Ramsay HM, Reece SM, Fryer AA, Smith AG, Harden PN,. Seven-year prospective study of nonmelanoma skin cancer incidence in U.K. renal transplant recipients. Transplantation 2007; 84: 437-439.
43. Wisgerhof HC, Edelbroek JR, de Fijter JW, et al.. Subsequent squamous- and basal-cell carcinomas in kidney-transplant recipients after the first skin cancer: Cumulative incidence and risk factors. Transplantation 2010; 89: 1231-1238.
44. Lindelof B, Sigurgeirsson B, Gabel H, Stern RS,. Incidence of skin cancer in 5356 patients following organ transplantation. Br J Dermatol 2000; 143: 513.
45. Euvrard S, Kanitakis J, Decullier E, et al.. Subsequent skin cancers in kidney and heart transplant recipients after the first squamous cell carcinoma. Transplantation 2006; 81: 1093-1100.
46. Brewer JD, Colegio OR, Phillips PK, et al.. Incidence of and risk factors for skin cancer after heart transplant. Arch Dermatol 2009; 145: 1391-1396.
47. Mackenzie KA, Wells JE, Lynn KL, et al.. First and subsequent nonmelanoma skin cancers: Incidence and predictors in a population of New Zealand renal transplant recipients. Nephrol Dial Transplant 2010; 25: 300.
48. Tessari G, Naldi L, Boschiero L, et al.. Incidence and clinical predictors of a subsequent nonmelanoma skin cancer in solid organ transplant recipients with a first nonmelanoma skin cancer: A multicenter cohort study. Arch Dermatol 2010; 146: 294-299.
49. Marcil I, Stern RS,. Risk of developing a subsequent nonmelanoma skin cancer in patients with a history of nonmelanoma skin cancer: A critical review of the literature and meta-analysis. Arch Dermatol 2000; 136: 1524.
50. Weigert AL, Pires A, Adraga T, et al.. Human herpes virus-8 serology and DNA analysis in recipients of renal allografts showing Kaposi's sarcoma and their respective donors. Transplant Proc 2004; 36: 902-904.
51. Lebbé C, Legendre C, Francès C,. Kaposi sarcoma in transplantation. Transplant Rev 2008; 22: 252-261.
52. Frances, C, Lebbé C,. Kaposi's Sarcoma. The SCOPE Collaborative Group (eds). Skin Cancer after organ transplantation. In:, Rosen T, ed. Cancer Treatment and Research 146. Rosen T, Series Editor. NY: Springer, 2009: pp. 467-481.
53. Brown VL, Matin RN, Leedham-Green M, Cerio R, Proby CM, Harwood CA,. Melanomas in renal transplant recipients: The London experience, and invitation to participate in a European study. Br J Dermatol 2007; 156: 165-167.
54. Matin RN, Mesher D, Proby CM, et al.. Melanoma in organ transplant recipients: Clinicopathological features and outcome in 100 cases. Am J Transplantation 2008; 8: 1191-1900.
55. Brewer JD, Christenson LJ, Weaver AL,. et al.. Malignant melanoma in solid transplant recipients collection of database cases and comparison with surveillance, epidemiology, and end results data for outcome analysis. Arch Dermatol 2011; 147: 790-796.
56. Harwood CA, McGregor JM, Swale VJ, et al.. High frequency and diversity of cutaneous appendageal tumours in organ transplant recipients. J Am Acad Dermatol 2003; 48: 401-408.
57. Harwood CA, Proby CM, Cerio R,. Appendageal malignancies. In:, J-N Bouwes Bavinck, et al.., Eds. Advances in Cutaneous Transplant Oncology. NY: Springer, 2009: 146: 353-374.
58. Koljonen V, Kukko H, Tukiainen E, et al.. Incidence of Merkel cell carcinoma in renal transplant recipients. Nephrol Dial Transplant 2009; 24: 3231-3235.
59. Kanitakis J,. Merkel cell carcinoma. In:, J-N Bouwes Bavinck, et al.., Eds. Advances in Cutaneous Transplant Oncology. NY: Springer, 2009: 146: 329-341.
60. Webster AC, Wong G, Craig JC, Chapman JR,. Managing cancer risk and decision making after kidney transplantation. Am J Transplant 2008; 11: 2185-2191.
61. Otley CC,. Pre-transplantation dermatologic screening and prophylaxis. The SCOPE Collaborative Group (eds). Skin Cancer after organ transplantation. Cancer Treatment and Research 146. Rosen T, Series Editor. Springer, 2009: pp. 391-404.
62. Singh MK, Brewer JD,. Current approaches to skin cancer management in organ transplant recipients. Semin Cutan Med Surg 2011; 30: 35-47.
63. Moosa MR, Gralla J,. Skin cancer in renal allograft recipients-Experience in different ethnic groups residing in the same geographical region. Clin Transplant 2005; 19: 735-741.
64. Serraino D, Piselli P, Angeletti C, et al.. Risk of Kaposi's sarcoma and of other cancers in Italian renal transplant patients. Br J Cancer 2005; 92: 572-575.
65. Einollahi B, Nemati E, Lessan-Pezeshki M, et al.. Skin cancer after renal transplantation: Results of a multicenter study in Iran. Ann Transplant 2010; 15: 44-50.