The Epidemiology of Transplant-Associated Keratinocyte Cancers in Different Geographical Regions

  • Charlotte M. Proby
  • Hermina C. Wisgerhof
  • Delphine Casabonne
  • Adele C. Green
  • Catherine A. Harwood
  • Jan N. Bouwes Bavinck
Part of the Cancer Treatment and Research book series (CTAR, volume 146)

There are believed to be more than 1 million individuals worldwide currently with an organ allograft [1], and a further steep increase in numbers is expected in the next decade. The life-enhancing benefits of organ transplantation are undisputed, but come at a cost. Complications from graft-preserving iatrogenic immunosuppression include a significantly increased risk of malignancy. More than 40 primary malignant neoplasms were reported in the first 4,000 patients to undergo renal transplantation [2], and this early observation has been consistently supported by subsequent studies [3–7].


Transplant Recipient Skin Cancer Basal Cell Carcinoma Renal Transplant Recipient Standardize Incidence Ratio 
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  1. 1.
    Stockfleth E, Ulrich C, Meyer T, Arndt R, Christophers E. Skin diseases following organ transplantation-risk factors and new therapeutic approaches. Transplant Proc. 2001; 33:1848–53.PubMedCrossRefGoogle Scholar
  2. 2.
    Doll R, Kinlen L. Immunosurveillance and cancer: epidemiological evidence. Br Med J 1970; 4:420–2.PubMedCrossRefGoogle Scholar
  3. 3.
    London NJ, Farmery SM, Will EJ, Davison AM, Lodge JP. Risk of neoplasia in renal transplant recipients. Lancet 1995; 346:403–6.PubMedCrossRefGoogle Scholar
  4. 4.
    Penn I. Posttransplant malignancies. Transplant Proc 1999; 31:1260–2.PubMedCrossRefGoogle Scholar
  5. 5.
    Moosa MR. Kaposi’s sarcoma in kidney transplant recipients: a 23-year experience. Q J Med 2005a; 98:205–14.Google Scholar
  6. 6.
    Vajdic CM, McDonald SP, McCredie MR, et al. Cancer incidence before and after kidney transplantation. JAMA 2001; 296:2823–31.CrossRefGoogle Scholar
  7. 7.
    Villeneuve PJ, Schaubel DE, Fenton SS, Shepherd RA, Jiang Y, Mao Y. Cancer incidence among Canadian kidney transplant recipients. Am J Transplant 2007; 7:941–8.PubMedCrossRefGoogle Scholar
  8. 8.
    Adami J, Gäbel H, Lindelöf B, et al. Cancer risk following organ transplantation: a nation-wide cohort study in Sweden. Br J Cancer 2003; 89:1221–7.PubMedCrossRefGoogle Scholar
  9. 9.
    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(9581):59–67.PubMedCrossRefGoogle Scholar
  10. 10.
    Birkeland SA, Storm HH, Lamm LU, et al. Cancer risk after renal transplantation in the Nordic countries 1964–1986. Int J Cancer 1995; 60:183–9.PubMedCrossRefGoogle Scholar
  11. 11.
    Kyllonen L, Salmela K, Pukkala E. Cancer incidence in a kidney-transplanted population. Transplant Int 2000; 13(suppl 1):394–8.Google Scholar
  12. 12.
    Penn I. Occurrence of cancers in immunosuppressed organ transplant recipients. Clin Transplant 1998a; 12:147–58.Google Scholar
  13. 13.
    Penn I. De novo malignancy in pediatric organ transplant recipients. Pediatr Transplant 1998b; 2:56–63.Google Scholar
  14. 14.
    Euvrard S, Kanitakis J, Cochat P, Claudy A. Skin cancers following pediatric organ transplantation. Dermatol Surg 2004; 30:616–21.PubMedCrossRefGoogle Scholar
  15. 15.
    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; 84:225–32.PubMedCrossRefGoogle Scholar
  16. 16.
    Qunibi W, 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; 25:1402–5.PubMedGoogle Scholar
  17. 17.
    Yang TC, Shu KH, Cheng CH, Wu MJ, Lian JD. Malignancy following renal transplantation. Zhonghua Yi Xue Za Zhi (Taipei) 1998; 61:281–8.Google Scholar
  18. 18.
    Hsu R-B, Chen RJ, Chou N-K, et al. Low incidence of malignancy after transplantation in Chinese heart allograft recipients. Transplant Int 2005; 18:283–88.CrossRefGoogle Scholar
  19. 19.
    Moosa MR. Racial and ethnic variations in incidence and pattern of malignancies after kidney transplantation. Medicine 2005b; 84:12–22.CrossRefGoogle Scholar
  20. 20.
    Ko CB, Walton S, Keczkes K, Bury HP, Nicholson C. The emerging epidemic of skin cancers. Br J Dermatol 1994; 130:269–72.PubMedCrossRefGoogle Scholar
  21. 21.
    Miller DL, Weinstock MA. Nonmelanoma skin cancer in the United States: incidence. J Am Acad Dermatol 1994; 30:774–8.PubMedCrossRefGoogle Scholar
  22. 22.
    Marks R. An overview of skin cancers. Incidence and causation. Cancer 1995; 75:607–12.Google Scholar
  23. 23.
    Miller SJ. Biology of basal cell carcinoma. Part I. J Am Acad Dermatol 1991; 24:1–13.PubMedCrossRefGoogle Scholar
  24. 24.
    Miller SJ. Biology of basal cell carcinoma. Part II. J Am Acad Dermatol 1991; 24:161–75.PubMedCrossRefGoogle Scholar
  25. 25.
    Leman JA, McHenry PM. Basal cell carcinoma: still an enigma. Arch Dermatol 2001; 137:1239–40.PubMedGoogle Scholar
  26. 26.
    Rubin AI, Chen EH, Ratner D. Basal cell carcinoma. N Engl J Med 2005; 353:2262–9.PubMedCrossRefGoogle Scholar
  27. 27.
    Kwa RE, Campana K, Moy RL. Biology of cutaneous squamous cell carcinoma. J Am Acad Dermatol 1992; 26:1–26.PubMedCrossRefGoogle Scholar
  28. 28.
    Alam M, Ratner D. Cutaneous squamous cell carcinoma. N Engl J Med 2001; 344L:975–83.CrossRefGoogle Scholar
  29. 29.
    Holme SA, Malinovszky K, Roberts DL. Changing trends in non-melanoma skin cancer in South Wales, 1988–98. Br J Dermatol 2000; 143;1224–9.PubMedCrossRefGoogle Scholar
  30. 30.
    Staples M, Marks R, Giles G. Trends in the incidence of non-melanocytic skin cancer (NMSC) treated in Australia 1985–1995: are primary prevention programs starting to have an effect? Int J Cancer 1998; 78:144–8.PubMedCrossRefGoogle Scholar
  31. 31.
    Trakatelli M, Ulrich C, del Marmol V, Euvrard S, Stockfleth E, Abeni D. Epidemiology of nonmelanoma skin cancer (NMSC) in Europe: accurate and comparable data are needed for effective public health monitoring and interventions. Br J Dermatol 2007; 156(suppl):1–7.PubMedCrossRefGoogle Scholar
  32. 32.
    Hoy WE. Nonmelanoma skin carcinoma in Albuquerque, New Mexico: experience of a major health care provider. Cancer 1996; 77:2489–95.PubMedCrossRefGoogle Scholar
  33. 33.
    Kodama M, Murakami M, Kodama T. Chronological transition of the age-adjusted incidence rates (AAIRs) of 20 major neoplasias from early 1960s to mid-1980s. Anticancer Res 1999; 19:779–87.PubMedGoogle Scholar
  34. 34.
    Karagas MR, Greenberg ER, Spencer SK, Stukel RA, Mott LA. Increase in incidence rates of basal cell and squamous cell skin cancer in New Hampshire, USA. New Hampshire Skin Cancer Study Group. Int J Cancer 1999; 81:555–9.PubMedCrossRefGoogle Scholar
  35. 35.
    Diepgen TL, Mahler V. The epidemiology of skin cancer. Br J Dermatol 2002; 146(suppl 61): 1–6.PubMedCrossRefGoogle Scholar
  36. 36.
    Giannakouris K. Ageing characterises the demographic perspectives of the European Societies. Eurostat Statistics in Focus 72/2008 population and Social Conditions: Population Projectious.
  37. 37.
    Nguyen TH, Ho DQ. Nonmelanoma skin cancer. Curr Treat Options Oncol 2002; 3:193–203.PubMedCrossRefGoogle Scholar
  38. 38.
    Lucke TW, Hole DJ, Mackie RM. An audit of the completeness of non-melanoma skin cancer registration in Greater Glasgow. Br J Dermatol 1997; 137:761–3.PubMedCrossRefGoogle Scholar
  39. 39.
    Lucas R, McMichael T, Smith W, et al. Environmental Burden of Disease Series No 13. Solar Ultraviolet Radiation. Global Burden on Disease from Solar Ultraviolet Radiation. Geneva: World Health Organisation, Public Health and Environment, 2006.Google Scholar
  40. 40.
    40. Series MB1 no. 35. Cancer Statistics Registrations. Registrations of Cancer Diagnosed in 2004, England. London: Office for National Statistics, 2006. Available at (last accessed 29 March 2007).
  41. 41.
    Eedy DJ. Non-melanoma skin cancer and the ‘new National Health Service’: implications for U.K. dermatology? Br J Dermatol 2000; 142:397–9.PubMedCrossRefGoogle Scholar
  42. 42.
    Housman TS, Feldman SR, Williford PM, et al. Skin cancer is among the most costly of all cancers to treat for the Medicare population. J Am Acad Dermatol 2003; 48:425–9.PubMedCrossRefGoogle Scholar
  43. 43.
    Walder B, Robertson M, Jeremy D. Skin cancer and immunosuppression. Lancet 1971; 2:1282.PubMedCrossRefGoogle Scholar
  44. 44.
    Hoover R, Fraumeni JF. Risk of cancer in renal-transplant recipients. Lancet 1973; 2(7820):55–7.PubMedCrossRefGoogle Scholar
  45. 45.
    Marshall V. Premalignant and malignant skin tumours in immunosuppressed patients. Transplantation 1974; 17:272–5.PubMedCrossRefGoogle Scholar
  46. 46.
    Koranda FC, Dehmel EM, Kahn G, Penh I. Cutaneous complications in immunosuppressed renal homograft recipients. JAMA 1974; 229:419–24.PubMedCrossRefGoogle Scholar
  47. 47.
    Mullen DL, Silverberg SG, Penn I, Hammond WS. Squamous cell carcinoma of the skin and lip in renal homograft recipients. Cancer 1976; 37:729–34.PubMedCrossRefGoogle Scholar
  48. 48.
    Sheil AG. Cancer in renal allograft recipients in Australia and New Zealand. Transplant Proc 1977; 9:1133–6.PubMedGoogle Scholar
  49. 49.
    Hoxtell EO, Mandel JS, Murray SS, Schuman LM, Goltz RW. Incidence of skin carcinoma after renal transplantation. Arch Dermatol 1977; 113:436–8.PubMedCrossRefGoogle Scholar
  50. 50.
    Kinlen LJ, Sheil AG, Peto J, Doll R. Collaborative United Kingdom-Australasian study of cancer in patients treated with immunosuppressive drugs. Br Med J 1979; 2:1461–6.PubMedCrossRefGoogle Scholar
  51. 51.
    Hardie IR, Strong RW, Hartley LC, Woodruff PW, Clunie GJ. Skin cancer in Caucasian renal allograft recipients living in a subtropical climate. Surgery 1980; 87:177–83.PubMedGoogle Scholar
  52. 52.
    Cohen EB, Komorowski RA, Clowry LJ. Cutaneous complications in renal transplant recipients. An J Clin Pathol 1987; 88:32–7.Google Scholar
  53. 53.
    Hartevelt M, Bouwes-Bavinck J, Koote J, et al. Incidence of skin cancer after renal transplantation in the Netherlands. Transplantation 1990; 49:506–9.PubMedCrossRefGoogle Scholar
  54. 54.
    Birkeland SA. Malignant tumors in renal transplant patients. The Scandia transplant material. Cancer 1983; 51:1571–5.PubMedCrossRefGoogle Scholar
  55. 55.
    Blohme I, Larko O. Premalignant and malignant skin lesions in renal transplant patients. Transplantation 1984; 37:165–7.PubMedGoogle Scholar
  56. 56.
    Boyle J, MacKie RM, Briggs JD, Junor BJ, Aitchison TC. Cancer, warts and sunshine in renal transplant patients. A case-control study. Lancet 1984; 1:702–5.PubMedCrossRefGoogle Scholar
  57. 57.
    Liddington M, Richardson AJ, Higgins RM, Endre ZH, Venning VA, Murie JA, Morris PJ. Skin cancer in renal transplant recipients. Br J Surg 1989; 76:1002–5.PubMedCrossRefGoogle Scholar
  58. 58.
    Glover MT, Deeks JJ, Raftery MJ, Cunningham J, Leigh IM. Immunosuppression and risk of non-melanoma skin cancer in renal transplant recipients. Lancet 1997; 349:398.PubMedCrossRefGoogle Scholar
  59. 59.
    Brown JH, Hutchison T, Kelly AM, McGeown MG. Dermatologic lesions in a transplant population. Transplantation 1988; 46:530–2.PubMedCrossRefGoogle Scholar
  60. 60.
    Montagnino G, Larca E, Tarantino A, Bencini P, Aroldi A, Cesana B, Braga M, Lonati F, Ponticelli C. Cancer incidence in 854 kidney transplant recipients from a single institution: comparison with normal population and with patients under dialytic treatment. Clin Transplant 1996; 10:461–9.PubMedGoogle Scholar
  61. 61.
    Espana A, Redondo P, Fernandez AL, Zabala M, Herreros J, Llorens R, Quintanilla E. Skin cancer in heart transplant recipients. J Am Acad Dermatol 1995; 32:458–65.PubMedCrossRefGoogle Scholar
  62. 62.
    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; 40:177–86.PubMedCrossRefGoogle Scholar
  63. 63.
    Lindelöf B, Sigurgeirsson B, Gäbel H, Stern RS. Incidence of skin cancer in 5356 patients following organ transplantation. Br J Dermatol 2000; 143:513–9.PubMedGoogle Scholar
  64. 64.
    Moloney FJ, Comber H, O’Lorcain P, et al. A population-based study of skin cancer incidence and prevalence in renal transplant recipients. Br J Dermatol 2006; 154:498–504.PubMedCrossRefGoogle Scholar
  65. 65.
    Bouwes-Bavinck J, Hardie D, Green A, et al. The risk of skin cancer in renal transplant recipients in Queensland, Australia. Transplantation 1996; 61:715–21.PubMedCrossRefGoogle Scholar
  66. 66.
    Ong C, Keogh A, Kossard S, et al. Skin cancer in Australian heart transplant recipients. J Am Acad Dermatol 1999; 40:27–34.PubMedCrossRefGoogle Scholar
  67. 67.
    Ramsay HM, Fryer AA, Hawley CM, et al. Factors associated with non-melanoma skin cancer following renal transplantation in Queensland, Australia. J Am Acad Dermatol 2003; 49:397–406.PubMedCrossRefGoogle Scholar
  68. 68.
    Hoshida Y, Aozasa K. Malignancies in organ transplant recipients. Pathol Int 2004; 54:649–58.PubMedCrossRefGoogle Scholar
  69. 69.
    Moosa MR, Gralla J. Skin cancer in renal allograft recipients: experience in different ethnic groups residing in the same geographical region. Clin Transplant 2005c; 19:735–41.Google Scholar
  70. 70.
    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; 147:950–6.PubMedCrossRefGoogle Scholar
  71. 71.
    Carroll RP, Ramsay HM, Hawley CM, Smith AG, Nicol DL, Harden PN. Incidence and prediction of nonmelanoma skin cancer post-renal transplantation: a prospective study in Queensland, Australia. Am J Kidney Dis 2003; 49:397–406.Google Scholar
  72. 72.
    Fuente MJ, Sabat M, Roca J, et al. A prospective study of the incidence of skin cancer and its risk factor in a Spanish Mediterranean population of kidney transplant recipients. Br J Dermatol 2003; 149:1221–6.PubMedCrossRefGoogle Scholar
  73. 73.
    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; 29:828–30.PubMedCrossRefGoogle Scholar
  74. 74.
    Bordea C, Wojnarowska F, Millard PR, et al. Skin cancer in renal-transplant recipients occur more frequently than previously recognized in a temperate climate. Transplantation 2004; 77:574–79.PubMedCrossRefGoogle Scholar
  75. 75.
    Euvrard S, Kanitakis J, Claudy A. Skin cancers after organ transplantation. N Engl J Med 2003; 348:1681–91.PubMedCrossRefGoogle Scholar
  76. 76.
    Otley CC, Cherikh WS, Salasche SJ, McBride MA, Cristenson LJ, Kauffman HM. Skin cancer in organ transplant recipients: effect of pretransplant end-organ disease. J Am Acad Dermatol 2005; 53:783–90.PubMedCrossRefGoogle Scholar
  77. 77.
    Naldi L, Fortina AB, Lovati S et al. Risk of nonmelanoma skin cancer in Italian organ transplant recipients. A registry-based study. Transplantation 2000; 70:1479–84.Google Scholar
  78. 78.
    Agraharkar ML, Cinclair RD, Kuo YF, Daller JA, Shahinian VB. Risk of malignancy with long-term immunosuppression in renal transplant recipients. Kidney Int 2004; 66:282–9.CrossRefGoogle Scholar
  79. 79.
    McGregor JM, Proby CM. Skin cancer in transplant recipients (correspondence to 3 London et al., 1995). Lancet 1995; 364:964–5.CrossRefGoogle Scholar
  80. 80.
    Gupta AK, Cardella CJ, Haberman HF. Cutaneous malignant neoplasms in patients with renal transplants. Arch Dermatol 1986; 122:1288–93.PubMedCrossRefGoogle Scholar
  81. 81.
    Fortina AB, Caforio AL, Piaserico S, et al. Skin cancer in heart transplant recipients: frequency and risk factor analysis. J Heart Lung Transplant 2000; 19:249–55.PubMedCrossRefGoogle Scholar
  82. 82.
    Ferrándiz C, Fuente MJ, Ribera M, Bielsa I, Fernandez MT, Lauzurica R, Roca J. Epidermal dysplasia and neoplasia in kidney transplant recipients. J Am Acad Dermatol 1995; 33:590–6.PubMedCrossRefGoogle Scholar
  83. 83.
    Caforio AL, Fortina AB, Piaserico S, et al. Skin cancer in heart transplant recipients: risk factor analysis and relevance of immunosuppressive therapy. Circulation 2000; 103(III):222–7.Google Scholar
  84. 84.
    Marcen R, Pascual J, Tato AM, et al. Influence of immunosuppression on the prevalence of cancer after kidney transplantation. Transplant Proc 2003; 35:1714–6.PubMedCrossRefGoogle Scholar
  85. 85.
    Giles GG, Marks R, Foley P. Incidence of non-melanocytic skin cancer treated in Australia. Br Med J (Clin Res Ed) 1988; 296:13–7.CrossRefGoogle Scholar
  86. 86.
    Gjersvik P, Hansen S, Moller B, et al. Are heart transplant recipients more likely to develop skin cancer than kidney transplant recipients? Transplant Int 2000; 13(suppl 1):5380–1.Google Scholar
  87. 87.
    Herrero JI, Espana A, Quiroga J et al. Nonmelanoma skin cancer after liver transplantation. Study of risk factors. Liver Transplant 2005; 11:1100–6.CrossRefGoogle Scholar
  88. 88.
    Haagsma EB, Hagens VE, Schaapveld M, et al. Increased cancer risk after liver transplantation: a population-based study. J Hepatol 2001; 34:84–91.PubMedCrossRefGoogle Scholar
  89. 89.
    Harden PN, Fryer AA, Reece S, Smith AG, Ramsay HM. Annual incidence and predicted risk of nonmelanoma skin cancer in renal transplant recipients. Transplant Proc 2001; 33:1302–4.PubMedCrossRefGoogle Scholar
  90. 90.
    Mithoefer AB, Supran S, Freeman RB. Risk factors associated with the development of skin cancer after liver transplantation. Liver Transplant 2002; 8:939–44.CrossRefGoogle Scholar
  91. 91.
    Bouwes Bavinck JN, de Boer A, Vermeer BJ, et al. Sunlight, keratotic skin lesions and skin cancer in renal transplant recipients. Br J Dermatol 1993; 129:242–49.CrossRefGoogle Scholar
  92. 92.
    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; 127:1647–56.PubMedGoogle Scholar
  93. 93.
    Mihalov ML, Gattuso P, Abraham K, Holmes EW, Reddy V. Incidence of post-transplant malignancy among 674 solid-organ-transplant recipients at a single center. Clin Transplant 1996; 10:248–55.PubMedGoogle Scholar
  94. 94.
    Wu MJ, Lian JD, Yang CR, et al. High cumulative incidence of urinary tract transitional cell carcinoma after kidney transplantation in Taiwan. Am J Kidney Dis 2004; 43:1091–7.PubMedCrossRefGoogle Scholar
  95. 95.
    Penn I. Sarcomas in organ allograft recipients. Transplantation 1995; 60:1485–91.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Charlotte M. Proby
    • 1
  • Hermina C. Wisgerhof
    • 2
  • Delphine Casabonne
    • 3
  • Adele C. Green
    • 4
  • Catherine A. Harwood
    • 5
    • 6
  • Jan N. Bouwes Bavinck
    • 7
  1. 1.Division of Surgery and OncologyCollege of Medicine, Dentistry and Nursing, University of Dundee, Ninewells HospitalDundeeUnited Kingdom
  2. 2.Department of DermatologyLeiden University Medical CenterThe Netherlands
  3. 3.Cancer Epidemiology Unit, Richard Doll BuildingUniversity of OxfordOxfordUnited Kingdom
  4. 4.Queensland Institute of Medical ResearchBrisbaneAustralia
  5. 5.Center for Cutaneous Research, Institute of Cell andMolecular ScienceBarts and The London, School of Medicine and Dentistry, Queen Mary University of LondonLondon
  6. 6.Department of DermatologyBarts and the London NHS TrustLondonUnited Kingdom
  7. 7.Department of DermatologyLeiden University Medical CenterThe Netherlands

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