Cell and Tissue Banking

, Volume 16, Issue 4, pp 503–512 | Cite as

The risk of transmitting cutaneous malignancy through skin transplantation: a literature-based risk assessment

  • Sarah BosmaEmail author
  • Marja J. Van Wijk
  • Cornelia D. Richters
  • Hilde Beele
Original Paper


According to the European Union Tissues and Cells Directives donation of tissue is contraindicated in the presence of or a previous history of malignant disease, with the exception of cutaneous basal cell carcinoma. Skin cancer is the most common cancer. Due to ultraviolet light exposure and increasing life expectancy an increasing prevalence of malignant or premalignant skin lesions is observed, which may result in a decline of the availability of skin for transplantation. A risk assessment based on published studies and expert opinion was performed in order to investigate the risk of transmitting malignant or premalignant skin lesions through tissue transplantation, and more particular through skin transplantation. The scarcity of data concerning cancer transmission in tissue transplantation was challenging. Circumstantial evidence, available for organ transplantation, was used to develop the following policy proposal for skin transplantation and cutaneous tumours. Malignant melanoma is an absolute contraindication for the donation of skin and also of other tissues, whereas, non-lesional skin and other tissues of a donor with non-melanoma skin cancer (basal cell and squamous cell carcinoma) or with a premalignant skin lesion can be considered for transplantation. The above mentioned protocol proposal might serve as a prototype for analogous protocols for non-cutaneous malignancies.


Tissue transplantation Cutaneous malignancies Transmission Risk assessment Guidelines 


  1. Akgül B, Akgül J, Cooke A (2006) HPV-associated skin disease. J Pathol 208(2):165–175CrossRefPubMedGoogle Scholar
  2. Bajaj NS, Watt C, Hadjiliadis D, Gillespie C, Haas AR, Pochettino A, Mendez J, Sterman DH, Schuchter LM, Christie JD, Lee JC, Ahya VN (2010) Donor transmission of malignant melanoma in a lung transplant recipient 32 years after curative resection. Transpl Int: Off J Eur Soc Organ Transplant 23(7):e26–e31. doi: 10.1111/j.1432-2277.2010.01090.x CrossRefGoogle Scholar
  3. Bavinck J, Feltkamp L, Struijk J, ter Schegget J (2001) Human papillomavirus infection and skin cancer risk in organ transplant recipients. J Investig Dermatol Symp Proc 6(3):207–211CrossRefGoogle Scholar
  4. Beele H, Van Wijk M, Bokhorst A, Van Geyt C (2009) Physical examination of the potential tissue donor, what does literature tell us? Cell Tissue Bank 10(3):253–257. doi: 10.1007/s10561-008-9116-x CrossRefPubMedGoogle Scholar
  5. Beele H, Van Wijk M, Parker R, Sánchez-Ibáňez J, Brubaker S, Wulff B, Richters C, Cox M, Warwick RM, Eastlund T (2013) Report of the clinical donor case workshop of the European Association of Tissue Banks Annual meeting 2012. Cell Tissue Banking 14:561–570CrossRefPubMedGoogle Scholar
  6. Berkhout RJM, Bouwes Bavinck J, Ter Schegget J (2000) Persistence of human papillomavirus DNA in benign and (pre) malignant skin lesions from renal transplant recipients. J Clin Microbiol 38(6):2087PubMedCentralPubMedGoogle Scholar
  7. Bernard H, Burk R, Chen Z, van Doorslaer K, Hausen H, de Villiers E (2010) Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401(1):70–79PubMedCentralCrossRefPubMedGoogle Scholar
  8. Bonatti H, Brandacher G, Margreiter R, Schneeberger S (2009) Infectious complications in three double hand transplant recipients: experience of a single center. Transpl Proc 41:517–520CrossRefGoogle Scholar
  9. Boxman I, Mulder B, Vermeer J, Bouwes Bavinck J, ter Schegget J, Ponec M (2000) HPV-DNA is not detectable in outgrowing cells from explant cultures of skin lesions established at the air-liquid-interface. J Med Virol 61(3):281–288CrossRefPubMedGoogle Scholar
  10. Buell JF, Trofe J, Hanaway MJ, Lo A, Rosengard B, Rilo H, Alloway R, Beebe T, First MR, Woodle ES (2001) Transmission of donor cancer into cardiothoracic transplant recipients. Surgery 130 (4):660–666; discussion 666–668. doi: 10.1067/msy.2001.117102
  11. Buell JF, Beebe TM, Trofe J, Gross TG, Alloway RR, Hanaway MJ, Woodle ES (2004) Donor transmitted malignancies. Ann Transplant: Q Pol Transpl Soc 9(1):53–56Google Scholar
  12. Cankovic M, Linden MD, Zarbo RJ (2006) Use of microsatellite analysis in detection of tumor lineage as a cause of death in a liver transplant patient. Arch Pathol Lab Med 130(4):529–532PubMedGoogle Scholar
  13. Clarke JA (1987) HIV transmission and skin grafts. Lancet 329(8539):983 (London)Google Scholar
  14. Cox M, Brubaker SA (2012) Regulations and standards. Tissue and cell processing: an essential guide. Wiley, New York, pp 1–26CrossRefGoogle Scholar
  15. Cubie H (2013) Diseases associated with human papillomavirus infection. Virology 445(1):21–34CrossRefPubMedGoogle Scholar
  16. Directives EUTaC (2006) Commission Directive 2006/17/EC: technical requirements for the donation, procurement and testing of human tissues and cells. Off J EU L38(49):40Google Scholar
  17. Eastlund T, Warwick RM (2012) Diseases transmitted by transplantation of tissue and cell allografts. In: Warwick RM, Brubaker SA (eds) Tissue and cells clinical use an essential guide. Wiley, New York, pp 72–113CrossRefGoogle Scholar
  18. England PH Current UK population. Accessed 08 Aug 2013
  19. European Commission (2008) Eudralex: The rules governing medicinal products in the European Union, Vol 4. EU guidelines to good manufacturing practice medicinale products for human an veterinary use. Annex 20. Quality Risk Management., Accessed September 2014
  20. Fiorentino M, D’Errico A, Corti B, Casanova S, Ridolfi L, Venturoli N, Sestigiani E, Grigioni WF (2003) A multiorgan donor cancer screening protocol: the Italian Emilia-Romagna region experience. Transplantation 76(12):1695–1699. doi: 10.1097/ CrossRefPubMedGoogle Scholar
  21. Fitzpatrick TB, Johnson RA, Wolff K, Suurmond D (2001) Colour atlas and synopsis of clinical dermatology: common and serious diseases. Precancerous lesions and cutaneous carcinomas. Section 9. Mc Graw Hill, New York, pp 248–269Google Scholar
  22. Fuchs A (2007) The kinetics of skin cancer: progression of actinic keratosis to squamous cell carcinoma. Dermatol Surg 33(9):1099PubMedGoogle Scholar
  23. Gandhi MJ, Strong DM (2007) Donor derived malignancy following transplantation: a review. Cell Tissue Bank 8(4):267–286. doi: 10.1007/s10561-007-9036-1 CrossRefPubMedGoogle Scholar
  24. Glogau RG (2000) The risk of progression to invasive disease. J Am Acad Dermatol 42(1):S23CrossRefGoogle Scholar
  25. Gogia R, Binstock M, Hirose R, Boscardin WJ, Chren MM, Arron ST (2012) Fitzpatrick skin phototype is an independent predictor of squamous cell carcinoma risk after solid organ transplantation. J Am Acad Dermatol. doi: 10.1016/j.jaad.2012.09.030 PubMedCentralPubMedGoogle Scholar
  26. Harwood CA, Mesher D, McGregor JM, Mitchell L, Leedham-Green M, Raftery M, Cerio R, Leigh IM, Sasieni P, Proby CM (2013) A surveillance model for skin cancer in organ transplant recipients: a 22-year prospective study in an ethnically diverse population. Am J Transplant: Off J Am Soc Transplant Am Soc Transplant Surg 13(1):119–129. doi: 10.1111/j.1600-6143.2012.04292.x CrossRefGoogle Scholar
  27. Huang Q, Pegg DE, Kearney JN (2004) Banking of non-viable skin allografts using high concentrations of glycerol or propylene glycol. Cell Tissue Bank 5(1):3–21CrossRefPubMedGoogle Scholar
  28. Iftner A (2003) The prevalence of human papillomavirus genotypes in nonmelanoma skin cancers of nonimmunosuppressed individuals identifies high-risk genital types as possible risk factors. Cancer Res 63(21):7515PubMedGoogle Scholar
  29. Kearney JN (1996) Banking of skin grafts and biological dressings. Principles and practice of burns management. Churchill Livingstone, New York, pp 329–351Google Scholar
  30. Kearney JN (2005) Guidelines on processing and clinical use of skin allografts. Clin Dermatol 23(4):357–364. doi: 10.1016/j.clindermatol.2004.07.018 CrossRefPubMedGoogle Scholar
  31. Kim JK, Carmody IC, Cohen AJ, Loss GE (2009) Donor transmission of malignant melanoma to a liver graft recipient: case report and literature review. Clin Transplant 23(4):571–574CrossRefPubMedGoogle Scholar
  32. Kuschal C, Thoms KM, Schubert S, Schafer A, Boeckmann L, Schon MP, Emmert S (2012) Skin cancer in organ transplant recipients: effects of immunosuppressive medications on DNA repair. Exp Dermatol 21(1):2–6. doi: 10.1111/j.1600-0625.2011.01413.x CrossRefPubMedGoogle Scholar
  33. Lanssens S, Ongenae K (2011) Dermatologic lesions and risk for cancer. Acta Clin Belg 66(3):177–185PubMedGoogle Scholar
  34. MacKie RM, Reid R, Junor B (2003) Fatal melanoma transferred in a donated kidney 16 years after melanoma surgery. N Engl J Med 348(6):567–568CrossRefPubMedGoogle Scholar
  35. Michael G, Hogan PG, Falk MC, Axelsen RA, Rigby R, Hawley C, Petrie J (1998) Advanced donor-origin melanoma in a renal transplant recipient: immunotherapy, cure, and retransplantation. Transplantation 66(5):655–661CrossRefGoogle Scholar
  36. Milton CA, Barbara J, Cooper J, Rao M, Russell C, Russ G (2006) The transmission of donor-derived malignant melanoma to a renal allograft recipient. Clin Transplant 20(5):547–550. doi: 10.1111/j.1399-0012.2006.00514.x CrossRefPubMedGoogle Scholar
  37. Morris-Stiff G, Steel A, Savage P, Devlin J, Griffiths D, Portman B, Mason M, Jurewicz WA (2004) Transmission of donor melanoma to multiple organ transplant recipients. Am J Transplant: Off J Am Soc Transplant Am Soc Transpl Surg 4(3):444–446CrossRefGoogle Scholar
  38. Myron Kauffman H, McBride MA, Cherikh WS, Spain PC, Marks WH, Roza AM (2002) Transplant tumor registry: donor related malignancies. Transplantation 74(3):358–362CrossRefPubMedGoogle Scholar
  39. Nalesnik MA, Woodle ES, Dimaio JM, Vasudev B, Teperman LW, Covington S, Taranto S, Gockerman JP, Shapiro R, Sharma V, Swinnen LJ, Yoshida A, Ison MG (2011) Donor-transmitted malignancies in organ transplantation: assessment of clinical risk. Am J Transplant : Off J Am Soc Transplant Am Soc Transpl Surg 11(6):1140–1147. doi: 10.1111/j.1600-6143.2011.03565.x CrossRefGoogle Scholar
  40. Network NCI (2010) The importance of skin cancer registration—NCIN data briefing. Accessed 20 Jan 2013
  41. Nindl I, Gottschling M, Stockfleth E (2007) Human papillomaviruses and non-melanoma skin cancer: basic virology and clinical manifestations. Dis Markers 23(4):247–259PubMedCentralCrossRefPubMedGoogle Scholar
  42. NOTIFY Exploring vigilance notification for organs tac (2011) The transmission of malignancies. Testi Centro Nazionale Trapianti, BolognaGoogle Scholar
  43. Penn I (1996) Malignant melanoma in organ allograft recipients. Transplantation 61(2):274–278CrossRefPubMedGoogle Scholar
  44. Penn I (1997) Transmission of cancer from organ donors. Ann Transplant: Q Pol Transplant Soc 2(4):7–12Google Scholar
  45. Pfister H, Ter Schegget J (1997) Role of HPV in cutaneous premalignant and malignant tumors. Clin Dermatol 15(3):335–347CrossRefPubMedGoogle Scholar
  46. Pianigiani E, Ierardi F, Cuciti C, Brignali S, Oggioni M, Fimiani M (2010) Processing efficacy in relation to microbial contamination of skin allografts from 723 donors. Burns: J Int Soc Burn Inj 36(3):347–351. doi: 10.1016/j.burns.2009.04.020 CrossRefGoogle Scholar
  47. Reuschenbach M (2011) High-risk human papillomavirus in non-melanoma skin lesions from renal allograft recipients and immunocompetent patients. Br J Cancer 104(8):1334PubMedCentralCrossRefPubMedGoogle Scholar
  48. Richters CD (1996) Morphology of glycerol-preserved human cadaver skin. Burns: J Int Soc Burn Inj 22(2):113CrossRefGoogle Scholar
  49. Sens MA, Zhou X, Weiland T, Cooley AM (2009) Unexpected neoplasia in autopsies: potential implications for tissue and organ safety. Arch Pathol Lab Med 133(12):1923–1931PubMedGoogle Scholar
  50. Smolko EE, Lombardo JH (2005) Virus inactivation studies using ion beams, electron and gamma irradiation. Nucl Instrum Methods Phys Res, Sect B: Beam Interact Mater Atoms 236(1):249–253Google Scholar
  51. Stephens JK, Everson GT, Elliott CL, Kam I, Wachs M, Haney J, Bartlett ST, Franklin WA (2000) Fatal transfer of malignant melanoma from multiorgan donor to four allograft recipients. Transplantation 70(1):232–236PubMedGoogle Scholar
  52. Strauss DC, Thomas JM (2010) Transmission of donor melanoma by organ transplantation. Lancet Oncol 11(8):790–796. doi: 10.1016/s1470-2045(10)70024-3 CrossRefPubMedGoogle Scholar
  53. Sullivan AN, Bryant EA, Mark LA (2012) Malignant melanoma in transplant patients: a case report and review of the literature. Cutis: Cutan Med Pract 89(3):133–136Google Scholar
  54. Ulrich C, Schmook T, Sachse MM, Sterry W, Stockfleth E (2004) Comparative epidemiology and pathogenic factors for nonmelanoma skin cancer in organ transplant patients. Dermatol Surg: Off Publ Am Soc Dermatol Surg 30(4 Pt 2):622–627. doi: 10.1111/j.1524-4725.2004.30147.x Google Scholar
  55. Van Geyt C, Van Wijk M, Bokhorst A, Beele H (2010) Physical examination of the potential tissue donor, what do European tissue banks do? Clin Transplant 24(2):259–264. doi: 10.1111/j.1399-0012.2009.01089.x CrossRefPubMedGoogle Scholar
  56. van Wijk MJ, Hogema BM, Maas DW, Bokhorst AG (2011) A Q fever outbreak in the Netherlands: consequences for tissue banking. Transfus Med Hemother: Offizielles Organ der Deutschen Gesellschaft fur Transfusionsmedizin und Immunhamatologie 38(6):357–364. doi: 10.1159/000334599 CrossRefGoogle Scholar
  57. van Wijk M, Geyt C, Laven A, Beele H, Bokhorst A (2012) Physical examination of potential tissue donors: results of a risk management procedure to identify the critical elements of the physical examination. Cell Tissue Bank 13(4):547–563CrossRefPubMedGoogle Scholar
  58. Verbeken G, Verween G, De Vos D, Pascual B, De Corte P, Richters C, De Coninck A, Roseeuw D, Ectors N, Rose T, Jennes S, Pirnay JP (2012) Glycerol treatment as recovery procedure for cryopreserved human skin allografts positive for bacteria and fungi. Cell Tissue Bank 13(1):1–7. doi: 10.1007/s10561-011-9244-6 PubMedCentralCrossRefPubMedGoogle Scholar
  59. Zucchini N, Fiorentino M, D’Errico Grigioni A, Rizzato L, Venettoni S, Nanni Costa A, Grigioni WF (2008) The Italian multiorgan donor cancer screening protocol: 2002-2005 experience. Transplantation 85(8 Suppl):S57–S60. doi: 10.1097/TP.0b013e31816c2d42 CrossRefPubMedGoogle Scholar
  60. Zwald FO (2010) Melanoma in solid organ transplant recipients. Am J Transplant 10(5):1297CrossRefPubMedGoogle Scholar
  61. Zwald FO, Brown M (2011) 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 (2):253–261; quiz 262. doi: 10.1016/j.jaad.2010.11.062

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Sarah Bosma
    • 1
    Email author
  • Marja J. Van Wijk
    • 2
  • Cornelia D. Richters
    • 3
  • Hilde Beele
    • 1
    • 4
  1. 1.Department of DermatologyGhent University HospitalGhentBelgium
  2. 2.BISLIFE FoundationLeidenThe Netherlands
  3. 3.Euro Tissue Bank, Division Euro Skin BankBeverwijkThe Netherlands
  4. 4.Tissue Bank, Ghent University HospitalGhentBelgium

Personalised recommendations