Skip to main content

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

Abstract

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.

This is a preview of subscription content, access via your institution.

References

  • Akgül B, Akgül J, Cooke A (2006) HPV-associated skin disease. J Pathol 208(2):165–175

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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):207–211

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 14:561–570

    Article  PubMed  Google Scholar 

  • 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):2087

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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):70–79

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Bonatti H, Brandacher G, Margreiter R, Schneeberger S (2009) Infectious complications in three double hand transplant recipients: experience of a single center. Transpl Proc 41:517–520

    CAS  Article  Google Scholar 

  • 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):281–288

    CAS  Article  PubMed  Google Scholar 

  • 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

  • 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):53–56

    Google Scholar 

  • 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):529–532

    PubMed  Google Scholar 

  • Clarke JA (1987) HIV transmission and skin grafts. Lancet 329(8539):983 (London)

    Google Scholar 

  • Cox M, Brubaker SA (2012) Regulations and standards. Tissue and cell processing: an essential guide. Wiley, New York, pp 1–26

    Chapter  Google Scholar 

  • Cubie H (2013) Diseases associated with human papillomavirus infection. Virology 445(1):21–34

    CAS  Article  PubMed  Google Scholar 

  • 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):40

    Google Scholar 

  • 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 72–113

    Chapter  Google Scholar 

  • England PH Current UK population. http://www.statistics.gov.uk/hub/index.html. Accessed 08 Aug 2013

  • 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. http://ec.europa.eu/health/files/eudralex/vo-4/pdfs-en/2008_02_12gmp_annex20_en.pdf, Accessed September 2014

  • 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:10.1097/01.tp.0000092306.29395.96

    Article  PubMed  Google Scholar 

  • 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 248–269

    Google Scholar 

  • Fuchs A (2007) The kinetics of skin cancer: progression of actinic keratosis to squamous cell carcinoma. Dermatol Surg 33(9):1099

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Glogau RG (2000) The risk of progression to invasive disease. J Am Acad Dermatol 42(1):S23

    Article  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • 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):3–21

    CAS  Article  PubMed  Google Scholar 

  • 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):7515

    CAS  PubMed  Google Scholar 

  • Kearney JN (1996) Banking of skin grafts and biological dressings. Principles and practice of burns management. Churchill Livingstone, New York, pp 329–351

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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):571–574

    Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • Lanssens S, Ongenae K (2011) Dermatologic lesions and risk for cancer. Acta Clin Belg 66(3):177–185

    CAS  PubMed  Google Scholar 

  • 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):567–568

    Article  PubMed  Google Scholar 

  • 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):655–661

    Article  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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):444–446

    CAS  Article  Google Scholar 

  • Myron Kauffman H, McBride MA, Cherikh WS, Spain PC, Marks WH, Roza AM (2002) Transplant tumor registry: donor related malignancies. Transplantation 74(3):358–362

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Network NCI (2010) The importance of skin cancer registration—NCIN data briefing. http://www.ncin.org.uk/publications/data_briefings/skin_cancer_registration.aspx. Accessed 20 Jan 2013

  • Nindl I, Gottschling M, Stockfleth E (2007) Human papillomaviruses and non-melanoma skin cancer: basic virology and clinical manifestations. Dis Markers 23(4):247–259

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • NOTIFY Exploring vigilance notification for organs tac (2011) The transmission of malignancies. Testi Centro Nazionale Trapianti, Bologna

    Google Scholar 

  • Penn I (1996) Malignant melanoma in organ allograft recipients. Transplantation 61(2):274–278

    CAS  Article  PubMed  Google Scholar 

  • Penn I (1997) Transmission of cancer from organ donors. Ann Transplant: Q Pol Transplant Soc 2(4):7–12

    CAS  Google Scholar 

  • Pfister H, Ter Schegget J (1997) Role of HPV in cutaneous premalignant and malignant tumors. Clin Dermatol 15(3):335–347

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  Google Scholar 

  • Reuschenbach M (2011) High-risk human papillomavirus in non-melanoma skin lesions from renal allograft recipients and immunocompetent patients. Br J Cancer 104(8):1334

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Richters CD (1996) Morphology of glycerol-preserved human cadaver skin. Burns: J Int Soc Burn Inj 22(2):113

    CAS  Article  Google Scholar 

  • 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):1923–1931

    PubMed  Google Scholar 

  • 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):249–253

  • 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):232–236

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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):133–136

    Google Scholar 

  • UK Cr (2010). http://www.cancerresearchuk.org/cancer-info/cancerstats/types/skin/incidence/uk-skin-cancer-incidence-statistics. Accessed 20 Jan 2013

  • 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 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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):547–563

    Article  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Zwald FO (2010) Melanoma in solid organ transplant recipients. Am J Transplant 10(5):1297

    CAS  Article  PubMed  Google Scholar 

  • 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

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sarah Bosma.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bosma, S., Van Wijk, M.J., Richters, C.D. et al. The risk of transmitting cutaneous malignancy through skin transplantation: a literature-based risk assessment. Cell Tissue Bank 16, 503–512 (2015). https://doi.org/10.1007/s10561-015-9497-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10561-015-9497-6

Keywords

  • Tissue transplantation
  • Cutaneous malignancies
  • Transmission
  • Risk assessment
  • Guidelines