Cutaneous oncology in organ transplant recipients: Meeting the challenge of squamous cell carcinoma

Journal of Investigative Dermatology

Volumn 123, Issue 5, 2004, Pages 809-816

  Carucci, John A ^a,b,c  

^a Mohs Microgr and Dermatologic Surg   (United States)

^b Department of Dermatology ^*  (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPALENE; ALPHA INTERFERON; AZATHIOPRINE; CISPLATIN; CORTICOSTEROID; CYCLOSPORIN; ETRETIN; FLUOROURACIL; IMIQUIMOD; IMMUNOSUPPRESSIVE AGENT; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; OKT 3; RAPAMYCIN; RETINOIC ACID; TACROLIMUS; TIOGUANINE;

CANCER RISK; CHEMOSURGERY; CLINICAL TRIAL; DISEASE SEVERITY; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; DRY EYE; ENVIRONMENTAL FACTOR; GENE EXPRESSION; GRAFT REJECTION; HAIR LOSS; HEALTH CARE; HEART TRANSPLANTATION; HEREDITY; HUMAN; HYPERCHOLESTEROLEMIA; HYPERTRIGLYCERIDEMIA; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY TRANSPLANTATION; LIVER TRANSPLANTATION; LONG TERM CARE; LYMPH NODE DISSECTION; METASTASIS; MOLECULAR BIOLOGY; ORGAN TRANSPLANTATION; PRIORITY JOURNAL; REVIEW; SKIN CANCER; SKIN CARCINOGENESIS; SQUAMOUS CELL CARCINOMA; XEROSTOMIA;

EID: 6344275667     PISSN: 0022202X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1523-1747.2004.23440.x     Document Type: Review

References (89)

1. Geller AC, Annas GD. Epidemiology of melanoma and nonmelanoma skin cancer. Semin Oncol Nurs. Feb 2003;19(1):2-11.
2. Rowe DE, Carroll RJ, Day CL, Jr. Prognostic factors for local recurrence, metastasis, and survival rates in squamous cell carcinoma of the skin, ear, and lip. Implications for treatment modality selection. J Am Acad Dermatol. Jun 1992;26(6): 976-990.
3. Ulrich C, Schmook T, Sachse MM, Sterry W, Stockfleth E. Comparative epidemiology and pathogenic factors for nonmelanoma skin cancer in organ transplant patients. Dermatol Surg. Apr 2004;30(4 Pt 2):622-627.
4. Berg D, Otley CC. Skin cancer in organ transplant recipients: Epidemiology, pathogenesis, and management. J Am Acad Dermatol. Jul 2002;47(1):1-17; quiz 18-20.
5. Ponticelli C, Tarantino A, Vegeto A. Renal transplantation, past, present and future. J Nephrol. Jul-Aug 1999;12 Suppl 2:S105-110.
6. Ponticelli C, Villa M, Cesana B, Montagnino G, Tarantino A. Risk factors for late kidney allograft failure. Kidney Int. Nov 2002;62(5):1848-1854.
7. Seron D, Arias M, Campistol JM, Morales JM. Late renal allograft failure between 1990 and 1998 in Spain: A changing scenario. Transplantation. Dec 15 2003;76(11):1588-1594.
8. Morgan JA, John R, Weinberg AD, Colletti NJ, Mancini DM, Edwards NM. Heart transplantation in diabetic recipients: A decade review of 161 patients at Columbia Presbyterian. J Thorac Cardiovasc Surg. May 2004;127(5):1486-1492.
9. Otley CC, Pittelkow MR. Skin cancer in liver transplant recipients. Liver Transpl. May 2000;6(3):253-262.
10. Espana A, Redondo P, Fernandez AL, et al. Skin cancer in heart transplant recipients. J Am Acad Dermatol. Mar 1995;32(3):458-465.
11. Euvrard S, Kanitakis J, Poutell-Noble C, Claudy A, Touraine JL. Skin cancers in organ transplant recipients. Ann Transplant. 1997;2(4):28-32.
12. Levy M, Backman L, Husberg B, et al. De novo malignancy following liver transplantation: A single-center study. Transplant Proc. Feb 1993;25(1 Pt 2):1397-1399.
13. Lampros TD, Cobanoglu A, Parker F, Ratkovec R, Norman DJ, Hershberger R. Squamous and basal cell carcinoma in heart transplant recipients. J Heart Lung Transplant. Jun 1998;17(6):586-591.
14. Veness MJ, Quinn DI, Ong CS, et al. Aggressive cutaneous malignancies following cardiothoracic transplantation: The Australian experience. Cancer. Apr 15 1999;85(8):1758-1764.
15. Ong CS, Keogh AM, Kossard S, Macdonald PS, Spratt PM. Skin cancer in Australian heart transplant recipients. J Am Acad Dermatol. Jan 1999;40(1):27-34.
16. 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. Feb 1999;40(2 Pt 1):177-186.
17. Naldi L, Fortina AB, Lovati S, et al. Risk of nonmelanoma skin cancer in Italian organ transplant recipients. A registry-based study. Transplantation. Nov 27 2000;70(10):1479-1484.
18. Lindelof B, Sigurgeirsson B, Gabel H, Stern RS. Incidence of skin cancer in 5356 patients following organ transplantation. Br J Dermatol. Sep 2000;143(3):513-519.
19. Frezza EE, Fung JJ, van Thiel DH. Non-lymphoid cancer after liver transplantation. Hepatogastroenterology. Jul-Aug 1997;44(16):1172-1181.
20. Brash DE, Ziegler A, Jonason AS, Simon JA, Kunala S, Leffell DJ. Sunlight and sunburn in human skin cancer: p53, apoptosis, and tumor promotion. J Investig Dermatol Symp Proc. Apr 1996;1(2):136-142.
21. Reiss M, Brash DE, Munoz-Antonia T, et al. Status of the p53 tumor suppressor gene in human squamous carcinoma cell lines. Oncol Res. 1992;4(8-9):349-357.
22. Brash DE, Ponten J. Skin precancer. Cancer Surv. 1998;32:69-113.
23. Green CL, Khavari PA. Targets for molecular therapy of skin cancer. Semin Cancer Biol. Feb 2004;14(1):63-69.
24. Mercurio AM. Invasive skin carcinoma - Ras and alpha6beta4 integrin lead the way. Cancer Cell. Mar 2003;3(3):201-202.
25. Budunova IV, Perez P, Vaden VR, Spiegelman VS, Slaga TJ, Jorcano JL. Increased expression of p50-NF-kappaB and constitutive activation of NF-kappaB transcription factors during mouse skin carcinogenesis. Oncogene. Dec 9 1999;18(52):7423-7431.
26. Dajee M, Lazarov M, Zhang JY, et al. NF-kappaB blockade and oncogenic Ras trigger invasive human epidermal neoplasia. Nature. Feb 6 2003;421(6923):639- 643.
27. Kubo Y, Murao K, Matsumoto K, Arase S. Molecular carcinogenesis of squamous cell carcinomas of the skin. J Med Invest. Aug 2002;49(3-4):111-117.
28. Sok JC, Kuriakose MA, Mahajan VB, Pearlman AN, DeLacure MD, Chen FA. Tissue-specific gene expression of head and neck squamous cell carcinoma in vivo by complementary DNA microarray analysis. Arch Otolaryngol Head Neck Surg. Jul 2003;129(7):760-770.
29. Salama ME, Mahmood MN, Qureshi HS, Ma C, Zarbo RJ, Ormsby AH. p16INK4a expression in actinic keratosis and Bowen's disease. Br J Dermatol. Nov 2003;149(5):1006-1012.
30. Dazard JE, Gal H, Amariglio N, Rechavi G, Domany E, Givol D. Genome-wide comparison of human keratinocyte and squamous cell carcinoma responses to UVB irradiation: Implications for skin and epithelial cancer. Oncogene. May 15 2003;22(19):2993-3006.
31. Gariboldi M, Peissel B, Fabbri A, et al. SCCA2-like serpins mediate genetic predisposition to skin tumors. Cancer Res. Apr 15 2003;63(8):1871-1875.
32. Grossman D, Leffell DJ. The molecular basis of nonmelanoma skin cancer: New understanding. Arch Dermatol. Oct 1997;133(10):1263-1270.
33. Viac J, Chardonnet Y, Chignol MC, Schmitt D. Papilloma viruses, warts, carcinoma and Langerhans cells. In Vivo. May-Jun 1993;7(3):207-212.
34. Bosch FX, Munoz N. The viral etiology of cervical cancer. Virus Res. Nov 2002;89(2):183-190.
35. Orth G, Favre M, Majewski S, Jablonska S. Epidermodysplasia verruciformis defines a subset of cutaneous human papillomaviruses. J Virol. May 2001;75(10):4952-4953.
36. Alam M, Caldwell JB, Eliezri YD. Human papillomavirus-associated digital squamous cell carcinoma: Literature review and report of 21 new cases. J Am Acad Dermatol. Mar 2003;48(3):385-393.
37. Jackson S, Storey A. E6 proteins from diverse cutaneous HPV types inhibit apoptosis in response to UV damage. Oncogene. Jan 27 2000;19(4):592-598.
38. Bouwes Bavinck JN, Feltkarmp M, Struijk L, ter Scheggett J. Human papillomavirus infection and skin cancer risk in organ transplant recipients. J Investig Dermatol Symp Proc. Dec 2001;6(3):207-211.
39. Stockfleth E, Nindl I, Sterry W, Ulrich C, Schmook T, Meyer T. Human papillomaviruses in transplant-associated skin cancers. Dermatol Surg. Apr 2004;30(4 Pt 2):604-609.
40. Euvrard S, Chardonnet Y, Pouteil-Noble C, et al. Association of skin malignancies with various and multiple carcinogenic and noncarcinogenic human papillomaviruses in renal transplant recipients. Cancer. Oct 1 1993;72(7):2198-2206.
41. Stockfleth E, Ulrich C, Meyer T, Christophers E. Epithelial malignancies in organ transplant patients: Clinical presentation and new methods of treatment. Recent Results Cancer Res. 2002;160:251-258.
42. Penn I. De novo tumors in pediatric organ transplant recipients. Transplant Proc. Feb 1994;26(1):1-2.
43. Penn I. Occurrence of cancers in immunosuppressed organ transplant recipients. Clin Transpl. 1994:99-109.
44. Penn I. Posttransplantation de novo tumors in liver allograft recipients. Liver Transpl Surg. Jan 1996;2(1):52-59.
45. Hong JC, Kahan BD. Immunosuppressive agents in organ transplantation: past, present, and future. Semin Nephrol. Mar 2000;20(2):108-125.
46. Chan GL, Erdmann GR, Gruber SA, Matas AJ, Canafax DM. Azathioprine metabolism: Pharmacokinetics of 6-mercaptopurine, 6-thiouric acid and 6-thioguanine nucleotides in renal transplant patients. J Clin Pharmacol. Apr 1990;30(4): 358-363.
47. Harvey JJ, East J, Katz FE. Azathioprine-induced lymphocytic neoplasms of NZB mice lack ecotropic murine leukaemia virus. Int J Cancer. Feb 1979;23(2):217-223.
48. Flechner SM. Cyclosporine: A new and promising immunosuppressive agent. Urol Clin North Am. May 1983;10(2): 263-275.
49. Landewe RB, van den Borne BE, Breedveld FC, Dijkmans BA. Does cyclosporin A cause cancer? Nat Med. Jul 1999;5(7):714.
50. Hojo M, Morimoto T, Maluccio M, et al. Cyclosporine induces cancer progression by a cell-autonomous mechanism. Nature. Feb 11 1999;397(6719):530- 534.
51. Nelson EW, Eichwald EJ, Shelby J. Increased ultraviolet radiation-induced skin cancers in cyclosporine-treated mice. Transplant Proc. Feb 1987;19(1 Pt 1):526-527.
52. Penn I, First MR. Development and incidence of cancer following cyclosporine therapy. Transplant Proc. Apr 1986;18(2 Suppl 1):210-215.
53. Lerut JP, Ciccarelli O, Mauel E, et al. Adult liver transplantation and steroid-azathioprine withdrawal in cyclosporine (Sandimmun)-based immunosuppression - 5 year results of a prospective study. Transpl Int. Dec 2001;14(6):420-428.
54. Karagas MR, Cushing GL, Jr., Greenberg ER, Mott LA, Spencer SK, Nierenberg DW. Non-melanoma skin cancers and glucocorticoid therapy. Br J Cancer. Sep 1 2001; 85(5):683-686.
55. Kitchin JE, Pomeranz MK, Pak G, Washenik K, Shupack JL. Rediscovering mycophenolic acid: A review of its mechanism, side effects, and potential uses. J Am Acad Dermatol. Sep 1997;37(3 Pt 1):445-449.
56. Triemer HL, Pearson TC, Odom KL, Larsen CP. Analysis of a single-center experience with mycophenolate mofetil based immunosuppression in renal transplantation. Clin Transplant. Aug 2000;14(4 Pt 2):413-420.
57. Batiuk TD, Barry JM, Bennett WM, Meyer MM, Tolzman D, Norman DJ. Incidence and type of cancer following the use of OKT3: A single center experience with 557 organ transplants. Transplant Proc. Feb 1993;25(1 Pt 2):1391.
58. Stempfle HU, Mudra H, Angermann CE, Weiss M, Reichart B, Theisen K. Rapid growth of cutaneous neuroendocrine (Merkel cell) carcinoma during treatment of refractory cardiac allograft rejection with OKT3 monoclonal antibody. J Heart Lung Transplant. May-Jun 1993;12(3):501-503.
59. Oechslin E, Kiowski W, Schneider J, Follath F, Turina M, Gallino A. Pretransplant malignancy in candidates and posttransplant malignancy in recipients of cardiac transplantation. Ann Oncol. Dec 1996;7(10):1059-1063.
60. De Tran QH, Guay E, Chartier S, Tousignant J. Tacrolimus in dermatology. J Cutan Med Surg. Jul-Aug 2001;5(4):329-335.
61. Jain AB, Yee LD, Nalesnik MA, et al. Comparative incidence of de novo nonlymphoid malignancies after liver transplantation under tacrolimus using surveillance epidemiologic end result data. Transplantation. Nov 15 1998;66(9):1193-1200.
62. Jiang H, Yamamoto S, Nishikawa K, Kato R. Anti-tumor-promoting action of FK506, a potent immunosuppressive agent. Carcinogenesis. Jan 1993;14(1):67-71.
63. Marsland AM, Griffiths CE. The macrolide immunosuppressants in dermatology: mechanisms of action. Eur J Dermatol. Nov-Dec 2002;12(6):618-622.
64. Euvrard S, Ulrich C, Lefrancois N. Immunosuppressants and skin cancer in transplant patients: Focus on rapamycin. Dermatol Surg. Apr 2004;30(4 Pt 2):628-633.
65. van Zuuren EJ, Posma AN, Scholtens RE, Vermeer BJ, van der Woude FJ, Bouwes Bavinck JN. Resurfacing the back of the hand as treatment and prevention of multiple skin cancers in kidney transplant recipients. J Am Acad Dermatol. Nov 1994;31(5 Pt 1):760-764.
66. Martinez JC, Otley CC, Stasko T, et al. Defining the clinical course of metastatic skin cancer in organ transplant recipients: A multicenter collaborative study. Arch Dermatol. Mar 2003;139(3):301-306.
67. Carucci JA, Martinez JC, Zeitouni NC, et al. In-transit metastasis from primary cutaneous squamous cell carcinoma in organ transplant recipients and nonimmunosuppressed patients: Clinical characteristics, management, and outcome in a series of 21 patients. Dermatol Surg. Apr 2004;30(4 Pt 2):651-655.
68. Euvrard S, Kanitakis J, Pouteil-Noble C, et al. Aggressive squamous cell carcinomas in organ transplant recipients. Transplant Proc. Apr 1995;27(2):1767-1768.
69. Preciado DA, Matas A, Adams GL. Squamous cell carcinoma of the head and neck in solid organ transplant recipients. Head Neck. Apr 2002;24(4):319-325.
70. Stasko T, Brown MD, Carucci JA, et al. Guidelines for the management of squamous cell carcinoma in organ transplant recipients. Dermatol Surg. Apr 2004;30(4 Pt 2):642-650.
71. Persaud AN, Shamuelova E, Sherer D, et al. Clinical effect of imiquimod 5% cream in the treatment of actinic keratosis. J Am Acad Dermatol. Oct 2002;47(4):553-556.
72. Boussen H, Zwik J, Mili-Boussen I, et al. Therapeutic results of 5-fluorouracil in multiple and unresectable facial carcinoma secondary to xeroderma pigmentosum. Therapie. Nov-Dec 2001;56(6):751-754.
73. Lebwohl M, Dinehart S, Whiting D, et al. Imiquimod 5% cream for the treatment of actinic keratosis: Results from two phase III, randomized, double-blind, parallel group, vehicle-controlled trials. J Am Acad Dermatol. May 2004;50(5): 714-721.
74. Harrison LI, Skinner SL, Marbury TC, et al. Pharmacokinetics and safety of imiquimod 5% cream in the treatment of actinic keratoses of the face, scalp, or hands and arms. Arch Dermatol Res. Apr 9 2004.
75. Stockfleth E, Meyer T, Benninghoff B, et al. A randomized, double-blind, vehicle-controlled study to assess 5% imiquimod cream for the treatment of multiple actinic keratoses. Arch Dermatol. Nov 2002;138(11):1498-1502.
76. Smith KJ, Germain M, Skelton H. Squamous cell carcinoma in situ (Bowen's disease) in renal transplant patients treated with 5% imiquimod and 5% 5-fluorouracil therapy. Dermatol Surg. Jun 2001;27(6):561-564.
77. Vandeghinste N, De Bersaques J, Geerts ML, Kint A. Acitretin as cancer chemoprophylaxis in a renal transplant recipient. Dermatology. 1992;185(4):307-308.
78. McNamara IR, Muir J, Galbraith AJ. Acitretin for prophylaxis of cutaneous malignancies after cardiac transplantation. J Heart Lung Transplant. Nov 2002;21(11):1201-1205.
79. Bavinck JN, Tieben LM, Van der Woude FJ, et al. Prevention of skin cancer and reduction of keratotic skin lesions during acitretin therapy in renal transplant recipients: A double-blind, placebo-controlled study. J Clin Oncol. Aug 1995;13(8): 1933-1938.
80. Yuan ZF, Davis A, Macdonald K, Bailey RR. Use of acitretin for the skin complications in renal transplant recipients. N Z Med J. Jun 28 1995;108(1002):255-256.
81. Tan SR, Tope WD. Effect of acitretin on wound healing in organ transplant recipients. Dermatol Surg. Apr 2004;30(4 Pt 2):667-673.
82. Euvrard S, Verschoore M, Touraine JL, et al. Topical retinoids for warts and keratoses in transplant recipients. Lancet. Jul 4 1992;340(8810):48-49.
83. Otley CC, Coldiron BM, Stasko T, Goldman GD. Decreased skin cancer after cessation of therapy with transplant-associated immunosuppressants. Arch Dermatol. Apr 2001;137(4): 459-463.
84. Moloney FJ, Kelly PO, Kay EW, Conlon P, Murphy GM. Maintenance versus reduction of immunosuppression in renal transplant recipients with aggressive squamous cell carcinoma. Dermatol Surg. Apr 2004;30(4 Pt 2):674-678.
85. Reschly MJ, Messina JL, Zaulyanov LL, Cruse W, Fenske NA. Utility of sentinel lymphadenectomy in the management of patients with high-risk cutaneous squamous cell carcinoma. Dermatol Surg. Feb 2003;29(2):135-140.
86. Altinyollar H, Berberoglu U, Celen O. Lymphatic mapping and sentinel lymph node biopsy in squamous cell carcinoma of the lower lip. Eur J Surg Oncol. Feb 2002;28(1):72-74.
87. Martinez JC, Otley CC, Okuno SH, Foote RL, Kasperbauer JL. Chemotherapy in the management of advanced cutaneous squamous cell carcinoma in organ transplant recipients: Theoretical and practical considerations. Dermatol Surg. Apr 2004;30(4 Pt 2):679-686.
88. Shin DM, Glisson BS, Khuri FR, et al. Phase II and biologic study of interferon alfa, retinoic acid, and cisplatin in advanced squamous skin cancer. J Clin Oncol. Jan 15 2002;20(2): 364-370.
89. Christenson LJ, Geusau A, Ferrandiz C, et al. Specialty clinics for the dermatologic care of solid-organ transplant recipients. Dermatol Surg. Apr 2004;30(4 Pt 2):598-603.