Mucosal melanoma: epidemiology, biology, management and the role of immunotherapy

References

• McLaughlin CC, Wu XC, Jemal A, et al. Incidence of noncutaneous melanomas in the U.S. Cancer. 2005;103(5):1000–1007.
   Google Scholar
• Chang AE, Karnell LH, Menck HR. The National Cancer Data Base report on cutaneous and noncutaneous melanoma: a summary of 84,836 cases from the past decade. The American College of Surgeons Commission on Cancer and the American Cancer Society. Cancer. 1998;83(8):1664–1678.
   Google Scholar
• Warszawik-Hendzel O, Slowinska M, Olszewska M, et al. Melanoma of the oral cavity: pathogenesis, dermoscopy, clinical features, staging and management. J Dermatol Case Rep. 2014;8(3):60–66.
   Google Scholar
• Yu GP, Hu DN, McCormick SA. Latitude and incidence of ocular melanoma. Photochem Photobiol. 2006;82(6):1621–1626.
   Google Scholar
• Griewank KG, Murali R, Schilling B, et al. TERT promoter mutations in ocular melanoma distinguish between conjunctival and uveal tumours. Br J Cancer. 2013;109(2):497–501.
   Google Scholar
• Rivolta C, Royer-Bertrand B, Rimoldi D, et al. UV light signature in conjunctival melanoma; not only skin should be protected from solar radiation. J Hum Genet. 2016;61(4):361–362.
   Google Scholar
• Lazarev S, Gupta V, Hu K, et al. Mucosal melanoma of the head and neck: a systematic review of the literature. Int J Radiat Oncol Biol Phys. 2014;90(5):1108–1118.
   Google Scholar
• Lourenco SV, A MS, Sotto MN, et al. Primary oral mucosal melanoma: a series of 35 new cases from South America. Am J Dermatopathol. 2009;31(4):323–330.
   Google Scholar
• Chi Z, Li S, Sheng X, et al. Clinical presentation, histology, and prognoses of malignant melanoma in ethnic Chinese: a study of 522 consecutive cases. BMC Cancer. 2011;11:85.
   Google Scholar
• Yu GP, Hu DN, McCormick S, et al. Conjunctival melanoma: is it increasing in the United States? Am J Ophthalmol. 2003;135(6):800–806.
   Google Scholar
• Jangard M, Hansson J, Ragnarsson-Olding B. Primary sinonasal malignant melanoma: a nationwide study of the Swedish population, 1960–2000. Rhinology. 2013;51(1):22–30.
   Google Scholar
• Carvajal RD, Spencer SA, Lydiatt W. Mucosal melanoma: a clinically and biologically unique disease entity. J Natl Compr Cancer Network. 2012;10(3):345–356.
   Google Scholar
• Kuk D, Shoushtari AN, Barker CA, et al. Prognosis of mucosal, uveal, acral, nonacral cutaneous, and unknown primary melanoma from the time of first metastasis. Oncologist. 2016;21(7):848–854.
   Google Scholar
• Sharma P, Wagner K, Wolchok JD, et al. Novel cancer immunotherapy agents with survival benefit: recent successes and next steps. Nat Rev Cancer. 2011;11(11):805–812.
   Google Scholar
• Hodi FS, O’Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8):711–723.
   Google Scholar
• Robert C, Thomas L, Bondarenko I, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med. 2011;364(26):2517–2526.
   Google Scholar
• Weber JS, D’Angelo SP, Minor D, et al. Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate 037): a randomised, controlled, open-label, phase 3 trial. Lancet Oncol. 2015;16(4):375–384.
   Google Scholar
• Ribas A, Puzanov I, Dummer R, et al. Pembrolizumab versus investigator-choice chemotherapy for ipilimumab-refractory melanoma (KEYNOTE-002): a randomised, controlled, phase 2 trial. Lancet Oncol. 2015;16(8):908–918.
   Google Scholar
• Robert C, Long GV, Brady B, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 2015;372(4):320–330.
   Google Scholar
• Robert C, Schachter J, Long GV, et al. Pembrolizumab versus ipilimumab in advanced melanoma. N Engl J Med. 2015;372(26):2521–2532.
   Google Scholar
• Larkin J, Chiarion-Sileni V, Gonzalez R, et al. Overall survival results from a phase III trial of nivolumab combined with ipilimumab in treatment-naive patients with advanced melanoma (CheckMate-067). In: Proceedings of the 107th Annual Meeting of the American Association for Cancer Research; 2017 Apr 1-5; Washington, DC. Philadelphia (PA): AACR; 2017. Abstract CT075.
   Google Scholar
• Novak N, Haberstok J, Bieber T, et al. The immune privilege of the oral mucosa. Trends Mol Med. 2008;14(5):191–198.
   Google Scholar
• Janeway CA Jr, Travers P, Walport M, et al. The mucosal immune system. The immune system in health and disease. 5th ed. New York: Garland Science; 2001.
   Google Scholar
• Furney SJ, Turajlic S, Stamp G, et al. Genome sequencing of mucosal melanomas reveals that they are driven by distinct mechanisms from cutaneous melanoma. J Pathol. 2013;230(3):261–269.
   Google Scholar
• Curtin JA, Fridlyand J, Kageshita T, et al. Distinct sets of genetic alterations in melanoma. N Engl J Med. 2005;353(20):2135–2147.
   Google Scholar
• Cancer Genome Atlas N. Genomic classification of cutaneous melanoma. Cell. 2015;161(7):1681–1696.
   Google Scholar
• Griewank KG, Westekemper H, Murali R, et al. Conjunctival melanomas harbor BRAF and NRAS mutations and copy number changes similar to cutaneous and mucosal melanomas. Clin Cancer Res. 2013;19(12):3143–3152.
   Google Scholar
• Sheng X, Kong Y, Li Y, et al. GNAQ and GNA11 mutations occur in 9.5% of mucosal melanoma and are associated with poor prognosis. Eur J Cancer. 2016;65:156–163.
   Google Scholar
• Cosgarea I, Ugurel S, Sucker A, et al. Targeted next generation sequencing of mucosal melanomas identifies frequent NF1 and RAS mutations. Oncotarget. 2017;8(25):40683–40692.
   Google Scholar
• Beadling C, Jacobson-Dunlop E, Hodi FS, et al. KIT gene mutations and copy number in melanoma subtypes. Clin Cancer Res. 2008;14(21):6821–6828.
   Google Scholar
• Curtin JA, Busam K, Pinkel D, et al. Somatic activation of KIT in distinct subtypes of melanoma. J Clin Oncol. 2006;24(26):4340–4346.
   Google Scholar
• Schoenewolf NL, Bull C, Belloni B, et al. Sinonasal, genital and acrolentiginous melanomas show distinct characteristics of KIT expression and mutations. Eur J Cancer. 2012;48(12):1842–1852.
   Google Scholar
• Yang HM, Hsiao SJ, Schaeffer DF, et al. Identification of recurrent mutational events in anorectal melanoma. Modern Pathol. 2017;30(2):286–296.
   Google Scholar
• Gavriel H, McArthur G, Sizeland A, et al. Review: mucosal melanoma of the head and neck. Melanoma Res. 2011;21(4):257–266.
   Google Scholar
• Mikkelsen LH, Larsen AC, von Buchwald C, et al. Mucosal malignant melanoma - a clinical, oncological, pathological and genetic survey. APMIS. 2016;124(6):475–486.
   Google Scholar
• Lian B, Si L, Cui C, et al. Phase II randomized trial comparing high-dose IFN-alpha2b with temozolomide plus cisplatin as systemic adjuvant therapy for resected mucosal melanoma. Clin Cancer Res. 2013;19(16):4488–4498.
   Google Scholar
• Shoushtari AN, Bluth MJ, Goldman DA, et al. Clinical features and response to systemic therapy in a historical cohort of advanced or unresectable mucosal melanoma. Melanoma Res. 2017;27(1):57–64.
   Google Scholar
• Yi JH, Yi SY, Lee HR, et al. Dacarbazine-based chemotherapy as first-line treatment in noncutaneous metastatic melanoma: multicenter, retrospective analysis in Asia. Melanoma Res. 2011;21(3):223–227.
   Google Scholar
• Carvajal RD, Antonescu CR, Wolchok JD, et al. KIT as a therapeutic target in metastatic melanoma. JAMA J Am Med Assoc. 2011;305(22):2327–2334.
   Google Scholar
• Guo J, Si L, Kong Y, et al. Phase II, open-label, single-arm trial of imatinib mesylate in patients with metastatic melanoma harboring c-Kit mutation or amplification. J Clin Oncol. 2011;29(21):2904–2909.
   Google Scholar
• Hodi FS, Corless CL, Giobbie-Hurder A, et al. Imatinib for melanomas harboring mutationally activated or amplified KIT arising on mucosal, acral, and chronically sun-damaged skin. J Clin Oncol. 2013;31(26):3182–3190.
   Google Scholar
• Lee SJ, Kim TM, Kim YJ, et al. Phase II trial of nilotinib in patients with metastatic malignant melanoma harboring KIT gene aberration: a multicenter trial of Korean Cancer Study Group (UN10-06). Oncologist. 2015;20(11):1312–1319.
   Google Scholar
• Carvajal RD, Lawrence DP, Weber JS, et al. Phase II study of nilotinib in melanoma harboring KIT alterations following progression to prior KIT inhibition. Clin Cancer Res. 2015;21(10):2289–2296.
   Google Scholar
• Kalinsky K, Lee S, Rubin KM, et al. A phase 2 trial of dasatinib in patients with locally advanced or stage IV mucosal, acral, or vulvovaginal melanoma: A trial of the ECOG-ACRIN Cancer Research Group (E2607). Cancer. 2017;123(14):2688–2697.
   Google Scholar
• Guo J, Carvajal RD, Dummer R, et al. Efficacy and safety of nilotinib in patients with KIT-mutated metastatic or inoperable melanoma: final results from the global, single-arm, phase II TEAM trial. Ann Oncol. 2017;28(6):1380–1387.
   Google Scholar
• Peng SB, Henry JR, Kaufman MD, et al. Inhibition of RAF isoforms and active dimers by LY3009120 leads to anti-tumor activities in RAS or BRAF mutant cancers. Cancer Cell. 2015;28(3):384–398.
   Google Scholar
• Kim KB, Sanguino AM, Hodges C, et al. Biochemotherapy in patients with metastatic anorectal mucosal melanoma. Cancer. 2004;100(7):1478–1483.
   Google Scholar
• Harting MS, Kim KB. Biochemotherapy in patients with advanced vulvovaginal mucosal melanoma. Melanoma Res. 2004;14(6):517–520.
   Google Scholar
• Bartell HL, Bedikian AY, Papadopoulos NE, et al. Biochemotherapy in patients with advanced head and neck mucosal melanoma. Head Neck. 2008;30(12):1592–1598.
   Google Scholar
• Keilholz U, Punt CJ, Gore M, et al. Dacarbazine, cisplatin, and interferon-alfa-2b with or without interleukin-2 in metastatic melanoma: a randomized phase III trial (18951) of the European Organisation for Research and Treatment of Cancer Melanoma Group. J Clin Oncol. 2005;23(27):6747–6755.
   Google Scholar
• Atkins MB, Hsu J, Lee S, et al. Phase III trial comparing concurrent biochemotherapy with cisplatin, vinblastine, dacarbazine, interleukin-2, and interferon alfa-2b with cisplatin, vinblastine, and dacarbazine alone in patients with metastatic malignant melanoma (E3695): a trial coordinated by the Eastern Cooperative Oncology Group. J Clin Oncol. 2008;26(35):5748–5754.
   Google Scholar
• Flaherty LE, Othus M, Atkins MB, et al. Southwest Oncology Group S0008: a phase III trial of high-dose interferon Alfa-2b versus cisplatin, vinblastine, and dacarbazine, plus interleukin-2 and interferon in patients with high-risk melanoma–an intergroup study of cancer and leukemia Group B, Children’s Oncology Group, Eastern Cooperative Oncology Group, and Southwest Oncology Group. J Clin Oncol. 2014;32(33):3771–3778.
   Google Scholar
• Postow MA, Luke JJ, Bluth MJ, et al. Ipilimumab for patients with advanced mucosal melanoma. Oncologist. 2013;18(6):726–732.
   Google Scholar
• Del Vecchio M, Di Guardo L, Ascierto PA, et al. Efficacy and safety of ipilimumab 3mg/kg in patients with pretreated, metastatic, mucosal melanoma. Eur J Cancer. 2014;50(1):121–127.
   Google Scholar
• Zimmer L, Eigentler TK, Kiecker F, et al. Open-label, multicenter, single-arm phase II DeCOG-study of ipilimumab in pretreated patients with different subtypes of metastatic melanoma. J Transl Med. 2015;13:351.
   Google Scholar
• Del Prete V, Chaloupka K, Holzmann D, et al. Noncutaneous melanomas: a single-center analysis. Dermatology. 2016;232(1):22–29.
   Google Scholar
• Schiavone MB, Broach V, Shoushtari AN, et al. Combined immunotherapy and radiation for treatment of mucosal melanomas of the lower genital tract. Gynecol Oncol Rep. 2016;16:42–46.
   Google Scholar
• Shoushtari AN, Munhoz RR, Kuk D, et al. The efficacy of anti-PD-1 agents in acral and mucosal melanoma. Cancer. 2016;122(21):3354–3362.
   Google Scholar
• D’Angelo SP, Larkin J, Sosman JA, et al. Efficacy and safety of nivolumab alone or in combination with ipilimumab in patients with mucosal melanoma: a pooled analysis. J Clin Oncol. 2017;35(2):226–235.
   Google Scholar
• Yamazaki N, Takenouchi T, Fujimoto M, et al. Phase 1b study of pembrolizumab (MK-3475; anti-PD-1 monoclonal antibody) in Japanese patients with advanced melanoma (KEYNOTE-041). Cancer Chemother Pharmacol. 2017;79(4):651–660.
   Google Scholar
• Le DT, Durham JN, Smith KN, et al. Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science. 2017;357(6349):409–413.
   Google Scholar
• Kaunitz GJ, Cottrell TR, Lilo M, et al. Melanoma subtypes demonstrate distinct PD-L1 expression profiles. Lab Invest. 2017.
   Google Scholar
• Danilova L, Wang H, Sunshine J, et al. Association of PD-1/PD-L axis expression with cytolytic activity, mutational load, and prognosis in melanoma and other solid tumors. Proc Natl Acad Sci U S A. 2016;113(48):E7769–E7777.
   Google Scholar
• Sullivan RJ, Gonzalez R, Lewis KD, et al. Atezolizumab (A) + cobimetinib (C) + vemurafenib (V) in BRAFV600-mutant metastatic melanoma (mel): updated safety and clinical activity. J Clin Oncol. 2017;35(15_suppl):abstr 3063.
   Google Scholar
• Balachandran VP, Cavnar MJ, Zeng S, et al. Imatinib potentiates antitumor T cell responses in gastrointestinal stromal tumor through the inhibition of Ido. Nat Med. 2011;17(9):1094–1100.
   Google Scholar
• Reilley MJ, Bailey A, Subbiah V, et al. Phase I clinical trial of combination imatinib and ipilimumab in patients with advanced malignancies. J Immunother Cancer. 2017;5:35.
   Google Scholar