melanoma who had developed cutaneous vitiligo and were examined at a tertiary eye care institution.
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1 Research Original Investigation CLINICAL SCIENCES Cutaneous Vitiligo Following Management of Uveal Melanoma in 6 Patients Pukhraj Rishi, MD; Carol L. Shields, MD; Kaitlin Patrick, BS; Jerry A. Shields, MD IMPORTANCE The relationship of vitiligo to cutaneous melanoma is believed to be due to an immune response generated to melanoma antigens that cross-react with normal skin. There is little in the literature on the relationship between cutaneous vitiligo and uveal melanoma. OBJECTIVE To describe the clinical profile, treatment, and outcome in patients with uveal melanoma who subsequently developed cutaneous vitiligo. DESIGN, SETTING, AND PARTICIPANTS Retrospective case series of 6 patients with uveal melanoma who had developed cutaneous vitiligo and were examined at a tertiary eye care institution. MAIN OUTCOME AND MEASURE Development of cutaneous vitiligo. RESULTS The mean age at presentation was 62 years (range, years). No patient had a personal history of cutaneous melanoma, autoimmune disease, or cutaneous vitiligo. The mean tumor basal diameter was 12.9 mm (median, 12.7 mm; range, 7-19 mm), with a mean thickness of 9.5 mm (median, 8.4 mm; range, 3-19 mm). Treatment included plaque radiotherapy in 4 patients and enucleation in 1 patient; 1 patient refused therapy. No patient had local tumor recurrence at the 71-month mean follow-up, but of the 3 patients who developed metastases at the 52-month mean follow-up, 2 were treated with a melanoma vaccine. The mean interval from initial presentation to onset of vitiligo was 77 months (range, months). The vitiligo developed bilaterally with multiple well-defined lesions, affecting 5% to 40% of the cutaneous surface, generally in the upper body. During the 71-month mean follow-up (range, months), there was 1 death. CONCLUSIONS AND RELEVANCE Patients with uveal melanoma can develop vitiligo spontaneously or following vaccine therapy. Involvement is multiple and bilateral, predominantly affecting the upper body. JAMA Ophthalmol. 2013;131(9): doi: /jamaophthalmol Published online July 25, Author Affiliations: Ocular Oncology Service, Wills Eye Institute, Thomas Jefferson University, Philadelphia, Pennsylvania (Rishi, Shields CL, Patrick, Shields JA); On sabbatical from Shri Bhagwan Mahavir Vitreoretinal Services, Sankara Nethralya, Chennai, India (Rishi). Corresponding Author: Carol L. Shields, MD, Ocular Oncology Service, Wills Eye Institute, Thomas Jefferson University, 840 Walnut St, Ste 1440, Philadelphia, PA (carol.shields@shieldsoncology.com). Vitiligo is an acquired chronic pigmentary disorder of the skin characterized by depigmented patches, often symmetrically distributed, and with a propensity to increase in size over time. The depigmented regions correspond to a loss of melanocytes within epidermal and sometimes hair follicle melanocytes. 1 This condition affects approximately 0.5% of the population. 2 Vitiligo is generally a sporadic autoimmune disease. However, vitiligo-like depigmentation can occur due to posttraumatic, postinflammatory, postinfectious, drug-induced situations and rare causes such as hypomelanosis from piebaldism and tuberous sclerosis. 1 A rare cause of vitiligo is previously treated or spontaneously regressed cutaneous melanoma. The relationship between vitiligo and cutaneous melanoma is believed to be due to an immune response generated to melanoma antigens that cross-react with normal skin. Melanoma-related vitiligo occurs in 1% to 5% of patients with cutaneous melanoma. 2-5 There is little in the literature on the relationship between cutaneous vitiligo and uveal melanoma Herein, we describe 6 patients with uveal melanoma who developed cutaneous vitiligo. Methods Of approximately 4760 patients with uveal melanoma examined at the Ocular Oncology Service, Wills Eye Institute, Thomas Jefferson University, Philadelphia, Pennsylvania, between July 1, 2003, and September 30, 2012, 6 patients had developed cutaneous vitiligo. The institutional review board at 1174 JAMA Ophthalmology September 2013 Volume 131, Number 9 jamaophthalmology.com
2 Cutaneous Vitiligo After Uveal Melanoma Management Original Investigation Research Table 1. Patient Demographics Patient No./Age, y/ Medical Visual Acuity Tumor Dimensions, mm Primary Race/Sex History Laterality at Presentation Base Height Treatment 1/58/W/M None Right eye 20/ Plaque RT 2/65/W/F HCh Left eye NLP Enucleation 3/78/AA/M HT Left eye CF 12 7 Plaque RT 4/85/W/M None Right eye LP None 5/39/W/M None Right eye 20/ Plaque RT 6/47/W/F None Left eye 20/ Plaque RT Abbreviations: AA, African American; CF, counting fingers; F, Female; HCh, hypercholesterolemia; HT, hypertension; LP, light perception; M, male; NLP, no light perception; RT, radiotherapy; W, white. Table 2. Treatment Outcomes Patient No. Metastases Time From Date First Seen to Metastases, mo Treatment of Metastases Death Final Visual Acuity 1 None NA NA No 20/150 2 Liver, lung, thyroid, lymph nodes, and abdomen 28 Radiation, chemoembolization, Hapten-modified melanoma cell vaccine ( 7), and surgical resection 3 None NA NA No NA 4 Liver 36 No treatment taken Yes LP 5 None NA NA No NLP 6 Liver, lung, and pancreas 96 Hapten-modified melanoma cell vaccine ( 7), radiofrequency ablation, and surgical resection No Enucleated No 20/400 Abbreviations: LP, light perception; NA, not applicable; NLP, no light perception. the Wills Eye Institute approved this study. The study and data collection conformed to local laws and were compliant with the principles of the Declaration of Helsinki. Data were reviewed regarding patient demographic information such as age, race, sex, and past personal or family history of cutaneous melanoma, autoimmune disorder, or cutaneous vitiligo. A detailed systemic and ocular history was obtained from the medical records, including best-corrected visual acuity, slitlamp biomicroscopy, intraocular pressure measurement, indirect ophthalmoscopy, and transillumination findings. B-scan ultrasonography was performed in all patients to quantify tumor dimensions. Additional imaging with computed tomography or magnetic resonance imaging was done when needed. Details of the uveal melanoma were recorded regarding tumor size (base and thickness in millimeters), location, related features, and treatment. Outcomes of therapy were recorded, including melanoma control, metastasis, and death. Details on the development of cutaneous vitiligo with regard to the extent, location, time to onset, progression, and treatment were noted. Vitiligo outcomes included progression of disease and relationship to the primary uveal melanoma. Results The demographic features and clinical characteristics of the 6 patients are listed in Table 1. The mean age at presentation was 62 years (median, 62 years; range, years). Five patients were white and 1 was African American. There was no personal or family history of cutaneous melanoma, autoimmune disease, or cutaneous vitiligo. No patient received treatment before referral to our department. The most common ocular symptom was reduction of vision, with visual acuity ranging from 20/20 to no light perception. The mean tumor basal diameter was 12.9 mm (median, 12.7 mm; range, 7-19 mm), with a mean thickness of 9.5 mm (median, 8.4 mm; range, 3-19 mm). The treatment outcomes are listed in Table 2. There was no local tumor recurrence during the 71-month mean follow-up. Three patients (patients 2, 4, and 6) developed metastases. The mean interval from treatment of the melanoma to onset of metastasiswas52months(median,33months;range,28-96months). Patient 4 refused therapy because of poor general health. The vitiligo outcomes are listed in Table 3. The mean interval from presentation to onset of vitiligo was 77 months (median, 74 months; range, months). The vitiligo developed bilaterally with multiple well-defined lesions, affecting 5% to 40% of the cutaneous surface, generally on the upper body (Figure 1, patient without metastasis; Figure 2, patient with metastasis). During the total 71-month mean follow-up (median, 50 months; range, months), there was 1 death from metastatic melanoma. None of the patients sought treatment for vitiligo. Discussion Cutaneous vitiligo is a common skin disorder, recognized as patchy depigmentation and occurs in approximately 0.5% to jamaophthalmology.com JAMA Ophthalmology September 2013 Volume 131, Number
3 Research Original Investigation Cutaneous Vitiligo After Uveal Melanoma Management Table 3. Details of Cutaneous Vitiligo Following Uveal Melanoma in 6 Patients Patient No. Time to Onset of Cutaneous Vitiligo From Date First Seen, mo Vitiligo Site Body Parts Extent, % 1 62 Both arms 10 Yes 2 a 87 Face 40 Neck 20 Abdomen 10 Right forearm 30 Yes Left forearm 10 Both shins 10 Back Nasolabial folds 5 No 4 31 Both arms 10 No Neck 10 Both arms 10 Yes 6 a 109 Both forearms 5 No Progression of Vitiligo a Patients who got vaccine therapy for metastatic disease. Figure 1. Vitiligo in a Patient Treated With Plaque Radiotherapy A B C D E F A 39-year-old man (patient 5) with an amelanotic melanoma (A) 9.9 mm in thickness on ultrasonography (B) was treated with plaque radiotherapy. Seventeen years later, the right eye displayed cataract (C) and regressed melanoma (D). Cutaneous vitiligo was found on both arms (E and F), and there was no evidence of metastatic disease. 1% of the world population. 2 There is no apparent predilection for sex, race, or skin type, and nearly half of affected patients manifest vitiligo by the third decade of life. 1 The cutaneous surface of the body is endowed with complex adaptive immune mechanisms. In the past 50 years, studies on tumor immunology have revealed a link between tumor immunity and autoimmunity, 11 with an extensive overlap between normally expressed antigens and those expressed by malignant neoplasms, such as melanoma. 1 Spontaneous regression of cutaneous nevi is recognized in children and ado JAMA Ophthalmology September 2013 Volume 131, Number 9 jamaophthalmology.com
4 Cutaneous Vitiligo After Uveal Melanoma Management Original Investigation Research Figure 2. Vitiligo in a Patient Treated With Enucleation and Immunotherapy A B C D E F A 65-year-old woman (patient 2) with eyelid edema, chemosis, and total hyphema (A) of the left eye had an ill-defined large intraocular mass filling the globe on ultrasonography (B), necessitating enucleation. At the 28-month follow-up, with a prosthesis in place (C), systemic metastases were detected and immunotherapy with vaccination was provided (D). Fifty-nine months later, cutaneous vitiligo of the periocular region (E) and arms (F) was detected. lescents, probably reflecting an active and robust immunosurveillance that eliminates normal and neoplastic melanocytes, thus preventing tumor development. 12 Conversely, it also has been shown that immunodeficiency is associated with a higher incidence of melanocytic nevi. 13 Furthermore, medication-related immunosuppression in transplant recipients can cause eruption of cutaneous nevi. 14 Such nevi are reported to involute after discontinuation of immunosuppressive therapy. These observations directly support the theory of skin immunosurveillance against melanocytic proliferation. 15 An important finding to further confirm this observation is the fact that cutaneous melanoma increases 4 to 7 times in immunosuppressed populations compared with age- and sex-matched controls. 16 Melanoma cells express a family of differentiation antigens that are shared by normal melanocytes. 11 This family of proteins includes tyrosinase and related proteins TRP-1 (gp75), TRP-2 (dopachrome tautomerase), gp100, and MART-1 (Melan- A). Each of these proteins plays a crucial role in melanin synthesis. Two major mechanisms of vitiligo pathogenesis in patients with cutaneous melanoma have been proposed by the antibody-based theory and the T-cell based theory. In the antibody-based theory, the host antibodies lyse melanocytes and melanoma cells. Studies have detected the presence of autoantibodies recognizing tyrosinase, TRP-1, and TRP-2 from the serum samples of patients with melanoma and those with vitiligo. 17 In the T-cell based theory, the host CD8 + T cells react with host melanoma and cross-react with benign melanocytes, leading to destruction. Clonotypically, identical T cells have been found in cutaneous melanoma and vitiligo patches. 18 Furthermore, most cells infiltrating vitiligo are CD8 + T cells that recognize melanocytes and melanoma cells. 19 The published incidence of melanoma-associated vitiligo has varied at 2.8%, 3.7%, 4.1%, and 5% and is higher than vitiligo in the general population. 3-5,20 On the basis of age differences, lack of family history, and clinicopathologic findings, Koh et al 21 have suggested that vitiligo associated with cutaneous melanoma may be different from autoimmune vitiligo unassociated with melanoma. There is little in the literature on cutaneous vitiligo in patients with uveal melanoma. Individual observations of cutaneous vitiligo developing after enucleation 7,8 or evisceration 9 jamaophthalmology.com JAMA Ophthalmology September 2013 Volume 131, Number
5 Research Original Investigation Cutaneous Vitiligo After Uveal Melanoma Management of eyes with uveal melanoma have been reported. In 1968, Nirankari et al 9 described a 57-year-old man who underwent evisceration for panophthalmitis from undetected ocular melanoma, and cutaneous vitiligo was detected 7 years later with subsequent orbital melanoma recurrence thereafter. A similar phenomenon of depigmentation of the cutaneous nevus into the halo nevus has been observed following treatment of uveal melanoma. 7,10 The development of vitiligo in patients with cutaneous melanoma has been associated with increased survival rates, attributed to activation of a systemic immune response. 4 In 1983, Nordlund et al 5 reported that the 5-year survival rate with patients who manifest melanoma-related vitiligo was significantly enhanced. In 1987, a more extensive study by Bystryn et al 3 reached similar conclusions. However, these studies drew patients with stage I or II disease. Recently, in a cohort of patients with metastatic cutaneous melanoma, Quaglino et al 4 reported that vitiligo was an independent positive prognostic factor correlated with significantly enhanced 5-year survival. In fact, vitiligo induction is recognized as a marker of effective melanoma tumor immunotherapy. Nordlund and Lerner 22 suggested that vitiligo should be induced in patients after resection of primary melanoma. In a series of 374 patients with metastatic melanoma who were treated with high-dose interleukin 2, 22% developed treatment-related vitiligo. 23 In conclusion, vitiligo can occur rarely in association with uveal melanoma. When present, it usually develops late in the clinical course with a predilection for bilateral, asymmetric involvement of the upper body. The potential prognostic benefit of this finding in these patients remains to be determined. ARTICLE INFORMATION Submitted for Publication: October 30, 2012; final revision received December 29, 2012; accepted February 26, Published Online: July 25, doi: /jamaophthalmol Author Contributions: Drs Rishi and C. L. Shields had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Rishi, Patrick. Acquisition of data: All authors. Analysis and interpretation of data: Rishi, C. L. Shields. Drafting of the manuscript: Rishi. Critical revision of the manuscript for important intellectual content: All authors. Statistical analysis: Rishi, C. L. Shields. Administrative, technical, and material support: Rishi, Patrick, J. A. Shields. Study supervision: C. L. Shields. Conflict of Interest Disclosures: None reported. Funding/Support: This study was supported by the Eye Tumor Research Foundation (Drs C. L. Shields and J. A. Shields). Role of the Sponsor: The funders had no role in the design and conduct of the study; in the collection, analysis, and interpretation of the data; and in the preparation, review or approval of the manuscript. REFERENCES 1. Taïeb A, Picardo M; VETF Members. The definition and assessment of vitiligo: a consensus report of the Vitiligo European Task Force. Pigment Cell Res. 2007;20(1): Taïeb A, Picardo M. Clinical practice: vitiligo. N Engl J Med. 2009;360(2): Bystryn JC, Rigel D, Friedman RJ, Kopf A. Prognostic significance of hypopigmentation in malignant melanoma. Arch Dermatol. 1987;123(8): Quaglino P, Marenco F, Osella-Abate S, et al. Vitiligo is an independent favourable prognostic factor in stage III and IV metastatic melanoma patients: results from a single-institution hospital-based observational cohort study. Ann Oncol. 2010;21(2): Nordlund JJ, Kirkwood JM, Forget BM, Milton G, Albert DM, Lerner AB. Vitiligo in patients with metastatic melanoma: a good prognostic sign. JAm Acad Dermatol. 1983;9(5): Shields CL, Maktabi AM, Jahnle E, Mashayekhi A, Lally SE, Shields JA. Halo nevus of the choroid in 150 patients: the 2010 Henry van Dyke Lecture. Arch Ophthalmol. 2010;128(7): Albert DM, Todes-Taylor N, Wagoner M, Nordlund JJ, Lerner AB. Vitiligo or halo nevi occurring in two patients with choroidal melanoma. Arch Dermatol. 1982;118(1): Duh EJ, Schachat AP, Albert DM, Patel SM. Long-term survival in a patient with uveal melanoma and liver metastasis. Arch Ophthalmol. 2004;122(2): Nirankari MS, Khanna KK, Mathur RP. Uveal malignant melanoma with leucoderma. J All India Ophthalmol Soc. 1968;16(2): Sarici AM, Shah SU, Shields CL, Birdsong RH, Shields JA. Cutaneous halo nevi following plaque radiotherapy for uveal melanoma. Arch Ophthalmol. 2011;129(11): Houghton AN, Eisinger M, Albino AP, Cairncross JG, Old LJ. Surface antigens of melanocytes and melanomas: markers of melanocyte differentiation and melanoma subsets. J Exp Med. 1982;156(6): Cui Z, Willingham MC. Halo naevus: a visible case of immunosurveillance in humans? Lancet Oncol. 2004;5(7): Baron J, Krol A. Management of nevi in transplant patients. Dermatol Ther. 2005;18(1): Piaserico S, Alaibac M, Fortina AB, Peserico A. Clinical and dermatoscopic fading of post-transplant eruptive melanocytic nevi after suspension of immunosuppressive therapy. JAm Acad Dermatol. 2006;54(2): Zattra E, Fortina AB, Bordignon M, Piaserico S, Alaibac M. Immunosuppression and melanocyte proliferation. Melanoma Res. 2009;19(2): Jensen P, Hansen S, Møller B, et al. Skin cancer in kidney and heart transplant recipients and different long-term immunosuppressive therapy regimens. J Am Acad Dermatol. 1999;40(2, pt 1): Ram M, Shoenfeld Y. Harnessing autoimmunity (vitiligo) to treat melanoma: a myth or reality? Ann N Y Acad Sci. 2007;1110: Becker JC, Guldberg P, Zeuthen J, Bröcker EB, Straten PT. Accumulation of identical T cells in melanoma and vitiligo-like leukoderma. JInvest Dermatol. 1999;113(6): Le Gal FA, Avril MF, Bosq J, et al. Direct evidence to support the role of antigen-specific CD8 + T cells in melanoma-associated vitiligo. J Invest Dermatol. 2001;117(6): Schallreuter KU, Levenig C, Berger J. Vitiligo and cutaneous melanoma: a case study. Dermatologica. 1991;183(4): Koh HK, Sober AJ, Nakagawa H, Albert DM, Mihm MC, Fitzpatrick TB. Malignant melanoma and vitiligo-like leukoderma: an electron microscopic study. J Am Acad Dermatol. 1983;9(5): Nordlund JJ, Lerner AB. Vitiligo and melanoma. Arch Dermatol. 1979;115(5):636. doi: / archderm Phan GQ, Attia P, Steinberg SM, White DE, Rosenberg SA. Factors associated with response to high-dose interleukin-2 in patients with metastatic melanoma. J Clin Oncol. 2001;19(15): JAMA Ophthalmology September 2013 Volume 131, Number 9 jamaophthalmology.com
Progression of Cutaneous Vitiligo in a Patient with Large Posterior Choroidal Melanoma: A Case Report
Received: November 27, 2014 Accepted after revision: January 28, 2015 Published online: April 1, 2015 2296 4681/15/0014 0241$39.50/0 Case Series and Brief Reports Progression of Cutaneous Vitiligo in a
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