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Published in: Annals of Surgical Oncology 8/2020

01-08-2020 | Lymphoma | Melanoma

Outcomes of Immunosuppressed Patients Who Develop Melanoma: A Population-Based Propensity-Matched Cohort Study

Authors: Janice Austin, MD, Frances C. Wright, MD, Stephanie Y. Cheng, MSc, Rinku Sutradhar, PhD, Nancy N. Baxter, MD, Nicole J. Look Hong, MD

Published in: Annals of Surgical Oncology | Issue 8/2020

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Abstract

Introduction

Few studies have examined outcomes in immunosuppressed patients who develop melanoma. The purpose of this study is to compare survival in immunosuppressed patients who developed melanoma with that in patients with melanoma who are not immunosuppressed.

Methods

Immunosuppressed patients were defined as having solid organ transplant, lymphoma, leukemia, or human immunodeficiency virus prior to diagnosis of melanoma. Patients with cutaneous melanoma with and without immunosuppression were identified retrospectively from the Ontario Cancer Registry (2007–2015) and linked with administrative databases to identify demographics, treatment, and outcomes. Immunosuppressed patients were matched with non-immunosuppressed patients based on age at diagnosis, sex, birth year, stage at diagnosis, and propensity score. The primary outcome was overall survival. Multivariable Cox proportional hazard regression was used to identify factors associated with survival.

Results

Baseline characteristics were well balanced in 218 immunosuppressed patients matched to 436 controls. Of the patients, 186 (28.4%) were female, and median age at melanoma diagnosis was 69 (interquartile range, IQR 59–78) years. Three-year overall survival (OS) was 65% for immunosuppressed patients and 79% for non-immunosuppressed patients. Melanoma was the leading cause of death for both groups. On multivariable analysis, immunosuppression was associated with increased mortality [hazard ratio (HR) 1.70, 95% confidence interval (CI) 1.30–2.23]. Adequate treatment (HR 0.36, 95% CI 0.22–0.58) and dermatologist visits either before (HR 0.52, 95% CI 0.36–0.73) or after (HR 0.61, 95% CI 0.41–0.90) melanoma diagnosis were associated with improved OS.

Conclusions

Immunosuppressed patients who develop melanoma have worse outcomes when matched to non-immunosuppressed patients. This decrease in survival appears related to the underlying condition rather than diagnosis of melanoma.
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Literature
1.
go back to reference Kubica AW, Brewer JD. Melanoma in immunosuppressed patients. Mayo Clin Proc. 2012;87:991–1003.CrossRef Kubica AW, Brewer JD. Melanoma in immunosuppressed patients. Mayo Clin Proc. 2012;87:991–1003.CrossRef
2.
go back to reference Lindelof B, Sigurgeirsson B, Gabel H, et al. Incidence of skin cancer in 5356 patients following organ transplantation. Br J Dermatol. 2000;143:513–519.PubMed Lindelof B, Sigurgeirsson B, Gabel H, et al. Incidence of skin cancer in 5356 patients following organ transplantation. Br J Dermatol. 2000;143:513–519.PubMed
3.
go back to reference Mudigonda T, Levender MM, O’Neill JL, et al. Incidence, risk factors, and preventative management of skin cancers in organ transplant recipients: A review of single‐ and multicenter retrospective studies from 2006 to 2010. Dermatol Surg. 2013;39:345–364.CrossRef Mudigonda T, Levender MM, O’Neill JL, et al. Incidence, risk factors, and preventative management of skin cancers in organ transplant recipients: A review of single‐ and multicenter retrospective studies from 2006 to 2010. Dermatol Surg. 2013;39:345–364.CrossRef
4.
go back to reference Vajdic CM, van Leeuwen MT, Webster AC, et al. Cutaneous melanoma is related to immune suppression in kidney transplant recipients. Cancer Epidemiol Biomarkers Prev. 2009;18:2297–2303.CrossRef Vajdic CM, van Leeuwen MT, Webster AC, et al. Cutaneous melanoma is related to immune suppression in kidney transplant recipients. Cancer Epidemiol Biomarkers Prev. 2009;18:2297–2303.CrossRef
5.
go back to reference Le Mire L, Hollowood K, Gray D, et al. Melanomas in renal transplant recipients. Br J Dermatol. 2006;154:472–477.CrossRef Le Mire L, Hollowood K, Gray D, et al. Melanomas in renal transplant recipients. Br J Dermatol. 2006;154:472–477.CrossRef
6.
go back to reference Brewer JD, Habermann TM, Shanafelt TD. Lymphoma‐associated skin cancer: Incidence, natural history, and clinical management. Int J Dermatol. 2014;53:267–274.CrossRef Brewer JD, Habermann TM, Shanafelt TD. Lymphoma‐associated skin cancer: Incidence, natural history, and clinical management. Int J Dermatol. 2014;53:267–274.CrossRef
7.
go back to reference Brewer JD, Shanafelt TD, Call TG, et al. Increased incidence of malignant melanoma and other rare cutaneous cancers in the setting of chronic lymphocytic leukemia. Int J Dermatol. 2015;54:287.CrossRef Brewer JD, Shanafelt TD, Call TG, et al. Increased incidence of malignant melanoma and other rare cutaneous cancers in the setting of chronic lymphocytic leukemia. Int J Dermatol. 2015;54:287.CrossRef
8.
go back to reference Famenini S, Martires KJ, Zhou H, et al. Melanoma in patients with chronic lymphocytic leukemia and non-hodgkin lymphoma. J Am Acad Dermatol. 2015;72:78–84.CrossRef Famenini S, Martires KJ, Zhou H, et al. Melanoma in patients with chronic lymphocytic leukemia and non-hodgkin lymphoma. J Am Acad Dermatol. 2015;72:78–84.CrossRef
9.
go back to reference McKenna DB, Stockton D, Brewster DH, et al. Evidence for an association between cutaneous malignant melanoma and lymphoid malignancy: A population-based retrospective cohort study in Scotland. Br J Cancer. 2003;88:74–78.CrossRef McKenna DB, Stockton D, Brewster DH, et al. Evidence for an association between cutaneous malignant melanoma and lymphoid malignancy: A population-based retrospective cohort study in Scotland. Br J Cancer. 2003;88:74–78.CrossRef
10.
go back to reference Olsen CM, Lane SW, Green AC. Increased risk of melanoma in patients with chronic lymphocytic leukaemia: Systematic review and meta-analysis of cohort studies. Melanoma Res. 2016;26:188–194.CrossRef Olsen CM, Lane SW, Green AC. Increased risk of melanoma in patients with chronic lymphocytic leukaemia: Systematic review and meta-analysis of cohort studies. Melanoma Res. 2016;26:188–194.CrossRef
11.
go back to reference Kind GM, VonRoenn J, Jansen DA, et al. Human immunodeficiency virus infection and subsequent melanoma. Ann Plast Surg. 1996;37:273–277.CrossRef Kind GM, VonRoenn J, Jansen DA, et al. Human immunodeficiency virus infection and subsequent melanoma. Ann Plast Surg. 1996;37:273–277.CrossRef
12.
go back to reference Olsen CM, Knight LL, Green AC. Risk of melanoma in people with HIV/AIDS in the pre- and post-HAART eras: a systematic review and meta-analysis of cohort studies. PLoS ONE. 2014;9:e95096.CrossRef Olsen CM, Knight LL, Green AC. Risk of melanoma in people with HIV/AIDS in the pre- and post-HAART eras: a systematic review and meta-analysis of cohort studies. PLoS ONE. 2014;9:e95096.CrossRef
13.
go back to reference Wilkins K, Turner R, Dolev JC, et al. Cutaneous malignancy and human immunodeficiency virus disease. J Am Acad Dermatol. 2006;54:189–206.CrossRef Wilkins K, Turner R, Dolev JC, et al. Cutaneous malignancy and human immunodeficiency virus disease. J Am Acad Dermatol. 2006;54:189–206.CrossRef
14.
go back to reference Crum-Cianflone N, Hullsiek KH, Satter E, et al. Cutaneous malignancies among HIV-infected persons. Arch Intern Med. 2009;169:1130–1138.CrossRef Crum-Cianflone N, Hullsiek KH, Satter E, et al. Cutaneous malignancies among HIV-infected persons. Arch Intern Med. 2009;169:1130–1138.CrossRef
15.
go back to reference Antoniou T, Zagorski B, Loutfy MR, Strike C, Glazier RH. Validation of case-finding algorithms derived from administrative data for identifying adults living with human immunodeficiency virus infection. PLOS One. 2011;6(6):e21748.CrossRef Antoniou T, Zagorski B, Loutfy MR, Strike C, Glazier RH. Validation of case-finding algorithms derived from administrative data for identifying adults living with human immunodeficiency virus infection. PLOS One. 2011;6(6):e21748.CrossRef
16.
go back to reference Johnson DB, Smalley KSM, Sosman JA. Molecular pathways: Targeting NRAS in melanoma and acute myelogenous leukemia. Clin Cancer Res. 2014;20:4186–4192.CrossRef Johnson DB, Smalley KSM, Sosman JA. Molecular pathways: Targeting NRAS in melanoma and acute myelogenous leukemia. Clin Cancer Res. 2014;20:4186–4192.CrossRef
17.
go back to reference Zattra E, Belloni Fortina A, Bordignon M, et al. Immunosuppression and melanocyte proliferation. Melanoma Res. 2009;19:63–68.CrossRef Zattra E, Belloni Fortina A, Bordignon M, et al. Immunosuppression and melanocyte proliferation. Melanoma Res. 2009;19:63–68.CrossRef
18.
go back to reference Look Hong NJ, Cheng SY, Baxter NN, et al. Melanoma patterns of care in Ontario: a call for a strategic alignment of multidisciplinary care. J Surg Oncol. 2018;117:597–617.CrossRef Look Hong NJ, Cheng SY, Baxter NN, et al. Melanoma patterns of care in Ontario: a call for a strategic alignment of multidisciplinary care. J Surg Oncol. 2018;117:597–617.CrossRef
19.
go back to reference Weiner JP, Starfield BH, Steinwachs DM, et al. Development and application of a population-oriented measure of ambulatory care case-mix. Med Care 1991;29:452–472.CrossRef Weiner JP, Starfield BH, Steinwachs DM, et al. Development and application of a population-oriented measure of ambulatory care case-mix. Med Care 1991;29:452–472.CrossRef
21.
go back to reference Bovenschen HJ, Tjioe M, Vermaat H, et al. Induction of eruptive benign melanocytic naevi by immune suppressive agents, including biologicals. Br J Dermatol. 2006;154:880–884.CrossRef Bovenschen HJ, Tjioe M, Vermaat H, et al. Induction of eruptive benign melanocytic naevi by immune suppressive agents, including biologicals. Br J Dermatol. 2006;154:880–884.CrossRef
22.
go back to reference Reid RJ, MacWilliam L, Verhulst L, et al. Performance of the ACG case-mix system in two Canadian provinces. Med Care. 2001;39:86–99.CrossRef Reid RJ, MacWilliam L, Verhulst L, et al. Performance of the ACG case-mix system in two Canadian provinces. Med Care. 2001;39:86–99.CrossRef
23.
go back to reference Reid RJ, Roos NP, MacWilliam L, et al. Assessing population health care need using a claims‐based ACG morbidity measure: A validation analysis in the province of Manitoba. Health Serv Res. 2002;37:1345–1364.CrossRef Reid RJ, Roos NP, MacWilliam L, et al. Assessing population health care need using a claims‐based ACG morbidity measure: A validation analysis in the province of Manitoba. Health Serv Res. 2002;37:1345–1364.CrossRef
24.
go back to reference Brewer JD, Christenson LJ, Weenig RH, et al. Effects of chronic lymphocytic leukemia on the development and progression of malignant melanoma. Dermatol Surg. 2010;36:368–376.CrossRef Brewer JD, Christenson LJ, Weenig RH, et al. Effects of chronic lymphocytic leukemia on the development and progression of malignant melanoma. Dermatol Surg. 2010;36:368–376.CrossRef
25.
go back to reference Velez NF, Karia PS, Vartanov AR, et al. Association of advanced leukemic stage and skin cancer tumor stage with poor skin cancer outcomes in patients with chronic lymphocytic leukemia. JAMA Dermatol. 2014;150:280–287.CrossRef Velez NF, Karia PS, Vartanov AR, et al. Association of advanced leukemic stage and skin cancer tumor stage with poor skin cancer outcomes in patients with chronic lymphocytic leukemia. JAMA Dermatol. 2014;150:280–287.CrossRef
26.
go back to reference McIntosh BC, Ariyan S, Esche G, et al. Metachronous primary melanoma and lymphoma. Ann Plast Surg. 2010;64:229–232.CrossRef McIntosh BC, Ariyan S, Esche G, et al. Metachronous primary melanoma and lymphoma. Ann Plast Surg. 2010;64:229–232.CrossRef
27.
go back to reference Donahue T, Lee CY, Sanghvi A, et al. Immunosuppression is an independent prognostic factor associated with aggressive tumor behavior in cutaneous melanoma. J Am Acad Dermatol. 2015;73:461–466.CrossRef Donahue T, Lee CY, Sanghvi A, et al. Immunosuppression is an independent prognostic factor associated with aggressive tumor behavior in cutaneous melanoma. J Am Acad Dermatol. 2015;73:461–466.CrossRef
28.
go back to reference Matin RN, Mesher D, Proby CM, et al. Melanoma in organ transplant recipients: Clinicopathological features and outcome in 100 cases. Am J Transplant. 2008;8:1891–1900.CrossRef Matin RN, Mesher D, Proby CM, et al. Melanoma in organ transplant recipients: Clinicopathological features and outcome in 100 cases. Am J Transplant. 2008;8:1891–1900.CrossRef
29.
go back to reference Brewer JD, Christenson LJ, Weaver AL, et al. Malignant melanoma in solid transplant recipients: Collection of database cases and comparison with surveillance, epidemiology, and end results data for outcome analysis. Arch Dermatol. 2011;147:790–796.CrossRef Brewer JD, Christenson LJ, Weaver AL, et al. Malignant melanoma in solid transplant recipients: Collection of database cases and comparison with surveillance, epidemiology, and end results data for outcome analysis. Arch Dermatol. 2011;147:790–796.CrossRef
30.
go back to reference Brewer JD, Shanafelt TD, Otley CC, et al. Chronic lymphocytic leukemia is associated with decreased survival of patients with malignant melanoma and Merkel cell carcinoma in a SEER population-based study. J Clin Oncol. 2012;30:843–849.CrossRef Brewer JD, Shanafelt TD, Otley CC, et al. Chronic lymphocytic leukemia is associated with decreased survival of patients with malignant melanoma and Merkel cell carcinoma in a SEER population-based study. J Clin Oncol. 2012;30:843–849.CrossRef
31.
go back to reference Rodrigues LKE. Altered clinical course of malignant melanoma in HIV-positive patients. JAMA 2002;288:1217. Rodrigues LKE. Altered clinical course of malignant melanoma in HIV-positive patients. JAMA 2002;288:1217.
32.
go back to reference Siegel RL, Miller KD, Jemal, A. Cancer statistics, 2016. CA: Cancer J Clin. 2016;66(1): 7–30.CrossRef Siegel RL, Miller KD, Jemal, A. Cancer statistics, 2016. CA: Cancer J Clin. 2016;66(1): 7–30.CrossRef
33.
go back to reference Sharon CE, Sinnamon AJ, et al. Association of marital status with T stage at presentation and management of early-stage melanoma. JAMA Dermatol. 2018;154(5):574–580.CrossRef Sharon CE, Sinnamon AJ, et al. Association of marital status with T stage at presentation and management of early-stage melanoma. JAMA Dermatol. 2018;154(5):574–580.CrossRef
34.
go back to reference Andrews MC, Turner N, Boyd J, et al. Cellular mechanisms underlying complete hematological response of chronic myeloid leukemia to BRAF and MEK1/2 inhibition in a patient with concomitant metastatic melanoma. Clin Cancer Res. 2015;21:5222–5234.CrossRef Andrews MC, Turner N, Boyd J, et al. Cellular mechanisms underlying complete hematological response of chronic myeloid leukemia to BRAF and MEK1/2 inhibition in a patient with concomitant metastatic melanoma. Clin Cancer Res. 2015;21:5222–5234.CrossRef
35.
go back to reference Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D. RAS oncogenes: weaving a tumorigenic web. Nat Rev Cancer. 2011;11:671–774.CrossRef Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D. RAS oncogenes: weaving a tumorigenic web. Nat Rev Cancer. 2011;11:671–774.CrossRef
36.
go back to reference Jakob JA, Bassett RL, Ng CS, et al. NRAS mutation status is an independent prognostic factor in metastatic melanoma. Cancer 2012;118:4014–4023.CrossRef Jakob JA, Bassett RL, Ng CS, et al. NRAS mutation status is an independent prognostic factor in metastatic melanoma. Cancer 2012;118:4014–4023.CrossRef
37.
go back to reference Richert S, Bloom EJ, Flynn K, et al. Widespread eruptive dermal and atypical melanocytic nevi in association with chronic myelocytic leukemia: case report and review of the literature. J Am Acad Dermatol. 1996;35:326–329.CrossRef Richert S, Bloom EJ, Flynn K, et al. Widespread eruptive dermal and atypical melanocytic nevi in association with chronic myelocytic leukemia: case report and review of the literature. J Am Acad Dermatol. 1996;35:326–329.CrossRef
38.
go back to reference Madeleine D, Lori L, Ronald PR, et al. Eruptive dysplastic nevi associated with human immunodeficiency virus infection. Arch Dermatol. 1989;125:125–136. Madeleine D, Lori L, Ronald PR, et al. Eruptive dysplastic nevi associated with human immunodeficiency virus infection. Arch Dermatol. 1989;125:125–136.
39.
go back to reference Grob JJ, Bastuji-Garin S, Vaillant L, et al. Excess of nevi related to immunodeficiency: a study in HIV-infected patients and renal transplant patients. J Investig Dermatol. 1996;107:694–697.CrossRef Grob JJ, Bastuji-Garin S, Vaillant L, et al. Excess of nevi related to immunodeficiency: a study in HIV-infected patients and renal transplant patients. J Investig Dermatol. 1996;107:694–697.CrossRef
Metadata
Title
Outcomes of Immunosuppressed Patients Who Develop Melanoma: A Population-Based Propensity-Matched Cohort Study
Authors
Janice Austin, MD
Frances C. Wright, MD
Stephanie Y. Cheng, MSc
Rinku Sutradhar, PhD
Nancy N. Baxter, MD
Nicole J. Look Hong, MD
Publication date
01-08-2020
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 8/2020
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-020-08265-4

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