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Journal of Clinical Oncology, Vol 26, No 1 (January 1), 2008: pp. 66-75 © 2008 American Society of Clinical Oncology. DOI: 10.1200/JCO.2007.12.3604 Survival for Patients With Invasive Cutaneous Melanoma Among Ethnic Groups: The Effects of Socioeconomic Status and Treatment
From the Division of Hematology/Oncology, Department of Internal Medicine, Chao Family Comprehensive Cancer Center; the Department of Epidemiology, School of Medicine; and the Genetic Epidemiology Research Institute, University of California, Irvine; and the Divisions of Hematology and Oncology, Stanford University, Palo Alto, CA Corresponding author: Jason A. Zell, DO, MPH, Department of Epidemiology, University of California, Irvine, 224 Irvine Hall, Irvine, CA 92697; e-mail: jzell{at}uci.edu
Purpose Although uncommon, melanoma is associated with poor survival characteristics among African Americans and Hispanics compared with non-Hispanic whites (NHWs). Low socioeconomic status (SES) is also associated with poor survival among patients with melanoma, but it is not known whether this is because of SES itself or because of treatment disparities. We set out to determine this by using the large, population-based California Cancer Registry (CCR) database as a model. Patients and Methods We conducted a case-only analysis of CCR data (1993 to 2003), including a descriptive analysis of relevant clinical variables and SES. The SES variable used has been derived from principle component analysis of census block-level CCR data that was linked to census data to address seven indicators of SES. Univariate analyses of overall survival (OS) were conducted using the Kaplan-Meier method. Multivariate survival analyses were performed using Cox proportional hazard ratios (HRs). Results A total of 39,049 incident patient cases of cutaneous melanoma, including 36,694 in NHWs; 127 in African Americans; 1,996 in Hispanics; and 262 in Asian-Americans, were analyzed. Higher SES was associated with an early stage at presentation (P < .0001), with treatment with surgery (P = .0005), and with prolonged survival (P < .0001). After adjustments for age, sex, histology, American Joint Committee on Cancer stage, anatomic site, treatment, and SES, a statistically significant increased risk of death was observed for African Americans compared with NHWs (HR, 1.60; 95% CI, 1.17 to 2.18); no survival differences were noted for Asians or Hispanics compared with NHWs in the adjusted analysis. Conclusion Low SES independently predicts poor outcome among patients with cutaneous melanoma. However, the poor OS observed for African American patients with melanoma is not explained by differences in treatment or SES.
Non-Hispanic whites (NHWs) are at an increased risk for developing melanoma.1 Melanomas in ethnic minority populations generally occur in different anatomic sites than in NHWs and are associated with different histologies, thicker lesions, and poorer survival.2-10 Poor survival characteristics have been observed in African Americans with cutaneous melanoma. This finding is not explained by differences in stage at presentation when using the 2002 edition of the American Joint Committee on Cancer staging system, which incorporates factors such as Breslow depth and presence of ulceration.10 Reasons for the observed poor survival characteristics among African American patients with cutaneous melanoma are currently unknown. Differences in socioeconomic status (SES) may explain the observed survival differences among ethnic minority populations in the United States. Although melanoma incidence is generally associated with high SES,11-13 low SES has been associated with an advanced stage at presentation9,14-16 and with decreased survival.9,17,18 However, the role of SES on treatment and survival among ethnic minority patients with melanoma in the United States has not been determined. We investigated if the differences in SES explain the differences in treatment rendered or in survival among ethnic minority patients with melanoma by using the large, population-based California Cancer Registry (CCR) as a model.
Study Population We performed a retrospective, case-only analysis of invasive cutaneous melanoma patient cases in the CCR database. The CCR is part of the National Cancer Institute's Surveillance, Epidemiology, and End Results (SEER) program and is the largest contiguous-area, population-based cancer registry in the world19; standardized data collection and quality control procedures have been in place since 1988.20-23 Case reporting is estimated at 99% for the entire state of California,24 and follow-up completion rates are more than 95%. Data were abstracted from medical and laboratory records by trained tumor registrars.22 Tumor site and histology were coded according to the WHO criteria in International Classification of Diseases for Oncology (ICD-O; 3rd edition).25 Patient cases were extracted based on histologic types for cutaneous melanomas (SEER code = 25010) according to ICD-O-3: superficial spreading melanoma (SSM; 8743), lentigo maligna melanoma (LMM; 8742), nodular melanoma (NM; 8721), acral lentiginous melanoma (ALM; 8744), melanoma not otherwise specified (NOS; 8720), and all other morphologies (other; 8722, 8723, 8730, 8740, 8745, 8761, 8770-8773, and 8780). Patient cases with melanoma in situ and patient cases with the following unknown or missing variables were excluded: missing information on the number of positive regional nodes (n = 1,661; 3.08%), unknown tumor thickness (n = 6,803; 12.6%), nonspecific or unknown SEER extent-of-disease classification (n = 1,018; 1.89%), and number of patients whose diagnosis dates and follow-up dates were inconsistent (n = 18; 0.03%). SEER extent-of-disease and surgical-staging variables were used to derive TNM data in accordance with the 2002 AJCC staging system, as performed previously.26-28 Patient cases of melanoma with tumor sizes less than 1.0 mm were coded as stage IA (without ulceration) or IB (with ulceration). Tumors between 1.0 and 2.0 mm were coded as stage IB (without ulceration) or IIA (with ulceration). Stage IIA patient cases also included nonulcerated tumors between 2.0 and 4.0 mm. Ulcerated tumors between 2.0 and 4.0 mm were coded as stage IIB along with nonulcerated tumors of greater than 4.0 mm. Stage IIC included ulcerated tumors greater than 4.0 mm. According to AJCC 2002, stage III classification requires inclusion of microscopic versus macroscopic nodal involvement. Because these variables were not available in the CCR, we could not assess nodal stage N1a through N3a. However, the CCR's variable for regional positive node status was used to classify the number of positive macroscopic lymph nodes. Stage IIIB patient cases included nonulcerated tumors with 1 to 3 positive regional nodes. Stage IIIC included ulcerated tumors with 1 to 3 positive regional nodes, or tumors with at least four positive regional nodes regardless of ulceration. Tumors of any size with metastatic involvement were coded as stage IV. Data were obtained on 39,049 incident patient cases of cutaneous melanoma during 1993 to 2003 in the CCR. Type of reporting source was available for each case: no cases were identified through death certificate only, and only two cases were identified through autopsy alone. The remaining cases were identified through high-quality reporting sources (ie, hospital inpatient/outpatient centers, oncology treatment centers, laboratories, private practitioners, or nursing home/convalescent home/hospice facilities). Recorded data included demographic information, stage at presentation, histology, treatment during the first course of therapy, SES, and vital status. SES is denoted as a single-index variable in the CCR by using statewide measures of education, income, and occupation from census data, as described previously.29 The SES variable used is a composite index that is based on the principle component analysis of census block-level CCR data linked to census data that assesses education level, median household income, proportion below 200% poverty level, median house value, median rent, percent employed, and percent with blue-collar employment, as previously described.19,29-33 Quintiles for the SES score were analyzed. Cause of death was recorded according to ICD criteria in effect at the time of death.25 Hospital registrars contacted cases annually, and CCR staff annually reviewed state death certificates to identify deceased registry patient cases. The last date of follow-up was either the date of death or the last date of contact.
Statistical Analysis
Ethical Considerations
Demographic Data Demographic and clinical data for the entire study population are presented in Table 1. Identified patient cases included 36,694 NHWs (94.0%); 127 African Americans (0.3%); 262 Asians (0.7%); and 1,966 Hispanics (5.0%; P < .0001). Additionally, 13 Native Americans and 2,953 patient cases reporting other race/ethnicity were identified and excluded, thereby restricting the primary analyses to the four major ethnic groups noted above. Median age at diagnosis was statistically different by race/ethnicity: 58 years for NHWs, 61 years for African Americans, 55 years for Asians, and 49 years for Hispanics (P < .0001). The distribution by sex also varied among the different races/ethnicities: NHW men account for 58.0%, African American men for 42.5%, Asian men for 51.5%, and Hispanic men for 39.0% (P < .0001).
Clinicopathologic Characteristics Among NHWs, 35.0% had SSM, 5.7% had LMM, 8.7% had NM, and only 0.8% had ALM. Among African Americans, the distribution was 13.4% with ALM, 11.0% with NM, and 24.4% with SSM. Asians and Hispanics had higher NM rates of 14.1% and 11.4%, respectively. The proportion of cases with stage I, stage II, stage III, and stage IV disease at presentation was as follows: 80.3%, 14.4%, 4.6%, and 0.7%, respectively, in NHWs; 62.2%, 33.8%, 4.0%, and 0.0%, respectively, in African Americans; 59.5%, 28.2%, 11.1%, and 1.2%, respectively, in Asians; and 71.1%, 18.7%, 8.4%, and 1.8%, respectively, in Hispanics. Although 34.6% of melanomas in NHW patient cases occurred in the trunk, melanomas in the African American, Asian/Pacific Islander, and Hispanic patient cases occurred in the lower extremity (54.3%, 47.3%, and 31.6%, respectively). African American and Asian/Pacific Islander patient cases had significantly higher incidences of ulcerated tumors (11.9% and 15.0%, respectively) compared with NHW and Hispanic patient cases (5.9% and 9.6%, respectively). Among the NHW, African American, Asian/Pacific Islander, and Hispanic patient cases that received surgery, the majority received wide excision (77.7%, 69.3%, 75.8%, and 73.6%, respectively), followed by local tumor excision (11.2%, 14.5%, 9.2%, and 13.0%, respectively). Although statistically significant differences were noted across the various ethnic groups by treatment variables (ie, surgery, chemotherapy, radiation therapy, and immunotherapy), these differences were small (Table 1).
SES Analysis
Univariate Survival Analysis
One year, 5-year, and 10-year melanoma-specific survival rates were 98.6%, 91.4%, and 87.3%, respectively, for NHWs; 98.2%, 77.1%, and 66.4%, respectively, for African Americans; 98.3%, 86.9%, and 80.6%, respectively, for Asians; and 97.3%, 88.1%, and 84.1%, respectively, for Hispanics (P < .0001; Fig 1B).
Cause of Death Analysis
Multivariate Survival Analysis
Multivariate survival analysis for treatment types after adjustment for age, sex, histologic subtype, 2002 AJCC stage, race/ethnicity, melanoma site, and SES revealed a significantly decreased risk of death for patient cases who received surgery (OS: HR, 0.53; 95% CI, 0.45 to 0.63; MSS: HR, 0.56; 95% CI, 0.41 to 0.75; Table 2). For OS and MSS, patient cases who received chemotherapy, radiation therapy, or immunotherapy had a significantly increased risk of death. This trend likely reflects the fact that such treatments were reserved for cases with poor prognostic features, advanced stage, or incompletely resected tumors. In the unadjusted (Fig 2) and adjusted survival analyses, there was an incremental increase in the risk of death for each decrease in SES quintile. For OS, the HRs for the highest to the lowest SES quintiles were as follows: 0.63 (95% CI, 0.58 to 0.69), 0.76 (95% CI, 0.70 to 0.83), 0.83 (95% CI, 0.76 to 0.91), 0.92 (95% CI, 0.83 to 1.00), and 1.00 (reference). A similar trend was noted for MSS (Table 2).
Our data show that, among invasive cutaneous melanoma patient cases, African Americans have poorer survival rates than NHWs, even after adjustment for age, sex, histologic subtype, 2002 AJCC stage (which includes Breslow depth), anatomic site, treatment with surgery, radiation therapy, chemotherapy, immunotherapy, and SES. Thus, treatment differences and differences in SES do not explain the poor survival for patient cases of melanoma in African Americans. Our epidemiologic analysis of 39,049 patient cases, including 127 African Americans and 1,966 Hispanics, represents one of the largest reported clinical outcomes studies to assess the role of SES on outcomes in cutaneous melanoma occurring in ethnic minority populations. African American race/ethnicity has been associated with poor survival for various malignancies, such as pancreatic cancer33 and breast cancer34; yet, in these cancer types, the observed survival differences were related to treatment disparities or to disparities in SES. Although we are the first to report the independent increase in hazard of death for African Americans with melanoma after accounting for the effects of treatment and SES differences, others have reported ethnic differences in clinical outcomes for melanoma. A recent study of US SEER data during 1992 to 2002 involved 48,143 NHWs, 251 African Americans, 932 Hispanics, and 394 Asians; NHWs had improved OS compared with African Americans.10 In the multivariate analysis, these investigators showed that, after adjustment for age, sex, and SEER region, there was an increased risk of mortality in other races/ethnicities compared with NHWs. When their analysis was adjusted for stage and for other factors, such as tumor size, anatomic site, and histologic subtypes, only the African Americans showed a greater mortality risk compared with NHWs.10 Although our study of melanoma using the CCR data has fewer African Americans (127 patient cases) than this SEER study (251 patient cases), the CCR contains information on SES and on additional treatment variables not recorded in SEER, which allowed us to account for the potential confounding effects of these factors on survival. The major observed difference in survival for African Americans compared with NHWs in our study resulted from differences in stage-specific survival, particularly within stage II melanoma. Rates of treatment (Table 1) were similar, and rates of treatment refusal were similarly low in both groups (data not shown). A greater proportion of African Americans (and also of Asians) had ulcerative lesions compared with NHWs, including those diagnosed as stage IIC (T4bN0M0)—a stage grouping that exhibits particularly poor survival when compared with stage IIA, IIB, or even stage III disease.28 The major survival differences become apparent after approximately 2 years (Fig 1A, B), and the reason for this is unknown. Two possible explanations are proposed. African Americans with melanoma may be inadequately staged compared with NHWs (because of factors unaccounted for in this study, such as access to subspecialty care), which results in inadequate treatment and long-term survival differences. Alternatively, melanoma in African Americans may represent a biologically different cancer, and certain individuals may have a particularly aggressive biology. Our study demonstrates significant differences in the distribution of melanoma histologic subtypes among various US races/ethnicities. A consideration might be that survival in African Americans is poorer because of a higher incidence of ALM and because of deeper lesions, but we have adjusted for these factors. ALM histology was associated with poor OS and MSS on unadjusted analysis in our study (data not shown)—a finding that did not persist in the adjusted analysis (Table 2). Melanoma NOS was the most common histologic subtype in all races/ethnicities, as has been shown in other population-based studies.2,6,9 A high percentage of melanoma-NOS exists in any large epidemiologic study2,35 and is a known limitation of such studies. It is possible that a high percentage of melanoma NOS histology among the African Americans is in fact misdiagnosed ALM; however, 99.96% of all our patient cases and 99.97% of the melanoma NOS patient cases were confirmed microscopically. Nonetheless, these specimens were not all reviewed by the same pathologists or by pathologists with the same background (a limitation of population-based analyses). The CCR data does not include comorbidity information, insurance status, or date of relapse; nor does it contain specific melanoma sites, like subungal melanoma or plantar melanoma. Thus, we are unable to account for the effect of these additional variables on survival. Gene-environment interactions may explain the observed survival differences in our study (ie, differential mutation spectra in BRAF or NRAS).36,37 Recently, gene alterations were shown to vary with melanoma site and also with sun exposure levels.38 Skin melanomas without signs of chronic sun-induced damage (CSD) frequently harbor mutations in BRAF or NRAS.38 However, CSD skin melanomas and melanomas of mucosal and acral sites often have wild-type BRAF or NRAS and are associated with increased copy numbers of downstream RAS-BRAF pathway components, including cyclin-dependent kinase 4 and cyclin D1.38 Gene amplification and mutations in KIT have also been discovered among these mucosal, acral, and CSD melanomas, thus implicating a potential role for targeted therapy with the cyclin-dependent kinase 4–inhibitor imatinib.39 Melanocortin-1 receptor (MC1R) gene variants are associated with BRAF mutations in non-CSD melanomas among NHW populations.40 However, potential differences in NRAS or KRAS mutational spectra across the major ethnicities represented in the United States are not yet determined. Alternatively, different DNA/gene ultraviolet (UV) repair mechanisms may exist that explain the ethnic differences in survival observed in our study. For both Hispanics and African Americans, melanoma incidence is positively associated with the UV index.5,6,41,42 However, another study showed that melanoma incidence was associated with increased UV index only in NHWs.43 Possible ethnic differences may exist in the oxidation of melanin and in the release of reactive oxygen species secondary to melanosomal damage, DNA damage, and redox metabolism.44-46 The results from our study indicate that more awareness efforts are warranted for the prevention and control of melanoma in all races/ethnicities, even for those patients who are at a lower risk of developing the disease. Additional biologic and genetic studies are required to explain differential effects among race/ethnicities, specifically among African Americans. Such research efforts will help uncover reasons for the observed poor survival of African Americans with melanoma and may also lead to targeted therapeutic interventions.
The author(s) indicated no potential conflicts of interest.
Conception and design: Jason A. Zell, Mehrdad Mobasher, Argyrios Ziogas, Frank L. Meyskens Jr, Hoda Anton-Culver Financial support: Hoda Anton-Culver Administrative support: Hoda Anton-Culver Provision of study materials or patients: Hoda Anton-Culver Collection and assembly of data: Jason A. Zell, Pelin Cinar, Hoda Anton-Culver Data analysis and interpretation: Jason A. Zell, Pelin Cinar, Mehrdad Mobasher, Argyrios Ziogas, Frank L. Meyskens Jr, Hoda Anton-Culver Manuscript writing: Jason A. Zell, Pelin Cinar, Mehrdad Mobasher, Argyrios Ziogas, Frank L. Meyskens Jr, Hoda Anton-Culver Final approval of manuscript: Jason A. Zell, Pelin Cinar, Mehrdad Mobasher, Argyrios Ziogas, Frank L. Meyskens Jr, Hoda Anton-Culver
Cancer incidence data used in this study under subcontract No. 050N-8707-S1527 with the Public Health Institute, State of California, was supported by the California Department of Health Services as part of the statewide cancer reporting program mandated by California Health and Safety Code Sections 103875 and 103885; the National Cancer Institute Surveillance, Epidemiology and End Results Program; and the Centers for Disease Control and Prevention National Program of Cancer Registries. Presented in part at the 42nd Annual Meeting of the American Society of Clinical Oncology, Atlanta, GA, June 2-6, 2006. The ideas and opinions expressed herein are those of the authors, and endorsement by the State of California, Department of Health Services, the National Cancer Institute, the Centers for Disease Control and Prevention, and/or the Genetic Epidemiology Research Institute of the University of California, Irvine is not intended, nor should it be inferred. Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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Copyright © 2008 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
2 test or Fisher's exact test for categoric and dichotomous variables and with the nonparametric Kruskall-Wallis test for the comparison of continuous variables for more than two groups. Life tables and Kaplan-Meier curves were generated for race/ethnicity and SES categories, and curves were compared with the log-rank test. Multivariate survival analysis was utilized to calculate overall survival and melanoma-specific survival (MSS) with Cox proportional hazard ratios (HRs). All statistical analyses were conducted using SAS 9.1 statistical software (SAS Institute, Inc, Cary, NC). Statistical significance was assumed for a two-tailed P < .05. 
