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Originally published as JCO Early Release 10.1200/JCO.2005.02.1436 on December 19 2005 © 2006 American Society of Clinical Oncology. Similar Outcomes Between African American and Non–African American Patients With Extensive-Stage Small-Cell Lung Carcinoma: Report From the Cancer and Leukemia Group BFrom the Wake Forest University School of Medicine, Winston-Salem; University of North Carolina at Chapel Hill, Chapel Hill; Cancer and Leukemia Group B Statistical Center, Duke University, Durham, NC; Ohio State University, Columbus OH; Dana Farber Cancer Institute, Boston MA; University of Tennessee–Memphis, Memphis TN; University of Chicago, Chicago IL; and Medical University of South Carolina, Charleston, SC Address reprint requests to A. William Blackstock, MD, Department of Radiation Oncology, Wake Forest University School of Medicine, Medical Center Blvd, Winston-Salem, NC 27157; e-mail: ablackst{at}wfubmc.edu
Purpose: Among patients with small-cell lung carcinoma, African Americans have lower survival rates than non–African Americans. We investigated whether the disparity in survival would persist when patients were treated with similar therapies (ie, phase II/III Cancer and Leukemia Group B [CALGB] trials). Patients and Methods: We assessed 995 patients (928 non–African American and 67 African American) receiving chemotherapy in CALGB studies for extensive-stage small-cell lung cancer (ES-SCLC). Clinical and demographic characteristics, treatment received, and survival data were obtained from the CALGB database. The Cox proportional hazards model was used to assess the effect of race/ethnicity on survival after adjustment for other known prognostic factors. All statistical tests were two sided. Results: The unadjusted survival distribution of African American patients was not significantly different from that of non–African American patients; median survival was 11.5 months (95% CI, 9.4 to 13.4 months) for African American patients versus 9.9 months (95% CI, 9.6 to 10.3 months) for non–African American patients. Multivariable adjustment for the effect of treatment arm, histology, and metastatic site at presentation did not alter the outcome for African American patients. Survival was similar even though African American patients were more likely to have a poorer performance status, present with significant weight loss, and be Medicaid recipients (20% v 6%), which is an indicator of lower socioeconomic status. Conclusion: African American patients tended to present with prognostic features associated with a worse survival. However, when offered equivalent therapy, the outcome for African American patients was the same as that observed for non–African American patients.
Lung cancer is the leading cause of cancer-related death in the United States and North America.1,2 Of the 172,570 Americans expected to be diagnosed with lung cancer in 2005, approximately 20% will be determined to have small-cell lung cancer (SCLC).3 At presentation, approximately 70% to 75% of patients with SCLC will be found to have extensive-stage SCLC (ES-SCLC), whereas the remaining 25% to 30% of patients will have local or regional disease classified as limited-stage SCLC (LS-SCLC).4 The use of systemic chemotherapy reflects the current standard of care for patients with ES-SCLC. Although the incidence of advanced-stage lung cancer has increased in most racial/ethnic groups, the rate of increase has been greatest for African American patients.5 Moreover, age-adjusted mortality rates from lung cancer are significantly higher in African Americans than in non–African Americans.6 National health surveillance statistics and other studies7-11 have examined race/ethnicity in relation to overall lung cancer prognosis, and specifically for SCLC. These data demonstrate that during the last several decades, non–African Americans have more favorable survival rates than African Americans. The prognosis for patients with SCLC is related to several factors, including pretreatment stage, sex, weight loss, and overall performance status.9,12,13 However, it is not clear that race/ethnicity, in and of itself, is important in determining the prognosis for patients diagnosed with lung cancer. Earle et al14 and others have reported variations in the use of palliative chemotherapy for advanced non-SCLC patients based on race and socioeconomic status,15-18 despite no evidence of differential treatment effectiveness according to these factors.19,20 It is possible that the overall poor outcome observed for African American patients with advanced lung cancer may be reduced or eliminated by adjusting for comorbid conditions, socioeconomic factors associated with race/ethnicity and, relevant to this report, equal access to equal (optimal) treatment. We examined survival after treatment of ES-SCLC among African American and non–African American patients participating in phase II or III Cancer and Leukemia Group B (CALGB) clinical trials. The cooperative group trial design defines the extent of disease at the time of study entry and provides for uniform therapy, thereby controlling for two major confounding factors affecting prognosis and allowing investigation of other determinants of prognosis. The mandate of the National Institutes of Health Revitalization Act of 1993 required that all National Institutes of Health–sponsored clinical trials include minorities and women in sufficient numbers to allow valid subset analysis to ascertain differences in the effect of treatments among women and minority participants.21 Our analysis in this study is an attempt to fulfill the intent of the mandate in a rational and ethically sound manner.
Patient Selection During the period from December 1990 through April 2002, the CALGB conducted four consecutive phase II/III clinical trials evaluating systemic chemotherapy as an initial treatment for 995 patients with ES-SCLC. We evaluated the database from these four trials retrospectively for this study. The CALGB definition of ES-SCLC follows the two-stage system developed by the Veterans Affairs Research Service Lung Cancer Study Group.22 LS-SCLC means tumor confined to the hemithorax of origin, the mediastinum, and the supraclavicular nodes, which can be encompassed within a tolerable radiation therapy port. ES-SCLC means tumor that is too widespread to be included within the definition of LS disease above. Patients with distant metastases (M1) were always considered to have ES disease. The four CALGB trials were protocols 9033, 9430, 9732, and 39901. During the period from December 1990 through October 1993, 303 patients with ES-SCLC were accrued to protocol 9033, a phase III trial that assessed the impact of the schedule of etoposide (3-day intravenous short course v a 21-day oral prolonged course) combined with cisplatin on efficacy, toxicity, and the quality of life of SCLC patients.23 From April 1995 through June 1999, 93 patients were accrued to protocol 9430, a randomized phase II study of topotecan plus cisplatin or topotecan paclitaxel in patients with ES-SCLC.24 Between April 1998 and July 2001, 563 patients with ES-SCLC were accrued to protocol 9732, a randomized phase III intergroup trial of etoposide and cisplatin with or without paclitaxel and granulocyte colony-stimulating factor in patients with ES-SCLC.25 Thirty-six patients were accrued to protocol 39901, a phase II study that evaluated dose-dense weekly paclitaxel in ES-SCLC from April 2000 through April 2002.26 All patients had an Eastern Cooperative Oncology Group (ECOG) performance status of 0 to 2 and adequate renal and hepatic functions. No patient received systemic chemotherapy before entry onto the study. Additional details of the design of the studies and primary findings were published elsewhere.23-26 For inclusion in this analysis, we selected all protocol-eligible patients with follow-up information whose race was reported (902 white, 12 Hispanic, eight Asian, three Native American, 67 African American, and three not otherwise specified). Patients who were registered but never received protocol treatment, patients who were determined retrospectively to have not been eligible to participate in the clinical study, and five patients who were lacking the predictors needed in the analysis were not included in this study. Thus, the multivariate survival analyses use data from 995 patients, of whom 928 were non–African American and 67 were African American patients.
Study End Points and Statistical Methods
Among the 995 patients included in this analysis, 67 (6.7%) were African American. Table 1 reflects the distribution of characteristics by race/ethnicity for all patients. Non–African Americans were more likely to present with liver involvement (50% v 37%; P = .057) than African American patients. African American patients, however, were more likely to present with worse pretreatment performance status; 83% of African American patients were ECOG  1 versus 72% for non–African American patients (P = .033). In addition, African American patients were more likely to present with greater than 5% weight loss (57% v 33%) than non–African American patients (P = .0001).
Initially, a multivariate Cox model was fit to the data and included predictors for study arm, ECOG performance status, sex, metastatic site, categorized age, and weight loss. Given that study arm was not statistically significant, it was removed from the model. Age was incorporated into the model as a categoric variable, describing age younger than 50, age 50 to 59, age 60 to 70, and age older than 70 years. All components that were not statistically significant were removed from the model. The resulting model is presented in Table 2 as the model without race. This model demonstrates that older patients had a poorer prognosis, that women had a better prognosis than men, that patients presenting with metastases to the brain and liver had a worse prognosis than those presenting with metastasis to the bone or adrenals, that pretreatment weight loss was a significant indictor of poorer prognosis, and that patients with an ECOG performance status
The survival pattern for non–African Americans was not statistically different from that for African Americans. The 1-year survival rate was 36% (95% CI, 33% to 39%) for non–African Americans and 47% (95% CI, 37% to 61%) for African Americans (Fig 1). The median survival for non–African Americans and African Americans was 9.9 months (95% CI, 9.6 to 10.3) and 11.5 months (95% CI, 9.4 to 13.4), respectively. Race/ethnicity was then incorporated into the clinical multivariate model. After adjustment for known clinical factors, race/ethnicity did not statistically significantly affect the survival of patients with ES-SCLC (Table 2). In fact, race/ethnicity did not have an independent prognostic effect on survival (relative risk = 0.87; 95% CI, 0.67 to 1.12).
Lung cancer remains the leading cause of cancer-related death in the United States. Across all stages and histologies of the disease, survival for African American patients lags behind that reported for non–African American patients.1-2,6 In a multivariate analysis of SCLC patients treated on Southwest Oncology Group trials, white race was deemed a significant favorable independent predictor of outcome. A number of potential explanations for this observation have been proposed, including later stage at diagnosis, differences in treatment, and differences in the biologic aggressiveness of the disease. Among the most controversial of these issues is whether race, in and of itself, is an independent prognostic factor. Although these factors may be important, perhaps the most relevant factor for African American patients is access to standard cancer care. Indeed, as discussed by Earle et al,14 and reflected in data from the Center for Outcomes and Policy Research at the Dana-Farber Cancer Institute, physicians have race and sex biases31 and perceived barriers to care32 that significantly influence their treatment recommendations. For example, when adjusted for associated comorbidities, African American patients with stage IV non-SCLC were less likely to receive chemotherapy than those of other races/ethnicities (odd ratio, 0.70; 95% CI, 0.55 to 0.88), as were those of lower compared with higher socioeconomic status. To this end, we proposed that African American and non–African American patients with ES-SCLC treated with equivalent therapies would have equivalent outcomes. Using the CALGB clinical trial database, we investigated this hypothesis. The CALGB lung cancer database offers several advantages over other data sources. First, stage of disease is comparable because of the constraints of the protocol entry criteria. Second, treatment and follow-up care are conducted according to a uniform standard. Third, detailed information on prognostic covariates, such as performance status and weight loss, is collected. However, one ongoing limitation of the CALGB data and data obtained by other national cooperative groups is the small number of participants from many racial groups, including African Americans.
In this cohort of 995 patients treated with chemotherapy for ES-SCLC, the 67 African American patients and 928 non–African American patients had similar clinical stages of disease at the time of protocol entry. However, the percentage of patients with a performance status of In a similar CALGB analysis of patients receiving treatment for stage IV non-SCLC, we observed that when corrected for socioeconomic factors such as income and health coverage, there was no difference in survival for African American patients and non–African American patients receiving comparable treatment.33 Somewhat in contrast to our experience, and as reported by McDavid et al34 in a population-based cancer registry study, Medicaid patients with lung cancer had a higher risk of death (comparable with those without insurance or of unknown insurance status) compared with patients who were privately insured. The authors postulate that this observation might reflect a scarcity of physicians willing to evaluate Medicaid patients for preventive care or screening. In our analysis, we found that although African American patients were more likely to be Medicaid recipients (20%) than non–African American patients (6%; P = .0012), this did not translate into a worse survival (with and without the adjustment for other factors such as race/ethnicity). One limitation of our report is the small number of African American patients with ES-SCLC treated on CALGB trials and available for analysis, making our ability to detect a difference in survival less precise. The problem with minority participation in clinical trials, however, is not unique to CALGB. In a cross-sectional population-based analysis of all participants in therapeutic nonsurgical National Cancer Institute Clinical Trial Cooperation Group lung cancer trials in 2000 through 2002, African American patients were less likely to participate in clinical trials compared with non–African American patients (odds ratio, 0.61; 95% CI, 0.59 to 0.70; P < .001).35 To this end, the CALGB, in conjunction with the National Cancer Institute, has implemented a number of initiatives to increase minority accrual in future trials (Minority Initiative Program, which established the Underserved Subcommittee within CALGB, and so on). However, our inability to detect a difference is not likely related to non–African American patients performing worse in our trials; the observed median survival of approximately 10 to 11 months in our analysis is similar to that reported in recent and comparable ES-SCLC trials from other cooperative groups,36,37 and slightly better than the 8.2 months observed in a recent Surveillance, Epidemiology, and End Results report.38,39 Our analysis would have been strengthened if data reflecting the socioeconomic differences (marital status, income, and so on) between the two groups, which may have influenced our findings, had been available for analysis. From our analysis, we conclude equal treatment in patients with ES-SCLC yields equal outcome among patients with the same stage of disease regardless of race/ethnicity. Differences in access to care, the quality of care received, and the impact of comorbid conditions may explain the lower survival reported for African American patients elsewhere in the literature. Continued efforts are needed to encourage disease awareness, promote early detection, implement prompt and proper treatment, and increase minority participation in clinical trials. Ultimately, potential interventions need to be introduced that will decrease the mortality for all patients diagnosed with ES-SCLC.
The following institutions participated in the study (institution, principal investigator, and grant numbers are listed): Cancer and Leukemia Group B (CALGB) Statistical Center, Durham, NC—Stephen George, Ph.D., supported by CA33601; Baptist Cancer Institute Community Clinical Oncology Program (CCOP)—Lee Schwartzberg, MD, Menphis, TN, supported by CA71323; Christiana Care Health Services, Inc. CCOP, Wilmington, DE—Stephen Grubbs, MD, supported by CA45418; Dana Farber Cancer Institute, Boston, MA—George P Canellos, MD, supported by CA32291; Dartmouth Medical School-Norris Cotton Cancer Center, Lebanon, NH—Marc S. Ernstoff, MD; supported by CA04326; Duke University Medical Center, Durham, NC—Jeffrey Crawford, MD, supported by CA47577; Eastern Maine Medical Center—Philip L. Brooks, MD, Bangor, ME, supported by CA35406; Green Mountain Oncology Group, Bennington, VT—H. James Wallace Jr., MD; supported by CA35091; Illinois Oncology Research Assoc, Peoria, IL, John W. Kugler, MD, supported by CA35113; Long Island Jewish Medical Center, Lake Success, NY—Marc Citron, MD, supported by CA11028; Massey Cancer Center—John D. Roberts, MD, Richmond, VA, supported by CA52784; Massachusetts General Hospital, Boston, MA—Michael L. Grossbard, MD, supported by CA12449; McGill University, Montreal, QC—Gerald Batist, MD; Medical University of South Carolina, Charleston, SC—Mark Green, MD, supported by CA03927; Memorial Sloan-Kettering Cancer Center, New York, NY, Clifford Hudis, MD, supported by CA77651; Missouri Baptist Medical Center, St. Louis, MO—Alan P Lyss, MD; Mount Sinai Medical Center, Miami, FL—Rogerio Lilenbaum, MD, supported by CA45564; Mount Sinai School of Medicine, New York, NY—Lewis R. Silverman, MD, supported by CA04457; North Shore-Long Island Jewish Medical Center, Manhasset, NY—Daniel R Budman, MD, supported by CA35279; Rhode Island Hospital, Providence, RI—William Sikov, MD, supported by CA08025; Roswell Park Cancer Institute, Buffalo, NY—Ellis Levine, MD, supported by CA02599; Southeast Cancer Control Consortium Inc. CCOP, Goldsboro, NC—James N. Atkins, MD; supported by CA45808; Southern Nevada Cancer Research Foundation CCOP, Las Vegas, NV—John Ellerton, MD, supported by CA35421; State University of New York (SUNY) Upstate Medical University, Syracuse, NY—Stephen L. Graziano, MD; supported by CA21060; Syracuse Hematology-Oncology Assoc. CCOP, Syracuse, NY—Jeffrey Kirshner, MD, supported by CA45389; The Ohio State University Medical Center, Columbus, OH—Clara D. Bloomfield, MD, supported by CA77658; University of Alabama Birmingham, Birmingham, AL—Robert Diasio, MD, supported by CA47545; University of California at San Diego, San Diego, CA—Stephen L. Seagren, MD, supported by CA11789; University of California at San Francisco, San Francisco, CA—Alan P. Venook, MD, supported by CA60138; University of Chicago Medical Center, Chicago, IL —Gini Fleming, MD, supported by CA41287; University of Illinois Missouri Baptist Community Clinical Oncology Program, Chicago, IL—Lawrence E. Feldman, MD, supported by CA74811; University of Iowa Hospitals— Iowa City, IA—Gerald Clamon, MD; supported by CA47642; University of Maryland Greenebaum Cancer Center, Baltimore, MD—Martin Edelman, MD, supported by CA31983; University of Massachusetts Medical Center, Worcester, MA—F. Marc Stewart, MD; supported by CA37135; University of Minnesota, Minneapolis, MN—Bruce Peterson MD; supported by CA16450; University of Missouri/Ellis Fischel Cancer Center, Columbia, MO—Michael C Perry, MD, supported by CA12046; University of Nebraska Medical Center, Omaha, NE—Anne Kessinger, MD, supported by CA77298; University of North Carolina at Chapel Hill, Chapel Hill, NC—Thomas C. Shea, MD, supported by CA47559; University of Tennessee Memphis, Memphis, TN—Harvey B. Niell, MD, supported by CA47555; University of Texas Southwestern Medical Center, Dallas, TX—Debasish Tripathy, MD; Vermont Cancer Center, Burlington, VT—Hyman B. Muss, MD, supported by CA77406; Wake Forest University School of Medicine, Winston-Salem, NC—David D Hurd, MD, supported by CA03927; Walter Reed Army Medical Center, Washington, DC—Joseph J. Drabeck, MD, supported by CA26806; Washington University School of Medicine — St. Louis, MO—Nancy Bartlett, MD; supported by CA77440; Weill Medical College of Cornell University, New York, NY—Michael Schuster, MD; supported by CA07968. All support grants are Public Health Service grants from the National Cancer Institute, National Institutes of Health, Department of Health and Human Services.
The authors indicated no potential conflicts of interest.
We thank Carrie E. Blackstock, PhD, University of North Carolina, Chapel Hill, NC, for her editorial support.
Supported in part by Public Health Service Grant No. CA31946 from the National Cancer Institute (NCI), National Institutes of Health, Department of Health and Human Services, to the Cancer and Leukemia Group B (Richard L. Schilsky, MD, Chairman). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the NCI. Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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Copyright © 2006 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
2 and Fisher’s exact tests. The Cox proportional hazards model was used to compute relative risk ratios for African Americans versus non–African Americans and to assess simultaneously and control for the confounding influence of other prognostic covariables.
