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Originally published as JCO Early Release 10.1200/JCO.2008.21.1532 on March 23 2009 © 2009 American Society of Clinical Oncology.
Disparities in Breast Cancer Adjuvant Chemotherapy: Moving Beyond Yes or NoDana-Farber Cancer Institute, Boston, MA
University of Michigan, Ann Arbor, MI The use of chemotherapy in the treatment of selected types of early breast cancer has been endorsed as a measure of high-quality care by numerous professional organizations and investigators.1–3 Racial disparities in breast cancer survival rates may result in part from disparities in the use and quality of curative therapies, particularly adjuvant systemic therapy. Practice patterns in the delivery of adjuvant chemotherapy that may contribute to disparities in breast cancer outcomes include underuse (ie, not providing adjuvant chemotherapy when it is indicated) and misuse (ie, providing adjuvant chemotherapy with delivery of nonstandard regimens or doses).4 Underuse is relatively easy to identify; several investigators have demonstrated underuse of adjuvant chemotherapy in black patients compared with white patients in clinical5 and population-based samples.6 Misuse is harder to recognize because administrative and other databases do not usually include detailed information on chemotherapy drugs, doses, or time to completion of treatment, and collecting such information is labor intensive and challenging.3 Studying disparities in the quality of chemotherapy is additionally complicated by the fact that many databases are missing self-reported race information. Previous studies addressing racial and socioeconomic disparities in the quality of adjuvant systemic therapy administration have demonstrated disparities in selection of chemotherapy regimens,7 selection of chemotherapy doses in the initial course of chemotherapy,8,9 dose reductions in the course of chemotherapy,10 prolonged time to chemotherapy completion,11 and termination of chemotherapy before completion of all planned cycles.9 One might expect that the receipt of standardized care through participation in clinical trials would reduce racial disparities in breast cancer treatment. In this issue of Journal of Clinical Oncology, Hershman et al12 challenge this expectation by investigating racial differences in the adjuvant chemotherapy administered to patients participating in two adjuvant trials, S8814 and S8897, led by the Southwest Oncology Group (SWOG). In both black and white women, 43% of patients had a relative dose intensity < 0.85 (a relative dose intensity of 1.0 indicates delivery of full doses without any delays in treatment). Black women were more likely to discontinue treatment before completion of all courses or experience a delay in chemotherapy than were white women (87% v 81%; P = .04), and they were more likely to miss appointments than were white women (19% v 9%; P = .0002). These patterns of care did not result in a difference in the mean relative dose intensity (0.87 in black women and 0.88 in white women). Although WBC and absolute neutrophil counts were lower in black women, myelosuppression did not account for early cessation of or delays in treatment. Similarly, other documented adverse effects of treatment were no more common among black women than in white women. Remarkably, relative dose intensity was not independently associated with progression-free or overall survival. However, as Hershman et al point out, the study may not have had sufficient power to detect a difference in outcome according to relative dose intensity. The importance of a full course of therapy may also be limited to certain groups of women, such as younger women,13 women with estrogen receptor–negative disease,14 and women with human epidermal growth factor receptor 2–positive disease.15 Although it is reassuring that Hershman et al12 found no racial disparities in relative dose intensity, their findings obviously do not address the issue of underuse of adjuvant systemic therapy in black women. Moreover, the finding that relative dose intensity did not account for the differences in outcomes does not mean that the racial differences described by Hershman et al—that black women were more likely to discontinue treatment early and experience delays in therapy—are unimportant. In fact, the results presented by Hershman et al reinforce previous findings that racial differences exist in the quality of breast cancer adjuvant chemotherapy and demonstrate that even in the standardized treatment setting afforded by a clinical trial, patients face obstacles to optimal therapy. It is sobering that despite our hope that patients who participate in clinical trials receive the highest quality care, participation alone does not guarantee treatment is delivered as designed. Clearly, there is room for improvement in the delivery of adjuvant chemotherapy to patients both on and off clinical trials. The article by Hershman et al also raises important questions about the relative impact of biology and the underuse and misuse of chemotherapy on the outcomes of patients with breast cancer and the mechanisms through which race influences patterns of care. Attempts to disentangle the relationship between race and socioeconomic status in breast cancer outcomes have generally found that disparities in outcomes are partially explained by, or mediated through, socioeconomic status.16–18 Given the higher rates of poverty and lack of insurance among black women,19,20 it is possible that socioeconomic factors not measured by Hershman et al12 played a role in delays in and early termination of treatment. We speculate that black women receiving chemotherapy may have more difficulty arranging child care, securing flexibility at work, and affording prescription medications to control adverse effects of chemotherapy.21,22 Well-documented differences in the quality of communication between patients and physicians23 may also impede effective navigation of chemotherapy and its adverse effects as well as communication about the purpose of treatment and the importance of receiving a full course of therapy. Hershman et al12 are to be commended for investigating actual doses of chemotherapy delivered, delays in completion of therapy, and cessation of therapy. Many clinical trials do not report the dose intensity received by trial participants,24 so it is not possible to compare the delivery of chemotherapy in these SWOG trials with that in other clinical trials. Previous research on patients with cancer treated outside of clinical trials has revealed that many do not achieve the recommended relative dose intensity of 0.85.3,25 For example, in one study25 of 20,799 patients treated in community settings, 55% of patients did not achieve a relative dose intensity of 0.85. In another study3 of 1,287 patients, 42% of patients received chemotherapy doses substantially lower than those in published regimens. This number is strikingly similar to the 43% of women who received chemotherapy with a relative dose intensity < 0.85 in the SWOG studies described by Hershman et al. Hershman et al12 have added to a body of literature indicating that we need to broaden our concept regarding the quality of chemotherapy given in the adjuvant setting. All chemotherapy is not created equal. In addition to measuring underuse, we must also assess misuse, including selection of nonstandard regimens or doses, and early cessation of therapy. Moreover, we must continue to evaluate the impact of race, ethnicity, and socioeconomic status on the administration of high-quality therapy. Identifying measures that extend beyond merely the receipt of indicated chemotherapy will bring us closer to supporting patients and physicians in achieving optimal care. Several strategies for improving the quality of care delivered to underserved and disadvantaged populations currently under investigation, such as those in the Patient Navigation Research Program26 funded by the National Cancer Institute, offer reason for hope. Other systems for identifying gaps in quality, such as the development of electronic mechanisms for monitoring the quality of care delivered to diverse patient groups,27 may likewise lead to improvements in the quality of care and outcomes. Only through these efforts will it be possible to identify points of derailment from high-quality care and design remedies that improve care for all of our patients. AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST The author(s) indicated no potential conflicts of interest. AUTHOR CONTRIBUTIONS Conception and design: Michael J. Hassett, Jennifer J. Griggs Manuscript writing: Michael J. Hassett, Jennifer J. Griggs Final approval of manuscript: Michael J. Hassett, Jennifer J. Griggs REFERENCES 1. Hassett MJ, Hughes ME, Niland JC, et al: Selecting high priority quality measures for breast cancer quality improvement. Med Care 46:762–770, 2008.[Medline] 2. American Society of Clinical Oncology. http://www.asco.org. 3. Malin JL, Schneider EC, Epstein AM, et al: Results of the National Initiative for Cancer Care Quality: How can we improve the quality of cancer care in the United States? J Clin Oncol 24:626–634, 2006. 4. Hewitt M, Simone JV. Ensuring Quality Cancer Care. Washington, DC: National Academies Press, 1999. 5. Bickell NA, Wang JJ, Oluwole S, et al: Missed opportunities: Racial disparities in adjuvant breast cancer treatment. J Clin Oncol 24:1357–1362, 2006. 6. Li CI, Malone KE, Daling JR: Differences in breast cancer stage, treatment, and survival by race and ethnicity. Arch Intern Med 163:49–56, 2003. 7. Griggs J, Culakova E, Sorbero ME, et al: Social and racial differences in selection of breast cancer adjuvant chemotherapy regimens. J Clin Oncol 25:2522–2527, 2007. 8. Griggs JJ, Culakova E, Sorbero ME, et al: Effect of patient socioeconomic status and body mass index on the quality of breast cancer adjuvant chemotherapy. J Clin Oncol 25:277–284, 2007. 9. Griggs JJ, Sorbero MES, Stark AT, et al: Racial disparity in the dose and dose intensity of breast cancer adjuvant chemotherapy. Breast Cancer Res Treat 81:21–31, 2003.[CrossRef][Medline] 10. Smith K, Wray L, Klein-Cabral M, et al: Ethnic disparities in adjuvant chemotherapy for breast cancer are not caused by excess toxicity in black patients. Clin Breast Cancer 6:260–266, 2005 discussion 267-269.[Medline] 11. Hershman D, Weinberg M, Rosner Z, et al: Ethnic neutropenia and treatment delay in African American women undergoing chemotherapy for early-stage breast cancer. J Natl Cancer Inst 95:1545–1548, 2003. 12. Hershman DL, Unger JM, Barlow WE, et al: Treatment quality and outcomes of African American versus white breast cancer patients: Retrospective analysis of Southwest Oncology Studies S8814/S8897. J Clin Oncol 13:2157–2162, 2009. 13. Colleoni M, Litman HJ, Castiglione-Gertsch M, et al: Duration of adjuvant chemotherapy for breast cancer: A joint analysis of two randomised trials investigating three versus six courses of CMF. Br J Cancer 86:1705–1714, 2002.[CrossRef][Medline] 14. Colleoni M, Li S, Gelber RD, et al: Relation between chemotherapy dose, oestrogen receptor expression, and body-mass index. Lancet 366:1108–1110, 2005.[CrossRef][Medline] 15. Thor AD, Berry DA, Budman DR, et al: erbB-2, p53, and efficacy of adjuvant therapy in lymph node-positive breast cancer. J Natl Cancer Inst 90:1346–1360, 1998. 16. Bradley CJ, Given CW, Roberts C: Race, socioeconomic status, and breast cancer treatment and survival. J Natl Cancer Inst 94:490–496, 2002. 17. Cross CK, Harris J, Recht A: Race, socioeconomic status, and breast carcinoma in the U.S: What have we learned from clinical studies. Cancer 95:1988–1999, 2002.[CrossRef][Medline] 18. Newman LA, Mason J, Cote D, et al: African-American ethnicity, socioeconomic status, and breast cancer survival: A meta-analysis of 14 studies involving over 10,000 African-American and 40,000 White American patients with carcinoma of the breast. Cancer 94:2844–2854, 2002.[CrossRef][Medline] 19. US Census Bureau. http://www.census.gov/population/www/socdemo. 20. Ward E, Halpern M, Schrag N, et al: Association of insurance with cancer care utilization and outcomes. CA Cancer J Clin 58:9–31, 2008. 21. Cobaugh DJ, Angner E, Kiefe CI, et al: Effect of racial differences on ability to afford prescription medications. Am J Health Syst Pharm 65:2137–2143, 2008. 22. Magai C, Consedine NS, Adjei BA, et al: Psychosocial influences on suboptimal adjuvant breast cancer treatment adherence among African American women: Implications for education and intervention. Health Educ Behav 2007. 23. Siminoff LA, Graham GC, Gordon NH: Cancer communication patterns and the influence of patient characteristics: Disparities in information-giving and affective behaviors. Patient Educ Couns 62:355–360, 2006.[CrossRef][Medline] 24. Dale DC, McCarter GC, Crawford J, et al: Myelotoxicity and dose intensity of chemotherapy: Reporting practices from randomized clinical trials. J Natl Compr Cancer Netw 1:440–454, 2003. 25. Lyman GH, Dale DC, Crawford J: Incidence and predictors of low dose-intensity in adjuvant breast cancer chemotherapy: A nationwide study of community practices. J Clin Oncol 21:4524–4531, 2003. 26. Freund KM, Battaglia TA, Calhoun E, et al: National Cancer Institute Patient Navigation Research Program: Methods, protocol, and measures. Cancer 113:3391–3399, 2008.[CrossRef][Medline] 27. Bickell NA, Shastri K, Fei K, et al: A tracking and feedback registry to reduce racial disparities in breast cancer care. J Natl Cancer Inst 100:1717–1723, 2008.
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Copyright © 2009 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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