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Journal of Clinical Oncology, Vol 24, No 9 (March 20), 2006: pp. 1357-1362 © 2006 American Society of Clinical Oncology. DOI: 10.1200/JCO.2005.04.5799 Missed Opportunities: Racial Disparities in Adjuvant Breast Cancer Treatment
From the Department of Health Policy, Mount Sinai School of Medicine; Department of Surgery, Harlem Hospital Center, Columbia University College of Physicians and Surgeons; Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center; Department of Surgery, North General Hospital; Department of Surgery, Bellevue Hospital and New York University School of Medicine; Department of Surgery, Metropolitan Hospital Center; Department of Surgery, New York University School of Medicine, New York, NY Address reprint requests to Nina A. Bickell, MD, MPH, Mount Sinai School of Medicine, 1 Gustave L. Levy Place, Box 1077, New York, NY 10029; e-mail: nina.bickell{at}mssm.edu
PURPOSE: Underuse of adjuvant therapy is a potentially important and remediable explanation for the inferior survival of minority women with breast cancer. We sought to measure a racial disparity in the underuse of adjuvant treatments for early-stage breast cancer and to identify associated factors.
METHODS: Cross-sectional study with review of all inpatient and outpatient medical records of 677 women treated surgically for a primary American Joint Committee on Cancer stage I or II breast cancer in 1999 to 2000. Underuse was defined as omissions of radiation therapy after breast-conserving surgery, adjuvant chemotherapy after resection of hormone-receptor-negative tumors RESULTS: One hundred forty-five (21%) of 677 women experienced underuse of appropriate adjuvant therapy: 16% in whites, 34% in blacks, and 23% in Hispanics (P < .001). Women referred to medical oncologists were less likely to experience underuse of necessary adjuvant treatments (relative risk [RR] for underuse = 0.2; 95% CI, 0.1 to 0.3). Women who were minorities (RR = 2.0; 95% CI, 1.3 to 3.1), had higher levels of comorbidity (RR = 1.4; 95% CI, 1.1 to 1.8) and lacked insurance (RR = 1.9; 95% CI, 0.9 to 4.0) were at greater risk for underuse. CONCLUSION: Minority women with early-stage breast cancer have double the risk of white women for failing to receive necessary adjuvant treatments despite rates of oncologic consultation similar to those for white women. Oncology referrals are necessary to reduce treatment disparities but are not sufficient to ensure patients' receipt of efficacious adjuvant treatment.
Despite lower incidence rates of breast cancer, black women are more likely than white women to die of the disease.1 Much of the racial disparity in breast cancer mortality has been attributed to later stage at diagnosis. Yet, even within stage categories, mortality rates are higher for minority women.2-4 One potential explanation for racial disparities is the underuse of adjuvant treatment strategies that have been demonstrated to improve disease-free and overall survival in large randomized trials.4-9 Available studies suggest that utilization varies considerably. However, few characterize the reasons for this variation or include large numbers of nonwhite women. Information about disparities in adjuvant treatment is sparse because measurement of utilization is especially challenging.5,10 Many analyses rely on claims data, which only permit limited insight regarding the reasons for underuse.11-13 Although tumor registries capture the details of hospital-based treatments including surgery (and to a lesser extent radiotherapy) with some reliability, they do not reliably capture systemic or hormonal therapy which are typically delivered in outpatient settings.10,11 Comprehensive medical record reviews are resource intensive to conduct and typically require acquisition of data from multiple providers. For example, because hormonal therapies such as tamoxifen can be provided by any licensed physician, determining whether or not they were administered requires either patient interview or comprehensive record review of all provider encounters. The challenge inherent in accurately assessing treatments provided in ambulatory settings has hindered detailed specification of the extent to which the underuse of adjuvant treatment is an important contributor to racial disparities in breast cancer outcomes. We undertook a medical record review of New York City women who received primary surgery for early-stage breast cancer at one of six sites that serve a high proportion of black, Hispanic, and poor patients. By acquiring comprehensive medical records from hospitals, outpatient clinics, and private physicians' offices, we sought to measure the underuse of efficacious adjuvant treatment among women by race and ethnicity, and to identify the mechanisms that contribute to underuse.
Case Ascertainment Structured review of inpatient and outpatient medical records for women diagnosed with early-stage breast cancer (American Joint Committee on Cancer stages I and II) in 1999 and 2000 was performed at six New York City hospitals. These institutions included three municipal, two tertiary referral centers, and one community hospital. Of the 1,277 women identified from pathology and tumor registries, 600 women were not eligible because of recurrent cancer (28%), in situ carcinoma (34%), late stage disease (17%), and primary surgical treatment performed at a nonparticipating hospital (21%). Six hundred seventy-seven women with an initial primary stage I or II breast cancer undergoing a definitive surgical treatment at one of the participating hospitals between 1999 and 2000 were included in the final study population.
Specification of Efficacious Therapy
Medical Record Abstraction The institutional review boards of the six participating hospitals approved the study protocol and medical record abstraction tool.
Statistical Analyses Logistic models assessing the underuse of radiotherapy among women with breast-conserving surgery, of chemotherapy among women with greater than stage IA hormone-receptor-negative cancer, and of hormonal therapy among women with greater than stage IA hormone-receptor-positive cancer were run. Because the independent factors in each of these models were similar, a single model assessing risk of the underuse of beneficial adjuvant therapy was run using the population of women who should have gotten additional therapy as per the guidelines. As chemotherapy is usually prescribed by oncologists and may represent an intermediate variable, the same model was run excluding women with hormone-receptor-negative tumors. Because the findings were no different, we report the model for the larger population.
The study population consisted of 677 women, of whom 332 (49%) were white. Table 1 describes the study population's characteristics. On average, the study's women were 59.7 years old; Hispanic women tended to be younger and white women tended to be older (P < .05). Ninety-three percent had health insurance. Black and Hispanic women were more likely to have Medicaid or be uninsured, as compared with white women. They were also more likely to have comorbidities than white and Asian women. Within early-stage breast cancer, black and Hispanic women were more likely to present with more advanced disease and were more likely to have hormone-receptor-negative tumors. There was no racial difference in the types of primary surgical treatments performed for breast cancer; however, white women were more likely than minority women to undergo a sentinel-node biopsy.
Underuse of Adjuvant Therapies There were racial disparities in the three adjuvant therapies assessed: receipt of radiotherapy following breast-conserving surgery, chemotherapy for hormone-receptor-negative tumors, and hormonal therapy for hormone-receptor-positive tumors (Table 2). Among the 396 women who underwent breast-conserving surgery, black women were significantly less likely to obtain radiation (73% v 84%; P < .0001). Among the 126 women with greater than stage IA hormone-receptor-negative tumors, black women were less likely to receive chemotherapy (67% v 78%; P < .01). Among the 421 women with greater than stage IA hormone-receptor-positive tumors, black and Hispanic women were less likely to receive hormonal therapy (71% and 75%, respectively, v 80%; P < .05). There were 177 episodes of underuse among 145 women. The likelihood of underuse of an efficacious adjuvant therapy in a woman with newly diagnosed early-stage breast cancer was 21% overall; 16% among whites, 23% among Hispanics, and 34% among black women.
Referral to Medical Oncology Referral to an oncologist was associated with a greater likelihood of receiving adjuvant therapy (P < .0001). Among women who could benefit from systemic treatment (> stage IA), the vast majority of patients (82%; 388 of 473) referred to a medical oncologist received adjuvant systemic treatments, as compared with 32% of women (24 of 74) with no such referral. There was no racial disparity in referral to an oncologist among women with greater than stage IA tumor: 85% of whites, 85% of blacks, and 90% of Hispanics were referred (P = not significant). Women with a greater than stage IA tumor referred to medical oncology were much more likely to be younger (mean age, 57 years v 69 years; P < .0001), have no comorbidities (80% v 70%; P = .05), have commercial insurance (49% v 24%; P < .0001), and have stage II cancer (56% v 39%; P < .01) than those women who were not referred. Among women with greater than stage IA who did not see a medical oncologist (n = 74), there was a racial difference in receipt of adjuvant therapy. White women were significantly more likely to undergo treatment than black or Hispanic women (56% v 5% and 22%, respectively; P < .001). Among women with a greater than stage IA tumor who did see a medical oncologist, there was not a statistically significant difference in receipt of adjuvant therapy among the racial-ethnic groups (85% in whites, 75% in blacks, 81% in Hispanics; P = .18); however, black women were more likely to experience underuse than nonblack women (25% v 16%; P < .05). Multivariate logistic analysis revealed that black and Hispanic women were more than twice as likely to experience underuse of beneficial adjuvant therapies after taking into account important clinical (stage, comorbidity), demographic (age), and access factors (insurance, referral to medical oncologist; Table 3). Referral to a medical oncologist was associated with a reduced chance of underuse of necessary adjuvant treatments, regardless of whether the oncologist provided that treatment (eg, radiotherapy). The presence of a comorbid condition was associated with a greater chance of underuse of adjuvant therapy. Women 70 years and older were not less likely than younger women to experience underuse.
In a large sample of women diagnosed with breast cancer in New York City where multidisciplinary breast cancer providers are plentiful, we found evidence of a large disparity in the rates at which white versus minority women received appropriate adjuvant therapy. Specifically, we found evidence of underuse of one or more efficacious adjuvant treatment strategies for 16% of white women, 34% of black women, and 23% of Hispanic women. Our finding of one in three black women of our study, and nearly one in four Hispanic women, highlights just how much progress could be made to eliminate cancer death and suffering by closing the gap on racial disparities in breast cancer treatment. For white women, there was evidence of underuse for one in six women, suggesting that across the spectrum of race, there are frequent missed opportunities to optimize outcomes. Adjuvant therapies are an integral component of the management of early-stage breast cancer. Large prospective randomized controlled trials demonstrate that adjuvant systemic chemotherapy for women with hormone-receptor-negative disease and adjuvant hormonal therapy for women with hormone-receptor-positive disease each improve disease-free and overall survival.17,18 To a great extent, dissemination of these treatment strategies has contributed to the improvement in stage-specific survival following breast cancer diagnosis since the 1980s. Radiation following breast-conserving surgery is also an important treatment because it decreases the chance of local recurrence.19,20 Each of these adjuvant treatments has been recommended as part of national practice guidelines since the early 1990s.21,22 They are frequently considered as metrics for evaluating the quality of cancer care. Numerous studies have documented inferior survival among minority women with breast cancer.3,5-7,22,23 However, specification of the reasons for this persistent phenomenon have been more elusive. In part, worse outcomes for nonwhite women are due to greater disease severity and later stage at diagnosis,1,2,22 and indeed we observed that black and Hispanic women were more likely to present with larger tumors or more adverse prognostic features than white women. However, the primary explanations for observed racial differences in survival after cancer diagnosis have been (1) that there are disparities in the utilization of effective treatments4,8,23; and (2) that the burden of comorbid illness is higher in nonwhite populations.24,25 Despite the widespread assumption of a racial disparity in treatment contributing to minority women's worse survival, there have been sparse data to support this belief and little information to explain the mechanisms underlying this pattern. Previous studies relying on cancer registry data from the Surveillance, Epidemilogy, and End Results (SEER) program have suggested racial disparity in adjuvant treatment but have been hampered by the limited information about systemic treatments recorded by hospital-based tumor registries. Analyses of SEER registry data linked to Medicare claims have delineated treatment utilization for elderly women and also suggest a disparity, but hormonal treatments such as tamoxifen may be inconsistently coded in Medicare claims.11 By conducting a comprehensive medical record review and accessing the outpatient office records we were able to measure treatment rates in a large multiracial multiethnic urban cohort. In our urban cohort where breast cancer providers were plentiful during the years of our study, it is implausible to consider that insufficient provider availability is an important contributor to underuse. Why do minority women who have successfully accessed the care system to obtain surgical treatment so frequently go on to receive suboptimal adjuvant treatment? We can shed some light on reasons for treatment disparities. The presence of comorbidities and lack of insurance explains part of the underuse. Black and Hispanic women had significantly more comorbidities and less insurance than white women, which might affect a physician's decision to prescribe and a patient's decision and ability to receive these treatments. In this New York City population, access and insurance barriers cannot fully explain these disparities because all of the hospitals accept the insurance and all uninsured patients were able to receive care. Indeed, controlling for these risk factors does not erase the effect of race on the risk of treatment omission. Based on preliminary work26,27 and conversations with surgeons, medical, and radiation oncologists, we anticipated that women who did not receive appropriate adjuvant treatment would make these decisions without having the benefit of an oncology consultation. Practically, this finding would suggest the importance of postoperative intervention and facilitation of access to oncology consultations by breast surgeons and their support teams. Indeed, for 14% of all women, despite an exhaustive review of multisite medical records, there was no evidence that an oncology consultation ever took place. Among women without an oncologic referral, white women were much more likely to receive adjuvant treatments. This finding suggests that despite lack of medical oncology input, either white women were more aware of, receptive to, or able to receive hormonal and radiotherapies. Alternatively, their surgeons or primary care physicians may have been more likely to prescribe hormonal therapies and ensure connection with radiation oncology. Among women of all races who did not receive adjuvant treatment, the majority did so despite undergoing oncology consultation. These findings have practical implications for quality improvement initiatives and specify key leverage points. For all women recovering from primary surgery for early-stage breast cancer, particularly minority women, it is critical to ensure that triage to medical oncology is successfully accomplished. Reducing such missed opportunities to facilitate oncology connections and enabling receipt of appropriate adjuvant therapy has the potential to reduce racial disparities in treatment.28 However, undergoing oncologic evaluation does not appear sufficient, because despite medical oncology consultation, a substantial proportion of women still do not embark on a course of appropriate therapy. Special attention and in-depth discussion of the risks and benefits of adjuvant treatment may provide reinforcement necessary for a woman to embark on therapy. Understanding the different approaches used by oncologists to encourage adherence to adjuvant treatment should inform the design of interventions to reduce underuse. Ongoing patient interviews conducted by our research team and by other investigators (eg, National Initiative on Cancer Care Quality) will need to adopt anthropological methods so as to evaluate interactions between medical oncologists and patients that are and are not successful. However, until such mechanisms are more precisely elucidated, heightened awareness of this phenomenon among oncologists may itself encourage special attention to adjuvant treatment conversations. Logical approaches may include encouraging patients to bring a supportive care provider, providing written materials in advance of appointments, providing a written recommendation at the appointment, encouraging questions about patients' concerns regarding treatment risks and benefits as well as their physical, emotional, and financial ability to undergo treatment. Professional societies like the American Society of Clinical Oncology and the American Board of Internal Medicine, which focus on physician credentialing, are developing physician self-assessment tool kits to help doctors hone their communication skills. For oncologists, evaluation and critique of important adjuvant conversations by peers may be an effective strategy to improve these encounters and thereby improve the quality of breast cancer care. This study is limited in that patient race is based on chart documentation. The six participating hospitals are all located in the New York City area, thereby limiting the generalizability. It is possible that rates of underuse are slightly overestimated and rates of oncology referral slightly underestimated due to poor documentation, abstractor error, or inability to locate the source of treatment. However, we believe this number to be small since many more physician offices than the 187 physician offices that ultimately provided treatment data were consulted to identify possible sources of treatment information. Another study using similar methodology incorrectly classified 8% of the total cases as underuse due to errors in chart abstraction.29 As surgeons with only one breast cancer case did not have different rates of underuse than high volume surgeons, it is unlikely that surgeon workload or practice patterns affected underuse rates. The proportion of white patients treated at half the study hospitals was minimal, making it impossible to disentangle the effects of the hospital from those of race. All six hospitals are located within approximately 5 miles of one another so that distance to the hospital is unlikely to deter women in their choice of hospital. We are unable to determine from this chart review why a woman chose to undergo surgery at a particular hospital. The reasons underlying this choice may be related to subsequent decisions regarding adjuvant treatment. Medical record review precludes definitive determination of whether the decision to forego treatment was initiated by the physician withholding or discouraging adjuvant therapy or the patient's own reluctance to undergo this treatment. In conclusion, we found that minority women with early-stage breast cancer are more likely than white women to experience underuse of proven effective local and systemic treatments. Such treatment differences may explain in part the poorer survival experienced by minority women. Oncologic referral confers protection against underuse. Instituting a required oncology consultation may reduce racial disparities in care, but our findings suggest it will not suffice. Improving the overall quality of early-stage breast cancer care will require elucidating and addressing both patient and physician barriers to, expectations of, and communications about adjuvant therapy.
The authors indicated no potential conflicts of interest.
We thank all the physicians and their staff who kindly opened their office practices to our abstractors.
Supported by the AHRQ (Grant No. P-01HS10859-02), Commonwealth Fund (Grant No. 20010102), and NCMHHD (Grant No. P60 MD00270). Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.
1. Weir HK, Thus MJ, Hankey BF, et al: Annual report to the nation on the status of cancer, 1975-2000, featuring the uses of surveillance data for cancer prevention and control. J Natl Cancer Inst 95:1276-1299, 2003 2. Shavers VL, Harlan LC, Stevens JL: Racial/ethnic variation in clinical presentation, treatment, and survival among breast cancer patients under age 35. Cancer 97:134-147, 2003[CrossRef][Medline] 3. Chu KC, Lamar CA, Freeman HP: Racial disparities in breast carcinoma survival rates: Separating factors that affect diagnosis from factors that affect treatment. Cancer 97:2853-2860, 2003[CrossRef][Medline] 4. Shavers VL, Brown ML: Racial and ethnic disparities in the receipt of cancer treatment. J Natl Cancer Inst 94:334-357, 2002 5. Moormeier J: Breast cancer in black women. Ann Intern Med 124:897-905, 1996 6. Joslyn SA: Racial differences in treatment and survival from early-stage breast carcinoma. Cancer 95:1759-1766, 2002[CrossRef][Medline] 7. 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 8. Griggs JJ, Sorbero ME, 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] 9. Mandelblatt JS, Kerner JF, Hadley J, et al: Variations in breast carcinoma treatment in older Medicare beneficiaries: Is it black and white? Cancer 95:1401-1414, 2002[CrossRef][Medline] 10. Bickell NA, Chassin MR: Determining the quality of breast cancer care: Do tumor registries measure up? Ann Intern Med 132:705-710, 2000 11. Du XL, Key CR, Osborne C: Community-based assessment of adjuvant hormone therapy in women with breast cancer, 1991-1997. Breast J 10:433-439, 2004[Medline] 12. Malin JL, Schuster MA, Kahn KA, et al: Quality of breast cancer care: What do we know? J Clin Oncol 20:4381-4393, 2002 13. Elmore JG, Nakano CY, Linden HM, et al: Racial inequities in the timing of breast cancer detection, diagnosis, and initiation of treatment. Med Care 43:141-148, 2005[CrossRef][Medline] 14. Carlson RW, Anderson BO, Bensinger W, et al: National Comprehensive Cancer Network: NCCN Practice Guidelines for Breast Cancer. Oncology (Williston Park) 14:33-49, 2000 15. Charlson ME, Pompei P, Ales KL, et al: A new method of classifying prognostic comorbidity in longitudinal studies: Development and validation. J Chronic Dis 40:373-383, 1987[CrossRef][Medline] 16. Yancik R, Wesley MN, Ries LA, et al: Effect of age and comorbidity in postmenopausal breast cancer patients aged 55 years and older. JAMA 285:885-892, 2001 17. Early Breast Cancer Trialists' Collaborative Group (EBCTCG): Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: An overview of the randomised trials. Lancet 365:1687-1717, 2005[CrossRef][Medline] 18. Early Breast Cancer Trialists' Collaborative Group.Tamoxifen for early breast cancer [Cochrane Database System Review]. Oxford, United Kingdom, The Cochrane Library, 2003 19. Early Breast Cancer Trialists' Collaborative Group: Favourable and unfavourable effects on long-term survival of radiotherapy for early breast cancer: An overview of the randomised trials. Lancet 355:1757-1770, 2000[CrossRef][Medline] 20. Early Breast Cancer Trialists' Collaborative Group. Radiotherapy for early breast cancer [Cochrane Database System Review]. Oxford, United Kingdom, The Cochrane Library, 2003 21. National Institutes of Health Consensus Development Panel: National Institutes of Health Consensus Development Conference statement: Adjuvant therapy for breast cancer, November 1-3, 2000. J Natl Cancer Inst Monogr (30):5-15, 2001[Medline] 22. NIH consensus conference: Treatment of early-stage breast cancer. JAMA 265:391-395, 1991 23. Eley JW, Hill HA, Chen VW, et al: Racial differences in survival from breast cancer: Results of the National Cancer Institute Black/White Cancer Survival Study. JAMA 272:947-954, 1994 24. Bigby J, Holmes MD: Disparities across the breast cancer continuum. Cancer Causes Control 16:35-44, 2005[CrossRef][Medline] 25. Tammemagi CM, Nerenz D, Neslund-Dudas C, et al: Comorbidity and survival disparities among black and white patients with breast cancer. JAMA 294:1765-1772, 2005 26. Bach PB, Schrag D, Brawley OW, et al: Survival of blacks and whites after a cancer diagnosis. JAMA 287:2106-2113, 2002 27. Bickell NA, Aufses AH Jr, Chassin MR: The quality of early-stage breast cancer care. Ann Surg 232:220-224, 2000[CrossRef][Medline] 28. Bickell NA, Young GJ: Coordination of care for early-stage breast cancer patients. J Gen Intern Med 16:737-742, 2001[CrossRef][Medline] 29. Bickell NA, McEvoy MD: Physicians' reasons for failing to deliver effective breast cancer care: A framework for underuse. Med Care 41:442-446, 2003[CrossRef][Medline] Submitted October 12, 2005; accepted December 29, 2005.
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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
1 cm, or hormonal therapy for receptor-positive tumors 
2 tests for categoric, t tests for continuous bivariate comparisons, and logistic models for multivariable assessments. Insurance was analyzed initially by type: Medicaid, Medicare, commercial, and no insurance. As no differences emerged among the insured groups, the categories were collapsed into a dichotomous insured versus uninsured variable. Age was run as a continuous variable and then dichotomized at age 70 years because the majority of trials assessing treatment efficacy were conducted in women younger than 70 years old.
