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Originally published as JCO Early Release 10.1200/JCO.2006.08.3063 on December 11 2006 © 2007 American Society of Clinical Oncology. Effect of Patient Socioeconomic Status and Body Mass Index on the Quality of Breast Cancer Adjuvant Chemotherapy
From the Department of Medicine, University of Rochester, Rochester, NY; RAND Corporation, Pittsburgh, PA; University of Washington, Seattle, WA; Duke Comprehensive Cancer Center and the Department of Medicine, Duke University, Durham, NC Address reprint requests to Jennifer J. Griggs, MD, MPH, Department of Medicine, Hematology/Oncology, University of Michigan, 1500 East Medical Center Dr, 4310 CCGC, Ann Arbor, MI 48109-0936; e-mail: JenGrigg{at}umich.edu
PURPOSE: The purpose of this study was to investigate the relationship between socioeconomic status (SES) and the use of intentionally reduced doses of chemotherapy in the adjuvant treatment of breast cancer. PATIENTS AND METHODS: Patients with breast cancer treated with a standard chemotherapy regimen (n = 764) were enrolled in a prospective registry after signing informed consent. Detailed information was collected on patient, disease, and treatment, including chemotherapy doses. Zip code level data on median household income, proportion of people living below the poverty level, and educational attainment were obtained from the US Census. Doses for the first cycle of chemotherapy lower than 85% of standard were considered to be reduced. Univariate analyses and multivariate logistic regression were performed to identify factors associated with the use of reduced first cycle doses. RESULTS: In univariate analysis, individual education attainment, zip code SES measures, body mass index, and geographic region were all significantly associated with receipt of intentionally reduced doses of chemotherapy. In multivariate analysis, controlling for geography, factors independently associated with reduced doses were obesity (odds ratio [OR], 2.47; 95% CI, 1.36 to 4.51), severe obesity (OR, 4.04; 95% CI, 1.46 to 11.19), and education less than high school (OR, 3.07; 95% CI, 1.57 to 5.99). CONCLUSION: Social disparities in breast cancer outcomes may be in part the result of lower quality chemotherapy doses in the adjuvant treatment of breast cancer. Efforts to address such prescribing patterns may help reduce SES disparities in breast cancer survival.
Breast cancer survival rates are lower among women of lower socioeconomic status (SES) despite the fact that the incidence of breast cancer is lower in disadvantaged women.1-9 Disparities in breast cancer outcome are due to several factors, including more advanced disease in women living in high poverty areas,1,10 a higher likelihood of biologically unfavorable tumor characteristics,11-14 obesity (associated with worse prognosis),15-17 and higher rates of comorbid illnesses.18 Disparities in survival persist, however, independent of these determinants. Consequently, SES disparities in quality of cancer care have received considerable scrutiny. There is evidence that patient SES is associated with type of breast cancer surgery, use of radiation, and use of systemic therapy, with low income women receiving poorer quality of care in all these areas.19-27 The causes of the demonstrated disparities in care are uncertain. It has been hypothesized that patient behavior, choices, or adherence account for the observed variations in care. Alternatively, provider decision making may be influenced by patient nonclinical factors. This study examines provider decisions regarding first chemotherapy dose reductions in order to test the hypothesis that cancer providers are influenced by patient SES in their treatment decision making. The benefit of adjuvant chemotherapy is compromised in patients who do not receive full doses of therapy, and reductions in chemotherapy doses below 85% of the standard doses are ill-advised.28-31 Chemotherapy dose intensity has thus been adopted as a quality measure by the National Initiative for Cancer Care Quality and other groups.32-34 Reduced doses with the first course of therapy are highly correlated with reduced dose and dose intensity for the entire treatment course.35-37 Furthermore, first cycle dose reductions below standard doses represent intentional physician prescribing behavior rather than reductions or delays in chemotherapy doses in response to adverse effects, myelosuppression, or missed appointments. There is ample evidence that many patients do not receive the recommended chemotherapy dose and dose intensity. Only 45% to 78% of patients receive adjuvant chemotherapy at a relative dose intensity of 85% or higher.34,36,38-40 Black race, increasing age, comorbidity, and obesity have all been associated with intentionally reduced doses of chemotherapy for the first course of chemotherapy and overall lower relative dose intensity.36,37,41-43 There has been, however, only one prior published study examining the effect of patient SES on chemotherapy dose.43 This study examines a large geographically dispersed sample of breast cancer patients in order to address the gap in knowledge regarding the impact of patient SES on oncologists' decisions regarding chemotherapy dose reduction.
The data for this study were collected through the Awareness of Neutropenia in Cancer (ANC) Study Group registry, a prospective observational multicenter study of cancer patients starting chemotherapy for nonmyeloid malignancies. The purpose of the ANC Study Group is to study the incidence of chemotherapy-induced neutropenia and the complications thereof. Participants were enrolled at 115 sites within the United States. The ANC study sites were randomly selected after stratification for location and treatment volume. The data collection for this study was conducted March 2002 through March 2005. The study was approved by the University of Rochester Research Subjects' Review Board (Rochester, NY) and by a central institutional review board. All patients signed informed consent. A unique identifier number was created for each participating patient and treatment site. Subject selection. Participating sites enrolled consecutive eligible patients. Subjects were eligible if older than 18 years of age, had histologically confirmed diagnosis of nonmyeloid cancer, and were initiating a new myelosuppressive regimen with at least four planned courses (cycles). This study includes only participants with stages I, II, or III breast cancer who were treated with standard chemotherapy regimens.44 Data collection and measures. Information was collected on subject characteristics through medical record review and patient interview. Characteristics included age, comorbidity using the Charlson Comorbidity Index (CCI),45 performance status, level of education, marital status, occupation, employment status, type of insurance, zip code, height, weight, tumor characteristics, planned and actual chemotherapy received, and dates of treatment. A trained study coordinator at each site performed data abstraction. Data were double entered by a contracted organization. A nurse practitioner and study physician who is also a biostatistician continuously assessed the quality of the data. Area-based socioeconomic measures. The 2000 US Census Bureau American Factfinder web program (http://factfinder.census.gov) was used to obtain information on median household income, racial and ethnic composition, percentage of individuals and households below the poverty level, percentage of individuals with a high school degree, and percentage of individuals with a Bachelor's degree for the zip code of residence for each participant. This information is available in the 2000 Census by zip code tabulation areas (ZCTA). The ZCTA, which approximate census blocks, were created by the US Census Bureau for the 2000 Census. ZCTA are similar but not identical to zip codes. One trained abstractor performed all census data entry, and the data abstraction was repeated for 10% of the patient subjects to confirm accuracy. Chemotherapy dose reductions. The expected dose of each drug was calculated using the standard published doses for each adjuvant chemotherapy regimen and the subject's body-surface area. The body-surface area was calculated using the height and weight in the Mosteller formula.46 For each drug, the planned dose was compared with the actual dose. The ratio of the actual:expected dose was calculated and then averaged to determine the ratio for the regimen as a whole.39 Chemotherapy was considered to be reduced if the ratio of actual:expected was lower than 0.85. For patients treated with a regimen containing cyclophosphamide and doxorubicin, only the doses of cyclophosphamide and doxorubicin were included in the analyses. Body mass index (BMI) was calculated and categorized according to BMI category using the Quatelet index (kg/cm2) and the WHO criteria.47 Age, comorbidity, and BMI were split into clinically meaningful categories for the analysis. Zip code level (census) education data (percentage of high school graduates and percentage of college graduates) were combined into one categoric variable based on the lowest quartiles of the original variables. In addition, age, BMI, and census measures were also evaluated as continuous variables.
Analyses Role of the funding agency. This study was not funded. The data collection was funded by Amgen Inc through the ANC study group. Amgen played no role in the data collection, study design, or interpretation of data.
Subject Characteristics During the study period, 806 participants treated with a standard adjuvant chemotherapy regimen for stage I, II, or III breast cancer were entered onto the registry from 91 practices. (Twenty four of 115 sites did not contribute breast cancer patients to the registry.) The planned doses of chemotherapy were available for 99% of the subjects. The actual doses delivered were available for 93% of the subjects. The planned and actual doses delivered for the first course of therapy were closely correlated with one another (correlation coefficient, 0.99). Of the 806 participants, 35 (4%) were excluded from the analysis of first cycle dose reduction based on a priori selection criteria (see Patients and Methods). Reasons for exclusion included treatment with oral cyclophosphamide (n = 18) and treatment with day 1, day 8 dosing (n = 17). Seven additional subjects (0.8%) were excluded because of missing first cycle dose data. The characteristics of the 764 subjects included in the univariate analysis are shown in Table 1.
Univariate Analysis Region (P < .0001), BMI category (P = .0003), patient education (P = .002), and area-level education (P = .014) were associated with the use of reduced initial doses of chemotherapy (Table 2 and Fig 1). Race was of borderline significance (P = .056). BMI and zip code characteristics differed significantly between those subjects who received a first cycle dose reduction (dose ratio, < 0.85) and those subjects who did not (Table 3). First cycle dose reductions were more commonly administered to heavier patients and to those who lived in zip codes with lower median household income, lower educational attainment, and higher levels of poverty (Table 3). Age, cancer stage, comorbidity, hormone receptor status, and type of insurance were not significantly associated with use of reduced first cycle doses (Table 2). Employment status, occupation, and marital status were also not found to be associated with dose reductions (data not shown).
Multivariate Analysis The multivariate analysis included 737 (96%) of the subjects. Reasons for exclusion were unknown age (n = 1) and zip code that did not correspond to a ZCTA (n = 26). Factors that were independently associated with use of first cycle dose reduction were obesity (P = .003), severe obesity (P = .007), patient education less than high school (P = .001), and geographic region (P < .0001). Severely obese patients were four times as likely to have a dose reduction compared with subjects with normal BMI. Subjects with less than a high school education were three times as likely to have a dose reduction as subjects with at least a high school education. Patients in the southern region were 5.6-fold more likely to have a dose reduction than those in the northeast. Lower median household income was not significant in the final model after adjusting for individual level of education and geographic region but was significant (P = .03) before these two variables were entered into the model. The results of the multivariate analyses are reported as odds ratios, 95% CIs, and P values in Table 4.
In summary, in this large sample of patients treated with breast cancer adjuvant chemotherapy in 91 geographically diverse practices, geographic region, obesity status, and level of education were all independently associated with the administration of intentionally reduced chemotherapy doses. Comorbidity, age, and tumor characteristics were not associated with intentional dose reductions. Geographic variations in patterns of cancer care have been demonstrated in other studies. For example, the use of granulocyte colony-stimulating factor in older women with breast cancer varies according to geography.48 Regional variations have been seen in rates of compliance with locoregional treatment standards in breast cancer,25 rates of breast conserving surgery,49 and in chemotherapy dose intensity.34 In the treatment of prostate cancer, geographic variation in the use of watchful waiting versus surgery or radiation therapy has been described.50 Our finding of geographic variations in chemotherapy dosing suggests that physicians practice within a local treatment culture that either endorses or discourages full doses of chemotherapy.51 It is not possible to discern whether there are individual physician effects as opposed to regional effects, but nonetheless, our results offer a heretofore unexplored explanation for documented geographic variations in breast cancer survival.52-54 The use of reduced chemotherapy doses in heavy patients is a consistent finding in previous studies.36,37,43,55 Even when enrolled on clinical trials, obese patients are significantly more likely than lean patients to receive intentionally reduced doses of chemotherapy, in which case the dose reductions represent violations of the clinical trial protocols.35,56 Equally important is the fact that in these studies, the majority of heavy patients received full doses of therapy with no increase in treatment-related toxicity. The motivation for administering reduced chemotherapy doses for the first course of chemotherapy is most likely the result of physicians' desire to avoid toxicity as in the case of obese patients. There appears to be persistent uncertainty among oncologists about the safety of full weight-based doses despite published research supporting the use of actual body weight in calculating doses.35,56-59 In contrast, the reasons for the use of reduced doses in women of lower SES are not as clear. Differences in cancer treatment according to SES have been demonstrated in the type of breast cancer surgery, use of radiation,21-23 and use of systemic therapy.19-21 The appropriate use of adjuvant chemotherapy also appears to vary according to level of education, household income, and insurance status.24,25 Guideline concordant care is given less often to patients insured by only Medicaid or Medicare.60 Each of these disparities may be related to differences in referral, recommendation, and preferences for treatment. Given the multiple steps involved in multimodality cancer care, isolating the sources of differences in treatment is difficult.61 In contrast, in the case of chemotherapy dosing patterns, the patient has been referred to specialty care, has been advised to receive chemotherapy, has accepted the recommendation, and has presented for treatment. The intentional use of reduced chemotherapy for the first course of chemotherapy is physician driven. The only other study we are aware of that examines the effect of SES on chemotherapy dosing in a different sample of patients found that area level income was associated with first cycle dose reductions.43 We suggest that medical providers anticipate a different patient response to the same adverse effects rather than a different adverse effect profile according to SES. Dose reductions, for example, would be intended to decrease the likelihood of such adverse effects in order to improve patient acceptance of continuing therapy. While this is somewhat speculative, there is evidence that physicians hold assumptions and biases about patients based on SES. For example, in a study of postangiography patients, physicians were found to perceive their patients of lower SES as less likely to adhere to treatment, to lack social support, and to be at higher risk of substance abuse.62,63 Moreover, these perceptions have been shown to influence physician decision making and diagnostic and treatment recommendations.63-66 Such biases are more likely to play a role in physician prescribing behavior under conditions of uncertainty.62,67 The adjuvant treatment of breast cancer, in which the benefit of treatment is not clear in an individual patient, may be precisely the type of setting in which uncertainty plays a greater role. In addition, lower social status is associated with less information exchange, shorter visit duration, less partnership building, and less social talk in physician-patient encounters.68-70 Differences in communication may in turn heighten a provider's uncertainty about a patient's living situation, monetary and nonmonetary resources and stressors, expectations of treatment, and social support and may account for the intentional chemotherapy dose reductions seen in this study. One might also ask the converse—why are physicians more willing to give full doses of chemotherapy to people with higher SES? Negotiating a patient through treatment adverse effects may seem more straightforward with patients of higher SES with whom there is less social distance. A limitation of this study is the assignment of SES. Multiple measures of SES have been used in investigating social disparities in treatment and outcome.71 SES measures are not interchangeable, and the SES information in this study was limited to individual educational attainment and zip code. Census level information was collected using patient zip codes rather than ZCTA (which requires street address). This approach may decrease the precision and accuracy of our area-level SES measures. Nonetheless, the strong association between individual educational attainment and the area-level household income supports the use of our measures. This study demonstrates that nonclinical factors, such as SES and geography in addition to obesity, are associated with intentional chemotherapy dose reductions in the adjuvant treatment of breast cancer. The independent association between SES, controlling for geography, suggests that the impact of SES on dosing is not merely related to local practice patterns. These results offer an explanation for the disparities in breast cancer-specific survival in patients of lower SES and may offer an opportunity to improve patient care and possibly patient outcome. Further research to understand physician decision making in chemotherapy dosing and to develop interventions to reduce the variation in chemotherapy dosing is warranted to decrease disparities in breast cancer treatment in vulnerable populations.
Although all authors completed the disclosure declaration, the following authors or their immediate family members indicated a financial interest. No conflict exists for drugs or devices used in a study if they are not being evaluated as part of the investigation. For a detailed description of the disclosure categories, or for more information about ASCO's conflict of interest policy, please refer to the Author Disclosure Declaration and the Disclosures of Potential Conflicts of Interest section in Information for Contributors. Employment: N/A Leadership: N/A Consultant: Melony E.S. Sorbero, Amgen; Jeffrey Crawford, Amgen; David C. Dale, Amgen Stock: N/A Honoraria: Jennifer J. Griggs, Novartis, Aventis; David C. Dale, Amgen; Gary H. Lyman, Amgen, GlaxoSmithKlein Research Funds: Jeffrey Crawford, Amgen; David C. Dale, Amgen; Gary H. Lyman, Amgen, GlaxoSmithKlein Testimony: N/A Other: N/A
Conception and design: Jennifer J. Griggs, Melony E.S. Sorbero, Debra A. Wolff, Jeffrey Crawford, David C. Dale, Gary H. Lyman Provision of study materials or patients: Gary H. Lyman Collection and assembly of data: Eva Culakova, Marek S. Poniewierski, Debra A. Wolff, Gary H. Lyman Data analysis and interpretation: Jennifer J. Griggs, Eva Culakova, Melony E.S. Sorbero, Michelle van Ryn, Debra A. Wolff, Jeffrey Crawford, David C. Dale, Gary H. Lyman Manuscript writing: Jennifer J. Griggs, Eva Culakova, Michelle van Ryn, Gary H. Lyman Final approval of manuscript: Jennifer J. Griggs, Eva Culakova, Melony E.S. Sorbero, Michelle van Ryn, Marek S. Poniewierski, Debra A. Wolff, Jeffrey Crawford, David C. Dale, Gary H. Lyman
published online ahead of print at www.jco.org on December 11, 2006. This research was not funded. The data collection was supported by Amgen Inc through the Awareness of Neutropenia in Chemotherapy (ANC) Study Group. Presented in part at the San Antonio Breast Cancer Symposium, San Antonio, TX, December 8-11, 2005; and at the 42nd Annual Meeting of the American Society of Clinical Oncology, Atlanta, GA, June 2-6, 2006. Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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ABSTRACT
INTRODUCTION
2 tests were used to assess significant differences in first cycle doses for categoric covariates. The Kruskal-Wallis test was used to investigate the association between continuous measures and the use of first cycle dose reductions. Multivariate logistic regression was performed to identify factors independently associated with the use of reduced first cycle doses. Treatment regimen, age, comorbidity, race, and BMI were selected for incorporation into the model a priori based on the literature. Selection of specific SES variables was based on the results of the univariate analysis. Individual education level and geographic region were included in the final model. Census level measures of SES were highly correlated; median household income was selected for the multivariate model. The P values for variables with one degree of freedom were calculated using z-statistics with robust SE estimates. The overall P values for categoric variables with three or more categories were evaluated using the likelihood ratio test. The value of P < .05 was considered to be significant. All analyses were done in SAS, version 9.1 (2004, SAS Institute Inc, Cary, NC). 
