Journal of the National Cancer Institute Advance Access originally published online on May 13, 2008
JNCI Journal of the National Cancer Institute 2008 100(10):738-744; doi:10.1093/jnci/djn145
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ARTICLES |
Residual Treatment Disparities After Oncology Referral for Rectal Cancer
Affiliations of authors: Department of Surgery, University of Michigan, Ann Arbor, MI (AMM, AJH, JDB); Michigan Surgical Collaborative for Outcomes Research and Evaluation, University of Michigan, Ann Arbor, MI (AMM, JDB); Department of Family Medicine, University of Washington, Seattle, WA (BM, LMB); Department of Surgery, Oregon Health and Science University, Portland, OR (KGB)
Correspondence to: Arden M. Morris, MD, MPH, Department of Surgery, University of Michigan, 1500 East Medical Center Dr, TC-5343, Ann Arbor, MI 48109-0331 (e-mail: ammsurg{at}umich.edu).
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ABSTRACT |
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Background: Black patients with rectal cancer are considerably less likely than white patients to receive adjuvant therapy. We examined the hypothesis that the lower treatment rate for blacks is due to underreferral to medical and radiation oncologists.
Methods: We used 1992–1999 Surveillance, Epidemiology, and End Results–Medicare data to identify elderly (
66 years of age) patients who had been hospitalized for resection of stage II or III rectal cancer (n = 2716). We used 
2 tests to examine associations between race and 1) consultation with an oncologist and 2) receipt of adjuvant therapy. We then used logistic regression to analyze the influence of sociodemographic and clinical characteristics (age at diagnosis, sex, marital status, median income and education in area of residence, comorbidity, and cancer stage) on black–white differences in the receipt of adjuvant therapy. All statistical tests were two-sided.
Results: There was no statistically significant difference between the 134 black patients and the 2582 white patients in the frequency of consultation with a medical oncologist (73.1% for blacks vs 74.9% for whites, difference = 1.8%, 95% confidence interval [CI] = >5.9% to 9.5%, P = .64) or radiation oncologist (56.7% vs 64.8%, difference = 8.1%, 95% CI = >0.5% to 16.7%, P = .06), but blacks were less likely than whites to consult with both a medical oncologist and a radiation oncologist (49.2% vs 58.8%, difference = 9.6%, 95% CI = 0.9% to 18.2%, P = .03). Among patients who saw an oncologist, black patients were less likely than white patients to receive chemotherapy (54.1% vs 70.2%, difference = 16.1%, 95% CI = 6.0% to 26.2%, P = .006), radiation therapy (73.7% vs 83.4%, difference = 9.7%, 95% CI = 0.4% to 19.8%, P = .06), or both (60.6% vs 76.9%, difference = 16.3%, 95% CI = 4.3% to 28.3%, P = .008). Patient and provider characteristics had minimal influence on the racial disparity in the use of adjuvant therapy.
Conclusion: Racial differences in oncologist consultation rates do not explain disparities in the use of adjuvant treatment for rectal cancer. A better understanding of patient preferences, patient–provider interactions, and potential influences on provider decision making is necessary to develop strategies to increase the use of adjuvant treatment for rectal cancer among black patients.
Prior knowledge Black patients with rectal cancer are considerably less likely than white patients to receive adjuvant therapy, but it is unclear whether this disparity is due to underreferral of blacks to medical and radiation oncologists. Study design
Surveillance, Epidemiology, and End Results (SEER)–Medicare data were used to identify elderly ( Contribution There was no difference in the frequency of consultation with a medical or radiation oncologist between the black patients and the white patients, but blacks were less likely than whites to consult with both a medical oncologist and a radiation oncologist. Among patients who saw an oncologist, black patients were less likely than white patients to receive chemotherapy, radiation therapy, or both. Patient and provider characteristics had minimal influence on the racial disparity in the use of adjuvant therapy. Implications A better understanding of patient preferences, patient–provider interactions, and potential influences on provider decision making is necessary to develop strategies to increase the use of adjuvant treatment for rectal cancer among black patients. Limitations Aggregate data were used to describe patient-level income. Patient and physician decision making was not explored. Medicare data are limited to patients older than 65 years; thus, the findings may not apply to all patients with rectal cancer.
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Despite recent overall improvements in rectal cancer outcomes (1,2), black patients continue to have substantially worse prognosis than white patients. Current data from the Surveillance, Epidemiology, and End Results (SEER) registry reveal that the long-term survival rates after rectal cancer surgery are 14%–20% lower for black patients than for white patients (3). Many non–cancer-related reasons for this difference have been identified, such as increased burden of comorbid disease among black patients, later stage at presentation, and sociodemographic factors that are independently associated with decreased survival (4–6). However, our group and others (7,8) have shown that disparities in survival are also partly attributable to lower use of adjuvant radiation and chemotherapy among black patients.
It is unclear why blacks are less likely than whites to receive appropriate adjuvant therapy. One possibility is that black patients and their oncologists actively consider therapy but make an explicit decision not to proceed with treatment. Black patients may be more likely to decline adjuvant treatment than white patients because of a sense of fatalism toward disease, a general lack of trust in health-care providers, or concerns about the risks and side effects of treatment (9). These concerns may stem from previous personal experiences or fundamental cultural beliefs. Alternatively, black patients may be more likely than white patients to decline therapy because of compelling personal circumstances, such as being the family caregiver (10) or being unable to travel for regular treatment. Oncologists may recommend against adjuvant therapy because of clinical considerations such as the presence of comorbid disease, which is more common among black patients (11,12), or because, as suggested by limited retrospective data (13), they believe that therapy is less effective among black patients. Even in the absence of overt discrimination, race-related differences in patient–provider interactions may also influence patients’ preferences or oncologists’ clinical recommendations regarding adjuvant treatment for rectal cancer.
Another possible reason for the disparity in adjuvant treatment is that black patients are simply not being offered a choice. That is, it is possible that black patients with advanced rectal cancer have a lower rate of referral to oncologists in the first place and thus have no opportunity to choose adjuvant therapy. Previous studies (14–16) indicate that black patients who are diagnosed with a host of diseases are less likely than white patients to be referred for treatment or simply to obtain access to specialty care. To better understand the role of access to consultation in subsequent use of adjuvant therapy, we used a large national database to compare the frequency of oncologist consultations between black and white patients with stage II or III rectal cancer. We then explored whether disparities in the use of adjuvant therapy persisted among patients who had an initial consultation.
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Methods |
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Data
We used the SEER-Medicare–linked database (17) of the National Cancer Institute, which contains clinical, demographic, and medical claims data on patients aged 65 years or older, to identify rectal cancer patients who were diagnosed between January 1, 1992, and December 31, 1999. During this time period, SEER registries that covered five states—New Mexico (includes Arizona Indians), Connecticut, Hawaii, Iowa, and Utah—and six county-based areas within an additional four states—Atlanta–rural Georgia, Detroit, Los Angeles, San Francisco–Oakland, San Jose–Monterey, and Seattle–Puget Sound—ascertained the incident cases of rectal cancer among a population that represents approximately 14% of persons living in the United States. The SEER data included information about tumor stage and patient demographics. The Medicare claims data included information about Medicare enrollment dates, health maintenance organization membership, and fee-for-service claims for inpatient and outpatient services provided to patients, including surgical care and hospital stays, physician consultations, and treatment with chemotherapy and/or radiation. This study was approved by the University of Washington Institutional Review Board.
Study Population
We identified all patients aged 66 years or older who were diagnosed with rectal cancer of American Joint Committee on Cancer [AJCC (18)] stage II or III between January 1, 1992, and December 31, 1999 (n = 4647). Patients were excluded if 1) their tumor histology (ie, a sarcoma or carcinoid tumor) required that they receive atypical treatment (n = 119); 2) they had a prior colorectal cancer diagnosis (n = 112); 3) their cancer was diagnosed at death or autopsy (n = 6); or 4) they had a simultaneous diagnosis of AJCC stage IV cancer (n = 8).
We used three additional exclusion criteria to ensure adequate preoperative data to identify comorbid diseases and adequate postoperative time duration for implementation of adjuvant therapy. First, because we used Medicare data to ascertain comorbidity for appropriate risk adjustment, patients who were not enrolled in Parts A and B of the Medicare fee-for-service plan for the 12 months before the month of their rectal cancer diagnosis were excluded (n = 1005). Second, because AJCC stage II/III rectal cancer patients who have not undergone resection within 6 months of diagnosis are highly unlikely to undergo curative resection and therefore to receive adjuvant therapy (as opposed to salvage or palliative therapy), we excluded patients who had not undergone surgical resection within 6 months of the diagnosis month (n = 813). Third, to ensure that we could ascertain receipt of adjuvant treatment with radiation or chemotherapy, we excluded all patients who were not alive and fully enrolled in parts A and B of the Medicare fee-for-service plan for the 9-month period that began with the month of diagnosis (n = 1457). (Some patients met more than one exclusion criteria; thus, the total number excluded was less than the sum of each category.)
Nearly identical proportions of black and white patients were excluded for histology, previous cancer, or diagnosis at death. Different proportions of black and white patients were excluded for incomplete prior enrollment (22% white vs 30% black), no resection (18% white vs 27% black), and incomplete subsequent enrollment (32% white vs 44% black). Overall, 41% of white patients and 54% of black patients were excluded. The final study sample included 2716 patients, of whom 134 were black and 2582 were white.
Study Variables
The primary outcome of interest was administration of radiation or chemotherapy within 9 months of diagnosis of stage II or III rectal cancer among patients who had consulted with a radiation oncologist and/or a medical oncologist. The secondary outcome was having an initial consultation with a radiation or medical oncologist. The independent variable was black or white patient race, as designated by the SEER database.
We defined the administration of chemotherapy as the presence of inpatient and outpatient hospital claims or physician office claims for chemotherapeutic agents that are specifically used to treat colon and rectal cancers, that is, 5-fluorouracil, leucovorin, or floxuridine (Healthcare Common Procedure Coding System codes J9190 and J0640) and by general codes for chemotherapy during the appropriate time period (Current Procedural Terminology [CPT] codes 96408–96414, 96520, 96530, 96545, and 96549 and International Classification of Diseases, Ninth Revision, Clinical Modification [ICD-9-CM], diagnosis codes E0781, Q0083–Q0085, and V58.1 and procedure code 99.25).
We defined administration of radiation therapy as any of the following codes for management or administration of radiation therapy: CPT codes 77401–77417, 77419–77431, 77470, 77499, 77750, 77761–77763, 77789–77790, or 77799; ICD-9-CM codes 92.20–92.26, 92.28, or 92.29, ICD-9-CM diagnosis code V58.0; or revenue center code 0333. We defined the initial medical oncologist consultation as the first Medicare claim from a medical oncologist (identified by carrier file Health Care Financing Administration [HCFA] provider specialty code 90) who was seen during the 1 month before or the 9 months after (and including) the month of diagnosis. We defined radiation oncologist (HCFA provider specialty code 92) consultations in an identical fashion.
Patient Characteristics
We obtained information about each patient's age at diagnosis, sex, and marital status from the SEER database. We collected information about each patient's income and education as detailed below using data from the year 1990 US Census for patients who were diagnosed through December 31, 1995, and data from the year 2000 US Census for patients who were diagnosed on January 1, 1996, or later. US Census data include median household income and median education level (according to race and ethnicity) for each census tract and zip code. Each patient was assigned the median income in their zip code of residence. Education level from 1990 US Census data was used to establish the race-specific percentage of persons older than 25 years with more than 12 years of education within each patient's census tract. Patients were classified according to their comorbidity index scores (0, 1, or 2). To assign the comorbidity score, we examined inpatient and outpatient Medicare claims during the 11 months before the month before the diagnosis month and used Romano's adaptation of the Charlson comorbidity index, as previously described (19). We used inpatient Medicare claims to determine the length of stay for the cancer resection hospitalization and, per common practice, defined prolonged hospitalization as a hospital stay that lasted more than 14 days. For some analyses, length of hospital stay was divided into three categories: hospitalization up to 7 days (a normal length of stay); 8–14 days, a prolonged stay after colectomy but one that does not definitively imply a complication; and more than 14 days, a prolonged stay that implies some sort of complication.
Provider Characteristics
We linked the Unique Physician Identifier Numbers in the Medicare files to the 1993 and 1997 American Medical Association Masterfiles to determine characteristics of each patient's surgeon, medical oncologist, and/or radiation oncologist. Physician characteristics included race, age, number of years in practice, board certification (American Board of Surgery, American Board of Colon and Rectal Surgery, American Board of Internal Medicine, and/or American Board of Radiology), and practice type (solo or group). Case volume was calculated for all surgeons who treated the patients included in this study based on tertiles of total number of cases during the study period. Practice volume was calculated for each oncologist from the number of initial consultation claims for rectal cancer patients in the SEER database that were billed to Medicare in each study year.
Statistical Analysis
Initially, we used 2 tests to compare overall differences in demographic and clinical characteristics between black and white patients. We assessed the relative unadjusted rates of undergoing an adjuvant therapy consultation with either a radiation or a medical oncologist. For those patients who underwent an initial consultation, we used the test of binomial proportions to compare unadjusted rates of adjuvant therapy administration by patient race. We then used a multiple logistic regression model to examine the degree to which patient and provider variables were associated with racial differences in the receipt of adjuvant treatment. Sociodemographic and clinical variables (patient age at diagnosis, sex, marital status, median household income in zip code of residence, Charlson–Romano comorbidity score, and AJCC stage) were included in the model a priori. Cut points for categorical variables were chosen based on common use (eg, 5-year increments for age) or for generally equitably sized comparison groups (eg, median income); other variables were included in the model if they were statistically significantly associated (P 
.05) with the outcome or improved the goodness of fit in either model (ie, of the association between race and chemotherapy administration or radiation therapy administration). Because it is common for adjuvant therapy to be used to treat stage II or III rectal cancer, we calculated estimated relative risks (RRs) of adjuvant therapy by correction of the adjusted odds ratios, as previously described (20). All analyses were repeated with correction for clustering within hospitals using the general estimating equation; the results of these analyses are not reported because neither the point estimates nor the 95% confidence intervals (CIs) changed considerably. All tests of statistical significance were two-sided, and statistical significance was defined as P .05. All analyses were performed with SAS 9.1 software (SAS Institute, Inc, Cary, NC).
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Results |
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Among patients who met the inclusion criteria, the 134 black patients did not differ statistically significantly from the 2582 white patients with respect to the most relevant clinical variables, that is, age at diagnosis and stage of disease (Table 1). However, the two patient groups differed statistically significantly in every other demographic category. Black patients were more likely than white patients to be divorced, separated, or single (30.3% vs 11.1%, difference = 19.2%, 95% CI = 11.3% to 27.1%, P < .001); to reside in a zip code with a median household income less than $25 000 per year (50.4% vs 11.1%, difference = 39.3%, 95% CI = 30.7% to 47.9%, P < .001); and to reside in a census tract in which less than 80% of persons aged 25 years or older of the same race had completed 12 years of education (67.2% vs 19.5%, difference = 47.7%, 95% CI = 39.4% to 56.0%, P < .001). During the initial hospitalization for rectal cancer resection, black patients were also statistically significantly more likely than white patients to have a prolonged hospital stay (ie, more than 14 days; 33.1% vs 16.7%, difference = 16.4%, 95% CI = 8.2% to 24.6%, P < .001) and to be operated on by a surgeon in the lowest tertile of annual case volume (65.0% vs 45.3%, difference = 19.7%, 95% CI = 11.0% to 28.4%, P < .001). A greater proportion of black patients than white patients saw a general surgeon rather than a colorectal surgeon, but the difference was not statistically significant (74.0% vs 66.8%, difference = 7.2%, 95% CI = >0.8% to 15.1%, P = .096).
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Likelihood of Initial Consultation With an Oncologist
Although we found no statistically significant difference between black and white patients in the frequency of an initial consultation with either a medical oncologist (73.1% vs 74.9%, difference = 1.8%, 95% CI = >5.9% to 9.5%, P = .64; Table 2) or a radiation oncologist (56.7% vs 64.8%, difference = 8.1%, 95% CI = >0.5% to 16.7%, P = .06), black patients were less likely than white patients to consult with both a medical oncologist and a radiation oncologist (49.2% vs 58.8%, difference = 9.6%, 95% CI = 0.9% to 18.2%, P = .03). The medical and radiation oncologists seen by black patients were similar to those seen by white patients with respect to age, sex, number of years in practice, and board certification (data not shown). A greater proportion of black patients than white patients saw a black medical oncologist (14.8% vs 0.8%, difference = 14.0%, 95% CI = 4.5% to 23.5%, P = .004) or a black radiation oncologist (10.9% vs 2.8%, difference = 8.1%, 95% CI = >0.2% to 16.4%, P = .056), but the latter difference was not statistically significant.
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Likelihood of Subsequent Adjuvant Therapy
Although black patients and white patients were equally likely to have an initial oncologist consultation, the use of adjuvant therapy differed statistically significantly between blacks and whites who had an initial consultation (Table 2). Black patients were less likely than white patients to receive chemotherapy (54.1% vs 70.2%, difference = 16.1%, 95% CI = 6.0% to 26.2%, P = .006) or radiation therapy (73.7% vs 83.4%, difference = 9.7%, 95% CI = 0.4% to 19.8%, P = .06). Among the patients who saw both a medical oncologist and a radiation oncologist, fewer black patients than white patients underwent both chemotherapy and radiation (60.6% vs 76.9%, difference = 16.3%, 95% CI = 4.3% to 28.3%, P = .008).
Accounting for Differences in Adjuvant Therapy Use
We used a logistic regression model to examine patient and provider characteristics that were associated with the differential use of adjuvant therapy by black and white patients and derived estimated relative risks from the calculated odds ratios. Among patients who had an initial oncologist consultation, the unadjusted relative risk of chemotherapy use for black vs white patients was 0.76 (95% CI = 0.62 to 0.92) and the unadjusted relative risk of radiation use was 0.87 (95% CI = 0.73 to 0.98) (Table 3).
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Adjusting for specific patient and provider characteristics in the multivariable analysis had little effect on racial differences in the use of radiation or chemotherapy. After adjusting sequentially for demographic, clinical, and oncologist characteristics, black patients continued to have a statistically significantly lower likelihood of chemotherapy use than white patients (RR = 0.83, 95% CI = 0.67 to 0.98) (Table 3).
We found that the largest disparities in the use of chemotherapy between black and white patients were among patients who had characteristics associated with better health (Table 4). For example, among patients with no comorbidities (ie, those with a Charlson score of 0), 72.6% of whites but only 48.9% of blacks received adjuvant chemotherapy (difference = 23.7%, 95% CI = 9.2% to 38.2%, P < .001). Similarly, black–white differences in chemotherapy use were greater among patients who were younger at diagnosis or had shorter hospitalizations than among patients who were older or had prolonged hospitalizations.
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Discussion |
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TopAbstractContext and CaveatsMethodsResultsDiscussionFundingReferencesNotes |
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In recent years, rectal cancer survival rates overall have improved by 15%–20% due to the increasing use of adjuvant chemotherapy and radiation (2,21–25). However, black patients are less likely than white patients to survive rectal cancer, partly because they are less likely to receive adjuvant therapy (8). In this study, we found that racial differences in receipt of chemotherapy and radiation were not accounted for by racial differences in the initial access to a medical or radiation oncologist. Among patients who had an initial consultation with an oncologist, black patients were 22.9% less likely to have chemotherapy and 11.6% less likely to have radiation than white patients.
Several studies (26–29) have examined the reasons for nonuse of chemotherapy by rectal cancer patients in the general population without examining reasons for racial disparities in treatment rates. Previously identified factors associated with nonuse of chemotherapy in the general population include older age at diagnosis, excessive comorbidity, "lack of clinical indications," and—the most commonly cited reason—a simple lack of referral to an oncologist. However, none of these factors was associated with the lower receipt of adjuvant therapy among black patients in our cohort of rectal cancer patients.
Our examination of baseline patient characteristics that might account for racial disparities in treatment revealed that individual demographic and clinical variables had minimal influence. Predictably, we found that the use of chemotherapy by white patients declined with increasing age at diagnosis and increasing comorbidity. By contrast, among the black patients in our cohort, those with the lowest comorbidity scores, that is, those who were relatively healthier, were the least likely to receive treatment.
Although we were unable to discern why our findings were magnified among the healthier black patients, previous studies have found that poorer adherence to screening and other health recommendations among healthier patients is associated with lack of patient experience in medical encounters or increased family caretaker responsibilities (10,30,31). In addition, despite having access to an initial consultation, black patients overall may have been less likely to undergo adjuvant treatment because of difficulty or unfamiliarity with navigating the medical system (32). Finally, it is possible that black patients overall are more likely than white patients to refuse adjuvant therapy because of social or cultural reasons, such as reduced risk tolerance, lack of faith in medical treatment, or simple resignation to a disease state (9).
Health-care providers play a crucial role in recommending and helping patients navigate treatment options. However, none of the provider characteristics that we examined was associated with racial differences in receipt of adjuvant therapy. It is possible that oncologists’ recommendations about adjuvant treatment are influenced in unmeasured ways by the race of the patient. For example, on the basis of retrospective cohort data (13), oncologists may believe that the efficacy of adjuvant therapy for colon and rectal cancers differs by patient race. However, large randomized prospective studies have not shown a difference in efficacy according to race (33–35). Alternatively, patient–provider interactions or race concordance between patients and their physicians may influence provider behavior, as has been previously reported (36,37). In this study, black patients were more likely than white patients to see a nonwhite oncologist. However, the number of nonwhite oncologists was too small to draw conclusions about whether provider race was statistically significantly associated with the use of adjuvant chemotherapy. It is also possible that black patients may receive care from providers or in settings with fewer resources to ensure follow-up or initiation of adjuvant care (14).
Our findings support those of Baldwin et al. (38), who evaluated the use of chemotherapy among stage III colon cancer patients. In that study, although black and white patients were equally likely to be referred to an oncologist, the black patients in the youngest age group were statistically significantly less likely than their white counterparts to undergo chemotherapy for stage III colon cancer. Taken together, data from Baldwin et al. (38) and from this study indicate that black patients who are younger and healthier—that is, those who have the most potential life years to gain from chemotherapy—are the least likely to receive chemotherapy. However, other data (39) indicate that once therapy for colon cancer is initiated, the completion rates for blacks and whites are the same. Given the persistent racial disparity in colorectal cancer survival, data from this and the previous (38,39) studies highlight the importance of initiating adjuvant treatment for black patients.
Our study has several limitations that are worth noting. First, we used aggregate data to describe patient-level income, which could have contributed to the finding that income was not associated with the black–white disparity in the use of chemotherapy. However, results of one study (40) indicate that geographic setting or neighborhood aggregate data may be as important as individual patient attributes in terms of access to care. Second, although our administrative data included a record of a first oncologist visit, it inherently lacked the depth necessary to explore patient or physician decision making during that visit. Similarly, administrative data permit a limited assessment of comorbidity and the risk of potential complications of chemotherapy. If better risk adjustment were possible using administrative data, more inference about physician decisions might be feasible. Third, Medicare data are limited to patients older than 65 years; thus, our findings may not apply to all patients with rectal cancer. However, through Medicare, all of the patients included in this study had comparable health coverage. It is probable that younger black patients, who are more likely to lack medical insurance than white patients (41), undergo appropriate adjuvant therapy at even lower rates.
In summary, our data indicate that racial disparities in the use of adjuvant therapy for rectal cancer exist despite equal access to an initial oncologist consultation. Moreover, disparities in the use of recommended adjuvant treatment cannot be attributed to easily identifiable attributes of the patient or the provider. Until targets for intervention can be clarified, such as patient–physician communication and physician decision making, or the distribution of resources to settings where black patients are most likely to obtain care is improved, it is unlikely that racial disparities in the care of rectal and, possibly, other cancers will be improved in a meaningful way.
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Funding |
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American Cancer Society, Atlanta, GA (Mentored Research Scholar Grant #MRSGT06-076-01-CHPHS); National Cancer Institute, National Institutes of Health, Bethesda, MD (R01CA089544).
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NOTES |
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The views expressed in this article are the authors' and do not necessarily represent the views of the American Cancer Society or the National Cancer Institute. The study sponsors had no role in the design of the study; the collection, analysis, or interpretation of the data; the writing of the manuscript; or the decision to submit the manuscript for publication.
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Manuscript received November 28, 2007; revised March 20, 2008; accepted April 7, 2008.
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