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Journal of Clinical Oncology, Vol 25, No 24 (August 20), 2007: pp. 3589-3595
© 2007 American Society of Clinical Oncology.
DOI: 10.1200/JCO.2006.10.0156

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Disparities in Treatment and Outcome for Renal Cell Cancer Among Older Black and White Patients

Sonja I. Berndt, H. Ballentine Carter, Mark P. Schoenberg, Craig J. Newschaffer

From the Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health; Department of Urology, James Buchanan Brady Urological Institute, Johns Hopkins School of Medicine, Baltimore; and Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD

Address reprint requests to Sonja Berndt, PhD, Division of Cancer Epidemiology and Genetics, National Cancer Institute, 6120 Executive Blvd, EPS 8012, MSC 7240, Bethesda, MD 20892-7240; e-mail: berndts{at}mail.nih.gov


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
Purpose: Black patients with renal cell cancer have shorter survival compared with their white counterparts, but the causes for this disparity are unclear. To elucidate reasons for this inequality, we examined differences in treatment and survival between black and white patients.

Patients and Methods: A retrospective cohort study was conducted using data from the linked Surveillance, Epidemiology and End Results (SEER) cancer registry and Medicare databases. Participants included 964 black and 10,482 white patients age ≥ 65 years who were enrolled into Medicare and diagnosed with renal cell cancer between 1986 and 1999. Information on surgical treatment was ascertained from both databases, whereas data regarding coexisting illness and survival was obtained from the Medicare database.

Results: The percentage of black patients receiving nephrectomy treatment was significantly lower compared with whites (61.2% v 70.4%; P < .0001). After adjustment for age, sex, median income, cancer stage, tumor size, and comorbidity index, blacks were less likely to undergo nephrectomy treatment compared with whites (risk ratio = 0.93; 95% CI, 0.90 to 0.96). Overall survival was worse for blacks than whites even after adjustment for demographic and cancer prognostic factors (hazard ratio [HR] = 1.16; 95% CI, 1.07 to 1.25); however, additional adjustment for comorbidity index and nephrectomy treatment reduced the disparity substantially (HR = 1.00; 95% CI, 0.93 to 1.09).

Conclusion: This study indicates that the lower survival rate among blacks compared with whites with renal cell cancer can be explained largely by the increased number of comorbid health conditions and the lower rate of surgical treatment among black patients.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
The incidence and mortality of renal cell cancer has increased in the United States since the 1970s,1 making kidney and renal pelvis cancer the seventh leading cancer among men.2 Incidental detection of kidney tumors through the use of computed tomography and other radiographic procedures is believed to account for at least part of the increase in incidence in developed countries.3-6 For both blacks and whites, the largest increase in renal cell carcinoma has been observed for the localized disease.1,7 Over time, 5-year survival rates have improved among whites; however, little change in survival has been seen among blacks.1 The reasons for this disparity are not entirely clear.

Surgical excision is the primary treatment for renal cell cancer, with 5-year survival rates of 65% to 93% for localized disease.8 Although radical nephrectomy is considered the standard treatment, other less invasive or more limited approaches, such as laparoscopic nephrectomy or partial nephrectomy, have gained popularity.9 Nephrectomy is the only known effective treatment for nonmetastatic disease, making access to surgical treatment critical for patients with renal cell cancer. Disparities in treatment could contribute to differences in survival among racial or ethnic groups.

To examine differences in treatment and survival between black and white renal cell cancer patients, we conducted a retrospective cohort study among Medicare beneficiaries using Surveillance, Epidemiology and End Results (SEER) cancer registry data and linked Medicare claims data.


    PATIENTS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
Study Design
The SEER registry is a population-based cancer registry that was started in 1973 to track the incidence and mortality from cancer in the United States. For incident cancer cases within a SEER region, information is collected on demographic factors, cancer diagnosis (eg, site, histology, and stage), initial treatment, and vital status. The geographic areas covered by SEER include six metropolitan areas (Atlanta, GA; Detroit, MI; Los Angeles, CA; San Francisco-Oakland, CA; San Jose-Monterey, CA; and Seattle-Puget Sound, WA) and five states (Connecticut, Hawaii, Iowa, New Mexico, and Utah) and represent approximately 14% of the US population.10

Medicare provides health care insurance for approximately 97% of persons age ≥ 65 years in the United States. For Medicare beneficiaries not enrolled onto a managed care plan, information regarding hospitalizations is captured in the Medicare Provider Analysis and Review (MEDPAR) files. In 1991, the SEER and Medicare databases were linked to allow health outcomes research. Ninety-four percent of persons age ≥ 65 years in the SEER database were linked successfully to Medicare records.11 At the time we requested the data, the SEER-Medicare database contained cancer cases reported to SEER from 1973 through 1999 and Medicare claims from 1986 through 2001. Our study was restricted to cancer cases diagnosed between 1986 and 1999. The study was considered exempt research by the Institutional Review Board at the Johns Hopkins Bloomberg School of Public Health (Baltimore, MD).

Study Population
This study included Medicare participants age ≥ 65 years diagnosed with invasive kidney cancer (International Classification of Diseases for Oncology [ed 2], site code C64.9) in SEER regions between 1986 and 1999. Participants were excluded if they had nonepithelial tumors (eg, sarcomas and lymphomas), were diagnosed on autopsy, or had cancer reported by death certificate only. Participants were also excluded if they were enrolled in health maintenance organizations at the time of or after diagnosis. The analysis was limited to participants classified as non-Hispanic white or black according to the SEER race variable (Race Recode B). This variable is based on race and ethnic information from registration data and medical records and is believed to have greater specificity than Medicare categories of race.12 After exclusions, a total of 964 black and 10,482 white patients with renal cell cancer remained.

Demographic Factors, Comorbidity, and Treatment
Information on age at diagnosis and sex was obtained from Medicare records, whereas data on race, cancer stage, and tumor size were captured through SEER records. No individual measures of socioeconomic status were available within the SEER-Medicare database, so socioeconomic status was estimated for each patient using the median income in 1990 for the census tract of residence. Quartiles of median income were estimated from the cohort, and the upper three quartiles were collapsed into one stratum for the analysis. Other aggregate measures of socioeconomic status, such as percentage of persons with less than a high school education within the census tract, were explored in analyses with similar results. Thus, only analyses conducted using census tract median income are presented.

Coexisting illness was assessed using MEDPAR inpatient records of hospital admissions occurring within the year before diagnosis. The Charlson comorbidity index13 with modifications that reflect the Deyo14 and Romano15 adaptations was used to calculate a comorbidity score for each patient who had been enrolled onto Medicare for at least 1 year before diagnosis. Given that the index uses data from hospital admissions during the year before diagnosis, the Charlson comorbidity score could not be calculated for persons enrolled into Medicare for less than 1 year before diagnosis or enrolled in a health maintenance organization within the year before diagnosis because earlier hospitalizations may not have been captured by Medicare.

Surgical treatment was examined using both SEER and MEDPAR data. SEER captures surgical treatment performed within the first 4 months after diagnosis; however, we allowed a 6-month window for surgery using the MEDPAR data. Patients were considered to have undergone surgical treatment if either SEER or MEDPAR records indicated that nephrectomy (SEER site-specific surgery codes 10-70 and 90; International Classification of Diseases [9th revision] procedure codes 55.4 and 55.5x [except 55.53]) had been performed. There was 93% concordance for nephrectomy status between the two sources of data. We chose to use both sources of data to improve our sensitivity for nephrectomy; however, the results were similar when we restricted the analysis to individuals with concordant treatment status.

Medicare records were used to determine vital status and dates of death. Medicare obtains information regarding death from the Social Security Administration. All records of death in the data set were complete through December 31, 2002. Follow-up time for the participants was determined from the date of first renal cell cancer diagnosis to the date of death or the last date of follow-up (December 31, 2002), whichever came first. For survivors, the median length of follow-up time was 6.9 years for whites and 6.3 years for blacks.

Statistical Analysis
Baseline characteristics of black and white patients were compared using a {chi}2 test. Given that binomial regression provides a better approximation of the relative risk compared to logistic regression when outcome is common,16 crude and adjusted risk ratios (RRs) of nephrectomy associated with race were estimated using binomial regression17 with the modification suggested by Deddens et al18 as needed. Conclusions drawn from logistic regression models were similar to those inferred from binomial regression models (data not shown). Survival curves were generated using the Kaplan-Meier method,19 and a log-rank statistic was used to assess crude differences in survival between blacks and whites. Cox proportional hazards regression20 was using to estimate hazard ratios (HRs) and 95% CIs of death associated with race adjusted for potential confounders. Potential interactions were examined by including the main effect and cross-product terms in the regression model and comparing nested models with and without the cross-product terms using a likelihood ratio test. All statistical analyses were performed using SAS version 8.1 (SAS Institute Inc, Cary, NC).


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
Baseline characteristics of the black (n = 964) and white (n = 10,482) renal cell cancer patients are listed in Table 1. Black patients were younger and more likely to reside in a census tract with a low median income. Blacks were somewhat less likely to be diagnosed at a regional cancer stage than whites, but no difference was observed in the percentage diagnosed at a distant stage, and the average tumor size was similar between the groups. Blacks were more likely to have higher comorbidity scores as measured by the Charlson comorbidity index.


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Table 1. Characteristics of Black and White Patients Diagnosed With Renal Cell Cancer Between 1986 to 1999

 
Black patients were significantly less likely to undergo nephrectomy treatment than whites (P < .0001). Only 61.2% (n = 590) of black patients underwent nephrectomy compared with 70.4% (n = 7,384) of white patients. We examined factors that might influence the decision to perform nephrectomy and explain some of the difference in treatment rates. Demographic characteristics (eg, age, sex, and median income), cancer prognostic factors (eg, cancer stage and tumor size), and comorbidity index explained a fraction of the disparity (Table 2). However, even after adjustment for these factors, blacks were less likely to undergo nephrectomy treatment than whites (RR = 0.93; 95% CI, 0.90 to 0.96; P < .0001).


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Table 2. Factors Associated With Differences in Nephrectomy Rates Between Blacks and Whites

 
To assess the robustness of this disparity, we conducted a number of stratified analyses. The lower rate of nephrectomy among blacks was consistent across strata of age, sex, stage, tumor size, and comorbidity index (Table 3). Even among patients with localized renal cell cancer, blacks were 7% less likely to undergo nephrectomy compared with similar whites (P < .0001). The treatment difference was similar across SEER regions (data not shown), and there was little evidence that the disparity had improved over time; the RR was nearly the same for patients diagnosed in 1996 to 1999 compared with 1986 to 1990 (RR = 0.94; 95% CI, 0.89 to 0.98 v RR = 0.93; 95% CI, 0.87 to 0.99).


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Table 3. RR of Nephrectomy for Blacks Compared With Whites Stratified by Various Characteristics

 
Overall, survival was shorter for blacks compared with whites (median survival, 2.6 v 3.2 years, respectively; Fig 1). At 5 years, the crude survival rate was 40.8% among whites but only 34.5% among blacks, and the HR of death was 1.18 (95% CI, 1.09 to 1.27) for blacks compared with whites. Adjustment for age, sex, census tract median income, cancer stage, and tumor size had little impact on the racial divergence in survival (Table 4). However, additional adjustment for comorbidity index and nephrectomy treatment substantially reduced the difference in survival between blacks and whites (HR = 1.00; 95% CI, 0.93 to 1.09), suggesting that these two factors explained a large portion of the disparity.


Figure 1
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Fig 1. Survival of renal cell cancer patients by race.

 

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Table 4. Factors Associated With Differences in Survival Between Blacks and Whites

 
In a secondary analysis, we examined whether the racial disparity in survival persisted when the results were stratified by nephrectomy. Overall, survival was better for individuals receiving nephrectomy than those not undergoing treatment, irrespective of race. Among those who underwent nephrectomy, blacks had worse survival than whites, whereas survival was better for blacks not undergoing nephrectomy compared with their white counterparts (Pinteraction = 0.001; Fig 2). Adjustment for demographic factors, cancer prognostic indicators, and comorbidity index reduced these racial differences in survival, so that the 95% CIs included 1.0 (Table 4). Additional adjustment for end-stage renal disease reduced the racial disparity among those undergoing nephrectomy (HR = 1.07; 95% CI, 0.96 to 1.20), but not among those without surgical treatment (HR = 0.89; 95% CI, 0.80 to 1.00).


Figure 2
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Fig 2. Survival of renal cell cancer patients by race and surgical treatment.

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
Nephrectomy is the primary treatment for renal cell cancer. Although the use of nephrectomy for metastatic disease is controversial, it is the standard treatment for nonmetastatic renal cell cancer. Despite its effectiveness, we found that black patients with renal cell cancer were less likely to undergo nephrectomy than whites, regardless of age, sex, socioeconomic status, cancer stage, tumor size, or comorbidity score. Even among patients with localized disease, the rates of nephrectomy were lower for blacks than similar whites. Our results are consistent with other studies that have observed lower rates of surgery among blacks for metastatic renal cell cancer,21 lung cancer,22-24 colorectal cancer,25-27 and other medical conditions.28

The reasons for the difference in nephrectomy rates between blacks and whites are not entirely clear. It is possible that blacks are more likely to have health conditions that make them poor candidates for surgical treatment. Although we adjusted for comorbidity in our analysis, there may be coexisting illnesses not captured by this index that account for the difference in treatment rates. The Charlson index was created to adjust for comorbidities that might affect survival and not necessarily treatment choice. There may be conditions that influence the decision whether to perform surgery that may not be captured in this index. In addition, several studies have noted that comorbid conditions are underreported in claims databases compared with medical records or clinical data.29-31

Socioeconomic factors may also play a larger role in the treatment disparity than our study suggests. Although this study was restricted to Medicare beneficiaries and thus, insurance coverage was similar across races, there may be other socioeconomic factors that contributed to the decision whether to undergo surgery. Other factors include competing demands (eg, childcare), ancillary costs (eg, discharge medications), and potential loss of income or work due to hospitalization. Given that only aggregate measures of socioeconomic status were available in this study, our ability to examine the role of socioeconomic factors in nephrectomy treatment was limited.

Differences in access and quality of health care may have also contributed to racial disparity in nephrectomy rates. Bach et al32 reported that primary care physicians who treated mostly black patients had greater difficulty delivering high-quality care and obtaining access to high-quality specialists for their patients. Similarly, Groeneveld et al33 found that hospitals with more than 20% black inpatients were less likely to perform new medical procedures than hospitals with less than 9% black inpatients. Other studies have reported that the quality of care is poorer for black patients enrolled onto Medicare managed care health plans than for whites.34,35

Alternatively, differences in patients' attitudes or beliefs about surgery may have played a role in the choice of treatment. Several studies have suggested that blacks may be more averse to surgical treatment than whites.36-38 Margolis et al39 found that blacks were more likely to believe that air exposure during lung cancer surgery would cause the tumor to spread and were more likely to oppose surgery because of this belief than whites. Historically, minorities have not been treated well by the medical establishment, and lower levels of trust and less participatory communication in their visits with physicians among blacks40-43 may contribute to an increased aversion to surgery among blacks.

Among those who underwent nephrectomy, we found that blacks had slightly worse survival than whites. Adjustment for comorbidity and other factors reduced the disparity, but other factors may have contributed to the survival difference. On average, blacks are more likely to have surgery at low-volume hospitals, which are reported to have increased mortality rates.44 Although the reasons for the higher mortality rates among low-volume hospitals are not entirely clear, less experienced surgeons and reduced resources are believed to play a role. Lower quality of postoperative care may have contributed to the reduced survival among blacks.

Among those who did not undergo surgery, blacks had slightly better crude survival rate than whites. This was partially due to higher percentage of blacks with localized disease and hence, better prognosis; the difference in survival was reduced substantially after adjustment for cancer stage and tumor size. In a smaller study, Tripathi et al21 found that white patients with metastatic renal cell cancer who did not undergo nephrectomy had longer time to progression than black patients, but no effect modification by treatment was reported with survival. In our study, both blacks and whites who did not undergo nephrectomy had worse survival than those who did receive surgical treatment.

Our study had several limitations. First, our analysis was restricted to Medicare recipients ≥ age 65 years, and the results may not be generalizable to younger patients with renal cell cancer. Second, we did not have individual measures of socioeconomic status and thus our ability to examine socioeconomic factors that could have contributed to racial differences in treatment or outcomes was limited. Third, residual confounding by comorbid illness may still exist. The Charlson index is not a perfect measure of the impact of comorbid disease, and claims data are not error free. It is possible that some comorbid health conditions were missed, leading to comorbidity misclassification. In addition, we did not have information regarding the mode of cancer detection (incidental v symptomatic), which may be related to survival,45 or performance status, which is likely correlated with the receipt of treatment. Information regarding tumor grade was also missing for a substantial fraction (62%) of patients. Both performance status and tumor grade have been shown to be prognostic indicators for renal cell cancer46 and could have contributed to the racial disparity observed in this study.

In conclusion, we found that nephrectomy rates were significantly lower among black renal cell cancer patients compared with similar whites. The lower rate of surgical treatment as well as a higher frequency of comorbidities among blacks explained a large proportion of the survival disparity between blacks and whites. Although the reasons for the disparity in treatment are not entirely clear and need to be examined in future studies, this study suggests black patients may benefit from efforts to improve the availability of health care and interventions to reduce comorbid illness.


    AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
The author(s) indicated no potential conflicts of interest.


    AUTHOR CONTRIBUTIONS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
Conception and design: Sonja I. Berndt, H. Ballentine Carter, Mark Schoenberg, Craig J. Newschaffer

Financial support: H. Ballentine Carter

Collection and assembly of data: Sonja I. Berndt, H. Ballentine Carter, Craig J. Newschaffer

Data analysis and interpretation: Sonja I. Berndt, Craig J. Newschaffer

Manuscript writing: Sonja I. Berndt

Final approval of manuscript: Sonja I. Berndt, H. Ballentine Carter, Mark Schoenberg, Craig J. Newschaffer


    ACKNOWLEDGMENTS
 
We thank the Applied Research Program, National Cancer Institute; the Office of Research, Development and Information, Centers for Medicare & Medicaid Services; Information Management Services Inc; and the Surveillance, Epidemiology, and End Results (SEER) Program tumor registries for their efforts in the creation of the SEER-Medicare database.


    NOTES
 
Supported by the Arguild Foundation and the Intramural Research Program of the National Cancer Institute, National Institutes of Health.

This study used the linked Surveillance, Epidemiology and End Results–Medicare database. The interpretation and reporting of these data are the sole responsibility of the authors.

Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
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11. Potosky AL, Riley GF, Lubitz JD, et al: Potential for cancer related health services research using a linked Medicare-tumor registry database. Med Care 31:732-748, 1993[Medline]

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20. Cox DR: Regression models and life tables (with discussion). J Roy Stat Soc B 34:187-220, 1972

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23. Greenwald HP, Polissar NL, Borgatta EF, et al: Social factors, treatment, and survival in early-stage non-small cell lung cancer. Am J Public Health 88:1681-1684, 1998[Abstract/Free Full Text]

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25. Cooper GS, Yuan Z, Landefeld CS, et al: Surgery for colorectal cancer: Race-related differences in rates and survival among Medicare beneficiaries. Am J Public Health 86:582-586, 1996[Abstract/Free Full Text]

26. Demissie K, Oluwole OO, Balasubramanian BA, et al: Racial differences in the treatment of colorectal cancer: A comparison of surgical and radiation therapy between Whites and Blacks. Ann Epidemiol 14:215-221, 2004[CrossRef][Medline]

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28. Jha AK, Fisher ES, Li Z, et al: Racial trends in the use of major procedures among the elderly. N Engl J Med 353:683-691, 2005[Abstract/Free Full Text]

29. Romano PS, Mark DH: Bias in the coding of hospital discharge data and its implications for quality assessment. Med Care 32:81-90, 1994[Medline]

30. Malenka DJ, McLerran D, Roos N, et al: Using administrative data to describe casemix: A comparison with the medical record. J Clin Epidemiol 47:1027-1032, 1994[CrossRef][Medline]

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32. Bach PB, Pham HH, Schrag D, et al: Primary care physicians who treat blacks and whites. N Engl J Med 351:575-584, 2004[Abstract/Free Full Text]

33. Groeneveld PW, Laufer SB, Garber AM: Technology diffusion, hospital variation, and racial disparities among elderly Medicare beneficiaries: 1989-2000. Med Care 43:320-329, 2005[CrossRef][Medline]

34. Schneider EC, Zaslavsky AM, Epstein AM: Racial disparities in the quality of care for enrollees in medicare managed care. JAMA 287:1288-1294, 2002[Abstract/Free Full Text]

35. Trivedi AN, Zaslavsky AM, Schneider EC, et al: Trends in the quality of care and racial disparities in Medicare managed care. N Engl J Med 353:692-700, 2005[Abstract/Free Full Text]

36. Oddone EZ, Horner RD, Diers T, et al: Understanding racial variation in the use of carotid endarterectomy: The role of aversion to surgery. J Natl Med Assoc 90:25-33, 1998[Medline]

37. Oddone EZ, Horner RD, Johnston DC, et al: Carotid endarterectomy and race: Do clinical indications and patient preferences account for differences? Stroke 33:2936-2943, 2002[Abstract/Free Full Text]

38. McCann J, Artinian V, Duhaime L, et al: Evaluation of the causes for racial disparity in surgical treatment of early stage lung cancer. Chest 128:3440-3446, 2005[CrossRef][Medline]

39. Margolis ML, Christie JD, Silvestri GA, et al: Racial differences pertaining to a belief about lung cancer surgery: Results of a multicenter survey. Ann Intern Med 139:558-563, 2003[Abstract/Free Full Text]

40. Doescher MP, Saver BG, Franks P, et al: Racial and ethnic disparities in perceptions of physician style and trust. Arch Fam Med 9:1156-1163, 2000[Abstract/Free Full Text]

41. Keating NL, Gandhi TK, Orav EJ, et al: Patient characteristics and experiences associated with trust in specialist physicians. Arch Intern Med 164:1015-1020, 2004[Abstract/Free Full Text]

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43. Cooper-Patrick L, Gallo JJ, Gonzales JJ, et al: Race, gender, and partnership in the patient-physician relationship. JAMA 282:583-589, 1999[Abstract/Free Full Text]

44. Birkmeyer JD, Siewers AE, Finlayson EV, et al: Hospital volume and surgical mortality in the United States. N Engl J Med 346:1128-1137, 2002[Abstract/Free Full Text]

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Submitted November 16, 2006; accepted May 25, 2007.





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