Original Article
Survival Disparities Among African American Women With Invasive Bladder Cancer in Florida Kathleen F. Brookfield, MD, PhD, MPH1; Michael C. Cheung, MD2; Christopher Gomez, MD3; Relin Yang, MD, MPH2; Alan M. Nieder, MD3; David J. Lee, PhD4; and Leonidas G. Koniaris, MD2
BACKGROUND: The authors sought to understand the effect of patient sex, race, and socioeconomic status (SES) on outcomes for bladder cancer. METHOD: The Florida Cancer Data System and the Agency for Health Care Administration data sets (1998-2003) were merged and queried. Survival outcomes for patients with bladder cancer were compared between different races, ethnicities, and community poverty levels. RESULTS: A total of 31,100 people with bladder cancer were identified. Overall median survival time was 62.7 months. Statistically significantly longer survival times were observed in men (62.8 months vs 62.3 months for women), whites (63.0 months vs 39.6 months for African Americans [AAs], P < .001), non-Hispanics (62.9 months vs 56.4 months for Hispanics, P < .001), and patients from more affluent communities (74.0 months where 15% live in poverty, P < .001). Surgery was associated with dramatically improved survival. AA women diagnosed with bladder cancer were significantly less likely to have endoscopic surgical resection compared with white women (P < .001). On multivariate analysis, independent predictors of poorer outcomes were older age, AA race, female sex, degree of community poverty, histologic tumor grade, advanced tumor stage, and lack of surgical treatment. CONCLUSIONS: Racial and SES disparities in bladder cancer survival were not fully explained by late-stage presentation and undertreatment. Although earlier diagnosis and greater access to surgery would likely yield some improvement in outcomes for AA women, more research is needed to understand C 2009 American Cancer the remaining survival gap for this population. Cancer 2009;115:4196–209. V Society. KEY WORDS: African Americans, bladder cancer, race, socioeconomic status.
Disparities in diagnosis, treatment, and outcome for cancers in African Americans (AAs) and whites have been documented over the past 30 years.1 The Annual Report to the Nation on the Status of Cancer (1975-2002) showed that the incidence of urinary bladder cancer deaths is highest for AA males (9.3 per 100,000), followed by white and Hispanic males (8.0 per 100,000) and AA females (2.8 per 100,000).2 Many studies demonstrating disparities in cancer outcomes among different races and ethnicities have pointed to a lack of screening and therefore delays in diagnosis and treatment.3-12 The increased risk of
Corresponding author: Leonidas G. Koniaris, MD, University of Miami School of Medicine, 3550 Sylvester Comprehensive Cancer Center, 1475 NW 12th Ave, Miami, FL 33136; Fax: (305) 243-7083;
[email protected] 1 Department of Obstetrics and Gynecology, University of Miami Miller School of Medicine, Miami, Florida; 2DeWitt Daughtry Family Department of Surgery, University of Miami Miller School of Medicine, Miami, Florida; 3Department of Urology, University of Miami, Miller School of Medicine, Miami, Florida; 4Department of Epidemiology and Public Health, University of Miami Miller School of Medicine, Miami, Florida
Received: October 9, 2008; Revised: February 2, 2009; Accepted: February 24, 2009 Published online June 30, 2009 in Wiley InterScience (www.interscience.wiley.com) DOI: 10.1002/cncr.24497, www.interscience.wiley.com
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death for AAs with bladder cancer has not so far been attributable to underutilization of cancer screening, as prior studies have demonstrated no effective screening method for this type of cancer. The literature describing survival differences between Hispanics and non-Hispanics is sparse relative to that published regarding AA survival.13-15 Underwood et al,15 Prout et al,14 and Lee et al13 found that after adjustment for demographic and clinical factors, AA women with bladder cancer had an increased risk of death compared with their white counterparts; however, none of these studies commented on survival outcomes for Hispanic women. Watson and Sidor,16 in contrast, reported decreased survival rates for Native Americans and Alaskan Natives with bladder cancer. The lack of data on survival outcomes for Hispanic women bears further exploration to examine whether or not they too are subject to presentation at a later stage relative to their white counterparts. Low socioeconomic status (SES) has also been linked to poor outcomes in cancer patients,16,17 with bladder cancer being no exception.15 A clear relationship exists between race and SES, as evidenced by the finding that the median income of whites in the United States was approximately 60% more than that of AAs in 2006.18 Additional factors implicated in survival disparities among racial and ethnic minorities and the poor are advanced stage at presentation,15,19-25 treatment differences,19-21,23,26,27 and comorbidities.27 Bladder cancer represents the fourth most common malignancy diagnosed in the United States among men and the 12th most common malignancy among women. Approximately 68,810 new cases of bladder cancer were expected to be diagnosed in 2008, with 14,100 deaths directly related to these types of tumors.28 We sought to examine differences in survival observed in patients with bladder cancer based on race, sex, and SES in an ethnically diverse population. Although studies thus far have demonstrated relatively consistent results pointing to decreased survival times for AAs, the current study further elucidates survival disparities by including ethnicity and evaluating the independent effects of race and SES in a population-based sample. We hoped by revisiting this topic using a large state cancer registry, we might identify possible points of intervention that will lead to improved survival in these groups. Cancer
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MATERIALS AND METHODS The 2007 Florida Cancer Data System (FCDS) data set was used to identify all incident cases of invasive bladder cancer diagnosed in the state of Florida from 1998-2002. Patients with carcinoma in situ and benign bladder neoplasms were excluded from the analysis. The FCDS data set was enhanced with 2007 data linked from the Florida Agency for Health Care Administration (AHCA) data set. AHCA maintains 2 databases (Hospital Patient Discharge Data and Ambulatory Outpatient Data) on all patient encounters within hospitals and freestanding ambulatory surgical and radiation therapy centers in Florida. All hospitals have been required to report all discharges and outpatient encounters to AHCA since 1987. The AHCA data sets used in this study contain diagnoses and procedures performed during every hospitalization or outpatient encounter in the state of Florida, for the period 1998-2003. The comorbidity data obtained from the AHCA data set allowed for better correction of covariates. Tobacco and alcohol consumption data are self-reported at the time of cancer diagnosis, and information on duration of use was not available. Cases in the FCDS and AHCA data sets were linked on the basis of unique identifiers.29,30 These matches were confirmed with the patient’s date of birth and sex. Postal codes listed in the FCDS-AHCA database were then used to determine community poverty levels according to the 2007 US Census Bureau report.31 Non-Florida residents were not included in the analysis, because follow-up for such patients, particularly survival information, may be inaccurate in up to 10% of such patients (FCDS personal communication). The University of Miami Miller School of Medicine Institutional Review Board approved this study. The staging criteria used by the FCDS are consistent with the Surveillance, Epidemiology, and End Results (SEER) summary staging. In this study, local staging represents disease that does not extend beyond the primary organ, whereas those having positive lymph nodes at the time of resection were classified as having regional disease. Documentation of distant metastases during the perioperative period led to classification of affected patients as having distant disease. Statistical analysis was performed with SPSS Statistical Package version 15.0 (SPSS Inc., Chicago, Ill). 4197
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Correlations between categorical variables were made using the chi-square test. Median survival rates were calculated by the Kaplan-Meier method. Because the FCDS collects only primary cause of death, we analyzed only overall survival and not disease-specific survival. Survival was calculated from the time of the initial diagnosis to date of last contact, or date of death, which was the time of censoring. The univariate effects of demographic, clinical, and treatment variables on survival were tested by the log-rank test for categorical values. To estimate the impact of race, ethnicity, and SES on survival outcomes, we used a Cox proportional hazards model, adding demographic, clinical, and treatment variables in a stepwise fashion.
RESULTS Patient Demographics and Clinical Characteristics Over the 5-year period studied, 31,100 patients with bladder cancer were identified. Demographics, social, and tumor characteristics of the entire study population, including subset analysis, are summarized in Table 1. The majority of the patients were men (n ¼ 23,432, 75.3%), white (n ¼ 29,734, 96.6%), and non-Hispanic (n ¼ 28,511, 92.6%). Most patients were also >65 years old (n ¼ 23,766, 76.4%) and were smokers (n ¼ 15,948, 64.7%). The majority of tumors were moderately differentiated (n ¼ 9981, 39.0%) or poorly differentiated (n ¼ 8232, 32.2%) in histology. Localized disease was most common (n ¼ 7758, 82.2%). Approximately 36.6% of the study population lived in a community where >10% of the area population was living below the poverty line.
Survival Median survival rates of the entire study population, including subset analyses, are summarized in Table 2. The median survival time (MST) for the entire cohort was 62.7 months. Significantly longer survival times were observed in younger patients at the time of diagnosis (median survival not yet reached vs 54.7 months for patients 66 years old, P < .001), men (62.8 months vs 62.3 months for women, P < .001), whites (63.0 months vs 39.6 months for AAs, P < .001), non-Hispanics (62.9 months vs 56.4 months for Hispanics, P ¼ .048), and 4198
patients who live in communities where 15% live in poverty, P < .001). Survival was significantly longer in patients who did not drink alcohol (63.5 months vs 53.8 months, P < .001), but was not significantly different for smokers compared with nonsmokers (62.2 months vs 62.1 months, P ¼ .895). Survival was significantly longer for patients with localized disease compared with distant disease (65.2 months vs 11.4 months, P < .001). Patients with well-differentiated tumors fared better than those with poorly differentiated tumors (median survival not reached vs 40.5 months, P < .001). Similarly, patients treated with only endoscopic surgical resection had significantly longer survival times than patients treated with open surgery or those who had no surgery (68.2 months vs 34.2 months vs 29.8 months, P < .001). This difference based upon surgical approach likely is because of differences in the use of laparoscopy versus open approaches based on tumor stage.
AAs Have Worse Survival Outcomes Compared with whites, AAs tended to be diagnosed at an earlier age and lived in communities with significantly higher levels of poverty (Table 1). A smaller percentage of AAs reported tobacco usage compared with their white counterparts. With respect to clinical characteristics, AAs presented with more regional and distant disease and had more poorly differentiated tumors compared with whites. A greater proportion of AAs diagnosed with bladder cancer underwent radiation or chemotherapy treatment compared with whites. Univariate subset analysis demonstrated that AA race conferred a significantly poorer prognosis for bladder cancer (Table 2). MST of AAs with bladder cancer was significantly shorter than for whites among men and women; however, differences in median survival were particularly disparate for black women (63.4 months for whites vs 25.5 months for AAs; P < .001). For all tumor stages and grades, MST for AA patients was significantly less than for whites. At all poverty level strata, AAs had a shorter MST than whites. Differences in treatment modality and outcomes between AA and white patients were also observed. Whereas more white patients underwent endoscopic surgical resection or open surgery (93.8% vs 88.1%), AA patients received more radiation therapy (6.6% vs 3.0%, Cancer
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Yes No
Tobacco use
Yes No
Alcohol use
15%
Community poverty level
Non-Hispanic Hispanic
Ethnicity
White AA Other
Race
Men Women
Sex
£40 41-65 ‡65
Age groups, y
Median age at diagnosis, y
15,948 8703
1098 28,044
8389 10,425 5146 5695
28,511 2270
29,734 899 148
23,432 7658
356 6968 23,766
72.4
No.
64.7 35.3
3.8 96.2
28.3 35.2 17.4 19.2
92.6 7.4
96.6 2.9 0.5
75.3 24.7
1.1 22.4 76.4
% of Total
Entire Cohort
65.1 34.9
3.7 96.3
28.8 35.6 17.5 18.1
92.6 7.4
— — —
76 24
1.1 22 76.9
72.5
White
55.5 44.5
4.9 95.1
13.1 19.6 13.1 54.2
96.2 3.8
— — —
64.3 35.7
2.9 32.9 64.3
68.7
AA
57.9 42.1
3.8 96.2
28.1 33.1 18.7 20.1
88.8 11.2
— — —
70.9 29.1
2 37.2 60.8
67.9
Other
Race, % of Total
