survival disparities among african american women with invasive bladder cancer in florida

Survival Disparities Among AfricanAmerican Women With InvasiveBladder Cancer in FloridaKathleen 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 <5% live in poverty vs 53.0 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

the remaining survival gap for this population. Cancer 2009;115:4196–209. VC 2009 American Cancer

Society.

KEY WORDS: African Americans, bladder cancer, race, socioeconomic status.

Disparities in diagnosis, treatment, and outcome for cancers in African Americans (AAs) and whiteshave 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 per100,000), 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 havepointed to a lack of screening and therefore delays in diagnosis and treatment.3-12 The increased risk of

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

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]

1Department 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

4196 Cancer September 15, 2009

Original Article

death for AAs with bladder cancer has not so far been at-tributable to underutilization of cancer screening, as priorstudies have demonstrated no effective screening methodfor 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 differen-

ces,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 dem-

onstrated 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.

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 Administra-

tion (AHCA) data set. AHCA maintains 2 databases

(Hospital Patient Discharge Data and Ambulatory Out-

patient Data) on all patient encounters within hospitals

and freestanding ambulatory surgical and radiation ther-

apy 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 rep-

resents 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 perioper-

ative period led to classification of affected patients as

having distant disease.

Statistical analysis was performed with SPSS Statisti-

cal Package version 15.0 (SPSS Inc., Chicago, Ill).

Disparities in Bladder Cancer/Brookfield et al

Cancer September 15, 2009 4197

Correlations between categorical variables were made

using the chi-square test. Median survival rates were calcu-

lated 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, clini-

cal, 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 ¼28,511, 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 differ-

entiated (n ¼ 9981, 39.0%) or poorly differentiated (n ¼8232, 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

patients who live in communities where<5% of the pop-

ulation dwell in poverty (74.0 months vs 53.0 months

where >15% live in poverty, P < .001). Survival was sig-

nificantly longer in patients who did not drink alcohol

(63.5 months vs 53.8 months, P< .001), but was not sig-

nificantly different for smokers compared with non-

smokers (62.2 months vs 62.1 months, P ¼ .895).

Survival was significantly longer for patients with local-

ized disease compared with distant disease (65.2 months

vs 11.4 months, P < .001). Patients with well-differenti-

ated tumors fared better than those with poorly differenti-

ated tumors (median survival not reached vs 40.5 months,

P < .001). Similarly, patients treated with only endo-

scopic 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 lapa-

roscopy 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 can-

cer underwent radiation or chemotherapy treatment com-

pared 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 pov-

erty 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 sur-

gical resection or open surgery (93.8% vs 88.1%), AA

patients received more radiation therapy (6.6% vs 3.0%,

Original Article


Table

1.Demographic,Social,andClinicalCharacteristicsofth

eStu

dyGro

upAccord

ingto

Race,Eth

nicity,andSocioeconomic

Statu

s

Entire

Cohort

Race,%

ofTotal

Sex,%

ofTotal

CommunityPovertyLevel,%

ofTotal

No.

%of

Total

White

AA

Other

PMen

Women

P<5

%5%-10%

10%-15%

>15%

P

Medianageatdiagnosis,y

72.4

72.5

68.7

67.9

<.001

72.3

72.8

.002

72.2

72.7

72.8

71.7

<.001

Agegroups,y

£40

356

1.1

1.1

2.9

2<.001

1.1

1.4

.015

1.1

1.1

1.2

1.4

<.001

41-65

6968

22.4

22

32.9

37.2

22.6

21.9

22.1

21

22.7

24.9

‡65

23,766

76.4

76.9

64.3

60.8

76.4

76.7

76.8

77.9

76.1

73.8

Sex Men

23,432

75.3

76

64.3

70.9

<.001

——

—76.8

75.7

74.5

72.7

<.001

Women

7658

24.7

24

35.7

29.1

——

23.2

24.3

25.5

27.3

Race

White

29,734

96.6

——

——

97.1

95.2

<.001

98.2

97.9

97.3

91.3

<.001

AA

899

2.9

——

—2.5

4.2

1.3

1.6

2.2

8.2

Other

148

0.5

——

—0.5

0.6

0.5

0.4

0.5

0.5

Ethnicity

Non-H

ispanic

28,511

92.6

92.6

96.2

88.8

<.001

92.4

93.3

.009

96.1

94.6

91.7

85.5

<.001

Hispanic

2270

7.4

7.4

3.8

11.2

7.6

6.7

3.9

5.4

8.3

14.5

Communitypovertylevel

<5%

8389

28.3

28.8

13.1

28.1

<.001

28.9

26.5

<.001

——

——

—

5%-10%

10,425

35.2

35.6

19.6

33.1

35.4

34.5

——

——

10%-15%

5146

17.4

17.5

13.1

18.7

17.2

17.9

——

——

>15%

5695

19.2

18.1

54.2

20.1

18.6

21.2

——

——

Alcoholuse

Yes

1098

3.8

3.7

4.9

3.8

.204

4.2

2.5

<.001

3.4

3.5

3.8

4.9

<.001

No

28,044

96.2

96.3

95.1

96.2

95.8

97.5

96.6

96.5

96.2

95.1

Tobaccouse

Yes

15,948

64.7

65.1

55.5

57.9

<.001

67.7

55.4

<.001

64.6

64.8

63.9

64.8

.794

No

8703

35.3

34.9

44.5

42.1

32.3

44.6

35.4

35.2

36.1

35.2 (C

ontinued)



Table

1.(C

ontinued)

Entire

Cohort

Race,%

ofTotal

Sex,%

ofTotal

CommunityPovertyLevel,%

ofTotal

No.

%of

Total

White

AA

Other

PMen

Women

P<5

%5%-10%

10%-15%

>15%

P

Tumorstage

Localized

7758

82.2

82.6

69.8

78.9

<.001

83

79.9

.001

84.4

83.1

81.4

80.7

.019

Regional

1110

11.8

11.5

18.5

18.4

11.4

12.7

10.6

11.2

12.9

12.4

Distant

572

6.1

5.9

11.7

2.6

5.6

7.4

55.6

5.7

7

Tumorgrade

Welldifferentiated

5437

21.3

21.3

18.6

23.1

<.001

20.6

23.2

<.001

21.6

21.2

22

21.2

<.001

Moderately

differentiated

9981

39.0

39.3

29.1

41.3

39.5

37.7

40

40.2

37.6

36.9

Poorlydifferentiated

8232

32.2

32

39.4

26.4

32.5

31.2

32.3

31.4

32.4

32.6

Undifferentiated

1935

7.6

7.4

12.9

9.1

7.4

86.1

7.3

7.9

9.2

Surgery

Endoscopic

resection

26,491

85.6

85.8

76.4

88.5

<.001

86.1

84

<.001

87.4

86.4

85.2

84

<.001

Opensurgery

2515

8.1

811.7

6.1

7.7

9.4

77.9

7.8

8.6

Nosurgery

1953

6.3

6.1

11.9

5.4

6.2

6.6

5.6

5.7

77.4

Chemotherapy

Yes

1920

6.3

6.2

9.1

7.002

6.1

6.8

.03

66.2

5.9

6.9

.092

No

28,507

93.7

93.8

90.9

93

93.9

93.2

94

93.8

94.1

93.1

Radiation

Yes

941

3.1

36.6

3.4

<.001

2.8

3.8

<.001

2.6

33.3

3.6

.012

No

29,834

96.9

97

93.4

96.6

97.2

96.2

97.4

97

96.7

96.4

AAindicatesAfricanAmerican.

Original Article


Table 2. Median Survival According to Race, Ethnicity, and Socioeconomic Status

EntireCohort

Median Survival, mo

Race Sex Community Poverty Level

Median

Survival,

mo

P White AA P Men Women P <5% 5%-10% 10%-15% >15% P

Age groups<40 NR <.001 NR NR .581 NR NR .550 NR NR NR NR .702

40-64 NR NR NR <.001 NR NR .485 NR NR NR NR <.001

‡65 54.7 NR NR <.001 55.2 53.3 <.001 62.2 55.1 51.4 45.6 <.001

SexMen 62.8 <.001 62.8 45.1 <.001 — — — 72.7 63.6 58.9 53.7 <.001

Women 62.3 63.4 25.5 <.001 — — — 76.1 62.8 59.4 51.5 <.001

RaceWhite 63.0 <.001 — — — 62.8 63.4 .002 73.9 63.4 59.5 54.0 <.001

AA 39.6 — — — 45.1 25.5 <.001 53.8 45.1 29.6 36.3 .079

EthnicityNon-Hispanic 62.9 .048 63.4 39.5 <.001 63.1 62.5 <.001 73.9 63.6 59.5 52.7 <.001

Hispanic 56.4 55.4 NR .603 56.7 54.3 .162 NR 53.7 54.8 56.7 .098

Communitypoverty level<5% 74.0 <.001 73.9 53.8 .026 72.7 76.1 .573 — — — — —

5%-10% 63.4 63.4 45.1 .003 63.6 62.8 .023 — — — — —

10%-15% 59.1 59.5 29.6 <.001 58.9 59.4 .018 — — — — —

>15% 53.0 54.0 36.3 <.001 53.7 51.5 .006 — — — — —

Alcohol useYes 53.8 <.001 53.7 53.6 .645 53.6 55.7 .631 57.6 58.1 51.4 44.3 .197

No 63.5 63.6 37.5 <.001 63.5 63.5 <.001 76.2 64.0 60.4 54.0 <.001

Tobacco useYes 62.2 .895 62.3 40.3 <.001 61.0 65.9 .949 72.1 60.9 60.5 53.6 <.001

No 62.1 63.0 33.2 <.001 64.4 55.7 <.001 77.2 63.6 56.0 50.1 <.001

Localized 65.2 <.001 65.3 44.3 <.001 65.9 64.4 .088 76.5 64.5 61.5 60.0 <.001

Regional 22.2 22.5 17.3 .261 23.7 18.5 .200 27.1 19.9 23.8 17.9 .015

Distant 11.4 12.0 5.7 .086 12.4 7.6 .348 9.6 12.3 8.5 10.1 .764

Tumor gradeWell differentiated NR <.001 NR NR .162 NR NR .029 NR NR NR 83.9 .004

Moderately

differentiated

76.9 76.9 63.1 <.001 76.2 80.8 .855 NR 73.1 70.0 70.1 <.001

Poorly differentiated 40.5 41.0 23.5 <.001 43.5 30.1 <.001 45.0 40.5 37.6 31.2 <.001

Undifferentiated 29.4 30.0 18.7 .001 32.6 23.5 .002 34.1 31.2 21.8 25.7 .003

SurgeryEndoscopic

resection

68.2 <.001 68.6 45.9 <.001 67.8 68.7 <.001 80.5 66.6 65.0 60.4 <.001

Open surgery 34.2 34.8 28.6 .277 33.8 36.3 .524 38.0 34.2 32.5 28.0 .055

No surgery 29.8 30.5 12.8 <.001 32.5 20.3 <.001 31.8 38.2 27.8 20.2 .007

ChemotherapyYes 27.5 <.001 27.8 18.0 <.001 29.4 21.7 .030 28.4 25.3 29.4 23.8 .077

No 64.9 65.1 41.2 <.001 64.7 65.1 <.001 76.5 65.1 61.5 56.8 <.001

RadiationYes 16.6 <.001 17.2 10.6 .003 18.0 14.7 .038 15.0 14.7 17.1 18.5 .074

No 64.9 65.0 41.5 <.001 64.6 65.4 <.001 76.7 65.0 61.5 56.2 <.001

AA indicates African American; NR, not reached.



P < .001) and chemotherapy (9.1% vs 6.2%; P ¼ .002).

Regardless of whether or not patients underwent endo-

scopic procedures, open surgical procedures, or no surgery

at all, AA patients had decreased survival times compared

with whites. Kaplan-Meier survival curves for white and

AA patients are shown in Figure 1a.

Sex Differences in Bladder Cancer

Cancer of the urinary bladder was diagnosed in men

almost 3 times more often than in women (Table 1). Male

patients used alcohol and tobacco with higher frequencies,

and had significantly higher proportions of localized

disease compared with women. Men more frequently

underwent endoscopic resection as opposed to open

surgery or no surgery at all compared with women. They

were also less likely to undergo chemotherapy or radiation

treatment for their cancer.

Differences in outcomes for male and female

patients were also observed in univariate subset analyses.

More women with bladder cancer lived in communities

with a >15% incidence of poverty compared with men

(21.2% vs 18.6%, P < .001) and they had a significantly

shorter MST than men. MST in female patients was

significantly longer than in male patients who underwent

endoscopic resection (68.7 months vs 67.8 months,

P< .001).

Effects of Area Poverty on Prognosis of

Bladder Cancer

Patients living in communities with>15% of the popula-

tion living in poverty were more frequently younger,

women, AA, Hispanic, and alcohol users compared with

patients living in more affluent communities (Table 1).

Patients living at greater poverty levels tended to have can-

cers that were more poorly differentiated, and had open

surgery or no surgery at all as opposed to endoscopic

resections, when compared with communities where

<5% of the population lived in poverty. Univariate analy-

sis demonstrated that community poverty level also affects

MST in bladder cancer. Communities with greater

percentages of the population living in poverty had signif-

icantly worse survival outcomes compared with commun-

ities with less poverty. For patients >65 years old, MST

decreased significantly with increasing poverty level.

Patients from communities where >15% of the popula-

tion lives in poverty more frequently presented with

advanced-stage disease compared with patients living in

communities with a smaller proportion of poverty.

FIGURE 1. Kaplan-Meier survival curves are shown (a) for white and African American patients and (b) by area poverty level.

Original Article


Patients living in communities with the greatest amount

of poverty were less likely to undergo endoscopic resection

of their bladder cancer, and among all patients under-

going endoscopic procedures, those patients living in the

poorest communities experienced worse survival out-

comes compared with patients living in communities with

the least amount of poverty (60.4 months vs 80.5 months;

P < .001). Kaplan-Meier survival curves by area poverty

level are shown in Figure 1b.

Tobacco

Whites diagnosed with bladder cancer were significantly

more likely to use tobacco compared with AAs (65.1% vs

55.5%, P < .001), and men diagnosed with bladder can-

cer were significantly more likely to use tobacco compared

with women (67.7% vs 55.4%, P< .001). The survival of

white smokers was significantly longer than that of their

AA counterparts (62.3 months vs 40.3 months, P <

.001). A survival advantage was also observed in whites

who did not smoke when compared with AA nonsmokers

(63.0 months vs 33.2 months, P < .001). Women who

used tobacco had longer MST than men who used

tobacco; however, this result was not statistically signifi-

cant (65.9 months vs 61.0 months, P ¼ .949). Smoking

was not an effect modifier for race or sex. Among smokers

and nonsmokers, women who lived in communities with

>15% of the population living in poverty had signifi-

cantly diminished median survival times.

Comorbidities in Bladder Cancer

The frequency of comorbidities in the study population is

shown in Table 3. The most frequent comorbidity was

hypertension (61.4%), whereas the most infrequent ill-

ness observed was human immunodeficiency virus/

acquired immune deficiency syndrome (HIV/AIDS)

(0.2%). Compared with whites, AAs were more likely to

be diagnosed with hypertension, diabetes, renal failure,

liver disease, HIV/AIDS, anemia, and fluid and electro-

lyte disorders in addition to bladder cancer. Women were

more often diagnosed with hypothyroidism, obesity,

weight loss, anemia, depression, and fluid and electrolyte

imbalances. Patients living in less affluent areas were more

often diagnosed with congestive heart failure, hyperten-

sion, paralysis, pulmonary diseases, diabetes, renal failure,

liver disease, obesity, weight loss, anemia, and depression.

By univariate analysis, all listed comorbid conditions

significantly affected MST, with the exception of

hypertension and AIDS/HIV.

Multivariate Analysis

Results of multivariate analysis using the Cox regression

model are summarized in Table 4. Independent predictors

of survival of bladder cancer in the final model included

age >65 years, AA race, female sex, community poverty

level, histologic tumor grade, tumor stage, and surgical

treatment. No differences were observed between

ethnicity, alcohol consumption, tobacco usage, and

chemotherapy.

AA patients were 27% more likely to die during the

study period compared with white patients (P < .001),

and women were 11% more likely to die during the study

period compared with men (P < .001). Patients living in

areas where >15% of the residents live in poverty were

17% more likely to die during the study compared with

patients living in areas where <5% of the residents live in

poverty (P ¼ .001). Clinical and treatment characteristics

proved to have the largest effect on survival outcomes.

Patients with regional disease were 1.53 times more likely

to die during the study period, and patients with distant

disease were 2.73 times more likely to die during the study

period compared with patients with localized disease (P<

.001). A dose-response effect was observed between tumor

grade and risk of death during the study period. Patients

with poorly differentiated tumors were 2.18 times more

likely to die during the study period compared with

women with well-differentiated tumors. Patients who

were not treated surgically had a 51% increased risk of

death compared with those who received any surgical

therapy (P < .001). Those who did not receive radiation

treatment had a 34% decreased risk of death compared

with patients who received radiation therapy (P< .001).

DISCUSSION

Differences in cancer survival based on race, ethnicity,

and SES remain a major issue despite recognition of these

inequalities for>30 years. In an effort to understand out-

comes for bladder cancer patients and potentially improve

survival, we examined a population-based registry to



Table

3.ElixhauserComorb

iditiesAccord

ingto

Race,Sex,andSES

Frequency

MedianSurvival

Overall,

%Race,%

Sex,%

PovertyLevel,%

Present,

mo

Not

Present,

mo

P

White

AA

Other

PMen

Women

P<5

%5%-10%

10%-15%

>15%

P

Congestiveheartfailure

20.6

22.08

23.20

15.04

.109

22.9

19.4

<.001

20.0

22.0

23.6

23.9

<.001

39.5

77.5

<.001

Cardiacarrhythmias

31.6

34.08

26.56

22.56

<.001

35.6

28.2

<.001

33.2

34.2

34.5

33.0

.184

48.7

78.8

<.001

Valvulardisease

19.7

21.25

14.06

15.04

<.001

21.9

18.0

<.001

21.3

21.1

21.3

19.9

.183

55.0

66.3

<.001

Pulm

onary

circulationdisorders

2.7

2.88

3.73

1.50

.226

2.9

3.0

.688

2.9

2.8

3.0

3.1

.687

37.4

64.1

<.001

Peripheralvasculardisease

15.7

16.95

12.62

14.29

.003

18.1

12.7

<.001

16.1

17.1

17.6

16.6

.096

54.5

65.1

<.001

Hypertension

61.4

65.35

73.80

65.41

<.001

65.8

64.5

.047

64.1

65.9

66.1

66.1

.028

60.8

67.3

.262

Paralysis

2.8

2.99

3.97

1.50

.160

3.1

2.8

.268

2.6

2.9

3.1

3.6

.008

38.0

64.2

<.001

Neurologicaldisorders

9.2

9.81

11.30

7.52

.244

10.2

8.7

<.001

9.5

9.9

9.5

10.5

.249

38.9

68.6

<.001

Chronic

pulm

onary

disease

39.1

42.00

37.62

31.58

.002

43.4

36.7

<.001

37.9

41.1

43.9

46.3

<.001

50.1

78.5

<.001

Diabetes,uncomplicated

20.4

21.44

31.01

29.32

<.001

23.2

17.4

<.001

20.2

21.9

22.3

23.4

<.001

58.1

64.4

<.001

Diabetes,complicated

5.0

5.26

8.65

4.51

<.001

5.7

4.4

<.001

5.1

5.3

5.4

5.9

.184

45.1

64.4

<.001

Hypothyroidism

8.8

9.53

5.29

9.02

<.001

6.5

18.2

<.001

9.7

9.5

9.2

8.9

.384

58.7

63.5

.004

Renalfailure

11.6

12.11

21.88

13.53

<.001

13.2

9.8

<.001

10.8

12.1

13.2

14.4

<.001

33.3

72.1

<.001

Liverdisease

13.1

13.88

20.55

14.29

<.001

14.3

13.1

.010

13.1

13.7

14.1

15.8

<.001

39.9

67.0

<.001

Pepticulcerdisease

4.0

4.22

4.33

4.51

.975

4.3

4.0

.250

4.0

4.2

4.5

4.3

.606

54.2

63.5

.003

AIDS/H

IV0.2

0.15

0.72

0.00

<.001

0.2

0.1

.582

0.2

0.1

0.1

0.2

.750

67.3

62.9

.760

Lymphoma

1.7

1.90

1.32

1.50

.462

1.9

1.7

.403

1.8

1.9

2.1

1.6

.393

41.0

63.6

<.001

Rheumatoid

arthritis/collagen

vasculardisease

22.8

24.42

24.04

23.31

.928

24.2

24.8

.295

24.4

23.2

25.8

24.8

.003

67.0

60.8

<.001

Coagulopathy

7.7

8.19

9.38

6.02

.308

8.5

7.1

<.001

7.9

8.3

7.9

8.6

.508

35.2

67.2

<.001

Obesity

5.3

5.58

8.05

4.51

.008

5.3

6.6

<.001

4.9

5.7

5.8

6.3

.004

73.0

62.2

<.001

Weightloss

8.7

9.16

13.82

11.28

<.001

9.0

10.0

.010

8.1

9.0

9.7

10.9

<.001

31.1

69.2

<.001

Fluid

andelectrolyte

disorder

31.3

33.08

45.07

35.34

<.001

32.1

37.1

<.001

29.6

33.7

34.1

37.3

<.001

33.6

NA

<.001

Bloodlossanemia

7.0

7.27

14.30

7.52

<.001

7.2

8.3

.002

6.4

7.4

7.5

8.7

<.001

32.8

66.2

<.001

Anemia,deficiency

5.0

4.92

9.98

3.01

<.001

4.7

6.0

<.001

4.5

5.2

4.9

5.7

.014

47.5

64.0

<.001

Drugabuse

1.9

2.02

1.80

0.75

.531

2.1

1.8

.217

1.8

2.0

1.9

2.4

.066

52.2

63.2

.015

Psychoses

4.8

5.13

5.17

2.26

.323

5.1

5.1

.911

5.4

4.9

4.8

5.3

.354

76.0

62.2

<.001

Depression

8.9

9.58

7.81

6.02

.090

8.6

12.3

<.001

8.6

9.2

10.5

10.6

<.001

43.6

66.1

<.001

SESindicatessocioeconomic

status;AA,AfricanAmerican;AIDS/H

IV,humanim

munodeficiencyvirus/acquiredim

munedeficiencysyndrome.

Original Article


identify global prognostic factors important in the survival

of patients diagnosed with urinary bladder cancer. In this

analysis, emphasis was placed on the effects of race, sex,

and area poverty level on overall survival. Although our

report is consistent with others that have also found racial

and socioeconomic disparities in cancer, this study is

unique in that patients from all age groups, Hispanics and

non-Hispanics, as well as their comorbid conditions, were

included in the analysis. To our knowledge, this study

represents the largest, most comprehensive analysis of

Table 4. Multivariate Regression Analyses*

HR Lower Upper P

Age groups<40 (reference group)

40-64 1.04 0.671 1.600 .872

‡65 1.77 1.150 2.720 .009

RaceCaucasian (reference group)

African American 1.27 1.110 1.450 <.001

SexMen (reference group)

Women 1.11 1.040 1.180 <.001

EthnicityNon-Hispanic (reference group)

Hispanic 0.99 0.895 1.100 .890

Community poverty level<5% (reference group)

5%-10% 1.09 1.030 1.170 .006

10%-15% 1.11 1.020 1.200 .011

>15% 1.17 1.090 1.260 <.001

Alcohol useYes (reference group)

No 0.98 0.869 1.100 .675

Tobacco useYes (reference group)

No 0.99 0.936 1.040 .681

Tumor stageLocalized (reference group)

Regional 1.53 1.380 1.710 <.001

Distant 2.73 2.370 3.140 <.001

Tumor gradeWell differentiated (reference group)

Moderately differentiated 1.19 1.100 1.300 <.001

Poorly differentiated 2.18 2.010 2.370 <.001

Undifferentiated 2.46 2.210 2.740 <.001

SurgeryEndoscopic resection (reference group)

Open surgery 1.10 1.000 1.200 .043

No 1.51 1.350 1.680 <.001

ChemotherapyYes (reference group)

No 0.91 0.830 1.000 .051

RadiationYes (reference group)

No 0.66 0.593 0.740 <.001

HR indicates hazard ratio.

* Regression model includes patient comorbidities as categorical variables.



these variables on the outcomes of patients with bladder

cancer to date.

We observed that after controlling for sociodemo-

graphic, clinical, and treatment characteristics, as well as

comorbidities, race, sex, and poverty were independent

predictors of urinary bladder cancer survival. With respect

to race, these results are supported by previous studies that

lacked comorbidity data.13-15,32 Prior published studies

examining racial and gender disparities in bladder cancer

have included data on patients diagnosed over many deca-

des. The results of the current study suggest that despite

the knowledge of existing disparities, little progress in

improving survival of urinary bladder cancer has been

made. In the cohort reported herein, AA patients had sig-

nificantly more regional and distant disease and more

poorly differentiated tumors compared with their white

counterparts. AAs and women were also significantly less

likely to have endoscopic resection compared with their

white and male counterparts. Our comorbidity data did

not indicate that AAs were more likely to be of increased

operative risk secondary to poor health; however, the

findings of more advanced disease at presentation may

indicate that the extent of disease made these patients

more likely to be inoperable at time of diagnosis, leading

to more frequent use of chemotherapy or radiation

treatment.

Survival of AA patients who underwent endoscopic

resection was significantly shorter than that of whites by

univariate analysis, whereas no difference in survival was

noted with open procedures. After controlling for socio-

demographic variables and clinical disease characteristics

in multivariate analysis, endoscopic resection was associ-

ated with superior outcomes. These results indicate that

for patients who receive surgical treatment for urothelial

cancer, race, sex, and poverty were all independent predic-

tors of survival. In part because bladder cancer is 3 times

less common in women than in men, many health practi-

tioners may overlook presenting symptoms of bladder

cancer in women and reflexively attribute hematuria to

cystitis or a variety of gynecologic pathologies. The find-

ings of our study indicate that poor survival outcomes,

particularly for AA women, regardless of poverty level, are

at least in part the result of delays in diagnosis and treat-

ment, or less than adequate treatment, and presentation

of illness in advanced stages. These findings are particu-

larly troubling considering that the incidence of bladder

cancer in AA women is increasing. Previous studies from

the 1980s and 1990s have also demonstrated that there is

often a delay in diagnosis of bladder cancer, especially for

women compared with men.33,34

In a much smaller study, Prout et al14 found that

black patients working in the most affluent occupations

did not significantly differ in terms of survival compared

with whites. Our study results suggest patients living in

communities with>15% of the population living in pov-

erty had significantly decreased MST compared with

patients living in communities with less poverty, even

when they had surgical treatment for their bladder cancer.

After adjustment for confounding variables in the multi-

variate analysis, community poverty level continued to be

an independent predictor of survival. These results suggest

that when socioeconomically disadvantaged patients with

bladder cancer are treated, their survival outcomes con-

tinue to be poorer relative to those of patients living in

more affluent communities. Our findings are likely more

robust, as we included a larger and more heterogeneous

population of patients. Much like the association between

AA race and survival, these results likely indicate poorer

patients may be subject to incomplete follow-up of physi-

cian visits and treatment.

The American Cancer Society (ACS) has suggested

that low SES in AAs is responsible for many inequalities.35

Moreover, the ACS, in collaboration with the National

Cancer Institute and Center for Disease Control, issued a

landmark report highlighting the key issues.36 The poor

were found to have worse outcomes because of financial

hardship and lack of insurance, and therefore poor access

to healthcare. This report also suggested that the poor

endured more pain and suffering when diagnosed with

cancer and that they did not benefit from cancer educa-

tion and outreach programs. Finally, the report suggested

that poor patients regard cancer diagnoses with a sense of

resignation and futility, and therefore are less likely to

seek medical treatment.36 In our final Cox regression

model, race, sex, and poverty remained independent

predictors of survival, along with lack of surgical

treatment for bladder cancer.

In light of the finding that access to care has been

highlighted as a major factor affecting cancer survival,

many organizations have increased their efforts to level

the playing field in the burden of cancer. The ACS has

made this issue the centerpiece of their goal to be attained

Original Article


by the year 2015,37 and the US Department of Health

and Human Services has made a commitment to reduce

cancer disparities with the Healthy People 2010 initiative.

These efforts are primarily focused on modifiable, socioe-

conomic factors such as poverty level, education, and

healthcare. The results of our study suggest programs that

increase the likelihood of AAs and the poor to seek treat-

ment and education programs aimed at better compliance

with treatment programs may have the most substantial

impact on bladder cancer survival.

Although significant differences in survival by race

and SES were observed, no survival disparities were

observed for Hispanic men and women with bladder can-

cer. No significant difference in survival times was

observed relative to white non-Hispanic patients. Ethnic-

ity also failed to reach significance in the final multivariate

regression model. Previous studies examining bladder

cancer survival have not commented on possible ethnic

differences outside that of the Native American and

Native Alaskan populations.16 Although only 7.4% of our

sample identified themselves as Hispanic, this observation

may reflect the finding that ethnicity does not play as large

a role as race or sex in predicting bladder cancer survival.

In addition, the predominately Cuban population of

South Florida has been shown to have more favorable

health outcomes relative to other Hispanics, and therefore

these results may not be generalizable to other Hispanic

subgroups, such as Mexican Americans. These results may

also point to improving awareness of signs and symptoms

of bladder cancer in the Hispanic population and earlier

identification of the disease at more treatable stages. Previ-

ously we have also failed to observe disparate outcomes for

Florida Hispanics for several other cancers.29,38,39

We have provided the most comprehensive analysis

of bladder cancer to date using a linked FCDS and

AHCA database. This linkage dramatically improved the

power of the study, as it provided additional data such as

comorbidities, enhanced follow-up, socioeconomic infor-

mation, and improved treatment information. Our study

was restricted to 1998-2003, as linkage of these data sets

was not possible in data sets for prior years. The FCDS,

which currently includes over 2.7 million records, is a

population-based registry of all cancer cases diagnosed or

treated in the state of Florida, which represents about 6%

of the total US population. The data collected from large

cancer registries provide insight into tumor behavior and

allow us to examine outcomes from current treatment

strategies.40-45 Although this represents an excellent data-

base for comparative outcomes analysis, it is not without

limitations. By using area poverty as a proxy for SES may

result in misclassification of some patients whose postal

codes do not accurately reflect the true income level of the

individual. In addition, FCDS records only primary cause

of death; as a result, we were unable to include disease-

specific survival in our examination. Furthermore,

although data on radiotherapy and chemotherapy were

examined, information on specific regimens and dosages

were also not available.

In conclusion, after controlling for socioeconomic

factors, clinical characteristics, and treatment modality,

we demonstrate significant racial, gender, and SES dispar-

ities exist in bladder cancer survival. The inequalities were

observed in both the univariate and multivariate analysis.

Programs geared toward diminishing disparities in blad-

der cancer survival should be aimed both at providing ear-

lier diagnosis and assuring optimal delivery of therapies,

including increased use of minimally invasive surgical

treatment to patients, particularly AAs and women whose

diagnosis is often under-recognized.

Conflict of Interest Disclosures

Supported in part by a grant from the James and Ester KingTobacco Grant from the State of Florida.

References

1. Henschke UK, Leffall LD Jr, Mason CH, et al. Alarmingincrease of the cancer mortality in the U.S. black popula-tion (1950-1967). Cancer. 1973;31:763-768.

2. Surveillance, Epidemiology and End Results (SEER) Pro-gram. Bethesda, MD: National Cancer Institute; 2005.

3. Carey P, Gjerdingen DK. Follow-up of abnormal Papani-colaou smears among women of different races. J FamPract. 1993;37:583-587.

4. Chang SW, Kerlikowske K, Napoles-Springer A, et al.Racial differences in timeliness of follow-up after abnormalscreening mammography. Cancer. 1996;78:1395-1402.

5. Eley JW, Hill HA, Chen VW, et al. Racial differences insurvival from breast cancer. Results of the National CancerInstitute Black/White Cancer Survival Study. JAMA.1994;272:947-954.

6. Hegarty V, Burchett BM, Gold DT, Cohen HJ. Racial dif-ferences in use of cancer prevention services among olderAmericans. J Am Geriatr Soc. 2000;48:735-740.

7. Liu WL, Kasl S, Flannery JT, et al. The accuracy of pros-tate cancer staging in a population-based tumor registry



and its impact on the black-white stage difference (Con-necticut, United States). Cancer Causes Control. 1995;6:425-430.

8. McCarthy BD, Yood MU, Boohaker EA, et al. Inadequatefollow-up of abnormal mammograms. Am J Prev Med.1996;12:282-288.

9. Optenberg SA, Thompson IM, Friedrichs P, et al. Race,treatment, and long-term survival from prostate cancer inan equal-access medical care delivery system. JAMA.1995;274:1599-1605.

10. Shavers VL, Brown ML. Racial and ethnic disparities in thereceipt of cancer treatment. J Natl Cancer Inst. 2002;94:334-357.

11. Suarez L, Pulley L. Comparing acculturation scales andtheir relationship to cancer screening among older Mexi-can-American women. J Natl Cancer Inst Monogr. 1995;(18):41-47.

12. Sung HY, Kearney KA, Miller M, et al. Papanicolaousmear history and diagnosis of invasive cervical carcinomaamong members of a large prepaid health plan. Cancer.2000;88:2283-2289.

13. Lee CT, Dunn RL, Williams C, Underwood W III.Racial disparity in bladder cancer: trends in tumor presenta-tion at diagnosis. J Urol. 2006;176:927-933; discussion933-934.

14. Prout GR Jr, Wesley MN, Greenberg RS, et al. Bladdercancer: race differences in extent of disease at diagnosis.Cancer. 2000;89:1349-1358.

15. Underwood W III, Dunn RL, Williams C, Lee CT.Gender and geographic influence on the racial disparity inbladder cancer mortality in the US. J Am Coll Surg.2006;202:284-290.

16. Watson RA, Sidor M. Bladder cancer in Native Americansand Alaskan Natives. Urology. 2008;72:10-14.

17. Zell JA, Cinar P, Mobasher M, et al. Survival for patientswith invasive cutaneous melanoma among ethnic groups:the effects of socioeconomic status and treatment. J ClinOncol. 2008;26:66-75.

18. DeNavas-Walt C, Proctor BD, Smith J. Income, Poverty,and Health Insurance Coverage in the United States: 2006.Washington, DC: U.S. Census Bureau; 2006.

19. Brooks SE, Baquet CR, Gardner JF, et al. Cervicalcancer—the impact of clinical presentation, health and raceon survival. J Assoc Acad Minor Phys. 2000;11:55-59.

20. del Carmen MG, Montz FJ, Bristow RE, et al. Ethnicdifferences in patterns of care of stage 1A and stage 1Acervical cancer: a SEER database study. Gynecol Oncol.1999;75:113-117.

21. Howell EA, Chen YT, Concato J. Differences in cervicalcancer mortality among black and white women. ObstetGynecol. 1999;94:509-515.

22. Jones WB, Shingleton HM, Russell A, et al. Patterns ofcare for invasive cervical cancer. Results of a national surveyof 1984 and 1990. Cancer. 1995;76(10 suppl):1934-1947.

23. Leath CA III, Straughn JM Jr, Kirby TO, et al. Predictorsof outcomes for women with cervical carcinoma. GynecolOncol. 2005;99:432-436.

24. Mandelblatt J, Andrews H, Kerner J, et al. Determinants oflate stage diagnosis of breast and cervical cancer: the impactof age, race, social class, and hospital type. Am J PublicHealth. 1991;81:646-649.

25. Mitchell JB, McCormack LA. Time trends in late-stagediagnosis of cervical cancer. Differences by race/ethnicityand income. Med Care. 1997;35:1220-1224.

26. Eifel PJ, Moughan J, Owen J, et al. Patterns of radiother-apy practice for patients with squamous carcinoma of theuterine cervix: patterns of care study. Int J Radiat OncolBiol Phys. 1999;43:351-358.

27. Mundt AJ, Connell PP, Campbell T, et al. Race and clini-cal outcome in patients with carcinoma of the uterine cer-vix treated with radiation therapy. Gynecol Oncol. 1998;71:151-158.

28. Cancer Facts & Figures 2008. Atlanta, GA: American Can-cer Society; 2008.

29. Brookfield KF, Cheung MC, Lucci J, Fleming LE, KoniarisLG. Disparities in survival among women with invasivecervical cancer: a problem of access to care. Cancer.2009;115:166-178.

30. Molina MA, Cheung MC, Perez EA, et al. African Ameri-can and poor patients carry a dramatically worse prognosisfor head and neck cancer: an examination of 20,915patients. Cancer. 2008;113:2797-2806.

31. DeNavas-Walt C, Proctor B, Mills R. Current PopulationReports. Washington, DC: US Census Bureau; 2007:P60-P226.

32. Nieder AM, Mackinnon JA, Huang Y, et al. Floridabladder cancer trends 1981 to 2004: minimal progress indecreasing advanced disease. J Urol. 2008;179:491-495;discussion 495.

33. Mansson A, Anderson H, Colleen S. Time lag to diagnosisof bladder cancer—influence of psychosocial parametersand level of health-care provision. Scand J Urol Nephrol.1993;27:363-369.

34. Mommsen S, Aagaard J, Sell A. Presenting symptoms,treatment delay and survival in bladder cancer. Scand JUrol Nephrol. 1983;17:163-167.

35. Special Report on Cancer in the Economically Disadvan-taged. Atlanta, GA: American Cancer Society; 1986.

36. Cancer in the Poor: A Report to the Nation. Atlanta, GA:American Cancer Society; 1989.

37. Byers T, Mouchawar J, Marks J, et al. The AmericanCancer Society challenge goals. How far can cancer ratesdecline in the US by the year 2015? Cancer. 1999;86:715-727.

38. Cheung MC, Hamilton K, Sherman R, et al. Impact ofteaching facility status and high-volume centers on out-comes for lung cancer resection: an examination of 13,469surgical patients. Ann Surg Oncol. 2009;16:3-13.

Original Article


39. Gutierrez JC, Hurley JD, Housri N, et al. Are many com-munity hospitals undertreating breast cancer?: lessons from24,834 patients. Ann Surg. 2008;248:154-162.

40. Cheung MC, Perez EA, Molina MA, et al. Defining therole of surgery for primary gastrointestinal tract melanoma.J Gastrointest Surg. 2008;12:731-738.

41. Gutierrez JC, Perez EA, Moffat FL, et al. Should soft tissuesarcomas be treated at high-volume centers? An analysis of4205 patients. Ann Surg. 2007;245:952-958.

42. Hodgson N, Koniaris LG, Livingstone AS, Franceschi D.Gastric carcinoids: a temporal increase with proton pumpintroduction. Surg Endosc. 2005;19:1610-1612.

43. Perez EA, Gutierrez JC, Jin X, et al. Surgical outcomes ofgastrointestinal sarcoma including gastrointestinal stromaltumors: a population-based examination. J Gastrointest Surg.2007;11:114-125.

44. Perez EA, Koniaris LG, Snell SE, et al. 7201carcinoids: increasing incidence overall and dispro-portionate mortality in the elderly. World J Surg. 2007;31:1022-1030.

45. Perez EA, Livingstone AS, Franceschi D, et al. Currentincidence and outcomes of gastrointestinal mesenchymaltumors including gastrointestinal stromal tumors. J Am CollSurg. 2006;202:623-629.



survival disparities among african american women with invasive bladder cancer in florida

Documents