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American Journal of Epidemiology Advance Access originally published online on April 9, 2007
American Journal of Epidemiology 2007 166(1):71-78; doi:10.1093/aje/kwm052
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American Journal of Epidemiology Copyright © 2007 by the Johns Hopkins Bloomberg School of Public Health All rights reserved; printed in U.S.A.

ORIGINAL CONTRIBUTIONS

Differences in Prognostic Factors and Survival among White Men and Black Men with Prostate Cancer, California, 1995–2004

Anthony S. Robbins, Daixin Yin and Arti Parikh-Patel

From the California Cancer Registry, Public Health Institute, Sacramento, CA

Correspondence to Dr. Anthony S. Robbins, California Cancer Registry, 1700 Tribute Road, Suite 100, Sacramento, CA 95815-4402 (e-mail: arobbins{at}ccr.ca.gov).

Received for publication October 4, 2006. Accepted for publication January 5, 2007.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The authors conducted a study to determine whether differences in prostate cancer survival between White men and Black men are reduced or eliminated after accounting for differences in prognostic factors. Using population-based statewide cancer registry data, the authors analyzed data from a cohort of 122,375 non-Hispanic White men and Black men from California who were newly diagnosed with prostate cancer between 1995 and 2004 and followed through 2004. Compared with White men, Black men were characterized by younger age at diagnosis, more distant stage, less treatment with surgery or radiation therapy, higher tumor grades, lower neighborhood socioeconomic status, and more recent year of diagnosis. Adjusted only for age, the hazard ratio for prostate cancer death (Blacks vs. Whites) was 1.61 (95% confidence interval (CI): 1.50, 1.72). Additional adjustment for potentially modifiable factors (stage and treatment) eliminated most of the racial difference in survival (adjusted hazard ratio = 1.10, 95% CI: 1.03, 1.18). The racial difference in survival was completely eliminated after further adjustment for other factors (grade, socioeconomic status, and year of diagnosis) (adjusted hazard ratio = 0.99, 95% CI: 0.92, 1.06). Thus, the large difference in prostate cancer survival between White men and Black men was completely explained by known prognostic factors, with potentially modifiable disparities playing the largest role.

African Americans; carcinoma; ethnology; prostatic neoplasms; registries; survival analysis

Abbreviations: AJCC, American Joint Committee on Cancer; CI, confidence interval; HR, hazard ratio; ICD-O-2, International Classification of Diseases for Oncology, Second Edition; SEER, Surveillance, Epidemiology, and End Results


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Prostate cancer exhibits some of the largest differences between Whites and Blacks in incidence, mortality, and survival seen for any cancer site (1). These differences have been consistently observed for over 30 years, across a variety of geographic regions and different health-care delivery systems. Some factors offered as potential explanations for survival disparities between White men and Black men include differences in patient characteristics (age, competing causes of death, socioeconomic status, genetic factors), tumor characteristics (stage, grade), and treatment. The question of whether racial differences in prostate cancer survival can be explained by known risk factors has major public health and research implications but has not been settled, with roughly half the studies concluding that the differences can be explained and half concluding that they cannot (2–24). For example, one study found that racial survival differences were eliminated among men treated with surgery (11), while another reported that racial differences were greatest among men treated with surgery (14). Limitations of some prior studies include the following: use of older data, that is, pre-1988 cases; restrictions by age and stage; lack of data on treatment or cause of death; and use of small or non-population-based samples. Mixing of cases diagnosed before and after 1988 is not advisable, because of the dramatic changes in incidence, stage, grade, and survival seen after the introduction of prostate-specific antigen screening.

A meta-analysis published in 2002 examined racial survival differences for all major cancer sites and attempted to remove confounding by stage, treatment, and competing causes of death (25). However, the investigators were forced to use national mortality data to estimate and subtract the risk of noncancer death, rather than using actual data from subjects in the individual studies. For prostate cancer, results of the meta-analysis suggested that racial differences in survival could be explained by differences in stage, treatment, and noncancer causes of death.

In an effort to overcome the limitations of prior studies, we analyzed data from all non-Hispanic White men and Black men diagnosed with incident prostate cancer in the state of California between 1995 and 2004 (n = 122,375). The present study was designed to simultaneously evaluate the role of patient characteristics, tumor characteristics, and treatment, while also accounting for racial differences in competing causes of death. Unlike the prior meta-analysis, our analysis used patient-level cause-of-death data from all patients who died, rather than group-level estimates derived from national vital statistics, to account for differences in noncancer mortality. Completeness of follow-up for vital status through 2004 was close to 100 percent. Thus, the study appears to be unique in incorporating all of the following features: very large sample size, only recently diagnosed cases, population-based case finding, no restrictions by age or stage, assessment of all major prognostic factors including treatment, and nearly complete ascertainment of the endpoint (prostate cancer death).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Study population
Prostate cancer cases were identified through the California Cancer Registry, a population-based registry that has collected cancer incidence data for the entire population of California since 1988 through a system of regional registries. With the state's population at 33.9 million in the 2000 US Census (26), nearly 140,000 cases of invasive cancer are added to the Registry each year; data on over 2.2 million invasive cases have been collected since 1988. The California Cancer Registry is a participant in the National Cancer Institute's Surveillance, Epidemiology, and End Results (SEER) Program, which requires the highest standards of data quality, as judged by completeness, accuracy, and timeliness. The SEER Program includes data for one California Cancer Registry region from 1973 forward, for two other regions from 1992 forward, and for all regions from 2000 forward.

We restricted eligibility to men diagnosed between 1995 and 2004, because of significant changes in the staging of prostate cancer beginning in 1995, and because 2004 was the latest year with complete case ascertainment. Cases were followed though the end of 2004, the latest year with complete cause-of-death ascertainment. Between January 1, 1995, and December 31, 2004, 150,384 non-Hispanic White men and Black men were newly diagnosed with primary, histologically confirmed, invasive prostate cancer (International Classification of Diseases for Oncology, Second Edition (ICD-O-2), site code C619). We restricted study eligibility to men who were actively followed, with adenocarcinoma (ICD-O-2 histology codes 8010, 8140–8570), and for whom prostate cancer was the only known cancer (n = 122,985). After excluding 611 patients (0.5 percent of eligible patients) with missing cause of death, the final sample included 122,374 men.

Measurements
The California Cancer Registry routinely groups race/ethnicity into six mutually exclusive categories (non-Hispanic White, non-Hispanic Black, Hispanic, Asian/Pacific Islander, non-Hispanic American Indian, and other/unknown), using information in the medical record. Hispanic ethnicity was determined using race, Spanish origin, and place of birth from the medical record, as well as surname. A list of 12,497 Latino surnames derived from the 1980 US Census was adopted to more accurately identify Hispanic ethnicity, which is often underreported in medical records. The present study was limited to non-Hispanic White men and Black men. In a previous study (27), block group-level data from the US Census were used to create a composite area-based measure of socioeconomic status. Using principal-component analysis, each residential block group in California was assigned a socioeconomic status score. These residential block groups were also ranked into quintiles on the basis of their socioeconomic status scores. Using residential address at diagnosis, cases accessed into the California Cancer Registry are routinely geocoded and assigned the socioeconomic status score for their block group. Cases missing a block group because of an incomplete address at the time of diagnosis are randomly allocated to block groups within their county of residence.

To determine stage at diagnosis, we used the SEER Program summary stage (or simply, summary stage), a combined clinical and operative/pathologic assessment that includes all information available within 4 months of diagnosis in the absence of disease progression or through completion of the first course of surgery. For prostate cancer, summary stage is derived from six extant disease fields: tumor size, clinical extension, pathologic extension (for patients undergoing prostatectomy), level of lymph node involvement, number of regional lymph nodes examined, and number of regional lymph nodes involved by tumor. Summary staging was chosen over American Joint Committee on Cancer (AJCC) staging because, in contrast to the small proportion of men missing data for summary stage (3.2 percent), AJCC stage data were missing for an unacceptably large proportion of men who were otherwise eligible for the study (38.2 percent were missing both clinical and pathologic stage). Collection of AJCC stage data is mandatory only for hospitals accredited by the American College of Surgeons. During the study period, two schemes for summary staging were in effect, one for diagnosis years 1995–2000 and the other for diagnosis years 2001–2004. For the prostate, there were only minor changes in the staging rules. For example, a case with tumor extension to the levator muscles would have been coded as distant stage during 1995–2000 but as regional stage during 2001–2004.

The ICD-O-2 grade levels used in the present study correspond to the following ranges in the Gleason score: well differentiated, 2–4; moderately differentiated, 5–7; poorly differentiated/undifferentiated, 8–10. Because men could receive more than one type of treatment for their prostate cancer, we determined each patient's primary treatment through a hierarchical scheme used by SEER Program investigators (28, p. 6). In this scheme, "surgery" denotes radical prostatectomy.

The date of death and the cause of death were available through linkages to death certificate data. Using rules developed by the SEER Program, we calculated survival time as the number of completed months between the date of diagnosis and whichever of the following was earliest: date of death; date last known to be alive; or December 31, 2004 (for patients with follow-up after this date). Patients' date of last known vital status is regularly updated through various follow-up activities, including contacting hospitals and physicians and linking patients' data to administrative databases (death certificate file, Department of Motor Vehicles, voter registration, and so on). The survival endpoint for the present study was death from prostate cancer (International Classification of Diseases, Ninth Revision code 185 or Tenth Revision code C61).

Statistical analysis
We used t tests and chi-squared tests to compare prognostic factors among White men and Black men. To confirm the proportional hazards assumption, we examined Kaplan-Meier plots of survival (S) versus time (T) and log(–log(S)) versus log(T) for Whites and Blacks. The Cox proportional hazards model was then used to assess the effect of race on survival, before and after adjustment for age and other prognostic factors. In these models, we estimated the hazard ratio and 95 percent confidence interval for prostate cancer death, comparing Blacks with Whites. Using product terms, we tested for and did not find any statistically significant interactions between race and any of the following covariates: age, stage, treatment, grade, socioeconomic status, or year of diagnosis. Age and socioeconomic status were modeled as quintiles rather than as continuous variables. Patients with missing stage and/or grade were not dropped from the analysis but were assigned a value of "unknown" for stage and/or grade. All survival analyses were conducted using PROC LIFETEST and PROC TPHREG in SAS software 9.1.3 (SAS Institute, Inc., Cary, North Carolina) for Windows (Microsoft Corporation, Redmond, Washington).

To account for racial differences in competing causes of death, we used the cause-specific survival methodology described by Marubini and Valsecchi (29, pp. 331–361). Cause-specific survival is a net survival measure representing survival of a specified cause of death in the absence of other causes. We specified prostate cancer as the cause of death; men who did not die or died from other causes were coded as censored observations.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Main analyses
The men contributed a total of 508,629 person-years of follow-up. During this time, a total of 19,268 (15.7 percent) patients died; prostate cancer was listed as the underlying cause of death for 6,752 (35.0 percent), and 12,516 (65.0 percent) were listed as deaths from other causes. Overall, the proportion of men with complete follow-up for vital status through 2004 was 99.2 percent (99.2 percent for Whites and 98.8 percent for Blacks).

Table 1 shows that White men and Black men had significant differences in all prognostic factors. Compared with Whites, Blacks were diagnosed at younger ages, had more distant stage tumors, underwent curative treatment (surgery or radiation) less frequently, had higher-grade tumors, lived in neighborhoods with lower socioeconomic status, and were diagnosed more recently. Among men of all ages, the age-adjusted risk of death from prostate cancer over 10 years was 12.0 percent for Whites and 19.0 percent for Blacks (figure 1). Because some have hypothesized that the survival disadvantage for Black men might be worse at younger ages, we also examined racial differences in death from prostate cancer after stratifying by age. The elevation in risk for Black men was quite similar above and below the median age at diagnosis (68 years).


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  		TABLE 1. Differences in prognostic factors, White men and Black men with prostate cancer, California, 1995–2004 (n = 122,374)*

 

Figure 1
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  		FIGURE 1. Differences in age-adjusted risk of death from prostate cancer, White men and Black men, California, 1995–2004 (n = 122,374). Cases were diagnosed between 1995 and 2004 and followed until death, loss to follow-up, or December 31, 2004, whichever occurred first.

 
To explore how the racial differences in prognostic factors related to differences in death from prostate cancer, we adjusted for the factors in table 1 in a sequential fashion. As shown in table 2, initially we adjusted only for age, then added potentially modifiable factors (stage and treatment), and finally added nonmodifiable factors (grade, socioeconomic status, and year of diagnosis). Adjusted only for age, the hazard ratio for prostate cancer death (Blacks vs. Whites) was 1.61 (95 percent confidence interval (CI): 1.50, 1.72). Additional adjustment for stage and treatment eliminated most of the racial difference in survival (adjusted hazard ratio (HR) = 1.10, 95 percent CI: 1.03, 1.18). The racial difference in survival was completely eliminated after further adjustment for other factors (grade, socioeconomic status, and year of diagnosis) (adjusted HR = 0.99, 95 percent CI: 0.92, 1.06).


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  		TABLE 2. Differences in survival after sequential adjustment for prognostic factors, White men and Black men with prostate cancer, California, 1995–2004 (n = 122,374)*

 
Results of simultaneous adjustment for all prognostic factors are presented in table 3. Although all of these factors were significantly related to survival, the strongest risk factors were clearly stage and grade. Distant stage was associated with a dramatically worse survival (adjusted HR = 12.31, 95 percent CI: 11.55, 13.13), as was undifferentiated/anaplastic grade (adjusted HR = 8.07, 95 percent CI: 6.29, 10.37). Survival also worsened with increasing age. Primary treatment with surgery or radiation was associated with improved survival: for surgery, the adjusted hazard ratio was 0.24 (95 percent CI: 0.22, 0.27); for radiation, the adjusted hazard ratio was 0.76 (95 percent CI: 0.69, 0.82). Survival was also improved among men with diagnoses after 1998 and among men who lived in areas with higher socioeconomic status. Table 4 shows race-specific estimates for all prognostic factors, and the results show very little racial difference in the effects of the factors.


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  		TABLE 3. Differences in survival after simultaneous adjustment for all prognostic factors, White men and Black men with prostate cancer, California, 1995–2004 (n = 122,374)*

 

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  		TABLE 4. Race-specific effects of prognostic factors, White men and Black men with prostate cancer, California, 1995–2004 (n = 122,374)*

 
Additional analyses
In additional analyses, we examined the effect of including study subjects whose address could not be fully geocoded and so had the block group randomly assigned from within their county. These subjects represented approximately 6.5 percent of the entire study population and had similar distributions of age and race when compared with those with fully geocodable addresses. The results of the multivariate Cox regression were essentially identical to those in table 3 when we excluded these subjects from the analysis. The multivariate hazard ratio for Black race was 0.97 (95 percent CI: 0.90, 1.04) with the subjects excluded.

Because two slightly different summary staging schemes were used during 1995–2000 and 2001–2004, we performed analyses to examine whether our main results would have differed if we had used data from only one time period. The results of the multivariate Cox regression were essentially identical to those in table 3 when we restricted the analysis to cases diagnosed during 1995–2000. For this earlier time period, the multivariate hazard ratio for Black race was 1.00 (95 percent CI: 0.92, 1.08).

Because summary stage is based on both clinical and pathologic data, the fact that Whites undergo surgery more frequently creates the possibility of staging bias, that is, racial difference in the accuracy of staging. In patients undergoing radical prostatectomy, stage may be reclassified from clinically localized to regional stage disease, while this does not occur with other therapies. To evaluate the impact of this selective upstaging, we performed analyses where radical prostatectomy cases coded as regional disease were recoded as localized stage. The results of the multivariate Cox regression were essentially identical to those in table 3. After these regional stage surgery cases were recoded, the multivariate hazard ratio for the Black race was 0.99 (95 percent CI: 0.92, 1.06).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
In this study of 122,374 non-Hispanic White men and Black men from California followed for up to 10 years, we found that the age-adjusted death rate from prostate cancer was 61 percent higher for Blacks than for Whites. However, this large difference in prostate cancer survival was completely explained by known prognostic factors, with potentially modifiable disparities in stage and treatment playing the largest role. These findings are based on population-based statewide cancer registry data that include all newly diagnosed prostate cancer cases among men in California between 1995 and 2004. Patient inclusion for the study was not restricted by stage at diagnosis, age, region of California, enrollment in a specific health-care system, or type of treatment. Completeness of follow-up was excellent, with approximately 99 percent of the men having follow-up for vital status through 2004. The cause of death was available for all study participants who died, allowing for accurate adjustment for death from other causes. Studies of prostate cancer patients have indicated excellent agreement between the underlying cause of death listed on death certificates and the clinician review of medical records (30). In contrast to previous studies that used group-level estimates derived from national vital statistics to account for differences in noncancer mortality, we used patient-level death certificate data from study participants who died to adjust for competing causes of death.

Later stage at diagnosis appeared to be the most important reason for the poorer survival from prostate cancer among Black men. Prostate tumors can be detected at early stages through screening, and there are well-documented Black/White differences in the use of prostate-specific antigen testing, for example (31). These differences could imply disparities in prostate cancer screening awareness, access to screening programs, health insurance status, and other factors. We used summary staging rather than other, more clinically oriented staging schemes such as the one developed by the AJCC. While AJCC staging is useful for making treatment decisions, summary staging is adequate for population-based research. One study that assessed the accuracy of prostate cancer staging in a population-based tumor registry found that more accurate clinical staging through medical record review did not have an appreciable impact on the Black/White stage difference (32).

Blacks also received curative treatment less frequently, perhaps because of more advanced disease, more frequent comorbid conditions, or patient preferences. We did not have any data on the quality of treatment, and there may have been substantial differences in outcomes for White men and Black men who both underwent radical prostatectomy, for example. If so, this would have limited our ability to adjust for confounding by treatment, limiting our ability to "explain" Black/White differences. Because of the observational study design, we could not determine whether our findings regarding treatment and survival were due to causal effects of treatment or to confounding by unmeasured factors. For example, men who were treated with surgery might have had a better general health status than men who were treated with "watchful waiting." This issue will not be resolved until the results of several ongoing randomized trials of prostate cancer treatment are published in the near future.

Among Black men, 24.3 percent had a Gleason score of 7 or more compared with 22.9 percent of White men. Black/White differences in tumor grade have led some to speculate on differences in tumor biology, while others believe that the differences in grade are due to confounding by stage (due to the relation between stage and grade). One study reported that the Black/White difference in tumor grade was decreasing from 1992 to 1998 and was not significant after adjustment for stage (33). However, another study found that Black/White differences in grade persisted after adjustment for stage (34). We also found that residing in a lower socioeconomic status area was an independent predictor of poorer survival from prostate cancer, not because of its relation to other prognostic factors.

Our finding that race was not an independent predictor of survival from prostate cancer is in agreement with the meta-analysis of Bach et al. (25), who reported that there were no significant differences in survival between White men and Black men with prostate cancer after accounting for differences in stage, treatment, and noncancer causes of death. Our findings contrast with those of a number of prior studies that found that prostate cancer survival differences between White men and Black men persisted even after adjustment for confounding factors such as age, competing causes of death, socioeconomic status, stage, grade, and treatment (3, 9, 22, 24). It is possible that our study was better able to adjust for confounding factors, perhaps because of more accurate measurements or because the men were more similar on key variables (e.g., stage) than men in these prior studies.

In summary, in a cohort of over 122,000 men followed for up to 10 years after diagnosis, we found large differences in age-adjusted prostate cancer survival between White men and Black men, but these differences were entirely explained by differences in known prognostic factors. Encouragingly, most of the survival difference was due to two potentially modifiable factors, stage and treatment. By increasing early detection, stage can be "shifted down" so that fewer Black men are diagnosed after their cancer has spread to regional or distant sites. However, it must be noted that, at present, there is no definitive evidence that shifting prostate cancer stage toward less advanced disease will have an impact on mortality (35). If the beneficial effects that we observed for surgery and radiation are causal, then increasing the use of curative treatment among Black men would also improve their survival. However, our data suggest that even if all Black/White differences in stage and treatment were eliminated, there would still be a diminished but statistically significant survival disadvantage for Blacks that is associated with differences in socioeconomic status. Further research is necessary to identify the causal factors that mediate this socioeconomic status-survival relation and to determine whether greater use of "curative" treatment for prostate cancer will, in fact, result in improved survival for this cancer that disproportionately strikes and kills Black men.


   ACKNOWLEDGMENTS
 
The collection of cancer incidence data used in this study was supported by the California Department of Health Services as part of the statewide cancer-reporting program mandated by section 103885 of the California Health and Safety Code; the National Cancer Institute's Surveillance, Epidemiology, and End Results Program under contract N01-PC-35136 awarded to the Northern California Cancer Center, contract N01-PC-35139 awarded to the University of Southern California, and contract N02-PC-15105 awarded to the Public Health Institute; and the Centers for Disease Control and Prevention's National Program of Cancer Registries, under agreement U55/CCR921930-02 awarded to the Public Health Institute.

The ideas and opinions expressed herein are those of the authors, and endorsement by the state of California, Department of Health Services, the National Cancer Institute, and the Centers for Disease Control and Prevention or their contractors and subcontractors is not intended nor should be inferred.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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R. Gao, D. K. Price, T. Sissung, E. Reed, and W. D. Figg
Ethnic disparities in Americans of European descent versus Americans of African descent related to polymorphic ERCC1, ERCC2, XRCC1, and PARP1
Mol. Cancer Ther., May 1, 2008; 7(5): 1246 - 1250.
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