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Published online before print October 2, 2002, 10.1148/radiol.2252011491
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Radiation Oncology

Effect of Race on Biochemical Disease-free Outcome in Patients with Prostate Cancer Treated with Definitive Radiation Therapy in an Equal-Access Health Care System: Radiation Oncology Report of the Department of Defense Center for Prostate Disease Research1

Peter A. S. Johnstone, MD, Christopher J. Kane, MD, Leon Sun, MD, PhD, Hongyu Wu, MD, MPH, Judd W. Moul, MD, David G. McLeod, MD, Douglas D. Martin, MD, Leo Kusuda, MD, Raymond Lance, MD, Robert Douglas, MD, Timothy Donahue, MD, Michael G. Beat, MD, John Foley, MD, Dalton Baldwin, MD, Douglas Soderdahl, MD, Jason Do, MS and Christopher L. Amling, MD

1 From the Naval Medical Ctr, San Diego, Calif (P.A.S.J., C.J.K., J.D., C.L.A.); Ctr for Prostate Disease Research, Dept of Surgery, Uniformed Service Univ, Bethesda, Md (L.S., H.W., J.W.M., D.G.M.); Walter Reed Army Medical Ctr, Washington, DC (J.W.M., D.G.M.); Naval Medical Ctr, Portsmouth, Va (D.D.M., L.K.); Madigan Army Medical Ctr, Tacoma, Wash (R.L.); National Naval Medical Ctr, Bethesda, Md (R.D., T.D.); Brooke Army Medical Ctr, San Antonio, Tex (M.G.B., J.F.); Malcolm Grow Air Force Medical Ctr, Andrews Air Force Base, Md (D.B.); Eisenhower Army Medical Ctr, Augusta, Ga (D.S.); and the Univ of California, San Diego (P.A.S.J.). From the 2001 RSNA scientific assembly. Received September 6, 2001; revision requested October 2; final revision received April 2, 2002; accepted April 30. Supported by the Ctr for Prostate Disease Research, a program of the Uniformed Services Univ of the Health Sciences administered by the Henry M. Jackson Foundation for the Advancement of Military Medicine and funded by the U.S. Army Medical Research and Materiel Command. Address correspondence to P.A.S.J., Naval Medical Center, San Diego, CA 92134-1014 (e-mail: pajohnstone@nmcsd.med.navy.mil).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To report on the first collaboration of the Department of Defense Center for Prostate Disease Research concerned with the relationship between African American race and biochemical disease–free outcomes after definitive radiation therapy.

MATERIALS AND METHODS: Information from the medical records of 1,806 patients (1,349 white, 343 African American, 42 of "other" races, and 72 of "unknown" races) treated with definitive radiation therapy between 1973 and 2000 was reviewed. Patients receiving adjuvant hormonal therapy or postoperative adjuvant or salvage radiation therapy were excluded. Biochemical failure was calculated in over 96% of cases by using ASTRO criteria; patients with fewer than three follow-up visits were considered to have biochemical failure with a prostate-specific antigen (PSA) value more than 10-fold the previous value or with any value greater than 50.0 ng/mL. Median radiation therapy doses were similar. The median follow-up was 58.4 months. Kaplan-Meier tests, Cox proportional hazards regression analysis, and log-rank tests were used for data analysis.

RESULTS: There was no statistically significant difference in biochemical disease-free survival according to race when patients were stratified according to T stage. African American race conferred a negative prognosis for patients with lesions of Gleason biopsy score 7 (P = .004) but not for patients with lesions of Gleason score 2-4 (P = .14), 5-6 (P = .79), or 8-10 (P = .86). Similarly, African American race conferred a negative prognosis in patients with PSA values of 20.1–50.0 ng/mL (P = .01) at presentation but not in patients with PSA values less than or equal to 4.0 ng/mL (P = .84), 4.1–10.0 ng/mL (P = .71), 10.1–20.0 ng/mL (P = .75), or above 50.0 ng/mL (P = .15) at presentation. At multivariate analysis, race was not a statistically significant predictor of outcome.

CONCLUSION: In the equal-access health care system of the Department of Defense, African American race is not associated with a consistently negative prognosis in patients treated with definitive radiation therapy for prostate cancer. Race appears to confer a negative prognosis only in patients with advanced disease at presentation.

Index terms: Data analysis • Prostate neoplasms, 844.32 • Prostate neoplasms, therapeutic radiology, 844.1269


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Race and ethnicity are evocative concepts in oncology. Numerous studies have revealed that outcome in several malignancies may be traced at least in part to socioeconomic status or barriers to access. These are divisive issues and have been invoked as potential reasons that African American men have a higher incidence of prostate cancer (PC) (1), worse stage (2–7) and higher prostate-specific antigen (PSA) levels at presentation (8–10), and decreased overall survival after diagnosis (2,3,11–14).

The role of African American race as a prognostic factor in PC has been investigated by numerous groups. Large population-based studies reveal mixed results, with either a negative prognostic value (2,12,17) or no survival decrement (18,19) associated with African American race. Results of smaller institutional or collaborative group studies are similarly mixed between those of African American race as conferring a negative effect after radical prostatectomy (20,21) or radiation therapy (RT) (22) and those that find that outcome is race neutral (23–28). In both large and small studies, the effect of socioeconomic status and access to care contribute to potential difficulties in generalization (15,16) that are often directly referable to insurance status (10).

All active and retired military personnel have completely equal access to care under a program supported by the U.S. Department of Defense (DOD). Despite recent changes to this schema for primary care and some subspecialty services, the urology and radiation oncology services at the largest DOD medical treatment facilities continue to provide completely unfettered access for military retirees. Thus, for the discrete population of patients with PC, equal access to health care at no cost to the patients remains possible. As such, the military health care system provides an infrastructure that largely removes access and socioeconomic status from confounding clinical outcomes in patients with PC. When data from multiple geographically disparate medical treatment facilities are rigorously collected and analyzed, the effect further removes those two variables from the analysis.

Prior research in patients with PC has revealed that African American men have higher PSA levels at diagnosis when data are corrected for socioeconomic status, cancer stage and grade, and patient age and that this finding may be due to increased tumor burden (defined as tumor volume on whole-organ prostatectomy mounts after radical prostatectomy) (9). Moul et al (20) and Tarman et al (21) examined military populations of patients with PC and found that African American race remained a clinically important adverse prognostic factor at multivariate analysis. Conversely, Optenberg et al (19) examined the entire DOD tumor registry database and found no racial differences in survival.

Care for patients with PC in the DOD system also benefited from Congressional funding made available to organize the Center for Prostate Disease Research (CPDR) in 1992. The offices and research facilities of the CPDR are in Rockville, Md, with a clinical center at the Walter Reed Army Medical Center in Washington, DC. Contingent on funding, other clinical centers are planned for San Diego, Calif, and San Antonio, Tex, at centers of large military retirement populations coincident with large medical treatment facilities. While much of the CPDR funding has supported preclinical research, a large computer database has been developed that contains demographic, prognostic, and outcomes data from the largest medical treatment facilities: Naval Medical Centers in San Diego, Bethesda, Md, and Portsmouth, Va; Army Medical Centers, or AMCs, in Washington, DC (Walter Reed AMC), Tacoma, Wash (Madigan AMC), Augusta, Ga (Eisenhower AMC), and San Antonio (Brooke AMC); and Air Force Medical Centers in San Antonio (Lackland Air Force Base) and Washington, DC (Andrews Air Force Base).

The most complete initial data sets in the collective CPDR databases are surgical, and prior clinical publications have been related to the population of patients undergoing radical prostatectomy. Authors of prior publications have reported short- and long-term outcomes (29–31) and quality of life findings (32) after definitive radical prostatectomy in single-institution settings. The purpose of our study was to report on the first collaboration of the DOD CPDR concerned with the relationship between African American race and biochemical disease–free outcomes after definitive RT.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
A request for data was submitted to the CPDR for information on patient demographics, race and/or ethnicity, diagnosis, age, PSA, T stage, Gleason score, and outcomes after definitive RT. Patients receiving adjuvant or salvage RT after radical prostatectomy were excluded. The uniform staging system used was the unified system that was in place in 1992, when the database was inaugurated (Table 1). CPDR databases are maintained at the individual medical treatment facilities, and data collection at some sites began as early as 1994 at the largest CPDR sites. Retrospective data collection for the CPDR database was an ongoing process, and patient clinical records were entered from as early as 1970. Therefore, it is inevitable that different staging systems were used. Thus, when the standard CPDR database was implemented in 1999, CPDR management ordered that a single system be used and that all records be reformatted for this system. This work was completed by August 2000 at all CPDR sites.


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  		TABLE 1. Unified Cancer Staging System

 
The medical records of 1,806 eligible patients were reviewed. Diagnosis dates ranged from July 1973 to June 2000; the median follow-up was 58.4 months. Such data are collected with informed patient consent under the auspices of the institutional review board at the Uniformed Services University in Bethesda, Md, with full concurrence of individual institutional review boards at each medical treatment facility.

For this study, the records of 1,806 patients who underwent primary external RT out of 6,727 patients with PC were retrieved, representing 26.9% of the total population of patients with PC in the database as of the end of June 2000. The percentage of patients in different racial groups was similar to that within the entire CPDR population of patients with PC (data not included). If charts were missing data on T stage, Gleason score, or PSA levels at presentation, they were excluded from further analysis.

A majority of racial information was determined by the treating physicians, since they had completed the registration forms from which the database entries had been generated. This information is also available at each site with use of a DOD health care computer system, which was used to verify race, if necessary. The assumption is that patients will be accurate when reporting race themselves, but no further verification of race is performed at the time of registry. No data are readily available regarding the race of the treating physician, as this is not a parameter within the database and is not recorded. Cases in the "unknown" race group were collected if race was noted in neither the CPDR demographic registration nor the computer system. Race was reported as white in 74.7% (n = 1,349) of cases, as African American in 19.0% (n = 343), as Filipino (n = 15) or Hispanic (n = 14) in 0.8% each, as Asian (Chinese, Guamanian, or Japanese) in 0.3% (n = 5); and as "other" in 0.4% (n = 8). Unknown race was reported in 4.0% (n = 72).

Data were collected for patients who had received only RT but had never received hormonal therapy prior to PSA recurrence, if any. It was understood that these data might cloud the data in a population of patients with locally advanced disease presenting after 1996, since the patients might have received neoadjuvant hormonal therapy, but we considered the data necessary to maintain the most accurate biochemical disease-free survival data based on RT alone. This further removed any potential bias between institutions, some of which may have begun using neoadjuvant hormonal therapy at different times and under different clinical circumstances. No patients were included if they had undergone prostatectomy prior to RT.

Median RT doses delivered (68.4 Gy in whites, African Americans, and patients of unknown race; 69.2 Gy in patients of other races) were similar. When measured as a percentage of all patients treated, more African Americans were treated after 1990 (by using more sophisticated techniques) than prior to 1990 (data not included; P < .001). Median follow-up was 58.4 months.

Failure to remain free of biochemical disease was determined according to the ASTRO criteria (33). For patients treated before the PSA era (defined as earlier than 1990; n = 318), failure was defined as local failure (abnormal digital rectal examination findings, cancerous biopsy findings), bone metastasis, or death resulting from PC. For patients with fewer than three follow-up visits, a 10-fold increase from the prior PSA value, or any PSA value above 50.0 ng/mL after a nadir below 50.0 ng/mL was considered evidence of failure to remain free of biochemical disease. These were infrequently used end points representing less than 4.0% of the sample.

As with other large multicenter databases, some data were missing. Because of this, analyses included an unknown group for which the parameter of race was unknown. Statistical software (SPSS version 8.0; SPSS, Chicago, Ill) was used for all assays of the data in the current study to describe potential differences between race and ethnicity and the parameters at presentation. Distribution analysis of the data set was performed to examine the mean and median of the parameters. Simple descriptive statistics were calculated. Disease-free survival was determined by using the Kaplan-Meier technique. Survival curves were compared by using the log-rank test. Multivariate analysis (Cox proportional hazards regression analysis) was performed on the basis of patient age, race, PSA level, cancer stage, and Gleason score sum.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient demographic data are presented in Table 2. Differences between median Gleason scores at presentation were not significant between white and African American patients (P = .37); differences at presentation were significant between these groups in terms of age, PSA values at presentation, and cancer stage (P < .001 at all levels).


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  		TABLE 2. Demographics of CPDR Population Undergoing RT

 
Kaplan-Meier plots of biochemical disease-free survival according to patient race and cancer stage at presentation are shown in Figure 1, according to race and biopsy Gleason score in Figure 2, and according to race and PSA level at presentation in Figure 3.



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  		Figure 1a. Graphs show that patient race is not associated with biochemical disease-free survival, as stratified according to clinical T stage. (a) For stage T1, the log-rank P value is equal to .24. (b) For stage T2, the log-rank P value is equal to .37. (c) For stage T3, the log-rank P value is equal to .06.

 


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  		Figure 1b. Graphs show that patient race is not associated with biochemical disease-free survival, as stratified according to clinical T stage. (a) For stage T1, the log-rank P value is equal to .24. (b) For stage T2, the log-rank P value is equal to .37. (c) For stage T3, the log-rank P value is equal to .06.

 


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  		Figure 1c. Graphs show that patient race is not associated with biochemical disease-free survival, as stratified according to clinical T stage. (a) For stage T1, the log-rank P value is equal to .24. (b) For stage T2, the log-rank P value is equal to .37. (c) For stage T3, the log-rank P value is equal to .06.

 


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  		Figure 2a. Graphs show that patient race is not associated with biochemical disease-free survival, as stratified according to diagnostic Gleason score. (a) For Gleason score 2-4, the log-rank P value equals .14. (b) For Gleason score 5-7, the log-rank P value equals .14. (c) For Gleason score 8-10, the log-rank P value equals .86.

 


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  		Figure 2b. Graphs show that patient race is not associated with biochemical disease-free survival, as stratified according to diagnostic Gleason score. (a) For Gleason score 2-4, the log-rank P value equals .14. (b) For Gleason score 5-7, the log-rank P value equals .14. (c) For Gleason score 8-10, the log-rank P value equals .86.

 


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  		Figure 2c. Graphs show that patient race is not associated with biochemical disease-free survival, as stratified according to diagnostic Gleason score. (a) For Gleason score 2-4, the log-rank P value equals .14. (b) For Gleason score 5-7, the log-rank P value equals .14. (c) For Gleason score 8-10, the log-rank P value equals .86.

 


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  		Figure 3a. Graphs show that patient race is associated with biochemical disease-free survival only for a diagnostic PSA level greater than 20 ng/mL. (a) For a PSA level less than or equal to 4.0 ng/mL, the log-rank P value equals .84. (b) For a PSA level of 4.1—10.0 ng/mL, the log-rank P value equals .71. (c) For a PSA level of 10.1-20.0 ng/mL, the log-rank P value equals .75. (d) For a PSA level greater than 20.0 ng/mL, the log-rank P value is less than .001.

 


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  		Figure 3b. Graphs show that patient race is associated with biochemical disease-free survival only for a diagnostic PSA level greater than 20 ng/mL. (a) For a PSA level less than or equal to 4.0 ng/mL, the log-rank P value equals .84. (b) For a PSA level of 4.1—10.0 ng/mL, the log-rank P value equals .71. (c) For a PSA level of 10.1-20.0 ng/mL, the log-rank P value equals .75. (d) For a PSA level greater than 20.0 ng/mL, the log-rank P value is less than .001.

 


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  		Figure 3c. Graphs show that patient race is associated with biochemical disease-free survival only for a diagnostic PSA level greater than 20 ng/mL. (a) For a PSA level less than or equal to 4.0 ng/mL, the log-rank P value equals .84. (b) For a PSA level of 4.1—10.0 ng/mL, the log-rank P value equals .71. (c) For a PSA level of 10.1-20.0 ng/mL, the log-rank P value equals .75. (d) For a PSA level greater than 20.0 ng/mL, the log-rank P value is less than .001.

 


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  		Figure 3d. Graphs show that patient race is associated with biochemical disease-free survival only for a diagnostic PSA level greater than 20 ng/mL. (a) For a PSA level less than or equal to 4.0 ng/mL, the log-rank P value equals .84. (b) For a PSA level of 4.1—10.0 ng/mL, the log-rank P value equals .71. (c) For a PSA level of 10.1-20.0 ng/mL, the log-rank P value equals .75. (d) For a PSA level greater than 20.0 ng/mL, the log-rank P value is less than .001.

 
Differences between only two curves were statistically significant: when analyzed for patients with a Gleason score of 7 at biopsy (log rank, P = .004) and for a PSA level of 20.1–50.0 ng/mL at presentation (log rank, P = .01). These data are not graphically presented separately herein; Gleason score data are included with Gleason scores of 5 and 6 in Figure 2b, and all PSA data greater than 20.0 ng/mL are included in Figure 3d. At multivariate analysis, only Gleason score and PSA value at presentation were identified as statistically significant factors associated with biochemical relapse. Race was not statistically significant.

When subset analysis was performed only in patients with advanced disease (T3-4, Gleason score sum 8-10, or PSA level > 20.0 ng/mL) at presentation, African American men showed a significantly lower disease-free survival rate (P = .017, Fig 4).



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  		Figure 4. Graph shows that patient race is associated with the biochemical disease-free survival in the advanced disease group (stage T3-4, Gleason score 8-10, or PSA level greater than 20.0 ng/mL; log-rank P value equal to .017).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
At univariate analysis, race served as a prognostic factor in only some subsets of patients. This is difficult to consider as anything more than a statistical aberration, since it is inconceivable that Gleason score 7 lesions would be so different from either Gleason score 5-6 or 8-10 lesions, or that PSA values of 21.0–50.0 ng/mL would be so different from those of less than 20.0 or greater than 50.0 ng/mL.

If analysis is performed in all patients with PSA values greater than 20.0 ng/mL at presentation, race confers a negative prognosis (P = .001). This, as well as a trend toward race being prognostic in T3 lesions (P = .06), initially led us to consider that race has significance only in advanced disease. When patients with advanced disease (T3-4 lesions, Gleason score sum of 8-10, or PSA value > 20.0 ng/mL) at presentation were analyzed separately (Fig 4), the result showed a significantly lower disease-free survival rate for African American men (P = .017 [Fig 4]). However, multivariate analysis within the entire study population confirmed that race is not a prognostic factor exclusive of PSA level and cancer grade and stage.

Thus, our data reveal that race is not associated with a negative biochemical disease-free bias in patients with PC who are treated with RT within an equal-access health care system. This conclusion reinforces findings in several previous studies (18,19,23–28) and is intriguing because the findings of numerous studies (2–10), as well as our own data, demonstrate that African American men have higher PSA values and disease stages at presentation. To further cloud the issue, differences in survival between races in larger population-based studies (15,34,35) may also be attributed to differences in the percentage of African Americans offered definitive therapy.

The differences noted by others may represent differences in access to care and in affordability of care. However, it may also represent a true biochemical difference between PC in African Americans and that in whites or may represent a delay in African American patients seeking care for their disease. Since we found no significant effect of race, these data in the patient population in the current study support the societal perspective. The lack of consistent racial effect on the patients, when stratified by means of clinical disease stage at presentation, by using biopsy Gleason score sum (noting the aberrance of the Gleason score 7 cohort) or PSA value at presentation (noting the aberrance of values of 20.1–50.0 ng/mL), strongly supports the beneficial socioeconomic and access characteristics of the DOD health care environment for these patients. This has been noted previously in patients with PC who underwent prostatectomy (21) and in African American women with breast (36) or cervical (37) cancer.

It must be emphasized, however, that equal access to care does not mean equal use of care. This point was made in an analysis of patients with breast cancer at the Naval Medical Center in San Diego, Calif (36). Although race did not affect the time from entrance into the medical system to treatment (in fact, African American women had a non–statistically significant shorter interval from presentation to treatment), African American women had a significantly longer interval from self-discovery of breast masses to presentation for evaluation. This clearly indicates that patients affect their own care, even in an equal-access environment; this finding may explain some of the disparate data in the literature.

It is an unfortunate correlate of large multiinstitutional data collection that data will be absent from the database. Further, we are acutely aware of the potential implications for the broader generalizability of our results and to this end performed as rigorous and select a statistical analysis as possible. We do not think the missing data would have changed these results had they been present. Patients of unknown race were included in analysis in each case to ensure that they did not represent a group that was positively or negatively selected, and that exclusion from their "rightful" categories did not adversely affect the analysis. Nevertheless, these data confirm published results for the DOD Health Care System with regard to breast (36) and cervical (37) cancer: Equal access, if used, contributes to equal results, without regard to race.

In conclusion, African American race was not associated with a negative prognosis in patients in the DOD Health Care System, who are the beneficiaries of an equal-access health care system with the subspecialty care required for patients with PC. Race appears to be associated with a negative prognosis in only the subset of patients with advanced disease at presentation.


   FOOTNOTES
 
The opinions or assertions contained herein are those of the authors and should not be construed as representing the views of the U.S. Department of Defense or the U.S. Government.

Abbreviations: CPDR = Center for Prostate Disease Research, DOD = Department of Defense, PC = prostate cancer, PSA = prostate-specific antigen, RT = radiation therapy

Author contributions: Guarantor of integrity of entire study, P.A.S.J.; study concepts, P.A.S.J., J.W.M., C.J.K., C.L.A.; study design, P.A.S.J., J.W.M., C.J.K., C.L.A., L.S.; literature research, P.A.S.J.; clinical studies, J.W.M., D.G.M., R.D., T.D., M.G.B., J.F., D.B., D.S., J.D.; data acquisition, J.W.M., D.G.M., R.D., T.D., M.G.B., J.F., D.B., D.S., J.D., R.L., L.K.; data analysis/interpretation, H.W., P.A.S.J., L.S., J.W.M.; statistical analysis, H.W., L.S.; manuscript preparation, P.A.S.J., L.S., C.J.K., C.L.A., J.W.M., R.D., D.D.M.; manuscript definition of intellectual content, P.A.S.J., J.W.M., C.L.A., D.G.M., C.J.K., L.S.; manuscript editing, revision/review, and final version approval, J.W.M., L.S., C.J.K., R.D., D.D.M., C.L.A.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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