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Journal of Clinical Oncology, Vol 20, Issue 12 (June), 2002: 2863-2868
© 2002 American Society for Clinical Oncology

Impact of Race on Prostate-Specific Antigen Outcome After Radical Prostatectomy for Clinically Localized Adenocarcinoma of the Prostate

By Chaundre K. Cross, Delray Shultz, S. Bruce Malkowicz, William C. Huang, Richard Whittington, John E. Tomaszewski, Andrew A. Renshaw, Jerome P. Richie, Anthony V. D’Amico

From the Departments of Radiation Oncology, Pathology, and Urology, Brigham and Women’s Hospital and Dana-Farber Cancer Institute, Boston, MA; and Department of Mathematics, Millersville University, Millersville, and Departments of Urology, Radiation Oncology, and Pathology, Hospital of University of Pennsylvania, Philadelphia, PA.

Address reprint requests to Chaundre Cross, MD, and Anthony D’Amico, MD, Department of Radiation Oncology, Brigham and Women’s Hospital, 75 Francis St, L-2 Level, Boston, MA 02215; email: ccross{at}partners.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To compare prostate-specific antigen (PSA) outcome after radical prostatectomy (RP) for prostate cancer in African-American and white men using previously established risk groups.

PATIENTS AND METHODS: Between 1989 and 2000, 2,036 men (n = 162 African-American men, n = 1,874 white men) underwent RP for clinically localized prostate cancer. Using pretreatment PSA, Gleason score, clinical T stage, and percentage of positive biopsy specimens, patients were stratified into low- and high-risk groups. For each risk group, PSA outcome was estimated using the actuarial method of Kaplan and Meier. Comparisons of PSA outcome between African-American and white men were made using the log-rank test.

RESULTS: The median age and PSA level for African-American and white men were 60 and 62 years old and 8.8 and 7.0 ng/mL, respectively. African-Americans had a statistically significant increase in PSA (P = .002), Gleason score (P = .003), clinical T stage (P = .004), and percentage of positive biopsy specimens (P = .04) at presentation. However, there was no statistical difference in the distribution of PSA, clinical T stage, or Gleason score between racial groups in the low- and high-risk groups. The 5-year estimate of PSA outcome was 87% in the low-risk group for all patients (P = .70) and 28% versus 32% in African-American and white patients in the high-risk group (P = .28), respectively. Longer follow-up is required to confirm if these results are maintained at 10 years.

CONCLUSION: Even though African-American men presented at a younger age and with more advanced disease compared with white men with prostate cancer, PSA outcome after RP when controlled for known clinical predictive factors was not statistically different. This study supports earlier screening in African-American men.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
APPROXIMATELY 198,100 new cases of prostate cancer are expected in the United States during 2001. Secondary to the introduction of prostate-specific antigen (PSA) screening, incidence rates increased dramatically between 1988 and 1992. From 1992 to 1998, African-American men were almost two times as likely to be diagnosed with prostate cancer compared with white men (234.2/100,000 men v 144.6/100,000 men, respectively). Incidence rates for African-American men have declined between 1992 and 1998 by 4.0% per year. However, white men have experienced more of a decline in incidence rates during this 7-year period (5.7% per year).1,2 Also, African-American men were twice as likely to die of prostate cancer in comparison with white men between 1992 and 1998 (53.1/100,000 men and 22.4/100,000 men, respectively). From 1994 to 1998, prostate cancer death rates declined for white and African-American men (4.7% and 3.0%, respectively).1,2

The reason for the discrepancy of worse incidence and death rates among African-American men in comparison with white men in the United States is still debated. More biologic, aggressive cancer has been proposed as one possible explanation given for the higher PSA level and younger age at presentation,3-14 as well as more multifocal disease on autopsy,15,16 higher prevalence of (allegedly) high-risk alleles, such as CAG repeat,17-20 vitamin D binding protein,21 and SRD5A2 gene,22 a higher testosterone level in younger men,23,24 and adverse pathologic factors after radical prostatectomy (RP)25-29 in African-American men compared with white men. Socioeconomic factors such as income, education, nutrition, and screening have also been cited as factors contributing to the more aggressive and advanced stage of prostate cancer in African-American men.30-33

Studies to date have suggested that when patients with early-stage prostate cancer are stratified by pretreatment tumor characteristics, PSA outcome is not different between ethnic groups.34,35 Limitations of these studies include adjuvant therapy given after local therapy and a lack of consistent definition of the risk groups. In this analysis, patients with clinically localized prostate cancer from the Hospital of University of Pennsylvania (HUP), Philadelphia, PA, and Brigham and Women’s Hospital (BWH), Boston, MA, treated with RP and no adjuvant therapy formed the study cohort. PSA outcome for African-American and white men were compared using a previously established risk group stratification based on the PSA, Gleason score, clinical T stage, and percentage of positive biopsy specimens.36,37


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patient Population
Between 1989 and 2000, 2,036 men were treated with RP for PSA detected or clinically palpable localized prostate cancer at the BWH and the HUP. Patients who received neoadjuvant androgen-suppression therapy, adjuvant radiation, or both were excluded. One hundred sixty-two African-American men and 1,874 white men were included in this study. Table 1 lists the preoperative clinical characteristics of the entire study cohort.


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  		Table 1.  Pretreatment Characteristics of All Patients
 
Preoperative Staging
In all cases, staging evaluation included a history and physical examination, including a digital rectal examination (DRE), serum PSA, computed tomography scan of the pelvis or an endorectal and pelvic coil magnetic resonance imaging scan of the prostate and pelvis, bone scan, and a transrectal ultrasound-guided needle biopsy of the prostate with Gleason score histologic grading.38 Whereas during the study period, bone scans, magnetic resonance imaging, or computed tomography scans were obtained routinely, on this day they would only be obtained in patients with high-risk disease. A sextant biopsy was performed using an 18-gauge Tru-Cut needle (Travenol Laboratories, Deerfield, IL). Sextant biopsy specimens were obtained in the majority of RP-managed patients at HUP (56%) and BWH (75%). The remaining 44% of patients at HUP had fewer than six (18% of patients) or more than six (26% of patients) biopsy specimens. The clinical stage was obtained from the DRE findings using the 1992 American Joint Committee on Cancer (AJCC) staging system.39 Radiologic and biopsy information was not used to determine clinical stage. The PSA level was obtained on an ambulatory basis before radiologic studies and the biopsy procedure. All pretreatment PSA values were obtained within 1 month of the date of the surgery. PSA measurements40 were made using the Hybritech (Beckman Coulter Inc, Fullerton, CA), Tosoh (Tosoh Inc, San Francisco, CA), or Abbott (Abbott Laboratories, Abbott Park, IL) assays.

Treatment and Histopathologic Assessment
A referee genitourinary pathologist reviewed the diagnostic biopsy specimens for all patients undergoing surgery at the HUP (J.E.T.) or BWH (A.A.R.). Surgical treatment consisted of a retropubic RP and bilateral pelvic lymph node sampling. If the intraoperative frozen sections of any sampled lymph node were positive for carcinoma, then RP was aborted. Evidence of extracapsular extension, positive margin, and seminal vesicle invasion were noted and recorded.

Follow-Up
The median follow-up duration for the entire cohort was 42 months (range, 6 to 132 months). The patients were examined 1 month after surgery and then at 3-month intervals for 2 years, every 6 months for 5 years, and annually thereafter. At each follow-up appointment, the serum PSA level was measured before the DRE was performed. No patients were lost to follow-up.

Statistical Analysis
PSA failure was defined as two detectable (> 0.2 ng/mL) PSA values obtained after an undetectable measurement. The time of PSA failure was taken as the time of the first detectable PSA. Time zero was the date of RP. If a PSA never became undetectable after surgery, then PSA failure was considered to have occurred at time equal to zero. PSA outcome was defined as PSA failure-free survival at 5 years, which was estimated using the actuarial method of Kaplan and Meier41 and graphically displayed.

Three risk groups were defined36,37 based on the pretreatment PSA level, biopsy Gleason score, and 1992 AJCC T stage. Low-risk patients had a preoperative PSA level of <= 10 ng/mL, a biopsy Gleason score of <= 6, and 1992 AJCC clinical stage T1c or T2a disease. High-risk patients had a PSA level of greater than 20 ng/mL, a biopsy Gleason score of >= 8, or 1992 AJCC clinical stage T2c disease. The remaining patients with <= 50% or more than 50% positive biopsy specimens were classified as low- and high-risk, respectively, based on a previous study showing the importance of the percentage of positive biopsy specimens in intermediate-risk patients. PSA outcome was reported for the low- and high-risk groups. Specifically, using a log-rank test,42 PSA outcome was compared in low- and high-risk groups stratified by race.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Pretreatment Clinical Characteristics
The median age for white and African-American men was 62 and 60 years, respectively, and the median PSA level was 7.0 and 8.8 ng/mL, respectively (Table 1). The pretreatment clinical factors for all patients revealed more advanced disease in the African-American cohort (Table 1). African-American men had a statistically significant increase in PSA (P = .002), Gleason score (P = .003), clinical T stage (P = .004), and percentage of positive biopsy specimens (P = .04). Also, 55% of the African-American patients were in the high-risk group versus 37% of the white patients. However, there was no statistical difference in the distribution of PSA, clinical T stage, or Gleason score between racial groups within each of the low- and high-risk groups as summarized in Table 2.


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  		Table 2.  Pretreatment Characteristics of Low- and High-Risk Patients
 
PSA Failure-Free Survival
The median follow-up for African-American and white patients in the low- and high-risk groups was not statistically different. Specifically, the median follow-up for African-American and white men in the low-risk groups for patients censored at the time of PSA failure was 38 and 35 months, respectively. For high-risk groups, it was 22 and 23 months, respectively. The 5-year estimate of PSA outcome was 87% in the low-risk group for both African-American and white patients (P = .70) and 28% versus 32% in African-American and white patients, respectively, in the high-risk group (P = .28). These results are illustrated in Figs 1 and 2.



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  		Fig 1. PSA failure-free (bNED) survival by race for low-risk patients (P = .70). bNED, biochemical no evidence of disease.

 


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  		Fig 2. PSA failure-free (bNED) survival by race for high-risk patients (P = .28). bNED, biochrmical no evidence of disease.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Previous studies have attempted to compare PSA outcome stratified by race after RP for early-stage prostate cancer. These studies are listed in Table 3. Four of the six studies revealed that race was not a significant predictor of PSA failure.6-11 These studies are limited because they fail to stratify patients for known clinical predictors of PSA failure. Previously published studies confirm that the pretreatment PSA level, 1992 AJCC clinical T stage, and biopsy Gleason score are independent predictors of PSA failure-free survival after RP43-45 or external-beam radiation therapy.44 Therefore, when comparing PSA outcome, it is important to control for these factors. Two studies reported on PSA outcome between African-American and white patients with localized prostate cancer by risk groups based on PSA, clinical T stage, and Gleason score.34,35 Both of these studies included patients that had received neoadjuvant or adjuvant hormonal therapy or adjuvant radiation. In addition, whereas low-risk was defined consistently in these studies, intermediate- and high-risk definitions differed.


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  		Table 3.  Studies Evaluating the Association of Race and Recurrence After RP for Clinically Localized Prostate Cancer
 
The current study compared PSA outcome among racial groups after RP for localized prostate cancer stratified by pretreatment clinical factors into established risk groups and in the absence of adjuvant or neoadjuvant therapies. The main finding of this study was that PSA outcomes between racial groups were not significantly different for the low- and high-risk groups (P = .70 and P = .28, respectively). However, at presentation, the PSA, clinical T stage, Gleason score, and percentage of positive biopsy specimens for African-American men were significantly more advanced compared with white men. As a result, African-American men presented with more advanced disease and at younger ages, as noted by a higher proportion of African-American men compared with white men in the high-risk group (55% v 37%, respectively) and lower proportion of African-American men compared with white men in the low-risk group (45% v 63%, respectively).

This study has limitations. First, the follow-up period may not have been long enough to see a statistical difference in PSA outcome in the low-risk group because failure can be protracted. Second, retrospective studies are not conclusive because of the possibility of unknown confounding factors that can impact results. Third, given the numerical difference, although not statistically significant in PSA outcome for high-risk patients stratified by race as shown in Fig 2, there is the possibility that a difference may emerge with a larger cohort of African-American men and longer follow-up.

Despite the worse mortality rate for African-American men with prostate cancer compared with white men, this study and four others7-10 did not find race to be a significant predictor of recurrence after RP. However, African-American men with prostate cancer present at a younger age and with more advanced disease. Given that PSA outcome is not significantly different and more favorable for low-risk African-American and white individuals at 5 years, this article provides evidence to support prostate cancer screening in African-American men at a younger age.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
1. American Cancer Society: Cancer facts and figures in 2001: Prostate cancer in minorities. Http: //www3.cancer.org/eprise/main/docroot/stt/stt_0

2. Howe HL, Wingo PA, Ries AG, et al: Annual report to the nation on the status of cancer (1973 through 1998), featuring cancers with recent increasing trends. J Natl Cancer Inst 93: 824-841, 2001[Abstract/Free Full Text]

3. Moul JW, Sesterhenn IA, Connelly RR, et al: Prostate specific antigen values at the time of prostate cancer diagnosis in African-American men. JAMA 274: 1277-1281, 1995[Abstract/Free Full Text]

4. Moul JW, Connelly RR, Mooneyhan RM, et al: Racial differences in tumor volume and prostate specific antigen among radical prostatectomy patients. J Urol 162: 394-397, 1999[CrossRef][Medline]

5. Ibrahim GK, Coetzee LJ, Paulson DF: Outcomes of surgical therapy for clinically localized prostatic carcinoma adenocarcinoma: Caucasians and Afro-Americans. J Urol 153: 504a, 1995 (abstr)

6. Moul JW, Douglas TH, McCarthy WF, et al: Black race is an adverse prognostic factor for prostate cancer recurrence following radical prostatectomy in an equal access health care setting. J Urol 155: 1667-1673, 1996[CrossRef][Medline]

7. Iselin CE, Box JW, Vollmer RT, et al: Surgical control of clinically localized prostate carcinoma is equivalent in African-American and white males. Cancer 83: 2353-2360, 1998[CrossRef][Medline]

8. Eastham JA, Kattan MW: Disease recurrence in black and white men undergoing radical prostatectomy for clinical stage T1-T2 prostate cancer. J Urol 163: 143-145, 2000[CrossRef][Medline]

9. Powell IJ, Banerjee M, Novallo M, et al: Prostate cancer biochemical recurrence stage for stage is more frequent among African-American than white men with locally advanced but not organ-confined disease. Urology 55: 246-251, 2000[CrossRef][Medline]

10. Freedland SJ, Jalkut M, Dorey F, et al: Race is not an independent predictor of biochemical recurrence after radical prostatectomy in an equal access medical center. Urology 56: 87-91, 2000[Medline]

11. Tarman GJ, Kane CJ, Moul JW, et al: Impact of socioeconomic status and race on clinical parameters of patients undergoing radical prostatectomy in an equal access health care system. Urology 56: 1016-1020, 2000[CrossRef][Medline]

12. Powell IJ, Banerjee M, Sakr W, et al: Should African-American men be tested for prostate carcinoma at an earlier age than white men? Cancer 85: 472-477, 1999[CrossRef][Medline]

13. Zhang W, Sesterhenn IA, Connelly RR, et al: Inflammatory infiltrate (prostatitis) in whole mounted radical prostatectomy specimens from black and white patients is not an etiology for racial difference in prostate specific antigen. J Urol 163: 131-136, 2000[CrossRef][Medline]

14. Pettaway CA, Troncoso P, Ramirez EI, et al: Prostate-specific antigen and pathological features of prostate cancer in black and white patients: A comparative study based on radical prostatectomy specimens. J Urol 160: 437-442, 1998[CrossRef][Medline]

15. Sakr WA, Hass GP, Cassin BF, et al: The frequency of carcinoma and intraepithelial neoplasia of the prostate in young male patients. J Urol 150: 379-385, 1993[Medline]

16. Sakr WA, Grignon DJ, Haas GP, et al: Epidemiology of high grade prostatic intraepithelial neoplasia. Pathol Res Pract 191: 838-841, 1995[Medline]

17. Sartor O, Zheng Q, Eastham JA: Androgen receptor gene CAG repeat length varies in a race-specific fashion in men without prostate cancer. Urology 53: 378-380, 1999[CrossRef][Medline]

18. Giovannucci E, Stampfer MJ, Krithivas K, et al: The CAG repeat within the androgen receptor gene and its relationship to prostate cancer. Proc Natl Acad Sci U S A 94: 3320-3323, 1997[Abstract/Free Full Text]

19. Hardy DO, Scher HI, Bogenreider T, et al: Androgen receptor CAG repeat lengths in prostate cancer: Correlation with age of onset. J Clin Endocrinol Metab 81: 4400-4405, 1996[Abstract]

20. Irvine RA, Yu MC, Ross RK, et al: The CAG and GGC microsatellites of the androgen receptor gene are in linkage disequilibrium in men with prostate cancer. Cancer Res 55: 1937-1940, 1995[Abstract/Free Full Text]

21. Corder EH, Friedman GD, Vogelman JH, et al: Seasonal variation in vitamin D, vitamin D-binding protein, and dehydroepiandrosterone: Risk of prostate cancer in black and white men. Cancer Epidemiol Biomarkers Prev 4: 655-659, 1995[Abstract]

22. Reichardt JK, Makridakis N, Ross RK, et al: Genetic variability of the human SRD5A2 gene: Implications for prostate cancer risk. Cancer Res 55: 3973-3975, 1995[Abstract/Free Full Text]

23. Kubricht WS, Williams BJ, Whatley T, et al: Serum testosterone levels in African-American and white men undergoing prostate biopsy. Urology 54: 1035-1038, 1999[CrossRef][Medline]

24. Ross R, Bernstein L, Judd H, et al: Serum testosterone levels in healthy young black and white men. J Natl Cancer Inst 76: 45-48, 1986[Medline]

25. Freedland SJ, Dorey F, Aronson WJ: Multivariate Analysis of race and adverse pathologic findings after radical prostatectomy. Urology 56: 807-811, 2000[CrossRef][Medline]

26. Witte MN, Kattan MW, Albani J, et al: Race is not an independent predictor of positive surgical margins after radical prostatectomy. Urology 54: 869-874, 1999[CrossRef][Medline]

27. Powell IJ, Heilbrun LK, Sakr W, et al: The predictive value of race as a clinical prognostic factor among patients with clinically localized prostate cancer: A multivariate analysis of positive margins. Urology 49: 726-731, 1997[CrossRef][Medline]

28. Shekarriz B, Tiguret R, Upadhyay J, et al: Impact of location and multifocality of positive surgical margins on disease-free survival following radical prostatectomy: A comparison between African-American and white men. Urology 55: 899-903, 2000[CrossRef][Medline]

29. Barroso U, Oskanian P, Tefilli MV, et al: Population-based study of pelvic lymph node positivity in clinically localized prostate cancer: A study comparing African-Americans and whites. Urology 53: 187-191, 1999[CrossRef][Medline]

30. Vijayakumar S, Karrison T, Weichselbaum R, et al: Racial differences in prostate-specific antigen levels in patients with local-regional prostate cancer. Cancer Epidemiol Biomarkers Prev 1: 541-545, 1992[Abstract/Free Full Text]

31. Vijayakumar S, Weichselbaum R, Vaida F, et al: Prostate-specific antigen levels in African-American correlate with insurance status as an indicator of socioeconomic status. Cancer J Sci Am 2: 225-233, 1996[Medline]

32. Dale W, Vijayakumar S, Lawlor E, et al: Prostate cancer, race, and socioeconomic status: Inadequate adjustment for social factors in assessing racial differences. Prostate 29: 271-281, 1996[CrossRef][Medline]

33. Vijayakumar S, Winter K, Sause W, et al: Prostate specific antigen levels are higher in African-American than in white patients in a multicenter registration study: Results of RTOG 94-12. Int J Radiat Oncol Biol Phys 40: 17-25, 1998[CrossRef][Medline]

34. Altsman K, Kupelian PA, Sohayda C, et al: Race is not an independent factor affecting outcome after radical prostatectomy or definitive radiotherapy for localized adenocarcinoma. Int J Radiat Oncol Biol Phys 42: 303, 1998 (suppl 1, abstr)[CrossRef]

35. Connell PP, Ignacio L, Vijayakumar S, et al: Equivalent racial outcome after conformal radiotherapy for prostate cancer: A single departmental experience. J Clin Oncol 19: 54-61, 2001[Abstract/Free Full Text]

36. D’Amico AV, Whittington R, Malkowicz SB, et al: Biochemical outcome after radical prostatectomy, external beam radiation therapy, or interstitial radiation therapy for clinically localized prostate cancer. JAMA 280: 969-974, 1998[Abstract/Free Full Text]

37. D’Amico AV, Whittington R, Malkowicz SB, et al: Clinical utility of the percentage of positive prostate biopsies in defining biochemical outcome after radical prostatectomy for patients with clinically localized prostate cancer. J Clin Oncol 18: 1164-1172, 2000[Abstract/Free Full Text]

38. Gleason DF: Histologic grading and staging of prostatic carcinoma, in Tannenabum M (ed): Urologic Pathology. Philadelphia, PA, Lea & Febiger, 1977, pp 171-187

39. Beahrs OH, Henson DE, Hutter RVP: American Joint Committee on Cancer: Manual for Staging Cancer, ed 4 . Philadelphia, PA, JB Lippincott, 1992

40. Epstein JL, Pizov G, Walsh PC: Correlation of pathologic findings with progression after radical retropubic prostatectomy. Cancer 71: 3582-3589, 1993[CrossRef][Medline]

41. Kaplan EL, Meier P: Nonparametric estimation from incomplete observations. J Am Stat Assoc 53: 457-481, 1958[CrossRef]

42. Neter J: Simultaneous inferences and other topics in regression analysis-1, in Neter J, Wasserman W, Kutner M (eds): Applied Linear Regression Models, ed 1. Homewood, IL, Richard D. Irwin, Inc, 1983, pp 150-153

43. Kupelian P, Katcher J, Levin HS, et al: Stage T1-2 prostate cancer: A multivariate analysis of factors affecting biochemical and clinical features after radical prostatectomy. Int J Radiat Oncol Biol Phys 37: 1043-1052, 1997[CrossRef][Medline]

44. D’Amico AV, Whittington R, Kaplan I, et al: Equivalent biochemical failure free survival after external beam radiation therapy or radical prostatectomy in patients with a pretreatment prostate specific antigen of > 4-20 ng/ml. Int J Radiat Oncol Biol Phys 37: 1053-1058, 1997[CrossRef][Medline]

45. Kattan MW, Easthan JA, Stapleton AMF, et al: A preoperative nomogram for disease recurrence following radical prostatectomy for prostate cancer. J Natl Cancer Inst 90: 766-771, 1998[Abstract/Free Full Text]

Submitted November 14, 2001; accepted March 18, 2002.


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