Clinical Research

Race is associated with discontinuation of active surveillance of low-risk prostate cancer: Results from the Duke Prostate Center

Abstract

Background:

Active surveillance (AS) is increasingly utilized in low-risk prostate cancer (PC) patients. Although black race has traditionally been associated with adverse PC characteristics, its prognostic value for patients managed with AS is unclear.

Methods:

A retrospective review identified 145 patients managed with AS at the Duke Prostate Center from January 2005 to September 2011. Race was patient-reported and categorized as black, white or other. Inclusion criteria included PSA <10 ng ml−1, Gleason sum 6, and 33% of cores with cancer on diagnostic biopsy. The primary outcome was discontinuation of AS for treatment due to PC progression. In men who proceeded to treatment after AS, the trigger for treatment, follow-up PSA and biopsy characteristics were analyzed. Time to treatment was analyzed with univariable and multivariable Cox proportional hazards models and also stratified by race.

Results:

In our AS cohort, 105 (72%) were white, 32 (22%) black and 8 (6%) another race. Median follow-up was 23.0 months, during which 23% percent of men proceeded to treatment. The demographic, clinical and follow-up characteristics did not differ by race. There was a trend toward more uninsured black men (15.6% black, 3.8% white, 0% other, P=0.06). Black race was associated with treatment (hazard ratio (HR) 2.93, P=0.01) as compared with white. When the analysis was adjusted for socioeconomic and clinical parameters at the time of PC diagnosis, black race remained the sole predictor of treatment (HR 3.08, P=0.01). Among men undergoing treatment, the trigger was less often patient driven in black men (8 black, 33 white, 67% other, P=0.05).

Conclusions:

Black race was associated with discontinuation of AS for treatment. This relationship persisted when adjusted for socioeconomic and clinical parameters.

Introduction

In light of recent concerns regarding overtreatment of prostate cancer (PC), active surveillance (AS) has gained acceptance as a management strategy in men believed to be at low-risk for progression.1, 2, 3, 4 Although follow-up protocols for AS vary, the fundamental principles are to monitor patients with serial PSA testing, digital rectal examinations (DREs) and prostate needle biopsies, with the intent to intervene with curative therapy if disease progression is evident. The safety of AS relies upon the protracted natural history of low-risk PC so that the ‘window’ of curability is not missed during the follow-up period.5

The effect of race on PC has been studied extensively because of the fact that US black men have a 1.5 times increased incidence of PC and 2.5 times increased mortality compared with white men.6 The explanations for this are multifactorial and encompass sociological and biological factors,7 as well as potential disparities in quality of care.8

Whether racial differences in PC outcomes exist after adjustment for socioeconomic factors is unclear. Several studies have failed to show an association between race and PC outcomes after attempted curative therapy,9, 10, 11, 12, 13, 14 however, several others have demonstrated that black race independently predicts biochemical recurrence after prostatectomy and radiotherapy.15, 16, 17, 18, 19, 20 The data conflict even in studies adjusting for socioeconomic status or using ‘equal-access’ cohorts with some showing no association between race and outcome,21, 22, 23, 24 while others show black race predicts biochemical progression after prostatectomy.15, 19, 20, 25, 26

Whether race is truly a risk factor for PC aggressiveness is an important question for AS because delaying therapy for aggressive disease may compromise eventual curability. There have been two studies analyzing the effect of race on overall mortality in men undergoing delayed PC therapy or watchful waiting, with neither finding a significant difference.27, 28 A recent analysis has shown, however, that race is a predictor of biopsy progression on AS.29

We hypothesize that black men have more aggressive PC that are more likely to progress on AS, and are therefore more likely to proceed to treatment faster than white men. To test this, we performed a detailed comparison of the PC and socioeconomic characteristics of our AS cohort stratified by race. Furthermore, we analyzed the impact of race on the discontinuation of AS for treatment adjusting for these important potential confounders.

Materials and methods

Cohort

Following institutional review board approval, we retrospectively reviewed the records of 1820 patients with a PC diagnosis undergoing a prostate needle biopsy at our center between 1 January 2005 and 1 September 2011. Of these, we found 263 men (14.4%) who were either previously or currently managed expectantly. Specifically, to differentiate AS from other forms of expectant management, we required documentation in the medical record that men were counseled as to the necessary follow-up (PSA and biopsies) required on AS, elected AS over definitive local treatment, with the intent for curative therapy if there was evidence of disease progression on AS. We therefore excluded 45/263 (17%) patients that did not meet these criteria (either previously or currently undergoing watchful waiting), resulting in 218 patients on AS. We restricted our analysis to men on AS with clinically organ-confined PC (<cT3), and at least 12 cores sampled on diagnostic biopsy. We consider ideal candidates for AS to have PSA <10 ng ml−1, Gleason sum 6, and 33% of cores positive on initial biopsy. For the final analysis we therefore excluded 73/218 (33%) additional men who received AS, but had higher risk disease, resulting in a cohort of 145 men. As only eight of these men were of a non-black and non-white race (‘Other’), they were excluded from the progression to treatment analyses, but included in the descriptive analyses of the cohort for completeness.

Follow-up

As this was a retrospective analysis, follow-up protocols were not predetermined and were left to the discretion of the treating physicians. Men were deemed lost to follow-up if >1 year elapsed since the last documented visit, and their follow-up censored at the date of the last visit (23/145 (16%)). In men opting out of AS and electing treatment, follow-up was censored at the date of the communication in the medical record. When the treating physician determined PC progression based on surveillance biopsy, PSA, or physical examination and recommended definitive treatment, the censor date was the date of the performance of the study (PSA, DRE or biopsy) prompting that decision.

Statistical analysis

Race was patient-reported and classified as black, white or other. Positive family history was defined as PC in a first-degree male relative. Household income was derived by matching the patient’s home zip code at the time of diagnosis with the 2000 US census data. Uninsured patients were those coded as ‘self-pay’ in our institutional billing database.

Triggers for treatment were categorized as patient driven (preference, symptoms) or disease progression (biopsy, PSA, DRE). Disease progression was determined by the treating physician. PSA progression was typically determined using PSA velocity, which was calculated as the slope of the linear regression line (ng ml−1 per year) for each patient using all available PSA values on AS.30 Biopsy reclassification was determined by Gleason score upgrading, or an increase in the proportion of positive biopsy cores over 33%. In men who were treated for biopsy progression, the Gleason score of the final biopsy was stratified by sum (6, 7, 8). Treatment after AS was classified as androgen deprivation therapy, brachytherapy, cryosurgery, high-frequency focused ultrasound, radical prostatectomy and external beam radiotherapy. Vital status was determined by record review and was cross-referenced with the Social Security Administration death master file.

Univariable comparisons of characteristics for the overall cohort and in patients proceeding to treatment were performed across race groups using Fisher’s exact test for categorical variables and Kruskal–Wallis signed-rank tests for continuous variables. Continuous variables are reported as median values with interquartile ranges unless otherwise specified.

The association between race and time to discontinuation of AS for treatment was tested using Kaplan–Meier plots and the log-rank test, starting at the date of diagnostic biopsy. Two triggers for treatment were tested: all-cause and disease progression (patient-driven treatment censored). To estimate the hazard ratio (HR) and 95% confidence interval for proceeding to treatment, Cox proportional hazards regression models were utilized. A socioeconomic multivariable model was adjusted for household income (continuous, log-transformed) and insurance status (categorical uninsured vs insured). A clinical multivariable model was adjusted for PSA at diagnosis (continuous, log-transformed), age at diagnosis (continuous) and number of positive cores on initial biopsy (categorical 2 vs >2). A final model adjusted for household income and diagnostic PSA as these were the statistically significant covariates in the socioeconomic and clinical models, respectively.

Our primary aim was to determine whether black race was associated with PC progression-triggered treatment on multivariable analyses. All other analyses were considered secondary. All tests were two-tailed and P<0.05 considered significant. All statistical analyses were performed using R version 2.13.1 (R Foundation for Statistical Computing, Vienna, Austria).

Results

Of the 145 men meeting the enrollment criteria, 105 (72%) were Caucasian, 32 (22%) black and 8 (6%) any other race. There was a trend toward more uninsured black men (15.6% black, 3.8% white, 0% other, P=0.06). The race groups were well matched with regard to all of the other demographic, PSA, follow-up and other initial biopsy characteristics tested (Table 1).

Table 1 Characteristics of the AS cohort.

At a median follow-up time of 23.0 months after diagnosis, 77% of the cohort remain on AS. White men were more likely to remain on AS (83 white, 63 black, 63% other). The median time to treatment (both PC progression-triggered and any-cause) was 31.2 months for black men, and was not reached for men of white or other race. Among patients who received treatment, there were no statistically significant differences between races in PSA, number of biopsy cores with cancer or final Gleason sum (Table 2). However, there were trends toward higher median PSA (6.8 ng ml−1 vs 5.3 ng ml−1) and more positive cores on follow-up biopsies (median 7 vs 2.5) in black men that progressed to treatment compared with white men. In addition, there was a trend toward lower PSA velocities in white men proceeding to treatment, but not for those remaining on AS (Figure 1).

Table 2 Characteristics of men on AS proceeding to treatment.
Figure 1
figure1

Median PSA velocity by race and active surveillance (AS) status (remain on AS vs progressed to treatment).

Compared with other races, black men were more likely to be treated for PSA progression and less likely patient preference (P=0.05). In men who underwent at least one confirmatory biopsy, 11/62 white men (18%) were reclassified and underwent treatment compared with 7/19 black men (37%), which did not reach statistical significance (P=0.15). Complete treatment data were available for 30/33 men (91%) in which AS was discontinued. The most frequent treatment was radical prostatectomy in white men (56%) and external beam radiotherapy in black men (42%), which was not statistically different (P=0.37).

On unadjusted analysis, black men had a shorter time to treatment triggered by changes in disease parameters compared with white men (HR 2.93, P=0.01, Figure 2a). When we included treatment for patient-driven factors the results were similar (Figure 2b). As shown in Table 3, when the models were adjusted for socioeconomic status, clinical data and both, black race remained a statistically significant predictor of treatment for disease characteristics (HR 3.05–3.57, all P0.01), as well as treatment for any reason (HR 2.18–2.43, all P0.05).

Figure 2
figure2

(a) Crude time to treatment for changes in disease characteristics stratified by race. (b) Crude time to treatment for any reason stratified by race. AS, active surveillance; HR, hazard ratio.

Table 3 Effect of black race on proceeding to treatment.

At the time of data abstraction, the overall survival was 98%, metastases-free survival was 99%, and the PC-specific survival 100%. The three men who died (two white, one black) did so outside of our institution and had no evidence of metastases at the time of last follow-up. One patient (black), on AS for 5 years, was ultimately found to have metastatic disease when restaged after a surveillance biopsy revealed extensive Gleason 4+4 disease.

Discussion

To our knowledge two studies have examined the effect of race on overall survival for men undergoing expectant management for PC.27, 28 In their analysis of the Center for Prostate Disease Research database, Cullen et. al.27 found that although black men had a significantly shorter time to treatment of 24.5 months (vs 32.7 in white men, P=0.01), their overall survival was not different from white men. In their cohort 60% of the black men were intermediate or high risk. The other study, by Koscuiszka et. al.28, again found no difference in overall survival between black and white men undergoing watchful waiting. The authors highlight that competing causes of death are more common than death from PC, especially in their cohort in which the median age at PC diagnosis was 73 years. The applicability of the findings from these two studies to modern AS cohorts—which consist of low-risk men that are often surgical candidates—is limited. Recently, the University of Miami group explored a variety of clinical and demographic characteristics and found that non-white race predicted AS progression in their cohort, which is in-line with our findings.29 However, as racial differences were not the primary hypothesis of that study a detailed stratification by race was neither presented, nor were socioeconomic factors suspected to impact racial disparities (such as income and insurance status) examined.

The main finding of our study is that black race was associated with the discontinuation of AS for treatment, even when adjusted for socioeconomic status and clinical characteristics. Black men tended to have higher PSA velocity on AS and were less likely to opt-out than white men.

If black men on AS indeed proceed to treatment faster, what are the reasons? Are they primarily socioeconomic or biological? In this cohort, we identified a trend toward black men being less insured, which may alter health care availability. However, when adjusting our model for available socioeconomic indicators—insurance status and household income—the association between black race and progression to treatment strengthened. Furthermore, in contrast to earlier reports that non-white men may receive less frequent monitoring on watchful waiting for PC,31 in our cohort this was not evident as the number of PSA tests and biopsies on AS did not differ by race. Finally, to exclude the possibility that race was associated with opting out of AS, we considered treatment triggered by changes in PC clinical parameters alone. Regardless of the definition for proceeding to treatment the outcome was similar: black race was associated with earlier discontinuation of AS.

Although the actual explanation for the racial difference in our data is likely multifactorial and complex, our results support the hypothesis that in black men PC may progress more rapidly than in white men. While black men have been shown to have higher PSA at the time of PC diagnosis in the early PSA-era, the racial differences were explained by larger tumor volume on whole-mounted radical prostatectomy specimens.32 This suggested that a lack of screening penetrance in black men caused them to present with more advanced disease. In our cohort racial differences in PSA were not present initially, however, black men tended to progress to treatment based on higher PSA and PSA velocity. In addition, although not statistically different due to modest patient numbers, we found that black men were twice as likely to be reclassified at biopsy.

Several studies point to possible biological differences between black and white men with PC. In a study of over 1000 prostates examined on autopsy in men dying of reasons other than PC, black and white men aged 20–29 years were found to have equal prevalence of PC and similar tumor characteristics. However, in this same geographic population, black men had greater tumor volume in prostatectomy specimens and had a 4 × increased rate of metastatic disease, suggesting a faster growth rate and/or earlier transformation to aggressive PC in black men.33 In addition, black men have been shown to have higher levels of prostatic androstenedione and serum hormone-binding globulin that may activate the androgen receptor.34 Furthermore, several genes are more methylated in PC tissue of black men as compared with white.35 Finally, prostate biopsy tissue from black men has been shown to express higher levels of markers of aggressive disease such as Ki67.36 Future directions should include similar molecular testing of tissue from black and white men on AS to determine whether these biomarker or others can help further predict disease progression.

This study has several limitations. As this report contains our early AS experience, median follow-up was a relatively short 23 months. Although we feel this is adequate for the study of progression to treatment as an outcome, as it has been demonstrated that 80% of biopsy upgrading on AS will occur within 2 years,37 clearly more follow-up is necessary to determine how earlier progression to treatment correlates with other outcomes, such as metastases, and PC-specific and overall survival. Furthermore, biopsy upgrading can represent sampling error rather than biological progression. Although this could confound our results, we do not expect the rate of sampling error on prostate biopsy to vary by race. Also, the number of men included, especially black men, was modest. Despite limited statistical power, we still were able to detect a racial difference in AS progression, which is in-line with the aforementioned recent report from Miami.29 Finally, as this study was retrospective, the criteria for proceeding to treatment were heterogeneous as they were based on the judgment of the treating physician. We cannot exclude the possibility that some physicians may be biased toward a lower threshold to initiate treatment based on race, however, we feel this to be unlikely as black men tended to have higher PSA velocity and tumor volume when AS was discontinued.

Despite these limitations, this study has several strengths. To the best of our knowledge it is the first study to describe racial differences in PSA kinetics on AS. In addition, we present socioeconomic data and reasons for progressing to treatment in an attempt to define and control for non-biological factors. Our results have several potential applications. First, although AS remains a reasonable option for both black and white men, providers treating a racially diverse population can use theseis data to describe the expected course of AS. Second, as our data support building evidence that black men may progress faster on AS, future models of AS outcomes should consider race as a potential confounder. Ultimately, these findings require validation after additional follow-up and in other prospective studies.

Conclusion

In our early experience with AS, we demonstrate that black race was associated with earlier discontinuation of AS for PC treatment. This association appears to be independent of socioeconomic status and more consistent with faster PC growth rate in black men. Additional follow-up is necessary to determine how this affects the long-term outcomes in these men. If confirmed in prospective studies, race may be a useful factor to include in prognostic models for AS and may help guide more stringent follow-up for black men.

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Acknowledgements

This work was financially supported by Duke Urology Committee for Urologic Research, Education and Development (CURED) Endowment Fund.

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Correspondence to J W Moul.

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The authors declare no conflict of interest.

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Abern, M., Bassett, M., Tsivian, M. et al. Race is associated with discontinuation of active surveillance of low-risk prostate cancer: Results from the Duke Prostate Center. Prostate Cancer Prostatic Dis 16, 85–90 (2013). https://doi.org/10.1038/pcan.2012.38

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Keywords

  • prostate adenocarcinoma
  • active surveillance
  • race

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