Abstract
Background
Prostate-specific antigen (PSA) surveillance testing is a cornerstone of prostate cancer survivorship because patients with biochemical recurrence often have no symptoms. However, the investigation of guideline-concordant PSA surveillance across racial groups is limited. We examined racial differences in PSA surveillance testing 5-years post-definitive treatment for localized prostate cancer.
Methods
We created a population-based retrospective cohort from the Surveillance, Epidemiology, and End Results-Medicare linked database for men diagnosed with prostate cancer between the years 2007 to 2011 with Medicare claims through 2016 (N = 21,372). Multivariable log-binomial regression models were used to examine the effect of race on the likelihood of not receiving at least one PSA surveillance test annually 5-years post-definitive treatment.
Results
Black men had 90%, 71%, 44%, 34%, and 23% increased risk of not receiving at least one PSA surveillance test annually in the first, second, third, fourth, and fifth years of post-definitive treatment follow-up, respectively. The adjusted relative risk [ARR] for Black men compared to White men were 1.68 (95% Confidence Interval [CI], 1.37–2.07), 1.52 (95% CI, 1.32–1.75), 1.32 (95% CI, 1.17–1.48), and 1.16 (95% CI, 1.05–1.29) in the first, second, third, and fourth year of post-definitive treatment, respectively.
Conclusion
Black men were more likely not to receive guideline-concordant PSA surveillance testing following definitive treatment for localized prostate cancer during the first 4 years post-treatment. This study suggest room for improvement in defining survivorship care plans for Black men to increase use of PSA surveillance testing.
Introduction
In 2020, an estimated 191,930 new cases of prostate cancer will be diagnosed in the United States and 33,330 men will die from the disease [1]. Black men have the highest death rate for prostate cancer of any racial or ethnic groups in the United States, 2.4 times higher than White men [2]. The difference in mortality is reflective of higher incidence rates among Black men but may also reflect variations in treatment patterns by race [2]. There is great interest in defining optimal strategies for detection, treatment, and follow-up for Black men with prostate cancer in order to address these issues [3–6].
Detectable or rising prostate-specific antigen (PSA) levels after treatment are often the first indicator of recurrent prostate cancer. Early detection of rising PSA levels can facilitate potentially curative salvage therapy initiation [7]. However, since patients with biochemical recurrence often have no associated symptoms, PSA surveillance is a cornerstone of prostate cancer survivorship care [8]. If left untreated, biochemical recurrence can progress to metastatic disease and death [9]. PSA surveillance testing may be especially important in groups of men (e.g., Black men) experience documented disparities in cancer treatment, recurrence, and survival [4, 10]. Accordingly, we hypothesize a lower frequency of PSA surveillance testing in Black men compared to White men.
The National Comprehensive Cancer Network, in 2007, recommends PSA testing every 6–12 months for the first five years following definitive treatment for localized prostate cancer [11]. However, little research exists to document the extent to which guideline-concordant PSA surveillance following definitive treatment (surgery or radiation therapy) for clinically localized prostate cancer is utilized across racial groups [8]. Thus, the primary study objective was to examine racial differences in PSA surveillance testing and monitoring for the first 5 years post-definitive treatment for localized prostate cancer.
Materials and methods
Data source
We created a population-based retrospective cohort from the Surveillance, Epidemiology, and End Results-Medicare (SEER-Medicare) linked database for men diagnosed with prostate cancer between the years 2007 and 2011 (N = 246,608), with Medicare claims through the year 2016. SEER registries account for ~28% of the United States population [12]. The SEER-Medicare database link patient-level information on incident cancer diagnoses reported from the SEER registries with a master file of Medicare enrollment and claims for inpatient, outpatient, and physician services [12, 13].
We utilized several SEER-Medicare data files in this study. Cancer clinical information, Medicare status, and patients’ demographics were obtained from the Patient Entitlement and Diagnosis Summary File (PEDSF). Claims for inpatient and outpatient services were provided by physician billing, and non-institutional provider services (Part B) were captured from the Carrier/ National Claims History (NCH) file. Further, the Medicare Provider Analysis and Review (MEDPAR), institutional, through Part A file, and the Outpatient, institutional, through Part B, file was utilized to extract information regarding inpatient cancer care and hospital outpatient services, respectively. This study received IRB waiver from The University of Georgia Institutional Review Board.
Study cohort
The study cohort included Black and White men 66 years of age and older, whose first and only diagnosis of clinically localized prostate cancer was treated with definitive therapy, either surgery or radiation therapy. To ensure each patient had sufficient claims for PSA testing over the 5-year study period, we restricted the dates of diagnosis to January 1, 2007 through December 31, 2011 and followed patients until December 31, 2016. We further restricted the inclusion criteria of the study to men who were alive at five-year post-definitive treatment. Figure 1 presents the details on the inclusion and exclusion criteria of the analytical cohort.
Fig. 1. Study flow diagram displaying the sample counts for included and excluded observations, with the number of men excluded at each stage in the sample creation process.
SEER Surveillance, Epidemiology, and End Results, HMO health maintenance organization, ESRD end-stage renal disease, AJCC TNM, clinical staging system is the tumor, node, and metastasis (TNM) staging system developed by the American Joint Committee on Cancer (AJCC: 6th ed effective with 2004+ diagnosis, 7th effective with 2010+ diagnosis); PSA, prostate-specific antigen.
Men diagnosed at autopsy, or who had additional cancer diagnoses, metastatic disease at diagnosis, nodal involvement, or who were enrolled in Medicare because of End-Stage Renal Disease (ESRD) or disability were excluded from the study. We also excluded men enrolled in any health maintenance organization (Medicare Advantage Plan), and men not enrolled in both Medicare Part A (hospital coverage) and Part B (elective coverage for outpatient care) through the study period and 12 months pre-diagnosis to ensure complete capture of health services. We also excluded men who received definitive therapy and had missing claims data for the first 5-years following definitive therapy because of death or other reasons.
Outcomes
The primary outcome of interest was annual PSA testing during the first five years following receipt of definitive therapy (surgery or radiation therapy) among men with clinically localized prostate cancer. We defined annual PSA testing as having at least one PSA surveillance test post-definitive therapy (dichotomous variable – yes/no) per year. The beginning of the follow-up period was defined as the date of the end of primary therapy – for example., date of radical prostatectomy or last day of radiation therapy, more description in the appendix (Table A1). The Current Procedural Terminology (CPT)/Healthcare Common Procedure Coding System (HCPCS) procedure codes (PSA test - 84152, 84153, 84154, and G0103) were used to identify men who received PSA surveillance testing. Definitive therapy was identified using SEER treatment variables and Medicare claims, as described in the appendix (Table A1).
Covariates
We used demographic characteristics including race (Black and White), age (grouped into four categories: 66–69 years, 70–74 years, 75–79 years, and ≥80 years), marital status (grouped into married and unmarried/unknown), and population location (urban vs. rural) from the SEER. We grouped SEER regions into Northeast (Connecticut, New Jersey), South (Atlanta, rural Georgia, Kentucky, Louisiana), Central (Detroit, Iowa, New Mexico, Utah), and West (San Francisco, Hawaii, Seattle, San Jose, Los Angeles, greater California).
The Research Data Assistance Center (ResDAC) previously defined Medicare and Medicaid dual enrollees as Medicare enrollees who; (1) might have their Medicare Part B premium paid by their states’ Medicaid program (Specified Low-Income Beneficiaries); (2) might have both their Medicare Part B premium and their Medicare cost-sharing amounts paid by their states’ Medicaid under the Qualified Medicare Beneficiaries program; (3) might receive full Medicaid benefits [14]. The state buy-in variable in the Medicare denominator file as per the ResDAC definition is one potential way of identifying dual eligibility and has been used previously in population-based studies [14–16]. For the current study, we also used the state buy-in variable and categorized it as binary, yes if state buy-in, no otherwise. Men were also categorized into four groups based on the census tract poverty indicator for income percentile 0%–<5%, 5%–<10%, 10%–<20%, and 20–100%, as a proxy for access to health care resources.
The median household income level was divided into quartiles based on the total median household income of the entire cohort (<$45,875, $45,876–$63,988, $63,989–$88,596, and >$88,596). Additionally, we added the education level to the descriptive table (Table A4) for more insights about the socioeconomic status of the entire cohort. Education level was defined as the percentage of adults aged ≥25 across a neighborhood level with a high school diploma only in the census tract. We divided the education level into quartiles based on the total percentage of the entire cohort (<17%, 17%–26%, 27%–34%, and >34%).
Medicare claims data from the 12 months preceding prostate cancer diagnosis were used to obtain a combined National Cancer Institute (NCI) comorbidity score validated specifically for claims data [17]. Clinical characteristics at diagnosis included a clinical T stage, Gleason score, and PSA level were used to classify patients into low, intermediate, high risk using D’Amico criteria [18]. We were also interested in examining socioeconomic status by race on the likelihood of not receiving at least one PSA surveillance test. We obtained the median household income level measures from the Census Tract File; thus, men with missing census tract information were excluded from the follow-up models.
Statistical analysis
Descriptive statistics were used to characterize to the study cohort at baseline. Chi-square tests were performed to evaluate group differences in PSA testing. Multivariable log-binomial regression models were used to examine the effect of including demographic variables and clinical characteristics on the likelihood of not receiving at least one PSA surveillance test annually for the first five years following definitive treatment for localized prostate cancer. We also stratified the multivariable log-binomial regression models based on the risk of disease progression at diagnosis to investigate the differences in PSA monitoring across strata for White and Black men. We also stratified the multivariable log-binomial regression models based on the median household income to examine whether differences in PSA monitoring were due to socioeconomic status.
Sensitivity and robustness checks were conducted when the log-binomial models converged or not, as described in the appendix (Table A3). Statistical significance thresholds were set at α = 0.05. All analyses were performed using SAS statistical software (version 9.4, SAS Institute, Cary, NC).
Results
A total of 21,372 men met the study inclusion criteria (Fig. 1). Baseline demographic and clinical characteristics comparing Black and White men are listed in Table 1. Black men were more likely to live in urban areas, the South, states with more Medicaid buy-in, and in poorer regions [e.g., regional poverty indicator 20% to 100%] (all P, 0.0001; Table 1), compared to White men. Further, Black men were younger at diagnosis, had more comorbidities, and had a higher risk of disease progression at diagnosis (all P, .01; Table 1). Overall, in the first five years post-definitive treatment, Black men were more likely not to receive at least one PSA surveillance test annually (all P, 0.0001; Table 2), compared to White men.
Table 1.
Baseline characteristics of the study cohort.
| Characteristics | Entire cohort No. (%) |
White No. (%) |
Black No. (%) |
P |
|---|---|---|---|---|
| Age at diagnosis, y | ||||
| 66–69 | 8,049 (38) | 7,230 (37) | 819 (41) | 0.0037* |
| 70–74 | 8,010 (37) | 7,281 (38) | 729 (37) | |
| 75–79 | 3,983 (19) | 3,639 (19) | 344 (17) | |
| ≥80 | 1,330 (6) | 1,227 (6) | 103 (5) | |
| Year of diagnosis | ||||
| 2007 | 4,343 (20) | 3,961 (20) | 382 (19) | 0.4562 |
| 2008 | 4,110 (19) | 3,701 (19) | 409 (21) | |
| 2009 | 3,979 (19) | 3,616 (19) | 363 (18) | |
| 2010 | 4,452 (21) | 4,036 (21) | 416 (21) | |
| 2011 | 4,488 (21) | 4,063 (21) | 425 (21) | |
| Marital status | ||||
| Married | 16,148 (76) | 14,906 (77) | 1,242 (62) | <0.0001** |
| Not married or unknown | 5,224 (24) | 4,471 (23) | 753 (38) | |
| Prostate cancer risk group | ||||
| Low-risk | 8,129 (38) | 7,328 (38) | 801 (40) | 0.0077* |
| Intermediate-risk | 7,268 (34) | 6,652 (34) | 616 (31) | |
| High-risk | 5,975 (28) | 5,397 (28) | 578 (29) | |
| NCI comorbidity index at diagnosis | ||||
| 0 | 14,529 (68) | 13,449 (69) | 1,080 (54) | <0.0001** |
| >0 | 6,843 (32) | 5,928 (31) | 915 (46) | |
| Population | ||||
| Urban | 17,617 (82) | 15,803 (82) | 1,814 (91) | <0.0001** |
| Rural | 3,755 (18) | 3,574 (18) | 181 (9) | |
| Medicaid state buy-in status | ||||
| Yes | 1,289 (6) | 961 (5) | 328 (16) | <0.0001** |
| No | 20,083 (94) | 18,416 (95) | 1,667 (84) | |
| Census tract poverty indicator | ||||
| 0%–<5% Poverty | 6,713 (31) | 6,468 (33) | 245 (12) | <0.0001** |
| 5%–<10% Poverty | 6,171 (29) | 5,832 (30) | 339 (17) | |
| 10%–<20% Poverty | 5,440 (25) | 4,834 (25) | 606 (31) | |
| 20%–100% Poverty | 3,048 (14) | 2,243 (12) | 805 (40) | |
| Geographic region | ||||
| South | 5,629 (26) | 4,792 (25) | 837 (42) | <0.0001** |
| Northeast | 5,505 (26) | 4,975 (25) | 530 (27) | |
| Central | 3,382 (16) | 3,065 (16) | 317 (16) | |
| West | 6,856 (32) | 6,545 (34) | 311 (15) | |
NCI National Cancer Institute.
p value < 0.01;
p value < 0.0001.
Table 2.
PSA surveillance test distribution 5-years after definitive therapy for localized prostate cancer.
| PSA surveillance test year | Entire cohort No. (%) |
White No. (%) |
Black No. (%) |
P |
|---|---|---|---|---|
| Year 1 post-treatment | ||||
| No test | 746 (3) | 624 (3) | 122 (6) | <0.0001** |
| At least one test | 20,626 (97) | 18,753 (97) | 1,873 (94) | |
| Year 2 post-treatment | ||||
| No test | 1,601 (7) | 1,362 (7) | 239 (12) | <0.0001** |
| At least one test | 19,771 (93) | 18,015 (93) | 1,756 (88) | |
| Year 3 post-treatment | ||||
| No test | 2,434 (11) | 2,120 (11) | 314 (16) | <0.0001** |
| At least one test | 18,938 (89) | 17,257 (89) | 1,681 (84) | |
| Year 4 post-treatment | ||||
| No test | 3,091 (14) | 2,716 (14) | 375 (19) | <0.0001** |
| At least one test | 18,281 (86) | 16,661 (86) | 1,620 (81) | |
| Year 5 post-treatment | ||||
| No test | 4,034 (19) | 3,581 (18) | 453 (23) | <0.0001** |
| At least one test | 17,338 (81) | 15,796 (82) | 1,542 (77) | |
Abbreviations: PSA, prostate-specific antigen.
p value < 0.01;
p value < 0.0001.
In the unadjusted model, Black men had a 90% increased risk of not receiving at least one PSA surveillance in the first-year post-definitive treatment (relative risk [RR], 1.90; 95% Confidence Interval [CI], 1.58–2.30; Table A1). Black men also had a 71% increased risk of not receiving at least one PSA surveillance test during the second year of post-definitive treatment follow-up (RR, 1.71; 95% CI, 1.50–1.94; Table A1). Further, in the third, fourth, and fifth years of post-definitive treatment, Black men had 44%, 34%, and 23% increased risks of not receiving at least one PSA surveillance test annually (RR, 1.44; 95% CI, 1.29–1.60, RR, 1.34; 95% CI, 1.22–1.48, and RR, 1.23; 95% CI, 1.13–1.34, respectively; Table A1). In the adjusted model, controlling for potentially relevant covariates, racial differences persisted as shown in Table 3. Overall, the risks of not receiving at least one PSA surveillance test annually decreased with time since receiving definitive treatment.
Table 3.
Multivariate log-binomial regression models for patients not receiving at least one annual PSA surveillance test in the first five years following post-definitive treatment.
| First year | Second year | Third year | Fourth year | Fifth year | |
|---|---|---|---|---|---|
| Adj-RR (95% CI) | Adj-RR (95% CI) | Adj-RR (95% CI) | Adj-RR (95% CI) | Adj-RR (95% CI) | |
| Race | |||||
| White | Ref. | Ref. | Ref. | Ref. | Ref. |
| Black | 1.68 (1.37–2.07) | 1.52 (1.32–1.75) | 1.32 (1.17–1.48) | 1.16 (1.05–1.29) | 1.07 (0.98–1.18) |
| Age at diagnosis, y | |||||
| 66–69 | Ref. | Ref. | Ref. | Ref. | Ref. |
| 70–74 | 1.07 (0.91–1.26) | 1.05 (0.94–1.18) | 0.99 (0.91–1.09) | 1.05 (0.97–1.13) | 1.13 (1.06–1.21) |
| 75–79 | 1.02 (0.83–1.25) | 1.06 (0.93–1.21) | 1.10 (0.99–1.22) | 1.13 (1.03–1.24) | 1.31 (1.21–1.41) |
| ≥80 | 1.07 (0.79–1.45) | 1.12 (0.91–1.37) | 1.13 (0.97–1.32) | 1.38 (1.22–1.57) | 1.72 (1.56–1.90) |
| Year of diagnosis | |||||
| 2007 | Ref. | Ref. | Ref. | Ref. | Ref. |
| 2008 | 0.75 (0.61–0.93) | 0.84 (0.73–0.96) | 0.88 (0.79–0.99) | 1.01 (0.92–1.12) | 1.07 (0.98–1.17) |
| 2009 | 0.80 (0.65–0.99) | 0.84 (0.72–0.97) | 0.84 (0.74–0.95) | 0.93 (0.84–1.03) | 1.01 (0.92–1.10) |
| 2010 | 0.62 (0.50–0.78) | 0.74 (0.64–0.86) | 0.81 (0.72–0.91) | 0.90 (0.82–0.99) | 0.96 (0.88–1.05) |
| 2011 | 0.67 (0.54–0.83) | 0.72 (0.62–0.84) | 0.79 (0.70–0.90) | 0.83 (0.75–0.93) | 1.01 (0.92–1.10) |
| Marital status | |||||
| Married | Ref. | Ref. | Ref. | Ref. | Ref. |
| Not married or unknown | 1.06 (0.90–1.25) | 1.15 (1.04–1.28) | 1.14 (1.05–1.24) | 1.19 (1.11–1.28) | 1.15 (1.08–1.22) |
| Prostate cancer risk group | |||||
| Low-risk | Ref. | Ref. | Ref. | Ref. | |
| Intermediate-risk | 1.14 (0.95–1.35) | 1.18 (1.05–1.32) | 1.14 (1.04–1.25) | 1.13 (1.04–1.22) | 1.1 (1.03–1.18) |
| High-risk | 1.11 (0.93–1.33) | 0.97 (0.86–1.10) | 1.02 (0.93–1.13) | 1.02 (0.94–1.11) | 0.96 (0.89–1.03) |
| NCI comorbidity index at diagnosis | |||||
| 0 | Ref. | Ref. | Ref. | Ref. | Ref. |
| >0 | 0.65 (0.55–0.76) | 0.92 (0.83–1.02) | 0.90 (0.83–0.98) | 0.98 (0.92–1.06) | 1.08 (1.02–1.15) |
| Population | |||||
| Urban | Ref. | Ref. | Ref. | Ref. | Ref. |
| Rural | 0.82 (0.67–1.01) | 0.99 (0.87–1.13) | 1.08 (0.97–1.19) | 1.01 (0.92–1.10) | 1.04 (0.97–1.12) |
| Medicaid state buy-in status | |||||
| No | Ref. | Ref. | Ref. | Ref. | Ref. |
| Yes | 1.54 (1.21–1.97) | 1.47 (1.25–1.73) | 1.51 (1.32–1.71) | 1.54 (1.38–1.72) | 1.54 (1.41–1.67) |
| Census tract poverty indicatoi | |||||
| 0%–<5% Poverty | Ref. | Ref. | Ref. | Ref. | Ref. |
| 5%–<10% Poverty | 1.19 (0.97–1.48) | 1.05 (0.91–1.21) | 0.99 (0.89–1.11) | 1.06 (0.97–1.17) | 1.17 (1.08–1.26) |
| 10%–<20% Poverty | 1.35 (1.06–1.72) | 1.23 (1.04–1.44) | 1.05 (0.93–1.20) | 1.13 (1.01–1.26) | 1.22 (1.11–1.34) |
| 20%–100% Poverty | 1.23 (1.01–1.49) | 1.18 (1.04–1.34) | 0.98 (0.89–1.09) | 1.02 (0.93–1.15) | 1.08 (1.00–1.17) |
| Geographic region | |||||
| South | Ref. | Ref. | Ref. | Ref. | Ref. |
| Northeast | 0.99 (0.81–1.22) | 0.87 (0.76–1.00) | 0.81 (0.73–0.92) | 0.89 (0.81–0.98) | 0.99 (0.91–1.08) |
| Central | 0.72 (0.57–0.92) | 0.85 (0.73–0.98) | 0.95 (0.84–1.06) | 1.03 (0.93–1.14) | 1.05 (0.96–1.15) |
| West | 0.83 (0.69–1.01) | 0.87 (0.77–0.98) | 0.87 (0.78–0.96) | 0.87 (0.79–0.95) | 0.98 (0.90–1.05) |
Statistically significant findings are bolded.
Abbreviations: NCI, National Cancer Institute.
We next examined whether risk-stratified multivariable analysis would eliminate racial disparities. Black men who were high-risk at diagnosis were more likely to not receive at least one PSA surveillance test annually, compared to White men who were high-risk at diagnosis. In the first five years of follow-up post-definitive treatment relative risk for each year was (adjusted relative risk [ARR]: 1.53 (95% CI, 1.05–2.21), 1.75 (95% CI, 1.34–2.28), 1.35 (95% CI, 1.08–1.69), 1.27 (95% CI, 1.06–1.54), and 1.18 (95% CI, 1.00–1.39), respectively Table 4). Black men who were intermediate-risk at diagnosis were more likely to not receive, at least one PSA surveillance test annually, in the first three years post-definitive treatment compared to White men who were intermediate-risk at diagnosis (ARR, 2.04 (95% CI, 1.45–2.86), 1.45 (95% CI, 1.14–1.85), and 1.39 (95% CI, 1.14–1.69), respectively [Table 4]). Black men who were low-risk at diagnosis were more likely not to receive, at least one PSA surveillance test annually, in the first two years post-definitive treatment compared to White men who were low-risk at diagnosis (ARR, 1.75 (95% CI, 1.26–2.42), and 1.35 (95% CI, 1.07–1.69), respectively [Table 4]).
Table 4.
Risk status stratified multivariate log-binomial regression models for patients not receiving at least one annual PSA surveillance test in the first five years following post-definitive treatment.
| Not receiving PSA surveillance test year | Low-risk Adjusted-RR (95% CI)a | Intermediate-risk Adjusted-RR (95% CI)a | High-risk Adjusted-RR (95% CI)a |
|---|---|---|---|
| Year 1 post-treatment | |||
| Black vs. White | 1.753 (1.269–2.421) | 2.041 (1.452–2.867) b | 1.53 (1.054–2.216) b |
| Year 2 post-treatment | |||
| Black vs. White | 1.352 (1.077–1.697) | 1.456 (1.142–1.856) | 1.753 (1.347–2.281) |
| Year 3 post-treatment | |||
| Black vs. White | 1.181 (0.974–1.431) | 1.394 (1.145–1.697) | 1.356 (1.088–1.691) |
| Year 4 post-treatment | |||
| Black vs. White | 1.157 (0.979–1.368) | 1.028 (0.848–1.246) | 1.278 (1.060–1.541) |
| Year 5 post-treatment | |||
| Black vs. White | 1.045 (0.902–1.211) | 1.027 (0.872–1.208) | 1.182 (1.004–1.393) |
Statistically significant results are bolded.
Abbreviations: NCI, National Cancer Institute, RR, relative risk, CI, confidence interval.
Covariates adjusted in the log-binomial models: age at diagnosis, year of diagnosis, marital status, geographic region, population density, poverty indicator, state buy-in status, NCI comorbidity index at diagnosis.
Covariates (regional poverty indicator and state buy-in status) were not included in the log-binomial models because of the models did not converge.
Analyses also were conducted to examine whether differences in PSA monitoring were due to socioeconomic status. Black men with the median household income <$45,875 at diagnosis were more likely to not receive at least one PSA surveillance test annually for each of the five years of follow-up examined, compared to White men who were in the same household income quarter. In the first five years of follow-up post-definitive treatment, the relative risks for years 1–5, were (ARR: 1.60 (95% CI, 1.14–2.25), 1.45 (95% CI, 1.17–1.81), 1.51 (95% CI, 1.26–1.80), 1.20 (95% CI, 1.02–1.40), and 1.14 (95% CI, 1.00–1.31), respectively Table A5).
Results also showed that racial disparities in the likelihood of not receiving at least one PSA surveillance test annually in the first and second-year post-definitive treatment (Table A5) between Black and White men with incomes <$45,875 and between $45,876 and $63,988 were statistically significant (ARR: 1.603, 2.969 (95% CI, 1.141–2.252; 2.023–4.356) and ARR: 1.450, 1.520 (95% CI, 2.023–4.356; 1.097–2.106). Racial disparities in the likelihood of not receiving at least one PSA surveillance test annually were also statistically significant between Black and White men in the third, fourth, and fifth years post-definitive treatment (Table A5) with income <$45,875 (ARR: 1.508, 1.200, 1.141 (95% CI, 1.261–1.803; 1.025–1.404; 1.001–1.307). Table A6 shows that racial disparities in the likelihood of not receiving at least one PSA surveillance test annually in the first and second-year post-definitive treatment were similar without including covariates. Table A7 show that overall patterns of PSA surveillance were not changed when the follow-up window for PSA surveillance testing five years post-definitive treatment were allowed to be 14 Months. Table A8 shows results for Risk Status Stratified Subsamples, demonstrating that racial disparities were not limited to low-risk groups.
Discussion
After definitive surgery or radiation treatment, the measurement of serum PSA level is regarded as the most useful tool for monitoring patients because serum PSA is the first indicator of recurrence preceding the development of symptomatic disease [19]. For patients initially treated with intent to cure, a serum PSA level should be measured every 6–12 months for the first five years and then rechecked annually [11]. When prostate cancer recurred after radical prostatectomy, Pound et al. [9], found that 45% of patients experienced recurrence within the first two years, 77% within the first five years, and 96% by ten years. Therefore, monitoring serum PSA is essential for surveillance after radical prostatectomy in order to identify patients who might need additional treatment for recurrence. In addition, higher risk individuals have increased need for this surveillance and identifying early recurrence in the first two years is particularly important. However, our study finds that among Black men, among whom the disease rate is highest, and who are at greater risk on average, PSA monitoring is often underutilized, and is substantially underutilized relative to its use with White men. The disparity among White and Black men in PSA monitoring is widest in the first year after post-definitive treatment. The disparity narrows gradually in years two, three, and four, post definitive treatment but remains significantly different between the races. The disparity is not accounted for risk level, with substantially greater risk for low monitoring among Black men in years one and two of the follow-up period, even among those in the highest risk category.
Dess et al. [20], assessed prostate cancer specific mortality, other-cause mortality, and all-cause mortality differences between Black and White men to quantify population-based estimates of disparities. The researchers examined data from a US population-based cohort using the SEER program, a multicenter cohort from five equal access regional hospitals within the Veterans Affairs (VA) health system, and an individual patient-level cohort of men treated in four National Cancer Institute-sponsored Radiation Therapy Oncology Group (RTOG) randomized clinical trials (RCTs) with mature follow-up. Within SEER Black men had a 0.5% absolute increased rate of prostate cancer specific mortality at 10 years, with no statistically significant difference evident in the high-risk subgroup. However, Black men were not associated with inferior prostate cancer specific mortality outcomes in systems with equal access to care (VA cohort) or cooperative group trials (RCT cohort) using standardized treatment approaches and follow-up. The authors demonstrated that significant disparities remain at the population level for Black men with prostate cancer.
In the unadjusted SEER cohort, Black men had higher rates of socioeconomic barriers to access of timely, high quality medical care including lower composite scores of income, housing, occupation, and educational attainment, along with lower rates of insurance [20]. Black race remains associated with many factors that negatively affect outcomes and disparities persist at the population level [20]. To a large extent, health inequalities by race may be due to differences in the quality of treatment received [21]. Continued efforts are needed to address this clear racial health inequity driven by modifiable nonbiological risk factors.
Our study adds to the modifiable nonbiological risk factors for prostate cancer health inequity and finds race-related disparities in adherence to monitoring recommendations. Despite the public health burden of prostate cancer and the importance of monitoring serum PSA in survivorship care, little still remains known about patterns of adherence to evidence-based recommendations in real-world patients [8]. A retrospective SEER-Medicare study investigating whether men receive guideline-concordant PSA surveillance testing conducted by Trantham et al. [8], found that receipt of surveillance testing was high, with 96% of men receiving at least one test the first year after treatment and ~80% receiving at least one test in the fifth year. However, Non-Hispanic Blacks and Hispanics had higher odds of not receiving a test compared to Non-Hispanics White men [8]. Although the racial disparity results in no way suggest that differences in surveillance lead to differences in mortality, they do suggest that the difference in surveillance by race may be clinically significant as well as statistically significant [8].
In our study, we followed men who received definitive therapy (surgery or radiation therapy), which enabled us to capture a larger sample size; whereas Trantham et al. [8], who only followed men who had a radical prostatectomy. Furthermore, Trantham et al. [8], did not account for the changes in not receiving at least one PSA surveillance test each year individually. We evaluated the relative risk of not receiving at least one PSA surveillance test annually over a five-year per year to mirror the clinical practice in the real world. In each year’s model, we stratified men based on their prostate cancer risk group to gain more insights about racial disparity in receiving PSA surveillance tests. Moreover, we also stratified prostate cancer risk at diagnosis as low, intermediate, high risk [18], and evaluated the risk of receiving at least one PSA annually, whereas Trantham et al. [8], did not account for prostate cancer risk at diagnosis.
We also found that the risks of not receiving at least one PSA surveillance test annually decreased with time since receiving definitive treatment. A major problem in assessing PSA surveillance frequency is that patients who have an increasing PSA are often treated differently than those who do not [7]. Very often, patients with a rising PSA will have their PSA rechecked several times while being treated with antibiotics for a possible infection or anti-inflammatories for possible prostatitis [7]. In contrast, patients without an increasing PSA will not have such intensive PSA testing [7]. This may be a possible explanation for the decreased risk of not receiving at least one PSA surveillance test annually since receiving definitive treatment.
Furthermore, there is some concern in healthcare regarding disparate attitudes toward patients based on their race by healthcare providers. Previous studies have shown that in some cases Black patients with similar symptoms as White patients receive different medical treatment. For example, Black patients are less likely to be given pain medication, are more likely to wait longer to receive emergency room care and are more likely to receive different treatment for chest pain in comparison to White patients [22–25]. Similarly, there is some concern in healthcare that Black patients may have less trust of physicians than do white patients [26, 27], leading them to be less inclined to participate in medical screenings [28], a factor that could potentially be addressed via enhanced engagement protocols [29, 30]. Recent studies have also shown that physician encouragement is not enough and should be paired with tailored discussion that provide pros and cons of screening.
Another limitation of this study is that we did not identify reasons that may contribute to disparities in PSA surveillance testing after treatment. While our study does not examine factors associated with race-related disparities in monitoring PSA during follow-up to treatment for prostate cancer, results indicate that there are important disparities in care processes which should be considered by health care stakeholders. Future research should identify factors that are associated with these disparities in an effort to develop tailored and targeted interventions to enhance care, improve outcomes, and reduce costs.
Notably, we also found that high risk Black patients did have receive more PSA surveillance testing than low-risk Black patients. We had expected high risk Black patients to be monitored more rigorously in order to reduce the increased likelihood of prostate cancer specific morality. Despite the widespread adoption of PSA screening leading to a greater incidence of localized prostate cancer, minority patients continue to present with higher rates of advanced-stage cancer or cancer-related mortality [31–33]. Another population-based SEER-Medicare study found that the gap in definitive therapy for Black men did not decrease from 2004 to 2010 across different prostate cancer risk strata, thereby leading to higher prostate cancer specific mortality [34].
To the best of our knowledge, this study is the first analysis to investigate racial differences in PSA surveillance testing 5-years post-definitive treatment for localized prostate cancer. However, this study has limitations that warrant mention. First, this study used SEER cancer registry with Medicare fee-for-service insurance claims to identify PSA testing and the study sample. The use of claims data may limit the generalizability of results to the entire prostate cancer population. In our study, Black men were more likely to be excluded on the basis of age at diagnosis, enrollment in Medicare because of end-stage renal disease or other disability, enrollment in any health maintenance organization, and missing claims data for the following first 5-years because of death or other reasons (Table A9). However, the applied exclusion criteria were used to ensure that utilization data were complete for every patient. Second, unmeasured factors such as not knowing whether patients may progress to a metastatic disease during the 5-year observational study follow-up period may affect measuring PSA testing follow up. Disease progressing status after diagnosis is not provided by the Medicare claims. Nevertheless, we used clinical characteristics at diagnosis such as clinical T stage, Gleason score, and PSA level to calculate each patient’s risk of 5-year treatment failure [18]. Finally, we stratified prostate cancer risk at diagnosis as low, intermediate, high risk [18], and evaluated the risk of receiving at least one PSA annually to appropriately reflect real-world clinical practice.
Conclusion
Overall, we found that in the first four years of post-definitive treatment, Black men had an increased risk of not receiving at least one PSA surveillance test annually compared to White men. Further, Black men who were high-risk were more likely to not receive, at least one PSA surveillance test annually, in the first five years post-definitive treatment compared to White men who were high-risk. This disparity in PSA surveillance testing was also observed in Black men who were intermediate-risk at diagnosis compared to White men for the first three years post-definitive treatment, and Black men were at low-risk for the first two years post-definitive treatment compared to White men. However, the disparity in PSA surveillance testing was not observed among Black and White men who had high household incomes in the majority of years post-definitive treatment.
Supplementary Material
Funding
The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by National Cancer Institute Grant 1K01CA230193-01A1, National Institute of Health KL2 Scholars Grant KL2TR00238, National Center for Advancing Translational Sciences UL1 Diversity Supplement Grant 3UL1TR002378-02S2, and Institutional Research Grant-14-193-01 from the American Cancer Society.
Footnotes
Conflict of interest The authors declare no competing interests.
Previously presented as a poster presentation at the 2020 American Society for Clinical Oncology Annual Meeting.
Supplementary information The online version contains supplementary material available at https://doi.org/10.1038/s41391-021-00365-w.
References
- 1.American Cancer Society. Cancer facts & figures 2020. Atlanta: American Cancer Society; 2020. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.American Cancer Society. Cancer facts & figures for African Americans 2016–8. Atlanta: American Cancer Society. 2016. [Google Scholar]
- 3.Chen RC, Rumble RB, Jain S. Active surveillance for the management of localized prostate cancer (Cancer Care Ontario guideline): American Society of Clinical Oncology Clinical Practice Guideline Endorsement Summary. J Oncol Pract. 2016; 12:267–9. [DOI] [PubMed] [Google Scholar]
- 4.Godley PA, Schenck AP, Amamoo MA, Schoenbach VJ, Peacock S, Manning M, et al. Racial differences in mortality among Medicare recipients after treatment for localized prostate cancer. J Natl Cancer Inst. 2003;95:1702–10. [DOI] [PubMed] [Google Scholar]
- 5.Carpenter WR, Howard DL, Taylor YJ, Ross LE, Wobker SE, Godley PA. Racial differences in PSA screening interval and stage at diagnosis. Cancer Causes Control CCC. 2010;21:1071–80. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Cobran EK, Chen RC, Overman R, Meyer AM, Kuo TM, O’Brien J, et al. Racial differences in diffusion of intensity-modulated radiation therapy for localized prostate cancer. Am J Men Health. 2016;10:399–407. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Ciezki JP, Reddy CA, Stephenson AJ, Angermeier K, Ulchaker J, Altman A, et al. The importance of serum prostate-specific antigen testing frequency in assessing biochemical and clinical failure after prostate cancer treatment. Urology. 2010;75:467–71. [DOI] [PubMed] [Google Scholar]
- 8.Trantham LC, Nielsen ME, Mobley LR, Wheeler SB, Carpenter WR, Biddle AK. Use of prostate-specific antigen testing as a disease surveillance tool following radical prostatectomy. Cancer. 2013;119:3523–30. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Pound CR, Partin AW, Eisenberger MA, Chan DW, Pearson JD, Walsh PC. Natural history of progression after PSA elevation following radical prostatectomy. JAMA 1999;281:1591–7. [DOI] [PubMed] [Google Scholar]
- 10.Jemal A, Ward E, Wu X, Martin HJ, McLaughlin CC, Thun MJ. Geographic patterns of prostate cancer mortality and variations in access to medical care in the United States. Cancer Epidemiol Prev Biomark. 2005;14:590–5. [DOI] [PubMed] [Google Scholar]
- 11.Mohler JL. The 2010 NCCN clinical practice guidelines in oncology on prostate cancer. J Natl Compr Canc Netw. 2010;8:145. [DOI] [PubMed] [Google Scholar]
- 12.Warren JL, Klabunde CN, Schrag D, Bach PB, Riley GF. Overview of the SEER-Medicare data: content, research applications, and generalizability to the United States elderly population. Medical Care. 2002;40:Iv-3–18. [DOI] [PubMed] [Google Scholar]
- 13.National Cancer Institute. Surveillance, epidemiology, and end results (SEER) overview fact sheets. Rockville, MD: NCI; 2020. https://seer.cancer.gov/about/factsheets/SEER_Overview.pdf. [Google Scholar]
- 14.Koroukian SM, Dahman B, Copeland G, Bradley CJ. The utility of the state buy-in variable in the Medicare denominator file to identify dually eligible Medicare-Medicaid beneficiaries: a validation study. Health Serv Res. 2010;45:265–82. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Koroukian SM, Xu F, Dor A, Cooper GS. Colorectal cancer screening in the elderly population: disparities by dual Medicare-Medicaid enrollment status. Health Serv Res. 2006;41:2136–54. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.O’Leary JE, Sloss EM, Melnick G. Disabled Medicare beneficiaries by dual eligible status: California, 1996–2001. Health Care Financing Rev. 2007;28:57–67. [PMC free article] [PubMed] [Google Scholar]
- 17.Stokes WA, Hendrix LH, Royce TJ, Allen IM, Godley PA, Wang AZ, et al. Racial differences in time from prostate cancer diagnosis to treatment initiation: a population-based study. Cancer. 2013; 119:2486–93. [DOI] [PubMed] [Google Scholar]
- 18.D’Amico AV, Whittington R, Malkowicz SB, Schultz D, Blank K, Broderick GA, et al. Biochemical outcome after radical prostatectomy, external beam radiation therapy, or interstitial radiation therapy for clinically localized prostate cancer. JAMA 1998;280:969–74. [DOI] [PubMed] [Google Scholar]
- 19.Matsumoto K, Niwa N, Hattori S, Takeda T, Morita S, Kosaka T, et al. Establishment of the optimal follow-up schedule after radical prostatectomy. Urologic Oncol. 2018;36:341.e9–.e14. [DOI] [PubMed] [Google Scholar]
- 20.Dess RT, Hartman HE, Mahal BA, Soni PD, Jackson WC, Cooperberg MR, et al. Association of black race with prostate cancer–specific and other-cause mortality. JAMA Oncol. 2019;5: 975–83. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Paller CJ, Wang L, Brawley OW. Racial inequality in prostate cancer outcomes—socioeconomics. Not Biol JAMA Oncol. 2019;5:983–4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Johnson TJ, Weaver MD, Borrero S, Davis EM, Myaskovsky L, Zuckerbraun NS, et al. Association of race and ethnicity with management of abdominal pain in the emergency department. Pediatrics 2013;132:e851–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Venkat A, Hoekstra J, Lindsell C, Prall D, Hollander JE, Pollack CV Jr., et al. The impact of race on the acute management of chest pain. Acad Emerg Med. 2003;10:1199–208. [DOI] [PubMed] [Google Scholar]
- 24.Weisse CS, Sorum PC, Dominguez RE. The influence of gender and race on physicians’ pain management decisions. J Pain. 2003; 4:505–10. [DOI] [PubMed] [Google Scholar]
- 25.Weisse CS, Sorum PC, Sanders KN, Syat BL. Do gender and race affect decisions about pain management? J Gen Intern Med. 2001;16:211–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Armstrong K, McMurphy S, Dean LT, Micco E, Putt M, Halbert CH, et al. Differences in the patterns of health care system distrust between blacks and whites. J Gen Intern Med. 2008; 23:827–33. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Armstrong K, Ravenell KL, McMurphy S, Putt M. Racial/ethnic differences in physician distrust in the United States. Am J Public Health. 2007;97:1283–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Davis JL, Bynum SA, Katz RV, Buchanan K, Green BL. Socio-demographic differences in fears and mistrust contributing to unwillingness to participate in cancer screenings. J Health Care Poor Underserved. 2012;23:67–76. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Myers RE, Chodak GW, Wolf TA, Burgh DY, McGrory GT, Marcus SM, et al. Adherence by African American men to prostate cancer education and early detection. Cancer: Inter-disciplinary. Int J Am Cancer Soc. 1999;86:88–104. [DOI] [PubMed] [Google Scholar]
- 30.Wen W, Luckenbaugh AN, Bayley CE, Penson DF, Shu XO. Racial disparities in mortality for patients with prostate cancer after radical prostatectomy. Cancer. 2020. 10.1002/cncr.33152. [Eub ahead of print]. [DOI] [PubMed] [Google Scholar]
- 31.Wang EH, Yu JB, Abouassally R, Meropol NJ, Cooper G, Shah ND, et al. Disparities in treatment of patients with high-risk prostate cancer: results from a population-based cohort. Urology. 2016;95:88–94. [DOI] [PubMed] [Google Scholar]
- 32.Welch HG, Fisher ES, Gottlieb DJ, Barry MJ. Detection of prostate cancer via biopsy in the Medicare-SEER population during the PSA era. J Natl Cancer Inst. 2007;99:1395–400. [DOI] [PubMed] [Google Scholar]
- 33.Jones BA, Liu WL, Araujo AB, Kasl SV, Silvera SN, Soler-Vila H, et al. Explaining the race difference in prostate cancer stage at diagnosis. Cancer Epidemiol Biomark Prev. 2008;17: 2825–34. [DOI] [PubMed] [Google Scholar]
- 34.Mahal BA, Aizer AA, Ziehr DR, Hyatt AS, Sammon JD, Schmid M, et al. Trends in disparate treatment of African American men with localized prostate cancer across National Comprehensive Cancer Network risk groups. Urology. 2014;84:386–92. [DOI] [PubMed] [Google Scholar]
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