Progression on active surveillance for prostate cancer in Black men: a systematic review and meta-analysis | Prostate Cancer and Prostatic Diseases
Progression on active surveillance for prostate cancer in Black men: a systematic review and meta-analysis
Abstract
Background
Several studies evaluated prostate cancer (PCa) outcomes in Black men on active surveillance (AS); most studies contained few Black men and results were conflicting. We performed a systematic review and meta-analyze of race and outcomes on AS.
Methods
A systematic search was performed for articles of men with Grade Group 1 or 2 (GG1 or GG2) PCa on AS. All studies required race-specific comparative progression data. Progression to treatment, PSA, or biopsy progression were considered and relative risk (RR) estimates of Black men progressing were extracted and pooled using random-effects models. Differences by study-level characteristics were evaluated using subgroup and a cumulative meta-analysis by time.
Results
In total, 12 studies were included (3137 Black and 12,206 non-Black men); eight prospective (27%, n = 4210) and four retrospectives (73%, n = 11,133) cohorts. The overall RR of progression for Black men was 1.62 (95%CI, 1.21–2.17), I2 = 64% (95% CI, 32–80%), (χ2 = 30.23; P = 0.001; Ï„2 = 0.16). Black men with GG1 PCa alone had a higher pooled progression: RR = 1.81 (95% CI, 1.23–2.68). Including only studies with clinical progression (excluding progression to treatment), potentiated results: RR = 1.82 (95%CI, 1.27–2.60). However, a cumulative meta-analysis demonstrated decreasing pooled effect over time, with contemporary studies after 2019 showing a tempered effect (RR: 1.29, 95% CI: 1.20–1.39).
Conclusions
Many studies attribute racial disparity in PCa to delayed presentation of disease, however, AS is unique since all AS eligible men have a low grade and stage PCa. Our findings suggest Black men may have an increased risk of progression during AS, but the association is not so strong that Black men should be discouraged from undergoing AS. Indeed, contemporary evidence suggests stricter inclusion, better confirmatory testing or better access to care may temper these findings. Importantly, these results utilize self-reported race, a social construct that has many limitations.
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References
- 1.
Schroder FH, Hugosson J, Roobol MJ, Tammela TL, Ciatto S, Nelen V, et al. Screening and prostate-cancer mortality in a randomized European study. N Engl J Med. 2009;360:1320–8.
- 2.
Schaeffer E, Srinivas S, Antonarakis ES, Armstrong AJ, Bekelman JE, Cheng H, et al. NCCN guidelines insights: prostate cancer, version 1.2021. J Natl Compr Canc Netw. 2021;19:134–43.
- 3.
Chen RC, Rumble RB, Loblaw DA, Finelli A, Ehdaie B, Cooperberg MR, et al. Active surveillance for the management of localized prostate cancer (cancer care Ontario guideline): American society of clinical oncology clinical practice guideline endorsement. J Clin Oncol. 2016;34:2182–90.
- 4.
Hamdy FC, Donovan JL, Lane JA, Mason M, Metcalfe C, Holding P, et al. 10-Year outcomes after monitoring, surgery, or radiotherapy for localized prostate cancer. N Engl J Med. 2016;375:1415–24.
- 5.
Potts JM, Lutz M, Walker E, Modlin C, Klein E. Trends in PSA, age and prostate cancer detection among black and white men from 1990–2006 at a tertiary care center. Cancer. 2010;116:3910–5.
- 6.
Powell IJ, Banerjee M, Sakr W, Grignon D, Wood DP Jr., Novallo M, et al. Should African-American men be tested for prostate carcinoma at an earlier age than white men? Cancer. 1999;85:472–7.
- 7.
Chornokur G, Dalton K, Borysova ME, Kumar NB. Disparities at presentation, diagnosis, treatment, and survival in African American men, affected by prostate cancer. Prostate. 2011;71:985–97.
- 8.
Tsivian M, Banez LL, Keto CJ, Abern MR, Qi P, Gerber L, et al. African-American men with low-grade prostate cancer have higher tumor burdens: results from the Duke Prostate Center. Prostate Cancer Prostatic Dis. 2013;16:91–4.
- 9.
Gokce MI, Sundi D, Schaeffer E, Pettaway C. Is active surveillance a suitable option for African American men with prostate cancer? A systemic literature review. Prostate Cancer Prostatic Dis. 2017;20:127–36.
- 10.
Iremashvili V, Soloway MS, Rosenberg DL, Manoharan M. Clinical and demographic characteristics associated with prostate cancer progression in patients on active surveillance. J Urol. 2012;187:1594–9.
- 11.
Abern MR, Bassett MR, Tsivian M, Banez LL, Polascik TJ, Ferrandino MN, 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. 2013;16:85–90.
- 12.
Odom BD, Mir MC, Hughes S, Senechal C, Santy A, Eyraud R, et al. Active surveillance for low-risk prostate cancer in African American men: a multi-institutional experience. Urology. 2014;83:364–8.
- 13.
Cohn JA, Dangle PP, Wang CE, Brendler CB, Novakovic KR, McGuire MS, et al. The prognostic significance of perineural invasion and race in men considering active surveillance. BJU Int. 2014;114:75–80.
- 14.
Davis JW, Ward JF 3rd, Pettaway CA, Wang X, Kuban D, Frank SJ, et al. Disease reclassification risk with stringent criteria and frequent monitoring in men with favourable-risk prostate cancer undergoing active surveillance. BJU Int. 2016;118:68–76.
- 15.
Kelly SP, Van Den Eeden SK, Hoffman RM, Aaronson DS, Lobo T, Luta G, et al. Sociodemographic and clinical predictors of switching to active treatment among a large, ethnically diverse cohort of men with low risk prostate cancer on observational management. J Urol. 2016;196:734–40.
- 16.
Bloom JB, Lebastchi AH, Gold SA, Hale GR, Sanford T, Mehralivand S, et al. Use of multiparametric magnetic resonance imaging and fusion-guided biopsies to properly select and follow African-American men on active surveillance. BJU Int. 2019;124:768–74.
- 17.
Shelton JB, Paivanas TA, Buffington P, Ruyle SR, Cohen ES, Natale R 2nd, et al. Three-year active surveillance outcomes in a contemporary community urology cohort in the United States. Urology. 2019;130:72–78.
- 18.
Schenk JM, Newcomb LF, Zheng Y, Faino AV, Zhu K, Nyame YA, et al. African American race is not associated with risk of reclassification during active surveillance: results from the canary prostate cancer active surveillance study. J Urol. 2020;203:727–33.
- 19.
Tosoian JJ, Mamawala M, Epstein JI, Landis P, Macura KJ, Simopoulos DN, et al. Active surveillance of grade group 1 prostate cancer: long-term outcomes from a large prospective cohort. Eur Urol. 2020;77:675–82.
- 20.
Deka R, Courtney PT, Parsons JK, Nelson TJ, Nalawade V, Luterstein E, et al. Association between African American race and clinical outcomes in men treated for low-risk prostate cancer with active surveillance. JAMA. 2020;324:1747–54.
- 21.
Greenberg JW, Leinwand G, Feibus AH, Haney NM, Krane LS, Thomas R, et al. Prospective observational study of a racially diverse group of men on active surveillance for prostate cancer. Urology. 2020;148:203–10.
- 22.
Simpkin AJ, Tilling K, Martin RM, Lane JA, Hamdy FC, Holmberg L, et al. Systematic review and meta-analysis of factors determining change to radical treatment in active surveillance for localized prostate cancer. Eur Urol. 2015;67:993–1005.
- 23.
Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Open Med. 2009;3:e123–30.
- 24.
Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA. 2000;283:2008–12.
- 25.
Egger M, Smith GD, Phillips AN. Meta-analysis: principles and procedures. BMJ. 1997;315:1533–7.
- 26.
Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–58.
- 27.
Cochran WG. The comparison of percentages in matched samples. Biometrika. 1950;37:256–66.
- 28.
Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–34.
- 29.
Balduzzi S, Rucker G, Schwarzer G. How to perform a meta-analysis with R: a practical tutorial. Evid Based Ment Health. 2019;22:153–60.
- 30.
Viechtbauer W. Conducting meta-analyses in R with the metafor package. J Stat Softw. 2010;36:1–48.
- 31.
Fuentes A, Ackermann RR, Athreya S, Bolnick D, Lasisi T, Lee SH, et al. AAPA statement on race and racism. Am J Phys Anthropol. 2019;169:400–2.
- 32.
Mersha TB, Abebe T. Self-reported race/ethnicity in the age of genomic research: its potential impact on understanding health disparities. Hum Genom. 2015;9:1.
- 33.
Bryc K, Durand EY, Macpherson JM, Reich D, Mountain JL. The genetic ancestry of African Americans, Latinos, and European Americans across the United States. Am J Hum Genet. 2015;96:37–53.
- 34.
Hjelmborg JB, Scheike T, Holst K, Skytthe A, Penney KL, Graff RE, et al. The heritability of prostate cancer in the Nordic twin study of cancer. Cancer Epidemiol Biomark Prev. 2014;23:2303–10.
- 35.
Ben J, Cormack D, Harris R, Paradies Y. Racism and health service utilisation: a systematic review and meta-analysis. PLoS ONE. 2017;12:e0189900.
- 36.
Kelly SP, Rosenberg PS, Anderson WF, Andreotti G, Younes N, Cleary SD, et al. Trends in the Incidence of fatal prostate cancer in the United States by race. Eur Urol. 2017;71:195–201.
- 37.
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.
- 38.
Mygatt JG, Cullen J, Streicher SA, Kuo HC, Chen Y, Young D, et al. Race, tumor location, and disease progression among low-risk prostate cancer patients. Cancer Med. 2020;9:2235–42.
- 39.
Mahal BA, Berman RA, Taplin ME, Huang FW. Prostate cancer-specific mortality across Gleason scores in Black vs Nonblack men. JAMA. 2018;320:2479–81.
- 40.
Lawrentschuk N, Fleshner N. The role of magnetic resonance imaging in targeting prostate cancer in patients with previous negative biopsies and elevated prostate-specific antigen levels. BJU Int. 2009;103:730–3.
- 41.
Sundi D, Kryvenko ON, Carter HB, Ross AE, Epstein JI, Schaeffer EM. Pathological examination of radical prostatectomy specimens in men with very low risk disease at biopsy reveals distinct zonal distribution of cancer in black American men. J Urol. 2014;191:60–7.
- 42.
Jalloh M, Myers F, Cowan JE, Carroll PR, Cooperberg MR. Racial variation in prostate cancer upgrading and upstaging among men with low-risk clinical characteristics. Eur Urol. 2015;67:451–7.
- 43.
Leapman MS, Freedland SJ, Aronson WJ, Kane CJ, Terris MK, Walker K, et al. Pathological and biochemical outcomes among African-American and caucasian men with low risk prostate cancer in the SEARCH database: implications for active surveillance candidacy. J Urol. 2016;196:1408–14.
- 44.
Ching CB, Moussa AS, Li J, Lane BR, Zippe C, Jones JS. Does transrectal ultrasound probe configuration really matter? End fire versus side fire probe prostate cancer detection rates. J Urol. 2009;181:2077–82. Discussion 2082–3.
- 45.
Demura T, Hioka T, Furuno T, Kaneta T, Gotoda H, Muraoka S, et al. Differences in tumor core distribution between palpable and nonpalpable prostate tumors in patients diagnosed using extensive transperineal ultrasound-guided template prostate biopsy. Cancer. 2005;103:1826–32.
- 46.
Meyer AR, Mamawala M, Winoker JS, Landis P, Epstein JI, Macura KJ, et al. Transperineal prostate biopsy improves the detection of clinically significant prostate cancer among men on active surveillance. J Urol. 2021;205:1069–74.
- 47.
Xiang J, Yan H, Li J, Wang X, Chen H, Zheng X. Transperineal versus transrectal prostate biopsy in the diagnosis of prostate cancer: a systematic review and meta-analysis. World J Surg Oncol. 2019;17:31.
- 48.
Murphy AB, Abern MR, Liu L, Wang H, Hollowell CMP, Sharifi R, et al. Impact of a genomic test on treatment decision in a predominantly African American population with favorable-risk prostate cancer: a randomized trial. J Clin Oncol. 2021;39:1660–70.
- 49.
Sohn H. Racial and ethnic disparities in health insurance coverage: dynamics of gaining and losing coverage over the life-course. Popul Res Policy Rev. 2017;36:181–201.
- 50.
Butler S, Muralidhar V, Chavez J, Fullerton Z, Mahal A, Nezolosky M, et al. Active surveillance for low-risk prostate cancer in Black patients. N Engl J Med. 2019;380:2070–2.
- 51.
Eggener SE, Rumble RB, Armstrong AJ, Morgan TM, Crispino T, Cornford P, et al. Molecular biomarkers in localized prostate cancer: ASCO guideline. J Clin Oncol. 2020;38:1474–94.
- 52.
Mahal BA, Alshalalfa M, Kensler KH, Chowdhury-Paulino I, Kantoff P, Mucci LA, et al. Racial differences in genomic profiling of prostate cancer. N Engl J Med. 2020;383:1083–5.
- 53.
Cullen J, Rosner IL, Brand TC, Zhang N, Tsiatis AC, Moncur J, et al. A biopsy-based 17-gene genomic prostate score predicts recurrence after radical prostatectomy and adverse surgical pathology in a racially diverse population of men with clinically low- and intermediate-risk prostate cancer. Eur Urol. 2015;68:123–31.
- 54.
Spratt DE, Yousefi K, Deheshi S, Ross AE, Den RB, Schaeffer EM, et al. Individual patient-level meta-analysis of the performance of the decipher genomic classifier in high-risk men after prostatectomy to predict development of metastatic disease. J Clin Oncol. 2017;35:1991–8.
- 55.
Yamoah K, Johnson MH, Choeurng V, Faisal FA, Yousefi K, Haddad Z, et al. Novel biomarker signature that may predict aggressive disease in African American men with prostate cancer. J Clin Oncol. 2015;33:2789–96.
Acknowledgements
Thank you to Jonathan Bloom, for the post hoc analysis of internal data [16].
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Vigneswaran, H.T., Mittelstaedt, L., Crippa, A. et al. Progression on active surveillance for prostate cancer in Black men: a systematic review and meta-analysis. Prostate Cancer Prostatic Dis (2021). https://doi.org/10.1038/s41391-021-00425-1
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