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| Clinicopathological and oncological significance of persistent prostate-specific antigen after radical prostatectomy: A systematic review and meta-analysis |
Shulin Wua,b,Sharron X. Lina,Kristine M. Cornejob,Rory K. Crottyb,Michael L. Blutea,Douglas M. Dahla,Chin-Lee Wua,b,*( )
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a Department of Urology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA
b Department of Pathology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA |
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Abstract Objective To investigate the association of persistently elevated prostate-specific antigen (PSA) after radical prostatectomy (RP) with clinicopathological features and long-term oncological prognosis for the development of a potential management strategy.
Methods A systematic literature search was performed using PubMed and Web of Science up to June 2021 to identify the eligible studies focusing on understanding the impact of persistent PSA in patients who underwent RP for localized prostate cancer. Meta-analyses were performed on parameters with available information.
Results A total of 32 RP studies were identified, of which 11 included 26 719 patients with consecutive cohorts and the remaining 21 comprised 24 177 patients with cohorts carrying specific restrictions. Of the 11 studies with consecutive cohorts, the incidence of persistent PSA varied between 3.1% and 34.6% with a median of 11.0%. Meta-analyses revealed patients with persistent PSA consistently showed unfavorable clinicopathological features and a more than 3.5-fold risk of poorer biochemical recurrence, metastasis, and prostate cancer-specific mortality prognosis independently, when compared to patients with undetectable PSA. Similarly, cases with persistent PSA in different specific patient cohorts with a higher risk of prostate cancer also showed a trend of worse outcomes.
Conclusion We found that the frequency of persistent PSA was about 11.0% in consecutive RP cohorts. Persistent PSA was significantly associated with unfavorable clinicopathological characteristics and worse oncological outcomes. Patients with persistent PSA after RP may benefit from early salvage treatment to delay or prevent biochemical recurrence, improving oncological outcomes for these patients. Further prospective randomized controlled trials are warranted to understand optimal systemic therapy in these patients.
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Received: 05 August 2021
Available online:
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Corresponding Authors:
Chin-Lee Wu
E-mail: cwu2@mgh.harvard.edu
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| Reference | Year | Group | Period | Total/persistent (n) | RP cohort | Persist cutoff (ng/mL) | Persistent rate (%) | BCR (ng/mL) | F/U (M) | NOS | Clinical significance of persistent PSA after RP | | Micoogullari et al. [8] | 2021 | Turkey | 2009-2017 | 875/97 | Consecutive | ≥0.1 at 6-8 weeks | 11.1 | Two consecutive PSA≥0.2 | 18-24 | 9 | -0.1-0.2 ng/mL associated with aggressive disease and BCR in UVa | | Milonas et al. [9] | 2021 | Lithuania | 2001-2019 | 1225/246 | Consecutive | ≥0.1 at 4-8 weeks | 20.1 | Two consecutive PSA>0.2 | 103 | 7 | -Worse outcomes in high risk, worse BCR in intermedium in MVa | | Preisser et al. [10] | 2019 | Germany | 1992-2016 | 11 604/1025 | Consecutive | ≥0.1 at 6 weeks | 8.8 | Two consecutive PSA≥0.2 | 62 | 9 | -Worse prognosis of Mets, OS, PCSM in MVa | | Spratt et al. [11] | 2018 | USA | 1990-2015 | 477/150 | Consecutive | ≥0.1 at 8 weeks | 31.4 | NA | 77 | 8 | -Worse prognosis of Mets in MVa | | García-Barreras et al. [12] | 2018 | France | 2000-2016 | 2500/229 | Consecutive | ≥0.1 at 6 weeks | 9.2 | PSA≥0.2 | 58 | 6 | -Associated with aggressive disease | | Kumar et al. [13] | 2017 | USA | 2008-2013 | 5300/162 | Consecutive | ≥0.1 at 6 weeks | 3.1 | PSA≥0.2 | 38 | 7 | -Associated with aggressive disease and BCR in UVa | | Audenet et al. [14] | 2012 | France | 1996-2006 | 240/83 | Consecutive | ≥0.1 at 6 weeks | 34.6 | PSA>0.2 | 44 | 8 | -Worse prognosis of BCR in MVa | | Eisenberg et al. [35] | 2010 | USA | 1996-2006 | 525/69 | Consecutive | >0.05 at 4-12 weeks | 13.1 | Two consecutive PSA≥0.2 | 56 | 8 | -Worse 5-year BCR prognosis in MVa | | Moreira et al. [36] | 2010 | USA | 2001-2008 | 901/230 | Consecutive | ≥0.03 at 4-24 weeks | 25.5 | PSA>0.2 | ≥6 | 8 | -≥0.03 ng/mL showed aggressive features and BCR outcome in MVa | | Naselli et al. [15] | 2009 | Italy | 2002-2007 | 318/33 | Consecutive | ≥0.1 at 6 weeks | 10.3 | PSA>0.4 | 5 | 8 | -Associated with aggressive disease, worse BCR outcome in MVa | | Sengupta et al. [16] | 2006 | USA | 1990-1999 | 2754/303 | Consecutive | >0.1/0.15 at 8-16 weeks | 11.0 | NA | 102 | 7 | -Worse prognosis of Mets and PCSM in MVa | | Sood et al. [37] | 2020 | USA | NA | NA/760 | RTOG9601 | >0.4 | NA | PSA 0.2-4.0 | 144 | 6 | -Worse local recurrence, Mets, and OS than BCR patients in UVa | | Venclovas et al. [17] | 2019 | Lithuania | 2001-2017 | 433/130 | High-risk PCa | ≥0.1 at 6-8 weeks | 30.0 | Two consecutive PSA≥0.2 | 64 | 8 | -Predict Mets and PCSM in UVa but not in MV; early BCR | | Roy et al. [38] | 2019 | Canada | 2005-2014 | 167/52 | pN1 | ≥0.2 at 4-8 weeks | 31.1 | >0.2 | 48 | 6 | -Worse prognosis of Mets in MVa, not in OS | | Kim et al. [18] | 2019 | Korea | 2002-2014 | 96/52 | pN1 | ≥0.1 at 6 weeks | 54.2 | Two consecutive PSA>0.2 | 45 | 7 | -Worse prognosis of Mets in MVa | | Bartkowiak et al. [19] | 2019 | Germany | 1997-2002 | 555/133 | pN0, SRT | ≥0.1 | 24.0 | Two consecutive PSA≥0.2 | 73 | 7 | -Worse PFS prognosis in UVa but not in MV by pre-SRT PSA | | Xiang et al. [20] | 2018 | China | 2009-2014 | 198/104 | Persistent | ≥0.1 and < 0.2 at 6-8 weeks | NA | Two consecutive PSA≥0.2 | 53 | 6 | -RT and ADT control BCR progress well in MVa | | Schmidt-Hegemann et al. [39] | 2018 | Germany | 2014-2017 | 129/67 | PSMA PET/CT RT | Undefined | 52.0 | PSA>0.2 | 20 | 6 | -With high-risk PCa and shorter time interval to BCR before Tx | | McDonald et al. [40] | 2018 | USA | 1982-2015 | 124/44 | pN1 | ≥0.2 | 35.5 | PSA≥0.2 | 98 | 7 | -Associated with Mets in MVa | | Fossati et al. [21] | 2018 | Italy | 1996-2009 | 925/324 | SRT | ≥0.1 at 4 weeks | 35.0 | PSA≥0.1 | 96 | 7 | -Worse Mets prognosis treated with SRT in MVa | | Gandaglia et al. [22] | 2017 | Italy | 1994-2014 | 982/496 | Persistent | ≥0.1 at 6-8 weeks | NA | NA | 110 | 6 | -Worse PCSM prognosis in UVa, RT benefit | | Bianchi et al. [23] | 2016 | Italy | 1998-2013 | 391/83 | pN1 | ≥0.1 at 6 weeks | 26.0 | PSA≥0.2 | 53 | 7 | -Worse Mets and PCSM prognosis in MVa | | Ploussard et al. [24] | 2013 | France | 1998-2011 | 9735/496 | Persistent | ≥0.1 at 6 weeks | NA | NA | 27 | 6 | -Worse BCR prognosis and worse salvage Tx outcome in MVa | | Lohm et al. [25] | 2013 | Germany | 1997-2004 | 159/72 | BCR, SRT | ≥0.1 | 45.3 | PSA≥0.1 | 42 | 7 | -Similar BCR prognosis as undetectable, SRT benefit | | Rogers et al. [26] | 2004 | USA | 1989-2002 | 2680/160 | Persistent | ≥0.1 at 12 weeks | NA | NA | ≥12 | 6 | -PSA change ≥0.05 ng/mL showed worse Mets prognosis in UVa | | Song et al. [27] | 2002 | USA | 1989-1999 | NA/73 | SRT | ≥0.1 | NA | NA | 36 | 6 | -Worse disease PFS after RT in UVa | | Catton et al. [41] | 2001 | Canada | 1987-1994 | 113/21 | ART, SRT | ≥0.2 | 18.6 | NA | 44 | 6 | -Worse BCR prognosis than undetectable in UVa | | Garg et al. [42] | 1998 | USA | 1991-1997 | 78/37 | SRT | ≥0.05 | 47.4 | NA | 27 | 7 | -Similar 3 years disease-free survival as undetectable | | Coetzee et al. [43] | 1996 | USA | NA | 45/15 | PSM, ART | ≥0.5 | 33.3 | NA | 33 | 6 | -80% disease progress, may with micro Mets or local disease | | Wu et al. [28] | 1995 | USA | 1987-1993 | 53/38 | RT | Decreased from 0.3 to 0.1 | 82.6 | NA | 15 | 7 | -Predict less undetectable PSA after RT in UVa but not in MV | | Link et al. [44] | 1991 | USA | 1984-1988 | 25/12 | ART | Undefined | 48.0 | NA | 33 | 6 | -Less durable response after RT | | Hudson and Catalona [30] | 1990 | USA | 1983-1988 | 80/21 | RT | >0.6 | 26.3 | NA | 13 | 6 | -At risk of further progression |
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Main characteristics of the included radical prostatectomy studies.
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| Variable | Study (n) | I2 (%) | Heterogeneity (p-value) | OR | 95% CI | p-Value | Effects model | Reference | | D'amico risk (H vs. M+L) | 5 | 90 | <0.001 | 3.11 | 1.78-5.45 | <0.001 | Random | [9,[11], [12], [13],35] | | GS (≥8 vs. <8) | 7 | 92 | <0.001 | 3.55 | 2.04-6.74 | <0.001 | Random | [8,[10], [11], [12], [13], [14],16] | | pT stage (≥T3 vs. T2) | 8 | 93 | <0.001 | 3.51 | 2.28-5.41 | <0.001 | Random | [8,[10], [11], [12], [13], [14], [15], [16]] | | EPE (+ vs. -) | 5 | 83 | <0.001 | 2.73 | 1.82-4.09 | <0.001 | Random | [8,[11], [12], [13],36] | | SVI (+ vs. -) | 4 | 64 | 0.04 | 4.49 | 3.10-6.51 | <0.001 | Random | [8,11,16,36] | | Margin (PSM vs. NSM) | 10 | 84 | <0.001 | 2.99 | 2.28-3.92 | <0.001 | Random | [8,[10], [11], [12], [13], [14], [15], [16],35,36] | | LNI (+ vs. -) | 8 | 89 | <0.001 | 4.83 | 2.39-9.76 | <0.001 | Random | [8,[10], [11], [12], [13],15,16,36] | | SRT (with vs. without) | 3 | 85 | 0.001 | 14.9 | 7.58-25.22 | <0.001 | Random | [8,10,11] |
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Meta-analyses of clinicopathological features by PSA status after radical prostatectomy in consecutive patient cohorts.
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| Reference | Log-rank test (K-M analysis), p-value | Univariate HR (95% CI), p-value | Multivariate HR (95% CI), p-value | Covariate | | Micoogullari et al. [8] | | BCR | p<0.001 (persistent worse) | NA | NA | NA | | Preisser et al. [10] | | Mets | p<0.001 (persistent worse) | NA | 3.59 (2.83-4.57), p<0.001 | Year/age/pT/GG/pN1 | | Cancer-specific death | p<0.001 (persistent worse) | NA | 3.15 (1.92-5.18), p<0.001 | Year/pT/GG/PSM | | All-cause death | p<0.001 (persistent worse) | NA | 1.86 (1.41-2.45), p<0.001 | Age/pT/GG/PSM/CCI | | Spratt et al. [11] | | Mets | NA | 2.36 (0.89-6.72), p=0.08 | 4.26 (1.16-21.8), p=0.03 | Decipher risk/pN1 | | Kumar et al. [13] | | BCR | p<0.01 (persistent worse) | NA | NA | NA | | Audenet et al. [14] | | BCR | p<0.001 (persistent worse) | NA | NA | NA | | Eisenberg et al. [35] | | BCR | p<0.01 (persistent worse) | NA | NA | NA | | Naselli et al. [15] | | BCR | p<0.001 (persistent worse) | NA | 4.54 (2.35-8.78), p<0.001 | pT/pN | | Moreira et al. [36] | | BCR | p<0.001 (persistent worse) | 3.88 (2.13-7.06), p<0.001 | 3.23 (1.62-6.48), p=0.001 | BMI/GS/PSM | | Sengupta et al. [16] | | Mets | p<0.001 (persistent worse) | NA | 3.58 (2.37-5.41), p<0.001 | PSA (log2)/GS/SVI/PSM | | Cancer-specific death | p<0.001 (persistent worse) | NA | 4.26 (2.27-7.99), p<0.001 | PSA (log2)/GS/SVI/PSM |
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Summary of oncological prognostic information in the included radical prostatectomy studies with consecutive cohorts.
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Forest plots of multivariate analysis on BCR, metastasis, and PCSM prognosis from patients with or without persistent PSA. (A) BCR; (B) Metastasis; (C) PCSM. The horizontal lines correspond to the study-specific hazard ratio and 95% CI, respectively. The area of the squares reflects the study-specific weight. The diamond represents the pooled results of hazard ratio and 95% CI. BCR, biochemical recurrence; PCSM, prostate cancer specific mortality; PSA, prostate-specific antigen; CI, confidence interval; SE, standard error; IV, weighted mean difference.
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