Association of Negative Followup Biopsy and Reclassification during Active Surveillance of Prostate Cancer: A Systematic Review and Meta-Analysis
2021; Lippincott Williams & Wilkins; Volume: 205; Issue: 6 Linguagem: Inglês
10.1097/ju.0000000000001701
ISSN1527-3792
AutoresPaweł Rajwa, Benjamin Pradère, Keiichiro Mori, Guillaume Ploussard, Michael Leapman, Shahrokh F. Shariat,
Tópico(s)Statistical Methods in Clinical Trials
ResumoYou have accessJournal of UrologyReview Article1 Jun 2021Association of Negative Followup Biopsy and Reclassification during Active Surveillance of Prostate Cancer: A Systematic Review and Meta-Analysis Pawel Rajwa, Benjamin Pradere, Keiichiro Mori, Guillaume Ploussard, Michael S. Leapman, and Shahrokh F. Shariat Pawel RajwaPawel Rajwa http://orcid.org/0000-0003-4073-6584 Department of Urology, Medical University of Vienna, Vienna, Austria Department of Urology, Medical University of Silesia, Zabrze, Poland More articles by this author , Benjamin PradereBenjamin Pradere Department of Urology, Medical University of Vienna, Vienna, Austria More articles by this author , Keiichiro MoriKeiichiro Mori Department of Urology, Medical University of Vienna, Vienna, Austria Department of Urology, The Jikei University School of Medicine, Tokyo, Japan More articles by this author , Guillaume PloussardGuillaume Ploussard Department of Urology, La Croix du Sud Hospital, Quint Fonsegrives, France More articles by this author , Michael S. LeapmanMichael S. Leapman Department of Urology, Yale School of Medicine, New Haven, Connecticut More articles by this author , and Shahrokh F. ShariatShahrokh F. Shariat *Correspondence: Department of Urology, Comprehensive Cancer Center, Medical University Vienna, Vienna General Hospital, Währinger Gürtel 18-20, A-1090Vienna, Austria telephone: 43 1 4040026150; FAX: 43 1 40400 23320; E-mail Address: [email protected] Department of Urology, Medical University of Vienna, Vienna, Austria Department of Urology, Weill Cornell Medical College, New York, New York Department of Urology, University of Texas Southwestern, Dallas, Texas Karl Landsteiner Institute of Urology and Andrology, Vienna, Austria Department of Urology, Second Faculty of Medicine, Charles University, Prague, Czech Republic Institute for Urology and Reproductive Health, I.M. Sechenov First Moscow State Medical University, Moscow, Russia More articles by this author View All Author Informationhttps://doi.org/10.1097/JU.0000000000001701AboutAbstractPDF ToolsAdd to favoritesDownload CitationsTrack CitationsPermissionsReprints ShareFacebookTwitterLinked InEmail Abstract Purpose: With the growing adoption of active surveillance clinical parameters that can tailor the intensity of monitoring are increasingly needed. Therefore, we aimed to evaluate the prognostic value of negative followup biopsy for reclassification and upgrading in prostate cancer patients managed with active surveillance. Materials and Methods: The PubMed®, Web of ScienceTM, and Scopus® databases were queried to identify relevant studies published until November 2020 according to the Preferred Reporting Items for Systematic Review and Meta-analysis statement. We performed a formal meta-analysis for the reclassification and upgrading in the full cohort and selected subgroups. Results: We identified 13 and 9 studies eligible for the systematic review and meta-analysis, respectively. A total of 2,628 patients were included in the meta-analysis. Any negative followup biopsy was associated with significantly lower risk of reclassification (HR 0.46, 95% CI 0.39–0.55; p <0.01), and upgrading (HR 0.54, 95% CI 0.44–0.66; p <0.01). For the confirmatory biopsy subgroup, the results remained significant for reclassification (HR 0.44, 95% CI 0.36–0.55; p <0.01) and upgrading (HR 0.55, 95% CI 0.42–0.73; p <0.01). These patterns remained robust among patients with only Gleason Grade prognostic group 1 (reclassification HR 0.47, 95% CI 0.39–0.57; p <0.01; upgrading HR 0.54, 95% CI 0.42–0.69; p <0.01). Conclusions: A negative followup biopsy is associated with an approximately 50% decrease in the risk of future reclassification and upgrading. Incorporation of the negative followup biopsy into current protocols should allow for personalized active surveillance tailoring and more precise decision making. Abbreviations and Acronyms AS active surveillance GG Gleason Grade MRI magnetic resonance imaging PCa prostate cancer PSA prostate specific antigen TRUS transrectal ultrasound The feasibility of active surveillance is supported by a large and expanding body of evidence among patients with low and favorable intermediate risk prostate cancer.1–3 By definition, surveillance involves monitoring of cancer characteristics with the opportunity to provide curative local therapy should it be warranted on the basis of PCa reclassification.1–3 To date, PCa monitoring during AS is based on repetitive prostate specific antigen testing, digital rectal examination, and prostate biopsy every 1 to 5 years, and implementation of novel adjunctive tools such as magnetic resonance imaging and genomic testing.1,2 Despite recent attempts of major urological guidelines to develop clear recommendations on followup strategies and reclassification definitions, there are still no standardized criteria.1,2,4 Several prediction models have been recently developed that aim at tailoring active surveillance.1,2,5–8 This is particularly important given the widespread adoption of AS and the fact that more than 50% of initially enrolled AS patients may avoid transitioning to curative treatment.9,10 Subsequently, some men with stable PCa profiles possibly undergo excessive invasive prostate biopsies.11,12 Analyses from prospective AS cohorts reveal that between 30% and 50% of patients will experience at least 1 biopsy that is negative for cancer.13–15 Low volume disease or sampling errors are some of the explanations for negative biopsies during followup.16 The consequence is a lack of confidence and further questions associated with prognosis and future monitoring of the disease. Only a few studies have analyzed the prognostic value of negative biopsies for reclassification during AS.5,13 In general, negative followup biopsy appears as a prognostic factor of future PCa progression and active treatment. Nevertheless, due to the heterogeneity of AS eligibility criteria and reclassification definitions, the data are sparse and inconclusive. Hence, a 5-organization consensus-based DETECTIVE study indicated that the role of a negative confirmatory (first followup) biopsy in active surveillance should be further elucidated.4 In this context, we undertook a systematic review and meta-analysis of available studies, which analyzed the prognostic value of negative surveillance biopsy in PCa patients on AS. Our goal was to assess the prognostic value of negative followup biopsies on the risk of reclassification, with a special focus on initial confirmatory biopsy. Materials and Methods The protocol has been registered in the International Prospective Register of Systematic Reviews database (registration number: CRD 42020220976). Search Strategy This systematic review and meta-analysis were performed according to the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) statement.17,18 A completed PRISMA 2009 checklist is shown in supplementary Appendix 1 (https://www.jurology.com). PubMed®, Web of ScienceTM, and Scopus® databases were searched systematically in November 2020 to identify studies analyzing the prognostic value of negative surveillance biopsy for reclassification in patients on AS. The terms used in our search strategy were as follows: PubMed: (prostate cancer) AND (active surveillance) AND (negative biopsy); Scopus: (prostate AND cancer AND active AND surveillance AND negative AND biopsy); and Web of Science: (prostate AND cancer) AND (active AND surveillance) AND (negative AND biopsy). Two investigators (P.R., K.M.) independently reviewed the search results and initially excluded ineligible studies based on the titles and abstracts. Full texts were retrieved and reviewed for eligibility. Inclusion and Exclusion Criteria Studies were included if they fulfilled the predefined PICOS (patient, intervention, comparator, outcome, study type) approach. Therefore we included reports, which analyzed whether patients with prostate cancer on AS (population), who underwent surveillance biopsy with negative results (intervention), comparing to patients with positive surveillance biopsy results (comparator) have a different prognosis for reclassification at followup biopsies (outcome), in prospective and retrospective studies (study design). We included studies that analyzed patients who underwent at least 1 followup biopsy after a negative biopsy. As there is no universal definition of reclassification in active surveillance and major active surveillance cohorts use different criteria, we defined reclassification if there was a Gleason Grade upgrading and/or volume progression and/or clinical progression.1,2 Studies were deemed ineligible if the prognostic value of negative followup was not analyzed in multivariable models. We included studies evaluating the cohorts from the same ongoing prospective studies or institutions with partly overlapping recruitment periods if the study populations were different. We excluded meta-analyses, reviews, letters, meeting abstracts, author replies, case reports and articles not written in English. The included studies’ bibliography was scanned for additional studies of interest. Data Extraction Two authors (P.R., K.M.) independently retrieved data on authors, publication year, recruitment country, study period, number of patients, followup duration, Gleason Grade Groups of analyzed cohorts, reclassification definition and oncological outcome (reclassification). The hazard ratios and 95% confidence intervals of negative biopsy from multivariable models for reclassification were extracted. In the case of multiple models, we extracted data from analyses with the longest followup (more followup biopsies). Also, when data were provided for more than 1 negative biopsy, to increase homogeneity we retrieved HRs from multivariable models which included single negative biopsy. In the meta-analysis we excluded studies, which provided only odds ratios for reclassification. Disagreements were resolved by consultation with coauthors. Quality and Risk of Bias Assessment The risk of bias evaluation of each study was assessed according to RoBANS (supplementary Appendix 2, https://www.jurology.com). The Newcastle–Ottawa Scale (NOS) was adopted to analyze the quality of the nonrandomized studies, which is in line with the Cochrane Handbook for Systematic Reviews of Interventions (see table).19,20 The scale rates 3 factors—selection, comparability and exposure—with total scores ranging from 0 (lowest) to 9 (highest). The main confounders were identified as the important prognostic factors of oncological outcomes. The presence of confounders was determined by consensus and review of the literature. We defined studies with scores greater than 6 as “high-quality” studies. Table. Basic characteristics of included studies Reference Year Country Patients Enrollment No. Pts Median Mos Followup Meta-Analysis Eligble GG ≥2 Included % GG ≥2 Included MRI Biopsy Included Confirmatory Biopsy Time Interval to Confirmatory Biopsy GG1 Sub-Group Reclassification Definition Upgrading Sub-Group Newcastle-Ottawa Scale Singh24 2020 UK 2004–2018 222 62 Yes Yes 15.87 Yes Yes No data Yes Upgrading, vol, clinical Yes 7 Bloom15 2020 USA 2007–2017 182 43.6 Yes Yes 14.02 Yes† Yes Neg biopsy mean 12.2 mos; pos biopsy mean 16.4 mos No Upgrading Yes 8 Cooperberg5 2020 USA 2003–2017 850 49.2 Yes No 0.00 Yes No Not applicable Yes Upgrading Yes 8 Kearns13 2018 USA 2008–2016 313 34.8 Yes Yes 6.00 Yes Yes Median 12 mos Yes Upgrading, vol Yes 8 Ganesan25 2017 USA 2002–2015 224 55.8 Yes Yes 8.04 No Yes Neg biopsy median 13.3 mos; pos biopsy median 12.7 mos Yes Upgrading Yes 7 Wong14 2014 Canada 1995–2012 286 41 Yes No 0.00 No Yes No data Yes Upgrading, vol Yes 8 Adamy26 2011 USA 1997–2009 233 21.6 Yes No 0.00 No Yes Median 4.7 mos Yes Upgrading, vol, clinical No 7 Tseng27 2010 USA 1995–2006 226 27.6 Yes No 0.00 No Yes Median 8.4 mos Yes Upgrading, vol No 7 Otaibi28 2009 Canada 1987–2006 92 76 Yes Yes 22.83 No Yes Annually No Upgrading, vol, clinical No 7 Liss29 2020 USA 2010–2019 395 49.2 No No 0.00 Yes No Not applicable Yes Upgrading Yes 7 Lin30 2017 USA 2015‡ 558 ND No Yes 18.80 Yes No Not applicable No Upgrading Yes 7 Ankerst6 2015 USA 2008–2013 458 35.8 No No 0.00 No No Not applicable Yes Upgrading, vol No 8 Cary31 2014 USA 1996–2011 131 51 No Yes 6.67 No Yes Median 12 mos No Upgrading, vol No 8 Range of scores is 0 (lowest) to 9 (highest). †All patients underwent MRI-TRUS fusion biopsy. ‡Retrospective data, prospective study. Statistical Analyses Forest plots were used to assess multivariable HRs and to obtain summary HRs to describe the relationships between negative surveillance biopsy and reclassification. Studies were considered in the meta-analysis only if they used a multivariable Cox proportional hazards regression model. In studies with only HRs and p values, we calculated the corresponding 95% CI.21 We also performed a subgroup analysis of studies, which analyzed the prognostic value of only confirmatory biopsies, included only GG1 patients, the risk of upgrading, and compared patients with negative vs positive followup biopsy without reclassification. Heterogeneity among the outcomes of included studies in this meta-analysis was evaluated using the Cochrane Q-test and the I2 statistic. Significant heterogeneity was indicated by p <0.05 in the Cochrane Q-tests and I2 greater than 50%. Random effects models were used for the initial calculation of the Cochrane Q-test and the I2 statistic. We used fixed-effects models to calculate pooled HRs for nonheterogeneous results.22,23 Publication bias was assessed with funnel plots. All analyses were conducted using Cochrane Collaboration Review Manager software (RevMan v.5.4; Cochrane Collaboration, Oxford, UK) and statistical significance was set at p <0.05. Results Study Selection and Characteristics The PRISMA flowchart is depicted in figure 1. A total of 1,064 initial searches were identified. After duplicate removal, title and abstract screening, and full-text review, we included 13 studies with 4,170 patients for the systematic review and 9 studies with 2,628 patients for qualitative meta-analysis.5,6,13–15,24–31 Overall, all studies were considered as “high-quality” according to NOS. The major characteristics of the included studies are presented in the table. Most of the studies were retrospective, however, based on prospectively maintained databases. The median followup varied from 21.6 to 76 months. In total, 9 studies investigated the association between negative confirmatory biopsy and reclassification, whereas 4 evaluated the prognostic value of any negative biopsy after PCa diagnosis. One study included patients who underwent solely confirmatory multiparametric MRI-TRUS fusion biopsy.15 In all articles, GG upgrading was the common component of reclassification criteria, with 8 studies including also volume (eg number of cores and percentage of core involvement), and 3 clinical (eg clinical stage, PSA, MRI results) criteria to the definition. In total 7 studies included men with both GG1 and GG2, and 8 analyzed the association between negative biopsy and GG upgrading. Figure 1. Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) flow diagram Meta-Analysis Association of negative followup biopsy and reclassification A total of 9 studies provided data (HRs in multivariable analyses) on the association between negative followup biopsy and reclassification. The forest plot (fig. 2) shows that negative followup biopsy was significantly associated with the risk of reclassification (HR 0.46, 95% CI 0.39–0.55; p <0.001). Cochran Q test (p=0.74) and I2 test (0%) did not reveal significant heterogeneity. The funnel plot did not identify any study over the pseudo-95% CI (supplementary figure, part A, https://www.jurology.com). Figure 2. Forest plot shows association of negative followup biopsy and reclassification Association between negative confirmatory biopsy and reclassification We further analyzed 8 studies, which evaluated the association between confirmatory biopsy and reclassification, to determine prognostic value. After pooling the results, a negative confirmatory biopsy was a significant predictor of reclassification (HR 0.44, 95% CI 0.36–0.55; p <0.001; fig. 3). Cochrane's Q test (p=0.72) and I2 test (0%) did not reveal significant heterogeneity. The funnel plot did not identify any study over the pseudo-95% CI (supplementary figure, part B, https://www.jurology.com). Figure 3. Forest plot shows association of negative confirmatory biopsy and reclassification Association between negative followup biopsy and reclassification in GG1 patients Seven studies provided data regarding the association between negative followup biopsy and reclassification in the subset of patients with GG1 disease. The forest plot (fig. 4) revealed that GG1 patients with negative surveillance biopsy had a lower risk of reclassification (HR 0.47, 95% CI 0.39–0.57; p <0.001). Cochrane's Q test (p=0.56) and I2 test (0%) did not reveal significant heterogeneity. The funnel plot did not identify any study over the pseudo-95% CI (supplementary figure, part C, https://www.jurology.com). Figure 4. Forest plot shows association of negative followup biopsy and reclassification in Gleason Grade 1 subgroup Association of negative followup biopsy and upgrading Analysis of pooled data from 6 studies revealed a significant prognostic value of negative followup biopsy on the risk of upgrading (HR 0.54, 95% CI 0.44–0.66; p <0.001; fig. 5). Cochrane's Q test (p=0.79) and I2 test (0%) did not reveal significant heterogeneity. The funnel plot did not identify any study over the pseudo-95% CI (supplementary figure, part D, https://www.jurology.com). Figure 5. Forest plot shows association of negative followup biopsy and upgrading Association of negative confirmatory biopsy and upgrading Five studies provided data on the association between negative confirmatory biopsy and upgrading (fig. 6). The pooled results revealed a similar, significant prognostic value of negative confirmatory biopsy for upgrading (HR 0.55, 95% CI 0.42–0.73; p <0.001). Cochrane's Q test (p=0.67) and I2 test (0%) did not reveal significant heterogeneity. The funnel plot did not identify any study over the pseudo-95% CI (supplementary figure, part E, https://www.jurology.com). Figure 6. Forest plot shows association of negative confirmatory biopsy and upgrading Association of negative followup biopsy and upgrading in GG1 patients Four studies provided data on the association between negative followup biopsy and upgrading among GG 1 patients (fig. 7). Forest plot revealed that GG1 patients with negative followup biopsy were at lower risk of upgrading (HR 0.54, 95% CI 0.42–0.69; p <0.001). Cochrane's Q test (p=0.65) and I2 test (0%) did not reveal significant heterogeneity. Figure 7. Forest plot shows association of negative followup biopsy and upgrading in Gleason Grade 1 subgroup Association of negative confirmatory biopsy vs positive confirmatory biopsy without reclassification for future reclassification and upgrading Five studies specifically analyzed the prognosis of patients with negative confirmatory biopsy and positive biopsy without reclassification for future reclassification. Forest plot (fig. 8) revealed negative biopsy patients were at a decreased risk of reclassification (HR 0.42, 95% CI 0.33–0.54; p <0.001). Three studies undertook a similar analysis for upgrading with results following the same pattern (HR 0.62, 95% CI 0.44–0.87; p=0.005; fig. 9). Cochrane's Q tests (p=0.51 and p=0.66, respectively) and I2 tests (0% both) did not reveal significant heterogeneity. The funnel plot for reclassification did not identify any study over the pseudo-95% CI (supplementary figure, part F, https://www.jurology.com). Figure 8. Forest plot shows association of negative confirmatory biopsy vs positive confirmatory biopsy without reclassification for reclassification. Figure 9. Forest plot shows association of negative confirmatory biopsy vs positive confirmatory biopsy without reclassification for upgrading. Sensitivity analysis Sensitivity analyses for reclassification and upgrading were performed based on the quality of the studies, length of followup, and any MRI biopsy inclusion. We did not observe a significant influence of quality of studies, length of followup, or inclusion of studies with any MRI biopsies on overall HRs. Also, the use of random effects instead of the fixed effects model did not change the results. These findings confirm the robustness and reliability of our results. Discussion In our systematic review and meta-analysis, we comprehensively assessed the association between negative followup biopsy and the risk of future reclassification among patients with prostate cancer on active surveillance. We believe this is the first meta-analysis on this topic with further subanalyses to strengthen and specify our results. First, a negative followup biopsy was associated with half the risk of future pathologically or clinically driven reclassification, which was also seen in the negative confirmatory biopsy subgroup. Second, patients with negative followup biopsies were at least 38% less likely to experience upgrading, a pivotal factor for triggering reclassification and subsequent treatment.1,4,32 Third, these patterns remained robust among patients with only GG1 PCa. Fourth, positive biopsies for cancer without reclassification were associated with twice the future risk of reclassification. These findings can complement a growing interest in tailoring the intensity of surveillance protocols. At present, there is no consensus on how to safely monitor PCa during AS, and existing guidelines are mostly based on local protocols and expert opinions1,2,33 We do, however, virtually continue to rely on PSA, digital rectal examination, repetitive biopsies, and novel tools that lack sufficient prognostic accuracy on oncological outcomes. As revealed in the PROTECT trial clinically driven only (PSA) monitoring is still associated with a higher risk of metastasis and may be insufficient.34 Despite its inaccuracy (up to 50%) prostate biopsy remains the most reliable source of information on PCa cellular dedifferentiation, which may also increase over time.35–37 Our results suggest that negative followup biopsy (including confirmatory biopsy) can serve as one prognostic measure to inform clinical management during AS and that patients with negative followup biopsies may undergo less intensive followup without missing disease progression. This prognostic value of a negative followup biopsy may be explained by low volume lesions, which suggest limited progression in more stable (indolent) profiles.16,38 In well-established AS cohorts, only 9% to 25% of the patients were reclassified per biopsy round—fewer over time; this pattern suggests that most patients underwent unnecessary biopsies.37,39 For disease reclassification, a few models achieve 60% to 70% accuracy, and even fewer incorporate the history of negative biopsies.5,6,29,40 Our pooled results suggest an approximately 50% lower risk of reclassification in all subgroups, including GG1 subcohort and the confirmatory biopsy. These results would help to propose earlier personalized followup tailoring. The risk stratification in AS is particularly important, as patients with stable, low reclassification risk may undergo multiple, excessive biopsies, which puts them at risk of considerable morbidity (approximately 5%) and reduces quality-adjusted life years.41,42 Furthermore, a tailored AS would allow for cost savings compared to other modalities.43 Given the present evidence, upgrading is the most relevant comparator and should be the pivotal factor for triggering reclassification and subsequent treatment.1,4,32 In our study, previous negative followup biopsy was associated with a significantly lower risk of future upgrading in all analyzed subgroups. Through the exclusion of confounding factors of reclassifications such as volume or clinical progression, we unified and strengthened our findings. Similarly, to limit the possible influence of the various proportion of GG2 patients in included studies, we performed a subanalysis of GG1 only patients, with similar results. This is noteworthy as patients with initial GG2 tend to harbor more aggressive disease, and currently the feasibility of AS in this subgroup is still being studied and mostly regarded rather as deferred treatment with little evidence on treatment avoidance.1,2 Of note, most of the studies did not include or included only some proportion of patients who underwent MRI-TRUS fusion biopsy. The utility of fusion biopsies in AS was recently confirmed in the ASIST trial, which provided evidence on a lower risk of reclassification at 2 years after confirmatory fusion biopsy but little benefit at the time of confirmatory biopsy.44 In our review, 1 study that did examine negative fusion biopsies showed that negative confirmatory biopsy is associated with an almost 60% decreased risk of future reclassification.15 However, after fusion biopsy the risk of future reclassification still exists.15,29,44,45 This is partly in contrast to recent European Association of Urology and National Institute for Health and Care Excellence (NICE) guidelines, but not U.S. guidelines, which allow omitting followup prostate biopsy in a case of stable clinical profiles and diagnostic fusion biopsy.1,2,33 Nevertheless, the role of MRI and fusion biopsies in AS deserves further study, but considering the present state of knowledge, the negative fusion biopsy could be an even more robust prognosticator than systematic biopsy only.1,2,29,44 Our study has several limitations. First, most studies were retrospective. Second, patients were monitored according to different local protocols, and the length of followups varied. Third, only a few studies included novel risk stratification tools such as MRI and genomics, and it was not possible to extract detailed data because of the lack of these specifics in the patient characteristics and protocols. Fourth, based on the available data, running a proper meta-analysis of the association between eg 2 consecutive negative biopsies and reclassification was not possible. Finally, we restricted our meta-analysis to studies which used Cox proportional hazards regression models, and therefore did not include in the analyses logistic regression models studies. Even though this approach led to higher homogeneity of our included studies, this may make the current meta-analysis less representative. Conclusions This systematic review and meta-analysis provides high evidence of the prognostic value of negative followup biopsy in AS. Patients with a negative followup biopsy are at 50% lower risk of future reclassification and upgrading. Incorporation of the negative followup biopsy and especially negative confirmatory biopsy into current protocols could allow for personalized AS de-intensification and more precise decision making in these cases. Further studies analyzing the role of negative MRI-TRUS fusion biopsies in AS are warranted. References 1. National Compehensive Cancer Network: Prostate Cancer (Version 3. 2020), Plymouth Meeting, Pennsylvania: National Compehensive Cancer Network 2020. Google Scholar 2. : EAU-EANM-ESTRO-ESUR-SIOG Guidelines on Prostate Cancer—2020 Update. Part 1: Screening, Diagnosis, and Local Treatment with Curative Intent. Eur Urol 2020; 79: 243. Google Scholar 3. : Active surveillance for low-risk prostate cancer-an evolving international standard of care. JAMA Oncol 2017; 3: 1398. Google Scholar 4. : EAU-EANM-ESTRO-ESUR-SIOG prostate cancer guideline panel consensus statements for deferred treatment with curative intent for localised prostate cancer from an international collaborative study (DETECTIVE study). Eur Urol 2019; 76: 790. Google Scholar 5. : Tailoring intensity of active surveillance for low-risk prostate cancer based on individualized prediction of risk stability. JAMA Oncol 2020; 6: e203187. Google Scholar 6. : Precision medicine in active surveillance for prostate cancer: development of the canary-early detection research network active surveillance biopsy risk calculator. Eur Urol 2015; 68: 1083. Google Scholar 7. : Predictive factors for reclassification and relapse in prostate cancer eligible for active surveillance: a systematic review and meta-analysis. Urology 2016; 91: 136. Google Scholar 8. : An overview of current and emerging diagnostic, staging and prognostic markers for prostate cancer. Expert Rev Mol Diagn 2020; 20: 841. Google Scholar 9. : Quantifying the transition from active surveillance to watchful waiting among men with very low-risk prostate cancer. Eur Urol 2017; 72: 534. Google Scholar 10. : Long-term follow-up of a large active surveillance cohort of patients with prostate cancer. J Clin Oncol 2015; 33: 272. Google Scholar 11. : When and how should active surveillance for prostate cancer be de-escalated?Eur Urol Focus 2020; doi: 10.1016/j.euf.2020.01.001. Crossref, Google Scholar 12. : When should active surveillance for prostate cancer stop if no progression is detected?Prostate 2017; 77: 962. Google Scholar 13. : Role of surveillance biopsy with no cancer as a prognostic marker for reclassification: results from the canary prostate active surveillance study. Eur Urol 2018; 73: 706. Google Scholar 14. : A negative confirmatory biopsy among men on active surveillance for prostate cancer does not protect them from histologic grade progression. Eur Urol 2014; 66: 406. Google Scholar 15. : Predicting Gleason group progression for men on prostate cancer active surveillance: role of a negative confirmatory magnetic resonance imaging-ultrasound fusion biopsy. J Urol 2019; 201: 84. Link, Google Scholar 16. : When is a negative prostate biopsy really negative? Repeat biopsies in detection and active surveillance. J Urol 2017; 197: 973. Link, Google Scholar 17. : The Cochrane Collaboration's tool for assessing risk of bias in randomised trials. BMJ 2011; 343: d5928. Google Scholar 18. : Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 2010; 8: 336. Google Scholar 19. : Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 2010; 25: 603. Google Scholar 20. : Evaluating non-randomised intervention studies. Health Technol Assess 2003; 7: iii. Google Scholar 21. : How to obtain the confidence interval from a p value. BMJ 2011; 343: d2090. Google Scholar 22. : Random-effects model for meta-analysis of clinical trials: an update. Contemp Clin Trials 2007; 28: 105. Google Scholar 23. : Measuring inconsistency in meta-analyses. BMJ 2003; 327: 557. Google Scholar 24. : Negative first follow-up prostate biopsy on active surveillance is associated with decreased risk of upgrading, suspicion of progression and converting to active treatment. BJU Int 2020; doi: 10.1111/bju.15281. Crossref, Google Scholar 25. : Prognostic significance of a negative confirmatory biopsy on reclassification among men on active surveillance. Urology 2017; 107: 184. Google Scholar 26. : Role of prostate specific antigen and immediate confirmatory biopsy in predicting progression during active surveillance for low risk prostate cancer. J Urol 2011; 185: 477. Link, Google Scholar 27. : Risk stratification of men choosing surveillance for low risk prostate cancer. J Urol 2010; 183: 1779. Link, Google Scholar 28. : Role of repeated biopsy of the prostate in predicting disease progression in patients with prostate cancer on active surveillance. Cancer 2008; 113: 286. Google Scholar 29. : Magnetic resonance imaging for the detection of high grade cancer in the CANARY Prostate Active Surveillance Study. J Urol 2020; 204: 701. Link, Google Scholar 30. : Evaluating the four kallikrein panel of the 4Kscore for prediction of high-grade prostate cancer in men in the canary prostate active surveillance study. Eur Urol 2017; 72: 448. Google Scholar 31. : Predictors of pathologic progression on biopsy among men on active surveillance for localized prostate cancer: the value of the pattern of surveillance biopsies. Eur Urol 2014; 66: 337. Google Scholar 32. : A decade of active surveillance in the PRIAS study: an update and evaluation of the criteria used to recommend a switch to active treatment. Eur Urol 2016; 70: 954. Google Scholar 33. : Active surveillance for low-risk prostate cancer—in pursuit of a standardized protocol. Cent Eur J Urol 2020; 73: 123. Google Scholar 34. : 10-Year outcomes after monitoring, surgery, or radiotherapy for localized prostate cancer. N Engl J Med 2016; 375: 1415. Google Scholar 35. : Upgrading and downgrading of prostate cancer from biopsy to radical prostatectomy: incidence and predictive factors using the modified Gleason grading system and factoring in tertiary grades. Eur Urol 2012; 61: 1019. Google Scholar 36. : Active surveillance in younger men with prostate cancer. J Clin Oncol 2017; 35: 1898. Google Scholar 37. : Changes in prostate cancer grade on serial biopsy in men undergoing active surveillance. J Clin Oncol 2011; 29: 2795. Google Scholar 38. : Do low-grade and low-volume prostate cancers bear the hallmarks of malignancy?Lancet Oncol 2012; 13: e509. Google Scholar 39. : Predicting biopsy outcomes during active surveillance for prostate cancer: external validation of the CANARY Prostate Active Surveillance Study risk calculators in five large active surveillance cohorts. Eur Urol 2019; 76: 693. Google Scholar 40. : Active surveillance: a review of risk-based, dynamic monitoring. Transl Androl Urol 2018; 7: 106. Google Scholar 41. : Infective complications after prostate biopsy: outcome of the Global Prevalence Study of Infections in Urology (GPIU) 2010 and 2011, a prospective multinational multicentre prostate biopsy study. Eur Urol 2013; 63: 521. Google Scholar 42. : Active surveillance versus watchful waiting for localized prostate cancer: a model to inform decisions. Eur Urol 2017; 72: 899. Google Scholar 43. : Cost-effectiveness analysis of active surveillance strategies for men with low-risk prostate cancer. Eur Urol 2019; 75: 910. Google Scholar 44. : Randomized study of systematic biopsy versus magnetic resonance imaging and targeted and systematic biopsy in men on active surveillance (ASIST): 2-year postbiopsy follow-up. Eur Urol 2020; 77: 311. Google Scholar 45. : Value of serial multiparametric magnetic resonance imaging and magnetic resonance imaging-guided biopsies in men with low-risk prostate cancer on active surveillance after 1 yr follow-up. Eur Urol Focus 2019; 5: 407. Google Scholar Funding: National Institutes of Health/National Cancer Institute K08CA204732 (ML). Author Contributions: Project development: P. Rajwa, M. S. Leapman, S. F. Shariat. Data collection: P. Rajwa, B. Pradere, K. Mori. Data analysis: P. Rajwa, B. Pradere, K. Mori. Manuscript writing/editing: P. Rajwa, B. Pradere, K. Mori, G. Ploussard, M. S. Leapman, S. F. Shariat. © 2021 by American Urological Association Education and Research, Inc.FiguresReferencesRelatedDetailsCited ByMontorsi F, Leni R, Briganti A and Gandaglia G (2021) Association of Negative Followup Biopsy and Reclassification during Active Surveillance of Prostate Cancer: A Systematic Review and Meta-Analysis. Letter.Journal of Urology, VOL. 207, NO. 1, (242-242), Online publication date: 1-Jan-2022. Volume 205Issue 6June 2021Page: 1559-1568Supplementary Materials Advertisement Copyright & Permissions© 2021 by American Urological Association Education and Research, Inc.Keywordsprostatic neoplasms, magnetic resonance imagingprognosis, biopsywatchful waitingMetricsAuthor Information Pawel Rajwa Department of Urology, Medical University of Vienna, Vienna, Austria Department of Urology, Medical University of Silesia, Zabrze, Poland More articles by this author Benjamin Pradere Department of Urology, Medical University of Vienna, Vienna, Austria More articles by this author Keiichiro Mori Department of Urology, Medical University of Vienna, Vienna, Austria Department of Urology, The Jikei University School of Medicine, Tokyo, Japan More articles by this author Guillaume Ploussard Department of Urology, La Croix du Sud Hospital, Quint Fonsegrives, France More articles by this author Michael S. Leapman Department of Urology, Yale School of Medicine, New Haven, Connecticut More articles by this author Shahrokh F. Shariat Department of Urology, Medical University of Vienna, Vienna, Austria Department of Urology, Weill Cornell Medical College, New York, New York Department of Urology, University of Texas Southwestern, Dallas, Texas Karl Landsteiner Institute of Urology and Andrology, Vienna, Austria Department of Urology, Second Faculty of Medicine, Charles University, Prague, Czech Republic Institute for Urology and Reproductive Health, I.M. Sechenov First Moscow State Medical University, Moscow, Russia *Correspondence: Department of Urology, Comprehensive Cancer Center, Medical University Vienna, Vienna General Hospital, Währinger Gürtel 18-20, A-1090Vienna, Austria telephone: 43 1 4040026150; FAX: 43 1 40400 23320; E-mail Address: [email protected] More articles by this author Expand All Funding: National Institutes of Health/National Cancer Institute K08CA204732 (ML). Author Contributions: Project development: P. Rajwa, M. S. Leapman, S. F. Shariat. Data collection: P. Rajwa, B. Pradere, K. Mori. Data analysis: P. Rajwa, B. Pradere, K. Mori. Manuscript writing/editing: P. Rajwa, B. Pradere, K. Mori, G. Ploussard, M. S. Leapman, S. F. Shariat. Advertisement Advertisement PDF DownloadLoading ...
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