- Research article
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Favorable intermediate risk prostate cancer with biopsy Gleason score of 6
BMC Urology volume 21, Article number: 52 (2021)
Abstract
Background
To identify potential prognostic factors among patients with favorable intermediate risk prostate cancer with a biopsy Gleason score 6.
Methods
From 2003 to 2019, favorable intermediate risk patients who underwent radical prostatectomy were included in this study. All patients were evaluated preoperatively with MRI. Using PI-RADS scores, patients were divided into two groups, and clinic-pathological outcomes were compared. The impact of preoperative factors on significant pathologic Gleason score upgrading (≥ 4 + 3) and biochemical recurrence were assessed via multivariate analysis. Subgroup analysis was performed in patients with PI-RADS ≤ 2.
Results
Among the 239 patients, 116 (48.5%) were MRI-negative (PI-RADS ≤ 3) and 123 (51.5%) were MRI-positive (PI-RADS > 3). Six patients in the MRI-negative group (5.2%) were characterized as requiring significant pathologic Gleason score upgrading compared with 34 patients (27.6%) in the MRI-positive group (p < 0.001). PI-RADS score was shown to be a significant predictor of significant pathologic Gleason score upgrading (OR = 6.246, p < 0.001) and biochemical recurrence (HR = 2.595, p = 0.043). 10-years biochemical recurrence-free survival was estimated to be 84.4% and 72.6% in the MRI-negative and MRI-positive groups (p = 0.035). In the 79 patients with PI-RADS ≤ 2, tumor length in biopsy cores was identified as a significant predictor of pathologic Gleason score (OR = 11.336, p = 0.014).
Conclusions
Among the patients with favorable intermediate risk prostate cancer with a biopsy Gleason score 6, preoperative MRI was capable of predicting significant pathologic Gleason score upgrading and biochemical recurrence. Especially, the patients with PI-RADS ≤ 2 and low biopsy tumor length could be a potential candidate to active surveillance.
Background
Clinically localized prostate cancer can be managed with active surveillance (AS) [1]. Importantly, AS has emerged as a preferred initial management strategy for patients with low-risk (LR) PCa as it helps decrease the overtreatment of clinically indolent disease [2]. The safety and utility of AS in patients with LR PCa was confirmed and its use has rapidly increased worldwide. However, the utility of AS in patients with intermediate risk (IR) PCa remains unclear [3].
In the United States SEER (Surveillance, Epidemiology and End Results)-Medicare program, expectant management of LR PCa cases increased from 22 to 43% between 2004 and 2011; 15% to 18% of IR PCa cases were managed conservatively [4]. According to the National Comprehensive Cancer Network (NCCN) stratification, those classified within the favorable intermediate risk (FIR) group had better prognoses compared with those within the unfavorable intermediate risk (UFIR) group [5]; other studies revealed similar oncological results compared to LR PCa [6, 7]. Data from one long-term study revealed that a similar percentage of those in the IR group with a biopsy Gleason score of 6 and PSA between 10–20 ng/ml experienced 15-year metastatic-free survival compared to those with LR PCa (94% for both groups) [3]. Therefore, here we evaluated the potential utility of AS in individuals within the IR group, specifically those characterized as FIR.
Biochemical recurrence rates (BCR) following definitive primary treatment for IR PCa vary dramatically, with 5-year rates ranging from 2 to 70% [8,9,10,11]. Of note, current criteria for AS have a misclassification rate of between 15–30% [12,13,14,15]. Another study revealed that individuals with a bGS of 6 and a PSA between 10 and 20 ng/ml are at higher risk of pathologic Gleason score upgrading (PGU) and upstaging, making them poor candidates for AS [2]. A rate of 50% PGU has been reported in a variety of studies [16,17,18], suggesting that not all patients with bGS of 6 may be characterized appropriately.
Therefore, in this study, we characterized the outcomes of patients with FIR PCa who have a bGS of 6 and PSA between 10 and 20 ng/ml. Prognosis using MRI according to stratification was analyzed, and potential prognosticators were investigated among patients (and subgroups) with FIR PCa and clear MRI results.
Methods
All data analysis was carried out in accordance with applicable laws and regulations described in the Declaration of Helsinki and approved by institutional review board approval (Seoul National University Bundang Hospital (B-2004–608-104), we reviewed the records of patients who underwent radical prostatectomy (RP) in a single tertiary hospital between November 2003 and April 2019. Among them, patients with FIR PCa, preoperative bGS of 6, PSA between 10 and 20 ng/ml and a percent of positive biopsy cores < 50% were finally enrolled. All patients received ≥ 12 core transrectal prostate biopsy (MR fusion) and preoperative prostate MRI.
Prostate MRI exams were conducted 2–6 weeks after transrectal ultrasound–guided biopsy and before surgery. Prostate MRI up to 2006 was acquired in a biparametric manner including T2-weighted image (T2WI) and diffusion-weighted image (DWI). Since 2007, multiparametric prostate MRI, including dynamic contrast-enhanced (DCE) image, have been obtained. As PI-RADS was released and revised during this period, and to minimize the bias that may occur due to accumulated MRI reading experience over time, an experienced uroradiologist blinded from relevant information reviewed the preoperative MRI of the included patients for this retrospective study. Final scores for each patient were assigned according to PI-RADS (version 2) standards on a 5-point scale [19, 20]. The probability of clinically significant cancer was defined as follows: 1 (very low), 2 (low), 3 (intermediate), 4 (high), and 5 (very high).
Enrolled patients were stratified into two group according to preoperative MRI findings—the MRI-negative group (PI-RADS < 4) and the MRI-positive group (PI-RADS ≥ 4). Baseline characteristics [ie, age, body mass index (BMI), prostate volume, PSA, percent of positive biopsy core (%), total tumor length in cores, percentage of total tumor of all cores] between the two groups were compared using the student-t and chi-square tests.
RP specimens were assessed as previously reported [21]. Pathological parameters [ie, pGS, PGU, extracapsular extension (ECE), seminal vesicle invasion (SVI), positive surgical margin (PSM), pathologic tumor volume] were compared. We defined significant PGU (SPGU) as pathologic Gleason score ≥ 4 + 3 from bGS 6. All biopsy and RP pathology was newly reviewed by one uro-pathologist. A multivariate analysis was performed to predict SPGU using preoperative parameters and the PI-RADS grouping. Median follow-up duration was 58 months. BCR was defined as postoperative PSA ≥ 0.2 ng/mL taken twice at least 6 weeks apart [22]. Multivariate Cox proportional hazard model was also performed to predict BCR using preoperative parameters. A subgroup analysis was conducted in patients whose preoperative MRI showed no significant lesions and identified other preoperative parameters that could be predictors of PGU.
Results
In all, 239 patients with bGS of 6 and PSA between 10 and 20 ng/ml were enrolled in this study. Among them, 116 (48.5%) were placed into the MRI-negative group and 123 (51.5%) into the MRI-positive group. As shown in Table 1, those in the MRI-positive group had: i) a higher percentage of positive cores (28.51 vs. 20.42%, p = 0.003), ii) longer tumor lengths (0.51 vs. 0.32, mm, p < 0.001) and iii) percentage of total tumors of cores (32.02 vs. 20.76, %, p < 0.001). In the MRI-positive group, 64 (52.0%) and 59 (48.0%) of patients had PI-RADS scores of 4 and 5, respectively.
Pathological outcomes are presented in Table 2. A total of 199 (83.3%) and 40 (16.7%) of patients, respectively demonstrated PGU and SPGU. The percentage of patients demonstrated PGU was significantly higher in the MRI-positive group (96.7%) compared with the MRI-negative group (69.0%) (p < 0.001); similar results were noted for SPGU (≥ 4 + 3) (27.6% vs 5.2% in the MRI-positive and MRI-negative group, respectively) (p < 0.001). Other parameters (ie, ECE, PSM, pathologic tumor volume) were also higher in the MRI-positive group compared with the MRI-negative group (all p < 0.001).
A multivariate analysis revealed that SPGU, PI-RADS (OR 6.246, 95% CI 2.400–16.255, p < 0.001) and percentage of total tumors of core (OR 1.049, 95% CI 1.014–1.086, p < 0.006) were significant predictors of SPGU (Table 3).
During a median follow-up of 58 months, 31 patients experienced BCR. 10-year BCR-free survival was achieved by 83.2% and 54.8% of those in the MRI-negative and MRI-positive groups, respectively (log rant test p = 0.027, Fig. 1). A mutivariate Cox proportional hazard model revealed that prostate volume (HR = 0.956, 95% CI 0.923–0.991, p = 0.013) and PI-RADS score (HR = 2.595, 95% CI 1.949–7.098, p = 0.043) were significant predictors of BCR (Table 4).
A subgroup analysis of the 79 patients with bGS of 6, PSA between 10-20 ng/ml and PI-RADS < 3, revealed that 48 (60.8%) and 10 (12.7%) required PGU and SPGU, respectively. Among this subgroup, BCR occurred in only 4 patients (5.1%). 10-year BCR-free survival was 84.4%. Multivariate analysis was used to predict PGU in this group and results are presented in Table 5. Tumor length as assessed from biopsy cores was a significant predictor of PGU (OR: 11.336, p = 0.014).
Discussion
In the current study, we investigated potential prognosticators of individuals with FIR PCa, a bGS of 6 and a PSA between 10 and 20 ng/ml. Among the 239 patients included: i) 10-year BCR-free survival was estimated to be 70.9%, ii) PGU and SPGU from bGS 6 were determined to be 83.3% and 16.7%, respectively, iii) and preoperative MRI findings were significantly predictors of PGU and SPGU. These results could help inform the selection of FIR patients who would be most appropriate for AS.
The possibility of using AS for patients in the IR risk group has been previously raised. Accumulating evidence suggests that FIR PCa may be similar biologically to LR PCa. For instance, a previous study revealed that there was no significant difference in BCR between those with FIR and LR PCa [5]. Additionally, this study reported 5-year progression-free survival (PFS) rates of 93% and 87% in LR and FIR risk groups, respectively (p = 0.054). These results are similar to what was observed in this study, namely a 10-year BCR-free survival rate of 70.9% in the FIR group.
Reports suggest that less aggressive IR cancer could be a potential candidate for AS. In particular, patients with Grade Group 1 (bGS 6) IR have been shown to have a low risk of progression to metastasis [23,24,25,26]. One large surveillance study (Sunnybrook in Toronto) reported data from a cohort of individuals receiving conservative treatment for IR PCa. Although the 15-year PCa metastatsis rate was 3.7 times higher in the IR risk group compared with the LR group, the presence of Gleason 7 cancer at initial diagnosis accounted for almost all of this increase in risk [3]. Patients with a bGS of 6 and PSA between 10 and 20 ng/ml had an estimated 15-year metastasis-free survival rate of 94%, a rate very similar to patients with LR PCa. This group highlighted that a PSA above 10 did not confer a significantly increased risk of metastasis in those without a cancer with a Gleason score of 4 [27]. Loeb et al. [28] revealed the patients with a bGS of 6 (Grade Group 1), PSA between 10 and 15 mg/ml and a PSA density less than 0.15 ng/ml did not significantly differ in adverse pathology findings when compared to those with LR PCa. As a result, the authors concluded that patients with bGS 6 IR PCa could be candidates for AS.
It should be noted, however, that other studies with contradictory findings have also been published. Aghazadeh et al. [5] conducted a large study (3,686 patients) which compared prognoses between FIR and LR PCa. The rate of adverse pathological findings in those with FIR was significantly higher when compared with those with lower risk PCa and significantly lower when compared with those with unfavorable intermediate risk PCa (27.4% vs 14.8% and 48.5%, respectively, each p < 0.001). In an Asian population study, the FIR group had significantly lower 5-year BCR-free survival when compared with the LR group (87.5 vs 93.5%; P = 0.002) [29]. These results could be caused by a discrepancy between bGS and pathological Gleason score. Yang et al. reported that 25.5% of patients with bGS 6 FIR PCa and PSA between 10 and 20 ng/ml required PGU and pathological upstaging [2]. Similarly, a report involving 359 men with bGS 6 and PSA between 10 and 20 ng/ml who underwent RP, revealed that 40.4% patients required PGU; among this group, 5% were upgraded into GS ≥ 8 [30]. Here, 83.3% of patients required PGU after RP, 16.7% had pathologic GS above 4 + 3. These results suggest that a proportion of patients with Gleason score 6 at preoperative biopsy may always require PGU.
Advances in software and hardware technology has led to the development of multi-parametric MRI for use in the detection of prostate cancer. Validation of this and other MRI-based tools have been summarized in guidelines published by the European Society of Urogenital Radiology (ESUR) along with a scoring system for PCa known as PI-RADS. Seo et al. revealed that PI-RADS can serve as a predictor of GS upgrading, with an estimated accuracy of 0.672–0.685 [1]. Another study of 126 cancer foci demonstrated that: i) PIRAD scores were 90% accurate at predicting Gleason score agreement between biopsy and pathologic GS (OR: 2.64, p < 0.001) and ii) MRI findings were capable of predicting PGU. Here, it was revealed that PI-RADS scores were a significant predictor of PGU (OR: 7.407, p < 0.001, data not shown) and SPGU (OR: 6.246, p < 0.001). Therefore, patients with FIR PCa, a bGS of 6 and a PI-RADS score ≤ 3 may be good candidates for AS. Among them, estimated 10-year BCR-free survival for patients with PCa and a PI-RADS score ≤ 2 was 84.4%, as good or better than the results reported from other studies of patients with LR PCa (66% to 88%) [31, 32]. Therefore, patients with FIR PCa with preoperative MRI (PI-RADS score ≤ 2) appear to be the ideal candidate for AS; furthermore, AS was seven safer in a subset of these patients with smaller biopsy tumor lengths.
This study does have several limitations that should be mentioned, primarily, the limited number of subjects and retrospective nature. Additionally, the PI-RADS score was assigned on biparametric MRI in patients included in earlier period. However, the diagnostic performance of the PI-RADS score of biparametric MRI is not reported to be inferior to that of multiparametric MRI [33]. Another limitation is the relatively high rate of PGU. The single pathologist who has a specialty for uro-oncology reviewed all of the specimens included in this study through International Society of Urological Pathology (ISUP) recommendation of modified Gleason score which announced in 2005 after handling by very thin sectioned. Regardless the extent of tumor, any Gleason pattern 4 was found in any section at radical prostatectomy specimen with 99% Gleason pattern 3, therefore Gleason score was 3 + 4. It was reason for high rate of PGU. In our results, 159 patients (79.9%) were pathologically upgraded to Gleason score 3 + 4 and only 38 patients (15.9%) to Gleason score 4 + 3 among 203 patients had experienced PGU after RP. The pathologic profiles of our participants appear to be relatively more aggressive (ie, higher PSA level, higher rate of high-grade disease) than those reported in western series. It is important to note that the rate of PSA screening in Asia is still not as high as in Western countries [34].
Conclusions
Among the patients with FIR PCa, a bGS of 6 and a PSA of between 10-20 ng.ml, preoperative MRI was capable of predicting sPGU and BCR. Based on these results, we suggest that patients with FIR PCa who had a negative preoperative MRI and minimal tumor volume as assessed by biopsy are ideal candidates for AS.
Availability of data and materials
The full dataset generated and analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- PCa:
-
Prostate cancer
- bGS:
-
Biopsy Gleason score
- AS:
-
Active surveillance
- LR:
-
Low risk
- IR:
-
Intermediate risk
- SEER:
-
Surveillance, Epidemiology and End Results
- NCCN:
-
National Comprehensive Cancer Network
- FIR:
-
Favorable intermediate risk
- UFIR:
-
Unfavorable intermediate risk
- PSA:
-
Prostate specific antigen
- BCR:
-
Biochemical recurrence
- PGU:
-
Pathologic Gleason score upgrading
- MRI:
-
Magnetic resonance imaging
- RP:
-
Radical prostatectomy
- T2WI:
-
T2-weighted image
- DWI:
-
Diffusion-weighed image
- DCE:
-
Dynamic contrast-enhanced
- BMI:
-
Body mass index
- ECE:
-
Extracapsular extension
- SVI:
-
Seminal vesicle invasion
- PSM:
-
Positive surgical margin
- SPGU:
-
Significant pathologic Gleason score upgrading
References
Seo JW, Shin SJ, Taik OhY, Jung DC, Cho NH, Choi YD, et al. PI-RADS Version 2: Detection of Clinically Significant Cancer in Patients With Biopsy Gleason Score 6 Prostate Cancer. AJR Am J Roentgenol. 2017;209(1):W1-w9.
Yang DD, Mahal BA, Muralidhar V, Vastola ME, Boldbaatar N, Labe SA, et al. Pathologic Outcomes of Gleason 6 Favorable Intermediate-Risk Prostate Cancer Treated With Radical Prostatectomy: Implications for Active Surveillance. Clin Genitourin Cancer. 2018;16(3):226–34.
Musunuru HB, Yamamoto T, Klotz L, Ghanem G, Mamedov A, Sethukavalan P, et al. Active Surveillance for Intermediate Risk Prostate Cancer: Survival Outcomes in the Sunnybrook Experience. J Urol. 2016;196(6):1651–8.
Tsai HT, Philips G, Taylor KL, Kowalczyk K, Huai-Ching K, Potosky AL: Utilization and predictors of expectant management among elderly men with low-and intermediate-risk localized prostate cancer in U.S. urological practice. Urol Pract. 2017;4(2):132–9.
Aghazadeh MA, Frankel J, Belanger M, McLaughlin T, Tortora J, Staff I, et al. National Comprehensive Cancer Network(R) Favorable Intermediate Risk Prostate Cancer-Is Active Surveillance Appropriate? J Urol. 2018;199(5):1196–201.
Tosoian JJ, Mamawala M, Epstein JI, Landis P, Wolf S, Trock BJ, et al. Intermediate and Longer-Term Outcomes From a Prospective Active-Surveillance Program for Favorable-Risk Prostate Cancer. J Clin Oncol. 2015;33(30):3379–85.
Godtman RA, Holmberg E, Khatami A, Pihl CG, Stranne J, Hugosson J. Long-term Results of Active Surveillance in the Goteborg Randomized, Population-based Prostate Cancer Screening Trial. Eur Urol. 2016;70(5):760–6.
Grossfeld GD, Latini DM, Lubeck DP, Broering JM, Li YP, Mehta SS, et al. Predicting disease recurrence in intermediate and high-risk patients undergoing radical prostatectomy using percent positive biopsies: results from CaPSURE. Urology. 2002;59(4):560–5.
Morris WJ, Keyes M, Palma D, Spadinger I, McKenzie MR, Agranovich A, et al.: Population-based study of biochemical and survival outcomes after permanent 125I brachytherapy for low- and intermediate-risk prostate cancer. Urology 2009;73(4):860–5; discussion 5–7
Weiner AB, Patel SG, Etzioni R, Eggener SE. National trends in the management of low and intermediate risk prostate cancer in the United States. J Urol. 2015;193(1):95–102.
Abern MR, Aronson WJ, Terris MK, Kane CJ, Presti JC Jr, Amling CL, et al. Delayed radical prostatectomy for intermediate-risk prostate cancer is associated with biochemical recurrence: possible implications for active surveillance from the SEARCH database. Prostate. 2013;73(4):409–17.
Iremashvili V, Manoharan M, Parekh DJ, Punnen S. Can nomograms improve our ability to select candidates for active surveillance for prostate cancer? Prostate Cancer Prostatic Dis. 2016;19(4):385–9.
Iremashvili V, Pelaez L, Manoharan M, Jorda M, Rosenberg DL, Soloway MS. Pathologic prostate cancer characteristics in patients eligible for active surveillance: a head-to-head comparison of contemporary protocols. Eur Urol. 2012;62(3):462–8.
Gandaglia G, Ploussard G, Isbarn H, Suardi N, De Visschere PJ, Futterer JJ, et al. What is the optimal definition of misclassification in patients with very low-risk prostate cancer eligible for active surveillance? Results from a multi-institutional series. Urol Oncol. 2015;33(4):164.e1-9.
Morlacco A, Cheville JC, Rangel LJ, Gearman DJ, Karnes RJ. Adverse Disease Features in Gleason Score 3 + 4 “Favorable Intermediate-Risk” Prostate Cancer: Implications for Active Surveillance. Eur Urol. 2017;72(3):442–7.
Heidegger I, Ladurner M, Skradski V, Klocker H, Schafer G, Horninger W, et al. Adverse pathological findings in needle biopsy gleason score 6 prostate cancers with low and intermediate preoperative PSA levels following radical prostatectomy. Anticancer Res. 2012;32(12):5481–5.
Montironi R, Scarpelli M, Lopez-Beltran A, Cheng L. Editorial comment on: Expression of the endothelin axis in noninvasive and superficially invasive bladder cancer: relation to clinicopathologic and molecular prognostic parameters. Eur Urol. 2009;56(5):846–7.
Cookson MS, Fleshner NE, Soloway SM, Fair WR. Correlation between Gleason score of needle biopsy and radical prostatectomy specimen: accuracy and clinical implications. J Urol. 1997;157(2):559–62.
Weinreb JC, Barentsz JO, Choyke PL, Cornud F, Haider MA, Macura KJ, et al. PI-RADS Prostate Imaging - Reporting and Data System: 2015, Version 2. Eur Urol. 2016;69(1):16–40.
Vargas HA, Hotker AM, Goldman DA, Moskowitz CS, Gondo T, Matsumoto K, et al. Updated prostate imaging reporting and data system (PIRADS v2) recommendations for the detection of clinically significant prostate cancer using multiparametric MRI: critical evaluation using whole-mount pathology as standard of reference. Eur Radiol. 2016;26(6):1606–12.
Kim K, Lee JK, Choe G, Hong SK. Intraprostatic locations of tumor foci of higher grade missed by diagnostic prostate biopsy among potential candidates for active surveillance. Sci Rep. 2016;6:36781.
Cookson MS, Aus G, Burnett AL, Canby-Hagino ED, D’Amico AV, Dmochowski RR, et al. Variation in the definition of biochemical recurrence in patients treated for localized prostate cancer: the American Urological Association Prostate Guidelines for Localized Prostate Cancer Update Panel report and recommendations for a standard in the reporting of surgical outcomes. J Urol. 2007;177(2):540–5.
Raldow AC, Zhang D, Chen MH, Braccioforte MH, Moran BJ, D’Amico AV. Risk Group and Death From Prostate Cancer: Implications for Active Surveillance in Men With Favorable Intermediate-Risk Prostate Cancer. JAMA Oncol. 2015;1(3):334–40.
Rodrigues G, Lukka H, Warde P, Brundage M, Souhami L, Crook J, et al. The prostate cancer risk stratification (ProCaRS) project: recursive partitioning risk stratification analysis. Radiother Oncol. 2013;109(2):204–10.
Klotz L. Active Surveillance for Intermediate Risk Prostate Cancer. Curr Urol Rep. 2017;18(10):80.
Sebastianelli A, Morselli S, Vitelli FD, Gabellini L, Tasso G, Venturini S, et al. The role of prostate-specific antigen density in men with low-risk prostate cancer suitable for active surveillance: results of a prospective observational study. Prostate Int. 2019;7(4):139–42.
Yamamoto T, Musunuru HB, Vesprini D, Zhang L, Ghanem G, Loblaw A, et al. Metastatic Prostate Cancer in Men Initially Treated with Active Surveillance. J Urol. 2016;195(5):1409–14.
Loeb S, Folkvaljon Y, Bratt O, Robinson D, Stattin P. Defining Intermediate Risk Prostate Cancer Suitable for Active Surveillance. J Urol. 2019;201(2):292–9.
Jung JW, Lee JK, Hong SK, Byun SS, Lee SE. Stratification of patients with intermediate-risk prostate cancer. BJU Int. 2015;115(6):907–12.
Santok GD, Abdel Raheem A, Kim LH, Chang K, Lum TG, Chung BH, et al. Prostate-specific antigen 10–20 ng/mL: A predictor of degree of upgrading to >/=8 among patients with biopsy Gleason score 6. Investig Clin Urol. 2017;58(2):90–7.
Kane CJ, Im R, Amling CL, Presti JC Jr, Aronson WJ, Terris MK, et al. Outcomes after radical prostatectomy among men who are candidates for active surveillance: results from the SEARCH database. Urology. 2010;76(3):695–700.
Weight CJ, Reuther AM, Gunn PW, Zippe CR, Dhar NB, Klein EA. Limited pelvic lymph node dissection does not improve biochemical relapse-free survival at 10 years after radical prostatectomy in patients with low-risk prostate cancer. Urology. 2008;71(1):141–5.
Monni F, Fontanella P, Grasso A, Wiklund P, Ou YC, Randazzo M, et al. Magnetic resonance imaging in prostate cancer detection and management: a systematic review. Minerva Urol Nefrol. 2017;69(6):567–78.
Zhang K, Bangma CH, Roobol MJ. Prostate cancer screening in Europe and Asia. Asian J Urol. 2017;4(2):86–95.
Acknowledgements
This work was supported by Grant Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2020R1A2C1100011)
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Protocol/project development: Sung Kyu Hong. Data collection or management: Hyungwoo Ahn, Sung Il Hwang, Hak Jong Lee, Sangchul Lee, Hakmin Lee, Seok-Soo Byun, Gheeyoung Choe. Data analysis: Jong Jin Oh. Manuscript writing/editing: Jong Jin Oh. All authors read and approved the final manuscript.
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All data analysis was carried out in accordance with applicable laws and regulations described in the Declaration of Helsinki and approved by institutional review board approval (Seoul National University Bundang Hospital ((B-2004–608-104). All participants gave their informed written consent.
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Oh, J.J., Ahn, H., Hwang, S.I. et al. Favorable intermediate risk prostate cancer with biopsy Gleason score of 6. BMC Urol 21, 52 (2021). https://doi.org/10.1186/s12894-021-00827-2
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DOI: https://doi.org/10.1186/s12894-021-00827-2