Skip to main content
Top
Published in: Annals of Surgical Oncology 12/2018

01-11-2018 | Urologic Oncology

Contemporary Epstein Criteria with Biopsy-Naïve Multiparametric Magnetic Resonance Imaging to Prevent Incorrect Assignment to Active Surveillance in the PI-RADS Version 2.0 Era

Authors: Yu Fan, MD, Lingyun Zhai, MD, Yisen Meng, MD, Yuke Chen, MD, Shaoshuai Sun, MD, Huihui Wang, MD, Shuai Hu, MD, PhD, Qi Shen, MD, PhD, Yi Liu, MD, Derun Li, MD, Xueru Feng, MD, Qun He, MD, PhD, Xiaoying Wang, MD, Wei Yu, MD, Jie Jin, MD, PhD

Published in: Annals of Surgical Oncology | Issue 12/2018

Login to get access

Abstract

Purpose

The aim of this study is to evaluate the effectiveness of multiparametric magnetic resonance imaging (mp-MRI) in prostate cancer (PCa) patients with biopsy Gleason score ≤ 6 who may otherwise be assigned to active surveillance (AS).

Patients and Methods

This was a retrospective study of 90 patients who underwent transrectal systematic biopsy for prostate cancer with Gleason score ≤ 6 without neoadjuvant therapy, with radical prostatectomy (RP) conducted between September 2009 and March 2018. All patients underwent prebiopsy mp-MRI. The prostate imaging reporting and data system (PI-RADS) version 2.0 score was evaluated. The correlation between imaging results and pathological findings was analyzed. We established models based on Epstein criteria with or without PI-RADS score and evaluated their ability for screening of potential PCa AS candidates.

Results

Among 90 patients, 60 (66.7%) had upgrade (Gleason ≥ 7), 30 (33.3%) had extraprostatic extension, and 9 (10%) had seminal vesicle invasion on RP specimens. The rate of unfavorable disease was 67.8% (61 of 90). On multivariate analysis, independent risk factors for unfavorable disease were prostate-specific antigen density and PI-RADS score. The model based on Epstein criteria with PI-RADS score showed improved integrated discrimination improvement index and was superior to the classical Epstein criteria on decision curve analysis for screening potential prostate cancer AS candidates.

Conclusions

Multiparametric MRI with PIRADS 2.0 provides useful supplementary information to Epstein criteria, and may prevent incorrect assignment to active surveillance.
Appendix
Available only for authorised users
Literature
1.
go back to reference Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–86.CrossRef Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–86.CrossRef
2.
go back to reference Wong MC, Goggins WB, Wang HH, et al. Global incidence and mortality for prostate cancer: analysis of temporal patterns and trends in 36 countries. Eur Urol. 2016;70:862–74.CrossRef Wong MC, Goggins WB, Wang HH, et al. Global incidence and mortality for prostate cancer: analysis of temporal patterns and trends in 36 countries. Eur Urol. 2016;70:862–74.CrossRef
3.
go back to reference Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66:115–32.CrossRef Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66:115–32.CrossRef
4.
go back to reference Klotz L, Zhang L, Lam A, Nam R, Mamedov A, Loblaw A. Clinical results of long-term follow-up of a large, active surveillance cohort with localized prostate cancer. J Clin Oncol. 2010;28:126–31.CrossRef Klotz L, Zhang L, Lam A, Nam R, Mamedov A, Loblaw A. Clinical results of long-term follow-up of a large, active surveillance cohort with localized prostate cancer. J Clin Oncol. 2010;28:126–31.CrossRef
5.
go back to reference Huang GJ, Sadetsky N, Penson DF. Health related quality of life for men treated for localized prostate cancer with long-term followup. J Urol. 2010;183:2206–12.CrossRef Huang GJ, Sadetsky N, Penson DF. Health related quality of life for men treated for localized prostate cancer with long-term followup. J Urol. 2010;183:2206–12.CrossRef
6.
go back to reference Dall’Era MA, Albertsen PC, Bangma C, et al. Active surveillance for prostate cancer: a systematic review of the literature. Eur Urol. 2012;62:976–83.CrossRef Dall’Era MA, Albertsen PC, Bangma C, et al. Active surveillance for prostate cancer: a systematic review of the literature. Eur Urol. 2012;62:976–83.CrossRef
7.
go back to reference 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;62:462–8.CrossRef 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;62:462–8.CrossRef
8.
go back to reference Lim SK, Kim KH, Shin TY, et al. Yonsei criteria: a new protocol for active surveillance in the era of robotic and local ablative surgeries. Clin Genitourin Cancer. 2013;11:501–7.CrossRef Lim SK, Kim KH, Shin TY, et al. Yonsei criteria: a new protocol for active surveillance in the era of robotic and local ablative surgeries. Clin Genitourin Cancer. 2013;11:501–7.CrossRef
9.
go back to reference Kim TH, Jeon HG, Choo SH, et al. Pathological upgrading and upstaging of patients eligible for active surveillance according to currently used protocols. Int J Urol. 2014;21:377–81.CrossRef Kim TH, Jeon HG, Choo SH, et al. Pathological upgrading and upstaging of patients eligible for active surveillance according to currently used protocols. Int J Urol. 2014;21:377–81.CrossRef
10.
go back to reference Lee SE, Kim DS, Lee WK, et al. Application of the Epstein criteria for prediction of clinically insignificant prostate cancer in Korean men. BJU Int. 2010;105:1526–30.CrossRef Lee SE, Kim DS, Lee WK, et al. Application of the Epstein criteria for prediction of clinically insignificant prostate cancer in Korean men. BJU Int. 2010;105:1526–30.CrossRef
11.
go back to reference Yamada Y, Sakamoto S, Sazuka T, et al. Validation of active surveillance criteria for pathologically insignificant prostate cancer in Asian men. Int J Urol. 2016;23:49–54.CrossRef Yamada Y, Sakamoto S, Sazuka T, et al. Validation of active surveillance criteria for pathologically insignificant prostate cancer in Asian men. Int J Urol. 2016;23:49–54.CrossRef
12.
go back to reference Cantiello F, Russo GI, Cicione A, et al. PHI and PCA3 improve the prognostic performance of PRIAS and Epstein criteria in predicting insignificant prostate cancer in men eligible for active surveillance. World J Urol. 2016;34(4):485–93.CrossRef Cantiello F, Russo GI, Cicione A, et al. PHI and PCA3 improve the prognostic performance of PRIAS and Epstein criteria in predicting insignificant prostate cancer in men eligible for active surveillance. World J Urol. 2016;34(4):485–93.CrossRef
13.
go back to reference Ferro M, Lucarelli G, Bruzzese D, et al. Improving the prediction of pathologic outcomes in patients undergoing radical prostatectomy: the value of prostate cancer antigen 3 (PCA3), prostate health index (phi) and sarcosine. Anticancer Res. 2015;35(2):1017–23.PubMed Ferro M, Lucarelli G, Bruzzese D, et al. Improving the prediction of pathologic outcomes in patients undergoing radical prostatectomy: the value of prostate cancer antigen 3 (PCA3), prostate health index (phi) and sarcosine. Anticancer Res. 2015;35(2):1017–23.PubMed
14.
go back to reference Schoots IG, Petrides N, Giganti F, et al. Magnetic resonance imaging in active surveillance of prostate cancer: a systematic review. Eur Urol. 2015;67:627–36.CrossRef Schoots IG, Petrides N, Giganti F, et al. Magnetic resonance imaging in active surveillance of prostate cancer: a systematic review. Eur Urol. 2015;67:627–36.CrossRef
15.
go back to reference van den Bergh RC, Ahmed HU, Bangma CH, Cooperberg MR, Villers A, Parker CC. Novel tools to improve patient selection and monitoring on active surveillance for low-risk prostate cancer: a systematic review. Eur Urol. 2014;65:1023–31.CrossRef van den Bergh RC, Ahmed HU, Bangma CH, Cooperberg MR, Villers A, Parker CC. Novel tools to improve patient selection and monitoring on active surveillance for low-risk prostate cancer: a systematic review. Eur Urol. 2014;65:1023–31.CrossRef
16.
go back to reference Shukla-Dave A, Hricak H, Akin O, et al. Preoperative nomograms incorporating magnetic resonance imaging and spectroscopy for prediction of insignificant prostate cancer. BJU Int. 2012;109:1315–22.CrossRef Shukla-Dave A, Hricak H, Akin O, et al. Preoperative nomograms incorporating magnetic resonance imaging and spectroscopy for prediction of insignificant prostate cancer. BJU Int. 2012;109:1315–22.CrossRef
17.
go back to reference Somford DM, Hambrock T, Hulsbergen-van de Kaa CA, et al. Initial experience with identifying high-grade prostate cancer using diffusion-weighted MR imaging (DWI) in patients with a Gleason score </= 3 + 3 = 6 upon schematic TRUS-guided biopsy: a radical prostatectomy correlated series. Invest Radiol. 2012;47:153–8.PubMed Somford DM, Hambrock T, Hulsbergen-van de Kaa CA, et al. Initial experience with identifying high-grade prostate cancer using diffusion-weighted MR imaging (DWI) in patients with a Gleason score </= 3 + 3 = 6 upon schematic TRUS-guided biopsy: a radical prostatectomy correlated series. Invest Radiol. 2012;47:153–8.PubMed
18.
go back to reference Borofsky MS, Rosenkrantz AB, Abraham N, Jain R, Taneja SS. Does suspicion of prostate cancer on integrated T2 and diffusion-weighted MRI predict more adverse pathology on radical prostatectomy? Urology. 2013;81:1279–83.CrossRef Borofsky MS, Rosenkrantz AB, Abraham N, Jain R, Taneja SS. Does suspicion of prostate cancer on integrated T2 and diffusion-weighted MRI predict more adverse pathology on radical prostatectomy? Urology. 2013;81:1279–83.CrossRef
19.
go back to reference Lee DH, Koo KC, Lee SH, et al. Tumor lesion diameter on diffusion weighted magnetic resonance imaging could help predict insignificant prostate cancer in patients eligible for active surveillance: preliminary analysis. J Urol. 2013;190:1213–17.CrossRef Lee DH, Koo KC, Lee SH, et al. Tumor lesion diameter on diffusion weighted magnetic resonance imaging could help predict insignificant prostate cancer in patients eligible for active surveillance: preliminary analysis. J Urol. 2013;190:1213–17.CrossRef
20.
go back to reference Lee DH, Koo KC, Lee SH, et al. Low-risk prostate cancer patients without visible tumor (T1c) on multiparametric MRI could qualify for active surveillance candidate even if they did not meet inclusion criteria of active surveillance protocol. Jpn J Clin Oncol. 2013;43:553–8.CrossRef Lee DH, Koo KC, Lee SH, et al. Low-risk prostate cancer patients without visible tumor (T1c) on multiparametric MRI could qualify for active surveillance candidate even if they did not meet inclusion criteria of active surveillance protocol. Jpn J Clin Oncol. 2013;43:553–8.CrossRef
21.
go back to reference Park BH, Jeon HG, Choo SH, et al. Role of multiparametric 3.0-Tesla magnetic resonance imaging in patients with prostate cancer eligible for active surveillance. BJU Int. 2014;113:864–70.CrossRef Park BH, Jeon HG, Choo SH, et al. Role of multiparametric 3.0-Tesla magnetic resonance imaging in patients with prostate cancer eligible for active surveillance. BJU Int. 2014;113:864–70.CrossRef
22.
go back to reference Rosenkrantz AB, Prabhu V, Sigmund EE, Babb JS, Deng FM, Taneja SS. Utility of diffusional kurtosis imaging as a marker of adverse pathologic outcomes among prostate cancer active surveillance candidates undergoing radical prostatectomy. Am J Roentgenol. 2013;201:840–6.CrossRef Rosenkrantz AB, Prabhu V, Sigmund EE, Babb JS, Deng FM, Taneja SS. Utility of diffusional kurtosis imaging as a marker of adverse pathologic outcomes among prostate cancer active surveillance candidates undergoing radical prostatectomy. Am J Roentgenol. 2013;201:840–6.CrossRef
23.
go back to reference Turkbey B, Mani H, Aras O, et al. Prostate cancer: can multiparametric MR imaging help identify patients who are candidates for active surveillance? Radiology. 2013;268:144–52.CrossRef Turkbey B, Mani H, Aras O, et al. Prostate cancer: can multiparametric MR imaging help identify patients who are candidates for active surveillance? Radiology. 2013;268:144–52.CrossRef
24.
go back to reference Ploussard G, Xylinas E, Durand X, et al. Magnetic resonance imaging does not improve the prediction of misclassification of prostate cancer patients eligible for active surveillance when the most stringent selection criteria are based on the saturation biopsy scheme. BJU Int. 2011;108:513–7.CrossRef Ploussard G, Xylinas E, Durand X, et al. Magnetic resonance imaging does not improve the prediction of misclassification of prostate cancer patients eligible for active surveillance when the most stringent selection criteria are based on the saturation biopsy scheme. BJU Int. 2011;108:513–7.CrossRef
25.
go back to reference Guzzo TJ, Resnick MJ, Canter DJ, et al. Endorectal T2-weighted MRI does not differentiate between favorable and adverse pathologic features in men with prostate cancer who would qualify for active surveillance. Urol Oncol. 2012;30:301–5.CrossRef Guzzo TJ, Resnick MJ, Canter DJ, et al. Endorectal T2-weighted MRI does not differentiate between favorable and adverse pathologic features in men with prostate cancer who would qualify for active surveillance. Urol Oncol. 2012;30:301–5.CrossRef
26.
go back to reference Bjurlin MA, Carter HB, Schellhammer P, et al. Optimization of initial prostate biopsy in clinical practice: sampling, labeling and specimen processing. J Urol. 2013;189(6):2039–46.CrossRef Bjurlin MA, Carter HB, Schellhammer P, et al. Optimization of initial prostate biopsy in clinical practice: sampling, labeling and specimen processing. J Urol. 2013;189(6):2039–46.CrossRef
27.
go back to reference Eskew LA, Bare RL, McCullough DL. Systematic 5 region prostate biopsy is superior to sextant method for diagnosing carcinoma of the prostate. J Urol. 1997;157(1):199–202. (Discussion 202–193). CrossRef Eskew LA, Bare RL, McCullough DL. Systematic 5 region prostate biopsy is superior to sextant method for diagnosing carcinoma of the prostate. J Urol. 1997;157(1):199–202. (Discussion 202–193). CrossRef
28.
go back to reference Weinreb JC, Barentsz JO, Choyke PL, et al. PI-RADS prostate imaging—reporting and data system: 2015, version 2. Eur Urol. 2016;69:16–40.CrossRef Weinreb JC, Barentsz JO, Choyke PL, et al. PI-RADS prostate imaging—reporting and data system: 2015, version 2. Eur Urol. 2016;69:16–40.CrossRef
29.
go back to reference Yim JH, Kim CK. Clinically insignificant prostate cancer suitable for active surveillance according to Prostate Cancer Research International: active surveillance criteria: utility of PI-RADS v2. J Magn Reson Imaging. 2018;47:1072–79.CrossRef Yim JH, Kim CK. Clinically insignificant prostate cancer suitable for active surveillance according to Prostate Cancer Research International: active surveillance criteria: utility of PI-RADS v2. J Magn Reson Imaging. 2018;47:1072–79.CrossRef
30.
go back to reference Collins GS, Reitsma JB, Altman DG, Moons KG. Transparent reporting of a multivariable prediction model for individual prognosis or diagnosis (TRIPOD): the TRIPOD statement. BMC Med. 2015;13:1.CrossRef Collins GS, Reitsma JB, Altman DG, Moons KG. Transparent reporting of a multivariable prediction model for individual prognosis or diagnosis (TRIPOD): the TRIPOD statement. BMC Med. 2015;13:1.CrossRef
32.
go back to reference DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics. 1988;44:837–45.CrossRef DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics. 1988;44:837–45.CrossRef
33.
go back to reference Pencina MJ, D’Agostino RB, Vasan RS. Statistical methods for assessment of added usefulness of new biomarkers. Clin Chem Lab Med. 2010;48:1703–11.CrossRef Pencina MJ, D’Agostino RB, Vasan RS. Statistical methods for assessment of added usefulness of new biomarkers. Clin Chem Lab Med. 2010;48:1703–11.CrossRef
34.
go back to reference Pulleyblank R, Chuma J, Gilbody SM, Thompson C. Decision curve analysis for assessing the usefulness of tests for making decisions to treat: an application to tests for prodromal psychosis. Psychol Assess. 2013;25:730–7.CrossRef Pulleyblank R, Chuma J, Gilbody SM, Thompson C. Decision curve analysis for assessing the usefulness of tests for making decisions to treat: an application to tests for prodromal psychosis. Psychol Assess. 2013;25:730–7.CrossRef
35.
go back to reference Vargas HA, Akin O, Afaq A, et al. Magnetic resonance imaging for predicting prostate biopsy findings in patients considered for active surveillance of clinically low risk prostate cancer. J Urol. 2012;188:1732–8.CrossRef Vargas HA, Akin O, Afaq A, et al. Magnetic resonance imaging for predicting prostate biopsy findings in patients considered for active surveillance of clinically low risk prostate cancer. J Urol. 2012;188:1732–8.CrossRef
36.
go back to reference Zhang L, Tang M, Chen S, Lei X, Zhang X, Huan Y. A meta-analysis of use of prostate imaging reporting and data system version 2 (PI-RADS V2) with multiparametric MR imaging for the detection of prostate cancer. Eur Radiol. 2017;27:5204–4.CrossRef Zhang L, Tang M, Chen S, Lei X, Zhang X, Huan Y. A meta-analysis of use of prostate imaging reporting and data system version 2 (PI-RADS V2) with multiparametric MR imaging for the detection of prostate cancer. Eur Radiol. 2017;27:5204–4.CrossRef
37.
go back to reference Zhao C, Gao G, Fang D, et al. The efficiency of multiparametric magnetic resonance imaging (mpMRI) using PI-RADS version 2 in the diagnosis of clinically significant prostate cancer. Clin Imaging. 2016;40:885–8.CrossRef Zhao C, Gao G, Fang D, et al. The efficiency of multiparametric magnetic resonance imaging (mpMRI) using PI-RADS version 2 in the diagnosis of clinically significant prostate cancer. Clin Imaging. 2016;40:885–8.CrossRef
38.
go back to reference Park JJ, Park BK. Role of PI-RADSv2 with multiparametric MRI in determining who needs active surveillance or definitive treatment according to PRIAS. J Magn Reson Imaging. 2017;45:1753–9.CrossRef Park JJ, Park BK. Role of PI-RADSv2 with multiparametric MRI in determining who needs active surveillance or definitive treatment according to PRIAS. J Magn Reson Imaging. 2017;45:1753–9.CrossRef
39.
go back to reference Almeida GL, Petralia G, Ferro M, et al. Role of multi-parametric magnetic resonance image and PIRADS score in patients with prostate cancer eligible for active surveillance according PRIAS criteria. Urol Int. 2016;96:459–69.CrossRef Almeida GL, Petralia G, Ferro M, et al. Role of multi-parametric magnetic resonance image and PIRADS score in patients with prostate cancer eligible for active surveillance according PRIAS criteria. Urol Int. 2016;96:459–69.CrossRef
40.
go back to reference Porpiglia F, Cantiello F, De Luca S, et al. Multiparametric magnetic resonance imaging and active surveillance: How to better select insignificant prostate cancer? Int J Urol. 2016;23(9):752–7.CrossRef Porpiglia F, Cantiello F, De Luca S, et al. Multiparametric magnetic resonance imaging and active surveillance: How to better select insignificant prostate cancer? Int J Urol. 2016;23(9):752–7.CrossRef
41.
go back to reference de Cobelli O, Terracciano D, Tagliabue E, et al. Predicting pathological features at radical prostatectomy in patients with prostate cancer eligible for active surveillance by multiparametric magnetic resonance imaging. PloS One. 2015;10(10):e0139696.CrossRef de Cobelli O, Terracciano D, Tagliabue E, et al. Predicting pathological features at radical prostatectomy in patients with prostate cancer eligible for active surveillance by multiparametric magnetic resonance imaging. PloS One. 2015;10(10):e0139696.CrossRef
42.
go back to reference Morlacco A, Sharma V, Viers BR, et al. The incremental role of magnetic resonance imaging for prostate cancer staging before radical prostatectomy. Eur Urol. 2017;71:701–4.CrossRef Morlacco A, Sharma V, Viers BR, et al. The incremental role of magnetic resonance imaging for prostate cancer staging before radical prostatectomy. Eur Urol. 2017;71:701–4.CrossRef
43.
go back to reference Fang D, Zhao C, Ren D, et al. Could magnetic resonance imaging help to identify the presence of prostate cancer before initial biopsy? The development of nomogram predicting the outcomes of prostate biopsy in the Chinese population. Ann Surg Oncol. 2016;23:4284–92.CrossRef Fang D, Zhao C, Ren D, et al. Could magnetic resonance imaging help to identify the presence of prostate cancer before initial biopsy? The development of nomogram predicting the outcomes of prostate biopsy in the Chinese population. Ann Surg Oncol. 2016;23:4284–92.CrossRef
Metadata
Title
Contemporary Epstein Criteria with Biopsy-Naïve Multiparametric Magnetic Resonance Imaging to Prevent Incorrect Assignment to Active Surveillance in the PI-RADS Version 2.0 Era
Authors
Yu Fan, MD
Lingyun Zhai, MD
Yisen Meng, MD
Yuke Chen, MD
Shaoshuai Sun, MD
Huihui Wang, MD
Shuai Hu, MD, PhD
Qi Shen, MD, PhD
Yi Liu, MD
Derun Li, MD
Xueru Feng, MD
Qun He, MD, PhD
Xiaoying Wang, MD
Wei Yu, MD
Jie Jin, MD, PhD
Publication date
01-11-2018
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 12/2018
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-018-6720-2

Other articles of this Issue 12/2018

Annals of Surgical Oncology 12/2018 Go to the issue