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. 2019 Apr 25;4(4):CD012663.
doi: 10.1002/14651858.CD012663.pub2.

Prostate MRI, with or without MRI-targeted biopsy, and systematic biopsy for detecting prostate cancer

Frank-Jan H Drost  1 , Daniël F Osses, Daan Nieboer, Ewout W Steyerberg, Chris H Bangma, Monique J Roobol, Ivo G Schoots
Affiliations

Prostate MRI, with or without MRI-targeted biopsy, and systematic biopsy for detecting prostate cancer

Frank-Jan H Drost et al. Cochrane Database Syst Rev. .

Abstract

Background: Multiparametric magnetic resonance imaging (MRI), with or without MRI-targeted biopsy, is an alternative test to systematic transrectal ultrasonography-guided biopsy in men suspected of having prostate cancer. At present, evidence on which test to use is insufficient to inform detailed evidence-based decision-making.

Objectives: To determine the diagnostic accuracy of the index tests MRI only, MRI-targeted biopsy, the MRI pathway (MRI with or without MRI-targeted biopsy) and systematic biopsy as compared to template-guided biopsy as the reference standard in detecting clinically significant prostate cancer as the target condition, defined as International Society of Urological Pathology (ISUP) grade 2 or higher. Secondary target conditions were the detection of grade 1 and grade 3 or higher-grade prostate cancer, and a potential change in the number of biopsy procedures.

Search methods: We performed a comprehensive systematic literature search up to 31 July 2018. We searched CENTRAL, MEDLINE, Embase, eight other databases and one trials register.

Selection criteria: We considered for inclusion any cross-sectional study if it investigated one or more index tests verified by the reference standard, or if it investigated the agreement between the MRI pathway and systematic biopsy, both performed in the same men. We included only studies on men who were biopsy naïve or who previously had a negative biopsy (or a mix of both). Studies involving MRI had to report on both MRI-positive and MRI-negative men. All studies had to report on the primary target condition.

Data collection and analysis: Two reviewers independently extracted data and assessed the risk of bias using the QUADAS-2 tool. To estimate test accuracy, we calculated sensitivity and specificity using the bivariate model. To estimate agreement between the MRI pathway and systematic biopsy, we synthesised detection ratios by performing random-effects meta-analyses. To estimate the proportions of participants with prostate cancer detected by only one of the index tests, we used random-effects multinomial or binary logistic regression models. For the main comparisions, we assessed the certainty of evidence using GRADE.

Main results: The test accuracy analyses included 18 studies overall.MRI compared to template-guided biopsy: Based on a pooled sensitivity of 0.91 (95% confidence interval (CI): 0.83 to 0.95; 12 studies; low certainty of evidence) and a pooled specificity of 0.37 (95% CI: 0.29 to 0.46; 12 studies; low certainty of evidence) using a baseline prevalence of 30%, MRI may result in 273 (95% CI: 249 to 285) true positives, 441 false positives (95% CI: 378 to 497), 259 true negatives (95% CI: 203 to 322) and 27 (95% CI: 15 to 51) false negatives per 1000 men. We downgraded the certainty of evidence for study limitations and inconsistency.MRI-targeted biopsy compared to template-guided biopsy: Based on a pooled sensitivity of 0.80 (95% CI: 0.69 to 0.87; 8 studies; low certainty of evidence) and a pooled specificity of 0.94 (95% CI: 0.90 to 0.97; 8 studies; low certainty of evidence) using a baseline prevalence of 30%, MRI-targeted biopsy may result in 240 (95% CI: 207 to 261) true positives, 42 (95% CI: 21 to 70) false positives, 658 (95% CI: 630 to 679) true negatives and 60 (95% CI: 39 to 93) false negatives per 1000 men. We downgraded the certainty of evidence for study limitations and inconsistency.The MRI pathway compared to template-guided biopsy: Based on a pooled sensitivity of 0.72 (95% CI: 0.60 to 0.82; 8 studies; low certainty of evidence) and a pooled specificity of 0.96 (95% CI: 0.94 to 0.98; 8 studies; low certainty of evidence) using a baseline prevalence of 30%, the MRI pathway may result in 216 (95% CI: 180 to 246) true positives, 28 (95% CI: 14 to 42) false positives, 672 (95% CI: 658 to 686) true negatives and 84 (95% CI: 54 to 120) false negatives per 1000 men. We downgraded the certainty of evidence for study limitations, inconsistency and imprecision.Systemic biopsy compared to template-guided biopsy: Based on a pooled sensitivity of 0.63 (95% CI: 0.19 to 0.93; 4 studies; low certainty of evidence) and a pooled specificity of 1.00 (95% CI: 0.91 to 1.00; 4 studies; low certainty of evidence) using a baseline prevalence of 30%, systematic biopsy may result in 189 (95% CI: 57 to 279) true positives, 0 (95% CI: 0 to 63) false positives, 700 (95% CI: 637 to 700) true negatives and 111 (95% CI: 21 to 243) false negatives per 1000 men. We downgraded the certainty of evidence for study limitations and inconsistency.Agreement analyses: In a mixed population of both biopsy-naïve and prior-negative biopsy men comparing the MRI pathway to systematic biopsy, we found a pooled detection ratio of 1.12 (95% CI: 1.02 to 1.23; 25 studies). We found pooled detection ratios of 1.44 (95% CI 1.19 to 1.75; 10 studies) in prior-negative biopsy men and 1.05 (95% CI: 0.95 to 1.16; 20 studies) in biopsy-naïve men.

Authors' conclusions: Among the diagnostic strategies considered, the MRI pathway has the most favourable diagnostic accuracy in clinically significant prostate cancer detection. Compared to systematic biopsy, it increases the number of significant cancer detected while reducing the number of insignificant cancer diagnosed. The certainty in our findings was reduced by study limitations, specifically issues surrounding selection bias, as well as inconsistency. Based on these findings, further improvement of prostate cancer diagnostic pathways should be pursued.

PubMed Disclaimer

Conflict of interest statement

Frank‐Jan H Drost: none known

Daniel F Osses: none known

Daan Nieboer: none known

Ewout W Steyerberg reports the following relevant financial activities outside the submitted work: receives royalties from Springer for the textbook entitled Clinical Prediction Models

Chris H Bangma: none known

Monique J Roobol: none known

Ivo G Schoots reports the following relevant activities related to the submitted work: a guideline associate panel member of the EAU–ESTRO–ESUR–SIOG Guidelines on Prostate Cancer

Figures

1
1
Clinical pathway flow diagram and study design
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2
Study flow chart
 csPCa: clinically significant prostate cancer; MRI: magnetic resonance imaging; MRI pathway: magnetic resonance imaging with subsequent magnetic resonance imaging‐targeted biopsy; MRI‐TBx: magnetic resonance imaging‐targeted biopsy; SBx: systematic biopsy
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Diagnostic test accuracy of magnetic resonance imaging (MRI) verified by template‐guided biopsy: risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study
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Diagnostic test accuracy of magnetic resonance imaging‐targeted biopsy (MRI‐TBx) in MRI‐positive men: risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study
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Diagnostic test accuracy of the MRI pathway: risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study
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Diagnostic test accuracy of systematic biopsy (SBx): risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study
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Agreement analyses between the MRI pathway and systematic biopsy (SBx): risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study
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Diagnostic test accuracy of MRI for indicating grade 2 and higher prostate cancer. Summary ROC plot of MRI verified by template‐guided biopsy. The 95% confidence region illustrates the uncertainty around the pooled summary point; the 95% prediction region illustrates the heterogeneity
 MRI: magnetic resonance imaging
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Diagnostic test accuracy of MRI‐targeted biopsy for detecting grade 2 and higher prostate cancer Summary ROC plot of MRI‐targeted biopsy (in an MRI‐positive population) verified by template‐guided biopsy. The 95% confidence region illustrates the uncertainty around the pooled summary point; the 95% prediction region illustrates the heterogeneity
 MRI: magnetic resonance imaging
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Diagnostic test accuracy of the MRI pathway for detecting grade 2 and higher prostate cancer Summary ROC plot of the MRI pathway verified by template‐guided biopsy. The 95% confidence region illustrates the uncertainty around the pooled summary point; the 95% prediction region illustrates the heterogeneity
 MRI: magnetic resonance imaging; MRI pathway: MRI with or without MRI‐targeted biopsy
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Test consequence graphic showing results that would be obtained if a hypothetical cohort of 1000 men were tested for prostate cancer using the MRI pathway.
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Diagnostic test accuracy of systematic biopsy for detecting grade 2 and higher prostate cancer Summary ROC plot of systematic biopsy verified by template‐guided biopsy
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Test consequence graphic showing results that would be obtained if a hypothetical cohort of 1000 men were tested for prostate cancer using systematic biopsy.
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Comparison of diagnostic test accuracy between MRI and the MRI pathway for detecting grade 2 and higher prostate cancer. Summary ROC plot of MRI and the MRI pathway verified by template‐guided biopsy
 G: International Society of Urological Pathology grade; MRI: magnetic resonance imaging; MRI pathway: MRI with or without MRI‐targeted biopsy
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Comparison of diagnostic test accuracy between the MRI pathway and systematic biopsy for detecting grade 2 and higher prostate cancer. Summary ROC plot of the MRI pathway versus systematic biopsy, verified by template‐guided biopsy
 G: International Society of Urological Pathology grade; MRI: magnetic resonance imaging; MRI pathway: MRI with or without MRI‐targeted biopsy; SBx: systematic biopsy
16
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MRI‐positivity threshold effect for indicating grade 2 and higher prostate cancer. Summary ROC plot of MRI verified by template‐guided biopsy, with different thresholds for positivity: intermediate (3/5) vs high (4/5)
 G: International Society of Urological Pathology grade; MRI: magnetic resonance imaging
17
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MRI‐positivity threshold effect for indicating grade 3 and higher prostate cancer. Summary ROC plot of MRI verified by template‐guided biopsy, with different thresholds for positivity: intermediate (3/5) vs high (4/5)
 G: International Society of Urological Pathology grade; MRI: magnetic resonance imaging
18
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Forest plots of the agreement analysis (MRI pathway vs systematic biopsy) for detecting grade 2 and higher prostate cancer
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Added value of systematic biopsy plotted against the added value of the MRI pathway per population type in the agreement analysis, for detecting grade 2 and higher prostate cancer
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Diagnostic accuracy of MRI ‐ G = 1.
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Diagnostic accuracy of MRI ‐ G ≥ 1.
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Diagnostic accuracy of MRI ‐ G ≥ 2.
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Diagnostic accuracy of MRI ‐ Sensitivity analysis with composite reference standard (template‐guided biopsy + MRI‐TBx) ‐ G ≥ 2.
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Diagnostic accuracy of TBx ‐ G ≥ 3.
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Diagnostic accuracy of the MRI‐pathway ‐ G = 1.
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Diagnostic accuracy of the MRI‐pathway ‐ G ≥ 1.
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Diagnostic accuracy of the MRI‐pathway ‐ G ≥ 2.
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Diagnostic accuracy of the MRI‐pathway ‐ G ≥ 3.
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Diagnostic accuracy of SBx ‐ G = 1.
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Diagnostic accuracy of SBx ‐ G ≥ 2.
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Diagnostic accuracy of SBx ‐ G ≥ 3.
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MRI‐pathway vs SBx ‐ Negative MRI ‐ Prior‐negative biopsy ‐ G ≥ 3.
See this image and copyright information in PMC

Comment in

  • Editorial Comment.
    Kilpeläinen T, Lahdensuo K, Rannikko A. Kilpeläinen T, et al. J Urol. 2020 Jul;204(1):32. doi: 10.1097/JU.0000000000000757.01. Epub 2020 Apr 7. J Urol. 2020. PMID: 32255755 No abstract available.
  • Editorial Comment.
    Moschini M, Rozet F. Moschini M, et al. J Urol. 2020 Jul;204(1):32. doi: 10.1097/JU.0000000000000757.02. Epub 2020 Apr 7. J Urol. 2020. PMID: 32255756 No abstract available.

References

References to studies included in this review

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Say 2016 {published data only}
    1. Say RK. MRI‐ultrasound fusion targeted biopsy in men with prior negative prostate biopsy for prostate cancer [PhD thesis]. Vol. 2078, New Haven, CT: Yale Medicine Thesis Digital Library, 2016. [elischolar.library.yale.edu/ymtdl/2078]
Thompson 2016 {published and unpublished data}
    1. Thompson JE, Leeuwen PJ, Moses D, Shnier R, Brenner P, Delprado W, et al. The diagnostic performance of multiparametric magnetic resonance imaging to detect significant prostate cancer. Journal of Urology 2016;195(5):1428‐35. - PubMed
Tonttilla 2016 {published and unpublished data}
    1. Tonttila PP, Lantto J, Pääkkö E, Piippo U, Kauppila S, Lammentausta E, et al. Prebiopsy multiparametric magnetic resonance imaging for prostate cancer diagnosis in biopsy‐naïve men with suspected prostate cancer based on elevated prostate‐specific antigen values: results from a randomized prospective blinded controlled trial. European Urology 2016;69(3):419‐25. - PubMed
Tsivian 2017 {published and unpublished data}
    1. Tsivian M, Gupta RT, Tsivian E, Qi P, Mendez MH, Abern MR, et al. Assessing clinically significant prostate cancer: diagnostic properties of multiparametric magnetic resonance imaging compared to three‐dimensional transperineal template mapping histopathology. International Journal of Urology 2017;24(2):137‐43. - PubMed
Van der Leest 2018 {published data only}
    1. Leest MM, Cornel EB, Israël B, Hendriks RJ, Padhani AR, Hoogenboom M, et al. Head‐to‐head comparison of transrectal ultrasound‐guided prostate biopsy versus multiparametric prostate resonance imaging with subsequent magnetic resonance‐guided biopsy in biopsy‐naïve men with elevated prostate‐specific antigen: a large prospective multicenter clinical study. European Urology 23 November 2018 [Epub ahead of print];S0302‐2838(18):30880‐7. [DOI: 10.1016/j.eururo.2018.11.023] - DOI - PubMed

References to studies excluded from this review

Arsov 2015 {published data only}
    1. Arsov C, Rabenalt R, Blondin D, Quentin M, Hiester A, Godehardt E, et al. Prospective randomized trial comparing magnetic resonance imaging (MRI)‐guided in‐bore biopsy to MRI‐ultrasound fusion and transrectal ultrasound‐guided prostate biopsy in patients with prior negative biopsies. European Urology 2015;68(4):713‐20. - PubMed
Baco 2016 {published data only}
    1. Baco E, Rud E, Eri LM, Moen G, Vlatkovic L, Svindland A, et al. A randomized controlled trial to assess and compare the outcomes of two‐core prostate biopsy guided by fused magnetic resonance and transrectal ultrasound images and traditional 12‐core systematic biopsy. European Urology 2016;69(1):149‐56. - PubMed
Boesen 2017b {published data only}
    1. Boesen L, Norgaard N, Logager V, Balslev I, Thomsen HS. Multiparametric MRI in men with clinical suspicion of prostate cancer undergoing repeat biopsy: a prospective comparison with clinical findings and histopathology. Acta Radiologica 2017;59(3):371‐80. - PubMed
Brock 2015 {published data only}
    1. Brock M, Bodman C, Palisaar J, Becker W, Martin‐Seidel P, Noldus J. Detecting prostate cancer a prospective comparison of systematic prostate biopsy with targeted biopsy guided by fused MRI and transrectal ultrasound. Deutsches Ärzteblatt International 2015;112(37):605‐U13. - PMC - PubMed
Fiard 2013 {published data only}
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Haffner 2011 {published data only}
    1. Haffner J, Lemaitre L, Puech P, Haber GP, Leroy X, Jones JS, et al. Role of magnetic resonance imaging before initial biopsy: comparison of magnetic resonance imaging‐targeted and systematic biopsy for significant prostate cancer detection. BJU International 2011;108(8 B):E171‐E8. - PubMed
Hansen 2016b {published data only}
    1. Hansen N, Patruno G, Wadhwa K, Gaziev G, Miano R, Barrett T, et al. Magnetic resonance and ultrasound image fusion supported transperineal prostate biopsy using the Ginsburg protocol: technique, learning points, and biopsy results. European Urology 2016;70(2):332‐40. - PubMed
Kasivisvanathan 2018 {published data only}
    1. Kasivisvanathan V, Rannikko AS, Borghi M, Panebianco V, Mynderse LA, Vaarala MH, et al. MRI‐targeted or standard biopsy for prostate‐cancer diagnosis. New England Journal of Medicine 2018;378:1767‐77. - PMC - PubMed
Komai 2013 {published data only}
    1. Komai Y, Numao N, Yoshida S, Matsuoka Y, Nakanishi Y, Ishii C, et al. High diagnostic ability of multiparametric magnetic resonance imaging to detect anterior prostate cancer missed by transrectal 12‐core biopsy. Journal of Urology 2013;190(3):867‐73. - PubMed
Kuru 2013a {published data only}
    1. Kuru TH, Roethke MC, Seidenader J, Simpfendörfer T, Boxler S, Alammar K, et al. Critical evaluation of magnetic resonance imaging targeted, transrectal ultrasound guided transperineal fusion biopsy for detection of prostate cancer. Journal of Urology 2013;190(4):1380‐6. - PubMed
Numao 2013 {published data only}
    1. Numao N, Yoshida S, Komai Y, Ishii C, Kagawa M, Kijima T, et al. Usefulness of pre‐biopsy multiparametric magnetic resonance imaging and clinical variables to reduce initial prostate biopsy in men with suspected clinically localized prostate cancer. Journal of Urology 2013;190(2):502‐8. - PubMed
Pepe 2015 {published data only}
    1. Pepe P, Garufi A, Priolo G, Pennisi M. Can 3‐tesla pelvic phased‐array multiparametric MRI avoid unnecessary repeat prostate biopsy in patients with PSA < 10 ng/mL?. Clinical Genitourinary Cancer 2015;13(1):e27‐e30. - PubMed
Pepe 2017 {published data only}
    1. Pepe P, Garufi A, Priolo G, Pennisi M. Transperineal versus transrectal MRI/TRUS fusion targeted biopsy: detection rate of clinically significant prostate cancer. Clinical Genitourinary Cancer 2017;15(1):e33‐e6. - PubMed
Porpiglia 2017 {published data only}
    1. Porpiglia F, Manfredi M, Mele F, Cossu M, Bollito E, Veltri A, et al. Diagnostic pathway with multiparametric magnetic resonance imaging versus standard pathway: results from a randomized prospective study in biopsy‐naïve patients with suspected prostate cancer. European Urology 2017;72(2):282‐8. - PubMed
Radtke 2015 {published data only}
    1. Radtke JP, Kuru TH, Boxler S, Alt CD, Popeneciu IV, Huettenbrink C, et al. Comparative analysis of transperineal template saturation prostate biopsy versus magnetic resonance imaging targeted biopsy with magnetic resonance imaging‐ultrasound fusion guidance. Journal of Urology 2015;193(1):87‐94. - PubMed
Simmons 2018 {published data only (unpublished sought but not used)}
    1. Simmons LA, Kanthabalan A, Arya M, Briggs T, Barratt D, Charman SC. Accuracy of transperineal targeted prostate biopsies, both visual‐estimation and image‐fusion for men needing a repeat biopsy in the PICTURE trial. Journal of Urology 2018;200(6):1227‐34. - PubMed
Sonn 2014 {published data only}
    1. Sonn GA, Chang E, Natarajan S, Margolis DJ, MacAiran M, Lieu P, et al. Value of targeted prostate biopsy using magnetic resonance‐ultrasound fusion in men with prior negative biopsy and elevated prostate‐specific antigen. European of Urology 2014;65(4):809‐15. - PMC - PubMed
Thompson 2014 {published data only}
    1. Thompson JE, Moses D, Shnier R, Brenner P, Delprado W, Ponsky L, et al. Multiparametric magnetic resonance imaging guided diagnostic biopsy detects significant prostate cancer and could reduce unnecessary biopsies and over detection: a prospective study. Journal of Urology 2014;192(1):67‐74. - PubMed
Weaver 2016 {published data only}
    1. Weaver JK, Kim EH, Vetter JM, Fowler KJ, Siegel CL, Andriole GL. Presence of magnetic resonance imaging suspicious lesion predicts Gleason 7 or greater prostate cancer in biopsy naïve patients. Urology 2016;88:119‐24. - PubMed
Winther 2017 {published data only}
    1. Winther MD, Balslev I, Boesen L, Logager V, Noergaard N, Thestrup KC, et al. Magnetic resonance imaging‐guided biopsies may improve diagnosis in biopsy naïve men with suspicion of prostate cancer. Danish Medical Journal 2017;64(5):A5355. - PubMed

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