Evidence review for diagnosing and identifying clinically significant prostate cancer

Introduction

This review question aims to capture one of the key themes which prompted early upgrade of the 2014 NICE Guidance CG175: how is the clinical suspicion of prostate cancer best investigated?

Template biopsy must be the most comprehensive test for identifying prostate cancer, but universal application of this diagnostic approach would have significant cost and morbidity implications, as well as placing an impossible strain on health care services. Template biopsy was therefore used as the standard against which the diagnostic accuracy of mpMRI and/or TRUS biopsy were gauged.

Evidence from diagnostic test accuracy studies and from randomised controlled trials was used, as set out in PICO tables 1 and 2. For full protocols please see Appendix A.

Table 1

PICO table –Diagnostic test accuracy studies.

Table 2

PICO table –Randomised control studies.

Methods and process

This evidence review was developed using the methods and process described in Developing NICE guidelines: the manual. Methods specific to this review question are described in the review protocol in appendix A, and the methods section in appendix B.

Declarations of interest were recorded according to NICE’s 2014 and 2018 conflicts of interest policy

This review was conducted as part of a larger update of the NICE Prostate Cancer guideline (CG175).

Clinical evidence

Summary of clinical studies included in the evidence review

Table 3

Summary of studies for diagnosing prostate cancer in people suspected to have prostate cancer (cross-sectional studies).

Table 4

Summary of studies for diagnosing prostate cancer in people suspected to have prostate cancer (randomised control studies).

See appendix E for full evidence tables.

Quality assessment of clinical studies included in the evidence review

See appendix G for full GRADE tables.

Economic evidence

Standard health economics filters were applied to the clinical search strategy for this review question. In total, 802 references were returned, of which 790 could be confidently excluded on screening of titles and abstracts. The remaining 12 studies were reviewed in full text, and 11 were found not to be relevant. This left 1 unique cost–utility analysis.

Summary of studies included in the economic evidence review

Faria et al. (2018) developed a cost-effectiveness model for lifetime health outcomes and costs, using data captured in PROMIS, a paired-cohort diagnostic study (Ahmed et al., 2017), adopting the perspective of the UK NHS and using 2015 prices. Patients at study entry were people at risk of prostate cancer referred to secondary care for further investigation.

The study assessed the performance of 3 tests: multi-parametric magnetic resonance imaging (MP-MRI), trans-rectal ultra-sound biopsy (TRUS) and transperineal mapping biopsy (TPMB). In the economic analysis, the combination of TRUS and TPMB, whichever was most severe, was the reference standard. The model examined 383 diagnostic strategies, based on possible sequences of the 3 tests, 2 pathological definitions of clinically significant prostate cancer (CS PC) and different thresholds of Likert score at which prostate cancer is considered clinically significant using MP-MRI.

A decision tree model was structured to model the diagnostic stage. The long-term stage used a Markov structure to model the lifetime costs and health benefits of people diagnosed with clinically significant (CS), non-clinically significant (NCS) or no cancer (NC), by whether they were correctly classified or not. The Markov model consisted of 2 health states for no cancer: alive or dead, and 3 health states for men with cancer: localised, metastatic and dead.

Diagnostic accuracy data were obtained from PROMIS, if possible, and also identified from other published literature, as diagnostic accuracy data varied according to the diagnostic test position in the sequence and whether it was combined with other test(s). Risk of mortality and progression included in the long-term model were derived from a clinical trial in the US: Prostate Cancer Intervention Versus Observation Trial (PIVOT). Patients misclassified as no cancer were assigned probability of progression or death observed in the watchful waiting arm, whereas data for those correctly diagnosed with cancer were taken from the radical treatment arm. Cases with underlying prostate cancer, misclassified as having no cancer, were not considered for re-testing; thus, they would stay on active surveillance. The cost effectiveness of a strategy was defined based on number of CS cancer detected for a given pound spent in the diagnostic stage, while the long-term cost effectiveness was defined based on the maximum health outcome achieved given the cost.

Health-related utilities were derived from EQ-5D questionnaires collected in PROMIS, where TPM directly affected the health-related quality of life, while TRUS and MP-MRI were assumed to have no effect. Disutility, assigned due to aging and progression for health states in the long-run, were identified in published literature.

When the total expected lifetime cost and effectiveness results of the all 383 strategies were compared with each other, the authors found that only 14 strategies were expected to be cost effective at different values of cost-effectiveness thresholds. The strategy that was found to be optimal (when QALYs are valued at less than £30,000 each) was called “M7 222”:

• all people receive MP-MRI
• people with lesion volume <0.2 cc on MP-MRI and/or assessed by the radiologist as highly likely benign (score 1 on a 5-point Likert scale reflecting probability of malignancy) are judged not to have clinically significant prostate cancer
• people with lesion volume ≥0.2 cc and/or Gleason score ≥3+4, assessed by the radiologist as ≥2 on the Likert scale undergo MRI-targeted TRUS biopsy

  • people with any Gleason ≥3+4 and/or cancer core length ≥4 mm are diagnosed with clinically significant prostate cancer
  • people not meeting these criteria receive a 2^nd MRI-targeted TRUS biopsy

    -

    people with any Gleason ≥3+4 and/or cancer core length ≥4 mm are diagnosed with clinically significant prostate cancer

    -

    people not meeting these criteria are judged not to have clinically significant prostate cancer

• template biopsies are not used in this strategy

This strategy (which was the 2^nd most effective of those simulated) had an ICER of £7,076/QALY compared with the next best strategy. The most effective strategy (P4 2-) was for all people to receive TRUS biopsy, after which anyone with negative findings undergoes template biopsy. However, this strategy was associated with an ICER of £30,084/QALY compared with M7 222.

The results are sensitive to the sensitivity of the 1^st and 2^nd MRI-targeted TRUS and the costs of the test. For example, a reduction in the sensitivity assigned to MRI-targeted TRUS resulted in the cost-effectiveness results favouring strategies beginning with TRUS.

Economic model

This question was not prioritised for economic modelling.

Evidence statements

The evidence statements in these sections are written with reference to the size of the likelihood ratios in the GRADE tables in appendix G, using the interpretation detailed in the methods section on diagnostic test accuracy (Table 6).

The committee’s discussion of the evidence

RQ1. Review protocol for prostate cancer diagnosis in men with suspected prostate (diagnostic cross-sectional studies)

Table

Multiparametric or biparametric MRI alone MRI influenced TRUS biopsy (MRI-targeted and MRI-guided TRUS biopsy)

RQ1a. Review protocol for prostate cancer diagnosis in men with suspected prostate (randomised control studies)

Table

Multiparametric or biparametric MRI alone MRI influenced TRUS biopsy (MRI-targeted and MRI-guided TRUS biopsy)

Incorporating published systematic reviews

For all review questions where a literature search was undertaken looking for a particular study design, systematic reviews containing studies of that design were also included. All included studies from those systematic reviews were screened to identify any additional relevant primary studies not found as part of the initial search.

Evidence of effectiveness of interventions

Diagnostic test accuracy evidence

In this guideline, diagnostic test accuracy (DTA) data are classified as any data in which a feature – be it a symptom, a risk factor, a test result or the output of some algorithm that combines many such features – is observed in some people who have the condition of interest at the time of the test and some people who do not. Such data either explicitly provide, or can be manipulated to generate, a 2x2 classification of true positives and false negatives (in people who, according to the reference standard, truly have the condition) and false positives and true negatives (in people who, according to the reference standard, do not).

The ‘raw’ 2x2 data can be summarised in a variety of ways. Those that were used for decision making in this guideline are as follows:

• Positive likelihood ratios describe how many times more likely positive features are in people with the condition compared to people without the condition. Values greater than 1 indicate that a positive result makes the condition more likely.
  • LR⁺ = (TP/[TP+FN])/(FP/[FP+TN])
• Negative likelihood ratios describe how many times less likely negative features are in people with the condition compared to people without the condition. Values less than 1 indicate that a negative result makes the condition less likely.
  • LR^- = (FN/[TP+FN])/(TN/[FP+TN])
• Sensitivity is the probability that the feature will be positive in a person with the condition.
  • sensitivity = TP/(TP+FN)
• Specificity is the probability that the feature will be negative in a person without the condition.
  • specificity = TN/(FP+TN)

The following schema, adapted from the suggestions of Jaeschke et al. (1994), was used to interpret the likelihood ratio findings from diagnostic test accuracy reviews.

Table 6. Interpretation of likelihood ratios

The schema above has the effect of setting a minimal important difference for positive likelihoods ratio at 2, and a corresponding minimal important difference for negative likelihood ratios at 0.5. Likelihood ratios (whether positive or negative) falling between these thresholds were judged to indicate no meaningful change in the probability of disease.

Search summary

The search strategies are based on the review protocol provided. The MRI/biopsy terms have been taken from the search strategy used in CG175.

Clinical searches

Source searched for this review question:

• Cochrane Database of Systematic Reviews – CDSR (Wiley)
• Cochrane Central Register of Controlled Trials – CENTRAL (Wiley)
• Database of Abstracts of Reviews of Effects – DARE (Wiley)
• Health Technology Assessment Database – HTA (Wiley)
• EMBASE (Ovid)
• MEDLINE (Ovid)
• MEDLINE In-Process (Ovid)

The clinical searches were conducted in January 2018.

The MEDLINE search strategy is presented below. It was translated for use in all other databases.

Table

Study design filters and limits

A diagnostic filter was appended to the review question above. The MEDLINE filter is presented below. It were translated for use in the MEDLINE In-Process and Embase databases.

An English language limit has been applied.

A date limit from 2007 was applied as the committee members were confident we would unlikely find studies on MRI guided biopsy prior to 2007 that reflect current practice.

Animal studies and certain publication types (letters, historical articles, comments, editorials, news and case reports) have been excluded.

Table

Health Economics search strategy

Economic evaluations and quality of life data.

Sources searched:

• NHS Economic Evaluation Database – NHS EED (Wiley) (legacy database)
• Health Technology Assessment (HTA Database)
• EconLit (Ovid)
• Embase (Ovid)
• MEDLINE (Ovid)
• MEDLINE In-Process (Ovid)

Search filters to retrieve economic evaluations and quality of life papers were appended to population search terms in MEDLINE, MEDLINE In-Process and Embase to identify relevant evidence and can be seen below.

An English language limit has been applied.

A date limit from 2007 was applied as the committee members were confident we would unlikely find studies on MRI guided biopsy prior to 2007 that reflect current practice.

Animal studies and certain publication types (letters, historical articles, comments, editorials, news and case reports) have been excluded.

The economic searches were conducted in February 2018.

Health Economics filters

Table

Clinical evidence – Diagnostic Cross sectional studies

Clinical evidence - Randomised control studies

Economic evidence

Clinical evidence tables

Diagnosing prostate cancer in people suspected to have prostate cancer – cross-sectional studies

TRUS biopsy compared to Transperineal Template Biopsy – Sensitivity and specificity for clinically significant cancer

TRUS biopsy compared to Transperineal Template Biopsy - Likelihood ratios for clinically significant cancer

Diagnosing prostate cancer in people suspected to have prostate cancer – randomised control studies

MRI influenced Biopsy versus TRUS biopsy – Proportion of people with clinically significant cancer

Proportion of people with clinically insignificant cancer

People who avoided biopsy

The forest plot shows the odds and not odds ratio – this was converted to the equivalent proportion for easy interpretation and this equates to 0.27 (0.22, 0.31)

Health related quality of life EQ 5D description

Investigator reported adverse events related to the interventions

Patient reported 30 day post intervention complications

Diagnosing prostate cancer in people suspected to have prostate cancer (diagnostic cross-sectional studies)

Multiparametric MRI

TRUS biopsy

Diagnosing prostate cancer – randomised control trials

MRI influenced prostate biopsy (Targeted biopsy) versus prostate biopsy

Clinical studies

RQ1 Diagnostic cross-sectional studies

Table

Only included population with negative TRUS/MRI results Only included people with overall MRI score ≥3

Randomised control studies

Table

Study does not contain any relevant interventions Not a randomised controlled trial

Economic studies

Table

Clinical studies - included - cross-sectional studies

• Ahmed Hu, El-Shater Bosaily A, Brown Lc, Gabe R, Kaplan R, Parmar Mk, Collaco-Moraes Y, Ward K, Hindley Rg, Freeman A, Kirkham Ap, Oldroyd R, Parker C, and Emberton M (2017) Diagnostic accuracy of multi-parametric MRI and TRUS biopsy in prostate cancer (PROMIS): a paired validating confirmatory study. Lancet (no pagination), [PubMed: 28110982]

• Nafie S, Mellon Jk, Dormer Jp, and Khan Ma (2014)The role of transperineal template prostate biopsies in prostate cancer diagnosis in biopsy naive men with PSA less than 20 ng ml-1. Prostate cancer and prostatic diseases 17(2), 170–173 [PubMed: 24590360]

Clinical studies - included - randomised control studies

• Kasivisvanathan V, Rannikko AS, Borghi M, Panebianco V, Mynderse LA, Vaarala MH, Briganti A, Budaus L, Hellawell G, Hindley RG, Roobol MJ, Eggener S, Ghei M, Villers A, Bladou F, Villeirs GM, Virdi J, Boxler S, Robert G, Singh PB, Venderink W, Hadaschik BA, Ruffion A, Hu JC, Margolis D, Crouzet S, Klotz L, Taneja SS, Pinto P, Gill I, Allen C, Giganti F, Freeman A, Morris S, Punwani S, Williams NR, Brew-Graves C, Deeks J, Takwoingi Y, Emberton M, and Moore CM. (2018). MRI-Targeted or Standard Biopsy for Prostate-Cancer Diagnosis.. The New England journal of medicine, 378(19), pp.1767–1777. [PMC free article: PMC9084630] [PubMed: 29552975]

• Porpiglia F, Mele F, Manfredi M, Luca S, Checcucci E, Garrou D, Cattaneo G, Amparore D, Bollito E, Russo F, Gned D, Pascale A, Cirillo S, and Fiori C (2017) Standard prostate biopsy Versus MRI-fusion biopsy: results after two years of a prospective randomized study. Anticancer research. Conference: 27th annual meeting of the Italian society of uro-oncology, and siuro 2017. Italy 37(4), 2148

Clinical studies – excluded – cross-sectional studies

• A’Amar O M, Liou L, Rodriguez-Diaz E, De Las Morenas, A, and Bigio I J (2013) Comparison of elastic scattering spectroscopy with histology in ex vivo prostate glands: Potential application for optically guided biopsy and directed treatment. Lasers in Medical Science 28(5), 1323–1329 [PubMed: 23247663]

• Abd-Alazeez Mohamed, Ahmed Hashim U, Arya Manit, Allen Clare, Dikaios Nikolaos, Freeman Alex, Emberton Mark, and Kirkham Alex (2014) Can multiparametric magnetic resonance imaging predict upgrading of transrectal ultrasound biopsy results at more definitive histology?. Urologic oncology 32(6), 741–7 [PubMed: 24981993]

• Abd-Alazeez M, Kirkham A, Ahmed H U, Arya M, Anastasiadis E, Charman S C, Freeman A, and Emberton M (2014) Performance of multiparametric MRI in men at risk of prostate cancer before the first biopsy: A paired validating cohort study using template prostate mapping biopsies as the reference standard. Prostate Cancer and Prostatic Diseases 17(1), 40–46 [PMC free article: PMC3954968] [PubMed: 24126797]

• Abd-Alazeez M, Ramachandran N, Dikaios N, Ahmed H U, Emberton M, Kirkham A, Arya M, Taylor S, Halligan S, and Punwani S (2015) Multiparametric MRI for detection of radiorecurrent prostate cancer: Added value of apparent diffusion coefficient maps and dynamic contrast-enhanced images. Prostate Cancer and Prostatic Diseases 18(2), 128–136 [PubMed: 25644248]

• Abdi H, Pourmalek F, Zargar H, Walshe T, Harris A C, Chang S D, Eddy C, So A I, Gleave M E, Machan L, Goldenberg S L, and Black P C (2015) Multiparametric magnetic resonance imaging enhances detection of significant tumor in patients on active surveillance for prostate cancer. Urology 85(2), 423–428 [PubMed: 25623709]

• Abdollah F, Novara G, Briganti A, Scattoni V, Raber M, Roscigno M, Suardi N, Gallina A, Artibani W, Ficarra V, Cestari A, Guazzoni G, Rigatti P, and Montorsi F (2011) Trans-rectal versus trans-perineal saturation rebiopsy of the prostate: Is there a difference in cancer detection rate?. Urology 77(4), 921–925 [PubMed: 21131034]

• Abedi I, Tavakkoli M B, Rabbani M, Jabbari K, Sirous M, and Far G Y (2017) Multiparametric magnetic resonance imaging of prostate cancer: Association of quantitative magnetic resonance parameters with histopathologic findings. Iranian Journal of Radiology 14(3), e37844

• Abouassaly R, Lane B R, and Jones J S (2008) Staging Saturation Biopsy in Patients with Prostate Cancer on Active Surveillance Protocol. Urology 71(4), 573–577 [PubMed: 18387385]

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• Arumainayagam N, Ahmed H U, Moore C M, Freeman A, Allen C, Sohaib S A, Kirkham A, Van Der Meulen, J, and Emberton M (2013) Multiparametric MR imaging for detection of clinically significant prostate cancer: A validation cohort study with transperineal template prostate mapping as the reference standard. Radiology 268(3), 761–769 [PubMed: 23564713]

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• Barrett T, and Haider M A (2017) The emerging role of MRI in prostate cancer active surveillance and ongoing challenges. American Journal of Roentgenology 208(1), 131–139 [PubMed: 27726415]

• Barzell W E, and Melamed M R (2007) Appropriate Patient Selection in the Focal Treatment of Prostate Cancer: The Role of Transperineal 3-Dimensional Pathologic Mapping of the Prostate-A 4-Year Experience. Urology 70(6 SUPPL. 1), S27–S35 [PubMed: 18194708]

• Barzell W E, Melamed M R, Cathcart P, Moore C M, Ahmed H U, and Emberton M (2012) Identifying candidates for active surveillance: An evaluation of the repeat biopsy strategy for men with favorable risk prostate cancer. Journal of Urology 188(3), 762–767 [PubMed: 22818143]

• Becker A S, Cornelius A, Reiner C S, Stocker D, Ulbrich E J, Barth B K, Mortezavi A, Eberli D, and Donati O F (2017) Direct comparison of PI-RADS version 2 and version 1 regarding interreader agreement and diagnostic accuracy for the detection of clinically significant prostate cancer. European Journal of Radiology 94, 58–63 [PubMed: 28941761]

• Bittner N, Merrick G S, Butler W M, Bennett A, and Galbreath R W (2013) Incidence and pathological features of prostate cancer detected on transperineal template guided mapping biopsy after negative transrectal ultrasound guided biopsy. Journal of Urology 190(2), 509–514 [PubMed: 23416641]

• Bjurlin M A, Mendhiratta N, Wysock J S, and Taneja S S (2016) Multiparametric MRI and targeted prostate biopsy: Improvements in cancer detection, localization, and risk assessment. Central European Journal of Urology 69(1), 9–18 [PMC free article: PMC4846729] [PubMed: 27123316]

• Bladou F, Fogaing C, Levental M, Aronson S, Alameldin M, and Anidjar M (2017) Transrectal ultrasound-guided biopsy for prostate cancer detection: Systematic and/or magnetic-resonance imaging-targeted. Canadian Urological Association Journal 11(9), E330–E337 [PMC free article: PMC5798436] [PubMed: 29382454]

• Boesen L, Noergaard N, Chabanova E, Logager V, Balslev I, Mikines K, and Thomsen H S (2015) Early experience with multiparametric magnetic resonance imaging-targeted biopsies under visual transrectal ultrasound guidance in patients suspicious for prostate cancer undergoing repeated biopsy. Scandinavian Journal of Urology 49(1), 25–34 [PubMed: 24922550]

• Borkowetz A, Platzek I, Toma M, Laniado M, Baretton G, Froehner M, Koch R, Wirth M, and Zastrow S (2015) Comparison of systematic transrectal biopsy to transperineal magnetic resonance imaging/ultrasound-fusion biopsy for the diagnosis of prostate cancer. BJU International 116(6), 873–879 [PubMed: 25523210]

• Borkowetz A, Zastrow S, Platzek I, Toma M, Froehner M, Koch R, and Wirth M (2015) Assessment of tumour aggressiveness in tranperineal mri/ultrasound-fusion biopsy in comparison to transrectal systematic prostate biopsy. Journal of urology. 193(4 suppl. 1), e596

• Bosco C, Cozzi G, Kinsella J, Bianchi R, Acher P, Challacombe B, Popert R, Brown C, George G, Van Hemelrijck, M, and Cahill D (2016) Confirmatory biopsy for the assessment of prostate cancer in men considering active surveillance: Reference centre experience. ecancermedicalscience 10, 633 [PMC free article: PMC4854226] [PubMed: 27170833]

• Brock Marko, von Bodman, Christian, Palisaar Juri, Becker Wolfgang, Martin-Seidel Philipp, and Noldus Joachim (2015) Detecting Prostate Cancer. Deutsches Arzteblatt international 112(37), 605–11 [PMC free article: PMC4581108] [PubMed: 26396046]

• Brown L C, Gabe R, Hindley R G, Ahmed H U, Bosaily A E. S, Parker C, Cooper C, Oldroyd R, Kaplan R, Brown L, Rhian Gabe, Collaco-Moraes Y, Adusei, Ward, Stewart S, Mulrenan K T. C, Gardner H, Diaz-Montana C, Coyle C, Sculpher M, Faria R, David Guthrie, Chester J, Cowan R, Jewitt M, Ahmed H, Coe J, El-Shater Bosaily, A, Emberton M, Freeman A, Hung M, Jameson C, Kirkham A, Punwani S, Scott R, Hindley R, Edwards A, El-Mahallawi H, Peppercorn D, Smith J, Thrower A, Winkler M, Ansu K, Barwick T, Edwards S, Honeyfield L, Qazi N, Statton B, Stewart V, Temple E, Burns-Cox N, Burn P, Gordon K, Routley H, Maccormick A, Paterson D, Henderson A, Bernsten E, Casey R, Day D, Ghosh S, James J, McMillan P J, Russell G, Persad R, Ash-Miles J, Elmahdy M, Pandian S, Shiridzinomwa C, Sohail M, Treasure A, Ghei M, Conteh V, Harbin L, Katz R, Kumaradevan J, Trinidade A, Verjee A, Dudderidge T, Smart J, Rosario D, Catto J, Selem F, Shergill I, and Agarwal S (2015) PROMIS - Prostate MR imaging study: A paired validating cohort study evaluating the role of multi-parametric MRI in men with clinical suspicion of prostate cancer. Contemporary Clinical Trials 42, 26–40 [PMC free article: PMC4460714] [PubMed: 25749312]

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• Chen J, Yi X L, Jiang L X, Wang R, Zhao J G, Li Y H, and Hu B (2015) 3-tesla magnetic resonance imaging improves the prostate cancer detection rate in transrectral ultrasound-guided biopsy. Experimental and Therapeutic Medicine 9(1), 207–212 [PMC free article: PMC4247284] [PubMed: 25452804]

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• Dikaios N, Alkalbani J, Sidhu H S, Fujiwara T, Abd-Alazeez M, Kirkham A, Allen C, Ahmed H, Emberton M, Freeman A, Halligan S, Taylor S, Atkinson D, and Punwani S (2014) Logistic regression model for diagnosis of transition zone prostate cancer on multi-parametric MRI. European Radiology 25(2), 523–532 [PMC free article: PMC4291517] [PubMed: 25226842]

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• El-Shater Bosaily, A, Parker C, Brown L C, Gabe R, Hindley R G, Kaplan R, Emberton M, Ahmed H U, and Group Promis (2015) PROMIS-Prostate MR imaging study: A paired validating cohort study evaluating the role of multi-parametric MRI in men with clinical suspicion of prostate cancer. Contemporary clinical trials 42, 26–40 [PMC free article: PMC4460714] [PubMed: 25749312]

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• Pessoa R R, Viana P C, Mattedi R L, Guglielmetti G B, Cordeiro M D, Coelho R F, Nahas W C, and Srougi M (2017) Value of 3-Tesla multiparametric magnetic resonance imaging and targeted biopsy for improved risk stratification in patients considered for active surveillance. BJU International 119(4), 535–542 [PubMed: 27500389]

• Pokharel S S, Patel N U, Garg K, La Rosa, F G, Arangua P, Jones C, and Crawford E D (2014) Multi-parametric MRI findings of transitional zone prostate cancers: correlation with 3-dimensional transperineal mapping biopsy. Abdominal Imaging, [PubMed: 25038718]

• Raber M, Scattoni V, Gallina A, Freschi M, De Almeyda, E P, Girolamo V D, Montorsi F, and Rigatti P (2012) Does the transrectal ultrasound probe influence prostate cancer detection in patients undergoing an extended prostate biopsy scheme? Results of a large retrospective study. BJU International 109(5), 672–677 [PubMed: 21871054]

• Radtke J P, Kuru T H, Boxler S, Alt C D, Popeneciu I V, Huettenbrink C, Klein T, Steinemann S, Bergstraesser C, Roethke M, Roth W, Schlemmer H P, Hohenfellner M, and Hadaschik B A (2015) Comparative Analysis of Transperineal Template Saturation Prostate Biopsy Versus Magnetic Resonance Imaging Targeted Biopsy with Magnetic Resonance Imaging-Ultrasound Fusion Guidance. Journal of Urology 193(1), 87–94 [PubMed: 25079939]

• Radtke Jan P, Kuru Timur H, Boxler Silvan, Alt Celine D, Popeneciu Ionel V, Huettenbrink Clemens, Klein Tilman, Steinemann Sarah, Bergstraesser Claudia, Roethke Matthias, Roth Wilfried, Schlemmer Heinz-Peter, Hohenfellner Markus, and Hadaschik Boris A (2015) Comparative analysis of transperineal template saturation prostate biopsy versus magnetic resonance imaging targeted biopsy with magnetic resonance imaging-ultrasound fusion guidance. The Journal of urology 193(1), 87–94 [PubMed: 25079939]

• Reis Leonardo O, Sanches Brunno C. F, de Mendonca, Gustavo Borges, Silva Daniel M, Aguiar Tiago, Menezes Ocivaldo P, and Billis Athanase (2015) Gleason underestimation is predicted by prostate biopsy core length. World journal of urology 33(6), 821–6 [PubMed: 25084976]

• Robertson N L, Hu Y, Ahmed H U, Freeman A, Barratt D, and Emberton M (2014) Prostate cancer risk inflation as a consequence of image-targeted biopsy of the prostate: A computer simulation study. European Urology 65(3), 628–634 [PMC free article: PMC3925797] [PubMed: 23312572]

• Russo F, Regge D, Armando E, Giannini V, Vignati A, Mazzetti S, Manfredi M, Bollito E, Correale L, and Porpiglia F (2015) Detection of prostate cancer index lesions with multiparametric magnetic resonance imaging (mp-MRI) using whole-mount histological sections as the reference standard. BJU International, [PubMed: 26198404]

• Salami S S, Vira M A, Turkbey B, Fakhoury M, Yaskiv O, Villani R, Ben-Levi E, and Rastinehad A R (2014) Multiparametric magnetic resonance imaging outperforms the prostate cancer prevention trial risk calculator in predicting clinically significant prostate cancer. Cancer 120(18), 2876–2882 [PubMed: 24917122]

• Scheltema M J, Chang J I, van den Bos, W, Bohm M, Delprado W, Gielchinsky I, de Reijke, T M, de la Rosette, J J, Siriwardana A R, Shnier R, and Stricker P D (2017) Preliminary Diagnostic Accuracy of Multiparametric Magnetic Resonance Imaging to Detect Residual Prostate Cancer Following Focal Therapy with Irreversible Electroporation. European Urology Focus, [PubMed: 29102671]

• Schimmoller L, Blondin D, Arsov C, Rabenalt R, Albers P, Antoch G, and Quentin M (2016) MRI-guided in-bore biopsy: Differences between prostate cancer detection and localization in primary and secondary biopsy settings. American Journal of Roentgenology 206(1), 92–99 [PubMed: 26700339]

• Schimmoller L, Quentin M, Blondin D, Dietzel F, Hiester A, Schleich C, Thomas C, Rabenalt R, Gabbert H E, Albers P, Antoch G, and Arsov C (2016) Targeted MRI-guided prostate biopsy: are two biopsy cores per MRI-lesion required?. European Radiology 26(11), 3858–3864 [PubMed: 26920391]

• Schoots I G, Roobol M J, Nieboer D, Bangma C H, Steyerberg E W, and Hunink M G. M (2015) Magnetic Resonance Imaging-targeted Biopsy May Enhance the Diagnostic Accuracy of Significant Prostate Cancer Detection Compared to Standard Transrectal Ultrasound-guided Biopsy: A Systematic Review and Meta-analysis. European Urology 68(3), 438–450 [PubMed: 25480312]

• Scott S, Samaratunga H, Chabert C, Breckenridge M, and Gianduzzo T (2015) Is transperineal prostate biopsy more accurate than transrectal biopsy in determining final Gleason score and clinical risk category? A comparative analysis. BJU International 116(Supplement 3), 26–30 [PubMed: 26260531]

• Sheikh N, Wei C, Szewczyk-Bieda M, Campbell A, Memon S, Lang S, and Nabi G (2017) Combined T2 and diffusion-weighted MR imaging with template prostate biopsies in men suspected with prostate cancer but negative transrectal ultrasound-guided biopsies. World journal of urology 35(2), 213–220 [PMC free article: PMC5272897] [PubMed: 27236302]

• Shen P F, Zhu Y C, Wei W R, Li Y Z, Yang J, Li Y T, Li D M, Wang J, and Zeng H (2012) The results of transperineal versus transrectal prostate biopsy: A systematic review and meta-analysis. Asian Journal of Andrology 14(2), 310–315 [PMC free article: PMC3735101] [PubMed: 22101942]

• Shin T, Smyth T B, Ukimura O, Ahmadi N, de Castro Abreu, A L, Ohe C, Oishi M, Mimata H, and Gill I S (2018) Diagnostic accuracy of a five-point Likert scoring system for magnetic resonance imaging (MRI) evaluated according to results of MRI/ultrasonography image-fusion targeted biopsy of the prostate. BJU International 121(1), 77–83 [PMC free article: PMC6192038] [PubMed: 28749070]

• Shoji S, Hiraiwa S, Endo J, Hashida K, Tomonaga T, Nakano M, Sugiyama T, Tajiri T, Terachi T, and Uchida T (2015) Manually controlled targeted prostate biopsy with real-time fusion imaging of multiparametric magnetic resonance imaging and transrectal ultrasound: An early experience. International Journal of Urology 22(2), 173–178 [PubMed: 25316213]

• Shoji S, Hiraiwa S, Ogawa T, Kawakami M, Nakano M, Hashida K, Sato Y, Hasebe T, Uchida T, and Tajiri T (2017) Accuracy of real-time magnetic resonance imaging-transrectal ultrasound fusion image-guided transperineal target biopsy with needle tracking with a mechanical position-encoded stepper in detecting significant prostate cancer in biopsy-naive men. International Journal of Urology 24(4), 288–294 [PubMed: 28222486]

• Shukla-Dave A, and Hricak H (2014) Role of MRI in prostate cancer detection. NMR in Biomedicine 27(1), 16–24 [PubMed: 23495081]

• Sim J, Schieda N, Robertson Sj, Breau Rh, Morash C, Belanger Ec, and Flood Ta (2017) Evaluation of tumor morphologies at radical prostatectomy in high risk gleason score >9 prostate cancer diagnosed at trus-guided biopsy. Laboratory investigation. Conference: 106th annual meeting of the united states and canadian academy of pathology, and USCAP 2017. United states 97, 260a

• Simmons Lam, Kanthabalan A, Arya M, Briggs T, Barratt D, Charman Sc, Freeman A, Gelister J, Hawkes D, Hu Y, Jameson C, McCartan N, Moore Cm, Punwani S, Ramachandran N, Meulen J, Emberton M, and Ahmed Hu (2017) The PICTURE study: diagnostic accuracy of multiparametric MRI in men requiring a repeat prostate biopsy. British journal of cancer (no pagination), [PMC free article: PMC5418442] [PubMed: 28350785]

• Sivaraman A, Sanchez-Salas R, Ahmed H U, Barret E, Cathala N, Mombet A, Uriburu Pizarro, F, Carneiro A, Doizi S, Galiano M, Rozet F, Prapotnich D, and Cathelineau X (2015) Clinical utility of transperineal template-guided mapping biopsy of the prostate after negative magnetic resonance imaging-guided transrectal biopsy. Urologic Oncology: Seminars and Original Investigations 33(7), 329 [PubMed: 25957713]

• Taira A V, Merrick G S, Bennett A, Andreini H, Taubenslag W, Galbreath R W, Butler W M, Bittner N, and Adamovich E (2013) Transperineal template-guided mapping biopsy as a staging procedure to select patients best suited for active surveillance. American Journal of Clinical Oncology: Cancer Clinical Trials 36(2), 116–120 [PubMed: 22307210]

• Takuma K, Mikio S, Masashi I, Nobufumi U, Hiromi H, Yushi H, and Yoshiyuki K (2012) Transperineal ultrasound-guided multiple core biopsy using template for patients with one or more previous negative biopsies: comparison with systematic 10-core biopsy. Urology 80(3 suppl. 1), S306–s307

• Taneja Samir S (2017) Re: Diagnostic Accuracy of Multi-Parametric MRI and TRUS Biopsy in Prostate Cancer (PROMIS): A Paired Validating Confirmatory Study. The Journal of urology 198(1), 101–102 [PubMed: 28618668]

• Tay Kae Jack, Cheng Christopher W. S, Lau Weber K. O, Khoo James, Thng Choon Hua, and Kwek Jin Wei (2017) Focal Therapy for Prostate Cancer with In-Bore MR-guided Focused Ultrasound: Two-Year Follow-up of a Phase I Trial-Complications and Functional Outcomes. Radiology 285(2), 620–628 [PubMed: 28654336]

• Taymoorian K, Thomas A, Slowinski T, Khiabanchian M, Stephan C, Lein M, Deger S, Lenk S, Loening S A, and Fischer T (2007) Transrectal broadband-Doppler sonography with intravenous contrast medium administration for prostate imaging and biopsy in men with an elevated PSA value and previous negative biopsies. Anticancer Research 27(6 C), 4315–4320 [PubMed: 18214038]

• Tewes Susanne, Peters Inga, Tiemeyer Ansgar, Peperhove Matti, Hartung Dagmar, Pertschy Stefanie, Kuczyk Markus A, Wacker Frank, and Hueper Katja (2017) Evaluation of MRI/Ultrasound Fusion-Guided Prostate Biopsy Using Transrectal and Transperineal Approaches. BioMed research international 2017, 2176471 [PMC free article: PMC5637860] [PubMed: 29094042]

• Thestrup Karen Cecilie Duus, Logager Vibeke, Baslev Ingerd, Moller Jakob M, Hansen Rasmus Hvass, and Thomsen Henrik S (2016) Biparametric versus multiparametric MRI in the diagnosis of prostate cancer. Acta radiologica open 5(8), 2058460116663046 [PMC free article: PMC4990814] [PubMed: 27583170]

• Thompson J E, Moses D, Shnier R, Brenner P, Delprado W, Ponsky L, Pulbrook M, Bohm M, Haynes A M, Hayen A, and Stricker P D (2014) 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 192(1), 67–74 [PubMed: 24518762]

• Thompson J, Shnier R, Moses D, Brenner P, Delprado W, Tran M, Ponsky L, Boehm M, Hayen A, and Stricker P (2015) Prospective study of pre-biopsy multiparametric magnetic resonance imaging (MP-MRI) compared to transperineal template mapping biopsy (TTMB) for detection of clinically significant prostate cancer: is it accurate enough to guide selection of men for biopsy?. Journal of urology. 193(4 suppl. 1), e959

• Thompson J E, Hayen A, Landau A, Haynes A M, Kalapara A, Ischia J, Matthews J, Frydenberg M, and Stricker P D (2015) Medium-term oncological outcomes for extended vs saturation biopsy and transrectal vs transperineal biopsy in active surveillance for prostate cancer. BJU International 115(6), 884–891 [PubMed: 24989062]

• Thompson J E, Van Leeuwen, P J, Moses D, Shnier R, Brenner P, Delprado W, Pulbrook M, Bohm M, Haynes A M, Hayen A, and Stricker P D (2016) The diagnostic performance of multiparametric magnetic resonance imaging to detect significant prostate cancer. Journal of Urology 195(5), 1428–1435 [PubMed: 26529298]

• Thompson J E, and Stricker P D (2017) Diagnostic accuracy of multi-parametric MRI and transrectal ultrasound-guided biopsy in prostate cancer. The Lancet 389(10071), 767–768 [PubMed: 28126331]

• Ting F, Van Leeuwen, P J, Thompson J, Shnier R, Moses D, Delprado W, and Stricker P D (2016) Assessment of the Performance of Magnetic Resonance Imaging/Ultrasound Fusion Guided Prostate Biopsy against a Combined Targeted Plus Systematic Biopsy Approach Using 24-Core Transperineal Template Saturation Mapping Prostate Biopsy. Prostate Cancer 2016, 3794738 [PMC free article: PMC4884827] [PubMed: 27293898]

• Toner L, Weerakoon M, Bolton D M, Ryan A, Katelaris N, and Lawrentschuk N (2015) Magnetic resonance imaging for prostate cancer: Comparative studies including radical prostatectomy specimens and template transperineal biopsy. Prostate International 3(4), 107–114 [PMC free article: PMC4685231] [PubMed: 26779455]

• Tonttila Pp, Lantto J, Pääkkö E, Piippo U, Kauppila S, Lammentausta E, Ohtonen P, and Vaarala Mh (2016) Prebiopsy Multiparametric Magnetic Resonance Imaging for Prostate Cancer Diagnosis in Biopsy-naive Men with Suspected Prostate Cancer Based on Elevated Prostate-specific Antigen Values: results from a Randomized Prospective Blinded Controlled Trial. European urology 69(3), 419–425 [PubMed: 26033153]

• Tsivian M, Gupta R T, Tsivian E, Qi P, Mendez M H, Abern M R, Tay K J, and Polascik T J (2017) Assessing clinically significant prostate cancer: Diagnostic properties of multiparametric magnetic resonance imaging compared to three-dimensional transperineal template mapping histopathology. International Journal of Urology 24(2), 137–143 [PubMed: 27859637]

• Tran G N, Leapman M S, Nguyen H G, Cowan J E, Shinohara K, Westphalen A C, and Carroll P R (2017) Magnetic Resonance Imaging-Ultrasound Fusion Biopsy During Prostate Cancer Active Surveillance. European Urology 72(2), 275–281 [PubMed: 27595378]

• Valerio M, McCartan N, Freeman A, Punwani S, Emberton M, and Ahmed H U (2015) Visually directed vs. software-based targeted biopsy compared to transperineal template mapping biopsy in the detection of clinically significant prostate cancer. Urologic Oncology: Seminars and Original Investigations 33(10), 424 [PubMed: 26195330]

• Van Vugt, H A, Kranse R, Steyerberg E W, Van Der Poel, H G, Busstra M, Kil P, Oomens E H, De Jong, I J, Bangma C H, and Roobol M J (2012) Prospective validation of a risk calculator which calculates the probability of a positive prostate biopsy in a contemporary clinical cohort. European Journal of Cancer 48(12), 1809–1815 [PubMed: 22406050]

• Volkin D, Turkbey B, Hoang A N, Rais-Bahrami S, Yerram N, Walton-Diaz A, Nix J W, Wood B J, Choyke P L, and Pinto P A (2014) Multiparametric magnetic resonance imaging (MRI) and subsequent MRI/ultrasonography fusion-guided biopsy increase the detection of anteriorly located prostate cancers. BJU International 114(6), E43–E49 [PMC free article: PMC5613950] [PubMed: 24712649]

• Walton Diaz, A, Shakir N A, George A K, Rais-Bahrami S, Turkbey B, Rothwax J T, Stamatakis L, Hong C W, Siddiqui M M, Okoro C, Raskolnikov D, Su D, Shih J, Han H, Parnes H L, Merino M J, Simon R M, Wood B J, Choyke P L, and Pinto P A (2015) Use of serial multiparametric magnetic resonance imaging in the management of patients with prostate cancer on active surveillance. Urologic Oncology: Seminars and Original Investigations 33(5), 202e1–202e7 [PMC free article: PMC6663486] [PubMed: 25754621]

• Wang R, Wang H, Zhao C, Hu J, Jiang Y, Tong Y, Liu T, Huang R, and Wang X (2015) Evaluation of multiparametric magnetic resonance imaging in detection and prediction of prostate cancer. PLoS ONE 10(6), e0130207 [PMC free article: PMC4466371] [PubMed: 26067423]

• Wang Z, Schaefferkoetter J, Kok T, Stephenson M, Schneider E, Niaf E, Totman J, Townsend D, Thamboo T, and Chiong E (2017) Primary prostate cancer imaging with MP-MRI, PET/CT and PET/MRI with focus on localisation and grading. BJU international. Conference: individualised urological treatment, and UROFAIR 2017. Singapore 119, 4

• Weaver J K, Kim E H, Vetter J M, Fowler K J, Siegel C L, and Andriole G L (2016) Presence of magnetic resonance imaging suspicious lesion predicts gleason 7 or greater prostate cancer in biopsy-naive patients. Urology 88, 119–124 [PubMed: 26545849]

• Wegelin Olivier, Henken Kirsten R, Somford Diederik M, Breuking Frans A. M, Bosch Ruud J, van Swol, Christiaan F P, van Melick, and Harm H E (2016) An Ex Vivo Phantom Validation Study of an MRI-Transrectal Ultrasound Fusion Device for Targeted Prostate Biopsy. Journal of endourology 30(6), 685–91 [PubMed: 26886510]

• Westhoff N, Siegel F P, Hausmann D, Polednik M, von Hardenberg, J, Michel M S, and Ritter M (2017) Precision of MRI/ultrasound-fusion biopsy in prostate cancer diagnosis: an ex vivo comparison of alternative biopsy techniques on prostate phantoms. World journal of urology 35(7), 1015–1022 [PubMed: 27830373]

• Winter M, Garcia C, Bergersen P, Woo H, and Chalasani V (2013) A systematic review with metaanalysis of transrectal prostate biopsy versus transperineal prostate biopsy for detecting prostate cancer. BJU international. 112, 22

• Wu L M, Yao Q Y, Zhu J, Lu Q, Suo S T, Liu Q, Xu J R, Chen X X, Haacke E M, and Hu J (2017) T2* mapping combined with conventional T2-weighted image for prostate cancer detection at 3.0T MRI: A multi-observer study. Acta Radiologica 58(1), 114–120 [PubMed: 26917785]

• Wysock Js, Rosenkrantz Ab, Huang Wc, Stifelman Md, Lepor H, Deng Fm, Melamed J, and Taneja Ss (2014) A prospective, blinded comparison of magnetic resonance (MR) imaging-ultrasound fusion and visual estimation in the performance of MR-targeted prostate biopsy: the PROFUS trial. European urology 66(2), 343–351 [PubMed: 24262102]

• Yaxley A J, Yaxley J W, Thangasamy I A, Ballard E, and Pokorny M R (2017) Comparison between target magnetic resonance imaging (MRI) in-gantry and cognitively directed transperineal or transrectal-guided prostate biopsies for Prostate Imaging-Reporting and Data System (PI-RADS) 3-5 MRI lesions. BJU International 120(Supplement 3), 43–50 [PubMed: 28749035]

• Yoo Sangjun, Hong Jun Hyuk, Byun Seok-Soo, Lee Ji Youl, Chung Byung Ha, and Kim Choung-Soo (2017) Is suspicious upstaging on multiparametric magnetic resonance imaging useful in improving the reliability of Prostate Cancer Research International Active Surveillance (PRIAS) criteria? Use of the K-CaP registry. Urologic oncology 35(7), 459.e7–459.e13 [PubMed: 28476529]

• Zhang Q, Wang W, Yang R, Zhang G, Zhang B, Li W, Huang H, and Guo H (2015) Free-hand transperineal targeted prostate biopsy with real-time fusion imaging of multiparametric magnetic resonance imaging and transrectal ultrasound: single-center experience in China. International Urology and Nephrology, [PubMed: 25820744]

• Zhang Q, Wang W, Zhang B, Shi J, Fu Y, Li D, Guo S, Zhang S, Huang H, Jiang X, Zhou W, and Guo H (2017) Comparison of free-hand transperineal MP-MRI/TRUS fusion-guided biopsy with transperineal 12-core systematic biopsy for the diagnosis of prostate cancer: a single-center prospective study in China. International Urology and Nephrology 49(3), 439–448 [PubMed: 28005230]

Clinical studies – excluded – randomised control studies

• Arsov C, Hiester A, Schimmoller L, Quentin M, Blondin D, Godehardt E, Antoch G, Albers P, and Rabenalt R (2015) A prospective randomized study comparing MR-guided in-bore versus MRI/ultrasound fusionguided prostate biopsy in patients with prior tumor-negative TRUS biopsy. European urology, and supplements. 14(2), e761

• Arsov C, Rabenalt R, Blondin D, Quentin M, Hiester A, Godehardt E, Gabbert He, Becker N, Antoch G, Albers P, and Schimmöller L (2015) 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 68(4), 713–720 [PubMed: 26116294]

• Arsov Christian, Rabenalt Robert, Quentin Michael, Hiester Andreas, Blondin Dirk, Albers Peter, Antoch Gerald, and Schimmoller Lars (2016) Comparison of patient comfort between MR-guided in-bore and MRI/ultrasound fusion-guided prostate biopsies within a prospective randomized trial. World journal of urology 34(2), 215–20 [PubMed: 26055645]

• Baco E, Rud E, Eri Lm, Moen G, Vlatkovic L, Svindland A, Eggesbo Hb, and Ukimura O (2016) 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 69(1), 149–156 [PubMed: 25862143]

• Baur Alexander D. J, Henkel Thomas, Johannsen Manfred, Speck Thomas, Weisbach Lothar, Hamm Bernd, and Konig Frank (2017) A prospective study investigating the impact of multiparametric MRI in biopsy-naive patients with clinically suspected prostate cancer: The PROKOMB study. Contemporary clinical trials 56, 46–51 [PubMed: 28279782]

• Cam Kamil, Sener Murat, Kayikci Ali, Akman Yavuz, and Erol Ali (2008) Combined periprostatic and intraprostatic local anesthesia for prostate biopsy: a double-blind, placebo controlled, randomized trial. The Journal of urology 180(1), 141–5 [PubMed: 18485414]

• Chae Y, Kim Y-J, Kim T, Yun Sj, Lee S-C, and Kim W-J (2009) The comparison between transperineal and transrectal ultrasound-guided prostate needle biopsy. Korean journal of urology 50(2), 119–124

• Choi Hy, Park Jw, Park Sy, Lee Hm, Jeon Ss, Seo Si, and Park Bk (2011) Prospective evaluation of 3T magnetic resonance imaging performed prior to an initial transrectal ultrasound-guided biopsy in the detection of prostate cancer. International journal of urology 18(5), 398–399

• Cicione Antonio, Cantiello Francesco, De Nunzio, Cosimo, Tubaro Andrea, and Damiano Rocco (2012) Prostate biopsy quality is independent of needle size: a randomized single-center prospective study. Urologia internationalis 89(1), 57–60 [PubMed: 22738882]

• Davuluri Meena, and Loeb Stacy (2015) The Comparison of Magnetic Resonance Image-Guided Targeted Biopsy Versus Standard Template Saturation Biopsy in the Detection of Prostate Cancer. Reviews in urology 17(2), 110–1 [PMC free article: PMC4857905] [PubMed: 27222650]

• Dell’Oglio P, Stabile A, Gandaglia G, Brembilla G, Maga T, Cristel G, Kinzikeeva E, Losa A, Esposito A, Cardone G, Cobelli F, Maschio A, Gaboardi F, Montorsi F, and Briganti A (2017) Inclusion of mpMRI into the European Randomized study of Screening for Prostate Cancer (ERSPC) risk calculator: a new proposal to improve the accuracy of prostate cancer detection. European urology, supplements. Conference: 32nd annual european association of urology congress, and EAU 2017. United kingdom 16(3), e420–e421

• (2016) Diagnostic performance of power doppler and ultrasound contrast agents in early imaging-based diagnosis of organ-confined prostate cancer: is it possible to spare cores with contrast-guided biopsy?. European journal of radiology 85(10), 1778–1785 [PubMed: 27666616]

• (2015) Diagnostic Yield and Complications Using a 20 Gauge Prostate Biopsy Needle versus a Standard 18 Gauge Needle: a Randomized Controlled Study. Urology journal. 12 (5) (pp 2329–2333), and 2015. Date of publication: 01 sep 2015., [PubMed: 26571315]

• DiBianco J M, Mullins J K, and Allaway M (2016) Ultrasound Guided, Freehand Transperineal Prostate Biopsy: An Alternative to the Transrectal Approach. Urology Practice 3(2), 134–140

• Fiard G, Hohn N, Descotes Jl, Rambeaud Jj, Troccaz J, and Long Ja (2013) Targeted MRI-guided prostate biopsies for the detection of prostate cancer: initial clinical experience with real-time 3-dimensional transrectal ultrasound guidance and magnetic resonance/transrectal ultrasound image fusion. Urology 81(6), 1372–1378 [PubMed: 23540865]

• Garcia C, Winter M, Bergersen P, Woo H, and Chalasani V (2016) Transperineal versus transrectal prostate biopsy in prostate cancer detection: a systematic review with meta-analysis. BJU international. 117, 38

• Garcia C, Winter M, Bergersen P, Woo H, and Chalasani V (2016) Does transperineal prostate biopsy reduce complications compared with transrectal biopsy? A systematic review and metaanalysis of randomised controlled trials. BJU international. 117, 68–69

• Gayet Maudy, van der Aa, Anouk, Beerlage Harrie P, Schrier Bart Ph, Mulders Peter F. A, and Wijkstra Hessel (2016) The value of magnetic resonance imaging and ultrasonography (MRI/US)-fusion biopsy platforms in prostate cancer detection: a systematic review. BJU international 117(3), 392–400 [PubMed: 26237632]

• Grenabo Bergdahl A, Wilderäng U, Aus G, Carlsson S, Damber Je, Frånlund M, Geterud K, Khatami A, Socratous A, Stranne J, Hellström M, and Hugosson J (2016) Role of Magnetic Resonance Imaging in Prostate Cancer Screening: a Pilot Study Within the Göteborg Randomised Screening Trial. European urology 70(4), 566–573 [PMC free article: PMC4958033] [PubMed: 26724840]

• Grummet Jeremy, Pepdjonovic Lana, Huang Sean, Anderson Elliot, and Hadaschik Boris (2017) Transperineal vs. transrectal biopsy in MRI targeting. Translational andrology and urology 6(3), 368–375 [PMC free article: PMC5503965] [PubMed: 28725578]

• Guo Lh, Wu R, Xu Hx, Xu Jm, Wu J, Wang S, Bo Xw, and Liu Bj (2015) Comparison between Ultrasound Guided Transperineal and Transrectal Prostate Biopsy: a Prospective, Randomized, and Controlled Trial. Scientific reports 5, 16089 [PMC free article: PMC4630643] [PubMed: 26526558]

• Guo Le-Hang, Wu Rong, Xu Hui-Xiong, Xu Jun-Mei, Wu Jian, Wang Shuai, Bo Xiao-Wan, and Liu Bo-Ji (2015) Comparison between Ultrasound Guided Transperineal and Transrectal Prostate Biopsy: A Prospective, Randomized, and Controlled Trial. Scientific reports 5, 16089 [PMC free article: PMC4630643] [PubMed: 26526558]

• Halpern Ej, Gomella Lg, Forsberg F, McCue Pa, and Trabulsi Ej (2012) Contrast enhanced transrectal ultrasound for the detection of prostate cancer: a randomized, double-blind trial of dutasteride pretreatment. Journal of urology 188(5), 1739–1745 [PMC free article: PMC5942221] [PubMed: 22998915]

• Hara Ryoei, Jo Yoshimasa, Fujii Tomohiro, Kondo Norio, Yokoyoma Teruhiko, Miyaji Yoshiyuki, and Nagai Atsushi (2008) Optimal approach for prostate cancer detection as initial biopsy: prospective randomized study comparing transperineal versus transrectal systematic 12-core biopsy. Urology 71(2), 191–5 [PubMed: 18308081]

• Hove A, Savoie Ph, Maurin C, Brunelle S, Gravis G, Salem N, and Walz J (2014) Comparison of image-guided targeted biopsies versus systematic randomized biopsies in the detection of prostate cancer: a systematic literature review of well-designed studies (Provisional abstract). Database of Abstracts of Reviews of Effects (2), 847–858 [PubMed: 24919965]

• Kasivisvanathan V, Arya M, Ahmed Hu, Moore Cm, and Emberton M (2015) A randomized controlled trial to investigate magnetic resonance imaging-targeted biopsy as an alternative diagnostic strategy to transrectal ultrasound-guided prostate biopsy in the diagnosis of prostate cancer. Urologic oncology: seminars and original investigations 33(3), 156–157 [PubMed: 25573054]

• Kasivisvanathan V, Jichi F, Klotz L, Villers A, Taneja Ss, Punwani S, Freeman A, Emberton M, and Moore Cm (2017) A multicentre randomised controlled trial assessing whether MRI-targeted biopsy is non-inferior to standard transrectal ultrasound guided biopsy for the diagnosis of clinically significant prostate cancer in men without prior biopsy: a study protocol. BMJ open 7(10) (no pagination), [PMC free article: PMC5706484] [PubMed: 29025845]

• Klotz Lh, Loblaw A, Chin J, Fleshner Ne, Kebabdjian M, Pond G, and Haider M (2017) Magnetic resonance imaging-targeted vs. systematic biopsies in men on active surveillance: results of a prospective, randomized Canadian Urology Research Consortium trial. Canadian urological association journal. Conference: 72nd annual meeting of the canadian urological association. Canada 11(6 Supplement 4), S173

• Leitao T, Rodrigues T, Soares C, Silva R, Garcia R, Martinho D, Romao A, Sandul A, Mendonca T, Pereira S, Varela J, and Lopes T (2011) A prospective randomized trial of prostate biopsy protocols comparing the vienna nomogram and a standard 10-core biopsy scheme. Urology. 78(3 suppl. 1), S302

• Leitao Tito Palmela, Alfarelos Joana, Rodrigues Teresa, Pereira E Silva, Ricardo, Garcia Rodrigo Miguel, Martinho David, Sandul Anatoliy, Mendonca Tiago, Pereira Sergio, and Lopes Tome Matos (2017) A Prospective Randomized Trial Comparing the Vienna Nomogram and a Ten-Core Prostate Biopsy Protocol: Effect on Cancer Detection Rate. Clinical genitourinary cancer 15(1), 117–121 [PubMed: 27436153]

• Lenherr O, Fayyazi A, Lahme S, and Liske P (2013) Real-time-elastography (RTE): its detection rate compared to multiple core biopsy and an evaluation of psa and prostate volume as predictors. Journal of urology. 189(4 suppl. 1), e904

• Mitterberger M, Horninger W, Pelzer A, Strasser H, Bartsch G, Moser P, Halpern Ej, Gradl J, Aigner F, Pallwein L, and Frauscher F (2007) A prospective randomized trial comparing contrast-enhanced targeted versus systematic ultrasound guided biopsies: impact on prostate cancer detection. Prostate 67(14), 1537–1542 [PubMed: 17705242]

• Panebianco V, Sciarra A, Ciccariello M, Lisi D, Bernardo S, Cattarino S, Gentile V, and Passariello R (2010) Role of magnetic resonance spectroscopic imaging ([1H]MRSI) and dynamic contrast-enhanced MRI (DCE-MRI) in identifying prostate cancer foci in patients with negative biopsy and high levels of prostate-specific antigen (PSA). La Radiologia medica 115(8), 1314–29 [PubMed: 20852963]

• Panebianco V, Barchetti F, Sciarra A, Ciardi A, Indino El, Papalia R, Gallucci M, Tombolini V, Gentile V, and Catalano C (2015) Multiparametric magnetic resonance imaging vs. standard care in men being evaluated for prostate cancer: a randomized study. Urologic oncology 33(1), 17.e1–17.e7 [PubMed: 25443268]

• Park Bk, Park Jw, Park Sy, Kim Ck, Lee Hm, Jeon Ss, Seo Si, Jeong Bc, and Choi Hy (2011) Prospective evaluation of 3-T MRI performed before initial transrectal ultrasound-guided prostate biopsy in patients with high prostate-specific antigen and no previous biopsy. AJR. American journal of roentgenology 197(5), W876–81 [PubMed: 22021535]

• Park Byung Kwan, Park Jong Wook, Park Seo Yong, Kim Chan Kyo, Lee Hyun Moo, Jeon Seong Soo, Seo Seong Il, Jeong Byong Chang, and Choi Han Yong (2011) Prospective evaluation of 3-T MRI performed before initial transrectal ultrasound-guided prostate biopsy in patients with high prostate-specific antigen and no previous biopsy. AJR. American journal of roentgenology 197(5), W876–81 [PubMed: 22021535]

• Porpiglia Francesco, Manfredi Matteo, Mele Fabrizio, Cossu Marco, Bollito Enrico, Veltri Andrea, Cirillo Stefano, Regge Daniele, Faletti Riccardo, Passera Roberto, Fiori Cristian, De Luca, and Stefano (2017) Diagnostic Pathway with Multiparametric Magnetic Resonance Imaging Versus Standard Pathway: Results from a Randomized Prospective Study in Biopsy-naive Patients with Suspected Prostate Cancer. European urology 72(2), 282–288 [PubMed: 27574821]

• Porpiglia F, Mele F, Manfredi M, Luca S, Checcucci E, Bertolo R, Garrou D, Cattaneo G, Amparore D, Bollito E, Russo F, Gned D, Pascale A, Cirillo S, and Fiori C (2017) A prospective randomized study comparing standard prostate biopsy and a new diagnostic path with MRI and fusion biopsy: results after two years. European urology, supplements. Conference: 32nd annual european association of urology congress, and EAU 2017. United kingdom 16(3), e869–e870

• Sciarra A, Panebianco V, Cattarino S, Busetto Gm, Berardinis E, Ciccariello M, Gentile V, and Salciccia S (2012) Multiparametric magnetic resonance imaging of the prostate can improve the predictive value of the urinary prostate cancer antigen 3 test in patients with elevated prostate-specific antigen levels and a previous negative biopsy. BJU international 110(11), 1661–1665 [PubMed: 22564540]

• Shah Taimur Tariq, To Wilson King Lim, and Ahmed Hashim Uddin (2017) Magnetic resonance imaging in the early detection of prostate cancer and review of the literature on magnetic resonance imaging-stratified clinical pathways. Expert review of anticancer therapy 17(12), 1159–1168 [PubMed: 28933973]

• Singh S, Dorairajan Ln, Manikandan R, Sreerag Ks, Sunil K, Kant Du, and Tepukiel Z (2017) Comparison of infective complications in transperineal versus transrectal ultrasound guided prostatic biopsy in patients suspected to have prostate cancer. Indian journal of urology. Conference: 50th annual conference of urological society of india, and USICON 2017. India 33(Supplement 1) (no pagination),

• Takenaka A, Hara R, Ishimura T, Fujii T, Jo Y, Nagai A, and Fujisawa M (2008) A prospective randomized comparison of diagnostic efficacy between transperineal and transrectal 12-core prostate biopsy. Prostate cancer and prostatic diseases 11(2), 134–8 [PubMed: 17533394]

• Takuma K, Mikio S, Masashi I, Nobufumi U, Hiromi H, Yushi H, and Yoshiyuki K (2012) Transperineal ultrasound-guided multiple core biopsy using template for patients with one or more previous negative biopsies: comparison with systematic 10-core biopsy. Urology 80(3 suppl. 1), S306–s307

• Taverna Gianluigi, Bozzini Giorgio, Grizzi Fabio, Seveso Mauro, Mandressi Alberto, Balzarini Luca, Mrakic Federica, Bono Pietro, De Franceco, Oliviero, Buffi NicoloMaria, Lughezzani Giovanni, Lazzeri Massimo, Casale Paolo, and Guazzoni Giorgio Ferruccio (2016) Endorectal multiparametric 3-tesla magnetic resonance imaging associated with systematic cognitive biopsies does not increase prostate cancer detection rate: a randomized prospective trial. World journal of urology 34(6), 797–803 [PubMed: 26481226]

• Thompson J, Shnier R, Moses D, Brenner P, Delprado W, Tran M, Ponsky L, Boehm M, Hayen A, and Stricker P (2015) Prospective study of pre-biopsy multiparametric magnetic resonance imaging (MPMRI) compared to transperineal template mapping biopsy (TTMB) for detection of clinically significant prostate cancer: is it accurate enough to guide selection of men for biopsy?. Journal of urology. 193(4 suppl. 1), e959

• Tonttila Pp, Lantto J, Pääkkö E, Piippo U, Kauppila S, Lammentausta E, Ohtonen P, and Vaarala Mh (2016) Prebiopsy Multiparametric Magnetic Resonance Imaging for Prostate Cancer Diagnosis in Biopsy-naive Men with Suspected Prostate Cancer Based on Elevated Prostate-specific Antigen Values: results from a Randomized Prospective Blinded Controlled Trial. European urology 69(3), 419–425 [PubMed: 26033153]

• van Hove, A, Savoie P H, Maurin C, Brunelle S, Gravis G, Salem N, and Walz J (2014) Comparison of image-guided targeted biopsies versus systematic randomized biopsies in the detection of prostate cancer: a systematic literature review of well-designed studies. World journal of urology 32(4), 847–858 [PubMed: 24919965]

• Wegelin O, Melick H, Somford D, Bosch R, Kummer A, Vreuls W, and Barentsz J (2016) An interim analysis of the FUTURE trial; A RCT on three techniques of target prostate biopsy based on MR imaging. Comparison of detection rates of (significant) prostate cancer. European urology, and supplements. Conference: 8th european multidisciplinary meeting on urological cancers. Italy 15(13), e1555–e1556

• Winter M, Garcia C, Bergersen P, Woo H, and Chalasani V (2013) A systematic review with metaanalysis of transrectal prostate biopsy versus transperineal prostate biopsy for detecting prostate cancer. BJU international. 112, 22

• Xie L-P, Wang X, Zheng X-Y, Liu B, Li J-F, and Wang S (2017) A randomized controlled trial to assess and compare the outcomes of AIUS-CT guided biopsy, transrectal ultrasound guided 12-core systematic biopsy, and mpMRI assisted 12-core systematic biopsy. European urology, supplements. Conference: 32nd annual european association of urology congress, and EAU 2017. United Kingdom 16(3), e865–e866

Economic studies – included

• Faria R, Soares MO, Spackman E, Ahmed HU, Brown LC, Kaplan R, Emberton M, Sculpher MJ. Optimising the diagnosis of prostate cancer in the era of multiparametric magnetic resonance imaging: a cost-effectiveness analysis based on the Prostate MR Imaging Study (PROMIS). European urology. 2018 Jan 1;73(1):23–30. [PMC free article: PMC5718727] [PubMed: 28935163]

Economic studies – excluded

• Venderink W, Govers TM, de Rooij M, Fütterer JJ, Sedelaar JM. Cost-effectiveness comparison of imaging-guided prostate biopsy techniques: systematic transrectal ultrasound, direct in-bore MRI, and image fusion. American Journal of Roentgenology. 2017 May;208(5):1058–63. [PubMed: 28225639]

• Willis SR, van der Meulen J, Valerio M, Miners A, Ahmed HU, Emberton M. A review of economic evaluations of diagnostic strategies using imaging in men at risk of prostate cancer. Current opinion in urology. 2015 Nov 1;25(6):483–9. [PubMed: 26372036]

• Pahwa S, Schiltz NK, Ponsky LE, Lu Z, Griswold MA, Gulani V. Cost-effectiveness of MR imaging–guided strategies for detection of prostate cancer in biopsy-naive men. Radiology. 2017 May 17;285(1):157–66. [PMC free article: PMC5621719] [PubMed: 28514203]

• Loeb S, Zhou Q, Siebert U, Rochau U, Jahn B, Mühlberger N, Carter HB, Lepor H, Braithwaite RS. Active surveillance versus watchful waiting for localized prostate cancer: a model to inform decisions. European urology. 2017 Dec 1;72(6):899–907. [PMC free article: PMC5694372] [PubMed: 28844371]

• Gordon LG, James R, Tuffaha HW, Lowe A, Yaxley J. Cost‐effectiveness analysis of multiparametric MRI with increased active surveillance for low‐risk prostate cancer in Australia. Journal of Magnetic Resonance Imaging. 2017 May 1;45(5):1304–15. [PubMed: 27726240]

• de Rooij M, Crienen S, Witjes JA, Barentsz JO, Rovers MM, Grutters JP. Cost-effectiveness of magnetic resonance (MR) imaging and MR-guided targeted biopsy versus systematic transrectal ultrasound–guided biopsy in diagnosing prostate cancer: a modelling study from a health care perspective. European urology. 2014 Sep 1;66(3):430–6. [PubMed: 24377803]

• Cerantola Y, Dragomir A, Tanguay S, Bladou F, Aprikian A, Kassouf W. Cost-effectiveness of multiparametric magnetic resonance imaging and targeted biopsy in diagnosing prostate cancer. InUrologic Oncology: Seminars and Original Investigations 2016 Mar 1 (Vol. 34, No. 3, pp. 119–e1). Elsevier. [PubMed: 26602178]

• Mowatt G, Scotland G, Boachie C, Cruickshank M, Ford JA, Fraser C, Kurban L, Lam TB, Padhani AR, Royle J, Scheenen TW. The diagnostic accuracy and cost-effectiveness of magnetic resonance spectroscopy and enhanced magnetic resonance imaging techniques in aiding the localisation of prostate abnormalities for biopsy: a systematic review and economic evaluation. Health technology assessment. 2013. [PMC free article: PMC4781459] [PubMed: 23697373]

• Hövels AM, Heesakkers RA, Adang EM, Barentsz JO, Jager GJ, Severens JL. Cost-effectiveness of MR lymphography for the detection of lymph node metastases in patients with prostate cancer. Radiology. 2009 Sep;252(3):729–36. [PubMed: 19717752]

• Roth JA, Ramsey SD, Carlson JJ. Cost-effectiveness of a biopsy-based 8-protein prostate cancer prognostic assay to optimize treatment decision making in gleason 3+ 3 and 3+ 4 early stage prostate cancer. The oncologist. 2015 Dec 1;20(12):1355–64. [PMC free article: PMC4679086] [PubMed: 26482553]

• Nicholson A, Mahon J, Boland A, Beale S, Dwan K, Fleeman N, Hockenhull J, Dundar Y. The clinical effectiveness and cost-effectiveness of the PROGENSA (R) prostate cancer antigen 3 assay and the Prostate Health Index in the diagnosis of prostate cancer: a systematic review and economic evaluation. Health Technol Assess. 2015 Oct 1;19(87):1–92. [PMC free article: PMC4780983] [PubMed: 26507078]