World Journal of Urology

, Volume 32, Issue 4, pp 847–858

Comparison of image-guided targeted biopsies versus systematic randomized biopsies in the detection of prostate cancer: a systematic literature review of well-designed studies

  • Antoine van Hove
  • Pierre-Henri Savoie
  • Charlotte Maurin
  • Serge Brunelle
  • Gwenaëlle Gravis
  • Naji Salem
  • Jochen Walz
Topic Paper

Abstract

Objective

The clinical utility of image-targeted biopsies can only be judged by a comparison of the current standard of systematic 10–12 core biopsy schemes. The aim of this review was to gather the current evidence in favor of or against targeted biopsies in the detection of prostate cancer based on well-designed, controlled studies, in order to draw clinical relevant conclusions.

Subjects/patients and methods

A systematic literature review was performed addressing studies that compared the prostate cancer detection rates of targeted and systematic biopsy schemes using the imaging techniques of elastography, contrast-enhanced ultrasound, histoscanning and multiparametric MRI. Only well-designed, controlled studies were included and the results summarized.

Results

All imaging techniques are associated with varying results regarding better or poorer detection rates relative to systematic biopsies. No technique provides a clear trend in favor of or against image-targeted biopsies. In almost all studies, the combination of targeted and systematic biopsies provided sometimes a substantial, increase in the detection rate relative to systematic biopsies alone. MRI-targeted biopsies show no advantage in the initial biopsy setting, whereas in the repeat biopsy setting improvements in the detection rates are often observed relative to systemic biopsies.

Conclusion

Based on well-designed, controlled studies no clear advantage of targeted biopsies over the current standard of systematic biopsies can be observed. Therefore, targeted biopsies cannot replace systematic biopsies in the diagnosis of prostate cancer. In all indications, the combination of systematic and targeted biopsy schemes provides the highest detection rate.

Keywords

Prostate cancer Diagnosis MRI Contrast enhanced ultrasound Elastography Histoscanning Targeted biopsy Randomized biopsy 

References

  1. 1.
    Heidenreich A, Bastian PJ, Bellmunt J, Bolla M, Joniau S, van der Kwast T, Mason M, Matveev V, Wiegel T, Zattoni F, Mottet N (2014) EAU guidelines on prostate cancer. Part 1: screening, diagnosis, and local treatment with curative intent—update 2013. Eur Urol 65(1):124–137. doi:10.1016/j.eururo.2013.09.046 PubMedCrossRefGoogle Scholar
  2. 2.
    Pallwein L, Mitterberger M, Struve P, Horninger W, Aigner F, Bartsch G, Gradl J, Schurich M, Pedross F, Frauscher F (2007) Comparison of sonoelastography guided biopsy with systematic biopsy: impact on prostate cancer detection. Eur Radiol 17(9):2278–2285. doi:10.1007/s00330-007-0606-1 PubMedCrossRefGoogle Scholar
  3. 3.
    Puech P, Rouviere O, Renard-Penna R, Villers A, Devos P, Colombel M, Bitker MO, Leroy X, Mege-Lechevallier F, Comperat E, Ouzzane A, Lemaitre L (2013) Prostate cancer diagnosis: multiparametric MR-targeted biopsy with cognitive and transrectal US-MR fusion guidance versus systematic biopsy—prospective multicenter study. Radiology 268(2):461–469. doi:10.1148/radiol.13121501 PubMedCrossRefGoogle Scholar
  4. 4.
    Mitterberger MJ, Aigner F, Horninger W, Ulmer H, Cavuto S, Halpern EJ, Frauscher F (2010) Comparative efficiency of contrast-enhanced colour Doppler ultrasound targeted versus systematic biopsy for prostate cancer detection. Eur Radiol 20(12):2791–2796. doi:10.1007/s00330-010-1860-1 PubMedCrossRefGoogle Scholar
  5. 5.
    Hamann MF, Hamann C, Schenk E, Al-Najar A, Naumann CM, Junemann KP (2013) Computer-aided (histoscanning) biopsies versus conventional transrectal ultrasound-guided prostate biopsies: do targeted biopsy schemes improve the cancer detection rate? Urology 81(2):370–375. doi:10.1016/j.urology.2012.08.072 PubMedCrossRefGoogle Scholar
  6. 6.
    Loch T (2007) Computerized transrectal ultrasound (C-TRUS) of the prostate: detection of cancer in patients with multiple negative systematic random biopsies. World J Urol 25(4):375–380. doi:10.1007/s00345-007-0181-8 PubMedCrossRefGoogle Scholar
  7. 7.
    Walz J, Loch T, Salomon G, Wijkstra H (2013) Imaging of the prostate. Urologe A 52(4):490–496. doi:10.1007/s00120-012-3103-3 PubMedCrossRefGoogle Scholar
  8. 8.
    Moore CM, Robertson NL, Arsanious N, Middleton T, Villers A, Klotz L, Taneja SS, Emberton M (2013) Image-guided prostate biopsy using magnetic resonance imaging-derived targets: a systematic review. Eur Urol 63(1):125–140. doi:10.1016/j.eururo.2012.06.004 PubMedCrossRefGoogle Scholar
  9. 9.
    Frauscher F, Klauser A, Volgger H, Halpern EJ, Pallwein L, Steiner H, Schuster A, Horninger W, Rogatsch H, Bartsch G (2002) Comparison of contrast enhanced color Doppler targeted biopsy with conventional systematic biopsy: impact on prostate cancer detection. J Urol 167(4):1648–1652PubMedCrossRefGoogle Scholar
  10. 10.
    Brock M, von Bodman C, Palisaar RJ, Loppenberg B, Sommerer F, Deix T, Noldus J, Eggert T (2012) The impact of real-time elastography guiding a systematic prostate biopsy to improve cancer detection rate: a prospective study of 353 patients. J Urol 187(6):2039–2043PubMedCrossRefGoogle Scholar
  11. 11.
    Pinto PA, Chung PH, Rastinehad AR, Baccala AA Jr, Kruecker J, Benjamin CJ, Xu S, Yan P, Kadoury S, Chua C, Locklin JK, Turkbey B, Shih JH, Gates SP, Buckner C, Bratslavsky G, Linehan WM, Glossop ND, Choyke PL, Wood BJ (2011) Magnetic resonance imaging/ultrasound fusion guided prostate biopsy improves cancer detection following transrectal ultrasound biopsy and correlates with multiparametric magnetic resonance imaging. J Urol 186(4):1281–1285. doi:10.1016/j.juro.2011.05.078 PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Syme DB, Corcoran NM, Bouchier-Hayes DM, Costello AJ (2006) Hope springs eternal: cavernosal nerve regeneration. BJU Int 97(1):17–21PubMedCrossRefGoogle Scholar
  13. 13.
    Sonn GA, Natarajan S, Margolis DJ, MacAiran M, Lieu P, Huang J, Dorey FJ, Marks LS (2013) Targeted biopsy in the detection of prostate cancer using an office based magnetic resonance ultrasound fusion device. J Urol 189(1):86–91. doi:10.1016/j.juro.2012.08.095 PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Siddiqui MM, Rais-Bahrami S, Truong H, Stamatakis L, Vourganti S, Nix J, Hoang AN, Walton-Diaz A, Shuch B, Weintraub M, Kruecker J, Amalou H, Turkbey B, Merino MJ, Choyke PL, Wood BJ, Pinto PA (2013) Magnetic resonance imaging/ultrasound-fusion biopsy significantly upgrades prostate cancer versus systematic 12-core transrectal ultrasound biopsy. Eur Urol 64(5):713–719. doi:10.1016/j.eururo.2013.05.059 PubMedCrossRefGoogle Scholar
  15. 15.
    Hambrock T, Somford DM, Hoeks C, Bouwense SA, Huisman H, Yakar D, van Oort IM, Witjes JA, Futterer JJ, Barentsz JO (2010) Magnetic resonance imaging guided prostate biopsy in men with repeat negative biopsies and increased prostate specific antigen. J Urol 183(2):520–527. doi:10.1016/j.juro.2009.10.022 PubMedCrossRefGoogle Scholar
  16. 16.
    Hambrock T, Hoeks C, Hulsbergen-van de Kaa C, Scheenen T, Futterer J, Bouwense S, van Oort I, Schroder F, Huisman H, Barentsz J (2012) Prospective assessment of prostate cancer aggressiveness using 3-T diffusion-weighted magnetic resonance imaging-guided biopsies versus a systematic 10-core transrectal ultrasound prostate biopsy cohort. Eur Urol 61(1):177–184. doi:10.1016/j.eururo.2011.08.042 PubMedCrossRefGoogle Scholar
  17. 17.
    Grabski B, Baeurle L, Loch A, Wefer B, Paul U, Loch T (2011) Computerized transrectal ultrasound of the prostate in a multicenter setup (C-TRUS-MS): detection of cancer after multiple negative systematic random and in primary biopsies. World J Urol 29(5):573–579PubMedCrossRefGoogle Scholar
  18. 18.
    Habchi H, Bratan F, Paye A, Pagnoux G, Sanzalone T, Mege-Lechevallier F, Crouzet S, Colombel M, Rabilloud M, Rouviere O (2014) Value of prostate multiparametric magnetic resonance imaging for predicting biopsy results in first or repeat biopsy. Clin Radiol 69(3):e120–e128. doi:10.1016/j.crad.2013.10.018 PubMedCrossRefGoogle Scholar
  19. 19.
    Natarajan S, Marks LS, Margolis DJ, Huang J, Macairan ML, Lieu P, Fenster A (2011) Clinical application of a 3D ultrasound-guided prostate biopsy system. Urol Oncol 29(3):334–342. doi:10.1016/j.urolonc.2011.02.014 PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Aigner F, Pallwein L, Junker D, Schafer G, Mikuz G, Pedross F, Mitterberger MJ, Jaschke W, Halpern EJ, Frauscher F (2010) Value of real-time elastography targeted biopsy for prostate cancer detection in men with prostate specific antigen 1.25 ng/ml or greater and 4.00 ng/ml or less. J Urol 184(3):913–917. doi:10.1016/j.juro.2010.05.026 PubMedCrossRefGoogle Scholar
  21. 21.
    Ganzer R, Brandtner A, Wieland WF, Fritsche HM (2012) Prospective blinded comparison of real-time sonoelastography targeted versus randomised biopsy of the prostate in the primary and re-biopsy setting. World J Urol 30(2):219–223. doi:10.1007/s00345-011-0679-y PubMedCrossRefGoogle Scholar
  22. 22.
    Salomon G, Drews N, Autier P, Beckmann A, Heinzer H, Hansen J, Michl U, Schlomm T, Haese A, Steuber T, Graefen M, Becker A (2014) Incremental detection rate of prostate cancer by real-time elastography targeted biopsies in combination with a conventional 10-core biopsy in 1024 consecutive patients. BJU Int 113(4):548–553. doi:10.1111/bju.12517 PubMedCrossRefGoogle Scholar
  23. 23.
    Halpern EJ, Gomella LG, Forsberg F, McCue PA, Trabulsi EJ (2012) Contrast enhanced transrectal ultrasound for the detection of prostate cancer: a randomized, double-blind trial of dutasteride pretreatment. J Urol 188(5):1739–1745PubMedCrossRefGoogle Scholar
  24. 24.
    Linden RA, Trabulsi EJ, Forsberg F, Gittens PR, Gomella LG, Halpern EJ (2007) Contrast enhanced ultrasound flash replenishment method for directed prostate biopsies. J Urol 178(6):2354–2358. doi:10.1016/j.juro.2007.08.022 PubMedCrossRefGoogle Scholar
  25. 25.
    Taverna G, Morandi G, Seveso M, Giusti G, Benetti A, Colombo P, Minuti F, Grizzi F, Graziotti P (2011) Colour Doppler and microbubble contrast agent ultrasonography do not improve cancer detection rate in transrectal systematic prostate biopsy sampling. BJU Int 108(11):1723–1727PubMedCrossRefGoogle Scholar
  26. 26.
    Zhao HX, Xia CX, Yin HX, Guo N, Zhu Q (2013) The value and limitations of contrast-enhanced transrectal ultrasonography for the detection of prostate cancer. Eur J Radiol 82(11):e641–e647. doi:10.1016/j.ejrad.2013.07.004 PubMedCrossRefGoogle Scholar
  27. 27.
    Javed S, Chadwick E, Edwards AA, Beveridge S, Laing R, Bott S, Eden C, Langley S (2013) Does prostate HistoScanning play a role in detecting prostate cancer in routine clinical practice? results from three independent studies. BJU Int. doi:10.1111/bju.12568 Google Scholar
  28. 28.
    Haffner J, Lemaitre L, Puech P, Haber GP, Leroy X, Jones JS, Villers A (2011) Role of magnetic resonance imaging before initial biopsy: comparison of magnetic resonance imaging-targeted and systematic biopsy for significant prostate cancer detection. BJU Int 108(8 Pt 2):E171–E178. doi:10.1111/j.1464-410X.2011.10112.x PubMedCrossRefGoogle Scholar
  29. 29.
    Delongchamps NB, Peyromaure M, Schull A, Beuvon F, Bouazza N, Flam T, Zerbib M, Muradyan N, Legman P, Cornud F (2013) Prebiopsy magnetic resonance imaging and prostate cancer detection: comparison of random and targeted biopsies. J Urol 189(2):493–499. doi:10.1016/j.juro.2012.08.195 PubMedCrossRefGoogle Scholar
  30. 30.
    Wysock JS, Rosenkrantz AB, Huang WC, Stifelman MD, Lepor H, Deng FM, Melamed J, Taneja SS (2013) 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. Eur Urol. doi:10.1016/j.eururo.2013.10.048 PubMedGoogle Scholar
  31. 31.
    Mozer P, Roupret M, Le Cossec C, Granger B, Comperat E, de Gorski A, Cussenot O, Renard-Penna R (2014) First round of targeted biopsies with magnetic resonance imaging/ultrasound-fusion images compared to conventional ultrasound-guided trans-rectal biopsies for the diagnosis of localised prostate cancer. BJU Int. doi:10.1111/bju.12690 Google Scholar
  32. 32.
    Miyagawa T, Ishikawa S, Kimura T, Suetomi T, Tsutsumi M, Irie T, Kondoh M, Mitake T (2010) Real-time virtual sonography for navigation during targeted prostate biopsy using magnetic resonance imaging data. Int J Urol 17(10):855–860. doi:10.1111/j.1442-2042.2010.02612.x PubMedCrossRefGoogle Scholar
  33. 33.
    Labanaris AP, Engelhard K, Zugor V, Nutzel R, Kuhn R (2010) Prostate cancer detection using an extended prostate biopsy schema in combination with additional targeted cores from suspicious images in conventional and functional endorectal magnetic resonance imaging of the prostate. Prostate Cancer Prostatic Dis 13(1):65–70. doi:10.1038/pcan.2009.41 PubMedCrossRefGoogle Scholar
  34. 34.
    Lee SH, Chung MS, Kim JH, Oh YT, Rha KH, Chung BH (2012) Magnetic resonance imaging targeted biopsy in men with previously negative prostate biopsy results. J Endourol 26(7):787–791. doi:10.1089/end.2011.0393 PubMedCrossRefGoogle Scholar
  35. 35.
    Vourganti S, Rastinehad A, Yerram NK, Nix J, Volkin D, Hoang A, Turkbey B, Gupta GN, Kruecker J, Linehan WM, Choyke PL, Wood BJ, Pinto PA (2012) Multiparametric magnetic resonance imaging and ultrasound fusion biopsy detect prostate cancer in patients with prior negative transrectal ultrasound biopsies. J Urol 188(6):2152–2157. doi:10.1016/j.juro.2012.08.025 PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Sonn GA, Chang E, Natarajan S, Margolis DJ, Macairan M, Lieu P, Huang J, Dorey FJ, Reiter RE, Marks LS (2014) Value of targeted prostate biopsy using magnetic resonance-ultrasound fusion in men with prior negative biopsy and elevated prostate-specific antigen. Eur Urol 65(4):809–815. doi:10.1016/j.eururo.2013.03.025 PubMedCrossRefGoogle Scholar
  37. 37.
    Pepe P, Garufi A, Priolo G, Candiano G, Pietropaolo F, Pennisi M, Fraggetta F, Aragona F (2013) Prostate cancer detection at repeat biopsy: can pelvic phased-array multiparametric MRI replace saturation biopsy? Anticancer Res 33(3):1195–1199PubMedGoogle Scholar
  38. 38.
    Fiard G, Hohn N, Descotes JL, Rambeaud JJ, Troccaz J, 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. doi:10.1016/j.urology.2013.02.022 PubMedCrossRefGoogle Scholar
  39. 39.
    Rastinehad AR, Turkbey B, Salami SS, Yaskiv O, George AK, Fakhoury M, Beecher K, Vira MA, Kavoussi LR, Siegel DN, Villani R, Ben-Levi E (2013) Improving detection of clinically significant prostate cancer: magnetic resonance imaging/transrectal ultrasound fusion guided prostate biopsy. J Urol. doi:10.1016/j.juro.2013.12.007 PubMedGoogle Scholar
  40. 40.
    Park BK, Park JW, Park SY, Kim CK, Lee HM, Jeon SS, Seo SI, Jeong BC, 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 Am J Roentgenol 197(5):W876–W881. doi:10.2214/AJR.11.6829 PubMedCrossRefGoogle Scholar
  41. 41.
    Sciarra A, Panebianco V, Ciccariello M, Salciccia S, Cattarino S, Lisi D, Gentilucci A, Alfarone A, Bernardo S, Passariello R, Gentile V (2010) Value of magnetic resonance spectroscopy imaging and dynamic contrast-enhanced imaging for detecting prostate cancer foci in men with prior negative biopsy. Clin Cancer Res Off J Am Assoc Cancer Res 16(6):1875–1883. doi:10.1158/1078-0432.CCR-09-2195 CrossRefGoogle Scholar
  42. 42.
    Walz J, Graefen M, Chun FK, Erbersdobler A, Haese A, Steuber T, Schlomm T, Huland H, Karakiewicz PI (2006) High incidence of prostate cancer detected by saturation biopsy after previous negative biopsy series. Eur Urol 50(3):498–505PubMedCrossRefGoogle Scholar
  43. 43.
    Keetch DW, Catalona WJ, Smith DS (1994) Serial prostatic biopsies in men with persistently elevated serum prostate specific antigen values. J Urol 151(6):1571–1574PubMedGoogle Scholar
  44. 44.
    Wilt TJ, Brawer MK, Jones KM, Barry MJ, Aronson WJ, Fox S, Gingrich JR, Wei JT, Gilhooly P, Grob BM, Nsouli I, Iyer P, Cartagena R, Snider G, Roehrborn C, Sharifi R, Blank W, Pandya P, Andriole GL, Culkin D, Wheeler T, Prostate Cancer Intervention versus Observation Trial Study G (2012) Radical prostatectomy versus observation for localized prostate cancer. N Engl J Med 367(3):203–213. doi:10.1056/NEJMoa1113162 PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Schroder FH, Hugosson J, Roobol MJ, Tammela TL, Ciatto S, Nelen V, Kwiatkowski M, Lujan M, Lilja H, Zappa M, Denis LJ, Recker F, Paez A, Maattanen L, Bangma CH, Aus G, Carlsson S, Villers A, Rebillard X, van der Kwast T, Kujala PM, Blijenberg BG, Stenman UH, Huber A, Taari K, Hakama M, Moss SM, de Koning HJ, Auvinen A, Investigators E (2012) Prostate-cancer mortality at 11 years of follow-up. N Engl J Med 366(11):981–990. doi:10.1056/NEJMoa1113135 PubMedCrossRefGoogle Scholar
  46. 46.
    Epstein JI, Walsh PC, Carmichael M, Brendler CB (1994) Pathologic and clinical findings to predict tumor extent of nonpalpable (stage T1c) prostate cancer. JAMA 271(5):368–374PubMedCrossRefGoogle Scholar
  47. 47.
    Robertson NL, Hu Y, Ahmed HU, Freeman A, Barratt D, Emberton M (2014) Prostate cancer risk inflation as a consequence of image-targeted biopsy of the prostate: a computer simulation study. Eur Urol 65(3):628–634. doi:10.1016/j.eururo.2012.12.057 PubMedCentralPubMedCrossRefGoogle Scholar
  48. 48.
    Jeldres C, Suardi N, Walz J, Hutterer GC, Ahyai S, Lattouf JB, Haese A, Graefen M, Erbersdobler A, Heinzer H, Huland H, Karakiewicz PI (2008) Validation of the contemporary epstein criteria for insignificant prostate cancer in European men. Eur Urol 54(6):1306–1313. doi:10.1016/j.eururo.2007.11.057 PubMedCrossRefGoogle Scholar
  49. 49.
    Moore CM, Kasivisvanathan V, Eggener S, Emberton M, Futterer JJ, Gill IS, Grubb Iii RL, Hadaschik B, Klotz L, Margolis DJ, Marks LS, Melamed J, Oto A, Palmer SL, Pinto P, Puech P, Punwani S, Rosenkrantz AB, Schoots IG, Simon R, Taneja SS, Turkbey B, Ukimura O, van der Meulen J, Villers A, Watanabe Y, Consortium S (2013) Standards of reporting for MRI-targeted biopsy studies (START) of the prostate: recommendations from an International Working Group. Eur Urol 64(4):544–552. doi:10.1016/j.eururo.2013.03.030 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Antoine van Hove
    • 1
  • Pierre-Henri Savoie
    • 2
  • Charlotte Maurin
    • 1
  • Serge Brunelle
    • 3
  • Gwenaëlle Gravis
    • 4
  • Naji Salem
    • 5
  • Jochen Walz
    • 1
  1. 1.Department of UrologyInstitut Paoli-Calmettes Cancer CentreMarseilleFrance
  2. 2.Department of UrologyHôpital Ste.AnneToulonFrance
  3. 3.Department of RadiologyInstitut Paoli-Calmettes Cancer CentreMarseilleFrance
  4. 4.Department of OncologyInstitut Paoli-Calmettes Cancer CentreMarseilleFrance
  5. 5.Department of RadiotherapyInstitut Paoli-Calmettes Cancer CentreMarseilleFrance

Personalised recommendations