We use cookies to improve your experience. By continuing to browse this site, you accept our cookie policy.×
Skip main navigation
Aging Health
Bioelectronics in Medicine
Biomarkers in Medicine
Breast Cancer Management
CNS Oncology
Colorectal Cancer
Concussion
Epigenomics
Future Cardiology
Future Microbiology
Future Neurology
Future Oncology
Future Rare Diseases
Future Virology
Hepatic Oncology
HIV Therapy
Immunotherapy
International Journal of Endocrine Oncology
International Journal of Hematologic Oncology
Journal of 3D Printing in Medicine
Journal of Comparative Effectiveness Research
Lung Cancer Management
Melanoma Management
Nanomedicine
Neurodegenerative Disease Management
Pain Management
Pediatric Health
Personalized Medicine
Pharmacogenomics
Regenerative Medicine

Effect of the number of biopsy cores on prostate cancer detection and staging

    Giovanni Lughezzani

    Cancer Prognostics & Health Outcomes Unit, University of Montreal Health Center (CHUM), 1058, rue St-Denis, Montréal, Québec, Canada, H2X 3J4 and Department of Urology, Vita-Salute San Raffaele University, Milan, Italy

    ,
    Maxine Sun

    Cancer Prognostics & Health Outcomes Unit, University of Montreal Health Center (CHUM), 1058, rue St-Denis, Montréal, Québec, Canada, H2X 3J4

    ,
    Lars Budäus

    Cancer Prognostics & Health Outcomes Unit, University of Montreal Health Center (CHUM), 1058, rue St-Denis, Montréal, Québec, Canada, H2X 3J4 and Martini-clinic, Prostate Cancer Center Hamburg-Eppendorf, Hamburg, Germany

    ,
    Rodolphe Thuret

    Cancer Prognostics & Health Outcomes Unit, University of Montreal Health Center (CHUM), 1058, rue St-Denis, Montréal, Québec, Canada, H2X 3J4 and Department of Urology, University of Montpellier Health Centre, Montpellier, France

    ,
    Shahrokh F Shariat

    Cancer Prognostics & Health Outcomes Unit, University of Montreal Health Center (CHUM), 1058, rue St-Denis, Montréal, Québec, Canada, H2X 3J4

    ,
    Paul Perrotte

    Department of Urology, University of Montreal, Montreal, QC, Canada

    &
    Pierre I Karakiewicz

    † Author for correspondence

    Cancer Prognostics & Health Outcomes Unit, University of Montreal Health Center (CHUM), 1058, rue St-Denis, Montréal, Québec, Canada, H2X 3J4 and Department of Urology, University of Montreal, Montreal, Québec, Canada.

    Published Online:https://doi.org/10.2217/fon.10.4

    Digital rectal examination, serum concentration of prostate cancer-specific antigen and transrectal ultrasound-guided biopsies are currently the main diagnostic tools to detect evidence of prostate cancer. Different prostatic biopsy strategies have been proposed in order to achieve an optimal prostate cancer detection rate and an accurate characterization of prostate cancer stage and grade. We examined the role of the number of biopsy cores on prostate cancer detection rates at initial and repeat biopsies. Moreover, we examined the relationship between the number of biopsy cores and the detection of insignificant prostate cancer. Finally, we reviewed the ability of biopsy cores in predicting prostate cancer stage and grade at radical prostatectomy. We relied on a PubMed systematic review of the contemporary English language literature using the terms ‘prostate cancer’, ‘diagnosis’, ‘transrectal ultrasound’ and ‘prostate biopsy’.

    Bibliography

    • Heidenreich A, Aus G, Bolla M et al.: EAU guidelines on prostate cancer. Eur. Urol.53(1),68–80 (2008).Crossref, MedlineGoogle Scholar
    • Chun FK-H, Briganti A, Graefen M et al.: Development and external validation of an extended 10-core biopsy nomogram. Eur. Urol.52(2),436–444 (2007).Crossref, MedlineGoogle Scholar
    • Presti JC Jr: Prostate biopsy: how many cores are enough? Urol. Oncol.21(2),135–140 (2003).Crossref, MedlineGoogle Scholar
    • Eichler K, Hempel S, Wilby J, Myers L, Bachmann LM, Kleijnen J: Diagnostic value of systematic biopsy methods in the investigation of prostate cancer: a systematic review. J. Urol.175(5),1605–1612 (2006).Crossref, MedlineGoogle Scholar
    • Scattoni V, Zlotta A, Montironi R, Schulman C, Rigatti P, Montorsi F: Extended and saturation prostatic biopsy in the diagnosis and characterisation of prostate cancer: a critical analysis of the literature. Eur. Urol.52(5),1309–1322 (2007).Crossref, MedlineGoogle Scholar
    • Hodge KK, McNeal JE, Terris MK, Stamey TA: Random systematic versus directed ultrasound guided transrectal core biopsies of the prostate. J. Urol.142(1),71–74; discussion 4–5 (1989).Crossref, Medline, CASGoogle Scholar
    • Stamey TA: Making the most out of six systematic sextant biopsies. Urology45(1),2–12 (1995).Crossref, Medline, CASGoogle Scholar
    • Norberg M, Egevad L, Holmberg L, Sparen P, Norlen BJ, Busch C: The sextant protocol for ultrasound-guided core biopsies of the prostate underestimates the presence of cancer. Urology50(4),562–566 (1997).Crossref, Medline, CASGoogle Scholar
    • Rabbani F, Stroumbakis N, Kava BR, Cookson MS, Fair WR: Incidence and clinical significance of false-negative sextant prostate biopsies. J. Urol.159(4),1247–1250 (1998).Crossref, Medline, CASGoogle Scholar
    • 10  Levine MA, Ittman M, Melamed J, Lepor H: Two consecutive sets of transrectal ultrasound guided sextant biopsies of the prostate for the detection of prostate cancer. J. Urol.159(2),471–475; discussion 5–6 (1998).Crossref, Medline, CASGoogle Scholar
    • 11  Durkan GC, Sheikh N, Johnson P, Hildreth AJ, Greene DR: Improving prostate cancer detection with an extended-core transrectal ultrasonography-guided prostate biopsy protocol. BJU Int.89(1),33–39 (2002).Crossref, Medline, CASGoogle Scholar
    • 12  Singh H, Canto EI, Shariat SF et al.: Improved detection of clinically significant, curable prostate cancer with systematic 12-core biopsy. J. Urol.171(3),1089–1092 (2004).Crossref, MedlineGoogle Scholar
    • 13  Elabbady AA, Khedr MM: Extended 12-core prostate biopsy increases both the detection of prostate cancer and the accuracy of Gleason score. Eur. Urol.49(1),49–53; discussion (2006).Crossref, MedlineGoogle Scholar
    • 14  Presti JC Jr: Repeat prostate biopsy – when, where, and how. Urol. Oncol.27(3),312–314 (2009).Crossref, MedlineGoogle Scholar
    • 15  Delongchamps NB, Haas GP: Saturation biopsies for prostate cancer: current uses and future prospects. Nat. Rev. Urol.6(12),645–652 (2009).Crossref, MedlineGoogle Scholar
    • 16  Watanabe H, Kato H, Kato T: Diagnostic application of ultrasonotomography to the prostate. Nippon Hinyokika Gakkay Zasshi59,273–279 (1968).Medline, CASGoogle Scholar
    • 17  Cooner WH, Mosley BR, Rutherford CL Jr et al. Clinical application of transrectal ultrasonography and prostate specific antigen in the search for prostate cancer. J. Urol.139(4),758–761 (1988).Crossref, Medline, CASGoogle Scholar
    • 18  Shinohara K, Wheeler TM, Scardino PT: The appearance of prostate cancer on transrectal ultrasonography: correlation of imaging and pathological examinations. J. Urol.142(1),76–82 (1989).Crossref, Medline, CASGoogle Scholar
    • 19  McNeal JE: The prostate and prostatic urethra: a morphologic synthesis. J. Urol.107(6),1008–1016 (1972).Crossref, Medline, CASGoogle Scholar
    • 20  Uzzo RG, Wei JT, Waldbaum RS, Perlmutter AP, Byrne JC, Vaughan ED Jr: The influence of prostate size on cancer detection. Urology46(6),831–836 (1995).Crossref, Medline, CASGoogle Scholar
    • 21  Karakiewicz PI, Bazinet M, Aprikian AG et al.: Outcome of sextant biopsy according to gland volume. Urology49(1),55–59 (1997).Crossref, Medline, CASGoogle Scholar
    • 22  Chen ME, Troncoso P, Johnston DA, Tang K, Babaian RJ: Optimization of prostate biopsy strategy using computer based analysis. J. Urol.158(6),2168–2175 (1997).Crossref, Medline, CASGoogle Scholar
    • 23  Chen ME, Troncoso P, Tang K, Babaian RJ, Johnston D: Comparison of prostate biopsy schemes by computer simulation. Urology53(5),951–960 (1999).Crossref, Medline, CASGoogle Scholar
    • 24  Eskicorapci SY, Baydar DE, Akbal C et al.: An extended 10-core transrectal ultrasonography guided prostate biopsy protocol improves the detection of prostate cancer. Eur. Urol.45(4),444–448; discussion 8–9 (2004).Crossref, MedlineGoogle Scholar
    • 25  Babaian RJ, Toi A, Kamoi K et al.: A comparative analysis of sextant and an extended 11-core multisite directed biopsy strategy. J. Urol.163(1),152–157 (2000).Crossref, Medline, CASGoogle Scholar
    • 26  Ravery V, Goldblatt L, Royer B, Blanc E, Toublanc M, Boccon-Gibod L: Extensive biopsy protocol improves the detection rate of prostate cancer. J. Urol.164(2),393–396 (2000).Crossref, Medline, CASGoogle Scholar
    • 27  Presti JC Jr, Chang JJ, Bhargava V, Shinohara K: The optimal systematic prostate biopsy scheme should include 8 rather than 6 biopsies: results of a prospective clinical trial. J. Urol.163(1),163–166; discussion 6–7 (2000).Crossref, MedlineGoogle Scholar
    • 28  Presti JC Jr, O’Dowd GJ, Miller MC, Mattu R, Veltri RW: Extended peripheral zone biopsy schemes increase cancer detection rates and minimize variance in prostate specific antigen and age related cancer rates: results of a community multi-practice study. J. Urol.169(1),125–129 (2003).Crossref, MedlineGoogle Scholar
    • 29  Gore JL, Shariat SF, Miles BJ et al.: Optimal combinations of systematic sextant and laterally directed biopsies for the detection of prostate cancer. J. Urol.165(5),1554–1559 (2001).Crossref, Medline, CASGoogle Scholar
    • 30  Eskew LA, Bare RL, McCullough DL: Systematic 5 region prostate biopsy is superior to sextant method for diagnosing carcinoma of the prostate. J. Urol.157(1),199–202; discussion 202–203 (1997).Crossref, Medline, CASGoogle Scholar
    • 31  Scattoni V, Roscigno M, Raber M et al.: Initial extended transrectal prostate biopsy – are more prostate cancers detected with 18 cores than with 12 cores? J. Urol.179(4),1327–1331; discussion 31 (2008).Crossref, MedlineGoogle Scholar
    • 32  Iguchi T, Wang CY, Delongchamps NB et al.: Occult prostate cancer effects the results of case–control studies due to verification bias. Anticancer Res.28,3007–3010 (2008).MedlineGoogle Scholar
    • 33  Punglia RS, D’Amico AV, Catalona WJ, Roehl KA, Kuntz KM: Effect of verification bias on screening for prostate cancer by measurement of prostate-specific antigen. N. Engl. J. Med.349(4),335–342 (2003).Crossref, MedlineGoogle Scholar
    • 34  Pound CR, Partin AW, Eisenberger MA, Chan DW, Pearson JD, Walsh PC: Natural history of progression after PSA elevation following radical prostatectomy. JAMA281(17),1591–1597 (1999).Crossref, Medline, CASGoogle Scholar
    • 35  De la Taille A, Antiphon P, Salomon L et al.: Prospective evaluation of a 21-sample needle biopsy procedure designed to improve the prostate cancer detection rate. Urology61(6),1181–1186 (2003).Crossref, MedlineGoogle Scholar
    • 36  Ravery V, Dominique S, Panhard X, Toublanc M, Boccon-Gibod L: The 20-core prostate biopsy protocol – a new gold standard? J. Urol.179(2),504–507 (2008).Crossref, Medline, CASGoogle Scholar
    • 37  Guichard G, Larre S, Gallina A et al.: Extended 21-sample needle biopsy protocol for diagnosis of prostate cancer in 1000 consecutive patients. Eur. Urol.52(2),430–435 (2007).Crossref, MedlineGoogle Scholar
    • 38  Jones JS, Patel A, Schoenfield L, Rabets JC, Zippe CD, Magi-Galluzzi C: Saturation technique does not improve cancer detection as an initial prostate biopsy strategy. J. Urol.175(2),485–488 (2006).Crossref, MedlineGoogle Scholar
    • 39  Pepe P, Aragona F: Saturation prostate needle biopsy and prostate cancer detection at initial and repeat evaluation. Urology70(6),1131–1135 (2007).Crossref, MedlineGoogle Scholar
    • 40  Delongchamps NB, de la Roza G, Jones R, Jumbelic M, Haas G: Saturation biopsies on autopsied prostates for detecting and characterizing prostate cancer. BJU Int.103,49–54 (2008).Crossref, MedlineGoogle Scholar
    • 41  McNeal JE, Redwine EA, Freiha FS, Stamey TA: Zonal distribution of prostatic adenocarcinoma. Correlation with histologic pattern and direction of spread. Am. J. Surg. Pathol.12(12),897–906 (1988).Crossref, Medline, CASGoogle Scholar
    • 42  Epstein JI, Walsh PC, Carmichael M, Brendler CB: Pathologic and clinical findings to predict tumor extent of nonpalpable (stage T1c) prostate cancer. JAMA271(5),368–374 (1994).Crossref, Medline, CASGoogle Scholar
    • 43  Stamey TA, Sozen TS, Yemoto CM, McNeal JE: Classification of localized untreated prostate cancer based on 791 men treated only with radical prostatectomy: common ground for therapeutic trials and TNM subgroups. J. Urol.159(6),2009–2012 (1998).Crossref, Medline, CASGoogle Scholar
    • 44  Peyromaure M, Ravery V, Boccon-Gibod L: The role of the biopsy of the transitonal zone and of the seminal vesicles in the diagnosis and staging of prostate cancer. Eur. Urol. Suppl.1(6),40–46 (2002).CrossrefGoogle Scholar
    • 45  Bazinet M, Karakiewicz PI, Aprikian AG et al.: Value of systematic transition zone biopsies in the early detection of prostate cancer. J. Urol.155(2),605–606 (1996).Crossref, Medline, CASGoogle Scholar
    • 46  Terris MK, Pham TQ, Issa MM, Kabalin JN: Routine transition zone and seminal vesicle biopsies in all patients undergoing transrectal ultrasound guided prostate biopsies are not indicated. J. Urol.157(1),204–206 (1997).Crossref, Medline, CASGoogle Scholar
    • 47  Onder AU, Yalcin V, Arar O, Yaycioglu O, Citci A, Solok V: Impact of transition zone biopsies in detection and evaluation of prostate cancer. Eur. Urol.33(6),542–548 (1998).Crossref, Medline, CASGoogle Scholar
    • 48  Morote J, Lopez M, Encabo G, de Torres I: Value of routine transition zone biopsies in patients undergoing ultrasound-guided sextant biopsies for the first time. Eur. Urol.35(4),294–297 (1999).Crossref, Medline, CASGoogle Scholar
    • 49  Pelzer AE, Bektic J, Berger AP et al.: Are transition zone biopsies still necessary to improve prostate cancer detection? Results from the tyrol screening project. Eur. Urol.48(6),916–921; discussion 21 (2005).Crossref, MedlineGoogle Scholar
    • 50  Fleshner NE, O’Sullivan M, Fair WR: Prevalence and predictors of a positive repeat transrectal ultrasound guided needle biopsy of the prostate. J. Urol.158(2),505–508; discussion 8–9 (1997).Crossref, Medline, CASGoogle Scholar
    • 51  Applewhite JC, Matlaga BR, McCullough DL: Results of the 5 region prostate biopsy method: the repeat biopsy population. J. Urol.168(2),500–503 (2002).Crossref, MedlineGoogle Scholar
    • 52  Mian BM, Naya Y, Okihara K, Vakar-Lopez F, Troncoso P, Babaian RJ: Predictors of cancer in repeat extended multisite prostate biopsy in men with previous negative extended multisite biopsy. Urology60(5),836–840 (2002).Crossref, MedlineGoogle Scholar
    • 53  Chon CH, Lai FC, McNeal JE, Presti JC Jr: Use of extended systematic sampling in patients with a prior negative prostate needle biopsy. J. Urol.167(6),2457–2460 (2002).Crossref, MedlineGoogle Scholar
    • 54  Philip J, Hanchanale V, Foster CS, Javle P: Importance of peripheral biopsies in maximising the detection of early prostate cancer in repeat 12-core biopsy protocols. BJU Int.98(3),559–562 (2006).Crossref, MedlineGoogle Scholar
    • 55  Chun FK, Briganti A, Graefen M et al.: Development and external validation of an extended repeat biopsy nomogram. J. Urol.177(2),510–515 (2007).Crossref, MedlineGoogle Scholar
    • 56  Borboroglu PG, Comer SW, Riffenburgh RH, Amling CL: Extensive repeat transrectal ultrasound guided prostate biopsy in patients with previous benign sextant biopsies. J. Urol.163(1),158–162 (2000).Crossref, Medline, CASGoogle Scholar
    • 57  Stewart CS, Leibovich BC, Weaver AL, Lieber MM: Prostate cancer diagnosis using a saturation needle biopsy technique after previous negative sextant biopsies. J. Urol.166(1),86–91; discussion 91–92 (2001).Crossref, Medline, CASGoogle Scholar
    • 58  Fleshner N, Klotz L: Role of ‘saturation biopsy’ in the detection of prostate cancer among difficult diagnostic cases. Urology60(1),93–97 (2002).Crossref, MedlineGoogle Scholar
    • 59  Rabets JC, Jones JS, Patel A, Zippe CD: Prostate cancer detection with office based saturation biopsy in a repeat biopsy population. J. Urol.172(1),94–97 (2004).Crossref, MedlineGoogle Scholar
    • 60  Patel AR, Jones JS, Rabets J, DeOreo G, Zippe CD: Parasagittal biopsies add minimal information in repeat saturation prostate biopsy. Urology63(1),87–89 (2004).Crossref, MedlineGoogle Scholar
    • 61  Walz J, Graefen M, Chun FK et al.: High incidence of prostate cancer detected by saturation biopsy after previous negative biopsy series. Eur. Urol.50(3),498–505 (2006).Crossref, MedlineGoogle Scholar
    • 62  Tan N, Lane BR, Li J, Moussa AS, Soriano M, Jones JS: Prostate cancers diagnosed at repeat biopsy are smaller and less likely to be high grade. J. Urol.180(4),1325–1329; discussion 1329 (2008).Crossref, MedlineGoogle Scholar
    • 63  Stamey TA, Freiha FS, McNeal JE, Redwine EA, Whittemore AS, Schmid HP: Localized prostate cancer. Relationship of tumor volume to clinical significance for treatment of prostate cancer. Cancer71(3 Suppl.),933–938 (1993).Crossref, Medline, CASGoogle Scholar
    • 64  Haas GP, Delongchamps NB, Jones RF et al.: Needle biopsies on autopsy prostates: sensitivity of cancer detection based on true prevalence. J. Natl Cancer Inst.99(19),1484–1489 (2007).Crossref, MedlineGoogle Scholar
    • 65  Eskew LA, Woodruff RD, Bare RL, McCullough DL: Prostate cancer diagnosed by the 5 region biopsy method is significant disease. J. Urol.160(3 Pt 1),794–796 (1998).Crossref, Medline, CASGoogle Scholar
    • 66  Chan TY, Chan DY, Stutzman KL, Epstein JI: Does increased needle biopsy sampling of the prostate detect a higher number of potentially insignificant tumors? J. Urol.166(6),2181–2184 (2001).Crossref, Medline, CASGoogle Scholar
    • 67  Meng MV, Elkin EP, DuChane J, Carroll PR: Impact of increased number of biopsies on the nature of prostate cancer identified. J. Urol.176(1),63–68; discussion 9 (2006).Crossref, MedlineGoogle Scholar
    • 68  Siu W, Dunn RL, Shah RB, Wei JT: Use of extended pattern technique for initial prostate biopsy. J. Urol.174(2),505–509 (2005).Crossref, MedlineGoogle Scholar
    • 69  Boccon-Gibod LM, de Longchamps NB, Toublanc M, Boccon-Gibod LA, Ravery V: Prostate saturation biopsy in the reevaluation of microfocal prostate cancer. J. Urol.176(3),961–963; discussion 3–4 (2006).Crossref, Medline, CASGoogle Scholar
    • 70  Delongchamps NB, de la Roza G, Chandan V et al.: Diagnostic accuracy of extended biopsies for the staging of microfocal prostate cancers in autopsy specimen. Prostate Cancer Prostatic Dis.12,137–142 (2009).Crossref, Medline, CASGoogle Scholar
    • 71  Berglund RK, Masterson TA, Vora KC, Eggener SE, Eastham JA, Guillonneau BD: Pathological upgrading and up staging with immediate repeat biopsy in patients eligible for active surveillance. J. Urol.180(5),1964–1967; discussion 7–8 (2008).Crossref, MedlineGoogle Scholar
    • 72  Bostwick DG: Gleason grading of prostatic needle biopsies. Correlation with grade in 316 matched prostatectomies. Am. J. Surg. Pathol.18(8),796–803 (1994).Crossref, Medline, CASGoogle Scholar
    • 73  Steinberg DM, Sauvageot J, Piantadosi S, Epstein JI: Correlation of prostate needle biopsy and radical prostatectomy Gleason grade in academic and community settings. Am. J. Surg. Pathol.21(5),566–576 (1997).Crossref, Medline, CASGoogle Scholar
    • 74  King CR: Patterns of prostate cancer biopsy grading: trends and clinical implications. Int. J. Cancer90(6),305–311 (2000).Crossref, Medline, CASGoogle Scholar
    • 75  San Francisco IF, DeWolf WC, Rosen S, Upton M, Olumi AF: Extended prostate needle biopsy improves concordance of Gleason grading between prostate needle biopsy and radical prostatectomy. J. Urol.169(1),136–140 (2003).Crossref, MedlineGoogle Scholar
    • 76  Emiliozzi P, Maymone S, Paterno A et al.: Increased accuracy of biopsy Gleason score obtained by extended needle biopsy. J. Urol.172(6 Pt 1),2224–2226 (2004).Crossref, Medline, CASGoogle Scholar
    • 77  Coogan CL, Latchamsetty KC, Greenfield J, Corman JM, Lynch B, Porter CR: Increasing the number of biopsy cores improves the concordance of biopsy Gleason score to prostatectomy Gleason score. BJU Int.96(3),324–327 (2005).Crossref, MedlineGoogle Scholar
    • 78  Mian BM, Lehr DJ, Moore CK et al.: Role of prostate biopsy schemes in accurate prediction of Gleason scores. Urology67(2),379–383 (2006).Crossref, MedlineGoogle Scholar
    • 79  Divrik RT, Eroglu A, Sahin A, Zorlu F, Ozen H: Increasing the number of biopsies increases the concordance of Gleason scores of needle biopsies and prostatectomy specimens. Urol. Oncol.25(5),376–382 (2007).Crossref, MedlineGoogle Scholar
    • 80  Capitanio U, Karakiewicz PI, Valiquette L et al.: Biopsy core number represents one of foremost predictors of clinically significant gleason sum upgrading in patients with low-risk prostate cancer. Urology73(5),1087–1091 (2009).Crossref, MedlineGoogle Scholar
    • 81  Numao N, Kawakami S, Yokoyama M et al.: Improved accuracy in predicting the presence of Gleason pattern 4/5 prostate cancer by three-dimensional 26-core systematic biopsy. Eur. Urol.52(6),1663–1668 (2007).Crossref, MedlineGoogle Scholar
    • 82  Naya Y, Ochiai A, Troncoso P, Babaian RJ: A comparison of extended biopsy and sextant-biopsy schemes for predicting the pathological stage of prostate cancer. J. Urol.171(6 Pt 1),2203–2208 (2004).Crossref, MedlineGoogle Scholar
    • 83  Schulte RT, Wood DP, Daignault S, Shah RB, Wei JT: Utility of extended pattern prostate biopsies for tumor localization: pathologic correlations after radical prostatectomy. Cancer113(7),1559–1565 (2008).Crossref, MedlineGoogle Scholar
    • 84  Paul R, Scholer S, van Randenborgh H et al.: Morbidity of prostatic biopsy for different biopsy strategies: is there a relation to core number and sampling region? Eur. Urology45,450–456 (2004).Crossref, MedlineGoogle Scholar
    • 85  Peyromaure M, Ravery V, Messas A, Toublanc M, Boccon-Gibod L, Boccon-Gibod L: Pain and morbidity of an extensive prostate 10-biopsy protocol: a prospective study in 289 patients. J. Urol.167,218–221 (2002).Crossref, MedlineGoogle Scholar
    • 86  Ecke TH, Gunia S, Bartel P, Hallmann S, Koch S, Ruttloff J: Complications and risk factors of transrectal ultrasound guided needle biopsies of the prostate evaluated by questionnaire. Urol. Oncol.26,474–478 (2008).Crossref, MedlineGoogle Scholar
    • 87  Tricoli JV, Schoenfeldt M, Conley BA: Detection of prostate cancer and predicting progression: current and future diagnostic markers. Clin. Cancer Res.10(12 Pt 1),3943–3953 (2004).Crossref, MedlineGoogle Scholar
    • 88  Quinn DI, Henshall SM, Sutherland RL: Molecular markers of prostate cancer outcome. Eur. J. Cancer41(6),858–887 (2005).Crossref, Medline, CASGoogle Scholar
    • 89  Jhavar S, Bartlett J, Kovacs G et al.: Biopsy tissue microarray study of Ki-67 expression in untreated, localized prostate cancer managed by active surveillance. Prostate Cancer Prostatic Dis.12(2),143–147 (2009).Crossref, Medline, CASGoogle Scholar
    • 90  Zellweger T, Gunther S, Zlobec I et al.: Tumour growth fraction measured by immunohistochemical staining of Ki67 is an independent prognostic factor in preoperative prostate biopsies with small-volume or low-grade prostate cancer. Int. J. Cancer124(9),2116–2123 (2009).Crossref, Medline, CASGoogle Scholar
    • 91  Vergis R, Corbishley CM, Norman AR et al.: Intrinsic markers of tumour hypoxia and angiogenesis in localised prostate cancer and outcome of radical treatment: a retrospective analysis of two randomised radiotherapy trials and one surgical cohort study. Lancet Oncol.9(4),342–351 (2008).Crossref, MedlineGoogle Scholar
    • 92  Amiel GE, Slawin KM: Newer modalities of ultrasound imaging and treatment of the prostate. Urol. Clin. North Am.33(3),329–337 (2006).Crossref, MedlineGoogle Scholar
    • 93  Pallwein L, Mitterberger M, Gradl J et al.: Value of contrast-enhanced ultrasound and elastography in imaging of prostate cancer. Curr. Opin. Urol.17(1),39–47 (2007).Crossref, MedlineGoogle Scholar
    • 94  Salomon G, Kollerman J, Thederan I et al.: Evaluation of prostate cancer detection with ultrasound real-time elastography: a comparison with step section pathological analysis after radical prostatectomy. Eur. Urol.54(6),1354–1362 (2008).Crossref, MedlineGoogle Scholar
    • 95  Onik G, Miessau M, Bostwick DG: Three-dimensional prostate mapping biopsy has a potentially significant impact on prostate cancer management. J. Clin. Oncol.27(26),4321–4326 (2009).Crossref, MedlineGoogle Scholar
    • 101  National Comprehensive Cancer Network Clinical Practice Guidelines in Oncology: Prostate Cancer Early Detection www.nccn.orgGoogle Scholar