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Landmarks in the evolution of prostate biopsy

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Abstract

Approaches and techniques used for diagnostic prostate biopsy have undergone considerable evolution over the past few decades: from the original finger-guided techniques to the latest MRI-directed strategies, from aspiration cytology to tissue core sampling, and from transrectal to transperineal approaches. In particular, increased adoption of transperineal biopsy approaches have led to reduced infectious complications and improved antibiotic stewardship. Furthermore, as image fusion has become integral, these novel techniques could be incorporated into prostate biopsy methods in the future, enabling 3D-ultrasonography fusion reconstruction, molecular targeting based on PET imaging and autonomous robotic-assisted biopsy.

Key points

  • The techniques of prostate biopsy have undergone considerable evolution over time, from early finger-guided techniques to current MRI-targeted strategies.

  • The improvement in performance associated with pre-biopsy multiparametric MRI compared with random transrectal ultrasonography-guided biopsy sampling has led to a dramatic change in the prostate cancer diagnostic pathway.

  • Pre-biopsy multiparametric MRI has mitigated the risk of underdiagnosis of clinically significant disease and overdiagnosis of clinically insignificant disease, both of which were associated with random prostate sampling.

  • Increased adoption of transperineal rather than transrectal approaches to biopsy sampling has minimized infectious complications and improved antibiotic stewardship.

  • Novel techniques — including 3D-ultrasound fusion reconstruction, multiparametric ultrasonography, high-resolution micro-ultrasonography, molecular (positron emission) image targeting and autonomous robotic-assisted biopsy — have been integrated into prostate biopsy sampling at various stages of deployment and use.

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Fig. 1: Landmarks in the history of prostate biopsy.
Fig. 2: Historical biopsy techniques before transrectal ultrasonography invention.
Fig. 3: Transperineal MRI–transrectal ultrasound fusion biopsy.
Fig. 4: Transperineal template mapping biopsy.
Fig. 5: Combined pelvic PSMA PET–CT and multiparametric MRI prostate.

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References

  1. Sung, H. et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 71, 209–249 (2021).

    Article  PubMed  Google Scholar 

  2. Baade, P. D., Youlden, D. R., Cramb, S. M., Dunn, J. & Gardiner, R. A. Epidemiology of prostate cancer in the Asia-Pacific region. Prostate Int. 1, 47–58 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Lomas, D. J. & Ahmed, H. U. All change in the prostate cancer diagnostic pathway. Nat. Rev. Clin. Oncol. 17, 372–381 (2020).

    Article  PubMed  Google Scholar 

  4. Ahmed, H. U. et al. Diagnostic accuracy of multi-parametric MRI and TRUS biopsy in prostate cancer (PROMIS): a paired validating confirmatory study. Lancet 389, 815–822 (2017).

    Article  PubMed  Google Scholar 

  5. Sathianathen, N. J. et al. Negative predictive value of multiparametric magnetic resonance imaging in the detection of clinically significant prostate cancer in the prostate imaging reporting and data system era: a systematic review and meta-analysis. Eur. Urol. 78, 402–414 (2020).

    Article  PubMed  Google Scholar 

  6. Ahmed, H. U., Arya, M., Freeman, A. & Emberton, M. Do low-grade and low-volume prostate cancers bear the hallmarks of malignancy? Lancet Oncol. 13, e509–e517 (2012).

    Article  PubMed  Google Scholar 

  7. Miah, S., Ahmed, H. U., Freeman, A. & Emberton, M. Does true Gleason pattern 3 merit its cancer descriptor? Nat. Rev. Urol. 13, 541–548 (2016).

    Article  PubMed  Google Scholar 

  8. Gleason, D. F. in Urologic Pathology: The Prostate (ed Tannenbaum, M.) 171–198 (Lea and Febiger, 1977).

  9. Gleason, D. F. Classification of prostatic carcinomas. Cancer Chemother. Rep. 50, 125–128 (1966).

    CAS  PubMed  Google Scholar 

  10. Mottet, N. et al. EAU-EANM-ESTRO-ESUR-SIOG guidelines on prostate cancer — 2020 update. Part 1: screening, diagnosis, and local treatment with curative intent. Eur. Urol. 79, 243–262 (2021).

    Article  CAS  PubMed  Google Scholar 

  11. Moore, C. M. et al. Standards of reporting for MRI-targeted biopsy studies (START) of the prostate: recommendations from an International Working Group. Eur. Urol. 64, 544–552 (2013).

    Article  PubMed  Google Scholar 

  12. Tsaur, I. et al. Aggressive variants of prostate cancer — are we ready to apply specific treatment right now? Cancer Treat. Rev. 75, 20–26 (2019).

    Article  PubMed  Google Scholar 

  13. Kitzing, Y. X. et al. Benign conditions that mimic prostate carcinoma: MR imaging features with histopathologic correlation. Radiographics 36, 162–175 (2016).

    Article  PubMed  Google Scholar 

  14. Barrett, T., Rajesh, A., Rosenkrantz, A. B., Choyke, P. L. & Turkbey, B. PI-RADS version 2.1: one small step for prostate MRI. Clin. Radiol. 74, 841–852 (2019).

    Article  CAS  PubMed  Google Scholar 

  15. Kasivisvanathan, V. et al. MRI-targeted or standard biopsy for prostate-cancer diagnosis. N. Engl. J. Med. 378, 1767–1777 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Michael, A. et al. MRI-targeted, systematic, and combined biopsy for prostate cancer diagnosis. N. Engl. J. Med. 382, 917–928 (2020).

    Article  Google Scholar 

  17. Bennett, H. Y., Roberts, M. J., Doi, S. & Gardiner, R. A. The global burden of major infectious complications following prostate biopsy. Epidemiol. Infect. 144, 1784–1791 (2016).

    Article  CAS  PubMed  Google Scholar 

  18. Borghesi, M. et al. Complications after systematic, random, and image-guided prostate biopsy. Eur. Urol. 71, 353–365 (2017).

    Article  PubMed  Google Scholar 

  19. Anastasiadis, E., van der Meulen, J. & Emberton, M. Hospital admissions after transrectal ultrasound‐guided biopsy of the prostate in men diagnosed with prostate cancer: a database analysis in England. Int. J. Urol. 22, 181–186 (2015).

    Article  PubMed  Google Scholar 

  20. Tamhankar, A. S. et al. The clinical and financial implications of a decade of prostate biopsies in the NHS: analysis of Hospital Episode Statistics data 2008–2019. BJU Int. 126, 133–141 (2020).

  21. Young, H. H., Davis, D. M. & Johnson, F. P. in Young’s Practice of Urology: Based on a Study of 12,500 Cases (WB Saunders Company, 1926).

  22. Sathianathen, N. J., Konety, B. R., Crook, J., Saad, F. & Lawrentschuk, N. Landmarks in prostate cancer. Nat. Rev. Urol. 15, 627–642 (2018).

    Article  PubMed  Google Scholar 

  23. Barringer, B. S. Carcinoma of the prostate. Surg. Gynecol. Obstet. 34, 168–176 (1922).

    Google Scholar 

  24. Ferguson, R. S. Prostatic neoplasms: their diagnosis by needle puncture and aspiration. Am. J. Surg. 9, 507–511 (1930).

    Article  Google Scholar 

  25. Astraldi, A. Diagnosis of cancer of the prostate: biopsy by rectal route. Urol. Cutan. Rev. 41, 421 (1937).

    Google Scholar 

  26. Barnes, R. W. & Emery, D. S. Management of early prostatic carcinoma. Calif. Med. 91, 57 (1959).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Grabstald, H. Biopsy techniques in the diagnosis of cancer of the prostate. CA Cancer J. Clin. 15, 134–138 (1965).

    Article  CAS  PubMed  Google Scholar 

  28. Kaufman, J. J., Rosenthal, M. & Goodwin, W. E. Needle biopsy in diagnosis of prostatic cancer. Calif. Med. 81, 308 (1954).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Denton, S. E., Valk, W. L., Jacobson, J. M. & Kettunen, R. C. Comparison of the perineal needle biopsy and the transurethral prostatectomy in the diagnosis of prostatic carcinoma: an analysis of 300 cases. J. Urol. 97, 127–129 (1967).

    Article  CAS  PubMed  Google Scholar 

  30. Purser, B. N., Robinson, B. C. & Mostofi, F. K. Comparison of needle biopsy and transurethral resection biopsy in the diagnosis of carcinoma of the prostate. J. Urol. 98, 224–228 (1967).

    Article  CAS  PubMed  Google Scholar 

  31. Humphrey, P. A. Gleason grading and prognostic factors in carcinoma of the prostate. Mod. Pathol. 17, 292–306 (2004).

    Article  PubMed  Google Scholar 

  32. Van Leenders, G. J. et al. The 2019 International Society of Urological Pathology (ISUP) consensus conference on grading of prostatic carcinoma. Am. J. Surg. Pathol. 44, e87 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Villers, A., McNeal, J. E., Freiha, F. S. & Stamey, T. A. Multiple cancers in the prostate. Morphologic features of clinically recognized versus incidental tumors. Cancer 70, 2313–2318 (1992).

    Article  CAS  PubMed  Google Scholar 

  34. Ahmed, H. U. The index lesion and the origin of prostate cancer. N. Engl. J. Med. 361, 1704–1706 (2009).

    Article  CAS  PubMed  Google Scholar 

  35. Bott, S. R. et al. The index lesion and focal therapy: an analysis of the pathological characteristics of prostate cancer. BJU Int. 106, 1607–1611 (2010).

    Article  PubMed  Google Scholar 

  36. Gundem, G. et al. The evolutionary history of lethal metastatic prostate cancer. Nature 520, 353 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. McNeal, J. E. Regional morphology and pathology of the prostate. Am. J. Clin. Pathol. 49, 347–357 (1968).

    Article  CAS  PubMed  Google Scholar 

  38. McNeal, J. E. The zonal anatomy of the prostate. Prostate 2, 35–49 (1981).

    Article  CAS  PubMed  Google Scholar 

  39. Takahashi, H. The ultrasonic diagnosis in the field of urology (The 1st report). Proc. 3rd Meeting. Jpn. Soc. Ultrasonics Med. 1963 (1963).

  40. Sedelaar, J. et al. Transrectal ultrasound imaging of the prostate: review and perspectives of recent developments. Prostate Cancer Prostatic Dis. 2, 241–252 (1999).

    Article  CAS  PubMed  Google Scholar 

  41. Watanabe, H., Igari, D., Tanahasi, Y., Harada, K. & Saitoh, M. Development and application of new equipment for transrectal ultrasonography. J. Clin. Ultrasound 2, 91–98 (1974).

    Article  CAS  PubMed  Google Scholar 

  42. Watanabe, H. History and applications of transrectal sonography of the prostate. Urol. Clin. North. Am. 16, 617–622 (1989).

    Article  CAS  PubMed  Google Scholar 

  43. Hodge, K. K., McNeal, J. E. & Stamey, T. A. Ultrasound guided transrectal core biopsies of the palpably abnormal prostate. J. Urol. 142, 66–70 (1989).

    Article  CAS  PubMed  Google Scholar 

  44. Levine, M. A., 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, 471–476 (1998).

    Article  CAS  PubMed  Google Scholar 

  45. Grummet, J. P. et al. Sepsis and ‘superbugs’: should we favour the transperineal over the transrectal approach for prostate biopsy? BJU Int. 114, 384–388 (2014).

    PubMed  Google Scholar 

  46. Stewart, C. S., Leibovich, B. C., Weaver, A. L. & Lieber, M. M. Prostate cancer diagnosis using a saturation needle biopsy technique after previous negative sextant biopsies. J. Urol. 166, 86–92 (2001).

    Article  CAS  PubMed  Google Scholar 

  47. Langer, J. E. The Current Role of Transrectal Ultrasonography in the Evaluation of Prostate Carcinoma (Elsevier, 1999).

  48. Patel, U. et al. Infection after transrectal ultrasonography‐guided prostate biopsy: increased relative risks after recent international travel or antibiotic use. BJU Int. 109, 1781–1785 (2012).

    Article  PubMed  Google Scholar 

  49. Hodge, K. K., McNeal, J. E., Terris, M. K. & Stamey, T. A. Random systematic versus directed ultrasound guided transrectal core biopsies of the prostate. J. Urol. 142, 71–74 (1989).

    Article  CAS  PubMed  Google Scholar 

  50. Naughton, C. K., Ornstein, D. K., Smith, D. S. & Catalona, W. J. Pain and morbidity of transrectal ultrasound guided prostate biopsy: a prospective randomized trial of 6 versus 12 cores. J. Urol. 163, 168–171 (2000).

    Article  CAS  PubMed  Google Scholar 

  51. Babaian, R. J. et al. A comparative analysis of sextant and an extended 11-core multisite directed biopsy strategy. J. Urol. 163, 152–157 (2000).

    Article  CAS  PubMed  Google Scholar 

  52. Presti, J. C., Chang, J. J., 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, 163–167 (2000).

    Article  PubMed  Google Scholar 

  53. Eichler, K. et al. Diagnostic value of systematic biopsy methods in the investigation of prostate cancer: a systematic review. J. Urol. 175, 1605–1612 (2006).

    Article  PubMed  Google Scholar 

  54. Kawata, N. et al. Laterally directed biopsies detect more clinically threatening prostate cancer: computer simulated results. Prostate 57, 118–128 (2003).

    Article  PubMed  Google Scholar 

  55. Steyn, J. H. & Smith, F. W. Nuclear magnetic resonance imaging of the prostate. Br. J. Urol. 54, 726–728 (1982).

    Article  CAS  PubMed  Google Scholar 

  56. Price, J. M. & Davidson, A. J. Computed tomography in the evaluation of the suspected carcinomatous prostate. Urol. Radiol. 1, 39 (1980).

    Article  Google Scholar 

  57. Hricak, H. et al. MR imaging of the prostate gland: normal anatomy. Am. J. Roentgenol. 148, 51–58 (1987).

    Article  CAS  Google Scholar 

  58. Weinreb, J. C. et al. Prostate cancer: sextant localization at MR imaging and MR spectroscopic imaging before prostatectomy — results of ACRIN prospective multi-institutional clinicopathologic study. Radiology 251, 122–133 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Issa, B. In vivo measurement of the apparent diffusion coefficient in normal and malignant prostatic tissues using echo‐planar imaging. J. Magn. Reson. Imaging 16, 196–200 (2002).

    Article  PubMed  Google Scholar 

  60. Brown, G., Macvicar, D. A., Ayton, V. & Husband, J. E. The role of intravenous contrast enhancement in magnetic resonance imaging of prostatic carcinoma. Clin. Radiol. 50, 601–606 (1995).

    Article  CAS  PubMed  Google Scholar 

  61. Kirkham, A. P., Emberton, M. & Allen, C. How good is MRI at detecting and characterising cancer within the prostate? Eur. Urol. 50, 1163–1175 (2006).

    Article  PubMed  Google Scholar 

  62. Dickinson, L. et al. Clinical applications of multiparametric MRI within the prostate cancer diagnostic pathway. Urol. Oncol. 31, 281 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  63. Bloch, B. N. et al. 3 Tesla magnetic resonance imaging of the prostate with combined pelvic phased-array and endorectal coils: initial experience(1). Acad. Radiol. 11, 863–867 (2004).

    PubMed  Google Scholar 

  64. Barentsz, J. O. et al. ESUR prostate MR guidelines 2012. Eur. Radiol. 22, 746–757 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  65. Seo, J. W. et al. PI-RADS version 2: detection of clinically significant cancer in patients with biopsy Gleason score 6 prostate cancer. Am. J. Roentgenol. 209, W1–W9 (2017).

    Article  Google Scholar 

  66. Khoo, C. C. et al. Likert vs PI‐RADS v2: a comparison of two radiological scoring systems for detection of clinically significant prostate cancer. BJU Int. 125, 49–55 (2020).

    Article  CAS  PubMed  Google Scholar 

  67. Turkbey, B. et al. Prostate imaging reporting and data system version 2.1: 2019 update of prostate imaging reporting and data system version 2. Eur. Urol. 76, 340–351 (2019).

    Article  PubMed  Google Scholar 

  68. Brizmohun Appayya, M. et al. National implementation of multi‐parametric magnetic resonance imaging for prostate cancer detection — recommendations from a UK consensus meeting. BJU Int. 122, 13–25 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  69. Greer, M. D. et al. Accuracy and agreement of PIRADSv2 for prostate cancer mpMRI: a multireader study. J. Magn. Reson. Imaging 45, 579–585 (2017).

    Article  PubMed  Google Scholar 

  70. National Institute for Health and Care Excellence. Prostate cancer: diagnosis and management (NG131) (2021).

  71. Brizmohun Appayya, M. et al. Characterizing indeterminate (Likert-score 3/5) peripheral zone prostate lesions with PSA density, PI-RADS scoring and qualitative descriptors on multiparametric MRI. Br. J. Radiol. 90, 20170645 (2017).

    Article  Google Scholar 

  72. Shin, T. et al. 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 Int. 121, 77–83 (2018).

    Article  PubMed  Google Scholar 

  73. Harada, T. et al. Five-point Likert scaling on MRI predicts clinically significant prostate carcinoma. BMC Urol. 15, 1–7 (2015).

    Article  Google Scholar 

  74. Gaziev, G. et al. Defining the learning curve for multiparametric magnetic resonance imaging (MRI) of the prostate using MRI‐transrectal ultrasonography (TRUS) fusion‐guided transperineal prostate biopsies as a validation tool. BJU Int. 117, 80–86 (2016).

    Article  PubMed  Google Scholar 

  75. Barth, B. K. et al. Detection of clinically significant prostate cancer: short dual-pulse sequence versus standard multiparametric MR imaging — a multireader study. Radiology 284, 725–736 (2017).

    Article  PubMed  Google Scholar 

  76. Junker, D. et al. Comparison of multiparametric and biparametric MRI of the prostate: are gadolinium-based contrast agents needed for routine examinations? World J. Urol. 37, 691–699 (2019).

    Article  PubMed  Google Scholar 

  77. Latifoltojar, A., Appayya, M. B., Barrett, T. & Punwani, S. Similarities and differences between Likert and PIRADS v2. 1 scores of prostate multiparametric MRI: a pictorial review of histology-validated cases. Clin. Radiol. 74, 895.e1–895.e15 (2019).

    Article  CAS  PubMed  Google Scholar 

  78. Brembilla, G. et al. Diagnostic accuracy of abbreviated bi-parametric MRI (a-bpMRI) for prostate cancer detection and screening: a multi-reader study. Diagnostics 12, 231 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Marsden, T. et al. ReIMAGINE prostate cancer screening study: protocol for a single-centre feasibility study inviting men for prostate cancer screening using MRI. BMJ Open 11, e048144 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  80. Ahmed, H. U. et al. Is it time to consider a role for MRI before prostate biopsy? Nat. Rev. Clin. Oncol. 6, 197–206 (2009).

    Article  PubMed  Google Scholar 

  81. Houlahan, K. E. et al. Molecular hallmarks of multiparametric magnetic resonance imaging visibility in prostate cancer. Eur. Urol. 76, 18–23 (2019).

    Article  CAS  PubMed  Google Scholar 

  82. Venderink, W. et al. Multiparametric magnetic resonance imaging and follow‐up to avoid prostate biopsy in 4259 men. BJU Int. 124, 775–784 (2019).

    Article  PubMed  Google Scholar 

  83. Peters, M. et al. Predicting the need for biopsy to detect clinically significant prostate cancer in patients with a magnetic resonance imaging–detected prostate imaging reporting and data system/Likert≥ 3 lesion: development and multinational external validation of the imperial rapid access to prostate imaging and diagnosis risk score. Eur. Urol. 82, 559–568 (2022).

    Article  PubMed  Google Scholar 

  84. Drost, F. H. et al. Prostate magnetic resonance imaging, with or without magnetic resonance imaging-targeted biopsy, and systematic biopsy for detecting prostate cancer: a Cochrane systematic review and meta-analysis. Eur. Urol. 77, 78–94 (2020).

    Article  PubMed  Google Scholar 

  85. Rouvière, O. et al. Use of prostate systematic and targeted biopsy on the basis of multiparametric MRI in biopsy-naive patients (MRI-FIRST): a prospective, multicentre, paired diagnostic study. Lancet Oncol. 20, 100–109 (2019).

    Article  PubMed  Google Scholar 

  86. Elkhoury, F. F. et al. Comparison of targeted vs systematic prostate biopsy in men who are biopsy naive: the prospective assessment of image registration in the diagnosis of prostate cancer (PAIREDCAP) study. JAMA Surg. 154, 811–818 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  87. Miah, S. A multi-centre analysis of detection of clinically significant prostate cancer following transperineal image-fusion targeted and non-targeted systematic prostate biopsy in men at risk. Eur. Urol. Oncol. 3, 262–269 (2019).

  88. van der Leest, M. et al. Head-to-head comparison of transrectal ultrasound-guided prostate biopsy versus multiparametric prostate resonance imaging with subsequent magnetic resonance-guided biopsy in biopsy-naïve men with elevated prostate-specific antigen: a large prospective multicenter clinical study. Eur. Urol. 75, 570–578 (2018).

  89. Connor, M. J. et al. A multicentre study of the clinical utility of non-targeted systematic transperineal prostate biopsies in patients undergoing pre-biopsy mpMRI. J. Urol. https://doi.org/10.1097/JU.0000000000001184 (2020).

    Article  PubMed  Google Scholar 

  90. Kuru, T. H. et al. Definitions of terms, processes and a minimum dataset for transperineal prostate biopsies: a standardization approach of the Ginsburg Study Group for Enhanced Prostate Diagnostics. BJU Int. 112, 568–577 (2013).

    Article  PubMed  Google Scholar 

  91. Mortezavi, A. et al. Diagnostic accuracy of multiparametric magnetic resonance imaging and fusion guided targeted biopsy evaluated by transperineal template saturation prostate biopsy for the detection and characterization of prostate cancer. J. Urol. 200, 309–318 (2018).

    Article  PubMed  Google Scholar 

  92. Williams, C. et al. Why does magnetic resonance imaging-targeted biopsy miss clinically significant cancer? J. Urol. 207, 95–107 (2022).

    Article  PubMed  Google Scholar 

  93. Brisbane, W. G. et al. Targeted prostate biopsy: umbra, penumbra, and value of perilesional sampling. Eur. Urol. 82, 303–310 (2022).

  94. Miyai, K. et al. Histological differences in cancer cells, stroma, and luminal spaces strongly correlate with in vivo MRI-detectability of prostate cancer. Mod. Pathol. 32, 1536–1543 (2019).

    Article  CAS  PubMed  Google Scholar 

  95. Tan, N. et al. Characteristics of detected and missed prostate cancer foci on 3-T multiparametric MRI using an endorectal coil correlated with whole-mount thin-section histopathology. Am. J. Roentgenol. 205, W87–W92 (2015).

    Article  Google Scholar 

  96. Norris, J. M. et al. What type of prostate cancer is systematically overlooked by multiparametric magnetic resonance imaging? An analysis from the PROMIS cohort. Eur. Urol. 78, 163–170 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  97. Kuhlmann, P. K. et al. Patient-and tumor-level risk factors for MRI-invisible prostate cancer. Prostate Cancer Prostatic Dis. 24, 794–801 (2021).

    Article  PubMed  Google Scholar 

  98. Marks, L. S. Some prostate cancers are invisible to magnetic resonance imaging! BJU Int. 118, 492–493 (2016).

    Article  PubMed  Google Scholar 

  99. Schieda, N. et al. Prostatic ductal adenocarcinoma: an aggressive tumour variant unrecognized on T2 weighted magnetic resonance imaging (MRI). Eur. Radiol. 24, 1349–1356 (2014).

    Article  PubMed  Google Scholar 

  100. Truong, M. et al. A comprehensive analysis of cribriform morphology on magnetic resonance imaging/ultrasound fusion biopsy correlated with radical prostatectomy specimens. J. Urol. 199, 106–113 (2018).

    Article  PubMed  Google Scholar 

  101. Mottet, N. et al. EAU-EANM-ESTRO-ESUR-SIOG guidelines on prostate cancer — 2020 update. Part 1: screening, diagnosis, and local treatment with curative intent. Eur. Urol. 79, 243–262 (2021).

    Article  CAS  PubMed  Google Scholar 

  102. NICE. Guideline Updates Team UK. Prostate cancer: diagnosis and management. (2019).

  103. Bjurlin, M. A. et al. Update of the standard operating procedure on the use of multiparametric magnetic resonance imaging for the diagnosis, staging and management of prostate cancer. J. Urol. https://doi.org/10.1097/JU.0000000000000617 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  104. Venderink, W. et al. Multiparametric magnetic resonance imaging for the detection of clinically significant prostate cancer: what urologists need to know. Part 3: targeted biopsy. Eur. Urol. 77, 481–490 (2020).

    Article  PubMed  Google Scholar 

  105. Beyersdorff, D. et al. MR imaging-guided prostate biopsy with a closed MR unit at 1.5 T: initial results. Radiology 234, 576–581 (2005).

    Article  PubMed  Google Scholar 

  106. Venderink, W., Govers, T. M., de Rooij, M., Fütterer, J. J. & Sedelaar, J. M. Cost-effectiveness comparison of imaging-guided prostate biopsy techniques: systematic transrectal ultrasound, direct in-bore MRI, and image fusion. Am. J. Roentgenol. 208, 1058–1063 (2017).

    Article  Google Scholar 

  107. Overduin, C. G., Fütterer, J. J. & Barentsz, J. O. MRI-guided biopsy for prostate cancer detection: a systematic review of current clinical results. Curr. Urol. Rep. 14, 209–213 (2013).

    Article  PubMed  Google Scholar 

  108. Siddiqui, M. M. et al. Comparison of MR/ultrasound fusion-guided biopsy with ultrasound-guided biopsy for the diagnosis of prostate cancer. JAMA 313, 390–397 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Hamid, S. et al. The SmartTarget biopsy trial: a prospective, within-person randomised, blinded trial comparing the accuracy of visual-registration and magnetic resonance imaging/ultrasound image-fusion targeted biopsies for prostate cancer risk stratification. Eur. Urol. 75, 733–740 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  110. Natarajan, S. et al. Clinical Application of a 3D Ultrasound-Guided Prostate Biopsy System (Elsevier, 2011).

  111. Meng, X. et al. The institutional learning curve of magnetic resonance imaging-ultrasound fusion targeted prostate biopsy: temporal improvements in cancer detection in 4 years. J. Urol. 200, 1022–1029 (2018).

    Article  PubMed  Google Scholar 

  112. Wegelin, O. et al. The FUTURE Trial: a multicenter randomised controlled trial on target biopsy techniques based on magnetic resonance imaging in the diagnosis of prostate cancer in patients with prior negative biopsies. Eur. Urol. 75, 582–590 (2018).

  113. Kwak, J. T. et al. Is visual registration equivalent to semiautomated registration in prostate biopsy? Biomed. Res. Int. 2015, 394742 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  114. Connor, M. J., Gorin, M. A., Ahmed, H. U. & Nigam, R. Focal therapy for localized prostate cancer in the era of routine multi-parametric MRI. Prostate Cancer Prostatic Dis. 23, 232–243 (2020).

    Article  CAS  PubMed  Google Scholar 

  115. Natarajan, S. et al. Clinical Application of a 3D Ultrasound-Guided Prostate Biopsy System (Elsevier, 2011).

  116. Kaplan, I. et al. Real time MRI-ultrasound image guided stereotactic prostate biopsy. Magn. Reson. Imaging 20, 295–299 (2002).

    Article  PubMed  Google Scholar 

  117. Sarkar, S. & Das, S. A review of imaging methods for prostate cancer detection: supplementary issue: image and video acquisition and processing for clinical applications. Biomed. Eng. Comput. Biol. 7, BECB. S34255 (2016).

    Article  Google Scholar 

  118. Wajswol, E. et al. A cohort of transperineal electromagnetically tracked magnetic resonance imaging/ultrasonography fusion‐guided biopsy: assessing the impact of inter‐reader variability on cancer detection. BJU Int. 125, 531–540 (2020).

    Article  CAS  PubMed  Google Scholar 

  119. Venderink, W., de Rooij, M., Sedelaar, J. M., Huisman, H. J. & Fütterer, J. J. Elastic versus rigid image registration in magnetic resonance imaging–transrectal ultrasound fusion prostate biopsy: a systematic review and meta-analysis. Eur. Urol. Focus. 4, 219–227 (2018).

    Article  PubMed  Google Scholar 

  120. Wysock, J. S. et al. 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. 66, 343–351 (2014).

    Article  PubMed  Google Scholar 

  121. Bass, E. J. et al. Diagnostic accuracy of magnetic resonance imaging targeted biopsy techniques compared to transrectal ultrasound guided biopsy of the prostate: a systematic review and meta-analysis. Prostate Cancer Prostatic Dis. 25, 174–179 (2022).

    Article  CAS  PubMed  Google Scholar 

  122. Johansen, T. E. B. et al. Antibiotic resistance, hospitalizations, and mortality related to prostate biopsy: first report from the Norwegian Patient Registry. World J. Urol. 38, 17–26 (2020).

    Article  PubMed  Google Scholar 

  123. Pepdjonovic, L. et al. Zero hospital admissions for infection after 577 transperineal prostate biopsies using single-dose cephazolin prophylaxis. World J. Urol. 35, 1199–1203 (2017).

    Article  CAS  PubMed  Google Scholar 

  124. Loeb, S. et al. Systematic review of complications of prostate biopsy. Eur. Urol. 64, 876–892 (2013).

    Article  PubMed  Google Scholar 

  125. Miah, S. et al. A multicentre analysis of the detection of clinically significant prostate cancer following transperineal image-fusion targeted and nontargeted systematic prostate biopsy in men at risk. Eur. Urol. Oncol. 3, 262–269 (2019).

    Article  PubMed  Google Scholar 

  126. Stefanova, V. et al. Transperineal prostate biopsies using local anesthesia: experience with 1,287 patients. Prostate cancer detection rate, complications and patient tolerability. J. Urol. 201, 1121–1126 (2019).

    Article  PubMed  Google Scholar 

  127. Grummet, J. et al. “TREXIT 2020”: why the time to abandon transrectal prostate biopsy starts now. Prostate Cancer Prostatic Dis. 23, 62–65 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  128. Wright, J. L. & Ellis, W. J. Improved prostate cancer detection with anterior apical prostate biopsies (Elsevier, 2006).

  129. Kawakami, S. et al. Transrectal ultrasound‐guided transperineal 14‐core systematic biopsy detects apico‐anterior cancer foci of T1c prostate cancer. Int. J. Urol. 11, 613–618 (2004).

    Article  PubMed  Google Scholar 

  130. Takashima, R., Egawa, S., Kuwao, S. & Baba, S. Anterior distribution of Stage T1c nonpalpable tumors in radical prostatectomy specimens. Urology 59, 692–697 (2002).

    Article  PubMed  Google Scholar 

  131. Merrick, G. S. et al. Prostate cancer distribution in patients diagnosed by transperineal template-guided saturation biopsy. Eur. Urol. 52, 715–724 (2007).

    Article  PubMed  Google Scholar 

  132. Nix, J. W. et al. Very distal apical prostate tumours: identification on multiparametric MRI at 3 Tesla. BJU Int. 110, E694–E700 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  133. US National Library of Medicine. ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/NCT05179694 (2022).

  134. Holm, H. H. & Gammelgaard, J. Ultrasonically guided precise needle placement in the prostate and the seminal vesicles. J. Urol. 125, 385–387 (1981).

    Article  CAS  PubMed  Google Scholar 

  135. Filderman, P. S. & Jacobs, S. C. Prostatic ultrasound in the patient without a rectum. Urology 43, 722–724 (1994).

    Article  CAS  PubMed  Google Scholar 

  136. Yamamoto, S. et al. Transperineal ultrasound-guided 12-core systematic biopsy of the prostate for patients with a prostate-specific antigen level of 2.5–20 ng/ml in Japan. Int. J. Clin. Oncol. 10, 117–121 (2005).

    Article  PubMed  Google Scholar 

  137. Barzell, W. E. & Whitmore, W. F. Transperineal template guided saturation biopsy of the prostate: rationale, indications and technique. Urol. Times 31, 41–42 (2003).

    Google Scholar 

  138. Barzell, W. E. & Melamed, M. R. 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, S27–S35 (2007).

    Article  Google Scholar 

  139. Simmons, L. A. et al. Accuracy of transperineal targeted prostate biopsies, visual estimation and image fusion in men needing repeat biopsy in the picture trial. J. Urol. 200, 1227–1234 (2018).

    Article  PubMed  Google Scholar 

  140. Bott, S. R. et al. Extensive transperineal template biopsies of prostate: modified technique and results. Urology 68, 1037–1041 (2006).

    Article  PubMed  Google Scholar 

  141. Moran, B. J. & Braccioforte, M. H. Stereotactic transperineal prostate biopsy. Urology 73, 386–388 (2009).

    Article  PubMed  Google Scholar 

  142. Gershman, B., Zietman, A. L., Feldman, A. S. & McDougal, W. S. Transperineal Template-Guided Prostate Biopsy for Patients with Persistently Elevated PSA and Multiple Prior Negative Biopsies (Elsevier, 2013).

  143. Miah, S. et al. Patient reported outcome measures for transperineal template prostate mapping biopsies in the PICTURE study. J. Urol. 200, 1235–1240 (2018).

    Article  PubMed  Google Scholar 

  144. Connor, M. et al. Value of systematic sampling in an mp-MRI targeted prostate biopsy strategy. Transl. Androl. Urol. 9, 1501–1509 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  145. Zimmerman, M. E., Meyer, A. R., Carter, H. B., Allaf, M. E. & Gorin, M. A. In-office transperineal prostate biopsy using biplanar ultrasound guidance: a step-by-step guide. Urology 133, 247 (2019).

    Article  PubMed  Google Scholar 

  146. Radtke, J. P. et al. Multiparametric magnetic resonance imaging (MRI) and MRI–transrectal ultrasound fusion biopsy for index tumor detection: correlation with radical prostatectomy specimen. Eur. Urol. 70, 846–853 (2016).

    Article  PubMed  Google Scholar 

  147. Emiliozzi, P. et al. The value of a single biopsy with 12 transperineal cores for detecting prostate cancer in patients with elevated prostate specific antigen. J. Urol. 166, 845–850 (2001).

    Article  CAS  PubMed  Google Scholar 

  148. Meyer, A. R. et al. Initial experience performing in-office ultrasound-guided transperineal prostate biopsy under local anesthesia using the PrecisionPoint Transperineal Access System. Urology 115, 8–13 (2018).

    Article  PubMed  Google Scholar 

  149. Lee, J. J. et al. Biologic differences between peripheral and transition zone prostate cancer. Prostate 75, 183–190 (2015).

    Article  PubMed  Google Scholar 

  150. Cohen, R. J. et al. Central zone carcinoma of the prostate gland: a distinct tumor type with poor prognostic features. J. Urol. 179, 1762–1767 (2008).

    Article  PubMed  Google Scholar 

  151. van Houdt, P. J. et al. Histopathological features of MRI‐invisible regions of prostate cancer lesions. J. Magn. Reson. Imaging 51, 1235–1246 (2020).

    Article  PubMed  Google Scholar 

  152. Bass, E. J. et al. Magnetic resonance imaging targeted transperineal prostate biopsy: a local anaesthetic approach. Prostate Cancer Prostatic Dis. 20, 311–317 (2017).

    Article  CAS  PubMed  Google Scholar 

  153. Corey, G. et al. UK & Ireland Prostate Brachytherapy Practice Survey 2014–2016. J. Contemp. Brachytherapy 10, 238–245 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  154. National Institute for Health and Care Excellence. Diagnostics Consultation Document Transperineal Biopsy for Diagnosing Prostate Cancer GID-DG10043 (2022).

  155. Szabo, R. J. “Free-Hand” transperineal prostate biopsy under local anesthesia: review of the literature. J. Endourol. 35, 525–543 (2021).

    Article  PubMed  Google Scholar 

  156. Gnanapragasam, V. J. et al. Multicentre clinical evaluation of the safety and performance of a simple transperineal access system for prostate biopsies for suspected prostate cancer: The CAMbridge PROstate Biopsy DevicE (CamPROBE) study. J. Clin. Urol. 13, 364–370 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  157. Gorin, M. A. et al. Transperineal prostate biopsy with cognitive magnetic resonance imaging/biplanar ultrasound fusion: description of technique and early results. World J. Urol. 38, 1943–1949 (2020).

    Article  PubMed  Google Scholar 

  158. Kum, F. et al. Initial outcomes of local anaesthetic freehand transperineal prostate biopsies in the outpatient setting. BJU Int. 125, 244–252 (2020).

    Article  CAS  PubMed  Google Scholar 

  159. Ristau, B. T. et al. Free-Hand Transperineal Prostate Biopsy Provides Acceptable Cancer Detection and Minimizes Risk of Infection: Evolving Experience with a 10-Sector Template (Elsevier, 2018).

  160. Jacewicz, M. et al. Multicenter transperineal MRI-TRUS fusion guided outpatient clinic prostate biopsies under local anesthesia. Urol. Oncol. 39, 432.e1–432.e7 (2020).

  161. Ferraro, D. A. et al. Diagnostic performance of 68Ga-PSMA-11 PET/MRI-guided biopsy in patients with suspected prostate cancer: a prospective single-center study. Eur. J. Nucl. Med. Mol. Imaging 48, 3315–3324 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  162. Meyer, A. R., Leroy, A., Allaf, M. E., Rowe, S. P. & Gorin, M. A. Incidentally detected 18F-FDG-Avid prostate cancer diagnosed using a novel fusion biopsy platform. J. Endourol. Case Rep. 5, 68–70 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  163. Le-Le, Z. et al. 68Ga-PSMA PET/CT targeted biopsy for the diagnosis of clinically significant prostate cancer compared with transrectal ultrasound guided biopsy: a prospective randomized single-centre study. Eur. J. Nucl. Med. Mol. Imaging 48, 483–492 (2021).

    Article  Google Scholar 

  164. Fei, B., Nieh, P. T., Schuster, D. M. & Master, V. A. PET-directed, 3D ultrasound-guided prostate biopsy. Diagn. Imaging Eur. 29, 12 (2013).

    PubMed  PubMed Central  Google Scholar 

  165. Turkbey, B. et al. Localized prostate cancer detection with 18F FACBC PET/CT: comparison with MR imaging and histopathologic analysis. Radiology 270, 849–856 (2014).

    Article  PubMed  Google Scholar 

  166. Ross, J. S. et al. Correlation of primary tumor prostate-specific membrane antigen expression with disease recurrence in prostate cancer. Clin. Cancer Res. 9, 6357–6362 (2003).

    CAS  PubMed  Google Scholar 

  167. Hofman, M. S. et al. Prostate-specific membrane antigen PET-CT in patients with high-risk prostate cancer before curative-intent surgery or radiotherapy (proPSMA): a prospective, randomised, multi-centre study. Lancet 395, 1208–1216 (2020).

    Article  CAS  PubMed  Google Scholar 

  168. Perera, M. et al. Sensitivity, specificity, and predictors of positive 68Ga–prostate-specific membrane antigen positron emission tomography in advanced prostate cancer: a systematic review and meta-analysis. Eur. Urol. 70, 926–937 (2016).

    Article  PubMed  Google Scholar 

  169. Connor, M. J. et al. Clinical translation of positive metastases identified on prostate-specific membrane antigen positron emission tomography/computed tomography imaging in the management of de novo synchronous oligometastatic prostate cancer. Eur. Urol. Focus. 7, 951–954 (2021).

  170. Emmett, L. et al. The additive diagnostic value of prostate-specific membrane antigen positron emission tomography computed tomography to multiparametric magnetic resonance imaging triage in the diagnosis of prostate cancer (PRIMARY): a prospective multicentre study. Eur. Urol. 80, 682–689 (2021).

    Article  CAS  PubMed  Google Scholar 

  171. Pouliot, F. et al. A prospective phase II/III multicenter study of PSMA-targeted 18F-DCFPyL PET/CT imaging in patients with prostate cancer (OSPREY): a sub-analysis of regional and distant metastases detection rates at initial staging by 18F-DCFPyL PET/CT. Am. Soc. Clin. Oncol. 38, 9 (2020).

    Article  Google Scholar 

  172. Yildirim, Ö. A., Gündoğan, C., Can, C., Erdur, E. & Kömek, H. Correlations between whole body volumetric parameters of 68Ga-PSMA PET/CT and biochemical-histopathological parameters in castration-naive and resistant prostate cancer patients. Ann. Nucl. Med. 35, 540–548 (2021).

    Article  CAS  PubMed  Google Scholar 

  173. Light, A., Ahmed, H. U. & Shah, T. T. The unclear role of PET–CT in localized radiorecurrent prostate cancer. Nat. Rev. Urol. 19, 573–574 (2022).

    Article  PubMed  Google Scholar 

  174. Seitz, A. K. et al. Preliminary results on response assessment using 68Ga-HBED-CC-PSMA PET/CT in patients with metastatic prostate cancer undergoing docetaxel chemotherapy. Eur. J. Nucl. Med. Mol. imaging 45, 602–612 (2018).

    Article  CAS  PubMed  Google Scholar 

  175. Khreish, F. et al. Response assessment and prediction of progression-free survival by 68Ga-PSMA-11 PET/CT based on tumor-to-liver ratio (TLR) in patients with mCRPC undergoing 177Lu-PSMA-617 radioligand therapy. Biomolecules 11, 1099 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Wenzel, M., Hoeh, B., Mandel, P. & Chun, F. K. Diagnosis of clinically significant prostate cancer diagnosis without histological proof in the prostate-specific membrane antigen era: the jury is still out. Eur. Urol. Open Sci. 45, 50–51 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  177. Kesch, C. et al. Correlation between genomic index lesions and mpMRI and 68Ga-PSMA-PET/CT imaging features in primary prostate cancer. Sci. Rep. 8, 1–8 (2018).

    Article  CAS  Google Scholar 

  178. Zamboglou, C. et al. Radiomic features from PSMA PET for non-invasive intraprostatic tumor discrimination and characterization in patients with intermediate-and high-risk prostate cancer — a comparison study with histology reference. Theranostics 9, 2595 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Cohen, W. M. & Levinthal, D. A. Innovation and learning: the two faces of R & D. Econ. J. 99, 569–596 (1989).

    Article  Google Scholar 

  180. US National Library of Medicine. ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/results/NCT03429244 (2022).

  181. Zettinig, O. et al. Multimodal image-guided prostate fusion biopsy based on automatic deformable registration. Int. J. Comput. Assist. Radiol. Surg. 10, 1997–2007 (2015).

    Article  PubMed  Google Scholar 

  182. Minner, S. et al. High level PSMA expression is associated with early PSA recurrence in surgically treated prostate cancer. Prostate 71, 281–288 (2011).

    Article  PubMed  Google Scholar 

  183. Chen, M. et al. Combination of 68Ga-PSMA PET/CT and multiparametric MRI improves the detection of clinically significant prostate cancer: a lesion-by-lesion analysis. J. Nucl. Med. 60, 944–949 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Fei, B. et al. Feasibility and initial results: fluciclovine positron emission tomography/ultrasound fusion targeted biopsy of recurrent prostate cancer. J. Urol. 202, 413–421 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  185. NICE. Axumin for functional imaging of prostate cancer recurrence Medtech innovation briefing [MIB172]. (2019).

  186. Ho, H., Yuen, J., Mohan, P., Lim, E. W. & Cheng, C. Robotic transperineal prostate biopsy: pilot clinical study. Urology 78, 1203–1208 (2011).

    Article  CAS  PubMed  Google Scholar 

  187. Kaufmann, S. et al. First report of robot-assisted transperineal fusion versus off-target biopsy in patients undergoing repeat prostate biopsy. World J. Urol. 35, 1023–1029 (2017).

    Article  CAS  PubMed  Google Scholar 

  188. Patel, M. I., Muter, S., Vladica, P. & Gillatt, D. Robotic-assisted magnetic resonance imaging ultrasound fusion results in higher significant cancer detection compared to cognitive prostate targeting in biopsy naive men. Transl. Androl. Urol. 9, 601 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  189. Connor, M. J., Dasgupta, P., Ahmed, H. U. & Raza, A. Autonomous surgery in the era of robotic urology: friend or foe of the future surgeon? Nat. Rev. Urol. 17, 643–649 (2020).

    Article  PubMed  Google Scholar 

  190. Miah, S. et al. A prospective analysis of robotic targeted MRI-US fusion prostate biopsy using the centroid targeting approach. J. Robotic Surg. 14, 69–74 (2020).

    Article  Google Scholar 

  191. Sountoulides, P. et al. Micro-ultrasound-guided vs multiparametric magnetic resonance imaging-targeted biopsy in the detection of prostate cancer: a systematic review and meta-analysis. J. Urol. 205, 1254–1262 (2021).

    Article  PubMed  Google Scholar 

  192. Grey, A. D. et al. Multiparametric ultrasound versus multiparametric MRI to diagnose prostate cancer (CADMUS): a prospective, multicentre, paired-cohort, confirmatory study. Lancet Oncol. 23, 428–438 (2022).

    Article  PubMed  Google Scholar 

  193. Saita, A. et al. Assessing the feasibility and accuracy of high-resolution microultrasound imaging for bladder cancer detection and staging. Eur. Urol. 77, 727–732 (2020).

    Article  PubMed  Google Scholar 

  194. Klotz, L. et al. Optimization of prostate biopsy-micro-ultrasound versus MRI (OPTIMUM): A 3-arm randomized controlled trial evaluating the role of 29 MHz micro-ultrasound in guiding prostate biopsy in men with clinical suspicion of prostate cancer. Contemp. Clin. Trials 112, 106618 (2022).

    Article  PubMed  Google Scholar 

  195. Garrido, M. M., Bernardino, R. M., Marta, J. C., Holdenrieder, S. & Guimarães, J. T. Tumour markers in prostate cancer: the post-prostate-specific antigen era. Ann. Clin. Biochem. 59, 46–58 (2022).

    Article  CAS  PubMed  Google Scholar 

  196. Eldred-Evans, D. et al. Population-based prostate cancer screening with magnetic resonance imaging or ultrasonography: the IP1-PROSTAGRAM study. JAMA Oncol. 7, 395–402 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  197. National Comprehensive Cancer Network, (NCCN). NCCN guidelines version 2.2019 prostate cancer early detection. (2019).

  198. Vickers, A. J. et al. A four-kallikrein panel predicts prostate cancer in men with recent screening: data from the European Randomized Study of Screening for Prostate Cancer, Rotterdam. Clin. Cancer Res. 16, 3232–3239 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. Vickers, A. J. et al. A panel of kallikrein markers can reduce unnecessary biopsy for prostate cancer: data from the European Randomized Study of Prostate Cancer Screening in Göteborg, Sweden. BMC Med. 6, 1–10 (2008).

    Article  Google Scholar 

  200. Filella, X. & Giménez, N. Evaluation of [−2] proPSA and Prostate Health Index (phi) for the detection of prostate cancer: a systematic review and meta-analysis. Clin. Chem. Lab. Med. 51, 729–739 (2013).

    Article  CAS  PubMed  Google Scholar 

  201. Ferro, M. et al. Prostate Health Index and Multiparametric MRI: partners in crime fighting overdiagnosis and overtreatment in prostate cancer. Cancers 13, 4723 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  202. Nash, P. A., Bruce, J. E., Indudhara, R. & Shinohara, K. Transrectal ultrasound guided prostatic nerve blockade eases systematic needle biopsy of the prostate. J. Urol. 155, 607–609 (1996).

    Article  CAS  PubMed  Google Scholar 

  203. Millin, T. Retropubic prostatectomy a new extravesical technique: report on 20 cases. Lancet 246, 693–696 (1945).

    Article  Google Scholar 

  204. Abbou, C. et al. Laparoscopic radical prostatectomy with a remote controlled robot. J. Urol. 165, 1964–1966 (2001).

    Article  CAS  PubMed  Google Scholar 

  205. Wang, M. C., Valenzuela, L. A., Murphy, G. P. & Chu, T. M. Purification of a human prostate specific antigen. Invest. Urol. 17, 159–163 (1979).

    CAS  PubMed  Google Scholar 

  206. Demura, T. et al. Differences in tumor core distribution between palpable and nonpalpable prostate tumors in patients diagnosed using extensive transperineal ultrasound‐guided template prostate biopsy. Cancer 103, 1826–1832 (2005).

    Article  PubMed  Google Scholar 

  207. Haffner, J. et al. Role of magnetic resonance imaging before initial biopsy: comparison of magnetic resonance imaging‐targeted and systematic biopsy for significant prostate cancer detection. BJU Int. 108, E171–E178 (2011).

    Article  PubMed  Google Scholar 

  208. Devonec, M. et al. The significance of the prostatic hypoechoic area: results in 226 ultrasonically guided prostatic biopsies. J. Urol. 143, 316–319 (1990).

    Article  CAS  PubMed  Google Scholar 

  209. Peirson, E. L. & Nickerson, D. A. Biopsy of the prostate with the Silverman needle. N. Engl. J. Med. 228, 675–678 (1943).

    Article  Google Scholar 

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Authors and Affiliations

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Contributions

M.J.C. and D.E.-E. researched data for the article. M.J.C., D.E.-E., A.D., T.D., M.W. and H.U.A. contributed substantially to discussion of the content. M.J.C., M.A.G., D.E.-E., E.J.B., and A.D. wrote the article. M.J.C., M.A.G., D.E.-E., E.J.B., T.D., M.W. and H.U.A. reviewed and/or edited the manuscript before submission.

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Correspondence to Martin J. Connor.

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Competing interests

M.A.G. is a paid consultant for bk Medical ApS, KOELIS, and Perineologic. H.U.A. currently receives funding from Sonacare Inc., Trod Medical and Sophiris Biocorp for trials and studies in prostate cancer and is a paid medical consultant for Sophiris Biocorp, Sonacare Inc. and BTG/Galil, and a paid proctor for HIFU, cryotherapy and Rezum water vapour therapy. The other authors declare no competing interests.

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Glossary

Apparent diffusion coefficient

(ADC). ADC measures the magnitude of diffusion (of water molecules) within tissue.

Biplanar TRUS

In biplanar TRUS, a transrectal ultrasonography probe provides a longitudinal and transverse view.

Brachytherapy grid

Template grids consisting of rows and columns of holes, traditionally spaced 5 mm apart.

Brachytherapy stepper

Classic stabilizers for TRUS probes that provide six degrees of freedom of movement including X, Y and Z axis plus pitch, yaw and roll.

Cognitive-fusion

In cognitive-fusion, the operator interprets information from the patient’s MRI to target lesions during biopsy that might or might not be visible on ultrasonography.

Diffusion-weighting imaging

(DWI). DWI is a form of MR imaging based on measuring the random Brownian motion of water molecules within a voxel of tissue.

Freehand technique

For freehand biopsy, the needle is guided to the target with one hand whereas the other hand positions the ultrasonography transducer for adequate visualization.

Screw-tip

A screw-tip needle consists of a wide-bore needle that is rotated clockwise inside a sheath to activate. This motion results in tissue acquisition.

Software-fusion

In software-fusion, the operator uses software to overlay the MRI with TRUS images obtained at the time of biopsy sampling to generate a fused 3D computer model for use in real-time guidance of biopsy sampling.

Spectroscopy

Spectroscopy enables tissue to be interrogated for the presence and concentration of various metabolites identical to that of nuclear magnetic resonance.

Steady-state free precession image

A type of gradient echo MRI pulse sequence in which a steady, residual transverse magnetization (Mxy) is maintained between successive cycles.

SUVmax

A measure of the maximum standardized uptake value of a radiotracer by (malignant) tissue.

T2WI

T2-weighted images are basic pulse sequences representing the difference in the T2 relaxation time of tissues.

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Connor, M.J., Gorin, M.A., Eldred-Evans, D. et al. Landmarks in the evolution of prostate biopsy. Nat Rev Urol 20, 241–258 (2023). https://doi.org/10.1038/s41585-022-00684-0

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