Woodrum-MR-guided focal therapy for native and recurrent prostate cancer

Main Article Content

David A. Woodrum Stephanie Zawada Lance A. Mynderse

Abstract

This manuscript presents a current review of the importance of MR imaging, biopsy and ablation for treatment of prostate cancer either early native disease or recurrent prostate cancer after surgery or radiation. Prostate cancer is the most common cancer diagnosis for men, with approximately 35,000 men dying from it each year in the United States1. Many men with prostate cancer are often managed with aggressive therapy including radiotherapy or surgery.  No matter how expertly done, these therapies carry significant risk and morbidity to the patient’s health-related quality of life with impact on sexual, urinary, and bowel function2. Furthermore, screening programs using prostatic specific antigen (PSA) and transrectal ultrasound (TRUS) guided systematic biopsy have increasingly identified patients earlier, in the low-risk, low-grade “localized” prostate cancer categories.  The indolent nature of many prostate cancers presents a difficult decision of when to intervene given the possible comorbidities and side effects of aggressive treatment.  Active surveillance has been increasingly instituted to balance cancer control versus treatment side effects3. Although active debate continues on the suitability of focal or regional therapy for these low- or intermediate-risk prostate cancer patients, many unresolved issues remain which complicate this approach of management. Some of the largest unresolved issues are: prostate cancer multifocality, limitations of current biopsy strategies, suboptimal staging by accepted imaging modalities, less than robust prediction models for indolent prostate cancers, and whether established curative therapies can be safely and effectively used following focal therapy for prostate cancer. Despite these restrictions, focal therapy continues to confront the current paradigm of therapy for low- and even intermediate-risk disease4. Therefore, accurate assessment of cancer risk (i.e. grade and stage) using imaging and targeted biopsy is critical. Advances in prostate imaging with MRI have been accompanied with advances in MR-guided therapy, propelling prostate treatment solutions forward faster than ever. The following manuscript reviews the current state of MR imaging, biopsy and MR-guided prostate ablations for native and recurrent prostate cancer using laser ablation, cryoablation, and focused ultrasound.

Keywords: Prostate cancer, MR-guided therapy, Focal therapy, Prostate biopsy, Prostate ablation, Laser ablation, Cryoablation, Focused ultrasound, Prostate cancer recurrence, Prostate MRI

Article Details

How to Cite
WOODRUM, David A.; ZAWADA, Stephanie; MYNDERSE, Lance A.. Woodrum-MR-guided focal therapy for native and recurrent prostate cancer. Medical Research Archives, [S.l.], v. 12, n. 9, sep. 2024. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/5779>. Date accessed: 27 dec. 2024. doi: https://doi.org/10.18103/mra.v12i9.5779.
Section
Review Articles

References

1. Siegel RL, Giaquinto AN, Jemal A. Cancer statistics, 2024. CA Cancer J Clin. Jan-Feb 2024;74 (1):12-49. doi:10.3322/caac.21820

2. Potosky AL, Davis WW, Hoffman RM, et al. Five-year outcomes after prostatectomy or radiotherapy for prostate cancer: the prostate cancer outcomes study.[see comment]. Journal of the National Cancer Institute. Sep 15 Sep 15 2004;96(18):1358-67.

3. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2006. CA Cancer J Clin. Mar-Apr 2006;56 (2):106-30. doi:10.3322/canjclin.56.2.106

4. Vickers AJ, Ulmert D, Sjoberg DD, et al. Strategy for detection of prostate cancer based on relation between prostate specific antigen at age 40-55 and long term risk of metastasis: case-control study. BMJ. 2013;346:f2023.

5. Miller KD, Siegel RL, Lin CC, et al. Cancer treatment and survivorship statistics, 2016. CA: a Cancer Journal for Clinicians. Jul 2016;66(4):271-89. doi:10.3322/caac.21349

6. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA: a Cancer Journal for Clinicians. Jan 2015;65(1):5-29. doi:10.3322/caac.21254

7. Onik G. Rationale for a "male lumpectomy," a prostate cancer targeted approach using cryoablation: results in 21 patients with at least 2 years of follow-up. Cardiovascular & Interventional Radiology. Jan-Feb Jan-Feb 2008;31(1):98-106.

8. Bill-Axelson A, Holmberg L, Garmo H, et al. Radical prostatectomy or watchful waiting in early prostate cancer. N Engl J Med. Mar 6 2014;370(10) :932-42. doi:10.1056/NEJMoa1311593

9. Hambrock T, Somford DM, Huisman HJ, et al. Relationship between apparent diffusion coefficients at 3.0-T MR imaging and Gleason grade in peripheral zone prostate cancer. Radiology. May 2011;259(2):453-61. doi:10.1148 /radiol.11091409

10. Muller BG, Futterer JJ, Gupta RT, et al. The role of magnetic resonance imaging (MRI) in focal therapy for prostate cancer: recommendations from a consensus panel. BJU Int. Feb 2014;113 (2):218-27. doi:10.1111/bju.12243

11. Spektor M, Mathur M, Weinreb JC. Standards for MRI reporting-the evolution to PI-RADS v 2.0. Transl Androl Urol. Jun 2017;6(3):355-367. doi:10.2 1037/tau.2017.01.02

12. Siddiqui MM, Rais-Bahrami S, Turkbey B, et al. Comparison of MR/ultrasound fusion-guided biopsy with ultrasound-guided biopsy for the diagnosis of prostate cancer. JAMA. Jan 27 2015;313(4):390-7. doi:10.1001/jama.2014.17942

13. Stabile A, Giganti F, Rosenkrantz AB, et al. Multiparametric MRI for prostate cancer diagnosis: current status and future directions. Nat Rev Urol. Jan 2020;17(1):41-61. doi:10.1038/s41585-019-0212-4

14. Chiam K, Carle C, Hughes S, et al. Use of multiparametric magnetic resonance imaging (mpMRI) in active surveillance for low-risk prostate cancer: a scoping review on the benefits and harm of mpMRI in different biopsy scenarios. Prostate Cancer Prostatic Dis. Sep 2021;24(3):662-673. doi:10.1038/s41391-021-00320-9

15. Reske SN, Blumstein NM, Glatting G. [11C]choline PET/CT imaging in occult local relapse of prostate cancer after radical prostatectomy. Eur J Nucl Med Mol Imaging. Jan 2008;35(1):9-17. doi:10.1007/s00259-007-0530-2

16. Kitajima K, Murphy RC, Nathan MA, et al. Detection of recurrent prostate cancer after radical prostatectomy: comparison of 11C-choline PET/CT with pelvic multiparametric MR imaging with endorectal coil. J Nucl Med. Feb 2014;55(2):223-32. doi:10.2967/jnumed.113.123018

17. Parker WP, Davis BJ, Park SS, et al. Identification of Site-specific Recurrence Following Primary Radiation Therapy for Prostate Cancer Using C-11 Choline Positron Emission Tomography /Computed Tomography: A Nomogram for Predicting Extrapelvic Disease. Eur Urol. Mar 2017;71(3):340-348. doi:10.1016/j.eururo.2016.08.055

18. Corfield J, Perera M, Bolton D, Lawrentschuk N. (68)Ga-prostate specific membrane antigen (PSMA) positron emission tomography (PET) for primary staging of high-risk prostate cancer: a systematic review. World J Urol. Apr 2018;36 (4):519-527. doi:10.1007/s00345-018-2182-1

19. Afshar-Oromieh A, Holland-Letz T, Giesel FL, et al. Diagnostic performance of (68)Ga-PSMA-11 (HBED-CC) PET/CT in patients with recurrent prostate cancer: evaluation in 1007 patients. Eur J Nucl Med Mol Imaging. Aug 2017;44(8):1258-1268. doi:10.1007/s00259-017-3711-7

20. Wieder H, Beer AJ, Holzapfel K, et al. 11C-choline PET/CT and whole-body MRI including diffusion-weighted imaging for patients with recurrent prostate cancer. Oncotarget. Sep 12 2017;8(39):66516-66527. doi:10.18632/oncotarget.16227

21. Scobioala S, Kittel C, Wolters H, et al. Diagnostic efficiency of hybrid imaging using PSMA ligands, PET/CT, PET/MRI and MRI in identifying malignant prostate lesions. Ann Nucl Med. May 2021;35(5):628-638. doi:10.1007/s1214 9-021-01606-7

22. Hodge KK, McNeal JE, Terris MK, Stamey TA. Random systematic versus directed ultrasound guided transrectal core biopsies of the prostate. J Urol. Jul 1989;142(1):71-4; discussion 74-5. doi:10. 1016/s0022-5347(17)38664-0

23. 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. May 2006;175(5):1605-12. doi:10.1016/S0022-5347(05) 00957-2

24. Jones JS. Saturation biopsy for detecting and characterizing prostate cancer. BJU Int. Jun 2007 ;99(6):1340-4. doi:10.1111/j.1464-410X.2007.06868.x

25. Lane BR, Zippe CD, Abouassaly R, Schoenfield L, Magi-Galluzzi C, Jones JS. Saturation technique does not decrease cancer detection during followup after initial prostate biopsy. J Urol. May 2008;179(5):1746-50; discussion 1750. doi:10.1016 /j.juro.2008.01.049

26. Nelson AW, Harvey RC, Parker RA, Kastner C, Doble A, Gnanapragasam VJ. Repeat prostate biopsy strategies after initial negative biopsy: meta-regression comparing cancer detection of transperineal, transrectal saturation and MRI guided biopsy. PLoS One. 2013;8(2):e57480. doi:10.1371/journal.pone.0057480

27. Ahmed HU, Emberton M, Kepner G, Kepner J. A biomedical engineering approach to mitigate the errors of prostate biopsy. Nat Rev Urol. Feb 7 2012;9(4):227-31. doi:10.1038/nrurol.2012.3

28. Salami SS, Ben-Levi E, Yaskiv O, et al. In patients with a previous negative prostate biopsy and a suspicious lesion on magnetic resonance imaging, is a 12-core biopsy still necessary in addition to a targeted biopsy? BJU Int. Apr 2015;115(4):562-70. doi:10.1111/bju.12938

29. Bhanji Y, Allaway MJ, Gorin MA. Recent Advances and Current Role of Transperineal Prostate Biopsy. Urol Clin North Am. Feb 2021;48 (1):25-33. doi:10.1016/j.ucl.2020.09.010

30. Thomson A, Li M, Grummet J, Sengupta S. Transperineal prostate biopsy: a review of technique. Transl Androl Urol. Dec 2020;9(6):3009-3017. doi:10.21037/tau.2019.12.40

31. Arumainayagam N, Ahmed HU, Moore CM, et al. Multiparametric MR imaging for detection of clinically significant prostate cancer: a validation cohort study with transperineal template prostate mapping as the reference standard. Radiology. Sep 2013;268(3):761-9. doi:10.1148/radiol.13120641

32. Ahmed HU, Kirkham A, Arya M, et al. Is it time to consider a role for MRI before prostate biopsy? Nat Rev Clin Oncol. Apr 2009;6(4):197-206. doi:10. 1038/nrclinonc.2009.18

33. Kong M, Lee L, Mulcahy K, Rajesh A. A single centre service evaluation of the pre-biopsy mpMRI pathway for prostate cancer diagnosis. Journal of Clinical Urology. 2023;16(5):478-489. doi:10.1177/ 20514158211065946

34. Bryant RJ, Hobbs CP, Eyre KS, et al. Comparison of Prostate Biopsy with or without Prebiopsy Multiparametric Magnetic Resonance Imaging for Prostate Cancer Detection: An Observational Cohort Study. J Urol. Mar 2019; 201(3):510-519. doi:10.1016/j.juro.2018.09.049

35. Haffner J, Lemaitre L, Puech P, 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. Oct 2011;108(8 Pt 2):E171-8. doi:10.1111/j.1464-410X.2011.10112.x

36. Valerio M, McCartan N, Freeman A, Punwani S, Emberton M, Ahmed HU. Visually directed vs. software-based targeted biopsy compared to transperineal template mapping biopsy in the detection of clinically significant prostate cancer. Urol Oncol. Oct 2015;33(10):424 e9-16. doi:10. 1016/j.urolonc.2015.06.012

37. Watts KL, Frechette L, Muller B, et al. Systematic review and meta-analysis comparing cognitive vs. image-guided fusion prostate biopsy for the detection of prostate cancer. Urol Oncol. Sep 2020;38(9):734 e19-734 e25. doi:10.1016/ j.urolonc.2020.03.020

38. Padhani AR, Barentsz J, Villeirs G, et al. PI-RADS Steering Committee: The PI-RADS Multiparametric MRI and MRI-directed Biopsy Pathway. Radiology. Aug 2019;292(2):464-474. doi:10.1148/radiol.2019182946

39. Drost FH, Osses DF, Nieboer D, et al. Prostate MRI, with or without MRI-targeted biopsy, and systematic biopsy for detecting prostate cancer. Cochrane Database Syst Rev. Apr 25 2019;4(4):CD 012663. doi:10.1002/14651858.CD012663.pub2

40. Tyson MD, Arora SS, Scarpato KR, Barocas D. Magnetic resonance-ultrasound fusion prostate biopsy in the diagnosis of prostate cancer. Urol Oncol. Jul 2016;34(7):326-32. doi:10.1016/j.urolo nc.2016.03.005

41. Mozer P, Roupret M, Le Cossec C, et al. First round of targeted biopsies using magnetic resonance imaging/ultrasonography fusion compared with conventional transrectal ultrasonography-guided biopsies for the diagnosis of localised prostate cancer. BJU Int. Jan 2015;115(1):50-7. doi:10.1111/bju.12690

42. Meng X, Rosenkrantz AB, Mendhiratta N, et al. Relationship Between Prebiopsy Multiparametric Magnetic Resonance Imaging (MRI), Biopsy Indication, and MRI-ultrasound Fusion-targeted Prostate Biopsy Outcomes. Eur Urol. Mar 2016;69( 3):512-7. doi:10.1016/j.eururo.2015.06.005

43. Sonn GA, Chang E, Natarajan S, et al. Value of targeted prostate biopsy using magnetic resonance-ultrasound fusion in men with prior negative biopsy and elevated prostate-specific antigen. Eur Urol. Apr 2014;65(4):809-15. doi:10.1 016/j.eururo.2013.03.025

44. Hoeks CM, Schouten MG, Bomers JG, et al. Three-Tesla magnetic resonance-guided prostate biopsy in men with increased prostate-specific antigen and repeated, negative, random, systematic, transrectal ultrasound biopsies: detection of clinically significant prostate cancers. Eur Urol. Nov 2012;62(5):902-9. doi:10.1016/j.euru ro.2012.01.047

45. Delongchamps NB, Lefevre A, Bouazza N, Beuvon F, Legman P, Cornud F. Detection of significant prostate cancer with magnetic resonance targeted biopsies--should transrectal ultrasound-magnetic resonance imaging fusion guided biopsies alone be a standard of care? J Urol. Apr 2015;193(4):1198-204. doi:10.1016/j.juro .2014.11.002

46. Filson CP, Natarajan S, Margolis DJ, et al. Prostate cancer detection with magnetic resonance-ultrasound fusion biopsy: The role of systematic and targeted biopsies. Cancer. Mar 15 2016;122(6):884-92. doi:10.1002/cncr.29874

47. Ploussard G, Borgmann H, Briganti A, et al. Positive pre-biopsy MRI: are systematic biopsies still useful in addition to targeted biopsies? World J Urol. Feb 2019;37(2):243-251. doi:10.1007/s0034 5-018-2399-z

48. Borofsky S, George AK, Gaur S, et al. What Are We Missing? False-Negative Cancers at Multiparametric MR Imaging of the Prostate. Radiology. Jan 2018;286(1):186-195. doi:10.1148/r adiol.2017152877

49. Richenberg J, Logager V, Panebianco V, Rouviere O, Villeirs G, Schoots IG. The primacy of multiparametric MRI in men with suspected prostate cancer. Eur Radiol. Dec 2019;29(12):6940-6952. doi:10.1007/s00330-019-06166-z

50. Penzkofer T, Tuncali K, Fedorov A, et al. Transperineal in-bore 3-T MR imaging-guided prostate biopsy: a prospective clinical observational study. Radiology. Jan 2015;274(1):170-80. doi:10.1 148/radiol.14140221

51. Elhawary H, Zivanovic A, Rea M, et al. The feasibility of MR-image guided prostate biopsy using piezoceramic motors inside or near to the magnet isocentre. Med Image Comput Comput Assist Interv. 2006;9(Pt 1):519-26. doi:10.1007/ 11866565_64

52. Lagerburg V, Moerland MA, van Vulpen M, Lagendijk JJ. A new robotic needle insertion method to minimise attendant prostate motion. Radiother Oncol. Jul 2006;80(1):73-7. doi:10.1016/ j.radonc.2006.06.013

53. Del Monte M, Cipollari S, Del Giudice F, et al. MRI-directed biopsy for primary detection of prostate cancer in a population of 223 men: MRI In-Bore vs MRI-transrectal ultrasound fusion-targeted techniques. Br J Radiol. Mar 1 2022;95(1131) :20210528. doi:10.1259/bjr.20210528

54. Ramos F, Korets R, Fleishman A, et al. Comparative Effectiveness of Magnetic Resonance Imaging-Ultrasound Fusion Versus In-bore Magnetic Resonance Imaging-targeted Prostate Biopsy. Urology. Jan 2023;171:164-171. doi:10.10 16/j.urology.2022.09.016

55. Prince M, Foster BR, Kaempf A, et al. In-Bore Versus Fusion MRI-Targeted Biopsy of PI-RADS Category 4 and 5 Lesions: A Retrospective Comparative Analysis Using Propensity Score Weighting. AJR Am J Roentgenol. Nov 2021;217 (5):1123-1130. doi:10.2214/AJR.20.25207

56. Heidenreich A, Bastian PJ, Bellmunt J, et al. EAU guidelines on prostate cancer. part 1: screening, diagnosis, and local treatment with curative intent-update 2013. Eur Urol. Jan 2014; 65(1):124-37. doi:10.1016/j.eururo.2013.09.046

57. Wallis CJD, Saskin R, Choo R, et al. Surgery Versus Radiotherapy for Clinically-localized Prostate Cancer: A Systematic Review and Meta-analysis. Eur Urol. Jul 2016;70(1):21-30. doi:10.1016/j.euru ro.2015.11.010

58. Hamdy FC, Donovan JL, Lane JA, et al. Fifteen-Year Outcomes after Monitoring, Surgery, or Radiotherapy for Prostate Cancer. N Engl J Med. Apr 27 2023;388(17):1547-1558. doi:10.1056/NE JMoa2214122

59. Lei JH, Liu LR, Wei Q, et al. Systematic review and meta-analysis of the survival outcomes of first-line treatment options in high-risk prostate cancer. Sci Rep. Jan 12 2015;5:7713. doi:10.1038/srep07713

60. Petrelli F, Vavassori I, Coinu A, Borgonovo K, Sarti E, Barni S. Radical prostatectomy or radiotherapy in high-risk prostate cancer: a systematic review and metaanalysis. Clin Genitourin Cancer. Aug 2014;12(4):215-24. doi:10. 1016/j.clgc.2014.01.010

61. Cooperberg MR, Broering JM, Carroll PR. Time trends and local variation in primary treatment of localized prostate cancer. J Clin Oncol. Mar 1 2010;28(7):1117-23. doi:10.1200/JC O.2009.26.0133

62. Potosky AL, Davis WW, Hoffman RM, et al. Five-year outcomes after prostatectomy or radiotherapy for prostate cancer: the prostate cancer outcomes study. J Natl Cancer Inst. Sep 15 2004;96(18):1358-67. doi:10.1093/jnci/djh259

63. Chen C, Chen Z, Wang K, Hu L, Xu R, He X. Comparisons of health-related quality of life among surgery and radiotherapy for localized prostate cancer: a systematic review and meta-analysis. Oncotarget. Nov 17 2017;8(58):99057-99065. doi:10.18632/oncotarget.21519

64. Sanda MG, Cadeddu JA, Kirkby E, et al. Clinically Localized Prostate Cancer: AUA/ ASTRO/SUO Guideline. Part II: Recommended Approaches and Details of Specific Care Options. J Urol. Apr 2018;199(4):990-997. doi:10.1016/j.juro .2018.01.002

65. Hakimi AA, Feder M, Ghavamian R. Minimally invasive approaches to prostate cancer: a review of the current literature. Urol J. Summer 2007;4(3):130-7.

66. Menon M, Tewari A, Peabody JO, et al. Vattikuti Institute prostatectomy, a technique of robotic radical prostatectomy for management of localized carcinoma of the prostate: experience of over 1100 cases. Urol Clin North Am. Nov 2004;31(4):701-17. doi:10.1016/j.ucl.2004.06.011

67. Passoni NM, Polascik TJ. How to select the right patients for focal therapy of prostate cancer? Curr Opin Urol. May 2014;24(3):203-8. doi:10.10 97/MOU.0000000000000045

68. Blana A, Rogenhofer S, Ganzer R, et al. Eight years' experience with high-intensity focused ultrasonography for treatment of localized prostate cancer. Urology. Dec 2008;72(6):1329-33; discussion 1333-4. doi:10.1016/j.urology.2008.06.062

69. Lee T, Mendhiratta N, Sperling D, Lepor H. Focal laser ablation for localized prostate cancer: principles, clinical trials, and our initial experience. Rev Urol. 2014;16(2):55-66.

70. Ritch CR, Katz AE. Prostate cryotherapy: current status. Curr Opin Urol. Mar 2009;19(2):177-81. doi:10.1097/mou.0b013e32831e16ce

71. Punnen S, Cooperberg MR, D'Amico AV, et al. Management of biochemical recurrence after primary treatment of prostate cancer: a systematic review of the literature. Eur Urol. Dec 2013;64 (6):905-15. doi:10.1016/j.eururo.2013.05.025

72. Fainberg JS, Al Hussein Al Awamlh B, DeRosa AP, et al. A systematic review of outcomes after thermal and nonthermal partial prostate ablation. Prostate Int. Dec 2021;9(4):169-175. doi:10.1016/j. prnil.2021.04.001

73. Budaus L, Spethmann J, Isbarn H, et al. Inverse stage migration in patients undergoing radical prostatectomy: results of 8916 European patients treated within the last decade. BJU Int. Oct 2011;1 08(8):1256-61. doi:10.1111/j.1464-410X.2010.09982.x

74. Muller BG, van den Bos W, Pinto PA, de la Rosette JJ. Imaging modalities in focal therapy: patient selection, treatment guidance, and follow-up. Curr Opin Urol. May 2014;24(3):218-24. doi:10.1097/MOU.0000000000000041

75. Stephenson AJ, Scardino PT, Bianco FJ, Jr., Eastham JA. Salvage therapy for locally recurrent prostate cancer after external beam radiotherapy. Curr Treat Options Oncol. Oct 2004;5(5):357-65. doi:10.1007/s11864-004-0026-2

76. Tacke J, Adam G, Haage P, Sellhaus B, Grosskortenhaus S, Gunther RW. MR-guided percutaneous cryotherapy of the liver: in vivo evaluation with histologic correlation in an animal model. J Magn Reson Imaging. Jan 2001;13(1):50-6. doi:10.1002/1522-2586(200101)13:1<50::aid-jmri1008>3.0.co;2-a

77. Tuncali K, Morrison PR, Tatli S, Silverman SG. MRI-guided percutaneous cryoablation of renal tumors: use of external manual displacement of adjacent bowel loops. Eur J Radiol. Aug 2006;59 (2):198-202. doi:10.1016/j.ejrad.2006.04.013

78. Josan S, Bouley DM, van den Bosch M, Daniel BL, Butts Pauly K. MRI-guided cryoablation: In vivo assessment of focal canine prostate cryolesions. J Magn Reson Imaging. Jul 2009;30(1):169-76. doi:1 0.1002/jmri.21827

79. van den Bosch MA, Josan S, Bouley DM, et al. MR imaging-guided percutaneous cryoablation of the prostate in an animal model: in vivo imaging of cryoablation-induced tissue necrosis with immediate histopathologic correlation. J Vasc Interv Radiol. Feb 2009;20(2):252-8. doi:10.1016 /j.jvir.2008.10.030

80. Gangi A, Tsoumakidou G, Abdelli O, et al. Percutaneous MR-guided cryoablation of prostate cancer: initial experience. Eur Radiol. Aug 2012; 22(8):1829-35. doi:10.1007/s00330-012-2411-8

81. Woodrum DA, Kawashima A, Karnes RJ, et al. Magnetic resonance imaging-guided cryoablation of recurrent prostate cancer after radical prostatectomy: initial single institution experience. Urology. Oct 2013;82(4):870-5. doi:10.1016/j.urol ogy.2013.06.011

82. de Marini P, Cazzato RL, Garnon J, et al. Percutaneous MR-guided prostate cancer cryoablation technical updates and literature review. BJR Open. 2019;1(1):20180043. doi:10.12 59/bjro.20180043

83. McNichols RJ, Gowda A, Kangasniemi M, Bankson JA, Price RE, Hazle JD. MR thermometry-based feedback control of laser interstitial thermal therapy at 980 nm. Lasers Surg Med. 2004;34 (1):48-55. doi:10.1002/lsm.10243

84. Hynynen K, Freund WR, Cline HE, et al. A clinical, noninvasive, MR imaging-monitored ultrasound surgery method. Radiographics. Jan 1996;16(1) :185-95. doi:10.1148/radiographics.16.1.185

85. Ishihara Y, Calderon A, Watanabe H, et al. A precise and fast temperature mapping using water proton chemical shift. Magn Reson Med. Dec 1995;34(6):814-23. doi:10.1002/mrm.1910340606

86. Vitkin IA, Moriarty JA, Peters RD, et al. Magnetic resonance imaging of temperature changes during interstitial microwave heating: a phantom study. Med Phys. Feb 1997;24(2):269-77. doi:10.1118/1.598096

87. Sapareto SA, Dewey WC. Thermal dose determination in cancer therapy. Int J Radiat Oncol Biol Phys. Jun 1984;10(6):787-800. doi:10.1016/ 0360-3016(84)90379-1

88. Zhu M, Sun Z, Ng CK. Image-guided thermal ablation with MR-based thermometry. Quant Imaging Med Surg. Jun 2017;7(3):356-368. doi:10. 21037/qims.2017.06.06

89. McNichols RJ, Gowda, A., Gelnett, M. D., Stafford, R. J. Percutaneous MRI-guided laser thermal therapy in canine prostate. Progress in Biomedical Optics and Imaging - Proceedings of SPIE. 2005;5686:214-225. doi:10.1117/12.587747

90. Stafford RJ, Shetty A, Elliott AM, et al. Magnetic resonance guided, focal laser induced interstitial thermal therapy in a canine prostate model. J Urol. Oct 2010;184(4):1514-20. doi:10.10 16/j.juro.2010.05.091

91. Woodrum DA, Gorny KR, Mynderse LA, et al. Feasibility of 3.0T magnetic resonance imaging-guided laser ablation of a cadaveric prostate. Urology. Jun 2010;75(6):1514 e1-6. doi:10.1016/ j.urology.2010.01.059

92. Raz O, Haider MA, Davidson SR, et al. Real-time magnetic resonance imaging-guided focal laser therapy in patients with low-risk prostate cancer. Eur Urol. Jul 2010;58(1):173-7. doi:10.1016 /j.eururo.2010.03.006

93. Natarajan S, Raman S, Priester AM, et al. Focal Laser Ablation of Prostate Cancer: Phase I Clinical Trial. J Urol. Jul 2016;196(1):68-75. doi:10.1016 /j.juro.2015.12.083

94. Thuroff S, Chaussy C, Vallancien G, et al. High-intensity focused ultrasound and localized prostate cancer: efficacy results from the European multicentric study. J Endourol. Oct 2003;17(8):673-7. doi:10.1089/089277903322518699

95. Gelet A, Chapelon JY, Bouvier R, et al. Transrectal high-intensity focused ultrasound: minimally invasive therapy of localized prostate cancer. J Endourol. Aug 2000;14(6):519-28. doi:10 .1089/end.2000.14.519

96. Gelet A, Chapelon JY, Bouvier R, Rouviere O, Lyonnet D, Dubernard JM. Transrectal high intensity focused ultrasound for the treatment of localized prostate cancer: factors influencing the outcome. Eur Urol. Aug 2001;40(2):124-9. doi:10. 1159/000049761

97. Uchida T, Tomonaga T, Kim H, et al. Improved outcomes with advancements in high intensity focused ultrasound devices for the treatment of localized prostate cancer. J Urol. Jan 2015;193 (1):103-10. doi:10.1016/j.juro.2014.07.096

98. Crouzet S, Chapelon JY, Rouviere O, et al. Whole-gland ablation of localized prostate cancer with high-intensity focused ultrasound: oncologic outcomes and morbidity in 1002 patients. Eur Urol. May 2014;65(5):907-14. doi:10.1016/j.eururo.2013.04.039

99. van Velthoven R, Aoun F, Marcelis Q, et al. A prospective clinical trial of HIFU hemiablation for clinically localized prostate cancer. Prostate Cancer Prostatic Dis. Mar 2016;19(1):79-83. doi:10.1038 /pcan.2015.55

100. Profound Medical Receives U.S. FDA 510(k) Clearance for TULSA-PRO®. Global News Wire. https://www.globenewswire.com/news-release/2019/08/16/1903004/0/en/Profound-Medical-Receives-U-S-FDA-510-k-Clearance-for-TULSA-PRO.html

101. Klotz L PD, Chin J, Pavlovich C, Relle J, Koch M, et al. LBA20 MRI-GUIDED TRANSURETHRAL ULTRASOUND ABLATION (TULSA) IN PATIENTS WITH LOCALIZED PROSTATE CANCER: PRELIMINARY RESULTS OF TACT PIVOTAL STUDY. Journal of Urology 2018;199(4S):e1077–8. doi: https://doi.org/10.1016/j.juro.2018.03.091

102. Ehdaie B, Tempany CM, Holland F, et al. MRI-guided focused ultrasound focal therapy for patients with intermediate-risk prostate cancer: a phase 2b, multicentre study. Lancet Oncol. Jul 2022;23(7):910-918. doi:10.1016/S1470-2045(22)0 0251-0

103. INSIGHTEC ANNOUNCES FDA CLEARANCE FOR EXABLATE PROSTATE TO TREAT PROSTATE TISSUE. Insightec. https://insightec.com/news/insightec-announces-fda-clearance-for-exablate-prostate/

104. Shore ND, Moul JW, Pienta KJ, Czernin J, King MT, Freedland SJ. Biochemical recurrence in patients with prostate cancer after primary definitive therapy: treatment based on risk stratification. Prostate Cancer Prostatic Dis. Jun 2024;27(2):192-201. doi:10.1038/s41391-023-00712-z

105. Stephenson AJ, Slawin KM. The value of radiotherapy in treating recurrent prostate cancer after radical prostatectomy. Nat Clin Pract Urol. Dec 2004;1(2):90-6. doi:10.1038/ncpuro0056

106. Brandeis J, Pashos CL, Henning JM, Litwin MS. A nationwide charge comparison of the principal treatments for early stage prostate carcinoma. Cancer. Oct 15 2000;89(8):1792-9.

107. Sella T, Schwartz LH, Swindle PW, et al. Suspected local recurrence after radical prostatectomy: endorectal coil MR imaging. Radiology. May 2004;231(2):379-85. doi:10.1148/ radiol.2312030011

108. Agarwal PK, Sadetsky N, Konety BR, Resnick MI, Carroll PR, Cancer of the Prostate Strategic Urological Research E. Treatment failure after primary and salvage therapy for prostate cancer: likelihood, patterns of care, and outcomes. Cancer. Jan 15 2008;112(2):307-14. doi:10.1002/cncr.23161

109. Kuban DA, Thames HD, Levy LB, et al. Long-term multi-institutional analysis of stage T1-T2 prostate cancer treated with radiotherapy in the PSA era. Int J Radiat Oncol Biol Phys. Nov 15 2003;57(4):915-28. doi:10.1016/s0360-3016(03)00632-1

110. Kramer S, Gorich J, Gottfried HW, et al. Sensitivity of computed tomography in detecting local recurrence of prostatic carcinoma following radical prostatectomy. Br J Radiol. Oct 1997;70(83 8):995-9. doi:10.1259/bjr.70.838.9404201

111. Connolly JA, Shinohara K, Presti JC, Jr., Carroll PR. Local recurrence after radical prostatectomy: characteristics in size, location, and relationship to prostate-specific antigen and surgical margins. Urology. Feb 1996;47(2):225-31. doi:10.1016/S009 0-4295(99)80421-X

112. Leventis AK, Shariat SF, Slawin KM. Local recurrence after radical prostatectomy: correlation of US features with prostatic fossa biopsy findings. Radiology. May 2001;219(2):432-9. doi:10.1148/ radiology.219.2.r01ma20432

113. Linder BJ, Kawashima A, Woodrum DA, et al. Early localization of recurrent prostate cancer after prostatectomy by endorectal coil magnetic resonance imaging. Can J Urol. Jun 2014;21 (3):7283-9.

114. Roy C, Foudi F, Charton J, et al. Comparative sensitivities of functional MRI sequences in detection of local recurrence of prostate carcinoma after radical prostatectomy or external-beam radiotherapy. AJR Am J Roentgenol. Apr 2013; 200(4):W361-8. doi:10.2214/AJR.12.9106

115. May EJ, Viers LD, Viers BR, et al. Prostate cancer post-treatment follow-up and recurrence evaluation. Abdom Radiol (NY). May 2016;41(5): 862-76. doi:10.1007/s00261-015-0562-1

116. Kitajima K, Hartman RP, Froemming AT, Hagen CE, Takahashi N, Kawashima A. Detection of Local Recurrence of Prostate Cancer After Radical Prostatectomy Using Endorectal Coil MRI at 3 T: Addition of DWI and Dynamic Contrast Enhancement to T2-Weighted MRI. AJR Am J Roentgenol. Oct 2015;205(4):807-16. doi:10.2214/ AJR.14.14275

117. Amling CL, Blute ML, Bergstralh EJ, Seay TM, Slezak J, Zincke H. Long-term hazard of progression after radical prostatectomy for clinically localized prostate cancer: continued risk of biochemical failure after 5 years. J Urol. Jul 2000;164(1):101-5.

118. Bianco FJ, Jr., Scardino PT, Stephenson AJ, Diblasio CJ, Fearn PA, Eastham JA. Long-term oncologic results of salvage radical prostatectomy for locally recurrent prostate cancer after radiotherapy. Int J Radiat Oncol Biol Phys. Jun 1 2005;62(2):448-53. doi:10.1016/j.ijrobp.2004.09.049

119. Boris RS, Bhandari A, Krane LS, Eun D, Kaul S, Peabody JO. Salvage robotic-assisted radical prostatectomy: initial results and early report of outcomes. BJU Int. Apr 2009;103(7):952-6. doi:10.1111/j.1464-410X.2008.08245.x

120. Kimura M, Mouraviev V, Tsivian M, Mayes JM, Satoh T, Polascik TJ. Current salvage methods for recurrent prostate cancer after failure of primary radiotherapy. BJU Int. Jan 2010;105(2):191-201. doi:10.1111/j.1464-410X.2009.08715.x

121. Chade DC, Shariat SF, Cronin AM, et al. Salvage radical prostatectomy for radiation-recurrent prostate cancer: a multi-institutional collaboration. Eur Urol. Aug 2011;60(2):205-10. doi:10.1016/j.eururo.2011.03.011

122. De Groote R, Nathan A, De Bleser E, et al. Techniques and Outcomes of Salvage Robot-Assisted Radical Prostatectomy (sRARP). Eur Urol. Dec 2020;78(6):885-892. doi:10.1016/j.eururo.2020.05.003

123. Grado GL, Collins JM, Kriegshauser JS, et al. Salvage brachytherapy for localized prostate cancer after radiotherapy failure. Urology. Jan 1999;53(1):2-10. doi:Doi 10.1016/S0090-4295(98)0 0492-0

124. Koutrouvelis P, Hendricks F, Lailas N, et al. Salvage reimplantation in patient with local recurrent prostate carcinoma after brachytherapy with three dimensional computed tomography-guided permanent pararectal implant. Technol Cancer Res Treat. Aug 2003;2(4):339-44. doi:10.11 77/153303460300200409

125. Kollmeier MA, McBride S, Taggar A, et al. Salvage brachytherapy for recurrent prostate cancer after definitive radiation therapy: A comparison of low-dose-rate and high-dose-rate brachytherapy and the importance of prostate-specific antigen doubling time. Brachytherapy. Nov-Dec 2017;16(6):1091-1098. doi:10.1016/j.bra chy.2017.07.013

126. Zaine H, Vandendorpe B, Bataille B, et al. Salvage Radiotherapy for Macroscopic Local Recurrence Following Radical Prostatectomy. Front Oncol. 2021;11:669261. doi:10.3389/fonc.2021.669261

127. Murat FJ, Poissonnier L, Rabilloud M, et al. Mid-term results demonstrate salvage high-intensity focused ultrasound (HIFU) as an effective and acceptably morbid salvage treatment option for locally radiorecurrent prostate cancer. Eur Urol. Mar 2009;55(3):640-7. doi:10.1016/j.eururo.2008.04.091

128. Zacharakis E, Ahmed HU, Ishaq A, et al. The feasibility and safety of high-intensity focused ultrasound as salvage therapy for recurrent prostate cancer following external beam radiotherapy. BJU Int. Sep 2008;102(7):786-92. doi:10.1111/j.1464-410X.2008.07775.x

129. Gelet A, Chapelon JY, Poissonnier L, et al. Local recurrence of prostate cancer after external beam radiotherapy: early experience of salvage therapy using high-intensity focused ultrasonography. Urology. Apr 2004;63(4):625-9. doi:10.1016/j.urolo gy.2004.01.002

130. Crouzet S, Blana A, Murat FJ, et al. Salvage high-intensity focused ultrasound (HIFU) for locally recurrent prostate cancer after failed radiation therapy: Multi-institutional analysis of 418 patients. BJU Int. Jun 2017;119(6):896-904. doi:10.1111/bju .13766

131. Maestroni U, Tafuri A, Dinale F, Campobasso D, Antonelli A, Ziglioli F. Oncologic outcome of salvage high-intensity focused ultrasound (HIFU) in radiorecurrent prostate cancer. A systematic review. Acta Biomed. Sep 2 2021;92(4):e2021191. doi:10.23750/abm.v92i3.11475

132. Chin JL, Pautler SE, Mouraviev V, Touma N, Moore K, Downey DB. Results of salvage cryoablation of the prostate after radiation: identifying predictors of treatment failure and complications. J Urol. Jun 2001;165(6 Pt 1):1937-41; discussion 1941-2. doi:10.1097/00005392-200 106000-00022

133. Siddiqui SA ML, Zincke H, Hoffmann NE, Lobo JR, Wilson TM. Treatment of prostate cancer local recurrence after radical retropubic prostatectomy with 17-guage interstitial transperineal cryoablation: initial experience. Urology. 2007;70(117)

134. Pisters LL, Rewcastle JC, Donnelly BJ, Lugnani FM, Katz AE, Jones JS. Salvage prostate cryoablation: initial results from the cryo on-line data registry. J Urol. Aug 2008;180(2):559-63; discussion 563-4. doi:10.1016/j.juro.2008.04.005

135. Wenske S, Quarrier S, Katz AE. Salvage cryosurgery of the prostate for failure after primary radiotherapy or cryosurgery: long-term clinical, functional, and oncologic outcomes in a large cohort at a tertiary referral centre. Eur Urol. Jul 2013;64(1):1-7. doi:10.1016/j.eururo.2012.07.008

136. Chin YF, Lynn N. Systematic Review of Focal and Salvage Cryotherapy for Prostate Cancer. Cureus. Jun 2022;14(6):e26400. doi:10.7759/cureus.26400

137. Uchida T, Shoji S, Nakano M, et al. High-intensity focused ultrasound as salvage therapy for patients with recurrent prostate cancer after external beam radiation, brachytherapy or proton therapy. BJU Int. Feb 2011;107(3):378-82. doi:10.1 111/j.1464-410X.2010.09518.x

138. Bomers JG, Yakar D, Overduin CG, et al. MR imaging-guided focal cryoablation in patients with recurrent prostate cancer. Radiology. Aug 2013;268(2):451-60. doi:10.1148/radiol.13121291

139. Overduin CG, Jenniskens SFM, Sedelaar JPM, Bomers JGR, Futterer JJ. Percutaneous MR-guided focal cryoablation for recurrent prostate cancer following radiation therapy: retrospective analysis of iceball margins and outcomes. Eur Radiol. Nov 2017;27(11):4828-4836. doi:10.1007/s00330-017-4833-9

140. Porter CAt, Woodrum DA, Callstrom MR, et al. MRI after technically successful renal cryoablation: early contrast enhancement as a common finding. AJR Am J Roentgenol. Mar 2010;194(3):790-3. doi:10.2214/AJR.09.2518

141. Gage AA, Baust J. Mechanisms of tissue injury in cryosurgery. Cryobiology. Nov 1998;37(3):171-86. doi:10.1006/cryo.1998.2115

142. Favazza CP, Gorny KR, King DM, et al. An investigation of the effects from a urethral warming system on temperature distributions during cryoablation treatment of the prostate: a phantom study. Cryobiology. Aug 2014;69(1):128-33. doi:10 .1016/j.cryobiol.2014.06.004

143. Butts K, Sinclair J, Daniel BL, Wansapura J, Pauly JM. Temperature quantitation and mapping of frozen tissue. J Magn Reson Imaging. Jan 2001;13(1):99-104. doi:10.1002/1522-2586(20010 1)13:1<99::aid-jmri1015>3.0.co;2-o

144. Wansapura JP, Daniel BL, Vigen KK, Butts K. In vivo MR thermometry of frozen tissue using R2* and signal intensity. Acad Radiol. Sep 2005; 12(9):1080-4. doi:10.1016/j.acra.2005.06.006

145. Lu A, Daniel BL, Pauly JM, Pauly KB. Improved slice selection for R2* mapping during cryoablation with eddy current compensation. J Magn Reson Imaging. Jul 2008;28(1):190-8. doi:10.1002/jmri.21396

146. Soher BJ, Wyatt C, Reeder SB, MacFall JR. Noninvasive temperature mapping with MRI using chemical shift water-fat separation. Magn Reson Med. May 2010;63(5):1238-46. doi:10.1002/mrm.22310

147. Alabousi M, Ghai S, Haider MA. MRI-guided Minimally Invasive Focal Therapies for Prostate Cancer. Radiology. Dec 2023;309(3):e230431. doi: 10.1148/radiol.230431