Abstract
Purpose
Focal therapy (FT) is gaining increasing acceptance in the management of localized prostate cancer particularly due to its favorable safety. Preliminary evidence suggests advantageous utilization of local treatment in the field of oligometastatic prostate cancer (OMPC). Since data on the utilization of FT in OMPC are scarce, we sought to summarize available evidence.
Methods
For this narrative comprehensive review, we employed PubMed®, Web of Science™, Embase®, Scopus®, and clinicaltrial.gov databases and Google web search engine to seek peer-reviewed articles, published abstracts from international congresses, and ongoing trials in the English language using the terms “prostate cancer”, “oligometastatic”, “hormone-sensitive”, “focal therapy”, “focal treatment”, “cryotherapy”, “ablation”, “cancer” as well as “metastasis-directed therapy. We focused on relevant publications on FT utilized in OMPC targeting the primary or metastatic sites as well as completed and ongoing clinical trials.
Results
Growing evidence points to distinct differences in the biologic behavior and molecular signaling processes of OMPC as compared to polymetastatic disease (PMPC). No established biomarkers are available to accurately identify OMPC yet, while several candidates are currently under investigation. The evolution of molecular imaging is set to aid in selecting patients benefitting most from local management. Differences between OMPC and PMPC should be considered when designing the optimal therapeutic strategy. While efficacy data for FT in comparison to standard care in OMPC are scarce, longer progression-free survival and time to castration resistance have been demonstrated for bone metastatic prostate cancer with the primary tumor treated by cryosurgery followed by androgen deprivation therapy (ADT) compared to ADT alone.
Conclusion
Ongoing research efforts are eagerly awaited to better characterize OMPC and establish customized strategies for patients with this condition.
Similar content being viewed by others
References
Ong S, O’Brien J, Medhurst E, Lawrentschuk N, Murphy D, Azad A (2021) Current treatment options for newly diagnosed metastatic hormone-sensitive prostate cancer-a narrative review. Transl Androl Urol. 10(10):3918–3930. https://doi.org/10.21037/tau-20-1118
Teo MY, Rathkopf DE, Kantoff P (2019) Treatment of advanced prostate cancer. Annu Rev Med 70:479–499. https://doi.org/10.1146/annurev-med-051517-011947
Smith MR, Hussain M, Saad F, Fizazi K, Sternberg CN, Crawford ED et al (2022) Darolutamide and survival in metastatic, hormone-sensitive prostate cancer. N Engl J Med. https://doi.org/10.1056/NEJMoa2119115
Boeve LMS, Hulshof M, Vis AN, Zwinderman AH, Twisk JWR, Witjes WPJ et al (2019) Effect on survival of androgen deprivation therapy alone compared to androgen deprivation therapy combined with concurrent radiation therapy to the prostate in patients with primary bone metastatic prostate cancer in a prospective randomised clinical trial: data from the HORRAD trial. Eur Urol 75(3):410–418. https://doi.org/10.1016/j.eururo.2018.09.008
Parker CC, James ND, Brawley CD, Clarke NW, Hoyle AP, Ali A et al (2018) Radiotherapy to the primary tumour for newly diagnosed, metastatic prostate cancer (STAMPEDE): a randomised controlled phase 3 trial. Lancet 392(10162):2353–2366. https://doi.org/10.1016/S0140-6736(18)32486-3
Ali A, Hoyle A, Haran AM, Brawley CD, Cook A, Amos C et al (2021) Association of bone metastatic burden with survival benefit from prostate radiotherapy in patients with newly diagnosed metastatic prostate cancer: a secondary analysis of a randomized clinical trial. JAMA Oncol 7(4):555–563. https://doi.org/10.1001/jamaoncol.2020.7857
Knipper S, Beyer B, Mandel P, Tennstedt P, Tilki D, Steuber T et al (2020) Outcome of patients with newly diagnosed prostate cancer with low metastatic burden treated with radical prostatectomy: a comparison to STAMPEDE arm H. World J Urol 38(6):1459–1464. https://doi.org/10.1007/s00345-019-02950-0
Phillips R, Shi WY, Deek M, Radwan N, Lim SJ, Antonarakis ES et al (2020) Outcomes of observation vs stereotactic ablative radiation for oligometastatic prostate cancer: the ORIOLE phase 2 randomized clinical trial. JAMA Oncol 6(5):650–659. https://doi.org/10.1001/jamaoncol.2020.0147
Ost P, Reynders D, Decaestecker K, Fonteyne V, Lumen N, Bruycker AD et al (2020) Surveillance or metastasis-directed therapy for oligometastatic prostate cancer recurrence (STOMP): five-year results of a randomized phase II trial. J Clin Oncol 38(6_suppl):10. https://doi.org/10.1200/JCO.2020.38.6_suppl.1.0
van der Poel HG, van den Bergh RCN, Briers E, Cornford P, Govorov A, Henry AM et al (2018) Focal therapy in primary localised prostate cancer: the European association of urology position in 2018. Eur Urol 74(1):84–91. https://doi.org/10.1016/j.eururo.2018.01.001
Hellman S, Weichselbaum RR (1995) Oligometastases. J Clin Oncol 13(1):8–10. https://doi.org/10.1200/JCO.1995.13.1.8
Weichselbaum RR, Hellman S (2011) Oligometastases revisited. Nat Rev Clin Oncol 8(6):378–382. https://doi.org/10.1038/nrclinonc.2011.44
Gundem G, Van Loo P, Kremeyer B, Alexandrov LB, Tubio JMC, Papaemmanuil E et al (2015) The evolutionary history of lethal metastatic prostate cancer. Nature 520(7547):353–357. https://doi.org/10.1038/nature14347
Meagher MF, Mir MC, Autorino R, Minervini A, Kriegmair M, Maurer T et al (2022) Impact of metastasectomy on cancer specific and overall survival in metastatic renal cell carcinoma: analysis of the REMARCC registry. Clin Genitourin Cancer. https://doi.org/10.1016/j.clgc.2022.03.013
Antonelli A, Cozzoli A, Simeone C, Zani D, Zanotelli T, Portesi E et al (2006) Surgical treatment of adrenal metastasis from renal cell carcinoma: a single-centre experience of 45 patients. BJU Int 97(3):505–508. https://doi.org/10.1111/j.1464-410X.2006.05934.x
Raoux L, Maulat C, Mokrane FZ, Fares N, Suc B, Muscari F (2020) Impact of the strategy for curative treatment of synchronous colorectal cancer liver metastases. J Visc Surg 157(4):289–299. https://doi.org/10.1016/j.jviscsurg.2019.10.007
Pawlik TM, Scoggins CR, Zorzi D, Abdalla EK, Andres A, Eng C et al (2005) Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases. Ann Surg 241(5):715–722. https://doi.org/10.1097/01.sla.0000160703.75808.7d (discussion 22–4)
Debbi K, Loganadane G, To NH, Kinj R, Husain ZA, Chapet S et al (2022) Curative intent Stereotactic Ablative Radiation Therapy (SABR) for treatment of lung oligometastases from head and neck squamous cell carcinoma (HNSCC): a multi-institutional retrospective study. Br J Radiol. https://doi.org/10.1259/bjr.20210033
Lemoine P, Bruand M, Kammerer E, Bogart E, Comte P, Royer P et al (2021) Stereotactic body radiation therapy for oligometastatic breast cancer: a retrospective multicenter study. Front Oncol 11:736690. https://doi.org/10.3389/fonc.2021.736690
Surcel C, Kretschmer A, Mirvald C, Sinescu I, Heidegger I, Tsaur I (2022) Molecular mechanisms related with oligometastatic prostate cancer-is it just a matter of numbers? Cancers (Basel). https://doi.org/10.3390/cancers14030766
Ahmad AE, Leao R, Hamilton RJ (2017) Radical prostatectomy for patients with oligometastatic prostate cancer. Oncology (Williston Park) 31(11):794–802
Joice GA, Rowe SP, Pienta KJ, Gorin MA (2017) Oligometastatic prostate cancer: shaping the definition with molecular imaging and an improved understanding of tumor biology. Curr Opin Urol 27(6):533–541. https://doi.org/10.1097/MOU.0000000000000449
Muller PJ, Dietlein M, Kobe C, Heidenreich A, Drzezga A (2022) Oligometastatic disease in biochemical recurrence of prostate cancer: Prevalence on PSMA PET/CT and consecutive metastasis-directed therapy—experience at a tertiary referral center. Nuklearmedizin. https://doi.org/10.1055/a-1697-8111
Kucharczyk MJ, Gravis G, Niazi T (2019) The biology of oligometastatic prostate cancer: a different beast than polymetastatic prostate cancer. Eur Urol Focus 5(2):117–118. https://doi.org/10.1016/j.euf.2018.11.011
Buelens S, Poelaert F, Dhondt B, Fonteyne V, De Visschere P, Ost P et al (2018) Metastatic burden in newly diagnosed hormone-naive metastatic prostate cancer: comparing definitions of CHAARTED and LATITUDE trial. Urol Oncol 36(4):158 e13-158 e20. https://doi.org/10.1016/j.urolonc.2017.12.009
Gravis G, Boher JM, Chen YH, Liu G, Fizazi K, Carducci MA et al (2018) Burden of metastatic castrate naive prostate cancer patients, to identify men more likely to benefit from early docetaxel: further analyses of CHAARTED and GETUG-AFU15 studies. Eur Urol 73(6):847–855. https://doi.org/10.1016/j.eururo.2018.02.001
Formosa A, Markert EK, Lena AM, Italiano D, Finazzi-Agro E, Levine AJ et al (2014) MicroRNAs, miR-154, miR-299-5p, miR-376a, miR-376c, miR-377, miR-381, miR-487b, miR-485-3p, miR-495 and miR-654-3p, mapped to the 14q32.31 locus, regulate proliferation, apoptosis, migration and invasion in metastatic prostate cancer cells. Oncogene 33(44):5173–5182. https://doi.org/10.1038/onc.2013.451
Lussier YA, Xing HR, Salama JK, Khodarev NN, Huang Y, Zhang Q et al (2011) MicroRNA expression characterizes oligometastasis(es). PLoS ONE 6(12):e28650. https://doi.org/10.1371/journal.pone.0028650
Janiszewska M, Tabassum DP, Castano Z, Cristea S, Yamamoto KN, Kingston NL et al (2019) Subclonal cooperation drives metastasis by modulating local and systemic immune microenvironments. Nat Cell Biol 21(7):879–888. https://doi.org/10.1038/s41556-019-0346-x
Deek MP, Van der Eecken K, Phillips R, Parikh NR, Isaacsson Velho P, Lotan TL et al (2021) The mutational landscape of metastatic castration-sensitive prostate cancer: the spectrum theory revisited. Eur Urol 80(5):632–640. https://doi.org/10.1016/j.eururo.2020.12.040
Manini C, Gonzalez A, Buchser D, Garcia-Olaverri J, Urresola A, Ezquerro A et al (2020) Oligometastatic prostate adenocarcinoma. Clinical-pathologic study of a histologically under-recognized prostate cancer. J Pers Med. https://doi.org/10.3390/jpm10040265
Dhondt B, De Bleser E, Claeys T, Buelens S, Lumen N, Vandesompele J et al (2019) Discovery and validation of a serum microRNA signature to characterize oligo- and polymetastatic prostate cancer: not ready for prime time. World J Urol 37(12):2557–2564. https://doi.org/10.1007/s00345-018-2609-8
Nakamura M, Kageyama SI, Seki M, Suzuki A, Okumura M, Hojo H et al (2021) Liquid biopsy cell-free DNA biomarkers in patients with oligometastatic colorectal cancer treated by ablative radiotherapy. Anticancer Res 41(2):829–834. https://doi.org/10.21873/anticanres.14835
Mimoto R, Kobayashi T, Imawari Y, Kamio M, Kato K, Nogi H et al (2014) Clinical relevance and low tumor-initiating properties of oligometastatic breast cancer in pulmonary metastasectomy. Breast Cancer Res Treat 147(2):317–324. https://doi.org/10.1007/s10549-014-3111-7
Lin J, Chen Z, Li Z, Nong D, Li X, Huang G et al (2021) Screening of hub genes and evaluation of the growth regulatory role of CD44 in metastatic prostate cancer. Oncol Rep. https://doi.org/10.3892/or.2021.8147
Yamanaka M, Hayashi M, Yamada S, Sonohara F, Takami H, Inokawa Y et al (2021) A possible definition of oligometastasis in pancreatic cancer and associated survival outcomes. Anticancer Res 41(8):3933–3940. https://doi.org/10.21873/anticanres.15189
Zhao X, Zhang Y, Gao Z, Han Y (2022) Prognostic value of peripheral naive CD8(+) T cells in oligometastatic non-small-cell lung cancer. Future Oncol 18(1):55–65. https://doi.org/10.2217/fon-2021-0728
Evans JD, Morris LK, Zhang H, Cao S, Liu X, Mara KC et al (2019) Prospective immunophenotyping of CD8(+) T cells and associated clinical outcomes of patients with oligometastatic prostate cancer treated with metastasis-directed SBRT. Int J Radiat Oncol Biol Phys 103(1):229–240. https://doi.org/10.1016/j.ijrobp.2018.09.001
Guo Y, Arciero CA, Jiang R, Behera M, Peng L, Li X (2020) Different breast cancer subtypes show different metastatic patterns: a study from a large public database. Asian Pac J Cancer Prev 21(12):3587–3593. https://doi.org/10.31557/APJCP.2020.21.12.3587
Gomez V, Galazi M, Weitsman G, Monypenny J, Al-Salemee F, Barber PR et al (2022) HER2 mediates PSMA/mGluR1-driven resistance to the DS-7423 dual PI3K/mTOR inhibitor in PTEN wild-type prostate cancer models. Mol Cancer Ther. https://doi.org/10.1158/1535-7163.MCT-21-0320
Giraud N, Buy X, Vuong NS, Gaston R, Cazeau AL, Catena V et al (2021) Single-center experience of focal thermo-ablative therapy after pelvic radiotherapy for in-field prostate cancer oligo-recurrence. Front Oncol 11:709779. https://doi.org/10.3389/fonc.2021.709779
Abdo J, Cornell DL, Mittal SK, Agrawal DK (2018) Immunotherapy plus cryotherapy: potential augmented abscopal effect for advanced cancers. Front Oncol 8:85. https://doi.org/10.3389/fonc.2018.00085
Sheng MX, Wan LL, Liu CM, Liu CX, Chen SS (2017) Cytoreductive cryosurgery in patients with bone metastatic prostate cancer: a retrospective analysis. Kaohsiung J Med Sci 33(12):609–615. https://doi.org/10.1016/j.kjms.2017.07.002
Sheng M, Wan L, Liu C, Liu C (2018) Is cryosurgery a feasible local therapy for bone metastatic prostate cancer? Singapore Med J 59(11):584–589. https://doi.org/10.11622/smedj.2018119
Ross AE, Hurley PJ, Tran PT, Rowe SP, Benzon B, Neal TO et al (2020) A pilot trial of pembrolizumab plus prostatic cryotherapy for men with newly diagnosed oligometastatic hormone-sensitive prostate cancer. Prostate Cancer Prostatic Dis 23(1):184–193. https://doi.org/10.1038/s41391-019-0176-8
Valle LF, Lehrer EJ, Markovic D, Elashoff D, Levin-Epstein R, Karnes RJ et al (2021) A systematic review and meta-analysis of local salvage therapies after radiotherapy for prostate cancer (MASTER). Eur Urol 80(3):280–292. https://doi.org/10.1016/j.eururo.2020.11.010
Fredman E, Traughber B, Kharouta M, Podder T, Lo S, Ponsky L et al (2021) Focal prostate stereotactic body radiation therapy with correlative pathological and radiographic-based treatment planning. Front Oncol 11:744130. https://doi.org/10.3389/fonc.2021.744130
Tsoumakidou G, Mandralis K, Hocquelet A, Duran R, Denys A (2020) Salvage lymph-node percutaneous cryoablation: safety profile and oncologic outcomes. Cardiovasc Intervent Radiol 43(2):264–272. https://doi.org/10.1007/s00270-019-02341-3
Autrusseau PA, Cazzato RL, Koch G, Ramamurthy N, Auloge P, De Marini P et al (2021) Freezing nodal disease: local control following percutaneous image-guided cryoablation of locoregional and distant lymph node oligometastases: a 10-year, single-center experience. J Vasc Interv Radiol 32(10):1435–1444. https://doi.org/10.1016/j.jvir.2021.07.002
Cazzato RL, Garnon J, Ramamurthy N, Koch G, Tsoumakidou G, Caudrelier J et al (2016) Percutaneous image-guided cryoablation: current applications and results in the oncologic field. Med Oncol 33(12):140. https://doi.org/10.1007/s12032-016-0848-3
Cornelis FH, Durack JC, Morris MJ, Scher HI, Solomon SB (2017) Effective prostate-specific membrane antigen-based 18F-DCFPyL-guided cryoablation of a single positive site in a patient believed to be more metastatic on 11C-choline PET/CT. Clin Nucl Med 42(12):e516–e518. https://doi.org/10.1097/RLU.0000000000001846
Levy J, Hopkins T, Morris J, Tran ND, David E, Massari F et al (2020) Radiofrequency ablation for the palliative treatment of bone metastases: outcomes from the multicenter osteocool tumor ablation post-market study (OPuS One study) in 100 patients. J Vasc Interv Radiol 31(11):1745–1752. https://doi.org/10.1016/j.jvir.2020.07.014
Fares A, Shaaban MH, Reyad RM, Ragab AS, Sami MA (2018) Combined percutaneous radiofrequency ablation and cementoplasty for the treatment of extraspinal painful bone metastases: a prospective study. J Egypt Natl Canc Inst 30(3):117–122. https://doi.org/10.1016/j.jnci.2018.05.002
Mehta TI, Heiberger C, Kazi S, Brown M, Weissman S, Hong K et al (2020) Effectiveness of radiofrequency ablation in the treatment of painful osseous metastases: a correlation meta-analysis with machine learning cluster identification. J Vasc Interv Radiol 31(11):1753–1762. https://doi.org/10.1016/j.jvir.2020.08.002
Erie AJ, Morris JM, Welch BT, Kurup AN, Weisbrod AJ, Atwell TD et al (2017) Retrospective review of percutaneous image-guided ablation of oligometastatic prostate cancer: a single-institution experience. J Vasc Interv Radiol 28(7):987–992. https://doi.org/10.1016/j.jvir.2017.03.012
Ost P, Jereczek-Fossa BA, As NV, Zilli T, Muacevic A, Olivier K et al (2016) Progression-free Survival Following Stereotactic Body Radiotherapy for Oligometastatic Prostate Cancer Treatment-naive Recurrence: A Multi-institutional Analysis. Eur Urol 69(1):9–12. https://doi.org/10.1016/j.eururo.2015.07.004
Jereczek-Fossa BA, Beltramo G, Fariselli L, Fodor C, Santoro L, Vavassori A et al (2012) Robotic image-guided stereotactic radiotherapy, for isolated recurrent primary, lymph node or metastatic prostate cancer. Int J Radiat Oncol Biol Phys 82(2):889–897. https://doi.org/10.1016/j.ijrobp.2010.11.031
Mohler JL, Antonarakis ES, Armstrong AJ, D’Amico AV, Davis BJ, Dorff T et al (2019) Prostate cancer, version 2.2019, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 17(5):479–505. https://doi.org/10.6004/jnccn.2019.0023
Rogowski P, Roach M 3rd, Schmidt-Hegemann NS, Trapp C, von Bestenbostel R, Shi R et al (2021) Radiotherapy of oligometastatic prostate cancer: a systematic review. Radiat Oncol 16(1):50. https://doi.org/10.1186/s13014-021-01776-8
Yan M, Moideen N, Bratti VF, Moraes FY (2020) Stereotactic body radiotherapy (SBRT) in metachronous oligometastatic prostate cancer: a systematic review and meta-analysis on the current prospective evidence. Br J Radiol 93(1116):20200496. https://doi.org/10.1259/bjr.20200496
Marvaso G, Volpe S, Pepa M, Augugliaro M, Corrao G, Biffi A et al (2021) Oligorecurrent prostate cancer and stereotactic body radiotherapy: where are we now? A systematic review and meta-analysis of prospective studies. Eur Urol Open Sci 27:19–28. https://doi.org/10.1016/j.euros.2021.02.008
Viani GA, Arruda CV, Hamamura AC, Faustino AC, Freitas Bendo Danelichen A, Guimaraes FS (2020) Stereotactic body radiotherapy for oligometastatic prostate cancer recurrence: a meta-analysis. Am J Clin Oncol 43(2):73–81. https://doi.org/10.1097/COC.0000000000000635
Olson R, Mathews L, Liu M, Schellenberg D, Mou B, Berrang T et al (2020) Stereotactic ablative radiotherapy for the comprehensive treatment of 1–3 Oligometastatic tumors (SABR-COMET-3): study protocol for a randomized phase III trial. BMC Cancer 20(1):380. https://doi.org/10.1186/s12885-020-06876-4
Palma DA, Olson R, Harrow S, Correa RJM, Schneiders F, Haasbeek CJA et al (2019) Stereotactic ablative radiotherapy for the comprehensive treatment of 4–10 oligometastatic tumors (SABR-COMET-10): study protocol for a randomized phase III trial. BMC Cancer 19(1):816. https://doi.org/10.1186/s12885-019-5977-6
Connor MJ, Shah TT, Smigielska K, Day E, Sukumar J, Fiorentino F et al (2021) Additional treatments to the local tumour for metastatic prostate cancer-assessment of novel treatment algorithms (IP2-ATLANTA): protocol for a multicentre, phase II randomised controlled trial. BMJ Open 11(2):e042953. https://doi.org/10.1136/bmjopen-2020-042953
Acknowledgements
The following authors are part of EAU YAU Prostate cancer Working Party: Igor Tsaur, Roman A. Blaheta, Maximilian Brandt, Robert Dotzauer, Jonathan Olivier, Giorgio Gandaglia and Christian Surcel.
Author information
Authors and Affiliations
Consortia
Contributions
IT: project development, data collection and management, data analysis, manuscript writing, manuscript editing. RAB: project development, data collection and management, data analysis, manuscript writing, manuscript editing. RD: project development, data collection and management, data analysis, manuscript writing, manuscript editing. MPB: manuscript writing, manuscript editing. GG: manuscript writing, manuscript editing. IS: manuscript writing, manuscript editing. CM: project development, data collection and management, data analysis, manuscript writing, manuscript editing. JO: project development, data collection and management, data analysis, manuscript writing, manuscript editing. CS: project development, data collection and management, data analysis, manuscript writing, manuscript editing.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there are no conflicts of interest.
Research involving human participants and/or animals
None.
Informed consent
Non-applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Tsaur, I., Blaheta, R.A., Dotzauer, R. et al. Focal therapy for primary tumor and metastases in de novo or recurrent oligometastatic prostate cancer: current standing and future perspectives. World J Urol 41, 2077–2090 (2023). https://doi.org/10.1007/s00345-022-04162-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00345-022-04162-5