To review the current understanding and recent developments regarding the concept of oligometastases in hormone-sensitive prostate cancer.
A comprehensive literature search of electronic databases, including PubMed and Embase was conducted for the search term ‘oligometastases’ in combinations with ‘prostate cancer’, ‘hormone sensitive’, ‘genetics’, and ‘molecular’. All articles relating to these search terms have been taken into account.
Prostate cancer remains a major cause of morbidity and mortality worldwide. The majority of these cancer-related deaths result from metastases. Currently, there is a dichotomy in prostate cancer management where it is only deemed curable if it is localized, while any signs of metastasis relegate patients to systemic therapies to delay their inevitable death. A growing body of evidence supports the notion that aggressive treatments during the stable ‘oligometastatic’ state can have significant clinical benefits and potentially ‘reset’ prostate cancer to an earlier time point in cancer progression. This concept of oligometastases has been adopted in other cancer settings such as colorectal and non-small-cell lung cancers.
Multiple clinical and molecular biological studies have been influential in the support of a stable state in metastatic cancer progression coined ‘oligometastases’. As our understanding of oligometastases in hormone-sensitive prostate cancer develops, we will be able to molecularly define the oligometastatic state and develop clinically available diagnostic tests. In doing so, prostate cancer patients will experience significant clinical benefits and the burden of prostate cancer worldwide will likely be reduced.
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Stewart BW, Wild CP (2014) World Cancer Report 2014. Lyon, France: International Agency for Research on Cancer. World Health Organization 630
Langley RR, Fidler IJ (2007) Tumor cell-organ microenvironment interactions in the pathogenesis of cancer metastasis. Endocr Rev 28:297–321
Mottet N, van den Bergh RCN, Briers E et al (2018) EAU Guidelines. Edn. presented at the EAU Annual Congress Copenhagen 2018. EAU Guidelines Office, Arnhem, The Netherlands
Hellman S, Weichselbaum RR (1995) Oligometastases. J Clin Oncol 13:8–10
Reyes DK, Pienta KJ (2015) The biology and treatment of oligometastatic cancer. Oncotarget 6:8491–8524
Tosoian JJ, Gorin MA, Ross AE et al (2017) Oligometastatic prostate cancer: definitions, clinical outcomes, and treatment considerations. Nat Rev Urol 14:15–25
Gillessen S, Attard G, Beer TM et al (2018) Management of patients with advanced prostate cancer: the Report of the Advanced Prostate Cancer Consensus Conference APCCC 2017. Eur Urol 73:178–211
Nordlinger B, Quilichini MA, Parc R et al (1987) Hepatic resection for colorectal liver metastases. Influence on survival of preoperative factors and surgery for recurrences in 80 patients. Ann Surg 205:256–263
Hughes KS, Rosenstein RB, Songhorabodi S et al (1988) Resection of the liver for colorectal carcinoma metastases. Dis Colon Rectum 31:1–4
Gayowski TJ, Iwatsuki S, Madariaga JR et al (1994) Experience in hepatic resection for metastatic colorectal cancer: analysis of clinical and pathologic risk factors. Surgery 116:703–710 (discussion 710–1)
Scheele J, Stang R, Altendorf-Hofmann A, Paul M (1995) Resection of colorectal liver metastases. World J Surg 19:59–71
Fong Y, Cohen AM, Fortner JG et al (1997) Liver resection for colorectal metastases. J Clin Oncol 15:938–946
Rougier PH, Milan C, Lazorthes F et al (1995) Prospective study of prognostic factors in patients with unresected hepatic metastases from colorectal cancer. Br J Surg 82:1397–1400
Fong Y, Fortner J, Sun RL et al (1999) Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg 230:309–318 (discussion 318–21)
Kanas GP, Taylor A, Primrose JN et al (2012) Survival after liver resection in metastatic colorectal cancer: review and meta-analysis of prognostic factors. Clin Epidemiol 4:283–301
Van Cutsem E, Cervantes A, Adam R et al (2016) ESMO consensus guidelines for the management of patients with metastatic colorectal cancer. Ann Oncol 27:1386–1422
Pastorino U, Buyse M, Friedel G et al (1997) Long-term results of lung metastasectomy: prognostic analyses based on 5206 cases. J Thorac Cardiovasc Surg 113:37–49
Pfannschmidt J, Dienemann H (2010) Surgical treatment of oligometastatic non-small cell lung cancer. Lung Cancer 69:251–258
Peters S, Adjei AA, Gridelli C et al (2012) Metastatic non-small-cell lung cancer (NSCLC): ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 23(Suppl 7):56–64
Richards P, McKISSOCK W (1963) Intracranial metastases. Br Med J 1:15–18
Gomez DR, Blumenschein GR Jr, Lee JJ et al (2016) Local consolidative therapy versus maintenance therapy or observation for patients with oligometastatic non-small-cell lung cancer without progression after first-line systemic therapy: a multicentre, randomised, controlled, phase 2 study. Lancet Oncol 17:1672–1682
Iyengar P, Wardak Z, Gerber DE et al (2018) Consolidative radiotherapy for limited metastatic non-small-cell lung cancer: a phase 2 randomized clinical trial. JAMA Oncol 4:e173501
Yao HH, Hong MK, Corcoran NM et al (2014) Advances in local and ablative treatment of oligometastasis in prostate cancer. Asia Pac J Clin Oncol 10:308–321
Koo KC, Dasgupta P (2018) Treatment of oligometastatic hormone-sensitive prostate cancer: a comprehensive review. Yonsei Med J 59:567–579
Culp SH, Schellhammer PF, Williams MB (2014) Might men diagnosed with metastatic prostate cancer benefit from definitive treatment of the primary tumor? A SEER-based study. Eur Urol 65:1058–1066
Gratzke C, Engel J, Stief CG (2014) Role of radical prostatectomy in metastatic prostate cancer: data from the Munich Cancer Registry. Eur Urol 66:602–603
Heidenreich A, Pfister D, Porres D (2015) Cytoreductive radical prostatectomy in patients with prostate cancer and low volume skeletal metastases: results of a feasibility and case-control study. J Urol 193:832–838
Cho Y, Chang JS, Rha KH et al (2016) Does radiotherapy for the primary tumor benefit prostate cancer patients with distant metastasis at initial diagnosis? PLoS One 11:e0147191
Ost P, Reynders D, Decaestecker K et al (2018) Surveillance or metastasis-directed therapy for oligometastatic prostate cancer recurrence: a prospective, randomized, multicenter phase II trial. J Clin Oncol 36:446–453
Tree AC, Khoo VS, Eeles RA et al (2013) Stereotactic body radiotherapy for oligometastases. Lancet Oncol 14:e28–e37
Campbell PJ, Yachida S, Mudie LJ et al (2010) The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 467:1109–1113
Yachida S, Jones S, Bozic I et al (2010) Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 467:1114–1117
Gerlinger M, Rowan AJ, Horswell S et al (2012) Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 366:883–892
Wuttig D, Baier B, Fuessel S et al (2009) Gene signatures of pulmonary metastases of renal cell carcinoma reflect the disease-free interval and the number of metastases per patient. Int J Cancer 125:474–482
Pitroda SP, Khodarev NN, Huang L et al (2018) Integrated molecular subtyping defines a curable oligometastatic state in colorectal liver metastasis. Nat Commun 9:1793
Lussier YA, Khodarev NN, Regan K et al (2012) Oligo- and polymetastatic progression in lung metastasis(es) patients is associated with specific microRNAs. PLoS One 7:e50141
Wong AC, Watson SP, Pitroda SP et al (2016) Clinical and molecular markers of long-term survival after oligometastasis-directed stereotactic body radiotherapy (SBRT). Cancer 122:2242–2250
Uppal A, Ferguson MK, Posner MC et al (2014) Towards a molecular basis of oligometastatic disease: potential role of micro-RNAs. Clin Exp Metastasis 31:735–748
Zhang H-W, Wang E-W, Li L-X et al (2016) A regulatory loop involving miR-29c and Sp1 elevates the TGF-β1 mediated epithelial-to-mesenchymal transition in lung cancer. Oncotarget 7:85905–85916
Harazono Y, Muramatsu T, Endo H et al (2013) miR-655 Is an EMT-suppressive microRNA targeting ZEB1 and TGFBR2. PLoS One 8:e62757
Huang B, Luo W, Sun L et al (2013) MiRNA-125a-3p is a negative regulator of the RhoA-actomyosin pathway in A549 cells. Int J Oncol 42:1734–1742
Anaya-Ruiz M, Bandala C, Perez-Santos JLM (2013) miR-485 acts as a tumor suppressor by inhibiting cell growth and migration in breast carcinoma T47D cells. Asian Pac J Cancer Prev 14:3757–3760
Vaira V, Faversani A, Dohi T et al (2012) miR-296 regulation of a cell polarity-cell plasticity module controls tumor progression. Oncogene 31:27–38
Dykxhoorn DM, Wu Y, Xie H et al (2009) miR-200 enhances mouse breast cancer cell colonization to form distant metastases. PLoS One 4:e7181
Korpal M, Ell BJ, Buffa FM et al (2011) Direct targeting of Sec23a by miR-200 s influences cancer cell secretome and promotes metastatic colonization. Nat Med 17:1101–1108
Sapre N, Hong MKH, Macintyre G et al (2014) Curated microRNAs in urine and blood fail to validate as predictive biomarkers for high-risk prostate cancer. PLoS One 9:e91729
Hong MKH, Macintyre G, Wedge DC et al (2015) Tracking the origins and drivers of subclonal metastatic expansion in prostate cancer. Nat Commun 6:6605
Shah RB, Mehra R, Chinnaiyan AM et al (2004) Androgen-independent prostate cancer is a heterogeneous group of diseases: lessons from a rapid autopsy program. Cancer Res 64:9209–9216
Yuhas JM, Tarleton AE (1978) Dormancy and spontaneous recurrence of human breast cancer in vitro. Cancer Res 38:3584–3589
Braun S, Vogl FD, Naume B et al (2005) A pooled analysis of bone marrow micrometastasis in breast cancer. N Engl J Med 353:793–802
Kobayashi A, Okuda H, Xing F et al (2011) Bone morphogenetic protein 7 in dormancy and metastasis of prostate cancer stem-like cells in bone. J Exp Med 208(13):2641–2655
Zhou Y, Zhang G-J, Wang J et al (2017) Current status of lymph node micrometastasis in gastric cancer. Oncotarget 8:51963–51969
The Australian Prostate Cancer Centre Epworth is supported by the Australian Government as represented by the Department of Health and Ageing. KC is supported by a Postgraduate Medical Research Scholarship from the Prostate Cancer Research Fund, and the Research Training Program Scholarship from the Australian Commonwealth Government. NMC is supported by a Movember—Distinguished Gentleman’s Ride Clinician Scientist Award through Prostate Cancer Foundation of Australia’s Research Program.
The work had no specific source of funding.
Conflict of interest
The authors declare that they have no conflict of interest.
Research involving human participants and/or animals
This review does not contain any studies with human participants or animals performed by any of the authors.
Informed consent was not solicited as it was not applicable in this review.
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Chow, K., McCoy, P., Stuchbery, R. et al. Developments in oligometastatic hormone-sensitive prostate cancer. World J Urol 37, 2549–2555 (2019). https://doi.org/10.1007/s00345-018-2542-x
- Prostate cancer
- Hormone sensitive