Skip to main content

Advertisement

SpringerLink
Log in

Clinical and pathological characterization of 158 consecutive and unselected oligometastatic breast cancers in a single institution

  • Clinical trial
  • Published:
Breast Cancer Research and Treatment Aims and scope Submit manuscript

Abstract

Purpose

Data about incidence, biological, and clinical characteristics of oligometastatic breast cancer (OMBC) are scarce. However, these data are essential in determining optimal treatment strategy. Gaining knowledge of these elements means observing and describing large, recent, and consecutive series of OMBC in their natural history.

Methods

We collected data retrospectively at our institution from 998 consecutive patients diagnosed and treated with synchronous or metachronous metastatic breast cancer (MBC) between January 2014 and December 2018. The only criterion used to define OMBC was the presence of one to five metastases at diagnosis.

Results

Of 998 MBC, 15.8% were classified OMBC. Among these, 88% had one to three metastases, and 86.7% had only one organ involved. Bone metastases were present in 52.5% of cases, 20.9% had progression to lymph nodes, 14.6% to the liver, 13.3% to the brain, 8.2% to the lungs, and 3.8% had other metastases. 55.7% had HR+/HER2− OMBC, 25.3% had HER2+OMBC, and 19% had HR−/HER2− OMBC. The HR+/HER2− subtype statistically correlated with bone metastases (p = 0.001), the HER2+subtype with brain lesions (p = 0.001), and the HR−/HER2− subtype with lymph node metastases (p = 0.008). Visceral metastases were not statistically associated with any OMBC subtypes (p = 0.186). OMBC-SBR grade III was proportionally higher than in the ESME series of 22,109 MBC (49.4% vs. 35.1%, p < 0.001).

Conclusion

OMBC is a heterogeneous entity whose incidence is higher than has commonly been published. Not an indolent disease, each subgroup, with its biological and anatomical characteristics, merits specific management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are not publicly available. They include personal data resulting from medical care but are available from the corresponding author on reasonable request.

References

  1. Hellman S, Weichselbaum RR (1995) Oligometastases. J Clin Oncol Off J Am Soc Clin Oncol 13:8–10. https://doi.org/10.1200/JCO.1995.13.1.8

    Article  CAS  Google Scholar 

  2. Weichselbaum RR, Hellman S (2011) Oligometastases revisited. Nat Rev Clin Oncol 8:378–382. https://doi.org/10.1038/nrclinonc.2011.44

    Article  CAS  PubMed  Google Scholar 

  3. Iyengar P, Wardak Z, Gerber DE, Tumati V, Ahn C, Hughes RS et al (2018) Consolidative radiotherapy for limited metastatic non–small-cell lung cancer: a phase 2 randomized clinical trial. JAMA Oncol 4:e173501. https://doi.org/10.1001/jamaoncol.2017.3501

    Article  PubMed  Google Scholar 

  4. Palma DA, Olson R, Harrow S, Gaede S, Louie AV, Haasbeek C et al (2019) Stereotactic ablative radiotherapy versus standard of care palliative treatment in patients with Oligometastatic cancers (SABR-COMET): a randomised, phase 2, open-label trial. The Lancet 393:2051–2058. https://doi.org/10.1016/S0140-6736(18)32487-5

    Article  Google Scholar 

  5. Guckenberger M, Lievens Y, Bouma AB, Collette L, Dekker A, deSouza NM et al (2020) Characterisation and classification of Oligometastatic disease: a European society for radiotherapy and oncology and European organisation for research and treatment of cancer consensus recommendation. Lancet Oncol 21:e18-28. https://doi.org/10.1016/S1470-2045(19)30718-1

    Article  PubMed  Google Scholar 

  6. Chmura SJ, Winter KA, Woodward WA, Borges VF, Salama JK, Al-Hallaq HA et al (2022) NRG-BR002: A phase IIR/III trial of standard of care systemic therapy with or without stereotactic body radiotherapy (SBRT) and/or surgical resection (SR) for newly Oligometastatic breast cancer (NCT02364557). J Clin Oncol 40:1007–1007. https://doi.org/10.1200/JCO.2022.40.16_suppl.1007

    Article  Google Scholar 

  7. Tree AC, Khoo VS, Eeles RA, Ahmed M, Dearnaley DP, Hawkins MA et al (2013) Stereotactic body radiotherapy for oligometastases. Lancet Oncol 14:e28-37. https://doi.org/10.1016/S1470-2045(12)70510-7

    Article  PubMed  Google Scholar 

  8. Salama JK, Kirkpatrick JP, Yin F-F (2012) Stereotactic body radiotherapy treatment of extracranial metastases. Nat Rev Clin Oncol 9:654–665. https://doi.org/10.1038/nrclinonc.2012.166

    Article  CAS  PubMed  Google Scholar 

  9. Yu JB, Brock KK, Campbell AM, Chen AB, Diaz R, Escorcia FE et al (2020) Proceedings of the ASTRO-RSNA Oligometastatic disease research workshop. Int J Radiat Oncol Biol Phys 108:539–545. https://doi.org/10.1016/j.ijrobp.2020.05.018

    Article  PubMed  Google Scholar 

  10. Viani GA, Gouveia AG, Louie AV, Korzeniowski M, Pavoni JF, Hamamura AC et al (2021) Stereotactic body radiotherapy to treat breast cancer oligometastases: a systematic review with meta-analysis. Radiother Oncol J Eur Soc Ther Radiol Oncol 164:245–250. https://doi.org/10.1016/j.radonc.2021.09.031

    Article  Google Scholar 

  11. Lievens Y, Guckenberger M, Gomez D, Hoyer M, Iyengar P, Kindts I et al (2020) Defining Oligometastatic disease from a radiation oncology perspective: an ESTRO-ASTRO consensus document. Radiother Oncol J Eur Soc Ther Radiol Oncol 148:157–166. https://doi.org/10.1016/j.radonc.2020.04.003

    Article  Google Scholar 

  12. Franklin JM, Sharma RA, Harris AL, Gleeson FV (2016) Imaging Oligometastatic cancer before local treatment. Lancet Oncol 17:e406–e414. https://doi.org/10.1016/S1470-2045(16)30277-7

    Article  PubMed  Google Scholar 

  13. deSouza NM, Liu Y, Chiti A, Oprea-Lager D, Gebhart G, Van Beers BE et al (1990) Strategies and technical challenges for imaging Oligometastatic disease: recommendations from the European Organisation for Research and Treatment of Cancer imaging group. Eur J Cancer Oxf Engl 2018(91):153–163. https://doi.org/10.1016/j.ejca.2017.12.012

    Article  Google Scholar 

  14. Lacaze J-L, Aziza R, Chira C, De Maio E, Izar F, Jouve E et al (2021) Diagnosis, biology and epidemiology of Oligometastatic breast cancer. The Breast 59:144–156. https://doi.org/10.1016/j.breast.2021.06.010

    Article  PubMed  PubMed Central  Google Scholar 

  15. van Ommen-Nijhof A, Steenbruggen TG, Schats W, Wiersma T, Horlings HM, Mann R et al (2020) Prognostic factors in patients with Oligometastatic breast cancer - a systematic review. Cancer Treat Rev 91:102114. https://doi.org/10.1016/j.ctrv.2020.102114

    Article  CAS  PubMed  Google Scholar 

  16. Cardoso F, Paluch-Shimon S, Senkus E, Curigliano G, Aapro MS, André F et al (2020) 5th ESO-ESMO international consensus guidelines for advanced breast cancer (ABC 5). Ann Oncol 31:1623–1649. https://doi.org/10.1016/j.annonc.2020.09.010

    Article  CAS  PubMed  Google Scholar 

  17. Steenbruggen TG, Schaapveld M, Horlings HM, Sanders J, Hogewoning SJ, Lips EH et al (2021) Characterization of Oligometastatic disease in a real-world nationwide cohort of 3447 patients with de novo metastatic breast cancer. JNCI Cancer Spectr 5:pkab010. https://doi.org/10.1093/jncics/pkab010

    Article  PubMed  PubMed Central  Google Scholar 

  18. Selvarajan G, Dhanushkodi M, Radhakrishnan V, Murali CS, Ananthi B, Iyer P et al (2022) The continuing conundrum in Oligometastatic breast carcinoma: a real-world data. Breast Off J Eur Soc Mastol 63:140–148. https://doi.org/10.1016/j.breast.2022.03.010

    Article  Google Scholar 

  19. Lan B, Abudureheiyimu N, Zhang J, Wang C, Jiang S, Wang J et al (2020) Clinical features and prognostic factors for extracranial oligometastatic breast cancer in China. Int J Cancer 147:3199–3205. https://doi.org/10.1002/ijc.33152

    Article  CAS  PubMed  Google Scholar 

  20. Deluche E, Antoine A, Bachelot T, Lardy-Cleaud A, Dieras V, Brain E et al (2020) Contemporary outcomes of metastatic breast cancer among 22,000 women from the multicentre ESME cohort 2008–2016. Eur J Cancer 129:60–70. https://doi.org/10.1016/j.ejca.2020.01.016

    Article  CAS  PubMed  Google Scholar 

  21. Kelly P, Ma Z, Baidas S, Moroose R, Shah N, Dagan R et al (2017) Patterns of progression in metastatic estrogen receptor positive breast cancer: an argument for local therapy. Int J Breast Cancer. https://doi.org/10.1155/2017/1367159

    Article  PubMed  PubMed Central  Google Scholar 

  22. Grégoire V, Ang K, Budach W, Grau C, Hamoir M, Langendijk JA et al (2014) Delineation of the neck node levels for head and neck tumors: a 2013 update. DAHANCA, EORTC, HKNPCSG, NCIC CTG, NCRI, RTOG, TROG consensus guidelines. Radiother Oncol J Eur Soc Ther Radiol Oncol 110:172–81. https://doi.org/10.1016/j.radonc.2013.10.010

    Article  Google Scholar 

  23. Chapet O, Kong F-M, Quint LE, Chang AC, Ten Haken RK, Eisbruch A et al (2005) CT-based definition of thoracic lymph node stations: an atlas from the University of Michigan. Int J Radiat Oncol Biol Phys 63:170–178. https://doi.org/10.1016/j.ijrobp.2004.12.060

    Article  PubMed  Google Scholar 

  24. [Recommendations for the immunohistochemistry of the hormonal receptors on paraffin sections in breast cancer. Update (1999) Group for Evaluation of prognostic factors using immunohistochemistry in breast cancer (GEFPICS-FNCLCC)]. Ann Pathol 1999(19):336–343

    Google Scholar 

  25. Harbeck N, Penault-Llorca F, Cortes J, Gnant M, Houssami N, Poortmans P et al (2019) Breast cancer. Nat Rev Dis Primer 5:1–31. https://doi.org/10.1038/s41572-019-0111-2

    Article  Google Scholar 

  26. Dorn PL, Meriwether A, LeMieux M, Weichselbaum RR, Chmura SJ, Hasan Y (2011) Patterns of distant failure and progression in breast cancer: implications for the treatment of Oligometastatic disease. Int J Radiat Oncol Biol Phys 81:S643. https://doi.org/10.1016/j.ijrobp.2011.06.1901

    Article  Google Scholar 

  27. Jain SK, Dorn PL, Chmura SJ, Weichselbaum RR, Hasan Y (2012) Incidence and implications of oligometastatic breast cancer. J Clin Oncol 30:e11512–e11512. https://doi.org/10.1200/jco.2012.30.15_suppl.e11512

    Article  Google Scholar 

  28. Piroth MD, Krug D, Feyer P, Baumann R, Combs S, Duma M-N et al (2022) Oligometastasis in breast cancer—current status and treatment options from a radiation oncology perspective. Strahlenther Onkol 198:601–611. https://doi.org/10.1007/s00066-022-01938-x

    Article  PubMed  PubMed Central  Google Scholar 

  29. Berghoff AS, Bago-Horvath Z, Ilhan-Mutlu A, Magerle M, Dieckmann K, Marosi C et al (2012) Brain-only metastatic breast cancer is a distinct clinical entity characterised by favourable median overall survival time and a high rate of long-term survivors. Br J Cancer 107:1454–1458. https://doi.org/10.1038/bjc.2012.440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Nagasaki E, Kudo R, Tamura M, Hayashi K, Uwagawa T, Kijima Y et al (2021) Long-term outcomes of oligometastatic breast cancer patients treated with curative intent: an updated report. Breast Cancer Tokyo Jpn. https://doi.org/10.1007/s12282-021-01240-1

    Article  Google Scholar 

  31. Kobayashi T, Ichiba T, Sakuyama T, Arakawa Y, Nagasaki E, Aiba K et al (2012) Possible clinical cure of metastatic breast cancer: lessons from our 30-year experience with Oligometastatic breast cancer patients and literature review. Breast Cancer Tokyo Jpn 19:218–237. https://doi.org/10.1007/s12282-012-0347-0

    Article  Google Scholar 

  32. Steenbruggen TG, Bouwer NI, Smorenburg CH, Rier HN, Jager A, Beelen K et al (2019) Radiological complete remission in HER2-positive metastatic breast cancer patients: what to do with trastuzumab? Breast Cancer Res Treat 178:597–605. https://doi.org/10.1007/s10549-019-05427-1

    Article  CAS  PubMed  Google Scholar 

  33. Ren Z, Li Y, Hameed O, Siegal GP, Wei S (2014) Prognostic factors in patients with metastatic breast cancer at the time of diagnosis. Pathol - Res Pract 210:301–306. https://doi.org/10.1016/j.prp.2014.01.008

    Article  CAS  PubMed  Google Scholar 

  34. Andre F, Slimane K, Bachelot T, Dunant A, Namer M, Barrelier A et al (2004) Breast cancer with synchronous metastases: trends in survival during a 14-year period. J Clin Oncol Off J Am Soc Clin Oncol 22:3302–3308. https://doi.org/10.1200/JCO.2004.08.095

    Article  Google Scholar 

  35. Cha C, Ahn SG, Yoo T-K, Kim KM, Bae SJ, Yoon C et al (2020) Local treatment in addition to endocrine therapy in hormone receptor-positive and HER2-negative Oligometastatic breast cancer patients: a retrospective multicenter analysis. Breast Care Basel Switz 15:408–414. https://doi.org/10.1159/000503847

    Article  Google Scholar 

  36. Milano MT, Katz AW, Zhang H, Huggins CF, Aujla KS, Okunieff P (2019) Oligometastatic breast cancer treated with hypofractionated stereotactic radiotherapy: some patients survive longer than a decade. Radiother Oncol J Eur Soc Ther Radiol Oncol 131:45–51. https://doi.org/10.1016/j.radonc.2018.11.022

    Article  Google Scholar 

  37. Trovo M, Furlan C, Polesel J, Fiorica F, Arcangeli S, Giaj-Levra N et al (2018) Radical radiation therapy for oligometastatic breast cancer: results of a prospective phase II trial. Radiother Oncol 126:177–180. https://doi.org/10.1016/j.radonc.2017.08.032

    Article  PubMed  Google Scholar 

  38. Yoo GS, Yu JI, Park W, Huh SJ, Choi DH (2015) Prognostic factors in breast cancer with extracranial oligometastases and the appropriate role of radiation therapy. Radiat Oncol J 33:301–309. https://doi.org/10.3857/roj.2015.33.4.301

    Article  PubMed  PubMed Central  Google Scholar 

  39. Paget S (1889) The distribution of secondary growths in cancer of the breast. The Lancet 133:571–573

    Article  Google Scholar 

  40. Fidler IJ, Poste G (2008) The, “seed and soil” hypothesis revisited. Lancet Oncol 9:808. https://doi.org/10.1016/S1470-2045(08)70201-8

    Article  PubMed  Google Scholar 

  41. Fidler IJ (2003) The pathogenesis of cancer metastasis: the “seed and soil” hypothesis revisited. Nat Rev Cancer 3:453–458. https://doi.org/10.1038/nrc1098

    Article  CAS  PubMed  Google Scholar 

  42. Klein CA (2020) Cancer progression and the invisible phase of metastatic colonization. Nat Rev Cancer 20:681–694. https://doi.org/10.1038/s41568-020-00300-6

    Article  CAS  PubMed  Google Scholar 

  43. Bertucci F, Ng CKY, Patsouris A, Droin N, Piscuoglio S, Carbuccia N et al (2019) Genomic characterization of metastatic breast cancers. Nature 569:560–564. https://doi.org/10.1038/s41586-019-1056-z

    Article  CAS  PubMed  Google Scholar 

  44. Gupta GP, Massagué J (2006) Cancer metastasis: building a framework. Cell 127:679–695. https://doi.org/10.1016/j.cell.2006.11.001

    Article  CAS  PubMed  Google Scholar 

  45. Katipally RR, Pitroda SP, Juloori A, Chmura SJ, Weichselbaum RR (2022) The oligometastatic spectrum in the era of improved detection and modern systemic therapy. Nat Rev Clin Oncol 19:585–599. https://doi.org/10.1038/s41571-022-00655-9

    Article  PubMed  Google Scholar 

  46. Reyes DK, Pienta KJ (2015) The biology and treatment of Oligometastatic cancer. Oncotarget 6:8491–524. https://doi.org/10.18632/oncotarget.3455

    Article  PubMed  PubMed Central  Google Scholar 

  47. Palma DA, Salama JK, Lo SS, Senan S, Treasure T, Govindan R et al (2014) The oligometastatic state—separating truth from wishful thinking. Nat Rev Clin Oncol 11:549–557. https://doi.org/10.1038/nrclinonc.2014.96

    Article  PubMed  Google Scholar 

  48. Wuerstlein R, Cardoso F, Haidinger R (2022) Expert discussion: highlights from ABC6: bridging the gap and insights in this first virtual ABC conference and from 10 years ABC consensus. Breast Care 17:107–112. https://doi.org/10.1159/000521342

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Gail Taillefer, native speaker experienced in scientific publication and Emeritus professor of English, for her review of the manuscript.

Funding

The authors declare that no funds, grants, or other support was received during the preparation of this manuscript.

Author information

Authors and Affiliations

  1. Départment d’Oncologie Médicale, Institut Claudius Regaud (ICR), Institut Universitaire du Cancer de Toulouse-Oncopole (IUCT-O), 1 Av. Irène Joliot Curie, 31059, Toulouse Cedex 9, France

    Jean-Louis Lacaze, Eleonora De Maio, Clémence Brac de la Perrière, Mony Ung & Vincent Nicolai

  2. Département de Radiothérapie, Institut Claudius Regaud (ICR), Institut Universitaire du Cancer de Toulouse-Oncopole (IUCT-O), 1 Av. Irène Joliot Curie, 31059, Toulouse Cedex 9, France

    Ciprian Chira, Gauthier Glemarec & Carole Massabeau

  3. Biostatistics & Health Data Science Unit, Institut Claudius Regaud (ICR), Institut Universitaire du Cancer de Toulouse-Oncopole (IUCT-O), 1 Av. Irène Joliot Curie, 31059, Toulouse Cedex 9, France

    Nils Monselet & Bastien Cabarrou

  4. Département de Chirurgie, Institut Claudius Regaud (ICR), Institut Universitaire du Cancer de Toulouse-Oncopole (IUCT-O), 1 Av. Irène Joliot Curie, 31059, Toulouse Cedex 9, France

    Eva Jouve & Gabrielle Selmes

  5. Département de Médecine Nucléaire, Institut Claudius Regaud (ICR), Institut Universitaire du Cancer de Toulouse-Oncopole (IUCT-O), 1 Av. Irène Joliot Curie, 31059, Toulouse Cedex 9, France

    Thibaut Cassou-Mounat

  6. Département d’Oncologie Médicale, Institut Claudius Regaud (ICR), Institut Universitaire du Cancer de Toulouse-Oncopole (IUCT-O), Université de Toulouse, UPS, 1 av. Irène Joliot Curie, 31059, Toulouse Cedex 9, France

    Florence Dalenc

Authors
  1. Jean-Louis Lacaze
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ciprian Chira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gauthier Glemarec
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nils Monselet
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thibaut Cassou-Mounat
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eleonora De Maio
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Eva Jouve
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Carole Massabeau
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Clémence Brac de la Perrière
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Gabrielle Selmes
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Mony Ung
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Vincent Nicolai
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Bastien Cabarrou
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Florence Dalenc
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Dr. J-LL, Dr. GG, MBC, and MNM. The first draft of the manuscript was written by Dr. J-LL, and all authors commented on the previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Jean-Louis Lacaze.

Ethics declarations

Competing Interests

The authors have no relevant financial or non-financial interests to disclose.

Ethical approval

This retrospective and observational study was approved by our Multidisciplinary Breast Committee and our Institutional Board Committee (BEC-FO-0227).

Consent to participate

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 21 KB)

Supplementary file2 (DOCX 19 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) 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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lacaze, JL., Chira, C., Glemarec, G. et al. Clinical and pathological characterization of 158 consecutive and unselected oligometastatic breast cancers in a single institution. Breast Cancer Res Treat 198, 463–474 (2023). https://doi.org/10.1007/s10549-023-06880-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10549-023-06880-9

Keywords

Search

Navigation