Skip to main content

Advertisement

Log in

The Attitudes of Brazilian Breast Surgeons on Axillary Management in Early Breast Cancer—10 Years after the ACOSOG Z0011 Trial First Publication

  • Breast Oncology
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Purpose

To evaluate the impact of the ACOSOG Z0011 trial on axillary breast cancer surgery management in Brazil following publication of that study (2010) and again in 2020.

Patients and Methods

A survey of members of the Brazilian Society of Mastology.

Results

Of 1627 breast surgeons, 799 (49.1%) completed and returned the questionnaire. For patients with the Z11 inclusion criteria, following detection of a positive sentinel lymph node (SLN), axillary dissection (AD) was recommended by 99.2% of respondents before publication of the study, 47.5% in 2010 and 18.5% in 2020 (p < 0.001). In breast-conserving surgery, if there were micro-metastases, 2.6% would perform AD, 30.3% axillary radiotherapy, and 67.1% no additional axillary treatment, while with macro-metastases, these proportions were 21.3%, 52.2%, and 26.5%, respectively. In cases of mastectomy and of nodal extracapsular extension, 43.4% and 36% of surgeons, respectively, recommended AD. For clinically negative axilla and suspicious findings at ultrasonography, 69% of the surgeons would apply the Z11 approach. Most applied the Z11 criteria in cases of younger patients (83.6%) and triple-negative and/or HER2 positive tumors (74%). AD was significantly more likely to be recommended by surgeons who did not work in academic institutes, who worked in locations other than capital cities, who were not board-certified, and who were ≥ 50 years old.

Conclusions

This survey revealed substantial changes in axillary surgery management in cN0/pathologically positive SLN, particularly following publication of the updated Z11 results and other similar studies. A better education environment and long-term follow-up were factors associated with the incorporation of Z11-related changes in practice.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Magnoni F, Galimberti V, Corso G, Intra M, Sacchini V, Veronesi P. Axillary surgery in breast cancer: an updated historical perspective. Semin Oncol. 2020;47(6):341–52. https://doi.org/10.1053/j.seminoncol.2020.09.001.

    Article  PubMed  Google Scholar 

  2. Giuliano AE, Haigh PI, Brennan MB, et al. Prospective observational study of sentinel lymphadenectomy without further axillary dissection in patients with sentinel node-negative breast cancer. J Clin Oncol. 2000;18(13):2553–9. https://doi.org/10.1200/JCO.2000.18.13.2553.

    Article  CAS  PubMed  Google Scholar 

  3. Giuliano AE, Dale PS, Turner RR, Morton DL, Evans SW, Krasne DL. Improved axillary staging of breast cancer with sentinel lymphadenectomy. Ann Surg. 1995;222(3):394–9. https://doi.org/10.1097/00000658-199509000-00016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Veronesi U, Paganelli G, Viale G, et al. A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med. 2003;349(6):546–53. https://doi.org/10.1056/nejmoa012782.

    Article  PubMed  Google Scholar 

  5. Veronesi U, Viale G, Paganelli G, et al. Sentinel lymph node biopsy in breast cancer: ten-year results of a randomized controlled study. Ann Surg. 2010;251(4):595–600. https://doi.org/10.1097/SLA.0b013e3181c0e92a.

    Article  PubMed  Google Scholar 

  6. Krag DN, Anderson SJ, Julian TB, et al. Technical outcomes of sentinel-lymph-node resection and conventional axillary-lymph-node dissection in patients with clinically node-negative breast cancer: results from the NSABP B-32 randomised phase III trial. Lancet Oncol. 2007;8(10):881–8. https://doi.org/10.1016/S1470-2045(07)70278-4.

    Article  CAS  PubMed  Google Scholar 

  7. Giuliano AE, Hunt KK, Ballman KV, et al. Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA. 2011;305(6):569–75. https://doi.org/10.1001/jama.2011.90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Giuliano AE, Ballman KV, McCall L, et al. Effect of axillary dissection vs no axillary dissection on 10-year overall survival among women with invasive breast cancer and sentinel node metastasis: the ACOSOG Z0011 (Alliance) randomized clinical trial. JAMA. 2017;318(10):918–26. https://doi.org/10.1001/jama.2017.11470.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Galimberti V, Cole BF, Zurrida S, et al. Axillary dissection versus no axillary dissection in patients with sentinel-node micrometastases (IBCSG 23–01): a phase 3 randomised controlled trial. Lancet Oncol. 2013;14(4):297–305. https://doi.org/10.1016/S1470-2045(13)70035-4.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Galimberti V, Cole BF, Viale G, et al. Axillary dissection versus no axillary dissection in patients with breast cancer and sentinel-node micrometastases (IBCSG 23–01): 10-year follow-up of a randomised, controlled phase 3 trial. Lancet Oncol. 2018;19(10):1385–93. https://doi.org/10.1016/S1470-2045(18)30380-2.

    Article  PubMed  Google Scholar 

  11. Donker M, van Tienhoven G, Straver ME, et al. Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981–22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol. 2014;15(12):1303–10. https://doi.org/10.1016/S1470-2045(14)70460-7.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Sávolt Á, Péley G, Polgár C, et al. Eight-year follow up result of the OTOASOR trial: the optimal treatment of the Axilla—surgery or radiotherapy after positive sentinel lymph node biopsy in early-stage breast cancer: a randomized, single centre, phase III, non-inferiority trial. Eur J Surg Oncol. 2017;43(4):672–9. https://doi.org/10.1016/j.ejso.2016.12.011.

    Article  PubMed  Google Scholar 

  13. NCCN Guidelines for Breast Cancer V.2.2021 – Interim on 02/23/21.

  14. Morrow M, Van Zee KJ, Patil S, et al. Axillary dissection and nodal irradiation can be avoided for most node-positive Z0011-eligible breast cancers: a prospective validation study of 793 patients. Ann Surg. 2017;266(3):457–62. https://doi.org/10.1097/SLA.0000000000002354.

    Article  PubMed  Google Scholar 

  15. Gainer SM, Hunt KK, Beitsch P, Caudle AS, Mittendorf EA, Lucci A. Changing behavior in clinical practice in response to the ACOSOG Z0011 trial: a survey of the American Society of Breast Surgeons. Ann Surg Oncol. 2012;19(10):3152–8. https://doi.org/10.1245/s10434-012-2523-z.

    Article  PubMed  Google Scholar 

  16. Massimino KP, Hessman CJ, Ellis MC, Naik AM, Vetto JT. Impact of American college of surgeons oncology group Z0011 and national surgical adjuvant breast and bowel project B-32 trial results on surgeon practice in the Pacific Northwest. Am J Surg. 2012;203(5):618–22. https://doi.org/10.1016/j.amjsurg.2011.12.015.

    Article  PubMed  Google Scholar 

  17. Pitt SC, Schwartz TA, Chu D. AAPOR reporting guidelines for survey studies. JAMA Surg. 2021. https://doi.org/10.1001/jamasurg.2021.0543.

    Article  PubMed  Google Scholar 

  18. Buzaid AC, Achatz MI, Amorim GLS, et al. Challenges in the journey of breast cancer patients in Brazil. Braz J Oncol. 2020;16:e-20200021. https://doi.org/10.5935/2526-8732.20200021.

    Article  Google Scholar 

  19. Rosa DD, Bines J, Werutsky G, et al. The impact of sociodemographic factors and health insurance coverage in the diagnosis and clinicopathological characteristics of breast cancer in Brazil: AMAZONA III study (GBECAM 0115). Breast Cancer Res Treat. 2020;183(3):749–57. https://doi.org/10.1007/s10549-020-05831-y.

    Article  PubMed  Google Scholar 

  20. Bilimoria KY, Bentrem DJ, Hansen NM, et al. Comparison of sentinel lymph node biopsy alone and completion axillary lymph node dissection for node-positive breast cancer. J Clin Oncol. 2009;27(18):2946–53. https://doi.org/10.1200/JCO.2008.19.5750.

    Article  PubMed  Google Scholar 

  21. Tinterri C, Marrazzo E, Frusone F, et al. Abstract OT3-01-02: preservation of axillary lymph nodes compared to complete dissection in T1–T2 breast cancer patients presenting 1–2 metastatic sentinel lymph nodes: a multicenter randomized clinical trial. Sinodar One Study. Cancer Res. 2020;80(4 Supplement):OT3-01-02 LP-OT3-01–2. https://doi.org/10.1158/1538-7445.SABCS19-OT3-01-02.

    Article  Google Scholar 

  22. Recht A, Comen EA, Fine RE, et al. Postmastectomy radiotherapy: an American Society of Clinical Oncology, American Society for Radiation Oncology, and Society of Surgical Oncology focused guideline update. J Clin Oncol. 2016;34(36):4431–42. https://doi.org/10.1200/JCO.2016.69.1188.

    Article  PubMed  Google Scholar 

  23. Burstein HJ, Curigliano G, Loibl S, et al. Estimating the benefits of therapy for early-stage breast cancer: the St. Gallen International Consensus Guidelines for the primary therapy of early breast cancer 2019. Ann Oncol. 2019;30(10):1541–57. https://doi.org/10.1093/annonc/mdz235.

    Article  CAS  PubMed  Google Scholar 

  24. Pepels MJE, Vestjens JH, De Boer M, et al. Models predicting non-sentinel node involvement also predict for regional recurrence in breast cancer patients without axillary treatment. Eur J Surg Oncol. 2013;39(12):1351–7. https://doi.org/10.1016/j.ejso.2013.09.006.

    Article  CAS  PubMed  Google Scholar 

  25. Tjan-Heijnen VC, de Boer M. Minimal lymph node involvement and outcome of breast cancer. The results of the Dutch MIRROR study. Discov Med. 2009;8(42):137–9.

    PubMed  Google Scholar 

  26. Mamtani A, Patil S, Stempel M, Morrow M. Axillary micrometastases and isolated tumor cells are not an indication for post-mastectomy radiotherapy in stage 1 and 2 breast cancer. Ann Surg Oncol. 2017;24(8):2182–8. https://doi.org/10.1245/s10434-017-5866-7.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Choi AH, Blount S, Perez MN, et al. Size of extranodal extension on sentinel lymph node dissection in the American College of Surgeons Oncology Group Z0011 trial era. JAMA Surg. 2015;150(12):1141–8. https://doi.org/10.1001/jamasurg.2015.1687.

    Article  PubMed  Google Scholar 

  28. Barrio AV, Downs-Canner S, Edelweiss M, et al. Microscopic extracapsular extension in sentinel lymph nodes does not mandate axillary dissection in Z0011-eligible patients. Ann Surg Oncol. 2020;27(5):1617–24. https://doi.org/10.1245/s10434-019-08104-1.

    Article  PubMed  Google Scholar 

  29. Harris CK, Tran HT, Lee K, et al. Positive ultrasound-guided lymph node needle biopsy in breast cancer may not mandate axillary lymph node dissection. Ann Surg Oncol. 2017;24(10):3004–10. https://doi.org/10.1245/s10434-017-5935-y.

    Article  PubMed  Google Scholar 

  30. Pilewskie M, Mautner SK, Stempel M, Eaton A, Morrow M. Does a positive axillary lymph node needle biopsy result predict the need for an axillary lymph node dissection in clinically node-negative breast cancer patients in the ACOSOG Z0011 Era? Ann Surg Oncol. 2016;23(4):1123–8. https://doi.org/10.1245/s10434-015-4944-y.

    Article  PubMed  Google Scholar 

  31. Paiva DM, Rodrigues VO, Cesca MG, Palma PV, Leite IC. Prevalence of lymphedema in women undergoing treatment for breast cancer in a referral center in southeastern Brazil. BMC Womens Health. 2013;13:6. https://doi.org/10.1186/1472-6874-13-6.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Vieira RA, da Costa AM, de Souza JL, et al. Risk factors for arm lymphedema in a cohort of breast cancer patients followed up for 10 years. Breast Care. 2016;11(1):45–50. https://doi.org/10.1159/000442489.

    Article  PubMed  Google Scholar 

  33. Weber WP, Barry M, Stempel MM, et al. A 10-year trend analysis of sentinel lymph node frozen section and completion axillary dissection for breast cancer: are these procedures becoming obsolete? Ann Surg Oncol. 2012;19(1):225–32. https://doi.org/10.1245/s10434-011-1823-z.

    Article  PubMed  Google Scholar 

  34. Gentilini O, Veronesi U. Abandoning sentinel lymph node biopsy in early breast cancer? A new trial in progress at the European Institute of Oncology of Milan (SOUND: sentinel node vs observation after axillary UltraSouND). Breast. 2012;21(5):678–81. https://doi.org/10.1016/j.breast.2012.06.013.

    Article  PubMed  Google Scholar 

  35. NCT01901094. Comparison of axillary lymph node dissection with axillary radiation for patients with node-positive breast cancer treated with chemotherapy. (2013). https://clinicaltrials.gov/show/nct01901094

  36. Mamounas EP, Bandos H, White JR, et al. NRG Oncology/NSABP B-51/RTOG 1304: Phase III trial to determine if chest wall and regional nodal radiotherapy (CWRNRT) post mastectomy (Mx) or the addition of RNRT to whole breast RT post breast-conserving surgery (BCS) reduces invasive breast cancer recurrence-free interval (IBCR-FI) in patients (pts) with pathologically positive axillary (PPAx) nodes who are ypN0 after neoadjuvant chemotherapy (NC). J Clin Oncol. 2019;37(15_suppl). https://doi.org/:https://doi.org/10.1200/jco.2019.37.15_suppl.tps600

Download references

Acknowledgments

The authors are grateful to Fernanda Pereira Alves and Jéssica Telles Bonavita for their administrative work in providing the relevant data on the SBM members and to all the affiliated members of the SBM who participated in this study.

Funding

None.

Author information

Authors and Affiliations

Authors

Contributions

E.C.M., F.P.C., G.N., F.Z., and R.F.J. participated in the conception and design of the study. All authors were involved in data collection. F.P.C., E.C.M., J.H.P.R., G.N., F.Z., A.B.A.S., and R.F.J. analyzed and interpreted the data. All authors contributed to the writing of the manuscript, approved the final version, and agree to be accountable for the work.

Corresponding author

Correspondence to Eduardo Camargo Millen PhD.

Ethics declarations

Disclosures

The authors declare that there are no conflicts of interest.

Ethical approval

All procedures performed in this study were in accordance with the ethical standards of the institutional and national research committees and with the 1964 Declaration of Helsinki and its later amendments. This is a survey study. All of those who answered the questionnaire agreed to participate. The completed survey forms were maintained anonymous.

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 31 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Millen, E.C., Cavalcante, F.P., Zerwes, F. et al. The Attitudes of Brazilian Breast Surgeons on Axillary Management in Early Breast Cancer—10 Years after the ACOSOG Z0011 Trial First Publication. Ann Surg Oncol 29, 1087–1095 (2022). https://doi.org/10.1245/s10434-021-10812-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-021-10812-6

Keywords

Navigation