Potential Impact of the Z0011 Trial on the Omission of Axillary Dissection: A Retrospective Cohort Study

Abstract

Objective To evaluate the number of patients with early-stage breast cancer who could benefit from the omission of axillary surgery following the application of the Alliance for Clinical Trials in Oncology (ACOSOG) Z0011 trial criteria.

Methods A retrospective cohort study conducted in the Hospital da Mulher da Universidade Estadual de Campinas. The study population included 384 women diagnosed with early-stage invasive breast cancer, clinically negative axilla, treated with breast-conserving surgery and sentinel lymph node biopsy, radiation therapy, chemotherapy and/or endocrine therapy, from January 2005 to December 2010. The ACOSOG Z0011 trial criteria were applied to this population and a statistical analysis was performed to make a comparison between populations.

Results A total of 384 patients underwent breast-conserving surgery and sentinel lymph node biopsy. Of the total number of patients, 86 women underwent axillary lymph node dissection for metastatic sentinel lymph nodes (SNLs). One patient underwent axillary node dissection due to a suspicious SLN intraoperatively, thus, she was excluded from the study. Among these patients, 82/86 (95.3%) had one to two involved sentinel lymph nodes and met the criteria for the ACOSOG Z0011 trial with the omission of axillary lymph node dissection. Among the 82 eligible women, there were only 13 cases (15.9%) of lymphovascular invasion and 62 cases (75.6%) of tumors measuring up to 2 cm in diameter (T1).

Conclusion The ACOSOG Z0011 trial criteria can be applied to a select group of SLN-positive patients, reducing the costs and morbidities of breast cancer surgery.

Resumo

Objetivo Avaliar o número de pacientes com câncer de mama em estágio inicial que se beneficiariam da omissão da linfadenectomia axilar segundo o protocolo Z0011 da Alliance for Clinical Trials in Oncology (ACOSOG).

Métodos Estudo de coorte retrospectiva conduzido no Hospital da Mulher da Universidade Estadual de Campinas. Foram incluídas mulheres diagnosticadas com carcinoma invasivo de mama em estágio inicial, com axila clinicamente negativa, tratadas com cirurgia conservadora e biópsia do linfonodo sentinela, radioterapia, quimioterapia e/ou hormonioterapia, de janeiro de 2005 a dezembro de 2010. Os critérios do estudo da ACOSOG Z0011 foram aplicados a essas mulheres e foi realizada uma análise estatística que comparou ambas as populações dos estudos.

Resultados Foram estudadas 384 mulheres submetidas a cirurgia conservadora de mama e biópsia do linfonodo sentinela. Entre elas, 86 mulheres foram submetidas a linfadenectomia axilar por metástase presente no linfonodo sentinela. Uma paciente foi submetida a linfadenectomia axilar por ter um linfonodo palpável suspeito no intraoperatório, não incluída no estudo. Entre essas 86 pacientes, 82 (95,3%) tiveram de 1 a 2 linfonodos sentinela comprometidos e seriam elegíveis para omissão da linfadenectomia axilar pelos critérios do ACOSOG Z0011. Entre as 82 pacientes elegíveis, apenas 13 (15,9%) delas apresentaram tumores com invasão angiolinfática, e 62 (75,6%) dos tumores mediram até 2 cm (T1).

Conclusão Os critérios do estudo ACOZOG Z0011 podem ser aplicados a um seleto grupo de pacientes com linfonodo sentinela positivo reduzindo os custos e a morbidade cirúrgica do tratamento do câncer de mama.

Keywords

breast cancer - sentinel lymph node biopsy - lymph node dissection - axilla - clinical trial

Palavras-chave

câncer de mama - biópsia do linfonodo sentinel - dissecção de linfonodos - axila - estudo clínico

Contributors

J. Y. S. and K. P. S. contributed to the surgery, conception and design, acquisition, analysis, and interpretation of data, as well as drafting of the manuscript. C. C. was involved in the surgery and drafting of the manuscript. C. C. F. was involved in the surgery and acquisition of data. C. E. was involved in the acquisition of data. L. C. Z. critically revised the manuscript for important intellectual content. All authors approved the final version to be published and agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work were appropriately investigated and resolved.

Publication History

Received: 10 August 2020

Accepted: 21 December 2020

Article published online:
30 March 2021

• References

• 1 Veronesi U, Paganelli G, Viale G, Galimberti V, Luini A, Zurrida S. et al. Sentinel lymph node biopsy and axillary dissection in breast cancer: results in a large series. J Natl Cancer Inst 1999; 91 (04) 368-373
• 2 Veronesi U, Paganelli G, Viale G, Galimberti V, Luini A, Zurrida S. et al. A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med 2003; 349 (06) 546-553
• 3 Mansel RE, Fallowfield L, Kissin M, Goyal A, Newcombe RG, Dixon JM. et al. Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC Trial. J Natl Cancer Inst 2006; 98 (09) 599-609
• 4 Veronesi U, Viale G, Paganelli G, Zurrida S, Luini A, Galimberti V. et al. Sentinel lymph node biopsy in breast cancer: ten-year results of a randomized controlled study. Ann Surg 2010; 251 (04) 595-600
• 5 Krag DN, Anderson SJ, Julian TB. et al. Sentinel-lymph-node resection compared with conventional axillary-lymph-node dissection in clinically node-negative patients with breast cancer: overall survival findings from the NSABP B-32 randomised phase 3 trial. Lancet Oncol 2010; 11 (10) 927-933
• 6 de Boniface J, Frisell J, Bergkvist L, Andersson Y. Swedish Breast Cancer Group and the Swedish Society of Breast Surgery. Ten-year report on axillary recurrence after negative sentinel node biopsy for breast cancer from the Swedish Multicentre Cohort Study. Br J Surg 2017; 104 (03) 238-247
• 7 Van Zee KJ, Manasseh DM, Bevilacqua JL, Boolbol SK, Fey JV, Tan LK. et al. A nomogram for predicting the likelihood of additional nodal metastases in breast cancer patients with a positive sentinel node biopsy. Ann Surg Oncol 2003; 10 (10) 1140-1151
• 8 Giuliano AE, McCall L, Beitsch P, Whitworth PW, Blumencranz P, Leitch AM. et al. Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: the American College of Surgeons Oncology Group Z0011 randomized trial. Ann Surg 2010; 252 (03) 426-432, discussion 432–433
• 9 Donker M, van Tienhoven G, Straver ME, Meijnen P, van de Velde CJ, Mansel RE. 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) 1303-1310
• 10 Morrow M, Van Zee KJ, Patil S, Petruolo O, Mamtani A, Barrio AV. 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 (03) 457-462
• 11 Verheuvel NC, Voogd AC, Tjan-Heijnen VCG, Roumen RMH. Potential impact of application of Z0011 derived criteria to omit axillary lymph node dissection in node positive breast cancer patients. Eur J Surg Oncol 2016; 42 (08) 1162-1168
• 12 Delpech Y, Bricou A, Lousquy R, Hudry D, Jankowski C, Willecocq C. et al. The exportability of the ACOSOG Z0011 criteria for omitting axillary lymph node dissection after positive sentinel lymph node biopsy findings: a multicenter study. Ann Surg Oncol 2013; 20 (08) 2556-2561
• 13 Ribeiro Pereira ACP, Koifman RJ, Bergmann A. Incidence and risk factors of lymphedema after breast cancer treatment: 10 years of follow-up. Breast 2017; 36: 67-73
• 14 Fleissig A, Fallowfield LJ, Langridge CI, Johnson L, Newcombe RG, Dixon JM. et al. Post-operative arm morbidity and quality of life. Results of the ALMANAC randomised trial comparing sentinel node biopsy with standard axillary treatment in the management of patients with early breast cancer. Breast Cancer Res Treat 2006; 95 (03) 279-293
• 15 Sackey H, Magnuson A, Sandelin K, Liljegren G, Bergkvist L, Fulep ZF. et al. Arm lymphoedema after axillary surgery in women with invasive breast cancer. Br J Surg 2014; 101 (04) 390-397
• 16 De Gournay E, Guyomard A, Coutant C, Boulet S, Arveux P, Causeret S. et al. Impact of sentinel node biopsy on long-term quality of life in breast cancer patients. Br J Cancer 2013; 109 (11) 2783-2791
• 17 Pugliese MS, Karam AK, Hsu M, Stempel MM, Patil SM, Ho AY. et al. Predictors of completion axillary lymph node dissection in patients with immunohistochemical metastases to the sentinel lymph node in breast cancer. Ann Surg Oncol 2010; 17 (04) 1063-1068
• 18 Vieni S, Graceffa G, La Mendola R, Latteri S, Cordova A, Latteri MA. et al. Application of a predictive model of axillary lymph node status in patients with sentinel node metastasis from breast cancer. A retrospective cohort study. Int J Surg 2016; 35: 58-63
• 19 Giuliano AE, Ballman K, McCall L, Beitsch P, Whitworth PW, Blumencranz P. et al. Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases. Long-term follow-up from the American College of Surgeons Oncology Group (Alliance) ACOSOG Z0011 randomized trial. Ann Surg 2016; 264 (03) 413-420