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Changes in Surgical Management of the Axilla Over 11 Years – Report on More Than 1500 Breast Cancer Patients Treated with Neoadjuvant Chemotherapy on the Prospective I-SPY2 Trial

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

Abstract

Background

Axillary surgery after neoadjuvant chemotherapy (NAC) is becoming less extensive. We evaluated the evolution of axillary surgery after NAC on the multi-institutional I-SPY2 prospective trial.

Methods

We examined annual rates of sentinel lymph node (SLN) surgery with resection of clipped node, if present), axillary lymph node dissection (ALND), and SLN and ALND in patients enrolled in I-SPY2 from January 1, 2011 to December 31, 2021 by clinical N status at diagnosis and pathologic N status at surgery. Cochran-Armitage trend tests were calculated to evaluate patterns over time.

Results

Of 1578 patients, 973 patients (61.7%) had SLN-only, 136 (8.6%) had SLN and ALND, and 469 (29.7%) had ALND-only. In the cN0 group, ALND-only decreased from 20% in 2011 to 6.25% in 2021 (p = 0.0078) and SLN-only increased from 70.0% to 87.5% (p = 0.0020). This was even more striking in patients with clinically node-positive (cN+) disease at diagnosis, where ALND-only decreased from 70.7% to 29.4% (p < 0.0001) and SLN-only significantly increased from 14.6% to 56.5% (p < 0.0001). This change was significant across subtypes (HR−/HER2−, HR+/HER2−, and HER2+). Among pathologically node-positive (pN+) patients after NAC (n = 525) ALND-only decreased from 69.0% to 39.2% (p < 0.0001) and SLN-only increased from 6.9% to 39.2% (p < 0.0001).

Conclusions

Use of ALND after NAC has significantly decreased over the past decade. This is most pronounced in cN+ disease at diagnosis with an increase in the use of SLN surgery after NAC. Additionally, in pN+ disease after NAC, there has been a decrease in use of completion ALND, a practice pattern change that precedes results from clinical trials.

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References

  1. Giuliano AE, Dale PS, Turner RR, Morton DL, Evans SW, Krasne DL. Improved axillary staging of breast cancer with sentinel lymphadenectomy. Ann Surg. 1995;222:394–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Giuliano AE, Jones RC, Brennan M, Statman R. Sentinel lymphadenectomy in breast cancer. J Clin Oncol. 1997;15:2345–50.

    Article  CAS  PubMed  Google Scholar 

  3. Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 1994;220:391–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Krag D, Weaver D, Ashikaga T, et al. The sentinel node in breast cancer–a multicenter validation study. N Engl J Med. 1998;339:941–6.

    Article  CAS  PubMed  Google Scholar 

  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;11:927–33.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Hunt KK, Yi M, Mittendorf EA, et al. Sentinel lymph node surgery after neoadjuvant chemotherapy is accurate and reduces the need for axillary dissection in breast cancer patients. Ann Surg. 2009;250:558–66.

    Article  PubMed  Google Scholar 

  7. Gimbergues P, Abrial C, Durando X, et al. Sentinel lymph node biopsy after neoadjuvant chemotherapy is accurate in breast cancer patients with a clinically negative axillary nodal status at presentation. Ann Surg Oncol. 2008;15:1316–21.

    Article  CAS  PubMed  Google Scholar 

  8. Mamounas EP, Brown A, Anderson S, et al. Sentinel node biopsy after neoadjuvant chemotherapy in breast cancer: results from national surgical adjuvant breast and bowel project protocol B-27. J Clin Oncol. 2005;23:2694–702.

    Article  PubMed  Google Scholar 

  9. Xing Y, Foy M, Cox DD, Kuerer HM, Hunt KK, Cormier JN. Meta-analysis of sentinel lymph node biopsy after preoperative chemotherapy in patients with breast cancer. Br J Surg. 2006;93:539–46.

    Article  CAS  PubMed  Google Scholar 

  10. Kelly AM, Dwamena B, Cronin P, Carlos RC. Breast cancer sentinel node identification and classification after neoadjuvant chemotherapy-systematic review and meta analysis. Acad Radiol. 2009;16:551–63.

    Article  PubMed  Google Scholar 

  11. Boughey JC, Suman VJ, Mittendorf EA, et al. Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial. JAMA. 2013;310:1455–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kuehn T, Bauerfeind I, Fehm T, et al. Sentinel-lymph-node biopsy in patients with breast cancer before and after neoadjuvant chemotherapy (SENTINA): a prospective, multicentre cohort study. Lancet Oncol. 2013;14:609–18.

    Article  PubMed  Google Scholar 

  13. Boileau JF, Poirier B, Basik M, et al. Sentinel node biopsy following neoadjuvant chemotherapy in biopsy proven node positive breast cancer: the SN FNAC study. J Clin Oncol. 2013;31:1018.

    Article  Google Scholar 

  14. Classe J-M, Loaec C, Gimbergues P, et al. Sentinel lymph node biopsy without axillary lymphadenectomy after neoadjuvant chemotherapy is accurate and safe for selected patients: the GANEA 2 study. Breast Cancer Res Treat. 2019;173:343–52.

    Article  PubMed  Google Scholar 

  15. Piltin M, Boughey J. Axillary management: how has neoadjuvant chemotherapy changed our surgical approach? Curr Breast Cancer Rep. 2022;14:1–7. https://doi.org/10.1007/s12609-022-00442-6.

    Article  Google Scholar 

  16. Boughey JC, Alvarado MD, Lancaster RB, et al. Surgical standards for management of the axilla in breast cancer clinical trials with pathological complete response endpoint. NPJ Breast Cancer. 2018;4:26.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Khan TM, Rossi AJ, Suman V, Haffty B, Hernandez JM, Boughey JC. Is axillary radiation not inferior to axillary dissection for sentinel lymph node-positive breast cancer after neoadjuvant chemotherapy? Ann Surg Oncol. 2022;29:1526–7.

    Article  PubMed  Google Scholar 

  18. Clinicaltrials.gov. I-SPY TRIAL: Neoadjuvant and personalized adaptive novel agents to treat breast cancer (I-SPY). https://clinicaltrials.gov/ct2/show/NCT01042379. Accessed 20 March 2023.

  19. Barker AD, Sigman CC, Kelloff GJ, Hylton NM, Berry DA, Esserman LJ. I-SPY 2: an adaptive breast cancer trial design in the setting of neoadjuvant chemotherapy. Clin Pharmacol Ther. 2009;86:97–100.

    Article  CAS  PubMed  Google Scholar 

  20. Park JW, Liu MC, Yee D, et al. Adaptive randomization of neratinib in early breast cancer. N Engl J Med. 2016;375:11–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Rugo HS, Olopade OI, DeMichele A, et al. Adaptive randomization of veliparib-carboplatin treatment in breast cancer. N Engl J Med. 2016;375:23–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. van de Vijver MJ, He YD, van’t Veer LJ, et al. A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med. 2002;347:1999–2009.

    Article  PubMed  Google Scholar 

  23. DeMichele A, Berry DA, Zujewski J, et al. Developing safety criteria for introducing new agents into neoadjuvant trials. Clin Cancer Res. 2013;19:2817–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Yee D, DeMichele AM, et al. Association of event-free and distant recurrence-free survival with individual-level pathologic complete response in neoadjuvant treatment of stages 2 and 3 breast cancer: three-year follow-up analysis for the I-SPY2 adaptively randomized clinical trial. JAMA Oncol. 2020;6:1355–62.

    Article  PubMed  Google Scholar 

  25. Piltin MA, Hoskin TL, Day CN, Davis J, Boughey JC. Oncologic outcomes of sentinel lymph node surgery after neoadjuvant chemotherapy for node-positive breast cancer. Ann Surg Oncol. 2020;27:4795–801.

    Article  PubMed  Google Scholar 

  26. Nguyen TT, Hoskin TL, Day CN, et al. Decreasing use of axillary dissection in node-positive breast cancer patients treated with neoadjuvant chemotherapy. Ann Surg Oncol. 2018;25:2596–602.

    Article  PubMed  Google Scholar 

  27. Mamtani A, Barrio AV, King TA, et al. How often does neoadjuvant chemotherapy avoid axillary dissection in patients with histologically confirmed nodal metastases? results of a prospective study. Ann Surg Oncol. 2016;23:3467–74.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Srour MK, Tseng J, Luu M, Alban RF, Giuliano AE, Chung A. Patterns in the use of axillary operations for patients with node-positive breast cancer after neoadjuvant chemotherapy: a national cancer database (NCDB) analysis. Ann Surg Oncol. 2019;26:3305–11.

    Article  PubMed  Google Scholar 

  29. Naffouje SA, Barker V, Lee MC, Hoover SJ, Laronga C. Surgical management of axilla of triple-negative breast cancer in the Z1071 era: a propensity score-matched analysis of the national cancer database. Ann Surg Oncol. 2022;29:2985–97.

    Article  PubMed  Google Scholar 

  30. Naffouje SA, Sabesan A, Hoover SJ, Lee MC, Laronga C. Surgical management of the axilla of HER2+ breast cancer in the Z1071 era: a propensity-score-matched analysis of the NCDB. Ann Surg Oncol. 2021;28:8777–88.

    Article  PubMed  Google Scholar 

Download references

Funding

National Institutes of Health’s National Cancer Institute (P01 CA210961) and Quantum Leap Healthcare Collaborative.

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Authors and Affiliations

  1. Division of Breast and Melanoma Surgical Oncology, Department of Surgery, Mayo Clinic, Rochester, MN, USA

    Judy C. Boughey MD, FACS & Mara A. Piltin DO

  2. Quantum Leap Healthcare Collaborative, San Francisco, CA, USA

    Hongmei Yu PhD

  3. Breast Care Center, UCSF Health, San Francisco, CA, USA

    Catherine Lu Dugan BA

  4. Division of Surgical Oncology, Department of Surgery, Emory University School of Medicine, Atlanta, GA, USA

    Lauren Postlewait MD

  5. Ourisman Breast Center, MedStar Georgetown University, Washington, DC, USA

    Jennifer D. Son MD

  6. Department of Surgery, University of Virginia, Inova Campus, Fairfax, VA, USA

    Kirsten K. Edmiston MD, MPH, FACS

  7. Department of Surgery, Loyola University Medical Center, Maywood, IL, USA

    Constantine V. Godellas MD

  8. Division of Breast Oncology, H. Lee Moffitt Cancer Center, Tampa, FL, USA

    Marie C. Lee MD, FACS

  9. Department of Breast Surgery, Moffitt Cancer Center, Tampa, FL, USA

    Michael J. Carr MD, MS

  10. Division of Surgical Oncology, Oregon Health and Science University, Portland, OR, USA

    Jennifer E. Tonneson MD, FACS

  11. True Family Women’s Cancer Center, Swedish Cancer Institute, Seattle, WA, USA

    Angelena Crown MD

  12. Division of Surgical Oncology, The University of Alabama at Birmingham Medical Center, Birmingham, AL, USA

    Rachel B. Lancaster MD, FACS

  13. Division of Surgical Oncology, Duke University of School of Medicine, Durham, NC, USA

    Hannah E. Woriax MD

  14. Division of Surgical Oncology, University of California, San Francisco, CA, USA

    Cheryl A. Ewing MD

  15. Department of Surgery, UC San Diego, La Jolla, CA, USA

    Harrison S. Chau MD

  16. Division of Surgical Oncology, Department of Surgery, University of California, San Francisco, CA, USA

    Anne K. Patterson BS, Jasmine M. Wong MD & Michael D. Alvarado MD

  17. Department of Surgery, Stanford Hospital and Clinics, Stanford, CA, USA

    Rachel L. Yang MD, CLC

  18. Department of Breast Surgical Oncology, Ironwood Cancer and Research Centers, Scottsdale, AZ, USA

    Theresa W. Chan MD

  19. Division of Hematology and Oncology, University of Chicago, Chicago, IL, USA

    Jori B. Sheade MD

  20. Division of Surgical Oncology, University of Colorado Denver – Anschutz Medical Campus, Boulder, CO, USA

    Gretchen M. Ahrendt MD

  21. Department of Surgery, University of Kansas Cancer Center, Kansas City, KS, USA

    Kelsey E. Larson MD, FACS

  22. Department of Surgery, University of Minnesota, Minneapolis, MN, USA

    Kayla Switalla BS & Todd M. Tuttle MD

  23. Department of Breast Surgery Research, Penn Medicine at University of Pennsylvania, Philadelphia, PA, USA

    Julia C. Tchou MD, PhD, FACS

  24. Division of Breast Surgery, Columbia University Vagelos College of Physicians and Surgeons, New York, NY, USA

    Roshni Rao MD, FACS

  25. Department of Breast Surgical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA

    Nina Tamirisa MD, MS

  26. Department of Breast Surgical Oncology, Division of Surgery, The University of Texas MD Anderson Cancer Center, Houston, TX, USA

    Puneet Singh MD, FACS

  27. Department of Translational Molecular Pathology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA

    Rebekah E. Gould MS

  28. Division of Surgical Oncology, Department of Surgery, Huntington Cancer Center/Cedars Sinai Cancer, Pasadena, CA, USA

    Alicia Terando MD

  29. Department of Surgery, UC Davis Health Comprehensive Cancer Center, Sacramento, CA, USA

    Candice Sauder MD

  30. Division of Surgical Oncology and Endocrine Surgery, Department of Surgery, Vanderbilt University Medical Center, Nashville, TN, USA

    Kelly Hewitt MD

  31. Department of Surgery, Duke University Medical Center, Durham, NC, USA

    Akiko Chiba MD

  32. Departments of Surgery and Radiology, UCSF, San Francisco, CA, USA

    Laura J. Esserman MD, MBA

  33. Department of Surgery, UCSF, San Francisco, CA, USA

    Rita A. Mukhtar MD

Authors
  1. Judy C. Boughey MD, FACS
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  2. Hongmei Yu PhD
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  3. Catherine Lu Dugan BA
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  4. Mara A. Piltin DO
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  5. Lauren Postlewait MD
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  6. Jennifer D. Son MD
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  7. Kirsten K. Edmiston MD, MPH, FACS
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  8. Constantine V. Godellas MD
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  9. Marie C. Lee MD, FACS
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  10. Michael J. Carr MD, MS
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  11. Jennifer E. Tonneson MD, FACS
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  12. Angelena Crown MD
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  13. Rachel B. Lancaster MD, FACS
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  14. Hannah E. Woriax MD
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  15. Cheryl A. Ewing MD
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  16. Harrison S. Chau MD
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  17. Anne K. Patterson BS
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  18. Jasmine M. Wong MD
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  19. Michael D. Alvarado MD
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  20. Rachel L. Yang MD, CLC
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  21. Theresa W. Chan MD
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  22. Jori B. Sheade MD
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  23. Gretchen M. Ahrendt MD
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  24. Kelsey E. Larson MD, FACS
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  25. Kayla Switalla BS
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  26. Todd M. Tuttle MD
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  27. Julia C. Tchou MD, PhD, FACS
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  28. Roshni Rao MD, FACS
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  29. Nina Tamirisa MD, MS
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  30. Puneet Singh MD, FACS
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  31. Rebekah E. Gould MS
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  32. Alicia Terando MD
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  33. Candice Sauder MD
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  34. Kelly Hewitt MD
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  35. Akiko Chiba MD
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  36. Laura J. Esserman MD, MBA
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  37. Rita A. Mukhtar MD
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Corresponding author

Correspondence to Judy C. Boughey MD, FACS.

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Disclosures

Dr. Esserman is an uncompensated board member of the Quantum Leap Healthcare Collaborative, which sponsors the I-SPY TRIAL. She also reports that she is on the Blue Cross Medical Advisory Panel, is paid for travel, and is given an honorarium for her time; she leads an investigator-initiated vaccine trial for high-risk ductal carcinoma in situ, which is funded by Merck through the University of California San Francisco. There are no conflicts related to this manuscript. Dr. Singh reports funding to the institution for the trial through trial sponsors, specifically Foundation for the National Institutes of Health and ACRI. Dr. Tchou is a consultant for BD.

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Boughey, J.C., Yu, H., Dugan, C.L. et al. Changes in Surgical Management of the Axilla Over 11 Years – Report on More Than 1500 Breast Cancer Patients Treated with Neoadjuvant Chemotherapy on the Prospective I-SPY2 Trial. Ann Surg Oncol 30, 6401–6410 (2023). https://doi.org/10.1245/s10434-023-13759-y

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