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Surgical Management of the Axilla for Breast Cancer

  • Author Footnotes
    1 These authors contributed equally.
    Alison Laws
    Footnotes
    1 These authors contributed equally.
    Affiliations
    Division of Breast Surgery, Department of Surgery, Brigham and Women’s Hospital, Boston, MA, USA

    Breast Oncology Program, Dana-Farber Brigham Cancer Center, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA

    Harvard Medical School, Boston, MA, USA
    Search for articles by this author
  • Author Footnotes
    1 These authors contributed equally.
    Olga Kantor
    Footnotes
    1 These authors contributed equally.
    Affiliations
    Division of Breast Surgery, Department of Surgery, Brigham and Women’s Hospital, Boston, MA, USA

    Breast Oncology Program, Dana-Farber Brigham Cancer Center, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA

    Harvard Medical School, Boston, MA, USA
    Search for articles by this author
  • Tari A. King
    Correspondence
    Corresponding author. Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215.
    Affiliations
    Division of Breast Surgery, Department of Surgery, Brigham and Women’s Hospital, Boston, MA, USA

    Breast Oncology Program, Dana-Farber Brigham Cancer Center, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA

    Harvard Medical School, Boston, MA, USA
    Search for articles by this author
  • Author Footnotes
    1 These authors contributed equally.

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      References

        • Morton D.L.
        • Wen D.R.
        • Wong J.H.
        • et al.
        Technical Details of Intraoperative Lymphatic Mapping for Early Stage Melanoma.
        Arch Surg. 1992; 127: 392-399
        • Giuliano A.E.
        The evolution of sentinel node biopsy for breast cancer: Personal experience.
        Breast J. 2020; 26: 17-21
        • Fisher B.
        • Montague E.
        • Redmond C.
        • et al.
        Findings from NSA BP∗ Protocol No. B-04-Comparison of Radical Mastectomy with Alternative Treatments for Primary Breast Cancer 1. Radiation Compliance and its Relation to Treatment Outcome.
        Cancer. 1980; 46: 1-13
        • Fisher E.R.
        • Anderson S.
        • Redmond C.
        • et al.
        Ipsilaterial breast tumor recurrence and survival following lumpectomy and irradiation: Pathological findings from NSABP protocol B-06.
        Semin Surg Oncol. 1992; 8: 161-166
        • Black D.M.
        • Mittendorf E.A.
        Landmark trials affecting the surgical management of invasive breast cancer.
        Surg Clin North Am. 2013; 93: 501-518
        • Krag D.N.
        • Anderson S.J.
        • Julian T.B.
        • 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: 881-888
        • Mansel R.E.
        • Fallowfield L.
        • Kissin M.
        • 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: 599-609
        • Veronesi U.
        • Paganelli G.
        • Viale G.
        • et al.
        Sentinel-lymph-node biopsy as a staging procedure in breast cancer: update of a randomised controlled study.
        Lancet Oncol. 2006; 7: 983-990
        • Ashikaga T.
        • Krag D.N.
        • Land S.R.
        • et al.
        Morbidity results from the NSABP B-32 trial comparing sentinel lymph node dissection versus axillary dissection.
        J Surg Oncol. 2010; 102: 111-118
        • Land S.R.
        • Kopec J.A.
        • Julian T.B.
        • et al.
        Patient-reported outcomes in sentinel node-negative adjuvant breast cancer patients receiving sentinel-node biopsy or axillary dissection: National Surgical Adjuvant Breast and Bowel Project phase III protocol B-32.
        J Clin Oncol. 2010; 28: 3929-3936
        • Fleissig A.
        • Fallowfield L.J.
        • Langridge C.I.
        • 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: 279-293
        • 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: 546-553
        • Krag D.N.
        • Anderson S.J.
        • Julian T.B.
        • 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: 927-933
        • 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: 595-600
        • Canavese G.
        • Catturich A.
        • Vecchio C.
        • et al.
        Sentinel node biopsy compared with complete axillary dissection for staging early breast cancer with clinically negative lymph nodes: results of randomized trial.
        Ann Oncol. 2009; 20: 1001-1007
        • Giuliano A.E.
        • Hawes D.
        • Ballman K.v.
        • et al.
        Association of occult metastases in sentinel lymph nodes and bone marrow with survival among women with early-stage invasive breast cancer.
        JAMA. 2011; 306: 385-393
        • Galimberti V.
        • Cole B.F.
        • 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: 1385-1393
        • Solá M.
        • Alberro J.A.
        • Fraile M.
        • et al.
        Complete axillary lymph node dissection versus clinical follow-up in breast cancer patients with sentinel node micrometastasis: final results from the multicenter clinical trial AATRM 048/13/2000.
        Ann Surg Oncol. 2013; 20: 120-127
        • Andersson Y.
        • Bergkvist L.
        • Frisell J.
        • et al.
        Omitting completion axillary lymph node dissection after detection of sentinel node micrometastases in breast cancer: first results from the prospective SENOMIC trial.
        Br J Surg. 2021; 108: 1105-1111
        • Giuliano A.E.
        • Hunt K.K.
        • Ballman K.v.
        • 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: 569-575
        • Giuliano A.E.
        • Ballman K.v.
        • 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 - J Am Med Assoc. 2017; 318: 918-926
        • Donker M.
        • van Tienhoven G.
        • Straver M.E.
        • 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: 1303-1310
        • Sávolt
        • 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: 672-679
        • Garcia-Etienne C.A.
        • Mansel R.E.
        • Tomatis M.
        • et al.
        Trends in axillary lymph node dissection for early-stage breast cancer in Europe: Impact of evidence on practice.
        Breast. 2019; 45: 89-96
        • Poodt I.G.M.
        • Spronk P.E.R.
        • Vugts G.
        • et al.
        Trends on Axillary Surgery in Nondistant Metastatic Breast Cancer Patients Treated Between 2011 and 2015: A Dutch Population-based Study in the ACOSOG-Z0011 and AMAROS Era.
        Ann Surg. 2018; 268: 1084-1090
        • Kantor O.
        • Chang C.
        • Yao K.
        • et al.
        Uptake of Breast Cancer Clinical Trials at Minority Serving Cancer Centers.
        Ann Surg Oncol. 2021; 28: 4995-5004
        • Yao K.
        • Liederbach E.
        • Pesce C.
        • et al.
        Impact of the American College of Surgeons Oncology Group Z0011 Randomized Trial on the Number of Axillary Nodes Removed for Patients with Early-Stage Breast Cancer.
        J Am Coll Surg. 2015; 221: 71-81
        • Jagsi R.
        • Chadha M.
        • Moni J.
        • et al.
        Radiation field design in the ACOSOG Z0011 (Alliance) Trial.
        J Clin Oncol. 2014; 32: 3600-3606
        • Cortina C.S.
        • Bergom C.
        • Craft M.A.
        • et al.
        A National Survey of Breast Surgeons and Radiation Oncologists on Contemporary Axillary Management in Mastectomy Patients.
        Ann Surg Oncol. 2021; 28: 5568-5579
        • de Boniface J.
        • Frisell J.
        • Andersson Y.
        • et al.
        Survival and axillary recurrence following sentinel node-positive breast cancer without completion axillary lymph node dissection: The randomized controlled SENOMAC trial.
        BMC Cancer. 2017; 17https://doi.org/10.1186/s12885-017-3361-y
        • Tinterri C.
        • Canavese G.
        • Bruzzi P.
        • et al.
        SINODAR ONE, an ongoing randomized clinical trial to assess the role of axillary surgery in breast cancer patients with one or two macrometastatic sentinel nodes.
        Breast. 2016; 30: 197-200
        • Goyal A.
        • Mann G.B.
        • Fallowfield L.
        • et al.
        POSNOC-POsitive Sentinel NOde: adjuvant therapy alone versus adjuvant therapy plus Clearance or axillary radiotherapy: a randomised controlled trial of axillary treatment in women with early-stage breast cancer who have metastases in one or two sentinel nodes.
        BMJ Open. 2021; 11https://doi.org/10.1136/BMJOPEN-2021-054365
        • Houvenaeghel G.
        • Cohen M.
        • Raro P.
        • et al.
        Sentinel node involvement with or without completion axillary lymph node dissection: treatment and pathologic results of randomized SERC trial.
        NPJ Breast Cancer. 2021; 7: 133
        • Hildebrandt G.
        • Stachs A.
        • Gerber B.
        • et al.
        Central Review of Radiation Therapy Planning Among Patients with Breast-Conserving Surgery: Results from a Quality Assurance Process Integrated into the INSEMA Trial.
        Int J Radiat Oncol Biol Phys. 2020; 107: 683-693
        • Tinterri C.
        • Marrazzo E.
        • Anghelone C.
        • et al.
        Abstract PD4-01: 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.
        Cancer Res. 2021; 81: PD4-01
        • Leidenius M.
        • Leivonen M.
        • Vironen J.
        • et al.
        The consequences of long-time arm morbidity in node-negative breast cancer patients with sentinel node biopsy or axillary clearance.
        J Surg Oncol. 2005; 92: 23-31
        • Martelli G.
        • Boracchi P.
        • Ardoino I.
        • et al.
        Axillary dissection versus no axillary dissection in older patients with T1N0 breast cancer: 15-year results of a randomized controlled trial.
        Ann Surg. 2012; 256: 920-924
        • Rudenstam C.M.
        • Zahrieh D.
        • Forbes J.F.
        • et al.
        Randomized trial comparing axillary clearance versus no axillary clearance in older patients with breast cancer: first results of International Breast Cancer Study Group Trial 10-93.
        J Clin Oncol. 2006; 24: 337-344
        • Hughes K.S.
        • Schnaper L.A.
        • Bellon J.R.
        • et al.
        Lumpectomy plus tamoxifen with or without irradiation in women age 70 years or older with early breast cancer: Long-term follow-up of CALGB 9343.
        J Clin Oncol. 2013; 31: 2382-2387
        • van Roozendaal L.M.
        • Vane M.L.G.
        • van Dalen T.
        • et al.
        Clinically node negative breast cancer patients undergoing breast conserving therapy, sentinel lymph node procedure versus follow-up: a Dutch randomized controlled multicentre trial (BOOG 2013-08).
        BMC Cancer. 2017; 17
      1. Sentinel Node Biopsy Vs Observation After Axillary PET - Full Text View - ClinicalTrials.gov.
        (Available at:) (Accessed May 9, 2022)
        • Gentilini O.
        • Botteri E.
        • Dadda P.
        • et al.
        Physical function of the upper limb after breast cancer surgery. Results from the SOUND (Sentinel node vs. Observation after axillary Ultra-souND) trial.
        Eur J Surg Oncol. 2016; 42: 685-689
        • Chang J.M.
        • Shin H.J.
        • Choi J.S.
        • et al.
        Imaging Protocol and Criteria for Evaluation of Axillary Lymph Nodes in the NAUTILUS Trial.
        J Breast Cancer. 2021; 24: 554-560
        • Aihara T.
        • Munakata S.
        • Morino H.
        • et al.
        Feasibility of sentinel node biopsy for breast cancer after neoadjuvant endocrine therapy: a pilot study.
        J Surg Oncol. 2004; 85: 77-81
        • Shirzadi A.
        • Mahmoodzadeh H.
        • Qorbani M.
        Assessment of sentinel lymph node biopsy after neoadjuvant chemotherapy for breast cancer in two subgroups: Initially node negative and node positive converted to node negative - A systemic review and meta-analysis.
        J Res Med Sci. 2019; 24: 18
        • Kantor O.
        • Wakeman M.
        • Weiss A.
        • et al.
        Axillary Management After Neoadjuvant Endocrine Therapy for Hormone Receptor-Positive Breast Cancer.
        Ann Surg Oncol. 2021; 28: 1358-1367
        • Un Park K.
        • Gregory M.
        • Bazan J.
        • et al.
        Neoadjuvant endocrine therapy use in early stage breast cancer during the covid-19 pandemic.
        . 2021; 188: 249-258
        • Whitehead I.
        • Irwin G.W.
        • Bannon F.
        • et al.
        The NeST (Neoadjuvant systemic therapy in breast cancer) study: National Practice Questionnaire of United Kingdom multi-disciplinary decision making.
        BMC Cancer. 2021; 21https://doi.org/10.1186/S12885-020-07757-6
        • Weiss A.
        • Wong S.
        • Golshan M.
        • et al.
        Patterns of Axillary Management in Stages 2 and 3 Hormone Receptor-Positive Breast Cancer by Initial Treatment Approach.
        Ann Surg Oncol. 2019; 26: 4326-4336
        • Pilewskie M.
        • Zabor E.C.
        • Mamtani A.
        • et al.
        The Optimal Treatment Plan to Avoid Axillary Lymph Node Dissection in Early-Stage Breast Cancer Patients Differs by Surgical Strategy and Tumor Subtype.
        Ann Surg Oncol. 2017; 24: 3527-3533
        • Kalinsky K.
        • Barlow W.E.
        • Gralow J.R.
        • et al.
        21-Gene Assay to Inform Chemotherapy Benefit in Node-Positive Breast Cancer.
        N Engl J Med. 2021; 385: 2336-2347
        • Bevilacqua J.L.B.
        • Kattan M.W.
        • Fey J.V.
        • et al.
        Doctor, What Are My Chances of Having a Positive Sentinel Node? A Validated Nomogram for Risk Estimation.
        J Clin Oncol. 2007; 25: 3670-3679
        • Martin C.
        • Cutuli B.
        • Velten M.
        Predictive model of axillary lymph node involvement in women with small invasive breast carcinoma: Axillary metastases in breast carcinoma.
        Cancer. 2002; 94: 314-322
        • Maibenco D.C.
        • Weiss L.K.
        • Pawlish K.S.
        • et al.
        Axillary lymph node metastases associated with small invasive breast carcinomas.
        Cancer. 1999; 85: 1530-1536
        • Schmid P.
        • Cortes J.
        • Dent R.
        • et al.
        Event-free Survival with Pembrolizumab in Early Triple-Negative Breast Cancer.
        N Engl J Med. 2022; 386: 556-567
        • Mittendorf E.A.
        • Zhang H.
        • Barrios C.H.
        • et al.
        Neoadjuvant atezolizumab in combination with sequential nab-paclitaxel and anthracycline-based chemotherapy versus placebo and chemotherapy in patients with early-stage triple-negative breast cancer (IMpassion031): a randomised, double-blind, phase 3 trial.
        Lancet. 2020; 396: 1090-1100
        • Geyer C.E.
        • Sikov W.M.
        • Huober J.
        • et al.
        Long-term efficacy and safety of addition of carboplatin with or without veliparib to standard neoadjuvant chemotherapy in triple-negative breast cancer: 4-year follow-up data from BrighTNess, a randomized phase III trial.
        Ann Oncol. 2022; 33: 384-394
        • von Minckwitz G.
        • Huang C.S.
        • Mano M.S.
        • et al.
        Trastuzumab Emtansine for Residual Invasive HER2-Positive Breast Cancer.
        N Engl J Med. 2019; 380: 617-628
        • Masuda N.
        • Lee S.J.
        • Ohtani S.
        • et al.
        Adjuvant Capecitabine for Breast Cancer after Preoperative Chemotherapy.
        N Engl J Med. 2017; 376: 2147-2159
        • Alvarez S.
        • Añorbe E.
        • Alcorta P.
        • et al.
        Role of sonography in the diagnosis of axillary lymph node metastases in breast cancer: a systematic review.
        AJR Am J Roentgenol. 2006; 186: 1342-1348
        • Houssami N.
        • Ciatto S.
        • Turner R.M.
        • et al.
        Preoperative ultrasound-guided needle biopsy of axillary nodes in invasive breast cancer: meta-analysis of its accuracy and utility in staging the axilla.
        Ann Surg. 2011; 254: 243-251
        • Tan V.K.M.
        • Goh B.K.P.
        • Fook-Chong S.
        • et al.
        The feasibility and accuracy of sentinel lymph node biopsy in clinically node-negative patients after neoadjuvant chemotherapy for breast cancer--a systematic review and meta-analysis.
        J Surg Oncol. 2011; 104: 97-103
        • 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: 343-352
        • Hunt K.K.
        • Yi M.
        • Mittendorf E.A.
        • 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: 558-564
        • van der Heiden-Van Der Loo M.
        • de Munck L.
        • Sonke G.S.
        • et al.
        Population based study on sentinel node biopsy before or after neoadjuvant chemotherapy in clinically node negative breast cancer patients: Identification rate and influence on axillary treatment.
        Eur J Cancer. 2015; 51: 915-921
        • Nogi H.
        • Uchida K.
        • Mimoto R.
        • et al.
        Long-Term Follow-Up of Node-Negative Breast Cancer Patients Evaluated via Sentinel Node Biopsy After Neoadjuvant Chemotherapy.
        Clin Breast Cancer. 2017; 17: 644-649
        • Kahler-Ribeiro-Fontana S.
        • Pagan E.
        • Magnoni F.
        • et al.
        Long-term standard sentinel node biopsy after neoadjuvant treatment in breast cancer: a single institution ten-year follow-up.
        Eur J Surg Oncol. 2021; 47: 804-812
        • Wong S.M.
        • Basik M.
        • Florianova L.
        • et al.
        Oncologic Safety of Sentinel Lymph Node Biopsy Alone After Neoadjuvant Chemotherapy for Breast Cancer.
        Ann Surg Oncol. 2021; 28: 2621-2629
        • Martelli G.
        • Miceli R.
        • Folli S.
        • et al.
        Sentinel node biopsy after primary chemotherapy in cT2 N0/1 breast cancer patients: Long-term results of a retrospective study.
        Eur J Surg Oncol. 2017; 43: 2012-2020
        • Wong S.M.
        • Almana N.
        • Choi J.
        • et al.
        Prognostic Significance of Residual Axillary Nodal Micrometastases and Isolated Tumor Cells After Neoadjuvant Chemotherapy for Breast Cancer.
        Ann Surg Oncol. 2019; 26: 3502-3509
        • Barron A.U.
        • Hoskin T.L.
        • Boughey J.C.
        Predicting Non-sentinel Lymph Node Metastases in Patients with a Positive Sentinel Lymph Node After Neoadjuvant Chemotherapy.
        Ann Surg Oncol. 2018; 25: 2867-2874
        • Leonardi M.C.
        • Arrobbio C.
        • Gandini S.
        • et al.
        Predictors of positive axillary non-sentinel lymph nodes in breast cancer patients with positive sentinel lymph node biopsy after neoadjuvant systemic therapy.
        Radiother Oncol. 2021; 163: 128-135
        • Zetterlund L.H.
        • Frisell J.
        • Zouzos A.
        • et al.
        Swedish prospective multicenter trial evaluating sentinel lymph node biopsy after neoadjuvant systemic therapy in clinically node-positive breast cancer.
        Breast Cancer Res Treat. 2017; 163: 103-110
        • Ryu J.M.
        • Lee S.K.
        • Kim J.Y.
        • et al.
        Predictive Factors for Nonsentinel Lymph Node Metastasis in Patients With Positive Sentinel Lymph Nodes After Neoadjuvant Chemotherapy: Nomogram for Predicting Nonsentinel Lymph Node Metastasis.
        Clin Breast Cancer. 2017; 17: 550-558
        • Boileau J.F.
        • Poirier B.
        • Basik M.
        • et al.
        Sentinel node biopsy after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: the SN FNAC study.
        J Clin Oncol. 2015; 33: 258-263
        • Jeruss J.S.
        • Newman L.A.
        • Ayers G.D.
        • et al.
        Factors predicting additional disease in the axilla in patients with positive sentinel lymph nodes after neoadjuvant chemotherapy.
        Cancer. 2008; 112: 2646-2654
        • Moo T.A.
        • Pawloski K.R.
        • Flynn J.
        • et al.
        Is Residual Nodal Disease at Axillary Dissection Associated with Tumor Subtype in Patients with Low Volume Sentinel Node Metastasis After Neoadjuvant Chemotherapy?.
        Ann Surg Oncol. 2021; 28: 6044-6050
        • Liedtke C.
        • Görlich D.
        • Bauerfeind I.
        • et al.
        Validation of a Nomogram Predicting Non-Sentinel Lymph Node Metastases among Patients with Breast Cancer after Primary Systemic Therapy - a transSENTINA Substudy.
        Breast Care (Basel). 2018; 13: 440-446
        • Moo T.A.
        • Edelweiss M.
        • Hajiyeva S.
        • et al.
        Is Low-Volume Disease in the Sentinel Node After Neoadjuvant Chemotherapy an Indication for Axillary Dissection?.
        Ann Surg Oncol. 2018; 25: 1488-1494
        • Barron A.U.
        • Hoskin T.L.
        • Day C.N.
        • et al.
        Association of Low Nodal Positivity Rate Among Patients With ERBB2-Positive or Triple-Negative Breast Cancer and Breast Pathologic Complete Response to Neoadjuvant Chemotherapy.
        JAMA Surg. 2018; 153: 1120-1126
        • Weiss A.
        • Campbell J.
        • Ballman K.v.
        • et al.
        Factors Associated with Nodal Pathologic Complete Response Among Breast Cancer Patients Treated with Neoadjuvant Chemotherapy: Results of CALGB 40601 (HER2+) and 40603 (Triple-Negative) (Alliance).
        Ann Surg Oncol. 2021; 28: 5960-5971
        • Scheel J.R.
        • Kim E.
        • Partridge S.C.
        • et al.
        MRI, Clinical Examination, and Mammography for Preoperative Assessment of Residual Disease and Pathologic Complete Response After Neoadjuvant Chemotherapy for Breast Cancer: ACRIN 6657 Trial.
        AJR Am J Roentgenol. 2018; 210: 1376-1385
        • de Los Santos J.F.
        • Cantor A.
        • Amos K.D.
        • et al.
        Magnetic resonance imaging as a predictor of pathologic response in patients treated with neoadjuvant systemic treatment for operable breast cancer. Translational Breast Cancer Research Consortium trial 017.
        Cancer. 2013; 119: 1776-1783
        • Tasoulis M.K.
        • Lee H.B.
        • Yang W.
        • et al.
        Accuracy of Post-Neoadjuvant Chemotherapy Image-Guided Breast Biopsy to Predict Residual Cancer.
        JAMA Surg. 2020; 155
        • van Loevezijn A.A.
        • van der Noordaa M.E.M.
        • van Werkhoven E.D.
        • et al.
        Minimally Invasive Complete Response Assessment of the Breast After Neoadjuvant Systemic Therapy for Early Breast Cancer (MICRA trial): Interim Analysis of a Multicenter Observational Cohort Study.
        Ann Surg Oncol. 2021; 28: 3243-3253
        • van der Noordaa M.E.M.
        • van Duijnhoven F.H.
        • Cuijpers F.N.E.
        • et al.
        Toward omitting sentinel lymph node biopsy after neoadjuvant chemotherapy in patients with clinically node-negative breast cancer.
        Br J Surg. 2021; 108: 667-674
        • National Institute of Health, U.S
        National Library of Medicine ClinicalTrials.gov. Omission of SLNB in Triple-negative and HER2-positive Breast Cancer Patients With rCR and pCR in the Breast After NAST.
        (Available at:) (Accessed May 7, 2022)
        • National Institute of Health, U.S. National Library of Medicine ClinicalTrials.gov
        Avoiding Sentinel Lymph Node Biopsy in Breast Cancer Patients After Neoadjuvant Chemotherapy.
        (Available at:) (Accessed May 7, 2022)
        • Sparano J.A.
        • Gray R.J.
        • Makower D.F.
        • et al.
        Adjuvant Chemotherapy Guided by a 21-Gene Expression Assay in Breast Cancer.
        N Engl J Med. 2018; 379: 111-121
        • Pilewskie M.
        • Mautner S.K.
        • Stempel M.
        • et al.
        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: 1123-1128
        • Harris C.K.
        • Tran H.T.
        • 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: 3004-3010
        • Lim G.H.
        • Upadhyaya V.S.
        • Acosta H.A.
        • et al.
        Preoperative predictors of high and low axillary nodal burden in Z0011 eligible breast cancer patients with a positive lymph node needle biopsy result.
        Eur J Surg Oncol. 2018; 44: 945-950
        • Wang X.
        • Chen L.
        • Sun Y.
        • et al.
        Evaluation of axillary lymph node metastasis burden by preoperative ultrasound in early-stage breast cancer with needle biopsy-proven metastasis.
        Clin Transl Oncol. 2020; 22: 468-473
        • Yoo T.K.
        • Kang B.J.
        • Kim S.H.
        • et al.
        Axillary lymph node dissection is not obligatory in breast cancer patients with biopsy-proven axillary lymph node metastasis.
        Breast Cancer Res Treat. 2020; 181: 403-409
        • Rashmi Kumar N.
        • Burns J.
        • Abraham J.
        • et al.
        NCCN Guidelines Version 3.2022 Breast Cancer.
        (Available at:) (Accessed May 30, 2022)
        • Brackstone M.
        • Baldassarre F.G.
        • Perera F.E.
        • et al.
        Management of the Axilla in Early-Stage Breast Cancer: Ontario Health (Cancer Care Ontario) and ASCO Guideline.
        J Clin Oncol. 2021; 39: 3056-3082
        • Weber W.P.
        • Matrai Z.
        • Hayoz S.
        • et al.
        Tailored axillary surgery in patients with clinically node-positive breast cancer: Pre-planned feasibility substudy of TAXIS (OPBC-03, SAKK 23/16, IBCSG 57-18, ABCSG-53, GBG 101).
        Breast. 2021; 60: 98-110
        • Schipper R.J.
        • de Bruijn A.
        • Voogd A.C.
        • et al.
        Rate and predictors of nodal pathological complete response following neoadjuvant endocrine treatment in clinically biopsy-proven node-positive breast cancer patients.
        Eur J Surg Oncol. 2021; 47: 1928-1933
        • Murphy B.M.
        • Hoskin T.L.
        • Degnim A.C.
        • et al.
        Surgical management of axilla following neoadjuvant endocrine therapy.
        Ann Surg Ancol. 2021; https://doi.org/10.1245/s10434
        • Friedman-Eldar O.
        • Ozmen T.
        • el Haddi S.J.
        • et al.
        Axillary Response to Neoadjuvant Therapy in Node-Positive, Estrogen Receptor-Positive, Human Epidermal Growth Factor Receptor 2-Negative Breast Cancer Patients: Predictors and Oncologic Outcomes.
        Ann Surg Oncol. 2022; https://doi.org/10.1245/S10434-022-11473-9
        • Kantor O.
        • Wong S.
        • Weiss A.
        • et al.
        Prognostic significance of residual nodal disease after neoadjuvant endocrine therapy for hormone receptor-positive breast cancer.
        NPJ Breast Cancer. 2020; 6https://doi.org/10.1038/S41523-020-00177-6
        • Samiei S.
        • Simons J.M.
        • Engelen S.M.E.
        • et al.
        Axillary Pathologic Complete Response After Neoadjuvant Systemic Therapy by Breast Cancer Subtype in Patients With Initially Clinically Node-Positive Disease: A Systematic Review and Meta-analysis.
        JAMA Surg. 2021; 156https://doi.org/10.1001/JAMASURG.2021.0891
        • Boughey J.C.
        • Suman V.J.
        • Mittendorf E.A.
        • 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: 1455-1461
        • 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: 609-618
        • Boughey J.C.
        • Ballman K.v.
        • Le-Petross H.T.
        • et al.
        Identification and Resection of Clipped Node Decreases the False-negative Rate of Sentinel Lymph Node Surgery in Patients Presenting With Node-positive Breast Cancer (T0-T4, N1-N2) Who Receive Neoadjuvant Chemotherapy: Results From ACOSOG Z1071 (Alliance).
        Ann Surg. 2016; 263: 802-807
        • Donker M.
        • Straver M.E.
        • Wesseling J.
        • et al.
        Marking axillary lymph nodes with radioactive iodine seeds for axillary staging after neoadjuvant systemic treatment in breast cancer patients: the MARI procedure.
        Ann Surg. 2015; 261: 378-382
        • Gallagher K.K.
        • Iles K.
        • Kuzmiak C.
        • et al.
        Prospective Evaluation of Radar-Localized Reflector-Directed Targeted Axillary Dissection in Node-Positive Breast Cancer Patients after Neoadjuvant Systemic Therapy.
        J Am Coll Surg. 2022; 234: 538-545
        • Caudle A.S.
        • Yang W.T.
        • Krishnamurthy S.
        • et al.
        Improved Axillary Evaluation Following Neoadjuvant Therapy for Patients With Node-Positive Breast Cancer Using Selective Evaluation of Clipped Nodes: Implementation of Targeted Axillary Dissection.
        J Clin Oncol. 2016; 34: 1072-1078
        • van Nijnatten T.J.A.
        • Simons J.M.
        • Smidt M.L.
        • et al.
        A Novel Less-invasive Approach for Axillary Staging After Neoadjuvant Chemotherapy in Patients With Axillary Node-positive Breast Cancer by Combining Radioactive Iodine Seed Localization in the Axilla With the Sentinel Node Procedure (RISAS): A Dutch Prospective Multicenter Validation Study.
        Clin Breast Cancer. 2017; 17: 399-402
        • Simons J.
        • JA v Nijnatten T.
        • Koppert L.B.
        • et al.
        Abstract GS1-10: Radioactive Iodine Seed placement in the Axilla with Sentinel lymph node biopsy after neoadjuvant chemotherapy in breast cancer: Results of the prospective multicenter RISAS trial.
        Cancer Res. 2021; 81: GS1-GS10
        • Banys-Paluchowski M.
        • Gruber I.V.
        • Hartkopf A.
        • et al.
        Axillary ultrasound for prediction of response to neoadjuvant therapy in the context of surgical strategies to axillary dissection in primary breast cancer: a systematic review of the current literature.
        Arch Gynecol Obstet. 2020; 301: 341-353
        • Patel R.
        • MacKerricher W.
        • Tsai J.
        • et al.
        Pretreatment Tattoo Marking of Suspicious Axillary Lymph Nodes: Reliability and Correlation with Sentinel Lymph Node.
        Ann Surg Oncol. 2019; 26: 2452-2458
        • de Boniface J.
        • Frisell J.
        • Kühn T.
        • et al.
        False-negative rate in the extended prospective TATTOO trial evaluating targeted axillary dissection by carbon tattooing in clinically node-positive breast cancer patients receiving neoadjuvant systemic therapy.
        Breast Cancer Res Treat. 2022; https://doi.org/10.1007/S10549-022-06588-2
        • Allweis T.M.
        • Menes T.
        • Rotbart N.
        • et al.
        Ultrasound guided tattooing of axillary lymph nodes in breast cancer patients prior to neoadjuvant therapy, and identification of tattooed nodes at the time of surgery.
        Eur J Surg Oncol. 2020; 46: 1041-1045
        • Plecha D.
        • Bai S.
        • Patterson H.
        • et al.
        Improving the Accuracy of Axillary Lymph Node Surgery in Breast Cancer with Ultrasound-Guided Wire Localization of Biopsy Proven Metastatic Lymph Nodes.
        Ann Surg Oncol. 2015; 22: 4241-4246
        • Kuemmel S.
        • Heil J.
        • Rueland A.
        • et al.
        A Prospective, Multicenter Registry Study to Evaluate the Clinical Feasibility of Targeted Axillary Dissection (TAD) in Node-Positive Breast Cancer Patients.
        Ann Surg. 2020;
        • Wu S.
        • Wang Y.
        • Zhang N.
        • et al.
        Intraoperative Touch Imprint Cytology in Targeted Axillary Dissection After Neoadjuvant Chemotherapy for Breast Cancer Patients with Initial Axillary Metastasis.
        Ann Surg Oncol. 2018; 25: 3150-3157
        • Sun J.
        • Henry D.A.
        • Carr M.J.
        • et al.
        Feasibility of Axillary Lymph Node Localization and Excision Using Radar Reflector Localization.
        Clin Breast Cancer. 2021; 21: e189-e193
        • Greenwood H.I.
        • Wong J.M.
        • Mukhtar R.A.
        • et al.
        Feasibility of Magnetic Seeds for Preoperative Localization of Axillary Lymph Nodes in Breast Cancer Treatment.
        AJR Am J Roentgenol. 2019; 213: 953-957
        • Simons J.M.
        • Scoggins M.E.
        • Kuerer H.M.
        • et al.
        Prospective Registry Trial Assessing the Use of Magnetic Seeds to Locate Clipped Nodes After Neoadjuvant Chemotherapy for Breast Cancer Patients.
        Ann Surg Oncol. 2021; 28: 4277-4283
        • Laws A.
        • Dillon K.
        • Kelly B.N.
        • et al.
        Node-Positive Patients Treated with Neoadjuvant Chemotherapy Can Be Spared Axillary Lymph Node Dissection with Wireless Non-Radioactive Localizers.
        Ann Surg Oncol. 2020; 27: 4819-4827
        • Pinto C.S.
        • Peleteiro B.
        • Pinto C.A.
        • et al.
        Initial experience with targeted axillary dissection after neoadjuvant therapy in breast cancer patients.
        Breast Cancer. 2022; https://doi.org/10.1007/S12282-022-01349-X
        • Siso C.
        • de Torres J.
        • Esgueva-Colmenarejo A.
        • et al.
        Intraoperative Ultrasound-Guided Excision of Axillary Clip in Patients with Node-Positive Breast Cancer Treated with Neoadjuvant Therapy (ILINA Trial) : A New Tool to Guide the Excision of the Clipped Node After Neoadjuvant Treatment.
        Ann Surg Oncol. 2018; 25: 784-791
        • Barrio A.v.
        • Montagna G.
        • Mamtani A.
        • et al.
        Nodal Recurrence in Patients With Node-Positive Breast Cancer Treated With Sentinel Node Biopsy Alone After Neoadjuvant Chemotherapy-A Rare Event.
        JAMA Oncol. 2021; 7: 1851-1855
        • Piltin M.A.
        • Hoskin T.L.
        • Day C.N.
        • et al.
        Oncologic Outcomes of Sentinel Lymph Node Surgery After Neoadjuvant Chemotherapy for Node-Positive Breast Cancer.
        Ann Surg Oncol. 2020; 27: 4795-4801
        • Choi H.J.
        • Kim I.
        • Alsharif E.
        • et al.
        Use of Sentinel Lymph Node Biopsy after Neoadjuvant Chemotherapy in Patients with Axillary Node-Positive Breast Cancer in Diagnosis.
        J Breast Cancer. 2018; 21: 433-441
        • Kang Y.J.
        • Han W.
        • Park S.
        • et al.
        Outcome following sentinel lymph node biopsy-guided decisions in breast cancer patients with conversion from positive to negative axillary lymph nodes after neoadjuvant chemotherapy.
        Breast Cancer Res Treat. 2017; 166: 473-480
        • Kim H.
        • Han J.
        • Kim S.Y.
        • et al.
        Sentinel Lymph Node Biopsy in Breast Cancer Patients With Pathological Complete Response in the Axillary Lymph Node After Neoadjuvant Chemotherapy.
        J Breast Cancer. 2021; 24: 531-541
        • Cabıoğlu N.
        • Karanlık H.
        • Yıldırım N.
        • et al.
        Favorable outcome with sentinel lymph node biopsy alone after neoadjuvant chemotherapy in clinically node positive breast cancer at diagnosis: Turkish Multicentric NEOSENTI-TURK MF-18-02-study.
        Eur J Surg Oncol. 2021; 47: 2506-2514
        • van Loevezijn A.A.
        • van der Noordaa M.E.M.
        • Stokkel M.P.M.
        • et al.
        Three-year follow-up of de-escalated axillary treatment after neoadjuvant systemic therapy in clinically node-positive breast cancer: the MARI-protocol.
        Breast Cancer Res Treat. 2022; 193: 37-48
        • Banys-paluchowski M.
        • Gasparri M.L.
        • de Boniface J.
        • et al.
        Surgical Management of the Axilla in Clinically Node-Positive Breast Cancer Patients Converting to Clinical Node Negativity through Neoadjuvant Chemotherapy: Current Status, Knowledge Gaps, and Rationale for the EUBREAST-03 AXSANA Study.
        Cancers (Basel). 2021; 13https://doi.org/10.3390/CANCERS13071565
        • de Wild S.R.
        • Simons J.M.
        • Vrancken Peeters M.J.T.F.D.
        • et al.
        MINImal vs. MAXimal Invasive Axillary Staging and Treatment After Neoadjuvant Systemic Therapy in Node Positive Breast Cancer: Protocol of a Dutch Multicenter Registry Study (MINIMAX).
        Clin Breast Cancer. 2022; 22: e59-e64
        • National Institute of Health, U.S. National Library of Medicine ClinicalTrials.gov
        Comparison of Axillary Lymph Node Dissection With Axillary Radiation for Patients With Node-Positive Breast Cancer Treated With Chemotherapy.
        (Available at:) (Accessed May 14, 2022)
        • Tinterri C.
        • Canavese G.
        • Bruzzi P.
        • et al.
        NEONOD 2: Rationale and design of a multicenter non-inferiority trial to assess the effect of axillary surgery omission on the outcome of breast cancer patients presenting only micrometastasis in the sentinel lymph node after neoadjuvant chemotherapy.
        Contemp Clin Trials Commun. 2019; 17https://doi.org/10.1016/J.CONCTC.2019.100496
        • National Institute of Health, U.S. National Library of Medicine ClinicalTrials.gov
        Axillary Lymph Node Dissection vs Axillary Radiotherapy in Positive Sentinel Node After Neoadjuvant Therapy (ADARNAT).
        (Available at:) (Accessed May 14, 2022)