Targeted Axillary Dissection: A Review Covering Technical Aspects, Current Recommendations and the Future
Main Article Content
Abstract
For clinically node positive patients with breast cancer, traditionally the gold standard for management of the axilla has been axillary lymph node dissection. This however has been associated with a high rate of morbidity including lymphoedema and shoulder stiffness. With the introduction of neo-adjuvant systemic therapy many patients undergo pathological complete response within the breast and axilla, particularly in certain molecular subtypes of breast cancer propelling interest in de-escalation surgery to reduce this morbidity.
Targeted axillary dissection is a procedure combining targeted lymph node biopsy, removing a previously marked node with confirmed cancer prior to neo-adjuvant systemic therapy and sentinel lymph node biopsy. The aim of the procedure is to accurately re-stage the axilla in patients with known nodal metastases after systemic therapy and reduce the morbidity associated with axillary dissection. Current meta-analyses have demonstrated that performing targeted axillary clearance has a consistently lower false negative rate when re-staging the axilla compared to sentinel or targeted node biopsy alone. This has led to a huge increase in popularity for the procedure. However, long-term data for oncological outcomes and morbidity are still lacking.
This review article aims to provides an overview of targeted axillary dissection. Focusing on technical aspects, including clip selection, number of clipped nodes and localization techniques for identifying the clipped node prior to surgery. The improved false negative rates of targeted lymph node dissection compared to sentinel node biopsy in clinically node positive patients converting to clinically node negative patients after neo-adjuvant systemic therapy. Pathological and radiological factors that may help in predicting nodal response to neo-adjuvant systemic therapy. Current guidelines/ recommendations for patient selection and management of residual disease within the axilla based on limited data and future studies aiming to clarify treatment decisions for this group of patients.
Article Details
How to Cite
AA, Winder; K, Swift; A, Miu.
Targeted Axillary Dissection: A Review Covering Technical Aspects, Current Recommendations and the Future.
Medical Research Archives, [S.l.], v. 11, n. 5, may 2023.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/3892>. Date accessed: 26 apr. 2024.
doi: https://doi.org/10.18103/mra.v11i5.3892.
Section
Review Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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2. Kim T, Giuliano AE, Lyman GH. Lymphatic mapping and sentinel lymph node biopsy in early-stage breast carcinoma: a meta-analysis. Cancer. 2006 Jan 1;106(1):4-16. doi: 10.1002/cncr.21568. PMID: 16329134
3. 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 Nov;15(12):1303-10. doi: 10.1016/S1470-2045(14)70460-7
4. 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(14):1455–1461. doi:10.1001/jama.2013.278932
5. 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 Jun;14(7):609-18. doi: 10.1016/S1470-2045(13)70166-9
6. 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. 2022 Nov 1;276(5):e553-e562. doi: 10.1097/SLA.0000000000004572
7. 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 Mar;25(3):784-791. doi: 10.1245/s10434-017-6270-z
8. Hyde B, Geske J, Lee C. Challenges to I-125 Seed Localization of Metastatic Axillary Lymph Nodes Following Neoadjuvant Chemotherapy, Journal of Breast Imaging, 2019;1(3):223–229. https://doi.org/10.1093/jbi/wbz032
9. Gurleyik G, Aksu SA, Aker F, Tekyol KK, Tanrikulu E, Gurleyik E. Targeted axillary biopsy and sentinel lymph node biopsy for axillary restaging after neoadjuvant chemotherapy. Ann Surg Treat Res. 2021 Jun;100(6):305-312. doi: 10.4174/astr.2021.100.6.305
10. Balasubramanian R, Morgan C, Shaari E, et al. Wire guided localisation for targeted axillary node dissection is accurate in axillary staging in node positive breast cancer following neoadjuvant chemotherapy. Eur J Surg Oncol. 2020 Jun;46(6):1028-1033. doi: 10.1016/j.ejso.2019.12.007
11. García-Novoa A, Acea-Nebril B, Díaz Carballada C, et al. Combining Wire Localization of Clipped Nodes with Sentinel Lymph Node Biopsy After Neoadjuvant Chemotherapy in Node-Positive Breast Cancer: Preliminary Results from a Prospective Study. Ann Surg Oncol. 2021 Feb;28(2):958-967. doi: 10.1245/s10434-020-08925-5
12. Hartmann S, Reimer T, Gerber B, Stubert J, Stengel B, Stachs A. Wire localization of clip-marked axillary lymph nodes in breast cancer patients treated with primary systemic therapy. Eur J Surg Oncol. 2018 Sep;44(9):1307-1311. doi: 10.1016/j.ejso.2018.05.035
13. Goyal A, Puri S, Marshall A, et al. A multicentre prospective feasibility study of carbon dye tattooing of biopsied axillary node and surgical localisation in breast cancer patients. Breast Cancer Res Treat. 2021 Jan;185(2):433-440. doi: 10.1007/s10549-020-05961-3
14. 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 Aug;26(8):2452-2458. doi: 10.1245/s10434-019-07419-3
15. Hartmann S, Kühn T, de Boniface J, et al. Carbon tattooing for targeted lymph node biopsy after primary systemic therapy in breast cancer: prospective multicentre TATTOO trial. Br J Surg. 2021 Apr 5;108(3):302-307. doi: 10.1093/bjs/znaa083
16. 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 Jun;193(3):589-595. doi: 10.1007/s10549-022-06588-2
17. Straver ME, Loo CE, Alderliesten T, Rutgers EJ, Vrancken Peeters MT. Marking the axilla with radioactive iodine seeds (MARI procedure) may reduce the need for axillary dissection after neoadjuvant chemotherapy for breast cancer. Br J Surg. 2010 Aug;97(8):1226-31. doi: 10.1002/bjs.7073
18. van Nijnatten TJA, Simons JM, Smidt ML, 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 Aug;17(5):399-402. doi: 10.1016/j.clbc.2017.04.006
19. F, Forsthuber E, Sir A. The applicability of Magseed® for targeted axillary dissection in breast cancer patients treated with neoadjuvant chemotherapy. Breast. 2021 Jun;57:113-117. doi: 10.1016/j.breast.2021.03.008
20. Greenwood HI, Wong JM, Mukhtar RA, Alvarado MD, Price ER. Feasibility of Magnetic Seeds for Preoperative Localization of Axillary Lymph Nodes in Breast Cancer Treatment. AJR Am J Roentgenol. 2019 Oct;213(4):953-957. doi: 10.2214/AJR.19.21378
21. Simons JM, Scoggins ME, Kuerer HM, 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 Aug;28(8):4277-4283. doi: 10.1245/s10434-020-09542-y
22. Gallagher KK, Iles K, Kuzmiak C, Louie R, McGuire KP, Ollila DW. 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 Apr 1;234(4):538-545. doi: 10.1097/XCS.0000000000000098
23. Winder AA, Spillane AJ, Sood S, McKessar M, Cohn D, Snook K. Radio-isotope occult lesion localization (ROLL) techniques to identify the clipped node for targeted axillary dissection (TAD) in breast cancer. ANZ J Surg. 2022 Nov;92(11):3017-3021. doi: 10.1111/ans.18079
24. Lim GH, Gudi M, Teo SY, et al. Would Removal of All Ultrasound Abnormal Metastatic Lymph Nodes Without Sentinel Lymph Node Biopsy Be Accurate in Patients with Breast Cancer with Neoadjuvant Chemotherapy? Oncologist. 2020 Nov;25(11):e1621-e1627. doi: 10.1634/theoncologist.2020-0494
25. Hartmann S, Stachs A, Schultek G, Gerber B, Reimer T. The Clinical Relevance of Target Lymph Node Biopsy after Primary Systemic Therapy in Initially Node-Positive Breast Cancer Patients. Cancers (Basel). 2021;13(11):2620.
26. van der Noordaa MEM, van Duijnhoven FH, Straver ME, et al. Major Reduction in Axillary Lymph Node Dissections After Neoadjuvant Systemic Therapy for Node-Positive Breast Cancer by combining PET/CT and the MARI Procedure. Ann Surg Oncol. 2018 25(6): 1512-1520.
27. Gasparri ML, de Boniface J, Poortmans P, et al. Axillary surgery after neoadjuvant therapy in initially node-positive breast cancer: international EUBREAST survey. Br J Surg. 2022;109(9):857-863.
28. Samiei S, Simons JM, Engelen SME, 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;156(6):e210891.
29. ELAMIN, G., SAPRE, D., TEHNIYAT, W., JAHAN, A., DAKKA, M.. Pathological complete response in the axillary lymph nodes post neo-adjuvant chemotherapy in breast cancer, is it predictable?. Annals of Breast Surgery, North America. 2019 Aug;3. Available at:
30. Kim R, Chang JM, Lee HB, et al. Predicting Axillary Response to Neoadjuvant Chemotherapy: Breast MRI and US in Patients with Node-Positive Breast Cancer. Radiology. 2019;293(1):49-57.
31. Corsi F, Albasini S, Sorrentino L, et al. Development of a novel nomogram-based online tool to predict axillary status after neoadjuvant chemotherapy in cN+ breast cancer: A multicentre study on 1,950 patients. Breast. 2021;60:131-137.
32. Reig B, Lewin AA, Du L, et al. Breast MRI for Evaluation of Response to Neoadjuvant Therapy. Radiographics. 2021;41(3):665-679.
33. Moo TA, Jochelson MS, Zabor EC, et al. Is Clinical Exam of the Axilla Sufficient to Select Node-Positive Patients Who Downstage After NAC for SLNB? A Comparison of the Accuracy of Clinical Exam Versus MRI. Ann Surg Oncol. 2019;26(13):4238–4243.
34. Turan U, Aygun M, Duman BB, et al. Efficacy of US, MRI, and F-18 FDG-PET/CT for Detecting Axillary Lymph Node Metastasis after Neoadjuvant Chemotherapy in Breast Cancer Patients. Diagnostics (Basel). 2021;11(12):2361.
35. Pesek S, Ashikaga T, Krag LE, Krag D. The false-negative rate of sentinel node biopsy in patients with breast cancer: a meta-analysis. World J Surg. 2012;36(9):2239-2251. doi:10.1007/s00268-012-1623-z
36. Simons JM, van Nijnatten TJA, van der Pol CC, Luiten EJT, Koppert LB, Smidt ML. Diagnostic Accuracy of Different Surgical Procedures for Axillary Staging After Neoadjuvant Systemic Therapy in Node-positive Breast Cancer: A Systematic Review and Meta-analysis. Ann Surg. 2019;269(3):432-442. doi:10.1097/SLA.0000000000003075
37. Swarnkar PK, Tayeh S, Michell MJ, Mokbel K. The Evolving Role of Marked Lymph Node Biopsy (MLNB) and Targeted Axillary Dissection (TAD) after Neoadjuvant Chemotherapy (NACT) for Node-Positive Breast Cancer: Systematic Review and Pooled Analysis. Cancers (Basel). 2021;13(7):1539.
38. Caudle AS, Yang WT, 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(10):1072-1078.
39. 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(4):804-812.
40. Friedrich M, Kühn T, Janni W, et al. AGO Recommendations for the Surgical Therapy of the Axilla After Neoadjuvant Chemotherapy: 2021 Update [published correction appears in Geburtshilfe Frauenheilkd. 2021 Oct 22;81(10):e31]. Geburtshilfe Frauenheilkd. 2021;81(10):1112-1120. doi:10.1055/a-1499-8431
41. Cardoso F, Kyriakides S, Ohno S, et al. Early breast cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2019;30(8):1194-1220.
42. Nikyar N, Tegnelius E, Valachis A. Adjuvant locoregional radiation therapy in breast cancer patients with pathologic complete response after neoadjuvant chemotherapy: A systematic review and meta-analysis. Clin Transl Radiat Oncol. 2022;33:45-52. Published 2022 Jan 5. doi:10.1016/j.ctro.2021.12.010
43. Banys-Paluchowski M, Thill M, Kühn T, et al. AGO Recommendations for the Surgical Therapy of Breast Cancer: Update 2022. Geburtshilfe Frauenheilkd. 2022;82(10):1031-1043. doi:10.1055/a-1904-6231
44. Tinterri C, Canavese G, Bruzzi P, Dozin B. 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;17:100496. Published 2019 Nov 23. doi:10.1016/j.conctc.2019.100496
2. Kim T, Giuliano AE, Lyman GH. Lymphatic mapping and sentinel lymph node biopsy in early-stage breast carcinoma: a meta-analysis. Cancer. 2006 Jan 1;106(1):4-16. doi: 10.1002/cncr.21568. PMID: 16329134
3. 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 Nov;15(12):1303-10. doi: 10.1016/S1470-2045(14)70460-7
4. 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(14):1455–1461. doi:10.1001/jama.2013.278932
5. 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 Jun;14(7):609-18. doi: 10.1016/S1470-2045(13)70166-9
6. 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. 2022 Nov 1;276(5):e553-e562. doi: 10.1097/SLA.0000000000004572
7. 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 Mar;25(3):784-791. doi: 10.1245/s10434-017-6270-z
8. Hyde B, Geske J, Lee C. Challenges to I-125 Seed Localization of Metastatic Axillary Lymph Nodes Following Neoadjuvant Chemotherapy, Journal of Breast Imaging, 2019;1(3):223–229. https://doi.org/10.1093/jbi/wbz032
9. Gurleyik G, Aksu SA, Aker F, Tekyol KK, Tanrikulu E, Gurleyik E. Targeted axillary biopsy and sentinel lymph node biopsy for axillary restaging after neoadjuvant chemotherapy. Ann Surg Treat Res. 2021 Jun;100(6):305-312. doi: 10.4174/astr.2021.100.6.305
10. Balasubramanian R, Morgan C, Shaari E, et al. Wire guided localisation for targeted axillary node dissection is accurate in axillary staging in node positive breast cancer following neoadjuvant chemotherapy. Eur J Surg Oncol. 2020 Jun;46(6):1028-1033. doi: 10.1016/j.ejso.2019.12.007
11. García-Novoa A, Acea-Nebril B, Díaz Carballada C, et al. Combining Wire Localization of Clipped Nodes with Sentinel Lymph Node Biopsy After Neoadjuvant Chemotherapy in Node-Positive Breast Cancer: Preliminary Results from a Prospective Study. Ann Surg Oncol. 2021 Feb;28(2):958-967. doi: 10.1245/s10434-020-08925-5
12. Hartmann S, Reimer T, Gerber B, Stubert J, Stengel B, Stachs A. Wire localization of clip-marked axillary lymph nodes in breast cancer patients treated with primary systemic therapy. Eur J Surg Oncol. 2018 Sep;44(9):1307-1311. doi: 10.1016/j.ejso.2018.05.035
13. Goyal A, Puri S, Marshall A, et al. A multicentre prospective feasibility study of carbon dye tattooing of biopsied axillary node and surgical localisation in breast cancer patients. Breast Cancer Res Treat. 2021 Jan;185(2):433-440. doi: 10.1007/s10549-020-05961-3
14. 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 Aug;26(8):2452-2458. doi: 10.1245/s10434-019-07419-3
15. Hartmann S, Kühn T, de Boniface J, et al. Carbon tattooing for targeted lymph node biopsy after primary systemic therapy in breast cancer: prospective multicentre TATTOO trial. Br J Surg. 2021 Apr 5;108(3):302-307. doi: 10.1093/bjs/znaa083
16. 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 Jun;193(3):589-595. doi: 10.1007/s10549-022-06588-2
17. Straver ME, Loo CE, Alderliesten T, Rutgers EJ, Vrancken Peeters MT. Marking the axilla with radioactive iodine seeds (MARI procedure) may reduce the need for axillary dissection after neoadjuvant chemotherapy for breast cancer. Br J Surg. 2010 Aug;97(8):1226-31. doi: 10.1002/bjs.7073
18. van Nijnatten TJA, Simons JM, Smidt ML, 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 Aug;17(5):399-402. doi: 10.1016/j.clbc.2017.04.006
19. F, Forsthuber E, Sir A. The applicability of Magseed® for targeted axillary dissection in breast cancer patients treated with neoadjuvant chemotherapy. Breast. 2021 Jun;57:113-117. doi: 10.1016/j.breast.2021.03.008
20. Greenwood HI, Wong JM, Mukhtar RA, Alvarado MD, Price ER. Feasibility of Magnetic Seeds for Preoperative Localization of Axillary Lymph Nodes in Breast Cancer Treatment. AJR Am J Roentgenol. 2019 Oct;213(4):953-957. doi: 10.2214/AJR.19.21378
21. Simons JM, Scoggins ME, Kuerer HM, 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 Aug;28(8):4277-4283. doi: 10.1245/s10434-020-09542-y
22. Gallagher KK, Iles K, Kuzmiak C, Louie R, McGuire KP, Ollila DW. 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 Apr 1;234(4):538-545. doi: 10.1097/XCS.0000000000000098
23. Winder AA, Spillane AJ, Sood S, McKessar M, Cohn D, Snook K. Radio-isotope occult lesion localization (ROLL) techniques to identify the clipped node for targeted axillary dissection (TAD) in breast cancer. ANZ J Surg. 2022 Nov;92(11):3017-3021. doi: 10.1111/ans.18079
24. Lim GH, Gudi M, Teo SY, et al. Would Removal of All Ultrasound Abnormal Metastatic Lymph Nodes Without Sentinel Lymph Node Biopsy Be Accurate in Patients with Breast Cancer with Neoadjuvant Chemotherapy? Oncologist. 2020 Nov;25(11):e1621-e1627. doi: 10.1634/theoncologist.2020-0494
25. Hartmann S, Stachs A, Schultek G, Gerber B, Reimer T. The Clinical Relevance of Target Lymph Node Biopsy after Primary Systemic Therapy in Initially Node-Positive Breast Cancer Patients. Cancers (Basel). 2021;13(11):2620.
26. van der Noordaa MEM, van Duijnhoven FH, Straver ME, et al. Major Reduction in Axillary Lymph Node Dissections After Neoadjuvant Systemic Therapy for Node-Positive Breast Cancer by combining PET/CT and the MARI Procedure. Ann Surg Oncol. 2018 25(6): 1512-1520.
27. Gasparri ML, de Boniface J, Poortmans P, et al. Axillary surgery after neoadjuvant therapy in initially node-positive breast cancer: international EUBREAST survey. Br J Surg. 2022;109(9):857-863.
28. Samiei S, Simons JM, Engelen SME, 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;156(6):e210891.
29. ELAMIN, G., SAPRE, D., TEHNIYAT, W., JAHAN, A., DAKKA, M.. Pathological complete response in the axillary lymph nodes post neo-adjuvant chemotherapy in breast cancer, is it predictable?. Annals of Breast Surgery, North America. 2019 Aug;3. Available at:
30. Kim R, Chang JM, Lee HB, et al. Predicting Axillary Response to Neoadjuvant Chemotherapy: Breast MRI and US in Patients with Node-Positive Breast Cancer. Radiology. 2019;293(1):49-57.
31. Corsi F, Albasini S, Sorrentino L, et al. Development of a novel nomogram-based online tool to predict axillary status after neoadjuvant chemotherapy in cN+ breast cancer: A multicentre study on 1,950 patients. Breast. 2021;60:131-137.
32. Reig B, Lewin AA, Du L, et al. Breast MRI for Evaluation of Response to Neoadjuvant Therapy. Radiographics. 2021;41(3):665-679.
33. Moo TA, Jochelson MS, Zabor EC, et al. Is Clinical Exam of the Axilla Sufficient to Select Node-Positive Patients Who Downstage After NAC for SLNB? A Comparison of the Accuracy of Clinical Exam Versus MRI. Ann Surg Oncol. 2019;26(13):4238–4243.
34. Turan U, Aygun M, Duman BB, et al. Efficacy of US, MRI, and F-18 FDG-PET/CT for Detecting Axillary Lymph Node Metastasis after Neoadjuvant Chemotherapy in Breast Cancer Patients. Diagnostics (Basel). 2021;11(12):2361.
35. Pesek S, Ashikaga T, Krag LE, Krag D. The false-negative rate of sentinel node biopsy in patients with breast cancer: a meta-analysis. World J Surg. 2012;36(9):2239-2251. doi:10.1007/s00268-012-1623-z
36. Simons JM, van Nijnatten TJA, van der Pol CC, Luiten EJT, Koppert LB, Smidt ML. Diagnostic Accuracy of Different Surgical Procedures for Axillary Staging After Neoadjuvant Systemic Therapy in Node-positive Breast Cancer: A Systematic Review and Meta-analysis. Ann Surg. 2019;269(3):432-442. doi:10.1097/SLA.0000000000003075
37. Swarnkar PK, Tayeh S, Michell MJ, Mokbel K. The Evolving Role of Marked Lymph Node Biopsy (MLNB) and Targeted Axillary Dissection (TAD) after Neoadjuvant Chemotherapy (NACT) for Node-Positive Breast Cancer: Systematic Review and Pooled Analysis. Cancers (Basel). 2021;13(7):1539.
38. Caudle AS, Yang WT, 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(10):1072-1078.
39. 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(4):804-812.
40. Friedrich M, Kühn T, Janni W, et al. AGO Recommendations for the Surgical Therapy of the Axilla After Neoadjuvant Chemotherapy: 2021 Update [published correction appears in Geburtshilfe Frauenheilkd. 2021 Oct 22;81(10):e31]. Geburtshilfe Frauenheilkd. 2021;81(10):1112-1120. doi:10.1055/a-1499-8431
41. Cardoso F, Kyriakides S, Ohno S, et al. Early breast cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2019;30(8):1194-1220.
42. Nikyar N, Tegnelius E, Valachis A. Adjuvant locoregional radiation therapy in breast cancer patients with pathologic complete response after neoadjuvant chemotherapy: A systematic review and meta-analysis. Clin Transl Radiat Oncol. 2022;33:45-52. Published 2022 Jan 5. doi:10.1016/j.ctro.2021.12.010
43. Banys-Paluchowski M, Thill M, Kühn T, et al. AGO Recommendations for the Surgical Therapy of Breast Cancer: Update 2022. Geburtshilfe Frauenheilkd. 2022;82(10):1031-1043. doi:10.1055/a-1904-6231
44. Tinterri C, Canavese G, Bruzzi P, Dozin B. 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;17:100496. Published 2019 Nov 23. doi:10.1016/j.conctc.2019.100496