Selection of Breast Cancer Patients for Omission of Axillary Lymph Node Surgery
Main Article Content
Abstract
The surgical procedure of complete axillary lymph node dissection, which initially included all the level I, II, and III nodes combined with a radical mastectomy in breast cancer patients, de-escalated to include only level I and II nodes with a modified radical mastectomy, leaving intact level III nodes. The sentinel node era, which began thirty years ago, allowed for removal of a small number of only level I nodes. The further decrease in the extent of node removal did not decrease the likelihood of curing patients with breast cancer. In addition, diminished axillary nodal surgery resulted in less complications, including less arm lymphedema. The latest advance is to use clinical, radiological, pathological, molecular, genetic, and other criteria to select breast cancer patients in whom all axillary nodal surgery can be avoided. In this review we summarize the current recommendations for axillary lymph node surgery, highlight and discuss the concomitant development of lymph node imaging, molecular genetic technologies, improved systemic and locoregional therapies, and more clearly elucidate the potential indications for omission of axillary nodal surgery.
Article Details
How to Cite
BUI, Jenny et al.
Selection of Breast Cancer Patients for Omission of Axillary Lymph Node Surgery.
Medical Research Archives, [S.l.], v. 12, n. 10, oct. 2024.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/5861>. Date accessed: 22 dec. 2024.
doi: https://doi.org/10.18103/mra.v12i10.5861.
Section
Research 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
1. Fisher B, Montague E, Redmond C, et al. Comparison of radical mastectomy with alternative treatments for primary breast cancer:A first report of results from a prospective randomized clinical trial. Cancer. 1977;39(6):2827-2839. doi:10.1002/1 097-0142(197706)39:6<2827::AID-CNCR2820390 671>3.0.CO;2-I
2. Fisher B, Dignam J, Bryant J, Wolmark N. Five versus more than five years of tamoxifen for lymph node-negative breast cancer: updated findings from the National Surgical Adjuvant Breast and Bowel Project B-14 randomized trial. JNCI J Natl Cancer Inst. 2001;93(9):684-690. doi:10.1093/jnci/ 93.9.684
3. Fisher B, Dignam J, Mamounas EP, et al. Sequential methotrexate and fluorouracil for the treatment of node-negative breast cancer patients with estrogen receptor-negative tumors: eight-year results from National Surgical Adjuvant Breast and Bowel Project (NSABP) B-13 and first report of findings from NSABP B-19 comparing methotrexate and fluorouracil with conventional cyclophosphamide, methotrexate, and fluorouracil. J Clin Oncol. 1996; 14(7):1982-1992. doi:10.1200/JCO.1996.14.7.1982
4. Romond EH, Perez EA, Bryant J, et al. Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N Engl J Med. 2005;353(16):1673-1684. doi:10.1056/NEJM oa052122
5. Shah C, Al-Hilli Z, Vicini F. Advances in Breast Cancer Radiotherapy: Implications for Current and Future Practice. JCO Oncol Pract. 2021;17(12): 697-706. doi:10.1200/OP.21.00635
6. Corti C, Batra-Sharma H, Kelsten M, Shatsky RA, Garrido-Castro AC, Gradishar WJ. Systemic Therapy in Breast Cancer. Am Soc Clin Oncol Educ Book. 2024;44(3):e432442. doi:10.1200/EDBK_432442
7. American Society of Breast Surgeons. Consensus statement on axillary management for patients with in-situ and invasive breast cancer: a concise overview. 2022. Accessed September 24, 2024. https://www.breastsurgeons.org/docs/statements/management-of-the-axilla.pdf
8. National Comprehensive Cancer Network. NCCN Clinical Practice Guidelines in Oncology: Breast cancer, version 4.2024. Published online July 3, 2024. Accessed September 24, 2024. https://www.nccn.org/professionals/physician_gls/pdf/breast.pdf
9. American Society of Clinical Oncology. Breast Cancer. Accessed September 24, 2024. https://society.asco.org/practice-patients/guidelines/breast-cancer
10. Society of Surgical Oncology. Breast Cancer. Accessed September 24, 2024.
https://surgonc.org/resources/guidelines/
11. 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. doi:10.1016/S1470-2045(10)70207-2
12. Veronesi U, Viale G, Paganelli G, et al. Sentinel lymph node biopsy in breast cancer: ten-year results of a randomized controlled study. Ann Surg. 2010;251(4):595-600. doi:10.1097/SLA.0b01 3e3181c0e92a
13. Boughey JC. 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. doi:10.1001/jama.2013.278932
14. Fayanju OM, Ren Y, Greenup RA, et al. Extent of axillary surgery in inflammatory breast cancer: a survival analysis of 3500 patients. Breast Cancer Res Treat. 2020;180(1):207-217. doi:10.1007/s105 49-020-05529-1
15. Rehman S, Reddy CA, Tendulkar RD. Modern outcomes of inflammatory breast cancer. Int J Radiat Oncol. 2012;84(3):619-624. doi:10.1016/j.ijr obp.2012.01.030
16. Britton P, Moyle P, Benson JR, et al. Ultrasound of the axilla: where to look for the sentinel lymph node. Clin Radiol. 2010;65(5):373-376. doi:10.1016/j.crad.2010.01.013
17. Swinson C, Ravichandran D, Nayagam M, Allen S. Ultrasound and fine needle aspiration cytology of the axilla in the pre-operative identification of axillary nodal involvement in breast cancer. Eur J Surg Oncol EJSO. 2009;35(11):1152-1157. doi:10.1016/j.ejso.2009.03.008
18. Ha SM, Chae EY, Cha JH, Shin HJ, Choi WJ, Kim HH. Diagnostic performance of standard breast MR imaging compared to dedicated axillary MR imaging in the evaluation of axillary lymph node. BMC Med Imaging. 2020;20(1):45. doi:10.1186/s 12880-020-00449-4
19. Kuijs VJL, Moossdorff M, Schipper RJ, et al. The role of MRI in axillary lymph node imaging in breast cancer patients: a systematic review. Insights Imaging. 2015;6(2):203-215. doi:10.1007/s13244-015-0404-2
20. De Mooij CM, Sunen I, Mitea C, et al. Diagnostic performance of PET/computed tomography versus PET/MRI and diffusion-weighted imaging in the N- and M-staging of breast cancer patients. Nucl Med Commun. 2020;41(10):995-1004. doi:10.1097/MNM.0000000000001254
21. Riegger C, Koeninger A, Hartung V, et al. Comparison of the diagnostic value of FDG-PET/CT and axillary ultrasound for the detection of lymph node metastases in breast cancer patients. Acta Radiol. 2012;53(10):1092-1098. doi:10.125 8/ar.2012.110635
22. Zheng H, Zhao R, Wang W, et al. The accuracy of ultrasound-guided fine-needle aspiration and core needle biopsy in diagnosing axillary lymph nodes in women with breast cancer: a systematic review and meta-analysis. Front Oncol. 2023;13:11 66035. doi:10.3389/fonc.2023.1166035
23. Huang Y, Liu Y, Wang Y, et al. Quantitative analysis of shear wave elastic heterogeneity for prediction of lymphovascular invasion in breast cancer. Br J Radiol. 2021;94(1127):20210682. doi:10.1259/bjr.20210682
24. Schwartz T. At the speed of SOUND: the pace of change for axillary management in breast cancer. Ann Surg Oncol. 2024;31(5):2801-2803. doi:10.1245/s10434-024-15010-8
25. Zhang H, Sui X, Zhou S, Hu L, Huang X. Correlation of conventional ultrasound characteristics of breast tumors With axillary lymph node metastasis and Ki‐67 expression in patients with breast cancer. J Ultrasound Med. 2019;38(7):1833-1840. doi:10.1002/jum.14879
26. Kim WH, Kim HJ, Lee SM, et al. Preoperative axillary nodal staging with ultrasound and magnetic resonance imaging: predictive values of quantitative and semantic features. Br J Radiol. 2018;91(1092):2 0180507. doi:10.1259/bjr.20180507
27. Gentilini OD, Botteri E, Sangalli C, et al. Sentinel lymph node biopsy vs no axillary surgery in patients with small breast cancer and negative results on ultrasonography of axillary lymph nodes: the SOUND randomized clinical trial. JAMA Oncol. 2023;9(11):1557. doi:10.1001/jamaoncol.2023.3759
28. Guo Q, Dong Z, Zhang L, et al. Ultrasound features of breast cancer for predicting axillary lymph node metastasis. J Ultrasound Med. 2018; 37(6):1354-1353. doi:10.1002/jum.14469
29. Li XL, Xu HX, Li DD, et al. A risk model based on ultrasound, ultrasound elastography, and histologic parameters for predicting axillary lymph node metastasis in breast invasive ductal carcinoma. Sci Rep. 2017;7(1):3029. doi:10.1038/s41598-017-03582-3
30. Yun SJ, Sohn YM, Seo M. Risk stratification for axillary lymph node metastases in breast cancer patients: what clinicopathological and radiological factors of primary breast cancer can predict preoperatively axillary lymph node metastases? Ultrasound Q. 2017;33(1):15-22. doi:10.1097/RU Q.0000000000000249
31. Tran HT, Pack D, Mylander C, et al. Ultrasound -based nomogram Identifies breast cancer patients unlikely to harbor axillary metastasis: towards selective omission of sentinel lymph node biopsy. Ann Surg Oncol. 2020;27(8):2679-2686.
doi:10.1245/s10434-019-08164-3
32. Zhang M, Zha H, Pan J, et al. Development of an ultrasound-based nomogram for predicting pathologic complete response and axillary response in node-positive patients with triple- negative breast cancer. Clin Breast Cancer. 2024;24(6):e48 5-e494.e1. doi:10.1016/j.clbc.2024.03.012
33. Lee J, Park HY, Kim WW, Park CS, Jeong M, Jung JH. Efficacy of ultrasound-guiided core needle biopsy in detecting metastatic axillary lymph nodes in breast cancer. J Surg Ultrasound. 2020;7(2):21-28. doi:10.46268/jsu.2020.7.2.21
34. Luo Y, Zhao C, Gao Y, et al. Predicting axillary lymph node status With a nomogram based on breast lesion ultrasound features: performance in N1 breast cancer patients. Front Oncol. 2020; 10:581321. doi:10.3389/fonc.2020.581321
35.Nathanson SD, Burke M, Slater R, Kapke A. Preoperative Identification of the Sentinel Lymph Node in Breast Cancer. Ann Surg Oncol. 2007; 14(11):3102-3110. doi:10.1245/s10434-007-9494-5
36. Giuliano AE, Ballman KV, McCall L, et al. Effect of axillary dissection vs no axillary dissection on 10-year overall survival among women with invasive breast cancer and sentinel node metastasis: the ACOSOG Z0011 (Alliance) randomized clinical trial. JAMA. 2017;318(10):918. doi:10.1001/jama.201 7.11470
37. Donker M, Van Tienhoven G, Straver ME, et al. Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981-22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol. 2014;15(12):1303-1310. doi:10.1016/S1470 -2045(14)70460-7
38. De Boniface J, Filtenborg Tvedskov T, Rydén L, et al. Omitting axillary dissection in breast cancer with sentinel-node metastases. N Engl J Med. 2024;390(13):1163-1175. doi:10.1056/NEJMoa23 13487
39. The American Board of Internal Medicine Foundation. Choosing Wisely® Campaign. Accessed September 24, 2024. https://choosingwisely.org/
40. 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(7):609-618. doi:10.1016/S1 470-2045(13)70166-9
41. 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. doi:10.1200/J CO.2015.64.0094
42. Nathanson D. Sentinel lymph node biopsy in breast cancer: past, present, and future. J Oncol Res Ther. 2023;8(3). doi:10.29011/2574-710X.10178
43. Caudle AS, Yang WT, Mittendorf EA, et al. Selective Surgical Localization of Axillary Lymph Nodes Containing Metastases in Patients With Breast Cancer: A Prospective Feasibility Trial. JAMA Surg. 2015;150(2):137. doi:10.1001/jamasurg.201 4.1086
44. Plecha D, Bai S, Patterson H, Thompson C, Shenk R. 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(13):4241-4246. doi:10.1245/s10434-015-4527-y
45. 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;44(9):1307-1311. doi:10.1016/j.ejso.2 018.05.035
46. 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;46(6):1028-1033. doi:10.1016/j.ejso.2019.12.007
47. Anderson WF, Chu KC, Chang S. Inflammatory breast carcinoma and noninflammatory locally advanced breast carcinoma: distinct clinicopathologic entities? J Clin Oncol. 2003;21(12):2254-2259. doi:10.1200/JCO.2003.07.082
48. Yang WT, Le-Petross HT, Macapinlac H, et al. Inflammatory breast cancer: PET/CT, MRI, mammography, and sonography findings. Breast Cancer Res Treat. 2008;109(3):417-426. doi:10.100 7/s10549-007-9671-z
49. Fields RC, Jeffe DB, Trinkaus K, et al. Surgical resection of the primary tumor is associated with increased long-term survival in patients with stage IV breast cancer after controlling for site of metastasis. Ann Surg Oncol. 2007;14(12):3345-3351. doi:10.1245/s10434-007-9527-0
50. Gnerlich J, Jeffe DB, Deshpande AD, Beers C, Zander C, Margenthaler JA. Surgical removal of the primary tumor increases overall survival in patients with metastatic breast cancer: analysis of the 1988–2003 SEER data. Ann Surg Oncol. 2007; 14(8):2187-2194. doi:10.1245/s10434-007-9438-0
51. Rao R, Feng L, Kuerer HM, et al. Timing of surgical intervention for the intact primary in stage IV breast cancer patients. Ann Surg Oncol. 2008; 15(6):1696-1702. doi:10.1245/s10434-008-9830-4
52. Brown M, Assen FP, Leithner A, et al. Lymph node blood vessels provide exit routes for metastatic tumor cell dissemination in mice. Science. 2018;359(6382):1408-1411. doi:10.1126/science.a al3662
53. Pereira ER, Kedrin D, Seano G, et al. Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice. Science. 2018;359(6382):1403-1407. doi:10.112 6/science.aal3622
54. Tada K, Ogiya A, Kimura K, et al. Ductal carcinoma in situ and sentinel lymph node metastasis in breast cancer. World J Surg Oncol. 2010;8(1):6. doi:10.1186/1477-7819-8-6
55. Martelli G, Miceli R, Daidone MG, et al. Axillary dissection versus no axillary dissection in elderly patients with breast cancer and no palpable axillary nodes: results after 15 Years of follow-Up. Ann Surg Oncol. 2011;18(1):125-133. doi:10.1245/s10434-010-1217-7
56. Chung AP, Dang CM, Karlan SR, et al. A prospective study of sentinel node biopsy omission in women age ≥ 65 years with ER+ breast cancer. Ann Surg Oncol. 2024;31(5):3160-3167. doi:10.124 5/s10434-024-15000-w
57. Hughes KS, Schnaper LA, Berry D, et al. Lumpectomy plus tamoxifen with or without Irradiation in women 70 years of age or older with early breast cancer. N Engl J Med. 2004;351(10): 971-977. doi:10.1056/NEJMoa040587
58. Nathanson S, Leonard-Murali S, Bui J, et al. Combined selected pathological variables predict a low likelihood of axillary node metastasis in breast cancer patients regardless of age. Poster presented at: American Society of Breast Surgeons 25th Annual Meeting; April 10, 2024; Orlando, FL.
59. Min Y, Bae SY, Lee HC, et al. Tubular carcinoma of the breast: clinicopathologic features and survival outcome compared with ductal Carcinoma in situ. J Breast Cancer. 2013;16(4):404. doi:10.4048/jbc.2013.16.4.404
60. Javid SH, Smith BL, Mayer E, et al. Tubular carcinoma of the breast: results of a large contemporary series. Am J Surg. 2009;197(5):674-677. doi:10.1016/j.amjsurg.2008.05.005
61. Budzik M, Sobieraj M, Sobol M, et al. Medullary breast cancer is a predominantly triple-negative breast cancer – histopathological analysis and comparison with invasive ductal breast cancer. Arch Med Sci. 2019;18(2):432-439. doi:10.5114/a oms.2019.86763
62. Marrazzo E, Frusone F, Milana F, et al. Mucinous breast cancer: A narrative review of the literature and a retrospective tertiary single-centre analysis. The Breast. 2020;49:87-92. doi:10.1016/j. breast.2019.11.002
63. Bhargava R, Esposito NN, OʹConnor SM, et al. Magee EquationsTM and response to neoadjuvant chemotherapy in ER+/HER2-negative breast cancer: a multi-institutional study. Mod Pathol. 2021;34(1):77-84. doi:10.1038/s41379-020-0620-2
64. Paik S, Shak S, Tang G, et al. A Multigene Assay to Predict Recurrence of Tamoxifen-Treated, Node-Negative Breast Cancer. N Engl J Med. 2004; 351(27):2817-2826. doi:10.1056/NEJMoa041588
65. Pauls M, Chia S. Clinical Utility of Genomic Assay in Node-Positive Early-Stage Breast Cancer. Curr Oncol. 2022;29(7):5139-5149. doi:10.3390/cu rroncol29070407
66. Jana S, Muscarella RA, Jones D. The Multifaceted Effects of Breast Cancer on Tumor-Draining Lymph Nodes. Am J Pathol. 2021;191 (8):1353-1363. doi:10.1016/j.ajpath.2021.05.006
67. Nathanson SD, Detmar M, Padera TP, et al. Mechanisms of breast cancer metastasis. Clin Exp Metastasis. 2022;39(1):117-137. doi:10.1007/s105 85-021-10090-2
68. Naxerova K, Reiter JG, Brachtel E, et al. Origins of lymphatic and distant metastases in human colorectal cancer. Science. 2017;357(6346):55-60. doi:10.1126/science.aai8515
69. Nathanson SD, Dieterich LC, Zhang XHF, et al. Associations amongst genes, molecules, cells, and organs in breast cancer metastasis. Clin Exp Metastasis. 2023;41:417-437. doi:10.1007/s10585-023-10230-w
70. Rakha EA, Tse GM, Quinn CM. An update on the pathological classification of breast cancer. Histopathology. 2023;82(1):5-16. doi:10.1111/his14786
71. Bonadonna G, Rossi A, Valagussa P, Banfi A, Veronesi U. The CMF program for operable breast cancer with positive axillary nodes:Updated analysis on the disease-free interval, site of relapse and drug tolerance. Cancer. 1977;39(6):2904-2915. doi:10.1002/1097-0142(197706)39:6<2904::AID-CNCR2820390677>3.0.CO;2-8
72. Kaidar-Person O, Meattini I, Poortmans P, eds. Breast Cancer Radiation Therapy: A Practical Guide for Technical Applications. 1st ed. Springer International Publishing; 2022.
73. Hoda SAF, Koerner FC, Brogi E, Rosen PP. Rosen’s Breast Pathology. 5th edition. Wolters Kluwer; 2021.
74. Perou CM, Sørlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature. 2000; 406(6797):747-752. doi:10.1038/35021093
75. Van Zee KJ, Manasseh DME, Bevilacqua JLB, 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. doi:10.124 5/ASO.2003.03.015
76. Narod SA, Foulkes WD. BRCA1 and BRCA2: 1994 and beyond. Nat Rev Cancer. 2004;4(9):665-676. doi:10.1038/nrc1431
77. Coles CE, Earl H, Anderson BO, et al. The Lancet Breast Cancer Commission. The Lancet. 2024;403(10439):1895-1950. doi:10.1016/S0140-6736(24)00747-5
2. Fisher B, Dignam J, Bryant J, Wolmark N. Five versus more than five years of tamoxifen for lymph node-negative breast cancer: updated findings from the National Surgical Adjuvant Breast and Bowel Project B-14 randomized trial. JNCI J Natl Cancer Inst. 2001;93(9):684-690. doi:10.1093/jnci/ 93.9.684
3. Fisher B, Dignam J, Mamounas EP, et al. Sequential methotrexate and fluorouracil for the treatment of node-negative breast cancer patients with estrogen receptor-negative tumors: eight-year results from National Surgical Adjuvant Breast and Bowel Project (NSABP) B-13 and first report of findings from NSABP B-19 comparing methotrexate and fluorouracil with conventional cyclophosphamide, methotrexate, and fluorouracil. J Clin Oncol. 1996; 14(7):1982-1992. doi:10.1200/JCO.1996.14.7.1982
4. Romond EH, Perez EA, Bryant J, et al. Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N Engl J Med. 2005;353(16):1673-1684. doi:10.1056/NEJM oa052122
5. Shah C, Al-Hilli Z, Vicini F. Advances in Breast Cancer Radiotherapy: Implications for Current and Future Practice. JCO Oncol Pract. 2021;17(12): 697-706. doi:10.1200/OP.21.00635
6. Corti C, Batra-Sharma H, Kelsten M, Shatsky RA, Garrido-Castro AC, Gradishar WJ. Systemic Therapy in Breast Cancer. Am Soc Clin Oncol Educ Book. 2024;44(3):e432442. doi:10.1200/EDBK_432442
7. American Society of Breast Surgeons. Consensus statement on axillary management for patients with in-situ and invasive breast cancer: a concise overview. 2022. Accessed September 24, 2024. https://www.breastsurgeons.org/docs/statements/management-of-the-axilla.pdf
8. National Comprehensive Cancer Network. NCCN Clinical Practice Guidelines in Oncology: Breast cancer, version 4.2024. Published online July 3, 2024. Accessed September 24, 2024. https://www.nccn.org/professionals/physician_gls/pdf/breast.pdf
9. American Society of Clinical Oncology. Breast Cancer. Accessed September 24, 2024. https://society.asco.org/practice-patients/guidelines/breast-cancer
10. Society of Surgical Oncology. Breast Cancer. Accessed September 24, 2024.
https://surgonc.org/resources/guidelines/
11. 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. doi:10.1016/S1470-2045(10)70207-2
12. Veronesi U, Viale G, Paganelli G, et al. Sentinel lymph node biopsy in breast cancer: ten-year results of a randomized controlled study. Ann Surg. 2010;251(4):595-600. doi:10.1097/SLA.0b01 3e3181c0e92a
13. Boughey JC. 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. doi:10.1001/jama.2013.278932
14. Fayanju OM, Ren Y, Greenup RA, et al. Extent of axillary surgery in inflammatory breast cancer: a survival analysis of 3500 patients. Breast Cancer Res Treat. 2020;180(1):207-217. doi:10.1007/s105 49-020-05529-1
15. Rehman S, Reddy CA, Tendulkar RD. Modern outcomes of inflammatory breast cancer. Int J Radiat Oncol. 2012;84(3):619-624. doi:10.1016/j.ijr obp.2012.01.030
16. Britton P, Moyle P, Benson JR, et al. Ultrasound of the axilla: where to look for the sentinel lymph node. Clin Radiol. 2010;65(5):373-376. doi:10.1016/j.crad.2010.01.013
17. Swinson C, Ravichandran D, Nayagam M, Allen S. Ultrasound and fine needle aspiration cytology of the axilla in the pre-operative identification of axillary nodal involvement in breast cancer. Eur J Surg Oncol EJSO. 2009;35(11):1152-1157. doi:10.1016/j.ejso.2009.03.008
18. Ha SM, Chae EY, Cha JH, Shin HJ, Choi WJ, Kim HH. Diagnostic performance of standard breast MR imaging compared to dedicated axillary MR imaging in the evaluation of axillary lymph node. BMC Med Imaging. 2020;20(1):45. doi:10.1186/s 12880-020-00449-4
19. Kuijs VJL, Moossdorff M, Schipper RJ, et al. The role of MRI in axillary lymph node imaging in breast cancer patients: a systematic review. Insights Imaging. 2015;6(2):203-215. doi:10.1007/s13244-015-0404-2
20. De Mooij CM, Sunen I, Mitea C, et al. Diagnostic performance of PET/computed tomography versus PET/MRI and diffusion-weighted imaging in the N- and M-staging of breast cancer patients. Nucl Med Commun. 2020;41(10):995-1004. doi:10.1097/MNM.0000000000001254
21. Riegger C, Koeninger A, Hartung V, et al. Comparison of the diagnostic value of FDG-PET/CT and axillary ultrasound for the detection of lymph node metastases in breast cancer patients. Acta Radiol. 2012;53(10):1092-1098. doi:10.125 8/ar.2012.110635
22. Zheng H, Zhao R, Wang W, et al. The accuracy of ultrasound-guided fine-needle aspiration and core needle biopsy in diagnosing axillary lymph nodes in women with breast cancer: a systematic review and meta-analysis. Front Oncol. 2023;13:11 66035. doi:10.3389/fonc.2023.1166035
23. Huang Y, Liu Y, Wang Y, et al. Quantitative analysis of shear wave elastic heterogeneity for prediction of lymphovascular invasion in breast cancer. Br J Radiol. 2021;94(1127):20210682. doi:10.1259/bjr.20210682
24. Schwartz T. At the speed of SOUND: the pace of change for axillary management in breast cancer. Ann Surg Oncol. 2024;31(5):2801-2803. doi:10.1245/s10434-024-15010-8
25. Zhang H, Sui X, Zhou S, Hu L, Huang X. Correlation of conventional ultrasound characteristics of breast tumors With axillary lymph node metastasis and Ki‐67 expression in patients with breast cancer. J Ultrasound Med. 2019;38(7):1833-1840. doi:10.1002/jum.14879
26. Kim WH, Kim HJ, Lee SM, et al. Preoperative axillary nodal staging with ultrasound and magnetic resonance imaging: predictive values of quantitative and semantic features. Br J Radiol. 2018;91(1092):2 0180507. doi:10.1259/bjr.20180507
27. Gentilini OD, Botteri E, Sangalli C, et al. Sentinel lymph node biopsy vs no axillary surgery in patients with small breast cancer and negative results on ultrasonography of axillary lymph nodes: the SOUND randomized clinical trial. JAMA Oncol. 2023;9(11):1557. doi:10.1001/jamaoncol.2023.3759
28. Guo Q, Dong Z, Zhang L, et al. Ultrasound features of breast cancer for predicting axillary lymph node metastasis. J Ultrasound Med. 2018; 37(6):1354-1353. doi:10.1002/jum.14469
29. Li XL, Xu HX, Li DD, et al. A risk model based on ultrasound, ultrasound elastography, and histologic parameters for predicting axillary lymph node metastasis in breast invasive ductal carcinoma. Sci Rep. 2017;7(1):3029. doi:10.1038/s41598-017-03582-3
30. Yun SJ, Sohn YM, Seo M. Risk stratification for axillary lymph node metastases in breast cancer patients: what clinicopathological and radiological factors of primary breast cancer can predict preoperatively axillary lymph node metastases? Ultrasound Q. 2017;33(1):15-22. doi:10.1097/RU Q.0000000000000249
31. Tran HT, Pack D, Mylander C, et al. Ultrasound -based nomogram Identifies breast cancer patients unlikely to harbor axillary metastasis: towards selective omission of sentinel lymph node biopsy. Ann Surg Oncol. 2020;27(8):2679-2686.
doi:10.1245/s10434-019-08164-3
32. Zhang M, Zha H, Pan J, et al. Development of an ultrasound-based nomogram for predicting pathologic complete response and axillary response in node-positive patients with triple- negative breast cancer. Clin Breast Cancer. 2024;24(6):e48 5-e494.e1. doi:10.1016/j.clbc.2024.03.012
33. Lee J, Park HY, Kim WW, Park CS, Jeong M, Jung JH. Efficacy of ultrasound-guiided core needle biopsy in detecting metastatic axillary lymph nodes in breast cancer. J Surg Ultrasound. 2020;7(2):21-28. doi:10.46268/jsu.2020.7.2.21
34. Luo Y, Zhao C, Gao Y, et al. Predicting axillary lymph node status With a nomogram based on breast lesion ultrasound features: performance in N1 breast cancer patients. Front Oncol. 2020; 10:581321. doi:10.3389/fonc.2020.581321
35.Nathanson SD, Burke M, Slater R, Kapke A. Preoperative Identification of the Sentinel Lymph Node in Breast Cancer. Ann Surg Oncol. 2007; 14(11):3102-3110. doi:10.1245/s10434-007-9494-5
36. Giuliano AE, Ballman KV, McCall L, et al. Effect of axillary dissection vs no axillary dissection on 10-year overall survival among women with invasive breast cancer and sentinel node metastasis: the ACOSOG Z0011 (Alliance) randomized clinical trial. JAMA. 2017;318(10):918. doi:10.1001/jama.201 7.11470
37. Donker M, Van Tienhoven G, Straver ME, et al. Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981-22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol. 2014;15(12):1303-1310. doi:10.1016/S1470 -2045(14)70460-7
38. De Boniface J, Filtenborg Tvedskov T, Rydén L, et al. Omitting axillary dissection in breast cancer with sentinel-node metastases. N Engl J Med. 2024;390(13):1163-1175. doi:10.1056/NEJMoa23 13487
39. The American Board of Internal Medicine Foundation. Choosing Wisely® Campaign. Accessed September 24, 2024. https://choosingwisely.org/
40. 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(7):609-618. doi:10.1016/S1 470-2045(13)70166-9
41. 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. doi:10.1200/J CO.2015.64.0094
42. Nathanson D. Sentinel lymph node biopsy in breast cancer: past, present, and future. J Oncol Res Ther. 2023;8(3). doi:10.29011/2574-710X.10178
43. Caudle AS, Yang WT, Mittendorf EA, et al. Selective Surgical Localization of Axillary Lymph Nodes Containing Metastases in Patients With Breast Cancer: A Prospective Feasibility Trial. JAMA Surg. 2015;150(2):137. doi:10.1001/jamasurg.201 4.1086
44. Plecha D, Bai S, Patterson H, Thompson C, Shenk R. 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(13):4241-4246. doi:10.1245/s10434-015-4527-y
45. 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;44(9):1307-1311. doi:10.1016/j.ejso.2 018.05.035
46. 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;46(6):1028-1033. doi:10.1016/j.ejso.2019.12.007
47. Anderson WF, Chu KC, Chang S. Inflammatory breast carcinoma and noninflammatory locally advanced breast carcinoma: distinct clinicopathologic entities? J Clin Oncol. 2003;21(12):2254-2259. doi:10.1200/JCO.2003.07.082
48. Yang WT, Le-Petross HT, Macapinlac H, et al. Inflammatory breast cancer: PET/CT, MRI, mammography, and sonography findings. Breast Cancer Res Treat. 2008;109(3):417-426. doi:10.100 7/s10549-007-9671-z
49. Fields RC, Jeffe DB, Trinkaus K, et al. Surgical resection of the primary tumor is associated with increased long-term survival in patients with stage IV breast cancer after controlling for site of metastasis. Ann Surg Oncol. 2007;14(12):3345-3351. doi:10.1245/s10434-007-9527-0
50. Gnerlich J, Jeffe DB, Deshpande AD, Beers C, Zander C, Margenthaler JA. Surgical removal of the primary tumor increases overall survival in patients with metastatic breast cancer: analysis of the 1988–2003 SEER data. Ann Surg Oncol. 2007; 14(8):2187-2194. doi:10.1245/s10434-007-9438-0
51. Rao R, Feng L, Kuerer HM, et al. Timing of surgical intervention for the intact primary in stage IV breast cancer patients. Ann Surg Oncol. 2008; 15(6):1696-1702. doi:10.1245/s10434-008-9830-4
52. Brown M, Assen FP, Leithner A, et al. Lymph node blood vessels provide exit routes for metastatic tumor cell dissemination in mice. Science. 2018;359(6382):1408-1411. doi:10.1126/science.a al3662
53. Pereira ER, Kedrin D, Seano G, et al. Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice. Science. 2018;359(6382):1403-1407. doi:10.112 6/science.aal3622
54. Tada K, Ogiya A, Kimura K, et al. Ductal carcinoma in situ and sentinel lymph node metastasis in breast cancer. World J Surg Oncol. 2010;8(1):6. doi:10.1186/1477-7819-8-6
55. Martelli G, Miceli R, Daidone MG, et al. Axillary dissection versus no axillary dissection in elderly patients with breast cancer and no palpable axillary nodes: results after 15 Years of follow-Up. Ann Surg Oncol. 2011;18(1):125-133. doi:10.1245/s10434-010-1217-7
56. Chung AP, Dang CM, Karlan SR, et al. A prospective study of sentinel node biopsy omission in women age ≥ 65 years with ER+ breast cancer. Ann Surg Oncol. 2024;31(5):3160-3167. doi:10.124 5/s10434-024-15000-w
57. Hughes KS, Schnaper LA, Berry D, et al. Lumpectomy plus tamoxifen with or without Irradiation in women 70 years of age or older with early breast cancer. N Engl J Med. 2004;351(10): 971-977. doi:10.1056/NEJMoa040587
58. Nathanson S, Leonard-Murali S, Bui J, et al. Combined selected pathological variables predict a low likelihood of axillary node metastasis in breast cancer patients regardless of age. Poster presented at: American Society of Breast Surgeons 25th Annual Meeting; April 10, 2024; Orlando, FL.
59. Min Y, Bae SY, Lee HC, et al. Tubular carcinoma of the breast: clinicopathologic features and survival outcome compared with ductal Carcinoma in situ. J Breast Cancer. 2013;16(4):404. doi:10.4048/jbc.2013.16.4.404
60. Javid SH, Smith BL, Mayer E, et al. Tubular carcinoma of the breast: results of a large contemporary series. Am J Surg. 2009;197(5):674-677. doi:10.1016/j.amjsurg.2008.05.005
61. Budzik M, Sobieraj M, Sobol M, et al. Medullary breast cancer is a predominantly triple-negative breast cancer – histopathological analysis and comparison with invasive ductal breast cancer. Arch Med Sci. 2019;18(2):432-439. doi:10.5114/a oms.2019.86763
62. Marrazzo E, Frusone F, Milana F, et al. Mucinous breast cancer: A narrative review of the literature and a retrospective tertiary single-centre analysis. The Breast. 2020;49:87-92. doi:10.1016/j. breast.2019.11.002
63. Bhargava R, Esposito NN, OʹConnor SM, et al. Magee EquationsTM and response to neoadjuvant chemotherapy in ER+/HER2-negative breast cancer: a multi-institutional study. Mod Pathol. 2021;34(1):77-84. doi:10.1038/s41379-020-0620-2
64. Paik S, Shak S, Tang G, et al. A Multigene Assay to Predict Recurrence of Tamoxifen-Treated, Node-Negative Breast Cancer. N Engl J Med. 2004; 351(27):2817-2826. doi:10.1056/NEJMoa041588
65. Pauls M, Chia S. Clinical Utility of Genomic Assay in Node-Positive Early-Stage Breast Cancer. Curr Oncol. 2022;29(7):5139-5149. doi:10.3390/cu rroncol29070407
66. Jana S, Muscarella RA, Jones D. The Multifaceted Effects of Breast Cancer on Tumor-Draining Lymph Nodes. Am J Pathol. 2021;191 (8):1353-1363. doi:10.1016/j.ajpath.2021.05.006
67. Nathanson SD, Detmar M, Padera TP, et al. Mechanisms of breast cancer metastasis. Clin Exp Metastasis. 2022;39(1):117-137. doi:10.1007/s105 85-021-10090-2
68. Naxerova K, Reiter JG, Brachtel E, et al. Origins of lymphatic and distant metastases in human colorectal cancer. Science. 2017;357(6346):55-60. doi:10.1126/science.aai8515
69. Nathanson SD, Dieterich LC, Zhang XHF, et al. Associations amongst genes, molecules, cells, and organs in breast cancer metastasis. Clin Exp Metastasis. 2023;41:417-437. doi:10.1007/s10585-023-10230-w
70. Rakha EA, Tse GM, Quinn CM. An update on the pathological classification of breast cancer. Histopathology. 2023;82(1):5-16. doi:10.1111/his14786
71. Bonadonna G, Rossi A, Valagussa P, Banfi A, Veronesi U. The CMF program for operable breast cancer with positive axillary nodes:Updated analysis on the disease-free interval, site of relapse and drug tolerance. Cancer. 1977;39(6):2904-2915. doi:10.1002/1097-0142(197706)39:6<2904::AID-CNCR2820390677>3.0.CO;2-8
72. Kaidar-Person O, Meattini I, Poortmans P, eds. Breast Cancer Radiation Therapy: A Practical Guide for Technical Applications. 1st ed. Springer International Publishing; 2022.
73. Hoda SAF, Koerner FC, Brogi E, Rosen PP. Rosen’s Breast Pathology. 5th edition. Wolters Kluwer; 2021.
74. Perou CM, Sørlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature. 2000; 406(6797):747-752. doi:10.1038/35021093
75. Van Zee KJ, Manasseh DME, Bevilacqua JLB, 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. doi:10.124 5/ASO.2003.03.015
76. Narod SA, Foulkes WD. BRCA1 and BRCA2: 1994 and beyond. Nat Rev Cancer. 2004;4(9):665-676. doi:10.1038/nrc1431
77. Coles CE, Earl H, Anderson BO, et al. The Lancet Breast Cancer Commission. The Lancet. 2024;403(10439):1895-1950. doi:10.1016/S0140-6736(24)00747-5