Can axillary surgery be omitted in breast cancer using ultrasound-guided needle aspiration or biopsy? CORPA trial: a phase 1 prospective study
DOI:
https://doi.org/10.29289/2594539420250054Palavras-chave:
breast neoplasms, ultrasonography, fine-needle biopsy, large-core needle biopsy, sentinel lymph nodeResumo
Introduction: Fine-needle aspiration or core needle biopsy guided by ultrasound of the axilla can provide crucial information for the treatment of breast cancer. Methods: This prospective phase 1 real-world study evaluated the effectiveness of the triple test, physical examination (PE), ultrasound (US), and ultrasound-guided fine-needle aspiration (USFNA) or ultrasound-guided core needle biopsy (USCNB) in predicting axillary metastases. It also explored the possibility of omitting axillary surgery based on negative results. The study included patients with high-penetrance mutations, ductal carcinoma in situ, or invasive breast cancer (cT1–4, axillary cN0–2), all of whom underwent aspiration or biopsy along with lymph node marking (using charcoal or clips), followed by sentinel lymph node biopsy and/or axillary dissection. Results: A total of 363 lymph nodes were dissected in 43 patients. The sensitivity of PE and US was 33.3% and 53.3%, respectively. When combining USFNA/USCNB with PE and US, sensitivity increased from 66.67% to 80%. Among patients with mutations or ductal carcinoma in situ or invasive cancer (cT1–4), when all three methods (PE, US, and USFNA/USCNB) were negative, the rate of positive lymph nodes was only 10%. Conclusions: Relying solely on PE, US, or USFNA/USCNB has limitations in detecting axillary metastases. Incorporating USFNA/USCNB significantly improved sensitivity and decreased false-negative rates. When all three methods were negative, the rate of axillary involvement was only 10%, indicating that axillary surgery could potentially be omitted. However, further studies are needed to validate these methods as reliable predictive tools for treatment decisions.
Downloads
Referências
1. World Health Organization. Câncer de mama agora a forma mais comum de cancer: OMS tomando medidas [Internet]. 2021 [cited on Feb 03, 2021]. Available from: https://www.who.int/pt/news/item/03-02-2021-breast-cancer-now-most-common-form-of-cancer-who-taking-action
2. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al . Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209-49. https://doi.org/10.3322/caac.21660
3. Lanng C, Hoffmann J, Galatius H, Engel U. Assessment of clinical palpation of the axilla as a criterion for performing the sentinel node procedure in breast cancer. Eur J Surg Oncol. 2007;33(3):281-4. https://doi.org/10.1016/j.ejso.2006.09.032
4. Majid S, Tengrup I, Manjer J. Clinical assessment of axillary LNs and tumor size in breast cancer compared with histopathological examination: a population-based analysis of 2,537 women. World J Surg. 2013;37(1):67-71. https://doi.org/10.1007/s00268-012-1788-5
5. Feng Y, Huang R, He Y, Lu A, Fan Z, Fan T, et al. Efficacy of physical examination, ultrasound, and ultrasound combined with fine-needle aspiration for axilla staging of primary breast cancer. Breast Cancer Res Treat. 2015;149(3):761-5. https://doi.org/10.1007/s10549-015-3280-z
6. Dihge L, Grabau DA, Rasmussen RW, Bendahl PO, Rydén L. The accuracy of preoperative axillary nodal staging in primary breast cancer by ultrasound is modified by nodal metastatic load and tumor biology. Acta Oncol. 2016;55(8):976-82. https://doi.org/10.3109/0284186X.2016.1146826
7. Alvarez S, Añorbe E, Alcorta P, López F, Alonso I, Cortés J. Role of sonography in the diagnosis of axillary lymph node metastases in breast cancer: a systematic review. AJR Am J Roentgenol. 2006;186(5):1342-8. https://doi.org/10.2214/AJR.05.0936
8. Riedel F, Schaefgen B, Sinn HP, Feisst M, Hennigs A, Hug S, et al. Diagnostic accuracy of axillary staging by ultrasound in early breast cancer patients. Eur J Radiol. 2021;135:109468. https://doi.org/10.1016/j.ejrad.2020.109468
9. Man V, Luk WP, Fung LH, Kwong A. The role of pre-operative axillary ultrasound in assessment of axillary tumor burden in breast cancer patients: a systematic review and meta-analysis. Breast Cancer Res Treat. 2022;196(2):245-54. https://doi.org/10.1007/s10549-022-06699-w
10. Weber WP, Gentilini OD, Morrow M, Montagna G, Boniface J, Fitzal F, et al. Uncertainties and controversies in axillary management of patients with breast cancer. Cancer Treat Rev. 2023;117:102556. https://doi.org/10.1016/j.ctrv.2023.102556
11. Karampelias V, Koukouras D, Tzorakoleftherakis E, Mariolis-Sapsakos T, Chrysikos D. Breast cancer section analysis correlates with sentinel lymph node biopsies: precision and topographic anatomy. Breast Dis. 2019;38(1):1-5. https://doi.org/10.3233/BD-180355
12. Giuliano AE, Ballman KV, McCall L, Beitsch PD, Brennan MB, Kelemen PR, 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):918-26. https://doi.org/10.1001/jama.2017.11470
13. van Roozendaal LM, Vane MLG, van Dalen T, van der Hage JA, Strobbe LJA, Boersma LJ, 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):459. https://doi.org/10.1186/s12885-017-3443-x
14. Galimberti V, Cole BF, Viale G, Veronesi P, Vicini E, Intra M, 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(10):1385-93. https://doi.org/10.1016/S1470-2045(18)30380-2
15. Tran HT, Pack D, Mylander C, Martino L, Rosman M, Tafra L, 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):2679-86. https://doi.org/10.1245/s10434-019-08164-3
16. Lee MK, Montagna G, Pilewskie ML, Sevilimedu V. axillary staging is not justified in postmenopausal clinically node-negative women based on nodal disease burden. Ann Surg Oncol. 2023;30(1):92-7. https://doi.org/10.1245/s10434-022-12203-x
17. Gentilini OD, Botteri E, Sangalli C, Galimberti V, Porpiglia M, Agresti R, 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):1557-64. https://doi.org/10.1001/jamaoncol.2023.3759
18. Pessoa EC, Rodrigues JR, Pessoa CKCP, Véspoli HML, Uemura G. Punção aspirativa de linfonodo axilar guiada pela ultrassonografia é eficaz como método de predição de acometimento linfonodal em pacientes com câncer de mama? Rev Bras Ginecol Obstet. 2014;36(3):118-23. https://doi.org/10.1590/S0100-72032014000300005
19. Balasubramanian I, Fleming CA, Corrigan MA, Redmond HP, Kerin MJ, Lowery AJ. Meta-analysis of the diagnostic accuracy of ultrasound-guided fine-needle aspiration and core needle biopsy in diagnosing axillary lymph node metastasis. Br J Surg. 2018;105(10):1244-53. https://doi.org/10.1002/bjs.10920
20. Huang Y, Zheng S, Lin Y. Accuracy and utility of preoperative ultrasound- guided axillary lymph node biopsy for invasive breast cancer: a systematic review and meta-analysis. Comput Intell Neurosci. 2022;2022:3307627. https://doi.org/10.1155/2022/3307627
21. American Joint Committee on Cancer. Cancer staging manual. 8th ed. New York: Springer International Publishing; 2016.
22. Le Boulc'h M, Gilhodes J, Steinmeyer Z, Molière S, Mathelin C. Pretherapeutic imaging for axillary staging in breast cancer: a systematic review and meta- analysis of ultrasound, MRI and FDG PET. J Clin Med. 2021;10(7):1543. https://doi.org/10.3390/jcm10071543
23. Tucker NS, Cyr AE, Ademuyiwa FO, Tabchy A, George K, Sharma PK, et al. Axillary ultrasound accurately excludes clinically significant lymph node disease in patients with early stage breast cancer. Ann Surg. 2016;264(6):1098-102. https://doi.org/10.1097/SLA.0000000000001549
24. Zheng H, Zhao R, Wang W, Liu X, Wang X, Wen C, 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;13:1166035. https://doi.org/10.3389/fonc.2023.1166035
25. Xu Q, Wang J, Wang J, Guo R, Qian Y, Liu F. The effectiveness of ultrasound-guided core needle biopsy in detecting lymph node metastases in the axilla in patients with breast cancer: systematic review and meta-analysis. Clinics (Sao Paulo). 2023;78:100207. https://doi.org/10.1016/j.clinsp.2023.100207
26. Boniface J, Tvedskov TF, Rydén L, Szulkin R, Reimer T, Kühn T, et al. Omitting axillary dissection in breast cancer with sentinel-node metastases. N Engl J Med. 2024;390(13):1163-75. https://doi.org/10.1056/NEJMoa2313487
27. Madan V, Mamounas EP. Is sentinel lymph node biopsy necessary in patients who undergo prophylactic mastectomy? Clin Breast Cancer. 2023;23(2):231-6. https://doi.org/10.1016/j.clbc.2022.12.003
28. Wong SM, Ferroum A, Apostolova C, Alhassan B, Prakash I, Basik M, et al. Incidence of occult breast cancer in carriers of brca1/2 or other high-penetrance pathogenic variants undergoing prophylactic mastectomy: when is sentinel lymph node biopsy indicated? Ann Surg Oncol. 2022;29(11):6660-8. https://doi.org/10.1245/s10434-022-11916-3
29. Fat SC, Weed C, Samaha Y, Chung A, Boyle MK, Giuliano A, et al. Incidence of cancer and role of sentinel lymph node biopsy in BRCA mutation carriers undergoing prophylactic mastectomies. Am Surg. 2023;89(10):4066-71. https://doi.org/10.1177/00031348231175498
30. Davey MG, O'Flaherty C, Cleere EF, Nohilly A, Phelan J, Ronane E, et al. Sentinel lymph node biopsy in patients with ductal carcinoma in situ: systematic review and meta-analysis. BJS Open. 2022;6(2):zrac022. https://doi.org/10.1093/bjsopen/zrac022
31. Li X, Zhou C, Xu T, Ren Y, Li M, Shang J. Meta-analysis on axillary lymph node metastasis rate in ductal carcinoma in situ with microinvasion. Cancer Med. 2024;13(12):e7413. https://doi.org/10.1002/cam4.7413
32. Reimer T, Stachs A, Veselinovic K, Kühn T, Heil J, Polata S, et al. Axillary surgery in breast cancer – primary results of the INSEMA trial. N Engl J Med. 2025;392(11):1051-64. https://doi.org/10.1056/NEJMoa2412063
33. Astvatsaturyan K, Ramazyan A, Bose S. Is ultrasound-guided fine needle aspiration biopsy of axillary lymph nodes a viable alternative to sentinel lymph node biopsy? Diagn Cytopathol. 2021;49(10):1099-109. https://doi.org/10.1002/dc.24824
34. Sallout L, Tashkandi M, Moqnas A, AlMajed H, Al-Naeem A, Alwelaie Y. Fine- needle aspiration biopsy of axillary lymph nodes: a reliable diagnostic tool for breast cancer staging. Cancer Cytopathol. 2024;132(2):103-8. https://doi.org/10.1002/cncy.22770
35. Le-Petross HT, McCall LM, Hunt KK, Mittendorf EA, Ahrendt GM, Wilke LG, et al. Axillary ultrasound identifies residual nodal disease after chemotherapy: results from the American College of Surgeons Oncology Group Z1071 Trial (Alliance). AJR Am J Roentgenol. 2018;210(3):669-76. https://doi.org/10.2214/AJR.17.18295
36. Schwentner L, Helms G, Nekljudova V, Ataseven B, Bauerfeind I, Ditsch N, et al. Using ultrasound and palpation for predicting axillary lymph node status following neoadjuvant chemotherapy – results from the multi-center SENTINA trial. Breast. 2017;31:202-7. https://doi.org/10.1016/j.breast.2016.11.012
37. Morency D, Dumitra S, Parvez E, Martel K, Basik M, Robidoux A, et al. Axillary lymph node ultrasound following neoadjuvant chemotherapy in biopsy-proven node- positive breast cancer: results from the SN FNAC study. Ann Surg Oncol. 2019;26(13):4337-45. https://doi.org/10.1245/s10434-019-07809-7
38. Barron AU, Hoskin TL, Day CN, Hwang ES, Kuerer HM, Boughey JC, 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(12):1120-6. https://doi.org/10.1001/jamasurg.2018.2696
39. Montagna G, Laws A, Ferrucci M, Mrdutt MM, Sun SX, Bademler S, et al. Nodal burden and oncologic outcomes in patients with residual isolated tumor cells after neoadjuvant chemotherapy (ypN0i+): the OPBC-05/ICARO study. J Clin Oncol. 2025;43(7):810-20. https://doi.org/10.1200/JCO.24.01052
40. Topps AR, Barr SP, Pikoulas P, Pritchard SA, Maxwell AJ. Pre-operative axillary ultrasound-guided needle sampling in breast cancer: comparing the sensitivity of fine needle aspiration cytology and core needle biopsy. Ann Surg Oncol. 2018;25(1):148-53. https://doi.org/10.1245/s10434-017-6090-1
Downloads
Publicado
Como Citar
Edição
Seção
Licença
Copyright (c) 2026 Emmanuel Filizola Cavalcante, José Juvenal Linhares, Luciana Gomes da Rocha, Silvando Carmo de Oliveira, Fernando Daniel de Oliveira Mayorga, Valbert Oliveira Costa Filho, Luiz Gonzaga Porto Pinheiro, Filipe Nobre Chaves, Diane Isabelle Magno Cavalcante
Este trabalho está licenciado sob uma licença Creative Commons Attribution 4.0 International License.
