Abstract
Purpose
The findings from the American College of Surgeons Oncology Group (ACOSOG) Z0011 trial have questioned the use of axillary lymph node (ALN) dissection (ALND) in breast cancer patients with low ALN burden. In this study, our aim was to evaluate axillary nodal metastasis burden in patients with early-stage breast cancer who presented with metastatic lymph nodes diagnosed by fine needle aspiration biopsy (FNAB).
Methods
The data from 346 patients with cT1–T2 breast cancer who showed positive FNAB results and were seen at Tianjin Medical University Cancer Hospital from January 2014 to December 2017 were retrospectively analyzed. The patients were divided into high axillary nodal burden (≥ 3 positive lymph nodes) or low axillary nodal burden (one to two positive lymph nodes) groups. The clinical, radiological, and pathological features were compared between the two groups.
Results
From the 346 patients, 136 (39.3%) had low axillary nodal burden and 210 patients had high axillary nodal burden. Compared to patients with high metastatic burden, the patients with low metastatic burden were more likely to have two or fewer abnormal lymph nodes detected by AUS (95.6% vs. 65.3%, p < 0.05), and more likely to have HR−/HER2− lesions (15.4% vs. 5.2%, p < 0.05). Multivariate analysis revealed that patients with more than two abnormal lymph nodes had an odds ratio of 18.385 (95% CI 7.315–46.205, p < 0.05) to have axillary metastasis.
Conclusions
The presence of three or more abnormal lymph nodes on AUS was a significant indicator of high axillary nodal burden in early-stage breast cancer patients with positive FNAB findings. The combination of radiological and clinicopathological findings allows physicians to identify patients with high axillary nodal burden who will likely benefit from ALND in the post-ACOSOG Z0011 trial era.
Similar content being viewed by others
Abbreviations
- BCT:
-
Breast-conserving therapy
- ALN:
-
Axillary lymph node
- SLN:
-
Sentinel lymph node
- ALND:
-
Axillary lymph node dissection
- SLNB:
-
Sentinel lymph node biopsy
- NSLN:
-
Non-sentinel lymph node
- ROC:
-
Receiver-operator characteristic
- AUC:
-
Areas under the ROC curves
- ACOSOG:
-
American College of Surgeons Oncology Group
- AJCC:
-
American Joint Committee on Cancer
- ER:
-
Estrogen receptor
- PR:
-
Progesterone receptor
- HER2:
-
Human epidermal growth factor receptor-2
- AUS:
-
Axillary lymph node ultrasound
- IHC:
-
Immunohistochemistry
- FISH:
-
Fluorescence in situ hybridization
- CEP17:
-
Chromosome 17 centromere locus
- HE:
-
Hematoxylin–eosin
- PPV:
-
Positive predictive value
- NPV:
-
Negative predictive value
- OR:
-
Odds ratio
References
National Comprehensive Cancer Network. NCCN Clinical Practice Guidelines in Oncology: Breast Cancer (2018) https://www.nccn.org/professionals/physician_gls/default.aspx. Accessed 10 Nov 2018
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.
Cools-Lartigue J, Sinclair A, Trabulsi N, Meguerditchian A, Mesurolle B, Fuhrer R, et al. Preoperative axillary ultrasound and fine-needle aspiration biopsy in the diagnosis of axillary metastases in patients with breast cancer: predictors of accuracy and future implications. Ann Surg Oncol. 2013;20(3):819–27. https://doi.org/10.1245/s10434-012-2609-7.
del Riego J, Diaz-Ruiz MJ, Teixido M, Ribe J, Vilagran M, Canales L, et al. The impact of preoperative axillary ultrasonography in T1 breast tumours. Eur Radiol. 2016;26(4):1073–81. https://doi.org/10.1007/s00330-015-3901-2.
Farshid G, Kollias J, Grantley Gill P. The clinical utility of assessment of the axilla in women with suspicious screen detected breast lesions in the post Z0011 era. Breast Cancer Res Treat. 2015;151(2):347–55. https://doi.org/10.1007/s10549-015-3388-1.
Galimberti V, Cole BF, Zurrida S, Viale G, Luini A, Veronesi P, et al. Axillary dissection versus no axillary dissection in patients with sentinel-node micrometastases (IBCSG 23–01): a phase 3 randomised controlled trial. Lancet Oncol. 2013;14(4):297–305. https://doi.org/10.1016/S1470-2045(13)70035-4.
Giuliano AE, McCall L, Beitsch P, Whitworth PW, Blumencranz P, Leitch AM, et al. Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: the American College of Surgeons Oncology Group Z0011 randomized trial. Ann Surg. 2010;252(3):426–32. (discussion 32-3. doi:10.1097/SLA.0b013e3181f08f32)
Donker M, van Tienhoven G, Straver ME, Meijnen P, van de Velde CJ, Mansel RE, 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):1303–10. https://doi.org/10.1016/S1470-2045(14)70460-7.
Bilimoria KY, Bentrem DJ, Hansen NM, Bethke KP, Rademaker AW, Ko CY, et al. Comparison of sentinel lymph node biopsy alone and completion axillary lymph node dissection for node-positive breast cancer. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2009;27(18):2946–53. https://doi.org/10.1200/JCO.2008.19.5750.
Fant JS, Grant MD, Knox SM, Livingston SA, Ridl K, Jones RC, et al. Preliminary outcome analysis in patients with breast cancer and a positive sentinel lymph node who declined axillary dissection. Ann Surg Oncol. 2003;10(2):126–30.
Pilewskie M, Morrow M. Reply to "Implications of abnormal preoperative axillary imaging in the post Z011 era". Gland surgery. 2016;5(4):453–4. https://doi.org/10.21037/gs.2016.07.03.
Lim GH, Upadhyaya VS, Acosta HA, Lim JMA, Allen JC Jr, Leong LCH. 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(7):945–50. https://doi.org/10.1016/j.ejso.2018.04.003.
Hieken TJ, Trull BC, Boughey JC, Jones KN, Reynolds CA, Shah SS, et al. Preoperative axillary imaging with percutaneous lymph node biopsy is valuable in the contemporary management of patients with breast cancer. Surgery. 2013;154(4):831–8. (discussion 8-40. doi:10.1016/j.surg.2013.07.017).
Pilewskie M, Mautner SK, Stempel M, Eaton A, Morrow M. 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(4):1123–8. https://doi.org/10.1245/s10434-015-4944-y.
Zhu Y, Zhou W, Zhou JQ, Fei XC, Ye TJ, Huang O, et al. Axillary staging of early-stage invasive breast cancer by ultrasound-guided fine-needle aspiration cytology: which ultrasound criteria for classifying abnormal lymph nodes should be adopted in the post-ACOSOG Z0011 trial Era? J Ultrasound Med. 2016;35(5):885–93. https://doi.org/10.7863/ultra.15.06019.
Lowery AJ, Kell MR, Glynn RW, Kerin MJ, Sweeney KJ. Locoregional recurrence after breast cancer surgery: a systematic review by receptor phenotype. Breast Cancer Res Treat. 2012;133(3):831–41. https://doi.org/10.1007/s10549-011-1891-6.
Nguyen PL, Taghian AG, Katz MS, Niemierko A, Abi Raad RF, Boon WL, et al. Breast cancer subtype approximated by estrogen receptor, progesterone receptor, and HER-2 is associated with local and distant recurrence after breast-conserving therapy. J Clin Oncol. 2008;26(14):2373–8. https://doi.org/10.1200/JCO.2007.14.4287.
Dominici LS, Mittendorf EA, Wang X, Liu J, Kuerer HM, Hunt KK, et al. Implications of constructed biologic subtype and its relationship to locoregional recurrence following mastectomy. Breast Cancesr Res BCR. 2012;14(3):R82. https://doi.org/10.1186/bcr3197.
Voduc KD, Cheang MC, Tyldesley S, Gelmon K, Nielsen TO, Kennecke H. Breast cancer subtypes and the risk of local and regional relapse. J Clin Oncol. 2010;28(10):1684–91. https://doi.org/10.1200/JCO.2009.24.9284.
Holm-rasmussen EV, Jensen MB, Balslev E, et al. Reduced risk of axillary lymphatic spread in triple-negative breast cancer. Breast Cancer Res Treatment 2015, 149(1): 229–36. dio: 10.1007/s10549–014–3225-y
Freedman GM, Anderson PR, Li T, et al. Locoregional recurrence of triple-negative breast cancer after breast-conserving surgery and radiation. Cancer. 2009;115(5):946–51. https://doi.org/10.1002/cncr.24094.
Crabb SJ, Cheang MC, Leung S, et al. Basal breast cancer molecular subtype predicts for lower incidence of axillary lymph node metastases in primary breast cancer. Clinical Breast Cancer. 2008;8(3):249–56. https://doi.org/10.3816/cbc.2008.n.028.
Dent R, Hanna WM, Trudeau M, et al. Pattern of metastatic spread in triple-negative breast cancer. Breast Cancer Res Treat. 2009;115(2):423–8. https://doi.org/10.1007/s10549-008-0086-2.
Caudle AS, Kuerer HM, Le-Petross HT, Yang W, Yi M, Bedrosian I, et al. Predicting the extent of nodal disease in early-stage breast cancer. Ann Surg Oncol. 2014;21(11):3440–7. https://doi.org/10.1245/s10434-014-3813-4.
Morrow M, Van Zee KJ, Patil S, Petruolo O, Mamtani A, Barrio AV, et al. Axillary Dissection and Nodal Irradiation Can Be Avoided for Most Node-positive Z0011-eligible Breast Cancers: A Prospective Validation Study of 793 Patients. Ann Surg. 2017;266(3):457–62. https://doi.org/10.1097/SLA.0000000000002354.
Acknowledgements
The authors would like to acknowledge all the nurses in the breast cancer center for their services, along with the patients involved in this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest. All authors have approved the final version of this manuscript.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. This article does not contain any studies with animals performed by any of the author.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
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 22, 468–473 (2020). https://doi.org/10.1007/s12094-019-02162-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12094-019-02162-3