World Journal of Surgery

, Volume 42, Issue 2, pp 582–589 | Cite as

Feasibility of Preoperative Axillary Lymph Node Marking with a Clip in Breast Cancer Patients Before Neoadjuvant Chemotherapy: A Preliminary Study

  • Eun Young Kim
  • Woo Seok Byon
  • Kwan Ho Lee
  • Ji-Sup Yun
  • Yong Lai Park
  • Chan Heun ParkEmail author
  • In Young Youn
  • Seon Hyeong Choi
  • Yoon Jung Choi
  • Shin Ho KookEmail author
  • Sung-Im Do
Original Scientific Report



The aim of this study was to determine the feasibility of image-guided marker-clip placement in axillary lymph nodes (ALNs) for breast cancer upon initial presentation and to assess the reliability of this method with sentinel lymph node biopsy (SLNB) for axillary restaging after neoadjuvant chemotherapy (NAC).


Between June 2015 and August 2016, a marker clip was placed at a clinically positive ALN under ultrasonography (US) guidance before initiation of NAC in 20 patients. Preoperative localization of marker-clipped LNs was performed, and the localized LNs were removed by SLNB. We compared the postoperative results of the marker-clipped LNs, SLNs and ALNs.


Image-guided marker-clip placements and localization of marker-clipped LNs were performed successfully in 20 patients. A total of 24 marker clips were inserted, and 23 marker-clipped LNs were successfully retrieved during surgery (identification rate, 23/24, 95.8%). In the 11 patients with pathologically confirmed metastatic marker-clipped LNs, four became negative after NAC, and seven maintained metastatic residues on the marker-clipped LNs. Three of the seven patients had metastatic residues on the ALNs, and two of the three patients also had negative SLNs. Marker-clipped nodes accurately predicted the axillary nodal status in these two patients compared with SLNs alone.


Image-guided marker-clip placement on positive ALNs before NAC and removal with SLNB is technically feasible. This technique can improve the accuracy of the residual disease evaluation on the axilla, especially in patients with negative SLNB results, and can identify candidates for limited axillary surgery after NAC.



This work was supported by a Samsung Biomedical Research Institute (SBRI) grant.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare. This manuscript has not been published elsewhere.


  1. 1.
    Fisher B, Brown A, Mamounas E et al (1997) Effect of preoperative chemotherapy on local-regional disease in women with operable breast cancer: findings from national surgical adjuvant breast and bowel project B-18. J Clin Oncol 15:2483–2493CrossRefPubMedGoogle Scholar
  2. 2.
    Kuerer HM, Sahin AA, Hunt KK et al (1999) Incidence and impact of documented eradication of breast cancer axillary lymph node metastases before surgery in patients treated with neoadjuvant chemotherapy. Ann Surg 230:72–78CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Fu JF, Chen HL, Yang J et al (2014) Feasibility and accuracy of sentinel lymph node biopsy in clinically node-positive breast cancer after neoadjuvant chemotherapy: a meta-analysis. PLoS ONE 9:e105316CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Mamounas EP, Brown A, Anderson S et al (2005) Sentinel node biopsy after neoadjuvant chemotherapy in breast cancer: results from national surgical adjuvant breast and bowel project protocol B-27. J Clin Oncol 23:2694–2702CrossRefPubMedGoogle Scholar
  5. 5.
    Shen J, Gilcrease MZ, Babiera GV et al (2007) Feasibility and accuracy of sentinel lymph node biopsy after preoperative chemotherapy in breast cancer patients with documented axillary metastases. Cancer 109:1255–1263CrossRefPubMedGoogle Scholar
  6. 6.
    Hieken TJ, Boughey JC, Jones KN et al (2013) Imaging response and residual metastatic axillary lymph node disease after neoadjuvant chemotherapy for primary breast cancer. Ann Surg Oncol 20:3199–3204CrossRefPubMedGoogle Scholar
  7. 7.
    Straver ME, Loo CE, Alderliesten T et al (2010) 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 97:1226–1231CrossRefPubMedGoogle Scholar
  8. 8.
    Boughey JC, Suman VJ, Mittendorf EA et al (2013) Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial. JAMA 310:1455–1461CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Boileau JF, Poirier B, Basik M et al (2015) Sentinel node biopsy after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: the SN FNAC study. J Clin Oncol 33:258–264CrossRefPubMedGoogle Scholar
  10. 10.
    Kuehn T, Bauerfeind I, Fehm T et al (2013) Sentinel-lymph-node biopsy in patients with breast cancer before and after neoadjuvant chemotherapy (SENTINA): a prospective, multicentre cohort study. Lancet Oncol 14:609–618CrossRefPubMedGoogle Scholar
  11. 11.
    Boughey JC, Ballman KV, Le-Petross HT et al (2016) 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 263:802–807CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    National Comprehensive Cancer Network NCCN (2016) Clinical practice guidelines in oncology, version 2. National Comprehensive Cancer, Network, WashingtonGoogle Scholar
  13. 13.
    Youn I, Choi SH, Kook SH et al (2015) Ultrasonography-guided surgical clip placement for tumor localization in patients undergoing neoadjuvant chemotherapy for breast cancer. J Breast Cancer 18:44–49CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Giuliano AE, Hunt KK, Ballman KV et al (2011) Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA 305:569–575CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Edge SB, Compton CC (2010) The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol 17:1471–1474CrossRefPubMedGoogle Scholar
  16. 16.
    Sinn HP, Schmid H, Junkermann H et al (1994) Histologic regression of breast cancer after primary (neoadjuvant) chemotherapy. Geburtshilfe Frauenheilkd 54:552–558CrossRefPubMedGoogle Scholar
  17. 17.
    Xing Y, Foy M, Cox DD et al (2006) Meta-analysis of sentinel lymph node biopsy after preoperative chemotherapy in patients with breast cancer. Br J Surg 93:539–546CrossRefPubMedGoogle Scholar
  18. 18.
    Pilewskie M, Morrow M (2017) Axillary nodal management following neoadjuvant chemotherapy: a review. JAMA Oncol 3:549–555CrossRefPubMedGoogle Scholar
  19. 19.
    El Hage Chehade H, Headon H, Kasem A et al (2016) Refining the performance of sentinel lymph node biopsy post-neoadjuvant chemotherapy in patients with pathologically proven pre-treatment node-positive breast cancer: an update for clinical practice. Anticancer Res 36:1461–1471Google Scholar
  20. 20.
    Hennessy BT, Hortobagyi GN, Rouzier R et al (2005) Outcome after pathologic complete eradication of cytologically proven breast cancer axillary node metastases following primary chemotherapy. J Clin Oncol 23:9304–9311CrossRefPubMedGoogle Scholar
  21. 21.
    Enokido K, Watanabe C, Nakamura S et al (2016) Sentinel lymph node biopsy after neoadjuvant chemotherapy in patients with an initial diagnosis of cytology-proven lymph node-positive breast cancer. Clin Breast Cancer 16:299–304CrossRefPubMedGoogle Scholar
  22. 22.
    Donker M, Straver ME, Wesseling J et al (2015) Marking axillary lymph nodes with radioactive iodine seeds for axillary staging after neoadjuvant systemic treatment in breast cancer patients: the MARI procedure. Ann Surg 261:378–382CrossRefPubMedGoogle Scholar
  23. 23.
    Patten DK, Zacharioudakis KE, Chauhan H et al (2015) Sentinel lymph node biopsy after neo-adjuvant chemotherapy in patients with breast cancer: are the current false negative rates acceptable? Breast 24:318–320CrossRefPubMedGoogle Scholar
  24. 24.
    Caudle AS, Yang WT, Krishnamurthy S et al (2016) 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 34:1072–1078CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Coates AS, Winer EP, Goldhirsch A et al (2015) Tailoring therapies–improving the management of early breast cancer: st Gallen international expert consensus on the primary therapy of early breast cancer 2015. Ann Oncol 26:1533–1546CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    ICRP (2007) The 2007 recommendations of the international commission on radiological protection. ICRP publication 103. Ann ICRP 37:1–332Google Scholar

Copyright information

© Société Internationale de Chirurgie 2017

Authors and Affiliations

  • Eun Young Kim
    • 1
  • Woo Seok Byon
    • 1
  • Kwan Ho Lee
    • 1
  • Ji-Sup Yun
    • 1
  • Yong Lai Park
    • 1
  • Chan Heun Park
    • 1
    Email author
  • In Young Youn
    • 2
  • Seon Hyeong Choi
    • 2
  • Yoon Jung Choi
    • 2
  • Shin Ho Kook
    • 2
    Email author
  • Sung-Im Do
    • 3
  1. 1.Department of SurgeryKangbuk Samsung Hospital, Sungkyunkwan University School of MedicineJongno-GuRepublic of Korea
  2. 2.Department of RadiologyKangbuk Samsung Hospital, Sungkyunkwan University School of MedicineJongno-GuRepublic of Korea
  3. 3.Department of PathologyKangbuk Samsung Hospital, Sungkyunkwan University School of MedicineJongno-GuRepublic of Korea

Personalised recommendations