Research Article| Volume 47, ISSUE 8, P1907-1912, August 2021

Lost clips after targeted lymph node biopsy in breast cancer patients: Follow-up of the CLIP-study

Published:April 30, 2021DOI:



      Clipping and selective removal of axillary lymph nodes in breast cancer patients presenting with initially node-positive disease and achieving a nodal downstaging after primary systemic therapy is a less invasive method for axillary staging. An imaging guided localization and successful extirpation of these clipped lymph nodes is not possible in all patients. To date no follow-up data regarding patients with lost clips are available.

      Material and methods

      The oncological outcome of all participants of the CLIP-study and the results of postoperative axillary imaging in those patients with unproven clip resection are presented.


      A total of thirty patients were included into the pilot study. In ten of these patients (33%) the removal of the clipped axillary lymph node could not be verified by intraoperative radiograph. Postoperative imaging did not find lost clips in eight of these ten patients (80%). The lost clip was detected in two patients after surgery (20%), by mammography in one patient during routine follow-up and by computed tomography scan in one patient before radiotherapy. After a median follow-up of 40 months, 26 (87%) patients were still alive. Seven patients (23%) developed distant recurrent disease. No local or axillary recurrences were observed.


      Lost clips were detected by postoperative imaging only in a minority of patients. The impact of lost clips on axillary recurrences in breast cancer patients is still unclear and should be further clarified in larger, multicentric trials.


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        • Dominici L.S.
        • Negron Gonzalez V.M.
        • Buzdar A.U.
        • Lucci A.
        • Mittendorf E.A.
        • Le-Petross H.T.
        • et al.
        Cytologically proven axillary lymph node metastases are eradicated in patients receiving preoperative chemotherapy with concurrent trastuzumab for HER2-positive breast cancer.
        Cancer. 2010 Jun 15; 116: 2884-2889
        • Boughey J.C.
        • McCall L.M.
        • Ballman K.V.
        • Mittendorf E.A.
        • Ahrendt G.M.
        • Wilke L.G.
        • et al.
        Tumor biology correlates with rates of breast-conserving surgery and pathologic complete response after neoadjuvant chemotherapy for breast cancer: findings from the ACOSOG Z1071 (Alliance) prospective multicenter clinical trial.
        Ann Surg. 2014 Oct; 260: 608-614
        • Diego E.J.
        • McAuliffe P.F.
        • Soran A.
        • McGuire K.P.
        • Johnson R.R.
        • Bonaventura M.
        • et al.
        Axillary staging after neoadjuvant chemotherapy for breast cancer: a pilot study combining sentinel lymph node biopsy with radioactive seed localization of pre-treatment positive axillary lymph nodes.
        Ann Surg Oncol. 2016 May; 23: 1549-1553
        • Fleissig A.
        • Fallowfield L.J.
        • Langridge C.I.
        • Johnson L.
        • Newcombe R.G.
        • Dixon J.M.
        • et al.
        Post-operative arm morbidity and quality of life. Results of the ALMANAC randomised trial comparing sentinel node biopsy with standard axillary treatment in the management of patients with early breast cancer.
        Breast Canc Res Treat. 2006 Feb; 95: 279-293
        • Lucci A.
        • McCall L.M.
        • Beitsch P.D.
        • Whitworth P.W.
        • Reintgen D.S.
        • Blumencranz P.W.
        • et al.
        Surgical complications associated with sentinel lymph node dissection (SLND) plus axillary lymph node dissection compared with SLND alone in the American College of Surgeons Oncology Group Trial Z0011.
        J Clin Oncol. 2007 Aug 20; 25: 3657-3663
        • Simons J.M.
        • van Nijnatten T.J.A.
        • van der Pol C.C.
        • Luiten E.J.T.
        • Koppert L.B.
        • Smidt M.L.
        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 Mar; 269: 432-442
        • Caudle A.S.
        • Yang W.T.
        • Krishnamurthy S.
        • Mittendorf E.A.
        • Black D.M.
        • Gilcrease M.Z.
        • et al.
        Improved axillary evaluation following neoadjuvant chemotherapy for patients with node-positive breast cancer using selective evaluation of clipped nodes: implementation of targeted axillary dissection.
        J Clin Oncol. 2016 Apr 1; 34: 1072-1078
        • 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: 1307-1311
      1. Kuemmel S, Heil J, Rueland A, Seiberling C, Harrach H, Schindowski D 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. DOI: 10.1097/SLA.0000000000004572.

        • Ditsch N.
        • Untch M.
        • Kolberg-Liedtke C.
        • Jackisch C.
        • Krug D.
        • Friedrich M.
        • et al.
        AGO recommendations for the diagnosis and treatment of patients with locally advanced and metastatic breast cancer: update 2020.
        Breast Care. 2020 Jun; 15: 294-309
        • National Comprehensive Cancer Network [Internet]
        NCCN clinical practice guidelines in Oncology, breast cancer. Version 1.2021.
        (Available from)
        • Banys-Paluchowski M.
        • Gruber I.V.
        • Hartkopf A.
        • Paluchowski P.
        • Krawczyk N.
        • Marx M.
        • et al.
        Axillary ultrasound for prediction of response to neoadjuvant therapy in the context of surgical strategies to axillary dissection in primary breast cancer: a systematic review of the current literature.
        Arch Gynecol Obstet. 2020 Feb; 301: 341-353
        • Piltin M.A.
        • Hoskin T.L.
        • Day C.N.
        • Davis Jr., J.
        • Boughey J.C.
        Oncologic outcomes of sentinel lymph node surgery after neoadjuvant chemotherapy for node-positive breast cancer.
        Ann Surg Oncol. 2020 Nov; 27: 4795-4801
        • Kahler-Ribeiro-Fontana S.
        • Pagan E.
        • Magnoni F.
        • Vicini E.
        • Morigi C.
        • Corso G.
        • 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. 2020 Oct; S0748–7983 (30846-5)
        • Wong S.M.
        • Almana N.
        • Choi J.
        • Hu J.
        • Gagnon H.
        • Natsuhara K.
        • et al.
        Prognostic significance of residual axillary nodal micrometastases and isolated tumor cells after neoadjuvant chemotherapy for breast cancer.
        Ann Surg Oncol. 2019 Oct; 26: 3502-3509
        • von Minckwitz G.
        • Huang C.S.
        • Mano M.S.
        • Loibl S.
        • Mamounas E.P.
        • Untch M.
        • et al.
        Trastuzumab emtansine for residual invasive HER2-positive breast cancer.
        N Engl J Med. 2019 Feb; 380: 617-628
        • Masuda N.
        • Lee S.J.
        • Ohtani S.
        • Im Y.H.
        • Lee E.S.
        • Yokota I.
        • et al.
        Adjuvant capecitabine for breast cancer after preoperative chemotherapy.
        N Engl J Med. 2017 Jun; 376: 2147-2159
        • [Internet]
        Minimal invasive axillary staging and treatment after neoadjuvant systemic therapy in node positive breast cancer (MINIMAX).
        (Available from)
        • [Internet]
        AXillary surgery after NeoAdjuvant treatment (AXSANA).
        (Available from)