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Published in: EJNMMI Research 1/2019

Open Access 01-12-2019 | Ultrasound | Original research

Feasibility of radioguided occult lesion localization of clip-marked lymph nodes for tailored axillary treatment in breast cancer patients treated with neoadjuvant systemic therapy

Authors: Daan Hellingman, Maarten L. Donswijk, Gonneke A. O. Winter-Warnars, Petra de Koekkoek-Doll, Marilyn Pinas, Yvonne Budde-van Namen, Johan Westerga, Marie-Jeanne T. F. D. Vrancken Peeters, Nikola Kimmings, Marcel P. M. Stokkel

Published in: EJNMMI Research | Issue 1/2019

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Abstract

Background

Selective removal of initially tumor-positive axillary lymph nodes in breast cancer patients who underwent neoadjuvant systemic treatment (NST) improves the accuracy of nodal staging and provides the opportunity for more tailored axillary treatment. This study evaluated whether radioguided occult lesion localization (ROLL) of clip-marked lymph nodes is feasible in clinical practice.

Methods

Prior to NST, a clip marker was placed inside a proven tumor-positive lymph node in all breast cancer patients (cTis-4N1-3 M0). After NST, technetium-99m-labeled macroaggregated albumin was injected in the clip-marked lymph nodes. The next day, these ROLL-marked nodes were selectively removed at surgery to evaluate the pathological response of the axilla.

Results

Thirty-seven patients (38 axillae) underwent clip insertion. After NST, the clip was visible by ultrasound in 36 procedures (95%). In the other two patients, the ROLL-node injection was performed in a sonographically suspicious unclipped node (1), and near the clip under computed tomography guidance (1). Initial surgery successfully identified the ROLL-marked node with clip in 33 procedures (87%). Removed specimens in the other five procedures contained only the sonographically suspicious tumor-positive unclipped node (1), a node with signs of complete response but no clip (2), a clip without node (1), and tissue without node nor clip, and a second successful ROLL-node procedure was performed (1). Overall, 10 ROLL-marked nodes had no residual disease.

Conclusions

This study demonstrates that the ROLL procedure to identify clip-marked lymph nodes is feasible. This facilitates selective removal at surgery and may tailor axillary treatment in patients treated with NST.
Literature
1.
go back to reference Ataseven B, von Minckwitz G. The impact of neoadjuvant treatment on surgical options and outcomes. Ann Surg Oncol. 2016;23:3093–9.CrossRef Ataseven B, von Minckwitz G. The impact of neoadjuvant treatment on surgical options and outcomes. Ann Surg Oncol. 2016;23:3093–9.CrossRef
2.
go back to reference Rouzier R, Extra J-M, Klijanienko J, Falcou M-C, Asselain B, Vincent-Salomon A, et al. Incidence and prognostic significance of complete axillary downstaging after primary chemotherapy in breast cancer patients with T1 to T3 tumors and cytologically proven axillary metastatic lymph nodes. J Clin Oncol. 2002;20:1304–10.CrossRef Rouzier R, Extra J-M, Klijanienko J, Falcou M-C, Asselain B, Vincent-Salomon A, et al. Incidence and prognostic significance of complete axillary downstaging after primary chemotherapy in breast cancer patients with T1 to T3 tumors and cytologically proven axillary metastatic lymph nodes. J Clin Oncol. 2002;20:1304–10.CrossRef
3.
go back to reference Galimberti V, Ribeiro Fontana SK, Maisonneuve P, Steccanella F, Vento AR, Intra M, et al. Sentinel node biopsy after neoadjuvant treatment in breast cancer: five-year follow-up of patients with clinically node-negative or node-positive disease before treatment. Eur J Surg Oncol. 2016;42:361–8.CrossRef Galimberti V, Ribeiro Fontana SK, Maisonneuve P, Steccanella F, Vento AR, Intra M, et al. Sentinel node biopsy after neoadjuvant treatment in breast cancer: five-year follow-up of patients with clinically node-negative or node-positive disease before treatment. Eur J Surg Oncol. 2016;42:361–8.CrossRef
4.
go back to reference Diego EJ, McAuliffe PF, Soran A, McGuire KP, Johnson RR, 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;23:1549–53.CrossRef Diego EJ, McAuliffe PF, Soran A, McGuire KP, Johnson RR, 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;23:1549–53.CrossRef
5.
go back to reference Dominici LS, Negron Gonzalez VM, Buzdar AU, Lucci A, Mittendorf EA, Le-Petross HT, 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;116:2884–9.CrossRef Dominici LS, Negron Gonzalez VM, Buzdar AU, Lucci A, Mittendorf EA, Le-Petross HT, 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;116:2884–9.CrossRef
6.
go back to reference Boughey JC, McCall LM, Ballman KV, Mittendorf EA, Ahrendt GM, Wilke LG, 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;260:606–8.CrossRef Boughey JC, McCall LM, Ballman KV, Mittendorf EA, Ahrendt GM, Wilke LG, 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;260:606–8.CrossRef
7.
go back to reference Lyman GH, Somerfield MR, Bosserman LD, Perkins CL, Weaver DL, Giuliano AE. Sentinel lymph node biopsy for patients with early-stage breast cancer: American Society of Clinical Oncology Clinical Practice Guideline Update. J Clin Oncol. 2016;35:561–4.CrossRef Lyman GH, Somerfield MR, Bosserman LD, Perkins CL, Weaver DL, Giuliano AE. Sentinel lymph node biopsy for patients with early-stage breast cancer: American Society of Clinical Oncology Clinical Practice Guideline Update. J Clin Oncol. 2016;35:561–4.CrossRef
8.
go back to reference Boughey JC, Suman VJ, Mittendorf EA, Ahrendt GM, Wilke LG, Taback B, et al. Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial. JAMA. 2013;310:1455–61.CrossRef Boughey JC, Suman VJ, Mittendorf EA, Ahrendt GM, Wilke LG, Taback B, et al. Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial. JAMA. 2013;310:1455–61.CrossRef
9.
go back to reference Kuehn T, Bauerfeind I, Fehm T, Fleige B, Hausschild M, Helms G, 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;14:609–18.CrossRef Kuehn T, Bauerfeind I, Fehm T, Fleige B, Hausschild M, Helms G, 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;14:609–18.CrossRef
10.
go back to reference Boileau J-F, Poirier B, Basik M, Holloway CMB, Gaboury L, Sideris L, et al. Sentinel node biopsy after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: the SN FNAC study. J Clin Oncol. 2015;33:258–64.CrossRef Boileau J-F, Poirier B, Basik M, Holloway CMB, Gaboury L, Sideris L, et al. Sentinel node biopsy after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: the SN FNAC study. J Clin Oncol. 2015;33:258–64.CrossRef
11.
go back to reference Caudle AS, Yang WT, Krishnamurthy S, Mittendorf EA, Black DM, Gilcrease MZ, 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;34:1072–8.CrossRef Caudle AS, Yang WT, Krishnamurthy S, Mittendorf EA, Black DM, Gilcrease MZ, 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;34:1072–8.CrossRef
12.
go back to reference Straver ME, Loo CE, Alderliesten T, Rutgers EJT, Vrancken Peeters MTFD. 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. 2010;97:1226–31.CrossRef Straver ME, Loo CE, Alderliesten T, Rutgers EJT, Vrancken Peeters MTFD. 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. 2010;97:1226–31.CrossRef
13.
go back to reference Donker M, Straver ME, Wesseling J, Loo CE, Schot M, Drukker CA, et al. Marking axillary lymph nodes with radioactive iodine seeds for axillary staging after neoadjuvant systemic treatment in breast cancer patients: the MARI procedure. Ann Surg. 2015;261:378–82.CrossRef Donker M, Straver ME, Wesseling J, Loo CE, Schot M, Drukker CA, et al. Marking axillary lymph nodes with radioactive iodine seeds for axillary staging after neoadjuvant systemic treatment in breast cancer patients: the MARI procedure. Ann Surg. 2015;261:378–82.CrossRef
14.
go back to reference Janssen NNY, Nijkamp J, Alderliesten T, Loo CE, Rutgers EJT, Sonke J-J, et al. Radioactive seed localization in breast cancer treatment. Br J Surg. 2016;103:70–80.CrossRef Janssen NNY, Nijkamp J, Alderliesten T, Loo CE, Rutgers EJT, Sonke J-J, et al. Radioactive seed localization in breast cancer treatment. Br J Surg. 2016;103:70–80.CrossRef
15.
go back to reference Pavlicek W, Walton HA, Karstaedt PJ, Gray RJ. Radiation safety with use of I-125 seeds for localization of nonpalpable breast lesions. Acad Radiol. 2006;13:909–15.CrossRef Pavlicek W, Walton HA, Karstaedt PJ, Gray RJ. Radiation safety with use of I-125 seeds for localization of nonpalpable breast lesions. Acad Radiol. 2006;13:909–15.CrossRef
16.
go back to reference Goudreau SH, Joseph JP, Seiler SJ. Preoperative radioactive seed localization for nonpalpable breast lesions: technique, pitfalls, and solutions. Radiographics. 2015;35:1319–34.CrossRef Goudreau SH, Joseph JP, Seiler SJ. Preoperative radioactive seed localization for nonpalpable breast lesions: technique, pitfalls, and solutions. Radiographics. 2015;35:1319–34.CrossRef
17.
go back to reference Aydogan F, Ozben V, Atasoy D, Yilmaz MH, Halac M, Celik V. Excision of axillary lymph node recurrences in breast cancer patients with axillary ROLL (A-ROLL). J Surg Oncol. 2010;101:141–4.PubMed Aydogan F, Ozben V, Atasoy D, Yilmaz MH, Halac M, Celik V. Excision of axillary lymph node recurrences in breast cancer patients with axillary ROLL (A-ROLL). J Surg Oncol. 2010;101:141–4.PubMed
18.
go back to reference Ozben V, Aydogan F, Atasoy D, Ferahman M, Yilmaz MH, Esen G, et al. Radio-guided lymph node biopsy for the diagnosis of axillary lymphadenopathy. Nucl Med Commun. 2011;32:233–7.CrossRef Ozben V, Aydogan F, Atasoy D, Ferahman M, Yilmaz MH, Esen G, et al. Radio-guided lymph node biopsy for the diagnosis of axillary lymphadenopathy. Nucl Med Commun. 2011;32:233–7.CrossRef
19.
go back to reference Koolen BB, Donker M, Straver ME, van der Noordaa MEM, Rutgers EJT, Valdes Olmos RA, et al. Combined PET-CT and axillary lymph node marking with radioactive iodine seeds (MARI procedure) for tailored axillary treatment in node-positive breast cancer after neoadjuvant therapy. Br J Surg. 2017;104:1188–96.CrossRef Koolen BB, Donker M, Straver ME, van der Noordaa MEM, Rutgers EJT, Valdes Olmos RA, et al. Combined PET-CT and axillary lymph node marking with radioactive iodine seeds (MARI procedure) for tailored axillary treatment in node-positive breast cancer after neoadjuvant therapy. Br J Surg. 2017;104:1188–96.CrossRef
20.
go back to reference van der Noordaa MEM, van Duijnhoven FH, Straver ME, Groen EJ, Stokkel M, Loo CE, et al. Major reduction in axillary lymph node dissections after neoadjuvant systemic therapy for node-positive breast cancer by combining PET/CT and the MARI procedure. Ann Surg Oncol. 2018;25:1512–20.CrossRef van der Noordaa MEM, van Duijnhoven FH, Straver ME, Groen EJ, Stokkel M, Loo CE, et al. Major reduction in axillary lymph node dissections after neoadjuvant systemic therapy for node-positive breast cancer by combining PET/CT and the MARI procedure. Ann Surg Oncol. 2018;25:1512–20.CrossRef
21.
go back to reference Choy N, Lipson J, Porter C, Ozawa M, Kieryn A, Pal S, et al. Initial results with preoperative tattooing of biopsied axillary lymph nodes and correlation to sentinel lymph nodes in breast cancer patients. Ann Surg Oncol. 2015;22:377–82.CrossRef Choy N, Lipson J, Porter C, Ozawa M, Kieryn A, Pal S, et al. Initial results with preoperative tattooing of biopsied axillary lymph nodes and correlation to sentinel lymph nodes in breast cancer patients. Ann Surg Oncol. 2015;22:377–82.CrossRef
22.
go back to reference Ong JSL, Teh J, Saunders C, Bourke AG, Lizama C, Newton J, et al. Patient satisfaction with Radioguided Occult Lesion Localisation using iodine-125 seeds (‘ROLLIS’) versus conventional hookwire localisation. Eur J Surg Oncol. 2017;43:2261–9.CrossRef Ong JSL, Teh J, Saunders C, Bourke AG, Lizama C, Newton J, et al. Patient satisfaction with Radioguided Occult Lesion Localisation using iodine-125 seeds (‘ROLLIS’) versus conventional hookwire localisation. Eur J Surg Oncol. 2017;43:2261–9.CrossRef
23.
go back to reference Siso C, de Torres J, Esgueva-Colmenarejo A, Espinosa-Bravo M, Rus N, Cordoba O, et al. Intraoperative ultrasound-guided excision of axillary clip in patients with node-positive breast cancer treated with neoadjuvant therapy ( ILINA Trial ) a new tool to guide the excision of the clipped node after neoadjuvant treatment. Ann Surg Oncol. 2018;25:784–91.CrossRef Siso C, de Torres J, Esgueva-Colmenarejo A, Espinosa-Bravo M, Rus N, Cordoba O, et al. Intraoperative ultrasound-guided excision of axillary clip in patients with node-positive breast cancer treated with neoadjuvant therapy ( ILINA Trial ) a new tool to guide the excision of the clipped node after neoadjuvant treatment. Ann Surg Oncol. 2018;25:784–91.CrossRef
24.
go back to reference Dashevsky BZ, Altman A, Abe H, Jaskowiak N, Bao J, Schacht DV, et al. Lymph node wire localization post-chemotherapy: towards improving the false negative sentinel lymph node biopsy rate in breast cancer patients. Clin Imaging. 2018;48:69–73.CrossRef Dashevsky BZ, Altman A, Abe H, Jaskowiak N, Bao J, Schacht DV, et al. Lymph node wire localization post-chemotherapy: towards improving the false negative sentinel lymph node biopsy rate in breast cancer patients. Clin Imaging. 2018;48:69–73.CrossRef
25.
go back to reference 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;44:1307–11.CrossRef 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;44:1307–11.CrossRef
26.
go back to reference Nguyen TT, Hieken TJ, Glazebrook KN, Boughey JC. Localizing the clipped node in patients with node-positive breast cancer treated with neoadjuvant chemotherapy: early learning experience and challenges. Ann Surg Oncol. 2017;24:3011–6.CrossRef Nguyen TT, Hieken TJ, Glazebrook KN, Boughey JC. Localizing the clipped node in patients with node-positive breast cancer treated with neoadjuvant chemotherapy: early learning experience and challenges. Ann Surg Oncol. 2017;24:3011–6.CrossRef
27.
go back to reference Kim EY, Byon WS, Lee KH, Yun J-S, Park YL, Park CH, et al. Feasibility of preoperative axillary lymph node marking with a clip in breast cancer patients before neoadjuvant chemotherapy: a preliminary study. World J Surg. 2018;42:582–9.CrossRef Kim EY, Byon WS, Lee KH, Yun J-S, Park YL, Park CH, et al. Feasibility of preoperative axillary lymph node marking with a clip in breast cancer patients before neoadjuvant chemotherapy: a preliminary study. World J Surg. 2018;42:582–9.CrossRef
28.
go back to reference 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;22:4241–6.CrossRef 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;22:4241–6.CrossRef
Metadata
Title
Feasibility of radioguided occult lesion localization of clip-marked lymph nodes for tailored axillary treatment in breast cancer patients treated with neoadjuvant systemic therapy
Authors
Daan Hellingman
Maarten L. Donswijk
Gonneke A. O. Winter-Warnars
Petra de Koekkoek-Doll
Marilyn Pinas
Yvonne Budde-van Namen
Johan Westerga
Marie-Jeanne T. F. D. Vrancken Peeters
Nikola Kimmings
Marcel P. M. Stokkel
Publication date
01-12-2019
Publisher
Springer Berlin Heidelberg
Published in
EJNMMI Research / Issue 1/2019
Electronic ISSN: 2191-219X
DOI
https://doi.org/10.1186/s13550-019-0560-3

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