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Published in: Annals of Surgical Oncology 8/2019

01-08-2019 | Breast Cancer | Breast Oncology

The Sentinel Lymph Node Biopsy Using Indocyanine Green Fluorescence Plus Radioisotope Method Compared With the Radioisotope-Only Method for Breast Cancer Patients After Neoadjuvant Chemotherapy: A Prospective, Randomized, Open-Label, Single-Center Phase 2 Trial

Authors: So-Youn Jung, MD, PhD, Jai Hong Han, MD, Soo Jin Park, MD, Eun-Gyeong Lee, MD, Joohwa Kwak, MD, Sun Hye Kim, MD, Moo Hyun Lee, MD, PhD, Eun Sook Lee, MD, PhD, Han-Sung Kang, MD, PhD, Keun Seok Lee, MD, PhD, In Hae Park, MD, PhD, Sung Hoon Sim, MD, PhD, Hae Jeong Jeong, MD, PhD, Youngmee Kwon, MD, PhD, Dong-Eun Lee, MS, Seok-Ki Kim, MD, PhD, Seeyoun Lee, MD, PhD

Published in: Annals of Surgical Oncology | Issue 8/2019

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Abstract

Background

This study aimed to compare the sentinel lymph node (SLN) identification rates for breast cancer patients after neoadjuvant chemotherapy (NAC) between the dual method (DM) of indocyanine green fluorescence (ICG-F) plus a radioisotope (RI) and RI alone.

Methods

This randomized study enrolled 130 patients who received NAC for breast cancer and 122 patients who received SLN biopsy (SLNB) using either DM (n = 58) or RI only (n = 64). The study compared the identification rate, number of SLNs, and detection time of SLNB.

Results

Among the 122 patients, 113 (92.6%) were clinically node-positive before NAC. The SLN identification rate was 98.3% in the DM group and 93.8% in the RI group (p = 0.14). The DM group and the RI group were similar in the average number of SLNs (2.2 ± 1.13 vs. 1.9 ± 1.33; p = 0.26) and the time to detection of the first SLN (8.7 ± 4.98 vs. 8.3 ± 4.31 min; p = 0.30). In the DM group, transcutaneous lymphatic drainage was visualized by fluorescence imaging for 65.5% (38 of 58) of the patients. The SLN identification rate was 94.7% using ICG-F and 93% using RI (p = 0.79). During and after the operation, no complications, including allergic reactions or skin necrosis, occurred.

Conclusions

This study is the first randomized trial to use ICG-F for SLNB in breast cancer patients after NAC. The DM including ICG-F could be a feasible and safe method for SLNB in initially node-positive breast cancer patients with NAC.
Literature
1.
go back to reference Kuerer HM, Sahin AA, Hunt KK, et al. Incidence and impact of documented eradication of breast cancer axillary lymph node metastases before surgery in patients treated with neoadjuvant chemotherapy. Ann Surg. 1999;230:72–8.CrossRefPubMedPubMedCentral Kuerer HM, Sahin AA, Hunt KK, et al. Incidence and impact of documented eradication of breast cancer axillary lymph node metastases before surgery in patients treated with neoadjuvant chemotherapy. Ann Surg. 1999;230:72–8.CrossRefPubMedPubMedCentral
2.
go back to reference Buzdar AU, Ibrahim NK, Francis D, et al. Significantly higher pathologic complete remission rate after neoadjuvant therapy with trastuzumab, paclitaxel, and epirubicin chemotherapy: results of a randomized trial in human epidermal growth factor receptor 2-positive operable breast cancer. J Clin Oncol. 2005;23:3676–85.CrossRefPubMed Buzdar AU, Ibrahim NK, Francis D, et al. Significantly higher pathologic complete remission rate after neoadjuvant therapy with trastuzumab, paclitaxel, and epirubicin chemotherapy: results of a randomized trial in human epidermal growth factor receptor 2-positive operable breast cancer. J Clin Oncol. 2005;23:3676–85.CrossRefPubMed
3.
go back to reference Hennessy BT, Hortobagyi GN, Rouzier R, et al. Outcome after pathologic complete eradication of cytologically proven breast cancer axillary node metastases following primary chemotherapy. J Clin Oncol. 2005;23:9304–11.CrossRefPubMed Hennessy BT, Hortobagyi GN, Rouzier R, et al. Outcome after pathologic complete eradication of cytologically proven breast cancer axillary node metastases following primary chemotherapy. J Clin Oncol. 2005;23:9304–11.CrossRefPubMed
4.
go back to reference Fisher B, Brown A, Mamounas E, et al. 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. 1997;15:2483–93.CrossRefPubMed Fisher B, Brown A, Mamounas E, et al. 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. 1997;15:2483–93.CrossRefPubMed
5.
go back to reference Dominici LS, Negron Gonzalez VM, Buzdar AU, 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.CrossRefPubMed Dominici LS, Negron Gonzalez VM, Buzdar AU, 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.CrossRefPubMed
6.
go back to reference Boughey JC, Suman VJ, Mittendorf EA, 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.CrossRefPubMedPubMedCentral Boughey JC, Suman VJ, Mittendorf EA, 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.CrossRefPubMedPubMedCentral
7.
go back to reference Kang YJ, Han W, Park S, et al. Outcome following sentinel lymph node biopsy-guided decisions in breast cancer patients with conversion from positive to negative axillary lymph nodes after neoadjuvant chemotherapy. Breast Cancer Res Treat. 2017;166:473–80.CrossRefPubMed Kang YJ, Han W, Park S, et al. Outcome following sentinel lymph node biopsy-guided decisions in breast cancer patients with conversion from positive to negative axillary lymph nodes after neoadjuvant chemotherapy. Breast Cancer Res Treat. 2017;166:473–80.CrossRefPubMed
8.
go back to reference Kelly AM, Dwamena B, Cronin P, Carlos RC. Breast cancer sentinel node identification and classification after neoadjuvant chemotherapy-systematic review and meta analysis. Acad Radiol. 2009;16:551–63.CrossRefPubMed Kelly AM, Dwamena B, Cronin P, Carlos RC. Breast cancer sentinel node identification and classification after neoadjuvant chemotherapy-systematic review and meta analysis. Acad Radiol. 2009;16:551–63.CrossRefPubMed
9.
go back to reference van Deurzen CH, Vriens BE, Tjan-Heijnen VC, et al. Accuracy of sentinel node biopsy after neoadjuvant chemotherapy in breast cancer patients: a systematic review. Eur J Cancer. 2009;45:3124–30.CrossRefPubMed van Deurzen CH, Vriens BE, Tjan-Heijnen VC, et al. Accuracy of sentinel node biopsy after neoadjuvant chemotherapy in breast cancer patients: a systematic review. Eur J Cancer. 2009;45:3124–30.CrossRefPubMed
10.
go back to reference Kuehn T, Bauerfeind I, Fehm T, 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.CrossRefPubMed Kuehn T, Bauerfeind I, Fehm T, 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.CrossRefPubMed
11.
go back to reference Boileau JF, Poirier B, Basik M, 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.CrossRefPubMed Boileau JF, Poirier B, Basik M, 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.CrossRefPubMed
12.
go back to reference Krag DN, Weaver DL, Alex JC, Fairbank JT. Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol. 1993;2:335–9; discussion 340.CrossRefPubMed Krag DN, Weaver DL, Alex JC, Fairbank JT. Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol. 1993;2:335–9; discussion 340.CrossRefPubMed
13.
go back to reference Borgstein PJ, Pijpers R, Comans EF, van Diest PJ, Boom RP, Meijer S. Sentinel lymph node biopsy in breast cancer: guidelines and pitfalls of lymphoscintigraphy and gamma probe detection. J Am Coll Surg. 1998;186:275–83.CrossRefPubMed Borgstein PJ, Pijpers R, Comans EF, van Diest PJ, Boom RP, Meijer S. Sentinel lymph node biopsy in breast cancer: guidelines and pitfalls of lymphoscintigraphy and gamma probe detection. J Am Coll Surg. 1998;186:275–83.CrossRefPubMed
14.
15.
go back to reference Morrow M, Rademaker AW, Bethke KP, et al. Learning sentinel node biopsy: results of a prospective randomized trial of two techniques. Surgery. 1999;126:714–20; discussion 720–712.CrossRefPubMed Morrow M, Rademaker AW, Bethke KP, et al. Learning sentinel node biopsy: results of a prospective randomized trial of two techniques. Surgery. 1999;126:714–20; discussion 720–712.CrossRefPubMed
16.
go back to reference Jung SY, Kim SK, Kim SW, et al. Comparison of sentinel lymph node biopsy guided by the multimodal method of indocyanine green fluorescence, radioisotope, and blue dye versus the radioisotope method in breast cancer: a randomized controlled trial. Ann Surg Oncol. 2014;21:1254–9.CrossRefPubMed Jung SY, Kim SK, Kim SW, et al. Comparison of sentinel lymph node biopsy guided by the multimodal method of indocyanine green fluorescence, radioisotope, and blue dye versus the radioisotope method in breast cancer: a randomized controlled trial. Ann Surg Oncol. 2014;21:1254–9.CrossRefPubMed
17.
go back to reference Ahmed M, Purushotham AD, Douek M. Novel techniques for sentinel lymph node biopsy in breast cancer: a systematic review. Lancet Oncol. 2014;15:e351–62.CrossRefPubMed Ahmed M, Purushotham AD, Douek M. Novel techniques for sentinel lymph node biopsy in breast cancer: a systematic review. Lancet Oncol. 2014;15:e351–62.CrossRefPubMed
18.
go back to reference Kitai T, Inomoto T, Miwa M, Shikayama T. Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer. Breast Cancer. 2005;12:211–5.CrossRefPubMed Kitai T, Inomoto T, Miwa M, Shikayama T. Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer. Breast Cancer. 2005;12:211–5.CrossRefPubMed
19.
go back to reference Mamounas EP, Brown A, Anderson S, et al. Sentinel node biopsy after neoadjuvant chemotherapy in breast cancer: results from National Surgical Adjuvant Breast and Bowel Project Protocol B-27. J Clin Oncol. 2005;23:2694–702.CrossRefPubMed Mamounas EP, Brown A, Anderson S, et al. Sentinel node biopsy after neoadjuvant chemotherapy in breast cancer: results from National Surgical Adjuvant Breast and Bowel Project Protocol B-27. J Clin Oncol. 2005;23:2694–702.CrossRefPubMed
20.
go back to reference Giuliano AE, Hunt KK, Ballman KV, et al. Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA. 2011;305:569–75.CrossRefPubMedPubMedCentral Giuliano AE, Hunt KK, Ballman KV, et al. Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA. 2011;305:569–75.CrossRefPubMedPubMedCentral
21.
go back to reference Boughey JC, Ballman KV, Le-Petross HT, et al. 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. 2016;263:802–7.CrossRefPubMed Boughey JC, Ballman KV, Le-Petross HT, et al. 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. 2016;263:802–7.CrossRefPubMed
22.
go back to reference Classe JM, Bordes V, Campion L, et al. Sentinel lymph node biopsy after neoadjuvant chemotherapy for advanced breast cancer: results of Ganglion Sentinelle et Chimiotherapie Neoadjuvante, a French prospective multicentric study. J Clin Oncol. 2009;27:726–32.CrossRefPubMed Classe JM, Bordes V, Campion L, et al. Sentinel lymph node biopsy after neoadjuvant chemotherapy for advanced breast cancer: results of Ganglion Sentinelle et Chimiotherapie Neoadjuvante, a French prospective multicentric study. J Clin Oncol. 2009;27:726–32.CrossRefPubMed
23.
go back to reference Boughey JC, Suman VJ, Mittendorf EA, et al. Factors affecting sentinel lymph node identification rate after neoadjuvant chemotherapy for breast cancer patients enrolled in ACOSOG Z1071 (Alliance). Ann Surg. 2015;261:547–52.CrossRefPubMed Boughey JC, Suman VJ, Mittendorf EA, et al. Factors affecting sentinel lymph node identification rate after neoadjuvant chemotherapy for breast cancer patients enrolled in ACOSOG Z1071 (Alliance). Ann Surg. 2015;261:547–52.CrossRefPubMed
24.
go back to reference Tsuyuki S, Yamaguchi A, Kawata Y, Kawaguchi K. Assessing the effects of neoadjuvant chemotherapy on lymphatic pathways to sentinel lymph nodes in cases of breast cancer: usefulness of the indocyanine green-fluorescence method. Breast. 2015;24:298–301.CrossRefPubMed Tsuyuki S, Yamaguchi A, Kawata Y, Kawaguchi K. Assessing the effects of neoadjuvant chemotherapy on lymphatic pathways to sentinel lymph nodes in cases of breast cancer: usefulness of the indocyanine green-fluorescence method. Breast. 2015;24:298–301.CrossRefPubMed
25.
go back to reference Stoffels I, Dissemond J, Poppel T, Schadendorf D, Klode J. Intraoperative fluorescence imaging for sentinel lymph node detection: prospective clinical trial to compare the usefulness of indocyanine green vs technetium Tc 99 m for identification of sentinel lymph nodes. JAMA Surg. 2015;150:617–23.CrossRefPubMed Stoffels I, Dissemond J, Poppel T, Schadendorf D, Klode J. Intraoperative fluorescence imaging for sentinel lymph node detection: prospective clinical trial to compare the usefulness of indocyanine green vs technetium Tc 99 m for identification of sentinel lymph nodes. JAMA Surg. 2015;150:617–23.CrossRefPubMed
Metadata
Title
The Sentinel Lymph Node Biopsy Using Indocyanine Green Fluorescence Plus Radioisotope Method Compared With the Radioisotope-Only Method for Breast Cancer Patients After Neoadjuvant Chemotherapy: A Prospective, Randomized, Open-Label, Single-Center Phase 2 Trial
Authors
So-Youn Jung, MD, PhD
Jai Hong Han, MD
Soo Jin Park, MD
Eun-Gyeong Lee, MD
Joohwa Kwak, MD
Sun Hye Kim, MD
Moo Hyun Lee, MD, PhD
Eun Sook Lee, MD, PhD
Han-Sung Kang, MD, PhD
Keun Seok Lee, MD, PhD
In Hae Park, MD, PhD
Sung Hoon Sim, MD, PhD
Hae Jeong Jeong, MD, PhD
Youngmee Kwon, MD, PhD
Dong-Eun Lee, MS
Seok-Ki Kim, MD, PhD
Seeyoun Lee, MD, PhD
Publication date
01-08-2019
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 8/2019
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-019-07400-0

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