Annals of Surgical Oncology

, Volume 23, Issue 1, pp 44–50 | Cite as

Evaluation of the Clinical Utility of the ICG Fluorescence Method Compared with the Radioisotope Method for Sentinel Lymph Node Biopsy in Breast Cancer

  • Tomoharu Sugie
  • Takayuki Kinoshita
  • Norikazu Masuda
  • Terumasa Sawada
  • Akira Yamauchi
  • Katsumasa Kuroi
  • Tetsuya Taguchi
  • Hiroko Bando
  • Hiroyasu Yamashiro
  • Tecchuu Lee
  • Nobuhiko Shinkura
  • Hironori Kato
  • Takafumi Ikeda
  • Kenichi Yoshimura
  • Hanae Ueyama
  • Masakazu Toi
Breast Oncology

Abstract

Purpose

This study compared the clinical utility of indocyanine green (ICG) fluorescence and radioisotope (RI) for sentinel lymph node (SLN) detection in breast cancer.

Methods

Women with node-negative breast cancer underwent SLN biopsy using ICG fluorescence and RI. The primary end point was the sensitivity of ICG fluorescence compared with RI in the patients with tumor-positive SLNs. Secondary end points included detection rates for SLN, the additive effect of ICG fluorescence to RI, signature of positive SLNs according to tier, and adverse events related to ICG administration.

Results

A total of 847 women with clinical node-negative breast cancer underwent SLN biopsy, and 821 patients were included in the per-protocol analysis. SLN mapping was performed using ICG fluorescence and RI. The overall detection of SLNs using ICG fluorescence was identical to RI (97.2 vs. 97.0 %, P = 0.88), and the combination of both methods achieved a significant improvement compared with RI alone (99.8 vs. 97.0 %, P < 0.001). The detection rate for tumor-positive SLN was 93.3 % for ICG fluorescence and 90.0 % for RI, and the sensitivity of the ICG fluorescence method was 95.7 % (95 % CI 91.3–98.3, P = 0.11). The additional use of ICG significantly improved positive SLN detection for RI (97.2 vs. 90.0 %, P < 0.001). There were no serious adverse events related to hypersensitivity to ICG.

Conclusions

The ICG fluorescence method may be an acceptable alternative to SLN detection using RI in breast cancer.

Keywords

Sentinel Lymph Node Sentinel Lymph Node Biopsy Positive Sentinel Lymph Node Sentinel Lymph Node Detection Completion Axillary Lymph Node Dissection 

Notes

Acknowledgment

This work was supported by research funding from Hamamatsu Photonics. The authors thank Akira Shimizu and Masahiro Takada for scientific advice and the staff of Institute for Advancement of Clinical and Translational Science, Kyoto University Hospital, for their valuable help.

Disclosure

T.S. received honoraria from Hamamatsu Photonics. The other authors declare no conflict of interest.

References

  1. 1.
    Cody HS 3rd, Fey J, Akhurst T, Fazzari, M., Mazumdar, M., Yeung, H, et al. Complemental of blue dye and isotope in sentinel node localization for breast cancer: univariate and multivariate analysis of 966 procedures. Ann Surg Oncol. 2001;18:2560–6.Google Scholar
  2. 2.
    Tafra L, Lannin DR, Swanson MS, Van Eyk, J. J., Verbanac, K. M., Chua, A. N., et al. Multicenter trial of sentinel node biopsy for breast cancer using both technetium sulfur colloid and isosulfan blue dye. Ann Surg. 2001;233:51–9.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Krag DN, Anderson SJ, Julian TB, Brown, A. M., Harlow, S. P., Ashikaga, T., et al. Technical outcome of sentinel-lymph-node resection and conventional axillary lymph node dissection in patients with clinically node-negative breast cancer: result from the NSABP B-32 randomised phase III trial. Lancet Oncol. 2007;8:881–8.PubMedCrossRefGoogle Scholar
  4. 4.
    Morrow M, Rademaker AW, Bethke KP, Talamonti, M. S., Dawes, L. G., Clauson, J, et al. Learning sentinel node biopsy: results of a prospective randomized trial of two techniques. Surgery. 1999;126:714–20.PubMedCrossRefGoogle Scholar
  5. 5.
    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.PubMedCrossRefGoogle Scholar
  6. 6.
    Sugie T, Kassim KA, Takeuchi M, Hashimoto, T., Yamagami, K., Masai, Y, et al. A novel method for sentinel lymph node biopsy by indocyanine green fluorescence technique in breast cancer. Cancers. 2010;2:713–20.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Takeuchi M, Sugie T, Abdelazeem K, Kato, H., Shinkura, N., Takada, M, et al. Lymphatic mapping with fluorescence navigation using indocyanine green and axillary surgery in patients with primary breast cancer. Breast J. 2012;18:535–41.PubMedCrossRefGoogle Scholar
  8. 8.
    Abe H, Mori T, Umeda T, Tanaka, M., Kawai, Y., Shimizu, T., et al. Indocyanine green fluorescence imaging system for sentinel lymph node biopsies in early breast cancer patients. Surg Today. 2011;41:197–202.PubMedCrossRefGoogle Scholar
  9. 9.
    Tagaya N, Yamazaki R, Nakagawa A, Abe, A., Hamada, K., Kubota, K., et al. Intraoperative identification of sentinel lymph node by near-infrared fluorescence imaging in patients with breast cancer. Am J Surg. 2008;195:850–3.PubMedCrossRefGoogle Scholar
  10. 10.
    Tagaya N, Aoyagi H, Nakagawa A, Abe, A., Iwasaki, Y., Tachibana, M., et al. A novel approach for sentinel lymph node identification using fluorescence imaging and image overlay navigation surgery in patients with breast cancer. World J Surg. 2011;35:154–8.PubMedCrossRefGoogle Scholar
  11. 11.
    Sugie T, Sawada T, Tagaya N, Kinoshita, T., Yamagami, K., Suwa, H., et al. Comparison of the indocyanine green fluorescence and blue dye methods in detection of sentinel lymph nodes in early-stage breast cancer. Ann Surg Oncol. 2013;20:2213–8.PubMedCrossRefGoogle Scholar
  12. 12.
    Inoue T, Nishi T, Nakano Y, Nishimae, A., Sawai, Y., Yamasaki, M., et al. Axillary lymph node recurrence after sentinel lymph node biopsy performed using a combination of indocyanine green fluorescence and the blue dye method in early breast cancer. Breast Cancer. 2014. doi: 10.1007/s12282-014-0573-8.Google Scholar
  13. 13.
    Hojo T, Nagao T, Kikuyama M, Akashi S, Kinoshita T. Evaluation of sentinel node biopsy by combined fluorescence and dye method and lymph flow for breast cancer. Breast. 2010;19:210–3.PubMedCrossRefGoogle Scholar
  14. 14.
    Wishart GC, Loh SW, Jones L, Benson JR. A feasibility study (ICG-10) of indocyanine green (ICG) fluorescence mapping for sentinel lymph node detection in early breast cancer. Eur J Surg Oncol. 2012;38:651–6.PubMedCrossRefGoogle Scholar
  15. 15.
    van der Vorst JR, Schaafsma BE, Verbeek FP, Hutteman, M., Mieog, J. S. D., Lowik, C. W., et al. Randomized comparison of near-infrared fluorescence imaging using indocyanine green and 99mtechnetium with or without patent blue for the sentinel lymph node procedure in breast cancer patients. Ann Surg Oncol. 2012;19:4104–11.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Ballardini B, Santoro L, Sangalli C, Gentilini, O., Renne, G., Lissidini, G., et al. The indocyanine green method is equivalent to the 99mTc-labeled radiotracer method for identifying the sentinel node in breast cancer: a concordance and validation study. Eur J Surg Oncol. 2013;39:1332–6.PubMedCrossRefGoogle Scholar
  17. 17.
    Schaafsma BE, Verbeek FP, Riebergen DD, Hiel, B., Vorst, J. R., Liefers, G. J., et al. Clinical trial of combined radio- and fluorescence-guided sentinel lymph node biopsy in breast cancer. Br J Surg. 2013;100:1037–44.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Tamaki Y, Akiyama F, Iwase T, Kaneko, T., Tsuda, H., Sato, K., et al. Molecular detection of lymph node metastases in breast cancer patients: results of a multicenter trial using the one-step nucleic acid amplification assay. Clin Cancer Res. 2009;15:2879–84.PubMedCrossRefGoogle Scholar
  19. 19.
    Murawa D, Hirche C, Dresel S, Hünerbein M. Sentinel lymph node biopsy in breast cancer guided by indocyanine green fluorescence. Br J Surg. 2009;96:1289–94.PubMedCrossRefGoogle Scholar
  20. 20.
    Verbeek FP, Troyan SL, Mieog JS, Liefers, G. J., Moffitt, L. A., Rosenberg, M., et al. Near-infrared fluorescence sentinel lymph node mapping in breast cancer: a multicenter experience. Breast Cancer Res Treat. 2014;143:333–42.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Samorani D, Fogacci T, Panzini I, Frisoni, G., Accardi, F. G., Ricci, M., et al. The use of indocyanine green to detect sentinel nodes in breast cancer: a prospective study. Eur J Surg Oncol. 2015;41:64–70.PubMedCrossRefGoogle Scholar
  22. 22.
    Reuthebuch O, Haussler A, Genoni M, Tavakoli, R., Odavic, D., Kadner, A., et al. Novadaq SPY: intraoperative quality assessment in off-pump coronary artery bypass grafting. Chest. 2004;125:418–24.PubMedCrossRefGoogle Scholar
  23. 23.
    Troyan SL, Kianzad V, Gibbs-Strauss SL, Gioux, S., Matsui, A., Oketokoun, R., et al. The FLARE intraoperative near-infrared fluorescence imaging system: a first-in-human clinical trial in breast cancer sentinel lymph node mapping. Ann Surg Oncol. 2009;16:2943–52.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    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.PubMedCrossRefGoogle Scholar
  25. 25.
    Lyman GH, Temin S, Edge SB, Newman, L. A., Turner, R. R., Weaver, D. L., et al. Sentinel lymph node biopsy for patients with early-stage breast cancer: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol. 2014;32:1365–83.PubMedCrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2015

Authors and Affiliations

  • Tomoharu Sugie
    • 1
  • Takayuki Kinoshita
    • 2
  • Norikazu Masuda
    • 3
  • Terumasa Sawada
    • 4
  • Akira Yamauchi
    • 5
  • Katsumasa Kuroi
    • 6
  • Tetsuya Taguchi
    • 7
  • Hiroko Bando
    • 8
  • Hiroyasu Yamashiro
    • 9
  • Tecchuu Lee
    • 10
  • Nobuhiko Shinkura
    • 11
  • Hironori Kato
    • 12
  • Takafumi Ikeda
    • 13
  • Kenichi Yoshimura
    • 14
  • Hanae Ueyama
    • 13
  • Masakazu Toi
    • 15
  1. 1.Department of SurgeryKansai Medical UniversityHirakataJapan
  2. 2.National Cancer Center HospitalTokyoJapan
  3. 3.National Hospital Organization Osaka National HospitalOsakaJapan
  4. 4.Department of Breast Surgery OncologyShowa University School of MedicineTokyoJapan
  5. 5.Tazuke-Kofukai Medical Research InstituteKitano HospitalOsakaJapan
  6. 6.Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome HospitalTokyoJapan
  7. 7.Department of Endocrine and Breast SurgeryKyoto Prefectural University of MedicineKyotoJapan
  8. 8.Department of Breast and Endocrine Surgery, Faculty of MedicineUniversity of TsukubaTsukubaJapan
  9. 9.Tenri HospitalTenriJapan
  10. 10.Japanese Red Cross Kyoto Daiichi HospitalKyotoJapan
  11. 11.Kyoto Breast Center Sawai Memorial ClinicKyotoJapan
  12. 12.Kobe City Medical Center General HospitalKobeJapan
  13. 13.Institute for Advancement of Clinical and Translational ScienceKyoto University HospitalKyotoJapan
  14. 14.Innovative Clinical Research CenterKanazawa University HospitalKanazawaJapan
  15. 15.Department of Breast SurgeryGraduate School of Medicine, Kyoto UniversityKyotoJapan

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