Comparisons of ICG‑fluorescence with conventional tracers in sentinel lymph node biopsy for patients with early‑stage breast cancer: A meta‑analysis

Yin,Rui; Ding,Lu-Yu; Wei,Qing-Zhong; Zhou,Ya; Tang,Guang-Yuan; Zhu,Xun

doi:10.3892/ol.2020.12375

Comparisons of ICG‑fluorescence with conventional tracers in sentinel lymph node biopsy for patients with early‑stage breast cancer: A meta‑analysis

Authors:
- Rui Yin
- Lu-Yu Ding
- Qing-Zhong Wei
- Ya Zhou
- Guang-Yuan Tang
- Xun Zhu
View Affiliations

Affiliations: Department of General Surgery, Beijing Aerospace General Hospital, Beijing 100076, P.R. China, Department of Psychiatry, The First Affiliated Hospital of China Medical University, Shenyang, Liaoning 110001, P.R. China, Department of General Surgery, The Second Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215004, P.R. China
Published online on: December 15, 2020 https://doi.org/10.3892/ol.2020.12375
Article Number: 114
Copyright: © Yin et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Radioisotopes (RI) and blue dye (BD) are routinely used markers for staining during sentinel lymph node biopsy (SLNB) in breast cancer. Compared with traditional tracers, tracer performance of indocyanine green (ICG) has been controversial. A total of 21 studies were selected from the PubMed, EMBASE and Cochrane Library databases. Detection ability was judged based on four endpoints: i) The identification rate (IR) of the patients; ii) the IR of the sentinel lymph nodes (SLNs); iii) the IR of the positive SLNs; and iv) the false negative rate (FNR). Compared with BD, ICG was superior in terms of the IR of the patients [odds ratio (OR)=7.17; 95% CI, 3.98‑12.94), the IR of the SLNs (OR=8.84; 95% CI, 6.71‑11.66) and FNR (OR=0.20; 95% CI, 0.08‑0.48) using a fixed‑effects model. There was a significant difference in both the IR of the positive SLNs (OR=21.32; 95% CI, 2.84‑160.14) and FNR (OR=0.46; 95% CI, 0.23‑0.91) in the ICG vs. RI group. Furthermore, when using ICG at the recommended dose, a significant difference was found in the IR of the patients (OR=1.77; 95% CI, 1.09‑2.85) and the IR of the SLNs (OR=21.62; 95% CI, 5.23‑89.43) using a fixed‑effects model. In the ICG vs. BD combined with RI group, there were no differences in either the IR of the patients (OR=5.10; 95% CI, 0.24‑107.48) or the IR of SLNs (OR=5.10; 95% CI, 0.60‑256.66). In conclusion, ICG was a better tracer compared with BD or RI alone and was not a worse tracer compared with BD combined with RI. The use of the recommended dose of ICG had an improved tracer effect. ICG is expected to be widely used in SLNB in view of its clinical advantages.

View Figures

View References

1	Mansel RE, Fallowfield L, Kissin M, Goyal A, Newcombe RG, Dixon JM, Yiangou C, Horgan K, Bundred N, Monypenny I, et al: Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: The ALMANAC trial. J Natl Cancer Inst. 98:599–609. 2006. View Article : Google Scholar : PubMed/NCBI
2	Krag DN, Weaver DL, Alex JC and Fairbank JT: Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol. 2:335–340. 1993. View Article : Google Scholar : PubMed/NCBI
3	Giuliano AE, Kirgan DM, Guenther JM and Morton DL: Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 220:391–401. 1994. View Article : Google Scholar : PubMed/NCBI
4	Kitai T, Inomoto T, Miwa M and Shikayama T: Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer. Breast Cancer. 12:211–215. 2005. View Article : Google Scholar : PubMed/NCBI
5	Ahmed M, Purushotham AD and Douek M: Novel techniques for sentinel lymph node biopsy in breast cancer: A systematic review. Lancet Oncol. 15:e351–e362. 2014. View Article : Google Scholar : PubMed/NCBI
6	Sugie T, Ikeda T, Kawaguchi A, Shimizu A and Toi M: Sentinel lymph node biopsy using indocyanine green fluorescence in early-stage breast cancer: A meta-analysis. Int J Clin Oncol. 22:11–17. 2017. View Article : Google Scholar : PubMed/NCBI
7	Moher D, Liberati A, Tetzlaff J and Altman DG; PRISMA Group, : Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Ann Intern Med. 151:264–269, W64. 2009. View Article : Google Scholar : PubMed/NCBI
8	Stang A: Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 25:603–605. 2010. View Article : Google Scholar : PubMed/NCBI
9	Schaafsma BE, Verbeek FP, Rietbergen DD, van der Hiel B, van der Vorst JR, Liefers GJ, Frangioni JV, van de Velde CJ, van Leeuwen FW and Vahrmeijer AL: Clinical trial of combined radio and fluorescence guided sentinel lymph node biopsy in breast cancer. Br J Surg. 100:1037–1044. 2013. View Article : Google Scholar : PubMed/NCBI
10	Liu J, Huang L, Wang N and Chen P: Indocyanine green detects sentinel lymph nodes in early breast cancer. J Int Med Res. 45:514–524. 2017. View Article : Google Scholar : PubMed/NCBI
11	Sugie T, Kinoshita T, Masuda N, Sawada T, Yamauchi A, Kuroi K, Taguchi T, Bando H, Yamashiro H, Lee T, et al: Evaluation of the clinical utility of the ICG fluorescence method compared with the radioisotope method for sentinel lymph node biopsy in breast cancer. Ann Surg Oncol. 23:44–50. 2016. View Article : Google Scholar : PubMed/NCBI
12	Samorani D, Fogacci T, Panzini I, Frisoni G, Accardi FG, Ricci M, Fabbri E, Nicoletti S, Flenghi L, Tamburini E, et al: The use of indocyanine green to detect sentinel nodes in breast cancer: A prospective study. Eur J Surg Oncol. 41:64–70. 2015. View Article : Google Scholar : PubMed/NCBI
13	Stoffels I, Dissemond J, Pöppel T, Schadendorf D and Klode J: Intraoperative fluorescence imaging for sentinel lymph node detection: Prospective clinical trial to compare the usefulness of indocyanine green vs technetium Tc 99m for identification of sentinel lymph nodes. JAMA Surg. 150:617–623. 2015. View Article : Google Scholar : PubMed/NCBI
14	Ji Y, Luo N, Jiang Y, Li Q, Wei W, Yang H and Liu J: Clinical utility of the additional use of blue dye for indocyanine green for sentinel node biopsy in breast cancer. J Surg Res. 215:88–92. 2017. View Article : Google Scholar : PubMed/NCBI
15	Grischke EM, Röhm C, Hahn M, Helms G, Brucker S and Wallwiener D: ICG fluorescence technique for the detection of sentinel lymph nodes in breast cancer: Results of a prospective open-label clinical trial. Geburtshilfe Frauenheilk. 75:935–940. 2015. View Article : Google Scholar
16	Tong M, Guo W and Gao W: Use of fluorescence imaging in combination with patent blue dye versus patent blue dye alone in sentinel lymph node biopsy in breast cancer. J Breast Cancer. 17:250–255. 2014. View Article : Google Scholar : PubMed/NCBI
17	Wishart GC, Loh SW, Jones L and 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. 38:651–656. 2012. View Article : Google Scholar : PubMed/NCBI
18	Sugie T, Sawada T, Tagaya N, Kinoshita T, Yamagami K, Suwa H, Ikeda T, Yoshimura K, Niimi M, Shimizu A and Toi M: Comparison of the indocyanine green fluorescence and blue dye methods in detection of sentinel lymph nodes in early-stage breast cancer. Ann Surg Oncol. 20:2213–2218. 2013. View Article : Google Scholar : PubMed/NCBI
19	Hirano A, Kamimura M, Ogura K, Kim N, Hattori A, Setoguchi Y, Okubo F, Inoue H, Miyamoto R, Kinoshita J, et al: A comparison of indocyanine green fluorescence imaging plus blue dye and blue dye alone for sentinel node navigation surgery in breast cancer patients. Ann Surg Oncol. 19:4112–4116. 2012. View Article : Google Scholar : PubMed/NCBI
20	van der Vorst JR, Schaafsma BE, Verbeek FP, Hutteman M, Mieog JS, Lowik CW, Liefers GJ, Frangioni JV, van de Velde CJ and Vahrmeijer AL: Randomized comparison of near-infrared fluorescence imaging using indocyanine green and 99(m) technetium with or without patent blue for the sentinel lymph node procedure in breast cancer patients. Ann Surg Oncol. 19:4104–4111. 2012. View Article : Google Scholar
21	Jung SY, Kim SK, Kim SW, Kwon Y, Lee ES, Kang HS, Ko KL, Shin KH, Lee KS, Park IH, 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. 21:1254–1259. 2014. View Article : Google Scholar : PubMed/NCBI
22	Hojo T, Nagao T, Kikuyama M, Akashi S and Kinoshita T: Evaluation of sentinel node biopsy by combined fluorescent and dye method and lymph flow for breast cancer. Breast. 19:210–213. 2010. View Article : Google Scholar : PubMed/NCBI
23	Hutteman M, Mieog JS, van der Vorst JR, Liefers GJ, Putter H, Löwik CW, Frangioni JV, van de Velde CJ and Vahrmeijer AL: Randomized, double-blind comparison of indocyanine green with or without albumin premixing for near-infrared fluorescence imaging of sentinel lymph nodes in breast cancer patients. Breast Cancer Res Treat. 127:163–170. 2011. View Article : Google Scholar : PubMed/NCBI
24	Verbeek FP, Troyan SL, Mieog JS, Liefers GJ, Moffitt LA, Rosenberg M, Hirshfield-Bartek J, Gioux S, van de Velde CJ, Vahrmeijer AL and Frangioni JV: Near-infrared fluorescence sentinel lymph node mapping in breast cancer: A multicenter experience. Breast Cancer Res Treat. 143:333–342. 2014. View Article : Google Scholar : PubMed/NCBI
25	Ballardini B, Santoro L, Sangalli C, Gentilini O, Renne G, Lissidini G, Pagani GM, Toesca A, Blundo C, del Castillo A, 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. 39:1332–1336. 2013. View Article : Google Scholar : PubMed/NCBI
26	Pitsinis V, Provenzano E, Kaklamanis L, Wishart GC and Benson JR: Indocyanine green fluorescence mapping for sentinel lymph node biopsy in early breast cancer. Surg Oncol. 24:375–379. 2015. View Article : Google Scholar : PubMed/NCBI
27	Polom K, Murawa D, Nowaczyk P, Rho YS and Murawa P: Breast cancer sentinel lymph node mapping using near infrared guided indocyanine green and indocyanine green-human serum albumin in comparison with gamma emitting radioactive colloid tracer. Eur J Surg Oncol. 38:137–142. 2012. View Article : Google Scholar : PubMed/NCBI
28	Guo W, Zhang L, Ji J, Gao W, Liu J and Tong M: Evaluation of the benefit of using blue dye in addition to indocyanine green fluorescence for sentinel lymph node biopsy in patients with breast cancer. World J Surg Oncol. 12:2902014. View Article : Google Scholar : PubMed/NCBI
29	Murawa D, Hirche C, Dresel S and Hünerbein M: Sentinel lymph node biopsy in breast cancer guided by indocyanine green fluorescence. Br J Surg. 96:1289–1294. 2009. View Article : Google Scholar : PubMed/NCBI
30	Mieog JS, Troyan SL, Hutteman M, Donohoe KJ, Van Der Vorst JR, Stockdale A, Liefers GJ, Choi HS, Gibbs-Strauss SL, Putter H, et al: Toward optimization of imaging system and lymphatic tracer for near-infrared fluorescent sentinel lymph node mapping in breast cancer. Ann Surg Oncol. 18:2483–2491. 2011. View Article : Google Scholar : PubMed/NCBI
31	Kusano M, Kokudo N, Toi M and Kaibori M: ICG fluorescence imaging and navigation surgery. Springer; Japan: 2016, View Article : Google Scholar