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Surgical Endoscopy

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01-06-2022 | Metastasis

Near-infrared fluorescence imaging-guided lymphatic mapping in thoracic esophageal cancer surgery

Authors: Xiaojin Wang, Yi Hu, Xiangwen Wu, Mingzhu Liang, Zhenhua Hu, Xiangfeng Gan, Dan Li, Qingdong Cao, Hong Shan

Published in: Surgical Endoscopy | Issue 6/2022

Abstract

Purpose

Identifying the lymphatic drainage pathway is important for accurate lymph node (LN) dissection in esophageal cancer (EC). This study aimed to assess lymphatic drainage mapping in thoracic EC using near-infrared fluorescent (NIRF) imaging with indocyanine green (ICG) and identify its feasibility for intraoperative LN drainage visualization and dissection.

Methods

From November 2019 to August 2020, esophagectomy was performed using intraoperative NIRF navigation with ICG injected into the esophageal submucosa by endoscopy. All LNs were divided into four groups according to the NIRF status and presence of metastasis: NIRF⁺LN⁺, NIRF⁺LN⁻, NIRF⁻LN⁺, and NIRF⁻LN⁻.

Results

Regional LNs were detected in all 84 enrolled patients with thoracic EC. A total of 2164 LNs were removed, and the mean number of dissected LNs was 25.68 ± 12.00. NIRF⁺ LNs were observed in all patients and distributed at 19 LN stations, which formed lymphatic drainage maps. The top five LN stations of NIRF⁺ probability in upper thoracic EC were No. 7, 106ecR, 107, 1, and 106recL; in middle thoracic EC, they were No. 107, 7, 110, 1, and 105; and in lower thoracic EC, they were No. 107, 7, 110, 106recR, and 1. There were no cases of ICG-related adverse events or chylothorax. The 30-day mortality rate was 0%. Major complications included anastomotic fistula (7.14%), pneumonia (4.76%), pleural effusion (13.10%), atelectasis (3.75%), hoarseness (8.33%), and arrhythmia (4.76%).

Conclusion

Regional LN mapping of thoracic EC was performed using ICG/NIRF imaging, which showed different preferred LN drainage stations in various anatomical locations of the thoracic esophagus. ICG/NIRF imaging is feasible for intraoperative LN drainage visualization and dissection.

Clinical trial registration

The clinical trial registration number is NCT04173676 (http://www.clinicaltrials.gov/).

Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424. https://doi.org/10.3322/caac.21492CrossRefPubMed

Lagergren J, Smyth E, Cunningham D, Lagergren P (2017) Oesophageal cancer. Lancet 390(10110):2383–2396. https://doi.org/10.1016/s0140-6736(17)31462-9CrossRefPubMed

Miyata H, Yamasaki M, Kurokawa Y, Takiguchi S, Nakajima K, Fujiwara Y et al (2011) Survival factors in patients with recurrence after curative resection of esophageal squamous cell carcinomas. Ann Surg Oncol 18(12):3353–3361. https://doi.org/10.1245/s10434-011-1747-7CrossRefPubMed

Yamashita K, Watanabe M, Mine S, Kurogochi T, Okamura A, Hayami M et al (2017) Patterns and outcomes of recurrent esophageal cancer after curative esophagectomy. World J Surg 41(9):2337–2344. https://doi.org/10.1007/s00268-017-4024-5CrossRefPubMed

Ma DW, Jung DH, Kim JH, Park JJ, Youn YH, Park H (2019) Predicting lymph node metastasis for endoscopic resection of superficial esophageal squamous cell carcinoma. J Thorac Cardiovasc Surg 157(1):397-402.e1. https://doi.org/10.1016/j.jtcvs.2018.07.034CrossRefPubMed

Akutsu Y, Kato K, Igaki H, Ito Y, Nozaki I, Daiko H et al (2016) The prevalence of overall and initial lymph node metastases in clinical T1N0 thoracic esophageal cancer: from the results of JCOG0502, a Prospective Multicenter Study. Ann Surg 264(6):1009–1015. https://doi.org/10.1097/SLA.0000000000001557CrossRefPubMed

Kato H, Fukuchi M, Miyazaki T, Nakajima M, Tanaka N, Inose T et al (2007) Surgical treatment for esophageal cancer. Current issues. Dig Surg 24(2):88–95. https://doi.org/10.1159/000101894CrossRefPubMed

Cai M, Zhang Z, Shi X, Hu Z, Tian J (2020) NIR-II/NIR-I Fluorescence molecular tomography of heterogeneous mice based on gaussian weighted neighborhood fused lasso method. IEEE Trans Med Imaging 39(6):2213–2222. https://doi.org/10.1109/tmi.2020.2964853CrossRefPubMed

Mariette C, Piessen G, Briez N, Triboulet JP (2008) The number of metastatic lymph nodes and the ratio between metastatic and examined lymph nodes are independent prognostic factors in esophageal cancer regardless of neoadjuvant chemoradiation or lymphadenectomy extent. Ann Surg 247(2):365–371. https://doi.org/10.1097/SLA.0b013e31815aaadfCrossRefPubMed

10.

Rizk NP, Ishwaran H, Rice TW, Chen LQ, Schipper PH, Kesler KA et al (2010) Optimum lymphadenectomy for esophageal cancer. Ann Surg 251(1):46–50. https://doi.org/10.1097/SLA.0b013e3181b2f6eeCrossRefPubMed

11.

Lj H (2010) Extent of lymphadenectomy in esophageal cancer: how many lymph nodes is enough? Ann Surg Oncol 17(3):676–678. https://doi.org/10.1245/s10434-009-0824-7CrossRef

12.

Nishihira T, Hirayama K, Mori S (1998) A prospective randomized trial of extended cervical and superior mediastinal lymphadenectomy for carcinoma of the thoracic esophagus. Am J Surg 175(1):47–51. https://doi.org/10.1016/s0002-9610(97)00227-4CrossRefPubMed

13.

Altorki N, Kent M, Ferrara C, Port J (2002) Three-field lymph node dissection for squamous cell and adenocarcinoma of the esophagus. Ann Surg 236(2):177–183. https://doi.org/10.1097/00000658-200208000-00005CrossRefPubMedPubMedCentral

14.

Yoon YC, Lee KS, Shim YM, Kim BT, Kim K, Kim TS (2003) Metastasis to regional lymph nodes in patients with esophageal squamous cell carcinoma: CT versus FDG PET for presurgical detection prospective study. Radiology 227(3):764–770. https://doi.org/10.1148/radiol.2281020423CrossRefPubMed

15.

Kato H, Miyazaki T, Nakajima M, Takita J, Sohda M, Fukai Y et al (2003) Sentinel lymph nodes with technetium-99m colloidal rhenium sulfide in patients with esophageal carcinoma. Cancer 98(5):932–939. https://doi.org/10.1002/cncr.11559CrossRefPubMed

16.

Gilmore DM, Khullar OV, Gioux S, Stockdale A, Frangioni JV, Colson YL et al (2013) Effective low-dose escalation of indocyanine green for near-infrared fluorescent sentinel lymph node mapping in melanoma. Ann Surg Oncol 20(7):2357–2363. https://doi.org/10.1245/s10434-013-2905-xCrossRefPubMed

17.

Mieog JS, Troyan SL, Hutteman M, Donohoe KJ, van der Vorst JR, Stockdale A et al (2011) Toward optimization of imaging system and lymphatic tracer for near-infrared fluorescent sentinel lymph node mapping in breast cancer. Ann Surg Oncol 18(9):2483–2491. https://doi.org/10.1245/s10434-011-1566-xCrossRefPubMedPubMedCentral

18.

Soares AS, Lovat LB, Chand M (2019) Intracorporeal lymph node mapping in colon cancer surgery. Eur J Surg Oncol 45(12):2316–2318. https://doi.org/10.1016/j.ejso.2019.07.013CrossRefPubMed

19.

Hachey KJ, Gilmore DM, Armstrong KW, Harris SE, Hornick JL, Colson YL et al (2016) Safety and feasibility of near-infrared image-guided lymphatic mapping of regional lymph nodes in esophageal cancer. J Thorac Cardiovasc Surg 152(2):546–554. https://doi.org/10.1016/j.jtcvs.2016.04.025CrossRefPubMedPubMedCentral

20.

Schlottmann F, Barbetta A, Mungo B, Lidor AO, Molena D (2017) Identification of the lymphatic drainage pattern of esophageal cancer with near-infrared fluorescent imaging. J Laparoendosc Adv Surg Tech A 27(3):268–271. https://doi.org/10.1089/lap.2016.0523CrossRefPubMedPubMedCentral

21.

Jiang H, Teng H, Sun Y, Guo X, Hua R, Su Y et al (2020) Near-infrared fluorescent image-guided lymphatic mapping in esophageal squamous cell carcinoma. Ann Surg Oncol 27(10):3799–3807. https://doi.org/10.1245/s10434-019-07969-6CrossRefPubMed

22.

Rice TW, Ishwaran H, Ferguson MK, Blackstone EH, Goldstraw P (2017) Cancer of the esophagus and esophagogastric: an eighth edition junction staging primer. J Thorac Oncol 12(1):36–42. https://doi.org/10.1016/j.jtho.2016.10.016CrossRefPubMed

23.

Wang X, Li X, Cheng H, Zhang B, Zhong H, Wang R et al (2019) Single-port inflatable mediastinoscopy combined with laparoscopic-assisted small incision surgery for radical esophagectomy is an effective and safe treatment for esophageal cancer. J Gastrointest Surg 23(8):1533–1540. https://doi.org/10.1007/s11605-018-04069-wCrossRefPubMed

24.

He K, Chi C, Kou D, Huang W, Wu J, Wang Y et al (2016) Comparison between the indocyanine green fluorescence and blue dye methods for sentinel lymph node biopsy using novel fluorescence image-guided resection equipment in different types of hospitals. Transl Res 178:74–80. https://doi.org/10.1016/j.trsl.2016.07.010CrossRefPubMed

25.

Mao Y, Wang K, He K, Ye J, Yang F, Zhou J et al (2017) Development and application of the near-infrared and white-light thoracoscope system for minimally invasive lung cancer surgery. J Biomed Opt 22(6):66002. https://doi.org/10.1117/1.Jbo.22.6.066002CrossRefPubMed

26.

Japanese Classification of Esophageal Cancer (2017) 11th edition: part I. Esophagus 14(1):1–36. https://doi.org/10.1007/s10388-016-0551-7CrossRef

27.

Nakagawa S, Kanda T, Kosugi S, Ohashi M, Suzuki T, Hatakeyama K (2004) Recurrence pattern of squamous cell carcinoma of the thoracic esophagus after extended radical esophagectomy with three-field lymphadenectomy. J Am Coll Surg 198(2):205–211. https://doi.org/10.1016/j.jamcollsurg.2003.10.005CrossRefPubMed

28.

Park SY, Suh JW, Kim DJ, Park JC, Kim EH, Lee CY et al (2018) Near-infrared lymphatic mapping of the recurrent laryngeal nerve nodes in T1 esophageal cancer. Ann Thorac Surg 105(6):1613–1620. https://doi.org/10.1016/j.athoracsur.2018.01.083CrossRefPubMed

29.

Heerdt AS (2018) Lymphatic mapping and sentinel lymph node biopsy for breast cancer. JAMA Oncol 4(3):431. https://doi.org/10.1001/jamaoncol.2017.4000CrossRefPubMed

30.

Rossi EC, Kowalski LD, Scalici J, Cantrell L, Schuler K, Hanna RK et al (2017) A comparison of sentinel lymph node biopsy to lymphadenectomy for endometrial cancer staging (FIRES trial): a multicentre, prospective, cohort study. Lancet Oncol 18(3):384–392. https://doi.org/10.1016/s1470-2045(17)30068-2CrossRefPubMed

31.

Zhang S, Zhang P, Guo S, Lian J, Chen Y, Chen A et al (2020) Comparative study of three types of lymphadenectomy along the left recurrent laryngeal nerve by minimally invasive esophagectomy. Thorac Cancer 11(2):224–231. https://doi.org/10.1111/1759-7714.13210CrossRefPubMed

32.

Hu Z, Fang C, Li B, Zhang Z, Cao C, Cai M et al (2020) First-in-human liver-tumour surgery guided by multispectral fluorescence imaging in the visible and near-infrared-I/II windows. Nat Biomed Eng 4(3):259–271. https://doi.org/10.1038/s41551-019-0494-0CrossRefPubMed

33.

Rosenthal EL, Warram JM, de Boer E, Chung TK, Korb ML, Brandwein-Gensler M et al (2015) Safety and tumor specificity of cetuximab-IRDye800 for surgical navigation in head and neck cancer. Clin Cancer Res 21(16):3658–3666. https://doi.org/10.1158/1078-0432.Ccr-14-3284CrossRefPubMedPubMedCentral

34.

Tummers WS, Miller SE, Teraphongphom NT, van den Berg NS, Hasan A, Longacre TA et al (2019) Detection of visually occult metastatic lymph nodes using molecularly targeted fluorescent imaging during surgical resection of pancreatic cancer. HPB (Oxford) 21(7):883–890. https://doi.org/10.1016/j.hpb.2018.11.008CrossRef

35.

Liang M, Yang M, Wang F, Wang X, HE B, Mei C et al (2021) Near-infrared fluorescence-guided resection of micrometastases derived from esophageal squamous cell carcinoma using a c-Met-targeted probe in a preclinical xenograft model. J Controll Release 332:171–183. https://doi.org/10.1016/j.jconrel.2021.02.019CrossRef

Title: Near-infrared fluorescence imaging-guided lymphatic mapping in thoracic esophageal cancer surgery
Authors: Xiaojin Wang
Yi Hu
Xiangwen Wu
Mingzhu Liang
Zhenhua Hu
Xiangfeng Gan
Dan Li
Qingdong Cao
Hong Shan
Publication date: 01-06-2022
Publisher: Springer US
Keywords: Metastasis
Esophageal Cancer
Esophagus Resection
Esophageal Cancer
Esophagus Resection
Published in: Surgical Endoscopy / Issue 6/2022
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI: https://doi.org/10.1007/s00464-021-08720-7

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Near-infrared fluorescence imaging-guided lymphatic mapping in thoracic esophageal cancer surgery

Abstract

Purpose

Methods

Results

Conclusion

Clinical trial registration

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Clinical trial registration

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