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Near-Infrared Fluorescent Image-Guided Lymphatic Mapping in Esophageal Squamous Cell Carcinoma

  • Thoracic Oncology
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

Recently, the feasibility of near-infrared (NIR) image-guided sentinel lymph node (SLN) mapping has been tested in patients with gastrointestinal cancer. The aim of this study is to investigate whether SLN mapping can be used to identify mediastinal lymph node metastases during minimally invasive esophagectomy and explore the lymphatic drainage pattern of esophageal squamous cell carcinoma (ESCC) using NIR fluorescent imaging.

Patients and Methods

A total of 21 patients diagnosed with cT1–3 stage ESCC were enrolled. Patients received submucosal injection of indocyanine green diluted with sodium chloride (0.9%) at the start of the esophagectomy procedure followed by NIR mapping.

Results

Thoracoscopic-assisted McKeown esophagectomy with NIR imaging was successfully performed in all patients. The detection rate and number of NIR+ lymph nodes were 95.2% (20/21) and 4.0 (2.0–6.5), respectively. The accuracy, false-negative rates, and negative predictive value were 100% (10 of 10 cases), 0% (0 of 4), and 100% (6 of 6), respectively, for pT1/T2 diseases; and 80.0% (8 of 10), 40% (2 of 5), and 71.4% (5 of 7), respectively, for pT3 diseases. The NIR+ region was the most commonly detected in the right recurrent laryngeal nerve (80%), and the NIR+ region was identified in the upper mediastinal zone in 20 patients.

Conclusions

Evaluation of the lymphatic drainage pattern and the application of sentinel lymph node in ESCC with real-time NIR imaging could be effective, especially in pT1/2 disease. NIR imaging-guided SLN navigation appears to be a clinically beneficial less-invasive method for treating ESCC.

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References

  1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J. 2019;69(1):7–34.

    Article  Google Scholar 

  2. Arnold M, Soerjomataram I, Ferlay J, Forman D. Global incidence of oesophageal cancer by histological subtype in 2012. Gut. Mar 2015;64(3):381–7.

    Article  Google Scholar 

  3. Markar S, Gronnier C, Duhamel A, et al. Salvage surgery after chemoradiotherapy in the management of esophageal cancer: is it a viable therapeutic option? J Clin Oncol. 2015;33(33):3866–873.

    Article  CAS  Google Scholar 

  4. Swisher SG, Moughan J, Komaki RU, et al. Final results of NRG oncology RTOG 0246: an organ-preserving selective resection strategy in esophageal cancer patients treated with definitive chemoradiation. J Thorac Oncol. 2017;12(2):368–74.

    Article  Google Scholar 

  5. Roder JD, Busch R, Stein HJ, Fink U, Siewert JR. Ratio of invaded to removed lymph nodes as a predictor of survival in squamous cell carcinoma of the oesophagus. Br J Surg. Mar 1994;81(3):410–3.

    Article  CAS  Google Scholar 

  6. Tachibana M, Kinugasa S, Shibakita M, et al. Surgical treatment of superficial esophageal cancer. Langenbeck’s Arch Surg. 2006;391(4):304–21.

    Article  Google Scholar 

  7. Kuge K, Murakami G, Mizobuchi S, Hata Y, Aikou T, Sasaguri S. Submucosal territory of the direct lymphatic drainage system to the thoracic duct in the human esophagus. J Thorac Cardiovasc Surg. 2003;125(6):1343–9.

    Article  Google Scholar 

  8. Lerut T, Nafteux P, Moons J, et al. Three-field lymphadenectomy for carcinoma of the esophagus and gastroesophageal junction in 174 R0 resections: impact on staging, disease-free survival, and outcome: a plea for adaptation of TNM classification in upper-half esophageal carcinoma. Ann Surg. 2004;240(6):962–72 (discussion 972–64).

    Article  CAS  Google Scholar 

  9. Fujita H, Kakegawa T, Yamana H, et al. Mortality and morbidity rates, postoperative course, quality of life, and prognosis after extended radical lymphadenectomy for esophageal cancer. Comparison of three-field lymphadenectomy with two-field lymphadenectomy. Ann Surg. 1995;222(5):654–62.

    Article  CAS  Google Scholar 

  10. Hulscher JB, van Sandick JW, de Boer AG, et al. Extended transthoracic resection compared with limited transhiatal resection for adenocarcinoma of the esophagus. New Engl J Med. 2002;347(21):1662–9.

    Article  Google Scholar 

  11. Cabanas RM. An approach for the treatment of penile carcinoma. Cancer. 1977;39(2):456–66.

    Article  CAS  Google Scholar 

  12. Morton DL, Wen DR, Wong JH, et al. Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg. (Chicago, Ill.: 1960). 1992;127(4):392–9.

  13. 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(6):335–9 (discussion 340).

    Article  CAS  Google Scholar 

  14. Izbicki JR, Hosch SB, Pichlmeier U, et al. Prognostic value of immunohistochemically identifiable tumor cells in lymph nodes of patients with completely resected esophageal cancer. New Engl J Med. 1997;337(17):1188–94.

    Article  CAS  Google Scholar 

  15. Lamb PJ, Griffin SM, Burt AD, Lloyd J, Karat D, Hayes N. Sentinel node biopsy to evaluate the metastatic dissemination of oesophageal adenocarcinoma. Br J Surg. 2005;92(1):60–7.

    Article  CAS  Google Scholar 

  16. Grotenhuis BA, Wijnhoven BP, van Marion R, et al. The sentinel node concept in adenocarcinomas of the distal esophagus and gastroesophageal junction. J Thorac Cardiovasc Surg. 2009;138(3):608–12.

    Article  Google Scholar 

  17. Uenosono Y, Arigami T, Yanagita S, et al. Sentinel node navigation surgery is acceptable for clinical T1 and N0 esophageal cancer. Ann Surg Oncol. 2011;18(7):2003–9.

    Article  Google Scholar 

  18. Kim HK, Kim S, Park JJ, Jeong JM, Mok YJ, Choi YH. Sentinel node identification using technetium-99 m neomannosyl human serum albumin in esophageal cancer. Ann Thorac Surg. 2011;91(5):1517–22.

    Article  Google Scholar 

  19. Hirche C, Murawa D, Mohr Z, Kneif S, Hunerbein M. ICG fluorescence-guided sentinel node biopsy for axillary nodal staging in breast cancer. Breast Cancer Res Treat. 2010;121(2):373–8.

    Article  Google Scholar 

  20. Jewell EL, Huang JJ, Abu-Rustum NR, et al. Detection of sentinel lymph nodes in minimally invasive surgery using indocyanine green and near-infrared fluorescence imaging for uterine and cervical malignancies. Gynecol Oncol. 2014;133(2):274–7.

    Article  Google Scholar 

  21. Tajima Y, Murakami M, Yamazaki K, et al. Sentinel node mapping guided by indocyanine green fluorescence imaging during laparoscopic surgery in gastric cancer. Ann Surg Oncol. 2010;17(7):1787–93.

    Article  Google Scholar 

  22. Yuasa Y, Seike J, Yoshida T, et al. Sentinel lymph node biopsy using intraoperative indocyanine green fluorescence imaging navigated with preoperative CT lymphography for superficial esophageal cancer. Ann Surg Oncol. 2012;19(2):486–93.

    Article  Google Scholar 

  23. Hachey KJ, Gilmore DM, Armstrong KW, et al. Safety and feasibility of near-infrared image-guided lymphatic mapping of regional lymph nodes in esophageal cancer. J Thorac Cardiovasc Surg. 2016;152(2):546–54.

    Article  Google Scholar 

  24. Schlottmann F, Barbetta A, Mungo B, Lidor AO, Molena D. Identification of the lymphatic drainage pattern of esophageal cancer with near-infrared fluorescent imaging. J Laparoendosc Adv Surg Tech Part A. 2017;27(3):268–71.

    Article  Google Scholar 

  25. Gurfinkel M, Thompson AB, Ralston W, et al. Pharmacokinetics of ICG and HPPH-car for the detection of normal and tumor tissue using fluorescence, near-infrared reflectance imaging: a case study. Photochem Photobiol. 2000;72(1):94–102.

    Article  CAS  Google Scholar 

  26. Kirchherr AK, Briel A, Mader K. Stabilization of indocyanine green by encapsulation within micellar systems. Mol Pharm. 2009;6(2):480–91.

    Article  CAS  Google Scholar 

  27. Japanese Classification of Esophageal Cancer, 11th Edition: part I. Esophagus. 2017;14(1):1–36.

    Article  Google Scholar 

  28. Nagaraja V, Eslick GD, Cox MR. Sentinel lymph node in oesophageal cancer-a systematic review and meta-analysis. J Gastrointest Oncol. 2014;5(2):127–41.

    PubMed  PubMed Central  Google Scholar 

  29. Kitai T, Inomoto T, Miwa M, Shikayama T. Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer. Breast Cancer (Tokyo, Japan). 2005;12(3):211–5.

    Article  Google Scholar 

  30. Ogawa M, Kosaka N, Choyke PL, Kobayashi H. In vivo molecular imaging of cancer with a quenching near-infrared fluorescent probe using conjugates of monoclonal antibodies and indocyanine green. Cancer Res. 2009;69(4):1268–72.

    Article  CAS  Google Scholar 

  31. Ohnishi S, Lomnes SJ, Laurence RG, Gogbashian A, Mariani G, Frangioni JV. Organic alternatives to quantum dots for intraoperative near-infrared fluorescent sentinel lymph node mapping. Mol Imaging. 2005;4(3):172–81.

    Google Scholar 

  32. Schaafsma BE, van der Vorst JR, Gaarenstroom KN, et al. Randomized comparison of near-infrared fluorescence lymphatic tracers for sentinel lymph node mapping of cervical cancer. Gynecol Oncol. 2012;127(1):126–30.

    Article  Google Scholar 

  33. Takeuchi H, Kawakubo H, Takeda F, Omori T, Kitagawa Y. Sentinel node navigation surgery in early-stage esophageal cancer. Ann Thorac Cardiovasc Surg. 2012;18(4):306–13.

    Article  Google Scholar 

  34. Helminen O, Mrena J, Sihvo E. Near-infrared image-guided lymphatic mapping in minimally invasive oesophagectomy of distal oesophageal cancer. Eur J Cardio-Thorac Surg. 2017;52(5):952–7.

    Article  Google Scholar 

  35. Tachimori Y, Nagai Y, Kanamori N, Hokamura N, Igaki H. Pattern of lymph node metastases of esophageal squamous cell carcinoma based on the anatomical lymphatic drainage system. Dis Esophagus. 2011;24(1):33–8.

    Article  CAS  Google Scholar 

  36. Tachimori Y, Ozawa S, Numasaki H, et al. Efficacy of lymph node dissection by node zones according to tumor location for esophageal squamous cell carcinoma. Esophagus. 2016;13:1–7.

    Article  Google Scholar 

  37. Donohoe CL, Phillips AW. Cancer of the esophagus and esophagogastric junction: an 8(th) edition staging primer. J Thorac Dis. 2017;9(3):E282–4.

    Article  Google Scholar 

Download references

Acknowledgement

This study was supported by Shanghai Collaborative Innovation Center for Translational Medicine.

Disclosures

The authors have no conflict of interest.

Author information

Author notes

  1. Haoyao Jiang and Haohua Teng are co-first authors.

Authors and Affiliations

  1. Department of Thoracic Surgery, Section of Esophageal Surgery, Shanghai Chest Hospital, Shanghai Jiao Tong University, Shanghai, China

    Haoyao Jiang MD, Yifeng Sun MD, PhD, Xufeng Guo MD, PhD, Rong Hua MD, PhD, Yuchen Su MD, Bin Li MD, PhD, Bo Ye MD, PhD, Yu Yang MD & Zhigang Li MD, PhD

  2. Department of Pathology, Shanghai Chest Hospital, Shanghai Jiao Tong University, Shanghai, China

    Haohua Teng MD

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  1. Haoyao Jiang MD
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Correspondence to Zhigang Li MD, PhD.

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Jiang, H., Teng, H., Sun, Y. et al. Near-Infrared Fluorescent Image-Guided Lymphatic Mapping in Esophageal Squamous Cell Carcinoma. Ann Surg Oncol 27, 3799–3807 (2020). https://doi.org/10.1245/s10434-019-07969-6

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  • DOI: https://doi.org/10.1245/s10434-019-07969-6

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