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Sentinel Lymph Node Biopsy Using Intraoperative Indocyanine Green Fluorescence Imaging Navigated with Preoperative CT Lymphography for Superficial Esophageal Cancer

  • Gastrointestinal Oncology
  • Published:
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The sentinel lymph node (SLN) concept has been gaining attention for gastrointestinal neoplasms but remains controversial for esophageal cancer. This study evaluated the feasibility of SLN identification using intraoperative indocyanine green (ICG) fluorescence imaging (IGFI) navigated by preoperative computed tomographic lymphography (CTLG) to treat superficial esophageal cancer.


Subjects comprised 20 patients clinically diagnosed with superficial esophageal cancer. Five minutes after endoscopic submucosal injection of iopamidol around the primary lesion using a four-quadrant injection pattern with a 23-gauge endoscopic injection sclerotherapy needle, three-dimensional multidetector computed tomography was performed to identify SLNs and lymphatic routes. ICG solution was injected intraoperatively around the tumor. Fluorescence imaging was obtained by infrared ray electronic endoscopy. Thoracoscope-assisted standard radical esophagectomy with lymphadenectomy was performed to confirm fluorescent lymph nodes detected by CTLG.


Lymphatic vessels and SLNs were identified preoperatively using CTLG in all cases. Intraoperative detection rates were 100% using CTLG and 95% using IGFI. Lymph node metastases were found in four cases, including one false-negative case with SLNs occupied by bulky metastatic tumor that were not enhanced with both methods. The other 19 cases, including three cases of metastatic lymph nodes, were accurately identified by both procedures.


Preoperative CTLG visualized the correct number and site of SLNs in surrounding anatomy during routine computed tomography to evaluate distant metastases. Referring to CTLG, SLNs were identified using IGFI, resulting in successful SLN navigation and saving time and cost. This method appears clinically applicable as a less-invasive method for treating superficial esophageal cancer.

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  1. Morton DL, Thompson JF, Essner R, et al. Validation of the accuracy of intraoperative lymphatic mapping and sentinel lymphadenectomy for early-stage melanoma: a multicenter trial. Ann Surg. 1999;230:453–63.

    Article  PubMed  CAS  Google Scholar 

  2. Krag D, Weaver D, Ashikaga T, et al. The sentinel node in breast cancer—a multicenter validation study. N Eng J Med. 1998;339:941–6.

    Article  CAS  Google Scholar 

  3. Kitagawa Y, Fujii H, Mukai M, Kubota T, Otani Y, Kitajima M. Radio-guided sentinel node detection for gastric cancer. Br J Surg. 2002;89:604–8.

    Article  PubMed  CAS  Google Scholar 

  4. Schlag PM, Bembenek A, Schulze T. Sentinel node biopsy in gastrointestinal tract cancer. Eur J Cancer. 2004;40:2022–32.

    Article  PubMed  CAS  Google Scholar 

  5. Kitagawa Y, Fujii H, Kumai K, et al. Recent advances in sentinel node navigation for gastric cancer: a paradigm shift of surgical management. J Surg Oncol. 2005;90:147–52.

    Article  PubMed  Google Scholar 

  6. Tachibana M, Kinugasa S, Shibakita M, et al. Langenbecks surgical treatment of superficial esophageal cancer. Arch Surg. 2006;391:304–21.

    Article  Google Scholar 

  7. Ando N, Ozawa S, Kitagawa Y, Shinozawa Y, Kitajima M. Improvement in the results of surgical treatment of advanced squamous esophageal carcinoma during 15 consecutive years. Ann Surg. 2000;232:225–32.

    Article  PubMed  CAS  Google Scholar 

  8. Altorki NK, Skinner DB. Occult cervical nodal metastasis in esophageal cancer: preliminary series of the three-field lymphadenectomy. J Thorac Cardiovasc Surg. 1997;113:540–4.

    Article  PubMed  CAS  Google Scholar 

  9. Altorki N, Kent M, Ferrara C, Port J. Three-field lymph node dissection for squamous cell and adenocarcinoma of the esophagus. Ann Surg. 2002;236:177–83.

    Article  PubMed  Google Scholar 

  10. Fang W, Kato H, Tachimori Y, Igaki H, Sato H, Daiko H. Analysis of pulmonary complications after three-field lymph node dissection for esophageal cancer. Ann Thorac Surg. 2003;76:903–8.

    Article  PubMed  Google Scholar 

  11. 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;222:654–62.

    Article  PubMed  CAS  Google Scholar 

  12. Endo M, Yoshino K, Kawano T, Nagai K, Inoue H. Clinicopathological analysis of lymph node metastasis in surgically resected superficial cancer of the thoracic esophagus. Dis Esophagus. 2000;13:125–9.

    Article  PubMed  CAS  Google Scholar 

  13. Hayashi H, Tangoku A, Suga K, et al. CT Lymphography-navigated sentinel lymph node biopsy in patients with superficial esophageal cancer. Surgery. 2006;139:224–35.

    Article  PubMed  Google Scholar 

  14. Tangoku A, Seike J, Nakano K, et al. Current status of sentinel lymph node navigation surgery in breast and gastrointestinal tract. J Med Invest. 2007;54:1–18.

    Article  PubMed  Google Scholar 

  15. Tangoku A, Yamamoto S, Suga K, et al. Sentinel lymph node biopsy using computed tomography-lymphography in patients with breast cancer. Surgery. 2004;135:258–65.

    Article  PubMed  Google Scholar 

  16. Landsman ML, Kwant G, Mook GA, Zijlstra WG. Light-absorbing properties, stability, and spectral stabilization of indo-cyanine green. J Appl Physiol. 1976;40:575–83.

    PubMed  CAS  Google Scholar 

  17. Mordon S, Devoisselle JM, Soulie-Begu S, Desmettre T. Indo-cyanine green: physicochemical factors affecting its fluorescence in vivo. Microvasc Res. 1998;55:146–52.

    Article  PubMed  CAS  Google Scholar 

  18. Kusano M, Tajima Y, Yamazaki K, Kato M, Watanabe M, Miwa M. sentinel node mapping guided by indocyanine green fluorescence imaging: a new method for sentinel node navigation surgery in gastrointestinal cancer. Digest Surg. 2008;25:103–8.

    Article  Google Scholar 

  19. Tajima Y, Yamazaki K, Masuda Y, et al. Sentinel node mapping guided by indocyanine green fluorescence imaging in gastric cancer. Ann Surg. 2009;249:58–62.

    Article  PubMed  Google Scholar 

  20. Miyashiro I, Miyoshi N, Hiratsuka M, et al. Detection of sentinel node in gastric cancer surgery by indocyanine green fluorescence imaging: comparison with infrared imaging. Ann Surg Oncol. 2008;15:1640–3.

    Article  PubMed  Google Scholar 

  21. 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.

    Article  PubMed  Google Scholar 

  22. Parungo CP, Ohnishi S, Kim SW, et al. Intraoperative identification of esophageal sentinel lymph nodes with near-infrared fluorescence imaging. J Thorac Cardiovasc Surg. 2005;129:844–50.

    Article  PubMed  Google Scholar 

  23. Japan Esophageal Society. 2007 Guidelines for the clinical and pathologic studies on carcinoma of the esophagus. 10th ed. Tokyo: Kanehara Public.

    Google Scholar 

  24. Ueda K, Suga K, Kaneda Y, Li TS, Ueda K, Hamano K. Preoperative imaging of the lung sentinel lymphatic basin with computed tomographic lymphography: a preliminary study. Ann Thorac Surg. 2004;77:1033–7.

    Article  PubMed  Google Scholar 

  25. Grainger RG, Thomas AMK. History of the development of radiological contrast media (1895–1996). In: Dawson P, Cosgrove DO, Grainger RG, eds. Textbook of contrast media. Oxford: Isis Medical Media; 1999. p. 1–14.

    Google Scholar 

  26. Hayashi H, Ochiai T, Mori M, et al. Sentinel lymph node mapping for gastric cancer using a dual procedure with dye- and gamma probe–guided techniques. J Am Coll Surg. 2003;196:68–74.

    Article  PubMed  Google Scholar 

  27. Yasuda S, Shimada H, Chino O, et al. Sentinel lymph node detection with tc-99m tin colloids in patients with esophagogastric cancer. Jpn J Clin Oncol. 2003;33:68–72.

    Article  PubMed  Google Scholar 

  28. Takeuchi H, Fujii H, Ando N, et al. Validation study of radio-guided sentinel lymph node navigation in esophageal cancer. Ann Surg. 2009;249:757–63.

    Article  PubMed  Google Scholar 

  29. Albertini JJ, Lyman GH, Cox C. Lymphatic mapping and sentinel node biopsy in the patient with breast cancer. JAMA. 1996;276:1818–22.

    Article  PubMed  CAS  Google Scholar 

  30. Schwartz GF, Giuliano AE, Veronesi U; Consensus Conference Committee. Proceedings of the consensus conference on the role of sentinel lymph node biopsy in carcinoma of the breast, April 19 to 22, 2001, Philadelphia, Pennsylvania. Cancer. 2002;94:2542–51.

    Google Scholar 

  31. Burian M, Stein HJ, Siebert JR. Pattern of lymphatic spread of Barrett’s cancer. World J Surg. 2003;27:1052–7.

    Article  Google Scholar 

  32. Tangoku A, Yoshino S, Abe T, Hayashi H, Satou T, Ueno T, Oka M. Mediastinoscope-assisted transhiatal esophagectomy for esophageal cancer. Surg Endosc. 2004;18:383–9.

    Article  PubMed  CAS  Google Scholar 

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This work was supported by the Department of Radiology in the Institute of Health Bioscience at the University of Tokushima Graduate School. We are grateful for image processing and diagnostic advice provided by the department regarding CT images.

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Correspondence to Yasuhiro Yuasa MD.

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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 19, 486–493 (2012).

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