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The Clinical Value of Fluorescent Lymphography with Indocyanine Green During Robotic Surgery for Gastric Cancer: a Matched Cohort Study

Journal of Gastrointestinal Surgery volume 24, pages 2197–2203 (2020)Cite this article

Abstract

Background

Near-infrared (NIR) fluorescence imaging with indocyanine green (ICG) has been recently introduced for lymphatic mapping in several tumors. We aimed at investigating whether this technology may improve the intraoperative visualization of lymph nodes during robotic gastrectomy for gastric cancer.

Methods

Between June 2014 and June 2018, a total of 94 patients underwent robotic gastrectomy with D2 lymph node dissection for gastric cancer. In 37 patients, ICG was injected endoscopically into the submucosal layer around the tumor the day before surgery. After propensity score matching, the results of these 37 patients were compared with the results of 37 control patients who had undergone robotic gastrectomy without ICG injection.

Results

Among the 37 patients within the ICG group, no adverse events related to ICG injection or intraoperative NIR imaging occurred. After completion of D2 lymph node dissection, no residual fluorescent lymph nodes were left in the surgical field. A mean of 19.4 ± 14.7 fluorescent lymph nodes was identified per patient. The mean total number of harvested lymph nodes was significantly higher in the ICG group than in the control group (50.8 vs 40.1, P = 0.03). In the ICG group, 23 patients had metastatic lymph nodes. The accuracy, sensitivity, and specificity of ICG fluorescence for metastatic lymph nodes were 62.2%, 52.6%, and 63.0%, respectively.

Conclusion

Our study indicates that NIR imaging with ICG may provide additional node detection during robotic surgery for gastric cancer. Unfortunately, this technique failed to show good selectivity for metastatic lymph nodes.

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References

  1. Son T, Kwon IG and Hyung WJ. Minimally invasive surgery for gastric cancer treatment: current status and future perspectives. Gut Liver 2014;8:229–236.

    Article  Google Scholar 

  2. Strong VE, Devaud N, Karpeh M. The role of laparoscopy for gastric surgery in the West. Gastric Cancer 2009;2:127–131.

    Article  Google Scholar 

  3. Zou ZH, Zhao LY, Mou TY, Hu YF, Yu J, Liu H, Chen H, Wu JM, An SL, Li GX. Laparoscopic vs open D2 gastrectomy for locally advanced gastric cancer: a meta-analysis. World J Gastroenterol 2014;20:16750–16764.

    Article  Google Scholar 

  4. Alander JT, Kaartinen I, Laakso A, Patila T, Spillmann T, Tuchin VV, Venermo M, Välisuo P. A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging 2012;2012:940585.

    Article  Google Scholar 

  5. Majlesara A, Golriz M, Hafezi M, Saffari A, Stenau E, Maier-Hein L, Müller-Stich BP, Mehrabi A. Indocyanine green fluorescence imaging in hepatobiliary surgery. Photodiagnosis Photodyn Ther 2017;17:208–215.

    CAS  Article  Google Scholar 

  6. Keller DS, Ishizawa T, Cohen R, Chand M. Indocyanine green fluorescence imaging in colorectal surgery: overview, applications, and future directions. Lancet Gastroenterol Hepatol 2017;2:757–766.

    Article  Google Scholar 

  7. Nimura H, Narimiya N, Mitsumori N, Yamazaki Y, Yanaga K, Urashima M. Infrared ray electronic endoscopy combined with indocyanine green injection for detection of sentinel nodes of patients with gastric cancer. Br J Surg 2004;91:575–579.

    CAS  Article  Google Scholar 

  8. Kimmig R, Aktas B, Buderath P, Rusch P, Heubner M. Intraoperative navigation in robotically assisted compartmental surgery of uterine cancer by visualisation of embryologically derived lymphatic networks with indocyanine-green (ICG). J Surg Oncol 2016;113:554–559.

    CAS  Article  Google Scholar 

  9. Manny TB, Hemal AK. Fluorescence-enhanced robotic radical cystectomy using unconjugated indocyanine green for pelvic lymphangiography, tumor marking, and mesenteric angiography: the initial clinical experience. Urology 2014;83:824–829.

    Article  Google Scholar 

  10. Hachey KJ, Gilmore DM, Armstrong KW, Harris SE, Hornick JL, Colson YL, Wee JO. Safety and feasibility of near-infrared image-guided lymphatic mapping of regional lymph nodes in esophageal cancer. J Thorac Cardiovasc Surg 2016;152:546–554.

    Article  Google Scholar 

  11. Tajima Y, Yamazaki K, Masuda Y, Kato M, Yasuda D, Aoki T, Kato T, Murakami M, Miwa M, Kusano M. Sentinel node mapping guided by indocyanine green fluorescence imaging in gastric cancer. Ann Surg 2009;249:58–62.

    Article  Google Scholar 

  12. Tajima Y, Murakami M, Yamazaki K, Masuda Y, Kato M, Sato A, Goto S, Otsuka K, Kato T, Kusano M. Sentinel node mapping guided by indocyanine green fluorescence imaging during laparoscopic surgery in gastric cancer. Ann Surg Oncol 2010;17:1787–17893.

    Article  Google Scholar 

  13. Tummers QR, Boogerd LS, de Steur WO, Verbeek FP, Boonstra MC, Handgraaf HJ, Frangioni JV, van de Velde CJ, Hartgrink HH, Vahrmeijer AL. Near-infrared fluorescence sentinel lymph node detection in gastric cancer: A pilot study. World J Gastroenterol 2016;22:3644–3651.

    Article  Google Scholar 

  14. Skubleny D, Dang JT, Skulsky S, Switzer N, Tian C, Shi X, de Gara C, Birch DW, Karmali S. Diagnostic evaluation of sentinel lymph node biopsy using indocyanine green and infrared or fluorescent imaging in gastric cancer: a systematic review and meta-analysis. Surg End 2018;32:2620–2631.

    Article  Google Scholar 

  15. Kim TH, Kong SH, Park JH, Son YG, Huh YJ, Suh YS, Lee HJ, Yang HK. Assessment of the completeness of lymph node dissection using near-infrared imaging with indocyanine green in laparoscopic gastrectomy for gastric cancer. J Gastric Cancer 2018;18:161–171.

    Article  Google Scholar 

  16. Herrera-Almario G, Patane M, Sarkaria I, Strong VE. Initial report of near-infrared fluorescence imaging as an intraoperative adjunct for lymph node harvesting during robot-assisted laparoscopic gastrectomy. J Surg Oncol 2016; 113:768–770.

    CAS  Article  Google Scholar 

  17. Lan YT, Huang KH, Chen PH, Liu CA, Lo SS, Wu CW Shyr YM, Fang WL. A pilot study of lymph node mapping with indocyanine green in robotic gastrectomy for gastric cancer. SAGE Open Med 2017; 5:1–8.

    Article  Google Scholar 

  18. Japanese Gastric Cancer Association: Japanese classification of gastric carcinoma, 2nd English ed. Gastric Cancer 1998;1:10–24.

    CAS  Article  Google Scholar 

  19. Cianchi F, Indennitate G, Trallori G, Ortolani M, Paoli B, Macrì G, Lami G, Mallardi B, Badii B, Staderini F, Qirici E, Taddei A, Ringressi MN, Messerini L, Novelli L, Bagnoli S, Bonanomi A, Foppa C, Skalamera I, Fiorenza G, Perigli G. Robotic vs laparoscopic distal gastrectomy with D2 lymphadenectomy for gastric cancer: a retrospective comparative mono-institutional study. BMC Surg 2016; 16:65.

  20. Cianchi F, Indennitate G, Trallori G, Paoli B, Ortolani M, Taddei A, Lami G, Foppa C, Badii B, Novelli L, Skalamera I, Montanelli P, Coratti F, Perigli G, Staderini F. Lymph node mapping with near-infrared imaging during robotic surgery for gastric cancer: a pilot study. Ann Laparosc Endosc Surg 2018;3:31.

    Article  Google Scholar 

  21. Kinami S, Fujimura T, Ojima E, Fushida S, Ojima T, Funaki H, Fujita H, Takamura H, Ninomiya I, Nishimura G, Kayahara M, Ohta T, Yoh Z. PTD classification: proposal for a new classification of gastric cancer location based on physiological lymphatic flow. Int J Clin Oncol 2008; 13:320–329.

    Article  Google Scholar 

  22. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Troti A. AJCC Cancer staging manual, 7th edition. New York: Springer Verlag, 2010.

    Google Scholar 

  23. Wu CW, Hsiung CA, Lo SS, Hsieh MC, Chen JH, Li AF, Lui WY, Whang-Peng J. Nodal dissection for patients with gastric cancer: a randomized controlled trial. Lancet Oncol. 2006;7:309–315.

    CAS  Article  Google Scholar 

  24. Coburn NG. Lymph nodes and gastric cancer. J Surg Oncol. 2009; 99:199–206.

    Article  Google Scholar 

  25. Songun I, Outter H, Kranenbarg EM, Sasako M, van de Velde CJ. Surgical treatment of gastric cancer: 15-year follow up results of the randomized nationwide Dutch D1D2 trial. Lancet Oncol. 2010;11:439–449.

    Article  Google Scholar 

  26. Son T, Hyung WJ, Lee JH, Kim YM, Kim HI, An JY, Cheong JH, Noh SH. Clinical implication of an insufficient number of examined lymph nodes after curative resection for gastric cancer. Cancer. 2012;118:4687–4693.

    Article  Google Scholar 

  27. Verlato G, Roviello F, Marchet A, Giacopuzzi S, Marrelli D, Nitti D, de Manzoni G. Indexes of surgical quality in gastric cancer surgery: experience of an Italian network. Ann Surg Oncol. 2009;16:594–602.

    CAS  Article  Google Scholar 

  28. Takahashi N, Nimura H, Fujita T, Mitsumori N, Shiraishi N, Kitano S, Satodate H, Yanaga K. Laparoscopic sentinel node navigation surgery for early gastric cancer: a prospective multicenter trial. Langenbecks Arch Surg 2017;402:27–32

    Article  Google Scholar 

  29. Kinami S, Oonishi T, Fujita J, Tomita Y, Funaki H, Fujita H, Nakano Y, Ueda N, Kosaka T. Optimal settings and accuracy of indocyanine green fluorescence imaging for sentinel node biopsy in early gastric cancer. Oncol Lett 2016; 11:4055–4062.

    CAS  Article  Google Scholar 

  30. Kwon IG, Son T, Kim H-II, Hyung WJ. Fluorescent lymphography-guided lymphadenectomy during robotic radical gastrectomy for gastric cancer. JAMA Surg. 2018 Nov 14. https://doi.org/10.1001/jamasurg.2018.4267

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Affiliations

  1. Center for Oncological Minimally Invasive Surgery (COMIS), Department of Experimental and Clinical Medicine, University of Florence, Largo Brambilla 3, 50134, Florence, Italy

    Fabio Cianchi, Benedetta Badii, Ileana Skalamera, Tommaso Nelli, Francesco Coratti, Giuliano Perigli & Fabio Staderini

  2. IFCA, Florence, Italy

    Giampiero Indennitate, Beatrice Paoli & Manuela Ortolani

  3. Gastroenterology Unit, Careggi University Hospital, Florence, Italy

    Gabriele Lami & Natalia Manetti

  4. Gastroenterology Unit, San Giuseppe Hospital, Empoli, Italy

    Ottaviano Tarantino & Sara Messeri

  5. Humanitas Clinical and Research Hospital, Milan, Italy

    Caterina Foppa

  6. Pathology Unit, Careggi University Hospital, Florence, Italy

    Luca Novelli

Authors
  1. Fabio Cianchi
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  2. Giampiero Indennitate
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  3. Beatrice Paoli
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  4. Manuela Ortolani
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  10. Benedetta Badii
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  11. Luca Novelli
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Contributions

All authors have made substantial contributions to the conception of the work or the acquisition, analysis, or interpretation of the data for this work; drafted or revised the paper; and provided final approval of the version to be published. All authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Corresponding author

Correspondence to Fabio Cianchi.

Ethics declarations

All patients had been thoroughly informed about the study and gave their written consent for the investigation in compliance with the Helsinki Declaration and in accordance with the ethical committee of our University Hospital, Azienda Ospedaliero-Universitaria Careggi (Florence, Italy).

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The authors declare that they have no conflicts of interest.

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Cianchi, F., Indennitate, G., Paoli, B. et al. The Clinical Value of Fluorescent Lymphography with Indocyanine Green During Robotic Surgery for Gastric Cancer: a Matched Cohort Study. J Gastrointest Surg 24, 2197–2203 (2020). https://doi.org/10.1007/s11605-019-04382-y

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Keywords

  • Near-infrared fluorescence
  • Indocyanine green
  • Lymph node
  • Robotic gastrectomy
  • Gastric cancer