Skip to main content

Near-infrared fluorescence-guided surgery using indocyanine green facilitates secure infrapyloric lymph node dissection during laparoscopic distal gastrectomy

Surgery Today volume 50, pages 1187–1196 (2020)Cite this article

Abstract

Purpose

We aimed to investigate the usefulness of near-infrared indocyanine green (ICG)-enhanced fluorescence guidance for infrapyloric LN dissection in laparoscopic distal gastrectomy.

Methods

This study enrolled patients with early gastric cancer scheduled for laparoscopic distal gastrectomy. After intraoperative submucosal injection of ICG (0.1 mg/mL), LN dissection was conducted under near-infrared ICG fluorescence guidance. The operation time, bleeding events during infrapyloric LN dissection were analyzed. Cases were retrospectively 1:3 propensity-score matched to patients who underwent laparoscopic distal gastrectomy without ICG injection.

Results

The mean time from midline omentectomy to exposure of the right gastroepiploic vein was significantly shorter in the ICG group (n = 20) than in the non-ICG group (n = 60) (13.05 ± 5.77 vs 18.68 ± 7.92 min; p = 0.001), and the incidence of bleeding during infrapyloric LN dissection was lower in the ICG group (20% vs 68.3%, p < 0.001). The two groups did not differ significantly regarding the number of LNs retrieved from the infrapyloric area (p = 0.434).

Conclusions

Near-infrared ICG fluorescence guidance facilitates safe and fast infrapyloric LN dissection in laparoscopic distal gastrectomy.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer. 2017;20:1–19.

    Article  Google Scholar 

  2. Shinohara H, Kurahashi Y, Kanaya S, Haruta S, Ueno M, Udagawa H, et al. Topographic anatomy and laparoscopic technique for dissection of no. 6 infrapyloric lymph nodes in gastric cancer surgery. Gastric Cancer. 2013;16:615–20.

    CAS  Article  Google Scholar 

  3. Shinohara H, Haruta S, Ohkura Y, Udagawa H, Sakai Y. Tracing dissectable layers of mesenteries overcomes embryologic restrictions when performing infrapyloric lymphadenectomy in laparoscopic gastric cancer surgery. J Am Coll Surg. 2015;220:e81–7.

    Article  Google Scholar 

  4. Shibasaki S, Suda K, Nakauchi M, Nakamura T, Kadoya S, Kikuchi K, et al. Outermost layer-oriented medial approach for infrapyloric nodal dissection in laparoscopic distal gastrectomy. Surg Endosc. 2018;32:2137–48.

    Article  Google Scholar 

  5. Matsuki M, Tanikake M, Kani H, Tatsugami F, Kanazawa S, Kanamoto T, et al. Dual-phase 3D CT angiography during a single breath-hold using 16-MDCT: assessment of vascular anatomy before laparoscopic gastrectomy. AJR Am J Roentgenol. 2006;186:1079–85.

    Article  Google Scholar 

  6. Natsume T, Shuto K, Yanagawa N, Akai T, Kawahira H, Hayashi H, et al. The classification of anatomic variations in the perigastric vessels by dual-phase CT to reduce intraoperative bleeding during laparoscopic gastrectomy. Surg Endosc. 2011;25:1420–4.

    Article  Google Scholar 

  7. Cao LL, Huang CM, Lu J, Zheng CH, Li P, Xie JW, et al. The impact of confluence types of the right gastroepiploic vein on no. 6 lymphadenectomy during laparoscopic radical gastrectomy. Medicine (Baltimore). 2015;94:e1383.

    Article  Google Scholar 

  8. Sano T, Sasako M, Katai H, Maruyama K. Amylase concentration of drainage fluid after total gastrectomy. Br J Surg. 1997;84:1310–2.

    CAS  Article  Google Scholar 

  9. Katai H, Yoshimura K, Fukagawa T, Sano T, Sasako M. Risk factors for pancreas-related abscess after total gastrectomy. Gastric Cancer. 2005;8:137–41.

    Article  Google Scholar 

  10. Miki Y, Tokunaga M, Bando E, Tanizawa Y, Kawamura T, Terashima M. Evaluation of postoperative pancreatic fistula after total gastrectomy with D2 lymphadenectomy by ISGPF classification. J Gastrointest Surg. 2011;15:1969–76.

    Article  Google Scholar 

  11. Kong SH, Noh YW, Suh YS, Park HS, Lee HJ, Kang KW, et al. Evaluation of the novel near-infrared fluorescence tracers pullulan polymer nanogel and indocyanine green/γ-glutamic acid complex for sentinel lymph node navigation surgery in large animal models. Gastric Cancer. 2015;18:55–64.

    CAS  Article  Google Scholar 

  12. Kim TH, Kong SH, Park JH, Son YG, Huh YJ, Suh YS, et al. 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;18:161–71.

    Article  Google Scholar 

  13. Desiderio J, Trastulli S, Gemini A, Di Nardo D, Palazzini G, Parisi A, et al. Fluorescence image-guided lymphadenectomy using indocyanine green and near infrared technology in robotic gastrectomy. Chin J Cancer Res. 2018;30:568–70.

    Article  Google Scholar 

  14. Huh YJ, Lee HJ, Kim TH, Choi YS, Park JH, Son YG, et al. Efficacy of assessing intraoperative bowel perfusion with near-infrared camera in laparoscopic gastric cancer surgery. J Laparoendosc Adv Surg Tech A. 2019;29:476–83.

    Article  Google Scholar 

  15. Kim M, Son SY, Cui LH, Shin HJ, Hur H, Han SU. Real-time vessel navigation using indocyanine green fluorescence during robotic or laparoscopic gastrectomy for gastric cancer. J Gastric Cancer. 2017;17:145–53.

    Article  Google Scholar 

  16. Lan YT, Huang KH, Chen PH, Liu CA, Lo SS, Wu CW, et al. A pilot study of lymph node mapping with indocyanine green in robotic gastrectomy for gastric cancer. SAGE Open Med. 2017;5:2050312117727444.

    Article  Google Scholar 

  17. Mitsumori N, Nimura H, Takahashi N, Kawamura M, Aoki H, Shida A, et al. Sentinel lymph node navigation surgery for early stage gastric cancer. World J Gastroenterol. 2014;20:5685–93.

    Article  Google Scholar 

  18. Miyashiro I, Hiratsuka M, Kishi K, Takachi K, Yano M, Takenaka A, et al. Intraoperative diagnosis using sentinel node biopsy with indocyanine green dye in gastric cancer surgery: an institutional trial by experienced surgeons. Ann Surg Oncol. 2013;20:542–6.

    Article  Google Scholar 

  19. Tsutsui N, Yoshida M, Kitajima M, Suzuki Y. Laparoscopic cholecystectomy using the PINPOINT® endoscopic fluorescence imaging system with intraoperative fluorescent imaging: a case report. Int J Surg Case Rep. 2016;21:129–32.

    Article  Google Scholar 

  20. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–13.

    Article  Google Scholar 

  21. Kim TH, Suh YS, Huh YJ, Son YG, Park JH, Yang JY, et al. The comprehensive complication index (CCI) is a more sensitive complication index than the conventional Clavien-Dindo classification in radical gastric cancer surgery. Gastric Cancer. 2018;21:171–81.

    Article  Google Scholar 

  22. Haruta S, Shinohara H, Ueno M, Udagawa H, Sakai Y, Uyama I. Anatomical considerations of the infrapyloric artery and its associated lymph nodes during laparoscopic gastric cancer surgery. Gastric Cancer. 2015;18:876–80.

    Article  Google Scholar 

  23. Xuan Y, Hur H, Byun CS, Han SU, Cho YK. Efficacy of intraoperative gastroscopy for tumor localization in totally laparoscopic distal gastrectomy for cancer in the middle third of the stomach. Surg Endosc. 2013;27:4364–70.

    Article  Google Scholar 

  24. Jin SH, Kim DY, Kim H, Jeong IH, Kim MW, Cho YK, et al. Multidimensional learning curve in laparoscopy-assisted gastrectomy for early gastric cancer. Surg Endosc. 2007;21:28–33.

    Article  Google Scholar 

  25. Lee HH, Song KY, Park CH, Jeon HM. Training of surgical endoscopists in Korea: assessment of the learning curve using a cumulative sum model. J Surg Educ. 2012;69(559–63):26.

    Google Scholar 

  26. Kim H, Lee SK, Kim YM, Lee EH, Lim SJ, Kim SH, et al. Fluorescent iodized emulsion for pre- and intraoperative sentinel lymph node imaging: validation in a preclinical model. Radiology. 2015;275:196–204.

    Article  Google Scholar 

  27. 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. Dig Surg. 2008;25:103–8.

    Article  Google Scholar 

  28. Rossi EC, Ivanova A, Boggess JF. Robotically assisted fluorescence-guided lymph node mapping with ICG407 for gynecologic malignancies: a feasibility study. Gynecol Oncol. 2012;124(1):78–82.

    Article  Google Scholar 

Download references

Acknowledgements

None.

Funding

This study was partly supported by Novadaq® Inc. (incorporated to Stryker Inc.). The funder had no role in study design, data analysis, or writing of this article.

Author information

Affiliations

  1. Department of Surgery, Seoul National University College of Medicine, 101 Daehark-ro, Jongno-gu, Seoul, 03080, Korea

    Shin-Hoo Park, Felix Berlth, Jong-Ho Choi, Ji-Hyeon Park, Yun-Suhk Suh, Seong-Ho Kong, Do Joong Park, Hyuk-Joon Lee & Han-Kwang Yang

  2. Department of General, Visceral and Transplant Surgery, Medical Center of the Johannes Gutenberg University, Mainz, Germany

    Felix Berlth

  3. Cancer Research Institute, Seoul National University College of Medicine, Seoul, Korea

    Hyuk-Joon Lee & Han-Kwang Yang

Authors
  1. Shin-Hoo Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Felix Berlth
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jong-Ho Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ji-Hyeon Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yun-Suhk Suh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Seong-Ho Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Do Joong Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hyuk-Joon Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Han-Kwang Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S-HP, J-HC, Y-SS, S-HK, DJP, H-KY: Substantial contributions to the conception or design of the work; or the acquisition, analysis, or interpretation of data for the work. S-HP, FB, J-HC, J-HP, Y-SS, S-HK, DJP, H-KY: Drafting the work or revising it critically for important intellectual content. S-HP, S-HK, H-JL, H-KY: Final approval of the version to be published. S-HP, FB, J-HC, J-HP, Y-SS, S-HK, DJP, H-JL, H-KY S-HP, FB, J-HC, J-HP, Y-SS, S-HK, DJP, H-JL, H-KY: Agreement to be 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 Han-Kwang Yang.

Ethics declarations

Conflict of interest

The authors have no competing interests to declare in relation to this paper. The authors have full control of all primary data and agree to allow the journal to review our data, if requested.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 Online Resource 1 Near-infrared fluorescence guidance using indocyanine green during infrapyloric lymph node dissection in laparoscopic distal gastrectomy for early gastric cancer (MPG 68474 kb)

595_2020_1993_MOESM2_ESM.docx

Supplementary file2 Online Resource 2 Percentage of patients with ICG fluorescence uptake at each LN station. ICG indocyanine green, LN lymph node. Online Resource 3 Time for ICG injection (minutes) over chronological cases (DOCX 342 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Park, SH., Berlth, F., Choi, JH. et al. Near-infrared fluorescence-guided surgery using indocyanine green facilitates secure infrapyloric lymph node dissection during laparoscopic distal gastrectomy. Surg Today 50, 1187–1196 (2020). https://doi.org/10.1007/s00595-020-01993-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00595-020-01993-w

Keywords

  • Indocyanine green
  • Laparoscopic surgery
  • Lymph node dissection
  • Near-infrared imaging
  • Gastric cancer