The Feasibility and Safety of Preoperative Fluorescence Marking with Indocyanine Green (ICG) in Laparoscopic Gastrectomy for Gastric Cancer
- 246 Downloads
Securing the surgical margin is the most essential and important task in curative surgery. However, it is difficult to accurately identify the tumor location during laparoscopic surgery for gastric cancer, and existing methods, such as preoperative endoscopic marking with tattooing and clipping, have multiple disadvantages.
We investigated the feasibility and safety of indocyanine green (ICG) fluorescence marking for determining the tumor location during laparoscopic gastrectomy.
We retrospectively analyzed preoperative and perioperative data from consecutive patients with gastric cancer undergoing planned laparoscopic distal gastrectomy. Data was maintained in a prospectively compiled surgical database, and patients were categorized into ICG (n = 84) or non-ICG (n = 174) groups based on whether they underwent preoperative endoscopic mucosal ICG injection. One-to-one propensity score matching (PSM) was performed to compare outcomes between the two groups.
We included 84 patient pairs after PSM, and there were no significant differences in preoperative patient characteristics. The ICG group had shorter procedure time (p < 0.001), lower estimated blood loss (p = 0.005), and significantly shorter postoperative hospital stay (p < 0.001). Positive resection margins were confirmed in five cases (6.0%) in the non-ICG group, whereas there were none in the ICG group (p = 0.008). Real-time confirmation was possible during laparoscopy, and the injected ICG did not affect the surgical procedure or result in adverse events.
ICG fluorescence imaging is feasible and safe and can potentially be used as a tumor-marking agent for determining the surgical resection line.
KeywordsGastric cancer Curative resection Indocyanine green fluorescence imaging Tumor localization Total laparoscopic gastrectomy
Ushimaru designed the study and wrote the initial draft of the manuscript. Omori contributed to the interpretation of the data and to the critical revision of the manuscript for important intellectual content. All the other authors (Fujiwara, Yanagimoto, Sugimura, Yamamoto, Moon, Miyata, Ohue, and Yano) contributed to data collection and interpretation and critical review of the manuscript. All the authors have read and approved the final version of the manuscript and have agreed to the accountability of all aspects of the study, ensuring that any queries related to the accuracy or integrity of any part of the work are answerable.
Compliance with Ethical Standards
This study was approved by the Institutional Review Board of the Osaka International Cancer Institute. All patients signed a written informed consent. Data collection and analysis were performed in compliance with the Helsinki Declaration of 1975.
Drs. Yuki Ushimaru, Takeshi Omori, Yoshiyuki Fujiwara, Yoshitomo Yanagimoto, Keijiro Sugimura, Kazuyoshi Yamamoto, Jeong-Ho Moon, Hiroshi Miyata, Masayuki Ohue, and Masahiko Yano have no conflicts of interest or financial ties to declare.
Conflict of Interest
There are no funding sources for this study or any associated financial conflicts.
- 2.Kojima F, Sato T, Tsunoda S, Takahata H, Hamaji M, Komatsu T et al. Development of a novel marking system for laparoscopic gastrectomy using endoclips with radio frequency identification tags: feasibility study in a canine model. Surg Endosc. 2014;28(9):2752–9. https://doi.org/10.1007/s00464-014-3501-2.CrossRefGoogle Scholar
- 3.Ohdaira T, Nagai H, Shibusawa H. Intraoperative localization of early-stage gastrointestinal tumors using a marking clip detector system. Surgical Technology International. 2005;14:79–83.Google Scholar
- 4.Matsuda T, Iwasaki T, Hirata K, Tsugawa D, Sugita Y, Ishida S et al. Simple and reliable method for tumor localization during totally laparoscopic gastrectomy: intraoperative laparoscopic ultrasonography combined with tattooing. Gastric Cancer. 2017;20(3):548–52. https://doi.org/10.1007/s10120-016-0635-z.CrossRefGoogle Scholar
- 5.Qi XD. [Gastroscopic mucosal biopsy and carbon ink injection marking for determination of resection line on the gastric wall in stomach cancer]. Zhonghua zhong liu za zhi [Chinese Journal of Oncology]. 1989;11(2):136–8.Google Scholar
- 6.Tokuhara T, Nakata E, Tenjo T, Kawai I, Satoi S, Inoue K et al. A novel option for preoperative endoscopic marking with India ink in totally laparoscopic distal gastrectomy for gastric cancer: a useful technique considering the morphological characteristics of the stomach. Molecular and clinical oncology. 2017;6(4):483–6. https://doi.org/10.3892/mco.2017.1191.CrossRefGoogle Scholar
- 10.Chung JW, Seo KW, Jung K, Park MI, Kim SE, Park SJ et al. A promising method for tumor localization during total laparoscopic distal gastrectomy: preoperative endoscopic clipping based on negative biopsy and selective intraoperative radiography findings. Journal of Gastric Cancer. 2017;17(3):220–7. https://doi.org/10.5230/jgc.2017.17.e25.CrossRefGoogle Scholar
- 11.Daskalaki D, Fernandes E, Wang X, Bianco FM, Elli EF, Ayloo S et al. Indocyanine green (ICG) fluorescent cholangiography during robotic cholecystectomy: results of 184 consecutive cases in a single institution. Surgical Innovation. 2014;21(6):615–21. https://doi.org/10.1177/1553350614524839.CrossRefGoogle Scholar
- 12.Spinoglio G, Priora F, Bianchi PP, Lucido FS, Licciardello A, Maglione V et al. Real-time near-infrared (NIR) fluorescent cholangiography in single-site robotic cholecystectomy (SSRC): a single-institutional prospective study. Surg Endosc. 2013;27(6):2156–62. https://doi.org/10.1007/s00464-012-2733-2.CrossRefGoogle Scholar
- 13.Luo S, Zhang E, Su Y, Cheng T, Shi C. A review of NIR dyes in cancer targeting and imaging. Biomaterials. 2011;32(29):7127–38. https://doi.org/10.1016/j.biomaterials.2011.06.024.CrossRefGoogle Scholar
- 16.Goto O, Takeuchi H, Kawakubo H, Matsuda S, Kato F, Sasaki M et al. Feasibility of non-exposed endoscopic wall-inversion surgery with sentinel node basin dissection as a new surgical method for early gastric cancer: a porcine survival study. Gastric Cancer. 2015;18(2):440–5. https://doi.org/10.1007/s10120-014-0358-y.CrossRefGoogle Scholar
- 20.Yano K, Nimura H, Mitsumori N, Takahashi N, Kashiwagi H, Yanaga K. The efficiency of micrometastasis by sentinel node navigation surgery using indocyanine green and infrared ray laparoscopy system for gastric cancer. Gastric Cancer. 2012;15(3):287–91. https://doi.org/10.1007/s10120-011-0105-6.CrossRefGoogle Scholar
- 25.Kanaya S, Kawamura Y, Kawada H, Iwasaki H, Gomi T, Satoh S et al. The delta-shaped anastomosis in laparoscopic distal gastrectomy: analysis of the initial 100 consecutive procedures of intracorporeal gastroduodenostomy. Gastric Cancer. 2011;14(4):365–71. https://doi.org/10.1007/s10120-011-0054-0.CrossRefGoogle Scholar
- 26.Kitagami H, Morimoto M, Nozawa M, Nakamura K, Tanimura S, Murakawa K et al. Evaluation of the delta-shaped anastomosis in laparoscopic distal gastrectomy: midterm results of a comparison with Roux-en-Y anastomosis. Surg Endosc. 2014;28(7):2137–44. https://doi.org/10.1007/s00464-014-3445-6.CrossRefGoogle Scholar
- 29.Squires MH, 3rd, Kooby DA, Pawlik TM, Weber SM, Poultsides G, Schmidt C et al. Utility of the proximal margin frozen section for resection of gastric adenocarcinoma: a 7-Institution Study of the US Gastric Cancer Collaborative. Ann Surg Oncol. 2014;21(13):4202–10. https://doi.org/10.1245/s10434-014-3834-z.CrossRefGoogle Scholar
- 30.Kim MG, Lee JH, Ha TK, Kwon SJ. The distance of proximal resection margin dose not significantly influence on the prognosis of gastric cancer patients after curative resection. Annals of Surgical Treatment and Research. 2014;87(5):223–31. https://doi.org/10.4174/astr.2014.87.5.223.CrossRefGoogle Scholar
- 31.Bissolati M, Desio M, Rosa F, Rausei S, Marrelli D, Baiocchi GL et al. Risk factor analysis for involvement of resection margins in gastric and esophagogastric junction cancer: an Italian multicenter study. Gastric Cancer. 2017;20(1):70–82. https://doi.org/10.1007/s10120-015-0589-6.CrossRefGoogle Scholar
- 32.Hur H, Son SY, Cho YK, Han SU. Intraoperative gastroscopy for tumor localization in laparoscopic surgery for gastric adenocarcinoma. Journal of Visualized Experiments: JoVE. 2016(114). https://doi.org/10.3791/53170.
- 38.Yoshida M, Kubota K, Kuroda J, Ohta K, Nakamura T, Saito J et al. Indocyanine green injection for detecting sentinel nodes using color fluorescence camera in the laparoscopy-assisted gastrectomy. Journal of Gastroenterology and Hepatology. 2012;27 Suppl 3:29–33. https://doi.org/10.1111/j.1440-1746.2012.07067.x.CrossRefGoogle Scholar
- 41.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(2):542–6. https://doi.org/10.1245/s10434-012-2608-8.CrossRefGoogle Scholar
- 42.Miyashiro I, Hiratsuka M, Sasako M, Sano T, Mizusawa J, Nakamura K et al. High false-negative proportion of intraoperative histological examination as a serious problem for clinical application of sentinel node biopsy for early gastric cancer: final results of the Japan Clinical Oncology Group multicenter trial JCOG0302. Gastric Cancer. 2014;17(2):316–23. https://doi.org/10.1007/s10120-013-0285-3.CrossRefGoogle Scholar