Download PDF
Digestive Disease Interventions 2021; 05(03): 216-221
DOI: 10.1055/s-0041-1723806
Review Article

Indocyanine Green Use in the Minimally Invasive Gastrointestinal Surgery

Francisco A. Ferri
1   Department of General Surgery and the Bariatric and Metabolic Institute, Cleveland Clinic, Weston, Florida
,
Samuel Szomstein
1   Department of General Surgery and the Bariatric and Metabolic Institute, Cleveland Clinic, Weston, Florida
› Author Affiliations
› Further Information
Also available at
    Permissions and Reprints

Abstract

Indocyanine green (ICG) is a fluorescent dye that has been used in some medical specialties already for almost 60 years and has gained popularity in recent years due to the clinical applications recently proposed in the surgical field. This review article details the current use of the ICG in the minimally invasive gastrointestinal surgery. There is abundant evidence validating the usefulness of ICG fluorescence angiography in the gastrointestinal surgery, leading to a decrease of complications. Other uses, such as its lymphographic use for sentinel lymph node mapping or detection of metastatic lymph nodes, need further investigation to prove its benefit. The heterogeneity and subjective nature of the data remain the greatest challenge when analyzing the possible effects ICG can bring to the gastrointestinal surgery.

Keywords

indocyanine green - ICG - fluorescence imaging


Publication History

Received: 23 September 2020

Accepted: 31 December 2020

Article published online:
11 February 2021

© 2021. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 Alander JT, Kaartinen I, Laakso A. et al. A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging 2012; 2012: 940585
    CrossrefPubMedGoogle Scholar
  • 2 Reinhart MB, Huntington CR, Blair LJ, Heniford BT, Augenstein VA. Indocyanine green: historical context, current applications, and future considerations. Surg Innov 2016; 23 (02) 166-175
    CrossrefPubMedGoogle Scholar
  • 3 Yannuzzi LA. Indocyanine green angiography: a perspective on use in the clinical setting. Am J Ophthalmol 2011; 151 (05) 745.e1-751.e1
    CrossrefPubMedGoogle Scholar
  • 4 Engel E, Schraml R, Maisch T. et al. Light-induced decomposition of indocyanine green. Invest Ophthalmol Vis Sci 2008; 49 (05) 1777-1783
    CrossrefPubMedGoogle Scholar
  • 5 Lau CT, Au DM, Wong KKY. Application of indocyanine green in pediatric surgery. Pediatr Surg Int 2019; 35 (10) 1035-1041
    CrossrefPubMedGoogle Scholar
  • 6 Obinu A, Gavini E, Rassu G. et al. Indocyanine green loaded polymeric nanoparticles: physicochemical characterization and interaction studies with Caco-2 cell line by light and transmission electron microscopy. Nanomaterials (Basel) 2020; 10 (01) 133
    CrossrefPubMedGoogle Scholar
  • 7 Vettoretto N, Foglia E, Ferrario L. et al. Could fluorescence-guided surgery be an efficient and sustainable option? A SICE (Italian Society of Endoscopic Surgery) health technology assessment summary. Surg Endosc 2020; 34 (07) 3270-3284
    CrossrefPubMedGoogle Scholar
  • 8 Ladak F, Dang JT, Switzer N. et al. Indocyanine green for the prevention of anastomotic leaks following esophagectomy: a meta-analysis. Surg Endosc 2019; 33 (02) 384-394
    CrossrefPubMedGoogle Scholar
  • 9 Van Daele E, Van Nieuwenhove Y, Ceelen W. et al. Near-infrared fluorescence guided esophageal reconstructive surgery: a systematic review. World J Gastrointest Oncol 2019; 11 (03) 250-263
    CrossrefPubMedGoogle Scholar
  • 10 Slooter MD, Eshuis WJ, Cuesta MA, Gisbertz SS, van Berge Henegouwen MI. Fluorescent imaging using indocyanine green during esophagectomy to prevent surgical morbidity: a systematic review and meta-analysis. J Thorac Dis 2019; 11 (Suppl. 05) S755-S765
    CrossrefPubMedGoogle Scholar
  • 11 Kitagawa H, Namikawa T, Iwabu J. et al. Correlation between indocyanine green visualization time in the gastric tube and postoperative endoscopic assessment of the anastomosis after esophageal surgery. Surg Today 2020; 50 (11) 1375-1382
    CrossrefPubMedGoogle Scholar
  • 12 Koyanagi K, Ozawa S, Oguma J. et al. Blood flow speed of the gastric conduit assessed by indocyanine green fluorescence: new predictive evaluation of anastomotic leakage after esophagectomy. Medicine (Baltimore) 2016; 95 (30) e4386
    CrossrefPubMedGoogle Scholar
  • 13 Mori M, Shuto K, Hirano A. et al. A novel parameter identified using indocyanine green fluorescence angiography may contribute to predicting anastomotic leakage in gastric cancer surgery. World J Surg 2020; 44 (08) 2699-2708
    CrossrefPubMedGoogle Scholar
  • 14 Yamana I, Murakami T, Ryu S. et al. Subtotal gastrectomy for gastric tube cancer using intraoperative indocyanine green fluorescence method. Int J Surg Case Rep 2020; 71: 290-293
    CrossrefPubMedGoogle Scholar
  • 15 Hirota M, Tomimaru Y, Nagase H. et al. A case of resection of a metastatic tumor combined with the spleen, preserving the remnant stomach, for recurrent gastric cancer of the splenic hilar region after distal gastrectomy [in Japanese]. Gan To Kagaku Ryoho 2020; 47 (02) 322-324
    PubMedGoogle Scholar
  • 16 Ezaki S, Tomimaru Y, Noguchi K. et al. Intraoperative assessment of blood flow in the remnant stomach using indocyanine green and regional oxygen saturation monitoring at distal pancreatectomy following gastrectomy [in Japanese]. Gan To Kagaku Ryoho 2019; 46 (13) 2045-2047
    PubMedGoogle Scholar
  • 17 Chen QY, Xie JW, Zhong Q. et al. Safety and efficacy of indocyanine green tracer-guided lymph node dissection during laparoscopic radical gastrectomy in patients with gastric cancer: a randomized clinical trial. JAMA Surg 2020; 155 (04) 300-311
    CrossrefPubMedGoogle Scholar
  • 18 Kwon IG, Son T, Kim HI, Hyung WJ. Fluorescent lymphography-guided lymphadenectomy during robotic radical gastrectomy for gastric cancer. JAMA Surg 2019; 154 (02) 150-158
    CrossrefPubMedGoogle Scholar
  • 19 Kim TH, Kong SH, Park JH. 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 (02) 161-171
    CrossrefPubMedGoogle Scholar
  • 20 Skubleny D, Dang JT, Skulsky S. et al. 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 Endosc 2018; 32 (06) 2620-2631
    CrossrefPubMedGoogle Scholar
  • 21 Kim DW, Jeong B, Shin IH. et al. Sentinel node navigation surgery using near-infrared indocyanine green fluorescence in early gastric cancer. Surg Endosc 2019; 33 (04) 1235-1243
    CrossrefPubMedGoogle Scholar
  • 22 Kinami S, Kosaka T. Laparoscopic sentinel node navigation surgery for early gastric cancer. Transl Gastroenterol Hepatol 2017; 2: 42
    CrossrefPubMedGoogle Scholar
  • 23 Mori M, Shuto K, Hirano A, Kosugi C, Narushima K, Koda K. Laparoscopic surgery for an esophageal duplication cyst using a near-infrared indocyanine green fluorescence system: a case report. Asian J Endosc Surg 2020; 13 (02) 211-214
    CrossrefPubMedGoogle Scholar
  • 24 Vecchiato M, Martino A, Sponza M. et al. Thoracic duct identification with indocyanine green fluorescence during minimally invasive esophagectomy with patient in prone position. Dis Esophagus 2020; 33 (12) doaa030
    CrossrefPubMedGoogle Scholar
  • 25 Matsutani T, Hirakata A, Nomura T. et al. Transabdominal approach for chylorrhea after esophagectomy by using fluorescence navigation with indocyanine green. Case Rep Surg 2014; 2014: 464017
    PubMedGoogle Scholar
  • 26 Kaburagi T, Takeuchi H, Oyama T. et al. Intraoperative fluorescence lymphography using indocyanine green in a patient with chylothorax after esophagectomy: report of a case. Surg Today 2013; 43 (02) 206-210
    CrossrefPubMedGoogle Scholar
  • 27 Yang F, Zhou J, Li H. et al. Near-infrared fluorescence-guided thoracoscopic surgical intervention for postoperative chylothorax. Interact Cardiovasc Thorac Surg 2018; 26 (02) 171-175
    CrossrefPubMedGoogle Scholar
  • 28 Karampinis I, Keese M, Jakob J. et al. Indocyanine green tissue angiography can reduce extended bowel resections in acute mesenteric ischemia. J Gastrointest Surg 2018; 22 (12) 2117-2124
    CrossrefPubMedGoogle Scholar
  • 29 Ishizuka M, Nagata H, Takagi K. et al. Usefulness of intraoperative observation using a fluorescence imaging instrument for patients with nonocclusive mesenteric ischemia. Int Surg 2015; 100 (04) 593-599
    CrossrefPubMedGoogle Scholar
  • 30 Nakagawa Y, Kobayashi K, Kuwabara S, Shibuya H, Nishimaki T. Use of indocyanine green fluorescence imaging to determine the area of bowel resection in non-occlusive mesenteric ischemia: a case report. Int J Surg Case Rep 2018; 51: 352-357
    CrossrefPubMedGoogle Scholar
  • 31 Ryu S, Yoshida M, Ohdaira H. et al. Intestinal blood flow assessment by indocyanine green fluorescence imaging in a patient with the incarcerated umbilical hernia: Report of a case. Ann Med Surg (Lond) 2016; 8: 40-42
    CrossrefPubMedGoogle Scholar
  • 32 Hirakawa M, Ishizuka R, Sato M. et al. Management of multiple arteriovenous malformations of the small bowel. Case Rep Med 2019; 2019: 2046857
    CrossrefPubMedGoogle Scholar
  • 33 Khan A, Choudhary G, Ivo T, Jeon H, Benedetti E. Real-time intraoperative assessment of microcirculation in living-donor small bowel transplant: a case report. Exp Clin Transplant 2019; (e-pub ahead of print) DOI: 10.6002/ect.2019.0039.
    CrossrefPubMedGoogle Scholar
  • 34 Ryu S, Yoshida M, Ohdaira H. et al. Blood flow evaluation using PINPOINT® in a case of incarcerated inguinal hernia: a case report. Asian J Endosc Surg 2017; 10 (01) 75-78
    CrossrefPubMedGoogle Scholar
  • 35 Liu YY, Pop R, Diana M. et al. Real-time fluorescence angiography by intra-arterial indocyanine green injection to identify obscure gastrointestinal bleeding territory: proof of concept in the porcine model. Surg Endosc 2016; 30 (05) 2143-2150
    CrossrefPubMedGoogle Scholar
  • 36 Jafari MD, Wexner SD, Martz JE. et al. Perfusion assessment in laparoscopic left-sided/anterior resection (PILLAR II): a multi-institutional study. J Am Coll Surg 2015; 220 (01) 82.e1-92.e1
    CrossrefPubMedGoogle Scholar
  • 37 Mizrahi I, Abu-Gazala M, Rickles AS. et al. Indocyanine green fluorescence angiography during low anterior resection for low rectal cancer: results of a comparative cohort study. Tech Coloproctol 2018; 22 (07) 535-540
    CrossrefPubMedGoogle Scholar
  • 38 Mizrahi I, de Lacy FB, Abu-Gazala M. et al. Transanal total mesorectal excision for rectal cancer with indocyanine green fluorescence angiography. Tech Coloproctol 2018; 22 (10) 785-791
    CrossrefPubMedGoogle Scholar
  • 39 Mizrahi I, Wexner SD. Clinical role of fluorescence imaging in colorectal surgery - a review. Expert Rev Med Devices 2017; 14 (01) 75-82
    CrossrefPubMedGoogle Scholar
  • 40 De Nardi P, Elmore U, Maggi G. et al. Intraoperative angiography with indocyanine green to assess anastomosis perfusion in patients undergoing laparoscopic colorectal resection: results of a multicenter randomized controlled trial. Surg Endosc 2020; 34 (01) 53-60
    CrossrefPubMedGoogle Scholar
  • 41 Arezzo A, Bonino MA, Ris F. et al. Intraoperative use of fluorescence with indocyanine green reduces anastomotic leak rates in rectal cancer surgery: an individual participant data analysis. Surg Endosc 2020; 34 (10) 4281-4290
    CrossrefPubMedGoogle Scholar
  • 42 Watanabe J, Ishibe A, Suwa Y. et al. Indocyanine green fluorescence imaging to reduce the risk of anastomotic leakage in laparoscopic low anterior resection for rectal cancer: a propensity score-matched cohort study. Surg Endosc 2020; 34 (01) 202-208
    CrossrefPubMedGoogle Scholar
  • 43 Amagai H, Miyauchi H, Muto Y. et al. Clinical utility of transanal indocyanine green near-infrared fluorescence imaging for evaluation of colorectal anastomotic perfusion. Surg Endosc 2019; 34 (12) 5283-5293
    CrossrefPubMedGoogle Scholar
  • 44 Alekseev M, Rybakov E, Shelygin Y, Chernyshov S, Zarodnyuk I. A study investigating the perfusion of colorectal anastomoses using fluorescence angiography: results of the FLAG randomized trial. Colorectal Dis 2020; 22 (09) 1147-1153
    CrossrefPubMedGoogle Scholar
  • 45 Otero-Piñeiro AM, de Lacy FB, Van Laarhoven JJ. et al. The impact of fluorescence angiography on anastomotic leak rate following transanal total mesorectal excision for rectal cancer: a comparative study. Surg Endosc 2021; 35 (02) 754-762
    CrossrefPubMedGoogle Scholar
  • 46 Su H, Wu H, Bao M. et al. Indocyanine green fluorescence imaging to assess bowel perfusion during totally laparoscopic surgery for colon cancer. BMC Surg 2020; 20 (01) 102
    CrossrefPubMedGoogle Scholar
  • 47 Munechika T, Kajitani R, Matsumoto Y. et al. Safety and effectiveness of high ligation of the inferior mesenteric artery for cancer of the descending colon under indocyanine green fluorescence imaging: a pilot study. Surg Endosc 2020; (e-pub ahead of print) DOI: 10.1007/s00464-020-07556-x.
    CrossrefPubMedGoogle Scholar
  • 48 Carrara A, Motter M, Amabile D. et al. Predictive value of the sentinel lymph node procedure in the staging of non-metastatic colorectal cancer. Int J Colorectal Dis 2020; 35 (10) 1921-1928
    CrossrefPubMedGoogle Scholar
  • 49 Emile SH, Elfeki H, Shalaby M. et al. Sensitivity and specificity of indocyanine green near-infrared fluorescence imaging in detection of metastatic lymph nodes in colorectal cancer: Systematic review and meta-analysis. J Surg Oncol 2017; 116 (06) 730-740
    CrossrefPubMedGoogle Scholar
  • 50 Villegas-Tovar E, Jimenez-Lillo J, Jimenez-Valerio V. et al. Performance of Indocyanine green for sentinel lymph node mapping and lymph node metastasis in colorectal cancer: a diagnostic test accuracy meta-analysis. Surg Endosc 2020; 34 (03) 1035-1047
    CrossrefPubMedGoogle Scholar
  • 51 Satoyoshi T, Okita K, Ishii M. et al. Timing of indocyanine green injection prior to laparoscopic colorectal surgery for tumor localization: a prospective case series. Surg Endosc 2020; (e-pub ahead of print) DOI: 10.1007/s00464-020-07443-5.
    CrossrefPubMedGoogle Scholar
  • 52 Liberale G, Vankerckhove S, Caldon MG. et al; Group R&D for the Clinical Application of Fluorescence Imaging of the Jules Bordet's Institute.. Fluorescence imaging after indocyanine green injection for detection of peritoneal metastases in patients undergoing cytoreductive surgery for peritoneal carcinomatosis from colorectal cancer: a pilot study. Ann Surg 2016; 264 (06) 1110-1115
    CrossrefPubMedGoogle Scholar
  • 53 Ortega CB, Guerron AD, Yoo JS. The use of fluorescence angiography during laparoscopic sleeve gastrectomy. JSLS 2018; 22 (02) e2018
    CrossrefPubMedGoogle Scholar
  • 54 Frattini F, Lavazza M, Mangano A. et al. Indocyanine green-enhanced fluorescence in laparoscopic sleeve gastrectomy. Obes Surg 2015; 25 (05) 949-950
    CrossrefPubMedGoogle Scholar
  • 55 Di Furia M, Romano L, Salvatorelli A. et al. Indocyanine green fluorescent angiography during laparoscopic sleeve gastrectomy: preliminary results. Obes Surg 2019; 29 (12) 3786-3790
    CrossrefPubMedGoogle Scholar
  • 56 Kalmar CL, Reed CM, Peery CL, Salzberg AD. Intraluminal indocyanine green for intraoperative staple line leak testing in bariatric surgery. Surg Endosc 2020; 34 (09) 4194-4199
    CrossrefPubMedGoogle Scholar
  • 57 Hagen ME, Diaper J, Douissard J. et al. Early experience with intraoperative leak test using a blend of methylene blue and indocyanine green during robotic gastric bypass surgery. Obes Surg 2019; 29 (03) 949-952
    CrossrefPubMedGoogle Scholar