Indocyanine green-based fluorescence imaging in visceral and hepatobiliary and pancreatic surgery: State of the art and future directions

Gian Luca Baiocchi, Michele Diana, Luigi Boni, Gian Luca Baiocchi, Michele Diana, Luigi Boni

Abstract

In recent years, the use of fluorescence-guided surgery (FGS) to treat benign and malignant visceral, hepatobiliary and pancreatic neoplasms has significantly increased. FGS relies on the fluorescence signal emitted by injected substances (fluorophores) after being illuminated by ad hoc laser sources to help guide the surgical procedure and provide the surgeon with real-time visualization of the fluorescent structures of interest that would be otherwise invisible. This review surveys and discusses the most common and emerging clinical applications of indocyanine green (ICG)-based fluorescence in visceral, hepatobiliary and pancreatic surgery. The analysis, findings, and discussion presented here rely on the authors' significant experience with this technique in their medical institutions, an up-to-date review of the most relevant articles published on this topic between 2014 and 2018, and lengthy discussions with key opinion leaders in the field during recent conferences and congresses. For each application, the benefits and limitations of this technique, as well as applicable future directions, are described. The imaging of fluorescence emitted by ICG is a simple, fast, relatively inexpensive, and harmless tool with numerous different applications in surgery for both neoplasms and benign pathologies of the visceral and hepatobiliary systems. The ever-increasing availability of visual systems that can utilize this tool will transform some of these applications into the standard of care in the near future. Further studies are needed to evaluate the strengths and weaknesses of each application of ICG-based fluorescence imaging in abdominal surgery.

Keywords: Biliary anatomy; Biliary surgery; Fluorescence imaging; Gastrointestinal surgery; Indocyanine green; Liver surgery; Pancreatic surgery; Peritoneal carcinomatosis; Visceral perfusion.

Conflict of interest statement

Conflict-of-interest statement: Baiocchi GL, Diana M, and Boni L have received no funding and declare no conflicts of interest in relation to this specific work. Baiocchi GL received a travel grant from Stryker and from Karl Storz and has been the scientific organizer of the international workshop “Intraoperative ICG Fluorescence Imaging in Hepatobiliary and Visceral Surgery: State of the Art and New Frontiers,” (Brescia, Italy, October 21, 2017) partly funded (travel expenses) by Karl Storz and Stryker companies. Diana M is the recipient of a grant from the ARC Foundation (Project ELIOS) to develop fluorescence image-guided surgery. Boni L is a consultant for Storz and Olympus.

Figures

Figure 1
Figure 1
Colon perfusion before anastomosis during left colectomy. A few seconds after the i.v. injection of 0.3 mg/kg indocyanine green, bowel arteries clearly appear (A); thereafter, the bowel perfusion cut-off area becomes evident (B and C).
Figure 2
Figure 2
Indocyanine green-enhanced biliary anatomy. During a difficult cholecystectomy for acute cholecystitis (A), the confluence between the cystic duct (CyD) and the common hepatic duct (CHD) is shown by fluorescence imaging (B); common hepatic duct (arrow) is further visualized before (C and D) and after (E and F) cystic duct division. ICG: Indocyanine green.
Figure 3
Figure 3
Indocyanine green in liver surgery. Primary liver tumors show intense and complete staining because their hepatocytes take up ICG but do not secrete it (A and B); liver metastases show a ring appearance because their cells do not take up ICG but hepatocytes surrounding the nodule are compressed (C and D). ICG: Indocyanine green.
Figure 4
Figure 4
Indocyanine green fluorescence imaging in extended right hemicolectomy. The figure displays the right branches of middle colic vessel division during extended right hemicolectomy for transverse colon cancer. ICG injected in the tumor site spreads in nodes at the very proximal root of the artery. ICG fluorescence imaging allows a radical lymphadenectomy, including very small nodes (A and B). Only when all the stained nodes are removed may the nodal dissection be considered radical (C). ICG: Indocyanine green.

References

    1. Diana M. Enabling precision digestive surgery with fluorescence imaging. Transl Gastroenterol Hepatol. 2017;2:97.
    1. Gioux S, Choi HS, Frangioni JV. Image-guided surgery using invisible near-infrared light: fundamentals of clinical translation. Mol Imaging. 2010;9:237–255.
    1. Nguyen QT, Tsien RY. Fluorescence-guided surgery with live molecular navigation--a new cutting edge. Nat Rev Cancer. 2013;13:653–662.
    1. Reinhart MB, Huntington CR, Blair LJ, Heniford BT, Augenstein VA. indocyanine green: historical context, current applications, and future considerations. Surg Innov. 2016;23:166–175.
    1. Starker PM, Chinn B. Using outcomes data to justify instituting new technology: a single institution’s experience. Surg Endosc. 2018;32:1586–1592.
    1. Gossedge G, Vallance A, Jayne D. Diverse applications for near infra-red intraoperative imaging. Colorectal Dis. 2015;17 Suppl 3:7–11.
    1. Boni L, Fingerhut A, Marzorati A, Rausei S, Dionigi G, Cassinotti E. Indocyanine green fluorescence angiography during laparoscopic low anterior resection: results of a case-matched study. Surg Endosc. 2017;31:1836–1840.
    1. Mangano A, Gheza F, Chen LL, Minerva EM, Giulianotti PC. Indocyanine green (Icg)-enhanced fluorescence for intraoperative assessment of bowel microperfusion during laparoscopic and robotic colorectal surgery: The quest for evidence-based results. Surg Technol Int. 2018;32:101–104.
    1. Ris F, Liot E, Buchs NC, Kraus R, Ismael G, Belfontali V, Douissard J, Cunningham C, Lindsey I, Guy R, et al. Multicentre phase II trial of near-infrared imaging in elective colorectal surgery. Br J Surg. 2018 Epub ahead of print.
    1. Hellan M, Spinoglio G, Pigazzi A, Lagares-Garcia JA. The influence of fluorescence imaging on the location of bowel transection during robotic left-sided colorectal surgery. Surg Endosc. 2014;28:1695–1702.
    1. Kin C, Vo H, Welton L, Welton M. Equivocal effect of intraoperative fluorescence angiography on colorectal anastomotic leaks. Dis Colon Rectum. 2015;58:582–587.
    1. Sujatha-Bhaskar S, Jafari MD, Stamos MJ. The role of fluorescent angiography in anastomotic leaks. Surg Technol Int. 2017;30:83–88.
    1. Kumagai Y, Ishiguro T, Haga N, Kuwabara K, Kawano T, Ishida H. Hemodynamics of the reconstructed gastric tube during esophagectomy: assessment of outcomes with indocyanine green fluorescence. World J Surg. 2014;38:138–143.
    1. Karampinis I, Ronellenfitsch U, Mertens C, Gerken A, Hetjens S, Post S, Kienle P, Nowak K. Indocyanine green tissue angiography affects anastomotic leakage after esophagectomy. A retrospective, case-control study. Int J Surg. 2017;48:210–214.
    1. Kitagawa H, Namikawa T, Iwabu J, Fujisawa K, Uemura S, Tsuda S, Hanazaki K. Assessment of the blood supply using the indocyanine green fluorescence method and postoperative endoscopic evaluation of anastomosis of the gastric tube during esophagectomy. Surg Endosc. 2018;32:1749–1754.
    1. Koyanagi K, Ozawa S, Oguma J, Kazuno A, Yamazaki Y, Ninomiya Y, Ochiai H, Tachimori Y. Blood flow speed of the gastric conduit assessed by indocyanine green fluorescence: New predictive evaluation of anastomotic leakage after esophagectomy. Medicine (Baltimore) 2016;95:e4386.
    1. Frattini F, Lavazza M, Mangano A, Amico F, Rausei S, Rovera F, Boni L, Dionigi G. Indocyanine green-enhanced fluorescence in laparoscopic sleeve gastrectomy. Obes Surg. 2015;25:949–950.
    1. Irie T, Matsutani T, Hagiwara N, Nomura T, Fujita I, Kanazawa Y, Kakinuma D, Uchida E. Successful treatment of non-occlusive mesenteric ischemia with indocyanine green fluorescence and open-abdomen management. Clin J Gastroenterol. 2017;10:514–518.
    1. Ishizawa T, Bandai Y, Ijichi M, Kaneko J, Hasegawa K, Kokudo N. Fluorescent cholangiography illuminating the biliary tree during laparoscopic cholecystectomy. Br J Surg. 2010;97:1369–1377.
    1. Ashitate Y, Stockdale A, Choi HS, Laurence RG, Frangioni JV. Real-time simultaneous near-infrared fluorescence imaging of bile duct and arterial anatomy. J Surg Res. 2012;176:7–13.
    1. Pesce A, Piccolo G, La Greca G, Puleo S. Utility of fluorescent cholangiography during laparoscopic cholecystectomy: A systematic review. World J Gastroenterol. 2015;21:7877–7883.
    1. Vlek SL, van Dam DA, Rubinstein SM, de Lange-de Klerk ESM, Schoonmade LJ, Tuynman JB, Meijerink WJHJ, Ankersmit M. Biliary tract visualization using near-infrared imaging with indocyanine green during laparoscopic cholecystectomy: results of a systematic review. Surg Endosc. 2017;31:2731–2742.
    1. Osayi SN, Wendling MR, Drosdeck JM, Chaudhry UI, Perry KA, Noria SF, Mikami DJ, Needleman BJ, Muscarella P 2nd, Abdel-Rasoul M, Renton DB, Melvin WS, Hazey JW, Narula VK. Near-infrared fluorescent cholangiography facilitates identification of biliary anatomy during laparoscopic cholecystectomy. Surg Endosc. 2015;29:368–375.
    1. Liu YY, Kong SH, Diana M, Lègner A, Wu CC, Kameyama N, Dallemagne B, Marescaux J. Near-infrared cholecysto-cholangiography with indocyanine green may secure cholecystectomy in difficult clinical situations: proof of the concept in a porcine model. Surg Endosc. 2016;30:4115–4123.
    1. Liu YY, Liao CH, Diana M, Wang SY, Kong SH, Yeh CN, Dallemagne B, Marescaux J, Yeh TS. Near-infrared cholecystocholangiography with direct intragallbladder indocyanine green injection: preliminary clinical results. Surg Endosc. 2018;32:1506–1514.
    1. van den Bos J, Schols RM, Luyer MD, van Dam RM, Vahrmeijer AL, Meijerink WJ, Gobardhan PD, van Dam GM, Bouvy ND, Stassen LP. Near-infrared fluorescence cholangiography assisted laparoscopic cholecystectomy versus conventional laparoscopic cholecystectomy (FALCON trial): study protocol for a multicentre randomised controlled trial. BMJ Open. 2016;6:e011668.
    1. Verbeek FP, Schaafsma BE, Tummers QR, van der Vorst JR, van der Made WJ, Baeten CI, Bonsing BA, Frangioni JV, van de Velde CJ, Vahrmeijer AL, et al. Optimization of near-infrared fluorescence cholangiography for open and laparoscopic surgery. Surg Endosc. 2014;28:1076–1082.
    1. Hiwatashi K, Ueno S, Sakoda M, Iino S, Minami K, Mori S, Kita Y, Baba K, Kurahara H, Mataki Y, et al. The evaluation of liver function and surgical influence by ICGR15 after chemotherapy for colorectal liver metastases. J Cancer. 2016;7:595–599.
    1. Levesque E, Martin E, Dudau D, Lim C, Dhonneur G, Azoulay D. Current use and perspective of indocyanine green clearance in liver diseases. Anaesth Crit Care Pain Med. 2016;35:49–57.
    1. Ishizawa T, Fukushima N, Shibahara J, Masuda K, Tamura S, Aoki T, Hasegawa K, Beck Y, Fukayama M, Kokudo N. Real-time identification of liver cancers by using indocyanine green fluorescent imaging. Cancer. 2009;115:2491–2504.
    1. Gotoh K, Yamada T, Ishikawa O, Takahashi H, Eguchi H, Yano M, Ohigashi H, Tomita Y, Miyamoto Y, Imaoka S. A novel image-guided surgery of hepatocellular carcinoma by indocyanine green fluorescence imaging navigation. J Surg Oncol. 2009;100:75–79.
    1. Kaibori M, Matsui K, Ishizaki M, Iida H, Sakaguchi T, Tsuda T, Okumura T, Inoue K, Shimada S, Ohtsubo S, et al. Evaluation of fluorescence imaging with indocyanine green in hepatocellular carcinoma. Cancer Imaging. 2016;16:6.
    1. Shimada S, Ohtsubo S, Ogasawara K, Kusano M. Macro- and microscopic findings of ICG fluorescence in liver tumors. World J Surg Oncol. 2015;13:198.
    1. Lim C, Vibert E, Azoulay D, Salloum C, Ishizawa T, Yoshioka R, Mise Y, Sakamoto Y, Aoki T, Sugawara Y, et al. Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications. J Visc Surg. 2014;151:117–124.
    1. Peloso A, Franchi E, Canepa MC, Barbieri L, Briani L, Ferrario J, Bianco C, Quaretti P, Brugnatelli S, Dionigi P, et al. Combined use of intraoperative ultrasound and indocyanine green fluorescence imaging to detect liver metastases from colorectal cancer. HPB (Oxford) 2013;15:928–934.
    1. Abo T, Nanashima A, Tobinaga S, Hidaka S, Taura N, Takagi K, Arai J, Miyaaki H, Shibata H, Nagayasu T. Usefulness of intraoperative diagnosis of hepatic tumors located at the liver surface and hepatic segmental visualization using indocyanine green-photodynamic eye imaging. Eur J Surg Oncol. 2015;41:257–264.
    1. Terasawa M, Ishizawa T, Mise Y, Inoue Y, Ito H, Takahashi Y, Saiura A. Applications of fusion-fluorescence imaging using indocyanine green in laparoscopic hepatectomy. Surg Endosc. 2017;31:5111–5118.
    1. Zhang YM, Shi R, Hou JC, Liu ZR, Cui ZL, Li Y, Wu D, Shi Y, Shen ZY. Liver tumor boundaries identified intraoperatively using real-time indocyanine green fluorescence imaging. J Cancer Res Clin Oncol. 2017;143:51–58.
    1. Harada N, Ishizawa T, Muraoka A, Ijichi M, Kusaka K, Shibasaki M, Yamamoto K, Hasegawa K, Bandai Y, Kokudo N. Fluorescence navigation hepatectomy by visualization of localized cholestasis from bile duct tumor infiltration. J Am Coll Surg. 2010;210:e2–e6.
    1. Kaibori M, Ishizaki M, Matsui K, Kwon AH. Intraoperative indocyanine green fluorescent imaging for prevention of bile leakage after hepatic resection. Surgery. 2011;150:91–98.
    1. Kobayashi Y, Kawaguchi Y, Kobayashi K, Mori K, Arita J, Sakamoto Y, Hasegawa K, Kokudo N. Portal vein territory identification using indocyanine green fluorescence imaging: Technical details and short-term outcomes. J Surg Oncol. 2017;116:921–931.
    1. Diana M, Liu YY, Pop R, Kong SH, Legnèr A, Beaujeux R, Pessaux P, Soler L, Mutter D, Dallemagne B, et al. Superselective intra-arterial hepatic injection of indocyanine green (ICG) for fluorescence image-guided segmental positive staining: experimental proof of the concept. Surg Endosc. 2017;31:1451–1460.
    1. Ueno M, Hayami S, Sonomura T, Tanaka R, Kawai M, Hirono S, Okada KI, Yamaue H. Indocyanine green fluorescence imaging techniques and interventional radiology during laparoscopic anatomical liver resection (with video) Surg Endosc. 2018;32:1051–1055.
    1. Benedicenti S, Molfino S, Alfano MS, Molteni B, Porsio P, Portolani N, Baiocchi GL. Indocyanine green fluorescence-guided liver resection of metastasis from squamous cell carcinoma invading the biliary tree. Case Reports Gastrointest Med. 2018:In press.
    1. 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.
    1. Satou S, Ishizawa T, Masuda K, Kaneko J, Aoki T, Sakamoto Y, Hasegawa K, Sugawara Y, Kokudo N. Indocyanine green fluorescent imaging for detecting extrahepatic metastasis of hepatocellular carcinoma. J Gastroenterol. 2013;48:1136–1143.
    1. Watanabe M, Murakami M, Ozawa Y, Yoshizawa S, Matsui N, Aoki T. Intraoperative identification of colonic tumor sites using a near-infrared fluorescence endoscopic imaging system and indocyanine green. Dig Surg. 2017;34:495–501.
    1. Nagata J, Fukunaga Y, Akiyoshi T, Konishi T, Fujimoto Y, Nagayama S, Yamamoto N, Ueno M. Colonic marking with near-infrared, light-emitting, diode-activated indocyanine green for laparoscopic colorectal surgery. Dis Colon Rectum. 2016;59:e14–e18.
    1. 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;25:103–108.
    1. 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.
    1. 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.
    1. 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.
    1. Cahill RA, Anderson M, Wang LM, Lindsey I, Cunningham C, Mortensen NJ. Near-infrared (NIR) laparoscopy for intraoperative lymphatic road-mapping and sentinel node identification during definitive surgical resection of early-stage colorectal neoplasia. Surg Endosc. 2012;26:197–204.
    1. Sartori CA, Dal Pozzo A, Franzato B, Balduino M, Sartori A, Baiocchi GL. Laparoscopic total mesorectal excision for rectal cancer: experience of a single center with a series of 174 patients. Surg Endosc. 2011;25:508–514.
    1. Nishigori N, Koyama F, Nakagawa T, Nakamura S, Ueda T, Inoue T, Kawasaki K, Obara S, Nakamoto T, Fujii H, et al. Visualization of lymph/blood flow in laparoscopic colorectal cancer surgery by ICG fluorescence imaging (Lap-IGFI) Ann Surg Oncol. 2016;23 Suppl 2:S266–S274.
    1. Watanabe J, Ota M, Suwa Y, Ishibe A, Masui H, Nagahori K. Real-time indocyanine green fluorescence imaging-guided complete mesocolic excision in laparoscopic flexural colon cancer surgery. Dis Colon Rectum. 2016;59:701–705.
    1. Watanabe J, Ota M, Suwa Y, Ishibe A, Masui H, Nagahori K. Evaluation of lymph flow patterns in splenic flexural colon cancers using laparoscopic real-time indocyanine green fluorescence imaging. Int J Colorectal Dis. 2017;32:201–207.
    1. Kamiya S, Takeuchi H, Nakahara T, Niihara M, Nakamura R, Takahashi T, Wada N, Kawakubo H, Saikawa Y, Omori T, et al. Auxiliary diagnosis of lymph node metastasis in early gastric cancer using quantitative evaluation of sentinel node radioactivity. Gastric Cancer. 2016;19:1080–1087.
    1. Liberale G, Bourgeois P, Larsimont D, Moreau M, Donckier V, Ishizawa T. Indocyanine green fluorescence-guided surgery after IV injection in metastatic colorectal cancer: A systematic review. Eur J Surg Oncol. 2017;43:1656–1667.
    1. Rho SY, Kim JS, Chong JU, Hwang HK, Yoon DS, Lee WJ, Kang CM. Indocyanine green perfusion imaging-guided laparoscopic pancreaticoduodenectomy: Potential application in retroperitoneal margin dissection. J Gastrointest Surg. 2018 Epub ahead of print.
    1. Hirono S, Tani M, Kawai M, Okada K, Miyazawa M, Shimizu A, Uchiyama K, Yamaue H. Identification of the lymphatic drainage pathways from the pancreatic head guided by indocyanine green fluorescence imaging during pancreaticoduodenectomy. Dig Surg. 2012;29:132–139.
    1. Paiella S, De Pastena M, Landoni L, Esposito A, Casetti L, Miotto M, Ramera M, Salvia R, Secchettin E, Bonamini D, et al. Is there a role for near-infrared technology in laparoscopic resection of pancreatic neuroendocrine tumors? Results of the COLPAN “colour-and-resect the pancreas” study. Surg Endosc. 2017;31:4478–4484.
    1. Filippello A, Porcheron J, Klein JP, Cottier M, Barabino G. Affinity of indocyanine green in the detection of colorectal peritoneal carcinomatosis. Surg Innov. 2017;24:103–108.
    1. Lieto E, Auricchio A, Cardella F, Mabilia A, Basile N, Castellano P, Orditura M, Galizia G. Fluorescence-guided surgery in the combined treatment of peritoneal carcinomatosis from colorectal cancer: Preliminary Results and Considerations. World J Surg. 2018;42:1154–1160.
    1. Cheng H, Chi C, Shang W, Rengaowa S, Cui J, Ye J, Jiang S, Mao Y, Zeng C, Huo H, et al. Precise integrin-targeting near-infrared imaging-guided surgical method increases surgical qualification of peritoneal carcinomatosis from gastric cancer in mice. Oncotarget. 2017;8:6258–6272.
    1. Liberale G, Vankerckhove S, Caldon MG, Ahmed B, Moreau M, Nakadi IE, Larsimont D, Donckier V, Bourgeois P; 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;264:1110–1115.

Source: PubMed

Sponsors en medewerkers

Medische omstandigheden

Geneesmiddelinterventies

3
Abonneren