Skip to main content
Top
Published in: Surgical Endoscopy 10/2020

01-10-2020 | Ultrasound | Dynamic Manuscript

Laparoscopic anatomical liver resection guided by real-time indocyanine green fluorescence imaging: experience and lessons learned from the initial series in a single center

Authors: Yinzhe Xu, Mingyi Chen, Xiangfei Meng, Peng Lu, Xun Wang, Wenwen Zhang, Ying Luo, Weidong Duan, Shichun Lu, Hongguang Wang

Published in: Surgical Endoscopy | Issue 10/2020

Login to get access

Abstract

Background

Anatomical liver resection is an established procedure for primary hepatic tumors. Laparoscopic anatomical hepatectomy has been proven to be technically achievable from S1 to S8 in experienced hands. The indocyanine green (ICG) fluorescence imaging technique offers a novel tool of intraoperative visualization in hepatobiliary surgery. This study aims to investigate the feasibility of laparoscopic anatomical liver resection based on segmental staining using real-time ICG fluorescence.

Methods

From December 2015 to October 2017, 36 patients in our institute underwent lap-ALR using real-time ICG fluorescence mapping of the tumor-bearing portal territory. The procedural and perioperative data were collected and analyzed.

Results

In our case series, we successfully performed the fashion of positive staining mostly in segmentectomy or sub-segmentectomy by individually injecting 5–10 ml of ICG (0.025 mg/ml) into its feeding portal branch guided by intraoperative ultrasound, and the negative staining mainly for sectionectomy, hemihepatectomy and multi-segmentectomy by interrupting the Glissonean pedicle serving the tumor-bearing segments and systemically injecting 1 ml of ICG (2.5 mg/ml). Our total successful rate of staining is 53%. No conversion to laparotomy, Clavien III–IV complication or 90-day mortality occurred. Valuable technical feedback, experience and lessons are learned from this initial practice.

Conclusions

Real-time ICG fluorescence imaging adds much precision to laparoscopic anatomical hepatectomy. The success of segmental staining requires a high proficiency of IOUS and skillful interpretation of preoperative 3D simulation. Decision-making on the fashions of positive and negative staining have been initially recommended. Multi-centered practice and technical modification are necessary to standardize its application.
Appendix
Available only for authorised users
Literature
1.
go back to reference Makuuchi M, Hasegawa H, Yamazaki S (1985) Ultrasonically guided subsegmentectomy. Surg Gynecol Obstet 161:346–350PubMed Makuuchi M, Hasegawa H, Yamazaki S (1985) Ultrasonically guided subsegmentectomy. Surg Gynecol Obstet 161:346–350PubMed
2.
go back to reference Hasegawa K, Kokudo N, Imamura H, Matsuyama Y, Aoki T, Minagawa M, Sano K, Sugawara Y, Takayama T, Makuuchi M (2005) Prognostic impact of anatomic resection for hepatocellular carcinoma. Ann Surg 242:252–259CrossRef Hasegawa K, Kokudo N, Imamura H, Matsuyama Y, Aoki T, Minagawa M, Sano K, Sugawara Y, Takayama T, Makuuchi M (2005) Prognostic impact of anatomic resection for hepatocellular carcinoma. Ann Surg 242:252–259CrossRef
3.
go back to reference Agrawal S, Belghiti J (2011) Oncologic resection for malignant tumors of the liver. Ann Surg 253:656–665CrossRef Agrawal S, Belghiti J (2011) Oncologic resection for malignant tumors of the liver. Ann Surg 253:656–665CrossRef
4.
go back to reference Eguchi S, Kanematsu T, Arii S, Okazaki M, Okita K, Omata M, Ikai I, Kudo M, Kojiro M, Makuuchi M, Monden M, Matsuyama Y, Nakanuma Y, Takayasu K, Liver Cancer Study Group of J (2008) Comparison of the outcomes between an anatomical subsegmentectomy and a non-anatomical minor hepatectomy for single hepatocellular carcinomas based on a Japanese nationwide survey. Surgery. 143:469–475CrossRef Eguchi S, Kanematsu T, Arii S, Okazaki M, Okita K, Omata M, Ikai I, Kudo M, Kojiro M, Makuuchi M, Monden M, Matsuyama Y, Nakanuma Y, Takayasu K, Liver Cancer Study Group of J (2008) Comparison of the outcomes between an anatomical subsegmentectomy and a non-anatomical minor hepatectomy for single hepatocellular carcinomas based on a Japanese nationwide survey. Surgery. 143:469–475CrossRef
5.
go back to reference Dong J, Yang S, Zeng J, Cai S, Ji W, Duan W, Zhang A, Ren W, Xu Y, Tan J, Bu X, Zhang N, Wang X, Wang X, Meng X, Jiang K, Gu W, Huang Z (2013) Precision in liver surgery. Semin Liver Dis 33:189–203CrossRef Dong J, Yang S, Zeng J, Cai S, Ji W, Duan W, Zhang A, Ren W, Xu Y, Tan J, Bu X, Zhang N, Wang X, Wang X, Meng X, Jiang K, Gu W, Huang Z (2013) Precision in liver surgery. Semin Liver Dis 33:189–203CrossRef
6.
go back to reference Takasaki K (1998) Glissonean pedicle transection method for hepatic resection: a new concept of liver segmentation. J Hepato-biliary-pancreat Surg 5:286–291CrossRef Takasaki K (1998) Glissonean pedicle transection method for hepatic resection: a new concept of liver segmentation. J Hepato-biliary-pancreat Surg 5:286–291CrossRef
7.
go back to reference Shindoh J, Mise Y, Satou S, Sugawara Y, Kokudo N (2010) The intersegmental plane of the liver is not always flat–tricks for anatomical liver resection. Ann Surg 251:917–922CrossRef Shindoh J, Mise Y, Satou S, Sugawara Y, Kokudo N (2010) The intersegmental plane of the liver is not always flat–tricks for anatomical liver resection. Ann Surg 251:917–922CrossRef
8.
go back to reference Inoue Y, Arita J, Sakamoto T, Ono Y, Takahashi M, Takahashi Y, Kokudo N, Saiura A (2015) Anatomical liver resections guided by 3-dimensional parenchymal staining using fusion indocyanine green fluorescence imaging. Ann Surg 262:105–111CrossRef Inoue Y, Arita J, Sakamoto T, Ono Y, Takahashi M, Takahashi Y, Kokudo N, Saiura A (2015) Anatomical liver resections guided by 3-dimensional parenchymal staining using fusion indocyanine green fluorescence imaging. Ann Surg 262:105–111CrossRef
9.
go back to reference Fan ST (2010) Liver functional reserve estimation: state of the art and relevance for local treatments: the Eastern perspective. J Hepato-biliary-pancreat Sci 17:380–384CrossRef Fan ST (2010) Liver functional reserve estimation: state of the art and relevance for local treatments: the Eastern perspective. J Hepato-biliary-pancreat Sci 17:380–384CrossRef
10.
go back to reference Aoki T, Yasuda D, Shimizu Y, Odaira M, Niiya T, Kusano T, Mitamura K, Hayashi K, Murai N, Koizumi T, Kato H, Enami Y, Miwa M, Kusano M (2008) Image-guided liver mapping using fluorescence navigation system with indocyanine green for anatomical hepatic resection. World J Surg 32:1763–1767CrossRef Aoki T, Yasuda D, Shimizu Y, Odaira M, Niiya T, Kusano T, Mitamura K, Hayashi K, Murai N, Koizumi T, Kato H, Enami Y, Miwa M, Kusano M (2008) Image-guided liver mapping using fluorescence navigation system with indocyanine green for anatomical hepatic resection. World J Surg 32:1763–1767CrossRef
11.
go back to reference Gotoh K, Yamada T, Ishikawa O, Takahashi H, Eguchi H, Yano M, Ohigashi H, Tomita Y, Miyamoto Y, Imaoka S (2009) A novel image-guided surgery of hepatocellular carcinoma by indocyanine green fluorescence imaging navigation. J Surg Oncol 100:75–79CrossRef Gotoh K, Yamada T, Ishikawa O, Takahashi H, Eguchi H, Yano M, Ohigashi H, Tomita Y, Miyamoto Y, Imaoka S (2009) A novel image-guided surgery of hepatocellular carcinoma by indocyanine green fluorescence imaging navigation. J Surg Oncol 100:75–79CrossRef
12.
go back to reference Ishizawa T, Fukushima N, Shibahara J, Masuda K, Tamura S, Aoki T, Hasegawa K, Beck Y, Fukayama M, Kokudo N (2009) Real-time identification of liver cancers by using indocyanine green fluorescent imaging. Cancer 115:2491–2504CrossRef Ishizawa T, Fukushima N, Shibahara J, Masuda K, Tamura S, Aoki T, Hasegawa K, Beck Y, Fukayama M, Kokudo N (2009) Real-time identification of liver cancers by using indocyanine green fluorescent imaging. Cancer 115:2491–2504CrossRef
13.
go back to reference Hong SK, Lee KW, Kim HS, Yoon KC, Ahn SW, Choi JY, Kim H, Yi NJ, Suh KS (2017) Optimal bile duct division using real-time indocyanine green near-infrared fluorescence cholangiography during laparoscopic donor hepatectomy. Liver Transplant 23:847–852CrossRef Hong SK, Lee KW, Kim HS, Yoon KC, Ahn SW, Choi JY, Kim H, Yi NJ, Suh KS (2017) Optimal bile duct division using real-time indocyanine green near-infrared fluorescence cholangiography during laparoscopic donor hepatectomy. Liver Transplant 23:847–852CrossRef
14.
go back to reference Meng X, Wang H, Xu Y, Chen M, Duan W, Lu S (2018) Indocyanine green fluorescence image-guided total laparoscopic living donor right hepatectomy: the first case report from Mainland China. Int J Sur Case Rep 53:406–409CrossRef Meng X, Wang H, Xu Y, Chen M, Duan W, Lu S (2018) Indocyanine green fluorescence image-guided total laparoscopic living donor right hepatectomy: the first case report from Mainland China. Int J Sur Case Rep 53:406–409CrossRef
15.
go back to reference Ishizawa T, Zuker NB, Kokudo N, Gayet B (2012) Positive and negative staining of hepatic segments by use of fluorescent imaging techniques during laparoscopic hepatectomy. Arch Surg 147:393–394CrossRef Ishizawa T, Zuker NB, Kokudo N, Gayet B (2012) Positive and negative staining of hepatic segments by use of fluorescent imaging techniques during laparoscopic hepatectomy. Arch Surg 147:393–394CrossRef
16.
go back to reference Cho A, Okazumi S, Miyazawa Y, Makino H, Miura F, Ohira G, Yoshinaga Y, Tohma T, Kudo H, Matsubara K, Ryu M, Ochiai T (2004) Limited resection based on reclassification of segment 8 of the liver. Hepatogastroenterology 51:575–576PubMed Cho A, Okazumi S, Miyazawa Y, Makino H, Miura F, Ohira G, Yoshinaga Y, Tohma T, Kudo H, Matsubara K, Ryu M, Ochiai T (2004) Limited resection based on reclassification of segment 8 of the liver. Hepatogastroenterology 51:575–576PubMed
17.
go back to reference Winkler K, Tygstrup N (1960) Determination of hepatic blood flow in man by cardio green. Scand J Clin Lab Invest 12:353–356CrossRef Winkler K, Tygstrup N (1960) Determination of hepatic blood flow in man by cardio green. Scand J Clin Lab Invest 12:353–356CrossRef
18.
go back to reference Cherrick GR, Stein SW, Leevy CM, Davidson CS (1960) Indocyanine green: observations on its physical properties, plasma decay, and hepatic extraction. J Clin Investig 39:592–600CrossRef Cherrick GR, Stein SW, Leevy CM, Davidson CS (1960) Indocyanine green: observations on its physical properties, plasma decay, and hepatic extraction. J Clin Investig 39:592–600CrossRef
19.
go back to reference Ishizawa T, Bandai Y, Kokudo N (2009) Fluorescent cholangiography using indocyanine green for laparoscopic cholecystectomy: an initial experience. Arch Surg 144:381–382CrossRef Ishizawa T, Bandai Y, Kokudo N (2009) Fluorescent cholangiography using indocyanine green for laparoscopic cholecystectomy: an initial experience. Arch Surg 144:381–382CrossRef
20.
go back to reference Dip F, LoMenzo E, Sarotto L, Phillips E, Todeschini H, Nahmod M, Alle L, Schneider S, Kaja L, Boni L, Ferraina P, Carus T, Kokudo N, Ishizawa T, Walsh M, Simpfendorfer C, Mayank R, White K, Rosenthal RJ (2019) Randomized trial of near-infrared incisionless fluorescent cholangiography. Ann Surg 270:992–999CrossRef Dip F, LoMenzo E, Sarotto L, Phillips E, Todeschini H, Nahmod M, Alle L, Schneider S, Kaja L, Boni L, Ferraina P, Carus T, Kokudo N, Ishizawa T, Walsh M, Simpfendorfer C, Mayank R, White K, Rosenthal RJ (2019) Randomized trial of near-infrared incisionless fluorescent cholangiography. Ann Surg 270:992–999CrossRef
21.
go back to reference Sherwinter DA (2012) Identification of anomolous biliary anatomy using near-infrared cholangiography. J Gastrointest Surg 16:1814–1815CrossRef Sherwinter DA (2012) Identification of anomolous biliary anatomy using near-infrared cholangiography. J Gastrointest Surg 16:1814–1815CrossRef
22.
go back to reference Kaibori M, Ishizaki M, Matsui K, Kwon AH (2011) Intraoperative indocyanine green fluorescent imaging for prevention of bile leakage after hepatic resection. Surgery 150:91–98CrossRef Kaibori M, Ishizaki M, Matsui K, Kwon AH (2011) Intraoperative indocyanine green fluorescent imaging for prevention of bile leakage after hepatic resection. Surgery 150:91–98CrossRef
23.
go back to reference Abo T, Nanashima A, Tobinaga S, Hidaka S, Taura N, Takagi K, Arai J, Miyaaki H, Shibata H, Nagayasu T (2015) 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 41:257–264CrossRef Abo T, Nanashima A, Tobinaga S, Hidaka S, Taura N, Takagi K, Arai J, Miyaaki H, Shibata H, Nagayasu T (2015) 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 41:257–264CrossRef
24.
go back to reference Kawaguchi Y, Ishizawa T, Masuda K, Sato S, Kaneko J, Aoki T, Beck Y, Sugawara Y, Hasegawa K, Kokudo N (2011) Hepatobiliary surgery guided by a novel fluorescent imaging technique for visualizing hepatic arteries, bile ducts, and liver cancers on color images. J Am Coll Surg 212:e33–39CrossRef Kawaguchi Y, Ishizawa T, Masuda K, Sato S, Kaneko J, Aoki T, Beck Y, Sugawara Y, Hasegawa K, Kokudo N (2011) Hepatobiliary surgery guided by a novel fluorescent imaging technique for visualizing hepatic arteries, bile ducts, and liver cancers on color images. J Am Coll Surg 212:e33–39CrossRef
25.
go back to reference Kawaguchi Y, Nagai M, Nomura Y, Kokudo N, Tanaka N (2015) Usefulness of indocyanine green-fluorescence imaging during laparoscopic hepatectomy to visualize subcapsular hard-to-identify hepatic malignancy. J Surg Oncol 112:514–516CrossRef Kawaguchi Y, Nagai M, Nomura Y, Kokudo N, Tanaka N (2015) Usefulness of indocyanine green-fluorescence imaging during laparoscopic hepatectomy to visualize subcapsular hard-to-identify hepatic malignancy. J Surg Oncol 112:514–516CrossRef
26.
go back to reference Peloso A, Franchi E, Canepa MC, Barbieri L, Briani L, Ferrario J, Bianco C, Quaretti P, Brugnatelli S, Dionigi P, Maestri M (2013) Combined use of intraoperative ultrasound and indocyanine green fluorescence imaging to detect liver metastases from colorectal cancer. HPB 15:928–934CrossRef Peloso A, Franchi E, Canepa MC, Barbieri L, Briani L, Ferrario J, Bianco C, Quaretti P, Brugnatelli S, Dionigi P, Maestri M (2013) Combined use of intraoperative ultrasound and indocyanine green fluorescence imaging to detect liver metastases from colorectal cancer. HPB 15:928–934CrossRef
27.
go back to reference Miyata A, Ishizawa T, Tani K, Shimizu A, Kaneko J, Aoki T, Sakamoto Y, Sugawara Y, Hasegawa K, Kokudo N (2015) Reappraisal of a dye-staining technique for anatomic hepatectomy by the concomitant use of indocyanine green fluorescence imaging. J Am Coll Surg 221:e27–36CrossRef Miyata A, Ishizawa T, Tani K, Shimizu A, Kaneko J, Aoki T, Sakamoto Y, Sugawara Y, Hasegawa K, Kokudo N (2015) Reappraisal of a dye-staining technique for anatomic hepatectomy by the concomitant use of indocyanine green fluorescence imaging. J Am Coll Surg 221:e27–36CrossRef
28.
go back to reference Ishizawa T, Gumbs AA, Kokudo N, Gayet B (2012) Laparoscopic segmentectomy of the liver: from segment I to VIII. Ann Surg 256:959–964CrossRef Ishizawa T, Gumbs AA, Kokudo N, Gayet B (2012) Laparoscopic segmentectomy of the liver: from segment I to VIII. Ann Surg 256:959–964CrossRef
29.
go back to reference Buell JF, Cherqui D, Geller DA, O'Rourke N, Iannitti D, Dagher I, Koffron AJ, Thomas M, Gayet B, Han HS, Wakabayashi G, Belli G, Kaneko H, Ker CG, Scatton O, Laurent A, Abdalla EK, Chaudhury P, Dutson E, Gamblin C, D'Angelica M, Nagorney D, Testa G, Labow D, Manas D, Poon RT, Nelson H, Martin R, Clary B, Pinson WC, Martinie J, Vauthey JN, Goldstein R, Roayaie S, Barlet D, Espat J, Abecassis M, Rees M, Fong Y, McMasters KM, Broelsch C, Busuttil R, Belghiti J, Strasberg S, Chari RS, World Consensus Conference on Laparoscopic S (2009) The international position on laparoscopic liver surgery: the Louisville Statement. Ann Surg 250:825–830CrossRef Buell JF, Cherqui D, Geller DA, O'Rourke N, Iannitti D, Dagher I, Koffron AJ, Thomas M, Gayet B, Han HS, Wakabayashi G, Belli G, Kaneko H, Ker CG, Scatton O, Laurent A, Abdalla EK, Chaudhury P, Dutson E, Gamblin C, D'Angelica M, Nagorney D, Testa G, Labow D, Manas D, Poon RT, Nelson H, Martin R, Clary B, Pinson WC, Martinie J, Vauthey JN, Goldstein R, Roayaie S, Barlet D, Espat J, Abecassis M, Rees M, Fong Y, McMasters KM, Broelsch C, Busuttil R, Belghiti J, Strasberg S, Chari RS, World Consensus Conference on Laparoscopic S (2009) The international position on laparoscopic liver surgery: the Louisville Statement. Ann Surg 250:825–830CrossRef
30.
go back to reference Xiang L, Xiao L, Li J, Chen J, Fan Y, Zheng S (2015) Safety and feasibility of laparoscopic hepatectomy for hepatocellular carcinoma in the posterosuperior liver segments. World J Surg 39:1202–1209CrossRef Xiang L, Xiao L, Li J, Chen J, Fan Y, Zheng S (2015) Safety and feasibility of laparoscopic hepatectomy for hepatocellular carcinoma in the posterosuperior liver segments. World J Surg 39:1202–1209CrossRef
31.
go back to reference Terasawa M, Ishizawa T, Mise Y, Inoue Y, Ito H, Takahashi Y, Saiura A (2017) Applications of fusion-fluorescence imaging using indocyanine green in laparoscopic hepatectomy. Surg Endosc 31:5111–5118CrossRef Terasawa M, Ishizawa T, Mise Y, Inoue Y, Ito H, Takahashi Y, Saiura A (2017) Applications of fusion-fluorescence imaging using indocyanine green in laparoscopic hepatectomy. Surg Endosc 31:5111–5118CrossRef
32.
go back to reference Aoki T, Koizumi T, Mansour DA, Fujimori A, Kusano T, Matsuda K, Tashiro Y, Watanabe M, Otsuka K, Murakami M (2019) Ultrasound-guided preoperative positive percutaneous indocyanine green fluorescence staining for laparoscopic anatomical liver resection. J Am Coll Surg 230(3):e7–e12CrossRef Aoki T, Koizumi T, Mansour DA, Fujimori A, Kusano T, Matsuda K, Tashiro Y, Watanabe M, Otsuka K, Murakami M (2019) Ultrasound-guided preoperative positive percutaneous indocyanine green fluorescence staining for laparoscopic anatomical liver resection. J Am Coll Surg 230(3):e7–e12CrossRef
33.
go back to reference Gunji H, Cho A, Tohma T, Okazumi S, Makino H, Shuto K, Mochizuki R, Matsubara K, Hayano K, Mori C, Murakami G, Ochiai T (2006) The blood supply of the hilar bile duct and its relationship to the communicating arcade located between the right and left hepatic arteries. Am J Surg 192:276–280CrossRef Gunji H, Cho A, Tohma T, Okazumi S, Makino H, Shuto K, Mochizuki R, Matsubara K, Hayano K, Mori C, Murakami G, Ochiai T (2006) The blood supply of the hilar bile duct and its relationship to the communicating arcade located between the right and left hepatic arteries. Am J Surg 192:276–280CrossRef
Metadata
Title
Laparoscopic anatomical liver resection guided by real-time indocyanine green fluorescence imaging: experience and lessons learned from the initial series in a single center
Authors
Yinzhe Xu
Mingyi Chen
Xiangfei Meng
Peng Lu
Xun Wang
Wenwen Zhang
Ying Luo
Weidong Duan
Shichun Lu
Hongguang Wang
Publication date
01-10-2020
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 10/2020
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-020-07691-5

Other articles of this Issue 10/2020

Surgical Endoscopy 10/2020 Go to the issue