New technical development for pure laparoscopic donor hepatectomy: indocyanine green cholangiography and three-dimensional laparoscopy
Review Article

New technical development for pure laparoscopic donor hepatectomy: indocyanine green cholangiography and three-dimensional laparoscopy

Akihiko Soyama, Susumu Eguchi

Department of Surgery, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki, Japan

Contributions: (I) Conception and design: All authors; (II) Administrative support: None; (III) Provision of study materials or patients: None; (IV) Collection and assembly of data: All authors; (V) Data analysis and interpretation: All authors; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

Correspondence to: Susumu Eguchi. Department of Surgery, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki 852-8501, Japan. Email: sueguchi@nagasaki-u.ac.jp.

Abstract: In addition to the accumulation of experience, improvements in laparoscopic imaging systems, devices, and introduction of new techniques have been reported to overcome limitations in pure laparoscopic donor surgery. Major limitations of conventional laparoscopy are the lack of depth perception and tactile feedback. As a possible solution for the limitations, the successful application of three-dimensional (3D) visualization has been reported; 3D laparoscopy can provide depth perception and also excellent hand-eye coordination. Optimal intraoperative visualization of the biliary duct anatomy and an appropriate cutting point were considered major issues during pure laparoscopic donor hepatectomy. Recently, real-time intraoperative imaging using indocyanine green (ICG) has been reported as a reliable method that may replace conventional intraoperative cholangiography in pure laparoscopic donor hepatectomy. In this review, we describe the current status of ICG cholangiography and 3D laparoscopy in laparoscopic donor hepatectomy.

Keywords: Living donor liver transplantation; laparoscopic liver resection; indocyanine green (ICG); three-dimensional laparoscopy (3D laparoscopy); intraoperative cholangiogram


Received: 21 December 2019; Accepted: 07 February 2020; Published: 15 April 2020.

doi: 10.21037/ls.2020.02.05


Introduction

Laparoscopic donor hepatectomy is becoming increasingly common. However, pure laparoscopic donor hemihepatectomy is currently performed only at centers that are highly experienced in both donor surgery and laparoscopic hepatectomy. In addition to the accumulation of experience, improvements in laparoscopic imaging systems, devices, and introduction of new techniques have been reported to overcome the limitations associated with pure laparoscopic donor surgery.

One of the major limitations of laparoscopy are the lack of depth perception and tactile feedback (1). Recent advances in laparoscopic imaging systems have increased the performance of pure laparoscopic donor hepatectomy. For example, three-dimensional (3D) visualization can provide depth perception as well as excellent hand-eye coordination (2). The successful application of 3D laparoscopy for increasing the application of laparoscopic donor hepatectomy has recently been reported (3).

Although an intraoperative cholangiogram with contrast injection via the cystic duct has been established as a standard technique in the conventional open procedure and even hybrid donor hepatectomy (4-6), that procedure can be cumbersome in pure laparoscopic surgery. As a result, optimal intraoperative visualization of the biliary duct anatomy and establishment of an appropriate cutting point have been considered major problematic issues associated with laparoscopic donor hepatectomy (7). The introduction of intraoperative imaging using indocyanine green (ICG) has been reported in laparoscopic hepatobiliary surgery (8,9). In pure laparoscopic donor surgery as well, ICG cholangiography has recently been reported as a reliable method (10).

We herein report the current status of ICG cholangiography and 3D laparoscopy in laparoscopic donor hepatectomy.


ICG near-infrared fluorescence cholangiography (NIFC)

The establishment of an appropriate point of the bile duct division of the graft liver is the most important point for preventing biliary complications of both donors and recipients. Since donor safety should be the top priority in living donor liver transplantation, the bile duct must be divided with great caution.

In living donor hepatectomy, intraoperative cholangiography has been considered the standard procedure in most centers, with bile duct division performed under the guidance of a C-arm fluoroscope with a radiopaque marker (11,12). However, a standard cholangiogram is not always easy to perform in pure laparoscopic donor hepatectomy. Even at highly experienced centers, in their initial experience, the application of pure laparoscopic donor hepatectomy has been limited to donors with a simple biliary anatomy (2,13,14).

Troisi et al. mentioned the potential utility of ICG NIFC in laparoscopic donor hepatectomy in their report on their initial experience with laparoscopic donor hepatectomy (7). ICG has been used clinically to estimate the cardiac output and liver function since its approval by the U.S. Food and Drug Administration (FDA) in 1954 (9). Protein-bound ICG was found to emit fluorescence, peaking at about 840 nm under illumination with near-infrared light (750−810 nm) (15). Because little light at 840 nm is absorbed by hemoglobin or water, the fluorescence signals emitted by protein-bound ICG can be visualized.

In the field of hepatobiliary surgery, in the late 2000s, some Japanese groups reported methods of intraoperatively visualizing the hepatobiliary structures using ICG-fluorescence imaging (8,16,17). For an intraoperative cholangiogram with ICG-fluorescence imaging, intrabiliary injection and intravenous injection have been reported as the route of ICG. Ishizawa et al. reported fluorescent cholangiography with ICG excreted into bile following preoperative intravenous injection (8). Cholangiography with the injection of 2.5 mg of ICG diluted into 1 mL solution was first reported by Ishizawa et al.; according to that report, ICG fluorescence in the extrahepatic bile ducts continues up to 6 h after the injection (8).

Mizuno et al. reported the application of intraoperative ICG cholangiography in conventional open donor left hepatectomy in 2010 as the first report of this concept (18). In that case report, ICG (0.025 mg/mL) was injected through a transcystic tube. Following this report, several case reports and case series have been published (19,20) (Table 1).

Table 1
Table 1 Summary of findings of previous studies about ICG cholangiography in donor hepatectomy
Full table

With respect to techniques for the administration of ICG, the intravenous injection of ICG compared to the conventional direct injection of contrast into the bile duct may be associated with saving time. Also, the intravenous injection may ignore the difficulty and avoid bile duct injury caused by the catheterization into the bile ducts for injecting contrasts, especially in laparoscopic surgery.

Hong et al. first reported the use of ICG NIFC with intravenous injection during various types of laparoscopic donor hepatectomy (10) (Table 1). In their prospective study of ten cases (right hemihepatectomy in eight donors, extended right hemihepatectomy in 1 donor, left lateral sectionectomy with in vivo reduction in 1), the history of iodine allergy was preoperatively checked in all donors. ICG (0.05 mg/kg) was injected intravenously 30–60 minutes before exposure of the hilar plate with considering the timing of bile excretion (21). After exposing the anterior surface of the hilar plate, the distal bile duct was temporarily clamped to congest the bile and eventually visualize the bile duct. In all donors, the biliary system around the hilar plate, including any aberrant hepatic ducts, was visualized (10). Concerning the safety of ICG cholangiography, Hong et al. mentioned that the risk of an adverse reaction to ICG injection is negligible because the amount of ICG injected at a dosage of 0.05 mg/kg is approximately 0.003% at doses exceeding 0.5 mg/kg (10). The amount of ICG injected for the liver function estimation is 0.5 mg/kg (22,23). Furthermore, ICG cholangiography does not require consideration of the risk of radiation exposure for donors or operating room personnel.

Recently, a single-blind, randomized, 2-arm trial comparing the efficacy of ICG NIFC versus white light (WL) alone during laparoscopic cholecystectomy was reported (24). In that study, the detection rates for seven biliary structures before and after surgical dissection were evaluated. The detection rates before dissection were significantly higher in the NIFC group for all seven biliary structures than in WL group. In addition, an increased body mass index was reported to be associated with a reduced detection rates in both groups, especially before dissection.

For wide application of ICG cholangiography into the field of donor hepatectomy, we should pay attention to the limitations associated with ICG cholangiography performed by presently available devices. For example, ICG fluorescence can penetrate approximately 5–10 mm into the tissue, and it cannot easily visualize bile ducts surrounded with thick connective tissue (21). The importance of preserving the surrounding tissue of the bile duct to maintain optimal vascularization and prevent biliary complication has been well recognized (4). Therefore, we should not compromise the vascularization of the bile duct for better visualization when using ICG cholangiography.

Suh et al. retrospectively evaluated the outcomes of donors who underwent pure laparoscopic donor right hepatectomy with ICG cholangiography (n=45) compared with those who underwent conventional donor right hepatectomy (n=42) (25). While both groups had a comparable length of postoperative hospital stay and rates of complications and re-hospitalization, the proportion of grafts with multiple bile duct orifices was significantly higher in the pure laparoscopic donor hepatectomy with ICG cholangiography group than in the conventional donor hepatectomy group (53.3% vs. 26.2%; P=0.010) (25) (Table 1). Suh et al. hypothesized that this might be because surgeons may still lack confidence in determining the point of bile duct division and move to the right side more naturally, despite preoperative magnetic resonance cholangiopancreatography (MRCP) images and ICG cholangiography. Whereas, in the conventional open procedure, Takatsuki et al. reported the efficacy of encircling the bile duct using a radiopaque marker filament for determining the precise point of bile duct division under real-time C-arm cholangiography to reduce the incidence of multiple bile ducts (4). In addition to confirming the quality of visualization achieved by ICG cholangiography, the optimal procedure for determining the appropriate cutting line of the bile duct should be discussed in future studies.

Recently, some centers have reported successful pure laparoscopic right donor hepatectomy in donors with variant biliary anatomy (26,27) (Table 1). Although these reports support the wider spread of laparoscopic donor surgery, liver transplant surgeons should be reminded that these successful cases have been reported from highly experienced transplant teams with expertise in performing laparoscopic donor surgery.


3D laparoscopy

Compared to the conventional two-dimensional (2D) video-assisted system, the 3D video-assisted system was reported to provide depth perception and precise measurement of the anatomical space (28). In addition, it provides excellent hand-eye coordination (1). The clinical benefit of 3D displays during laparoscopic/thoracoscopic surgery has been reported in various types of surgery, including gastrectomy, esophagectomy, rectal surgery, etc. (28-31). For example, a significantly shortened operative time was reported in gastrectomy, esophagectomy, radical resection for rectal cancer, and thoracoscopic lobectomy. In addition, in the field of liver surgery, Velayutham et al. reported a reduced operating time by 3D visualization compared to 2D visualization in laparoscopic liver resection (1).

Suh et al. noted that the introduction of a 3D laparoscopy for liver surgery in 2015 resulted in the more frequent use of the laparoscopic-assisted procedure for donor hepatectomy; thereafter, the first pure laparoscopic donor extended right hepatectomy using 3D laparoscopy was performed (2). Recently, Lee et al. reported their experiences with pure laparoscopic donor right hepatectomy with the largest number of donors (n=115) from a single center (3). At present, further experiences with 3D laparoscopy and ICG cholangiography are being accumulated without any selection criteria, such as cases with anatomical variance for pure laparoscopic donor hepatectomy (25). Findings of previous studies are summarized in Table 2.

Table 2
Table 2 Summary of findings of previous studies about 3D laparoscopy in hepatectomy
Full table

The successful application of 3D laparoscopy accompanied with ICG cholangiography in laparoscopic donor hepatectomy has been reported in cases demanding complex procedures. Hong et al. reported a successful case of left lateral sectionectomy by a pure 3D laparoscopic procedure with in situ reduction to obtain a monosegment graft in a case of pediatric living donor liver transplantation (32). Park et al. recently reported successful pure laparoscopic donor right hepatectomy with 3D laparoscopy and ICG cholangiography in donors with type II and III portal vein variations with a comparison between pure laparoscopic donor right hepatectomy and the conventional open procedure (33).

Concerning scientific evidence, as shown in other types of surgery, although 3D laparoscopy may offer clinically quantitative benefits, such as a shorter operative time, comparative studies between laparoscopic donor hepatectomy with 3D laparoscopy and 2D laparoscopy with a sufficient number of cases have not yet been published.


Conclusions

It is apparent that advances in surgical device and techniques such as ICG cholangiography and 3D laparoscopy have offered benefits for the application of pure laparoscopic surgery to living donor hepatectomy. Furthermore, in highly skilled teams or centers, these techniques have been successfully used to expand the indication of pure laparoscopic donor hepatectomy. Thus far, however, the benefits of these techniques have been reported mostly from expert teams. The accumulation of more experiences will bring new information on not only the benefits but also the obstacles that should be considered in order to expand the application of these techniques for safe laparoscopic donor hepatectomy.


Acknowledgments

None.


Footnote

Conflicts of Interest: The authors have no conflicts of interest to declare.

Ethical Statement: The authors are 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.


References

  1. Velayutham V, Fuks D, Nomi T, et al. 3D visualization reduces operating time when compared to high-definition 2D in laparoscopic liver resection: a case-matched study. Surg Endosc 2016;30:147-53. [Crossref] [PubMed]
  2. Suh KS, Hong SK, Yi NJ, et al. Pure 3-dimensional laparoscopic extended right hepatectomy in a living donor. Liver Transpl 2016;22:1431-6. [Crossref] [PubMed]
  3. Lee KW, Hong SK, Suh KS, et al. One Hundred Fifteen Cases of Pure Laparoscopic Living Donor Right Hepatectomy at a Single Center. Transplantation 2018;102:1878-84. [Crossref] [PubMed]
  4. Takatsuki M, Eguchi S, Yamanouchi K, et al. Technical refinements of bile duct division in living donor liver surgery. J Hepatobiliary Pancreat Sci 2011;18:170-5. [Crossref] [PubMed]
  5. Soyama A, Takatsuki M, Hidaka M, et al. Standardized less invasive living donor hemihepatectomy using the hybrid method through a short upper midline incision. Transplant Proc 2012;44:353-5. [Crossref] [PubMed]
  6. Eguchi S, Soyama A, Hara T, et al. Standardized hybrid living donor hemihepatectomy in adult-to-adult living donor liver transplantation. Liver Transpl 2018;24:363-8. [Crossref] [PubMed]
  7. Troisi RI, Wojcicki M, Tomassini F, et al. Pure laparoscopic full-left living donor hepatectomy for calculated small-for-size LDLT in adults: proof of concept. Am J Transplant 2013;13:2472-8. [Crossref] [PubMed]
  8. Ishizawa T, Bandai Y, Kokudo N. Fluorescent cholangiography using indocyanine green for laparoscopic cholecystectomy: an initial experience. Arch Surg 2009;144:381-2. [Crossref] [PubMed]
  9. Ishizawa T, Saiura A, Kokudo N. Clinical application of indocyanine green-fluorescence imaging during hepatectomy. Hepatobiliary Surg Nutr 2016;5:322-8. [Crossref] [PubMed]
  10. Hong SK, Lee KW, Kim HS, et al. Optimal bile duct division using real-time indocyanine green near-infrared fluorescence cholangiography during laparoscopic donor hepatectomy. Liver Transpl 2017;23:847-52. [Crossref] [PubMed]
  11. Takatsuki M, Eguchi S, Tokai H, et al. A secured technique for bile duct division during living donor right hepatectomy. Liver Transpl 2006;12:1435-6. [Crossref] [PubMed]
  12. Lee SG, Park KM, Hwang S, et al. Adult-to-adult living donor liver transplantation at the Asan Medical Center, Korea. Asian J Surg 2002;25:277-84. [Crossref] [PubMed]
  13. Soubrane O, Perdigao Cotta F, Scatton O. Pure laparoscopic right hepatectomy in a living donor. Am J Transplant 2013;13:2467-71. [Crossref] [PubMed]
  14. Han HS, Cho JY, Yoon YS, et al. Total laparoscopic living donor right hepatectomy. Surg Endosc 2015;29:184. [Crossref] [PubMed]
  15. Landsman ML, Kwant G, Mook GA, et al. Light-absorbing properties, stability, and spectral stabilization of indocyanine green. J Appl Physiol 1976;40:575-83. [Crossref] [PubMed]
  16. Kubota K, Kita J, Shimoda M, et al. Intraoperative assessment of reconstructed vessels in living-donor liver transplantation, using a novel fluorescence imaging technique. J Hepatobiliary Pancreat Surg 2006;13:100-4. [Crossref] [PubMed]
  17. Mitsuhashi N, Kimura F, Shimizu H, et al. Usefulness of intraoperative fluorescence imaging to evaluate local anatomy in hepatobiliary surgery. J Hepatobiliary Pancreat Surg 2008;15:508-14. [Crossref] [PubMed]
  18. Mizuno S, Isaji S. Indocyanine green (ICG) fluorescence imaging-guided cholangiography for donor hepatectomy in living donor liver transplantation. Am J Transplant 2010;10:2725-6. [Crossref] [PubMed]
  19. Tomassini F, Scarinci A, Elsheik Y, et al. Indocyanine green near-infrared fluorescence in pure laparoscopic living donor hepatectomy: a reliable road map for intra-hepatic ducts? Acta Chir Belg 2015;115:2-7. [Crossref]
  20. Mizuno S, Inoue H, Tanemura A, et al. Biliary complications in 108 consecutive recipients with duct-to-duct biliary reconstruction in living-donor liver transplantation. Transplant Proc 2014;46:850-5. [Crossref] [PubMed]
  21. Ishizawa T, Bandai Y, Ijichi M, et al. Fluorescent cholangiography illuminating the biliary tree during laparoscopic cholecystectomy. Br J Surg 2010;97:1369-77. [Crossref] [PubMed]
  22. Seyama Y, Kokudo N. Assessment of liver function for safe hepatic resection. Hepatol Res 2009;39:107-16. [Crossref] [PubMed]
  23. Kamohara Y, Takatsuki M, Hidaka M, et al. 99mTc-Galactosyl sialyl albumin (GSA) scintigram adjusts hepatic resection range in ICG based estimation. Hepatogastroenterology 2011;58:2058-61. [PubMed]
  24. Dip F, LoMenzo E, Sarotto L, et al. Randomized Trial of Near-infrared Incisionless Fluorescent Cholangiography. Ann Surg 2019;270:992-9. [Crossref] [PubMed]
  25. Suh KS, Hong SK, Lee KW, et al. Pure laparoscopic living donor hepatectomy: Focus on 55 donors undergoing right hepatectomy. Am J Transplant 2018;18:434-43. [Crossref] [PubMed]
  26. Hong SK, Suh KS, Kim HS, et al. Pure 3D laparoscopic living donor right hemihepatectomy in a donor with separate right posterior and right anterior hepatic ducts and portal veins. Surg Endosc 2017;31:4834-5. [Crossref] [PubMed]
  27. Han YS, Ha H, Kwon HJ, et al. Pure laparoscopic donor right hepatectomy in a living donor with type 3a biliary variation: A case report. Medicine (Baltimore) 2017;96:e8076. [Crossref] [PubMed]
  28. Yamashita K, Mine S, Toihata T, et al. The usefulness of three-dimensional video-assisted thoracoscopic esophagectomy in esophageal cancer patients. Esophagus 2019;16:272-7. [Crossref] [PubMed]
  29. Dong S, Yang XN, Zhong WZ, et al. Comparison of three-dimensional and two-dimensional visualization in video-assisted thoracoscopic lobectomy. Thorac Cancer 2016;7:530-4. [Crossref] [PubMed]
  30. Zeng Q, Lei F, Gao Z, et al. Case-matched study of short-term effects of 3D vs 2D laparoscopic radical resection of rectal cancer. World J Surg Oncol 2017;15:178. [Crossref] [PubMed]
  31. Itatani Y, Obama K, Nishigori T, et al. Three-dimensional Stereoscopic Visualization Shortens Operative Time in Laparoscopic Gastrectomy for Gastric Cancer. Sci Rep 2019;9:4108. [Crossref] [PubMed]
  32. Hong SK, Suh KS, Kim HS, et al. Pediatric Living Donor Liver Transplantation Using a Monosegment Procured by Pure 3D Laparoscopic Left Lateral Sectionectomy and In situ Reduction. J Gastrointest Surg 2018;22:1135-6. [Crossref] [PubMed]
  33. Park K, Shehta A, Lee JM, et al. Pure 3D laparoscopy versus open right hemihepatectomy in a donor with type II and III portal vein variations. Ann Hepatobiliary Pancreat Surg 2019;23:313-8. [Crossref] [PubMed]
doi: 10.21037/ls.2020.02.05
Cite this article as: Soyama A, Eguchi S. New technical development for pure laparoscopic donor hepatectomy: indocyanine green cholangiography and three-dimensional laparoscopy. Laparosc Surg 2020;4:17.