Minimally invasive liver resection in Japan: is the robot necessary?

Minimally


INTRODUCTION
During the past three decades, the indications for laparoscopic hepatectomy (LH) have been dramatically extended based on technical, oncological, and regional factors.In Japan, LH for limited resections and left lateral sectionectomy was first reimbursed by the national health insurance system in 2010; this was  (1993-2019).Since the first insurance reimbursement in 2010, the numbers of laparoscopic hepatectomies have progressively increased, and this increase has been further boosted by the extension of insurance support to a wider range of hepatectomy procedures in 2016.This figure was created based on the 15th Nationwide Survey of Endoscopic Surgery.
followed by extension of its indications to all LH procedures except hepatectomy requiring biliary reconstruction in 2016 [1] and reimbursement of robot-assisted distal pancreatectomy and pancreaticoduodenectomy in 2020.As of 2021, however, robot-assisted hepatectomy (RAH) has not been reimbursed.We herein introduce the current status of minimally invasive hepatectomy in Japan and discuss the potential advantages of RAH over conventional hepatectomy procedures in an effort to promote future proliferation of robot-assisted hepatobiliary surgery.

CURRENT DISSEMINATION STATUS OF RAH IN JAPAN
Since the first insurance reimbursement in 2010, the number of LH cases in Japan has progressively increased, and this increase was further boosted by the extension of insurance support to a wider range of hepatectomy procedures in 2016 [Figure 1].Based on the National Clinical Database, 13% of hepatectomy procedures (more than one segment excluding the lateral segment) were performed laparoscopically in 2019 [2] .In contrast, RAH has rarely been performed in Japan; according to the 15th Nationwide Survey of Endoscopic Surgery, RAH accounted for only 0.5% of all minimally invasive hepatectomy procedures performed in 459 medical centers belonging to the Japan Society for Endoscopic Surgery [Table 1, The 15th Nationwide Survey of Endoscopic Surgery in Japan (The Japanese Society for Endoscopic Surgery)].In Japan, where all citizens receive medical care under the universal health insurance system, insurance reimbursement is critical for both patients and surgeons to ensure access to newly developed therapeutic modalities such as robot-assisted surgery.
Another feature to consider in the dissemination of RAH is the safety of hepatectomy in Japan.Even after the nationwide establishment of LH, the overall mortality rates after hepatectomy remained quite low (0.7%-1.4% at 30 days and 1.3%-2.6%at 90 days from 2011 to 2019), with favorable morbidity rates (3.4%-4.3%Clavien-Dindo grade IIIa-V complications) [2] .Step-by-step establishment of LH under the board certification systems provided by the Japan Society for Endoscopic Surgery [3] , the Japanese Society of Hepato-Biliary-Pancreatic Surgery [4,5] , and the nationwide online registry system [6] have contributed to the safe and consistent dissemination of LH in Japan.

POSSIBLE ADVANTAGES OF PROMOTING FUTURE DISSEMINATION OF RAH
Recent systemic reviews and meta-analyses have already shown that RAH offers acceptable operative outcomes at least comparable to those of LH, except for possible extension of the operation time [7][8][9] .More recently, a meta-analysis focusing on major (three or more Couinaud's segments) hepatectomies suggested advantages of RAH over LH in decreasing a conversion rate and perioperative blood loss [10] .Considering the higher cost of RAH [7,9] , however, we need more evidence supporting the clear advantages of using robotic surgical systems in specific aspects of hepatectomy procedures, as suggested below, which enables selection of the patient appropriate to RAH.

Resection of superior/posterior hepatic regions
One of the major limitations of LH lies in the fact that conventional procedures allow only tangential movements of laparoscopic forceps.This makes deep wedge resections difficult to perform, especially for lesions located in the right superior/posterior regions of the liver.Using a "lateral approach" with intercostal trocars [11,12] is a possible solution for LH, but this technique may not be applicable to patients with a history of pulmonary disease or surgery.Vertical transection of the hepatic parenchyma enabled by multiarticulated movements of robotic devices may facilitate resection of hepatic tumors located in difficult regions, as suggested by a previous comparative study [13] .Melstrom et al. [14] also suggested efficacy of RAH in decreasing postoperative hospital stay (even on the day of surgery), especially in cases of superior/posterior hepatic regions where the incision for open surgery would dominate the course of recovery.

Hilar dissection and biliary reconstruction
Flexible movements of robotic surgical forceps also enable minute dissections of hepatic vessels running in the hilar plates and hepatoduodenal ligament; this may be associated with favorable operative outcomes with a lower probability of open conversion in major hepatectomies and complicated hepatectomy procedures requiring hilar dissection as compared with LH [7,10,15] .Suturing with the use of multi-articulated needle holders is an obvious advantage of robot-assisted surgery over conventional laparoscopic techniques.
In the context of hepatobiliary surgery, this feature would work most effectively for biliary anastomosis as demonstrated in surgery for choledochal cysts [16] , although no LH procedures requiring biliary reconstruction have been reimbursed by the Japanese health insurance system to date.

Hepatic segmentation by fluorescence imaging for anatomic resection
Because the latest robotic surgical systems are equipped with near-infrared imaging technology (da Vinci Firefly; Intuitive Surgical, Sunnyvale, CA, USA), intraoperative fluorescence imaging using indocyanine green (ICG) can be easily applied to RAH as well as LH and open hepatectomy for real-time visualization of the biliary anatomy (fluorescence cholangiography), liver cancers, and boundaries of hepatic segments [17] .Among these procedures, hepatic segmentation can be achieved by direct injection of ICG into the target portal branch (positive staining technique) [18,19] or by systemic injection of ICG following closure of the portal pedicle feeding tumor-bearing hepatic segments (negative staining technique) [18,20] .If a robotic surgical system could be used to perform a positive staining technique, it would facilitate easier puncture of the target portal branch under ultrasound guidance compared with laparoscopic needle manipulation [21] .The use of robotic surgical devices also enables multidirectional dissection of the hepatic hilum to reach the corresponding Glissonian sheaths to be divided [22] , which may extend the indications for the negative staining technique to anatomic resection of deeply located hepatic segments.Although near-infrared imaging has been installed in the latest model of laparoscopic imaging systems as well as robotic surgical systems, use of this technology with multi-articulated forceps and three-dimensional color imaging may further extend applications of fluorescence imaging during hepatobiliary surgery.

Integrated surgical navigation, autonomous actions, and surgical decision-making by artificial intelligence
In addition to intraoperative information obtained by techniques such as fluorescence imaging and ultrasonography, preoperative simulation can be placed in the surgeon's console of the robotic surgical system and displayed in real time with three-dimensional images of operative fields.In this respect, RAH has a potential advantage over LH in terms of the ability of surgeons to understand special relationships between anatomical structures and tumors by integrating preoperative and intraoperative imaging information.Applications of augmented reality [23] and artificial intelligence [24] may further promote the development of surgical navigation systems.In addition, application of artificial intelligence in robotic surgery may enable autonomous control of surgical installments like a laparoscope and staplers and provide precision information for accurate surgical decision-making [25] .

POSSIBLE DISADVANTAGES OF APPLYING ROBOT-ASSISTED SURGERY TO HEPATECTOMY
As mentioned previously, the major disadvantage of RAH over LH is the higher cost associated with the initial installation and use of each instalment.Especially in Japan, the amount of future insurance claim for RAH may be the same as that for LH as in the case of pancreatectomy, which can press management of the medical institutions.Limited lineup of aspiration and dissection devices (no angular ultrasonic dissectors) designed for hepatic parenchymal transection is another drawback of RAH, leading to longer operation time than LH as demonstrated in previous studies [7][8][9] .We expect that the next-generation robotic surgical systems are devised with the opinions from liver surgeons to adjust to the specific conditions of hepatectomy.

CONCLUSIONS
With the accumulation of evidence indicating the specific advantages of RAH over LH, robotic surgical systems will become more commonly used for hepatobiliary surgery in Japan as well as in other countries.After reimbursement by the health insurance system, we aim to apply RAH with prioritization of surgical safety using a nationwide reporting system and board certification systems for the performance of LH and robot-assisted pancreatic resections.

Figure 1 .
Figure 1.Trends of annual numbers of laparoscopic hepatectomies in Japan (1993-2019).Since the first insurance reimbursement in 2010, the numbers of laparoscopic hepatectomies have progressively increased, and this increase has been further boosted by the extension of insurance support to a wider range of hepatectomy procedures in 2016.This figure was created based on the 15th Nationwide Survey of Endoscopic Surgery.

Table 1 . Numbers of different minimally invasive hepatectomy procedures in Japan in 2019
**Based on the 15th Nationwide Survey of Endoscopic Surgery in Japan (the Japan Society for Endoscopic Surgery).†Hand-assisted or hybrid procedures.LH: Laparoscopic hepatectomy; RAH: robot-assisted hepatectomy.