Surgical technique for fully robotic two-stage hepatectomy using indocyanine green fluorescence imaging for bilobar colorectal liver metastases

Introduction

Background and rationale

The liver is the most common site of metastasis in colorectal cancer with up to 50% of patients presenting with colorectal liver metastases (CLRM) (1). Local treatment is the most effective curative treatment option for patients with CRLM (2). However, only 20% of patients with CRLM are considered candidates for surgery at the time of diagnosis (3). Patients with extensive or bilobar CRLM are mainly unresectable due to insufficient future liver remnant (FLR) which is a major risk factor for post hepatectomy liver failure (4,5). Due to developments of novel surgical techniques such as two-stage hepatectomy, extensive and/or bilobar CRLM are increasingly eligible for local treatment (6,7). In recent years, the technique for two-stage hepatectomy has been further improved by the implementation of minimally invasive approaches and image-guided surgery including indocyanine green (ICG) fluorescence imaging (8-11).

Since two-stage hepatectomy is in itself a technically demanding procedure, attempts to perform a robot-assisted two-stage hepatectomy including a robot-assisted first- and second-stage procedure are hardly described in the current literature.

Objective

The objective of this video-report is to describe a fully robot-assisted two-stage hepatectomy using ICG fluorescence imaging as curative intent therapy in a patient with initially unresectable bilobar CRLM. We present this article in accordance with the SUPER reporting checklist (available at https://jovs.amegroups.com/article/view/10.21037/jovs-24-24/rc).

Ethics statement

All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patient for publication of this study and the video. A copy of the written consent is available for review by the editorial office of this journal.

Case description

A 44-year-old woman was diagnosed with a cT3N2M1 rectal carcinoma with six synchronous CRLM lesions in segments 2 (25 mm), 2/3 (43 mm), 5 (42 mm), 7 (18 mm), 7 (45 mm), 8 (37 mm). Her medical history stated a laparoscopic cholecystectomy. Preoperative liver function tests were as follows: aspartate aminotransferase (AST) 14 U/L, alanine aminotransferase (ALT) 13 U/L, alkaline phosphatase (ALP) 91 U/L, gamma-glutamyl transferase (GGT) 23 U/L, albumin 47 g/L, and total bilirubin 7 µmol/L. During the first multidisciplinary team (MDT) meeting, the CRLM were considered initially unresectable owing to insufficient FLR. The MDT agreed on the start of induction systemic chemotherapy capecitabin/oxaliplatin-bevacizumab (CAPOX-B). After 3 cycles of CAPOX-B, the metastases were reassessed. The metastases were now deemed resectable owing to a significant reduction in tumor size in response to chemotherapy. A two-stage hepatectomy was indicated due to a too small FLR in case of a one-stage resection. A fourth cycle of CAPOX (without bevacizumab) was given before the two-stage hepatectomy according to Dutch guidelines.

Preoperative preparations and requirements

Surgeon training and experience

The console surgeon in both procedures had extensive experience in hepatobiliary surgery, having performed more than 100 robotic procedures prior to these operations.

Patient selection

Contraindications for a totally minimally invasive two-stage hepatectomy at our centre include insufficient FLR, or large tumours (>10 cm), without margin towards the hepatocaval or biliary confluence.

Assessment of FLR and portal vein embolization

Preoperative assessment of FLR was performed by computed tomography (CT)-volumetry and a technetium-99m (^99mTc) mebrofenin hepatobiliary scintigraphy (HBS). Prior to first stage surgery, scans showed a FLR (segment 1–4) of 40% and 2.1%/min/m². Four days after the first stage surgery PVE was performed by the intervention radiologist under local anesthesia. Under the guidance of ultrasound, percutaneous puncture was performed and angiography showed the left and right branches. The catheter was guided into the right portal vein branch, and lipiodol 1:8 mixture of glue was used for the embolization. The small side branch was embolized with coils. The angiography showed complete embolization of the right portal vein. Twenty-nine days after PVE, new imaging was performed to assess whether second stage hepatectomy was feasible. The second CT-volumetry and HBS showed a FLR of 47% and 2.9%/min/m².

Step-by-step description

A video of the procedure is available as a Supplementary (Video S1).

Surgical technique—first stage: robot-assisted wedge resections of segment 2 and 3

One day before the surgery, ICG 10 mg is injected intravenously into the patient.

The operation was performed by a team consisting of two surgeons (one console and one bedside surgeon).

Positioning the patient

• The patient is positioned on a vacuum mattress in a supine French position with the right arm alongside the body on an arm support and the left arm extended. The operating table is tilted in 10–20° in anti-Trendelenburg and 5–10° to the right.
• All safety procedures (hood, sterile glove and sterile scrub) are ascertained, and a sterile exposition is created. The pneumoperitoneum is created with CO₂ to 12 mmHg using a Veress needle.
• The da Vinci Xi robotic camera (Intuitive Surgical, Inc., Sunnyvale, CA, USA) is inserted through a visiport 12 mm trocar in the right pararectal space, just below the umbilicus. The remaining trocars are placed as shown in Figure 1.
  

  Figure 1 Port placement.
• The robot is placed on the right side next to the patient and the arms are docked onto the four robotic trocars.
• The first surgeon takes place at the robot console and the tableside surgeon between the patient’s legs.

Identification and exposure

• A diagnostic laparoscopy is undertaken. The metastases in segments 2 and 3 were visible by rim fluorescence.
• An intraoperative ultrasound (Hitachi Arietta Echo Endoscopic Drop-In Probe, Fujifilm Europe, Steinhausen) is performed to confirm that no additional lesions are present. This diagnostic procedure confirmed there were no contraindications for surgery.
• The falciform and round ligaments are divided using the Vessel Sealer Extend and cautery hook.
• The left liver lobe is mobilized by dividing the coronary ligaments using the cautery hook.
• The resection margins are determined in segment 2 and 3 using ICG-fluorescence and intra-operative ultrasound.

Resection

• The parenchyma is transected to perform a wedge resection of segment 2 using both the robotic scissors and Vessel Sealer Extend guided by fluorescence imaging using the Firefly imaging system.
• A Pringle maneuver is prepared by passing a “Huang loop” (12) around the hepatoduodenal ligament.
• The parenchyma is transected to perform a wedge resection of the metastasis in segment 3 using robotic scissors and Vessel Sealer Extend guided by fluorescence imaging using the Firefly imaging system.

Closure

Both surgical specimens are placed in an extraction bag (Endo Catch II Pouch 10 mm) and removed through a Pfannenstiel incision.

Operative time was 183 minutes.

Surgical procedure—second stage: robotic right hemihepatectomy

One day before the surgery ICG 10 mg is injected intravenously into the patient.

The operation was performed by a team consisting of two surgeons (one console and one bedside surgeon).

Positioning of the patient

• The patient is positioned on a vacuum mattress in a supine French position with the right arm alongside the body on an arm support and the left arm extended. The operating table is tilted 10–20° in anti-Trendelenburg and 5–10° to the left.
• The pneumoperitoneum is created with CO₂ to 12 mmHg via open introduction.
• The daVinci Xi robotic camera (Intuitive Surgical, Inc., Sunnyvale, California) is inserted through a visiport 12 mm trocar in the right pararectal space, just below the umbilicus. The remaining trocars are placed as shown in Figure 1.

Identification and exposure

• A diagnostic laparoscopy is performed. Diagnostic laparoscopy revealed a white-colored lesion on the right side of the diaphragm. The frozen section showed no malignancy.
• After adhesiolysis of previous surgeries on the left lobe, the right liver lobe is mobilized by dividing the right coronary and triangular ligaments towards the origin of the right hepatic vein draining into the vena cava using a cautery hook and SynchroSeal. Short hepatic veins are divided between Hem-o-lock clips (not shown in the video).

Resection

• The right hepatic artery is identified in the hepatoduodenal ligament. The right hepatic artery is dissected and isolated using robotic bipolar forceps.
• After clamping the right hepatic artery using a bulldog clamp, the flow is confirmed in the left hepatic artery by intraoperative ultrasound.
• The right hepatic artery is clipped with Hem-o-lock clips (Weck, Telefex, Morrisville, North Carolina) and divided using robotic scissors.
• The right portal vein is identified. The right portal vein is dissected and isolated using the robotic bipolar forceps and the robotic cautery hook. In this particular case, it was not possible to isolate the right portal vein due to its broad base.
• An alternative route is created through parenchymal transection towards the right hepatic duct. The ischemia (Cantlie’s line) on the liver surface is visualized and the planned transection line is demarcated using a monopolar cautery hook. Parenchymal transection is performed using the monopolar cautery, ultrasound aspirator device (by the table side surgeon) and the SynchroSeal.
• The Firefly imaging system is used to acquire ICG-fluorescence imaging and identify the right bile duct. The right bile duct is isolated. The right bile duct is transected with an endostapler (Ethicon Endo Surgery Industries, Cincinnati, OH, USA).
• Isolation of the right portal vein is now safe. The inflow of the portal vein is controlled by placement of a bulldog clamp.
• After control of the inflow, clips are placed on the right portal vein.
• The right portal vein is transected between the clips with the robotic vascular stapler (Ethicon).
• The transection of the parenchyma is continued using the monopolar cautery, SynchroSeal and Vessel Sealer Extend for control of intrahepatic vascular structures, until the right hepatic vein is reached.
• The right hepatic vein is identified and transected using a 35 mm vascular stapler, Endostapler (Ethicon Endo Surgery Industries, Cincinnati, OH, USA).
• The falciform ligament is reattached.

Closure

The specimen is placed in an extraction bag (Endo Catch II Pouch 15 mm) and removed through a Pfannenstiel incision.

Operative time was 428 minutes.

Postoperative considerations and tasks

During the first-stage hepatectomy, no intra-operative incidents occurred. The estimated total blood loss was 10 mL. PVE was performed three days postoperatively, during the same hospital admission. The patient was discharged after 7 days. Gastroparesis grade A was registered as a postoperative complication. New imaging was performed twenty-nine days after PVE to allow for sufficient time for liver regeneration before reassessing patient eligibility for second stage resection. Hereafter, once the patient was deemed resectable by the MDT, the patient was scheduled for second stage hepatectomy which was performed 48 days after the discharge of the first stage. The second stage was performed without any intraoperative incidents. A total blood loss of 200 cc was registered. The patient was discharged after 5 days without any postoperative complications. Histopathological reports of all lesions in both procedures revealed R0 resection margins.

Tips and pearls

Minimally invasive surgery accelerates recovery following liver resection. This makes it particularly advantageous in the context of two-stage hepatectomy, where rapid recovery between the first and second surgeries is crucial for patients.

Minimally invasive surgery is associated with a steep learning curve. The second-stage procedure described above involves a complex operation—major liver resection in a patient with prior liver surgery and PVE. Surgeons should only attempt complex hepatobiliary procedures, especially minimally invasive ones, after surmounting the learning curve. The authors strongly advocate for a proficiency-based progression approach, where experience is gained with simpler procedures before advancing to more complex resections. Patient selection is key in matching the procedure difficulty with the surgeon’s capabilities, promoting patient safety. Moreover, structured training programs are important for the development of skills in a stepwise manner.

ICG fluorescence imaging can help guide surgeons intraoperatively, providing real-time information on the localization of tumors and liver anatomy. This is especially helpful in minimally invasive surgery where tactile feedback is limited. The authors therefore encourage its use.

The Huang Loop technique facilitates the Pringle maneuver by enabling intracorporeal control of the Pringle by the console surgeon.

The intraoperative ultrasound is an indispensable tool in liver surgery, helping to guarantee patient safety through resection margin assessment, identification of anatomy, and assessment of vascular flow after clamping.

Discussion

This video-report demonstrates the feasibility of a complete robotic two-stage procedure. A two-stage hepatectomy gives the opportunity for a curative resection of extensive CRLM. The success of a two-stage hepatectomy depends partially on the recovery of the patients after the first stage (13). Minimally invasive surgery, such as robot-assisted surgery demonstrated advantages including lower blood loss, decreased morbidity and shortened length of hospitalization (14).

Robotic liver surgery might overcome the limitations of conventional laparoscopic liver surgery. Robotic technology provides the surgeon with better three-dimensional view, instruments have an increased dexterity compared to the conventional rigid laparoscopic instruments, tremor filtration, ease of suturing, better motion scaling and improved ergonomics for the surgeon (8,15-17). Another major benefit of the robotic system is the ability to build an interactive visual interface, using customized software in which surgeons may be assisted by preoperative and/or intra-operative imaging such as intraoperative ultrasound and ICG fluorescence imaging during parenchymal transection (18).

ICG fluorescence imaging is emerging as a promising and useful tool during robotic liver surgery. Intra-operative ultrasound is routinely performed during robotic liver surgery and provides information on number and size of lesions (19). However, it may be challenging to give precise information of tumor margins as well as biliary tract anatomy. ICG-fluorescence imaging can help in visualizing liver lesions and the trajectory of intra- and extrahepatic biliary ducts, therefore helping to perform an uncomplicated, tumor-margin negative liver resection (20,21).

To our knowledge, this is the first video-report of a fully robotic two-stage hepatectomy, with PVE. Limited reports are written of fully robotic two-stage procedures including an associating liver partition with portal vein ligation for staged hepatectomy (ALPPS) instead of PVE. In 2016, Vicente et al. (Spain) described a two-stage procedure including a robotic ALPPS procedure in a patient with CRLM (22). The first phase consisted of a tumor resection in segment 1 combined with an ALPPS procedure. Thirteen days later, the second phase, a robotic hemihepatectomy, was performed. No postoperative complications were mentioned, and postoperative pathology showed margins free from disease. In 2021, Hu et al. (China) described a two stage hepatectomy with an ALPPS procedure in the first phase in a patient with a hepatocellular carcinoma (HCC) (23). In the first phase the ALPPS procedure was performed robotically, and 12 days later, the second phase, a robotic hemihepatectomy. Postoperative recovery was without complications. After the second phase, the patient had a hospital stay of 6 days. The resection margins were without disease. The main difference between these case reports and our case is the application of the ALPPS procedure instead of a PVE, which might explain the longer waiting period between the two stages in our report. Although PVE is associated with slower hypertrophy rates compared to ALPPS, it was opted for because of its minimal invasiveness and favorable safety profile (24,25). Reports have demonstrated high mortality rates for ALPPS (26). Moreover, if liver hypertrophy proves insufficient for a second stage resection with PVE, a salvage ALPPS procedure can still be considered (27).

The use of laparoscopy for a two-stage hepatectomy has been described several times in literature. In 2012, Machado et al. (Brazil) described a fully laparoscopic two-stage hepatectomy for bilateral liver metastases (28). In the initial phase, a resection of segment 3 was performed, together with a ligature of the right portal vein. After 4 weeks, the second phase, a right hemihepatectomy, was performed. The patient recovered without any complications from both surgeries. The hospital stay was 2 and 7 days after the first and second phase respectively. The same group described in a retrospective analysis that the outcomes of the laparoscopic two-stage procedures was not inferior to the open approach, the analysis focused on patients who underwent an ALPPS procedure (29). The median hospital stay was 11 days for this group, with no mortality or major complications. The superiority of robotic liver surgery over laparoscopic liver surgery is still a matter of debate in literature (30-32). No direct comparisons of robotic and laparoscopic procedures have been made in literature for two-stage hepatic resections.

Conclusions

This video-report describes the technical details of a fully robot-assisted two-stage hepatectomy using ICG fluorescence imaging. This procedure seems to be safe and feasible for curative-intent treatment of extensive bilobar CRLM.

Acknowledgments

We thank our patient for giving informed consent for using the operation video for science.

Funding: None.

Footnote

Reporting Checklist: The authors have completed the SUPER reporting checklist. Available at https://jovs.amegroups.com/article/view/10.21037/jovs-24-24/rc

Peer Review File: Available at https://jovs.amegroups.com/article/view/10.21037/jovs-24-24/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jovs.amegroups.com/article/view/10.21037/jovs-24-24/coif). R.J.S. is a proctor for Intuitive Surgical and receives fees from Intuitive Surgical for proctorship in robotic liver surgery. These fees are not for personal use, but transferred to the AMC Medical Research fund. The other 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. All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patient for publication of this study, the accompanying image, and the video. A copy of the written consent is available for review by the editorial office of this journal.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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