Real-Time Depiction of Intrahepatic Biliary Anatomy During Recipient Surgery with Contrast-Enhanced Ultrasonography in Living-Donor Liver Transplantation

Introduction

In living-donor liver transplantation (LDLT), biliary complications are considered an Achilles’ heel. Hence, various attempts have been made to reduce their incidence, resulting in reports of multiple innovations in surgical techniques. Accurate evaluation of the biliary anatomy is extremely important to prevent biliary complications, with appropriate surgical planning. In addition to preoperative evaluation using magnetic resonance cholangiopancreatography (MRCP) or drip infusion cholangiography-computed tomography (DIC-CT), various intraoperative evaluation methods have been developed to assess both the donor safety and the bile duct anatomy of grafts. We previously reported the use of a real-time intraoperative cholangiography (IOC) in donor surgery to achieve a desirable transection point for both the donor and recipient, with the identification of the tissue containing the bile duct to be dissected using radiopaque lead threads [1]. Regarding the difficulties encountered when performing IOC and probing through the divided bile duct opening or cystic duct opening during laparoscopic hepatectomy, Hong et al successfully delineated the biliary anatomy by using indocyanine green (ICG) [2]. Urade et al reported the efficacy of contrast-enhanced intraoperative ultrasonic cholangiography (IOUSC) for real-time biliary navigation in living donor liver surgery [3]; this was demonstrated through results such as the ability to detect second-order caudate branches that could not be visualized with preoperative DIC-CT [3].

Here, we report, for the first time, a case in which IOUSC demonstrated effectiveness in detecting the bile duct (not detected by IOC during donor surgery) not only in the donor hepatectomy but also in the recipient’s abdominal cavity after reperfusion of the graft.

Case Report

All procedures in this report were conducted in accordance with the Declarations of Helsinki. The report was approved by the Ethics Committee of Nagasaki University Hospital (decision number 20012022). Written informed consent was obtained from the patient for the publication of details of the medical case and any accompanying images. The authors are accountable for all aspects of this work and ensure that questions related to the accuracy or integrity of any part of the work have been appropriately investigated and resolved.

A 39-year-old male patient was admitted to our hospital with a diagnosis of decompensated alcoholic liver cirrhosis. Liver cirrhosis was first diagnosed in 2014, and the patient received conservative therapy. At the beginning of 2023, the patient presented with severe ascites and jaundice. The preoperative laboratory results revealed a total bilirubin level of 11.1 mg/dL and a model for end-stage liver disease score of 26. Severe coagulopathy was also observed, due to thrombocytopenia (thrombocytes 65 000/mm3, PT-INR 1.78). Abdominal CT showed cirrhotic liver and splenomegaly. The donor was his younger brother. Preoperative computer tomography volumetry showed that the volume of the extended left lobe graft was 443 mL, which was equivalent to 34.0% of the recipient’s standard liver volume, as calculated using Urata’s formula [4]. According to our institute’s criteria, we decided to transplant the extended left lobe graft. Preoperative MRCP revealed no evidence of the biliary anatomy; this could have been problematic when donating the left lobe graft (Figure 1). During donor operation, intraoperative contrast medium was injected through a cannula inserted through the cystic duct, and no confluence of the bile duct from the right lobe was observed in the left hepatic duct; therefore, it was determined that the left hepatic duct could be transected with sufficient length for anastomosis while securing smooth passage of the donor bile duct (Figure 2). After encircling the left hepatic artery and left branch of the portal vein, the bile duct, including the hilar plate, was encircled using radiopaque lead threads [3]. IOC showed that the left hepatic duct was sufficiently long for division, guaranteeing donor safety. After the parenchymal transection was completed, the bile duct was transected, the bile duct on the donor side was closed with continuous sutures, and an IOC was performed again to confirm that there was no stenosis in the donor’s bile duct.

Back-table observation of the bile duct revealed 3 orifices; of these, the central orifice was very small, and the corresponding bile duct was not evident on cholangiography during donor surgery. Reperfusion after implantation was smooth, and arterial anastomosis was completed without any problems. Cold ischemic time was 77 min, and warm ischemic time was 5 min. To reconstruct the biliary tract, we determined whether all 3 orifices in the bile duct on the graft side required reconstruction. The bile duct in the center of the 3 orifices was too thin to confirm its path using the probe; therefore, we cannulated it using the outer sheath of a 22 G needle for infusion (Figure 3). Before injection of perfluorobutane microbubbles, a vial of Sonazoid (Daiichi-Sankyo Pharmaceutical Tokyo, Japan) was reconstituted with 2 mL of sterile water. This stock solution was diluted 1000-fold with saline for intrabiliary injection [5]. In the next step, the solution was administered into the bile ducts. Since the microbubbles begin to break down shortly after entering the bile ducts, real-time imaging with the probe was performed immediately following the injection. If the initial injection did not produce satisfactory results, additional injections of the contrast agent were administered, to achieve optimal visualization. Using real-time IOUSC with the Aplio XG system (Toshiba Medical Systems, Tokyo, Japan), the bile duct of segment 4 (B4) was clearly visualized (Figure 4, Video 1). Based on this finding, we determined that all 3 openings required reconstruction and reconstructed them using a previously reported telescope reconstruction method [6]. The total duration of the recipient’s surgery was 831 min. Blood loss was 12 000 mL. Recovery of the liver function was uneventful. The patient is currently followed-up with a biliary internal stent at the outpatient clinic, and normal liver function is reported.

Discussion

In LDLT, despite the advancements in surgical techniques and diagnostic methods, biliary complications can develop in 15% to 25% of recipients [7,8]. Precise preoperative and intraoperative evaluations of biliary anatomy variations in living donors play a crucial role in preventing biliary complications. Multiple bile ducts are a potential risk factor for developing biliary complications, occurring in 19% to 54% of cases [9–11]. The presence of multiple bile duct orifices in the left lobe graft is relatively uncommon. In our case, 3 separate bile ducts were unexpectedly identified after the division, despite the fact that the position of the division was determined after confirming the findings of intraoperative cholangiogram. The main diagnostic modality was MRCP, which is considered safe, repeatable, reproducible, and highly accurate. However, the sensitivity of MRCP decreases in the presence of variance in biliary anatomy. The sensitivity of MRCP for normal and variant anatomy is 100% and 67%, respectively [12]. The DIC-CT modality is also used as an alternative for MRCP. However, it has several pitfalls related to radiation and contrast media usage. Persson et al performed a review and reported the presence of an adverse effect with the injection of contrast: 1.5–2.2% adverse effects of minor degree, 1.1–1.8% adverse effects of intermediate degree, and 0–0.1% adverse effects of severe degree [13].

New techniques, such as intraoperative evaluation of biliary anatomy using ICG, have been reported with the development of laparoscopic surgery [2]. Intraoperative imaging of the biliary system using ICG needs devices for near-infrared fluorescence imaging. The drawbacks of ICG imaging of the biliary system include possible weak depiction of the biliary system with thick surrounding connective tissue. Additionally, the intrahepatic biliary system cannot be visualized using ICG imaging.

Real-time IOC remains the main investigation method for evaluating bile duct morphology intraoperatively. IOC has several benefits, including a clear depiction of potential biliary tree anomalies, a reduced risk of biliary tract injuries, and the detection of stones in the common bile duct. However, the main disadvantages include radiation exposure and the potential for contrast leakage into the surgical field, which can result in poor image quality, particularly when evaluating small ducts [14–16].

Contrast-enhanced ultrasound, compared with IOC, offers unique benefits, such as affordability, real-time imaging of the biliary tree, repeatability, absence of radiation exposure, and ease of use. Xu et al first reported the successful use of IOUSC to delineate the anatomy of the biliary tract in a liver donor [17]. Zheng et al performed IOUSC on 12 donors and reported an accurate depiction of anatomical patterns, including 3 biliary variations; no adverse effects were observed in the donors [18].

To the best of our knowledge, this is the first report describing intraoperative IOUSC of the liver graft during recipient surgery after reperfusion in LDLT. In partial liver transplantation, such as LDLT or split liver transplantation, unexpected bile duct anatomy can be encountered, which may not be evident during preoperative evaluation. In the present case, IOUSC successfully identified small bile ducts that were not evident on pre-operative MRCP or IOC. IOUSC does not require large imaging equipment; only an ultrasound system is required. Therefore, it can be set up quickly and repeated as needed. Surgeons can operate the ultrasound probe by themselves to evaluate the bile ducts in the region of interest in real time.

Conclusions

We verified that IOUSC is useful as a tool to confirm the anatomy of the bile duct, especially when it cannot be visualized with other evaluation methods. Hence, it is a method that transplant surgeons should be familiar with.