Laparoscopic Extended Left Lateral Sectionectomy for Hepatocellular Carcinoma in a Patient with Right-Sided Ligamentum Teres: A Case Report and Literature Review

Right-sided ligamentum teres (RSLT) is a rare anatomic variant in which the fetal umbilical vein connects to the right portal vein. Patients with RSLT frequently have hepatic vasculature and bile duct anomalies, which increase the risk of complications with hepatectomy. Most patients with RSLT undergo open hepatectomy. Herein, we describe a patient with RSLT and hepatocellular carcinoma who underwent laparoscopic hepatectomy. The patient was a 69-year-old man with hepatocellular carcinoma located in the left liver based on computed tomography (CT) and magnetic resonance imaging. Imaging also demonstrated RSLT. Three-dimensional CT analysis revealed independent right lateral type anomalies of the portal vein and bile duct. A laparoscopic extended left lateral sectionectomy was performed after careful surgical planning. Ultrasonography was used frequently during surgery to avoid damaging the right hepatic vasculature. The left lateral and partial left median sections were removed as planned. The patient’s postoperative recovery was uneventful. Avoiding injury to the right hepatic vasculature is essential when performing left lobectomy, including left lateral sectionectomy, in patients with RSLT. Laparoscopic hepatectomy can be performed safely in patients with RSLT, provided that careful surgical planning is conducted using preoperative three-dimensional CT analysis and intraoperative ultrasonography.


Introduction
Right-sided ligamentum teres (RSLT) is a rare anatomical variant in which the fetal umbilical vein is connected to the right paramedian trunk of the portal vein instead of the left portal vein [1]. The reported incidence rates of RSLT range between 0.2% and 1.2% [1,2]. The ligamentum teres is the remnant of the functioning fetal umbilical vein. RSLT is thought to result from obstruction of the left umbilical vein during development, which causes persistence of the right umbilical vein; normally, the right umbilical vein obliterates and the left one persists [3]. In the past, many cases of RSLT were reported as a left-sided gallbladder because the ligamentum teres and gallbladder often assumed the opposite position to normal [1,2]. However, a left-sided gallbladder associated with RSLT is actually an abnormality of the position of the ligamentum teres and should be distinguished from a "true" left-sided gallbladder, which is an abnormality of the position of the gallbladder itself [2,4]. Liver resection in patients with RSLT should be performed cautiously because this variant is associated with a high frequency of portal vein, hepatic vein, and bile duct abnormalities [5]. For this reason, most liver tumor patients with RSLT undergo open hepatectomy [6]. Herein, we report a patient with RSLT who successfully underwent laparoscopic extended lateral sectionectomy for the resection of hepatocellular carcinoma.

Case Report
A 69-year-old man was referred for an evaluation of a liver tumor detected on abdominal ultrasonography performed for a nonalcoholic steatohepatitis follow-up. Blood testing showed elevations in concentrations of aspartate transaminase (56 U/L), alanine transaminase (51 U/L), and protein induced by vitamin K absence-II (224 mAU/mL). Other tumor markers and hepatitis virus markers were negative. The indocyanine green retention rate at 15 min was 15.2% and the Child-Pugh score was 5 points (class A), suggesting good hepatic function. Computed tomography (CT) showed a 2.4 × 2.0 cm hypodense mass in the left lobe of the liver (segment 2/3/4b) which exhibited early arterial enhancement and washout ( Figure 1). Hepatocellular carcinoma was highly suspected. In addition, the ligamentum teres was connected to the right anterior branch of the portal vein, and the gallbladder was located to its left, indicating RSLT ( Figure 2). On magnetic resonance imaging, the mass had low signal intensity on T1-weighted images and high signal intensity on T2-weighted and diffusion-weighted images; contrasted imaging using gadolinium ethoxybenzyl diethylenetriamine penta-acetic acid revealed a perfusion defect in the mass in the liver phase ( Figure 3). Three-dimensional CT (Synapse Vincent ® ; Fujifilm Medical, Tokyo, Japan) demonstrated the right posterior, right anterior, and left branches of the portal vein. The left branch branched into a lateral superior branch (P2) and a lateral inferior branch (P3) after two medial branches (P4a,b) separated. A right inferior hepatic vein and a hepatic vein of an anterior superior segment (V8) were present ( Figure 4). Magnetic resonance cholangiopancreatography revealed that the bile duct system was trifurcated into the right posterior, right anterior branch, and left branches ( Figure 5). After the pertinent anatomy was clarified and the preoperative evaluation was completed, we elected to perform laparoscopic extended lateral sectionectomy.
Diagnostics 2023, 13, x FOR PEER REVIEW 2 of 8 underwent laparoscopic extended lateral sectionectomy for the resection of hepatocellular carcinoma.

Case Report
A 69-year-old man was referred for an evaluation of a liver tumor detected on abdominal ultrasonography performed for a nonalcoholic steatohepatitis follow-up. Blood testing showed elevations in concentrations of aspartate transaminase (56 U/L), alanine transaminase (51 U/L), and protein induced by vitamin K absence-II (224 mAU/mL). Other tumor markers and hepatitis virus markers were negative. The indocyanine green retention rate at 15 min was 15.2% and the Child-Pugh score was 5 points (class A), suggesting good hepatic function. Computed tomography (CT) showed a 2.4 × 2.0 cm hypodense mass in the left lobe of the liver (segment 2/3/4b) which exhibited early arterial enhancement and washout ( Figure 1). Hepatocellular carcinoma was highly suspected. In addition, the ligamentum teres was connected to the right anterior branch of the portal vein, and the gallbladder was located to its left, indicating RSLT ( Figure 2). On magnetic resonance imaging, the mass had low signal intensity on T1-weighted images and high signal intensity on T2-weighted and diffusion-weighted images; contrasted imaging using gadolinium ethoxybenzyl diethylenetriamine penta-acetic acid revealed a perfusion defect in the mass in the liver phase ( Figure 3). Three-dimensional CT (Synapse Vincent®; Fujifilm Medical, Tokyo, Japan) demonstrated the right posterior, right anterior, and left branches of the portal vein. The left branch branched into a lateral superior branch (P2) and a lateral inferior branch (P3) after two medial branches (P4a,b) separated. A right inferior hepatic vein and a hepatic vein of an anterior superior segment (V8) were present ( Figure 4). Magnetic resonance cholangiopancreatography revealed that the bile duct system was trifurcated into the right posterior, right anterior branch, and left branches ( Figure 5). After the pertinent anatomy was clarified and the preoperative evaluation was completed, we elected to perform laparoscopic extended lateral sectionectomy.         superior branch (P2) and a lateral inferior branch (P3) after two medial branc The PRA was connected to the right umbilical portion (RUP). A right inferio and a hepatic vein branch of an anterior superior segment (V8) were presen vein (MHV) and left hepatic vein (LHV) were normal. The planned resection l yellow dotted line. Surgery was performed with the patient in the supine positio definition/three-dimensional monitor. Five laparoscopy ports were camera port at the umbilicus, 12 mm ports below the xiphoid proce arch, and 5 mm ports outside the right and left rib arches. After confir the location of the gallbladder (Figure 6A), the falciform ligament ligament were dissected. The tumor was then located using u determine the extent of resection while avoiding damage to the righ the head side was marked at the boundary between the segment 4b an section ( Figure 6B), and the caudal side was marked at the line wh remained ( Figure 6C). The liver resection was performed using a cav surgical aspirator (CUSA® Excel; Integra, Princeton, NJ, USA) and (Harmonic® HD 1000i shears; Ethicon, Raritan, NJ, USA). The med superior, lateral inferior, and lateral superior branches of Glisson a were individually double-clipped using a polymer locking ligation s Teleflex, Wayne, PA, USA) and resected. Thin vein branches were clip clip applier (Endo Clip ® ; Medtronic, Dublin, Ireland) and cut. Fin section, including the partial left median section, was resected ( operation time was 7 h and 35 min. The blood loss volume was 10 Surgery was performed with the patient in the supine position using a 2K highdefinition/three-dimensional monitor. Five laparoscopy ports were placed: a 12 mm camera port at the umbilicus, 12 mm ports below the xiphoid process and the right rib arch, and 5 mm ports outside the right and left rib arches. After confirming the RSLT and the location of the gallbladder ( Figure 6A), the falciform ligament and left triangular ligament were dissected. The tumor was then located using ultrasonography. To determine the extent of resection while avoiding damage to the right-sided vasculature, the head side was marked at the boundary between the segment 4b and the right anterior section (Figure 6B), and the caudal side was marked at the line where the segment 4a remained ( Figure 6C). The liver resection was performed using a cavitational ultrasonic surgical aspirator (CUSA ® Excel; Integra, Princeton, NJ, USA) and ultrasonic scalpel (Harmonic ® HD 1000i shears; Ethicon, Raritan, NJ, USA). The medial inferior, medial superior, lateral inferior, and lateral superior branches of Glisson and left hepatic vein were individually double-clipped using a polymer locking ligation system (Hem-o-lok ® ; Teleflex, Wayne, PA, USA) and resected. Thin vein branches were clipped using a metallic clip applier (Endo Clip ® ; Medtronic, Dublin, Ireland) and cut. Finally, the left lateral section, including the partial left median section, was resected ( Figure 6D-F). The operation time was 7 h and 35 min. The blood loss volume was 109 mL. The patient's postoperative recovery was uneventful and he was discharged on postoperative day 7. The final pathological diagnosis was well-differentiated hepatocellular carcinoma.

Discussion
To the best of our knowledge, laparoscopic sectionectomy for a malignant liver tumor in a patient with RSLT has been reported only once previously [6]. Most patients with RSLT are treated using open surgery because of the high frequency of vascular and bile duct abnormalities [5]. However, the laparoscopic approach can be safe and effective with adequate preoperative and intraoperative imaging evaluations.
Our patient exhibited an independent posterior branch of the portal venous system, which is present in more than half of patients with RSLT [1,2,5]. Shindoh et al. classified RSLT into three types based on the portal branching pattern: bifurcation, trifurcation, and independent right lateral (posterior) type [1]. In contrast, Terasaki et al. classified patients into four types: one bilateral ligamentum teres group and three RSLT groups (bifurcation, trifurcation, and independent posterior branch types) [5,7]. The newer Terasaki system may become the standard in the future. Regarding hepatic veins in patients with RSLT, a thick vein running along the ventral-dorsal segment border of the anterior sector and a developed V8 are likely to be present [1,5]. Our patient exhibited a developed V8. Because the middle hepatic vein (MHV) in patients with RSLT tends to be atrophic and displaced medially, the V8 may be misidentified as the MHV and should be treated with caution [5]. As for the hepatic artery, most bifurcate and branch normally in patients with an RSLT, as in our patient [1,8].
The bile duct system frequently does not bifurcate normally in patients with RSLT. Nishitai et al. classified the biliary architecture in such patients into four types: the symmetrical type, in which the right umbilical portion (RUP) is the watershed between the right and left branches of the bile duct; the independent right lateral type, in which the right posterior branch is independent and the right anterior sector branch comes around from the left side of the RUP; and the total left and total right types, in which the

Discussion
To the best of our knowledge, laparoscopic sectionectomy for a malignant liver tumor in a patient with RSLT has been reported only once previously [6]. Most patients with RSLT are treated using open surgery because of the high frequency of vascular and bile duct abnormalities [5]. However, the laparoscopic approach can be safe and effective with adequate preoperative and intraoperative imaging evaluations.
Our patient exhibited an independent posterior branch of the portal venous system, which is present in more than half of patients with RSLT [1,2,5]. Shindoh et al. classified RSLT into three types based on the portal branching pattern: bifurcation, trifurcation, and independent right lateral (posterior) type [1]. In contrast, Terasaki et al. classified patients into four types: one bilateral ligamentum teres group and three RSLT groups (bifurcation, trifurcation, and independent posterior branch types) [5,7]. The newer Terasaki system may become the standard in the future. Regarding hepatic veins in patients with RSLT, a thick vein running along the ventral-dorsal segment border of the anterior sector and a developed V8 are likely to be present [1,5]. Our patient exhibited a developed V8. Because the middle hepatic vein (MHV) in patients with RSLT tends to be atrophic and displaced medially, the V8 may be misidentified as the MHV and should be treated with caution [5]. As for the hepatic artery, most bifurcate and branch normally in patients with an RSLT, as in our patient [1,8].
The bile duct system frequently does not bifurcate normally in patients with RSLT. Nishitai et al. classified the biliary architecture in such patients into four types: the symmetrical type, in which the right umbilical portion (RUP) is the watershed between the right and left branches of the bile duct; the independent right lateral type, in which the right posterior branch is independent and the right anterior sector branch comes around from the left side of the RUP; and the total left and total right types, in which the entire liver is drained only by the bile duct coming around the RUP from one direction [8]. In their study, half were symmetrical and 28% were the independent right lateral type, as in our patient.
The presence of these vascular and bile duct system abnormalities can lead to unexpected complications [6,8]. In our patient, both the portal vein and the bile duct had a bifurcation type in which the right posterior branch independently diverged; this branch then diverged into the right anterior and left branches. In such cases, caution is required when performing a left lobectomy, including left lateral sectionectomy, because an incision that is too deep or more right-sided than planned may result in injury to the right anterior branch. In addition, the ligamentum teres and the falciform ligament do not represent landmarks for the P2 and P3 origins in patients with LSRT [6]. Furthermore, the misidentification of a developed V8 as MHV may lead to a situation in which a planned left lobectomy must be converted to a left trisectionectomy. These possibilities were all considered in our case. However, the points to keep in mind will vary depending on the particular combination of anatomical anomalies and the type of surgery planned.
Fifteen cases of hepatectomy for malignant tumors in patients with RSLT have been reported in the English literature: thirteen open and two laparoscopic (Table 1) [2,6,7,[9][10][11][12][13][14][15][16][17]. Three-dimensional liver anatomy simulation systems using CT images allow a detailed and easy evaluation of tumor location and vasculature. Several reports have shown that such an evaluation is quite useful in RSLT cases characterized by many anatomical abnormalities [6,15,16]. Compared with open surgery, many operations are more difficult when performed laparoscopically because of instrument angle limitations and the inability to directly observe the intraperitoneal cavity. Therefore, a careful preoperative evaluation of tumor location, progression, and anatomy is necessary. With a thorough evaluation and frequent use of ultrasonography during surgery, laparoscopic hepatectomy can be performed safely in many patients.

Conclusions
RSLT is frequently associated with abnormalities of the liver vasculature and bile duct system. These abnormalities can lead to complications when performing hepatectomy. With left lobectomy, including left lateral sectionectomy, it is important to avoid injury to the right liver vasculature. Laparoscopic hepatectomy can be performed safely in patients with RSLT, provided that careful surgical planning is conducted using preoperative three-dimensional CT analysis and intraoperative ultrasonography.  Informed Consent Statement: Informed consent was obtained from all subjects involved in the study.

Data Availability Statement:
The original data presented in the study are included in the article. Further inquiries can be directed to hidekiyokoo@asahikawa-med.ac.jp.