Dorsal approach with Glissonian approach in laparoscopic anatomic hepatectomy for right lobe

Background: Laparoscopic anatomic hepatectomyLAHhas gradually become the routine surgical procedure. We reported previously that Glissonian approach combined with major hepatic vein first was effective for LAH. Owing to Dorsal approach could expose the major hepatic vein effectively, we merged dorsal approach and Glissonian approach in LAH for right lobe. Methods: Twenty patients who underwent LAH from January 2017 to November 2018 were retrospectively analyzed. These comprised seven patients who underwent laparoscopic right hemihepatectomy (group LRH), seven patients who underwent laparoscopic right posterior hepatectomy (group LRPH), and six patients who underwent laparoscopic hepatectomy for segment 7 (group LS7). Firstly, the corresponding hepatic pedicles were isolated through Glissonian approach. Next, the liver parenchyma was transected by dorsal approach until the corresponding major hepatic vein was exposed. Then liver parenchyma was transected by a ventral approach. Finally, the root of the major hepatic vein was transected. Results: The mean age of the patients was 53.8 years and the male: female ratio was 8:12. The median operation time was 306.0 ± 58.2 min and the mean estimated volume of blood loss was 412.5 ± 255.4 mL. The mean duration of postoperative hospital stay was 10.2 days. The mean Pringle maneuver time was 64.8 ± 27.7 min. Five patients received transfusion of 2–4 U of red blood cells. Two patients suffered from transient hepatic dysfunction and one from pleural effusion. No patient underwent conversion to an open procedure. The operative duration, volume of the blood loss, Pringle maneuver time, and postoperative hospital stay duration did not differ significantly among groups LRH, LRPH, and LS7 (P > 0.05). Conclusion: Dorsal approach combined with Glissonian approach for right lobe in LAH is feasible and effective, though, it is essential to include more cases for further study.

Two patients suffered from transient hepatic dysfunction and one from pleural effusion. No patient underwent conversion to an open procedure. The operative duration, volume of the blood loss, Pringle maneuver time, and postoperative hospital stay duration did not differ significantly among groups LRH, LRPH, and LS7 (P > 0.05).
Conclusion: Dorsal approach combined with Glissonian approach for right lobe in LAH is feasible and effective, though, it is essential to include more cases for further study.

Background
Hepatectomy has become a curative procedure for several liver diseases, such as liver neoplasms and hepatolithiasis 1 − 6 . Since being first successfully performed in 1991 7 , laparoscopic hepatectomy has become a routine procedure 8,9 . However, the technical difficulties and the unique vision of laparoscope have restricted performance of laparoscopic anatomic hepatectomy (LAH) remaining in large medical centers 10,11 . Use of an appropriate approach can reduce the operation time and the volume of blood loss, promoting recovery 12,13 . We reported previously the feasibility of LAH using the Glissonian approach combined the major hepatic vein first 14 . However, exposing the whole hepatic vein is still a challenge because of the caudate lobe, particularly in right hepatectomy. Dorsal approach in laparoscopic left hemihepatectomy (LLH) was firstly reported to be efficient in 2014 15 , which was free to transect the caudate lobe. Therefore, we combined dorsal approach and Glissonian approach in LAH for right lobe to expose the hepatic veins quickly. This surgical procedure is safe and effective for LAH, including for laparoscopic right hemihepatectomy (LRH), laparoscopic right posterior hepatectomy (LRPH), and laparoscopic segmentectomy for segment 7 (LS7).

Patients
From January 2017 to November 2018, 20 patients underwent LAH in Department of Hepato-biliarypancreatic Center and Transplantation Center, the Affiliated Drum Tower Hospital, School of Medicine, Nanjing University. Among the patients, seven underwent LRH (group LRH), seven received LRPH (group LRPH), and six patients underwent LS7 (group LS7). Seven of the patients had hepatocellular carcinoma (HCC), one had intrahepatic cholangiocarcinoma (ICC), seven had hepatic hemangioma, three had hepatolithiasis (HH), one had hepatic adenoma (HA), and one patient had hepatic angiomyolipoma (HAML). The perioperative indices of all patients are listed in Table 1.

Operative procedures
The preoperative evaluation, postoperative management, port arrangement, and positioning of the 20 patients were as described previously 14 . All patients were placed in a left semi-decubitus position.
The main surgeon stood on the patient's left side. The patient was placed in the reverse Trendelenburg position and the central venous pressure was maintained at < 5 cmH 2 O. Five trocars were needed for LAH. One 12 mm paraumbilical trocar and carbon dioxide were used to establish the pneumoperitoneum, the pressure of which was maintained at 10-12 mmHg. A 30° flexible laparoscope was introduced through the paraumbilical trocar, and the other four working trocars were placed surrounding the right lobe. A tourniquet for the Pringle maneuver was set using a Nelaton catheter and vessel tape through a 5 mm incision on the left mid-clavicular line. The Pringle maneuver was performed at 15-min intervals to control hemorrhage. The operation began with division of the falciform ligament, which exposed the gap between the middle hepatic vein (MHV) and right hepatic vein (RHV). Next, the gallbladder was resected (in LRH or LRPH). The paracaval portion of the caudate lobe was freed from the IVC by means of the liver hanging maneuver.
Glissonian approach served to isolate and dissect the corresponding hepatic pedicles (right pedicle for LRH, right posterior pedicle for LRPH, or the pedicles for S7), then the demarcation line of the ischemic area appeared on the liver surface. Harmonic shear was used to transect parenchyma between IVC and main hepatic vein (MHV or RHV) firstly through dorsal approach. The corresponding major hepatic vein exposed from the dorsal approach as the intrahepatic landmark. Liver parenchyma between the diaphragmatic demarcation along the MHV or RHV was transected through the ventral approach toward to the root of the RHV. The branches of the hepatic vein were dissected by Hem-Olok ligating clip, meanwhile the root of the RHV was dissected by an automatic stapler in LRH or LRPH.
Lastly the specimen was free from the coronary, right triangular ligaments, and right adrenal gland.
The key procedures were summarized. ( Fig. 1 for LRH, Fig. 2 for LRPH, Fig. 3 for LS7 ). The tumor specimen was removed via a mini-laparotomy.

Statistical Analysis
Data analysis was conducted using SPSS Version 21.0 (SPSS, Inc., Chicago, IL, USA). The operative duration, volume of the blood loss, Pringle maneuver time, and postoperative hospital stay duration (POD) were analyzed. Data are expressed as medians (range) and were compared by one-way analysis of variance or the Kruskal-Wallis test. A value of P < 0.05 was considered indicative of statistical significance.

Results
The mean age of the patients was 53.8 years (range 35-66 years), and the male: female ratio was None of the 20 patients underwent conversion to an open procedure. The operative duration, volume of the blood loss, Pringle maneuver time, and POD did not differ significantly among groups LRH, LRPH, and LS7 (P > 0.05) (Fig. 4).

Discussion
Anatomic hepatectomy is beneficial for patients with HCC in terms of the recurrence-free survival rate compared with non-anatomic hepatectomy in open surgery, although it may increase the operation time 16 − 20 . Because anatomic hepatectomy is based on the inflow and outflow corresponding to the target lobe or segment, the root of the Glisson pedicle and hepatic vein can serve as extrahepatic landmark, while the major hepatic vein can serve as intrahepatic boundary. Therefore, the pedicle is isolated through Glissonian approach, while the intrahepatic main hepatic vein is located with the guidance under intraoperative ultrasound. It is still a challenge for performers to locate the intrahepatic major hepatic vein under laparoscopy because of the double transection of two dimensions, especially in LAH, having a long learning curve of close to 50 cases 21,22 .
We reported in 2017 that the pedicles are connected to the corresponding main hepatic veins and we could expose the major hepatic vein first 14 . We used this strategy to perform more than 50 patients.
During LAH, we found that the caudate lobe hampered exposure of the main hepatic veins. This hindered to expose the middle hepatic vein in right hepatectomy or of the right hepatic vein in right posterior segmentectomy. Koki Maeda et al. 23 previously reported 13 patients underwent LRH with caudodorsal appoach. Soubrane Olivier et al. 24 deemed that it is unnecessary for liver hanging maneuver. However, when a patient suffered from a huge carcinoma, due to little space to reverse the liver and expose the whole IVC, it is difficult to transect the liver through dorsal approach. The liver hanging maneuver is critical in hepatectomy 25 . Under laparoscopic view, it is convenient to perform hanging maneuver than under open view and we use this way in all cases 26 . When Glisson pedicles were isolated, Goldfinger dissector was used to dissect the anterior surface of the IVC. With the assistance of intraoperative ultrasound and extrahepatic landmark, we have enough space to transect the parenchymal between IVC and MHV through hanging maneuver. Although a group of scholars hold that ventral approach using the liver hanging maneuver is better than caudal approach, the number of the patients is too small and it is a retrospective study design 27 . High quality of randomized controlled trials (RCT) are required, and we have registered a Chinese clinical trial in 2018 titled "A randomized controlled trial of Glissonian maneuver combined with dorsal approach and anterior approach: a practical strategy for laparoscopic anatomic hepatectomy" (ChiCTR1800015563).
Under laparoscopic view, Glissonian approach could find the main hepatic vein quickly, while dorsal approach could transect the caudate lobe with the liver hanging maneuver effectively. Thus, combined dorsal approach with Glissonian approach could facilitated exposure of the entire main hepatic vein. This modified strategy was testified to be feasible and efficient in LRH, LRPH and LS7 as well.
When performing segmentectomy for S7, dorsal approach cannot apply to the liver with thick inferior right hepatic vein. Okuda et al. 28 reported six patients were performed LS7 through intrahepatic Glissonian approach with dorsal approach by intercostal trocars, which could increase the risk of intercostal artery hemorrhage and need two more trocars. In our center, the main surgeon stood on the patient's left side, which could follow an oblique angle and expose the right hepatic vein. By means of intraoperative ultrasound, S7 pedicles could be showed from the dorsal vision.
Although it still took us a long time to perform LAH with dorsal approach and Glissonian approach, the distinct landmark made us no longer 'get lost'.

Conclusion
Dorsal approach with Glissonian approach in LAH for right lobe is feasible and effective. However, the operation time was approximately 300 min, similar to that of the traditional approach. The sample size was small and it is essential to include more cases for further study.

Consent for publication
Written informed consent for publication was obtained from all of the patients. Copies of consent forms containing personal or clinical details or any identifying images published in this study are available on request.

Availability of data and materials
All data generated or analyzed during this study are included in this published article and its supplementary information files. The datasets generated and analyzed during the current study are available from the corresponding author by email yudecai@nju.edu.cn on reasonable request.

Competing interests
The authors declare that they have no competing interests.