Author Affiliations: Department of Liver Surgery and Liver Transplantation Center, West China Hospital, Sichuan University, Chengdu 610041, China (Chen X, Li B, He W, Wei YG, Du ZG and Jiang L)

Corresponding Author: Bo Li, MD, PhD, Department of Liver Surgery and Liver Transplantation Center, West China Hospital, Sichuan University, 37 Guoxue Street, Chengdu 610041, China (Tel: 86-28-85422476; Email: cdlibo@medmail.com.cn)

 

© 2014, Hepatobiliary Pancreat Dis Int. All rights reserved.

doi: 10.1016/S1499-3872(14)60253-8

 

 

Contributors: LB proposed the study. CX and LB performed research and wrote the first draft. CX collected and analyzed the data. All authors contributed to the design and interpretation of the study and to further drafts. LB is the guarantor.

Funding: None.

Ethical approval: The study was approved by the Ethics Committee of our hospital.

Competing interest: The authors do not choose to declare any conflict of interest related directly or indirectly to the subject of this article.

 

 

BACKGROUND: Extended hemihepatectomy is usually recommended to treat large centrally located hepatocellular carcinoma (HCC). However, the morbidity and mortality are high because of the postoperative liver failure. Mesohepatectomy is seldom used because of its technical complexity. This study aimed to evaluate the short-term and long-term curative effect of mesohepatectomy.

 

METHODS: From January 2002 to September 2008, a total of 198 consecutive patients with centrally located HCC underwent hepatectomy in our department. According to the surgical procedures, they were divided into mesohepatectomy (group M, n=118), extended right hemihepatectomy (group RE, n=47) and extended left hemihepatectomy (group LE, n=33) groups. The surgical techniques, clinical pathological characteristics and outcomes were compared between group M, group RE and group LE.

 

RESULTS: The operative time of group M was significantly longer than that of the other two groups (P<0.05); however the total bilirubin on postoperative day 3 in group M was the lowest among the three groups (P<0.01). In group M, the number of the patients whose resection margin achieving 1 cm was significantly lower than that of the other two groups (P<0.05). The mortality rates in groups M, RE and LE were 2.5%, 8.5% and 3.0%, respectively (P>0.05). The morbidity rate in group M was significantly lower than that in group RE (37.3% vs 55.3%, P=0.034), but not in group LE (37.3% vs 24.2%, P=0.163). The biliary leakage tended to be more common in group M (10.2%, P>0.05). The incidence of postoperative liver failure in group M was significantly lower than that in group RE (1.7% vs 10.6%, P=0.032), but not in group LE (1.7% vs 6.1%, P=0.208). The 1-, 3- and 5-year tumor-free survival rates and the overall survival rates after mesohepatectomy were 53.4%, 30.5% and 16.9% and 67.8%, 45.5% and 28.9%, respectively.

 

CONCLUSIONS: Mesohepatectomy is a safe and effective technique for centrally located HCC patients. Compared with extended right hemihepatectomy, mesohepatectomy can retain residual liver volume to the maximum limit and reduce postoperative liver failure rate. But no significant advantage was found compared mesohepatectomy to extended left hemihepatectomy.

 

(Hepatobiliary Pancreat Dis Int 2014;13:264-270)

 

KEY WORDS: hepatocellular carcinoma; mesohepatectomy; extended hemihepatectomy; complication; survival

Hepatocellular carcinoma (HCC) is the sixth most common cancer in the world.^[1] More than one million people died from HCC each year.^[2] As we know, hepatectomy is the first choice for the treatment of HCC.^[3] Because the central HCC, which located in the liver segments IV, V and VIII±I (Couinaud's segments), is close to the first, second and third hilar, many surgeons choose extended hemihepatectomy to resect the tumor.^{[4, 5]} However, extended hemihepatectomy will theoretically increase the risk of liver failure owing to the extensive liver resection,^[6-8] especially for those with cirrhosis which frequently represents a compromised liver function and regenerative capacity. The mortality rate will reach to 10% as described in the literature.^[9]

 

In 1972, McBride and Wallace^[10] performed the first en bloc resection of liver segments IV, V and VIII successfully. This technique was gradually adopted by surgeons and named as mesohepatectomy. Compared with the extended hemihepatectomy, mesohepatectomy can keep residual liver volume as much as possible and effectively decrease the occurrence of postoperative liver failure.^[11] Because of its complex technical requirements, however, mesohepatectomy was still not widely used. To the best of our knowledge, there were only few nonrandomized retrospective studies on whether mesohepatectomy or extended hemihepatectomy is the preferred option for treatment of central HCC. In recent years, with the accumulation of clinical experience and continuous improvement of surgical techniques, more mesohepatectomies have been performed in our hospital. This study aimed to compare the short-term and long-term outcomes of the two methods (mesohepatectomy vs extended hemihepatectomy) for the patients with central HCC.

 

 

From January 2002 to September 2008, a total of 198 consecutive patients with centrally located HCC underwent hepatectomy in our department. Informed consent was obtained from each patient, and the study was approved by the Ethics Committee of our hospital.According to the surgical procedures, they were divided into three groups, group M (n=118): the patients underwent mesohepatectomy; group RE (n=47): the subjects underwent extended right hemihepatectomy, and group LE (n=33): the patients underwent extended left hemihepatectomy. All patients were assessed for the resectability of the tumor as well as its relationships with the liver vasculature through enhanced CT or MRI. The functional reserve of the liver was evaluated by biochemical test, indocyanine green retention rate at 15 minutes and blood coagulation test. The choice of surgical approach was determined by comprehensive assessment of liver function, future residual liver volume, imaging studies, and tumor characteristics such as location, size and vascular involvement. Mesohepatectomy was performed preferentially as long as each side of the peripheral segment of the liver could be preserved. If this was not feasible, extended hemihepatectomy was carried out.^[12] The tumor pathological stage was classified according to the Japanese tumor node metastasis (TNM) classification system^[13] and tumor differentiation by the Edmondson criteria.^[14] We used the 50-50 criteria (prothrombin time <50% and serum bilirubin >50 µmol/L on postoperative day 5) to define postoperative liver failure.^[15]

 

After general anesthesia, a J-shaped right subcostal incision was made to expose the abdominal cavity, then both right and left perihepatic attachments were divided. Intraoperative ultrasonography was used to detect the tumor region and, existence of intrahepatic metastasis and cancer embolus in the portal vein and hepatic vein; meanwhile, the spatial relations between the tumor and the vascular system were also thoroughly examined. We did not dissect the hepatic hilus, instead, we utilize Glissonean pedicle transection method to reduce operative time and intraoperative bleeding as well as the metastases which might occur through the portal vein during operation.^[16] Cholecystectomy was performed at the beginning, followed by removal of the connective tissues within the Calot's triangle, exposing and mobilizing the right anterior Glissonean pedicle. Then a blocking strap was placed around the root of the right anterior Glissonean pedicle using a blunt-end right angle clamp, followed by transection of the right anterior Glissonean pedicle. The left and right posterior branches of Glissonean pedicle were prepared for blocking. After the above procedures were completed, ischemia area appeared obviously. During the liver resection, the blood flow into the right and the left liver was blocked alternately, each blockade lasted for 30 minutes with a 5-minute intermission. The liver parenchyma was dissected using Cavitron Ultrasonic Surgical Aspirator (CUSA; Valleylab, Boulder, CO, USA); the major vessels and bile ducts encountered were ligated and cut using titanium clips or silk suture. The central venous pressure was maintained below 5 mmHg so as to effectively reduce bleeding from the hepatic vein during liver resection.^[17] After the resection, intraoperative cholangiography through the cystic duct was performed to check whether there were an injury to the right posterior branch of the bile duct and bile leakage. The wound surface was covered with SURGICEL (Johnson & Johnson Medical, Gargrave, UK); and two 24F drainage tubes were placed at the wound surface and at the foramen of Winslow.

 

After cholecystectomy, the left tertiary branches of Glissonean pedicle which supply the segment IV were dissected along the right side of the umbilical portion which made the dissection of the right posterior and anterior Glissonean pedicles much easier. The liver parenchyma was cut off under intermittent blood blocking (15-minute clamping periods separated by 5-minute intervals). An electrotome was used to mark the boundary between the left lateral lobe and segment IV, and CUSA to dissect the liver upward along the right side of the falciform ligament. After hemostats of the surgical wound surface, the resection area was covered with SURGICEL, drainage tubes were placed properly, followed by abdominal closure.

 

After cholecystectomy, the left and the right anterior Glissonean pedicles were blocked, the ischemic area in the liver was identified. After mobilization of the left lobe, the hepatogastric ligament, the retroperitoneum on the left side of the retrohepatic inferior vena cava, the left short hepatic vein and the Arantius duct were ligated and cut. The right lobe was mobilized, and the right short hepatic vein was then processed. The liver was cut off using CUSA and with the dissection going deeper, the anatomic structure of the hepatic hilus was identified from the cephalad; then, the remaining portal vein and bile duct were cut off. The left and middle hepatic veins were continuously sutured using 5-0 prolene. The wound surface was covered with SURGICEL, and drainage tubes were routinely placed. The operation was completed after abdominal closure.

 

After operation, electrocardiogram monitoring, oxygen inhalation, antibiotics, liver protecting drugs, albumin support and maintenance balance of water and electrolyte were routinely applied. Blood routine analysis, liver function and coagulation function were examined at postoperative days 1, 3, 5 and 7. Chest radiography and abdominal ultrasound were used according to the postoperative conditions. The follow-up was carried out in the outpatient service. Abdominal ultrasound, blood routine test, serum biochemical test and alpha-fetoprotein measure were performed every month for the first half year, then every 3 months. CT or MRI was performed when in suspicion of HCC recurrence.

 

Statistical analysis was performed with SPSS 16.0 for Windows. The data were expressed as the number (percentage) and mean±SD (range). The continuous variables were compared using one-way analysis of variance (ANOVA). Frequencies were evaluated by the Chi-square test and Fisher's exact test. The cumulative survival rate and the cumulative tumor-free survival rate were calculated using the Kaplan-Meier method. Statistical differences were tested by the log-rank test. A P value of <0.05 was considered statistically significant.

 

 

The demographic data of the three groups are shown in Table 1. All patients had Child-Pugh class A. The preoperative transarterial chemoembolization rates in groups M, RE and LE were 8.5%, 17.0% and 12.1%, respectively. According to the TNM classification, none of the patients in our study belongs to stage I. There were no statistical differences in demographic data between group M, group RE and group LE.

 

The mean operative duration was 244.3±55.3 minutes in group M which was longer than that in group RE (225.3±43.1 minutes) or group LE (218.9±37.2 minutes) (P<0.05). The total bilirubin on postoperative day 3 in group M was lowest compared with the other two groups (P<0.01, Table 2). The rate of resection margin achieving 1 cm in group M was 66.9% and significantly lower than that in group RE and group LE (83.0% and 84.8%, respectively, P<0.05). No statistically significant difference was observed in the three groups in intraoperative blood transfusion, tumor size, vascular invasion, pathological classification and total occlusion time of hepatic inflow. The levels of alanine aminotransferase and albumin on postoperation day 3 were also not significantly different.

 

Complications are summarized in Table 3. The morbidity rate in group M was significantly lower than that in group RE (37.3% vs 55.3%, P=0.034), but not in group LE (37.3% vs 24.2%, P=0.163). The most common postoperative complication was pleural effusion, which usually resolved after conservative treatment. The incidence of postoperative liver failure in group M was significantly lower than that in group RE (1.7% vs 10.6%, P=0.032), but no in group LE (1.7% vs 6.1%, P=0.208). Biliary leakage tended to be more common in group M (10.2%, P>0.05). There were no significant differences in hemorrhage, pulmonary infections, wound infection and deep venous thrombosis. The postoperative level of direct bilirubin of a patient in group RE increased progressively, and choledochojejunostomy anastomosis was made secondarily after left hepatic duct stenosis was confirmed by magnetic resonance cholangiopancreatography. Three patients died within 30 days postoperatively in group M (2.5%): 2 died from liver failure and 1 from severe pulmonary infection; 4 patients died postoperatively in group RE (8.5%): 3 died from liver failure and 1 from postoperative bleeding; one patient died from liver failure in group LE. There was no significant difference in the postoperative mortality rate in 30 days among the groups (P>0.05).

 

Postoperative pathological examination revealed that all patients underwent radical excision. None of them received postoperative cancer adjuvant therapy until tumor recurrence. The mean follow-up time was 36.5±28.6 months (range 1-96). The 1-, 3- and 5-year overall survival rates and tumor-free survival rates of 198 patients with centrally located HCC after hepatectomy were 70.2%, 45.1% and 29.5% and 56.6%, 33.3% and 21.1%, respectively (Fig. 1). The 1-, 3- and 5-year overall survival rates after mesohepatectomy (n=118) were 67.8%, 45.5% and 28.9%, whereas after extended hemihepatectomy (n=80) 73.8%, 44.5% and 30.3%, respectively (P=0.580) (Fig. 2). The 1-, 3- and 5-year tumor-free survival rates were 53.4%, 30.5% and 16.9% after mesohepatectomy (n=118) versus 61.2%, 37.5% and 27.4% after extended hemihepatectomy (n=80), respectively (P=0.107) (Fig. 3).

 

 

Extended hemihepatectomy is usually recommended to treat large centrally located liver tumor. However, extended hemihepatectomy is associated with a high risk of liver failure because of extensive liver resection.^[18] The mortality rates of patients with cirrhosis undergoing liver resection is 8%-32%.^{[19, 20]} Furthermore, HCC patients in China are usually viral hepatitis/cirrhosis related. Chen et al^[21] analyzed 256 cases of central-type HCC and found that 84% of them had cirrhosis. Therefore, extended hemihepatectomy is limited to the patients with well-preserved liver function. Portal vein embolism increases the residual liver volume as the preparation for the extended hemihepatectomy to help patients go through the perioperative period safely.^[22,23] However, this procedure might not work well for centrally located HCC, because the central region of the liver has two blood supplies (left and right). Even if one branch of the portal vein is blocked, the tumor can still progress with a comparatively high speed.^[24] Mesohepatectomy represents an alternative option for those patients with liver cirrhosis and this surgical technique might improve the perioperative management to some extent.

 

In this study, the baseline characteristics were similar among the three groups. Compared with extended right/left hemihepatectomy, mesohepatectomy had a longer operative time, which was similar to the results of other reports.^{[25, 26]} The possible reasons might be: i) The tumor clings to important tissue structures such as the portal vein, the hepatic vein and the inferior vena cava, which are prone to massive hemorrhage; ii) Large surgical wound surfaces indicate that more liver parenchyma should be dissected; iii) The blood supply should be carefully preserved for the remnant liver to prevent postoperative necrosis; iv) Cholangioplasty is sometimes needed. Intraoperative blood loss is undoubtedly related to postoperative complications.^[27]

 

The amount of intraoperative blood transfusion in mesohepatectomy was comparable with that in extended left hemihepatectomy and was lower than that in extended right hemihepatectomy although it required a larger surgical wound surface and a longer operative duration. This may be attributed to the Glissonean pedicle transection method, low central venous pressure and the use of intraoperative ultrasonography. Recent studies^{[28, 29]} reported that during the parenchymal phase, clamping the infrahepatic inferior vena cava is more effective in reducing intraoperative bleeding while maintaining the intraoperative hemodynamic stability.

 

Since mesohepatectomy leads to a larger transection plane, it is performed around the major bile ducts. Some studies^{[11, 30, 31]} reported that mesohepatectomy was associated with higher surface-related complications such as postoperative bleeding and bile leakage. In our study, the rate of bile leakage was the highest in group M (10.2%). Although there is no statistical difference, the possibility that the mesohepatectomy has a higher bile leakage rate still cannot be ruled out. No statistical difference may be due to the small samples, so the P value in this case may represent underpower for leak detection, and more case analyses are needed in future studies. In addition, comparison of mesohepatectomy with extended hemihepatectomy revealed that bile leakage was significantly higher in mesohepatectomy (10.2% vs 2.5%, P=0.039) (data not shown).

 

We did not find the significant difference in the mortality rate among the groups. However, the present study demonstrated that mesohepatectomy was superior to extended hemihepatectomy in terms of the preservation of liver function. The postoperative liver failure rate was the highest in group RE, indicating the extent of parenchymal resection. According to the literature, right hepatic trisegmentectomy combined with caudate lobectomy is equivalent to 81% liver resection, and left liver trisegmentectomy combined with caudate lobectomy corresponds to 67% liver resection.^[32] Therefore, portal vein embolism should be exclusively performed in patients undergoing extended right hemihepatectomy, because the liver remnant may be <20% of the total liver volume after extended right hemihepatectomy.^[33] Compared with extended right hemihepatectomy, mesohepatectomy avoided unnecessary sacrifice of functional parenchyma and reduced the postoperative liver failure rate. It also increased the chance for a second liver resection for recurrent intrahepatic tumor.^[34]

 

The tumor-free survival rate tends to be lower in patients undergoing mesohepatectomy than in those undergoing extended hemihepatectomy. This may be associated with a narrow resection margin in mesohepatectomy. It is sometimes difficult to keep the surgical margin to 1 cm in all directions in mesohepatectomy because when the tumor is close to the liver vein branches the dissection must be performed close to the tumor side.^[17] Chen et al^[35] found that preoperative transarterial chemoembolization for large centrally located HCC improved the cumulative survival and disease-free survival rates. Okano et al^[36] suggested that preoperative transarterial chemoembolization might reduce the rate of intrahepatic recurrence after liver resection for HCC.

 

In conclusion, mesohepatectomy is a safe and effective treatment for centrally located HCC patients. Compared with extended right hemihepatectomy, mesohepatectomy could retain residual liver volume to a maximum and reduce the postoperative liver failure rate. But mesohepatectomy is not superior to extended left hemihepatectomy.

 

 

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