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DOI:10.1111/j.1477-2574.2012.00615.x
ORIGINAL ARTICLE
Outcomes of central bisectionectomy for hepatocellular carcinoma Thomas K. Gallagher1, Albert C.Y. Chan1, Ronnie T.P. Poon1,2, Tan To Cheung1, Kenneth S.H. Chok1, See Ching Chan1,2 & Chung Mau Lo1,2 1
Department of Surgery and 2State Key Laboratory for Liver Research, The University of Hong Kong, Hong Kong
Abstract Background: Central bisectionectomy (resection of Couinaud segments IV, V and VIII) for malignant or benign disease poses a technical challenge to the surgeon but if feasible, has significant benefits in terms of conserving liver volume and options for future intervention. This study reviews a cohort of patients who underwent this procedure; outlines the indications, optimal operative technique as well as both short- and long-term outcomes. Methods: A retrospective review of a prospectively maintained database was performed. Pre-operative clinicopathological data, operative details and post-operative outcomes including overall and diseasefree survival were analysed. Results: Between 1989 and 2009, 21 patients underwent a central bisectionectomy. All procedures were performed for hepatocellular carcinoma (HCC). All patients underwent a R0 resection with a median resection margin of 5 mm (1–15 mm). The 1-, 3- and 5-year disease-free survivals were 65%, 34.8% and 34.8%, and the corresponding overall survival rates were 90.5%, 66.8% and 66.8%, respectively. Conclusion: These data support the use of a central bisectionectomy in selected cases in the management of HCC. With the use of a meticulous operative technique and adherence to surgical oncological principles, satisfactory long-term outcomes were achievable. Received 15 August 2012; accepted 2 October 2012
Correspondence Albert C. Y. Chan, Department of Surgery, Queen Mary Hospital, 102 Pokfulam Road, Hong Kong. Tel: +852 22553025. Fax: +852 28165284. E-mail:
[email protected]
Introduction Hepatic resection remains an important curative treatment option for patients with hepatocellular carcinoma (HCC). With refined surgical techniques and better peri-operative management, liver resection has become a safer operation.1 As a result, more extensive and complicated liver resections have been advocated. A central bisectionectomy (resection of Couinaud segments IV, V and VIII) for malignant or benign disease poses a technical challenge to the surgeons. It is often indicated for centrally located HCC in patients with a marginal liver volume. Recent studies have shown the survival benefit of an anatomical resection over a nonanatomical resection.2–4 Indeed, anatomical resections according to the architecture of the portal vein have the potential to remove undetected cancerous foci disseminated from the primary tumour.5A central bisectionectomy has the dual benefits of preserving the liver volume and complete oncological clearance. Nonetheless, there is a scarcity of data in addressing the operative
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technicality, post-operative and oncological outcome of this operation. The aim of this study was to review the role of a central bisectionectomy in the management of patients with HCC.
Methods From January 1989 to December 2009, 1406 patients underwent hepatic resections for HCC at the Department of Surgery in Queen Mary Hospital. Among them, 21 patients received hepatic resections of Couinaud’s segment 4,5 and 8 (i.e. a central bisectionectomy) as defined by the International HepatoPancreato-Biliary Association (IHPBA) classification.6 Their clinicopathological and peri-operative details were reviewed. The selection criteria employed for a major hepatic resection included Child–Pugh class A cirrhosis, a indocyanine clearance rate ⱕ15% at 15 min, a platelet count ⱖ100 ¥ 109/l and the absence of ascites. A central bisectionectomy was considered for centrally locating the tumor when a right or left trisectionectomy would result in a
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liver remnant volume less than 30% of the estimated total liver volume in normal liver or less than 35% in a cirrhotic liver, irrespective of the tumour size. The anatomical relationship of the tumour in relation to the hepatic veins, portal veins and bile ducts was evaluated by high-resolution computed tomography (CT). Statistical analysis Disease-free and overall survivals were assessed by Kaplan–Meier methods. Continuous variables were expressed in median (range) and compared between subgroups when appropriate using the Mann–Whitney U-test. Categorical variables were compared between subgroups using the chi-square test. A P-value ⱕ0.05 was considered to be significant. Statistical analysis was performed using computer software SPSS Version 16.0 (SPSS Inc., Chicago, IL, USA). Operative technique Surgical exposure is obtained via a bilateral subcostal incision with midline sternal extension. An intra-operative ultrasonography is performed routinely to detect any tumour invasion into the main right and left portal veins, and if there is any additional tumour nodule in the rest of the liver. The falciform ligament is then divided and the suprahepatic inferior vena cava and hepatic veins are exposed. Both the right liver and left lateral sections are mobilized after division of the ligamentous attachments to the diaphragm. A cholecystectomy is then performed and the cystic duct is cannulated with a Fr3.5 Argyle infant feeding tube. Parenchymal transection is performed with an ultrasonic dissector under a low central venous pressure (<5 mmHg) achieved by intravenous fluid restriction with or without a low dose of intravenous frusemide (5–10 mg). An intermittent Pringle manoeuver is applied when excessive bleeding is encountered during parenchymal transection. The central bisectionectomy is commenced by dividing branches of the inflow portal pedicle to Segment 4b that arises from right side of the falciform ligament. Once the left Glissonian sheath comes into operative view as segment 4 is separated away from the left lateral section, the plane of the parenchymal transection turns medially and follows the anterior surface of the left Glissonian sheath, then to the right Glissonian sheath that contains the right anterior portal pedicle. Use of an ultrasonic dissector facilitates exposure of the Glissonian sheath and the hepatic veins that provide important anatomic landmark and hence, guidance to the plane of transection. To facilitate identification of the left Glissonian sheath, a large metal clip may be placed in its vicinity followed by an operative cholangiography. The right anterior Glissonian sheath is then isolated and divided. By now, the ischaemic demarcation of the right anterior section i.e. segment 5 and 8 becomes apparent. The plane of transection follows the demarcation line posteriorly and cranially until the root of middle hepatic vein is reached (Fig. 1a). A selective Pringle manoeuver with inflow control of the right portal pedicle may facilitate transection along the right lateral plane with preservation of perfusion to the left lateral section. The course of the right
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hepatic vein is an important landmark that guides the transection towards the inferior vena cava and the root of the middle hepatic vein (Fig. 1b) which is divided using a vascular stapler towards the end of the operation. Haemostasis is ensured and a bile leak test is performed by injecting 10 ml of methylene blue solution into the biliary tree via the cystic duct. A completion cholangiogram is performed to confirm the patency of the right posterior duct and the left duct. The raw surface of the liver is covered by a piece of greater omentum and placement of an abdominal drain is considered if necessary. Post-operative tumour surveillance and management of recurrences CT of the liver is performed at 1 month after resection to confirm macroscopic tumour clearance and subsequently repeated every 3 months in the first 2 years after the resection, and every 6 months thereafter. Blood sampling for serum alpha-fetoprotein (AFP) and liver biochemistry are also performed at 3-monthly intervals in the first 2 years after resections and 6 monthly in subsequent years. Intra-hepatic recurrence is defined as new lesions with a typical contrast enhancement pattern on CT scan. Repeated resection would be first considered providing the tumor is anatomically resectable and the liver function is well preserved. Radiofrequency ablation, transarterial oily chemoembolization or salvage liver transplantation would be considered otherwise.
Results Table 1 lists the patient and tumour characteristics of 21 central bisectionectomies performed for HCC. All patients had Child– Pugh Class A cirrhosis. Table 2 summarizes the intra-operative and immediate post-operative data. A peri-operative blood transfusion was required in 12 patients. Four patients developed postoperative complications. There was one in-hospital mortality that occurred in a 65-year-old patient who developed multi-organ failure and succumbed on post-operative day 4 after resection of a 10-cm tumor in segment 4,5 and 8. The median duration of hospital stay was 7 days (interquartile range 5–10). The median tumour size was 7 cm (2.3–11). All patients underwent a R0 resection with a median resection margin of 5 mm (1–15). The median follow-up was 32.3 months. The 1-, 3- and 5-year disease-free survivals were 65%, 34.8% and 34.8% (Fig. 2), and the corresponding overall survival rates were 90.5%, 66.8% and 66.8%, respectively (Fig. 3). Intrahepatic recurrences were detected in seven patients at the time of analysis. Among them, five patients received second resections for first recurrence and two patients received third resections for second recurrence. Among those patients who received second resections for tumour recurrence, three of them underwent a right posterior sectionectomy for segment 7 recurrences due to adequate hypertrophy of the left lateral section, and two patients received wedge resections for recurrence in segments 2 and 7, respectively.
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a
b
c
d
e
Figure 1 (a) Magnetic resonance imaging (MRI) of a centrally located tumour in a 50-year old patient. Volumetry confirmed that an extended
right hepatectomy would leave just 24% of the liver volume remaining whereas an extended left hepatectomy would leave 32%, an unacceptably small volume in a patient with chronic hepatitis B and early cirrhosis. (b) Operative view after a central bisectionectomy (RHV, right hepatic vein; IVC, inferior vena cava; RPP, right posterior portal pedicle; S4P, ligated stump of segment 4 portal pedicle). (c) Post-operative computed tomography (CT) images of the liver remnant. Note that the left lateral section has hypertrophied. (d) A solitary intrahepatic recurrence in S7 at 7 months after the first resection; (e) further hypertrophy of left lateral section after right posterior sectionectomy for S7 recurrence HPB 2013, 15, 529–534
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Table 1 The clinicopathological data of patients with a central bisectionectomy
Age (years)
62.0 (38–72)
Gender (M/F)
19:2
Aetiology HBsAg positivity
16
Anti-HCV positivity
2
Idiopathic
3
Pre-operative liver function reserve Serum bilirubin (umol/l)
13 (5–23)
Serum GOT (IU/l)
47 (27–145)
Serum albumin (g/l)
43 (32–48)
Serum creatinine (mmol/l)
89 (51–114)
Platelet count ¥109/l
194 (103–282)
ICG (%)
9.9 (1.3–25.7)
Tumour characteristics Solitary HCC
19
Portal vein invasion
6
Microvascular invasion
7
Tumour differentiation Well differentiated
7
Moderately differentiated
9
Poorly differentiated
5
Figure 2 Disease-free survival after a central bisectionectomy
Tumour staging AJCC TNM (7th TNM)5 Stage I
12
Stage II
3
Stage IIIA + IIIB
5
Stage IV
1
HCC, hepatocellular carcinoma.
Table 2 Intra-operative and immediate post-operative data
Length of procedure (min) Blood Loss (ml)
627 (240–1149) 1590 (120–3750)
Complications Chest infection
1
Pleural effusion: tapping not required
2
Pleural effusion: tapping required
1
Urinary tract infection
1
Cardiac arrhythmia
1
Liver failure
1
Renal failure
1
Others DVT
1
Wound Infection
0
Bile leak Mortality in first 30 days DVT, deep vein thrombosis.
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0 1 Figure 3 Overall survival after a central bisectionectomy
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Discussion The concept of a central bisectionectomy as a technique in its own right, which has been outlined in this paper, is not new. A number of authors, as far back as 1972, have previously described this procedure7,8; however, as Yanaga pointed out in a description of the technique,9 it is not described in the Brisbane 2000 system of nomenclature of hepatic anatomy and resections, the universal terminology approved by the IHPBA in 2000.10 A central bisectionectomy is one of the most technically challenging procedures in a liver resection, especially for cirrhotic livers. A genuine appreciation of the liver anatomy is imperative to conduct this procedure safely without compromising the oncological clearance. As this procedure is usually indicated for patients with a marginal liver volume, failure to recognize and safeguard the right posterior or left portal pedicle intraparenchymally may lead to insufficient remnant liver volume and subsequently post-hepatectomy liver failure. The routine use of the ultrasonic dissector for a parenchymal transection in the present series facilitates exposure of the portal pedicles which are important landmarks to guide the plane of transection. Without adequate exposure of these important biliary and vascular anatomical landmarks, the plane of transection may be easily skewed into the right posterior section or left lateral section, hence sacrificing more non-tumourous liver parenchyma. Likewise, the anatomical course of a right hepatic vein provides an important landmark to guide the parenchymal transection deep to the root of the middle hepatic vein. Failure to establish this transection plane could leave excessive segment 4 tissues close to the root of the middle hepatic vein and could potentially compromise the deep posterior and lateral resection margin in large tumours. Conversely, a major drawback of using an ultrasonic dissector especially for two different transection planes is the prolonged operative time compared with other studies.11,12 Nonetheless, only a meticulous transection permits the performance of a precise hepatectomy that is regarded as an important technical attribute to the feasibility of this complicated operation. An adequate resection margin is often considered an important surgical factor to ensure long-term disease-free survival after a liver resection.13 However, in the setting of a central bisectionectomy, the resection margin is often limited by the anatomical boundary of the major vascular and biliary pedicle. Recent studies have shown that a narrow resection margin may not compromise the oncological efficacy of this operation.14,15 The findings from the present study confirmed that in spite of a narrow resection margin, satisfactory disease-free survival is still attainable as long as an R0 tumour clearance is achieved. One important finding from the present study was the high proportion (71%) of patients amenable for a repeated resection for post-operative tumour recurrence. A repeated resection has been shown to be an efficacious treatment for recurrent HCC in recent studies.16,17 The findings from the present study showed that a completion right hepatectomy was often feasible for tumour
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recurrence in the right posterior section because of left lateral section hypertrophy (Fig. 1c–e). This illustrated the benefit of a central bisectionectomy in the preservation of remnant liver volume so as to enhance the opportunity for further resection if needed.
Conclusion Central bisectionectomy is a technically challenging operation that demands a thorough analytical knowledge of the liver anatomy. This study demonstrates that it is a safe and oncologically appropriate operation for centrally located HCC with satisfactory long-term survivals, and permits repeated resections for post-operative tumour recurrence. Conflicts of interest None declared.
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Long-term follow-up of central hepatocellular carcinoma in comparison
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