Annals of Surgical Oncology Cite Track
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10.1245/ASO.2006.08.007
Annals of Surgical Oncology 13:940-946 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Effects of Location and Extension of Portal Vein Tumor Thrombus on Long-Term Outcomes of Surgical Treatment for Hepatocellular Carcinoma

Xiao-Ping Chen, MD, PhD, FACS, Fa-Zu Qiu, MD, PhD, Zai-De Wu, MD, PhD, Zhi-Wei Zhang, MD, PhD, Zhi-Yong Huang, MD, PhD, Yi-Fa Chen, MD, PhD, Bi-Xiang Zhang, MD, PhD, Song-Qing He, MD, PhD and Wan-Guang Zhang, MD, PhD

Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, 430030 Wuhan, People’s Republic of China

Correspondence: Address correspondence and reprint requests to: Xiao-Ping Chen, MD, PhD, FACS; E-mail: chenxp{at}medmail.com.cn.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The role of surgical resection and thrombectomy for hepatocellular carcinoma (HCC) with portal vein tumor thrombus (PVTT) is controversial. This study aimed to evaluate the effects of the location and extent of PVTT on the long-term outcomes of surgical treatment for HCC.

Methods: A total of 438 patients with HCC and PVTT underwent liver resection with or without thrombectomy. These 438 patients were divided into 2 groups: in group A, PVTT was located in the hepatic resection area or protruded into the first branch of the main portal vein beyond the resection line for <1 cm (286 patients), and in group B, PVTT extended into the main portal vein (152 patients). Concomitant thrombectomy was performed in 147 patients (51.4%) of group A and in all patients of group B.

Results: PVTT recurrence within 6 months after surgery in group B was significantly higher than that in group A: 76.9% vs. 11.3%. Remnant liver recurrence within 1 year after surgery was 45.0% in group A and 78.8% in group B. The cumulative 1-, 2-, 3-, and 5-year overall survival rates were 58.7%, 39.9%, 22.7%, and 18.1% for group A and 39.5%, 20.4%, 5.7%, and 0% for group B, respectively. The overall survivals were significantly better in group A than group B (P <.02).

Conclusions: Liver resection with thrombectomy yielded better outcomes in the HCC patients with PVTT confined to the first or second branch of the main portal vein compared with PVTT extending into the main portal vein.

Key Words: Hepatocellular carcinoma • Portal vein tumor thrombus • Liver resection • Survival • Thrombectomy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Hepatocellular carcinoma (HCC) is one of the most common malignant diseases in mainland China, with an annual incidence of 24 per 100,000 population. During the past decade, it has become the leading cause of cancer-related deaths among men in rural areas and second in cities.1–3 Recent technological advances in imaging modalities and therapeutic procedures have facilitated early diagnosis and curative treatment in patients with HCC. Despite this marked progress in medical science, the prognosis of advanced HCC remains poor, particularly in patients with tumor thrombus in the major branches of the main portal vein.4–9 The management of HCC with portal vein tumor thrombus (PVTT) is complicated and controversial.10 Liver transplantation has proven to be an effective treatment for both incidentally discovered and known small HCC in patients with cirrhosis.11 However, the results of transplantation for HCC with PVTT are disappointing because of the high rates of tumor recurrence.12–14 Many investigators state that transcatheter arterial chemoembolization (TACE) is contraindicated in HCC with tumor thrombus in the main portal vein without cavernous transformation, because of the potential risk of liver failure attributable to ischemia after these procedures.15,16 However, some investigators have reported the safety and efficacy of TACE for HCC with PVTT. The 5-year survival rate for these patients was only 0% to 6.1%.17 Furthermore, most histological examinations performed after hepatectomy have indicated that TACE has a poor anticancer effect on PVTT. Accordingly, concomitant partial liver resection and thrombectomy may be regarded as a reasonable treatment for HCC with PVTT. Unfortunately, the potential benefits of liver resection and thrombectomy for patients with HCC and PVTT have not been fully delineated. In this retrospective study, we analyzed our experience with surgical treatment for HCC with PVTT and evaluated the effects of the location and extent of PVTT on the long-term outcomes.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From January 1990 to December 2003, hepatic resection for 4875 patients with HCC was performed in the Hepatic Surgery Center, Tongji Hospital, Huazhong Science and Technology University, China. Among these patients, 438 patients (8.9%) had PVTT in the main portal vein (its first or second branches) but without distant or extrahepatic metastases. A preoperative diagnosis was verified by abdominal ultrasonography (US), computed tomography, magnetic resonance imaging, or angiography. Color Doppler US was performed to determine the size and location of PVTT and the impairment in portal flow. Endoscopic examination was performed to check for possible complications of esophageal and cardiac varices. For patients with severe varices of the esophagus, sclerotherapy was performed before surgery to prevent perioperative bleeding.

Liver functional reserve was assessed in all patients by serum biochemical data, including total protein, albumin, total bilirubin (TB), cholesterol, and prothrombin time (PT). Our criteria for hepatectomy were that ascites was absent or was controllable with diuretics and the serum TB level was <20.5 µmol/L. The amount of liver resection was decided on the basis of TB, albumin, cholesterol, and PT. Patients with a TB level of 12 to 20.5 µmol/L, albumin ≤3.5 g/ L, cholesterol ≤3.6 mmol/L, and PT 3 to 4 seconds more than the control were selected only for minor resection. In patients with a TB level of ≤12 µmol/L, albumin > 3.5 g/L, cholesterol > 3.6 mmol/L, and PT < 3 seconds more than the control, major liver resection was considered feasible. Hepatic resection was defined as major if three or more Couinaud segments were resected (as recommended by the International Hepato-Pancreato-Biliary Association) and minor if fewer than three segments were resected.15 This study was approved by the Clinical Research Review Board of Tongji Hospital. A total of 438 patients with HCC and gross PVTT underwent hepatic resection according to these selection criteria. Liver parenchymal transections were performed with the conventional forceps fracture method in 311 patients and with an ultrasonic dissector or ERBE VIO (ERBE Elektromedizin GmbH, Tübingen, Germany) in 127 patients. At the operation, intraoperative US was performed to determine the size and location and the relationship between the tumor and the vascular system, as well as to define the plane of liver parenchymal transection.

According to the location and extent of PVTT, 438 patients were divided into 2 groups. In group A, PVTT was located in the hepatic resection area or protruded into the first branch of the main portal vein beyond the resection line for< 1 cm (286 cases; Fig. 1Go). In group B, PVTT extended into the main portal vein (152 cases; Fig. 2Go). Thrombectomy was performed with temporary occlusion of the portal veins before removal of the tumor thrombus from the vessels. A total of 286 patients in group A underwent anatomical resection with Pringle’s maneuver. The PVTT was located in the resection area in 185 patients. The PVTT protruded into the first branch of the portal vein beyond the resection line for<1 cm in 101 patients, and the thrombus was pulled out from the stump of the portal vein in these patients. In all patients in group B, the PVTT extended into the main portal vein. The main bile duct, hepatic artery, and main portal vein were individually taped. The portal vein to the contralateral lobe was also dissected and taped. The vascular tape for the main portal vein was applied as distally as possible. The right portal vein, the left portal vein, and the main portal vein were exposed. The portal vein was incised at the bifurcation of the right and left portal veins, and the PVTT was extracted from the incision in the portal vein. With this procedure, we were able to examine under direct vision the exact extent of the portal vein thrombus and identified whether the tumor thrombus was adherent to the venous wall or was freely floating in the venous lumen. When the procedure was performed in this manner, squeezing or fragmenting the tumor thrombus could be avoided, although it occurred easily if clamps were applied bluntly to the branches of the portal vein. Also, spreading of tumor cells in the portal vein to the remnant liver during surgical manipulation could be prevented. After confirming that no PVTT remained, the stump and/ or incision in the portal vein was sutured continuously. The PVTT was confirmed by histopathologic examination of the resected specimens.


Figure 1
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  		FIG. 1. In group A, the PVTT either was located in the hepatic resection area (A) or protruded into the first branch of the main portal vein beyond the resection line for <1 cm (B). PV, portal vein; PVTT, portal vein tumor thrombus.

 

Figure 2
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  		FIG. 2. In group B, the PVTT extended into the main portal vein. PV, portal vein; PVTT, portal vein tumor thrombus.

 
Operative mortality was defined as death within 30 days after the operation. Follow-up after surgery included serum alfa fetoprotein (AFP) and US every 4 to 6 weeks and chest radiography every 1 to 2 months during the first postoperative year and at 3- to 4-month intervals thereafter. Computed tomography, magnetic resonance imaging, or hepatic angiography was performed when intrahepatic recurrence was suspected.

A microcomputer was used for the storage and statistical analysis of the clinical data. Survival rates, excluding 30-day mortality, were calculated by using the Kaplan-Meier method. A Cox proportional hazards model was used for multivariate analyses of prognostic factors. Statistical differences were tested by the log-rank method.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The clinical, surgical, and postoperative data for the two groups of patients are listed in Tables 1Go and 2Go. Although complete data were not available for every patient, all available data were analyzed. There was no significant difference in age, male:female ratio, hepatitis B surface antigen positivity, or hepatic function reserve between the two groups. In group B, there were more patients with large tumors, multiple tumors, and hepatic vein invasion, but there was no significant difference when compared with group A. There were significantly more patients with ascites and esophageal varices in group B than in group A. The AFP level in group B was also significantly higher than in group A. There were no significant differences in the proportion of the major/minor hepatic resections. The total operative time and the total occlusion time of hepatic inflow in group A were significantly shorter than in group B. Patients in group B had more intraoperative blood loss (P =.0015) when compared with group A. The blood transfusion rate in group B (77.6%) was significantly higher (P =.0001) than in group A (19.5%). The incidences of postoperative complications (21.0%) and operative mortality (2.6%) in group B were higher than in group A (15.5% and 0%, respectively), but without a significant difference. PVTT recurrence within 6 months after surgery in group B was significantly higher than in group A (76.9% vs. 11.3%).


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  		TABLE 1. Clinical features of groups A and B
 

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  		TABLE 2. Surgical and postoperative data in groups A and B
 
The remnant liver was the most common site of tumor recurrence. Remnant liver recurrence within 1 year after surgery was 45.0% in group A and 78.8% in group B. The total percentages of patients with metastases to the lung, bone, lymph node, brain, and suprarenal glands in the two groups were 21.5% vs. 57.1%, 14.3% vs. 28.6%, 11.5% vs. 22.9%, 1.1% vs. 8.4%, and.5% vs. 0%, respectively. Treatment of HCC recurrence was based on the site and pattern of recurrence and the residual liver function. In our study, TACE was most often used for recurrent HCC in group A (59.5%), followed by radiofrequency ablation (RFA; 35.4%), percutaneous ethanol injection therapy (PEIT; 27.1%), and hepatic arterial infusion (HAI) (8.8%). In group B, PEIT was most often used for recurrent HCC (44.7%), followed by TACE (37.3%), RFA (23.3%), and HAI chemotherapy (10.1%). No patient with remnant liver recurrence was treated by systemic chemotherapy. There was no patient without treatment for recurrent HCC.

The median overall survivals in groups A and B were 18.8 and 10.1 months at a median follow-up of 22.5 and 13.7 months, respectively. The overall survival was significantly better in group A than in group B (Fig. 3Go; P <.02). The cumulative 1-, 2-, 3-, and 5-year overall survival rates were 58.7%, 39.9%, 22.7%, and 18.1% for group A and 39.5%, 20.4%, 5.7%, and 0% for group B, respectively.


Figure 3
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  		FIG. 3. Survival curves showing the overall survival rates of group A and group B. There was a significant difference between the two curves (log-rank test; P <.0164).

 
The relative risk of overall survival using the Cox proportional hazards model is shown in Table 3Go. On univariate analyses, the prognostic factors that had a significant effect on long-term survival were tumor >5 cm, multiple tumors, tumor thrombus adherent to the venous wall, the main portal vein occluded completely by PVTT, an AFP level of >3000 ng/mL, and intra-operative blood loss of >1000 mL (Table 3Go). When PVTT did not extend into the main portal vein, there was no significant difference in the relative risk regardless of where the PVTT was. When PVTT extended into the main portal vein, the relative risk increased to 5.4 (P <.0001). On multivariate analyses, multiple tumors, a main portal vein completely occluded by PVTT, and tumor thrombus adherent to the venous wall were significant prognostic factors for a favorable prognosis (P<.0001).


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  		TABLE 3. Relative risk of overall survival using Cox’s proportional hazards model
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
HCC has a high predilection for portal vein invasion, which is reportedly observed in 64.7% of patients at autopsy.18 PVTT is a poor prognostic factor because it can lead not only to the wide dissemination of tumors throughout the liver, but also to a marked deterioration of hepatic function. The median survival of untreated patients with HCC and PVTT was reported to be 2.7 months, whereas survival in those without PVTT was 24.4 months.19 A universally acceptable therapy for HCC with PVTT is still lacking. In view of the limitations of nonoperative treatments, several investigators have advocated an aggressive surgical approach for HCC with PVTT. In surgically resected series, the 3-year survival rate was reported to be 0% to 43% if patients with all degrees of PVTT were included.20–23 However, for patients with PVTT in the main portal vein and its first or second branch, the 3- and 5-year survival rates were reported to be 15% to 28% and 0% to 10%, respectively.24,25 As discussed26, Fujii et al. reported that the 1- and 2-year survival rates in patients with tumor thrombus in the main portal vein and in the right, left, and both portal veins were 20.9% and 6.2%, respectively. In our series, the 1-, 2-, 3-, and 5-year survival rates in all patients with PVTT were 52.1%, 33.1%, 16.0%, and 11.8%, respectively. If only patients with PVTT in the first or second branch of the main portal vein were considered, the 1-, 2-, 3-, and 5-year overall survival rates were 58.7%, 39.9%, 22.7%, and 18.1%, respectively.

It is worth pointing out that we adopted an aggressive treatment for tumor recurrence after surgery. The incidence of tumor recurrence in patients with HCC and PVTT was high. The PVTT recurrence rates within 6 months in groups A and B were 7.6% and 63.8%, respectively. Remnant liver recurrence within 1 year after surgery was 45.0% in group A and 78.8% in group B. Repeat hepatic resection has been shown to prolong survival in patients who develop recurrent HCC relative to patients who do not undergo repeat resection.14,27 However, repeat hepatic resection could not be used in our patients because of advanced disease and low functional reserve of the liver. Instead, we used TACE, PEIT, RFA, and HAI for recurrent HCC.

For most surgeons, a patient is selected for liver resection only when tumor thrombus is located in the second or the first branch of the main portal vein. In such cases, the cancer can be completely removed by liver resection with resection of the ipsilateral portal vein branch containing the tumor thrombus. When tumor thrombus of HCC extends to the main portal vein, surgical resection is usually considered not indicated. Unlike in other studies, we included patients for concomitant liver resection and thrombectomy even when the main portal vein was totally occluded by tumor thrombus. This procedure not only decompresses portal hypertension, but has also been shown to prolong the survival of patients with advanced HCC.28–31 In our study, the 1-, 2-, and 3-year overall survival rates of patients with tumor thrombus in the main portal vein were 39.5%, 20.4%, and 5.7%, respectively.

Using univariate analysis, we identified several prognostic factors, including single tumors, tumor size <5 cm, AFP level <3000 ng/mL, intraoperative blood loss <1000 mL, and PVTT without extension into the main portal vein, that were associated with a better survival for patients with HCC and PVTT after liver resection and thrombectomy. However, when the PVTT extended into the main portal vein, the relative risk increased to 5.4 (P <.0001). On multivariate analysis, the number of primary nodules, total occlusion of the main portal vein by PVTT, and tumor thrombus adherent to the venous wall were significant prognostic factors (P <.0001).

In conclusion, hepatic resection with portal vein thrombectomy yielded satisfactory results in patients with PVTT in the first or second branch of the main portal vein. The benefit of surgery is less clear when the PVTT extends into the main portal vein.


   ACKNOWLEDGMENTS
 
The authors thank Professor W. Y. Lau, Department of Surgery, Chinese University of Hong Kong, for reading the manuscript and providing valuable advice. Supported by grant 321 (2001) from the Chinese Ministry of Public Health for the Key Clinical Projects.

Received for publication August 3, 2005. Accepted for publication December 15, 2005.


   REFERENCES
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 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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