Journal of Cancer Research and Therapeutics

: 2016  |  Volume : 12  |  Issue : 7  |  Page : 143--147

Laparoscopic combined with percutaneous ablation for hepatocellular carcinoma under liver capsule: A single Chinese center experience of thirty patients

Zhe Tang, Yi Zhu, Kezhong Tang, Linping Dong, Bin Yang, Heqin Fang, Yulian Wu, Bo Zhang 
 Department of Surgery, Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, People's Republic of China

Correspondence Address:
Bo Zhang
Department of Surgery, Second Affiliated Hospital, School of Medicine, Zhejiang University, 88 Jiefang Road, Hangzhou, Zhejiang 310009
People's Republic of China


Aim of Study: For the tumor lesions close to capsule of the liver, traditional percutaneous radiofrequency ablation (PRFA) is limited due to high incidence of postoperative complications. The aim of the present study is to whether laparoscopic combined with PRFA (LCPR) could effectively ablate the tumor lesions close to capsule of the liver. Methods: A total of 119 patients with subcapsular hepatocellular carcinoma (HCC) were divided into two groups: PRFA group (89 patients) and LCPR group (30 patients). RFA was accomplished through cool-tip RFA system. For LCPR, PRFA was first carried out to destroy tumors deep inside the liver tissue. Then, laparoscopic RFA was performed under the guide of laparoscopic view and destroyed the superficial part of the tumor. Postoperative morbidity and technique effectiveness between two groups were evaluated. Results: In PRFA group, the rate of fever was 70.8% (63/89), and two patients had gallbladder damage. Five patients had ascites. Pain was found in 26 patients (29.2%). In LCPR group, the rate of fever was 22/30 (73.3%). Two patients had ascites and only two patients complained of pain. In PRFA group, 77.5% (69/89) of the tumors were totally ablated, and in LCPR, 93.3% (28/30) of the tumors were destroyed without any residuals. Conclusion: LCPR could significantly reduce the incidence of postoperative pain and the rate of regional tumor residuals compared to the PRFA, suggesting this method could potentially be useful for subcapsular HCC ablation treatment.

How to cite this article:
Tang Z, Zhu Y, Tang K, Dong L, Yang B, Fang H, Wu Y, Zhang B. Laparoscopic combined with percutaneous ablation for hepatocellular carcinoma under liver capsule: A single Chinese center experience of thirty patients.J Can Res Ther 2016;12:143-147

How to cite this URL:
Tang Z, Zhu Y, Tang K, Dong L, Yang B, Fang H, Wu Y, Zhang B. Laparoscopic combined with percutaneous ablation for hepatocellular carcinoma under liver capsule: A single Chinese center experience of thirty patients. J Can Res Ther [serial online] 2016 [cited 2022 Jul 3 ];12:143-147
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Hepatocellular carcinoma (HCC) is currently the fifth leading cause of cancer-related death in the US, accounting for approximately 23,000 deaths in 2014.[1] The main radical treatment methods rely on hepatic lobe resection or transplantation. However, surgical treatments are often not applicable due to the poor hepatic reserve in patients with cirrhosis and a shortage of donors. Radiofrequency ablation (RFA) was previously considered as palliative care. Recent clinical studies demonstrated that RFA has much lower rate of complications with comparable local tumor control effect in comparison to resection.[2],[3] Meanwhile, RFA had been identified as a curative way in the NCCN guideline in 2015 for HCC tumor <3 cm.[4]

Traditionally, RFA could be guided by ultrasound through the skin, which is also named as percutaneous RFA (PRFA). However, for superficial lesions adjacent to liver capsule, PRFA has its limitation because of the possibility of normal tissue damage, such as abdominal viscera or gallbladder.[5],[6],[7] Tumor lesions near the surface usually could not be ablated completely using PRFA. Laparoscopic RFA (LRFA) could effectively avoid the abdominal viscera or diaphragm injury by separating the ablation area from adjacent organs. However, it is generally difficult to accurately determine the range of deep-seated tumor and the relationship between tumor and vascular structures, which is visible only by laparoscopy. Therefore, laparoscopic ultrasound (Lap-US) is often used to improve the accuracy in detecting tumor.[8] However, operator with lots of experience is required to perform Lap-US-guided probe insertion because the procedure is very difficult. Percutaneous ultrasound is relatively easier than Lap-US. To assess the feasibility, we designed laparoscopic combined with PRFA (LCPR) to destroy the whole subcapsular tumors.

LCPR for ablating the subcapsular lesions has been applied in our institution since 2011. It has demonstrated that LCPR can offer a much safer approach to liver lesions located at a position that is difficult or even impossible to perform a percutaneous treatment. In this study, we collected the data from 119 patients with tumors localized near the capsule of liver between January 2013 and December 2015. The postoperative morbidity, mortality, and the incidence of tumor residues were analyzed. The aim of this study is to report our experiences with this technique for the treatment of HCC near the capsule.



In total, 119 patients between January 2013 and December 2015 diagnosed to have HCC were collected. The patients were included in this research according to the following standards: (1) the largest HCC nodule on preoperative imaging had to be smaller than 5 cm in diameter; (2) the number of HCC nodules was less or equal to be three; (3) localization of the HCC within 0.5 cm of the liver capsule. Complete medical history was obtained in each patient. The procedures for RFA were described in detail to all patients, and informed consent was obtained for all participating patients.

Technical notes

The procedure was performed under general anesthesia with a standard laparoscopic technique. Intraoperative laparoscopic nonenhanced US was performed to assess residual liver and to confirm the location of the tumor to be treated.

PRFA was first carried out to destroy tumors deep inside the liver tissue. Then, LRFA was performed under the guide of laparoscopic view and mainly destroyed the upper part of the tumor [Figure 1]. In case of tumor adjacent to abdominal viscera, PRFA was used to destroy the tumor part relatively far from the surrounding organ before LRFA [Figure 2]. Then, a laparoscopic retractor or surgical sponge was used to isolate tumor from viscera organ to avoid thermal injury, and Lap-US-guided RFA was performed under direct visualization [Figure 3]. In tumor lesions, in which no liver parenchyma was interposed between the lesion and the RFA needle, continuous aspiration was performed to avoid blood spreading.{Figure 1}{Figure 2}{Figure 3}

For tumors in the subcapsule of liver next to gallbladder, PRFA was first carried out to destroy deep part of the tumor which is relatively far away from gallbladder. After separating liver from gallbladder, LRFA was carried out to destroy the remaining tumor tissue.

RFA was accomplished through cool-tip RFA system (Radionics, Burlington, MA, USA). This electrode was placed into and in the periphery of the lesion under US guidance. Several insertions to treat overlapping zones were needed to complete the procedure and to maximize tumor ablation effect. The thermal ablation was performed at 100–200 W. The electrode was maintained for 12 min. Cool water was used to prevent burning of the neighboring organs. Tissue impedance was monitored throughout the procedure. The appearance and progression of hyperechogenicity were used to guide the therapy. After finishing the nodule ablation, the intrahepatic needle track was treated by thermocoagulation to avoid local seeding and any bleeding.

Treatment response evaluation

One month after RFA, all patients underwent a contrast-enhanced magnetic resonance imaging (MRI). After the imaging, the treatment response was classified as an initial complete response (absence of any enhancing areas within the treated nodule) or an initial incomplete response (presence of enhanced tissue in the tumor site, tumor residues). When the latter occurred, either a new LCPR or an ablative percutaneous treatment was performed depending on tumor size and location.

Statistical analysis

Data were analyzed by a Chi-square test. Statistical analysis was performed using IBM SPSS Statistics Version 20 software.


Data collection

We retrospectively analyzed a total of 119 HCC patients who underwent RFA during January 2013 to December 2015. These patients could be divided into two groups: (1) PRFA group and (2) LCPR group. The tumors of all these 119 patients localized near the capsule of the liver and we defined them by this standard: ≤0.5 cm between tumor edge and liver capsule.

As showed in [Table 1], PRFA group contains 89 patients (18 females and 71 males), and the average age was 59.5 years old. The tumors were adjacent to the gallbladder in 19 patients. The data of 30 patients (9 females and 21 males) belonged to the LCPR group was also been collected, and the average age was 62.9 years old. The tumors were adjacent to the gallbladder in three patients. The rates of hepatitis B virus infection were both more than 90% in these two groups.{Table 1}

Postoperative morbidity and technique effectiveness

As indicated in [Table 2], the mean postoperative hospital stay was 3.23 days in PRFA group and 3.41 days in LCPR group. Thirty-day mortality rates were 0% in two groups. The common complications after RFA included fever, adjacent organ damage, ascites, and pain. In PRFA group, the rate of fever was 70.8% (63/89), and two patients had gallbladder damage, which demonstrated symptoms of acute cholecystitis. Five patients had ascites in the abdomen detected by ultrasound because of the hepatic dysfunction. Pain was found in 26 patients (29.2%). In LCPR group, the rate of fever was 22/30 (73.3%), and one patient had intestinal leakage because of the adhesiolysis procedure. Two patients had ascites and only two patients complained of pain. We designed to evaluate the tumor residuals by MRI 1 month after RFA. We found in PRFA group, 77.5% (69/89) of the tumors were totally destroyed, and in LCPR, nearly 93.3% (28/30) of the tumors were destroyed without any residuals, showing this technique significantly decreased the rate of regional tumor residuals.{Table 2}


In recent years, RFA had been suggested to be the first-line therapy for HCC with the size smaller than 3 cm, and hepatic resection should be considered only in patients with failure or contraindications to RFA.[9],[10],[11] Traditional PRFA could not always be performed mainly because of difficulty or impossibility of transabdominal US visualization of the lesion. This was confirmed by a publication by Kim et al., who described a 25.3% rate of HCC undetectable by common percutaneous US.[12] RFA through percutaneous pathway could be hazardous; sometimes, due to high incidence of diaphragm injury and other surrounding organ's damage even when superficial tumor could be visualized by percutaneous US.[13],[14] LRFA could overcome such drawbacks by isolating tumor from other structures and performing ablation under direct monitoring. However, it is more difficult to avoid vascular injury during electrode insertion without any guidance and also difficult to confirm whether the deep part of the tumor is completely ablated. Laparoscopic US could be applied for probe insertion guidance and for monitoring/assessing ablation procedure. However, Lap-US-guided RFA is technologically difficult compared to percutaneous approach. Up to now, the usage of LRFA has been reported and evaluated in comparison to the PRFA.[15],[16],[17] However, few studies focused on the application of combination of laparoscopic and percutaneous methods for treatment of tumor near the capsule of liver.

In this study, we reported our experiences of LCPR in the last 2 years and compared the results with simple PRFAs. We found that LCPR did not prolong the time of hospitalization compared with the PRFA (P > 0.05). The adjacent organs' damage was rare in both groups. However, gallbladder damage was found in two patients in PRFA groups, whereas no gallbladder injury in LCPR group. During laparoscopic surgery, the operator could stretch the gallbladder away from tumor to avoid any heat injury. Similarly, when superficial tumor was very close to the gastrointestinal tract, such as duodenum and colon, LCPR was still safe and effective by isolating and protecting visceral organs. The intestinal leakage was found in one patient in LCPR group due to the adhesion in the abdomen rather than RFA procedure. This patient was finally recovered after percutaneous drainage. It is obvious that postoperative adhesion remains the major obstacle for surgeon to perform laparoscopic tumor ablation, which is sometimes nearly impossible under severe adhesive condition. In our LCPR group, 30% patients have previous abdominal operation, but none was converted to open procedure.

PRFA in tumor near the capsule may damage the abdominal viscera or skin and could cause pain after surgery. On the contrary, LCPR could produce pneumoperitoneum and elongate the distance between tumor and abdominal viscera, which could decrease the incidence of postoperative pain.

In addition, under laparoscopic condition, other tiny lesions could be detected accidently (not indicated in preoperative imaging studies) and ablated simultaneously. Accurate tumor stage (tumor recurrence, lymph nodes involvement, etc.) could be established. For experienced surgeon, laparoscopic liver resection combined with ablation is feasible and would be more effective for HCC radical treatment. Despite of these advantages, LRFA is not an easy procedure which needs very skilled operator to handle the laparoscopic US and to insert the probe into proper location of the tumor under the guidance. For tumors near important vascular structures, it is relatively more difficult to observe the relationship among probe, tumor, and surrounding vessels under lap-US guidance, leading to a higher rate of vascular injury compared with percutaneous approach. Therefore, we considered to combine LRFA and PRFA for superficial tumor treatment.

First, we ablated the deep structure of tumor with percutaneous US guidance, which can be easily conducted and can clearly show the structures' relationship. Then, we used LRFA to destroy the superficial lesions. Not only to separate lesions but also ablating tumor by multiple directions, which largely improved the tumor ablation rate. In the present study, the short-term follow-up data collected at 1 month after RFA showed that LCPR could improve the rate of complete ablation for tumor near the capsule of the liver. No patients died within 30 days after RFA, which indicated RFA was safe in these high-risk regions in our center.


LCPR in our center displays lots of advantages in postoperative morbidity and rate of regional tumor residuals on the HCC which localized at subcapsular compared to the single PRFA. However, the survival time of patients had not been analyzed because majority of short time. In the future, we will continue with data collection to figure out if LCPR will have effect on the recurrence rate of HCC.

Financial support and sponsorship

Supported by grants from the Natural Science Foundation of Zhejiang Province (No. LY15H160022 and LY16H070003), National Natural Science Foundation of China (No.81570698) and the Traditional Chinese Medicine Foundation of Zhejiang Province (No. 2015ZA056).

Conflicts of interest

There are no conflicts of interest.


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