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Year : 2019  |  Volume : 15  |  Issue : 4  |  Page : 766-772

Percutaneous thermal ablation combined with simultaneous transarterial chemoembolization for hepatocellular carcinoma ≤5 cm

1 Department of Interventional Radiology, Zhongshan Hospital, Fudan University, Shanghai, China
2 Department of Interventional Radiology, Zhongshan Hospital, Fudan University; Shanghai Institute of Medical Imaging, Shanghai, China

Date of Web Publication14-Aug-2019

Correspondence Address:
Lingxiao Liu
180 Fenglin Road, Shanghai 200032
Yi Chen
180 Fenglin Road, Shanghai 200032
Zhiping Yan
180 Fenglin Road, Shanghai 200032
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jcrt.JCRT_250_19

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 > Abstract 

Background/Aim: Percutaneous thermal ablation combined with transarterial chemoembolization (TACE) becomes a treatment option for unresectable hepatocellular carcinoma (HCC). This study aims to investigate the safety and feasibility of percutaneous thermal ablation combined with simultaneous TACE for patients with HCC ≤ 5 cm.
Materials and Methods: From June 2010 to February 2017, a total of 280 patients with HCC ≤ 5 cm who underwent percutaneous thermal ablation combined with simultaneous TACE were included in our study. Their clinical data were collected and analyzed.
Results: Major complications occurred in five cases (1.8%). The complete necrosis rate was 91.9%. The median overall survival (OS) was 66.5 months (95% confidence interval [CI] = 57.7–75.2). The OS rates in 1-, 3-, 5-, and 7-year were 96.7%, 76.0%, 59.7%, and 31.1%, respectively. Tumor size (hazard ratio = 1.826; 95% CI = 1.131–2.947; P = 0.014) was considered as independent prognostic factors of long-term survival.
Conclusion: Percutaneous thermal ablation combined with simultaneous TACE is a safe and effective treatment for HCC ≤ 5 cm.

Keywords: Hepatocellular carcinoma, simultaneous combination therapy, survival, thermal ablation, transarterial chemoembolization

How to cite this article:
Wu M, Gao S, Song H, Zhang Z, Wang J, Liu R, Wang X, Cheng J, Luo J, Liu Q, Chen Y, Yan Z, Liu L. Percutaneous thermal ablation combined with simultaneous transarterial chemoembolization for hepatocellular carcinoma ≤5 cm. J Can Res Ther 2019;15:766-72

How to cite this URL:
Wu M, Gao S, Song H, Zhang Z, Wang J, Liu R, Wang X, Cheng J, Luo J, Liu Q, Chen Y, Yan Z, Liu L. Percutaneous thermal ablation combined with simultaneous transarterial chemoembolization for hepatocellular carcinoma ≤5 cm. J Can Res Ther [serial online] 2019 [cited 2023 Jan 27];15:766-72. Available from: https://www.cancerjournal.net/text.asp?2019/15/4/766/264283

Mengfei Wu and Shanshan Gao contributed equally to this work.

 > Introduction Top

Hepatocellular carcinoma (HCC) is a worldwide common digestive malignancy with extremely high morbidity and mortality, especially in China.[1] Currently, liver transplantation and surgical resection are commonly considered as curative treatments for HCC. However, only 20%–30% of patients can benefit from surgical performance because of advanced staging, poor liver function, and other complications.[2],[3] Transarterial chemoembolization (TACE) is recommended and widely performed as a palliative treatment for unresectable HCC, because of the nature of palliative treatment that TACE has a low rate of complete response (CR),[4] especially for complex blood supply or bulky tumors. When the tumor is not completely necrotic, meaning, there is active residual tumor, the active residual tumor may cause tumor recurrence and metastasis.[5] Although it is possible to control by TACE more than once, it can also do harm to the liver function.

The minimally invasive, reproducible, and high necrosis rate of percutaneous thermal ablation is a hallmark for patients who cannot or refuse to undergo surgical resection.[6] Percutaneous thermal ablation is considered to be one of the main treatments for HCC <5 cm.[7],[8] Earlier, when radiofrequency ablation (RFA) was applied in HCC, it was only used in tumors ≤3 cm because of its limited effective range. The expansion of the applicable diameter range was due to the improved design process of the radiofrequency needle and the application of microwave ablation (MWA). In addition, with thermal ablation monotherapy, high-risk locations such as perivascular, subcapsular, subdiaphragm, and paraventricular have a lower complete ablation rate than safe locations in the liver parenchyma and high-risk locations are associated with higher complications rate and local recurrence rate.[9],[10]

Combination therapy has become a trend for the current treatment of HCC, either that was sequential combination treatment or simultaneous combination treatment. Improved survival is reported in TACE combined with percutaneous thermal ablation, but most reports are about sequential combination therapy.[11],[12],[13] There are only a few studies on simultaneous combination therapy, most of which are studies on HCC >5 cm. Since 2010, our center has carried out percutaneous thermal ablation combined with TACE for HCC. We retrospectively assessed survival time, local tumor response, and complications of percutaneous thermal ablation combined with simultaneous TACE for HCC ≤5 cm.

 > Materials and Methods Top

Patient cohort

We retrospectively collected patients received percutaneous RFA/MWA ablation combined with simultaneous TACE treatment at our hospital from June 2010 to February 2017. In our center, percutaneous thermal ablation combined with simultaneous TACE is generally used in patients with ≤5-cm HCC due to the following conditions: (1) patients with Barcelona Clinic Liver Cancer (BCLC)-A stage have lesions at high-risk locations and (2) in patients with BCLC-B, preoperative imaging examination showed that the enhancement of arterial phase was not obvious. Preoperative judgment of TACE alone was not effective or patients who received TACE treatment, but the effect was not good. The final treatment plan is determined by multidisciplinary consultations (radiology, liver tumor surgery, interventional therapy, radiotherapy, and oncology). The imaging manifestations of low blood supply HCC were diverse, so the diagnosis of low blood supply HCC is perspectively performed by two radiologists with extensive abdominal diagnostic experience. All patients signed an informed consent before treatment.

HCC is diagnosed according to histopathology or American Association for the Study of Liver Diseases.[14] The inclusion criteria include: (1) patients with primary or recurrent HCC who were not surgical candidate or refuse surgical resection; (2) (radiological) ≤5 cm, ≤5 nodules; (3) Child-Pugh grade A/B; (4) platelet >50 × 109/L, prothrombin time ≤18 s; and (5) Eastern Cooperative Oncology Group perform status ≤2 scores. Patients who had vascular invasion or instant metastasis are excluded.

Patients with tumor >3 cm or located in perivascular give priority to MWA combined with simultaneous TACE treatment.

Clinical procedure

Abdomen contrast-enhanced computed tomography (CT) or magnetic resonance imaging (MRI) was done within 2 weeks before treatment. Visibility under ultrasound (US) is judged.

All procedures were performed in single-stage approach with conscious sedation and/or local anesthesia. A 5F-sheath was punctured into femoral artery using the Seldinger technique. 5F RH catheter (Terumo, Tokyo, Japan) is selected into the celiac artery for angiography (Ultravist 300 Bayer AG, Leverkusen, Germany) by digital subtraction angiography (DSA), and the superior mesenteric artery angiography was used to find the lateral branch blood supply. The angiographic images were collected in the arterial phase, the parenchymal phase, and the venous phase. When position, size, number, and blood supply artery were confirmed, 14G water-cooled MWA needle (Nanjing Vison-China Medical Devices R and D Center, China) or 17G RFA electrode needle (MedSphere Shanghai, China) was inserted into tumor through percutaneous puncture guided by US. To covering the entire tumor nodule and achieving a safe range of 0.5–1.0 cm, overlapping ablation is allowed. It was not required to meet the safety margin of 0.5–1.0 cm in tumors located in high-risk locations, and we premised the safety margin in order not to damage the surrounding organs. Needle track ablation is performed with 50 W to prevent bleeding and planting metastases. After which, microcatheter superselective catheterization was performed in target artery. The emulsion made with platinum-based chemotherapy (100–150 mg) (Jiangsu Hengrui Medicine, Lianyungang, China) + epirubicin (30–50 mg) (Farmorubicin; Pfizer, Wuxi, China) + lipiodol (5–10 ml) (Guerbet, Roissy, France) + Embosphere 500 μm or less (Merit Medical Systems, Inc., South Jordan, UT, USA) was injected. Under fluoroscopy, when the small branch of the portal vein around the tumor was observed, the injection was stopped. According to the angiography, gelatin sponge particles (350–510 μm; Ailikang Medicine Co Ltd, Hangzhou, People's Republic of China) were used for further embolization.


We collected ten factors (age, gender, primary or recurrence, tumor number, tumor size, Child–Pugh class, serum alpha-fetoprotein (AFP) level, BCLC stage, TACE before simultaneous therapy, and thermal ablation type) based on electronic medical records, patients were followed up by a full-time clinical researcher. All patients received abdominal contrast-enhanced CT/MRI and laboratory tests (blood routine, liver function, AFP) at 1-, 3-, 6-, 9-, and 12-month after treatment for the 1st year and every 3–6 months thereafter.

One month after treatment, patients received abdominal enhanced CT or MRI to evaluate local efficacy. The local efficacy can be divided into: (1) CR: abdominal-enhanced CT or MRI scan showed no enhancement in the arterial phase of the tumor [Figure 1] and (2) Incomplete response: abdominal-enhanced CT or MRI scan showed enhancement of local arterial phase in the original lesion, suggesting tumor residual. Three months after treatment, local tumor response was evaluated according to m-RECIST evaluation criteria.[15] Local tumor response was divided into CR, partial response (PR), stable disease (SD), or progressive disease (PD). When enhanced lesions were found, new treatment would be formulated according to the tumor and patient's physical condition.
Figure 1: A 49-year-old male with a history of chronic hepatitis B, receiving percutaneous MWA combined with simultaneous transarterial chemoembolization after a transarterial chemoembolization treatment with no obvious tumor necrosis. (A-C) Preoperative abdominal enhanced magnetic resonance imaging; (i-iii) Arterial angiography (i), after microwave ablation procedure (ii), after the end of the overall procedure (iii); (D-F) 1 month after treatment; (G-I) 2 years after treatment

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Complications were defined as adverse events that occurred within 1 month after treatment. According to Common Terminology Criteria for Adverse Events v5.0, complications of treatment were evaluated. Overall survival (OS) is defined as the time from first percutaneous thermal ablation combined with simultaneous TACE treatment to death or October 31, 2017.

Statistical analysis

All statistical results in this study were calculated with SPSS 24 (SPSS Inc., Chicago, IL, USA). Continuous variables were presented as mean ± standard deviation. Categorical variables were presented as a percentage. The survival curves were drafted using the Kaplan–Meier method, and the log-rank test and Cox proportional hazards model were used to analyze prognostic factors. P < 0.05 was considered statistically significant.

 > Results Top

Basic clinical characteristics of the patients

A total of 280 patients with HCC were enrolled in our study. Of all patients, 224 patients were male and 56 were female, aging from 25 to 85 (mean 62.8 ± 11.0). They received a total of 387 percutaneous thermal ablations combined with simultaneous TACE sessions, which means 1.38 sessions for each patient (from 1 to 5 sessions). According to the modified BCLC staging system recommended by the European Association for the Study of the Liver, 212 patients were BCLC-A and 68 patients were BCLC-B [Table 1].
Table 1: Baseline characteristics of patients

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Complete necrosis rate and local tumor response

After abdominal-enhanced CT/magnetic resonance (MR) follow-up for the 1st month after treatment, among 504 tumor nodules, 91.9% (463/504) was completely necrotic. The BCLC-A group was 96.4% (264/274) and the BCLC-B group was 86.5% (199/230) (P < 0.001).

After abdominal-enhanced CT/MR follow-up for the 3rd month after treatment, in the BCLC-A group, CR: 87.7% (186/212); PR: 10.4% (22/212); SD: 1.9% (4/212); and PD: 0% (0/212); and in BCLC-B group, CR: 51.5% (35/68); PR: 41.2% (28/68); SD: 4.4% (3/68); and PD: 2.9% (2/68).

The local recurrence rate was 10.4% (36/280) in the entire cohort, 9.4% (20/212) in the BCLC-A group and 23.5% (16/68) in the BCLC-B group.

Survival outcome

Until October 31, 2017, the median follow-up was 28.3 months (ranging from 9.4–89.7 months). At the end of follow-up, 72 patients were confirmed dead. The median OS was 66.5 months (95% confidence interval [CI] = 57.7–75.2). The OS rates in 1-, 3-, 5-, and 7-year were 96.7%, 76.0%, 59.7%, and 31.1%, respectively [Figure 2]. The 1-, 3-, 5-, and 7-year OS rates in patients with BCLC-A HCC were 98.1%, 79.0%, 63.9%, and 35.2% and 92.6%, 65.7%, 45.0%, and 20% in patients with BCLC-B HCC. The patients with BCLC-A HCC have a better OS than BCLC-B HCC (69.9 vs. 56.4 months, P = 0.002, log-rank test) [Figure 3].
Figure 2: The cumulative overall survival rate of 280 patients who underwent percutaneous thermal ablation combined with simultaneous transarterial chemoembolization

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Figure 3: Comparison of cumulative overall survival rates between the Barcelona clinic liver cancer-A hepatocellular carcinoma group and the Barcelona clinic liver cancer-B hepatocellular carcinoma group

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Prognostic factors

We subjected eight factors (age, gender, primary or recurrence, thermal ablation type, tumor number, tumor size, Child–Pugh class, and serum AFP level) into univariate analyses. Univariate analysis showed that serum AFP level, tumor size, and tumor number were significantly correlated with survival of the patients (P < 0.1). Further multivariable analysis showed that tumor size (hazard ratio = 1.826; 95% CI = 1.131–2.947; P = 0.014) was independent prognostic factors for OS [Table 2]. Patients with HCC ≤ 3 cm have a better OS than HCC between 3 and 5 cm (72.9 vs. 56.4 months, P = 0.003, log-rank test).
Table 2: Univariate analysis and multivariate analysis results

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No treatment-related deaths occurred. The most common minor complication was postembolization syndrome, including fever (n = 92, 32.9%) and mild-to-moderate pain (n = 45, 16.1%) and vomiting (n = 8, 2.9%). All of the above was cured after symptomatic treatment. Severe complications were found in five patients (intestinal perforation: 1; bleeding: 1; hepatic abscess: 2; and pseudoaneurysm: 1). No permanent treatment-related sequelae occurred.

 > Discussion Top

TACE is a beneficial treatment for patients with unresectable HCC, no matter when tumor in early, middle, or advanced stage.[1] However, TACE treatment has limited effect on large or multiple HCC. In the past decades, percutaneous thermal ablation is increasingly used in solid tumors. Although percutaneous thermal ablation is defined as a localized radical treatment, it is greatly affected by tumor size and has a reduced rate of complete ablation of tumors at high-risk locations.[7] The prognostic factor analysis in our study showed that tumor size was an independent factor about patient survival. This result is consistent with many studies.[12],[16] Nowadays, comprehensive treatment is the mainstream concept of managing cancer, and combination therapy is the embodiment of comprehensive treatment concept. At present, there are many studies on transcutaneous thermal ablation combined with TACE in the treatment of HCC.[17],[18] However, most of the current reports of combination therapy are sequential therapy. The studies of safety and effectiveness of percutaneous thermal ablation combined with simultaneous TACE is remaining rare. In this study, we reviewed the safety and effectiveness of percutaneous thermal ablation combined with simultaneous TACE for HCC ≤5 cm. We found that this method is safe and effective, and tumor size may be the factor influencing the survival of patients with HCC ≤5 cm underwent this simultaneous combination treatment. To our knowledge, our research is the first study to observe such a long time about thermal ablation combined with simultaneous TACE.

According to the BCLC strategy,[19] the recommended treatment is thermal ablation for early-stage HCC patients who are nonsurgical candidates or unwilling to undergo surgery. However, for tumors in high-risk locations with only thermal ablation, the complete ablation rate is reduced, and the incidence of complications is increased.[9] There is a report that the complete ablation rate of RFA for high-risk locations BCLC-A HCC is 94.1% (48/51), the local recurrence rate was 23.5%, and the OS rates at 1-, 3-, and 5-year were 92.6%, 64.5%, and 43%.[20] In our study, In the BCLC-A group, the complete necrosis rate was 96.4%, and the local recurrence rate was 8.5%. The 1-, 3-, 5-, and 7-year cumulative survival rates of the BCLC-A group were 98.1%, 79.0%, and 63.9%, respectively. The simultaneous combination therapy has improved long-term survival rate. Percutaneous thermal ablation combined with simultaneous TACE treatment using percutaneous thermal ablation and TACE treatment of target lesions complement each other. Especially for high-risk locations and lesions unclear under US, the effect of simultaneous therapy should be better than only percutaneous thermal ablation.

In recent years, combination therapy has been widely used in intermediate-stage HCC, and TACE combined with percutaneous thermal ablation being the most common. The OS rates at 1-, 3-, and 5-year of percutaneous thermal ablation combined with sequential TACE for intermediate stage HCC were 91%, 53%, and 27%.[21] We performed simultaneous combination treatment for BCLC-B HCC. The OS rates in 1-, 3-, 5-, and 7-year were 92.6%, 65.7%, 45.0%, and 20%. According to a retrospective study by Tanaka et al., 1-, 3-, and 5-year OS rates for patients with BCLC-B who were treated with percutaneous thermal ablation combined with sequential TACE were 91%, 53%, and 27%, respectively.[21] In general, percutaneous thermal ablation is performed after TACE in thermal ablation combined with sequential TACE. That is because hepatic artery embolization of TACE is effective in reducing heat loss due to “heat-sinking effect” in percutaneous thermal ablation. There is usually a 2 weeks interval between TACE and percutaneous thermal ablation.[22] During this period, hepatic arterial embolization due to TACE may cause the formation of collateral circulation, and arteries that have undergone embolization may also be recanalized, which may lead to recurrence or tumor progression.

Tu et al.[23] counted the incidence of major complications of 1120 HCC patients who underwent TACE. The study showed that the incidence of major complications of TACE for HCC was 2.1%. Ding et al.[24] found the incidence of major complications of RFA and MWA were 3.5% and 3.1%, and there was no statistical difference between RFA and MWA. Our study showed that the major complications rate of percutaneous thermal ablation combined with simultaneous TACE for HCC was 1.8%. Compared with TACE or percutaneous thermal ablation, this treatment did not increase the incidence of major complications. In addition, there are no treatment-related death patients.

Percutaneous thermal ablation combined with simultaneous or sequential TACE commonly have several advantages:First, chemotherapeutic drugs and embolic agents used in TACE can enhance necrosis of tumors after RFA/MWA and may also reduce frequency of treatment.[25],[26] Second, TACE combined with RFA or MWA can reduce the amount of chemotherapeutic drugs and embolic agents, and thus have an advantage in the protection of liver function.[27] Third, artery angiography of TACE can also show the extent of tumor necrosis after RFA/MWA. In sequential combination therapy, TACE and thermal ablation are separated by a 2 weeks interval. During this period, collateral circulation and recanalization may occur. Therefore, sequential combination is not a strict simultaneous combination therapy.

Furthermore, percutaneous thermal ablation combined with simultaneous TACE treatment had advantages over sequential treatment: first, immediate thermal ablation after TACE minimize heat loss caused by perfusion mediated tissue cooling and improved the efficacy of ablation, especially RFA. Another way, immediate TACE after thermal ablation was considered to increase tumor necrosis by exposing sublethal heat-damaging tumor tissues to high drug concentration.[28] Considering that lipiodol of TACE have an effect on US imaging, we took immediate TACE after thermal ablation. Second, it is well known that one of the serious intraoperative and postoperative complications of percutaneous thermal ablation was bleeding. The incidence of bleeding after thermal ablation requiring treatment is only 0.1%–0.9%, but it is dangerous if not detected in time.[29] In patients with HCC, the occurrence of arteriovenous fistula is also very common. Immediate TACE after thermal ablation can detect and treat the bleeding and arteriovenous fistula in time. Third, in the procedure of simultaneous treatment, combined with preoperative imaging (CT/MR), the operator can use intraoperative US and DSA to observe lesions, including lesion location, size, blood supply; satellite lesions; residual lesions; and occult lesions. Triple image visualization increases the detection of lesions and improves the efficacy. Studies have found that treating occult lesions gives patients survival benefits.[30] Finally, thermal ablation and TACE treatment can achieve double insurance control of the lesions.[31]

Of course, there are some shortcomings in this study. First of all, this study is a retrospective study. Compared with prospective study, the data collection is limited, and observation of patients is not timely enough. Second, in our center, patients with tumors in high-risk locations, unobservable US, or low blood supply received simultaneous therapy, so there is no data of percutaneous thermal ablation or TACE monotherapy compared with simultaneous therapy. Finally, in our study, the effects of combined RFA/MWA on the survival of patients were compared. The results showed no statistical difference in median survival between patients using RFA/MWA. Although the current studies reported that there was no significant difference in OS between RFA and MWA for patients with HCC.[32] Since the type of ablation is selected based on the size and location of lesions, the patient is heterogeneous in two groups. There is some bias of the conclusion. We believe that percutaneous thermal ablation combined with simultaneous TACE can be further studied, including comparative studies with TACE or MWA or RFA monotherapy.

 > Conclusion Top

Percutaneous thermal ablation combined with simultaneous TACE is a safe and effective treatment for HCC ≤5 cm. Future studies are needed to compare the efficacy between the simultaneous TACE and other treatments for HCC.

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Conflicts of interest

There are no conflicts of interest.

 > References Top

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  [Figure 1], [Figure 2], [Figure 3]

  [Table 1], [Table 2]

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