|Year : 2022 | Volume
| Issue : 2 | Page : 345-351
Efficacy and safety of transcatheter arterial chemoembolization plus hepatic arterial infusion chemotherapy in the treatment of advanced hepatocellular carcinoma with portal vein tumor thrombosis in the main trunk
Zhiqiang Wu1, Jian Gao2, Wenquan Zhuang1, Jianyong Yang1, Wenbo Guo1
1 Department of Interventional Radiology, The First Affiliated Hospital of Sun Yat-Sen University, Guangzhou, Guangdong Province, China
2 Department of Interventional Radiology, Baoan District People's Hospital of Shenzhen; Shenzhen, Guangdong Province, China
|Date of Submission||06-Jul-2021|
|Date of Acceptance||01-Feb-2022|
|Date of Web Publication||20-May-2022|
Department of Interventional Radiology, The First Affiliated Hospital of Sun Yat-Sen University, No. 58 Zhongshan 2 Road, Guangzhou 510080
Source of Support: None, Conflict of Interest: None
Background: Hepatocellular carcinoma (HCC) is the most common primary liver cancer and the sixth most prevalent malignancy worldwide. The incidence of portal vein tumor thrombosis (PVTT) is recorded as high as 10%–60% in HCC patients. The purpose of this study was to assess the efficacy and safety of transcatheter arterial chemoembolization (TACE) plus hepatic arterial infusion chemotherapy (HAIC) in advanced HCC patients complicated with PVTT in the main trunk.
Patients and Methods: A total of 33 HCC patients were treated with TACE + HAIC or TACE, respectively. The primary endpoint was overall survival (OS), while the secondary endpoints included progression-free survival, objective response rate (ORR), and disease control rate (DCR) of HCC lesions and PVTT in the trunk. Adverse events and main complications were also investigated. A COX model was used to identify the risk factors associated with OS.
Results: There were 16 patients receiving TACE + HAIC and 17 receiving TACE. The median OS was longer in the TACE + HAIC group than the TACE group (P < 0.05). There were no significant differences in the ORR and DCR of HCC lesions and PVTT response between the two groups (P > 0.05). Alpha-fetoprotein was <400 ng/ml. Multivariate analysis showed that cavernous transformation of portal vein was associated with longer OS. In terms of complications, the addition of HAIC showed more myelosuppression than the TACE alone group (P < 0.05).
Conclusion: Compared with TACE alone, HAIC + TACE may be more safe and provide more benefits for HCC patients complicated with PVTT in the trunk.
Keywords: Hepatic arterial infusion chemotherapy, hepatocellular carcinoma, portal vein tumor thrombosis, survival, transcatheter arterial chemoembolization
|How to cite this article:|
Wu Z, Gao J, Zhuang W, Yang J, Guo W. Efficacy and safety of transcatheter arterial chemoembolization plus hepatic arterial infusion chemotherapy in the treatment of advanced hepatocellular carcinoma with portal vein tumor thrombosis in the main trunk. J Can Res Ther 2022;18:345-51
|How to cite this URL:|
Wu Z, Gao J, Zhuang W, Yang J, Guo W. Efficacy and safety of transcatheter arterial chemoembolization plus hepatic arterial infusion chemotherapy in the treatment of advanced hepatocellular carcinoma with portal vein tumor thrombosis in the main trunk. J Can Res Ther [serial online] 2022 [cited 2022 Jul 4];18:345-51. Available from: https://www.cancerjournal.net/text.asp?2022/18/2/345/345521
| > Introduction|| |
Hepatocellular carcinoma (HCC) is the most common primary liver cancer and the sixth most prevalent malignancy worldwide. The incidence of portal vein tumor thrombosis (PVTT) is recorded as high as 10%–60% in the HCC patients.,,, The complications of PVTT usually lead to poor prognosis, with the median overall survival (OS) of 2–4 months owing to high rates of metastasis and relapse.,,
There are few treatment options for PVTT, and it is controversial due to limited therapeutic efficacy at present. According to the most widely accepted Barcelona Clinic Liver Cancer (BCLC) guidelines for HCC management, HCC with PVTT is classified as advanced stage, and sorafenib is the only recommended therapeutic option. However, the OS of patients receiving sorafenib is 10 months only, which is just nearly 3 months longer than those receiving placebos. Particularly, it has been reported that for patients with HCC III/IV PVTT receiving sorafenib monotherapy, the OS is only 3.1 months. It is not satisfactory, suggesting that better treatment strategies are required.
Although there is little low-level evidence of other therapeutic alternations, including surgery, transcatheter arterial chemoembolization (TACE), external radiotherapy, selective internal radiation therapy systematic chemotherapy, and portal vein stenting implantation, as promising approaches for PVTT in terms of improving OS.,, Among all types of PVTT, HCC patients with tumor invading the main portal vein are identified to have extremely poor prognosis, with median survival of 1.9–7.4 months.,,, In those patients, surgery or TACE monotherapy is not adopted as they are considered as regional treatment on liver lesions. Therefore, the combination of systematic therapy with PVTT is usually accepted in clinical practice. However, the refractoriness of HCC with PVTT in the main trunk still remains an enormous challenge for clinicians.
Recently, researches on hepatic arterial infusion chemotherapy (HAIC) plus FOLFOX (oxaliplatin plus fluorouracil/leucovorin) regimen to treat unresectable HCC have shown favorable outcomes,,, especially in patients with BCLC stage C and median OS of 14.5 months. It also has been reported that manifested HAIC could achieve better efficacy than sorafenib for PVTT patients., However, few studies have concentrated on HCC with PVTT in the main trunk, despite the fact that patients with BCLC stage C or PVTT are heterogeneous population.
In the clinical practice and Chinese guideline for HCC, TACE is still the most commonly used treatment for unresectable HCC patients, including those complicated with PVTT or not. The most possible reason is that the majority of Chinese HCC patients cannot afford expensive molecular target drugs such as sorafenib and lenvatinib. In this study, we retrospectively analyzed the clinical data of HCC patients with PVTT in the main trunk receiving TACE + HAIC or TACE.
| > Patients and Methods|| |
Classification of portal vein tumor thrombosis
Currently, there are two classifications of PVTT, including the Japanese Vp classification and the Cheng's classification proposed by Cheng Shuqun, a Chinese Professor. The Japanese classification was listed as follows:, Vp0, no PVTT; Vp1, PVTT distal to but not in second-order branches of the portal vein; Vp2, PVTT in second-order branches of portal vein; Vp3, PVTT in first-order branches of portal vein; and Vp4, PVTT in the main trunk of portal vein or a contralateral portal vein branch or both. The Chinese Cheng's classification was as follows:, Type I0, only under microscopy; type I, segmental or sectoral branches of portal vein or above; type II, right/left portal vein; type III, main portal vein; and type IV, superior mesenteric vein. The target type of PVTT analyzed in our study was Vp4 of Japanese Vp classification and type III in Cheng's classification. In other words, the patients with PVTT in main trunk of portal vein were included in our study.
We retrospectively reviewed the medical records of 95 patients who received >1 cycle of TACE + HAIC or TACE alone in the First Affiliated Hospital of Sun Yat-sen University between January 2015 and January 2018. The study flowchart was shown in [Figure 1].
|Figure 1: Screening and filtration of HCC + PVTT. Abbreviation: HCC: Hepatocellular carcinoma; PVTT: Portal vein tumor thrombosis; TACE: Transcatheter arterial chemoembolization; HAIC: Hepatic arterial infusion chemotherapy; ECOG-PS: Eastern Cooperative Oncology Group performance status|
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(1) patients aged 20-70 years; (2) patients diagnosed as HCC based on the American Association for the Study of Liver Diseases guidelines; (3) patients diagnosed as PVTT complications according to the enhancement of contrast in the arterial phase and washout in the portal venous phase images of CT;, (4) patients with tolerable liver function (Child-Pugh score 5-6) at admission; (5) treatment naïve;(6) patients who refused to receive sorafenib treatment due to financial problems or other causes.
(1) patients whose baseline data was not complete; (2) patients with Eastern Cooperative Oncology Group-performance status (ECOG-PS) >2; (3) patients with unmeasurable lesions, such as diffusive ones, according to the modified Response Evaluation Criteria in Solid Tumors (RECIST version 1.1) criteria;, (4) patients with Vp0-Vp3 in Japanese Vp classification, type I0-II or IV in Cheng's classification, hepatic vein tumor thrombosis, inferior vena cava tumor thrombosis, or atrium tumor thrombosis; (5) patients who received substandard treatments plus sorafenib, ablation, etc.; (6) patients with significant complications in the cardiopulmonary or nervous systems.
TACE and hepatic arterial infusion chemotherapy procedure
A 5-F catheter was inserted into femoral artery through Seldinger technique after routine preoperative preparation. Arteriography of the celiac trunk, hepatic artery or superior mesenteric artery was performed to visualize the arterial vascularization of the tumor and evaluate the portal vein patency, respectively. The tip of the catheter or microcatheter (if necessary) was super-selected into the tumor-feeding branches with the guidance of a guidewire under the fluoroscopy. Then, 10–50 mg epirubicin was administrated into the target tumor-feeding vessels, and embolization was implemented by microscope (BioSphere Medical S. A., Roissy en France-FR), gelatin sponge (JinLing pharmaceutical; Jiangsu, China) or polyvinyl alcohol particles (Eric Kang pharmaceutical; Zhejiang, China). The embolization endpoint of the target vessel was subjective angiographic chemoembolization endpoint (SACE) level III according to SACE scale., Once the embolization endpoint was reached, the arterial catheter was removed for TACE-alone group, but it was indwelled for TACE + HAIC group. Modified FOLFOX4 regiment was administrated in TACE + HAIC group and detailed information is shown in [Figure 2]. Treatment was repeated every 3–5 weeks and continued until the occurrence of untreatable progression or intolerant treatment-related toxicity.
|Figure 2: Modified FOLFOX4 regimen administrated through superselected hepatic artery|
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The primary endpoint in this study was OS. Other evaluation indexes were also analyzed, such as progression-free survival (PFS), objective response rate (ORR), and disease control rate (DCR) of liver target lesions. The measurement of target lesions was based on modified Response Evaluation Criteria in Solid Tumors criteria., PVTT responses were assessed by the criteria proposed by Changfu Liu, et al.: complete response, complete disappearance of the PVTT; partial response, decrease more than 50% in the thrombus diameter; stable disease, decrease <50% or increase more than 25% in the thrombus diameter; progressive disease, increase more than 25% in the thrombus diameter. ORR and DCR were evaluated at the 3rd month after treatment. Safety was assessed by monitoring the adverse events (AE) and complications.
Statistical analyses were processed by SPSS 20.0 software (IBM Co, Armonk, NY). Continuous variables were expressed as means ± standard deviations and compared by independent sample t-test. Categorical variables were analyzed through Chi-square test or Fisher's exact test when appropriate. Kaplan–Meier survival curves were adopted to compare OS and PFS between the two groups. A COX proportional hazards regression model was applied to analyze the underlying prognostic factors for OS. P < 0.05 was considered statistically significant.
| > Results|| |
Baseline characteristics in the TACE + HAIC and TACE groups were listed in [Table 1]. All patients in the two groups were all male, and most of them were infected with hepatitis B virus (87.5% vs. 94.1%), Child-Turcotte-Pugh score 5 (75% vs. 8.2%), multiple tumors of >3 (81.3% vs. 88.2%), and massive HCC lesions (12.09 ± 5.35 vs. 11.67 ± 5.17 cm). Patients with serum alpha-fetoprotein positive (>400 ng/ml) accounted for nearly a half population in both groups. All characteristics between the two groups showed no statistical difference (P > 0.05).
Effects of transcatheter arterial chemoembolization + hepatic arterial infusion chemotherapy versus transcatheter arterial chemoembolization alone
Kaplan–Meier curves depicted in [Figure 3] demonstrated that the median OS in the TACE + HAIC group (10.0 months) was significantly longer than TACE alone (4.78 months) group (P < 0.05, hazard ratio [HR]: 2.436 [1.000, 5.933]). PFS of intrahepatic HCC lesions showed the similar outcome (6.0 months vs. 3.0 months, P < 0.05). ORR and DCR of HCC lesions in the two groups were 37.5% and 62.5% vs. 17.6% and 58.8% (P > 0.05). ORR and DCR of PVTT response in the two groups were 31.3% and 81.3% vs. 11.8% and 64.7% [P > 0.05, [Table 2]]. Univariable and multivariable analysis by a COX model in [Table 3] indicated that the alpha-fetoprotein (AFP) levels (HR = 2.572, 95% confidence interval [CI] [1.036, 6.382]) and cavernous transformation of portal vein (CTPV) (HR = 0.292, 95% CI [0.117, 0.730]) were the two independent factors that affected OS. Patients with AFP <400 ng/ml and CTPV may survive longer during follow-up.
|Figure 3: Kaplan–Meier curves of OS and PFS time in TACE + HAIC and TACE groups. Abbreviation: SD: OS: Overall survival; PFS: Progression-free survival; TACE: Transcatheter arterial chemoembolization; HAIC: Hepatic arterial infusion chemotherapy. HR: Hazard ratio|
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|Table 3: Uni- and multivariate analysis of potential prognostic factors of survival time.|
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No treatment-related mortality occurred in the two groups. The most common treatment-related AEs were fatigue, abdominal pain, fever, emesis, anorexia, ALT or AST elevation, and bilirubin elevation in the two groups [Table 4]. Differently, TACE + HAIC showed more myelosuppression than TACE alone (P < 0.05), which needed additional remedies, such as myelostimulation. Corresponding symptomatic treatments were conducted to alleviate the above side effects. No cardiac toxicity was observed in the two treatment groups.
| > Discussion|| |
The refractory nature of HCC patients complicated with PVTT in the main trunk has always been the firmest challenge in the treatment performed by oncologists. The occurrence of PVTT in the main trunk could decrease the portal blood flowing into the liver parenchyma, and accordingly lead to liver function deterioration and portal hypertension. Hepatic failure and portal hypertension-related hemorrhage, especially variceal bleeding, are the direct causes of death in HCC patients. Therefore, the patency of portal vein becomes vital among HCC population. Our retrospective research focused on this particular cohort and confirmed the favorable effects of HAIC on PVTT patients with a median OS of 10 months, which is longer than reported data of 1.9–7.4 months.,,,
Compared with TACE alone, the addition of HAIC can improve the OS and PFS. However, no statistically improvement was observed on ORR and DCR of HCC lesions or PVTT at the 3rd month in spite of that improvement in percentage was observed. One of the potential causes might be the small sample size with potential biases. Another underlying cause was that the traits of our patients were multiple tumors with great tumor burden (over 10 cm in diameter). A 30% reduction in the diameter indicated more than 50% reduction in volume, which was extremely challenging to achieve for massive HCCs.
Regarding safety analysis, a completely embolized main portal vein with few collateral blood vessels is believed to be one of the contraindications for traditional TACE. However, TACE or HAIC related AEs occurring in this study were mild and well-tolerated. We attributed this to the precise selection and embolization of the tumor blood supply in TACE procedure, as well as to SACE level III embolization endpoint. By super-selective and mild embolization, liver function was maximally preserved. Previously studies have also reported that TACE or HAIC could be safely performed in HCC patients with PVTT,, which was consistent with our study.
One of the independent prognostic factors in our study was serum AFP level of >400 ng/ml (HR 2.575, 95% CI [1.036–6.382]). Consistent with previously reported studies,, our results indicated that high serum AFP level was closely related to poor prognosis, as high-serum AFP levels might be associated with poorer differentiation grade of HCC.
The other identified prognostic factor was the presence of CTPV (HR 0.292, 95% CI [0.117–0.730]), which played the protective role for PVTT patients. CTPV, also known as portal cavernoma, is a compensatory result of portal vein congestion that causes the formation of periportal or intrahepatic venous collaterals., These venous collaterals can be categorized as hepatopetal (portal-portal shunts) or hepatofugal (portal-systemic shunts). On the one hand, CTPV is related to portal hypertension, splenomegaly, ascites, and esophageal and gastric variceal bleeding. Therefore, it seems to be a disease with potential for insidious clinical sequelae. On the other hand, hepatopetal venous collaterals increase the perfusion of liver parenchyma, which may protect liver function and improve OS for patients with main PVTT. Nevertheless, the long-term consequences of portal cavernoma remain unclear. The outcomes of patients with CTPV in this study indicated that positive effect might play a dominant role when the main trunk of the portal vein was congested. We hoped further studies on this aspect would verify our results.
Several limitations of this study should be noted. First, the small sample size might inevitably contain information bias. Second, there are no uniform criteria for PVTT response assessment at present. The criteria we arbitrarily chose as a reference are those used by Changfu Liu et al., which are not well accepted and lack rigorous evidential support. For conducting further studies on PVTT, it is crucial that a consensus on the therapeutic response to PVTT is reached among HCC experts.
| > Conclusion|| |
For HCC patients complicated by PVTT in the main portal trunk with tolerable liver function, TACE + HAIC can be safely performed. Compared to TACE alone, the addition of HAIC may achieve better effects in aspect of prolonging OS. Therefore, the combination of TACE and HAIC may be a new potential beneficial palliative treatment for HCC patients with main PVTT.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4]