Introduction: The effectiveness of transarterial chemoembolization (TACE) in treating hepatocellular carcinoma (HCC) has been well established. The differential impacts of drug-eluting bead TACE (DEB-TACE) as opposed to conventional TACE (cTACE) on vascular changes, such as arterial-portal venous shunts (APSs), have been recognized. However, their subsequent effects on treatment outcomes have not been fully explored. This study aims to identify risk factors associated with the occurrence of APS in HCC patients treated with DEB-TACE and to evaluate its impact on patient survival. Methods: A retrospective analysis was conducted from January 2012 to December 2018 including 74 HCC patients receiving DEB-TACE as initial treatment and a 1:1 cTACE. Kaplan-Meier analysis estimated overall survival (OS) and progression-free survival (PFS). Logistic regression identified significant risk factors for APS occurrence after DEB-TACE. Results: APS incidence was significantly higher after DEB-TACE than cTACE (46.0% vs. 16.2%, p < 0.001). There was no significant difference in median OS between APS and non-APS groups after DEB-TACE: 50 months (24.6–75.4) versus 26.9 months (19.5–43.2), p = 0.111; median PFS was 15.6 months (4.1–27.1) and 9.5 months (6.8–12.1) for the two groups, respectively, p = 0.065. Risk factors for APS occurrence after DEB-TACE were more than two feeding arteries (OR: 7.25, 95% CI: 1.82–28.95, p = 0.005) and non-selective embolization (OR: 8.02, 95% CI: 2.30–27.95, p = 0.001). Conclusion: APS occurrence was higher in DEB-TACE-treated HCC patients, but it did not significantly affect OS and PFS. More than two feeding arteries and non-selective embolization were significant risk factors for APS occurrence after DEB-TACE.

Hepatocellular carcinoma (HCC) ranks among the foremost causes of mortality in cancer patients worldwide [1]. Despite the increasing proportion of patients diagnosed at an early stage who are candidates for curative therapeutic approaches such as surgical resection or liver transplantation, a significant number of patients receive diagnoses at intermediate or advanced stages when complete tumor eradication is no longer possible. In recent years, alongside the remarkable surge in systemic therapeutic advancements, there has been a slight decline in the number of patients suitable for local treatment modalities. Nonetheless, transarterial chemoembolization (TACE) remains the primary and favored choice for this specific patient group in all currently available clinical guidelines [2‒4].

TACE has two basic techniques: conventional transarterial chemoembolization (cTACE) and drug-eluting bead transarterial chemoembolization (DEB-TACE). Multiple randomized controlled trials comparing DEB-TACE with cTACE have identified no statistically significant difference between the two groups regarding overall survival (OS) or tumor response [5, 6]. However, in the randomized controlled study by Ikeda, selective cTACE demonstrated a higher complete response rate in tumor control compared to selective DEB-TACE, with rates of 75.2% versus 27.6% respectively [7]. Post-treatment adverse events associated with the postembolization syndrome were more prevalent in the cTACE group; biliary injuries and hepatic artery or portal vein damages were more prevalent in the DEB-TACE group [8‒11, 12].

Shimosea et al. [13] observed that the incidence of the arterio-portal venous shunt (APS) after DEB-TACE was significantly higher than after cTACE (48.7% vs. 8.1%, p < 0.0001) and higher in patients with a Child-Pugh A score. This is a novel and intriguing finding when considering DEB-TACE options. The presence of an APS is often associated with a poor prognosis for patients with HCC due to the treatment process difficulties and the diminished efficacy of TACE [14]. Therefore, the higher prevalence of APS in patients treated with DEB-TACE compared to cTACE may be a determining factor in choosing the most effective treatment method for the patients. However, the actual impact of APS on patient survival has not been previously confirmed. The objective of the study is to investigate the risk factors for the occurrence of APS in HCC patients treated with DEB-TACE and their impact on patient survival.

Patient Selection

A retrospective study was conducted by selecting HCC patients who underwent TACE treatment from January 2012 to December 2018, which was approved by our hospital’s Institutional Review Board, and patient consent was waived due to the retrospective study design. All HCC patients were diagnosed based on the Barcelona Clinic Liver Cancer (BCLC) criteria, using imaging studies such as contrast-enhanced CT or MRI, tumor markers, and/or histopathological criteria. We selected HCC patients receiving TACE who met the following criteria: (1) TACE as the first-line treatment, (2) BCLC stages A, B, or C, (3) follow-up imaging available post-TACE using CT/MRI or DSA methods, (4) age ≥18 years. Patients were excluded if they met the following criteria: (1) age <18, (2) no post-TACE CT/MRI or DSA imaging available, (3) BCLC stage D, (4) concurrent or previous malignancy within the past 5 years, (5) death from any known cause. We did not differentiate between DEB-TACE and cTACE when selecting the treatment modality primarily during the study period. The choice of DEB-TACE was based on the multidisciplinary discussion among the interventional radiologists, hepatologists, oncologists, and patients regarding the cost and potential adverse effects of each material type, and the patients made the final decision. Two patient groups were selected in a 1:1 ratio, with no significant differences between the two groups in terms of stage, baseline parameters, and tumor characteristics.

Table 1.

Logistic regression analysis for factors influencing the occurrence of APS after DEB-TACE treatment

VariableUnivariable analysisMultivariable analysis
OR (95% CI)p valueOR (95% CI)p value
Child-Pugh class 
 A    
 B, C 0.594 (0.18–1.98) 0.397   
BCLC 
 A    
 B, C 0.800 (0.29–2.20) 0.670   
Tumor size 
 ≤3 cm    
 >3 cm 0.870 (0.34–2.25) 0.773   
Tumor number 
 1     
 >1 0.987 (0.84–1.17) 0.881   
Tumor capsule 2.255 (0.76–6.69) 0.143   
Peripheral tumor 1.146 (0.46–2.87) 0.771   
AFP, ng/mL 
 ≤400    
 >400 0.538 (0.19–1.56) 0.253   
ABLI score 0.561 (0.27–1.16) 0.120   
Feeding arteries 
 ≤2    
 >2 2.80 (0.94–8.33) 0.064 7.25 (1.82–28.95) 0.005 
Bead size 
 70–150 µm    
 >150 µm 0.54 (0.21–1.44) 0.217   
Vascular lake 2.07 (0.80–5.39) 0.134   
Non-selective embolization 3.49 (1.33–9.12) 0.092 8.02 (2.30–27.95) 0.001 
VariableUnivariable analysisMultivariable analysis
OR (95% CI)p valueOR (95% CI)p value
Child-Pugh class 
 A    
 B, C 0.594 (0.18–1.98) 0.397   
BCLC 
 A    
 B, C 0.800 (0.29–2.20) 0.670   
Tumor size 
 ≤3 cm    
 >3 cm 0.870 (0.34–2.25) 0.773   
Tumor number 
 1     
 >1 0.987 (0.84–1.17) 0.881   
Tumor capsule 2.255 (0.76–6.69) 0.143   
Peripheral tumor 1.146 (0.46–2.87) 0.771   
AFP, ng/mL 
 ≤400    
 >400 0.538 (0.19–1.56) 0.253   
ABLI score 0.561 (0.27–1.16) 0.120   
Feeding arteries 
 ≤2    
 >2 2.80 (0.94–8.33) 0.064 7.25 (1.82–28.95) 0.005 
Bead size 
 70–150 µm    
 >150 µm 0.54 (0.21–1.44) 0.217   
Vascular lake 2.07 (0.80–5.39) 0.134   
Non-selective embolization 3.49 (1.33–9.12) 0.092 8.02 (2.30–27.95) 0.001 

BCLC, Barcelona Clinic Liver Cancer; AFP, alpha-fetoprotein; ABLI score, albumin-bilirubin score.

Technique

The procedure was performed by experienced interventional radiologists with expertise in HCC treatment. Local anesthesia was administered at the subcutaneous level prior to using the Seldinger technique to place a vascular sheath into the femoral artery. A 5 Fr catheter was then used to get angiographic images of the superior mesenteric artery and visualize the portal vein system on deplayed phase. Subsequently, the catheter was advanced into the common hepatic artery via celiac trunk, and the tumor-feeding artery was identified using the EmboGuide software (Syngo Embolization Guidance, Siemens, Frankenthal, Germany) through cone-beam CT imaging. A 1.8 Fr-2.0 Fr microcatheter (Progreat; Terumo, Tokyo, Japan, and Asahi; Asahi Intecc, Nagoya, Japan) was used to access the tumor-feeding vessels using superselective or selective techniques. For cTACE, we used a dose of 20–50 mg of doxorubicin (Ildong, Seoul, Korea) dissolved in contrast media (Visipaque 270; GE HealthCare, Waukesha, USA) and 2–10 mL of Lipiodol (Guerbet, Roissy, France) and mixed them at a 1:4 ratio (doxorubicin: Lipiodol). The amount of chemotherapeutic agent and Lipiodol used depended on the size and vascularity of the tumor. Finally, the tumor-feeding vessels were embolized using 150–350 µm-sized gelatine microparticles (EG gel, Engain, Gyeonggi, Korea). On the other hand, for DEB-TACE, we used drug-eluting beads (DC Bead, Boston Scientific, Marlborough, MA, USA) of different sizes, including 70–150 µm (M1) or 100–300 µm, depending on tumor size. A vial of DC Bead was loaded with 50 mg of doxorubicin over a period of 30–60 min. A vial of DC Bead loaded with doxorubicin was diluted with 20 mL of contrast agent (Visipaque 270) and 20 mL of normal saline, creating a 40 mL mixture. For DEB-TACE, the contrast media near stasis as the endpoint for occlusion of the feeding arteries are common in the majority of cases.

Diagnosis of APS

Diagnosis of APS relied on different imaging methods, depending on the response of the tumor and the observed imaging findings. For patients with tumors showing complete response on CT/MRI 4–6 weeks after TACE, the diagnosis of APS was based on CT/MRI imaging findings, including (a) early visualization of peripheral portal vein branches and (b) remarkable discrepancy in contrast enhancement between the treated and preserved liver parenchyma [15]. In cases where tumors do not achieve complete response, the diagnosis is established based on angiogram/CBCT findings during the subsequent TACE session. For patients diagnosed with APS based on CT/MRI, APS relies on imaging characteristics and longitudinal monitoring to differentiate it from other potentially misleading conditions, such as tumor or inflammation [15‒17]. APS classification is based on Zhou et al. [18]: grade 1 refers to shunt flow into the subsegmental portal vein branch; grade 2 indicates shunt flow into the segmental portal vein branch; grade 3 represents shunt flow into the ipsilateral main portal vein branch; grade 4 signifies shunt flow into the contralateral main portal vein branch and/or main portal vein; and grade 5 corresponds to shunt flow into the main portal vein with hepatofugal portal venous flow.

Study Parameters

The BCLC stage is classified based on the characteristics of the disease at the time of the first TACE session. Liver function indices such as the Child-Pugh score and ALBI (albumin-bilirubin) level are considered. Tumor features are also documented, including the largest tumor size, number of tumors, and the presence of a capsule, which is defined as a thin signal layer surrounding the tumor visible in arterial phase imaging and enhanced in venous and late phases [19]. Peripheral tumors are described as those located adjacent to the liver capsule. Factors related to the TACE procedure itself are recorded, including the number of feeding arteries or the size of the drug-eluting beads. A vascular lake phenomenon, indicating the accumulation of contrast agent due to ruptured neovascular vessels within the tumor during DEB-TACE, is noted [20]. Non-selective embolization occurs when the microcatheter cannot be navigated into the artery feeding the tumor.

OS was calculated from the time of TACE treatment initiation to patient death. Progression-free survival (PFS) was measured from the time of TACE treatment to disease progression or patient death (whichever occurred first).

Statistical Analysis

Descriptive statistics such as means, medians, and standard deviations were used for quantitative variables, while categorical variables were described using proportions. For comparisons between the two groups, Student’s t test was used for quantitative variables, and Fisher’s exact test or χ2 test was used for categorical variables. Kaplan-Meier analysis was used to estimate survival rates for OS and PFS, and survival between the two groups was compared using the log-rank test. Logistic regression analysis was performed, and factors with a p value <0.1 in univariate analysis were included in the multivariate analysis to identify risk factors for APS. Statistical significance was set at p < 0.05. The odds ratio (OR) is calculated as the ratio of the odds of exposure to certain risk factors in the group with APS to the odds of exposure in the group without APS. Statistical analyses were performed using SPSS software version 26.

From January 2012 to December 2018, we identified a total of 74 patients who received initial treatment with DEB-TACE and an additional 74 patients who were selected as a matched control group and underwent treatment with cTACE during the same period. There were no significant differences between the two groups in major characteristics such as age (p = 0.741), gender (p = 1.000), and Child-Pugh class (p = 0.128), maximum tumor size (p = 0.102), number of tumors (p = 0.516), AFP serum level (p = 0.110), or BCLC stage (p = 0.117) (online suppl. Table 1; for all online suppl. material, see https://doi.org/10.1159/000537867). The incidence rate of APS after DEB-TACE was 46.0% (34 patients), whereas it was 16.2% (12 patients) in the cTACE group, with a significant difference of p value <0.001. All APS cases that occurred after DEB-TACE were classified into low grades, with 70.6% grade 1 and 29.4% grade 2.

There was no significant difference in OS between the DEB-TACE and cTACE groups, with a median follow-up time of 36.2 months (24.1–48.3) for the DEB-TACE group and 39.3 months 14.7–63.8) for the cTACE group (p = 0.982), HR: 0.995 (0.659–1.503) (Fig. 1a). Similarly, the median PFS was 12.1 months (6.3–17.7) for the DEB-TACE group and 9.9 months (8.4–13.2) for the cTACE group, with no significant difference (p = 0.802), HR: 0.956 (0.669–1.365) (Fig. 1b).

Fig. 1.

a The Kaplan-Meier survival curves demonstrate the similarity in OS between the two groups using cTACE and DEB-TACE. b The Kaplan-Meier curves show no significant difference in PFS between the cTACE and DEB-TACE groups.

Fig. 1.

a The Kaplan-Meier survival curves demonstrate the similarity in OS between the two groups using cTACE and DEB-TACE. b The Kaplan-Meier curves show no significant difference in PFS between the cTACE and DEB-TACE groups.

Close modal

In the DEB-TACE group, the median OS was 50 months (95% CI: 24.6–75.4) for patients with APS and 26.9 months (19.5–34.3) for those without APS (p = 0.111), HR: 0.621 (0.344–1.121) (Fig. 2a). The median PFS was 15.6 months (4.1–27.1) for patients with APS and 9.5 months (6.8–12.1) for those without APS (p = 0.065), HR: 0.626 (0.379–1.035) (Fig. 2b). Using logistic regression analysis to identify risk factors associated with increased incidence of APS in DEB-TACE groups patients, we found two factors with a p value <0.1, which were included in the multivariate analysis: more than two feeding arteries with an OR of 7.25 (1.82–28.95, p = 0.005) and non-selective embolization with an OR of 8.02 (2.30–27.95, p = 0.001) (Table 1).

Fig. 2.

a The Kaplan-Meier survival curves demonstrate no significant difference in OS between the APS and non-APS in groups receiving DEB-TACE treatment. b The Kaplan-Meier curves show no significant difference in PFS between APS and non-APS groups treated with DEB-TACE.

Fig. 2.

a The Kaplan-Meier survival curves demonstrate no significant difference in OS between the APS and non-APS in groups receiving DEB-TACE treatment. b The Kaplan-Meier curves show no significant difference in PFS between APS and non-APS groups treated with DEB-TACE.

Close modal

Several randomized controlled trials comparing cTACE and DEB-TACE have shown equivalent efficacy in terms of patient survival when treating unresectable HCC patients. In our study, we also found similar results, with no significant difference in OS and PFS between the two groups. The study by Shimosea et al. [13] was the first to demonstrate a higher incidence of APS after DEB-TACE compared to cTACE (48.7% vs. 8.1%, p < 0.0001). Our study also yielded similar results, with an APS occurrence rate of 46.0% after DEB-TACE compared to 16.2% after cTACE, showing a statistically significant difference with p value <0.001. However, all APS cases that appeared after DEB-TACE had low grades, with 70.6% classified as grade 1 and 29.4% as grade 2 according to the classification by Zhou et al. [18]. We did not encounter any severe APS cases with a grade ≥3.

In the study conducted by Demachi et al. [21], the presence of arterio-portal shunting (APS) was observed more frequently in the cohort with hepatic artery obstruction than in the group without. The development of APS varied between the central and peripheral regions of the liver; in central areas, APS developed through the peribiliary venous plexus, whereas in peripheral regions, APS formation occurred through direct communication from the hepatic artery to the terminal vein, a phenomenon more commonly observed in patients with cirrhosis [21]. Meanwhile, according to Lee, hepatic arterial damage was significantly higher in the group undergoing DEB-TACE compared to cTACE (OR, 6.36; p < 0.001) [12]. Minamiguchi suggested that the use of microsphere particles sometimes leads to aggregation and blockage of blood flow near the hepatic artery, causing increased subcapsular pressure post-TACE [22]. Additionally, the peritumoral portal veins were not embolized as in cTACE, creating favorable conditions for a higher incidence of APS in patients undergoing DEB-TACE [23].

The presence of APS has been identified as a poor prognostic factor in HCC patients, particularly in cases with portal vein thrombosis. APS can complicate the treatment process and increase the risk of complications associated with TACE. However, in our study, we did not observe a significant difference in OS and PFS between HCC patients treated with DEB-TACE with or without the occurrence of APS. The median OS was 50 months (24.6–75.4) for patients with APS and 26.9 months (19.5–34.3) for those without, with a p value of 0.111. Similarly, the PFS for both groups was 15.6 months (4.1–27.1) for patients with APS and 9.5 months (6.8–12.1) for those without, with a p value of 0.065. These results suggest that patients with APS may have a better prognosis than those without APS; although the difference was not statistically significant, this observation requires confirmation by a larger study. The occurrence of APS following DEB-TACE did not affect patient survival, as the majority were of low grade, with 70.6% being grade 1 according to Zhou’s classification, where APS was localized to the subsegment. These results indicate that although APS occurs more frequently after DEB-TACE compared to cTACE, the observed APS cases are of low grade and do not significantly affect liver function or the therapeutic efficacy of TACE on tumor response (Fig. 3). Therefore, the presence of APS may not be a crucial factor in the decision to choose between cTACE or DEB-TACE for HCC patients.

Fig. 3.

The patient is a 64-year-old male with hepatitis B and Child-Pugh B7 cirrhosis. a CT scan depicts an HCC tumor with a diameter of 35 mm in the posterior segment. b Celiac trunk angiogram showing a hypervascular tumor (location indicated by the arrow). c The HCC tumor was treated with DC Bead, with the post-TACE image showing drug uptake in the tumor (location indicated by the arrow). d Cone beam CT image, taken immediately after the procedure without contrast, displays drug uptake of the HCC tumor and surrounding liver tissue. e CT scan 1 month post-TACE reveals early signs of a portal vein shunt near the HCC tumor (location indicated by the arrow).

Fig. 3.

The patient is a 64-year-old male with hepatitis B and Child-Pugh B7 cirrhosis. a CT scan depicts an HCC tumor with a diameter of 35 mm in the posterior segment. b Celiac trunk angiogram showing a hypervascular tumor (location indicated by the arrow). c The HCC tumor was treated with DC Bead, with the post-TACE image showing drug uptake in the tumor (location indicated by the arrow). d Cone beam CT image, taken immediately after the procedure without contrast, displays drug uptake of the HCC tumor and surrounding liver tissue. e CT scan 1 month post-TACE reveals early signs of a portal vein shunt near the HCC tumor (location indicated by the arrow).

Close modal

In our investigation of risk factors associated with the occurrence of APS after DEB-TACE, we found that the presence of more than two feeding arteries had an OR of 7.25 (95% CI: 1.82–28.95, p = 0.005) and non-selective embolization had an OR of 8.02 (95% CI: 2.30–27.95, p = 0.001). Superselective DEB-TACE techniques can reduce the incidence of arterial, portal vein, and biliary injuries following DEB-TACE treatment [23]. The presence of multiple feeding arteries increases the risk of APS following DEB-TACE, potentially due to an increased risk of hepatic arterial damage, a factor that may elevate the incidence of APS [12]. Conversely, the existence of an excessive number of feeding pedicles can diminish the capability for superselective targeting. Therefore, for patients with multiple (>2) feeding arteries, cTACE should be considered the preferred option over DEB-TACE.

We acknowledge several limitations in our study. First, as a retrospective study, there may have been inherent biases in patient selection for the study, potentially affecting the representativeness of the broader population, and the sample size of our DEB-TACE group was relatively small with only 74 patients, which may limit the accuracy and generalizability of the survival analysis. Second, in our study, the concentration of doxorubicin in both the DEB-TACE and cTACE groups was not collected, which may be associated with an increased incidence of APS in patients undergoing DEB-TACE compared to those receiving cTACE. However, this was not the primary objective of our investigation and holds no practical significance in determining the choice of treatment modality for patients. Third, the diagnosis of APS in our study was not consistently standardized among patients as most patients who achieved complete response after the first TACE session were subsequently followed up with contrast-enhanced MRI or CT scans. However, the confirmation of APS was based on the monitoring of specific lesions to exclude similar-looking lesions, and this confirmation process was similar between the cTACE and DEB-TACE groups, thus minimizing potential discrepancies.

In conclusion, APS occurs at a higher rate in HCC patients treated with DEB-TACE compared to cTACE, but it does not impact patient survival. Non-selective embolization and the presence of more than two feeding arteries are risk factors associated with an increased occurrence of APS after DEB-TACE.

This study protocol was reviewed and approved by the Institutional Review Board of Seoul St. Mary’s Hospital, the Catholic University of Korea: KC23RISI0417. Opt-out informed consent protocol was used for use of participant data for research purposes. This consent procedure was reviewed and approved by Institutional Review Boards of our institution (Seoul St. Mary’s Hospital, the Catholic University of Korea) (approval number: KC23RISI0417).

None of the authors have conflicts of interest to disclose for this study.

This study was not supported by any sponsor or funder.

P.N.H., H.J.C., and J.S.O. were involved in the conceptualization. P.H.N. and H.J.C. edited the manuscript and analyzed the patients’ data. P.N.H., H.J.C., J.S.O., S.H.K., and B.G.C. collected the patients’ data. All the authors have read and approved the manuscript.

All data generated or analyzed during this study are included in this article and its online supplementary material files. Further inquiries can be directed to the corresponding author.

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