Radioembolization of Primary Liver Tumors for Patients with Pre-Existing Ascites: Beyond Child-Pugh score

doi:10.21203/rs.3.rs-7853339/v1

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Radioembolization of Primary Liver Tumors for Patients with Pre-Existing Ascites: Beyond Child-Pugh score

https://doi.org/10.21203/rs.3.rs-7853339/v1

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Journal Publication

published 11 Dec, 2025

Read the published version in Abdominal Radiology →

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Purpose

This study evaluates baseline characteristics associated with worsening ascites following TARE. A secondary objective was to examine survival among patients who developed ascites after TARE.

Methods

A total of 288 TARE deliveries (237 patients) for primary liver tumors were retrospectively reviewed. Imaging before and six months after TARE was assessed for ascites. Tumor volume, treated area, delivered activity, and liver function tests were reviewed. Logistic regression was performed for risk factors of liver decompensation including pre-existing ascites as a risk factor. Survival curves were plotted for overall survival.

Results

Mean (SD) age was 66 (11). 204 were male (71%). 266 (92%), 11 (4%), and 11 (4%) had hepatocellular carcinoma, intrahepatic cholangiocarcinoma and biphenotypic tumor, respectively. 60 (of 288, 21%) patients had pre-existing ascites. New/worsening ascites occurred in 121 (of 288, 42%) [93 (77%) new, 28 (23%) worsening]. Patients with new/worsening ascites had significantly greater increases in bilirubin (p = 0.01, p < 0.001). Pre-existing ascites was not associated with increased risk of post-TARE ascites progression, but a higher ALBI score was (OR = 2.89, p < 0.001). Neither perfused volume nor activity delivered predicted new/worsening ascites. Child-Pugh class (HR = 2.3, p < 0.001), pre-existing ascites (HR = 2, p < 0.001), ALBI score (HR = 1.5, p < 0.011) and new/worsening ascites (HR = 2.1, p < 0.001) were associated with lower survival.

Conclusions

Pre-existing ascites is associated with worse survival but should not preclude TARE. ALBI scoring can help distinguish patients at higher risk of post-TARE ascites.

Liver

hepatocellular carcinoma

trans-arterial radioembolization

ascites

ALBI score

1. Identifying patients at risk of new or worsening ascites after TARE is key to optimizing outcomes.

2. Pre-existing ascites alone was not associated with higher rates of post-TARE worsening ascites, but a higher baseline ALBI was. Both pre-existing and new/worsening ascites after TARE were associated with worse survival.

3. Identifying optimal candidates for TARE allows for safe and effective treatment. Patients with pre-existing ascites can still safely undergo TARE if ALBI score is favorable.

Liver cancer is the third leading cause of cancer-related mortality globally [1], and it is often unresectable at the time of diagnosis [2]. Loco-regional therapies, such as transarterial radioembolization (TARE), play a critical role in reducing tumor burden and enhancing survival [3, 4]. TARE has demonstrated the ability to prolong time to hepatic progression in primary liver tumors [5], but it does carry risks of adverse events, like radioembolization-induced liver disease (REILD) [6]. REILD is rare but can be associated with jaundice and ascites occurring in the first two months after TARE.

Assessing hepatic toxicity of TARE can be challenging as it is usually performed in patients who have underlying liver disease and an intermediate to advanced tumor [6]. A study by Su et al. reviewing TARE for neuroendocrine tumors in 54 patients with non-cirrhotic livers found that 41% of those who received whole-liver radiation developed ascites, and 15% developed varices [7]. Fortunately, patients with primary liver tumors tend to have a more targeted focus of treatment and do not require whole-liver radiation.

The presence of ascites prior to TARE has previously been identified as a negative prognostic factor for overall survival [8–11]. Given the risk of death without any treatment, certain patients with ascites will still receive TARE [2]. The influence of pre-existing ascites on mortality or worsened ascites following TARE remains uncertain. The primary objective of this study was to identify characteristics associated with worsening ascites following TARE. Pre-existing ascites was included as an independent risk factor. A secondary objective was to evaluate the survival of patients who develop new or worsening ascites after TARE.

Patient selection:

This is a retrospective institutional review board-approved study compliant with the Health Insurance Portability and Accountability Act of 1996. Adult patients who underwent TARE for treatment of primary liver tumors between January 2013 and July of 2020 were included in this study. The decision to perform TARE was based on multidisciplinary board decision making. Patients with inadequate follow-up data and/or metastatic liver disease were excluded. A total of 288 TARE deliveries for 237 patients with primary liver tumors were included. Given a single patient could undergo TARE at different times, the number of encounters to treat lesions were used as the basis of calculations in the study. Patients who developed main portal vein thrombosis (PVT) or tumor progression after TARE were excluded from the analysis to reduce confounding factors that could influence the development of ascites or liver decompensation independent of the effects of TARE itself. Patients who underwent lobar conventional trans-arterial chemoembolization (cTACE) prior to TARE, were included in the study but analyzed separately.

Data collection and definitions:

Clinical notes, laboratory studies, and imaging were reviewed prior to TARE and throughout the treatment course until an end point of transplantation, death, or loss to follow-up. Most patients were evaluated with imaging approximately every 3 months after TARE for tumor progression. Ascites was evaluated by two investigators through a review of cross-sectional imaging obtained at the closest date prior to TARE and again at least six months following the procedure. Review for paracentesis performed at or around imaging time points was also used to assess for ascites. Ascites was graded mild if confined to the perihepatic space and moderate-severe if it extended beyond the perihepatic space.

Overall survival and transplantation at follow up were collected. ALBI (Albumin-Bilirubin), MELD (model for end stage liver disease) and Child-Pugh scores were calculated and used in the regression model analysis.

TARE Technique:

Radioembolization with TheraSpheres (Boston Scientific, Marlborough, Massachusetts) was performed by 12 board-certified, fellowship-trained interventional radiologists with experience ranging from 1–20 years. TheraSpheres were prescribed based on the previously described standard protocol.

Total tumor volume, baseline and follow-up laboratory values, other liver-directed therapies undertaken before TARE (including embolization or ablation) were evaluated. The number of treatments, total Y90 activity (GBq), and distribution of treated area in TARE were collected. Treated area was evaluated based on the angiograms and defined as lobar if delivery was via left or right hepatic arteries; segmental if delivery was via a segmental branch; divisional if delivery was via anterior or posterior division of the right hepatic artery.

Statistics:

The last date of follow-up was recorded as the date of death, transplantation, or last encounter with the patient. Logistic regression analysis was performed for the risk factors of ascites. Patients were censored at the time of transplant or at the date of last follow up for the Kaplan-Meier survival analysis. Cox regression analysis for predictors of survival. A 2-tailed Fisher exact test, Student t-test, and Mann-Whitney U test were used as appropriate to identify differences in patients with and without ascites. Data were analyzed using STATA version 17 software (StataCorp, College Station, Texas). A p value of < 0.05 was used as the threshold for statistical significance.

Demographics:

The mean (SD) age was 66 (11) years. 204 (of 288, 71%) patients were male. Of the 288 tumors, 266 (92%) were hepatocellular carcinoma (HCC), 11 (4%) were intrahepatic cholangiocarcinoma (IHC), and 11 (4%) were biphenotypic tumors. Median (IQR) tumor volume was 65mL (14–268). Mean (SD) total administered Y90 activity was 2.8 (1.5) GBq. The treated area was distributed as follows: lobar 104 (of 288, 70%), segmental 39 (of 288, 14%), and divisional 45 (of 288, 16%). Table 1 highlights baseline demographics and patient characteristics, comparing those with and without ascites before TARE.

Table 1
, baseline characteristics of patient in the cohort, classified by if they developed ascites after TARE.
Baseline characteristics	WITHOUT new or worsening ascites after TARE (n = 167)	WITH New or worsening ascites after TARE (n = 121)	P-value
Age – years	66 (64–68)	66 (64–68)	0.435
Male:Female (percent male)	108:59 (65%)	96:25 (79%)	0.007
Child-Pugh score	5.5 (5.4–5.7)	5.7 (5.7–5.9)	0.971
Bilirubin	0.75 (0.68–0.83)	0.92 (0.83-1.00)	0.005
Albumin	3.85 (3.76–3.93)	3.63 (3.55–3.72)	0.002
ALBI score	-2.59 (-2.67 - -2.50)	-2.33 (-2.42 - -2.25)	0.001
MELD	9.3 (8.9–9.7)	9.8 (9.2–10.3)	0.945
Lobar Y90 delivery	119 (71%)	84 (69%)	0.736
Mean total activity administered (GBq)	2.74 (2.48-3.00)	2.83 (2.59–3.08)	0.696
Baseline portal vein thrombosis (main or branch)	41 (25%)	42 (35%)	0.060

Liver Toxicity after TARE:

Following TARE, total bilirubin increased from 0.8 to 2.3 mg/dL (p < 0.001) and alkaline phosphatase increased from159 to 212 U/L (p < 0.001). There was no significant increase in aminotransferase levels (ALT from 51 to 88, p = 0.206; AST from 69 to 180, p = 0.154). Comparing patients with and without pre-existing ascites, there was no significant difference in the rise of bilirubin (0.6 vs 0.3 mg/dL, p = 0.32). In patients without new/worsening ascites after TARE, bilirubin increased from 0.7 to 1.8 mg/dL (paired t-test, p < 0.001), whereas in those with new/worsening ascites after TARE bilirubin increased from 0.9 to 3.0 mg/dL (paired t-test, p < 0.001). The magnitude of increase in bilirubin was greater in patients who developed new/worsening ascites (p = 0.01). Similarly, MELD score increased significantly in all patients who received TARE, but the rise was greater in those who developed new/worsening ascites (2.2 vs. 5.9, p < 0.001).

Ascites before and after TARE:

At baseline, ascites was present in 60 (of 288, 21%) patients, with a majority classified as mild in severity [44 (of 60, 73%) mild ascites; 16 (of 60, 27%) moderate-severe ascites]. After TARE, 121 (of 288, 42%) developed new onset or worsening ascites. Among these, 93 (of 121, 77%) represented new onset ascites, while 28 (of 121, 23%) involved worsening of pre-existing ascites. Of the 121 patients with new/worsening ascites, 41 (34%) were classified as mild and 80 (66%) as moderate-severe.

Illustrated by Fig. 1, there was no significant difference in the incidence of new/worsening ascites after TARE when comparing patients with and without pre-existing ascites. The development of new onset ascites was observed in 93 (of 228, 41%), while worsening of pre-existing ascites was observed in 28 (of 60, 47%) (p = 0.412).

In the patients who developed new/worsening ascites, 21 (of 121, 17%) experienced new onset hepatic encephalopathy, likely suggesting a more severe liver decompensation. Of these, 15 (of 21, 71%) had no ascites at baseline, while 6 (of 21, 29%) had pre-existing ascites.

Risk Factors for Ascites after TARE

Amongst the patients who developed new/worsening ascites, 96 (of 121, 79%) were male, and 25 (of 121, 21%) underwent prior lobar cTACE. Review of the entire cohort revealed PVT in 83 patients (of 288, 29%) before TARE, with branch PVT in 32 (of 288, 11%) and segmental PVT in 51 (of 288, 18%). There was no significant association between PVT and new/worsening ascites [PVT present at baseline versus absent: 42 (35%) and 79 (65%), p = 0.060]. Lobar TARE was performed in 203 cases (70%). Lobar delivery of TARE was not associated with the development of new/worsening ascites after treatment. [37 (of 85, 44%) non-lobar treatment vs. 84 (of 203, 41%) lobar treatment, p = 0.736].

Univariable and multivariable logistic regression analyses of baseline characteristics and the development of new/worsening ascites after TARE is presented in Table 2. Factors such as PVT type, tumor volume, extent of Y90 infusion (segmental, divisional, lobar), total activity administered, Child-Pugh and MELD scores, baseline creatinine, INR, and alkaline phosphatase were not significantly associated with the development of new/worsening ascites after TARE. Multivariable analysis showed that pre-existing ascites was not associated with worsening ascites after TARE. However, male gender (OR = 2.1, p = 0.01), baseline albumin (OR = 0.4, p = 0.003), and ALBI score (OR = 2.89, p < 0.001) were all significantly associated with new/worsening ascites after TARE.

Table 2
, Univariable and multivariable logistic regression analysis evaluating association between baseline characteristics and new/worsening ascites after TARE.
	HR (95%CI)	P-value
Univariable analysis
Age – years	0.99 (0.98-1.00)	0.807
Sex (0 = male, 1 = female)	0.46	0.005
Child-Pugh score	1.24	0.088
Albumin	0.43	0.001
Bilirubin	1.8	0.017
ALBI score	2.6	< 0.001
MELD	1.06	0.143
Pre-existing ascites	1.26	0.410
Lobar Y90 delivery	0.92	0.765
Total Y90 activity (GBq)	1.03	0.888
Baseline portal vein thrombosis (0 = none, 1 = main portal, 2 = branch portal)	1.03	0.768
Total tumor volume	0.999	0.198
Multivariable analysis
Age – years	0.99 (0.97–1.02)	0.770
Sex (0 = male, 1 = female)	0.54 (0.3–0.9)	0.032
ALBI score	3.7 (1.7-8)	< 0.001
Pre-existing ascites	1.4 (0.58–3.4)	0.464
TARE = transarterial radioembolization, ALBI score = Albumin-Bilirubin score.

Child-Pugh and ALBI Score Stratification:

A majority (234, 86%) of patients had a baseline Child-Pugh A classification, while the remaining (38, 14%) were Child-Pugh B.

At baseline, 118 (of 288, 41%) patients were classified as ALBI Grade I, while 161 (of 288, 56%) were ALBI Grade II (9 patients had missing values that precluded ALBI calculation). Patients who developed new/worsening ascites after TARE had significantly higher ALBI scores (-2.59 vs. -2.34, p = 0.0001). Among those with new/worsening ascites, 34 (of 121, 28%) were baseline ALBI grade 1, whereas 85 (of 121, 70%) were ALBI grade 2 (p < 0.001).

Among patients with pre-existing ascites, 14 (of 60, 23%) classified as ALBI grade 1, while 45 (of 60, 75%) were ALBI grade 2 (p = 0.001). Within this group with pre-existing ascites, patients who experienced progression of ascites had significantly higher baseline ALBI grades [3 out of 14 (21%) in ALBI grade 1, versus 25 out of 45 (56%) in ALBI grade 2, p = 0.026].

Liver Transplant and Overall Survival

Patients with pre-existing ascites had a median overall survival of 11 months (IQR: 5–33), compared to 24 months (IQR: 14-not reached) for those without pre-existing ascites (Logrank p < 0.001). There was no statistically significant difference in median survival between patients with baseline mild versus moderate-severe ascites (15 months vs. 7 months, Logrank, p = 0.247). (Fig. 2)

Median overall survival was 27 months (IQR: 12-not-reached) for patients with baseline ALBI Grade 1 and 17 months (IQR: 5–46 months) for those with baseline ALBI Grade 2 (Logrank p = 0.001). In the subset of patients with pre-existing ascites, median overall survival was 27 months with baseline ALBI Grade I and 7 months with baseline ALBI Grade II (Logrank p = 0.001)

Cox regression showed a decreased survival in patients who developed new/worsening ascites after TARE (HR = 2.1, p < 0.001) (Fig. 3). Multivariable Cox regression showed that Child-Pugh class (HR = 2.3, p < 0.001), pre-existing ascites (HR = 2, p < 0.001), and ALBI score (HR = 1.5, p < 0.011) were significantly associated with higher mortality.

Following TARE, 41 (of 237, 17%) patients underwent liver transplant. This included 4 (10%) patients who had pre-existing ascites and 12 (29%) patients who experienced new/worsening ascites after TARE.

Most patients who undergo TARE do not have ascites prior to receiving therapy [5, 8, 12]. This can be attributed to patients with clinically significant ascites often not having sufficient functional liver reserve to safely undergo TARE. However, as demonstrated by the 60 patients (21%) in this cohort, there are certain patients with pre-existing ascites who maintain adequate liver function to be considered eligible for TARE.

Studies have shown that the presence of ascites prior to TARE can be associated with worse survival outcomes [8, 10, 11]. Consistent with previous studies, the presence of pre-existing ascites in this cohort, regardless of subsequent ascites progression, was a strong predictor of lower survival (11 vs 24 months, p < 0.001). New or worsening ascites after TARE was also independently associated with increased mortality (HR = 2.1, p < 0.001).

Patients with pre-existing ascites already have a reduced overall survival at baseline, but with the increased mortality risk without treatment, TARE can still offer meaningful benefit. From a palliative perspective, it can help reduce tumor burden, alleviate symptoms, and prolong survival [10]. Notably, the incidence of new/worsening ascites after TARE was similar between patients with and without pre-existing ascites. This highlights the fact that a subset of patients with pre-existing ascites can safely undergo TARE, without increasing the risk of progression. TARE can also serve as a bridge to liver transplant [13–15]. In our cohort, 41 patients (17%) underwent liver transplant, including four patients with pre-existing ascites and 12 patients with new/worsening ascites after TARE.

Selecting patients to safely undergo TARE requires a careful multi-disciplinary approach [2]. Previous studies have utilized traditional stratification methods, such as Child-Pugh and MELD, to demonstrate the influence of baseline liver function on survival after TARE [8, 16–18]. Salem et al. reported a survival difference of 9.5 months in patients with baseline Child-Pugh A and Child-Pugh B scores [5]. This current study also corroborates with these findings, demonstrating that increased Child-Pugh scores are associated with higher mortality (HR = 2.3, p < 0.001).

ALBI scoring has proven to be an effective tool for evaluating liver function and predicting outcomes in HCC patients undergoing tumor resection, cTACE, or TARE [2, 19–24]. In this cohort, higher baseline ALBI grade was also strongly associated with lower overall survival (10-month median survival difference, p = 0.001). These associations held true in patients with pre-existing ascites (20-month median survival difference, p = 0.001). Additionally, while pre-existing ascites did not predict progression of ascites after TARE, ALBI score was significantly associated with new/worsening ascites. These findings suggest that ALBI scoring can offer a more nuanced stratification of TARE candidates including those with pre-existing ascites who are at risk for worsening ascites.

This study has several limitations. This was a single center retrospective analysis. Due to the retrospective nature of the study, the evaluation of encephalopathy was limited. The study period encompasses older practice patterns, including more frequent use of lobar TARE. However, it is important to note that lobar treatment did not correlate with the development of ascites after TARE. Despite these limitations, the wide timespan of the study offers a more representative spectrum of disease and treatment approaches, enhancing the generalizability of the results to patients with primary liver tumors. The larger sample size and case-control design allows for meaningful conclusions to be drawn.

In summary, while the presence of ascites before TARE is associated with worse survival outcomes, it should not preclude patients from receiving treatment. ALBI scoring can aid in making more informed decisions when selecting candidates for TARE, including patients with pre-existing ascites. Future multi-center prospective studies are needed to further validate these findings.

Transarterial radioembolization (TARE), radioembolization-induced liver disease (REILD), portal vein thrombosis (PVT), conventional transarterial chemoembolization (cTACE), albumin-bilirubin (ALBI), model for end stage liver disease (MELD), hepatocellular carcinoma (HCC), intrahepatic cholangiocarcinoma (IHC), Barcelona clinic liver cancer (BCLC)

Author Contribution

Fayez Jabboure and Nassir Rostambeigi contributed in data collection, design, writing and final editing. Naganathan Mani contributed in design and editing and data collection Joshua Marlow contributed in design and data collection and editing Wyatt Reed contributed in data collection and editing and design of the study.

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No competing interests reported.

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You are reading this latest preprint version

Radioembolization of Primary Liver Tumors for Patients with Pre-Existing Ascites: Beyond Child-Pugh score

Status:

Journal Publication

Version 1

Abstract

Figures

Key Points

Introduction

Methods

Patient selection:

Data collection and definitions:

TARE Technique:

Statistics:

Results

Demographics:

Liver Toxicity after TARE:

Ascites before and after TARE:

Risk Factors for Ascites after TARE

Child-Pugh and ALBI Score Stratification:

Liver Transplant and Overall Survival

Discussion

Abbreviations

Declarations

Author Contribution

References

Additional Declarations

Status:

Journal Publication

Version 1