Effectiveness of balloon occlusion in percutaneous transhepatic portal vein embolization with gelatin sponge: a single-institutional retrospective study

doi:10.21203/rs.3.rs-4882066/v1

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Effectiveness of balloon occlusion in percutaneous transhepatic portal vein embolization with gelatin sponge: a single-institutional retrospective study

https://doi.org/10.21203/rs.3.rs-4882066/v1

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Background

Standard methods for percutaneous transhepatic portal vein embolization (PTPE) have not yet been established. This study aimed to elucidate the effectiveness of balloon occlusion in PTPE using gelatin sponges on the future liver remnant volume hypertrophy ratio. This retrospective study included 93 patients who underwent PTPE for right hepatectomy between January 2018 and September 2022. Based on the embolization procedure, patients were divided into balloon group (n = 13) and non-balloon group (n = 80). The clinical factors and the future liver remnant volume hypertrophy ratios were compared. Moreover, significant factors associated with the future liver remnant volume hypertrophy ratio between the groups were analyzed.

Results

The future liver remnant volume hypertrophy ratio was significantly higher in the balloon group than in the non-balloon group (1.44 [interquartile range, 1.37–1.89] vs. 1.29 [1.15–1.46], P = 0.011). The initial future liver remnant volume (289 [interquartile range, 259–454] vs. 400 [324–479] mL, P = 0.036) and number of gelatin sponge sheets (5 [interquartile range, 5–6] vs. 4 [3–5], P = 0.008) significantly differed. However, recanalization and severe complications were not different between groups. According to the multivariate linear regression analysis, diabetes mellitus (coefficient, -0.202; P = 0.009), initial future liver remnant volume (coefficient, -0.001; P < 0.001), and balloon occlusion (coefficient, 0.228; P = 0.007) were independent factors affecting the future liver remnant volume hypertrophy ratio.

Conclusion

Balloon occlusion may be effective in future liver remnant volume hypertrophy in PTPE using gelatin sponges.

Balloon occlusion

percutaneous transhepatic portal vein embolization

hypertrophy

Preoperative portal vein embolization (PVE) involves embolization of the portal vein of the liver segment to be resected before major hepatectomy, thereby promoting hypertrophy of the remnant liver segment to prevent postoperative liver failure. Since its introduction by Kinoshita et al. and Makuuchi et al. [1, 2], PVE has been reported as a useful procedure [3, 4]. However, hypertrophy of the future liver remnant volume (FLRV) following PVE was not sufficient in some patients. Previous reports have indicated that different patient conditions, such as initial FLRV or liver function and PVE methods, could influence hypertrophy [5, 6].

There are various methods for PVE. These approaches may include percutaneous transhepatic portal vein embolization (PTPE) or laparotomic trans-ileocolic vein approach [7]. The types of embolic materials used include gelatin sponges (GS), fibrin glue, metallic coils, n-butyl-2-cyanoacrylate (NBCA), and absolute ethanol, which may be used alone or in combination [3, 4, 7–10]. The CIRSE guidelines recommend NBCA as the first-line embolic material in PTPE [11]. In contrast, the first-line embolic material is still controversial in the Japanese Society of Interventional Radiology guidelines [12]. In Japan, NBCA for endovascular procedures has been commercially available from September 2022. Therefore, PTPE is performed using GS with a non-balloon catheter as the standard procedure in our hospital. We hypothesized that balloon occlusion in PTPE with GS may improve the hypertrophy ratio of FLRV in some patients, because balloon occlusion may allow the practitioner to inject more GS without the fear of backflow. The balloon catheter is usually used for liquid embolic materials, such as ethanol or ethanolamine oleate with iopamidol [13, 14]. These procedures are heterogeneous and depend on the discretion of the physician. Although certain studies have reported that PVE using GS alone [15] or GS with balloon occlusion was effective [16, 17], no study has compared PVE using GS between with and without balloon occlusion.

In the present study, we aimed to elucidate the efficacy of balloon occlusion in PTPE with GS on the hypertrophy ratio of FLRV.

Study design and Patient selection

This was a single-institutional retrospective study conducted at our hospital. We reviewed medical records between January 2018 and September 2022 and identified that 102 patients underwent PTPE for right hepatectomies. Of these, nine patients, including four patients who underwent medial branch embolization for right trisectionectomy, three patients who underwent embolization of only the anterior branch, and two patients who underwent embolization of only the posterior branch were excluded. A total of 93 patients who underwent embolization of the anterior and posterior branches for right hepatectomy were included. The patients were divided into two groups: the balloon occlusion (using a balloon catheter, n = 13) and non-balloon occlusion groups (using a non-balloon catheter, n = 80). Figure 1 shows a consort diagram of this study.

This study was approved by the Institutional Review Board of the Shizuoka Cancer Center (approval number: J2022-212-2022-1-3).

Portal vein embolization

PTPE was indicated when right hepatectomy was planned or when the future liver remnant volume × indocyanine green plasma disappearance rate was ≤ 0.05 [18]. All PTPE procedures were performed by three board-certified interventional radiologists with 30, 18, and 13 years of experience, respectively. The patient was sedated with intravenous administration of pentazocine (15 mg) and hydroxyzine hydrochloride (25 mg) as premedication and local anesthesia with lidocaine (1.0%). Subsequently, the right anterior portal branch was punctured using a 21-gauge needle with an ultrasound-guided ipsilateral approach. Thereafter, a 0.018-inch guidewire was inserted. After dilation using a two-step procedure, a 5 Fr catheter (Hook type; Hanako Medical, Saitama, Japan; 70 cm) or a 5 Fr balloon catheter with a 9-mm balloon diameter (Selecon MP catheter II®, Terumo Clinical Supply, Gifu, Japan) (Fig. 2A, B) was inserted through a 5 Fr sheath. A balloon catheter was employed when the initial liver volume was small and required great hypertrophy or when the neck length of the right portal vein was short and backflow was a concern. However, there are no definite criteria for catheter selection and it is at the discretion of the physician. GS particles (Serescue®, Astellas Pharma Inc, Tokyo, Japan), prepared by pumping two syringes connected with a three-way stopcock back and forth several times, were used as the embolic material in all patients. Serescue® sheet (2.5 × 2.5 × 1 cm; width × length × thickness) is composed of the same material as Spongel® (LTL Pharma Co., Ltd., Tokyo, Japan). The particle size distribution mainly ranges from 2–3 mm (33.3%) when the sheet is processed by pumping five times [19]. Embolization was terminated when there was minimal or absent antegrade flow into the anterior and posterior portal branches, and hepatic parenchymal enhancement had disappeared in both balloon and non-balloon groups (Fig. 2C). Furthermore, tract embolization to prevent post-procedure bleeding was performed using 0.035-inch metallic coils (MReye; diameter, 3 mm; length, 4 cm; Cook Medical, Bloomington, IN, USA) (Fig. 2D) in accordance with the guideline [12].

Complications associated with PTPE were assessed by the Common Terminology Criteria for Adverse Events version 5.0 [20]. Severe complications were defined as Grade 3 or more.

Assessment of liver volume

Two to four weeks after PTPE, contrast-enhanced computed tomography (CT) was performed to assess the blood flow and FLRV. Recanalization was defined as portal venous flow after PTPE on contrast-enhanced CT. FLRV was calculated using a three-dimensional image analysis system (SYNAPSE VINCENT; FUJIFILM, Tokyo, Japan). The hypertrophy and hypertrophy ratio of the FLRV were calculated using the following formula:

Hypertrophy of FLRV = (FLRV after PTPE) – (initial FLRV)

Hypertrophy ratio of FLRV = (FLRV after PTPE) / (initial FLRV)

Statistical analyses

The chi-squared test or Fisher’s exact test was used to compare categorical variables. The Mann–Whitney U test was used to compare continuous variables. Continuous variables are expressed as medians with interquartile ranges. Linear regression analysis was used to analyze the factors affecting the hypertrophy ratio of FLRV. If a variable showed statistical significance at P < 0.05 in the univariate analysis, it was incorporated into the multivariate analysis model. To estimate a causal effect, intermediate variables were excluded in the multivariate analysis.

Statistical analyses were performed using JMP software (version 13.0; SAS Institute, Cary, NC, USA). A P-value < 0.05 was considered statistically significant.

Patient characteristics, PTPE procedure, and hypertrophy ratio of FLRV

The comparison between the non-balloon and balloon groups regarding patient characteristics, results of the PTPE procedure, and hypertrophy ratio of the FLRV are listed in Table 1. Initial FLRV was significantly lower in the balloon group than in the non-balloon group (289 mL [interquartile range (IQR), 259–454] vs. 400 [324–479] mL, P = 0.036). Age, sex, body mass index, diabetes mellitus (DM), and various factors reflecting liver function, such as serum total bilirubin level, serum albumin level, plasma prothrombin time, and indocyanine green plasma disappearance rate, were not significantly different between the two groups. According to the PTPE procedure, the number of GS sheets was significantly higher in the balloon group than in the non-balloon group (5 [IQR, 5–6] vs. 4 [3–5], P = 0.008). The procedure time, proportion of recanalization, and severe complications were not significantly different between the two groups. The hypertrophy and hypertrophy ratio of the FLRV were significantly higher in the balloon group than in the non-balloon group (hypertrophy of FLRV: 142 [IQR, 114–239] vs. 116 [75–173] mL, P = 0.038; hypertrophy ratio of FLRV: 1.44 [IQR, 1.37–1.89] vs. 1.29 [1.15–1.46], P = 0.011), whereas the number of days from PTPE to assessment of the FLRV was not.

Table 1

The association between catheter with balloon and clinical factors in PTPE
Variable (n = 93)	Non-balloon (n = 80)	Balloon (n = 13)	P-value
Patient characteristics
Age, years, median (IQR)	71 (64–75)	70 (67–75)	0.978
Sex, Male (%)	57 (71)	12 (92)	0.108
BMI, kg/m², median (IQR)	22 (20–24)	23 (22–25)	0.215
DM, present (%)	12 (15)	3 (23)	0.463
Type of disease, BDC/HCC/meta	49/7/24	10/1/2	0.522
Background liver, cirrhosis (%)	1 (1.3)	1 (7.7)	0.261
Serum T-bil level before PTPE, mg/dL, median (IQR)	0.8 (0.5–1.2)	0.7 (0.5–1.2)	0.469
Serum albumin level before PTPE, g/dL, median (IQR)	4.0 (3.7–4.3)	3.8 (3.7–4.1)	0.339
Plasma PT before PTPE, %, median (IQR)	100 (92–109)	98 (88–104)	0.233
ICGK before PTPE, median (IQR)	0.19 (0.16–0.22)	0.18 (0.16–0.24)	0.872
Initial FLRV, mL (IQR)	400 (324–479)	289 (259–454)	0.036
PTPE procedure
Time of PTPE, min, median (IQR)	65 (51–90)	80 (68–95)	0.095
Number of gelatin sponge used, median (IQR)	4 (3–5)	5 (5–6)	0.008
Recanalization of blood flow, positive (%)	28 (35)	2 (15)	0.161
Severe complication of PTPE
Bile leakage required drainage	1	1	0.469
Hepatic hemorrhage required embolization	1	0
Thrombus in left portal branch	1	0
The assessment of hypertrophy ratio
Days from PTPE to FLRV assessment, median (IQR)	16 (14–21)	18 (14–24)	0.264
Hypertrophy of FLRV, mL, median (IQR)	116 (75–173)	142 (114–239)	0.038
Hypertrophy ratio of FLRV, median (IQR)	1.29 (1.15–1.46)	1.44 (1.37–1.89)	0.011
PTPE, percutaneous transhepatic portal vein embolization; IQR, interquartile range; BMI, body mass index; DM, diabetes mellitus; BDC, bile duct cancer; HCC, hepatocellular carcinoma; meta, metastatic disease; T-bil, total bilirubin; PT, prothrombin time; ICGK, indocyanine green clearance rate; FLRV, future liver remnant volume Significant values are shown in bold.

Association between future liver remnant volume and clinical factors

Table 2 presents the factors affecting the FLRV hypertrophy ratio. Univariate linear regression analysis showed that the presence of DM (regression coefficient, -0.206 [95% confidence interval (CI), -0.384 to -0.029], P = 0.023) and initial larger FLRV (regression coefficient, -0.001 [95% CI, -0.002 to -0.001], P < 0.001) were negatively correlated with the hypertrophy ratio of FLRV. The number of GS used (regression coefficient, 0.090 [95% CI, 0.047–0.013], P < 0.001) and balloon occlusion (regression coefficient, 0.293 [95% CI, 0.109–0.477], P = 0.002) were positively correlated with the hypertrophy ratio of FLRV. Age, sex, body mass index, disease type, background liver, and liver function were not significantly correlated. Balloon occlusion increases the number of GS used. From a causal inference perspective, the number of GS used is an intermediate variable. However, as we estimated the total causal effect of balloon occlusion on the hypertrophy ratio of FLRV, the number of GS used was excluded from the multivariate analysis. Multivariate linear regression analysis showed that presence of DM (regression coefficient, -0.202 [95% CI, -0.352 to 0.051], P = 0.009), initial FLRV (regression coefficient, -0.001 [95% CI, -0.001 to 0.001], P < 0.001), and balloon occlusion (regression coefficient, 0.228 [95% CI, 0.066–0.391], P = 0.007) were independent factors affecting the hypertrophy ratio of FLRV.

Table 2

Univariate and multivariate linear regression analyses predicting hypertrophy ratio of the future liver remnant
Variable (n = 93)	Hypertrophy ratio
	Univariate			Multivariate
	Coefficient	95% CI	P-value	Coefficient	95% CI	P-value
Age, year	-0.004	-0.011, 0.004	0.313
Sex, Male	0.074	-0.079, 0.227	0.338
BMI, kg/m²	0.021	-0.002, 0.043	0.071
DM, present	-0.206	-0.384, -0.029	0.023	-0.202	-0.352, -0.051	0.009
Disease, HCC	0.013	-0.226, 0.253	0.913
Background liver, cirrhosis	-0.004	-0.236, 0.228	0.973
Serum T-bil level before PTPE, mg/dL	-0.094	-0.206, 0.018	0.098
Serum albumin level before PTPE, g/dL	0.130	-0.010, 0.270	0.069
Plasma PT before PTPE, %	0.000	-0.005, 0.004	0.837
ICGK before PTPE	1.426	-0.295, 3.147	0.103
Initial FLRV, mL	-0.001	-0.002, -0.001	< 0.001	-0.001	-0.001, -0.001	< 0.001
Number of gelatin sponge used	0.090	0.047, 0.013	< 0.001	-	-	-
Balloon occlusion	0.293	0.109, 0.477	0.002	0.228	0.066, 0.391	0.007
BMI, body mass index; DM, diabetes mellitus; PTPE, percutaneous transhepatic portal vein embolization; T-bil, total bilirubin; PT, prothrombin time; ICGK, indocyanine green clearance rate; FLRV, future liver remnant volume; CI, confidence interval Significant values are shown in bold.

In this study, we found that the balloon catheter, along with the absence of DM and a smaller initial FLRV, had an influence on the hypertrophy ratio of FLRV in PTPE with GS.

A balloon catheter in PTPE is used for liquid embolic materials to prevent backflow into the portal vein branches of the remnant liver [13, 14]. The current study revealed that balloon occlusion could enable the use of more GS sheets for embolization, resulting in a greater FLRV hypertrophy ratio. This may be attributed to the fact that the practitioner injected them without the fear of backflow during the procedure. Although there was no significant difference in the proportion of radiological recanalization, packing more GS sheets may have contributed to hypertrophy. Previous reports of PVE using GS with balloon occlusion indicated that the hypertrophy ratio of FLRV (average/median) was 1.29/1.20 [16] or 1.35/1.34 [17]. In this study, the hypertrophy ratio of FLRV (average/median = 1.62/1.44) was comparable. Balloon occlusion in PTPE using GS may be useful in terms of the hypertrophy ratio without severe complications that would affect the clinical course.

The optimal embolic material for PTPE has not yet been determined. NBCA is highly effective in treating FLRV hypertrophy [21]. However, NBCA has some disadvantages. The contralateral approach is required to avoid the risk of catheter entrapment within the portal venous system [22]. Moreover, NBCA can cause backflow into the left portal vein that is difficult to handle. Since the contralateral approach has potential risks of complications, including biliary hemorrhage, arterioportal shunt formation, or portal thrombosis [23], the ipsilateral approach may be preferred for protecting the remnant liver over the contralateral approach. Therefore, we used GS, which is easy to handle and affordable as an embolic agent via the ipsilateral approach, as the standard method in our hospital. Although we did not compare GS with other embolic materials, our results revealed that balloon occlusion may be effective in causing greater hypertrophy when GS is used.

Additionally, the current study revealed that DM, initial FLRV, and balloon occlusion were significantly associated with the FLRV hypertrophy ratio. Although DM was not reported as a significantly associated factor according to a recent review article [6], some reports indicated that DM or steatosis was associated with impaired hypertrophy [24–26]. Since DM may cause steatosis, it may negatively affect FLRV hypertrophy. In terms of initial FLRV, the result was consistent with previous reports that indicated that the initial FLRV was a predictor of a higher hypertrophy ratio [5, 6]. Watanabe et al. reported that a large FLRV before PVE could indicate a small embolized liver volume and had little influence on the volume shift [5]. These predictive factors—DM and initial FLRV—for the hypertrophy ratio of the FLRV may aid in the selection of cases in which a catheter with a balloon should be used, anticipating larger hypertrophy.

The present study had some limitations. First, this was a retrospective, single-center study with a limited number of patients. Second, there was a potential for selection bias by desiring greater hypertrophy of FLRV. Third, this study did not evaluate liver function after PVE. Although the remnant liver was enlarged, its function remained unclear after PTPE with balloon occlusion. Therefore, a future concern is whether dominant hypertrophy of FLRV by balloon occlusion is beneficial in hepatectomy.

Balloon occlusion in PTPE with GS may contribute to improving the hypertrophy ratio of FLRV; however, further research is required to confirm this finding.

Ethics approval and consent to participate: This study was approved by the Institutional Review Board of the Shizuoka Cancer Center (approval number: J2022-212-2022-1-3).

This study is a retrospective study. We provided information about the study on our website and offered an opt-out opportunity. Specifically, it was created detailing the study’s content, purpose, and the handling of personal information. Patients and their families were given clear instructions on how to refuse participation in the study.

Consent for publication: Consent for publication was obtained for every individual person’s data included in the study.

Availability of data and material: All data collected in this study were obtained retrospectively from medical records and have been anonymized to protect patient privacy.

Competing interests: The authors have no relevant financial or non-financial interests to disclose.

Funding: No funding was received for conducting this study.

Authors' contributions: HK, AS and RS contributed to the conception and design of the study. HK and AS performed the data collection and analysis, and drafted the manuscript. RS, OS, AR, KO, MY, YK, KU, AN, TS and TA critically revised the manuscript for important intellectual content. AN provided critical feedback on the statistical analysis. All authors provided final approval of the version to be published.

Acknowledgements: We would like to thank Editage (www.editage.jp) for English language editing.

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Effectiveness of balloon occlusion in percutaneous transhepatic portal vein embolization with gelatin sponge: a single-institutional retrospective study

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Abstract

Background

Results

Conclusion

Figures

Background

Materials & Methods

Study design and Patient selection

Portal vein embolization

Assessment of liver volume

Statistical analyses

Results

Patient characteristics, PTPE procedure, and hypertrophy ratio of FLRV

Association between future liver remnant volume and clinical factors

Discussion

Conclusion

Declarations

References

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