Efficacy and safety of endoscopic ultrasound-guided hepaticogastrostomy for biliary drainage in hypervascular hepatocellular carcinoma: a retrospective study from Japan

Kenneth Tachi; Kazuo Hara; Nozomi Okuno; Shin Haba; Takamichi Kuwahara; Toshitaka Fukui; Ahmed Mohammed Sadek; Hossam El-Din Shaaban Mahmoud Ibrahim; Minako Urata; Takashi Kondo; Yoshitaro Yamamoto

doi:10.5946/ce.2024.079

Articles

Page Path: HOME > Clin Endosc > Ahead-of print articles > Article

Original Article Efficacy and safety of endoscopic ultrasound-guided hepaticogastrostomy for biliary drainage in hypervascular hepatocellular carcinoma: a retrospective study from Japan: Kenneth Tachi, Kazuo Hara^,, Nozomi Okuno, Shin Haba, Takamichi Kuwahara, Toshitaka Fukui, Ahmed Mohammed Sadek, Hossam El-Din Shaaban Mahmoud Ibrahim, Minako Urata, Takashi Kondo, Yoshitaro Yamamoto; DOI: https://doi.org/10.5946/ce.2024.079
Published online: November 11, 2024

Department of Gastroenterology, Aichi Cancer Center Hospital, Nagoya, Japan

Correspondence: Kazuo Hara Department of Gastroenterology, Aichi Cancer Center Hospital, 1-1 Kanokoden, Chikusa-ku, Nagoya 464-8681, Japan Tel: +81-52-762-6111 E-mail: khara@aichi-cc.jp

• Received: April 2, 2024 • Revised: July 28, 2024 • Accepted: July 29, 2024

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

230 Views
40 Download

Full Article

Download PDF

Abstract
Graphical abstract
INTRODUCTION
METHODS
RESULTS
DISCUSSION
NOTES
REFERENCES

Abstract

Background/Aims
Biliary obstruction drainage in patients with hepatocellular carcinoma (HCC) is associated with symptom palliation, improved access to chemotherapy, and improved survival. Stent placement and exchange via endoscopic retrograde cholangiopancreatography biliary drainage risk traversing the HCC, a hypervascular tumor and causing bleeding. Endoscopic ultrasound-guided hepaticogastrostomy (EUS-HGS) potentially prevents procedure-related bleeding. Therefore, we evaluated the efficacy and safety of EUS-HGS as an alternative treatment for biliary obstruction in patients with HCC.
Methods
This was a retrospective study of all EUS-HGS procedures performed in patients with HCC at the Aichi Cancer Center Hospital, Japan, from February 2017 to August 2023.
Results
A total of 14 EUS-HGS procedures (42.9% primary) were attempted in 10 HCC patients (mean age 71.5 years, 80.0% male). Clinical and technical success rates were 92.9% and 90.9%, respectively. The observed procedure details in the 13 successful procedures included B3 puncture (53.8%), 22-G needle (53.8%), fully covered self-expandable metal stent (100%), and mean procedure time (32.7 minutes). There was no bleeding. Mild complications occurred in 27.3%. All patients resumed oral intake within 24 hours.
Conclusions
EUS-HGS is a technically feasible and clinically effective initial or salvage drainage option for the treatment of biliary obstruction in patients with HCC.
Keywords: Cholangitis; Endosonography; Fibrosis; Hepatocellular carcinoma; Obstructive jaundice

Graphical abstract

INTRODUCTION

Hepatocellular carcinoma (HCC) is the seventh most commonly diagnosed cancer and the third leading cause of cancer-related deaths worldwide.¹ Jaundice is common and reported in 5% to 44% of patients at the time of diagnosis. It often occurs due to underlying liver cirrhosis and/or extensive hepatic parenchymal destruction by the tumor. Biliary obstruction as a cause of jaundice is uncommon, but does occur in the late stages of the disease in approximately 0.5% to 13% of cases.²^,³ Biliary obstruction may result from tumor thrombi, hemobilia, direct tumor infiltration, extrinsic compression by tumor encasement, or metastatic lymph nodes of the major bile ducts.⁴ The presence of obstructive jaundice is associated with debilitating symptoms, such as pruritus, denial of access to chemotherapy, and poor prognosis.³ Therefore, biliary drainage offers palliation of jaundice and significantly improves patient survival.²^,⁵^-⁸

Endoscopic retrograde cholangiopancreatography (ERCP) biliary drainage (EBD) via transpapillary biliary stent placement has traditionally been the standard of care for unresectable malignant biliary obstructions.⁹^,¹⁰ Percutaneous transhepatic biliary drainage (PTBD) or surgery are alternatives when EBD fails. However, with the advent of endoscopic ultrasound (EUS)-based therapies, EUS-guided biliary drainage procedures, including transmural drainage, such as EUS-guided hepaticogastrostomy (EUS-HGS) and EUS-guided choledochoduodenostomy (EUS-CDS), have evolved into salvage procedures when ERCP fails or is not possible.¹¹ They are even used as first-line options for biliary drainage in patients with unresectable malignant biliary obstructions at some centers.¹² These have been shown to have equivalent or superior technical and clinical success rates to PTBD and surgery, but are less invasive, have fewer side effects, and offer a better quality of life.¹³^,¹⁴

EBD for obstructive jaundice in patients with HCC poses a unique challenge because of the highly vascularized nature of the tumor and the associated increased risk of bleeding from traversing the tumor. Subsequent stent exchange is associated with a high risk of bleeding. However, EUS-HGS is performed via a route that does not traverse the tumor (Fig. 1). Although we acknowledge that bleeding is the most common complication of EUS-HGS and that cirrhosis, if present, can pose an additional bleeding risk, we hypothesized that EUS-HGS could be a safe and effective biliary drainage option for HCC patients with obstructive jaundice and retrospectively investigated the use of EUS-HGS in these patients.

METHODS

The medical records of all patients with biliary obstruction due to unresectable hypervascular HCC who underwent EUS-HSG drainage at the Aichi Cancer Center, Japan, between February 2017 and August 2023, were retrospectively reviewed (Fig. 2A). At Aichi Cancer Center, EUS-HGS is the primary drainage procedure for malignant biliary obstructions. This procedure was performed to avoid ERCP-associated pancreatitis.

The last recorded clinical and laboratory data before the EUS-HGS procedure were used as baseline characteristics. Baseline ascites, if present, was graded as mild when detectable only by ultrasound examination, moderate when it caused moderately symmetrical distension of the abdomen, and severe or large when it caused marked abdominal distension.¹⁵

All EUS-HGS procedures were performed under midazolam sedation with the patients lying prone. A gastroscope was initially used to identify the gastroesophageal junction, which was marked with a clip to direct the endosonographer away from erroneous esophageal puncture. All EUS-HGSs were performed or supervised by an experienced endosonographer using a convex echoendoscope (oblique-viewing EUS GU-UCT260; Olympus Medical Systems or EG-740UT; FUJIFILM) or a forward-viewing EUS (GU-UCT260J; Olympus Medical Systems). The echoendoscope was inserted into the stomach and manipulated under endoscopic, ultrasonographic, and fluoroscopic guidance to identify the relevant structures.

After identification of the dilated left intrahepatic bile ducts (IHBD), either B2 or B3 was punctured after excluding the presence of interposing vessels with color Doppler (Fig. 2B). Depending on the diameter of the targeted IHBD, either a 22-G (Expect Slimline; Boston Scientific Co.) or 19-G EUS-FNA needle (EZ shot 3 plus; Olympus) preloaded with a guidewire through an attached Y-connector was chosen for puncturing the gastric wall and across the intervening liver tissue into the bile duct. The 19-G needle was selected if the IHBD diameter was greater than 5 mm and a 22-G for the rest. A 0.025-inch guidewire (VisiGlide2; Olympus Medical Systems), M-Through (Medicos Hirata), or a 0.018 inch (Fielder 18; Olympus Medical Systems) was used depending on whether a 19-G or 22-G needle respectively was used for the puncture. The guidewire was subsequently manipulated into the bile duct under fluoroscopic and echoendoscopic guidance, and a small amount of contrast medium was injected through the Y-connector to confirm the appropriate placement of the needle and guidewire (Fig. 2C). Once confirmed, the guidewire was inserted towards the hilum and the needle was withdrawn while maintaining the position of the guidewire. An uneven double-lumen cannula (PIOLAX Medical Devices) was passed through the guidewire into the bile duct. Bile content aspiration was performed to confirm the locations of the intraductal catheter tips. The aspirated bile was sent for culture and sensitivity testing. If a 22-G needle and 0.018-inch wire were used, fistula dilation was necessary. The fistula tract was dilated using a non-cautery device. The choice of device for dilation, a 6-Fr tapered cannula mechanical dilator (ES dilator soft type; Zeon Medical Co., Ltd.), uneven double-lumen cannula (PIOLAX Medical Devices), or a drill dilator (7-Fr, Tornus ES; Asahi Intec), was at the discretion of the endosonographer.

Cholangiography was performed by using an uneven double-lumen cannula. Finally, a fully covered self-expandable metal stent (FCSEMS) (6 mm×12 cm, HANAROSTENT Benefit; M.I.Tech Co.,Ltd.) was placed and the implantation site was confirmed both fluoroscopically and endoscopically (Fig. 2D).

All patients were administered intravenous antibiotics before and after the procedure. Other post-procedure management steps included monitoring symptoms (fever, abdominal pain, vomiting, hematemesis, and melena), vital signs (blood pressure, pulse rate, and body temperature), physical examination, blood tests (full blood count, C-reactive protein, and bilirubin), and contrast-enhanced computed tomography within 24 hours after the procedure to identify early complications.

Patients were discharged when they had no complaints and were clinically stable and a downward trend in bilirubin levels was observed. After discharge, clinical reviews were arranged, and blood tests were performed to assess cholestasis approximately 2 and 4 weeks after the procedure.

The total duration of the procedure was measured from the time of gastroscope insertion to the completion of all procedures. The following outcomes were evaluated: (1) technical success was defined as successful placement of the stent via the stomach into the left IHBD, as planned and confirmed by endoscopy and computed tomography; (2) clinical success was defined as postprocedural improvement in cholangitis or reduction in the total serum bilirubin level by 50% or more from preprocedural values within 4 weeks¹⁴; (3) complications: clinical, laboratory and/or radiological evaluation consistent with any of the following: bleeding (reduction in the serum hemoglobin level to <2.0 g/L from the pretreatment value), bile leakage, biloma, stent migration, stent misplacement, intrahepatic hematoma, sepsis, peritonitis, pseudoaneurysm of the hepatic artery, and death. The severity of adverse events was classified into grades I–V according to the classification of adverse events for GastRointEstinal Endoscopy (AGREE).¹⁶

Statistical analysis

Data were captured using an Excel spreadsheet. Baseline characteristics of clinical and laboratory data are presented as means (range) for continuous variables and as numbers of subjects or EUS procedures (percentages) for categorical variables, as stated.

Ethical statements

This study was approved by the Institutional Review Board of the Aichi Cancer Center Hospital (approval number: 2024-0-064). The requirement for informed consent was waived because of the retrospective nature of this study.

RESULTS

Ten patients with HCC who underwent 14 EUS-HGS attempts were included in this study. One patient underwent two procedures on the same day, whereas three patients underwent repeat procedures on different days ranging from 4 to 120 days apart.

The baseline patient characteristics are presented in Table 1. The mean age of the patients was 71.5 years with more males (80.0%) than females. Six patients presented with comorbidities: six (60.0%) had hypertension, and four (40.0%) had diabetes. Five (50.0%) had background cirrhosis and infection with viral hepatitis. Ascites was present in 5 of the 11 separate procedures. The mean total bilirubin was 130 (44.5–244.5) μmol/L, hemoglobin was 11.5 (7.3–14.5) g/L and C-reactive protein was 7.1 (0.6–17.9 mg/L). The mean baseline platelet count of 130.13 (60–270)×10⁹/L and international normalized ratio of 1.22 (1.0–1.52) did not warrant any pre-procedure correction of coagulopathy. None of the patients had cholangitis as an indication for EUS-HGS. Majority (69.2%) of the biliary obstructions occurred at the level of the hepatic hilum. The tumor, either by direct invasion or extrinsic compression of the bile duct, was the cause of the obstruction in 92.3% of cases. In the remaining 7.7%, the obstruction was caused by tumor thrombi. Three (60.0%) of the five patients with background cirrhosis were categorized in Child-Pugh class B. All cases were deemed inoperable, and four (36.4%) of the 11 distinct cases were classified as stage II according to the American Joint Commission on Cancer Staging System.

The technical details of the procedure are presented in Table 2. Six (42.9%) of the attempted 14 EUS-HGS were performed as primary procedures without prior ERCP. In another six (42.9%), EBD had been attempted at another facility before referral to the Aichi Cancer Center. One patient underwent two EUS-HGSs (simultaneous B2 and B3) in the same session, and another patient underwent separate EUS-HGSs of B2 and B3 4 days apart. These procedures were performed to improve the quality of drainage or the percentage of drained liver segments. A third patient also underwent a second EUS-HGS (B3) 3 months after the initial diagnosis (B2) because of the recurrence of biliary obstruction and increased bilirubin levels. In one patient, the initial attempt at EUS-HGS failed because of the inability to correctly identify and puncture the bile duct. However, the second attempt 18 days later was successful. Therefore, an overall technical success rate of 92.9% was achieved. Technical success was 100% for the primary procedures.

The mean diameter of the IHBD in the 13 successful cases was 3.7 (2.0 – 6.4) mm. In 7 (53.8%) cases, B3 was punctured, and the 22-G needles and 0.018-inch guidewires were used. In three of these seven cases, the initial 0.018-inch guidewire was changed to a 0.025 guidewire to complete the procedure. A 6×120 mm FCSEMS was deployed in all cases. The mean procedure time was 32.7 (15–50) minutes.

Details of the postprocedural events are shown in Table 3. 50% or more reduction in baseline bilirubin levels was recorded in 8 (72.7%) by the end of week 2. Clinical success was reported in 10 (90.9%) of the 11 distinct procedures. Clinical success and other post-procedure details could not be assessed in two cases because they were too close to other procedures to be evaluated separately. All patients resumed eating within 24 hours. No adverse bleeding events were observed. However, other mild (AGREE grades I and II) adverse events were reported in 3 (27.3%) patients, all of which resolved with conservative management. Two patients with AGREE grade I required antipyretics, whereas a single patient with grade II required additional antibiotics to treat cholecystitis. The patient in whom the initial EUS-HGS was unsuccessful had cholecystitis that persisted at the time of the second attempt and continued thereafter. The mean duration of hospital stay was 11 (4–37) days.

DISCUSSION

Advancements in therapeutic options for patients with late-stage HCC warrant the identification of safer and more effective biliary drainage methods so that these patients can benefit from such therapies, enjoy jaundice palliation, and improve survival. In this study, we demonstrated that EUS-HGS is a technically feasible and highly effective procedure for patients with HCC that can be performed by experienced surgeons without causing bleeding. To the best of our knowledge, this is the first report of EUS-HGS as a drainage procedure performed solely in patients with HCC.

The technical success rate of 92.9% reported in this study was comparable to the 93.1% and 93.7 reported by Li et al.¹⁷ and Uemura et al.,¹⁸ respectively in meta-analyses of EUS-HGS for drainage of various unresectable malignant biliary obstructions. It was also not inferior to EBD procedures previously reported for HCC.⁵ In patients in whom EUS-BD failed initially, the procedure was successful on a second attempt. This high technical success rate was achieved despite the presence of ascites in three patients before the performance of EUS-HGS. Although moderate ascites is generally considered a contraindication, Yasuda et al.¹⁹ demonstrated that such a procedure is technically feasible and safe. The experience of the group undoubtedly played a role in high success rates.

Fistula dilatation before stent deployment is an important step in EUS-HGS. Mechanical dilatation using the ES dilator soft type or the novel tornus device was preferred over the technically easier to use electric cautery devices because of their superior safety.¹⁴^,²⁰^,²¹ Generally, a balloon dilator is a good rescue device because it creates a larger tract; however, some expertise is required to avoid bile leakage. Electric cautery devices have been shown to have a higher risk of procedure-related bleeding; therefore, avoiding these devices in these cases was good.¹⁴ Thankfully, the cautery dilator was not needed as a rescue in these cases.

Although a 19-G needle and 0.035 or 0.025 guidewires are favored during EUS-HGS, in this study, the 22-G needle and 0.018-inch wires were successfully used to start and finish the procedure in 4 of 13 procedures. Although more technically difficult to use, a smaller needle offers less traumatic puncture and, therefore, probably contributes to a lower bleeding risk, especially in the setting of cirrhosis. Experience with smaller needles and guidewires has been previously reported.²²^,²³

The clinical success rate of 90.9% reported in this study is superior to clinical success rate of 35% to 81% reported for EBD drainage procedures.⁵^,⁶^,²⁴ This was also higher than the 84.5% reported by Uemura et al.¹⁸ in a meta-analysis of EUS-BD for all malignant biliary obstructions. Successful drainage can provide patients with HCC relief from the symptoms of obstructive jaundice, particularly intense pruritus, and the opportunity to receive additional chemotherapy. Therefore, successful biliary drainage improves both patient survival and quality of life. In 8/11 (72.7%) of cases in this study, significant (≥50%) reduction in baseline bilirubin levels were achieved within 2 weeks; therefore, these patients could potentially start or restart chemotherapy after this period.

Although EBD is the gold standard for unresectable malignant biliary obstructions, several studies have demonstrated the utility of EUS-HGS as the primary drainage procedure for malignant biliary obstructions.¹²^,²⁵^,²⁶ Our study adds to the body of evidence that EUS-HGS is technically feasible and safe as a primary procedure, even for HCC. Technical success rate was 100% for all the seven primary EUS-HGS procedures, and clinical success was achieved in five out of six patients.

There is a higher risk of stent migration and clogging by food materials after successful stent placement with EUS-HGS than with EUS-CDS or PTBD. However, stent patency has been reported to be longer with EUS-HGS than with PTBD, ranging from 62 to 402 days.²⁷ Longer stent patency is associated with factors such as the stent type and length. In this study, an FCSEMS with a length of 12 cm was used to conform to the recommendations. FCSEMS have a wider diameter and are less susceptible to tumor ingrowth. A long stent also allows an intragastric stent length of >3 cm, which reduces the risk of inward stent migration.

The reported total complication rate of 27.3% was higher than the pooled early adverse event rate of 18.2% reported by Isayama et al. for EUS-HGS of other malignant biliary strictures.¹⁴ This was better though than the adverse event rate of 35% and mortality of 5% reported by Winkler et al. on the feasibility of EUS-HGS for similarly inoperable malignant hilar strictures.²⁶ In this study, all three complications were mild and resolved with conservative management. No bleeding was observed. This is significant because most biliary obstructions were caused by tumor compression of the bile duct at the hilum. Drainage through the EBD route would have meant traversing the tumor and significantly increasing bleeding risk. In a previous study that used EBD in HCC patients, a bleeding rate of 2.9% and 18.6% incidence rate of post ERCP pancreatitis were reported.⁵ One patient, in whom the procedure technically failed on the first attempt, developed cholecystitis. This delayed reintervention by approximately 18 days, after which a repeat EUS-HGS was successfully performed. The course of cholecystitis prolonged the hospital stay to 37 days. The mean duration of the hospital stay after the procedure was 11 days. This is longer than the mean durations of 7.5 and 8 days of hospital stay reported by Winkler et al.²⁶ and Sportes et al.,¹³ respectively. However, this confirms the findings of Sportes et al.¹³ that EUS-HGS is associated with a shorter hospital stay than PTBD (15 days).

In addition, all patients were able to resume feeding within 24 hours after the procedure. This early resumption of feeding and the observed shorter duration of hospital stay certainly contributed to a better quality of life, which has been severally reported with EUS-HGS over other EBD salvage procedures.²⁸

The relatively small number of patients from a single center in this study means that extrapolation of the results must be performed with caution. However, the baseline characteristics of the patients in this study mirror those previously reported for patients with HCC in Japan: more males, a mean age of more than 70 years, and a predominant HCV association.²⁹

Clinical success could not be determined when two separate procedures were performed on two different patients. In one patient, a repeat procedure was performed less than 4 weeks after the initial procedure, while in another patient, two procedures were performed at the same time. Therefore, it is impossible to distinguish the clinical success of these procedures separately.

In conclusion, EUS-HGS is a technically feasible and clinically effective procedure that can be used to drain biliary obstructions in patients with hypervascular HCC. This can be performed without causing bleeding by experienced hands. It can be considered the primary drainage procedure or a salvage procedure when others fail. Further research is recommended to explore the survival benefits of this procedure for different stages of HCC and liver disease severities.

Conflicts of Interest

The authors have no potential conflicts of interest.

Funding

None.

Author Contributions

Conceptualization: KT, KH, NO, SH, TKu; Data curation: KT, NO, TF, AMS, HEDSMI, MU, TKo, YY; Formal analysis: KT, NO, TF, AMS, HEDSMI, MU, TKo, YY; Methodology: KT, KH, NO, SH, TKu, AMS, HEDSMI, MU, TKo, YY; Resources: KT, KH, NO, SH, TKu, TF, MU, TKo, YY; Supervision: KH, NO, SH, TKu; Validation: KT, KH, NO, SH, TKu; Visualization: KT, KH, NO, SH, TKu; Writing–original draft: KT, KH, NO, SH, TKu; Writing–review & editing: all authors.

Fig. 1.

Schematic representation showing the position of a stent placed via (A) endoscopic retrograde cholangiopancreatography biliary drainage and (B) endoscopic ultrasound-guided hepaticogastrostomy for drainage of malignant biliary obstruction.

Fig. 2.

(A) Computed tomography scan image of a hypervascular hepatocellular carcinoma causing biliary obstruction (arrowhead). (B) Endoscopic ultrasound image of dilated intrahepatic bile duct, B3. (C) Fluoroscopy image highlighting the dilated bile duct and appropriately placed guidewire after contrast injection. (D) Endoscopic image of the implantation site and intragastric portion of a successfully deployed fully covered self-expandable metal stent.

Table 1.

Baseline patient characteristics

Characteristic	Value
Total no. of patients	10
Age (yr)	70.7 (63–79)
Sex
Male	8 (80.0)
Female	2 (20.0)
Comorbidity
Hypertension	6 (60.0)
Diabetes	4 (40.0)
Stroke	0 (0)
Drug history
Anticoagulant	0 (0)
Antiplatelet	0 (0)
Presence of ascites (n=11)
Absent	6 (54.5)
Mild	2 (18.2)
Moderate	3 (27.3)
Severe	0 (0)
Cirrhosis
Present	5 (50.0)
Absent	5 (50.0)
Etiology
HBsAg	2 (20.0)
Anti-HCV	3 (30.0)
Unknown	5 (50.0)
Laboratory parameters (n=11)
Hemoglobin (g/L)	11.5 (7.3–14.5)
C-reactive protein (mg/L)	7.1 (0.6–17.9)
White cell count (×10⁹/L)	6.1 (3.2–10.0)
Bilirubin (μmol/L)	130 (44.5–244.5)
Albumin (g/L)	26 (14–41)
AST/ALT (U/L)	1.61 (0.90–4.50)
ALP (U/L)	801 (231–1,347)
Platelets (×10⁹/L)	130.13 (60–270)
International normalized ratio	1.22 (1.0–1.52)
Concomitant cholangitis	0 (0)
Anatomical level of biliary obstruction (n=13)
Hepatic hilum	9 (69.2)
Intrahepatic bile duct	3 (23.1)
Common hepatic duct	1 (7.7)
Cause of biliary obstruction (n=13)
Tumor	12 (92.3)
Tumor thrombi	1 (7.7)
Lymph nodes	0 (0)
Child-Pugh class (n=5)
A	0 (0)
B	3 (60.0)
C	2 (40.0)
AJCC 8th edition stage (n=11)
IA	0 (0)
1B	2 (18.2)
II	4 (36.4)
IIIA	1 (9.1)
IIIB	1 (9.1)
IVA	1 (9.1)
IVB	2 (18.2)

Values are presented as median (range) or number (%).

HBsAg, hepatitis B surface antigen; anti-HCV, antibodies against hepatitis C virus; AST, aspartate aminotransferase; ALT, alanine aminotransferase; ALP, alkaline phosphatase; AJCC, American Joint Commission on Cancer.

^a)Child-Pugh class was determined only for patients with cirrhosis.

Table 2.

Technical details of EUS-HGS procedures

Characteristic	Value
Total number of EUS-HGS	14
Technical success
Yes	13 (92.9)
No	1 (7.1)
Timing of procedure
Primary	6 (42.9)
Previous EBD	6 (42.9)
EUS-HGS salvage	2 (14.3)
Biliary duct diameter (mm)	3.7 (2.0–6.4)
Puncture site (n=13)
B2	6 (46.2)
B3	7 (53.8)
Puncture needle (n=13)
22-G	7 (53.8)
19-G	6 (46.2)
Guidewire (n=13)
0.018 inch	7 (53.8)
0.025 inch	6 (46.2)
Guidewire exchange after use of 0.018 inch (n=7)
Yes	3 (42.9)
No	4 (57.1)
Procedure time (min) (n=13)	32.7 (15–50)
Stent type (n=13)
FCSEMS	13 (100.0)
PS	0 (0)
Stent length (cm) (n=13)
12	13 (100.0)
Others	0 (0)

Values are presented as number (%) or median (range).

EUS-HGS, endoscopic ultrasound-guided hepaticogastrostomy; EBD, endoscopic retrograde cholangiopancreatography biliary drainage; FCSEMS, fully covered self-expandable metal stent; PS, plastic stent.

Table 3.

Post-EUS events for 11 procedures^a)

Characteristic	Value
Return to feeding
Within 1 day	11 (100)
>1 day	0 (0)
Duration of hospital stay (day)	11 (4–37)
Clinical success
Yes	10 (90.9)
No	1 (9.1)
Complications	3 (27.3)
Fever	2 (18.2)
Bleeding	0 (0)
Stent migration	0 (0)
Cholecystitis	1 (9.1)
Peritonitis	0 (0)
Severity of complications (AGREE grade)
I	2 (15.4)
II	1 (7.7)
III	0 (0)
IV	0 (0)
V	0 (0)

Values are presented as number (%) or median (range).

EUS, endoscopic ultrasound; AGREE, adverse events for GastRointEstinal Endoscopy.

^a)These variables could only be determined for 11 distinct procedures. The oother two procedures were too close to each other to be evaluated separately.

REFERENCES

1. Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021;71:209–249.Article PubMed PDF
2. Qin LX, Tang ZY. Hepatocellular carcinoma with obstructive jaundice: diagnosis, treatment and prognosis. World J Gastroenterol 2003;9:385–391.Article PubMed PMC
3. Huang JF, Wang LY, Lin ZY, et al. Incidence and clinical outcome of icteric type hepatocellular carcinoma. J Gastroenterol Hepatol 2002;17:190–195.Article PubMed
4. Soyer P, Laissy JP, Bluemke DA, et al. Bile duct involvement in hepatocellular carcinoma: MR demonstration. Abdom Imaging 1995;20:118–121.Article PubMed PDF
5. Woo HY, Han SY, Heo J, et al. Role of endoscopic biliary drainage in advanced hepatocellular carcinoma with jaundice. PLoS One 2017;12:e0187469.Article PubMed PMC
6. Matsumi A, Kato H, Ueki T, et al. Effectiveness, safety, and factors associated with the clinical success of endoscopic biliary drainage for patients with hepatocellular carcinoma: a retrospective multicenter study. BMC Gastroenterol 2021;21:28.Article PubMed PMC PDF
7. An J, Lee KS, Kim KM, et al. Clinical features and outcomes of patients with hepatocellular carcinoma complicated with bile duct invasion. Clin Mol Hepatol 2017;23:160–169.Article PubMed PMC PDF
8. Minami Y, Kudo M. Hepatocellular carcinoma with obstructive jaundice: endoscopic and percutaneous biliary drainage. Dig Dis 2012;30:592–597.Article PubMed PDF
9. Dumonceau JM, Tringali A, Papanikolaou IS, et al. Endoscopic biliary stenting: indications, choice of stents, and results: European Society of Gastrointestinal Endoscopy (ESGE) clinical guideline: updated October 2017. Endoscopy 2018;50:910–930.Article PubMed
10. Giovannini M, Moutardier V, Pesenti C, et al. Endoscopic ultrasound-guided bilioduodenal anastomosis: a new technique for biliary drainage. Endoscopy 2001;33:898–900.Article PubMed
11. Jagielski M, Zieliński M, Piątkowski J, Jackowski M. Outcomes and limitations of endoscopic ultrasound-guided hepaticogastrostomy in malignant biliary obstruction. BMC Gastroenterol 2021;21:202.Article PubMed PMC PDF
12. Hara K, Yamao K, Hijioka S, et al. Prospective clinical study of endoscopic ultrasound-guided choledochoduodenostomy with direct metallic stent placement using a forward-viewing echoendoscope. Endoscopy 2013;45:392–396.Article PubMed
13. Sportes A, Camus M, Greget M, et al. Endoscopic ultrasound-guided hepaticogastrostomy versus percutaneous transhepatic drainage for malignant biliary obstruction after failed endoscopic retrograde cholangiopancreatography: a retrospective expertise-based study from two centers. Therap Adv Gastroenterol 2017;10:483–493.Article PubMed PMC PDF
14. Isayama H, Nakai Y, Itoi T, et al. Clinical practice guidelines for safe performance of endoscopic ultrasound/ultrasonography-guided biliary drainage: 2018. J Hepatobiliary Pancreat Sci 2019;26:249–269.Article PubMed PMC PDF
15. Aithal GP, Palaniyappan N, China L, et al. Guidelines on the management of ascites in cirrhosis. Gut 2021;70:9–29.Article PubMed
16. Nass KJ, Zwager LW, van der Vlugt M, et al. Novel classification for adverse events in GI endoscopy: the AGREE classification. Gastrointest Endosc 2022;95:1078–1085.Article PubMed
17. Li J, Tang J, Liu F, et al. Comparison of choledochoduodenostomy and hepaticogastrostomy for EUS-guided biliary drainage: a meta-analysis. Front Surg 2022;9:811005.Article PubMed PMC
18. Uemura RS, Khan MA, Otoch JP, et al. EUS-guided choledochoduodenostomy versus hepaticogastrostomy: a systematic review and meta-analysis. J Clin Gastroenterol 2018;52:123–130.Article PubMed
19. Yasuda T, Hara K, Mizuno N, et al. Safety of endoscopic ultrasound-guided hepaticogastrostomy in patients with malignant biliary obstruction and ascites. Clin Endosc 2024;57:246–252.Article PubMed PDF
20. Yamada M, Hara K, Haba S, et al. Endoscopic ultrasound-guided hepaticogastrostomy using a novel drill dilator. Endoscopy 2022;54(S 02):E856–E857.Article PubMed PMC
21. Hara K, Okuno N, Haba S, et al. How to perform EUS-guided hepaticogastrostomy easier and safer. J Hepatobiliary Pancreat Sci 2020;27:563–564.Article PubMed PDF
22. Iwashita T, Ogura T, Ishiwatari H, et al. Utility of dedicated bougie dilator for a 0.018-inch guidewire during EUS-guided biliary drainage: a multi-center retrospective cohort study. J Hepatobiliary Pancreat Sci 2022;29:810–816.Article PubMed PDF
23. Ogura T, Ueno S, Okuda A, et al. Expanding indications for endoscopic ultrasound-guided hepaticogastrostomy for patients with insufficient dilatation of the intrahepatic bile duct using a 22G needle combined with a novel 0.018-inch guidewire (with video). Dig Endosc 2022;34:222–227.Article PubMed PDF
24. Sugiyama G, Okabe Y, Ishida Y, et al. Evaluation of endoscopic biliary stenting for obstructive jaundice caused by hepatocellular carcinoma. World J Gastroenterol 2014;20:6968–6973.Article PubMed PMC
25. Okuno N, Hara K, Mizuno N, et al. Efficacy of the 6-mm fully covered self-expandable metal stent during endoscopic ultrasound-guided hepaticogastrostomy as a primary biliary drainage for the cases estimated difficult endoscopic retrograde cholangiopancreatography: a prospective clinical study. J Gastroenterol Hepatol 2018;33:1413–1421.Article PubMed PDF
26. Winkler J, Caillol F, Ratone JP, et al. Feasibility of EUS-guided hepaticogastrostomy for inoperable malignant hilar biliary strictures. Endosc Ultrasound 2021;10:51–56.Article PubMed PMC
27. Paik WH, Park DH. Outcomes and limitations: EUS-guided hepaticogastrostomy. Endosc Ultrasound 2019;8(Suppl 1):S44–S49.Article PubMed PMC
28. Nakai Y, Kogure H, Isayama H, et al. Endoscopic ultrasound-guided biliary drainage for unresectable hilar malignant biliary obstruction. Clin Endosc 2019;52:220–225.Article PubMed PMC PDF
29. Kiyosawa K, Umemura T, Ichijo T, et al. Hepatocellular carcinoma: recent trends in Japan. Gastroenterology 2004;127(5 Suppl 1):S17–S26.Article PubMed

Figure & Data

REFERENCES

Citations

Citations to this article as recorded by

PubReader
ePub Link

Cite

CITE: export Copy Download Format; Close

Download Citation

Download a citation file in RIS format that can be imported by all major citation management software, including EndNote, ProCite, RefWorks, and Reference Manager.

Format:

RIS — For EndNote, ProCite, RefWorks, and most other reference management software
BibTeX — For JabRef, BibDesk, and other BibTeX-specific software

Include:

Citation for the content below
Citation and abstract for the content below

Efficacy and safety of endoscopic ultrasound-guided hepaticogastrostomy for biliary drainage in hypervascular hepatocellular carcinoma: a retrospective study from Japan

DOI: https://doi.org/10.5946/ce.2024.079

XML Download

Figure

Related articles

Efficacy and safety of endoscopic ultrasound-guided hepaticogastrostomy for biliary drainage in hypervascular hepatocellular carcinoma: a retrospective study from Japan

Fig. 1. Schematic representation showing the position of a stent placed via (A) endoscopic retrograde cholangiopancreatography biliary drainage and (B) endoscopic ultrasound-guided hepaticogastrostomy for drainage of malignant biliary obstruction.

Fig. 2. (A) Computed tomography scan image of a hypervascular hepatocellular carcinoma causing biliary obstruction (arrowhead). (B) Endoscopic ultrasound image of dilated intrahepatic bile duct, B3. (C) Fluoroscopy image highlighting the dilated bile duct and appropriately placed guidewire after contrast injection. (D) Endoscopic image of the implantation site and intragastric portion of a successfully deployed fully covered self-expandable metal stent.

Graphical abstract

Fig. 1.

Fig. 2.

Graphical abstract

Efficacy and safety of endoscopic ultrasound-guided hepaticogastrostomy for biliary drainage in hypervascular hepatocellular carcinoma: a retrospective study from Japan

Characteristic	Value
Total no. of patients	10
Age (yr)	70.7 (63–79)
Sex
Male	8 (80.0)
Female	2 (20.0)
Comorbidity
Hypertension	6 (60.0)
Diabetes	4 (40.0)
Stroke	0 (0)
Drug history
Anticoagulant	0 (0)
Antiplatelet	0 (0)
Presence of ascites (n=11)
Absent	6 (54.5)
Mild	2 (18.2)
Moderate	3 (27.3)
Severe	0 (0)
Cirrhosis
Present	5 (50.0)
Absent	5 (50.0)
Etiology
HBsAg	2 (20.0)
Anti-HCV	3 (30.0)
Unknown	5 (50.0)
Laboratory parameters (n=11)
Hemoglobin (g/L)	11.5 (7.3–14.5)
C-reactive protein (mg/L)	7.1 (0.6–17.9)
White cell count (×10⁹/L)	6.1 (3.2–10.0)
Bilirubin (μmol/L)	130 (44.5–244.5)
Albumin (g/L)	26 (14–41)
AST/ALT (U/L)	1.61 (0.90–4.50)
ALP (U/L)	801 (231–1,347)
Platelets (×10⁹/L)	130.13 (60–270)
International normalized ratio	1.22 (1.0–1.52)
Concomitant cholangitis	0 (0)
Anatomical level of biliary obstruction (n=13)
Hepatic hilum	9 (69.2)
Intrahepatic bile duct	3 (23.1)
Common hepatic duct	1 (7.7)
Cause of biliary obstruction (n=13)
Tumor	12 (92.3)
Tumor thrombi	1 (7.7)
Lymph nodes	0 (0)
Child-Pugh class (n=5)
A	0 (0)
B	3 (60.0)
C	2 (40.0)
AJCC 8th edition stage (n=11)
IA	0 (0)
1B	2 (18.2)
II	4 (36.4)
IIIA	1 (9.1)
IIIB	1 (9.1)
IVA	1 (9.1)
IVB	2 (18.2)

Characteristic	Value
Total number of EUS-HGS	14
Technical success
Yes	13 (92.9)
No	1 (7.1)
Timing of procedure
Primary	6 (42.9)
Previous EBD	6 (42.9)
EUS-HGS salvage	2 (14.3)
Biliary duct diameter (mm)	3.7 (2.0–6.4)
Puncture site (n=13)
B2	6 (46.2)
B3	7 (53.8)
Puncture needle (n=13)
22-G	7 (53.8)
19-G	6 (46.2)
Guidewire (n=13)
0.018 inch	7 (53.8)
0.025 inch	6 (46.2)
Guidewire exchange after use of 0.018 inch (n=7)
Yes	3 (42.9)
No	4 (57.1)
Procedure time (min) (n=13)	32.7 (15–50)
Stent type (n=13)
FCSEMS	13 (100.0)
PS	0 (0)
Stent length (cm) (n=13)
12	13 (100.0)
Others	0 (0)

Characteristic	Value
Return to feeding
Within 1 day	11 (100)
>1 day	0 (0)
Duration of hospital stay (day)	11 (4–37)
Clinical success
Yes	10 (90.9)
No	1 (9.1)
Complications	3 (27.3)
Fever	2 (18.2)
Bleeding	0 (0)
Stent migration	0 (0)
Cholecystitis	1 (9.1)
Peritonitis	0 (0)
Severity of complications (AGREE grade)
I	2 (15.4)
II	1 (7.7)
III	0 (0)
IV	0 (0)
V	0 (0)

Table 1. Baseline patient characteristics

Values are presented as median (range) or number (%).

Child-Pugh class was determined only for patients with cirrhosis.

Table 2. Technical details of EUS-HGS procedures

Values are presented as number (%) or median (range).

EUS-HGS, endoscopic ultrasound-guided hepaticogastrostomy; EBD, endoscopic retrograde cholangiopancreatography biliary drainage; FCSEMS, fully covered self-expandable metal stent; PS, plastic stent.

Table 3. Post-EUS events for 11 proceduresa)

Values are presented as number (%) or median (range).

EUS, endoscopic ultrasound; AGREE, adverse events for GastRointEstinal Endoscopy.

These variables could only be determined for 11 distinct procedures. The oother two procedures were too close to each other to be evaluated separately.