Primary endoscopic ultrasound-guided hepaticogastrostomy for biliary drainage prior to pancreatoduodenectomy: a retrospective study in Japan

Nozomi Okuno; Kazuo Hara; Seiji Natsume; Masataka Okuno; Shin Haba; Tomonari Asano; Takamichi Kuwahara; Hiroki Koda; Yasuhiro Shimizu

doi:10.5946/ce.2024.218

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Original Article Primary endoscopic ultrasound-guided hepaticogastrostomy for biliary drainage prior to pancreatoduodenectomy: a retrospective study in Japan: Nozomi Okuno¹, Kazuo Hara¹, Seiji Natsume², Masataka Okuno², Shin Haba¹, Tomonari Asano², Takamichi Kuwahara¹, Hiroki Koda¹, Yasuhiro Shimizu²; Clinical Endoscopy 2025;58(4):604-611.
DOI: https://doi.org/10.5946/ce.2024.218
Published online: February 11, 2025

¹Department of Gastroenterology, Aichi Cancer Center Hospital, Nagoya, Japan

²Department of Surgery, Aichi Cancer Center Hospital, Nagoya, Japan

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

• Received: August 18, 2024 • Revised: September 15, 2024 • Accepted: September 16, 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.

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Abstract
Graphical abstract
INTRODUCTION
METHODS
RESULTS
DISCUSSION
NOTES
REFERENCES

See letter "Assessment of endoscopic ultrasound-guided hepaticogastrostomy as a feasible option for preoperative biliary drainage before pancreaticoduodenectomy" in Volume 58 on page 549.

Abstract

Background/Aims
Malignant lesions of the pancreatic head can cause obstructive jaundice requiring biliary drainage. However, the effect of post-endoscopic retrograde cholangiopancreatography (ERCP) pancreatitis and metal stents on surgical resection remains controversial. This study aimed to investigate the efficacy of primary endoscopic ultrasound-guided hepaticogastrostomy (EUS-HGS) performed prior to pancreatoduodenectomy, excluding patients with biliary duct cancer.
Methods
We retrospectively analyzed consecutive patients who underwent pancreatoduodenectomy at our institution between January 2019 and December 2022. The patients were divided into three groups: without biliary drainage (n=130), endoscopic biliary stenting (EBS) (n=57), and primary EUS-HGS (n=20).
Results
The positivity rate of the intraoperative bile juice culture was significantly higher in the EBS group (p<0.001). No significant difference was observed among the groups in terms of postoperative adverse events (Clavien-Dindo grade 3 or higher, p=0.784) or the positive rate of peritoneal lavage cytology (p=0.984). Seven patients in the EBS group (12.3%) experienced early adverse events related to biliary drainage (post-ERCP pancreatitis, n=3; acute cholecystitis, n=3; bile duct perforation, n=1), whereas none in the EUS-HGS group experienced adverse events.
Conclusions
Primary EUS-HGS is technically feasible as a preoperative procedure and has no short-term postoperative disadvantages.
Keywords: Endosonography; Obstructive jaundice; Pancreaticoduodenectomy; Preoperative care

Graphical abstract

INTRODUCTION

Malignant diseases of the pancreatic head, most commonly pancreatic head cancers, often result in obstructive jaundice. However, the necessity of preoperative biliary drainage (PBD) in resectable cases of obstructive jaundice remains controversial. A multicenter randomized controlled trial (RCT) that compared PBD with surgery alone in pancreatic head cancer reported that PBD for curative surgery could increase adverse biliary events.¹ However, another study suggested that PBD could decrease the rate of postoperative complications.² In the clinical setting, patients with pancreatic cancer are often administered neoadjuvant chemotherapy before surgery, and PBD is frequently performed to control conditions such as obstructive jaundice and cholangitis. Endoscopic retrograde cholangiopancreatography (ERCP) might be required, and endoscopic biliary stenting (EBS) might be required in clinical settings. However, ERCP carries the risk of post-ERCP pancreatitis, and severe necrotizing pancreatitis may occasionally occur, which can be fatal.³

Endoscopic ultrasound-guided hepaticogastrostomy (EUS-HGS) is widely used. Although it initially served as salvage therapy after failed ERCP,⁴ it is now also performed for primary drainage in patients in whom ERCP is expected to be difficult or impossible.⁵ EUS-HGS has two significant advantages preoperatively in patients undergoing pancreatoduodenectomy (PD): it carries no risk of pancreatitis after the procedure,⁶^,⁷ and the site of EUS-HGS does not interfere with the surgical field, thus minimally affecting the surgery. Because of these two major advantages, we have performed primary EUS-HGS before PD (excluding patients with bile duct cancer) since 2019. The objectives of the current study were to evaluate the efficacy of primary EUS-HGS and to assess the technical feasibility and short-term postoperative outcomes of PD performed after EUS-HGS.

METHODS

Patients

We retrospectively analyzed consecutive patients who underwent PD at our institution between January 2019 and December 2022. Patients with biliary duct cancer were excluded. The indications for PBD were obstructive jaundice (total bilirubin ≥2.0 mg/dL) and/or liver dysfunction and/or cholangitis caused by malignant distal biliary stricture.

A total of 211 patients who underwent PD were eligible for inclusion. The patients were divided into three groups: without biliary drainage (n=130), EBS (n=57), and primary EUS-HGS (n=20). Four patients were excluded from the study: one who underwent percutaneous transhepatic biliary drainage and three who were converted from EBS to EUS-HGS (Fig. 1).

Procedures

1) EUS-HGS

All EUS-HGS procedures were performed by a single expert endoscopist in our department. An oblique-viewing convex-type echo-endoscope (GU-UCT260; Olympus or EG-740UT; FUJIFILM) or a forward-viewing convex-type EUS (GU-UCT260J; Olympus) was used for EUS-HGS.⁸^,⁹ First, a marking clip was placed at the esophagogastric junction to facilitate easy identification and prevent trans-esophageal puncture.¹⁰

EUS-HGS is generally performed as follows: A 22-gauge needle (Expect Slimline; Boston Scientific Co.) was filled with the contrast medium and preloaded with a 0.018-inch guidewire (Fielder 18; ASAHI Intecc) using a connector (Rotating Hemostatic Valve, 0.096’’; Abbott). B2 was punctured to maintain a distance from the gastrectomy line under color Doppler imaging, which was stabilized by insertion of the guidewire. Although a few patients had B3 punctures, the following method was used. Next, a small amount of contrast medium was injected to verify insertion into the bile duct. The needle tract was gradually dilated using a dilator or catheter (ES Dilator, Zeon Medical Co., Ltd.; Tornus ES, Asahi Intecc; or Uneven Double Lumen Cannula, PIOLAX Medical Devices). After aspirating the bile and injecting contrast medium to outline the biliary tree, a fully covered self-expandable metal stent (FCSEMS: 6 mm×12 cm HANAROSTENT biliary, HANAROSTENT Benefit; Boston Scientific Co. or 8 mm×10 cm or 12 cm Covered Bile Rush Advance; PIOLAX) is deployed. The distal end of the stent was placed on the B2 side at the confluence of segments 2–3 to prevent B3 obstruction. To prevent internal stent migration, its length should be at least 10 cm.¹¹ Nevertheless, the HANAROSTENT Benefit stent is quite flexible and easy to bend between the stomach and liver, which can lead to internal stent migration. Therefore, when using this stent, a clip was placed on the gastric side as a flap.¹² Computed tomography was conducted for all patients 24 hours post-procedure to verify the absence of adverse events.

2) EUS-HGS stent removal

After surgery, we confirmed adequate bile flow to the choledocojejunostomy by fluoroscopy with injection of contrast medium from the HGS fistula and subsequently removed the stent with forceps in all 20 patients.

3) Outcome measures and definitions

The primary endpoint was the incidence of adverse events associated with endoscopic procedures. We recorded early adverse events that might be associated with the endoscopic procedure and that occurred within 14 days after the procedure, as defined in the American Society for Gastrointestinal Endoscopy lexicon.¹³ The secondary endpoints included surgical outcomes, positive rate of intraoperative bile culture, and surgery-related adverse events. Postoperative mortality included all deaths that occurred before or within 90 days of discharge. Morbidity included all postoperative complications up to discharge and/or readmission and was classified according to the Clavien-Dindo classification.¹⁴

Statistical analysis

All data were analyzed using the StatMate V statistical software (ATMS). Differences were considered statistically significant when p-values were less than 0.05.

Ethical statements

All patients consented to the procedure, and this study was approved by the institutional review board at Aichi Cancer Center Hospital (approval no. 2023-0-266).

RESULTS

Patient characteristics are summarized in Table 1. Among the 207 patients, 62.8% (130/207) did not require PBD, 27.5% (57/207) underwent EBS, and 9.7% (20/207) underwent primary EUS-HGS as PBD. There were no significant differences between groups in terms of age or sex. Malignant diseases were more common in the EBS and EUS-HGS groups.

Postoperative outcomes are summarized in Table 2. Blood loss was significantly different among the three groups (332.5, 480, and 470 mL in the no biliary drainage, EBS, and primary EUS-HGS groups, respectively; p=0.048). Blood loss was lowest in the non-BD group. The positive rate of intraoperative bile juice culture was significantly higher in the EBS group (7.8% vs. 75.4% vs. 36.8%, p<0.001). However, there was no significant difference in the complication rate following surgery (43.8% vs. 38.6% vs. 40.0%, p=0.784) or length of hospital stay (27 days vs. 23 days vs. 23 days, p=0.160). The overall postoperative mortality was nil. There was no significant difference in the positivity rate of intraoperative peritoneal lavage cytology (5.6% vs. 5.6% vs. 6.7%, p=0.984).

Details of EUS-HGS are presented in Table 3. B2 was punctured in 85.0% (17/20) of patients. Median bile duct diameter was 2.8 mm (range, 2.2–6.0 mm) and procedure time, defined as the time from puncture to stent deployment, was 13.2 min (range, 6.4–29.5 min).

The clinical outcomes of the PBD are shown in Table 4. Early adverse events occurred in 12.3% (7/57) of the EBS group and in none of the EUS-HGS groups (no significant difference, p=0.233). In the EBS group, post-ERCP pancreatitis occurred in 5.3% (3/57) and acute cholecystitis occurred in 5.3% (3/57) of the patients.

Recurrent biliary obstruction (RBO) was assessed according to the 2014 Tokyo criteria.¹⁵ The interval from PBD to surgery was not significantly different between the EBS and EUS-HGS groups (90 vs. 69 days, p=0.171). Among the patients with pancreatic ductal adenocarcinoma, 56.1% in the EBS group and 55.0% in the primary EUS-HGS group received neoadjuvant chemotherapy. The RBO rates were 29.1% and 30.0% (p=0.138) in the EBS and primary EUS-HGS groups, respectively. The Kaplan-Meier curves of the cumulative time to RBO are shown in Figure 2. The log-rank test revealed no significant difference between the two groups (67 vs. 73 days, p=0.298).

DISCUSSION

Biliary drainage, including PBD, is considered the gold standard treatment. Percutaneous biliary drainage (PTBD) was previously performed as an alternative drainage technique when ERCP is difficult or impossible.

In an RCT, Artifon et al.¹⁶ reported no significant differences in technical or clinical success or complication rates between PTBD and EUS-guided choledochoduodenostomy (EUS-CDS). In another RCT, Lee et al.¹⁷ reported that compared with PTBD, EUS-guided biliary drainage (EUS-BD) was associated with fewer adverse events (31.2% vs. 8.8%, p=0.022) and less frequently required unscheduled reinterventions (0.93 vs. 0.34, p=0.02). In that study, EUS-CDS and EUS-HGS were performed for EUS-BD. A systematic review by Sharaiha et al.¹⁸ concluded that, when ERCP fails, EUS-BD may be preferred over PTBD when sufficient advanced endoscopic expertise and logistics are available. EUS-BD is associated with significantly better clinical success, a lower rate of adverse events, and fewer reinterventions than PTBD. Accordingly, EUS-BD is widely used as an alternative to PTBD after failed or impossible ERCP. Furthermore, in recent years, RCTs comparing EUS-BD as primary drainage without attempted ERCP with conventional ERCP have reported comparable efficacy, safety, and avoidance of pancreatitis.¹⁹^-²¹ The reduced risk of pancreatitis is a significant advantage of surgery. However, few studies have performed EUS-BD as PBD (Table 5).²²^-²⁷ Fabbri et al.²² reported three cases of EUS-CDS with a lumen-apposing metal stent (LAMS) as a bridge to surgery following failed ERCP, and Gaujoux et al.²³ reported that performing PD after EUS-CDS with LAMS was technically feasible and resulted in acceptable short-term postoperative outcomes. Although LAMS appears to have a low risk of bile leakage, it is placed after needle puncture in EUS-CDS as a two-step procedure,²⁸ and bile leakage is not completely prevented. Moreover, EUS-CDS interferes with the surgical field of the PD, which is undesirable for preoperative primary drainage. The second disadvantage of EUS-CDS with LAMS as a PBD is the risk of reflux cholangitis and food impaction due to the large caliber of the LAMS.²⁹ Akashi et al.³⁰ reported that preoperative cholangitis significantly increases ascitic bacterial contamination and the incidence of postoperative infectious complications. Darnell et al.³¹ reported that preoperative cholangitis was associated with increased mortality (hazard ratio, 2.67; 95% confidence interval, 1.16–6.13) in patients who successfully completed PD. Appropriate PBD is required to prevent preoperative cholangitis and improve outcomes after PD. Sundaram et al.²⁶ reported 10 cases of bridge-to-surgery after EUS-guided antegrade stenting (EUS-AGS). However, EUS-AGS carries the risk of pancreatitis and interferes with the surgical field.

Unlike other drainage methods, such as EBS, EUS-CDS, and EUS-AGS, EUS-HGS does not interfere with the surgical field. We believe that this is a significant advantage of preoperative EUS-HGS. Furthermore, EUS-HGS can prevent pancreatitis. Therefore, we performed a primary EUS-HGS for preoperative drainage. Mukai et al.²⁵ reported the clinical feasibility of EUS-HGS after failed ERCP for preoperative drainage; however, plastic stents were used in all cases. Plastic stents have a higher risk of bile leakage than metal stents,³² and bile leakage can cause seeding. This is one of the most important considerations when preoperatively performing EUS-BD for primary drainage. We excluded patients with bile duct cancer from the study because of the higher possibility that cancer cells may be present in the bile, and used FCSEMS in almost all cases (95%). Although there was no difference in the positivity rate among the three groups in peritoneal lavage cytology performed at the time of surgery, the long-term follow-up results are unknown. Therefore, a long-term observational follow-up study is required. Furthermore, it may be difficult to perform EUS-HGS in patients without intrahepatic bile duct dilation. ERCP is likely to be performed in these cases. If an attempt at EUS-HGS fails, there is a risk of adverse events, such as bile leakage and peritonitis. Prospective clinical trials are required for further investigations.

Tyberg et al.²⁷ compared EUS-BD after failed ERCP with ERCP before hepaticobiliary surgery and reported that the technical and clinical success rates of surgery were significantly higher in the EUS-BD group than in the ERCP group (97% vs. 83%, p=0.009 and 97.0% vs. 75%, p=0.004, respectively). The authors also found that the total length of hospital stay from surgery to discharge was significantly longer in the ERCP group (19 vs. 10 days, p=0.0082). However, it must be considered that EUS-BD included CDS, HGS and rendezvous, and the type of surgery varied. In the present study, we only considered patients with PD, and blood loss was significantly different among the three groups. This finding could also be influenced by differences in primary disease. There was no significant difference in the rate of adverse events or length of hospital stay between the groups. There were no obvious disadvantages of EUS-HGS; in contrast, the positivity rate of intraoperative bile juice culture was lower than that of EBS. This may be an advantage that contributes to the future surgical outcomes.

This study had several limitations. First, it was retrospective and was performed at a single center. Second, patients with various primary pancreaticobiliary diseases with different backgrounds were included. Third, the long-term outcomes are unknown. Further clinical studies are required to evaluate the efficacy of primary EUS-HGS before PD. However, to the best of our knowledge, this retrospective study is the first to focus on EUS-HGS as a primary drainage technique in preoperative surgery and is specifically limited to patients undergoing PD.

In conclusion, primary EUS-HGS performed before PD demonstrated no early adverse events and lower rates of positive intraoperative bile cultures than did EBS, and no disadvantages were apparent in the postoperative course. These findings suggest the potential to expand the indications for EUS-HGS.

Conflicts of Interest

The authors have no potential conflicts of interest.

Funding

None.

Author Contributions

Conceptualization: NO, KH; Data curation: NO; Formal analysis: NO; Investigation: NO; Methodology: KH; Project administration: KH, YS; Resources: NO, SN, MO, SH, TA, TK, HK; Supervision: KH, YS; Validation: SH, TK; Visualization: NO; Writing–original draft: NO; Writing–review & editing: all authors.

Fig. 1.

Flowchart of patients who underwent pancreatoduodenectomy at our institution, excluding those with bile duct cancer. ^a)Excluding patients with bile duct cancer. ^b)Converted from endoscopic biliary stenting (EBS) to endoscopic ultrasound-guided hepaticogastrostomy (EUS-HGS). PTBD, percutaneous biliary drainage.

Fig. 2.

Kaplan-Meier curves for time to biliary obstruction in endoscopic biliary stenting (EBS) (solid line) and endoscopic ultrasound-guided hepaticogastrostomy (EUS-HGS) (broken line).

Table 1.

Patient characteristics

Characteristic	Without BD (n=130, 62.8%)	EBS (n=57, 27.5%)	EUS-HGS (n=20, 9.7%)	p-value^a)
Age (yr)^a)	69 (35–83)	70 (32–91)	69.5 (49–82)	0.854
Male	74 (56.9)	37 (64.9)	10 (50.0)	0.428
Primary disease				<0.001
PDAC	44 (33.8)	52 (91.2)	13 (65.0)
IPMN	29 (22.3)	1 (1.8)	0 (0)
IPMC	18 (13.8)	0 (0)	1 (5.0)
Other pancreatic tumors	16 (12.3)	2 (3.5)	0 (0)
Duodenal cancer	9 (6.9)	0 (0)	2 (10.0)
Ampullar of Vater cancer	8 (6.2)	2 (3.5)	2 (10.0)
Duodenal NET	4 (3.1)	0 (0)	0 (0)
Other	2 (1.5)	0 (0)	2 (10.0)

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

BD, biliary drainage; EBS, endoscopic biliary stenting; EUS-HGS, endoscopic ultrasound-guided hepaticogastrostomy; PDAC, pancreatic ductal adenocarcinoma; IPMN, intraductal papillary mucinous neoplasm; IPMC, intraductal papillary mucinous carcinoma; NET, neuroendocrine tumor.

^a)Chi-square test, Mann-Whitney U-test.

Table 2.

Postoperative outcomes

Outcome	Without BD (n=130)	EBS (n=57)	EUS-HGS (n=20)	p-value^a)
Operative time (min)	397 (248–665)	407 (297–705)	398 (221–576)	0.629
Blood loss (mL)	332.5 (30–5,920)	480 (75–3,440)	470 (30–1,390)	0.048
Positive rate of intraoperative bile juice culture	10/129 (7.8)	43/57 (75.4)	7/19 (36.8)	<0.001
Complication following surgery (Clavien-Dindo>3)	57/130 (43.8)	22/57 (38.6)	8/20 (40.0)	0.784
Pancreatic fistula (Clavien-Dindo>3)	49/130 (37.7)	19/57 (33.3)	5/20 (25.0)	0.508
Bile leakage (Clavien-Dindo>3)	9/130 (6.9)	0/57 (0)	0/20 (0)	0.061
Length of stay (d)	27 (10–134)	23 (7–56)	23 (12–47)	0.160
Intraoperative peritoneal lavage cytology	3/54 (5.6)	3/54 (5.6)	1/15 (6.7)	0.984

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

BD, biliary drainage; EBS, endoscopic biliary stenting; EUS-HGS, endoscopic ultrasound-guided hepaticogastrostomy.

^a)Chi-square test, Mann-Whitney U-test.

Table 3.

Details of endoscopic ultrasound-guided hepaticogastrostomy

	Value (n=20)
Puncture site
B2	17 (85.0)
B3	3 (15.0)
Bile duct diameter (mm)	2.8 (2.2–6.0)
Procedure time (min)	13.2 (6.4–29.5)
Stent
Plastic stent	1 (5.0)
Fully covered self-expandable stent	19 (95.0)

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

Table 4.

Clinical outcomes of preoperative biliary drainage

Outcome	EBS (n=57)	EUS-HGS (n=20)	p-value^a)
Early adverse events (≤14 days)	7 (12.3)	0 (0)	0.233
Post-ERCP pancreatitis	3 (5.3) (mild 3)	0 (0)	0.707
Acute cholecystitis	3 (5.3) (moderate 3)	0 (0)	0.707
Bile duct perforation	1 (1.8) (moderate 1)	0 (0)	0.251
Bleeding	0 (0)	0 (0)
Interval period (days)^b)	90 (19–714)	69 (14–321)	0.171
Neoadjuvant chemotherapy	32 (56.1)	11 (55.0)	0.929
RBO before surgery	28 (29.1)	6 (30.0)	0.138

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

EBS, endoscopic biliary stenting; EUS-HGS, endoscopic ultrasound-guided hepaticogastrostomy; ERCP, endoscopic retrograde cholangiopancreatography; RBO, recurrent biliary obstruction.

^a)Chi-square test, Mann-Whitney U-test, log-rank test;

^b)interval period: between preoperative drainage and surgery.

Table 5.

Summary of studies/case reports on EUS-BD for preoperative biliary drainage

Study	Year	Patient	Modality of EUS-BD	Reason for EUS-BD	Stent	Adverse events after EUS-BD	Surgical procedure	Mortality after surgery
Fabbri et al.²²	2019	5	EUS-CDS 5	Failed ERCP	LAMS	0/5 (0)	PPPD 5	1/5 (20.0)
Gaujoux et al.²³	2020	21	EUS-CDS 21	Failed ERCP 14, MDPTB decision 7	LAMS	0/21 (0)	PD 21	0/21 (0)
Koutlas et al.²⁴	2022	3	EUS-HGS 3	Failed ERCP 3	FCSEMS and PS	0/3 (0)	PD 3	0/3 (0)
Mukai et al.²⁵	2022	15	EUS-HGS 13, EUS-HDS 1, EUS-AGS+HGS 1	Failed ERCP 15	PS	1/15 (6.7), bile peritonitis	PD 13, hepatectomy 2	0/15 (0)
Sundaram et al.²⁶	2023	10	EUS-AGS 10	Failed ERCP, etc.	UCSEMS	2/10 (20.0), cholecystitis, pneumoperitoneum	PPPD 10	1/10 (10.0)
Tyberg et al.²⁷	2023	58	EUS-HGS 29, EUS-CDS 24, transpapillary via RDV 5	Failed ERCP 56	N/A	10/56 (17.5), bleeding 4, biloma 3, stent dislodgement 2, infection 1	PD 41, hepatectomy 7, etc.	N/A
Present study	2023	20	EUS-HGS	Primary	FCSEMS 18, PS 2	0/20 (0)	PD 20	0/20 (0)

Values are presented as number only or number/total number (%).

EUS, endoscopic ultrasound; EUS-BD, EUS-guided biliary drainage; EUS-CDS, EUS-guided choledochoduodenostomy; ERCP, endoscopic retrograde cholangiopancreatography; LAMS, lumen-apposing metal stent; PPPD, pylorus-preserving pancreatoduodenectomy; MDPTB, multidisciplinary pancreatic tumor board; PD, pancreatoduodenectomy; EUS-HGS, EUS-guided hepaticogastrostomy; FCSEMS, fully covered self-expandable stent; EUS-HDS, EUS-guided hepaticoduodenostomy; EUS-AGS, EUS-guided antegrade stenting; PS, plastic stent; UCSEMS, uncovered self-expandable stent; RDV, rendezvous technique; N/A, not applicable.

REFERENCES

1. van der Gaag NA, Rauws EA, van Eijck CH, et al. Preoperative biliary drainage for cancer of the head of the pancreas. N Engl J Med 2010;362:129–137.Article PubMed
2. Gao Z, Wang J, Shen S, et al. The impact of preoperative biliary drainage on postoperative outcomes in patients with malignant obstructive jaundice: a retrospective analysis of 290 consecutive cases at a single medical center. World J Surg Oncol 2022;20:7.Article PubMed PMC PDF
3. Matsumoto K, Noma H, Fujita K, et al. Prognostic factors for severe-to-fatal post-endoscopic retrograde cholangiopancreatography pancreatitis: a multicenter prospective cohort study. J Clin Med 2024;13:1135.Article PubMed PMC
4. Park DH, Jang JW, Lee SS, et al. EUS-guided biliary drainage with transluminal stenting after failed ERCP: predictors of adverse events and long-term results. Gastrointest Endosc 2011;74:1276–1284.Article PubMed
5. 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
6. 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
7. Paik WH, Park DH. Outcomes and limitations: EUS-guided hepaticogastrostomy. Endosc Ultrasound 2019;8:S44–S49.Article PubMed PMC
8. Okuno N, Hara K, Mizuno N, et al. B2 puncture with forward-viewing EUS simplifies EUS-guided hepaticogastrostomy (with video). Endosc Ultrasound 2022;11:319–324.Article PubMed PMC
9. Ishikawa S, Hara K, Okuno N, et al. Safety and efficacy of novel oblique-viewing scope for B2-endoscopic ultrasound-guided hepaticogastrostomy. Clin Endosc 2024;57:527–533.Article PubMed PMC PDF
10. Okuno N, Hara K, Mizuno N, et al. Risks of transesophageal endoscopic ultrasonography-guided biliary drainage. Gastrointest Interv 2017;6:82–84.Article
11. Okuno N, Hara K, Mizuno N, et al. Stent migration into the peritoneal cavity following endoscopic ultrasound-guided hepaticogastrostomy. Endoscopy 2015;47 Suppl 1 UCTN:E311.Article PubMed
12. Fujisawa T, Isayama H, Ishii S. "ClipFlap" anchoring method for endoscopic ultrasonography-guided hepaticogastrostomy with a covered self-expandable metallic stent. Dig Endosc 2020;32:628.Article PubMed PDF
13. Cotton PB, Eisen GM, Aabakken L, et al. A lexicon for endoscopic adverse events: report of an ASGE workshop. Gastrointest Endosc 2010;71:446–454.Article PubMed
14. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240:205–213.Article PubMed PMC
15. Isayama H, Hamada T, Yasuda I, et al. TOKYO criteria 2014 for transpapillary biliary stenting. Dig Endosc 2015;27:259–264.Article PubMed
16. Artifon EL, Aparicio D, Paione JB, et al. Biliary drainage in patients with unresectable, malignant obstruction where ERCP fails: endoscopic ultrasonography-guided choledochoduodenostomy versus percutaneous drainage. J Clin Gastroenterol 2012;46:768–774.Article PubMed
17. Lee TH, Choi JH, Park do H, et al. Similar efficacies of endoscopic ultrasound-guided transmural and percutaneous drainage for malignant distal biliary obstruction. Clin Gastroenterol Hepatol 2016;14:1011–1019.Article PubMed
18. Sharaiha RZ, Khan MA, Kamal F, et al. Efficacy and safety of EUS-guided biliary drainage in comparison with percutaneous biliary drainage when ERCP fails: a systematic review and meta-analysis. Gastrointest Endosc 2017;85:904–914.Article PubMed
19. Bang JY, Navaneethan U, Hasan M, et al. Stent placement by EUS or ERCP for primary biliary decompression in pancreatic cancer: a randomized trial (with videos). Gastrointest Endosc 2018;88:9–17.Article PubMed
20. Paik WH, Lee TH, Park DH, et al. EUS-guided biliary drainage versus ERCP for the primary palliation of malignant biliary obstruction: a multicenter randomized clinical trial. Am J Gastroenterol 2018;113:987–997.Article PubMed PDF
21. Park JK, Woo YS, Noh DH, et al. Efficacy of EUS-guided and ERCP-guided biliary drainage for malignant biliary obstruction: prospective randomized controlled study. Gastrointest Endosc 2018;88:277–282.Article PubMed
22. Fabbri C, Fugazza A, Binda C, et al. Beyond palliation: using EUS-guided choledochoduodenostomy with a lumen-apposing metal stent as a bridge to surgery. A case series. J Gastrointestin Liver Dis 2019;28:125–128.Article PubMed
23. Gaujoux S, Jacques J, Bourdariat R, et al. Pancreaticoduodenectomy following endoscopic ultrasound-guided choledochoduodenostomy with electrocautery-enhanced lumen-apposing stents an ACHBT: SFED study. HPB (Oxford) 2021;23:154–160.Article PubMed
24. Koutlas NJ, LePage EM, Lucioni T, et al. Preoperative endoscopic ultrasound-guided hepaticogastrostomy facilitates decompression and diagnosis in patients with suspected malignant biliary obstruction: a case series. Cureus 2022;14:e23209.Article PubMed PMC
25. Mukai S, Itoi T, Tsuchiya T, et al. Clinical feasibility of endoscopic ultrasound-guided biliary drainage for preoperative management of malignant biliary obstruction (with videos). J Hepatobiliary Pancreat Sci 2023;30:983–992.Article PubMed PDF
26. Sundaram S, Mane K, Patil P, et al. Endoscopic ultrasound-guided antegrade stent placement in patients with failed ERCP as a modality of preoperative and palliative biliary drainage. Dig Dis Sci 2023;68:1551–1558.Article PubMed PDF
27. Tyberg A, Sarkar A, Shahid HM, et al. EUS-guided biliary drainage versus ERCP in malignant biliary obstruction before hepatobiliary surgery: an international multicenter comparative study. J Clin Gastroenterol 2023;57:962–966.Article PubMed
28. Jacques J, Privat J, Pinard F, et al. Endoscopic ultrasound-guided choledochoduodenostomy with electrocautery-enhanced lumen-apposing stents: a retrospective analysis. Endoscopy 2019;51:540–547.Article PubMed
29. Tsuchiya T, Teoh AY, Itoi T, et al. Long-term outcomes of EUS-guided choledochoduodenostomy using a lumen-apposing metal stent for malignant distal biliary obstruction: a prospective multicenter study. Gastrointest Endosc 2018;87:1138–1146.Article PubMed
30. Akashi M, Nagakawa Y, Hosokawa Y, et al. Preoperative cholangitis is associated with increased surgical site infection following pancreaticoduodenectomy. J Hepatobiliary Pancreat Sci 2020;27:640–647.Article PubMed PDF
31. Darnell EP, Wang TJ, Lumish MA, et al. Preoperative cholangitis is an independent risk factor for mortality in patients after pancreatoduodenectomy for pancreatic cancer. Am J Surg 2021;221:134–140.Article PubMed
32. Kawakubo K, Isayama H, Kato H, et al. Multicenter retrospective study of endoscopic ultrasound-guided biliary drainage for malignant biliary obstruction in Japan. J Hepatobiliary Pancreat Sci 2014;21:328–334.Article PubMed

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Primary endoscopic ultrasound-guided hepaticogastrostomy for biliary drainage prior to pancreatoduodenectomy: a retrospective study in Japan

Clin Endosc. 2025;58(4):604-611. Published online February 11, 2025

DOI: https://doi.org/10.5946/ce.2024.218

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Primary endoscopic ultrasound-guided hepaticogastrostomy for biliary drainage prior to pancreatoduodenectomy: a retrospective study in Japan

Fig. 1. Flowchart of patients who underwent pancreatoduodenectomy at our institution, excluding those with bile duct cancer. a)Excluding patients with bile duct cancer. b)Converted from endoscopic biliary stenting (EBS) to endoscopic ultrasound-guided hepaticogastrostomy (EUS-HGS). PTBD, percutaneous biliary drainage.

Fig. 2. Kaplan-Meier curves for time to biliary obstruction in endoscopic biliary stenting (EBS) (solid line) and endoscopic ultrasound-guided hepaticogastrostomy (EUS-HGS) (broken line).

Graphical abstract

Fig. 1.

Fig. 2.

Graphical abstract

Primary endoscopic ultrasound-guided hepaticogastrostomy for biliary drainage prior to pancreatoduodenectomy: a retrospective study in Japan

Characteristic	Without BD (n=130, 62.8%)	EBS (n=57, 27.5%)	EUS-HGS (n=20, 9.7%)	p-value^a)
Age (yr)^a)	69 (35–83)	70 (32–91)	69.5 (49–82)	0.854
Male	74 (56.9)	37 (64.9)	10 (50.0)	0.428
Primary disease				<0.001
PDAC	44 (33.8)	52 (91.2)	13 (65.0)
IPMN	29 (22.3)	1 (1.8)	0 (0)
IPMC	18 (13.8)	0 (0)	1 (5.0)
Other pancreatic tumors	16 (12.3)	2 (3.5)	0 (0)
Duodenal cancer	9 (6.9)	0 (0)	2 (10.0)
Ampullar of Vater cancer	8 (6.2)	2 (3.5)	2 (10.0)
Duodenal NET	4 (3.1)	0 (0)	0 (0)
Other	2 (1.5)	0 (0)	2 (10.0)

Outcome	Without BD (n=130)	EBS (n=57)	EUS-HGS (n=20)	p-value^a)
Operative time (min)	397 (248–665)	407 (297–705)	398 (221–576)	0.629
Blood loss (mL)	332.5 (30–5,920)	480 (75–3,440)	470 (30–1,390)	0.048
Positive rate of intraoperative bile juice culture	10/129 (7.8)	43/57 (75.4)	7/19 (36.8)	<0.001
Complication following surgery (Clavien-Dindo>3)	57/130 (43.8)	22/57 (38.6)	8/20 (40.0)	0.784
Pancreatic fistula (Clavien-Dindo>3)	49/130 (37.7)	19/57 (33.3)	5/20 (25.0)	0.508
Bile leakage (Clavien-Dindo>3)	9/130 (6.9)	0/57 (0)	0/20 (0)	0.061
Length of stay (d)	27 (10–134)	23 (7–56)	23 (12–47)	0.160
Intraoperative peritoneal lavage cytology	3/54 (5.6)	3/54 (5.6)	1/15 (6.7)	0.984

	Value (n=20)
Puncture site
B2	17 (85.0)
B3	3 (15.0)
Bile duct diameter (mm)	2.8 (2.2–6.0)
Procedure time (min)	13.2 (6.4–29.5)
Stent
Plastic stent	1 (5.0)
Fully covered self-expandable stent	19 (95.0)

Outcome	EBS (n=57)	EUS-HGS (n=20)	p-value^a)
Early adverse events (≤14 days)	7 (12.3)	0 (0)	0.233
Post-ERCP pancreatitis	3 (5.3) (mild 3)	0 (0)	0.707
Acute cholecystitis	3 (5.3) (moderate 3)	0 (0)	0.707
Bile duct perforation	1 (1.8) (moderate 1)	0 (0)	0.251
Bleeding	0 (0)	0 (0)
Interval period (days)^b)	90 (19–714)	69 (14–321)	0.171
Neoadjuvant chemotherapy	32 (56.1)	11 (55.0)	0.929
RBO before surgery	28 (29.1)	6 (30.0)	0.138

Study	Year	Patient	Modality of EUS-BD	Reason for EUS-BD	Stent	Adverse events after EUS-BD	Surgical procedure	Mortality after surgery
Fabbri et al.22	2019	5	EUS-CDS 5	Failed ERCP	LAMS	0/5 (0)	PPPD 5	1/5 (20.0)
Gaujoux et al.23	2020	21	EUS-CDS 21	Failed ERCP 14, MDPTB decision 7	LAMS	0/21 (0)	PD 21	0/21 (0)
Koutlas et al.24	2022	3	EUS-HGS 3	Failed ERCP 3	FCSEMS and PS	0/3 (0)	PD 3	0/3 (0)
Mukai et al.25	2022	15	EUS-HGS 13, EUS-HDS 1, EUS-AGS+HGS 1	Failed ERCP 15	PS	1/15 (6.7), bile peritonitis	PD 13, hepatectomy 2	0/15 (0)
Sundaram et al.26	2023	10	EUS-AGS 10	Failed ERCP, etc.	UCSEMS	2/10 (20.0), cholecystitis, pneumoperitoneum	PPPD 10	1/10 (10.0)
Tyberg et al.27	2023	58	EUS-HGS 29, EUS-CDS 24, transpapillary via RDV 5	Failed ERCP 56	N/A	10/56 (17.5), bleeding 4, biloma 3, stent dislodgement 2, infection 1	PD 41, hepatectomy 7, etc.	N/A
Present study	2023	20	EUS-HGS	Primary	FCSEMS 18, PS 2	0/20 (0)	PD 20	0/20 (0)

Table 1. Patient characteristics

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

Chi-square test, Mann-Whitney U-test.

Table 2. Postoperative outcomes

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

BD, biliary drainage; EBS, endoscopic biliary stenting; EUS-HGS, endoscopic ultrasound-guided hepaticogastrostomy.

Chi-square test, Mann-Whitney U-test.

Table 3. Details of endoscopic ultrasound-guided hepaticogastrostomy

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

Table 4. Clinical outcomes of preoperative biliary drainage

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

EBS, endoscopic biliary stenting; EUS-HGS, endoscopic ultrasound-guided hepaticogastrostomy; ERCP, endoscopic retrograde cholangiopancreatography; RBO, recurrent biliary obstruction.

Chi-square test, Mann-Whitney U-test, log-rank test;

interval period: between preoperative drainage and surgery.

Table 5. Summary of studies/case reports on EUS-BD for preoperative biliary drainage