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

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Clin Endosc. 2024;.ce.2024.218

Publication date (electronic) : 2024 November 1

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

Nozomi Okuno¹, Kazuo Hara^,1, Seiji Natsume², Masataka Okuno², Shin Haba¹, Tomonari Asano², Takamichi Kuwahara¹, Hiroki Koda¹, Yasuhiro Shimizu²

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 2024 August 18; Revised 2024 September 15; Accepted 2024 September 16.

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 cancer1 reported that PBD for curative surgery could increase adverse biliary events. 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).

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.

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.

Table 1.

Patient characteristics

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).

Table 2.

Postoperative outcomes

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).

Table 3.

Details of endoscopic ultrasound-guided hepaticogastrostomy

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.

Table 4.

Clinical outcomes of preoperative biliary drainage

Recurrent biliary obstruction (RBO) was assessed according to the 2014 Tokyo criteria.15 The interval from PBD to surgery (90 vs. 69 days, p=0.171) was not significantly different between the EBS and EUS-HGS groups. 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).

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).

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-CDS28 as a two-step procedure, 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.

Table 5.

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

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.

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