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Focused Review Series: Expanding Indication: Interventional Endoscopic Management for Pancreaticobiliary Diseases Endoscopic Ultrasound-Guided Biliary Drainage for Unresectable Hilar Malignant Biliary Obstruction
Yousuke Nakai1,orcid, Hirofumi Kogure1, Hiroyuki Isayama1,2, Kazuhiko Koike1
Clinical Endoscopy 2019;52(3):220-225.
DOI: https://doi.org/10.5946/ce.2018.094
Published online: November 29, 2018

1Department of Gastroenterology, Graduate School of Medicine, The University of Tokyo, Japan

2Department of Gastroenterology, Graduate School of Medicine, Juntendo University, Tokyo, Japan

Correspondence: Yousuke Nakai Department of Gastroenterology, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo Bunkyo-ku, Tokyo 113-8655, Japan Tel: +81-3-3815-5411, Fax: +81-3-5800-9801, E-mail: ynakai-tky@umin.ac.jp
• Received: June 1, 2018   • Revised: June 26, 2018   • Accepted: June 27, 2018

Copyright © 2019 Korean Society of Gastrointestinal Endoscopy

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • Endoscopic transpapillary biliary drainage is the current standard of care for unresectable hilar malignant biliary obstruction (MBO) and bilateral metal stent placement is shown to have longer patency. However, technical and clinical failure is possible and percutaneous transhepatic biliary drainage (PTBD) is sometimes necessary. Endoscopic ultrasound-guided biliary drainage (EUS-BD) is increasingly being reported as an alternative rescue procedure to PTBD. EUS-BD has a potential advantage of not traversing the biliary stricture and internal drainage can be completed in a single session. Some approaches to bilateral biliary drainage for hilar MBO under EUS-guidance include a bridging method, hepaticoduodenostomy, and a combination of EUS-BD and transpapillary biliary drainage. The aim of this review is to summarize data on EUS-BD for hilar MBO and to clarify its advantages over the conventional approaches such as endoscopic transpapillary biliary drainage and PTBD.
Patients with hilar malignant biliary obstruction (MBO) often present at an unresectable stage. Endoscopic transpapillary biliary drainage (EBD) is the current standard of care to relieve jaundice. Multiple metallic stent (MS) placement is often performed but is technically demanding and percutaneous transhepatic biliary drainage (PTBD) is sometimes needed after technical or clinical failure by endoscopic approach [1].
Endoscopic ultrasound-guided biliary drainage (EUSBD) for MBO is being increasingly reported but is mostly performed for distal MBO and only by experts [2,3]. Since it has the potential advantage of not traversing the biliary stricture, it may play a role in the management of hilar MBO as well [4]. However, data on EUS-BD for hilar MBO are still limited. In this review article, we will overview EUS-BD for hilar MBO.
In unresectable hilar MBO, biliary drainage can be achieved either by EBD or PTBD. Although a systematic review [5] showed a better success rate of PTBD, EBD is the current standard of care because PTBD impairs the quality of life in general whereas EBD does not. There are some options for endoscopic management of hilar MBO: Plastic stent (PS) vs. MS [6,7] and unilateral vs. bilateral stenting [8,9].
MS is shown to have longer stent patency than PS in randomized controlled trials (RCTs) [6,7]. Some reports have demonstrated the association of liver volume with adequate biliary drainage. One study [10] showed that 33% of the liver volume should be drained in cases that have preserved liver function to obtain adequate biliary drainage, whereas 50% of the liver volume should be drained in those with impaired liver function. In another study, longer survival rates were observed in cases of hilar MBO after draining ≥50% of the liver volume [11]. To drain ≥50% the liver volume, bilateral biliary drainage is necessary in most cases. A recent Korean RCT [12] clearly demonstrated the superiority of bilateral MS placement over unilateral MS placement. Bilateral MS placement showed a longer duration of stent patency (252 days vs. 139 days, p<0.01) and statistically non-significant but clinically significant differences in survival (270 days vs. 178 days, p=0.053).
The recent development of MS suitable for hilar stenting via a thin delivery system allows easy bilateral stent placement, either by using a stent-in-stent method [13,14] or a sideby-side method [15]. These MS also allow re-interventions after recurrent biliary obstruction (RBO) following bilateral stent placement [16]; nevertheless, the procedure can be technically difficult or even impossible. When endoscopic re-intervention fails, PTBD may be necessary to relieve jaundice or cholangitis, which impairs the quality of life due to the indwelling drainage tube. Technical and clinical hurdles of transpapillary multiple MS placement for hilar MBO are caused by the complexity of the stent configuration at the hepatic hilum. To overcome the limitations of conventional approaches such as EBD and/or PTBD, another novel approach for hilar MBO has been long awaited.
EUS-BD is being increasingly utilized in the management of MBO in cases of failed or difficult endoscopic retrograde cholangiopancreatography (ERCP). In addition to obtaining biliary access after failed ERCP, EUS-BD does not traverse the biliary stricture, which may provide an advantage in the management of hilar MBO. There are two approaches used by EUS-BD, intrahepatic and extrahepatic, but the intrahepatic approach is mandatory for hilar MBO.
Indications and contraindications of EUS-BD for hilar MBO are shown in Table 1. Theoretically, EUS-BD can be indicated for any hilar MBO but the current indications are failed ERCP, surgically altered anatomy, and failed re-interventions for occlusion of transpapillary placed stents. Contraindications are severe coagulopathy, massive ascites, intervening vessels, and unstable conditions unfit for endoscopic procedures. In such cases, EUS-BD might have higher risks of morbidity or mortality due to complications such as bleeding, bile leak, and stent migration. Furthermore, despite reports of a high technical success rate and acceptable adverse event rate, expertise is necessary for EUS-BD as dedicated devices for EUS-BD are currently limited.
EUS-guided hepaticogastrostomy (EUS-HGS) is one of the most common EUS-BD procedures via an intrahepatic approach [17]. In EUS-HGS, biliary access to segment 2 or 3 is established via the cardia or lesser curvature of the stomach under EUS guidance, and a stent is placed from B2 or B3 to the stomach. In hilar MBO, therefore, biliary drainage of the left biliary system alone is achieved by EUS-HGS, leaving the right biliary system undrained with potential risks of inadequate biliary drainage or segmental cholangitis.
As shown in transpapillary stenting, bilateral drainage can potentially lead to better clinical outcomes for hilar MBO. The approaches to obtain bilateral drainage with EUS-BD include a bridging method, EUS-guided hepaticoduodenostomy (EUS-HDS), and a combined EUS and ERCP approach (Fig. 1).
The bridging method [18] employs a left intrahepatic bile duct (IHBD) access similar to conventional EUS-HGS. After obtaining biliary access from the stomach to the left IHBD using a 19-gauge fine needle aspiration needle and a guidewire, the needle is replaced by a standard catheter and a guidewire is advanced through the hilar stricture into the right IHBD. In difficult cases, a steerable catheter and a hydrophilic guidewire are helpful to pass the hilar stricture. An uncovered bridging MS with a thin delivery system is placed across the hilar stricture, followed by a covered MS placement from the left IHBD to the stomach, as seen with conventional EUS-HGS. During this bridging method, guidewire passage or stent deployment to the right biliary system through the hilar stricture can be technically challenging depending on the angle of left and right hepatic duct confluence. In technically difficult cases, a prolonged procedure time can increase the risk of bile leak and sequential bridging stent placement can be an option. A conventional HGS stent is placed in the left IHBD in the first session and after fistula maturation of the HGS, a bridging stent placement can be attempted by cannulating through the HGS stent (Fig. 2).
EUS-HDS [18,19] employs a right IHBD access from the duodenum, which is a complement of EUS-HGS to the left IHBD. However, EUS-HDS procedures are performed only in a few expert centers and therefore, reports are limited. Ogura et al. [18] reported a locking method with a combination of uncovered and covered MSs to prevent stent migration but the use of a PS dedicated to EUS-BD [20] was also reported. Given the limited number of reports, the best technique of EUS-HDS has not been established thus far.
In high-grade hilar MBO, a combined EUS and ERCP approach proposed by Park [21] can be a treatment option. In this approach, EUS-HGS to the left IHBD and transpapillary stenting to the right IHBD are performed (Fig. 3). This approach is feasible due to two anatomical reasons. First, as observed with resectable hilar MBO, the left hepatic duct is longer than the right hepatic duct, allowing drainage of the whole left biliary system by a single EUS-HGS stent. Second, the right IHBD is more prone to cancer invasion especially in cases with gallbladder cancer, necessitating multiple stenting of the right biliary system. Although multiple stenting in EUS-BD is theoretically possible, transpapillary multiple stent placement is more established. Therefore, a combination of simple EUS-HGS in the left IHBD and multiple stenting in the right IHBD can achieve >50% biliary drainage with technical feasibility.
Table 2 summarized data on EUS-BD for hilar MBO [18-20,22-29]. The overall technical success rate was 98% and the overall adverse event rate was 8%. However, the overall clinical success rate was 77%, which was lower than previously reported in a systematic review of EUS-BD [30]. Clinical outcomes were comparable between the initial EUS-BD procedure and the rescue EUS-BD procedure after failed transpapillary drainage. However, the number of cases was too small and the procedures were performed only by experts. Therefore, publication bias was possible especially with respect to adverse events. A relatively low clinical success rate suggests that appropriate biliary drainage for unresectable hilar MBO is difficult in any approach: ERCP, EUS, or PTBD. The available literature was focused on short-term outcomes and long-term outcomes such as RBO and its re-interventions were not investigated. Future studies should be focused on patient selection or on treatment selection for better management of hilar MBO.
Transpapillary stenting is still the standard of care for unresectable hilar MBO, and PTBD is often a rescue procedure for failed endoscopic management. As described above, EUS-BD has a definite role in the management of hilar MBO. The advantages and disadvantages are summarized in Table 3. Overall, EUS-BD has a common advantage of both transpapillary stenting and PTBD, namely, a single session internal drainage without crossing the biliary stricture. Internal drainage maintains the quality of life and drainage without crossing the stricture potentially allows longer stent patency.
First of all, the number of reported cases is small. Although the rate of technical success is high, most studies were reported by experts and publication bias may exist. Theoretically, EUS-BD provides better stent patency but long-term outcomes are unclear. Given the improved survival in cases of biliary malignancy, many patients with unresectable hilar MBO need re-intervention for RBO. Endoscopic re-interventions through the EUS-BD route are often possible but PTBD is sometimes necessary to control cholangitis after complex biliary drainage procedures. In addition, the rate of adverse events was only 8% in our review but the intrahepatic approach reportedly had a higher adverse event rate compared to the extrahepatic approach [31]. Finally, technical expertise for performing EUS-BD is not always available in most centers. In such situations, if urgent drainage for cholangitis is necessary, a PTBD can be temporarily placed and conversion from PTBD to EUS-BD can be performed at a later stage [32]. Overall, the evidence regarding these issues is limited and further investigation is warranted.
In conclusion, EUS-BD can be a promising treatment option for unresectable hilar MBO, both as the initial and the rescue procedure. Standardization of procedures as well as development of dedicated devices are necessary to establish the role of EUS-BD in the management of hilar MBO. Future RCTs comparing EUS-BD with EBD or PTBD are warranted to confirm the role of EUS-BD for managing hilar MBO.

Conflicts of Interest:The authors have no financial conflicts of interest.

Fig. 1.
Techniques of bilateral endoscopic ultrasound-guided biliary drainage. (A) Bridging method. (B) Endoscopic ultrasound-guided hepaticoduodenostomy. (C) Combined endoscopic ultrasound-guided hepaticogastrostomy and transpapillary stenting.
ce-2018-094f1.jpg
Fig. 2.
Bridging method. (A) Endoscopic ultrasound-guided hepaticogastrostomy was performed during the first session. (B) A bridging stent was placed during the second session.
ce-2018-094f2.jpg
Fig. 3.
Combined endoscopic ultrasound-guided hepaticogastrostomy and transpapillary stenting. (A) Endoscopic ultrasound-guided hepaticogastrostomy was performed during the first session. (B) Transpapillary multiple stent-in-stent placement was performed during the second session.
ce-2018-094f3.jpg
Table 1.
Current Indications and Contraindications of Endoscopic Ultrasound-Guided Biliary Drainage for Hilar Malignant Biliary Obstruction
Indications
 Failed ERCP
 Surgically altered anatomy i.e., Roux-en-Y reconstruction
 Failed re-intervention for transpapillary stent occlusion
Contraindications
 Severe coagulopathy
 Massive ascites
 Intervening vessels including collateral vessels
 Unstable conditions unfit for endoscopic procedures

ERCP, endoscopic retrograde cholangiopancreatography.

Table 2.
Data on Endoscopic Ultrasound-Guided Biliary Drainage for Hilar Malignant Biliary Obstruction
Study n Initial/rescue Stent Drainage method Technical success Clinical success Adverse events
Bories et al. (2007) [22] 4 Initial PS HGS 4 4 1 stent clogging
Ogura et al. (2014) [23] 1 Initial UMS+CMS Bridging 1 N/A N/A
Ogura et al. (2015) [18] 11 Initial/Rescue UMS+CMS 4 HDS, 7 Bridging 11 N/A 0
Prachayakul et al. (2015) [24] 1 Initial UMS+CMS Bridging 1 1 0
Moryoussef et al. (2017) [25] 18 Initial UMS+CMS 14 HGS, 3 Bridging 17 13 3
Park et al. (2010) [26] 3 Rescue CMS HGS 3 3 0
Park et al. (2013) [19] 2 Rescue CMS HDS 2 2 0
Minaga et al. (2017) [27] 30 Rescue CMS or PS 28 HGS, 2 HDS 29 22 3 bile peritonitis
Ogura et al. (2017) [28] 10 Rescue CMS 8 HGS, 2 HDS 10 9 0
Kanno et al. (2017) [29] 7 Rescue CMS HGS 7 4 0
Mukai et al. (2017) [20] 1 Rescue PS HDS 1 N/A 0
Overall 88 98% (86/88) 77% (58/75) 8% (7/87)

CMS, covered metal stent; HDS, hepaticoduodenostomy; HGS, hepaticogastrostomy; N/A, not available; PS, plastic stent; UMS, uncovered metal stent.

Table 3.
Advantages and Disadvantages of EUS-BD
EUS-BD EBD PTBD
Advantage A single step internal drainage Long term data available High technical success rate
Simplicity at the hilum: possible longer patency Possible tube rinse for clogging
Disadvantage No long term data Technical difficulty for multiple stenting Impaired QOL
Special technique necessary for right IHBD approach Complexity at the hilum High AE rate and re-intervention rate
Contraindications: ascites, coagulopathy Chance of Post-ERCP pancreatitis Contraindications: ascites, coagulopathy
Chance of bile leak, stent migration

AE, adverse event; EBD, endoscopic transpapillary biliary drainage; ERCP, endoscopic retrograde cholangiopancreatography; EUS-BD, endoscopic ultrasound-guided biliary drainage; IHBD, intrahepatic bile duct; PTBD, percutaneous transhepatic biliary drainage; QOL, quality of life.

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      Endoscopic Ultrasound-Guided Biliary Drainage for Unresectable Hilar Malignant Biliary Obstruction
      Clin Endosc. 2019;52(3):220-225.   Published online November 29, 2018
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    Endoscopic Ultrasound-Guided Biliary Drainage for Unresectable Hilar Malignant Biliary Obstruction
    Image Image Image
    Fig. 1. Techniques of bilateral endoscopic ultrasound-guided biliary drainage. (A) Bridging method. (B) Endoscopic ultrasound-guided hepaticoduodenostomy. (C) Combined endoscopic ultrasound-guided hepaticogastrostomy and transpapillary stenting.
    Fig. 2. Bridging method. (A) Endoscopic ultrasound-guided hepaticogastrostomy was performed during the first session. (B) A bridging stent was placed during the second session.
    Fig. 3. Combined endoscopic ultrasound-guided hepaticogastrostomy and transpapillary stenting. (A) Endoscopic ultrasound-guided hepaticogastrostomy was performed during the first session. (B) Transpapillary multiple stent-in-stent placement was performed during the second session.
    Endoscopic Ultrasound-Guided Biliary Drainage for Unresectable Hilar Malignant Biliary Obstruction
    Indications
     Failed ERCP
     Surgically altered anatomy i.e., Roux-en-Y reconstruction
     Failed re-intervention for transpapillary stent occlusion
    Contraindications
     Severe coagulopathy
     Massive ascites
     Intervening vessels including collateral vessels
     Unstable conditions unfit for endoscopic procedures
    Study n Initial/rescue Stent Drainage method Technical success Clinical success Adverse events
    Bories et al. (2007) [22] 4 Initial PS HGS 4 4 1 stent clogging
    Ogura et al. (2014) [23] 1 Initial UMS+CMS Bridging 1 N/A N/A
    Ogura et al. (2015) [18] 11 Initial/Rescue UMS+CMS 4 HDS, 7 Bridging 11 N/A 0
    Prachayakul et al. (2015) [24] 1 Initial UMS+CMS Bridging 1 1 0
    Moryoussef et al. (2017) [25] 18 Initial UMS+CMS 14 HGS, 3 Bridging 17 13 3
    Park et al. (2010) [26] 3 Rescue CMS HGS 3 3 0
    Park et al. (2013) [19] 2 Rescue CMS HDS 2 2 0
    Minaga et al. (2017) [27] 30 Rescue CMS or PS 28 HGS, 2 HDS 29 22 3 bile peritonitis
    Ogura et al. (2017) [28] 10 Rescue CMS 8 HGS, 2 HDS 10 9 0
    Kanno et al. (2017) [29] 7 Rescue CMS HGS 7 4 0
    Mukai et al. (2017) [20] 1 Rescue PS HDS 1 N/A 0
    Overall 88 98% (86/88) 77% (58/75) 8% (7/87)
    EUS-BD EBD PTBD
    Advantage A single step internal drainage Long term data available High technical success rate
    Simplicity at the hilum: possible longer patency Possible tube rinse for clogging
    Disadvantage No long term data Technical difficulty for multiple stenting Impaired QOL
    Special technique necessary for right IHBD approach Complexity at the hilum High AE rate and re-intervention rate
    Contraindications: ascites, coagulopathy Chance of Post-ERCP pancreatitis Contraindications: ascites, coagulopathy
    Chance of bile leak, stent migration
    Table 1. Current Indications and Contraindications of Endoscopic Ultrasound-Guided Biliary Drainage for Hilar Malignant Biliary Obstruction

    ERCP, endoscopic retrograde cholangiopancreatography.

    Table 2. Data on Endoscopic Ultrasound-Guided Biliary Drainage for Hilar Malignant Biliary Obstruction

    CMS, covered metal stent; HDS, hepaticoduodenostomy; HGS, hepaticogastrostomy; N/A, not available; PS, plastic stent; UMS, uncovered metal stent.

    Table 3. Advantages and Disadvantages of EUS-BD

    AE, adverse event; EBD, endoscopic transpapillary biliary drainage; ERCP, endoscopic retrograde cholangiopancreatography; EUS-BD, endoscopic ultrasound-guided biliary drainage; IHBD, intrahepatic bile duct; PTBD, percutaneous transhepatic biliary drainage; QOL, quality of life.


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