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EUS-guided antegrade intervention for benign biliary diseasesin patients with surgically altered anatomy (with videos)

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Shuntaro Mukai, MD,1 Takao Itoi, MD, FASGE,1 Atsushi Sofuni, MD,1 Takayoshi Tsuchiya, MD,1

Reina Tanaka, MD,1 Ryosuke Tonozuka, MD,1 Mitsuyoshi Honjo, MD,1 Mitsuru Fujita, MD,1

Kenjiro Yamamoto, MD,1 Yuichi Nagakawa, MD2

Tokyo, Japan

Background and Aims: Although balloon enteroscopy–assisted ERCP (BE-ERCP) is effective and safe for benign

biliary diseases in patients with surgically altered anatomy (SAA), BE-ERCP is not always successful. Recently, EUS-guided antegrade intervention (EUS-AI) by using a 1-stage or 2-stage procedure has been developed for BE-ERCPfailure cases. The aim of the present study was to evaluate the outcome of EUS-AI for benign biliary diseases inpatients with SAA.

Methods: Of 48 patients in whom BE-ERCP failed, percutaneous transhepatic intervention was performed in 11.From November 2013 until November 2017, we retrospectively reviewed cases of an additional 37 patients withSAA who failed BE-ERCP and underwent EUS-AI for benign biliary diseases (common bile duct stones [n Z 11],intrahepatic bile duct stones [n Z 5], anastomotic strictures [n Z 21]).

Results: The overall technical success of the creation of the hepatoenteric tract by EUSwas 91.9% (34/37).Moderateadverse events were observed in 8.1% (biliary peritonitis [n Z 3]). One-stage EUS-AI by EUS succeeded in 8 cases(100%) without any adverse events. In another 26 cases, 2-stage EUS-AI by ERCP was performed about 1 or 2monthslater. Endoscopic antegrade therapy under fluoroscopy was successful in 6 cases. Per-oral cholangioscopy–assistedantegrade intervention was required in 19 cases (guidewire manipulation across the anastomotic stricture [nZ 6],cholangioscopy-guided lithotripsy by using electrohydraulic lithotripsy [nZ 13]). In 1 case, magnetic compressionanastomosis was performed. The final clinical success rate of all EUS-AIs was 91.9%.

Conclusions: EUS-AI for benign biliary diseases in patients with SAA appears to be a feasible and safe alternativeprocedure after BE-ERCP failure.

Management of benign biliary diseases such as anasto-motic strictures and/or bile duct stones in patients withsurgically altered anatomy (SAA) often is troublesome.Recently, the efficacy and safety of balloon enteroscopy–assisted ERCP (BE-ERCP) in such patients has been re-ported.1-4 However, BE-ERCP is not always successfulbecause of the technical difficulty and time constraints,

ns: BE-ERCP, balloon enteroscopy–assisted ERCP; EUS-AI,antegrade intervention; EUS-BD, EUS-guided biliaryUS-HGS, EUS-guided hepaticogastrostomy; EUS-HJS, EUS-ticojejunostomy; MS, metal stent; PCSEMS, partially coveredble metal stent; POCS-AI, per-oral cholangioscopy–assistedntervention; SAA, surgically-altered anatomy.

E: T. Itoi is a speaker for Boston Scientific Japan andedical System. All other authors disclosed no financials relevant to this publication.

2018 by the American Society for Gastrointestinal Endoscopy

urnal.org

even when performed by endoscopists skilled in pancrea-ticobiliary procedures. Traditionally, in cases of BE-ERCPfailure, percutaneous transhepatic intervention or surgicalintervention has been performed. However, those alterna-tives may lead to a patient burden because of the long hos-pitalization as well as cosmetic issues, resulting in adecrease in quality of life.

0016-5107/$36.00https://doi.org/10.1016/j.gie.2018.07.030

Received March 27, 2018. Accepted July 25, 2018.

Current affiliations: Department of Gastroenterology and Hepatology (1);Third Department of Surgery, Tokyo Medical University, Tokyo, Japan (2).

Reprint requests: Takao Itoi, MD, PhD, FACG, FASGE, Department ofGastroenterology and Hepatology, Tokyo Medical University, 6-7-1Nishishinjuku, Shinjuku-ku, Tokyo 160-0023, Japan.

If you would like to chat with an author of this publication, you maycontact Dr Itoi at itoi@tokyo-med.ac.jp.

Volume -, No. - : 2018 GASTROINTESTINAL ENDOSCOPY 1

TABLE 1. Patient characteristics and disease with surgically alteredanatomy

Patientno. [ 37

Age, median (range), y 69 (22-90)

Sex, men/women 18/19

Benign biliary disease

Common bile duct stones 11

Intrahepatic bile duct stones 5

Anastomotic stricture 10

Anastomotic stricture complicated by stones 11

Anatomy

Gastrectomy with Roux-en-Y 9

Gastrectomy with Billroth-II procedure 2

Hepaticojejunostomy with Roux-en-Y 17

EUS-guided antegrade intervention Mukai et al

Recently, endosonograpy-guided biliary drainage (EUS-BD) has been developed in cases of ERCP failure includingBE-ERCP.5 Furthermore, a recent study demonstrated thatEUS-BD was superior to BE-ERCP, although it was a retro-spective study.6 However, apart from terminal-stage malig-nant diseases, the ultimate aim of the therapy in patientswith benign diseases is not to salvage biliary drainage butto dilate anastomoses and remove stones. Therefore,EUS-guided antegrade intervention (EUS-AI), including a1-stage procedure7,8 or a 2-stage procedure via an EUS-guided hepaticoenterostomy route, can be optimal therapyin cases of BE-ERCP failure as an alternative to percuta-neous and surgical intervention.9,10 However, limiteddata are available on the outcome of EUS-AI for benignbiliary diseases. Herein, we retrospectively evaluated theefficacy and safety of EUS-AI for benign biliary diseases inpatients with SAA.

Hepaticoduodenostomy 3

Pancreaticoduodenectomy with Whipple procedure 6

Causes of BE-ERCP failure

Difficulty with endoscope insertion 13

Difficulty with stone removal 9

Difficulty with drainage procedure 4

Difficulty with biliary cannulation 6

Difficulty with identification of anastomosis 5

BE-ERCP, Balloon enteroscopy–assisted ERCP.

METHODS AND PATIENTS

PatientsWe recorded cases of 37 consecutive patients (18 men,

19 women; median age 69 years, range 22-90 years) withSAA, who failed BE-ERCP and underwent EUS-AI for benignbiliary diseases including bilioenteric anastomosis stric-tures and/or bile duct stones between November 2013and November 2017 at Tokyo Medical University Hospital.Patient characteristics and diseases are shown in Table 1.The benign biliary diseases were as follows: common bileduct stones (n Z 11), intrahepatic bile duct stones (n Z5), and anastomotic strictures (n Z 21). Eleven caseswere complicated by intrahepatic bile duct stones. Theclinical diagnosis of benign biliary disease was based onCT, MRCP, and endoscopic imaging, with or withoutcytology and biopsy. The causes of failed BE-ERCP wereas follows: difficulty with endoscope insertion to thepapilla or the anastomosis (n Z 13), difficulty with stoneremoval (n Z 9), difficulty with the drainage procedure(n Z 4), difficulty with selective biliary cannulation (n Z6), and difficulty with identification of the anastomosis(n Z 5). Written informed consent for EUS-AI was ob-tained from all patients. This retrospective study wasapproved by our institutional review board (no. 3995).

ENDOSCOPIC PROCEDURES

Creation of the hepatoenteric tract fortransmural procedures by EUS

A hepatoenteric tract was created by the EUS-BD tech-nique. EUS-guided hepaticogastrostomy (EUS-HGS) orEUS-guided hepaticojejunostomy (EUS-HJS) was per-formed according to prior gastrectomy. All procedureswere performed by using a conventional curved lineararray echoendoscope as described previously.11 Briefly, astandard 19-gauge needle was used to puncture the left in-

2 GASTROINTESTINAL ENDOSCOPY Volume -, No. - : 2018

trahepatic bile duct under EUS guidance. A 22-gauge nee-dle was used if the targeted bile duct was not dilatedsufficiently. With regard to the puncture site, the B2branch bile duct is preferable compared with the B3branch bile duct because sequential antegrade interven-tions are easier to perform from the B2 approach. Howev-er, because B2 puncture may cause a transesophagealpuncture, leading to mediastinitis, the puncture pointshould be verified carefully under endoscopic view. Aftercontrast medium injection, an insulated stiff guidewire(0.025-inch VisiGlide; Olympus Medical Systems, Tokyo,Japan for a 19-gauge needle or a 0.018-inch Pathfinder;Boston Scientific, Natick, Mass for a 22-gauge needle)was advanced into the bile duct. If possible, the guidewirewas manipulated through the papilla or the anastomosis.The needle tract was dilated initially by using an ultra-tapered mechanical dilator (ES dilator DC7R180S; ZeonMedical Co, Ltd, Tokyo, Japan). If necessary, additionaldilation was performed with a cautery dilator (6.5F Cyst-Gastro set; Endoflex, Voerde, Germany), an 8F dilationcatheter (Soehendra dilator; Cook Medical, Bloomington,Ind, USA) or a 4 mm–diameter dilating balloon (Hurricane;Boston Scientific, Marlborough, Mass or REN; KanekaMedix Corp, Osaka, Japan). When we used a 0.018-inchguidewire, we exchanged it for a 0.025-inch stiff guidewireafter catheter advancement in the bile duct.

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Mukai et al EUS-guided antegrade intervention

One-stage EUS-AI by EUSOur intention was to perform EUS-AI in 2 sessions (crea-

tion of tract and endoscopic procedure) tominimize the riskof adverse events. However, in cases of bile ductstones <15 mm or anastomotic strictures that were not se-vere (passage of the guidewire across the anastomotic stric-ture in <3 minutes), EUS-guided transhepatic antegradestone removal and/or antegrade balloon dilation for anasto-motic strictures was performed after tract dilationaccording to the physician’s preference as described previ-ously (Video 1, available online at www.giejournal.org).7

Two-stage EUS-AI by ERCPAfter tract dilation, a single-pigtail plastic stent dedi-

cated for EUS-HGS or EUS-HJS (8F diameter, 20-cmlength; Gadelius Medical Co, Ltd, Tokyo, Japan)11 or apartially covered self-expandable metal stent (PCSEMS)(8 mm or 10 mm diameter, 10 cm or 12 cm length, Tae-woong Medical Co, Seoul, Korea) was placed in the bileduct (Video 2, available online at www.giejournal.org).Endoscopic antegrade interventions in 2-stage EUS-AIwere conducted by using a therapeutic duodenoscopeat least 1 month after EUS-BD to allow the tract tomature. At first, a 0.025-inch guidewire wasinserted into the bile duct alongside the plastic stent.Then, the plastic stent was removed by using rat or snareforceps. In PCSEMSs, endoscopic procedures were per-formed through the PCSEMS. When endoscopistsconsidered that the PCSEMS would complicate subse-quent procedures, it was removed in advance by usingsnare forceps.

A standard ERCP injection catheter (ERCP catheter;MTW, Dusseldorf, Germany) was used for cholangiographyto evaluate the bile duct stones and the stricture of theanastomosis. When the standard guidewire was notadvanced across the papilla or the anastomosis, a hydro-philic guidewire (0.032-inch Radifocus Guidewire; Terumo,Tokyo, Japan) was used. Then, dilation of the papilla orstricture of the anastomosis was performed by using a stan-dard or large balloon (4-mm to 18-mm, Hurricane RXBiliary Balloon Dilatation Catheter; CRE Balloon; BostonScientific, Tokyo, Japan, Giga; Century Medical, Tokyo,Japan or REN; Kaneka Medix Corp) under fluoroscopicguidance. Bile duct stones were pushed out of the bileduct in the duodenum or jejunum across the major papillaor the anastomosis, and/or were extracted by using aretrieval balloon catheter (20-mm, Multi-3V; Olympus Med-ical Systems) or basket catheter (FGY0002; Olympus) overthe wire. In cases of large and hard stones, a mechanicallithotripter (Lithocrush V, Over-the-wire type; OlympusMedical Systems) was used to crush the stones over thewire. Finally, after the antegrade interventions, an 8Fplastic stent was placed to maintain the fistula for possiblereintervention. In anastomotic stricture cases, the plastic

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stent was placed across the anastomosis and the HGS orHJS route.

Per-oral cholangioscopy–assisted antegradeintervention

When endoscopic antegrade treatment was difficultbecause of large intrahepatic bile duct stones or the diffi-culty of guidewire passage across a severe anastomotic stric-ture under fluoroscopic guidance, per-oral cholangioscopy–assisted antegrade intervention (POCS-AI) was performedvia the hepaticoenteric tract (Fig. 1). In cases of 8F plasticstent placement, after tract dilation by a 10F dilationcatheter (Soehendra Dilator; Cook Medical), a digitalcholangioscope (SpyGlass DS Direct Visualization System;Boston Scientific Corp) was advanced over the guidewire.If cholangioscope insertion was impossible because ofinflexibility of the tract, a 10F plastic stent was placedtemporarily. A few days later, the insertion of thecholangioscope was attempted again. After the insertion ofthe cholangioscope, cholangioscopy-guided lithotripsy byusing electrohydraulic lithotripsy for the stones and guide-wire manipulation across the anastomotic stricture, underdirect visualization (Figs. 2 and 3) (Videos 3 and 4,available online at www.giejournal.org). POCS-AI was con-ducted by 2 experienced endoscopists who used the“mother-baby” method.

Outcome measurementsWe calculated the technical success rate, the clinical suc-

cess rate, and the adverse event rate of EUS-AI. The tech-nical success of the creation of a hepatoenteric tract wasdefined as successful stent placement in the bile duct.The outcome of endoscopic antegrade interventions wasevaluated in 1-stage EUS-AI and 2-stage EUS-AI, respec-tively. The technical success of endoscopic antegrade inter-vention was defined as successful balloon dilation for theanastomotic stricture and/or successful removal ofthe bile duct stones. Clinical success was defined as theimprovement of jaundice and the remission of cholangitisfor >3 months after the achievement of the antegradetreatment procedure. Adverse events were graded accord-ing to the severity grading system of the American Societyfor Gastrointestinal Endoscopy lexicon.

RESULTS

BE-ERCP was performed in 224 patients for benignbiliary diseases with SAA at Tokyo Medical University Hos-pital during this study. A flowchart of our treatment out-comes in this case series is shown in Figure 4. Of 48patients in whom BE-ERCP failed, EUS-AI was attemptedfrom the left intrahepatic bile duct in 37 patients, andpercutaneous transhepatic intervention was performed in11 patients because the approach from the right hepaticbile duct was necessary for the treatment. Details of the

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Figure 1. Schema of per-oral cholangioscopy–assisted antegrade intervention. A, Antegrade guidewire manipulation across a severe anastomotic strictureat the hepaticojejunostomy site. B, Antegrade lithotripsy by using electrohydraulic lithotripsy for the intrahepatic bile duct stone afterpancreaticoduodenectomy.

EUS-guided antegrade intervention Mukai et al

EUS-AI procedure are shown in Table 2. The overalltechnical success of creation of a hepatoenteric tract byEUS was 91.9% (34/37, hepaticogastrostomy 31 cases,hepaticojejunostomy 3 cases). Three cases involveddifficulty regarding creating a hepatoenteric tract becauseof the non-dilated bile duct. In 1 of those cases, the EUS-rendezvous technique was performed, resulting in success-ful transpapillary stone removal with BE-ERCP. In another 2cases, observational management was selected. Moderateadverse events were observed in 3 cases for the creationof the hepatoenteric tract by EUS (8.1%, 3/37, biliary peri-tonitis, n Z 3). Three cases of biliary peritonitis weremanaged conservatively and successfully. Of 34 cases ofsuccessful creation of a hepatoenteric tract, 1-stage EUS-AI by EUS was performed in 8 cases (23.5%). Endoscopicantegrade stone removal and/or antegrade balloon dilationunder fluoroscopic guidance were successful in all 8 cases(100%), without any adverse events.

In 26 cases (76.5%), 2-stage EUS-AI by ERCP was per-formed about 1 or 2 months later. Endoscopic antegradestone removal and/or antegrade balloon dilation underfluoroscopic guidance were successful in 6 cases. POCS-AI was required in 19 cases (guidewire manipulation acrossthe severe anastomotic stricture under direct visualization[n Z 6], cholangioscopy-guided lithotripsy by using elec-trohydraulic lithotripsy for the stones [n Z 13]). In 1case, magnetic compression anastomosis was performedvia the hepaticogastrostomy route for the completeobstruction of hepatic duodenostomy. Of 26 cases, com-plete stone removal or treatment for anastomotic stricturesby 2-stage EUS-AI was achieved in all patients (100%)

4 GASTROINTESTINAL ENDOSCOPY Volume -, No. - : 2018

without any adverse events. The final clinical success rateof total EUS-AI for benign biliary diseases with SAA was91.9% (34/37, intention-to-treat analysis).

DISCUSSION

Recently, BE-ERCP has become the first-line interven-tion in patients with SAA, although traditional percuta-neous transhepatic drainage and sequential percutaneoustranshepatic cholangioscopy–assisted procedures or surgi-cal intervention may be performed when BE-ERCP fails oris not available. Lately, transgastric or transenteric EUS-guided interventions have become popular because theyare minimally invasive and possible “short cut” procedurescompared with surgical and BE-ERCP-related interventions,respectively. A summary of reports in the literature aboutEUS-AI in patients with SAA is shown in Table 3.12-17 Thesedata indicated that EUS-AI could be a useful and safe alter-native procedure for benign biliary diseases in patientswith SAA.

EUS-AI appears to have the following advantages overother procedures: (1) it can be performed within a shortprocedure time, (2) it is easy and safe to perform ante-grade reintervention by using a therapeutic duodenoscopevia the mature hepatoenteric tract in the same manner asthe transpapillary ERCP procedure, and (3) the internaldrainage of EUS-BD eliminates several issues associatedwith using an external drainage catheter. Percutaneousintervention is an established alternative procedure, butthe external drainage of percutaneous biliary drainage

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Figure 2. Per-oral cholangioscopy–assisted antegrade intervention of guidewire manipulation across a severe anastomotic stricture at the hepaticojeju-nostomy site. A, The severe anastomotic stricture, appearing like a pin-hole (white arrow), was detected under direct visualization. B, A guidewire couldbe passed across the anastomotic stricture at the hepaticojejunostomy site.

Figure 3. Per-oral cholangioscopy–assisted antegrade lithotripsy by using electrohydraulic lithotripsy for the intrahepatic bile duct stone. A, Creation of ahepatoenteric tract by EUS-guided hepaticogastrostomy was performed as a first stage of a 2-stage EUS-guided antegrade intervention. B, Cholangioscopy-guided lithotripsy by using electrohydraulic lithotripsy was performed 1 month after EUS-guided hepaticogastrostomy.

Mukai et al EUS-guided antegrade intervention

may add to the patient’s burden because of the externalbile loss, the cosmetic problem, or bile leakage, compro-mising quality of life. In especially benign biliary disorders,the percutaneous management during the long period mayplace more of a burden to patients and their families.4

The clinical success of EUS-AI appears to be higher thanthat of BE-ERCP. Skinner et al2 reported in their systematicreview that BE-ERCP achieved an overall success rate of74%. Shah et al1 reported in a multicenter U.S.experience that successful BE-ERCP was achieved in 63%of patients. These data indicate that BE-ERCP is usefulbut technically challenging even if it is performed by anexperienced endoscopist. However, we consider that atthis time BE-ERCP is basically first-line therapy for benignbiliary diseases, and EUS-AI should be performed only asan alternative procedure. A systematic review of BE-ERCPshowed an adverse event rate of 3.4%. On the otherhand, a systematic review of EUS-BD showed an adverseevent rate of 23.3%.2,5 These data indicate that BE-ERCPis clearly a less-invasive and safer procedure than EUS-

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BD. Khashab et al6 showed in their comparative studybetween BE-ERCP and EUS-BD for patients with SAA thatadverse events occurred more commonly in the EUS-BDgroup (20% vs 4%; P Z .01) although EUS-BD procedureswere significantly less time consuming, with an average of40 minutes saved per procedure. Sequential antegradeintervention is not established, and the devices that canbe used are limited compared with BE-ERCP. Althoughsome reports showed the efficacy of EUS-guided antegradestone removal in patients with SAA, the success rate ofcomplete stone removal was 60% to 100%.7,12,13 Further-more, the risk of bleeding during or after balloon dilationof the papilla or the anastomosis should be a matter ofconcern, although such an adverse event was not observedin this study. Endoscopic antegrade hemostasis without anendoscopic view may be difficult.

In terms of endoscopic antegrade intervention, 2-stageEUS-AI after hepatoenteric tract maturation, resulting inthe prevention of bile leakage, can be considered saferthan 1-stage EUS-AI. The matured access route to the

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EUS-RZ + BE-ERCPn = 1

Observationn = 2

PTBDn = 11

EUS-AIn = 37

BE-ERCPn = 224

Benign biliary disease with SAAn = 224

Failure (n = 48)Success (n = 176)

Success (n = 11) Success (n = 34) Failure (n = 3)

Figure 4. Flow chart of outcome of EUS-guided antegrade intervention for benign biliary diseases in patients with surgically altered anatomy. SAA,surgically altered anatomy; PTBD, percutaneous biliary drainage; EUS-AI, EUS-guided antegrade intervention; EUS-RZ, EUS-guided rendezvous; BE-ERCP, balloon enteroscopy–assisted ERCP.

EUS-guided antegrade intervention Mukai et al

bile duct allows the safe use of mechanical lithotripsy orcholangioscopy for antegrade intervention. However, ifthe creation of a hepatoenteric tract by the EUS-BD tech-nique is not difficult in cases of bile duct stones that arenot large or anastomotic strictures that are not severe,sequential 1-stage EUS-AI would be acceptable, resultingin a decrease of the number of interventions. In this study,adverse events related to bile leakage were not observed incases of 1-stage EUS-AI even though our study consisted ofa small number of cases. Further evaluation is necessary toclarify that the characteristics of stones and/or anatomy aremaximally suitable for 1-stage EUS-AI.

Regarding the selection of the stent for placementacross the hepatoenteric tract in 2-stage EUS-AI, the signif-icance of EUS-BD lies more in the creation of an accessroute from the GI tract to the bile duct than in drainageof bile juice. Basically, because the stent is removed for an-tegrade intervention about 1 or 2 months later, the long-term patency is not highly important. When consideredfrom the viewpoint of medical cost, the plastic stent is bet-ter than a PCSEMS. Previously we reported the technicalfeasibility and safety of a newly designed 8F plastic stentdedicated for EUS-HGS.11 The advantage of this plasticstent for EUS-BD in benign biliary diseases is as follows:(1) the tapered and straight distal tip can be advancedeasily in the bile duct even if many intrahepatic bile ductstones disturb the insertion of the stent, (2) reintervention

6 GASTROINTESTINAL ENDOSCOPY Volume -, No. - : 2018

or stent exchange is easy to perform after stent removal byusing a forceps via the hepaticoenterostomy tract, and (3)there is no concern about proximal and distal stent migra-tion. In fact, the results of this study showed that in the ma-jority of cases of EUS-BD, the dedicated plastic stent wasplaced successfully with fewer adverse events (8.1%) thanreported in a previous systematic review of EUS-BD in pa-tients with SAA (17.5%).18

In the intrahepatic bile duct stone cases, often there isnot enough space to grasp the stones by mechanical litho-tripsy, and large stones can be difficult to remove. In caseswith severe anastomotic strictures, it is extremely difficultto negotiate severe anastomotic strictures with guidewiremanipulation under fluoroscopic guidance. In such cases,it appears to be effective to insert a per-oral cholangio-scope from the matured hepatoenteric tract to perform an-tegrade treatment. Recently, per-oral cholangioscopy hasbecome increasingly common for diagnostic and therapeu-tic indications in patients with biliary diseases. To selec-tively advance the cholangioscope through a curved andtortuous intrahepatic bile duct and directly view the targetstones and pinhole anastomosis site, it is particularly effec-tive to use the novel digital cholangioscope (SpyGlass DS)that can be operated with 4-way steering.19 Moreover,specially designed working channels for passingaccessories such as electrohydraulic lithotripsy anddedicated irrigation and aspiration channels, enable

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TABLE 2. Details of EUS-AI for biliary benign diseases in patients withsurgically altered anatomy

Patientno. [ 37

Overall technical success ofcreation of hepatoenteric tractsby EUS, no. (%)

34/37 (91.9%)

1-stage EUS-AI 8

2-stage EUS-AI 26

Adverse events of total EUS-AI, no. (%) 3/37 (8.1%)

Moderate biliary peritonitis 3

Clinical success of total EUS-AI(intention-to-treat), no. (%)

34/37 (91.9%)

1-Stage EUS-AI by EUS (n Z 8)

Benign disease

Common bile duct stone, no. 8

Stone size, mean (range), mm 9.6 (5-15)

No. of stones, mean (range) 3.3 (1-10)

Hepatoenteric tract, no.

Hepaticogastrostomy 6

Hepaticojejunostomy 2

Type of stent in hepatoenteric tract

8F dedicated plastic stent 8

Technical success of antegradeintervention, no. (%)

8/8 (100%)

Technique of antegrade intervention, no.

Antegrade stone removal and/orballoon dilation

8

Procedure time (range), min 27.4 (22-35)

Adverse events of 1-stage EUS-AI, no. (%) 0 (0%)

Clinical success of 1-stage EUS-AI, no. (%) 8 (100%)

2-stage EUS-AI by ERCP (no. Z 26)

Hepatoenteric tract, no.

Hepaticogastrostomy 25

Hepaticojejunostomy 1

Type of stent of hepatoenteric tract

8F dedicated plastic stent 23

Partially covered self-expandablemetal stent

3

Technical success of antegradeintervention, no. (%)

26/26 (100%)

Technique of antegrade intervention, no.

Antegrade stone removal and/or balloondilation

6

Per-oral cholangioscopy–assisted antegradeintervention

19

Magnetic compression anastomosis 1

Procedure time of first creation of ahepatoenteric tract (range), min

17.9 (8-43)

Procedure time of 2-stage EUS-AI (range), min 47.8 (14-84)

TABLE 2. Continued

Patientno. [ 37

Adverse events of first creation ofhepatoenteric tract, no. (%)

3 (11.5%)

Moderate biliary peritonitis 3

Adverse events of 2-stage EUS-AI, no. (%) 0 (0%)

Clinical success of 2-stage EUS-AI, no. (%) 26 (100%)

EUS-AI, EUS-guided antegrade intervention.

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Mukai et al EUS-guided antegrade intervention

efficient treatment for stones, with good directvisualization. If the hepatoenteric tract is created with an8F plastic stent and dilated with a 10F dilation catheter,in many cases it is possible to insert the cholangioscope,of which the 10.5F catheter tip is tapered, by operating itat an angle and aligning the axis. If the insertion of thecholangioscope is difficult, a 10F plastic stent can beinserted temporarily for further dilation of the fistula,making the subsequent insertion possible several dayslater. However, further improvements are necessary intechniques for cholangioscope insertion from thehepatoenteric tract. Recently, we removed the plasticstent after dilation of the hepatoenteric tract aside fromthe plastic stent, with an ultra-tapered mechanical dilator(ES dilator DC7R180S, Zeon Medical Co, Tokyo, Japan).The digital cholangioscope cannot be inserted into thebile duct through the available enteroscope at present.This point is a distinct advantage of EUS-AI over BE-ERCP. Although BE-ERCP is basically first-line therapy forbenign biliary diseases, EUS-AI (POCS-AI) may be selectedas a first-line therapy for cases in which the digital cholan-gioscope is likely to be used.

EUS-AI appears to be a useful procedure, but there aresome critical points that require special attention in this pro-cedure. One is the fact that many cases are particularlydemanding technical difficulties. Because the dilated intra-hepatic bile duct in cases of benign biliary diseases is oftenthinner than in cases of malignant biliary strictures andobstructive jaundice, the puncture of the bile duct may bedifficult. Furthermore, the fistula dilation and stent place-ment are difficult in cases in which repeated cholangitis re-sults in a rigid bile duct wall or cases of bile ductscontaining many intrahepatic bile duct stones. Antegradetreatment also may be difficult in cases of severe anasto-motic strictures. It has been reported that temporary place-ment ofmetal stent (MS) is effective for cases of anastomoticstrictures that cannot be improved by the regular balloondilation and plastic stent placement. Although antegradeMS placement is possible in the anastomosis site, theremoval of MS becomes an issue if it is difficult to insertthe endoscope to the anastomosis. The development ofMS for which antegrade placement in the anastomosis andantegrade removal are possible or the development of a

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TABLE 3. Summary of reports in the literature of EUS-guided antegrade intervention in patients with surgically altered anatomy

First author Anatomy Biliary diseaseNo. ofpatients

Antegradeintervention

Technicalsuccess (%)

Adverseevents (%)

Weilert12 RYGB Choledocholithiasis 6 ASR 67 8.3

Iwashita13 RY, Whipple BBD þ MBO 6 ASR, ABD, ABS 100 33

Itoi7 RY, B-II Choledocholithiasis 5 ASR 60 0

Khashab6 RY, RYGB, Whipple, B-II BBD þ MBO 49 ASR, ABS 98 20.4

Iwashita8 RY, Whipple, B-II Choledocholithiasis 29 ASR 72 17

Miranda-Garcia14 N/A Anastomotic stricture 7 ABD þ ABS 57.1 71.4

Iwashita15 RY, B-II, GB, BR MBO 20 ABS 95 20

Hosmer16 RYGB, RY Choledocholithiasis 9 ASR 100 11

James17 RYGB, RY, B-II, Whipple BBD 20 ASR, ABS 15

RYGB, Roux-en-Y gastric bypass; ASR, antegrade stone removal; RY, Roux-en-Y reconstruction; BBD, benign biliary disease; MBO, malignant biliary obstruction; ABD, antegradeballoon dilation; ABS, antegrade biliary stenting; B-II, Billroth II reconstruction; N/A, not available; GB, gastric bypass; BR, biliary reconstruction.

POCS is likely to be used for therapy

Failure

Yes

No

Failure

Failure

Failure

Failure

Yes

No

One-stage EUS-guided antegrade intervention

Salvage surgeryAlternative pathway (EDGE or EUS-GI)

PTBD + Percutaneous antegrade intervention

EUS-antigrade intervention(POCS-assisted antegrade intervention)

POCS-assisted antegrade intervention

Two-stage EUS-guided antegrade interventionunder fluoroscopy

No difficulty of EUS-BD procedure?Non-large bile duct stones?Non-severe anastomic stricture?

EUS-guided antegrade intervention

Possible to approach via left IHBD?

Benign biliary disease with surgically altered anatomy

Balloon enteroscopy-assisted ERCP

Figure 5. Current algorithm for benign biliary diseases in patients with surgically altered anatomy. POCS, per-oral cholangioscopy; IHBD, intrahepatic bileduct; PTBD, percutaneous biliary drainage; EUS-BD, EUS-guided biliary drainage; EDGE, EUS-directed transgastric ERCP.

EUS-guided antegrade intervention Mukai et al

novel large-bore stent that allows for permanent placementin the anastomosis is warranted. Furthermore, when themanagement of benign biliary diseases cannot be achievedby EUS-AI alone, salvage surgery would be considered,although this was not performed in this study. If salvage sur-gery would be required, there is a possibility that EUS-AIwould hinder surgery by placed stent or created fistula.

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Recently, other novel alternative techniques have beenreported such as EUS-directed transgastric ERCP in pa-tients with Roux-en-Y gastric bypass.20 This technique isto perform standard ERCP by using a duodenoscopeadvanced through the created fistula with EUS-guidedtransgastric fistula by placing a lumen-apposing metalstent. This technique may be possible to apply to another

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Mukai et al EUS-guided antegrade intervention

altered anatomy by creating the fistula between theremnant stomach or the jejunum and the afferent limb.It has become an issue how to use EUS-AI in the futureand these alternative techniques properly.

This study has several limitations. Because it was a single-center retrospective study, and all procedures of EUS-AIwere performed by an expert on interventional EUS andERCP procedures, there may have been selection bias anda technical bias regarding procedure feasibility and safety.The procedure strategy or the devices used for EUS-AIwere not standardized. Furthermore, in this study thelong-term outcome has not yet been evaluated. Because itis treatment for benign biliary diseases, the long-termoutcome is important, especially in anastomotic stricturecases. The influence of long-term exposure of the stomachto bile juice is also concerning. Besides, in this study the fac-tors associated with successful or unsuccessful procedurescould not be assessed. It was considered that the factor asso-ciated with unsuccessful therapy with EUS-AI was probablyan intrahepatic bile duct that had not beendilated.However,it could not be confirmed in this retrospective study. To ac-cess these factors, a prospective analysis is required.

In conclusion, EUS-AI for benign biliary diseases withSAA appears to be a feasible and safe alternative procedureafter BE-ERCP failure, although further large-scale prospec-tive feasibility studies with long-term follow-up and thestandardization of the procedure are required to validateEUS-AI. Finally, we propose the current treatment algo-rithm for benign biliary diseases in patients with SAA inFigure 5. This algorithm is not mature, and so furtherevaluation and modification would be required.

ACKNOWLEDGMENT

The authors are grateful to Professor Emeritus J. PatrickBarron of Tokyo Medical University for his editorialguidance.

REFERENCES

1. Shah RJ, Smolkin M, Yen R, et al. A multicenter, U.S. experience ofsingle-balloon, double-balloon, and rotational overtube-assisted en-teroscopy ERCP in patients with surgically altered pancreaticobiliaryanatomy (with video). Gastrointest Endosc 2013;77:593-600.

2. Skinner M, Popa D, Neumann H, et al. ERCP with the overtube-assistedenteroscopy technique: a systematic review. Endoscopy 2014;46:560-72.

3. Ishii K, Itoi T, Tonozuka R, et al. Balloon enteroscopy-assisted ERCP inpatients with Roux-en-Y gastrectomy and intact papillae (with videos).Gastrointest Endosc 2016;83:377-86.

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4. Mukai S, Itoi T, Baron TH, et al. Indications and techniques of biliarydrainage for acute cholangitis in updated Tokyo Guidelines 2018.J Hepatobiliary Pancreat Sci 2017;24:537-49.

5. Wang K, Zhu J, Xing L, et al. Assessment of efficacy and safety of EUS-guided biliary drainage: a systematic review. Gastrointest Endosc2016;83:1218-27.

6. Khashab MA, El Zein MH, Sharzehi K, et al. EUS-guided biliary drainageor enteroscopy-assisted ERCP in patients with surgical anatomy andbiliary obstruction: an international comparative study. Endosc IntOpen 2016;4:E1322-7.

7. Itoi T, Sofuni A, Tsuchiya T, et al. Endoscopic ultrasonography-guidedtranshepatic antegrade stone removal in patients with surgicallyaltered anatomy: case series and technical review (with videos).J Hepatobiliary Pancreat Sci 2014;21:E86-93.

8. Iwashita T, Nakai Y, Hara K, et al. Endoscopic ultrasound-guided ante-grade treatment of bile duct stone in patients with surgically alteredanatomy: a multicenter retrospective cohort study. J HepatobiliaryPancreat Sci 2016;23:227-33.

9. Nakai Y, Isayama H, Koike K. Two-step endoscopic ultrasonography-guided antegrade treatment of a difficult bile duct stone in a surgicallyaltered anatomy patient. Dig Endosc 2018;30:125-7.

10. Shimatani M, Mitsuyama T, Takaoka M, et al. Role of two-step endo-scopic ultrasonography-guided antegrade treatment as an option forbile duct stones in patients with surgically altered anatomy. Dig En-dosc 2018;30:50-1.

11. Umeda J, Itoi T, Tsuchiya T, et al. A newly designed plastic stent forEUS-guided hepaticogastrostomy: a prospective preliminary feasibilitystudy (with videos). Gastrointest Endosc 2015;82:390-6.

12. Weilert F, Binmoeller KF, Marson F, et al. Endoscopic ultrasound-guided anterograde treatment of biliary stones following gastricbypass. Endoscopy 2011;43:1105-8.

13. Iwashita T, Yasuda I, Doi S, et al. Endoscopic ultrasound-guided ante-grade treatments for biliary disorders in patients with surgically alteredanatomy. Dig Dis Sci 2013;58:2417-22.

14. Miranda-García P, Gonzalez JM, Tellechea JI, et al. EUS hepaticogastros-tomy for bilioenteric anastomotic strictures: a permanent access forrepeated ambulatory dilations? Results from a pilot study. Endosc IntOpen 2016;4:E461-5.

15. Iwashita T, Yasuda I, Mukai T, et al. Endoscopic ultrasound-guided an-tegrade biliary stenting for unresectable malignant biliary obstructionin patients with surgically altered anatomy: single-center prospectivepilot study. Dig Endosc 2017;29:362-8.

16. Hosmer A, Abdelfatah MM, Law R, et al. Endoscopic ultrasound-guidedhepaticogastrostomy and antegrade clearance of biliary lithiasis in pa-tients with surgically-altered anatomy. Endosc Int Open 2018;6:E127-30.

17. James TW, Fan YC, Baron TH. EUS-guided hepaticoenterostomy as aportal to allow definitive antegrade treatment of benign biliary dis-eases in patients with surgically altered anatomy. Gastrointest Endosc.Epub 2018 May 2.

18. Siripun A, Sripongpun P, Ovartlarnporn B. Endoscopic ultrasound-guided biliary intervention in patients with surgically altered anatomy.World J Gastrointest Endosc 2015;7:283-9.

19. Tanaka R, Itoi T, Honjo M, et al. New digital cholangiopancreatoscopyfor diagnosis and therapy of pancreaticobiliary diseases (with videos).J Hepatobiliary Pancreat Sci 2016;23:220-6.

20. Kedia P, Sharaiha RZ, Kumta NA, et al. Internal EUS-directedtransgastric ERCP (EDGE): game over. Gastroenterology2014;147:566-8.

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