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CLINICAL REVIEW

Clinical Review of EUS-guided Gastroenterostomy (EUS-GE)


Ana Y. Carbajo, MD,* Michel Kahaleh, MD,†
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and Amy Tyberg, MD†


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carries a complication risk of up to 40%. These include


Abstract: Gastric outlet obstruction (GOO) refers to mechanical delayed gastric emptying, prolonged hospital stay, and delay
obstruction of the distal stomach or proximal duodenum and it is in cancer treatment.5–7 SEMS placement for GOO have found
associated with a significant decrease in quality of life. Surgical gas- technical and clinical success rates in over 80% to 90% of
trojejunostomy and self-expandable metal stents were the traditional
treatment for GOO. Recently, endoscopic ultrasound guided gastro-
cases.8 However, long-term efficacy is limited with recurrent
enterostomy (EUS-GE) has emerged as a third therapeutic option for obstruction occurring in up to 50% of patients after
patients with GOO. Most EUS-GE techniques utilize the placement 6 months.9 When comparing these 2 techniques, SEMS has
of a lumen-apposing metal stent under echoendoscopy but differ in been shown to be associated with lower complication rates,
the method of localizing the jejunal loop prior to EUS puncture. Data decrease time to initiation of oral feeding, and shorter hospital
supporting EUS-GE have been promising. Case series including 10 or stay but with a suboptimal patency suggesting benefit of SGJ
more cases showed the technical success rate to be approximately in patients with longer life expectancies ( > 6 mo).10,11
90%. Clinical success is achieved in approximately 85–90% and a less Endoscopic ultrasound-guided gastroenterostomy
than 18% risk of adverse events is reported. EUS-GE was associated (EUS-GE) has emerged as a third therapeutic option for
with a lower recurrence of GOO and need for re-intervention when
compared to enteral stenting. In addition, EUS-GE shows sig-
patients with GOO. EUS-GE provides symptom relief
nificantly fewer adverse events compared with surgical gastro- without the risks of surgical bypass and without the limited
jejunostomy. In conclusion, EUS-GE provides symptom relief with- long-term efficacy of enteral SEMS placement. Many
out the risks of surgical intervention and the limited patency of enteral patients with GOO, especially those with malignant GOO,
SEMS placement. EUS-GE is an exciting new option in the man- are too debilitated to be considered surgical candidates.
agement of GOO. Despite the excellent results, randomized studies However, EUS-GE can be offered to the majority of
comparing these different modalities of treatment for GOO are patients with GOO. In this article, we will review the indi-
needed before EUS-GE can be accepted as standard of care. cations, techniques, safety and efficacy, and current con-
Key Words: therapeutic endoscopic ultrasound, EUS-guided gastro- troversies of EUS-GE.
jejunostomy, gastric outlet obstruction, lumen-apposing metal stent
(J Clin Gastroenterol 2020;54:1–7) EUS-GE
With this technique, a bypass is created by inserting a
stent from the stomach to the small bowel distal to the
obstruction under endoscopic ultrasound guidance. EUS-
G astric outlet obstruction (GOO) refers to mechanical
obstruction of the distal stomach or proximal duode-
num. Malignancy is the most common cause of GOO in the
GE includes 2 options based on the target anastomotic site,
gastroduodenostomy (into the distal part of the duodenum),
era of adequate medical therapy for acid suppression, and gastrojejunostomy.
accounting for 50% to 80% of cases. In patients with pan- Endoscopic gastroenterostomy was first described in
creatic cancer, it is estimated that 15% to 20% of patients 1991 in an animal model using a forward viewing flexible
develop GOO.1–3 Immediate treatment of GOO is indicated, endoscope and a compression button.12 Since then, several
as dehydration and malnutrition can quickly develop in these other animal models using different types of stents, acces-
patients.4 The aim of treatment is to relieve symptoms from sories, and techniques including natural orifice transluminal
obstruction, allowing for resumption of oral diet and endoscopic surgery (NOTES) were then performed.10,13–16
improved quality of life. Surgical gastrojejunostomy (SGJ) The first concept of EUS-GE was introduced by Fritscher-
and self-expandable metal stents (SEMS) were the traditional Ravens et al17 in 2002 in a porcine model.18 However, the
treatment for GOO. SGJ achieves high long-term efficacy, but technique was not adopted because of the complexity of the
procedure, need for special devices, and endoscope
exchange.
From the *University Hospital Rio Hortega, Valladolid, Spain; and In 2012, Binmoeller et al19 first introduced EUS-GE
†Rutgers Robert Wood Johnson University Hospital, New Bruns- with a lumen-apposing metal stent (LAMS), (AXIOS TM
wick, NJ.
A.T. has done consulting work for EndoGastric Solutions, NinePoint
stent; Boston Scientific, Marlborough, MA) in an animal
Medical, and Obalon Therapeutics. M.K. has Grant support from model. Theoretically, LAMS allows adhesion between 2
Boston Scientific, MaunaKea, Apollo Endosurgery, Cook Endos- organs as is done with a surgical anastomosis minimizing
copy, ASPIRE Bariatrics, NinePoint Medical, Merit Medical, the risk for leakage and stent migration. With this stent,
Olympus, and Interscope Med. Consultant for Boston Scientific,
Concordia Laboratories Inc., Interscope Med. and ABBvie. A.Y.C.
creation of an endoscopic GE under EUS guidance became
declares that there is nothing to disclose. feasible. This was quickly adopted in humans by endo-
Address correspondence to: Michel Kahaleh, MD, Rutgers, The State scopists with expertise in interventional EUS.20–27
University of New Jersey, Robert Wood Johnson University Hos- Currently, the 2 available endoscopic methods for
pital, 1 RWJ Place, MEB 491B, New Brunswick, NJ 08901 (e-mail:
mkahaleh@gmail.com).
gastroenterostomies are EUS-GE and NOTES. Barthet
Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved. et al28 reported the first clinical experience of NOTES
DOI: 10.1097/MCG.0000000000001262 approach to endoscopic gastroenterostomy by using LAMS.

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Clinical Review of EUS-guided Gastroenterostomy J Clin Gastroenterol  Volume 54, Number 1, January 2020

However, very limited data exist in humans and the appli- TECHNIQUES
cation of NOTES-GE is limited. Several techniques can be used to create an EUS-GE.
All methods require a therapeutic linear echoendoscope and
INDICATIONS AND CONTRAINDICATIONS use a biflanged LAMS but differ in the method of localizing
Symptomatic GOO is amenable for EUS-GE regard- the jejunal loop before EUS puncture.
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less of the etiology (benign or malignant). In addition, sev- Direct EUS-GE


eral cases of EUS-guided gastrojejunostomy for the treat-
ment of afferent loop syndrome have been reported.29–34 A duodenal or jejunal loop adjacent to the stomach is
Afferent loop syndrome is an obstruction of the afferent identified by EUS.20,21,37 This may be difficult when the
loops are poorly distended or contain air. Careful EUS
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intestinal limb that can occur after gastrointestinal surgery


and causes intestinal dilation with subsequent biliary examination can usually yield an appropriate loop for direct
obstruction. Traditionally, limited treatment options have puncture by a 19-G needle (Fig. 1). If jejunal loops cannot
been available for this condition, sometimes requiring sur- be adequately imaged, a 22-G needle puncture can be per-
gical intervention. Retrograde endoscopic decompression of formed first with injection of saline to distend the bowel
the afferent loop is not always possible because of a long loops before puncture with a 19-G needle.21 Similarly, a
enteric segment, completely obstructing mass, tight angu- gastroscope or nasojejunal tube can be first inserted and
lation, or long stricture. Therefore, EUS-GE may also be fluid infused into the small bowel distal to the obstruction.
useful for the treatment of this syndrome. Generally, a total of 500 mL of fluid (more can lead to the
An additional benefit of EUS-GE is to provide access to the development of hyponatremia) is infused. As such, isotonic
saline may be the preferred solution. After transgastric
ampulla for patients with concurrent biliary obstruction. This can
be done by deploying the LAMS with the proximal end in the puncture of the small bowel, an enterogram is obtained by
small bowel loop near to the ampulla and then advancing injection of contrast under fluoroscopic guidance to ensure
the duodenoscope through the LAMS in a retrograde manner to correct positioning of the needle tip within the lumen of the
the ampulla in order to perform conventional endoscopic retro- small bowel (Fig. 2). Either a 1-step or 2-step procedure can
grade cholangiopancreatography.35,36 be then performed to create the gastrojejunostomy (GJ).
Some consideration must be taken into account before Like other EUS-guided procedures, in the 2-step method, a
the procedure. Localization of an appropriate target small- guidewire is advanced into the jejunal lumen. The 19-G
bowel loop close enough to the gastric wall is essential. Any needle is then exchanged under endosonographic guidance
distance longer than 2 cm may result in incomplete apposi- leaving the wire in place. The gastrojejunal tract is dilated to
tion of the lumens by the metal stent. If there is diffuse allow for passage of the 10.8 Fr LAMS delivery catheter,
which is subsequently passed over the wire transgastrically
malignant gastric infiltration, a gastroenterostomy may not
be safe or technically feasible (similarly, in case of cancer into the jejunum. More aggressive dilation is discouraged
extending into the fourth portion of duodenum and prox- because this may result in peritoneal leakage. The intro-
imal jejunum around the ligament of Treitz). Ascites is not a duction of a commercially available cautery-enabled LAMS
contraindication to performing the procedure, but should be delivery catheter (Hot-Axios; Boston Scientific) has allowed
drained before the procedure to minimize intestinal mobi- single-step insertion, without the need for prior dilation,
lization. Indications and contraindications to perform EUS- either over a wire or freehand.21,22 The LAMS is deployed
GE are shown in Table 1. with the distal end in the small bowel lumen and the prox-
imal end in the stomach (Fig. 3). The lumen of the LAMS is
then dilated using a through-the-scope balloon dilator
PERIPROCEDURAL CARE AND PREREQUISITES (Fig. 4).
A clear liquid diet or low-residue diet should be
established days before the procedure to minimize gastric Assisted Technique
residue. In case of large amounts of food residue, endo- An endoscope is advanced into the stomach and across
scopic removal should be accomplished before starting the the obstruction into the distal small bowel if feasible. A wire
procedure. All patients receive intravenous antibiotics is then advanced and coiled in the jejunum beyond the
immediately before the procedure. The procedure requires obstruction. If the stenosis cannot be traversed with the
fluoroscopy and general anesthesia with endotracheal intu- endoscope, the wire is advanced from the stomach through
bation. Carbon dioxide insufflation should be used the stenosis under fluoroscopic guidance alone.20,37–39 A
throughout the procedure. Most patients remain in the dilating balloon, biliary extraction balloon, or nasobiliary
hospital and receive a course of antibiotics (gram negative drain catheter is advanced over the wire into the jejunum
and anaerobe coverage). Liquid diet is often started the under fluoroscopic guidance.21 Then, a linear echoendo-
following day, and diet is advanced slowly as tolerated. scope is advanced into the stomach alongside the balloon or

TABLE 1. Indications and Contraindications of Endoscopic Ultrasound (EUS)-guided Gastroenterostomy


Indications Contraindications
Symptomatic GOO Diffuse cancer invasion into the site of puncture (stomach or small bowel)
Afferent loop syndrome Inability to identify an appropriate small bowel loop close to the gastric wall under EUS
Allow access for performing an ERCP in the Luminal obstruction distal to the jejunum puncture site (in the setting of peritoneal
setting of GOO carcinomatosis or extensive lymphadenopathy)
Large volume ascitis
ERCP indicates endoscopic retrograde cholangiopancreatography; GOO, gastric outlet obstruction.

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J Clin Gastroenterol  Volume 54, Number 1, January 2020 Clinical Review of EUS-guided Gastroenterostomy
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FIGURE 1. Echosonographic view of direct puncture of


jejunum.

catheter. Contrast is injected into the balloon or directly into FIGURE 3. Fluoroscopic image of deployed lumen-apposing
the jejunal lumen through the nasobiliary drain to help metal stent.
identify the jejunal loop echosonographically and fluo-
roscopically (Fig. 5). The loop is accessed with a 19-G lumen. Forceps through the ultraslim scope is used to grasp
needle. The fistulous tract is then created, and the LAMS the guidewire for traction and the LAMS is then deployed.
deployed as previously described. Alternatively, a snare can
be advanced into the jejunum and once puncture occurs, the
EUS-guided Balloon-occluded Gastrojejunostomy
guidewire is advanced through the snare, which is then
closed onto the wire and pulled through the patient’s mouth Bypass (EPASS)
giving the endoscopist access to both ends of the wire to This technique was described by Itoi et al.22,43,44 A
facilitate stent deployment.40 specialized double balloon enteric tube (Tokyo Medical
Variations on the use of an assisted device to fill and University Type; Create Medic, Yokohoma, Japan) is
subsequently localize a jejunal loop have also been described advanced through the obstruction over a guidewire. If
with an ultraslim endoscope (hybrid rendezvous) passed needed, an overtube may be used to facilitate passage of the
through the stricture.41,42 This scope can be advanced balloon catheter to avoid looping in the fornix of the
orally, or through a previously placed percutaneous gas- stomach as it passes through the stenosis. The 2 balloons are
trostomy tract when present.41 Water is injected through the then inflated with saline or contrast to seal the small bowel
ultraslim scope to distend the bowel lumen. A linear at 2 ends. Saline is used also to fill the lumen between the
echoendoscope is then advanced into the stomach (alongside balloons leading to easier and safer transgastric EUS
the ultraslim scope). After the puncture, a guidewire is puncture and stent insertion with the LAMS (using the 1
advanced through the needle and coiled within the bowel step or 2 step method described previously).

NOTES-GE
A 19-G needle is used to puncture the gastric wall
under EUS guidance. A guidewire is then passed into the
peritoneal cavity close to the ligament of Treitz. The
echoendoscope is then removed, leaving the guidewire in
place. The double-channel endoscope is advanced over the

FIGURE 2. Fluoroscopic enterogram after direct puncture FIGURE 4. Endoscopic image of deployed lumen-apposing
injection. metal stent.

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Clinical Review of EUS-guided Gastroenterostomy J Clin Gastroenterol  Volume 54, Number 1, January 2020

period. In 2016, Itoi et al22 described the first clinical study


of EUS-GE using the EPASS technique in 20 patients with
malignant GOO. The technical success rate was 90% due to
2 unsuccessful stent deployment cases. After technique
adjustment, technical success rate increased from 81.8% to
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100% when the authors abandoned the use of an over-the-


wire method. In those 2 patients the stent was removed, and
the patients were treated by conservative therapy. No stent
occlusion or migration was observed. The third experience is
a multicenter study in 26 patients (benign obstruction in 9
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cases), in which multiple EUS-GE techniques were used.21


They incorporated novel methods to help locate the target
bowel (nasobiliary drain catheter and hybrid rendezvous),41
and salvage strategies for LAMS misplacement. Technical
success was achieved in 24 patients (92%) and clinical suc-
cess in 22 (85%). In this series, misplacement occurred in 7
of 26 cases (27%) and was the only reason for technical
FIGURE 5. Echosonographic view of inflated balloon catheter in failure overall. Five misplacements were able to salvaged
the target small bowel loop. with a telescoping fully covered SEMS.45–47 Adverse events
such as bleeding, peritonitis, and surgery occurred in 3
wire into the stomach. An incision on the gastric wall is patients (11.5%). After successful LAMS placement, no
performed with a needle-knife and then it is dilated. The migration or dysfunction was noted. Most recently, a ret-
gastroscope is passed into the peritoneal cavity, the jejunum rospective study evaluated EUS-GE in 26 patients with
is identified, and the jejunum is incised with the needle-knife benign GOO.26 Several patients in this study were reported
under endoscopic visualization. Afterwards, a guidewire is in other separate publications. Outcomes are comparable to
introduced into the lumen. A LAMS is advanced over the other studies with malignant GOO; technical and clinical
wire through the jejunal incision and the distal flange is success rates were 96.2% and 84.0% respectively, with 3
deployed inside the jejunum. The gastroscope is then pulled adverse events noted (2 mild AE).
back into the stomach, with both the opened LAMS flange EUS-GE compared with enteral stenting was evaluated
and a rat-tooth forceps through the second working channel in a retrospective series of 82 patients:23 30 who underwent
used as retractors. The proximal LAMS flange is then EUS-GE and 52 who underwent enteral stenting. There was
deployed inside the stomach, and a balloon can be used to no observed difference in technical success, clinical success,
dilate the LAMS to its diameter.28 or adverse events between the 2 groups. In addition, EUS-
GE was associated with a lower recurrence of GOO and
Technical Considerations need for reintervention when compared with ES. In other
EUS-GE technique has not been standardized yet, as words, EUS-GE is at least as effective and safe as ES with
there are several advantages and disadvantages in each the benefit of improved long-term patency.
technique. The major concern using the direct technique is EUS-GE was compared with SGJ in a retrospective
the difficulty in accessing the small bowel via needle punc- study of 93 patients with malignant GOO: 30 in the EUS-
ture, because the lumen is often collapsed. In addition, the GE and 63 in the SGJ arm.24 In the EUS-GE cohort, 23
injection of a large amount of fluid distends both the tar- patients were previously reported in a separate study. The
geted small intestine and the colon, which can lead to a miss- rate of clinical success was similar between both groups
puncture. However, the use of methylene blue infusion into (92% vs. 87%, P = 0.42) and there was no significant dif-
the small intestinal lumen followed by needle puncture and ference in the rate of AEs (16% vs. 25%, P = 0.3). Impor-
aspiration of blue tinge fluid before stent insertion minimizes tantly, the rate of GOO recurrence was equally low in both
the risk for inadvertent colonic stent insertion. Unlike the groups (3% vs. 14%, P = 0.08), which suggests that EUS-GE
direct technique, the assisted and the EPASS techniques provides long-lasting symptom palliation of GOO similar to
facilitate small bowel puncture. However, advancement of that of surgical bypass. However, this was a retrospective
the balloon catheter or the double balloon enteric tube may study in which patients in the SGJ group were recruited
be challenging in cases of tight strictures. from 1 center, whereas patients in the EUS-GE group were
recruited from multiple centers. This may have introduced
heterogeneity to the study population. In addition, patients
OUTCOME OF EUS-GE in the surgical group underwent open surgery which may
Data supporting EUS-GE have been promising. Case not be the standard of care at some centers.
series including ≥ 10 cases showed the technical success rate A similar study comparing EUS-GE with SGJ retro-
to be ~90% regardless of the technique used. Table 2 sum- spectively evaluated 25 patients who underwent EUS-GE and
marizes the available literature on the success of EUS-GE. 29 patients who underwent laparoscopic gastrojejunostomy
The first large clinical experience was reported in (Lap-GJ).25 The indication for GE included malignant and
201520 in which 10 patients with GOO (3 malignant and 7 benign GOO. No significant differences in terms of technical
benign) underwent EUS-GE using a LAMS. EUS-GE was and clinical success rates were observed between the 2 groups.
performed by using direct or balloon-assisted technique. The This is especially notable because the EUS-GE group con-
authors reported technical and clinical success rate of 90%. tained more patients with symptomatic GOO with failed prior
All patients underwent placement of a 15 mm×10 mm attempts at palliation, and all patients in the EUS-GE group
LAMS. There were no procedure-related adverse events were deemed unsuitable for surgical intervention indicative of
and there was no symptom recurrence during the follow-up a sicker group of patients preprocedurally. These discrepancies

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J Clin Gastroenterol
TABLE 2. Outcomes of EUS-guided Gastroenterostomy (Studies With ≥ 10 Patients)


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LAMS Technical Clinical

Volume 54, Number 1, January 2020


Study Patients Type of Diameter Type of Success Success* Misplacement Recurrent Follow-
References Design (n) Indication Technique LAMS (mm) EUS-EE (%) (%) (%) Adverse Events (%) GOO up (wk)
Khashab RS 10 Malignant: 3 D: 1 N-C: 10 15×10: 10 GJ: 6 9/10 (90) 9/10 (90) None None None 21
et al20 MC Benign: 7 A: 9 GD: 3
Itoi et al22 PS 20 Malignant: 20 EPASS: 20 N-C: 11 15×10: 20 GJ: 20 18/20 (90) 18/20 (90) 2 (10) 1 Pneumoperitoneum None 14
C: 9 NS: 2
Tyberg et al21 RS 26 Malignant: 17 D: 3 N-C: 17 15×10: 25 — 24/26 (92) 22/26 (85) 7 (27) 3 (11.5) None 8
MC Benign: 9 A: 21 (B: 13/ C: 9 10×10: 1 SS: 5 Pain: 1
NBD: 3/ NS: 2 Bleeding: 1
UUS: 5) Peritonitis: 1
NOTES: 2
Chen et al23, RS 30 Malignant: 30 D: 2 N-C: 7 15×10: 30 GJ: 26 26/30 (87) 25/30 (83) 3 (10) 5 (17) 1 15
Khashab MC A: 6 C: 21 GD: 4 NS: 3 —
et al24 Comp EPASS: 22 Spaxus:
2
Perez-Miranda RS 25† Malignant: 17 D: 6 N-C: 12 — — 22/25 (88) 21/25 (84) 9 (36) 3 (12) None 8
et al25 MC Benign: 8 A: 19 (B: 9/ C: 13 SS: 6 Peritonitis: 1
Comp NBD: 3/ NS: 3 Bleeding: 2
USS: 7)
Chen et al23 RS 77† Malignant: 52 D: 55 N-C: 16 15×10: 72 GJ: 63 72/77 (94) 71/77 (92) 5 (7) 5 (7) 4 17
MC Benign: 25 A: 22 C: 56 GD: 14 SS: 3 —
Comp NS: 2
Chen et al26 RS 26† Benign: 26 D: 15 N-C: 2 15×10: 26 GJ: 21 25/26 (96) 21/26 (81) 2 (8) 3 (11.5) 1 25
MC A: 7 C: 24 GD: 5 SS: 2 MD: 2 (mild)
EPASS: 4 Gastric leak: 1

Clinical Review of EUS-guided Gastroenterostomy


*Intention-to-treat analysis.
†Several patients in this study may have also been included in other publications.
Definitions of technical and clinical success.
Tyberg et al21 and Perez-Miranda et al:25
Technical success: successful placement of a gastrojejunal LAMS.
Clinical success: patient’s ability to tolerate oral intake.
Other studies: Technical success: adequate positioning and deployment of the stent.
Clinical success: patient’s ability to tolerate oral intake without vomiting.
A indicates assisted methods EUS-gastrojejunostomy (B, balloon; NBD, nasobiliary drain; USS, ultraslim scope); C, cautery LAMS; EUS-EE, endoscopic ultrasound enteroenterostomy; Comp, comparative; D, direct
EUS gastrojejunostomy; EPASS, EUS-guided double balloon-occluded gastrojejunostomy bypass; GD, gastroduodenostomy; GJ, gastrojejunostomy; MC, multicenter; MD: misdeployment; N-C, noncautery LAMS;
NOTES, natural orifice transluminal endoscopic surgery; NS, not salvaged; PS, prospective study; RS, retrospective study; SS, successfully salvaged.
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Clinical Review of EUS-guided Gastroenterostomy J Clin Gastroenterol  Volume 54, Number 1, January 2020

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