Int J Gastrointest Interv 2020; 9(4): 177-183
Published online October 31, 2020 https://doi.org/10.18528/ijgii200031
Copyright © International Journal of Gastrointestinal Intervention.
Kenjiro Yamamoto and Takao Itoi*
Department of Gastroenterology and Hepatology, Tokyo Medical University, Tokyo, Japan
Correspondence to:* Corresponding author. Department of Gastroenterology and Hepatology, Tokyo Medical University, 6-7-1 Nishishinjuku, Shinjuku-ku, Tokyo 160-0023, Japan.
E-mail address: itoi@tokyo-med.ac.jp (T. Itoi).
This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Gastric outlet obstruction (GOO) can be caused by benign and malignant diseases. GOO often leads to a decreased quality of life, because of nausea, vomiting, and problems with oral food intake. Traditionally, surgical gastrojejunostomy (SGJ) has been the primary treatment for GOO. Endoscopic enteral stenting (EES) has also been carried out for the treatment of malignant GOO. In recent years, endoscopic ultrasonography-guided gastroenterostomy (EUS-GE) using a lumen apposing metal stent has emerged as a procedure to treat patients with GOO, as an alternative to surgery or to standard endoscopy when EES is not possible. Various techniques, such as direct EUS-GE, assisted EUS-GE, and EUS-guided balloon-occluded gastrojejunostomy bypass have been established to perform EUS-GE safety and accurately. Previous reports of EUS-GE with lumen apposing metal stent demonstrated that the technical and clinical success rates were 87% to 100% and 84% to 100%, respectively, without differentiating the various procedural techniques. The adverse events rate ranged from 0% to 18.1%, and included stent misdeployment, bleeding, peritonitis, leakage, abdominal pain, etc. In addition, the reintervention rate ranged from 0% to 15.1%. Moreover, a comparison of EUS-GE and SGJ showed that there was no significant difference in clinical success, rate of adverse events, or need for reintervention between these procedures. On the other hand, studies comparing EUS-GE with EES showed that EUS-GE may have higher clinical success and a lower rate of stent failure requiring repeated intervention than EES. Furthermore, EUS-GE has been used in several clinical scenarios, such as the management of endoscopic retrograde cholangiopancreatography in patients who underwent Roux-en-Y gastric bypass, or for the treatment of afferent loop syndrome. The present review describes the presently available EUS-GE techniques and introduces the recent clinical advances in the treatment of GOO.
Keywords: Endoscopic enteral stenting, Endoscopic ultrasonography-guided gastroenterostomy, Gastric outlet obstruction, Surgical gastrojejunostomy
Gastric outlet obstruction (GOO) can be caused by benign and malignant diseases. In particular, malignant GOO occurs in up to 20% of patients with various digestive malignancies, such as gastric, duodenal, and pancreaticobiliary cancers.1 The onset of malignant GOO portends a poor prognosis, with patients having a median survival of 3 to 6 months.2 GOO often leads to a decrease in the quality of life of a patient, because of nausea, vomiting, and problems with oral food intake. Furthermore, in patients with a malignant disease who develop GOO, chemotherapy must be temporarily or permanently discontinued as a result of the patient’s poor general condition and/or need for surgical intervention. Most of these patients have advanced, unresectable tumors, and thus, symptom palliation and improving their quality of life are the usual goals of any intervention.3
Traditionally, surgical gastrojejunostomy (SGJ; either open or laparoscopic) has been the primary treatment method for both benign and malignant GOO. Endoscopic intervention using enteral self-expanding metal stents placed across the obstruction, i.e., endoscopic enteral stenting (EES), has been carried out for the treatment of malignant GOO. At present, the most common interventions performed in such patients for the treatment of GOO are EES or SGJ.1,4
To date, 3 randomized trials have compared the outcomes of EES and SGJ, with mixed results; 2 trials obtained more favorable results for EES whereas 1 trial reported more favorable results for SGJ.5-7 The main shortcome of EES is recurrent GOO owing to tumor ingrowth and overgrowth, which occurs in the majority of patients who survive for longer than 6 months.7 Although SGJ is associated with better luminal patency outcomes compared with EES,8 surgical adverse events are not uncommon and include delayed gastric emptying, prolonged hospital stay, increased cost, and delay in cancer treatment.8,9
Furthermore, recent developments in chemotherapies have resulted in the prolongation of the life expectancy of cancer patients. Therefore, advances in minimally invasive strategies and techniques to relieve GOO are needed.
More recently, endoscopic ultrasonography (EUS)-guided gastroenterostomy (EUS-GE) has been developed as a procedure to treat patients with GOO, as an alternative to surgery or to standard endoscopy, when EES is not possible.10,11 Herein, we describe the current status and perspectives of the use of EUS-GE.
Recently, a lumen-apposing metal stent (LAMS) (AXIOSTM, Boston Scientific Corp., Marlborough, MA, USA) has been developed to safely tie together 2 adjacent luminal structures, resulting in new insights into the development of the EUS-GE procedure.12 This stent consists of a fully covered metal stent with bilateral anchor flanges. When fully expanded, the diameter of the anchor flange is almost twice that of the “saddle” section (24 mm and 15 mm, respectively). The stent anchors are designed to distribute pressure evenly on the luminal wall and to securely anchor the stent, preventing migration. The proximal and distal anchor flanges also securely connect the jejunal wall to the gastric wall, preventing detachment of the nonadherent jejunum. The collapsible braided stent is delivered through a 10.8-Fr catheter. The proprietary stent delivery system is luer-locked onto the echoendoscope instrumentation channel inlet port, to give the operator full control of stent deployment. The handle is designed to enable controlled release of each anchor flange, independently of the others, with a full “stop” after the release of the distal anchor flange to prevent premature deployment of the proximal anchor flange. Furthermore, the AXIOS-ECTM stent (often referred to as “Hot Axios”) (Fig. 1), includes an electrocautery-enhanced delivery system (a cautery tip equipped in the tip of the delivery system), which makes it possible to place the stent without needle puncture and guidewire placement, and may help to avoid missing the target during EUS-GE.
In principle, EUS-GE offers long-lasting luminal patency without the risk of tumor ingrowth or overgrowth, while avoiding morbidity owing to the surgical procedure in these terminally ill patients.13 In 2012, Binmoeller and Shah14 reported the results of the use of the newly developed LAMS in performing EUS-GE in 5 pigs. The procedure was technically successful in all animals, with no bleeding or perforation. Although this animal study demonstrated the utility of EUS-GE, its use in clinical practice was technically challenging, because accessing the duodenum and jejunum was difficult and unpredictable. The jejunum ordinarily contains air, and scope insertion can cause air insufflation, not only in the stomach but also in the small intestine and colon, which makes ultrasound imaging less clear. In addition, the normal jejunum does not distend. Thus, safe puncture into the small bowel is not guaranteed. To resolve these issues, water-filling luminal techniques with or without inflated balloons have been attempted by several endoscopists.14–16 However, the rapid infusion of a large amount of water to sufficiently dilate the small bowel has the risk of serious adverse events, such as hyponatremia and water intoxication, and is a general burden on the cardiovascular system. In addition, injection of a large amount of fluid distends not only the targeted small intestine, but also the colon, leading to mispuncture into the colon, namely, a gastrocolonostomy. Therefore, various techniques have been established to perform EUS-GE safely and accurately.
In the direct EUS-GE technique, careful identification of the duodenal or jejunal loop that is adjacent to the gastric body is first performed using a therapeutic echoendoscope. After transgastric puncture with a 22-gauge needle and distention of the bowel by injection of saline to enable its visualization by ultrasound, the small bowel is punctured using a 19-gauge fine needle aspiration (FNA) needle to obtain an enterogram, and then a guidewire is passed through the needle into the small bowel. After the GE tract is dilated using dilating balloons or electrocautery devices placed over the guidewire, the LAMS delivery system is inserted and the LAMS is placed.
The assisted EUS-GE technique using a retrieval or dilating balloon has been developed to improve access to the small bowel and to facilitate stent insertion.17,18 A guidewire is initially placed under endoscopic or radiologic guidance across the luminal stenosis into the distal duodenum or proximal jejunum, followed by insertion of a retrieval or dilating balloon catheter over a guidewire placed inthe small bowel where the anastomosis is to be created, which is then filled with water or saline. After the echoendoscope is inserted alongside the balloon catheter, the balloon is punctured with a 19-gauge FNA needle. A guidewire is advanced through the FNA needle, and a LAMS stent is subsequently placed.
EUS-guided balloon-occluded gastrojejunostomy bypass (EPASS) (Fig. 2) has been conducted based on the results of an animal study.19 This unique procedure is performed using a special double-balloon enteric tube (Tokyo Medical University type; Create Medic Co., Ltd., Yokohama, Japan), which enables instillation of saline between the 2 inflated balloons. A standard upper gastrointestinal endoscope with an overtube for a single balloon enteroscope (ST-SB1; Olympus Medical Systems, Tokyo, Japan) is advanced in front of the stenosis that is causing the GOO. The reason for using the overtube is to avoid looping of the special double balloon enteric tube in the fornix of the stomach and facilitate the tube passage through the pyloric-duodenal stenosis. After a guidewire is inserted over the stricture as far as possible beyond the duodenum and jejunum loop, the endoscope is removed, leaving the guidewire and the overtube. Then, a double-balloon tube is perorally inserted over the guidewire in combination with a 0.89-inch dedicated guidewire for enhanced torquability, and a balloon is placed in both the duodenum and jejunum, in an area adjacent to the stomach. Both balloons are filled with saline and contrast material to hold the small intestine open. After gently removing the overtube out of the mouth and a sufficient quantity of saline with contrast material is introduced into the space between the 2 balloons to distend the small bowel lumen, an echoendoscope is advanced into the stomach to identify the distended duodenum or jejunum.
EPASS is divided into 2 types of procedures, namely the 1-step procedure (freestyle technique) and 2-step procedure (standard technique). The freestyle technique is carried out using direct electrocautery-enhanced tip delivery system insertion without needle puncture. When the AXIOS-ECTM stent is used, the delivery system is directly advanced over the guidewire into the duodenum or jejunum while applying a current (usually in Autocut mode, 100 W, Effect 4). On the other hand, the standard technique is carried out as follows: a 19-gauge FNA needle is used to puncture the duodenum or jejunum under EUS guidance. A guidewire is inserted through the 19-gauge FNA needle. When an AXIOSTM stent is used for EPASS, the 19-gauge FNA needle is removed and the gastrojejunostomy tract is dilated over the wire using a 6-Fr electrocautery dilator and a 6-mm dilating balloon.20 The delivery system is advanced over the guidewire into the duodenum or jejunum. The stent is deployed across the GE tract under combined EUS, fluoroscopic, and endoscopic guidance. Finally, the lumen of the deployed stent is dilated using a dilating balloon.
A summary of the literature on the use of EUS-GE for patients with benign and malignant GOO is shown in Table 1.17,18,20–27 Although almost all of the studies were retrospective, the technical and clinical success rates were 87% to 100% and 84% to 100%, respectively, without differentiating the various procedural techniques. The rate of adverse events ranged from 0% to 18.1%, which included stent misdeployment, bleeding, peritonitis, leakage, abdominal pain, etc. In addition, the reintervention rate ranged from 0% to 15.1% for the entire cohort.
Table 1 . Clinical Outcomes of EUS-GE.
Author | Year | Study design | Sample size (n) | EUS-GE technique | B/M | TS/CS (%) | Rate of AEs (%) | Details of AEs | Reintervention (%) |
---|---|---|---|---|---|---|---|---|---|
Khashab et al17 | 2015 | M-R | 10 | D-GE ( | 1/9 | 90/90 | 0 | - | 0 |
Tyberg et al18 | 2016 | M-R | 26 | D-GE ( | 9/17 | 92/85 | 11.5 | Peritonitis ( | N/A |
Itoi et al21 | 2016 | S-P | 20 | EPASS ( | 0/20 | 90/100 | 10 | Misdeployment ( | 0 |
Chen et al20 | 2017 | M-R | 30 | D-GE ( | 0/30 | 87/87 | 16.7 | Misdeployment ( | 3 |
Khashab et al22 | 2017 | M-R | 30 | EPASS ( | 0/30 | 87/87 | 16 | Misdeployment ( | 3 |
Perez-Miranda et al24 | 2017 | M-R | 25 | D-GE ( | 8/17 | 88/84 | 13.6 | Bleeding ( | 0 |
Chen et al26 | 2018 | M-R | 26 | D-GE ( | 26/0 | 96.2/84 | 11.5 | Misdeployment ( | 4.8 |
Chen et al23 | 2018 | M-R | 74 | D-GE ( | 25/49 | 94.2/92.3 | 6.8 | Misdeployment ( | 9.5 |
Ge et al25 | 2019 | S-R | 22 | D-GE ( | 0/22 | 100/96 | 18.1 | Misdeployment ( | 4.5 |
Kerdsirichairat et al27 | 2019 | M-R | 57 | D-GE ( | 23/34 | 93/90 | 3.5 | Leakage ( | 15.1 |
EUS-GE, endoscopic ultrasonography-guided gastroenterostomy; B, benign; M, malignant; TS, technical success; CS, clinical success; AEs, adverse events; S-P, single-center prospective; S-R, single-center retrospective; M-R, multicenter retrospective; D-GE, direct gastroenterostomy; BA-GE, balloon-assisted gastroenterostomy; NOTES, natural orifice transluminal endoscopic surgery; EPASS, EUS-guided double balloon-occluded gastrojejunostomy bypass; LAMS, lumen apposing metal stent; N/A, not available..
In addition, recently, 2 systematic review and meta-analyses of EUS-GE for the management of GOO have been published. One meta-analysis,28 including 5 studies with 199 patients showed a technical success rate of 92.90% (95% confidence interval [95% CI] = 88.26–95.79; I2 = 0.00%) and a clinical success rate of 90.11% (95% CI = 84.64–93.44; I2 = 0.00%). Serious adverse events occurred in 5.61% (95% CI = 2.87–10.67; I2 = 1.67%) of patients, and were associated with peritonitis, perforation, bleeding, and abdominal pain. The reintervention rate was 11.43% (95% CI = 7.29–17.46; I2 = 17.38%). Another meta-analysis29 including 12 studies with 266 patients demonstrated that the technical success rate was 92% (95% CI = 88–95), and the clinical success rate was 90% (95% CI = 85–94). AEs were reported in 12% of the patients (95% CI = 8–16), and symptom recurrence occurred and unplanned reintervention was needed in 9% of the patients (95% CI = 6–13). These meta-analyses strongly supported that EUS-GE is an effective treatment modality for the management of benign and malignant GOO, with lower adverse events and reintervention rates.
On the other hand, the EUS-GE technique has not been standardized yet and the most appropriate technique is still unclear. The direct EUS-GE technique is simple and less labor intensive; however, this technique has the risk of colonic puncture and stent deployment into the colon. In addition, it is difficult to distinguish the small bowel from the colon on fluoroscopy. Therefore, to avoid inadvertent gastrocolostomy, the technique of methylene blue infusion into the small intestinal lumen followed by needle puncture and aspiration of the infused material before stent insertion may be useful. In contrast, the balloon-assisted EUS-GE method requires the insertion of a guidewire, which can push the small bowel away from the stomach during stent advancement over the wire, which may increase the risk for stent misdeployment. Chen et al23 compared the efficacy and safety of the direct EUS-GE technique with balloon-assisted EUS-GE. There are no differences between the 2 techniques in terms of technical and clinical success rates, rate of adverse events, postprocedure length of hospital stay, need for reintervention, and survival. However, the mean procedure time was shorter using the direct EUS-GE technique (35.7 minutes vs 89.9 minutes,
At present, the standard treatments for GOO are SGJ and EES, based on their favorable clinical outcomes; SGJ (technical success of 99%–100% and clinical success of 80%–90%) and EES (technical success of 96%–97% and clinical success of 85%–90%).8,30–33 However, the substantial morbidity and high adverse event rate associated with surgery has suggested the need for a less invasive and better tolerated alternative treatment.8,10,34 In contrast, EES is frequently needed for reintervention, owing to stent migration or stent occlusion caused by tumor ingrowth/overgrowth,7,8,34 although EES achieves comparable technical and clinical success rates with lower overall adverse event rates compared with surgery.31
To date, there have been a number of studies directly comparing the efficacy and safety of EUS-GE with SGJ or EES. In a multicenter retrospective study, Khashab et al22 compared EUS-GE with SGJ in 93 patients who had malignant GOO (EUS-GE,
Regarding EUS-GE and EES, Chen et al20 conducted a multicenter retrospective study comparing EUS-GE with EES in 82 patients (30 patients underwent EUS-GE and 52 patients underwent EES). Technical success rates between the 2 methods were not significantly different; 86.7% (26/30) in the EUS-GE group and 94.2% (49/52) in the EES group (
GOO arises from not only malignant diseases but also benign diseases with several etiologies, including peptic ulcer disease (PUD), acute and chronic pancreatitis, and caustic injury owing to substance ingestion.35,36 Endoscopic balloon dilation (EBD) has largely been performed as the initial treatment for benign GOO.33 Although the clinical success rate is high regarding EBD performed for GOO occurring secondary to PUD, treatment frequently requires multiple endoscopy sessions with repeated dilations, has a risk of perforation in 3% to 7% of patients, and a limited long-term response of 70% to 80%.33,37-41 In addition, EBD may have limited efficacy for GOO caused by other diseases, such as caustic injury42,43 and strictures secondary to pancreatitis owing to extensive fibrosis and inflammation.36 As another treatment option, EES has also been considered for the management of benign GOO, and has shown favorable results, but stent migration occurs in up to 60% of patients with fully covered metal stents.33,44 Chen et al26 conducted a study on 26 patients with GOO secondary to benign etiologies, who underwent EUS-GE. Technical success was achieved in 96.2% and clinical success was observed in 84.0% of patients, with a median follow-up time of 176.5 days. The rate of unplanned reintervention was 4.8%, and 3 adverse events were noted, including 2 misdeployed stents and 1 gastric leak needing surgical intervention following elective GE stent removal. EUS-GE is also a promising method for the management of benign GOO caused by a variety of etiologies. However, the safety of long-term stent placement and subsequent stent removal should be clarified. Furthermore, the criteria for performing EUS-GE in patients with benign GOO should be standardized, and EUS-GE should not be performed unless surgery is strictly contraindicated.
The EUS-GE method has been applied to several clinical scenarios, such as for the management of endoscopic retrograde cholangiopancreatography (ERCP) in patients who underwent Roux-en-Y gastric bypass (RYGB) or for the treatment of afferent loop syndrome (ALS).
Rapid weight loss after RYGB is associated with a high incidence of gallstones and their associated adverse events, which often necessitate pancreatobiliary interventions.45,46 Balloon enteroscopy-assisted ERCP (BE-ERCP) for patients with an RYGB anatomy can be performed at most tertiary centers, but is associated with low technical success and the procedure is time-consuming.47–49 Recently, a novel method using the EUS-GE technique to create a gastrogastrostomy to access the excluded stomach and thus facilitate subsequent anterograde ERCP, namely EUS-guided gastrogastrostomy-assisted ERCP (EUS-GG-ERCP) was reported.50-53 Bukhari et al50 conducted a comparative retrospective study between EUS-GG-ERCP and BE-ERCP in a total of 60 patients with RYGB anatomy (30 patients in the EUS-GG-ERCP group and 30 patients in the BE-ERCP group). The EUS-GG-ERCP group showed a higher technical success rate (100% vs 60.0%,
On the other hand, ALS is defined as a mechanical obstruction of the afferent limb, resulting in debilitating and fatal pancreaticobiliary symptoms. Therefore, early and appropriate decompression treatment is needed. Although to date, ALS has been treated surgically or endoscopically, recently there have been attempts to manage ALS using EUS-GE.54-56 Brewer Gutierrez et al54 assessed the utility and safety of EUS-GE for 18 patients with ALS. Technical success was achieved in 100% of the cases, and clinical success, namely, resolution of symptoms was observed in 88.9% of the patients, and improvement in their ALS-associated symptoms was observed in 11.1% of patients. Adverse events occurred in 16.7% of patients, which were all treated conservatively, and reintervention was required in 16.7% of the patients.
The development of effective chemotherapies has improved the prognosis of terminal cancer patients, particularly patients with pancreatic cancer, who often have GOO. Therefore, EUS-GE, which is a minimally invasive procedure with long-term stent patency, is increasingly used for these patients. Although favorable data on EUS-GE have been published, this procedure is technically demanding and can only be performed by highly trained endosonographers and experts in therapeutic EUS. Therefore, the dissemination of EUS-GE as a standard procedure for the treatment of GOO is needed to establish a safer optimal method. To correctly identify and perform a puncture in the target loops, it is necessary to fill the small intestine with water or saline and dilate it in advance. This is performed using a prior needle puncture, and a single balloon (balloon-assisted technique) or a double-lumen balloon device (EPASS). In addition, it is difficult to puncture the target loops because they are highly movable. Therefore, the puncture is performed with a 19-gauge needle that is required to pass a 0.035-inch guidewire. Similarly, dilation of the fistulous tract can also be difficult for the same reason, and may cause leakage of the bowel contents into the peritoneum. These problems can be overcome by the use of the AXIOS-ECTM device with an electrocautery-enhanced delivery system, which enables penetration and stent placement in a single-step procedure. As mentioned above, the advantages of the 1-step procedure over the 2-step procedure have been reported by Itoi et al21; the 1-step procedure showed a technical success rate of 100% versus 82% for the 2-step procedure. Furthermore, available LAMS have a maximum diameter that does not appear to be completely appropriate for EUS-GE, for which a bigger anastomosis is usually required. Recently, a 20-mm diameter stent has become available, to overcome this limitation of LAMS. The design of a short central portion and wide biflanges, which minimizes the risk of stent obstruction and migration, appears to be appropriate for creating a tight anastomosis. Additionally, the learning curve of surgeons and the endoscopic training required for various types of EUS-GE are an important concern. An effective training system using an appropriate training model is warranted. To date, the clinical data regarding EUS-GE are still based on many retrospective and few prospective studies. Therefore, further verified prospective randomized trials are necessary to establish EUS-GE as a standard treatment for GOO.
Recently, a lumen-apposing metal stent (LAMS) (AXIOSTM, Boston Scientific Corp., Marlborough, MA, USA) has been developed to safely tie together 2 adjacent luminal structures, resulting in new insights into the development of the EUS-GE procedure.12 This stent consists of a fully covered metal stent with bilateral anchor flanges. When fully expanded, the diameter of the anchor flange is almost twice that of the “saddle” section (24 mm and 15 mm, respectively). The stent anchors are designed to distribute pressure evenly on the luminal wall and to securely anchor the stent, preventing migration. The proximal and distal anchor flanges also securely connect the jejunal wall to the gastric wall, preventing detachment of the nonadherent jejunum. The collapsible braided stent is delivered through a 10.8-Fr catheter. The proprietary stent delivery system is luer-locked onto the echoendoscope instrumentation channel inlet port, to give the operator full control of stent deployment. The handle is designed to enable controlled release of each anchor flange, independently of the others, with a full “stop” after the release of the distal anchor flange to prevent premature deployment of the proximal anchor flange. Furthermore, the AXIOS-ECTM stent (often referred to as “Hot Axios”) (Fig. 1), includes an electrocautery-enhanced delivery system (a cautery tip equipped in the tip of the delivery system), which makes it possible to place the stent without needle puncture and guidewire placement, and may help to avoid missing the target during EUS-GE.
No potential conflict of interest relevant to this article was reported.
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