Endoscopic ultrasound-guided gastroenterostomy: a review

Introduction

Gastric outlet obstruction (GOO) results from the partial or complete blockage of the stomach and/or duodenum. Symptoms frequently include abdominal pain, early satiety, and post-prandial nausea and vomiting due to mechanical obstruction. A variety of benign and malignant conditions may be attributed to the development of GOO with the vast majority being related to malignancy, including pancreatic cancer, gastric cancer, cholangiocarcinoma, gallbladder cancer and lymphoma (1). Most common benign etiologies include peptic ulcer disease, acute and chronic pancreatitis, afferent loop syndrome, post-operative stenosis, superior mesenteric artery (SMA) syndrome, and caustic ingestion (1). GOO has a significant effect on a patient’s quality of life and often can delay or preclude treatment for malignant diseases (2).

Management of GOO has traditionally focused on palliating the cause of obstruction, and for many years has been by surgical means (open or laparoscopic gastrojejunostomy), endoscopically placed self-expanding metal stents (e.g., enteral stenting) or venting gastrostomy (3,4). Historically, survival in GOO has been shown to be quite poor. A 2009 study comparing enteral stenting vs. surgery demonstrated that nearly 50% of patient had a life expectancy of approximately 12 weeks, regardless of intervention (5). With advances in treatment, particularly for malignant diseases, patients are living longer, thus shifting the dynamic of how we approach this condition. Traditional surgical approaches achieve excellent long-term efficacy, but has been associated with increased risk of tissue trauma, longer recovery and hospitalization times, and post-operative complications such as bleeding and anastomotic leaks (6-8). Due to these concerns, surgical modalities may not be appropriate in frail patients. Enteral stenting has been favored as a less invasive endoscopic treatment for GOO; however, recurrent obstruction from tissue ingrowth/overgrowth is common, resulting in the need for reinterventions (6). The issues associated with the morbidity of an operation and the concerns over long-lasting luminal patency with enteral stenting has been the catalyst for innovative ideas to address the therapeutic dilemma posed by GOO. Most recently, endoscopic ultrasound-guided gastroenterostomy (EUS-GE) has emerged as an alternative method for the palliation of GOO. EUS-GE allows for a lumen apposing metal stent (LAMS) to be placed from the gastric lumen to a segment of small bowel distal to the region of obstruction, ultimately creating an endoscopic bypass. This technique offers symptomatic relief without the risks associated with surgery and without the short-term efficacy of enteral stents (9).

The advent of endoscopic ultrasound (EUS) has been an essential and rapidly expanding technology in the field of gastroenterology for over forty years. Since the development of the first radial echoendoscope in the 1980’s, this technology has ushered in creative approaches to address complex gastrointestinal problems. The concept of laparotomy-assisted endoscopic gastrojejunostomy was first described in 1991 by Swain and colleagues (10). Two flexible endoscopes accompanied by two compression buttons designed to induce ischemia and a resultant anastomosis were used in eight cases with patent anastomoses identified at nine months of follow up (10). The possibility of an endoscopically placed gastroenterostomy was revisited in 2002 in porcine models by Fritscher-Ravens et al. (11). They demonstrated that by using an echoendoscope in the stomach, it was possible to place needles with threaded tags and guidewires into the small bowel to create anastomoses (11,12). However, the procedure was not readily adopted due to complexity and need for specific devices (11,12). Over a decade later, Binmoeller and colleagues described a new method of EUS-GE in porcine models using a fully covered bi-flanged nitinol braided stent and delivery system, promoting apposition of the gastric wall to the jejunal wall (AXIOS^TM; Boston Scientific, Marlborough, MA, USA) (13). This ultimately led to the first clinical implementation by those with expertise in interventional EUS (14). Evolution of the LAMS lead to the development of the cautery-enhanced delivery system, which enables puncture, tract dilation, and stent placement with one device (AXIOS-EC^TM; Boston Scientific). This system has arguably become the most commonly used device for EUS-GE due to its technical feasibility and safety.

At present, there are no standardized methods to performing this procedure and various techniques have been described in the literature. Additionally, natural orifice transluminal endoscopic surgery (NOTES) has been reported as a means by which access to the abdominal cavity can be obtained and gastroenterostomy placement performed (15). The most common indication for EUS-GE is malignant GOO; however, this technique has also been successfully described in patients with benign etiologies such as chronic pancreatitis, peptic ulcer disease and surgical anastomotic strictures (16). A recent meta-analysis demonstrated a pooled technical success rate of 92% and clinical success rate of 90%, further solidifying EUS-GE as a viable alternative to traditional means of GOO management (17).

Procedural methods

EUS-GE can be considered in patients with symptomatic GOO and evidence of outlet obstruction on cross-sectional imaging. Cross-sectional imaging allows for assessment of technical feasibility based upon the proximity of the small bowel to the stomach. Evaluation for potential limitations such as diffuse malignant infiltration of the stomach, large volume ascites or multiple sites of gastrointestinal obstruction can also be assessed which could potentially preclude successful EUS-GE. Detailed informed consent should be obtained from patients with explanation that EUS-GE is an off-label use of and Food and Drug Administrative (FDA)-approved device. Patients should be aware of all options including surgical gastrojejunostomy and endoscopic alternatives such as enteral stenting or venting gastrostomy, as appropriate. A liquid diet prior to the procedure should be considered to minimize residual gastric contents days prior to the procedure. The procedure is performed with general anesthesia, fluoroscopy, and antibiotics are typically administered at the discretion of the endoscopist.

Various EUS-guided GE methods have been described each with nuances related to the identification of an appropriate small bowel loop and method of puncture for LAMS deployment. All methods require a therapeutic linear echoendoscope and a bi-flanged LAMS. Endosonographically, the targeted loop of small bowel should be in close apposition (<1 cm) from the gastric wall and the gastric site of puncture should be devoid of malignant involvement.

The direct method

The direct method was developed in part to simplify procedural steps, minimize device exchanges and ultimately increase the likelihood of technical success (14). To date, it is the preferred method of performing EUS-GE (18). This method requires adequate expansion of the small bowel with contrast mixed with methylene blue for appropriate targeting, which can be performed in two ways. A 19-gauge fine needle aspiration (FNA) needle can be used to puncture the targeted loop of small bowel with EUS guidance (19). Saline with methylene blue and contrast can be injected through the needle to distend the bowel prior to puncture. Alternatively, an endoscope is passed in close proximity to the region of obstruction and a guidewire is passed beyond the ligament of Treitz and into the jejunum (18). A nasojejunal catheter is advanced over the guidewire, and the endoscope and guidewire are carefully removed while maintaining the catheter in place. The catheter is subsequentially attached to an installation pump which allows for the rapid infusion of saline, contrast and methylene blue into the jejunum for adequate distention.

Once an adequately distended small bowel loop is identified by EUS, it is punctured with a 19G FNA needle. Methylene blue is aspirated and contrast is subsequently injected, thereby confirming location in the small bowel and ensuring the transverse colon is not inadvertently punctured. A one step or two step procedure can then be performed to create the gastroenterostomy. In the two-step method, a guidewire can be advanced through the FNA needle and into the jejunal lumen. Dilation of the fistula tract to accommodate the 10.8 Fr LAMS delivery catheter is performed with care to reduce the risk of peritoneal leakage followed by stent placement. Alternatively, cautery-enhanced LAMS allows for direct puncture and deployment of the stent, either with or without a guidewire. Reports of initial experience in EUS-GE described the deployment of the stent over a guidewire (13). With time, there was concern that the guidewire pushes the small bowel away from the stomach during stent deployment, increasing the risk of misdeployment. For safety, a guidewire can be preloaded within the LAMS delivery system, only to be used as a salvage maneuver in the event of stent misdeployment (SM) (20).

This technique is considered to be ideal since there are fewer steps and less risk of pushing away the small bowel during LAMS deployment without a guidewire. Challenges include the inability to puncture small bowel despite cautery (21). This can be overcome by using purecut current. Inadequate distention of bowel or rapid dissipation of saline can also occur, which can be treated with glucagon administration (21).

Device-assisted techniques

With these techniques, devices such as balloon catheters, nasoenteral tubes or ultraslim gastroscopes are used to reliably identify and target the small intestine. If an ultrathin gastroscope can be advanced across the stenosis, it can be used to distend the small bowel with saline to facilitate puncture (22). Otherwise, a guidewire can be advanced through a gastroscope and beyond the ligament of Treitz, either with direct visualization and/or with fluoroscopic guidance. A dilating balloon, biliary extraction balloon or nasoenteral catheter is then advanced over the wire with subsequent removal of the scope and the guidewire. Contrast is then injected directly into the balloon or contrast mixed with saline and methylene blue can be used to distend the jejunal lumen through the nasoenteral catheter. The echoendoscope is then positioned in the stomach and a loop of bowel can be targeted echoendoscopically and fluoroscopically (Figure 1).

Figure 1 Images of various steps of EUS guided gastroenterostomy. (A) Fluoroscopic image of guidewire advanced across stenosis with a gastroscope. (B) Fluoroscopic image of nasobiliary drain and EUS scope positioning. (C) Fluoroscopic image of small bowel puncture with a 19-gauge needle and subsequent enterogram. (D) EUS image of distended small bowel loop. (E) EUS image of the distal flange in the loop of small bowel. (F) Endoscopic image of the proximal flange deployment in the stomach with drainage of methylene blue. (G) Contrast examination through the lumen-apposing metal stent. (H) Endoscopic image of proximal flange in the stomach. EUS, endoscopic ultrasound.

The use of balloon catheters has been commonly described, particularly in early studies. In this method, an endoscope is used to pass a guidewire into the proximal jejunum beyond the region of obstruction. With the guidewire in place, the endoscope is withdrawn and under fluoroscopic guidance, a large dilating balloon (typically 18–20 mm in diameter) is advanced over the wire into the jejunum (21). A linear echoendoscope is positioned in the stomach, and a 19G FNA needle is used to puncture the inflated balloon. A second guidewire is then advanced downstream into the jejunum. The LAMS can then be deployed over the second guidewire to create a gastroenterostomy. Challenges with this technique include difficulty advancing a balloon catheter into the jejunum due to looping, which can be managed using forceps or an overtube (21). Alternatively, after the loop of bowel is punctured, a guidewire can be advanced through the needle and either by coiled within a balloon or using a snare or stone retrieval basket within the jejunum (23). The guidewire is pulled out through the patient’s mouth and the stent can be deployed with traction using a “rendezvous” technique. The major limitations of this approach stems from the need for frequent device exchanges, difficulty in passage of a large balloon catheter or ability to capture the second guidewire (21).

EUS-guided balloon-occluded gastroenterostomy bypass (EPASS)

The EPASS technique was first described in 2013 by Itoi and colleagues as a modification of the direct technique (24). This method is predicated on a novel device equipped with a double-balloon overtube (Tokyo Medical University type, Create Medic Co., Ltd., Yokohama, Japan) that is advanced into the jejunum using a double balloon enteroscope to avoid looping of the balloon catheter within the stomach. Once in position, two balloons placed 20 cm apart are inflated with contrast and saline material which allow for the anchoring of a small bowel segment in close proximity to the gastric wall. Following double balloon inflation, the bowel between the two balloons is filled with a saline and contrast to distend the small bowel. An echoendoscope is then advanced into the stomach and used to localize the distended jejunal lumen between the two balloon catheters. A cautery-enhanced LAMS is then deployed without the need for 19G needle puncture for small bowel confirmation. This technique is unique in that it allows for fixation of a small bowel target, provides segmental small bowel distention and fixation, and mitigates risk of SM or deployment within the colon (21). The main limitations are the requirement of a novel device which is not yet commercially available and the multi-step process it entails. This technique may not be successful if the duodenum and proximal jejunum aren’t in close proximity to the gastric wall (18).

Retrograde EUS-enterogastrostomy

The retrograde technique is a modification of the rendezvous method with the main distinction being the directionality of LAMS deployment. In this technique, the LAMS is deployed on the gastric side first with the scope positioned in the jejunum beyond the region of obstruction and is essentially an enterogastrostomy (25). As in the traditional method, a gastroscope is used to pass a guidewire beyond the region of obstruction into the proximal jejunum. A large dilating balloon is then passed over the guidewire into the jejunum. A linear echoendoscope equipped with a 19G FNA needle is used to puncture the balloon and pass a second guidewire which is either trapped in the balloon or captured with a snare/stone retrieval basket. The second guidewire is then pulled back beyond the region of obstruction and secured outside of the mouth. A therapeutic endoscope or linear echoendoscope is advanced over the guidewire, traversing the region of obstruction and positioned at the duodenal/jejunal insertion point in preparation for LAMS deployment. The LAMS is subsequently deployedfrom the enteral side. The main advantage of this technique is that the stomach is a larger, fixed target for LAMS deployment (18,25). The stomach is less likely to be pushed away, and the fluoroscopic view of the stomach allows for easier deployment (18). In the antegrade approach, one common concern is that the small bowel is a smaller, mobile target that can easily result in SM due to invagination of the small bowel during transgastric puncture. The main limitation of this technique is the feasibility of passing a therapeutic endoscope or echoendoscope beyond the region of obstruction which has the added risk of perforation during scope advancement (18).

Retrograde EUS-enterogastrostomy is less commonly performed in clinical practice due to the technical limitations encountered with advancement of an echoendoscope beyond the region of obstruction. In 2021, Kesar et al. published a retrospective multicenter study comparing antegrade and retrograde EUS-GE techniques (26). Clinical success was found to be comparable in both groups however the study included nearly three times the number of patients in the anterograde group (34 patients) as compared to the retrograde group (12 patients) (26).

NOTES-GE

NOTES predates the introduction of cautery enhanced LAMS (15). In this technique, the gastric wall is punctured using a 19-gauge needle under EUS guidance. A guidewire is advanced through the needle into the peritoneal cavity in close proximity to the ligament of Treitz. The echoendoscope is removed while maintaining the guidewire in place and a double-channel endoscope is advanced over the wire into the gastric lumen. A needle knife is used to create an incision through the gastric wall. The incisional tract is dilated to facilitate advancement of the scope into the peritoneal cavity. A segment of jejunum is identified and a small incision is made using the needle-knife. A guidewire is advanced into the jejunum and a LAMS is then introduced over the wire into the jejunum. The distal flange is deployed within the jejunum and the gastroscope is withdrawn into the gastric lumen with subsequent deployment of the proximal flange. Post-procedurally, patients are often hospitalized overnight. An upper GI series can be performed to evaluate for leak and stent patency, stent migration, but is not standard or necessary if a patient is clinically well (18).

Outcomes

A summary of the previously published major studies is listed in Table 1. The overall technical success ranges from 80-100% and clinical success rates ranging from 74–100%, regardless of indication or technique. Adverse events range from 0–30% and include misdeployed stent, bleeding, gastric leak, peritonitis, sepsis, stent ingrowth, erosion of stent, fistula, ulcer, and DVT/PE.

Barthet and colleagues reported the first case series of EUS-GE using a NOTES technique for LAMS placement in three patients (15). This technique was not widely adopted due to complexity. The first retrospective case series in the US utilizing LAMS for EUS-GE was published in 2015 by Khashab and colleagues (14). They reported LAMS placement in 10 patients (7 benign and 3 malignant GOO), in which all patients underwent placement of a 15 mm × 10 mm LAMS under either direct or balloon-assisted technique. Technical and clinical success was achieved in 90% of patients with no reported adverse events or symptom recurrence (14).

Subsequently, the first prospective clinical study on the EPASS technique was published in 2016 by Itoi et al. (19). A total of 20 patients with malignant GOO underwent 15 mm LAMS placement with a technical and clinical success rate of 90%. Adverse events occurred in 2 patients (10%) in which SM occurred. In this series, the authors note that multiple procedural steps may contribute to procedural challenges and suggest that over-the-wire LAMS deployment may result in pushing the jejunum away from the gastric wall (19). When a one-step EPASS technique was employed, success rate of this procedure increased from 82% to 100%.

In 2016, Tyberg et al. published a multicenter retrospective study with various EUS-GE techniques employed (27). A total of 26 patients (9 benign and 17 malignant GOO) were included with novel methods described including nasobiliary catheter employment, hybrid rendezvous with an ultra-thin gastroscope and salvage strategies for LAMS misdeployment. Overall, technical success was reported in 92% of patients. The only technical failures were related to SM which occurred in 27% of cases (7 of 26 patients). Endoscopic salvage was able to be achieved with the aid of fully covered self-expanding metal stents in 5 of the 7 patients (71%).

Adverse events associated with EUS-GE are well described in the literature particularly given the degree of technical expertise required in this novel procedure. In an effort to establish a classification system associated with SM, a 2022 study by Ghandour and colleagues proposed a new system to characterize SM into four types (43). SM is defined based on the LAMS flange and location associated with the misdeployment. The overall rate of SM was 9.85% with the majority of cases able to be managed endoscopically. The majority of misdeployments (63%) were characterized as Type 1, with the proximal flange deployed within the stomach and the distal flange within the peritoneum. In these instances, 90% were able to be salvaged endoscopically. Type 2 SM (30.4%) were characterized as the same, but with a visible enterostomy seen endoscopically or fluoroscopically. 93% of these cases were managed endoscopically. Type 3 SM (2%) was described as the proximal flange in the peritoneum and the distal flange in the jejunum. This patient required surgical intervention and ultimately died. Type 4 SM (4.3%) is a gastrocolonic fistula creation, which was managed endoscopically. Surgical intervention due to misdeployment was comparatively low (10.9%) relative to past studies and perhaps reflects the greater degree of endoscopic salvage strategies being employed today (43).

Adverse events apart from SM are also well described in the literature. Other potential procedural complications include peritonitis, sepsis, refeeding syndrome, bleeding, anastomotic leaks and GOO recurrence (8,27,35,36,38). The risk of these alternative adverse events represents a minority of cases in the described studies and overall represents less than 10% of cases (Table 1). In general, the possibility of encountering an adverse event may be mitigated by ensuring appropriate patient selection, proficient endoscopist expertise, routine use of prophylactic antibiotics and performance of cases under general anesthesia. Factors such as peritoneal carcinomatosis and ascites, while not absolute contraindications to performance of EUS-GE, are thought to contribute to the likelihood of procedural complications (36,44,45).

Discussion

Over the past 10 years, robust data validate that EUS-GE is an effective and minimally invasive treatment option for patients with both benign and malignant causes of GOO. High technical and clinical success rates are comparable to surgical and endoscopic alternatives. Various studies demonstrate reduced morbidity, fewer reintervention rates and decreased frequency of treatment delay as compared to surgical gastrojejunostomy and enteral stenting (28,34,42). While this option is promising, further studies comparing the various techniques of EUS-GE are needed since there is currently no standardization and is seldomly performed outside of expert centers. Additionally, developments in EUS-GE and supplementary prospective studies are needed to focus on identifying appropriate candidates, simplify procedural challenges and minimize adverse events.

Comparative data between EUS-GE, enteral stenting and surgical gastroenterostomy is an area of considerable interest. Several retrospective studies have demonstrated that EUS-GE is superior in terms of safety and efficacy while maintaining lower rates of adverse events as compared to surgical gastrojejunostomy (38). Khashab and colleagues reported a multi-center retrospective comparative study of EUS-GE and open gastrojejunostomy in patients with malignant GOO (28). While the technical success rate was lower in the EUS-GE group (87% vs. 100%), the clinical success rate was not significantly different (87% vs. 90%) and the rate of adverse events was lower in the EUS-GE group (16% vs. 25%). There were no significant differences in recurrent GOO (3% vs. 14%) and time to reintervention (88 vs. 121 days), between the two groups (28). Perez-Miranda et al. also reported a multi-center retrospective comparative review of EUS-GE and laparoscopic gastrojejunostomy in patients with both benign and malignant GOO (30). There was no significant difference in technical and clinical success rates, however the rate of adverse events was significantly lower in the EUS-GE group (12% vs. 41%) as well as less expensive ($4,905.50 vs. $14,778.80) (30). Similarly, Bronswijk et al. reported a multi-center, retrospective analysis of EUS-GE and laparoscopic GE for patients with GOO that demonstrated reduced time to oral intake, shorter mean-hospital stays, and a lower rate of adverse events associated with EUS-GE (38).

With respect to EUS-GE and enteral stenting, several retrospective studies comparing the two modalities have demonstrated that EUS-GE is comparable in terms of efficacy and safety with notably better outcomes related to symptom recurrence and reintervention rates (31,46,47). Chen et al. reported a multi-center retrospective comparative study between EUS-GE and enteral stenting in patients with malignant GOO (31). There was no difference in technical success (86.7% vs. 94.2%), clinical success (83.3% vs. 67.3%), and rate of adverse events (16.7% vs. 11.5%) amongst the two groups (31). Most notably, the recurrence of GOO symptoms and the need for reintervention were significantly lower in the EUS-GE group (4% vs. 28.65) (31). In 2019, Ge et al. published a study comparing EUS-GE and enteral stenting in 100 consecutive patients, 22 of whom underwent EUS-GE (33). A greater number of adverse events were noted in the enteral stent group, with 32% of patients in the enteral stent group having symptom recurrence most commonly due to stent failure requiring repeat intervention (33). Perez-Cuadrado-Robles et al. reported their single-center experience with EUS-GE in patients with and without prior ES placement (46). Twenty-eight patients with prior ES and 13 without prior ES were included in the study. There was no difference between the groups for technical success (92.3% vs. 86.7%). Clinical success was attained in all patients with technical success except for two patients with adverse events and one with carcinomatosis. The diet progression was quicker in patients with a previous ES, but the GOO score and nutritional status were comparable in the long term. Overall, current trends suggest that EUS-GE may be superior to both enteral stenting and surgical gastrojejunostomy in terms of efficacy and safety while allowing for prolonged stent patency and shorter hospital stay.

Evolving iterations of EUS-GE methods stem from the need to simplify procedural steps, reduce intraprocedural time, and ultimately reduce the risk of intraprocedural complications. Current published literature demonstrates promising results with technical and clinical success achieved in >90% of patients regardless of the technique employed (8,16,38). Comparative data on the various employed techniques are limited, but nonetheless needed to establish a consensus protocol to provide the highest level of technical success (32). Chen et al. compared the efficacy and safety of the direct technique with the balloon-assisted technique, but there were no significant differences between the two groups in regards to the technical and clinical success, adverse events, need for reintervention, or survival however intraprocedural time was significantly shorter with the direct technique (32). Wannhoff and colleagues reported retrospective data on factors associated with successful direct EUS-GE (36). The distance between the two-lumen connected with the LAMS was substantially shorter in patients with successful procedures, and this distance was the only predictor of success on multivariate analysis (36). Additionally, they demonstrated that the presence and degree of ascites have a direct effect on procedural success with those patients with moderate or severe ascites having considerably lower technical success (43%) (36). In 2021, Basha and colleagues reported 12 patients with ascites who underwent EUS-GE for malignant GOO (45). There was no significant difference in technical success, clinical success, mean procedural time and adverse events in patients with ascites. However, the median survival time was significantly lower in patients with ascites (36 vs. 290 days) (45). Mahmoud et al. reported EUS-GE in 24 patients with ascites (44). Technical success was attained in 91.7% of patients, but a higher rate of adverse events was noted in patients with ascites as compared to those without ascites (37.5% vs. 19.4%, P=0.13). Four patients with ascites (16.6%) developed clinical evidence of peritonitis or sepsis post-EUS-GE (44). The efficacy of EUS-GJ in the presence of ascites is promising; however, the safety profile remains concerning given the high rates of adverse events, namely peritonitis and sepsis despite antibiotics and pre-procedural therapeutic paracentesis.

Long-term follow-up data is also needed to understand stent durability and standardization of stent revision or removal. Kerdsirichairat et al. studied 57 patients who underwent EUS-GE utilizing the direct technique, with a median follow up of 196 days in the malignant GOO group and 319 days in the benign group (34). Technical and clinical success rates were achieved in 93% and 89%, respectively. Eight of the 53 (15.1%) patients required unplanned reintervention, two of whom had stent occlusion and six had patent stents (34). Jaruvongvanich and colleagues reported a retrospective comparative study of 436 patients undergoing EUS-GE, ES or surgical GE at two academic institutions (42). Rates of reintervention of the EUS-GE group were lower than in the ES and surgical GE groups (0.9%, 12.2%, 13.7%). Technical success rates were similar, while clinical success was highest in the EUS-GE group. The EUS-GE group had a shorter length of stay and a lower rate of adverse events during the mean follow-up of 185 days (42). Irani et al. described occurrences of stent induced ulcerations and granulation tissue hypertrophy causing structuring in their series of LAMS used to treat benign gastrointestinal strictures (48). Taibi et al. reported a case of delayed perforation of a jejunal loop adjacent to the LAMS 6 months after an EUS-GE was performed in a patient with cystic duodenal dystrophy. In the majority of studies, symptom recurrence and need for reintervention occurred in <10% of cases (49). Additionally, with respect to stent durability, one longitudinal study following patient outcomes for over 6 months demonstrated an overall reintervention rate of 15% (34). In the 8 patients that required reintervention, only two patients had stent occlusion with the remaining patients demonstrating evidence of symptomatic gastroparesis that was managed with promotility agents (34).

EUS-GE has also been reported in benign diseases, and the patency of the LAMS has been reported for more than a year in some patients (16,35). In 2018, Chen et al. reported a retrospective, multi-center study of 26 patients with EUS-GE for benign causes of GOO (16). Technical success was reported in 96.2% and clinical success in 84%. Clinical failures were attributed to gastroparesis and required alternate means of nutrition or surgical intervention. In one patient with clinical failure, the LAMS was removed after 88 days with subsequent development of a gastric leak requiring surgery. One patient underwent unplanned reintervention due to stent occlusion with food that was successfully treated with endoscopic stent cleaning and two patients underwent elective LAMS removal (16). In 2020, James and colleagues published their series on EUS-GE in benign disease, reporting that surgery was avoided in 83.3% of patients and regression of the benign stricture allowed for LAMS removal in most patients over time (35). EUS-GE may be a promising modality in benign GOO, particularly in patients who have failed balloon dilation or when it is not technically feasible (16) however the long-term effects of an indwelling LAMS and safety of its removal still need to be elucidated.

EUS-GE has been described for the treatment of afferent limb syndrome, which occurs after gastrointestinal surgery and causes intestinal dilation with resultant biliary obstruction (50,51). In the past, there have been limited treatment options, including various surgical and endoscopic interventions. Endoscopic decompression of the afferent limb is not always technically feasible due to a long enteric segment, completely obstructive mass, tight angulation, or long stricture (9). EUS-GE may be useful in treating this syndrome, but consideration must be taken in terms of the proximity of the targeted small bowel loop to the gastric wall (9). Brewer-Gutierrez et al. described a multicenter study of EUS-enteroenterostomy for 18 patients with afferent loop syndrome (29). Resolution of symptoms was observed in 88.9% of patients, and improvement to enable hospital discharge was found in 11.1% of patients. Technical success was achieved in 100% of the patients, with a mean procedure time of 29.7 minutes. Compared to enteroscopy-assisted stent placement, patients treated with EUS-GE required fewer interventions (16.6% vs. 76.5%) (29).

Additionally, in cases of both GOO as well as biliary obstruction, single session EUS guided therapies have been shown to be promising. Brewer-Gutierrez and colleagues presented the first case of double endoscopic bypass in patients with both GOO and biliary obstruction (29). Seven patients with malignant GOO and biliary obstruction underwent EUS-GE and EUS-BD during the same session or on separate occasions with optimal results. This single-session technique is advantageous because the two bypasses are not across the tumor, so long-term patency can be obtained without stent occlusion due to tumor invasion (29). Vanella et al. reported experience at three tertiary academic centers in 93 patients with combined biliary obstruction and GOO resulting in 103 procedure combinations (52). Over the 5-year study period, they found an increase in EUS-GE and EUS-guided choledochoduodenostomy procedures with a decrease in enteral stent and transpapillary metal stent placement. It remains unclear which combination of procedures is ideal, but it was confirmed that combinations including enteral stenting led to higher primary clinical failure and stent dysfunction (52). In a limited sample, EUS-GE combined with EUS hepaticogastrostomy showed the lowest risk of stent dysfunction followed by EUS-GE and transpapillary SEMS, while EUS-choledochoduodenostomy showed a higher risk, particularly when combined with enteral stenting (52).

Irani and colleagues described EUS-duodenojejunostomy or EUS-jejunojejunostomy for difficult EUS-GE cases, notably in patients with surgically altered anatomy, where there is intervening colon, a long distance between the gastric wall and small bowel, or adhesions trapping the small bowel to the right side of the abdomen. In these cases, the echoendoscope is in the long position and stent deployment can be challenging, so the scope needs to be withdrawn into the stomach, advancing the LAMS catheter into puncturing position, then readvancing the scope into the duodenum or jejunum to allow for successful deployment (53).

To date, despite the advances in interventional endoscopy, EUS-GE is seldomly performed outside of expert centers. Given the significant intraprocedural complications that can occur, extensive experience with therapeutic EUS is required to mitigate the risk of adverse events. The most commonly encountered adverse event is attributable to SM requiring knowledge of LAMS salvage techniques. In nearly all cases, misdeployment can be managed endoscopically, however expertise in NOTES is required as well as the use of bridging stents and closure devices. One of the most challenging aspects to this procedure is successful deployment of the LAMS. To avoid the instance where small bowel is pushed away before the cautery tip has pierced the small bowel, Ghandour and colleagues suggest using pure cut cautery at a slightly higher wattage than recommended by the manufacturer, while slowly advancing the tip of the catheter through the gastric wall so that when it impacts the small bowel, its slow advancement does not push the mobile small bowel from the cautery tip (43,54). When stent deployment occurs, salvage maneuvers such as overlapping LAMSs or fully-covered, 20 mm through-the-scope self-expanding esophageal metal stents can be used (54). James and colleagues reported a case of Type 1 misdeployed LAMS, with the distal flange within the peritoneum. The LAMS was dilated to 15 mm with a through-the-scope balloon dilator, and the EUS scope was advanced into the peritoneum. The targeted bowel was then brought into close proximity, and repeated puncture of the jejunum with successful enterogram was performed with successful deployment of a second 20 mm LAMS (54).

Given the complexity of this procedure, endoscopic experience and learning curve encountered to master EUS-GE has been studied. One prospective study conducted over three years on 23 patients demonstrated a learning rate of 7 cases, however some limitations included an experienced single-operator and lack of standardized techniques (55). Jovani et al. demonstrated that a single operator was able to achieve proficiency after approximately 25 cases and mastery after 40 cases based upon duration of procedure and adverse events (56). Single-operator assessments cannot be extrapolated to all endoscopists, and thus is a limitation of both of these studies. While EUS-GE remains a technically challenging procedure, present day endoscopists have the advantage of learning from early experience with EUS-GE as well as evolving techniques that may simplify the procedure and minimize adverse events (57). As EUS-GE continues to be an evolving technique that requires a multidisciplinary approach with experienced endoscopy nurses and technicians, it remains difficult to assess a generally applicable competency rate. Predictably, most cases with SM correlated to endoscopic experience with the majority occurring in the first 13 cases performed by the operator (43). For those attempting to implement EUG-GE into their armamentarium, they should be proficient in LAMS deployment (58). Perez-Miranda suggested that a sequence of 4 technical skills is necessary to master EUS-GE: (I) to adequately distend the target small bowel distal to the stricture using instillation of fluid; (II) to correctly identify the target small bowel under EUS from the stomach; (III) to smoothly insert and deploy a cautery-enhanced LAMS across the stomach and small bowel walls; and (IV) to assess for LAMS misdeployment and apply basic salvage strategies in such cases. Appropriate multidisciplinary discussion and surgical back up should be available (57).

Conclusions

Despite the robust data on various applications of EUS-GE, there is yet to be an established protocol for the management of GOO. In deciding between EUS-GE, enteral stenting and surgical gastroenterostomy for the management of GOO, consideration should be given to appropriate indication (benign vs malignant etiology), available technical expertise, patient life expectancy, informed consent and relative contraindications (e.g., ascites, frail patient status, carcinomatosis).

EUS guided-gastroenterostomy has clearly been demonstrated to be a promising endoscopic modality for both benign and malignant indications for GOO. Additional research for optimization of techniques and prospective randomized data comparing EUS-GE with enteral stents and surgical gastrojejunostomy are needed.

Acknowledgments

Funding: None.

Footnote

Peer Review File: Available at https://tgh.amegroups.com/article/view/10.21037/tgh-23-51/prf

Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://tgh.amegroups.com/article/view/10.21037/tgh-23-51/coif). J.W. reports receiving consulting fee from Boston Scientific. The other author has no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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