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AGA Clinical Practice Update on the Optimal Management of the Malignant Alimentary Tract Obstruction: Expert Review

  • Osman Ahmed
    Affiliations
    Department of Medicine, University of Toronto, Toronto, Ontario, Canada
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  • Jeffrey H. Lee
    Correspondence
    Reprint requests Address requests for reprints to: Jeffrey H. Lee, MD, MPH, FASGE, FACG, AGAF, Endoscopy Center, Department of Gastroenterology, Hepatology and Nutrition, University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Avenue, Houston, Texas 77030. fax: (713) 563-4408.
    Affiliations
    Department of Gastroenterology, M. D. Anderson Cancer Center, Houston, Texas
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  • Author Footnotes
    b Authors share co-senior authorship.
    Christopher C. Thompson
    Footnotes
    b Authors share co-senior authorship.
    Affiliations
    Division of Gastroenterology, Hepatology and Endoscopy, Brigham and Women’s Hospital, Boston, Massachusetts
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  • Author Footnotes
    b Authors share co-senior authorship.
    Ashley Faulx
    Footnotes
    b Authors share co-senior authorship.
    Affiliations
    Department of Medicine, Case Western Reserve University, and University Hospitals, Cleveland Medical Center, Cleveland, Ohio
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  • Author Footnotes
    b Authors share co-senior authorship.
Published:April 01, 2021DOI:https://doi.org/10.1016/j.cgh.2021.03.046

      Background & Aims

      The purpose of this expert review is to describe the current methodologies available to manage malignant alimentary tract obstructions as well the evidence behind the various methods (including their efficacy and safety), indications, and appropriate timing of interventions.

      Methods

      This is not a formal systematic review but is based on a review of the literature to provide best practice advice statements. No formal rating of the quality of evidence or strength of recommendation is carried out.

      Best Practice Advice 1

      For all patients with alimentary tract obstruction, the decision about specific interventions should be made in a multidisciplinary setting including oncologists, surgeons, and endoscopists and take into account the characteristics of the obstruction, patient’s expectations, prognosis, expected subsequent therapies, and functional status.

      Best Practice Advice 2

      For patients who present with esophageal obstruction from esophageal cancer and who are potential candidates for resection or chemoradiation, clinicians should not routinely insert a self-expanding metal stent (SEMS) without multidisciplinary review because of high rates of stent migration, higher morbidity and mortality, and potentially lower R0 (microscopically negative margins) resection rates.

      Best Practice Advice 3

      For patients who present with esophageal obstruction from esophageal cancer who are potential candidates for resection and who have concerns of malnutrition, clinicians may consider the use of enteral feeding tubes (via nasogastric or percutaneous route). Clinicians should be aware of the potential risk of abdominal wall tumor seeding as well as making subsequent gastric conduit formation difficult with percutaneous endoscopic gastrostomy placement.

      Best Practice Advice 4

      For patients who present with esophageal obstruction from esophageal cancer who are not candidates for resection, clinicians should consider either SEMS insertion or brachytherapy as sole therapy or in combination. Clinicians should not consider the use of laser therapy or photodynamic therapy because of the lack of evidence of better outcomes and superior alternatives.

      Best Practice Advice 5

      For patients with malignant esophageal obstruction who are undergoing SEMS placement, clinicians should use a fully covered or partially covered SEMS and not an uncovered SEMS, with consideration of a stent-anchoring/fixation method.

      Best Practice Advice 6

      For patients with gastric outlet obstruction who have a life expectancy greater than 2 months, have good functional status, and who are surgically fit, surgical gastrojejunostomy should be considered.

      Best Practice Advice 7

      For patients with gastric outlet obstruction who are undergoing surgical gastrojejunostomy, a laparoscopic approach is favored over an open approach because of lower blood loss and shorter hospital stay.

      Best Practice Advice 8

      For patients with gastric outlet obstruction who are not candidates for gastrojejunostomy (surgical or endoscopic ultrasound-guided), clinicians should consider the insertion of an enteral stent.

      Best Practice Advice 9

      Enteral stents should not be used in patients with multiple luminal obstructions or severely impaired gastric motility because of the limited benefit in these scenarios. Clinicians can consider placement of a venting gastrostomy in these patients.

      Best Practice Advice 10

      Depending on the experience of the endoscopist, endoscopic ultrasound-guided gastrojejunostomy is an acceptable alternative to surgical gastrojejunostomy and enteral stent placement. Clinicians should be aware that there are currently no dedicated Food and Drug Administration–approved devices for endoscopic ultrasound–guided gastrojejunostomy.

      Best Practice Advice 11

      For patients with malignant colonic obstruction who are candidates for resection, insertion of SEMS is a reasonable choice as a “bridge to surgery” to allow for one-stage, elective resection.

      Best Practice Advice 12

      For patients with malignant colonic obstruction who are not candidates for resection, either SEMS placement or a diverting colostomy are reasonable choices depending on the patient’s goals and functional status.

      Best Practice Advice 13

      SEMS is a reasonable option for patients with proximal (or right-sided) malignant obstructions, both as a “bridge to surgery” and in the palliative setting.

      Best Practice Advice 14

      SEMS placement is a reasonable alternative for patients with extracolonic malignancy who are not candidates for surgery, although their placement is more technically challenging, clinical success rates are more variable, and complications (including stent migration) are more frequent.

      Abbreviations used in this paper:

      AE (adverse event), ECM (extracolonic malignancy), ECOG (Eastern Cooperative Oncology Group), ERCP (endoscopic retrograde cholangiopancreatography), EUS-GE (endoscopic ultrasound-guided gastroenterostomy), FCSEMS (fully covered self-expanding metal stents), GJ (gastrojejunostomy), GOO (gastric outlet obstructions), MATO (malignant alimentary tract obstructions), MCO (malignant colonic obstructions), PCSEMS (partially covered self-expanding metal stents), PDT (photodynamic therapy), PEG (percutaneous endoscopic gastrostomy), SEMS (self-expanding metal stents), UCSEMS (uncovered self-expanding metal stents)
      Malignant alimentary tract obstructions (MATOs) are clinically significant blockages of the gastrointestinal tract that can occur in a variety of malignancies. The most common locations include the distal esophagus/gastric cardia, gastric outlet, and colonic. They can cause debilitating symptoms and result in life-threatening emergencies if not dealt with promptly. The approach to the management of MATOs should ideally be done in a multidisciplinary setting that includes oncologists, surgeons, and endoscopists and takes into account the characteristics of the obstruction, patient’s expectations, prognosis, expected subsequent therapies, and functional status.
      • Krouse R.S.
      The international conference on malignant bowel obstruction: a meeting of the minds to advance palliative care research.
      The purpose of this clinical update is to describe the current methodologies available to manage MATOs as well as the evidence behind the various methods (including their efficacy and safety), indications, and appropriate timing of interventions.
      This expert review was commissioned and approved by the AGA Institute Clinical Practice Updates Committee and the AGA Governing Board to provide timely guidance on a topic of high clinical importance to the AGA membership and underwent internal peer review by the Clinical Practice Updates Committee and external peer review through standard procedures of Clinical Gastroenterology and Hepatology.

      Best Practice Advice 1

      For all patients with alimentary tract obstruction, the decision about specific interventions should be made in a multidisciplinary setting including oncologists, surgeons, and endoscopists and take into account the characteristics of the obstruction, patient’s expectations, prognosis, expected subsequent therapies, and functional status.

       Esophageal and Gastric Cardia Obstruction

      The clinical presentation for esophageal cancers is variable, but almost three-fourths of patients present with dysphagia due to obstruction.
      • Daly J.M.
      • Fry W.A.
      • Little A.G.
      • et al.
      Esophageal cancer: results of an American College of Surgeons Patient Care Evaluation Study.
      Malnutrition is another major concern and has important implications in patient management and overall survival.
      • Bower M.R.
      • Martin 2nd, R.C.G.
      Nutritional management during neoadjuvant therapy for esophageal cancer.
      ,
      • Halliday V.
      • Kierczuk G.
      • Madhusudan S.
      • et al.
      Screening for malnutrition: implications for upper gastrointestinal cancer services.
      In addition, ongoing dysphagia and loss of appetite are independent predictors of poor health-related quality of life in patients with esophageal cancers.
      • Darling G.E.
      Quality of life in patients with esophageal cancer.

       Esophageal and Gastric Cardia Obstruction in Resectable Patients

      Although evolving, the approach to the management of malignant obstructions in resectable patients is still controversial. The most seminal study in the role of esophageal self-expanding metal stents (SEMS) as a bridge to surgery compared 38 patients who underwent SEMS with 152 propensity-score matched controls. It found that patients who underwent SEMS had higher mortality and morbidity as well as lower R0 resections, time to recurrence, and overall survival.
      • Mariette C.
      • Gronnier C.
      • Duhamel A.
      • et al.
      Self-expanding covered metallic stent as a bridge to surgery in esophageal cancer: impact on oncologic outcomes.
      Likewise, a previously published narrative review on the role of esophageal SEMS in the neoadjuvant setting (16 studies involving 383 patients) found that overall stent migration occurred in 29.9% of patients, chest pain in 15.6%, and tumor ingrowth in 2.2%. Five patients (1.5%) had an esophageal perforation.
      • Huddy J.R.
      • Huddy F.M.S.
      • Markar S.R.
      • et al.
      Nutritional optimization during neoadjuvant therapy prior to surgical resection of esophageal cancer: a narrative review.
      One study cited post-insertion 30-day mortality at 10%.
      • Pellen M.G.C.
      • Sabri S.
      • Razack A.
      • et al.
      Safety and efficacy of self-expanding removable metal esophageal stents during neoadjuvant chemotherapy for resectable esophageal cancer.
      On the basis of these studies, the most recent European guidelines do not recommend placement of an esophageal stent as a bridge to surgery.
      • Lordick F.
      • Mariette C.
      • Haustermans K.
      • et al.
      Oesophageal cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up.
      Because of the high risk of adverse events (AEs) with SEMS placement in the neoadjuvant setting, enteral feeds have been favored. Currently, the main types of enteral feeds in esophageal and gastric cardia obstruction patients include nasogastric/nasojejunal tubes, percutaneous gastrostomy tubes (PEGs) (inserted endoscopically, surgically, or by radiology), percutaneous gastrostomy with jejunal extension, or percutaneous jejunostomy tubes.
      • Toussaint E.
      • Van Gossum A.
      • Ballarin A.
      • et al.
      Enteral access in adults.
      Previous studies examining the role of enteral feeding have demonstrated good technical success, tolerability, and weight gain. AEs included tube blockage, dislodgement, and infection.
      • Huddy J.R.
      • Huddy F.M.S.
      • Markar S.R.
      • et al.
      Nutritional optimization during neoadjuvant therapy prior to surgical resection of esophageal cancer: a narrative review.
      ,
      • Lorimer P.D.
      • Motz B.M.
      • Watson M.
      • et al.
      Enteral feeding access has an impact on outcomes for patients with esophageal cancer undergoing esophagectomy: an analysis of SEER-Medicare.
      In addition, enteral feeds do not improve the patient’s dysphagia or ability to tolerate oral intake. Of note, there have been concerns about the potential of abdominal wall seeding with the insertion of PEG tubes; however, the majority of the documented cases have been in the setting of head and neck cancers.
      • Cappell M.S.
      Risk factors and risk reduction of malignant seeding of the percutaneous endoscopic gastrostomy track from pharyngoesophageal malignancy: a review of all 44 known reported cases.
      Another caveat is that PEG placement can make subsequent gastric conduit formation in patients undergoing esophagectomy difficult for the surgeon, and therefore, discussion about type of enteral feed should be had with the surgeon before proceeding.

      Best Practice Advice 2

      For patients who present with esophageal obstruction from esophageal cancer and who are potential candidates for resection or chemoradiation, clinicians should not routinely insert a SEMS without multidisciplinary review because of high rates of stent migration, higher morbidity and mortality, and potentially lower R0 (microscopically negative margins) resection rates.

      Best Practice Advice 3

      For patients who present with esophageal obstruction from esophageal cancer who are potential candidates for resection and who have concerns of malnutrition, clinicians may consider the use of enteral feeding tubes (via nasogastric or percutaneous route). Clinicians should be aware of the potential risk of abdominal wall tumor seeding as well as making subsequent gastric conduit formation difficult with PEG placement.

       Esophageal and Gastric Cardia Obstruction in Nonresectable Patients

      For patients with nonoperative esophageal cancer, the options become more varied including esophageal SEMS placement, external radiotherapy, brachytherapy, and chemotherapy. Each of these can be done as a sole intervention or as combination therapy. A systematic review and meta-analysis of 8 randomized controlled trials consisting of 732 patients found that the combination of esophageal stent and either chemotherapy or radiation resulted in more significant relief of dysphagia long-term (more than 5 months) compared with esophageal stent only, but there was no difference in short-term dysphagia (less than 3 months). Combination therapy also had significantly improved overall survival compared with esophageal stent alone, with no other significant differences in terms of AEs between the two, although a large proportion of patients developed chest pain.
      • Lai A.
      • Lipka S.
      • Kumar A.
      • et al.
      Role of esophageal metal stents placement and combination therapy in inoperable esophageal carcinoma: a systematic review and meta-analysis.
      When comparing esophageal stent alone with brachytherapy alone, no significant differences were seen in improvement of dysphagia or overall survival. In terms of AEs, esophageal stent placement resulted in a higher risk for hemorrhage but no difference in fistula formation or perforation.
      • Lai A.
      • Lipka S.
      • Kumar A.
      • et al.
      Role of esophageal metal stents placement and combination therapy in inoperable esophageal carcinoma: a systematic review and meta-analysis.
      Therefore, both brachytherapy as well as SEMS placement are recommended by European guidelines for non-operable malignant obstructions.
      • Spaander M.C.W.
      • Baron T.H.
      • Siersema P.D.
      • et al.
      Esophageal stenting for benign and malignant disease: European Society of Gastrointestinal Endoscopy (ESGE) clinical guideline.
      Alternative endoscopic modalities that have been used to palliate malignant esophageal obstructions include laser therapy, photodynamic therapy (PDT), and the insertion of rigid plastic stents. A large Cochrane review of 53 studies involving 3684 patients examined these different interventions compared with esophageal SEMS and found that all 3 alternative modalities (laser, PDT, and plastic stents) were less effective and had an increased risk of AEs.
      • Dai Y.
      • Li C.
      • Xie Y.
      • et al.
      Interventions for dysphagia in oesophageal cancer.
      Recent studies have also looked at the role of cryoablation (liquid nitrogen by endoscopic spray) for the palliation of dysphagia in unresectable patients. Although the studies have been small and retrospective, they have suggested significant improvements in dysphagia.
      • Kachaamy T.
      • Prakash R.
      • Kundranda M.
      • et al.
      Liquid nitrogen spray cryotherapy for dysphagia palliation in patients with inoperable esophageal cancer.

      Best Practice Advice 4

      For patients who present with esophageal obstruction from esophageal cancer who are not candidates for resection, clinicians should consider either SEMS insertion or brachytherapy as sole therapy or in combination. Clinicians should not consider the use of laser therapy or PDT because of the lack of evidence of better outcomes and superior alternatives.

       Special Considerations

      In terms of SEMS, there is still ongoing debate about the ideal characteristics of a stent, including length, diameter, and type. In terms of length and diameter, ultimately the decision lies with the clinician depending on the severity and length of the stricture encountered. The general thought is to allow for at least 2 cm of margin both proximally and distally from the stricture. A randomized study comparing small (16–18 mm) with large (20–23 mm) diameter stents found no difference in dysphagia improvement, but an increase in recurrent dysphagia, tissue overgrowth, and food bolus obstruction in patients with small-diameter stents. However, hemorrhage and perforation rates were increased in patients with large-diameter stents.
      • Verschuur E.M.L.
      • Steyerberg E.W.
      • Kuipers E.J.
      • et al.
      Effect of stent size on complications and recurrent dysphagia in patients with esophageal or gastric cardia cancer.
      On the basis of the current literature, clinicians should consider the use of larger diameters when the stent crosses the gastroesophageal junction to prevent migration.
      • Law R.
      • Baron T.H.
      Choosing the appropriate esophageal stent for your patient.
      Initial studies comparing uncovered self-expanding metal stents (UCSEMS) with fully covered self-expanding metal stents (FCSEMS) found no difference in initial dysphagia improvement but an increase in recurrent tumor ingrowth and re-interventions in the UCSEMS group.
      • Vakil N.
      • Morris A.I.
      • Marcon N.
      • et al.
      A prospective, randomized, controlled trial of covered expandable metal stents in the palliation of malignant esophageal obstruction at the gastroesophageal junction.
      Therefore, for esophageal and gastric cardia malignant obstructions, FCSEMS or partially covered SEMS (PCSEMS) are generally favored.
      Novel developments to prevent the complications associated with esophageal SEMS placement continue to be developed. Because of the risk of stent migration, a few methods to anchor the stent have been studied. The use of endoscopic suturing has demonstrated effectiveness in reducing stent migration in both neoadjuvant and inoperable settings.
      • Yang J.
      • Siddiqui A.A.
      • Kowalski T.E.
      • et al.
      Esophageal stent fixation with endoscopic suturing device improves clinical outcomes and reduces complications in patients with locally advanced esophageal cancer prior to neoadjuvant therapy: a large multicenter experience.
      ,
      • Law R.
      • Prabhu A.
      • Fujii-Lau L.
      • et al.
      Stent migration following endoscopic suture fixation of esophageal self-expandable metal stents: a systematic review and meta-analysis.
      Similarly, the use of an over-the-scope clip to anchor the stent has also been shown to decrease the rate of migration.
      • Watanabe K.
      • Hikichi T.
      • Nakamura J.
      • et al.
      Feasibility of esophageal stent fixation with an over-the-scope-clip for malignant esophageal strictures to prevent migration.
      Finally, because of the nature of SEMS, gastric contents (food, secretions) can reflux back into the esophagus unimpeded. In fact, gastroesophageal reflux has been reported in 70%–100% of cases with esophageal SEMS placement. Recently, there has been extensive research into the development of anti-reflux mechanisms (including anti-reflux valves); however, a definitive mechanism has yet to be determined.
      • Dua K.S.
      • DeWitt J.M.
      • Kessler W.R.
      • et al.
      A phase III, multicenter, prospective, single-blinded, noninferiority, randomized controlled trial on the performance of a novel esophageal stent with an antireflux valve (with video).

      Best Practice Advice 5

      For patients with malignant esophageal obstruction who are undergoing SEMS placement, clinicians should use a FCSEMS or PCSEMS and not an UCSEMS, with consideration of a stent-anchoring/fixation method.

       Gastric Outlet Obstructions

      Malignant gastric outlet obstructions (GOO) are usually due to stricturing at the level of the pylorus or duodenum. They are most commonly caused by malignancies involving the pancreas, stomach, duodenum, ampulla, or biliary tree (cholangiocarcinoma).
      • Brimhall B.
      • Adler D.G.
      Enteral stents for malignant gastric outlet obstruction.
      The development of GOO generally portends an unfavorable prognosis.
      • Brimhall B.
      • Adler D.G.
      Enteral stents for malignant gastric outlet obstruction.
      The establishment of luminal patency is important in patients with GOO not only to potentially allow resumption of chemoradiation therapies but also for quality of life concerns in patients with intolerable symptoms.
      • Fujitani K.
      • Ando M.
      • Sakamaki K.
      • et al.
      Multicentre observational study of quality of life after surgical palliation of malignant gastric outlet obstruction for gastric cancer.

       Surgical Gastrojejunostomy

      Although open surgical gastrojejunostomy (GJ) was the mainstay of therapy in the past, it has generally been replaced by the advent of laparoscopic GJ. Previous studies have shown significantly lower blood loss and shorter hospital stay with laparoscopic GJ.
      • Bergamaschi R.
      • Mårvik R.
      • Thoresen J.E.
      • et al.
      Open versus laparoscopic gastrojejunostomy for palliation in advanced pancreatic cancer.
      The theoretical benefit of a GJ is that there are fewer limitations in terms of food texture and consistency. The main consideration is that the patient must be well enough to undergo surgery.
      The pivotal study that underlined the ongoing role for surgical GJ was the SUSTENT study, which randomized patients with GOO to either GJ (open or laparoscopic) or enteral stent placement. The study found that although enteral stent placement allowed for earlier food intake, it was offset by the better long-term relief offered by surgical GJ. In addition, patients who underwent stent placement had higher rates of recurrent obstructions and re-intervention. On the basis of that study, the consideration was made that patients with life expectancy more than 2 months who are surgically fit should undergo surgical GJ, whereas those with less should undergo enteral stent placement.
      • Jeurnink S.M.
      • Steyerberg E.W.
      • van Hooft J.E.
      • et al.
      Surgical gastrojejunostomy or endoscopic stent placement for the palliation of malignant gastric outlet obstruction (SUSTENT study): a multicenter randomized trial.
      A more recent retrospective study involving 310 patients found that poor nutritional status, ascites, and poor functional status were independent predictors of clinical failure of a surgical GJ.
      • Jang S.
      • Stevens T.
      • Lopez R.
      • et al.
      Superiority of gastrojejunostomy over endoscopic stenting for palliation of malignant gastric outlet obstruction.
      Similar results were seen in a recent meta-analysis as well as a Cochrane review from 2018, although most of the studies were of low quality.
      • Mintziras I.
      • Miligkos M.
      • Wächter S.
      • et al.
      Palliative surgical bypass is superior to palliative endoscopic stenting in patients with malignant gastric outlet obstruction: systematic review and meta-analysis.
      ,
      • Upchurch E.
      • Ragusa M.
      • Cirocchi R.
      Stent placement versus surgical palliation for adults with malignant gastric outlet obstruction.
      Conventionally, no intervention was performed at the site of the obstruction, and therefore up to 50% of patients who underwent surgical GJ subsequently developed delayed gastric emptying after surgery because of food contents accumulating in the antrum. The technique was therefore modified with the addition of gastric partitioning, either partial or complete, by which access to the antrum was either limited (partial) or excluded (complete) and thus decreasing the rates of delayed gastric emptying.
      • Oida T.
      • Mimatsu K.
      • Kawasaki A.
      • et al.
      Modified Devine exclusion with vertical stomach reconstruction for gastric outlet obstruction: a novel technique.
      A recent retrospective study showed that although gastric partitioning was as safe as conventional GJ, no significant clinical outcome differences were noticed other than a trend of improved solid diet tolerance with partitioning.
      • Ramos M.F.K.P.
      • Barchi L.C.
      • de Oliveira R.J.
      • et al.
      Gastric partitioning for the treatment of malignant gastric outlet obstruction.
      On the other hand, a recent meta-analysis demonstrated improvement in overall oral nutrition and gastric emptying rates with partitioning.
      • Lorusso D.
      • Giliberti A.
      • Bianco M.
      • et al.
      Stomach-partitioning gastrojejunostomy is better than conventional gastrojejunostomy in palliative care of gastric outlet obstruction for gastric or pancreatic cancer: a meta-analysis.

      Best Practice Advice 6

      For patients with GOO who have a life expectancy more than 2 months, have good functional status, and who are surgically fit, surgical GJ should be considered.

      Best Practice Advice 7

      For patients with GOO who are undergoing surgical GJ, a laparoscopic approach is favored over an open approach because of lower blood loss and shorter hospital stay.

       Enteral Stent

      Although enteral stents should not be considered as first-line therapy for high-functioning patients, they still have an important role to play in patients with malignant GOO with poor functional status. Contraindications to enteral stent placement include multiple luminal obstructions (especially if distal to the duodenum), very short life expectancy (less than a few weeks), and evidence of impaired gastric motility (eg, patients with linitis plastica). The benefits of enteral stent placement in these patients are fairly limited.
      • Wai C.T.
      • Ho K.Y.
      • Yeoh K.G.
      • et al.
      Palliation of malignant gastric outlet obstruction caused by gastric cancer with self-expandable metal stents.
      A venting gastrostomy tube should be considered in these patients.
      Enteral stent placement is feasible in most patients. A systematic review from 2007 found 89% clinical success rate with enteral stent placement. In the review, early AEs occurred in 7% of patients and consisted of stent migration, jaundice, and bleeding. Eighteen percent of patients developed late AEs, of which the majority consisted of stent migration or occlusion (from tumor ingrowth or food obstruction). The mean hospital stay was 7 days after insertion, and mean overall survival was 105 days after stent placement.
      • Jeurnink S.M.
      • van Eijck C.H.J.
      • Steyerberg E.W.
      • et al.
      Stent versus gastrojejunostomy for the palliation of gastric outlet obstruction: a systematic review.
      In terms of predictive factors for failure of enteral stents, poor baseline functional status, presence of peritoneal dissemination, and lack of subsequent chemotherapy were found to be predictors of poor outcome.
      • Hori Y.
      • Naitoh I.
      • Hayashi K.
      • et al.
      Predictors of outcomes in patients undergoing covered and uncovered self-expandable metal stent placement for malignant gastric outlet obstruction: a multicenter study.
      A pooled analysis from 2015 demonstrated significantly increased technical and clinical success with PCSEMS compared with UCSEMS as well as an increase in recurrent obstructions from tumor ingrowth with UCSEMS. However, it also demonstrated increased stent migration with PCSEMS.
      • van Halsema E.E.
      • Rauws E.A.J.
      • Fockens P.
      • et al.
      Self-expandable metal stents for malignant gastric outlet obstruction: a pooled analysis of prospective literature.
      A separate meta-analysis found no difference in technical or clinical success but lower rates of occlusion and higher rates of migration with PCSEMS/FCSEMS.
      • Hamada T.
      • Hakuta R.
      • Takahara N.
      • et al.
      Covered versus uncovered metal stents for malignant gastric outlet obstruction: systematic review and meta-analysis.
      One concern with SEMS placement for GOO is the potential risk of covering the ampulla with placement. Although there remains concerns about the ability to perform endoscopic retrograde cholangiopancreatography (ERCP) after enteral stent placement, a previous retrospective study demonstrated an overall 85% technical success rate in achieving biliary drainage by ERCP after enteral stent placement.
      • Staub J.
      • Siddiqui A.
      • Taylor L.J.
      • et al.
      ERCP performed through previously placed duodenal stents: a multicenter retrospective study of outcomes and adverse events.
      In addition, although biliary drainage can by achieved by ERCP in the majority of cases, alternative methods include percutaneous transhepatic cholangiogram drainage or endoscopic ultrasound (EUS)-guided biliary drainage.
      • Uemura S.
      • Iwashita T.
      • Iwata K.
      • et al.
      Endoscopic duodenal stent versus surgical gastrojejunostomy for gastric outlet obstruction in patients with advanced pancreatic cancer.

      Best Practice Advice 8

      For patients with GOO who are not candidates for GJ (surgical or EUS-guided), clinicians should consider the insertion of an enteral stent.

      Best Practice Advice 9

      Enteral stents should not be used in patients with multiple luminal obstructions or severely impaired gastric motility because of the limited benefit in these scenarios. Clinicians can consider placement of a venting gastrostomy in these patients.

       EUS-Guided Gastroenterostomy

      Endoscopic ultrasound-guided gastroenterostomy (EUS-GE) is a novel endoscopic method that allows for the creation of a fistulous tract between the stomach and the jejunum. Using this modality, the aim was to achieve the benefits of a laparoscopic GJ using a less invasive approach and potentially fewer associated AEs. Initial experience with EUS-GE was positive, with a technical and clinical success rate of 90% and no procedure-related AEs, although this was limited to a few expert and experienced endoscopists.
      • Khashab M.A.
      • Kumbhari V.
      • Grimm I.S.
      • et al.
      EUS-guided gastroenterostomy: the first U.S. clinical experience (with video).
      A systematic review and meta-analysis from 2020 including 12 studies with 285 patients found a technical success rate of 92%, with a clinical success rate of 90%. AEs were reported in 12% of patients, with the most common being stent misdeployment.
      • Iqbal U.
      • Khara H.S.
      • Hu Y.
      • et al.
      EUS-guided gastroenterostomy for the management of gastric outlet obstruction: a systematic review and meta-analysis.
      With more widespread adoption of EUS-GE in the management of malignant GOO in recent years, there have been a few studies comparing EUS-GE with enteral stent placement. In one retrospective study, 100 consecutive patients at a single center were identified (78 with enteral stents, 22 with EUS-GE), and they identified higher re-intervention rates with enteral stents compared with EUS-GE. No difference was seen in technical success, but EUS-GE had higher initial clinical success rates. In addition, there was a non-statistically significant trend toward increased AEs with enteral stent placements.
      • Ge P.S.
      • Young J.Y.
      • Dong W.
      • et al.
      EUS-guided gastroenterostomy versus enteral stent placement for palliation of malignant gastric outlet obstruction.
      A multicenter retrospective study of 82 patients found no significant difference in technical success, clinical success, or AEs, but it similarly found that symptom recurrence and re-intervention rates were lower with EUS-GE.
      • Chen Y.-I.
      • Itoi T.
      • Baron T.H.
      • et al.
      EUS-guided gastroenterostomy is comparable to enteral stenting with fewer re-interventions in malignant gastric outlet obstruction.
      Another retrospective study including 54 patients from 4 academic centers in 3 countries found similar efficacy between laparoscopic GJ and EUS-GE, with significantly lower AEs with EUS-GE.
      • Perez-Miranda M.
      • Tyberg A.
      • Poletto D.
      • et al.
      EUS-guided gastrojejunostomy versus laparoscopic gastrojejunostomy: an international collaborative study.
      Overall, although there are promising evidence and growth in the use of EUS-GE, it is still not widely available because of the lack of experienced endoscopists.

      Best Practice Advice 10

      Depending on the experience of the endoscopist, EUS-guided GJ is an acceptable alternative to surgical GJ and enteral stent placement. Clinicians should be aware that there are currently no dedicated Food and Drug Administration–approved devices for EUS-guided GJ.

       Malignant Colonic Obstructions

      Malignant colonic obstructions (MCOs) are usually encountered because of intrinsic colorectal cancer or metastatic deposits from extracolonic malignancies (ECMs). The most common malignancies associated with MCOs are colorectal cancer and gynecological malignancies.
      • Ripamonti C.
      • De Conno F.
      • Ventafridda V.
      • et al.
      Management of bowel obstruction in advanced and terminal cancer patients.
      MCOs are an important clinical condition because of the accompanying significant morbidity and debilitating symptoms.

       Malignant Colonic Obstructions in Resectable Patients

      In patients who are potential candidates for resection, SEMS have been used as a bridge to surgery, allowing for elective surgery (thereby permitting preoperative bowel cleansing, full preoperative staging, and potentially performing a one-stage surgery) rather than emergent surgery. A previous systematic review involving 407 patients in 21 studies showed a technical success rate of 91.9% in SEMS placement as a bridge to surgery. The number of patients who were subsequently able to undergo one-stage surgery was 71.7%. There were 7 perforations (1.7%) and 16 cases of stent migration (3.9%).
      • Sebastian S.
      • Johnston S.
      • Geoghegan T.
      • et al.
      Pooled analysis of the efficacy and safety of self-expanding metal stenting in malignant colorectal obstruction.
      A similar study from 2011 that examined 2 international registries with 182 patients found a technical success rate of 98%, clinical success rate of 94%, and overall AE rate of 7.8% (perforation 3%, stent migration 1.2%). When comparing SEMS with emergency surgery, a meta-analysis of 7 randomized controlled trials with 382 patients found the SEMS group had significantly higher rates of primary anastomosis and lower rates of permanent stoma and overall AEs. No difference in overall survival was noted.
      • Huang X.
      • Lv B.
      • Zhang S.
      • et al.
      Preoperative colonic stents versus emergency surgery for acute left-sided malignant colonic obstruction: a meta-analysis.
      Two similar meta-analyses were performed in 2017 (randomized controlled trials only) and 2019 (both randomized controlled trials and non-randomized controlled trials) and had similar conclusions.
      • Cao Y.
      • Gu J.
      • Deng S.
      • et al.
      Long-term tumour outcomes of self-expanding metal stents as “bridge to surgery” for the treatment of colorectal cancer with malignant obstruction: a systematic review and meta-analysis.
      ,
      • Arezzo A.
      • Passera R.
      • Lo Secco G.
      • et al.
      Stent as bridge to surgery for left-sided malignant colonic obstruction reduces adverse events and stoma rate compared with emergency surgery: results of a systematic review and meta-analysis of randomized controlled trials.
      However, a study from South Korea retrospectively compared SEMS with emergency surgery and found that patients who underwent a SEMS placement that was complicated by a perforation had an odds ratio of 46 to subsequently develop metastasis from seeding (although the study was limited by being single-center and retrospective with a small number of patients and a higher rate of perforation than demonstrated in previous meta-analyses).
      • Kim S.J.
      • Kim H.W.
      • Park S.B.
      • et al.
      Colonic perforation either during or after stent insertion as a bridge to surgery for malignant colorectal obstruction increases the risk of peritoneal seeding.
      Although the evidence for SEMS in left-sided malignant obstructions is growing, there are still concerns about the use of SEMS for right-sided or proximal MCO (proximal to the splenic flexure) because of the technical challenges of SEMS insertion in those areas. One study compared SEMS with emergency surgery for resectable right-sided (or proximal) colorectal cancer and found that SEMS was associated with lower mortality, lower morbidity, and lower rates of permanent stoma.
      • Amelung F.J.
      • de Beaufort H.W.L.
      • Siersema P.D.
      • et al.
      Emergency resection versus bridge to surgery with stenting in patients with acute right-sided colonic obstruction: a systematic review focusing on mortality and morbidity rates.
      For any patient presenting with MCO deemed a surgical candidate, a multidisciplinary approach should be taken, with evaluation of the risks and benefits of stent placement that is based on local surgical and endoscopic expertise.

      Best Practice Advice 11

      For patients with malignant colonic obstruction who are candidates for resection, insertion of SEMS is a reasonable choice as a bridge to surgery to allow for one-stage, elective resection.

       Malignant Colonic Obstructions in Non-Resectable Patients

      For patients who are not a candidate for resection, the placement of SEMS is useful alternative to provide comfort, avoid a stoma, and potentially allow palliative therapies. In fact, European guidelines published in 2020 unequivocally recommended SEMS as the preferred option for left-sided MCO in non-resectable patients.
      • van Hooft J.E.
      • Veld J.V.
      • Arnold D.
      • et al.
      Self-expandable metal stents for obstructing colonic and extracolonic cancer: European Society of Gastrointestinal Endoscopy (ESGE) guideline—update 2020.
      In one study comparing SEMS with diverting colostomy, SEMS allowed for earlier initiation of oral intake and shorter hospital stay. However, there was a trend favoring colostomy for overall survival and duration to readmission.
      • Tomiki Y.
      • Watanabe T.
      • Ishibiki Y.
      • et al.
      Comparison of stent placement and colostomy as palliative treatment for inoperable malignant colorectal obstruction.
      In a meta-analysis from 2013 involving 13 studies and 837 patients, SEMS had lower clinical success rates and no difference in overall mortality compared with colostomy.
      • Zhao X.-D.
      • Cai B.-B.
      • Cao R.-S.
      • et al.
      Palliative treatment for incurable malignant colorectal obstructions: a meta-analysis.
      However, another meta-analysis from 2015 found no difference in clinical success rates, but SEMS was associated with significantly reduced early AEs, as well as the need for a stoma, and had improved overall survival. Nevertheless, SEMS was associated with a higher risk of perforation and late AEs.
      • Takahashi H.
      • Okabayashi K.
      • Tsuruta M.
      • et al.
      Self-expanding metallic stents versus surgical intervention as palliative therapy for obstructive colorectal cancer: a meta-analysis.
      A separate study showed that for patients who were Eastern Cooperative Oncology Group (ECOG) 0 or 1, palliative surgery had improved overall survival compared with SEMS placement. There was no difference in overall survival in patients who were ECOG 2 or 3.
      • Ahn H.J.
      • Kim S.W.
      • Lee S.W.
      • et al.
      Long-term outcomes of palliation for unresectable colorectal cancer obstruction in patients with good performance status: endoscopic stent versus surgery.
      With regard to right-sided obstructions, an early study of proximal colonic obstructions due to colorectal cancer showed high technical and clinical success rates with SEMS placement with no procedure-related AEs.
      • Repici A.
      • Adler D.G.
      • Gibbs C.M.
      • et al.
      Stenting of the proximal colon in patients with malignant large bowel obstruction: techniques and outcomes.
      Likewise, a more recent study also found similar results with high technical and clinical success rates and minimal AEs with SEMS in right-sided obstructions.
      • Morita S.
      • Yamamoto K.
      • Ogawa A.
      • et al.
      Benefits of using a self-expandable metallic stent as a bridge to surgery for right- and left-sided obstructive colorectal cancers.

      Best Practice Advice 12

      For patients with malignant colonic obstruction who are not candidates for resection, either SEMS placement or a diverting colostomy are reasonable choices depending on the patient’s goals and functional status.

      Best Practice Advice 13

      SEMS is a reasonable option for patients with proximal (or right-sided) malignant obstructions, both as a bridge to surgery and in the palliative setting.

       Malignant Colonic Obstructions in Extracolonic Malignancy

      The pathophysiology of colonic obstructions that are due to ECM are different than those due to colorectal cancer. Colorectal cancers generally cause obstruction caused by space-occupying growth, whereas extracolonic obstructions are due to extrinsic compression, mesenteric infiltration, and dysmotility. The role of colonic stents in ECMs is controversial. One of the initial studies comparing SEMS placement in colorectal cancer compared with ECMs (15 patients) found that ECMs had significantly lower clinical success rates (20%), higher persistent obstructive symptoms, and higher AE rates.
      • Keswani R.N.
      • Azar R.R.
      • Edmundowicz S.A.
      • et al.
      Stenting for malignant colonic obstruction: a comparison of efficacy and complications in colonic versus extracolonic malignancy.
      In contrast, 2 subsequent studies involving 60 and 44 patients with ECMs found no difference in technical, clinical, and AE rates between SEMS placement in ECMs and colorectal malignancies.
      • Moon S.J.
      • Kim S.W.
      • Lee B.-I.
      • et al.
      Palliative stent for malignant colonic obstruction by extracolonic malignancy: a comparison with colorectal cancer.
      ,
      • Kim J.Y.
      • Kim S.G.
      • Im J.P.
      • et al.
      Comparison of treatment outcomes of endoscopic stenting for colonic and extracolonic malignant obstruction.
      A similar study examining SEMS placement as a bridge to surgery in 9 ECM patients found a 100% technical success rate, with 77.8% subsequently undergoing elective surgery. No SEMS-related AEs were seen in that study.
      • Kim E.J.
      • Han S.H.
      • Kim K.O.
      • et al.
      Stenting as a bridge to surgery for extra-colonic malignancy induced colorectal obstruction: preliminary experience.

      Best Practice Advice 14

      SEMS placement is a reasonable alternative for patients with ECM who are not candidates for surgery, although their placement is more technically challenging, clinical success rates are more variable, and complications (including stent migration) are more frequent.

       Stent Migration

      There have been a few studies comparing UCSEMS with covered SEMS. Although initially studies showed that UCSEMS had lower migration rates and higher tumor ingrowth, more recent studies, including a systematic review and meta-analysis, showed that UCSEMS have lower AEs, longer rates of patency, and lower re-intervention rates. No differences were noted in technical or clinical success rates.
      • Mashar M.
      • Mashar R.
      • Hajibandeh S.
      Uncovered versus covered stent in management of large bowel obstruction due to colorectal malignancy: a systematic review and meta-analysis.
      ,
      • Park S.
      • Cheon J.H.
      • Park J.J.
      • et al.
      Comparison of efficacies between stents for malignant colorectal obstruction: a randomized, prospective study.

       Perforation

      There was concern that the use of bevacizumab may lead to higher rates of perforation with SEMS; however, recent large retrospective studies have not shown any association.
      • Lee J.H.
      • Emelogu I.
      • Kukreja K.
      • et al.
      Safety and efficacy of metal stents for malignant colonic obstruction in patients treated with bevacizumab.
      However, the study emphasizes its limitation stemming from the fact that many patients in the study received bevacizumab outside ±6 weeks of the stent placement. A study examining factors associated with perforation with SEMS found that sigmoid location and age older than 70 were associated with early perforation, whereas flexure location and absence of peritoneal carcinomatosis were associated with delayed perforation.
      • Lee Y.J.
      • Yoon J.Y.
      • Park J.J.
      • et al.
      Clinical outcomes and factors related to colonic perforations in patients receiving self-expandable metal stent insertion for malignant colorectal obstruction.

      Conclusion

      There are many options available for the management of MATOs, with the addition of new modalities as interventional endoscopy continues to evolve. The important concept to understand for any physician managing MATOs is that there is no longer a “one-size-fits-all” approach that can be applied to all patients. In addition, it is important for physicians to understand their limits and expertise and recognize when cases are best managed at experienced high-volume centers.

      Acknowledgment

      This expert review was commissioned and approved by the AGA Institute Clinical Practice Updates Committee (CPUC) and the AGA Governing Board to provide timely guidance on a topic of high clinical importance to the AGA membership, and underwent internal peer review by the CPUC and external peer review through standard procedures of Clinical Gastroenterology and Hepatology.

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