Endoscopic management of dumping syndrome after Roux-en-Y gastric bypass: a large international series and proposed management strategy

ORIGINAL ARTICLE: Clinical Endoscopy

Endoscopic management of dumping syndrome after Roux-en-Y gastric bypass: a large international series and proposed management strategy Eric J. Vargas, MD,1 Barham K. Abu Dayyeh, MD, MPH,1 Andrew C. Storm, MD,1 Fateh Bazerbachi, MD,2 Reem Matar, BSc,1 Adrian Vella, MD,3 Todd Kellogg, MD,4 Christine Stier, MD5 Rochester, Minnesota; Boston, Massachusetts, USA; Würzburg, Germany

GRAPHICAL ABSTRACT

Background and Aims: Roux-en-Y gastric bypass (RYGB) is refractory to lifestyle and pharmacotherapy measures, requiring reversal of the patient’s bariatric surgery. Reversal can lead to weight regain and recrudescence of their comorbidities. Our aim was to report a multicenter experience on the endoscopic management of refractory dumping syndrome with endoscopic transoral outlet reduction (TORe). Methods: A multicenter international series of consecutive patients who underwent TORe with a full-thickness endoscopic suturing device was analyzed for technical success, improvement in Sigstad scores, and weight trajectories after the procedure. Failure was defined as needing an enteral feeding tube, surgical reversal, or repeat TORe. Results: One hundred fifteen patients across 2 large academic centers in Germany and the United States underwent TORe for dumping syndrome. Patient age was mean 8.9  1.1 years from their initial RYGB with an average percent total body weight loss of 31%  10.6% at the time of endoscopy. Three months postprocedure, the Sigstad score improved from a mean of 17  6.1 to 2.6  1.9 (paired t test P Z .0001) with only 2% of patients (n Z 2) experiencing weight gain. Mean weight loss and percentage of total body weight loss 3 months post-TORe were 9.47  3.6 kg and 9.47%  2.5%, respectively. Six patients (5%) failed initial endoscopic therapy, with 50% (n Z 3) successfully treated with a repeat TORe. Three patients underwent surgical reversal, indicating an overall 97% endoscopic success rate. Conclusions: TORe as an adjunct to lifestyle and pharmacologic therapy for refractory dumping syndrome is safe and effective at improving dumping syndrome and reducing rates of surgical revision. (Gastrointest Endosc 2020;92:91-6.)

(footnotes appear on last page of article)

Roux-en-Y gastric bypass (RYGB) surgery has been proven to be a highly successful treatment for obesity and its related comorbidities.1-3 With the rising rate of obesity and increasing access to bariatric surgery, the www.giejournal.org

number of bariatric surgeries performed across the globe will continue to grow.4,5 Consequently, increasingly more patients will present with long-term adverse events of bariatric surgery, including but not limited to dumping Volume 92, No. 1 : 2020 GASTROINTESTINAL ENDOSCOPY 91

Use of TORe for dumping syndrome after RYGB

syndrome, vitamin deficiencies, marginal ulcers, and weight regain.6 Dumping syndrome is a postprandial phenomenon in which patients experience a constellation of GI and vasomotor symptoms including tachycardia, fatigue, syncope, and at times shock and seizures because of profound hypoglycemia.7 Dumping symptoms can occur early (within an hour) after a meal or up to 3 hours afterward, with the latter associated with postprandial hypoglycemia. Classic dumping symptom (early) is believed to occur by rapid pouch emptying of hyperosmolar contents into the small bowel, leading to rapid fluid shifts, whereas late symptoms are believed to occur by exaggerated incretin responses by early nutrient delivery to the distal small bowel.8 Similar to weight regain after RYGB, a dilated gastrojejunal anastomosis (GJA; >30 mm) has also been associated with dumping syndrome.9,10 However, the cause likely remains multifactorial. Analogous to the pathophysiology, the incidence and prevalence of dumping syndrome remain largely undefined. Dumping symptoms have been reported to occur in 5% to 75% of patients after RYGB because of the differences in terminology and method of case ascertainment.11,12 Because dumping symptoms can be expected in the first 12 to 24 months after bariatric surgery, previous investigators have looked at whether dumping symptoms are associated with weight loss after surgery, with conflicting findings.13,14 Nevertheless, the condition is associated with poor quality of life and outcomes after bariatric surgery.15 When symptoms persist, the traditional treatment involves lifestyle and behavior modification, medications, and, in refractory cases, surgical reversal or enteral nutrition. Previously, surgical revision of the dilated GJA was offered, but the practice fell out of favor because of high adverse event rates.16,17 Early on, endoscopic revision of the dilated GJA using superficial thickness plication devices for dumping symptoms showed promise, but with the advent of full-thickness suturing devices for the treatment of weight regain,18 GJA outlet revision for patients with weight regain and dumping syndrome has been increasingly reported in small series.19-21 Surgical reversal or enteral feeding improves dumping symptoms but can be associated with weight regain. Thus, endoscopic revision of the dilated GJA for dumping, similar to weight regain, may be an attractive interventional option that avoids the inherent risks of revision surgery. The aims of our study were to report the effectiveness of endoscopic revision of the GJA using a full-thickness suturing device in a large cohort of patients experiencing dumping symptoms after RYGB.

METHODS Study design and population A prospective single-arm study across 2 tertiary care centers from Germany and United States was conducted 92 GASTROINTESTINAL ENDOSCOPY Volume 92, No. 1 : 2020

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in patients presenting between 2014 and 2018 with dumping symptoms. Institutional Review Board approval for conducting human subject research was obtained (Institutional Review Board no. 18-010157) at the U.S. site, with all research participants in Germany providing informed consent abiding and practicing by the principles of the Declaration of Helsinki. Inclusion criteria included adults with prior RYGB for obesity with dumping symptoms. The severity of dumping syndrome was assessed using the Sigstad score.22 The Sigstad score is obtained after patients consume a glucose-containing meal, and symptoms are captured. Each symptom is weighted, and a total score 7 is highly suggestive of dumping syndrome. A score <7 suggests an alternative etiology (Table 1). Patient weight at the time of index RYGB and endoscopic intervention as well as their baseline Sigstad score were collected. The number of patients on pharmaceutical therapy for dumping was also assessed.

Intervention Patients underwent endoscopic transoral outlet reduction (TORe) using the Overstitch device (Apollo Endosurgery, Austin, Tex, USA) mounted on a standard doublechannel therapeutic endoscope (GIF 2HT180; Olympus, Spring Valley, Pa, USA). Procedures were performed by 2 endoscopists, 1 at each site. All patients underwent a simple interrupted suturing technique (Fig. 1) using a combination of figure of 8 or a simple interrupted technique depending on anatomy to reduce the outlet diameter to <10 mm. Argon plasma coagulation at a flow of .8 L/s and 55 W was used to resurface the gastric side

TABLE 1. Sigstad score Symptom

Points

Shock

5

Fainting/syncope

4

Desire to lie or sit down

4

Dyspnea

3

Weakness

3

Sleepiness

3

Palpitations

3

Restlessness

2

Dizziness

2

Headaches

1

Diaphoresis

1

Nausea

1

Abdominal fullness

1

Borborygmus

1

Eructation

–1

Vomiting

–4

Score > 7 Z dumping syndrome; score 5-7 Z indeterminate; score < 4 Z not dumping syndrome.

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Use of TORe for dumping syndrome after RYGB

Figure 1. Transoral outlet reduction using a simple interrupted suture technique. A, Suturing device performing single interrupted sutures. B, Final revised gastrojejunal anastomosis. TABLE 3. Postintervention results

TABLE 2. Baseline characteristics Variable

Value

Variable

At 3 months

Mean difference

P value

Age, y

44.9  9.2

Sigstad score

2.55  1.87

–14.5  5.5

<.0001

Weight, kg

98.4  22.7

Weight, kg

89.4  1.96

–9.3  3.8

<.0001

Female, %

84

Baseline weight at time of Roux-en-Y gastric bypass, kg

143.5  26.8

Weight at intervention, kg

98.2  22.6

Baseline Sigstad score

17.02  6.1

Values are mean  standard deviation unless otherwise defined.

of the dilated GJA before endoscopic suturing. Suturing was performed from the jejunal to the gastric side in a “vest over pants” technique using nonabsorbable 2-0 polypropylene sutures. After the procedure, patients were instructed to follow a standardized postprocedure diet for 2 weeks. Standard antiemetics and pain medications were prescribed for 1 week after the TORe procedure. After 3 months, Sigstad score, weight, percent total body weight loss, weight gain, and rates of medication discontinuation were recorded.

Study outcomes The outcomes of interest were technical success, improvement in dumping symptoms as measured through the Sigstad score, weight trajectories, and rates of medication discontinuation. Failure was defined as needing repeat TORe, enteral feeding tube placement, or surgical RYGB reversal. www.giejournal.org

Values are mean  standard deviation.

Statistical analysis Continuous variables were described by their means and standard deviations. Categorical variables were described by their frequencies. Baseline Sigstad score and weight were compared with 3-month outcomes using the paired t test with a .05 2-sided significance level. All statistical analyses were conducted using JMP Pro version 12.0 (SAS Institute, Cary, NC, USA).

RESULTS One hundred fifteen patients underwent TORe for the treatment of dumping syndrome after RYGB (Germany, 97; United States, 18). Mean patient age was 44.7  9 years, and 84% were women. Pre-RYGB weight and body mass index were 143.6  26.9 kg and 51.6  7.3 kg/m2, respectively. Patients were on average 8.9  1.1 years from their initial bariatric surgery, with an average total body weight loss of 31%  10.6% at the time of endoscopic treatment for dumping syndrome. At the time of intervention, their mean weight and body mass index were 98.4  22.7 kg and 35.3  22.6 kg/m2, respectively. Baseline Sigstad score was 17.23  5.9 (Table 2). Eighty-seven percent Volume 92, No. 1 : 2020 GASTROINTESTINAL ENDOSCOPY 93

Use of TORe for dumping syndrome after RYGB

Patient presents with dumping symptoms

Vargas et al

Mild •

Re-enforce diet modification • Add Guar Gum or Pectin

Treatment dosages

Pectin 5-15g TID with meals

Confirm Dumping Syndrome

Moderate 1) Initiate pharmacotherapy 2) Consider TORe

Assess Anatomy

Guar gum 5g TID with meals Acarbose 50-100mg TID before meals

Dumping Syndrome Excluded Seek alternative etiologies

Moderately Severe 1) TORe 2) Pharmacotherapy

Somatostatin 25-50␮g TID before meals

Refractory: 1) Remnant stomach access with LAMS / PEG or reversal

Figure 2. Proposed management strategy. TORe, Transoral outlet reduction; LAMS, lumen-apposing metal stent; TID, three times a day.

of patients (n Z 100) were on acarbose for dumping syndrome. All cases (100%) were technically successful. Average procedural time was 38.9  17.3 minutes. The mean number of sutures was 3 (range, 2-5). The mean GJA diameter before the procedure was 39.8  6.7 mm, reduced to approximately 8 to 10 mm after suturing because it allowed passage of the gastroscope. At 3 months, 97% of cases (n Z 109) were clinically successful, with 100% of patients reporting discontinuation of their medication for dumping syndrome. Of the 6 failures, 3 (50%) were rescued with repeat TORe because of a dilated GJA found on repeat endoscopy after reporting initial response and gradual recrudescence of symptoms and 3 underwent surgical treatment with a surgically placed G-tube for enteral feeding to the excluded stomach for refractory symptoms despite intact revised outlet on endoscopy. Mean Sigstad scores improved at 3 months, with a mean decrease of 14.5 points (mean difference, –14.5  5.5; P < .0001). Only 2 patients experienced weight regain after the procedure, with an average .25  .35 kg weight regain. Most patients lost weight at 3 months, with an average total body weight loss of 9.3%  2.84% and a mean weight decrease of 9.3  3.8 kg at 3 months (P < .0001) (Table 3). There were no serious adverse events such as bleeding, need for dilation, perforation, or deaths postprocedure in the follow-up period.

DISCUSSION In this large prospective study, we illustrate that TORe using a full-thickness suturing device is an effective and safe treatment option for dumping syndrome after RYGB in the short term. Over 95% of cases were successfully treatment with TORe, and only 3 cases required enteral feeding tube placement for refractory dumping symptoms. Second, most patients lost weight after this procedure, with only 2 patients gaining a mild amount of weight, a 94 GASTROINTESTINAL ENDOSCOPY Volume 92, No. 1 : 2020

common unintended consequence that can be seen with surgical reversal or enteral feeding tube placement. Third, 100% of patients on acarbose for dumping syndrome discontinued the medication, with over 97% of cases showing improvement in their Sigstad scores to less than 7 after the procedure, and 0% of patients experiencing a worsening of their symptoms. Although dumping syndrome is an expected adverse effect of RYGB, it is usually self-limited and resolves a few months after surgery. When symptoms persist, the initial treatment includes reinforcing lifestyle and dietary modifications aimed at minimizing both liquids around a meal and simple carbohydrates (sugary foods). Next, thickening agents such as guar gum and pectin can help by delaying pouch emptying into the small bowel. However, patients usually do not tolerate thickening agents, and pharmacotherapy agents such as acarbose, diaxozide, and somatostatin analogues are often used in this situation.7 Acarbose, an alpha-glucosidase hydrolase inhibitor, helps control postbariatric hypoglycemia by slowing carbohydrate digestion and modulating postprandial hypoglycemia. Octreotide delays gastric motility and reduces GI hormone secretion, reducing dumping symptoms. To date, the best evidence-based pharmacologic treatment options include acarbose and somatostatin analogues, with evidence suggesting superiority of octreotide over acarbose.23 However, no head-to-head studies have been performed, and obtaining octreotide can be cost prohibitive, leading to increased used of acarbose. TORe delays pouch emptying similarly to octreotide but by anatomic manipulation of the anastomosis. In refractory cases, enteral feeding and surgical revision may be considered, with surgical revision associated with a significantly higher risk for morbidity and mortality. Of note, total or subtotal pancreatectomy is no longer recommended given poor outcomes associated with these procedures and reversal of dumping syndrome after restoring continuity or enteral feeding.24-26 Before advances in endoscopic technology, limited options existed between medications and surgical treatments. www.giejournal.org

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Our study contributes to the growing literature of endoscopic outlet revision for dumping syndrome, providing patients with another treatment option after a trial of medications and before consideration of surgery. The concept of endoscopic tightening of the dilated GJA for dumping syndrome first appeared in 2010, when FernandezEsparrach et al19 successfully reported the use of the EndoCinch suturing system (CR Bard, Murray Hill, NJ, USA), a superficial thickness plication device, to treat dumping symptoms in a series of 6 patients. All patients had successful improvement in symptoms. Over the years, however, full-thickness suturing devices and the use of argon plasma coagulation have replaced superficial thickness plication devices, with a recent series of 40 patients reporting 90% success after 1 endoscopic suturing procedure, comparable with our results.21 The strengths of our study include its prospective design, large sample size of over 100 patients, and multicenter approach. The limitations of this study include the lack of a comparator group with a sham procedure (placebo effect), referral bias at a tertiary care center, and limited follow-up beyond 3 months. However, extrapolating from the long-term success of TORe for management of weight regain after RYGB, the procedure is likely equally durable for dumping syndrome.10,27-30 In the future, double-blinded prospective studies randomizing patients to TORe versus an active control group with a sham procedure are needed to validate these findings, eliminating the potential for a placebo effect influencing the results. The management of dumping syndrome nevertheless remains challenging despite the advances in medications, endoscopy, and minimally invasive surgery. Based on our experience herein, we propose a multidisciplinary management strategy based on the severity of the dumping syndrome (Fig. 2). In mild cases resistant to dietary changes, the use of thickening agents and medications should be recommended. In more moderate to severe cases, TORe can be used as an alternative to surgical revision of a dilated outlet or reversal of surgery. In refractory cases or those associated with life-threatening neuroglycopenic seizures, surgical G-tube placement may be a necessary step while discussing the use of TORe for dumping syndrome. In the future, EUS-guided access to the remnant stomach using lumen-apposing metal stents may be attractive option (endoscopic ultrasound directed transgastric ERCP procedure without ERCP portion), minimizing the need for gastrostomy tube placement, but we eagerly await prospective data using lumen-apposing metal stents for this indication. In the interim, TORe is a viable endoscopic treatment option for dumping syndrome, helping to avoid surgical revision. Combination therapy with medications such as octreotide or acarbose may increase its therapeutic yield and remains to be investigated with TORe in longterm studies.

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Use of TORe for dumping syndrome after RYGB

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Use of TORe for dumping syndrome after RYGB 21. Tsai C, Steffen R, Kessler U, et al. Short-term outcomes of endoscopic gastro-jejunal revisions for treatment of dumping syndrome after Roux-En-Y gastric bypass. Surg Endosc 2019. 22. Sigstad H. A clinical diagnostic index in the diagnosis of the dumping syndrome. Changes in plasma volume and blood sugar after a test meal. Acta Med Scand 1970;188:479-86. 23. Arts J, Caenepeel P, Bisschops R, et al. Efficacy of the long-acting repeatable formulation of the somatostatin analogue octreotide in postoperative dumping. Clin Gastroenterol Hepatol 2009;7: 432-7. 24. Davis DB, Khoraki J, Ziemelis M, et al. Roux en Y gastric bypass hypoglycemia resolves with gastric feeding or reversal: confirming a nonpancreatic etiology. Mol Metab 2018;9:15-27. 25. Vanderveen KA, Grant CS, Thompson GB, et al. Outcomes and quality of life after partial pancreatectomy for noninsulinoma pancreatogenous hypoglycemia from diffuse islet cell disease. Surgery 2010;148: 1237-45; discussion 45-6. 26. Jirapinyo P, Thompson AC, Kroner PT, et al. Metabolic effect of foregut exclusion demonstrated by the impact of gastrogastric fistula on recurrence of diabetes. J Am Coll Surg 2018;226: 259-66. 27. Jirapinyo P, Kroner PT, Thompson CC. Purse-string transoral outlet reduction (TORe) is effective at inducing weight loss and improvement in metabolic comorbidities after Roux-en-Y gastric bypass. Endoscopy 2017;50:371-7. 28. Kumar N, Thompson CC. Transoral outlet reduction for weight regain after gastric bypass: long-term follow-up. Gastrointest Endosc 2016;83:776-9. 29. Brunaldi VO, Jirapinyo P, de Moura DTH, et al. Endoscopic treatment of weight regain following Roux-en-Y gastric bypass: a systematic review and meta-analysis. Obes Surg 2018;28:266-76. 30. Vargas EJ, Bazerbachi F, Rizk M, et al. Transoral outlet reduction with full thickness endoscopic suturing for weight regain after gastric bypass: a large multicenter international experience and meta-analysis. Surg Endosc 2018;32:252-9.

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Abbreviations: GJA, gastrojejunal anastomosis; RYGB, Roux-en-Y gastric bypass; TORe, transoral outlet reduction. DISCLOSURE: The following authors disclosed financial relationships: B. K. Abu Dayyeh: Consultant for USGI Medical, Metamodix, BFKW, DyaMx, and Boston Scientific; research support from Apollo Endosurgery, USGI, Spatz Medical, Boston Scientific, GI Dynamics, Cairn Diagnostics, Aspire Bariatrics, and Medtronic; speaker for Johnson and Johnson, Endogastric Solutions, and Olympus. A.C. Storm: Consultant for GI Dynamics, ERBE, Endo-TAGSS, and Apollo Endosurgery; and received research support from Apollo Endosurgery and Boston Scientific. A. Vella: Consultant for vTv Therapeutics and Zeeland Pharmaceuticals; research support from U.S. National Institutes of Health and Novo Nordisk. C. Stier: Consultant for Apollo Endosurgery, Novo Nordisk, Johnson and Johnson, and Sanofi. All other authors disclosed no financial relationships. Copyright ª 2020 by the American Society for Gastrointestinal Endoscopy 0016-5107/$36.00 https://doi.org/10.1016/j.gie.2020.02.029 Received November 13, 2019. Accepted February 17, 2020. Current affiliations: Division of Gastroenterology and Hepatology (1), Division of Endocrinology, Diabetes, Metabolism and Nutrition (3), Department of General Surgery (4), Mayo Clinic, Rochester, Minnesota, USA; Division of Gastroenterology, Interventional Endoscopy Program, Harvard Medical School and Massachusetts General Hospital, Boston, Massachusetts, USA (2), Department of Endocrinology, University Hospital, Würzburg, Germany (5). Reprint requests: Barham K. Abu Dayyeh, MD, MPH, Division of Gastroenterology and Hepatology, Mayo Clinic Rochester, 200 First St SW, Rochester, MN 55905. If you would like to chat with an author of this article, you may contact Dr Abu Dayyeh at [email protected].

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