Barrett’s esophagus after sleeve gastrectomy: a systematic review and meta-analysis

Published:August 13, 2020DOI:https://doi.org/10.1016/j.gie.2020.08.008

      Background and Aims

      Sleeve gastrectomy (SG) has become significantly more common in recent years. Gastroesophageal reflux disease (GERD) is a major concern in patients undergoing SG and is the major risk factor for Barrett’s esophagus (BE). We aimed to assess the prevalence of BE in patients who had undergone SG.

      Methods

      We searched the major search engines ending in July 2020. We included studies on patients who had undergone esophagogastroduodenoscopy (EGD) after SG. The primary outcome was the prevalence of BE in patients who had undergone SG. We assessed heterogeneity using I2 and Q statistics. We used funnel plots and the classic fail-safe test to assess for publication bias. We used random-effects modeling to report effect estimates.

      Results

      Our final analysis included 10 studies that included 680 patients who had undergone EGD 6 months to 10 years after SG. The pooled prevalence of BE was 11.6% (95% confidence interval [CI], 8.1%-16.4%; P < .001; I2 = 28.7%). On logistic meta-regression analysis, there was no significant association between BE and the prevalence of postoperative GERD (β = 3.5; 95% CI, −18 to 25; P = .75). There was a linear relationship between the time of postoperative EGD and the rate of esophagitis (β = 0.13; 95% CI, 0.06-0.20; P = .0005); the risk of esophagitis increased by 13% each year after SG.

      Conclusions

      The prevalence of BE in patients who had EGD after SG appears to be high. There was no correlation with GERD symptoms. Most cases were observed after 3 years of follow-up. Screening for BE should be considered in patients after SG even in the absence of GERD symptoms postoperatively.

      Graphical abstract

      Abbreviations:

      BE (Barrett’s esophagus), CI (confidence interval), EAC (esophageal adenocarcinoma), EE (erosive esophagitis), EGD (esophagogastroduodenoscopy), ESG (endoscopic sleeve gastroplasty), SG (sleeve gastrectomy)

      Introduction

      As the epidemic of obesity continues to increase in our nation and worldwide, bariatric surgery has emerged as an effective, yet invasive, approach to help patients with severe obesity.
      • Schauer P.R.
      • Kashyap S.R.
      • Wolski K.
      • et al.
      Bariatric surgery versus intensive medical therapy in obese patients with diabetes.
      Among the various techniques, the number of patients undergoing sleeve gastrectomy (SG) has increased significantly.
      • Khan S.
      • Rock K.
      • Baskara A.
      • et al.
      Trends in bariatric surgery from 2008 to 2012.
      ,
      • Campos G.M.
      • Khoraki J.
      • Browning M.G.
      • et al.
      Changes in utilization of bariatric surgery in the United States from 1993 to 2016.
      Yet, gastroesophageal reflux disease (GERD) has become a major concern in patients undergoing SG.
      • Oor J.E.
      • Roks D.J.
      • Unlu C.
      • et al.
      Laparoscopic sleeve gastrectomy and gastroesophageal reflux disease: a systematic review and meta-analysis.
      Many studies have reported a significant increase in GERD symptoms after SG.
      • Coupaye M.
      • Gorbatchef C.
      • Calabrese D.
      • et al.
      gastroesophageal reflux after sleeve gastrectomy: a prospective mechanistic study.
      ,
      • Genco A.
      • Soricelli E.
      • Casella G.
      • et al.
      Gastroesophageal reflux disease and Barrett's esophagus after laparoscopic sleeve gastrectomy: a possible, underestimated long-term complication.
      Several mechanisms have been reported for this phenomenon, including loss of angle of His flap valve, decreased pressure at the lower esophageal sphincter, and damage of sling fibers.
      • Wright F.G.
      • Duro A.
      • Medici J.R.
      • et al.
      Esophageal adenocarcinoma five years after laparoscopic sleeve gastrectomy. A case report.
      GERD is the major risk factor for the development of Barrett’s esophagus (BE),
      • Qumseya B.J.
      • Bukannan A.
      • Gendy S.
      • et al.
      Systematic review and meta-analysis of prevalence and risk factors for Barrett's esophagus.
      which is recognized as a precursor for esophageal adenocarcinoma (EAC).
      • Shaheen N.J.
      • Richter J.E.
      Barrett's oesophagus.
      Unfortunately, we have seen trends indicating that the incidence of EAC and BE has increased in recent years in some western populations.
      • Thrift A.P.
      • Whiteman D.C.
      The incidence of esophageal adenocarcinoma continues to rise: analysis of period and birth cohort effects on recent trends.
      ,
      • Hayeck T.J.
      • Kong C.Y.
      • Spechler S.J.
      • et al.
      The prevalence of Barrett's esophagus in the US: estimates from a simulation model confirmed by SEER data.
      The prevalence of GERD and hiatal hernias is higher than normal in obese patients, which would be expected to increase the prevalence of BE in this population.
      • Qumseya B.J.
      • Bukannan A.
      • Gendy S.
      • et al.
      Systematic review and meta-analysis of prevalence and risk factors for Barrett's esophagus.
      ,
      • Chandar A.K.
      • Iyer P.G.
      Role of obesity in the pathogenesis and progression of Barrett's esophagus.
      Despite this, a meta-analysis of more than 13,000 patients who underwent esophagogastroduodenoscopy (EGD) before bariatric surgery reported a low rate of BE at less than 1%.
      • Qumseya B.
      • Gendy S.
      • Wallace A.
      • et al.
      Prevalence of Barrett’s esophagus in obese patients undergoing pre-bariatric surgery evaluation: a systematic review and meta-analysis.
      Yet, if patients have worsening GERD after SG, we hypothesize that they would have an increased risk for developing BE. Based on clinical practice guidelines,
      • Qumseya B.
      • Sultan S.
      • Bain P.
      • et al.
      ASGE Standards of Practice Committee
      ASGE guideline on screening and surveillance of Barrett's esophagus.
      patients whose expected prevalence of BE is above 10% are thought to be at high risk for BE, and screening for BE is recommended. Assessing the risk of post-SG BE has important clinical implications for all gastroenterologists who may perform pre- and postoperative endoscopy, bariatric surgeons who perform the procedure, patients who undergo the procedure, and primary physicians who may need to recommend screening for BE in such patients.
      • Sebastianelli L.
      • Benois M.
      • Vanbiervliet G.
      • et al.
      Systematic endoscopy 5 years after sleeve gastrectomy results in a high rate of Barrett's esophagus: results of a multicenter study.
      • El Khoury L.
      • Benvenga R.
      • Romero R.
      • et al.
      Esophageal adenocarcinoma in Barrett's esophagus after sleeve gastrectomy: case report and literature review.
      • Felsenreich D.M.
      • Kefurt R.
      • Schermann M.
      • et al.
      Reflux, sleeve dilation, and Barrett's esophagus after laparoscopic sleeve gastrectomy: long-term follow-up.
      Therefore, we conducted a systematic review and meta-analysis of studies that assessed the risk of BE in patients who underwent SG for obesity.

      Methods

      Study selection

      We used our a priori protocol to conduct a literature search with the help of an expert librarian. We included studies if they met the following criteria: (1) randomized trials, prospective, retrospective cohort studies, or meeting abstracts from the last 3 years; (2) patients who underwent SG for treatment of obesity; (3) all patients who underwent EGD before SG; (4) the study authors invited all patients for EGD, or all consecutive patients underwent EGD at least 6 months after surgery; and (5) BE, if found, was confirmed by biopsy. We excluded studies that (1) performed EGD only on symptomatic patients postoperatively rather than all patients; (2) were case reports or case series; (3) were deemed to be of poor quality based on the Downs and Black scoring system; or (4) were not available in English. We used the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines for our study.

      Search strategy and data extraction

      Our literature search was conducted with the help of an expert librarian at Florida State University (Robyn Rosasco). We searched MEDLINE (Ovid), Cochrane Library and CENTRAL, Embase, and Web of Science from inception to July 2020. Details of our literature search are described in Appendix 1 (available online at www.giejournal.org). The librarian imported all citations into Covidence.org, where all duplicates were removed. Two independent reviewers (Y.Q. and S.P.) conducted the initial review based on our inclusion and exclusion criteria. A third reviewer (B.Q.) with expertise in BE and systematic reviews resolved all conflicts. We extracted data on study authors, publication year, country, study design, mean age, mean body mass index, preoperative EGD, time to follow-up EGD, number of patients, number with BE, BE in GERD versus no GERD, number with de novo GERD, GERD definition, and number with esophagitis before and after surgery.

      Outcomes of interest

      The primary outcome of interest was the proportion of patients who developed BE after SG. Histologic confirmation was a requirement for diagnosis of BE. This meant that biopsy of the area of suspected BE was performed, and histology was consistent with BE based on that institution’s definition of BE. We also stratified cases of BE based on GERD symptoms, follow-up time, and presence of esophagitis on follow-up EGD. Secondary outcomes included the prevalence of esophagitis and GERD on follow-up.
      Sources of heterogeneity were hypothesized a priori as follows:
      • 1.
        Variation of GERD definition
      • 2.
        Variation in follow-up time
      • 3.
        Variation in the prevalence of GERD in the baseline population
      • 4.
        Variation in surgical techniques and experience
      The following analyses were planned a priori to control for possible heterogeneity: follow-up time (long-term [3 or more years] vs short-term follow-up [<3 years]), and meta-regressions controlling for proportion of GERD, esophagitis, and follow-up time.

      Quality assessment

      We used the Downs and Black scoring system to assess the quality of each study; however, many questions in the scoring system do not apply to the studies we reviewed.
      • Downs S.H.
      • Black N.
      The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions.
      The final score for studies (with a maximum score of 16) was reported, as previously described.
      • Qumseya B.
      • Gendy S.
      • Wallace A.
      • et al.
      Prevalence of Barrett’s esophagus in obese patients undergoing pre-bariatric surgery evaluation: a systematic review and meta-analysis.
      Based on this system, we rated studies as high (12–16); moderate (9–11); fair (7–8), and poor (≤6). We also planned to identify and remove possible outliers. We defined these a priori as studies that reported an effect estimate that was ≥10 times higher or lower than expected.

      Statistical analysis

      We decided to use random-effects modeling in all analyses a priori. The primary metameter (effect estimate) of interest was the prevalence of de novo BE after SG and was reported as rated with 95% confidence intervals (CIs). We reported the magnitude and direction of effect estimates on forest plots. Secondary outcomes included the risk difference in erosive esophagitis (EE) and GERD before surgery compared with after surgery. We defined the risk difference as the proportion of patients with EE after surgery minus the proportion of patients with EE before surgery. Because these patients underwent pre- and postprocedure EGDs, we used matched proportions. In doing so, we had to assume a correlation coefficient. This was assumed to be 0.5 (halfway between no correlation and complete correlation). We assessed heterogeneity using I2 and Cochrane’s Q statistic. Heterogeneity was defined as low, I2 ≤ 50%; moderate, I2 = 51%–75%; or high, I2 >75%. We used both funnel plots and the classic fail-safe test to screen for publication bias. Exploratory logistic meta-regression analyses were used to assess for a possible relationship between prevalence of BE and potential risk factors: duration of follow-up, GERD, and EE. In such cases, we used R2 analog to report the in-between study variance explained by our model. We used CMA V3 (Biostat, Inc, Englewood, NJ, USA) for all statistical analyses.

      Results

      Our initial search identified 4389 studies, of which 4359 were excluded based on the title and abstract. After reviewing 30 full-text articles, 10 studies,
      • Sebastianelli L.
      • Benois M.
      • Vanbiervliet G.
      • et al.
      Systematic endoscopy 5 years after sleeve gastrectomy results in a high rate of Barrett's esophagus: results of a multicenter study.
      ,
      • Felsenreich D.M.
      • Kefurt R.
      • Schermann M.
      • et al.
      Reflux, sleeve dilation, and Barrett's esophagus after laparoscopic sleeve gastrectomy: long-term follow-up.
      • Soricelli E.
      • Casella G.
      • Baglio G.
      • et al.
      Lack of correlation between gastroesophageal reflux disease symptoms and esophageal lesions after sleeve gastrectomy.
      • Sharma A.
      • Aggarwal S.
      • Ahuja V.
      • et al.
      Evaluation of gastroesophageal reflux before and after sleeve gastrectomy using symptom scoring, scintigraphy, and endoscopy.
      • Viscido G.
      • Gorodner V.
      • Signorini F.
      • et al.
      Laparoscopic sleeve gastrectomy: endoscopic findings and gastroesophageal reflux symptoms at 18-month follow-up.
      • Elkassem S.
      Endoscopic surveillance three to five years post sleeve gastrectomy: possible progression to reflux esophagitis and Barretts.
      • Csendes A.
      • Orellana O.
      • Martinez G.
      • et al.
      Clinical, endoscopic, and histologic findings at the distal esophagus and stomach before and late (10.5 years) after laparoscopic sleeve gastrectomy: results of a prospective study with 93% follow-up.
      • Dimbezel V.
      • Nedelcu A.
      • Danan M.
      • et al.
      Endoscopic findings 5 years following sleeve gastrectomy.
      • Lallemand L.
      • Greilsamer T.
      • Krempf M.
      • et al.
      Five years sleeve gastrectomy impact on gastroesophageal reflux and esophageal mucosa aspect. a monocentric study.
      • Tai C.M.
      • Huang C.K.
      Increase in gastroesophageal reflux disease symptoms and erosive esophagitis 1 year after laparoscopic sleeve gastrectomy among obese adults.
      including 2 abstracts, were included in the final analysis totaling 680 patients (Fig. 1). All patients underwent EGD preoperatively and 1 had BE before surgery. All studies assessed patients who underwent SG and had undergone EGD after a minimum of 6 months. Seven studies
      • Sebastianelli L.
      • Benois M.
      • Vanbiervliet G.
      • et al.
      Systematic endoscopy 5 years after sleeve gastrectomy results in a high rate of Barrett's esophagus: results of a multicenter study.
      ,
      • Felsenreich D.M.
      • Kefurt R.
      • Schermann M.
      • et al.
      Reflux, sleeve dilation, and Barrett's esophagus after laparoscopic sleeve gastrectomy: long-term follow-up.
      ,
      • Soricelli E.
      • Casella G.
      • Baglio G.
      • et al.
      Lack of correlation between gastroesophageal reflux disease symptoms and esophageal lesions after sleeve gastrectomy.
      ,
      • Elkassem S.
      Endoscopic surveillance three to five years post sleeve gastrectomy: possible progression to reflux esophagitis and Barretts.
      • Csendes A.
      • Orellana O.
      • Martinez G.
      • et al.
      Clinical, endoscopic, and histologic findings at the distal esophagus and stomach before and late (10.5 years) after laparoscopic sleeve gastrectomy: results of a prospective study with 93% follow-up.
      • Dimbezel V.
      • Nedelcu A.
      • Danan M.
      • et al.
      Endoscopic findings 5 years following sleeve gastrectomy.
      • Lallemand L.
      • Greilsamer T.
      • Krempf M.
      • et al.
      Five years sleeve gastrectomy impact on gastroesophageal reflux and esophageal mucosa aspect. a monocentric study.
      assessed patients after a minimum of 3 years. These were referred to as “long-term” follow-up. Three studies
      • Sharma A.
      • Aggarwal S.
      • Ahuja V.
      • et al.
      Evaluation of gastroesophageal reflux before and after sleeve gastrectomy using symptom scoring, scintigraphy, and endoscopy.
      ,
      • Viscido G.
      • Gorodner V.
      • Signorini F.
      • et al.
      Laparoscopic sleeve gastrectomy: endoscopic findings and gastroesophageal reflux symptoms at 18-month follow-up.
      ,
      • Tai C.M.
      • Huang C.K.
      • Lee Y.C.
      • et al.
      Increase in gastroesophageal reflux disease symptoms and erosive esophagitis 1 year after laparoscopic sleeve gastrectomy among obese adults.
      assessed patients with EGD within a minimum of 6 months from surgery. These were termed “short-term” follow-up studies. Mean age, body mass index, and ratio of females to males were comparable among the studies. Study locations included Europe, Canada, Argentina, Chile, India, and Taiwan. Further patient and study characteristics are summarized in Table 1.
      Figure thumbnail gr1
      Figure 1Flowchart of study selection. BE, Barrett’s esophagus; EGD, esophagogastroduodenoscopy.
      Table 1Patient and study characteristics of the 10 studies included in the analysis
      StudyType of studyPublicationCountryMean age (SD or range)Mean BMI% male% Excess WL% TBWLBougie size (FR)Time to EGD or follow-up timeNo. of patientsNo. with BEBE with GERDBE without GERDType of BEPreop EEPostop EEDefinition of GERDPreop GERDPostop GERDDe novo GERDD&B
      Sebastianelli et al, 2019
      • Sebastianelli L.
      • Benois M.
      • Vanbiervliet G.
      • et al.
      Systematic endoscopy 5 years after sleeve gastrectomy results in a high rate of Barrett's esophagus: results of a multicenter study.
      ProspectiveManuscriptMultinational41 ± 1146 ± 80.2758 ± 2725NA78 ± 15 months901716 of 681 of 22NDBE937Montreal Consensus2068NC14
      Felsenreich et al, 2017
      • Felsenreich D.M.
      • Kefurt R.
      • Schermann M.
      • et al.
      Reflux, sleeve dilation, and Barrett's esophagus after laparoscopic sleeve gastrectomy: long-term follow-up.
      ProspectiveManuscriptAustria38.4 ± 12.449.5 ± 9.60.21NANA42-4810 years2031 of 102 of 10NDBENA6Reflux Symptoms Index01010 of 2613
      Soricelli et al, 2018
      • Soricelli E.
      • Casella G.
      • Baglio G.
      • et al.
      Lack of correlation between gastroesophageal reflux disease symptoms and esophageal lesions after sleeve gastrectomy.
      ProspectiveManuscriptItalyNANANANANA4866 (41-89) months1441915 of 1014 of 43NDBENA86Visual Analog Scale59101NC9
      Elkassem, 2018
      • Elkassem S.
      Endoscopic surveillance three to five years post sleeve gastrectomy: possible progression to reflux esophagitis and Barretts.
      ProspectiveAbstractCanada47.849.1NANA26NAAt least 3 year213NANANA1016NCNC
      Tai and Huang, 2013
      • Tai C.M.
      • Huang C.K.
      • Lee Y.C.
      • et al.
      Increase in gastroesophageal reflux disease symptoms and erosive esophagitis 1 year after laparoscopic sleeve gastrectomy among obese adults.
      ProspectiveManuscriptTaiwan37.2 ± 12.736.3 ± 4.10.29NANA3612 (12-21) months6601144Reflux Disease Questionnaire84726 of 5812
      Sharma et al, 2014
      • Sharma A.
      • Aggarwal S.
      • Ahuja V.
      • et al.
      Evaluation of gastroesophageal reflux before and after sleeve gastrectomy using symptom scoring, scintigraphy, and endoscopy.
      ProspectiveManuscriptIndia35.8 (19-60)47.80.3164.3 ± 18.4NA366 months32068Scintigraphy, Severity Symptoms, and Carlson Dent825NC12
      Viscido et al, 2018
      • Viscido G.
      • Gorodner V.
      • Signorini F.
      • et al.
      Laparoscopic sleeve gastrectomy: endoscopic findings and gastroesophageal reflux symptoms at 18-month follow-up.
      ProspectiveManuscriptArgentina40 ± 947 ± 160.3464 ± 9.4NA4218 months10902237Montreal Consensus364827 of 7310
      Csendes et al, 2019
      • Csendes A.
      • Orellana O.
      • Martinez G.
      • et al.
      Clinical, endoscopic, and histologic findings at the distal esophagus and stomach before and late (10.5 years) after laparoscopic sleeve gastrectomy: results of a prospective study with 93% follow-up.
      ProspectiveManuscriptChile38 ± 10.238.6 ± 2.90.22NANA3895 ± 15 months10441433Burning symptoms446931 of 5312
      Dimbezel et al, 2020
      • Dimbezel V.
      • Nedelcu A.
      • Danan M.
      • et al.
      Endoscopic findings 5 years following sleeve gastrectomy.
      ProspectiveManuscriptFrance49.6 ± 11.740 ± 1.90.1262.4 months404118No clearly defined preop181311
      Lallemand et al, 2019
      • Lallemand L.
      • Greilsamer T.
      • Krempf M.
      • et al.
      Five years sleeve gastrectomy impact on gastroesophageal reflux and esophageal mucosa aspect. a monocentric study.
      ProspectiveAbstractFrance43 ± 1249.4 ± 7.45 years544Unclear
      SD, Standard deviation; BMI, body mass index; WL, weight loss; TBWL, total body weight loss; EGD, esophagogastroduodenoscopy; BE, Barrett’s esophagus; preop, preoperative; postop, postoperative; EE, erosive esophagitis; D&B, Downs and Black score; NA, not available; NDBE, nondysplastic Barrett’s esophagus; NC, not clear.

      Prevalence of BE

      Overall, there were 680 patients, and 54 of these patients had BE. All cases of BE were nondysplastic and were de novo. In addition, all cases were observed in studies with long-term follow-up. The pooled prevalence of BE was 11.4% (95% CI, 7.7%-16.6%; P < .001) (Fig. 2A). There was no significant heterogeneity in the model with I2 = 28.7% (Q = 12.6, P = .18). When we analyzed only the studies that had long-term follow-up, the results were essentially identical with pooled prevalence of BE of 11.5% (95% CI, 7.8%-16.7%; P < .001), I2 = 46%, and Q = 11.2.
      Figure thumbnail gr2
      Figure 2A, The prevalence of Barrett’s esophagus in patients with follow-up esophagogastroduodenoscopy. B, The odds of having Barrett’s esophagus in patients with GERD symptoms compared with those without with or without GERD. C, Funnel plot assessing publication bias. CI, Confidence interval.

      BE and GERD symptoms

      We further assessed the prevalence of BE in patients with or without postoperative GERD symptoms based on 3 long-term studies.
      • Sebastianelli L.
      • Benois M.
      • Vanbiervliet G.
      • et al.
      Systematic endoscopy 5 years after sleeve gastrectomy results in a high rate of Barrett's esophagus: results of a multicenter study.
      ,
      • Felsenreich D.M.
      • Kefurt R.
      • Schermann M.
      • et al.
      Reflux, sleeve dilation, and Barrett's esophagus after laparoscopic sleeve gastrectomy: long-term follow-up.
      ,
      • Soricelli E.
      • Casella G.
      • Baglio G.
      • et al.
      Lack of correlation between gastroesophageal reflux disease symptoms and esophageal lesions after sleeve gastrectomy.
      Overall, 7 patients had BE without postoperative GERD symptoms. The pooled rate on meta-analysis was 10.3% (95% CI, 5%-20%; P < .001). The pooled rate of BE in patients with GERD symptoms was 18.2% (95% CI, 12.4%-26%). There was no significant difference in the odds of having BE based on GERD symptoms (odds ratio, 1.74; 95% CI, 0.52-5.89; P = .37) (Fig. 2B). There was no significant heterogeneity (I2 = 52%, Q = 4.2).
      Only 1 study
      • Felsenreich D.M.
      • Kefurt R.
      • Schermann M.
      • et al.
      Reflux, sleeve dilation, and Barrett's esophagus after laparoscopic sleeve gastrectomy: long-term follow-up.
      reported the rate of columnar lined esophagus (as seen endoscopically). In this study, the rate of columnar lined esophagus was high (50%, n = 10). But only 3 of these patients were confirmed by biopsies.
      These results were also confirmed on multivariable logistic meta-regression analysis, controlling for mean age and follow-up time, which showed no significant association between the prevalence of BE and the prevalence of postoperative GERD (β = 3.5; 95% CI, −18 to 25; P = .75). However, there was a significant association between mean age and prevalence of GERD, when controlling for GERD and follow-up time (β = 0.8; 95% CI, 0.3-1.4; P = .0028). R2 analog was 1. This indicates that the model explained most of the heterogeneity between studies.
      On multivariable logistic meta-regression analysis, there was also no significant association between the prevalence of BE and the duration of follow-up (β = −0.02; 95% CI, −0.3 to 0.3; P = .874) or the prevalence of postoperative esophagitis (β = 1; 95% CI, −4.1 to 6; P = .70).

      Esophagitis after SG

      Seven studies reported esophagitis before and after SG at various follow-up intervals. The study by Tai et al
      • Tai C.M.
      • Huang C.K.
      • Lee Y.C.
      • et al.
      Increase in gastroesophageal reflux disease symptoms and erosive esophagitis 1 year after laparoscopic sleeve gastrectomy among obese adults.
      was excluded from this analysis because the surgeons were reported to be in their initial learning curve, which could skew data from experienced centers. For Soricelli et al,
      • Soricelli E.
      • Casella G.
      • Baglio G.
      • et al.
      Lack of correlation between gastroesophageal reflux disease symptoms and esophageal lesions after sleeve gastrectomy.
      the rate of preoperative esophagitis was extracted from a previous study
      • Genco A.
      • Soricelli E.
      • Casella G.
      • et al.
      Gastroesophageal reflux disease and Barrett's esophagus after laparoscopic sleeve gastrectomy: a possible, underestimated long-term complication.
      on the same cohort. In 5 studies
      • Sebastianelli L.
      • Benois M.
      • Vanbiervliet G.
      • et al.
      Systematic endoscopy 5 years after sleeve gastrectomy results in a high rate of Barrett's esophagus: results of a multicenter study.
      ,
      • Soricelli E.
      • Casella G.
      • Baglio G.
      • et al.
      Lack of correlation between gastroesophageal reflux disease symptoms and esophageal lesions after sleeve gastrectomy.
      ,
      • Elkassem S.
      Endoscopic surveillance three to five years post sleeve gastrectomy: possible progression to reflux esophagitis and Barretts.
      • Csendes A.
      • Orellana O.
      • Martinez G.
      • et al.
      Clinical, endoscopic, and histologic findings at the distal esophagus and stomach before and late (10.5 years) after laparoscopic sleeve gastrectomy: results of a prospective study with 93% follow-up.
      • Dimbezel V.
      • Nedelcu A.
      • Danan M.
      • et al.
      Endoscopic findings 5 years following sleeve gastrectomy.
      with long-term follow-up, the relative increase in the rate of esophagitis was 86% (64%-109%), P < .001, I2 = 47%, Q = 7.6 (P = .107). This means that there is an 86% increase in the risk of esophagitis on long-term follow-up after SG. For short-term studies.
      • Sharma A.
      • Aggarwal S.
      • Ahuja V.
      • et al.
      Evaluation of gastroesophageal reflux before and after sleeve gastrectomy using symptom scoring, scintigraphy, and endoscopy.
      ,
      • Viscido G.
      • Gorodner V.
      • Signorini F.
      • et al.
      Laparoscopic sleeve gastrectomy: endoscopic findings and gastroesophageal reflux symptoms at 18-month follow-up.
      there was a 35% increase (14%-57%), P < .001, I2 = 0, Q = 0.5. This difference between short-term and long-term studies was statistically significant (P = .001; Fig. 3A).
      Figure thumbnail gr3
      Figure 3A, Relative risk increase in the rate of esophagitis after sleeve gastrectomy compared with the preoperative rate of esophagitis. B, Meta-regression of the risk difference of esophagitis based on follow-up times. C, Funnel plot assessing publication bias. CI, Confidence interval.
      On univariate logistic meta-regression analysis, there was a linear relationship between the time of postoperative EGD and the rate of esophagitis (β = 0.08; 95% CI, 0.007-0.16; P = .048). This indicates that the risk of esophagitis increases by 8% each year after SG. The study by Csendes et al
      • Elkassem S.
      Endoscopic surveillance three to five years post sleeve gastrectomy: possible progression to reflux esophagitis and Barretts.
      was acting as an outlier. When this was excluded from the meta-regression, the results on the association between EE and follow-up time were more pronounced: (β = 0.13; 95% CI, 0.06-0.20; P = .0005; Fig. 3B). The funnel plot showed some risk of publication bias (Fig. 3C). A classic fail-safe test showed that we would need to identify 208 additional “null” studies for the combined P value to exceed .05. On meta-regression, the size of bougie used intraoperatively was not associated with the rate of esophagitis (β = 0.036; 95% CI, −0.02-0.09; P = .186).

      GERD after SG

      Eight studies reported the rate of GERD after SG. One study by Dimbezel et al
      • Dimbezel V.
      • Nedelcu A.
      • Danan M.
      • et al.
      Endoscopic findings 5 years following sleeve gastrectomy.
      did not have a clear definition of how GERD was identified preoperatively, so this was excluded from this analysis. As expected, the definition of GERD varied greatly by study, as detailed in Table 1. As a result, significant heterogeneity was noted in the magnitude of postoperative GERD. However, all studies showed the effect estimate to be in the same direction: a significant increase in the prevalence of GERD postoperatively with odds ratios ranging from 1.6 to 49 as shown in Figure 4A. Four studies
      • Felsenreich D.M.
      • Kefurt R.
      • Schermann M.
      • et al.
      Reflux, sleeve dilation, and Barrett's esophagus after laparoscopic sleeve gastrectomy: long-term follow-up.
      ,
      • Viscido G.
      • Gorodner V.
      • Signorini F.
      • et al.
      Laparoscopic sleeve gastrectomy: endoscopic findings and gastroesophageal reflux symptoms at 18-month follow-up.
      ,
      • Csendes A.
      • Orellana O.
      • Martinez G.
      • et al.
      Clinical, endoscopic, and histologic findings at the distal esophagus and stomach before and late (10.5 years) after laparoscopic sleeve gastrectomy: results of a prospective study with 93% follow-up.
      ,
      • Tai C.M.
      • Huang C.K.
      • Lee Y.C.
      • et al.
      Increase in gastroesophageal reflux disease symptoms and erosive esophagitis 1 year after laparoscopic sleeve gastrectomy among obese adults.
      reported on de novo GERD after SG. Among those who had no GERD symptoms before surgery, the rate of having GERD postoperatively was 45% (95% CI, 35%-55%), I2 = 51%, Q = 6.1, P = .106 (Fig. 4B). Use of proton pump inhibitors before and after SG was reported in only 2 of the studies. Sebastianelli et al
      • Sebastianelli L.
      • Benois M.
      • Vanbiervliet G.
      • et al.
      Systematic endoscopy 5 years after sleeve gastrectomy results in a high rate of Barrett's esophagus: results of a multicenter study.
      reported an increase in the use proton pump inhibitors from 22% preoperatively to 76% postoperatively. Similarly, Soricelli et al
      • Soricelli E.
      • Casella G.
      • Baglio G.
      • et al.
      Lack of correlation between gastroesophageal reflux disease symptoms and esophageal lesions after sleeve gastrectomy.
      reported an increase in the use of proton pump inhibitors from 24% preoperatively to 73% postoperatively.
      Figure thumbnail gr4
      Figure 4A, Forest plot of the odds ratios of having GERD after sleeve gastrectomy compared with before. B, Pooled rate of de novo GERD in patients who had no GERD symptoms preoperatively. CI, Confidence interval.

      Considerations: bias and quality assessment

      Based on Down and Black, all studies were of adequate quality to be included in the study (Table 1). Publication bias was assessed using funnel plots. This showed no evidence of publication bias (Fig. 2C), but there was some asymmetry noted due to the 3 studies with zero prevalence of BE. Using the classic fail-safe test, we need to identify 340 additional “null” studies for the combined P value to exceed .05. When removing 1 study at a time from the analysis, we found no evidence of overdue effect on the final results of our study.

      Discussion

      SG has gained wider acceptance as an effective bariatric procedure for patients with severe obesity.
      • Khan S.
      • Rock K.
      • Baskara A.
      • et al.
      Trends in bariatric surgery from 2008 to 2012.
      However, our study shows that the prevalence of BE is high on long-term follow-up after surgery. On meta-analysis of all existing studies, we found that the prevalence of BE was about 11.6%. Furthermore, we found that BE was not limited to patients with GERD symptoms only. BE appeared around 3 years after SG and continued to be detected at 10 years after the procedure.
      Previous meta-analyses
      • Oor J.E.
      • Roks D.J.
      • Unlu C.
      • et al.
      Laparoscopic sleeve gastrectomy and gastroesophageal reflux disease: a systematic review and meta-analysis.
      ,
      • Yeung K.T.D.
      • Penney N.
      • Ashrafian L.
      • et al.
      Does sleeve gastrectomy expose the distal esophagus to severe reflux? A systematic review and meta-analysis.
      focused on GERD and EE after SG. In a meta-analysis by Yeung et al,
      • Yeung K.T.D.
      • Penney N.
      • Ashrafian L.
      • et al.
      Does sleeve gastrectomy expose the distal esophagus to severe reflux? A systematic review and meta-analysis.
      the authors conducted a subanalysis in which they reported the pooled prevalence of BE to be around 8%. However, the results were limited by high heterogeneity of 92%, making the pooled estimate grossly uninterpretable. An abstract by Hoerter et al
      • Hoerter N.A.
      • Smukalla S.M.
      • Pitman M.
      • et al.
      Barrett's esophagus is a long-term complication of sleeve gastrectomy: a systematic review and meta-analysis.
      focused on the prevalence of BE after SG. Although the study has not been published in full yet, we noted that heterogeneity was also high at 88% making interpretation difficult. Despite that, the pooled prevalence of BE in long-term studies was 13.3%, which is similar to our value of 11.6%. We believe that our results are more accurate for several reasons. First, we had a strict a priori protocol with clear inclusion criteria. Specifically, if a study did not ask all, or consecutive patients, to enroll, then the patients who were missed on follow-up EGD may be different from the ones who had no EGD. Including such studies will skew the results. An example of this is the study by Braghetto and Csendes.
      • Braghetto I.
      • Csendes A.
      Prevalence of Barrett's esophagus in bariatric patients undergoing sleeve gastrectomy.
      After the first year of follow-up, EGD was only done “selectively.” As a result, about 47% of patients did not have follow-up EGD at 3 years, and >70% did not have follow-up at 5 years. In such cases, the reported rates of BE and esophagitis may be greatly misleading. Such studies were excluded from our analysis.

      Clinical implications

      To our knowledge, this is the largest evidence-based study to assess the risk of BE after SG as a primary outcome. There are several important clinical implications to our findings. First, due to the growth popularity and demand for SG, bariatric surgeons, primary care providers, and gastroenterologists need to be aware of these potential adverse outcomes. Our data warrant a discussion with patients regarding the risks and benefits of screening for BE after SG. Based on American Society for Gastrointestinal Endoscopy guidelines,
      • Qumseya B.
      • Sultan S.
      • Bain P.
      • et al.
      ASGE Standards of Practice Committee
      ASGE guideline on screening and surveillance of Barrett's esophagus.
      screening for BE may be indicated in any patient population in which the prevalence of BE is more than 10%. Note that 11.6% of cases were de novo; none of the patients who had SG had BE at the screening EGD before the procedure. In our previous meta-analysis,
      • Qumseya B.
      • Gendy S.
      • Wallace A.
      • et al.
      Prevalence of Barrett’s esophagus in obese patients undergoing pre-bariatric surgery evaluation: a systematic review and meta-analysis.
      we studied more than 13,000 patients who had EGD before bariatric surgery and showed that despite their obesity, the risk of BE in this patient population was low (<1%). The above data would suggest that screening might be more useful if started around 3 years after SG. More data on this issue will be needed before such recommendations are adopted in clinical guidelines.
      Second, although BE may take several years to develop, the risk of esophagitis appears to increase by 13% each year based on our regression analysis. Many patients with BE and esophagitis may be asymptomatic. Although these secondary results require further investigation, our results indicate that early post-SG acid suppression may be considered to mitigate the risk of GERD and ultimately the risk of BE and EAC.
      Third, the increased risk of BE due to SG should be discussed with patients at the time of surgical referral. Patients at increased risk of BE should be given the option to have an alternative procedure. These patients may include those with GERD, documented esophagitis, family history of BE or EAC, males, and smokers.
      None of the studies reported on the rate of progression of BE into dysplasia. However, there would be no reason for us to assume that BE after SG would behave differently from BE in other patients. We know, for instance, that cases of EAC and gastric cancers have been reported in patients after SG.
      • Wright F.G.
      • Duro A.
      • Medici J.R.
      • et al.
      Esophageal adenocarcinoma five years after laparoscopic sleeve gastrectomy. A case report.
      ,
      • Masrur M.
      • Elli E.
      • Gonzalez-Ciccarelli L.F.
      • et al.
      De novo gastric adenocarcinoma 1 year after sleeve gastrectomy in a transplant patient.
      In addition, cases of cancer after SG may be diagnosed at later stages because patients have common upper GI symptoms and may present for evaluation at later stages. Therefore, we have to assume that BE in this population has to be considered seriously.
      In addition, there could be clinical implications for endoscopic sleeve gastroplasty (ESG). This procedure has been gaining traction among gastroenterologists and surgeons.
      • Abu Dayyeh B.K.
      • Rajan E.
      • Gostout C.J.
      Endoscopic sleeve gastroplasty: a potential endoscopic alternative to surgical sleeve gastrectomy for treatment of obesity.
      The procedure mimics SG but is done through an endoscope by plicating the wall of stomach on itself to reduce its size. Although ESG mimics SG in its technique, the effect of ESG on GERD, EE, and BE has not been well studied. Fayad et al
      • Fayad L.
      • Adam A.
      • Schweitzer M.
      • et al.
      Endoscopic sleeve gastroplasty versus laparoscopic sleeve gastrectomy: a case-matched study.
      conducted a case-control retrospective study of 83 ESG patients and 54 SG patients. They found that the risk of reflux was lower in the ESG group. However, the true effect of ESG on GERD and EE has not yet been established. We hope that our results will serve as a motivation to clinicians and researchers in the field of ESG to design and conduct research studies that investigate this topic and provide much needed answers.
      Besides the risk of BE after SG, the risk of EE is also of significant interest and shares the same pathophysiology with BE and GERD. Although this was not a primary outcome of our study, it was one of the secondary outcomes planned a priori. We reported the increased risk using the prevalence of EE before and after the procedure. This gives the reader and the patient a better understanding of the magnitude of risk for developing esophagitis after SG. The data we found on EE were compelling. In the long-term studies, the relative increase in EE was 87%. In the short-term studies, the relative increase was 35%. One study
      • Tai C.M.
      • Huang C.K.
      • Lee Y.C.
      • et al.
      Increase in gastroesophageal reflux disease symptoms and erosive esophagitis 1 year after laparoscopic sleeve gastrectomy among obese adults.
      was removed from this analysis. However, the effect estimate of removed studies was high in favor of more EE after SG. Furthermore, our meta-regression showed a 13% increase in the risk of esophagitis every year postoperatively. Although some literature continues to debate the risk of GERD and EE after SG,
      • Rebecchi F.
      • Allaix M.E.
      • Giaccone C.
      • et al.
      Gastroesophageal reflux disease and laparoscopic sleeve gastrectomy: a physiopathologic evaluation.
      the data from our study show a consistent and substantial trend toward more EE after SG. As we have shown, we will need to identify 208 additional studies that show no increase in the risk of EE after SG to negate the results of our study, which would be highly unlikely. As a secondary outcome, our study also assessed the risk of GERD. As we expected, the definition of GERD varied greatly by study. Thus, we could not pool the estimates. However, all studies showed a higher prevalence of GERD after SG compared with before the procedure. Moreover, among patients who had no diagnosis of GERD before the procedure, as many as 40% developed de novo GERD.

      Strengths and limitations

      Our study has several strengths. It is the first study to focus on BE as a primary outcome. Our literature search was broad and inclusive. Heterogeneity was minimal in most of our analyses. In addition, we had a strict definition of studies to be included. This resulted in a more reliable analysis of studies with interpretable effect estimates. When heterogeneity was significant, as was the case with GERD, the effect estimates were not pooled.
      A potential limitation of our study is the relatively small sample size. Despite our comprehensive search, only a few studies reported the outcomes of interest based on our a priori inclusion criteria. Although we recognize that larger studies will be helpful in confirming our results, we also note that our results showed that we would need a large number of “null” studies to negate the results of our analyses.
      In addition, our primary outcome was BE. As a result, some of the secondary outcome results should be used with caution, because we did not set out to find the risk of EE or GERD. However, the trends noted in our study regarding secondary outcomes are consistent and profound and are in line with previous studies.
      We used funnel plots to assess for publication bias despite having fewer than 10 studies. This can cause the power of the test to be low. To adjust for this, we have also reported the results of the classic fail-safe test, which showed a low risk of publication bias.

      Conclusions

      Patients who undergo SG are at increased risk of developing BE. Larger studies are needed to understand the pathophysiology of this phenomenon. Gastroenterologists, primary care providers, and bariatric surgeons should be aware of the above data. Careful discussion with patients regarding the risks of SG before the procedure, and the risk-benefit assessment of screening for BE after SG, should be considered.

      Acknowledgments

      We would like to acknowledge Robyn Rosasco, MSLIS, AHIP, librarian at Florida State University, for her help in developing and running the search strategy.

      Appendix: search strategy

      Ovid MEDLINE(R) and in-process and other non-indexed citations and daily (1946 to present)

      Search run July 2020
      • 1.
        Barrett Esophagus/
      • 2.
        (Barrett$ adj1 (esophagus or oesophagus)).ti,ab.
      • 3.
        (barrett esophag$ or barrett's esophag$ or barretts esophag$ or barrett oesophag$ or barrett's oesophag$ or barretts oesophag$).ti,ab.
      • 4.
        (esophag$ or oesophag$ or esophagoscop$ or oesophagoscop$).ti,ab.
      • 5.
        ((esophagogastric or oesophagogastric or gastro-esophageal or gastroesophageal or gastro-oesophageal or gastrooesophageal or esophageal or esophagus or oesophag$) and (inflamed or inflammation or inflammatory or irritat$ or erythem$ or erythaem$ or inflitrat$ or ulcer or ulcers or ulcerat$ or dyspla$ or hyperplas$ or metaplas$)).ti,ab.
      • 6.
        (reflux or heartburn or GER or GERD or dyspepsi$).ti,ab.
      • 7.
        exp esophagitis/
      • 8.
        1 or 2 or 3 or 4 or 5 or 6 or 7
      • 9.
        exp Bariatric Surgery/ or exp Obesity/su
      • 10.
        (jejunoileal bypass$ or vertical banded gastroplast$ or gastric bypass$ or stomach bypass$ or Roux-En-Y or "fobi" or biliopancreatic diversion or gastric band$ or AGB or biliopancreatic diversion$ or gastroplasty or gastroplasties or gastric stapl$ or stomach stapl$ or bariatric$ or "lap. band" or lap-band or "lap band" or gastric partition$ or sleeve gastrectom$).ti,ab.
      • 11.
        9 or 10
      • 12.
        ("weight loss" or "weight reduction" or obesity or bariatric).ti,ab.
      • 13.
        exp bariatric medicine/
      • 14.
        12 or 13
      • 15.
        (surgery or surgeries or surgical or operation or operations or operative).ti.
      • 16.
        14 and 15
      • 17.
        11 or 16
      • 18.
        (prevalence or incidence or epidemiol∗ or survey or "rapid assessment" or "situation assessment" or "situational assessment" or RAR or cohort or surveillance or seroprevalence or seroincidence or seroepidemiol∗ or screening).ti,ab,kw. or exp epidemiologic methods/ or exp epidemiologic studies/ or exp sentinel surveillance/ or exp seroepidemiologic studies/ or exp cohort studies/ or exp cross-sectional studies/ or exp longitudinal studies/ or exp follow-up studies/ or exp prospective studies/
      • 19.
        8 and 17 and 18

      Embase (Elsevier) (1947 to present)

      Search run July 2020
      • 1.
        ‘Barrett esophagus'/exp OR ((Barrett∗ NEAR/1 esophagus) OR (Barrett∗ NEAR/1 oesophagus) OR "barrett esophag∗" OR "barrett?s esophag∗" OR "barretts esophag∗" OR "barrett oesophag∗" OR "barrett?s oesophag∗" OR "barretts oesophag∗"):ti,ab OR ((esophagi∗ OR oesophag∗ OR esophagoscop∗ OR oesophagoscop∗)):ti,ab OR ((esophagogastric OR oesophagogastric OR gastro-esophageal OR gastroesophageal OR gastro-oesophageal OR gastrooesophageal OR esophageal OR esophagus OR oesophag∗) AND (inflamed OR inflammation OR inflammatory OR irritat∗ OR erythem∗ OR erythaem∗ OR inflitrat∗ OR ulcer OR ulcers OR ulcerat∗ OR dyspla∗ OR hyperplas∗ OR metaplas∗)):ti,ab OR (reflux OR heartburn OR GER OR GERD OR dyspepsi∗):ti,ab OR 'esophagitis'/exp
      • 2.
        ‘Bariatric Surgery'/exp OR 'Obesity'/exp su OR ("jejunoileal bypass∗" OR "vertical banded gastroplast∗" OR "gastric bypass∗" OR "stomach bypass∗" OR Roux-En-Y OR fobi OR "biliopancreatic diversion" OR "gastric band∗" OR AGB OR "biliopancreatic diversion∗" OR gastroplasty OR gastroplasties OR "gastric stapl∗" OR "stomach stapl∗" OR bariatric∗ OR "lap. band" OR lap-band OR "lap band" OR "gastric partition∗" OR "sleeve gastrectom∗"):ti,ab OR (('bariatrics'/exp OR ("weight loss" OR "weight reduction" OR obesity OR bariatric):ti,ab) AND (surgery OR surgeries OR surgical OR operation OR operations OR operative):ti)
      • 3.
        ((prevalence or incidence or epidemiology or survey or surveillance or screening or seroprevalence or seroincidence or cohort or "rapid assessment" or "situation assessment" or "situational assessment" or "RAR"):ti,ab,kw or 'seroepidemiology'/exp or 'seroprevalence'/exp or 'epidemiology'/exp or 'prevalence'/exp or 'epidemiological data'/exp or 'incidence'/exp or 'observational study'/exp or 'cohort analysis'/exp)
      • 4.
        #1 AND #2 AND #3

      Web of Science

      Science Citation Index Expanded (SCI-EXPANDED) --1900-present
      Conference Proceedings Citation Index- Science (CPCI-S) --1993-present
      Search run July 2020
      TS= ("Barrett Esophagus" OR (Barrett∗ NEAR/1 esophagus) OR (Barrett∗ NEAR/1 oesophagus) OR "barrett esophagi∗" OR "barrett's esophag∗" OR "barretts esophagi" OR "barrett oesophag∗" OR "barrett's oesophag∗" OR "barretts oesophag∗" OR esophag∗ OR oesophag∗ OR esophagoscop∗ OR oesophagoscop∗ OR ((esophagogastric OR oesophagogastric OR gastro-esophageal OR gastroesophageal OR gastro-oesophageal OR gastrooesophageal OR esophageal OR esophagus OR oesophag∗) AND (inflamed OR inflammation OR inflammatory OR irritat∗ OR erythem∗ OR erythaem∗ OR inflitrat∗ OR ulcer OR ulcers OR ulcerat∗ OR dyspla∗ OR hyperplas∗ OR metaplas∗)) OR reflux OR heartburn OR GER OR GERD OR dyspepsi∗)
      TS= ("Bariatric Surgery" OR (Obesity NEAR/3 surgery) OR (Obese NEAR/3 surgery) OR "jejunoileal bypass∗" OR "vertical banded gastroplast∗" OR "gastric bypass∗" OR "stomach bypass∗" OR Roux-En-Y OR fobi OR "biliopancreatic diversion" OR "gastric band∗" OR AGB OR "biliopancreatic diversion∗" OR gastroplasty OR gastroplasties OR "gastric stapl∗" OR "stomach stapl∗" OR bariatric∗ OR "lap. band" OR lap-band OR "lap band" OR "gastric partition∗" OR "sleeve gastrectom∗" OR (("weight loss" OR "weight reduction" OR obesity OR bariatric OR "bariatric medicine") AND (surgery OR surgeries OR surgical OR operation OR operations OR operative)))
      TS=(prevalence OR incidence OR epidemiol∗ OR survey OR "rapid assessment" OR "situation assessment" OR "situational assessment" OR RAR OR cohort OR surveillance OR seroprevalence OR seroincidence OR seroepidemiol∗ OR screening OR "epidemiologic methods" OR "epidemiologic studies" OR "sentinel surveillance" OR "seroepidemiologic studies" OR "cohort studies" OR "cross-sectional studies" OR "longitudinal studies" OR "follow-up studies" OR "prospective studies")
      #1 AND #2 AND #3

      Cochrane Library and Central Register of Controlled Trials (CENTRAL)

      Search run on July 2020
      #1 [mh ˆ"Barrett Esophagus"]
      #2 ((Barrett∗ NEAR1 esophagus) OR (Barrett∗ NEAR1 oesophagus)):ti,ab
      #3 (barrett esophag∗ OR barrett's esophag∗ OR barretts esophag∗ OR barrett oesophag∗ OR barrett's oesophag∗ OR barretts oesophag∗):ti,ab
      #4 (esophag∗ OR oesophag∗ OR esophagoscop∗ OR oesophagoscop∗):ti,ab
      #5 ((esophagogastric OR oesophagogastric OR gastro-esophageal OR gastroesophageal OR gastro-oesophageal OR gastrooesophageal OR esophageal OR esophagus OR oesophag∗) AND (inflamed OR inflammation OR inflammatory OR irritat∗ OR erythem∗ OR erythaem∗ OR inflitrat∗ OR ulcer OR ulcers OR ulcerat∗ OR dyspla∗ OR hyperplas∗ OR metaplas∗)):ti,ab
      #6 ("reflux" OR "heartburn" OR "GER" OR "GERD" OR "dyspepsi∗"):ti,ab
      #7 [mh esophagitis]
      #8 #1 OR #2 OR #3 OR #4 OR #5 OR #6 OR #7
      #9 [mh "Bariatric Surgery"] OR [mh Obesity] su
      #10 ("jejunoileal bypass∗" OR "vertical banded gastroplast∗" OR "gastric bypass∗" OR "stomach bypass∗" OR "Roux-En-Y OR fobi" OR "biliopancreatic diversion" OR "gastric band∗" OR "AGB" OR "biliopancreatic diversion∗" OR "gastroplasty" OR "gastroplasties" OR "gastric stapl∗" OR "stomach stapl∗" OR "bariatric∗" OR "lap. band" OR "lap-band" OR "lap band" OR "gastric partition∗" OR "sleeve gastrectom∗"):ti,ab
      #11 #9 OR #10
      #12 ("weight loss" OR "weight reduction" OR "obesity" OR "bariatric"):ti,ab
      #13 [mh "bariatric medicine"]
      #14 #12 OR #13
      #15 (surgery OR surgeries OR surgical OR operation OR operations OR operative):ti
      #16 #14 AND #15
      #17 #11 OR #16
      #18 (prevalence OR incidence OR epidemiol∗ OR survey OR "rapid assessment" OR "situation assessment" OR "situational assessment" OR RAR OR cohort OR surveillance OR seroprevalence OR seroincidence OR seroepidemiol∗ OR screening):ti,ab,kw OR [mh "epidemiologic methods"] OR [mh "epidemiologic studies"] OR [mh "sentinel surveillance"] OR [mh "seroepidemiologic studies"] OR [mh "cohort studies"] OR [mh "cross-sectional studies"] OR [mh "longitudinal studies"] OR [mh "follow-up studies"] OR [mh "prospective studies"]
      #19 #8 AND #17 AND #18

      References

        • Schauer P.R.
        • Kashyap S.R.
        • Wolski K.
        • et al.
        Bariatric surgery versus intensive medical therapy in obese patients with diabetes.
        N Engl J Med. 2012; 366: 1567-1576
        • Khan S.
        • Rock K.
        • Baskara A.
        • et al.
        Trends in bariatric surgery from 2008 to 2012.
        Am J Surg. 2016; 211: 1041-1046
        • Campos G.M.
        • Khoraki J.
        • Browning M.G.
        • et al.
        Changes in utilization of bariatric surgery in the United States from 1993 to 2016.
        Ann Surg. 2020; 271: 201-209
        • Oor J.E.
        • Roks D.J.
        • Unlu C.
        • et al.
        Laparoscopic sleeve gastrectomy and gastroesophageal reflux disease: a systematic review and meta-analysis.
        Am J Surg. 2016; 211: 250-267
        • Coupaye M.
        • Gorbatchef C.
        • Calabrese D.
        • et al.
        gastroesophageal reflux after sleeve gastrectomy: a prospective mechanistic study.
        Obes Surg. 2018; 28: 838-845
        • Genco A.
        • Soricelli E.
        • Casella G.
        • et al.
        Gastroesophageal reflux disease and Barrett's esophagus after laparoscopic sleeve gastrectomy: a possible, underestimated long-term complication.
        Surg Obes Relat Dis. 2017; 13: 568-574
        • Wright F.G.
        • Duro A.
        • Medici J.R.
        • et al.
        Esophageal adenocarcinoma five years after laparoscopic sleeve gastrectomy. A case report.
        Int J Surg Case Rep. 2017; 32: 47-50
        • Qumseya B.J.
        • Bukannan A.
        • Gendy S.
        • et al.
        Systematic review and meta-analysis of prevalence and risk factors for Barrett's esophagus.
        Gastrointest Endosc. 2019; 90: 707-717 e1
        • Shaheen N.J.
        • Richter J.E.
        Barrett's oesophagus.
        Lancet. 2009; 373: 850-861
        • Thrift A.P.
        • Whiteman D.C.
        The incidence of esophageal adenocarcinoma continues to rise: analysis of period and birth cohort effects on recent trends.
        Ann Oncol. 2012; 23: 3155-3162
        • Hayeck T.J.
        • Kong C.Y.
        • Spechler S.J.
        • et al.
        The prevalence of Barrett's esophagus in the US: estimates from a simulation model confirmed by SEER data.
        Dis Esophagus. 2010; 23: 451-457
        • Chandar A.K.
        • Iyer P.G.
        Role of obesity in the pathogenesis and progression of Barrett's esophagus.
        Gastroenterol Clin North Am. 2015; 44: 249-264
        • Qumseya B.
        • Gendy S.
        • Wallace A.
        • et al.
        Prevalence of Barrett’s esophagus in obese patients undergoing pre-bariatric surgery evaluation: a systematic review and meta-analysis.
        Endoscopy. 2020; 52: 537-547
        • Qumseya B.
        • Sultan S.
        • Bain P.
        • et al.
        • ASGE Standards of Practice Committee
        ASGE guideline on screening and surveillance of Barrett's esophagus.
        Gastrointest Endosc. 2019; 90: 335-359 e2
        • Sebastianelli L.
        • Benois M.
        • Vanbiervliet G.
        • et al.
        Systematic endoscopy 5 years after sleeve gastrectomy results in a high rate of Barrett's esophagus: results of a multicenter study.
        Obes Surg. 2019; 29: 1462-1469
        • El Khoury L.
        • Benvenga R.
        • Romero R.
        • et al.
        Esophageal adenocarcinoma in Barrett's esophagus after sleeve gastrectomy: case report and literature review.
        Int J Surg Case Rep. 2018; 52: 132-136
        • Felsenreich D.M.
        • Kefurt R.
        • Schermann M.
        • et al.
        Reflux, sleeve dilation, and Barrett's esophagus after laparoscopic sleeve gastrectomy: long-term follow-up.
        Obes Surg. 2017; 27: 3092-3101
        • Downs S.H.
        • Black N.
        The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions.
        J Epidemiol Community Health. 1998; 52: 377-384
        • Soricelli E.
        • Casella G.
        • Baglio G.
        • et al.
        Lack of correlation between gastroesophageal reflux disease symptoms and esophageal lesions after sleeve gastrectomy.
        Surg Obes Relat Dis. 2018; 14: 751-756
        • Sharma A.
        • Aggarwal S.
        • Ahuja V.
        • et al.
        Evaluation of gastroesophageal reflux before and after sleeve gastrectomy using symptom scoring, scintigraphy, and endoscopy.
        Surg Obes Relat Dis. 2014; 10: 600-605
        • Viscido G.
        • Gorodner V.
        • Signorini F.
        • et al.
        Laparoscopic sleeve gastrectomy: endoscopic findings and gastroesophageal reflux symptoms at 18-month follow-up.
        J Laparoendosc Adv Surg Tech A. 2018; 28: 71-77
        • Elkassem S.
        Endoscopic surveillance three to five years post sleeve gastrectomy: possible progression to reflux esophagitis and Barretts.
        Obes Surg. 2018; 28 (152-2)
        • Csendes A.
        • Orellana O.
        • Martinez G.
        • et al.
        Clinical, endoscopic, and histologic findings at the distal esophagus and stomach before and late (10.5 years) after laparoscopic sleeve gastrectomy: results of a prospective study with 93% follow-up.
        Obes Surg. 2019; 29: 3809-3817
        • Dimbezel V.
        • Nedelcu A.
        • Danan M.
        • et al.
        Endoscopic findings 5 years following sleeve gastrectomy.
        Obes Surg. 2020; 30: 3847-3851
        • Lallemand L.
        • Greilsamer T.
        • Krempf M.
        • et al.
        Five years sleeve gastrectomy impact on gastroesophageal reflux and esophageal mucosa aspect. a monocentric study.
        Obes Surg. 2019; 29: 47
        • Tai C.M.
        • Huang C.K.
        Increase in gastroesophageal reflux disease symptoms and erosive esophagitis 1 year after laparoscopic sleeve gastrectomy among obese adults.
        Surg Endosc. 2013; 27: 3937
        • Tai C.M.
        • Huang C.K.
        • Lee Y.C.
        • et al.
        Increase in gastroesophageal reflux disease symptoms and erosive esophagitis 1 year after laparoscopic sleeve gastrectomy among obese adults.
        Surg Endosc. 2013; 27: 1260-1266
        • Yeung K.T.D.
        • Penney N.
        • Ashrafian L.
        • et al.
        Does sleeve gastrectomy expose the distal esophagus to severe reflux? A systematic review and meta-analysis.
        Ann Surg. 2020; 271: 257-265
        • Hoerter N.A.
        • Smukalla S.M.
        • Pitman M.
        • et al.
        Barrett's esophagus is a long-term complication of sleeve gastrectomy: a systematic review and meta-analysis.
        Gastroenterology. 2019; 156 (S-141)
        • Braghetto I.
        • Csendes A.
        Prevalence of Barrett's esophagus in bariatric patients undergoing sleeve gastrectomy.
        Obes Surg. 2016; 26: 710-714
        • Masrur M.
        • Elli E.
        • Gonzalez-Ciccarelli L.F.
        • et al.
        De novo gastric adenocarcinoma 1 year after sleeve gastrectomy in a transplant patient.
        Int J Surg Case Rep. 2016; 20: 10-13
        • Abu Dayyeh B.K.
        • Rajan E.
        • Gostout C.J.
        Endoscopic sleeve gastroplasty: a potential endoscopic alternative to surgical sleeve gastrectomy for treatment of obesity.
        Gastrointest Endosc. 2013; 78: 530-535
        • Fayad L.
        • Adam A.
        • Schweitzer M.
        • et al.
        Endoscopic sleeve gastroplasty versus laparoscopic sleeve gastrectomy: a case-matched study.
        Gastrointest Endosc. 2019; 89: 782-788
        • Rebecchi F.
        • Allaix M.E.
        • Giaccone C.
        • et al.
        Gastroesophageal reflux disease and laparoscopic sleeve gastrectomy: a physiopathologic evaluation.
        Ann Surg. 2014; 260 (discussion 914-15): 909-914

      Linked Article

      • Screening for Barrett’s esophagus after sleeve gastrectomy
        Gastrointestinal EndoscopyVol. 93Issue 2
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          Sleeve gastrectomy (SG) is an increasingly popular bariatric surgical procedure in which the greater curvature of the stomach is resected, thereby increasing satiety and decreasing appetite through structural and neurohormonal changes. First performed in 1988 as a component of the biliopancreatic division with duodenal switch,1 SG has now evolved into a stand-alone procedure and, since 2013, has become the most common bariatric surgery performed. SG made up over three-quarters of primary procedures to treat obesity in the United States in 2018, with 154,976 cases reported by the American Society for Metabolic and Bariatric Surgery.
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