medicina

Review
GERD after Bariatric Surgery. Can We Expect
Endoscopic Findings?
Ramon Vilallonga 1,2 , Sergi Sanchez-Cordero 3, * , Nicolas Umpiérrez Mayor 4 , Alicia Molina 5 ,
Arturo Cirera de Tudela 4 , Elena Ruiz-Úcar 6 and Manel Armengol Carrasco 4

1 Endocrine, Metabolic and Bariatric Unit, Department of General and Digestive Surgery,
Center of Excellence for the EAC-BC, Vall d’Hebron University Hospital,
Universitat Autònoma de Barcelona, Passeig de la Vall d’Hebron 119-129, 08035 Barcelona, Spain;
[email protected]
2 ELSAN, Clinique Saint Michel, Centre Chirurgical de l’Obésité, 83100 Toulon, France
3 Department of General and Digestive Surgery, Igualada University Hospital, Av. Catalunya 11, Igualada,
08700 Barcelona, Spain
4 Department of General and Digestive Surgery, Vall d’Hebron University Hospital,
Universitat Autònoma de Barcelona, Passeig de la Vall d’Hebron 119-129, 08035 Barcelona, Spain;
[email protected] (N.U.M.); [email protected] (A.C.d.T.);
[email protected] (M.A.C.)
5 UCON, Obesity and Nutrition Surgery Unit, Corachan Clinic, Tres Torres, 7, 08017 Barcelona, Spain;
[email protected]
6 Endocrine, Metabolic and Bariatric Unit, Department of General and Digestive Surgery,
Fuenlabrada University Hospital, Rey Juan Carlos University, Camino del Molino, 2, 28942 Madrid, Spain;
[email protected]



* Correspondence: [email protected]



Citation: Vilallonga, R.; Sanchez- Abstract: Background and Objectives: Bariatric surgery remains the gold standard treatment for
Cordero, S.; Umpiérrez Mayor, N.; morbidly obese patients. Roux-en-y gastric bypass and laparoscopic sleeve gastrectomy are the
Molina, A.; Cirera de Tudela, A.; most frequently performed surgeries worldwide. Obesity has also been related to gastroesophageal
Ruiz-Úcar, E.; Carrasco, M.A. GERD reflux disease (GERD). The management of a preoperative diagnosis of GERD, with/without hiatal
after Bariatric Surgery. Can We Expect hernia before bariatric surgery, is mandatory. Endoscopy can show abnormal findings that might
Endoscopic Findings? Medicina 2021, influence the final type of surgery. The aim of this article is to discuss and review the evidence
57, 506. https://doi.org/10.3390/
related to the endoscopic findings after bariatric surgery. Materials and Methods: A systematic review
medicina57050506
of the literature has been conducted, including all recent articles related to endoscopic findings
after bariatric surgery. Our review of the literature has included 140 articles, of which, after final
Academic Editor: Giovanni Tarantino
review, only eight were included. The polled articles included discussion of the endoscopy findings
Received: 7 April 2021
after roux-en-y gastric bypass and laparoscopic sleeve gastrectomy. Results: We found that the
Accepted: 13 May 2021 specific care of bariatric patients might include an endoscopic diagnosis when GERD symptoms
Published: 17 May 2021 are present. Conclusions: Recent evidence has shown that endoscopic follow-up after laparoscopic
sleeve gastrectomy could be advisable, due to the pathological findings in endoscopic procedures in
Publisher’s Note: MDPI stays neutral asymptomatic patients.
with regard to jurisdictional claims in
published maps and institutional affil- Keywords: gastroesophageal reflux disease; endoscopy; bariatric surgery; sleeve gastrectomy; gastric
iations. bypass; hiatal hernia; obesity; GERD

Copyright: © 2021 by the authors. 1. Introduction

Licensee MDPI, Basel, Switzerland. Bariatric surgery (BS) is the most effective treatment for morbid obesity and obtains
This article is an open access article the best long-term outcomes [1]. Bariatric surgery is also the only treatment option that
distributed under the terms and achieves sustained weight loss and has a positive impact on related co-morbidities [2].
conditions of the Creative Commons
Gastroesophageal reflux disease (GERD) is recognized as a linked condition to obesity,
Attribution (CC BY) license (https://
especially morbid obesity [1,3,4]. This association between obesity and GERD is very
creativecommons.org/licenses/by/
well-known. In comparison to the general population, obese patients have 2–2.5 more
4.0/).

Medicina 2021, 57, 506. https://doi.org/10.3390/medicina57050506 https://www.mdpi.com/journal/medicina

Medicina 2021, 57, 506 2 of 9

chances of developing reflux symptoms [5,6]. More than 50% of obese patients develop
GERD symptoms, and the condition is found in up to 70% of morbidly obese patients
who seek bariatric surgery [7,8]. GERD is a common condition with a prevalence of 9%
to 25% in Europe [9] and it is increasing in Eastern and Western countries [3]. Part of
the problem with GERD is that sometimes we cannot find a correlation between self-
reported reflux symptoms and their correlation with objectified reflux, meaning that a high
percentage of patients with severe GERD symptoms do not have true pathological GERD
on objective testing.
Laparoscopic sleeve gastrectomy (LSG) is currently the most performed surgery world-
wide, followed by laparoscopic Roux-en-Y gastric bypass (LRYGB) [10,11]. Laparoscopic
sleeve gastrectomy (LSG) seems to achieve equal weight loss as laparoscopic Roux-en-Y
bypass (LRYGB), but there is still much debate about other aspects, including metabolic co-
morbidity results, long term weight loss, and the quality of life after LSG, mainly concerning
the association with gastroesophageal reflux [2]. Mid and long-term follow-up of GERD
after bariatric surgery is controversial, however, data suggest that some procedures, such
as LSG, could have more severe endoscopic findings compared to clinical symptoms [8].
There is no clear data regarding the correlation between GERD and endoscopic findings,
however, some recent reports suggest that there is a need for endoscopic follow-up after
LSG to avoid potential serious complications. The aim of this review article is to evaluate
the relevant endoscopic findings in patients with GERD symptoms after LRYGB and LSG.
Additionally, this review aims to elucidate the appearance of GERD in patients after LSG
and LRYGB, and the endoscopic findings and correlations with clinical symptoms.

2. Materials and Methods

2.1. Search Strategy and Study Selection
An online search was conducted in PubMed/MEDLINE in February 2021 to identify
articles reporting gastroesophageal reflux disease (GERD) and endoscopic findings after
bariatric surgery. The eligible studies were selected following PRISMA guidelines. The
searched keywords used were “gastroesophageal reflux”, “GERD”, “de novo GERD”,
“endoscopy”, “Roux-en-Y gastric bypass”, or “following sleeve gastrectomy” or “following
LSG”. The reference list of the selected studies was also manually checked to identify
relevant papers. The conference abstracts considered as “gray literature”, were not selected.
No publication date or language limit was considered for our search strategy.
Two authors searched and reviewed the full text of all clinical studies. The reference
lists of selected studies were examined to obtain other relevant articles. The inclusion
criteria of the review were the management or treatment of GERD after LSG or LRYGB.
The most relevant, or comprehensive publications were finally included in the analysis to
avoid duplicates, ambiguity, or papers reporting data from the same study population.
A total of 140 records were identified by the initial search of the PubMed/MEDLINE
databases. Of these, 125 papers were excluded after screening by title and abstract. Our ini-
tial analysis included a prescreen to identify the clearly irrelevant reports by title, abstract,
and keywords of the publication. Relevant papers, including short series, review papers,
and meta-analysis were kept for the further review process. Two other independent review-
ers (AC. and SS.) then assessed the studies for relevance, inclusion, and methodological
quality. The studies were classified as relevant (meeting all specified inclusion criteria);
possibly relevant (meeting some but not all inclusion criteria); and rejected (not relevant to
our review). Two reviewers (ER. and RV.) independently reviewed the full-text versions of
all studies classified as relevant or possibly relevant. Any disagreements were resolved by
repeat extraction.

2.2. Data Extraction and Quality Assessment

Two investigators extracted data from each included study, which were then reviewed
independently by a third investigator (ER). The extracted information included details of
Medicina 2021, 57, 506 3 of 9

clinical and demographic characteristics (e.g., age, gender), number of patients, GERD
symptoms, and endoscopic findings. All repetitive information was excluded.

3. Results
Search Results
A total of 140 studies were identified using our search criteria for screening. After
an assessment of the title, according to our inclusion criteria (endoscopic findings as a
primary outcome), 125 articles were removed as they were not relevant and specific for the
topic. Finally, 15 studies remained for content review. Of the 15 studies, 8 were identified
as being not relevant for the paper, as they mixed aspects of our primary key questions
with other aspects of their proper research. Thus, a total of 7 primary studies meeting the
inclusion criteria, and one meta-analysis, were identified after careful screening, and are
summarized in Table 1.

Table 1. RYGB-Roux en Y gastric bypass, SG-Sleeve Gastrectomy, Pts—patients; yrs—years; mo—months; Endoscopic find-
ings were graded according to the Los Angeles Classification, Barrett’s esophagus was biopsy proven. NA: not applicable.

Interval Endoscopic Weight Loss

Number of Age Gender Time from Additional
Study Journal/Year Patients (Years) (Female) Surgery to Findings Results at Comments
Endoscopy (Pts) [%] Evaluation

Esophagitis Esophagitis
(C and D LA) improved in
(5) [10.6%] 19 patients
Borbély et al. Barrett’s (41.3%),
SOARD 2018 47 36.5 27 esophagus 30.3
(100%RYGB) (19–67) (57.4%) 3.8 yrs (3–12) (20.3–47.2) remained
[12] (7) [14.9%] similar in 14
Marginal (30.4%), and
ulcers (4) worsened in
[8.5%] 13 (28.3%).
Reflux
esophagitis
(6) [2.4%]
Marginal
ulcer (46)
[18.4%]
Stomal
Boerlage stenosis (26)
SOARD 2020 98 41 [10.4%] TWL% 25.7
(100%RYGB) (±10.0) 223 (89.2%) 7 Mo (2–16) (±12.9)
et al. [13] Bleeding (7)
[2.8%]
Candida
esophagitis
(3) [1.2%]
Food
impaction (2)
[0.8%]
Marginal
ulcer (13)
Gastrointestinal [27%]
Huang et al. 49 42 Stomal
endoscopy (100%RYGB) 46 y (28–65) (85.7%) 49 Mo
[14] 2003 stenosis (9)
[19%]
Esophagitis
(2) [0.4%]
Medicina 2021, 57, 506 4 of 9

Table 1. Cont.

Interval Endoscopic Weight Loss

Number of Age Gender Time from Additional
Study Journal/Year Patients (Years) Findings Results at
(Female) Surgery to (Pts) [%] Evaluation Comments
Endoscopy
SG had more
de novo EE
HH de novo than GBP
SG group (25% vs. 5%,
(20) [46%] p = 0.001).
RYGB group EE improved
227 in 10%, was
Signorini Surgical RYGB 80 (1) [2%] resolved in
endoscopy (35.2%) 44.9 (36–53) 179 (78.9%) 2 yrs HH+EE post- NA 31.2%,
et al. [15] SG 147 operative
2019 worsened in
(64.8%) SG group 2.5% and
(16) [11%] remained
RYGB group unchanged
(8) [10%] in 10% of
RYGB
cases.
LSG was
associated
Correlation with a higher
23 studies ** of
Lihu Gu et al. Obesity LSG 2463 endoscopic risk of GERD
(49.2%) NA NA NA NA than LRYGB
[16] Surgery 2019 RGYB 2537 findings and (odds ratio
(51.3%) GERD [OR] = 5.10
symptoms. [3.60–7.23],
p < 0.001).
Esophagitis
(A and B LA)
(17) [35.4%] RYGB
Esophagitis
Dimbezel Obesity 48 49.63 42 40 ± 1.89 conversion
100% LSG (±11.69) (87.5%) 62.4 mo (C and D LA) kg/m2 improved EE
et al. [17] Surgery 2020
(1) [0.2%] (14) [29.2%].
Barrett’s
esophagus
(4) [8.3%]
CLE is
significantly
Hiatal hernia longer in
de novo (9)
[16.9%] patients who
Columnar suffer from
lined symptomatic
esophagus reflux
Felsenreich Obeisty 53 (10) [5.3%] (4.0 mm)
et al. [18] Sugery 2017 100% LSG 38.4 (±12.4) 42 (79%) 129 mo
(symp- than in
tomatic patients who
reflux, 7; no do not
reflux, 3). (2.3 mm)
Barrett’s (p = 0.013).
esophagus RYGBP
(3) [15%] conversion
due to reflux
(8) [14%]
Erosive
esophagitis
(33) [84.6%]
Esophagitis mean time of
appearance
(A and B LA)
Braghetto Arq Bras Cir 39 (28) [71.7%] 38.4 + 13.4 of reflux
Dig 2021 100% LSG 43.7 (±8.5) 34 5.6 (±2.5 yrs) Esophagitis kg/m2 symptoms
et al. [19]
(C LA) (5) after surgery
[12.8%] was 26.8 +
Barrett’s 24.1 mo.
esophagus
(5) [12.8%]
** Systematic review and meta-analysis include 23 studies: 6 RCTs, 6 prospective observational studies, and 11 retrospective observa-
tional studies.

4. Discussion
There is a vast amount of controversy regarding the symptoms of GERD and their
correlation with previous bariatric surgery, and the anatomical situation of the esophageal
hiatus. Studies concerning the analysis of the initial anatomical situation of an obese
Medicina 2021, 57, 506 5 of 9

patient, which occurs whenever a LRYGB or LSG is performed, are extremely limited. In
fact, there is little evidence that allows us to promote any single technique according to
the hiatus situation. It seems that when large hiatal hernias are present in an obese patient
in the preoperative setting, LRYGB is the most reasonable surgery [20]. However, some
authors have developed protocols to include large hiatoplasties with mesh placement, and
even antireflux surgical strategies, while performing LSG.
As we can see in Table 1, sometimes there is a lack of clear correlation between self-
reported reflux symptoms and endoscopic findings [21]; bariatric surgery caused either de
novo GERD or the aggravation of existing GERD. Gu et al. [16] found the improvement or
remission of GERD (40.4%) in LSG and (74.2%) in LRYGB patients. LRYGB had a better
effect on GERD (OR = 0.19, 95% CI: 0.12–0.30, p < 0.001) compared to LSG, especially within
3 years and > 3 years [16]. 3534 patients were included, 1918 were subjected to LSG and
1616 to LRYGB, the appearance of new GERD was 9.3% and 2.3% after LSG and LRYGB,
respectively (179 in LSG and 37 in LRYGB). In the global analysis, the authors found that
LSG showed a higher risk of GERD than LRYGB (OR = 5.10, 95% CI 3.60–7.23, p < 0.001);
the results were consistent in the subgroup analysis according to type of study, follow-up
time, low heterogeneity, and the risk of GERD after surgery.
LSG is known to have long-term complications related to GERD when compared to
LRYGB [17]. The appearance of GERD and its evolution after LSG or LRYGB is related
to the drawbacks of these two types of bariatric surgeries. The signs of improvement
in GERD following LSG include: the acceleration of gastric emptying [22], a decrease in
intra-abdominal pressure associated with the weight loss, and a decrease in acid production
with the resection of the stomach [1]. However, the worsening of GERD following LSG
includes predominantly the dissection of the gastroesophageal junction [1], the decrement
of the lower esophageal sphincter pressure [23], and the modification of the anatomy at the
angle of Hiss (responsible for the immediate postoperative GERD) [24].
Some authors defend a routine endoscopy prior to bariatric surgery. Moulla, Y. et al. [25]
published a study where the incidence of upper-GI pathologies detected prior to bariatric
surgery was evaluated. They reported a total of 636 obese patients with a median BMI
(body mass index) reaching super-obesity (Mean BMI: 49 kg/m2 [range 31–92]). Endoscopy
detected pathological conditions, such as Helicobacter pylori (Hp) gastritis, in more than
20% of endoscopies, and gastric or duodenal polyps in 6.8%. They also described peptic
ulcers in 3.5% of the patients. Reflux esophagitis could be detected in 21.9%. Barrett’s
esophagus (BE) was histologically diagnosed in 15.0%, while BE was suspected endo-
scopically in only 11.3%. Esophageal adenocarcinomas were detected in 0.5%. However,
these endoscopic and pathological findings only changed the operative strategy in 1.6%
(10 patients) [26]. In agreement with the other authors, they concluded that preoperative
upper-GI endoscopy identifies a wide range of abnormal endoscopic findings in obese
patients, which may have a significant impact on decision-making, so it should be consid-
ered in all obese patients before a bariatric procedure [25]. Unfortunately, the influence of
preoperative gastroesophageal reflux disease cannot always be evaluated due to the lack of
routine preoperative upper endoscopy, especially in LRYGB [18,26].
On the other hand, Saarinen T. et al. analyzed the clinically significant findings in
preoperative endoscopy and how they associate with preexisting GERD symptoms and
premalignant lesions. They included 1474 operations, of which 71.0% were RYGB and 27.6%
were LSG. They reviewed 86.5% preoperative endoscopic reports, finding that 50.7% were
normal and 23.0% had a clinically significant finding, relevant for LSG (HH, esophagitis,
BE, esophageal dysplasia). In the same analysis, for patients undergoing LRYGB, only 1.6%
of the patients had significant findings relevant for LRYGB (peptic ulcer, atrophic gastritis,
gastrointestinal stromal tumor, GIST) and 3.2% of the patients with LSG were converted
to LRYGB, due to GERD [27]. These data show that preoperative endoscopy is indicated
before LSG, but could be avoided in asymptomatic patients for LRYGB without the risk of
gastric pathology.
Medicina 2021, 57, 506 6 of 9

During the follow-up, upper gastrointestinal symptoms are often difficult to interpret
after LSG and LRYGB [13]. Abdominal pain is an especially common symptom after
bariatric surgery and endoscopic exploration is commonly used to discard any type of
potential complication. However, most common complications can cause gastrointestinal
symptoms, such as gallstone disease, marginal ulcer, internal herniation, and stomal
stenosis in LRYGB. Stenotic sleeves can also lead to abdominal symptoms, including GERD,
nausea, and vomiting [28–30]. Complementary explorations need to be performed, such as
an upper gastrointestinal X-Ray and upper endoscopy. With these imaging tests, we aim
to understand what could produce complications. There is a lack of evidence and clinical
data to help us understand which patients will benefit more from an upper endoscopy,
because of the high number of upper endoscopies without relevant findings.
Tai et al. [3] show that GERD with morbid obesity and LRYGB substantially improves
not only the reflux symptoms but also the erosive esophagitis. Csendes et al. [4] concluded
that LRYGB is effective to control pathological gastroesophageal reflux in patients with
morbid obesity and Biter et al. [2] demonstrated in a randomized controlled trial that pa-
tients who underwent LSG have significantly higher GerdQ scores at both 2 and 12 months,
postoperatively, than patients who underwent LRYGB.
An abnormal upper gastrointestinal endoscopy series and dysphagia as a reason
for GERD for referral were associated with stomal stenosis in LRYGB [9,31] and margin
ulcer [30] after LRYGB. Marginal ulcer incidence has been described as ranging from 0.1%
to 4.6% after LRYGB [32]. It is most prevalent in the first year after surgery, but not restricted
to the first year, with a mean time between surgery and the first symptoms of approximately
4 months [33]. Stomal stenosis has reported a prevalence ranging from 3.1% to 7.8% [34].
Some of these patients might refer to GERD symptoms, however, it is infrequent to find clear
esophagitis in LRYGB patients complaining of upper gastrointestinal symptoms [29,30].
In contrast to the situation following LSG, Gastroesophageal reflux after sleeve gastrec-
tomy is mainly due to the progressive dilatation of cardia, or the presence of a hiatal hernia
for an extended period after surgery. It is, however, very relevant and important to notice
that asymptomatic patients might have very abnormal endoscopic findings, including
esophagitis grades B or C, or even Barrett’s esophagus [35]. The lack of clinical correla-
tion between endoscopy findings and patient symptoms, especially after LSG, have been
recently described in the long-term follow-up after laparoscopic sleeve gastrectomy [36].
Genco et al. first demonstrated that almost 17.2% of 110 patients undergoing LSG will de-
velop Barrett’s esophagus (BE) at a median follow-up superior to 55 months. Interestingly,
the authors also reported that 26.4% of patients with Barrett’s had no GERD symptoms.
This preliminary finding was also confirmed by Soricelli et al. reporting that 21% of patients
with evidence of BE had no symptoms of GERD. [37] Felsenreich et al. [18] also reported
a high prevalence of BE in 15% of the patients, 10 years after SG, associated with 45% of
esophagitis, while only 37% of patients complained of GERD symptoms. From these data,
we can extract that the need for systematic endoscopic control beyond 5 years after LSG
is independent to the presence of GERD symptoms. More recently, the ASMBS position
statement on the rationale for the performance of upper gastrointestinal endoscopy, before
and after metabolic and bariatric surgery, stated that a clinical evaluation by symptoms
alone does not reliably diagnose or rule out GERD, and that patients with conclusive and
objective evidence of preoperative GERD are better served by current techniques of RYGB,
rather than SG [38]. Both the expert panel and the current available literature recommend
an endoscopy screening of all patients with gastrointestinal symptoms, including GERD
symptoms. Therefore, it would be reasonable to perform an endoscopy on patients 3 years
after SG, irrespective of GERD symptoms, to rule out Barrett’s esophagus [38].
Another debate is the correlation between symptoms and time after surgery. Shorter
time between LRYGB or LSG and the onset of symptoms can lead to technical aspects,
such as stenosis of the anastomosis or a kinking of the LSG, which causes an abnormal
functioning of the sleeve, along with nausea, vomiting, and GERD [39].
Medicina 2021, 57, 506 7 of 9

In a recent meta-analysis, in which GERD symptoms were evaluated after bariatric

surgery, LSG was converted to LRYGB for patients suffering from severe GERD [16]. The
conversion rate was approximately 1.82–8.91% [16]. RYGB is an antireflux procedure
because the new anatomy avoids bile reflux, and the small lesser curvature in the gastric
pouch excludes the acid-secreting gastric fundus dramatically. It should be stressed that a
conversional RYGB due to GERD from a SG should be done with a short gastric pouch.
The conversion from LSG to LRYGB to treat severe GERD after LSG (with or without
relevant endoscopic findings) requires complementary studies to detect anatomical defects,
such as hiatal hernia de novo [18,31,40,41]. As the effect of a RYGB conversion on the
evolution of Barrett’s mucosa is still unclear, endoscopic surveillance should be wisely
performed in this setting. Bariatric surgery can improve GERD symptoms; however, new
data need to emerge in the next few years, especially to avoid the lack of correlation
between endoscopy and symptoms.

5. Conclusions
Endoscopic findings after bariatric surgery are controversial and might have a bad
correlation with clinical symptoms. It seems that GERD outcomes for patients with previous
GERD or de novo symptoms, are better in patients after being operated by LRYGB, than
by LSG. There is a need to study in more depth the meaning of these GERD events,
both in the preoperative period and after any bariatric procedure. Multifactorial reasons
appear to be related to GERD. In order to avoid severe complications in the mid-long
term, such as the appearance of the worsening of GERD, we should recommend LRYGB
conversions. Endoscopy should also be recommended after bariatric surgery when clinical
symptoms are present and after 3 years of a SG, even without symptoms, in order to
diagnose Barret’s esophagus.

Author Contributions: Individual contributions are: Conceptualization, R.V. and S.S.-C.; methodol-
ogy, S.S.-C. and A.C.d.T.; formal analysis, S.S.-C.; resources, N.U.M.; data curation, S.S.-C.; writing—
original draft preparation, R.V., A.M., E.R.-Ú., M.A.C.; writing—review and editing, all authors. All
authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: Ethical review and approval were waived for this study, due
to no inclusion of patients from our institution; Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: All the data are available from the corresponding author upon reason-
able request.
Conflicts of Interest: The authors declare no conflict of interest.

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