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REVIEW

CURRENT
OPINION Effects of bariatric surgery on the esophagus
Edoardo Savarino a, Elisa Marabotto b, and Vincenzo Savarino b

Purpose of review
Bariatric surgery is the best therapeutic approach to patients with morbid obesity, but there is mounting
evidence that it is associated with esophageal dysfunctions, including gastroesophageal reflux disease
(GERD) and motor disorders. In the present review, we summarize the existing information on the complex
link between bariatric surgery and esophageal disorders.
Recent findings
Although high-quality studies on these effects are lacking, because of evident methodological flaws and
retrospective nature, the review of published investigations show that pure restrictive procedures, such as
laparoscopic adjustable gastric banding (LAPG) and laparoscopic sleeve gastrectomy (LSG), are associated
with de novo development or worsening of GERD. Moreover, LAGB is the procedure with the greatest
frequency of esophageal motor disorders, including impairment of LES relaxation and ineffective
esophageal peristalsis associated with esophageal dilation. LSG seems to be less associated with
esophageal dysmotility, although evidence derived from studies with objective measurements of esophageal
dysfunction is limited. Finally, RYGB seems to be the best procedure for improvement of GERD symptoms
and preservation of esophageal function.
Summary
Overall, the restrictive-malabsorptive approach represented by RYGB must be preferred to pure restrictive
operations in order to avoid the negative consequences of bariatric surgery on esophageal functions.
Keywords
bariatric surgery, esophageal motility disorders, gastroesophageal reflux disease, obesity, reflux disease

INTRODUCTION pathophysiological alterations leading to GERD


Obesity is a worldwide epidemic in Western coun- [6]. Abdominal fat seems to be the most important
tries [1] and its prevalence, when defined as a BMI at pathogenetic factor, because it contributes to
least 30 kg/m2, increased from 15 to 32.9% through- increase intragastric pressure [7] and the gastro-
out three decades among adults aged 20–74 years in esophageal pressure gradient [8], to favor transient
the USA [2]. In addition, a recent study [3] has also lower esophageal sphincter (LES) relaxations [9]
shown that, over the past four decades, mean BMI and to induce the formation of hiatal hernias
and obesity have increased in most regions and [10]. An additional mechanism by which obesity
countries of the world, even in children and ado- can cause GERD relies on the release of some
lescents aged 5–19 years. The rise in children and hormones, such as estrogens, or on the low serum
adolescents’ BMI has plateaued, albeit at high levels, levels of potentially protective substances, such as
in many high-income countries, but has accelerated adiponectins [11].
in parts of Asia.
The association of obesity with several impor-
tant medical conditions, such as metabolic syn-
a
drome, acute myocardial infarction, hypertension, Gastrointestinal Unit, Department of Surgery, Oncology and Gastroen-
terology, University of Padua, Padova and bGastrointestinal Unit, Depart-
sleep apnea, nonalcoholic fatty liver disease and
ment of Internal Medicine and Medical Specialties, University of Genoa,
type II diabetes mellitus is well known [4]. There is Genoa, Italy
also increasing evidence that obesity is associated Correspondence to Edoardo Savarino, Gastrointestinal Unit, Depart-
with esophageal diseases, including gastroesopha- ment of Surgery, Oncology and Gastroenterology, University of Padua,
geal reflux disease (GERD) and motor disorders [5]. Via Giustiniani 2, 35128 Padova, Italy. Tel: +39 498217749;
As to the mechanisms linking obesity to GERD, in fax: +39 010 3538956; e-mail: edoardo.savarino@unipd.it
particular, various studies have clearly docu- Curr Opin Gastroenterol 2018, 34:243–248
mented that obese patients bear all the main DOI:10.1097/MOG.0000000000000439

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Copyright © 2018 Wolters Kluwer Health, Inc. All rights reserved.


Esophagus

hold and also to slow gastric emptying [13], and the


KEY POINTS latter is the Roux-en-Y gastric by pass (RYGB), which
 Bariatric surgery is an efficient method to successfully is the most frequently used restrictive-malabsorp-
achieve weight loss and improvements in morbidity and tive procedure and serves both to limit the size of the
mortality, but it has been associated with impairment of stomach and to favor selective malabsorption as an
esophageal function leading to GERD and esophageal additional weight loss-inducing benefit [14].
motility abnormalities.
 RYGB is the best approach to avoid the appearance of
GERD symptoms and to improve those cases with
Laparoscopic adjustable gastric banding
preoperative reflux complains, whereas the pure This a restrictive weight loss operation that involves
restrictive procedures, such as LAGB and LSG, often the placement of a silicone ring around the proximal
are associated with worsening of GERD or de novo part of the stomach. The band is connected to a
GERD development in some patients. subcutaneous port, which allows injection of saline
 LAGB is the procedure with the greatest frequency of to adjust the band tightness. Inflation leads to a
esophageal motor disorders, including impairment of reduction in size of the gastric reservoir and limits
LES relaxation and ineffective esophageal peristalsis food capacity. In the early 1990s, the first reports of
associated with esophageal dilation, whereas LSG LAGB were published, suggesting that was a well
seems to be less associated with tolerated and effective weight-loss operation.
esophageal dysmotility.
Among both patients and surgeons, the popularity
 RYGB seems to be the best procedure for patients with of this technique grew rapidly, owing to short
known and unknown preoperative motor disorders operative times, low perioperative morbidity and
because of its absent or minimal effects on mortality, absence of need to re-route the gastroin-
esophageal motility. testinal tract, reversibility of the operation and fewer
 High-quality studies on the effects of the various nutritional deficiencies. Over the next two decades,
bariatric surgery procedures are lacking because of LAGB became the most frequently used operation
evident methodological flaws and their predominant for the management of morbid obesity and obesity-
retrospective nature, thus future high-quality related complications. However, as long-term out-
randomized controlled trials with longer follow-up comes of this procedure were collected, its effective-
examinations are sorely needed.
ness in terms of durability of weight loss and
resolution of comorbidities was questioned. Fur-
thermore, relevant long-term adverse events
Due to the relevant therapeutic limitations of and complications mainly related to the migration
lifestyle modifications and available pharmacologi- of the device were reported, as described in the
cal treatments in inducing weight loss, mainly in the following.
long term, bariatric surgery has become the most
effective therapy in reaching prolonged benefits in
terms of both weight reduction and improvement of Laparoscopic sleeve gastrectomy
the above-mentioned comorbidities and overall This is a restrictive weight loss operation that is
mortality [12] in morbidly obese patients with a performed by removing the majority of the stomach
BMI greater than 35–40 kg/m2. along a line within the angle of His and a point
With the increasing use of bariatric operations, along the greater curvature of the stomach, approx-
however, there is mounting evidence that they may imately 3–6 cm from the pylorus. This results in
affect esophageal function. In this review, we have removing about the 80% of the body and the entire
summarized the effects of bariatric surgery proce- fundus of the stomach, but the pylorus is preserved.
dures on the esophagus with a focus on their impact Obviously, the resection of the majority of the acid-
on GERD and esophageal motor alterations and producing mucosa of the stomach leads to the fact
related symptoms. that the amount of acid in the gastric sleeve is
substantially diminished. Despite little or no mal-
absorptive component to this operation, it has been
BARIATRIC SURGERY PROCEDURES associated with durable weight loss and control of
There are two main categories of bariatric opera- medical comorbidities.
tions: pure restrictive and restrictive-malabsorptive.
The former are represented by the laparoscopic
adjustable gastric banding (LAGB) and the laparo- Roux-en-Y gastric by pass
scopic sleeve gastrectomy (LSG), which are intended A gastric by-pass is performed by creating a small
to reduce the total amount of food the stomach can gastric pouch and a Roux-en-Y gastro-jejunostomy

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Effects of bariatric surgery on the esophagus Savarino et al.

of variable length. In this way, the pouch prevents than objective measurements of reflux [24]. Other
overeating and the long Roux limb decreases calorie important methodological differences among the
absorption. Also this procedure is characterized by various investigators (patient selection, GERD diag-
very little acid production in the proximal gastric nosis, length of follow-up, exclusion criteria) also
pouch. It is associated with durable weight loss and may have affected their study results. Taking into
control of obesity-related comorbidities. For these account the above limitations, there are studies
reasons, RYGB is one of the most commonly per- reporting a decreased prevalence of GERD [25–27]
formed bariatric operations. and other showing an increased prevalence of the
disease [28–30]. However, it must be emphasized
that two investigations [31,32] using objective mea-
EFFECTS OF BARIATRIC SURGERY ON sures of GERD after LSG (esophageal pH-metry and
GASTROESOPHAGEAL REFLUX DISEASE pH-impedance monitoring, respectively) found that
there is an increase in esophageal acid exposure and
Laparoscopic adjustable gastric banding also a major number of nonacid reflux episodes after
Several long-term studies have shown that there is a surgery, thus confirming that LSG can cause the
general increase in GERD following this surgical development of GERD. In fact, it is likely that the
approach in both patients with preoperative symp- sleeve leads to a disruption of the competency of the
toms of GERD, which are aggravated, and in those esophagogastric junction and to an increased inci-
who were previously asymptomatic [15]. Interest- dence of hiatal hernia. Accordingly, two recent
ingly, however, patients with symptomatic GERD studies combining LSG with hiatal hernia repair
often describe an initial improvement of their com- [33,34] have shown a dramatic reduction in postop-
plaints, but some months later (6 months on aver- erative GERD over 12–18 months of follow-up.
age) symptoms tend to return [16–17]. Moreover, it Moreover, a recent multicenter study by Mion
has been shown that the type of symptoms tends to &
et al. [35 ] evaluating, by means of high-resolution
change, because regurgitation predominates post- impedance manometry, 53 patients who underwent
operatively, whereas heartburn is prominent before LSG, showed that the operation significantly modi-
surgery [18]. On the other hand, in a retrospective fied esophagogastric motility, inducing a marked
study by Dixon and O’Brien [19] evaluating 48 increase of intragastric pressure (as potential mech-
symptomatic GERD patients who consecutively anism of reflux occurrence), and a significant aug-
underwent LAGB, in 77% of the cases symptoms mentation of impedance-detected reflux episodes
vanished after 3 weeks of surgery. Furthermore, in associated with GER symptoms and esophageal
another prospective investigation assessing the dysmotility.
aggravation of GERD symptoms in 167 morbidly
obese patients following adjustable gastric banding
[20], 68% of them were symptom-free after the Roux-en-Y gastric bypass
operation. Gastric bypass has been shown to provide excellent
The most severe form of esophageal dysfunction control of typical GERD symptoms. For example,
that results after LAGB is pseudoachalasia, which is a Schauer et al. [36] found that 96% of their patients
condition characterized by esophageal aperistalsis had improvement or total relief of symptoms and
associated with impaired distal esophageal LES none had aggravation of gastroesophageal reflux
relaxation. It is reported in less than 2% of patients occurrence, whereas Frezza et al. [37] observed a
undergoing band placement [21], but it is likely that marked reduction of heartburn, from 87% of
its incidence is underreported because of limited patients preoperatively to 23% postoperatively.
manometric assessment of the phenomenon. It Moreover, the latter authors observed that atypical
has been hypothesized that the progressive filling symptom refractory to conventional medical ther-
of the band overtime leads to stasis in the pouch and apy also improved after RYGB. The protective effect
the relative obstruction can cause regurgitation. of RYGB on GERD was also objectively demon-
Overall, this procedure can favor esophageal dys- strated by means of traditional pH monitoring,
function and other important complications, such which showed that all pH-based parameters
as slippage of the band and erosions [22,23]. improve significantly in both short-term and
long-term investigations [38,39].
The mechanisms by which RYGB mitigate distal
Laparoscopic sleeve gastrectomy esophageal acid exposure and GERD symptoms
The postoperative prevalence of GERD in patients probably depend on the new anatomy formed by
treated with this procedure is highly variable, per- surgery. First, the volume of the new gastric pouch is
haps because of the use of questionnaires rather small, averaging 30 ml [40], and this reduces the

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Esophagus

reservoir’s capacity to promote regurgitation. Sec- in a prospective study carried out using high-reso-
ond, the cardia region of the stomach, where the lution impedance manometry in 25 consecutive
pouch is created, is relatively poor in density of acid- patients who underwent LSG, Del Genio et al. [32]
producing parietal cells. Third, bile reflux is avoided found a normal LES pressure after surgery at a
because of the Roux-en-Y biliary diversion. median follow-up of 13 months. However, this latter
It must be also emphasized that a recent varia- study also reported an increase in ineffective esoph-
tion of the RYGB, that is the omega-loop gastric ageal peristalsis, incomplete bolus transit and retro-
bypass, otherwise known as minigastric bypass or grade flow within the esophagus.
the one anastomosis gastric bypass, was shown to Overall, the medical literature regarding the
prevent the de-novo development of abnormal effects of sleeve gastrectomy on LES function is
&&
reflux or esophagitis [41 ]. However, data evaluat- inconsistent, but this seems to be highly dependent
ing the effect of the omega-loop gastric by-pass on on differences in the surgical technique of gastric
esophageal function are still limited. transection at the time of sleeve creation. However,
more objective data are necessary to understand
this association.
EFFECTS OF BARIATRIC SURGERY ON
ESOPHAGEAL MOTILITY DIORDERS
In addition to the pathophysiological alterations Roux-en-Y gastric by pass
leading to GERD with some of the major bariatric The majority of functional studies do not show any
surgery procedures, the development of frequent esophageal motor alteration after RYGB, although
abnormalities in esophageal motor function has some authors have reported several manometric
been well documented. These unintended conse- abnormalities including hypotonic LES [47,48], and
quences can be very disabling for patients, because an increase in esophageal wave amplitude and esoph-
the predominant symptom is persistent and often ageal wave duration in postoperative patients [48].
progressive dysphagia. Regarding the appearance of dysphagia, two
studies have shown contradictory results [49,50].
At present, the limited evidence of any major esoph-
Laparoscopic adjustable gastric banding ageal motor disorders developing after RYGB is the
Traditional esophageal manometry and the modern main reason why many surgeons recommend this
high-resolution manometry (HRM) have frequently type of operation in patients with known esoph-
demonstrated various motor alterations, such as ageal dysmotility [51].
ineffective esophageal motility or aperistalsis, and
incomplete LES relaxation in patients undergoing
LAGB [42,43]. We have already mentioned the pos- CONCLUSION
sible development of pseudoachalasia, which is a Bariatric surgery is an efficient method to success-
rare but severe complication [21] and can be man- fully achieve weight loss and improvements in mor-
aged by band deflation or band removal. An alter- bidity and mortality, but it can impair esophageal
native treatment option can be the conversion of a function leading to GERD and esophageal motility
LAGB to RYGB, which has been shown to favor a abnormalities. This effect is variable depending on
considerable improvement of dysphagia as well as a the type of operation performed. Although high-
reduction of the intrabolus pressure 5 cm above the quality studies on the effects of the various bariatric
LES [44]. The advantage of this approach consists in surgery procedures are lacking because of evident
improving esophageal dysmotility and providing a methodological flaws and their predominant retro-
concurrent procedure to manage obesity and its spective nature, this review dealing with the existing
related comorbidities. published material in the field seems to permit the
following conclusions:

Laparoscopic sleeve gastrectomy (1) RYGB is the best approach to avoid the appear-
An increase in ineffective peristalsis has been docu- ance of GERD symptoms and to improve those
mented after LSG, resulting in stasis and postpran- cases with preoperative reflux complains,
dial regurgitation [32]. Braghetto et al. [45] reported because the pure restrictive procedures, such as
a hypotensive LES in 73% (17/23) of their patients LAGB and LSG, are associated with worsening of
(n ¼ 20 patients), perhaps because of the disruption GERD or developing of de novo GERD in some
of gastric sling fibers during creation of the sleeve. In patients. A recent study comparing the three
contrast, Petersen et al. [46] found an overall techniques in a very large number of obese
increase in postoperative LES pressure. Moreover, patients (n ¼ 116136) showed that 56.5% of them

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Effects of bariatric surgery on the esophagus Savarino et al.

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