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Impact of Laparoscopic Sleeve Gastrectomy on Gastrointestinal Motility.

1. Introduction

Laparoscopic sleeve gastrectomy (LSG) is the most frequently performed procedure in the world and has overtaken the "gold standard" Roux-en-Y gastric bypass (RYGB), which remains the most performed bariatric/metabolic procedure only in Latin/South America. The trend analysis demonstrated that LSG had the largest average annual percentage increase of approximately 9% from 2013 of the worldwide bariatric/metabolic surgical procedures [1]. Laparoscopic sleeve gastrectomy is positioned between the adjustable gastric banding and RYGB in terms of morbidity with effectiveness comparable to RYGB even at five years [2, 3].

Laparoscopic sleeve gastrectomy involves the removal of the gastric fundus and greater curvature portion of the stomach, leaving only a lesser curvature tube. Yehoshua et al. showed that after the sleeve, the fundus, which is the most distensible part of the stomach, is removed, thus leaving a sleeve which is characterized by markedly lesser distensibility and high intraluminal pressure, leading to the feeling of early satiety [4]. The abstraction of the fundus is related to physiological alterations in the upper gastrointestinal tract, since the angle of His and the receptive relaxation mechanism is abolished, and the gastric pacemaker is abandoned. Furthermore, the antrum is preserved in some cases depending on the distance of the resection, and the pylorus remains intact. These physiological changes are expected to provoke motility alterations at the gastrointestinal tract.

The aim of the study was to review the impact of laparoscopic sleeve gastrectomy on gastrointestinal motility.

2. Material and Methods

2.1. Search Strategy. A search of the medical literature was undertaken in Pubmed, Web of Science, and Cochrane library until August 2017. The keywords used were "sleeve gastrectomy" AND (motility OR gastrointestinal motility OR esophageal motility OR gastric motility OR bowel motility OR emptying OR manometry).

2.2. Eligibility Criteria

2.2.1. Types of Studies. All studies assessing the impact of LSG on gastrointestinal motility were included. Esophageal, stomach, and bowel motilities were assessed separately.

2.2.2. Types of Participants. The types of participants were obese patients (BMI > 30) undergoing laparoscopic sleeve gastrectomy.

2.2.3. Types of Outcome Measures. The outcomes measured were esophageal, gastric, and bowel motility.

2.3. Inclusion and Exclusion Criteria. Two independent reviewers (Eleni Sioka and Konstantinos Perivoliotis) screened abstracts, reviewed full text versions of all studies classified, and extracted data. Any trial considered relevant was retrieved for further review. The full texts were independently assessed by two reviewers. Disagreements were resolved with a third reviewer. Only published articles in the English language were included. Meta-analysis, systematic reviews, letters to the editor, case studies, non-English language publications, duplicate studies, experimental studies, and conference papers were excluded.

2.4. Data Extraction and Quality Assessment. One reviewer (Konstantinos Perivoliotis) extracted data from selected trials and a second reviewer (Eleni Sioka) checked for accuracy. The data were standardized and extracted from each study, and data were recorded into a database. The variables collected were first author, year of publication, country, type of study, number of participants, method of assessment, timing points, and main findings.

3. Results

3.1. Study Selection. One hundred seventy eight studies were screened for eligibility and fifty two studies assessed in full text. Twenty four studies were excluded due to various reasons. Finally, 28 studies were eligible to be included in the review (Figure 1). There was complete agreement among the authors as to the inclusion of these studies.

3.2. Esophageal Motility. Nine studies assessed esophageal motility. Two studies were conducted in Greece [5, 6], one in France [7], two in Italy [8, 9], one in Argentina [10], one in Netherlands [11], one in Germany [12], aand one in Chile [13]. All except of one [7] were prospective studies.

The postoperative follow-up ranged from 6 days to 50 months. The bougie size ranged from 32 to 40F. The distance from the pylorus ranged from 2 to 6 cm. The lower esophageal sphincter (LES) length was reduced in three studies [5, 9, 13] increased in two studies [6, 10], and unchanged in one study [8]. The LES resting pressure decreased in four studies [5, 10, 11, 13], increased in two studies [6, 12], and remained unchanged in two studies [8, 9]. The amplitude pressure was reduced in two studies [5, 11], increased in one study [10], and unchanged in one study [8]. Amplitude pressure decreased in distal esophagus and increased in the other parts in one study [6]. Ineffective motility was reported in four studies. The percentage was increased from 10% to 45% postoperatively in one study [9], while it was the same preoperatively (7%) in another study [10], was increased at 5% (1/20 patients) in one study [11], and was reported at 37.7% (20/53 patients) in another study [7]. The percentage of normal peristaltic contractions was not affected in one study [11], while it increased in another study [5]. The summary of studies is reported in Table 1.

3.3. Stomach Motility. Eighteen studies assessed stomach motility. Eleven studies were conducted in Europe (Spain [n = 2] [14, 15], Italy [n = 3] [16-18], Greece [n = 3] [19-21], Czech Republic [n = 1] [22], Germany [n = 1] [23], and the Netherlands [n = 1] [24]), whereas one study was performed in the USA [25], two studies in India [26, 27], one study in New Zealand [28], one in Egypt [29], one in Chile [30], and one in Israel [31]. Twelve studies were prospective studies, four studies were prospective randomized controlled studies [14, 17, 22, 27], and two were retrospective studies [18, 25]. The method of gastric emptying assessment was gastric scintigraphic studies in fourteen studies and magnetic resonance imaging (MRI) in one study [23], while one study assessed the gastric slow-wave pacemaking using laparoscopic high-resolution (HR) electrical mapping [28], and two studies assessed the gastroduodenal transit time by radiological upper gastrointestinal series [18, 25].

The postoperative follow-up ranged from 3 to 24 months. The bougie size ranged from 32 to 48F. The distance from the pylorus ranged from 2 to 8 cm. All studies showed accelerated gastric emptying after LSG except for one [31]. Functionally, the sleeve was divided into a passive sleeve and an accelerated antrum. The patients demonstrated a rapid gastroduodenal transit time. The resection of the gastric pacemaker had as a consequence aberrant distal ectopic pacemaking or bioelectrical quiescence after LSG. No correlation was observed between gastric emptying and postprandial symptoms in one study. No correlation was found between gastroduodenal transit time and weight loss in one study [25], while in another study, patients showing a rapid gastroduodenal transit had better weight loss than patients presenting with a slow voiding rate [18]. The summary of the studies are presented in Table 2.

3.4. Bowel Motility. Three studies assessed the bowel motility. Two were prospective studies and one was prospective randomized study. One study was conducted in Japan, one in Greece, and one in India [21,27,32]. Trung et al. evaluated the intestinal motility using cine MRI preoperatively and 3 months postoperatively and found reduced intestinal transit time leading to accelerated intestinal motility [32]. Melissas et al. evaluated prospectively 21 patients preoperatively with a g-camera and 4 months postoperatively. Apart from the acceleration of small bowel transit time, the authors showed that initiation of cecal filling and the ileocecal valve transit was delayed [21]. Similarly, Shah et al. showed decreased small bowel transit time after LSG [27] (Table 3).

4. Discussion

The aim of this study was to review the impact of laparoscopic sleeve gastrectomy on gastrointestinal motility. The gastrointestinal motility research might be essential to recognize the behavior of the created sleeve, to explain possible clinical symptoms-implications, and to elucidate possible mechanisms of actions of this procedure. According to the Second International Consensus Summit for Sleeve Gastrectomy, the panel of experts voted the following as mechanisms of action: restriction:

79%, gastric emptying: 0%, hormonal: 16%, malabsorption: 0%, and other: 3% [33]. Since 2007, LSG was characterized as more than a restrictive procedure [19]. Additional supportive evidence came from studies assessing hormonal alterations after LSG. Concerning hormonal changes, it seems that patients experienced a pronounced and long-lasting decrease of circulating ghrelin and increased postprandial release of the CCK, GLP-1, and PYY, the so-called gut peptides after LSG. It was hypothesized that the faster delivery of nutrients to the distal intestinal tract postoperatively may provoke increased the postprandial release of the gut peptides contributing to the improvement of glucose control as well as to the reduction of food intake and subsequently body weight [34].

The esophageal motility was assessed in several studies. The limitations of the studies include the small sample size. The data remain debatable. The variability in the outcomes of esophageal motility may be attributable to the timing of postoperative follow-up, the variability of surgical techniques, the different bougie sizes, and the different dissections from pylorus, thus creating a sleeve with variable distensibility and intraluminal pressure with, in part, the preservation of the antrum. The percentage of peristaltic normal contractions increased postoperatively and is not statistically significant at 3 months [11] but statistically significant later [5]. It seems that the motility of the body of the esophagus was normalized. Perhaps, this might be attributable to the reduced intrabdominal pressure due to weight loss. An increase in the esophageal acidification was reported in few studies [9, 11]. Del Genio et al. pointed out a decrease in the esophageal transit after LSG in impedance study. Furthermore, the authors explained the reflux episodes as a consequence of retrograde movements into the esophagus [9].

Gastric motility emerges as the role of the stomach as an endocrine organ. Gastric motility acts as a central mediator of hunger, satiation, and satiety. Gastric emptying plays a key role in regulating food intake. Gastric distention acts a satiety signal to inhibit food intake [35]. During food intake, it is the gastric distention and gastric accommodation that regulate satiation in a manner. After food intake, when the stomach empties gradually, it is the gastric emptying and the intestinal exposure of the nutrients that play a key role, while the role of gastric distention follows. It seems that gastric accommodation and gastric emptying are implicated in the regulation of gastric distention and intestinal exposure of nutrients, thus control satiation and satiety. The correlations between gastric accommodation, gastric emptying, and body weight suggest that gastric motility may also affect the long-term regulation of body weight [36].

A number of studies assessed gastric motility. Baumann et al. showed that the sleeve was completely motionless without any coordinate peristalsis, while the antrum had faster peristaltic folds, concluding that gastric emptying is directly linked to the function of the antrum when the antrum is preserved in LSG [23]. It seems that the resection of the normal gastric pacemaker during LSG had as a result the acute gastric slow-wave quiescence or the generation of distal ectopic pacemakers accompanied by a markedly increased propagation velocity. It seems that the sleeve affects the electrophysiology of the stomach. Further studies are needed to support this.

There was a consensus except for one study that gastric emptying was accelerated. The rapid gastric emptying was also strengthened by the observation of our team that a significant proportion of patients experienced dumping syndrome upon provocation at six weeks and 6 and 12 months after LSG. These symptoms included both early and late symptoms suggesting that LSG may lead to changes in eating patterns after LSG, especially in sweeters [37, 38]. Only one study showed no effect on gastric emptying. In this study, the follow-up was done in 3 months, and the created sleeve was performed using a bougie 48F at a distance of 6 cm from the pylorus [31]. Therefore, the sleeve might be large enough without increasing its intraluminal pressure.

There is still a debate concerning the maintenance of the antrum in order to avoid interference with the gastric physiology or its resection to increase the restrictive mechanism. Abdallah et al., who compared groups with resections at 2 cm versus 6 cm distances from the pylorus, showed that there was statistically significant excess weight loss between the groups, concluding that increasing the size of the resected antrum was associated with better weight loss, without increasing significantly the rate of complications [39]. Similarly, Obeidat et al. showed that patients with resection at 2 cm distance from the pylorus experienced statistically significant better maintained weight loss than did patients with resection at 6 cm [40]. On the contrary, ElGeidie et al. found no statistical differences regarding weight loss at the groups at 2 cm and 6 cm from the pylorus [41]. Vives et al. showed that gastric emptying was faster in the group with the resection at 3 cm from the pylorus compared to that at 8 cm from the pylorus at 6 and 12 months postoperatively [14]. Unlike the previous, Fallahat et al. compared the gastric emptying in patients at 4 cm and 7 cm distance from pylorus 3 months postoperatively. The authors showed that resection at 4 cm from the pylorus were associated with delayed gastric emptying, and resection at 7 cm from the pylorus, with accelerated gastric emptying. The authors speculated that resection at 4 cm from the pylorus had as a consequence neural innervations of the antrum being abolished, contributing to slower emptying. These patients experienced nausea, vomiting, and poor appetite. On the other hand, the resection at 7 cm from the pylorus preserved the contractility of the antrum, leading to rapid gastric emptying due to the absence of redistribution process since the body and fundus were excised. These patients complained of dumping-like symptoms and had more frequent meals [42]. Further prospective randomized trials are needed to compare the motility changes and clinical symptoms in patients with the preservation or not of antrum.

There is scant information concerning the possible explanation of how these motility alterations may affect clinical symptoms or explain the underlying mechanisms of action. It seems that the technique is not standardized, and different sleeves are created. Thus, different residual gastric volumes are produced. Since now, no clear association was found between gastric volume and weight loss. Researchers suggest that the physiological changes and not the size of the sleeve are responsible as mechanisms of action. What is known is that LSG changes the profile of gut hormones. Sista et al. showed that the rapid gastric emptying was correlated with the increased production of GLP-1 in the distal bowel [16]. Burgerhart et al. associated postprandial symptoms with gastric emptying. No difference on gastric-emptying characteristics was found between patients with low or high postprandial symptoms [24]. Pomerri et al. found that patients presenting with a rapid gastroduodenal transit experienced better weight loss than patients presenting with a slow voiding rate [18]. It seems that little is known regarding the underlining mechanisms by which LSG controls appetite and food intake. Since the data are restricted to medium term, it would be interesting to see if the sleeve behaves differently in the long term and how weight regain is explained in some patients.

Bowel motility was the least studied. It seems that the food reaches the terminal ileum faster but arrives at the cecum later. Thus, the contact of the food with the area of terminal ileum is extended. Perhaps, this altered interaction of food with the gastrointestinal tract may be a key component to explain the neurohormonal changes via the stimulation of intestinal L cells producing incretions and understanding the underlining mechanisms which improve the metabolic profile of the patients.

The limitations of the review include the lack of standardization of the surgical technique, the different follow-up timings, the different measured outcomes, the small sample siz,e and the lack of available long-term data beyond four years.

Further pathophysiological studies are needed to investigate the exact correlation of the motility parameters with the clinical symptoms and gut peptide alterations and potential hormonal interactions between gastrointestinal tract and brain.

5. Conclusion

Laparoscopic sleeve gastrectomy has impacts on the gastrointestinal motility. The data remain debatable for esophageal motility. The stomach and small bowel motilities were accelerated, while the initiation of cecal filling and the ileocecal valve transit was delayed. Further pathophysiological studies are needed to investigate the exact correlation of the motility parameters with the clinical symptoms and gut peptide alterations.

https://doi.org/10.1155/2018/4135813

Conflicts of Interest

The authors declare that there is no conflict of interest regarding the publication of this article.

References

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Eleni Sioka, George Tzovaras, Konstantinos Perivoliotis (iD), Vissarion Bakalis, Eleni Zachari, Dimitrios Magouliotis, Vassiliki Tassiopoulou, Spyridon Potamianos, Andreas Kapsoritakis, Antigoni Poultsidi, Konstantinos Tepetes (iD), Constantine Chatzitheofilou, and Dimitris Zacharoulis (iD)

Department of Surgery, University Hospital of Larissa, Larissa, Greece

Correspondence should be addressed to Dimitris Zacharoulis; zachadim@yahoo.com

Received 24 December 2017; Accepted 4 March 2018; Published 5 April 2018

Academic Editor: Riccardo Casadei

Caption: Figure 1: Flow diagram.
Table 1: Studies assessing esophageal motility.

No.    Author, year of        Type of study     Patients
       publication,
       country

1      Sioka, E. et al.,      Prospective       18
       2017 [5], Greece       study

2      Mion, F. et al.,       Retrospective     53
       2016 [7], France       study

3      Rebecchi, F. et al.,   Prospective       65
       2014 [8], Italy        clinical study

4      Gorodner, V.           Prospective       14
       et al., 2015 [10],     study
       Argentina

5      Burgerhart, J. S.      Prospective       20
       et al., 2014 [11],     study
       Netherlands

6      Del Genio, J. et       Prospective       25
       al., 2014 [9],         study
       Italy

7      Kleidi, E. et al.,     Prospective       23
       2013 [6], Greece       study

8      Petersen, W. V.        Prospective               37
       et al., 2012 [12],     study                  Group I
       Germany                                    (BMI = 19-25)
                                                20 (control group)
                                                     Group II
                                                  (BMI = 42-65)
                                                   20 patients
                                                    (8 months)
                                                    Group III
                                                  (BMI = 37-57)
                                                   17 patients
                                                     (6 days)

9      Braghetto, I. et       Prospective       20
       al., 2010 [13],        study
       Chile

No.    Method of assessment/    Distance from
       follow-up                pylorus/bougie size

1      Esophageal manometry     5 cm/36F
       preoperatively and at
       median interval of
       7 months

2      High-resolution          NR/NR
       impedance manometry
       Sleeve volume and
       diameter with CT scan
       Median follow-up at
       11 months (1-50)

3      Clinically validated     6 cm/36F
       questionnaire, upper
       endoscopy, esophageal
       manometry, and 24-hour
       pH monitoring before
       and 24 months after
       LSG.

4      Esophageal manometry     6 cm/36F
       (EM) and 24 h pH
       monitoring before and
       1 year after LSG.

5      Esophageal function      6 cm/34F
       tests (high/
       resolution manometry
       (HRM), 24/h pH/
       impedance metry)
       before and 3 months
       after LSG

6      High-resolution          NR/40F
       impedance manometry
       (HRiM) and combined 24
       h pH and multichannel
       intraluminal impedance
       (MII-pH). Median
       follow-up at 13 months

7      Esophageal manometry     3-4 cm/34F
       preoperatively and 6
       weeks postoperatively

8      Esophageal manometry      2 cm/35 Ch

9      Esophageal manometry     2 cm/32F
       preoperatively, 6
       months postoperatively

No.    Main findings of the study

1      The lower esophageal sphincter (LES) total length
       decreased postoperatively (p =0 002). The resting
       and residual pressures tended to decrease
       postoperatively (mean difference [95% confidence
       interval]: -4[-8.3-0.2] mmHg, p =0 060; -.4 [-3-
       0.1] mmHg, p =0 071, resp.). The amplitude
       pressure decreased from 95.7 [+ or -] 37.3 to 69.8
       [+ or -] 26.3mmHg at the upper border of LES (p =0
       014) and tended to decrease at the distal
       esophagus from 128.5 [+ or -] 30.1 to 112.1 [+ or
       -] 35.4mmHg (p =0 06) and midesophagus from 72.7
       [+ or -] 34.5 to 49.4 [+ or -] 16.7mmHg (p =0
       006). The peristaltic normal swallow percentage
       increased from 47.2 [+ or -] 36.8 to 82.8 [+ or -
       ] 28% (p =0 003). The postoperative regurgitation
       was strongly negatively correlated with LES total
       length (Spearman's r = -0 670). When groups were
       compared according to heartburn status, the
       statistical significance was observed between the
       groups of improvement and deterioration regarding
       postoperative residual pressure and postoperative
       relaxation (p <0 002 and p <0 002, resp.). With
       regard to regurgitation status, there was
       statistically significant difference between groups
       regarding preoperative amplitude pressure at the
       upper border of LES (p <0 056). Patients developed
       decreased LES length and weakened LES pressure
       after LSG. Esophageal body peristalsis was also
       affected in terms of decreased amplitude pressure,
       especially at the upper border of LES.
       Nevertheless, body peristalsis was normalized
       postoperatively. LSG might not deteriorate
       heartburn. Regurgitation might increase following
       LSG due to shortening of LES length, particularly
       in patients with range of preoperative amplitude
       pressure at the upper border of LES of
       38.9-92.6mmHg.

2      The increased intragastric pressure occurred very
       frequently in patients after SG (77%) and was not
       associated with any upper GI symptoms, specific
       esophageal manometric profile, or impedance reflux.
       Impedance reflux episodes were also frequently
       observed after SG (52%): they were significantly
       associated with gastroesophageal reflux (GER)
       symptoms and ineffective esophageal motility. The
       sleeve volume and diameters were also significantly
       smaller in patients with impedance reflux episodes
       (p <0 01).

       SG significantly modified esophagogastric motility.
       The IIGP is frequent, not correlated to symptoms
       and should be regarded as a HRIM marker of SG. The
       impedance reflux episodes were also frequent,
       associated with GER symptoms and esophageal
       dysmotility. HRIM may thus have a clinical impact
       on the management of patients with upper GI
       symptoms after SG.

3      On the basis of preoperative 24-hour pH
       monitoring, patients were divided into group A
       (pathologic, n =28) and group B (normal, n =37).
       The symptoms improved in group A, with the
       gastroesophageal reflux disease symptom assessment
       scale score decreasing from 53.1 [+ or -] 10.5 to
       13.1 [+ or -] 3.5 (p <0 001). The DeMeester score
       and total acid exposure (% pH < 4) decreased in
       group A patients (DeMeester score from 39.5 [+ or
       -] 16.5 to 10.6 [+ or -] 5.8, p <0 001; % pH < 4
       from 10.2 [+ or -] 3.7 to 4.2 [+ or -] 2.6, p <0
       001). Real de novo GERD occurred in 5.4% of group
       B patients. No significant changes in the lower
       esophageal sphincter pressure and esophageal
       peristalsis amplitude were found in both groups.

       LSG improves symptoms and controls reflux in most
       morbidly obese patients with preoperative GERD. In
       obese patients without preoperative evidence of
       GERD, the occurrence of de novo reflux is uncommon.
       Therefore, LSG should be considered as an effective
       option for the surgical treatment of obese
       patients with GERD.

4      The lower esophageal sphincter (LES) length
       increased from 2.7 to 3.2 cm (p =NS), and LES
       pressure decreased from 17.1 to 12.4mmHg (p - 0
       05). Preoperatively, LES was normotensive in 13
       (93%) patients; postoperatively, LES was normal in
       10 (71%) (p =NS).
       After LSG, the LESP significantly decreased

5      Esophageal acid exposure significantly increased
       after sleeve gastrectomy: upright from 5.1 [+ or -
       ] 4.4 to 12.6 [+ or -] 9.8% (p =0 003), supine
       from1.4 [+ or -] 2.4 to 11 [+ or -] 15% (p =0 003)
       and total acid exposure from 4.1 [+ or -] 3.5 to
       12 [+ or -] 10.4% (p =0 004). The percentage of
       normal peristaltic contractions remained
       unchanged, but the distal contractile integral
       decreased after LSG from 2006.0 [+ or -] 1806.3 to
6      1537.4 [+ or -] 1671.8mmHg x cmx s (p =0 01). The
       lower esophageal sphincter (LES) pressure
       decreased from 18.3 [+ or -] 9.2 to 11.0 [+ or -]
       7.0mmHg (p =0 02). After LSG, the patients have
       significantly higher esophageal acid exposure,
       which may well be due to a decrease in the LES
       resting pressure following the procedure.

       Unchanged LES function, increased ineffective
       peristalsis, and incomplete bolus transit. MII-pH
       showed an increase of both acid exposure of the
       esophagus and number of nonacid reflux events in
       postprandial periods.
       Laparoscopic SG is an effective restrictive
       procedure that creates delayed esophageal emptying
       without impairing LES function. A correctly
       fashioned sleeve does not induce de novo GERD.
       Retrograde movements and increased acid exposure
       are probably due to stasis and postprandial
       regurgitation

7      The LES total and abdominal lengths increased
       significantly postoperatively, whereas the
       contraction amplitude in the lower esophagus
       decreased. There was an increase in reflux symptoms
       postoperatively (p <0 009). The approximation of
       the angle of His mostly from the operating surgeon
       resulted in an increased abdominal LES length (p
       <0 01). The presence of esophageal tissue in the
       specimen correlated with the increased total GERD
       score (p <0 05).

       LSG weakens the contraction amplitude of the lower
       esophagus, which may contribute to postoperative
       reflux deterioration. It also increases the total
       and the abdominal lengths of the LES, especially
       when the angle of His is mostly approximated.
       However, if this approximation leads to esophageal
       tissue excision, the reflux is again aggravated.
       Thus, stapling too close to the angle of His
       should be done cautiously.

8      Postoperatively, the LESP increased significantly,
       namely, from preoperative 8.4 to 21.2mmHg in group
       II and from 11 to 24mmHg (p <0 0001) in group III.
       The tubular esophageal motility profits from LSG.
       The LSG significantly increased the lower
       esophageal pressure independent of weight loss
       after LSG and may protect obese patients from
       gastroesophageal reflux.

9      Preoperative mean LESP was 14.2 [+ or -] 5.8mmHg.
       The postoperative manometry decreased in 17-20
       (85%), with a mean value of 11.2 [+ or -] 5.7mmHg
       (p =0 01). Seven of them presented LESP of <12mmHg
       and ten patients presented LESP of <6mmHg after
       the operation. Furthermore, the abdominal length
       and total length of the high pressure zone at the
       esophagogastric junction were affected. A sleeve
       gastrectomy produces an important decrease in LES
       pressure, which can, in turn, cause the appearance
       of reflux symptoms and esophagitis after the
       operation due to a partial resection of the sling
       fibers during the gastrectomy.

Table 2: Studies assessing stomach motility.

     Author, year of         Type of study    Patients
     publication,                             (N)
     country

1    Vives, M. et al.,       Prospective      60 (30 patients with
     2017 [14], Spain        randomized       the section at 3
                             study            cm and 30 patients
                                              with that at 8 cm
                                              from the pylorus

2    Berry, R. et al.,       Prospective      8 (1 patient with
     2017 [28],              study            chronic refux,
     New Zealand                              nausea, and
                                              dysmotility)

3    Sista, F. et al.,       Prospective      52
     2017 [16], Italy        study

4    Vigneshwaran, B.        Prospective      20 with T2DM and
     et al., 2016 [26],      study            with a BMI of
     India                                    30.0-35.0 kg/
                                              [m.sup.2]

5    Mans, E. et al.,        Prospective      Three groups were
     2015 [15], Spain        comparative      studied: morbidly
                             study            obese patients (n
                                              =16), morbidly obese
                                              patients who had had
                                              sleeve gastrectomy
                                              (n =8), and nonobese
                                              patients (n =16)

6    Kandeel, A. A. et       Prospective      40
     al., 2015 [29],          study
     Egypt

7    Burgerhart, J. S.       Prospective      20
     et al., 2015 [24],      study
     Netherlands

8    Melissas, J. et al.,    Prospective      21
     2013 [21], Greece       study

9    Pilone, V. et al.,      Prospective      45
     2013 [17], Italy        controlled       Group A exam before
                             randomized       (A1) and after the
                             study            operation (A2).
                                              Control group (Group
                                              B)

10   Michalsky, D. et al.,   Prospective      12
     2013 [22],              randomized
     Czech Republic          study

11   Parikh, M. et al.,      Data from an     62
     2012 [25], USA          institutional
                             review board-
                             approved
                             electronic
                             registry

12   Baumann, T. et al.,     Prospective      5
     2011 [23], Germany      pilot study

13   Pomerri, F. et al.,     Retrospective    57
     2011 [18], Italy        study

14   Shah, S. et al.,        Prospective      24 were lean
     2010 [27], India        controlled       controls (body mass
                             study            index 22.2 [+ or -]
                                              2.84 kg/m (2)), 20
                                              were severely and
                                              morbidly obese
                                              patients with T2DM
                                              who had not
                                              undergone SG (body
                                              mass index 37.73 [+
                                              or /] 5.35 kg/m
                                              (2)), and 23 were
                                              severely and
                                              morbidly obese
                                              patients with T2DM
                                              after SG.

15   Braghetto, I. et        Prospective      20 obese submitted
     al., 2009 [30],         study            to LSG 18 normal
     Chile                                    subjects

16   Bernstine H et al.,     Prospective      21
     2009 [31], Israel       study

17   Melissas, J. et al.,    Prospective      14
     2008 [20], Greece       study

18   Melissas, J. et al.,    Prospective      23
     2007 [19], Greece       study

     Method of assessment/  Bougie size/distance
     follow-up              from pylorus

1    Gastric emptying by       38F/3 cm/8 cm
     scintigraphy (T1/
     2min), gastric
     volume by CT scan
     (cc) at 6 and 12
     months

2    Laparoscopic high-              NR
     resolution (HR)
     electrical mapping
     before and after LSG

3    Gastric emptying             36F/5 cm
     scintigraphy for
     liquid and solid
     foods, before and 3
     months after LSG.

4    The gastric emptying         36F/4 cm
     times were measured
     at baseline, 3
     months, 6 months, 12
     months, and 24
     months after
     surgery.

5    Gastric and                  42F/5 cm
     gallbladder emptying

6    Tc-sulfur colloid GE        36F/3-4cm
     scintigraphy was
     performed on all
     patients submitted
     to LSG before and
     after surgery (1-4
     weeks for liquids
     and 4-6 weeks for
     solids)

7    Gastric emptying             34F/6 cm
     study with solid and
     liquid meal
     components in the
     second year after
     LSG

8    The gastric transit         34F/5 cm
     times were studied
     with a gamma camera
     before and 4 months
     postoperatively

9    Gastric emptying            34Ch/4-5cm
     scintigraphy 1 month
     preoperatively and 3
     months
     postoperatively

10   Group A antrum               42F/7cm
     resection Group B
     Antrum preservation
     Gastric emptying
     scintigraphy before
     and 3 months
     postoperatively

11   Gastroduodenal              40F/5-7cm
     transit time (antrum
     to duodenum) was
     calculated from a
     postoperative day 1
     esophagram.
     Postoperative
     esophagrams

12   MRI 1 day before LSG        32F/5-6cm
     and 6 days and 6
     months after LSG

13   The size of the              NR/4-6cm
     gastric fundus
     remaining after LSG
     and gastric voiding
     rate (fast-slow) by
     radiological upper
     gastrointestinal
     series (UGS) with a
     water-soluble
     contrast medium
     (CM).

14   Scintigraphic                   NR
     imaging with g-
     camera

15   Gastric emptying of          32F/2 cm
     liquids and solids
     was measured by
     scintigraphic
     technique 3 months
     postoperatively.

16   Gastric emptying             48F/6 cm
     scintigraphy of
     semisolids was
     performed before and
     3 months after LSG

17   Nine patients                   NR
     underwent gastric
     emptying studies,
     using radioisotopic
     technique before, 6
     months, and 24
     months after the
     operation. The
     remaining five
     patients underwent
     gastric emptying
     studies, 6 months
     and 24 months after
     the operation.
     Scintigraphic
     imaging was
     performed with a
     [gamma]-camera

18   The scintigraphic            34F/7 cm
     measurement of the
     gastric emptying of
     a solid meal
     preoperatively and 6
     months
     postoperatively.
     Gastric emptying
     studies using
     radioisotopic
     technique before and
     6 months after the operation.

     Main findings of the study

1    Gastric emptying increases the speed significantly
     in both groups but is greater in the 3 cm group (p
     <0.05).

     When dividing groups into type 2 diabetic patients
     and nondiabetic patients, the speed in nondiabetic
     patients is significantly higher for the 3 cm
     group. The residual volume increases significantly
     in both groups, and there are no differences
     between them. Gastric emptying is faster in
     patients with antrum resection.
     The distance does not influence the gastric
     emptying of diabetic patients.

2    The baseline activity showed exclusively normal
     propagation. Acutely after LSG, all patients
     developed either a distal unifocal ectopic
     pacemaker with retrograde propagation (50%) or
     bioelectrical quiescence (50%). The propagation
     velocity was abnormally rapid after LSG (12.5 [+
     or -] 0.8 versus baseline 3.8 [+ or -] 0.8mms -1 ;
     p =0 01), whereas the frequency and amplitude were
     unchanged (2.7 [+ or -] 0.3 versus 2.8 [+ or -]
     0.3 cpm, p =0 7; 1.7 [+ or -] 0.2 versus 1.6 [+ or
     -] 0.6mV, p =0 7). In the patient with chronic
     dysmotility after LSG, mapping also revealed a
     stable antral ectopic pacemaker with retrograde
     rapid propagation (12.6 [+ or -] 4.8mms -1). The
     resection of the gastric pacemaker during LSG
     acutely resulted in aberrant distal ectopic
     pacemaking or bioelectrical quiescence. Ectopic
     pacemaking can persist long after LSG, inducing
     chronic dysmotility. The clinical and therapeutic
     significance of these findings now require further
     investigation.

3    After surgery, T1-2 was significantly accelerated:
     15.2 [+ or -] 13min and 33.5 [+ or -] 18min in the
     L group and S group, respectively (p < 05). In
     both groups, GLP-1 plasma concentrations were
     increased at each blood sampling time: 2.91 [+ or
     -] 2.9 pg-mL, 3.06 [+ or -] 3.1 pg-mL, and 3.21 [+
     or -] 2.6 pg-mL at 15, 30, and 60 minutes,
     respectively, (p < 05) for the L group and 2.72 [+
     or -] 1.5 pg-mL, 2.89 [+ or -] 2.1 pg-mL, 2.93 [+
     or -] 1.8 pg-mL, and 2.95 [+ or -] 1.9 pg-mL at
     30, 60, 90, and 120 minutes, respectively, (p <
     05) for the S group. After LSG, GLP-1 and %GR
     presented a negative linear correlation (r) at
     each blood sampling time in both groups. Rapid
     gastric emptying 3 months after LSG

4    There was a significant decrease in gastric
     emptying time.
     Accelerated gastric emptying

5    The antrum area during fasting in morbidly obese
     patients was statistically significantly larger than
     that in the nonobese and sleeve gastrectomy
     groups. Gastric emptying was accelerated in the
     sleeve gastrectomy group compared with the other
     2 groups (which had very similar results).
     Gallbladder emptying was similar in the 3 groups.
     Gastric emptying was accelerated in the sleeve
     gastrectomy group compared with the other 2
     groups (which had very similar results)

6    T1-2 was significantly enhanced after LSG compared
     with the baseline (25.3 [+ or -] 4.4 versus 11.8
     [+ or -] 3.0min for liquids and 74.9 [+ or -] 7.1
     versus 28.4 [+ or -] 8.3min for solids, resp., p
     <0 001). The percentage of gastric retention in
     operated patients was significantly less than that
     at baseline for liquids at 15, 30, and 60min (33.9
     [+ or -] 5.6, 17.7 [+ or -] 3.9, and 7.5 [+ or -]
     2.8% versus 69.4 [+ or -] 10.5, 55.6 [+ or -]
     14.95, and 26.1 [+ or -] 4.7%, resp., p <0 001),
     as well as for solids at 30, 60, 90, and 120min
     (42.0 [+ or -] 11.1, 20.8 [+ or -] 6.1, 11.0 [+ or
     -] 5.9, and 3.8 [+ or -] 2.7% versus 79.9 [+ or -
     ] 8.7, 67.4 [+ or -] 12.2, 37.0 [+ or -] 10.9%,
     and 13.8 [+ or -] 4.4%, resp., p <0 001).

     The significant acceleration of GE of liquids and
     solids after LSG may have contributed to weight
     loss in the immediate postoperative period
     (4-6 weeks).

     It remains to be determined whether the weight
     loss will continue beyond that period.

7    The lag phase (solid) was 6.4 [+ or -] 4.5min in
     group I and 7.3 [+ or -] 6.3 in group II (p =0
     94); T1/2 (solid) was 40.6 [+ or -] 10.0min in
     group I and 34.4 [+ or -] 9.3 in group II (p =0
     27); the caloric emptying rate was 3.9 [+ or -]
     0.6 kcal/min in group I and 3.9 [+ or -] 1.0 kcal/
     min in group II (p =0 32).

     Patients with postprandial symptoms after LSG
     reported more symptoms during the gastric
     emptying study than did patients without
     symptoms. However, there was no difference
     between gastric emptying characteristics between
     both groups, suggesting that abnormal gastric
     emptying is not a major determinant of
     postprandial symptoms after LSG.

8    SG accelerates the gastric emptying of semisolids

9    The scintigraphic study showed a reduced half-life
     tracer (A1 versus A2: 80.4 [+ or -] 16.5min versus
     64.3 [+ or -] 22min p =0 06), without a significant
     difference. Comparing the two groups, no
     differences occurred before operation (B versus
     A1). The gastric emptying time resulted in a
     significant reduction in group A2 rather than in
     groups A1 and B.

     LSG reduces gastric emptying time
     In the antrum resection group, the average time
     T1/2 declined from 57.5 to 32.25min (p =0 016)
     and average retention %GE dropped from 20.5 to
     9.5% (p =0 073).

10   In the antrum resection group, an increase in
     gastric emptying postoperatively was noted.
     Complications such as failure of stomach
     evacuation were not observed in the RA group;
     even more radical resection of the pyloric antrum
     performed by LSG is possible without concerns of
     postoperative disorder of the stomach evacuation
     function

11   The mean gastroduodenal transit time was
     12.3 [+ or -] 19.8 s. Almost all patients (99%)
     had a transit time of less than 60 s.
     No correlation was found between gastroduodenal
     transit time and %EWL at 3, 6, or 12 months.

12   The dynamic analysis showed that antral
     propulsive peristalsis was preserved immediately
     after surgery and during follow-up, but fold speed
     increased significantly from 2.7mm/s before LSG
     to 4.4mm/s after 6 months. The sleeve itself
     remained without recognizable peristalsis in three
     patients and showed only uncoordinated or passive
     motion in two patients. Consequently, the fluid
     transport through the sleeve was markedly delayed,
     whereas the antrumshowed accelerated propulsion
     with the emptying half-time decreasing from
     16.5min preoperatively to 7.9min 6 months after
     surgery.
     The stomach is functionally divided into a sleeve
     without propulsive peristalsis and an accelerated
     antrum. Accelerated emptying seems to be caused
     by faster peristaltic folds.

13   Sleeve voiding was fast in 49 of 57 patients
     (85.96%) and slow in eight (14.03%).
     Patients showing a rapid gastroduodenal transit of
     the CM achieved a better weight loss than patients
     with a slow voiding rate.

14   The gastric emptying half-time values were also
     significantly shorter (p < 05) in the post-SG
     (52.8 [+ or -] 13.5 minutes) than in the non-SG
     (73.7 [+ or -] 29.0 minutes) and control (72.8
     [+ or -] 29.6 minutes) groups decreased gastric
     emptying half-time after SG

15   In the group of operated patients, 70% of them (n
     =14) presented accelerated emptying for liquids
     and 75% (n =15) for solids compared to 22.2% and
     27.7%, respectively, in the control group. The
     half/time of gastric emptying (T(1/2)) in patients
     submitted to SG both for liquids and solids were
     significantly more accelerated compared to the
     control group (34.9 [+ or -] 24.6 versus 13.6 [+
     or /] 11.9min for liquids and 78 [+ or -] 15.01
     versus 38.3 [+ or -] 18.77min for solids; p <0
     01). The gastric emptying for liquids expressed as
     the percentages of retention at 20, 30, and 60min
     were 30.0 [+ or -] 0.25%, 15.4 [+ or -] 0.18%, and
     5.7 [+ or -] 0.10%, respectively, in operated
     patients, significantly less than the control
     subjects (p <0 001). For solids, the percentage of
     retention at 60, 90, and 120min was 56 +/- 28%, 34
     +/- 22%, and 12 +/- 8%, respectively, for
     controls, while it was 25.3 +/- 0.20%, 9 +/-
     0.12%, and 3 +/- 0.05%, respectively, in operated
     patients (p < 001). Gastric emptying after SG is
     accelerated either for liquids as well as for
     solids in the majority of patients.

16   The mean T 1-2 raw data were 62.39 [+ or -] 19.83
     and 56.79 [+ or -] 18.72min (p =0 36, t = -0.92,
     NS) before and 3 months after LSG, respectively.
     The T 1-2 linear was 103.64 [+ or -] 9.82 and
     106.92 [+ or -] 14.55, (p =0 43, t = -0.43, NS),
     and the linear fit slope 0.48 [+ or -] 0.04 and
     0.47 [+ or -] 0.05 (p =0 48, t =0 7, NS). LSG with
     antrum preservation as performed in this series
     has no effect on gastric emptying.

17   In the nine patients who underwent gastric
     emptying studies preoperatively and 6 and 24
     months postoperatively, the T-lag phase duration
     significantly decreased, following the SG, from
     17.30 (range 15.50-20.90) min, to 12.50 (range
     9.20-18.00) min at 6 months and 12.16 (range
     10.90-20.00) min at 24 months postoperatively
     (p <0 05)

     The gastric emptying half time (T1/2) accelerated
     significantly postoperatively from 86.50 (range
     77.50-104.60) min, to 62.50 (range 46.30-80.00)
     min at 6 months and 60.80 (range 54.80-100.00)
     min at 24 months after SG (p <0 05). The
     percentage of gastric emptying (%GE) increased
     significantly postoperatively, from 52 (range
     43-58) % to 72 (range 57-97) % at 6 months and
     74 (range 45-82) % at 24 months, following SG
     (P <0 05). No differences in gastric emptying were
     observed, when values at 24 months were
     compared to those at 6 months postoperatively.
     When the whole group of 14 patients was studied,
     there were also no significant changes in T-lag,
     T1/2 and %GE between 6 and 24 months
     postoperatively.

     Constant effect of SG in the acceleration of gastric
     emptying of solids, which occurs faster, not only in
     short but also in long-term postoperatively
18   Although the meal size was drastically reduced, the
     meal frequency increased postoperatively in 12
     patients (52.2%).

     Only 5 patients (21.8%) reported occasional
     vomiting after meals following SG. The gastric
     emptying half-time (T1-2) accelerated (47.6 [+ or
     -] 23.2 versus 94.3 [+ or -] 15.4, p <0 01), and
     the T-lag phase duration decreased (9.5 [+ or -]
     2min versus 19.2 [+ or -] 2min, p <0 05)
     postoperatively. The percentage of the meal
     emptied from the stomach 90min after consumption
     increased significantly after SG (75.4 [+ or -]
     14.9% versus 49.2 [+ or -] 8.7%, p <0 01); the
     stomach empties its contents rapidly into the
     small intestine and symptoms of vomiting after
     eating (characteristic of restrictive procedures)
     are either absent or very mild

Table 3: Studies assessing bowel motility.

     Author, year of
     publication,
     country                Type of study           Patients (N)

1    Trung, V. N. et al.,   Prospective study      12
     2013 [32], Japan

2    Melissas, J. et al.,   Prospective study      21
     2013 [21], Greece

3    Shah, S. et al.,       Prospective            67
     2010 [27], India       controlled study       Controls: 24
                                                   Morbidly obese
                                                   patients with T2DM
                                                   not undergone SG: 20
                                                   Morbidly obese
                                                   patients with T2DM
                                                   after SG: 23

     Method of assessment

1    Intestinal motility
     during OGTT was
     assessed using cine
     MRI before and 3
     months
     postoperatively

2    g-Camera before and
     4 months
     postoperatively

3    Scintigraphic
     imaging

     Study main finding

1    LSG leads to accelerated intestinal motility and
     reduced intestinal transit time

2    LSG accelerates the small bowel transit of
     semisolids. In addition, it delays the initiation
     of cecal filling and T ICVt.

3    Decreased small bowel transit time after SG
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Author:Sioka, Eleni; Tzovaras, George; Perivoliotis, Konstantinos; Bakalis, Vissarion; Zachari, Eleni; Mago
Publication:Gastroenterology Research and Practice
Date:Jan 1, 2018
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