Decreased Prevalence of Nonspecific Functional Bowel Disorders and Increased Constipation in Patients after Sleeve Gastrectomy or Gastric Banding

Abstract

Aim:

To examine the effect of laparoscopic adjustable gastric banding (LAGB) and sleeve gastrectomy (SG) on the prevalence of functional gastrointestinal disorders (FGIDs) as defined by the Rome III criteria.

Methods:

All patients fulfilled the French consensus inclusion criteria for bariatric surgery (BS). Patients eligible for BS, but did not undergo surgery, constituted the control group (n = 124), whereas patients that underwent LAGB (n = 93) and SG (n = 70) formed the two BS groups.

Results:

The control group was younger (p = 0.041). Dysphagia (22.1% vs. 9.7%; p = 0.005) and constipation (45.4% vs. 28.2%; p < 0.003) were significantly increased in operated patients; however, these factors were not significantly different between the LAGB and SG groups. In the presence of functional defecation disorder, the odds of constipation in the LAGB and SG groups were increased threefold. In operated patients, the number of nonspecific abdominal symptoms was significantly decreased from that in the control patients (16.6% vs. 33.1%; p < 0.001); this factor was not significantly different between the LAGB and SG groups.

Conclusions:

No differences were found between the LAGB and SG groups regarding the postoperative prevalence of FGIDs. Improved screening for FGIDs before BS may prevent increased prevalence of dysphagia and constipation.

Introduction

The prevalence of obesity has nearly doubled since 1980, with the percentage of American adults classified as overweight or obese (body mass index [BMI] ≥25 kg/m²) after the age of 60 years estimated to be 74.6% for men and 69.1% for women. From 2004 to 2012, the number of obese women further increased from 31.5% to 38.1%.¹ Sleeve gastrectomy (SG) and laparoscopic adjustable gastric banding (LAGB) are the most commonly performed weight-reduction surgical interventions.^2–4 During the weight loss period after surgery, significant improvements in comorbidities are observed; patients undergo major changes in hormonal levels depending on the type of surgery,⁵ and adaptive modifications are detected with reprogramming of the intestinal glucose metabolism.⁶ These events can potentially alter the course of symptoms or diseases already present in the intestinal tract. Studies thus far have demonstrated three major associations between obesity and digestive symptoms. These include the association of obesity with upper abdominal symptoms,⁷ with fecal incontinence and pelvic floor disorders,⁸ and with multiple functional disorders.⁹ In a previous study, we showed that functional gastrointestinal disorders (FGIDs) were highly prevalent in morbidly obese patients before bariatric surgery (BS); FGIDs were present in 89% of the subjects, with an average of 2.5 functional digestive symptoms per subject.¹⁰

The primary objective of the present study was to examine the effect of SG and LAGB on the prevalence of FGIDs. The secondary objective was to determine whether weight loss had an impact on FGID prevalence.

Patients and Methods

Patient characteristics

All patients completed a demographics questionnaire, which included age, weight, and height.

The control group (n = 124) was composed of morbidly obese patients eligible for BS who had attended seminars at the tertiary University Hospital of Avicenne Bariatric Surgery Program between October 2009 and January 2011 for surgical weight loss. All patients were asked to participate in the study. Part of the data for this group has been previously published.¹⁰

The second group (n = 163) was composed of patients that had either LABG (n = 93) or SG (n = 70) BS who were contacted by mail between January 2012 and December 2013. All patients received questionnaires that were mailed with a stamped and addressed return envelope, at least 6 months after BS. Patients belonged either to the control or BS groups, and no patient belonged to both groups. In previous studies, we had observed that only a small percentage of patients participated in the follow-up; thus, all operated patients were contacted to ensure the enrollment of a sufficient number of participants. As LABG and SG were restrictive procedures affecting the stomach and were the most widely performed surgical approaches during the study period, only those patients undergoing LABG or SG were contacted. Only eight patients had Roux-en-Y gastric bypass as a second operation and these were excluded from further analysis due to lack of statistical power. In all SG-operated patients, a 34-French bougie was used for SG calibration.

Inclusion criteria

All patients who agreed to participate in this study fulfilled the French consensus inclusion criteria for BS: age <65 years, BMI >35 kg/m² with at least one comorbidity (e.g., hypertension, dyslipidemia, severe rheumatologic disease, diabetes, sleep apnea) or BMI >40 kg/m², and at least 6 months of follow-up by a nutritionist or a registered dietitian.¹¹

Exclusion criteria

Patients with neurologic diseases such as stroke, spinal trauma, and multiple sclerosis were excluded from the study. Patients with endocrine diseases such as hypercalcemia or thyroid disorders or autoimmune diseases such as scleroderma, rheumatoid polyarthritis, or connective tissue disorders were excluded. Patients using nonsteroidal anti-inflammatory drugs more than once per month were also excluded. Diabetic patients were referred to diabetes specialists (M.F., R.C.) if their diabetes was poorly controlled. Medications such as calcium channel inhibitors were assessed at the initial patient evaluation, and a new antihypertensive treatment from a different pharmacological class was prescribed. Of these patients, those that showed symptomatic improvement were excluded from the study and it was considered a side effect of antihypertensive treatment, whereas those with persistent symptoms were included in the study. In addition, all patients underwent morphological evaluation by endoscopy or radiology. Patients with anorectal symptoms and symptomatic hemorrhoids were excluded, whereas patients with nonsymptomatic hemorrhoids, a very common finding, were included; however, they were not tracked in our database. Patients with anal fistulas and abscesses were also excluded. Gastric fibroscopy was performed in all patients with upper gastrointestinal disorders, and patients with Helicobacter pylori (HP) infection were excluded. Patients with a history of drug or alcohol addiction were also excluded from the study. The same investigator independently confirmed the validity of initial FGIDs during the medical visits for all patients.¹²

Clinical questionnaire

A standard clinical questionnaire based on diagnostic questions for FGIDs was administered at the office (95% acceptance rate) to the control patients and at home to the BS patients (33% acceptance rate); the answers were not reviewed. The diagnosis of FGIDs was based on the Rome III criteria for esophageal,¹³ gastroduodenal,¹⁴ intestinal,¹⁵ and abdominal pain,¹⁶ as well as for anorectal functional disorders.¹⁷ A two-question case-finding instrument for depression was used to determine the presence of depressive symptoms.¹⁸ The ideal BMI was considered as ≤25 kg/m², and the percentage of excess BMI loss (%EBL) was calculated according to the recommendations for reporting weight loss.¹⁹ Stool consistence was evaluated using the Bristol stool scale through a questionnaire.

Clinical evaluation

During evaluation for BS, all patients had a 12-lead electrocardiogram as well as a stress test if needed and polygraphy or polysomnography to detect potential obstructive sleep apnea–hypopnea syndrome. Gastroesophageal endoscopy was conducted, and patients with any abnormalities, with or without the presence of HP infection, were excluded from the study. An interview with a clinical dietician or a nutritionist was conducted to detect any eating disorders, and an interview with a psychiatrist was included for the detection of severe psychiatric illness. Each patient was evaluated at a multidisciplinary team meeting during which the approval of the surgeon, the endocrinologist, the anesthetist, the dietician, and the psychiatrist was needed for the patient to proceed to BS.

Dietary advice

Pre- and postsurgery dietary advice on the number and duration of meals and the return to a solid and normal diet postoperatively was given to each patient. Soda drinks, even those without calories, were prohibited, and patients were encouraged to have 1.4–1.9 liters of daily water intake.

Data analyses

Symptoms were expressed as percentages in all analyses (%). Data from the questionnaires were analyzed for each symptom; the four major symptom categories, namely esophageal, gastroduodenal, intestinal, and anorectal symptoms, were also coded as dichotomous variables. Analysis of variance was used for continuous variables, and the Bonferroni correction was used to adjust for the multitude of tests using SPSS version 20.0 (Chicago, IL). The χ² test was used for categorical values. Logistic regression was performed with the preoperative group as the reference group; all operated patients and SG and LAGB groups were compared to the reference group to calculate odds ratios (ORs). The LAGB group was used as a reference group for comparisons with the SG group to determine differences between the two surgical approaches. Results were first considered statistically significant at two-tailed α = 0.05. The Bonferroni adjustment was applied to correct for the number of primary outcomes tested, and the significance levels were set at less than 0.003 for logistic regression. Univariate linear regression was used to study the effect of weight loss in the surgery group.

Results

Population description

Patient characteristics are shown in Table 1. Morbidly obese patients eligible for BS were the control group (n = 124), whereas the operated group (n = 163) was composed of 93 patients that underwent LAGB and 70 patients that underwent SG. The majority of patients were female, but the gender distribution was not significantly different among the three groups (p = 0.106). The control group was slightly younger than the surgery group (p = 0.041). The ethnic distribution was significantly different among groups (p < 0.001); the majority of participants were Caucasian (62.2%, p < 0.001).

Table 1.

Demographics

	Total (n = 287)	Control group (n = 124)	LAGB (n = 93)	SG (n = 70)
Sex ratio total (% of females)	257 (89.5)	113 (40.5)	86 (29)	58 (20)
Age (years) (M ± SD)	42.7 ± 13.3	40.4 ± 11.5	44.6 ± 12.2	44.1 ± 16.7^*
Preoperative BMI (kg/m²) (M ± SD)	43.2 ± 7.2	43.6 ± 6.0	42.1 ± 6.7	43.6 ± 8.9
Depressive symptoms (% total)	38.7	19.2	12.9	6.6
Ethnic origin (% total)
Caucasian	133 (62.2)	34 (15.9)	55 (26)	44 (21)^†
North Africa	34 (15.9)	18 (8.4)	9 (4)	7 (3)
Central Africa and Caribbean	47 (21.9)	36 (16.8)	6 (3)	5 (2)
Stool consistency (% total)
Floating	24 (8.3)	1 (0.3)	13 (5)	10 (4)^†
Oily	6 (2.0)	1 (0.3)	3 (1)	2 (1)
Abdominal pain (% total)	62 (21.6)	23 (8.0)	18 (6)	21 (7)
%Excess of BMI loss (M ± SD)	48.5 ± 24.8		41.5 ± 24.5	61.0 ± 20.2^**
Follow-up (days) (M ± SD)	383 ± 285		450 ± 323	268 ± 151^**

ANOVA for three groups:^*p < 0.05, ^**p < 0.001, ^†χ², p < 0.001.

BMI, body mass index; LAGB, laparoscopic adjustable gastric banding; SD, standard deviation; SG, sleeve gastrectomy.

Depressive symptoms were more frequent in the control group and had a tendency to decrease in all operated patients (OR, 0.66; 95% confidence interval [CI], 0.41–1.06; p = 0.085), particularly in the SG group (OR, 0.47; 95% CI, 0.25–0.88; p = 0.018). The BMI, prevalence of abdominal pain, and frequency of oily stools were similar among the three groups before surgery. Stool appearance changed significantly for operated patients, who reported frequently floating stools (OR, 20.2; 95% CI, 2.7–151.8; p < 0.001).

The SG group had a higher %EBL than the LAGB group (61.0% vs. 41.5%, respectively; p < 0.001), and the mean follow-up period was longer for the LAGB than the SG group (p < 0.001). The LAGB group had a mean follow-up of 15.0 ± 10.8 months and the SG group 8.9 ± 5.0 months (Table 1).

Prevalence of FGIDs: the role of ethnic origin and the presence of depressive symptoms

The prevalence of FGIDs was similar among the three ethnic groups, and ethnic origin was not associated with differences in %EBL (p = 0.270). In the univariate analysis, there was no significant association between depressive symptoms and FGIDs. Specifically, there were no statistically significant differences between the control and operated groups and between the three ethnic groups. The presence of depressive symptoms was not associated with differences in %EBL (49.2% ± 27.1% vs. 48.0% ± 23.5%, respectively; p = 0.833).

Number of reported symptoms

The percentage of patients reporting FGIDs did not significantly differ between the control and operated groups (87% vs. 83%, respectively; p = 0.28). Symptoms were also coded as dichotomous variables for each part of the intestinal tract and analyzed. The number of reported esophageal (0.6 ± 0.9, p = 0.135), gastroduodenal (0.6 ± 0.8, p = 0.263), intestinal (1.5 ± 1.5, p = 0.98), and anorectal symptoms (0.5 ± 0.7, p = 0.50) was similar in the control and operated patients.

Change in FGIDs following BS

Functional esophageal symptoms

Functional esophageal symptoms were reported more frequently by the operated patients than the control patients (Table 2, 42.9% vs. 33.1%, respectively, OR, 1.52; 95% CI, 0.94–2.5; p = 0.09); however, a statistically significant difference was observed only between the SG and control groups (OR, 1.91; 95% CI, 1.05–3.48; p = 0.03), not between the LAGB and control groups (OR, 1.28; 95% CI, 0.73–2.24; p = 0.39). There was no difference between the SG and LAGB groups in this regard (p = 0.209).

Table 2.

Frequencies of Functional Gastrointestinal Disorders in Control Obese Patients and after Bariatric Surgery

		Operated patients
	Morbid obesity group, N = 124 (% of total)	Total, N = 163 (% of total)	LAGB, N = 93 (% of total)	SG, N = 70 (% of total)
Functional esophageal disorders
Heartburn	28 (22.6)	30 (18.4)	13 (14)	17 (24)
Chest pain of presumed esophageal origin	13 (10.5)	27 (16.6)	16 (17)	11 (16)
Dysphagia	12 (9.7)	36 (22.1)^*	18 (19)^*	18 (26)^**
Globus	9 (7.3)	16 (9.8)	7 (8)	9 (13)
All functional esophageal disorders	41 (33.1)	70 (42.9)	36 (39)	34 (49)^*
Functional gastroduodenal disorders
Functional dyspepsia	12 (9.7)	21 (12.9)	13 (14)	9 (13)
Postprandial distress syndrome	13 (10.5)	22 (13.5)	11 (12)	11 (16)
Epigastric pain syndrome	8 (6.5)	10 (6.1)	3 (3)	7 (10)
Belching disorders	16 (12.9)	30 (18.4)	17 (18)	13 (19)
All functional gastroduodenal disorders	39 (31.5)	64 (39.3)	34 (37)	30 (43)
Functional bowel disorders
Irritable bowel syndrome	22 (17.7)	33 (20.2)	18 (19)	15 (21)
Functional bloating	1 (0.8)	0 (0.0)	0 (0)	0 (0)
Functional constipation	35 (28.2)	74 (45.4)^**	41 (44)^*	33 (47)^**
Functional diarrhea	24 (19.4)	35 (21.5)	22 (24)	13 (19)
Unspecified functional bowel disorder	41 (33.1)	27 (16.6)^**	14 (15)^**	13 (19)^*
All functional bowel disorders	100 (80.6)	123 (75.5)	68 (73)	55 (79)
Functional anorectal disorders
Functional fecal incontinence	5 (4.0)	2 (1.2)	1 (1)	1 (1)
Functional defecation disorder (dyschezia)	37 (29.8)	55 (33.7)	32 (34)	23 (33)
Functional anorectal pain
Proctalgia fugax	8 (6.5)	10 (6.1)	3 (3)	7 (10)
Levator ani syndrome	3 (2.4)	2 (1.2)	2 (2)	0 (0)
Nonspecific anorectal disorders	0 (0.0)	5 (3.1)	3 (3)	2 (3)
All functional anorectal disorders	48 (38.7)	63 (38.7)	36 (39)	27 (39)

p < 0.05, versus morbid obese group; ^**p < 0.003, versus morbid obese group.

Dysphagia was the main symptom described after surgery and was reported in 22.1% of the operated group (OR, 2.65; 95% CI, 1.31–5.33; p = 0.005). A statistically significant difference regarding the presence of this symptom was observed only between the SG and control groups (OR, 3.23; 95% CI, 1.45–7.20; p < 0.001). The odds of dysphagia were also increased in the LAGB group (OR, 2.24; 95% CI, 1.02–4.72; p = 0.04); however, there was no difference in this parameter between the SG and LAGB groups (p = 0.33).

Functional gastroduodenal symptoms

Postoperatively, functional gastroduodenal symptoms were present in 39.3% of the operated patients and in 31.5% of the control group; however, this increase was not statistically significant (p = 0.17). The prevalence of dyspeptic symptoms and aerophagia remained constant in all groups, and there was no difference in prevalence between the SG and LAGB groups (p = 0.41).

Functional intestinal disorders

Postoperatively, functional intestinal disorders were reported by 81% of the control patients. The prevalence of symptoms did not significantly differ between the LAGB and SG groups (73.1% vs. 78.6% respectively; p = 0.69). The presence of functional constipation was increased for all operated patients (45.4% vs. 28.2% for the control group; OR, 2.11; 95% CI, 1.28–3.48; p < 0.003); however, there was no difference in this parameter between the LABG and SG groups (p = 0.699). The prevalence of nonspecific abdominal symptoms was decreased in the operated patients from that in the control group (16.6% vs. 33.1%, respectively; OR, 0.40; 95% CI, 0.23–0.7; p < 0.001); the prevalence of these symptoms was similar between the LAGB and SG groups (15.1% vs. 18.6%, respectively; p = 0.559).

Abdominal pain was reported by 8% of patients in the control group and by 13.6% of patients in the operated group (p = 0.274).

Functional anorectal symptoms

Functional anorectal symptoms were reported by 38.7% of the operated and 38.7% of the control group; these percentages were not significantly different (p = 0.99). Nonspecific anorectal symptoms were reported only after BS (3.1%, p = 0.07), and there were no significant differences in this parameter between the LAGB and SG groups (3% vs. 3%, respectively, p = 0.99).

The presence of functional defecation disorders was associated with a 10-fold increase in constipation risk in the control group (Fig. 1). In the presence of functional defecation disorder in the operated group, the odds of constipation were increased threefold, and this effect was more pronounced in the SG group (OR, 14.3; 95% CI, 4.9–41.2; p < 0.003).

FIG. 1.

Increased odds of constipation in the presence of functional defecation disorder. The presence of functional defecation disorder led to a threefold increase in the odds of laparoscopic adjustable gastric band and sleeve gastrectomy.

Prevalence of FGIDs and %EBL

To determine the effect of weight loss on the prevalence of FGIDs, we compared the %EBL for the three symptoms that showed a significant change after BS. The presence of dysphagia was associated with greater %EBL (59.9% ± 20% vs. 45.6% ± 25%, p = 0.028), whereas the presence of functional constipation (51.7% ± 27% vs. 45.7% ± 22%, p = 0.255) and nonspecific functional intestinal disorders had similar %EBL values (48.0% ± 22% vs. 48.6% ± 25%, p = 0.937).

Discussion

The present study confirmed the high prevalence of FGIDs in obese patients and demonstrated the persistence of these disorders after BS (83% of our cohort); their number also remained constant. There was no difference in the prevalence of FGIDs among the SG and LAGB groups. The types of complaints changed after BS, and there was a postoperative increase in upper symptoms, that is, dysphagia, as has been previously reported. These restrictive procedures also had an impact in the prevalence of one FGID; the incidence of constipation was increased postoperatively, whereas the incidence of nonspecific intestinal disorders decreased after surgery.

The increase in postoperative dysphagia, particularly in the SG group, confirmed previous findings in SG²⁰ and LAGB²¹ patients. Esophageal motor dysfunction in LAGB has been well studied; it is experienced at a frequency of 14–72% and can present as esophageal dilatation.²² Given that the prevalence of esophageal motility disorders is increased in morbidly obese patients,²³ these findings underline the need for improved screening of patients to identify those that may have preexisting dysphagia, particularly before restrictive procedures.

In the present study, functional dysphagia was present in 9.7% of morbidly obese patients in the control group; its prevalence was probably underestimated as these patients were treated for weight problems, and esophageal dysmotility was not the chief complaint. The use of LAGB doubled the odds of dysphagia: the prevalence of these symptoms was 19.4%. The main mechanisms underlying esophageal dysmotility and dilatation are impairment of the lower esophageal sphincter (LES) relaxation and increases in the LES pressure.²⁴ Acid exposure can worsen or appear de novo, while additional mechanisms involve increased duration of esophageal contractions, increased LES high-pressure zone length, and increased percentage of defective esophageal propagations²⁵

SG also increased the prevalence of dysphagia, as previously reported; however, this phenomenon is less well studied. An increased gastroesophageal pressure gradient may have a “band-like” effect on esophageal motor function. A significant decrease in LES pressure after SG due to the partial division of sling fibers to the cardia has been reported,²⁶ whereas others have reported increased LES pressure.²⁷ Technical approaches in SG, including approximation of the angle, may weaken the amplitude of contraction.²⁸ In addition, the portion of the antrum resected and the bougie used to calibrate the sleeve may also have an impact by virtue of increased intraluminal pressure.²⁹ The formation of a tube-like structure with removal of most of the stomach decreases the gastric reservoir and may cause upper gastrointestinal discomfort due to misinterpretation of the feeling provoked by decreased distensibility of the neo-stomach.

Postoperative increase of the prevalence of constipation has already been reported in LAGB patients.³⁰ Constipation was mentioned in the Clinical Practice Guidelines for the Perioperative Nutritional, Metabolic, and Nonsurgical Support of the Bariatric Surgery Patient for an optimal care and follow-up.³¹Another important finding was the absence of any difference in the prevalence of constipation between the two surgical approaches. To the best of our knowledge, this is the first report of the increased frequency of functional constipation after SG. In this study, all patients received dietary advice for fiber intake, adequate water intake, and for low-calorie meals both in the pre- and postoperative period. We propose that the restrictive part of the surgery may be reducing food intake and fecal volume, leading to slower colonic transit with subsequent increase in the probability of constipation; this notion has already been studied in animal models.³² Furthermore, the change in stool consistency (Table 1), with an increase in floating stools, depends on differences in gas rather than fat content and seems to indirectly confirm our hypothesis.³³

The colonic response to food starts with entry of food to the stomach, which stimulates postprandial colonic movements. The presence of functional defecation disorder that increased the odds of reporting functional constipation by threefold suggested that preexisting pelvic floor abnormalities may have a major impact on the appearance or aggravation of existing constipation, which should be assessed before surgery.³⁴ Difficult defecation could result from dyssynergic defecation and/or inadequate defecation propulsion. Anorectal manometry and dynamic defecography can be helpful, but are not used systematically before BS.

The percentage of patients in both the control and operated group that declared FGIDs remained stable, so did the number of the reported symptoms after surgery. However, BS had a protective effect on the prevalence of nonspecific functional symptoms. Further clinical and physiological studies are needed to determine the mechanisms underlying the exact relationship between these changes.

Depressive symptoms improved in patients that underwent SG; however, the %EBL was not different in these patients from that in the LAGB patients, and depressive symptoms did not appear to be affected by the surgical outcome. Dysphagia was associated with better %EBL, potentially due to an associated decrease in food intake, which is known to be improved by restrictive bariatric surgeries. The %EBL was not associated with either constipation or nonspecific functional bowel disorders.

One of the limitations of the present study was the recruitment design. Patients were not recruited before the BS for the operated group; thus, we were obliged to use a separate control group. Another weak point was the low questionnaire response rate from operated patients due to the difficulty with efficient follow-up in these patients. This cohort was predominantly female, and there were ethnic differences with fewer non-Caucasian participants. These factors could present a selection bias by recruiting patients with higher education levels, although the educational level was not recorded, or result in better results for weight loss.

One of the strong points of this study was the systematic evaluation of all FGIDs in a large cohort with two of the most widely used bariatric procedures. The use of a systematic approach with a standardized questionnaire for the Rome III criteria permitted the comparison among groups with a threshold for statistical significance that was adjusted for the number of statistical tests.

In conclusion, patients with morbid obesity had a high prevalence of postoperative FGIDs. The presence of at least two symptoms, dysphagia and constipation, should be screened during preoperative evaluation. FGIDs can be detected with a simple questionnaire during initial patient workup, and, if present, specific tests such as esophageal or anorectal manometry can modify the choice of surgery. For example, in the presence of dysphagia, a gastric bypass procedure may be preferable to LAGB or SG. In the presence of constipation, the treatment should include at least 1.5 L of water per day, dietary fibers, and, if constipation persists, the biofeedback therapy can improve anorectal dyssynergic defecation. While the prevalence of nonspecific intestinal disorders was decreased in patients with LAGB or SG, the presence of dysphagia was associated with increased weight loss. These associations underline the need for improved screening of patients for FGIDs before BS and for intensified provision of adequate care and nutritional advice after surgery.

Footnotes

Acknowledgment

The authors would like to thank Vivi Fissekidou for editing this article.

Author Contributions

M.F. performed data analysis, participated in the interpretation of data, wrote the article, and approved its final version to be published. M.B. performed the research, contributed to the design of the study, revised the article for its content, and approved its final version. H.B. participated in the selection of the patients and revised the article for its content. G.R. participated in the selection of the patients and revised the article for its content. R.C. participated in the selection of the patients and revised the article for its content. R.B. participated in the design of the study, revised the article for content, and approved its final version. J.M.C. participated in the selection of the patients, contributed in the design of the study, revised the article's content, and gave final approval of the version to be published

Author Disclosure Statement

No competing financial interests exist.

References

Ogden

, Carroll

, Kit

, Flegal

. Prevalence of childhood and adult obesity in the United States, 2011–2012. JAMA, 2014; 311:806–814.

Schauer

, Bhatt

, Kirwan

, Wolski

, Brethauer

, Navaneethan

, et al. Bariatric surgery versus intensive medical therapy for diabetes—3-year outcomes. N Engl J Med, 2014; 370:2002–2013.

Chang

S-H

, Stoll

, Song

, Varela

, Eagon

, Colditz

. The effectiveness and risks of bariatric surgery: an updated systematic review and meta-analysis, 2003–2012. JAMA Surg, 2014; 149:275–287.

Ward

, Prachand

. Surgical treatment of obesity. Gastrointest Endosc, 2009; 70:985–990.

Lindqvist

, Spégel

, Ekelund

, Mulder

, Groop

, Hedenbro

, et al. Effects of ingestion routes on hormonal and metabolic profiles in gastric-bypassed humans. J Clin Endocrinol Metabol, 2013; 98:E856–E861.

Saeidi

, Meoli

, Nestoridi

, Gupta

, Kvas

, Kucharczyk

, et al. Reprogramming of intestinal glucose metabolism and glycemic control in rats after gastric bypass. Science, 2013; 341:406–410.

El-Serag

, Graham

, Satia

, Rabeneck

. Obesity is an independent risk factor for GERD symptoms and erosive esophagitis. Am J Gastroenterol, 2005; 100:1243–1250.

Cremonini

, Camilleri

, Clark

, Beebe

, Locke

, Zinsmeister

, et al. Associations among binge eating behavior patterns and gastrointestinal symptoms: a population-based study. Int J Obes Relat Metab Disord, 2009; 33:342–353.

Gunnbjornsdottir

, Omenaas

, Gislason

, Norrman

, Olin

, Jogi

, et al. Obesity and nocturnal gastro-oesophageal reflux are related to onset of asthma and respiratory symptoms. Eur Res J, 2004; 24:116–121.

10.

Fysekidis

, Bouchoucha

, Bihan

, Reach

, Benamouzig

, Catheline

J-M

. Prevalence and co-occurrence of upper and lower functional gastrointestinal symptoms in patients eligible for bariatric surgery. Obes Surg, 2011; 22:403–410.

11.

Haute Autorité de santé. Obésité: prise en charge chirurgicale chez l'adulte. (Recommandations pour la pratique clinique, janvier 2009.). Saint Denis. Haute Autorité de santé, 2009.

12.

Bouchoucha

, Fysekidis

, Julia

, Airinei

, Catheline

, Cohen

, et al. Body mass index association with functional gastrointestinal disorders: differences between genders. Results from a study in a tertiary center. J Gastroenterol, 2016; 51:337–345.

13.

Galmiche

, Clouse

, Bálint

, Cook

, Kahrilas

, Paterson

, et al. Functional esophageal disorders. Gastroenterology, 2006; 130:1459–1465.

14.

Tack

, Talley

, Camilleri

, Holtmann

, Hu

, Malagelada

J-R

, et al. Functional gastroduodenal disorders. Gastroenterology, 2006; 130:1466–1479.

15.

Longstreth

, Thompson

, Chey

, Houghton

, Mearin

, Spiller

. Functional bowel disorders. Gastroenterology, 2006; 130:1480–1491.

16.

Clouse

, Mayer

, Aziz

, Drossman

, Dumitrascu

, Mönnikes

, et al. Functional abdominal pain syndrome. Gastroenterology, 2006; 130:1492–1497.

17.

Bharucha

, Wald

, Enck

, Rao

. Functional anorectal disorders. Gastroenterology, 2006; 130:1510–1518.

18.

Whooley

, Avins

, Miranda

, Browner

. Case-finding instruments for depression. J Gen Intern Med, 1997; 12:439–445.

19.

Deitel

, Greenstein

. Recommendations for reporting weight loss. Obes Surg, 2003; 13:159–160.

20.

Carabotti

, Silecchia

, Greco

, Leonetti

, Piretta

, Rengo

, et al. Impact of laparoscopic sleeve gastrectomy on upper gastrointestinal symptoms. Obes Surg, 2013; 23:1551–1557.

21.

de Jong

, van Ramshorst

, Timmer

, Gooszen

, Smout

. Effect of laparoscopic gastric banding on esophageal motility. Obes Surg, 2006; 16:52–58.

22.

Klaus

, Gruber

, Wetscher

, Nehoda

, Aigner

, Peer

, et al. Prevalent esophageal body motility disorders underlie aggravation of GERD symptoms in morbidly obese patients following adjustable gastric banding. Arch Surg, 2006; 141:247–251.

23.

Quiroga

, Cuenca-Abente

, Flum

, Dellinger

, Oelschlager

. Impaired esophageal function in morbidly obese patients with gastroesophageal reflux disease: evaluation with multichannel intraluminal impedance. Surg Endosc, 2006; 20:739–743.

24.

Weiss

, Nehoda

, Labeck

, Peer-Kuehberger

, Oberwalder

, Aigner

, et al. Adjustable gastric and esophagogastric banding: a randomized clinical trial. Obes Surg, 2002; 12:573–578.

25.

Ardila-Hani

, Soffer

. Review article: the impact of bariatric surgery on gastrointestinal motility. Aliment Pharmacol Ther, 2011; 34:825–831.

26.

Braghetto

, Lanzarini

, Korn

, Valladares

, Molina

, Henriquez

. Manometric changes of the lower esophageal sphincter after sleeve gastrectomy in obese patients. Obes Surg, 2009; 20:357–362.

27.

Petersen

, Schneider

. Functional importance of laparoscopic sleeve gastrectomy for the lower esophageal sphincter in patients with morbid obesity. Obes Surg, 2012; 22:949.

28.

Kleidi

, Theodorou

, Albanopoulos

, Menenakos

, Karvelis

, Papailiou

, et al. The effect of laparoscopic sleeve gastrectomy on the antireflux mechanism: can it be minimized?. Surg Endosc, 2013; 27:4625–4630.

29.

Parikh

, Issa

, McCrillis

, Saunders

, Ude-Welcome

, Gagner

. Surgical strategies that may decrease leak after laparoscopic sleeve gastrectomy. Ann Surg, 2013; 257:231–237.

30.

Potoczna

, Harfmann

, Steffen

, Briggs

, Bieri

, Horber

. Bowel habits after bariatric surgery. Obes Surg, 2008; 18:1287–1296.

31.

Mechanick

, Youdim

, Jones

, Garvey

, Hurley

, McMahon

, et al. Clinical practice guidelines for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient-2013 update: cosponsored by American Association of Clinical Endocrinologists, The Obesity Society, and American Society for Metabolic & Bariatric Surgery. Obesity, 2013; 21(S1):S1–S27.

32.

Wilson-Pérez

, Chambers

, Sandoval

, Stefater

, Woods

, Benoit

, et al. The effect of vertical sleeve gastrectomy on food choice in rats. Int J Obes Relat Metab Disord, 2012; 37:288–295.

33.

Levitt

, Duane

. Floating stools—flatus versus fat. N Engl J Med, 1972; 286:973–975.

34.

Wasserberg

, Haney

, Petrone

, Ritter

, Emami

, Rosca

, et al. Morbid obesity adversely impacts pelvic floor function in females seeking attention for weight loss surgery. Dis Colon Rectum, 2007; 50:2096–2103.