Int J Gastrointest Interv 2024; 13(1): 16-22
Published online January 31, 2024 https://doi.org/10.18528/ijgii230045
Copyright © International Journal of Gastrointestinal Intervention.
Sharif Yassin1,*, Noa Sori2, Ophir Gilad1, Mati Shnell1, Relly Richer1, Nir Bar3, Yishai Ron3, Nathaniel Aviv Cohen1, Subhi Abu-Abeid4, Danit Dayan4, Shai Meron Eldar4, Shira Zelber-Sagi2, and Sigal Fishman1
1Bariatric Endoscopy Service, Department of Gastroenterology and Liver Diseases, Tel Aviv Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv-Yafo, Israel
2Department of Nutrition, Health and Behavior, Faculty of Public Health, Haifa University, Haifa, Israel
3Neurogastroenterology and Motility Service, Department of Gastroenterology and Liver Diseases, Tel Aviv Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv-Yafo, Israel
4Bariatric Surgery Unit, Division of General Surgery, Tel Aviv Medical Center, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv-Yafo, Israel
Correspondence to:*Bariatric Endoscopy Service, Department of Gastroenterology and Liver Diseases, Tel Aviv Medical Center, Sackler Faculty of Medicine, Tel Aviv University, 6 Weizman Street, Tel Aviv-Yafo 6423906, Israel.
E-mail address: shariefyas@gmail.com (S. Yassin).
This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/bync/4.0) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Background: Functional bowel disorders (FBDs), including irritable bowel syndrome (IBS), are common worldwide. Recently, increasingly many bariatric surgical procedures have been performed in response to rising obesity rates. However, data on the association between FBDs and bariatric surgery are scarce. We examined the prevalence of FBDs among candidates for bariatric surgery and prospectively investigated the association between FBDs and bariatric surgery.
Methods: This prospective cohort study included 112 bariatric surgery candidates at the Tel Aviv Medical Center from 2019 to 2020. Before and after surgery, patients completed the Rome III questionnaire. Data regarding demographics, socioeconomic status, and gastrointestinal symptoms were recorded. The rates of FBDs—IBS, functional constipation (FC), functional diarrhea (FDi), and unspecified functional bowel disorder (UFBD)—were then compared from before surgery to 6 months after the procedure.
Results: Of 112 candidates with obesity at baseline, 68 underwent surgery and completed the postoperative questionnaire. Overall, the respective prevalence rates of FBDs, IBS, FC, FDi, and UFBD were 37.5%, 2.7%, 17.9%, 5.4%, and 11.6%. Female sex and single status were particularly common among patients with FBDs, whereas divorced status was more frequent in the group without FBDs. However, these factors were not independently associated with FBD presence upon multivariable analysis. IBS was more prevalent after surgery than before (8.8% vs. 1.5%, P = 0.06), but FBDs in general did not share this trend (44.1% vs. 36.8%, P = 0.44).
Conclusion: Bariatric surgery appears to increase the risk of developing IBS, while not impacting the overall risk of FBDs.
Keywords: Bariatric surgery, Irritable bowel syndrome, Obesity, Risk factors
Functional bowel disorders (FBDs) are common conditions, collectively impacting up to one-third of the global population. They lead to diminished quality of life and work productivity, while placing a substantial burden on healthcare systems.1–4 The Rome III criteria categorize these disorders into several distinct types, including irritable bowel syndrome (IBS), functional constipation (FC), functional diarrhea (FDi), and unspecified FBD (UFBD).
The pathogenesis of FBD is diverse, encompassing abnormalities in motility, visceral sensitivity, brain-gut communication, and psychological distress.5 In recent years, changes in gut immune response, intestinal permeability, and the microbiome of the intestine and colon have been observed in some individuals with IBS, offering additional understanding of the possible pathophysiological mechanisms at play.6–10 Risk factors for IBS include young age, female sex, family history of IBS, anxiety, and smoking.11–13
Obesity affects between 12% and 19.5% of adults, with the highest prevalence found in the sixth and seventh decades of life for women and men, respectively.14,15 Among individuals with obesity, the prevalence of IBS ranges from 11.6% to 24%.16 The role of obesity as a risk factor for FBDs remains unclear.17 One investigation reported that up to 30% of those with morbid obesity have IBS.18 However, a recent comprehensive review of the literature presented mixed findings regarding whether obesity represents a risk factor for IBS onset.16
The escalating rates of obesity around the world have been paralleled by an increase in the number of bariatric surgical procedures performed. Data from the global registry of the International Federation for the Surgery of Obesity and Metabolic Disorders indicate that laparoscopic sleeve gastrectomy (LSG) is the most common, accounting for 46% of bariatric procedures. This is followed by Roux-en-Y gastric bypass (RYGB) (38.2%), mini-gastric bypass (MGB) (7.6%), and gastric banding (5%).19 An expanding body of evidence supports bariatric surgery as the most effective method for achieving substantial weight loss and mitigating comorbidities associated with obesity.20,21 Additionally, improvements in various dimensions of health-related quality of life have been reported.22
Several studies have explored the link between bariatric surgical procedures and the emergence of FBDs, yielding mixed results. IBS has been reported to impact 24% to 29.1% of patients following bariatric surgery, with higher rates among women than men.23–25 Furthermore, abdominal bloating and pain are frequently reported after LSG and RYGB, affecting 33.8% and 54.4% of patients, respectively.23,26,27 In one study, only 18.5% of patients who experienced chronic abdominal pain after surgery had reported pain prior to the procedure.23 However, most of these studies were not specifically aimed at investigating the relationship between bariatric surgery and FBD onset, resulting in limited and inconsistent data.
In the present study, our goal was to quantify the prevalence of FBDs at baseline and to characterize risk factors for FBDs among obese candidates for bariatric surgery. Additionally, we aimed to examine the relationship between bariatric surgery and the emergence of FBDs over a 6-month follow-up period. Of note, due to the impact of bariatric surgery on the continuity and function of the upper gastrointestinal (UGI) tract, we intentionally excluded functional UGI disorders from our investigation.
This prospective cohort study enrolled adult patients (aged over 18 years) with obesity who were candidates for bariatric surgery, following their attendance at the Obesity and Pre-Surgery Clinic of the Tel Aviv Medical Center. The inclusion criteria were the ability to complete the study questionnaire and consent to participate in the study. Patients were excluded if they had a known diagnosis of inflammatory bowel disease, previous bariatric surgery, early or late surgical complications necessitating additional surgical or endoscopic interventions or hospitalization, or an objective explanation for their symptoms upon evaluation, such as anastomotic marginal ulcer or dumping syndrome. Eligible candidates were asked to complete the Rome III questionnaire at baseline during a preoperative clinic visit and again via a telephone survey 6 months after surgery.28 This questionnaire was used to assess the presence of FBDs along with additional demographic, medical, and socioeconomic parameters.29 Based on the criteria for IBS diagnosis, responses to the questionnaire were used to classify FBDs into four subgroups: IBS, FC, FDi, and UFBD.30 We omitted questions pertaining to functional UGI disorders, such as functional dyspepsia, as these are commonly observed after bariatric surgery and may related to the surgical procedure itself.27 The use of the Rome III questionnaire was authorized by the Rome Foundation. Additional data were gathered during the preoperative clinic visit and confirmed through the review of electronic medical records. The bariatric procedures included in the study were LSG, RYGB, and MGB.
This study was approved by the Tel Aviv Medical Center review board (protocol no. 0748-18) and conformed to the principles of the Declaration of Helsinki. Written informed consent was obtained from all participants.
IBS is characterized by recurrent abdominal pain or discomfort occurring at least 3 days per month over the prior 3 months. This discomfort is associated with two or more of the following symptoms: alleviation of pain upon defecation, the onset of symptoms coinciding with a change in stool frequency, and the onset of symptoms coinciding with a change in stool form. FC is defined by difficult, infrequent, or incomplete bowel movements, while FDi involves the recurrent passage of loose or watery stools; both of these conditions occur without associated pain or discomfort. UFBD is diagnosed when patients experience functional abdominal symptoms but do not meet the criteria for IBS, FDi, or FC.30
Differences in continuous variables were assessed using the Student
A total of 112 consecutive bariatric surgery candidates at the Tel-Aviv Medical Center bariatric clinic completed the initial questionnaire. The prospective analysis encompassed 68 patients who underwent surgery and submitted the postoperative questionnaire. Regarding the type of procedure, 42 patients underwent MGB, 5 underwent RYGB, and 21 underwent LSG. The remaining participants were either lost to follow-up or did not proceed with surgery for various reasons (Fig. 1).
The cohort comprised 112 patients (64.3% female; mean age, 41.1 ± 13.0 years), with a mean body mass index (BMI) of 42.5 ± 5.3 kg/m2. Of these, 42 (37.5%) were found to have FBDs. FC was the most frequently observed disorder, while IBS was the least common (Table 1). Relative to patients without FBDs, higher proportions of patients with FBDs were female (76.2% vs. 22.9%,
Table 1 . FBDs, Demographics, and Medical Characteristics among Candidates for Bariatric Surgery.
Parameter | Value ( |
---|---|
IBS | 3 (2.7) |
FC | 20 (17.9) |
FDi | 6 (5.4) |
UFBD | 13 (11.6) |
Total FBDs | 42 (37.5) |
Age (yr) | 41.1 ± 13.0 |
Sex, female | 72 (64.3) |
Born in Israel | 84 (75.0) |
Family status | |
Married | 59 (52.7) |
Divorced | 13 (11.6) |
Widowed | 2 (1.8) |
Single | 38 (33.9) |
Education | |
High school | 64 (57.1) |
More than high school | 48 (42.9) |
BMI (kg/m2) | 42.5 ± 5.3 |
Dyslipidemia | 3 (2.7) |
Hypertension | 39 (34.8) |
Ischemic heart disease | 5 (4.5) |
Diabetes mellitus 2 | 22 (19.6) |
NAFLD | 63 (56.3) |
Colorectal cancer | 3 (2.7) |
Past surgery | 7 (6.3) |
Medications | |
PPIs | 14 (12.5) |
Iron supplements | 16 (14.3) |
Aspirin | 11 (9.8) |
Insulin | 8 (7.1) |
Anti-diabetic medications | 14 (12.5) |
NSAIDs | 8 (7.1) |
Oral contraceptives | 6 (5.4) |
Values are presented as mean ± standard deviation or n (%).
FBDs, functional bowel disorders; IBS, irritable bowel syndrome; FC, functional constipation; FDi, functional diarrhea; UFBD, unspecified functional bowel disorder; BMI, body mass index; NAFLD, non-alcoholic fatty liver disease; PPIs, proton pump inhibitors; NSAIDs, non-steroidal anti-inflammatory drugs.
A total of 68 patients underwent surgery and completed the postoperative questionnaire. Among the 61 patients for whom BMI data were available, the average postoperative BMI was 28.7 ± 4.9 kg/m2, with a mean reduction in BMI of 13.6 ± 4.3 kg/m2. An increase was observed in the frequency of IBS following surgery (from 1.5% to 8.8%,
Table 2 . Demographic and Medical Characteristics of Patients with Obesity Who Underwent Bariatric Surgery, Comparing Those with and without Postoperative FBD.
Parameter | All patients who underwent surgery ( | With postoperative FBD ( | Without postoperative FBD ( | |
---|---|---|---|---|
Age (yr) | 41.8 ± 12.6 | 41.5 ± 12.6 | 41.95 ± 12.7 | 0.82 |
Sex, female | 46 (67.6) | 19 (63.3) | 27 (71.1) | 0.49 |
Born in Israel | 48 (70.6) | 21 (70.0) | 27 (71.1) | 0.96 |
Family status | ||||
Married | 39 (57.4) | 17 (56.7) | 22 (57.9) | 0.92 |
Divorced | 7 (10.3) | 5 (16.7) | 2 (5.3) | 0.12 |
Widowed | 2 (2.9) | 0 (0.0) | 2 (5.3) | 0.20 |
Single | 20 (29.4) | 8 (26.7) | 12 (31.6) | 0.69 |
Education | ||||
High school | 35 (51.5) | 15 (50.0) | 20 (52.6) | 0.83 |
More than high school | 33 (48.5) | 15 (50.0) | 18 (47.4) | 0.83 |
BMI (kg/m2)* | 42.49 ± 4.6 | 43.90 ± 5.2 | 41.37 ± 3.7 | 0.47 |
Hypertension | 25 (36.8) | 11 (36.7) | 14 (36.8) | 0.99 |
Ischemic heart disease | 3 (4.4) | 2 (6.7) | 1 (2.6) | 0.42 |
Diabetes mellitus 2 | 15 (22.1) | 9 (30.0) | 6 (15.8) | 0.16 |
NAFLD | 43 (63.2) | 17 (56.7) | 26 (68.4) | 0.32 |
Prior abdominal surgery | 5 (7.4) | 5 (16.7) | 0 (0.0) | 0.01 |
Medications | ||||
PPI | 7 (10.3) | 4 (13.3) | 3 (7.9) | 0.70 |
Iron supplements | 11 (16.2) | 6 (20.0) | 5 (13.2) | 0.15 |
Aspirin | 6 (8.8) | 3 (10.0) | 3 (7.9) | 0.76 |
Insulin | 6 (8.8) | 4 (13.3) | 2 (5.3) | 0.14 |
Anti-diabetic medications | 9 (13.2) | 4 (13.3) | 5 (13.2) | 0.13 |
NSAIDs | 5 (7.4) | 4 (13.3) | 1 (2.6) | 0.16 |
Type of surgery | ||||
MGB | 42 (61.8) | 17 (56.7) | 25 (65.8) | 0.11 |
REYGB | 5 (7.4) | 2 (6.7) | 3 (7.9) | 0.90 |
LSG | 21 (30.9) | 11 (36.7) | 10 (26.3) | 0.16 |
Values are presented as mean ± standard deviation or n (%).
FBDs, functional bowel disorders; BMI, body mass index; NAFLD, non-alcoholic fatty liver disease; PPI, proton pump inhibitor; NSAIDs, non-steroidal anti-inflammatory drugs; MGB, mini-gastric bypass; RYGB, Roux-En-Y gastric bypass; LSG, laparoscopic sleeve gastrectomy.
*Postoperative BMI was retrieved and computed for 61 patients.
Among the patients who underwent surgery, 37% developed new FBD postoperatively (Fig. 3). Non-alcoholic fatty liver disease (NAFLD) was less prevalent in the cohort that developed new FBD than among patients who did not (31.3% vs. 77.8%,
In this prospective study, the respective prevalence rates of FBDs and IBS among obese candidates for bariatric surgery were 37.5% and 2.7%, respectively. Furthermore, our findings suggest that bariatric surgery may pose a risk for the development of IBS, but not for other FBDs. Interestingly, NAFLD was found to be inversely associated with the emergence of new FBDs following surgery. As mentioned earlier, we did not analyze UGI functional disorders, as their symptoms can arise from the surgical procedures performed.
Our cohort, consisting of 112 candidates for bariatric surgery, had a mean BMI of 41.1 ± 13.0 kg/m2. The majority were female (64.3%), with over half being married (52.7%) and having a high school education (57.1%). Additionally, we observed high rates of obesity-related comorbidities, including hypertension (34.8%), NAFLD (56.3%), and T2DM (19.6%). The profile of our group resembles those described in other large studies of bariatric surgery candidates.19,31–35 This similarity may facilitate the comparison of our results with findings from other series investigating FBDs.
Intriguingly, among our series of bariatric surgery candidates, risk factors for FBDs included female sex and single status. In contrast, a history of divorce was significantly more common among the patients with obesity who did not have FBDs. Although female sex is a recognized risk factor for FBDs,11 the influence of marital status on the emergence of these disorders remains unclear, with the literature presenting mixed findings.18,36 Other established risk factors for the development of FBDs, such as younger age and higher educational attainment, were not associated with the presence of FBDs in our cohort.12,37,38
Few studies have explored the relationship between obesity and the broad range of FBDs. Two retrospective studies have identified an association between FDi and increased BMI. In these studies, the rate of FDi was greater than in our series (20% vs. 5.4%).39,40 Two key factors may account for this discrepancy. First, the abdominal symptoms in those studies were based on patient reports, as opposed to our study, which utilized validated Rome III questionnaires. Second, the mean BMI of our cohort was higher than that of these studies, complicating the comparison of outcomes. FC and UFBD have been reported to occur in as many as 60% and 30% of overweight adults, respectively—rates considerably higher than those found in our study.41,42 However, other research has demonstrated no link between FC, UFBD, and obesity.39,40 These conflicting findings could stem from variations in study methodology and the retrospective nature of the research. Separately, Schneck et al18 conducted a prospective study among morbidly obese candidates for bariatric surgery and reported a sharply higher prevalence of IBS compared to our findings (30% vs. 2.7%). Although the study design and patient populations were similar in both studies, the differences in IBS prevalence might be partially due to geographical, cultural, and temporal factors.
The pathophysiology of postoperative abdominal symptoms may be attributed to alterations in the anatomy of the digestive tract, hormonal fluctuations, dumping syndromes, and the volume of consumed nutrients, all of which promote changes to the microbiome.43 Other exacerbating factors could include changes in intestinal permeability, gut-immune function, gut motility, visceral sensitivity, brain-gut interactions, and psychosocial status.44 Consequently, it is logical to assume that FBDs would be more common among individuals who have undergone bariatric surgery.
In our cohort, the rate of IBS after surgery (8.8%) was higher than that before (1.5%,
Our findings unexpectedly revealed an inverse relationship between NAFLD and the emergence of IBS following surgery. This stands in contrast to a cross-sectional study involving 100 consecutive patients with IBS, which reported a high NAFLD prevalence of 74%. In that study, moderate to severe NAFLD and metabolic syndrome were identified as independent predictors of moderate to severe IBS.48 However, the study was not conducted prospectively. The link between NAFLD and FBDs is currently being explored, with factors such as innate immunity, the gut microbiota, and intestinal motility suspected to play a role in their common pathogenesis.49 Intriguingly, our research identified T2DM as a risk factor for the persistence of IBS after bariatric surgery. Prior research has shown that approximately 70% of individuals with diabetes experience at least one gastrointestinal symptom.50 Furthermore, the prevalence of prediabetes has been found to be higher in patients with IBS compared to matched controls.51 Glucose control and IBS are closely linked. Hyperglycemia can disrupt gastric and small intestinal motility, potentially through inhibition of vagal-cholinergic neural pathways or by altering serum osmolality and gastrointestinal peptide secretion.52 Conversely, disorders of gastrointestinal motility, such as IBS, can lead to postprandial glycemic dysregulation.53
Our study had several limitations. First, the assessment of symptoms is inherently subjective and can be influenced by bias. To mitigate this issue, we employed a validated questionnaire that included recurrent symptom-specific questions. Second, candidates for bariatric surgery may have underreported their symptoms due to concerns that such disclosures could impact their eligibility for the procedure. To address this, the interviewer reassured participants regarding these concerns prior to completion of the questionnaire. Third, the research was carried out at a single center, raising the possibility of selection bias. Nonetheless, our center is a tertiary hospital, and the patients referred to our obesity and pre-surgery clinic come from a wide range of sociodemographic and clinical backgrounds, which is reflective of the broader population in Israel. Furthermore, the characteristics of our study group are consistent with those reported in other large series, as previously discussed. Fourth, the sample size of our study was relatively small, which may not have provided sufficient power to detect differences in the rates of IBS and FBDs before and after surgery. Fifth, the follow-up period was limited to 6 months post-surgery, which restricted our ability to explore long-term outcomes. The major strengths of this study lie in its prospective nature, accurate methodology, and contribution of new insights to the existing body of knowledge regarding the emergence of FBDs following bariatric surgery.
In conclusion, our findings suggest that bariatric surgery may elevate the risk of developing IBS, although it does not appear to increase the risk of other FBDs. Further research is required to clarify this relationship and to identify risk factors for FBDs following bariatric surgery, with the aim of potentially mitigating these risks before the procedure.
Supplementary data is available at https://doi.org/10.18528/ijgii230045.
None.
The datasets generated and analyzed in this study are not publicly available due to privacy and ethical considerations. However, they can be obtained from the corresponding author upon reasonable request.
No potential conflict of interest relevant to this article was reported.
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