Abstract
Background and Aims
Obesity is a predisposing factor for small intestinal bacterial overgrowth (SIBO). The aim of this study was to prospectively evaluate the prevalence of SIBO as well as its clinical, biological, and nutritional aspects before and up to 24 months after a Roux-en-Y gastric bypass (RYGB) surgery.
Patients and Methods
Fifty-one patients (mean BMI 46.9 kg/m2, 66.7% women) requesting RYGB were included between 2016 and 2020. Each patient underwent a glucose breath test, a standardized interrogation on functional digestive signs, a dietary survey, a blood test, a fecalogram, and anthropometric data gathering. These investigations were carried out before surgery and at 1, 3, 6, 9, 12, 18, and 24 months after RYGB.
Results
Before surgery, we found a prevalence of 17.6% of SIBO (95% CI = [8.9%; 31.4%]). After RYGB, at the end of 24 months of follow-up, 89.5% of patients developed SIBO. Anal incontinence appeared to be very frequent after surgery, affecting 18.8% of our population 18 months after surgery. We observed positive steatorrhea after surgery with an average of 11.1 g of lipids/24 h despite a significant limitation of dietary lipids (p = 0.0282).
Conclusion
Our study corroborates data in the literature on the prevalence of SIBO in severe obesity patients. For the first time, we observed the sudden appearance of SIBO after RYGB, with a correlation between exhaled hydrogen on a breath test and lipid malabsorption on the fecalogram. As a result, these patients develop fatty diarrhea, with frequent fecal incontinence.
Graphical Abstract
Similar content being viewed by others
Data Availability
The data that support the findings of this study are available from the corresponding author, VF, upon reasonable request.
References
Pimentel M, Saad RJ, Long MD, et al. ACG clinical guideline: small intestinal bacterial overgrowth. Am J Gastroenterol. 2020;115(2):165–78.
Adike A, DiBaise JK. Small intestinal bacterial overgrowth: nutritional implications, diagnosis, and management. Gastroenterol Clin North Am. 2018;47(1):193–208.
Rana SV, Bhardwaj SB. Small intestinal bacterial overgrowth. Scand J Gastroenterol. 2008;43(9):1030–7.
Dolan RD, Baker J, Harer K, et al. Small intestinal bacterial overgrowth: clinical presentation in patients with Roux-en-Y gastric bypass. Obes Surg. 2021;31(2):564–9.
Gabrielli M, D’Angelo G, Di Rienzo T, et al. Diagnosis of small intestinal bacterial overgrowth in the clinical practice. Eur Rev Med Pharmacol Sci. 2013;17(Suppl 2):30–5.
Lakhani SV, Shah HN, Alexander K, et al. Small intestinal bacterial overgrowth and thiamine deficiency after Roux-en-Y gastric bypass surgery in obese patients. Nutr Res. 2008;28(5):293–8.
Folope V, Coëffier M, Déchelotte P. Nutritional deficiencies associated with bariatric surgery. Gastroenterol Clin Biol. 2007;31(4):369–77.
Ferolla SM, Armiliato GN, Couto CA, et al. The role of intestinal bacteria overgrowth in obesity-related nonalcoholic fatty liver disease. Nutrients. 2014;6(12):5583–99.
Novljan U, Pintar T. Small intestinal bacterial overgrowth in patients with Roux-en-Y gastric bypass and one-anastomosis gastric bypass. Obes Surg. 2022;32(12):4102–9.
Bures J, Cyrany J, Kohoutova D, et al. Small intestinal bacterial overgrowth syndrome. World J Gastroenterol. 2010;16(24):2978–90.
Mouillot T, Rhyman N, Gauthier C, et al. Study of small intestinal bacterial overgrowth in a cohort of patients with abdominal symptoms who underwent bariatric surgery. Obes Surg. 2020;30(6):2331–7.
Wijarnpreecha K, Werlang ME, Watthanasuntorn K, et al. Obesity and risk of small intestine bacterial overgrowth: a systematic review and meta-analysis. Dig Dis Sci. 2020;65(5):1414–22.
Sabate JM, Jouet P, Harnois F, et al. High prevalence of small intestinal bacterial overgrowth in patients with morbid obesity: a contributor to severe hepatic steatosis. Obes Surg. 2008;18(4):371–7.
Sabate JM, Coupaye M, Ledoux S, et al. Consequences of small intestinal bacterial overgrowth in obese patients before and after bariatric surgery. Obes Surg. 2017;27(3):599–605.
Madrid AM, Poniachik J, Quera R, et al. Small intestinal clustered contractions and bacterial overgrowth: a frequent finding in obese patients. Dig Dis Sci. 2011;56(1):155–60.
Tosetti C, Corinaldesi R, Stanghellini V, et al. Gastric emptying of solids in morbid obesity. Int J Obes Relat Metab Disord. 1996;20(3):200–5.
Massey BT, Wald A. Small intestinal bacterial overgrowth syndrome: a guide for the appropriate use of breath testing. Dig Dis Sci. 2021;66(2):338–47.
Saad RJ, Chey WD. Breath tests for gastrointestinal disease: the real deal or just a lot of hot air? Gastroenterology. 2007;133(6):1763–6.
Rezaie A, Pimentel M, Rao SS. How to test and treat small intestinal bacterial overgrowth: an evidence-based approach. Curr Gastroenterol Rep. 2016;18(2):8.
Riegler G, Esposito I. Bristol scale stool form A still valid help in medical practice and clinical research. Tech Coloproctol. 2001;5(3):163–4.
Edholm D, Svensson F, Naslund I, et al. Long-term results 11 years after primary gastric bypass in 384 patients. Surg Obes Relat Dis. 2013;9(5):708–13.
Cortez APB, Fisberg M, de Morais MB. Intestinal permeability and small intestine bacterial overgrowth in excess weight adolescents. Pediatr Obes. 2021;16(5):e12741.
Ierardi E, Losurdo G, Sorrentino C, et al. Macronutrient intakes in obese subjects with or without small intestinal bacterial overgrowth: an alimentary survey. Scand J Gastroenterol. 2016;51(3):277–80.
Quigley EMM. The spectrum of small intestinal bacterial overgrowth (SIBO). Curr Gastroenterol Rep. 2019;21(1):3.
Rezaie A, Buresi M, Lembo A, et al. Hydrogen and methane-based breath testing in gastrointestinal disorders: the North American Consensus. Am J Gastroenterol. 2017;112(5):775–84.
Lombardo L, Foti M, Ruggia O, et al. Increased incidence of small intestinal bacterial overgrowth during proton pump inhibitor therapy. Clin Gastroenterol Hepatol. 2010;8(6):504–8.
Andalib I, Shah H, Bal BS, et al. Breath hydrogen as a biomarker for glucose malabsorption after Roux-en-Y gastric bypass surgery. Dis Markers. 2015;2015:102760.
Kitaghenda FK, Hong J, Shao Y, et al. The prevalence of small intestinal bacterial overgrowth after Roux-en-Y gastric bypass (RYGB): a systematic review and meta-analysis. Obes Surg. 2024;34(1):250–7.
Kaniel O, Sherf-Dagan S, Szold A, Langer P, Khalfin B, Kessler Y, Raziel A, Sakran N, Motro Y, Goitein D, Moran-Gilad J. The effects of one anastomosis gastric bypass surgery on the Gastrointestinal Tract Nutrients 2022;14(2):304.
Schulman AR, Thompson CC. Abdominal pain in the Roux-en-Y gastric bypass patient. Am J Gastroenterol. 2018;113(2):161–6.
Decker GA, DiBaise JK, Leighton JA, et al. Nausea, bloating and abdominal pain in the Roux-en-Y gastric bypass patient: more questions than answers. Obes Surg. 2007;17(11):1529–33.
Bouchoucha M, Fysekidis M, Julia C, 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(4):337–45.
Aro P, Ronkainen J, Talley NJ, et al. Body mass index and chronic unexplained gastrointestinal symptoms: an adult endoscopic population based study. Gut. 2005;54(10):1377–83.
Zhang H, DiBaise JK, Zuccolo A, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci USA. 2009;106(7):2365–70.
Ishida RK, Faintuch J, Paula AM, et al. Microbial flora of the stomach after gastric bypass for morbid obesity. Obes Surg. 2007;17(6):752–8.
Kong LC, Tap J, Aron-Wisnewsky J, et al. Gut microbiota after gastric bypass in human obesity: increased richness and associations of bacterial genera with adipose tissue genes. Am J Clin Nutr. 2013;98(1):16–24.
Sollier C, Barsamian C, Bretault M, et al. Diagnostic and therapeutic management of post-gastric bypass chronic diarrhea: a systematic review. Obes Surg. 2020;30(3):1102–11.
Saldana Ruiz N, Kaiser AM. Fecal incontinence - challenges and solutions. World J Gastroenterol. 2017;23(1):11–24.
Bochenska K, Boller AM. Fecal incontinence: epidemiology, impact, and treatment. Clin Colon Rectal Surg. 2016;29(3):264–70.
Burgio KL, Richter HE, Clements RH, et al. Changes in urinary and fecal incontinence symptoms with weight loss surgery in morbidly obese women. Obstet Gynecol. 2007;110(5):1034–40.
Poylin V, Serrot FJ, Madoff RD, et al. Obesity and bariatric surgery: a systematic review of associations with defecatory dysfunction. Colorectal Dis. 2011;13(6):e92-103.
Mohamed F, Jeram M, Coomarasamy C, et al. Does bariatric surgery improve faecal incontinence? A systematic review and meta-analysis. Obes Surg. 2021;31(7):2942–53.
Elias K, Bekhali Z, Hedberg J, et al. Changes in bowel habits and patient-scored symptoms after Roux-en-Y gastric bypass and biliopancreatic diversion with duodenal switch. Surg Obes Relat Dis. 2018;14(2):144–9.
Jorge JM, Wexner SD. Etiology and management of fecal incontinence. Dis Colon Rectum. 1993;36(1):77–97.
DomperBardají F, Gil Rendo A, IllescasFernández-Bermejo S, et al. An assessment of bacterial overgrowth and translocation in the non-alcoholic fatty liver of patients with morbid obesity. Rev Esp Enferm Dig. 2019;111(4):294–300.
Scarpellini E, Abenavoli L, Cassano V, et al. The apparent asymmetrical relationship between small bowel bacterial overgrowth, endotoxemia, and liver steatosis and fibrosis in cirrhotic and non-cirrhotic patients: a single-center pilot study. Front Med. 2022;9:872428 (Lausanne).
Wagner NRF, Ramos MRZ, de Oliveira CL, et al. Effects of probiotics supplementation on gastrointestinal symptoms and SIBO after Roux-en-Y gastric bypass: a prospective, randomized, double-blind, placebo-controlled trial. Obes Surg. 2021;31(1):143–50.
Rao SSC, Bhagatwala J. Small intestinal bacterial overgrowth: clinical features and therapeutic management. Clin Transl Gastroenterol. 2019;10(10):e00078.
Lauritano EC, Gabrielli M, Scarpellini E, et al. Small intestinal bacterial overgrowth recurrence after antibiotic therapy. Am J Gastroenterol. 2008;103(8):2031–5.
Alcaraz F, Frey S, Iannelli A. Surgical management of small intestinal bacterial overgrowth after Roux-en-Y gastric bypass. Obes Surg. 2020;30(11):4677–8.
Azer SA, Sankararaman S. Steatorrhea. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2023.
Quigley EMM, Murray JA, Pimentel M. AGA Clinical practice update on small intestinal bacterial overgrowth: expert review. Gastroenterology. 2020;159(4):1526–32.
Odstrcil EA, Martinez JG, Santa Ana CA, et al. The contribution of malabsorption to the reduction in net energy absorption after long-limb Roux-en-Y gastric bypass. Am J Clin Nutr. 2010;92(4):704–13.
Moreland AM, Santa Ana CA, Asplin JR, et al. Steatorrhea and hyperoxaluria in severely obese patients before and after Roux-en-Y gastric bypass. Gastroenterology. 2017;152(5):1055-67.e3.
Pedron FF, de Moura DS, Calcing A, et al. Analysis of hepatic markers and lipid profile of patients submitted to gastric by-pass after 2 years - cohort retrospective. Ann Med Surg. 2022;81:104211 (Lond).
Hamdan K, Somers S, Chand M. Management of late postoperative complications of bariatric surgery. Br J Surg. 2011;98(10):1345–55.
Acknowledgements
SANTELYS association for financial support. Nutrition Team: Yoanne P., nurses, for breath testing. Véronique J. from GHAT research team and GHICL research team. Thank you Rasika for your help.
Funding
The Quitron chromatograph was paid for by a research grant from the SANTELYS association.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics Approval and Consent to Participate
All patients provided written informed consent to participate in the study, which was conducted in compliance with the tenets of the Declaration of Helsinki. The study complied with the MR001 reference methodology with regard to the French Data Protection Authority (CNIL). Informed consent was obtained from all individual participants included in the study. The trial protocol was reviewed and approved by a French National IRB (CPP Nord-Ouest I). All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Key Points
- High prevalence of bacterial overgrowth in 89.5% of patients after a RYGB
- Positive correlation between exhaled hydrogen and lipid malabsorption
- Functional disorders induced by SIBO such as diarrhea with anal incontinence
- Clinical discrepancy between symptoms and breath test positivity
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Florent, V., Dennetiere, S., Gaudrat, B. et al. Prospective Monitoring of Small Intestinal Bacterial Overgrowth After Gastric Bypass: Clinical, Biological, and Gas Chromatographic Aspects. OBES SURG 34, 947–958 (2024). https://doi.org/10.1007/s11695-024-07080-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11695-024-07080-0