Abstract
Background
With the increasing prevalence of obesity, non-alcoholic fatty liver disease (NAFLD) has become a major cause of liver diseases. Small intestinal bacterial overgrowth (SIBO) could be related to NAFLD. Our aim was to determine the prevalence of SIBO and its relationship with liver lesions in morbidly obese patients.
Methods
A glucose hydrogen (H2) breath test (positive if fasting breath H2 concentration > 20 ppm and/or an increase of > 10 ppm over baseline within the first 2 h) was performed in obese patients referred for bariatric surgery (body mass index [BMI] > 40 kg/m2 or > 35 in association with comorbidities) and in healthy non-obese subjects. In obese patients, a surgical liver biopsy was performed.
Results
One hundred and forty-six patients (129 women, age [mean±SE]: 40.7 ± 11.4 years) were prospectively included in the study. The mean BMI was 46.1±6.4 kg/m2. A liver biopsy was available in 137 patients and a breath test in 136. The frequency of positive breath tests was higher in obese patients (24/136, 17.1%) than in healthy subjects (1/40, 2.5%; P=0.031). In the univariate analysis, SIBO was not associated with clinical variables, but tended to be associated with more frequent severe hepatic steatosis (26.3 vs. 10.3%, P=0.127), whereas the frequency of sinusoidal or portal fibrosis, lobular necrosis and non-alcoholic steatohepatitis (NASH) were not different. In the multivariate analysis, SIBO (P=0.005) and the presence of a metabolic syndrome (P=0.006) were independent factors of severe hepatic steatosis.
Conclusion
In morbidly obese patients, bacterial overgrowth prevalence is higher than in healthy subjects and is associated with severe hepatic steatosis.
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Abbreviations
- BMI:
-
Body mass index
- NAFLD:
-
Non-alcoholic fatty liver disease
- NASH:
-
Non-alcoholic steatohepatitis
- SIBO:
-
Small intestinal bacterial overgrowth
References
Ogden CL, Carroll MD, Curtin LR, et al. Prevalence of overweight and obesity in the United States, 1999–2004. JAMA. 2006;295:1549–55.
James OFW, Day CP. Non-alcoholic steatohepatitis (NASH): a disease of emerging identity and importance. J Hepatol. 1998;29:495–501.
Fassio E, Alvarez E, Domínguez N, et al. Natural history of nonalcoholic steatohepatitis: a longitudinal study of repeat liver biopsies. Hepatology. 2004;40:820–6.
Bugianesi E, Leone N, Vanni E, et al. Expanding the natural history of nonalcoholic steatohepatitis: from cryptogenic cirrhosis to hepatocellular carcinoma. Gastroenterology. 2002;123:134–40.
Harnois F, Msika S, Sabaté JM, et al. Prevalence and predictive factors of non-alcoholic steatohepatitis (NASH) in morbidly obese patients undergoing bariatric surgery. Obes Surg. 2006;16:183–8.
Machado M, Marques-Vidal P, Cortez-Pinto H. Hepatic histology in obese patients undergoing bariatric surgery. J Hepatol. 2006;45:600–6.
Imagawa S, Yamaguchi Y, Ogawa K, et al. Interleukin-6 and tumor necrosis factor-alpha in patients with obstructive sleep apnea-hypopnea syndrome. Respiration. 2004;71:24–9.
Bondar GF, Pisesky W. Complications of small intestinal short-circuiting for obesity. Arch Surg. 1967;94:707–16.
Maxwell JG, Richards RC, Albo D Jr. Fatty degeneration of the liver after intestinal bypass for obesity. Am J Surg. 1968;116:648–52.
Nazim M, Stamp G, Hodgson HJF. Non-alcoholic steatohepatitis associated with small intestinal diverticulosis and bacterial overgrowth. Hepatogastroenterology. 1989;36:349–51.
Wigg AJ, Roberts-Thomson IC, Dymock RB, et al. The role of small intestinal bacterial overgrowth, intestinal permeability, endotoxaemia, and tumour necrosis factor alpha in the pathogenesis of non-alcoholic steatohepatitis. Gut. 2001;48:206–11.
Sajjad A, Mottershead M, Syn WK, et al. Ciprofloxacin suppresses bacterial overgrowth, increases fasting insulin but does not correct low acylated ghrelin concentration in non-alcoholic steatohepatitis. Aliment Pharmacol Ther. 2005;22:291–9.
Chitturi S, Abeygunasekera S, Farrell GC, et al. NASH and insulin resistance: insulin hypersecretion and specific association with the insulin resistance syndrome. Hepatology. 2002;35:373–9.
[No authors listed] Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care. 1997;20:1183–97.
Executive summary of the third report of the National Cholesterol Education Program (NCEP) Expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III). JAMA. 2001;285:2486–97.
Kerlin P, Wong L. Breath hydrogen testing in bacterial overgrowth of the small intestine. Gastroenterology. 1988;95:982–8.
Flourie B, Turk J, Lemann M, et al. Breath hydrogen in bacterial overgrowth. Gastroenterology. 1989;96:1225.
Attar A, Flourie B, Rambaud JC, et al. Antibiotic efficacy in small intestinal bacterial overgrowth-related chronic diarrhea: a crossover, randomized trial. Gastroenterology. 1999;117:794–7.
Chang C-S, Chen G-H, Lien H-C, et al. Small intestine dysmotility and bacterial overgrowth in cirrhotic patients with spontaneous bacterial peritonitis. Hepatology. 1998;28:1187–90.
Lupascu A, Gabrielli M, Lauritano EC, et al. Hydrogen glucose breath test to detect small intestinal bacterial overgrowth: a prevalence case-control study in irritable bowel syndrome. Aliment Pharmacol Ther. 2005;22:1157–60.
Brunt EM, Janney CG, Di Bisceglie AM, et al. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol. 1999;94:2467–74.
Bauer TM, Schwacha H, Steinbrückner B, et al. Diagnosis of small intestinal bacterial overgrowth in patients with cirrhosis of the liver: poor performance of the glucose breath hydrogen test. J Hepatol. 2000;33:382–6.
Casafont MF, de las Heras Castaño G, Martín Ramos L, et al. Small bowel bacterial overgrowth in patients with alcoholic cirrhosis. Dig Dis Sci. 1996;41:552–6.
Yang C-Y, Chang C-S, Chen G-H. Small-intestinal bacterial overgrowth in patients with liver cirrhosis, diagnosed with glucose H2 or CH4 breath tests. Scand J Gastroenterol. 1998;33:867–71.
Mitsui T, Shimaoka K, Goto Y, et al. Small bowel bacterial overgrowth is not seen in healthy adults but is in disabled older adults. Hepatogastroenterology. 2006;53:82–5.
Parlesak A, Klein B, Schecher K, et al. Prevalence of small bowel bacterial overgrowth and its association with nutrition intake in nonhospitalized older adults. J Am Geriatr Soc. 2003;51:768–73.
Elphick DA, Chew TS, Higham SE, et al. Small bowel bacterial overgrowth in symptomatic older people: can it be diagnosed earlier? Gerontology. 2005;51:396–401.
Suter M, Dorta G, Giusti V, et al. Gastro-esophageal reflux and esophageal motility disorders in morbidly obese patients. Obes Surg. 2004;14:959–66.
Merrouche M, Sabaté JM, Jouet P, et al. Gastro-esophageal reflux and esophageal motility disorders in morbidly obese patients before and after bariatric surgery. Obes Surg. 2007;17:894–900.
Quigley EM, Quera R. Small intestinal bacterial overgrowth: roles of antibiotics, prebiotics, and probiotics. Gastroenterology. 2006;130:S78–90.
Nieuwenhuijs VB, Verheem A, van Duijvenbode-Beumer H, et al. The role of interdigestive small bowel motility in the regulation of gut microflora, bacterial overgrowth, and bacterial translocation in rats. Ann Surg. 1998;228:188–93.
Pieramico O, Malfertheiner P, Nelson DK, et al. Interdigestive gastroduodenal motility and cycling of putative regulatory hormones in severe obesity. Scand J Gastroenterol. 1992;27:538–44.
Larson SP, Bowers SP, Palekar NA, et al. Histopathologic variability between the right and left lobes of the liver in morbidly obese patients undergoing Roux-en-Y Bypass. Clin Gastroenterol Hepatol. 2007;5:1329–32.
Merriman RB, Ferrell LD, Patti MG, et al. Correlation of paired liver biopsies in morbidly obese patients with suspected nonalcoholic fatty liver disease. Hepatology. 2006;44:874–80.
Mathurin P, Gonzalez F, Kerdraon O, et al. The evolution of severe steatosis after bariatric surgery is related to insulin resistance. Gastroenterology. 2006;130:1617–24.
Cheal KL, Abbasi F, Lamendola C, et al. Relationship to insulin resistance of the adult treatment panel III diagnostic criteria for identification of the metabolic syndrome. Diabetes. 2004;53:1195–200.
Drenick EJ, Fisler J, Johnson D. Hepatic steatosis after intestinal bypass—prevention and reversal by metronidazole, irrespective of protein-calorie malnutrition. Gastroenterology. 1982;82:535–48.
Lichtman SN, Sartor RB, Keku J, et al. Hepatic inflammation in rats with experimental small intestinal bacterial overgrowth. Gastroenterology. 1990;98:414–23.
Lichtman SN, Keku J, Schwab JH, et al. Hepatic injury associated with small bowel bacterial overgrowth in rats is prevented by metronidazole and tetracycline. Gastroenterology. 1991;100:513–9.
Lichtman SN, Okoruwa EE, Keku J, et al. Degradation of endogenous bacterial cell wall polymers by the muralytic enzyme mutanolysin prevents hepatobiliary injury in genetically susceptible rats with experimental intestinal bacterial overgrowth. J Clin Invest. 1992;90:1313–22.
Cani PD, Amar J, Iglesias MA, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56:1761–72.
Cani PD, Neyrinck AM, Fava F, et al. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia. 2007;50:2374–83.
Yang SQ, Lin HZ, Lane MD, et al. Obesity increases sensitivity to endotoxin liver injury: implications for the pathogenesis of steatohepatitis. Proc Natl Acad Sci U S A. 1997;94:2557–62.
Li Z, Yang S, Lin H, et al. Probiotics and antibodies to TNF inhibit inflammatory activity and improve nonalcoholic fatty liver disease. Hepatology. 2003;37:343–50.
Day CP, James OF. Steatohepatitis: a tale of two “hits”? Gastroenterology. 1998;114:842–5.
Berson A, De Beco V, Letteron P, et al. Steatohepatitis-inducing drugs cause mitochondrial dysfunction and lipid peroxidation in rat hepatocytes. Gastroenterology. 1998;114:764–74.
Browning JD, Horton JD. Molecular mediators of hepatic steatosis and liver injury. J Clin Invest. 2004;114:147–52.
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Sabaté, JM., Jouët, 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 18, 371–377 (2008). https://doi.org/10.1007/s11695-007-9398-2
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DOI: https://doi.org/10.1007/s11695-007-9398-2