Association of small intestinal bacterial overgrowth and non-alcoholic fatty liver disease in children

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Yu.M. Stepanov
N.Yu. Zavhorodnia
O.Yu. Lukianenko
E.V. Zygalo
V.B. Yagmur


Background. Non-alcoholic fatty liver disease (NAFLD) is a leading etiological factor of chronic liver diseases in children in industrialized countries. The high prevalence of small intestinal bacterial overgrowth (SIBO) is common in patients with NAFLD. Therefore, the purpose of our work is to study the impact of SIBO on the structural and functional parameters of the liver in obese/overweight children. Materials and methods. We examined 73 children aged 6 to 17 years, mean age of patients was (11.41 ± 2.68) years. Depending on the presence of overweight/obesity and the results of glucose hydrogen breath test (HBT), patients were divided into 2 groups: group 1 — 30 overweight/obese persons with SIBO, group 2 — 28 overweight/obese children without SIBO. The control group consisted of 15 apparently healthy children with normal weight and without SIBO. The presence of liver steatosis was established by means of transient elastography with controlled attenuation parameter. Additionally, we performed lactose HBT and a biochemical blood test with biochemical hepatogram, determination of lipid and carbohydrate parameters. Results. It was found that 70 % of children in group 1 had NAFLD, compared to 32 % in group 2. Also, erythrocyte sedimentation rate was higher in group 1 than in groups 2 and 3 (p < 0.05). Patients of group 1 had 1.5 times higher levels of triglycerides and very low-density lipoproteins. There was a tendency towards higher values of insulin and homeostatic model assessment in group 1 compared to group 2. Lactose malabsorption was diagnosed in 17 (56.7 %) children with NAFLD, lactose-dependent SIBO — in 15 (50.0 %). Among obese patients without NAFLD, lactose malabsorption was found in 10 (35.7 %) cases, and lactose-dependent SIBO — in 9 (32.1 %). Thus, in children with NAFLD, lactose malabsorption was detected 1.6 times more frequently than in children without NAFLD. Conclusions. It has been found that NAFLD is a risk factor for SIBO development. SIBO was associated with low-grade inflammation and adverse metabolic profile. The high frequency of lactose malabsorption and lactose-dependent SIBO among children with NAFLD was demonstrated.

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Stepanov, Y., Zavhorodnia, N., Lukianenko, O., Zygalo, E., & Yagmur, V. (2019). Association of small intestinal bacterial overgrowth and non-alcoholic fatty liver disease in children. GASTROENTEROLOGY, 53(4), 266–272.
Original Researches


Babak OYa, Lapshyna KA, Chernyak AM. Complex treatment of non-alcoholic fatty liver disease: experience of the use of hepatoprotectors. Modern Gastroenterology. 2018;(100):32-36. (in Ukrainian).

Ministry of Нealth of Ukraine. Order on January 29, 2013 № 59. On Adoption of unified Clinical Protocols for Medical Care for Children with Digestive Diseases. Available from: Accessed: January 29, 2013. (in Ukrainian).

Belei O, Olariu L, Dobrescu A, Marcovici T, Marginean O. The relationship between non-alcoholic fatty liver disease and small intestinal bacterial overgrowth among overweight and obese children and adolescents. J Pediatr Endocrinol Metab. 2017 Oct 26;30(11):1161-1168. doi: 10.1515/jpem-2017-0252.

Clemente MG, Mandato C, Poeta M, Vajro P. Pediatric non-alcoholic fatty liver disease: Recent solutions, unresolved issues, and future research directions. World J Gastroenterol. 2016 Sep 28;22(36):8078-93. doi: 10.3748/wjg.v22.i36.8078.

De Campos Mazo DF, Mattar R, Stefano JT, et al. Hypolactasia is associated with insulin resistance in nonalcoholic steatohepatitis. World J Hepatol. 2016 Aug 28;8(24):1019-27. doi: 10.4254/wjh.v8.i24.1019.

Cani PD, Amar J, Iglesias MA, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007 Jul;56(7):1761-72. doi: 10.2337/db06-1491.

Caricilli AM, Saad MJ. The role of gut microbiota on insulin resistance. Nutrients. 2013 Mar 12;5(3):829-51. doi: 10.3390/nu5030829. 

Clemente MG, Mandato C, Poeta M, Vajro P. Pediatric non-alcoholic fatty liver disease: Recent solutions, unresolved issues, and future research directions. World J Gastroenterol. 2016 Sep 28;22(36):8078-93. doi: 10.3748/wjg.v22.i36.8078.

Fialho A, Fialho A, Thota P, McCullough AJ, Shen B. Small Intestinal Bacterial Overgrowth Is Associated with Non-Alcoholic Fatty Liver Disease. J Gastrointestin Liver Dis. 2016 Jun;25(2):159-65. doi: 10.15403/jgld.2014.1121.252.iwg.

Ferolla SM, Armiliato GN, Couto CA, Ferrari TC. The role of intestinal bacteria overgrowth in obesity-related nonalcoholic fatty liver disease. Nutrients. 2014 Dec 3;6(12):5583-99. doi: 10.3390/nu6125583.

Gasbarrini A, Corazza GR, Gasbarrini G, et al. Methodology and indications of H2-breath testing in gastrointestinal diseases: the Rome Consensus Conference. Aliment Pharmacol Ther. 2009 Mar 30;29 Suppl 1:1-49. doi: 10.1111/j.1365-2036.2009.03951.x.

Lamri A, Poli A, Emery N, et al. The lactase persistence genotype is associated with body mass index and dairy consumption in the D.E.S.I.R. Study. Metabolism. 2013 Sep;62(9):1323-9. doi: 10.1016/j.metabol.2013.04.006.

De Onis M. World Health Organization Reference Curves. In: Frelut ML, editor. The ECOG’s eBook on Child and Adolescent Obesity. Available from:

Nier A, Engstler AJ, Maier IB, Bergheim I. Markers of intestinal permeability are already altered in early stages of non-alcoholic fatty liver disease: Studies in children. PLoS One. 2017 Sep 7;12(9):e0183282. doi: 10.1371/journal.pone.0183282.

Paolella G, Mandato C, Pierri L, Poeta M, Di Stasi M, Vajro P. Gut-liver axis and probiotics: Their role in non-alcoholic fatty liver disease. World J Gastroenterol. 2014 Nov 14;20(42):15518-31. doi: 10.3748/wjg.v20.i42.15518.

Perla FM, Prelati M, Lavorato M, Visicchio D, Anania C. The Role of Lipid and Lipoprotein Metabolism in Non-Alcoholic Fatty Liver Disease. Children (Basel). 2017 Jun 6;4(6). pii: E46. doi: 10.3390/children4060046.

International Diabetes Federation (IDF). IDF consensus definition of the metabolc syndrome in children and adolescents. Brussels, Belgium: IDF; 2007. 23 p.

Shanab AA, Scully P, Crosbie O, et al. Small intestinal bacterial overgrowth in nonalcoholic steatohepatitis: association with toll-like receptor 4 expression and plasma levels of interleukin 8. Dig Dis Sci. 2011 May;56(5):1524-34. doi: 10.1007/s10620-010-1447-3.

Troisi J, Pierri L, Landolfi A, et al. Urinary Metabolomics in Pediatric Obesity and NAFLD Identifies Metabolic Pathways/Metabolites Related to Dietary Habits and Gut-Liver Axis Perturbations. Nutrients. 2017 May 11;9(5). pii: E485. doi: 10.3390/nu9050485.

Wigg AJ, Roberts-Thomson IC, Dymock RB, McCarthy PJ, Grose RH, Cummins AG. The role of small intestinal bacterial overgrowth, intestinal permeability, endotoxaemia, and tumour necrosis factor alpha in the pathogenesis of non-alcoholic steatohepatitis. Gut. 2001 Feb;48(2):206-11. doi: 10.1136/gut.48.2.206.

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