Intestinal microbiota in obese children with non-alcoholic fatty liver disease depending on the gallbladder function

Authors

DOI:

https://doi.org/10.14739/2310-1210.2022.2.240879

Keywords:

gallbladder, hypokinesia, non-alcoholic fatty liver disease, microbiota, short-chain fatty acids

Abstract

Aim. To determine the features of the intestinal microbiota in obese children with non-alcoholic fatty liver disease (NAFLD) depending on the functional state of the gallbladder.

Materials and methods. A total of 73 children aged 10–17 years (mean age – 12.15 ± 2.51 years) were examined. According to body mass index, transient elastography (Fibroscan®), and ultrasound data, the patients were divided into 3 groups: group I – 35 obese children with NAFLD and gallbladder hypokinesia, group II – 30 obese children with NAFLD and gallbladder normokinesia, group III (control) – 8 healthy children with normal weight and gallbladder normokinesia. Contractile function of the gallbladder was assessed by ultrasound examination after physiological food loading. Small intestinal bacterial overgrowth (SIBO) and lactose absorption were assessed with the hydrogen breath test (HBT) with lactose loading using a Gastrolyzer (Bedfont Scientific Ltd, UK). Qualitative and quantitative intestinal microbiome composition were studied using bacterial culture method with ten-fold dilutions (10-1–10-9) on standard sets of selective and differential-diagnostic culture media for the isolation of aerobic and anaerobic microbes. Fecal short-chain fatty acid (SCFA) content was evaluated with gas chromatography (Chromatec-Crystal-5000).

Results. Lactose-dependent SIBO was observed in almost half of NAFLD patients (42.9 %) without significant differences depending on functional activity of the gallbladder. Patients with decompensated dysbiosis predominated in group I children (37.1 % of patients). In group II children, the subcompensated dysbiosis was more common (36.7 % of patients). The concentration of Lactobacillus and Enterococcus in group I patients was significantly 1.9 times (P < 0.05) and 1.4 times (P < 0.05) lower, respectively, than that in group IІ patients. The level of fecal acetic acid and butyric acid in group I children was 6.9 and 2.0 times (P < 0.05) increased, respectively, compared to control group, assuming bile acids involvement in the regulation of microbiome composition.

Conclusions. Impaired contractile function of the gallbladder in NAFLD children is associated with a sharp decrease in the number of major symbionts of the intestinal microbiota as well as increased production of acetic and butyric SCFA.

Author Biographies

Yu. M. Stepanov, State Institution “Institute of Gastroenterology of the National Academy of Medical Sciences of Ukraine”, Dnipro

MD, PhD, DSc, Professor, Corresponding member of the National Academy of Medical Sciences of Ukraine, Director of the State Institution “Institute of Gastroenterology of the National Academy of Medical Sciences of Ukraine”, Dnipro

N. Yu. Zavhorodnia, State Institution “Institute of Gastroenterology of the National Academy of Medical Sciences of Ukraine”, Dnipro

MD, PhD, Head of the Department of Pediatric Gastroenterology

O. M. Tatarchuk, State Institution “Institute of Gastroenterology of the National Academy of Medical Sciences of Ukraine”, Dnipro

PhD, Senior researcher of the Research Sector

I. A. Klenina, State Institution “Institute of Gastroenterology of the National Academy of Medical Sciences of Ukraine”, Dnipro

PhD, Head of the Research Sector

O. I. Hrabovska, State Institution “Institute of Gastroenterology of the National Academy of Medical Sciences of Ukraine”, Dnipro

Researcher of the Research Sector

E. V. Zyhalo, State Institution “Institute of Gastroenterology of the National Academy of Medical Sciences of Ukraine”, Dnipro

MD, PhD, Senior researcher of the Department of Miniinvasive Endoscopic Interventions and Instrumental Diagnostics

O. P. Petishko, State Institution “Institute of Gastroenterology of the National Academy of Medical Sciences of Ukraine”, Dnipro

Researcher of the Department of Scientific-Organizational, Methodical Work and Information Technologies

N. S. Vishnarevska, State Institution “Institute of Gastroenterology of the National Academy of Medical Sciences of Ukraine”, Dnipro

bacteriologist of the Research Sector

V. V. Dolhopolova, State Institution “Institute of Gastroenterology of the National Academy of Medical Sciences of Ukraine”, Dnipro

MD, bacteriologist of the Research Sector

References

Shaunak, M., Byrne, C. D., Davis, N., Afolabi, P., Faust, S. N., & Davies, J. H. (2021). Non-alcoholic fatty liver disease and childhood obesity. Archives of Disease in Childhood, 106(1), 3-8. https://doi.org/10.1136/archdischild-2019-318063

Fang, Y. L., Chen, H., Wang, C. L., & Liang, L. (2018). Pathogenesis of non-alcoholic fatty liver disease in children and adolescence: From "two hit theory" to "multiple hit model". World Journal of Gastroenterology, 24(27), 2974-2983. https://doi.org/10.3748/wjg.v24.i27.2974

Kolesnikova, O. V. (2016). Kyshkova mikrobiota i metabolichnyi syndrom: shcho yikh obiednuie? [The intestinal microbiota and metabolic syndrome: the unifying factors?]. Suchasna hastroenterolohiia, 88(2), 61-70. [in Ukrainian].

Zavhorodnia, N. Yu., Lukianenko, O. Yu., Klenina, I. A., Hrabovska, O. I., Tatarchuk, O. M., & Vishnarevska, N. S. (2020). Assessment of the intestinal microbiota and fecal short-chain fatty acids content in children with non-alcoholic fatty liver disease. Gastroenterology, 54(1), 56-62. https://doi.org/10.22141/2308-2097.54.1.2020.199143

Stepanov, Y. M, Zavgorodnya, N. Y, Babiy, S. O., & Klenina, I. A. (2016). Vplyv funktsionalnoho stanu zhovchnoho mikhura na osoblyvosti lipidnoho obminu v ditei zi steatozom pechinky [Effect of functional disorders of the biliary tract on the peculiarities of lipid metabolism in children with hepatic steatosis]. Hastroenterolohiia, (4), 47-53. https://doi.org/10.22141/2308-2097.4.62.2016.81094 [in Ukrainian].

Colak, Y., Bozbey, G., Erim, T., Caklili, O. T., Ulasoglu, C., Senates, E., Mutlu, H. H., Mesci, B., Doğan, M. S., Tasan, G., Enc, F. Y., & Tuncer, I. (2016). Impaired Gallbladder Motility and Increased Gallbladder Wall Thickness in Patients with Nonalcoholic Fatty Liver Disease. Journal of Neurogastroenterology and Motility, 22(3), 470-476. https://doi.org/10.5056/jnm15159

Qi, L., Tian, Y., & Chen, Y. (2019). Gall bladder: The metabolic orchestrator. Diabetes/Metabolism Research and Reviews, 35(5), Article e3140. https://doi.org/10.1002/dmrr.3140

Jasirwan, C., Lesmana, C., Hasan, I., Sulaiman, A. S., & Gani, R. A. (2019). The role of gut microbiota in non-alcoholic fatty liver disease: pathways of mechanisms. Bioscience of Microbiota, Food and Health, 38(3), 81-88. https://doi.org/10.12938/bmfh.18-032

Sirchak, Ye. S., Griga, V. I., Petrichko, O. I., & Рichkar, Y. I. (2020). Efektyvnist vykorystannia Bifidobacterium infantis 35624 dlia likuvannia khvorykh na nealkoholnu zhyrovu khvorobu pechinky [Efficiency of using Bifidobacterium infantis 35624 in patients with non-alcoholic fatty liver disease]. Hastroenterolohiia, 54(1), 8-17. https://doi.org/10.22141/2308-2097.54.1.2020.199136 [in Ukrainian].

Fadieienko, G. D., & Solomentseva, T. A. (2020). Vozmozhnosti nemedikamentoznoi korrektsii kishechnoi mikrobioty u bol'nykh nealkogol'noi zhirovoi bolezn'yu pecheni [Possibilities of non-pharmacological correction of intestinal microbiota in patients with non-alcoholic fatty liver disease]. Suchasna hastroenterolohiia, (5), 71-78. https://doi.org/10.30978/MG-2020-5-71 [in Russian].

Zhang, H., DiBaise, J. K., Zuccolo, A., Kudrna, D., Braidotti, M., Yu, Y., Parameswaran, P., Crowell, M. D., Wing, R., Rittmann, B. E., & Krajmalnik-Brown, R. (2009). Human gut microbiota in obesity and after gastric bypass. PNAS, 106(7), 2365-2370. https://doi.org/10.1073/pnas.0812600106

Zhao, G., Nyman, M., & Jönsson, J. A. (2006). Rapid determination of short-chain fatty acids in colonic contents and faeces of humans and rats by acidified water-extraction and direct-injection gas chromatography. Biomedical Chromatography, 20(8), 674-682. https://doi.org/10.1002/bmc.580

Stepanov, Yu. M., & Boiko, T. Y. (2016). Dysbioz kyshechnyka ta efektyvnist vykorystannia probiotyka-bioenteroseptyka Enterozhermina v yoho korektsii (metodychni rekomendatsii) [Intestinal Dysbiosis and Efficacy of Probiotic Bioenteroseptic Enterogermina for Its Treatment (Practice Guidelines)]. Hastroenterolohiia, (3), 73-79. https://doi.org/10.22141/2308-2097.3.61.2016.79162 [in Ukrainian].

Stepanov, Yu. M., Didenko, V. I., Klenina, I. A., Zigalo, E. V., & Petishko, O. P. (2019). Patohenetychni aspekty vplyvu nadlyshkovoho bakterialnoho rostu na metabolizm zhyrnykh kyslot u khvorykh na khronichni dyfuzni zakhvoriuvannia pechinky [Pathogenetic aspects of the effects of the bacterial overgrowth syndrome on metabolism of free fatty acids in patients with chronic diffusive liver diseases]. Suchasna hastroenterolohiia, (6), 21-27. https://doi.org/10.30978/MG-2019-6-21 [in Ukrainian].

Safari, Z., & Gérard, P. (2019). The links between the gut microbiome and non-alcoholic fatty liver disease (NAFLD). Cellular and Molecular Life Sciences, 76(8), 1541-1558. https://doi.org/10.1007/s00018-019-03011-w

Puddu, A., Sanguineti, R., Montecucco, F., & Viviani, G. L. (2014). Evidence for the Gut Microbiota Short-Chain Fatty Acids as Key Pathophysiological Molecules Improving Diabetes. Mediators of Inflammation, 2014, Article 162021. https://doi.org/10.1155/2014/162021

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Published

2022-04-04

How to Cite

1.
Stepanov YM, Zavhorodnia NY, Tatarchuk OM, Klenina IA, Hrabovska OI, Zyhalo EV, Petishko OP, Vishnarevska NS, Dolhopolova VV. Intestinal microbiota in obese children with non-alcoholic fatty liver disease depending on the gallbladder function. Zaporozhye Medical Journal [Internet]. 2022Apr.4 [cited 2024Nov.14];24(2):181-6. Available from: http://zmj.zsmu.edu.ua/article/view/240879

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Original research