Year 2019 / Volume 111 / Number 4
Original
An altered fecal microbiota profile in patients with non-alcoholic fatty liver disease (NAFLD) associated with obesity

275-282

DOI: 10.17235/reed.2019.6068/2018

Esther Nistal, Luis E. Sáenz de Miera, María Ballesteros Pomar, Sonia Sánchez-Campos, María Victoria García-Mediavilla, Begoña Álvarez-Cuenllas, Pedro Linares, José Luis Olcoz, María Teresa Arias-Loste, Juan María García-Lobo, Javier Crespo, Javier González-Gallego, Francisco Jorquera Plaza,

Abstract
Introduction: increasing evidence suggests a role of intestinal dysbiosis in obesity and non-alcoholic fatty liver disease (NAFLD). The advances in recent years with regard to the role of the gut microbiota raise the potential utility of new therapeutic approaches based on the modification of the microbiome. Objective: the aim of this study was to compare the bacterial communities in obese patients with or without NAFLD to those of healthy controls. Patients and methods: the fecal microbiota composition of 20 healthy adults, 36 obese patients with NAFLD and 17 obese patients without NAFLD was determined by 16S ribosomal RNA sequencing using the Illumina MiSeq system. Results: the results highlighted significant differences in the phylum Firmicutes between patients with and without NAFLD, which was a determining factor of the disease and supported its possible role as a marker of NAFLD. At the genus level, the relative abundance of Blautia, Alkaliphilus, Flavobacterium and Akkermansia was reduced in obese patients, both with or without NAFLD, compared to healthy controls. Furthermore, the number of sequences from the genus Streptococcus was significantly higher in patients with NAFLD in comparison with individuals without the disease, constituting another possible marker. Comparison of bacterial communities at the genus level by a principal coordinate analysis indicated that the bacterial communities of patients with NAFLD were dispersed and did not form a group. Conclusion: in conclusion, these results indicate the role of intestinal dysbiosis in the development of NAFLD associated with obesity. There was a differential microbiota profile between obese patients, with and without NAFLD. Thus, supporting gut microbiota modulation as a therapeutic alternative for the prevention and treatment of NAFLD.
Share Button
New comment
Comments
No comments for this article
References
1 White DL, Kanwal F, El–Serag HB. Association between Nonalcoholic fatty liver disease and risk for hepatocellular cancer, based on systematic review. Clin Gastroenterol Hepatol 2012; 10: 1342–1359.e2.
2 Stepanova M, Rafiq N, Makhlouf H, et al. Predictors of all-cause mortality and liver-related mortality in patients with mon-alcoholic fatty liver disease (NAFLD). Dig Dis Sci 2013; 58: 3017–23.
3 Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006; 444: 1027–31.
4 Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature 2009; 457: 480–4.
5 Vrieze A, Van Nood E, Holleman F, et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 2012; 143: 913–916.e7.
6 Larsen N, Vogensen FK, van den Berg FWJ, et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 2010; 5: e9085.
7 Qin J, Li Y, Cai Z, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012; 490: 55–60.
8 Sato J, Kanazawa A, Ikeda F, et al. Gut dysbiosis and detection of "live gut bacteria" in blood of Japanese patients with type 2 diabetes. Diabetes Care 2014; 37: 2343–50.
9 Li J, Zhao F, Wang Y, et al. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome 2017; 5: 14.
10 Le Roy T, Llopis M, Lepage P, et al. Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice. Gut 2013; 62: 1787–94.
11 Henao-Mejia J, Elinav E, Jin C, et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 2012; 482: 179–85.
12 Porras D, Nistal E, Martínez-Flórez S, et al. Protective effect of quercetin on high-fat diet-induced non-alcoholic fatty liver disease in mice is mediated by modulating intestinal microbiota imbalance and related gut-liver axis activation. Free Radic Biol Med 2017; 102: 188–202.
13 Abu-Shanab A, Quigley EMM. The role of the gut microbiota in nonalcoholic fatty liver disease. Nat Rev Gastroenterol Hepatol 2010; 7: 691–701.
14 Bashiardes S, Shapiro H, Rozin S, Shibolet O, Elinav E. Non-alcoholic fatty liver and the gut microbiota. Mol Metab 2016; 5: 782–94.
15 Shen F, Zheng R-D, Sun X-Q, Ding W-J, Wang X-Y, Fan J-G. Gut microbiota dysbiosis in patients with non-alcoholic fatty liver disease. Hepatobiliary Pancreat Dis Int 2017; 16: 375–81.
16 Li F, Sun G, Wang Z, et al. Characteristics of fecal microbiota in non-alcoholic fatty liver disease patients. Sci China Life Sci 2018; 61: 770–8.
17 Michail S, Lin M, Frey MR, et al. Altered gut microbial energy and metabolism in children with non-alcoholic fatty liver disease. FEMS Microbiol Ecol 2015; 91: 1–9.
18 Raman M, Ahmed I, Gillevet PM, et al. Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2013; 11: 868–875.e3.
19 Spencer MD, Hamp TJ, Reid RW, Fischer LM, Zeisel SH, Fodor AA. Association between composition of the human gastrointestinal microbiome and development of fatty liver with choline deficiency. Gastroenterology 2011; 140: 976–86.
20 Boursier J, Mueller O, Barret M, et al. The severity of nonalcoholic fatty liver disease is associated with gut dysbiosis and shift in the metabolic function of the gut microbiota. Hepatology 2016; 63: 764–75.
21 Schnabl B, Brenner DA. Interactions between the intestinal microbiome and liver diseases. Gastroenterology 2014; 146: 1513–24.
22 Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007; 73: 5261–7.
23 Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010; 7: 335–6.
24 Kuczynski J, Stombaugh J, Walters WA, González A, Caporaso JG, Knight R. Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr. Protoc. Microbiol., Hoboken, NJ, USA: John Wiley & Sons, Inc., 2012:1E.5.1-1E.5.20.
25 Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26: 2460–1.
26 De Mandal S, Zothansanga, Panda AK, Bisht SS, Senthil Kumar N. MiSeq HV4 16S rRNA gene analysis of bacterial community composition among the cave sediments of Indo-Burma biodiversity hotspot. Environ Sci Pollut Res Int 2016; 23: 12216–26.
27 Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 2010; 26: 266–7.
28 Oksanen J, Blanchet FG, Kindt R, et al. Vegan: community ecology package. R package vegan, vers. 2.2-1 2015.
29 Inceoğlu Ö, Al-Soud WA, Salles JF, Semenov A V, van Elsas JD. Comparative analysis of bacterial communities in a potato field as determined by pyrosequencing. PLoS One 2011; 6: e23321.
30 Wong VW-S, Tse C-H, Lam TT-Y, et al. Molecular characterization of the fecal microbiota in patients with nonalcoholic steatohepatitis – a longitudinal study. PLoS One 2013; 8: e62885.
31 Wang B, Jiang X, Cao M, et al. Altered fecal microbiota correlates with liver biochemistry in nonobese patients with non-alcoholic fatty liver disease. Sci Rep 2016; 6: 32002.
32 Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Human gut microbes associated with obesity. Nature 2006; 444: 1022–3.
33 Bervoets L, Van Hoorenbeeck K, Kortleven I, et al. Differences in gut microbiota composition between obese and lean children: a cross-sectional study. Gut Pathog 2013; 5: 10.
34 Park JS, Seo JH, Youn H-S. Gut microbiota and clinical disease: obesity and nonalcoholic fatty liver disease. Pediatr Gastroenterol Hepatol Nutr 2013; 16: 22.
35 Kallus SJ, Brandt LJ. The intestinal microbiota and obesity. J Clin Gastroenterol 2012; 46: 16–24.
36 Yasir M, Angelakis E, Bibi F, et al. Comparison of the gut microbiota of people in France and Saudi Arabia. Nutr Diabetes 2015; 5: e153.
37 Kong L-C, 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: 16–24.
38 Zoetendal EG, Rajilic-Stojanovic M, de Vos WM. High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut 2008; 57: 1605–15.
39 Schwenger KJP, Bolzon CM, Li C, Allard JP. Non-alcoholic fatty liver disease and obesity: the role of the gut bacteria. Eur J Nutr 2018;doi: 10.1007/s00394-018-1844-5.
40 Sharpton SR, Ajmera V, Loomba R. Emerging role of the gut microbiome in nonalcoholic fatty liver disease: from composition to function. Clin Gastroenterol Hepatol 2018;doi: 10.1016/j.cgh.2018.08.065.
41 Liu J-P, Zou W-L, Chen S-J, et al. Effects of different diets on intestinal microbiota and nonalcoholic fatty liver disease development. World J Gastroenterol 2016; 22: 7353–64.
42 Del Chierico F, Nobili V, Vernocchi P, et al. Gut microbiota profiling of pediatric nonalcoholic fatty liver disease and obese patients unveiled by an integrated meta-omics-based approach. Hepatology 2017; 65: 451–64.
43 Miura K. Role of gut microbiota and Toll-like receptors in nonalcoholic fatty liver disease. World J Gastroenterol 2014; 20: 7381.
44 Everard A, Belzer C, Geurts L, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A 2013; 110: 9066–71.
45 Million M, Maraninchi M, Henry M, et al. Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii. Int J Obes 2012; 36: 817–25.
46 Chakraborti CK. New-found link between microbiota and obesity. World J Gastrointest Pathophysiol 2015; 6: 110–9.
47 Zhang X, Zhao Y, Xu J, et al. Modulation of gut microbiota by berberine and metformin during the treatment of high-fat diet-induced obesity in rats. Sci Rep 2015; 5: 14405.
Related articles

Letter to the Editor

GETTEMO position statement on bariatric endoscopic techniques as a voluntary medicine

DOI: 10.17235/reed.2017.5144/2017

Review

From the intestinal flora to the microbiome

DOI: 10.17235/reed.2017.4947/2017

Original

Multicenter study on the safety of bariatric endoscopy

DOI: 10.17235/reed.2017.4499/2016

Citation tools
Nistal E, Sáenz de Miera L, Ballesteros Pomar M, Sánchez-Campos S, García-Mediavilla M, Álvarez-Cuenllas B, et all. An altered fecal microbiota profile in patients with non-alcoholic fatty liver disease (NAFLD) associated with obesity. 6068/2018


Download to a citation manager

Download the citation for this article by clicking on one of the following citation managers:

Metrics
This article has received 1867 visits.
This article has been downloaded 668 times.

Statistics from Dimensions


Statistics from Plum Analytics

Publication history

Received: 26/11/2018

Accepted: 06/02/2019

Online First: 27/02/2019

Published: 04/04/2019

Article revision time: 63 days

Article Online First time: 93 days

Article editing time: 129 days


Share
This article hasn't been rated yet.
Reader rating:
Valora este artículo:




Asociación Española de Ecografía Digestiva Sociedad Española de Endoscopia Digestiva Sociedad Española de Patología Digestiva
The Spanish Journal of Gastroenterology is the official organ of the Sociedad Española de Patología Digestiva, the Sociedad Española de Endoscopia Digestiva and the Asociación Española de Ecografía Digestiva
Cookie policy Privacy Policy Legal Notice © Copyright 2023 y Creative Commons. The Spanish Journal of Gastroenterology