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The severity of nonalcoholic fatty liver disease is associated with gut dysbiosis and shift in the metabolic function of the gut microbiota
Open accessAbstract
Several animal studies have emphasized the role of gut microbiota in nonalcoholic fatty liver disease (NAFLD). However, data about gut dysbiosis in human NAFLD remain scarce in the literature, especially studies including the whole spectrum of NAFLD lesions. We aimed to evaluate the association between gut dysbiosis and severe NAFLD lesions, that is, nonalcoholic steatohepatitis (NASH) and fibrosis, in a well‐characterized population of adult NAFLD. Fifty‐seven patients with biopsy‐proven NAFLD were enrolled. Taxonomic composition of gut microbiota was determined using 16S ribosomal RNA gene sequencing of stool samples. Thirty patients had F0/F1 fibrosis stage at liver biopsy (10 with NASH), and 27 patients had significant F≥2 fibrosis (25 with NASH). Bacteroides abundance was significantly increased in NASH and F≥2 patients, whereas Prevotella abundance was decreased. Ruminococcus abundance was significantly higher in F≥2 patients. By multivariate analysis, Bacteroides abundance was independently associated with NASH and Ruminococcus with F≥2 fibrosis. Stratification according to the abundance of these two bacteria generated three patient subgroups with increasing severity of NAFLD lesions. Based on imputed metagenomic profiles, Kyoto Encyclopedia of Genes and Genomes pathways significantly related to NASH and fibrosis F≥2 were mostly related to carbohydrate, lipid, and amino acid metabolism. Conclusion: NAFLD severity associates with gut dysbiosis and a shift in metabolic function of the gut microbiota. We identified Bacteroides as independently associated with NASH and Ruminococcus with significant fibrosis. Thus, gut microbiota analysis adds information to classical predictors of NAFLD severity and suggests novel metabolic targets for pre‐/probiotics therapies. (H epatology 2016;63:764–775)
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“Boursier et al. found that NAFLD severity was associated with gut dysbiosis and a shift in the metabolic function of the gut microbiota with Bacteroides independently associated with the occurrence of NASH, and Ruminococcus with the presence of significant fibrosis [230].”
From Gut-pancreas-liver Axis as a target for treatment of NAFLD/NASH (2020) · cites this paper as [230]
In the citing paper
“Likewise, a number of studies have demonstrated alterations of the gut microbiota in earlier stages of liver disease 35,36 as well as in animal models16,31.”
From The gut microbiome and liver cancer: mechanisms and clinical translation (2017) · cites this paper as [36]
In the citing paper
“However, bacterial abundance patterns were not consistent between studies, with levels of Bacteroidetes increased in some studies36,56 and decreased in other studies57,58, and a substantial overlap with healthy individuals59.”
From The gut microbiome and liver cancer: mechanisms and clinical translation (2017) · cites this paper as [36]
In the citing paper
“Interestingly, Ruminococcaceae have been found to be enriched in samples from fibrotic patients with NAFLD/NASH36,37, supporting their role in the pathogenesis of other chronic liver diseases that also associate with impaired intestinal barrier function.”
From Cholestasis induced by bile duct ligation promotes changes in the intestinal microbiome in mice (2019) · cites this paper as [37]
In the citing paper
“As well, in those studies it was shown that NALFD/NASH in patients associated with increased abundance of Bacteroides abundance36,37.”
From Cholestasis induced by bile duct ligation promotes changes in the intestinal microbiome in mice (2019) · cites this paper as [37]
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Probiotics and Prebiotics as a Strategy for Non-Alcoholic Fatty Liver Disease, a Narrative Review
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ResultThe Intestinal Microbiome in Nonalcoholic Fatty Liver Disease
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BackgroundGut microbiota plasticity in insular lizards under reversed island syndrome
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“Recently, the relationship between gut microbiota and metabolic diseases has attracted attention from the scholarly community because intestinal flora has been confirmed as a target for the prevention and treatment of obesity, metabolic syndrome and cardiovascular diseases (21).”
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BackgroundGut microbiota in MAFLD: therapeutic and diagnostic implications
Alghamdi, W., Mosli, M. H., & Alqahtani, S. A. (2024) · Therapeutic Advances in Endocrinology and Metabolism · doi:10.1177/20420188241242937 · Cited by 33
“In 25–29 Further comprehensive investigations are required to establish microbial signatures associated with MAFLD, enabling the development of targeted preventive and therapeutic strategies.”
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The Microbiome and Hepatocellular Carcinoma
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“(51) Animal models have demonstrated similar findings with both Akkermansia and Bifidobacterium linked to reduced inflammation and attenuation of liver injury,(74,75) whereas numerous models have shown increased Bacteroides in NASH animal models.(23,45)”
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“As shown in Figure 4A, at the family level, the main intestinal flora of chow group were Akkermansiaceae and Muribaculaceae, which belong to Verrucomicrobia and Bacteroidetes, respectively, according to the phylogenetic tree.”
BackgroundNext Generation Probiotics for Neutralizing Obesogenic Effects: Taxa Culturing Searching Strategies
López‐Moreno, A., Acuña, I., Torres-Sánchez, A., Ruiz-Moreno, Á., Cerk, K., Rivas, A., Suárez, A., Monteoliva‐Sánchez, M., & Aguilera, J. (2021) · Nutrients · doi:10.3390/nu13051617 · Cited by 35
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Host–Microbiota Interactions in Liver Inflammation and Cancer
Giraud, J., & Saleh, M. (2021) · Cancers · doi:10.3390/cancers13174342 · Cited by 32
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“Increased abundance of genus Bacteroides and decreased Prevotella levels have been found in NASH compared with NAFLD patients, and Ruminococcus abundance increased in patients in fibrosis stage F ≥ 2 [10].”
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Molecular Mechanisms Regulating Obesity-Associated Hepatocellular Carcinoma
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Buchynskyi, M., Kamyshna, I., Halabitska, I., Petakh, P., Kunduzova, O., Oksenych, V., & Kamyshnyi, O. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1577724 · Cited by 30
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“Intestinal dysbiosis favors development and progression of metabolic liver disease and is characterized in adult patients by reduced abundance of Bacteroidetes and elevated Prevotella and Prophyromonas spp.(104) together with reduced diversity of the microbiota.”
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“The gut microbes, which are part of this two-way communication between the gut and liver, are essential for maintaining the homeostasis of the gut-liver axis (18, 19).”
BackgroundCai, T., Song, X., Xu, X., Dong, L., Liang, S., Xin, M., Huang, Y., Zhu, L., Li, T., Wang, X., et al. (2024) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2024.1323261 · Cited by 32
“For example, the ratio of Firmicutes to Bacteroides is greater in patients with MAFLD than in healthy people, and the abundances of Proteobacteria and Enterobacteriaceae increase while that of Ruminococcaceae decreases in these patients (Boursier et al., 2016).”
BackgroundIs psoriasis a bowel disease? Successful treatment with bile acids and bioflavonoids suggests it is
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Are There Potential Applications of Fecal Microbiota Transplantation beyond Intestinal Disorders?
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Systems biology perspective for studying the gut microbiota in human physiology and liver diseases
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“In addition, Proteobacteria, which includes Escherichia, is the most common differentially abundant taxon between obese patients with NASH and those without NASH (Boursier et al., 2016).”
BackgroundGenetic regulation of liver lipids in a mouse model of insulin resistance and hepatic steatosis
Norheim, F., Krishnan, K. C., Bjellaas, T., Vergnes, L., Pan, C., Parks, B. W., Meng, Y., Lang, J., Ward, J. A., Reue, K., et al. (2021) · Molecular Systems Biology · doi:10.15252/msb.20209684 · Cited by 29
“These analyses highlighted clusters of TAGs strongly correlated with the abundance of Ruminococcus, a relationship which has been observed with progression from NAFLD to non-alcoholic steatohepatitis (NASH) in humans (Boursier et al, 2016; Fig 2B).”
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“WT mice which is intriguing, given that elevated Ruminococcus abundance was reported in NASH patients and associated with increased liver fibrosis [45].”
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“Altered fecal microbiota have been described in human fatty liver disease [21], and probiotics may reduce liver fat [22].”
BackgroundDistinctive features of hepatocellular carcinoma in non-alcoholic fatty liver disease.
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Pathophysiological Mechanisms in Non-Alcoholic Fatty Liver Disease: From Drivers to Targets
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“The second and third articles were published in PNAS and Hepatology, with 777 and 638 citations, respectively (25, 26).”
BackgroundBastian, W. P., Hasan, I., Lesmana, C. R. A., Rinaldi, I., & Gani, R. A. (2019) · Case Reports in Gastroenterology · doi:10.1159/000498946 · Cited by 31
Dai, J.-J., Zhang, Y., & Zhang, Z. (2023) · World Journal of Gastroenterology · doi:10.3748/wjg.v29.i37.5339 · Cited by 31
“A gut microbiota analysis provided a theoretical basis for NAFLD patients to regulate diet structure and intestinal microbial preparations[98].”
The implication of neutrophil extracellular traps in nonalcoholic fatty liver disease
Fa, P., Ke, B. G., Dupre, A., Tsung, A., & Zhang, H. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1292679 · Cited by 31
“Numerous studies have demonstrated that an imbalance in gut microbiota can disrupt the homeostasis of the intestinal system, thereby increasing the risk of advanced NAFLD (127 – 132).”
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Bahitham, W., Banoun, Y., Aljahdali, M., Almuaiqly, G., Bahshwan, S. M., Aljahdali, L., Sanai, F. M., Rosado, A. S., & Sergi, C. M. (2025) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1637071 · Cited by 36
The Fecal Metagenomics of Malayan Pangolins Identifies an Extensive Adaptation to Myrmecophagy
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“In particular, Bacteroides and Ruminococcus abundance correlate with the severity of liver inflammation and fibrosis [51].”
BackgroundStatins in Non-alcoholic Steatohepatitis
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“An association between enteric malnutrition and NASH was proposed not long ago [28].”
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“First, anomalous abundance changes of bacterial phyla affect the severity of NAFLD (Boursier et al., 2016).”
BackgroundEffects of probiotics on non-alcoholic fatty liver disease: a review of human clinical trials
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Current Therapeutical Approaches Targeting Lipid Metabolism in NAFLD
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“In addition, bacterial products derived from the microbiota can also trigger the immune response in the liver, either through the activation of T [77] or B lymphocytes [78] and thus have a role in determining the severity of the phenotype [72].”
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“Notably, butyric acid-producing bacteria and other SCFA-producing microbes have been shown to reduce the progression of liver cirrhosis and NASH [37, 38].”
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“Moreover, a correlation between the increased levels of Bacteroidetes and NAFLD development/progression as well as escalation of the Bacteroidetes/Firmicutes ratio in NAFLD patients was previously reported.(41,42) a ab abc abcd”
Background
Metadata
- Authors
- Boursier, J., Mueller, O., Barret, M., Machado, M., Fizanne, L., Araujo‐Perez, F., Guy, C. D., Seed, P. C., Rawls, J. F., David, L. A., Hunault, G., Oberti, F., Calès, P., & Diehl, A. M.
- Affiliations
- Centre Hospitalier Universitaire d'Angers (FR)
- Duke University (US)
- Institut de Recherche en Horticulture et Semences (FR)
- Duke Medical Center (US)
- HIFIH Laboratory, UPRES 3859, SFR 4208,LUNAM University,Angers,France
- Department of Pediatrics,Duke University Medical Center,Durham,NC
- Corresponding author
- Boursier, Jérôme
- ORCID
- Venue
- Hepatology
- Published
- 2016-01-13
- Volume
- 63
- Issue
- 3
- Pages
- 764-775
- ISSN
- 0270-9139 (ISSN-L)
- 1527-3350
- PMC
- PMC4975935
- OpenAlex
- W2178380008
- Cited by
- 1,483
- References
- 51
- Citations by year
- 2026: 105 · 2025: 162 · 2024: 180 · 2023: 190 · 2022: 161 · 2021: 191 · 2020: 154 · 2019: 132 · 2018: 91 · 2017: 74 · 2016: 37
- FWCI
- 29.69
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Hepatology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion)
- Funders
- Association Française pour l'Etude du Foie
- Société Nationale Française de Gastro-Entérologie
- National Institutes of Health
- National Institute of Diabetes and Digestive and Kidney Diseases (R01-DK106633, R56DK106633, R01DK053792)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Hepatology › Liver Disease Diagnosis and Treatment
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Keywords
- non-alcoholic fatty liver disease, nonalcoholic steatohepatitis, liver fibrosis, gut dysbiosis, gut microbiota, Bacteroides, Ruminococcus, Prevotella, NAFLD severity, carbohydrate metabolism, lipid metabolism, amino acid metabolism, probiotics
- MeSH terms
- Gastrointestinal Microbiome, Aged, Feces, Female, Fibrosis, Humans, Liver, Male, Middle Aged, Metagenome, Dysbiosis, Non-alcoholic Fatty Liver Disease
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