The DOI matches its Crossref record; 58 of the 58 references it cites were found in a registry or an index.
Microbiome Signatures Associated With Steatohepatitis and Moderate to Severe Fibrosis in Children With Nonalcoholic Fatty Liver Disease
Open accessAbstract
Background & aims The intestinal microbiome might affect the development and severity of nonalcoholic fatty liver disease (NAFLD). We analyzed microbiomes of children with and without NAFLD.Methods We performed a prospective, observational, cross-sectional study of 87 children (age range, 8-17 years) with biopsy-proven NAFLD and 37 children with obesity without NAFLD (controls). Fecal samples were collected and microbiome composition and functions were assessed using 16S ribosomal RNA amplicon sequencing and metagenomic shotgun sequencing. Microbial taxa were identified using zero-inflated negative binomial modeling. Genes contributing to bacterial pathways were identified using gene set enrichment analysis.Results Fecal microbiomes of children with NAFLD had lower α-diversity than those of control children (3.32 vs 3.52, P = .016). Fecal microbiomes from children with nonalcoholic steatohepatitis (NASH) had the lowest α-diversity (control, 3.52; NAFLD, 3.36; borderline NASH, 3.37; NASH, 2.97; P = .001). High abundance of Prevotella copri was associated with more severe fibrosis (P = .036). Genes for lipopolysaccharide biosynthesis were enriched in microbiomes from children with NASH (P < .001). Classification and regression tree model with level of alanine aminotransferase and relative abundance of the lipopolysaccharide pathway gene encoding 3-deoxy-d-manno-octulosonate 8-phosphate-phosphatase identified patients with NASH with an area under the receiver operating characteristic curve value of 0.92. Genes involved in flagellar assembly were enriched in the fecal microbiomes of patients with moderate to severe fibrosis (P < .001). Classification and regression tree models based on level of alanine aminotransferase and abundance of genes encoding flagellar biosynthesis protein had good accuracy for identifying case children with moderate to severe fibrosis (area under the receiver operating characteristic curve, 0.87).Conclusions In an analysis of fecal microbiomes of children with NAFLD, we associated NAFLD and NASH with intestinal dysbiosis. NAFLD and its severity were associated with greater abundance of genes encoding inflammatory bacterial products. Alterations to the intestinal microbiome might contribute to the pathogenesis of NAFLD and be used as markers of disease or severity.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“MASH fibrosis is linked to a unique gut microbiome (193-197), and specific microbiome signatures can distinguish human MASH from MASLD (4, 198, 199).”
From Found in translation—Fibrosis in metabolic dysfunction–associated steatohepatitis (MASH) (2023) · cites this paper as [195]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
McMurdie, P. J., & Holmes, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061217 · Cited by 21,942
UPARSE: highly accurate OTU sequences from microbial amplicon reads
Edgar, R. C. (2013) · Nature Methods · doi:10.1038/nmeth.2604 · Cited by 16,770
Non‐parametric multivariate analyses of changes in community structure
Clarke, K. R. (1993) · Australian Journal of Ecology · doi:10.1111/j.1442-9993.1993.tb00438.x · Cited by 14,449
An obesity-associated gut microbiome with increased capacity for energy harvest
Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006) · Nature · doi:10.1038/nature05414 · Cited by 12,444
Structure, function and diversity of the healthy human microbiome
The Human Microbiome Project Consortium (2012) · Nature · doi:10.1038/nature11234 · Cited by 11,726
Design and validation of a histological scoring system for nonalcoholic fatty liver disease†
Kleiner, D. E., Brunt, E. M., Van Natta, M., Behling, C., Contos, M. J., Cummings, O. W., Ferrell, L. D., Liu, Y., Torbenson, M. S., Unalp‐Arida, A., et al. (2005) · Hepatology · doi:10.1002/hep.20701 · Cited by 10,791
Self-citationDiet rapidly and reproducibly alters the human gut microbiome
David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., Wolfe, B. E., Ling, A. V., Devlin, A. S., Varma, Y., Fischbach, M. A., et al. (2014) · Nature · doi:10.1038/nature12820 · Cited by 10,100
SPECIES ASSEMBLAGES AND INDICATOR SPECIES:THE NEED FOR A FLEXIBLE ASYMMETRICAL APPROACH
Dufrêne, M., & Legendre, P. (1997) · Ecological Monographs · doi:10.1890/0012-9615(1997)067[0345:saaist]2.0.co;2 · Cited by 8,537
Human gut microbiome viewed across age and geography
Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I., Dominguez-Bello, M. G., Contreras, M., Magris, M., Hidalgo, G., Baldassano, R. N., Anokhin, A. P., et al. (2012) · Nature · doi:10.1038/nature11053 · Cited by 7,815
Turnbaugh, P. J., Ley, R. E., Hamady, M., Fraser-Liggett, C. M., Knight, R., & Gordon, J. I. (2007) · Nature · doi:10.1038/nature06244 · Cited by 6,091
Cited by
Sorted by citations
Mechanisms and disease consequences of nonalcoholic fatty liver disease
Loomba, R., Friedman, S. L., & Shulman, G. I. (2021) · Cell · doi:10.1016/j.cell.2021.04.015 · Cited by 2,002
“A link betweenNAFLD/NASH and themicrobiome is supported by several studies (Caussy et al., 2019; Da Silva et al., 2018; Hoyles et al., 2018; Loomba et al., 2017; Oh et al., 2020; Raman et al., 2013; Schwimmer et al., 2019; Sharpton et al., 2019).”
ResultTargher, G., Byrne, C. D., & Tilg, H. (2020) · Gut · doi:10.1136/gutjnl-2020-320622 · Cited by 879
“78 At a species level, concentrations of Ruminococcus, Blautia and Dorea were increased in NASH patients.”
The role of the gut microbiome and its metabolites in metabolic diseases
Wu, J., Wang, K., Wang, X., Pang, Y., & Jiang, C. (2020) · Protein & Cell · doi:10.1007/s13238-020-00814-7 · Cited by 592
Role of Insulin Resistance in MAFLD
Sakurai, Y., Kubota, N., Yamauchi, T., & Kadowaki, T. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22084156 · Cited by 448
Gut Microbiota Metabolites in NAFLD Pathogenesis and Therapeutic Implications
Chen, J., & Vitetta, L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21155214 · Cited by 370
“Schwimmer et al. (2019) studied the gut microbiota in NAFLD children, reporting that NAFLD had lower alpha-diversity of gut microbiota compared with healthy controls, while NASH had the lowest alpha-diversity [10].”
BackgroundNonalcoholic Fatty Liver Disease
Zhao, Y.-C., Zhao, G., Chen, Z., She, Z., Cai, J., & Li, H. (2019) · Hypertension · doi:10.1161/hypertensionaha.119.13419 · Cited by 244
“Recent randomized controlled trials have suggested that the use of probiotics and prebiotics may be an alternative therapy for NAFLD.67 Likewise, a number of studies have shown that the administration of probiotics could induce a modest but statistically significant decrease in blood pressure and might affect the meta…”
InfluentialLiver fibrosis in NAFLD/NASH: from pathophysiology towards diagnostic and therapeutic strategies
Parola, M., & Pinzani, M. (2023) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2023.101231 · Cited by 239
Lujan, P. V., Esmel, E. V., & Sacanella, E. (2021) · Nutrients · doi:10.3390/nu13051442 · Cited by 225
“The only consistent observations from the data are that greater amounts of Proteobacteria (especially Escherichia coli and other Enterobacteriaceae spp) and lower quantity of Bacteroidetes are observed in patients suffering from NAFLD, whereas a decreased Firmicutes:Bacteroidetes ratio is also noted [44,45].”
BackgroundIntrahepatic bacterial metataxonomic signature in non-alcoholic fatty liver disease
Sookoian, S. C., Salatino, A., Castaño, G. O., Landa, M. S., Fijalkowky, C., Garaycoechea, M. E., & Pirola, C. J. (2020) · Gut · doi:10.1136/gutjnl-2019-318811 · Cited by 207
An Introduction to Next Generation Sequencing Bioinformatic Analysis in Gut Microbiome Studies
Gao, B., Chi, L., Zhu, Y., Shi, X., Tu, P., Li, B. J., Yin, J., Gao, N., Shen, W., & Schnabl, B. (2021) · Biomolecules · doi:10.3390/biom11040530 · Cited by 178
“Shotgun metagenomic sequencing has been applied to study the functional changes of the gut microbiome in various diseases, such as inflammatory bowel disease [76], irritable bowel syndrome [77], alcohol‐associated liver disease [78,79], nonalcoholic fatty liver disease [80,81], hepatic steatosis [82], Crohn’s disease…”
BackgroundThe curious case of Prevotella copri
Abdelsalam, N. A., Hegazy, S. M., & Aziz, R. K. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2249152 · Cited by 174
“copri may represent a noninvasive predictor of liver fibrosis, particularly in the state of microbiome dysbiosis.(24,39) As stated above, liver health status is strongly associated with bile-microbiome interactions.”
BackgroundInfluentialFound in translation—Fibrosis in metabolic dysfunction–associated steatohepatitis (MASH)
Wang, S., & Friedman, S. L. (2023) · Science Translational Medicine · doi:10.1126/scitranslmed.adi0759 · Cited by 158
Witjes, J. J., Smits, L. P., Pekmez, C. T., Prodan, A., Meijnikman, A. S., Troelstra, M., Bouter, K. E. C., Herrema, H., Levin, E., Holleboom, A. G., et al. (2020) · Hepatology Communications · doi:10.1002/hep4.1601 · Cited by 158
“Feces from 4 healthy lean vegan donors (2 donated three times and five times, respectively; the other 2 donated only once) were used for allogenic gut microbiota transfer to individuals with NAFLD.”
BackgroundInfluentialRisk assessment with gut microbiome and metabolite markers in NAFLD development
Leung, H., Long, X., Ni, Y., Qian, L., Nychas, E., Siliceo, S. L., Pohl, D., Hanhineva, K., Liu, Y., Xu, A., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abk0855 · Cited by 152
Plaza‐Díaz, J., Solis‐Urra, P., Rodríguez‐Rodríguez, F., Arancibia, J. E. O., Navarro-Oliveros, M., Abadía‐Molina, F., & Álvarez‐Mercado, A. I. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21218351 · Cited by 150
Xu, L., Zhang, Y., Li, X., Li, C., Hu, H., Hu, J., Liu, M., Yang, Q. Z., Gu, P., Li, J., et al. (2025) · iMeta · doi:10.1002/imt2.270 · Cited by 143
Non-alcoholic fatty liver disease and childhood obesity
Shaunak, M., Byrne, C. D., Davis, N. L., Afolabi, P. R., Faust, S. N., & Davies, J. H. (2020) · Archives of Disease in Childhood · doi:10.1136/archdischild-2019-318063 · Cited by 128
Nonalcoholic Fatty Liver Disease and the Gut-Liver Axis: Exploring an Undernutrition Perspective
Bauer, K. C., Littlejohn, P. T., Ayala, V., Creus-Cuadros, A., & Finlay, B. B. (2022) · Gastroenterology · doi:10.1053/j.gastro.2022.01.058 · Cited by 127
Nonalcoholic Fatty Liver Disease in Children: Unique Considerations and Challenges
Goldner, D. L., & Lavine, J. E. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.01.048 · Cited by 129
Self-citationKhan, A., Ding, Z., Ishaq, M. H., Bacha, A. S., KHAN, I. A., Hanif, A., Li, W., & Guo, X. (2021) · International Journal of Biological Sciences · doi:10.7150/ijbs.56214 · Cited by 130
“Variations in the intestinal microbiome can contribute to the pathogenesis of NAFLD and can be used as biomarkers of disease and its severity [16].”
BackgroundResultBile acid and receptors: biology and drug discovery for nonalcoholic fatty liver disease
Jiao, T., Ma, Y., Guo, X., Ye, Y., & Xie, C. (2022) · Acta Pharmacologica Sinica · doi:10.1038/s41401-022-00880-z · Cited by 122
“Currently, accumulated evidences have disclosed the possible role of gut dysbiosis in NASH [161, 162].”
BackgroundRole of Microbiota-Derived Metabolites in Alcoholic and Non-Alcoholic Fatty Liver Diseases
Park, J. W., Kim, S. E., Lee, N. Y., Kim, J. H., Jung, J.-H., Jang, M.-K., Park, S.-H., Lee, M.-S., Kim, D.-J., Kim, H.-S., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms23010426 · Cited by 110
“Among the various risk factors contributing to NAFLD, changes in gut microbial composition have been recognized as risk factors for NAFLD, obesity, and diabetes [70,89,90].”
BackgroundEpidemiology of Pediatric Nonalcoholic Fatty Liver Disease
Yu, E. L., & Schwimmer, J. B. (2021) · Clinical Liver Disease · doi:10.1002/cld.1027 · Cited by 107
Self-citationGut Microbiome and Its Impact on Obesity and Obesity-Related Disorders
Sankararaman, S., Noriega, K. J., Velayuthan, S., Sferra, T. J., & Martindale, R. G. (2022) · Current Gastroenterology Reports · doi:10.1007/s11894-022-00859-0 · Cited by 114
Tokuhara, D. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.700058 · Cited by 106
“As in adults, dysbiosis of the gut microbiota has been found in children and adolescents with NAFLD or NASH worldwide (52, 54, 56, 57, 59, 61) (Table 1).”
BackgroundLau, H. C.-H., Zhang, X., & Yu, J. (2025) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-025-01089-1 · Cited by 126
Houttu, V., Csader, S., Nieuwdorp, M., Holleboom, A. G., & Schwab, U. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.716783 · Cited by 104
Kanda, T., Goto, T., Hirotsu, Y., Masuzaki, R., Moriyama, M., & Omata, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21041525 · Cited by 97
Tsai, M., Liu, Y.-Y., Lin, C., Wang, C., Wu, Y., Yong, C., Chen, K., Chuah, S., Yao, C., Huang, P., et al. (2020) · Nutrients · doi:10.3390/nu12030820 · Cited by 96
Zhu, X., Cai, J., Wang, Y., Liu, X., Chen, X., Wang, H., Wu, Z., Bao, W., Fan, H., & Wu, S. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242316733 · Cited by 96
“A study on pediatric subjects revealed that NAFLD was associated with higher levels of the phyla Bacteroidetes and Proteobacteria, while children who were simply overweight or obese had elevated levels of the phylum Firmicutes [8].”
BackgroundThe role of the gut microbiome and diet in the pathogenesis of non-alcoholic fatty liver disease
Jennison, E., & Byrne, C. D. (2020) · Clinical and Molecular Hepatology · doi:10.3350/cmh.2020.0129 · Cited by 91
“Schwimmer et al.(31) The gut microbiome composition was analysed in a group of 87 children with biopsy proven NAFLD & 37 obese children without NAFLD.”
BackgroundZhang, X., Lau, H. C.-H., & Yu, J. Q. (2025) · Pharmacological Reviews · doi:10.1016/j.pharmr.2024.100018 · Cited by 100
Watanabe, T., Tsuchiya, A., Takeuchi, S., Nojiri, S., Yoshida, T., Ogawa, M., Itoh, M., Takamura, M., Suganami, T., Ogawa, Y., et al. (2020) · Regenerative Therapy · doi:10.1016/j.reth.2020.03.012 · Cited by 87
“They also reported that genes for LPS biosynthesis were upregulated under NASH conditions [20].”
BackgroundEpidemiology and Rb1 gene of retinoblastoma.
Yun, J., Li, Y., Xu, C.-T., & Pan, B.-R. (2011) · PubMed · doi:10.3980/j.issn.2222-3959.2011.01.24 · Cited by 84
Kravetz, A. M., Testerman, T., Galuppo, B., Graf, J., Pierpont, B. M., Siebel, S., Feinn, R., & Santoro, N. (2020) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaa382 · Cited by 84
Lin, Y., Lin, H.-F., Wu, C.-C., Chen, C., & Ni, Y. (2022) · Journal of Gastroenterology · doi:10.1007/s00535-022-01909-0 · Cited by 83
Xanthakos, S. A., Ibrahim, S. H., Adams, K. H., Kohli, R., Sathya, P., Sundaram, S. S., Vos, M. B., Dhawan, A., Caprio, S., Behling, C. A., et al. (2025) · Hepatology · doi:10.1097/hep.0000000000001368 · Cited by 88
Self-citationFianchi, F., Liguori, A., Gasbarrini, A., Grieco, A., & Miele, L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22126485 · Cited by 77
“When considering the microbial populations, a high abundance of Prevotella copri was associated with more severe fibrosis [35].”
BackgroundThe gut microbiota–bile acid axis: A potential therapeutic target for liver fibrosis
Zhang, Y., Li, Z.-J., Gou, H.-Z., Song, X., & Zhang, L. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.945368 · Cited by 77
“As fibros i s progresses , the abundance of Firmicutes , Verrucomicrobia, and Actinobacteria decreases, and that of Bacteroidetes and Proteobacteria increases (Chen et al., 2011; Bajaj et al., 2012b; Qin et al., 2014; Lelouvier et al., 2016; Loomba et al., 2017; Schwimmer et al., 2019).”
BackgroundInfluentialSu, X. B., Chen, S., Liu, J., Feng, Y., Han, E., Hao, X., Liao, M., Cai, J., Zhang, S., Niu, J., et al. (2023) · Obesity Reviews · doi:10.1111/obr.13646 · Cited by 80
Dong, T. S., Katzka, W. R., Lagishetty, V., Luu, K., Hauer, M., Pisegna, J. R., & Jacobs, J. P. (2020) · Scientific Reports · doi:10.1038/s41598-020-59535-w · Cited by 72
Gut microbes in metabolic disturbances. Promising role for therapeutic manipulations?
Portincasa, P., Khalil, M., Graziani, A., Frühbeck, G., Baffy, G., Garruti, G., Ciaula, A. D., & Bonfrate, L. (2023) · European Journal of Internal Medicine · doi:10.1016/j.ejim.2023.10.002 · Cited by 78
Pan, X., Kaminga, A. C., Liu, A., Wen, S. W., Luo, M., & Luo, J. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.683743 · Cited by 68
Precision Medicine and Public Health: New Challenges for Effective and Sustainable Health
Traversi, D., Pulliero, A., Izzotti, A., Franchitti, E., Iacoviello, L., Gianfagna, F., Gialluisi, A., Izzi, B., Agodi, A., Barchitta, M., et al. (2021) · Journal of Personalized Medicine · doi:10.3390/jpm11020135 · Cited by 74
“Therefore, as can be expected, microbiota aberrations (dysbiosis), since childhood, have been associated with a range of communicable [108–110] and noncommunicable diseases, including obesity and metabolic syndrome [111], diabetes [112,113], inflammatory bowel disease, nonalcoholic fatty liver disease [114], asthma, a…”
BackgroundIntegrated Multi‐Cohort Analysis of the Parkinson's Disease Gut Metagenome
Boktor, J. C., Sharon, G., Metman, L. V., Hall, D. A., Engen, P. A., Zreloff, Z. J., Hakim, D., Bostick, J. W., Ousey, J. A., Lange, D., et al. (2023) · Movement Disorders · doi:10.1002/mds.29300 · Cited by 67
The Role of Gut-Derived Microbial Antigens on Liver Fibrosis Initiation and Progression
Chen, D., Le, T. H., Shahidipour, H., Read, S. A., & Ahlenstiel, G. (2019) · Cells · doi:10.3390/cells8111324 · Cited by 71
Vitamin D alleviates non-alcoholic fatty liver disease via restoring gut microbiota and metabolism
Zhang, X., Chen, L., Yang, J., Zhao, S.-S., Jin, S., Ao, N., Yang, J., Liu, H., & Du, J. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1117644 · Cited by 66
“Also, the Prevotella, negatively correlated with NAFLD severity, (Schwimmer et al., 2019) was increased after VD intervention.”
BackgroundKwan, S., Jiao, J., Joon, A. Y., Wei, P., Petty, L. E., Below, J. E., Daniel, C. R., Wu, X., Zhang, J., Jenq, R. R., et al. (2021) · Hepatology · doi:10.1002/hep.32197 · Cited by 65
“[40] Lastly, Clostridium sensu stricto 1 carries genes related to production of trimethylamine (TMA),[41] which is further metabolized by the host into trimethylamine N- oxide (TMAO), which may promote NAFLD.”
BackgroundInfluentialZheng, C., Wang, L., Zou, T., Lian, S., Luo, J., Lu, Y., Hao, H., Xu, Y., Xiang, Y., Zhang, X., et al. (2024) · Journal of Hepatology · doi:10.1016/j.jhep.2023.12.024 · Cited by 70
Zhao, T., Zhan, L., Zhou, W., Chen, W., Luo, J., Zhang, L., Weng, Z., Zhao, C., & Liu, S. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.647529 · Cited by 61
Maevskaya, M. V., Kotovskaya, Y. V., Ivashkin, V. T., Ткачева, О. Н., Troshina, E. A., Shestakova, M. V., Breder, V. V., Geyvandova, N. I., Doshchitsin, V. L., Dudinskaya, Е. N., et al. (2022) · Terapevticheskii arkhiv · doi:10.26442/00403660.2022.02.201363 · Cited by 66
Li, F., Zhang, T., He, Y., Gu, W., Yang, X., Zhao, R., & Yu, J. (2019) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2019.112232 · Cited by 60
Skin Microbiome Variation with Cancer Progression in Human Cutaneous Squamous Cell Carcinoma
Voigt, A. Y., Emiola, A., Johnson, J. S., Fleming, E. S., Nguyen, H. T., Zhou, W. L., Tsai, K. Y., Fink, C., & Oh, J. (2022) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2022.03.017 · Cited by 63
Self-citationZhou, J., Zhang, Q., Zhao, Y., Zou, Y. F., Chen, M., Zhou, S., & Wang, Z. (2022) · Scientific Reports · doi:10.1038/s41598-022-25140-2 · Cited by 60
Pediatric Non-Alcoholic Fatty Liver Disease: Nutritional Origins and Potential Molecular Mechanisms
Mandala, A., Janssen, R. C., Palle, S. K., Short, K. R., & Friedman, J. E. (2020) · Nutrients · doi:10.3390/nu12103166 · Cited by 61
“Genes involved in LPS biosynthesis were enriched in the gut microbiome of children with NASH [89].”
BackgroundZhang, L., El-Shabrawi, M. H. F., Baur, L. A., Byrne, C. D., Targher, G., Kehar, M., Porta, G., Lee, W. S., Lefere, S., Turan, S., et al. (2024) · Med · doi:10.1016/j.medj.2024.03.017 · Cited by 59
Yang, M., Yin, Y., Wang, F., Zhang, H., Ma, X., Yin, Y., Tan, B., & Chen, J. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.719967 · Cited by 56
Ali, R., Quinn, G. M., Umarova, R., Haddad, J. A., Zhang, G. Y., Townsend, E. C., Scheuing, L., Hill, K., Gewirtz, M. A., Rampertaap, S., et al. (2022) · Nature Microbiology · doi:10.1038/s41564-022-01273-y · Cited by 55
Gut Microbiome and Organ Fibrosis
Costa, C. F. F. A., Sampaio‐Maia, B., Araújo, R., Nascimento, D. S., Ferreira‐Gomes, J., Pestana, M., Azevedo, M. J., & Alencastre, I. S. (2022) · Nutrients · doi:10.3390/nu14020352 · Cited by 53
“[45] showed that a high abundance of Prevotella copri was associated with more severe fibrosis in children with NAFLD.”
BackgroundImpact of Helicobacter pylori-Related Metabolic Syndrome Parameters on Arterial Hypertension
Kountouras, J., Papaefthymiou, A., Pοlyzos, S. A., Deretzi, G., Vardaka, E., Soteriades, E. S., Tzitiridou‐Chatzopoulou, M., Gkolfakis, P., Karafyllidou, K., & Doulberis, M. (2021) · Microorganisms · doi:10.3390/microorganisms9112351 · Cited by 52
The influence of host genetics on liver microbiome composition in patients with NAFLD
Pirola, C. J., Salatino, A., Quintanilla, M. F., Castaño, G. O., Garaycoechea, M. E., & Sookoian, S. C. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.103858 · Cited by 49
Depletion of Gut Microbiota Inhibits Hepatic Lipid Accumulation in High-Fat Diet-Fed Mice
Han, H. L., Wang, M., Zhong, R., Yi, B., Schroyen, M., & Zhang, H. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23169350 · Cited by 52
“For example, patients with NAFLD had lower microbial diversity than healthy controls [5,6].”
BackgroundStatistical analysis of microbiome data: The challenge of sparsity
Pan, A. (2021) · Current Opinion in Endocrine and Metabolic Research · doi:10.1016/j.coemr.2021.05.005 · Cited by 49
Self-citationHe, L., Yao, D.-H., Wang, L., Zhang, L., & Bai, X. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.761836 · Cited by 49
Dietary Factors in the Control of Gut Homeostasis, Intestinal Stem Cells, and Colorectal Cancer
Francescangeli, F., Angelis, M. L. D., & Zeuner, A. (2019) · Nutrients · doi:10.3390/nu11122936 · Cited by 51
“In line with other studies showing gut microbiome signatures driven by specific diseases [160,161], Wirbel et al.”
ResultGut microbiota and their metabolites in the progression of non-alcoholic fatty liver disease
Zhou, J., Tripathi, M., Sinha, R. A., Singh, B. K., & Yen, P. M. (2021) · Hepatoma Research · doi:10.20517/2394-5079.2020.134 · Cited by 49
“NAFLD Proteobacteria([16-20]) Enterobacteriaceae([17,20]) Escherichia([16,20]) Rikenellaceae([18,21]) Dorea([18,22]) Rumminoccaceae([17-20]) Anaerosporobacter([21,23]) Coprococcus([16,20,21]) Eubacterium([16,20]) Faecalibacterium([20,23]) Prevotella([16,24]) Liver fibrosis or cirrhosis Proteobacteria([27]) Enterobacte…”
BackgroundShen, B., Gu, T., Shen, Z., Zhou, C., Guo, Y., Wang, J., Li, B., Xu, X., Li, F., Zhang, Q., et al. (2023) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2023.08.001 · Cited by 50
“30 Studies have found that fl agellin-TLR5 signaling contributes to hepatic lipid accumulation in a mice model of liver regeneration, whereas TLR5 knockout can attenuate tetrachloride-induced liver fi brosis.”
BackgroundPerspectives on youth‐onset nonalcoholic fatty liver disease
Castillo‐Leon, E., Cioffi, C. E., & Vos, M. B. (2020) · Endocrinology Diabetes & Metabolism · doi:10.1002/edm2.184 · Cited by 45
The pathogenic oral–gut–liver axis: new understandings and clinical implications
Imai, J., Kitamoto, S., & Kamada, N. (2021) · Expert Review of Clinical Immunology · doi:10.1080/1744666x.2021.1935877 · Cited by 46
Han, Y., Li, L., & Wang, B. (2022) · Frontiers of Medicine · doi:10.1007/s11684-022-0960-z · Cited by 43
“They showed that the abundance of Akkermansia in individuals with NAFL significantly decreased compared with that of control individuals [65].”
BackgroundWu, H., Chen, J., Guo, S., Deng, J., Zhou, Z., Zhang, X., Qi, T., Yu, F., & Yang, Q. L. (2025) · Gut Microbes · doi:10.1080/19490976.2025.2500099 · Cited by 42
“30 These studies suggest that as the disease progresses, patients with MASLD have a higher abundance of potentially pathogenic microbiota (such as Enterobacteriaceae and Enterococcaceae) but a lower abundance of commensal microbiota in the gut.”
Chen, L., Zhang, L., Wang, W., Qiu, W., Liu, L., Ning, A., Cao, J., Huang, M., & Zhong, M. (2020) · PLoS ONE · doi:10.1371/journal.pone.0232972 · Cited by 41
“The ALT level was used to identify steatohepatitis and to predict NASH or moderate to severe advanced fibrosis in previous studies [47, 48].”
MethodTrust Your Gut: The Association of Gut Microbiota and Liver Disease
Manzoor, R., Ahmed, W., Afify, N., Memon, M., Yasin, M., Memon, H., Rustom, M., Akeel, M. A., & Alhajri, N. (2022) · Microorganisms · doi:10.3390/microorganisms10051045 · Cited by 40
“[35] United States Prospective, observational, crosssectional study 87 NAFLD 37 healthy controls ↑ Bacteroidetes ↑ Proteobacteria ↓ Firmicutes ↓ α-diversity in NAFLD was attributed to the differences in bacterial abundance rather than an increase in specific phyla or genus ↑ Pro-inflammatory bacterial products (LPS) i…”
BackgroundAlterations of nasal microbiome in eosinophilic chronic rhinosinusitis
Liang, Y., Xie, R., Xiong, X., Hu, Z., Mao, X., Wang, X., Zhang, J., Sun, P., Yue, Z., Wang, W., et al. (2023) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2022.11.031 · Cited by 39
Gut Microbiota and Metabolic Dysfunction-Associated Steatotic Liver Disease
Scarpellini, E., Scarcella, M., Tack, J. F., Scarlata, G. G. M., Zanetti, M., & Abenavoli, L. (2024) · Antioxidants · doi:10.3390/antiox13111386 · Cited by 48
Hu, Y., He, J., Zheng, P., Mao, X., Huang, Z., Yan, H., Luo, Y., Yu, J., Luo, J., Yu, B., et al. (2021) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2021.1955654 · Cited by 39
“Increasing evidence supports a central role of gut microbiome in promoting energy intake and NAFLD development in obese patients (Moreira et al. 2018; Schwimmer et al. 2019; Soderborg et al. 2018).”
BackgroundDoes Resveratrol Improve Metabolic Dysfunction-Associated Steatotic Liver Disease (MASLD)?
Kasprzak‐Drozd, K., Niziński, P., Kasprzak, P., Kondracka, A., Oniszczuk, T., Rusinek, A., & Oniszczuk, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25073746 · Cited by 39
“In turn, studies in children suggest that elevated levels of Bacterioidetes, Proteobacteria, Enterobacteriaceae, Gammaproteobacteria, and lowered Firmicutes phyla can be significantly associated with liver steatosis [38].”
BackgroundZheng, Y., Hou, J., Guo, S., & Song, J. (2025) · Diabetology & Metabolic Syndrome · doi:10.1186/s13098-025-01589-9 · Cited by 41
The Role of the Intestinal Microbiota in Nonalcoholic Steatohepatitis
Xiang, H., Sun, D., Liu, X., She, Z., & Chen, Y. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.812610 · Cited by 37
“Similarly, Schwimmer et al. found that NAFLD patients had higher abundance of Oscillibacter, Lactonifactor, Akkermansia and Enterococcus, while NASH patients were accompanied by higher abundance of Lactobacillus and Oribacterium (14).”
ResultMorán‐Ramos, S., Cerqueda‐García, D., López-Contreras, B. E., Larrieta‐Carrasco, E., Villamil‐Ramírez, H., Molina‐Cruz, S., Torres, N., Sánchez‐Tapia, M., Hernández‐Pando, R., Aguilar-Salinas, C. A., et al. (2023) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.16147 · Cited by 36
Hoozemans, J., de Brauw, M., Nieuwdorp, M., & Gerdes, V. E. A. (2021) · Metabolites · doi:10.3390/metabo11060353 · Cited by 36
“In children, high abundance of Prevotella copri is associated with more severe fibrosis [65].”
BackgroundGuo, Q., Tang, Y., Li, Y., Xu, Z., Zhang, D., Liu, J., Wang, X., Xia, W., & Xu, S. (2021) · Nutrients · doi:10.3390/nu13072135 · Cited by 35
“Fecal microbiomes of children with NAFLD showed greater variation in fecal microbial beta-diversity (β-diversity) and higher abundance of Proteobacteria, which were demonstrated to lead to liver fibrosis [17].”
BackgroundHallmarks of the human intestinal microbiome on liver maturation and function
Almeida, J. I., Tenreiro, M. F., Martínez‐Santamaría, L., Guerrero‐Aspizua, S., Gisbert, J. P., Alves, P. M., Serra, M., & Baptista, P. M. (2021) · Journal of Hepatology · doi:10.1016/j.jhep.2021.10.015 · Cited by 37
de Conti, A., Tryndyak, V., Willett, R. A., Borowa‐Mazgaj, B., Watson, A., Patton, R. E., Khare, S., Muskhelishvili, L., Olson, G. R., Avigan, M., et al. (2020) · The FASEB Journal · doi:10.1096/fj.202000194r · Cited by 33
Carr, R. M., Li, Y., Chau, L., Friedman, E. S., Lee, J., Adorini, L., Erickson, M., Zaru, L., Shringarpure, R., MacConell, L., et al. (2023) · Hepatology · doi:10.1097/hep.0000000000000474 · Cited by 34
Hu, X., Zhou, R., Li, H., Zhao, X., Sun, Y., Fan, Y., & Zhang, S. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2021.805812 · Cited by 32
“Recent studies showed that NAFLD and its severity were associated with a high abundance of inflammatory bacterial products (19).”
BackgroundRecent advances in understanding and managing pediatric nonalcoholic fatty liver disease
Vittorio, J., & Lavine, J. E. (2020) · F1000Research · doi:10.12688/f1000research.24198.1 · Cited by 31
Self-citationZhang, Y., Jiang, W., Xu, J., Wu, N., Wang, Y., Lin, T., Liu, Y., & Liu, Y. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.535940 · Cited by 32
Alemán, J. O., Henderson, W. A., Walker, J. M., Ronning, A., Jones, D. R., Walter, P. J., Daniel, S. G., Bittinger, K. L., VAUGHAN, R. D., MacArthur, R. B., et al. (2021) · Journal of Clinical and Translational Science · doi:10.1017/cts.2021.801 · Cited by 35
“Some children with NAFLD or NASH have a distinctive gut microbiome [47], but the human response to excess fructose is very heterogeneous due to differences in liver metabolism [12].”
BackgroundZhao, Y., Zhao, M., Zhang, Y., Fu, Z., Jin, T., Song, J., Huang, Y., Zhao, C., & Wang, M. (2023) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2023.117383 · Cited by 30
The Microbiome and Its Implications in Cancer Immunotherapy
Choudhry, H. (2021) · Molecules · doi:10.3390/molecules26010206 · Cited by 31
“Scientists have identified that NAFLD, hepatitis B, hepatitis C, and alcoholic liver disease are primarily caused by unique patterns in the gut microbiome of patients with cirrhosis [135].”
BackgroundThe role of the gut microbiome and exercise in non-alcoholic fatty liver disease
Houttu, V., Boulund, U., Grefhorst, A., Soeters, M. R., Pinto‐Sietsma, S., Nieuwdorp, M., & Holleboom, A. G. (2020) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756284820941745 · Cited by 32
Mao, Q., Lin, B., Zhang, W., Zhang, Y., Zhang, Y., Cao, Q., & Xu, M. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1371574 · Cited by 29
Jia, W. P., Luo, J., Yang, F., Feng, X., Zeng, M., Dai, W., Pan, X., Yang, Y., Li, Y., Duan, Y., et al. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2351620 · Cited by 34
“17 Moreover, the taxonomic and functional resolution of gut microbiota has been limited to the 16S ribosomal RNA (16S rRNA) gene sequencing.”
BackgroundMetabolomic Predictors of Non-alcoholic Steatohepatitis and Advanced Fibrosis in Children
Kordy, K., Li, F., Lee, D., Kinchen, J. M., Jew, M., Rocque, M. E. L., Zabih, S., Saavedra, M., Woodward, C. L., Cunningham, N. J., et al. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.713234 · Cited by 32
“Our study builds upon recent multi-omics studies of fatty liver disease in adult cohorts and highlights key differences in non-invasive biomarker profiles of NASH and fibrosis that may be specific to the pediatric population (Qin et al., 2010; Bajaj et al., 2015; Boursier et al., 2016; Loomba et al., 2017; Schwimmer e…”
BackgroundGut microbiome and nonalcoholic fatty liver disease
Wu, M., & Fan, J. (2023) · Hepatobiliary & pancreatic diseases international · doi:10.1016/j.hbpd.2023.06.006 · Cited by 32
Gui, Q., Jin, H., Zhu, F., Lu, H., Zhang, Q., Xu, J. M., Yang, Y., & Xiao, C. (2021) · Infectious Diseases of Poverty · doi:10.1186/s40249-021-00821-8 · Cited by 28
Gillard, J., & Leclercq, I. A. (2023) · Clinical Science · doi:10.1042/cs20220697 · Cited by 29
Updates in Metabolic Dysfunction‐Associated Fatty Liver Disease (MAFLD) in Children
Rupasinghe, K., Hind, J. M., & Hegarty, R. (2023) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000003919 · Cited by 30
“…cross-sectional study of 87 children with biopsy confirmed MAFLD and 37 children with obesity without MAFLD (controls) showed that fecal microbiomes of children with MAFLD were associated with intestinal dysbiosis as well as greater abundance of genes encoding inflammatory bacterial products (44).”
BackgroundLiu, X., Liu, D., Tan, C., & Feng, W. (2023) · BMC Medical Informatics and Decision Making · doi:10.1186/s12911-023-02402-1 · Cited by 29
Metadata
- Authors
- Schwimmer, J. B., Johnson, J. S., Angeles, J. E., Behling, C., Belt, P. H., Borecki, I., Bross, C., Durelle, J., Goyal, N. P., Hamilton, G., Holtz, M. L., Lavine, J. E., Mitreva, M., Newton, K. P., Pan, A., Simpson, P. M., Sirlin, C. B., Sodergren, E., Tyagi, R., Yates, K. P., Weinstock, G. M., & Salzman, N. H.
- Affiliations
- University of California San Diego (US)
- The Jackson Laboratory for Genomic Medicine (US)
- Sharp Memorial Hospital (US)
- Johns Hopkins University (US)
- Washington University in St. Louis (US)
- Medical College of Wisconsin (US)
- Columbia University Irving Medical Center (US)
- Corresponding author
- Salzman, Nita H.
- ORCID
- Venue
- Gastroenterology
- Publisher
- Elsevier BV
- Published
- 2019-10
- Volume
- 157
- Issue
- 4
- Pages
- 1109-1122
- ISSN
- 0016-5085 (ISSN-L)
- PMC
- PMC6756995
- OpenAlex
- W2953761756
- Cited by
- 298
- References
- 58
- Citations by year
- 2026: 31 · 2025: 37 · 2024: 41 · 2023: 54 · 2022: 32 · 2021: 56 · 2020: 40 · 2019: 6
- FWCI
- 11.16
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Gastroenterology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
- Funders
- School of Medicine, University of California, San Diego
- Office of Extramural Research, National Institutes of Health
- 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 microbiota, fecal microbiota, Prevotella copri, lipopolysaccharide biosynthesis, flagellar assembly, dysbiosis, alpha diversity, alanine aminotransferase, children, obesity, disease severity markers, 16S rRNA
- MeSH terms
- Gastrointestinal Microbiome, Adolescent, Bacteria, Child, Cross-Sectional Studies, DNA, Bacterial, Feces, Female, Humans, Intestines, Liver Cirrhosis, Male, Prospective Studies, RNA, Ribosomal, 16S, Severity of Illness Index, Case-Control Studies, Ribotyping, Host-Pathogen Interactions, Metagenome, Dysbiosis, Non-alcoholic Fatty Liver Disease
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
