Hepatology, volume 68, issue 3, pages 918-932

Link between gut-microbiome derived metabolite and shared gene-effects with hepatic steatosis and fibrosis in NAFLD

Cyrielle Caussy ^{1, 2}

Cynthia Hsu ¹

Min‐Tzu Lo ³

Amy Liu ¹

Ricki Bettencourt ¹

Veeral Ajmera ¹

Shirin Bassirian ¹

Jonathan Hooker ⁴

Ethan Sy ⁴

Lisa Richards ¹

Nicholas Schork ⁵

Bernd Schnabl ^{1, 6}

David A. Brenner ^{1, 6}

Claude B. Sirlin ⁴

Chi‐Hua Chen ³

Rohit Loomba ^{1, 6, 7}

Hide authors affiliations Show authors affiliations: 7 affiliations

NAFLD Research Center; Department of Medicine; La Jolla California |

Université Lyon 1; Hospices Civils de Lyon; Lyon France |

Department of Radiology; University of California at San Diego; La Jolla California |

⁴

Liver Imaging Group, Department of Radiology; University of California at San Diego; La Jolla California |

⁵

Human Biology; J. Craig Venter Institute; La Jolla California |

⁶

Division of Gastroenterology, Department of Medicine; La Jolla California |

⁷

Division of Epidemiology, Department of Family and Preventive Medicine; University of California at San Diego; La Jolla California |

Publication type: Journal Article

Publication date: 2018-05-20

Wiley

Journal: Hepatology

Quartile SCImago

Quartile WOS

Impact factor: 13.5

ISSN: 02709139, 15273350

DOI: 10.1002/hep.29892

Copy DOI

Hepatology

Abstract

Previous studies have shown that gut-microbiome is associated with nonalcoholic fatty liver disease (NAFLD). We aimed to examine if serum metabolites, especially those derived from the gut-microbiome, have a shared gene-effect with hepatic steatosis and fibrosis. This is a cross-sectional analysis of a prospective discovery cohort including 156 well-characterized twins and families with untargeted metabolome profiling assessment. Hepatic steatosis was assessed using magnetic-resonance-imaging proton-density-fat-fraction (MRI-PDFF) and fibrosis using MR-elastography (MRE). A twin additive genetics and unique environment effects (AE) model was used to estimate the shared gene-effect between metabolites and hepatic steatosis and fibrosis. The findings were validated in an independent prospective validation cohort of 156 participants with biopsy-proven NAFLD including shotgun metagenomics sequencing assessment in a subgroup of the cohort. In the discovery cohort, 56 metabolites including 6 microbial metabolites had a significant shared gene-effect with both hepatic steatosis and fibrosis after adjustment for age, sex and ethnicity. In the validation cohort, 6 metabolites were associated with advanced fibrosis. Among them, only one microbial metabolite, 3-(4-hydroxyphenyl)lactate, remained consistent and statistically significantly associated with liver fibrosis in the discovery and validation cohort (fold-change of higher-MRE versus lower-MRE: 1.78, P < 0.001 and of advanced versus no advanced fibrosis: 1.26, P = 0.037, respectively). The share genetic determination of 3-(4-hydroxyphenyl)lactate with hepatic steatosis was RG :0.57,95%CI:0.27-0.80, P < 0.001 and with fibrosis was RG :0.54,95%CI:0.036-1, P = 0.036. Pathway reconstruction linked 3-(4-hydroxyphenyl)lactate to several human gut-microbiome species. In the validation cohort, 3-(4-hydroxyphenyl)lactate was significantly correlated with the abundance of several gut-microbiome species, belonging only to Firmicutes, Bacteroidetes and Proteobacteria phyla, previously reported as associated with advanced fibrosis. Conclusion: This proof of concept study provides evidence of a link between the gut-microbiome and 3-(4-hydroxyphenyl)lactate that shares gene-effect with hepatic steatosis and fibrosis. (Hepatology 2018).

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Top-30

Citations by journals

	1 2 3 4 5 6
Microorganisms	Microorganisms, 6, 4.29% Microorganisms 6 publications, 4.29%
World Journal of Gastroenterology	World Journal of Gastroenterology, 5, 3.57% World Journal of Gastroenterology 5 publications, 3.57%
Hepatology	Hepatology, 4, 2.86% Hepatology 4 publications, 2.86%
Frontiers in Immunology	Frontiers in Immunology, 4, 2.86% Frontiers in Immunology 4 publications, 2.86%
Clinical Gastroenterology and Hepatology	Clinical Gastroenterology and Hepatology, 4, 2.86% Clinical Gastroenterology and Hepatology 4 publications, 2.86%
Gut Microbes	Gut Microbes, 4, 2.86% Gut Microbes 4 publications, 2.86%
Gut	Gut, 4, 2.86% Gut 4 publications, 2.86%
International Journal of Molecular Sciences	International Journal of Molecular Sciences, 3, 2.14% International Journal of Molecular Sciences 3 publications, 2.14%
Nature Reviews Gastroenterology and Hepatology	Nature Reviews Gastroenterology and Hepatology, 3, 2.14% Nature Reviews Gastroenterology and Hepatology 3 publications, 2.14%
European Journal of Clinical Investigation	European Journal of Clinical Investigation, 3, 2.14% European Journal of Clinical Investigation 3 publications, 2.14%
American Journal of Physiology - Gastrointestinal and Liver Physiology	American Journal of Physiology - Gastrointestinal and Liver Physiology, 3, 2.14% American Journal of Physiology - Gastrointestinal and Liver Physiology 3 publications, 2.14%
Nature Communications	Nature Communications, 2, 1.43% Nature Communications 2 publications, 1.43%
Hepatology Communications	Hepatology Communications, 2, 1.43% Hepatology Communications 2 publications, 1.43%
Journal of Clinical Medicine	Journal of Clinical Medicine, 2, 1.43% Journal of Clinical Medicine 2 publications, 1.43%
Cells	Cells, 2, 1.43% Cells 2 publications, 1.43%
Metabolites	Metabolites, 2, 1.43% Metabolites 2 publications, 1.43%
Biomedicines	Biomedicines, 2, 1.43% Biomedicines 2 publications, 1.43%
Diagnostics	Diagnostics, 2, 1.43% Diagnostics 2 publications, 1.43%
Frontiers in Nutrition	Frontiers in Nutrition, 2, 1.43% Frontiers in Nutrition 2 publications, 1.43%
Pharmacological Research	Pharmacological Research, 2, 1.43% Pharmacological Research 2 publications, 1.43%
Gastroenterology	Gastroenterology, 2, 1.43% Gastroenterology 2 publications, 1.43%
Cell Metabolism	Cell Metabolism, 2, 1.43% Cell Metabolism 2 publications, 1.43%
Journal of Nutrition	Journal of Nutrition, 2, 1.43% Journal of Nutrition 2 publications, 1.43%
Journal of Hepatology	Journal of Hepatology, 2, 1.43% Journal of Hepatology 2 publications, 1.43%
Alimentary Pharmacology and Therapeutics	Alimentary Pharmacology and Therapeutics, 2, 1.43% Alimentary Pharmacology and Therapeutics 2 publications, 1.43%
Molecular Nutrition and Food Research	Molecular Nutrition and Food Research, 2, 1.43% Molecular Nutrition and Food Research 2 publications, 1.43%
Journal of Clinical Biochemistry and Nutrition	Journal of Clinical Biochemistry and Nutrition, 2, 1.43% Journal of Clinical Biochemistry and Nutrition 2 publications, 1.43%
Endocrinology	Endocrinology, 2, 1.43% Endocrinology 2 publications, 1.43%
Journal of Immunology	Journal of Immunology, 1, 0.71% Journal of Immunology 1 publication, 0.71%
	1 2 3 4 5 6

Citations by publishers

	5 10 15 20 25 30
Elsevier	Elsevier, 27, 19.29% Elsevier 27 publications, 19.29%
Multidisciplinary Digital Publishing Institute (MDPI)	Multidisciplinary Digital Publishing Institute (MDPI), 22, 15.71% Multidisciplinary Digital Publishing Institute (MDPI) 22 publications, 15.71%
Wiley	Wiley, 20, 14.29% Wiley 20 publications, 14.29%
Springer Nature	Springer Nature, 13, 9.29% Springer Nature 13 publications, 9.29%
Frontiers Media S.A.	Frontiers Media S.A., 11, 7.86% Frontiers Media S.A. 11 publications, 7.86%
Baishideng Publishing Group	Baishideng Publishing Group, 5, 3.57% Baishideng Publishing Group 5 publications, 3.57%
Taylor & Francis	Taylor & Francis, 5, 3.57% Taylor & Francis 5 publications, 3.57%
BMJ	BMJ, 4, 2.86% BMJ 4 publications, 2.86%
American Physiological Society	American Physiological Society, 4, 2.86% American Physiological Society 4 publications, 2.86%
SAGE	SAGE, 3, 2.14% SAGE 3 publications, 2.14%
Wolters Kluwer Health	Wolters Kluwer Health, 2, 1.43% Wolters Kluwer Health 2 publications, 1.43%
American Society for Microbiology	American Society for Microbiology, 2, 1.43% American Society for Microbiology 2 publications, 1.43%
American Society for Nutrition	American Society for Nutrition, 2, 1.43% American Society for Nutrition 2 publications, 1.43%
Oxford University Press	Oxford University Press, 2, 1.43% Oxford University Press 2 publications, 1.43%
Cold Spring Harbor Laboratory	Cold Spring Harbor Laboratory, 2, 1.43% Cold Spring Harbor Laboratory 2 publications, 1.43%
Institute of Applied Biochemistry	Institute of Applied Biochemistry, 2, 1.43% Institute of Applied Biochemistry 2 publications, 1.43%
The American Association of Immunologists	The American Association of Immunologists, 1, 0.71% The American Association of Immunologists 1 publication, 0.71%
American Society for Clinical Investigation	American Society for Clinical Investigation, 1, 0.71% American Society for Clinical Investigation 1 publication, 0.71%
KeAi Communications Co.	KeAi Communications Co., 1, 0.71% KeAi Communications Co. 1 publication, 0.71%
Thieme	Thieme, 1, 0.71% Thieme 1 publication, 0.71%
Moscow Regional Research and Clinical Institute (MONIKI)	Moscow Regional Research and Clinical Institute (MONIKI), 1, 0.71% Moscow Regional Research and Clinical Institute (MONIKI) 1 publication, 0.71%
Bioscientifica	Bioscientifica, 1, 0.71% Bioscientifica 1 publication, 0.71%
American Association for the Advancement of Science (AAAS)	American Association for the Advancement of Science (AAAS), 1, 0.71% American Association for the Advancement of Science (AAAS) 1 publication, 0.71%
The Endocrine Society	The Endocrine Society, 1, 0.71% The Endocrine Society 1 publication, 0.71%
OAE Publishing Inc.	OAE Publishing Inc., 1, 0.71% OAE Publishing Inc. 1 publication, 0.71%
Autonomous Non-profit Organization Editorial Board of the journal Uspekhi Khimii	Autonomous Non-profit Organization Editorial Board of the journal Uspekhi Khimii, 1, 0.71% Autonomous Non-profit Organization Editorial Board of the journal Uspekhi Khimii 1 publication, 0.71%
Research Square Platform LLC	Research Square Platform LLC, 1, 0.71% Research Square Platform LLC 1 publication, 0.71%
	5 10 15 20 25 30

We do not take into account publications without a DOI.
Statistics recalculated only for publications connected to researchers, organizations and labs registered on the platform.
Statistics recalculated weekly.

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Caussy C. et al. Link between gut-microbiome derived metabolite and shared gene-effects with hepatic steatosis and fibrosis in NAFLD // Hepatology. 2018. Vol. 68. No. 3. pp. 918-932.

GOST all authors (up to 50) Copy

Caussy C., Hsu C., Lo M., Liu A., Bettencourt R., Ajmera V., Bassirian S., Hooker J., Sy E., Richards L., Schork N., Schnabl B., Brenner D. A., Sirlin C. B., Chen C., Loomba R. Link between gut-microbiome derived metabolite and shared gene-effects with hepatic steatosis and fibrosis in NAFLD // Hepatology. 2018. Vol. 68. No. 3. pp. 918-932.

RIS |

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RIS Copy

TY - JOUR

DO - 10.1002/hep.29892

UR - https://doi.org/10.1002/hep.29892

TI - Link between gut-microbiome derived metabolite and shared gene-effects with hepatic steatosis and fibrosis in NAFLD

T2 - Hepatology

AU - Caussy, Cyrielle

AU - Hsu, Cynthia

AU - Lo, Min‐Tzu

AU - Liu, Amy

AU - Bettencourt, Ricki

AU - Bassirian, Shirin

AU - Hooker, Jonathan

AU - Sy, Ethan

AU - Richards, Lisa

AU - Schork, Nicholas

AU - Schnabl, Bernd

AU - Brenner, David A.

AU - Sirlin, Claude B.

AU - Chen, Chi‐Hua

AU - Loomba, Rohit

AU - Ajmera, Veeral

PY - 2018

DA - 2018/05/20 00:00:00

PB - Wiley

SP - 918-932

IS - 3

VL - 68

SN - 0270-9139

SN - 1527-3350

ER -

BibTex |

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BibTex Copy

@article{2018_Caussy,

author = {Cyrielle Caussy and Cynthia Hsu and Min‐Tzu Lo and Amy Liu and Ricki Bettencourt and Shirin Bassirian and Jonathan Hooker and Ethan Sy and Lisa Richards and Nicholas Schork and Bernd Schnabl and David A. Brenner and Claude B. Sirlin and Chi‐Hua Chen and Rohit Loomba and Veeral Ajmera},

title = {Link between gut-microbiome derived metabolite and shared gene-effects with hepatic steatosis and fibrosis in NAFLD},

journal = {Hepatology},

year = {2018},

volume = {68},

publisher = {Wiley},

month = {may},

url = {https://doi.org/10.1002/hep.29892},

number = {3},

pages = {918--932},

doi = {10.1002/hep.29892}

}

MLA

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MLA Copy

Caussy, Cyrielle, et al. “Link between gut-microbiome derived metabolite and shared gene-effects with hepatic steatosis and fibrosis in NAFLD.” Hepatology, vol. 68, no. 3, May. 2018, pp. 918-932. https://doi.org/10.1002/hep.29892.

Found error?

Publisher

Wiley

Journal

Hepatology

Quartile SCImago

Quartile WOS

Impact factor

13.5

ISSN

02709139 (Print)
15273350 (Electronic)