Elevated C-reactive protein mediates the liver-brain axis: a preliminary study.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Jul 2023
Historique:
received: 18 02 2023
revised: 10 06 2023
accepted: 11 06 2023
medline: 17 7 2023
pubmed: 26 6 2023
entrez: 25 6 2023
Statut: ppublish

Résumé

Chronic liver diseases of all etiologies exist along a spectrum with varying degrees of hepatic fibrosis. Despite accumulating evidence implying associations between liver fibrosis and cognitive functioning, there is limited research exploring the underlying neurobiological factors and the possible mediating role of inflammation on the liver-brain axis. Using data from the UK Biobank, we examined the cross-sectional association of liver fibrosis (as measured by Fibrosis-4 score) with cognitive functioning and regional grey matter volumes (GMVs) while adjusting for numerous covariates and multiple comparisons. We further performed post-hoc preliminary analysis to investigate the mediating effect of C-reactive protein (CRP) on the association between liver fibrosis and both cognitive functioning and GMVs. We analysed behaviour from up to 447,626 participants (N ranged from 45,055 to 447,533 per specific cognitive metric) 37 years and older. 38,244 participants (age range 44-82 years) had GMV data collected at a median 9-year follow-up. Liver fibrosis showed significant associations with cognitive performance in reasoning, working memory, visual memory, prospective memory, executive function, and processing speed. Subgroup analysis indicated larger effects sizes for symbol digital substitution but smaller effect sizes for trail making in middle-aged people than their old counterparts. Neuroimaging analyses revealed significant associations between liver fibrosis and reduced regional GMVs, primarily in the hippocampus, thalamus, ventral striatum, parahippocampal gyrus, brain stem, and cerebellum. CRP levels were significantly higher in adults with advanced liver fibrosis than those without, indicating an elevated systemic inflammation. Moreover, the serum CRP significantly mediated the effect of liver fibrosis on most cognitive measures and regional GMVs in the hippocampus and brain stem. This study provides a well-powered characterization of associations between liver fibrosis, cognitive impairment, and grey matter atrophy. It also highlights the possibly mediating role of systemic inflammation on the liver-brain axis. Early surveillance and prevention of liver diseases may reduce cognitive decline and brain GMV loss. National Science Foundation, and National Institutes of Health.

Sections du résumé

BACKGROUND BACKGROUND
Chronic liver diseases of all etiologies exist along a spectrum with varying degrees of hepatic fibrosis. Despite accumulating evidence implying associations between liver fibrosis and cognitive functioning, there is limited research exploring the underlying neurobiological factors and the possible mediating role of inflammation on the liver-brain axis.
METHODS METHODS
Using data from the UK Biobank, we examined the cross-sectional association of liver fibrosis (as measured by Fibrosis-4 score) with cognitive functioning and regional grey matter volumes (GMVs) while adjusting for numerous covariates and multiple comparisons. We further performed post-hoc preliminary analysis to investigate the mediating effect of C-reactive protein (CRP) on the association between liver fibrosis and both cognitive functioning and GMVs.
FINDINGS RESULTS
We analysed behaviour from up to 447,626 participants (N ranged from 45,055 to 447,533 per specific cognitive metric) 37 years and older. 38,244 participants (age range 44-82 years) had GMV data collected at a median 9-year follow-up. Liver fibrosis showed significant associations with cognitive performance in reasoning, working memory, visual memory, prospective memory, executive function, and processing speed. Subgroup analysis indicated larger effects sizes for symbol digital substitution but smaller effect sizes for trail making in middle-aged people than their old counterparts. Neuroimaging analyses revealed significant associations between liver fibrosis and reduced regional GMVs, primarily in the hippocampus, thalamus, ventral striatum, parahippocampal gyrus, brain stem, and cerebellum. CRP levels were significantly higher in adults with advanced liver fibrosis than those without, indicating an elevated systemic inflammation. Moreover, the serum CRP significantly mediated the effect of liver fibrosis on most cognitive measures and regional GMVs in the hippocampus and brain stem.
INTERPRETATION CONCLUSIONS
This study provides a well-powered characterization of associations between liver fibrosis, cognitive impairment, and grey matter atrophy. It also highlights the possibly mediating role of systemic inflammation on the liver-brain axis. Early surveillance and prevention of liver diseases may reduce cognitive decline and brain GMV loss.
FUNDING BACKGROUND
National Science Foundation, and National Institutes of Health.

Identifiants

pubmed: 37356206
pii: S2352-3964(23)00244-X
doi: 10.1016/j.ebiom.2023.104679
pmc: PMC10320521
pii:
doi:

Substances chimiques

C-Reactive Protein 9007-41-4

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104679

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Rongtao Jiang (R)

Department of Radiology and Biomedical Imaging, Yale School of Medicine, New Haven, CT 06510, USA. Electronic address: rongtao.jiang@yale.edu.

Jing Wu (J)

Second Department of Liver Disease Center, Youan Hospital, Capital Medical University, Beijing, 100069, China.

Matthew Rosenblatt (M)

Department of Biomedical Engineering, Yale University, New Haven, CT 06520, USA.

Wei Dai (W)

Department of Biostatistics, Yale University, New Haven, CT 06520, USA.

Raimundo X Rodriguez (RX)

Interdepartmental Neuroscience Program, Yale University, New Haven, CT 06520, USA.

Jing Sui (J)

State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, 100088, China.

Shile Qi (S)

Tri-institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS), Georgia State University, Georgia Institute of Technology, and Emory University, Atlanta, GA 30303, USA.

Qinghao Liang (Q)

Department of Biomedical Engineering, Yale University, New Haven, CT 06520, USA.

Bin Xu (B)

Second Department of Liver Disease Center, Youan Hospital, Capital Medical University, Beijing, 100069, China. Electronic address: xubin1016@ccmu.edu.cn.

Qinghua Meng (Q)

Department of Medical Oncology, Beijing You-An Hospital, Capital Medical University, Beijing, 100069, China.

Vince D Calhoun (VD)

Tri-institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS), Georgia State University, Georgia Institute of Technology, and Emory University, Atlanta, GA 30303, USA.

Dustin Scheinost (D)

Department of Radiology and Biomedical Imaging, Yale School of Medicine, New Haven, CT 06510, USA; Department of Biomedical Engineering, Yale University, New Haven, CT 06520, USA; Interdepartmental Neuroscience Program, Yale University, New Haven, CT 06520, USA; Department of Statistics & Data Science, Yale University, New Haven, CT 06520, USA; Child Study Center, Yale School of Medicine, New Haven, CT 06510, USA; Wu Tsai Institute, Yale University, 100 College Street, New Haven, CT 06510, USA. Electronic address: dustin.scheinost@yale.edu.

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