Comprehensive Metabolic Profiling of Inflammation Indicated Key Roles of Glycerophospholipid and Arginine Metabolism in Coronary Artery Disease

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Abstract

Background

Systemic immune inflammation is a key mediator in the progression of coronary artery disease (CAD), concerning various metabolic and lipid changes. In this study, the relationship between the inflammatory index and metabolic profile in patients with CAD was investigated to provide deep insights into metabolic disturbances related to inflammation.

Methods

Widely targeted plasma metabolomic and lipidomic profiling was performed in 1,234 patients with CAD. Laboratory circulating inflammatory markers were mainly used to define general systemic immune and low-grade inflammatory states. Multivariable-adjusted linear regression was adopted to assess the associations between 860 metabolites and 7 inflammatory markers. Least absolute shrinkage and selection operator (LASSO) logistic-based classifiers and multivariable logistic regression were applied to identify biomarkers of inflammatory states and develop models for discriminating an advanced inflammatory state.

Results

Multiple metabolites and lipid species were linearly associated with the seven inflammatory markers [false discovery rate (FDR) <0.05]. LASSO and multivariable-adjusted logistic regression analysis identified significant associations between 45 metabolites and systemic immune-inflammation index, 46 metabolites and neutrophil–lymphocyte ratio states, 32 metabolites and low-grade inflammation score, and 26 metabolites and high-sensitivity C-reactive protein states ( P < 0.05). Glycerophospholipid metabolism and arginine and proline metabolism were determined as key altered metabolic pathways for systemic immune and low-grade inflammatory states. Predictive models based solely on metabolite combinations showed feasibility (area under the curve: 0.81 to 0.88) for discriminating the four parameters that represent inflammatory states and were successfully validated using a validation cohort. The inflammation-associated metabolite, namely, β-pseudouridine, was related to carotid and coronary arteriosclerosis indicators ( P < 0.05).

Conclusions

This study provides further information on the relationship between plasma metabolite profiles and inflammatory states represented by various inflammatory markers in CAD. These metabolic markers provide potential insights into pathological changes during CAD progression and may aid in the development of therapeutic targets.

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Author and article information

Contributors

Qian Zhu: URI : https://loop.frontiersin.org/people/789640

Yonglin Wu: URI : https://loop.frontiersin.org/people/1306485

Xianhong Fang: URI : https://loop.frontiersin.org/people/1321721

Xiaoping Chen: URI : https://loop.frontiersin.org/people/525420

Chen Liu: URI : https://loop.frontiersin.org/people/729429

Shilong Zhong: URI : https://loop.frontiersin.org/people/321660

Journal

Journal ID (nlm-ta): Front Immunol

Journal ID (iso-abbrev): Front Immunol

Journal ID (publisher-id): Front. Immunol.

Title: Frontiers in Immunology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1664-3224

Publication date (Electronic): 08 March 2022

Publication date Collection: 2022

Publication date PMC-release: 08 March 2022

Volume: 13

Electronic Location Identifier: 829425

Affiliations

[1] ¹School of Medicine, South China University of Technology , Guangzhou, China

[2] ²Department of Pharmacy, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences , Guangzhou, China

[3] ³School of Pharmaceutical Sciences, Southern Medical University , Guangzhou, China

[4] ⁴Guangdong Provincial Key Laboratory of Coronary Heart Disease Prevention, Guangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences , Guangzhou, China

[5] ⁵Department of Cardiology, Guangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences , Guangzhou, China

[6] ⁶Department of Clinical Pharmacology, Xiangya Hospital, Central South University , Changsha, China

[7] ⁷Department of Cardiology, The First Affiliated Hospital of Sun Yat-sen University , Guangzhou, China

Author notes

Edited by: Huaizhu Wu, Baylor College of Medicine, United States

Reviewed by: Changcheng Zhou, University of California, Riverside, United States; Zeqin Lian, Baylor College of Medicine, United States

*Correspondence: Shilong Zhong, gdph_zhongsl@ 123456gd.gov.cn

This article was submitted to Inflammation, a section of the journal Frontiers in Immunology

Article

DOI: 10.3389/fimmu.2022.829425

PMC ID: 8965586

PubMed ID: 35371012

SO-VID: 470bcd00-f5f8-4a6d-917c-fadd0f77dc88

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 05 December 2021

Date accepted : 31 January 2022

Page count

Figures: 6, Tables: 1, Equations: 0, References: 78, Pages: 16, Words: 8050

Funding

Funded by: National Natural Science Foundation of China , doi 10.13039/501100001809;

Comprehensive Metabolic Profiling of Inflammation Indicated Key Roles of Glycerophospholipid and Arginine Metabolism in Coronary Artery Disease

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Abstract

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Conclusions

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Cardiovascular Innovations and Applications

Most cited references 78

Heart Disease and Stroke Statistics—2017 Update: A Report From the American Heart Association

Markers of Inflammation and Cardiovascular Disease: Application to Clinical and Public Health Practice: A Statement for Healthcare Professionals From the Centers for Disease Control and Prevention and the American Heart Association

Systemic immune-inflammation index predicts prognosis of patients after curative resection for hepatocellular carcinoma.

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