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Elevated plasma succinate levels are linked to higher cardiovascular disease risk factors in young adults

BACKGROUND: Succinate is produced by both host and microbiota, with a key role in the interplay of immunity and metabolism and an emerging role as a biomarker for inflammatory and metabolic disorders in middle-aged adults. The relationship between plasma succinate levels and cardiovascular disease (...

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Autores principales: Osuna-Prieto, Francisco J., Martinez-Tellez, Borja, Ortiz-Alvarez, Lourdes, Di, Xinyu, Jurado-Fasoli, Lucas, Xu, Huiwen, Ceperuelo-Mallafré, Victoria, Núñez-Roa, Catalina, Kohler, Isabelle, Segura-Carretero, Antonio, García-Lario, José V., Gil, Angel, Aguilera, Concepción M., Llamas-Elvira, Jose M., Rensen, Patrick C. N., Vendrell, Joan, Ruiz, Jonatan R., Fernández-Veledo, Sonia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8314524/
https://www.ncbi.nlm.nih.gov/pubmed/34315463
http://dx.doi.org/10.1186/s12933-021-01333-3
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author Osuna-Prieto, Francisco J.
Martinez-Tellez, Borja
Ortiz-Alvarez, Lourdes
Di, Xinyu
Jurado-Fasoli, Lucas
Xu, Huiwen
Ceperuelo-Mallafré, Victoria
Núñez-Roa, Catalina
Kohler, Isabelle
Segura-Carretero, Antonio
García-Lario, José V.
Gil, Angel
Aguilera, Concepción M.
Llamas-Elvira, Jose M.
Rensen, Patrick C. N.
Vendrell, Joan
Ruiz, Jonatan R.
Fernández-Veledo, Sonia
author_facet Osuna-Prieto, Francisco J.
Martinez-Tellez, Borja
Ortiz-Alvarez, Lourdes
Di, Xinyu
Jurado-Fasoli, Lucas
Xu, Huiwen
Ceperuelo-Mallafré, Victoria
Núñez-Roa, Catalina
Kohler, Isabelle
Segura-Carretero, Antonio
García-Lario, José V.
Gil, Angel
Aguilera, Concepción M.
Llamas-Elvira, Jose M.
Rensen, Patrick C. N.
Vendrell, Joan
Ruiz, Jonatan R.
Fernández-Veledo, Sonia
author_sort Osuna-Prieto, Francisco J.
collection PubMed
description BACKGROUND: Succinate is produced by both host and microbiota, with a key role in the interplay of immunity and metabolism and an emerging role as a biomarker for inflammatory and metabolic disorders in middle-aged adults. The relationship between plasma succinate levels and cardiovascular disease (CVD) risk in young adults is unknown. METHODS: Cross-sectional study in 100 (65% women) individuals aged 18–25 years from the ACTIvating Brown Adipose Tissue through Exercise (ACTIBATE) study cohort. CVD risk factors, body composition, dietary intake, basal metabolic rate, and cardiorespiratory fitness were assessed by routine methods. Plasma succinate was measured with an enzyme-based assay. Brown adipose tissue (BAT) was evaluated by positron emission tomography, and circulating oxylipins were assessed by targeted metabolomics. Fecal microbiota composition was analyzed in a sub-sample. RESULTS: Individuals with higher succinate levels had higher levels of visceral adipose tissue (VAT) mass (+ 42.5%), triglycerides (+ 63.9%), C-reactive protein (+ 124.2%), diastolic blood pressure (+ 5.5%), and pro-inflammatory omega-6 oxylipins than individuals with lower succinate levels. Succinate levels were also higher in metabolically unhealthy individuals than in healthy overweight/obese peers. Succinate levels were not associated with BAT volume or activity or with fecal microbiota composition and diversity. CONCLUSIONS: Plasma succinate levels are linked to a specific pro-inflammatory omega-6 signature pattern and higher VAT levels, and seem to reflect the cardiovascular status of young adults. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12933-021-01333-3.
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spelling pubmed-83145242021-07-28 Elevated plasma succinate levels are linked to higher cardiovascular disease risk factors in young adults Osuna-Prieto, Francisco J. Martinez-Tellez, Borja Ortiz-Alvarez, Lourdes Di, Xinyu Jurado-Fasoli, Lucas Xu, Huiwen Ceperuelo-Mallafré, Victoria Núñez-Roa, Catalina Kohler, Isabelle Segura-Carretero, Antonio García-Lario, José V. Gil, Angel Aguilera, Concepción M. Llamas-Elvira, Jose M. Rensen, Patrick C. N. Vendrell, Joan Ruiz, Jonatan R. Fernández-Veledo, Sonia Cardiovasc Diabetol Original Investigation BACKGROUND: Succinate is produced by both host and microbiota, with a key role in the interplay of immunity and metabolism and an emerging role as a biomarker for inflammatory and metabolic disorders in middle-aged adults. The relationship between plasma succinate levels and cardiovascular disease (CVD) risk in young adults is unknown. METHODS: Cross-sectional study in 100 (65% women) individuals aged 18–25 years from the ACTIvating Brown Adipose Tissue through Exercise (ACTIBATE) study cohort. CVD risk factors, body composition, dietary intake, basal metabolic rate, and cardiorespiratory fitness were assessed by routine methods. Plasma succinate was measured with an enzyme-based assay. Brown adipose tissue (BAT) was evaluated by positron emission tomography, and circulating oxylipins were assessed by targeted metabolomics. Fecal microbiota composition was analyzed in a sub-sample. RESULTS: Individuals with higher succinate levels had higher levels of visceral adipose tissue (VAT) mass (+ 42.5%), triglycerides (+ 63.9%), C-reactive protein (+ 124.2%), diastolic blood pressure (+ 5.5%), and pro-inflammatory omega-6 oxylipins than individuals with lower succinate levels. Succinate levels were also higher in metabolically unhealthy individuals than in healthy overweight/obese peers. Succinate levels were not associated with BAT volume or activity or with fecal microbiota composition and diversity. CONCLUSIONS: Plasma succinate levels are linked to a specific pro-inflammatory omega-6 signature pattern and higher VAT levels, and seem to reflect the cardiovascular status of young adults. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12933-021-01333-3. BioMed Central 2021-07-27 /pmc/articles/PMC8314524/ /pubmed/34315463 http://dx.doi.org/10.1186/s12933-021-01333-3 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Original Investigation
Osuna-Prieto, Francisco J.
Martinez-Tellez, Borja
Ortiz-Alvarez, Lourdes
Di, Xinyu
Jurado-Fasoli, Lucas
Xu, Huiwen
Ceperuelo-Mallafré, Victoria
Núñez-Roa, Catalina
Kohler, Isabelle
Segura-Carretero, Antonio
García-Lario, José V.
Gil, Angel
Aguilera, Concepción M.
Llamas-Elvira, Jose M.
Rensen, Patrick C. N.
Vendrell, Joan
Ruiz, Jonatan R.
Fernández-Veledo, Sonia
Elevated plasma succinate levels are linked to higher cardiovascular disease risk factors in young adults
title Elevated plasma succinate levels are linked to higher cardiovascular disease risk factors in young adults
title_full Elevated plasma succinate levels are linked to higher cardiovascular disease risk factors in young adults
title_fullStr Elevated plasma succinate levels are linked to higher cardiovascular disease risk factors in young adults
title_full_unstemmed Elevated plasma succinate levels are linked to higher cardiovascular disease risk factors in young adults
title_short Elevated plasma succinate levels are linked to higher cardiovascular disease risk factors in young adults
title_sort elevated plasma succinate levels are linked to higher cardiovascular disease risk factors in young adults
topic Original Investigation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8314524/
https://www.ncbi.nlm.nih.gov/pubmed/34315463
http://dx.doi.org/10.1186/s12933-021-01333-3
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