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Exploration of the Gut–Brain Axis through Metabolomics Identifies Serum Propionic Acid Associated with Higher Cognitive Decline in Older Persons
The gut microbiome is involved in nutrient metabolism and produces metabolites that, via the gut–brain axis, signal to the brain and influence cognition. Human studies have so far had limited success in identifying early metabolic alterations linked to cognitive aging, likely due to limitations in m...
Autores principales: | , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
MDPI
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9655149/ https://www.ncbi.nlm.nih.gov/pubmed/36364950 http://dx.doi.org/10.3390/nu14214688 |
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author | Neuffer, Jeanne González-Domínguez, Raúl Lefèvre-Arbogast, Sophie Low, Dorrain Y. Driollet, Bénédicte Helmer, Catherine Du Preez, Andrea de Lucia, Chiara Ruigrok, Silvie R. Altendorfer, Barbara Aigner, Ludwig Lucassen, Paul J. Korosi, Aniko Thuret, Sandrine Manach, Claudine Pallàs, Mercè Urpi-Sardà, Mireia Sánchez-Pla, Alex Andres-Lacueva, Cristina Samieri, Cécilia |
author_facet | Neuffer, Jeanne González-Domínguez, Raúl Lefèvre-Arbogast, Sophie Low, Dorrain Y. Driollet, Bénédicte Helmer, Catherine Du Preez, Andrea de Lucia, Chiara Ruigrok, Silvie R. Altendorfer, Barbara Aigner, Ludwig Lucassen, Paul J. Korosi, Aniko Thuret, Sandrine Manach, Claudine Pallàs, Mercè Urpi-Sardà, Mireia Sánchez-Pla, Alex Andres-Lacueva, Cristina Samieri, Cécilia |
author_sort | Neuffer, Jeanne |
collection | PubMed |
description | The gut microbiome is involved in nutrient metabolism and produces metabolites that, via the gut–brain axis, signal to the brain and influence cognition. Human studies have so far had limited success in identifying early metabolic alterations linked to cognitive aging, likely due to limitations in metabolite coverage or follow-ups. Older persons from the Three-City population-based cohort who had not been diagnosed with dementia at the time of blood sampling were included, and repeated measures of cognition over 12 subsequent years were collected. Using a targeted metabolomics platform, we identified 72 circulating gut-derived metabolites in a case–control study on cognitive decline, nested within the cohort (discovery n = 418; validation n = 420). Higher serum levels of propionic acid, a short-chain fatty acid, were associated with increased odds of cognitive decline (OR for 1 SD = 1.40 (95% CI 1.11, 1.75) for discovery and 1.26 (1.02, 1.55) for validation). Additional analyses suggested mediation by hypercholesterolemia and diabetes. Propionic acid strongly correlated with blood glucose (r = 0.79) and with intakes of meat and cheese (r > 0.15), but not fiber (r = 0.04), suggesting a minor role of prebiotic foods per se, but a possible link to processed foods, in which propionic acid is a common preservative. The adverse impact of propionic acid on metabolism and cognition deserves further investigation. |
format | Online Article Text |
id | pubmed-9655149 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | MDPI |
record_format | MEDLINE/PubMed |
spelling | pubmed-96551492022-11-15 Exploration of the Gut–Brain Axis through Metabolomics Identifies Serum Propionic Acid Associated with Higher Cognitive Decline in Older Persons Neuffer, Jeanne González-Domínguez, Raúl Lefèvre-Arbogast, Sophie Low, Dorrain Y. Driollet, Bénédicte Helmer, Catherine Du Preez, Andrea de Lucia, Chiara Ruigrok, Silvie R. Altendorfer, Barbara Aigner, Ludwig Lucassen, Paul J. Korosi, Aniko Thuret, Sandrine Manach, Claudine Pallàs, Mercè Urpi-Sardà, Mireia Sánchez-Pla, Alex Andres-Lacueva, Cristina Samieri, Cécilia Nutrients Article The gut microbiome is involved in nutrient metabolism and produces metabolites that, via the gut–brain axis, signal to the brain and influence cognition. Human studies have so far had limited success in identifying early metabolic alterations linked to cognitive aging, likely due to limitations in metabolite coverage or follow-ups. Older persons from the Three-City population-based cohort who had not been diagnosed with dementia at the time of blood sampling were included, and repeated measures of cognition over 12 subsequent years were collected. Using a targeted metabolomics platform, we identified 72 circulating gut-derived metabolites in a case–control study on cognitive decline, nested within the cohort (discovery n = 418; validation n = 420). Higher serum levels of propionic acid, a short-chain fatty acid, were associated with increased odds of cognitive decline (OR for 1 SD = 1.40 (95% CI 1.11, 1.75) for discovery and 1.26 (1.02, 1.55) for validation). Additional analyses suggested mediation by hypercholesterolemia and diabetes. Propionic acid strongly correlated with blood glucose (r = 0.79) and with intakes of meat and cheese (r > 0.15), but not fiber (r = 0.04), suggesting a minor role of prebiotic foods per se, but a possible link to processed foods, in which propionic acid is a common preservative. The adverse impact of propionic acid on metabolism and cognition deserves further investigation. MDPI 2022-11-05 /pmc/articles/PMC9655149/ /pubmed/36364950 http://dx.doi.org/10.3390/nu14214688 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). |
spellingShingle | Article Neuffer, Jeanne González-Domínguez, Raúl Lefèvre-Arbogast, Sophie Low, Dorrain Y. Driollet, Bénédicte Helmer, Catherine Du Preez, Andrea de Lucia, Chiara Ruigrok, Silvie R. Altendorfer, Barbara Aigner, Ludwig Lucassen, Paul J. Korosi, Aniko Thuret, Sandrine Manach, Claudine Pallàs, Mercè Urpi-Sardà, Mireia Sánchez-Pla, Alex Andres-Lacueva, Cristina Samieri, Cécilia Exploration of the Gut–Brain Axis through Metabolomics Identifies Serum Propionic Acid Associated with Higher Cognitive Decline in Older Persons |
title | Exploration of the Gut–Brain Axis through Metabolomics Identifies Serum Propionic Acid Associated with Higher Cognitive Decline in Older Persons |
title_full | Exploration of the Gut–Brain Axis through Metabolomics Identifies Serum Propionic Acid Associated with Higher Cognitive Decline in Older Persons |
title_fullStr | Exploration of the Gut–Brain Axis through Metabolomics Identifies Serum Propionic Acid Associated with Higher Cognitive Decline in Older Persons |
title_full_unstemmed | Exploration of the Gut–Brain Axis through Metabolomics Identifies Serum Propionic Acid Associated with Higher Cognitive Decline in Older Persons |
title_short | Exploration of the Gut–Brain Axis through Metabolomics Identifies Serum Propionic Acid Associated with Higher Cognitive Decline in Older Persons |
title_sort | exploration of the gut–brain axis through metabolomics identifies serum propionic acid associated with higher cognitive decline in older persons |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9655149/ https://www.ncbi.nlm.nih.gov/pubmed/36364950 http://dx.doi.org/10.3390/nu14214688 |
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