Exploration of the Gut–Brain Axis through Metabolomics Identifies Serum Propionic Acid Associated with Higher Cognitive Decline in Older Persons
Open accessAbstract
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.
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A positive association exists between serum propionic acid and cognitive decline in older adults, with potential mediation by hypercholesterolemia and diabetes.
“A recent population-based study has revealed a positive association between serum propionic acid and cognitive decline in older adults, with potential mediation by hypercholesterolemia and diabetes.307”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [307]
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- Authors
- Neuffer, J., González-Domínguez, R., Lefèvre-Arbogast, S., Low, D. Y., Driollet, B., Helmer, C., Du Preez, A., de Lucia, C., Ruigrok, S. R., Altendorfer, B., Aigner, L., Lucassen, P. J., Korosi, A., Thuret, S., Manach, C., Pallàs, M., Urpi-Sardà, M., Sánchez-Pla, A., Andres-Lacueva, C., & Samieri, C.
- Affiliations
- Université de Bordeaux (FR)
- Nutrition, Food Science and Gastronomy Department, Food Innovation Network (XIA), Institute of Nutrition and Food Safety (INSA-UB), Faculty of Pharmacy and Food Science, University of Barcelona, 08028 Barcelona, Spain
- Bordeaux Population Health Research Center, University of Bordeaux, INSERMUMR 1219, F-33000 Bordeaux, France
- Nanyang Technological University (SG)
- Department of Basic and Clinical Neuroscience, Maurice Wohl Clinical Neuroscience Institute, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London SE5 9NU, UK
- University of Amsterdam (NL)
- Paracelsus Medical University (AT)
- Brain Plasticity Group, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098 XH Amsterdam, The Netherlands
- King's College London (GB)
- Université Clermont Auvergne (FR)
- Universitat de Barcelona (ES)
- Corresponding author
- Neuffer, Jeanne
- ORCID
- 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.
- Thuret, Sandrine
- Manach, Claudine
- Pallàs, Mercè
- Urpi-Sardà, Mireia
- Andres-Lacueva, Cristina
- Samieri, Cécilia
- Venue
- Nutrients
- Publisher
- MDPI AG
- Published
- 2022-11-05
- Volume
- 14
- Issue
- 21
- Pages
- 4688
- ISSN
- 2072-6643 (ISSN-L)
- PMC
- PMC9655149
- OpenAlex
- W4308442050
- Cited by
- 40
- References
- 70
- Citations by year
- 2026: 8 · 2025: 11 · 2024: 12 · 2023: 8 · 2022: 1
- FWCI
- 2.61
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Nutrients (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (publishedVersion, cc-by)
- Pure Amsterdam UMC (acceptedVersion, cc-by)
- Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (submittedVersion, cc-by)
- HAL (submittedVersion, cc-by)
- Research Portal (King's College London) (submittedVersion, cc-by)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- DR-NTU (Nanyang Technological University) (submittedVersion)
- Oskar-Bordeaux (Universite de Bordeaux) (submittedVersion, cc-by)
- Funders
- the Institut National de la Santé et de la Recherche Médicale (INSERM), the Institut de Santé Publique, Epidémiologie et Développement of the University of Bordeaux and Sanofi-Aventis
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Keywords
- gut-brain axis, propionic acid, short-chain fatty acids, cognitive decline, older adults, gut microbiota, serum metabolites, hypercholesterolemia, diabetes mellitus, blood glucose, prebiotic foods, cognitive aging
- MeSH terms
- Brain-Gut Axis, Aged, Aged, 80 and over, Humans, Propionates, Case-Control Studies, Metabolomics, Cognitive Dysfunction
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