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...
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MDPI AG
2022-11-01
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| Series: | Nutrients |
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| Online Access: | https://www.mdpi.com/2072-6643/14/21/4688 |
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| author | Jeanne Neuffer Raúl González-Domínguez Sophie Lefèvre-Arbogast Dorrain Y. Low Bénédicte Driollet Catherine Helmer Andrea Du Preez Chiara de Lucia Silvie R. Ruigrok Barbara Altendorfer Ludwig Aigner Paul J. Lucassen Aniko Korosi Sandrine Thuret Claudine Manach Mercè Pallàs Mireia Urpi-Sardà Alex Sánchez-Pla Cristina Andres-Lacueva Cécilia Samieri |
| author_facet | Jeanne Neuffer Raúl González-Domínguez Sophie Lefèvre-Arbogast Dorrain Y. Low Bénédicte Driollet Catherine Helmer Andrea Du Preez Chiara de Lucia Silvie R. Ruigrok Barbara Altendorfer Ludwig Aigner Paul J. Lucassen Aniko Korosi Sandrine Thuret Claudine Manach Mercè Pallàs Mireia Urpi-Sardà Alex Sánchez-Pla Cristina Andres-Lacueva Cécilia Samieri |
| author_sort | Jeanne Neuffer |
| collection | DOAJ |
| 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 <i>n</i> = 418; validation <i>n</i> = 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. |
| first_indexed | 2024-03-09T18:46:31Z |
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| id | doaj.art-e9901464fcbf4a7581dfda0fb758ef41 |
| institution | Directory Open Access Journal |
| issn | 2072-6643 |
| language | English |
| last_indexed | 2024-03-09T18:46:31Z |
| publishDate | 2022-11-01 |
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| record_format | Article |
| series | Nutrients |
| spelling | doaj.art-e9901464fcbf4a7581dfda0fb758ef412023-11-24T06:15:40ZengMDPI AGNutrients2072-66432022-11-011421468810.3390/nu14214688Exploration of the Gut–Brain Axis through Metabolomics Identifies Serum Propionic Acid Associated with Higher Cognitive Decline in Older PersonsJeanne Neuffer0Raúl González-Domínguez1Sophie Lefèvre-Arbogast2Dorrain Y. Low3Bénédicte Driollet4Catherine Helmer5Andrea Du Preez6Chiara de Lucia7Silvie R. Ruigrok8Barbara Altendorfer9Ludwig Aigner10Paul J. Lucassen11Aniko Korosi12Sandrine Thuret13Claudine Manach14Mercè Pallàs15Mireia Urpi-Sardà16Alex Sánchez-Pla17Cristina Andres-Lacueva18Cécilia Samieri19Bordeaux Population Health Research Center, University of Bordeaux, INSERMUMR 1219, F-33000 Bordeaux, FranceNutrition, 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, SpainBordeaux Population Health Research Center, University of Bordeaux, INSERMUMR 1219, F-33000 Bordeaux, FranceHuman Nutrition Unit, Université Clermont Auvergne, INRAEUMR1019, F-63000 Clermont Ferrand, FranceBordeaux Population Health Research Center, University of Bordeaux, INSERMUMR 1219, F-33000 Bordeaux, FranceBordeaux Population Health Research Center, University of Bordeaux, INSERMUMR 1219, F-33000 Bordeaux, FranceDepartment of Basic and Clinical Neuroscience, Maurice Wohl Clinical Neuroscience Institute, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London SE5 9NU, UKDepartment of Basic and Clinical Neuroscience, Maurice Wohl Clinical Neuroscience Institute, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London SE5 9NU, UKBrain Plasticity Group, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098 XH Amsterdam, The NetherlandsInstitute of Molecular Regenerative Medicine, Spinal Cord Injury and Tissue Regeneration Center Salzburg, Paracelsus Medical University, 5020 Salzburg, AustriaInstitute of Molecular Regenerative Medicine, Spinal Cord Injury and Tissue Regeneration Center Salzburg, Paracelsus Medical University, 5020 Salzburg, AustriaBrain Plasticity Group, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098 XH Amsterdam, The NetherlandsBrain Plasticity Group, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098 XH Amsterdam, The NetherlandsDepartment of Basic and Clinical Neuroscience, Maurice Wohl Clinical Neuroscience Institute, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London SE5 9NU, UKHuman Nutrition Unit, Université Clermont Auvergne, INRAEUMR1019, F-63000 Clermont Ferrand, FrancePharmacology Section, Department of Pharmacology, Toxicology and Medicinal Chemistry, Faculty of Pharmacy and Food Sciences, and Institute of Neurociencies, University of Barcelona, 08028 Barcelona, SpainNutrition, 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, SpainNutrition, 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, SpainNutrition, 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, SpainBordeaux Population Health Research Center, University of Bordeaux, INSERMUMR 1219, F-33000 Bordeaux, FranceThe 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 <i>n</i> = 418; validation <i>n</i> = 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.https://www.mdpi.com/2072-6643/14/21/4688propionic acidgut microbiotametabolomicscognitive declinegut–brain axisAlzheimer’s disease |
| spellingShingle | Jeanne Neuffer Raúl González-Domínguez Sophie Lefèvre-Arbogast Dorrain Y. Low Bénédicte Driollet Catherine Helmer Andrea Du Preez Chiara de Lucia Silvie R. Ruigrok Barbara Altendorfer Ludwig Aigner Paul J. Lucassen Aniko Korosi Sandrine Thuret Claudine Manach Mercè Pallàs Mireia Urpi-Sardà Alex Sánchez-Pla Cristina Andres-Lacueva Cécilia Samieri Exploration of the Gut–Brain Axis through Metabolomics Identifies Serum Propionic Acid Associated with Higher Cognitive Decline in Older Persons Nutrients propionic acid gut microbiota metabolomics cognitive decline gut–brain axis Alzheimer’s disease |
| 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 | propionic acid gut microbiota metabolomics cognitive decline gut–brain axis Alzheimer’s disease |
| url | https://www.mdpi.com/2072-6643/14/21/4688 |
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