Mediterranean Diet intervention alters the gut microbiome in older people reducing frailty and improving health status: the NU-AGE 1-year dietary intervention across five European countries
Open accessAbstract
OBJECTIVE: Ageing is accompanied by deterioration of multiple bodily functions and inflammation, which collectively contribute to frailty. We and others have shown that frailty co-varies with alterations in the gut microbiota in a manner accelerated by consumption of a restricted diversity diet. The Mediterranean diet (MedDiet) is associated with health. In the NU-AGE project, we investigated if a 1-year MedDiet intervention could alter the gut microbiota and reduce frailty. DESIGN: We profiled the gut microbiota in 612 non-frail or pre-frail subjects across five European countries (UK, France, Netherlands, Italy and Poland) before and after the administration of a 12-month long MedDiet intervention tailored to elderly subjects (NU-AGE diet). RESULTS: Adherence to the diet was associated with specific microbiome alterations. Taxa enriched by adherence to the diet were positively associated with several markers of lower frailty and improved cognitive function, and negatively associated with inflammatory markers including C-reactive protein and interleukin-17. Analysis of the inferred microbial metabolite profiles indicated that the diet-modulated microbiome change was associated with an increase in short/branch chained fatty acid production and lower production of secondary bile acids, p-cresols, ethanol and carbon dioxide. Microbiome ecosystem network analysis showed that the bacterial taxa that responded positively to the MedDiet intervention occupy keystone interaction positions, whereas frailty-associated taxa are peripheral in the networks. CONCLUSION: Collectively, our findings support the feasibility of improving the habitual diet to modulate the gut microbiota which in turn has the potential to promote healthier ageing.
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The microbiome appears to be influenced by diet.
“the microbiome appears to be influenced by exercise 118 and diet 119”
From A meta-review of "lifestyle psychiatry": the role of exercise, smoking, diet and sleep in the prevention and treatment of mental disorders (2020) · cites this paper as [119]
A significant body of evidence demonstrates that consuming a GM-favorable diet can positively influence the GM, improve health status, and enhance cognitive function.
“A comprehensive review of this topic is beyond the scope of this review, however, a significant body of evidence demonstrates that consuming a GM-favorable diet can positively influence the GM, improve health status, and enhance cognitive function (506–510).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [508]
The positive effects of a GM-favorable diet are likely due to the availability of prebiotics, probiotics, SCFAs, and polyphenols.
“This is likely due to the availability of prebiotics, probiotics, SCFAs, and polyphenols.”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [508]
Large epidemiological studies have implicated dietary factors in some psychiatric disorders as risk factors and potential therapies.
“a number of large epidemiological studies have implicated dietary factors in some of these disorders [1–5], both in terms of risk factors [6] as well as potential therapies [2, 5, 7].”
From Role of diet and its effects on the gut microbiome in the pathophysiology of mental disorders (2022) · cites this paper as [6]
Mediterranean-like diets can promote healthy brain function as demonstrated in a variety of dietary intervention trials in depression and in cognitive decline.
“Such Mediterranean-like diets can promote healthy brain function as demonstrated in a variety of dietary intervention trials in depression and in cognitive decline [1–3, 6].”
From Role of diet and its effects on the gut microbiome in the pathophysiology of mental disorders (2022) · cites this paper as [6]
In the NUAGE study, dietary adherence to a Mediterranean diet was correlated with specific bacterial taxa which were negatively associated with inflammatory markers and also positively associated with markers of low frailty.
“Results of this study showed that dietary adherence to a Mediterranean diet was correlated with specific bacterial taxa which were negatively associated with inflammatory markers and also positively associated with markers of low frailty.”
From Role of diet and its effects on the gut microbiome in the pathophysiology of mental disorders (2022) · cites this paper as [6]
In the human NU-AGE cohort, adherence to the Mediterranean diet in elderly subjects was associated with microbial taxa that were positively correlated with markers of healthy aging, including improved cognitive function.
“In the human European Project on Nutrition in Elderly People (NU-AGE) cohort, adherence to the Mediterranean diet in elderly subjects was associated with microbial taxa that were positively correlated with markers of healthy aging, including improved cognitive function (300).”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [300]
In the NU-AGE cohort, Mediterranean diet-induced increases in microbial taxa were associated with improved cognition and reduced risk of frailty and inflammation in elderly individuals who followed a customized Mediterranean diet for 12 months.
“In the NU-AGE cohort, Mediterranean diet-induced increases in microbial taxa were associated with improved cognition and reduced risk of frailty and inflammation in elderly individuals who followed a customized Mediterranean diet for 12 mo (300).”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [300]
Consumption of a diet high in fibres, polyphenols, and unsaturated fatty acids can promote gut microbial taxa which can metabolise these food sources into anti-inflammatory metabolites, such as short chain fatty acids, while lowering the production of secondary bile acids and p-cresol.
“Conversely, the consumption of a diet high in fibres, polyphenols, and unsaturated fatty acids (as found in a Mediterranean diet) can promote gut microbial taxa which can metabolise these food sources into anti-inflammatory metabolites,15 28 such as short chain fatty acids, while lowering the production of secondary bile acids and p-cresol.”
From Food and mood: How do diet and nutrition affect mental wellbeing? (2020) · cites this paper as [28]
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RetractedThe Gut Microbiota and Unhealthy Aging: Disentangling Cause from Consequence
DeJong, E. N., Surette, M. G., & Bowdish, D. M. E. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.07.013 · Cited by 370 · see citing works
Wenzel, T. J., Gates, E. J., Ranger, A. L., & Klegeris, A. (2020) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2020.103493 · Cited by 320 · see citing works
From gut microbiota to host appetite: gut microbiota-derived metabolites as key regulators
Han, H., Yi, B., Zhong, R., Wang, M., Zhang, S., Ma, J., Yin, Y., Yin, J., Chen, L., & Zhang, H. (2021) · Microbiome · doi:10.1186/s40168-021-01093-y · Cited by 292 · see citing works
Rethinking healthy eating in light of the gut microbiome
Armet, A. M., Deehan, E. C., O’Sullivan, A. F., Mota, J. F., Field, C. J., Prado, C. M., Lucey, A. J., & Walter, J. (2022) · Cell Host & Microbe · doi:10.1016/j.chom.2022.04.016 · Cited by 252 · see citing works
Billot, M., Calvani, R., Urtamo, A., Sánchez-Sánchez, J. L., Ciccolari-Micaldi, C., Chang, M., Roller-Wirnsberger, R., Wirnsberger, G., Sinclair, A., Vaquero-Pinto, M. N., et al. (2020) · Clinical Interventions in Aging · doi:10.2147/cia.s253535 · Cited by 242 · see citing works
Adjusting for age improves identification of gut microbiome alterations in multiple diseases
Ghosh, T. S., Das, M., Jeffery, I. B., & O'Toole, P. W. (2020) · eLife · doi:10.7554/elife.50240 · Cited by 233 · see citing works
Self-citationThe Potential Role of Gut Microbiota in Alzheimer’s Disease: From Diagnosis to Treatment
Varesi, A., Pierella, E., Romeo, M., Piccini, G. B., Alfano, C., Bjørklund, G., Oppong, A., Ricevuti, G., Esposito, C., Chirumbolo, S., et al. (2022) · Nutrients · doi:10.3390/nu14030668 · Cited by 225 · see citing works
Role of diet and its effects on the gut microbiome in the pathophysiology of mental disorders
Horn, J., Mayer, D. E., Chen, S., & Mayer, E. A. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-01922-0 · Cited by 193 · see citing works
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Berding, K., Bastiaanssen, T. F. S., Moloney, G. M., Boscaini, S., Strain, C. R., Anesi, A., Long-Smith, C., Mattivi, F., Stanton, C., Clarke, G., et al. (2023) · Molecular Psychiatry · doi:10.1038/s41380-022-01817-y · Cited by 153 · see citing works
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- Authors
- Ghosh, T. S., Rampelli, S., Jeffery, I. B., Santoro, A., Neto, M., Capri, M., Giampieri, E., Jennings, A., Candela, M., Turroni, S., Zoetendal, E. G., Hermes, G. D. A., Elodie, C., Meunier, N., Brugere, C. M., Pujos-Guillot, E., Berendsen, A. M., De Groot, L. C. P. G. M., Feskins, E. J. M., Kaluza, J., Pietruszka, B., Bielak, M. J., Comte, B., Maijo-Ferre, M., Nicoletti, C., De Vos, W. M., Fairweather-Tait, S., Cassidy, A., Brigidi, P., Franceschi, C., & O'Toole, P. W.
- Affiliations
- University College Cork (IE)
- University of Bologna (IT)
- University of East Anglia (GB)
- Wageningen University & Research (NL)
- Centre de Recherche en Nutrition Humaine d'Auvergne (FR)
- Warsaw University of Life Sciences (PL)
- Université Clermont Auvergne (FR)
- Quadram Institute (GB)
- N. I. Lobachevsky State University of Nizhny Novgorod (RU)
- ORCID
- Ghosh, Tarini Shankar
- Rampelli, Simone
- Jeffery, Ian B
- Santoro, Aurelia
- Neto, Marta
- Capri, Miriam
- Giampieri, Enrico
- Jennings, Amy
- Candela, Marco
- Turroni, Silvia
- Zoetendal, Erwin G
- Hermes, Gerben D A
- Meunier, Nathalie
- Kaluza, Joanna
- Pietruszka, Barbara
- Comte, Blandine
- Nicoletti, Claudio
- Brigidi, Patrizia
- Franceschi, Claudio
- O'Toole, Paul W
- Venue
- Gut
- Publisher
- BMJ
- Published
- 2020-02-17
- Volume
- 69
- Issue
- 7
- Pages
- 1218-1228
- ISSN
- 0017-5749 (ISSN-L)
- 1468-3288
- PMC
- PMC7306987
- OpenAlex
- W3002445804
- Cited by
- 991
- References
- 63
- Citations by year
- 2026: 148 · 2025: 185 · 2024: 196 · 2023: 152 · 2022: 112 · 2021: 123 · 2020: 72
- FWCI
- 37.23
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Gut (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- UEA Digital Repository (University of East Anglia) (acceptedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion, cc-by-nc)
- HAL (submittedVersion, cc-by)
- Florence Research (University of Florence) (submittedVersion, other-oa)
- Research Portal (Queen's University Belfast) (submittedVersion, cc-by-nc)
- Lenus, The Irish Health Repository (Dr Steevens Hospital Library) (submittedVersion, cc-by-nc)
- Institutional Research Information System (University of Udine) (submittedVersion, cc-by-nc-nd)
- Institutional Research Information System (University of Udine) (submittedVersion)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion, cc-by-nc)
- Työväentutkimus Vuosikirja (submittedVersion)
- HighWire Press Open Archive (submittedVersion)
- Use Siena air (University of Siena) (submittedVersion, cc-by-nc)
- Data Archiving and Networked Services (DANS) (submittedVersion, cc-by-nc)
- Funders
- Science Foundation Ireland (13/SIRG/2128, APC/SFI/12/RC/2273)
- Seventh Framework Programme (266486 (‘NU-AGE: New dietary strategies addressi)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Health Sciences › Medicine › Geriatrics and Gerontology › Frailty in Older Adults
- Keywords
- Mediterranean diet, gut microbiota, frailty, older adults, dietary intervention, cognitive function, inflammation, C-reactive protein, IL-17, short-chain fatty acids, secondary bile acids, microbial metabolites, keystone species, healthy aging
- MeSH terms
- Gastrointestinal Microbiome, Frailty, Aged, Europe, Female, Health Status, Humans, Male, Patient Compliance, RNA, Ribosomal, 16S, Single-Blind Method, Diet, Mediterranean
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