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
Tarini Shankar Ghosh, Simone Rampelli, Ian B Jeffery, Aurelia Santoro, Marta Neto, Miriam Capri, Enrico Giampieri, Amy Jennings, Marco Candela, Silvia Turroni, Erwin G Zoetendal, Gerben D A Hermes, Caumon Elodie, Nathalie Meunier, Corinne Malpuech Brugere, Estelle Pujos-Guillot, Agnes M Berendsen, Lisette C P G M De Groot, Edith J M Feskins, Joanna Kaluza, Barbara Pietruszka, Marta Jeruszka Bielak, Blandine Comte, Monica Maijo-Ferre, Claudio Nicoletti, Willem M De Vos, Susan Fairweather-Tait, Aedin Cassidy, Patrizia Brigidi, Claudio Franceschi, Paul W O'Toole, Tarini Shankar Ghosh, Simone Rampelli, Ian B Jeffery, Aurelia Santoro, Marta Neto, Miriam Capri, Enrico Giampieri, Amy Jennings, Marco Candela, Silvia Turroni, Erwin G Zoetendal, Gerben D A Hermes, Caumon Elodie, Nathalie Meunier, Corinne Malpuech Brugere, Estelle Pujos-Guillot, Agnes M Berendsen, Lisette C P G M De Groot, Edith J M Feskins, Joanna Kaluza, Barbara Pietruszka, Marta Jeruszka Bielak, Blandine Comte, Monica Maijo-Ferre, Claudio Nicoletti, Willem M De Vos, Susan Fairweather-Tait, Aedin Cassidy, Patrizia Brigidi, Claudio Franceschi, Paul W O'Toole
Abstract
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.
Keywords: ageing; diet; enteric bacterial microflora; inflammation; intestinal bacteria.
Conflict of interest statement
Competing interests: None declared.
© Author(s) (or their employer(s)) 2020. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ.
Figures
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MedDiet microbiome index correlates with…
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MedDiet microbiome index correlates with reduced frailty, improved cognitive function and reduced inflammation,…
Figure 5
Bacterial taxa that respond positively…
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Bacterial taxa that respond positively to Mediterranean diet intervention occupy keystone interaction nodes…
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- Mechanisms of gut microbiota-immune-host interaction on glucose regulation in type 2 diabetes.Zhou YD, Liang FX, Tian HR, Luo D, Wang YY, Yang SR. Zhou YD, et al. Front Microbiol. 2023 Feb 20;14:1121695. doi: 10.3389/fmicb.2023.1121695. eCollection 2023. Front Microbiol. 2023. PMID: 36891383 Free PMC article. Review.
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- Multicenter Study
- Randomized Controlled Trial
- Research Support, Non-U.S. Gov't
- Aged
- Diet, Mediterranean*
- Europe
- Female
- Frailty / diet therapy
- Frailty / prevention & control*
- Gastrointestinal Microbiome* / genetics
- Health Status
- Humans
- Male
- Patient Compliance
- RNA, Ribosomal, 16S / genetics
- Single-Blind Method
- RNA, Ribosomal, 16S
- Full Text Sources
- Other Literature Sources
- Medical
- Research Materials
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![Figure 4](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/7306987/bin/gutjnl-2019-319654f04.jpg)
Figure 5
Bacterial taxa that respond positively…
Figure 5
Bacterial taxa that respond positively to Mediterranean diet intervention occupy keystone interaction nodes…
- Mediterranean diet, gut microbiota and health: when age and calories do not add up!Cani PD, Van Hul M. Cani PD, et al. Gut. 2020 Jul;69(7):1167-1168. doi: 10.1136/gutjnl-2020-320781. Epub 2020 Mar 13. Gut. 2020. PMID: 32169906 Free PMC article. No abstract available.
- Effect on gut microbiota of a 1-y lifestyle intervention with Mediterranean diet compared with energy-reduced Mediterranean diet and physical activity promotion: PREDIMED-Plus Study.Muralidharan J, Moreno-Indias I, Bulló M, Lopez JV, Corella D, Castañer O, Vidal J, Atzeni A, Fernandez-García JC, Torres-Collado L, Fernández-Carrión R, Fito M, Olbeyra R, Gomez-Perez AM, Galiè S, Bernal-López MR, Martinez-Gonzalez MA, Salas-Salvadó J, Tinahones FJ. Muralidharan J, et al. Am J Clin Nutr. 2021 Sep 1;114(3):1148-1158. doi: 10.1093/ajcn/nqab150. Am J Clin Nutr. 2021. PMID: 34020445 Free PMC article. Clinical Trial.
- Prebiotic supplementation in frail older people affects specific gut microbiota taxa but not global diversity.Tran TTT, Cousin FJ, Lynch DB, Menon R, Brulc J, Brown JR, O'Herlihy E, Butto LF, Power K, Jeffery IB, O'Connor EM, O'Toole PW. Tran TTT, et al. Microbiome. 2019 Mar 13;7(1):39. doi: 10.1186/s40168-019-0654-1. Microbiome. 2019. PMID: 30867067 Free PMC article.
- Associations between Pro- and Anti-Inflammatory Gastro-Intestinal Microbiota, Diet, and Cognitive Functioning in Dutch Healthy Older Adults: The NU-AGE Study.van Soest APM, Hermes GDA, Berendsen AAM, van de Rest O, Zoetendal EG, Fuentes S, Santoro A, Franceschi C, de Groot LCPGM, de Vos WM. van Soest APM, et al. Nutrients. 2020 Nov 12;12(11):3471. doi: 10.3390/nu12113471. Nutrients. 2020. PMID: 33198235 Free PMC article. Clinical Trial.
- Intestinal microbiome in normal ageing, frailty and cognition decline.Strasser B, Ticinesi A. Strasser B, et al. Curr Opin Clin Nutr Metab Care. 2023 Jan 1;26(1):8-16. doi: 10.1097/MCO.0000000000000878. Epub 2022 Sep 14. Curr Opin Clin Nutr Metab Care. 2023. PMID: 36102345 Review.
- The Mediterranean diet and its association with selected gut bacteria.Krznarić Ž, Vranešić Bender D, Meštrović T. Krznarić Ž, et al. Curr Opin Clin Nutr Metab Care. 2019 Sep;22(5):401-406. doi: 10.1097/MCO.0000000000000587. Curr Opin Clin Nutr Metab Care. 2019. PMID: 31232713 Review.
- Cardiometabolic health, diet and the gut microbiome: a meta-omics perspective.Valles-Colomer M, Menni C, Berry SE, Valdes AM, Spector TD, Segata N. Valles-Colomer M, et al. Nat Med. 2023 Mar;29(3):551-561. doi: 10.1038/s41591-023-02260-4. Epub 2023 Mar 17. Nat Med. 2023. PMID: 36932240 Review.
- To Fiber or Not to Fiber: The Swinging Pendulum of Fiber Supplementation in Patients with Inflammatory Bowel Disease.Haskey N, Gold SL, Faith JJ, Raman M. Haskey N, et al. Nutrients. 2023 Feb 21;15(5):1080. doi: 10.3390/nu15051080. Nutrients. 2023. PMID: 36904081 Free PMC article. Review.
- Mechanisms of gut microbiota-immune-host interaction on glucose regulation in type 2 diabetes.Zhou YD, Liang FX, Tian HR, Luo D, Wang YY, Yang SR. Zhou YD, et al. Front Microbiol. 2023 Feb 20;14:1121695. doi: 10.3389/fmicb.2023.1121695. eCollection 2023. Front Microbiol. 2023. PMID: 36891383 Free PMC article. Review.
- Pathways to healing: Plants with therapeutic potential for neurodegenerative diseases.Tyler SEB, Tyler LDK. Tyler SEB, et al. IBRO Neurosci Rep. 2023 Feb 10;14:210-234. doi: 10.1016/j.ibneur.2023.01.006. eCollection 2023 Jun. IBRO Neurosci Rep. 2023. PMID: 36880056 Free PMC article.
- Design of the Building Research in CRC prevention (BRIDGE-CRC) trial: a 6-month, parallel group Mediterranean diet and weight loss randomized controlled lifestyle intervention targeting the bile acid-gut microbiome axis to reduce colorectal cancer risk among African American/Black adults with obesity.McLeod A, Wolf P, Chapkin RS, Davidson LA, Ivanov I, Berbaum M, Williams LR, Gaskins HR, Ridlon J, Sanchez-Flack J, Blumstein L, Schiffer L, Hamm A, Cares K, Antonic M, Bernabe BP, Fitzgibbon M, Tussing-Humphreys L. McLeod A, et al. Trials. 2023 Feb 15;24(1):113. doi: 10.1186/s13063-023-07115-4. Trials. 2023. PMID: 36793105 Free PMC article. Clinical Trial.
- Multicenter Study
- Randomized Controlled Trial
- Research Support, Non-U.S. Gov't
- Aged
- Diet, Mediterranean*
- Europe
- Female
- Frailty / diet therapy
- Frailty / prevention & control*
- Gastrointestinal Microbiome* / genetics
- Health Status
- Humans
- Male
- Patient Compliance
- RNA, Ribosomal, 16S / genetics
- Single-Blind Method
- RNA, Ribosomal, 16S
- Full Text Sources
- Other Literature Sources
- Medical
- Research Materials
![Figure 5](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/7306987/bin/gutjnl-2019-319654f05.jpg)
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