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

Gut - Tập 69 Số 7 - Trang 1218-1228 - 2020
Tarini Shankar Ghosh1,2, Simone Rampelli3, Ian B. Jeffery1,2, Aurelia Santoro4,5, Marta C. Neto1,2, Miriam Capri3, Enrico Giampieri5, Amy Jennings6, Marco Candela3, Silvia Turroni3, Erwin G. Zoetendal7, Gerben D. A. Hermes7, Elodie Caumon8, Nathalie Meunier8, Corinne Malpuech‐Brugère9, Estelle Pujos‐Guillot10, Agnes A. M. Berendsen11, C.P.G.M. de Groot11, Edith J M Feskins11, Joanna Kałuża12, Barbara Pietruszka12, Marta Jeruszka-Bielak12, Blandine Comte10, Monica Maijo-Ferre13, Claudio Nicoletti14,13, Willem M. de Vos15,7, Susan J. Fairweather‐Tait16, Aedín Cassidy17, Patrizia Brigidi18, Claudio Franceschi19,20, Paul W. O’Toole21
1APC Microbiome Ireland, University College Cork, Cork, Ireland
2School of Microbiology, University College Cork, Cork, Ireland
3Unit of Microbial Ecology of Health, Department of Pharmacy and Biotechnology, University of Bologna, Bologna, Italy
4CIG Interdepartmental Centre “L Galvani”, Alma Mater Studiorum, University of Bologna, Bologna, Italy
5Department of Experimental, Diagnostic and Speciality Medicine, Alma Mater Studiorum, University of Bologna, Bologna, Italy
6Norwich Medical School, University of East Anglia Faculty of Medicine and Health Sciences, Norwich, Norfolk, UK
7Laboratory of Microbiology, Wageningen University and Research, Wageningen, Netherlands
8CRNH Auvergne, F-63000 Clermont-Ferrand, CHU Clermont-Ferrand, Clermont-Ferrand, France
9Unité de Nutrition Humaine, Université Clermont Auvergne, Clermont-Ferrand, Auvergne, France
10Plateforme d’Exploration du Métabolisme, MetaboHUB Clermont, Clermont-Ferrand, Université Clermont Auvergne, Clermont-Ferrand, Auvergne, France
11Division of Human Nutrition and Health, Wageningen University and Research, Wageningen, Netherlands
12Department of Human Nutrition, Warsaw University of Life Sciences, Warszawa, Poland
13Gut Health Institute Strategic Programme, Quadram Institute Bioscience, Norwich, Norfolk, UK
14Department of Experimental and Clinical Medicine, Section of Anatomy, University of Florence, Firenze, Toscana, Italy
15Human Microbiome Research Program, Faculty of Medicine, University of Helsinki, Helsinki, Finland
16Department of Nutrition and Preventive Medicine, Norwich Medical School, University of East Anglia, Norwich, Norfolk, UK
17The Institute of Global Food Security, Queen's University Belfast, Belfast, UK
18Unit of Microbial Ecology of Health, Department of Pharmacy and Biotechnology, University of Bologna, Bolognas, Italy
19Department of Applied Mathematics, Institute of Information Technology, Mathematics and Mechanics (ITMM), Lobachevsky State University of Nizhny Novgorod-National Research University (UNN), Nizhny Novgorod, Russian Federation
20Department of Experimental, Diagnostic and Speciality Medicine, Alma Mater Studiorum, University of Bologna, Bologna, Emilia-Romagna, Italy
21School of Microbiology, University College Cork APC Microbiome Institute, Cork T12 YN60, Ireland

Tóm tắt

ObjectiveAgeing 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.DesignWe 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).ResultsAdherence 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.ConclusionCollectively, 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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Tài liệu tham khảo

10.1016/S0140-6736(12)62167-9

10.1097/MCO.0b013e32835ada13

10.1111/j.1749-6632.2000.tb06651.x

Sugimoto, 2018, Epidemiological and clinical significance of cognitive frailty: a mini review, Ageing Res Rev, 44, 1, 10.1016/j.arr.2018.03.002

Wilson, 2017, Frailty and sarcopenia: the potential role of an aged immune system, Ageing Res Rev, 36, 1, 10.1016/j.arr.2017.01.006

10.1136/gutjnl-2017-315542

Trichopoulou A , Martínez-González MA , Tong TY , et al . Definitions and potential health benefits of the Mediterranean diet: views from experts around the world. BMC Med 2014;12:112.doi:10.1186/1741-7015-12-112

Sofi F , Cesari F , Abbate R , et al . Adherence to Mediterranean diet and health status: meta-analysis. BMJ 2008;337:a1344.doi:10.1136/bmj.a1344

Kojima, 2018, Adherence to Mediterranean diet reduces incident frailty risk: systematic review and meta-analysis, J Am Geriatr Soc, 66, 783, 10.1111/jgs.15251

10.1136/gutjnl-2015-309957

Mitsou, 2017, Adherence to the Mediterranean diet is associated with the gut microbiota pattern and gastrointestinal characteristics in an adult population, Br J Nutr, 117, 1645, 10.1017/S0007114517001593

10.1038/nature11319

O'Toole PW , Jeffery IB . Gut microbiota and aging. (1095-9203 (Electronic)).

10.1038/ismej.2015.88

Tran, 2019, Prebiotic supplementation in frail older people affects specific gut microbiota taxa but not global diversity, Microbiome, 7, 39, 10.1186/s40168-019-0654-1

10.1016/j.mad.2013.10.002

Marseglia A , Xu W , Fratiglioni L , et al . Effect of the NU-AGE diet on cognitive functioning in older adults: a randomized controlled trial. Front Physiol 2018;9:349.doi:10.3389/fphys.2018.00349

Jennings, 2018, A Mediterranean-like dietary pattern with vitamin D3 (10 µg/d) supplements reduced the rate of bone loss in older Europeans with osteoporosis at baseline: results of a 1-y randomized controlled trial, Am J Clin Nutr, 108, 633, 10.1093/ajcn/nqy122

Maijo M , Ivory K , Clements SJ , et al . One-year consumption of a Mediterranean-like dietary pattern with vitamin D3 supplements induced small scale but extensive changes of immune cell phenotype, co-receptor expression and innate immune responses in healthy elderly subjects: results from the United Kingdom arm of the NU-AGE trial. Front Physiol 2018;9:997.doi:10.3389/fphys.2018.00997

Jennings, 2019, Mediterranean-style diet improves systolic blood pressure and arterial stiffness in older adults, Hypertension, 73, 578, 10.1161/HYPERTENSIONAHA.118.12259

10.1016/j.mad.2013.12.001

Santoro, 2019, Gender-specific association of body composition with inflammatory and adipose-related markers in healthy elderly Europeans from the NU-AGE study, Eur Radiol, 29, 4968, 10.1007/s00330-018-5973-2

10.2144/04365ST04

10.1038/nbt.3960

10.1093/bioinformatics/btr507

10.1093/bioinformatics/btq461

10.1093/bioinformatics/btr381

Allard G , Ryan FJ , Jeffery IB , et al . SPINGO: a rapid species-classifier for microbial amplicon sequences. BMC Bioinformatics 2015;16:324.doi:10.1186/s12859-015-0747-1

10.1128/AEM.00062-07

Faust K , Sathirapongsasuti JF , Izard J , et al . Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol 2012;8:e1002606.doi:10.1371/journal.pcbi.1002606

10.1093/bioinformatics/bts438

Noronha, 2019, The virtual metabolic human database: integrating human and gut microbiome metabolism with nutrition and disease, Nucleic Acids Res, 47(D1), D614, 10.1093/nar/gky992

Sung J , Kim S , Cabatbat JJT , et al . Global metabolic interaction network of the human gut microbiota for context-specific community-scale analysis. Nat Commun 2017;8:15393.doi:10.1038/ncomms15393

10.1101/gr.1239303

Berendsen AAM , van de Rest O , Feskens EJM , et al . Changes in dietary intake and adherence to the NU-AGE diet following a one-year dietary intervention among European older adults: results of the NU-AGE randomized trial. Nutrients 2018;10:E1905.doi:10.3390/nu10121905

10.1136/gutjnl-2013-304833

10.1038/nature11450

10.1136/gutjnl-2015-309800

Jackson MA , Jackson M , Jeffery IB , et al . Signatures of early frailty in the gut microbiota. Genome Med 2016;8:8.doi:10.1186/s13073-016-0262-7

Gomez-Arango, 2018, Low dietary fiber intake increases Collinsella abundance in the gut microbiota of overweight and obese pregnant women, Gut Microbes, 9, 189, 10.1080/19490976.2017.1406584

10.1016/j.celrep.2019.02.090

10.1038/nature13568

Karlsson FH , Fåk F , Nookaew I , et al . Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat Commun 2012;3:1245.doi:10.1038/ncomms2266

Giampieri E , Ostan R , Guidarelli G , et al . A novel approach to improve the estimation of a diet adherence considering seasonality and short term variability - the NU-AGE Mediterranean diet experience. Front Physiol 2019;10:149.doi:10.3389/fphys.2019.00149

10.1016/j.cca.2007.01.026

10.1172/JCI57158

10.1053/j.gastro.2017.01.055

10.1177/1535370214538743

Sanna, 2019, Causal relationships among the gut microbiome, short-chain fatty acids and metabolic diseases, Nat Genet, 51, 600, 10.1038/s41588-019-0350-x

Pagliai G , Russo E , Niccolai E , et al . Influence of a 3-month low-calorie Mediterranean diet compared to the vegetarian diet on human gut microbiota and SCFA: the CARDIVEG study. Eur J Nutr 2019;11.doi:10.1007/s00394-019-02050-0

10.3945/ajcn.112.056689

O'Keefe SJD , Li JV , Lahti L , et al . Fat, fibre and cancer risk in African Americans and rural Africans. Nat Commun 2015;6:6342.doi:10.1038/ncomms7342

10.1093/ajcn/29.12.1448

Elshaghabee FMF , Bockelmann W , Meske D , et al . Ethanol production by selected intestinal microorganisms and lactic acid bacteria growing under different nutritional conditions. Front Microbiol 2016;7:47.doi:10.3389/fmicb.2016.00047

10.1099/00222615-28-3-211

10.1016/j.cmet.2014.07.006

Ghoshal, 2017, Small intestinal bacterial overgrowth and irritable bowel syndrome: a bridge between functional organic dichotomy, Gut Liver, 11, 196, 10.5009/gnl16126

10.1084/jem.20180448

Zaneveld, 2017, Stress and stability: applying the Anna Karenina principle to animal microbiomes, Nat Microbiol, 2, 17121, 10.1038/nmicrobiol.2017.121

10.1136/gutjnl-2019-320438

Ghosh D , Jeffery O' Toole . Adjusting for age improvesidentification of gut microbiome alterations in multiple diseases. eLife In Press.

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Gut

Tập 69 Số 7

1218-1228

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