High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome

Gut

Volumn 65, Issue 11, 2016, Pages

  De Filippis, Francesca ^a   Pellegrini, Nicoletta ^b   Vannini, Lucia ^c   Jeffery, Ian B ^d,e   La Storia, Antonietta ^a   Laghi, Luca ^c   I Serrazanetti, Diana ^c   Di Cagno, Raffaella ^f   Ferrocino, Ilario ^g   Lazzi, Camilla ^b   Turroni, Silvia ^c   Cocolin, Luca ^g   Brigidi, Patrizia ^c   Neviani, Erasmo ^b   Gobbetti, Marco ^f   O'Toole, Paul W ^d,e   Ercolini, Danilo ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF PARMA   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

^d UNIVERSITY COLLEGE CORK   (Ireland)

^e UNIVERSITY COLLEGE CORK   (Ireland)

^f UNIVERSITY OF BARI   (Italy)

^g UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

SHORT CHAIN FATTY ACID; TRIMETHYLAMINE OXIDE; FATTY ACID; METHYLAMINE; TRIMETHYLOXAMINE;

ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DIETARY COMPLIANCE; FECES LEVEL; FIRMICUTES; FOOD INTAKE; HUMAN; HUMAN EXPERIMENT; INTESTINE FLORA; ITALIAN (CITIZEN); MEDICAL RECORD; MEDITERRANEAN DIET; METABOLOME; METABOLOMICS; NORMAL HUMAN; OMNIVORE; PREVOTELLA; PRIORITY JOURNAL; URINE LEVEL; VEGAN; VEGETABLE; VEGETARIAN; WESTERN DIET; ADULT; CHEMISTRY; DIETARY FIBER; FECES; FEEDING BEHAVIOR; FEMALE; GASTROINTESTINAL TRACT; ISOLATION AND PURIFICATION; MALE; METABOLISM; MICROBIOLOGY; PATIENT COMPLIANCE; PHYSIOLOGY; PSYCHOLOGY; STATISTICS; URINE;

ADULT; CROSS-SECTIONAL STUDIES; DIET, MEDITERRANEAN; DIETARY FIBER; FATTY ACIDS; FECES; FEEDING BEHAVIOR; FEMALE; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HEALTHY VOLUNTEERS; HUMANS; MALE; METHYLAMINES; PATIENT COMPLIANCE; PREVOTELLA; STATISTICS AS TOPIC; VEGETABLES;

EID: 84992533219     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2015-309957     Document Type: Article

References (70)

1. Jeffery IB, O'Toole PW. Diet-microbiota interactions and their implications for healthy living. Nutrients 2013;5:234-52.
2. Wu GD, Bushmanc FD, Lewis JD. Diet, the human gut microbiota, and IBD. Anaerobe 2013;24:117-20.
3. Albenberg LG, Wu GD. Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterol 2014;146:1564-72.
4. Power SE, O'Toole PW, Stanton C, et al. Intestinal microbiota, diet and health. Br J Nutr 2014;111:387-402.
5. O'Keefe SJ. Towards the determination of the nutritional needs of the body and its microbiome in sickness and in health. Curr Opin Gastroenterol 2014;30:175-7.
6. Flint HJ, Duncan SH, Scott KP, et al. Links between diet, gut microbiota composition and gut metabolism. Proc Nutr Soc 2015;74:13-22.
7. Wu GD, Compher C, Chen EZ, et al. Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production. Gut Published Online First: 26 Nov 2014. doi:10.1136/gutjnl-2014- 308209
8. De Filippo C, Cavalieri D, Di Paola M, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 2010;107:14691-6.
9. Yatsunenko T, Rey FE, Manary MJ, et al. Human gut microbiome viewed across age and geography. Nature 2012;486:222-7.
10. Schnorr SL, Candela M, Rampelli S, et al. Gut microbiome of the Hadza hunter-gatherers. Nat Commun 2014;5:3654.
11. Wu GD, Chen J, Hoffmann C, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011;334:105-8.
12. Claesson MJ, Jeffery IB, Conde S, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature 2012;488:178-84.
13. Cotillard A, Kennedy SP, Kong LC, et al. Dietary intervention impact on gut microbial gene richness. Nature 2013;500:585-8.
14. Le Chatelier E, Nielsen T, Qin J, et al. Richness of human gut microbiome correlates with metabolic markers. Nature 2013;500:541-6.
15. David LA, Maurice CF, Carmody RN, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014;505:559-63.
16. Walker AW, Ince J, Duncan SH, et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J 2011;5:220-30.
17. Kim MS, Hwang SS, Park EJ, et al. Strict vegetarian diet improves the risk factors associated with metabolic diseases by modulating gut microbiota and reducing intestinal inflammation. Environ Microbiol Rep 2013;5:765-75.
18. Kelsen JR, Wu G. The gut microbiota, environment and diseases of modern society. Gut Microbes 2012;3:374-82.
19. Turnbaugh PJ, Ridaura VK, Faith JJ, et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 2009;1:6ra14.
20. Turnbaugh PJ, Bäckhed F, Fulton L, et al. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008;3:213-23.
21. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, et al. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 2009;137:1716-24.
22. Ou J, Carbonero F, Zoetendal EG, et al. Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am J Clin Nutr 2013;98:111-20.
23. Craig WJ. Health effects of vegan diets. Am J Clin Nutr 2009;89:1627S-33S.
24. Craig WJ. Nutrition concerns and health effects of vegetarian diets. Nutr Clin Pract 2010;25:613-20.
25. Trichopoulou A, Kouris-Blazos A, Wahlqvist ML, et al. Diet and overall survival in elderly people. BMJ 1995;311:1457-60.
26. Salas-Salvadó J, Bulló M, Babio N, et al. Reduction in the incidence of type 2 diabetes with the Mediterranean diet results of the PREDIMED-Reus nutrition intervention randomized trial. Diabetes Care 2011;34:14-19.
27. Marlow G, Ellet S, Ferguson IR, et al. Transcriptomics to study the effect of a Mediterranean-inspired diet on inflammation in Crohn's disease patients. Hum Genomics 2013;7:24.
28. Lopez-Legarrea P, Fuller NR, Zulet MA, et al. The influence of Mediterranean, carbohydrate and high protein diets on gut microbiota composition in the treatment of obesity and associated inflammatory state. Asia Pac J Clin Nutr 2014;23:360-8.
29. Estruch R, Ros E, Salas-Salvadó J, et al. Primary prevention of cardiovascular disease with a Mediterranean Diet. New Engl J Med 2013;368:1279-90.
30. Santoro A, Pini E, Scurti M, et al. Combating inflammaging through a Mediterranean whole diet approach: the NU-AGE project's conceptual framework and design. Mech Ageing Dev 2014;136:3-13.
31. Dall'Asta C, Scarlato AP, Galaverna G, et al. Dietary exposure to fumonisins and evaluation of nutrient intake in a group of adult celiac patients on a gluten-free diet. Mol Nutr Food Res 2012;56:632-40.
32. European Institute of Oncology. Food Composition Database for Epidemiological Studies in Italy, Version 2008. http://www.ieo.it/bda (accessed Dec 2012).
33. Agnoli C, Krogh V, Grioni S, et al. A priori-defined dietary patterns are associated with reduced risk of stroke in a large Italian cohort. J Nutr 2011;141:1552-8.
34. Drescher LS, Thiele S, Mesink GB. A new index to measure healthy food diversity better reflects a healthy diet than traditional measures. J Nutr 2007;137:647-51.
35. De Filippis F, Vannini L, La Storia A, et al. The same microbiota and a potentially discriminant metabolome in the saliva of omnivore, ovo-lacto-vegetarian and vegan individuals. PLoS ONE 2014;9:e112373.
36. Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010;7:335-6.
37. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010;11:R106.
38. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 1995;57:289-300.
39. Fagan A, Culhane AC, Higgins DG. A multivariate analysis approach to the integration of proteomic and gene expression data. Proteomics 2007; 7:2162-71.
40. Langille MG, Zaneveld J, Caporaso JG, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 2013;8:1-10.
41. Luo W, Friedman MS, Shedden K, et al. GAGE: generally applicable gene set enrichment for pathway analysis. BMC Bioinformatics 2009;10:161.
42. De Angelis M, Piccolo M, Vannini L, et al. Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. PLoS ONE 2013;8:e76993.
43. Laghi L, Picone G, Cruciani F, et al. Rifaximin modulates the vaginal microbiome and metabolome in women affected by bacterial vaginosis. Antimicrob Agents Chemother 2014;58:3411-20.
44. Wishart DS, Tzur D, Knox C, et al. HMDB: the Human Metabolome Database. Nucleic Acids Res 2007;35:D521-6.
45. Dieterle F, Ross A, Schlotterbeck G, et al. Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures. Application in 1H NMR metabonomics. Anal Chem 2006;78:4281-90.
46. Couto E, Boffetta P, Lagiou P, et al. Mediterranean dietary pattern and cancer risk in the EPIC cohort. Br J Cancer 2011;104:1493-9.
47. Cust AE, Skilton MR, van Bakel MM, et al. Total dietary carbohydrate, sugar, starch and fibre intakes in the European Prospective Investigation into Cancer and Nutrition. Eur J Clin Nutr 2009;63:S37-60.
48. Tan J, McKenzie C, Potamitis M, et al. The role of short chain fatty acids in health and disease. Adv Immunol 2014;121:91-119.
49. Thorburn AN, Macia L, Mackay CR. Diet, metabolites, and "western-lifestyle" inflammatory diseases. Immunity 2014;40:833-42.
50. Vipperla K, O'Keefe SJ. The microbiota and its metabolites in colonic mucosal health and cancer risk. Nutr Clin Pract 2012;27:624-35.
51. Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short chain fatty acids, regulate the colonic Treg cell homeostasis. Science 2013;341:569-73.
52. Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 2014;12:661-72.
53. Vital M, Gao J, Rizzo M, et al. Diet is a major factor governing the fecal butyrate-producing community structure across Mammalia, Aves and Reptilia. ISME J 2015;9:832-43.
54. O'Keefe SJ, Ou J, Aufreiter S, et al. Products of the colonic microbiota mediate the effects of diet on colon cancer risk. J Nutr 2009;139:2044-8.
55. 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.
56. Fernandes J, Su W, Rahat-Rozenbloom S, et al. Adiposity, gut microbiota and faecal short chain fatty acids are linked in adult humans. Nutr Diabetes 2014;4:e121.
57. Dunn WB, Lin W, Broadhurst D, et al. Molecular phenotyping of a UK population: defining the human serum metabolome. Metabolomics 2015;11:9-26.
58. Sampson JN, Boca SM, Shu XO, et al. Metabolomics in epidemiology: sources of variability in metabolite measurements and implications. Cancer Epidemiol Biomarkers Prev 2013;22:631-40.
59. Birkett A, Muir J, Phillips J, et al. Resistant starch lowers fecal concentrations of ammonia and phenols in humans. Eur J Clin Nutr 1996;63:766-72.
60. Patel KP, Luo FJ-G, Plummer NS, et al. The production of p-cresol sulfate and indoxyl sulfate in vegetarians versus omnivores. Clin J Am Soc Nephrol 2012;7:982-8.
61. Flint HJ, Scott KP, Duncan SH, et al. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 2012;3:289-306.
62. Wu T, Zhang Z, Liu B, et al. Gut microbiota dysbiosis and bacterial community assembly associated with cholesterol gallstones in large-scale study. BMC Genomics 2013;14:669.
63. McHardy IH, Li X, Tong M, et al. HIV infection is associated with compositional and functional shifts in the rectal mucosal microbiota. Microbiome 2013;1:26.
64. Vitaglione P, Mennella I, Ferracane R, et al. Wholegrain wheat consumption reduces inflammation in a randomized controlled trial on overweight and obese subjects with unhealthy dietary and lifestyle behaviors: role of polyphenols bound to cereal dietary fiber. Am J Clin Nutr 2015;101:1-12.
65. Roager HM, Licht TR, Poulsen SK, et al. Microbial enterotypes, inferred by the prevotella-to-bacteroides ratio, remained stable during a 6-month randomized controlled diet intervention with the new nordic diet. Appl Environ Microbiol 2013;80:1142-9.
66. Martinez-Medina M, Denizot J, Dreux N, et al. Western diet induces dysbiosis with increased E coli in CEABAC10 mice, alters host barrier function favouring AIEC colonisation. Gut 2014;63:116-24.
67. Stock J. Gut microbiota: an environmental risk factor for cardiovascular disease. Atherosclerosis 2013;229:440-2.
68. Tang WH, Wang Z, Levison BS, et al. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N Engl J Med 2013;368: 1575-84.
69. Koeth RA, Wang Z, Levison BS, et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 2013;19:576-85.
70. Wang Z, Klipfell E, Bennett BJ, et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 2011;472:57-63.