Cited by 601Gut microbiota and healthNutritional Studies and DietInflammatory Bowel Disease

Long-term dietary patterns are associated with pro-inflammatory and anti-inflammatory features of the gut microbiome

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Bolte, Laura A, Vich Vila, Arnau, Imhann, Floris, Collij, Valerie, Gacesa, Ranko, Peters, Vera, Wijmenga, Cisca, Kurilshikov, Alexander +5 more·2021·Gut

Abstract

Objective: The microbiome directly affects the balance of pro-inflammatory and anti-inflammatory responses in the gut. As microbes thrive on dietary substrates, the question arises whether we can nourish an anti-inflammatory gut ecosystem. We aim to unravel interactions between diet, gut microbiota and their functional ability to induce intestinal inflammation. Design: We investigated the relation between 173 dietary factors and the microbiome of 1425 individuals spanning four cohorts: Crohn’s disease, ulcerative colitis, irritable bowel syndrome and the general population. Shotgun metagenomic sequencing was performed to profile gut microbial composition and function. Dietary intake was assessed through food frequency questionnaires. We performed unsupervised clustering to identify dietary patterns and microbial clusters. Associations between diet and microbial features were explored per cohort, followed by a meta-analysis and heterogeneity estimation. Results: We identified 38 associations between dietary patterns and microbial clusters. Moreover, 61 individual foods and nutrients were associated with 61 species and 249 metabolic pathways in the meta-analysis across healthy individuals and patients with IBS, Crohn’s disease and UC (false discovery rate<0.05). Processed foods and animal-derived foods were consistently associated with higher abundances of Firmicutes, Ruminococcus species of the Blautia genus and endotoxin synthesis pathways. The opposite was found for plant foods and fish, which were positively associated with short-chain fatty acid-producing commensals and pathways of nutrient metabolism. Conclusion: We identified dietary patterns that consistently correlate with groups of bacteria with shared functional roles in both, health and disease. Moreover, specific foods and nutrients were associated with species known to infer mucosal protection and anti-inflammatory effects. We propose microbial mechanisms through which the diet affects inflammatory responses in the gut as a rationale for future intervention studies.

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Crossref · 10.1136/gutjnl-2020-322670

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  • The gut microbiota releases byproducts from the cell wall, such as endotoxins like LPS, which can act locally and may be present in the gut, gingiva, and skin, as well as other tissues, causing dysregulation of GBA signaling, or can cross the intestinal barrier to enter the circulatory system (metabolic endotoxemia).

    “The gut microbiota releases byproducts from the cell wall, such as endotoxins like LPS, which can act locally and may be present in the gut, gingiva, and skin, as well as other tissues, causing dysregulation of GBA signaling (64), or can cross the intestinal barrier to enter the circulatory system; this is called metabolic endotoxemia (65).”
  • The Mediterranean diet has been associated with an increased abundance of bacteria producing short-chain fatty acids (SCFAs) that have been shown to be predictive of immunotherapy response.

    “The Mediterranean diet has been associated with an increased abundance of bacteria producing SCFAs3 that have been shown to be predictive of immunotherapy response in several studies.2,4,5,6”
  • Long-term dietary habits play a role in shaping the composition and metabolic activity of the gut microbiota.

    “Previous studies have suggested that long-term dietary habits play a role in shaping the composition and metabolic activity of the gut microbiota.”

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  1. [58]Singh RK, Chang H-W, Yan D, et al. Influence of diet on the gut microbiome and implications for human health. J Transl Med 2017; 15: 73. 10.1186/s12967-017-1175-y 28388917 PMC5385025 · DOI · Paper page

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Authors
Bolte, L. A., Vich Vila, A., Imhann, F., Collij, V., Gacesa, R., Peters, V., Wijmenga, C., Kurilshikov, A., Campmans-Kuijpers, M. J. E., Fu, J., Dijkstra, G., Zhernakova, A., & Weersma, R. K.
Affiliations
  • University Medical Center Groningen (NL)
  • Department of Gastroenterology and Hepatology, University of Groningen and University Medical Centre Groningen, Groningen, The Netherlands
Corresponding author
Weersma, Rinse K
Venue
Gut
Publisher
BMJ
Published
2021-04-02
Volume
70
Issue
7
Pages
1287-1298
ISSN
  • 0017-5749 (ISSN-L)
  • 1468-3288
OpenAlex
W3151963551
Cited by
595
References
60
Citations by year
2026: 87 · 2025: 151 · 2024: 121 · 2023: 117 · 2022: 92 · 2021: 26 · 2017: 1
FWCI
28.57
Type
journal article
Language
en
Open access
Locations
  • Gut (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, cc-by)
  • University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
Funders
  • CardioVasculair Onderzoek Nederland (CVON 2012-03)
  • Netherlands’ Top Institute Food and Nutrition (GH001)
  • Top Sector Life Sciences & Health, Samenwerkende Gezondheidsfondsen (LSHM18057-SGF)
  • European Research Council (ERC Consolidator grant 101001678, ERC-715772)
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO Gravitation grant ExposomeNL 024.004.017, NWO Gravitation grant Organ-on-Chip 024.003.001, NWO SPI 92-266, NWO VIDI grant 016.178.056)
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
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
Keywords
dietary habits, gut microbiota, intestinal inflammation, Crohn's disease, ulcerative colitis, irritable bowel syndrome, processed foods, animal products, plant-based foods, fish consumption, Firmicutes, Ruminococcus, Blautia, short-chain fatty acids, mucosal protection, anti-inflammatory bacteria, microbial metabolic pathways
MeSH terms
Gastrointestinal Microbiome, Adult, Bacteria, Beverages, Colitis, Ulcerative, Crohn Disease, Diet, Feces, Food, Humans, Inflammation, Middle Aged, Surveys and Questionnaires, Time Factors, Irritable Bowel Syndrome, Metagenomics

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