One year of gluten-free diet impacts gut function and microbiome in celiac disease

Costigan, Carolyn M., Warren, Frederick J., Duncan, Anthony P., Hoad, Caroline L., Lewis, Nina, Hill, Trevor, Crooks, Colin J., Morgan, Paul S., Ciacci, Carolina, Iovino, Paola, Sanders, David S., Hildebrand, Falk, Gowland, Penny A., Spiller, Robin C. and Marciani, Luca (2025) One year of gluten-free diet impacts gut function and microbiome in celiac disease. Clinical Gastroenterology and Hepatology, 23 (9). 1525-1534.e14. ISSN 1542-3565

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Abstract

Background & Aims: Currently, the main treatment for celiac disease (CD) is the gluten-free diet (GFD). This observational cohort study investigated the impact of CD and 1 year of GFD on gut function and microbiome. Methods: A total of 36 newly diagnosed patients and 36 healthy volunteers (HVs) were studied at baseline and at 12-month follow-up. Small bowel water content (SBWC), whole gut transit time (WGTT), and colon volumes were measured by magnetic resonance imaging. Stool sample DNA was subjected to shotgun metagenomic sequencing. Species-level abundances and gene functions, including CAZymes (carbohydrate active enzymes) were determined. Results: SBWC was significantly higher in people with CD (157 ± 15 mL) vs (HVs 100 ± 12 mL) (P = .003). WGTT was delayed in people with CD (68 ± 8 hours) vs HVs (41 ± 5 hours) (P = .002). The differences reduced after 12 months of GFD but not significantly. Well-being in the CD group significantly improved after GFD but did not recover to control values. CD fecal microbiota showed a high abundance of proteolytic gene functions, associated with Escherichia coli, Enterobacter, and Peptostreptococcus. GFD significantly reduced Bifidobacteria and increased Blautia wexlerae. Microbiome composition correlated positively with WGTT, colonic volume, and Akkermansia municphilia but negatively with B wexerelae. Following GFD, the reduction in WGTT and colonic volume was significantly associated with increased abundance of B wexlerae. There were also significant alterations in CAZyme profiles, specifically starch- and arabinoxylan-degrading families. Conclusions: CD impacted gut function and microbiota. GFD ameliorated but did not reverse these effects, significantly reducing Bifidobacteria associated with reduced intake of resistant starch and arabinoxylan from wheat. ClinicalTrials.gov, number: NCT02551289.

Item Type: Article
Additional Information: Data Availability: Raw read data from the metagenomic sequencing runs can be accessed through the NCBI SRA project number PRJNA1023737 at http://www.ncbi.nlm.nih.gov/bioproject/1023737. The associated metadata can be accessed through the University of Nottingham Research Repository (https://doi.org/10.17639/nott.7352). The full MATAFILER pipeline is available at https://github.com/hildebra/MATAF3. The RTK package is available at www.github.com/hildebra/Rarefaction/ Acknowledgments: The authors sincerely thank all participants who have contributed to this study. They gratefully acknowledge the support of the Biotechnology and Biological Sciences Research Council. The authors also thank J. Price (Nottingham University Hospitals NHS Trust), specialist celiac dietitian, for help with recruitment and clinical advice; M. Lingaya (NIHR Nottingham Biomedical Research Centre) for preparation of stool samples and DNA extraction; D. Baker and R. Evans (Quadram Institute Bioscience) for DNA normalization and sequencing library preparation; A. Wragg (NIHR Nottingham Biomedical Research Centre) for his assistance with the patient and public involvement group; and C. Lam and S. Beg for their expert gastrenterology advice. This article was posted as a preprint on bioRxiv.org: https://doi.org/10.1101/2024.06.20.599876.
Uncontrolled Keywords: celiac disease,gluten-free diet,microbiome,mri,hepatology,gastroenterology ,/dk/atira/pure/subjectarea/asjc/2700/2721
Faculty \ School: Faculty of Science > School of Chemistry, Pharmacy and Pharmacology
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Depositing User: LivePure Connector
Date Deposited: 24 Feb 2025 15:30
Last Modified: 23 Jul 2025 08:30
URI: https://ueaeprints.uea.ac.uk/id/eprint/98573
DOI: 10.1016/j.cgh.2024.11.006

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