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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.; Marciani, Luca

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Authors

Carolyn M. Costigan

Frederick J. Warren

Anthony P. Duncan

Nina Lewis

Carolina Ciacci

Paola Iovino

David S. Sanders

Falk Hildebrand



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.

Citation

Costigan, C. M., Warren, F. J., Duncan, A. P., Hoad, C. L., Lewis, N., Hill, T., Crooks, C. J., Morgan, P. S., Ciacci, C., Iovino, P., Sanders, D. S., Hildebrand, F., Gowland, P. A., Spiller, R. C., & Marciani, L. (2024). One Year of Gluten-Free Diet Impacts Gut Function and Microbiome in Celiac Disease. Clinical Gastroenterology and Hepatology, https://doi.org/10.1016/j.cgh.2024.11.006

Journal Article Type Article
Acceptance Date Nov 21, 2024
Online Publication Date Dec 9, 2024
Publication Date Dec 9, 2024
Deposit Date Nov 24, 2024
Publicly Available Date Dec 10, 2025
Journal Clinical Gastroenterology and Hepatology
Print ISSN 1542-3565
Electronic ISSN 1542-3565
Publisher Elsevier
Peer Reviewed Peer Reviewed
DOI https://doi.org/10.1016/j.cgh.2024.11.006
Keywords Celiac Disease; Microbiome; Gluten-Free Diet; MRI
Public URL https://nottingham-repository.worktribe.com/output/42468687
Publisher URL https://www.sciencedirect.com/science/article/pii/S1542356524010486