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Oxidative stress, DNA stability and evoked inflammatory signaling in young celiac patients consuming a gluten-free diet

Abstract

Purpose

Celiac disease (CD) is a multifactorial, autoimmune, gluten-sensitive inflammatory disorder of the small intestine. Taking into account the pathogenesis of CD, a strict gluten-free diet (GFD) is the only treatment able to restore epithelium integrity and eliminate complications. The current study was designed to assess whether the use of a GFD is sufficient for maintaining a correct oxidative/antioxidant balance and ameliorating the evoked inflammatory signaling in young patients with CD.

Methods

The study covered 80 children, aged between 7 and 18 years, attending the Gastroenterology Service of the Gastroenterology, Hepatology and Child Nutrition Service from the Virgen de las Nieves Hospital in Granada. Children with CD diagnosed were included in the celiac group who followed a strict GFD for 2 years (n = 40) and the control group (n = 40) included healthy children, with negative serological screening. Soluble superoxide dismutase 1 and 2, total antioxidant status, 8-hydroxy-2′-deoxyguanosine, cortisol, melatonin and inflammatory parameters in plasma, 15-F2t-isoprostanes in urine, and DNA breaks in peripheral blood lymphocytes were analysed.

Results

No differences were found in oxidative stress between CD patients and controls; however, IFN-γ, IL-1α, IP-10 and TNF-β were higher in the CD patients. VEGF was also higher than in the control group.

Conclusion

The GFD in the CD patients is enough to reduce the oxidative stress; however, in the case of the inflammatory signaling, the initial exposure to gluten prior to stablish the GFD is strong enough to induce an inflammatory state which is maintained (even when consuming the GFD); meanwhile the increase in VEGF recorded in the CD group could be a compensatory mechanism to restore the damaged mucosa and duodenal villous atrophy, due to its role in endothelial activation and generation of new functional and stable vascular networks.

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Acknowledgements

This work was supported by Andalusian Government, Excellence Research Project no P12-AGR-2581. Carlota Muriel-Neyra and Jorge Moreno-Fernandez are grateful to the Excellence Ph.D. Program “Nutrición y Ciencias de los Alimentos” from the University of Granada. The authors also thank the patients for their participation in the current study and Ms. Susan Stevenson for her efficient support in the revision with the English language.

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Correspondence to Teresa Nestares.

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The authors declare no conflict of interest. The funding sponsor had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results.

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Diaz-Castro, J., Muriel-Neyra, C., Martin-Masot, R. et al. Oxidative stress, DNA stability and evoked inflammatory signaling in young celiac patients consuming a gluten-free diet. Eur J Nutr 59, 1577–1584 (2020). https://doi.org/10.1007/s00394-019-02013-5

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  • DOI: https://doi.org/10.1007/s00394-019-02013-5

Keywords

  • Celiac disease
  • Gluten-free diet
  • Oxidative stress
  • Inflammatory signaling