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Effect of Gluten-Free Diet on Serum Antioxidant Levels in Children with Celiac

Yıl 2023, Cilt: 82 Sayı: 2, 263 - 269, 21.12.2023
https://doi.org/10.26650/EurJBiol.2023.1307239

Öz

Objective: Celiac disease (CD) is an inflammatory condition of the small intestine triggered by the consumption of gluten. A strict gluten-free diet (GFD) is the only treatment that can eliminate CD complications. It was aimed to evaluate the effect of a gluten-free diet on serum total glutathione (tGSH) level, superoxide dismutase (SOD), myeloperoxida (MPO), paroxanase (PON-1) and aryl esterase (ARE) activity in patients with celiac disease, an autoimmune disease.

Materials and Methods: The study was conducted with 68 participants, 39 of whom were celiac and 29 were healthy. Two groups were formed in patients with celiac disease as newly diagnosed and previously diagnosed and following a gluten-free diet. Blood samples were taken from all participants and tGSH, SOD, MPO, PON-1, and ARE measurements were made spectrophotometrically from serum samples.

Results: While no significant change was observed in tGSH, SOD, and ARE levels, MPO activity was observed to be significantly lower in celiac patients compared to healthy controls, while this decrease was found to be higher in the newly diagnosed group. While PON-1 activity was significantly lower in newly diagnosed patients compared to the control group, it was higher in the gluten-compatible diet group.

Conclusion: Low MPO values in celiac patients may be insufficient to function by creating oxidative stress in inflammation. While PON-1 values are significantly lower in newly diagnosed celiacs, it can be said that they reach normal values with adherence to a gluten-free diet.

Kaynakça

  • Sollid LM, Jabri B. Is celiac disease an autoimmune disorder? Curr Opin Immunol. 2005;17(6):595-600. google scholar
  • Sayar E, Ozdem S, Uzun G, Islek A, Yilmaz A, Artan R. Total oxidant status, total antioxidant capacity and ischemia modified albumin levels in children with celiac disease. Turkish J Pediatr. 2015;57(5):498-503. google scholar
  • Ferretti G, Bacchetti T, Masciangelo S, Saturni L. Celiac disease, inflammation and oxidative damage: A nutrigenetic approach. Nutrients. 2012;4(4):243-257. google scholar
  • Green PH, Lebwohl B. Mesalamine for refractory celiac dis-ease: An old medicine for a new disease. J Clin Gastroenterol. 2011;45(1):1-3. google scholar
  • King JA, Jeong J, Underwood FE, et al. Incidence of celiac disease is increasing over time: A systematic review and meta-analysis. Am J Gastroenterol. 2020;115(4):507-525. google scholar
  • Ciacci C, Cirillo M, Cavallaro R, Mazzacca G. Long-term follow-up of celiac adults on gluten-free diet: Prevalence and correlates of intestinal damage. Digestion. 2002;66(3):178-185. google scholar
  • Wu XX, Qian L, Liu KX, Wu J, Shan ZW. Gastrointestinal micro-biome and gluten in celiac disease. Ann Med. 2021;53(1):1797-1805. google scholar
  • Granot E, Kohen R. Oxidative stress in childhood in health and disease states. Clin Nutr. 2004;23(1):3-11. google scholar
  • Luciani A, Villella VR, Vasaturo A, et al. Lysosomal accumula-tion of gliadin p31-43 peptide induces oxidative stress and tissue transglutaminase-mediated PPARgamma downregulation in in-testinal epithelial cells and coeliac mucosa. Gut. 2010;59(3):311-319. google scholar
  • Bagdi E, Diss TC, Munson P, Isaacson PG. Mucosal intra-epithelial lymphocytes in enteropathy-associated T-cell lym-phoma, ulcerative jejunitis, and refractory celiac disease con-stitute a neoplastic population. Blood. 1999;94(1):260-264. google scholar
  • Ferretti G, Bacchetti T, Masciangelo S, Saturni L. Celiac disease, inflammation and oxidative damage: A nutrigenetic approach. Nutrients. 2012;4(4):243-257. google scholar
  • Pereira B, Costa Rosa LF, Safi DA, Medeiros MH, Curi R, Bechara EJ. Superoxide dismutase, catalase, and glutathione per-oxidase activities in muscle and lymphoid organs of sedentary and exercise-trained rats. Physiol Behav. 1994;56(5):1095-1099. google scholar
  • Genestra M. Oxyl radicals, redox-sensitive signalling cascades and antioxidants. Cell Signal. 2007;19(9):1807-1819. google scholar
  • Watson AD, Berliner JA, Hama SY, et al. Protective effect of high density lipoprotein associated paraoxonase. Inhibition of the biological activity of minimally oxidized low density lipoprotein. J Clin Invest. 1995;96(6):2882-2891. google scholar
  • Primo-Parmo SL, Sorenson RC, Teiber J, La Du BN. The human serum paraoxonase/arylesterase gene (PON1) is one member of a multigene family. Genomics. 1996;33(3):498-507. google scholar
  • Winterbourn CC, Vissers MC, Kettle AJ. Myeloperoxidase. Curr Opin Hematol. 2000;7(1):53-58. google scholar
  • Eiserich JP, Baldus S, Brennan ML, et al. Myeloperox-idase, a leukocyte-derived vascular NO oxidase. Science. 2002;296(5577):2391-2394. google scholar
  • Szaflarska-Poplawska A, Siomek A, Czerwionka-Szaflarska M, et al. Oxidatively damaged DNA/oxidative stress in chil-dren with celiac disease. Cancer Epidemiol Biomarkers Prev. 2010;19(8):1960-1965. google scholar
  • Husby S, Koletzko S, Korponay-Szabo IR, et al. European Society for Pediatric Gastroenterology, Hepatology, and Nutrition guide-lines for the diagnosis of coeliac disease. J Pediatr Gastroenterol Nutr. 2012;54(1):136-160. google scholar
  • Bradley PP, Priebat DA, Christensen RD, Rothstein G. Measure-ment of cutaneous inflammation: Estimation of neutrophil content with an enzyme marker. J Invest Dermatol. 1982;78(3):206-209. google scholar
  • Sedlak J, Lindsay RH. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem. 1968;25(1):192-205. google scholar
  • Charlton-Menys V, Liu Y, Durrington PN. Semiautomated method for determination of serum paraoxonase activity using paraoxon as substrate. Clin Chem. 2006;52(3):453-457. google scholar
  • Cayir Y, Cayir A, Turan MI, et al. Antioxidant status in blood of obese children: The relation between trace elements, paraoxonase, and arylesterase values. Biol Trace Elem Res. 2014;160(2):155-160. google scholar Shahbazkhani B, Forootan M, Merat S, et al. Coeliac disease presenting with symptoms of irritable bowel syndrome. Aliment Pharmacol Ther. 2003;18(2):231-235. google scholar
  • Halliwell B. How to characterize a biological antioxidant. Free Radic Res Commun. 1990;9(1):1-32. google scholar
  • Pham-Huy LA, He H, Pham-Huy C. Free radicals, antioxidants in disease and health. Int J Biomed Sci. 2008;4(2):89-96. google scholar
  • Fasano A, Catassi C. Clinical practice. Celiac disease. N Engl J Med. 2012;367(25):2419-2426. google scholar
  • Olinski R, Gackowski D, Rozalski R, Foksinski M, Bialkowski K. Oxidative DNA damage in cancer patients: A cause or a con-sequence of the disease development? Mutat Res. 2003;531(1-2):177-190. google scholar
  • Stojiljkovic V, Todorovic A, Radlovic N, et al. Antioxidant en-zymes, glutathione and lipid peroxidation in peripheral blood of children affected by coeliac disease. Ann Clin Biochem. 2007;44(Pt 6):537-543. google scholar
  • Wang CF, Cui CX, Li N, et al. Antioxidant activity and pro-tective effect of wheat germ peptides in an in vitro celiac dis-ease model via Keap1/Nrf2 signaling pathway. Food Res Int. 2022;161.doi:ARTN 11186410.1016/j.foodres.2022.111864 google scholar
  • Rowicka G, Czaja-Bulsa G, Chelchowska M, et al. Oxidative and antioxidative status of children with celiac disease treated with a gluten free-diet. Oxid Med Cell Longev. 2018:1324820. doi:10.1155/2018/1324820 google scholar
  • Stojiljkovic V, Pejic S, Kasapovic J, et al. Glutathione redox cycle in small intestinal mucosa and peripheral blood of pediatric celiac disease patients. An Acad Bras Cienc. 2012;84(1):175-184. google scholar
  • Di Stefano M, Miceli E, Mengoli C, Corazza GR, Di Sabatino A. The effect of a gluten-free diet on vitamin D metabolism in celiac disease: The state of the art. Metabolites. 2023;13(1).doi:ARTN 7410.3390/metabo13010074 google scholar
  • Franckilin LRD, Dos Santos ACPM, Freitas FEDA, et al. Gluten: Do only celiac patients benefit from its removal from the diet?Food Rev Int. 2022;doi:10.1080/87559129.2021.2024566 google scholar
  • Hogberg L, Webb C, Falth-Magnusson K, et al. Children with screening-detected coeliac disease show increased levels of nitric oxide products in urine. Acta Paediatr. 2011;100(7):1023-1027. google scholar
  • Sayar E, Ozdem S, Uzun G, Islek A, Yilmaz A, Artan R. Total oxidant status, total antioxidant capacity and ischemia modified albumin levels in children with celiac disease. Turk J Pediatr. 2015;57(5):498-503. google scholar
  • Ferretti G, Bacchetti T, Saturni L, et al. Lipid peroxidation and paraoxonase-1 activity in celiac disease. J Lipids. 2012;587479. doi:10.1155/2012/587479 google scholar
  • Stojiljkovic V, Todorovic A, Pejic S, et al. Antioxidant status and lipid peroxidation in small intestinal mucosa of children with celiac disease. Clin Biochem. 2009;42(13-14):1431-1437. google scholar
  • Shamir R, Hartman C, Karry R, et al. Paraoxonases (PONs) 1, 2, and 3 are expressed in human and mouse gastrointestinal tract and in Caco-2 cell line: Selective secretion of PON1 and PON2. Free Radical Bio Med. 2005;39(3):336-344. google scholar
  • Rothem L, Hartman C, Dahan A, Lachter J, Eliakim R, Shamir R. Paraoxonases are associated with intestinal inflammatory diseases and intracellularly localized to the endoplasmic reticulum. Free Radic Biol Med. 2007;43(5):730-739. google scholar
  • Kaplan M, Ates I, Yuksel M, et al. The Role of oxidative stress in the etiopathogenesis of gluten-sensitive enteropathy disease. J Med Biochem. 2017;36(3):243-250. google scholar
  • Maluf SW, Wilhelm Filho D, Parisotto EB, et al. DNA damage, oxidative stress, and inflammation in children with celiac disease. Genet Mol Biol. 2020;43(2):e20180390. doi:10.1590/1678-4685-GMB-2018-0390 google scholar
Yıl 2023, Cilt: 82 Sayı: 2, 263 - 269, 21.12.2023
https://doi.org/10.26650/EurJBiol.2023.1307239

Öz

Kaynakça

  • Sollid LM, Jabri B. Is celiac disease an autoimmune disorder? Curr Opin Immunol. 2005;17(6):595-600. google scholar
  • Sayar E, Ozdem S, Uzun G, Islek A, Yilmaz A, Artan R. Total oxidant status, total antioxidant capacity and ischemia modified albumin levels in children with celiac disease. Turkish J Pediatr. 2015;57(5):498-503. google scholar
  • Ferretti G, Bacchetti T, Masciangelo S, Saturni L. Celiac disease, inflammation and oxidative damage: A nutrigenetic approach. Nutrients. 2012;4(4):243-257. google scholar
  • Green PH, Lebwohl B. Mesalamine for refractory celiac dis-ease: An old medicine for a new disease. J Clin Gastroenterol. 2011;45(1):1-3. google scholar
  • King JA, Jeong J, Underwood FE, et al. Incidence of celiac disease is increasing over time: A systematic review and meta-analysis. Am J Gastroenterol. 2020;115(4):507-525. google scholar
  • Ciacci C, Cirillo M, Cavallaro R, Mazzacca G. Long-term follow-up of celiac adults on gluten-free diet: Prevalence and correlates of intestinal damage. Digestion. 2002;66(3):178-185. google scholar
  • Wu XX, Qian L, Liu KX, Wu J, Shan ZW. Gastrointestinal micro-biome and gluten in celiac disease. Ann Med. 2021;53(1):1797-1805. google scholar
  • Granot E, Kohen R. Oxidative stress in childhood in health and disease states. Clin Nutr. 2004;23(1):3-11. google scholar
  • Luciani A, Villella VR, Vasaturo A, et al. Lysosomal accumula-tion of gliadin p31-43 peptide induces oxidative stress and tissue transglutaminase-mediated PPARgamma downregulation in in-testinal epithelial cells and coeliac mucosa. Gut. 2010;59(3):311-319. google scholar
  • Bagdi E, Diss TC, Munson P, Isaacson PG. Mucosal intra-epithelial lymphocytes in enteropathy-associated T-cell lym-phoma, ulcerative jejunitis, and refractory celiac disease con-stitute a neoplastic population. Blood. 1999;94(1):260-264. google scholar
  • Ferretti G, Bacchetti T, Masciangelo S, Saturni L. Celiac disease, inflammation and oxidative damage: A nutrigenetic approach. Nutrients. 2012;4(4):243-257. google scholar
  • Pereira B, Costa Rosa LF, Safi DA, Medeiros MH, Curi R, Bechara EJ. Superoxide dismutase, catalase, and glutathione per-oxidase activities in muscle and lymphoid organs of sedentary and exercise-trained rats. Physiol Behav. 1994;56(5):1095-1099. google scholar
  • Genestra M. Oxyl radicals, redox-sensitive signalling cascades and antioxidants. Cell Signal. 2007;19(9):1807-1819. google scholar
  • Watson AD, Berliner JA, Hama SY, et al. Protective effect of high density lipoprotein associated paraoxonase. Inhibition of the biological activity of minimally oxidized low density lipoprotein. J Clin Invest. 1995;96(6):2882-2891. google scholar
  • Primo-Parmo SL, Sorenson RC, Teiber J, La Du BN. The human serum paraoxonase/arylesterase gene (PON1) is one member of a multigene family. Genomics. 1996;33(3):498-507. google scholar
  • Winterbourn CC, Vissers MC, Kettle AJ. Myeloperoxidase. Curr Opin Hematol. 2000;7(1):53-58. google scholar
  • Eiserich JP, Baldus S, Brennan ML, et al. Myeloperox-idase, a leukocyte-derived vascular NO oxidase. Science. 2002;296(5577):2391-2394. google scholar
  • Szaflarska-Poplawska A, Siomek A, Czerwionka-Szaflarska M, et al. Oxidatively damaged DNA/oxidative stress in chil-dren with celiac disease. Cancer Epidemiol Biomarkers Prev. 2010;19(8):1960-1965. google scholar
  • Husby S, Koletzko S, Korponay-Szabo IR, et al. European Society for Pediatric Gastroenterology, Hepatology, and Nutrition guide-lines for the diagnosis of coeliac disease. J Pediatr Gastroenterol Nutr. 2012;54(1):136-160. google scholar
  • Bradley PP, Priebat DA, Christensen RD, Rothstein G. Measure-ment of cutaneous inflammation: Estimation of neutrophil content with an enzyme marker. J Invest Dermatol. 1982;78(3):206-209. google scholar
  • Sedlak J, Lindsay RH. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem. 1968;25(1):192-205. google scholar
  • Charlton-Menys V, Liu Y, Durrington PN. Semiautomated method for determination of serum paraoxonase activity using paraoxon as substrate. Clin Chem. 2006;52(3):453-457. google scholar
  • Cayir Y, Cayir A, Turan MI, et al. Antioxidant status in blood of obese children: The relation between trace elements, paraoxonase, and arylesterase values. Biol Trace Elem Res. 2014;160(2):155-160. google scholar Shahbazkhani B, Forootan M, Merat S, et al. Coeliac disease presenting with symptoms of irritable bowel syndrome. Aliment Pharmacol Ther. 2003;18(2):231-235. google scholar
  • Halliwell B. How to characterize a biological antioxidant. Free Radic Res Commun. 1990;9(1):1-32. google scholar
  • Pham-Huy LA, He H, Pham-Huy C. Free radicals, antioxidants in disease and health. Int J Biomed Sci. 2008;4(2):89-96. google scholar
  • Fasano A, Catassi C. Clinical practice. Celiac disease. N Engl J Med. 2012;367(25):2419-2426. google scholar
  • Olinski R, Gackowski D, Rozalski R, Foksinski M, Bialkowski K. Oxidative DNA damage in cancer patients: A cause or a con-sequence of the disease development? Mutat Res. 2003;531(1-2):177-190. google scholar
  • Stojiljkovic V, Todorovic A, Radlovic N, et al. Antioxidant en-zymes, glutathione and lipid peroxidation in peripheral blood of children affected by coeliac disease. Ann Clin Biochem. 2007;44(Pt 6):537-543. google scholar
  • Wang CF, Cui CX, Li N, et al. Antioxidant activity and pro-tective effect of wheat germ peptides in an in vitro celiac dis-ease model via Keap1/Nrf2 signaling pathway. Food Res Int. 2022;161.doi:ARTN 11186410.1016/j.foodres.2022.111864 google scholar
  • Rowicka G, Czaja-Bulsa G, Chelchowska M, et al. Oxidative and antioxidative status of children with celiac disease treated with a gluten free-diet. Oxid Med Cell Longev. 2018:1324820. doi:10.1155/2018/1324820 google scholar
  • Stojiljkovic V, Pejic S, Kasapovic J, et al. Glutathione redox cycle in small intestinal mucosa and peripheral blood of pediatric celiac disease patients. An Acad Bras Cienc. 2012;84(1):175-184. google scholar
  • Di Stefano M, Miceli E, Mengoli C, Corazza GR, Di Sabatino A. The effect of a gluten-free diet on vitamin D metabolism in celiac disease: The state of the art. Metabolites. 2023;13(1).doi:ARTN 7410.3390/metabo13010074 google scholar
  • Franckilin LRD, Dos Santos ACPM, Freitas FEDA, et al. Gluten: Do only celiac patients benefit from its removal from the diet?Food Rev Int. 2022;doi:10.1080/87559129.2021.2024566 google scholar
  • Hogberg L, Webb C, Falth-Magnusson K, et al. Children with screening-detected coeliac disease show increased levels of nitric oxide products in urine. Acta Paediatr. 2011;100(7):1023-1027. google scholar
  • Sayar E, Ozdem S, Uzun G, Islek A, Yilmaz A, Artan R. Total oxidant status, total antioxidant capacity and ischemia modified albumin levels in children with celiac disease. Turk J Pediatr. 2015;57(5):498-503. google scholar
  • Ferretti G, Bacchetti T, Saturni L, et al. Lipid peroxidation and paraoxonase-1 activity in celiac disease. J Lipids. 2012;587479. doi:10.1155/2012/587479 google scholar
  • Stojiljkovic V, Todorovic A, Pejic S, et al. Antioxidant status and lipid peroxidation in small intestinal mucosa of children with celiac disease. Clin Biochem. 2009;42(13-14):1431-1437. google scholar
  • Shamir R, Hartman C, Karry R, et al. Paraoxonases (PONs) 1, 2, and 3 are expressed in human and mouse gastrointestinal tract and in Caco-2 cell line: Selective secretion of PON1 and PON2. Free Radical Bio Med. 2005;39(3):336-344. google scholar
  • Rothem L, Hartman C, Dahan A, Lachter J, Eliakim R, Shamir R. Paraoxonases are associated with intestinal inflammatory diseases and intracellularly localized to the endoplasmic reticulum. Free Radic Biol Med. 2007;43(5):730-739. google scholar
  • Kaplan M, Ates I, Yuksel M, et al. The Role of oxidative stress in the etiopathogenesis of gluten-sensitive enteropathy disease. J Med Biochem. 2017;36(3):243-250. google scholar
  • Maluf SW, Wilhelm Filho D, Parisotto EB, et al. DNA damage, oxidative stress, and inflammation in children with celiac disease. Genet Mol Biol. 2020;43(2):e20180390. doi:10.1590/1678-4685-GMB-2018-0390 google scholar
Toplam 41 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Biyokimya ve Hücre Biyolojisi (Diğer)
Bölüm Themed Articles - Research Articles
Yazarlar

Mehmet Ali Gül 0000-0002-5849-0116

Fatma Betül Özgeriş 0000-0002-4568-5782

Nezahat Kurt 0000-0002-1685-5332

Burcu Volkan 0000-0002-0528-3826

Ali İşlek 0000-0001-6172-7797

Atilla Çayır 0000-0001-9776-555X

Yayımlanma Tarihi 21 Aralık 2023
Gönderilme Tarihi 8 Haziran 2023
Yayımlandığı Sayı Yıl 2023 Cilt: 82 Sayı: 2

Kaynak Göster

AMA Gül MA, Özgeriş FB, Kurt N, Volkan B, İşlek A, Çayır A. Effect of Gluten-Free Diet on Serum Antioxidant Levels in Children with Celiac. Eur J Biol. Aralık 2023;82(2):263-269. doi:10.26650/EurJBiol.2023.1307239