The Role of Viruses in Celiac Disease Pathogenesis: Current Status
https://doi.org/10.15690/pf.v21i4.2771
Abstract
The purpose of this review is to present modern data on the correlations between viruses and celiac disease. Some viruses probably have crucial role in celiac disease pathogenesis according to the results of recent studies. However, the virus exposure itself does not lead to the development of autoimmune disease. Number of studies have demonstrated that there are several viruses that can cause celiac disease, and several activation pathways leading to food tolerance loss. Thus far, the role of some reoviruses strains has been proven in the development of celiac disease. Further research is needed for better understanding of the viruses role in the celiac disease development and to improve management and prevention of this disease.
Supporting agencies: Not specified.
About the Authors
Anatoly I. Khavkin
Research Clinical Institute of Childhood; Belgorod State University
Russian Federation
Disclosure of interest:
Russian Federation
Anatoly I. Khavkin, MD, PhD, Professor
62, Bolshaya Serpukhovskaya Str., Moscow, 115093
tel.: +7 (499) 237-02-23
Disclosure of interest:
Not declared.
Andrew V. Nalyotov
Donetsk State Medical University named after M. Gorky
Russian Federation
Disclosure of interest:
Russian Federation
Andrew V. Nalyotov, MD, PhD, Professor
Donetsk
Disclosure of interest:
Not declared.
Polina I. Kuropjatnik
Central city clinical hospital No. 1
Russian Federation
Disclosure of interest:
Russian Federation
Polina I. Kuropjatnik, MD
Donetsk
Disclosure of interest:
Not declared.
References
1. Khavkin AI, Bystrova VI, Schreiner EV, et al. Celiac disease and vitamin-mineral deficiencies. Voprosy dietologii = Nutrition. 2024;14(1):54–60. doi: https://doi.org/10.20953/2224-5448-2024-1-54-60 (In Russ).
2. Khavkin АI, Bystrova VI, Schreiner ЕV, et al. Celiac disease: old problem, new solutions. Voprosy dietologii = Nutrition. 2023;13(4):64–71. (In Russ). doi: https://doi.org/10.20953/2224-5448-2023-4-64-71
3. Khavkin AI, Yablokova EA, Shapovalova NS, Erokhina MI. Gut microbiota and prospects for probiotics in paediatric celiac disease. Archives of Pediatrics and Pediatric Surgery. 2024;2(1):121–132. (In Russ). doi: https://doi.org/10.31146/2949-4664-apps-2-1-121-132
4. Shapovalova NS, Novikova VP, Yablokova EA, et al. Non-celiac gluten sensitivity: approaches to differential diagnosis and potential biomarkers. Voprosy detskoi dietologii = Pediatric Nutrition. 2023;21(2):32–44. (In Russ). doi: https://doi.org/10.20953/1727-5784-2023-2-32-44
5. Barone MV, Auricchio S. A cumulative effect of food and viruses to trigger celiac disease [CD]: a commentary on the recent literature. Int J Mol Sci. 2021;22(4):2027. doi: https://doi.org/10.3390/ijms22042027
6. Porpora M, Conte M, Lania G, et al. Inflammation is present, persistent and more sensitive to proinflammatory triggers in celiac disease enterocytes. Int J Mol Sci. 2022;23(4):1973. doi: https://doi.org/10.3390/ijms23041973
7. Hussein HM, Rahal EA. The role of viral infections in the development of autoimmune diseases. Crit Rev Microbiol. 2019;45(4):394–412. doi: https://doi.org/10.1080/1040841X.2019.1614904
8. Lernmark Å. Environmental factors in the etiology of type 1 diabetes, celiac disease, and narcolepsy. Pediatr Diabetes. 2016;17(Suppl 22):65–72. doi: https://doi.org/10.1111/pedi.12390 9. Brown JJ, Jabri B, Dermody TS. A viral trigger for celiac disease. PLoS Pathog. 2018;14(9):e1007181. doi: https://doi.org/10.1371/journal.ppat.1007181
9. Jeon JH, Kim IG. Role of protein modifications mediated by transglutaminase 2 in human viral diseases. Front Biosci. 2006;11:221–231. doi: https://doi.org/10.2741/1793 11. Ferrara F, Quaglia S, Caputo I, et al. Anti-transglutaminase antibodies in non-coeliac children suffering from infectious diseases. Clin Exp Immunol. 2010;159(2):217–223. doi: https://doi.org/10.1111/j.1365-2249.2009.04054.x
10. Bouziat R, Hinterleitner R, Brown JJ, et al. Reovirus infection triggers inflammatory responses to dietary antigens and development of celiac disease. Science. 2017;356(6333):44–50. doi: https:// doi.org/10.1126/science.aah5298
11. Brown JJ, Short SP, Stencel-Baerenwald J, et al. Reovirusinduced apoptosis in the intestine limits establishment of enteric infection. J Virol. 2018;92(10):e02062–e02117. doi: https://doi.org/10.1128/JVI.02062-17
12. Ramig RF. Systemic rotavirus infection. Expert Rev Anti Infect Ther. 2007;5(4):591–612. doi: https://doi.org/10.1586/14787210.5.4.591 15. Rivero-Calle I, Gomez-Rial J, Martinon-Torres F. Systemic features of rotavirus infection. J Infect. 2016;72(Suppl):S98–S105. doi: https://doi.org/10.1016/j.jinf.2016.04.029
13. Gomez-Rial J, Sanchez-Batan S, Rivero-Calle I, et al. Rotavirus infection beyond the gut. Infect Drug Resist. 2018;12:55–64. doi: https://doi.org/10.2147/IDR.S186404
14. Sadiq A, Khan J, Ullah I, et al. Seroprevalence of Anti-tTg-IgA among symptomized celiac disease patients and their correlation with rotavirus infection. Biomed Res Int. 2022;2022:6972624. doi: https://doi.org/10.1155/2022/6972624
15. Stene LC, Honeyman MC, Hoffenberg EJ, et al. Rotavirus infection frequency and risk of celiac disease autoimmunity in early childhood: a longitudinal study. Am J Gastroenterol. 2006;101(10):2333– 2340. doi: https://doi.org/10.1111/j.1572-0241.2006.00741.x
16. Zanoni G, Navone R, Lunardi C, et al. In celiac disease, a subset of autoantibodies against transglutaminase binds toll-like receptor 4 and induces activation of monocytes. PLoS Med. 2006;3(9):e358. doi: https://doi.org/10.1371/journal.pmed.0030358
17. Ziberna F, De Lorenzo G, Schiavon V, et al. Lack of evidence of rotavirus-dependent molecular mimicry as a trigger of celiac disease. Clin Exp Immunol. 2016;186(3):356–363. doi: https://doi.org/10.1111/cei.12855
18. Cho MJ, Ellebrecht CT, Hammers CM, et al. Determinants of VH1- 46 cross-reactivity to pemphigus vulgaris autoantigen desmoglein 3 and rotavirus antigen VP6. J Immunol. 2016;197(4):1065–1073. doi: https://doi.org/10.4049/jimmunol.1600567
19. Aliabadi N, Antoni S, Mwenda JM, et al. Global impact of rotavirus vaccine introduction on rotavirus hospitalisations among children under 5 years of age, 2008–16: findings from the global rotavirus surveillance network. Lancet Glob Health. 2019;7(7):e893–903. doi: https://doi.org/10.1016/S2214-109X(19)30207-4
20. Puccetti A, Saverino D, Opri R, et al. Immune response to rotavirus and gluten sensitivity. J Immunol Res. 2018;2018:9419204. doi: https://doi.org/10.1155/2018/9419204
21. Sarmiento L, Galvan JA, Cabrera-Rode E, et al. Type 1 diabetes associated and tissue transglutaminase autoantibodies in patients without type 1 diabetes and coeliac disease with confirmed viral infections. J Med Virol. 2012;84(7):1049–1053. doi: https://doi.org/10.1002/jmv.23305
22. Jansen MA, van den Heuvel D, van der Zwet KV, et al. Herpesvirus infections and transglutaminase type 2 antibody positivity in childhood: the generation R study. J Pediatr Gastroenterol Nutr. 2016;63(4):423–430. doi: https://doi.org/10.1097/MPG.0000000000001163
23. Jansen MAE, van den Heuvel D, Jaddoe VWV, et al. Abnormalities in CD57+ cytotoxic T cells and Vδ1 + γδT cells in subclinical celiac disease in childhood are affected by cytomegalovirus. The Generation R Study. Clin Immunol. 2017;183:233–239. doi: https://doi. org/10.1016/j.clim.2017.04.008
24. Calabretto M, Di Carlo D, Falasca F, et al. Analysis of viral nucleic acids in duodenal biopsies from adult patients with celiac disease. Eur J Gastroenterol Hepatol. 2022;34(11):1107–1110. doi: https:// doi.org/10.1097/MEG.0000000000002404
25. Perfetti V, Baldanti F, Lenti MV, et al. Detection of active epsteinbarr virus infection in duodenal mucosa of patients with refractory celiac disease. Clin Gastroenterol Hepatol. 2016;14(8):1216–20. doi: https://doi.org/10.1016/j.cgh.2016.03.022
26. Oikarinen M, Puustinen L, Lehtonen J, et al. Enterovirus infections are associated with the development of celiac disease in a birth cohort study. Front Immunol. 2021;11:604529. doi: https://doi.org/10.3389/fimmu.2020.604529
27. Lindfors K, Lin J, Lee HS, et al. TEDDY Study Group Metagenomics of the faecal virome indicate a cumulative efect of enterovirus and gluten amount on the risk of coeliac disease autoimmunity in genetically at risk children: the TEDDY study. Gut. 2020;69(8):1416– 1422. doi: https://doi.org/10.1136/gutjnl-2019-319809
28. Kahrs CR, Chuda K, Tapia G, et al. Enterovirus as trigger of coeliac disease: nested case-control study within prospective birth cohort. BMJ. 2019;364:l231. doi: https://doi.org/10.1136/bmj.l231
29. Khavkin AI, Bogdanova NM, Novikova VP. Biological role of zonulin: a biomarker of increased intestinal permeability syndrome. Rossiyskiy Vestnik Perinatologii i Pediatrii = Russian Bulletin of Perinatology and Pediatrics. 2021;66(1):31–38. (In Russ). doi: https://doi.org/10.21508/1027-4065-2021-66-1-31-38
30. Vorobjova T, Raikkerus H, Kadaja L, et al. Circulating zonulin correlates with density of enteroviruses and tolerogenic dendritic cells in the small bowel mucosa of celiac disease patients. Dig Dis Sci. 2017;62(2):358–371. doi: https://doi.org/10.1007/s10620-016-4403-z
31. Opri R, Veneri D, Mengoli C, Zanoni G. Immune response to Hepatitis B vaccine in patients with celiac disease: a systematic review and meta-analysis. Hum Vaccin Immunother. 2015;11(12):2800– 2805. doi: https://doi.org/10.1080/21645515.2015.1069448
32. Zifman E, Zevit N, Heshin-Bekenstein M, et al. Effect of a gluten free diet on hepatitis B surface antibody concentration in previously immunized pediatric celiac patients. Pediatr Gastroenterol Hepatol Nutr. 2020;23(2):132–136. doi: https://doi.org/10.5223/pghn.2020.23.2.132
33. Mormile R. Hepatitis B vaccine non response: a predictor of latent autoimmunity? Med Hypotheses. 2017;104:45–47. doi: https://doi.org/10.1016/j.mehy.2017.05.020 37. Leonardi S, La Rosa M. Are hepatitis B virus and celiac disease linked? Hepat Mon. 2010;10(3):173–175. 38. Habash N, Choung RS, Jacobson RM, et al. Celiac disease: risk of hepatitis B infection. J Pediatr Gastroenterol Nutr. 2022;74(3):328– 332. doi: https://doi.org/10.1097/MPG.0000000000003362
34. Jadali Z, Alavian SM. Autoimmune diseases co-existing with hepatitis C virus infection. Iran J Allergy Asthma Immunol. 2010;9(4):191–206.
35. Wakim-Fleming J, Pagadala MR, McCullough AJ, et al. Prevalence of celiac disease in cirrhosis and outcome of cirrhosis on a gluten free diet: a prospective study. J Hepatol. 2014;61(3):558–563. doi: https://doi.org/10.1016/j.jhep.2014.05.020
36. Durante-Mangoni E, Iardino P, Resse M, et al. Silent celiac disease in chronic hepatitis C: impact of interferon treatment on the disease onset and clinical outcome. J Clin Gastroenterol. 2004;38(10):901– 905. doi: https://doi.org/10.1097/00004836-200411000-00014
37. Casella G, Viganò D, Romano Settanni C, et al. Association between celiac disease and chronic hepatitis C. Gastroenterol Hepatol Bed Bench. 2016;9(3):153–157.
38. Casella G, Antonelli E, Di Bella C, et al. Prevalence and causes of abnormal liver function in patients with coeliac disease. Liver Int. 2013;33(7):1128–1131. doi: https://doi.org/10.1111/liv.12178
39. Gravina AG, Federico A, Masarone M, et al. Coeliac disease and C virus-related chronic hepatitis: a non association. BMC Res Notes. 2012;5:533. doi: https://doi.org/10.1186/1756-0500-5-533
40. Kårhus LL, Gunnes N, Størdal K, et al. Influenza and risk of later celiac disease: a cohort study of 2.6 million people. Scand J Gastroenterol. 2018;53(1):15–23. doi: https://doi.org/10.1080/ 00365521.2017.1362464
41. Mårild K, Fredlund H, Ludvigsson JF. Increased risk of hospital admission for influenza in patients with celiac disease: a nationwide cohort study in Sweden. Am J Gastroenterol. 2010;105(11):2465– 2473. doi: https://doi.org/10.1038/ajg.2010.352
42. Del Prete A, Scutera S, Sozzani S, Musso T. Role of osteopontin in dendritic cell shaping of immune responses. Cytokine Growth Factor Rev. 2019;50:19–28. doi: https://doi.org/10.1016/j.cytogfr.2019.05.004
43. Tjernberg AR, Ludvigsson JF. Children with celiac disease are more likely to have attended hospital for prior respiratory syncytial virus infection. Dig Dis Sci. 2014;59(7):1502–1508. doi: https://doi.org/10.1007/s10620-014-3046-1
Review
For citations:
Khavkin A.I., Nalyotov A.V., Kuropjatnik P.I. The Role of Viruses in Celiac Disease Pathogenesis: Current Status. Pediatric pharmacology. 2024;21(4):369-374. (In Russ.) https://doi.org/10.15690/pf.v21i4.2771
Views:
239
Email this article 