Correlation of Autoimmune Thyroid Diseases With Helicobacter pylori Infection
,
Abstract
Autoimmune thyroid diseases are multifactorial conditions caused by genetic and environmental factors. Among environmental factors, infectious agents include viruses, bacteria, and parasites acting as triggers. The current study intended to investigate the association between Helicobacter pylori infection and autoimmune thyroid diseases in a group of Iranian cases with Hashimoto's thyroiditis (HT) and Graves' disease (GD). This study included adult cases newly diagnosed with GD and HT and euthyroid controls. A number of clinical and biochemical factors were evaluated, including tests of thyroid function and serum Helicobacter Ab (IgG), and then inter-group comparisons were performed. Data from 404 patients with HT and 248 cases with GD were analyzed. Also, data from 480 healthy controls were analyzed. For those with HT, GD, and controls, the prevalence of Helicobacter pylori infection was 93.3%, 92.7%, and 88.8%, respectively. The prevalence of H. pylori infection in cases with HT and GD was significantly higher compared to controls. While concerning the prevalence of H. pylori infection, the two groups (HT and GD) were not significantly different. H. pylori antibody level was significantly correlated with FT4, FT3, Anti-TPO, and Anti-Tg in cases with HT. In the group of patients with GD, the H. pylori antibody had a significant positive correlation with Anti-TPO and Anti-Tg. According to the present results, H. pylori is associated with autoimmune thyroid diseases (both Hashimoto's and Graves' diseases).
1. Dong YH, Fu DG. Autoimmune thyroid disease: mechanism, genetics and current knowledge. Eur Rev Med Pharmacol Sci 2014;18:3611-8.
2. Bogdanos DP, Smyk DS, Invernizzi P, Rigopoulou EI, Blank M, Pouria S, et al. Infectome: a platform to trace infectious triggers of autoimmunity. Autoimmun Rev 2013;12:726-40.
3. Hargreaves CE, Grasso M, Hampe CS, Stenkova A, Atkinson S, Joshua GW, et al. Yersinia enterocolitica provides the link between thyroid-stimulating antibodies and their germline counterparts in Graves' disease. J Immunol 2013;190:5373-81.
4. Antonelli A, Ferri C, Fallahi P, Ferrari SM, Ghinoi A, Rotondi M, et al. Thyroid disorders in chronic hepatitis C virus infection. Thyroid 2006;16:563-72.
5. Valtonen VV, Ruutu P, Varis K, Ranki M, Malkamaki M, Makela PH. Serological evidence for the role of bacterial infections in the pathogenesis of thyroid diseases. Acta Med Scand 1986;219:105-11.
6. Figura N, Di Cairano G, Moretti E, Iacoponi F, Santucci A, Bernardini G, et al. Helicobacter pylori Infection and Autoimmune Thyroid Diseases: The Role of Virulent Strains. Antibiotics (Basel) 2019;9:12.
7. Konturek SJ, Konturek PC, Konturek JW, Plonka M, Czesnikiewicz-Guzik M, Brzozowski T, et al. Helicobacter pylori and its involvement in gastritis and peptic ulcer formation. J Physiol Pharmacol 2006;57:29-50.
8. Bassi V, Santinelli C, Iengo A, Romano C. Identification of a correlation between Helicobacter pylori infection and Graves' disease. Helicobacter 2010;15:558-62.
9. Beswick EJ, Suarez G, Reyes VE. H pylori and host interactions that influence pathogenesis. World J Gastroenterol 2006;12:5599-605.
10. Wotherspoon AC, Ortiz-Hidalgo C, Falzon MR, Isaacson PG. Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet 1991;338:1175-6.
11. Parsonnet J. Helicobacter pylori and gastric cancer. Gastroenterol Clin North Am 1993;22:89-104.
12. Umit H, Umit EG. Helicobacter pylori and mean platelet volume: a relation way before immune thrombocytopenia? Eur Rev Med Pharmacol Sci 2015;19:2818-23.
13. Candelli M, Rigante D, Schiavino A, Gabrielli M, Crea F, Minguell Del Lungo L, et al. High reinfection rate of Helicobacter pylori in young type 1 diabetic patients: a three-year follow-up study. Eur Rev Med Pharmacol Sci 2012;16:1468-72.
14. Han X, Li Y, Wang J, Liu B, Hu H, Li X, et al. Helicobacter pylori infection is associated with type 2 diabetes among a middle- and old-age Chinese population. Diabetes Metab Res Rev 2016;32:95-101.
15. Pullen R. A Clinical Review of Primary Biliary Cholangitis. Gastroenterol Nurs 2020;43:E48-55.
16. Gasbarrini A, Serricchio M, Tondi P, Gasbarrini G, Pola P. Association of Helicobacter pylori infection with primary Raynaud phenomenon. Lancet 1996;348:966-7.
17. Gasbarrini A, De Luca A, Fiore G, Gambrielli M, Franceschi F, Ojetti V, et al. Beneficial effects of Helicobacter pylori eradication on migraine. Hepatogastroenterology 1998;45:765-70.
18. Eskandarian R, Malek M, Mousavi SH, Babaei M. Association of Helicobacter pylori infection with cardiac syndrome X. Singapore Med J 2006;47:704-6.
19. de Luis DA, Varela C, de La Calle H, Canton R, de Argila CM, San Roman AL, et al. Helicobacter pylori infection is markedly increased in patients with autoimmune atrophic thyroiditis. J Clin Gastroenterol 1998;26:259-63.
20. Figura N, Di Cairano G, Lore F, Guarino E, Gragnoli A, Cataldo D, et al. The infection by Helicobacter pylori strains expressing CagA is highly prevalent in women with autoimmune thyroid disorders. J Physiol Pharmacol 1999;50:817-26.
21. Bassi V, Marino G, Iengo A, Fattoruso O, Santinelli C. Autoimmune thyroid diseases and Helicobacter pylori: the correlation is present only in Graves's disease. World J Gastroenterol 2012;18:1093-7.
22. Aghili R, Jafarzadeh F, Ghorbani R, Khamseh ME, Salami MA, Malek M. The association of Helicobacter pylori infection with Hashimoto's thyroiditis. Acta Med Iran
2013;51:293-6.
23. Soveid M, Hosseini Asl K, Omrani GR. Infection by Cag A positive strains of Helicobacter pylori is associated with autoimmune thyroid disease in Iranian patients. Iran J Immunol 2012;9:48-52.
24. Delitala AP, Pes GM, Errigo A, Maioli M, Delitala G, Dore MP. Helicobacter pylori CagA antibodies and thyroid function in latent autoimmune diabetes in adults. Eur Rev Med Pharmacol Sci 2016;20:4041-7.
25. Hou Y, Sun W, Zhang C, Wang T, Guo X, Wu L, et al. Meta-analysis of the correlation between Helicobacter pylori infection and autoimmune thyroid diseases. Oncotarget 2017;8:115691-700.
26. Shi WJ, Liu W, Zhou XY, Ye F, Zhang GX. Associations of Helicobacter pylori infection and cytotoxin-associated gene A status with autoimmune thyroid diseases: a meta-analysis. Thyroid 2013;23:1294-300.
27. Choi YM, Kim TY, Kim EY, Jang EK, Jeon MJ, Kim WG, et al. Association between thyroid autoimmunity and Helicobacter pylori infection. Korean J Intern Med 2017;32:309-13.
28. Sterzl I, Hrda P, Potuznikova B, Matucha P, Hana V, Zamrazil V. Autoimmune thyroiditis and Helicobacter pylori--is there a connection? Neuro Endocrinol Lett 2006;27:41-5.
29. Tomasi PA, Dore MP, Fanciulli G, Sanciu F, Realdi G, Delitala G. Is there anything to the reported association between Helicobacter pylori infection and autoimmune thyroiditis? Dig Dis Sci 2005;50:385-8.
30. Franceschi F, Satta MA, Mentella MC, Penland R, Candelli M, Grillo RL, et al. Helicobacter pylori infection in patients with Hashimoto's thyroiditis. Helicobacter 2004;9:369.
31. Shmuely H, Shimon I, Gitter LA. Helicobacter pylori infection in women with Hashimoto thyroiditis: A case-control study. Medicine (Baltimore) 2016;95:e4074.
32. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD, et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997;388:539-47.
33. Faria C, Zakout R, Araujo M. Helicobacter pylori and autoimmune diseases. Biomed Pharmacother 2013;67:347-9.
34. Fakheri H, Saberi Firoozi M, Bari Z. Eradication of Helicobacter Pylori in Iran: A Review. Middle East J Dig Dis 2018;10:5-17.
35. Graham DY, Osato MS, Olson CA, Zhang J, Figura N. Effect of H. pylori infection and CagA status on leukocyte counts and liver function tests: extra-gastric manifestations of H. pylori infection. Helicobacter 1998;3:174-8.
36. Perri F, Clemente R, Festa V, De Ambrosio CC,Quitadamo M, Fusillo M, et al. Serum tumour necrosis factor-alpha is increased in patients with Helicobacter pylori infection and CagA antibodies. Ital J Gastroenterol Hepatol 1999;31:290-4.
37. Patel P, Mendall MA, Khulusi S, Northfield TC, Strachan DP. Helicobacter pylori infection in childhood: risk factors and effect on growth. BMJ 1994;309:1119-23.
38. Getts MT, Miller SD. 99th Dahlem conference on infection, inflammation and chronic inflammatory disorders: triggering of autoimmune diseases by infections. Clin Exp Immunol 2010;160:15-21.
39. Fujinami RS, von Herrath MG, Christen U, Whitton JL. Molecular mimicry, bystander activation, or viral persistence: infections and autoimmune disease. Clin Microbiol Rev 2006;19:80-94.
40. McCoy L, Tsunoda I, Fujinami RS. Multiple sclerosis and virus induced immune responses: autoimmunity can be primed by molecular mimicry and augmented by bystander activation. Autoimmunity 2006;39:9-19.
41. Roner S, Zinser E, Menges M, Wiethe C, Littmann L, Hanig J, et al. Minor role of bystander tolerance to fetal
calf serum in a peptide-specific dendritic cell vaccine model against autoimmunity: comparison with serum-free cultures. J Immunother 2008;31:656-64.
42. Ram M, Shoenfeld Y. Hepatitis B: infection, vaccination and autoimmunity. Isr Med Assoc J 2008;10:61-4.
43. Ravel G, Christ M, Horand F, Descotes J. Autoimmunity, environmental exposure and vaccination: is there a link? Toxicology 2004;196:211-6.
44. Vial T, Descotes J. Autoimmune diseases and vaccinations. Eur J Dermatol 2004;14:86-90.
45. Ko GH, Park HB, Shin MK, Park CK, Lee JH, Youn HS, et al. Monoclonal antibodies against Helicobacter pylori cross-react with human tissue. Helicobacter 1997;2:210-5.
46. Raj P, Thompson JF, Pan DH. Helicobacter pylori serology testing is a useful diagnostic screening tool for symptomatic inner city children. Acta Paediatr 2017;106:470-7.
47. Raeiszadeh M, Massoud A, Siavoshi F, Malekzadeh R. IgG immune responses to different proteins of Helicobacter Pylori as defined by immunoblot assay. Acta Med Iran 2000;38:92-9.
2. Bogdanos DP, Smyk DS, Invernizzi P, Rigopoulou EI, Blank M, Pouria S, et al. Infectome: a platform to trace infectious triggers of autoimmunity. Autoimmun Rev 2013;12:726-40.
3. Hargreaves CE, Grasso M, Hampe CS, Stenkova A, Atkinson S, Joshua GW, et al. Yersinia enterocolitica provides the link between thyroid-stimulating antibodies and their germline counterparts in Graves' disease. J Immunol 2013;190:5373-81.
4. Antonelli A, Ferri C, Fallahi P, Ferrari SM, Ghinoi A, Rotondi M, et al. Thyroid disorders in chronic hepatitis C virus infection. Thyroid 2006;16:563-72.
5. Valtonen VV, Ruutu P, Varis K, Ranki M, Malkamaki M, Makela PH. Serological evidence for the role of bacterial infections in the pathogenesis of thyroid diseases. Acta Med Scand 1986;219:105-11.
6. Figura N, Di Cairano G, Moretti E, Iacoponi F, Santucci A, Bernardini G, et al. Helicobacter pylori Infection and Autoimmune Thyroid Diseases: The Role of Virulent Strains. Antibiotics (Basel) 2019;9:12.
7. Konturek SJ, Konturek PC, Konturek JW, Plonka M, Czesnikiewicz-Guzik M, Brzozowski T, et al. Helicobacter pylori and its involvement in gastritis and peptic ulcer formation. J Physiol Pharmacol 2006;57:29-50.
8. Bassi V, Santinelli C, Iengo A, Romano C. Identification of a correlation between Helicobacter pylori infection and Graves' disease. Helicobacter 2010;15:558-62.
9. Beswick EJ, Suarez G, Reyes VE. H pylori and host interactions that influence pathogenesis. World J Gastroenterol 2006;12:5599-605.
10. Wotherspoon AC, Ortiz-Hidalgo C, Falzon MR, Isaacson PG. Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet 1991;338:1175-6.
11. Parsonnet J. Helicobacter pylori and gastric cancer. Gastroenterol Clin North Am 1993;22:89-104.
12. Umit H, Umit EG. Helicobacter pylori and mean platelet volume: a relation way before immune thrombocytopenia? Eur Rev Med Pharmacol Sci 2015;19:2818-23.
13. Candelli M, Rigante D, Schiavino A, Gabrielli M, Crea F, Minguell Del Lungo L, et al. High reinfection rate of Helicobacter pylori in young type 1 diabetic patients: a three-year follow-up study. Eur Rev Med Pharmacol Sci 2012;16:1468-72.
14. Han X, Li Y, Wang J, Liu B, Hu H, Li X, et al. Helicobacter pylori infection is associated with type 2 diabetes among a middle- and old-age Chinese population. Diabetes Metab Res Rev 2016;32:95-101.
15. Pullen R. A Clinical Review of Primary Biliary Cholangitis. Gastroenterol Nurs 2020;43:E48-55.
16. Gasbarrini A, Serricchio M, Tondi P, Gasbarrini G, Pola P. Association of Helicobacter pylori infection with primary Raynaud phenomenon. Lancet 1996;348:966-7.
17. Gasbarrini A, De Luca A, Fiore G, Gambrielli M, Franceschi F, Ojetti V, et al. Beneficial effects of Helicobacter pylori eradication on migraine. Hepatogastroenterology 1998;45:765-70.
18. Eskandarian R, Malek M, Mousavi SH, Babaei M. Association of Helicobacter pylori infection with cardiac syndrome X. Singapore Med J 2006;47:704-6.
19. de Luis DA, Varela C, de La Calle H, Canton R, de Argila CM, San Roman AL, et al. Helicobacter pylori infection is markedly increased in patients with autoimmune atrophic thyroiditis. J Clin Gastroenterol 1998;26:259-63.
20. Figura N, Di Cairano G, Lore F, Guarino E, Gragnoli A, Cataldo D, et al. The infection by Helicobacter pylori strains expressing CagA is highly prevalent in women with autoimmune thyroid disorders. J Physiol Pharmacol 1999;50:817-26.
21. Bassi V, Marino G, Iengo A, Fattoruso O, Santinelli C. Autoimmune thyroid diseases and Helicobacter pylori: the correlation is present only in Graves's disease. World J Gastroenterol 2012;18:1093-7.
22. Aghili R, Jafarzadeh F, Ghorbani R, Khamseh ME, Salami MA, Malek M. The association of Helicobacter pylori infection with Hashimoto's thyroiditis. Acta Med Iran
2013;51:293-6.
23. Soveid M, Hosseini Asl K, Omrani GR. Infection by Cag A positive strains of Helicobacter pylori is associated with autoimmune thyroid disease in Iranian patients. Iran J Immunol 2012;9:48-52.
24. Delitala AP, Pes GM, Errigo A, Maioli M, Delitala G, Dore MP. Helicobacter pylori CagA antibodies and thyroid function in latent autoimmune diabetes in adults. Eur Rev Med Pharmacol Sci 2016;20:4041-7.
25. Hou Y, Sun W, Zhang C, Wang T, Guo X, Wu L, et al. Meta-analysis of the correlation between Helicobacter pylori infection and autoimmune thyroid diseases. Oncotarget 2017;8:115691-700.
26. Shi WJ, Liu W, Zhou XY, Ye F, Zhang GX. Associations of Helicobacter pylori infection and cytotoxin-associated gene A status with autoimmune thyroid diseases: a meta-analysis. Thyroid 2013;23:1294-300.
27. Choi YM, Kim TY, Kim EY, Jang EK, Jeon MJ, Kim WG, et al. Association between thyroid autoimmunity and Helicobacter pylori infection. Korean J Intern Med 2017;32:309-13.
28. Sterzl I, Hrda P, Potuznikova B, Matucha P, Hana V, Zamrazil V. Autoimmune thyroiditis and Helicobacter pylori--is there a connection? Neuro Endocrinol Lett 2006;27:41-5.
29. Tomasi PA, Dore MP, Fanciulli G, Sanciu F, Realdi G, Delitala G. Is there anything to the reported association between Helicobacter pylori infection and autoimmune thyroiditis? Dig Dis Sci 2005;50:385-8.
30. Franceschi F, Satta MA, Mentella MC, Penland R, Candelli M, Grillo RL, et al. Helicobacter pylori infection in patients with Hashimoto's thyroiditis. Helicobacter 2004;9:369.
31. Shmuely H, Shimon I, Gitter LA. Helicobacter pylori infection in women with Hashimoto thyroiditis: A case-control study. Medicine (Baltimore) 2016;95:e4074.
32. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD, et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997;388:539-47.
33. Faria C, Zakout R, Araujo M. Helicobacter pylori and autoimmune diseases. Biomed Pharmacother 2013;67:347-9.
34. Fakheri H, Saberi Firoozi M, Bari Z. Eradication of Helicobacter Pylori in Iran: A Review. Middle East J Dig Dis 2018;10:5-17.
35. Graham DY, Osato MS, Olson CA, Zhang J, Figura N. Effect of H. pylori infection and CagA status on leukocyte counts and liver function tests: extra-gastric manifestations of H. pylori infection. Helicobacter 1998;3:174-8.
36. Perri F, Clemente R, Festa V, De Ambrosio CC,Quitadamo M, Fusillo M, et al. Serum tumour necrosis factor-alpha is increased in patients with Helicobacter pylori infection and CagA antibodies. Ital J Gastroenterol Hepatol 1999;31:290-4.
37. Patel P, Mendall MA, Khulusi S, Northfield TC, Strachan DP. Helicobacter pylori infection in childhood: risk factors and effect on growth. BMJ 1994;309:1119-23.
38. Getts MT, Miller SD. 99th Dahlem conference on infection, inflammation and chronic inflammatory disorders: triggering of autoimmune diseases by infections. Clin Exp Immunol 2010;160:15-21.
39. Fujinami RS, von Herrath MG, Christen U, Whitton JL. Molecular mimicry, bystander activation, or viral persistence: infections and autoimmune disease. Clin Microbiol Rev 2006;19:80-94.
40. McCoy L, Tsunoda I, Fujinami RS. Multiple sclerosis and virus induced immune responses: autoimmunity can be primed by molecular mimicry and augmented by bystander activation. Autoimmunity 2006;39:9-19.
41. Roner S, Zinser E, Menges M, Wiethe C, Littmann L, Hanig J, et al. Minor role of bystander tolerance to fetal
calf serum in a peptide-specific dendritic cell vaccine model against autoimmunity: comparison with serum-free cultures. J Immunother 2008;31:656-64.
42. Ram M, Shoenfeld Y. Hepatitis B: infection, vaccination and autoimmunity. Isr Med Assoc J 2008;10:61-4.
43. Ravel G, Christ M, Horand F, Descotes J. Autoimmunity, environmental exposure and vaccination: is there a link? Toxicology 2004;196:211-6.
44. Vial T, Descotes J. Autoimmune diseases and vaccinations. Eur J Dermatol 2004;14:86-90.
45. Ko GH, Park HB, Shin MK, Park CK, Lee JH, Youn HS, et al. Monoclonal antibodies against Helicobacter pylori cross-react with human tissue. Helicobacter 1997;2:210-5.
46. Raj P, Thompson JF, Pan DH. Helicobacter pylori serology testing is a useful diagnostic screening tool for symptomatic inner city children. Acta Paediatr 2017;106:470-7.
47. Raeiszadeh M, Massoud A, Siavoshi F, Malekzadeh R. IgG immune responses to different proteins of Helicobacter Pylori as defined by immunoblot assay. Acta Med Iran 2000;38:92-9.
| Files | ||
| Issue | Vol 60 No 10 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/acta.v60i10.11555 | |
| Keywords | ||
| Graves’ disease Hashimoto’s disease Helicobacter pylori | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Heidari Z, Shahriari N. Correlation of Autoimmune Thyroid Diseases With Helicobacter pylori Infection. Acta Med Iran. 2022;60(10):628-634.
