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Helicobacter pylori seropositivity in patients with ankylosing spondylitis: What does it imply?

Yıl 2025, EARLY ONLINE, 1 - 10
https://doi.org/10.18621/eurj.1726121

Öz

Objectives: This study investigates clinical factors associated with Helicobacter pylori (H. pylori) seropositivity in patients with ankylosing spondylitis (AS), a condition in which H. pylori has been underexplored.

Methods: AS patients meeting the modified New York criteria, aged 18-65 years, without comorbidities and followed between 2022 and 2023, were included. Serum anti-H. pylori IgG and IgA antibodies were measured using ELISA and categorized as negative, positive, or highly positive based on titer levels.

Results: The cohort consisted of 243 patients, 36.8% males and 63.2% females, with a mean age of 46.6 years and a mean disease duration of 7.9 years. Logistic regression analysis revealed that increasing age significantly elevated the risk of both IgG and IgA seropositivity. Elevated erythrocyte sedimentation rate was strongly associated with IgA positivity (Odds Ratio [OR]: 3.08, 95% Confidence Interval [CI]: 2.05-4.11), while hypomagnesemia (mean serum Mg: 1.95±0.09) also increased the likelihood of IgA seropositivity (OR: 2.82, 95% CI: 1.05-2.88). Notably, hip involvement emerged as a robust predictor of IgG seropositivity (OR: 3.48, 95% CI: 1.52-6.04), and a history of uveitis was linked to a 1.61-fold increased risk of IgG positivity.

Conclusions: The findings suggest that older AS patients with systemic inflammation or low magnesium levels are more likely to exhibit H. pylori infection. Moreover, hip involvement and uveitis may serve as relevant clinical markers warranting H. pylori screening in this population. These associations highlight potential pathogenetic links between microbial triggers and disease expression in AS.

Etik Beyan

This study was approved by the Pamukkale University Non-Interventional Clinical Research Ethics Committeel (Decision No: 2019/20; date: 19.11.2019). All procedures were conducted in accordance with the ethical standards of the institutional and national research committee and with the 1964 Helsinki Declaration and its later amendments. Informed consent was waived because of the retrospective nature of the study and the analysis used anonymous clinical data.

Kaynakça

  • 1. Leja M, Grinberga-Derica I, Bilgilier C, Steininger C. Review: Epidemiology of Helicobacter pylori infection. Helicobacter. 2019;24 Suppl 1:e12635. doi: 10.1111/hel.12635.
  • 2. Gu J, He F, Clifford GM, et al. A systematic review and meta-analysis on the relative and attributable risk of Helicobacter pylori infection and cardia and non-cardia gastric cancer. Expert Rev Mol Diagn. 2023;23(12):1251-1261. doi: 10.1080/14737159.2023.2277377.
  • 3. Chen YC, Malfertheiner P, Yu HT, et al. Global Prevalence of Helicobacter pylori Infection and Incidence of Gastric Cancer Between 1980 and 2022. Gastroenterology. 2024;166(4):605-619. doi: 10.1053/j.gastro.2023.12.022.
  • 4. Etchegaray-Morales I, Jiménez-Herrera EA, Mendoza-Pinto C, et al. Helicobacter pylori and its association with autoimmune diseases: systemic lupus erythematosus, rheumatoid arthritis and Sjögren syndrome. J Transl Autoimmun. 2021;4:100135. doi: 10.1016/j.jtauto.2021.100135.
  • 5. Wang L, Cao ZM, Zhang LL, et al. Helicobacter Pylori and Autoimmune Diseases: Involving Multiple Systems. Front Immunol. 2022;13:833424. doi: 10.3389/fimmu.2022.833424.
  • 6. Radić M. Role of Helicobacter pylori infection in autoimmune systemic rheumatic diseases. World J Gastroenterol. 2014;20(36):12839-12846. doi: 10.3748/wjg.v20.i36.12839.
  • 7. Hwang MC, Ridley L, Reveille JD. Ankylosing spondylitis risk factors: a systematic literature review. Clin Rheumatol. 2021;40(8):3079-3093. doi: 10.1007/s10067-021-05679-7.
  • 8. Zhang X, Sun Z, Zhou A, et al. Association Between Infections and Risk of Ankylosing Spondylitis: A Systematic Review and Meta-Analysis. Front Immunol. 2021;12:768741. doi: 10.3389/fimmu.2021.768741.
  • 9. Su QY, Zhang Y, Qiao D, et al. Gut microbiota dysbiosis in ankylosing spondylitis: a systematic review and meta-analysis. Front Cell Infect Microbiol. 2024;14:1376525. doi: 10.3389/fcimb.2024.1376525.
  • 10. Bartels LE, Pedersen AB, Kristensen NR, Vilstrup H, Stengaard-Pedersen K, Dahlerup JF. A positive Helicobacter pylori test is associated with low spondylarthritis incidence in a Danish historical cohort study. Rheumatol Int. 2020;40(3):359-366. doi: 10.1007/s00296-019-04487-2.
  • 11. İnal EE, Aynalı A, Çanak S, et al. The Impacts of Helicobacter Pylori Antigen Positivity on Ankylosing Spondylitis. J Clin Anal Med 2016;7(3): 327-30. DOI:10.4328/JCAM.2767.
  • 12. Bilici R, Alp GT, Çelikdelen SÖ, Öztürk MA, Kekilli M. TNF ınhibitor resistance in ankylosing spondylitis: is Helicobacter pylori the overlooked culprit? Clin Rheumatol. 2025;44(8):3201-3207. doi: 10.1007/s10067-025-07536-3.
  • 13. Moll JM, Wright V. New York clinical criteria for ankylosing spondylitis. A statistical evaluation. Ann Rheum Dis. 1973;32(4):354-363. doi: 10.1136/ard.32.4.354.
  • 14. Albrecht J, Müller HA. HLA-B27 typing by use of flow cytofluorometry. Clin Chem. 1987;33(9):1619-1623.
  • 15. Bönisch A, Ehlebracht-König I. [The BASDAI-D--an instrument to defining disease status in ankylosing spondylitis and related diseases]. Z Rheumatol. 2003;62(3):251-263. doi: 10.1007/s00393-003-0519-6. [Article in German]
  • 16. Dhar R, Mustafa AS, Dhar PM, et al. Evaluation and comparison of two immunodiagnostic assays for Helicobacter pylori antibodies with culture results. Diagn Microbiol Infect Dis. 1998;30(1):1-6. doi: 10.1016/s0732-8893(97)00178-8.
  • 17. Lu J, Van Hoang D, Hayashi Y, et al. Negative-High Titer of Helicobacter pylori Antibody and Lipid Profiles. Biomed Res Int. 2022;2022:9984255. doi: 10.1155/2022/9984255.
  • 18. Otasevic L, Zlatanovic G, Stanojevic-Paovic A, et al. Helicobacter pylori: an underestimated factor in acute anterior uveitis and spondyloarthropathies? Ophthalmologica. 2007;221(1):6-13. doi: 10.1159/000096515.
  • 19. Pérez-Cano HJ, Ceja-Martínez J, Tellezgiron-Lara V, Voorduin-Ramos S, Morales-López O, Somilleda-Ventura SA. Relationship between Helicobacter pylori and undifferentiated non-granulomatous anterior uveitis. Infection. 2023;51(3):765-768. doi: 10.1007/s15010-022-01970-0.
  • 20. Markov G, Zdravkov Y, Oscar A. Helicobacter pylori and uveitis: a brief narrative literature review. Sriwijaya J Ophthalmol. 2023;6(2):276-278. doi:10.37275/sjo.v6i2.109.
  • 21. Ren S, Cai P, Liu Y, et al. Prevalence of Helicobacter pylori infection in China: A systematic review and meta-analysis. J Gastroenterol Hepatol. 2022;37(3):464-470. doi: 10.1111/jgh.15751.
  • 22. Moodley Y, Linz B, Bond RP, et al. Age of the association between Helicobacter pylori and man. PLoS Pathog. 2012;8(5):e1002693. doi: 10.1371/journal.ppat.1002693.
  • 23. Zaterka S, Eisig JN, Chinzon D, Rothstein W. Factors related to Helicobacter pylori prevalence in an adult population in Brazil. Helicobacter. 2007;12(1):82-88. doi: 10.1111/j.1523-5378.2007.00474.x.
  • 24. Franceschi F, Gasbarrini A, Polyzos SA, Kountouras J. Extragastric Diseases and Helicobacter pylori. Helicobacter. 2015 Sep;20 Suppl 1:40-46. doi: 10.1111/hel.12256.
  • 25. Liu G, Hao Y, Yang Q, Deng S. The Association of Fecal Microbiota in Ankylosing Spondylitis Cases with C-Reactive Protein and Erythrocyte Sedimentation Rate. Mediators Inflamm. 2020;2020:8884324. doi: 10.1155/2020/8884324.
  • 26. UstUn Y, Engin-UstUn Y, Ozkaplan E, Otlu B, Sait TekerekoGlu M. Association of Helicobacter pylori infection with systemic inflammation in preeclampsia. J Matern Fetal Neonatal Med. 2010;23(4):311-4. doi: 10.3109/14767050903121456.
  • 27. Kim TJ, Pyo JH, Lee H, et al. Lack of Association between Helicobacter pylori Infection and Various Markers of Systemic Inflammation in Asymptomatic Adults. Korean J Gastroenterol. 2018(25);72(1):21-27. doi: 10.4166/kjg.2018.72.1.21.
  • 28. Sağlam NÖ, Civan HA. Impact of chronic Helicobacter pylori infection on inflammatory markers and hematological parameters. Eur Rev Med Pharmacol Sci. 2023;27(3):969-979. doi: 10.26355/eurrev_202302_31190.
  • 29. Yalameha B, Nasri P. Helicobacter pylori infection and serum magnesium in kidney disease; current concepts. J Nephropharmacol. 2019;9(1):e11. doi: 10.15171/npj.2020.11.
  • 30. Hafizi M, Mardani S, Borhani A, Ahmadi A, Nasri P, Nasri H. Association of helicobacter pylori infection with serum magnesium in kidney transplant patients. J Renal Inj Prev. 2014(1);3(4):101-105. doi: 10.12861/jrip.2014.29.
  • 31. Baradaran A, Nasri H. Helicobacter pylori specific IgG antibody and serum magnesium in type-2 diabetes mellitus chronic kidney disease patients. Saudi J Kidney Dis Transpl. 2011;22(2):282-285.
  • 32. Öztürk N, Kurt N, Özgeriş FB, et al. Serum Zinc, Copper, Magnesium and Selenium Levels in Children with Helicobacter Pylori Infection. Eurasian J Med. 2015;47(2):126-129. doi: 10.5152/eurasianjmed.2015.104.
  • 33. Srinutta T, Chewcharat A, Takkavatakarn K, et al. Proton pump inhibitors and hypomagnesemia: A meta-analysis of observational studies. Medicine (Baltimore). 2019;98(44):e17788. doi: 10.1097/MD.0000000000017788.
  • 34. Liu Y, Jiang L, Cai Q, et al. Predominant association of HLA-B*2704 with ankylosing spondylitis in Chinese Han patients. Tissue Antigens. 2010;75(1):61-64. doi: 10.1111/j.1399-0039.2009.01379.x.
  • 35. Liu G, Ma Y, Yang Q, Deng S. Modulation of inflammatory response and gut microbiota in ankylosing spondylitis mouse model by bioactive peptide IQW. J Appl Microbiol. 2020;128(6):1669-1677. doi: 10.1111/jam.14588.
  • 36. Berland M, Meslier V, Berreira Ibraim S, et al. Both Disease Activity and HLA-B27 Status Are Associated With Gut Microbiome Dysbiosis in Spondyloarthritis Patients. Arthritis Rheumatol. 2023;75(1):41-52. doi: 10.1002/art.42289.
Yıl 2025, EARLY ONLINE, 1 - 10
https://doi.org/10.18621/eurj.1726121

Öz

Kaynakça

  • 1. Leja M, Grinberga-Derica I, Bilgilier C, Steininger C. Review: Epidemiology of Helicobacter pylori infection. Helicobacter. 2019;24 Suppl 1:e12635. doi: 10.1111/hel.12635.
  • 2. Gu J, He F, Clifford GM, et al. A systematic review and meta-analysis on the relative and attributable risk of Helicobacter pylori infection and cardia and non-cardia gastric cancer. Expert Rev Mol Diagn. 2023;23(12):1251-1261. doi: 10.1080/14737159.2023.2277377.
  • 3. Chen YC, Malfertheiner P, Yu HT, et al. Global Prevalence of Helicobacter pylori Infection and Incidence of Gastric Cancer Between 1980 and 2022. Gastroenterology. 2024;166(4):605-619. doi: 10.1053/j.gastro.2023.12.022.
  • 4. Etchegaray-Morales I, Jiménez-Herrera EA, Mendoza-Pinto C, et al. Helicobacter pylori and its association with autoimmune diseases: systemic lupus erythematosus, rheumatoid arthritis and Sjögren syndrome. J Transl Autoimmun. 2021;4:100135. doi: 10.1016/j.jtauto.2021.100135.
  • 5. Wang L, Cao ZM, Zhang LL, et al. Helicobacter Pylori and Autoimmune Diseases: Involving Multiple Systems. Front Immunol. 2022;13:833424. doi: 10.3389/fimmu.2022.833424.
  • 6. Radić M. Role of Helicobacter pylori infection in autoimmune systemic rheumatic diseases. World J Gastroenterol. 2014;20(36):12839-12846. doi: 10.3748/wjg.v20.i36.12839.
  • 7. Hwang MC, Ridley L, Reveille JD. Ankylosing spondylitis risk factors: a systematic literature review. Clin Rheumatol. 2021;40(8):3079-3093. doi: 10.1007/s10067-021-05679-7.
  • 8. Zhang X, Sun Z, Zhou A, et al. Association Between Infections and Risk of Ankylosing Spondylitis: A Systematic Review and Meta-Analysis. Front Immunol. 2021;12:768741. doi: 10.3389/fimmu.2021.768741.
  • 9. Su QY, Zhang Y, Qiao D, et al. Gut microbiota dysbiosis in ankylosing spondylitis: a systematic review and meta-analysis. Front Cell Infect Microbiol. 2024;14:1376525. doi: 10.3389/fcimb.2024.1376525.
  • 10. Bartels LE, Pedersen AB, Kristensen NR, Vilstrup H, Stengaard-Pedersen K, Dahlerup JF. A positive Helicobacter pylori test is associated with low spondylarthritis incidence in a Danish historical cohort study. Rheumatol Int. 2020;40(3):359-366. doi: 10.1007/s00296-019-04487-2.
  • 11. İnal EE, Aynalı A, Çanak S, et al. The Impacts of Helicobacter Pylori Antigen Positivity on Ankylosing Spondylitis. J Clin Anal Med 2016;7(3): 327-30. DOI:10.4328/JCAM.2767.
  • 12. Bilici R, Alp GT, Çelikdelen SÖ, Öztürk MA, Kekilli M. TNF ınhibitor resistance in ankylosing spondylitis: is Helicobacter pylori the overlooked culprit? Clin Rheumatol. 2025;44(8):3201-3207. doi: 10.1007/s10067-025-07536-3.
  • 13. Moll JM, Wright V. New York clinical criteria for ankylosing spondylitis. A statistical evaluation. Ann Rheum Dis. 1973;32(4):354-363. doi: 10.1136/ard.32.4.354.
  • 14. Albrecht J, Müller HA. HLA-B27 typing by use of flow cytofluorometry. Clin Chem. 1987;33(9):1619-1623.
  • 15. Bönisch A, Ehlebracht-König I. [The BASDAI-D--an instrument to defining disease status in ankylosing spondylitis and related diseases]. Z Rheumatol. 2003;62(3):251-263. doi: 10.1007/s00393-003-0519-6. [Article in German]
  • 16. Dhar R, Mustafa AS, Dhar PM, et al. Evaluation and comparison of two immunodiagnostic assays for Helicobacter pylori antibodies with culture results. Diagn Microbiol Infect Dis. 1998;30(1):1-6. doi: 10.1016/s0732-8893(97)00178-8.
  • 17. Lu J, Van Hoang D, Hayashi Y, et al. Negative-High Titer of Helicobacter pylori Antibody and Lipid Profiles. Biomed Res Int. 2022;2022:9984255. doi: 10.1155/2022/9984255.
  • 18. Otasevic L, Zlatanovic G, Stanojevic-Paovic A, et al. Helicobacter pylori: an underestimated factor in acute anterior uveitis and spondyloarthropathies? Ophthalmologica. 2007;221(1):6-13. doi: 10.1159/000096515.
  • 19. Pérez-Cano HJ, Ceja-Martínez J, Tellezgiron-Lara V, Voorduin-Ramos S, Morales-López O, Somilleda-Ventura SA. Relationship between Helicobacter pylori and undifferentiated non-granulomatous anterior uveitis. Infection. 2023;51(3):765-768. doi: 10.1007/s15010-022-01970-0.
  • 20. Markov G, Zdravkov Y, Oscar A. Helicobacter pylori and uveitis: a brief narrative literature review. Sriwijaya J Ophthalmol. 2023;6(2):276-278. doi:10.37275/sjo.v6i2.109.
  • 21. Ren S, Cai P, Liu Y, et al. Prevalence of Helicobacter pylori infection in China: A systematic review and meta-analysis. J Gastroenterol Hepatol. 2022;37(3):464-470. doi: 10.1111/jgh.15751.
  • 22. Moodley Y, Linz B, Bond RP, et al. Age of the association between Helicobacter pylori and man. PLoS Pathog. 2012;8(5):e1002693. doi: 10.1371/journal.ppat.1002693.
  • 23. Zaterka S, Eisig JN, Chinzon D, Rothstein W. Factors related to Helicobacter pylori prevalence in an adult population in Brazil. Helicobacter. 2007;12(1):82-88. doi: 10.1111/j.1523-5378.2007.00474.x.
  • 24. Franceschi F, Gasbarrini A, Polyzos SA, Kountouras J. Extragastric Diseases and Helicobacter pylori. Helicobacter. 2015 Sep;20 Suppl 1:40-46. doi: 10.1111/hel.12256.
  • 25. Liu G, Hao Y, Yang Q, Deng S. The Association of Fecal Microbiota in Ankylosing Spondylitis Cases with C-Reactive Protein and Erythrocyte Sedimentation Rate. Mediators Inflamm. 2020;2020:8884324. doi: 10.1155/2020/8884324.
  • 26. UstUn Y, Engin-UstUn Y, Ozkaplan E, Otlu B, Sait TekerekoGlu M. Association of Helicobacter pylori infection with systemic inflammation in preeclampsia. J Matern Fetal Neonatal Med. 2010;23(4):311-4. doi: 10.3109/14767050903121456.
  • 27. Kim TJ, Pyo JH, Lee H, et al. Lack of Association between Helicobacter pylori Infection and Various Markers of Systemic Inflammation in Asymptomatic Adults. Korean J Gastroenterol. 2018(25);72(1):21-27. doi: 10.4166/kjg.2018.72.1.21.
  • 28. Sağlam NÖ, Civan HA. Impact of chronic Helicobacter pylori infection on inflammatory markers and hematological parameters. Eur Rev Med Pharmacol Sci. 2023;27(3):969-979. doi: 10.26355/eurrev_202302_31190.
  • 29. Yalameha B, Nasri P. Helicobacter pylori infection and serum magnesium in kidney disease; current concepts. J Nephropharmacol. 2019;9(1):e11. doi: 10.15171/npj.2020.11.
  • 30. Hafizi M, Mardani S, Borhani A, Ahmadi A, Nasri P, Nasri H. Association of helicobacter pylori infection with serum magnesium in kidney transplant patients. J Renal Inj Prev. 2014(1);3(4):101-105. doi: 10.12861/jrip.2014.29.
  • 31. Baradaran A, Nasri H. Helicobacter pylori specific IgG antibody and serum magnesium in type-2 diabetes mellitus chronic kidney disease patients. Saudi J Kidney Dis Transpl. 2011;22(2):282-285.
  • 32. Öztürk N, Kurt N, Özgeriş FB, et al. Serum Zinc, Copper, Magnesium and Selenium Levels in Children with Helicobacter Pylori Infection. Eurasian J Med. 2015;47(2):126-129. doi: 10.5152/eurasianjmed.2015.104.
  • 33. Srinutta T, Chewcharat A, Takkavatakarn K, et al. Proton pump inhibitors and hypomagnesemia: A meta-analysis of observational studies. Medicine (Baltimore). 2019;98(44):e17788. doi: 10.1097/MD.0000000000017788.
  • 34. Liu Y, Jiang L, Cai Q, et al. Predominant association of HLA-B*2704 with ankylosing spondylitis in Chinese Han patients. Tissue Antigens. 2010;75(1):61-64. doi: 10.1111/j.1399-0039.2009.01379.x.
  • 35. Liu G, Ma Y, Yang Q, Deng S. Modulation of inflammatory response and gut microbiota in ankylosing spondylitis mouse model by bioactive peptide IQW. J Appl Microbiol. 2020;128(6):1669-1677. doi: 10.1111/jam.14588.
  • 36. Berland M, Meslier V, Berreira Ibraim S, et al. Both Disease Activity and HLA-B27 Status Are Associated With Gut Microbiome Dysbiosis in Spondyloarthritis Patients. Arthritis Rheumatol. 2023;75(1):41-52. doi: 10.1002/art.42289.
Toplam 36 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Romatoloji ve Artrit
Bölüm Original Article
Yazarlar

Firdevs Ulutaş 0000-0001-8441-5219

Veli Çobankara 0000-0001-5037-5327

Erken Görünüm Tarihi 13 Ağustos 2025
Yayımlanma Tarihi
Gönderilme Tarihi 24 Haziran 2025
Kabul Tarihi 9 Ağustos 2025
Yayımlandığı Sayı Yıl 2025 EARLY ONLINE

Kaynak Göster

AMA Ulutaş F, Çobankara V. Helicobacter pylori seropositivity in patients with ankylosing spondylitis: What does it imply?. Eur Res J. Published online 01 Ağustos 2025:1-10. doi:10.18621/eurj.1726121

e-ISSN: 2149-3189 


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