Skip to main content
SpringerLink
Log in

Helicobacter pylori infection contributes to high risk of ischemic stroke: evidence from a meta-analysis

  • Review
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Chronic infection of Helicobacter pylori (H. pylori) in ischemic stroke (IS) incidence has been previously studied in several publications; however, conflicting results have been reported. A meta-analysis was used to assess whether chronic infection of H. pylori was associated with risk of IS, and which of the following was more effective for predication of IS risk, antibody IgG of H. pylori (anti-H. pylori IgG), antibody IgG of cytotoxin-associated gene-A (anti-Cag A IgG) or the 13C-urea breath test. We searched the databases of Medline and Embase, and latest update was January 1, 2012. Case–control studies were considered to be eligible. The odds ratio (OR) and 95 % confidence interval (95 % CI) were calculated using the random-effect model. A total of 13 studies including 4,041 participants were included in this meta-analysis. Of these studies, ten, four and four studies were for anti-H. pylori IgG, anti-Cag A IgG and the 13C-urea breath test, respectively. Combined analysis indicated that positive anti-H. pylori IgG, anti-Cag A IgG and 13C-urea breath test were significantly associated with increased risk of IS, respectively, and positive anti-Cag A IgG was more effective for predication of IS risk [OR (95 % CI) = 1.60 (1.21–2.11), P heterogeneity = 0.001 for positive versus negative anti-H. pylori IgG; 2.33 (1.76–3.09), P heterogeneity = 0.71 for positive versus negative anti-Cag A IgG and 1.65 (1.11–2.47), P heterogeneity = 0.17 for positive versus negative 13C-urea breath test]. In addition, we found that positive anti-H. pylori IgG was closely associated with risk of IS caused by atherosclerosis and small artery disease, but not for cardioembolic IS. This meta-analysis indicated that chronic H. pylori infection was significantly associated with an increased risk of IS, especially for non-cardioembolic IS. Compared with anti-H. pylori IgG and the 13C-urea breath test, anti-Cag A IgG seemed more effective for prediction of risk of IS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Ford AC, Axon AT (2010) Epidemiology of Helicobacter pylori infection and public health implications. Helicobacter 15(Suppl 1):1–6

    Article  PubMed  Google Scholar 

  2. Suerbaum S, Michetti P (2002) Helicobacter pylori infection. N Engl J Med 347:1175–1186

    Article  PubMed  CAS  Google Scholar 

  3. Cavaleiro-Pinto M, Peleteiro B, Lunet N, Barros H (2011) Helicobacter pylori infection and gastric cardia cancer: systematic review and meta-analysis. Cancer Causes Control 22:375–387

    Article  PubMed  Google Scholar 

  4. Markus HS, Mendall MA (1998) Helicobacter pylori infection: a risk factor for ischaemic cerebrovascular disease and carotid atheroma. J Neurol Neurosurg Psychiatry 64:104–107

    Article  PubMed  CAS  Google Scholar 

  5. Heuschmann PU, Neureiter D, Gesslein M, Craiovan B, Maass M, Faller G, Beck G, Neundoerfer B, Kolominsky-Rabas PL (2001) Association between infection with Helicobacter pylori and Chlamydia pneumoniae and risk of ischemic stroke subtypes: Results from a population-based case-control study. Stroke 32:2253–2258

    Article  PubMed  CAS  Google Scholar 

  6. Majka J, Rog T, Konturek PC, Konturek SJ, Bielanski W, Kowalsky M, Szczudlik A (2002). Influence of chronic Helicobacter pylori infection on ischemic cerebral stroke risk factors. Med Sci Monit 8: CR675–684

    PubMed  Google Scholar 

  7. Langhorne P, Bernhardt J, Kwakkel G (2011) Stroke rehabilitation. Lancet 377:1693–1702

    Article  PubMed  Google Scholar 

  8. Li N, He Z, Xu J, Liu F, Deng S, Zhang H (2010) Association of PDE4D and IL-1 gene polymorphism with ischemic stroke in a Han Chinese population. Brain Res Bull 81:38–42

    Article  PubMed  CAS  Google Scholar 

  9. Gunarathne A, Patel JV, Gammon B, Gill PS, Hughes EA, Lip GY (2009) Ischemic stroke in South Asians: a review of the epidemiology, pathophysiology, and ethnicity-related clinical features. Stroke 40:e415–e423

    Article  PubMed  Google Scholar 

  10. Bhatnagar P, Scarborough P, Smeeton NC, Allender S (2010) The incidence of all stroke and stroke subtype in the United Kingdom, 1985 to 2008: a systematic review. BMC Public Health 10:539

    Article  PubMed  Google Scholar 

  11. Martin CO, Rymer MM (2011) Hemorrhagic stroke: aneurysmal subarachnoid hemorrhage. Mo Med 108:124–127

    PubMed  Google Scholar 

  12. Grau AJ, Urbanek C, Palm F (2010) Common infections and the risk of stroke. Nat Rev Neurol 6:681–694

    Article  PubMed  Google Scholar 

  13. Ayada K, Yokota K, Kobayashi K, Shoenfeld Y, Matsuura E, Oguma K (2009) Chronic infections and atherosclerosis. Clin Rev Allergy Immunol 37:44–48

    Article  PubMed  Google Scholar 

  14. Pietroiusti A, Diomedi M, Silvestrini M, Cupini LM, Luzzi I, Gomez-Miguel MJ, Bergamaschi A, Magrini A, Carrabs T, Vellini M, Galante A (2002) Cytotoxin-associated gene-A--positive Helicobacter pylori strains are associated with atherosclerotic stroke. Circulation 106:580–584

    Article  PubMed  CAS  Google Scholar 

  15. Ponzetto A, Marchet A, Pellicano R, Lovera N, Chianale G, Nobili M, Rizzetto M, Cerrato P (2002) Association of Helicobacter pylori infection with ischemic stroke of non-cardiac origin: the BAT.MA.N. project study. Hepatogastroenterology 49:631–634

    PubMed  Google Scholar 

  16. Moayyedi P, Carter AM, Braunholtz D, Catto AJ (2003) Helicobacter pylori infection in subjects with acute ischaemic stroke. Dig Liver Dis 35:16–19

    Article  PubMed  CAS  Google Scholar 

  17. Masoud SA, Arami MA, Kucheki E (2005). Association between infection with Helicobacter pylori and cerebral noncardioembolic ischemic stroke. Neurol India 53: 303–306; discussion 306–307

    Article  PubMed  CAS  Google Scholar 

  18. Cremonini F, Gabrielli M, Gasbarrini G, Pola P, Gasbarrini A (2004) The relationship between chronic H. pylori infection, CagA seropositivity and stroke: meta-analysis. Atherosclerosis 173:253–259

    Article  PubMed  CAS  Google Scholar 

  19. Preusch MR, Grau AJ, Buggle F, Lichy C, Bartel J, Black C, Rudi J (2004) Association between cerebral ischemia and cytotoxin-associated gene-A-bearing strains of Helicobacter pylori. Stroke 35:1800–1804

    Article  PubMed  CAS  Google Scholar 

  20. Sawayama Y, Ariyama I, Hamada M, Otaguro S, Machi T, Taira Y, Hayashi J (2005) Association between chronic Helicobacter pylori infection and acute ischemic stroke: Fukuoka Harasanshin Atherosclerosis Trial (FHAT). Atherosclerosis 178:303–309

    Article  PubMed  CAS  Google Scholar 

  21. Park MH, Min JY, Koh SB, Kim BJ, Park MK, Park KW, Lee DH (2006) Helicobacter pylori infection and the CD14 C(-260)T gene polymorphism in ischemic stroke. Thromb Res 118:671–677

    Article  PubMed  CAS  Google Scholar 

  22. De Bastiani R, Gabrielli M, Ubaldi E, Benedetto E, Sanna G, Cottone C, Candelli M, Zocco Maria A, Saulnier N, Santoliquido A, Papaleo P, Gasbarrini G, Gasbarrini A (2008) High prevalence of Cag-A positive H. pylori strains in ischemic stroke: a primary care multicenter study. Helicobacter 13:274–277

    Article  PubMed  Google Scholar 

  23. Yang X, Gao Y, Zhao X, Tang Y, Su Y (2011) Chronic Helicobacter pylori infection and ischemic stroke subtypes. Neurol Res 33:467–472

    Article  PubMed  Google Scholar 

  24. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 339:b2700

    Article  PubMed  Google Scholar 

  25. Mousavi SA, Ataei B, Karimi I, Ashrafi K (2011) Helicobacter pylori serum antibody titers in patients with cerebral non-cardioembolic ischemic stroke. J Res Med Sci 16:S407–S411

    PubMed  Google Scholar 

  26. Liu L, Zeng F, Wang K, Huang J, Xin L, Zhu PQ (2011) Meta-analysis of the association between VEGF-634 G>C and risk of malignancy based on 23 case–control studies. J Cancer Res Clin Oncol 137:1027–1036

    Article  PubMed  CAS  Google Scholar 

  27. Zhuang W, Wu XT, Zhou Y, Liu L, Liu GJ, Wu TX, Yao X, Du L, Wei ML (2010) Interleukin10-592 promoter polymorphism associated with gastric cancer among Asians: a meta-analysis of epidemiologic studies. Dig Dis Sci 55:1525–1532

    Article  PubMed  CAS  Google Scholar 

  28. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188

    Article  PubMed  CAS  Google Scholar 

  29. Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101

    Article  PubMed  CAS  Google Scholar 

  30. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634

    Article  PubMed  CAS  Google Scholar 

  31. Attia J, Thakkinstian A, D’Este C (2003) Meta-analyses of molecular association studies: methodologic lessons for genetic epidemiology. J Clin Epidemiol 56:297–303

    Article  PubMed  Google Scholar 

  32. Aslan M, Nazligul Y, Horoz M, Bolukbas C, Bolukbas FF, Gur M, Celik H, Erel O (2008) Serum paraoxonase-1 activity in Helicobacter pylori infected subjects. Atherosclerosis 196:270–274

    Article  PubMed  CAS  Google Scholar 

  33. Matsuura E, Kobayashi K, Matsunami Y, Shen L, Quan N, Makarova M, Suchkov SV, Ayada K, Oguma K, Lopez LR (2009) Autoimmunity, infectious immunity, and atherosclerosis. J Clin Immunol 29:714–721

    Article  PubMed  CAS  Google Scholar 

  34. Kim HL, Jeon HH, Park IY, Choi JM, Kang JS, Min KW (2011) Helicobacter pylori infection is associated with elevated low density lipoprotein cholesterol levels in elderly Koreans. J Korean Med Sci 26:654–658

    Article  PubMed  CAS  Google Scholar 

  35. Goldstein LB, Hankey GJ (2006) Advances in primary stroke prevention. Stroke 37:317–319

    Article  PubMed  Google Scholar 

  36. Huang B, Chen Y, Xie Q, Lin G, Wu Y, Feng Y, Li J, Zhuo Y, Zhang P (2011) CagA-positive Helicobacter pylori strains enhanced coronary atherosclerosis by increasing serum OxLDL and HsCRP in patients with coronary heart disease. Dig Dis Sci 56:109–114

    Article  PubMed  CAS  Google Scholar 

Download references

Conflicts of interest

All authors claimed no potential conflict of interest.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, The First Affiliated Hospital of Xinxiang Medical University, Health Road No. 88, Weihui, Henan, People’s Republic of China

    Zhong Wei Wang, Yan Li, Li Yong Huang, Qing Kai Guan, Da Wei Xu, Wen Ke Zhou & Xin Zhong Zhang

Authors
  1. Zhong Wei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Li Yong Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qing Kai Guan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Da Wei Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wen Ke Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xin Zhong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Li Yong Huang.

Additional information

Z. W. Wang, Y. Li and L. Y. Huang contributed equally to this paper and should be listed as co-first authors.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, Z.W., Li, Y., Huang, L.Y. et al. Helicobacter pylori infection contributes to high risk of ischemic stroke: evidence from a meta-analysis. J Neurol 259, 2527–2537 (2012). https://doi.org/10.1007/s00415-012-6558-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-012-6558-7

Keywords

Search

Navigation