Skip to main content

Advertisement

SpringerLink
Log in

Population attributable burden of Helicobacter pylori-related gastric cancer, coronary heart disease, and ischemic stroke in China

  • Review
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

Helicobacter pylori, a risk factor of cancer and chronic diseases, remains highly prevalent in China. This review aims to systematically evaluate the H. pylori-attributable burden for gastric cancer (GC), coronary heart disease (CHD), and ischemic stroke (IS) in the Chinese population. Helicobacter pylori prevalence was updated by pooling the results reported in studies across China. The population attributable fraction (PAF) was calculated based on the H. pylori prevalence 10 years ago and relative risks of specific disease by reviewing the prospective studies published from 2000 through 2015. In China, the nationwide average prevalence of H. pylori was estimated to be 42.06 % in the general population during 2009–2013. The fixed effects pooled relative risk (RR) of 1.89 [95 % confidence interval (CI): 1.57–2.26] was obtained for gastric cancer and H. pylori infection. Helicobacter pylori infection was responsible for around 37.38 % of noncardia GC, corresponding to about 105,536 cases in 2012. As for extra-gastric disorders, H. pylori infections had higher risk of CHD (RR = 1.55, 95 % CI: 1.37–1.76) and IS (RR = 1.54, 95 % CI: 1.42–1.66). About 23.15 % of CHD and 22.29 % of IS were attributable to H. pylori infection. The estimates of H. pylori-attributable burden reveal a great potential of reducing H. pylori-related chronic disease burden by H. pylori eradication. Large prospective studies are warranted to identify which H. pylori strains, which subtypes of the disease, and which subgroups of the population have the greatest risk of relevant diseases and the effect of H. pylori eradication on the prevention of H. pylori-related diseases.

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

Similar content being viewed by others

References

  1. de Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, Forman D et al (2012) Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol 13:607–615

    Article  PubMed  Google Scholar 

  2. Xiang W, Shi JF, Li P, Wang JB, Xu LN, Wei WQ et al (2011) Estimation of cancer cases and deaths attributable to infection in China. Cancer Causes Control 22:1153–1161

    Article  PubMed  Google Scholar 

  3. Censini S, Lange C, Xiang Z, Crabtree JE, Ghiara P, Borodovsky M et al (1996) cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci U S A 93:14648–14653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Møller H, Heseltine E, Vainio H (1995) Working group report on schistosomes, liver flukes and Helicobacter pylori. Int J Cancer 60:587–589

    Article  PubMed  Google Scholar 

  5. Zullo A, Hassan C, Ridola L, Repici A, Manta R, Andriani A (2014) Gastric MALT lymphoma: old and new insights. Ann Gastroenterol 27:27–33

    PubMed  PubMed Central  Google Scholar 

  6. Sun J, Rangan P, Bhat SS, Liu L (2016) A meta-analysis of the association between Helicobacter pylori infection and risk of coronary heart disease from published prospective studies. Helicobacter 21:11–23

    Article  PubMed  Google Scholar 

  7. 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  CAS  PubMed  Google Scholar 

  8. Vijayvergiya R, Vadivelu R (2015) Role of Helicobacter pylori infection in pathogenesis of atherosclerosis. World J Cardiol 7:134–143

    Article  PubMed  PubMed Central  Google Scholar 

  9. Chmiela M, Gajewski A, Rudnicka K (2015) Helicobacter pylori vs coronary heart disease—searching for connections. World J Cardiol 7:187–203

    PubMed  PubMed Central  Google Scholar 

  10. Huang WS, Tseng CH, Lin CL, Tsai CH, Kao CH (2014) Helicobacter pylori infection increases subsequent ischemic stroke risk: a nationwide population-based retrospective cohort study. QJM 107:969–975

    Article  PubMed  Google Scholar 

  11. Lai CY, Yang TY, Lin CL, Kao CH (2015) Helicobacter pylori infection and the risk of acute coronary syndrome: a nationwide retrospective cohort study. Eur J Clin Microbiol Infect Dis 34:69–74

    Article  PubMed  Google Scholar 

  12. Monzón H, Forné M, Esteve M, Rosinach M, Loras C, Espinós JC et al (2013) Helicobacter pylori infection as a cause of iron deficiency anaemia of unknown origin. World J Gastroenterol 19:4166–4171

    Article  PubMed  PubMed Central  Google Scholar 

  13. Marietti M, Gasbarrini A, Saracco G, Pellicano R (2013) Helicobacter pylori infection and diabetes mellitus: the 2013 state of art. Panminerva Med. 55:277–281

    CAS  PubMed  Google Scholar 

  14. Khamechian T, Movahedian AH, Ebrahimi Eskandari G, Heidarzadeh Arani M, Mohammadi A (2015) Evaluation of the correlation between childhood asthma and Helicobacter pylori in Kashan. Jundishapur J Microbiol 8, e17842

    Article  PubMed  PubMed Central  Google Scholar 

  15. Chang SS, Hu HY (2014) No inverse relationship between Helicobacter pylori infection and adult asthma with peptic ulcer disease. Hepatogastroenterology 61:529–534

    PubMed  Google Scholar 

  16. Vasapolli R, Malfertheiner P, Kandulski A (2016) Helicobacter pylori and non-malignant upper gastrointestinal diseases. Helicobacter 21(Suppl 1):30–33

    Article  CAS  PubMed  Google Scholar 

  17. Chen W, Zheng R, Zuo T, Zeng H, Zhang S, He J (2016) National cancer incidence and mortality in China, 2012. Chin J Cancer Res 28:1–11

    Article  PubMed  PubMed Central  Google Scholar 

  18. Zhang WD, Hu FL, Xiao SD, Xu ZM (2010) Prevalence of Helicobacter pylori infection in China. Mod Digest Interv 15:265–270

    Google Scholar 

  19. Levin ML (1953) The occurrence of lung cancer in man. Acta Unio Int Contra Cancrum 9:531–541

    CAS  PubMed  Google Scholar 

  20. Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M et al (2010) The Newcastle–Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. The Ottawa Hospital Research Institute

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

    Article  CAS  PubMed  Google Scholar 

  22. Kamangar F, Qiao YL, Blaser MJ, Sun XD, Katki H, Fan JH et al (2007) Helicobacter pylori and oesophageal and gastric cancers in a prospective study in China. Br J Cancer 96:172–176

    Article  CAS  PubMed  Google Scholar 

  23. Epplein M, Zheng W, Xiang YB, Peek RM Jr, Li H, Correa P et al (2012) Prospective study of Helicobacter pylori biomarkers for gastric cancer risk among Chinese men. Cancer Epidemiol Biomarkers Prev 21:2185–2192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ma JL, Zhang L, Pan KF, Liu WD, Feng GS, You WC (2005) Helicobacter pylori and the progression of gastric cancer: a 10-year cohort study. Natl Med J China 85:2758–2761

    Google Scholar 

  25. Zhang X, Xue L, Xing L, Wang J, Cui J, Mi J et al (2012) Low serum pepsinogen I and pepsinogen I/II ratio and Helicobacter pylori infection are associated with increased risk of gastric cancer: 14-year follow up result in a rural Chinese community. Int J Cancer 130:1614–1619

    Article  CAS  PubMed  Google Scholar 

  26. Wang RT, Wang T, Chen K, Wang JY, Zhang JP, Lin SR et al (2002) Helicobacter pylori infection and gastric cancer: evidence from a retrospective cohort study and nested case–control study in China. World J Gastroenterol 8:1103–1107

    Article  PubMed  PubMed Central  Google Scholar 

  27. Hsu WY, Lin CH, Lin CC, Sung FC, Hsu CP, Kao CH (2014) The relationship between Helicobacter pylori and cancer risk. Eur J Intern Med 25:235–240

    Article  CAS  PubMed  Google Scholar 

  28. Liu XH (2005) Relation between Helicobacter pylori infection and risk factors of coronary heart disease. J Pract Diagn Ther 19:881–883

    Google Scholar 

  29. Lu SY, Guo QH, Liu JS, Xie SZ, Li L, Sun YC et al (2003) The relative study of coronary heart disease and Helicobacter pylori. Med J Chin People Health 15:67–68

    Google Scholar 

  30. Qiao ZF, Hong Y, Zhou L (2010) Investigation on the association between Helicobacter pylori infection and coronary heart disease. Hainan Med J 21:38–40

    Google Scholar 

  31. Wang C, Liu YB, Han ML (2014) Research on correlation between Helicobacter pylori infection and coronary heart disease. Chin J Nosocomiol 24:3526–3527

    CAS  Google Scholar 

  32. Wang YP, Yan SQ, Tian HN, Jing H (2008) Correlation between Helicobacter pylori infection and coronary heart disease. Chin J Diffic Compl Cases 7:74–76

    Google Scholar 

  33. Lai YQ, Yang XL, Li M, Hu H, Yang G (2005) Study on relationship between Helicobacter pylori IgG antibody components and coronary heart disease. Chin J Pract Intern Med 25:241–242

    Google Scholar 

  34. Wang Y, Shen J, Yan S, Tian H, Jing H (2008) Correlation between Helicobacter pylori infection and coronary heart disease. Chin J Diffic Compl Cases 7:74–76

    Google Scholar 

  35. Cao PL, Liu XQ, Tang QZ, Liu Y, Wang XQ (2011) Correlation between different Helicobacter pylori genotypes and coronary heart disease. China Med Her 24–26

  36. Chuai Y, Song H, Xue M, Ning X, He Z, Li Y et al (2012) Relationship between Helicobacter pylori infection and coronary artery disease. Chin Heart J 24:57–59

    Google Scholar 

  37. Dian Q, Guo T, Liu Z, Liu R, Li C (2014) Correlation between coronary stenosis and lipid metabolism and Helicobacter pylori infection. Chin J Nosocomiol 24:6144–6146

    Google Scholar 

  38. Zhang J, Xun Y, Gai J, Li Y (2008) The relationship between Helicobacter pylori infection and risk factors associated with coronary heart disease. Chin J Prim Med Pharm 15:1686

    Google Scholar 

  39. Wang WY, Yang PH, Cao YY, Liu F, Ma B (2013) Relation between Helicobacter pylori infection and coronary heart disease. Chin Heart J 21:609–610

    Google Scholar 

  40. Guan XR, Jiang LX, Ma XH, Wang LF, Quan H, Li HY (2010) Respiratory syncytial virus infection and risk of acute myocardial infarction. Am J Med Sci 340:356–359

    Article  PubMed  Google Scholar 

  41. Liu MY (2011) Relationship between Helicobacter pylori infection and coronary heart disease. Chin J Nosocomiol 21:1599–1601

    CAS  Google Scholar 

  42. Deng X, Chen X, Li B (2005) Matching case–control study of the relation between Helicobacter pylori and coronary heart disease. J Nanhua Univ(Med Ed) 33:499–500

    CAS  Google Scholar 

  43. Qu W (2012) Research on the correlation of Helicobacter pylori infection in patients with coronary heart disease. China Med Herald 9:49–50

    CAS  Google Scholar 

  44. Tian F, Hu D, Sun X, Ge J, Ma J, Wang J et al (2004) The relation between coronary heart disease and chronic infection of microorganism. Tianjin Med J 32:554–556

    CAS  Google Scholar 

  45. Zeng Z, Huang MH, Liang YJ, Zhang Q, Jiang T, Liu YG (2000) Preliminary exploration of the association between Helicobacter pylori infection and coronary heart disease. China J Mod Med 10:27–28

    Google Scholar 

  46. Liu DN, He ZY, Li JS (2003) Relation between Helicobacter pylori infection and acute myocardial infarction. Chin J Arterioscler 11:541–544

    CAS  Google Scholar 

  47. Lu YL, Pan WQ (2015) Association between Hp infection and first cardio-cerebrovascular events in elderly hypertensive patients. Chin J Geriatr Heart Brain Vessel Dis 17:130–132

    CAS  Google Scholar 

  48. Hao R, Tian J (2013) Studies on correlation between acute cerebral infarction and Helicobacter pylori. Pharma Care Res 13:404, 432, 466

    Article  Google Scholar 

  49. Yu Z (2011) Correlation between cerebral infarction and Helicobacter pylori infection. Guide China Med 09:285–287

    Google Scholar 

  50. Shu AM, Zhou YA (2006) The study on relationship between acute cerebral infarction and chronic Helicobacter pylori (Hp) infection with 13C-UREA-Breath test. J Hebei North Univ (Med Ed) 23:3–6

    Google Scholar 

  51. Zhang A, Wang Y, Zhu K (2009) Relationship between the infection of Helicobacter pylori and ischemic stroke. J Neurol Neurorehabil 6:187–190

    Google Scholar 

  52. Wang YS, Jiao J, Wang G (2003) Analysis of Helicobacter pylori infection in patients with acute myocardial infarction patients. Chin J Gerontol 23:716–717

    Google Scholar 

  53. Wei ZH, He D, Zeng ZJ (2014) Situation of Helicobacter pylori infection in patients with cerebral infarction and its effect on high-sensitivity C-reactive protein and blood lipid metabolism. Guangxi Med J 36:335–337

    CAS  Google Scholar 

  54. Wu HQ, Zhang X, Tang Y (2012) Association of Helicobacter pylori infection and serum homocysteine level in patients with cerebral infarction. J Zhejiang Univ (Med Sci) 41:89–92

    CAS  Google Scholar 

  55. Wu XX, Huang ZY, Huang DH (2003) Study on the relationship between Helicobacter pylori infection and cerebral infarction. Chin J Prim Med Pharm 10:599–600

    Google Scholar 

  56. Zhang X (2007) Study on the relationship between Helicobacter pylori infection and cerebral infarction. Med Inf 20:872–873

    Google Scholar 

  57. Zhang Q, Zhang RB, Meng X (2008) Relationship between Helicobacter pylori infection and transient ischemic attack as well as cerebral infarction. Shandong Med J 48:29–30

    Google Scholar 

  58. Zhao M (2012) Correlation between Helicobacter pylori infection and cerebral infarction. Chin J Nosocomiol 22:3273–3274

    CAS  Google Scholar 

  59. Dou YC, Li X, Leng X (2008) Prevalence of H. pylori infection in cerebral infarction patients and the association between H. pylori infection and cerebral infarction. Chin J Lab Diagn 12:352–354

    Google Scholar 

  60. Duan HL, Shi LX, Chen YC, Wang YL (2005) A study on relationship between Helicobacter pylori infection and cerebral hemorrhage and cerebral infarction. J North China Coal Med Coll 7:557–558

    Google Scholar 

  61. Su Z, Pang Y (2007) Relation of Helicobacter pylori infection and coronary heart disease. J Pract Med 23:3019–3021

    CAS  Google Scholar 

  62. Zhou GA, Zhang FY, Wang AM (2013) The influence of Helicobacter pylori infection to cerebral infarction of different subtype. J Commun Med 11:33–34

    Google Scholar 

  63. Li XH, Yin L, Liu P (2007) The relationship between cytotoxin-associated gene-A positive Helicobacter pylori strains infection and cerebral infarction. Int J Cerebrovasc Dis 15:455–459

    Google Scholar 

  64. Xu F, Zhu B (2013) Study on correlation between Helicobacter pylori infectis and high sensitive C reactive protein in patients with ischemic stroke. Chin J Nosocomiol 23:3645–3646

    CAS  Google Scholar 

  65. 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 

  66. Wang KJ, Wang RT (2003) Meta-analysis on the epidemiology of Helicobacter pylori infection in China. Chin J Epidemiol 19–22

  67. Helicobacter and Cancer Collaborative Group (2001) Gastric cancer and Helicobacter pylori: a combined analysis of 12 case control studies nested within prospective cohorts. Gut 49:347–353

    Article  Google Scholar 

  68. Doorakkers E, Lagergren J, Engstrand L, Brusselaers N (2016) Eradication of Helicobacter pylori and gastric cancer: a systematic review and meta-analysis of cohort studies. J Natl Cancer Inst 108. pii: djw132

  69. Liu J, Wang F, Shi S (2015) Helicobacter pylori infection increase the risk of myocardial infarction: a meta-analysis of 26 studies involving more than 20,000 participants. Helicobacter 20:176–183

    Article  PubMed  Google Scholar 

  70. Wang ZW, Li Y, Huang LY, Guan QK, Xu DW, Zhou WK et al (2012) Helicobacter pylori infection contributes to high risk of ischemic stroke: evidence from a meta-analysis. J Neurol 259:2527–2537

    Article  PubMed  Google Scholar 

  71. Zhang S, Guo Y, Ma Y, Teng Y (2008) Relationship between the cytotoxin-associated gene-A status of H pylori strains and cerebral infarction in European Caucasians and Chinese Han: a meta-analysis. World J Gastroenterol 14:1286–1292

    Article  PubMed  PubMed Central  Google Scholar 

  72. Chen J, Bu XL, Wang QY, Hu PJ, Chen MH (2007) Decreasing seroprevalence of Helicobacter pylori infection during 1993–2003 in Guangzhou, southern China. Helicobacter 12:164–169

    Article  PubMed  Google Scholar 

  73. Zhang DH, Zhou LY, Lin SR, Ding SG, Huang YH, Gu F et al (2009) Recent changes in the prevalence of Helicobacter pylori infection among children and adults in high- or low-incidence regions of gastric cancer in China. Chin Med J (Engl) 122:1759–1763

    Google Scholar 

  74. Pan KF, Zhang L, Gerhard M, Ma JL, Liu WD, Ulm K et al (2016) A large randomised controlled intervention trial to prevent gastric cancer by eradication of Helicobacter pylori in Linqu County, China: baseline results and factors affecting the eradication. Gut 65:9–18

    Article  CAS  PubMed  Google Scholar 

  75. Liu WZ, Xie Y, Cheng H, Lu NH, Hu FL, Zhang WD et al (2013) Fourth Chinese National Consensus Report on the management of Helicobacter pylori infection. J Dig Dis 14:211–221

    Article  CAS  PubMed  Google Scholar 

  76. Everhart JE (2000) Recent developments in the epidemiology of Helicobacter pylori. Gastroenterol Clin North Am 29:559–578

    Article  CAS  PubMed  Google Scholar 

  77. Shi RH, Xu SF, Zhang HJ, Ding YB, Sun GQ, Huang XY et al (2008) Prevalence and risk factors for Helicobacter pylori infection in Chinese populations. Helicobacter 13:157–165

    Article  PubMed  Google Scholar 

  78. Xue FB, Xu YY, Wan Y, Pan BR, Ren J, Fan DM (2001) Association of H. pylori infection with gastric carcinoma: a meta analysis. World J Gastroenterol 7:801–804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Huang JQ, Zheng GF, Sumanac K, Irvine EJ, Hunt RH (2003) Meta-analysis of the relationship between cagA seropositivity and gastric cancer. Gastroenterology 125:1636–1644

    Article  PubMed  Google Scholar 

  80. Karnes WE Jr, Samloff IM, Siurala M, Kekki M, Sipponen P, Kim SW et al (1991) Positive serum antibody and negative tissue staining for Helicobacter pylori in subjects with atrophic body gastritis. Gastroenterology 101:167–174

    Article  PubMed  Google Scholar 

  81. Colquhoun A, Arnold M, Ferlay J, Goodman KJ, Forman D, Soerjomataram I (2015) Global patterns of cardia and non-cardia gastric cancer incidence in 2012. Gut 64:1881–1888

    Article  CAS  PubMed  Google Scholar 

  82. Chen WQ, Zheng RZ, Zeng HM, Zhang SW, He J (2015) Annual report on status of cancer in China, 2011. Chin J Cancer Res 27:2–12

    Article  PubMed  PubMed Central  Google Scholar 

  83. Ford AC, Forman D, Hunt RH, Yuan Y, Moayyedi P (2014) Helicobacter pylori eradication therapy to prevent gastric cancer in healthy asymptomatic infected individuals: systematic review and meta-analysis of randomised controlled trials. BMJ 348:g3174

    Article  PubMed  PubMed Central  Google Scholar 

  84. Lee YC, Chiang TH, Chou CK, Tu YK, Liao WC, Wu MS et al (2016) Association between Helicobacter pylori eradication and gastric cancer incidence: a systematic review and meta-analysis. Gastroenterology 150:1113–1124.e5

    Article  PubMed  Google Scholar 

  85. Yeh JM, Kuntz KM, Ezzati M, Goldie SJ (2009) Exploring the cost-effectiveness of Helicobacter pylori screening to prevent gastric cancer in China in anticipation of clinical trial results. Int J Cancer 124:157–166

  86. Rothenbacher D, Brenner H (2003) Burden of Helicobacter pylori and H. pylori-related diseases in developed countries: recent developments and future implications. Microbes Infect 5:693–703

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Epidemiology and Health Statistics, College of Public Health, Zhengzhou University, No. 100 Science Avenue, Zhengzhou, 450001, China

    J. Jiang, Y. Chen, C. Song & K. Wang

  2. Henan Key Laboratory of Tumor Epidemiology, Zhengzhou, China

    J. Jiang, Y. Chen, C. Song, J. Zhang & K. Wang

  3. College of Basic Medicine, Zhengzhou University, Zhengzhou, China

    J. Shi

Authors
  1. J. Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Y. Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. K. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. Wang.

Ethics declarations

Funding

None.

Conflict of interest

The authors have no competing interests.

Ethical approval

Not required.

Informed consent

All authors approved the final version of the manuscript.

Electronic supplementary material

Below are the links to the electronic supplementary material.

Supplementary Table 1

The detailed information from the studies on the prevalence of H. pylori across China (DOC 169 kb)

Supplementary Table 2

References cited in Table 2 (DOC 978 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, J., Chen, Y., Shi, J. et al. Population attributable burden of Helicobacter pylori-related gastric cancer, coronary heart disease, and ischemic stroke in China. Eur J Clin Microbiol Infect Dis 36, 199–212 (2017). https://doi.org/10.1007/s10096-016-2810-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-016-2810-x

Keywords

Search

Navigation