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Prevalence of Helicobacter pylori Virulence Genes and Their Association with Chronic Gastritis in Beijing, China

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Abstract

Helicobacter pylori is closely related to chronic gastritis. The aim of the study was to investigate the correlation between H. pylori virulence genes and chronic gastritis in order to determine the pathogenic role of H. pylori virulence genes in chronic gastritis. Gastric mucosal tissues were obtained from 142 patients with chronic gastritis at three Beijing hospitals. The presence of virulence genes was determined by polymerase chain reaction (PCR) from H. pylori DNA. Multilocus sequence typing (MLST) and a phylogenetic tree were performed to characterize the overall genetic diversity. 91 new sequence types were identified by MLST in this study, and all strains showed high genetic diversity. The H. pylori isolates were divided into three types: hspEAsia strains (61 strains), hpEurope strains (15 strains), and mixed strains (16 strains). Some virulence genes were found to be significantly different between strains. The highest positive rates were found for dupA in chronic atrophic gastritis (AG), iceA1 in chronic non-atrophic gastritis with erosions, and iceA2 in chronic non-atrophic gastritis. The presence of dupA was found to be inversely related to the risk of AG. The H. pylori strains display high genetic diversity. Some virulence genes were found to be significantly different between diseases. The detection of various virulence genes is critical for screening high-risk populations for precancerous lesions and for the early prevention and control of gastric cancer.

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Data Availability

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Code Availability

Yes.

References

  1. Hooi JKY et al (2017) Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology 153(2):420–429

    Article  Google Scholar 

  2. de Martel C et al (2012) Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol 13(6):607–615

    Article  Google Scholar 

  3. Trang THT, Thanh Binh T, Yamaoka Y (2016) Relationship between vacA types and development of gastroduodenal diseases. Toxins 8(6):182

    Article  Google Scholar 

  4. Suerbaum S, Josenhans C (2007) Helicobacter pylori evolution and phenotypic diversification in a changing host. Nat Rev Microbiol 5(6):441–452

    Article  CAS  Google Scholar 

  5. Breurec S et al (2011) Evolutionary history of Helicobacter pylori sequences reflect past human migrations in Southeast Asia. PLoS ONE 6(7):e22058

    Article  CAS  Google Scholar 

  6. Ogorodnik E, Raffaniello RD (2013) Analysis of the 3′-variable region of the cagA gene from Helicobacter pylori strains infecting patients at New York City hospitals. Microb Pathog 56:29–34

    Article  CAS  Google Scholar 

  7. Kim SS et al (2011) Helicobacter pylori in the pathogenesis of gastric cancer and gastric lymphoma. Cancer Lett 305(2):228–238

    Article  CAS  Google Scholar 

  8. Marie MAM (2012) Relationship between Helicobacter pylori virulence genes and clinical outcomes in Saudi patients. J Korean Med Sci 27(2):190–193

    Article  CAS  Google Scholar 

  9. Siddique I et al (2014) Association between Helicobacter pylori genotypes and severity of chronic gastritis, peptic ulcer disease and gastric mucosal interleukin-8 levels: evidence from a study in the Middle East. Gut pathogens 6(1):1–10

    Article  Google Scholar 

  10. Feliciano O et al (2015) Prevalence of Helicobacter pylori vacA, cagA, and iceA genotypes in Cuban patients with upper gastrointestinal diseases. Biomed Res Int. https://doi.org/10.1155/2015/753710

    Article  Google Scholar 

  11. Shiota S et al (2012) Association of Helicobacter pylori dupA with the failure of primary eradication. J Clin Gastroenterol 46(4):297

    Article  Google Scholar 

  12. Nguyen TL et al (2010) Helicobacter pylori infection and gastroduodenal diseases in Vietnam: a cross-sectional, hospital-based study. BMC Gastroenterol 10:114

    Article  Google Scholar 

  13. Alavifard H et al (2021) Investigation of clarithromycin resistance-associated mutations and virulence genotypes of Helicobacter pylori isolated from Iranian population: a cross-sectional study. Curr Microbiol 78(1):244–254

    Article  CAS  Google Scholar 

  14. Oktem-Okullu S et al (2020) Analysis of correlation between the seven important Helicobacter pylori (H. pylori) virulence factors and drug resistance in patients with gastritis. Gastroenterology Research and Practice. https://doi.org/10.1155/2020/3956838

    Article  Google Scholar 

  15. Shahi H, Kiaee F (2020) Association between expression of interleukin-32 gene and various Helicobacter pylori virulence factors in human infected gastric biopsy. Acta Med Iran. https://doi.org/10.18502/acta.v58i3.3772

    Article  Google Scholar 

  16. Amin M, Shayesteh AA, Serajian A (2019) Concurrent detection of cagA, vacA, sodB and hsp60 virulence genes and their relationship with clinical outcomes of disease in Helicobacter pylori isolated strains of southwest of Iran. Iranian Journal of Microbiology 11(3):198

    Google Scholar 

  17. Xia Y et al (2009) A comprehensive sequence and disease correlation analyses for the C-terminal region of CagA protein of Helicobacter pylori. PLoS ONE 4(11):e7736

    Article  Google Scholar 

  18. Pan KF 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(1):9–18

    Article  CAS  Google Scholar 

  19. Cardenas VM et al (2006) Iron deficiency and Helicobacter pylori infection in the United States. Am J Epidemiol 163(2):127–134

    Article  Google Scholar 

  20. Everhart JE et al (2000) Seroprevalence and ethnic differences in Helicobacter pylori infection among adults in the United States. J Infect Dis 181(4):1359–1363

    Article  CAS  Google Scholar 

  21. Lee JH et al (2018) Seroprevalence of Helicobacter pylori in Korea: a multicenter, nationwide study conducted in 2015 and 2016. Helicobacter 23(2):e12463

    Article  Google Scholar 

  22. Zhang F et al (2021) Prevalence and associated risk factors of Helicobacter pylori infection in the Wuwei cohort of North-Western China. Trop Med Int Health 26(3):290–300

    Article  CAS  Google Scholar 

  23. Lee SP et al (2017) Factors related to upper gastrointestinal symptom generation in 2275 Helicobacter pylori seroprevalent adults. Dig Dis Sci 62(6):1561–1570

    Article  CAS  Google Scholar 

  24. Rojas-Rengifo DF et al (2019) Helicobacter pylori culture as a key tool for diagnosis in Colombia. The Journal of Infection in Developing Countries 13(08):720–726

    Article  CAS  Google Scholar 

  25. Ndip RN et al (2003) Culturing Helicobacter pylori from clinical specimens: review of microbiologic methods. J Pediatr Gastroenterol Nutr 36(5):616–622

    Article  CAS  Google Scholar 

  26. Falush D et al (2001) Recombination and mutation during long-term gastric colonization by Helicobacter pylori: estimates of clock rates, recombination size, and minimal age. Proc Natl Acad Sci 98(26):15056–15061

    Article  CAS  Google Scholar 

  27. Falush D et al (2003) Traces of human migrations in Helicobacter pylori populations. Science 299(5612):1582–1585

    Article  CAS  Google Scholar 

  28. Yamaoka Y, Kato M, Asaka M (2008) Geographic differences in gastric cancer incidence can be explained by differences between Helicobacter pylori strains. Intern Med 47(12):1077–1083

    Article  Google Scholar 

  29. Su H et al (2019) Evolutionary mechanism leading to the multi-cagA genotype in Helicobacter pylori. Sci Rep 9(1):11203

    Article  Google Scholar 

  30. Wei GC et al (2012) Prevalence of Helicobacter pylori vacA, cagA and iceA genotypes and correlation with clinical outcome. Exp Ther Med 4(6):1039–1044

    Article  CAS  Google Scholar 

  31. Xue Z et al (2021) Geographic distribution of the cagA, vacA, iceA, oipA and dupA genes of Helicobacter pylori strains isolated in China. Gut Pathog 13(1):39

    Article  CAS  Google Scholar 

  32. Ladeira MS et al (2008) Relationship among oxidative DNA damage, gastric mucosal density and the relevance of cagA, vacA and iceA genotypes of Helicobacter pylori. Dig Dis Sci 53(1):248–255

    Article  CAS  Google Scholar 

  33. Ma YJ et al (2010) Mutation of iceA in Helicobacter pylori compromised IL-8 induction from human gastric epithelial cells. J Basic Microbiol 50(S1):S83–S88

    Article  Google Scholar 

  34. Chiurillo MA et al (2010) Combination of Helicobacter pylori-iceA2 and proinflammatory interleukin-1 polymorphisms is associated with the severity of histological changes in Venezuelan chronic gastritis patients. FEMS Immunol Med Microbiol 59(2):170–176

    Article  CAS  Google Scholar 

  35. Lu H et al (2005) Duodenal ulcer promoting gene of Helicobacter pylori. Gastroenterology 128(4):833–848

    Article  CAS  Google Scholar 

  36. Shiota S et al (2010) Systematic review and meta-analysis: the relationship between the Helicobacter pylori dupA gene and clinical outcomes. Gut Pathog 2(1):13

    Article  Google Scholar 

  37. Gomes LI et al (2008) Lack of association between Helicobacter pylori infection with dupA-positive strains and gastroduodenal diseases in Brazilian patients. Int J Med Microbiol 298(3–4):223–230

    Article  CAS  Google Scholar 

  38. Pacheco AR et al (2008) Involvement of the Helicobacter pylori plasticity region and cag pathogenicity island genes in the development of gastroduodenal diseases. Eur J Clin Microbiol Infect Dis 27(11):1053–1059

    Article  CAS  Google Scholar 

  39. Jung SW et al (2012) The intact dupA cluster is a more reliable Helicobacter pylori virulence marker than dupA alone. Infect Immun 80(1):381–387

    Article  CAS  Google Scholar 

  40. Harrison U et al (2017) Helicobacter pylori strains from a Nigerian cohort show divergent antibiotic resistance rates and a uniform pathogenicity profile. PLoS ONE 12(5):e0176454

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank the staff at the Department of Gastroenterology, Emergency General Hospital in Beijing, China, and the Department of Gastroenterology, Eighth Medical Center of PLA General Hospital in Beijing, China, for providing clinical specimens.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or nonprofit sectors.

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Author notes

  1. Xiaoyan Zhu, Chaohui Zhu and Yajiao Zhao have contributed equally to this work.

Authors and Affiliations

  1. Clinical Laboratory Center, Beijing Friendship Hospital, Capital Medical University, No. 95 Yong-an Road, Xi-Cheng District, Beijing, China

    Xiaoyan Zhu, Yaxuan Wang & Jianrong Su

  2. Department of Gastroenterology, The Eighth Medical Center of PLA General Hospital, No. 17, Heishanhu Road, Hai-Dian District, Beijing, China

    Chaohui Zhu, Xiaochuan Liu & Kai Wu

  3. Department of Gastroenterology, Emergency General Hospital, Beijing, China

    Yajiao Zhao

  4. Department of Gastroenterology, Jingdong Medical Area, General Hospital of Chinese PLA, Beijing, China

    Rina Sa

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  1. Xiaoyan Zhu
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  4. Xiaochuan Liu
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Contributions

XZ contributed to the conception of the study and the draft of the manuscript; CZ and YZ performed the experiment; XL worked on data analysis and interpretation; RS and YW performed the data analyses; KW and JS critically revised the manuscript. All authors approved the final version of the manuscript.

Corresponding authors

Correspondence to Kai Wu or Jianrong Su.

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Conflict of interest

The authors declare no potential conflict of interest.

Ethical Approval

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Ethical approval was approved by the Ethics Committee of Beijing Friendship Hospital, Capital Medical University, Beijing, China (Ethics approval number: 2021-P2-199-01). All experiments were carried out in accordance with relevant guidelines and regulations, and informed consent was obtained from all patients.

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Informed consent for participation was obtained from all participants included in this study.

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Zhu, X., Zhu, C., Zhao, Y. et al. Prevalence of Helicobacter pylori Virulence Genes and Their Association with Chronic Gastritis in Beijing, China. Curr Microbiol 80, 33 (2023). https://doi.org/10.1007/s00284-022-03135-6

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