Helicobacter pylori antibody and pepsinogen testing for predicting gastric microbiome abundance


Autoři: Saemi Choi aff001;  Jae Gon Lee aff002;  A-reum Lee aff002;  Chang Soo Eun aff002;  Dong Soo Han aff002;  Chan Hyuk Park aff002
Působiště autorů: Department of Medicine, Hanyang University College of Medicine, Seoul, Korea aff001;  Department of Internal Medicine, Hanyang University Guri Hospital, Hanyang University College of Medicine, Guri, Korea aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225961

Souhrn

Background

Although the high-throughput sequencing technique is useful for evaluating gastric microbiome, it is difficult to use clinically. We aimed to develop a predictive model for gastric microbiome based on serologic testing.

Methods

This study was designed to analyze sequencing data obtained from the Hanyang University Gastric Microbiome Cohort, which was established initially to investigate gastric microbial composition according to the intragastric environment. We evaluated the relationship between the relative abundance of potential gastric cancer-associated bacteria (nitrosating/nitrate-reducing bacteria or type IV secretion system [T4SS] protein gene-contributing bacteria) and serologic markers (IgG anti-Helicobacter pylori [HP] antibody or pepsinogen [PG] levels).

Results

We included 57 and 26 participants without and with HP infection, respectively. The relative abundance of nitrosating/nitrate-reducing bacteria was 4.9% and 3.6% in the HP-negative and HP-positive groups, respectively, while that of T4SS protein gene-contributing bacteria was 20.5% and 6.5% in the HP-negative and HP-positive groups, respectively. The relative abundance of both nitrosating/nitrate-reducing bacteria and T4SS protein gene-contributing bacteria increased exponentially as PG levels decreased. Advanced age (only for nitrosating/nitrate-reducing bacteria), a negative result of IgG anti-HP antibody, low PG levels, and high Charlson comorbidity index were associated with a high relative abundance of nitrosating/nitrate-reducing bacteria and T4SS protein gene-contributing bacteria. The adjusted coefficient of determination (R2) was 53.7% and 70.0% in the model for nitrosating/nitrate-reducing bacteria and T4SS protein gene-contributing bacteria, respectively.

Conclusion

Not only the negative results of IgG anti-HP antibody but also low PG levels were associated with a high abundance of nitrosating/nitrate-reducing bacteria and T4SS protein gene-contributing bacteria.

Klíčová slova:

Antibodies – Cyanobacteria – Gastric cancer – Helicobacter pylori – Microbiome – Secretion systems – Serology


Zdroje

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61: 69–90. doi: 10.3322/caac.20107 21296855

2. Karimi P, Islami F, Anandasabapathy S, Freedman ND, Kamangar F. Gastric cancer: descriptive epidemiology, risk factors, screening, and prevention. Cancer Epidemiol Biomarkers Prev. 2014;23: 700–713. doi: 10.1158/1055-9965.EPI-13-1057 24618998

3. Crew KD, Neugut AI. Epidemiology of gastric cancer. World J Gastroenterol. 2006;12: 354–362. doi: 10.3748/wjg.v12.i3.354 16489633

4. Wong BC, Lam SK, Wong WM, Chen JS, Zheng TT, Feng RE, et al. Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. JAMA. 2004;291: 187–194. doi: 10.1001/jama.291.2.187 14722144

5. Chen S, Ying L, Kong M, Zhang Y, Li Y. The Prevalence of Helicobacter pylori Infection Decreases with Older Age in Atrophic Gastritis. Gastroenterol Res Pract. 2013;2013: 494783. doi: 10.1155/2013/494783 24174932

6. Correa P. Helicobacter pylori and gastric carcinogenesis. Am J Surg Pathol. 1995;19 Suppl 1: S37–43.

7. Fox JG, Wang TC. Inflammation, atrophy, and gastric cancer. J Clin Invest. 2007;117: 60–69. doi: 10.1172/JCI30111 17200707

8. Calmels S, Dalla Venezia N, Bartsch H. Isolation of an enzyme catalysing nitrosamine formation in Pseudomonas aeruginosa and Neisseria mucosae. Biochem Biophys Res Commun. 1990;171: 655–660. doi: 10.1016/0006-291x(90)91196-y 2119577

9. Mowat C, Williams C, Gillen D, Hossack M, Gilmour D, Carswell A, et al. Omeprazole, Helicobacter pylori status, and alterations in the intragastric milieu facilitating bacterial N-nitrosation. Gastroenterology. 2000;119: 339–347. doi: 10.1053/gast.2000.9367 10930369

10. Forsythe SJ, Dolby JM, Webster AD, Cole JA. Nitrate- and nitrite-reducing bacteria in the achlorhydric stomach. J Med Microbiol. 1988;25: 253–259. doi: 10.1099/00222615-25-4-253 3357192

11. Williams C, McColl KE. Review article: proton pump inhibitors and bacterial overgrowth. Aliment Pharmacol Ther. 2006;23: 3–10.

12. Park CH, Lee AR, Lee Y, Eun CS, Lee SK, Han DS. Evaluation of gastric microbiome and metagenomic function in patients with intestinal metaplasia using 16S rRNA gene sequencing. Helicobacter. 2019;24: e12547–e12547. doi: 10.1111/hel.12547 30440093

13. Eun CS, Kim BK, Han DS, Kim SY, Kim KM, Choi BY, et al. Differences in gastric mucosal microbiota profiling in patients with chronic gastritis, intestinal metaplasia, and gastric cancer using pyrosequencing methods. Helicobacter. 2014;19: 407–416. doi: 10.1111/hel.12145 25052961

14. Jo HJ, Kim J, Kim N, Park JH, Nam RH, Seok YJ, et al. Analysis of Gastric Microbiota by Pyrosequencing: Minor Role of Bacteria Other Than Helicobacter pylori in the Gastric Carcinogenesis. Helicobacter. 2016;21: 364–374. doi: 10.1111/hel.12293 26915731

15. Miki K. Gastric cancer screening by combined assay for serum anti-Helicobacter pylori IgG antibody and serum pepsinogen levels—"ABC method". Proc Jpn Acad Ser B Phys Biol Sci. 2011;87: 405–414. doi: 10.2183/pjab.87.405 21785258

16. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7: 335–336. doi: 10.1038/nmeth.f.303 20383131

17. Kembel SW, Wu M, Eisen JA, Green JL. Incorporating 16S gene copy number information improves estimates of microbial diversity and abundance. PLoS Comput Biol. 2012;8: e1002743. doi: 10.1371/journal.pcbi.1002743 23133348

18. Ascencio F, Gama NL, De Philippis R, Ho B. Effectiveness of Cyanothece spp. and Cyanospira capsulata exocellular polysaccharides as antiadhesive agents for blocking attachment of Helicobacter pylori to human gastric cells. Folia Microbiol (Praha). 2004;49: 64–70.

19. Loke MF, Lui SY, Ng BL, Gong M, Ho B. Antiadhesive property of microalgal polysaccharide extract on the binding of Helicobacter pylori to gastric mucin. FEMS Immunol Med Microbiol. 2007;50: 231–238. doi: 10.1111/j.1574-695X.2007.00248.x 17521357

20. Williams DA. Generalized Linear Model Diagnostics Using the Deviance and Single Case Deletions. Journal of the Royal Statistical Society. Series C (Applied Statistics). 1987;36: 181–191.

21. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecology. 2001;26: 32–46.

22. Miftahussurur M, Yamaoka Y, Graham DY. Helicobacter pylori as an oncogenic pathogen, revisited. Expert Rev Mol Med. 2017;19: e4. doi: 10.1017/erm.2017.4 28322182

23. Sanduleanu S, Jonkers D, De Bruine A, Hameeteman W, Stockbrugger RW. Double gastric infection with Helicobacter pylori and non-Helicobacter pylori bacteria during acid-suppressive therapy: increase of pro-inflammatory cytokines and development of atrophic gastritis. Aliment Pharmacol Ther. 2001;15: 1163–1175. doi: 10.1046/j.1365-2036.2001.01029.x 11472319

24. Backert S, Selbach M. Role of type IV secretion in Helicobacter pylori pathogenesis. Cell Microbiol. 2008;10: 1573–1581. doi: 10.1111/j.1462-5822.2008.01156.x 18410539

25. Kudo T, Kakizaki S, Sohara N, Onozato Y, Okamura S, Inui Y, et al. Analysis of ABC (D) stratification for screening patients with gastric cancer. World J Gastroenterol. 2011;17: 4793–4798. doi: 10.3748/wjg.v17.i43.4793 22147980


Článek vyšel v časopise

PLOS One


2019 Číslo 12