Euroasian Journal of Hepato-Gastroenterology

Register      Login

VOLUME 10 , ISSUE 1 ( January-June, 2020 ) > List of Articles

REVIEW ARTICLE

Helicobacter pylori Infection and Gastric Microbiota

Gokben Ozbey, Emma Sproston, Alfizah Hanafiah

Keywords : Gastric microbiota, Helicobacter pylori, Stomach

Citation Information : Ozbey G, Sproston E, Hanafiah A. Helicobacter pylori Infection and Gastric Microbiota. Euroasian J Hepatogastroenterol 2020; 10 (1):36-41.

DOI: 10.5005/jp-journals-10018-1310

License: CC BY-NC 4.0

Published Online: 01-06-2020

Copyright Statement:  Copyright © 2020; Jaypee Brothers Medical Publishers (P) Ltd.


Abstract

Owing to its strong acid production, the stomach was known to be a bacteria-free organ for many years. On the other hand, the presence of Helicobacter pylori (H. pylori) and other acid-resistant microbiota that are to persist in the stomach challenged this. It is now recognized that the existence of H. pylori and non-H. pylori species have been linked to the improvement of gastric disease; despite this, there is little published data on the interaction of gastric bacterial flora and the resultant effect on gastric health. The stomach has a unique microbiota including five major phyla, such as Firmicutes, Proteobacteria, Actinobacteria, Fusobacteria and Bacteroidetes. These phyla are identified in both H. pylori-infected and uninfected persons. The resident gastric microflora may mediate the role of H. pylori in the gastric diseases. This article aims to review previous studies that examine the impact of H. pylori infection and the effect of resident gastric microbiota on gut health and disease conditions.


PDF Share
  1. Engstrand L, Lindberg M. Helicobacter pylori and the gastric microbiota. Best Pract Res Clin Gastroenterol 2013;27(1):39–45. DOI: 10.1016/j.bpg.2013.03.016.
  2. Wang B, Yao M, Lv L, et al. The human microbiota in health and disease. Engineering 2017;3(1):71–82. DOI: 10.1016/J.ENG.2017.01.008.
  3. Walsh CJ, Guinane CM, O’Toole PW, et al. Beneficial modulation of the gut microbiota. FEBS Lett 2014;588(22):4120–4130. DOI: 10.1016/j.febslet.2014.03.035.
  4. Yang I, Woltemate S, Piazuelo MB, et al. Different gastric microbiota compositions in two human populations with high and low gastric cancer risk in Colombia. Sci Rep 2016;6(18594):18594. DOI: 10.1038/srep18594.
  5. Delgado S, Cabrera-Rubio R, Mira A, et al. Microbiological survey of the human gastric ecosystem using culturing and pyrosequencing methods. Microb Ecol 2013;65(3):763–772. DOI: 10.1007/s00248-013-0192-5.
  6. Hooi JKY, Lai WY, Ng WK, et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology 2017;153(2):420–429. DOI: 10.1053/j.gastro.2017.04.022.
  7. Blaser MJ. Who are we? indigenous microbes and the ecology of human diseases. EMBO Rep 2006;7(10):956–960. DOI: 10.1038/sj.embor.7400812.
  8. Herrera V, Parsonnet J. Helicobacter pylori and gastric adenocarcinoma. Clin Microbiol Infect 2009;15(11):971–976. DOI: 10.1111/j.1469-0691.2009.03031.x.
  9. Titov SE, Panasyuk GV, Ivanov MK, et al. Detection of Helicobacter pylori in bioptates of gastric mucosa of patients with gastritis and gastric ulcers using real-time PCR. Mol Genet Microbiol Virol 2011;26(3):126–131. DOI: 10.3103/S0891416811030074.
  10. Ozbey G, Kilinc U, Ceribasi S, et al. Detection of Helicobacter pylori from gastric biopsy samples by culture, polymerase chain reaction and histopathological methods in eastern turkey. IJMCM 2012;2:112–118.
  11. Ozbey G, Dogan Y, Demiroren K, et al. Prevalence of Helicobacter pylori in children in eastern turkey and molecular typing of isolates. Braz J Microbiol 2015;46(2):505–511. DOI: 10.1590/S1517-838246220140234.
  12. Liu J, Xue Y, Zhou L. Detection of gastritis-associated pathogens by culturing of gastric juice and mucosa. Int J Clin Exp Pathol 2018;11(4):2214–2220.
  13. Gantuya B, El-Serag HB, Matsumoto T, et al. Gastric microbiota in Helicobacter pylori-negative and -positive gastritis among high incidence of gastric cancer area. Cancers 2019;11(4):504. DOI: 10.3390/cancers11040504.
  14. Hu Y, He LH, Xiao D, et al. Bacterial flora concurrent with Helicobacter pylori in the stomach of patients with upper gastrointestinal diseases. World J Gastroenterol 2012;18(11):1257–1261. DOI: 10.3748/wjg.v18.i11.1257.
  15. Lagier JC, Million M, Hugon P, et al. Human gut microbiota: repertoire and variations. Front Cell Infect Microbiol 2012;2:136. DOI: 10.3389/fcimb.2012.00136.
  16. Adamsson I, Nord CE, Lundquist P, et al. Comparative effects of omeprazole, amoxycillin plus metronidazole versus omeprazole, clarithromycin plus metronidazole on the oral, gastric and intestinal microflora in Helicobacter pylori infected patients. J Antimicrob Chemother 1999;44(5):629–640. DOI: 10.1093/jac/44.5.629.
  17. Savage DC. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 1977;31(1):107–133. DOI: 10.1146/annurev.mi.31.100177.000543.
  18. Bik EM, Eckburg PB, Gill SR, et al. Molecular analysis of the bacterial microbiota in the human stomach. ProcNatl Acad Sci USA 2006;103(3):732–737. DOI: 10.1073/pnas.0506655103.
  19. Andersson AF, Lindberg M, Jakobsson H, et al. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE 2008;3(7):e2836. DOI: 10.1371/journal.pone.0002836.
  20. Dicksved J, Lindberg M, Rosenquist M, et al. Molecular characterization of the stomach microbiota in patients with gastric cancer and in controls. J Med Microbiol 2009;58(Pt 4):509–516. DOI: 10.1099/jmm.0.007302-0.
  21. Li X-X, Wong GL-H, To K-F, et al. Bacterial microbiota profiling in gastritis without Helicobacter pylori infection or non-steroidal anti-inflammatory drug use. PLoS ONE 2009;4(11):e7985. DOI: 10.1371/journal.pone.0007985.
  22. Maldonado-Contreras A, Goldfarb KC, Godoy-Vitorino F, et al. Structure of the human gastric bacterial community in relation to Helicobacter pylori status. ISME J 2011;5(4):574–579. DOI: 10.1038/ismej.2010.149.
  23. Eun CS, Kim BK, Han DS, et al. Differences in gastric mucosal microbiota profiling in patients with chronic gastritis, intestinal metaplasia, and gastric cancer using pyrosequencing methods. Helicobacter 2014;19(6):407–416. DOI: 10.1111/hel.12145.
  24. Llorca L, Pérez-Pérez G, Urruzuno P, et al. Characterization of the gastric microbiota in a pediatric population according to Helicobacter pylori status. Pediatr Infect Dis J 2017;36(2):173–178. DOI: 10.1097/INF.0000000000001383.
  25. Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet 2012;13(4):260–270. DOI: 10.1038/nrg3182.
  26. Abreu MT, Peek JrRM. Gastrointestinal malignancy and the microbiome. Gastroenterol 2014;146(6):1534–1546. DOI: 10.1053/j.gastro.2014.01.001.
  27. Li TH, Sham PK, Lau KS, et al. Alterations in gastric microbiota after H. pylori eradication and in different histological stages of gastric carcinogenesis. Sci Rep 2017;7(1):44935. DOI: 10.1038/srep44935.
  28. Wroblewski LE, Peek RM,Jr, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 2010;23(4):713–739. DOI: 10.1128/CMR.00011-10.
  29. Alarcón T, Llorca L, Perez-Perez G. Impact of the microbiota and gastric disease development by Helicobacter pylori, in Molecular pathogenesis and signal transduction by Helicobacter pylori Tegtmeyer N, Backert S Cham: Springer; 2017. pp. 253–275.
  30. Ottman N, Smidt H, de Vos WM, et al. The function of our microbiota: who is out there and what do they do? Front Cell Infect Microbiol 2012;2:608–616. DOI: 10.3389/fcimb.2012.00104.
  31. He C, Yang Z, Lu N. Imbalance of gastrointestinal microbiota in the pathogenesis of Helicobacter pylori-associated diseases. Helicobacter 2016;21(5):337–348. DOI: 10.1111/hel.12297.
  32. Zilberstein B, Quintanilha AG, Santos MAA, et al. Digestive tract microbiota in healthy volunteers. Clinics (Sao Paulo) 2007;62(1):47–54. DOI: 10.1590/s1807-59322007000100008.
  33. Khosravi Y, Seow SW, Amoyo AA, et al. Helicobacter pylori infection can affect energy modulating hormones and body weight in germ free mice. Sci Rep 2015;5(1):8731. DOI: 10.1038/srep08731.
  34. Correa P, Piazuelo M. Gastric cancer: the colombian enigma. Rev Colomb Gastroenterol 2010;25:334–337.
  35. Tan MP, Kaparakis M, Galic M, et al. Chronic Helicobacter pylori infection does not significantly alter the microbiota of the murine stomach. Appl Environ Microbiol 2007;73(3):1010–1013. DOI: 10.1128/AEM.01675-06.
  36. Lofgren JL, Whary MT, Ge Z, et al. Lack of commensal flora in Helicobacter pylori–infected INS-GAS mice reduces gastritis and delays intraepithelial neoplasia. Gastroenterology 2011;140:(1):210–220. DOI: 10.1053/j.gastro.2010.09.048.
  37. Rolig AS, Cech C, Ahler E, et al. The degree of Helicobacter pylori-triggered inflammation is manipulated by preinfection host microbiota. Infect Immun 2013;81(5):1382–1389. DOI: 10.1128/IAI.00044-13.
  38. Sun YQ, Monstein HJ, Nilsson LE, et al. Profiling and identification of eubacteria in the stomach of mongolian gerbils with and without Helicobacter pylori infection. Helicobacter 2003;8(2):149–157. DOI: 10.1046/j.1523-5378.2003.00136.x.
  39. Osaki T, Matsuki T, Asahara T, et al. Comparative analysis of gastric bacterial microbiota in mongolian gerbils after long-term infection with Helicobacter pylori. Microb Pathog 2012;53(1):12–18. DOI: 10.1016/j.micpath.2012.03.008.
  40. Garcia-Mazcorro JF, Suchodolski JS, Jones KR. Effect of the proton pump inhibitor omeprazole on the gastrointestinal bacterial microbiota of healthy dogs. FEMS Microbiol Ecol 2012;80(3):624–636. DOI: 10.1111/j.1574-6941.2012.01331.x.
  41. King GM, Judd C, Kuske CR, et al. Analysis of stomach and gut microbiomes of the eastern oyster (crassostrea virginica) from coastal Louisiana, USA. PLoS ONE 2012;7(12):e51475. DOI: 10.1371/journal.pone.0051475.
  42. Husted L, Jensen TK, Olsen SN, et al. Examination of equine glandular stomach lesions for bacteria, including Helicobacter spp by fluorescence in situ hybridisation. BMC Microbiol 2010;10(1):84. DOI: 10.1186/1471-2180-10-84.
  43. Perkins GA, den Bakker HC, Burton AJ. Equine stomachs harbor an abundant and diverse mucosal microbiota. Appl Environ Microbiol 2012;78(8):2522–2532. DOI: 10.1128/AEM.06252-11.
  44. Wu S, Tian J, Wang G, et al. Characterization of bacterial community in the stomach of yellow catfish (Pelteobagrus fulvidraco) World J Microbiol Biotechnol 2012;28(5):2165–2174. DOI: 10.1007/s11274-012-1022-5.
  45. Lertpiriyapong K, Whary MT, Muthupalani S, et al. Gastric colonisation with a restricted commensal microbiota replicates the promotion of neoplastic lesions by diverse intestinal microbiota in the Helicobacter pylori INS-GAS mouse model of gastric carcinogenesis. Gut 2014;63(1):54–63. DOI: 10.1136/gutjnl-2013-305178.
  46. Russo F, Linsalata M, Orlando A. Probiotics against neoplastic transformation of gastric mucosa: effects on cell proliferation and polyamine metabolism. World J Gastroenterol 2014;20(37):13258–13272. DOI: 10.3748/wjg.v20.i37.13258.
  47. Navabi N, Johansson ME, Raghavan S, et al. Helicobacter pylori infection impairs the mucin production rate and turnover in the murine gastric mucosa. Infect Immun 2013;81(3):829–837. DOI: 10.1128/IAI.01000-12.
  48. Schmitz JM, Durham CG, Ho SB, et al. Gastric mucus alterations associated with murine Helicobacter infection. J Histochem Cytochem 2009;57(5):457–467. DOI: 10.1369/jhc.2009.952473.
  49. Schmitz JM, Durham CG, Schoeb TR, et al. Helicobacter felis-associated gastric disease in microbiota-restricted mice. J Histochem Cytochem 2011;59(9):826–841. DOI: 10.1369/0022155411416242.
  50. Noto JM, Peek RM,Jr. The gastric microbiome, its interaction with Helicobacter pylori, and its potential role in the progression to stomach cancer. PLoS Pathog 2017;13(10):e1006573. DOI: 10.1371/journal.ppat.1006573.
  51. Lee CW, Rickman B, Rogers AB, et al. Combination of sulindac and antimicrobial eradication of Helicobacter pylori prevents progression of gastric cancer in hypergastrinemic INS-GAS mice. Cancer Res 2009;69(20):8166–8174. DOI: 10.1158/0008-5472.CAN-08-3856.
  52. Lundberg JO, Weitzberg E. Biology of nitrogen oxides in the gastrointestinal tract. Gut 2013;62(4):616–629. DOI: 10.1136/gutjnl-2011-301649.
  53. Hsieh PS, Tsai YC, Chen YC, et al. Eradication of Helicobacter pylori infection by the probiotic strains Lactobacillus johnsonii MH-68 and “L. salivarius ssp. salicinius AP-32. Helicobacter 2012;17(6):466–477. DOI: 10.1111/j.1523-5378.2012.00992.x.
  54. Ge Z, Feng Y, Muthupalani S, et al. Coinfection with enterohepatic Helicobacter species can ameliorate or promote Helicobacter pylori-induced gastric pathology in C57BL/6 mice. Infect Immun 2011;79(10):3861–3871. DOI: 10.1128/IAI.05357-11.
  55. Lemke LB, Ge Z, Whary MT, et al. Concurrent Helicobacter bilis infection in C57BL/6 mice attenuates proinflammatory H. pylori-induced gastric pathology. Infect Immun 2009;77(5):2147–2158. DOI: 10.1128/IAI.01395-08.
  56. Thiraworawong T, Spinler JK, Werawatganon D, et al. Anti-inflammatory properties of gastric-derived lactobacillus plantarum XB7 in the context of Helicobacter pylori infection. Helicobacter 2014;19(2):144–155. DOI: 10.1111/hel.12105.
  57. Dharmani P, De Simone C, Chadee K. The probiotic mixture VSL#3 accelerates gastric ulcer healing by stimulating vascular endothelial growth factor. PLoS ONE 2013;8(3):e58671. DOI: 10.1371/journal.pone.0058671.
  58. Delgado S, Leite AMO, Ruas-Madiedo P, et al. Probiotic and technological properties of Lactobacillus spp. strains from the human stomach in the search for potential candidates against gastric microbial dysbiosis. Front Microbiol 2015;5:766. DOI: 10.3389/fmicb.2014.00766.
  59. Arthur JC, Perez-Chanona E, Mühlbauer M, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 2012;338(6103):120–123. DOI: 10.1126/science.1224820.
  60. Whary MT, Muthupalani S, Ge Z, et al. Helminth co-infection in Helicobacter pylori infected INS-GAS mice attenuates gastric premalignant lesions of epithelial dysplasia and glandular atrophy and preserves colonization resistance of the stomach to lower bowel microbiota. Microbes Infect Inst Pasteur 2014;16(4):345–355. DOI: 10.1016/j.micinf.2014.01.005.
PDF Share

© Jaypee Brothers Medical Publishers (P) LTD.