H.pylori and its modulation of gastrointestinal microbiota

Journal of Digestive Diseases

Volumn 16, Issue 3, 2015, Pages 109-117

  Schulz, Christian ^a,b   Koch, Nadine ^b   Schütte, Kerstin ^a   Pieper, Dietmar H ^b   Malfertheiner, Peter ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Gastric bacteria; Helicobacter pylori; Microbiome; Microbiota; Next Generation Sequencing

Indexed keywords

PROBIOTIC AGENT;

BACTERIA; ERADICATION THERAPY; GASTROINTESTINAL DISEASE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HOST; HUMAN; INTESTINE FLORA; MICROBIOME; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; STOMACH; STOMACH PH; BACTERIUM; GASTROINTESTINAL TRACT; HELICOBACTER INFECTIONS; HOST PATHOGEN INTERACTION; ISOLATION AND PURIFICATION; MEDICAL RESEARCH; MICROBIOLOGY; PHYSIOLOGY; PROCEDURES; STOMACH ACID;

BACTERIA; BIOMEDICAL RESEARCH; GASTRIC ACID; GASTROINTESTINAL DISEASES; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HOST-PATHOGEN INTERACTIONS; HUMANS; PROBIOTICS;

EID: 84925387774     PISSN: 17512972     EISSN: 17512980     Source Type: Journal    
DOI: 10.1111/1751-2980.12233     Document Type: Review

References (92)

1. Malfertheiner P, Link A, Selgrad M. Helicobacter pylori: perspectives and time trends. Nat Rev Gastroenterol Hepatol 2014; 11: 628-638.
2. Franceschi F, Zuccalà G, Roccarina D, Gasbarrini A. Clinical effects of Helicobacter pylori outside the stomach. Nat Rev Gastroenterol Hepatol 2014; 11: 234-242.
3. Basso D, Zambon CF, Letley DP etal. Clinical relevance of Helicobacter pylori cagA and vacA gene polymorphisms. Gastroenterology 2008; 135: 91-99.
4. Fischbach W, Malfertheiner P, Hoffmann JC etal. S3-Guideline 'Helicobacter pylori and gastroduodenal ulcer disease'. Z Gastroenterol 2009; 47: 68-102 (in German).
5. Malfertheiner P, Megraud F, O'Morain CA etal.; European Helicobacter Study Group. Management of Helicobacter pylori infection-the Maastricht IV/ Florence Consensus Report. Gut 2012; 61: 646-664.
6. Ménard A, Péré-Védrenne C, Haesebrouck F, Flahou B. Gastric and enterohepatic helicobacters other than Helicobacter pylori. Helicobacter 2014; 19 Suppl 1: 59-67.
7. Goh KL, Chan WK, Shiota S, Yamaoka Y. Epidemiology of Helicobacter pylori infection and public health implications. Helicobacter 2011; 16 Suppl 1: 1-9.
8. Wex T, Venerito M, Kreutzer J, Götze T, Kandulski A, Malfertheiner P. Serological prevalence of Helicobacter pylori infection in Saxony-Anhalt, Germany, in 2010. Clin Vaccine Immunol 2011; 18: 2109-2112.
9. Schreiber S, Konradt M, Groll C etal. The spatial orientation of Helicobacter pylori in the gastric mucus. Proc Natl Acad Sci U S A 2004; 101: 5024-5029.
10. Bode G, Malfertheiner P, Ditschuneit H. Invasion of campylobacter-like organisms in the duodenal mucosa in patients with active duodenal ulcer. Klin Wochenschr 1987; 65: 144-146.
11. Chen XG, Correa P, Offerhaus J etal. Ultrastructure of the gastric mucosa harboring Campylobacter-like organisms. Am J Clin Pathol 1986; 86: 575-582.
12. Necchi V, Candusso ME, Tava F etal. Intracellular, intercellular, and stromal invasion of gastric mucosa, preneoplastic lesions, and cancer by Helicobacter pylori. Gastroenterology 2007; 132: 1009-1023.
13. Dubois A, Borén T. Helicobacter pylori is invasive and it may be a facultative intracellular organism. Cell Microbiol 2007; 9: 1108-1116.
14. Hackelsberger A, Günther T, Schultze V, Peitz U, Malfertheiner P. Role of aging in the expression of Helicobacter pylori gastritis in the antrum, corpus, and cardia. Scand J Gastroenterol 1999; 34: 138-143.
15. Bayerdörffer E, Oertel H, Lehn N etal. Topographic association between active gastritis and Campylobacter pylori colonisation. J Clin Pathol 1989; 42: 834-839.
16. Malfertheiner P, Chan FK, McColl KE. Peptic ulcer disease. Lancet 2009; 374: 1449-1461.
17. McColl KE. Clinical practice. Helicobacter pylori infection. N Engl J Med 2010; 362: 1597-1604.
18. Uemura N, Okamoto S, Yamamoto S etal. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 2001; 345: 784-789.
19. Hsu PI, Lai KH, Hsu PN etal. Helicobacter pylori infection and the risk of gastric malignancy. Am J Gastroenterol 2007; 102: 725-730.
20. Wang C, Yuan Y, Hunt RH. The association between Helicobacter pylori infection and early gastric cancer: a meta-analysis. Am J Gastroenterol 2007; 102: 1789-1798.
21. Ekström AM, Held M, Hansson LE, Engstrand L, Nyrén O. Helicobacter pylori in gastric cancer established by CagA immunoblot as a marker of past infection. Gastroenterology 2001; 121: 784-791.
22. El-Omar EM, Oien K, El-Nujumi A etal. Helicobacter pylori infection and chronic gastric acid hyposecretion. Gastroenterology 1997; 113: 15-24.
23. Feldman M, Cryer B, Lee E. Effects of Helicobacter pylori gastritis on gastric secretion in healthy human beings. Am J Physiol 1998; 274: G1011-1017.
24. Stockbruegger RW. Bacterial overgrowth as a consequence of reduced gastric acidity. Scand J Gastroenterol Suppl 1985; 111: 7-16.
25. Yang I, Nell S, Suerbaum S. Survival in hostile territory: the microbiota of the stomach. FEMS Microbiol Rev 2013; 37: 736-761.
26. Lauwers GY, Fujita H, Nagata K, Shimizu M. Pathology of non-Helicobacter pylori gastritis: extending the histopathologic horizons. J Gastroenterol 2010; 45: 131-145.
27. Mowat C, Williams C, Gillen D etal. Omeprazole, Helicobacter pylori status, and alterations in the intragastric milieu facilitating bacterial N-nitrosation. Gastroenterology 2000; 119: 339-347.
28. Lofgren JL, Whary MT, Ge Z etal. Lack of commensal flora in Helicobacter pylori-infected INS-GAS mice reduces gastritis and delays intraepithelial neoplasia. Gastroenterology 2011; 140: 210-220.
29. Lertpiriyapong K, Whary MT, Muthupalani S etal. 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: 54-63.
30. Whary MT, Muthupalani S, Ge Z etal. 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 2014; 16: 345-355.
31. Malfertheiner P, Bazzoli F, Delchier JC etal.; Pylera Study Group. Helicobacter pylori eradication with a capsule containing bismuth subcitrate potassium, metronidazole, and tetracycline given with omeprazole versus clarithromycin-based triple therapy: a randomised, open-label, non-inferiority, phase 3 trial. Lancet 2011; 377: 905-913.
32. Sharma BK, Santana IA, Wood EC etal. Intragastric bacterial activity and nitrosation before, during, and after treatment with omeprazole. Br Med J (Clin Res Ed) 1984; 289: 717-719.
33. Savage DC. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 1977; 31: 107-133.
34. Sjöstedt S, Heimdahl A, Kager L, Nord CE. Microbial colonization of the oropharynx, esophagus and stomach in patients with gastric diseases. Eur J Clin Microbiol 1985; 4: 49-51.
35. Thorens J, Froehlich F, Schwizer W etal. Bacterial overgrowth during treatment with omeprazole compared with cimetidine: a prospective randomised double blind study. Gut 1996; 39: 54-59.
36. Adamsson I, Nord CE, Lundquist P, Sjöstedt S, Edlund C. 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: 629-640.
37. Zilberstein B, Quintanilha AG, Santos MA etal. Digestive tract microbiota in healthy volunteers. Clinics (Sao Paulo) 2007; 62: 47-54.
38. Monstein HJ, Tiveljung A, Kraft CH, Borch K, Jonasson J. Profiling of bacterial flora in gastric biopsies from patients with Helicobacter pylori-associated gastritis and histologically normal control individuals by temperature gradient gel electrophoresis and 16S rDNA sequence analysis. J Med Microbiol 2000; 49: 817-822.
39. Bik EM, Eckburg PB, Gill SR etal. Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci U S A 2006; 103: 732-737.
40. Engstrand L, Lindberg M. Helicobacter pylori and the gastric microbiota. Best Pract Res Clin Gastroenterol 2013; 27: 39-45.
41. Khosravi Y, Dieye Y, Loke MF, Goh KL, Vadivelu J. Streptococcus mitis induces conversion of Helicobacter pylori to coccoid cells during co-culture in vitro. PLoS One 2014; 9: e112214.
42. Rolig AS, Cech C, Ahler E, Carter JE, Ottemann KM. The degree of Helicobacter pylori-triggered inflammation is manipulated by preinfection host microbiota. Infect Immun 2013; 81: 1382-1389.
43. Sanduleanu S, Jonkers D, de Bruine A, Hameeteman W, Stockbrügger RW. Non-Helicobacter pylori bacterial flora during acid-suppressive therapy: differential findings in gastric juice and gastric mucosa. Aliment Pharmacol Ther 2001; 15: 379-388.
44. Roos S, Engstrand L, Jonsson H. Lactobacillus gastricus sp. nov., Lactobacillus antri sp. nov., Lactobacillus kalixensis sp. nov. and Lactobacillus ultunensis sp. nov., isolated from human stomach mucosa. Int J Syst Evol Microbiol 2005; 55: 77-82.
45. Kato S, Fujimura S, Kimura K etal. Non-Helicobacter bacterial flora rarely develops in the gastric mucosal layer of children. Dig Dis Sci 2006; 51: 641-646.
46. Andersson AF, Lindberg M, Jakobsson H, Bäckhed F, Nyrén P, Engstrand L. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS One 2008; 3: e2836.
47. Li XX, Wong GL, To KF etal. Bacterial microbiota profiling in gastritis without Helicobacter pylori infection or non-steroidal anti-inflammatory drug use. PLoS One 2009; 4: e7985.
48. Dicksved J, Lindberg M, Rosenquist M, Enroth H, Jansson JK, Engstrand L. Molecular characterization of the stomach microbiota in patients with gastric cancer and in controls. J Med Microbiol 2009; 58: 509-516.
49. Stearns JC, Lynch MD, Senadheera DB etal. Bacterial biogeography of the human digestive tract. Sci Rep 2011; 1: 170.
50. Maldonado-Contreras A, Goldfarb KC, Godoy-Vitorino F etal. Structure of the human gastric bacterial community in relation to Helicobacter pylori status. ISME J 2011; 5: 574-579.
51. Hu Y, He LH, Xiao D etal. Bacterial flora concurrent with Helicobacter pylori in the stomach of patients with upper gastrointestinal diseases. World J Gastroenterol 2012; 18: 1257-1261.
52. Delgado S, Cabrera-Rubio R, Mira A, Suárez A, Mayo B. Microbiological survey of the human gastric ecosystem using culturing and pyrosequencing methods. Microb Ecol 2013; 65: 763-772.
53. Eun CS, Kim BK, Han DS etal. Differences in gastric mucosal microbiota profiling in patients with chronic gastritis, intestinal metaplasia, and gastric cancer using pyrosequencing methods. Helicobacter 2014; 19: 407-416.
54. Khosravi Y, Dieye Y, Poh BH etal. Culturable bacterial microbiota of the stomach of Helicobacter pylori positive and negative gastric disease patients. Scientific World J 2014; 2014: 610421.
55. Sanduleanu S, Jonkers D, De Bruïne A, Hameeteman W, Stockbrügger 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.
56. Hagiwara T, Mukaisho K, Nakayama T, Sugihara H, Hattori T. Long-term proton pump inhibitor administration worsens atrophic corpus gastritis and promotes adenocarcinoma development in Mongolian gerbils infected with Helicobacter pylori. Gut 2011; 60: 624-630.
57. Sheh A, Fox JG. The role of the gastrointestinal microbiome in Helicobacter pylori pathogenesis. Gut Microbes 2013; 4: 505-531.
58. Mattarelli P, Brandi G, Calabrese C etal. Occurrence of Bifidobacteriaceae in human hypochlorhydria stomach. Microb Ecol Health Dis 2014; 25: 21379.
59. Sanduleanu S, Jonkers D, de Bruïne A, Hameeteman W, Stockbrügger RW. Changes in gastric mucosa and luminal environment during acid-suppressive therapy: a review in depth. Dig Liver Dis 2001; 33: 707-719.
60. Osaki T, Matsuki T, Asahara T etal. Comparative analysis of gastric bacterial microbiota in Mongolian gerbils after long-term infection with Helicobacter pylori. Microb Pathog 2012; 53: 12-18.
61. Heimesaat MM, Fischer A, Plickert R etal. Helicobacter pylori induced gastric immunopathology is associated with distinct microbiota changes in the large intestines of long-term infected Mongolian gerbils. PLoS One 2014; 9: e100362.
62. Jakobsson HE, Jernberg C, Andersson AF, Sjölund-Karlsson M, Jansson JK, Engstrand L. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS One 2010; 5: e9836.
63. Bühling A, Radun D, Müller WA, Malfertheiner P. Influence of anti-Helicobacter triple-therapy with metronidazole, omeprazole and clarithromycin on intestinal microflora. Aliment Pharmacol Ther 2001; 15: 1445-1452.
64. Myllyluoma E, Ahlroos T, Veijola L, Rautelin H, Tynkkynen S, Korpela R. Effects of anti-Helicobacter pylori treatment and probiotic supplementation on intestinal microbiota. Int J Antimicrob Agents 2007; 29: 66-72.
65. Imase K, Takahashi M, Tanaka A etal. Efficacy of Clostridium butyricum preparation concomitantly with Helicobacter pylori eradication therapy in relation to changes in the intestinal microbiota. Microbiol Immunol 2008; 52: 156-161.
66. Compare D, Nardone G. Contribution of gut microbiota to colonic and extracolonic cancer development. Dig Dis 2011; 29: 554-561.
67. Probiotics in food: Health and nutritional properties and guidelines for evaluation. Report of a Joint FAO/WHO Expert Consultation on Evaluation of Health and Nutritional Properties of Probiotics in Food including powder milk with live lactic acid bacteria. Cordoba, Argentina, 1-4 October 2001. Report of a Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food. FAO food and nutrition paper, Rome: Food and Agriculture Organization of the United Nations, 2006.
68. Zou J, Dong J, Yu X. Meta-analysis: Lactobacillus containing quadruple therapy versus standard triple first-line therapy for Helicobacter pylori eradication. Helicobacter 2009; 14: 97-107.
69. Tong JL, Ran ZH, Shen J, Zhang CX, Xiao SD. Meta-analysis: the effect of supplementation with probiotics on eradication rates and adverse events during Helicobacter pylori eradication therapy. Aliment Pharmacol Ther 2007; 25: 155-168.
70. Ryan KA, Daly P, Li Y, Hooton C, O'Toole PW. Strain-specific inhibition of Helicobacter pylori by Lactobacillus salivarius and other lactobacilli. J Antimicrob Chemother 2008; 61: 831-834.
71. Midolo PD, Lambert JR, Hull R, Luo F, Grayson ML. In vitro inhibition of Helicobacter pylori NCTC 11637 by organic acids and lactic acid bacteria. J Appl Bacteriol 1995; 79: 475-479.
72. Lorca GL, Wadström T, Valdez GF, Ljungh A. Lactobacillus acidophilus autolysins inhibit Helicobacter pylori in vitro. Curr Microbiol 2001; 42: 39-44.
73. Pinchuk IV, Bressollier P, Verneuil B etal. In vitro anti-Helicobacter pylori activity of the probiotic strain Bacillus subtilis 3 is due to secretion of antibiotics. Antimicrob Agents Chemother 2001; 45: 3156-3161.
74. Bernet MF, Brassart D, Neeser JR, Servin AL. Lactobacillus acidophilus LA 1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut 1994; 35: 483-489.
75. Mukai T, Asasaka T, Sato E, Mori K, Matsumoto M, Ohori H. Inhibition of binding of Helicobacter pylori to the glycolipid receptors by probiotic Lactobacillus reuteri. FEMS Immunol Med Microbiol 2002; 32: 105-110.
76. Skoog EC, Lindberg M, Lindén SK. Strain-dependent proliferation in response to human gastric mucin and adhesion properties of Helicobacter pylori are not affected by co-isolated Lactobacillus sp. Helicobacter 2011; 16: 9-19.
77. Johnson-Henry KC, Mitchell DJ, Avitzur Y, Galindo-Mata E, Jones NL, Sherman PM. Probiotics reduce bacterial colonization and gastric inflammation in H. pylori-infected mice. Dig Dis Sci 2004; 49: 1095-1102.
78. Verdu EF, Bercik P, Huang XX etal. The role of luminal factors in the recovery of gastric function and behavioral changes after chronic Helicobacter pylori infection. Am J Physiol Gastrointest Liver Physiol 2008; 295: G664-670.
79. Felley CP, Corthésy-Theulaz I, Rivero JL etal. Favourable effect of an acidified milk (LC-1) on Helicobacter pylori gastritis in man. Eur J Gastroenterol Hepatol 2001; 13: 25-29.
80. Pantoflickova D, Corthésy-Theulaz I, Dorta G etal. Favourable effect of regular intake of fermented milk containing Lactobacillus johnsonii on Helicobacter pylori associated gastritis. Aliment Pharmacol Ther 2003; 18: 805-813.
81. Yang Y, Sheu B. Probiotics-containing yogurts suppress Helicobacter pylori load and modify immune response and intestinal microbiota in the Helicobacter pylori-infected children. Helicobacter 2012; 17: 297-304.
82. Myllyluoma E, Ahonen A, Korpela R, Vapaatalo H, Kankuri E. Effects of multispecies probiotic combination on Helicobacter pylori infection in vitro. Clin Vaccine Immunol 2008; 15: 1472-1482.
83. Holz C, Busjahn A, Mehling H etal. Significant reduction in Helicobacter pylori load in humans with non-viable Lactobacillus reuteri DSM17648: A pilot study. Probiotics and Antimicrobial Proteins 2014 Dec 7. [Epub ahead of print].
84. Pei Z, Bini EJ, Yang L, Zhou M, Francois F, Blaser MJ. Bacterial biota in the human distal esophagus. Proc Natl Acad Sci U S A 2004; 101: 4250-4255.
85. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 2005; 43: 5721-5732.
86. Relman DA. New technologies, human-microbe interactions, and the search for previously unrecognized pathogens. J Infect Dis 2002; 186 Suppl 2: S254-258.
87. Hugenholtz P, Goebel BM, Pace NR. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 1998; 180: 4765-4774.
88. Degnan PH, Ochman H. Illumina-based analysis of microbial community diversity. ISME J 2012; 6: 183-194.
89. Zhou Y, Gao H, Mihindukulasuriya KA etal. Biogeography of the ecosystems of the healthy human body. Genome Biol 2013; 14: R1.
90. Cogen AL, Yamasaki K, Muto J etal. Staphylococcus epidermidis antimicrobial δ-toxin (phenol-soluble modulin-γ) cooperates with host antimicrobial peptides to kill group A Streptococcus. PLoS One 2010; 5: e8557.
91. Lai Y, Di Nardo A, Nakatsuji T etal. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat Med 2009; 15: 1377-1382.
92. Kamada N, Kim Y, Sham HP etal. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 2012; 336: 1325-1329.