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Probiotic therapy in Helicobacter pylori infection: a potential strategy against a serious pathogen?

  • Nuzhat Qureshi
  • Ping Li
  • Qing GuEmail author
Mini-Review

Abstract

Helicobacter pylori is a highly prevalent human pathogen responsible for chronic inflammation of the gastric tissues, gastroduodenal ulcers, and cancer. The treatment includes a pair of antibiotics with a proton pump inhibitor PPI. Despite the presence of different treatments, the infection rate is still increasing both in developed and developing states. The challenge of treatment failure is greatly due to the resistance of H. pylori to antibiotics and its side effects. Probiotics potential to cure H. pylori infection is well-documented. Probiotics combined with conventional treatment regime appear to have great potential in eradicating H. pylori infection, therefore, provide an excellent alternative approach to manage H. pylori load and its threatening disease outcome. Notably, anti-H. pylori activity of probiotics is strain specific,therefore establishing standard guidelines regarding the dose and formulation of individual strain is inevitable. This review is focused on probiotic’s antagonism against H. pylori summarizing their three main potential aspects: their efficiency (i) as an alternative to H. pylori eradication treatment, (ii) as an adjunct to H. pylori eradication treatment and (iii) as a vaccine delivery vehicle.

Keywords

Antibiotic resistance Side effects Alternate therapy Probiotics mechanism of action Helicobacter pylori Chronic infection Lactococcus lactis Vaccine 

Notes

Funding

This work was funded by the following organizations: The National Science Foundation of China (Grant numbers: 318755 and 316014489); International Science and Technology Cooperation Program of China (Grant number: 2013DFA32330); and National Science Foundation of Zhejiang Province (Grant number LY16C200002).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Ahmad K, Fatemeh F, Mehri N, Maryam S (2013) Probiotics for the treatment of pediatric Helicobacter pylori infection: a randomized double blind clinical trial. Iran J Pediatr 23:79–84PubMedGoogle Scholar
  2. Aiba Y, Suzuki N, Kabir AM, Takagi A, Koga Y (1998) Lactic acid-mediated suppression of Helicobacter pylori by the oral administration of Lactobacillus salivariusas a probiotic in a gnotobiotic murine model. Am J Gastroenterol 93(11):2097–2101CrossRefPubMedGoogle Scholar
  3. Armuzzi A, Cremonini F, Ojetti V, Bartolozzi F, Canducci F, Candelli M, Santarelli L, Cammarota G, De Lorenzo A, Pola P, Gasbarrini G, Gasbarrini A (2001) Effect of Lactobacillus GG supplementation on antibiotic-associated gastrointestinal side effects during Helicobacter pylori eradication therapy: a pilot study. Digestion 63:1–7CrossRefPubMedGoogle Scholar
  4. Arslan N, Yılmaz O, Demiray-Gürbüz E (2017) Importance of antimicrobial susceptibility testing for the management of eradication in Helicobacter pylori infection. World J Gastroenterol 23(16):2854–2869CrossRefPubMedPubMedCentralGoogle Scholar
  5. Backert S, Neddermann M, Maubach G, Naumann M (2016) Pathogenesis of Helicobacter pylori infection. Helicobacter 21(Suppl 1):19–25CrossRefPubMedGoogle Scholar
  6. Bagchi D, Bhattacharya G, Stohs SJ (1996) Production of reactive oxygen species by gastric cells in association with Helicobacter pylori. Free Radic Res 24:439–450CrossRefPubMedGoogle Scholar
  7. Barrera CA, Beswick EJ, Sierra JC, Bland D, Espejo R, Mifflin R, Adegboyega P, Crowe SE, Ernst PB, Reyes VE (2005) Polarized expression of CD74 by gastric epithelial cells. J Histochem Cytochem 53:1481–1489CrossRefPubMedPubMedCentralGoogle Scholar
  8. Behnsen J, Deriu E, Sassone-Corsi M, Raffatellu M (2013) Probiotics: properties, examples, and specific applications. Cold Spring Harb Perspect Med 3:A010074CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bergonzelli GE, Granato D, Pridmore RD, Marvin-Guy LF, Donnicola D, Corthésy-Theulaz IE (2006) GroEL of Lactobacillus johnsonii La1 (NCC 533) is cell surface associated: potential role in interactions with the host and the gastric pathogen Helicobacter pylori. Infect Immun 74:425–434CrossRefPubMedPubMedCentralGoogle Scholar
  10. Beswick EJ, Pinchuk IV, Das S, Powell DW, Reyes VE (2007) Expression of the programmed death ligand 1, B7-H1, on gastric epithelial cells after Helicobacter pylori exposure promotes development of CD4+ CD25+ FoxP3+ regulatory T cells. Infect Immun 75:4334–4341CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bhatia SJ, Kochar N, Abraham P, Nair NG, Mehta AP (1989) Lactobacillus acidophilus inhibits growth of Campylobacter pylori in vitro. J Clin Microbiol 27:2328–2330PubMedPubMedCentralGoogle Scholar
  12. Blaser MJ, Berg DE (2002) H.pylori and genetic diversity and risk of human disease. J Clin Invest 2:28–37Google Scholar
  13. Boonyanugomol W, Chomvarin C, Baik SC, Song JY, Hahnvajanawong C, Kim KM, Cho MJ, Lee WK, Kang HL, Rhee KH, Sripa B (2011) Role of cagA-positive Helicobacter pylori on cell proliferation, apoptosis, and inflammation in biliary cells. Dig Dis Sci 56:1682e92CrossRefGoogle Scholar
  14. Byrd JC, Yunker CK, Xu QS, Sternberg LR, Bresalier RS (2000) Inhibition of gastric mucin synthesis by Helicobacter pylori. Gastroenterol 118:1072–1079CrossRefGoogle Scholar
  15. Cadamuro AC, Rossi AF, Maniezzo NM, Silva AE (2014) Helicobacter pylori infection: host immune response, implications on gene expression and microRNAs. World J Gastroenterol 20:1424–1437CrossRefPubMedPubMedCentralGoogle Scholar
  16. Çekin AH, Şahintürk Y, Akbay Harmandar F, Uyar S, Yolcular BO, Çekin Y (2017) Use of probiotics as an adjuvant to sequential H. pylori eradication therapy: impact on eradication rates, treatment resistance, treatment-related side effects, and patient compliance. Turk J Gastroenterol 28:3–11CrossRefPubMedGoogle Scholar
  17. Chen X, Tian F, Liu X, Zhao J, Zhang HP, Zhang H, Chen W (2010) In vitro screening of lactobacilli with antagonistic activity against Helicobacter pylori from traditionally fermented foods. J Dairy Sci 93(12):5627–5634CrossRefPubMedGoogle Scholar
  18. Coconnier MH, Lievin V, Hemery E, Servin AL (1998) Antagonistic activity against Helicobacter infection in vitro and in vivo by the human Lactobacillus acidophilus strain LB. Appl Environ Microbiol 64:4573–4580PubMedPubMedCentralGoogle Scholar
  19. Corthesy-Theulaz I, Porta N, Glauser M, Sarage E, Vaney AC, Haas R, Kraehenbuhl JP, Blum A, Michetti P (1995) Oral immunization with Helicobacter pylori urease B subunit as a treatment against Helicobacter infection in mice. Gastroenterol 109:115–121CrossRefGoogle Scholar
  20. Cotter PD, Ross RP, Hill C (2013) Bacteriocins—a viable alternative toantibiotics? Nat Rev Microbiol 11(2):95–105CrossRefPubMedGoogle Scholar
  21. Covacci A, Telford JL, Del Giudice G, Parsonnet J, Rappuoli R (1999) Helicobacter pylori virulence and genetic geography. Science 284:1328–1333CrossRefPubMedGoogle Scholar
  22. Cover TL, Blanke SR (2005) Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat Rev Microbiol 3:320–332CrossRefGoogle Scholar
  23. Cover TL, Krishna US, Israel DA, Peek RM Jr (2003) Induction of gastric epithelial cell apoptosis by Helicobacter pylori vacuolating cytotoxin. Cancer Res 63:951–995PubMedGoogle Scholar
  24. Cruchet S, Obregon MC, Salazar G, Diaz E, Gotteland M (2003) Effect of the ingestion of a dietary product containing Lactobacillus johnsonii La1 on Helicobacter pylori colonization in children. Nutrition 19:716–721CrossRefPubMedGoogle Scholar
  25. Cullen TW, Giles DK, Wolf LN, Ecobichon C, Boneca IG, Trent MS (2011) Helicobacter pylori versus the host: remodeling of the bacterial outer membrane is required for survival in the gastric mucosa. PLoS Pathog 7:e10024CrossRefGoogle Scholar
  26. Dang Y, Reinhardt JD, Zhou X, Zhang G (2014) The effect of probiotic supplementation on Helicobacter pylori eradication therapy: a meta-analysis. PLoS One 9(11):1–15Google Scholar
  27. de Klerk N, Maudsdotter L, Gebreegziabher H, Saroj SD, Eriksson B, Eriksson OS, Roos S, Lindén S, Sjölinder H, Jonsson AB (2016) Lactobacilli reduce Helicobacter pylori attachment to host gastric epithelial cells by inhibiting adhesion gene expression. Infect Immun 84:1526–1535CrossRefPubMedPubMedCentralGoogle Scholar
  28. Denev SA (2006) Role of Lactobacilli in gastrointestinal ecosystem. Bulg J Agric Sci 12(1):63–114Google Scholar
  29. Dobson A, Cotter PD, Ross RP, Hill C (2011) Bacteriocin production: a probiotic trait? Appl Environ Microbiol 78(1):1–6CrossRefPubMedGoogle Scholar
  30. Doidge C, Crust I, Lee A, Buck F, Hazell S, Manne U (1994) Therapeutic immunisation against Helicobacter infection. Lancet 343:914–915CrossRefPubMedGoogle Scholar
  31. Du YQ, Su T, Fan JG, Lu YX, Zheng P, Li XH, Guo CY, Xu P, Gong YF, Li ZS (2012) Adjuvant probiotics improve the eradication effect of triple therapy for Helicobacter pyloriinfection. World J Gastroenterol 18:6302–6307CrossRefPubMedPubMedCentralGoogle Scholar
  32. Dunne C, Dolan B, Clyne M (2014) Factors that mediate colonization of the human stomach by Helicobacter pylori. World J Gastroenterol 20:5610–5624CrossRefPubMedPubMedCentralGoogle Scholar
  33. Eaton KA, Brooks CL, Morgan DR, Krakowka S (1991) Essential role of urease in pathogenesis of gastritis induced by Helicobacter pylori in gnotobiotic piglets. Infect Immun 59:2470–2475PubMedPubMedCentralGoogle Scholar
  34. Emara MH, Mohamed SY, Abdel-Aziz HR (2014) Lactobacillus reuteri in management of Helicobacter pylori infection in dyspeptic patients: a double-blind placebo-controlled randomized clinical trial. Ther Adv Gastroenterol 7:4–13CrossRefGoogle Scholar
  35. Engstrand L, Scheynius A, Påhlson C, Grimelius L, Schwan A, Gustavsson S (1989) Association of Campylobacter pylori with induced expression of class II transplantation antigens on gastric epithelial cells. Infect Immun 57:827–832PubMedPubMedCentralGoogle Scholar
  36. Fan X, Gunasena H, Cheng Z, Espejo R, Crowe SE, Ernst PB, Reyes VE (2000) Helicobacter pylori urease binds to class II MHC on gastric epithelial cells and induces their apoptosis. J Immunol 165:1918–1924CrossRefPubMedGoogle Scholar
  37. Felley CP, Corthesy-Theulaz I, Rivero JL, Sipponen P, Kaufmann M, Bauerfeind P, Wiesel PH, Brassart D, Pfeifer A, Blum AL, Michetti P (2001) Favourable effect of acidified milk (LC-1) on Helicobacter pylori gastritis in man. Eur J Gastroenterol Hepatol 13:25–29CrossRefPubMedGoogle Scholar
  38. Feng JR, Wang F, Qiu X, McFarland LV, Chen PF, Zhou R, Liu J, Zhao Q, Li J (2017) Efficacy and safety of probiotic-supplemented triple therapy for eradication of Helicobacter pylori in children: a systematic review and network meta-analysis. Eur J Clin Pharmacol 65:231–238Google Scholar
  39. Fox JG, Wang TC (2007) Inflammation, atrophy, and gastric cancer. J Clin Invest 117:60–69CrossRefPubMedGoogle Scholar
  40. Francavilla R, Lionetti E, Castellaneta SP, Magistà AM, Maurogiovanni G, Bucci N, De Canio A, Indrio F, Cavallo L, Ierardi E, Miniello VL (2008) Inhibition of Helicobacter pylori infection in humans by Lactobacillus reuteri ATCC 55730 and effect on eradication therapy: a pilot study. Helicobacter 13:127–134CrossRefPubMedGoogle Scholar
  41. Francavilla R, Polimeno L, Demichina A, Maurogiovanni G, Principi B, Scaccianoce G, Ierardi E, Russo F, Riezzo G, Di Leo A, Cavallo L, Francavilla A, Versalovic J (2014) Lactobacillus reuteri strain combination in Helicobacter pylori infection: a randomized, double-blind, placebo-controlled study. J Clin Gastroenterol 48:407–413PubMedGoogle Scholar
  42. Goderska K, Agudo Pena S, Alarcon T (2018) Helicobacter pylori treatment: antibiotics or probiotics. J Appl Microbiol Biotechnol 102(1):1–7CrossRefGoogle Scholar
  43. Goldman CG, Barrado DA, Balcarce N, Rua EC, Oshiro M, Calcagno ML, Janjetic M, Fuda J, Weill R, Salgueiro MJ, Valencia ME, Zubillaga MB, Boccio JR (2006) Effect of a probiotic food as an adjuvant to triple therapy for eradication of Helicobacter pylori infection in children. Nutrition 10:984–988CrossRefGoogle Scholar
  44. Gotteland M, Cruchet S (2003) Suppressive effect of frequent ingestion of Lactobacillus johnsonii La1 on Helicobacter pylori colonization in asymptomatic volunteers. J Antimicrob Chemother 51:1317–1319CrossRefPubMedGoogle Scholar
  45. Gotteland M, Poliak L, Cruchet S, Brunser O (2005) Effect of regular ingestion of Saccharomyces boulardii plus inulin orLactobacillus acidophilus LB in children colonized by Helicobacter pylori. Acta Paediatr 94:1747–1751CrossRefPubMedGoogle Scholar
  46. Graham DY (1998) Antibiotic resistance in Helicobacter pylori: implication for therapy. Gastroenterology 115:1272–1277CrossRefPubMedGoogle Scholar
  47. Graham DY, Malaty HM, Evans DG, Evans DJ, Klein PD, Adam E (1991) Epidemiology of Helicobacter pylori in an asymptomatic population in United States: effect of age, race, and socioeconomic status. Gastroenterology 100(6):1495–1501CrossRefPubMedGoogle Scholar
  48. Gu Q, Song D, Zhu M (2009) Oral vaccination of mice against Helicobacter pylori with recombinant Lactococcus lactis expressing urease subunit B. FEMS Immunol Med Microbiol 56(3):197–203CrossRefPubMedGoogle Scholar
  49. Harris PR, Mobley HL, Perez-Perez GI, Blaser MJ, Smith PD (1996) Helicobacter pylori urease is a potent stimulus of mononuclear phagocyte activation and inflammatory cytokine production. Gastroenterology 111:419–425CrossRefPubMedGoogle Scholar
  50. Hessey SJ, Spencer J, Wyatt JI, Sobala G, Rathbone BJ, Axon AT, Dixon MF (1990) Bacterial adhesion and disease activity in Helicobacter associated chronic gastritis. Gut 31:134–138.  https://doi.org/10.1136/gut.31.2.134 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Holz C, Busjahn A, Mehling H, Arya S, Boettner M, Habibi H, Lang C (2015) Significant reduction in Helicobacter pylori load in humans with non-viable Lactobacillus reuteri DSM17648: a pilot study. Probiotics Antimicrob Proteins 7:91–100CrossRefPubMedGoogle Scholar
  52. Holzapfel WH, Haberer P, Geisen R, Bjorkroth J, Schillinger U (2001) Taxonomy and important features of probiotic microorganisms in food nutrition. Am J Clin Nutr 73:365S–373SCrossRefPubMedGoogle Scholar
  53. IARC (1994) Schistosomes, liver flukes and Helicobacter pylori. Vol 61. International Agency for Research on Cancer. Lyon, France: IARC Press (1994) IARC Monographs on the evaluation of carcinogenic risks to humans pp.177–240Google Scholar
  54. International Agency for Research on Cancer GLOBOCAN (2012) Estimated cancer incidence, mortality and prevalence worldwide in 2012. World Health OrganisationGoogle Scholar
  55. Isolauri E, Sutas Y, Kankaanpaa P, Arvilommi H, Salminen S (2001) Probiotics: effects of immunity. Am J Clin Nutr 73(2 Suppl):S444–S450CrossRefGoogle Scholar
  56. Johnson-Henry KC, Mitchell DJ, Avitzur Y, Galindo-Mata E, Jones NL, Sherman PM (2004) Probiotics reduce bacterial colonization and gastric inflammation in H. pylori-infected mice. Dig Dis Sci 49:1095–1102CrossRefPubMedGoogle Scholar
  57. Kabir AM, Aiba Y, Takagi A, Kamiya S, Miwa T, Koga Y (1997) Prevention of Helicobacter pylori infection by Lactobacilli in a gnotobiotic murine model. Gut 41:49–55CrossRefPubMedPubMedCentralGoogle Scholar
  58. Kao CY, Sheu BS, Wu JJ (2016) Helicobacter pylori infection: an overview of bacterial virulence factors and pathogenesis. Biom J 39(1):14–23Google Scholar
  59. Karczewski J, Troost FJ, Konings I, Dekker J, Kleerebezem M, Brummer RJ, Wells JM (2010) Regulation of human epithelial tight junction proteins by Lactobacillus plantarumin vivo and protective effects on the epithelial barrier. Am J Physiol Gastrointest Liver Physiol 298(6):G851–G859CrossRefPubMedGoogle Scholar
  60. Kaur B, Garg N, Sachdev A, Kumar B (2014) Effect of the oral intake of probiotic Pediococcus acidilactici BA28 on Helicobacter pylori causing peptic ulcer in C57BL/6 mice models. Appl Biochem Biotechnol 172:973–983CrossRefPubMedGoogle Scholar
  61. Kim TS, Hur JW, Yu MA, Cheigh CI, Kim KN, Hwang JK, Pyun YR (2003) Antagonism of Helicobacter pylori by bacteriocins of lactic acid bacteria. J Food Prot 66:3–12CrossRefPubMedGoogle Scholar
  62. Kim SJ, Lee JY, Jun DY, Song JY, Lee WK, Cho MJ, Kim YH (2009) Oral administration of Lactococcus lactis expressing Helicobacter pylori Cag7-ct383 protein induces systemic anti-Cag7 immune response in mice. FEMS Immunol Med Microbiol 57:257–268CrossRefPubMedGoogle Scholar
  63. Kuipers EJ (1997) Helicobacter pyloriand the risk and management of associated diseases: gastritis, ulcer disease, atrophic gastritis and gastric cancer. Aliment Pharmacol Ther 11(1):71–88CrossRefPubMedGoogle Scholar
  64. Kusters JG, van Vliet AH, Kuipers EJ (2006) Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 19(3):449–490CrossRefPubMedPubMedCentralGoogle Scholar
  65. Lee MH, Roussel Y, Wilks M, Tabaqchali S (2001) Expression of Helicobacter pylori urease subunit B gene in Lactococcus lactis MG1363 and its use as a vaccine delivery system against H.pylori infection in mice. Vaccine 19:3927–3935CrossRefPubMedGoogle Scholar
  66. Lee KE, Khoi PN, Xia Y, Park JS, Joo YE, Kim KK, Choi SY, Jung YD (2013) Helicobacter pylori and interleukin-8 in gastric cancer. World J Gastroenterol 19(45):8192–8202CrossRefPubMedPubMedCentralGoogle Scholar
  67. Lesbros-Pantoflickova D, Corthe’Sy-Theulaz I, Blum AL (2007) Helicobacter pylori and probiotics. J Nutr 137:812S–818SCrossRefPubMedGoogle Scholar
  68. Lionetti E, Miniello VL, Castellaneta SP, Magista AM, de Canio A, Maurogiovanni G, Ierardi E, Cavallo L, Francavilla R (2006) Lactobacillus reuteritherapy to reduce side-effects during anti-Helicobacter pylori treatment in children: a randomized placebo controlled trial. Aliment Pharmacol Ther 24:1461–1468CrossRefPubMedGoogle Scholar
  69. Lorca GL, Wadström T, Valdez GF, Ljungh A (2001) Lactobacillus acidophilus autolysins inhibit Helicobacter pylori in vitro. Curr Microbiol 42:39–44CrossRefPubMedGoogle Scholar
  70. Lundgren A, Suri-Payer E, Enarsson K, Svennerholm AM, Lundin BS (2003) Helicobacter pylori-specific CD4+ CD25high regulatory T cells suppress memory T-cell responses to H. pylori in infected individuals. Infect Immun 71:1755–1762CrossRefPubMedPubMedCentralGoogle Scholar
  71. Lv X, Song H, Yang J, Li T, Xi T, Xing Y (2014) A multi-epitope vaccine CTB-UE relieves Helicobacter pylori-induced gastric inflammatory reaction via up-regulating microRNA-155 to inhibit Th17 response in C57/BL6 mice model. Hum Vaccin Immunother 10:3561–3569CrossRefPubMedPubMedCentralGoogle Scholar
  72. Mack DR, Michail S, Wei S, McDougall L, Hollingsworth MA (1999) Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am J Phys 276:G941–GG50Google Scholar
  73. Macrì A, Versaci A, Loddo S, Scuderi G, Travagliante M, Trimarchi G, Teti D, Famulari C (2006) Serum levels of interleukin 1beta, interleukin 8 and tumour necrosis factor alpha as markers of gastric cancer. Biomarkers 11:184–193CrossRefPubMedGoogle Scholar
  74. Magistà AM, Ierardi E, Castellaneta S, Miniello VL, Lionetti E, Francavilla A, Ros P, Rigillo N, Di Leo A, Francavilla R (2005) Helicobacter pylori status and symptom assessment two years after eradication in pediatric patients from a high prevalence area. J Pediatrics Gastroenterol Nutr 40:312–318CrossRefGoogle Scholar
  75. Marshall BJ, Warren RM (1984) Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 16:1311–1315CrossRefGoogle Scholar
  76. Marshall BJ, Barrett LJ, Prakash C, McCallum RW, Guerrant RL (1990) Urea protects Helicobacter (Campylobacter) pylori from the bactericidal effect of acid. Gastroenterology 99:697–702CrossRefPubMedGoogle Scholar
  77. McNicholl AG, Molina-Infante J, Lucendo AJ, Calleja JL, Pérez-Aisa Á, Modolell I, Aldeguer X, Calafat M, Comino L, Ramas M, Callejo Á, Badiola C, Serra J, Gisbert JP (2018) Probiotic supplementation with Lactobacillus plantarum and Pediococcus acidilactici for Helicobacter pylori therapy: a randomized, double-blind, placebo-controlled trial. Helicobacter 23:e12529CrossRefPubMedGoogle Scholar
  78. Mcnulty CA, Lasseter G, Shaw I, Nichols T, D’Arcy S, Lawson AJ, Glocker E (2012) Is Helicobacter pylori antibiotic resistance surveillance needed and how can it be delivered? Aliment Pharmacol Ther 35:1221–1230CrossRefPubMedGoogle Scholar
  79. Michetti P, Dorta G, Wiesel PH, Brassart D, Verdu E, Herranz M, Felley C, Porta N, Rouvet M, Blum AL, Corthésy-Theulaz I (1999) Effect of whey-based culture supernatant of Lactobacillus acidophilus (johnsonii) La1 on Helicobacter pylori infection in humans. Digestion 60:203–209CrossRefPubMedGoogle Scholar
  80. Midolo PD, Lambert JR, Hull R, Luo F, Grayson ML (1995) In vitro inhibition of Helicobacter pylori NCTC 11637 by organic acids and lactic acid bacteria. J Appl Bacteriol 79(4):475–479CrossRefPubMedGoogle Scholar
  81. Miki K, Urita Y, Ishikawa F, Iino T, Shibahara-Sone H, Akahoshi R, Mizusawa S, Nose A, Nozaki D, Hirano K, Nonaka C, Yokokura T (2007) Effect of Bifidobacterium bifidum fermented milk on Helicobacter pylori and serum pepsinogen levels in humans. J Dairy Sci 90:2630–2640CrossRefPubMedGoogle Scholar
  82. Mitchell HM, Li YY, Hu PJ, Liu Q, Chen M, Du GG, Wang ZJ, Lee A, Hazell SL (1992) Epidemiology of Helicobacter pylori in southern China: Identification of early childhood as the critical period for acquisition. J Infect Dis 166:149–153CrossRefPubMedGoogle Scholar
  83. Moayyedi P, Hunt RH (2004) Helicobacter pylori public health implications. Helicobacter 9(1):67–72CrossRefPubMedGoogle Scholar
  84. Mukai T, Asasaka T, Sato E, Mori K, Matsumoto M, Ohori H (2002) Inhibition of binding of Helicobacter pylori to the glycolipid receptors by probiotic Lactobacillus reuteri. FEMS Immunol Med Microbiol 32:105–110CrossRefPubMedGoogle Scholar
  85. Murosaki S, Muroyama K, Yamamoto Y, Yoshikai Y (2000) Antitumor effect of heat-killed Lactobacillus plantarum L-137 through restoration of impaired interleukin-12 production in tumor-bearing mice. Cancer Immunol Immunother 49:157–164CrossRefPubMedGoogle Scholar
  86. Myllyluoma E, Veijola L, Ahlroos T, Tynkkynen S, Kankuri E, Vapaatalo H, Rautelin H, Korpela R (2005) Probiotic supplementation improves tolerance to Helicobacter pylori eradication therapy a placebo-controlled, double-blind, randomized pilot study. Aliment Pharmacol Ther 21:1263–1272CrossRefPubMedGoogle Scholar
  87. Nam H, Ha M, Bae O, Lee Y (2002) Effect of Weissella confusa strain PL9001 on the adherence and growth of Helicobacter pylori. Appl Environ Microbiol 68:4642–4645CrossRefPubMedPubMedCentralGoogle Scholar
  88. Noach LA, Bosma NB, Jansen J (1994) Mucosal tumor necrosis factor alpha, interleukin-1 beta, and interleukin-8 production in patients with Helicobacter pylori infection. Scand J Gastroenterol 29:425–429CrossRefPubMedGoogle Scholar
  89. Odenbreit S, Faller G, Haas R (2002) Role of the alpAB proteins and lipopolysaccharide in adhesion of Helicobacter pylori to human gastric tissue. Int J Med Microbiol 292:247–256CrossRefPubMedGoogle Scholar
  90. Ojetti V, Bruno G, Ainora ME, Gigante G, Rizzo G, Roccarina D, Gasbarrini A (2012) Impact of Lactobacillus reuteri supplementation on anti-Helicobacter pylori Levofloxacin-Based Second-Line Therapy. Gastroenterol Res Pract:740381Google Scholar
  91. Pantoflickova D, Corthesy-Theulaz I, Dorta G, Isler P, Rochat F, Enslen M, Blum AL (2003) Favorable effect of long-term intake of fermented milk containing Lactobacillus johnsonii on H.pylori associated gastritis. Aliment Pharmacol Ther 18:805–813CrossRefPubMedGoogle Scholar
  92. Parkin DM (2006) The global health burden of infection-associated cancers in the year 2002. Int J Cancer 118:3030–3044CrossRefPubMedGoogle Scholar
  93. Patel A, Shah N, Prajapati JB (2014) Clinical application of probiotics in the treatment of Helicobacter pylori infection—a brief review. J Microbiol Immunol Infect 47:429–437CrossRefPubMedGoogle Scholar
  94. Peck B, Ortkamp M, Diehl KD, Hundt E, Knapp B (1999) Conservation, localization and expression of HopZ, a protein involved in adhesion of Helicobacter pylori. Nucleic Acids Res 27:3325–3333CrossRefPubMedPubMedCentralGoogle Scholar
  95. Peek RM Jr, Miller GG, Tham KT, Perez-Perez GI, Zhao X, Atherton JC, Blaser MJ (1995) Heightened inflammatory response and cytokine expression in vivo to cagA/ Helicobacter pylori strains. Lab Investig 71:760–770Google Scholar
  96. Peng X, Zhang R, Duan G, Sun N, Zhang L, Chen S, Fan Q, Xi Y (2018) Production and delivery of Helicobacter pylori NapA in Lactococcus lactis and its protective efficacy and immune modulatory activity. Sci Rep 8:6435CrossRefPubMedPubMedCentralGoogle Scholar
  97. Perdigón G, Medina M, Vintiñi E, Valdéz JC (2000) Intestinal pathway of internalization of lactic acid bacteria and gut mucosal immunostimulation. Int J Immunopathol Pharmacol 13:141–150PubMedGoogle Scholar
  98. Phadnis SH, ParlowM H, Levy M, Ilver D, CaulkinsC M, ConnorsJ B, DunnB E (1996) Surface localization of Helicobacter pylori urease and a heat shock protein homolog requires bacterial autolysis. Infect Immun 64(3):905–912PubMedPubMedCentralGoogle Scholar
  99. Pinchuk IV, Bressollier P, Verneuil B, Fenet B, Sorokulova IB, Megraud F, Urdaci MC (2001) In vitro anti-Helicobacter pylori activity of the probiotic strain Bacillus subtilis 3 is due to secretion of antibiotics. Antimicrob Agents Chemother 45:3156–3161CrossRefPubMedPubMedCentralGoogle Scholar
  100. Ramarao N, Gray-Owen SD, Backert S, Meyer TF (2000) Helicobacter pylori inhibits phagocytosis by professional phagocytes involving type IV secretion components. Mol Microbiol 37:1389–1404CrossRefPubMedGoogle Scholar
  101. Rickard A, Gilbert P, High N, Kolenbrander P, Handley P (2003) Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol 11(2):94–100.104CrossRefPubMedGoogle Scholar
  102. Roberts SE, Morrison-Rees S, Samuel DG, Thorne K, Akbari A, Williams JG (2016) Review article: the prevalence of Helicobacter pylori and the incidence of gastric cancer across Europe. Aliment Pharmacol Ther 43:334–345CrossRefPubMedGoogle Scholar
  103. Ruggiero P (2014) Use of probiotics in the fight against Helicobacter pylori. World J Gastrointest Pathophysiol 5(4):384–391CrossRefPubMedPubMedCentralGoogle Scholar
  104. Sakamoto I, Igarashi M, Kimura K, Takagi A, Miwa T, Koga Y (2001) Suppressive effect of Lactobacillus gasseri OLL 2716 (LG21) on Helicobacter pylori infection in humans. J Antimicrob Chemother 47:709–710CrossRefPubMedGoogle Scholar
  105. Sakarya S, Gunay N (2014) Saccharomyces boulardii expresses neuraminidase activity selective for α-2, 3-linked sialic acid that decreases Helicobacter pylori adhesion to host cells. APMIS 122:941–950CrossRefPubMedGoogle Scholar
  106. Sarowska J, Choroszy-Król I, Regulska-llow B, Frej-Mądrzak M, Jama-Kmiecik A (2013) The therapeutic effect of probiotic bacteria on gastrointestinal diseases. Adv Clin Exp Med 22:759–766PubMedGoogle Scholar
  107. Schembri M, Christiansen G, Klemm P (2001) FimH-mediated autoaggregation of Escherichia coli. Mol Microbiol 41(6):1419–1430CrossRefPubMedGoogle Scholar
  108. Seth A, Yan F, Polk DB, Rao RK (2008) Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC- and MAP kinase-dependent mechanism. Am J Physiol Gastrointest Liver Physiol 294(4):G1060–G1069CrossRefPubMedPubMedCentralGoogle Scholar
  109. Sgouras D, Maragkoudakis P, Petraki K, Martinez-Gonzalez B, Eriotou E, Michopoulos S, Kalantzopoulos G, Tsakalidou E, Mentis A (2004) In vitro and in vivo inhibition of Helicobacter pylori by Lactobacillus casei strain Shirota. Appl Environ Microbiol 70:518–526CrossRefPubMedPubMedCentralGoogle Scholar
  110. Smith SM, O’Morain C, Mcnamara D (2014) Antimicrobial susceptibility testing for Helicobacter pylori in times of increasing antibiotic resistance. World J Gastroenterol 20:9912–9921CrossRefPubMedPubMedCentralGoogle Scholar
  111. Song D, Gu Q (2009) Surface expression of Helicobacter pylori urease subunit B gene E fragment on Lactococcus lactis by means of the cell wall anchor of Staphylococcus aureus protein a. Biotechnol Lett 31:985–989CrossRefPubMedGoogle Scholar
  112. Sunanliganon C, Thong-Ngam D, Tumwasorn S, Klaikeaw N (2012) Lactobacillus plantarum B7 inhibits Helicobacter pylori growth and attenuates gastric inflammation. World J Gastroenterol 18:2472–2480CrossRefPubMedPubMedCentralGoogle Scholar
  113. Sutton P, Chionh YT (2013) Why can’t we make an effective vaccine against Helicobacter pylori? Expert Rev Vaccines 12:433–441CrossRefPubMedGoogle Scholar
  114. Sutton P, Doidge C (2003) Helicobacter pylori vaccines spiral into the new millennium. Dig Liver Dis 35(10):675–687CrossRefPubMedGoogle Scholar
  115. Sutton P, Wilson J, Kosaka T, Wolowczuk I, Lee A (2000) Therapeutic immunization against Helicobacter pylori infection in the absence of antibodies. Immunol Cell Biol 78:28–30CrossRefPubMedGoogle Scholar
  116. Tareb R, Bernardeau M, Gueguen M, Vernoux J (2013) In vitro characterization of aggregation and adhesion properties of viable and heat-killed forms of two probiotic Lactobacillus strains and interaction with foodborne zoonotic bacteria, especially Campylobacter jejuni. J Med Microbiol 62:637–649CrossRefPubMedGoogle Scholar
  117. Toracchio S, Cellini L, Di Campli E, Cappello G, Malatesta MG, Ferri A, Ciccaglione AF, Grossi L, Marzio L (2000) Role of antimicrobial susceptibility testing on efficacy of triple therapy in Helicobacter pylori eradication. Aliment Pharmacol Ther 14:1639–1643CrossRefPubMedGoogle Scholar
  118. Uitz E, Tonninger-Bahadori K, Nekrep K, Bahadori B (2017) The effect of Lactobacillus casei rhamnosus (LCR35) supplementation on the adherence tolerance and efficiency of Helicobacter pylori: an open-label, observational, non-intervational, multicentre pilot study. Int J Probiotics Prebiotics 12(4)Google Scholar
  119. Unemo M, Aspholm-Hurtig M, Ilver D, Bergström J, Borén T, Danielsson D, Teneberg S (2005) The sialic acid binding SabA adhesin of Helicobacter pylori is essential for nonopsonic activation of human neutrophils. J Biol Chem 280:15390–15397CrossRefPubMedGoogle Scholar
  120. Urrutia-Baca VH, Escamilla-García E, de la Garza-Ramos MA, Tamez-Guerra P, Gomez-Flores R, Urbina-Ríos CS (2017) In vitro antimicrobial activity and downregulation of virulence gene expression on Helicobacter pylori by Reuterin. Probiotics Antimicrob Proteins 10(2):168–175CrossRefGoogle Scholar
  121. Vandenbergh PA (1993) Lactic acid bacteria, their metabolic products and interference with microbial growth. FEMS Microbiol Rev 12:221–238CrossRefGoogle Scholar
  122. Viljanen M, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T (2005) Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: a double-blind placebo-controlled trial. Allergy 60:494–500CrossRefPubMedGoogle Scholar
  123. Wang KY, Li SN, Liu CS, Perng DS, Su YC, Wu DC, JanC M, LaiC H, WangT N, Wang W (2004) Effects of ingesting Lactobacillus and Bifidobacterium containing yogurt in subjects with colonized Helicobacter pylori. Am J Clin Nutr 80:737–741CrossRefPubMedGoogle Scholar
  124. Wang F, Feng J, Chen P, Liu X, Ma M, Zhou R, Chang Y, Liu J, Li J, Zhao Q (2017) Probiotics in Helicobacter pylori eradication therapy: systematic review and network meta-analysis. Res Hepatol Clin Gastroenterol 41:466–475CrossRefGoogle Scholar
  125. Wiese M, Eljaszewicz A, Andryszczyk M, Gronek S, Gackowska L, Kubiszewska I, Kaszewski W, Helmin-Basa A, Januszewska M, Motyl I, Wieczynska J, Michalkiewicz J (2012) Immunomodulatory effects of Lactobacillous plantarum and Helicobacter pylori CagA+ on the expression of selected superficial molecules on monocyte and lymphocyte and the synthesis of cytokines in whole blood culture. J Physiol Pharmacol 63(3):217–224PubMedGoogle Scholar
  126. Wilhelm SM, Johnson JL, Kale-Pradhan PB (2011) Treating bugs with bugs: the role of probiotics as adjunctive therapy for Helicobacter pylori. Ann Pharmacother 45:960–966CrossRefPubMedGoogle Scholar
  127. Winter JA, Letley DP, Cook KW, Rhead JL, Zaitoun AA, Ingram RJ, Amilon KR, Croxall NJ, Kaye PV, Robinson K, Atherton JC (2014) A role for the vacuolating cytotoxin, VacA, in colonization and Helicobacter pylori-induced metaplasia in the stomach. J Infect Dis 210:954–963CrossRefPubMedPubMedCentralGoogle Scholar
  128. Yang YJ, Chuang CC, Yang HB, Lu CC, Sheu BS (2012) Lactobacillus acidophilus ameliorates H. pylori-induced gastric inflammation by inactivating the Smad7 and NFκB pathways. BMC Microbiol 12:38CrossRefPubMedPubMedCentralGoogle Scholar
  129. Zeng M, Mao XH, Li JX, Tong WD, Wang B, Zhang YJ, Guo G, Zhao ZJ, Li L, Wu DL, Lu DS, Tan ZM, Liang HY, Wu C, Li DH, Luo P, Zeng H, Zhang WJ, Zhang JY, Guo BT, Zhu FC, Zou QM (2015) Efficacy, safety, and immunogenicity of an oral recombinant Helicobacter pylori vaccine in children in China: a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 386:1457–1464CrossRefPubMedGoogle Scholar
  130. Zheng PY, Jones NL (2003) Helicobacter pylori strains expressing the vacuolating cytotoxin interrupt phagosome maturation in macrophages by recruiting and retaining TACO (coronin 1) protein. Cell Microbiol 5:25–40CrossRefPubMedGoogle Scholar
  131. Zheng X, Lyu L, Mei Z (2013) Lactobacillus-containing probiotic supplementation increases Helicobacter pylori eradication rate: evidence from a meta-analysis. Rev Esp Enferm Dig 105:445–453CrossRefPubMedGoogle Scholar
  132. Zhou C, Ma FZ, Deng XJ, Yuan H, Ma HS (2008) Lactobacilli inhibit interleukin-8 production induced by Helicobacter pylori lipopolysaccharide-activated toll-like receptor 4. World J Gastroenterol 14:5090–5095CrossRefPubMedPubMedCentralGoogle Scholar
  133. Zhou Z, Gong S, Li XM, Yang Y, Guan R, Zhou S, Yao S, Xie Y, Ou Z, Zhao J, Liu Z (2015) Expression of Helicobacter pylori urease B on the surface of Bacillus subtilis spores. J Med Microbiol 64(Pt):104–110CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory for Food Microbial Technology of Zhejiang Province, Department of BiotechnologyZhejiang Gongshang UniversityHangzhouPeople’s Republic of China

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