Systematic review and meta-analysis: Multi-strain probiotics as adjunct therapy for Helicobacter pylori eradication and prevention of adverse events

United European Gastroenterology Journal

Volumn 4, Issue 4, 2016, Pages 546-561

  McFarland, Lynne V ^a   Huang, Ying ^b   Wang, Lin ^b   Malfertheiner, Peter ^c  

^a UNIVERSITY OF WASHINGTON   (United States)

^b CHILDREN S HOSPITAL OF FUDAN UNIVERSITY   (China)

^c UNIVERSITY HOSPITAL MAGDEBURG   (Germany)

Author keywords

adverse events; diarrhea; Helicobacter pylori; meta analysis; Probiotics

Indexed keywords

PROBIOTIC AGENT;

ARTICLE; BACTERIAL CLEARANCE; DRUG EFFICACY; FOLLOW UP; HELICOBACTER INFECTION; HUMAN; INCIDENCE; INFECTION PREVENTION; META ANALYSIS; PRIORITY JOURNAL; SYSTEMATIC REVIEW; TREATMENT OUTCOME;

EID: 85006201959     PISSN: 20506406     EISSN: 20506414     Source Type: Journal    
DOI: 10.1177/2050640615617358     Document Type: Article

References (71)

1. K.PapamichaelG.J.Mantzaris. Pathogenesis of Helicobacter pylori infection: Colonization, virulence factors of the bacterium and immune and non-immune host response. Nosokom Chron2012; 7: 32–37.
2. P.MalfertheinerA.LinkM.Selgrad. Helicobacter pylori: Perspectives and time trends. Nat Rev Gastroenterol Hepatol2014; 11: 628–638.
3. B.J.MarshallJ.R.Warren. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet1984; 1: 1311–1315.
4. A.C.FordD.FormanR.H.Hunt. Helicobacter pylori eradication therapy to prevent gastric cancer in healthy asymptomatic infected individuals: Systematic review and meta-analysis of randomised controlled trials. Br Med J2014; 348: g3174–g3174.
5. J.P.GisbertX.Calvet. Review article: The effectiveness of standard triple therapy for Helicobacter pylori has not changed over the last decade, but it is not good enough. Aliment Pharmacol Ther2011; 34: 1255–1268.
6. E.IerardiF.GiorgioG.Losurdo. How antibiotic resistances could change H. pylori treatment: A matter of geography?World J Gastroenterol2013; 19: 8168–8180.
7. J.C.YangC.W.LuC.J.Lin. Treatment of Helicobacter pylori infection: Current status and future concepts. World J Gastroenterol2014; 20: 5283–5293.
8. J.C.DelchierP.MalfertheinerR.Thieroff-Ekerdt. Use of a combination formulation of bismuth, metronidazole and tetracycline with omeprazole as a rescue therapy for eradication of H. pylori. Aliment Pharmacol Ther2014; 40: 171–177.
9. L.GattaN.VakilD.Vaira. Global eradication rates for Helicobacter pylori infection: Systematic review and meta-analysis of sequential therapy. Br Med J2013; 347: f4587–f4587.
10. P.MalfertheinerF.MegraudC.A.O'Morain. Management of Helicobacter pylori infection – the Maastricht IV/Florence Consensus Report. Gut2012; 61: 646–664.
11. J.P.GisbertM.RomanoA.G.Gravina. Helicobacter pylori second-line rescue therapy with levofloxacin- and bismuth-containing quadruple therapy, after failure of standard triple or non-bismuth quadruple treatments. Aliment Pharmacol Ther2015; 41: 768–775.
12. G.H.JhengI.C.WuH.Y.Shih. Comparison of second-line quadruple therapies with or without bismuth for H. pylori infection. Biomed Res Int2015; 2015: 163960–163960.
13. M.MasoodiM.Talebi-TaherK.Tabatabaie. Clarithromycin vs. gemifloxacin in quadruple therapy regimens for empiric primary treatment of H. pylori infection: A randomized clinical trial. Middle East J Dig Dis2015; 7: 88–93.
14. F.MegraudS.CoenenA.Versporten. Helicobacter pylori resistance to antibiotics in Europe and its relationship to antibiotic consumption. Gut2013; 62: 34–42.
15. S.M.WilhelmJ.L.JohnsonP.B.Kale-Pradhan. Treating bugs with bugs: The role of probiotics as adjunctive therapy for Helicobacter pylori. Ann Pharmacother2011; 45: 960–966.
16. L.V.McFarland. Application of meta-analysis to specific research fields: Lessons learned. World J Meta-analysis2015; 3: 188–192.
17. L.V.McFarlandS.Goh. Preventing pediatric antibiotic-associated diarrhea and Clostridium difficile infections with probiotics: A meta-analysis. World J Meta-analysis2013; 1: 102–120.
18. C.HillF.GuarnerG.Reid. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol2014; 11: 506–514.
19. S.SakaryaN.Gunay. Saccharomyces boulardii expresses neuraminidase activity selective for α2,3-linked sialic acid that decreases Helicobacter pylori adhesion to host cells. APMIS2014; 122: 941–950.
20. F.HongyingW.XianboY.Fang. Oral immunization with recombinant Lactobacillus acidophilus expressing the adhesin Hp0410 of Helicobacter pylori induces mucosal and systemic immune responses. Clin Vaccine Immunol2014; 21: 126–132.
21. E.MyllyluomaA.M.AhonenR.Korpela. Effects of multispecies probiotic combination on Helicobacter pylori infection in vitro. Clin Vaccine Immunol2008; 15: 1472–1482.
22. Y.J.YangB.S.Sheu. Probiotics-containing yogurts suppress Helicobacter pylori load and modify immune response and intestinal microbiota in the Helicobacter pylori-infected children. Helicobacter2012; 17: 297–304.
23. S.FujimuraA.WatanabeK.Kimura. Probiotic mechanism of Lactobacillus gasseri OLL2716 strain against Helicobacter pylori. J Clin Microbiol2012; 50: 1134–1136.
24. M.ManfrediB.BizzarriR.I.Sacchero. Helicobacter pylori infection in clinical practice: Probiotics and a combination of probiotics and lactoferrin improve compliance, but not eradication, in sequential therapy. Helicobacter2012; 17: 254–263.
25. F.CremoniniS.Di CaroM.Covino. Effect of different probiotic preparations on anti-Helicobacter pylori therapy-related side effects: A parallel group, triple blind, placebo-controlled study. Am J Gastroenterol2002; 97: 2744–2749.
26. H.YoonN.KimJ.Y.Kim. Effects of multi-strain probiotic-containing yogurt on second-line triple therapy for Helicobacter pylori infection. J Gastroenterol Hepatol2011; 26: 44–48.
27. T.Navarro-RodriguezF.M.SilvaR.C.Barbuti. Association of a probiotic to a Helicobacter pylori eradication regimen does not increase efficacy or decreases the adverse effects of the treatment: A prospective, randomized, double-blind, placebo-controlled study. BMC Gastroenterol2013; 13: 56–56.
28. L.V.McFarlandP.MalfertheinerY.Huang. Meta-analysis of single strain probiotics for the eradication of Helicobacter pylori and prevention of adverse events. World J Meta-analysis2015; 3: 97–117.
29. A.LiberatiD.G.AltmanJ.Tetzlaff. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: Explanation and elaboration. Br Med J2009; 339: e1–e34.
30. D.MoherL.ShamseerM.Clarke. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev2015; 4: 1–9.
31. L.ShamseerD.MoherM.Clarke. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: Elaboration and explanation. Br Med J2015; 349: g7647–g7647.
32. Higgins JPT and Green S (eds). Cochrane handbook for systematic reviews of interventions. Version 5.1.0. The Cochrane Collaboration, www.cochrane-handbook.org (March 2011, accessed 7 January 2015)
33. D.MoherS.HopewellK.F.Schulz. CONSORT 2010 explanation and elaboration: Updated guidelines for reporting parallel group randomized trials. J Clin Epidemiol2010; 63: e1–e37.
34. X.SunM.BrielS.Walter. Is a subgroup effect believable? Updating criteria to evaluate the credibility of subgroup analysis. Br Med J2010; 340: 850–854.
35. M.EggerG.Davey SmithM.Schneider. Bias in meta-analysis detected by a simple, graphical test. Br Med J1997; 315: 629–634.
36. C.B.BeggM.Mazumdar. Operating characteristics of a rank correlation test for publication bias. Biometrics1994; 50: 1088–1101.
37. J.L.PetersA.J.SuttonD.R.Jones. Comparison of two methods to detect publication bias in meta-analysis. JAMA2006; 295: 676–680.
38. B.S.SheuJ.J.WuC.Y.Lo. Impact of supplement with Lactobacillus- and Bifidobacterium containing yogurt on triple therapy for Helicobacter pylori eradication. Aliment Pharmacol Ther2002; 16: 1669–1675.
39. B.S.SheuH.C.ChengA.W.Kao. Pretreatment with Lactobacillus- and Bifidobacterium-containing yogurt can improve the efficacy of quadruple therapy in eradicating residual Helicobacter pylori infection after failed triple therapy. Am J Clin Nutr2006; 83: 864–869.
40. M.de VreseH.KristenP.Rautenberg. Probiotic lactobacilli and bifidobacteria in a fermented milk product with added fruit preparation reduce antibiotic associated diarrhea and Helicobacter pylori activity. J Dairy Res2011; 78: 396–403.
41. V.MirzaeeO.Rezahosseini. Randomized control trial: Comparison of Triple Therapy plus Probiotic Yogurt vs. Standard Triple Therapy on Helicobacter pylori Eradication. Iran Red Crescent Med J2012; 14: 657–666.
42. Y.H.WangY.Huang. Effect of Lactobacillus acidophilus and Bifidobacterium bifidum supplementation to standard triple therapy on Helicobacter pylori eradication and dynamic changes in intestinal flora. World J Microbiol Biotechnol2014; 30: 847–853.
43. E.PlewinskaI.Planeta-MaleckaL.Bak-Romaniszyn. Probiotics in the treatment of Helicobacter pylori infection in children (Polish). Gastroenterol Pol2006; 13: 315–319.
44. W.Ziemniak. Efficacy of Helicobacter pylori eradication taking into account its resistance to antibiotics. J Physiol Pharmacol2006; 57: 123–141.
45. O.Y.BabakL.T.Malaya. The use of Lacidofil in treatment of duodenal peptic ulcers associated with H. pylori. (Ukrainian). News of Pharmacy and Medicine2007; 5: 24–25.
46. V.L.VdovychenkoA.L.DemidovaO.A.Bidyuk. Efficiency of quadrotherapy with probiotics in patients with duodenal peptic ulcer (Ukrainian). Modern Gastroenterol2008; 5: 90–92.
47. M.N.KimN.KimS.H.Lee. The effects of probiotics on PPI-triple therapy for Helicobacter pylori eradication. Helicobacter2008; 13: 261–268.
48. Y.J.CaoC.M.QuQ.Yuan. Control of intestinal flora alteration induced by eradication therapy of Helicobacter pylori infection in the elders. Chin J Gastroenterol Hepatol2005; 14: 195–199.
49. J.Y.HuangH.B.CaoB.Y.Shi. Efficacy of bifid combining triple regimen on Helicobacter pylori eradication. Shanghai Med Pharm J2008; 12: 552–554.
50. J.J.WenR.F.Qiu. Clinical study in efficacy of bifid combining triple regimen on Helicobacter pylori eradication. J Gannan Med Univ2010; 30: 902–903.
51. X.M.HeB.S.LiY.J.Li. Bifid triple viable facilitates the sequential therapy for Helicobacter pylori eradication. Mod Digestion Intervent2011; 2: 90–92.
52. N.de BortoliG.LeonardiE.Ciancia. Helicobacter pylori eradication: A randomized prospective study of triple therapy versus triple therapy plus lactoferrin and probiotics. Am J Gastroenterol2007; 102: 951–956.
53. S.ToloneV.PellinoG.Vitaliti. Evaluation of Helicobacter pylori eradication in pediatric patients by triple therapy plus lactoferrin and probiotics compared to triple therapy alone. Ital J Pediatr2012; 38: 63–63.
54. L.V.McFarland. Deciphering meta-analytic results: A mini-review of probiotics for the prevention of paediatric antibiotic-associated diarrhea and Clostridium difficile infections. Benef Microbes2014; 2: 1–6.
55. S.Y.Lee. Current progress toward eradicating Helicobacter pylori in East Asian countries: Differences in the 2013 revised guidelines between China, Japan, and South Korea. World J Gastroenterol2014; 20: 1493–1502.
56. D.Y.Graham. Editorial-avoiding unethical H. pylori clinical trials: Susceptibility-based studies and probiotics as adjuvants. Helicobacter2015; 20: 321–325.
57. Y.DangJ.D.ReinhardtX.Zhou. The effect of probiotics supplementation on Helicobacter pylori eradication rates and side effects during eradication therapy: A meta-analysis. PLoS One2014; 9: e111030–e111030.
58. A.SachdevaJ.Nagpal. Effect of fermented milk-based probiotic preparations on Helicobacter pylori eradication: A systematic review and meta-analysis of randomized-controlled trials. Eur J Gastroenterol Hepatol2009; 21: 45–53.
59. J.ZouJ.DongX.Yu. Meta-analysis: Lactobacillus containing quadruple therapy versus standard triple first-line therapy for Helicobacter pylori eradication. Helicobacter2009; 14: 97–107.
60. Z.H.WangQ.Y.GaoJ.Y.Fang. Meta-analysis of the efficacy and safety of Lactobacillus-containing and Bifidobacterium-containing probiotic compound preparation in Helicobacter pylori eradication therapy. J Clin Gastroenterol2013; 47: 25–32.
61. L.PacificoJ.F.OsbornE.Bonci. C. Probiotics for the treatment of Helicobacter pylori infection in children. World J Gastroenterol2014; 20: 673–683.
62. S.LiX.L.HuangJ.Z.Sui. Meta-analysis of randomized controlled trials on the efficacy of probiotics in Helicobacter pylori eradication therapy in children. Eur J Pediatr2014; 173: 153–161.
63. H.Szajewska. Pooling data on different probiotics is not appropriate to assess the efficacy of probiotics. Eur J Pediatr2014; 173: 975–975.
64. Z.LvB.WangX.Zhou. Efficacy and safety of probiotics as adjuvant agents for Helicobacter pylori infection: A meta-analysis. Exp Ther Med2015; 9: 707–716.
65. X.ZhengL.LyuZ.Mei. Lactobacillus-containing probiotic supplementation increases Helicobacter pylori eradication rate: Evidence from a meta-analysis. Rev Esp Enferm Dig2013; 105: 445–453.
66. M.M.ZhangW.QianY.Y.Qin. Probiotics in Helicobacter pylori eradication therapy: A systematic review and meta-analysis. World J Gastroenterol2015; 21: 4345–4357.
67. K.Y.WangS.N.KiC.S.Liu. Effects of ingesting Lactobacillus and Bifidobacterium-containing yogurt in subjects with colonized Helicobacter pylori. Am J Clin Nutri2004; 80: 737–741.
68. S.CruchetM.C.ObregonG.Salazar. Effect of the ingestion of a dietary product containing Lactobacillus johnsonii La1 on Helicobacter pylori colonization in children. Nutrition2003; 19: 716–721.
69. R.RosaniaM.F.MinennaF.Giorgio. Probiotic multistrain treatment may eradicate Helicobacter pylori from the stomach of dyspeptics: A placebo-controlled pilot study. Inflamm Allergy Drug Targets2012; 11: 244–249.
70. B.C.JohnstonA.L.SupinaM.Ospina. Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Cochrane Database Syst Rev2007; 2: CD004827–CD004827.
71. J.ShenZ.ZuoA.Mao. Effect of probiotics on inducing remission and maintaining therapy in ulcerative colitis, Crohn's disease, and pouchitis: Meta-analysis of randomized controlled trials. Inflamm Bowel Dis2014; 20: 21–35.