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Probiotics as an Alternative Therapy for Helicobacter pylori-Associated Diseases

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Helicobacter pylori Research

Abstract

Probiotics are live microorganisms which, when administered in adequate amounts, confer a health benefit to the host. Probiotics are not part of the current treatment therapies prescribed for Helicobacter pylori eradication, but there are numerous studies, most of them using probiotics as adjuvants to therapy, showing a reduction of side effects in the greater majority of cases. The probiotics administered vary hugely in the composition of microorganisms used, as well as the duration and mode of administration, which renders the comparison difficult. However, the most used probiotics for H. pylori infection are composed of Lactobacillus, Bifidobacterium, Saccharomyces, and Streptococcus. The mode of action of these probiotics relies on competition for nutrients and for adhesion to cell receptors, antimicrobial activity, and modulation of the immune system and microbiota.

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References

  • 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 23:79–84

    PubMed  Google Scholar 

  • Armuzzi A, Cremonini F, Bartolozzi F, Canducci F, Candelli M, Ojetti V et al (2001a) The effect of oral administration of Lactobacillus GG on antibiotic-associated gastrointestinal side-effects during Helicobacter pylori eradication therapy. Aliment Pharmacol Ther 15:163–169

    Article  CAS  PubMed  Google Scholar 

  • Armuzzi A, Cremonini F, Ojetti V, Bartolozzi F, Canducci F, Candelli M et al (2001b) Effect of Lactobacillus GG supplementation on antibiotic-associated gastrointestinal side effects during Helicobacter pylori eradication therapy: a pilot study. Digestion 63:1–7

    Article  CAS  PubMed  Google Scholar 

  • Aslim B, Onbasili D, Yuksekdag ZN (2011) Determination of lactic acid production and antagonistic activity against Helicobacter pylori of L. delbrueckii subsp bulgaricus and S. thermophilus strains. Kafkas Univ Vet Fak Derg 17:609–614

    Google Scholar 

  • Basso D, Plebani M, Kusters JG (2010) Pathogenesis of Helicobacter pylori infection. Helicobacter 15(Suppl 1):14–20

    Article  CAS  PubMed  Google Scholar 

  • Bergonzelli GE, Blum S, Brussow H, Corthesy-Theulaz I (2005) Probiotics as a treatment strategy for gastrointestinal diseases? Digestion 72:57–68

    Article  PubMed  Google Scholar 

  • Bernet MF, Brassart D, Neeser JR, Servin AL (1993) Adhesion of human bifidobacterial strains to cultured human intestinal epithelial cells and inhibition of enteropathogen-cell interactions. Appl Environ Microbiol 59:4121–4128

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bhatia SJ, Kochar N, Abraham P, Nair NG, Mehta AP (1989) Lactobacillus acidophilus inhibits growth of Campylobacter pylori in vitro. J Clin Microbiol 27:2328–2330

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bik EM, Eckburg PB, Gill SR, Nelson KE, Purdom EA, Francois F et al (2006) Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci U S A 103:732–737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blaser MJ (2010) Harnessing the power of the human microbiome. Proc Natl Acad Sci U S A 107:6125–6126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown SM (2013) Introduction to DNA sequencing. In: Brown SM (ed) Next-generation DNA sequencing informatics. CSHL Press, New York

    Google Scholar 

  • Canchaya C, Claesson MJ, Fitzgerald GF, van Sinderen D, O’Toole PW (2006) Diversity of the genus Lactobacillus revealed by comparative genomics of five species. Microbiology 152:3185–3196

    Article  CAS  PubMed  Google Scholar 

  • Canducci F, Armuzzi A, Cremonini F, Cammarota G, Bartolozzi F, Pola P et al (2000) A lyophilized and inactivated culture of Lactobacillus acidophilus increases Helicobacter pylori eradication rates. Aliment Pharmacol Ther 14:1625–1629

    Article  CAS  PubMed  Google Scholar 

  • Cao YJ, Qu CM, Yuan Q, Wang S, Liang S, Yang X (2005) Control of intestinal flora alteration induced by eradication therapy of Helicobacter pylori infection in the elders. Chin J Gastroenterol Hepatol 14:195–199

    Google Scholar 

  • Charlop-Powers Z, Owen JG, Reddy BV, Ternei MA, Brady SF (2014) Chemical-biogeographic survey of secondary metabolism in soil. Proc Natl Acad Sci U S A 111:3757–3762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charteris WP, Kelly PM, Morelli L, Collins JK (1998) Antibiotic susceptibility of potentially probiotic Lactobacillus species. J Food Prot 61:1636–1643

    CAS  PubMed  Google Scholar 

  • Chenoll E, Casinos B, Bataller E, Astals P, Echevarria J, Iglesias JR et al (2011) Novel probiotic Bifidobacterium bifidum CECT 7366 strain active against the pathogenic bacterium Helicobacter pylori. Appl Environ Microbiol 77:1335–1343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cindoruk M, Erkan G, Karakan T, Dursun A, Unal S (2007) Efficacy and safety of Saccharomyces boulardii in the 14-day triple anti-Helicobacter pylori therapy: a prospective randomized placebo-controlled double-blind study. Helicobacter 12:309–316

    Article  PubMed  Google Scholar 

  • Clarke G, Stilling RM, Kennedy PJ, Stanton C, Cryan JF, Dinan TG (2014) Gut microbiota: the neglected endocrine organ. Mol Endocrinol 28:1221–1238

    Article  PubMed  CAS  Google Scholar 

  • Conway PL, Gorbach SL, Goldin BR (1987) Survival of lactic acid bacteria in the human stomach and adhesion to intestinal cells. J Dairy Sci 70:1–12

    Article  CAS  PubMed  Google Scholar 

  • Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R (2009) Bacterial community variation in human body habitats across space and time. Science 326:1694–1697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costello EK, Stagaman K, Dethlefsen L, Bohannan BJ, Relman DA (2012) The application of ecological theory toward an understanding of the human microbiome. Science 336:1255–1262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cremonini F, Di CS, Covino M, Armuzzi A, Gabrielli M, Santarelli L et al (2002) Effect of different probiotic preparations on anti-Helicobacter pylori therapy-related side effects: a parallel group, triple blind, placebo-controlled study. Am J Gastroenterol 97:2744–2749

    Article  PubMed  Google Scholar 

  • Crew KD, Neugut AI (2006) Epidemiology of gastric cancer. World J Gastroenterol 12:354–362

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 19:716–721

    Article  PubMed  Google Scholar 

  • de Bortoli N, Leonardi G, Ciancia E, Merlo A, Bellini M, Costa F et al (2007) Helicobacter pylori eradication: a randomized prospective study of triple therapy versus triple therapy plus lactoferrin and probiotics. Am J Gastroenterol 102:951–956

    Article  PubMed  CAS  Google Scholar 

  • Declich P, Ambrosiani L, Grassini R, Tavani E, Bellone S, Bortoli A et al (2000) Fundic gland polyps: a still elusive entity on the eve of the year 2000. Pol J Pathol 51:3–8

    CAS  PubMed  Google Scholar 

  • Dequin S, Casaregola S (2011) The genomes of fermentative Saccharomyces. C R Biol 334:687–693

    Article  CAS  PubMed  Google Scholar 

  • Dicksved J, Lindberg M, Rosenquist M, Enroth H, Jansson JK, Engstrand L (2009) Molecular characterization of the stomach microbiota in patients with gastric cancer and in controls. J Med Microbiol 58:509–516

    Article  CAS  PubMed  Google Scholar 

  • Didari T, Solki S, Mozaffari S, Nikfar S, Abdollahi M (2014) A systematic review of the safety of probiotics. Expert Opin Drug Saf 13:227–239

    Article  PubMed  Google Scholar 

  • Duman DG, Bor S, Ozutemiz O, Sahin T, Oguz D, Istan F et al (2005) Efficacy and safety of Saccharomyces boulardii in prevention of antibiotic-associated diarrhoea due to Helicobacter pylori eradication. Eur J Gastroenterol Hepatol 17:1357–1361

    Article  PubMed  Google Scholar 

  • FAO and WHO (2001) Report on joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Ref Type: Report

    Google Scholar 

  • FAO and WHO (2002) Report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food. Ref Type: Report

    Google Scholar 

  • Fiers W, Contreras R, Duerinck F, Haegeman G, Iserentant D, Merregaert J et al (1976) Complete nucleotide sequence of bacteriophage MS2 RNA: primary and secondary structure of the replicase gene. Nature 260:500–507

    Article  CAS  PubMed  Google Scholar 

  • Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR et al (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512

    Article  CAS  PubMed  Google Scholar 

  • Francavilla R, Lionetti E, Castellaneta SP, Magista AM, Maurogiovanni G, Bucci N et al (2008) Inhibition of Helicobacter pylori infection in humans by Lactobacillus reuteri ATCC 55730 and effect on eradication therapy: a pilot study. Helicobacter 13:127–134

    Article  PubMed  Google Scholar 

  • Fujimura S, Watanabe A, Kimura K, Kaji M (2012) Probiotic mechanism of Lactobacillus gasseri OLL2716 strain against Helicobacter pylori. J Clin Microbiol 50:1134–1136

    Article  PubMed  PubMed Central  Google Scholar 

  • Goldman CG, Barrado DA, Balcarce N, Rua EC, Oshiro M, Calcagno ML et al (2006) Effect of a probiotic food as an adjuvant to triple therapy for eradication of Helicobacter pylori infection in children. Nutrition 22:984–988

    Article  PubMed  Google Scholar 

  • Gotteland M, Poliak L, Cruchet S, Brunser O (2005) Effect of regular ingestion of Saccharomyces boulardii plus inulin or Lactobacillus acidophilus LB in children colonized by Helicobacter pylori. Acta Paediatr 94:1747–1751

    Article  PubMed  Google Scholar 

  • Gotteland M, Brunser O, Cruchet S (2006) Systematic review: are probiotics useful in controlling gastric colonization by Helicobacter pylori? Aliment Pharmacol Ther 23:1077–1086

    Article  CAS  PubMed  Google Scholar 

  • Govender M, Choonara YE, Kumar P, du Toit LC, van Vuuren S, Pillay V (2014) A review of the advancements in probiotic delivery: conventional vs. non-conventional formulations for intestinal flora supplementation. AAPS PharmSciTech 15:29–43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gul S, Masud T, Maqsood S, Latif A, Irshad I, ul Haque I (2012) Streptococcus thermophilus bacteriocin, from production to their application: an overview. Afr J Microbiol Res 6:859–866

    CAS  Google Scholar 

  • Hayashi H, Sakamoto M, Benno Y (2002) Phylogenetic analysis of the human gut microbiota using 16S rDNA clone libraries and strictly anaerobic culture-based methods. Microbiol Immunol 46:535–548

    Article  CAS  PubMed  Google Scholar 

  • Hittinger CT (2013) Saccharomyces diversity and evolution: a budding model genus. Trends Genet 29:309–317

    Article  CAS  PubMed  Google Scholar 

  • Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T et al (2013) Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155:1451–1463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsieh PS, Tsai YC, Chen YC, Teh SF, Ou CM, King VA (2012) Eradication of Helicobacter pylori infection by the probiotic strains Lactobacillus johnsonii MH-68 and L. salivarius ssp. salicinius AP-32. Helicobacter 17:466–477

    Article  PubMed  Google Scholar 

  • Hurduc V, Plesca D, Dragomir D, Sajin M, Vandenplas Y (2009) A randomized, open trial evaluating the effect of Saccharomyces boulardii on the eradication rate of Helicobacter pylori infection in children. Acta Paediatr 98:127–131

    Article  CAS  PubMed  Google Scholar 

  • Isawa K, Hojo K, Yoda N, Kamiyama T, Makino S, Saito M et al (2002) Isolation and identification of a new bifidogenic growth stimulator produced by Propionibacterium freudenreichii ET-3. Biosci Biotechnol Biochem 66:679–681

    Article  CAS  PubMed  Google Scholar 

  • Isobe H, Nishiyama A, Takano T, Higuchi W, Nakagawa S, Taneike I et al (2012) Reduction of overall Helicobacter pylori colonization levels in the stomach of Mongolian gerbil by Lactobacillus johnsonii La1 (LC1) and its in vitro activities against H. pylori motility and adherence. Biosci Biotechnol Biochem 76:850–852

    Article  CAS  PubMed  Google Scholar 

  • Jimenez E, Marin ML, Martin R, Odriozola JM, Olivares M, Xaus J et al (2008) Is meconium from healthy newborns actually sterile? Res Microbiol 159:187–193

    Article  CAS  PubMed  Google Scholar 

  • Karjalainnen H, Ahlroos T, Myllyluoma E, Tynkkynen S (2012) Real-time PCR assays for strain-specific quantification of probiotic strains in human faecal samples. Int Dairy J 27:58–64

    Article  CAS  Google Scholar 

  • Kemgang TS, Kapila S, Shanmugam VP, Kapila R (2014) Cross-talk between probiotic lactobacilli and host immune system. J Appl Microbiol 117:303–319

    Article  CAS  PubMed  Google Scholar 

  • Kim MN, Kim N, Lee SH, Park YS, Hwang JH, Kim JW et al (2008) The effects of probiotics on PPI-triple therapy for Helicobacter pylori eradication. Helicobacter 13:261–268

    Article  CAS  PubMed  Google Scholar 

  • Kourelis A, Zinonos I, Kakagianni M, Christidou A, Christoglou N, Yiannaki E et al (2010) Validation of the dorsal air pouch model to predict and examine immunostimulatory responses in the gut. J Appl Microbiol 108:274–284

    Article  CAS  PubMed  Google Scholar 

  • Lambert J, Hull R (1996) Upper gastrointestinal tract disease and probiotics. Asia Pac J Clin Nutr 5:31–35

    CAS  PubMed  Google Scholar 

  • Le MV, Fayol-Messaoudi D, Servin AL (2013) Compound(s) secreted by Lactobacillus casei strain Shirota YIT9029 irreversibly and reversibly impair the swimming motility of Helicobacter pylori and Salmonella enterica serovar Typhimurium, respectively. Microbiology 159:1956–1971

    Article  CAS  Google Scholar 

  • Lesbros-Pantoflickova D, Corthesy-Theulaz I, Blum AL (2007) Helicobacter pylori and probiotics. J Nutr 137:812S–818S

    CAS  PubMed  Google Scholar 

  • Li S, Huang XL, Sui JZ, Chen SY, Xie YT, Deng Y et al (2014) Meta-analysis of randomized controlled trials on the efficacy of probiotics in Helicobacter pylori eradication therapy in children. Eur J Pediatr 173:153–161

    Article  PubMed  Google Scholar 

  • Lin WH, Lin CK, Sheu SJ, Hwang CF, Ye WT, Hwang WZ, Tsen HY (2009) Antagonistic activity of spent culture supernatants of lactic acid bacteria against Helicobacter pylori growth and infection in human gastric epithelial AGS cells. J Food Sci 74:M225–M230

    Article  CAS  PubMed  Google Scholar 

  • Ling Z, Liu X, Luo Y, Yuan L, Nelson KE, Wang Y et al (2013) Pyrosequencing analysis of the human microbiota of healthy Chinese undergraduates. BMC Genomics 14:390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lionetti E, Miniello VL, Castellaneta SP, Magista AM, de Canio A, Maurogiovanni G et al (2006) Lactobacillus reuteri therapy to reduce side-effects during anti-Helicobacter pylori treatment in children: a randomized placebo controlled trial. Aliment Pharmacol Ther 24:1461–1468

    Article  CAS  PubMed  Google Scholar 

  • Lionetti E, Indrio F, Pavone L, Borrelli G, Cavallo L, Francavilla R (2010) Role of probiotics in pediatric patients with Helicobacter pylori infection: a comprehensive review of the literature. Helicobacter 15:79–87

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Brea M, Alarcon T, Domingo D, az-Reganon J (2008) Inhibitory effect of Gram-negative and Gram-positive microorganisms against Helicobacter pylori clinical isolates. J Antimicrob Chemother 61:139–142

    Article  CAS  PubMed  Google Scholar 

  • MacKenzie DA, Defernez M, Dunn WB, Brown M, Fuller LJ, de Herrera SR et al (2008) Relatedness of medically important strains of Saccharomyces cerevisiae as revealed by phylogenetics and metabolomics. Yeast 25:501–512

    Article  CAS  PubMed  Google Scholar 

  • Malfertheiner P, Megraud F, O’Morain CA, Atherton J, Axon AT, Bazzoli F et al (2012) Management of Helicobacter pylori infection – the Maastricht IV/Florence consensus report. Gut 61:646–664

    Article  CAS  PubMed  Google Scholar 

  • Maragkoudakis PA, Zoumpopoulou G, Miaris C, Kalantzopoulos G, Pot B, Tsakalidou E (2006) Probiotic potential of Lactobacillus strains isolated from dairy products. Int Dairy J 16:189–199

    Article  CAS  Google Scholar 

  • Martin R, Jimenez E, Heilig H, Fernandez L, Marin ML, Zoetendal EG, Rodriguez JM (2009) Isolation of bifidobacteria from breast milk and assessment of the bifidobacterial population by PCR-denaturing gradient gel electrophoresis and quantitative real-time PCR. Appl Environ Microbiol 75:965–969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mattar AF, Teitelbaum DH, Drongowski RA, Yongyi F, Harmon CM, Coran AG (2002) Probiotics up-regulate MUC-2 mucin gene expression in a Caco-2 cell-culture model. Pediatr Surg Int 18:586–590

    Article  CAS  PubMed  Google Scholar 

  • Mattarelli P, Brandi G, Calabrese C, Fornari F, Prati GM, Biavati B, Sgorbati B (2014) Occurrence of Bifidobacteriaceae in human hypochlorhydria stomach. Microb Ecol Health Dis 25: 10.3402/mehd.v25.21379

    Google Scholar 

  • McFarland LV (2010) Systematic review and meta-analysis of Saccharomyces boulardii in adult patients. World J Gastroenterol 16:2202–2222

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 79:475–479

    Article  CAS  PubMed  Google Scholar 

  • Miki K, Urita Y, Ishikawa F, Iino T, Shibahara-Sone H, Akahoshi R et al (2007) Effect of Bifidobacterium bifidum fermented milk on Helicobacter pylori and serum pepsinogen levels in humans. J Dairy Sci 90:2630–2640

    Article  CAS  PubMed  Google Scholar 

  • Moles L, Gomez M, Heilig H, Bustos G, Fuentes S, de Vos W et al (2013) Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiota during the first month of life. PLoS One 8:e66986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Molina-Infante J, Gisbert JP (2013) Probiotics for Helicobacter pylori eradication therapy: not ready for prime time. Rev Esp Enferm Dig 105:441–444

    Article  PubMed  Google Scholar 

  • Myllyluoma E, Veijola L, Ahlroos T, Tynkkynen S, Kankuri E, Vapaatalo H et al (2005) Probiotic supplementation improves tolerance to Helicobacter pylori eradication therapy – a placebo-controlled, double-blind randomized pilot study. Aliment Pharmacol Ther 21:1263–1272

    Article  CAS  PubMed  Google Scholar 

  • Myllyluoma E, Ahlroos T, Veijola L, Rautelin H, Tynkkynen S, Korpela R (2007) Effects of anti-Helicobacter pylori treatment and probiotic supplementation on intestinal microbiota. Int J Antimicrob Agents 29:66–72

    Article  CAS  PubMed  Google Scholar 

  • Myllyluoma E, Ahonen AM, Korpela R, Vapaatalo H, Kankuri E (2008) Effects of multispecies probiotic combination on Helicobacter pylori infection in vitro. Clin Vaccine Immunol 15:1472–1482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 68:4642–4645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nista EC, Candelli M, Cremonini F, Cazzato IA, Zocco MA, Franceschi F et al (2004) Bacillus clausii therapy to reduce side-effects of anti-Helicobacter pylori treatment: randomized, double-blind, placebo controlled trial. Aliment Pharmacol Ther 20:1181–1188

    Article  CAS  PubMed  Google Scholar 

  • Nobel Foundation (1967) Nobel lectures. Physiology or medicine 1901–1921. Elsevier Publishing Company, Amsterdam

    Google Scholar 

  • Pacifico L, Osborn JF, Bonci E, Romaggioli S, Baldini R, Chiesa C (2014) Probiotics for the treatment of Helicobacter pylori infection in children. World J Gastroenterol 20:673–683

    Article  PubMed  PubMed Central  Google Scholar 

  • Paineau D, Carcano D, Leyer G, Darquy S, Alyanakian MA, Simoneau G et al (2008) Effects of seven potential probiotic strains on specific immune responses in healthy adults: a double-blind, randomized, controlled trial. FEMS Immunol Med Microbiol 53:107–113

    Article  CAS  PubMed  Google Scholar 

  • Park SK, Park DI, Choi JS, Kang MS, Park JH, Kim HJ et al (2007) The effect of probiotics on Helicobacter pylori eradication. Hepatogastroenterology 54:2032–2036

    PubMed  Google Scholar 

  • Patel A, Shah N, Prajapati JB (2014) Clinical appliance of probiotics in the treatment of Helicobacter pylori infection-a brief review. J Microbiol Immunol Infect 47:429–437

    Google Scholar 

  • Peterson J, Garges S, Giovanni M, McInnes P, Wang L, Schloss JA et al (2009) The NIH human microbiome project. Genome Res 19:2317–2323

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pineiro M, Stanton C (2007) Probiotic bacteria: legislative framework – requirements to evidence basis. J Nutr 137:850S–853S

    CAS  PubMed  Google Scholar 

  • Prajapati JB, Nathani NM, Patel AK, Senan S, Joshi CG (2013) Genomic analysis of dairy starter culture Streptococcus thermophilus MTCC 5461. J Microbiol Biotechnol 23:459–466

    Article  CAS  PubMed  Google Scholar 

  • Rastogi P, Saini H, Dixit J, Singhal R (2011) Probiotics and oral health. Natl J Maxillofac Surg 2:6–9

    Article  PubMed  PubMed Central  Google Scholar 

  • Redman MG, Ward EJ, Phillips RS (2014) The efficacy and safety of probiotics in people with cancer: a systematic review. Ann Oncol 25:1919–1929

    Article  CAS  PubMed  Google Scholar 

  • Rinckel LA, Savage DC (1990) Characterization of plasmids and plasmid-borne macrolide resistance from Lactobacillus sp. strain 100-33. Plasmid 23:119–125

    Article  CAS  PubMed  Google Scholar 

  • Rokka S, Myllykangas S, Joutsjoki V (2008) Effect of specific colostral antibodies and selected lactobacilli on the adhesion of Helicobacter pylori on AGS cells and the Helicobacter-induced IL-8 production. Scand J Immunol 68:280–286

    Article  CAS  PubMed  Google Scholar 

  • 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 47:709–710

    Article  CAS  PubMed  Google Scholar 

  • Sanders ME (2008) Probiotics: definition, sources, selection, and uses. Clin Infect Dis 46(Suppl 2):S58–S61

    Article  PubMed  Google Scholar 

  • Sanders ME, Klaenhammer TR (2001) Invited review: the scientific basis of Lactobacillus acidophilus NCFM functionality as a probiotic. J Dairy Sci 84:319–331

    Article  CAS  PubMed  Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74:5463–5467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saraoui T, Parayre S, Guernec G, Loux V, Montfort J, Le CA et al (2013) A unique in vivo experimental approach reveals metabolic adaptation of the probiotic Propionibacterium freudenreichii to the colon environment. BMC Genomics 14:911

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Scaccianoce G, Zullo A, Hassan C, Gentili F, Cristofari F, Cardinale V et al (2008) Triple therapies plus different probiotics for Helicobacter pylori eradication. Eur Rev Med Pharmacol Sci 12:251–256

    CAS  PubMed  Google Scholar 

  • Schnorr SL, Candela M, Rampelli S, Centanni M, Consolandi C, Basaglia G et al (2014) Gut microbiome of the Hadza hunter-gatherers. Nat Commun 5:3654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schrezenmeir J, de Vrese M (2001) Probiotics, prebiotics, and synbiotics – approaching a definition. Am J Clin Nutr 73:361S–364S

    CAS  PubMed  Google Scholar 

  • Servin AL (2004) Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 28:405–440

    Article  CAS  PubMed  Google Scholar 

  • Shavakhi A, Tabesh E, Yaghoutkar A, Hashemi H, Tabesh F, Khodadoostan M et al (2013) The effects of multistrain probiotic compound on bismuth-containing quadruple therapy for Helicobacter pylori infection: a randomized placebo-controlled triple-blind study. Helicobacter 18:280–284

    Article  CAS  PubMed  Google Scholar 

  • Sheu BS, Wu JJ, Lo CY, Wu HW, Chen JH, Lin YS, Lin MD (2002) Impact of supplement with Lactobacillus- and Bifidobacterium-containing yogurt on triple therapy for Helicobacter pylori eradication. Aliment Pharmacol Ther 16:1669–1675

    Article  PubMed  Google Scholar 

  • Sheu BS, Cheng HC, Kao AW, Wang ST, Yang YJ, Yang HB, Wu JJ (2006) 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 Nutr 83:864–869

    CAS  PubMed  Google Scholar 

  • Shirasawa Y, Shibahara-Sone H, Iino T, Ishikawa F (2010) Bifidobacterium bifidum BF-1 suppresses Helicobacter pylori-induced genes in human epithelial cells. J Dairy Sci 93:4526–4534

    Article  CAS  PubMed  Google Scholar 

  • Smelt MJ, de Haan BJ, Bron PA, van Swam I, Meijerink M, Wells JM et al (2012) L. plantarum, L. salivarius, and L. lactis attenuate Th2 responses and increase Treg frequencies in healthy mice in a strain dependent manner. PLoS One 7:e47244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solanki HK, Pawar DD, Shah DA, Prajapati VD, Jani GK, Mulla AM, Thakar PM (2013) Development of microencapsulation delivery system for long-term preservation of probiotics as biotherapeutics agent. Biomed Res Int 2013:620719

    Article  PubMed  PubMed Central  Google Scholar 

  • Song MJ, Park DI, Park JH, Kim HJ, Cho YK, Sohn CI et al (2010) The effect of probiotics and mucoprotective agents on PPI-based triple therapy for eradication of Helicobacter pylori. Helicobacter 15:206–213

    Article  CAS  PubMed  Google Scholar 

  • Sougioultzis S, Simeonidis S, Bhaskar KR, Chen X, Anton PM, Keates S et al (2006) Saccharomyces boulardii produces a soluble anti-inflammatory factor that inhibits NF-kappaB-mediated IL-8 gene expression. Biochem Biophys Res Commun 343:69–76

    Article  CAS  PubMed  Google Scholar 

  • Suau A, Bonnet R, Sutren M, Godon JJ, Gibson GR, Collins MD, Dore J (1999) Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol 65:4799–4807

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sykora J, Valeckova K, Amlerova J, Siala K, Dedek P, Watkins S et al (2005) Effects of a specially designed fermented milk product containing probiotic Lactobacillus casei DN-114 001 and the eradication of H. pylori in children: a prospective randomized double-blind study. J Clin Gastroenterol 39:692–698

    Article  CAS  PubMed  Google Scholar 

  • Szajewska H, Albrecht P, Topczewska-Cabanek A (2009) Randomized, double-blind, placebo-controlled trial: effect of Lactobacillus GG supplementation on Helicobacter pylori eradication rates and side effects during treatment in children. J Pediatr Gastroenterol Nutr 48:431–436

    Article  CAS  PubMed  Google Scholar 

  • Thierry A, Deutsch SM, Falentin H, Dalmasso M, Cousin FJ, Jan G (2011) New insights into physiology and metabolism of Propionibacterium freudenreichii. Int J Food Microbiol 149:19–27

    Article  CAS  PubMed  Google Scholar 

  • Thomas CM, Versalovic J (2010) Probiotics-host communication: modulation of signaling pathways in the intestine. Gut Microbes 1:148–163

    Article  PubMed  PubMed Central  Google Scholar 

  • Tien MT, Girardin SE, Regnault B, Le BL, Dillies MA, Coppee JY et al (2006) Anti-inflammatory effect of Lactobacillus casei on Shigella-infected human intestinal epithelial cells. J Immunol 176:1228–1237

    Article  CAS  PubMed  Google Scholar 

  • Tissier H (1906) Traitement des infections intestinales par la méthode de la flore bactérienne de l’intestin. C R Soc Biol 60:361

    Google Scholar 

  • Tobita K, Yanaka H, Otani H (2010) Lactobacillus crispatus KT-11 enhances intestinal immune functions in C3H/HeN mice. J Nutr Sci Vitaminol (Tokyo) 56:441–445

    Article  CAS  Google Scholar 

  • Tolone S, Pellino V, Vitaliti G, Lanzafame A, Tolone C (2012) Evaluation of Helicobacter pylori eradication in pediatric patients by triple therapy plus lactoferrin and probiotics compared to triple therapy alone. Ital J Pediatr 38:63

    Article  PubMed  PubMed Central  Google Scholar 

  • Tong JL, Ran ZH, Shen J, Zhang CX, Xiao SD (2007) Meta-analysis: the effect of supplementation with probiotics on eradication rates and adverse events during Helicobacter pylori eradication therapy. Aliment Pharmacol Ther 25:155–168

    Article  CAS  PubMed  Google Scholar 

  • Tuomola E, Crittenden R, Playne M, Isolauri E, Salminen S (2001) Quality assurance criteria for probiotic bacteria. Am J Clin Nutr 73:393S–398S

    CAS  PubMed  Google Scholar 

  • Turroni F, van Sinderen D, Ventura M (2011) Genomics and ecological overview of the genus Bifidobacterium. Int J Food Microbiol 149:37–44

    Article  CAS  PubMed  Google Scholar 

  • Tursi A, Brandimarte G, Giorgetti GM, Modeo ME (2004) Effect of Lactobacillus casei supplementation on the effectiveness and tolerability of a new second-line 10-day quadruple therapy after failure of a first attempt to cure Helicobacter pylori infection. Med Sci Monit 10:CR662–CR666

    PubMed  Google Scholar 

  • Urdaci MC, Bressollier P, Pinchuk I (2004) Bacillus clausii probiotic strains: antimicrobial and immunomodulatory activities. J Clin Gastroenterol 38:S86–S90

    Article  PubMed  Google Scholar 

  • Valeur N, Engel P, Carbajal N, Connolly E, Ladefoged K (2004) Colonization and immunomodulation by Lactobacillus reuteri ATCC 55730 in the human gastrointestinal tract. Appl Environ Microbiol 70:1176–1181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM et al (2013) Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 368:407–415

    Article  PubMed  CAS  Google Scholar 

  • Vandenplas Y, Brunser O, Szajewska H (2009) Saccharomyces boulardii in childhood. Eur J Pediatr 168:253–265

    Article  PubMed  Google Scholar 

  • Vanhee LM, Goeme F, Nelis HJ, Coenye T (2010) Quality control of fifteen probiotic products containing Saccharomyces boulardii. J Appl Microbiol 109:1745–1752

    CAS  PubMed  Google Scholar 

  • Vitor JM, Vale FF (2011) Alternative therapies for Helicobacter pylori: probiotics and phytomedicine. FEMS Immunol Med Microbiol 63:153–164

    Article  CAS  PubMed  Google Scholar 

  • Wang KY, Li SN, Liu CS, Perng DS, Su YC, Wu DC et al (2004) Effects of ingesting Lactobacillus- and Bifidobacterium-containing yogurt in subjects with colonized Helicobacter pylori. Am J Clin Nutr 80:737–741

    CAS  PubMed  Google Scholar 

  • Wang ZH, Gao QY, Fang JY (2013) Meta-analysis of the efficacy and safety of Lactobacillus-containing and Bifidobacterium-containing probiotic compound preparation in Helicobacter pylori eradication therapy. J Clin Gastroenterol 47:25–32

    Article  PubMed  Google Scholar 

  • Wang LL, Yu XJ, Zhan SH, Jia SJ, Tian ZB, Dong QJ (2014) Participation of microbiota in the development of gastric cancer. World J Gastroenterol 20:4948–4952

    Article  PubMed  PubMed Central  Google Scholar 

  • Wong BC, Lam SK, Wong WM, Chen JS, Zheng TT, Feng RE et al (2004) Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. JAMA 291:187–194

    Article  CAS  PubMed  Google Scholar 

  • Ya T, Zhang Q, Chu F, Merritt J, Bilige M, Sun T et al (2008) Immunological evaluation of Lactobacillus casei Zhang: a newly isolated strain from koumiss in Inner Mongolia, China. BMC Immunol 9:68

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yoon H, Kim N, Kim JY, Park SY, Park JH, Jung HC, Song IS (2011) Effects of multistrain probiotic-containing yogurt on second-line triple therapy for Helicobacter pylori infection. J Gastroenterol Hepatol 26:44–48

    Article  PubMed  Google Scholar 

  • Zhang L, Li N, Caicedo R, Neu J (2005) Alive and dead Lactobacillus rhamnosus GG decrease tumor necrosis factor-alpha-induced interleukin-8 production in Caco-2 cells. J Nutr 135:1752–1756

    CAS  PubMed  Google Scholar 

  • Zhang L, Su P, Henriksson A, O’Rourke J, Mitchell H (2008) Investigation of the immunomodulatory effects of Lactobacillus casei and Bifidobacterium lactis on Helicobacter pylori infection. Helicobacter 13:183–190

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Laboratoire de Bactériologie, Université de Bordeaux, Bordeaux, France

    Filipa F. Vale

  2. INSERM U853, Bordeaux, France

    Filipa F. Vale

  3. Host-Pathogen Interaction Unit, Research Institute for Medicines (iMed-ULIsboa), Faculty of Pharmacy, Universidade de Lisboa, Av. Prof. Gama Pinto, 1649-003, Lisboa, Portugal

    Filipa F. Vale

  4. Biochemistry and Human Biology Department, Faculty of Pharmacy, Universidade de Lisboa, Av. Prof. Gama Pinto, 1649-003, Lisboa, Portugal

    Jorge M. B. Vítor

  5. Department of Infectious Diseases, National Institute of Health Dr. Ricardo Jorge, Av. Padre Cruz, 1649-016, Lisboa, Portugal

    Mónica Oleastro

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  1. Filipa F. Vale
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  2. Jorge M. B. Vítor
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  3. Mónica Oleastro
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Correspondence to Filipa F. Vale .

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  1. Division of Microbiology;Dept of Biology, Friedrich Alexander Univ;Erlangen-Nuremb, Erlangen, Bayern, Germany

    Steffen Backert

  2. Dept of Medicine-Gastroenteology, Baylor College of Medicine, Houston, USA

    Yoshio Yamaoka

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Vale, F.F., Vítor, J.M.B., Oleastro, M. (2016). Probiotics as an Alternative Therapy for Helicobacter pylori-Associated Diseases. In: Backert, S., Yamaoka, Y. (eds) Helicobacter pylori Research. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55936-8_24

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