Role of Probiotics in Prophylaxis of Helicobacter pylori Infection

Author(s): Kashyapi Chakravarty, Smriti Gaur*.

Journal Name: Current Pharmaceutical Biotechnology

Volume 20 , Issue 2 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Helicobacter pylori, a pathogenic bacterium, has been known to be the root cause of numerous gastrointestinal disorders. In patients showing symptoms of its infection, antibiotic therapy is a likely treatment. However, the high cost of antibiotic therapy, associated antibiotic resistance along with other adverse effects has led to the use of probiotics for Helicobacter pylori treatment. In recent times, probiotics have played an essential role as complementary prophylaxis for gastrointestinal diseases, thus minimizing antibiotics’ usage and their side effects. Probiotics are live microbial agents that exude beneficial effects on their hosts when administered in the proper dosage. The growth of the organism has been reported to be inhibited to a great extent by probiotics and research employing animal models has shown a significant reduction in H. pylori-associated gastric inflammation. In human clinical trials, it has been observed that treatment with probiotics alleviated gastritis symptoms caused by H. pylori and reduced colonization of the organism. As expected, complete eradication of H. pylori infection has not yet been reported by the administration of probiotics alone. Complement treatments using probiotics have shown to benefit infected individuals by decreasing the harmful effects of H. pylori eradication treatment using antibiotics. Long-term administration of probiotics might have favourable outcomes in H. pylori infection especially by decreasing the risk of development of diseases caused by increased levels of gastric inflammation. One such chronic condition is gastric ulcer which occurs due to considerable damage to the mucosal barrier by H. pylori colonization. This review provides a brief description of the promising role of probiotics as a complementary treatment to control H. pylori infection and consequently the management of various gastrointestinal disorders among populations with a special focus on gastric ulcer.

Keywords: Probiotics, Helicobacter pylori, gastrointestinal disorders, gastric ulcer, gastric inflammation, complement treatment.

Patel, A.; Shah, N.; Prajapati, J.B. Clinical application of probiotics in the treatment of Helicobacter pylori infection-a brief review. J. Microbiol. Immunol. Infect., 2014, 47(5), 429-437.
Go, M.F. Natural history and epidemiology of Helicobacter pylori infection. Aliment. Pharmacol. Ther., 2002, 16, 3-15.
Lesbros-Pantoflickova, D.; Corthesy-Theulaz, I.; Blum, A.L. Helicobacter pylori and probiotics. J. Nutr., 2007, 137(3), 812S-818S.
Kusters, J.G.; van Vliet, A.H.M.; Kuipers, E.J. Pathogenesis of Helicobacter pylori infection. Clin. Microbiol. Rev., 2006, 19, 449-490.
Brown, L.M. Helicobacter pylori: Epidemiology and routes of transmission. Epidemiol. Rev., 2000, 22, 283-297.
Malfertheiner, P.; Megraud, F.; O’Morain, C.; Hungin, A.P.S.; Jones, R.; Axon, A.; Graham, D.Y.; Tytgat, G. Current concepts in the management of Helicobacter pylori infection-the Maastricht 2-2000 Consensus Report. Aliment. Pharmacol. Ther., 2002, 16, 167-180.
Gerrits, M.M.; van Vliet, A.H.M.; Kuipers, E.J.; Kusters, J.G. Helicobacter pylori and antimicrobial resistance: molecular mechanisms and clinical implications. Lancet Infect. Dis., 2006, 6, 699-709.
FAO/WHO. Guidelines for the evaluation of probiotics in food. Report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food. London, Ontario, Canada, World Health Organization. fs_management/en/probiotic_guidelines.pdf (Accessed January 25, 2019)
Marshall, B.J.; Warren, J.R. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet, 1984, 323(8390), 1311-1315.
Ghotaslou, R.; Milani, M.; Akhi, M.T.; Nahaei, M.R.; Hasani, A.; Hejazi, M.S.; Meshkini, M. Diversity of Helicobacter pylori cagA and vacA genes and its relationship with clinical outcomes in Azerbaijan, Iran. Adv. Pharm. Bull., 2013, 3, 57-62.
Dadashzadeh, K.; Milani, M.; Rahmati, M.; Akbarzadeh, A. Real-Time PCR detection of 16S rRNA novel mutations associated with Helicobacter pylori tetracycline resistance in Iran. Asian Pac. J. Cancer Prev., 2014, 15, 8883-8886.
Lee, J.H.; Jun, S.H.; Kim, J-M.; Baik, S.C.; Lee, J.C. Morphological changes in human gastric epithelial cells induced by nuclear targeting of Helicobacter pylori urease subunit A. J. Microbiol., 2015, 53, 406-414.
Hellmig, S.; Ott, S.; Rosenstiel, P.; Fölsch, U.R.; Hampe, J.; Schreiber, S. Genetic variants in matrix metalloproteinase genes are associated with development of gastric ulcer in H. pylori infection. Am. J. Gastroenterol., 2006, 101, 29-35.
Lehours, P.; Zheng, Z.; Skoglund, A.; Mégraud, F.; Engstrand, L. Is there a link between the lipopolysaccharide of Helicobacter pylori gastric MALT lymphoma associated strains and lymphoma pathogenesis? PLoS One, 2009, 4, e7297.
Uemura, N.; Okamoto, S.; Yamamoto, S.; Matsumura, N.; Yamaguchi, S.; Yamakido, M.; Taniyama, K.; Sasaki, N.; Schlemper, R.J. Helicobacter pylori infection and the development of gastric cancer. N. Engl. J. Med., 2001, 345, 784-789.
Salihefendic, N.; Zildzic, M.; Cabric, E. A New approach to the management of uninvestigated dyspepsia in primary care. Med. Arh., 2015, 69, 133-134.
Kafshdooz, T.; Akbarzadeh, A.; Seghinsara, A.M.; Pourhassan, M.; Nasrabadi, H.T.; Milani, M. Role of probiotics in managing of Helicobacter pylori infection: A review. Drug Res., 2017, 67(02), 88-93.
Gong, Y.; Li, Y.; Sun, Q. Probiotics improve efficacy and tolerability of triple therapy to eradicate Helicobacter pylori: A meta-analysis of randomized controlled trials. Int. J. Clin. Exp. Med., 2015, 8(4), 6530-6543.
Richter, J.E. H pylori: The bug is not all bad. Gut, 2001, 49, 319-321.
Dunn, B.E.; Campbell, G.P.; Perez-Perez, G.I.; Blaser, M.J. Purification and characterization of urease from Helicobacter pylori. J. Biol. Chem., 1990, 265, 9464-9469.
Tokunaga, Y.; Shirahase, H.; Hoppou, T.; Kitaoka, A.; Tokuka, A.; Ohsumi, K. Density of Helicobacter pylori infection evaluated semiquantitatively in gastric cancer. J. Clin. Gastroenterol., 2000, 31, 217-221.
Yamaoka, Y.; Kodama, T.; Kita, M.; Imanishi, J.; Kashima, K.; Graham, D. Relation between clinical presentation, Helicobacter pylori density, interleukin 1β and 8 production, and cagA status. Gut, 1999, 45, 804-811.
Miftahussurur, M.; Yamaoka, Y. Appropriate first-line regimens to combat Helicobacter pylori antibiotic resistance: An Asian perspective. Molecules, 2015, 20, 6068-6092.
Yazbek, P.B.; Trindade, A.B.; Chin, C.M.; Dos Santos, J.L. Challenges to the treatment and new perspectives for the eradication of Helicobacter pylori. Dig. Dis. Sci., 2015, 60(10), 2901-2912.
Isolauri, E.; Kirjavainen, P.V.; Salminen, S. Probiotics: A role in the treatment of intestinal infection and inflammation? Gut, 2002, 50, iii54-iii59.
Marteau, P.; Seksik, P.; Jian, R. Probiotics and intestinal health effects: a clinical perspective. Br. J. Nutr., 2002, 88(S1), s51-s57.
Megraud, F. Helicobacter pylori and antibiotic resistance. Gut, 2007, 56, 1502.
Pacifico, L.; Osborn, J.F.; Bonci, E.; Romaggioli, S.; Baldini, R.; Chiesa, C. Probiotics for the treatment of Helicobacter pylori infection in children. World J. Gastroenterol., 2014, 20, 673-683.
Homan, M.; Orel, R. Are probiotics useful in Helicobacter pylori eradication? World J. Gastroenterol., 2015, 21(37), 10644-10653.
Kao, C-Y.; Sheu, B-S.; Wu, J-J. Helicobacter pylori infection: An overview of bacterial virulence factors and pathogenesis. Biomed. J., 2016, 39(1), 14-23.
Malfertheiner, P.; Chan, F.K.L.; McColl, K.E.L. Peptic ulcer disease. Lancet, 2009, 374, 1449-1461.
Hirayama, F.; Takagi, S.; Kusuhara, H.; Iwao, E.; Yokoyama, Y.; Ikeda, Y. Induction of gastric ulcer and intestinal metaplasia in Mongolian gerbils infected with Helicobacter pylori. J. Gastroenterol., 1996, 31, 755-757.
Wang, G-Z.; Huang, G-P.; Yin, G-L.; Zhou, G.; Guo, C-J.; Xie, C-G.; Jia, B-B.; Wang, J-F. Aspirin can elicit the recurrence of gastric ulcer induced with acetic acid in rats. Cell. Physiol. Biochem., 2007, 20, 205-212.
Tarnawski, A.; Ahluwalia, A.; Jones, M.K. Gastric cytoprotection beyond prostaglandins: Cellular and molecular mechanisms of gastroprotective and ulcer healing actions of antacids. Curr. Pharm. Des., 2013, 19, 126-132.
Hwang, J.J.; Lee, D.H.; Lee, A-R.; Yoon, H.; Shin, C.M.; Park, Y.S.; Kim, N. Characteristics of gastric cancer in peptic ulcer patients with Helicobacter pylori infection. World J. Gastroenterol., 2015, 21, 4954-4960.
Lau, J.Y.W.; Barkun, A.; Fan, D-m.; Kuipers, E.J.; Yang, Y-s.; Chan, F.K.L. Challenges in the management of acute peptic ulcer bleeding. Lancet, 2013, 381, 2033-2043.
Taş, İ.; Ülger, B.V.; Önder, A.; Kapan, M.; Bozdağ, Z. Risk factors influencing morbidity and mortality in perforated peptic ulcer disease. Ulus. Cerrahi Derg., 2015, 31, 20-25.
Malfertheiner, P. Helicobacter pylori infection-management from a European perspective. Dig. Dis., 2014, 32, 275-280.
Karam, S.M.; Forte, J.G. Inhibiting gastric H(+)-K(+)-ATPase activity by omeprazole promotes degeneration and production of parietal cells. Am. J. Physiol., 1994, 266, G745-G758.
Wallace, T.C.; Guarner, F.; Madsen, K.; Cabana, M.D.; Gibson, G.; Hentges, E.; Sanders, M.E. Human gut microbiota and its relationship to health and disease. Nutr. Rev., 2011, 69, 392-403.
Ghotaslou, R.; Leylabadlo, H.E.; Asl, Y.M. Prevalence of antibiotic resistance in Helicobacter pylori: A recent literature review. World J. Methodol., 2015, 5, 164-174.
Howden, C.W.; Chey, W.D.; Vakil, N.B. Clinical rationale for confirmation testing after treatment of Helicobacter pylori infection: Implications of rising antibiotic resistance. Gastroenterol. Hepatol. (N. Y.), 2014, 10(7)(Suppl. 3), S1-S19.
Arakawa, T.; Watanabe, T.; Tanigawa, T.; Tominaga, K.; Fujiwara, Y.; Morimoto, K. Quality of ulcer healing in gastrointestinal tract: Its pathophysiology and clinical relevance. World J. Gastroenterol., 2012, 18, 4811-4822.
Tarnawski, A.; Hollander, D.; Krause, W.J.; Dabros, W.; Stachura, J.; Gergely, H. ‘Healed’ experimental gastric ulcers remain histologically and ultrastructurally abnormal. J. Clin. Gastroenterol., 1990, 12(Suppl. 1), S139-S147.
Watanabe, T.; Higuchi, K.; Tominaga, K.; Fujiwara, Y.; Arakawa, T. Acid regulates inflammatory response in a rat model of induction of gastric ulcer recurrence by interleukin 1beta. Gut, 2001, 48, 774-781.
Khoder, G.; Al-Menhali, A.A.; Al-Yassir, F.; Karam, S.M. Potential role of probiotics in the management of gastric ulcer. Exp. Ther. Med., 2016, 12(1), 3-17.
Elliott, S.N.; Buret, A.; McKnight, W.; Miller, M.J.S.; Wallace, J.L. Bacteria rapidly colonize and modulate healing of gastric ulcers in rats. Am. J. Physiol., 1998, 275, G425-G432.
Lilly, D.M.; Stillwell, R.H. Probiotics: Growth-promoting factors produced by microorganisms. Science, 1965, 147, 747-748.
Podolsky, S.H. Metchnikoff and the microbiome. Lancet, 2012, 380, 1810-1811.
Hill, C.; Guarner, F.; Reid, G.; Gibson, G.R.; Merenstein, D.J.; Pot, B.; Morelli, L.; Canani, R.B.; Flint, H.J.; Salminen, S.; Calder, P.C.; Sanders, M.E. 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. Hepatol., 2014, 11(8), 506-514.
Wallace, J.L.; Syer, S.; Denou, E.; de Palma, G.; Vong, L.; McKnight, W.; Jury, J.; Bolla, M.; Bercik, P.; Collins, S.M.; Verdu, E.; Ongini, E. Proton pump inhibitors exacerbate NSAID-induced small intestinal injury by inducing dysbiosis. Gastroenterology, 2011, 141(4), 1314-1322.
Bezkorovainy, A. Probiotics: Determinants of survival and growth in the gut. Am. J. Clin. Nutr., 2001, 73(2), S399-S405.
Cain, A.M.; Karpa, K.D. Clinical utility of probiotics in inflammatory bowel disease. Altern. Ther. Health Med., 2011, 17, 72-79.
Hong, W-S.; Chen, Y-P.; Chen, M-J. The antiallergic effect of kefir lactobacilli. J. Food Sci., 2010, 75, H244-H253.
Isolauri, E.; Sütas, Y.; Kankaanpää, P.; Arvilommi, H.; Salminen, S. Probiotics: Effects on immunity. Am. J. Clin. Nutr., 2001, 73(2), S444-S450.
Shyu, P.T.; Oyong, G.G.; Cabrera, E.C. Cytotoxicity of probiotics from Philippine commercial dairy products on cancer cells and the effect on expression of cfos and cjun early apoptotic-promoting genes and interleukin 1β and tumor necrosis factor-α proinflammatory cytokine genes. BioMed Res. Int., 2014, 491740.
Uchida, M.; Shimizu, K.; Kurakazu, K. Yogurt containing Lactobacillus gasseri OLL 2716 (LG21 yogurt) accelerated the healing of acetic acid-induced gastric ulcer in rats. Biosci. Biotechnol. Biochem., 2010, 74, 1891-1894.
Uchida, M.; Kurakazu, K. Yogurt containing Lactobacillus gasseri OLL2716 exerts gastroprotective action against acute gastric lesion and antral ulcer in rats. J. Pharmacol. Sci., 2004, 96, 84-90.
Singh, P.K.; Kaur, I.P. Synbiotic (probiotic and ginger extract) loaded floating beads: A novel therapeutic option in an experimental paradigm of gastric ulcer. J. Pharm. Pharmacol., 2012, 64, 207-217.
Singh, P.K.; Deol, P.K.; Kaur, I.P. Entrapment of Lactobacillus acidophilus into alginate beads for the effective treatment of cold restraint stress induced gastric ulcer. Food Funct., 2012, 3, 83-90.
Lam, E.K.Y.; Yu, L.; Wong, H.P.S.; Wu, W.K.K.; Shin, V.Y.; Tai, E.K.K.; So, W.H.L.; Woo, P.C.Y.; Cho, C.H. Probiotic Lactobacillus rhamnosus GG enhances gastric ulcer healing in rats. Eur. J. Pharmacol., 2007, 565, 171-179.
Dharmani, P.; De Simone, C.; Chadee, K. The probiotic mixture VSL#3 accelerates gastric ulcer healing by stimulating vascular endothelial growth factor. PLoS One, 2013, 8(3), e58671.
Lam, E.K.Y.; Tai, E.K.K.; Koo, M.W.L.; Wong, H.P.S.; Wu, W.K.K.; Yu, L.; So, W.H.L.; Woo, P.C.Y.; Cho, C.H. Enhancement of gastric mucosal integrity by Lactobacillus rhamnosus GG. Life Sci., 2007, 80, 2128-2136.
Timmerman, H.M.; Koning, C.J.M.; Mulder, L.; Rombouts, F.M.; Beynen, A.C. Monostrain, multistrain and multispecies probiotics a comparison of functionality and efficacy. Int. J. Food Microbiol., 2004, 96, 219-233.
Flatley, E.A.; Wilde, A.M.; Nailor, M.D. Saccharomyces boulardii for the prevention of hospital onset Clostridium difficile infection. J. Gastrointestin. Liver Dis., 2015, 24, 21-24.
Girard, P.; Coppé, M.C.; Pansart, Y.; Gillardin, J.M. Gastroprotective effect of Saccharomyces boulardii in a rat model of ibuprofen-induced gastric ulcer. Pharmacology, 2010, 85, 188-193.
Sakarya, S.; Gunay, N. Saccharomyces boulardii expresses neuraminidase activity selective for α2,3-linked sialic acid that decreases Helicobacter pylori adhesion to host cells. APMIS, 2014, 122, 941-950.
Aragon, G.; Graham, D.B.; Borum, M.; Doman, D.B. Probiotic therapy for irritable bowel syndrome. Gastroenterol. Hepatol., 2010, 6, 39-44.
Brenner, D.M.; Moeller, M.J.; Chey, W.D.; Schoenfeld, P.S. The utility of probiotics in the treatment of irritable bowel syndrome: A systematic review. Am. J. Gastroenterol., 2009, 104, 1033-1049.
Moayyedi, P.; Ford, A.C.; Talley, N.J.; Cremonini, F.; Foxx-Orenstein, A.E.; Brandt, L.J.; Quigley, E.M. The efficacy of probiotics in the treatment of irritable bowel syndrome: A systematic review. Gut, 2010, 59, 325-332.
Cha, B.K.; Jung, S.M.; Choi, C.H.; Song, I-D.; Lee, H.W.; Kim, H.J.; Hyuk, J.; Chang, S.K.; Kim, K.; Chung, W-S.; Seo, J-G. The effect of a multispecies probiotic mixture on the symptoms and fecal microbiota in diarrhea-dominant irritable bowel syndrome: A randomized, double-blind, placebo-controlled trial. J. Clin. Gastroenterol., 2012, 46, 220-227.
Lyra, A.; Krogius-Kurikka, L.; Nikkilä, J.; Malinen, E.; Kajander, K.; Kurikka, K.; Korpela, R.; Palva, A. Effect of a multispecies probiotic supplement on quantity of irritable bowel syndrome related intestinal microbial phylotypes. BMC Gastroenterol., 2010, 10, 110.
Fuochi, V.; Petronio, G.P.; Lissandrello, E.; Furneri, P.M. Evaluation of resistance to low pH and bile salts of human Lactobacillus spp. isolates. Int. J. Immunopathol. Pharmacol., 2015, 28, 426-433.
Lankaputhra, W.E.V.; Shah, N.P. Survival of Lactobacillus acidophilus and Bifidobacterium spp. in the presence of acid and bile salts. Cultured Dairy Prod. J., 1995, 30, 2-7.
Pochart, P.; Marteau, P.; Bouhnik, Y.; Goderel, I.; Bourlioux, P.; Rambaud, J-C. Survival of bifidobacteria ingested via fermented milk during their passage through the human small intestine: An in vivo study using intestinal perfusion. Am. J. Clin. Nutr., 1992, 55, 78-80.
Clark, P.A.; Cotton, L.N.; Martin, J.H. Selection of bifidobacteria for use as dietary adjuncts in cultured dairy foods: II-Tolerance to simulated pH of human stomachs. Cultured Dairy Prod. J., 1993, 28, 11-14.
Costelloe, M. Probiotic foods In: Foodpro 93: International Food Processing Machinery and Technology Exhibition and Conference, Sydney Convention & Exhibition Centre, Australia July 12-14 1993
Cotter, P.D.; Hill, C. Surviving the acid test: Responses of Gram-positive bacteria to low pH. Microbiol. Mol. Biol. Rev., 2003, 67, 429-453.
Rius, N.; Solé, M.; Francia, A.; Lorén, J-G. Buffering capacity and membrane H+ conductance of lactic acid bacteria. FEMS Microbiol. Lett., 1994, 120, 291-295.
Chen, S.; Zhao, Q.; Ferguson, L.R.; Shu, Q.; Weir, I.; Garg, S. Development of a novel probiotic delivery system based on microencapsulation with protectants. Appl. Microbiol. Biotechnol., 2012, 93, 1447-1457.
Haghshenas, B.; Abdullah, N.; Nami, Y.; Radiah, D.; Rosli, R.; Khosroushahi, A.Y. Microencapsulation of probiotic bacteria Lactobacillus plantarum 15HN using alginate-psyllium-fenugreek polymeric blends. J. Appl. Microbiol., 2015, 118, 1048-1057.
Kailasapathy, K. Microencapsulation of probiotic bacteria: Technology and potential applications. Curr. Issues Intest. Microbiol., 2002, 3, 39-48.
Villena, M.J.M.; Lara Villoslada, F.; Martínez, M.A.R.; Hernández, M.E.M. Development of gastro-resistant tablets for the protection and intestinal delivery of Lactobacillus fermentum CECT 5716. Int. J. Pharm., 2015, 487, 314-319.
Mei, L.; He, F.; Zhou, R-Q.; Wu, C-D.; Liang, R.; Xie, R.; Ju, X-J.; Wang, W.; Chu, L-Y. Novel intestinal-targeted Ca-alginate-based carrier for pH-responsive protection and release of lactic acid bacteria. ACS Appl. Mater. Interfaces, 2014, 6, 5962-5970.
Zhao, Q.; Lee, S.; Mutukumira, A.; Maddox, I.; Shu, Q. Viability and delivery of immobilised Lactobacillus reuteri DPC16 within calcium alginate gel systems during sequential passage through simulated gastrointestinal fluids. Benef. Microbes, 2011, 2, 129-138.
Adams, C.A. The probiotic paradox: Live and dead cells are biological response modifiers. Nutr. Res. Rev., 2010, 23, 37-46.
Sashihara, T.; Sueki, N.; Ikegami, S. An analysis of the effectiveness of heat-killed lactic acid bacteria in alleviating allergic diseases. J. Dairy Sci., 2006, 89, 2846-2855.
Zhang, L.; Li, N.; Caicedo, R.; Neu, J. Alive and dead Lactobacillus rhamnosus GG decrease tumor necrosis factor-alpha-induced interleukin- 8 production in Caco-2 cells. J. Nutr., 2005, 135, 1752-1756.
Taverniti, V.; Guglielmetti, S. The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: Proposal of paraprobiotic concept). Genes Nutr., 2011, 6, 261-274.
Wagner, R.D.; Pierson, C.; Warner, T.; Dohnalek, M.; Hilty, M.; Balish, E. Probiotic effects of feeding heat-killed Lactobacillus acidophilus and Lactobacillus casei to Candida albicans-colonized immunodeficient mice. J. Food Prot., 2000, 63, 638-644.
Fuller, R.; Gibson, G.R. Probiotics and prebiotics: Microflora management for improved gut health. Clin. Microbiol. Infect., 1998, 4, 477-480.
Rolfe, R.D. The role of probiotic cultures in the control of gastrointestinal health. J. Nutr., 2000, 130, 396S-402S.
Jack, R.W.; Tagg, J.R.; Ray, B. Bacteriocins of Gram-positive bacteria. Microbiol. Rev., 1995, 59, 171-200.
Klaenhammer, T.R. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Rev., 1993, 12, 39-85.
Vandenbergh, P.A. Lactic acid bacteria, their metabolic products and interference with microbial growth. FEMS Microbiol. Rev., 1993, 12, 221-237.
Aiba, Y.; Suzuki, N.; Kabir, A.M.A.; Takagi, A.; Koga, Y. Lactic acid-mediated suppression of Helicobacter pylori by the oral administration of Lactobacillus salivarius as a probiotic in a gnotobiotic murine model. Am. J. Gastroenterol., 1998, 93, 2097-2101.
Midolo, P.D.; Lambert, J.R.; Hull, R.; Luo, F.; Grayson, M.L. In vitro inhibition of Helicobacter pylori NCTC 11637 by organic acids and lactic acid bacteria. J. Appl. Bacteriol., 1995, 79, 475-479.
Sgouras, D.; Maragkoudakis, P.; Petraki, K.; Martinez-Gonzalez, B.; Eriotou, E.; Michopoulos, S.; Kalantzopoulos, G.; Tsakalidou, E.; Mentis, A. In vitro and in vivo inhibition of Helicobacter pylori by Lactobacillus casei strain Shirota. Appl. Environ. Microbiol., 2004, 70, 518-526.
Michetti, P.; Dorta, G.; Wiesel, P.H.; Brassart, D.; Verdu, E.; Herranz, M.; Felley, C.; Porta, N.; Rouvet, M.; Blum, A.L.; Corthesy-Theulaz, I. Effect of whey-based culture supernatant of Lactobacillus acidophilus (johnsonii) La1 on Helicobacter pylori infection in humans. Digestion, 1999, 60, 203-209.
Guruge, J.L.; Falk, P.G.; Lorenz, R.G. Dans, M.; Wirth, H-P.; Blaser, M.J.; Berg, D.E.; Gordon, J.I. Epithelial attachment alters the outcome of Helicobacter pylori infection. Proc. Natl. Acad. Sci. USA, 1998, 95, 3925-3930.
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.
Nam, H.; Ha, M.; Bae, O.; Lee, Y. Effect of Weissella confusa strain PL9001 on the adherence and growth of Helicobacter pylori. Appl. Environ. Microbiol., 2002, 68, 4642-4645.
Bernet, M.F.; Brassart, D.; Neeser, J.R.; Servin, A.L. 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.
Byrd, J.C.; Yunker, C.K.; Xu, Q-S.; Sternberg, L.R.; Bresalier, R.S. Inhibition of gastric mucin synthesis by Helicobacter pylori. Gastroenterology, 2000, 118, 1072-1079.
Mack, D.R.; Michail, S.; Wei, S.; McDougall, L.; Hollingsworth, M.A. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am. J. Physiol., 1999, 276, G941-G950.
Mack, D.R.; Ahrne, S.; Hyde, L.; Wei, S.; Hollingsworth, M.A. Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut, 2003, 52, 827-833.
Gotteland, M.; Cruchet, S.; Verbeke, S. Effect of Lactobacillus ingestion on the gastrointestinal mucosal barrier alterations induced by indomethacin in humans. Aliment. Pharmacol. Ther., 2001, 15(1), 11-17.
Arakawa, T.; Watanabe, T.; Kobayashi, K. Regulation of acid secretion and peptic ulcer formation by inflammatory cytokines. In: Ernst, P.B.; Michetti, P.; Smith, P.D., editors The immunology of H. pylori: From pathogenesis to prevention. Philadelphia: Lippincott- Raven Publishers, 1997, pp. 183-199.
Noach, L.A.; Bosma, N.B.; Jansen, J.; Hoek, F.J.; van-Deventer, S.J.H.; Tytgut, G.N.J. Mucosal tumor necrosis factor-or, interleukin-1/3, and interleukin-8 production in patients with Helicobacter pylori infection. Scand. J. Gastroenterol., 1994, 29, 425-429.
Harris, P.R.; Smith, P.D. The role of the mononuclear phagocyte in H. pylori-associated infection. In: The immunology of H. pylori: From pathogenesis to prevention, Ernst PB, Michetti P, Smith PD, editors. Lippincott-Raven Publishers: Philadelphia, 1997, pp. 127- 137.
Gill, H.S. Probiotics to enhance anti-infective defences in the gastrointestinal tract. Best Pract. Res. Clin. Gastroenterol., 2003, 17, 755-773.
Kabir, A.M.; Aiba, Y.; Takagi, A.; Kamiya, S.; Miwa, T.; Koga, Y. Prevention of Helicobacter pylori infection by lactobacilli in a gnotobiotic murine model. Gut, 1997, 41, 49-55.
Vitini, E.; Alvarez, S.; Medina, M.; Medici, M.; de Budeguer, M.V.; Perdigon, G. Gut mucosal immunostimulation by lactic acid bacteria. Biocell, 2000, 24, 223-232.
Haller, D.; Bode, C.; Hammes, W.P.; Pfeifer, A.M.A.; Schiffrin, E.J.; Blum, S. Non-pathogenic bacteria elicit a differential cytokine response by intestinal epithelial cell/leucocyte co-cultures. Gut, 2000, 47, 79-87.
Malfertheiner, P.; Megraud, F.; O’Morain, C.A.; Atherton, J.; Axon, A.T.R.; Bazzoli, F.; Gensini, G.F.; Gisbert, J.P.; Graham, D.Y.; Rokkas, T.; El-Omar, E.M.; Kuipers, E.J. The European Helicobacter Study Group (EHSG). Management of Helicobacter pylori infection - the Maastricht IV/Florence consensus report. Gut, 2012, 61(5), 646-664.
Lu, C.; Sang, J.; He, H.; Wan, X.; Lin, Y.; Li, L.; Li, Y.; Yu, C. Probiotic supplementation does not improve eradication rate of Helicobacter pylori infection compared to placebo based on standard therapy: A meta-analysis. Sci. Rep., 2016, 6, 23522.
Zhang, M-M.; Qian, W.; Qin, Y-Y.; He, J.; Zhou, Y-H. Probiotics in Helicobacter pylori eradication therapy: A systematic review and meta-analysis. World J. Gastroenterol., 2015, 21(14), 4345-4357.
Coconnier, M-H.; Lievin, V.; Hemery, E.; Servin, A.L. Antagonistic activity against Helicobacter infection in vitro and in vivo by the human Lactobacillus acidophilus strain LB. Appl. Environ. Microbiol., 1998, 64, 4573-4580.
Johnson-Henry, K.C.; Mitchell, D.J.; Avitzur, Y.; Galindo-Mata, E.; Jones, N.L.; Sherman, P.M. Probiotics reduce bacterial colonization and gastric inflammation in H. pylori-infected mice. Dig. Dis. Sci., 2004, 49(7-8), 1095-1102.
Sgouras, D.N.; Panayotopoulou, E.G.; Martinez-Gonzalez, B.; Petraki, K.; Michopoulos, S.; Mentis, A. Lactobacillus johnsonii La1 attenuates Helicobacter pylori-associated gastritis and reduces levels of proinflammatory chemokines in C57BL/6 mice. Clin. Diagn. Lab. Immunol., 2005, 12(12), 1378-1386.
Cats, A.; Kuipers, E.J.; Bosschaert, M.A.R.; Pot, R.G.J.; Vandenbroucke-Grauls, C.M.J.E.; Kusters, J.G. Effect of frequent consumption of a Lactobacillus casei-containing milk drink in Helicobacter pylori-colonized subjects. Aliment. Pharmacol. Ther., 2003, 17, 429-435.
Gotteland, M.; Cruchet, S. Suppressive effect of frequent ingestion of Lactobacillus johnsonii La1 on Helicobacter pylori colonization in asymptomatic volunteers. J. Antimicrob. Chemother., 2003, 51(5), 1317-1319.
Linsalata, M.; Russo, F.; Berloco, P.; Caruso, M.L.; Matteo, G.D.I.; Cifone, M.G.; Simone, C.D.E.; Ierardi, E.; Di Leo, A. The influence of Lactobacillus brevis on ornithine decarboxylase activity and polyamine profiles in Helicobacter pylori-infected gastric mucosa. Helicobacter, 2004, 9(2), 165-172.
Lesbros-Pantoflickova, D.; Corthesy-Theulaz, I.; Dorta, G.; Stolte, M.; Isler, P.; Rochat, F.; Enslen, M.; Blum, A.L. Favourable effect of regular intake of fermented milk containing Lactobacillus johnsonii on Helicobacter pylori associated gastritis. Aliment. Pharmacol. Ther., 2003, 18(8), 805-813.
Sakamoto, I.; Igarashi, M.; Kimura, K.; Takagi, A.; Miwa, T.; Koga, Y. Suppressive effect of Lactobacillus gasseri OLL 2716 (LG21) on Helicobacter pylori infection in humans. J. Antimicrob. Chemother., 2001, 47(5), 709-710.
Gotteland, M.; Brunser, O.; Cruchet, S. Systematic review: are probiotics useful in controlling gastric colonization by Helicobacter pylori? Aliment. Pharmacol. Ther., 2006, 23(8), 1077-1086.
Cruchet, S.; Obregon, M.C.; Salazar, G.; Diaz, E.; Gotteland, M. Effect of the ingestion of a dietary product containing Lactobacillus johnsonii La1 on Helicobacter pylori colonization in children. Nutrition, 2003, 19(9), 716-721.
Gotteland, M.; Poliak, L.; Cruchet, S.; Brunser, O. Effect of regular ingestion of Saccharomyces boulardii plus inulin or Lactobacillus acidophilus LB in children colonized by Helicobacter pylori. Acta Paediatr., 2005, 94(12), 1747-1751.
Malfertheiner, P.; Venerito, M.; Schulz, C. Helicobacter pylori infection: New facts in clinical management. Curr. Treat. Options Gastroenterol., 2018, 16(4), 605-615.
Lv, Z.; Wang, B.; Zhou, X.; Wang, F.; Xie, Y.; Zheng, H.; Lv, N. Efficacy and safety of probiotics as adjuvant agents for Helicobacter pylori infection: A meta-analysis. Exp. Ther. Med., 2015, 9(3), 707-716.
Dang, Y.; Reinhardt, J.D.; Zhou, X.; Zhang, G. The effect of probiotics supplementation on Helicobacter pylori eradication rates and side effects during eradication therapy: A meta-analysis. PLoS One, 2014, 9(11), e111030.
McFarland, L.V.; Huang, Y.; Wang, L.; Malfertheiner, P. Systematic review and meta-analysis: Multi-strain probiotics as adjunct therapy for Helicobacter pylori eradication and prevention of adverse events. United European Gastroenterol. J., 2016, 4(4), 546-561.
Szajewska, H.; Shamir, R.; Chmielewska, A.; Pieścik-Lech, M.; Auricchio, R.; Ivarsson, A.; Kolacek, S.; Koletzko, S.; Korponay-Szabo, I.; Mearin, M.L.; Ribes-Koninckx, C.; Troncone, R. Systematic review with meta-analysis: Early infant feeding and coeliac disease-update 2015. Aliment. Pharmacol. Ther., 2015, 41(11), 1038-1054.
McNicholl, A.G.; Molina-Infante, J.; Lucendo, A.J.; Calleja, J.L.; Pérez‐Aisa, A.; Modolell, I.; Aldeguer, X.; Calafat, M.; Comino, L.; Ramas, M.; Callejo, A.; Badiola, C.; Serra, J.; Gisbert, J.P. Probiotic supplementation with Lactobacillus plantarum and Pediococcus acidilactici for Helicobacter pylori therapy: A randomized, double-blind, placebo-controlled trial. Helicobacter, 2018, 23(5), e12529.
Malfertheiner, P.; Megraud, F.; O’Morain, C.A.; Gisbert, J.P.; Kuipers, E.J.; Axon, A.T.; Bazzoli, F.; Gasbarrini, A.; Atherton, J.; Graham, D.Y.; Hunt, R.; Moayyedi, P.; Rokkas, T.; Rugge, M.; Selgrad, M.; Suerbaum, S.; Sugano, K.; El-Omar, E.M. Management of Helicobacter pylori infection-the Maastricht V/Florence consensus report. Gut, 2017, 66(1), 6-30.
Ernst, P.B.; Gold, B.D. The disease spectrum of Helicobacter pylori: The immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu. Rev. Microbiol., 2000, 54, 615-640.
Hammerman, C.; Bin-Nun, A.; Kaplan, M. Safety of probiotics: comparison of two popular strains. BMJ, 2006, 333, 1006-1008.
Boyle, R.J.; Robins-Browne, R.M.; Tang, M.L.K. Probiotic use in clinical practice: What are the risks? Am. J. Clin. Nutr., 2006, 83, 1256-1264.
Saarela, M.; Maukonen, J.; von Wright, A.; Vilpponen-Salmela, T.; Patterson, A.J.; Scott, K.P.; Hämynen, H.; Mättö, J. Tetracycline susceptibility of the ingested Lactobacillus acidophilus LaCH-5 and Bifidobacterium animalis subsp. lactis Bb-12 strains during antibiotic/probiotic intervention. Int. J. Antimicrob. Agents, 2007, 29(3), 271-280.
Kim, T-S.; Hur, J-W.; Yu, M-A.; Cheigh, C-I.; Kim, K-N.; Hwang, J-K.; Pyun, Y-R. Antagonism of Helicobacter pylori by bacteriocins of lactic acid bacteria. J. Food Prot., 2003, 66, 3-12.
Lorca, G.L.; Wadstrom, T.; de Valdez, G.F.; Ljungh, A. Lactobacillus acidophilus autolysins inhibit Helicobacter pylori in vitro. Curr. Microbiol., 2001, 42, 39-44.
Pinchuk, I.V.; Bressollier, P.; Verneuil, B.; Fenet, B.; Sorokulova, I.B.; Megraud, F.; Urdaci, M.C. 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.

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2019
Page: [137 - 145]
Pages: 9
DOI: 10.2174/1389201020666190227203107
Price: $58

Article Metrics

PDF: 19
PRC: 1