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Anti-Helicobacter pylori activity of antimicrobial substances produced by lactic acid bacteria isolated from Baikkimchi

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Abstract

The purpose of the present study was to determine the antagonistic activity of the 13 lactic acid bacteria strains isolated from Baikkimchi made with (Brassica rapa, subspecies pekinensis and chinensis) against Helicobacter pylori ATCC 43504 in vitro. Relatively good growth properties were found for Lactobacillus brevis BK11, Lactobacillus acidophilus BK13, and Leuconostoc mesenteroides BK26 strains with residual numbers of >106 CFU/mL after incubation for 2 h in artificial gastric juice. In co-culturing experiments, Lactobacillus plantarum BK10, L. brevis BK11, L. acidophilus BK13, Pediococcus pentosaceus BK34, Lactobacillus paracasei BK57, Enterococcus faecalis BK61, and Lactococcus lactis BK65 showed significant antimicrobial ability against H. pylori. The cell-free culture supernatants (CFCSs) obtained from L. brevis BK11, L. acidophilus BK13, P. pentosaceus BK34, L. paracasei BK57, and L. lactis BK65 strains producing very high levels of lactic acid dramatically decreased the viability of H. pylori. In addition, the bactericidal activity of L. plantarum BK10, L. brevis BK11, L. acidophilus BK13, L. paracasei BK57, and E. faecalis BK61 strains was significantly correlated with the bacteriocin production. The CFCS and bacteriocin solutions produced from the strains except for E. faecalis BK61 were effective in inhibiting the adhesion of H. pylori to human stomach adenocarcinoma cells and their urease activity.

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References

  • Adamsson I, Edlund C, and Nord CE. (2000) Microbial ecology and treatment of Helicobacter pyloriHelicobacter pylori infections: review. J Chemother 12, 5–16.

    CAS  Google Scholar 

  • Aiba Y, Suzuki N, Kabir AM, Takagi A, and Koga Y. (1998) Lactic acidmediated suppression of Helicobacter pylori of Lactobacillus salivarius as a probiotic in gnotobiotic murine model. Am J Gastroenterol 93, 2097–101.

    Article  CAS  Google Scholar 

  • Andrzejewska E and Szkaradkiewicz A. (2007) Evaluation of the antagonistic effect of Lactobacillus acidophilus on clinical strains of Helicobacter pylori. Med Dosw Mikrobiol 59, 59–64.

    Google Scholar 

  • Bhatia SJ, Kochar N, Abraham P, Nair NG, and Mehta AP. (1989) Lactobacillus acidophilus inhibits growth of Campylobacter pylori in vitro. J Clin Microbiol 27, 2328–30.

    CAS  Google Scholar 

  • Canducci F, Cremonini F, Armuzzi A, Di Caro S, Gabrielli M, Santarelli L, Nista E, Lupascu A, De Martini D, and Gasbarrini A. (2002) Probiotics and Helicobacter pylori eradication. Digest Liver Dis 34, S81–3.

    Article  Google Scholar 

  • Coconnier MH, Lievin V, Bernet-Camard MF, Hudault S, and Servin AL. (1997) Antibacterial effect of the adhering human Lactobacillus acidophilus strain LB. Antimicrob Agents Ch 41, 1046–52.

    CAS  Google Scholar 

  • Coconnier MH, Lievin V, Hemery E, and Servin AL. (1998) Antagonistic activity against Helicobacter infection in vitro and in vivo by the human Lactobacillus acidophilus strain LB. Appl Environ Microbiol 64, 4573–80.

    CAS  Google Scholar 

  • De Bortoli N, Leonardi G, Ciancia E, Merlo A, Bellini M, Costa F, Mumolo MG, and Ricchiuti A. (2007) Helicobacter pylori eradication: a randomized, prospective study of triple therapy versus triple therapy plus lactoferrin and probiotics. Am J Gastroenterol 102, 951–6.

    Article  Google Scholar 

  • De Vuyst L and Leroy F. (2007) Bacteriocins from lactic acid bacteria: production, purification, and food applications. J Mol Microbiol Biotechnol 13, 194–9.

    Article  Google Scholar 

  • Dunn BE, Cohen H, and Blaser MJ. (1997) Helicobacter pylori. Clin Microbiol Rev 10, 720–41.

    CAS  Google Scholar 

  • El-Adawi H, El-Sheekh M, Khalil M, El-Deeb N, and Hussein M. (2013) Lactic acid bacterial extracts as anti-Helicobacter pylori: a molecular approach. Ir J Med Sci 182, 439–52.

    Article  CAS  Google Scholar 

  • Felley C and Michetti P. (2003) Probiotics and Helicobacter pylori. Best Pract Res Cl Ga 17, 785–91.

    Article  CAS  Google Scholar 

  • Gotteland M, Brunser O, and Cruchet S. (2006) Systematic review: are probiotics useful in controlling gastric colonization by Helicobacter pylori? Aliment Pharmacol Ther 23, 1077–86.

    Article  CAS  Google Scholar 

  • Hamilton-Miller JM. (2003) The role of probiotics in the treatment and prevention of Helicobacter pylori infection. Int J Antimicrob Agents 22, 360–6.

    Article  CAS  Google Scholar 

  • Holo H, Nilssen O, and Nes IF. (1991) Lactococcin A, a new bacteriocin from Lactococcus lactis subsp. cremoris: Isolation and characterization of the protein and its gene. J Bacteriol 173, 3879–87.

    CAS  Google Scholar 

  • Jack RW, Tagg JR, and Ray B. (1995) Bacteriocins of gram-positive bacteria. Microbiol Mol Bol Rev 59, 171–200.

    CAS  Google Scholar 

  • Jung JY, Lee SH, and Jeon CO. (2014) Kimchi microflora: history, current status, and perspectives for industrial kimchi production. Appl Microbiol Biotechnol 98, 2385–93.

    Article  CAS  Google Scholar 

  • Kang JH and Lee MS. (2005) In vitro inhibition of Helicobacter pylori by Enterococcus faecium GM-1. Can J Microbiol 51, 629–36.

    Article  CAS  Google Scholar 

  • Kim MN, Kim N, Lee SH, Park YS, Hwang JH, Kim JW, Jeong SH, Lee DH, Kim JS, Jung HC, and Song IS. (2008) The effects of probiotics on PPItriple therapy for Helicobacter pylori eradication. Helicobacter 13, 261–8.

    Article  CAS  Google Scholar 

  • Kim TS, Hur JW, Yu MA, Cheigh CI, Kim KN, Hwang JK, and Pyun YR. (2003) Antagonism of Helicobacter pylori by bacteriocins of lactic acid bacteria. J Food Prot 66, 3–12.

    CAS  Google Scholar 

  • Lee HJ, Yoon HS, Ji YS, Kim HN, Park HJ, Lee JE, Shin HK, and Holzapfel W. (2011) Functional properties of Lactobacillus strains isolated from kimchi. Int J Food Microbiol 145, 155–61.

    Article  CAS  Google Scholar 

  • Lesbros-Pantoflickova D, Corthesy-Theulaz I, and Blum AL. (2007) Helicobacter pylori and probiotics. J Nutr 137, 812S–8S.

    CAS  Google Scholar 

  • Lin WH, Lin CK, Sheu SJ, Hwang CF, Ye WT, Hwang WZ, and 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, M225–30.

    Article  Google Scholar 

  • Lin WH, Wu CR, Fang TJ, Guo JT, Huang SY, Lee MS, and Yang HL. (2011) Anti-Helicobacter pylori activity of fermented milk with lactic acid bacteria. J Sci Food Agric 91, 1424–31.

    Article  CAS  Google Scholar 

  • Lorca GL, Wadstrom T, Valdez GF, and Ljungh A. (2001) Lactobacillus acidophilus autolysins inhibit Helicobacter pylori in vitro. Curr Microbiol 42, 39–44.

    Article  CAS  Google Scholar 

  • Malfertheiner P, Mgraud F, O’Morain C, Bazzoli F, El-Omar E, Graham D, Hunt R, Rokkas T, Vakil N, and Kuipers EJ. (2002) Current concepts in the management of Helicobacter pylori infection. Aliment Pharm Ther 16, 167–80.

    Article  CAS  Google Scholar 

  • Maragkoudakis PA, Zoumpopoulou G, Christos M, Kalantzopoulos G, Pot B, and Tsakalidou E. (2006) Probiotic potential of Lactobacillus strains isolated from dairy products. Int Dairy J 16, 189–99.

    Article  CAS  Google Scholar 

  • Martin NI, Hu H, Moake MM, Churey JJ, Whittal R, Worobo RW, and Vederas JC. (2003) Isolation, structural characterization, and properties of mattacin (polymyxin M), a cyclic peptide antibiotic produced by Paenibacillus kobensis M. J Biol Chem 278, 13124–32.

    Article  CAS  Google Scholar 

  • Matsumoto S, Washizuka Y, Matsumoto Y, Tawara S, Ikeda F, Yokota Y, and Karita M. (1997) Appearance of metronidazole-resistant Helicobacter pylori strain in an infected ICR-mouse model and difference in eradication of metronidazole-resistant and-sensitive strains. Antimicrob ai]Agents Chemother 41, 2602–5.

    CAS  Google Scholar 

  • McGowan CC, Cover TL, and Blaser MJ. (1996) Helicobacter pylori and gastric acid: biological and therapeutic implications. Gastroenterology 110, 926–38.

    Article  CAS  Google Scholar 

  • Medouakh L, Abdeslam AA, and Bensoltane A. (2010) Antagonistic activity of Lactobacillus sp. against Helicobacter pylori. Int J Microbiol Res 1, 80–6.

    Google Scholar 

  • Michetti P, Dorta G, Wiesel PH, Brassart D, Verdu E, Herranz M, Felley C, Porta N, Rouvet M, Blum AL, and Corthésy-Theulaz I. (1990) Effect of whey-based culture supernatant of Lactobacillus acidophilus (johnsonii) La1 on Helicobacter pylori infection in humans. Digestion 60, 203–9.

    Article  Google Scholar 

  • Midolo PD, Lambert JF, Hull R, Luo F, and Grayson ML. (1995) In vitro inhibition of Helicobacter pylori NCTC 11637 by organic acids and lactic acid bacteria. J Appl Bacteriol 79, 475–9.

    Article  CAS  Google Scholar 

  • Motta AS and Brandelli A. (2002) Characterization of an antibacterial peptide produced by Brevibacterium lines. J Appl Microbiol 92, 63–71.

    Article  CAS  Google Scholar 

  • Mukai T, Asasaka T, Sato E, Mori K, Matsumoto M, and Ohori H. (2002) Inhibition of binding of Helicobacter pylori to the glycolipid receptors by probiotic Lactobacillus reuteri. FEMS Immunol Med Mic 32, 105–10.

    Article  CAS  Google Scholar 

  • Murosaki S, Muroyama K, Yamamoto Y, and Yoshikai Y. (2000) Antitumor effect of heat-killed Lactobacillus plantarum L-137 through restoration of impaired interjeukin-12 production in tumor-bearing mice. Cancer Immunol Immun 49, 157–64.

    Article  CAS  Google Scholar 

  • Otero MC and Nader-Macias ME. (2006) Inhibition of Staphylococcus aureus by H2O2-producing Lactobacillus gasseri isolated from the vaginal tract of cattle. Anim Reprod Sci 96, 35–46.

    Article  CAS  Google Scholar 

  • Patel A, Shah N, and Prajapati JB. (2013) Clinical appliance of probiotics in the treatment of Helicobacter pylori infection-A brief review. J Microbiol Immunol Infect 46, 1–9.

    Article  Google Scholar 

  • Piard JC, Muriana PM, Desmaze MJ, and Kiaenhammer TR. (1992) Purification and partial characterization of lacticin 481, a lanthioninecontaining bacteriocin produced by Lactobacillus lactis subsp. lactis CNRZ 481. Appl Environ Microbiol 58, 279–84.

    CAS  Google Scholar 

  • Rhee SJ, Lee JE, and Lee CH. (2011) Importance of lactic acid bacteria in ai]Asian fermented foods. Microb Cell Fact 10, S5–18.

    Article  Google Scholar 

  • Ryan KA, Daly P, Li Y, Hooton C, and O’Toole PW. (2008) Strain-specific inhibition of Helicobacter pylori by Lactobacillus salivarius and other lactobacilli. J Antimicrob Chemoth 61, 831–4.

    Article  CAS  Google Scholar 

  • Sgouras D, Maragkoudakis P, Petraki K, Martine-Gonzalez B, Eriotou E, Michopoulos S, Kalantzopoulos G, Tsakalidou E, and Mentis A. (2004) In vitro and in vivo inhibition of Helicobacter pylori by Lactobacillus casei strains Shirota. Appl Environ Microbiol 70, 518–26.

    Article  CAS  Google Scholar 

  • Sullivan A and Nord CE. (2002) The place of probiotics in human intestinal infections. Int J Antimicrob Ag 20, 313–9.

    Article  CAS  Google Scholar 

  • Tsai CC, Huang LF, Lin CC, and Tsen HY. (2004) Antagonistic activity against Helicobacter pylori infection in vitro by a strain of Enterococcus faecium TM39. Int J Food Microbiol 96, 1–12.

    Article  Google Scholar 

  • Vitor JMB and Vale FF. (2011) Alternative therapies for Helicobacter pylori: probiotics and phytomedicine. FEMS immunol Med Microbiol 63, 153–64.

    Article  CAS  Google Scholar 

  • Yoon YH and Won BR. (2002) Antagonism against Helicobacter pylori and proteolysis of Lactobacillus helveticus CU631 and strain identification. Asian-Aust J Anim Sci 15, 1057–65.

    CAS  Google Scholar 

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  1. Department of Food Science & Nutrition, Tongmyong University, Busan, 608-735, Republic of Korea

    Sung-Mee Lim

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Lim, SM. Anti-Helicobacter pylori activity of antimicrobial substances produced by lactic acid bacteria isolated from Baikkimchi. J Korean Soc Appl Biol Chem 57, 621–630 (2014). https://doi.org/10.1007/s13765-014-4198-6

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