Anti-Helicobacter pylori Activity of Yogurt Fermented with Lactic Acid Bacteria from Baikkimchi

백김치 유래 유산균을 이용한 요구르트의 Anti-Helicobacter pylori 활성

  • Lim, Sung-Mee (Department of Food Science and Nutrition, Tongmyong University) ;
  • Kim, Duck-Sool (Department of Bio-medical Engineering, Tongmyong University) ;
  • Ahn, Dong-Hyun (Department of Food Science and Technology, Pukyong National University)
  • 임성미 (동명대학교 식품영양학과) ;
  • 김덕술 (동명대학교 의용공학과) ;
  • 안동현 (부경대학교 식품공학과)
  • Received : 2014.09.03
  • Accepted : 2014.10.07
  • Published : 2014.12.31


The objective of this study was to evaluate the microbiological and physicochemical characteristics, and the antagonistic activity against Helicobacter pylori ATCC 43504, of yogurt fermented with the lactic acid bacteria from Baikkimchi kept under cold storage. The viable cell counts, titratable acidity, viscosity, and total solid content of the yogurt were different according to the bacterial strains used for fermentation. There was no significant change (P>0.05) in the various properties of refrigerated yogurt. Among the tested strains, the strongest resistance against artificial gastric juice and bile salt was found for Lactobacillus brevis BK11 and Lactobacillus paracasei BK57. Due to high lactic acid levels obtained from these two lactic acid bacteria, yogurt may show good anti-Helicobacter effects according to the time-kill assay. In particular, yogurt fermented with L. brevis BK11 significantly reduced the number of H. pylori adhering to gastric epithelial AGS cells and the urease activity of this pathogen (P<0.05).


Helicobacter pylori;antimicrobial activity;lactic acid bacteria;probiotic;yogurt


  1. Adolfsson, O., Meydani, S.N., and Russell, R.M. 2004. Yogurt and gut function. Am. J. Clin. Nutr. 80, 245-256.
  2. Aiba, Y., Suzuki, N., Kabir, A.M., Takagi, A., and Koga, Y. 1998. 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. 93, 2097-2101.
  3. Aslim, B., Onbasili, D., and Yuksekdag, Z.N. 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.
  4. Begley, M., Gahan, C.G., and Hill, C. 2005. The interaction between bacteria and bile. FEMS Microbiol. Rev. 4, 625-651.
  5. Boyanova, L., Stephanova-Kondratenko, M., and Mitov, I. 2009. Anti-Helicobacter pylori activity of Lactobacillus delbrueckii subsp. bulgaricus strains: Preliminary report. Lett. Appl. Microbiol. 48, 579-584.
  6. Byrd, J.C., Yunker, C.K., Xu, Q.S., Sternberg, L.R., and Bresalier, R.S. 2000. Inhibition of gastric mucin synthesis by Helicobacter pylori. Gastroenterology 118, 1072-1079.
  7. Cats, A., Kuipers, E.J., Bosschaert, A.R., Pot, R.G.J., Vandenbroucke- Grauls, M.J.E., and Kusters, J.G. 2003. Effect of frequent consumption of a Lactobacillus casei-containing milk drink in Helicobacter pylori-colonized subjects. Aliment. Pharm. Therap. 17, 429-435.
  8. Coconnier, M.H., Lievin, V., Hemery, E., and Servin, A.L. 1998. Antagonistic activity against Helicobacter infection in vitro and in vivo by the human Lactobacillus acidophilus strain LB. Appl. Environ. Microbiol. 64, 4573-4580.
  9. Condon, S. 1987. Responses of lactic acid bacteria to oxygen. FEMS Microbiol. Lett. 46, 269-280.
  10. Corcoran, B.M., Santon, C., Fitzgerald, G.F., and Ross, R.P. 2005. Survival of probiotic Lactobacilli in acidic environments if enhanced in the presence of metabolizable sugars. Appl. Environ. Microbiol. 71, 3060-3067.
  11. Dave, R.I. and Shah, N.P. 1997. Viability of yoghurt and probiotic bacteria in yoghurts made from commercial starter cultures. Int. Dairy J. 7, 31-41.
  12. Dunn, B.E., Cohen, H., Blaser, M.J. 1997. Helicobacter pylori. Clin. Microbiol. Rev. 10, 720-741.
  13. 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, 439-452.
  14. Felley, C.P., Corthesy-Theulaz, I., Rivero, J.L., Sipponen, P., Kaufmann, M., Bauerfeind, P., Wiesel, P.H., Brassart, D., Pfeifer, A., Blum, A.L., and et al. 2001. Favorable effect of an acidified milk (LC-1) on Helicobacter pylori gastritis in man. Eur. J. Gastroen. Hepat. 13, 25-29.
  15. Fuller, R. 1991. Probiotics in human medicine. Gut 32, 439-442.
  16. Gill, H.S. and Guarner, F. 2004. Probiotics and human health: A clinical perspective. Postgrad. Med. J. 80, 516-526.
  17. Gilliland, S.E. 1969. Enzymatic determination of residual hydrogen peroxide in milk. J. Dairy Sci. 52, 321-324.
  18. Guetarni, H., Bensaid, A., and Bensoltane, A. 2012. Analysis of lactic acid responsible for inhibition in vitro of Helicobacter pylori by high performance chromatography (HPLC). J. Biotechnol. Lett. 3, 34-36.
  19. Guo, Z., Wang, J., Yan, L., Chen, W., Liu, X.M., and Zhang, H.P. 2009. In vitro comparison of probiotic properties of Lactobacillus casei Zhang, a potential new probiotic, with selected probiotic strains. LWT-Food Sci. Technol. 42, 1640-1646.
  20. Huang, Y. and Adams, M.C. 2004. In vitro assessment of the upper gastrointestinal tolerance of potential probiotic dairy propionibacteria. Int. J. Food Microbiol. 91, 253-260.
  21. Jack, R.W., Tagg, J.R., and Ray, B. 1995. Bacteriocins of Gram-positive bacteria. Microbiol. Mol. Biol. Rev. 59, 171-200.
  22. Kim, T.S., Hur, J.W., Yu, M.A., Cheigh, C.I., Kim, K.N., Hwang, J.K., and Pyun, Y.R. 2003. Antagonism of Helicobacter pylori by bacteriocins of lactic acid bacteria. J. Food Prot. 66, 3-12.
  23. Lee, N.K., Kim, S.Y., Han, K.J., Eom, S.J., and Paik, H.D. 2014. Probiotic potential of Lactobacillus strains with anti-allergic effects from kimchi for yogurt starters. LWT-Food Sci. Technol. 58, 130-134.
  24. Lim, S.M. 2014. Anti-Helicobacter pylori activity of antimicrobial substances produced by lactic acid bacteria isolated from Baikkimchi. J. Kor. Soc. Appl. Biol. Chem. 57, 621-630.
  25. Lin, W.H., Lin, C.K., Sheu, S.J., Hwang, C.F., Ye, W.T., Hwang, W.Z., and Tsen, H.Y. 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.
  26. Lorca, G.L., Wadstrom, T., Valdez, G.F., and Ljungh, A. 2001. Lactobacillus acidophilus autolysins inhibit Helicobacter pylori in vitro. Curr. Microbiol. 42, 39-44.
  27. Mercenier, A., Pavan, S., and Pot, B. 2002. Probiotics as biotherapeutic agents: Present knowledge and future prospects. Curr. Pharm. Design 8, 99-110.
  28. Michetti. P., Dorta, G., Wiesel, P.H., Brassart, D., Verdu, E., Herranz, M., Felley, C., Porta, N., Rouvet, M., and Blum, A.L. Corthesy-Theulaz I. 1999. Effect of whey-based culture supernatant of Lactobacillus acidophilus (johnsonii) La1 on Helicobacter pylori infection in humans. Digestion 60, 203-209.
  29. Midolo, P.D., Lambert, J.R., Hull, R., Luo, F., and Grayson, M.L. 1995. In vitro inhibition of Helicobacter pylori NCTC 11637 by organic acid and lactic acid bacteria. J. Appl. Bacteriol. 79, 475-479.
  30. 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. Microbiol. 32, 105-110.
  31. Nam, H.H.M., Bae, O., and Lee, Y. 2002. Effect of Weissella confuse strain PL9001 on the adherence and growth of Helicobacter pylori. Appl. Environ. Microbiol. 68, 4642-4645.
  32. Ouwehand, A.C., Kirjavainen, P.V., Shortt, C., and Salminen, S. 1999. Probiotics: Mechanisms and established effects. Int. Dairy J. 9, 43- 52.
  33. Parvez, S., Malik, K.A., Ah, K.S., and Kim, H.Y. 2006. Probiotics and their fermented food products are beneficial for health. J. Appl. Microbiol. 100, 1171-1185.
  34. Perri, F., Qasim, A., Marras, L., and O'Morain, C. 2003. Treatment of Helicobacter pylori infection, Helicobacter 8, 53-60.
  35. Petschow, B.W. and Talbott, R.D. 1990. Growth promotion of Bifidobacterium species by whey and casein fractions from human and bovine milk. J. Clin. Microbiol. 28, 287-292.
  36. Prasanthi, C.H., Prasanthi, N.L., Manikiran, S.S., and Rao, N.R. 2011. Focus on current trends in the treatment of Helicobacter pylori infection: An update. Int. J. Pharm. Sci. Rev. Res. 9, 42-51.
  37. Ross, R.P., Morgan, S., and Hill, C. 2002. Preservation and fermentation: past, present and future. Int. J. Food Microbiol. 79, 3-16.
  38. Salvador, A. and Fiszman, S.M. 2004. Textural and sensory characteristics of whole and skimmed flavored set-type yogurt during long storage. J. Dairy Sci. 87, 4033-4041.
  39. Saxelin, M., Lassig, A., Karjalainen, H., Tynkkynen, S., Surakka, A., Vapaatalo, H., Jarvenpaa, S., Korpela, R., Mutanen, M., and Hatakka, K. 2010. Persistence of probiotic strains in the gastrointestinal tract when administered as capsules, yoghurt, or cheese. Int. J. Food Microbiol. 144, 293-300.
  40. Schillinger, U., Guigas, C., and Holzapfel, W.H. 2005. In vitro adherence and other properties of lactobacilli used in probiotic yoghurt-like products. Int. Dairy J. 15, 1289-1297.
  41. Serrazanetti, D.I., Guerzoni, M.E., Corsetti, A., and Vogel, R. 2009. Metabolic impact and potential exploitation of the stress reactions in lactobacilli. Food Microbiol. 26, 700-711.
  42. Sgouras, D.N., Panayotopoulou, E.G., Martinez-Gonzalez, B., Petraki, K., Michopoulos, S., and Mentis, A. 2005. Lactobacillus johnsonii La1 attenuates Helicobacter pylori-associated gastritis and reduced levels of pro-inflammatory chemokines in C57BL/6 mice. Clin. Diag. Lab. Immun. 12, 1378-1386.
  43. Shah, N.P. 2000. Probiotic bacteria: Selective enumeration and survival in dairy foods. J. Dairy Sci. 83, 894-907.
  44. Shah, N.P. and Ravula, R.R. 2002. Influence of water activity on fermentation, organic acids production and viability of yoghurt and probiotic bacteria. Aust. J. Dairy Technol. 55, 127-131.
  45. Sheu, B.S., Wu, J.J., and Lo, C.Y. 2002. Impact of supplement with Lactobacillus- and Bifidobacterium-containing yogurt on triple therapy for Helicobacter pylori eradication. Aliment. Pharm. Therap. 16, 1669-1675.
  46. Siuta-Cruce, P. and Goulet, J. 2001. Improving probiotic survival rates. Food Technol. 55, 38-42.
  47. Stuart-Tilley, A., Sardet, C., Pouyssegur, J., Schwartz, M.A., Brown, D., and Alpher, S.L. 1994. Immunolocalization of anion exchanger AE2 and cation exchanger NHE-1 in distinct adjacent cells of gastric mucosa. Am. J. Physiol. 266, C559-C568.
  48. Sullivan, A. and Nord, C.E. 2002. The place of probiotics in human intestinal infections. Int. J. Antimicrob. Agents 20, 313-319.
  49. Tsai, C.C., Huang, L.F., Lin, C.C., and Tsen, H.Y. 2004. Antagonistic activity against Helicobacter pylori infection in vitro by a strain of Enterococcus faecium TM39. Int. J. Food Microbiol. 96, 1-12.
  50. Vasiljevic, T. and Shah, N.P. 2008. Probiotics-from Metchnikoff to bioactives. Int. Dairy J. 18, 714-728.
  51. Vinderola, C.G. and Reinheimer, J.A. 2003. Lactic acid starter and probiotic bacteria: a comparative "in vitro" study of probiotic characteristics and biological barrier resistance. Food Res. Int. 36, 895-904.
  52. Vitini, E., Alvarez, S., Medina M., Medici, M., de Budeguer, M.V., and Perdigon, G. 2000. Gut mucosal immunostimulation by lactic acid bacteria. Biocell. 24, 223-232.
  53. Wang, K.Y., Li, S.N., Liu, C.S., Perng, D.S., Su, Y.C., Wu, D.C., Jan, C.M., Lai, C.H., Wang, T.N., and Wang, W.M. 2004. Effects of ingesting Lactobacillus- and Bifidobacterium-containing yogurt in subjects with colonized Helicobacter pylori. Am. J. Clin. Nutr. 80, 737-741.
  54. Watanabe, T., Tada, M., Nagi, H., Sasaki, S., and Nakao, M. 1998. Helicobacter pylori infection induces gastric cancer in Mongolian gerbils. Gastroenterology 115, 642-648.