Browse > Article
http://dx.doi.org/10.7845/kjm.2014.4058

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

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)
Publication Information
Korean Journal of Microbiology / v.50, no.4, 2014 , pp. 334-344 More about this Journal
Abstract
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).
Keywords
Helicobacter pylori; antimicrobial activity; lactic acid bacteria; probiotic; yogurt;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Adolfsson, O., Meydani, S.N., and Russell, R.M. 2004. Yogurt and gut function. Am. J. Clin. Nutr. 80, 245-256.   DOI
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.   DOI   ScienceOn
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.   DOI
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI   ScienceOn
12 Dunn, B.E., Cohen, H., Blaser, M.J. 1997. Helicobacter pylori. Clin. Microbiol. Rev. 10, 720-741.
13 Gill, H.S. and Guarner, F. 2004. Probiotics and human health: A clinical perspective. Postgrad. Med. J. 80, 516-526.   DOI   ScienceOn
14 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.   DOI
15 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.   DOI   ScienceOn
16 Fuller, R. 1991. Probiotics in human medicine. Gut 32, 439-442.   DOI   ScienceOn
17 Gilliland, S.E. 1969. Enzymatic determination of residual hydrogen peroxide in milk. J. Dairy Sci. 52, 321-324.   DOI
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.   DOI   ScienceOn
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.   DOI   ScienceOn
21 Jack, R.W., Tagg, J.R., and Ray, B. 1995. Bacteriocins of Gram-positive bacteria. Microbiol. Mol. Biol. Rev. 59, 171-200.
22 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.   DOI
23 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.   DOI
24 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.   DOI
25 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.   DOI
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.   DOI   ScienceOn
27 Mercenier, A., Pavan, S., and Pot, B. 2002. Probiotics as biotherapeutic agents: Present knowledge and future prospects. Curr. Pharm. Design 8, 99-110.   DOI   ScienceOn
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.   DOI   ScienceOn
29 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.   DOI
30 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.   DOI   ScienceOn
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.   DOI   ScienceOn
32 Ouwehand, A.C., Kirjavainen, P.V., Shortt, C., and Salminen, S. 1999. Probiotics: Mechanisms and established effects. Int. Dairy J. 9, 43- 52.   DOI   ScienceOn
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.   DOI   ScienceOn
34 Perri, F., Qasim, A., Marras, L., and O'Morain, C. 2003. Treatment of Helicobacter pylori infection, Helicobacter 8, 53-60.   DOI   ScienceOn
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.   DOI   ScienceOn
38 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.   DOI   ScienceOn
39 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.   DOI
40 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.   DOI
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.   DOI   ScienceOn
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.   DOI   ScienceOn
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.   DOI
45 Sullivan, A. and Nord, C.E. 2002. The place of probiotics in human intestinal infections. Int. J. Antimicrob. Agents 20, 313-319.   DOI   ScienceOn
46 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.   DOI   ScienceOn
47 Siuta-Cruce, P. and Goulet, J. 2001. Improving probiotic survival rates. Food Technol. 55, 38-42.
48 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.   DOI
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.   DOI   ScienceOn
50 Vasiljevic, T. and Shah, N.P. 2008. Probiotics-from Metchnikoff to bioactives. Int. Dairy J. 18, 714-728.   DOI   ScienceOn
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.   DOI   ScienceOn
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 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.   DOI   ScienceOn
54 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.