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Antimicrobial Activity of Kefir against Various Food Pathogens and Spoilage Bacteria

  • Kim, Dong-Hyeon (Center for One Health, College of Veterinary Medicine, Konkuk University) ;
  • Jeong, Dana (Center for One Health, College of Veterinary Medicine, Konkuk University) ;
  • Kim, Hyunsook (Department of Food & Nutrition, College of Human Ecology, Hanyang University) ;
  • Kang, Il-Byeong (Center for One Health, College of Veterinary Medicine, Konkuk University) ;
  • Chon, Jung-Whan (Division of Microbiology, National Center for Toxicological Research, US Food and Drug Administration) ;
  • Song, Kwang-Young (Center for One Health, College of Veterinary Medicine, Konkuk University) ;
  • Seo, Kun-Ho (Center for One Health, College of Veterinary Medicine, Konkuk University)
  • Received : 2016.09.06
  • Accepted : 2016.11.25
  • Published : 2016.12.31

Abstract

Kefir is a unique fermented dairy product produced by a mixture of lactic acid bacteria, acetic acid bacteria, and yeast. Here, we compared the antimicrobial spectra of four types of kefirs (A, L, M, and S) fermented for 24, 36, 48, or 72 h against eight food-borne pathogens. Bacillus cereus, Staphylococcus aureus, Listeria monocytogenes, Enterococcus faecalis, Escherichia coli, Salmonella Enteritidis, Pseudomonas aeruginosa, and Cronobacter sakazakii were used as test strains, and antibacterial activity was investigated by the spot on lawn method. The spectra, potencies, and onsets of activity varied according to the type of kefir and the fermentation time. The broadest and strongest antimicrobial spectrum was obtained after at least 36-48 h of fermentation for all kefirs, although the traditional fermentation method of kefir is for 18-24 h at $25^{\circ}C$. For kefir A, B. cereus, E. coli, S. Enteritidis, P. aeruginosa, and C. sakazakii were inhibited, while B. cereus, S. aureus, E. coli, S. Enteritidis, P. aeruginosa, and C. sakazakii were inhibited to different extents by kefirs L, M, and S. Remarkably, S. aureus, S. Enteritidis, and C. sakazakii were only inhibited by kefirs L, M, and S, and L. monocytogenes by kefir M after fermentation for specific times, suggesting that the antimicrobial activity is attributable not only to a low pH but also to antimicrobial substances secreted during the fermentation.

Keywords

References

  1. Anderson, J. W. and Gilliland, S. E. (1999) Effect of fermented milk (yogurt) containing Lactobacillus acidophilus L1 on serum cholesterol in hypercholesterolemic humans. J. Am. Coll. Nutr. 18, 43-50. https://doi.org/10.1080/07315724.1999.10718826
  2. Beshkova, D., Simova, E. D., Simov, Z. I., Frengova, G. I., and Spasov, Z. N. (2002) Pure cultures for making kefir. Food Microbiol. 19, 537-544. https://doi.org/10.1006/fmic.2002.0499
  3. Cadirci, B. H. and Citak, S. (2005) A comparison of two methods used for measuring antagonistic activity of lactic acid bacteria. Pak. J. Nutr. 4, 237-241. https://doi.org/10.3923/pjn.2005.237.241
  4. Cevikbas, A., Yemni, E., Ezzedenn, F. W., Yardimici, T., Cevikbas, U., and Stohs, S. J. (1994) Antitumoural antibacterial and antifungal activities of kefir and kefir grain. Phytother. Res. 8, 78-82. https://doi.org/10.1002/ptr.2650080205
  5. Chifiriuc, M. C., Cioaca, A. B., and Lazar, V. (2011) In vitro assay of the antimicrobial activity of kephir against bacterial and fungal strains. Anaerobe 17, 433-435. https://doi.org/10.1016/j.anaerobe.2011.04.020
  6. Farnworth, E. R. and Mainville, I. (2008) Kefir - a fermented milk product. In: Handbook of fermented functional foods. 2nd ed. Farnworth, E. R. (ed) CRC Press Taylor & Francis Group, Boca Raton, London, New York, pp. 89-127.
  7. Garrote, G. L., Abraham, A. G., and De Antoni, G. L. (2000) Inhibitory power of kefir: The role of organics acids. J. Food Prot. 63, 364-369. https://doi.org/10.4315/0362-028X-63.3.364
  8. Gaware, V., Kotade, K., Dolas, R., and Dhamak, K. (2011) The magic of kefir: A review. Pharmacol. Online 1, 376-386.
  9. Guzel-Seydim, Z., Kok-Tas, T., and Greene, A. K. (2011) Review: Functional properties of kefir. Crit. Rev. Food. Sci. Nutr. 51, 261-268. https://doi.org/10.1080/10408390903579029
  10. Harris, L. J., Daeschel M. A., Stiles, M. E., and Klaenhammer, T. R. (1989) Antimicrobial activity of lactic acid bacteria against Listeria monocytogenes. J. Food Prot. 52, 384-387. https://doi.org/10.4315/0362-028X-52.6.384
  11. Joshi, V. K., Sharma, S., and Rana, N. S. (2006) Production, purification, stability and efficacy of bacteriocin from isolates of natural lactic acid fermentation of vegetables. Food Technol. Biotechnol. 44, 435-439.
  12. Kim, D. H., Chon, J. W., Kang, I. B., Kim, H., Kim, H. S., Song, K. Y., and Seo, K. H. (2015) Growth inhibition of Cronobacter sakazakii in experimentally contaminated powdered infant formula by kefir supernatant. J. Food Prot. 78, 1651-1655. https://doi.org/10.4315/0362-028X.JFP-15-119
  13. Meydani, S. N. and Ha, W. K. (2000) Immunologic effects of yogurt. Am. J. Clin. Nutr. 71, 861-872. https://doi.org/10.1093/ajcn/71.4.861
  14. Moraes, P. M., Perin, L. M., Ortolani, M. B., Yamazi, A. K., Vicosa, G. N., and Nero, L. A. (2010) Protocols for the isolation and detection of lactic acid bacteria with bacteriocinogenic potential. LWT-Food Sci. Technol. 43, 1320-1324. https://doi.org/10.1016/j.lwt.2010.05.005
  15. Otles, S. and Cagindi, O. (2003) Kefir: A probiotic dairy-composition, nutritional and therapeutic aspects. Pak. J. Nutr. 2, 54-59. https://doi.org/10.3923/pjn.2003.54.59
  16. Pintado, M. E., Lopes Da Silva, J. A., Fernandes, P. B., Malcata, F. X., and Hogg, T. A. (1996) Microbiological and rheological studies on Portuguese kefir grains. Int. J. Food Sci. Technol. 31, 15-26. https://doi.org/10.1111/j.1365-2621.1996.16-316.x
  17. Rodrigues, K. L., Carvalho, J. C., and Schneedorf, J. M. (2005) Anti-inflammatory properties of kefir and its polysaccharide extract. Inflammopharmacology 13, 485-492. https://doi.org/10.1163/156856005774649395
  18. Saloff-Coaste, C. (1996) Kefir. Danonne. Newslett. 11, 1-11.
  19. Santos, A., San Mauro, M., Sanchez, A., Torres, J. M., and Marquina D. (2003) The antimicrobial properties of different strains of Lactobacillus spp. isolated from kefir. System. Appl. Microbiol. 26, 434-437. https://doi.org/10.1078/072320203322497464
  20. Silva, K. R., Rodrigues, S. A., Filho, L. X., and Lima, A. S. (2009) Antimicrobial activity of broth fermented with kefir grains. Appl. Biochem. Biotechnol. 152, 316-325. https://doi.org/10.1007/s12010-008-8303-3
  21. Ulusoy, B. H., Olak, H. C., Hampikyan, H., and Erkan, M. (2007) An in vitro study on the antibacterial effect of kefir against some food-borne pathogens. Türk Mikrobiyol. Cem. Derg. 37, 103-107.
  22. Vinderola, C. G., Duart, J., Thangavel, D., Perdigon, G., Farnworth, E., and Matar, C. (2005) Distal mucosal site stimulation by kefir and duration of the immune response. Eur. J. Inflamm. 3, 63-73. https://doi.org/10.1177/1721727X0500300203
  23. Wheeler, J. G., Shema, S. J., Bogle, M. L., Shirrell, M. A., Burks, A. W., Pittler, A., and Helm, R. M. (1997) Immune and clinical impact of Lactobacillus acidophilus on asthma. Ann. Allergy Asthma Immunol. 79, 229-233. https://doi.org/10.1016/S1081-1206(10)63007-4
  24. Witthuhn, R. C., Schoeman, T., and Britz, T. J. (2005) Characterisation of the microbial population at different stages of Kefir production and Kefir grain mass cultivation. Int. Dairy J. 15, 383-389. https://doi.org/10.1016/j.idairyj.2004.07.016
  25. Zacconi, C., Scolari, G., Vescovo, M., and Sarra, P. G. (2003) Competitive exclusion of Campylobacter jejuni by kefir fermented milk. Ann. Microbiol. 53, 179-187.

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