Behavior of various strains of Yersinia enterocolitica in Ultra-filtered cheese and inhibitory effect of lactic starter bacteria
Subject Areas :
Food Science and Technology
رضا Vaseghi Bakhshayesh
1
,
شهرام Hanifian
2
1 - M.Sc Graduate in Food Science and Technology, Tabriz Branch, Islamic Azad University, Tabriz, Iran.
2 - Assistant Professor, Department of Food Science and Technology, Tabriz Branch, Islamic Azad University, Tabriz, Iran.
Received: 2015-01-11
Accepted : 2015-07-22
Published : 2015-05-22
Keywords:
Yersinia enterocolitica,
Ultra-filtered cheese,
Starter cultures,
Abstract :
This study aimed to assess the behavior of various strains of Yersinia enterocolitica in ultra-filtered (UF) cheese and to evaluate the inhibitory effect of lactic starter bacteria on survival of Y. enterocolitica. To this end, pasteurized ultra-filtered milk was inoculated with 3 log cfu/g of two standard strains (DSM 11502 and DSM 9499) and one native strain of Y. enterocolitica. UF cheese samples were produced with and without starter culture. Enumeration of Y. enterocolitica was performed at the time of inoculation, after incubation time and during the 2-months storage period on CIN agar. The enumerated colonies were confirmed by PCR. Results revealed that after incubation, the populations of Y. enterocolitica in both groups increased by 4.14 log cfu/g (P < 0.01). However, during the storage period the number of Y. enterocolitica decreased only in the samples made with starter cultures. pH values revealed a significant difference (P < 0.01) between the samples made with and without starter culture; therefore, it seems that acidic pH is the major factor inhibiting the survival of Y. enterocolitica in UF cheese. Besides, a significantly (P < 0.01) different behavior was observed among native and standard strains. Considering the inhibitory effect of starter bacteria,it seems that creation of proper conditions in terms of temperature and the time necessary for proliferation and activity of starter bacteria or application of cultures capable of producing antagonistic products can be effective in controlling possible microbial contaminations along with the development of desirable aroma and texture in UF cheese.
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Minnich, S.A., Smith, M.J., Weagant, S.D. and Feng, P. (2001). Yersinia, In: Hui, Y.H., Pierson, M.D. and Gorham, J.R. (Editors), Foodborne Diseases Handbook. Vol. 1, CRC Press LLC, p. 677.
Mohammadi, K. and Hanifian, S. (2014). Growth and enterotoxin production of Staphylococcus aureus in Iranian ultra-filtered white cheese. International Journal of Dairy Technology, DOI: 10.1111/1471-0307.12158.
Robins-Browne, R.M. and Hartland, E.L. (2003). Yersinia Species, In: Marianne, D.M., and Jeffery, W.B. (Editors), International Handbook of Foodborne Pathogens. Marcel Dekker Inc, p. 858.
Skurnik, M., Radström, P., Knutsson, R., Segerman, B., Hallanvuo, S., Thisted Lambertz, S., et al. (2010). Yersinia. In: Liu, D. (Editor), Molecular Detection of Foodborne Pathogens. CRC Press, New York, pp. 501–513.
Soltan-Dallal, M.M., Tabarraie, A. and MoezArdalan, K. (2004). Comparison of four methods for isolation of Yersinia enterocolitica from raw and pasteurized milk from northern Iran. International Journal of Food Microbiology, 94(1): 87–91.
Thisted Lambertz, S. and Danielsson-Tham, M.L. (2005). Identification and characterization of pathogenic Yersinia enterocolitica isolates by PCR and pulsed-field gel electrophoresis. Applied and Environmental Microbiology, 71(7): 3674–3681.
Zadernowska, A., Wierzchowska, W.C. and Trokenheim, L.L. (2014). Yersinia enterocolitica: A dangerous, but often ignored, foodborne pathogen. Food Reviews International, 30(1): 53–70.
Weagant, S.D. and Feng, P. (2001). Yersinia, In: Pouch Downes, F. and Ito, K. (Editors), Compendium of Methods for the Microbiological Examination of Foods, 3th Edition, American Public Health Association, Washington DC, pp. 421–428.
Weagant, S.D., Feng, P. and Stanfield, J.T. (1998). Yersinia enterocolitica and Yersinia pseudotuberculosis, In: Jackson, G.J., Merker, R.I. and Bandler, R. (Editors), Bacteriological Analytical Manual, 8th Edition, FDA publication, USA, pp. 156–170.
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Ackers, M.K., Schoenfeld, S., Markman, J., Smith, M.G., Nicholson, M.A., DeWitt, W., et al. (2000). An outbreak of Yersinia enterocolitica O:8 infections associated with pasteurized milk. Journal of Infectious Disease, 181(5): 1834–1837.
AOAC. (1995). Official Methods of Analysis, AOAC International. 16th Edition, Vol. 2, Chap: 33, Subchapter 7, Cheese, pp. 58–61.
Aytaç, S.A. and Özbaş, Z.Y. (1992). Isolation of Yersinia enterocolitica from Turkish pickled white cheese. Australian Journal of Dairy Technology, 47(1): 60–62.
Bergholz, T.M., Bowen, B., Wiedmann, M. and Boor, K.J. (2012). Listeria monocytogenes shows temperature-dependent and -independent responses to salt stress, including responses that induce cross-protection against other stresses. Applied and Environmental Microbiology, 78(8): 2602–2612.
Bhaduri, S. and Cottrell, B. (1998). A simplified sample preparation method from various foods for PCR detection of pathogenic Yersinia enterocolitica: a possible model for other food pathogens. Molecular and Cellular Probes, 12(2): 79–83.
Bottone, E.J. (1991). Yersinia enterocolitica: overview and epidemiologic correlates. Microbes and Infection, 1(4): 323–333.
Capozzi, V., Fiocco, D., Amodio, M.L., Gallone, A. and Spano, G. (2009). Bacterial stressors in minimally processed food. International Journal of Molecular Sciences, 10(7): 3076–3105.
Erkmen, O. (1997). Survival of virulent Yersinia enterocolitica during the manufacture and storage of Turkish Feta cheese. International Journal of Food Microbiology, 33(2-3): 285–292.
Gardiner, G., Ross, R.P., Collins, J.K., Fitzgerald, G. and Stanton, C. (1998). Development of a probiotic cheddar cheese containing human-derived Lactobacillus paracasei strains, Applied and Environmental Microbiology, 64: 2192–2199.
Hanifian, S. (2014). Survival of Mycobacterium avium subsp. paratuberculosis in Ultra-filtrated white cheese. Letters in Applied Microbiology, 58(5): 466–471.
Hanifian, S. and Khani, S. (2012a). Prevalence of virulent Yersinia enterocolitica in bulk raw milk and retail cheese in northern-west of Iran. International Journal of Food Microbiology, 155(1-2): 89–92.
Hanifian, S. and Khani, S. (2012b). Fate of Yersinia enterocolitica during manufacture, ripening and storage of Lighvan cheese. International Journal of Food Microbiology, 156(2): 141–146.
Hudson, J., King, N., Cornelius, A., Bigwood, T., Thom, K. and Monson, S. (2008). Detection, isolation and enumeration of Yersinia enterocolitica from raw pork. International Journal of Food Microbiology, 123(1-2): 25–31.
Karami, M., Ehsani, M.R., Mousavi, S.M., Rezaie, K. and Safari, M. (2009). Changes in the rheological properties of Iranian UF-Feta cheese during ripening. Food Chemistry, 112(3): 539–544.
Longenberger, A.H., Gronostaj, M.P., Yee, G.Y., Johnson, L.M., Lando, J.F., Voorhees, R.E., et al. (2014). Yersinia enterocolitica infections associated with improperly pasteurized milk products: southwest Pennsylvania, March-August, 2011. Epidemiology and Infection, 142(8): 1640–50.
Minnich, S.A., Smith, M.J., Weagant, S.D. and Feng, P. (2001). Yersinia, In: Hui, Y.H., Pierson, M.D. and Gorham, J.R. (Editors), Foodborne Diseases Handbook. Vol. 1, CRC Press LLC, p. 677.
Mohammadi, K. and Hanifian, S. (2014). Growth and enterotoxin production of Staphylococcus aureus in Iranian ultra-filtered white cheese. International Journal of Dairy Technology, DOI: 10.1111/1471-0307.12158.
Robins-Browne, R.M. and Hartland, E.L. (2003). Yersinia Species, In: Marianne, D.M., and Jeffery, W.B. (Editors), International Handbook of Foodborne Pathogens. Marcel Dekker Inc, p. 858.
Skurnik, M., Radström, P., Knutsson, R., Segerman, B., Hallanvuo, S., Thisted Lambertz, S., et al. (2010). Yersinia. In: Liu, D. (Editor), Molecular Detection of Foodborne Pathogens. CRC Press, New York, pp. 501–513.
Soltan-Dallal, M.M., Tabarraie, A. and MoezArdalan, K. (2004). Comparison of four methods for isolation of Yersinia enterocolitica from raw and pasteurized milk from northern Iran. International Journal of Food Microbiology, 94(1): 87–91.
Thisted Lambertz, S. and Danielsson-Tham, M.L. (2005). Identification and characterization of pathogenic Yersinia enterocolitica isolates by PCR and pulsed-field gel electrophoresis. Applied and Environmental Microbiology, 71(7): 3674–3681.
Zadernowska, A., Wierzchowska, W.C. and Trokenheim, L.L. (2014). Yersinia enterocolitica: A dangerous, but often ignored, foodborne pathogen. Food Reviews International, 30(1): 53–70.
Weagant, S.D. and Feng, P. (2001). Yersinia, In: Pouch Downes, F. and Ito, K. (Editors), Compendium of Methods for the Microbiological Examination of Foods, 3th Edition, American Public Health Association, Washington DC, pp. 421–428.
Weagant, S.D., Feng, P. and Stanfield, J.T. (1998). Yersinia enterocolitica and Yersinia pseudotuberculosis, In: Jackson, G.J., Merker, R.I. and Bandler, R. (Editors), Bacteriological Analytical Manual, 8th Edition, FDA publication, USA, pp. 156–170.
