Evaluation of Salmonella Growth at Low Concentrations of NaNO2 and NaCl in Processed Meat Products Using Probabilistic Model



Gwak, E.;Lee, H.;Lee, S.;Oh, M-H.;Park, B-Y.;Ha, J.;Lee, J.;Kim, S.;Yoon, Y.

  • 투고 : 2015.08.30
  • 심사 : 2015.12.15
  • 발행 : 2016.07.01


This study developed probabilistic models to predict Salmonella growth in processed meat products formulated with varying concentrations of NaCl and $NaNO_2$. A five-strain mixture of Salmonella was inoculated in nutrient broth supplemented with NaCl (0%, 0.25%, 0.5%, 0.75%, 0.5%, 1.0%, 1.25%, and 1.75%) and $NaNO_2$ (0, 15, 30, 45, 60, 75, 90, 105, and 120 ppm). The inoculated samples were then incubated under aerobic and anaerobic conditions at $4^{\circ}C$, $7^{\circ}C$, $10^{\circ}C$, $12^{\circ}C$, and $15^{\circ}C$ for up to 60 days. Growth (assigned the value of 1) or no growth (assigned the value of 0) for each combination was evaluated by turbidity. These growth response data were analyzed with a logistic regression to evaluate the effect of NaCl and $NaNO_2$ on Salmonella growth. The results from the developed model were compared to the observed data obtained from the frankfurters to evaluate the performance of the model. Results from the developed model showed that a single application of $NaNO_2$ at low concentrations did not inhibit Salmonella growth, whereas NaCl significantly (p<0.05) inhibited Salmonella growth at $10^{\circ}C$, $12^{\circ}C$, and $15^{\circ}C$, regardless of the presence of oxygen. At $4^{\circ}C$ and $7^{\circ}C$, Salmonella growth was not observed in either aerobic or anaerobic conditions. When $NaNO_2$ was combined with NaCl, the probability of Salmonella growth decreased. The validation value confirmed that the performance of the developed model was appropriate. This study indicates that the developed probabilistic models should be useful for describing the combinational effect of $NaNO_2$ and NaCl on inhibiting Salmonella growth in processed meat products.


Salmonella;$NaNO_2$;NaCl;Probabilistic Model


  1. Aguilera, J. M. and M. Karel. 1997. Preservation of biological materials under desiccation. Crit. Rev. Food Sci. Nutr. 37:287-309. https://doi.org/10.1080/10408399709527776
  2. Beery, J. T., M. B. Hugdahl, and M. P. Doyle. 1988. Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl. Environ. Microb. 54:2365-2370.
  3. Busani, L., A. Cigliano, E. Taioli, V. Caligiuri, L. Chiavacci, C. Di Bella, A. Battisti, A. Duranti, M. Gianfranceschi, M. C. Nardella, A. Ricci, S. Rolesu, M. Tamba, R. Marabelli, A. Caprioli, and Italian Group of Veterinary Epidemiology (GLEV). 2005. Prevalence of Salmonella enterica and Listeria monocytogenes contamination in foods of animal origin in Italy. J. Food Prot. 8:1556-1775.
  4. Christiansen, L. N., R. W. Johnston, D. A. Kautter, J. W. Howard, and W. J. Aunan. 1973. Effect of nitrite and nitrate on toxin production by Clostridium botulinum and on nitrosamine formation in perishable canned comminuted cured meat. Appl. Environ. Microbiol. 25:357-362.
  5. EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control). 2013. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2011. EFSA J. 11:3129 http://www.efsa.europa.eu/en/efsajournal/doc/3129.pdf Accessed August 1, 2015. https://doi.org/10.2903/j.efsa.2013.3129
  6. Fares, A. 2007. Quantitative risk assessment model of human salmonellosis linked to the consumption of Camembert cheese made from raw milk. AgroPrisTech. https://tel.archives-ouvertes.fr/pastel-00003463/document Acessed August 2, 2015.
  7. Frolich, E. D. 1999. Risk mechanisms in hypertensive heart disease. Hypertension 34:782-789. https://doi.org/10.1161/01.HYP.34.4.782
  8. Gwak, E., M. Oh, B. Park, H. Lee, S. Lee, J, Ha, J. Lee, S. Kim, K-H. Choi, and Y. Yoon. 2015. Probabilistic models to predict Listeria monocytogenes growth at low concentrations of $NaNO_2$ and NaCl in frankfurters. Korean J. Food Sci. An. 35:815-823. https://doi.org/10.5851/kosfa.2015.35.6.815
  9. Izat, A. L., C. D. Driggers, M. Colberg, M. A. Reiber, and M. H. Adams. 1989. Comparison of the DNA probe to culture methods for the detection of Salmonella on poultry carcasses and processing waters. J. Food Prot. 52:564-570. https://doi.org/10.4315/0362-028X-52.8.564
  10. Jantsch, J., D. Chikkaballi, and M. Hensel. 2011. Cellular aspects of immunity to intracellular Salmonella enterica. Immunol. Rev. 240:185-195. https://doi.org/10.1111/j.1600-065X.2010.00981.x
  11. Jira, W. 2004. Chemical reactions of curing and smoking. Fleischwirtschaft 84:235-239.
  12. Jo, H., B. Park, M. Oh, E. Gwak, H. Lee, S. Lee, and Y. Yoon. 2014. Probabilistic models to predict the growth initiation time for Pseudomonas spp. in processed meats formulated with NaCl and $NaNO_2$. Korean J. Food Sci. An. 34:736-741. https://doi.org/10.5851/kosfa.2014.34.6.736
  13. Kim, H-Y., E-S. Lee, J-Y. Jeong, J-H. Choi, Y-S. Choi, D-J. Han, M. A. Lee, S-Y. Kim, and C-J. Kim. 2010. Effect of bamboo salt on the physicochemical properties of meat emulsion systems. Meat Sci. 86:960-965. https://doi.org/10.1016/j.meatsci.2010.08.001
  14. Kostick, D. S. 2010. Salt, U.S. Geological Survey, 2008 Minerals Yearbook. http://minerals.usgs.gov/minerals/pubs/commodity/salt/myb1-2008-salt.pdf Accessed December 23, 2014.
  15. Koutsoumanis, K. P., P. A. Kendall, and J. N. Sofos. 2004. Modeling the boundaries of growth of Salmonella Typhimurium in broth as a function of temperature, water activity, and pH. J. Food Prot. 67:53-59. https://doi.org/10.4315/0362-028X-67.1.53
  16. Lee, S., H. Lee, J. Y. Lee, P. N. Skandamis, B. Y. Park, M. H. Oh, and Y. Yoon. 2013. Mathematical models to predict kinetic behavior and growth probabilities of Listeria monocytogenes on pork skin at constant and dynamic temperatures. J. Food Prot. 76:1868-1872. https://doi.org/10.4315/0362-028X.JFP-13-197
  17. Maekawa, A., T. Ogiu, H. Onodera, K. Furuta, C. Matsuoka, Y. Ohmo, and S. Odashima. 1982. Carcinogenicity studies of sodium nitrite and sodium nitrate in F-344 rats. Food. Chem. Toxicol. 20:25-33. https://doi.org/10.1016/S0278-6915(82)80005-7
  18. Meyer, C., S. Thiel, U. Ullrich, and A. Stolle. 2010. Salmonella in raw meat and by products from pork and beef. J. Food Prot. 73:1780-1784. https://doi.org/10.4315/0362-028X-73.10.1780
  19. Moller, C. O. A. 2012. The Transfer and Growth of Salmonella Modelled during Pork Processing and Applied to a Risk Assessment for the Catering Sector, Ph. D. Thesis. Technical University of Denmark, Lyngby, Denmark.
  20. Munasinghe, D. M. and T. Sakai. 2004. Sodium chloride as a preferred protein extractant for pork lean meat. Meat Sci. 67:697-703. https://doi.org/10.1016/j.meatsci.2004.02.001
  21. Pelroy, G., M. Peterson, R. Paranjpye, J. Almond, and M. Eklund. 1994. Inhinition of Listeria monocytogenes in cold-process (smoked) salmon by sodium nitrite and packaging method. J. Food Prot. 57:114-119. https://doi.org/10.4315/0362-028X-57.2.114
  22. Perry, I. J. and D. G. Beevers. 1992. Salt intake and stroke: A possible direct effect. J. Hum. Hypertens. 6:23-25.
  23. Pin, C., G. Avendano-Perez, E. Cosciani-Cunico, N. Gomez, A. Gounadakic, G-J. Nychas, P. Skandamis, and G. Barker. 2011. Modelling Salmonella concentration throughout the pork supply chain by considering growth and survival in fluctuating conditions of temperature, pH and aw. Int. J. Food Microbiol. 145:S96-S102. https://doi.org/10.1016/j.ijfoodmicro.2010.09.025
  24. Ratkowsky, D. A., T. Ross, T. A. McMeekin, and J. Olley. 1991. Comparison of Arrhenius-type and Belehradek-type models for prediction of bacterial growth in foods. J. Appl. Microbiol. 71:452-459.
  25. Ratkowsky, D. A. and T. Ross. 1995. Modelling the bacterial growth/no growth interface. Lett. Appl. Microbiol. 20:29-33. https://doi.org/10.1111/j.1472-765X.1995.tb00400.x
  26. Schaffner, D. W. and T. P. Labuza. 1997. Predictive microbiology: Where are we, and where are we going? Food Technol. 51:95-99.
  27. University of Nebrask Cooperative Extension. 2005. Salmonella. http://www.foodsafety.unl.edu/pathogens/salmonella.html Accessed August 2, 2015.
  28. Yoon, Y., P. A. Kendall, K. E. Belk, J. A. Scanga, G. C. Smith, and J. N. Sofos. 2009. Modeling the growth/no-growth boundaries of postprocessing Listeria monocytogenes contamination on frankfurters and bologna treated with lactic acid. Appl. Environ. Microbiol. 75:353-358. https://doi.org/10.1128/AEM.00640-08
  29. Voetsch, A. C., T. J. Van Gilder, F. J. Angulo, M. M. Farley, S. Shallow, R. Marcus, R. R. Cieslak, V. C. Deneen, R. V. Tauxe, and Emerging Infections Program FoodNet Working Group. 2004. FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin. Infect. Dis. 38:S127-S134. https://doi.org/10.1086/381578


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