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Response Surface Plots for the Behavioral Pattern of Yersinia enterocolitica in Chocolate Milk as Affected by Trans-Cinnamaldehyde, a Spice Essential Oil Constituent

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Abstract

Response surface plots were generated to determine the behavior of a native food isolate of Yersinia enterocolitica CFR 2301 in chocolate milk with added trans-cinnamaldehyde, an active spice essential oil constituent. The minimum inhibitory and bactericidal concentrations (MIC and MBC) for Y. enterocolitica in broth systems were 0.1 and 0.3 µl/ml, respectively, while in chocolate milk, the MBC was 0.9 µl/ml. In chocolate milk devoid of cinnamaldehyde, the culture of Y. enterocolitica CFR 2301 was able to reach risk-causing population levels in 12 h at 30 °C. In the presence of cinnamaldehyde, an inactivation model was generated for the behavior of Y. enterocolitica in chocolate milk, which revealed that, irrespective of initial inoculum levels, the death time (D T ) was primarily influenced by trans-cinnamaldehyde concentrations and incubation temperatures. The death times were found to decrease with higher cinnamaldehyde concentrations and incubation temperatures. Validation of the model revealed the adequacy of predictions derived for this inactivation model and potential application of compatible possibility to develop food formulations with inhibitory principles.

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References

  • Ackers, M., Schoenfeld, S., Markman, J., Smith, M. G., Nicholson, M. A., Dewill, W., et al. (2000). An outbreak of Yersinia enterocolitica O:8 infections associated with pasteurised milk. Journal of Infectious Diseases, 181, 1834–1837.

    Article  CAS  Google Scholar 

  • Amalaradjou, M. A., Hoagland, T. A., & Venkitanarayanan, K. (2009). Inactivation of Enterobacter sakazakii in reconstituted infant formula by trans-cinnamaldehyde. International Journal of Food Microbiology, 129, 146–149.

    Article  CAS  Google Scholar 

  • Avila-Sosa, R., Gastélum-Franco, M.G., Camacho-Dávila, A., Torres-Muñoz, J.V., Nevárez-Moorillón, G.V. (2009). Extracts of Mexican Oregano (Lippia berlandieri Schauer) with antioxidant and antimicrobial activity. Food Bioprocess Technology. doi:10.1007/s11947-008-0085-7.

  • Baranyi, J., & Roberts, T. A. (1994). A dynamic approach to predicting bacterial growth in food. International Journal of Food Microbiology, 23, 277–294.

    Article  CAS  Google Scholar 

  • Bhaduri, S., Turner-Jones, C. O., Buchanan, R. L., & Phillips, J. G. (1994). Response surface model of the effect of pH, sodium chloride and sodium nitrite on the growth of Yersinia enterocolitica at low temperatures. International Journal of Food Microbiology, 23, 333–343.

    Article  CAS  Google Scholar 

  • Bozkurt, H. & Erkmen, O. (2001). Predictive modelling of Yersinia enterocolitica inactivation in Turkish Feta cheese during storage. Journal of Food Engineering, 47, 81–87.

    Article  Google Scholar 

  • Burt, S. (2004). Essential oils: their antibacterial properties and potential applications in foods—A review. International Journal of Food Microbiology, 94, 223–253.

    Article  CAS  Google Scholar 

  • Burt, S. A. & Reinders, R. D. (2003). Antibacterial activity of selected plant essential oils against Escherichia coli O157:H7. Letters in Applied Microbiology, 36, 162–167.

    Article  CAS  Google Scholar 

  • Canillac, N. & Mourey, A. (2001). Antibacterial activity of the essential oil of Picea excelsa on Listeria, Staphylococcus aureus and coliform bacteria. Food Microbiology, 18, 261–268.

    Article  CAS  Google Scholar 

  • Carson, C. F., Hammer, K. A., & Riley, T. V. (1995). Broth microdilution method for determining the susceptibility of Escherichia coli and Staphylococcus aureus to the essential oil of Melaleuca alternifolia (tea tree oil). Microbios, 82, 181–185.

    CAS  Google Scholar 

  • Carson, C. F., Mee, B. J., & Riley, T. V. (2002). Mechanism of action of Melaleuca alternifolia (tea tree) oil on Staphylcoccus aureus determined by time-kill, lysis, leakage and salt tolerance assays and electron microscopy. Antimicrobial Agents and Chemotherapy, 46, 1914–1920.

    Article  CAS  Google Scholar 

  • Cava, R., Nowak, E., Taboada, A., & Marin-Iniesta, F. (2007). Antimicrobial activity of clove and cinnamon essential oils against Listeria monocytogenes in pasteurized milk. Journal of Food Protection, 70, 2757–2763.

    CAS  Google Scholar 

  • Chang, S. T., Chen, P. F., & Chang, S. C. (2001). Antibacterial activity of leaf essential oils and their constituents from Cinnamomum osmophloeum. Journal of Ethnopharmacology, 77, 123–127.

    Article  CAS  Google Scholar 

  • de Souza, E. L., Stamford, T. L. M., Lima, E. O., Trajano, V. N., & Filho, J. M. B. (2005). Antimicrobial effectiveness of spices: an approach for use in food conservation systems. Brazilian Archives of Biology and Technology, 48, 549–558.

    Article  Google Scholar 

  • Donnelly, C. W. (1990). Concerns of microbial pathogens in association with dairy foods. Journal of Dairy Science, 73, 1656–1661.

    Article  CAS  Google Scholar 

  • Dorman, H. J. D. & Deans, S. G. (2000). Antimicrobial agents from plants: antibacterial activity of plant volatile oils. Journal of Applied Microbiology, 88, 308–316.

    Article  CAS  Google Scholar 

  • Drago, L., Mombelli, B., Ciardo, G., De Vecchi, E., & Gismondo, M. R. (1999). Effects of three different fish oil formulations on Helicobacter pylori growth and viability: in vitro study. Journal of Chemotherapy, 11, 207–210.

    CAS  Google Scholar 

  • Geer, G. G., Gill, C. O., & Dilts, B. D. (1995). Predicting the aerobic growth of Yersinia enterocolitica on pork fat and muscle tissues. Food Microbiology, 12, 463–469.

    Article  Google Scholar 

  • Gill, C. O. & Reichel, M. P. (1989). Growth of the cold-tolerant pathogens Yersinia enterocolitica, Aeromonas hydrophila and Listeria monocytogenes on high pH beef packaged under vacuum or carbon dioxide. Food Microbiology, 6, 223–230.

    Article  Google Scholar 

  • Gupta, C., Garg, A. M., Uniyal, R. C., & Kumari, A. (2008). Comparative analysis of the antimicrobial activity of cinnamon extract on some foodborne microbes. African Journal of Microbiology Research, 2, 247–251.

    Google Scholar 

  • Hudson, J. A., Mott, S. J., & Penny, N. (1994). Growth of Listeria monocytogenes, Aeromonas hydrophila and Yersinia enterocolitica on vacuum and saturated carbon dioxide controlled atmosphere packaged sliced roast beef. Journal of Food Protection, 57, 204–208.

    Google Scholar 

  • Jones, J. E., Walker, S. J., Sutherland, J. P., Peck, M. W., & Little, C. L. (1994). Mathematical modelling of the growth, survival and death of Yersinia enterocolitica. International Journal of Food Microbiology, 23, 433–447.

    Article  CAS  Google Scholar 

  • Karatzas, A. K., Kets, E. P. W., Smid, E. J., & Bennik, M. H. J. (2001). The combined action of carvacrol and high hydrostatic pressure on Listeria monocytogenes Scott A. Journal of Applied Microbiology, 90, 463–469.

    Article  CAS  Google Scholar 

  • Kim, H. O., Park, S. W., & Park, H. D. (2004). Inactivation of Escherichia coli O157:H7 by cinnamic aldehyde purified from Cinnamomum cassia shoot. Food Microbiology, 21, 105–110.

    Article  CAS  Google Scholar 

  • Koutsoumanis, K., Lambropoulou, K., & Nychas, G. J. E. (1999). A predictive model for the non-thermal inactivation of Salmonella enteritidis in a food model system supplemented with a natural antimicrobial. International Journal of Food Microbiology, 49, 63–74.

    Article  CAS  Google Scholar 

  • Lopez, P., Sanchez, C., Batlle, R., & Nerin, C. (2005). Solid-and vapour phase antimicrobial activities of six essential oils: susceptibility of selected foodborne bacterial and fungal strains. Journal of Agricultural and Food Chemistry, 53, 6939–6946.

    Article  CAS  Google Scholar 

  • Matan, N., Rimkeeree, H., Mawson, A. J., Chompreeda, P., Haruthaithanasan, V., & Parker, M. (2006). Antimicrobial activity of cinnamon and clove oils under modified atmosphere conditions. International Journal of Food Microbiology, 107, 180–185.

    Article  CAS  Google Scholar 

  • Mendoza-Yepes, M. J., Sanchez-Hidalgo, L. E., Maertens, G., & Marin-Iniesta, F. (1997). Inhibition of Listeria monocytogenes and other bacteria by a plant essential oil (DMC) en Spanish soft cheese. Journal of Food Safety, 17, 47–55.

    Article  CAS  Google Scholar 

  • Oonmetta-Aree, J., Suzuki, T., Gasaluck, P., & Eumkeb, G. (2006). Antimicrobial properties and action of galangal (Alpinia galangal Linn.) on Staphylococcus aureus. Lebensmittel-Wissenschaft und-Technologie, 39, 1214–1220.

    Article  CAS  Google Scholar 

  • Opara, L. U., Al-Ani, M. R., & Al-Shuaibi, Y. S. (2009). Physico-chemical properties, vitamin c content and antimicrobial properties of pomegranate fruit (Punica granatum L.). Food Bioprocess Technology, 2, 315–321.

    Article  CAS  Google Scholar 

  • Pandit, V. A., & Shelef, L. A. (1994). Sensitivity of Listeria monocytogenes to rosemary (Rosmarinus officinalis L.). Food Microbiology, 11, 57–63.

    Article  Google Scholar 

  • Pin, C., Branyi, J., & de Fernando, G. (2000). Predictive model for the growth of Yersinia enterocolitica under modified atmospheres. Journal of Applied Microbiology, 88, 521–530.

    Article  CAS  Google Scholar 

  • Puangpronpitag, D., & Sittiwet, C. (2009). Antimicrobial properties of Cinnamomum verum aqueous extract. Asian Journal of Biological Sciences, 2, 49–53.

    Article  Google Scholar 

  • Raybaudi-Massilia, R. M., Mosqueda-Melgar, J., & Martin-Belloso, O. (2006). Antimicrobial activity of essential oils on Salmonella Enteritidis, Escherichia coli, and Listeria innocua in fruit juices. Journal of Food Protection, 69, 1579–1586.

    CAS  Google Scholar 

  • Shao, Y., & Ramaswamy, H. S. (2009). Clostridium sporogenes ATCC 7955 spore destruction kinetics in milk under high pressure and elevated temperature treatment conditions. Food Bioprocess Technology. doi: 10.1007/s11947-008-0165-8.

  • Shayegani, M., Morse, D., DeForge, I., Root, T., Parsons, L. M., & Maupin, P. S. (1983). Microbiology of a major foodborne outbreak of gastroenteritis caused by Yersinia enterocolitica serogroup O:8. Journal of Clinical Microbiology, 17, 35–40.

    CAS  Google Scholar 

  • Singh, G., Maurya, S., deLampasona, M. P., & Catalan, C. A. N. (2007). A comparison of chemical, antioxidant and antimicrobial studies of cinnamon leaf and bark volatile oils, oleoresins and their constituents. Food and Chemical Toxicology, 45, 1650–1661.

    Article  CAS  Google Scholar 

  • Smith-Palmer, A., Stewart, J., & Fyfe, L. (1998). Antimicrobial properties of plant essential oils and essences against five important foodborne pathogens. Letters in Applied Microbiology, 26, 118–122.

    Article  CAS  Google Scholar 

  • Sofia, P. K., Prasad, R., Vijay, V. K., & Srivastava, A. K. (2007). Evaluation of antibacterial activity of Indian spices against common foodborne pathogens. International Journal of Food Science and Technology, 42, 910–915.

    Article  CAS  Google Scholar 

  • Stonsaovapak, S., Chareonthamawat, P., & Boonyaratanakornkit, M. (2000). Inhibitory effects of selected Thai spices and medicinal plants on Escherichia coli O:157: H7 and Yersinia enterocolitica. The Kasetsart Journal: Natural Sciences, 34, 510–517.

    Google Scholar 

  • Sutherland, J. P., & Baylis, A. J. (1994). Predictive modelling of growth of Yersinia enterocolitica: the effects of temperature, pH and sodium chloride. International Journal of Food Microbiology, 21, 197–215.

    Article  CAS  Google Scholar 

  • Tacket, C. O., Narain, J. P., Sattin, R., Lofgren, J. P., Konigsberg, C., Jr., Rendtroff, R. C., et al. (1984). A multistate outbreak of infections caused by Yersinia enterocolitica transmitted by pasteurized milk. Journal of the American Medical Association, 251, 483–486.

    Article  CAS  Google Scholar 

  • Tiwari, B. K., Valdramidis, V. P., O’Donnell, C. P., Muthukumarappan, K., Bourke, P., & Cullen, P. J. (2009). Application of natural antimicrobials for food preservation. Journal of Agricultural and Food Chemistry, 57, 5987–6000.

    Article  CAS  Google Scholar 

  • Ultee, A., & Smid, E. J. (2001). Influence of carvacrol on growth and toxin production by Bacillus cereus. International Journal of Food Microbiology, 64, 373–378.

    Article  CAS  Google Scholar 

  • Vigil, A. L., Palau, E., & Davidson, P. M. (2005). Methods for activity assay and evaluation of results. In: Antimicrobials in food (3rd edn, p. 666). Boca Raton: CRC

  • Virto, R., Sanz, D., Alvarez, I., & Raso, C. J. (2005). Inactivation kinetics of Yersinia enterocolitica by citric acid and lactic acid at different temperatures. International Journal of Food Microbiology, 103, 251–257.

    Article  CAS  Google Scholar 

  • Vishu Kumar, A. B., Varadaraj, M. C., Gowda, L. R., & Tharanathan, R. N. (2005). Characterization of chito-oligosaccharides prepared with the aid of papain and pronase and their bactericidal action towards Bacillus cereus and Escherichia coli. Biochemical Journal, 391, 167–175.

    Article  Google Scholar 

  • Wang, M., Li, J., Rangarajan, M., Shao, Y., LaVoie, E. J., Huang, T. C., et al. (1998). Antioxidative phenolic compounds from sage (Salvia officinalis). Journal of Agricultural and Food Chemistry, 46, 4869–4873.

    Article  CAS  Google Scholar 

  • Wei, Q. K., Fang, T. J., & Chen, W. C. (2001). Development and validation of growth model for Yersinia enterocolitica in cooked chicken meats packaged under various atmosphere packaging and stored at different temperatures. Journal of Food Protection, 64, 987–993.

    CAS  Google Scholar 

  • Yuste, J., & Fung, D. Y. C. (2003). Evaluation of Salmonella typhimurium, Yersinia enterocolitica and Staphylococcus aureus counts in apple juice with cinnamon, by conventional media and thin agar layer method. Food Microbiology, 20, 365–370.

    Article  Google Scholar 

  • Zakaria, Z., Sreenivasan, S., & Mohamad, M. (2007). Antimicrobial activity of Piper ribesoides root extract against Staphylococcus aureus. Journal of Applied Biological Sciences, 1, 87–90.

    Google Scholar 

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Acknowledgement

The authors are thankful to Dr. V. Prakash, Director, CFTRI, Mysore for providing the facilities and interest in present work. The first author is grateful to Council of Scientific and Industrial Research, New Delhi for awarding Research Fellowship.

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  1. Human Resource Development, Central Food Technological Research Institute (Council of Scientific & Industrial Research), Mysore, 570020, India

    Kattathara H. Divya & Mandyam Chakravarathy Varadaraj

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  1. Kattathara H. Divya
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Correspondence to Mandyam Chakravarathy Varadaraj.

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Divya, K.H., Varadaraj, M.C. Response Surface Plots for the Behavioral Pattern of Yersinia enterocolitica in Chocolate Milk as Affected by Trans-Cinnamaldehyde, a Spice Essential Oil Constituent. Food Bioprocess Technol 5, 498–507 (2012). https://doi.org/10.1007/s11947-009-0297-5

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