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Antimicrobial Activity of Vanillin and Mixtures with Cinnamon and Clove Essential Oils in Controlling Listeria monocytogenes and Escherichia coli O157:H7 in Milk

Food and Bioprocess Technology volume 5, pages 2120–2131 (2012)Cite this article

Abstract

The minimal inhibitory concentration (MIC) and minimal bactericidal concentration (MBC) of vanillin against Listeria monocytogenes Scott A and Escherichia coli O157:H7 was determined in tripticase soy broth (TSB), pH 7 and 6, incubated at 35 °C/24 h and in semi-skim milk incubated at 35 °C/24 h and 7 °C/14 days. The influence of the fat content of milk on the antimicrobial activity of vanillin was tested in whole and skim milk incubated at 7 °C/14 days. Mixtures of clove and cinnamon with vanillin were also evaluated in semi skim milk incubated at 7 °C. The MICs for L. monocytogenes were 3,000 ppm in TSB (pH 7) and 2,800 ppm in TSB (pH 6). The MICs for E. coli O157:H7 were 2,800 ppm in TSB (pH 7) and 2,400 ppm in TSB (pH 6). The MBCs in TSB were 8,000 ppm for L. monocytogenes and 6,000 ppm for E. coli O157:H7. The pH values assayed did not influence significantly the MIC or MBC in TSB. The MICs in semi-skim milk for L. monocytogenes and E. coli O157:H7 were 4,000 and 3,000 ppm at 35 °C/24 h, and 2,500 and 1,000 ppm at 7 °C/7 days, respectively. The MBCs were 20,000 ppm for L. monocytogenes and 11,000 ppm for E. coli O157:H7. High incubation temperatures did not affect the MBC but increased the MIC of the vanillin in milk. This effect could be attributed to the increased membrane fluidity and to the membrane perturbing activity of vanillin at low temperatures. The fat in milk reduced significantly the antimicrobial activity of vanillin, probably due to effect protective of the fat molecules. Mixtures of clove and cinnamon leaves inhibited the growth of L. monocytogenes in a similar way that vanillin alone but had a synergistic effect on the E. coli O157:H7. Mixtures of cinnamon bark and vanillin had always a synergistic effect and some of the combination assayed showed bactericidal activity on the population of L. monocytogenes and E. coli O 157:H7.

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References

  • Ahrabi, S. S., Erguven, S., & Gunalp, A. (1998). Detection of Listeria in raw milk and pasteurised milk. Center of European Journal Public Health, 6(3), 254–255.

    CAS  Google Scholar 

  • Allavi, S. H., Puri, V. M., Knabel, S. J., Mohtar, R. H., & Whiting, R. C. (2001). Development and validation of a dynamic growth model for Listeria monocytogenes in fluid whole milk. Journal of Food Protection, 62(2), 170–176.

    Google Scholar 

  • Anklam, E., Gaglione, S., & Muller, A. (1997). Oxidation behaviour of vanillin in dairy products. Food Chemistry, 60(1), 43–51.

    Article  CAS  Google Scholar 

  • Burri, J., Graf, M., Lambelet, P., & Lo Liger, J. (1989). Vanillin: More than a flavouring agent a potent antioxidant. Journal of the Science of Food and Agriculture, 48(1), 49–56.

    Article  CAS  Google Scholar 

  • Burt, S. (2004). Essential oils: Their antibacterial properties and potential applications in foods—a review. International Journal of Food Microbiology, 94(3), 223–253.

    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(12), 2757–2763.

    CAS  Google Scholar 

  • Center for Disease Control and Prevention (CDC) (2007). Escherichia coli O157:H7 Infection Associated with Drinking Raw Milk-Washington and Oregon, November–December 2005. Morbidity and Mortality Weekly Report, 56,165–167. Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5608a3.htm. Accessed 11 Nov 2010.

  • Centers for Disease Control and Prevention (CDC) (2008). Outbreak of Listeria monocytogenes. Infections associated with pasteurized milk from a local dairy massachusetts 2007 October 10. Morbidity and Mortality Weekly Report, 57, 1097–1100 Available at http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5740a1.htm Accessed 11 Nov 2010.

  • Chobpattana, W., Jeon, I. J., Smith, J. S., & Loughin, T. M. (2002). Mechanisms of interaction between vanillin and milk proteins in model systems. Journal of Food Science, 67(3), 973–977.

    Article  CAS  Google Scholar 

  • Cerruti, P., & Alzamora, S. M. (1996). Inhibitory effects of vanillin on some food spoilage yeasts in laboratory media and fruit purées. International Journal of Food Microbiology, 29(2–3), 379–386.

    Article  Google Scholar 

  • Cerruti, P., Alzamora, S. M., & Vidales, S. L. (1997). Vanillin as an antimicrobial for producing shelf-stable strawberry purée. Journal of Food Science, 62(3), 608–661.

    Article  Google Scholar 

  • Chao, S. C., Young, G. D., & Oberg, C. J. (2000). Screening of inhibitory activity of essential oils on selected bacteria, fungi, and viruses. Journal of Essential Oil Research, 12(5), 639–649.

    Article  CAS  Google Scholar 

  • Char, C. D., Guerrero, S. N., & Alzamora, S. M. (2009). Survival of Listeria innocua in thermally processed orange juice as affected by vanillin addition. Food Control, 20(1), 67–74.

    Article  CAS  Google Scholar 

  • Char, C. D., Guerrero, S. N., & Alzamora, S. M. (2010). Mild thermal process combined with vanillin plus citral to help shorten the inactivation time for Listeria innocua in orange juice. Food and Bioprocess Technology, 3, 752–761. doi:10.1007/s11947-008-0155-x.

    Article  Google Scholar 

  • Corte, F. V., De Fabrizio, S. V., Salvatori, D. M. & Alzamora, S. M. (2004). Survival of Listeria Innocua in apple juice as affected by vanillin or potassium sorbate. Journal of Food Safety, 24, 1–15. doi:10.1111/j.1745-4565.2004.tb00372.x

  • Davidson, P. M., & Naidu, A. S. (2000). Phyto-Phenols. In A. S. Naidu (Ed.), Natural Food Antimicrobial Systems (pp. 265–294). Boca Raton: CRC Press.

    Google Scholar 

  • Davidson, P. M., & Parrish, M. E. (1989). Methods for testing the efficacy of antimicrobials. Food Technology, 43(1), 148–155.

    CAS  Google Scholar 

  • Delaquis, P., Stanich, K., & Toivonen, P. (2005). Effect of pH on the inhibition of Listeria sp. by vanillin and vanillic. Journal of Food Protection, 68(7), 1472–1476.

    CAS  Google Scholar 

  • Denny, J., Bhat, M., & Eckmann, K. (2008). Outbreak of Escherichia coli O157:H7 associated with raw milk consumption in the Pacific Northwest. Foodborne Pathogens and Diseases, 58(1), 321–328.

    Article  Google Scholar 

  • Evrendilek, G. A. (2007). Survival of Escherichia coli O157:H7 in yogurt drink, plain yogurt and salted (tuzlu) yogurt: effects of storage time, temperature, back groundflora and product characteristics. International Journal of Dairy Technology, 60(2), 118–122.

    Article  Google Scholar 

  • FDA/USDA (Food and Drug Administration) (2003) Listeria monocytogenes risk assessment: Interpretive Summary. Available at: http://www.fda.gov/Food/ScienceResearch/ResearchAreas/RiskAssessmentSafetyAssessment/ucm185291.htm. Accessed 10 June 2010.

  • Ferrante, S., Guerrero, S., & Alzamora, S. M. (2007). Combined use of ultrasound and natural antimicrobials to inactivate Listeria monocytogenes in orange juice. Journal of Food Protection, 70(8), 1850–1857.

    CAS  Google Scholar 

  • Fitzgerald, D. J., Stratford, M., & Narbad, A. (2003). Analysis of the inhibition of food spoilage yeasts by vanillin. International Journal of Food Microbiology, 86(1–2), 113–122.

    Article  CAS  Google Scholar 

  • Fitzgerald, D. J., Stratford, G., Jasson, M., Ueckert, J., Bos, A., & Narbad, A. (2004a). Mode of antimicrobial action of vanillin against Escherichia coli, Lactobacillus plantarum and Listeria innocua. Journal of Applied Microbiology, 97(1), 104–113.

    Article  CAS  Google Scholar 

  • Fitzgerald, D. J., Stratford, M., Gasson, M. J., & Narbad, A. (2004b). The potential application of vanillin in preventing yeast spoilage of soft drinks and fruit juices. Journal of Food Protection, 67(2), 391–395.

    CAS  Google Scholar 

  • Fitzgerald, D. J., Stratford, M., Gasson, M. J., & Narbad, A. (2005). Structure-function analysis of the vanillin molecule and its antifungal properties. Journal of Agriculture and Food Chemistry, 53(5), 1769–1775.

    Article  CAS  Google Scholar 

  • Gastélum, G. G, R Avila-Sosa, López-Malo, A., & Enrique, P. (2010) Listeria innocua multi-target inactivation by thermo-sonication and vanillin. Food Bioprocess Technologies. doi:10.1007/s11947-010-0334.

  • Helander, I. M., Alakomi, H. L., Latva-Kala, K., Mattila-Sandholm, T., Pol, I., Smid, E. J., et al. (1998). Characterization of the action of selected essential oil components on Gram-negative bacteria. Journal of Agriculture and Food Chemistry, 46(9), 3590–3595.

    Article  CAS  Google Scholar 

  • Hocking, M. B. (1997). Vanillin: synthetic flavoring from spent sulfite liquor. Journal of Chemical Education, 74(9), 1055–1059. doi:10.1021/ed074p1055.

    Google Scholar 

  • Holley, R. A., & Patel, D. (2005). Improvement in shelf-life and safety of perishable foods by 4 plant essential oils and smoke antimicrobials. Food Microbiology, 22(4), 273–292.

    Article  CAS  Google Scholar 

  • Inchem (International Programme on Chemical Safety-INCHEM). Summary of Evaluations Performed by the Joint FAO/WHO Expert Committee on Food Additives. Hamilton, Ontario, CN: Canadian Centre for Occupational Health and Safety (2004). Available at: http://www.inchem.org. Accessed 11 Nov 2010.

  • Jay, J. M., & Rivers, G. M. (1984). Antimicrobial activity of some food flavouring compounds. Journal of Food Safety, 6(2), 129–139.

    Article  CAS  Google Scholar 

  • Juven, B. J., Kanner, J., Schved, F., & Weisslowicz, H. (1994). Factors that interact with the antibacterial action of thyme essential oil and its active constituents. The Journal of Applied Bacteriology, 76(6), 626–631.

    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(3), 463–469.

    Article  CAS  Google Scholar 

  • Karns, J. S., Van Kessel, J. S., McClusky, B. J., & Perdue, M. L. (2007). Incidence of Escherichia coli O157:H7 and E. coli virulence factors in US bulk tank milk as determine by polymerase chain reaction. Journal of Dairy Science, 90(7), 3212–3219.

    Article  CAS  Google Scholar 

  • Lambert, R. J. W., & Pearson, J. (2000). Susceptibility testing: accurate and reproducible minimum inhibitory concentration (MIC) and non-inhibitory concentration (NIC) values. Journal of Applied Microbiology, 88(5), 7847–7890.

    Google Scholar 

  • Li, Z., Grün, I. U., & Fernando, L. N. (2000). Interaction of vanillin with soy and dairy proteins in aqueous model systems: A thermodynamic study. Journal of Food Science, 65(6), 997–1001.

    Article  CAS  Google Scholar 

  • Lirdprapamongkol, L. K. H., Sakurai, N., Kawasaki, M. K., & Choo, Y. (2005). Vanillin suppresses in vitro invasion and in vivo metastasis of mouse breast cancer cells. European Journal of Pharmaceutical Sciences, 25(1), 57–65.

    Article  CAS  Google Scholar 

  • Lopez-Malo, A., Palou, E., León-Cruz, R., & Alzamora, S. M. (2006). Mixtures of natural and synthetic antifungal agents. Advances in Experimental Medicine and Biology, 571, 261–286.

    Article  CAS  Google Scholar 

  • Mann, C. M., & Markham, J. L. (1998). A new method for determining the minimum inhibitory concentration of essential oils. Journal of Applied Microbiology, 84(4), 538–544.

    Article  CAS  Google Scholar 

  • Maurya, D. K., Adhikari, S., Nair, C. K. K., & Devasagayam, T. P. A. (2007). DNA protective properties of vanillin against radiation under different conditions: possible mechanisms. Mutation Research, 634(1–2), 69–80.

    Article  CAS  Google Scholar 

  • Mejlholm, O., & Dalgaard, P. (2002). Antimicrobial effect of essential oils on the seafood spoilage micro-organism Photobacterium phosphoreun, in liquid media and fish products. Letters in Applied Microbiology, 34(1), 27–31.

    Article  CAS  Google Scholar 

  • Moon, K., Delaquis, P., Poivonen, T., & Stanich, K. (2006). Effect of vanillin on the fate of Listeria monocytogenes and Escherichia coli O157:H7 in a model apple juice medium and in apple juice. Food Microbiology, 23(2), 169–174.

    Article  CAS  Google Scholar 

  • Mourtzinos, I., Konteles, S., Kalogeropoulos, N., & Karathanos, V. T. (2009). Thermal oxidation of vanillin affects its antioxidant and antimicrobial properties. Food Chemistry, 114(3), 791–797.

    Article  CAS  Google Scholar 

  • Naidu MM, Sujith Kumar PV, Shyamala BN, Guruguntla Sulochana Mma, Maya Prakash, Thakur MS (2009) Enzyme-Assisted Process for Production of Superior Quality Vanilla Extracts from Green Vanilla Pods Using Tea Leaf Enzymes. Food and Bioprocess Technology. doi:10.1007/s11947-009-0291-y.

  • Ng, P. K. W., Hoehn, E., & Bushuk, W. (1989). Binding of vanillin by fababean proteins. Journal of Food Science, 54(1), 105–107.

    Article  CAS  Google Scholar 

  • Ngarmsak, M., Delaquis, P., Toivonen, P., Ngarmsak, T., Oorajkul, B., & Mazza, G. (2006). Antimicrobial activity of vanillin against spoilage microorganisms in stored fresh-cut mangoes. Journal of Food Protection, 69(7), 1724–1727.

    CAS  Google Scholar 

  • Park, S., Worobo, R. W., & Durst, R. A. (1999). Escherichia coli O157:H7 as an emerging foodborne pathogen: A literature review. Critical reviews in food science, 39(6), 481–502.

    Article  CAS  Google Scholar 

  • Penney, V., Henderson, H., Blum, C., & Johnson-Green, P. (2004). The potential of phytopreservatives and nisin to control microbial spoilage of minimally processed fruit yogurts. Innovative Food Science & Emerging Technologies, 5(3), 369–375.

    Article  CAS  Google Scholar 

  • Rangel, J. M., Sparling, P. H., Crowe, C., Griffin, P. M., & Swerdlow, D. L. (2005). Epidemiology of Escherichia coli O157:H7 Outbreaks, United States, 1982–2002. Emerging Infectious Diseases, 11(4), 603–609.

    Article  Google Scholar 

  • Ramachandra, R. S., & Ravishankar, G. A. (2000). Vanilla flavor: production by conventional and biotechnological routes. Journal of Science of Food and Agriculture, 80(3), 289–304.

    Article  Google Scholar 

  • Rojas-Grau, M. A., Raybaudi-Massilia, R. M., Soliva-Fortuny, R. C., Avena, T., Bustillos, R., McHugh, T. H., et al. (2007). Apple puree-alginate edible coating as carrier of antimicrobials agents to prolong shelf-life of fresh-cut apples. Postharvest Biology and Technology, 45(2), 254–264.

    Article  Google Scholar 

  • Rupasinghe, H. P. V., Boulter-Bitzer, J., Ahn, T., & Odumeru, J. A. (2006). Vanillin inhibits pathogenic and spoilage microorganisms in vitro and aerobic microbial growth in fresh-cut apples. Food Research International, 39(2), 575–580.

    Article  CAS  Google Scholar 

  • Shaughnessy, D. T., Schaaper, R. M., Umbach, D. M., & DeMarini, D. M. (2006). Inhibition of spontaneous mutagenesis by vanillin and cinnamaldehyde in Escherichia coli: Dependence on recombinational repair. Mutation Research, 602(1–2), 54–64.

    Article  CAS  Google Scholar 

  • Shyamala, B. N., Naidu, M., Sulochanamma, G., & Srinivas, P. (2007). Studies on the antioxidant activities of natural vanilla extract and its constituent compounds through in vitro models. Journal of Agriculture and Food Chemistry, 55(19), 7738–7743.

    Article  CAS  Google Scholar 

  • Sinha, A. K., Sharma, U. K., & Sharma, N. (2008). A comprehensive review on vanilla flavor: Extraction, isolation and quantification of vanillin and others constituents. International Journal of Food Science and Nutrition, 4(2), 299–326.

    Article  Google Scholar 

  • Smith-Palmer, A., Stewart, J., & Fyfe, L. (2001). The potential application of plant essential oils as natural food preservatives in soft cheese. Food Microbiology, 18(4), 463–470.

    Article  CAS  Google Scholar 

  • Tassou, E. H., Drosinos, E. H., & Nychas, G. J. E. (1995). Effects of essential oil from Mint (Mentha piperita) on Salmonella enteritidis and Listeria monocytogenes in model food systems at 4 °C and 10 °C. The Journal of Applied Bacteriology, 78(6), 593–600.

    Article  CAS  Google Scholar 

  • Tipparaju, S., Ravishankar, S., & Slade, P. J. (2004). Survival of Listeria monocytogenes in vanilla-flavored soy and dairy products stored at 8 °C. Journal of Food Protection, 67(2), 378–382.

    Google Scholar 

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  1. Grupo de Investigación en Biotecnología de Alimentos, Departamento de Tecnología de Alimentos, Nutrición y Bromatología, Universidad de Murcia, Murcia, Spain

    Rita María Cava-Roda, Amaury Taboada-Rodríguez, María Teresa Valverde-Franco & Fulgencio Marín-Iniesta

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  1. Rita María Cava-Roda
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  2. Amaury Taboada-Rodríguez
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Correspondence to Fulgencio Marín-Iniesta.

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Cava-Roda, R.M., Taboada-Rodríguez, A., Valverde-Franco, M.T. et al. Antimicrobial Activity of Vanillin and Mixtures with Cinnamon and Clove Essential Oils in Controlling Listeria monocytogenes and Escherichia coli O157:H7 in Milk. Food Bioprocess Technol 5, 2120–2131 (2012). https://doi.org/10.1007/s11947-010-0484-4

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Keywords

  • Natural antimicrobial
  • Vanillin
  • Listeria monocytogenes
  • Escherichia coli O157:H7