Anti-staphylococcal effect of cinnamaldehyde in milk
Main Article Content
Keywords
antibacterial activity, cinnamaldehyde, fat, milk safety, Staphylococcus aureus
Abstract
The survival of Staphylococcus aureus in inoculated (105 colony forming units [CFU]/mL) 3.2% and 0.5% fat ultra-high temperature-pasteurized milk samples containing 0%, 0.05%, or 0.1% cinnamaldehyde stored at 4°C or 10°C was evaluated within 15 days. S. aureus populations reached 7.92 (0.5% fat) and 7.95 (3.2% fat) log CFU/mL in control milk samples stored at 10°C, while in milk sample stored at 4°C, S. aureus counts remained almost unchanged. At the end of the study, the number of this pathogen decreased by 1.52–4.04 log CFU/mL in milk treated with cinnamaldehyde. The greatest anti-staphylococcal effect was achieved in low-fat milk at 10°C and treated with 0.1% cinnamaldehyde.
References
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Martinsen B., Oppegaard H., Wichstrøm R. and Myhr E.G.I.L. 1992. Temperature-dependent in vitro antimicrobial activity of four 4-quinolones and oxytetracycline against bacteria pathogenic to fish. Antimicrob Agents Chemother. 36(8):1738–1743. https:// doi.org/10.1128/AAC.36.8.1738
Masghati S. and Ghoreishi S.M. 2018. Supercritical CO2 extraction of cinnamaldehyde and eugenol from cinnamon bark: optimi-zation of operating conditions via response surface methodol-ogy. J Supercrit Fluids. 140:62–71. https://doi.org/10.1016/j.supflu.2018.06.002
Medve?ová A. and Valík. 2012. Staphylococcus aureus: characterisation and quantitative growth description in milk and artisanal raw milk cheese production. In: Eissa A.A. (ed.) Structure and Function of Food Engineering. Books on Demand, Intech Open, London, pp. 71–101. https://doi.org/10.5772/48175
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Smith-Palmer A., Stewart J. and Fyfe L. 2001. The potential application of plant essential oils as natural food preservatives in soft cheese. Food Microbiol. 18(4):463–470. https://doi.org/10.1006/fmic.2001.0415
Tassou C.C., Drosinos E.H. and Nychas G.J.E. 1995. Effects of essential oil from mint (Menthapiperita) on Salmonella enteritidis and Listeria monocytogenes in model food systems at 4°C and 10°C. J. Appl. Microbiol. 78(6):593–600. https://doi.org/10.1111/j.1365-2672.1995.tb03104.x
Tayel A.A., Hussein H., Sorour N.M. and El-Tras W.F. 2015. Foodborne pathogens prevention and sensory attributes enhancement in processed cheese via flavoring with plant extracts. J. Food Sci. 80(12):2886–2891. https://doi.org/10.1111/1750-3841.13138
Usta J., Kreydiyyeh S., Barnabe P., Bou-Moughlabay Y. and Nakkash-Chmaisse H. 2003. Comparative study on the effect of cinna-mon and clove extracts and their main components on different types of ATPases. Hum. Exp.Toxicol. 22(7):355–362. https://doi. org/10.1191/0960327103ht379oa
Valero A., Pérez-Rodríguez F., Carrasco E., Fuentes-Alventosa J.M., García-Gimeno R.M. and Zurera G. 2009. Modelling the growth boundaries of Staphylococcus aureus: effect of temperature, pH and water activity. Int. J. Food Microbiol. 133(1–3):186–194. https://doi.org/10.1016/j.ijfoodmicro.2009.05.023
Vidanagamage S.A., Pathiraje P.M.H.D. and Perera O.D.A.N. 2016. Effects of cinnamon (Cinnamomumverum) extract on functional properties of butter. Procedia Food Sci. 6:136–142. https://doi.org/10.1016/j.profoo.2016.02.033
Wojtys A. and Jankowski T. 2004. The effect of temperature on the permeation rate of some selected essential oils into baker’s yeast cells. ywno Nauka Technologia Jako, 11(3):77–86.
Xing X., Zhang Y., Wu Q., Wang X., Ge W. and Wu C. 2016. Prevalence and characterization of Staphylococcus aureus isolated from goat milk powder processing plants. Food Control. 59:644–650. https://doi.org/10.1016/j.foodcont.2015.06.042
Yuste J. and 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 Microbiol. 20(3):365–370. https://doi.org/10.1016/S0740-0020(02)00130-2
Babic M., Glisic M., Zdravkovic N., Djordjevic J., Velebit B., Ledina T., et al. 2019. Inhibition of Staphylococcus aureus by cinnamaldehyde and its effect on sensory properties of milk. IOP Conf Ser Earth Environ Sci. 333:012042. https://doi.org/10.1088/1755-1315/333/1/012042
Basanisi M.G., La Bella G., Nobili G., Franconieri I., and La Salandra G. 2017. Genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and dairy products in South Italy. Food Microbiol. 62:141–146. https://doi.org/10.1016/j.fm.2016.10.020
Boskovic M., Djordjevic J., Glisic M., Ciric J., Janjic J., Zdravkovic N., et al. 2019. The effect of oregano (Origanumvulgare) essential oil on four Salmonella serovars and shelf life of refrigerated pork meat packaged under vacuum and modified atmosphere. J. Food Process. Preserv. 44(1):e14311. https://doi.org/10.1111/ jfpp.14311
Boskovic M., Djordjevic J., Ivanovic J., Janjic J., Zdravkovic N., Glisic M., et al. 2017. Inhibition of Salmonella by thyme essential oil and its effect on microbiological and sensory properties of minced pork meat packaged under vacuum and modified atmosphere. Int. J. Food Microbiol. 258:58–67. https://doi.org/10.1016/j.ijfoodmicro.2017.07.011
Burt S. 2004. Essential oils: their antibacterial properties and potential applications in foods-a review. Int. J. Food Microbiol. 94(3):223– 253. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022
Cava R., Nowak E., Taboada A. and Marin-Iniesta F. 2007. Antimicrobial activity of clove and cinnamon essential oils against Listeria monocytogenes in pasteurized milk. J. Food Prot. 70(12):2757–2763. https://doi.org/10.4315/0362-028X-70.12.2757
Cava-Roda R.M., Taboada-Rodríguez A., Valverde-Franco M.T. and Marín-Iniesta F. 2012. Antimicrobial activity of vanillin and mixtures with cinnamon and clove essential oils in controlling Listeria monocytogenes and Escherichia coli O157: H7 in milk. Food Bioproc. Tech. 5(6):2120–2131. https://doi.org/10.1007/ s11947-010-0484-4
Clinical and Laboratory Standards Institute (CLSI). 2006. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically. Approved Standard, 7th ed. CLSI Publication M7-A7. Clinical and Laboratory Standards Institute, Wayne PA.
Cui H.Y., Zhou H., Lin L., Zhao C.T., Zhang X.J., Xiao Z.H., et al. 2016. Antibacterial activity and mechanism of cinnamon essential oil and its application in milk. J. Anim. Plant. Sci. 26:532–541.
Di Pasqua R., Hoskins N., Betts G. and Mauriello G. 2006. Changes in membrane fatty acids composition of microbial cells induced by addiction of thymol, carvacrol, limonene, cinnamaldehyde, and eugenol in the growing media. J. Agric. Food Chem. 54(7):2745–2749. https://doi.org/10.1021/jf052722l
Doyle A.A. and Stephens J.C. 2019. A review of cinnamaldehyde and its derivatives as antibacterial agents. Fitoterapia.139:104405. https://doi.org/10.1016/j.fitote.2019.104405
Friedman M. 2017. Chemistry, antimicrobial mechanisms, and antibiotic activities of cinnamaldehyde against pathogenic bacteria in animal feeds and human foods. J. Agric. Food Chem. 65(48):10406–10423. https://doi.org/10.1021/acs.jafc.7b04344
Gill A.O. and Holley R.A. 2004. Mechanisms of bactericidal action of cinnamaldehyde against Listeria monocytogenes and of euge-nol against L. monocytogenes and Lactobacillus sakei. Appl. Environ. Microbiol. 70(10):5750–5755. https://doi.org/10.1128/ AEM.70.10.5750-5755.2004
Guler S. and Seker M. 2009. The effect of cinnamon and guar gum on Bacillus cereus population in milk. J. Food Process. Preserv. 33(3):415–426. https://doi.org/10.1111/j.1745-4549.2009.00417.x
Hyldgaard M., Mygind T. and Meyer R.L. 2012. Essential oils in food preservation: mode of action, synergies, and interactions with food matrix components. Front. Microbiol. 3:12. https://doi.org/10.3389/fmicb.2012.00012
International Organization for Standardization (ISO). 1999. ISO Standard No. 6888-1: Microbiology of food and animal feeding stuffs—horizontal method for the enumeration of coagulase-positive staphylococci (Staphylococcus aureus and other species) part 1: Technique using Baird-Parker agar medium. International Organization for Standardization, Geneva, Switzerland.
Jablonski L.M. and Bohach G.A. 1997. Staphylococcus aureus. In Doyle M.P., Beuchat L.R. and Montville T.J. (ed.). Food microbiology fundamentals and frontiers. ASM Press, Washington DC. 353–375.
Jans C., Merz A., Johler S., Younan M., Tanner S.A., Kaindi D.W.M., et al. 2017. East and west African milk products are reservoirs for human and livestock-associated Staphylococcus aureus. Food Microbiol. 65:64–73. https://doi.org/10.1016/j.fm.2017.01.017
Jørgensen H.J., Mørk T. and Rørvik L.M. 2005. The occurrence of Staphylococcus aureus on a farm with small-scale production of raw milk cheese. J. Dairy Sci. 88(11):3810–3817. https://doi.org/10.3168/jds.S0022-0302(05)73066-6
Leja K., Szudera-Ko?czal K., ?wita?a E., Juzwa W., KowalczewskiP.?. and Czaczyk K. 2019. The influence of selected plant essen-tial oils on morphological and physiological characteristics in Pseudomonas orientalis. Foods. 8(7):277. https://doi.org/ 10.3390/foods8070277
Lianou A., Moschonas G., Nychas G.J.E. and Panagou, E.Z. 2018. Growth of Listeria monocytogenes in pasteurized vanilla cream pudding as affected by storage temperature and the presence of cinnamon extract. Food Res. Int. 106:1114–1122. https://doi.org/10.1016/j.foodres.2017.11.027
Licon C.C., Moro A., Librán C.M., Molina A.M., Zalacain A., Berruga M.I., et al. 2020. Volatile transference and antimicrobial activity of cheeses made with ewes’ milk fortified with essential oils. Foods. 9(1):35. https://doi.org/10.3390/foods9010035
Liu T.T. and Yang T.S. 2012. Antimicrobial impact of the components of essential oil of Litseacubeba from Taiwan and antimi-crobial activity of the oil in food systems. Int. J. Food Microbiol. 156(1):68–75. https://doi.org/10.1016/j.ijfoodmicro.2012.03.005
Martinsen B., Oppegaard H., Wichstrøm R. and Myhr E.G.I.L. 1992. Temperature-dependent in vitro antimicrobial activity of four 4-quinolones and oxytetracycline against bacteria pathogenic to fish. Antimicrob Agents Chemother. 36(8):1738–1743. https:// doi.org/10.1128/AAC.36.8.1738
Masghati S. and Ghoreishi S.M. 2018. Supercritical CO2 extraction of cinnamaldehyde and eugenol from cinnamon bark: optimi-zation of operating conditions via response surface methodol-ogy. J Supercrit Fluids. 140:62–71. https://doi.org/10.1016/j.supflu.2018.06.002
Medve?ová A. and Valík. 2012. Staphylococcus aureus: characterisation and quantitative growth description in milk and artisanal raw milk cheese production. In: Eissa A.A. (ed.) Structure and Function of Food Engineering. Books on Demand, Intech Open, London, pp. 71–101. https://doi.org/10.5772/48175
Nam H.M., Lee A.L., Jung S.C., Kim M.N., Jang G.C., Wee S.H. and Lim S.K. 2011. Antimicrobial susceptibility of Staphylococcus aureus and characterization of methicillin-resistant Staphylococcus aureus isolated from bovine mastitis in Korea. Foodborne Pathog. Dis. 8(2):231–238. https://doi.org/10.1089/ fpd.2010.0661
Nazzaro F., Fratianni F., De Martino L., Coppola R. and De Feo V. 2013. Effect of essential oils on pathogenic bacteria. Pharmaceuticals. 6(12):1451–1474. https://doi.org/10.3390/ph6121451
Noël T.S., Kifouli A., Boniface Y., Edwige D.A., Farid B.M. and Fatiou T. 2016. Antimicrobial and physico-chemical effects of essential oils on fermented milk during preservation. J. Appl. Biosci. 99:9467–9475. https://doi.org/10.4314/jab.v99i1.12
Perricone M., Arace E., Corbo M.R., Sinigaglia M. and Bevilacqua A. 2015. Bioactivity of essential oils: a review on their interaction with food components. Front. Microbiol. 6:76. https://doi.org/10.3389/fmicb.2015.00076
Shen S., Zhang T., Yuan Y., Lin S., Xu J. and Ye H. 2015. Effects of cinnamaldehyde on Escherichia coli and Staphylococcus aureus membrane. Food Control. 47:196–202. https://doi.org/10.1016/j. foodcont.2014.07.003
Smith-Palmer A., Stewart J. and Fyfe L. 1998. Antimicrobial properties of plant essential oils and essences against five important food-borne pathogens. Lett. Appl. Microbiol. 26(2):118–122. https://doi.org/10.1046/j.1472-765X.1998.00303.x
Smith-Palmer A., Stewart J. and Fyfe L. 2001. The potential application of plant essential oils as natural food preservatives in soft cheese. Food Microbiol. 18(4):463–470. https://doi.org/10.1006/fmic.2001.0415
Tassou C.C., Drosinos E.H. and Nychas G.J.E. 1995. Effects of essential oil from mint (Menthapiperita) on Salmonella enteritidis and Listeria monocytogenes in model food systems at 4°C and 10°C. J. Appl. Microbiol. 78(6):593–600. https://doi.org/10.1111/j.1365-2672.1995.tb03104.x
Tayel A.A., Hussein H., Sorour N.M. and El-Tras W.F. 2015. Foodborne pathogens prevention and sensory attributes enhancement in processed cheese via flavoring with plant extracts. J. Food Sci. 80(12):2886–2891. https://doi.org/10.1111/1750-3841.13138
Usta J., Kreydiyyeh S., Barnabe P., Bou-Moughlabay Y. and Nakkash-Chmaisse H. 2003. Comparative study on the effect of cinna-mon and clove extracts and their main components on different types of ATPases. Hum. Exp.Toxicol. 22(7):355–362. https://doi. org/10.1191/0960327103ht379oa
Valero A., Pérez-Rodríguez F., Carrasco E., Fuentes-Alventosa J.M., García-Gimeno R.M. and Zurera G. 2009. Modelling the growth boundaries of Staphylococcus aureus: effect of temperature, pH and water activity. Int. J. Food Microbiol. 133(1–3):186–194. https://doi.org/10.1016/j.ijfoodmicro.2009.05.023
Vidanagamage S.A., Pathiraje P.M.H.D. and Perera O.D.A.N. 2016. Effects of cinnamon (Cinnamomumverum) extract on functional properties of butter. Procedia Food Sci. 6:136–142. https://doi.org/10.1016/j.profoo.2016.02.033
Wojtys A. and Jankowski T. 2004. The effect of temperature on the permeation rate of some selected essential oils into baker’s yeast cells. ywno Nauka Technologia Jako, 11(3):77–86.
Xing X., Zhang Y., Wu Q., Wang X., Ge W. and Wu C. 2016. Prevalence and characterization of Staphylococcus aureus isolated from goat milk powder processing plants. Food Control. 59:644–650. https://doi.org/10.1016/j.foodcont.2015.06.042
Yuste J. and 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 Microbiol. 20(3):365–370. https://doi.org/10.1016/S0740-0020(02)00130-2
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Babic, M., Glisic, M., Djordjevic, J., Zdravkovic, N., Savic-Radovanovic, R., Baltic, M., & Boskovic Cabrol, M. (2021). Anti-staphylococcal effect of cinnamaldehyde in milk. Italian Journal of Food Science, 33(2), 108-115. https://doi.org/10.15586/ijfs.v33i2.1976
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How to Cite
Babic, M., Glisic, M., Djordjevic, J., Zdravkovic, N., Savic-Radovanovic, R., Baltic, M., & Boskovic Cabrol, M. (2021). Anti-staphylococcal effect of cinnamaldehyde in milk. Italian Journal of Food Science, 33(2), 108-115. https://doi.org/10.15586/ijfs.v33i2.1976