Raw donkey milk versus raw cow’s milk. A preliminary study to compare the growth of Listeria monocytogenes and Staphylococcus aureus
DOI:
https://doi.org/10.12834/VetIt.2140.13666.1Keywords:
Raw milk, Donkey, Cow, Listeria monocytogenes, Staphylococcus aureus, Lactic acid bacteriaAbstract
Gram-positive foodborne pathogens such as Listeria monocytogenes and Staphylococcus aureus can grow in a wide variety of foods, including raw milk. The aim of the study was to compare the growth of L. monocytogenes and S. aureus inoculated in donkey and cow samples of raw milk during a storage time of 11 days at 8 °C. Moreover, the study aimed to evaluate the influence of lactic acid bacteria (LAB) content on the growth of the two microbiological populations considered. LAB content was lower in raw donkey milk than in raw cow’s milk during the entire analyses; on the other hand, pH levels were higher in the donkey milk rather than in the cow’s milk, although both values showed a decrease at the day 11. S. aureus showed no significant differences in the two types of milk. From day 0 to 11, L. monocytogenes increased from 3.68 ± 0.02 log CFU/mL to 6.31 ± 0.07 log CFU/mL and from 3.64 ± 0.04 log CFU/mL to 4.59 ± 1.04 log CFU/mL, in donkey milk and in cow’s milk, respectively. Our results showed that donkey milk is a more favourable matrix to support the growth of L. monocytogenes than cow’s milk.
References
Amézquita A., Brashears M.M. 2002. Competitive inhibition of Listeria monocytogenes in ready-to-eat meat products by lactic acid bacteria. J Food Prot. 65(2), 316-325.
Aspri M., Economou N., Papademas P. 2017. Donkey milk: An overview on functionality, technology, and future prospects. Food Rev Int. 33(3), 316-333.
Baldi A., Politis I., Pecorini C., Fusi E., Chronopoulou R., et al. 2005. Biological effects of milk proteins and their peptides with emphasis on those related to the gastrointestinal eco system. J Dairy Res. 72, 66-72.
Balla E., Dicks L.M., Du Toit M., Van Der Merwe M.J., Holzapfel W.H. 2000. Characterization and cloning of the genes encoding enterocin 1071A and enterocin 1071B, two antimicrobial peptides produced by Enterococcus faecalis BFE 1071. Appl Environ Microbiol. 66, 1298-1304.
Benkerroum N. 2008. Antimicrobial activity of lysozyme with special relevance to milk. Afr J Biotechnol. 7, 4856-4867.
Brumini D., Criscione A., Salvatore S., Vegarud G.E., Marletta D. 2016. Whey proteins and their antimicrobial properties in donkey milk: a brief review. Dairy Sci & Technol. 96, 1-14.
Carminati D., Tidona F., Fornasari M., Rossetti L., Meucci A., et al. 2014. Biotyping of cultivable lactic acid bacteria isolated from donkey milk. Lett Appl Microbiol. 59(3), 299-305.
Cavallarin L., Giribaldi M., Soto-Del Rio M.D., Valle E., Barbarino G., et al. 2015. A survey on the milk chemical and microbiological quality in dairy donkey farms located in North-Western Italy. Food Control. 50, 230-235.
Chiavari C., Coloretti F., Nanni M., Sorrentino E., Grazia L. 2005. Use of donkey’s milk for a fermented beverage with lactobacilli. Le Lait. 85, 481-490.
Cintas L.M., Casaus P., Herranz C., Håvarstein L.S., Holo H., et al. 2000. Biochemical and genetic evidence that Enterococcus faecium L50 produces enterocins L50A and L50B, the sec-dependent enterocin P, and a novel bacteriocin secreted without an N-terminal extension termed enterocin Q. J Bacteriol. 182(23), 6806-6814.
Coppola R., Salimei E., Succi M., Sorrentino E., Nanni M., et al. 2002. Behaviour of Lactobacillus rhamnosus strains in ass’s milk. Ann Microbiol. 52, 55-60.
Doreau M., Martin-Rosset W. 2011. Dairy animals: horse. In Encyclopedia of dairy sciences; Fuquay, J.W., Fox, P.F., McSweeney P.L.H., 2nd Eds.; Academic Press: San Diego, pp. 358-364.
European Commission. 2002. Commission Regulation (EC) No. 178/2002 of 28 January 2002 laying down the general principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in matters of food safety. Off J. L31, 1-24.
European Commission. 2004. Commission Regulation (EC) No. 853/2004 of 29 April 2004 laying down specific hygiene rules for on the hygiene of foodstuffs. Off J. L139, 55.
European Commission. 2005. Commission Regulation (EC) No. 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Off J. L338, 1-26.
EFSA Panel on Biological Hazards - BIOHAZ. 2015. Scientific opinion on the public health risks related to the consumption of raw drinking milk. EFSA Journal. 13(1), 39-40.
Ellison R.T., Giehl T.J. 1991. Killing of gram-negative bacteria by lactoferrin and lysozyme. J Clin Invest. 88, 1080-1091.
Farnaud S., Evans R.W. 2003. Lactoferrin - a multifunctional protein with antimicrobial properties. Mol Immunol. 40, 395-404.
Floris R., Recio I., Berkhout B., Visser S. 2003. Antibacterial and antiviral effects of milk proteins and derivatives thereof. Curr Pharm Des. 9, 1257-1275.
Giacometti F., Bardasi L., Merialdi G., Morbarigazzi M., Federici S., et al. 2016. Shelf life of donkey milk subjected to different treatment and storage conditions. J. Dairy Sci. 99, 1-9.
Gilmore M.S., Clewell D.B., Ike Y., Shankar N. 2014. Enterococci: from Commensals to Leading Causes of Drug Resistant Infection. Massachusetts Eye and Ear Infirmary, Boston.
Guo H.Y., Pang K., Zhang X.Y., Zhao L., Chen S.W., et al. 2007. Composition, physiochemical properties, nitrogen fraction distribution, and amino acid profile of donkey milk. J Dairy Sci. 90, 1635-1643.
Kang J.H., Lee M.S. 2005. Characterization of a bacteriocin produced by Enterococcus faecium GM-1 isolated from an infant. J Appl Microbiol. 98(5), 1169-1176.
Mehmeti I., Bytyqi H., Muji S., Nes I.F., Diep, D.B. 2017. The prevalence of Listeria monocytogenes and Staphylococcus aureus and their virulence genes in bulk tank milk in Kosovo. J Infect Dev Ctries. 11(3), 247-254.
Monti G., Bertino E., Muratore M.C., Coscia A., Cresi F., et al. 2007. Efficacy of donkey’s milk in treating highly problematic cow’s milk allergic children: An in vivo and in vitro study. Pediatr Allergy Immunol. 18, 258-264.
Mottola A., Alberghini L., Giaccone V., Marchetti P., Tantillo G., et al. 2018. Microbiological safety and quality of Italian donkey milk. J Food Saf. 38, e12444.
Murua A., Todorov S.D., Vieira A.D.S., Martinez R.C.R., Cencič A., et al. 2013. Isolation and identification of bacteriocinogenic strain of Lactobacillus plantarum with potential beneficial properties from donkey milk. J Appl Microbiol. 114(6), 1793-1809.
Neviani E., Carminati D., Veaux M., Hermier J., Giraffa G. 1991. Characterization of Lactobacillus helveticus strains resistant to lysozyme. Le Lait. 71, 65-73.
Nilsen T., Nes I.F., Holo H. 1998. An exported inducer peptide regulates bacteriocin production in Enterococcus faecium CTC492. J Bacteriol. 180 (7), 1848-1854.
Pilla R., Daprà V., Zecconi A., Piccinini R. 2010. Hygienic and health characteristics of donkey milk during a follow-up study. J Dairy Res. 77, 392-397.
Quigley L., O'Sullivan O., Stanton C., Beresford T.P., Ross R.P., et al. 2013. The complex microbiota of raw milk. FEMS Microbiol Rev. 37, 664-698.
Salimei E., Fantuz F. 2012. Equid milk for human consumption. Int Dairy J. 24(2), 130-142.
Salimei E., Fantuz F., Coppola R., Chiofalo B., Polidori P., et al. 2004. Composition and characteristics of ass’s milk. Anim Res. 53, 67-78.
Šarić L., Šarić B.M., Mandić A.I., Torbica A.M., Tomić J.M., et al. 2012. Antibacterial properties of domestic Balkan donkeys’ milk. Int Dairy J. 25, 142-146.
Šarić L.C., Šarić B.M., Kravić S.T., Plavšić D.V., Milovanović I.L., et al. 2014a. Antibacterial activity of domestic Balkan donkey milk toward Listeria monocytogenes and Staphylococcus aureus. Food Feed Res. 4, 47-54.
Šarić, L., Šarić, B., Mandić, A., Tomić, J., Torbica, A., et al. 2014b. Antibacterial activity of donkey milk against Salmonella. Agro Food Ind Hi Tech. 25, 30-34.
Soto Del Rio M.L.D., Dalmasso A., Civera T., Bottero M.T. 2017. Characterization of bacterial communities of donkey milk by high-throughput sequencing. Int J Food Microbiol. 251, 67-72.
Souroullas K., Aspri M., Papademas P. 2018. Donkey milk as a supplement in infant formula: Benefits and technological challenges. Food Res Int. 109, 416-425.
Tidona F., Sekse C., Criscione A., Jacobsen M., Bordonaro S., et al. 2011. Antimicrobial effect of donkeys’ milk digested in vitro with human gastrointestinal enzymes. Int Dairy J. 21, 158-165.
Tomita H., Fujimoto S., Tanimoto K., Ike Y. 1996. Cloning and genetic organization of the bacteriocin 31 determinant encoded on the Enterococcus faecalis pheromone-responsive conjugative plasmid pYI17. J Bacteriol. 178(12), 3585-3593.
Uniacke-Lowe T., Huppertz T., Fox P.F. 2010. Equine milk proteins: chemistry, structure and nutritional significance. Int Dairy J. 20, 609-629.
Vincenzetti S., Polidori P., Vita A. 2007. Nutritional characteristitcs of donkey’s milk protein fraction. In: J.R. Ling (ed.) Protein Research Trends. Nova Science Publishers Inc., New York, USA, pp. 207-225.
Vincenzetti S., Savini M., Cecchini C., Micozzi D., Carpi F., et al. 2011. Effects of lyophilization and use of probiotics on donkey’s milk nutritional characteristics. Int J Food Eng. 7(5), 8.
White C.H. 2001. Testing milk and milk products. In E. H. Marth & J. L. Steele (Eds.), Applied dairy microbiology (2nd ed., pp. 645-680). New York: Marcel Dekker.
Yamashita H., Tomita H., Inoue T., Ike Y. 2011. Genetic organization and mode of action of a novel bacteriocin, bacteriocin 51: determinant of VanA-type vancomycin-resistant Enterococcus faecium. Antimicrob Agents Chemother. 55(9), 4352-4360.
Yamauchi K., Wakabayashi H., Shin K., Takase M. 2006. Bovine lactoferrin: benefits and mechanism of action against infections. Biochem Cell Biol. 84(3), 291-296.
Zhang X.Y., Zhao L., Jiang L., Dong M.L., Ren F.Z. 2008. The antimicrobial activity of donkey milk and its microflora changes during storage. Food Control. 19, 1191-1195.
Zhao T., Doyle M.P., Zhao P. 2004. Control of Listeria monocytogenes in a biofilm by competitive-exclusion microorganisms. Appl Environ Microbiol. 70(7), 3996-4003.
Zhao T., Podtburg T.C., Zhao P., Schmidt B.E., Baker D.A., et al. 2006. Control of Listeria spp. by competitive-exclusion bacteria in floor drains of a poultry processing plant. Appl Environ Microbiol. 72(5), 3314-3320.
