Biotype characterization of Staphylococcus aureus isolated from milk and dairy products of private production in the western regions of Ukraine

Keywords: staphylococci, biotypes, MRSA, enterotoxins

Abstract

Prevention of foodborne diseases is a priority for the world health system. In the process of manufacturing milk and dairy products, the most important factor compromising their safety is seeding with a conditionally pathogenic and pathogenic microflora. Salmonella, Escherichia coli, Listeria and other microorganisms that reproduce in dairy products without changing their organoleptic properties are a particular danger. Staphylococcus aureus is an opportunistic, conditionally pathogenic microorganism that often contaminates raw milk and dairy products. The aim of the research presented in this article was to determine the dissemination of S. aureus in milk and milk products of household production in the western regions of Ukraine, to identify the biotypes of S. aureus, production of enterotoxins and the presence of methicillin-resistant strains. S. aureus was isolated on BD Baird-Parker Agar. The biotypes of S. aureus were determined according to Meer. The determination of MRSA was carried out on the chromogenic Agar chromID MRSA ("Biomerioux", Russia). The mecA gene was determined using the LightCycler MRSA Advanced Test with LightCycler 2.0 primer (Roche Molecular Biochemicals, Germany). To determine staphylococcal enterotoxins, the test system RIDASCREENSET A, B, C, D, E (R-Biopharm AG, Darmstadt, Germany) was used. We isolated saprophyte staphylococci from milk of raw and dairy products in western regions of Ukraine in 82.7–97.4% of samples. S. aureus is much more rarely isolated from these dairy products, so it was isolated from sour cream at 62.8 ± 0.9%, from milk at 35.5 ± 1.3% and cottage cheese at 23.0 ± 1.6%. Of the most well known biotypes of S. aureus present in milk of raw and dairy products of domestic production, two ecological types were distinguished: human and cattle. In this case S. aureus var. hominis was isolated more often than in S. aureus var. bovis. This gives grounds to believe that the main source of contamination with milk staphylococci of raw and dairy products of domestic production is people. Enterotoxin type A, which causes foodborne toxemia, was produced by S. aureus in 40.0 ± 0.5% of cases. Consequently, home-produced dairy products can spread staphylococcal toxicity caused by S. aureus var. hominis. It was found that 17.8 ± 0.6% of S. aureus var. hominis were resistant to methicillin, which is 1.8 times greater than that of S. aureus var. bovis. This gives grounds to consider that there is a risk of MRSA infection to consumers of home-produced dairy products. All methicillin-resistant staphylococci studied produced enterotoxins. 

References

Al-Ashmawy, M. A., Sallam, K. I., Abd-Elghany, S. M., Elhadidy, M., & Tamura, T. (2016). Prevalence, molecular characterization, and antimic robial susceptibility of methicillin-resistant Staphylococcus aureus iso lated from milk and dairy products. Foodborne Pathogens and Disease, 13(3), 156–162.

Anderson, K. L., Lyman, R., Moury, K., Ray, D., Watson, D. W., & Correa, M. T. (2012). Molecular epidemiology of Staphylococcus aureus masti tis in dairy heifers. Journal of Dairy Science, 95(9), 4921–4930.

Argudin, M. A., Mendoza, M. C., & Rodicio, M. R. (2010). Food poisoning and Staphylococcus aureus enterotoxins. Toxins, 2, 1751–1773.

Ateba, C. N., Mbewe, M., Moneoang, M. S., & Bezuidenhout, C. C. (2010). Antibiotic-resistant Staphylococcus aureus isolated from milk in the Mafikeng Area, North West province, South Africa. South African Journal of Science, 106(11–12), 1–6.

Bardiau, M., Yamazaki, K., Duprez, J. N., Taminiau, B., Mainil, J. G., & Ote, I. (2013). Genotypic and phenotypic characterization of methicillin resistant Staphylococcus aureus (MRSA) isolated from milk of bovine mastitis. Letters in Applied Microbiology, 57(3), 181–186.

Basanisi, M. G., La Bella, G., Nobili, G., Franconieri, I., & La Salandra, G. (2017). Genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and dairy products in South Italy. Food Microbiology, 62, 141–146.

Bharathy, S., Gunaseelan, L., Porteen, K., & Bojiraj, M. (2015). Prevalence of Staphylococcus aureus in raw milk: Can it be a potential public health threat. International Journal of Advanced Research, 3(2), 801–806.

Carfora, V., Caprioli, A., Marri, N., Sagrafoli, D., Boselli, C., Giacinti, G., Sor bara L., Dottarelli S., Battisti A., & Amatiste, S. (2015). Enterotoxin genes, enterotoxin production, and methicillin resistance in Staphylococcus aureus isolated from milk and dairy products in Central Italy. International Dairy Journal, 42, 12–15.

Crago, B., Ferrato, C., Drews, S. J., Svenson, L. W., Tyrrell, G., & Louie, M. (2012). Prevalence of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in food samples associated with foodborne illness in Alberta, Canada from 2007 to 2010. Food Microbiology, 32(1), 202–205.

Cremonesi, P., Perez, G., Pisoni, G., Moroni, P., Morandi, S., Luzzana, M., Brasca, M., & Castiglioni, B. (2007). Detection of enterotoxigenic Staphylo coccus aureus isolates in raw milk cheese. Letters in applied microbiology, 45(6), 586–591.

Davis, K. A., Stewart, J. J., Crouch, H. K., Florez, C. E., & Hospenthal, D. R. (2004). Methicillin-resistant Staphylococcus aureus (MRSA) nares colonization at hospital admission and its effect on subsequent MRSA infection. Clinical Infectious Diseases, 39(6), 776–782.

Doulgeraki, A. I., Di Ciccio, P., Ianieri, A., & Nychas, G. J. E. (2017). Methicillin-resistant food-related Staphylococcus aureus: A review of current knowledge and biofilm formation for future studies and applications. Research in Microbiology, 168(1), 1–15.

Febler, A., Scott, C., Kadlec, K., Ehricht, R., Monecke, S., & Schwarz, S. (2010). Characterization of methicillin-resistant Staphylococcus aureus ST-398 from cases of bovine mastitis. Journal of Antimicrobial Chemotherapy, 65(4), 619–625.

Fournier, C., Kuhnert, P., Frey, J., Miserez, R., Kirchhofer, M., Kaufmann, T., Stener, A., & Graber, H. U. (2008). Bovine Staphylococcus aureus: association of virulence genes, genotypes and clinical outcome. Re search in Veterinary Science, 85, 439–448.

Graber, H. U., Naskova, J., Studer, E., Kaufmann, T., Kirchhofer, M., Brech bühl, M., Schaeren, W., A. Steiner, A., & Fournier, C. (2009). Mastitis-related subtypes of bovine Staphylococcus aureus are characterized by different clinical properties. Journal of Dairy Science, 92, 1442–1451.

Habib, F., Rind, R., Durani, N., Bhutto, A. L., Buriro, R. S., Tunio, A., Aijaz, N., Lakho, S. A., Bugti, A. G., & Shoaib, M. (2015). Morphological and cultural characterization of Staphylococcus aureus isolated from differ rent animal species. Journal of Applied Environmental and Biological Sciences, 5(2), 15–26.

Hamid, S., Bhat, M. A., Mir, I. A., Taku, A., Badroo, G. A., Nazki, S., & Malik, A. (2017). Phenotypic and genotypic characterization of methi cillin-resistant Staphylococcus aureus from bovine mastitis. Veterinary World, 10(3), 363–367.

Jaber, S., Weder, D., Bridy, C., Huguenin, M. C., Robert, L., Hummerjohann, J., & Stephan, R. (2015). Outbreak of staphylococcal food poisoning among children and staff at a Swiss boarding school due to soft cheese made from raw milk. Journal of Dairy Science, 98, 2944–2948.

Jaber, N. N. (2011). Isolation and biotyping of Staphylococcus aureus from white cheese in Basrah local markets. Basrah Journal of Veterinary Research, 10(2), 55–66.

Kukhtyn, M. D., Kovalenko, V. L., Pokotylo, O. S., Horyuk, Y. V., Horyuk, V. V., & Pokotylo, O. O. (2017) Staphylococcal contamination of raw milk and handmade dairy products, which are realized at the markets of Ukraine. Journal for Veterinary Medicine, Biotechnology and Biosafety, 3(1), 12–16.

Kwon, N. H., Park, K. T., Moon, J. S., Jung, W. K., Kim, S. H., Kim, J. M., Hong, S. K., Koo, H. C., Joo, Y S., & Park, Y. H. (2005). Staphylococcal cassette chromosome mec (SCC mec) characterization and molecular analysis for methicillin-resistant Staphylococcus aureus and novel SCC mec subtype IVg isolated from bovine milk in Korea. Journal of Antimicrobial Chemotherapy, 56(4), 624–632.

Lowy, F. D. (1998). Staphylococcus aureus infections. New England Journal of Medicine, 339(8), 520–532.

Macori, G., Bellio, A., Bianchi, D. M., Gallina, S., Adriano, D., Zuccon, F., Chiesa, F., Acutis, P. L., Casalinuovo, F., & Decastelli, L. (2016). Molecular typing of Staphylococcus aureus isolate responsible for staphylococcal poisoning incident in homemade food. Italian Journal of Food Safety, 5(2), 5736.

Macori, G., Giacinti, G., Bellio, A., Gallina, S., Bianchi, D. M., Sagrafoli, D., Marri, N., Giangolini, G., Amatiste, S., & Decastelli, L. (2017). Molecular epidemiology of methicillin-resistant and methicillin-susceptible Staphylo coccus aureus in the ovine dairy chain and in farm-related humans. Toxins, 9(5), 161.

Mahmmod, Y. S., Klaas, I. C., & Enevoldsen, C. (2017). DNA carryover in milk samples from routine milk recording used for PCR-based diagnosis of bovine Staphylococcus aureus mastitis. Journal of Dairy Science, 100(7), 5709–5716.

Maurin, F., Mazerolles, G., Noel, Y., & Kodjo, A. (2004). Identification and biotyping of coagulase positive staphylococci (CPS) in ripened French raw milk cheeses and their in vitro ability to produce enterotoxins. Revue de Medecine Veterinaire, 155(2), 92–96.

Mayer, S. (1999). Eingenschaften von aus Kuhmilch isolaten Staphylokokken in Hinblick auf die Beurteilung von Milch. Milchwissenschaft, 30, 607–608.

Mehli, L., Hoel, S., Thomassen, G. M. B., Jakobsen, A. N., & Karlsen, H. (2017). The prevalence, genetic diversity and antibiotic resistance of Staphylococcus aureus in milk, whey, and cheese from artisan farm dairies. International Dairy Journal, 65, 20–27.

Normanno, G. L., Salandra, A., Dambrosio, N. C., Quaglia, M., Corrente, A., Parisi, G., Santagada, A., Firinu, E., & Crisetti, G. V. (2007). Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylo coccus aureus isolated from meat and dairy products. International Journal of Food Microbiology, 115(3), 290–296.

Paterson, G. K., Harrison, E. M., & Holmes, M. A. (2014). The emergence of mecC methicillin-resistant Staphylococcus aureus. Trends in Microbio logy, 22(1), 42–47.

Sergelidis, D., & Angelidis, A. S. (2017). Methicillin resistant Staphylococcus aureus (MRSA): A controversial food borne pathogen. Letters in Applied Microbiology, 64(6), 409–418.

Thaker, H. C., Brahmbhatt, M. N., Nayak, J. B., & Thaker, H. C. (2013). Isolation and identification of Staphylococcus aureus from milk and milk products and their drug resistance patterns in Anand, Gujarat. Veterinary World, 6(1), 10–13.

Wang, S. C., Wu, C. M., Xia, S. C., Yong-Hua, Q. I., Xia, L. N., & Shen, J. Z. (2009). Distribution of superantigenic toxin genes in Staphylococcus aureus isolates from milk samples of bovine subclinical mastitis cases in two major diary production regions of China. Veterinary Microbiology, 137(3), 276–281.

Wang, X., Li, G., Xia, X., Yang, B., Xi, M., & Meng, J. (2014). Antimicrobial susceptibility and molecular typing of methicillin-resistant Staphylococcus aureus in retail foods in Shaanxi, China. Foodborne Pathogens and Disease, 11(4), 281–286.

Published
2017-08-15
How to Cite
Kukhtyn, M. D., Horyuk, Y. V., Horyuk, V. V., Yaroshenko, T. Y., Vichko, O. I., & Pokotylo, O. S. (2017). Biotype characterization of Staphylococcus aureus isolated from milk and dairy products of private production in the western regions of Ukraine. Regulatory Mechanisms in Biosystems, 8(3), 384-388. https://doi.org/10.15421/021759

Most read articles by the same author(s)