Characteristics of antibiotic sensitivity of Staphylococcus aureus isolated from dairy farms in Ukraine
AbstractStaphylococcus aureus is one of the most important microorganism in the process of raw milk production and has significance for people’s health as it causes dangerous microbial contamination of dairy production. Furthermore, raw milk and the environment of livestock farms may be potential vehicles for distribution of antibiotic-resistant strains of S. aureus. The aim of the present study was to establish antibiotic sensitivity profiles of S. aureus depending on its origin from dairy farms, with a special focus on methicillin-resistant isolates. A total of 165 samples were collected for investigation in the period 2014–2016 from 5 dairy farms in Ukraine. All samples were analyzed for the presence of S. aureus using the Baird Parker Agar with Egg Yolk Tellurite Emulsion. Typical staphylococcal colonies were examined morphologically and for presence of coagulase and hemolysin activities. From these, positive samples for S. aureus were 62 (37.6%): 4 (6.5%) raw milk, 17 (77.4%) swabs of udder skin, 18 (29.0%) milk from cows with subclinical mastitis and 21 (33.9%) environmental samples. The standard disk diffusion method was used to determine sensitivity of S. aureus isolates to 10 antibiotics. The antimicrobial sensitivity profiles of S. aureus isolates showed differences between them, which depends on the origin of the isolates. Our results demonstrated that most of S. aureus isolates were resistant to penicillin, oxacillin and vancomycin. Of the 62 S.aureus isolates, 20 (32.3%) and 5 (8.1%) were found to be multiresistant to 3 different antibiotics, 6 (9.8%) isolates to 4 antibiotics, 12 (19.4%) and 3 (4.8%) to 5 antibiotics (P10, OX1, VA5, L10, TE30 and P10, OX1, VA5, CIP10, TE30 respectively). All isolates resistant to penicillin and oxacillin were typed by mec A gene in PCR with two primers (MecA147-F and MecA147-R). The results show that 66.7% of these isolates yielded a mecA product. The information obtained from this study is useful for understanding the prevalence of S. aureus and its antibiotic sensitivity in dairy farms and can be useful for local and national monitoring or for designing specific control programs of methicillin- and multiresistance isolates present in the food chain of milk production.
Abebe, R., Hatiya, H., Abera, M., Megersa, B., & Asmare, K. (2016). Bovine mastitis: Prevalence, risk factors and isolation of Staphylococcus aureus in dairy herds at Hawassa milk shed. South Ethiopia. BMC Veterinary Research, 12, 270–279.
Al-Ashmawy, M. A., Sallam, K. I., Abd-Elghany, S. M., Elhadidy, M., & Tamura, T. (2016). Prevalence, molecular characterization, and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus isolated from milk and dairy products. Foodborne Pathogens and Disease, 13(3), 156–162.
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.
Bhunia, A. K. (2008). Foodborne microbial pathogens: Mechanisms and pathogenesis. Springer Science + Business Media, NY, USA.
Brennan, G. I., Abbott, Y., Burn, A., Leonard, F., McManus, B. A., O’Connell, B., Coleman, D. C., & Shore, A. C. (2016). The emergence and spread of multiple livestock-associated clonal complex 398 methicillin-resistant and methicillin-susceptible Staphylococcus aureus strains among animals and humans in the Republic of Ireland, 2010–2014. PLoS One, 11, 1–11.
Carfora, V., Caprioli, A., Marri, N., Sagrafoli, D., Boselli, C., Giacinti, G., Sorbara, 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.
Deurenberg, R. H., Vink, C., Kalenic, S., Friderich, A. W., Bruggeman, C. A., & Stobberingh, E. E. (2007). The molecular evolution of methicillin-resistant Staphylococcus aureus. Clinical Microbiology and Infection, 13, 222–235.
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.
Ganai, A. W., Kotwal, S. K., Wani, N., Malik, M. A., Jeelani, R., Kour, S., & Zargar, R. (2016). Detection of mecA gene of methicillin resistant Staphylococcus aureus by PCR assay from raw milk. Indian Journal of Animal Sciences, 86(5), 508–511.
Gopal, S., & Divya, K. C. (2017). Can methicillin-resistant Staphylococcus aureus prevalence from dairy cows in India act as potential risk for community-associated infections?: A review. Veterinary World, 10(3), 311–318.
Hamid, S., Bhat, M. A., Mir, I. A., Taku, A., Badroo, G. A., Nazki, S., & Malik, A. (2017). Phenotypic and genotypic characterization of methicillin-resistant Staphylococcus aureus from bovine mastitis. Veterinary World, 10(3), 363–367.
İkiz, S., Basaran, B., Bingol, E. B., Çetin, Ö., Kasikci, G., Özgur, N. Y., Ucmak, M., Yilmaz, Ö., Gunduz, M. C., & Sabuncu, A. (2013). Presence and antibiotic susceptibility patterns of contagious mastitis agents (Staphylococcus aureus and Streptococcus agalactiae) isolated from milks of dairy cows with subclinical mastitis. Turkish Journal of Veterinary and Animal Sciences, 37, 569–574.
Jihasz-Kaszanytzky, E., Janosi, S., Somogyi, P., Dan, A., Van Der Graaf-Van Bloois, L., Van Duijkeren, E., & Wangenaar, J. A. (2007). MRSA transmission between cows and humans. Emerging Infectious Diseases,13, 630–632.
Keefe, G. (2012). Update on control of Staphylococcus aureus and Streptococcus agalactiae for management of mastitis. Veterinary Clinics of North America: Food Animal Practice, 28, 203–216.
Kirmusaoglu, S. (2017). MRSA and MSSA: The mechanism of methicillin resistance and the influence of methicillin resistance on biofilm phenotype of Staphylococcus aureus. In: The rise of virulence and antibiotic resistance in Staphylococcus aureus. InTech.
Kukhtyn, M. D., Berhilevych, O. M., Kravcheniuk, K., Shynkaruk, O., Horyuk, Y. V., & Semaniuk, N. (2017). Formation of biofilms on dairy equipment and the influence of disinfectants on them. Eastern-European Journal of Eenterprise Technologies, 89, 26–33.
Kukhtyn, M. D., Horyuk, Y. V., Horyuk, V. V., Yaroshenko, T. Y., Vichko, O. I., & Pokotylo, O. S. (2017). Biotype characterization of Staphylococcus aureus from milk and dairy products of private production in the western regions of Ukraine. Regulatory Mechanisms in Biosystems, 8(3), 384–388.
Li, J., Zhou, H., Yuan, L., He, T., & Hu, S. (2009). Prevalence, genetic diversity, and antimicrobial susceptibility profiles of Staphylococcus aureus isolated from bovine mastitis in Zhejiang Province, China. Journal of Zheijang University SCIENCE B (Biomedicine & Biotechnology), 10(10), 753–760.
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., Salandra, G. L., Dambrosio, A., Quaglia, N. C., Corrente, M., Parisi, A., Santagada, G., Firinu, A., Crisetti, E., & Celano, G. V. (2007). Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. International Journal of Food Microbiology, 115(3), 290–296.
Performance standards for antimicrobial disk susceptibility tests (2012). Approved Standard, CLSI, USA.
Pu, W., Su, Y., Li, J., Li, C., Yang, Z., Deng, H., & Ni, C. (2014). High incidence of oxacillin-susceptible mecA-positive Staphylococcus aureus (OS-MRSA) associated with bovine mastitis in China. PLoS One, 9(2), 88–134.
Rahim, A., Rachman, A., Suhaili, Z., & Desa, M. N. (2017). The evolution and dissemination of methicillin resistance determinant in Staphylococcus aureus. In: The rise of virulence and antibiotic resistance in Staphylococcus aureus. InTech.
Sergelidis, D., & Angelidis, A. S. (2017). Methicillin resistant Staphylococcus aureus (MRSA): A controversial food borne pathogen. Letters in Applied Microbiology, 64(6), 409–418.
Szweda, P., Schielmann, M., Frankowska, A., Kot, B., & Zalewska, M. (2014). Antibiotic resistance in Staphylococcus aureus strains isolated from cows with mastitis in Eastern Poland and analysis of susceptibility of resistant strains to alternative nonantibiotic agents: Lysostaphin, nisin and polymyxin B. Journal of Veterinary Medical Science, 76(3), 355–362.
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, 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.
Zhang, K., & McClure, J.-A. (2005). Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec Types I to V in methicillin-resistant Staphylococcus aureus. Journal of Clinical Microbiology, 43(10), 5026–5033.
Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons «Attribution» 4.0 License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.