DETECTION OF ENTEROTOXIN GENES OF Staphylococcus aureus ISOLATES FROM FOOD CONTACT SURFACES IN THE DAIRY INDUSTRY OF JALISCO, MEXICO
Staphylococcus aureus is widely distributed in nature, and two of the main sources of S. aureus contamination in the food industry are food handlers and Food Contact Surfaces (FCS). This pathogen is responsible for outbreaks of foodborne illnesses associated with the consumption of milk and dairy products. The aim of this study was to determine the prevalence of toxin-encoding genes in S. aureus isolates from FCS in the Jalisco dairy industry. The presence of enterotoxin genes was investigated by PCR. In this study, we identify 84 S. aureus isolates. Overall, 35.7% of the isolates tested positive for at least one of the nine studied enterotoxin genes, and 15.4% harbored 2-4 enterotoxin genes. The most predominant genes were sej and sed. This study demonstrates that FCS are a source of contamination for this food rotation and that there is a diversity of enterotoxin genes in S. aureus isolates. Therefore, vigilant food safety practices need to be implemented regarding FCS to prevent foodborne infections and intoxications due to S. aureus contamination.
Antoci, E., Pinzone, M.R., Nunnari, G., Stefani, S. and Cacopardo, B. 2013. Prevalence and molecular characteristic of methicillinresistant Staphylococcus aureus (MRSA) among subjects working on bovine dairy farms. Le Infezioni in Medicina. 21: 125-129.
Argudín, M.A., Mendoza, M.C. and Rodicio, M.R. 2010. Food poisoning and Staphylococcus aureus enterotoxins. Toxins. 2: 1751-1773.
Borelli, B.M., Lacerda, I.C.A., Brandao, L.R., Vianna, C.R., Ferreira, M.C., Gomes, F.C.O., Carmo, L.S., Heneine, L.G.D. and Rosa, C.A. 2011. Identification of Staphylococcus spp. isolated during the ripening process of a traditional Minas cheese. Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 63:481-487.
Brakstad, O.D., Aasbakk, K. and Maeland, J.A. 1992. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. Journal of Clinical Microbiology. 30: 1654-1660.
Brooks, J.D. and Flint, S.H. 2008. Biofilms in the food industry: problems and potential solutions. International Journal of Food Science + Technology. 43: 2163-2176.
Chen, Y.H., Jackson, K.M., Chea, F.P. and Schaffner, D.W. 2001. Quantification and variability analysis of bacterial cross-contamination rates in common food service tasks. Journal of Food Protection. 64: 72-80.
Djekic, I., Kuzmanovic, J., Andelkovic, A., Saracevic, M., Stojanovic, M.M. and Tomasevic, I. 2016. Relationships among hygiene indicators in take-away foodservice establishments and the impact of climatic conditions. Journal of Applied Microbiology. 121: 863-872.
FDA (Food and Drug Administration). 2016. Bacteriological Analytical Manual. USA: AOAC INTERNATIONAL.
Fisher, A., Francois, P., Holtfreter, S., Broeker, B. and Schrenzel, J. 2009. Development and evaluation of a rapid strategy to determine enterotoxin gene content in Staphylococcus aureus. Journal of Microbiological Methods. 77: 184-190.
Gucukoglu, A., Kevenk, T.O., Uyanik, T., Cadirci, O., Terzi, G. and Alisarli, M. 2012. Detection of enterotoxigenic Staphylococcus aureus in raw milk and dairy products by multiplex PCR. Journal of Food Science. 77: M620-M623.
Gutiérrez, D., Delgado, S., Vázquez-Sánchez, D., Martínez, B., Cabo, M.L., Rodríguez, A., Herrera, J.J. and García, P. 2012. Incidence of Staphylococcus aureus and analysis of associated bacterial communities on food industry surfaces. Applied and Environmental Microbiology. 78: 8547-8554.
Jarraud, S., Peyrat, M.A., Lim, A., Tristan, A., Bes, M., Mougel, C., Etienne, J., Vandenesch, F., Bonneville, M. and Lina, G. 2001. egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. The Journal of Immunology. 166: 669-677.
Le Loir, Y., Baron, F. and Gautier, M. 2003. Staphylococcus aureus and food poisoning. Genetics and Molecular Research. 2:63-76.
Lindsay, D. and von Holy, A. 2006. Bacterial biofilms within the clinical setting: what healthcare professionals should know. Journal of Hospital Infection. 64: 313-325.
Marino, M., Frigo, F., Bartolomeoil, I. and Maifreni, M. 2011. Safety-related proprieties staphylococci isolated from food and food environments. Journal of Applied Microbiology. 110: 550-561.
Marques, S.C., Silva-Rezende, J.G., de Freitas-Alves, L.A., Cássia- Silva, B., Alves, E., de Abreu, L.R. and Hilsdorf-Piccoli, R. 2007. Formation of biofilms by Staphylococcus aureus on stainless steel and glass surfaces and its resistance to some selected chemical sanitizers. Brazilian Journal of Microbiology. 38:538-543.
Moghassem-Hamidi, R., Hosseinzadeh, S., Shekarforoush, S.S., Poormontaseri, M. and Derakhshandeh A. 2015. Association between the enterotoxin production and presence of coa, nuc genes among Staphylococcus aureus isolated from various sources, in Shiraz. Iranian Journal of Veterinary Research. 16: 381-384.
Monday, S.R. and Bohach, G.A. 1999. Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. Journal of Clinical Microbiology. 37:3411-3414.
Moore, G. and Griffith, C. 2002. A comparison of traditional and recently developed methods for monitoring surface hygiene within the food industry: an industry trial. International Journal of Environmental Health Research. 12: 317-329.
Normanno, G., La Salandra, G., Dambrosio, A., Quaglia, N.C., Corrente, M., Parisi, A., Santagada, G., Firinu, A., Crisetti, E. and 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: 290-296.
Pu, S., Wang, F. and Ge, B. 2011. Characterization of toxin genes and antimicrobial susceptibility of Staphylococcus aureus isolates from Louisiana retail meats. Foodborne Pathogens and Disease. 8: 299-306.
Rahimi, E. 2013. Enterotoxigenicity of Staphylococcus aureus isolated from traditional and commercial dairy products marketed in Iran. Brazilian Journal of Microbiology. 44: 393-399.
Rong, D., Wu, Q., Xu, M., Zhang, J. and Yu, S. 2017. Prevalence, virulence genes, antimicrobial susceptibility, and genetic diversity of Staphylococcus aureus from retail aquatic products in China. Frontiers in Microbiology. 8:714.
Salgado-Ruiz, T.B., Rodríguez-González, A., Gutiérrez, D., Martínez-Fernández, B., García-Suárez, M.P., Espinoza-Ortega, A., Martínez Campos, A.R., Lagunas-Bernabé, S., Vicente, F. and Arriga-Jordán, C.M. 2015. Molecular characterization and antimicrobial susceptibility of Staphylococcus aureus from small-scale dairy systems in the highlands of Central México. Dairy Science & Technology. 95: 181-196.
Sato’o, Y., Omoe, K., Naito, I., Ono, H.K., Nakane, A., Sugai, M., Yamagishi, N. and Hu, D.L. 2014. Molecular epidemiology and identification of a Staphylococcus aureus clone causing food poisoning outbreaks in Japan. Journal of Clinical Microbiology. 52: 2637-2640.
Schlisselberg, D.B. and Yaron, S. 2013. The effects of stainless steel finish on Salmonella typhimurium attachment, biofilm formation and sensitivity to chlorine. Food Microbiology. 35:65–72.
Seo, K.S. and Bohach, G.A. 2007. Staphylococcus aureus. En: Food Microbiology: Fundamentals and Frontiers. M.P. Doyle y L.R. Beuchat (ed.), pp 493-518. ASM Press. Washington, USA. Shi, X. and Zhu, X. 2009. Biofilm formation and food safety in food industries. Trends in Food Science & Technology. 20:407-413.
Soares, J.C., Marques, M.R., Tavaria, F.K., Pereira, J.O., Malcata, X. and Pintado, M.M. 2011. Biodiversity and characterization of Staphylococcus species isolated from a small manufacturing dairy plant in Portugal. International Journal of Food Microbiology. 146: 123-129.
Sospedra, I., Mañes, J. and Soriano, J.M. 2012. Report of toxic shock syndrome toxin 1 (TSST-1) from Staphylococcus aureus isolated in food handlers and surfaces from foodservice establishments. Ecotoxicology and Environmental Safety. 80: 288-290.
Straub, J.A., Hertel, C. and Hammens, W.P. 1999. A 23S rDNAtargeted polymerase chain reaction-based system for detection of Staphylococcus aureus in meat starter cultures and dairy products. Journal of Food Protection. 62: 1150-1156.
Tang, J., Tang, C., Chen, J., Du, Y., Yang, X.N., Wang, C., Zhang, H. and Yue, H. 2011. Phenotypic characterization and prevalence of enterotoxin genes in Staphylococcus aureus isolates from outbreaks of illness in Chengdu City. Foodborne Pathogen and Disease. 8: 1317-1320.
Torres-Vitela, M.R., Mendoza-Bernardo, M., Castro-Rosas, J., Gomez-Aldapa, C.A., Garay-Martinez, L.E., Navarro-Hidalgo, V. and Villarruel-López A. 2012. Incidence of Salmonella, Listeria monocytogenes, Escherichia coli O157:H7 and staphylococcal enterotoxin in two types of Mexican fresh cheeses. Journal of Food Protection. 75: 79-84.
Van Houdt, R. and Michiels, C.W. 2010. Biofilm formation and the food industry, a focus on the bacterial outer surface. Journal of Applied Microbiology. 109: 1117-1131.
Zouharova, M. and Rysanek, D. 2008. Multiplex PCR and RPLA identification of Staphylococcus aureus enterotoxigenic strains from bulk tank milk. Zoonoses and Public Health. 55:313-319.