Prevalence of Methicillin-Resistant Staphylococcus aureus in Raw Hamburgers and Ready-to-Eat Sandwiches Commercialized in Supermarkets and Fast Food Outlets in Brazil
Although well known, Staphylococcus aureus is a bacterium that remains widely studied because of its high pathogenic potential and its ability to develop resistance to antibiotics routinely used in clinical practice. The present study investigated the occurrence of methicillin-resistant Staphylococcus aureus (MRSA) in hamburgers and sandwiches sold in supermarkets and fast food outlets in Salvador, BA, Brazil. Fifty samples of frozen raw hamburgers (25: beef and 25: chicken) and 50 samples of ready-to-eat sandwiches (25: beef and 25: chicken) were collected and investigated for the presence of MRSA. MRSA was present in 32% of the hamburgers and 8% of the sandwiches. The frequency of MRSA was higher in the samples containing chicken meat. However, the statistical analysis showed no association between MRSA presence and the type of meat investigated (P > 0.05). The high prevalence of MRSA in hamburgers and the presence of the microorganism in ready-to-eat sandwiches are worrying and indicate the need for better control during food preparation to prevent the spread of bacteria.
References
[1]
Fattori, F.F.A., Souza, L.C., Braoios, A., Ramos, A.P.D., Tashima, N.T., Neves, T.R.M. and Barbosa, H.R.L. (2005) Sanitary Aspects of Snacks Sold in Trailers in Presidente Prudente City, Brazil. Higiene Alimentar, 19, 54-62.
[2]
Levré, E., Valentini, P. and Chiaverini, F. (2000) Presenza di E. coli O157 verocitotossigeni inhamburger di carne bovina. Annali di Igiene, 12, 131-137.
[3]
Tavares, T.M. and Serafini, A.B. (2003) Microbiological Evaluation of Ground Beef Hamburgers Commercialized in Snack Bars in Goiânia City, Brazil. Revista de Patologia Tropical, 32, 45-52.
[4]
Normanno, G., Corrente, M., La Salandra, G., Dambrosio, A., Quaglia, N.C., Parisi, A., Greco, G., Bellacicco, A.L., Virgilio, S. and Celano, G.V. (2007) Methicillin-Resistant Staphylococcus aureus (MRSA) in Foods of Animal Origin Product in Italy. International Journal of Food Microbiology, 117, 219-222.
http://dx.doi.org/10.1016/j.ijfoodmicro.2007.04.006
Calfee, D.P. (2011) The Epidemiology, Treatment, and Prevention of Transmission of Methicillin-Resistant Staphylococcus aureus. The Art and Science of Infusion Nursing, 34, 359-364.
http://dx.doi.org/10.1097/NAN.0b013e31823061d6
[7]
Vaz, M.J.S.A.M. (1995) Characterization of Bacterial Resistance in Staphylococcus aureus. Thesis, Porto University, Porto.
[8]
Chambers, H.F. (1997) Methicillin-Resistance in Staphylococci Molecular and Biochemical Basis and Clinical Implications. Clinical Microbiology Reviews, 10, 781-791.
[9]
De Leo, F.R. and Chambers, H.F. (2009). Reemergence of Antibiotic-Resistant Staphylococcus aureus in the Genomics Era. The Journal of Clinical Investigations, 119, 2464-2474. http://dx.doi.org/10.1172/JCI38226
[10]
Sturmer, F.C.R. (2008) Partial Characterization of Ccr Element in Methicillin-Resistant Staphylococcus aureus Isolates from Southern Brazil. Dissertation, Federal University of Porto Alegre, Porto Alegre.
[11]
Kraushaar, B. and Fetsch, A. (2014) First Description of PVL-Positive Methicillin-Resistant Staphylococcus aureus (MRSA) in Wild Boar Meat. International Journal of Food Microbiology, 186, 68-73.
http://dx.doi.org/10.1016/j.ijfoodmicro.2014.06.018
[12]
De Boer, E., Zwartkruis-Nahuis, J.T.M., Wit, B., Huijsdens, X.W., de Neeling, A.J., Bosch, T., van Oosterom, R.A.A., Vila, A. and Heuvelink, A.E. (2009) Prevalence of Methicillin-Resistant Staphylococcus aureus in Meat. International Journal of Food Microbiology, 134, 52-56. http://dx.doi.org/10.1016/j.ijfoodmicro.2008.12.007
[13]
CLSI (2011) Performance Standards for Antimicrobial Susceptibility Testing. Twenty-First Informational Supplement 31, M100-S21, Clinical and Laboratory Standards Institute, Wayne.
[14]
Kitai, S., Shimizu, A., Kawano, J., Sato, E., Nakano, C., Uji, T. and Kitagawa, H. (2005) Characterization of Methicillin-Resistant Staphylococcus aureus Isolated from Retail Raw Chicken Meat in Japan. Journal of Veterinary Medical Science, 67, 107-110.
[15]
Van Loo, I., Huijsdens, X., Tiemersma, E., De Neeling, A. and Van de Sande-Bruinsma, N. (2007) Emergence of Methicillin-Resistant Staphylococcus aureus of Animal Origin in Humans. Emerging Infectious Diseases, 13, 1834-1839.
http://dx.doi.org/10.3201/eid1312.070384
Fessler, A.T., Kadlec, K., Hassel, M., Hauschild, T., Eidam, C. and Ehricht, R. (2011) Characterization of Methicillin-Resistant Staphylococcus aureus Isolates from Food and Food Products of Poultry Origin in Germany. Applied and Environmental Microbiology, 77, 7151-7157. http://dx.doi.org/10.1128/AEM.00561-11
[18]
Hanson, B.M., Dressler, A.E., Harper, A.L., Scheibel, R.P., Wardyn, S.E. and Roberts, L.K. (2011) Prevalence of Staphylococcus aureus and Methicillin-Resistant Staphylococcus aureus (MRSA) on Retail Meat in Iowa. Journal of Infection and Public Health, 4, 169-174. http://dx.doi.org/10.1016/j.jiph.2011.06.001
[19]
Agerso, Y., Hasman, H., Cavaco, L.M., Pedersen, K. and Aarestrup, F.M. (2012) Study of Methicillin Resistant Staphylococcus aureus (MRSA) in Danish Pigs at Slaughter and in Imported Retail Meat Reveals a Novel MRSA Type in Slaughter Pigs. Veterinary Microbiology, 157, 246-250. http://dx.doi.org/10.1016/j.vetmic.2011.12.023
[20]
Soares, L.S., Almeida, R.C.C., Cerqueira, E.S., Carvalho, J.S. and Nunes, I.L. (2012) Knowledge, Attitudes, and Practices in Food Safety and the Presence of Coagulase-Positive Staphylococci on Hands of Food Handlers in the Schools of Camaçari, Brazil. Food Control, 27, 206-213. http://dx.doi.org/10.1016/j.foodcont.2012.03.016
[21]
Costa, W.L.R., Ferreira, J.S., Carvalho, J.S., Cerqueira, E.S., Oliveira, L.C. and Almeida, R.C.C. (2015) Methicillin- Resistant Staphylococcus aureus in Raw Meats and Prepared Foods in Public Hospitals in Salvador, Bahia, Brazil. Journal of Food Science, 80, M147-M150. http://dx.doi.org/10.1111/1750-3841.12723
[22]
Andreotti, R. and Nicodemo, M.L.F. (2004) Use of Antimicrobials in the Cattle and Development of Resistance. EMBRAPA, Campo Grande.
[23]
Erskine, R.J., Walker, R.D., Bolin, C.A., Bartlett, P.C. and White, D.G. (2002) Trends in Antibacterial Susceptibility of Mastitis Pathogens during a Seven-Year Period. Journal of Dairy Science, 85, 1111-1118.
http://dx.doi.org/10.3168/jds.S0022-0302(02)74172-6
[24]
Lin, G., Wu, C., Wang, X. and Meng, J. (2015) Prevalence and Characterization of Methicillin Susceptible Staphylococcus aureus ST398 Isolates from Retail Foods. International Journal of Food Microbiology, 196, 94-97.
http://dx.doi.org/10.1016/j.ijfoodmicro.2014.12.002
[25]
Hososaka, Y., Hanaki, H., Endo, H., Suzuki, Y., Nagasawa, Z., Otsuka, Y., Nakae, T. and Sunakawa, K. (2007) Characterization of Oxacillin-Susceptible mecA-Positive Staphylococcus aureus: A New Type of MRSA. Journal of Infection and Chemotherapy, 13, 79-86. http://dx.doi.org/10.1007/s10156-006-0502-7
[26]
Shahraz, F., Dadkhah, H., Khaksar, R., Mahmoudzadeh, M., Hosseini, H. and Kamran, M. (2012) Analysis of Antibiotic Resistance Patterns and Detection of mecA Gene in Staphylococcus aureus Isolated from Packaged Hamburger. Meat Science, 90, 759-763. http://dx.doi.org/10.1016/j.meatsci.2011.11.009