The occurrence of methicillin-resistant staphylococci was investigated in fresh seafood, seafood products and related samples. Staphylococci were isolated from 13 (68.42%) fresh seafood samples, while 3 (15.78%) samples harbored coagulase-positive S. aureus. Resistance to methicillin was observed in 16 isolates of Staphylococcus spp., 15 of which were coagulase-negative S. aureus (MR-CoNS) and one was a coagulase-positive S. aureus (MRSA). The mecA gene is detected by PCR in 10 MR-CoNS and one MRSA strain. The lmrS gene, which codes for a multidrug efflux pump LmrS, is detected only in coagulase-positive isolates.
Genigeorgis, C.A. (1989) Present State of Knowledge on Staphylococcal Intoxication. International Journal of Food Microbiology, 9, 327-360. http://dx.doi.org/10.1016/0168-1605(89)90100-1
Zhang, S., Landolo, J. and Stewart, C. (1998) The Enterotoxin D Plasmid of Staphylococcus aureus Encodes a Second Enterotoxin Determinant (sej). FEMS Microbiology Letters, 168, 227-233. http://dx.doi.org/10.1111/j.1574-6968.1998.tb13278.x
Holden, M.T., Feil, E.J., Lindsay, J.A., Peacock, S.J., Day, N.P.J., Enright, M.C., Foster, T.J., et al. (2004) Complete Genomes of Two Clinical Staphylococcus aureus Strains: Evidence for the Rapid Evolution of Virulence and Drug Resistance. Proceedings of the National Academy of Sciences of the United States of America, 101, 9786-9791. http://dx.doi.org/10.1073/pnas.0402521101
Lowy, F.D. (1998) Staphylococcus aureus Infections. The New England Journal of Medicine, 339, 520-532. http://dx.doi.org/10.1056/NEJM199808203390806
Waldvogel, F.A. (2000) Staphylococcus aureus (Including Staphylococcal Toxic Shock). In: Mandell, G.L., Bennett, J. E. and Dolin, R., Eds., Principles and Practice of Infectious Diseases, Churchill Livingstone, Philadelphia, 2069-2092.
Chambers, H.F. (2005) Community-Associated MRSA—Resistance and Virulence Converge. The New England Journal of Medicine, 352, 1485-1487. http://dx.doi.org/10.1056/NEJMe058023
Farrell, D.J. (1997) The Reliability of MicroscanTM Conventional and Rapid Panels to Identify Staphylococcus aureus and Detect Methicillin Resistance: An Evaluation Using the Tube Coagulase Test and mecA PCR. Pathology, 29, 406-410. http://dx.doi.org/10.1080/00313029700169405
Lee, J.H. (2003) Methicillin (Oxacillin)-Resistant Staphylococcus aureus Strains Isolated from Major Food Animals and Their Potential Transmission to Humans. Applied and Environmental Microbiology, 69, 6489-6494. http://dx.doi.org/10.1128/AEM.69.11.6489-6494.2003
Boost, M.V., Wong, A., Ho, J. and O’Donoghue, M. (2013) Isolation of Methicillin-Resistant Staphylococcus aureus (MRSA) from Retail Meats in Hong Kong. Foodborne Pathogens and Disease, 10, 705-710. http://dx.doi.org/10.1089/fpd.2012.1415
O’Brien, A.M., Hanson, B.M., Farina, S.A., Wu, J.Y., Simmering, J.E., Wardyn, S.E., Forshey, B.M., Kulick, M.E., Wallinga, D.B. and Smith, T.C. (2012) MRSA in Conventional and Alternative Retail Pork Products. PLoS ONE, 7, e30092. http://dx.doi.org/10.1371/journal.pone.0030092
Haran, K.P., Godden, S.M., Boxrud, D., Jawahir, S., Bender, J.B. and Sreevatsan, S. (2012) Prevalence and Characterization of Staphylococcus aureus, including Methicillin-Resistant Staphylococcus aureus, Isolated from Bulk Tank Milk from Minnesota Dairy Farms. Journal of Clinical Microbiology, 50, 688-695. http://dx.doi.org/10.1128/JCM.05214-11
Wendlandt, S., Kadlec, K., FeBler, A.T., Monecke, S., Ehricht, R., van de Giessen, A.W., Hengeveld, P.D., Huijsdens, X., Schwarz, S. and van Duijkeren, E. (2013) Resistance Phenotypes and Genotypes of Methicillin-Resistant Staphylococcus aureus Isolates from Broiler Chickens at Slaughter and Abattoir Workers. Journal of Antimicrobial Chemotherapy, 68, 2458-2463. http://dx.doi.org/10.1093/jac/dkt239
Kock, R., Schaumburg, F., Mellmann, A., Koksal, M., Jurke, A., Becker, K. and Friedrich, A.W. (2013) Livestock Associated Methicillin-Resistant Staphylococcus aureus (MRSA) as Causes of Human Infection and Colonization in Germany. PLoS ONE, 8, e55040. http://dx.doi.org/10.1371/journal.pone.0055040
Voss, A., Loeffen, F., Bakker, J., Klaassen, C. and Wulf, M. (2005) Methicillin-Resistant Staphylococcus aureus in Pig Farming. Emerging Infectious Diseases, 11, 1965-1966. http://dx.doi.org/10.3201/eid1112.050428
Huss, H.H. (1988) Fresh Fish Quality and Quality Changes. FAO Fisheries Series, No. 29, FAO, Rome.
Bryan, F.L. (1980) Foodborne Diseases in the United States Associated with Meat and Poultry. Journal of Food Protection, 43, 140-150.
Beleneva, I.A. (2011) Incidence and Characteristics of Staphylococcus aureus and Listeria monocytogenes from the Japan and South China Seas. Marine Pollution Bulletin, 62, 382-387. http://dx.doi.org/10.1016/j.marpolbul.2010.09.024
Hammad, A.M., Watanbe, W., Fujii, T. and Shimamoto, T. (2012) Occurrence and Characteristics of Methicillin Resistant and -Susceptible Staphylococcus aureus and Methicillin-Resistant Coagulase-Negative Staphylococci from Japanese Retail Ready-to-Eat Raw Fish. International Journal of Food Microbiology, 156, 286-289. http://dx.doi.org/10.1016/j.ijfoodmicro.2012.03.022
Vázquez-Sánchez, D., López-Cabo, M., Saá-Ibusquiza, P. and Rodríguez-Herrera, J.J. (2012) Incidence and Characterization of Staphylococcus aureus in Fishery Products Marketed in Galicia Northwest Spain. International Journal of Food Microbiology, 157, 286-296. http://dx.doi.org/10.1016/j.ijfoodmicro.2012.05.021
Atyah, M.A., Zamri-Saad, M. and Siti-Zahrah, A. (2010) First Report of Methicillin-Resistant Staphylococcus aureus from Cage-Cultured Tilapia (Oreochromis niloticus). Veterinary Microbiology, 144, 502-504. http://dx.doi.org/10.1016/j.vetmic.2010.02.004
FDA (Food and Drug Administration) (2004) Bacteriological Analytical Manual on Line. 8th Edition, Revision A, 1998 (Online). AOAC International, Arlington.
CLSI (2008) Performance Standards for Antimicrobial Susceptibility Testing. 15th Informational Supplement, M100-S15, Clinical and Laboratory Standards Institute, Wayne.
Brakstad, O.G., Aasbakk, K. and Macland, J.A. (1992) Detection of Staphylococcus aureus by Polymerase Chain Reaction Amplification of nuc Gene. Journal of Clinical Microbiology, 30, 1654-1660.
Oliveira, D.C. and de Lencastre, H. (2002) Multiplex PCR Strategy for Rapid Identification of Structural Types and Variants of the mec Element in Methicillin-Resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 46, 2155-2161. http://dx.doi.org/10.1128/AAC.46.7.2155-2161.2002
Xu, B., Liu, L. Liu, L., Li, X.P., Li, X.F. and Wang, X. (2012) A Multiplex PCR Assay for the Rapid and Sensitive Detection of Methicillin-Resistant Staphylococcus aureus and Simultaneous Discrimination of Staphylococcus aureus from Coagulase-Negative Staphylococci. Journal of Food Science, 77, 638-642. http://dx.doi.org/10.1111/j.1750-3841.2012.02959.x
Abrahim, A., Sergelidis, D., Kirkoudis, I., Anagnostou, V., Kaitsa-Tsiopoulou, E., Kazila, P. and Papa, A. (2010) Isolation and Antimicrobial Resistance of Staphylococcus spp. in Freshwater Fish and Greek Marketplaces. Journal of Aquatic Food Product Technology, 19, 93-102. http://dx.doi.org/10.1080/10498850.2010.491597
Ayulo, A.M.R., Machado, R.A. and Scussel, V.M. (1994) Enterotoxigenic Escherichia coli and Staphylococcus aureus in Fish and Seafood from the Southern Region of Brazil. International Journal of Food Microbiology, 24, 171-178. http://dx.doi.org/10.1016/0168-1605(94)90116-3
Herrera, F.C., Santos, J.A., Otero, A. and García-López, M.-L. (2006) Occurrence of Foodborne Pathogenic Bacteria in Retail Prepackaged portions of Marine Fish in Spain. Journal of Applied Microbiology, 100, 527-536. http://dx.doi.org/10.1111/j.1365-2672.2005.02848.x
Oh, S.K., Lee, N., Cho, Y.S., Shin, D.B., Choi, S.Y. and Koo, M. (2007) Occurrence of Toxigenic Staphylococcus aureus in Ready-to-Eat Food in Korea. Journal of Food Protection, 70, 1153-1158
Rodma, P., Satjapala, T. and Suwanvitaya, P. (1991) Staphylococcus aureus Occurrence in Frozen Foods. Food, 21, 197-204.
Sokari, T. (1991) Distribution of Enterotoxigenic Staphylococcus aureus in Ready-to-Eat Foods in Eastern Nigeria. International Journal of Food Microbiology, 12, 275-279. http://dx.doi.org/10.1016/0168-1605(91)90079-5
Simon, S.S. and Sanjeev, S. (2007) Prevalence of Enterotoxigenic Staphylococcus aureus in Fishery Products and Fish Processing Factory Workers. Food Control, 18, 1565-1568. http://dx.doi.org/10.1016/j.foodcont.2006.12.007
Normanno, G., Firinu, A., Virgilio, S., Mula, G., Dambrosio, A., Poggiu, A., Decastelli, L., Mioni, R., Sucuota, S., Bolzoni, G., Di Giannatale, E., Salinetti, A.P., La Salandra, G., Bartoli, M., Zuccon, F., Pirino, T., Sias, S., Parisi, A., Quaglia, N.C. and Celano, G.V. (2005) Coagulase-Positive Staphylococci and Staphylococcus aureus in Foods Products Marketed in Italy. International Journal of Food Microbiology, 98, 73-79. http://dx.doi.org/10.1016/j.ijfoodmicro.2004.05.008
Zarei, M., Maktabi, S. and Ghorbanpour, M. (2012) Prevalence of Listeria monocytogenes, Vibrio parahaemolyticus, Staphylococcus aureus, and Salmonella spp. in Seafood Products Using Multiplex Polymerase Chain Reaction. Foodborne Pathogens and Disease, 9, 108-112. http://dx.doi.org/10.1089/fpd.2011.0989
Hansen, L., Gill, T., Truelstrup, T. and Hussa, H.H. (1995) Effects of Salt and Storage Temperature on Chemical, Microbiological and Sensory Changes in Cold-Smoked Salmon. Food Research International, 28, 123-130. http://dx.doi.org/10.1016/0963-9969(95)90795-C
Vilhelmsson, O., Hafsteinsson, H. and Kristjansson, J.K. (1997) Extremely Halotolerant Bacteria Characteristic of Fully Cured and Dried Cod. International Journal of Food Microbiology, 36, 163-170. http://dx.doi.org/10.1016/S0168-1605(97)01256-7
Siriken, B., Yildirim, T., Erol, I., Durupinar, B., Ciftci, A. and Onuk, E.E. (2013) Prevalence and Characterization of Coagulase Positive Staphylococci Isolated from Salted Anchovy. Journal of Aquatic Food Product Technology, 22, 339-352. http://dx.doi.org/10.1080/10498850.2011.651773
Basti, A.A., Misaghi, A., Salehi, T.Z. and Kamkar, A. (2006) Bacterial Pathogens in Fresh, Smoked and Salted Iranian Fish. Food Control, 17, 183-188. http://dx.doi.org/10.1016/j.foodcont.2004.10.001
Jay, J.M., Loessner, M.J. and Golden, D.A. (2005) Modern Food Microbiology. 7th Edition, Springer, New York.
Arkoudelos, J.S., Samaras, F.J. and Tassou, C.C. (2003) Survival of Staphylococcus aureus and Salmonella enteritidis on Salted Sardines (Sardinapilchardus) during Ripening. Journal of Food Protection, 66, 1479-1481
Vannuffel, P., Gigi, J., Ezzedine, H., Vandercam, B., Delmee, M., Wauters, G. and Gala, J.L. (1995) Specific Detection of Methicillin-Resistant Staphylococcus Species by Multiplex PCR. Journal of Clinical Microbiology, 33, 2864-2867.
Barbier, F., Ruppé, E., Hernandez, D., Lebeaux, D., Francois, P., Felix, B., Desprez, A., Maiga, A., Woerther, P.L., Gaillard, K., Jeanrot, C., Wolff, M., Schrenzel, J., Andremont, A. and Ruimy, R. (2010) Methicillin-Resistant Coagulase-Negative Staphylococci in the Community: High Homology of SCCmecIVa between Staphylococcus epidermidis and Major Clones of Methicillin-Resistant Staphylococcus aureus. The Journal of Infectious Diseases, 202, 270-281. http://dx.doi.org/10.1086/653483
Morgan, M. (2008) Methicillin-Resistant Staphylococcus aureus and Animals: Zoonosis or Humanosis? Journal of Antimicrobial Chemotherapy, 62, 1181-1187. http://dx.doi.org/10.1093/jac/dkn405
García-álvarez, L., Holden, M.T., Lindsay, H., Webb, C.R., Brown, D.F., Curran, M.D., Walpole, E., Brooks, K., Pickard, D.J., Teale, C., Parkhill, J., Bentley, S.D., Edwards, G.F., Girvan, E.K., Kearns, A.M., Pichon, B., Hill, R.L., Larsen, A.R., Skov, R.L., Peacock, S.J., Maskell, D.J. and Holmes, M.A. (2011) Methicillin-Resistant Staphylococcus aureus with a Novel mecA Homologue in Human and Bovine Populations in the UK and Denmark: A Descriptive Study. The Lancet Infectious Diseases, 11, 595-603. http://dx.doi.org/10.1016/S1473-3099(11)70126-8
Suzuki, E., Hiramatsu, K. and Yokota, T. (1992) Survey of Methicillin-Resistant Clinical Strains of Coagulase Negative Staphylococci for mecA Gene Distribution. Antimicrobial Agents and Chemotherapy, 36, 429-434. http://dx.doi.org/10.1128/AAC.36.2.429
Banerjee, R., Gretes, M., Harlem, C., Basuino, L. and Chambers, H.F. (2010) AmecA-Negative Strain of Methicillin-Resistant Staphylococcus aureus with High-Level β-Lactam Resistance Contains Mutations in Three Genes. Antimicrobial Agents and Chemotherapy, 54, 4900-4902. http://dx.doi.org/10.1128/AAC.00594-10
Duran, N., Ozer, B., Duran, G.G., Onlen, Y. and Demir, C. (2012) Antibiotic Resistance Genes and Susceptibility Patterns in Staphylococci. Indian Journal of Medical Research, 135, 389-396
Rhee, C.H. and Woo, G.J. (2010) Emergence and Characterization of Foodborne Methicillin-Resistant Staphylococcus aureus in Korea. Journal of Food Protection, 73, 2285-2290.
Kumar, S. and Varela, M.F. (2012) Biochemistry of Bacterial Multidrug Efflux Pumps. International Journal of Molecular Sciences, 13, 4484-4495. http://dx.doi.org/10.3390/ijms13044484
Piddock, L.J. (2006) Multidrug-Resistance Efflux Pumps? Not Just for Resistance. Nature Reviews Microbiology, 4, 629-636. http://dx.doi.org/10.1038/nrmicro1464
Floyd, J.L., Smith, K.P., Floyd, J.T., Kumar, S. and Manuel, F.V. (2010) LmrS Is a Multidrug Efflux Pump of the Major Facilitator Superfamily from Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 54, 5406-5412. http://dx.doi.org/10.1128/AAC.00580-10