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  • 1 Shahid Beheshti University of Medical Sciences Research Centers for Gastroenterology and Liver Diseases, School of Medicine Tehran Iran
  • | 2 Islamic Azad University Department of Theriogenology, Faculty of Specialized Veterinary Sciences, Science and Research Branch Tehran Iran
  • | 3 Shahid Beheshti University of Medical Sciences Department of Microbiology, School of Medicine Tehran Iran
  • | 4 Ilam University of Medical Sciences Department of Microbiology, School of Medicine Ilam Iran
  • | 5 Tehran University of Medical Sciences Department of Microbiology, School of Medicine Tehran Iran
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Staphylococcus aureus is considered one of the most important food borne pathogens.A total of 111 isolates of S. aureus were cultured from raw milk samples during January 2009 to June 2009 from Tehran and Mashhad. The coagulase gene polymorphism and the prevalence of classical enterotoxin genes of S. aureus strains were determined by PCR-RFLP (restriction fragment length polymorphism) and Multiplex-PCR. Disk diffusion method was used to determine the susceptibility of isolates to antimicrobial agents as instructed by Clinical and Laboratory Standards Institute.Sixty-seven % of the isolates harboured one or more enterotoxin genes. The most prevalent gene was sec, found in 59 % of the isolates. Approximately 8% of the isolates were positive for sea, seb and sed genes. Only one isolate had see gene. The rate of coexistence of enterotoxin genes was 14%. All S. aureus isolates were susceptible to ciprofloxacin, gentamicin, imipenem, minocycline, oxacillin and vancomycin. They were resistant to ampicillin (64%), penicillin (56%), clindamycin (22%), tetracycline (22%), doxycycline (19%), teicoplanin (13%), rifampin (2%) and trimethoprim-sulfamethoxazole (2%). On the basis of coagulase gene analysis of 111 S. aureus isolates, the PCR products of 56 isolates were digested with Alu I that produced three distinct patterns.These data indicate the high prevalence of enterotoxigenic S. aureus in raw bovine milk in Tehran and Mashhad, and highlight the importance of proper quality control of dairy products for public health.

  • Katsuda, K., Hata, E., Kobayashi, H., Kohmoto, M., Kawashima, K., Tsunemitsu, H. et al.: Molecular typing of Staphylococcus aureus isolated from bovine mastitic milk on the basis of toxin genes and coagulase gene polymorphisms. Vet. Microbiol. 105, 301–305 (2005).

    Tsunemitsu H. , 'Molecular typing of Staphylococcus aureus isolated from bovine mastitic milk on the basis of toxin genes and coagulase gene polymorphisms ' (2005 ) 105 Vet. Microbiol. : 301 -305.

    • Search Google Scholar
  • Raimundo, O., Deighton, M., Capstick, J., Gerraty, N.: Molecular typing of Staphylococcus aureus of bovine origin by polymorphisms of the coagulase gene. Vet. Microbiol. 66, 275–284 (1999).

    Gerraty N. , 'Molecular typing of Staphylococcus aureus of bovine origin by polymorphisms of the coagulase gene ' (1999 ) 66 Vet. Microbiol. : 275 -284.

    • Search Google Scholar
  • Peles, F., Wagner, M., Varga, L., Hein, I., Rieck, P., Gutser, K. et al.: Characterization of Staphylococcus aureus strains isolated from bovine milk in Hungary. Int. J. Food Microbiol. 15, 186–193 (2007).

    Gutser K. , 'Characterization of Staphylococcus aureus strains isolated from bovine milk in Hungary ' (2007 ) 15 Int. J. Food Microbiol. : 186 -193.

    • Search Google Scholar
  • Scherrer, D., Corti, S., Muehlherr, J. E., Zweifel, C., Stephan, R.: Phenotypic and genotypic characteristics of Staphylococcus aureus isolates from raw bulk-tank milk samples of goats and sheep. Vet. Microbiol. 101, 101–107 (2004).

    Stephan R. , 'Phenotypic and genotypic characteristics of Staphylococcus aureus isolates from raw bulk-tank milk samples of goats and sheep ' (2004 ) 101 Vet. Microbiol. : 101 -107.

    • Search Google Scholar
  • Balaban, N., Rasooly, A.: Staphylococcal enterotoxins. Int. J. Food Microbiol. 1, 1–10 (2000).

    Rasooly A. , 'Staphylococcal enterotoxins ' (2000 ) 1 Int. J. Food Microbiol. : 1 -10.

  • Chiang, Y. C., Liao, W. W., Fan, C. M., Pai, W. Y., Chiou, C. S., Tsen, H. Y.: PCR detection of Staphylococcal enterotoxins (SEs) N, O, P, Q, R, U, and survey of SE types in Staphylococcus aureus isolates from food-poisoning cases in Taiwan. Int. J. Food Microbiol. 121, 66–73 (2008).

    Tsen H. Y. , 'PCR detection of Staphylococcal enterotoxins (SEs) N, O, P, Q, R, U, and survey of SE types in Staphylococcus aureus isolates from food-poisoning cases in Taiwan ' (2008 ) 121 Int. J. Food Microbiol. : 66 -73.

    • Search Google Scholar
  • Le Loir, Y., Baron, F., Gautier, M.: Staphylococcus aureus and food poisoning. Genet. Mol. Res. 2, 63–76 (2003).

    Gautier M. , 'Staphylococcus aureus and food poisoning ' (2003 ) 2 Genet. Mol. Res. : 63 -76.

  • Moon, J. S., Lee, A. R., Kang, H. M., Lee, E. S., Joo, Y. S., Park, Y. H. et al.: Antibiogram and coagulase diversity in staphylococcal enterotoxin-producing Staphylococcus aureus from bovine mastitis. J. Dairy Sci. 90, 1716–1724 (2007).

    Park Y. H. , 'Antibiogram and coagulase diversity in staphylococcal enterotoxin-producing Staphylococcus aureus from bovine mastitis ' (2007 ) 90 J. Dairy Sci. : 1716 -1724.

    • Search Google Scholar
  • Hogan, J. S., González, R. N., Harmon, R. J., Nickerson, S.: Laboratory Handbook on Bovine Mastitis. Rev. ed. The National Mastitis Council, Madison, WI, 1999.

    Nickerson S. , '', in Laboratory Handbook on Bovine Mastitis , (1999 ) -.

  • Pezzlo, M.: Aerobic bacteriology. In: Isenberg, H. D. (Editor), Clinical Microbiology Procedures Handbook, American Society for Microbiology, Washington, DC, 1992.

    Pezzlo M. , '', in Clinical Microbiology Procedures Handbook , (1992 ) -.

  • Shahsavan, S., Jabalameli, L., Maleknejad, P., Aligholi, M., Imaneini, H., Jabalameli, F. et al.: Molecular analysis and antimicrobial susceptibility of methicillin resistant Staphylococcus aureus in one of the hospitals of Tehran University of Medical Sciences: High prevalence of sequence type 239 (ST239) clone. Acta Microbiol. Immunol. Hung. 58, 31–39 (2011).

    Jabalameli F. , 'Molecular analysis and antimicrobial susceptibility of methicillin resistant Staphylococcus aureus in one of the hospitals of Tehran University of Medical Sciences: High prevalence of sequence type 239 (ST239) clone ' (2011 ) 58 Acta Microbiol. Immunol. Hung. : 31 -39.

    • Search Google Scholar
  • Tang, Y. W., Waddington, M. G., Smith, D. H., Manahan, J. M., Kohner, P. C., Highsmith, L. M. et al.: Comparison of protein A gene sequencing with pulsed-field gel electrophoresis and epidemiologic data for molecular typing of methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 38, 1347–1351 (2000)

    Highsmith L. M. , 'Comparison of protein A gene sequencing with pulsed-field gel electrophoresis and epidemiologic data for molecular typing of methicillin-resistant Staphylococcus aureus ' (2000 ) 38 J. Clin. Microbiol. : 1347 -1351.

    • Search Google Scholar
  • Clinical laboratory Standards Institute. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals; Approved Standard Second Edition. CLSI, Wayne, PA, USA, 2006.

    '', in Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals , (2006 ) -.

  • Mehrotra, M., Wang, G., Johnson, W. M.: Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J. Clin. Microbiol. 38, 1032–1035 (2000).

    Johnson W. M. , 'Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance ' (2000 ) 38 J. Clin. Microbiol. : 1032 -1035.

    • Search Google Scholar
  • Emaneini, M., Jabalameli, L., Imaneini, H., Aligholi, M., Ghasemi, A., Nakhjavani, F. A. et al.: Multiple-locus variable number of tandem repeats fingerprinting (MLVF) and virulence factor analysis of methicillin resistant Staphylococcus aureus SCCmec type III. Pol. J. Microbiol. (In press).

  • Kérouanton, A., Hennekinne, J. A., Letertre, C., Petit, L., Chesneau, O., Brisabois, A. et al.: Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int. J. Food Microbiol. 115, 369–375 (2007).

    Brisabois A. , 'Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France ' (2007 ) 115 Int. J. Food Microbiol. : 369 -375.

    • Search Google Scholar
  • Shimizu, A., Fujita, M., Igarashi, H., Takagi, M., Nagase, N., Sasaki, A. et al.: Characterization of Staphylococcus aureus coagulase type VII isolates from staphylococcal food poisoning outbreaks (1980–1995) in Tokyo, Japan, by pulsed-field gel electrophoresis. J. Clin. Microbiol. 38, 3746–3749 (2000).

    Sasaki A. , 'Characterization of Staphylococcus aureus coagulase type VII isolates from staphylococcal food poisoning outbreaks (1980–1995) in Tokyo, Japan, by pulsed-field gel electrophoresis ' (2000 ) 38 J. Clin. Microbiol. : 3746 -3749.

    • Search Google Scholar
  • Rodrigues da Silva, E., da Silva, N.: Coagulase gene typing of Staphylococcus aureus isolated from cows with mastitis in southeastern Brazil. Can. J. Vet. Res. 69, 260–264 (2005).

    Silva N. , 'Coagulase gene typing of Staphylococcus aureus isolated from cows with mastitis in southeastern Brazil ' (2005 ) 69 Can. J. Vet. Res. : 260 -264.

    • Search Google Scholar
  • Schlegelová, J., Dendis, M., Benedík, J., Babák, V., Rysánek, D.: Staphylococcus aureus isolates from dairy cows and humans on a farm differ in coagulase genotype. Vet. Microbiol. 92, 327–334 (2003).

    Rysánek D. , 'Staphylococcus aureus isolates from dairy cows and humans on a farm differ in coagulase genotype ' (2003 ) 92 Vet. Microbiol. : 327 -334.

    • Search Google Scholar
  • Su, C., Herbelin, C., Frieze, N., Skardova, O., Sordillo, L. M.: Coagulase gene polymorphism of Staphylococcus aureus isolates from dairy cattle in different geographical areas. Epidemiol. Infect 122, 329–336 (1999).

    Sordillo L. M. , 'Coagulase gene polymorphism of Staphylococcus aureus isolates from dairy cattle in different geographical areas ' (1999 ) 122 Epidemiol. Infect : 329 -336.

    • Search Google Scholar
  • Su, C., Kanevsky, I., Jayarao, B. M., Sordillo, L. M.: Phylogenetic relationships of Staphylococcus aureus from bovine mastitis based on coagulase gene polymorphism. Vet. Microbiol. 71, 53–58 (2000).

    Sordillo L. M. , 'Phylogenetic relationships of Staphylococcus aureus from bovine mastitis based on coagulase gene polymorphism ' (2000 ) 71 Vet. Microbiol. : 53 -58.

    • Search Google Scholar
  • Saei, H. D., Ahmadi, M., Mardani, K., Batavani, R. A.: Molecular typing of Staphylococcus aureus isolated from bovine mastitis based on polymorphism of the coagulase gene in the north west of Iran. Vet. Microbiol. 137, 202–206 (2009).

    Batavani R. A. , 'Molecular typing of Staphylococcus aureus isolated from bovine mastitis based on polymorphism of the coagulase gene in the north west of Iran ' (2009 ) 137 Vet. Microbiol. : 202 -206.

    • Search Google Scholar
  • Kumar, R., Yadav, B. R., Singh, R. S.: Genetic determinants of antibiotic resistance in Staphylococcus aureus isolates from milk of mastitic crossbred cattle. Curr. Microbiol. 60, 379–386 (2010).

    Singh R. S. , 'Genetic determinants of antibiotic resistance in Staphylococcus aureus isolates from milk of mastitic crossbred cattle ' (2010 ) 60 Curr. Microbiol. : 379 -386.

    • Search Google Scholar
  • Moon, J. S., Lee, A. R., Jaw, S. H., Kang, H. M., Joo, Y. S., Park, Y. H. et al.: Comparison of antibiogram, staphylococcal enterotoxin productivity, and coagulase genotypes among Staphylococcus aureus isolated from animal and vegetable sources in Korea. J. Food Prot. 70, 2541–2548 (2007).

    Park Y. H. , 'Comparison of antibiogram, staphylococcal enterotoxin productivity, and coagulase genotypes among Staphylococcus aureus isolated from animal and vegetable sources in Korea ' (2007 ) 70 J. Food Prot. : 2541 -2548.

    • Search Google Scholar
  • De Oliveira, A. P., Watts, J. L., Salmon, S. A., Aarestrup, F. M.: Antimicrobial susceptibility of Staphylococcus aureus isolated from bovine mastitis in Europe and the United States. J. Dairy Sci. 83, 855–862 (2000).

    Aarestrup F. M. , 'Antimicrobial susceptibility of Staphylococcus aureus isolated from bovine mastitis in Europe and the United States ' (2000 ) 83 J. Dairy Sci. : 855 -862.

    • Search Google Scholar
  • Wang, Y., Wu, C. M., Lu, L. M., Ren, G. W., Cao, X. Y., Shen, J. Z.: Macrolide-lincosamide-resistant phenotypes and genotypes of Staphylococcus aureus isolated from bovine clinical mastitis. Vet. Microbiol. 130, 118–125 (2008).

    Shen J. Z. , 'Macrolide-lincosamide-resistant phenotypes and genotypes of Staphylococcus aureus isolated from bovine clinical mastitis ' (2008 ) 130 Vet. Microbiol. : 118 -125.

    • Search Google Scholar
  • Eslampour, M. A., Hovareshti, P., Feizabadi, M. M., Aligholi, M., Bolourchi, M., Jabalameli, F., Barin, A. et al.: Molecular characterization of Staphylococcus aureus isolated from bovine mastitis in Iran. Vet. Microbiol. 139, 207–208 (2009).

    Barin A. , 'Molecular characterization of Staphylococcus aureus isolated from bovine mastitis in Iran ' (2009 ) 139 Vet. Microbiol. : 207 -208.

    • Search Google Scholar
  • Morandi, S., Brasca, M., Andrighetto, C., Lombardi, A., Lodi, R.: Phenotypic and genotypic characterization of Staphylococcus aureus strains from Italian dairy products. Int. J. Microbiol. 2010 Jan 27 (2009).

  • Rall, V. L., Vieira, F. P., Rall, R., Vieitis, R. L., Fernandes, A. Jr., Candeias, J. M. et al.: PCR detection of staphylococcal enterotoxin genes in Staphylococcus aureus strains isolated from raw and pasteurized milk. Vet. Microbiol. 132, 408–413 (2008).

    Candeias J. M. , 'PCR detection of staphylococcal enterotoxin genes in Staphylococcus aureus strains isolated from raw and pasteurized milk ' (2008 ) 132 Vet. Microbiol. : 408 -413.

    • Search Google Scholar
  • Jørgensen, H. J., Mørk, T., Høgåsen, H. R., Rørvik, L. M.: Enterotoxigenic Staphylococcus aureus in bulk milk in Norway. J. Appl. Microbiol. 99, 158–166 (2005).

    Rørvik L. M. , 'Enterotoxigenic Staphylococcus aureus in bulk milk in Norway ' (2005 ) 99 J. Appl. Microbiol. : 158 -166.

    • Search Google Scholar
  • Villard, L., Lamprell, H., Borges, E., Maurin, F., Noël, Y., Beuvier, E. et al.: Enterotoxin D producing strains of Staphylococcus aureus are typeable by pulsed-field gel electrophoresis (PFGE). Food Microbiol. 22, 261–265 (2005).

    Beuvier E. , 'Enterotoxin D producing strains of Staphylococcus aureus are typeable by pulsed-field gel electrophoresis (PFGE) ' (2005 ) 22 Food Microbiol. : 261 -265.

    • Search Google Scholar
  • Boerema, J. A., Clemens, R., Brightwell, G.: Evaluation of molecular methods to determine enterotoxigenic status and molecular genotype of bovine, ovine, human and food isolates of Staphylococcus aureus. Int. J. Food Microbiol. 107, 192–201 (2006).

    Brightwell G. , 'Evaluation of molecular methods to determine enterotoxigenic status and molecular genotype of bovine, ovine, human and food isolates of Staphylococcus aureus ' (2006 ) 107 Int. J. Food Microbiol. : 192 -201.

    • Search Google Scholar

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