Acta Veterinaria Hungarica
Volume/Issue:
Volume 60: Issue 2
Investigation of the antibiotic resistance and biofilm formation of Staphylococcus aureus strains isolated from gangrenous mastitis of ewes
Authors: Osman Tel 1 , Özkan Aslantaş 2 , Oktay Keskin 1 , Ebru Yilmaz 3 , and Cemil Demir 4
View More View Less
  • 1 Harran University Department of Microbiology, Faculty of Veterinary Medicine Eyyubiye Campus Eyyubiye, Sanliurfa Turkey
  • 2 Mustafa Kemal University Department of Microbiology, Faculty of Veterinary Medicine Hatay Turkey
  • 3 Mustafa Kemal University Department of Biology, Faculty of Arts and Sciences Hatay Turkey
  • 4 Mustafa Kemal University Department of Microbiology, Faculty of Medicine Hatay Turkey
DOI:
https://doi.org/10.1556/avet.2012.016
Page Count:
189–197
Publication Date:
01 Jun 2012
Online Publication Date:
18 May 2012
Article Category:
Research Article
Restricted access

Purchase article

USD  $25.00

1 year subscription (Individual Only)

USD  $836.00
Purchase Online Subscription

  • Purchase article

    USD  $25.00

  • 1 year subscription (Individual Only)

    USD  $836.00

In this study, Staphylococcus aureus strains (n = 110) isolated from seven ewe flocks in Sanliurfa, Turkey were screened for antibiotic resistance and biofilmforming ability as well as for genes associated with antibiotic resistance and biofilm-forming ability. All isolates were found to be susceptible to oxacillin, gentamicin, clindamycin, cefoxitin, tetracycline, vancomycin, amoxicillin-clavulanic acid, ciprofloxacin and sulphamethoxazole-trimethoprim. The percent proportions of strains resistant to penicillin G, ampicillin and erythromycin were 27.2% (n = 30), 25.4% (n = 28) and 6.3% (n = 7), respectively. Regarding the antibiotic resistance genes, 32 (29%) isolates carried the blaZ and 8 (7.2%) the ermC gene. Other resistance genes were not detected in the isolates. All isolates showed biofilm-forming ability on Congo red agar (CRA), while 108 (98.18%) and 101 (91.81%) of them were identified as biofilm producers by the use of standard tube (ST) and microplate (MP) methods, respectively. All isolates carried the icaA and icaD genes but none of them harboured the bap gene. The results demonstrated that S. aureus isolates from gangrenous mastitis were mainly resistant to penicillins (which are susceptible to the staphylococcal beta-lactamase enzyme), and less frequently to erythromycin. Furthermore, all of the S. aureus isolates produced biofilm which was considered a potential virulence factor in the pathogenesis of staphylococcal mastitis.

  • Bengtsson, B., Unnerstad, H. E., Ekman, T., Artursson, K., Nilsson-Ost, M. and Waller, K. P. (2009): Antimicrobial susceptibility of udder pathogens from cases of acute clinical mastitis in dairy cows. Vet. Microbiol. 136, 142–149.

    Waller K. P. , 'Antimicrobial susceptibility of udder pathogens from cases of acute clinical mastitis in dairy cows ' (2009 ) 136 Vet. Microbiol. : 142 -149.

    • Search Google Scholar

  • Chen, S., Zhao, S., McDermott, P. F., Schroeder, C. M., White, D. G. and Meng, J. (2005): A DNA microarray for identification of virulence and antimicrobial resistance genes in Salmonella serovars and Escherichia coli. Mol. Cell. Probes 19, 195–201.

    Meng J. , 'A DNA microarray for identification of virulence and antimicrobial resistance genes in Salmonella serovars and Escherichia coli ' (2005 ) 19 Mol. Cell. Probes : 195 -201.

    • Search Google Scholar

  • Choi, S. M., Kim, S. H., Kim, H. J., Lee, D. G., Choi, J. H., Yoo, J. H., Kang, J. H., Shin, W. S. and Kang, M. W. (2003): Multiplex PCR for the detection of genes encoding aminoglycoside modifying enzymes and methicillin resistance among Staphylococcus species. J. Korean Med. Sci. 18, 631–636.

    Kang M. W. , 'Multiplex PCR for the detection of genes encoding aminoglycoside modifying enzymes and methicillin resistance among Staphylococcus species ' (2003 ) 18 J. Korean Med. Sci. : 631 -636.

    • Search Google Scholar

  • Christensen, G. D., Simpson, W. A., Younger, J. J., Baddour, L. M., Barrett, F. F., Melton, D. M. and Beachey, E. H. (1985): Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J. Clin. Microbiol. 22, 996–1006.

    Beachey E. H. , 'Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices ' (1985 ) 22 J. Clin. Microbiol. : 996 -1006.

    • Search Google Scholar

  • Chung, W. O., Werckenthin, C., Schwarz, S. and Roberts, M. C. (1999): Host range of the ermF rRNA methylase gene in bacteria of human and animal origin. J. Antimicrob. Chemother. 43, 5–14.

    Roberts M. C. , 'Host range of the ermF rRNA methylase gene in bacteria of human and animal origin ' (1999 ) 43 J. Antimicrob. Chemother. : 5 -14.

    • Search Google Scholar

  • Clinical and Laboratory Standards Institute (2006): Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard. Ninth Edition. M2-A9.

  • Wayne, Pennsylvania, USA. Cucarella, C., Angeles-Tormo, M., Ubeda, C., Pilar-Trotonda, M., Monzon, M., Peris, C., Amorena, B., Lasa, I. and Penades, J. S. (2004): Role of biofilm associated protein Bap in the pathogenesis of bovine Staphylococcus aureus. Infect. Immun. 72, 2177–2185.

    Penades J. S. , 'Role of biofilm associated protein Bap in the pathogenesis of bovine Staphylococcus aureus ' (2004 ) 72 Infect. Immun. : 2177 -2185.

    • Search Google Scholar

  • Cucarella, C., Solano, C., Valle, J., Amorena, B., Lasa, I. and Penades, J. R. (2001): Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol. 183, 2888–2896.

    Penades J. R. , 'Bap, a Staphylococcus aureus surface protein involved in biofilm formation ' (2001 ) 183 J. Bacteriol. : 2888 -2896.

    • Search Google Scholar

  • Dhanawade, N. B., Kalorey, D. R., Srinivasan, R., Barbuddhe, S. B. and Kurkure, N. V. (2010): Detection of intercellular adhesion genes and biofilm production in Staphylococcus aureus isolated from bovine subclinical mastitis. Vet. Res. Commun. 34, 81–89.

    Kurkure N. V. , 'Detection of intercellular adhesion genes and biofilm production in Staphylococcus aureus isolated from bovine subclinical mastitis ' (2010 ) 34 Vet. Res. Commun. : 81 -89.

    • Search Google Scholar

  • Eady, E. A., Ross, J. I., Tipper, J. L., Walters, C. E., Cove, J. H. and Noble, W. C. (1993): Distribution of genes encoding erythromycin ribosomal methylases and an erythromycin efflux pump in epidemiologically distinct groups of staphylococci. J. Antimicrob. Chemother. 31, 211–217.

    Noble W. C. , 'Distribution of genes encoding erythromycin ribosomal methylases and an erythromycin efflux pump in epidemiologically distinct groups of staphylococci ' (1993 ) 31 J. Antimicrob. Chemother. : 211 -217.

    • Search Google Scholar

  • Freeman, D. J., Falkiner, F. R. and Keane, C. T. (1989): New method for detecting slime production by coagulase negative staphylococci. J. Clin. Pathol. 42, 872–874.

    Keane C. T. , 'New method for detecting slime production by coagulase negative staphylococci ' (1989 ) 42 J. Clin. Pathol. : 872 -874.

    • Search Google Scholar

  • Jensen, L. B., Frimodt-Moller, N. and Aarestrup, F. M. (1999): Presence of erm gene classes in gram-positive bacteria of animal and human origin in Denmark. FEMS Microbiol. Lett. 170, 151–158.

    Aarestrup F. M. , 'Presence of erm gene classes in gram-positive bacteria of animal and human origin in Denmark ' (1999 ) 170 FEMS Microbiol. Lett. : 151 -158.

    • Search Google Scholar

  • Lollai, S. A., Ziccheddu, M., Di Mauro, C., Manunta, D., Nudda, A. and Leori, G. (2008): Profile and evolution of antimicrobial resistance of ovine mastitis pathogens (1995-2004). Small Rumin. Res. 74, 249–254.

    Leori G. , 'Profile and evolution of antimicrobial resistance of ovine mastitis pathogens (1995-2004) ' (2008 ) 74 Small Rumin. Res. : 249 -254.

    • Search Google Scholar

  • Otto, M. (2008): Staphylococcal biofilms. In: Romeo, T. (ed) Bacterial Biofilms. Springer-Verlag, Berlin, Heidelberg. Germany. pp. 207–228.

    Otto M. , '', in Bacterial Biofilms , (2008 ) -.

  • Quinn, P. J., Carter, M. E., Markey, B. K. and Carter, G. R. (eds) (1999): Clinical Veterinary Microbiology. 5th edition. Harcourt Publishers Limited, Spain.

    '', in Clinical Veterinary Microbiology , (1999 ) -.

  • Rajala-Schultz, P. J., Torres, A. H., Degraves, F. J., Gebreyes, W. A. and Patchanee, P. (2009): Antimicrobial resistance and genotypic characterization of coagulase-negative staphylococci over the dry period. Vet. Microbiol. 134, 55–64.

    Patchanee P. , 'Antimicrobial resistance and genotypic characterization of coagulase-negative staphylococci over the dry period ' (2009 ) 134 Vet. Microbiol. : 55 -64.

    • Search Google Scholar

  • Sambrook, J. and Russell, D. (2001): Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.

    Russell D. , '', in Molecular Cloning: A Laboratory Manual , (2001 ) -.

  • Simko, S. and Bartko, P. (1996): Antibiotic resistance in Staphylococcus aureus mastitis in sheep, sheep milk and its products. Vet. Med. (Praha). 41, 241–244.

    Bartko P. , 'Antibiotic resistance in Staphylococcus aureus mastitis in sheep, sheep milk and its products ' (1996 ) 41 Vet. Med. (Praha). : 241 -244.

    • Search Google Scholar

  • Strommenger, B., Kettlitz, C., Werner, G. and Witte, W. (2003): Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus. J. Clin. Microbiol. 41, 4089–4094.

    Witte W. , 'Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus ' (2003 ) 41 J. Clin. Microbiol. : 4089 -4094.

    • Search Google Scholar

  • Vancraeynest, D., Hermans, K. and Haesebrouck, F. (2004): Genotypic and phenotypic screening of high and low virulence Staphylococcus aureus isolates from rabbits for biofilm formation and MSCRAMMs. Vet. Microbiol. 103, 241–247.

    Haesebrouck F. , 'Genotypic and phenotypic screening of high and low virulence Staphylococcus aureus isolates from rabbits for biofilm formation and MSCRAMMs ' (2004 ) 103 Vet. Microbiol. : 241 -247.

    • Search Google Scholar

  • Vasudevan, P., Nair, M. K., Annamalai, T. and Venkitanarayanan, K. S. (2003): Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation. Vet. Microbiol. 92, 179–185.

    Venkitanarayanan K. S. , 'Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation ' (2003 ) 92 Vet. Microbiol. : 179 -185.

    • Search Google Scholar

  • Vautor, E., Abadiea, G., Ponta, A. and Thierya, R. (2008): Evaluation of the presence of the bap gene in Staphylococcus aureus isolates recovered from human and animal species. Vet. Microbiol. 127, 407–411.

    Thierya R. , 'Evaluation of the presence of the bap gene in Staphylococcus aureus isolates recovered from human and animal species ' (2008 ) 127 Vet. Microbiol. : 407 -411.

    • Search Google Scholar

  • Vesterholm-Nielsen, M., Olhom-Larsen, M., Elmerdahl-Olsen, J. and Moller-Aerestrup, F. (1999): Occurrence of the blaZ gene in penicillin resistant Staphylococcus aureus isolated from bovine mastitis in Denmark. Acta Vet. Scand. 40, 279–286.

    Moller-Aerestrup F. , 'Occurrence of the blaZ gene in penicillin resistant Staphylococcus aureus isolated from bovine mastitis in Denmark ' (1999 ) 40 Acta Vet. Scand. : 279 -286.

    • Search Google Scholar

  • Watkins, G. H. and Jones, J. E. T. (2007): Mastitis and contagious agalactia. In: Aitken, I. D. (ed.) Diseases of Sheep. Fourth Edition. Blackwell Publishing Ltd., Oxford. UK. pp. 99–105.

    Jones J. E. T. , '', in Diseases of Sheep , (2007 ) -.

  • Watson, D. J. and Buswell, J. F. (1984): Modern aspects of sheep mastitis. Br. Vet. J. 140, 529–534.

    Buswell J. F. , 'Modern aspects of sheep mastitis ' (1984 ) 140 Br. Vet. J. : 529 -534.

  • Yazdani, R., Oshaghi, M., Havayi, A., Pishva, E., Salehi, R., Sadeghizadeh, M. and Foroohesh, H. (2006): Detection of icaAD gene and biofilm formation in Staphylococcus aureus isolates from wound infection. Iranian J. Publ. Health 35, 25–28.

    Foroohesh H. , 'Detection of icaAD gene and biofilm formation in Staphylococcus aureus isolates from wound infection ' (2006 ) 35 Iranian J. Publ. Health : 25 -28.

    • Search Google Scholar
Cover Acta Veterinaria Hungarica
Acta Veterinaria Hungarica
Print ISSN:
0236-6290
Online ISSN:
1588-2705
Keywords:
Antibiotic resistance genes; biofilm formation; Staphylococcus aureus ; gangrenous mastitis; sheep

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Aug 2020 5 0 0
Sep 2020 3 1 1
Oct 2020 4 1 2
Nov 2020 5 1 0
Dec 2020 1 0 0
Jan 2021 9 0 0
Feb 2021 0 0 0