Determination of the diversity and antibiotic resistance profiles of Staphylococcus species from dogs with otitis externa and examination of mecA gene occurrence

https://doi.org/10.17221/8178-VETMEDCitation:Metiner K., Bagcigil A., Ilgaz A. (2015): Determination of the diversity and antibiotic resistance profiles of Staphylococcus species from dogs with otitis externa and examination of mecA gene occurrence. Veterinarni Medicina, 60: 261-267.
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The aim of this study was to determine the distribution of Staphylococci from swab samples of dogs with otitis externa and to determine their antibiotic resistance profiles, particularly methicillin resistance. For this purpose 116 ear swab samples were collected from 100 dogs and examined for the presence of Staphylococcus species by conventional culture methods. Antibiotic susceptibility of the isolates was determined by the disk diffusion test and for methicillin resistance, by PCR. Forty Staphylococci were isolated from 37 (31.9%) of the 116 ear swabs. Among the 40 isolates, 30 of them were coagulase-positive Staphylococcus species (CPS), while 10 (25%) were coagulase-negative Staphylococcus spp. (CNS). S. pseudintermedius (n = 11), S. aureus (n = 8), other not determined Staphylococcus spp. (n = 7), S. chromogenes (n = 7), S. schleiferi coagulans (n = 3), S. hyicus (n = 1), S. hominis subsp. hominis (n = 1), S. simulans (n = 1), S. saprophyticus (n = 1) were isolated. Results of the antibiotic susceptibility tests have shown that 60% of the isolates were resistant to sulfamethoxazole/trimethoprim, 32.5% of them were resistant to erythromycin, 25% were resistant to clindamycin, and all isolates (100%) were sensitive to amoxicillin/clavulanic acid and cephazolin. The majority of isolates (97.5%) were sensitive to ciprofloxacin and gentamicin which are frequently used in otitis externa treatment. It was determined that only one (2.5%) (S. hominis subsp. hominis) of the 40 isolates was resistant to methicillin and carried the mecA gene. We found 77% of Staphylococcus spp. to be resistant to one or more antimicrobial drugs, and 25% of Staphylococcus species were found to be resistant to three or more antimicrobial classes. Thus, multidrug-resistance as detected in our study should always be taken into account and close attention should be given to the antimicrobial therapy protocols of pet animals.
References:
Bagcigil FA, Ikiz S, Guzel O, Parkan Yaramis C, Ilgaz A (2012): Species distribution of methicillin resistant Staphylococci isolated from animals, environmental samples and staffs. The Journal of Faculty of Veterinary Medicine, Istanbul University 38, 151–160.
 
Boost M, O’Donoghue M, James A (2008): Investigation of the role of dogs as reservoirs of Staphylococcus aureus and the transmission of strains between pet owners and their dogs. Hong Kong Medical Journal 14, 15–18.
 
CLSI – Clinical and Laboratory Standards Institute (2010): Performance standards for antimicrobial susceptibility testing: Twentieth informational supplement M100-S20. CLSI, Wayne, PA, USA.
 
Duquette RA, Nuttall TJ (2004): Methicillin-resistant Staphylococcus aureus in dogs and cats: an emerging problem? Journal of Small Animal Practice 45, 591–597.
 
Epstein C.R., Yam W.C., Peiris J.S.M., Epstein R.J. (2009): Methicillin-resistant commensal staphylococci in healthy dogs as a potential zoonotic reservoir for community-acquired antibiotic resistance. Infection, Genetics and Evolution, 9, 283-285  https://doi.org/10.1016/j.meegid.2008.11.003
 
FINDIK Arzu, AKAN Nergiz, ONUK Ertan Emek, ÇAKIROĞLU Duygu, ÇİFTCİ Alper (2009): Sağlıklı Köpeklerin Burunlarından İzole Edilen Staphylococcus aureus Suşlarının Metisilin Direnç Profili ve Moleküler Tiplendirilmesi. Kafkas Universitesi Veteriner Fakultesi Dergisi, , -  https://doi.org/10.9775/kvfd.2009.319
 
Futagawa-Saito K, Ba-Thein W, Sakurai N, Fukuyasu T (2006): Prevalence of virulence factors in Staphylococcus intermedius isolates from dogs and pigeons. BMC Veterinary Research 26, 2–4.
 
Ganiere J.-P., Medaille C., Mangion C. (2005): Antimicrobial Drug Susceptibility of Staphylococcus intermedius Clinical Isolates from Canine Pyoderma. Journal of Veterinary Medicine Series B, 52, 25-31  https://doi.org/10.1111/j.1439-0450.2004.00816.x
 
Guardabassi L, Loeber ME, Jacobson A (2004a): Transmission of multiple antimicrobial-resistant Staphylococcus intermedius between dogs affected by deep pyoderma and their owners. Veterinary Microbiology 98, 23–27.
 
Guardabassi L, Schwarz S, Lloyd DH (2004b): Pet animals as reservoirs of antimicrobial-resistant bacteria. Journal of Antimicrobial Chemotherapy 54, 321–332.
 
Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST (1994): Bergey’s Manual of Determinative Bacteriology. 9th ed. Lippincott Williams & Wilkins, UK. 532, 544–551.
 
Jonas D., Speck M., Daschner F. D., Grundmann H. (2002): Rapid PCR-Based Identification of Methicillin-Resistant Staphylococcus aureus from Screening Swabs. Journal of Clinical Microbiology, 40, 1821-1823  https://doi.org/10.1128/JCM.40.5.1821-1823.2002
 
Jones Rebekah D., Kania Stephen A., Rohrbach Barton W., Frank Linda A., Bemis David A. (2007): Prevalence of oxacillin- and multidrug-resistant staphylococci in clinical samples from dogs: 1,772 samples (2001–2005). Journal of the American Veterinary Medical Association, 230, 221-227  https://doi.org/10.2460/javma.230.2.221
 
Keskin O, Kokcu L, Akan M (1999): Identification and antimicrobial sensitivity of microorganisms isolated from otitic dogs. Veterinary Journal of Ankara University 46, 163–168.
 
Loeffler A, Pfeiffer DU, Lloyd DH, Smith H, Soares-Magalhaes R, Lindsay JA (2010a): Methicillin-resistant Staphylococcus aureus carriage in UK veterinary staff and owners of infected pets: new risk groups. Journal of Hospital Infection 74, 282–288.
 
Loeffler A, Pfeiffer DU, Lindsay JA, Soares-Magalhaes R, Lloyd DH (2010b): Lack of transmission of methicillin-resistant Staphylococcus aureus (MRSA) between apparently healthy dogs in a rescue kennel. Veterinary Microbiology 141, 178–181.
 
Mouney MC, Stiles J, Townsend WM, Guptill L, Weese JS (2013): Prevalence of methicillin-resistant Staphylococcus spp. in the conjunctival sac of healthy dogs. Veterinary Ophthalmology doi: 10.1111/vop. 12130, 1–4.
 
O’Mahony R., Abbott Y., Leonard F.C., Markey B.K., Quinn P.J., Pollock P.J., Fanning S., Rossney A.S. (2005): Methicillin-resistant Staphylococcus aureus (MRSA) isolated from animals and veterinary personnel in Ireland. Veterinary Microbiology, 109, 285-296  https://doi.org/10.1016/j.vetmic.2005.06.003
 
Ozturk D, Avki S, Turutoglu H, Yigitarslan K, Sagnak S (2010): Methicillin resistance among coagulase-positive staphylococci isolated from dogs with otitis externa, skin wounds and pyoderma. Journal of the Faculty of Veterinary Medicine, Kafkas University 6, 651–656.
 
Sarierler M, Kirkan S (2004): Microbiological diagnosis and therapy of canine otitis externa. Veteriner Cerrahi Dergisi 10, 11–15.
 
Sasaki T., Kikuchi K., Tanaka Y., Takahashi N., Kamata S., Hiramatsu K. (): Methicillin-Resistant Staphylococcus pseudintermedius in a Veterinary Teaching Hospital. Journal of Clinical Microbiology, 45, 1118-1125  https://doi.org/10.1128/JCM.02193-06
 
Sasaki T., Tsubakishita S., Tanaka Y., Sakusabe A., Ohtsuka M., Hirotaki S., Kawakami T., Fukata T., Hiramatsu K. (): Multiplex-PCR Method for Species Identification of Coagulase-Positive Staphylococci. Journal of Clinical Microbiology, 48, 765-769  https://doi.org/10.1128/JCM.01232-09
 
Strommenger B. (2006): Molecular characterization of methicillin-resistant Staphylococcus aureus strains from pet animals and their relationship to human isolates. Journal of Antimicrobial Chemotherapy, 57, 461-465  https://doi.org/10.1093/jac/dki471
 
Tanner MA, Everett CL, Youvan DC (2000): Molecular phylogenetic evidence for noninvasive zoonotic transmission of Staphylococcus intermedius from a canine pet to a human. Journal of Clinical Microbiology 38, 1628–1631.
 
van Duijkeren E., Box A.T.A., Heck M.E.O.C., Wannet W.J.B., Fluit A.C. (2004): Methicillin-resistant staphylococci isolated from animals. Veterinary Microbiology, 103, 91-97  https://doi.org/10.1016/j.vetmic.2004.07.014
 
Vanderhaeghen Wannes, Van De Velde Evelien, Crombé Florence, Polis Ingeborgh, Hermans Katleen, Haesebrouck Freddy, Butaye Patrick (2012): Screening for methicillin-resistant staphylococci in dogs admitted to a veterinary teaching hospital. Research in Veterinary Science, 93, 133-136  https://doi.org/10.1016/j.rvsc.2011.06.017
 
Vanni M., Tognetti R., Pretti C., Crema F., Soldani G., Meucci V., Intorre L. (2009): Antimicrobial susceptibility of Staphylococcus intermedius and Staphylococcus schleiferi isolated from dogs. Research in Veterinary Science, 87, 192-195  https://doi.org/10.1016/j.rvsc.2009.01.011
 
Wedley AL (2012): Prevalance of Staphylococcus spp. Carriage in dogs. Department of Epidemiology and Population Health, Institute of Infection and Global Health, University of Liverpool.
 
Weese J.S., Rousseau J., Willey B.M., Archambault M., McGeer A., Low D.E. (2006): Methicillin-resistant Staphylococcus Aureus in Horses at a Veterinary Teaching Hospital: Frequency, Characterization, and Association with Clinical Disease. Journal of Veterinary Internal Medicine, 20, 182-  https://doi.org/10.1892/0891-6640(2006)20[182:MSAIHA]2.0.CO;2
 
Bagcigil FA, Ikiz S, Guzel O, Parkan Yaramis C, Ilgaz A (2012): Species distribution of methicillin resistant Staphylococci isolated from animals, environmental samples and staffs. The Journal of Faculty of Veterinary Medicine, Istanbul University 38, 151–160.
 
Boost M, O’Donoghue M, James A (2008): Investigation of the role of dogs as reservoirs of Staphylococcus aureus and the transmission of strains between pet owners and their dogs. Hong Kong Medical Journal 14, 15–18.
 
CLSI – Clinical and Laboratory Standards Institute (2010): Performance standards for antimicrobial susceptibility testing: Twentieth informational supplement M100-S20. CLSI, Wayne, PA, USA.
 
Duquette RA, Nuttall TJ (2004): Methicillin-resistant Staphylococcus aureus in dogs and cats: an emerging problem? Journal of Small Animal Practice 45, 591–597.
 
Epstein C.R., Yam W.C., Peiris J.S.M., Epstein R.J. (2009): Methicillin-resistant commensal staphylococci in healthy dogs as a potential zoonotic reservoir for community-acquired antibiotic resistance. Infection, Genetics and Evolution, 9, 283-285  https://doi.org/10.1016/j.meegid.2008.11.003
 
FINDIK Arzu, AKAN Nergiz, ONUK Ertan Emek, ÇAKIROĞLU Duygu, ÇİFTCİ Alper (2009): Sağlıklı Köpeklerin Burunlarından İzole Edilen Staphylococcus aureus Suşlarının Metisilin Direnç Profili ve Moleküler Tiplendirilmesi. Kafkas Universitesi Veteriner Fakultesi Dergisi, , -  https://doi.org/10.9775/kvfd.2009.319
 
Futagawa-Saito K, Ba-Thein W, Sakurai N, Fukuyasu T (2006): Prevalence of virulence factors in Staphylococcus intermedius isolates from dogs and pigeons. BMC Veterinary Research 26, 2–4.
 
Ganiere J.-P., Medaille C., Mangion C. (2005): Antimicrobial Drug Susceptibility of Staphylococcus intermedius Clinical Isolates from Canine Pyoderma. Journal of Veterinary Medicine Series B, 52, 25-31  https://doi.org/10.1111/j.1439-0450.2004.00816.x
 
Guardabassi L, Loeber ME, Jacobson A (2004a): Transmission of multiple antimicrobial-resistant Staphylococcus intermedius between dogs affected by deep pyoderma and their owners. Veterinary Microbiology 98, 23–27.
 
Guardabassi L, Schwarz S, Lloyd DH (2004b): Pet animals as reservoirs of antimicrobial-resistant bacteria. Journal of Antimicrobial Chemotherapy 54, 321–332.
 
Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST (1994): Bergey’s Manual of Determinative Bacteriology. 9th ed. Lippincott Williams & Wilkins, UK. 532, 544–551.
 
Jonas D., Speck M., Daschner F. D., Grundmann H. (2002): Rapid PCR-Based Identification of Methicillin-Resistant Staphylococcus aureus from Screening Swabs. Journal of Clinical Microbiology, 40, 1821-1823  https://doi.org/10.1128/JCM.40.5.1821-1823.2002
 
Jones Rebekah D., Kania Stephen A., Rohrbach Barton W., Frank Linda A., Bemis David A. (2007): Prevalence of oxacillin- and multidrug-resistant staphylococci in clinical samples from dogs: 1,772 samples (2001–2005). Journal of the American Veterinary Medical Association, 230, 221-227  https://doi.org/10.2460/javma.230.2.221
 
Keskin O, Kokcu L, Akan M (1999): Identification and antimicrobial sensitivity of microorganisms isolated from otitic dogs. Veterinary Journal of Ankara University 46, 163–168.
 
Loeffler A, Pfeiffer DU, Lloyd DH, Smith H, Soares-Magalhaes R, Lindsay JA (2010a): Methicillin-resistant Staphylococcus aureus carriage in UK veterinary staff and owners of infected pets: new risk groups. Journal of Hospital Infection 74, 282–288.
 
Loeffler A, Pfeiffer DU, Lindsay JA, Soares-Magalhaes R, Lloyd DH (2010b): Lack of transmission of methicillin-resistant Staphylococcus aureus (MRSA) between apparently healthy dogs in a rescue kennel. Veterinary Microbiology 141, 178–181.
 
Mouney MC, Stiles J, Townsend WM, Guptill L, Weese JS (2013): Prevalence of methicillin-resistant Staphylococcus spp. in the conjunctival sac of healthy dogs. Veterinary Ophthalmology doi: 10.1111/vop. 12130, 1–4.
 
O’Mahony R., Abbott Y., Leonard F.C., Markey B.K., Quinn P.J., Pollock P.J., Fanning S., Rossney A.S. (2005): Methicillin-resistant Staphylococcus aureus (MRSA) isolated from animals and veterinary personnel in Ireland. Veterinary Microbiology, 109, 285-296  https://doi.org/10.1016/j.vetmic.2005.06.003
 
Ozturk D, Avki S, Turutoglu H, Yigitarslan K, Sagnak S (2010): Methicillin resistance among coagulase-positive staphylococci isolated from dogs with otitis externa, skin wounds and pyoderma. Journal of the Faculty of Veterinary Medicine, Kafkas University 6, 651–656.
 
Sarierler M, Kirkan S (2004): Microbiological diagnosis and therapy of canine otitis externa. Veteriner Cerrahi Dergisi 10, 11–15.
 
Sasaki T., Kikuchi K., Tanaka Y., Takahashi N., Kamata S., Hiramatsu K. (): Methicillin-Resistant Staphylococcus pseudintermedius in a Veterinary Teaching Hospital. Journal of Clinical Microbiology, 45, 1118-1125  https://doi.org/10.1128/JCM.02193-06
 
Sasaki T., Tsubakishita S., Tanaka Y., Sakusabe A., Ohtsuka M., Hirotaki S., Kawakami T., Fukata T., Hiramatsu K. (): Multiplex-PCR Method for Species Identification of Coagulase-Positive Staphylococci. Journal of Clinical Microbiology, 48, 765-769  https://doi.org/10.1128/JCM.01232-09
 
Strommenger B. (2006): Molecular characterization of methicillin-resistant Staphylococcus aureus strains from pet animals and their relationship to human isolates. Journal of Antimicrobial Chemotherapy, 57, 461-465  https://doi.org/10.1093/jac/dki471
 
Tanner MA, Everett CL, Youvan DC (2000): Molecular phylogenetic evidence for noninvasive zoonotic transmission of Staphylococcus intermedius from a canine pet to a human. Journal of Clinical Microbiology 38, 1628–1631.
 
van Duijkeren E., Box A.T.A., Heck M.E.O.C., Wannet W.J.B., Fluit A.C. (2004): Methicillin-resistant staphylococci isolated from animals. Veterinary Microbiology, 103, 91-97  https://doi.org/10.1016/j.vetmic.2004.07.014
 
Vanderhaeghen Wannes, Van De Velde Evelien, Crombé Florence, Polis Ingeborgh, Hermans Katleen, Haesebrouck Freddy, Butaye Patrick (2012): Screening for methicillin-resistant staphylococci in dogs admitted to a veterinary teaching hospital. Research in Veterinary Science, 93, 133-136  https://doi.org/10.1016/j.rvsc.2011.06.017
 
Vanni M., Tognetti R., Pretti C., Crema F., Soldani G., Meucci V., Intorre L. (2009): Antimicrobial susceptibility of Staphylococcus intermedius and Staphylococcus schleiferi isolated from dogs. Research in Veterinary Science, 87, 192-195  https://doi.org/10.1016/j.rvsc.2009.01.011
 
Wedley AL (2012): Prevalance of Staphylococcus spp. Carriage in dogs. Department of Epidemiology and Population Health, Institute of Infection and Global Health, University of Liverpool.
 
Weese J.S., Rousseau J., Willey B.M., Archambault M., McGeer A., Low D.E. (2006): Methicillin-resistant Staphylococcus Aureus in Horses at a Veterinary Teaching Hospital: Frequency, Characterization, and Association with Clinical Disease. Journal of Veterinary Internal Medicine, 20, 182-  https://doi.org/10.1892/0891-6640(2006)20[182:MSAIHA]2.0.CO;2
 
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