The objective of this study was to evaluate the prevalence of coagulase-negative staphylococci in healthy dogs and to determine whether methicillin-resistant staphylococci expressed the mecA gene. Nasal and rectal swab samples were taken from 50 clinically healthy dogs. The prevalence of coagulase-negative staphylococci was evaluated according to phenotypic properties. The agar diffusion method was applied to evaluate antimicrobial resistance and the prevalence of methicillin resistance was determined using PCR analysing the mecA gene. A total of 59 coagulase-negative staphylococcus strains were isolated from the nostrils and rectums of 37 (74%) clinically healthy dogs. The prevalence of coagulase-negative staphylococci in female dogs was significantly higher compared with male dogs (P < 0.05). The results of antimicrobial susceptibility testing showed that 6.7% of the strains were resistant to oxacillin, 23.7% were resistant to penicillin, 22% to ampicillin and 16.9% to erythromycin. The mecA PCR revealed one oxacillin-sensitive and four oxacillin-resistant coagulase-negative staphylococci strains to be mecA carriers. Staphylococcus sciuri (60%) and Staphylococcus warneri (20%) were the most prevalent species among methicillin-resistant coagulase negative staphylococci. High antimicrobial resistance rates for these bacteria were observed against penicillin (100%), ampicillin (100%), oxacillin (80%), erythromycin (80%) and gentamicin (60%). All strains were susceptible to vancomycin and enrofloxacin. It is assumed that methicillin-resistance genes evolved in coagulase-negative staphylococcus and were then horizontally transferred among staphylococci.
Archer G L, Climo M W (1994): Antimicrobial susceptibility of coagulase-negative staphylococci.. Antimicrobial Agents and Chemotherapy, 38, 2231-2237
https://doi.org/10.1128/AAC.38.10.2231
Aslantas O, Turkyilmaz S, Yilmaz MA, Yilmaz ES (2013): Prevalence of methicillin – resistant staphylococci in dogs. Kafkas Universitesi Veteriner Fakultesi Dergisi Journal 19, 37–42.
Bagcigil Funda A., Moodley Arshnee, Baptiste Keith E., Jensen Vibeke F., Guardabassi Luca (2007): Occurrence, species distribution, antimicrobial resistance and clonality of methicillin- and erythromycin-resistant staphylococci in the nasal cavity of domestic animals. Veterinary Microbiology, 121, 307-315
https://doi.org/10.1016/j.vetmic.2006.12.007
Barigye Robert, Schaan Lynn, Gibbs Penelope S., Schamber Ev, Dyer Neil W. (2016): Diagnostic Evidence of
Staphylococcus Warneri as a Possible Cause of Bovine Abortion. Journal of Veterinary Diagnostic Investigation, 19, 694-696
https://doi.org/10.1177/104063870701900613
Bean DC, Wigmore SM, Wareham DW (2017a): Draft genome sequence of a canine isolate of methicillin-resistant Staphylococcus haemolyticus. Genome Announcement 5, 146–17.
Bean David C., Wigmore Sarah M., Wareham David W. (2017): Draft Genome Sequence of
Staphylococcus cohnii subsp.
urealyticus Isolated from a Healthy Dog. Genome Announcements, 5, e01628-16-
https://doi.org/10.1128/genomeA.01628-16
Chah Kennedy F., Gómez-Sanz Elena, Nwanta John A., Asadu Brendan, Agbo Ifeoma C., Lozano Carmen, Zarazaga Myriam, Torres Carmen (2014): Methicillin-resistant coagulase-negative staphylococci from healthy dogs in Nsukka, Nigeria. Brazilian Journal of Microbiology, 45, 215-220
https://doi.org/10.1590/S1517-83822014005000034
CLSI – Clinical and Laboratory Standards Institute (2010): Performance Standards for Antimicrobial Susceptibility Testing. Twentieth Informational Supplement M100-S20. CLSI, Wayne.
Couto Natacha, Monchique Cláudia, Belas Adriana, Marques Cátia, Gama Luís T., Pomba Constança (2016): Trends and molecular mechanisms of antimicrobial resistance in clinical staphylococci isolated from companion animals over a 16 year period. Journal of Antimicrobial Chemotherapy, 71, 1479-1487
https://doi.org/10.1093/jac/dkw029
Decristophoris PMA (2012): Epidemiology of multi-drug resistant staphylococci in cats, dogs and people in Switzerland. [PhD Thesis.] University of Basel, Switzerland. 183 pp.
Drougka Eleanna, Foka Antigoni, Koutinas Christos K., Jelastopulu Eleni, Giormezis Nikolaos, Farmaki Ourania, Sarrou Styliani, Anastassiou Evangelos D., Petinaki Efthimia, Spiliopoulou Iris (2016): Interspecies spread of Staphylococcus aureus clones among companion animals and human close contacts in a veterinary teaching hospital. A cross-sectional study in Greece. Preventive Veterinary Medicine, 126, 190-198
https://doi.org/10.1016/j.prevetmed.2016.02.004
Gandolfi-Decristophoris Paola, Regula Gertraud, Petrini Orlando, Zinsstag Jakob, Schelling Esther (2013): Prevalence and risk factors for carriage of multi-drug resistant
Staphylococci in healthy cats and dogs. Journal of Veterinary Science, 14, 449-
https://doi.org/10.4142/jvs.2013.14.4.449
Giannouli S., Labrou M., Kyritsis A., Ikonomidis A., Pournaras S., Stathopoulos C., Tsakris A. (2010): Detection of mutations in the FemXAB protein family in oxacillin-susceptible mecA-positive Staphylococcus aureus clinical isolates. Journal of Antimicrobial Chemotherapy, 65, 626-633
https://doi.org/10.1093/jac/dkq039
Han Jae-Ik, Yang Cheol-Ho, Park Hee-Myung (2016): Prevalence and risk factors of Staphylococcus spp. carriage among dogs and their owners: A cross-sectional study. The Veterinary Journal, 212, 15-21
https://doi.org/10.1016/j.tvjl.2015.10.059
Hariharan H, Sylvester EB, Matthew V (2009): Clinical isolates of bacteria from domestic cats in Grenada, and their antimicrobial susceptibility. West Indian Veterinary Journal 9, 14–16.
Hauschild Tomasz, Wójcik Agnieszka (2007): Species distribution and properties of staphylococci from canine dermatitis. Research in Veterinary Science, 82, 1-6
https://doi.org/10.1016/j.rvsc.2006.04.004
Karakulska Jolanta, Fijałkowski Karol, Nawrotek Paweł, Pobucewicz Anna, Poszumski Filip, Czernomysy-Furowicz Danuta (2012): Identification and methicillin resistance of coagulase-negative staphylococci isolated from nasal cavity of healthy horses. Journal of Microbiology, 50, 444-451
https://doi.org/10.1007/s12275-012-1550-6
Kern A., Perreten V. (2013): Clinical and molecular features of methicillin-resistant, coagulase-negative staphylococci of pets and horses. Journal of Antimicrobial Chemotherapy, 68, 1256-1266
https://doi.org/10.1093/jac/dkt020
Kloos WE, Bannerman T (1995): Staphylococcus and micrococcus. In: Murray PR, Baron EJ (eds.): Manual of Clinical Microbiology. 6th edn. ASM Press, Washington, D.C. 282–298.
Kobayashi N., Wu H., Kojima K., Taniguchi K., Urasawa S., Uehara N., Omizu Y., Kishi Y., Yagihashi A., Kurokawa I. (1994): Detection of mecA, femA, and femB genes in clinical strains of staphylococci using polymerase chain reaction. Epidemiology and Infection, 113, 259-266
https://doi.org/10.1017/S0950268800051682
Litster Annette, Moss Susan M., Honnery Mary, Rees Bob, Trott Darren J. (2007): Prevalence of bacterial species in cats with clinical signs of lower urinary tract disease: Recognition of Staphylococcus felis as a possible feline urinary tract pathogen. Veterinary Microbiology, 121, 182-188
https://doi.org/10.1016/j.vetmic.2006.11.025
Malik S. (2006): Molecular typing of methicillin-resistant staphylococci isolated from cats and dogs. Journal of Antimicrobial Chemotherapy, 58, 428-431
https://doi.org/10.1093/jac/dkl253
Moon J.-S., Lee A.-R., Kang H.-M., Lee E.-S., Kim M.-N., Paik Y.H., Park Y.H., Joo Y.-S., Koo H.C. (2007): Phenotypic and Genetic Antibiogram of Methicillin-Resistant Staphylococci Isolated from Bovine Mastitis in Korea. Journal of Dairy Science, 90, 1176-1185
https://doi.org/10.3168/jds.S0022-0302(07)71604-1
Nemeghaire Stéphanie, Argudín M. Angeles, Haesebrouck Freddy, Butaye Patrick (2014): Molecular epidemiology of methicillin-resistant Staphylococcus sciuri in healthy chickens. Veterinary Microbiology, 171, 357-363
https://doi.org/10.1016/j.vetmic.2014.01.041
Oliveira D. C., Lencastre H. d. (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
https://doi.org/10.1128/AAC.46.7.2155-2161.2002
Pu WanXia, Su Yang, Li JianXi, Li ChunHui, Yang ZhiQiang, Deng HaiPing, Ni ChunXia, Zhang Qijing (2014): High Incidence of Oxacillin-Susceptible mecA-Positive Staphylococcus aureus (OS-MRSA) Associated with Bovine Mastitis in China. PLoS ONE, 9, e88134-
https://doi.org/10.1371/journal.pone.0088134
Rahman Mohammed Tanvir, Kobayashi Nobumichi, Alam Mohammed Mahbub, Ishino Masaho (2005): Genetic Analysis of
mecA Homologues in
Staphylococcus sciuri Strains Derived from Mastitis in Dairy Cattle. Microbial Drug Resistance, 11, 205-214
https://doi.org/10.1089/mdr.2005.11.205
Schmidt Vanessa M, Williams Nicola J, Pinchbeck Gina, Corless Caroline E, Shaw Stephen, McEwan Neil, Dawson Susan, Nuttall Tim (2014): Antimicrobial resistance and characterisation of staphylococci isolated from healthy Labrador retrievers in the United Kingdom. BMC Veterinary Research, 10, 17-
https://doi.org/10.1186/1746-6148-10-17
Severin J. A., Lestari E. S., Kuntaman K., Pastink M., Snijders S. V., Lemmens-den Toom N., Horst-Kreft D., Hadi U., Duerink D. O., Goessens W. H., Fluit A. C., van Wamel W., van Belkum A., Verbrugh H. A. (2010): Nasal Carriage of Methicillin-Resistant and Methicillin-Sensitive Strains of Staphylococcus sciuri in the Indonesian Population. Antimicrobial Agents and Chemotherapy, 54, 5413-5417
https://doi.org/10.1128/AAC.00426-10
Smyth Davida S., Wong Agnes, Robinson D. Ashley (2011): Cross-species spread of SCCmec IV subtypes in staphylococci. Infection, Genetics and Evolution, 11, 446-453
https://doi.org/10.1016/j.meegid.2010.12.005
Suter Anja, Voelter Katrin, Hartnack Sonja, Spiess Bernhard Martin, Pot Simon Anton (): Septic keratitis in dogs, cats, and horses in Switzerland: associated bacteria and antibiotic susceptibility. Veterinary Ophthalmology, , -
https://doi.org/10.1111/vop.12480
Tulinski P., Fluit A. C., Wagenaar J. A., Mevius D., van de Vijver L., Duim B. (2011): Methicillin-Resistant Coagulase-Negative Staphylococci on Pig Farms as a Reservoir of Heterogeneous Staphylococcal Cassette Chromosome mec Elements. Applied and Environmental Microbiology, 78, 299-304
https://doi.org/10.1128/AEM.05594-11
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
Vengust M., Anderson M.E.C., Rousseau J., Weese J.S. (2006): Methicillin-resistant staphylococcal colonization in clinically normal dogs and horses in the community. Letters in Applied Microbiology, 43, 602-606
https://doi.org/10.1111/j.1472-765X.2006.02018.x
Wedley Amy L., Dawson Susan, Maddox Thomas W., Coyne Karen P., Pinchbeck Gina L., Clegg Peter, Jamrozy Dorota, Fielder Mark D., Donovan David, Nuttall Tim, Williams Nicola J. (2014): Carriage of Staphylococcus species in the veterinary visiting dog population in mainland UK: Molecular characterisation of resistance and virulence. Veterinary Microbiology, 170, 81-88
https://doi.org/10.1016/j.vetmic.2014.01.015
Zell Christiane, Resch Marion, Rosenstein Ralf, Albrecht Till, Hertel Christian, Götz Friedrich (2008): Characterization of toxin production of coagulase-negative staphylococci isolated from food and starter cultures. International Journal of Food Microbiology, 127, 246-251
https://doi.org/10.1016/j.ijfoodmicro.2008.07.016
GARZA-GONZÁLEZ E., MORFÍN-OTERO R., LLACA-DÍAZ J. M., RODRIGUEZ-NORIEGA E. (2010): Staphylococcal cassette chromosome mec (SCC mec) in methicillin-resistant coagulase-negative staphylococci. A review and the experience in a tertiary-care setting. Epidemiology and Infection, 138, 645-
https://doi.org/10.1017/S0950268809991361