Zoonotic Staphylococcus spp. among domestic animals in Ukraine: antibiotic resistance and diagnostic approaches

Keywords: Staphylococcus pseudintermedius; dog; resistance to antibiotics; microorganisms; prevalence; zoonotic pathogens

Abstract Staphylococcus pseudintermedius and S. aureus are common infectious agents with zoonotic potential, capable of acquiring antibiotic resistance and causing hospital-acquired infections. This study aimed to assess the prevalence of S. pseudintermedius among dogs in Ukraine and explore the possibility of using chromogenic media for accurate identification and differentiation of S. aureus and S. pseudintermedius. The data obtained indicate a higher prevalence of nasal carriage (44.8%) of Staphylococcus spp. in healthy dogs compared to ear carriage (28.5%). Among the isolated strains in nasal swabs, S. pseudintermedius was most often detected (24.1%), S. aureus was detected less often (5.2%). Among the samples taken from sick dogs, 36.5% were found to be Staphylococcus spp., of which 20.5% contained S. pseudintermedius and 4.5% S. aureus. Among the studied cats, 36.8% were found to contain Staphylococcus spp., S. pseudintermedius – 10.5%, and S. aureus – 5.3%. Antibiotic resistance profiles were different: S. pseudintermedius was resistant to the combination of trimethoprim-sulfamethoxazole, as well as to penicillin and erythromycin, while S. aureus was resistant to penicillin. It should be noted that only one coagulase-positive S. aureus isolate obtained from healthy animals was resistant to oxacillin. The use of chromogenic media demonstrated the possibility of successful differentiation of S. aureus and S. pseudintermedius based on differences in culture properties. In addition, various combinations of microbiological tests were evaluated, resulting in the development of two schemes that included specific media and additional reactions to improve identification accuracy. The combination of CHROMagar™ Orientation with the coagulase detection reaction demonstrated higher sensitivity (100%) for the detection of S. pseudintermedius compared to the combination of mannitol salt agar (MSA) with the coagulase detection reaction (75%). In addition, the PCR reaction was valuable for the definitive identification of coagulase-positive staphylococci (CoPS). These comprehensive results shed light on the prevalence, species distribution, antibiotic resistance patterns, and diagnostic approaches for S. aureus in dogs and cats in Ukraine, emphasizing the importance of developing reliable surveillance and control strategies.

References

Bannoehr, J., & Guardabassi, L. (2012). Staphylococcus pseudintermedius in the dog: Taxonomy, diagnostics, ecology, epidemiology and pathogenicity. Veterinary Dermatology, 23(4), 253–e52.
Beça, N., Bessa, L. J., Mendes, Â., Santos, J., Leite-Martins, L., Matos, A. J., & da Costa, P. M. (2015). Coagulase-positive Staphylococcus: Prevalence and antimicrobial resistance. Journal of the American Animal Hospital Association, 51(6), 365–371.
Bhooshan, S., Negi, V., & Khatri, P. K. (2020). Staphylococcus pseudintermedius: An undocumented, emerging pathogen in humans. GMS Hygiene and Infection Control, 15, Doc32.
Bourély, C., Cazeau, G., Jarrige, N., Leblond, A., Madec, J. Y., Haenni, M., & Gay, E. (2019). Antimicrobial resistance patterns of bacteria isolated from dogs with otitis. Epidemiology and Infection, 147, e121.
Burke, M., & Santoro, D. (2023). Prevalence of multidrug-resistant coagulase-positive staphylococci in canine and feline dermatological patients over a 10-year period: A retrospective study. Microbiology, 169(2), 001300.
Bzdil, J., Zouharova, M., Nedbalcova, K., Sladecek, V., Senk, D., & Holy, O. (2021). Oxacillin (methicillin) resistant staphylococci in domestic animals in the Czech Republic. Pathogens, 10(12), 1585.
Carricajo, A., Treny, A., Fonsale, N., Bes, M., Reverdy, M. E., Gille, Y., Aubert, G., & Freydiere, A. M. (2001). Performance of the chromogenic medium CHROMagar Staph Aureus and the Staphychrom coagulase test in the detection and identification of Staphylococcus aureus in clinical specimens. Journal of Clinical Microbiology, 39(7), 2581–2583.
Cuny, C., Layer-Nicolaou, F., Weber, R., Köck, R., & Witte, W. (2022). Colonization of dogs and their owners with Staphylococcus aureus and Staphylococcus pseudintermedius in households, veterinary practices, and healthcare facilities. Microorganisms, 10(4), 677.
De Jong, A., Youala, M., El Garch, F., Simjee, S., Rose, M., Morrissey, I., & Moyaert, H. (2020). Antimicrobial susceptibility monitoring of canine and feline skin and ear pathogens isolated from European veterinary clinics: Results of the ComPath Surveillance programme. Veterinary Dermatology, 31(6), 431-e114.
Dos Santos, I. C., Barbosa, L. N., Da Silva, G. R., Otutumi, L. K., Zaniolo, M. M., Dos Santos, M. C., De Paula Ferreira, L. R., Gonçalves, D. D., & De Almeida Martins, L. (2022). Pet dogs as reservoir of oxacillin and vancomycin-resistant Staphylococcus spp. Research in Veterinary Science, 143, 28–32.
Fungwithaya, P., Sontigun, N., Boonhoh, W., Boonchuay, K., & Wongtawan, T. (2022). Antimicrobial resistance in Staphylococcus pseudintermedius on the environmental surfaces of a recently constructed veterinary hospital in Southern Thailand. Veterinary World, 15(4), 1087–1096.
Gaillot, O., Wetsch, M., Fortineau, N., & Berche, P. (2000). Evaluation of CHROMagar Staph. Aureus, a new chromogenic medium, for isolation and presumptive identification of Staphylococcus aureus from Human Clinical Specimens. Journal of Clinical Microbiology, 38(4), 1587–1591.
Gentile, D., Allbaugh, R. A., Adiguzel, M. C., Kenne, D. E., Sahin, O., & Sebbag, L. (2020). Bacterial cross-contamination in a veterinary ophthalmology setting. Frontiers in Veterinary Science, 7, 571503.
Kateete, D. P., Kimani, C. N., Katabazi, F. A., Okeng, A., Okee, M. S., Nanteza, A., Joloba, M. L., & Najjuka, F. C. (2010). Identification of Staphylococcus aureus: DNAse and mannitol salt agar improve the efficiency of the tube coagulase test. Annals of Clinical Microbiology and Antimicrobials, 9(1), 23.
Lakhundi, S., & Zhang, K. (2018). Methicillin-resistant Staphylococcus aureus: Molecular characterization, evolution, and epidemiology. Clinical Microbiology Reviews, 31(4), e00020-18.
Lynch, S. A., & Helbig, K. J. (2021). The complex diseases of Staphylococcus pseudintermedius in canines: Where to next?. Veterinary Sciences, 8(1), 11.
Martineau, F., Picard, F. J., Ke, D., Paradis, S., Roy, P. H., Ouellette, M., & Bergeron, M. G. (2001). Development of a PCR assay for identification of staphylococci at genus and species levels. Journal of Clinical Microbiology, 39(7), 2541–2547.
Moses, I. B., Santos, F. F., & Gales, A. C. (2023). Human colonization and infection by Staphylococcus pseudintermedius: An emerging and underestimated zoonotic pathogen. Microorganisms, 11(3), 581.
Sasaki, T., Tsubakishita, S., Tanaka, Y., Sakusabe, A., Ohtsuka, M., Hirotaki, S., Kawakami, T., Fukata, T., & Hiramatsu, K. (2010). Multiplex-PCR method for species identification of coagulase-positive staphylococci. Journal of Clinical Microbiology, 48(3), 765–769.
Sirobhushanam, S., Parsa, N., Reed, T. J., & Kahlenberg, J. M. (2019). Chromagar™ requires secondary confirmation strategies to minimize false positive/negative results for detection of Staphylococcus aureus. Journal of Microbiological Methods, 161, 71–73.
Souza-Silva, T., Rossi, C. C., Andrade-Oliveira, A. L., Vilar, L. C., Pereira, M. F., Penna, B. A., & Giambiagi-deMarval, M. (2022). Interspecies transfer of plasmid-borne gentamicin resistance between Staphylococcus isolated from domestic dogs to Staphylococcus aureus. Infection, Genetics and Evolution, 98, 105230.
Tang, S., Prem, A., Tjokrosurjo, J., Sary, M., Van Bel, M. A., Rodrigues-Hoffmann, A., Kavanagh, M., Wu, G., Van Eden, M. E., & Krumbeck, J. A. (2020). The canine skin and ear microbiome: A comprehensive survey of pathogens implicated in canine skin and ear infections using a novel next-generation-sequencing-based assay. Veterinary Microbiology, 247, 108764.
Tooke, C. L., Hinchliffe, P., Bragginton, E. C., Colenso, C. K., Hirvonen, V. H. A., Takebayashi, Y., & Spencer, J. (2019). β-Lactamases and β-lactamase inhibitors in the 21st century. Journal of Molecular Biology, 431(18), 3472–3500.
Vishovan, Y., Ushkalov, V., Vygovska, L., Ishchenko, L., Salmanov, A., Bilan, A., Kalakailo, L., Hranat, A., & Boianovskiy, S. (2021). Biofilm formation and antibiotic resistance in Staphylococcus isolated from different objects. Eureka: Life Sciences, 4, 58–65.

留言 (0)

沒有登入
gif