Phenotypic Antimicrobial Resistance and Molecular Virulence Profiles of Staphylococcus aureus Isolated from Canine Skin Infections
DOI:
https://doi.org/10.64614/vzs-38Keywords:
Dog, MDR, pyoderma, staphylococciAbstract
Staphylococcus aureus is an important opportunistic pathogen associated with a wide range of infections in both humans and animals. In dogs, staphylococci are among the major etiological agents of pyoderma and other skin infections. The pathogenicity of these bacteria is closely related to their virulence factors and increasing antimicrobial resistance, which also pose a zoonotic risk. This study investigated the virulence gene profiles and antimicrobial resistance patterns of S. aureus isolates obtained from canine pyoderma cases. All isolates were confirmed as S. aureus by detection of the nuc gene. Molecular analyses revealed the presence of several virulence-associated genes, including exfoliative toxin genes (eta, etb), enterotoxin genes (sea, seb, sec), the Panton-Valentine leukocidin gene (pvl), toxic shock syndrome toxin gene (tst), hemolysin genes (hla, hlb), and adhesion-associated genes (clfA, fnbA, fnbB). Among these, clfA and tst were detected at notably high frequencies, indicating strong adhesion ability and considerable superantigenic potential. Antimicrobial susceptibility testing demonstrated high resistance rates to beta-lactam antibiotics, particularly ampicillin and amoxicillin/clavulanic acid. Moderate resistance rates were observed against clindamycin, doxycycline, gentamicin, and trimethoprim/sulfamethoxazole, whereas resistance to fusidic acid remained relatively low. Notably, 83.3% of the isolates were classified as multidrug-resistant (MDR). These findings highlight the clinical and public health significance of canine-origin S. aureus isolates and emphasize the importance of antimicrobial surveillance and rational antibiotic use.
References
AAbdel-Moein, K.A., & Samir, A. (2011). Isolation of enterotoxigenic Staphylococcus aureus from pet dogs and cats: A public health implication. Vector-Borne and Zoonotic Diseases, 11(6), 627-629.
DOI: https://doi.org/10.1089/vbz.2010.0272 DOI: https://doi.org/10.1089/vbz.2010.0272
Abdolghanizadeh, S., Salmeh, E., Mirzakhani, F., Soroush, E., Siadat, S.D., & Tarashi, S. (2024). Microbiota insights into pet ownership and human health. Research in Veterinary Science, 171, 105220.
DOI: https://doi.org/10.1016/j.rvsc.2024.105220 DOI: https://doi.org/10.1016/j.rvsc.2024.105220
Argudín, M.Á., Mendoza, M.C., & Rodicio, M.R. (2010). Food poisoning and Staphylococcus aureus enterotoxins. Toxins, 2(7), 1751-1773.
DOI: https://doi.org/10.3390/toxins2071751 DOI: https://doi.org/10.3390/toxins2071751
Awosile, B.B., McClure, J.T., Saab, M.E., & Heider, L.C. (2018). Antimicrobial resistance in bacteria isolated from cats and dogs from the Atlantic Provinces, Canada from 1994-2013. The Canadian Veterinary Journal, 59(8), 885-893.
Bertelloni, F., Cagnoli, G., & Ebani, V.V. (2021). Virulence and antimicrobial resistance in canine Staphylococcus spp. isolates. Microorganisms, 9(3), 515.
DOI: https://doi.org/10.3390/microorganisms9030515 DOI: https://doi.org/10.3390/microorganisms9030515
Berube, B.J., & Bubeck Wardenburg, J. (2013). Staphylococcus aureus α-toxin: nearly a century of intrigue. Toxins, 5(6), 1140-1166.
DOI: https://doi.org/10.3390/toxins5061140 DOI: https://doi.org/10.3390/toxins5061140
Bitrus, A.A., Zunita, Z., Bejo, S.K., Othman, S., & Nadzir, N.A.A. (2016). Detection of virulence genes and antibiotic resistance profiles of Staphylococcus aureus isolated from animals. Malaysian Journal of Microbiology, 12(6), 408-417.
DOI: https://doi.org/10.21161/mjm.s00116 DOI: https://doi.org/10.21161/mjm.s00116
Castanheira, M., Watters, A.A., Mendes, R.E., Farrell, D.J., & Jones, R.N. (2010). Occurrence and molecular characterization of fusidic acid resistance mechanisms among Staphylococcus spp. from European countries (2008). Journal of Antimicrobial Chemotherapy, 65(7), 1353-1358.
DOI: https://doi.org/10.1093/jac/dkq094 DOI: https://doi.org/10.1093/jac/dkq094
Chuprom, J., Kidsin, K., Sangkanu, S., Nissapatorn, V., Wiart, C., de Lourdes Pereira, M., Tipmanee, V. (2023). Knema retusa is antibacterial and antibiofilm against antibiotic resistant Staphylococcus aureus and S. haemolyticus isolated in bovine mastitis. Veterinary Research Communications, 47(2), 523-538.
DOI: https://doi.org/10.1007/s11259-022-09999-0 DOI: https://doi.org/10.1007/s11259-022-09999-0
CLSI (Clinical and Laboratory Standards Institute). (2023). Performance standards for antimicrobial susceptibility testing (33rd ed.). CLSI supplement M100. Clinical and Laboratory Standards Institute, Wayne, USA, M100-Ed33, 98-103p.
Dinges, M.M., Orwin, P.M., & Schlievert, P.M. (2000). Exotoxins of Staphylococcus aureus. Clinical Microbiology Reviews, 13(1), 16-34.
DOI: https://doi.org/10.1128/CMR.13.1.16 DOI: https://doi.org/10.1128/CMR.13.1.16
Drougka, E., Foka, A., Koutinas, C.K., Jelastopulu, E., Giormezis, N., Farmaki, O., Spiliopoulou, I. (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.
DOI: https://doi.org/10.1016/j.prevetmed.2016.02.004 DOI: https://doi.org/10.1016/j.prevetmed.2016.02.004
Escher, M., Vanni, M., Intorre, L., Caprioli, A., Tognetti, R., & Scavia, G. (2011). Use of antimicrobials in companion animal practice: a retrospective study in a veterinary teaching hospital in Italy. Journal of Antimicrobial Chemotherapy, 66(4), 920-927.
DOI: https://doi.org/10.1093/jac/dkq543 DOI: https://doi.org/10.1093/jac/dkq543
Foster, T.J., Geoghegan, J.A., Ganesh, V.K., & Höök, M. (2014). Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nature Reviews Microbiology, 12(1), 49-62.
DOI: https://doi.org/10.1038/nrmicro3161 DOI: https://doi.org/10.1038/nrmicro3161
Foster, T.J., & Höök, M. (1998). Surface protein adhesins of Staphylococcus aureus. Trends in Microbiology, 6(12), 484-488.
DOI: https://doi.org/10.1016/S0966-842X(98)01400-0 DOI: https://doi.org/10.1016/S0966-842X(98)01400-0
Fraser, J.D., & Proft, T. (2008). The bacterial superantigen and superantigen‐like proteins. Immunological Reviews, 225(1), 226-243.
DOI: https://doi.org/10.1111/j.1600-065X.2008.00681.x DOI: https://doi.org/10.1111/j.1600-065X.2008.00681.x
Hoffmann, A.R., Proctor, L., Surette, M., & Suchodolski, J. (2016). The microbiome: the trillions of microorganisms that maintain health and cause disease in humans and companion animals. Veterinary Pathology, 53(1), 10-21.
DOI: https://doi.org/10.1177/0300985815595517 DOI: https://doi.org/10.1177/0300985815595517
Hooper, D.C. (2003). Mechanisms of quinolone resistance. Quinolone Antimicrobial Agents, 3rd ed.; ASM Press: Washington, DC, USA, 2003; pp. 41–67.
DOI: https://doi.org/10.1128/9781555817817.ch3 DOI: https://doi.org/10.1128/9781555817817.ch3
Huang, T.M., & Chou, C.C. (2019). Methicillin‐sensitive and methicillin‐resistant Staphylococcus aureus strains and their toxin genes in the nostrils of dogs and workers at an animal shelter. Journal of Applied Microbiology, 126(6), 1899-1909.
DOI: https://doi.org/10.1111/jam.14266 DOI: https://doi.org/10.1111/jam.14266
Huerta, B., Maldonado, A., Ginel, P.J., Tarradas, C., Gómez-Gascón, L., Astorga, R.J., & Luque, I. (2011). Risk factors associated with the antimicrobial resistance of staphylococci in canine pyoderma. Veterinary Microbiology, 150, 302-308.
DOI: https://doi.org/10.1016/j.vetmic.2011.02.002 DOI: https://doi.org/10.1016/j.vetmic.2011.02.002
Huseby, M., Shi, K., Brown, C.K., Digre, J., Mengistu, F., Seo, K.S., Bohach, G.A., Schlievert, P.M., Ohlendorf, D.H., & Earhart, C.A. (2007). Structure and biological activities of beta toxin from Staphylococcus aureus. Journal of Bacteriology, 189(23), 8719-8726.
DOI: https://doi.org/10.1128/JB.00741-07
Huseby, M.J., Kruse, A.C., Digre, J., Kohler, P.L., Vocke, J.A., Mann, E.E., & Ohlendorf, D.H. (2010). Beta toxin catalyzes formation of nucleoprotein matrix in staphylococcal biofilms. Proceedings of the National Academy of Sciences, 107(32), 14407-14412. DOI: https://doi.org/10.1073/pnas.0911032107
DOI: https://doi.org/10.1128/JB.00741-07 DOI: https://doi.org/10.1128/JB.00741-07
Jin, M., Osman, M., Green, B.A., Yang, Y., Ahuja, A., Lu, Z., & Cazer, C.L. (2023). Evidence for the transmission of antimicrobial resistant bacteria between humans and companion animals: A scoping review. One Health, 17, 100593.
DOI: https://doi.org/10.1016/j.onehlt.2023.100593 DOI: https://doi.org/10.1016/j.onehlt.2023.100593
Korani, A. M., Ahmadi, E., & Derakhshan, S. (2026). Molecular profiling of methicillin‑resistant Staphylococcus aureus isolated from healthy pet dogs and their owners in western Iran. Iranian Journal of Microbiology, 18(2), 251-261.
DOI: https://doi.org/10.18502/ijm.v18i2.21302 DOI: https://doi.org/10.18502/ijm.v18i2.21302
Lai, C. H., Ma, Y.C., Shia, W.Y., Hsieh, Y.L., & Wang, C.M. (2022). Risk factors for antimicrobial resistance of Staphylococcus species isolated from dogs with superficial pyoderma and their owners. Veterinary Sciences, 9(7), 306.
DOI: https://doi.org/10.3390/vetsci9070306 DOI: https://doi.org/10.3390/vetsci9070306
Lindsay, J.A., & Holden, M.T. (2004). Staphylococcus aureus: superbug, super genome? Trends in Microbiology, 12(8), 378-385.
DOI: https://doi.org/10.1016/j.tim.2004.06.004 DOI: https://doi.org/10.1016/j.tim.2004.06.004
Loeffler, A., & Lloyd, D.H. (2018). What has changed in canine pyoderma? A narrative review. The Veterinary Journal, 235, 73-82.
DOI: https://doi.org/10.1016/j.tvjl.2018.04.002 DOI: https://doi.org/10.1016/j.tvjl.2018.04.002
Lowy, F.D. (2003). Antimicrobial resistance: the example of Staphylococcus aureus. The Journal of Clinical Investigation, 111(9), 1265-1273.
DOI: https://doi.org/10.1172/JCI18535 DOI: https://doi.org/10.1172/JCI18535
Magiorakos, A.P., Srinivasan, A., Carey, R.B., Carmeli, Y., Falagas, M., Giske, C., Olsson Liljequist, B. (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection, 18(3), 268-281.
DOI: https://doi.org/10.1111/j.1469-0691.2011.03570.x DOI: https://doi.org/10.1111/j.1469-0691.2011.03570.x
Makwana, P., Parmar, S., Vala, J., Parasana, D., Patel, D., Kalyani, I., & Solanki, J. (2023). Molecular characterization and antimicrobial-resistant pattern of Staphylococcus species isolated from pyoderma cases in dogs. Biological Forum, 15(11), 82-87.
Moraveji, Z., Tabatabaei, M., Aski, H.S., & Khoshbakht, R. (2014). Characterization of hemolysins of Staphylococcus strains isolated from human and bovine, southern Iran. Iranian Journal of Veterinary Research, 15(4), 326.
Morris, D.O., & Cole, S.D. (2023). The epidemiology of antimicrobial resistance and transmission of cutaneous bacterial pathogens in domestic animals. Journal of the American Veterinary Medical Association, 261(1), 122-129.
DOI: https://doi.org/10.2460/javma.22.12.0557 DOI: https://doi.org/10.2460/javma.22.12.0557
Musa, M.D. (2024). Prevalence and Risk Factors for Staphylococcus aureus Nasal Carriage in Healthy Companion Animals in Al-Nasiriyah, Iraq. Journal of Bacteriology and Virology, 54(4), 355-366.
DOI: https://doi.org/10.4167/jbv.2024.54.4.355 DOI: https://doi.org/10.4167/jbv.2024.54.4.355
Mustak, H.K., & Esendal, Ö.M. (2010). Detection of exfoliative toxin in Staphylococcus spp. isolated from skins of healthy dogs and dogs with skin lesions. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 57(4), 247-252.
DOI: https://doi.org/10.1501/Vetfak_0000002433 DOI: https://doi.org/10.1501/Vetfak_0000002433
Nalça, A., & Gülhan, T. (2021). Mastitisli sığırlardan izole edilen Staphylococcus aureus izolatlarının virülens gen profillerinin belirlenmesi. Harran University Journal of the Faculty of Veterinary Medicine, 10(2), 144-152.
DOI: https://doi.org/10.31196/huvfd.978277 DOI: https://doi.org/10.31196/huvfd.978277
Nemati, M., Hermans, K., Lipinska, U., Denis, O., Deplano, A., Struelens, M., Haesebrouck, F. (2008). Antimicrobial resistance of old and recent Staphylococcus aureus isolates from poultry: first detection of livestock-associated methicillin-resistant strain ST398. Antimicrobial Agents and Chemotherapy, 52(10), 3817-3819.
DOI: https://doi.org/10.1128/AAC.00613-08 DOI: https://doi.org/10.1128/AAC.00613-08
Older, C.E., Rodrigues Hoffmann, A., Hoover, K., & Banovic, F. (2020). Characterization of cutaneous bacterial microbiota from superficial pyoderma forms in atopic dogs. Pathogens, 9(8), 638.
DOI: https://doi.org/10.3390/pathogens9080638 DOI: https://doi.org/10.3390/pathogens9080638
Otto, M. (2008). Staphylococcal biofilms. Bacterial Biofilms, 322, 207-228.
DOI: https://doi.org/10.1007/978-3-540-75418-3_10 DOI: https://doi.org/10.1007/978-3-540-75418-3_10
Patti, J.M., Allen, B.L., McGavin, M.J., & Hook, M. (1994). MSCRAMM-mediated adherence of microorganisms to host tissues. Annual Review of Microbiology, 48, 585-618.
DOI: https://doi.org/10.1146/annurev.mi.48.100194.003101 DOI: https://doi.org/10.1146/annurev.mi.48.100194.003101
Peacock, S.J., Moore, C.E., Justice, A., Kantzanou, M., Story, L., Mackie, K., Day, N.P. (2002). Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infection and Immunity, 70(9), 4987-4996.
DOI: https://doi.org/10.1128/IAI.70.9.4987-4996.2002 DOI: https://doi.org/10.1128/IAI.70.9.4987-4996.2002
Putriningsih, P.A.S., Phuektes, P., Jittimanee, S., & Kampa, J. (2023). Methicillin-resistant Staphylococci in canine pyoderma in Thailand. Veterinary World, 16(11), 2340.
DOI: https://doi.org/10.14202/vetworld.2023.2340-2348 DOI: https://doi.org/10.14202/vetworld.2023.2340-2348
Sareyyüpoğlu, B., Müştak, H.K., Cantekin, Z., & Diker, K.S. (2013). Molecular detection of exfoliative toxin in Staphylococcus intermedius isolates from dogs with pyoderma. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 60(1), 15-19.
DOI: https://doi.org/10.1501/Vetfak_0000002547 DOI: https://doi.org/10.1501/Vetfak_0000002547
Shallcross, L.J., Fragaszy, E., Johnson, A.M., & Hayward, A.C. (2013). The role of the Panton Valentine leucocidin toxin in staphylococcal disease: a systematic review and meta-analysis. The Lancet Infectious Diseases, 13(1), 43-54.
DOI: https://doi.org/10.1016/S1473-3099(12)70238-4 DOI: https://doi.org/10.1016/S1473-3099(12)70238-4
Sinha, B., François, P. P., Nüße, O., Foti, M., Hartford, O.M., Vaudaux, P., Krause, K.H. (1999). Fibronectin‐binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin α5β1. Cellular Microbiology, 1(2), 101-117.
DOI: https://doi.org/10.1046/j.1462-5822.1999.00011.x DOI: https://doi.org/10.1046/j.1462-5822.1999.00011.x
Somayaji, R., Priyantha, M., Rubin, J., & Church, D. (2016). Human infections due to Staphylococcus pseudintermedius, an emerging zoonosis of canine origin: report of 24 cases. Diagnostic Microbiology and Infectious Disease, 85(4), 471-476.
DOI: https://doi.org/10.1016/j.diagmicrobio.2016.05.008 DOI: https://doi.org/10.1016/j.diagmicrobio.2016.05.008
Suepaul, S., Stegger, M., Boyen, F., Georges, K., & Butaye, P. (2023). The diversity and zoonotic potential of Staphylococcus pseudintermedius in humans and pet dogs in Trinidad and Tobago. Antibiotics, 12(8), 1266.
DOI: https://doi.org/10.3390/antibiotics12081266 DOI: https://doi.org/10.3390/antibiotics12081266
Tanabe, T., Toyoguchi, M., Hirano, F., Chiba, M., Onuma, K., & Sato, H. (2013). Prevalence of staphylococcal enterotoxins in Staphylococcus pseudintermedius isolates from dogs with pyoderma and healthy dogs. Microbiology and Immunology, 57(9), 651-654.
DOI: https://doi.org/10.1111/1348-0421.12069 DOI: https://doi.org/10.1111/1348-0421.12069
Türkyilmaz, S., & Kaya, O. (2006). Determination of some virulence factors in Staphylococcus spp. isolated from various clinical samples. Turkish Journal of Veterinary & Animal Sciences, 30(1), 127-132.
Vandenesch, F., Lina, G., & Henry, T. (2012). Staphylococcus aureus hemolysins, bi-component leukocidins, and cytolytic peptides: a redundant arsenal of membrane-damaging virulence factors? Frontiers in Cellular and Infection Microbiology, 2, 12.
DOI: https://doi.org/10.3389/fcimb.2012.00012 DOI: https://doi.org/10.3389/fcimb.2012.00012
Youn, J.H., Koo, H.C., Ahn, K.J., Lim, S.-K., & Park, Y.H. (2011). Determination of staphylococcal exotoxins, SCCmec types, and genetic relatedness of Staphylococcus intermedius group isolates from veterinary staff, companion animals, and hospital environments in Korea. Journal of Veterinary Science, 12(3), 221-226.
DOI: https://doi.org/10.4142/jvs.2011.12.3.221 DOI: https://doi.org/10.4142/jvs.2011.12.3.221
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