Occurrence and antimicrobial susceptibility patterns of canine Staphylococcus pseudintermedius strains isolated from two different Italian university veterinary hospitals
VetIt.2195.12897.1

Supplementary Files

Table I
Table II

Keywords

Methicillin-resistant and methicillin-susceptible S. pseudintermediu
Dog
Antibiotic resistance
University veterinary hospitals

How to Cite

Nocera, F. P., Meroni, G., Fiorito, F., De Martino, L., & Martino, P. A. (2020). Occurrence and antimicrobial susceptibility patterns of canine Staphylococcus pseudintermedius strains isolated from two different Italian university veterinary hospitals. Veterinaria Italiana, 56(4), 263-269. https://doi.org/10.12834/VetIt.2195.12897.1

Abstract

Staphylococcus pseudintermedius represents one of the most frequently bacteria isolated on dog's skin and it was recently recognized as a zoonotic pathogen responsible for severe diseases also in humans. This study aimed to define the occurrence of canine methicillin-resistant and methicillin-susceptible S. pseudintermedius (MRSP and MSSP) strains and to compare their antimicrobial profiles. The study was carried out at veterinary microbiology laboratories of two different Italian veterinary teaching hospitals, Milan and Naples, from 2015 to 2017. The statistical comparison of the results revealed significant differences in MRSP occurrence (p-value = 0.0435) and MRSP and MSSP antibiotic resistance profiles. In Milan, MRSP strains displayed significantly higher antibiotic resistance percentages (p < 0.001) for some antibiotics, such as ceftriaxone and tobramycin, compared to those of Naples. Conversely, MSSP strains of Naples presented significantly higher rates (p < 0.001) of resistance to amoxicillin/clavulanic acid, kanamycin, erythromycin, and tetracycline than to Milan isolates. In conclusion, the results highlighted relevant variances among region-specific antibiotic resistance profiles, probably due to different antimicrobial selection pressures. Therefore, this study stands out the need for continuous monitoring of both MRSP and MSSP linked to different geographical areas, also considering their impact and importance on animal and human health.
https://doi.org/10.12834/VetIt.2195.12897.1
VetIt.2195.12897.1

References

Adwan K. 2014. Fast DNA isolation and PCR protocols for detection of methicillin-resistant staphylococci. Folia Microbiol (Praha), 59, 5-8.

Bannoehr J. & Guardabassi L. 2012. Staphylococcus pseudintermedius in the dog: taxonomy, diagnostics, ecology, epidemiology and pathogenicity. Vet Dermatol, 23, 253-266.

Boerlin P., Burnens A.P., Frey J., Kuhnert P. & Nicolet J. 2001. Molecular epidemiology and genetic linkage of macrolide and aminoglycoside resistance in Staphylococcus intermedius of canine origin. Vet Microbiol, 79, 155-169.

Bond R. & Loeffler A. 2012. What's happened to Staphylococcus intermedius? Taxonomic revision and emergence of multidrug resistance. J Small Anim Pract, 53, 147-154.

Chovanovà R., Mikulášová M. & Vaverková S. 2016. Modulation of mecA gene expression by essential oil from Salvia sclarea and synergism with oxacillin in methicillin resistant Staphylococcus epidermidiscarrying different types of Staphylococcal chromosomal cassette mec. Int J Microbiol, 6475837.

Clinical and Laboratory Standards Institute (CLSI) 2015. Performance standard for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals, 3rd Edition CLSI VET01S (Wayne, Pennsylvannia, Clinical Laboratory and Standards Institute), 128, 2015.

Corrente M., Ventrella G., Greco M.F., Martella V., Parisi A. & Buonavoglia D. 2013. Characterisation of a catalse-negative methicillin-resistant Staphylococcus aureus isolate from a dog. Vet Microbiol, 167, 734-736.

De Martino L., Nocera F.P., Mallardo K., Nizza S., Masturzo E., Fiorito F., Iovane G. & Catalanotti P. 2016. An update on microbiological causes of canine otitis externa in Campania Region - Italy. Asian Pac J Trop Biomed, 6 (5), 384-389.

Deurenberg R.H., Vink C., Kalenic S., Friedrich A.W., Bruggeman A.C. & Stobberingh E.E. 2007. The molecular evolution of methicillin-resistant of Staphylococcus aureus. Clin Microbiol Infect, 13, 222-235.

Devriese L.A., Vancanneyt M., Baele M., Vaneechoutte M., De Graef E., Snauwaert C., Cleenwerck I., Dawyndt P., Swings J., Decostere A. & Haesebrouck F. 2005. Staphylococcus pseudintermedius sp. nov., a coagulase-positive species from animals. Int J Syst Evol Microbiol, 55, 1569-1573.

Fitzgerald J.R. 2009. The Staphylococcus intermediusgroup of bacterial pathogens: species reclassification, pathogenesis and the emergence of methicillin resistance. Vet Dermatol, 20, 490-495.

Ganiere J.P., Medaille C. & Mangion C. 2005. Antimicrobial drug susceptibility of Staphylococcus intermedius clinical isolates from canine pyoderma. J Vet Med B Infect Dis Vet Public Health, 52, 25-31.

Garbacz K., Zarnowska S., Piechowcz L. & Haras K. 2013. Pathogenicity potential of Staphylococcus pseudintermedius strains isolated from canine carriers and from dogs with infection signs. Virulence, 4, 255-259.

Gómez-Sanz E., Torres C., Lozano C. & Zarazaga M. 2013. High diversity of Staphylococcus aureus and Staphylococcus pseudintermedius lineages and toxigenic traits in healthy pet-owing household members. Underestimating normal household contact? Comp Immunol Microbiol Infec Dis, 36, 83-94.

Haenni M., de Moraes N.A., Châtre P., Médaille C., Moodley A. & Madec J.Y. 2014. Characterisation of clinical canine methicillin-resistant and methicillin-susceptible Staphylococcus pseudintermedius in France. J Glob Antimicrob Resist, 2, 119-123.

Iyori K., Hisatsune J., Kawakami T., Shibata S., Murayama N., Ide K., Nagata M., Fukata T., Iwasaki T., Oshima K., Hattori M., Sugai M. & Nishifuji K. 2010. Identification of a novel Staphylococcus pseudintermedius exfoliative toxin gene and its prevalence in isolates from canines with pyoderma and healthy dogs. FEMS Microbiol Lett, 312, 169-175.

Kang M.H., Chae M.J., Yoo J.W., Kim S.G., Lee S.Y., Yoo J.H. & Park H.M. 2014. Antibiotic resistance and molecular characterization of ophthalmic Staphylococcus pseudintermedius isolates from dogs. J Vet Sci, 15, 409-415.

Kasai T., Saesuga S., Shirai M., Murakami M. & Kato Y. 2016. New categories designated as healthcare-associated and community-associated methicillin-resistant Staphylococcus pseudintermedius. Microbiol Immunol, 60, 540-551.

Loeffler A., Linek M., Moodley A., Guardabassi L., Sung J.M., Winkler M., Weiss R. & Lloyd D.H. 2007. First report of multiresistant, mecA-positive Staphylococcus intermedius in Europe: 12 cases from a veterinary dermatology referral clinic in Germany. Vet Dermatol, 18, 412-421.

Lozano C., Rezusta A., Ferrer I., Pérez-Laguna V., Zarazaga M., Ruiz-Ripa L., Revillo M.J. & Torres C. 2017. Staphylococcus pseudintermedius human infection cases in Spain: dog-to-human transmission. Vector Borne Zoonotic Dis, 17, 268-270.

Lüthje P. & Schwarz S. 2007. Molecular basis of resistance to macrolides and lincosamides among staphylococci and streptococci from various animal sources collected in the resistance monitoring program BfT-GermVet. Inter J Antimicrob Agents, 29, 528-535.

Moodley A., Damborg P. & Nielsen S.S. 2014. Antimicrobial resistance in methicillin susceptible and methicillin resistant Staphylococcus pseudintermedius of canine origin: literature review from 1980 to 2013. Vet Microbiol, 171, 337-341.

Nisa S., Bercker C., Midwinter A.C., Bruce I., Graham C.F., Venter P., Bell A., French N.P., Benschop J., Bailey K.M. & Wilkinson D.A. 2019. Combining MALDI-TOF and genomics in the study of methicillin resistant and multidrug resistant Staphylococcus pseudintermedius in New Zealand. Sci Rep, 9, 1271.

Norström M., Sunde M., Tharaldsen H., Mørk T., Bergsjø B. & Kruse H. 2009. Antimicrobial resistance in Staphylococcus pseudintermedius in the Norwegian dog population. Microb Drug Resist, 15, 55-59.

Osland A.M., Vestby L.K., Fanuelsen H., Slettemeås J.S. & Sunde M. 2012. Clonal diversity and biofilm-forming ability of methicillin-resistant Staphylococcus pseudintermedius. J Antimicrob Chemother, 67, 841-848.

Paul N.C., Moodley A., Ghibaudo G. & Guardabassi L. 2011. Carriage of methicillin-resistant Staphylococcus pseudintermedius in small animal veterinarians: indirect evidence of zoonotic transmission. Zoonoses and Public Health, 58, 533-539.

Perreten V., Kadlec K., Schwarz S., Grönlund Andersson U., Finn M., Greko C., Moodley A., Kania S.A., Frank L.A., Bemis D.A., Franco A., Iurescia M., Battisti A., Duim B., Wagenaar J.A., van Duijkeren E., Weese J.S., Fitzgerald J.R., Rossano A. & Guardabassi L. 2010. Clonal spread of methicillin-resistant Staphylococcus pseudintermedius in Europe and North America: an international multicenter study. J Antimicrob Chemother, 65, 1145-1154.

Robb A.R., Wright E.D., Foster A.M.E., Walker R. & Malone C. 2017. Skin infection caused by a novel strain of Staphylococcus pseudintermedius in a Siberian husky dog owner. JJM Case Rep, 4, jmmcr005087.

Santos A.F., Cayô R., Schandert L. & Gales A.C. 2013. Evaluation of MALDI-TOF MS in the microbiology laboratory. J Bras Patol Med Lab, 49, 191-197.

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. J Clin Microbiol, 48, 765-769.

Schmitz F.J., Krey A., Sadurski R., Verhoef J., Milatovic D., Fluit A.C. & European SENTRY Participants 2001. Resistance to tetracycline and distribution of tetracycline genes in European Staphylococcus aureus isolates. J Antimicrob Chemother, 47, 239-240.

Somayaji R., Rubin J.E., Priyantha M.A. & Church D. 2016. Exploring Staphylococcus pseudintermedius: an emerging zoonotic pathogen? Future Microbiol, 11, 1371-1374.

Stefanetti V., Bietta A., Pascucci L., Marenzoni M.L., Coletti M., Franciosini M.P., Passamonti F. & Casagrande Proietti P. 2017. Investigation of the antibiotic resistance and biofilm formation of Staphylococcus pseudintermedius strains isolated from canine pyoderma. Vet Ital, 53, 289-296.

Stegger M., Andersen P.S., Kearns A., Pichon B., Holmes M.A., Edwards G., Laurent F., Teale C., Skov R. & Larse A.R. 2012. Rapid detection, differentiation and typing of methicillin-resistant Staphylococcus aureus harbouring either mecA or the new mecA homologue mecALGA251. Clin Microbiol Infect,18, 395-400.

Stegmann R., Burnens A., Maranta C.A. & Perreten V. 2010. Human infection associated with methicillin-resistant Staphylococcus pseudintermedius ST71. J Antimicrob Chemoter, 65, 2047-2048.

Strommenger B., Kettlitz C., Werner G. & 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.

Sutcliffe J., Tait-Kamradt A. & Wondrack L. 1996. Streptococcus pneumoniae and Streptococcus pyogenes resistant to macrolides but sensitive to clindamycin: a common resistance pattern mediated by an efflux system. Antimicrob Agents Chemother, 40, 1817-1824.

Ullah F., Malik S.A., Ahmed J., Ullah F., Shah S.M., Ayaz M., Hussain S. & Khatoon L. 2012. Investigation of the genetic basis of tetracycline resistance in Staphylococcus aureus from Pakistan. Trop J Pharm Res, 11, 925-931.

van Duijkeren E., Kamphuis M.I.C., Mije V., Laarhoven L.M., Duim B., Wagenaar J.A. & Houwers D.J. 2011. Staphylococcus pseudintermedius between infected dogs and cats and contact pets, humans and the environment in households and veterinary clinics. Vet Microbiol, 150, 338-343.

Van Hoovels L., Vankeerberghen A., Boel A., Van Vaerenbergh K. & De Beenhouwer H. 2006. First case of Staphylococcus pseudintermedius infection in a human. J Clin Microbiol, 44, 4609-4612.

Weese J.S. & van Duijkeren E. 2010. Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in veterinary medicine. Vet Microbiol, 140, 418-429.

Wettstein K., Descloux S., Rossano A. & Perreten V. 2008. Emergence of methicillin-resistant Staphylococcus pseudintermedius in Switzerland: three cases of urinary tract infections in cats. Schweiz Arch Tierheilkd, 150, 339-343.

Yoon J.W., Lee K.J., Lee S.Y., Chae M.J., Park J.K., Yoo J.H. & Park H.M. 2010. Antibiotic resistance profiles of Staphylococcus pseudintermedius isolates from canine patients in Korea. J Microbiol Biotechnol, 20, 1764-1768.

Youn J.H., Park Y.H., Hang' ombe B. & Sugimoto C. 2014. Prevalence and characterization of Staphylococcus aureus and Staphylococcus pseudintermedius isolated from companion animals and environment in the veterinary teaching hospital in Zambia, Africa. Comp Immunol Microbiol Infect Dis, 37, 123-130.