PARTICIPATION AND DRUG RESISTANCE OF COAGULASE-POSITIVE STAPHYLOCOCCI ISOLATED FROM CASES OF PYODERMA AND OTITIS EXTERNA IN DOGS

Authors

  • Małgorzata Szewczuk West Pomeranian University of Technology, Department of Ruminant Science, Klemensa Janickiego 29, 71-270 Szczecin, Poland
  • Sławomir Zych Veterinary Laboratory “Labo-Wet” Sp. z o.o., Pyrzycka 9A, 70-892 Szczecin, Poland
  • Piotr Sablik West Pomeranian University of Technology, Department of Ruminant Science, Klemensa Janickiego 29, 71-270 Szczecin, Poland

DOI:

https://doi.org/10.26873/SVR-926-2019

Abstract

Staphylococcus pseudintermedius is considered as a major pathogen in dogs, typically involved in skin and ear infections. Other staphylococci, as well as β-hemolytic streptococci, Pseudomonas aeruginosa or yeast-like fungi of the genus Malassezia also play an important role in inflammation. Because of this diversity, an appropriate choice of antimicrobial agent(-s) can be difficult. A total of 474 tests were performed (including 255 pyoderma and 219 otitis externa cases). In the case of pyoderma, 82.4% of skin lesions were caused by staphylococci. Co-infections with β-hemolytic streptococci (17.3 %), Malassezia sp. (15.7 %) and P. aeruginosa (4.3 %) were also recorded. For external ear infections, the share of staphylococci in inflammation was lower (44.8 %) than that of Malassezia sp. (58 %). Relatively frequent co-infections with β-hemolytic streptococci (18.8 %) and P. aeruginosa (7.8 %) were also noted. A total of 308 susceptibility tests for coagulase-positive staphylococci were performed (210 and 98 for skin and otitis externa, respectively). In ≥ 86 % of cases, amoxicillin potentiated with clavulanic acid, cephalexin and fluoroquinolones effectively inhibited the growth of all bacteria in vitro. A total of 25 isolates (24 S. pseudintermedius and one S. aureus) were considered as methicillin-resistant. The mecA gene was identified in 100 % of those strains but only 44 % of the isolates additionally carried the blaZ gene. All mecA-positive staphylococci were multidrug-resistant, mainly to all β-lactams, fluoroquinolones, linkozamides, macrolides as well as sulfonamides but always susceptible to mupirocin. Overall, multidrug-resistance varied between 6 % (otitis externa) and 9 % (inflamed skin) and may become a significant problem in the future.

Key words: pyoderma; otitis externa; dog; staphylococci; multidrug resistance; mecA, mupirocin

PARTICIPATION AND DRUG RESISTANCE OF COAGULASE-POSITIVE STAPHYLOCOCCI ISOLATED FROM CASES OF PYODERMA AND OTITIS EXTERNA IN DOGS

Povzetek: Staphylococcus pseudintermedius is considered as a major pathogen in dogs, typically involved in skin and ear infections. Other staphylococci, as well as β-hemolytic streptococci, Pseudomonas aeruginosa or yeast-like fungi of the genus Malassezia also play an important role in inflammation. Because of this diversity, an appropriate choice of antimicrobial agent(-s) can be difficult. A total of 474 tests were performed (including 255 pyoderma and 219 otitis externa cases). In the case of pyoderma, 82.4 % of skin lesions were caused by staphylococci. Co-infections with β-hemolytic streptococci (17.3 %), Malassezia sp. (15.7 %) and P. aeruginosa (4.3 %) were also recorded. For external ear infections, the share of staphylococci in inflammation was lower (44.8%) than that of Malassezia sp. (58 %). Relatively frequent co-infections with β-hemolytic streptococci (18.8 %) and P. aeruginosa (7.8 %) were also noted. A total of 308 susceptibility tests for coagulase-positive staphylococci were performed (210 and 98 for skin and otitis externa, respectively). In ≥ 86 % of cases, amoxicillin potentiated with clavulanic acid, cephalexin and fluoroquinolones effectively inhibited the growth of all bacteria in vitro. A total of 25 isolates (24 S. pseudintermedius and one S. aureus) were considered as methicillin-resistant. The mecA gene was identified in 100 % of those strains but only 44 % of the isolates additionally carried the blaZ gene. All mecA-positive staphylococci were multidrug-resistant, mainly to all β-lactams, fluoroquinolones, linkozamides, macrolides as well as sulfonamides but always susceptible to mupirocin. Overall, multidrug-resistance varied between 6 % (otitis externa) and 9 % (inflamed skin) and may become a significant problem in the future.

Ključne besede: pyoderma; otitis externa; dog; staphylococci; multidrug resistance; mecA, mupirocin

References

(1.) Loeffler A, Lloyd DH. Pyoderma, the march of the staphylococci. Vet Dermatol 2014; 25: 285–6.

(2.) Dégi J, Imre K, Catana N, Morar A, Sala C, Herman V. Frequency of isolation and antibiotic resistance of staphylococcal flora from external otitis of dogs. Vet Rec 2013; 173: 42.

(3.) Gross TL, Ihrke PJ, Walder EJ, Affolter VK. Skin diseases of the dog and cat: clinical and histopathologic diagnosis, 2nd ed. Oxford : Blackwell Publishing, 2005: 1–944.

(4.) Forster SL, Real T, Doucette KP, King SB. A randomized placebo-controlled trial of the efficacy and safety of a terbinafine, florfenicol and betamethasone topical ear formulation in dogs for the treatment of bacterial and/or fungal otitis externa. BMC Vet Res 2018; 14: e262.

(5.) Löwenstein C. Pyodermie beim Hund [Pyoderma in dogs]. Tierarztl Prax Ausg K Kleintiere Heimtiere 2011; 39: 405–17.

(6.) Duijkeren van E, Catry B, Greko C, et al. Review on methicillin-resistant Staphylococcus pseudintermedius. J Antimicrob Chemother 2011; 66: 2705–14.

(7.) Bannoehr J, Guardabassi L. Staphylococcus pseudintermedius in the dog: taxonomy, diagnostics, ecology, epidemiology and pathogenicity. Vet Dermatol 2012; 23: 253–66.

(8.) Paul NC, Latronico F, Moodley A, Nielsen SS, Damborg P, Guardabassi L. In vitro adherence of Staphylococcus pseudintermedius to canine corneocytes is influenced by colonization status of corneocyte donors. Vet Res 2013; 8: 44–52.

(9.) Min SH, Kang MH, Sur JH, Park HM. Staphylococcus pseudintermedius infection associated with nodular skin lesions and systemic inflammatory response syndrome in a dog. Can Vet J 2014; 55: 480–3.

(10.) Greene CE. Infectious disease of the dog and cat. 4th ed. St. Louis : Elsevier, 2012: 1–1376.

(11.) Ebani VV, Nardoni S, Bertelloni F, Najar B, Pistelli L, Mancianti F. Antibacterial and antifungal activity of essential oils against pathogens responsible for otitis externa in dogs and cats. Medicines 2017; 4: 21.

(12.) Patel A, Forsythe PJ. Saunders solutions in veterinary practice: small animal dermatology. Edinburgh, et al. : Saunders, Elsevier Health Science, 2008: 166–8.

(13.) Sasaki T, Kikuchi K, Tanaka Y, Takahashi N, Kamata S, Hiramatsu K. Reclassification of phenotypically identified Staphylococcus intermedius strains. J Clin Microbiol 2007; 45: 2770–8.

(14.) Kmieciak W, Szewczyk EM. Coagulase-positive species of the genus Staphylococcus – taxonomy, pathogenicity. Post Mikrobiol 2017; 56: 233–44. [in Polish] https://www.exeley.com/advancements_of_microbiology/doi/10.21307/PM-2017.56.2.233 (Dec. 2019)

(15.) Sasaki T, Tsubakishita S, Tanaka Y, et al. Multiplex-PCR method for species identification of coagulase-positive staphylococci. J Clin Microbiol 2010; 48: 765–9.

(16.) CLSI. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. Approved standard. 4th ed. CLSI document VET01-A4. Wayne : Clinical and Laboratory Standards Institute, 2013.

(17.) CLSI. Performance standards for antimicrobial susceptibility testing. 25th informational supplement. CLSI document M100-S25. Wayne : Clinical and Laboratory Standards Institute, 2017.

(18.) Ruzauskas M, Couto N, Pavilonis A, et al. Characterization of Staphylococcus pseudintermedius isolated from diseased dogs in Lithuania. Pol J Vet Sci 2016; 19: 7–14.

(19.) Ferreira AM, Martins KB, Silva VR, Mondelli AL, Cunha ML. Correlation of phenotypic tests with the presence of the blaZ gene for detection of beta-lactamase. Braz J Microbiol 2017; 48: 159–66.

(20.) Priyantha R, Gaunt MC, Rubin JE. Antimicrobial susceptibility of Staphylococcus pseudintermedius colonizing healthy dogs in Saskatoon, Canada. Can Vet J 2016; 57: 65–9.

(21.) Beça N, Bessa LJ, Mendes Â, et al. Coagulase-positive Staphylococcus: prevalence and antimicrobial resistance. J Am Anim Hosp Assoc 2015; 51: 365–71.

(22.) Griffeth GC, Morris DO, Abraham JL, Shofer FS, Rankin SC. Screening for skin carriage of methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi in dogs with healthy and inflamed skin. Vet Dermatol 2008; 19: 142–9.

(23.) Penna B, Varges R, Medeiros L, Martins GM, Martins RR, Lilenbaum W. Species distribution and antimicrobial susceptibility of staphylococci isolated from canine otitis externa. Vet Dermatol 2010; 21: 292–6.

(24.) Paul NC, Bargman SC, Moodley A, Nielsen SS, Guardabassi L. Staphylococcus pseudintermedius colonization patterns and strain diversity in healthy dogs: a cross-sectional and longitudinal study. Vet Microbiol 2012; 160: 420–7.

(25.) Rubin JE, Chirino-Trejo M. Prevalence, sites of colonization, and antimicrobial resistance among Staphylococcus pseudintermedius isolated from healthy dogs in Saskatoon, Canada. J Vet Diagn Invest 2011; 23: 351–4.

(26.) Grönthal T, Eklund M, Thomson K, Piiparinen H, Sironen T, Rantala M. Antimicrobial resistance in Staphylococcus pseudintermedius and the molecular epidemiology of methicillin-resistant S. pseudintermedius in small animals in Finland. J Antimicrob Chemother 2017; 72: 1021–30.

(27.) Detwiler A, Bloom P, Petersen A, Rosser EJ, Jr. Multi-drug and methicillin resistance of staphylococci from canine patients at a veterinary teaching hospital (2006–2011). Vet Q 2013; 33: 60 –7.

(28.) Bajwa J. Canine superficial pyoderma and therapeutic considerations. Can Vet J 2016; 57: 204–6.

(29.) Kjellman EE, Slettemeås JS, Small H, Sunde M. Methicillin-resistant Staphylococcus pseudintermedius (MRSP) from healthy dogs in Norway - occurrence, genotypes and comparison to clinical MRSP. MicrobiologyOpen 2015; 4: 857–66. doi: 10.1002/mbo3.258

(30.) Gold RM, Cohen ND, Lawhon SD. Amikacin resistance in Staphylococcus pseudintermedius isolated from dogs. J Clin Microbiol 2014; 52: 3641–6.

(31.) Cookson BD. The emergence of mupirocin resistance: a challenge to infection control and antibiotic prescribing practice. J Antimicrob Chemother 1998; 41: 11–18.

(32.) Matanović K, Pérez-Roth E, Pintarić S, Šeol Martinec B. Molecular characterization of high-level mupirocin resistance in Staphylococcus pseudintermedius. J Clin Microbiol 2013; 51: 1005–7.

(33.) Creagh S, Lucey B. Interpretive criteria for mupirocin susceptibility testing of Staphylococcus spp. using CLSI guidelines. Br J Biomed Sci 2007; 64: 1–5.

(34.) Opatrilova R, Jampilek J. Rapid screening of mupirocin skin permeation modification by micronized and nanonized alaptide. ADMET & DMPK 2014; 2: 56–62. doi:10.5599/admet.2.1.26

(35.) Hughes J, Mellows G. On the mode of action of pseudomonic acid: inhibition of protein synthesis in Staphylococcus aureus. J Antibiot 1978; 31: 330–5.

Downloads

Published

2020-03-31

How to Cite

Szewczuk, M., Zych, S., & Sablik, P. (2020). PARTICIPATION AND DRUG RESISTANCE OF COAGULASE-POSITIVE STAPHYLOCOCCI ISOLATED FROM CASES OF PYODERMA AND OTITIS EXTERNA IN DOGS. Slovenian Veterinary Research, 57(1). https://doi.org/10.26873/SVR-926-2019

Issue

Section

Original Research Article