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Volume 169, Issue 2

Prevalence of multidrug-resistant coagulase-positive staphylococci in canine and feline dermatological patients over a 10-year period: a retrospective study Open Access

Abstract

Coagulase-positive staphylococci (CPS) are common cutaneous pathogens often requiring multiple courses of antibiotics, which may facilitate selection for methicillin-resistant (MR) and/or multidrug-resistant (MDR) strains. To determine the prevalence of canine and feline MR/MDR CPS associated with skin diseases, medical records were retrospectively searched from April 2010 to April 2020. Pets with at least one positive culture for CPS were selected. Age, sex, antimicrobial sensitivity, previous history of antimicrobial/immunomodulatory medications and methicillin resistance/multidrug resistance status were recorded. (SP) (575/748) and (SS) (159/748) in dogs, and (12/22) in cats, were the most common CPS isolated. Three hundred and twenty-three out of 575 isolates were MR-SP (56.2 %), 304/575 were MDR-SP (52.8 %), 100/159 were MR-SS (62.9 %) and 71/159 were MDR-SS (44.6 %). A trend analysis showed a significant increase of resistance to oxacillin and chloramphenicol for (r=0.86, 0.8; =0.0007, 0.0034, respectively). Major risk factors for MDR-SP included oxacillin resistance (OR: 3; 95 % CI: 1.4–6.5; 0.0044), positivity for PBP2a (OR: 2.3; 95 % CI: 1–5; 0.031) and use of antibiotics in the previous year (OR: 2.8; 95 % CI: 1.3–5.8; =0.0071). Oxacillin resistance was identified as a major risk factor for MDR-SS (OR: 8.8; 95 % CI: 3.6–21.1; 0.0001). These results confirmed the widespread presence of MR/MDR CPS in referred dermatological patients. Judicious antibiotic use, surveillance for MR/MDR infections and consideration of alternative therapies are crucial in mitigating the development of resistant strains.

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Keyword(s): cats , coagulase-positive staphylococci , dermatology , dogs and multidrug resistance
Funding
This study was supported by the:
  • American Veterinary Medical Association
    • Principle Award Recipient: MikaelaBurke
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2023-02-14
2024-04-27
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References

  1. Jones RD, Kania SA, Rohrbach BW, Frank LA, Bemis DA. Prevalence of oxacillin- and multidrug-resistant staphylococci in clinical samples from dogs: 1,772 samples (2001-2005). J Am Vet Med Assoc 2007; 230:221–227 [View Article] [PubMed]
     [Google Scholar]
  2. Morris DO, Rook KA, Shofer FS, Rankin SC. Screening of Staphylococcus aureus, Staphylococcus intermedius, and Staphylococcus schleiferi isolates obtained from small companion animals for antimicrobial resistance: a retrospective review of 749 isolates (2003-04). Vet Dermatol 2006; 17:332–337 [View Article] [PubMed]
     [Google Scholar]
  3. Rosenstein R, Gotz F. What distinguishes highly pathogenic staphylococci from medium- and non-pathogenic?. Curr Top Microbiol Immunol 2013; 358:33–89 [View Article]
     [Google Scholar]
  4. Cain CL. Antimicrobial resistance in staphylococci in small animals. Vet Clin North Am Small Anim Pract 2013; 43:19–40 [View Article]
     [Google Scholar]
  5. Cohn LA, Middleton JR. A veterinary perspective on methicillin-resistant staphylococci. J Vet Emerg Crit Care 2010; 20:31–45 [View Article]
     [Google Scholar]
  6. Loeffler A, Lloyd DH. What has changed in canine pyoderma? A narrative review. Vet J 2018; 235:73–82 [View Article]
     [Google Scholar]
  7. Magiorakos A-P, Srinivasan A, Carey RB, Carmeli Y, Falagas ME et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012; 18:268–281 [View Article]
     [Google Scholar]
  8. Djordjevic SP, Stokes HW, Roy Chowdhury P. Mobile elements, zoonotic pathogens and commensal bacteria: conduits for the delivery of resistance genes into humans, production animals and soil microbiota. Front Microbiol 2013; 4:86 [View Article]
     [Google Scholar]
  9. Richards VP, Velsko IM, Alam T, Zadoks RN, Manning SD et al. Population gene introgression and high genome plasticity for the zoonotic pathogen Streptococcus agalactiae. Mol Biol Evol 2019; 36:2572–2590 [View Article] [PubMed]
     [Google Scholar]
  10. Morris DO, Loeffler A, Davis MF, Guardabassi L, Weese JS. Recommendations for approaches to meticillin-resistant staphylococcal infections of small animals: diagnosis, therapeutic considerations and preventative measures. Vet Dermatol 2017; 28:304–e69 [View Article]
     [Google Scholar]
  11. Lee GY, Lee H-H, Hwang SY, Hong J, Lyoo K-S et al. Carriage of Staphylococcus schleiferi from canine otitis externa: antimicrobial resistance profiles and virulence factors associated with skin infection. J Vet Sci 2019; 20:e6 [View Article]
     [Google Scholar]
  12. Beck KM, Waisglass SE, Dick HLN, Weese JS. Prevalence of meticillin-resistant Staphylococcus pseudintermedius (MRSP) from skin and carriage sites of dogs after treatment of their meticillin-resistant or meticillin-sensitive staphylococcal pyoderma. Vet Dermatol 2012; 23:369–375 [View Article] [PubMed]
     [Google Scholar]
  13. Grönthal T, Eklund M, Thomson K, Piiparinen H, Sironen T et al. Antimicrobial resistance in Staphylococcus pseudintermedius and the molecular epidemiology of methicillin-resistant S. pseudintermedius in small animals in Finland. J Antimicrob Chemother 2017; 72:1021–1030 [View Article] [PubMed]
     [Google Scholar]
  14. Kawakami T, Shibata S, Murayama N, Nagata M, Nishifuji K et al. Antimicrobial susceptibility and methicillin resistance in Staphylococcus pseudintermedius and Staphylococcus schleiferi subsp. coagulans isolated from dogs with pyoderma in Japan. J Vet Med Sci 2010; 72:1615–1619 [View Article] [PubMed]
     [Google Scholar]
  15. Nakaminami H, Okamura Y, Tanaka S, Wajima T, Murayama N et al. Prevalence of antimicrobial-resistant staphylococci in nares and affected sites of pet dogs with superficial pyoderma. J Vet Med Sci 2021; 83:214–219 [View Article] [PubMed]
     [Google Scholar]
  16. Beever L, Bond R, Graham PA, Jackson B, Lloyd DH et al. Increasing antimicrobial resistance in clinical isolates of Staphylococcus intermedius group bacteria and emergence of MRSP in the UK. Vet Rec 2015; 176:172 [View Article] [PubMed]
     [Google Scholar]
  17. Lehner G, Linek M, Bond R, Lloyd DH, Prenger-Berninghoff E et al. Case-control risk factor study of methicillin-resistant Staphylococcus pseudintermedius (MRSP) infection in dogs and cats in Germany. Vet Microbiol 2014; 168:154–160 [View Article] [PubMed]
     [Google Scholar]
  18. CLSI Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals, 1st CLSI supplement VET01S. Wayne, PA: Clinical and Laboratory Standards Institute; 2004
     [Google Scholar]
  19. CLSI Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals, 1st CLSI supplement VET01S. Wayne, PA: Clinical and Laboratory Standards Institute; 2013
     [Google Scholar]
  20. CLSI Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals, 1st CLSI supplement VET01S. Wayne, PA: Clinical and Laboratory Standards Institute; 2015
     [Google Scholar]
  21. CLSI Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals, 1st CLSI supplement VET01S. Wayne, PA: Clinical and Laboratory Standards Institute; 2018
     [Google Scholar]
  22. Gautheir TD. Detecting trends using Spearman’s rank correlation coefficient. Environmental Forensics 2001; 2:359–362 [View Article]
     [Google Scholar]
  23. Moodley A, Damborg P, Nielsen SS. Antimicrobial resistance in methicillin susceptible and methicillin resistant Staphylococcus pseudintermedius of canine origin: literature review from 1980 to 2013. Vet Microbiol 2014; 171:337–341 [View Article] [PubMed]
     [Google Scholar]
  24. Cain CL, Morris DO, Rankin SC. Clinical characterization of Staphylococcus schleiferi infections and identification of risk factors for acquisition of oxacillin-resistant strains in dogs: 225 cases (2003-2009). J Am Vet Med Assoc 2011; 239:1566–1573 [View Article] [PubMed]
     [Google Scholar]
  25. Kania SA, Williamson NL, Frank LA, Wilkes RP, Jones RD et al. Methicillin resistance of staphylococci isolated from the skin of dogs with pyoderma. Am J Vet Res 2004; 65:1265–1268 [View Article] [PubMed]
     [Google Scholar]
  26. Abraham JL, Morris DO, Griffeth GC, Shofer FS, Rankin SC. Surveillance of healthy cats and cats with inflammatory skin disease for colonization of the skin by methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi ssp. schleiferi. Vet Dermatol 2007; 18:252–259 [View Article] [PubMed]
     [Google Scholar]
  27. Ruzauskas M, Couto N, Kerziene S, Siugzdiniene R, Klimiene I et al. Prevalence, species distribution and antimicrobial resistance patterns of methicillin-resistant staphylococci in Lithuanian pet animals. Acta Vet Scand 2015; 57:27 [View Article]
     [Google Scholar]
  28. Kizerwetter-Świda M, Chrobak-Chmiel D, Rzewuska M. High-level mupirocin resistance in methicillin-resistant staphylococci isolated from dogs and cats. BMC Vet Res 2019; 15:238 [View Article]
     [Google Scholar]
  29. Evans JJ, Bolz DD. Regulation of virulence and antibiotic resistance in Gram-positive microbes in response to cell wall-active antibiotics. Curr Opin Infect Dis 2019; 32:217–222 [View Article]
     [Google Scholar]
  30. Li B, Webster TJ. Bacteria antibiotic resistance: new challenges and opportunities for implant-associated orthopedic infections. J Orthop Res 2018; 36:22–32 [View Article]
     [Google Scholar]
  31. Rousham EK, Unicomb L, Islam MA. Human, animal and environmental contributors to antibiotic resistance in low-resource settings: integrating behavioural, epidemiological and One Health approaches. Proc Biol Sci 2018; 285:20180332 [View Article]
     [Google Scholar]
  32. Hussain Z, Stoakes L, Garrow S, Longo S, Fitzgerald V et al. Rapid detection of mecA-positive and mecA-negative coagulase-negative staphylococci by an anti-penicillin binding protein 2a slide latex agglutination test. J Clin Microbiol 2000; 38:2051–2054 [View Article] [PubMed]
     [Google Scholar]
  33. Bemis DA, Jones RD, Hiatt LE, Ofori ED, Rohrbach BW et al. Comparison of tests to detect oxacillin resistance in Staphylococcus intermedius, Staphylococcus schleiferi, and Staphylococcus aureus isolates from canine hosts. J Clin Microbiol 2006; 44:3374–3376 [View Article] [PubMed]
     [Google Scholar]
  34. Paterson GK, Harrison EM, Holmes MA. The emergence of mecC methicillin-resistant Staphylococcus aureus. Trends Microbiol 2014; 22:42–47 [View Article] [PubMed]
     [Google Scholar]
  35. Platenik MO, Archer L, Kher L, Santoro D. Prevalence of mecA, mecC and Panton-Valentine-Leukocidin genes in clinical isolates of coagulase positive staphylococci from dermatological canine patients. Microorganisms 2022; 10:2239 [View Article]
     [Google Scholar]
  36. Wu MT, Burnham C-A, Westblade LF, Dien Bard J, Lawhon SD et al. Evaluation of Oxacillin and Cefoxitin disk and MIC breakpoints for prediction of methicillin resistance in human and veterinary isolates of Staphylococcus intermedius group. J Clin Microbiol 2016; 54:535–542 [View Article]
     [Google Scholar]
  37. Madhaiyan M, Wirth JS, Saravanan VS. Phylogenomic analyses of the Staphylococcaceae family suggest the reclassification of five species within the genus Staphylococcus as heterotypic synonyms, the promotion of five subspecies to novel species, the taxonomic reassignment of five Staphylococcus species to Mammaliicoccus gen. nov., and the formal assignment of Nosocomiicoccus to the family Staphylococcaceae. Int J Syst Evol Microbiol 2020; 70:5926–5936 [View Article] [PubMed]
     [Google Scholar]
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Prevalence of multidrug-resistant coagulase-positive staphylococci in canine and feline dermatological patients over a 10-year period: a retrospective study
Microbiology 169, 001300 (2023); https://doi.org/10.1099/mic.0.001300
/content/journal/micro/10.1099/mic.0.001300
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