Skip to main content

Advertisement

SpringerLink
Log in

Commensal Staphylococci Including Methicillin-Resistant Staphylococcus aureus from Dogs and Cats in Remote New South Wales, Australia

  • Host Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Staphylococci are important opportunistic pathogens in human and veterinary medicine in addition to being part of the normal flora of the skin and mucous membranes of mammals and birds. The rise of antimicrobial resistance amongst staphylococci warrants closer investigation of the diversity of skin commensal organisms—including coagulase-negative staphylococci (CoNS)—due to their potential as a source of resistance genes. This study is aimed at characterising the commensal staphylococci—including methicillin-resistant Staphylococcus species (spp.)—from mucocutaneous sites of dogs and cats from remote New South Wales (NSW), Australia. Pet dogs and cats were recruited from participants in a community companion animal health programme in six communities in western NSW. Three swabs were collected from each animal (anterior nares, oropharynx, and perineum) and from skin lesions or wounds if present and cultured on selective media for Staphylococcus spp. In total, 383 pets (303 dogs, 80 cats) were enrolled. Staphylococcus spp. were isolated from 67.3% of dogs and 73.8% of cats (494 isolates). The diversity of CoNS was high (20 species) whilst only three coagulase-positive spp. were isolated (S. pseudintermedius, S. aureus, S. intermedius). The prevalence of methicillin-resistant Staphylococcus aureus (MRSA) carriage in dogs was high (2.6%) relative to other studies but was only a small proportion of overall commensal staphylococci. No cats carried MRSA and no MRSP was isolated from either species. Dogs were significantly more likely to carry coagulase-positive staphylococci than cats (P < 0.001). Amongst dogs, males and those with skin lesions were more likely to carry S. pseudintermedius. This study highlights important differences in the diversity and patterns of carriage of commensal staphylococci between dogs and cats in remote NSW, Australia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. ABS (2016) ‘Remoteness structure’ Australian statistical geography standard (ASGS)

  2. Ahmadi M, Javadi S, Maroofi S (2009) Prevalence of coagulase-positive staphylococci in the skin of dogs; antibacterial resistance and plasmid profile of the isolates. Comp Clin Pathol 18:39–42

    CAS  Google Scholar 

  3. Alshaikh B, Yee W, Lodha A, Henderson E, Yusuf K, Sauve R (2014) Coagulase-negative staphylococcus sepsis in preterm infants and long-term neurodevelopmental outcome. J Perinatol: official journal of the California Perinatal Association 34:125–129

    CAS  Google Scholar 

  4. Bagcigil FA, Moodley A, Baptiste KE, Jensen VF, Guardabassi L (2007) Occurrence, species distribution, antimicrobial resistance and clonality of methicillin- and erythromycin-resistant staphylococci in the nasal cavity of domestic animals. Vet Microbiol 121:307–315

    PubMed  CAS  Google Scholar 

  5. Bannoehr J, Guardabassi L (2012) Staphylococcus pseudintermedius in the dog: taxonomy, diagnostics, ecology, epidemiology and pathogenicity. Vet Dermatol 23:253–266 e251–252

    PubMed  Google Scholar 

  6. Baptiste KE, Williams K, Willams NJ, Wattret A, Clegg PD, Dawson S, Corkill JE, O’Neill T, Hart CA (2005) Methicillin-resistant staphylococci in companion animals. Emerg Infect Dis 11:1942–1944

    PubMed  PubMed Central  Google Scholar 

  7. Barker SC, Walker AR (2014) Ticks of Australia. The species that infest domestic animals and humans. Zootaxa 3816:1

    Google Scholar 

  8. Bean DC, Wigmore SM (2016) Carriage rate and antibiotic susceptibility of coagulase-positive staphylococci isolated from healthy dogs in Victoria, Australia. Aust Vet J 94:456–460

    PubMed  CAS  Google Scholar 

  9. Becker K, Heilmann C, Peters G (2014) Coagulase-negative staphylococci. Clin Microbiol Rev 27:870–926

    PubMed  PubMed Central  CAS  Google Scholar 

  10. Bierowiec K, Ploneczka-Janeczko K, Rypula K (2016) Is the colonisation of Staphylococcus aureus in pets associated with their close contact with owners? PLoS One 11:e0156052

    PubMed  PubMed Central  Google Scholar 

  11. Bland IM, Guthrie-Jones A, Taylor RD, Hill J (2009) Dog obesity: owner attitudes and behaviour. Prev Vet Med 92:333–340

    PubMed  CAS  Google Scholar 

  12. Boost MV, O'Donoghue MM, James A (2008) Prevalence of Staphylococcus aureus carriage among dogs and their owners. Epidemiol Infect 136:953–964

    PubMed  CAS  Google Scholar 

  13. Bradley CW, Morris DO, Rankin SC, Cain CL, Misic AM, Houser T, Mauldin EA, Grice EA (2016) Longitudinal evaluation of the skin microbiome and association with microenvironment and treatment in canine atopic dermatitis. J Investig Dermatol 136:1182–1190

    PubMed  CAS  Google Scholar 

  14. Cain CL, Morris DO, Rankin SC (2011) 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 239:1566–1573

    PubMed  CAS  Google Scholar 

  15. Chah KF, Gómez-Sanz E, Nwanta JA, Asadu B, Agbo IC, Lozano C, Zarazaga M, Torres C (2014) Methicillin-resistant coagulase-negative staphylococci from healthy dogs in Nsukka, Nigeria. Braz J Microbiol 45:215–220

    PubMed  PubMed Central  Google Scholar 

  16. CLSI (2018) M02 performance standards for antimicrobial disk susceptibility tests13th edn. Clinical and Laboratory Standards Institute, Wayne, PA

    Google Scholar 

  17. Cox HU, Hoskins JD, Newman SS, Turnwald GH, Foil CS, Roy AF, Kearney MT (1985) Distribution of staphylococcal species on clinically healthy cats. Am J Vet Res 46:1824

    PubMed  CAS  Google Scholar 

  18. Cox HU, Hoskins JD, Newman SS, Foil CS, Turnwald GH, Roy AF (1988) Temporal study of staphylococcal species on healthy dogs. Am J Vet Res 49:747

    PubMed  CAS  Google Scholar 

  19. Daley P, Bajgai J, Penney C, Williams K, Whitney H, Golding GR, Weese S (2016) A cross sectional study of animal and human colonization with methicillin-resistant Staphylococcus aureus (MRSA) in an aboriginal community. BMC Public Health 16:595

    PubMed  PubMed Central  Google Scholar 

  20. Fazakerley J, Nuttall T, Sales D, Schmidt V, Carter SD, Hart CA, McEwan NA (2009) Staphylococcal colonization of mucosal and lesional skin sites in atopic and healthy dogs. Vet Dermatol 20:179–184

    PubMed  Google Scholar 

  21. Gandolfi-Decristophoris P, Regula G, Petrini O, Zinsstag J, Schelling E (2013) Prevalence and risk factors for carriage of multi-drug resistant staphylococci in healthy cats and dogs. J Vet Sci 14:449–456

    PubMed  PubMed Central  Google Scholar 

  22. Garland F (2016) Climate change addendum: western local strategic plan, region, L.L.S.W., ed. (LLS Western Region)

  23. Griffeth GC, Morris DO, Abraham JL, Shofer FS, Rankin SC (2008) Screening for skin carriage of methicillin-resistant coagulase-positive staphylococci and staphylococcus schleiferi in dogs with healthy and inflamed skin. Vet Dermatol 19:142–149

    PubMed  Google Scholar 

  24. Gronthal T, Ollilainen M, Eklund M, Piiparinen H, Gindonis V, Junnila J, Saijonmaa-Koulumies L, Liimatainen R, Rantala M (2015) Epidemiology of methicillin resistant Staphylococcus pseudintermedius in guide dogs in Finland. Acta Vet Scand 57:37

    PubMed  PubMed Central  Google Scholar 

  25. Guardabassi L, Loeber ME, Jacobson A (2004) Transmission of multiple antimicrobial-resistant Staphylococcus intermedius between dogs affected by deep pyoderma and their owners. Vet Microbiol 98:23–27

    PubMed  CAS  Google Scholar 

  26. Hájek V, Ludwig W, Schleifer KH, Springer N, Zitzelsberger W, Kroppenstedt RM, Kocur M (1992) Staphylococcus muscae, a new species isolated from flies. Int J Syst Bacteriol 42:97–101

    PubMed  Google Scholar 

  27. Hanselman BA, Kruth S, Weese JS (2008) Methicillin-resistant staphylococcal colonization in dogs entering a veterinary teaching hospital. Vet Microbiol 126:277–281

    PubMed  Google Scholar 

  28. Hanselman BA, Kruth SA, Rousseau J, Weese JS (2009) Coagulase positive staphylococcal colonization of humans and their household pets. Can Vet J 50:954–958

    PubMed  PubMed Central  Google Scholar 

  29. Higgins R, Gottschalk M (1991) Québec. Isolation of Staphylococcus felis from cases of external otitis in cats. Can Vet J = La revue vétérinaire canadienne 32:312–313

    CAS  Google Scholar 

  30. Hiramatsu K, Cui L, Kuroda M, Ito T (2001) The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol 9:486–493

    PubMed  CAS  Google Scholar 

  31. Igimi S, Atobe H, Tohya Y, Inoue A, Takahashi E, Konishi S (1994) Characterization of the most frequently encountered staphylococcus sp. in cats. Vet Microbiol 39:255–260

    PubMed  CAS  Google Scholar 

  32. Kong HH, Oh J, Deming C, Conlan S, Grice EA, Beatson MA, Nomicos E, Polley EC, Komarow HD, Mullikin J, Thomas J, Blakesley R, Young A, Chu G, Ramsahoye C, Lovett S, Han J, Legaspi R, Sison C, Montemayor C, Gregory M, Hargrove A, Johnson T, Riebow N, Schmidt B, Novotny B, Gupta J, Benjamin B, Brooks S, Coleman H, Ho S-L, Schandler K, Stantripop M, Maduro Q, Bouffard G, Dekhtyar M, Guan X, Masiello C, Maskeri B, McDowell J, Park M, Vemulapalli M, Murray PR, Turner ML, Segre JA, Program NCS (2012) Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 22:850–859

    PubMed  PubMed Central  CAS  Google Scholar 

  33. Lilenbaum W, Nunes ELC, Azeredo MAI (1998) Prevalence and antimicrobial susceptibility of staphylococci isolated from the skin surface of clinically normal cats. Lett Appl Microbiol 27:224–228

    PubMed  CAS  Google Scholar 

  34. Litster A, Moss SM, Honnery M, Rees B, Trott DJ (2007) Prevalence of bacterial species in cats with clinical signs of lower urinary tract disease: recognition of Staphylococcus felis as a possible feline urinary tract pathogen. Vet Microbiol 121:182–188

    PubMed  Google Scholar 

  35. Loeffler A, Lloyd D (2010) Companion animals: a reservoir for methicillin-resistant Staphylococcus aureus in the community? Epidemiol Infect 138:595–605

    PubMed  CAS  Google Scholar 

  36. Loeffler A, Pfeiffer DU, Lindsay JA, Magalhaes RJS, Lloyd DH (2011) Prevalence of and risk factors for MRSA carriage in companion animals: a survey of dogs, cats and horses. Epidemiol Infect 139:1019–1028

    PubMed  CAS  Google Scholar 

  37. Malik S, Coombs GW, O'Brien FG, Peng H, Barton MD (2006) Molecular typing of methicillin-resistant staphylococci isolated from cats and dogs. J Antimicrob Chemother 58:428–431

    PubMed  CAS  Google Scholar 

  38. Mouney MC, Stiles J, Townsend WM, Guptill L, Weese JS (2015) Prevalence of methicillin-resistant Staphylococcus spp. in the conjunctival sac of healthy dogs. Vet Ophthalmol 18:123–126

    PubMed  Google Scholar 

  39. Paul NC, Bärgman SC, Moodley A, Nielsen SS, Guardabassi L (2012) Staphylococcus pseudintermedius colonization patterns and strain diversity in healthy dogs: a cross-sectional and longitudinal study. Vet Microbiol 160:420–427

    PubMed  Google Scholar 

  40. Penna B, Varges R, Medeiros L, Martins GM, Martins RR, Lilenbaum W (2010) Species distribution and antimicrobial susceptibility of staphylococci isolated from canine otitis externa. Vet Dermatol 21:292–296

    PubMed  Google Scholar 

  41. Pinto Ferreira J, Anderson KL, Correa MT, Lyman R, Ruffin F, Reller LB, Fowler Jr VG (2011) Transmission of MRSA between companion animals and infected human patients presenting to outpatient medical care facilities. PLoS One 6:e26978

    Google Scholar 

  42. Rusdi B, Laird T, Abraham R, Ash A, Robertson DI, Mukerji S, Coombs G, Abraham S, O’Dea MA (2018) Carriage of critically important antimicrobial resistant bacteria and zoonotic parasites amongst camp dogs in remote Western Australian indigenous communities. Sci Rep 8:8725. https://doi.org/10.1038/s41598-018-26920-5

  43. Salgado CD, Farr BM, Calfee DP (2003) Community-acquired methicillin-resistant Staphylococcus aureus: a meta-analysis of prevalence and risk factors. (major article). Clin Infect Dis 36:131–139

    PubMed  Google Scholar 

  44. Santoro D, Rodrigues Hoffmann A (2016) Canine and human atopic dermatitis: two faces of the same host-microbe interaction. J Investig Dermatol 136:1087–1089

    PubMed  CAS  Google Scholar 

  45. Takada K, Iwase T, Mizunoe Y, Tajima A, Shinji H, Seo H, Agata T, Uehara Y (2010) Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465:346–349

    PubMed  Google Scholar 

  46. Tong SYC, Varrone L, Chatfield MD, Beaman M, Giffard PM (2015) Progressive increase in community-associated methicillin-resistant Staphylococcus aureus in indigenous populations in northern Australia from 1993 to 2012. Epidemiol Infect 143:1519–1523

    PubMed  CAS  Google Scholar 

  47. van Duijkeren E, Wolfhagen MJHM, Box ATA, Heck MEOC, Wannet WJB, Fluit AC (2004) Human-to-dog transmission of methicillin-resistant Staphylococcus aureus. Emerg Infect Dis 10:2235–2237

    PubMed  PubMed Central  Google Scholar 

  48. van Duijkeren E, Kamphuis M, van der Mije IC, Laarhoven LM, Duim B, Wagenaar JA, Houwers DJ (2011) Transmission of methicillin-resistant Staphylococcus pseudintermedius between infected dogs and cats and contact pets, humans and the environment in households and veterinary clinics. Vet Microbiol 150:338–343

    PubMed  Google Scholar 

  49. Vengust M, Anderson M, Rousseau J, Weese J (2006) Methicillin-resistant staphylococcal colonization in clinically normal dogs and horses in the community. Lett Appl Microbiol 43:602–606

    PubMed  CAS  Google Scholar 

  50. Vernozy-Rozand C, Mazuy C, Meugnier H, Bes M, Lasne Y, Fiedler F, Etienne J, Freney J (2000) Staphylococcus fleurettii sp. nov., isolated from goat’s milk cheeses. Int J Syst Evol Microbiol 50:1521–1527

    PubMed  CAS  Google Scholar 

  51. von Eiff C, Peters G, Heilmann C (2002) Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2:677–685

    Google Scholar 

  52. Walther B, Hermes J, Cuny C, Wieler LH, Vincze S, Abou Elnaga Y, Stamm I, Kopp PA, Kohn B, Witte W, Jansen A, Conraths FJ, Semmler T, Eckmanns T, Lübke-Becker A (2012) Sharing more than friendship--nasal colonization with coagulase-positive staphylococci (CPS) and co-habitation aspects of dogs and their owners. PLoS One 7:e35197

    PubMed  PubMed Central  CAS  Google Scholar 

  53. Weese JS (2010) Methicillin-resistant Staphylococcus aureus in animals. ILAR J 51:233–244

    PubMed  CAS  Google Scholar 

  54. Weese JS (2013) The canine and feline skin microbiome in health and disease. Vet Dermatol 24:137–e131

    PubMed  Google Scholar 

  55. Weese JS, Dick H, Willey BM, McGeer A, Kreiswirth BN, Innis B, Low DE (2006) Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household. Vet Microbiol 115:148–155

    PubMed  CAS  Google Scholar 

  56. Worthing K, Pang S, Trott DJ, Abraham S, Coombs GW, Jordan D, McIntyre L, Davies RM, Norris J (2018a) Characterisation of Staphylococcus felis isolated from cats using whole genome sequencing. Vet Microbiol 222:98–104

    PubMed  CAS  Google Scholar 

  57. Worthing KA, Brown J, Gerber L, Trott DJ, Abraham S, Norris JM (2018b) Methicillin-resistant staphylococci amongst veterinary personnel, personnel-owned pets, patients and the hospital environment of two small animal veterinary hospitals. Vet Microbiol 223:79–85

    PubMed  Google Scholar 

  58. Wu SW, de Lencastre H, Tomasz A (2001) Recruitment of the mecA gene homologue of Staphylococcus sciuri into a resistance determinant and expression of the resistant phenotype in Staphylococcus aureus. J Bacteriol 183:2417–2424

    PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We are very grateful to all communities and pet owners who participated in this study. Special thanks to Dr. Ann-Margret Withers and veterinary staff involved in community companion animal health programs for their assistance and support. We also thank Charlotte Webster and the team at the Department of Microbiology and Infectious Diseases at Concord Hospital (NSW, Australia) for their assistance with MALDI-TOF.

Author information

Authors and Affiliations

  1. Sydney School of Veterinary Science, The University of Sydney, Sydney, New South Wales, Australia

    Gemma C. Ma, Kate A. Worthing, Michael P. Ward & Jacqueline M. Norris

  2. Department of Microbiology and Immunology, Peter Doherty Institute for Infection and Immunity, University of Melbourne, Melbourne, Victoria, Australia

    Kate A. Worthing

Authors
  1. Gemma C. Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kate A. Worthing
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael P. Ward
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jacqueline M. Norris
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jacqueline M. Norris.

Ethics declarations

All dogs and cats were owned, and their participation was with written owner consent. Ethics approval was granted by the Animal Ethics Committee of the University of Sydney (2016/1044).

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, G.C., Worthing, K.A., Ward, M.P. et al. Commensal Staphylococci Including Methicillin-Resistant Staphylococcus aureus from Dogs and Cats in Remote New South Wales, Australia. Microb Ecol 79, 164–174 (2020). https://doi.org/10.1007/s00248-019-01382-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-019-01382-y

Keywords

Search

Navigation