FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Clinical medicine & research2010; 9(1); 7-16; doi: 10.3121/cmr.2010.944

Evidence of multiple virulence subtypes in nosocomial and community-associated MRSA genotypes in companion animals from the upper midwestern and northeastern United States.

Abstract: Not much is known about the zoonotic transmission of methicillin-resistant Staphylococcus aureus (MRSA) in companion animals in the United States. We report the rate of prevalence of S. aureus and MRSA recovered from clinical samples of animals requiring treatment at veterinary clinics throughout the upper midwestern and northeastern United States. Methods: We compared phenotypes, genotypes, and virulence profiles of the MRSA isolates identified in companion animals, such as cats, dogs, horses, and pigs, with typical human nosocomial and community-associated MRSA (CA-MRSA) genotypes to assess implied zoonotic transmission or zooanthroponosis. Five hundred thirty-three coagulase-positive staphylococci (CPS) isolates recovered between 2006 and 2008 from a variety of animal-source samples were screened for S. aureus by S. aureus-specific 16S rDNA primers and were screened for methicillin-resistance. All MRSA isolates were genotyped by pulsed-field gel electrophoresis (PFGE), multilocus sequence typing (MLST), and spa typing. They were also screened for common staphylococcal enterotoxin and adhesion genes by multiplex and singleplex PCR. Results: Among the 533 CPS isolates recovered, 66 (12.4%) were determined to be S. aureus and 24 (4.5%) were MRSA. The percent of animals that were positive for S. aureus were as follows: 6.6% (32 of 487) dogs, 39.6% (19 of 48) cats, 83.3% (10 of 12) horses, and 100% of pigs, rabbits, hamsters and rats. Notably, 36.4% of all S. aureus identified were MRSA. Methicillin-resistant S. aureus was present in clinical samples from 12 of 487 dogs (2.5%), 6 of 48 cats (12.5%), 5 of 12 horses (42%), and 1 of 2 pigs (50%). The 24 MRSA isolates resolved into 4 PFGE clones: USA100 (50%), USA300 (16.7%), USA500 (20.8%) and USA800 (12.5%) and 6 sequence types (ST5, ST8, ST105, ST830, and ST986) or 2 clonal complexes, CC5 and CC8. Five major virulence profiles (clusters A to E) were observed in these MRSA isolates. Genotypic and virulence profiles of cats and dogs were more similar to each other than to those of horses. A Panton-Valentine leukocidin positive isolate with ST8:USA300 background was identified in a pig causing skin and soft infection. Conclusions: The presence of human MRSA clones in these animals suggests possible reverse zoonotic transmission. This study reports the first case of a USA300 genotype in a pig. Presence of multiple virulence profiles within a MRSA genotype in these animals suggests the potential of emergence of new MRSA clones by gaining or losing additional virulence genes.
Get Full Text
Publication Date: 2010-08-25 PubMed ID: 20739580PubMed Central: PMC3064756DOI: 10.3121/cmr.2010.944Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The study investigates the transmission of Methicillin-resistant Staphylococcus aureus (MRSA), a type of bacteria resistant to many antibiotics, among companion animals such as dogs, cats, and horses in the United States. It also reports the first case of a certain type of MRSA found in a pig. There are indications that this MRSA can be transmitted from animals to humans.

Study Design and Methodology

  • The researchers collected clinical samples from various animals requiring treatment at veterinary clinics across upper midwestern and northeastern USA.
  • Out of 533 coagulase-positive staphylococci (CPS), a type of bacteria, samples were taken and checked for the presence of S. aureus and MRSA using S. aureus-specific 16S rDNA primers.
  • The samples were further screened for methicillin-resistance.
  • The researchers used pulsed-field gel electrophoresis (PFGE), multilocus sequence typing (MLST), and spa typing techniques to genotype the MRSA isolates.
  • The genes responsible for staphylococcal enterotoxin and adhesion were identified in the isolates using multiplex and singleplex PCR.

Results

  • Of the 533 CPS isolates recovered, 66 (12.4%) were identified as S. aureus and 24 (4.5%) were MRSA.
  • Animals positive for S. aureus were 6.6% (32 of 487) dogs, 39.6% (19 of 48) cats, 83.3% (10 of 12) horses, and 100% of pigs, rabbits, hamsters and rats.
  • Amongst these, 36.4% of all identified S. aureus were MRSA.
  • The 24 MRSA isolates were categorized into four major PFGE clones: USA100 (50%), USA300 (16.7%), USA500 (20.8%) and USA800 (12.5%).
  • Further, they were grouped into six different sequence types or two clonal complexes.
  • Five major virulence profiles were identified in the MRSA isolates.

Conclusions

  • Genotypic and virulence profiles of cats and dogs were found to be more similar to each other than to those of horses.
  • The presence of human MRSA clones in these animals suggests a possible reversed zoonosis, the transmission of the infection from animals to humans.
  • This study reported the first case of a USA300 genotype in a pig, supplemented with the speculate of potential emergence of new MRSA clones through gene gain or loss processes.

Cite This Article

APA
Lin Y, Barker E, Kislow J, Kaldhone P, Stemper ME, Pantrangi M, Moore FM, Hall M, Fritsche TR, Novicki T, Foley SL, Shukla SK. (2010). Evidence of multiple virulence subtypes in nosocomial and community-associated MRSA genotypes in companion animals from the upper midwestern and northeastern United States. Clin Med Res, 9(1), 7-16. https://doi.org/10.3121/cmr.2010.944

Publication

Clinical medicine & research
ISSN: 1554-6179
NlmUniqueID: 101175887
Country: United States
Language: English
Volume: 9
Issue: 1
Pages: 7-16

Researcher Affiliations

Lin, Yihan
  • Molecular Microbiology Laboratory, Marshfield Clinic Research Foundation, WI 54449, USA.
Barker, Emily
    Kislow, Jennifer
      Kaldhone, Pravin
        Stemper, Mary E
          Pantrangi, Madhulatha
            Moore, Frances M
              Hall, Matthew
                Fritsche, Thomas R
                  Novicki, Thomas
                    Foley, Steven L
                      Shukla, Sanjay K

                        MeSH Terms

                        • Animals
                        • Cats
                        • Communicable Diseases / diagnosis
                        • Communicable Diseases / epidemiology
                        • Communicable Diseases / genetics
                        • Communicable Diseases / microbiology
                        • Communicable Diseases / transmission
                        • Cricetinae
                        • Dogs
                        • Genotype
                        • Horses
                        • Humans
                        • Male
                        • Methicillin-Resistant Staphylococcus aureus
                        • Prevalence
                        • Rabbits
                        • Rats
                        • Staphylococcal Infections / diagnosis
                        • Staphylococcal Infections / epidemiology
                        • Staphylococcal Infections / genetics
                        • Staphylococcal Infections / microbiology
                        • Staphylococcal Infections / transmission
                        • Swine
                        • United States
                        • Zoonoses / epidemiology
                        • Zoonoses / microbiology
                        • Zoonoses / transmission

                        References

                        This article includes 52 references
                        1. Gordon RJ, Lowy FD. Pathogenesis of methicillin-resistant Staphylococcus aureus infection.. Clin Infect Dis 2008; 46 Suppl 5:S350–S359.
                          pmc: PMC2474459pubmed: 18462090
                        2. Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, McDougal LK, Carey R, Talan DA. Methicillin-resistant S. aureus infections in the emergency department.. N Engl J Med 2006;355:666–674.
                          pubmed: 16914702
                        3. David MZ, Glikman D, Crawford SE, Peng J, King KJ, Hostetler MA, Boyle-Vavra S, Daum RS. What is community-associated Methicillin-resistant Staphylococcus aureus?. J Infect Dis 2008;197:1235–1243.
                          pubmed: 18422435
                        4. McDougal LK, Steward CD, Killgore GE, Chaitram JM, McAllister SK, Tenover FC. Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database.. J Clin Microbiol 2003;41:5113–5120.
                          pmc: PMC262524pubmed: 14605147
                        5. McDougal LK, Wenming Z, Patel JB, Tenover FC. Characterization of two new community-associated oxacillin resistant Staphylococcus aureus pulsed-field types consisting of US isolates that carry SCCmec IV and Panton-Valentine leukocidin genes.. Abstr. 104th General Meeting American Society of Microbiology, New Orleans, LA 2004.
                        6. Devriese LA, Hommez J. Epidemiology of methicillin-resistant Staphylococcus aureus in dairy herds.. Res Vet Sci 1975;19:23–27.
                          pubmed: 125447
                        7. Cuny C, Strommenger B, Witte W, Stanek C. Clusters of infections in horses with MRSA ST1, ST254, and ST398 in a veterinary hospital.. Microb Drug Resist 2008;14:307–310.
                          pubmed: 19025385
                        8. Duquette RA, Nuttall TJ. Methicillin-resistant Staphylococcus aureus in dogs and cats: an emerging problem?. J Small Anim Pract 2004;45:591–597.
                          pubmed: 15600269
                        9. Weese JS. Methicillin-resistant Staphylococcus aureus: an emerging pathogen in small animals.. J Am Anim Hosp Assoc 2005;41:150–157.
                          pubmed: 15870248
                        10. Khanna T, Friendship R, Dewey C, Weese JS. Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers.. Vet Microbiol 2008;128:298303.
                          pubmed: 18023542
                        11. Loeffler A, Boag AK, Sung J, Lindsay JA, Guardabassi L, Dalsgaard A, Smith H, Stevens KB, Lloyd DH. Prevalence of methicillin-resistant Staphylococcus aureus among staff and pets in a small animal referral hospital in the UK.. J Antimicrob Chemother 2005;56:692–697.
                          pubmed: 16141276
                        12. Smith TC, Male MJ, Harper AL, Kroeger JS, Tinkler GP, Moritz ED, Capuano AW, Herwaldt LA, Diekema DJ. Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in midwestern U.S. swine and swine workers.. PLoS ONE 2008;4:e4258.
                          pmc: PMC2626282pubmed: 19145257
                        13. van Duijkeren E, Jansen MD, Flemming SC, de Neeling H, Wagenaar JA, Schoormans AH, van Nes A, Fluit AC. Methicillin-resistant Staphylococcus aureus in pigs with exudative epidermitis.. Emerg Infect Dis 2007;13:14081410.
                          pmc: PMC2857271pubmed: 18252124
                        14. Walther B, Wieler LH, Friedrich AW, Hanssen AM, Kohn B, Brunnberg L, Lubke-Becker A. Methicillin-resistant Staphylococcus aureus (MRSA) isolated from small and exotic animals at a university hospital during routine microbiological examinations.. Vet Microbiol 2008; 127:171–178.
                          pubmed: 17804179
                        15. Weese JS, Archambault M, Willey BM, Hearn P, Kreiswirth BN, Said-Salim B, McGeer A, Likhoshvay Y, Prescott JF, Low DE. Methicillin-resistant Staphylococcus aureus in horses and horse personnel, 2000–2002.. Emerg Infect Dis 2005;11:430–435.
                          pmc: PMC3298236pubmed: 15757559
                        16. Malik S, Coombs GW, O’Brien FG, Peng H, Barton MD. Molecular typing of methicillin-resistant staphylococci isolated from cats and dogs.. J Antimicrob Chemother 2006;58:428–431.
                          pubmed: 16782740
                        17. Moodley A, Stegger M, Bagcigil AF, Baptiste KE, Loeffler A, Lloyd DH, Williams NJ, Leonard N, Abbott Y, Skov R, Guardabassi L. spa typing of methicillin-resistant Staphylococcus aureus isolated from domestic animals and veterinary staff in the UK and Ireland.. J Antimicrob Chemother 2006;58:1118–1123.
                          pubmed: 17030517
                        18. Strommenger B, Kehrenberg C, Kettlitz C, Cuny C, Verspohl J, Witte W, Schwarz S. Molecular characterization of methicillin-resistant Staphylococcus aureus strains from pet animals and their relationship to human isolates.. J Antimicrob Chemother 2006;57:461465.
                          pubmed: 16387748
                        19. van Duijkeren E, Wolfhagen MJ, Box AT, Heck ME, Wannet WJ, Fluit AC. Human-to-dog transmission of methicillin-resistant Staphylococcus aureus.. Emerg Infect Dis 2004;10:2235–2237.
                          pmc: PMC3323405pubmed: 15663871
                        20. Weese JS, Dick H, Willey BM, McGeer A, Kreiswirth BN, Innis B, Low DE. Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household.. Vet Microbiol 2006;115:148–155.
                          pubmed: 16464540
                        21. Guinane CM, Sturdevant DE, Herron-Olson L, Otto M, Smyth DS, Villaruz AE, Kapur V, Hartigan PJ, Smyth CJ, Fitzgerald JR. Pathogenomic analysis of the common bovine Staphylococcus aureus clone (ET3): emergence of a virulent subtype with potential risk to public health.. J Infect Dis 2008;197:205213.
                          pubmed: 18177250
                        22. Hanselman BA, Kruth SA, Rousseau J, Low DE, Willey BM, McGeer A, Weese JS. Methicillin-resistant Staphylococcus aureus colonization in veterinary personnel.. Emerg Infect Dis 2006;12:1933–1938.
                          pmc: PMC3291342pubmed: 17326947
                        23. Weese JS, Caldwell F, Willey BM, Kreiswirth BN, McGeer A, Rousseau J, Low DE. An outbreak of methicillin-resistant Staphylococcus aureus skin infections resulting from horse to human transmission in a veterinary hospital.. Vet Microbiol 2006;114:160–164.
                          pubmed: 16384660
                        24. Witte W, Strommenger B, Stanek C, Cuny C. Methicillin-resistant Staphylococcus aureus ST398 in humans and animals, Central Europe.. Emerg Infect Dis 2007;13:255–258.
                          pmc: PMC2725865pubmed: 17479888
                        25. Wulf MW, Sorum M, van Nes A, Skov R, Melchers WJ, Klaassen CH, Voss A. Prevalence of methicillin-resistant Staphylococcus aureus among veterinarians: an international study.. Clin Microbiol Infect 2008;14:29–34.
                          pubmed: 17986212
                        26. Abraham JC, 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 Derm 2007;18:252–259.
                          pubmed: 17610491
                        27. Griffeth GC, Morris DO, Abraham JL, Shofer FS, Rankin SC. Screening of skin carriage of methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi in dogs with healthy and inflamed skin.. Vet Derm 2008;19:142–149.
                          pubmed: 18477330
                        28. Kottler S, Middleton JR, Perry J, Weese JS, Cohn LA. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus carriage in three populations.. J Vet Intern Med 2010;24:132–39.
                          pubmed: 20002557
                        29. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals: Approved Standard - Second Edition.. CLSI document M31-A2 Wayne, PA: Clinical and Laboratory Institute; 2002.
                        30. Brady JM, Stemper ME, Weigel A, Chyou PH, Reed KD, Shukla SK. Sporadic “transitional” community-associated methicillin-resistant Staphylococcus aureus strains from health care facilities in the United States.. J Clin Microbiol 2007;45:26542661.
                          pmc: PMC1951208pubmed: 17567793
                        31. Shimizu A, Kawano J, Yamamoto C, Kakutani O, Anzai T, Kamada M. Genetic analysis of equine methicillin-resistant Staphylococcus aureus by pulsed-field gel electrophoresis.. J Vet Med Sci 1997;59:935–937.
                          pubmed: 9362045
                        32. Bannerman TL, Hancock GA, Tenover FC, Miller JM. Pulsed-field gel electrophoresis as a replacement for bacteriophage typing of Staphylococcus aureus.. J Clin Microbiol 1995;33:551–555.
                          pmc: PMC227989pubmed: 7751356
                        33. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus.. J Clin Microbiol 2000;38:1008–1015.
                          pmc: PMC86325pubmed: 10698988
                        34. Koreen L, Ramaswamy SV, Graviss EA, Naidich S, Musser JM, Kreiswirth BN. spa typing method for discriminating among Staphylococcus aureus isolates: implications for use of a single marker to detect genetic micro- and macrovariation.. J Clin Microbiol 2004;42:792–799.
                          pmc: PMC344479pubmed: 14766855
                        35. Oliveira DC, Tomasz A, de Lencastre H. The evolution of pandemic clones of methicillin-resistant Staphylococcus aureus: identification of two ancestral genetic backgrounds and the associated mec elements.. Microb Drug Resist 2001;7:349–361.
                          pubmed: 11822775
                        36. Mellmann A, Weniger T, Berssenbrügge C, Rothgänger J, Sammeth M, Stoye J, Harmsen D. Based Upon Repeat Pattern (BURP): an algorithm to characterize the long-term evolution of Staphylococcus aureus populations based on spa polymorphisms.. BMC Microbiol 2007;7:98.
                          pmc: PMC2148047pubmed: 17967176
                        37. Shukla SK, Karow ME, Brady JM, Stemper ME, Kislow J, Moore N, Wroblewski K, Chyou P, Warshauer DM, Reed KD, Lynfield R, Schwan WR. Virulence Genes and Genotypic Associations in Nasal Carriage, Community-Associated Methicillin-Susceptible and Methicillin-Resistant USA400 Staphylococcus aureus.. J Clin Microbiol 2010; In press.
                          pmc: PMC2953128pubmed: 20668125
                        38. Hiramatsu K, Cui L, Kuroda M, Ito T. The emergence and evolution of methicillin-resistant Staphylococcus aureus.. Trends Microbiol 2001;9:486–493.
                          pubmed: 11597450
                        39. Proctor RA. Community acquired methicillin resistant Staphylococcus aureus: A Wisconsin perspective.. WMJ 2006;105:40–45.
                          pubmed: 17042419
                        40. Centers for Disease Control and Prevention (CDC). Methicillin-resistant Staphylococcus aureus skin or soft tissue infections in a state prison--Mississippi, 2000.. MMWR Morb Mortal Wkly Rep 2001;50:919–922.
                          pubmed: 11699844
                        41. Van den Eede A, Martens A, Lipinska U, Struelens M, Deplano A, Denis O, Haesebrouck F, Gasthuys F, Hermans K. High occurrence of methicillin-resistant Staphylococcus aureus ST398 in equine nasal samples.. Vet Microbiol 2009; 133:138–144.
                          pubmed: 18701224
                        42. van Belkum A, Melles DC, Peeters JK, van Leeuwen WB, van Duijkeren E, Huijsdens XW, Spalburg E, de Neeling AJ, Verbrugh HA. Methicillin-resistant and -susceptible Staphylococcus aureus sequence type 398 in pigs and humans.. Emerg Infect Dis 2008;14:479–483.
                          pmc: PMC2570802pubmed: 18325267
                        43. van Duijkeren E, Wolfhagen MJ, Heck ME, Wannet WJ. Transmission of a Panton-Valentine leukocidin-positive, methicillin-resistant Staphylococcus aureus strain between humans and a dog.. J Clin Microbiol 2005;43:62096211.
                          pmc: PMC1317200pubmed: 16333133
                        44. van Loo I, Huijsdens X, Tiemersma E, de Neeling A, van de Sande-Bruinsma N, Beaujean D, Voss A, Kluytmans J. Emergence of methicillin-resistant Staphylococcus aureus of animal origin in humans.. Emerg Infect Dis 2007; 13:1834–1839.
                          pmc: PMC2876750pubmed: 18258032
                        45. Vitale CB, Gross TL, Weese JS. Methicillin-resistant Staphylococcus aureus in cat and owner.. Emerg Infect Dis 2006;12:1998–2000.
                          pmc: PMC3291366pubmed: 17354344
                        46. Weese JS, Rousseau J, Traub-Dargatz JL, Willey BM, MCGeer AJ, Low DE. Community-associated methicillin-resistant Staphylococcus aureus in horses and humans who work with horses.. J Am Vet Med Assoc 2005;226:580–583.
                          pubmed: 15742700
                        47. Gorwitz RJ, Kruszon-Moran D, McAllister SK, McQuillan G, McDougal LK, Fosheim GE, Jensen BJ, Killgore G, Tenover FC, Kuehnert MJ. Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001–2004.. J Infect Dis 2008;197:1226–1234.
                          pubmed: 18422434
                        48. Tenover FC, McAllister S, Fosheim G, McDougal LK, Carey RB, Limbago B, Lonsway D, Patel JB, Kuehnert MJ, Gorwitz R. Characterization of Staphylococcus aureus isolates from nasal cultures collected from individuals in the United States in 2001 to 2004.. J Clin Microbiol 2008;46:2837–2841.
                          pmc: PMC2546757pubmed: 18632911
                        49. Klevens RM, Morrison MA, Fridkin SK, Reingold A, Petis S, Gershman K, Ray S, Harrison LH, Lynfield R, Dumyati G, Townes JM, Craig AS, Fosheim G, McDougal LK, Tenover FC. Community-associated methicillin-resistant Staphylococcus aureus and healthcare risk factors.. Emerg Infect Dis 2006;12:1991–1993.
                          pmc: PMC3291355pubmed: 17326962
                        50. Huang R, Mehta S, Weed D, Price CS. Methicillin-resistant Staphylococcus aureus survival on hospital fomites.. Infect Control Hosp Epidemiol 2006;27:1267–1269.
                          pubmed: 17080391
                        51. Johnson A, Pylka S, Olsen K, Sreevatsan S, Bender J. Methicillin-resistant Staphylococcus aureus isolated from therapy dogs and handlers within a hospital setting.. In: ASM-ESCMID Conference Proceedings: Methicillin-resistant staphylococci in animals: veterinary and public health implications September 22–25, 2009. London, England.
                        52. Umber JK, Bender JB. Pets and antimicrobial resistance.. Vet Clin Small Anim 2009;39:279292.
                          pubmed: 19185194

                        Citations

                        This article has been cited 33 times.
                        1. Arefin KSA, Rana EA, Islam MS, Hossain B, Rahman MA, Barua H. Molecular Prevalence and Antimicrobial Resistance Profile of Staphylococcus aureus and Staphylococcus pseudintermedius Isolated From Hospital-Visited Cats. Vet Med Int 2025;2025:4879266.
                          doi: 10.1155/vmi/4879266pubmed: 40893457google scholar: lookup
                        2. Viana AS, Tótola LPDV, Figueiredo AMS. ST105 Lineage of MRSA: An Emerging Implication for Bloodstream Infection in the American and European Continents. Antibiotics (Basel) 2024 Sep 18;13(9).
                          doi: 10.3390/antibiotics13090893pubmed: 39335066google scholar: lookup
                        3. Immergluck LC, Lin X, Geng R, Edelson M, Ali F, Li C, Lin TJ, Khalida C, Piper-Jenks N, Pardos de la Gandara M, de Lencastre H, Tomasz A, Evering TH, Kost RG, Vaughan R, Tobin JN. Molecular Epidemiologic and Geo-Spatial Characterization of Staphylococcus aureus Cultured from Skin and Soft Tissue Infections from United States-Born and Immigrant Patients Living in New York City. Antibiotics (Basel) 2023 Oct 14;12(10).
                          doi: 10.3390/antibiotics12101541pubmed: 37887242google scholar: lookup
                        4. Khairullah AR, Sudjarwo SA, Effendi MH, Ramandinianto SC, Gelolodo MA, Widodo A, Riwu KHP, Kurniawati DA. Pet animals as reservoirs for spreading methicillin-resistant Staphylococcus aureus to human health. J Adv Vet Anim Res 2023 Mar;10(1):1-13.
                          doi: 10.5455/javar.2023.j641pubmed: 37155545google scholar: lookup
                        5. Li G, Walker MJ, De Oliveira DMP. Vancomycin Resistance in Enterococcus and Staphylococcus aureus. Microorganisms 2022 Dec 21;11(1).
                          doi: 10.3390/microorganisms11010024pubmed: 36677316google scholar: lookup
                        6. Little SV, Hillhouse AE, Lawhon SD, Bryan LK. Analysis of Virulence and Antimicrobial Resistance Gene Carriage in Staphylococcus aureus Infections in Equids Using Whole-Genome Sequencing. mSphere 2021 Aug 25;6(4):e0019620.
                          doi: 10.1128/mSphere.00196-20pubmed: 34346711google scholar: lookup
                        7. Penna B, Silva MB, Soares AER, Vasconcelos ATR, Ramundo MS, Ferreira FA, Silva-Carvalho MC, de Sousa VS, Rabello RF, Bandeira PT, de Souza VS, Planet PJ, Vieira-da-Motta O, Botelho AMN, Figueiredo AMS. Comparative genomics of MRSA strains from human and canine origins reveals similar virulence gene repertoire. Sci Rep 2021 Feb 25;11(1):4724.
                          doi: 10.1038/s41598-021-83993-5pubmed: 33633263google scholar: lookup
                        8. Salgueiro V, Manageiro V, Bandarra NM, Ferreira E, Clemente L, Caniça M. Genetic Relatedness and Diversity of Staphylococcus aureus from Different Reservoirs: Humans and Animals of Livestock, Poultry, Zoo, and Aquaculture. Microorganisms 2020 Sep 3;8(9).
                          doi: 10.3390/microorganisms8091345pubmed: 32899267google scholar: lookup
                        9. Zhang L, Gao J, Barkema HW, Ali T, Liu G, Deng Y, Naushad S, Kastelic JP, Han B. Virulence gene profiles: alpha-hemolysin and clonal diversity in Staphylococcus aureus isolates from bovine clinical mastitis in China. BMC Vet Res 2018 Mar 2;14(1):63.
                          doi: 10.1186/s12917-018-1374-7pubmed: 29499697google scholar: lookup
                        10. Shukla SK, Ye Z, Sandberg S, Reyes I, Fritsche TR, Keifer M. The nasal microbiota of dairy farmers is more complex than oral microbiota, reflects occupational exposure, and provides competition for staphylococci. PLoS One 2017;12(8):e0183898.
                          doi: 10.1371/journal.pone.0183898pubmed: 28850578google scholar: lookup
                        11. Cuny C, Abdelbary MMH, Köck R, Layer F, Scheidemann W, Werner G, Witte W. Methicillin-resistant Staphylococcus aureus from infections in horses in Germany are frequent colonizers of veterinarians but rare among MRSA from infections in humans. One Health 2016 Dec;2:11-17.
                          doi: 10.1016/j.onehlt.2015.11.004pubmed: 28616471google scholar: lookup
                        12. Bierowiec K, Płoneczka-Janeczko K, Rypuła K. Prevalence and Risk Factors of Colonization with Staphylococcus aureus in Healthy Pet Cats Kept in the City Households. Biomed Res Int 2016;2016:3070524.
                          doi: 10.1155/2016/3070524pubmed: 27766257google scholar: lookup
                        13. Del Rosso JQ, Rosen T, Thiboutot D, Webster GF, Gallo RL, Leyden JJ, Walker C, Zhanel G, Eichenfield L. Status Report from the Scientific Panel on Antibiotic Use in Dermatology of the American Acne and Rosacea Society: Part 3: Current Perspectives on Skin and Soft Tissue Infections with Emphasis on Methicillin-resistant Staphylococcus aureus, Commonly Encountered Scenarios when Antibiotic Use May Not Be Needed, and Concluding Remarks on Rational Use of Antibiotics in Dermatology. J Clin Aesthet Dermatol 2016 Jun;9(6):17-24.
                          pubmed: 27386047
                        14. Mustapha M, Bukar-Kolo YM, Geidam YA, Gulani IA. Phenotypic and genotypic detection of methicillin-resistant Staphylococcus aureus in hunting dogs in Maiduguri metropolitan, Borno State, Nigeria. Vet World 2016 May;9(5):501-6.
                          doi: 10.14202/vetworld.2016.501-506pubmed: 27284227google scholar: lookup
                        15. Bierowiec K, Płoneczka-Janeczko K, Rypuła K. Is the Colonisation of Staphylococcus aureus in Pets Associated with Their Close Contact with Owners?. PLoS One 2016;11(5):e0156052.
                          doi: 10.1371/journal.pone.0156052pubmed: 27227897google scholar: lookup
                        16. Kuroda T, Kinoshita Y, Niwa H, Mizobe F, Ueno T, Kuwano A, Hatazoe T, Hobo S. Methicillin-resistant Staphylococcus aureus ulcerative keratitis in a Thoroughbred racehorse. J Equine Sci 2015;26(3):95-8.
                          doi: 10.1294/jes.26.95pubmed: 26435683google scholar: lookup
                        17. Ugwu CC, Gomez-Sanz E, Agbo IC, Torres C, Chah KF. Characterization of mannitol-fermenting methicillin-resistant staphylococci isolated from pigs in Nigeria. Braz J Microbiol 2015 Jul-Sep;46(3):885-92.
                          doi: 10.1590/S1517-838246320140644pubmed: 26413075google scholar: lookup
                        18. Smith TC, Wardyn SE. Human Infections with Staphylococcus aureus CC398. Curr Environ Health Rep 2015 Mar;2(1):41-51.
                          doi: 10.1007/s40572-014-0034-8pubmed: 26231241google scholar: lookup
                        19. Wardyn SE, Forshey BM, Farina SA, Kates AE, Nair R, Quick MK, Wu JY, Hanson BM, O'Malley SM, Shows HW, Heywood EM, Beane-Freeman LE, Lynch CF, Carrel M, Smith TC. Swine Farming Is a Risk Factor for Infection With and High Prevalence of Carriage of Multidrug-Resistant Staphylococcus aureus. Clin Infect Dis 2015 Jul 1;61(1):59-66.
                          doi: 10.1093/cid/civ234pubmed: 25931444google scholar: lookup
                        20. Harrison EM, Weinert LA, Holden MT, Welch JJ, Wilson K, Morgan FJ, Harris SR, Loeffler A, Boag AK, Peacock SJ, Paterson GK, Waller AS, Parkhill J, Holmes MA. A shared population of epidemic methicillin-resistant Staphylococcus aureus 15 circulates in humans and companion animals. mBio 2014 May 13;5(3):e00985-13.
                          doi: 10.1128/mBio.00985-13pubmed: 24825010google scholar: lookup
                        21. van Balen J, Mowery J, Piraino-Sandoval M, Nava-Hoet RC, Kohn C, Hoet AE. Molecular epidemiology of environmental MRSA at an equine teaching hospital: introduction, circulation and maintenance. Vet Res 2014 Mar 19;45(1):31.
                          doi: 10.1186/1297-9716-45-31pubmed: 24641543google scholar: lookup
                        22. Messenger AM, Barnes AN, Gray GC. Reverse zoonotic disease transmission (zooanthroponosis): a systematic review of seldom-documented human biological threats to animals. PLoS One 2014;9(2):e89055.
                          doi: 10.1371/journal.pone.0089055pubmed: 24586500google scholar: lookup
                        23. Himsworth CG, Miller RR, Montoya V, Hoang L, Romney MG, Al-Rawahi GN, Kerr T, Jardine CM, Patrick DM, Tang P, Weese JS. Carriage of methicillin-resistant Staphylococcus aureus by wild urban Norway rats (Rattus norvegicus). PLoS One 2014;9(2):e87983.
                          doi: 10.1371/journal.pone.0087983pubmed: 24498421google scholar: lookup
                        24. Quitoco IM, Ramundo MS, Silva-Carvalho MC, Souza RR, Beltrame CO, de Oliveira TF, Araújo R, Del Peloso PF, Coelho LR, Figueiredo AM. First report in South America of companion animal colonization by the USA1100 clone of community-acquired meticillin-resistant Staphylococcus aureus (ST30) and by the European clone of methicillin-resistant Staphylococcus pseudintermedius (ST71). BMC Res Notes 2013 Aug 27;6:336.
                          doi: 10.1186/1756-0500-6-336pubmed: 23981343google scholar: lookup
                        25. Chatterjee SS, Otto M. Improved understanding of factors driving methicillin-resistant Staphylococcus aureus epidemic waves. Clin Epidemiol 2013;5:205-17.
                          doi: 10.2147/CLEP.S37071pubmed: 23861600google scholar: lookup
                        26. Beceiro A, Tomás M, Bou G. Antimicrobial resistance and virulence: a successful or deleterious association in the bacterial world?. Clin Microbiol Rev 2013 Apr;26(2):185-230.
                          doi: 10.1128/CMR.00059-12pubmed: 23554414google scholar: lookup
                        27. Davis MF, Peterson AE, Julian KG, Greene WH, Price LB, Nelson K, Whitener CJ, Silbergeld EK. Household risk factors for colonization with multidrug-resistant Staphylococcus aureus isolates. PLoS One 2013;8(1):e54733.
                          doi: 10.1371/journal.pone.0054733pubmed: 23359808google scholar: lookup
                        28. Crombé F, Vanderhaeghen W, de Vogel CP, Van Wamel WJ, Barbé K, Hermans K, Haesebrouck F, Butaye P. Serological profiles in nursery piglets colonized with Staphylococcus aureus. Vet Res 2013 Jan 22;44(1):4.
                          doi: 10.1186/1297-9716-44-4pubmed: 23339425google scholar: lookup
                        29. Moodley A, Espinosa-Gongora C, Nielsen SS, McCarthy AJ, Lindsay JA, Guardabassi L. Comparative host specificity of human- and pig- associated Staphylococcus aureus clonal lineages. PLoS One 2012;7(11):e49344.
                          doi: 10.1371/journal.pone.0049344pubmed: 23166643google scholar: lookup
                        30. Sobral D, Schwarz S, Bergonier D, Brisabois A, Feßler AT, Gilbert FB, Kadlec K, Lebeau B, Loisy-Hamon F, Treilles M, Pourcel C, Vergnaud G. High throughput multiple locus variable number of tandem repeat analysis (MLVA) of Staphylococcus aureus from human, animal and food sources. PLoS One 2012;7(5):e33967.
                          doi: 10.1371/journal.pone.0033967pubmed: 22567085google scholar: lookup
                        31. Levin-Edens E, Soge OO, No D, Stiffarm A, Meschke JS, Roberts MC. Methicillin-resistant Staphylococcus aureus from Northwest marine and freshwater recreational beaches. FEMS Microbiol Ecol 2012 Feb;79(2):412-20.
                          doi: 10.1111/j.1574-6941.2011.01229.xpubmed: 22092827google scholar: lookup
                        32. Zhang L, Kinkelaar D, Huang Y, Li Y, Li X, Wang HH. Acquired antibiotic resistance: are we born with it?. Appl Environ Microbiol 2011 Oct;77(20):7134-41.
                          doi: 10.1128/AEM.05087-11pubmed: 21821748google scholar: lookup
                        33. Ferreira JP, Fowler VG Jr, Correa MT, Lyman R, Ruffin F, Anderson KL. Transmission of methicillin-resistant Staphylococcus aureus between human and hamster. J Clin Microbiol 2011 Apr;49(4):1679-80.
                          doi: 10.1128/JCM.02469-10pubmed: 21325561google scholar: lookup
                        Subscribe to our newsletter
                        Join 99,727 horse owners like you who receive our email updates on horse health and nutrition.