Prevalence and characteristics of Livestock-Associated Methicillin-Resistant Staphylococcus aureus (LA-MRSA) isolated from chicken meat in the province of Quebec, Canada


Autoři: Jocelyn Bernier-Lachance aff001;  Julie Arsenault aff001;  Valentine Usongo aff001;  Éric Parent aff001;  Josée Labrie aff001;  Mario Jacques aff002;  François Malouin aff001;  Marie Archambault aff001
Působiště autorů: Centre de Recherche en Infectiologie Porcine et Aviaire (CRIPA-FRQNT), Faculté de médecine vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec, Canada aff001;  Groupe de recherche sur les maladies infectieuses en production animale (GREMIP), Faculté de médecine vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec, Canada aff002;  Groupe de recherche en épidémiologie des zoonoses et santé publique (GREZOSP), Faculté de médecine vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec, Canada aff003;  Département de biologie, Faculté des sciences, Centre d'Étude et de Valorisation de la Diversité Microbienne (CEVDM), Université de Sherbrooke, Sherbrooke, Québec, Canada aff004
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227183

Souhrn

This study was conducted to estimate the prevalence of Livestock-Associated Methicillin-Resistant Staphylococcus aureus (LA-MRSA) in retail chicken meat and broiler chickens from the Province of Quebec, Canada, and to characterize LA-MRSA isolates. A total of 309 chicken drumsticks and thighs were randomly selected in 2013 from 43 retail stores in the Monteregie. In addition, nasal swabs and caeca samples were collected in 2013–2014 from 200 broiler chickens of 38 different flocks. LA-MRSA was not detected in broiler chickens. Fifteen LA-MRSA isolates were recovered from four (1.3%) of the 309 chicken meat samples. Multi-Locus Sequence Typing (MLST) and SCCmec typing revealed two profiles (ST398-MRSA-V and ST8-MRSA-IVa), which were distinct using pulse-field gel electrophoresis (PFGE) and microarray (antimicrobial resistance and virulence genes) analyses. In addition to beta-lactam resistance, tetracycline and spectinomycin resistance was detected in all isolates from the 3 positive samples of the ST398 profile. Southern blot hybridization revealed that the resistance genes aad(D) and lnu(A), encoding resistances to aminoglycosides and lincosamides respectively, were located on plasmid. All isolates were able to produce biofilms, but biofilm production was not correlated with hld gene expression. Our results show the presence of two separate lineages of MRSA in retail chicken meat in Quebec, one of which is likely of human origin.

Klíčová slova:

Antimicrobial resistance – Bacterial biofilms – Biofilms – Chickens – Meat – Methicillin-resistant Staphylococcus aureus – Polymerase chain reaction – Poultry


Zdroje

1. Lakhundi S, Zhang K. Methicillin-Resistant Staphylococcus aureus: Molecular Characterization, Evolution, and Epidemiology. Clin Microbiol Rev. 2018;31(4). doi: 10.1128/CMR.00020-18 30209034

2. Paterson GK, Harrison EM, Holmes MA. The emergence of mecC methicillin-resistant Staphylococcus aureus. Trends Microbiol. 2014;22(1):42–7. doi: 10.1016/j.tim.2013.11.003 24331435

3. Crombe F, Argudin MA, Vanderhaeghen W, Hermans K, Haesebrouck F, Butaye P. Transmission dynamics of methicillin-resistant Staphylococcus aureus in pigs. Front Microbiol. 2013;4:57. doi: 10.3389/fmicb.2013.00057 23518663

4. Weese JS, van Duijkeren E. Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in veterinary medicine. Vet Microbiol. 2010;140(3–4):418–29. doi: 10.1016/j.vetmic.2009.01.039 19246166

5. Vanderhaeghen W, Hermans K, Haesebrouck F, Butaye P. Methicillin-resistant Staphylococcus aureus (MRSA) in food production animals. Epidemiol Infect. 2010;138(5):606–25. doi: 10.1017/S0950268809991567 20122300

6. Wulf M, Voss A. MRSA in livestock animals-an epidemic waiting to happen? Clin Microbiol Infect. 2008;14(6):519–21. doi: 10.1111/j.1469-0691.2008.01970.x 18325034

7. de Neeling AJ, van den Broek MJ, Spalburg EC, van Santen-Verheuvel MG, Dam-Deisz WD, Boshuizen HC, et al. High prevalence of methicillin resistant Staphylococcus aureus in pigs. Vet Microbiol. 2007;122(3–4):366–72. doi: 10.1016/j.vetmic.2007.01.027 17367960

8. Khanna T, Friendship R, Dewey C, Weese JS. Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Vet Microbiol. 2008;128(3–4):298–303. doi: 10.1016/j.vetmic.2007.10.006 18023542

9. van Duijkeren E, Ikawaty R, Broekhuizen-Stins MJ, Jansen MD, Spalburg EC, de Neeling AJ, et al. Transmission of methicillin-resistant Staphylococcus aureus strains between different kinds of pig farms. Vet Microbiol. 2008;126(4):383–9. doi: 10.1016/j.vetmic.2007.07.021 17765409

10. Smith TC, Male MJ, Harper AL, Kroeger JS, Tinkler GP, Moritz ED, et al. Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in midwestern U.S. swine and swine workers. PLoS One. 2009;4(1):e4258. doi: 10.1371/journal.pone.0004258 19145257

11. Persoons D, Van Hoorebeke S, Hermans K, Butaye P, de Kruif A, Haesebrouck F, et al. Methicillin-resistant Staphylococcus aureus in poultry. Emerg Infect Dis. 2009;15(3):452–3. doi: 10.3201/eid1503.080696 19239762

12. Verhegghe M, Pletinckx LJ, Crombe F, Vandersmissen T, Haesebrouck F, Butaye P, et al. Methicillin-resistant Staphylococcus aureus (MRSA) ST398 in pig farms and multispecies farms. Zoonoses Public Health. 2013;60(5):366–74. doi: 10.1111/zph.12007 22925210

13. Nemati M, Hermans K, Lipinska U, Denis O, Deplano A, Struelens M, et al. Antimicrobial resistance of old and recent Staphylococcus aureus isolates from poultry: first detection of livestock-associated methicillin-resistant strain ST398. Antimicrob Agents Chemother. 2008;52(10):3817–9. doi: 10.1128/AAC.00613-08 18663024

14. Hasman H, Moodley A, Guardabassi L, Stegger M, Skov RL, Aarestrup FM. Spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry. Vet Microbiol. 2010;141(3–4):326–31. doi: 10.1016/j.vetmic.2009.09.025 19833458

15. Dressler AE, Scheibel RP, Wardyn S, Harper AL, Hanson BM, Kroeger JS, et al. Prevalence, antibiotic resistance and molecular characterisation of Staphylococcus aureus in pigs at agricultural fairs in the USA. Vet Rec. 2012;170(19):495. doi: 10.1136/vr.100570 22505242

16. Garcia-Graells C, Antoine J, Larsen J, Catry B, Skov R, Denis O. Livestock veterinarians at high risk of acquiring methicillin-resistant Staphylococcus aureus ST398. Epidemiol Infect. 2012;140(3):383–9. doi: 10.1017/S0950268811002263 22082716

17. Lewis HC, Molbak K, Reese C, Aarestrup FM, Selchau M, Sorum M, et al. Pigs as source of methicillin-resistant Staphylococcus aureus CC398 infections in humans, Denmark. Emerg Infect Dis. 2008;14(9):1383–9. doi: 10.3201/eid1409.071576 18760004

18. Golding GR, Bryden L, Levett PN, McDonald RR, Wong A, Graham MR, et al. Whole-genome sequence of livestock-associated ST398 methicillin-resistant Staphylococcus aureus isolated from humans in Canada. J Bacteriol. 2012;194(23):6627–8. doi: 10.1128/JB.01680-12 23144384

19. Schijffelen MJ, Boel CH, van Strijp JA, Fluit AC. Whole genome analysis of a livestock-associated methicillin-resistant Staphylococcus aureus ST398 isolate from a case of human endocarditis. BMC Genomics. 2010;11:376. doi: 10.1186/1471-2164-11-376 20546576

20. Huber H, Koller S, Giezendanner N, Stephan R, Zweifel C. Prevalence and characteristics of meticillin-resistant Staphylococcus aureus in humans in contact with farm animals, in livestock, and in food of animal origin, Switzerland, 2009. Euro Surveill. 2010;15(6):pii: 19542.

21. Mulders MN, Haenen AP, Geenen PL, Vesseur PC, Poldervaart ES, Bosch T, et al. Prevalence of livestock-associated MRSA in broiler flocks and risk factors for slaughterhouse personnel in The Netherlands. Epidemiol Infect. 2010;138(5):743–55. doi: 10.1017/S0950268810000075 20109255

22. Krupa P, Bystron J, Bania J, Podkowik M, Empel J, Mroczkowska A. Genotypes and oxacillin resistance of Staphylococcus aureus from chicken and chicken meat in Poland. Poult Sci. 2014;93(12):3179–86. doi: 10.3382/ps.2014-04321 25352679

23. de Boer E, Zwartkruis-Nahuis JT, Wit B, Huijsdens XW, de Neeling AJ, Bosch T, et al. Prevalence of methicillin-resistant Staphylococcus aureus in meat. Int J Food Microbiol. 2009;134(1–2):52–6. doi: 10.1016/j.ijfoodmicro.2008.12.007 19144432

24. Fessler AT, Kadlec K, Hassel M, Hauschild T, Eidam C, Ehricht R, et al. Characterization of methicillin-resistant Staphylococcus aureus isolates from food and food products of poultry origin in Germany. Appl Environ Microbiol. 2011;77(20):7151–7. doi: 10.1128/AEM.00561-11 21724898

25. Boost MV, Wong A, Ho J, O'Donoghue M. Isolation of methicillin-resistant Staphylococcus aureus (MRSA) from retail meats in Hong Kong. Foodborne Pathog Dis. 2013;10(8):705–10. doi: 10.1089/fpd.2012.1415 23692075

26. Weese JS, Avery BP, Reid-Smith RJ. Detection and quantification of methicillin-resistant Staphylococcus aureus (MRSA) clones in retail meat products. Lett Appl Microbiol. 2010;51(3):338–42. doi: 10.1111/j.1472-765X.2010.02901.x 20681968

27. Christianson S, Golding GR, Campbell J, Canadian Nosocomial Infection Surveillance P, Mulvey MR. Comparative genomics of Canadian epidemic lineages of methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2007;45(6):1904–11. doi: 10.1128/JCM.02500-06 17428941

28. Bhargava K, Wang X, Donabedian S, Zervos M, de Rocha L, Zhang Y. Methicillin-resistant Staphylococcus aureus in retail meat, Detroit, Michigan, USA. Emerg Infect Dis. 2011;17(6):1135–7. doi: 10.3201/eid/1706.101905 21749794

29. Otto M. Staphylococcal biofilms. Curr Top Microbiol Immunol. 2008;322:207–28. doi: 10.1007/978-3-540-75418-3_10 18453278

30. Jacques M, Aragon V, Tremblay YD. Biofilm formation in bacterial pathogens of veterinary importance. Anim Health Res Rev. 2010;11(2):97–121. doi: 10.1017/S1466252310000149 20969814

31. O'Neill E, Pozzi C, Houston P, Smyth D, Humphreys H, Robinson DA, et al. Association between methicillin susceptibility and biofilm regulation in Staphylococcus aureus isolates from device-related infections. J Clin Microbiol. 2007;45(5):1379–88. doi: 10.1128/JCM.02280-06 17329452

32. Novick RP. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol. 2003;48(6):1429–49. doi: 10.1046/j.1365-2958.2003.03526.x 12791129

33. Nemati M, Hermans K, Devriese LA, Maes D, Haesebrouck F. Screening of genes encoding adhesion factors and biofilm formation in Staphylococcus aureus isolates from poultry. Avian Pathol. 2009;38(6):513–7. doi: 10.1080/03079450903349212 19937541

34. Mehrotra M, Wang G, Johnson WM. Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J Clin Microbiol. 2000;38(3):1032–5. 10698991

35. Barski P, Piechowicz L, Galiński J, Kur J. Rapid assay for detection of methicillin-resistant Staphylococcus aureus using multiplex PCR. Mol Cell Probes. 1996;10(6):471–5. doi: 10.1006/mcpr.1996.0066 9025087

36. Cuny C, Layer F, Strommenger B, Witte W. Rare occurrence of methicillin-resistant Staphylococcus aureus CC130 with a novel mecA homologue in humans in Germany. PLoS One. 2011;6(9):e24360. doi: 10.1371/journal.pone.0024360 21931689

37. 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(3):1008–15. 10698988

38. Zhang K, McClure JA, Elsayed S, Louie T, Conly JM. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2005;43(10):5026–33. doi: 10.1128/JCM.43.10.5026-5033.2005 16207957

39. Mulvey MR, Chui L, Ismail J, Louie L, Murphy C, Chang N, et al. Development of a Canadian standardized protocol for subtyping methicillin-resistant Staphylococcus aureus using pulsed-field gel electrophoresis. J Clin Microbiol. 2001;39(10):3481–5. doi: 10.1128/JCM.39.10.3481-3485.2001 11574559

40. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. 20th ed. Wayne, PA: CLSI; 2010.

41. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. 4th ed. Wayne, PA: CLSI; 2018.

42. EUCAST. EUCAST clinical breakpoint table v. 5.0. European Committee on Antimicrobial Susceptibility Testing. 2013.

43. Monecke S, Jatzwauk L, Weber S, Slickers P, Ehricht R. DNA microarray-based genotyping of methicillin-resistant Staphylococcus aureus strains from Eastern Saxony. Clin Microbiol Infect. 2008;14(6):534–45. doi: 10.1111/j.1469-0691.2008.01986.x 18373691

44. Monecke S, Kuhnert P, Hotzel H, Slickers P, Ehricht R. Microarray based study on virulence-associated genes and resistance determinants of Staphylococcus aureus isolates from cattle. Vet Microbiol. 2007;125(1–2):128–40. doi: 10.1016/j.vetmic.2007.05.016 17614219

45. Fessler A, Scott C, Kadlec K, Ehricht R, Monecke S, Schwarz S. Characterization of methicillin-resistant Staphylococcus aureus ST398 from cases of bovine mastitis. J Antimicrob Chemother. 2010;65(4):619–25. doi: 10.1093/jac/dkq021 20164198

46. Lina G, Quaglia A, Reverdy ME, Leclercq R, Vandenesch F, Etienne J. Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramins among staphylococci. Antimicrob Agents Chemother. 1999;43(5):1062–6. doi: 10.1016/S1684-1182(10)60081-3 10223914

47. Tremblay YD, Lamarche D, Chever P, Haine D, Messier S, Jacques M. Characterization of the ability of coagulase-negative staphylococci isolated from the milk of Canadian farms to form biofilms. J Dairy Sci. 2013;96(1):234–46. doi: 10.3168/jds.2012-5795 23141829

48. Stepanovic S, Vukovic D, Hola V, Di Bonaventura G, Djukic S, Cirkovic I, et al. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS. 2007;115(8):891–9. doi: 10.1111/j.1600-0463.2007.apm_630.x 17696944

49. Veh KA, Klein RC, Ster C, Keefe G, Lacasse P, Scholl D, et al. Genotypic and phenotypic characterization of Staphylococcus aureus causing persistent and nonpersistent subclinical bovine intramammary infections during lactation or the dry period. J Dairy Sci. 2015;98(1):155–68. doi: 10.3168/jds.2014-8044 25468698

50. Allard M, Moisan H, Brouillette E, Gervais AL, Jacques M, Lacasse P, et al. Transcriptional modulation of some Staphylococcus aureus iron-regulated genes during growth in vitro and in a tissue cage model in vivo. Microbes Infect. 2006;8(7):1679–90. doi: 10.1016/j.micinf.2006.01.022 16969913

51. Goerke C, Campana S, Bayer MG, Döring G, Botzenhart K, Wolz C. Direct quantitative transcript analysis of theagr regulon of Staphylococcus aureus during human infection in comparison to the expression profile in vitro. Infect Immun. 2000;68(3):1304–11. doi: 10.1128/iai.68.3.1304-1311.2000 10678942

52. AC E, LS H. A SAS Macro implementation of a multiple comparison post hoc test for a Kruskal-Wallis analysis. Comp Meth Prog Bio. 2011;102:75–80. doi: 10.1016/j.cmpb.2010.11.002 21146248

53. Zimmermann-Meisse G, Prevost G, Jover E. Above and beyond C5a receptor targeting by staphylococcal leucotoxins: Retrograde transport of panton-valentine leucocidin and gamma-hemolysin. Toxins (Basel). 2017;9(1). doi: 10.3390/toxins9010041 28117704

54. Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR, Heffernan H, et al. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis. 2003;9(8):978–84. doi: 10.3201/eid0908.030089 12967497

55. Tremblay YD, Caron V, Blondeau A, Messier S, Jacques M. Biofilm formation by coagulase-negative staphylococci: impact on the efficacy of antimicrobials and disinfectants commonly used on dairy farms. Vet Microbiol. 2014;172(3–4):511–8. doi: 10.1016/j.vetmic.2014.06.007 24984943

56. Pletinckx LJ, Verhegghe M, Dewulf J, Crombe F, De Bleecker Y, Rasschaert G, et al. Screening of poultry-pig farms for methicillin-resistant Staphylococcus aureus: sampling methodology and within herd prevalence in broiler flocks and pigs. Infect Genet Evol. 2011;11(8):2133–7. doi: 10.1016/j.meegid.2011.07.008 21782977

57. Nemeghaire S, Roelandt S, Argudin MA, Haesebrouck F, Butaye P. Characterization of methicillin-resistant Staphylococcus aureus from healthy carrier chickens. Avian Pathol. 2013;42(4):342–6. doi: 10.1080/03079457.2013.805183 23777220

58. Buyukcangaz E, Velasco V, Sherwood JS, Stepan RM, Koslofsky RJ, Logue CM. Molecular typing of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) isolated from animals and retail meat in North Dakota, United States. Foodborne Pathog Dis. 2013;10(7):608–17. doi: 10.1089/fpd.2012.1427 23638848

59. Hanson BM, Dressler AE, Harper AL, Scheibel RP, Wardyn SE, Roberts LK, et al. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa. J Infect Public Health. 2011;4(4):169–74. doi: 10.1016/j.jiph.2011.06.001 22000843

60. Fromm S, Beisswanger E, Kasbohrer A, Tenhagen BA. Risk factors for MRSA in fattening pig herds—a meta-analysis using pooled data. Prev Vet Med. 2014;117(1):180–8. doi: 10.1016/j.prevetmed.2014.08.014 25241618

61. Weese JS, Reid-Smith R, Rousseau J, Avery B. Methicillin-resistant Staphylococcus aureus (MRSA) contamination of retail pork. Can Vet J. 2010;51(7):749–52. 20885828

62. Waters AE, Contente-Cuomo T, Buchhagen J, Liu CM, Watson L, Pearce K, et al. Multidrug-resistant Staphylococcus aureus in US meat and poultry. Clin Infect Dis. 2011;52(10):1227–30. doi: 10.1093/cid/cir181 21498385

63. Pu S, Han F, Ge B. Isolation and characterization of methicillin-resistant Staphylococcus aureus strains from Louisiana retail meats. Appl Environ Microbiol. 2009;75(1):265–7. doi: 10.1128/AEM.01110-08 18978079

64. Agnoletti F, Mazzolini E, Bacchin C, Bano L, Berto G, Rigoli R, et al. First reporting of methicillin-resistant Staphylococcus aureus (MRSA) ST398 in an industrial rabbit holding and in farm-related people. Vet Microbiol. 2014;170(1):172–7. doi: 10.1016/j.vetmic.2014.01.035 24602406

65. Benito D, Gómez P, Lozano C, Estepa V, Gómez-Sanz E, Zarazaga M, et al. Genetic lineages, antimicrobial resistance, and virulence in Staphylococcus aureus of meat samples in Spain: Analysis of Immune Evasion Cluster (IEC) genes. Foodborne Pathog Dis. 2014;11(5):354–6. doi: 10.1089/fpd.2013.1689 24479575

66. O'Brien AM, Hanson BM, Farina SA, Wu JY, Simmering JE, Wardyn SE, et al. MRSA in conventional and alternative retail pork products. PLoS One. 2012;7(1):e30092. doi: 10.1371/journal.pone.0030092 22276147

67. Kadlec K, Ehricht R, Monecke S, Steinacker U, Kaspar H, Mankertz J, et al. Diversity of antimicrobial resistance pheno- and genotypes of methicillin-resistant Staphylococcus aureus ST398 from diseased swine. J Antimicrob Chemother. 2009;64(6):1156–64. doi: 10.1093/jac/dkp350 19808235

68. Zarfel G, Krziwanek K, Johler S, Hoenigl M, Leitner E, Kittinger C, et al. Virulence and antimicrobial resistance genes in human MRSA ST398 isolates in Austria. Epidemiol Infect. 2013;141(4):888–92. doi: 10.1017/S0950268812001343 23084630

69. Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS, et al. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio. 2012;3(1). doi: 10.1128/mBio.00305-11 22354957

70. Jensen SO, Lyon BR. Genetics of antimicrobial resistance in Staphylococcus aureus. Future Microbiol. 2009;4(5):565–82. doi: 10.2217/fmb.09.30 19492967

71. Rouch DA, Byrne ME, Kong YC, Skurray RA. The aacA-aphD gentamicin and kanamycin resistance determinant of Tn4001 from Staphylococcus aureus: expression and nucleotide sequence analysis. J Gen Microbiol. 1987;133(11):3039–52. doi: 10.1099/00221287-133-11-3039 2833561

72. Luthje P, von Kockritz-Blickwede M, Schwarz S. Identification and characterization of nine novel types of small staphylococcal plasmids carrying the lincosamide nucleotidyltransferase gene lnu(A). J Antimicrob Chemother. 2007;59(4):600–6. doi: 10.1093/jac/dkm008 17329268

73. Nemeghaire S, Argudin MA, Haesebrouck F, Butaye P. Epidemiology and molecular characterization of methicillin-resistant Staphylococcus aureus nasal carriage isolates from bovines. BMC Vet Res. 2014;10:153. doi: 10.1186/1746-6148-10-153 25011427

74. Karageorgopoulos DE, Wang R, Yu XH, Falagas ME. Fosfomycin: evaluation of the published evidence on the emergence of antimicrobial resistance in Gram-negative pathogens. J Antimicrob Chemother. 2012;67(2):255–68. doi: 10.1093/jac/dkr466 22096042

75. Nicholson TL, Shore SM, Smith TC, Frana TS. Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) isolates of swine origin form robust biofilms. PLoS One. 2013;8(8):e73376. doi: 10.1371/journal.pone.0073376 23951352

76. Veh K, Klein R, Ster C, Keefe G, Lacasse P, Scholl D, et al. Genotypic and phenotypic characterization of Staphylococcus aureus causing persistent and nonpersistent subclinical bovine intramammary infections during lactation or the dry period. Journal of dairy science. 2015;98(1):155–68. doi: 10.3168/jds.2014-8044 25468698

77. Gonzalez BE, Rueda AM, Shelburne SA 3rd, Musher DM, Hamill RJ, Hulten KG. Community-associated strains of methicillin-resistant Staphylococccus aureus as the cause of healthcare-associated infection. Infect Control Hosp Epidemiol. 2006;27(10):1051–6. doi: 10.1086/507923 17006811

78. Osadebe LU, Hanson B, Smith TC, Heimer R. Prevalence and characteristics of Staphylococcus aureus in Connecticut swine and swine farmers. Zoonoses Public Health. 2013;60(3):234–43. doi: 10.1111/j.1863-2378.2012.01527.x 22883566

79. Lowder BV, Guinane CM, Ben Zakour NL, Weinert LA, Conway-Morris A, Cartwright RA, et al. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc Natl Acad Sci U S A. 2009;106(46):19545–50. doi: 10.1073/pnas.0909285106 19884497


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