Livestock-associated Staphylococcus aureus CC398: Animal reservoirs and human infections

Infection, Genetics and Evolution

Volumn 21, Issue , 2014, Pages 523-530

  Verkade, Erwin ^a,b   Kluytmans, Jan ^a,b,c  

^a AMPHIA HOSPITAL   (Netherlands)

^b CPRLab   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Animals; CC398; Epidemiology; Infections; Methicillin resistant Staphylococcus aureus; Transmission

Indexed keywords

VIRULENCE FACTOR;

ANIMAL; BACTERIAL GENOME; CLASSIFICATION; EVOLUTION; GENETICS; HUMAN; LIVESTOCK; MEAT; METABOLISM; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIOLOGY; PATHOGENICITY; STAPHYLOCOCCAL INFECTIONS; TRANSMISSION;

ANIMALS; BIOLOGICAL EVOLUTION; GENOME, BACTERIAL; HUMANS; LIVESTOCK; MEAT; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCAL INFECTIONS; VIRULENCE FACTORS;

EID: 84893773140     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2013.02.013     Document Type: Article

References (107)

1. Argudín M.A., Tenhagen B.A., Fetsch A., Sachsenröder J., Käsbohrer A., Schroeter A., Hammerl J.A., Hertwig S., Helmuth R., Bräunig J., Mendoza M.C., Appel B., Rodicio M.R., Guerra B. Virulence and resistance determinants of German Staphylococcus aureus ST398 isolates from nonhuman. Appl. Environ. Microbiol. 2011, 77:3052-3060.
2. Armand-Lefevre L., Ruimy R., Andremont A. Clonal comparison of Staphylococcus aureus isolates from healthy pig farmers, human controls, and pigs. Emerg. Infect. Dis. 2005, 11:711-714.
3. Bens C.C., Voss A., Klaassen C.H. Presence of a novel DNA methylation enzyme in methicillin-resistant Staphylococcus aureus isolates. J. Clin. Microbiol. 2006, 44:1875-1876.
4. Bhat M., Dumortier C., Taylor B.S., Miller M., Vasquez G., Yunen J., Brudney K., Sánchez-E J., Rodriguez-Taveras C., Rojas R., Leon P., Lowy F.D. Staphylococcus aureus ST398, New York City and Dominican Republic. Emerg. Infect. Dis. 2009, 15:285-287.
5. Bode L.G., Wertheim H.F., Kluytmans J.A., Bogaers-Hofman D., Vandenbroucke-Grauls C.M., Roosendaal R., Troelstra A., Box A.T., Voss A., van Belkum A., Verbrugh H.A., Vos M.C. Sustained low prevalence of Staphylococcus aureus upon admission to hospital in The Netherlands. J. Hosp. Infect. 2011, 79:198-201.
6. Bootsma M.C., Wassenberg M.W., Trapman P., Bonten M. The nosocomial transmission rate of animal-associated ST398 methicillin-resistant Staphylococcus aureus. J. R. Soc. Interface 2011, 57:578-584.
7. Broens E.M., Graat E.A., van der Wolf P.J., van de Giessen A.W., de Jong M.C. Prevalence and risk factor analysis of livestock associated MRSA-positive pig herds in The Netherlands. Prev. Vet. Med. 2011, 102:41-49.
8. Broens E.M., Graat E.A., van der Wolf P.J., van de Giessen A.W., van Duijkeren E., Wagenaar J.A., van Nes A., Mevius D.J., de Jong M.C. MRSA ST398 in the pig production chain. Prev. Vet. Med. 2011, 98:182-189.
9. Cavaco L.M., Hasman H., Aarestrup F.M. Zinc resistance of Staphylococcus aureus of animal origin is strongly associated with methicillin resistance. Vet. Microbiol. 2011, 150:344-348.
10. Centre for Disease Control and Prevention (CDC), 2008. HIV/AIDS in the United States. Available from: http://www.cdc.gov/hiv.
11. 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.
12. Cuny C., Nathaus R., Layer F., Strommenger B., Altmann D., Witte W. Nasal colonization of humans with methicillin-resistant Staphylococcus aureus (MRSA) ST398 with and without exposure to pigs. PLoS ONE 2009, 4:e6800.
13. DeLeo F.R., Chambers H.F. Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era. J. Clin. Invest. 2009, 119:2464-2474.
14. Deurenberg R.H., Stobberingh E.E. The molecular evolution of hospital- and community-associated methicillin-resistant Staphylococcus aureus. Curr. Mol. Med. 2009, 9:100-115.
15. Devriese L.A., Van Damme L.R., Fameree L. Methicillin (cloxacillin)-resistant Staphylococcus aureus strains isolated from bovine mastitis cases. J. Vet. Med. 1972, 19:598-605.
16. de Vries L.E., Christensen H., Skov R.L., Aarestrup F.M., Agerso Y. Diversity of the tetracyclin resistance gene tet(M) and identification of Tn916- and Tn5801-like (TN6014) transposons in Staphylococcus aureus from humans and animals. J. Antimicrob. Chemother. 2009, 64:490-500.
17. Dutch Food and Safety Authority, 2007. Prevalence of MRSA in meat products, 2007 - fact sheet. Available from:
18. Ekkelenkamp M.B., Sekkat M., Carpaij N., Troelstra A., Bonten M.J. Endocarditis due to methicillin-resistant Staphylococcus aureus originating from pigs. Ned. Tijdschr. Geneeskd. 2006, 150:2442-2447. In Dutch.
19. Enright M.C. The evolution of a resistant pathogen - the case of MRSA. Curr. Opin. Pharmacol. 2003, 3:474-479.
20. Faires M.C., Traverse M., Tater K.C., Pearl D.L., Weese J.S. Methicillin-resistant and -susceptible Staphylococcus aureus infections in dogs. Emerg. Infect. Dis. 2010, 16:69-75.
21. Fan J., Shu M., Zhang G., Zhou W., Jiang Y., Zhu Y., Chen G., Peacock S.J., Wan C., Pan W., Feil E.J. Biogeography and virulence of Staphylococcus aureus. PLoS ONE 2009, 4:e6216.
22. Fanoy E., Helmhout L.C., van der Vaart W.L., Weijdema K., van Santen-Verheuvel M.G., Thijsen S.F., de Neeling A.J., van Wamel W.J., Manaskova S.H., Kingma-Thijssen J.L. An outbreak of non-typeable MRSA within a residential care facility. Euro Surveill. 2009, 14. pii: 19080.
23. Feingold B.J., Silbergeld E.K., Curriero F.C., van Cleef B.A., Heck M.E., Kluytmans J.A. Livestock density as risk factor for livestock-associated methicillin-resistant Staphylococcus aureus, the Netherlands. Emerg. Infect. Dis. 2012, 18:1841-1849.
24. 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, 65:619-625.
25. Garcia-Alvarez L., Holden M.T.G., Lindsay H., Webb C.R., Brown D.F., Curran M.D., Walpole E., Brooks K., Pickard D.J., Teale C., Parkhill J., Bentley S.D., Edwards G.F., Girvan E.K., Kearns A.M., Pichon B., Hill R.L., Larsen A.R., Skov R.L., Peacock S.J., Maskell D.J., Holmes M.A. Methicillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect. Dis. 2011, 11:595-603.
26. Gorwitz R.J., Kruszon-Moran D., McAllister S.K., McQuillan G., McDougal L.K., Fosheim G.E., Jensen B.J., Killgore G., Tenover F.C., Kuehnert M.J. Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001-2004. J. Infect. Dis. 2008, 197:1226-1234.
27. Graham P.L., Lin S.X., Larson E.L. A U.S. population-based survey of Staphylococcus aureus colonization. Ann. Intern. Med. 2006, 144:318-325.
28. Graveland H., Wagenaar J.A., Heesterbeek H., Mevius D., van Duijkeren E., Heederik D. Methicillin resistant Staphylococcus aureus ST398 in veal calf farming: human MRSA carriage related with animal antimicrobial usage and farm hygiene. PLoS ONE 2010, 5:e10990.
29. Graveland H., Wagenaar J.A., Bergs K., Heesterbeek H., Heederik D. Persistence of livestock associated MRSA ST398 in humans is dependent on intensity of animal contact. PLoS ONE 2011, 6:e16830.
30. Grisold A.J., Zarfel G., Hoenigl M., Krziwanek K., Feierl G., Masoud L., Leitner E., Wagner-Eibel U., Badura A., Marth E. Occurrence and genotyping using automated repetitive-sequence-based PCR of methicillin-resistant Staphylococcus aureus ST398 in Southeast Austria. Diagn. Microbiol. Infect. Dis. 2010, 66:217-221.
31. Grundmann H., Aanensen D.M., van den Wijngaard C.C., Spratt B.G., Harmsen D., Friedrich A.W. Geographic distribution of Staphylococcus aureus causing invasive infections in Europe: a molecular-epidemiological analysis. PLoS Med. 2010, 7:e1000215.
32. Hallin M., De Mendonça R., Denis O., Lefort A., El Garch F., Butaye P., Hermans K., Struelens M.J. Diversity of accessory genome of human and livestock-associated ST398 methicillin resistant Staphylococcus aureus strains. Infect. Genet. Evol. 2011, 11:290-299.
33. Hasman H., Moodley A., Guardabassi L., Stegger M., Skov R.L., Aarestrup F.M. Spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry. Vet. Microbiol. 2010, 141:326-331.
34. Holmes M.A., Zadoks R.N. Methicillin resistant S. aureus in human and bovine mastitis. J. Mammary Gland Biol. Neoplasia 2011, 16:373-382.
35. Huijsdens X.W., van Dijke B.J., Spalburg E., van Santen-Verheuvel M.G., Heck M.E., Pluister G.N., Voss A., Wannet W.J., de Neeling A.J. Community-acquired MRSA and pig-farming. Ann. Clin. Microbiol. Antimicrob. 2006, 5:26.
36. Huijsdens, X.W., Bosch, T., van Santen-Verheuvel, M.G., Spalburg, E., Pluister, G.N., van Luit, M., Heck, M.E., Haenen, A., de Neeling, A.J., 2009. Molecular characterisation of PFGE non-typable methicillin-resistant Staphylococcus aureus in The Netherlands, 2007. Euro Surveill. 14, pii: 19335.
37. Juhász-Kaszanyitzky E., Szilárd J., Somogyi P., Dán A., van der Graaf-van Bloois L., van Duijkeren E., Wagenaar J.A. MRSA transmission between humans and cows. Emerg. Infect. Dis. 2007, 13:630-632.
38. Jevon M.P. Celbenin-resistant Staphylococci. Br. Med. J. 1961, 1:124-125.
39. Khanna T., Friendship R., Dewey C., Weese J.S. Methicillin-resistant Staphylococcus aureus colonization in pigs and pig farmers. Vet. Microbiol. 2008, 128:298-303.
40. Klevens R.M., Morrison M.A., Nadle J., Petit S., Gershman K., Ray S., Harrison L.H., Lynfield R., Dumyati G., Townes J.M., Craig A.S., Zell E.R., Fosheim G.E., McDougal L.K., Carey R.B., Fridkin S.K. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 2007, 298:1763-1771.
41. Kluytmans J.A. Methicillin-resistant Staphylococcus aureus in food products: cause for concern or case for complacency?. Clin. Microbiol. Infect. 2010, 16:11-15.
42. Kluytmans-Vandenbergh M.F., Kluytmans J.A. Community-acquired methicillin-resistant Staphylococcus aureus: current perspectives. Clin. Microbiol. Infect. 2006, 12:9-15.
43. Köck R., Loth B., Köksal M., Schulte-Wülwer J., Harlizius J., Friedrich A.W. Does nasal colonization with livestock-associated methicillin-resistant Staphylococcus aureus (MRSA) in pig farmers persist after holidays from pig exposure?. Appl. Environ. Microbiol 2012, 10.1128/AEM.00212-12.
44. Krziwanek K., Metz-Gercek S., Mittermayer H. Methicillin-resistant Staphylococcus aureus ST398 from human patients, upper Austria. Emerg. Infect. Dis. 2009, 15:766-769.
45. Kwon N.H., Park K.T., Moon J.S., Jung W.K., Kim S.H., Kim J.M., Hong S.K., Koo H.C., Joo Y.S., Park Y.H. Staphylococcal cassette chromosome mec (SCCmec) characterisation and molecular analysis for methicillin-resistant Staphylococcus aureus and novel SCCmec subtype IVg isolated from bovine milk in Korea. J. Antimicrob. Chemother. 2005, 56:624-632.
46. Leenders A., Janssen M., Renders N., Pelk M. Pig's MRSA on a poultry farm?. Infectieziekten Bulletin 2007, 18:43-44. (in Dutch, abstract in English).
47. Lekkerkerk W.S., van de Sande-Bruinsma N., van der Sande M.A., Tjon-A-Tsien A., Groenheide A., Haenen A., Timen A., van den Broek P.J., van Wamel W.J., de Neeling A.J., Richardus J.H., Verbrugh H.A., Vos M.C. Emergence of MRSA of unknown origin in the Netherlands. Clin. Microbiol. Infect. 2012, 18:656-661.
48. Lewis H.C., Mølbak K., Reese C., Aarestrup F.M., Selchau M., Sørum M., Skov R.L. Pigs as source of methicillin-resistant Staphylococcus aureus ST398 infections in humans, Denmark. Emerg. Infect. Dis. 2008, 14:1383-1389.
49. Li S., Skov R.L., Han X., Larsen A.R., Larsen J., Sørum M., Wulf M., Voss A., Hiramatsu K., Ito T. Novel types of staphylococcal cassette chromosome mec elements identified in clonal complex 398 methicillin-resistant Staphylococcus aureus strains. Antimicrob. Agents Chemother. 2011, 55:3046-3050.
50. Loeffler A., Boag A.K., Sung J., Lindsay J.A., Guardabassi L., Dalsgaard A., Smith H., Stevens K.B., Lloyd D.H. 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.
51. Loeffler A., Lloyd D.H. Companion animals: a reservoir for methicillin-resistant Staphylococcus aureus in the community?. Epidemiol. Infect. 2010, 138:595-605.
52. Lowy F.D. Staphylococcus aureus infections. N. Engl. J. Med. 1998, 339:520-532.
53. Lozano C., López M., Gómez-Sanz E., Ruiz-Larrea F., Torres C., Zarazaga M. Detection of methicillin-resistant Staphylococcus aureus ST398 in food samples of animal origin in Spain. J. Antimicrob. Chemother. 2009, 64:1325-1326.
54. Lozano C., Gómez-Sanz E., Benito D., Aspiroz C., Zarazaga M., Torres C. Staphylococcus aureus nasal carriage, virulence traits, antibiotic resistance mechanisms, and genetic lineages in healthy humans in Spain, with detection of ST398 and CC97 strains. Int. J. Med. Microbiol. 2011, 301:500-505.
55. McCarthy A.J., van Wamel W., Vandendriessche S., Larsen J., Denis O., Garcia-Graells C., Uhlemann A.C., Lowy F.D., Skov R., Lindsay J.A. Staphylococcus aureus CC398 clade associated with human-to-human transmission. Appl. Environ. Microbiol. 2012, 78:8845-8848.
56. 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, 15:128-140.
57. Morgan M. Methicillin-resistant Staphylococcus aureus and animals: zoonosis or humanosis?. J. Antimicrob. Chemother. 2008, 62:1181-1187.
58. Moritz E.D., Smith T.C. Livestock-associated Staphylococcus aureus in childcare worker. Emerg. Infect. Dis. 2011, 17:742-744.
59. Morris D.O., Lautenbach E., Zaoutis T., Leckerman K., Edelstein P.H., Rankin S.C. Potential for pet animals to harbor methicillin-resistant Staphylococcus aureus when residing with human MRSA patients. Zoonoses Public Health 2012, 59:286-293.
60. Mulders M.N., Haenen A.P., Geenen P.L., Vesseur P.C., Poldervaart E.S., Bosch T., Huijsdens X.W., Hengeveld P.D., Dam-Deisz W.D., Graat E.A., Mevius D., Voss A., van de Giessen A.W. Prevalence of livestock-associated MRSA in broiler flocks and risk factors for slaughterhouse personnel in The Netherlands. Epidemiol. Infect. 2010, 138:743-755.
61. Naimi T.S., LeDell K.H., Como-Sabetti K., Borchardt S.M., Boxrud D.J., Etienne J., Johnson S.K., Vandenesch F., Fridkin S., O'Boyle C., Danila R.N., Lynfield R. Comparison of community and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA 2003, 290:2976-2984.
62. de Neeling A.J., van den Broek M.J., Spalburg E.C., van Santen-Verheuvel M.G., Dam-Deisz W.D., Boshuizen H.C., van der Giessen A.W., van Duijkeren E., Huijsdens X.W. High prevalence of methicillin resistant Staphylococcus aureus in pigs. Vet. Microbiol. 2007, 122:366-372.
63. O'Brien A.M., Hanson B.M., Farina S.A., Wu J.Y., Simmering J.E., Wardyn S.E., Forshey B.M., Kulick M.E., Wallinga D.B., Smith T.C. MRSA in conventional and alternative retail pork products. PLoS ONE 2012, 7:e30092.
64. Otter J.A., French G.L. Molecular epidemiology of community-associated meticillin-resistant Staphylococcus aureus in Europe. Lancet Infect. Dis. 2010, 10:227-239.
65. Pan A., Battisti A., Zoncada A., Bernieri F., Boldini M., Franco A., Giorgi M., Iurescia M., Lorenzotti S., Martinotti M., Monaci M., Pantosti A. Community-acquired methicillin-resistant Staphylococcus aureus ST398 infection, Italy. Emerg. Infect. Dis. 2009, 15:845-847.
66. Paterson G.K., Larsen J., Harrison E.M., Larsen A.R., Morgan F.H., Peacock S.J., Parkhill J., Zadoks R.N. First detection of livestock-associated meticillin-resistant Staphylococcus aureus CC398 in bulk tank milk in the United Kingdom, January to July 2012. Euro Surveill. 2012, 17. pii: 20337.
67. Price L.B., Stegger M., Hasman H., Aziz M., Larsen J., Andersen P.S., Pearson T., Waters A.E., Foster J.T., Schupp J., Gellice J., Driebe E., Liu C.M., Springer B., Zdovc I., Battisti A., Franco A., Zmudzki J., Schwarz S., Butaye P., Jouy E., Pomba C., Porrero M.C., Ruimy R., Smith T.C., Robinson D.A., Weese J.S., Arriola C.S., Yu F., Laurent F., Keim P., Skov R., Aarestrup F.M. Staphylococcus aureus ST398: host adaptation and emergence of methicillin resistance in livestock. MBio 2012, 3. e00305-11.
68. Rasigade J.P., Laurent F., Hubert P., Vandenesch F., Etienne J. Lethal necrotizing pneumonia caused by an ST398 Staphylococcus aureus strain. Emerg. Infect. Dis. 2010, 16:1330.
69. Richter A., Sting R., Popp C., Rau J., Tenhagen B.A., Guerra B., Hafez H.M., Fetsch A. Prevalence of types of methicillin-resistant Staphylococcus aureus in turkey flocks and personnel attending the animals. Epidemiol. Infect. 2012, 140:2223-2232.
70. Robinson D.A., Enright M.C. Evolutionary models of the emergence of methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 2003, 47:3926-3934.
71. Rooijakkers S.H., Ruyken M., Roos A., Daha M.R., Presanis J.S., Sim R.B., van Wamel W.J., van Kessel K.P., van Strijp J.A. Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat. Immunol. 2005, 6:920-927.
72. Schulz J., Friese A., Klees S., Tenhagen B.A., Fetsch A., Rösler U., Hartung J. Longitudinal study of the contamination of air and of soil surfaces in the vicinity of pig barns by livestock-associated methicillin-resistant Staphylococcus aureus. Appl. Environ. Microbiol. 2012, 78:5666-5671.
73. Seguin J.C., Walker R.D., Caron J.P., Kloos W.E., George C.G., Hollis R.J., Jones R.N., Pfaller M.A. Methicillin-resistant Staphylococcus aureus outbreak in a veterinary teaching hospital: potential human-to-animal transmission. J. Clin. Microbiol. 1999, 37:1459-1463.
74. Slingerland B.C., Tavakol M., McCarthy A.J., Lindsay J.A., Snijders S.V., Wagenaar J.A., van Belkum A., Vos M.C., Verbrugh H.A., van Wamel W.J. Survival of Staphylococcus aureus ST398 in the human nose after artificial inoculation. PLoS ONE 2012, 7:e48896.
75. Smith T.C., Pearson N. The emergence of Staphylococcus aureus ST398. Vector Borne Zoonotic Dis. 2011, 11:327-339.
76. Stegger M., Lindsay J.A., Sørum M., Gould K.A., Skov R. Genetic diversity in ST398 methicillin-resistant Staphylococcus aureus isolates of different geographical origin. Clin. Microbiol. Infect. 2010, 16:1017-1019.
77. Uhlemann A.C., Porcella S.F., Trivedi S., Sullivan S.B., Hafer C., Kennedy A.D., Barbian K.D., McCarthy A.J., Street C., Hirschberg D.L., Lipkin W.I., Lindsay J.A., DeLeo F.R., Lowy F.D. Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties. MBio 2012, 3. pii: e00027-12.
78. Valentin-Domelier A.S., Girard M., Bertrand X., Violette J., François P., Donnio P.Y., Talon D., Quentin R., Schrenzel J., van der Mee-Marquet N. Methicillin-susceptible ST398 Staphylococcus aureus responsible for bloodstream infections: an emerging human-adapted subclone?. PLoS ONE 2011, 6:e28369.
79. van Belkum A., Melles D.C., Peeters J.K., van Leeuwen W.B., van Duijkeren E., Huijsdens X.W., Spalburg E., de Neeling A.J., Verbrugh H.A. Methicillin-resistant and -susceptible Staphylococcus aureus sequence type 398 in pigs and humans. Emerg. Infect. Dis. 2008, 14:479-483.
80. van Cleef B.A., Graveland H., Haenen A.P., van de Giessen A.W., Heederik D., Wagenaar J.A., Kluytmans J.A. Persistence of livestock-associated methicillin-resistant Staphylococcus aureus in field workers after short-term occupational exposure to pigs and veal calves. J. Clin. Microbiol. 2011, 49:1030-1033.
81. van Cleef B.A., Monnet D.L., Voss A., Krziwanek K., Allerberger F., Struelens M., Zemlickova H., Skov R.L., Vuopio-Varkila J., Cuny C., Friedrich A.W., Spiliopoulou I., Pászti J., Hardardottir H., Rossney A., Pan A., Pantosti A., Borg M., Grundmann H., Mueller-Premru M., Olsson-Liljequist B., Widmer A., Harbarth S., Schweiger A., Unal S., Kluytmans J.A. Livestock-associated methicillin-resistant Staphylococcus aureus in humans, Europe. Emerg. Infect. Dis. 2011, 17:502-505.
82. van Cleef B.A., Verkade E.J., Wulf M.W., Buiting A.G., Voss A., Huijsdens X.W., van Pelt W., Mulders M.N., Kluytmans J.A. Prevalence of livestock-associated MRSA in communities with high pig-densities in The Netherlands. PLoS ONE 2010, 5:e9385.
83. van den Broek I.V.F., van Cleef B.A., Haenen A., Broens E.M., van der Wolf P.J., van den Broek M.J., Huijsdens X.W., Kluytmans J.A., van de Giessen A.W., Tiemersma E.W. Methicillin-resistant Staphylococcus aureus in people living and working in pig farms. Epidemiol. Infect. 2008, 24:1-9.
84. Vandendriessche S., Kadlec K., Schwarz S., Denis O. Methicillin-susceptible Staphylococcus aureus ST398-t571 harbouring the macrolide-lincosamide-streptogramin B resistance gene erm(T) in Belgian hospitals. J. Antimicrob. Chemother. 2011, 66:2455-2459.
85. 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.
86. van der Mee-Marquet N., François P., Domelier A.S., Coulomb F., Decreux C., Hombrock-Allet C., Lehiani O., Neveu C., Ratovohery D., Schrenzel J., Quentin R. Emergence of unusual bloodstream infections associated with pig-borne-like Staphylococcus aureus ST398 in France. Clin. Infect. Dis. 2011, 52:152-153.
87. van Duijkeren E., Wolfhagen M.J., Box A.T., Heck M.E., Wannet W.J., Fluit A.C. Human-to-dog transmission of methicillin-resistant Staphylococcus aureus. Emerg. Infect. Dis. 2004, 10:2235-2237.
88. van Duijkeren E., Jansen M.D., Flemming S.C., de Neeling H., Wagenaar J.A., Schoormans A.H., van Nes A., Fluit A.C. Methicillin-resistant Staphylococcus aureus in pigs with exudative epidermitis. Emerg. Infect. Dis. 2007, 13:1408-1410.
89. van Duijkeren E., Ikawaty R., Broekhuizen-Stins M.J., Jansen M.D., Spalburg E.C., de Neeling A.J., Allaart J.G., van Nes A., Wagenaar J.A., Fluit A.C. Transmission of methicillin-resistant Staphylococcus aureus strains between different kinds of pig farms. Vet. Microbiol. 2008, 126:383-389.
90. van Duijkeren E., Moleman M., Sloet van Oldruitenborgh-Oosterbaan M.M., Multem J., Troelstra A., Fluit A.C., van Wamel W.J., Houwers D.J., de Neeling A.J., Wagenaar J.A. Methicillin-resistant Staphylococcus aureus in horses and horse personnel: an investigation of several outbreaks. Vet. Microbiol. 2010, 141:96-102.
91. van Loo I.H., Diederen B.M., Savelkoul P.H., Woudenberg J.H., Roosendaal R., van Belkum A., Lemmens-den Toom N., Verhulst C., van Keulen P.H., Kluytmans J.A. Methicillin-resistant Staphylococcus aureus in meat products, The Netherlands. Emerg. Infect. Dis. 2007, 13:1753-1755.
92. 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.
93. van Rijen M.M., van Keulen P.H., Kluytmans J.A. Increase in a Dutch hospital of methicillin-resistant Staphylococcus aureus related to animal farming. Clin. Infect. Dis. 2008, 46:261-263.
94. van Rijen, M.M., Kluytmans-Van den Bergh, M.F., ten Ham, P.B., Verkade, E., Kluytmans J., on behalf of the CAM Study Group, 2012. Consumption of meat as a risk factor for MRSA carriage: a case-control study. Poster Presentation P2363 on the 22nd European Congress of Clinical Microbiology and Infectious Diseases (ECCMID).
95. Verkade, E., van Benthem, B., Kluytmans-Vandenbergh, M.F., van Cleef, B., van Rijen, M., Kluytmans, J., 2013. Dynamics and determinants of Staphylococcus aureus carriage in livestock veterinarians: a prospective cohort study. Clin. Infect. Dis.
96. Verkade E., Bergmans A.M., Budding A.E., van Belkum A., Savelkoul P., Buiting A.G., Kluytmans J. Recent emergence of Staphylococcus aureus clonal complex 398 in human blood cultures. PLoS ONE 2012, 7:e41855.
97. Verkade E., Bosch T., Hendriks Y., Kluytmans J. Outbreak of methicillin-resistant Staphylococcus aureus ST398 in a Dutch nursing home. Infect. Control Hosp. Epidemiol. 2012, 33:624-626.
98. Voss A., Loeffen F., Bakker J., Klaassen C., Wulf M. Methicillin resistant Staphylococcus aureus in pig farming. Emerg. Infect. Dis. 2005, 11:1965-1966.
99. Wassenberg M.W., Bootsma M.C., Troelstra A., Kluytmans J.A., Bonten M.J. Transmissibility of livestock-associated methicillin-resistant Staphylococcus aureus (ST398) in Dutch hospitals. Clin. Microbiol. Infect. 2011, 17:316-319.
100. Walderon D., Lindsay J. SauI: a novel lineage-specific type I restriction-modification system that blocks horizontal gene transfer into Staphylococcus aureus and between Staphylococcus aureus isolates of different lineages. J. Bacteriol. 2006, 188:5578-5585.
101. Weese J.S., van Duijkeren E. Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in veterinary medicine. Vet. Microbiol. 2010, 140:418-429.
102. Weese J.S., Reid-Smith R., Rousseau J., Avery B. Methicillin-resistant Staphylococcus aureus (MRSA) contamination of retail pork. Can. Vet. J. 2010, 51:749-752.
103. Wertheim H.F., Melles D.C., Vos M.C., van Leeuwen W., van Belkum A., Verbrugh H.A., Nouwen J.L. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect. Dis. 2005, 5:751-762.
104. 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.
105. Wulf M.W., Markestein A., van der Linden F.T., Voss A., Klaassen C., Verduin C.M. First outbreak of methicillin-resistant Staphylococcus aureus ST398 in a Dutch hospital, 2007. Eurosurv. 2008, 13. pii: 8051.
106. Wulf M.W., Sorum M., van Nes A., Skov R., Melchers W.J., Klaassen C.H., Voss A. Prevalence of methicillin-resistant Staphylococcus aureus among veterinarians: an international study. Clin. Microbiol. Infect. 2008, 14:29-34.
107. Wulf M.W., Verduin C.M., van Nes A., Huijsdens X., Voss A. Infection and colonization with methicillin resistant Staphylococcus aureus ST398 versus other MRSA in an area with a high density of pig farms. Eur. J. Clin. Microbiol. Infect. Dis. 2012, 31:61-65.