Transmission of methicillin-resistant Staphylococcus aureus from food production animals to humans: A review

CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources

Volumn 3, Issue , 2008, Pages

  Broens, Els M ^a,b   Van Cleef, Brigitte A G L ^b,c   Graat, Elisabeth A M ^a   Kluytmans, Jan A J W ^c,d  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d AMPHIA HOSPITAL   (Netherlands)

Author keywords

Animals; Antibiotic resistance; Evolution; Methicillin resistance; Staphylococcus aureus; Transmission; Zoonoses

Indexed keywords

EID: 79952318957     PISSN: None     EISSN: 17498848     Source Type: Journal    
DOI: 10.1079/PAVSNNR20083095     Document Type: Review

References (160)

1. Acar J, Rostel B. Antimicrobial resistance: an overview. Revue Scientifique et Technique (International Office of Epizootics) 2001;20:797-810.
2. Tenover FC, McGowan Jr JE. Reasons for the emergence of antibiotic resistance. American Journal of Medical Sciences 1996;311:9-16. (Pubitemid 26030020)
3. Wassenaar TM. Use of antimicrobial agents in veterinary medicine and implications for human health. Critical Reviews in Microbiology 2005;31:155-69. (Pubitemid 41140886)
4. Aarestrup FM. Veterinary drug usage and antimicrobial resistance in bacteria of animal origin. Basic and Clinical Pharmacology and Toxicology 2005;96:271-81. (Pubitemid 40432474)
5. Hammerum AM, Heuer OE, Emborg HD, Bagger-Skjot L, Jensen VF, Rogues AM, et al. Danish integrated antimicrobial resistance monitoring and research program. Emerging Infectious Diseases 2007;13:1632-9. (Pubitemid 350126188)
6. Chambers HF. The changing epidemiology of Staphylococcus aureus? Emerging Infectious Diseases 2001;7:178-82. (Pubitemid 32374323)
7. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, et al. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. The Journal of the American Medical Association 2007;298:1763-71. (Pubitemid 47598444)
8. Centre for Disease Control and Prevention (CDC). HIV/AIDS in the United States. 2008. Available from: URL: http://www.cdc.gov/hiv
9. Voss A, Loeffen F, Bakker J, Klaassen C, Wulf M. Methicillinresistant Staphylococcus aureus in pig farming. Emerging Infectious Diseases 2005;11:1965-6. (Pubitemid 43356102)
10. 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. Veterinary Microbiology 2007;122:366-72. (Pubitemid 46756022)
11. Khanna T, Friendship R, Dewey C, Weese JS. Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Veterinary Microbiology 2008;128:298-303. (Pubitemid 351305091)
12. Graveland H, Wagenaar JA, Broekhuizen-Stins M, Oosting-Schothorst I, Schoorsmans A, van Duijkeren E, et al. Methicillin resistant Staphylococcus aureus (MRSA) in veal calf farmers and veal calves in The Netherlands. In: Proceedings of the American Society for Microbiology Conference on Antimicrobial Resistance in Zoonotic Bacteria and Foodborne Pathogens; 15-18 June 2008; Copenhagen, Denmark; 2008. p. 62-3.
13. Van den Eede A, Martens A, Lipinska U, Struelens M, Deplano A, Denis O, et al. High occurrence of methicillinresistant Staphylococcus aureus ST398 in equine nasal samples. Veterinary Microbiology 2008;133:138-44.
14. Tenover FC. Mechanisms of antimicrobial resistance in bacteria. The American Journal of Medicine 2006; 119(Suppl. 1):3-10; discussion 62-70.
15. Aarestrup FM, Wegener HC. The effects of antibiotic usage in food animals on the development of antimicrobial resistance of importance for humans in Campylobacter and Escherichia coli. Microbes and Infection 1999;1:639-44.
16. van Boven M, Veldman KT, de Jong MC, Mevius DJ. Rapid selection of quinolone resistance in Campylobacter jejuni but not in Escherichia coli in individually housed broilers. The Journal of Antimicrobial Chemotherapy 2003;52:719-23. (Pubitemid 37258442)
17. Eveillard M, Martin Y, Hidri N, Boussougant Y, Joly-Guillou ML. Carriage of methicillin-resistant Staphylococcus aureus among hospital employees: prevalence, duration, and transmission to households. Infection Control and Hospital Epidemiology 2004;25:114-20. (Pubitemid 38252339)
18. Kluytmans J, van Leeuwen W, Goessens W, Hollis R, Messer S, Herwaldt L, et al. Food-initiated outbreak of methicillinresistant Staphylococcus aureus analyzed by pheno- and genotyping. Journal of Clinical Microbiology 1995;33:1121-8.
19. Bywater R, Deluyker H, Deroover E, de Jong A, Marion H, McConville M, et al. A European survey of antimicrobial susceptibility among zoonotic and commensal bacteria isolated from food-producing animals. The Journal of Antimicrobial Chemotherapy 2004;54:744-54. (Pubitemid 39386726)
20. Aubry-Damon H, Grenet K, Sall-Ndiaye P, Che D, Cordeiro E, Bougnoux ME, et al. Antimicrobial resistance in commensal flora of pig farmers. Emerging Infectious Diseases 2004;10:873-9. (Pubitemid 38552756)
21. van den Bogaard AE, Stobberingh EE. Epidemiology of resistance to antibiotics. Links between animals and humans. International Journal of Antimicrobial Agents 2000;14: 327-35. (Pubitemid 30224497)
22. Swann MN. Report of the Joint Committee on the Use of Antibiotics in Animal Husbandry and Veterinary Medicine. Her Majesty's Stationary Office, London, UK; 1969.
23. Phillips I. Withdrawal of growth-promoting antibiotics in Europe and its effects in relation to human health. International Journal of Antimicrobial Agents 2007;30:101-7. (Pubitemid 46977184)
24. Grave K, Jensen VF, Odensvik K, Wierup M, Bangen M. Usage of veterinary therapeutic antimicrobials in Denmark, Norway and Sweden following termination of antimicrobial growth promoter use. Preventive Veterinary Medicine 2006;75:123-32. (Pubitemid 43817210)
25. Bengtsson B, Wierup M. Antimicrobial resistance in Scandinavia after ban of antimicrobial growth promoters. Animal Biotechnology 2006;17:147-56. (Pubitemid 44837675)
26. Wierup M. The Swedish experience of the 1986 year ban of antimicrobial growth promoters, with special reference to animal health, disease prevention, productivity, and usage of antimicrobials. Microbial Drug Resistance 2001;7:183-90. (Pubitemid 32586097)
27. SVARM 2007. Swedish Veterinary Antimicrobial Resistance Monitoring. 2008. Available from: URL: http://www.sva.se/upload/pdf/antibiotika/ Cairns%202006%20Bengtsson.pdf (Verified November 2008).
28. NORM/NORM-VET 2006. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway: Tromsø/Oslo; 2007. Available from: URL: http://www.vetinst.no/eng/Research/Publications/Norm-Norm-Vet-Report (Verified November 2008).
29. NARMS 2004 Executive Report. National Antimicrobial Resistance Monitoring System - Enteric Bacteria (NARMS). US Department of Health and Human Services, Food and Drug Administration; 2008. Available from: URL: http://www.fda.gov/cvm/ 2004NARMSExeRpt.htm (Verified November 2008).
30. DANMAP 2006. Use of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria from Food Animals, Foods and Humans in Denmark. 2007. Available from: URL: http://www.danmap.org/pdfFiles/Danmap-2006.pdf (Verified November 2008).
31. MARAN 2005. Monitoring of Antimicrobial Resistance and Antibiotic Usage in Animals in The Netherlands in 2005, 2006. Available from: URL: http://www.cvi.wur.nl/NL/publicaties/rapporten/maranrapportage.
32. EARSS Annual Report 2006. European Antimicrobial Resistance Surveillance System. 2007. Available from: URL: http://www.rivm.nl/earss/result/Monitoring- reports/Annual-reports.jsp (Verified November 2008).
33. Mevius D, Verbrugh H. Research priorities of the MRSA problem in the Dutch animal husbandry. Tijdschrift voor Diergeneeskunde 2006;131:930-3 (in Dutch, abstract in English). (Pubitemid 46179897)
34. Quinn PJ, Markey BK, Carter ME, Donnelly WJ, Leonard FC, editors. Veterinary Microbiology and Microbial Disease. Blackwell Science, Oxford, UK; 2002.
35. Scanvic A, Denic L, Gaillon S, Giry P, Andremont A, Lucet JC. Duration of colonization by methicillin-resistant Staphylococcus aureus after hospital discharge and risk factors for prolonged carriage. Clinical Infectious Diseases 2001;32:1393-8. (Pubitemid 32424271)
36. Kenner J, O'Connor T, Piantanida N, Fishbain J, Eberly B, Viscount H, et al. Rates of carriage of methicillin-resistant and methicillin-susceptible Staphylococcus aureus in an outpatient population. Infection Control and Hospital Epidemiology 2003;24:439-44. (Pubitemid 36818514)
37. Wertheim HF, Vos MC, Ott A, van Belkum A, Voss A, Kluytmans JA, et al. Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. The Lancet 2004;364:703-5. (Pubitemid 39140626)
38. Casewell MW. The nose: an underestimated source of Staphylococcus aureus causing wound infection. The Journal of Hospital Infection 1998;40(Suppl. B):3-11.
39. Gorwitz RJ, Kruszon-Moran D, McAllister SK, McQuillan G, McDougal LK, Fosheim GE, et al. Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001-2004. The Journal of Infectious Diseases 2008;197:1226-34. (Pubitemid 351632753)
40. Wertheim HF, Vos MC, Boelens HA, Voss A, Vandenbroucke-Grauls CM, Meester MH, et al. Low prevalence of methicillin-resistant Staphylococcus aureus (MRSA) at hospital admission in The Netherlands: the value of search and destroy and restrictive antibiotic use. The Journal of Hospital Infection 2004;56:321-5. (Pubitemid 38444086)
41. Begier EM, Frenette K, Barrett NL, Mshar P, Petit S, Boxrud DJ, et al. A high-morbidity outbreak of methicillin-resistant Staphylococcus aureus among players on a college football team, facilitated by cosmetic body shaving and turf burns. Clinical Infectious Diseases 2004;39:1446-53. (Pubitemid 39518207)
42. Ellis MW, Hospenthal DR, Dooley DP, Gray PJ, Murray CK. Natural history of community-acquired methicillin-resistant Staphylococcus aureus colonization and infection in soldiers. Clinical Infectious Diseases 2004;39:971-9. (Pubitemid 39313452)
43. Morris DO, Mauldin EA, O'Shea K, Shofer FS, Rankin SC. Clinical, microbiological, and molecular characterization of methicillin-resistant Staphylococcus aureus infections of cats. American Journal of Veterinary Research 2006;67:1421-5. (Pubitemid 44275499)
44. Noskin GA, Rubin RJ, Schentag JJ, Kluytmans J, Hedblom EC, Jacobson C, et al. National trends in Staphylococcus aureus infection rates: impact on economic burden and mortality over a 6-year period (1998-2003). Clinical Infectious Diseases 2007;45:1132-40. (Pubitemid 47580311)
45. Boyce JM. Environmental contamination makes an important contribution to hospital infection. The Journal of Hospital Infection 2007;65(Suppl. 2):50-4. (Pubitemid 46805839)
46. Albrich WC, Harbarth S. Health-care workers: source, vector, or victim of MRSA? The Lancet Infectious Diseases 2008;8:289-301. (Pubitemid 351615756)
47. Henderson DK. Managing methicillin-resistant staphylococci: a paradigm for preventing nosocomial transmission of resistant organisms. American Journal of Infection Control 2006;34(Suppl. 1):46-54; discussion 64-73.
48. Sexton T, Clarke P, O'Neill E, Dillane T, Humphreys H. Environmental reservoirs of methicillin-resistant Staphylococcus aureus in isolation rooms: correlation with patient isolates and implications for hospital hygiene. The Journal of Hospital Infection 2006;62:187-94. (Pubitemid 43056660)
49. Jevons MP, Coe AW, Parker MT. Methicillin resistance in staphylococci. The Lancet 1963;1:904-7.
50. Pinho MG, de Lencastre H, Tomasz A. An acquired and a native penicillin-binding protein cooperate in building the cell wall of drug-resistant staphylococci. Proceedings of the National Academy of Sciences of the United States of America 2001;98:10886-91. (Pubitemid 32878714)
51. Ito T, Katayama Y, Asada K, Mori N, Tsutsumimoto K, Tiensasitorn C, et al. Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 2001;45:1323-36. (Pubitemid 32374098)
52. Ito T, Ma XX, Takeuchi F, Okuma K, Yuzawa H, Hiramatsu K. Novel type V staphylococcal cassette chromosome mec driven by a novel cassette chromosome recombinase, ccrC. Antimicrobial Agents and Chemotherapy 2004;48:2637-51. (Pubitemid 38823437)
53. Katayama Y, Ito T, Hiramatsu K. A new class of genetic element, staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 2000;44:1549-55. (Pubitemid 30340793)
54. Wu SW, de Lencastre H, Tomasz A. Recruitment of the mecA gene homologue of Staphylococcus sciuri into a resistance determinant and expression of the resistant phenotype in Staphylococcus aureus. Journal of Bacteriology 2001;183:2417-24. (Pubitemid 32249748)
55. Deresinski S. Methicillin-resistant Staphylococcus aureus: an evolutionary, epidemiologic, and therapeutic odyssey. Clinical Infectious Diseases 2005;40:562-73. (Pubitemid 40270226)
56. Grundmann H, Aires-de-Sousa M, Boyce J, Tiemersma E. Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat. The Lancet 2006 2;368:874-85. (Pubitemid 44308640)
57. Deurenberg RH, Vink C, Kalenic S, Friedrich AW, Bruggeman CA, Stobberingh EE. The molecular evolution of methicillin-resistant Staphylococcus aureus. Clinical Microbiology and Infection 2007;13:222-35. (Pubitemid 46603352)
58. Oliveira DC, Tomasz A, de Lencastre H. Secrets of success of a human pathogen: molecular evolution of pandemic clones of methicillin-resistant Staphylococcus aureus. The Lancet Infectious Diseases 2002;2:180-9. (Pubitemid 34462453)
59. Maslow JN, Mulligan ME, Arbeit RD. Molecular epidemiology: application of contemporary techniques to the typing of microorganisms. Clinical Infectious Diseases 1993;17: 153-62.
60. Faria NA, Carrico JA, Oliveira DC, Ramirez M, de Lencastre H. Analysis of typing methods for epidemiological surveillance of both methicillin-resistant and methicillin susceptible Staphylococcus aureus strains. Journal of Clinical Microbiology 2008;46:136-44.
61. Cookson BD, Robinson DA, Monk AB, Murchan S, Deplano A, de Ryck R, et al. Evaluation of molecular typing methods in characterizing a European collection of epidemic methicillinresistant Staphylococcus aureus strains: the HARMONY collection. Journal of Clinical Microbiology 2007;45:1830-7. (Pubitemid 46933914)
62. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. Journal of Clinical Microbiology 1995;33:2233-9.
63. Melles DC, van Leeuwen WB, Snijders SV, Horst-Kreft D, Peeters JK, Verbrugh HA, et al. Comparison of multilocus sequence typing (MLST), pulsed-field gel electrophoresis (PFGE), and amplified fragment length polymorphism (AFLP) for genetic typing of Staphylococcus aureus. Journal of Microbiological Methods 2007;69:371-5. (Pubitemid 46551297)
64. Robinson DA, Enright MC. Multilocus sequence typing and the evolution of methicillin-resistant Staphylococcus aureus. Clinical Microbiology and Infection 2004;10:92-7. (Pubitemid 38256512)
65. 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. Journal of Clinical Microbiology 2000;38:1008-15. (Pubitemid 30140551)
66. Enright MC, Spratt BG. Multilocus sequence typing. Trends in Microbiology 1999;7:482-7. (Pubitemid 30017699)
67. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. Journal of Bacteriology 2004;186:1518-30. (Pubitemid 38248742)
68. Trindade PA, McCulloch JA, Oliveira GA, Mamizuka EM. Molecular techniques for MRSA typing: current issues and perspectives. The Brazilian Journal of Infectious Diseases 2003;7:32-43.
69. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, et al. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 1995;23:4407-14.
70. van der Zee A, Heck M, Sterks M, Harpal A, Spalburg E, Kazobagora L, et al. Recognition of SCCmec types according to typing pattern determined by multienzyme multiplex PCR-amplified fragment length polymorphism analysis of methicillin-resistant Staphylococcus aureus. Journal of Clinical Microbiology 2005;43:6042-7. (Pubitemid 43100658)
71. Oliveira DC, de Lencastre H. Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 2002;46:2155-61. (Pubitemid 34665910)
72. Chongtrakool P, Ito T, Ma XX, Kondo Y, Trakulsomboon S, Tiensasitorn C, et al. Staphylococcal cassette chromosome mec (SCCmec) typing of methicillin-resistant Staphylococcus aureus strains isolated in 11 Asian countries: a proposal for a new nomenclature for SCCmec elements. Antimicrobial Agents and Chemotherapy 2006;50:1001-12. (Pubitemid 43327806)
73. 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. Journal of Clinical Microbiology 2005;43:5026-33. (Pubitemid 41483999)
74. Harmsen D, Claus H, Witte W, Rothganger J, Claus H, Turnwald D, et al. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. Journal of Clinical Microbiology 2003;41:5442-8. (Pubitemid 37543228)
75. Frenay HM, Bunschoten AE, Schouls LM, van Leeuwen WJ, Vandenbroucke-Grauls CM, Verhoef J, et al. Molecular typing of methicillin-resistant Staphylococcus aureus on the basis of protein A gene polymorphism. European Journal of Clinical Microbiology and Infectious Diseases 1996;15:60-4. (Pubitemid 26051263)
76. Malachowa N, Sabat A, Gniadkowski M, Krzyszton-Russjan J, Empel J, Miedzobrodzki J, et al. Comparison of multiplelocus variable-number tandem-repeat analysis with pulsedfield gel electrophoresis, spa typing, and multilocus sequence typing for clonal characterization of Staphylococcus aureus isolates. Journal of Clinical Microbiology 2005;43:3095-100. (Pubitemid 40981307)
77. Kreiswirth B, Kornblum J, Arbeit RD, Eisner W, Maslow JN, McGeer A, et al. Evidence for a clonal origin of methicillin resistance in Staphylococcus aureus. Science 1993;259:227-30. (Pubitemid 23041799)
78. Musser JM, Kapur V. Clonal analysis of methicillin-resistant Staphylococcus aureus strains from intercontinental sources: association of the mec gene with divergent phylogenetic lineages implies dissemination by horizontal transfer and recombination. Journal of Clinical Microbiology 1992;30:2058-63.
79. Feil EJ, Cooper JE, Grundmann H, Robinson DA, Enright MC, Berendt T, et al. How clonal is Staphylococcus aureus? Journal of Bacteriology 2003;185:3307-16. (Pubitemid 36617742)
80. Enright MC, Robinson DA, Randle G, Feil EJ, Grundmann H, Spratt BG. The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proceedings of the National Academy of Sciences of the United States of America 2002;99:7687-92. (Pubitemid 34568752)
81. Kluytmans J. The clonal spread of resistant organisms: methicillin resistant Staphylococcus aureus. In: van der Meer J, editor. Epidemiological Behaviour of Resistant Micro-organisms. Proceedings of the 7th SB Kurhaus Workshop on Antibiotics. Scheveningen, The Netherlands; 1993. pp. 73-85.
82. Aires de Sousa M, de Lencastre H. Bridges from hospitals to the laboratory: genetic portraits of methicillin-resistant Staphylococcus aureus clones. FEMS Immunology and Medical Microbiology 2004;40:101-11. (Pubitemid 38249534)
83. Stefani S, Varaldo PE. Epidemiology of methicillin-resistant staphylococci in Europe. Clinical Microbiology and Infection 2003;9:1179-86. (Pubitemid 38035079)
84. Robinson DA, Enright MC. Evolutionary models of the emergence of methicillin-resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 2003;47:3926-34. (Pubitemid 37485009)
85. Enright MC. The evolution of a resistant pathogen - the case of MRSA. Current Opinion in Pharmacology 2003;3:474-9. (Pubitemid 37221126)
86. Hallin M, Denis O, Deplano A, De Ryck R, Crevecoeur S, Rottiers S, et al. Evolutionary relationships between sporadic and epidemic strains of healthcare-associated methicillinresistant Staphylococcus aureus. Clinical Microbiology and Infection 2008;14:659-69. (Pubitemid 351837026)
87. Aires de Sousa M, de Lencastre H. Evolution of sporadic isolates of methicillin-resistant Staphylococcus aureus (MRSA) in hospitals and their similarities to isolates of community-acquired MRSA. Journal of Clinical Microbiology 2003;41:3806-15. (Pubitemid 36994719)
88. Fey PD, Said-Salim B, Rupp ME, Hinrichs SH, Boxrud DJ, Davis CC, et al. Comparative molecular analysis of community- or hospital-acquired methicillin-resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 2003;47:196-203. (Pubitemid 36070364)
89. Naimi TS, LeDell KH, Como-Sabetti K, Borchardt SM, Boxrud DJ, Etienne J, et al. Comparison of community and health care-associated methicillin-resistant Staphylococcus aureus infection. The Journal of the American Medical Association 2003;290:2976-84. (Pubitemid 37505530)
90. Okuma K, Iwakawa K, Turnidge JD, Grubb WB, Bell JM, O'Brien FG, et al. Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. Journal of Clinical Microbiology 2002;40:4289-94. (Pubitemid 35285827)
91. Armand-Lefevre L, Ruimy R, Andremont A. Clonal comparison of Staphylococcus aureus isolates from healthy pig farmers, human controls, and pigs. Emerging Infectious Diseases 2005;11:711-4. (Pubitemid 40586396)
92. Malik S, Coombs GW, O'Brien FG, Peng H, Barton MD. Molecular typing of methicillin-resistant staphylococci isolated from cats and dogs. The Journal of Antimicrobial Chemotherapy 2006;58:428-31. (Pubitemid 44294959)
93. 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. Veterinary Microbiology 2007;125:128-40. (Pubitemid 47446066)
94. Weese JS, Dick H, Willey BM, McGeer A, Kreiswirth BN, Innis B, et al. Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household. Veterinary Microbiology 2006;115:148-55. (Pubitemid 43786357)
95. Bens CC, Voss A, Klaassen CH. Presence of a novel DNA methylation enzyme in methicillin-resistant Staphylococcus aureus isolates associated with pig farming leads to uninterpretable results in standard pulsed-field gel electrophoresis analysis. Journal of Clinical Microbiology 2006;44:1875-6. (Pubitemid 43726290)
96. van Loo I, Huijsdens X, Tiemersma E, de Neeling A, van de Sande-Bruinsma N, Beaujean D, et al. Emergence of methicillin-resistant Staphylococcus aureus of animal origin in humans. Emerging Infectious Diseases 2007;13:1834-9. (Pubitemid 350248483)
97. Huijsdens XW, van Dijke BJ, Spalburg E, van Santen-Verheuvel MG, Heck ME, Pluister GN, et al. Community-acquired MRSA and pig-farming. Annals of Clinical Microbiology and Antimicrobials 2006;5:26.
98. 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. Veterinary Microbiology 2008;126:383-9. (Pubitemid 350192090)
99. Lucet JC, Chevret S, Durand-Zaleski I, Chastang C, Regnier B. Prevalence and risk factors for carriage of methicillin-resistant Staphylococcus aureus at admission to the intensive care unit: results of a multicenter study. Archives of Internal Medicine 2003;163:181-8. (Pubitemid 36124003)
100. Troillet N, Carmeli Y, Samore MH, Dakos J, Eichelberger K, DeGirolami PC, et al. Carriage of methicillin-resistant Staphylococcus aureus at hospital admission. Infection Control and Hospital Epidemiology 1998;19:181-5. (Pubitemid 128506641)
101. Papia G, Louie M, Tralla A, Johnson C, Collins V, Simor AE. Screening high-risk patients for methicillin-resistant Staphylococcus aureus on admission to the hospital: is it cost effective? Infection Control and Hospital Epidemiology 1999;20:473-7.
102. Bootsma MC, Diekmann O, Bonten MJ. Controlling methicillin-resistant Staphylococcus aureus: quantifying the effects of interventions and rapid diagnostic testing. Proceedings of the National Academy of Sciences of the United States of America 2006;103:5620-5.
103. Panlilio AL, Culver DH, Gaynes RP, Banerjee S, Henderson TS, Tolson JS, et al. Methicillin-resistant Staphylococcus aureus in US hospitals, 1975-1991. Infection Control and Hospital Epidemiology 1992;13:582-6.
104. Klevens RM, Edwards JR, Tenover FC, McDonald LC, Horan T, Gaynes R. Changes in the epidemiology of methicillin-resistant Staphylococcus aureus in intensive care units in US hospitals, 1992-2003. Clinical Infectious Diseases 2006;42:389-91. (Pubitemid 43122317)
105. Johnson AP, Aucken HM, Cavendish S, Ganner M, Wale MC, Warner M, et al. Dominance of EMRSA-15 and -16 among MRSA causing nosocomial bacteraemia in the UK: analysis of isolates from the European Antimicrobial Resistance Surveillance System (EARSS). The Journal of Antimicrobial Chemotherapy 2001;48:143-4. (Pubitemid 32684742)
106. Kluytmans-Vandenbergh MF, Kluytmans JA. Community-acquired methicillin-resistant Staphylococcus aureus: current perspectives. Clinical Microbiology and Infection 2006;12(Suppl. 1):9-15.
107. Hiramatsu K, Cui L, Kuroda M, Ito T. The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends in Microbiology 2001;9:486-93. (Pubitemid 32939356)
108. Salgado CD, Farr BM, Calfee DP. Community-acquired methicillin-resistant Staphylococcus aureus: a metaanalysis of prevalence and risk factors. Clinical Infectious Diseases 2003;36:131-9. (Pubitemid 36143409)
109. Herold BC, Immergluck LC, Maranan MC, Lauderdale DS, Gaskin RE, Boyle-Vavra S, et al. Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. The Journal of the American Medical Association 1998;279:593-8. (Pubitemid 28110205)
110. Bukharie HA, Abdelhadi MS, Saeed IA, Rubaish AM, Larbi EB. Emergence of methicillin-resistant Staphylococcus aureus as a community pathogen. Diagnostic Microbiology and Infectious Diseases 2001;40:1-4. (Pubitemid 32614089)
111. Drews TD, Temte JL, Fox BC. Community-associated methicillin-resistant Staphylococcus aureus: review of an emerging public health concern. WMJ: Official Publication of the State Medical Society of Wisconsin 2006;105:52-7. (Pubitemid 43275870)
112. Nguyen DM, Mascola L, Brancoft E. Recurring methicillin-resistant Staphylococcus aureus infections in a football team. Emerging Infectious Diseases 2005;11: 526-32. (Pubitemid 40462900)
113. Zinderman CE, Conner B, Malakooti MA, LaMar JE, Armstrong A, Bohnker BK. Community-acquired methicillin-resistant Staphylococcus aureus among military recruits. Emerging Infectious Diseases 2004;10:941-4. (Pubitemid 38552772)
114. Shahin R, Johnson IL, Jamieson F, McGeer A, Tolkin J, Ford-Jones EL (For the Toronto Child Care Center Study Group). Methicillin-resistant Staphylococcus aureus carriage in a child care center following a case of disease. Archives of Pediatrics and Adolescent Medicine 1999;153:864-8. (Pubitemid 29362613)
115. Borer A, Gilad J, Yagupsky P, Peled N, Porat N, Trefler R, et al. Community-acquired methicillin-resistant Staphylococcus aureus in institutionalized adults with developmental disabilities. Emerging Infectious Diseases 2002;8:966-70. (Pubitemid 35000817)
116. Beam JW, Buckley B. Community-acquired methicillinresistant Staphylococcus aureus: prevalence and risk factors. Journal of Athletic Training 2006;41:337-40. (Pubitemid 46882406)
117. Jones TF, Kellum ME, Porter SS, Bell M, Schaffner W. An outbreak of community-acquired foodborne illness caused by methicillin-resistant Staphylococcus aureus. Emerging Infectious Diseases 2002;8:82-4. (Pubitemid 34094288)
118. Lee JH. Methicillin (oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Applied and Environmental Microbiology 2003;69:6489-94. (Pubitemid 37420181)
119. Normanno G, Corrente M, La Salandra G, Dambrosio A, Quaglia NC, Parisi A, et al. Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animal origin product in Italy. International Journal of Food Microbiology 2007;117:219-22. (Pubitemid 46802856)
120. Muto CA, Jernigan JA, Ostrowsky BE, Richet HM, Jarvis WR, Boyce JM, et al. SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and enterococcus. Infection Control and Hospital Epidemiology 2003;24:362-86. (Pubitemid 36612323)
121. Struelens MJ, Denis O. Can we control the spread of antibiotic-resistant nosocomial pathogens? The methicillin-resistant Staphylococcus aureus paradigm. Current Opinion in Infectious Diseases 2006;19:321-2. (Pubitemid 43982502)
122. Simor AE, Phillips E, McGeer A, Konvalinka A, Loeb M, Devlin HR, et al. Randomized controlled trial of chlorhexidine gluconate for washing, intranasal mupirocin, and rifampin and doxycycline versus no treatment for the eradication of methicillin-resistant Staphylococcus aureus colonization. Clinical Infectious Diseases 2007;44:178-85. (Pubitemid 46079977)
123. Kniehl E, Becker A, Forster DH. Bed, bath and beyond: pitfalls in prompt eradication of methicillin-resistant Staphylococcus aureus carrier status in healthcare workers. The Journal of Hospital Infection 2005;59:180-7. (Pubitemid 40197779)
124. Marshall C, Wesselingh S, McDonald M, Spelman D. Control of endemic MRSA - what is the evidence? A personal view. The Journal of Hospital Infection 2004;56:253-68. (Pubitemid 38444077)
125. Devriese LA, Van Damme LR, Fameree L. Methicillin (cloxacillin)-resistant Staphylococcus aureus strains isolated from bovine mastitis cases. Journal of Veterinary Medicine Series B 1972;19:598-605.
126. van Duijkeren E, Box AT, Heck ME, Wannet WJ, Fluit AC.
127. Weese JS, Archambault M, Willey BM, Hearn P, Kreiswirth BN, Said-Salim B, et al. Methicillin-resistant Staphylococcus aureus in horses and horse personnel, 2000-2002. Emerging Infectious Diseases 2005;1:430-5. (Pubitemid 40315729)
128. Goni P, Vergara Y, Ruiz J, Albizu I, Vila J, Gomez-Lus R. Antibiotic resistance and epidemiological typing of Staphylococcus aureus strains from ovine and rabbit mastitis. International Journal of Antimicrobial Agents 2004;23:268-72. (Pubitemid 38283596)
129. Juhasz-Kaszanyitzky E, Janosi S, Somogyi P, Dan A, van der Graaf-van Bloois L, van Duijkeren E, et al. MRSA transmission between cows and humans. Emerging Infectious Diseases 2007;13:630-2. (Pubitemid 46525116)
130. Mooij T, Troelstra A, Jenkins J, Thijssen S. MRSA in calves. Infectieziekten Bulletin 2007;18:234-6 (in Dutch, abstract in English).
131. Leenders A, Janssen M, Renders N, Pelk M. Pig's MRSA on a poultry farm? Infectieziekten Bulletin 2007;18:43-4 (in Dutch, abstract in English).
132. 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. Antimicrobial Agents and Chemotherapy 2008;52:3817-9.
133. Leonard FC, Markey BK. Meticillin-resistant Staphylococcus aureus in animals: a review. Veterinary Journal 2008;175:27-36. (Pubitemid 351187517)
134. Loeffler A, Boag AK, Sung J, Lindsay JA, Guardabassi L, Dalsgaard A, et al. Prevalence of methicillin-resistant Staphylococcus aureus among staff and pets in a small animal referral hospital in the UK. The Journal of Antimicrobial Chemotherapy 2005;56:692-7. (Pubitemid 41487770)
135. Manian FA. Asymptomatic nasal carriage of mupirocinresistant, methicillin-resistant Staphylococcus aureus (MRSA) in a pet dog associated with MRSA infection in household contacts. Clinical Infectious Diseases 2003;36:26-8.
136. van Duijkeren E, Wolfhagen MJ, Box AT, Heck ME, Wannet WJ, Fluit AC. Human-to-dog transmission of methicillin-resistant Staphylococcus aureus. Emerging Infectious Diseases 2004;10:2235-7. (Pubitemid 39587357)
137. Broens EM, Graat EAM, Van der Wolf PJ, Van den Broek IVF, Tiemersma EW, Van de Giessen AW, et al. Prevalence study and risk factor analysis of NT-MRSA in pigs in The Netherlands. In: Proceedings of the American Society for Microbiology Conference on Antimicrobial Resistance in Zoonotic Bacteria and Foodborne Pathogens; 15-18 June 2008; Copenhagen, Denmark; 2008. p. 37.
138. Dewaele I, De Man I, Stael A, Delputte P, Butaye P, Vlaemynck G, et al. Methicillin resistant Staphylococcus aureus (MRSA) on Belgian pig farms. In: Proceedings of the American Society for Microbiology Conference on Antimicrobial Resistance in Zoonotic Bacteria and Foodborne Pathogens; 15-18 June 2008; Copenhagen, Denmark; 2008. p. 43.
139. Guardabassi L, Stegger M, Skov R. Retrospective detection of methicillin resistant and susceptible Staphylococcus aureus ST398 in Danish slaughter pigs. Veterinary Microbiology 2007;122:384-6. (Pubitemid 46756027)
140. Meemken D, Cuny C, Witte W, Eichler U, Staudt R, Blaha T. Occurrence of MRSA in pigs and in humans involved in pig production - preliminary results of a study in the northwest of Germany. Deutsche Tierärztliche Wochenschrift 2008;115:132-9 (in German, abstract in English). (Pubitemid 351519044)
141. Smith TC, Male MJ, Harper AL, Moritz-Korolev ED, Diekema DJ, Herwaldt LA. Isolation of methicillin-resistant Staphylococcus aureus (MRSA) from swine in the midwestern United States. In: Program and Abstracts Book of the International Conference on Emerging Infectious Diseases, Addendum; 16-19 March 2008; Atlanta, GA; 2008. p. 10.
142. Weese JS, Lefebvre SL. Risk factors for methicillin-resistant Staphylococcus aureus colonization in horses admitted to a veterinary teaching hospital. Canadian Veterinary Journal 2007;48:921-6. (Pubitemid 47559523)
143. Duquette RA, Nuttall TJ. Methicillin-resistant Staphylococcus aureus in dogs and cats: an emerging problem? Journal of Small Animal Practice 2004;45:591-7. (Pubitemid 39656329)
144. Pfeiffer D, Lloyd D, Loeffler A, Soares-Magalhaes R, Rich M, Roberts L, et al. Identifying risk factors associated with MRSA infection in companion animals. Journal of Small Animal Practice 2005;46:490. (Pubitemid 41502822)
145. Broens EM, Graat EAM, Van der Wolf PJ, van Duijkeren E, van Nes A, Wagenaar JA, et al. Transmission of NTMRSA in the pig production chain in The Netherlands. In: Proceedings of the 20th International Pig Veterinary Science Congress. Volume 1: Keynote and Oral Papers; 22-26 June 2008; Durban, South Africa; 2008. p. 165.
146. Weese JS, Rousseau J. Attempted eradication of methicillinresistant Staphylococcus aureus colonisation in horses on two farms. Equine Veterinary Journal 2005;37:510-4. (Pubitemid 41585888)
147. Scott GM, Thomson R, Malone-Lee J, Ridgway GL. Cross-infection between animals and man: possible feline transmission of Staphylococcus aureus infection in humans? The Journal of Hospital Infection 1988;12:29-34.
148. Cefai C, Ashurst S, Owens C. Human carriage of methicillinresistant Staphylococcus aureus linked with pet dog. The Lancet 1994;344:539-40. (Pubitemid 24261580)
149. Seguin JC, Walker RD, Caron JP, Kloos WE, George CG, Hollis RJ, et al. Methicillin-resistant Staphylococcus aureus outbreak in a veterinary teaching hospital: potential human-to-animal transmission. Journal of Clinical Microbiology 1999;37:1459-63. (Pubitemid 29187818)
150. Wulf M, van Nes A, Eikelenboom-Boskamp A, de Vries J, Melchers W, Klaassen C, et al. Methicillin-resistant Staphylococcus aureus in veterinary doctors and students, The Netherlands. Emerging Infectious Diseases 2006;12:1939-41. (Pubitemid 44904935)
151. van den Broek IVF, van Cleef BAGL, Haenen A, Broens EM, van der Wolf PJ, van den Broek MJM, et al. Methicillinresistant Staphylococcus aureus in people living and working in pig farms. Epidemiology and Infection 2008, doi: 10.1017/S0950268808001507.
152. Wulf MW, Sorum M, van Nes A, Skov R, Melchers WJ, Klaassen CH, et al. Prevalence of methicillin-resistant Staphylococcus aureus among veterinarians: an international study. Clinical Microbiology and Infection 2008;14:29-34. (Pubitemid 350226567)
153. van Rijen MM, Van Keulen PH, Kluytmans JA. Increase in a Dutch hospital of methicillin-resistant Staphylococcus aureus related to animal farming. Clinical Infectious Diseases 2008;46:261-3. (Pubitemid 351269166)
154. Witte W, Strommenger B, Stanek C, Cuny C. Methicillin-resistant Staphylococcus aureus ST398 in humans and animals, Central Europe. Emerging Infectious Diseases 2007;13:255-8. (Pubitemid 46193169)
155. Ekkelenkamp MB, Sekkat M, Carpaij N, Troelstra A, Bonten MJ. Endocarditis due to meticillin-resistant Staphylococcus aureus originating from pigs. Nederlands Tijdschrift voor Geneeskunde 2006;150:2442-7 (in Dutch, abstract in English). (Pubitemid 44775440)
156. Declercq Ph, Petré D, Gordts B, Voss A. Complicated community-acquired soft tissue infection by MRSA from porcine origin. Infection 2007, doi: 10.1007/s15010-007- 7029-4.
157. Wulf MW, Markestein A, van der Linden FT, Voss A, Klaassen C, Verduin CM. First outbreak of methicillin resistant Staphylococcus aureus ST398 in a Dutch hospital, June 2007. Euro Surveillance 2008;13:8051.
158. Teale CJ. Antimicrobial resistance and the food chain. Journal of Applied Microbiology 2002;92(Suppl. I):85-9.
159. van Loo IH, Diederen BM, Savelkoul PH, Woudenberg JH, Roosendaal R, van Belkum A, et al. Methicillin-resistant Staphylococcus aureus in meat products, The Netherlands. Emerging Infectious Diseases 2007;13:1753-5. (Pubitemid 350126206)
160. Prevalence of MRSA in Meat Products, 2007 - Fact Sheet. Dutch Food and Safety Authority. 2007. Available from: URL: http://www.vwa.nl/portal/page?- pageid=119, 1639827&-dad=portal&-schema=PORTAL&p-file-id= 25742 (Verified November 2008).