Analysis of transmission of MRSA and ESBL-E among pigs and farm personnel

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Schmithausen, Ricarda Maria ^a,b   Schulze Geisthoevel, Sophia Veronika ^b   Stemmer, Franziska ^b   El Jade, Mohamed ^a   Reif, Marion ^a   Hack, Sylvia ^a   Meilaender, Alina ^a   Montabauer, Gabriele ^a   Fimmers, Rolf ^a   Parcina, Marijo ^a   Hoerauf, Achim ^a   Exner, Martin ^a   Petersen, Brigitte ^b   Bierbaum, Gabriele ^a   Bekeredjian Ding, Isabelle ^a,c   Smith, Tara C ^d  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c PAUL EHRLICH INSTITUT   (Germany)

^d KENT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BETA LACTAM ANTIBIOTIC; CEFAZOLIN; CEFOTAXIME; CEFOXITIN; CEFPODOXIME; CEFTAZIDIME; CIPROFLOXACIN; CLINDAMYCIN; COTRIMOXAZOLE; DOXYCYCLINE; ERYTHROMYCIN; GENTAMICIN; LINCOSAMIDE; MACROLIDE; METICILLIN; MOXIFLOXACIN; OXACILLIN; PENICILLIN DERIVATIVE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; SULFONAMIDE; TETRACYCLINE; VANCOMYCIN;

AGRICULTURAL WORKER; AIR SAMPLING; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATION; CARCASS; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; ESCHERICHIA COLI; EXTENDED SPECTRUM BETA LACTAMASE PRODUCING ENTEROBACTERIACEAE; GERMANY; HUMAN; LIVESTOCK; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOLECULAR TYPING; NONHUMAN; NOSE SMEAR; PIG; PIG FARMING; PREVALENCE; SLAUGHTERHOUSE; ANIMAL; ANIMAL HUSBANDRY; ESCHERICHIA COLI INFECTION; FEMALE; MALE; MICROBIOLOGY; STAPHYLOCOCCUS INFECTION; TRANSMISSION; ZOONOSIS;

ANIMAL HUSBANDRY; ANIMALS; BETA-LACTAM RESISTANCE; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; HUMANS; MALE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCAL INFECTIONS; SWINE; ZOONOSES;

EID: 84947755463     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0138173     Document Type: Article

References (94)

1. Hammerum AM, Heuer OE, Lester C.H., Agersø Y, Seyfarth AM, Emborg HD, et al. Comment on: withdrawal of growth-promoting antibiotics in Europe and its effects in relation to human health. Int J Antimi-crob Agents. 2007; 30(5):466-8. doi:10.1016/j.ijantimicag.2007.07.012 PMID: 17884357.
2. Gilchrist MJ, Greko C, Wallinga D.B., Beran GW, Riley DG, Thorne PS. The potential role of concentrated animal feeding operations in infectious disease epidemics and antibiotic resistance. Environ Health Perspect. 2007; 115(2):313-6. doi:10.1289/ehp.8837 PMID: 17384785; PubMed Central PMCID: PMCPMC1817683.
3. Mathew AG, Cissell R, Liamthong S. Antibiotic resistance in bacteria associated with food animals: a United States perspective of livestock production. Foodborne Pathog Dis. 2007; 4(2):115-33. doi:10.1089/fpd.2006.0066 PMID: 17600481.
4. Wegener HC. Antibiotics in animal feed and their role in resistance development. Curr Opin Microbiol. 2003; 6(5):439-45. PMID: 14572534.
5. 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 Infect. 1999; 1(8):639-44. PMID: 10611741.
6. Hiramatsu K, Okuma K, Ma X.X., Yamamoto M., Hori S, Kapi M. New trends in Staphylococcus aureus infections: glycopeptide resistance in hospital and methicillin resistance in the community. Curr Opin Infect Dis. 2002; 15(4):407-13. PMID: 12130938.
7. Strommenger B, Bartels MD, Kurt K, Layer F., Rohde SM, Boye K, et al. Evolution of methicillin-resistant Staphylococcus aureus towards increasing resistance. J Antimicrob Chemother. 2014; 69(3):616-22. doi:10.1093/jac/dkt413 PMID: 24150844.
8. Nübel U., Dordel J, Kurt K., Strommenger B, Westh H, Shukla SK, et al A timescale for evolution, population expansion, and spatial spread of an emerging clone of methicillin-resistant Staphylococcus aureus. PLOS Pathog. 2010; 6(4): e1000855. doi:10.1371/journal.ppat.1000855 PMID: 20386717; PubMed Central PMCID: PMCPMC2851736.
9. Graveland H, Duim B, van Duijkeren E, Heederik D, Wagenaar JA Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. Int J Med Microbiol. 2011; 301(8):630-4. doi:10.1016/j.ijmm.2011.09.004 PMID: 21983338.
10. Graveland H, Wagenaar JA, Bergs K, Heesterbeek H., Heederik D. Persistence of livestock associated MRSACC398 in humans is dependent on intensity of animal contact. PLOS One. 2011; 6(2): e16830. doi:10.1371/journal.pone.0016830 PMID: 21347386; PubMed Central PMCID: PMCPMC3036727.
11. VAN DEN Broek IV, VANCleef BA, Haenen A, Broens E.M., VAN DER Wolf PJ, VAN DEN Broek MJ, et al. Methicillin-resistant Staphylococcus aureus in people living and working in pig farms. Epidemiol Infect. 2009; 137(5):700-8. doi:10.1017/S0950268808001507 PMID: 18947444.
12. 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. Emerg Infect Dis. 2007; 13(12):1834-9. doi:10.3201/eid1312.070384 PMID: 18258032; PubMed Central PMCID: PMCPMC2876750.
13. Cuny C, Nathaus R, Layer F., Strommenger B, Altmann D, Witte W. Nasal colonization of humans with methicillin-resistant Staphylococcus aureus (MRSA) CC398 with and without exposure to pigs. PLOS One. 2009; 4(8): e6800. doi:10.1371/journal.pone. 0006800 PMID: 19710922; PubMed Central PMCID: PMCPMC2728842.
14. Cuny C, Köck R, Witte W. Livestock associated MRSA (LA-MRSA) and its relevance for humans in Germany. Int J Med Microbiol. 2013; 303(6-7):331-7. doi:10.1016/j.ijmm.2013.02.010 PMID: 23607972.
15. Bootsma MC, Wassenberg MW, Trapman P, Bonten MJ The nosocomial transmission rate of animal-associated ST398 meticillin-resistant Staphylococcus aureus. J R Soc Interface. 2011; 8(57):578-84. doi:10.1098/rsif.2010.0349 PMID: 20861037; PubMed Central PMCID: PMCPMC3061118.
16. Jakobsen L, Kurbasic A, Skjøt-Rasmussen L, Ejrnaes K, Porsbo LJ, Pedersen K, et al. Escherichia coli isolates from broiler chicken meat, broiler chickens, pork, and pigs share phylogroups and antimicrobial resistance with community-dwelling humans and patients with urinary tract infection. Foodborne Pathog Dis. 2010; 7(5):537-47. doi:10.1089/fpd.2009.0409 PMID: 20039794.
17. Magiorakos AP, Srinivasan A, Carey R.B., Carmeli Y., Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012; 18(3):268-81. Epub 2011/07/29. doi:10.1111/j.1469-0691.2011.03570.x S1198-743X(14)61632-3 [pii]. PMID: 21793988.
18. Seiler C, Berendonk TU. Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol. 2012; 3:399. Epub 2012/12/19. doi:10.3389/fmicb.2012.00399 PMID: 23248620; PubMed Central PMCID: PMC3522115.
19. Leelaporn A, Paulsen IT, Tennent J.M., Littlejohn TG, Skurray RA. Multidrug resistance to antiseptics and disinfectants in coagulase-negative staphylococci. J Med Microbiol. 1994; 40(3):214-20. Epub 1994/03/01. PMID: 8114073.
20. Littlejohn TG, Paulsen IT, Gillespie M.T., Tennent JM, Midgley M, Jones IG, et al Substrate specificity and energetics of antiseptic and disinfectant resistance in Staphylococcus aureus. FEMS Microbiol Lett. 1992; 74(2-3):259-65. Epub 1992/08/15. PMID: 1526458.
21. Teuber M. Veterinary use and antibiotic resistance. CurrOpin Microbiol. 2001; 4(5):493-9. PMID: 11587923.
22. 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 PMID: 17367960.
23. van Duijkeren E., Ikawaty R, Broekhuizen-Stins MJ, Jansen M.D., 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 PMID: 17765409.
24. Lassok B, Tenhagen BA From pig to pork: methicillin-resistant Staphylococcus aureus in the pork production chain. J Food Prot. 2013; 76(6): 1095-108. doi:10.4315/0362-028X. JFP-12-341 PMID: 23726208.
25. Beneke B, Klees S, Stührenberg B, Fetsch A., Kraushaar B, Tenhagen BA. Prevalence of methicillin-resistant Staphylococcus aureus in a fresh meat pork production chain. J Food Prot. 2011; 74(1):126-9. doi:10.4315/0362-028X. JFP-10-250 PMID: 21219774.
26. Wulf MW, Verduin CM, 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(1):61-5. doi:10.1007/s10096-011-1269-z PMID: 21533878.
27. van Cleef B.A., Verkade EJ, Wulf M.W., Buiting AG, Voss A, Huijsdens XW, et al Prevalence of livestock-associated MRSA in communities with high pig-densities in The Netherlands. PLOS One. 2010; 5(2): e9385. doi:10.1371/journal.pone.0009385 PMID: 20195538; PubMed Central PMCID: PMCPMC2828479.
28. Monaco M, Pedroni P, Sanchini A., Bonomini A, Indelicato A, Pantosti A. Livestock-associated methicillin-resistant Staphylococcus aureus responsible for human colonization and infection in an area of Italy with high density of pig farming. BMC Infect Dis. 2013; 13:258. doi:10.1186/1471-2334-13-258 PMID: 23731504; PubMed Central PMCID: PMCPMC3679754.
29. Geser N, Stephan R, Kuhnert P., Zbinden R, Kaeppeli U, Cernela N., et al. Fecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae in swine and cattle at slaughter in Switzerland. J Food Prot. 2011; 74(3):446-9. doi:10.4315/0362-028X. JFP-10-372 PMID: 21375882.
30. Pitout JD, Sanders CC, Sanders WE Jr. Antimicrobial resistance with focus on beta-lactam resistance in gram-negative bacilli. Am J Med. 1997; 103(1):51-9. Epub 1997/07/01. S0002934397000442 [pii]. PMID: 9236486.
31. Nedbalcova K, Nechvatalova K, Pokludova L., Bures J, Kucerova Z, Koutecka L., et al. Resistance to selected beta-lactam antibiotics. Vet Microbiol. 2014; 171(3-4):328-36. Epub 2014/03/13. doi:10.1016/j.vetmic.2014.02.004 S0378-1135(14)00079-0 [pii]. PMID: 24612952.
32. Geser N, Stephan R, Korczak BM, Beutin L, Hächler H. Molecular identification of extended-spectrum-β-lactamase genes from Enterobacteriaceae isolated from healthy human carriers in Switzerland. Antimicrob Agents Chemother. 2012; 56(3):1609-12. doi:10.1128/AAC.05539-11 PMID: 22155836; PubMed Central PMCID: PMCPMC3294945.
33. Horton RA, Randall LP, Snary E.L., Cockrem H., Lotz S, Wearing H, et al Fecal carriage and shedding density of CTX-M extended-spectrum {beta}-lactamase-producing escherichia coli in cattle, chickens, and pigs: implications for environmental contamination and food production. Appl Environ Microbiol. 2011; 77(11):3715-9. doi:10.1128/AEM.02831-10 PMID: 21478314; PubMed Central PMCID: PMCPMC3127594.
34. Leverstein-van Hall MA, Dierikx CM, Cohen Stuart J, Voets GM, van den Munckhof MP, van Essen-Zandbergen A, et al. Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect. 2011; 17(6):873-80. doi:10.1111/j.1469-0691.2011.03497.x PMID: 21463397.
35. Geser N, Stephan R, Hächler H. Occurrence and characteristics of extended-spectrum β-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Vet Res. 2012; 8:21. doi:10.1186/1746-6148-8-21 PMID: 22397509; PubMed Central PMCID: PMCPMC3319423.
36. Marshall BM, Levy SB Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev. 2011; 24(4):718-33. doi:10.1128/CMR.00002-11 PMID: 21976606; PubMed Central PMCID: PMCPMC3194830.
37. Harris DL. Multi-Site Pig Production. Iowa 2000.
38. Feller W. On the Kolmogorov-Smirnov Limit Theorems for Empirical Distributions. The Annals of Mathematical Statistics 1948. p. 177-89.
39. EUCAST ECoAST. Clinical breakpoints (Bacterial v3.1). Central Hospital, 351 85 Växjö, Sweden 2013.
40. Harmsen D, Claus H, Witte W., Rothgänger J, Turnwald D., Vogel U. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol. 2003; 41(12):5442-8. PMID: 14662923; PubMed Central PMCID: PMCPMC309029.
41. Strommenger B, Kettlitz C, Werner G., Witte W. Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus. J Clin Microbiol. 2003; 41 (9):4089-94. PMID: 12958230; PubMed Central PMCID: PMCPMC193808.
42. Naseer U, Sundsfjord A. The CTX-M conundrum: dissemination of plasmids and Escherichia coli clones. Microb Drug Resist. 2011; 17(1):83-97. doi:10.1089/mdr.2010.0132 PMID: 21281129.
43. Brolund A, Hæggman S, Edquist PJ, Gezelius L, Olsson-Liljequist B, Wisell KT, et al. The DiversiLab system versus pulsed-field gel electrophoresis: characterisation of extended spectrum β-lactamase producing Escherichia coli and Klebsiella pneumoniae. J Microbiol Methods. 2010; 83(2):224-30. doi:10.1016/j.mimet.2010.09.004 PMID: 20849889.
44. Köck R., Harlizius J, Bressan N., Laerberg R, Wieler LH, Witte W, et al Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) among pigs on German farms and import of livestock-related MRSA into hospitals. Eur J Clin Microbiol Infect Dis. 2009; 28(11):1375-82. doi:10.1007/s10096-009-0795-4 PMID: 19701815; PubMed Central PMCID: PMCPMC2772956.
45. Wagenaar JA, Yue H, Pritchard J., Broekhuizen-Stins M, Huijsdens X, Mevius D.J., et al. Unexpected sequence types in livestock associated methicillin-resistant Staphylococcus aureus (MRSA): MRSA ST9 and a single locus variant of ST9 in pig farming in China. Vet Microbiol. 2009; 139(3-4):405-9. Epub 2009/07/18. doi:10.1016/j.vetmic.2009.06.014 S0378-1135(09)00298-3 [pii]. PMID: 19608357.
46. Grohs P, Tillecovidin B, Caumont-Prim A, Carbonnelle E., Day N, Podglajen I, et al Comparison of five media for detection of extended-spectrum Beta-lactamase by use of the wasp instrument for automated specimen processing. J Clin Microbiol. 2013; 51(8):2713-6. Epub 2013/05/24. doi:10.1128/JCM.00077-13 JCM.00077-13 [pii]. PMID: 23698524; PubMed Central PMCID: PMC3719624.
47. Hu YY, Cai JC, Zhou H.W., Chi D., Zhang XF, Chen WL, et al. Molecular typing of CTX-M-producing escherichia coli isolates from environmental water, swine feces, specimens from healthy humans, and human patients. Appl Environ Microbiol. 2013; 79(19):5988-96. doi:10.1128/AEM.01740-13 PMID: 23892737; PubMed Central PMCID: PMCPMC3811354.
48. Liu BT, Yang QE, Li L, Sun J., Liao XP, Fang LX, et al. Dissemination and characterization of plasmids carrying oqxAB-bla CTX-M genes in Escherichia coli isolates from food-producing animals. PLOS One. 2013; 8(9): e73947. doi:10.1371/journal.pone.0073947 PMID: 24040123; PubMed Central PMCID: PMCPMC3767592.
49. Tian GB, Wang HN, Zou L.K., Tang JN, Zhao YW, Ye MY, et al Detection of CTX-M-15, CTX-M-22, and SHV-2 extended-spectrum beta-lactamases (ESBLs) in Escherichia coli fecal-sample isolates from pig farms in China. Foodborne Pathog Dis. 2009; 6(3):297-304. doi:10.1089/fpd.2008.0164 PMID: 19272004.
50. Blanc V, Mesa R, Saco M., Lavilla S, Prats G, Miró E, et al. ESBL-and plasmidicclassC beta-lacta-mase-producing E. coli strains isolated from poultry, pig and rabbit farms. Vet Microbiol. 2006; 118(3-4):299-304. doi:10.1016/j.vetmic.2006.08.002 PMID: 16973308.
51. Cavaco LM, Abatih E, Aarestrup F.M., Guardabassi L. Selection and persistence of CTX-M-producing Escherichia coli in the intestinal flora of pigs treated with amoxicillin, ceftiofur, orcefquinome. Antimicrob Agents Chemother. 2008; 52(10):3612-6. Epub 2008/07/23. doi:10.1128/AAC.00354-08 AAC.00354-08 [pii]. PMID: 18644956; PubMed Central PMCID: PMC2565910.
52. Hammerum AM, Larsen J, Andersen V.D., Lester CH, Skovgaard Skytte TS, Hansen F, et al. Characterization of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli obtained from Danish pigs, pig farmers and their families from farms with high or no consumption of third-or fourth-generation cephalosporins. J Antimicrob Chemother. 2014. doi:10.1093/jac/dku180 PMID: 24908045.
53. Voets GM, Platteel TN, Fluit A.C., Scharringa J., Schapendonk CM, Stuart JC, et al. Population distribution of Beta-lactamase conferring resistance to third-generation cephalosporins in human clinical Enter-obacteriaceae in the Netherlands. PLOS One. 2012; 7(12): e52102. doi:10.1371/journal.pone.0052102 PMID: 23284886; PubMed Central PMCID: PMCPMC3527366.
54. Deplano A, Denis O, Rodriguez-Villalobos H, De Ryck R, Struelens MJ, Hallin M. Controlled performance evaluation of the DiversiLab repetitive-sequence-based genotyping system for typing multidrug-resistant health care-associated bacterial pathogens. J Clin Microbiol. 2011; 49(10):3616-20. doi:10.1128/JCM.00528-11 PMID: 21813717; PubMed Central PMCID: PMCPMC3187349.
55. Smith DL, Harris AD, Johnson J.A., Silbergeld EK, Morris JG. Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. Proc Natl Acad Sci USA. 2002; 99(9):6434-9. doi:10.1073/pnas.082188899 PMID: 11972035; PubMed Central PMCID: PMCPMC122966.
56. Levy SB, Marshall B. Antibacterial resistance worldwide: causes, challenges and responses. Nat Med. 2004; 10(12 Suppl):S122-9. doi:10.1038/nm1145 PMID: 15577930.
57. Friese A, Schulz J, Hoehle L., Fetsch A, Tenhagen BA, Hartung J, et al Occurrence of MRSA in air and housing environment of pig barns. Vet Microbiol. 2012; 158(1-2):129-35. doi:10.1016/j.vetmic.2012. 01.019 PMID: 22386671.
58. Friese A, Schulz J, Laube H., von Salviati C, Hartung J, Roesler U. Faecal occurrence and emissions of livestock-associated methicillin-resistant Staphylococcus aureus (laMRSA) and ESbl/AmpC-producing E. coli from animal farms in Germany. Berl Munch Tierarztl Wochenschr. 2013; 126(3-4):175-80. PMID: 23540202.
59. Broens EM, Graat EA, van der Wolf PJ, van de Giessen AW, van Duijkeren E, Wagenaar JA, et al. MRSA CC398 in the pig production chain. Prev Vet Med. 2011; 98(2-3):182-9. doi:10.1016/j.prevetmed.2010.10.010 PMID: 21075466.
60. van der Fels-Klerx HJ, Puister-Jansen LF, van Asselt ED, Burgers SL. Farm factors associated with the use of antibiotics in pig production. J AnimSci. 2011; 89(6):1922-9. doi:10.2527/jas.2010-3046 PMID: 21606448.
61. Hansen KH, Damborg P, Andreasen M., Nielsen SS, Guardabassi L. Carriage and fecal counts of cefotaxime M-producing Escherichia coli in pigs: a longitudinal study. Appl Environ Microbiol. 2013; 79 (3):794-8. doi:10.1128/AEM.02399-12 PMID: 23160131; PubMed Central PMCID: PMCPMC3568556.
62. 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 PMID: 18023542.
63. Nadimpalli M, Rinsky JL, Wing S, Hall D., Stewart J, Larsen J, et al Persistence of livestock-associated antibiotic-resistant Staphylococcus aureus among industrial hog operation workers in North Carolina over 14 days. Occup Environ Med. 2015; 72(2):90-9. Epub 2014/09/10. doi:10.1136/oemed-2014-102095 PMID: 25200855; PubMed Central PMCID: PMC4316926.
64. Rinsky JL, Nadimpalli M, Wing S., Hall D, Baron D, Price L.B., et al. Livestock-associated methicillin and multidrug resistant Staphylococcus aureus is present among industrial, not antibiotic-free livestock operation workers in North Carolina. PLOS One. 2013; 8(7): e67641. Epub 2013/07/12. doi:10.1371/journal.pone.0067641 PMID: 23844044; PubMed Central PMCID: PMC3699663.
65. Kock R, Loth B, Koksal M., Schulte-Wulwer J, Harlizius J, Friedrich AW Persistence of nasal colonization with livestock-associated methicillin-resistant Staphylococcus aureus in pig farmers after holidays from pig exposure. Appl Environ Microbiol. 2012; 78(11):4046-7. Epub 2012/03/27. doi:10.1128/AEM.00212-12 AEM.00212-12 [pii]. PMID: 22447613; PubMed Central PMCID: PMC3346418.
66. Escudero E, Vinué L, Teshager T, Torres C, Moreno MA. Resistance mechanisms and farm-level distribution of fecal Escherichia coli isolates resistant to extended-spectrum cephalosporins in pigs in Spain. Res Vet Sci. 2010; 88(1):83-7. doi:10.1016/j.rvsc.2009.05.021 PMID: 19577265.
67. Smith TC, Male MJ, Harper A.L., Kroeger JS, Tinkler G.P., 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 PMID: 19145257; PubMed Central PMCID: PMCPMC2626282.
68. Callens B, Persoons D, Maes D., Laanen M, Postma M, Boyen F., et al. Prophylactic and metaphylactic antimicrobial use in Belgian fattening pig herds. Prev Vet Med. 2012; 106(1):53-62. doi:10.1016/j. prevetmed.2012.03.001 PMID: 22494905.
69. MARAN. MARAN 2009, Monitoring of Antimicrobial Resistanceand Antibiotic Usage in Animals in the Netherlands In 2009. 2009.
70. Aarestrup FM, Seyfarth AM, Emborg H.D., Pedersen K., Hendriksen RS, Bager F. Effect of abolishment of the use of antimicrobial agents for growth promotion on occurrence of antimicrobial resistance in fecal enterococci from food animals in Denmark. Antimicrob Agents Chemother. 2001; 45(7):2054-9. Epub 2001/06/16. doi:10.1128/AAC.45.7.2054-2059.2001 PMID: 11408222; PubMed Central PMCID: PMC90599.
71. Boerlin P, Wissing A, Aarestrup F.M., Frey J., Nicolet J. Antimicrobial growth promoter ban and resistance to macrolides and vancomycin in enterococci from pigs. J Clin Microbiol. 2001; 39(11):4193-5. Epub 2001/10/30. doi:10.1128/JCM.39.11.4193-4195.2001 PMID: 11682559; PubMed Central PMCID: PMC88516.
72. Cormican MG, Erwin ME, Jones RN Avoparcin, a glycopeptide used in animal foods: antimicrobial spectrum and potency tested against human isolates from the United States. Diagn Microbiol Infect Dis. 1997; 29(4):241-8. Epub 1998/02/12. S0732-8893(97)00134-X [pii]. PMID: 9458981.
73. Agerso Y, Aarestrup FM Voluntary ban on cephalosporin use in Danish pig production has effectively reduced extended-spectrum cephalosporinase-producing Escherichia coli in slaughter pigs. J Antimicrob Chemother. 2013; 68(3):569-72. Epub 2012/11/07. doi:10.1093/jac/dks427 dks427 [pii]. PMID: 23129728.
74. Kennedy K, Collignon P. Colonisation with Escherichia coli resistant to "critically important" antibiotics: a high risk for international travellers. Eur J Clin Microbiol Infect Dis. 2010; 29(12):1501-6. Epub 2010/09/14. doi:10.1007/s10096-010-1031-y PMID: 20835879.
75. Broens EM, Graat EA, van de Giessen AW, Broekhuizen-Stins MJ, de Jong MC. Quantification of transmission of livestock-associated methicillin resistant Staphylococcus aureus in pigs. Vet Microbiol. 2012; 155(2-4):381-8. doi:10.1016/j.vetmic.2011.09.010 PMID: 21963419.
76. 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]. Dtsch Tierarztl Wochenschr. 2008; 115(4):132-9. PMID: 18500146.
77. Moodley A, Guardabassi L. Transmission of IncN plasmids carrying blaCTX-M-1 between commensal Escherichia coli in pigs and farm workers. Antimicrob Agents Chemother. 2009; 53(4):1709-11. doi:10.1128/AAC.01014-08 PMID: 19188380; PubMed Central PMCID: PMCPMC2663060.
78. Carattoli A. Animal reservoirs for extended spectrum beta-lactamase producers. Clin Microbiol Infect. 2008; 14 Suppl 1:117-23. doi:10.1111/j.1469-0691.2007.01851.x PMID: 18154535.
79. Schulz J, Friese A, Klees S., Tenhagen BA, Fetsch A, Rösler U, et al. 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(16):5666-71. doi:10.1128/AEM.00550-12 PMID: 22685139; PubMed Central PMCID: PMCPMC3406131.
80. Agerso Y, Vigre H, Cavaco L.M., Josefsen MH. Comparison of air samples, nasal swabs, ear-skin swabs and environmental dust samples for detection of methicillin-resistant Staphylococcus aureus (MRSA) in pig herds. Epidemiol Infect. 2014; 142(8):1727-36. Epub 2013/11/16. S095026881300280X [pii]. PMID: 24229727.
81. Broens EM, Graat EA, Van der Wolf PJ, Van de Giessen AW, De Jong MC. Transmission of methicillin resistant Staphylococcus aureus among pigs during transportation from farm to abattoir. Vet J. 2011; 189(3):302-5. doi:10.1016/j.tvjl.2010.08.003 PMID: 20850359.
82. Huletsky A, Lebel P, Picard F.J., Bernier M., Gagnon M, Boucher N, et al Identification of methicillin-resistant Staphylococcus aureus carriage in less than 1 hour during a hospital surveillance program. Clin Infect Dis. 2005; 40(7):976-81. doi:10.1086/428579 PMID: 15824989.
83. Tenhagen BA, Fetsch A, Stührenberg B, Schleuter G., Guerra B, Hammerl JA, et al Prevalence of MRSA types in slaughter pigs in different German abattoirs. Vet Rec. 2009; 165(20):589-93. PMID: 19915190.
84. Hurd HS, Gailey JK, McKean J.D., Rostagno MH. Rapid infection in market-weight swine following exposure to a Salmonella typhimurium-contaminated environment. Am J Vet Res. 2001; 62(8):1194-7. PMID: 11497437.
85. Hurd HS, McKean JD, Griffith R.W., Wesley IV, Rostagno MH. Salmonella enterica infections in market swine with and without transport and holding. Appl Environ Microbiol. 2002; 68(5):2376-81. PMID: 11976111; PubMed Central PMCID: PMCPMC127561.
86. Adell E, Moset V, Zhao Y., Jiménez-Belenguer A, Cerisuelo A, Cambra-López M. Comparative performance of three sampling techniques to detect airborne Salmonella species in poultry farms. Ann Agric Environ Med. 2014; 21(1):15-24. PMID: 24742034.
87. Kastrup GN. Prevalence ofmeticillin-resistantStaphylococcusaureusalong the food chain from slaughter to meat processing in the production of raw pork meat: School of Veterinary Medicine Hannover; 2011.
88. Vandendriessche S, Vanderhaeghen W, Soares F.V., Hallin M., Catry B, Hermans K, et al Prevalence, risk factors and genetic diversity of methicillin-resistant Staphylococcus aureus carried by humans and animals across livestock production sectors. J Antimicrob Chemother. 2013; 68(7):1510-6. doi:10.1093/jac/dkt047 PMID: 23429641.
89. Vandendriessche S, Vanderhaeghen W, Larsen J., de Mendonça R, Hallin M, Butaye P, et al. High genetic diversity of methicillin-susceptible Staphylococcus aureus (MSSA) from humans and animals on livestock farms and presence of SCCmec remnant DNA in MSSACC398. J Antimicrob Chemother. 2014; 69(2):355-62. doi:10.1093/jac/dkt366 PMID: 24072172.
90. Harrison EM, Paterson GK, Holden M.T., Larsen J., Stegger M, Larsen AR, et al Whole genome sequencing identifies zoonotic transmission of MRSA isolates with the novel mecA homologue mecC. EMBOMol Med. 2013; 5(4):509-15. doi:10.1002/emmm.201202413 PMID: 23526809; PubMed Central PMCID: PMCPMC3628104.
91. 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). Epub 2012/02/23. doi:10.1128/mBio.00305-11 e00305-11 [pii] mBio.00305-11 [pii]. PMID: 22354957; PubMed Central PMCID: PMC3280451.
92. Köck R., Mellmann A, Schaumburg F., Friedrich AW, Kipp F, Becker K. The epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) in Germany. Dtsch Arztebl Int. 2011; 108(45):761-7. doi:10.3238/arztebl.2011.0761 PMID: 22163252; PubMed Central PMCID: PMCPMC3230165.
93. Anwar MS, Jaffery G, Rehman Bhatti KU, Tayyib M, Bokhari SR. Staphylococcus aureus and MRSA nasal carriage in general population. J Coll Physicians Surg Pak. 2004; 14(11):661-4. doi:11.2004/JCPSp.661664. PMID: 15530274.
94. Gonçalves A., Torres C, Silva N., Carneiro C, Radhouani H, Coelho C., et al. Genetic characterization of extended-spectrum beta-lactamases in Escherichia coli isolates of pigs from a Portuguese intensive swine farm. Foodborne Pathog Dis. 2010; 7(12):1569-73. doi:10.1089/fpd.2010.0598 PMID: 20704503.