Antibiotic resistance in Escherichia coli from pigs in organic and conventional farming in four european countries

PLoS ONE

Volumn 11, Issue 6, 2016, Pages

  Österberg, Julia ^a   Wingstrand, Anne ^b   Jensen, Annette Nygaard ^b   Kerouanton, Annaelle ^c   Cibin, Veronica ^d   Barco, Lisa ^d   Denis, Martine ^c   Aabo, Sören ^b   Bengtsson, Björn ^a  

^a NATIONAL VETERINARY INSTITUTE   (Sweden)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c FRENCH AGENCY FOR FOOD   (France)

^d ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLE VENEZIE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; CEFOTAXIME; CHLORAMPHENICOL; CIPROFLOXACIN; GENTAMICIN; NALIDIXIC ACID; STREPTOMYCIN; SULFONAMIDE; TETRACYCLINE; TRIMETHOPRIM; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM ISOLATE; CONTROLLED STUDY; CONVENTIONAL TILLAGE; DENMARK; ESCHERICHIA COLI; FRANCE; ITALY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; ORGANIC FARMING; PIG; SWEDEN; AGRICULTURE; ANIMAL; DRUG EFFECTS; EUROPE; FECES; ISOLATION AND PURIFICATION; MICROBIOLOGY;

AGRICULTURE; ANIMALS; ANTI-BACTERIAL AGENTS; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; EUROPE; FECES; SWINE;

EID: 84977080440     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0157049     Document Type: Article

References (35)

1. WHO. World Health Organization 2012; The evolving threat of antimicrobial resistance. Available: www.who.int.
2. Baquero F. The 2010 Garrod Lecture: the dimensions of evolution in antibiotic resistance: ex unibus plurum et ex pluribus unum. J Antimicrob Chemother. 2011; 66(8):1659-72. Epub 2011/06/18. doi: 10. 1093/jac/dkr214 dkr214 [pii]. PMID: 21680579.
3. Marshall BM, Levy SB. Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev. 2011; 24(4):718-33. Epub 2011/10/07. doi: 10.1128/CMR.00002-11 24/4/718 [pii]. PMID: 21976606; PubMed Central PMCID: PMC3194830.
4. Verraes C, Van Boxstael S, Van Meervenne E, Van Coillie E, Butaye P, Catry B, et al. Antimicrobial resistance in the food chain: a review. Int J Environ Res Public Health. 2013; 10(7):2643-69. Epub 2013/07/03. doi: 10.3390/ijerph10072643 ijerph10072643 [pii]. PMID: 23812024; PubMed Central PMCID: PMC3734448.
5. Council regulation (EC) No 834/2007of June 2007 on organic production and labelling of organic products and repealing Regulation (ECC) No2092/91.
6. WHO. World Health Organization 2014; Antimicrobial resistance-Global report on surveillance. Available: www.who.int.
7. Tadesse DA, Zhao S, Tong E, Ayers S, Singh A, Bartholomew MJ, et al. Antimicrobial drug resistance in Escherichia coli from humans and food animals, United States, 1950-2002. Emerg Infect Dis. 2012; 18(5):741-9. Epub 2012/04/21. doi: 10.3201/eid1805.111153 PMID: 22515968; PubMed Central PMCID: PMC3358085.
8. EFSA & ECDC. European Food Safety Authority and European Centre for Disease Prevention and Control; The Community Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2012. EFSA Journal. 2014; 12(3):3590-926.
9. EMA. European Medical Products Agency 2014; European Surveillance of Veterinary Antimicrobial Consumption. Sales of veterinary antimicrobial agents in 26 EU/EEA countries in 2012.
10. Chantziaras I, Boyen F, Callens B, Dewulf J. Correlation between veterinary antimicrobial use and antimicrobial resistance in food-producing animals: a report on seven countries. J Antimicrob Chemother. 2014; 69(3):827-34. doi: 10.1093/jac/dkt443 PMID: 24216767.
11. ECDC/EFSA/EMA. European Centre for Disease Prevention and Control, European Food Safety Authorithy and European Medicines Agency; ECDC/EFSA/EMA first joint report on the integrated analysis of the consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals. EFSA Journal. 2015; 13(1):114. doi: 10.2903/j.efsa.2015. 4006
12. Garcia-Migura L, Hendriksen RS, Fraile L, Aarestrup FM. Antimicrobial resistance of zoonotic and commensal bacteria in Europe: the missing link between consumption and resistance in veterinary medicine. Vet Microbiol. 2014; 170(1-2):1-9. Epub 2014/03/05. doi: 10.1016/j.vetmic.2014.01.013 S0378-1135(14)00048-0 [pii]. PMID: 24589430.
13. Call DR, Davis MA, Sawant AA. Antimicrobial resistance in beef and dairy cattle production. Anim Health Res Rev. 2008; 9(2):159-67. doi: 10.1017/S1466252308001515 PMID: 18983724.
14. Jacob ME, Fox JT, Reinstein SL, Nagaraja TG. Antimicrobial susceptibility of foodborne pathogens in organic or natural production systems: an overview. Foodborne Pathog Dis. 2008; 5(6):721-30. doi: 10.1089/fpd.2008.0095 PMID: 18847380.
15. Young I, Rajic A, Wilhelm BJ, Waddell L, Parker S, McEwen SA. Comparison of the prevalence of bacterial enteropathogens, potentially zoonotic bacteria and bacterial resistance to antimicrobials in organic and conventional poultry, swine and beef production: a systematic review and meta-analysis. Epidemiol Infect. 2009; 137(9):1217-32. Epub 2009/04/22. doi: 10.1017/S0950268809002635 S0950268809002635 [pii]. PMID: 19379542.
16. Wu S, Chouliara E, Jensen LB, Dalsgaard A. Evaluation of Petrifilm Select E. coli Count Plate medium to discriminate antimicrobial resistant Escherichia coli. Acta Veterinaria Scandinavica. 2008; 50:38. doi: 10.1186/1751-0147-50-38 PMID: 18817575; PubMed Central PMCID: PMC2564925.
17. CLSI. Clinical and Laboratory Standards Institute; Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animal; Approved standards- Fourth edition,2013. Wayne, Pennsylvania, USA.
18. DANMAP 2009. Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, foods and humans in Denmark. ISSN 1600-2032. Available: http://www.danmap.org.
19. Nulsen MF, Mor MB, Lawton DE. Antibiotic resistance among indicator bacteria isolated from healthy pigs in New Zealand. New Zealand veterinary journal. 2008; 56(1):29-35. doi: 10.1080/00480169. 2008.36801 PMID: 18322557.
20. Sato K, Bartlett PC, Saeed MA. Antimicrobial susceptibility of Escherichia coli isolates from dairy farms using organic versus conventional production methods. J Am Vet Med Assoc. 2005; 226(4):589-94.Epub 2005/03/04. PMID: 15742702.
21. Sato K, Bennedsgaard TW, Bartlett PC, Erskine RJ, Kaneene JB. Comparison of antimicrobial susceptibility of Staphylococcus aureus isolated from bulk tank milk in organic and conventional dairy herds in the midwestern United States and Denmark. J Food Prot. 2004; 67(6):1104-10. PMID: 15222534.
22. Miranda JM, Mondragon A, Vazquez BI, Fente CA, Cepeda A, Franco CM. Influence of farming methods on microbiological contamination and prevalence of resistance to antimicrobial drugs in isolates from beef. Meat Sci. 2009; 82(2):284-8. doi: 10.1016/j.meatsci.2009.01.020 PMID: 20416735.
23. van de Vijver LP, Tulinski P, Bondt N, Mevius D, Verwer C. Prevalence and Molecular Characteristics of Methicillin-Resistant Staphylococcus aureus (MRSA) in Organic Pig Herds in The Netherlands. Zoonoses Public Health. 2013. Epub 2014/04/23. doi: 10.1111/zph.12076 PMID: 24751151.
24. Cuny C, Friedrich AW, Witte W. Absence of livestock-associated methicillin-resistant staphylococcus aureus clonal complex CC398 as a nasal colonizer of pigs raised in an alternative system. Applied and Environmental Microbiology. 2012; 78(4):1296-7. Epub 2011/12/14. doi: 10.1128/AEM.07260-11PMID: 22156420; PubMed Central PMCID: PMC3273000.
25. Gerzova L, Babak V, Sedlar K, Faldynova M, Videnska P, Cejkova D, et al. Characterization of Antibiotic Resistance Gene Abundance and Microbiota Composition in Feces of Organic and Conventional Pigs from Four EU Countries. PLoS One. 2015; 10(7):e0132892. doi: 10.1371/journal.pone.0132892PMID: 26218075; PubMed Central PMCID: PMC4517930.
26. Guarddon M, Miranda JM, Rodriguez JA, Vazquez BI, Cepeda A, Franco CM. Real-time polymerase chain reaction for the quantitative detection of tetA and tetB bacterial tetracycline resistance genes inood. Int J Food Microbiol. 2011; 146(3):284-9. doi: 10.1016/j.ijfoodmicro.2011.02.026 PMID: 21420750.
27. EFSA & ECDC. European Food Safety Authorithy and European Centre for Disease Prevention and Control; The Community Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2011. EFSA Journal. 2013; 11(5):3196-555.
28. EFSA. European Food Safety Authorithy; The Community Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from animals and food in the European Union in 2004-2007. EFSA Journal. 2010; 8(4):1309-604. doi: 10.2903/j.efsa.2010.1309
29. Rosengren LB, Waldner CL, Reid-Smith RJ, Dowling PM, Harding JC. Associations between feed and water antimicrobial use in farrow-to-finish swine herds and antimicrobial resistance of fecal Escherichia coli from grow-finish pigs. Microb Drug Resist. 2007; 13(4):261-69. doi: 10.1089/mdr.2007.781 PMID: 18184052.
30. Maynard C, Fairbrother JM, Bekal S, Sanschagrin F, Levesque RC, Brousseau R, et al. Antimicrobial resistance genes in enterotoxigenic Escherichia coli O149:K91 isolates obtained over a 23-year period from pigs. Antimicrob Agents Chemother. 2003; 47(10):3214-21. PMID: 14506033; PubMed Central PMCID: PMC201132.
31. Bondt N, Jensen VF, Puister-Jansen LF, van Geijlswijk IM. Comparing antimicrobial exposure based on sales data. Prev Vet Med. 2013; 108(1):10-20. Epub 2012/08/18. doi: 10.1016/j.prevetmed.2012. 07.009 S0167-5877(12)00234-6 [pii]. PMID: 22897857.
32. Laanen M, Persoons D, Ribbens S, de Jong E, Callens B, Strubbe M, et al. Relationship between biosecurity and production/antimicrobial treatment characteristics in pig herds. Vet J. 2013; 198(2):508-12. doi: 10.1016/j.tvjl.2013.08.029 PMID: 24268483.
33. Alvarez-Ordonez A, Martinez-Lobo FJ, Arguello H, Carvajal A, Rubio P. Swine dysentery: aetiology, pathogenicity, determinants of transmission and the fight against the disease. Int J Environ Res Public Health. 2013; 10(5):1927-47. doi: 10.3390/ijerph10051927 PMID: 23665849; PubMed Central PMCID: PMC3709357.
34. Tobias TJ, Bouma A, van den Broek J, van Nes A, Daemen AJ, Wagenaar JA, et al. Transmission of Actinobacillus pleuropneumoniae among weaned piglets on endemically infected farms. Prev Vet Med. 2014; 117(1):207-14. doi: 10.1016/j.prevetmed.2014.07.017 PMID: 25156946.
35. Liebana E, Carattoli A, Coque TM, Hasman H, Magiorakos AP, Mevius D, et al. Public health risks of enterobacterial isolates producing extended-spectrum beta-lactamases or AmpC beta-lactamases in food and food-producing animals: an EU perspective of epidemiology, analytical methods, risk factors, and control options. Clin Infect Dis. 2013; 56(7):1030-7. doi: 10.1093/cid/cis1043 PMID: 23243183.