Vertical transmission of highly similar blaCTX-M-1-harbouring IncI1 plasmids in Escherichia coli with different MLST types in the poultry production pyramid

Frontiers in Microbiology

Volumn 5, Issue SEP, 2014, Pages

  Zurfluh, Katrin ^a   Wang, Juan ^b   Klumpp, Jochen ^c   Nüesch Inderbinen, Magdalena ^a   Fanning, Séamus ^b   Stephan, Roger ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

^c ETH ZURICH   (Switzerland)

Author keywords

Conjugation; CTX M 1; E. coli; IncI1; Plasmid sequencing; Poultry production pyramid

Indexed keywords

BETA LACTAM ANTIBIOTIC; BETA LACTAMASE; EXTENDED SPECTRUM BETA LACTAMASE; NALIDIXIC ACID; SULFAMETHOXAZOLE; TETRACYCLINE; TRIMETHOPRIM;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIUM CONJUGATION; BIOINFORMATICS; BLA GENE; BROILER; ENTEROBACTERIACEAE; ESCHERICHIA COLI; EXTENDED SPECTRUM BETA LACTAMASE PRODUCING ENTEROBACTERIACEAE; GENE; GENE IDENTIFICATION; GENE SEQUENCE; GENOTYPE; MECONIUM; MULTILOCUS SEQUENCE TYPING; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; PLASMID; POLYMERASE CHAIN REACTION; REPLICON TYPING;

ESCHERICHIA COLI;

EID: 84907700532     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00519     Document Type: Article

References (39)

1. Abgottspon, H., Stephan, R., Bagutti, C., Brodmann, P., Hächler, H., and Zurfluh, K. (2014). Characteristics of extended-spectrum cephalosporin-resistant Escherichia coli isolated from Swiss and imported poultry meat. J. Food Prot. 77, 112-5. doi:10.4315/0362-028X.JFP-13-120.
2. Agersø, Y., Jensen, J. D., Hasman, H., and Pedersen, K. (2014). Spread of extended spectrum cephalosporinase-producing Escherichia coli clones and plasmids from parent animals to broilers and to broiler meat in a production without use of cephalosporins. Foodborne Pathog. Dis. 0, 1-7. doi:10.1089/fpd.2014.1742.
3. Aziz, R. K., Bartels, D., Best, A., DeJongh, M., Disz, T., Edwards, R., Formsma, K., Gerdes, S., Glass, E. M., Kubal, M., et al. (2008). The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9, 75. doi:10.1186/1471-2164-9-75.
4. Bush K., and Jacoby G.A. (2010). Updated functional classification of beta lactamases. Antimicrob. Agent. Chemother. 54, 969-976.
5. Büttner S., Flurina S., Müntener C., Jäggi M., and Overesch, G. Report on the sales of antibiotics for veterinary use and antibiotic resistance monitoring of livestock in Switzerland. Bern: Federal Veterinary Office, 2013.
6. Carattoli A. (2009). Resistance plasmid families in Enterobacteriaceae. Antimicrob. Agents Chemother. 53, 2227-2238.
7. Carattoli, A., Bertini, A., Villa, L., Falbo, V., Hopkins, K. L., and Threlfall, E. J. (2005). Identification of plasmids by PCR-based replicon typing. J. Microbiol. Methods 63, 219-228. doi:10.1016/j.mimet.2005.03.018.
8. Clermont, O., Bonacorsi, S., and Bingen, E. (2000). Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Env. Microbiol 66, 4555-4558. Available at: http://www.ncbi.nlm.nih.gov/pubmed/11010916.
9. CLSI (2011). Performance Standards for Antimicrobial Susceptibility Testing; Twenty-First Informational Supplement. Vol.31 No1 ed. Wayne PA: Clinical and Laboratory Standards Institute.
10. Cortés, P., Blanc, V., Mora, A., Dahbi, G., Blanco, J. E., Blanco, M., López, C., Andreu, A., Navarro, F., Alonso, M. P., et al. (2010). Isolation and characterization of potentially pathogenic antimicrobial-resistant Escherichia coli strains from chicken and pig farms in Spain. Appl. Environ. Microbiol. 76, 2799-805. doi:10.1128/AEM.02421-09.
11. Dahmen, S., Haenni, M., and Madec, J. (2012). IncI1/ST3 plasmids contribute to the dissemination of the blaCTX-M-1 gene in Escherichia coli from several animal species in France. J. Antimicrob. Chemother., 3011-3012. doi:10.1093/jac/dks308.
12. Dierikx, C. M., van der Goot, J. a., Smith, H. E., Kant, A., and Mevius, D. J. (2013). Presence of ESBL/AmpC -producing Escherichia coli in the broiler production pyramid: A descriptive study. PLoS One 8, e79005. doi:10.1371/journal.pone.0079005.
13. EFSA Panel on Biological Hazards. Scientific Opinion on the public health risks of bacterial strains producing extended-spectrum β-lactamases and/or AmpC β-lactamases in food and food-producing animals. EFSA Journal 2011;9(8):2322. doi:10.2903/j.efsa.2011.2322.
14. Endimiani, A., Rossano, A., Kunz, D., Overesch, G., and Perreten, V. (2012). First countrywide survey of third-generation cephalosporin-resistant Escherichia coli from broilers, swine, and cattle in Switzerland. Diagn. Microbiol. Infect. Dis. 73, 31-8. doi:10.1016/j.diagmicrobio.2012.01.004.
15. Fischer, E. J., Dierikx, C. M., van Essen-Zandbergen, A., van Roermund, H. J. W., Mevius, D. J., Stegeman, A., and Klinkenberg, D. (2014). The IncI1 plasmid carrying the blaCTX-M-1 gene persists in in vitro culture of a Escherichia coli strain from broilers. BMC Microbiol. 14, 77. doi:10.1186/1471-2180-14-77.
16. Frère, J. M., Nguyen-Diste' che, M., Coyette, J. and Joris, B. (1992) in The Chemistry of β-Lactams (Page, M. I., ed.), pp. 148-197, Blackie, London.
17. García-Fernández A., Chiaretto G., Bertini A., Villa L., Fortini D., Ricci A., and Carattoli A. (2008). Multilocus sequence typing of IncI1 plasmids carrying extended spectrum beta-lactamases in Escherichia coli and Salmonella of human and animal origin. J. Antimicrob. Chemother. 61, 1229-1233.
18. Geser, N., Stephan, R., and Hächler, H. (2012). Occurrence and characteristics of extended- spectrum b-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Vet. Res. 7;8:21. doi: 10.1186/1746-6148-8-21.
19. Kayser, F. H., Morenzoni, G., and Homberger, F. (1982). Activity of cefoperazone against ampicillin-resistant bacteria in agar and broth dilution tests. Antimicrob. Agents Chemother. 22, 15-22. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=183666&tool=pmcentrez&r endertype=abstract.
20. Kim, S. R., Komano, T. (1997). The plasmid R64 thin pilus identified as a type IV pilus. J. Bacteriol. 179, 3594-3603.
21. Kola, A., Kohler, C., Pfeifer, Y., Schwab, F., Kühn, K., Schulz, K., Balau, V., Breitbach, K., Bast, A., Witte, W., et al. (2012). High prevalence of extended spectrum-β-lactamase-producing Enterobacteriaceae in organic and conventional retail chicken meat, Germany. J. Antimicrob. Chemother. 67, 2631-4. doi:10.1093/jac/dks295.
22. Leverstein-van Hall, M. A., Dierikx, C. M., Cohen Stuart, J., Voets, G. M., van den Munckhof, M. P., van Essen-Zandbergen, a, Platteel, T., Fluit, a C., van de Sande-Bruinsma, N., Scharinga, J., et al. (2011). Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin. Microbiol. Infect. 17, 873-80. doi:10.1111/j.1469-0691.2011.03497.x.
23. Naseer U., and Sundsfjord A. (2011). The CTX-M conundrum: dissemination of plasmids and Escherichia coli clones. Microb. Drug. Resist. 17, 83-97.
24. Nilsson, O., Börjesson, S., Landén, A., and Bengtsson, B. (2014). Vertical transmission of Escherichia coli carrying plasmid-mediated AmpC (pAmpC) through the broiler production pyramid. J. Antimicrob. Chemother. 69, 1497-500. doi:10.1093/jac/dku030.
25. Overdevest, I., Willemsen, I., Rijnsburger, M., Eustace, A., Xu, L., Hawkey, P., Heck, M., Savelkoul, P., Vandenbroucke-Grauls, C., van der Zwaluw, K., et al. (2011). Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands. Emerg. Infect. Dis. 17, 1216-22. doi:10.3201/eid1707.110209.
26. Perry, K. L., Elledge, S. J., Mitchell, B. B., Marsh, L., and Walker, G. C. (1985). umuDC and mucAB operons whose products are required for UV light- and chemical induced mutagenesis: UmuD, MucA, and LexA proteins share homology. Proc. Natl. Acad. Sci. U. S. A. 4, 1054-8.
27. Pitout, J. D. D., Thomson, K. S., Hanson, N. D., Ehrhardt, A. F., Moland, E. S., and Sanders, C. C. (1998). Beta-lactamases responsible for resistance to expanded spectrum cephalosporins in Klebsiella pneumoniae, Escherichia coli, and Proteus mirabilis isolates recovered in South Africa. Antimicrob. Agents Chemother. 42, 1350-1354.
28. Rådström, P., and Swedberg, G. (1988). RSF1010 and a conjugative plasmid contain sulII, one of two known genes for plasmid-borne sulfonamide resistance dihydropteroate synthase. Antimicrob. Agents Chemother. 32, 1684-92.
29. Randall, L. P., Clouting, C., Horton, R. A, Coldham, N. G., Wu, G., Clifton-Hadley, F. A, Davies, R. H., and Teale, C. J. (2011). Prevalence of Escherichia coli carrying extended-spectrum β-lactamases (CTX-M and TEM-52) from broiler chickens and turkeys in Great Britain between 2006 and 2009. J. Antimicrob. Chemother. 66, 86- 95. doi:10.1093/jac/dkq396.
30. Sambrook J., and Russel D. W. (2006). The Condensed Protocols from Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
31. Sampei, G., Furuya, N., Tachibana, K., Saitou, Y., Suzuki, T., Mizobuchi, K., and Komano, T. (2010). Complete genome sequence of the incompatibility group I1 plasmid R64. Plasmid 64, 92-103.
32. Smet, A., Martel, A., Persoons, D., Dewulf, J., Heyndrickx, M., Catry, B., Herman, L., Haesebrouck, F., and Butaye, P. (2008). Diversity of extended-spectrum beta lactamases and class C beta-lactamases among cloacal Escherichia coli isolates in Belgian broiler farms. Antimicrob. Agents Chemother. 52, 1238-43. doi:10.1128/AAC.01285-07.
33. Villa, L., García-Fernández, A., Fortini, D., and Carattoli, A. (2010). Replicon sequence typing of IncF plasmids carrying virulence and resistance determinants. J. Antimicrob. Chemother. 65, 2518-29. doi:10.1093/jac/dkq347.
34. Voets, G. M., Fluit, A. C., Scharringa, J., Schapendonk, C., van den Munckhof, T., Leverstein-van Hall, M. a, and Stuart, J. C. (2013). Identical plasmid AmpC beta lactamase genes and plasmid types in E. coli isolates from patients and poultry meat in the Netherlands. Int. J. Food Microbiol. 167, 359-62. doi:10.1016/j.ijfoodmicro.2013.10.001.
35. Vogt, D., Overesch, G., Endimiani, A., Collaud, A., Thomann, A., and Perreten, V. (2014). Occurrence and genetic characteristics of third-generation cephalosporin resistant Escherichia coli in Swiss retail meat. Microb. Drug Resist. in press.. doi:10.1089/mdr.2013.0210.
36. Wang, J., Stephan, R., Power, K., Yan, Q., Hächler, H., and Fanning, S. (2014). Nucleotide sequences of 16 transmissible plasmids identified in nine multidrug resistant Escherichia coli isolates expressing an ESBL phenotype isolated from food producing animals and healthy humans. J. Antimicrob. Chemother. in press. doi:10.1093/jac/dku206.
37. Wasyl, D., Hasman, H., Cavaco, L. M., and Aarestrup, F. M. (2012). Prevalence and characterization of cephalosporin resistance in nonpathogenic Escherichia coli from food-producing animals slaughtered in Poland. Microb. Drug Resist. 18, 79-82. doi:10.1089/mdr.2011.0033.
38. White, P.A., McIver, C.J., Deng, Y., and Rawlinson, W.D. (2000). Characterisation of two new gene cassettes, aadA5 and dfrA17. FEMS Microbiol. Lett. 182, 265-9.
39. Wirth, T., Falush, D., Lan, R., Colles, F., Mensa, P., Wieler, L. H., Karch, H., Reeves, P. R., Maiden, M. C. J., Ochman, H., et al. (2006). Sex and virulence in Escherichia coli: an evolutionary perspective. Mol. Microbiol. 60, 1136-1151. doi:10.1111/j.1365-2958.2006.05172.x.