The dissemination of drug-resistant bacteria from animal farms to aquatic environments can pose a potential threat to public health. In this study, antimicrobial resistance, resistance genes, and genetic similarity of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli of different origins (chicken feces and upstream and downstream river waters) were analyzed to track the spread of drug-resistant bacteria of animals. The results showed that a total of 29 ESBL-producing E. coli were obtained from 258 samples, and isolation rates of the ESBL-producing E. coli from chicken feces and upstream and downstream waters were 10.7% (16/150), 3.7% (1/27), and 14.8% (12/81), respectively. The ESBL-producing E. coli from upstream water was resistant to 7 antibiotics, but isolates from feces and downstream water had a higher resistance rate. In 29 ESBL-producing E. coli, the most common gene was CTX-M and the SHV gene was not detected. Five ESBL-producing isolates from downstream water showed >90% similarity with the fecal isolates, while the only one isolate from upstream water had <70% similarity with fecal isolates. The results suggest that animal farms' effluent, especially the untreated wastewater, could contribute to the spread of resistance genes.

1.
Baquero F, Martínez JL, Canton R: Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 2008;19:260-265.
[PubMed]
2.
Blanc V, Mesa R, Saco M, Lavilla S, Prats G, Miro E, Navarro F, Cortes P, Llagostera M: ESBL- and plasmidic class C β-lactamase-producing E. coli strains isolated from chicken, pig and rabbit farms. Vet Microbiol 2006;118:299-304.
[PubMed]
3.
Bradford PA: Extended-spectrum β-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin Microbiol Rev 2001;14:933-951.
[PubMed]
4.
Briñas L, Moreno MA, Zarazaga M, Porrero C, Sáenz Y, Garcia M, Sominguez L, Torres C: Detection of CMY-2, CTX-M-14, and SHV-12 β-lactamases in Escherichia coli fecal-sample isolates from healthy chickens. Antimicrob Agents Chemother 2003;47:2056-2058.
[PubMed]
5.
Canton R, Novais A, Valverde A, Machado E, Peixe L, Baquero F, Coque TM: Prevalence and spread of extended-spectrum β-lactamase-producing Enterobacteriaceae in Europe. Clin Microbiol Infect 2008;14:144-153.
[PubMed]
6.
Cheng D, Sun H, Xu J, Gao S: PCR detection of virulence factor genes in Escherichia coli isolates from weaned piglets with edema disease and/or diarrhea in China. Vet Microbiol 2006;115:320-328.
[PubMed]
7.
Clinical and Laboratory Standards Institute: Performance standards for antimicrobial susceptibility testing. 18th Informational Supplement, 2008; document M100-S18.
8.
Coque TM, Novais A, Carattoli A, Poirel L, Pitout J, Peixe L, Baquero F, Canton R, Nordmann P: Dissemination of clonally related Escherichia coli strains expressing extended-spectrum β-lactamase CTX-M-15. Emerg Infect Dis 2008;14:195-200.
[PubMed]
9.
Costa D, Vinué L, Poeta P, Coelho AC, Matos M, Sáenz Y, Somalo S, Zarazaga M, Rodrigues J, Torres C: Prevalence of extended-spectrum β-lactamase-producing Escherichia coli isolates in faecal samples of broilers. Vet Microbiol 2009;138:339-344.
[PubMed]
10.
De Boeck H, Lunguya O, Muyembe JJ, Glupczynski Y, Jacobs J: Presence of extended-spectrum β-lactamase-producing Enterobacteriaceae in waste waters, Kinshasa, the Democratic Republic of the Congo. Eur J Clin Microbiol Infect Dis 2012;31:3085-3088.
[PubMed]
11.
Dos Anjos Borges LG, Dalla Vechia V, Corção G: Characterisation and genetic diversity via REP-PCR of Escherichia coli isolates from polluted waters in southern Brazil. FEMS Microbiol Ecol 2006;45:173-180.
[PubMed]
12.
Edge TA, Hill S: Occurrence of antibiotic resistance in Escherichia coli from surface waters and fecal pollution sources near Hamilton, Ontario. Can J Microbiol 2005;5:501-505.
[PubMed]
13.
Eisner A, Fagan EJ, Feierl G, Kessler HH, Marth E, Livermore DM, Woodford N: Emergence of Enterobacteriaceae isolates producing CTX-M extended-spectrum β-lactamase in Austria. Antimicrob Agents Chemother 2006;50:785-787.
[PubMed]
14.
Falagas ME, Karageorgopoulos DE: Extended-spectrum β-lactamase-producing organisms. J Hosp Infect 2009;73:345-354.
[PubMed]
15.
Fendri I, Ben Hassena A, Grosset N, Barkallah M, Khannous L, Chuat V, Gautier M, Gdoura R: Genetic diversity of food-isolated Salmonella strains through pulsed field gel electrophoresis and Enterobacterial Repetitive Intergenic Consensus (ERIC-PCR). PLoS One 2013;8:e81315.
[PubMed]
16.
Forward KR, Matheson KM, Hiltz M, Musgrave H, Poppe C: Recovery of cephalosporin-resistant Escherichia coli and Salmonella from pork, beef and chicken marketed in Nova Scotia. Can J Infect Dis Med Microbiol 2004;15:226-230.
[PubMed]
17.
Glupczynski Y, Bogaerts P, Deplano A, Berhin C, Huang TD, Van Eldere J, Rodriguez-Villalobos H: Detection and characterization of class A extended-spectrum β-lactamase-producing Pseudomonas aeruginosa isolates in Belgian hospitals. J Antimicrob Chemother 2010;65:866-871.
[PubMed]
18.
Ho PL, Chow KH, Lai EL, Lo WU, Yeung MK, Chan J, Chan PY, Yuen KY: Extensive dissemination of CTX-M-producing Escherichia coli with multidrug resistance to ‘critically important' antibiotics among food animals in Hong Kong, 2008-10. J Antimicrob Chemother 2011;66:765-768.
[PubMed]
19.
Hu YY, Cai JC, Zhou HW, Chi D, Zhang XF, Chen WL, Zhang R, Chen GX: 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;79:5988-5996.
[PubMed]
20.
Jang J, Suh YS, Di DY, Unno T, Sadowsky MJ, Hur HG: Pathogenic Escherichia coli strains producing extended-spectrum β-lactamases in the Yeongsan River basin of South Korea. Environ Sci Technol 2013;47:1128-1136.
[PubMed]
21.
Kiratisin P, Apisarnthanarak A, Laesripa C, Saifon P: Molecular characterization and epidemiology of extended-spectrum-β-lactamase-producing Escherichia coli and Klebsiella pneumoniae isolates causing healthcare-associated infection in Thailand, where the CTX-M family is endemic. Antimicrob Agents Chemother 2008;52:2818-2824.
[PubMed]
22.
Kluytmans JA, Overdevest IT, Willemsen I, Kluytmans-van den Bergh MF, van der Zwaluw K, Heck M, Rijnsburger M, Vandenbroucke-Grauls CM, Savelkoul PH, Johnston BD, Gordon D, Johnson JR: Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans: comparison of strains, plasmids, resistance genes, and virulence factors. Clin Infect Dis 2013;56:478-487.
[PubMed]
23.
Knothe H, Shah P, Kremery V, Antal M, Mitsuhashi S: Transferable resistance to cefotaxime, cefoxitin, cefamandole and cefuroxime in clinical isolates of Klebsiella pneumoniae and Serratia marcescens. Infection 1983;11:315-317.
[PubMed]
24.
Koczura R, Kaznowski A: The Yersinia high-pathogenicity island and iron-uptake systems in clinical isolates of Escherichia coli. J Med Microbiol 2003;52:637-642.
[PubMed]
25.
Kumar R, Surendran PK, Thampuran N: Distribution and genotypic characterization of Salmonella serovars isolated from tropical seafood of Cochin, India. J Appl Microbiol 2009;106:515-524.
[PubMed]
26.
Kummerer K: Antibiotics in the aquatic environment - a review. Part I. Chemosphere 2009;75:347-354.
[PubMed]
27.
Leverstein-van Hall MA, Dierikx CM, Cohen Stuart J, Voets GM, van den Munckhof MP, van Essen-Zandbergen A, Platteel T, Fluit AC, van de Sande-Bruinsma N, Scharinga J, Bonten MJ, Mevius DJ; National ESBL surveillance group: Dutch patients, retail chicken meat and chicken share the same ESBL genes, plasmids and strains. Clin Microbiol Infect 2011;17:873-880.
[PubMed]
28.
Li S, Zhao MQ, Li YL, Zhang L, Zhang XZ, Miao ZM: Detection and source identi&#xFB01;cation of airborne extended-spectrum β-lactamase-producing Escherichia coli isolates in a chicken house. Aerobiologia 2013;29:315-319.
29.
Machado E, Coque TM, Cantón R, Sousa JC, Peixe L: Antibiotic resistance integrons and extended-spectrum β-lactamases among Enterobacteriaceae isolates recovered from chickens and swine in Portugal. J Antimicrob Chemother 2008;62:296-302.
[PubMed]
30.
Meacham KJ, Zhang L, Foxman B, Bauer RJ, Marrs CF: Evaluation of genotyping large numbers of Escherichia coli isolates by enterobacterial repetitive intergenic consensus-PCR. J Clin Microbiol 2003;41:5224-5226.
[PubMed]
31.
Mesa RJ, Blanc V, Blanch AR, Cortés P, González JJ, Lavilla S, Miró E, Muniesa M, Saco M, Tórtola MT, Mirelis B, Coll P, Llagostera M, Prats G, Navarro F: Extended-spectrum β-lactamase-producing Enterobacteriaceae in different environments (humans, food, animal farms and sewage). J Antimicrob Chemother 2006;58:211-215.
[PubMed]
32.
Meunier D, Jouy E, Lazizzera C, Kobisch M, Madec JY: CTX-M-1- and CTX-M-15-type β-lactamases in clinical Escherichia coli isolates recovered from food-producing animals in France. Int J Antimicrob Agents 2006;28:402-407.
[PubMed]
33.
Meyer E, Schwab F, Schroeren-Boersch B, Gastmeier P: Dramatic increase of third-generation cephalosporin-resistant Escherichia coli in German intensive care units: secular trends in antibiotic drug use and bacterial resistance, 2001-2008. Crit Care 2010;14:R113.
[PubMed]
34.
Paterson DL, Bonomo RA: Extended-spectrum β-lactamases: a clinical update. Clin Microbiol Rev 2005;18:657-686.
[PubMed]
35.
Paterson DL, Hujer KM, Hujer AM, Yeiser B, Bonomo MD, Rice LB, Bonomo RA; International Klebsiella Study Group: Extended-spectrum β-lactamases in Klebsiella pneumoniae bloodstream isolates from seven countries: dominance and widespread prevalence of SHV-and CTX-M-type β-lactamases. Antimicrob Agents Chemother 2003;47:3553-3560.
[PubMed]
36.
Pereira A, Santos A, Tacão M, Alves A, Henriques I, Correia A: Genetic diversity and antimicrobial resistance of Escherichia coli from Tagus estuary (Portugal). Sci Total Environ 2013;461-462:65-71.
[PubMed]
37.
Reinthaler FF, Feierl G, Galler H, Haas D, Leitner E, Mascher F, Melkes A, Posch J, Winter I, Zarfel G, Marth E: ESBL-producing E. coli in Austrian sewage sludge. Water Res 2010;44:1981-1985.
[PubMed]
38.
Servais P, Passerat J: Antimicrobial resistance of fecal bacteria in waters of the Seine river watershed (France). Sci Total Environ 2009;408:365-372.
[PubMed]
39.
Smet A, Martel A, Persoons D, Dewulf J, Heyndrickx M, Catry B, Herman L, Haesebrouck F, Butaye P: Diversity of extended-spectrum β-lactamases and class C β-lactamases among cloacal Escherichia coli Isolates in Belgian broiler farms. Antimicrob Agents Chemother 2008;52:1238-1243.
[PubMed]
40.
Tian GB, Wang HN, Zou LK, Tang JN, Zhao YW, Ye MY, Tang JY, Zhang Y, Zhang AY, Yang X, Xu CW, Fu YJ: Detection of CTX-M-15, CTX-M-22, and SHV-2 extended-spectrum β-lactamases (ESBLs) in Escherichia coli fecal-sample isolates from pig farms in China. Foodborne Pathog Dis 2009;6:297-304.
[PubMed]
41.
Versalovic J, Koeuth T, Lupski JR: Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 1991;19:6823-6831.
[PubMed]
42.
Wang Y, He T, Han J, Wang J, Foley SL, Yang G, Wan S, Shen J, Wu C: Prevalence of ESBLs and PMQR genes in fecal Escherichia coli isolated from the non-human primates in six zoos in China. Vet Microbiol 2012;14:53-59.
[PubMed]
43.
Wegener HC: Antibiotics in animal feed and their role in resistance development. Curr Opin Microbiol 2003;6:439-445.
[PubMed]
44.
Woodford N, Carattoli A, Karisik E, Underwood A, Ellington MJ, Livermore DM: Complete nucleotide sequences of plasmids pEK204, pEK499, and pEK516, encoding CTX-M enzymes in three major Escherichia coli lineages from the United Kingdom, all belonging to the international O25:H4-ST131 clone. Antimicrob Agents Chemother 2009;53:4472-4482.
[PubMed]
45.
Yuan L, Liu JH, Hu GZ, Pan YS, Liu ZM, Mo J, Wei YJ: Molecular characterization of extended-spectrum β-lactamase-producing Escherichia coli isolates from chickens in Henan Province of China. J Med Microbiol 2009;58:1449-1453.
[PubMed]
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