1. bookVolume 66 (2016): Issue 4 (December 2016)
Journal Details
License
Format
Journal
eISSN
1820-7448
First Published
25 Mar 2014
Publication timeframe
4 times per year
Languages
English
access type Open Access

Molecular Characterization of ESBL-Producing Escherichia Coli Isolated from Healthy Cattle and Sheep

Published Online: 30 Dec 2016
Volume & Issue: Volume 66 (2016) - Issue 4 (December 2016)
Page range: 520 - 533
Received: 28 Mar 2016
Accepted: 26 Sep 2016
Journal Details
License
Format
Journal
eISSN
1820-7448
First Published
25 Mar 2014
Publication timeframe
4 times per year
Languages
English
Abstract

The present study aims to characterize ESBL-producing Escherichia coli isolated from healthy cattle and sheep in the Burdur province of Turkey. Fecal samples from a total of 200 cattle and 200 sheep were tested and ESBL-producing E. coli was isolated from 31 (15.5%) cattle and three (1.5%) sheep samples using the Clinical and Laboratory Standards Institute’s combined disk method. Among the ESBL gene classes detected by PCR, blaCTX-M was the most frequent type, followed by the blaTEM and blaSHV families. ESBL-producing E. coli isolates showed co-resistance to multiple classes of antibiotics including aminoglycosides, phenicols, quinolones, folate pathway inhibitors and tetracyclines. The resistance rates were higher in the cattle isolates than in the sheep isolates. Phylogenetic grouping of the E. coli isolates indicated group A (particularly A1) was the predominant phylogenetic group (19/34, 55.9%), followed by groups B1 (9/34, 26.5%) and D (6/34, 17.6%); none of the isolates belonged to group B2. The study shows that ESBL-producing E. coli isolates exist in the intestinal flora of healthy cattle and sheep in the Burdur province of Turkey. This is the first report showing the emergence of CTX-M type ESBL-producing E. coli in sheep farms in Turkey

Keywords

1. Paterson DL, Bonomo RA: Extended-spectrum beta-lactamases: a clinical update. Clin Microbiol Rev 2005, 18:657-686.10.1128/CMR.18.4.657-686.2005Search in Google Scholar

2. Perez F, Endimiani A, Hujer KM, Bonomo RA: The continuing challenge of ESBLs. Curr Opin Pharmacol 2007, 7:459-469.10.1016/j.coph.2007.08.003Search in Google Scholar

3. Pitout JD, Laupland KB: Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 2008, 8:159-166.10.1016/S1473-3099(08)70041-0Search in Google Scholar

4. Rossolini GM, Mantengoli E: Antimicrobial resistance in Europe and its potential impact on empirical therapy. Clin. Microbiol Infect 2008, 14 Suppl 6:2-8.10.1111/j.1469-0691.2008.02126.x19040461Search in Google Scholar

5. Livermore DM: Current epidemiology and growing resistance of gram-negative pathogens. Korean J Intern Med 2012, 27:128-142.10.3904/kjim.2012.27.2.128337279422707882Search in Google Scholar

6. Rossolini GM, D’Andrea MM, Mugnaioli C: The spread of CTX-M-type extendedspectrum beta-lactamases. Clin Microbiol Infect 2008, 14 Suppl 1:33-41.10.1111/j.1469-0691.2007.01867.x18154526Search in Google Scholar

7. Bonnet R: Growing group of extended-spectrum beta-lactamases: The CTX-M enzymes. Antimicrob Agents Chemother 2004, 48:1-14.10.1128/AAC.48.1.1-14.200431018714693512Search in Google Scholar

8. Ben Sallem R, Ben Slama K, Sáenz Y, Rojo-Bezares B,Estepa V, Jouini A, Gharsa H, Klibi N, Boudabous A, Torres C: Prevalence and characterization of extended-spectrum beta-lactamase (ESBL)- and CMY-2-producing Escherichia coli isolates from healthy foodproducing animals in Tunisia. Foodborne Pathog Dis 2012, 9:1137-1142.10.1089/fpd.2012.126723194332Search in Google Scholar

9. Duan RS, SitTH, Wong SS, Wong RC,Chow KH, Mak GC, Yam WC, Ng LT, Yuen KY, Ho PL:Escherichia coli producing CTX-M beta-lactamases in food animals in Hong Kong. Microb Drug Resist 2006,12:145-148.10.1089/mdr.2006.12.14516922633Search in Google Scholar

10. 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: 175-180.Search in Google Scholar

11. Geser N, Stephan R, Hächler H: Occurrence and characteristics of extendedspectrum beta-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Vet Res 2012, 8:21.10.1186/1746-6148-8-21331942322397509Search in Google Scholar

12. Hiroi M, Yamazaki F, Harada T, Takahashi N, Iida N, Noda Y, Yagi M, Nishio T, Kanda T, Kawamori F, Sugiyama K, Masuda T, Hara-Kudo Y, Ohashi N: Prevalence of extendedspectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in foodproducing animals. J Vet Med Sci 2012, 74:189-195.10.1292/jvms.11-037221979457Search in Google Scholar

13. Aksoy A, Yildirim M, Kacmaz B, Apan TZ, Gocmen JS: Verotoxin production in strains of Escherichia coli isolated from cattle and sheep and their resistance to antibiotics. Turk J Vet Anim Sci 2007, 31:225-231.Search in Google Scholar

14. Dinc G, Ata Z, Temelli S: Investigation of extended-spectrum beta-lactamase activity and antibiotic resistance profile of Escherichia coli strains isolated from bovine mastitis. Ankara Univ Vet Fak Derg 2012, 59:85-88.Search in Google Scholar

15. Kucukbasmaci O, Ciftcioglu G,Midilli K, Issa G: Detection of extended spectrum betalactamase producing Enterobacteriaceae from food animals in Turkey. Revue Méd Vét 2008, 159:586-592.Search in Google Scholar

16. Canton R, Gonzalez-Alba JM, Galan JC: CTX-M-Enzymes: Origin and Diffusion. Front Microbiol 2012, 3:110.10.3389/fmicb.2012.00110331699322485109Search in Google Scholar

17. Winn, W, Allen S, Janda W, Koneman E, Procop G, Schreckenberger P, and Woods G: The Enterobactericeae. In: Koneman’s Color Atlas and Textbook of Diagnostic Microbiology. Sixth Edition, Lippincott Williams and Wilkins, Philadelphia, USA; 2006, 211-302.Search in Google Scholar

18. Wang G, Clark CG, Rodgers FG: Detection in Escherichia coli of the genes encoding the major virulence factors, the genes defining the O157:H7 serotype, and components of the type 2 shiga toxin family by multiplex PCR. J Clin Microbiol 2002, 40:3613-3619.10.1128/JCM.40.10.3613-3619.200213088812354854Search in Google Scholar

19. CLSI (Clinical and Laboratory Standards Institute): Performance standards for antimicrobial susceptibility testing, 26th edition, CLSI document M100S, Wayne, Pennsylvania, USA; 2016.Search in Google Scholar

20. CLSI (Clinical and Laboratory Standards Institute): Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals, approved standard, 3rd edition, CLSI document M31-A3, Wayne, Pennsylvania, USA; 2010.Search in Google Scholar

21. CLSI (Clinical and Laboratory Standards Institute): Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals, 2nd informational supplement, CLSI document VET01-S2, Wayne, Pennsylvania, USA; 2013.Search in Google Scholar

22. Arpin C, Dubois V, Coulange L, Andre C, Fischer I, Noury P, Grobost F, Brochet JP, Jullin J, Dutilh B, Larribet G, Lagrange I, Quentin C: Extended-spectrum beta-lactamaseproducing Enterobacteriaceae in community and private health care centers. Antimicrob Agents Chemother 2003, 47:3506-3514.10.1128/AAC.47.11.3506-3514.200325377614576109Search in Google Scholar

23. Costa D, Poeta P, Saenz Y, Vinue L, Rojo-Bezares B, Jouini A, Zarazaga M, Rodrigues J, Torres C: Detection of Escherichia coli harbouring extended-spectrum beta-lactamases of the CTX-M, TEM and SHV classes in faecal samples of wild animals in Portugal. J Antimicrob Chemother 2006, 58:1311-1312.10.1093/jac/dkl41517023496Search in Google Scholar

24. Heffernan HM, Woodhouse RE, Pope CE, Blackmore TK: Prevalence and types of extended-spectrum beta-lactamases among urinary Escherichia coli and Klebsiella spp. in New Zealand. Int J Antimicrob Agents 2009, 34:544-549.10.1016/j.ijantimicag.2009.07.01419748232Search in Google Scholar

25. Jeong SH, Bae IK, Kwon SB, Lee JH, Song JS, Jung HI, Sung KH, Jang SJ, Lee SH: Dissemination of transferable CTX-M-type extended-spectrum beta-lactamase-producing E. coli in Korea. J Appl Microbiol 2005, 98:921-927.10.1111/j.1365-2672.2004.02526.x15752339Search in Google Scholar

26. Saladin M, Cao VT, Lambert T, Donay JL, Herrmann JL, Ould-Hocine Z, Verdet C, Delisle F, Philippon A, Arlet G: Diversity of CTX-M beta-lactamases and their promoter regions from Enterobacteriaceae isolated in three Parisian hospitals. FEMS Microbiol Lett 2002, 209:161-168.10.1111/j.1574-6968.2002.tb11126.x12007800Search in Google Scholar

27. Tenover FC, Rasheed JK: Detection of antimicrobial resistance genes and mutations associated with antimicrobial resistance in microorganisms. In: Molecular microbiology: diagnostic principles and practice, Washington DC, USA, ASM Publishing; 2004, 391-406.Search in Google Scholar

28. Clermont O, Bonacorsi S, Bingen E: Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000, 66:4555-4558.10.1128/AEM.66.10.4555-4558.20009234211010916Search in Google Scholar

29. Higgins J, Hohn C, Hornor S, Frana M, Denver M, Joerger R: Genotyping of Escherichia coli from environmental and animal samples. J Microbiol Methods 2007, 70:227-235.10.1016/j.mimet.2007.04.00917521755Search in Google Scholar

30. Escobar-Páramo P, Le Menac’h A, Le Gall T, Amorin C, Gouriou S, Picard B, Skurnik D, Denamur E: Identification of forces shaping the commensal Escherichia coli genetic structure by comparing animal and human isolates. Environ Microbiol 2006, 8:1975-1984.10.1111/j.1462-2920.2006.01077.x17014496Search in Google Scholar

31. 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. 10.1093/jac/dkq53921393133Search in Google Scholar

32. Ohnishi M, Okatani AT, Esaki H, Harada K, Sawada T, Murakami M, Marumo K, Kato Y, Sato R, Shimura K, Hatanaka N, Takahashi T: Herd prevalence of Enterobacteriaceae producing CTX-M-type and CMY-2 β-lactamases among Japanese dairy farms. J Appl Microbiol 2013, 115:282-289.10.1111/jam.1221123551813Search in Google Scholar

33. Snow LC, Wearing H, Stephenson B, Teale CJ, Coldham NG: Investigation of the presence of ESBL-producing Escherichia coli in the North Wales and West Midlands areas of the UK in 2007 to 2008 using scanning surveillance. Vet Rec 2011, 169:656.10.1136/vr.10003722021063Search in Google Scholar

34. Ewers C, Bethe A, Semmler T, Guenther S, Wieler LH:Extended-spectrum beta-lactamaseproducing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clin Microbiol Infect 2012, 18:646-655.10.1111/j.1469-0691.2012.03850.x22519858Search in Google Scholar

35. Horton RA, Randall LP, Snary EL, Cockrem H, Lotz S, Wearing H, Duncan D, Rabie A, McLaren I, Watson E, La Ragione RM, Coldham NG: 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, 77:3715-3719.10.1128/AEM.02831-10312759421478314Search in Google Scholar

36. Madec JY, Lazizzera C, Chatre P, Meunier D, Martin S, Lepage G, Menard MF, Lebreton P, Rambaud T: Prevalence of fecal carriage of acquired expanded-spectrum cephalosporin resistance in Enterobacteriaceae strains from cattle in France. J Clin Microbiol 2008, 46:1566-1567.10.1128/JCM.02299-07229294318272707Search in Google Scholar

37. Meunier D, Jouy E, Lazizzera C, Kobisch M, Madec JY: CTX-M-1- and CTX-M-15-type beta-lactamases in clinical Escherichia coli isolates recovered from food-producing animals in France. Int J Antimicrob Agents 2006, 28:402-407.10.1016/j.ijantimicag.2006.08.01617027237Search in Google Scholar

38. Mustak HK, Ica T, Ciftci A, Diker KS: Plasmid-mediated quinolone resistance in Escherichia coli strains isolated from animals in Turkey. Ankara Univ Vet Fak Derg 2012, 59:255-258.10.1501/Vetfak_0000002535Search in Google Scholar

39. Picard B, Garcia JS, Gouriou S, Duriez P, Brahimi N, Bingen E, Elion J, Denamur E: The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect Immun 1999, 67:546-553.10.1128/IAI.67.2.546-553.1999963539916057Search in Google Scholar

40. Milanov D, Prunıć B, Velhner M, Todorovıć D, Polaček V: Investigation of biofilm formation and phylogenetic typing of Escherichia coli strains isolated from milk of cows with mastitis. Acta Vet-Beograd 2015, 65: 202-216. 10.1515/acve-2015-0017Search in Google Scholar

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