Determination of the ciprofloxacin-resistant Escherichia coli isolated from chicken meat in Turkey


S. SAHIN
Résumé
In this study, the occurrence of the ciprofloxacin-resistant (CR) Escherichia coli in chicken meat was determined, and their clonal relations were investigated by using pulsed-field gel electrophoresis (PFGE). Antimicrobialresistance patterns of E. coli isolates were determined by using disc diffusion assay, and minimum inhibitory concentration of ciprofloxacin was determined by E-test. Plasmid-mediated quinolone resistance (PMQR) and extended spectrum beta-lactamase (ESBL) resistance genes were also screened through polymerase chain reactions. Sixty chicken meat samples were collected from different supermarkets and butchers in Sivas, Turkey. CR E. coli strains were determined in 59 (98.3%) chicken meat samples. By analyzing PFGE fingerprint data, 34 different pulsotypes were determined. All E. coli strains were found to be resistant to nalidixic acid, enrofloxacin, and norfloxacin. In addition, isolates were resistant to levofloxacin (40.7%), ampicillin (94.9%), trimethoprim-sulfamethoxazole (76.3%), tetracycline (69.5%), and chloramphenicol (44.1%). However, isolates were susceptible to imipenem and colistin. In this study, 81.4% of CR E. coli isolates were observed to have a multidrug-resistant profile, which is defined as resistance to three or more classes of antibiotics. Through phenotypic confirmation tests, five isolates (8.3%) were determined to be ESBL-producing. The PMQR genes were not determined in any of the isolates. Two isolates (3.4%) possessed the blaCTX-M and blaCMY-2 genes, and 40 isolates (67.8%) had the blaTEM gene. Taken together, retail raw chicken meat is highly contaminated with CR E. coli. However, these isolates are not found to be carriers of the PMQR genes, indicating a low public health problem.
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Références
Ahmed AM, Motoi Y, Sato M, Maruyama A, Watanabe H, Fukumoto Y, Shimamoto T (2007) Zoo animals as reservoirs of gram-negative bacteria harboring integrons and antimicrobial resistance genes. Appl Environ Microbiol 73:6686-6690.
Allocati NM, Masulli M, Alexeyev MF, Di Ilio C (2013) Escherichia coli in Europe: an overview. Int J Environ Res Public Health 10:6235-6254.
Branger C, Zamfir O, Geoffroy S, Laurans G, Arlet G, Thien HV, Gouriou S, Picard B, Denamur E (2005) Genetic background of Escherichia coli and extended-spectrum beta-lactamase type. Emerg Infect Dis 11:54-61.
Borjesson S, Guillard T, Landen A, Bengtsson B, Nilsson O (2016) Introduction of quinolone resistant Escherichia coli to Swedish broiler population by imported breeding animals. Vet Microbiol 194:74-78.
Cattoir V, Poirel L, Rotimi V, Soussy CJ, Nordmann P (2007) Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother 60:394-397.
Cavaco LM, Hasman H, Xia S, Aarestrup FM (2009) qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Chemother 53:603-608.
Cavaco LM, Frimodt-Moller N, Hasman H, Guardabassi L, Nielsen L, Aarestrup FM (2008) Prevalence of quinolone resistance mechanisms and associations to minimum inhibitory concentrations in quinolone-resistant Escherichia coli isolated from humans and swine in Denmark. Microb Drug Resist 14:163-169.
Clinical and Laboratory Standards Institute (CLSI) (2015) Performance standards for antimicrobial susceptibility testing; twenty fifth informational supplement. CLSI document M100-S25. Clinical and Laboratory Standards Institute: Wayne, PA.
Cohen Stuart J, Munckhof van den T, Voets G, Scharringa J, Fluit A, Hall ML (2012) Comparison of ESBL contamination in organic and conventional retail chicken meat. Int J Food Microbiol 154:212-214.
Durmaz R, Otlu B, Koksal F, Hosoglu S, Ozturk R, Ersoy Y, Caliskan A (2009) The optimization of a rapid pulsed-field gel electrophoresis protocol for the typing of Acinetobacter baumannii, Escherichia coli and Klebsiella spp. Jpn J Infect Dis 62:372-377.
Elmas E, Şen A, Karaca S, Pamukçu Ö, Ergün A, Koca S (2019) Türkiye beyaz et üretiminde veteriner tıbbi ürün kullanım trendleri. 5th International Poultry Meat Congress, 24-28 April 2019, pp: 127-131, Antalya/Turkey.
European Medicines Agency (EMEA) (2006) Reflection paper on the use of fluoroquinolones in food producing animals precautions for use in the spc regarding prudent use guidance. EMEA/CVMP/416168/2006-FINAL. 8 November 2006. Available at: www.ema.europa.eu/docs/en_GB/document_library/Other/2009/10/
WC500005173.pdf, [accessed 16 July 2019]
European Food Safety Authority (EFSA) (2019) Available at: https://efsa. onlinelibrary.wiley.com/doi/10.2903/j.efsa.2019.5598. [accessed 14 March 2019]
Fu Y, Zhang W, Wang H, Zhao S, Chen Y, Meng F, Zhang Y, Xu H, Chen X, Zhang F (2013) Specific patterns of gyrA mutations determine the resistance difference to ciprofloxacin and levofloxacin in Klebsiella pneumoniae and Escherichia coli. BMC Infect Dis 13:8.
Ghodousi A, Bonura C, di Noto AM, Mammina C (2015) Extended-spectrum ß-Lactamase, AmpC-producing, and fluoroquinolone-resistant Escherichia coli in retail broiler chicken meat, Italy. Foodborne Pathog Dis 12:619-625.
Gouvea R, Santos FD, de Aquino M, Pereira VL de A (2015) Fluoroquinolones in industrial poultry production, bacterial resistance and food residues: A review. Braz J Poult Sci 17:1-10.
Hasman H, Mevius D, Veldman K, Olesen I, Aarestrup FM (2005) Beta-lactamases among extended-spectrum beta-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. J Antimicrob Chemother 56:115-121.
Jacoby GA, Strahilevitz J, Hooper DC (2014) Plasmid-mediated quinolone resistance. Microbiol Spectr 2:1-42.
Jacoby GA, Gacharna N, Black TA, Millera GH, Hooper DC (2009) Temporal appearance of plasmid-mediated quinolone resistance genes. Antimicrob Agents Chemother 53:1665-1666.
Jacoby GA (2005) Mechanisms of resistance to quinolones. Clin Infect Dis 41 (Suppl 2):120-126.
Jakobsen L, Kurbasic A, Skjøt-Rasmussen L, Ejrnaes K, Porsbo LJ, Pedersen K, Jensen LB, Emborg HD, Agersø Y, Olsen KE, Aarestrup FM, Frimodt-Møller N, Hammerum AM (2010) Escherichia coli isolates from broiler chicken meat, broiler chickens, pork, and pigs share phylogroups and antimicrobial resistance with communitydwelling humans and patients with urinary tract infection. Foodborne Pathog Dis 7:537-547.
Kürekci C, Osek J, Aydın M, Tekeli IO, Kurpas M, Wieczorek K, Sakin F (2018) Evaluation of bulk tank raw milk and raw chicken meat samples as source of ESBL producing Escherichia coli in Turkey: Recent insights. J Food Safety e12605:1-7.
Leinberger DM, Grimm V, Rubtsova M, Weile J, Schröppel K, Wichelhaus TA, Knabbe C, Schmid RD, Bachmann TT (2010) Integrated detection of extended-spectrum-beta-lactam resistance by DNA microarray-based genotyping of TEM, SHV, and CTX-M genes. J Clin Microbiol 48:460-471.
Literak I, Reitschmied T, Bujnakova D, Dolejska M, Cizek A, Bardon J, Pokludova L, Alexa P, Halova D, Jamborova I (2013) Broilers as a source of quinolone-resistant and extraintestinal pathogenic Escherichia coli in the Czech Republic. Microb Drug Resist 19:57-63.
Lu T, Zhao X, Li X, Drlica-Wagner A, Wang JY, Domagala J, Drlica K (2001) Enhancement of fluoroquinolone activity by C-8 halogen and methoxy moieties: action against a gyrase resistance mutant of mycobacterium smegmatis and a gyrase-topoisomerase IV double mutant of Staphylococcus aureus. Antimicrob Agents Chemother 45:2703-2709.
Martinez-Martinez L, Eliecer Cano M, Manuel Rodriguez-Martinez J, Calvo J, Pascual A (2008) Plasmid-mediated quinolone resistance. Expert Rev Anti Infect Ther 6:685-711.
Martinez-Martinez L, Pascual A, Jacoby GA (1998) Quinolone resistance from a transferable plasmid. Lancet 351:797-799.
Mavroidi A, Miriagou V, Liakopoulos A, Tzelepi E, Stefos A, Dalekos GN (2012) Ciprofloxacin-resistant Escherichia coli in Central Greece: mechanisms of resistance and molecular identification. BMC Infect Dis 12:371.
Mulvey MR, Soule G, Boyd D, Demczuk W, Ahmed R, the Multi-provincial Salmonella Typhimurium Case Control Study Group (2003) Characterization of the first extended-spectrum beta-lactamase-producing Salmonella isolate identified in Canada. J Clin Microbiol 41:460-462.
Müştak HK, İca T, Çiftci A, Diker KS (2012) Plasmid-mediated quinolone resistance in Escherichia coli strains isolated from animals in Turkey. Ankara Univ Vet Fak Derg 59:255-258.
Nazik H, Öngen B, Kuvat N (2008) Investigation of plasmid-mediated quinolone resistance among isolates obtained in a Turkish intensive care unit. Jpn J Infect Dis 61:310-312.
Nordman P, Poirel L (2005) Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J Antimicrob Chemother 56:463-69.
Park CH, Robicsek A, Jacoby GA, Sahm D, Hooper DC (2006) Prevalence in the United States of aac(6)-Ib-cr encoding a ciprofloxacin modifying enzyme. Antimicrob Agents Chemother 50:3953-3955.
Ray B (2004) Fundamental Food Microbiology. 3. ed, CRC Press, Boca Raton: Florida.
Resmi Gazete (RG) (2006) Yem Katkıları ve Premikslerin Üretimi, İthalatı, İhracatı, Satışı ve Kullanımı Hakkında Tebliğde Değişiklik Yapılmasına Dair Tebliğ. Tarım ve Köyişleri Bakanlığından. 21 Ocak 2006. Sayı: 26056 Tebliğ No: 2006/1 Resmi Gazete.
Robicsek A, Strahilevitz J, Sahm DF, Jacoby GA, Hooper DC (2006) Qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob Agents Chemother 50:2872-2874.
Rodríguez-Martínez JM, Machuca J, Cano ME, Calvo J, Martínez-Martínez L, Pascual A (2016) Plasmid-mediated quinolone resistance: two decades on. Drug Resist Updat 29:13-29.
Ruiz J (2003) Mechanisms of resistance to quinolones: target alterations, decreased accumulation and DNA gyrase protection. J Antimicrob Chemother 51:1109-1117.
Seo KW, Lee YJ (2019) Prevalence and characterization of plasmid mediated quinolone resistance genes and class 1 integrons among multidrug-resistant Escherichia coli isolates from chicken meat. J Appl Poult Res 28:761-770.
Slettemeas JS, Sunde M, Ulstad CR, Norstrom M, Wester AL, Urdahl AM (2019) Occurrence and characterization of quinolone resistant Escherichia coli from Norwegian turkey meat and complete sequence of an IncX1 plasmid encoding qnrS1. PLoS ONE 14:e0212936.
Sola-Gines M, Gonzalez-Lopez JJ, Cameron-Veas K, Piedra-Carrasco N, Cerda-Cuellar M, Migura-Garcia L (2015) Houseflies (Musca domestica) as vectors for extended-spectrum β-lactamase-producing Escherichia coli on Spanish broiler farms. Appl Environ Microbiol 81:3604-3611.
Soufi L, Sáenz Y, Vinué L, Abbassi MS, Ruiz E, Zarazaga M, Ben Hassen A, Hammami S, Torres C (2011) Escherichia coli of poultry food origin as reservoir of sulphonamide resistance genes and integrons. Int J Food Microbiol 144:497-502.
Şahinturk P, Arslan E, Buyukcangaz E, Sonal S, Şen A, Ersoy F, Webber MA, Piddock LJV Cengiz M (2016) High level fluoroquinolone resistance in Escherichia coli isolated from animals in Turkey is due to multiple mechanisms. Turk J Vet Anim Sci 40:214-218.
Vanni M, Meucci V, Tognetti R, Cagnardi P, Montesissa C, Piccirillo A, Rossi AM, di Bello D, Intorre L (2014) Fluoroquinolone resistance and molecular characterization of gyrA and parC quinolone resistance-determining regions in Escherichia coli isolated from poultry. Poultry Sci 93:856-863.
Wasyl D (2014) Prevalence and characterization of quinolone resistance mechanisms in commensal Escherichia coli isolated from slaughter animals in Poland, 2009-2012. Microb Drug Resist 20:544-549.
World Health Organization (WHO) (2007) Available at: https://www.who. int/whr/2007/en. [accessed 21 March 2019 ]
Xu X, Cui S, Zhang F, Luo Y, Gu Y, Yang B, Li F, Chen Q, Zhou G, Wang Y, Pang L, Lin L (2014) Prevalence and characterization of cefotaxime and ciprofloxacin co-resistant Escherichia coli isolates in retail chicken carcasses and ground pork, China. Microb Drug Resist 20:73-81.
Yang T, Zeng Z, Rao L, Chen X, He D, Lv L, Wang J, Zeng L, Feng M, Liu JH (2014) The association between occurrence of plasmid-mediated quinolone resistance and ciprofloxacin resistance in Escherichia coli isolates of different origins. Vet Microbiol 170:89-96.
Yu T, Jiang X, Fu K, Liu B, Xu D, Ji S, Zhou L (2015) Detection of extended-spectrum β-lactamase and plasmid-mediated quinolone resistance determinants in Escherichia coli isolates from retail meat in China. J Food Sci 80:M1039-1043.
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