There are growing concerns about the coselection of resistance against antibiotics and disinfectants in bacterial pathogens. The aim of this study was to characterize the antimicrobial susceptibility profiles, the prevalence of extended-spectrum β-lactamases (ESBLs), plasmid-mediated quinolone resistance genes (PMQRs), and quaternary ammonium compound resistance genes (QACs) in Escherichia coli isolated from ready-to-eat (RTE) meat products obtained in Guangzhou, China, and to determine whether these genes were colocalized in the isolates. A total of 64 E. coli isolates were obtained from 720 RTE meat samples. Multidrug resistance was observed in 70.3% of the isolates. A 100% of the isolates were resistant to benzalkonium chloride. Four types of β-lactamase genes were identified in the 16 ESBL-producing E. coli isolates: blaSHV (9.4%), blaTEM (7.8%), blaCTX-M-15 (1.6%), and blaCTX-M-9 (1.6%). PMQRs were present in nine isolates (14.1%), with aac(6′)-Ib-cr and qnrD detected in eight (12.5%) and one isolate (1.6%), respectively. The QACs ydgE/ydgF were most commonly present (60.9%), while qacF, mdfA, sugE(p), emrE, qacG, sugE(c), and qacE were less prevalent (1.6%–18.8%). Coexistence of ESBLs and/or PMQRs with QACs was found in 21 isolates (32.8%). The aac(6′)-Ib-cr and blaCTX-M-15 genes were found to be cotransferred with qacF in one isolate. The data obtained in this study indicate that ESBLs and/or PMQRs with QACs can not only be colocalized but can also be cotransferred in E. coli isolates from RTE meat products. The E. coli isolates with multiple antimicrobial resistance genes may transmit to humans through food chain and thus require further investigation and increased awareness.
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References
1.
AbdallahHM, ReulandEA, WintermansBB, Al NaiemiN, KoekA, AbdelwahabAM, AmmarAM, MohamedAA, Vandenbroucke-GraulsCM. Extended-spectrum β- lactamases and/or carbapenemases-producing Enterobacteriaceae isolated from retail chicken meat in Zagazig, Egypt. PLoS One, 2015; 10:e0136052.
2.
AlexanderTW, InglisGD, YankeLJ, ToppE, ReadRR, ReuterT, McAllisterTA. Farm-to-fork characterization of Escherichia coli associated with feedlot cattle with a known history of antimicrobial use. Int J Food Microbiol, 2010; 137:40–48.
3.
BadriS, FilliolI, CarleI, HassarM, FassouaneA, CohenN. Prevalence of virulence genes in Escherichia coli isolated from food in Casablanca (Morocco). Food Control, 2009; 20:560–564.
4.
BartonBM, HardingGP, ZuccarelliAJ. A general method for detecting and sizing large plasmids. Anal Biochem, 1995; 226:235–240.
5.
BrialesA, Rodríguez-MartínezJM, VelascoC, Díaz de AlbaP, Rodríguez-BañoJ, Martínez-MartínezL, PascualA. Prevalence of plasmid-mediated quinolone resistance determinants qnr and aac(6′)-Ib-cr in Escherichia coli and Klebsiella pneumoniae producing extended-spectrum β-lactamases in Spain. Int J Antimicrob Agents, 2012; 39:431–434.
6.
Buffet-BataillonS, Le JeuneA, Le Gall-DavidS, Bonnaure-MalletM, Jolivet- GougeonA. Molecular mechanisms of higher MICs of antibiotics and quaternary ammonium compounds for Escherichia coli isolated from bacteraemia. J Antimicrob Chemother, 2012b;67:2837–2842.
7.
Buffet-BataillonS, TattevinP, Bonnaure-MalletM, Jolivet-GougeonA. Emergence of resistance to antibacterial agents, the role of quaternary ammonium compounds -a critical review. Int J Food Microbiol, 2012a;39:381–389.
CallDR, SingerRS, MengD, BroschatSL, OrfeLH, AndersonJM, HerndonDR, KappmeyerLS, DanielsJB, BesserTE. blaCMY-2-positive IncA/C plasmids from Escherichia coli and Salmonella enterica are a distinct component of a larger lineage of plasmids. Antimicrob Agents Chemother, 2010; 54:590–596.
11.
ChungYJ, SaierMHJr.Overexpression of the Escherichia coli sugE gene confers resistance to a narrow range of quaternary ammonium compounds. J Bacteriol, 2002; 184:2543–2545.
12.
Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing:Twenty-Second Informational Supplement (M100-S22). Wayne, PA: Clinical and Laboratory Standards Institute, 2012.
DahmsC, HübnerNO, KossowA, MellmannA, DittmannK, KramerA. Occurrence of ESBL-producing Escherichia coli in livestock and farm workers in mecklenburg-western pomerania, Germany. PLoS One, 2015; 10:e0143326.
15.
DayMJ, RodríguezI, van Essen-ZandbergenA, DierikxC, KadlecK, SchinkAK, WuG, ChattawayMA, DoNascimentoV, WainJ, HelmuthR, GuerraB, SchwarzS, ThrelfallJ, WoodwardMJ, ColdhamN, MeviusD, WoodfordN. Diversity of STs, plasmids and ESBL genes among Escherichia coli from humans, animals and food in Germany, the Netherlands and the UK. J Antimicrob Chemother, 2016; 71:1178–1182.
16.
EckertC, GautierV, Saladin-AllardM, HidriN, VerdetC, Ould-HocineZ, BarnaudG, DelisleF, RossierA, LambertT, PhilipponA, ArletG. Dissemination of CTX-M-type beta lactamases among clinical isolates of Enterobacteriaceae in Paris, France. Antimicrob Agents Chemother, 2004; 48:1249–1255.
17.
EdgarR, BibiE. MdfA, an Escherichia coli multidrug resistance protein with an extraordinarily broad spectrum of drug recognition. J Bacteriol, 1997; 179:2274–2280.
18.
GerbaCP. Quaternary ammonium biocides, efficacy in application. Appl Environ Microbiol, 2015; 81:464–469.
19.
GhodousiA, BonuraC, Di NotoAM, MamminaC. Extended-spectrum β-lactamase, AmpC-producing, and fluoroquinolone-resistant Escherichia coli in retail broiler chicken meat, Italy. Foodborne Pathog Dis, 2015; 12:619–625.
20.
HanC, YangY, WangM, WangA, LuQ, XuX, WangC, LiuL, DengQ, ShenX. The prevalence of plasmid-mediated quinolone resistance determinants among clinical isolates of ESBL or AmpC-producing Escherichia coli from Chinese pediatric patients. Microbiol Immunol, 2010; 54:123–128.
21.
JiangX, YuT, WuN, MengH, ShiL. Detection of qnr, aac(6')-Ib-cr and qepA genes in Escherichia coli isolated from cooked meat products in Henan, China. Int J Food Microbiol, 2014; 187:22–25.
22.
KarlowskyJA, BiedenbachDJ, KazmierczakKM, StoneGG, SahmDF, GnanadhasDP, MaratheSA, ChakravorttyD. Activity of ceftazidime-avibactam against extended-spectrum- and AmpC β-lactamase-producing Enterobacteriaceae collected in the INFORM global surveillance study from 2012 to 2014. Antimicrob Agents Chemother, 2016; 60:2849–2857.
23.
Katharios-LanwermeyerS, Rakic-MartinezM, ElhanafiD, RataniS, TiedjeJM, KathariouS. Coselection of cadmium and benzalkonium chloride resistance in conjugative transfers from nonpathogenic Listeria spp. to other Listeriae. Appl Environ Microbiol, 2012; 78:7549–7556.
24.
Lavilla LermaL, BenomarN, Casado Muñoz MdelC, GálvezA, AbriouelH. Correlation between antibiotic and biocide resistance in mesophilic and psychrotrophic Pseudomonas spp. isolated from slaughterhouse surfaces through meat chain production. Food Microbiol, 2015; 51:33–44.
25.
Lavilla LermaL, BenomarN, GálvezA, AbriouelH. Prevalence of bacteria resistant to antibiotics and/or biocides on meat processing plant surfaces throughout meat chain production. Int J Food Microbiol, 2013; 161:97–106.
26.
LiL, WangB, FengS, LiJ, WuC, WangY, RuanX, ZengM. Prevalence and characteristics of extended-spectrum β-lactamase and plasmid-mediated fluoroquinolone resistance genes in Escherichia coli isolated from chickens in Anhui province, China. PLoS One, 2014; 9:e104356.
27.
MagiorakosAP, SrinivasanA, CareyRB, CarmeliY, FalagasME, GiskeCG, HarbarthS, HindlerJF, KahlmeterG, Olsson- LiljequistB, PatersonDL, RiceLB, StellingJ, StruelensMJ, VatopoulosA, WeberJT, MonnetDL. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect, 2012; 18:268–281.
28.
MoenB, RudiK, BoreE, LangsrudS. Subminimal inhibitory concentrations of the disinfectant benzalkonium chloride select for a tolerant subpopulation of Escherichia coli with inheritable characteristics. Int J Mol Sci, 2012; 13:4101–4123.
29.
MorrisseyI, OggioniMR, KnightD, CuriaoT, CoqueT, KalkanciA, MartinezJL, BIOHYPO Consortium. Evaluation of epidemiological cut-off values indicates that biocide resistant subpopulations are uncommon innatural isolates of clinically-relevant microorganisms. PLoS One, 2014; 9:e86669.
30.
NishinoK, YamaguchiA. Analysis of a complete library of putative drug transporter genes in Escherichia coli. J Bacteriol, 2001; 183:5803–5812.
31.
PaganiL, Dell'AmicoE, MigliavaccaR, D'AndreaMM, GiacoboneE, AmicosanteG, RomeroE, RossoliniGM. Multiple CTX-M-type extended-spectrum β- lactamases in nosocomial isolates of Enterobacteriaceae from a hospital in northern Italy. J Clin Microbiol, 2003; 41:4264–4269.
32.
Pehlivanlar ÖnenS, AslantaşÖ, Şebnem YılmazE, KürekciC. Prevalence of β-lactamase producing Escherichia coli from retail meat in Turkey. J Food Sci, 2015; 80:M2023–M2029.
33.
RibotEM, FairMA, GautomR, CameronDN, HunterSB, SwaminathanB, BarrettTJ. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog Dis, 2006; 3:59–67.
34.
RyuSH, LeeJH, ParkSH, SongMO, ParkSH, JungHW, ParkGY, ChoiSM, KimMS, ChaeYZ, ParkSG, LeeYK. Antimicrobial resistance profiles among Escherichia coli strains isolated from commercial and cooked foods. Int J Food Microbiol, 2012; 159:263–266.
35.
TausovaD, DolejskaM, CizekA, HanusovaL, HrusakovaJ, SvobodaO, CamlikG, LiterakI. Escherichia coli with extended-spectrum β-lactamase and plasmid mediated quinolone resistance genes in great cormorants. J Antimicrob Chemother, 2012; 67:1103–1107.
WelchTJ, FrickeWF, McDermottPF, WhiteDG, RossoML, RaskoDA, MammelMK, EppingerM, RosovitzMJ, WagnerD, RahalisonL, LeclercJE, HinshawJM, LindlerLE, CebulaTA, CarnielE, RavelJ. Multiple antimicrobial resistance in plague, an emerging public health risk. PLoS One, 2007; 2:e309.
38.
XuD, LiY, ZahidMS, YamasakiS, ShiL, LiJR, YanH. Benzalkonium chloride and heavy-metal tolerance in Listeria monocytogenes from retail foods. Int J Food Microbiol, 2014; 190:24–30.
39.
YangH, ChenH, YangQ, ChenM, WangH. High prevalence of plasmid mediated quinolone resistance genes qnr and aac(6’)-Ib-cr in clinical isolates of Enterobacteriaceae from nine teaching hospitals in China. Antimicrob Agents Chemother, 2008; 52:4268–4273.
40.
YuT, JiangX, FuK, LiuB, XuD, JiS, ZhouL. Detection of extended-spectrum β- lactamase and plasmid-mediated quinolone resistance determinants in Escherichia coli isolates from retail meat in China. J Food Sci, 2015; 80:M1039–M104.
41.
ZhangA, HeX, MengY, GuoL, LongM, YuH, LiB, FanL, LiuS, WangH, ZouL. Antibiotic and disinfectant resistance of Escherichia coli isolated from retail meats in Sichuan. China Microb Drug Resist, 2016; 22:80–87.
42.
ZhaoS, BlickenstaffK, Bodeis-JonesS, GainesSA, TongE, McDermottPF. Comparison of the prevalences and antimicrobial resistances of Escherichia coli isolates from different retail meats in the United States, 2002 to 2008. Appl Environ Microbiol, 2012; 78:1701–1707.
43.
ZhuYG, JohnsonTA, SuJQ, QiaoM, GuoGX, StedtfeldRD, HashshamSA, TiedjeJM. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci U S A, 2013; 110:3435–3440.
44.
ZouL, MengJ, McDermottPF, WangF, YangQ, CaoG, HoffmannM, ZhaoS. Presence of disinfectant resistance genes in Escherichia coli isolated from retail meats in the USA. J Antimicrob Chemoth, 2014; 69:2644–2649.
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