title: Characterization of extended-spectrum β-lactamases (ESBLs)-producing Salmonella in retail raw chicken carcasses.
abstract: Extended-spectrum β-lactamases (ESBLs)-producing Salmonella is considered a serious concern to public health worldwide. However, limited information is available on ESBLs-producing Salmonella in retail chicken products in China. The objective of this study was to characterize ESBLs-producing Salmonella isolates from retail chickens in China. A total of 890 Salmonella isolates from retail chicken carcasses collected from 4 provinces were firstly screened for ESBLs-production phenotype via the double-disk synergy test method. A total of 96 (10.8%, n=890) ESBLs-producing Salmonella were identified and subjected to PFGE analysis, characterization for the presence of ESBLs encoding genes, transposons, carbapenemase and virulence genes. A total of 59 PFGE profiles were detected in these 96 isolates, among which 57.3% were found to harbor blaTEM-1, whereas 30.2%, 24.0%, 18.8% and 7.3% were carrying blaOXA-1, blaCTX-M-15, blaCTX-M-3and blaPSE-1genes, respectively. Moreover, 42 (43.8%) isolates co-carried 2 ESBLs-producing genes, and two (2.1%) isolates co-carried 3 genes. Furthermore, 24 (25.0%) ESBLs-producing isolates carried VIM and 10 (10.4%) carried KPC encoding genes that closely associated with carbapenems resistance. Eighty-eight isolates harbored transposons ranging from 4.2% for Tn903 to 76.0% for Tn21. Out of the 88 Salmonella that harbored transposons, 25%, 22.7%, 23.9%, 10.2% and 1.1% of isolates were found to carry 2, 3, 4, 5 and 6 transposons, respectively. The minimum inhibitory concentration (MIC) values for cephalosporins (ceftriaxone, cefoperazone and cefoxitin) to ESBLs-producing isolates were from 4 to 1024μg/mL, for nalidixic acid were from 64 to 512μg/mL, for fluoroquinolones (ciprofloxacin, levofloxacin and gatifloxacin) were from 4 to 256μg/mL. Twenty-nine virulence genes were detected in the 96 ESBLs-producing isolates with 2.1% harbored spvR (lowest) and 90.6% harbored marT and steB (highest). All isolates carried at least one virulence gene, 83.3% of the isolates co-carried ≥10, 17.7% co-carried ≥15, and 1.0% co-carried 23 virulence genes. Interestingly, 16.7% of the isolates resistant to >12 antibiotics tested and shown to carry >4 transposons and 10 virulence genes. Our findings indicated that ESBLs-producing Salmonella isolated from retail chicken meat in China were highly resistant to antibiotics, frequently harbored transposons, virulence genes, carbapenems hydrolysis enzymes and ESBLs encoding genes. These isolates can pose a significant public health risk.
authors.affiliation: College of Food Science and Engineering, Northwest A&F University, Yangling 712100, China.
authors.forename: Jing
authors.initials: J
authors.lastname: Qiao
authors.affiliation: College of Food Science and Engineering, Northwest A&F University, Yangling 712100, China.
authors.forename: Qiang
authors.initials: Q
authors.lastname: Zhang
authors.affiliation: College of Public Health, Hamad bin Khalifa University, Doha, Qatar.
authors.forename: Walid Q
authors.initials: WQ
authors.lastname: Alali
authors.affiliation: College of Food Science and Engineering, Northwest A&F University, Yangling 712100, China.
authors.forename: Jiawei
authors.initials: J
authors.lastname: Wang
authors.affiliation: College of Food Science and Engineering, Northwest A&F University, Yangling 712100, China.
authors.forename: Lingyuan
authors.initials: L
authors.lastname: Meng
authors.affiliation: Institute of Quality and Standard for Agro-products, and State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China.
authors.forename: Yingping
authors.initials: Y
authors.lastname: Xiao
authors.affiliation: Institute of Quality and Standard for Agro-products, and State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China.
authors.forename: Hua
authors.initials: H
authors.lastname: Yang
authors.affiliation: State Key Laboratory of Chirosciences, Department of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong.
authors.forename: Sheng
authors.initials: S
authors.lastname: Chen
authors.affiliation: National Institutes for Food and Drug Control, Beijing 100050, China.
authors.forename: Shenghui
authors.initials: S
authors.lastname: Cui
authors.affiliation: College of Food Science and Engineering, Northwest A&F University, Yangling 712100, China. Electronic address: ybwsheng@163.com.
authors.forename: Baowei
authors.initials: B
authors.lastname: Yang
mesh_terms: D000818:Animals; D000900:Anti-Bacterial Agents / Q000494:pharmacology*; D001426:Bacterial Proteins / Q000235:genetics*; D002511:Cephalosporins / Q000494:pharmacology; D002645:Chickens / Q000382:microbiology*; D002681:China; D004251:DNA Transposable Elements / Q000235:genetics; D024901:Drug Resistance, Multiple, Bacterial / Q000235:genetics*; D024841:Fluoroquinolones / Q000494:pharmacology; D005517:Foodborne Diseases / Q000382:microbiology; D000077734:Gatifloxacin; D008460:Meat / Q000382:microbiology; D008826:Microbial Sensitivity Tests; D009268:Nalidixic Acid / Q000494:pharmacology; D012475:Salmonella / Q000187:drug effects* / Q000235:genetics* / Q000302:isolation & purification / Q000378:metabolism; D001618:beta-Lactamases / Q000235:genetics*
chemical_list: D000900:Anti-Bacterial Agents; D001426:Bacterial Proteins; D002511:Cephalosporins; D004251:DNA Transposable Elements; D024841:Fluoroquinolones; D009268:Nalidixic Acid; C473109:beta-lactamase CTX-M-15; C417271:beta-lactamase CTX-M-3; C039404:beta-lactamase OXA-2; C064821:beta-lactamase PSE-1; D001618:beta-Lactamases; C063912:carbapenemase; D000077734:Gatifloxacin
keywords: Antimicrobial resistance; Extended-spectrum β-lactamases; Foodborne Salmonella; Prevalence