Molecular characterization of extended-spectrum β-lactamases-producing Enterobacteriaceae species in ground beef and chicken meat

İnat G., Sırıken B., Çiftci A., Erol İ., Başkan C., Yıldırım T.

International journal of food microbiology, vol.398, pp.110228, 2023 (SCI-Expanded) identifier identifier

  • Publication Type: Article / Article
  • Volume: 398
  • Publication Date: 2023
  • Doi Number: 10.1016/j.ijfoodmicro.2023.110228
  • Journal Name: International journal of food microbiology
  • Journal Indexes: Science Citation Index Expanded (SCI-EXPANDED), Scopus, Academic Search Premier, PASCAL, Aquatic Science & Fisheries Abstracts (ASFA), BIOSIS, Biotechnology Research Abstracts, CAB Abstracts, EMBASE, Environment Index, Food Science & Technology Abstracts, MEDLINE, Veterinary Science Database, DIALNET
  • Page Numbers: pp.110228
  • Keywords: Antibiotic resistance, Chicken-meat, Class 1 integron (intI1), ESBL-Enterobacteriaceae, Ground-beef
  • Lokman Hekim University Affiliated: Yes


The objectives of this study were i) to characterize extended-spectrum β-lactamase-producing Enterobacteriaceae (ESBL-E) using pheno- and genotyping methods, ii) to evaluate the antimicrobial resistance pattern against 10 antibiotics, and iii) to investigate class 1 integron (intI1) in 80 Enterobacteriaceae isolates obtained from chicken meat (n = 40; 47 isolates) and ground beef (n = 40; 33 isolates) samples. Through the study, we found that 55 (68.7 %) of 80 Enterobacteriaceae isolates were capable of β-lactamase activity, and 38 (47.5 %) of them were multi-drug-resistant (MDR). The ground meat-origin isolates are 1.2 times more likely to produce imipenem resistance compared to chicken-meat-origin isolates (z = 2.1, p < 0.05, OR = 1.42). ESBL-E was found in 18 (22.5 %) of the isolates, 16.3 % of chicken meat and 6.3 % of ground beef origin. The bla genes were detected in 14 isolates [bla-TEM (n = 10; 12.5 %); bla-SHV (n = 4; 5.0 %); bla-CTX-M (n = 0)], where the predominant species were Escherichia (E.) coli and Citrobacter braakii. The nine ESBL-E isolates were MDR. Twenty-eight (35.0 %) of 80 isolates were found to be resistant to at least one third-generation cephalosporin, and eight (28.6 %) of them were also ESBL-E. Eleven of 16 (48.5 %) carbapenem-resistant isolates were ESBL-E. The intI1 gene was found in 13 (16.3 %) isolates, five of which were ESBL-E, and four of which were MDR. Co-existing with bla-TEM and the intI1 isolate was ESBL-E. coli, which was resistant to nine antibiotics. In conclusion, chicken meat and ground beef may pose a potential risk of containing ESBL-E, and bla genes which could be spread to the entire food chain.