{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,20]],"date-time":"2026-10-20T18:47:20Z","timestamp":1792522040105,"version":"4.5.0"},"reference-count":37,"publisher":"MDPI AG","issue":"22","license":[{"start":{"date-parts":[[2022,11,18]],"date-time":"2022-11-18T00:00:00Z","timestamp":1668729600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Science and Technology Major Project of Hubei Province","award":["2020ABA016"],"award-info":[{"award-number":["2020ABA016"]}]},{"name":"Science and Technology Major Project of Hubei Province","award":["2021CFA019"],"award-info":[{"award-number":["2021CFA019"]}]},{"name":"Science and Technology Major Project of Hubei Province","award":["CARS-41-G13"],"award-info":[{"award-number":["CARS-41-G13"]}]},{"name":"China Agriculture Research System of MOF and MARA","award":["2020ABA016"],"award-info":[{"award-number":["2020ABA016"]}]},{"name":"China Agriculture Research System of MOF and MARA","award":["2021CFA019"],"award-info":[{"award-number":["2021CFA019"]}]},{"name":"China Agriculture Research System of MOF and MARA","award":["CARS-41-G13"],"award-info":[{"award-number":["CARS-41-G13"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>The emergence and dissemination of Escherichia coli (E. coli) strains that produce extended-spectrum beta-lactamases (ESBLs) represents a major public health threat. The present study was designed to evaluate the prevalence and characteristics of ESBL-producing Escherichia coli isolates from chickens in central China during 2016\u20132019. A total of 407 E. coli strains isolated from 581 chicken swabs were identified conventionally and analyzed for various cephalosporin susceptibility by disk-diffusion assay. ESBL-producing strains were screened using the double=disk synergy test and ESBL-encoding genes were carried out by PCR\/sequencing. A total of 402 E. coli isolates exhibited strong resistance to first- to fourth-generation cephalosporins and monobactam antibiotics, especially cefazolin (60.69%), cefuroxime (54.05%), cefepime (35.14%), ceftriaxone (54.30%), and aztreonam (40.29%). Piperacillin\/tazobactam (1.72%) was the most effective drug against the strains, but the resistance rates increased each year. Among the isolates, 262 were identified as ESBL producers and the isolation rates for the ESBL producers increased from 63.37% to 67.35% over the four years. CTX-M (97.33%) was the most prevalent type, followed by TEM (76.72%) and SHV (3.05%). The most common ESBL genotype combination was blaTEM + blaCTX-M (74.46%), in which the frequency of carriers increased steadily, followed by blaCTX-M + blaSHV (3.05%). In addition, the most predominant specific CTX-M subtypes were CTX-M-55 (48.47%) and CTX-M-1 (17.94%), followed by CTX-M-14 (11.01%), CTX-M-15 (8.02%), CTX-M-9 (6.11%), CTX-M-65 (4.58%), and CTX-M-3 (1.15%). Moreover, a novel multiplex qPCR assay was developed to detect blaCTX-M, blaTEM, and blaSHV, with limits of detection of 2.06 \u00d7 101 copies\/\u03bcL, 1.10 \u00d7 101 copies\/\u03bcL, and 1.86 \u00d7 101 copies\/\u03bcL, respectively, and no cross-reactivity with other ESBL genes and avian pathogens. The assays exhibited 100% sensitivity and specificities of 85%, 100%, and 100% for blaCTX-M, blaTEM, and blaSHV, respectively. In conclusion, our findings indicated that ESBL-producing E.coli strains isolated from chickens in central China were highly resistant to cephalosporins and frequently harbored diversity in ESBL-encoding genes. These isolates can pose a significant public health risk. The novel multiplex qPCR method developed in this study may be a useful tool for molecular epidemiology and surveillance studies of ESBL genes.<\/jats:p>","DOI":"10.3390\/ani12223191","type":"journal-article","created":{"date-parts":[[2022,11,18]],"date-time":"2022-11-18T03:57:44Z","timestamp":1668743864000},"page":"3191","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["Prevalence of Extended-Spectrum \u03b2-Lactamase-Resistant Genes in Escherichia coli Isolates from Central China during 2016\u20132019"],"prefix":"10.3390","volume":"12","author":[{"given":"Zui","family":"Wang","sequence":"first","affiliation":[{"name":"Key Laboratory of Prevention and Control Agents for Animal Bacteriosis (Ministry of Agriculture and Rural Affairs), Institute of Animal Husbandry and Veterinary, Hubei Academy of Agricultural Sciences, Wuhan 430064, China"},{"name":"Hubei Hongshan Laboratory, Wuhan 430064, China"},{"name":"State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan 430064, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qin","family":"Lu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Prevention and Control Agents for Animal Bacteriosis (Ministry of Agriculture and Rural Affairs), Institute of Animal Husbandry and Veterinary, Hubei Academy of Agricultural Sciences, Wuhan 430064, China"},{"name":"Hubei Hongshan Laboratory, Wuhan 430064, China"},{"name":"State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan 430064, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaohui","family":"Mao","sequence":"additional","affiliation":[{"name":"Key Laboratory of Prevention and Control Agents for Animal Bacteriosis (Ministry of Agriculture and Rural Affairs), Institute of Animal Husbandry and Veterinary, Hubei Academy of Agricultural Sciences, Wuhan 430064, China"},{"name":"Hubei Hongshan Laboratory, Wuhan 430064, China"},{"name":"State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan 430064, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Li","sequence":"additional","affiliation":[{"name":"Key Laboratory of Prevention and Control Agents for Animal Bacteriosis (Ministry of Agriculture and Rural Affairs), Institute of Animal Husbandry and Veterinary, Hubei Academy of Agricultural Sciences, Wuhan 430064, China"},{"name":"Hubei Hongshan Laboratory, Wuhan 430064, China"},{"name":"State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan 430064, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junfeng","family":"Dou","sequence":"additional","affiliation":[{"name":"Key Laboratory of Prevention and Control Agents for Animal Bacteriosis (Ministry of Agriculture and Rural Affairs), Institute of Animal Husbandry and Veterinary, Hubei Academy of Agricultural Sciences, Wuhan 430064, China"},{"name":"Hubei Hongshan Laboratory, Wuhan 430064, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qigai","family":"He","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan 430064, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huabin","family":"Shao","sequence":"additional","affiliation":[{"name":"Key Laboratory of Prevention and Control Agents for Animal Bacteriosis (Ministry of Agriculture and Rural Affairs), Institute of Animal Husbandry and Veterinary, Hubei Academy of Agricultural Sciences, Wuhan 430064, China"},{"name":"Hubei Hongshan Laboratory, Wuhan 430064, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qingping","family":"Luo","sequence":"additional","affiliation":[{"name":"Key Laboratory of Prevention and Control Agents for Animal Bacteriosis (Ministry of Agriculture and Rural Affairs), Institute of Animal Husbandry and Veterinary, Hubei Academy of Agricultural Sciences, Wuhan 430064, China"},{"name":"Hubei Hongshan Laboratory, Wuhan 430064, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,11,18]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Kanokudom, S., Assawakongkarat, T., Akeda, Y., Ratthawongjirakul, P., Chuanchuen, R., and Chaichanawongsaroj, N. (2021). Rapid detection of extended spectrum beta-lactamase producing Escherichia coli isolated from fresh pork meat and pig cecum samples using multiplex recombinase polymerase amplification and lateral flow strip analysis. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0248536"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Fulgenzio, C., Massari, M., Traversa, G., Da Cas, R., Ferrante, G., Aschbacher, R., Moser, V., Pagani, E., Vestri, A.R., and Massidda, O. (2021). Impact of Prior Antibiotic Use in Primary Care on Escherichia coli Resistance to Third Generation Cephalosporins: A Case-Control Study. Antibiotics, 10.","DOI":"10.3390\/antibiotics10040451"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1590\/S0036-46652014000400012","article-title":"Antimicrobial drug resistance in strains of Escherichia coli isolated from food sources","volume":"56","author":"Rasheed","year":"2014","journal-title":"Rev. Inst. Med. Trop. Sao Paulo"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1111\/zph.12920","article-title":"Assessing antimicrobial resistance occurrence in the Portuguese food system: Poultry, pigs and derived food, 2014-2018","volume":"69","author":"Costa","year":"2022","journal-title":"Zoonoses Public Health"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"628738","DOI":"10.3389\/fmicb.2021.628738","article-title":"Occurrence and Molecular Characteristics of Extended-Spectrum Beta-Lactamase-Producing Enterobacterales Recovered From Chicken, Chicken Meat, and Human Infections in Sao Paulo State, Brazil","volume":"12","author":"Cardozo","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3472","DOI":"10.1016\/j.jmb.2019.04.002","article-title":"beta-Lactamases and beta-Lactamase Inhibitors in the 21st Century","volume":"431","author":"Tooke","year":"2019","journal-title":"J. Mol. Biol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Geser, N., Stephan, R., and Hachler, H. (2012). Occurrence and characteristics of extended-spectrum beta-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Vet. Res., 8.","DOI":"10.1186\/1746-6148-8-21"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1007\/s11033-020-06047-5","article-title":"The first evaluation relationship of integron genes and the multidrug-resistance in class A ESBLs genes in enteropathogenic Escherichia coli strains isolated from children with diarrhea in Southwestern Iran","volume":"48","author":"Jomehzadeh","year":"2021","journal-title":"Mol. Biol. Rep."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"7110","DOI":"10.1038\/s41598-021-86570-y","article-title":"Detection of extended spectrum beta-lactamase genes in Pseudomonas aeruginosa isolated from patients in rural Eastern Cape Province, South Africa","volume":"11","author":"Hosu","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"601924","DOI":"10.3389\/fmicb.2021.601924","article-title":"Detection of Cephalosporin and Fluoroquinolone Resistance Genes via Novel Multiplex qPCR in Fecal Salmonella Isolates From Northern Californian Dairy Cattle, 2002\u20132016","volume":"12","author":"Basbas","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Shahi, S.K., Singh, V.K., and Kumar, A. (2013). Detection of Escherichia coli and associated beta-lactamases genes from diabetic foot ulcers by multiplex PCR and molecular modeling and docking of SHV-1, TEM-1, and OXA-1 beta-lactamases with clindamycin and piperacillin-tazobactam. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0068234"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Bedenic, B., and Mestrovic, T. (2021). Mechanisms of Resistance in Gram-Negative Urinary Pathogens: From Country-Specific Molecular Insights to Global Clinical Relevance. Diagnostics, 11.","DOI":"10.3390\/diagnostics11050800"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1016\/j.ijmm.2013.02.008","article-title":"CTX-M-type beta-lactamases: A successful story of antibiotic resistance","volume":"303","author":"Arena","year":"2013","journal-title":"Int. J. Med. Microbiol. IJMM"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Havelaar, A.H., Kirk, M.D., Torgerson, P.R., Gibb, H.J., Hald, T., Lake, R.J., Praet, N., Bellinger, D.C., de Silva, N.R., and Gargouri, N. (2015). World Health Organization Global Estimates and Regional Comparisons of the Burden of Foodborne Disease in 2010. PLoS Med., 12.","DOI":"10.1371\/journal.pmed.1001923"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1007","DOI":"10.2147\/IDR.S160720","article-title":"The prevalence of plasmid-mediated quinolone resistance and ESBL-production in Enterobacteriaceae isolated from urinary tract infections","volume":"11","author":"Azargun","year":"2018","journal-title":"Infect. Drug Resist."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Rivoarilala, O.L., Garin, B., Andriamahery, F., and Collard, J.M. (2018). Rapid in vitro detection of CTX-M groups 1, 2, 8, 9 resistance genes by LAMP assays. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0200421"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"5859","DOI":"10.1038\/s41598-018-23962-7","article-title":"Poultry hatcheries as potential reservoirs for antimicrobial-resistant Escherichia coli: A risk to public health and food safety","volume":"8","author":"Osman","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"755545","DOI":"10.3389\/fcimb.2021.755545","article-title":"High Prevalence and Diversity Characteristics of blaNDM, mcr, and blaESBLs Harboring Multidrug-Resistant Escherichia coli From Chicken, Pig, and Cattle in China","volume":"11","author":"Liu","year":"2021","journal-title":"Front. Cell Infect. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1016\/j.jgar.2020.06.028","article-title":"Genetic diversity, antimicrobial resistance and extended-spectrum beta-lactamase type of Escherichia coli isolates from chicken, dog, pig and yak in Gansu and Qinghai Provinces, China","volume":"22","author":"Wang","year":"2020","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1089\/fpd.2014.1857","article-title":"Characterization of antimicrobial resistance and extended-spectrum beta-lactamase genes in Escherichia coli isolated from chickens","volume":"12","author":"Tong","year":"2015","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"105919","DOI":"10.1016\/j.ijantimicag.2020.105919","article-title":"Contribution of beta-lactamase and efflux pump overproduction to tazobactam-piperacillin resistance in clinical isolates of Escherichia coli","volume":"55","author":"Suzuki","year":"2020","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"S44","DOI":"10.1093\/jtm\/taw102","article-title":"The ecology of extended-spectrum beta-lactamases (ESBLs) in the developed world","volume":"24","author":"Doi","year":"2017","journal-title":"J. Travel. Med."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1016\/j.vetmic.2010.02.005","article-title":"Characterization of antimicrobial resistance and molecular determinants of beta-lactamase in Escherichia coli isolated from chickens in China during 1970\u20132007","volume":"144","author":"Li","year":"2010","journal-title":"Vet. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1038\/s41426-018-0033-1","article-title":"Rapid rise of the ESBL and mcr-1 genes in Escherichia coli of chicken origin in China, 2008\u20132014","volume":"7","author":"Wu","year":"2018","journal-title":"Emerg. Microbes Infect."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"110","DOI":"10.3389\/fmicb.2012.00110","article-title":"CTX-M Enzymes: Origin and Diffusion","volume":"3","author":"Canton","year":"2012","journal-title":"Front. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"6233","DOI":"10.1128\/AAC.01245-15","article-title":"Antimicrobial Peptide Novicidin Synergizes with Rifampin, Ceftriaxone, and Ceftazidime against Antibiotic-Resistant Enterobacteriaceae In Vitro","volume":"59","author":"Soren","year":"2015","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Merida-Vieyra, J., De Colsa, A., Calderon Castaneda, Y., Arzate Barbosa, P., and Aquino Andrade, A. (2016). First Report of Group CTX-M-9 Extended Spectrum Beta-Lactamases in Escherichia coli Isolates from Pediatric Patients in Mexico. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0168608"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1097\/INF.0000000000000623","article-title":"Emergence of extended spectrum-beta-lactamase-producing Escherichia coli O25b-ST131: A major community-acquired uropathogen in infants","volume":"34","author":"Cheng","year":"2015","journal-title":"Pediatr. Infect. Dis. J."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1475","DOI":"10.1111\/j.1469-0691.2010.03127.x","article-title":"High prevalence of bla(CTX-M) extended-spectrum beta-lactamase genes in Escherichia coli isolates from pets and emergence of CTX-M-64 in China","volume":"16","author":"Sun","year":"2010","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.ijfoodmicro.2016.07.017","article-title":"Prevalence, antibiotic resistance, and extended-spectrum and AmpC beta-lactamase productivity of Salmonella isolates from raw meat and seafood samples in Ho Chi Minh City, Vietnam","volume":"236","author":"Nguyen","year":"2016","journal-title":"Int. J. Food Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"e00107-20","DOI":"10.1128\/mSphere.00107-20","article-title":"Prevalence and Characteristics of Extended-Spectrum-beta-Lactamase-Producing and Carbapenemase-Producing Enterobacteriaceae from Freshwater Fish and Pork in Wet Markets of Hong Kong","volume":"5","author":"Sapugahawatte","year":"2020","journal-title":"mSphere"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1268","DOI":"10.3389\/fmicb.2019.01268","article-title":"The Emergence of Chromosomally Located blaCTX-M-55 in Salmonella From Foodborne Animals in China","volume":"10","author":"Zhang","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Szmolka, A., Wiener, Z., Matulova, M.E., Varmuzova, K., and Rychlik, I. (2015). Gene Expression Profiles of Chicken Embryo Fibroblasts in Response to Salmonella Enteritidis Infection. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0127708"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Nossair, M.A., Abd El Baqy, F.A., Rizk, M.S.Y., Elaadli, H., Mansour, A.M., Abd El-Aziz, A.H., Alkhedaide, A., Soliman, M.M., Ramadan, H., and Shukry, M. (2022). Prevalence and Molecular Characterization of Extended-Spectrum beta-Lactamases and AmpC beta-lactamase-Producing Enterobacteriaceae among Human, Cattle, and Poultry. Pathogens, 11.","DOI":"10.3390\/pathogens11080852"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Mallik, D., Jain, D., Bhakta, S., and Ghosh, A.S. (2022). Role of AmpC-Inducing Genes in Modulating Other Serine Beta-Lactamases in Escherichia coli. Antibiotics, 11.","DOI":"10.3390\/antibiotics11010067"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"390","DOI":"10.24171\/j.phrp.2021.0272","article-title":"Prevalence of plasmid-mediated AmpC beta-lactamases among uropathogenic Escherichia coli isolates in southwestern Iran","volume":"12","author":"Jomehzadeh","year":"2021","journal-title":"Osong. Public Health Res. Perspect."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1186\/s13568-015-0136-1","article-title":"A qPCR and multiplex pyrosequencing assay combined with automated data processing for rapid and unambiguous detection of ESBL-producers Enterobacteriaceae","volume":"5","author":"Deccache","year":"2015","journal-title":"AMB Express"}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/12\/22\/3191\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:20:47Z","timestamp":1760145647000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/12\/22\/3191"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,11,18]]},"references-count":37,"journal-issue":{"issue":"22","published-online":{"date-parts":[[2022,11]]}},"alternative-id":["ani12223191"],"URL":"https:\/\/doi.org\/10.3390\/ani12223191","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,11,18]]}}}