{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T11:20:55Z","timestamp":1788261655538,"version":"build-2803163510"},"reference-count":39,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2021,10,28]],"date-time":"2021-10-28T00:00:00Z","timestamp":1635379200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100011033","name":"agencia estatal de investigaci\u00f3n","doi-asserted-by":"publisher","award":["PID2019-107870RB-I00 EI\/10.13039\/5011000111033"],"award-info":[{"award-number":["PID2019-107870RB-I00 EI\/10.13039\/5011000111033"]}],"id":[{"id":"10.13039\/501100011033","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Universidad de Le\u00f3n","award":["Contrato Predoctoral"],"award-info":[{"award-number":["Contrato Predoctoral"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Foods"],"abstract":"<jats:p>Fresh vegetables are an essential part of a healthy diet, but microbial contamination of fruits and vegetables is a serious concern to human health, not only for the presence of foodborne pathogens but because they can be a vehicle for the transmission of antibiotic-resistant bacteria. This work aimed to investigate the importance of fresh produce in the transmission of extended-spectrum \u03b2-lactamases (ESBL)-producing Enterobacteriaceae. A total of 174 samples of vegetables (117) and farm environment (57) were analysed to determine enterobacterial contamination and presence of ESBL-producing Enterobacteriaceae. Enterobacterial counts above the detection limit were found in 82.9% vegetable samples and 36.8% environmental samples. The average count was 4.2 log cfu\/g or mL, with a maximum value of 6.2 log cfu\/g in a parsley sample. Leafy vegetables showed statistically significant higher mean counts than other vegetables. A total of 15 ESBL-producing isolates were obtained from vegetables (14) and water (1) samples and were identified as Serratia fonticola (11) and Rahnella aquatilis (4). Five isolates of S. fonticola were considered multi-drug resistant. Even though their implication in human infections is rare, they can become an environmental reservoir of antibiotic-resistance genes that can be further disseminated along the food chain.<\/jats:p>","DOI":"10.3390\/foods10112609","type":"journal-article","created":{"date-parts":[[2021,10,28]],"date-time":"2021-10-28T23:50:28Z","timestamp":1635465028000},"page":"2609","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":27,"title":["Extended-Spectrum Beta-Lactamase-Producing Enterobacteriaceae in Fresh Produce"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3389-8040","authenticated-orcid":false,"given":"Alberto","family":"Pintor-Cora","sequence":"first","affiliation":[{"name":"Department of Food Hygiene and Food Technology, Veterinary Faculty, Universidad de Le\u00f3n, 24071 Le\u00f3n, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9506-9312","authenticated-orcid":false,"given":"Laura","family":"\u00c1lvaro-Llorente","sequence":"additional","affiliation":[{"name":"Department of Food Hygiene and Food Technology, Veterinary Faculty, Universidad de Le\u00f3n, 24071 Le\u00f3n, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andr\u00e9s","family":"Otero","sequence":"additional","affiliation":[{"name":"Department of Food Hygiene and Food Technology, Veterinary Faculty, Universidad de Le\u00f3n, 24071 Le\u00f3n, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2677-5229","authenticated-orcid":false,"given":"Jose M.","family":"Rodr\u00edguez-Calleja","sequence":"additional","affiliation":[{"name":"Department of Food Hygiene and Food Technology, Veterinary Faculty, Universidad de Le\u00f3n, 24071 Le\u00f3n, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4001-3386","authenticated-orcid":false,"given":"Jes\u00fas A.","family":"Santos","sequence":"additional","affiliation":[{"name":"Department of Food Hygiene and Food Technology, Veterinary Faculty, Universidad de Le\u00f3n, 24071 Le\u00f3n, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,10,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1089\/fpd.2014.1821","article-title":"Reported Foodborne Outbreaks Due to Fresh Produce in the United States and European Union: Trends and Causes","volume":"12","author":"Ubeda","year":"2015","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.fm.2012.04.016","article-title":"Factors influencing the microbial safety of fresh produce: A review","volume":"32","author":"Olaimat","year":"2012","journal-title":"Food Microbiol."},{"key":"ref_3","unstructured":"FAO\/WHO (2008). Microbiological Hazards in Fresh Leafy Vegetables and Herbs: Meeting Report, FAO."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2643","DOI":"10.3390\/ijerph10072643","article-title":"Antimicrobial resistance in the food chain: A review","volume":"10","author":"Verraes","year":"2013","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/j.tifs.2017.09.007","article-title":"The agri-food chain and antimicrobial resistance: A review","volume":"69","author":"Hudson","year":"2017","journal-title":"Trends Food Sci. Technol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"EFSA BIOHAZ Panel (2021). Role played by the environment in the emergence and spread of antimicrobial resistance (AMR) through the food chain. EFSA J., 19, 6651.","DOI":"10.2903\/j.efsa.2021.6651"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"933","DOI":"10.1128\/CMR.14.4.933-951.2001","article-title":"Extended-spectrum \u03b2-lactamases in the 21st century: Characterization, epidemiology, and detection of this important resistance threat","volume":"14","author":"Bradford","year":"2001","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1111\/j.1469-0691.2007.01850.x","article-title":"Prevalence and spread of extended-spectrum \u03b2-lactamase-producing Enterobacteriaceae in Europe","volume":"14","author":"Novais","year":"2008","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1016\/j.ijfoodmicro.2016.10.036","article-title":"Evaluation of meat, fruit and vegetables from retail stores in five United Kingdom regions as sources of extended-spectrum beta-lactamase (ESBL)-producing and carbapenem-resistant Escherichia coli","volume":"241","author":"Randall","year":"2017","journal-title":"Int. J. Food Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.ijfoodmicro.2013.10.006","article-title":"Extended spectrum \u00df-lactamase- and constitutively AmpC-producing Enterobacteriaceae on fresh produce and in the agricultural environment","volume":"168\u2013169","author":"Blaak","year":"2014","journal-title":"Int. J. Food Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ijfoodmicro.2015.03.014","article-title":"Prevalence and characterization of ESBL- and AmpC-producing Enterobacteriaceae on retail vegetables","volume":"204","author":"Veenman","year":"2015","journal-title":"Int. J. Food Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1601","DOI":"10.1128\/AEM.02506-10","article-title":"Extended-spectrum beta-lactamase gene sequences in Gram-negative saprophytes on retail organic and nonorganic spinach","volume":"77","author":"Raphael","year":"2011","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1843","DOI":"10.1007\/s10096-014-2142-7","article-title":"Prevalence of ESBL-producing Enterobacteriaceae in raw vegetables","volume":"33","author":"Reuland","year":"2014","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1111\/j.1462-2920.2009.02100.x","article-title":"Organic and conventional fruits and vegetables contain equivalent counts of Gram-negative bacteria expressing resistance to antibacterial agents","volume":"12","author":"Ruimy","year":"2010","journal-title":"Environ. Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"5575","DOI":"10.1099\/ijsem.0.001485","article-title":"Genome-based phylogeny and taxonomy of the \u2018Enterobacteriales\u2019: Proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov","volume":"66","author":"Adeolu","year":"2016","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Trujillo, M.E., Dedysh, S., DeVos, P., Hedlund, B., K\u00e4mpfer, P., Rainey, F.A., and Whitman, W.B. (2015). Enterobacteriaceae. Bergey\u2019s Manual of Systematics of Archaea and Bacteria, John Wiley & Sons, Ltd.","DOI":"10.1002\/9781118960608"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1111\/j.1469-0691.2011.03570.x","article-title":"Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance","volume":"18","author":"Magiorakos","year":"2012","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1400","DOI":"10.1111\/j.1600-0463.2007.00722.x","article-title":"Multiplex PCR amplification assay for the detection of blaSHV, blaTEM and blaCTX-M genes in Enterobacteriaceae","volume":"115","author":"Monstein","year":"2007","journal-title":"APMIS"},{"key":"#cr-split#-ref_19.1","unstructured":"European Commission (2005). Commission Regulation"},{"key":"#cr-split#-ref_19.2","unstructured":"(EC) No 2073\/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Off. J. Eur. Union, L338, 1-26."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"EFSA BIOHAZ Panel (2011). Scientific Opinion on the public health risks of bacterial strains producing extended-spectrum \u03b2-lactamases and\/or AmpC \u03b2-lactamases in food and food-producing animals. EFSA J., 9, 2322.","DOI":"10.2903\/j.efsa.2011.2322"},{"key":"ref_21","unstructured":"M\u00e9ndez-Vilas, A. (2010). Coliform bacteria in fresh vegetables: From cultivated lands to consumers. Current Research Topics in Applied Microbiology and Microbial Biotechnology, Proceedings of the II International Conference on Environmental, Industrial and Applied Microbiology (BioMicroWorld2007), World Scientific."},{"key":"ref_22","first-page":"39","article-title":"Resistances to Chemotherapeutic Agents in Enterobacteriaceae Isolates from Organic Fresh Vegetables Marketed in Valencia (Spain)","volume":"5","author":"Falomir","year":"2014","journal-title":"Int. J. Food Nutr. Saf."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"894","DOI":"10.4315\/0362-028X-67.5.894","article-title":"Preharvest evaluation of coliforms, Escherichia coli, Salmonella, and Escherichia coli O157:H7 in organic and conventional produce grown by Minnesota farmers","volume":"67","author":"Mukherjee","year":"2004","journal-title":"J. Food Prot."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1729","DOI":"10.1111\/j.1365-2672.2008.03801.x","article-title":"Prepared salads and public health","volume":"105","author":"Little","year":"2008","journal-title":"J. Appl. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1016\/j.fm.2009.03.013","article-title":"Assessment of the microbiological safety of salad vegetables and sauces from kebab take-away restaurants in the United Kingdom","volume":"26","author":"Meldrum","year":"2009","journal-title":"Food Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1619","DOI":"10.1093\/jac\/dkq178","article-title":"RAHN-2, a chromosomal extended-spectrum class A \u03b2-lactamase from Rahnella aquatilis","volume":"65","author":"Ruimy","year":"2010","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1178","DOI":"10.4315\/0362-028X.JFP-15-018","article-title":"Assessment of the prevalence of extended-spectrum \u03b2-lactamase-producing Enterobacteriaceae in ready-to-eat salads, fresh-cut fruit, and sprouts from the Swiss market","volume":"78","author":"Zurfluh","year":"2015","journal-title":"J. Food Prot."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1089\/fpd.2018.2558","article-title":"Occurrence, identification, and antimicrobial resistance profiles of extended-spectrum and AmpC \u03b2-lactamase-producing Enterobacteriaceae from fresh vegetables retailed in Gauteng Province, South Africa","volume":"16","author":"Richter","year":"2019","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"638","DOI":"10.3389\/fmicb.2020.00638","article-title":"Occurrence, Phenotypic and Molecular Characterization of Extended-Spectrum- and AmpC- \u03b2-Lactamase Producing Enterobacteriaceae Isolated From Selected Commercial Spinach Supply Chains in South Africa","volume":"11","author":"Richter","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"834","DOI":"10.1128\/jcm.29.4.834-835.1991","article-title":"Serratia fonticola isolated from a leg abscess","volume":"29","author":"Bollet","year":"1991","journal-title":"J. Clin. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1097\/MAJ.0b013e3181dd0cca","article-title":"Infection caused by Rahnella aquatilis","volume":"339","author":"Bronze","year":"2010","journal-title":"Am. J. Med. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1016\/j.mib.2006.08.011","article-title":"The CTX-M \u03b2-lactamase pandemic","volume":"9","author":"Coque","year":"2006","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"167","DOI":"10.2147\/IDR.S48820","article-title":"Horizontal gene transfer in the human gastrointestinal tract: Potential spread of antibiotic resistance genes","volume":"7","author":"Huddleston","year":"2014","journal-title":"Infect. Drug Resist."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1128\/AAC.43.2.307","article-title":"Characterization of SFO-1, a plasmid-mediated inducible class A \u03b2-lactamase from Enterobacter cloacae","volume":"43","author":"Matsumoto","year":"1999","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1128\/JCM.01872-10","article-title":"Emergence in Spain of a multidrug-resistant Enterobacter cloacae clinical isolate producing SFO-1 extended-spectrum \u03b2-lactamase","volume":"49","author":"Pereira","year":"2011","journal-title":"J. Clin. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1016\/j.idcr.2016.05.003","article-title":"Serratia fonticola, pathogen or bystander? A case series and review of the literature","volume":"5","author":"Aljorayid","year":"2016","journal-title":"IDCases"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"100692","DOI":"10.1016\/j.nmni.2020.100692","article-title":"First report of biliary tract infection caused by multidrug-resistant Serratia fonticola","volume":"36","author":"Hai","year":"2020","journal-title":"New Microbes New Infect."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"4134","DOI":"10.1128\/AEM.00359-12","article-title":"Resistance to broad-spectrum antibiotics in aquatic systems: Anthropogenic activities modulate the dissemination of blaCTX-M-like genes","volume":"78","author":"Correia","year":"2012","journal-title":"Appl. Environ. Microbiol."}],"container-title":["Foods"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2304-8158\/10\/11\/2609\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:22:00Z","timestamp":1760167320000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2304-8158\/10\/11\/2609"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10,28]]},"references-count":39,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2021,11]]}},"alternative-id":["foods10112609"],"URL":"https:\/\/doi.org\/10.3390\/foods10112609","relation":{},"ISSN":["2304-8158"],"issn-type":[{"value":"2304-8158","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,10,28]]}}}