{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,18]],"date-time":"2026-03-18T17:39:38Z","timestamp":1773855578486,"version":"3.50.1"},"reference-count":57,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2022,10,24]],"date-time":"2022-10-24T00:00:00Z","timestamp":1666569600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Asociaci\u00f3n de Amigos de la Universidad de Navarra"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>In accordance with the global action plan on antimicrobial resistance adopted by the World Health Assembly in 2015, there is a need to develop surveillance programs for antimicrobial resistant bacteria. In this context, we have analyzed the clonal diversity of Extended-spectrum \u03b2-lactamase (ESBL)-producing Escherichia coli (E. coli) isolated from aquatic environments and human and food samples in Spain, with the aim of determining possible clonal complexes (CCs) that act as markers of the potential risk of transmission of these resistant bacteria. The phylogenetic groups, sequence types (STs) and CCs were determined by different Polymerase Chain Reaction (PCR) and Multilocus Sequence Typing (MLST) techniques. Phylogroup A was prevalent and was mainly present in food and water strains, while human strains were mostly associated with phylogroup B2. According to the observed prevalence in the different niches, CC23 and CC10 are proposed as markers of phylogroups A and C, related with the spread of blaCTX-M1 and blaCTX-M15 genes. Similarly, CC131 and CC38 could be associated to the dissemination of pathogenic strains (phylogroups B2 and D) carrying mainly blaCTX-M14 and blaCTX-M15 genes. Some strains isolated from wastewater treatment plants (WWTPs) showed identical profiles to those isolated from other environments, highlighting the importance that water acquires in the dissemination of bacterial resistance. In conclusion, the detection of these genetic markers in different environments could be considered as an alert in the spread of ESBL.<\/jats:p>","DOI":"10.3390\/antibiotics11111465","type":"journal-article","created":{"date-parts":[[2022,10,24]],"date-time":"2022-10-24T11:53:55Z","timestamp":1666612435000},"page":"1465","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Clonal Complexes 23, 10, 131 and 38 as Genetic Markers of the Environmental Spread of Extended-Spectrum \u03b2-Lactamase (ESBL)-Producing E. coli"],"prefix":"10.3390","volume":"11","author":[{"given":"Lara","family":"P\u00e9rez-Etayo","sequence":"first","affiliation":[{"name":"Department of Microbiology and Parasitology, University of Navarra, 31008 Pamplona, Spain"},{"name":"Navarra Institute for Health Research (IdiSNA), 31008 Pamplona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"David","family":"Gonz\u00e1lez","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Parasitology, University of Navarra, 31008 Pamplona, Spain"},{"name":"Navarra Institute for Health Research (IdiSNA), 31008 Pamplona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8242-4496","authenticated-orcid":false,"given":"Ana Isabel","family":"Vitas","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Parasitology, University of Navarra, 31008 Pamplona, Spain"},{"name":"Navarra Institute for Health Research (IdiSNA), 31008 Pamplona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,10,24]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1016\/S0140-6736(21)02724-0","article-title":"Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis","volume":"399","author":"Murray","year":"2022","journal-title":"Lancet"},{"key":"ref_2","unstructured":"WHO (2017). Global Priority List of Antibiotic-Resistant Bacteria to Guide Research, Discovery, and Development of New Antibiotics, World Health Organization."},{"key":"ref_3","unstructured":"WHO (2015). Global Action Plan on Antimicrobial Resistance, World Health Organization."},{"key":"ref_4","unstructured":"WHO Antimicrobial resistance (2014). Global report on surveillance. World Heal. Organ., 61, 383\u2013394."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1128\/CMR.00125-13","article-title":"Escherichia coli ST131, an intriguing clonal group","volume":"27","author":"Bertrand","year":"2014","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"6235","DOI":"10.3390\/ijerph10126235","article-title":"Escherichia coli in Europe: An overview","volume":"10","author":"Allocati","year":"2013","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1038\/nrmicro2265","article-title":"Molecular mechanisms of Escherichia coli pathogenicity","volume":"8","author":"Croxen","year":"2010","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1067\/mlc.2002.121550","article-title":"Extraintestinal pathogenic Escherichia coli: \u201cThe other bad E. coli\u201d","volume":"139","author":"Johnson","year":"2002","journal-title":"J. Lab. Clin. Med."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"54","DOI":"10.3201\/eid1101.040257","article-title":"Genetic background of Escherichia coli and extended-spectrum \u03b2-lactamase type","volume":"11","author":"Branger","year":"2005","journal-title":"Emerg. Infect. Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"6175","DOI":"10.1128\/jb.172.11.6175-6181.1990","article-title":"Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli","volume":"172","author":"Herzer","year":"1990","journal-title":"J. Bacteriol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1086\/317656","article-title":"Phylogenetic Distribution of Extraintestinal Virulence-Associated Traits in Escherichia coli","volume":"183","author":"Johnson","year":"2001","journal-title":"J. Infect. Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1089\/fpd.2010.0598","article-title":"Genetic characterization of extended-spectrum beta-lactamases in Escherichia coli isolates of pigs from a portuguese intensive swine farm","volume":"7","author":"Torres","year":"2010","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_13","first-page":"175","article-title":"Distribuci\u00f3n de grupos filogen\u00e9ticos y factores de virulencia en cepas de Escherichia coli uropat\u00f3gena productora de \u03b2-lactamasa CTX-M-15 aisladas de pacientes de la comunidad en m\u00e9rida, Venezuela","volume":"46","author":"Araque","year":"2014","journal-title":"Rev. Argent. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"4555","DOI":"10.1128\/AEM.66.10.4555-4558.2000","article-title":"Rapid and simple determination of the Escherichia coli phylogenetic group","volume":"66","author":"Clermont","year":"2000","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1111\/1758-2229.12019","article-title":"The Clermont Escherichia coli phylo-typing method revisited: Improvement of specificity and detection of new phylo-groups","volume":"5","author":"Clermont","year":"2013","journal-title":"Environ. Microbiol. Rep."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"7200","DOI":"10.1073\/pnas.1015622108","article-title":"Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species","volume":"108","author":"Luo","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2468","DOI":"10.1111\/j.1462-2920.2011.02519.x","article-title":"Characterization of the cryptic Escherichia lineages: Rapid identification and prevalence","volume":"13","author":"Clermont","year":"2011","journal-title":"Environ. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1111\/j.1365-2958.2006.05172.x","article-title":"Sex and virulence in Escherichia coli: An evolutionary perspective","volume":"60","author":"Wirth","year":"2006","journal-title":"Mol. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/bs.aambs.2014.09.002","article-title":"Escherichia coli ST131: The Quintessential Example of an International Multiresistant High-Risk Clone","volume":"90","author":"Mathers","year":"2015","journal-title":"Adv. Appl. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2125","DOI":"10.1093\/jac\/dkw133","article-title":"CTX-M-15-H30Rx-ST131 subclone is one of the main causes of healthcare-associated ESBL-producing Escherichia coli bacteraemia of urinary origin in Spain","volume":"71","author":"Merino","year":"2016","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1016\/j.meatsci.2012.09.009","article-title":"Prevalence of extended-spectrum \u03b2-lactamase-producing Enterobacteriaceae in meat products sold in Navarra, Spain","volume":"93","author":"Vitas","year":"2013","journal-title":"Meat Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/j.ijfoodmicro.2018.01.026","article-title":"Increased exposure to extended-spectrum \u03b2-lactamase-producing multidrug-resistant Enterobacteriaceae through the consumption of chicken and sushi products","volume":"269","author":"Vitas","year":"2018","journal-title":"Int. J. Food Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"P\u00e9rez-Etayo, L., Gonz\u00e1lez, D., Leiva, J., and Vitas, A.I. (2020). Multidrug-resistant bacteria isolated from different aquatic environments in the North of Spain and South of France. Microorganisms, 8.","DOI":"10.3390\/microorganisms8091425"},{"key":"ref_24","first-page":"7","article-title":"Prevalence and characterization of \u03b2-lactamase-producing Enterobacteriaceae in healthy human carriers","volume":"23","author":"Gallagher","year":"2019","journal-title":"Int. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1016\/S1055-7903(03)00181-7","article-title":"Decreasing the effects of horizontal gene transfer on bacterial phylogeny: The Escherichia coli case study","volume":"30","author":"Sabbagh","year":"2004","journal-title":"Mol. Phylogenet. Evol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Carlos, C., Pires, M.M., Stoppe, N.C., Hachich, E.M., Sato, M.I.Z., Gomes, T.A.T., Amaral, L.A., and Ottoboni, L.M.M. (2010). Escherichia coli phylogenetic group determination and its application in the identification of the major animal source of fecal contamination. BMC Microbiol., 161.","DOI":"10.1186\/1471-2180-10-161"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"642","DOI":"10.1099\/mic.0.000242","article-title":"Phylogenetic, virulence and antibiotic resistance characteristics of commensal strain populations of Escherichia coli from community subjects in the paris area in 2010 and evolution over 30 years","volume":"162","author":"Massot","year":"2016","journal-title":"Microbiology"},{"key":"ref_28","first-page":"4","article-title":"Phylogenetic Group Determination of Escherichia coli Isolated from Animals Samples","volume":"2015","author":"Coura","year":"2015","journal-title":"Sci. World J."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.foodcont.2017.07.028","article-title":"Occurrence of extended spectrum \u03b2-lactamase and AmpC genes among multidrug-resistant Escherichia coli and emergence of ST131 from poultry meat in Thailand","volume":"84","author":"Tansawai","year":"2018","journal-title":"Food Control"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1904","DOI":"10.1099\/mic.0.000367","article-title":"Phylogenetic diversity, antimicrobial susceptibility and virulence characteristics of phylogroup F Escherichia coli in Australia","volume":"162","author":"Vangchhia","year":"2016","journal-title":"Microbiology"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1116","DOI":"10.1128\/JCM.01949-16","article-title":"Rapid and Specific Detection of the Escherichia coli Sequence Type 648 Complex within Phylogroup F","volume":"55","author":"Johnson","year":"2017","journal-title":"J. Clin. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1224","DOI":"10.1093\/jac\/dkt516","article-title":"CTX-M-15-D-ST648 Escherichia coli from companion animals and horses: Another pandemic clone combining multiresistance and extraintestinal virulence?","volume":"69","author":"Ewers","year":"2014","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1016\/j.micinf.2014.12.016","article-title":"Human-associated fluoroquinolone-resistant Escherichia coli clonal lineages, including ST354, isolated from canine feces and extraintestinal infections in Australia","volume":"17","author":"Guo","year":"2015","journal-title":"Microbes Infect."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"195","DOI":"10.3201\/eid1402.070350","article-title":"Dissemination of clonally related E. coli strains expressing ESBL CTX-M-15","volume":"14","author":"Coque","year":"2008","journal-title":"Emerg. Infect. Dis."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1822","DOI":"10.1128\/AAC.01503-13","article-title":"High rate of fecal carriage of extended-spectrum-\u03b2-lactamase-producing Escherichia coli in healthy children in Gipuzkoa, northern Spain","volume":"58","author":"Vicente","year":"2014","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_36","unstructured":"Ojer-usoz, E., Gonzalez, D., and Vitas, A.I. (2015). Caracterizaci\u00f3n de Enterobacterias Productoras de \u03b2-Lactamasas de Espectro Extendido Aisladas en Muestras Alimentarias, Ambientales y Cl\u00ednicas. [Doctoral Thesis, Universidad de Navarra]."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1459","DOI":"10.1128\/AEM.03771-15","article-title":"Escherichia coli population structure and antibiotic resistance at a buffalo\/cattle interface in southern Africa","volume":"82","author":"Mercat","year":"2016","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"6534","DOI":"10.1128\/AEM.01262-09","article-title":"Cryptic lineages of the genus Escherichia","volume":"75","author":"Walk","year":"2009","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1038\/s41598-019-56763-7","article-title":"Meta-analysis of Pandemic Escherichia coli ST131 Plasmidome Proves Restricted Plasmid-clade Associations","volume":"10","author":"Kondratyeva","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/j.ijantimicag.2009.03.006","article-title":"Extended-spectrum \u03b2-lactamase-producing Escherichia coli in Spain belong to a large variety of multilocus sequence typing types, including ST10 complex\/A, ST23 complex\/A and ST131\/B2","volume":"34","author":"Oteo","year":"2009","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1016\/j.ijmm.2014.04.012","article-title":"Prevalence and genotypes of extended spectrum beta-lactamases in Enterobacteriaceae isolated from human stool and chicken meat in Hamburg, Germany","volume":"304","author":"Fenner","year":"2014","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Ojer-Usoz, E., Gonz\u00e1lez, D., and Vitas, A.I. (2017). Clonal diversity of ESBL-producing Escherichia coli isolated from environmental, human and food samples. Int. J. Environ. Res. Public Health, 14.","DOI":"10.3390\/ijerph14070676"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"712","DOI":"10.1093\/cid\/cis502","article-title":"Food-borne origins of Escherichia coli causing extraintestinal infections","volume":"55","author":"Griffin","year":"2012","journal-title":"Clin. Infect. Dis."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1016\/j.ijfoodmicro.2015.02.023","article-title":"Detection of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in vegetables, soil and water of the farm environment in Tunisia","volume":"203","author":"Jouini","year":"2015","journal-title":"Int. J. Food Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"e00135-18","DOI":"10.1128\/CMR.00135-18","article-title":"Global extraintestinal pathogenic Escherichia coli (Expec) lineages","volume":"32","author":"Manges","year":"2019","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1016\/j.scitotenv.2014.09.084","article-title":"Distribution and molecular characterization of genes encoding CTX-M and AmpC \u03b2-lactamases in Escherichia coli isolated from an Indian urban aquatic environment","volume":"505","author":"Bajaj","year":"2015","journal-title":"Sci. Total Environ."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/jac\/dkq415","article-title":"Escherichia coli O25b-ST131: A pandemic, multiresistant, community-associated strain","volume":"66","author":"Rogers","year":"2011","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1093\/jac\/dkx397","article-title":"Molecular relatedness of ESBL\/AmpC-producing Escherichia coli from humans, animals, food and the environment: A pooled analysis","volume":"73","author":"Smid","year":"2018","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Piedra-Carrasco, N., F\u00e0brega, A., Calero-C\u00e1ceres, W., Cornejo-S\u00e1nchez, T., Brown-Jaque, M., Mir-Cros, A., Muniesa, M., and Gonz\u00e1lez-L\u00f3pez, J.J. (2017). Carbapenemase-producing enterobacteriaceae recovered from a Spanish river ecosystem. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0175246"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"e00573-19","DOI":"10.1128\/AAC.00573-19","article-title":"Rapid increase in carbapenemase-producing Enterobacteriaceae in retail meat driven by the spread of the blaNDM-5-carrying IncX3 plasmid in China from 2016 to 2018","volume":"63","author":"Zhang","year":"2019","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"648","DOI":"10.1128\/AEM.02459-14","article-title":"Plasmid-mediated resistance to cephalosporins and fluoroquinolones in various Escherichia coli sequence types isolated from rooks wintering in Europe","volume":"81","author":"Jamborova","year":"2015","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1016\/j.vetmic.2011.10.033","article-title":"Emerging avian pathogenic Escherichia coli strains belonging to clonal groups O111: H4-D-ST2085 and O111: H4-D-ST117 with high virulence-gene content and zoonotic potential","volume":"156","author":"Mora","year":"2012","journal-title":"Vet. Microbiol."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Ronco, T., Stegger, M., Olsen, R.H., Sekse, C., Nordstoga, A.B., Pohjanvirta, T., Lilje, B., Lyhs, U., Andersen, P.S., and Pedersen, K. (2017). Spread of avian pathogenic Escherichia coli ST117 O78: H4 in Nordic broiler production. BMC Genom., 18.","DOI":"10.1186\/s12864-016-3415-6"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1597","DOI":"10.1007\/s42770-021-00538-8","article-title":"Phenotypic and genotypic characterization of mcr-1-positive multidrug-resistant Escherichia coli ST93, ST117, ST156, ST10, and ST744 isolated from poultry in Poland","volume":"52","author":"Siedlecka","year":"2021","journal-title":"Braz. J. Microbiol."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Xia, F., Jiang, M., Wen, Z., Wang, Z., Wang, M., Xu, Y., Zhuge, X., and Dai, J. (2022). Complete genomic analysis of ST117 lineage extraintestinal pathogenic Escherichia coli (ExPEC) to reveal multiple genetic determinants to drive its global transmission: ST117 E. coli as an emerging multidrug-resistant foodborne ExPEC with zoonotic potential. Transbound. Emerg. Dis., 1\u201318.","DOI":"10.1111\/tbed.14678"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/AEM.02748-19","article-title":"Isolation and characterization of ESKAPE-bacteria and ESBL-producing E. coli from waste- and process water of German poultry slaughterhouses","volume":"86","author":"Savin","year":"2020","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_57","first-page":"5860","article-title":"Analysis of a Uropathogenic Escherichia coli Clonal Group by Multilocus Sequence Typing","volume":"43","author":"Tartof","year":"2005","journal-title":"Society"}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/11\/11\/1465\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:01:57Z","timestamp":1760144517000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/11\/11\/1465"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,24]]},"references-count":57,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2022,11]]}},"alternative-id":["antibiotics11111465"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics11111465","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,10,24]]}}}