{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T12:06:02Z","timestamp":1792757162984,"version":"4.5.0"},"reference-count":32,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2023,1,11]],"date-time":"2023-01-11T00:00:00Z","timestamp":1673395200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>Escherichia coli able to produce extended spectrum \u03b2-lactamases (ESBLs) and plasmid-mediated AmpC \u03b2-lactamases (pAmpCs) represents a serious threat to public health, since these genes confer resistance to critically important antimicrobials (i.e., third generation cephalosporins) and can be transferred to non-resistant bacteria via plasmids. E. coli are known to be able to form a biofilm, which represents a favorable environment for the exchange of resistance determinants. Here, we assessed the ability of 102 ESBL\/pAmpC-producing E. coli isolated from the broiler production pyramid to form a biofilm and to identify genetic factors involved in biofilm formation. All but one of the ESBL\/pAmpC-producing E. coli were able to form a biofilm, and this represents a great concern to public health. E. coli belonging to phylogroups D, E, and F, as well as strains harboring the blaCTX-M-type gene, seem to be associated with an increased biofilm capability (p &lt; 0.05). Furthermore, virulence genes involved in adherence and invasion (i.e., csgBAC, csgDEFG, matABCDEF, and sfaX) seem to enhance biofilm formation in E. coli. Efforts should be made to reduce the presence of ESBL\/pAmpC- and biofilm-producing E. coli in the broiler production pyramid and, therefore, the risk of dissemination of resistant bacteria and genes.<\/jats:p>","DOI":"10.3390\/antibiotics12010155","type":"journal-article","created":{"date-parts":[[2023,1,12]],"date-time":"2023-01-12T02:28:44Z","timestamp":1673490524000},"page":"155","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Biofilm Formation Ability of ESBL\/pAmpC-Producing Escherichia coli Isolated from the Broiler Production Pyramid"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0102-7021","authenticated-orcid":false,"given":"Andrea","family":"Laconi","sequence":"first","affiliation":[{"name":"Department of Comparative Biomedicine and Food Science, University of Padua, 35020 Legnaro, PD, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roberta","family":"Tolosi","sequence":"additional","affiliation":[{"name":"Department of Comparative Biomedicine and Food Science, University of Padua, 35020 Legnaro, PD, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9840-5318","authenticated-orcid":false,"given":"Ilias","family":"Apostolakos","sequence":"additional","affiliation":[{"name":"Dairy Research Institute, Hellenic Agricultural Organization \u201cDIMITRA\u201d, 45221 Ioannina, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6207-4721","authenticated-orcid":false,"given":"Alessandra","family":"Piccirillo","sequence":"additional","affiliation":[{"name":"Department of Comparative Biomedicine and Food Science, University of Padua, 35020 Legnaro, PD, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,1,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1086\/595011","article-title":"Bad Bugs, No Drugs: No ESKAPE! An Update from the Infectious Diseases Society of America","volume":"48","author":"Boucher","year":"2009","journal-title":"Clin. Infect. Dis."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"18","DOI":"10.3109\/23744235.2015.1062536","article-title":"Characterization of ESBL Disseminating Plasmids","volume":"48","author":"Brolund","year":"2016","journal-title":"Infect. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.jgar.2016.04.009","article-title":"Multidrug Resistance and Transferability of BlaCTX-M among Extended-Spectrum \u03b2-Lactamase-Producing Enteric Bacteria in Biofilm","volume":"6","author":"Maheshwari","year":"2016","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1111\/2049-632X.12134","article-title":"Biofilm Models for the Food Industry: Hot Spots for Plasmid Transfer?","volume":"70","author":"Devlieghere","year":"2014","journal-title":"Pathog. Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1128\/CMR.15.2.167-193.2002","article-title":"Biofilms: Survival Mechanisms of Clinically Relevant Microorganisms","volume":"15","author":"Donlan","year":"2002","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1089\/mdr.2018.0175","article-title":"Disinfectant Resistance Profiles and Biofilm Formation Capacity of Escherichia Coli Isolated from Retail Chicken","volume":"25","author":"Sun","year":"2019","journal-title":"Microb. Drug Resist."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1093\/cid\/ciu785","article-title":"Do Human Extraintestinal Escherichia Coli Infections Resistant to Expanded-Spectrum Cephalosporins Originate from Food-Producing Animals? A Systematic Review","volume":"60","author":"Lazarus","year":"2015","journal-title":"Clin. Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"514","DOI":"10.1016\/j.fm.2009.03.004","article-title":"Production of Biofilm and Quorum Sensing by Escherichia Coli O157:H7 and Its Transfer from Contact Surfaces to Meat, Poultry, Ready-to-Eat Deli, and Produce Products","volume":"26","author":"Silagyi","year":"2009","journal-title":"Food Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2","DOI":"10.4103\/2249-5975.119797","article-title":"Determination of Correlation between Biofilm and Extended Spectrum \u03b2 Lactamases Producers of Enterobacteriaceae","volume":"2","author":"Subramanian","year":"2012","journal-title":"Sch. Res. J."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/s13756-016-0104-9","article-title":"Correlation between Biofilm Formation and Resistance toward Different Commonly Used Antibiotics along with Extended Spectrum Beta Lactamase Production in Uropathogenic Escherichia Coli Isolated from the Patients Suspected of Urinary Tract Infections Visit","volume":"5","author":"Neupane","year":"2016","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e0217174","DOI":"10.1371\/journal.pone.0217174","article-title":"Assessing the Occurrence and Transfer Dynamics of ESBL\/PAmpC-Producing Escherichia Coli across the Broiler Production Pyramid","volume":"14","author":"Apostolakos","year":"2019","journal-title":"PLoS One"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1016\/j.prevetmed.2018.12.002","article-title":"Transmission Routes of ESBL\/PAmpC Producing Bacteria in the Broiler Production Pyramid, a Literature Review","volume":"162","author":"Fischer","year":"2019","journal-title":"Prev. Vet. Med."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.ijmm.2018.10.008","article-title":"Biofilm Formation by ESBL-Producing Strains of Escherichia Coli and Klebsiella Pneumoniae","volume":"309","author":"Surgers","year":"2019","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1146\/annurev.micro.60.080805.142106","article-title":"Curli Biogenesis and Function. Annu. Rev","volume":"60","author":"Barnhart","year":"2006","journal-title":"Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2027","DOI":"10.1128\/JB.188.6.2027-2037.2006","article-title":"Gene Expression Regulation by the Curli Activator CsgD Protein: Modulation of Cellulose Biosynthesis and Control of Negative Determinants for Microbial Adhesion","volume":"188","author":"Brombacher","year":"2006","journal-title":"J. Bacteriol"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"602","DOI":"10.1086\/315233","article-title":"Expression of and Cytokine Activation by Escherichia Coli Curli Fibers in Human Sepsis","volume":"181","author":"Bian","year":"2000","journal-title":"J. Infect. Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"34568","DOI":"10.1074\/jbc.M206353200","article-title":"Identification of Two Protein-Binding and Functional Regions of Curli, a Surface Organelle and Virulence Determinant of Escherichia Coli","volume":"277","author":"Herwald","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"944","DOI":"10.1128\/IAI.66.3.944-949.1998","article-title":"Curli, Fibrous Surface Proteins of Escherichia Coli, Interact with Major Histocompatibility Complex Class I Molecules","volume":"66","author":"Wick","year":"1998","journal-title":"Infect. Immun."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2408","DOI":"10.1099\/mic.0.039610-0","article-title":"Mat Fimbriae Promote Biofilm Formation by Meningitis-Associated Escherichia Coli","volume":"156","author":"Lehti","year":"2010","journal-title":"Microbiology"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/j.micpath.2008.12.001","article-title":"Analysis of the SfaXII Locus in the Escherichia Coli Meningitis Isolate IHE3034 Reveals Two Novel Regulatory Genes within the Promoter-Distal Region of the Main S Fimbrial Operon","volume":"46","author":"Dobrindt","year":"2009","journal-title":"Microb. Pathog."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3287","DOI":"10.1099\/mic.0.28098-0","article-title":"Regulation of Type 1 Fimbriae Synthesis and Biofilm Formation by the Transcriptional Regulator LrhA of Escherichia Coli","volume":"151","author":"Blumer","year":"2005","journal-title":"Microbiology"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/j.pep.2012.09.006","article-title":"Expression and Purification of SfaXII, a Protein Involved in Regulating Adhesion and Motility Genes in Extraintestinal Pathogenic Escherichia Coli","volume":"86","author":"Paracuellos","year":"2012","journal-title":"Protein Expr. Purif."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"18495","DOI":"10.1038\/s41598-022-20342-0","article-title":"Pathogenome Comparison and Global Phylogeny of Escherichia Coli ST1485 Strains","volume":"12","author":"Hammad","year":"2022","journal-title":"Sci. Rep."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"4145","DOI":"10.1128\/IAI.68.7.4145-4154.2000","article-title":"Relationship between the Tsh Autotransporter and Pathogenicity of Avian Escherichia Coli and Localization and Analysis of the Tsh Genetic Region","volume":"68","author":"Dozois","year":"2000","journal-title":"Infect. Immun."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"104355","DOI":"10.1016\/j.meegid.2020.104355","article-title":"Antimicrobial Susceptibility, Biofilm Formation and Genetic Profiles of Escherichia Coli Isolated from Retail Chicken Meat","volume":"84","author":"Crecencio","year":"2020","journal-title":"Infect. Genet. Evol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1111\/j.1365-2672.2008.03791.x","article-title":"Measurement of Biofilm Formation by Clinical Isolates of Escherichia Coli Is Method-Dependent","volume":"105","author":"Naves","year":"2008","journal-title":"J. Appl. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1099\/mic.0.2007\/010454-0","article-title":"Type 3 Fimbriae, Encoded by the Conjugative Plasmid POLA52, Enhance Biofilm Formation and Transfer Frequencies in Enterobacteriaceae Strains","volume":"154","author":"Bahl","year":"2008","journal-title":"Microbiology"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Garc\u00eda-Contreras, R., Zhang, X.S., Kim, Y., and Wood, T.K. (2008). Protein Translation and Cell Death: The Role of Rare TRNAs in Biofilm Formation and in Activating Dormant Phage Killer Genes. PLoS One, 3.","DOI":"10.1371\/journal.pone.0002394"},{"key":"ref_29","unstructured":"(2017). CLSI Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute. [27th ed.]."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"11123","DOI":"10.1038\/s41598-020-68036-9","article-title":"High-Resolution Characterisation of ESBL\/PAmpC-Producing Escherichia Coli Isolated from the Broiler Production Pyramid","volume":"10","author":"Apostolakos","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"737720","DOI":"10.3389\/fvets.2021.737720","article-title":"Occurrence of Colibacillosis in Broilers and Its Relationship with Avian Pathogenic Escherichia Coli (APEC) Population Structure and Molecular Characteristics","volume":"8","author":"Apostolakos","year":"2021","journal-title":"Front. Vet. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/S0167-7012(00)00122-6","article-title":"A Modified Microtiter-Plate Test for Quantification of Staphylococcal Biofilm Formation","volume":"40","year":"2000","journal-title":"J. Microbiol. Methods"}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/1\/155\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:03:33Z","timestamp":1760119413000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/1\/155"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,11]]},"references-count":32,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2023,1]]}},"alternative-id":["antibiotics12010155"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics12010155","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,1,11]]}}}