{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T04:56:14Z","timestamp":1787028974459,"version":"build-2736575974"},"reference-count":102,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2022,3,17]],"date-time":"2022-03-17T00:00:00Z","timestamp":1647475200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001807","name":"S\u00e3o Paulo Research Foundation","doi-asserted-by":"publisher","award":["2018\/17353-7 to T.A.T.G. and 2015\/26207-6 to R.T.H."],"award-info":[{"award-number":["2018\/17353-7 to T.A.T.G. and 2015\/26207-6 to R.T.H."]}],"id":[{"id":"10.13039\/501100001807","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>(1) Background: Pathogenic Escherichia coli are divided into two groups: diarrheagenic (DEC) and extraintestinal pathogenic (ExPEC) E. coli. ExPEC causing urinary tract infections (UTIs) are termed uropathogenic E. coli (UPEC) and are the most common cause of UTIs worldwide. (2) Methods: Here, we characterized 112 UPEC in terms of phylogroup, serotype, the presence of virulence factor-encoding genes, and antimicrobial resistance. (3) Results: The majority of the isolates were assigned into the phylogroup B2 (41.07%), and the serogroups O6 (12.5%) and O25 (8.9%) were the most frequent. Five hybrid UPEC (4.5%), with markers from two DEC pathotypes, i.e., atypical enteropathogenic (aEPEC) and enteroaggregative (EAEC) E. coli, were identified, and designated UPEC\/aEPEC (one isolate) and UPEC\/EAEC (four isolates), respectively. Three UPEC\/EAEC harbored genes from the pap operon, and the UPEC\/aEPEC carried ibeA. The highest resistance rates were observed for ampicillin (46.4%) and trimethoprim\/sulfamethoxazole (34.8%), while 99.1% of the isolates were susceptible to nitrofurantoin and\/or fosfomycin. Moreover, 9.8% of the isolates were identified as Extended Spectrum \u03b2-Lactamase producers, including one hybrid UPEC\/EAEC. (4) Conclusion: Our data reinforce that hybrid UPEC\/DEC are circulating in the city of Botucatu, Brazil, as uropathogens. However, how and whether these combinations of genes influence their pathogenicity is a question that remains to be elucidated.<\/jats:p>","DOI":"10.3390\/microorganisms10030645","type":"journal-article","created":{"date-parts":[[2022,3,20]],"date-time":"2022-03-20T21:34:27Z","timestamp":1647812067000},"page":"645","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":35,"title":["Characterization of Uropathogenic Escherichia coli Reveals Hybrid Isolates of Uropathogenic and Diarrheagenic (UPEC\/DEC) E. coli"],"prefix":"10.3390","volume":"10","author":[{"given":"Rodrigo H. S.","family":"Tanabe","sequence":"first","affiliation":[{"name":"Departamento de Ci\u00eancias Qu\u00edmicas e Biol\u00f3gicas (Setor de Microbiologia e Imunologia), Instituto de Bioci\u00eancias, Universidade Estadual Paulista (UNESP), Botucatu 18618-689, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Regiane C. B.","family":"Dias","sequence":"additional","affiliation":[{"name":"Departamento de Ci\u00eancias Qu\u00edmicas e Biol\u00f3gicas (Setor de Microbiologia e Imunologia), Instituto de Bioci\u00eancias, Universidade Estadual Paulista (UNESP), Botucatu 18618-689, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Henrique","family":"Orsi","sequence":"additional","affiliation":[{"name":"Departamento de Ci\u00eancias Qu\u00edmicas e Biol\u00f3gicas (Setor de Microbiologia e Imunologia), Instituto de Bioci\u00eancias, Universidade Estadual Paulista (UNESP), Botucatu 18618-689, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3019-0629","authenticated-orcid":false,"given":"Daiany R. P.","family":"de Lira","sequence":"additional","affiliation":[{"name":"Departamento de Ci\u00eancias Qu\u00edmicas e Biol\u00f3gicas (Setor de Microbiologia e Imunologia), Instituto de Bioci\u00eancias, Universidade Estadual Paulista (UNESP), Botucatu 18618-689, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melissa A.","family":"Vieira","sequence":"additional","affiliation":[{"name":"Departamento de Ci\u00eancias Qu\u00edmicas e Biol\u00f3gicas (Setor de Microbiologia e Imunologia), Instituto de Bioci\u00eancias, Universidade Estadual Paulista (UNESP), Botucatu 18618-689, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6158-5247","authenticated-orcid":false,"given":"Lu\u00eds F.","family":"dos Santos","sequence":"additional","affiliation":[{"name":"Centro de Bacteriologia, Instituto Adolfo Lutz, S\u00e3o Paulo 01246-902, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adriano M.","family":"Ferreira","sequence":"additional","affiliation":[{"name":"Hospital das Cl\u00ednicas da Faculdade de Medicina de Botucatu, Botucatu 18607-741, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vera L. M.","family":"Rall","sequence":"additional","affiliation":[{"name":"Departamento de Ci\u00eancias Qu\u00edmicas e Biol\u00f3gicas (Setor de Microbiologia e Imunologia), Instituto de Bioci\u00eancias, Universidade Estadual Paulista (UNESP), Botucatu 18618-689, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alessandro L.","family":"Mondelli","sequence":"additional","affiliation":[{"name":"Departamento de Cl\u00ednica M\u00e9dica, Faculdade de Medicina, Universidade Estadual Paulista (UNESP), Botucatu 18618-970, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4525-8705","authenticated-orcid":false,"given":"T\u00e2nia A. T.","family":"Gomes","sequence":"additional","affiliation":[{"name":"Departamento de Microbiologia, Imunologia e Parasitologia, Universidade Federal de S\u00e3o Paulo-Escola Paulista de Medicina (UNIFESP-EPM), S\u00e3o Paulo 04023-062, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6834-0085","authenticated-orcid":false,"given":"Carlos H.","family":"Camargo","sequence":"additional","affiliation":[{"name":"Centro de Bacteriologia, Instituto Adolfo Lutz, S\u00e3o Paulo 01246-902, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6695-6003","authenticated-orcid":false,"given":"Rodrigo T.","family":"Hernandes","sequence":"additional","affiliation":[{"name":"Departamento de Ci\u00eancias Qu\u00edmicas e Biol\u00f3gicas (Setor de Microbiologia e Imunologia), Instituto de Bioci\u00eancias, Universidade Estadual Paulista (UNESP), Botucatu 18618-689, SP, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,3,17]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1128\/CMR.11.1.142","article-title":"Diarrheagenic Escherichia coli","volume":"11","author":"Nataro","year":"1998","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1038\/nrmicro818","article-title":"Pathogenic Escherichia coli","volume":"2","author":"Kaper","year":"2004","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1128\/CMR.00022-13","article-title":"Recent Advances in Understanding Enteric Pathogenic Escherichia coli","volume":"26","author":"Croxen","year":"2013","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"4196","DOI":"10.1093\/nar\/26.18.4196","article-title":"The Complete DNA Sequence and Analysis of the Large Virulence Plasmid of Escherichia coli O157:H7","volume":"26","author":"Burland","year":"1998","journal-title":"Nucleic Acids Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1038\/35054089","article-title":"Genome Sequence of Enterohaemorrhagic Escherichia coli O157:H7","volume":"409","author":"Perna","year":"2001","journal-title":"Nature"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"17020","DOI":"10.1073\/pnas.252529799","article-title":"Extensive Mosaic Structure Revealed by the Complete Genome Sequence of Uropathogenic Escherichia coli","volume":"99","author":"Welch","year":"2002","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1128\/JB.01238-08","article-title":"Complete Genome Sequence and Comparative Genome Analysis of Enteropathogenic Escherichia coli O127:H6 Strain E2348\/69","volume":"191","author":"Iguchi","year":"2009","journal-title":"J. Bacteriol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Chaudhuri, R.R., Sebaihia, M., Hobman, J.L., Webber, M.A., Leyton, D.L., Goldberg, M.D., Cunningham, A.F., Scott-Tucker, A., Ferguson, P.R., and Thomas, C.M. (2010). Complete Genome Sequence and Comparative Metabolic Profiling of the Prototypical Enteroaggregative Escherichia coli Strain 042. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0008801"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2262","DOI":"10.3201\/eid2412.180272","article-title":"Emerging Multidrug-Resistant Hybrid Pathotype Shiga Toxin\u2013Producing Escherichia coli O80 and Related Strains of Clonal Complex 165, Europe","volume":"24","author":"Cointe","year":"2018","journal-title":"Emerg. Infect. Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1753","DOI":"10.1086\/315418","article-title":"Proposal for a New Inclusive Designation for Extraintestinal Pathogenic Isolates of Escherichia coli: ExPEC","volume":"181","author":"Russo","year":"2000","journal-title":"J. Infect. Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1111\/j.1574-6968.2009.01664.x","article-title":"An Overview of Atypical Enteropathogenic Escherichia coli","volume":"297","author":"Hernandes","year":"2009","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1017\/S0950268818002595","article-title":"Diarrhoeagenic Escherichia coli and Escherichia albertii in Brazil: Pathotypes and Serotypes over a 6-Year Period of Surveillance","volume":"147","author":"Ori","year":"2019","journal-title":"Epidemiol. Infect."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Lima, A.A.M., Oliveira, D.B., Quetz, J.S., Havt, A., Prata, M.M.G., Lima, I.F.N., Soares, A.M., Filho, J.Q., Lima, N.L., and Medeiros, P.H.Q.S. (2019). Etiology and Severity of Diarrheal Diseases in Infants at the Semiarid Region of Brazil: A Case-Control Study. PLoS Negl. Trop. Dis., 13.","DOI":"10.1371\/journal.pntd.0007154"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/S0140-6736(13)60844-2","article-title":"Burden and Aetiology of Diarrhoeal Disease in Infants and Young Children in Developing Countries (the Global Enteric Multicenter Study, GEMS): A Prospective, Case-Control Study","volume":"382","author":"Kotloff","year":"2013","journal-title":"Lancet"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"3396","DOI":"10.1128\/JCM.00084-07","article-title":"Typical Enteroaggregative and Atypical Enteropathogenic Types of Escherichia coli Are the Most Prevalent Diarrhea-Associated Pathotypes among Brazilian Children","volume":"45","author":"Araujo","year":"2007","journal-title":"J. Clin. Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1590\/S0074-02762007005000116","article-title":"Detection of Diarrheagenic Escherichia coli from Children with and without Diarrhea in Salvador, Bahia, Brazil","volume":"102","author":"Bueris","year":"2007","journal-title":"Mem. Inst. Oswaldo Cruz"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1111\/apm.12501","article-title":"Diarrheagenic Escherichia coli Pathotypes Investigation Revealed Atypical Enteropathogenic E. coli as Putative Emerging Diarrheal Agents in Children Living in Botucatu, S\u00e3o Paulo State, Brazil","volume":"124","author":"Dias","year":"2016","journal-title":"APMIS"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1111\/j.1574-695X.2008.00388.x","article-title":"Uropathogenic Escherichia coli (UPEC) Strains May Carry Virulence Properties of Diarrhoeagenic E. coli","volume":"52","author":"Abe","year":"2008","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3703","DOI":"10.1128\/JCM.01909-12","article-title":"Enteroaggregative Escherichia coli O78:H10, the Cause of an Outbreak of Urinary Tract Infection","volume":"50","author":"Olesen","year":"2012","journal-title":"J. Clin. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"146","DOI":"10.3389\/fmicb.2017.00146","article-title":"Virulence Markers and Phylogenetic Analysis of Escherichia coli Strains with Hybrid EAEC\/UPEC Genotypes Recovered from Sporadic Cases of Extraintestinal Infections","volume":"8","author":"Lara","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e00353-20","DOI":"10.1128\/mBio.00353-20","article-title":"Emergence of Enteroaggregative Escherichia coli within the ST131 Lineage as a Cause of Extraintestinal Infections","volume":"11","author":"Boll","year":"2020","journal-title":"MBio"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Mandomando, I., Vubil, D., Boisen, N., Quint\u00f3, L., Ruiz, J., Siga\u00faque, B., Nhampossa, T., Garrine, M., Massora, S., and Aide, P. (2020). Escherichia coli ST131 Clones Harbouring AggR and AAF\/V Fimbriae Causing Bacteremia in Mozambican Children: Emergence of New Variant of fimH27 Subclone. PLoS Negl. Trop. Dis., 14.","DOI":"10.1371\/journal.pntd.0008274"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1038\/nrurol.2010.190","article-title":"The Epidemiology of Urinary Tract Infection","volume":"7","author":"Foxman","year":"2010","journal-title":"Nat. Rev. Urol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1038\/nrurol.2010.101","article-title":"Host\u2013Pathogen Interactions in Urinary Tract Infection","volume":"7","author":"Nielubowicz","year":"2010","journal-title":"Nat. Rev. Urol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1128\/microbiolspec.UTI-0015-2012","article-title":"Virulence and Fitness Determinants of Uropathogenic Escherichia coli","volume":"3","author":"Subashchandrabose","year":"2015","journal-title":"Microbiol. Spectr."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"6365","DOI":"10.1128\/IAI.70.11.6365-6372.2002","article-title":"Genetic Structure and Distribution of Four Pathogenicity Islands (PAI I536 to PAI IV536) of Uropathogenic Escherichia coli Strain 536","volume":"70","author":"Dobrindt","year":"2002","journal-title":"Infect. Immun."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"3532","DOI":"10.1128\/JB.01744-06","article-title":"Defining Genomic Islands and Uropathogen-Specific Genes in Uropathogenic Escherichia coli","volume":"189","author":"Lloyd","year":"2007","journal-title":"J. Bacteriol."},{"key":"ref_28","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_29","doi-asserted-by":"crossref","first-page":"3107","DOI":"10.1111\/1462-2920.14713","article-title":"Characterization and Rapid Identification of Phylogroup G in Escherichia coli, a Lineage with High Virulence and Antibiotic Resistance Potential","volume":"21","author":"Clermont","year":"2019","journal-title":"Environ. Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1038\/s41579-020-0416-x","article-title":"The Population Genetics of Pathogenic Escherichia coli","volume":"19","author":"Denamur","year":"2021","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"243","DOI":"10.3389\/fmicb.2018.00243","article-title":"Comprehensive Molecular Characterization of Escherichia coli Isolates from Urine Samples of Hospitalized Patients in Rio de Janeiro, Brazil","volume":"9","author":"Campos","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Flament-Simon, S.-C., Nicolas-Chanoine, M.-H., Garc\u00eda, V., Duprilot, M., Mayer, N., Alonso, M.P., Garc\u00eda-Meni\u00f1o, I., Blanco, J.E., Blanco, M., and Blanco, J. (2020). Clonal Structure, Virulence Factor-Encoding Genes and Antibiotic Resistance of Escherichia coli, Causing Urinary Tract Infections and Other Extraintestinal Infections in Humans in Spain and France during 2016. Antibiotics, 9.","DOI":"10.20944\/preprints202002.0463.v1"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1128\/microbiolspec.BAI-0014-2019","article-title":"Reaching the End of the Line: Urinary Tract Infections","volume":"7","author":"Tamadonfar","year":"2019","journal-title":"Microbiol. Spectr."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jgar.2016.02.003","article-title":"Multidrug Resistance Dissemination by Extended-Spectrum \u03b2-Lactamase-Producing Escherichia coli Causing Community-Acquired Urinary Tract Infection in the Central-Western Region, Brazil","volume":"6","year":"2016","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"104452","DOI":"10.1016\/j.meegid.2020.104452","article-title":"Prevalence of Fluoroquinolone-Resistant and Broad-Spectrum Cephalosporin-Resistant Community-Acquired Urinary Tract Infections in Rio de Janeiro: Impact of Escherichia coli Genotypes ST69 and ST131","volume":"85","author":"Longo","year":"2020","journal-title":"Infect. Genet. Evol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1330","DOI":"10.1099\/jmm.0.001043","article-title":"Characterization of Escherichia coli Obtained from Patients Undergoing Peritoneal Dialysis and Diagnosed with Peritonitis in a Brazilian Centre","volume":"68","author":"Dias","year":"2019","journal-title":"J. Med. Microbiol."},{"key":"ref_37","unstructured":"Ewing, W.H. (1986). Edwards and Ewing\u2019s Identification of Enterobacteriaceae, Elsevier Science Publishing. [4th ed.]."},{"key":"ref_38","unstructured":"CLSI (2020). Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute. [30th ed.]. CLSI Supplement M100."},{"key":"ref_39","unstructured":"CLSI (2015). Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute. [25th ed.]. CLSI Supplement M100-S25."},{"key":"ref_40","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_41","doi-asserted-by":"crossref","first-page":"1429","DOI":"10.1099\/jmm.0.000594","article-title":"Clonality, Virulence and Antimicrobial Resistance of Enteroaggregative Escherichia coli from Mirzapur, Bangladesh","volume":"66","author":"Chattaway","year":"2017","journal-title":"J. Med. Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2334","DOI":"10.3389\/fmicb.2017.02334","article-title":"Clonal Diversity, Virulence Potential and Antimicrobial Resistance of Escherichia coli Causing Community Acquired Urinary Tract Infection in Switzerland","volume":"8","author":"Baschera","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Dadi, B.R., Abebe, T., Zhang, L., Mihret, A., Abebe, W., and Amogne, W. (2020). Distribution of Virulence Genes and Phylogenetics of Uropathogenic Escherichia coli among Urinary Tract Infection Patients in Addis Ababa, Ethiopia. BMC Infect. Dis., 20.","DOI":"10.1186\/s12879-020-4844-z"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1007\/s12088-011-0175-5","article-title":"Distribution of Pathogenic Genes aatA, aap, aggR, among Uropathogenic Escherichia coli (UPEC) and Their Linkage with StbA Gene","volume":"51","author":"Nazemi","year":"2011","journal-title":"Indian J. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1128\/JCM.02069-13","article-title":"Characterization of Escherichia coli Isolates from Hospital Inpatients or Outpatients with Urinary Tract Infection","volume":"52","author":"Toval","year":"2014","journal-title":"J. Clin. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/JCM.01309-19","article-title":"Origin and Evolution of Hybrid Shiga Toxin-Producing and Uropathogenic Escherichia coli Strains of Sequence Type 141","volume":"58","author":"Gati","year":"2019","journal-title":"J. Clin. Microbiol."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Nascimento, J.A.S., Santos, F.F., Valiatti, T.B., Santos-Neto, J.F., Santos, A.C.M., Cay\u00f4, R., Gales, A.C., and Gomes, T.A.T. (2021). Frequency and Diversity of Hybrid Escherichia coli Strains Isolated from Urinary Tract Infections. Microorganisms, 9.","DOI":"10.3390\/microorganisms9040693"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1016\/j.ijmm.2005.06.009","article-title":"Enterohaemorrhagic Escherichia coli in Human Medicine","volume":"295","author":"Karch","year":"2005","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1002\/emmm.201303133","article-title":"Heteropathogenic Virulence and Phylogeny Reveal Phased Pathogenic Metamorphosis in Escherichia coli O2:H6","volume":"6","author":"Bielaszewska","year":"2014","journal-title":"EMBO Mol. Med."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"4631","DOI":"10.1128\/IAI.01701-14","article-title":"Characterization of Urinary Tract Infection-Associated Shiga Toxin-Producing Escherichia coli","volume":"82","author":"Toval","year":"2014","journal-title":"Infect. Immun."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1664","DOI":"10.1073\/pnas.92.5.1664","article-title":"A Genetic Locus of Enterocyte Effacement Conserved among Diverse Enterobacterial Pathogens","volume":"92","author":"McDaniel","year":"1995","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1340","DOI":"10.1128\/iai.41.3.1340-1351.1983","article-title":"Attaching and Effacing Activities of Rabbit and Human Enteropathogenic Escherichia coli in Pig and Rabbit Intestines","volume":"41","author":"Moon","year":"1983","journal-title":"Infect. Immun."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1290","DOI":"10.1128\/iai.57.4.1290-1298.1989","article-title":"Actin Accumulation at Sites of Bacterial Adhesion to Tissue Culture Cells: Basis of a New Diagnostic Test for Enteropathogenic and Enterohemorrhagic Escherichia coli","volume":"57","author":"Knutton","year":"1989","journal-title":"Infect. Immun."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"492","DOI":"10.3389\/fcimb.2020.00492","article-title":"Genetic and Virulence Characteristics of a Hybrid Atypical Enteropathogenic and Uropathogenic Escherichia coli (aEPEC\/UPEC) Strain","volume":"10","author":"Valiatti","year":"2020","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1007\/s101420100039","article-title":"A Novel Genetic Island of Meningitic Escherichia coli K1 Containing the ibeA Invasion Gene (GimA): Functional Annotation and Carbon-Source-Regulated Invasion of Human Brain Microvascular Endothelial Cells","volume":"1","author":"Huang","year":"2001","journal-title":"Funct. Integr. Genom."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"339","DOI":"10.3389\/fcimb.2020.00339","article-title":"Diversity of Hybrid- and Hetero-Pathogenic Escherichia coli and Their Potential Implication in More Severe Diseases","volume":"10","author":"Santos","year":"2020","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"998","DOI":"10.1099\/jmm.0.000313","article-title":"Atypical Enteropathogenic Escherichia coli as Aetiologic Agents of Sporadic and Outbreak-Associated Diarrhoea in Brazil","volume":"65","author":"Vieira","year":"2016","journal-title":"J. Med. Microbiol."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Hernandes, R.T., Hazen, T.H., dos Santos, L.F., Richter, T.K.S., Michalski, J.M., and Rasko, D.A. (2020). Comparative Genomic Analysis Provides Insight into the Phylogeny and Virulence of Atypical Enteropathogenic Escherichia coli Strains from Brazil. PLoS Negl. Trop. Dis., 14.","DOI":"10.1371\/journal.pntd.0008373"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1097\/00006454-198709000-00008","article-title":"Patterns of Adherence of Diarrheagenic Escherichia coli to HEp-2 Cells","volume":"6","author":"Nataro","year":"1987","journal-title":"Pediatr. Infect. Dis. J."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1016\/j.bbapap.2016.11.017","article-title":"Structural and Functional Studies of Escherichia coli Aggregative Adherence Fimbriae (AAF\/V) Reveal a Deficiency in Extracellular Matrix Binding","volume":"1865","author":"Liu","year":"2017","journal-title":"Biochim. Biophys. Acta. Proteins Proteom."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Boisen, N., \u00d8sterlund, M.T., Joensen, K.G., Santiago, A.E., Mandomando, I., Cravioto, A., Chattaway, M.A., Gonyar, L.A., Overballe-Petersen, S., and Stine, O.C. (2020). Redefining Enteroaggregative Escherichia coli (EAEC): Genomic Characterization of Epidemiological EAEC Strains. PLoS Negl. Trop. Dis., 14.","DOI":"10.1371\/journal.pntd.0008613"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"614","DOI":"10.1128\/CMR.00112-13","article-title":"Epidemiology and Clinical Manifestations of Enteroaggregative Escherichia coli","volume":"27","author":"Olsen","year":"2014","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1164","DOI":"10.1128\/IAI.01376-12","article-title":"Role of Enteroaggregative Escherichia coli Virulence Factors in Uropathogenesis","volume":"81","author":"Boll","year":"2013","journal-title":"Infect. Immun."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1007\/s15010-013-0569-x","article-title":"Diarrheagenic Enteroaggregative Escherichia coli Causing Urinary Tract Infection and Bacteremia Leading to Sepsis","volume":"42","author":"Herzog","year":"2014","journal-title":"Infection"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/femspd\/ftx106","article-title":"Enteroaggregative Escherichia coli with Uropathogenic Characteristics Are Present in Feces of Diarrheic and Healthy Children","volume":"75","author":"Nunes","year":"2017","journal-title":"Pathog. Dis."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1058","DOI":"10.1128\/JCM.42.3.1058-1063.2004","article-title":"Enteroaggregative Escherichia coli Virulence Factors Are Found To Be Associated with Infantile Diarrhea in Brazil","volume":"42","author":"Zamboni","year":"2004","journal-title":"J. Clin. Microbiol."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Fran\u00e7a, F.L.S.S., Wells, T.J., Browning, D.F., Nogueira, R.T., Sarges, F.S., Pereira, A.C., Cunningham, A.F., Lucheze, K., Rosa, A.C.P., and Henderson, I.R. (2013). Genotypic and Phenotypic Characterisation of Enteroaggregative Escherichia coli from Children in Rio de Janeiro, Brazil. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0069971"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"144","DOI":"10.3389\/fcimb.2020.00144","article-title":"Analysis of the Virulence Profile and Phenotypic Features of Typical and Atypical Enteroaggregative Escherichia coli (EAEC) Isolated From Diarrheal Patients in Brazil","volume":"10","author":"Dias","year":"2020","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"2075","DOI":"10.1007\/s42770-021-00580-6","article-title":"Identification of a Hybrid Atypical Enteropathogenic and Enteroaggregative Escherichia coli (aEPEC\/EAEC) Clone of Serotype O3:H2 Associated with a Diarrheal Outbreak in Brazil","volume":"52","author":"Cavalcanti","year":"2021","journal-title":"Braz. J. Microbiol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"962","DOI":"10.1111\/1469-0691.12089","article-title":"Healthcare-Associated, Community-Acquired and Hospital-Acquired Bacteraemic Urinary Tract Infections in Hospitalized Patients: A Prospective Multicentre Cohort Study in the Era of Antimicrobial Resistance","volume":"19","author":"Horcajada","year":"2013","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1016\/j.bjid.2020.04.002","article-title":"Joint Report of SBI (Brazilian Society of Infectious Diseases), FEBRASGO (Brazilian Federation of Gynecology and Obstetrics Associations), SBU (Brazilian Society of Urology) and SBPC\/ML (Brazilian Society of Clinical Pathology\/Laboratory Medicine): Recommendations for the clinical management of lower urinary tract infections in pregnant and non-pregnant women","volume":"24","author":"Cimerman","year":"2020","journal-title":"Braz. J. Infect. Dis."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1590\/0074-02760140389","article-title":"Widespread Distribution of CTX-M and Plasmid-Mediated AmpC \u03b2-Lactamases in Escherichia coli from Brazilian Chicken Meat","volume":"110","author":"Botelho","year":"2015","journal-title":"Mem. Inst. Oswaldo Cruz"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"e11726","DOI":"10.7717\/peerj.11726","article-title":"Enteroaggregative Escherichia coli Is Associated with Antibiotic Resistance and Urinary Tract Infection Symptomatology","volume":"9","year":"2021","journal-title":"PeerJ"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1086\/315217","article-title":"Extended Virulence Genotypes of Escherichia coli Strains from Patients with Urosepsis in Relation to Phylogeny and Host Compromise","volume":"181","author":"Johnson","year":"2000","journal-title":"J. Infect. Dis."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1189","DOI":"10.1128\/jcm.30.5.1189-1193.1992","article-title":"Rapid and Specific Detection of the pap, afa, and sfa Adhesin-Encoding Operons in Uropathogenic Escherichia coli Strains by Polymerase Chain Reaction","volume":"30","author":"Archambaud","year":"1992","journal-title":"J. Clin. Microbiol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"8391","DOI":"10.1128\/AEM.05376-11","article-title":"Fimbrial Adhesins Produced by Atypical Enteropathogenic Escherichia coli Strains","volume":"77","author":"Hernandes","year":"2011","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1016\/S0923-2508(02)01379-7","article-title":"Presence in Bovine Enteropathogenic (EPEC) and Enterohaemorrhagic (EHEC) Escherichia coli of Genes Encoding for Putative Adhesins of Human EHEC Strains","volume":"153","author":"Szalo","year":"2002","journal-title":"Res. Microbiol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/j.ijmm.2007.01.003","article-title":"Avian Pathogenic, Uropathogenic, and Newborn Meningitis-Causing Escherichia coli: How Closely Related Are They?","volume":"297","author":"Ewers","year":"2007","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1111\/j.1574-695X.1995.tb00179.x","article-title":"Detection of Urovirulence Factors in Escherichia coli by Multiplex Polymerase Chain Reaction","volume":"12","author":"Yamamoto","year":"1995","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Tennant, S.M., Tauschek, M., Azzopardi, K., Bigham, A., Bennett-Wood, V., Hartland, E.L., Qi, W., Whittam, T.S., and Robins-Browne, R.M. (2009). Characterisation of Atypical Enteropathogenic E. coli Strains of Clinical Origin. BMC Microbiol., 9.","DOI":"10.1186\/1471-2180-9-117"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"294","DOI":"10.4269\/ajtmh.2009.80.294","article-title":"High Prevalence of Serine Protease Autotransporter Cytotoxins among Strains of Enteroaggregative Escherichia coli","volume":"80","author":"Boisen","year":"2009","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1186\/1476-0711-12-8","article-title":"Uropathogenic Escherichia coli in Iran: Serogroup Distributions, Virulence Factors and Antimicrobial Resistance Properties","volume":"12","author":"Momtaz","year":"2013","journal-title":"Ann. Clin. Microbiol. Antimicrob."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/S0378-1097(03)00862-0","article-title":"PicU, a Second Serine Protease Autotransporter of Uropathogenic Escherichia coli","volume":"230","author":"Parham","year":"2004","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.vetmic.2004.09.008","article-title":"Molecular Epidemiology of Avian Pathogenic Escherichia coli (APEC) Isolated from Colisepticemia in Poultry","volume":"104","author":"Ewers","year":"2004","journal-title":"Vet. Microbiol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1128\/JB.188.2.745-758.2006","article-title":"DNA Sequence of a ColV Plasmid and Prevalence of Selected Plasmid-Encoded Virulence Genes among Avian Escherichia coli Strains","volume":"188","author":"Johnson","year":"2006","journal-title":"J. Bacteriol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"3040","DOI":"10.1128\/IAI.68.5.3040-3047.2000","article-title":"Molecular Epidemiological and Phylogenetic Associations of Two Novel Putative Virulence Genes, iha and iroNE. coli, among Escherichia coli Isolates from Patients with Urosepsis","volume":"68","author":"Johnson","year":"2000","journal-title":"Infect. Immun."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"2692","DOI":"10.1128\/IAI.67.6.2692-2699.1999","article-title":"Phylogenetic Analysis of Enteroaggregative and Diffusely Adherent Escherichia coli","volume":"67","author":"Czeczulin","year":"1999","journal-title":"Infect. Immun."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"1375","DOI":"10.1128\/JCM.41.4.1375-1385.2003","article-title":"Presence and Characterization of Extraintestinal Pathogenic Escherichia coli Virulence Genes in F165-Positive E. coli Strains Isolated from Diseased Calves and Pigs","volume":"41","author":"Dezfulian","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1051\/vetres:2004057","article-title":"Characterizing the APEC Pathotype","volume":"36","author":"Giddings","year":"2005","journal-title":"Vet. Res."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"3327","DOI":"10.1128\/IAI.68.6.3327-3336.2000","article-title":"Evidence of Commonality between Canine and Human Extraintestinal Pathogenic Escherichia coli Strains That Express PapG Allele III","volume":"68","author":"Johnson","year":"2000","journal-title":"Infect. Immun."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1637\/7293-102604R","article-title":"Rapid Detection of Virulence-Associated Genes in Avian Pathogenic Escherichia coli by Multiplex Polymerase Chain Reaction","volume":"49","author":"Ewers","year":"2005","journal-title":"Avian Dis."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"3793","DOI":"10.1128\/IAI.00620-13","article-title":"Dissection of the Role of Pili and Type 2 and 3 Secretion Systems in Adherence and Biofilm Formation of an Atypical Enteropathogenic Escherichia coli Strain","volume":"81","author":"Hernandes","year":"2013","journal-title":"Infect. Immun."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"3380","DOI":"10.1128\/AEM.02855-06","article-title":"Identification of Unconventional Intestinal Pathogenic Escherichia coli Isolates Expressing Intermediate Virulence Factor Profiles by Using a Novel Single-Step Multiplex PCR","volume":"73","author":"Greune","year":"2007","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1111\/j.1348-0421.1996.tb01078.x","article-title":"Typing of Verotoxins by DNA Colony Hybridization with Poly- and Oligonucleotide Probes, a Bead-Enzyme-Linked Immunosorbent Assay, and Polymerase Chain Reaction","volume":"40","author":"Yamasaki","year":"1996","journal-title":"Microbiol. Immunol."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1128\/jcm.33.3.701-705.1995","article-title":"Development of PCR for Screening of Enteroaggregative Escherichia coli","volume":"33","author":"Schmidt","year":"1995","journal-title":"J. Clin. Microbiol."},{"key":"ref_96","first-page":"211","article-title":"Investigation on Enteroaggregative Escherichia coli Infection by Multiplex PCR","volume":"39","author":"Ratchtrachenchai","year":"1997","journal-title":"Bull. Dep. Med. Sci."},{"key":"ref_97","first-page":"53","article-title":"A Preliminary Survey of Extended-Spectrum \u03b2-Lactamases (ESBLs) in Clinical Isolates of Klebsiella Pneumoniae and Escherichia coli in Japan","volume":"184","author":"Yagi","year":"2000","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"4263","DOI":"10.1128\/AAC.48.11.4263-4270.2004","article-title":"Infections with Nontyphoidal Salmonella Species Producing TEM-63 or a Novel TEM Enzyme, TEM-131, in South Africa","volume":"48","author":"Kruger","year":"2004","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"1790","DOI":"10.1128\/AAC.01440-07","article-title":"Multiclonal Outbreak of Klebsiella Pneumoniae Producing Extended-Spectrum \u03b2-Lactamase CTX-M-2 and Novel Variant CTX-M-59 in a Neonatal Intensive Care Unit in Brazil","volume":"52","author":"Doi","year":"2008","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"580","DOI":"10.1089\/mdr.2016.0085","article-title":"Prevalence of Extended-Spectrum \u03b2-Lactamases CTX-M-8 and CTX-M-2-Producing Salmonella Serotypes from Clinical and Nonhuman Isolates in Brazil","volume":"23","author":"Fernandes","year":"2017","journal-title":"Microb. Drug Resist."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"5715","DOI":"10.1128\/JCM.42.12.5715-5721.2004","article-title":"Phenotypic and Molecular Detection of CTX-M-\u03b2-Lactamases Produced by Escherichia coli and Klebsiella Spp.","volume":"42","author":"Pitout","year":"2004","journal-title":"J. Clin. Microbiol."},{"key":"ref_102","first-page":"182","article-title":"Plasmid-Encoded AmpC (pAmpC) in Enterobacteriaceae: Epidemiology of Microorganisms and Resistance Markers","volume":"44","author":"Cejas","year":"2012","journal-title":"Rev. Argent. Microbiol."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/10\/3\/645\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:38:21Z","timestamp":1760135901000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/10\/3\/645"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,3,17]]},"references-count":102,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2022,3]]}},"alternative-id":["microorganisms10030645"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms10030645","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,3,17]]}}}