{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,3]],"date-time":"2026-11-03T20:05:38Z","timestamp":1793736338838,"version":"4.6.1"},"reference-count":66,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,8,4]],"date-time":"2021-08-04T00:00:00Z","timestamp":1628035200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,8,4]],"date-time":"2021-08-04T00:00:00Z","timestamp":1628035200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"ACEPHEM","award":["-"],"award-info":[{"award-number":["-"]}]},{"name":"MLW-Core training","award":["206545\/Z\/17\/Z"],"award-info":[{"award-number":["206545\/Z\/17\/Z"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Infect Dis"],"published-print":{"date-parts":[[2021,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>\n                      Uropathogenic\n                      <jats:italic>Escherichia coli<\/jats:italic>\n                      (UPEC) are amongst the most frequent causes of urinary tract infections. We report a systematic review and meta-analysis of virulence factors and antimicrobial resistance of UPEC isolated from urinary tract infections.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>\n                      A systematic review and meta-analysis were performed using PRISMA guidelines (Research Registry ref. 5874). Data were extracted from PubMed\/MEDLINE and ScienceDirect databases for studies published from January 1, 2000 to December 31, 2019. Studies reporting antimicrobial resistance and virulence factors of UPEC isolated in confirmed urinary tract infections (\u226510\n                      <jats:sup>5<\/jats:sup>\n                      CFU\/ml) were eligible. Prevalence of antimicrobial resistance and virulence factors of UPEC were estimated using random-effects meta-analysis model. Estimates with 95% confidence intervals, I-square (\n                      <jats:italic>I<\/jats:italic>\n                      <jats:sup>2<\/jats:sup>\n                      ) statistic, and Cochran\u2019s Q test were computed using the score statistic and the exact binomial method by incorporating the Freeman-Tukey double arcsine transformation of proportions.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      Our search returned 2504 hits, of which 13 studies were included in the meta-analysis, totalling 1888 UPEC isolates. Highest antimicrobial resistance rates were observed among the antibiotic class of tetracycline in 69.1% (498\/721), followed by sulphonamides in 59.3% (1119\/1888), quinolones in 49.4% (1956\/3956), and beta-lactams in 36.9% (4410\/11964). Among beta-lactams, high resistance was observed in aminopenicillins in 74.3% (1157\/1557) and first generation cephalosporins in 38.8% (370\/953). Meanwhile, virulence factors with highest prevalence were immune suppressors (54.1%) followed by adhesins (45.9%). Taken individually, the most observed virulence genes were\n                      <jats:italic>shiA<\/jats:italic>\n                      (92.1%),\n                      <jats:italic>CSH<\/jats:italic>\n                      (80.0%),\n                      <jats:italic>fimH\/MSHA<\/jats:italic>\n                      (75.3%),\n                      <jats:italic>traT<\/jats:italic>\n                      (75.1%),\n                      <jats:italic>sisA<\/jats:italic>\n                      (72.2%),\n                      <jats:italic>iucD<\/jats:italic>\n                      (65.7%),\n                      <jats:italic>iutA<\/jats:italic>\n                      (61.8%),\n                      <jats:italic>kpsMTII<\/jats:italic>\n                      (60.6%), and\n                      <jats:italic>PAI<\/jats:italic>\n                      (55.2%).\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>The increased antibiotic resistance of UPEC isolates was demonstrated and suggested a need for reassessment of empirical therapies in urinary tract infections treatment caused by this pathogen. In addition, this pathotype exhibited diverse surface and secreted virulence factors.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s12879-021-06435-7","type":"journal-article","created":{"date-parts":[[2021,8,4]],"date-time":"2021-08-04T05:03:05Z","timestamp":1628053385000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":126,"title":["Virulence factors and antimicrobial resistance of uropathogenic Escherichia coli (UPEC) isolated from urinary tract infections: a systematic review and meta-analysis"],"prefix":"10.1186","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6368-7127","authenticated-orcid":false,"given":"Gabriel Kambale","family":"Bunduki","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eva","family":"Heinz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vincent Samuel","family":"Phiri","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patrick","family":"Noah","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicholas","family":"Feasey","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Janelisa","family":"Musaya","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,8,4]]},"reference":[{"key":"6435_CR1","doi-asserted-by":"publisher","first-page":"1566","DOI":"10.3389\/fmicb.2017.01566","volume":"8","author":"ME Terlizzi","year":"2017","unstructured":"Terlizzi ME, Gribaudo G, Maffei ME. UroPathogenic Escherichia coli (UPEC) infections : virulence factors, bladder responses, antibiotic and non-antibiotic antimicrobial strategies. Front Microbiol. 2017;8:1566. https:\/\/doi.org\/10.3389\/fmicb.2017.01566.","journal-title":"Front Microbiol"},{"issue":"1","key":"6435_CR2","doi-asserted-by":"publisher","first-page":"118","DOI":"10.1186\/s13756-018-0411-4","volume":"7","author":"M Raeispour","year":"2018","unstructured":"Raeispour M, Ranjbar R. Antibiotic resistance , virulence factors and genotyping of Uropathogenic Escherichia coli strains. Antimicrob Resist Infect Control. 2018;7(1):118. https:\/\/doi.org\/10.1186\/s13756-018-0411-4.","journal-title":"Antimicrob Resist Infect Control"},{"key":"6435_CR3","doi-asserted-by":"publisher","unstructured":"Bien J, Sokolova O, Bozko P. Role of uropathogenic Escherichia coli virulence factors in development of urinary tract infection and kidney damage. Int J Nephrol. 2012:681473. https:\/\/doi.org\/10.1155\/2012\/687473.","DOI":"10.1155\/2012\/687473"},{"issue":"8","key":"6435_CR4","doi-asserted-by":"publisher","first-page":"828","DOI":"10.1099\/jmm.0.000104","volume":"64","author":"V Calhau","year":"2015","unstructured":"Calhau V, Domingues S, Mendonc N, Jorge G, Silva D, Jorge G, et al. Interplay between pathogenicity island carriage, resistance profile and plasmid acquisition in uropathogenic Escherichia coli. J Med Microbiol. 2015;64(8):828\u201335. https:\/\/doi.org\/10.1099\/jmm.0.000104.","journal-title":"J Med Microbiol"},{"issue":"4","key":"6435_CR5","doi-asserted-by":"publisher","first-page":"e00088","DOI":"10.1128\/CMR.00088-17","volume":"31","author":"SR Partridge","year":"2018","unstructured":"Partridge SR, Kwong SM, Firth N, Jensen SO. Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev. 2018;31(4):e00088\u201317.","journal-title":"Clin Microbiol Rev"},{"issue":"6","key":"6435_CR6","doi-asserted-by":"publisher","first-page":"565","DOI":"10.1097\/00001574-200411000-00011","volume":"20","author":"F Yan","year":"2004","unstructured":"Yan F, Polk DB. Commensal bacteria in the gut: learning who our friends are. Curr Opin Gastroenterol. 2004;20(6):565\u201371. https:\/\/doi.org\/10.1097\/00001574-200411000-00011.","journal-title":"Curr Opin Gastroenterol"},{"issue":"2","key":"6435_CR7","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1038\/nrmicro818","volume":"2","author":"JB Kaper","year":"2004","unstructured":"Kaper JB, Nataro JP, Mobley HLT. Pathogenic Escherichia coli. Nat Rev Microbiol. 2004;2(2):123\u201340. https:\/\/doi.org\/10.1038\/nrmicro818.","journal-title":"Nat Rev Microbiol"},{"issue":"5","key":"6435_CR8","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1038\/nrmicro3432","volume":"13","author":"AL Flores-Mireles","year":"2015","unstructured":"Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol. 2015;13(5):269\u201384. https:\/\/doi.org\/10.1038\/nrmicro3432.","journal-title":"Nat Rev Microbiol"},{"key":"6435_CR9","doi-asserted-by":"publisher","DOI":"10.1590\/0037-8682-0499-2018","volume":"52","author":"A\u00d6 D\u00fczg\u00fcn","year":"2019","unstructured":"D\u00fczg\u00fcn A\u00d6, Okumu\u015f F, Saral A, \u00c7i\u00e7ek A\u00c7, Cinemre S. Determination of antibiotic resistance genes and virulence factors in Escherichia coli isolated from Turkish patients with urinary tract infection. Rev Soc Bras Med Trop. 2019;52:e20180499. https:\/\/doi.org\/10.1590\/0037-8682-0499-2018.","journal-title":"Rev Soc Bras Med Trop"},{"issue":"1","key":"6435_CR10","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1186\/s13099-019-0290-0","volume":"11","author":"J Sarowska","year":"2019","unstructured":"Sarowska J, Futoma-Koloch B, Jama-Kmiecik A, Frej-Madrzak M, Ksiazczyk M, Bugla-Ploskonska G, et al. Virulence factors, prevalence and potential transmission of extraintestinal pathogenic Escherichia coli isolated from different sources: recent reports. Gut Pathog. 2019;11(1):10. https:\/\/doi.org\/10.1186\/s13099-019-0290-0.","journal-title":"Gut Pathog"},{"issue":"1","key":"6435_CR11","doi-asserted-by":"publisher","first-page":"224","DOI":"10.1186\/s12879-015-0974-0","volume":"15","author":"R Ikram","year":"2015","unstructured":"Ikram R, Psutka R, Carter A, Priest P. An outbreak of multi-drug resistant Escherichia coli urinary tract infection in an elderly population: a case-control study of risk factors. BMC Infect Dis. 2015;15(1):224. https:\/\/doi.org\/10.1186\/s12879-015-0974-0.","journal-title":"BMC Infect Dis"},{"key":"6435_CR12","doi-asserted-by":"publisher","unstructured":"Lee DS, Lee SJ, Choe HS, Giacobbe DR. Community-acquired urinary tract infection by Escherichia coli in the era of antibiotic resistance. Biomed Res Int. 2018:7656752. https:\/\/doi.org\/10.1155\/2018\/7656752.","DOI":"10.1155\/2018\/7656752"},{"issue":"1","key":"6435_CR13","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1186\/s12941-018-0255-z","volume":"17","author":"MQ Alanazi","year":"2018","unstructured":"Alanazi MQ, Alqahtani FY, Aleanizy FS. An evaluation of E. coli in urinary tract infection in emergency department at KAMC in Riyadh, Saudi Arabia: retrospective study. Ann Clin Microbiol Antimicrob. 2018;17(1):3. https:\/\/doi.org\/10.1186\/s12941-018-0255-z.","journal-title":"Ann Clin Microbiol Antimicrob"},{"key":"6435_CR14","volume-title":"The review on antimicrobial resistance","author":"J O\u2019Neill","year":"2016","unstructured":"O\u2019Neill J. Tackling drug-reistant infections globally: final report and recommendations. In: The review on antimicrobial resistance; 2016."},{"issue":"7","key":"6435_CR15","doi-asserted-by":"publisher","first-page":"e1000097","DOI":"10.1371\/journal.pmed.1000097","volume":"6","author":"D Moher","year":"2009","unstructured":"Moher D, Liberati A, Tetzlaff J, Altman DG, Prisma-Group. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Plos Med. 2009;6(7):e1000097.","journal-title":"Plos Med"},{"issue":"12","key":"6435_CR16","doi-asserted-by":"publisher","first-page":"e1007457","DOI":"10.1371\/journal.ppat.1007457","volume":"14","author":"VP O\u2019Brien","year":"2018","unstructured":"O\u2019Brien VP, Dorsey DA, Hannan TJ, Hultgren SJ. Host restriction of Escherichia coli recurrent urinary tract infection occurs in a bacterial strain-specific manner. PLoS Pathoges. 2018;14(12):e1007457. https:\/\/doi.org\/10.1371\/journal.ppat.1007457.","journal-title":"PLoS Pathoges"},{"key":"6435_CR17","volume-title":"Urinary Tract Infection (Catheter-Associated Urinary Tract Infection [CAUTI] and Non-Catheter-Associated Urinary Tract Infection [ UTI ]) Events","author":"Centers for Disease Control and Prevention","year":"2020","unstructured":"Centers for Disease Control and Prevention. Urinary Tract Infection (Catheter-Associated Urinary Tract Infection [CAUTI] and Non-Catheter-Associated Urinary Tract Infection [ UTI ]) Events. 2020 [cited 2020 Feb 20]. Available from: http:\/\/www.cdc.gov\/nhsn\/PDFs\/pscManual\/7pscCAUTIcurrent.pdf"},{"issue":"1","key":"6435_CR18","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1186\/2049-3258-72-39","volume":"72","author":"VN Nyaga","year":"2014","unstructured":"Nyaga VN, Arbyn M, Aerts M. Metaprop: a Stata command to perform meta-analysis of binomial data. Arch Public Health. 2014;72(1):39. https:\/\/doi.org\/10.1186\/2049-3258-72-39.","journal-title":"Arch Public Health"},{"issue":"8","key":"6435_CR19","doi-asserted-by":"publisher","first-page":"897","DOI":"10.1016\/j.jclinepi.2014.03.003","volume":"67","author":"JP Hunter","year":"2014","unstructured":"Hunter JP, Saratzis A, Sutton AJ, Boucher RH, Sayers RD, Bown MH. In meta-analyses of proportion studies, funnel plots were found to be an inaccurate method of assessing publication bias. J Clin Epidemiol. 2014;67(8):897\u2013903. https:\/\/doi.org\/10.1016\/j.jclinepi.2014.03.003.","journal-title":"J Clin Epidemiol"},{"issue":"1","key":"6435_CR20","doi-asserted-by":"publisher","first-page":"361","DOI":"10.3906\/sag-1805-100","volume":"49","author":"H Ghazvini","year":"2019","unstructured":"Ghazvini H, Taheri K, Edalati E, Sedighi M, Mirkalantari S. Virulence factors and antimicrobial resistance in uropathogenic Escherichia coli strains isolated from cystitis and pyelonephritis. Turkish J Med Sci. 2019;49(1):361\u20137. https:\/\/doi.org\/10.3906\/sag-1805-100.","journal-title":"Turkish J Med Sci"},{"issue":"3","key":"6435_CR21","doi-asserted-by":"publisher","first-page":"e78063","DOI":"10.1371\/journal.pone.0018063","volume":"6","author":"S Jadhav","year":"2011","unstructured":"Jadhav S, Hussain A, Devi S, Kumar A, Parveen S, Gandham N, et al. Virulence characteristics and genetic affinities of multiple drug resistant uropathogenic Escherichia coli from a semi urban locality in India. PLoS One. 2011;6(3):e78063.","journal-title":"PLoS One"},{"issue":"6","key":"6435_CR22","doi-asserted-by":"publisher","first-page":"1908","DOI":"10.3906\/sag-1508-105","volume":"46","author":"B Kot","year":"2016","unstructured":"Kot B, Wicha J, Gru\u017cewska A, Piechota M, Wolska K, Obr\u0119bska M. Virulence factors, biofilm-forming ability, and antimicrobial resistance of urinary Escherichia coli strains isolated from hospitalized patients. Turkish J Med Sci. 2016;46(6):1908\u201314. https:\/\/doi.org\/10.3906\/sag-1508-105.","journal-title":"Turkish J Med Sci."},{"issue":"1","key":"6435_CR23","doi-asserted-by":"publisher","first-page":"572","DOI":"10.1186\/s12879-018-3467-0","volume":"18","author":"Y Malekzadegan","year":"2018","unstructured":"Malekzadegan Y, Khashei R, Sedigh Ebrahim-Saraie H, Jahanabadi Z. Distribution of virulence genes and their association with antimicrobial resistance among uropathogenic Escherichia coli isolates from Iranian patients. BMC Infect Dis. 2018;18(1):572. https:\/\/doi.org\/10.1186\/s12879-018-3467-0.","journal-title":"BMC Infect Dis"},{"issue":"7","key":"6435_CR24","doi-asserted-by":"publisher","first-page":"426","DOI":"10.1016\/j.eimc.2016.02.021","volume":"35","author":"LI Miranda-Estrada","year":"2017","unstructured":"Miranda-Estrada LI, Ru\u00edz-Rosas M, Molina-L\u00f3pez J, Parra-Rojas I, Gonz\u00e1lez-Villalobos E, Castro-Alarc\u00f3n N. Relationship between virulence factors, resistance to antibiotics and phylogenetic groups of uropathogenic Escherichia coli in two locations in Mexico. Enferm Infecc Microbiol Clin. 2017;35(7):426\u201333. https:\/\/doi.org\/10.1016\/j.eimc.2016.02.021.","journal-title":"Enferm Infecc Microbiol Clin"},{"issue":"2","key":"6435_CR25","doi-asserted-by":"publisher","first-page":"e17514","DOI":"10.5812\/jjm.17514","volume":"8","author":"F Neamati","year":"2015","unstructured":"Neamati F, Firoozeh F, Saffari M, Zibaei M. Virulence genes and antimicrobial resistance pattern in Uropathogenic Escherichia coli isolated from hospitalized patients in Kashan, Iran. Jundishapur J Microbiol. 2015;8(2):e17514. https:\/\/doi.org\/10.5812\/jjm.17514.","journal-title":"Jundishapur J Microbiol"},{"issue":"4","key":"6435_CR26","doi-asserted-by":"publisher","first-page":"4114","DOI":"10.4238\/2011.October.31.5","volume":"10","author":"FA Oliveira","year":"2011","unstructured":"Oliveira FA, Paludo KS, Arend LNVS, Farah SMSS, Pedrosa FO, Souza EM, et al. Virulence characteristics and antimicrobial susceptibility of uropathogenic Escherichia coli strains. Genet Mol Res. 2011;10(4):4114\u201325. https:\/\/doi.org\/10.4238\/2011.October.31.5.","journal-title":"Genet Mol Res"},{"issue":"1","key":"6435_CR27","doi-asserted-by":"publisher","first-page":"1","DOI":"10.4314\/ajid.v7i1.1","volume":"7","author":"FO Olorunmola","year":"2013","unstructured":"Olorunmola FO, Kolawole DO, Lamikanra A. Antibiotic resistance and virulence properties in escherichia coli strains from cases of urinary tract infections. Afr J Infect Dis. 2013;7(1):1\u20137. https:\/\/doi.org\/10.4314\/ajid.v7i1.1.","journal-title":"Afr J Infect Dis"},{"issue":"4","key":"6435_CR28","doi-asserted-by":"publisher","first-page":"648","DOI":"10.1016\/j.jksus.2018.03.009","volume":"31","author":"MAK Shakhatreh","year":"2019","unstructured":"Shakhatreh MAK, Swedan SF, Al-Odat MA, Khabour OF. Uropathogenic Escherichia coli (UPEC) in Jordan: prevalence of urovirulence genes and antibiotic resistance. J King Saud Univ Sci. 2019;31(4):648\u201352. https:\/\/doi.org\/10.1016\/j.jksus.2018.03.009.","journal-title":"J King Saud Univ Sci"},{"issue":"4","key":"6435_CR29","doi-asserted-by":"publisher","first-page":"261","DOI":"10.1016\/j.phrp.2015.08.002","volume":"6","author":"M Tabasi","year":"2015","unstructured":"Tabasi M, Asadi Karam MR, Habibi M, Yekaninejad MS, Bouzari S. Phenotypic assays to determine virulence factors of Uropathogenic Escherichia coli (UPEC) isolates and their correlation with antibiotic resistance pattern. Osong Public Heal Res Perspect. 2015;6(4):261\u20138. https:\/\/doi.org\/10.1016\/j.phrp.2015.08.002.","journal-title":"Osong Public Heal Res Perspect"},{"issue":"12","key":"6435_CR30","doi-asserted-by":"publisher","first-page":"799","DOI":"10.1038\/ja.2014.72","volume":"67","author":"Y Wang","year":"2014","unstructured":"Wang Y, Zhao S, Han L, Guo X, Chen M, Ni Y, et al. Drug resistance and virulence of uropathogenic Escherichia coli from Shanghai, China. J Antibiot (Tokyo). 2014;67(12):799\u2013805. https:\/\/doi.org\/10.1038\/ja.2014.72.","journal-title":"J Antibiot (Tokyo)"},{"issue":"10","key":"6435_CR31","doi-asserted-by":"publisher","first-page":"1682","DOI":"10.1086\/323810","volume":"33","author":"M Velasco","year":"2001","unstructured":"Velasco M, Horcajada JP, Moreno-martinez A, Vila J, Martinez A, Ruiz J, et al. Decreased invasive capacity of quinolone-resistant Escherichia coli in patients with urinary tract infections. Clin Infect Dis. 2001;33(10):1682\u2013386. https:\/\/doi.org\/10.1086\/323810.","journal-title":"Clin Infect Dis"},{"issue":"6","key":"6435_CR32","doi-asserted-by":"publisher","first-page":"1089","DOI":"10.1046\/j.1365-2958.1997.3101672.x","volume":"23","author":"J Hacker","year":"1997","unstructured":"Hacker J, Blum-Oehler G, Muhldorfer I, Tschape H. Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol. 1997;23(6):1089\u201397. https:\/\/doi.org\/10.1046\/j.1365-2958.1997.3101672.x.","journal-title":"Mol Microbiol"},{"issue":"7","key":"6435_CR33","doi-asserted-by":"publisher","first-page":"1039","DOI":"10.1086\/342955","volume":"186","author":"J Vila","year":"2002","unstructured":"Vila J, Simon K, Ruiz J, Horcajada JP, Velasco M, Barranco M, et al. Are quinolone-resistant uropathogenic Escherichia coli less virulent? J Infect Dis. 2002;186(7):1039\u201342. https:\/\/doi.org\/10.1086\/342955.","journal-title":"J Infect Dis"},{"issue":"1","key":"6435_CR34","doi-asserted-by":"publisher","first-page":"4828","DOI":"10.1038\/s41467-019-12823-0","volume":"10","author":"H Chung The","year":"2019","unstructured":"Chung The H, Boinett C, Pham Thanh D, Jenkins C, Weill FX, Howden BP, et al. Dissecting the molecular evolution of fluoroquinolone-resistant Shigella sonnei. Nat Commun. 2019;10(1):4828. https:\/\/doi.org\/10.1038\/s41467-019-12823-0.","journal-title":"Nat Commun"},{"issue":"5","key":"6435_CR35","doi-asserted-by":"publisher","first-page":"354","DOI":"10.4161\/viru.24498","volume":"4","author":"L-C Fortie","year":"2013","unstructured":"Fortie L-C, Sekulovic O. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence. 2013;4(5):354\u201365. https:\/\/doi.org\/10.4161\/viru.24498.","journal-title":"Virulence"},{"issue":"2","key":"6435_CR36","doi-asserted-by":"publisher","first-page":"649","DOI":"10.1128\/AAC.50.2.649-653.2006","volume":"50","author":"SM Soto","year":"2006","unstructured":"Soto SM, De Anta MTJ, Vila J. Quinolones induce partial or total loss of pathogenicity islands in uropathogenic Escherichia coli bt SOS-dependant or -independant pathways, respectively. Antimicrob Agents Chemother. 2006;50(2):649\u201353. https:\/\/doi.org\/10.1128\/AAC.50.2.649-653.2006.","journal-title":"Antimicrob Agents Chemother"},{"issue":"4","key":"6435_CR37","doi-asserted-by":"publisher","first-page":"750","DOI":"10.1128\/MMBR.00015-09","volume":"73","author":"TJ Johnson","year":"2009","unstructured":"Johnson TJ, Nolan LK. Pathogenomics of the virulence plasmids of Escherichia coli. Microbiol Mol Biol Rev. 2009;73(4):750\u201374. https:\/\/doi.org\/10.1128\/MMBR.00015-09.","journal-title":"Microbiol Mol Biol Rev"},{"issue":"12","key":"6435_CR38","doi-asserted-by":"publisher","first-page":"2518","DOI":"10.1093\/jac\/dkq347","volume":"65","author":"L Villa","year":"2010","unstructured":"Villa L, Garc\u00eda-Fern\u00e1ndez A, Fortini D, Carattoli A. Replicon sequence typing of IncF plasmids carrying virulence and resistance determinants. J Antimicrob Chemother. 2010;65(12):2518\u201329. https:\/\/doi.org\/10.1093\/jac\/dkq347.","journal-title":"J Antimicrob Chemother"},{"issue":"1","key":"6435_CR39","doi-asserted-by":"publisher","first-page":"18","DOI":"10.4161\/viru.3.1.18382","volume":"3","author":"GJ da Silva","year":"2012","unstructured":"da Silva GJ, Mendon\u00e7a N. Association between antimicrobial resistance and virulence in Escherichia coli. Virulence. 2012;3(1):18\u201328. https:\/\/doi.org\/10.4161\/viru.3.1.18382.","journal-title":"Virulence."},{"issue":"4","key":"6435_CR40","doi-asserted-by":"publisher","first-page":"647","DOI":"10.1128\/CMR.15.4.647-679.2002","volume":"15","author":"JL Mart\u00ednez","year":"2002","unstructured":"Mart\u00ednez JL, Baquero F. Interactions among strategies associated with bacterial infection: pathogenicity, Epidemicity, and antibiotic resistance. Clin Microbiol Rev. 2002;15(4):647\u201379. https:\/\/doi.org\/10.1128\/CMR.15.4.647-679.2002.","journal-title":"Clin Microbiol Rev"},{"issue":"1","key":"6435_CR41","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.plasmid.2008.03.002","volume":"60","author":"MP Garcill\u00e1n-Barcia","year":"2008","unstructured":"Garcill\u00e1n-Barcia MP, de la Cruz F. Why is entry exclusion an essential feature of conjugative plasmids? Plasmid. 2008;60(1):1\u201318. https:\/\/doi.org\/10.1016\/j.plasmid.2008.03.002.","journal-title":"Plasmid"},{"issue":"4","key":"6435_CR42","doi-asserted-by":"publisher","first-page":"1095","DOI":"10.1099\/mic.0.27773-0","volume":"154","author":"R Szczepanowski","year":"2005","unstructured":"Szczepanowski R, Braun S, Riedel V, Schneiker S, Krahn I, P\u00fchler A, et al. The 120 592 bp IncF plasmid pRSB107 isolated from a sewage-treatment plant encodes nine different antibiotic-resistance determinants, two iron-acquisition systems and other putative virulence-associated functions. Microbiology. 2005;154(4):1095\u2013111.","journal-title":"Microbiology"},{"issue":"6","key":"6435_CR43","doi-asserted-by":"publisher","first-page":"2227","DOI":"10.1128\/AAC.01707-08","volume":"53","author":"A Carattoli","year":"2009","unstructured":"Carattoli A. Resistance plasmid families in Enterobacteriaceae. Antimicrob Agents Chemother. 2009;53(6):2227\u201338. https:\/\/doi.org\/10.1128\/AAC.01707-08.","journal-title":"Antimicrob Agents Chemother"},{"issue":"11","key":"6435_CR44","doi-asserted-by":"publisher","first-page":"4667","DOI":"10.1128\/AAC.49.11.4667-4670.2005","volume":"49","author":"JD Pitout","year":"2005","unstructured":"Pitout JD, Laupland KB, Church DL, Menard ML, Johnson JR. Virulence factors of Escherichia coli isolates that produce CTX-M-type extended-spectrum beta-lactamases. Antimicrob Agents Chemother. 2005;49(11):4667\u201370. https:\/\/doi.org\/10.1128\/AAC.49.11.4667-4670.2005.","journal-title":"Antimicrob Agents Chemother"},{"issue":"1","key":"6435_CR45","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1093\/jac\/dkm401","volume":"61","author":"E Karisik","year":"2008","unstructured":"Karisik E, Ellington MJ, Livermore DM, Woodford N. Virulence factors in Escherichia coli with CTX-M-15 and other extended-spectrum beta-lactamases in the UK. J Antimicrob Chemother. 2008;61(1):54\u20138. https:\/\/doi.org\/10.1093\/jac\/dkm401.","journal-title":"J Antimicrob Chemother"},{"issue":"7","key":"6435_CR46","doi-asserted-by":"publisher","first-page":"2311","DOI":"10.1128\/iai.59.7.2311-2315.1991","volume":"59","author":"JR Johnson","year":"1991","unstructured":"Johnson JR, Goullet P, Picard B, Moseley SL, Roberts PL, Stamm WE. Association of carboxylesterase B electrophoretic pattern with presence and expression of urovirulence factor determinants and antimicrobial resistance among strains of Escherichia coli that cause urosepsis. Infect Immun. 1991;59(7):2311\u20135. https:\/\/doi.org\/10.1128\/iai.59.7.2311-2315.1991.","journal-title":"Infect Immun"},{"issue":"4","key":"6435_CR47","first-page":"361","volume":"40","author":"S Lee","year":"2010","unstructured":"Lee S, Yu JK, Park K, Oh E-J, Kim S-Y, Park Y-J. Phylogenetic groups and virulence factors in pathogenic and commensal strains of Escherichia coli and their association with blaCTX-M. Ann Clin Lab Sci. 2010;40(4):361\u20137.","journal-title":"Ann Clin Lab Sci"},{"issue":"12","key":"6435_CR48","doi-asserted-by":"publisher","first-page":"1199","DOI":"10.1111\/j.1469-0691.2006.01536.x","volume":"12","author":"J-P Lavigne","year":"2006","unstructured":"Lavigne J-P, Blanc-Potard A-B, Bourg G, Moreau J, Chanal C, Bouziges N, et al. Virulence genotype and nematode-killing properties of extra-intestinal Escherichia coli producing CTX-M beta-lactamases. Clin Microbiol Infect. 2006;12(12):1199\u2013206. https:\/\/doi.org\/10.1111\/j.1469-0691.2006.01536.x.","journal-title":"Clin Microbiol Infect"},{"issue":"10","key":"6435_CR49","doi-asserted-by":"publisher","first-page":"2035","DOI":"10.4066\/biomedicalresearch.29-17-1591","volume":"29","author":"SN Peerayeh","year":"2018","unstructured":"Peerayeh SN, Navidinia M, Fallah F, Bakhshi B, Jamali J. Pathogenicity determinants and epidemiology of uropathogenic E . coli ( UPEC ) strains isolated from children with urinary tract infection ( UTI ) to define distinct pathotypes. Biomed Res. 2018;29(10):2035\u201343.","journal-title":"Biomed Res"},{"issue":"2008\u20132009","key":"6435_CR50","first-page":"3","volume":"6","author":"G Slavchev","year":"2009","unstructured":"Slavchev G, Pisareva E, Markova N. Virulence of uropathogenic Escherichia coli. J Cult Collect. 2009;6(2008\u20132009):3\u20139.","journal-title":"J Cult Collect"},{"issue":"2","key":"6435_CR51","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1128\/CMR.00059-12","volume":"26","author":"A Beceiro","year":"2013","unstructured":"Beceiro A, Tom\u00e1s M, Bou G. Antimicrobial resistance and virulence : a successful or deleterious Association in the Bacterial World ? Clin Microbiol Rev. 2013;26(2):185\u2013230. https:\/\/doi.org\/10.1128\/CMR.00059-12.","journal-title":"Clin Microbiol Rev"},{"issue":"Suppl 1","key":"6435_CR52","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1093\/infdis\/jiw402","volume":"215","author":"E Geisinger","year":"2017","unstructured":"Geisinger E, Isberg RR. Interplay between antibiotic resistance and virulence during disease promoted by multidrug-resistant Bacteria. J Infect Dis. 2017;215(Suppl 1):9\u201317.","journal-title":"J Infect Dis"},{"issue":"1","key":"6435_CR53","doi-asserted-by":"publisher","first-page":"204","DOI":"10.1186\/s12866-019-1587-3","volume":"19","author":"C Shah","year":"2019","unstructured":"Shah C, Baral R, Bartaula B, Shrestha LB. Virulence factors of uropathogenic Escherichia coli ( UPEC ) and correlation with antimicrobial resistance. BMC Microbiol. 2019;19(1):204. https:\/\/doi.org\/10.1186\/s12866-019-1587-3.","journal-title":"BMC Microbiol"},{"key":"6435_CR54","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1186\/s12941-018-0286-5","volume":"17","author":"FY Ram\u00edrez-Castillo","year":"2018","unstructured":"Ram\u00edrez-Castillo FY, Moreno-Flores AC, Avelar-Gonz\u00e1lez FJ, M\u00e1rquez-D\u00edaz F, Harel J, Guerrero-Barrera AL. An evaluation of multidrug - resistant Escherichia coli isolates in urinary tract infections from Aguascalientes, Mexico: cross - sectional study. Ann Clin Microbiol Antimicrob. 2018;17:34.","journal-title":"Ann Clin Microbiol Antimicrob"},{"issue":"7","key":"6435_CR55","doi-asserted-by":"publisher","first-page":"426","DOI":"10.1016\/j.eimc.2016.02.021","volume":"35","author":"LI Miranda-estrada","year":"2017","unstructured":"Miranda-estrada LI, Ru\u00edz-rosas M, Molina-l\u00f3pez J, Parra-rojas I, Gonzalez-Villalobos E, Castro-Alarcon N. Relationship between virulence factors , resistance to antibiotics and phylogenetic groups of uropathogenic Escherichia coli in two locations. Enferm Infecc Microbiol Clin. 2017;35(7):426\u201333. https:\/\/doi.org\/10.1016\/j.eimc.2016.02.021.","journal-title":"Enferm Infecc Microbiol Clin"},{"issue":"1","key":"6435_CR56","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1186\/s12879-019-3763-3","volume":"19","author":"LM Irenge","year":"2019","unstructured":"Irenge LM, Ambroise J, Bearzatto B, Durant J, Chirimwami RB, Gala J-L. Whole-genome sequences of multidrug- resistant Escherichia coli in South-Kivu Province, Democratic Republic of Congo: characterization of phylogenomic changes, virulence and resistance genes. BMC Infect Dis. 2019;19(1):137. https:\/\/doi.org\/10.1186\/s12879-019-3763-3.","journal-title":"BMC Infect Dis"},{"issue":"1","key":"6435_CR57","first-page":"195","volume":"35","author":"A Pootong","year":"2018","unstructured":"Pootong A, Mungkornkeaw N, Norrapong B, Cowawintaweewat S. Phylogenetic background , drug susceptibility and virulence factors of uropathogenic E . coli isolate in a tertiary university hospital in central Thailand. Trop Biomed. 2018;35(1):195\u2013204.","journal-title":"Trop Biomed"},{"issue":"1","key":"6435_CR58","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1016\/S0255-0857(21)01997-6","volume":"26","author":"MA Vagarali","year":"2008","unstructured":"Vagarali MA, Karadesai SG, Patil CS, Metgud SC, Mutnal MB. Haemagglutination and siderophore production as the urovirulence markers of uropathogenic Escherichia coli. Indian J Med Microbiol. 2008;26(1):68\u201370. https:\/\/doi.org\/10.1016\/S0255-0857(21)01997-6.","journal-title":"Indian J Med Microbiol"},{"issue":"2","key":"6435_CR59","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1016\/j.femsle.2005.08.028","volume":"252","author":"CF Marrs","year":"2005","unstructured":"Marrs CF, Zhang L, Foxman B. Escherichia coli mediated urinary tract infections: are there distinct uropathogenic E. coli (UPEC) pathotypes? FEMS Microbiol Lett. 2005;252(2):183\u201390. https:\/\/doi.org\/10.1016\/j.femsle.2005.08.028.","journal-title":"FEMS Microbiol Lett"},{"issue":"10","key":"6435_CR60","first-page":"1699","volume":"6","author":"N Shruthi","year":"2012","unstructured":"Shruthi N, Ravishkukar R. Phenotypic study of virulence factors in Escherichia coli isolated from antenatal cases, catheterized patients, and faecal flora. J Clin Diagnostic Res. 2012;6(10):1699\u2013703.","journal-title":"J Clin Diagnostic Res"},{"issue":"4","key":"6435_CR61","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1128\/microbiolspec.UTI-0015-2012","volume":"3","author":"S Subashchandrabose","year":"2015","unstructured":"Subashchandrabose S, Mobley HLT. Virulence and fitness determinants of uropathogenic Escherichia coli. Microbiol Spectr. 2015;3(4):1\u201320.","journal-title":"Microbiol Spectr"},{"issue":"10","key":"6435_CR62","doi-asserted-by":"publisher","first-page":"6179","DOI":"10.1128\/IAI.69.10.6179-6185.2001","volume":"69","author":"AG Torres","year":"2001","unstructured":"Torres AG, Redford P, Welch RA, Payne SM. TonB-dependent systems of uropathogenic Escherichia coli: aerobactin and heme transport and TonB are required for virulence in the mouse. Infect Immun. 2001;69(10):6179\u201385. https:\/\/doi.org\/10.1128\/IAI.69.10.6179-6185.2001.","journal-title":"Infect Immun"},{"issue":"2","key":"6435_CR63","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1099\/0022-1317-51-2-138","volume":"51","author":"CF Marrs","year":"2002","unstructured":"Marrs CF, Zhang L, Tallman P, Manning S, Somsel P, Raz R, et al. Variations in 10 putative virulence genes among urinary, faecal and peri-urethral Escherichia coli. J Med Microbiol. 2002;51(2):138\u201342. https:\/\/doi.org\/10.1099\/0022-1317-51-2-138.","journal-title":"J Med Microbiol"},{"issue":"12","key":"6435_CR64","doi-asserted-by":"publisher","first-page":"5322","DOI":"10.1128\/IAI.00779-09","volume":"77","author":"AL Lloyd","year":"2009","unstructured":"Lloyd AL, Smith SN, Eaton KA, Mobley HLT. Uropathogenic Escherichia coli suppresses the host inflammatory response via Pathogenicity Island genes sisA and sisB. Infect Immun. 2009;77(12):5322\u201333. https:\/\/doi.org\/10.1128\/IAI.00779-09.","journal-title":"Infect Immun"},{"issue":"1","key":"6435_CR65","doi-asserted-by":"publisher","first-page":"24099","DOI":"10.1038\/srep24099","volume":"6","author":"Q Su","year":"2016","unstructured":"Su Q, Guan T, Lv H. Siderophore biosynthesis coordinately modulated the virulence-associated interactive metabolome of uropathogenic Escherichia coli and human urin. Sci Rep. 2016;6(1):24099. https:\/\/doi.org\/10.1038\/srep24099.","journal-title":"Sci Rep"},{"issue":"8","key":"6435_CR66","doi-asserted-by":"publisher","first-page":"439","DOI":"10.1038\/s41585-020-0350-8","volume":"17","author":"LL Mariano","year":"2020","unstructured":"Mariano LL, Ingersoll MA. The immune response to infection in the bladder. Nat Rev Urol. 2020;17(8):439\u201358. https:\/\/doi.org\/10.1038\/s41585-020-0350-8.","journal-title":"Nat Rev Urol"}],"container-title":["BMC Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12879-021-06435-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12879-021-06435-7\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12879-021-06435-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,8,4]],"date-time":"2021-08-04T05:06:48Z","timestamp":1628053608000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcinfectdis.biomedcentral.com\/articles\/10.1186\/s12879-021-06435-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,8,4]]},"references-count":66,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2021,12]]}},"alternative-id":["6435"],"URL":"https:\/\/doi.org\/10.1186\/s12879-021-06435-7","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-366326\/v1","asserted-by":"object"}]},"ISSN":["1471-2334"],"issn-type":[{"value":"1471-2334","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,8,4]]},"assertion":[{"value":"10 March 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 July 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 August 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"753"}}