1887

Abstract

Urinary tract infections (UTIs) are the most common bacterial infections requiring medical attention and a leading justification for antibiotic prescription. Trimethoprim is prescribed empirically for uncomplicated cases. UTIs are primarily caused by extraintestinal pathogenic (ExPEC) and ExPEC strains play a central role in disseminating antimicrobial-resistance genes worldwide. Here, we describe the whole-genome sequences of trimethoprim-resistant ExPEC and/or ExPEC from recurrent UTIs (67 in total) from patients attending a regional Australian hospital from 2006 to 2008. Twenty-three sequence types (STs) were observed, with ST131 predominating (28 %), then ST69 and ST73 (both 7 %). Co-occurrence of trimethoprim-resistance genes with genes conferring resistance to extended-spectrum β-lactams, heavy metals and quaternary ammonium ions was a feature of the ExPEC described here. Seven trimethoprim-resistance genes were identified, most commonly (38 %) and (18 %). An uncommon variant was also observed. Two variants were identified – (16 %) and (10 %). The former was always associated with , the latter with , and all genes co-occurred with chromate-resistance gene . Eighteen class 1 integron structures were characterized, and featured in eight structures; genes featured in seventeen. ST131 H30Rx isolates possessed distinct antimicrobial gene profiles comprising , , , , , . The most common virulence-associated genes (VAGs) were , , and (all 91 %). Virulence profile clustering showed ST131 H30 isolates carried similar VAGs to ST73, ST405, ST550 and ST1193 isolates. The sole ST131 H27 isolate carried molecular predictors of enteroaggregative /ExPEC hybrid strains (, , ). Seven isolates (10 %) carried VAGs suggesting ColV plasmid carriage. Finally, SNP analysis of serial UTI patients experiencing worsening sequelae demonstrated a high proportion of point mutations in virulence factors.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000475
2020-11-18
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/12/mgen000475.html?itemId=/content/journal/mgen/10.1099/mgen.0.000475&mimeType=html&fmt=ahah

References

  1. Simmering JE, Tang F, Cavanaugh JE, Polgreen LA, Polgreen PM. The increase in hospitalizations for urinary tract infections and the associated costs in the United States, 1998–2011. Open Forum Infect Dis 2017; 4:ofw281 [View Article][PubMed]
    [Google Scholar]
  2. Medical Technology Group Admissions of Failure: the Truth About Unplanned NHS Admissions in England ( https://mtg.org.uk/wp-content/uploads/2016/07/Admissions-of-Failure-2015.pdf) London: Medical Technology Group; 2015
    [Google Scholar]
  3. Australian Commission on Safety and Quality in Health Care Atlas 2017 - 1. Chronic Disease and Infection: Potentially Preventable Hospitalisations (www.safetyandquality.gov.au/our-work/healthcare-variation/atlas-2017/atlas-2017-1-chronic-disease-and-infection-potentially-preventable-hospitalisations) Sydney: Australian Commission on Safety and Quality in Health Care; 2017
    [Google Scholar]
  4. Australian Commission on Safety and Quality in Health Care AURA 2019: Third Australian Report on Antimicrobial Use and Resistance in Human Health (www.safetyandquality.gov.au/publications-and-resources/resource-library/aura-2019-third-australian-report-antimicrobial-use-and-resistance-human-health) Sydney: Australian Commission on Safety and Quality in Health Care; 2019
    [Google Scholar]
  5. Abbo LM, Hooton TM. Antimicrobial stewardship and urinary tract infections. Antibiotics 2014; 3:174–192 [View Article]
    [Google Scholar]
  6. Foxman B, Brown P. Epidemiology of urinary tract infections: transmission and risk factors, incidence, and costs. Infect Dis Clin North Am 2003; 17:227–241
    [Google Scholar]
  7. Manges AR, Geum HM, Guo A, Edens TJ, Fibke CD et al. Global extraintestinal pathogenic Escherichia coli (ExPEC) lineages. Clin Microbiol Rev 2019; 32:e00135-18 [View Article][PubMed]
    [Google Scholar]
  8. Yamaji R, Rubin J, Thys E, Friedman CR, Riley LW. Persistent pandemic lineages of uropathogenic Escherichia coli in a college community from 1999 to 2017. J Clin Microbiol 2018; 56:e01834-17 [View Article][PubMed]
    [Google Scholar]
  9. Manges AR, Johnson JR. Reservoirs of extraintestinal pathogenic Escherichia coli . Microbiol Spectr 2015; 3:UTI-0006-2012 [View Article][PubMed]
    [Google Scholar]
  10. Kantele A, Lääveri T, Mero S, Häkkinen IMK, Kirveskari J et al. Despite predominance of uropathogenic/extraintestinal pathotypes among travel-acquired extended-spectrum β-lactamase-producing Escherichia coli, the most commonly associated clinical manifestation is travelers' diarrhea. Clin Infect Dis 2020; 70:210–218 [View Article][PubMed]
    [Google Scholar]
  11. Russo TA, Johnson JR. Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect 2003; 5:449–456 [View Article]
    [Google Scholar]
  12. Epstein L, Dantes R, Magill S, Fiore A. Varying estimates of sepsis mortality using death certificates and administrative codes — United States, 1999–2014. MMWR Morb Mortal Wkly Rep 2016; 65:342–345 [View Article][PubMed]
    [Google Scholar]
  13. Rhee C, Dantes R, Epstein L, Murphy DJ, Seymour CW et al. Incidence and trends of sepsis in US hospitals using clinical vs claims data, 2009-2014. JAMA 2017; 318:1241–1249 [View Article]
    [Google Scholar]
  14. Daga AP, Koga VL, Soncini JGM, de Matos CM, Perugini MRE et al. Escherichia coli bloodstream infections in patients at a university hospital: virulence factors and clinical characteristics. Front Cell Infect Microbiol 2019; 9:191 [View Article][PubMed]
    [Google Scholar]
  15. Dale AP, Woodford N. Extra-intestinal pathogenic Escherichia coli (ExPEC): disease, carriage and clones. J Infect 2015; 71:615–626 [View Article]
    [Google Scholar]
  16. Micenková L, Bosák J, Vrba M, Ševčíková A, Šmajs D. Human extraintestinal pathogenic Escherichia coli strains differ in prevalence of virulence factors, phylogroups, and bacteriocin determinants. BMC Microbiol 2016; 16:218 [View Article][PubMed]
    [Google Scholar]
  17. Johnson TJ, Nolan LK. Pathogenomics of the virulence plasmids of Escherichia coli . MMBR 2009; 73:750–774 [View Article]
    [Google Scholar]
  18. Peirano G, Mulvey GL, Armstrong GD, Pitout JDD. Virulence potential and adherence properties of Escherichia coli that produce CTX-M and NDM β-lactamases. J Med Microbiol 2013; 62:525–530 [View Article]
    [Google Scholar]
  19. Johnson JR, Magistro G, Clabots C, Porter S, Manges A et al. Contribution of yersiniabactin to the virulence of an Escherichia coli sequence type 69 (“clonal group A”) cystitis isolate in murine models of urinary tract infection and sepsis. Microb Pathog 2018; 120:128–131 [View Article]
    [Google Scholar]
  20. Hancock V, Ferrières L, Klemm P. The ferric yersiniabactin uptake receptor FyuA is required for efficient biofilm formation by urinary tract infectious Escherichia coli in human urine. Microbiology 2008; 154:167–175 [View Article][PubMed]
    [Google Scholar]
  21. Magistro G, Hoffmann C, Schubert S. The salmochelin receptor IroN itself, but not salmochelin-mediated iron uptake promotes biofilm formation in extraintestinal pathogenic Escherichia coli (ExPEC). Int J Med Microbiol 2015; 305:435–445 [View Article]
    [Google Scholar]
  22. Alam M, Bastakoti B. Therapeutic guidelines: antibiotic, version 15. Aust Prescr 2015; 38:137 [View Article]
    [Google Scholar]
  23. Fasugba O, Mitchell BG, Mnatzaganian G, Das A, Collignon P et al. Five-year antimicrobial resistance patterns of urinary Escherichia coli at an Australian tertiary hospital: time series analyses of prevalence data. PLoS One 2016; 11:e0164306 [View Article]
    [Google Scholar]
  24. Nicolas-Chanoine M-H, Bertrand X, Madec J-Y. Escherichia coli ST131, an intriguing clonal group. Clin Microbiol Rev 2014; 27:543–574 [View Article]
    [Google Scholar]
  25. Price LB, Johnson JR, Aziz M, Clabots C, Johnston B et al. The epidemic of extended-spectrum-β-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. mBio 2013; 4:e00377-13 [View Article]
    [Google Scholar]
  26. Paltansing S, Kraakman MEM, Ras JMC, Wessels E, Bernards AT. Characterization of fluoroquinolone and cephalosporin resistance mechanisms in Enterobacteriaceae isolated in a Dutch teaching hospital reveals the presence of an Escherichia coli ST131 clone with a specific mutation in parE. J Antimicrob Chemother 2013; 68:40–45 [View Article]
    [Google Scholar]
  27. Johnson JR, Tchesnokova V, Johnston B, Clabots C, Roberts PL et al. Abrupt emergence of a single dominant multidrug-resistant strain of Escherichia coli . J Infect Dis 2013; 207:919–928 [View Article]
    [Google Scholar]
  28. Poolman JT, Wacker M. Extraintestinal pathogenic Escherichia coli, a common human pathogen: challenges for vaccine development and progress in the field. J Infect Dis 2016; 213:6–13 [View Article][PubMed]
    [Google Scholar]
  29. Zilberberg MD, Shorr AF. Secular trends in gram-negative resistance among urinary tract infection hospitalizations in the United States, 2000–2009. Infect Control Hosp Epidemiol 2013; 34:940–946 [View Article][PubMed]
    [Google Scholar]
  30. Bevan ER, Jones AM, Hawkey PM. Global epidemiology of CTX-M β-lactamases: temporal and geographical shifts in genotype. J Antimicrob Chemother 2017; 72:2145–2155 [View Article]
    [Google Scholar]
  31. Bajaj P, Singh NS, Virdi JS. Escherichia coli β-lactamases: what really matters. Front Microbiol 2016; 7:417 [View Article][PubMed]
    [Google Scholar]
  32. Partridge SR, Kwong SM, Firth N, Jensen SO. Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev 2018; 31:e00088-17 [View Article][PubMed]
    [Google Scholar]
  33. Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Susceptibility Testing Wayne, PA: Clinical and Laboratory Standards Institute; 2017
    [Google Scholar]
  34. Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Disk Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard, M02-A10, 10th edn. Wayne, PA: Clinical and Laboratory Standards Institute; 2009
    [Google Scholar]
  35. Reid CJ, Wyrsch ER, Chowdhury PR, Zingali T, Liu M et al. Porcine commensal Escherichia coli: a reservoir for class 1 integrons associated with IS26. Microb Genom 2017; 3:mgen.0.000143 [View Article][PubMed]
    [Google Scholar]
  36. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 2020; 37:1530–1534 [View Article]
    [Google Scholar]
  37. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15 [View Article][PubMed]
    [Google Scholar]
  38. Kallonen T, Brodrick HJ, Harris SR, Corander J, Brown NM et al. Systematic longitudinal survey of invasive Escherichia coli in England demonstrates a stable population structure only transiently disturbed by the emergence of ST131. Genome Res 2017; 27:1437–1449 [View Article]
    [Google Scholar]
  39. Nascimento V, Day MR, Doumith M, Hopkins KL, Woodford N et al. Comparison of phenotypic and WGS-derived antimicrobial resistance profiles of enteroaggregative Escherichia coli isolated from cases of diarrhoeal disease in England, 2015–16. J Antimicrob Chemother 2017; 72:3288–3297 [View Article]
    [Google Scholar]
  40. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article]
    [Google Scholar]
  41. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article]
    [Google Scholar]
  42. Hadfield J, Croucher NJ, Goater RJ, Abudahab K, Aanensen DM et al. Phandango: an interactive viewer for bacterial population genomics. Bioinformatics 2018; 34:292–293 [View Article]
    [Google Scholar]
  43. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
    [Google Scholar]
  44. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 2012; 50:1355–1361 [View Article]
    [Google Scholar]
  45. Joensen KG, Tetzschner AMM, Iguchi A, Aarestrup FM, Scheutz F. Rapid and easy in silico serotyping of Escherichia coli isolates by use of whole-genome sequencing data. J Clin Microbiol 2015; 53:2410–2426 [View Article][PubMed]
    [Google Scholar]
  46. Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 2013; 5:58–65 [View Article]
    [Google Scholar]
  47. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. blast+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article]
    [Google Scholar]
  48. Hunt M, Mather AE, Sánchez-Busó L, Page AJ, Parkhill J et al. ARIBA: rapid antimicrobial resistance genotyping directly from sequencing reads. Microb Genom 2017; 3:mgen.0.000131 [View Article][PubMed]
    [Google Scholar]
  49. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 2012; 67:2640–2644 [View Article]
    [Google Scholar]
  50. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O et al. In silico detection and typing of plasmids using plasmidfinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 2014; 58:3895–3903 [View Article]
    [Google Scholar]
  51. Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS et al. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli . J Clin Microbiol 2014; 52:1501–1510 [View Article]
    [Google Scholar]
  52. Johnson JR, Stell AL, Scheutz F, O'Bryan TT, Russo TA et al. Analysis of the F antigen-specific papAAlleles of extraintestinal pathogenic Escherichia coli using a novel multiplex PCR-based assay. Infect Immun 2000; 68:1587–1599 [View Article]
    [Google Scholar]
  53. Yu G, Smith DK, Zhu H, Guan Y, Lam Tommy Tsan‐Yuk. ggtree: an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 2017; 8:28–36 [View Article]
    [Google Scholar]
  54. Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article]
    [Google Scholar]
  55. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article]
    [Google Scholar]
  56. Leray M, Knowlton N, Ho S-L, Nguyen BN, Machida RJ. GenBank is a reliable resource for 21st century biodiversity research. Proc Natl Acad Sci USA 2019; 116:22651–22656 [View Article]
    [Google Scholar]
  57. Zhou Z, Alikhan N-F, Mohamed K, Fan Y. Agama Study Group et al. The EnteroBase user’s guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny and Escherichia core genomic diversity. Genome Res 2019; 119:251678
    [Google Scholar]
  58. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2011; 27:1009–1010 [View Article]
    [Google Scholar]
  59. Hendriksen RS, Bortolaia V, Tate H, Tyson GH, Aarestrup FM et al. Using genomics to track global antimicrobial resistance. Front Public Health 2019; 7:242 [View Article][PubMed]
    [Google Scholar]
  60. Al-Badr A, Al-Shaikh G. Recurrent urinary tract infections management in women. Sultan Qaboos Univ Med J 2013; 13:359–367
    [Google Scholar]
  61. Schmiemann G, Kniehl E, Gebhardt K, Matejczyk MM, Hummers-Pradier E. The diagnosis of urinary tract infection: a systematic review. Dtsch Arzteblatt Int 2010; 107:361–367
    [Google Scholar]
  62. Chu CM, Lowder JL. Diagnosis and treatment of urinary tract infections across age groups. Am J Obstet Gynecol 2018; 219:40–51 [View Article]
    [Google Scholar]
  63. Johnson JR, Menard M, Johnston B, Kuskowski MA, Nichol K et al. Epidemic clonal groups of Escherichia coli as a cause of antimicrobial-resistant urinary tract infections in Canada, 2002 to 2004. Antimicrob Agents Chemother 2009; 53:2733–2739 [View Article]
    [Google Scholar]
  64. Kudinha T, Johnson JR, Andrew SD, Kong F, Anderson P et al. Escherichia coli sequence type 131 as a prominent cause of antibiotic resistance among urinary Escherichia coli isolates from reproductive-age women. J Clin Microbiol 2013; 51:3270–3276 [View Article]
    [Google Scholar]
  65. Kudinha T, Johnson JR, Andrew SD, Kong F, Anderson P et al. Genotypic and phenotypic characterization of Escherichia coli isolates from children with urinary tract infection and from healthy carriers. Pediatr Infect Dis J 2013; 32:543–548 [View Article]
    [Google Scholar]
  66. Kudinha T, Johnson JR, Andrew SD, Kong F, Anderson P et al. Distribution of phylogenetic groups, sequence type ST131, and virulence-associated traits among Escherichia coli isolates from men with pyelonephritis or cystitis and healthy controls. Clin Microbiol Infect 2013; 19:E173–E180 [View Article]
    [Google Scholar]
  67. Liu CM, Stegger M, Aziz M, Johnson TJ, Waits K et al. Escherichia coli ST131- H22 as a foodborne thogen. mBio 2018; 9:mBio.00470-18 [View Article]
    [Google Scholar]
  68. Mathers AJ, Peirano G, Pitout JDD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae . Clin Microbiol Rev 2015; 28:565–591 [View Article]
    [Google Scholar]
  69. Ewers C, Göttig S, Bülte M, Fiedler S, Tietgen M et al. Genome sequence of avian Escherichia coli strain IHIT25637, an extraintestinal pathogenic E. coli strain of ST131 encoding colistin resistance determinant MCR-1. Genome Announc 2016; 4:e00863-16 [View Article][PubMed]
    [Google Scholar]
  70. Johnson TJ, Hargreaves M, Shaw K, Snippes P, Lynfield R et al. Complete genome sequence of a carbapenem-resistant extraintestinal pathogenic Escherichia coli strain belonging to the sequence type 131 H30R subclade. Genome Announc 2015; 3:e00272-15 [View Article][PubMed]
    [Google Scholar]
  71. World Health Organization Global Action Plan on Antimicrobial Resistance (www.who.int/antimicrobial-resistance/publications/global-action-plan/en/) Geneva: World Health Organization; 2015
    [Google Scholar]
  72. Pearson J, Turnidge J, Franklin C, Bell J. Australian Group on Antimicrobial Resistance Prevalence of antimicrobial resistances in common pathogenic Enterobacteriaceae in Australia, 2004: report from the Australian Group on Antimicrobial Resistance. Commun Dis Intell Q Rep 2007; 31:106–112[PubMed]
    [Google Scholar]
  73. Bell JM, Gottlieb T, Daley DA, Coombs GW. Australian Group on Antimicrobial Resistance (AGAR) Australian gram-negative sepsis outcome programme (GNSOP) annual report 2017. Commun Dis Intell 2019; 43:cdi.2019.43.37 [View Article]
    [Google Scholar]
  74. Kot B. Antibiotic resistance among uropathogenic Escherichia coli . Pol J Microbiol 2019; 68:403–415 [View Article]
    [Google Scholar]
  75. Thänert R, Reske KA, Hink T, Wallace MA, Wang B et al. Comparative genomics of antibiotic-resistant uropathogens implicates three routes for recurrence of urinary tract infections. mBio 2019; 10:e01977-19 [View Article]
    [Google Scholar]
  76. Mortazavi-Tabatabaei SAR, Ghaderkhani J, Nazari A, Sayehmiri K, Sayehmiri F et al. Pattern of antibacterial resistance in urinary tract infections: a systematic review and meta-analysis. Int J Prev Med 2019; 10:169
    [Google Scholar]
  77. Critchley IA, Cotroneo N, Pucci MJ, Mendes R. The burden of antimicrobial resistance among urinary tract isolates of Escherichia coli in the United States in 2017. PLoS One 2019; 14:e0220265 [View Article]
    [Google Scholar]
  78. Mulder M, Verbon A, Lous J, Goessens W, Stricker BH. Use of other antimicrobial drugs is associated with trimethoprim resistance in patients with urinary tract infections caused by E. coli . Eur J Clin Microbiol Infect Dis 2019; 38:2283–2290 [View Article]
    [Google Scholar]
  79. Seputiene V, Povilonis J, Ruzauskas M, Pavilonis A, Suziedeliene E. Prevalence of trimethoprim resistance genes in Escherichia coli isolates of human and animal origin in Lithuania. J Med Microbiol 2010; 59:315–322 [View Article]
    [Google Scholar]
  80. Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 2020; 48:D517–D525 [View Article][PubMed]
    [Google Scholar]
  81. Djordjevic SP, Stokes HW, Chowdhury PR. Mobile elements, zoonotic pathogens and commensal bacteria: conduits for the delivery of resistance genes into humans, production animals and soil microbiota. Front Microbiol 2013; 4:86 [View Article][PubMed]
    [Google Scholar]
  82. Cummins ML, Reid CJ, Chowdhury PR, Bushell RN, Esbert N et al. Whole genome sequence analysis of Australian avian pathogenic Escherichia coli that carry the class 1 integrase gene. Microb Genomics 2019; 5:e000250 [View Article]
    [Google Scholar]
  83. Jarocki VM, Reid CJ, Chapman TA, Djordjevic SP. Escherichia coli ST302: genomic analysis of virulence potential and antimicrobial resistance mediated by mobile genetic elements. Front Microbiol 2020; 10:3098 [View Article][PubMed]
    [Google Scholar]
  84. Reid CJ, Blau K, Jechalke S, Smalla K, Djordjevic SP. Whole genome sequencing of Escherichia coli from store-bought produce. Front Microbiol 2020; 10:03050 [View Article]
    [Google Scholar]
  85. Poirel L, Kämpfer P, Nordmann P. Chromosome-encoded ambler class A β-lactamase of Kluyvera georgiana, a probable progenitor of a subgroup of CTX-M extended-spectrum β-lactamases. Antimicrob Agents Chemother 2002; 46:4038–4040 [View Article]
    [Google Scholar]
  86. Cormier A, Zhang PLC, Chalmers G, Weese JS, Deckert A et al. Diversity of CTX-M-positive Escherichia coli recovered from animals in Canada. Vet Microbiol 2019; 231:71–75 [View Article]
    [Google Scholar]
  87. El-Badawy MF, Tawakol WM, Maghrabi IA, Mansy MS, Shohayeb MM et al. Iodometric and molecular detection of ESBL production among clinical isolates of E. coli fingerprinted by ERIC-PCR: the first Egyptian report declares the emergence of E. coli O25b-ST131clone harboring bla GES . Microb Drug Resist 2017; 23:703–717 [View Article]
    [Google Scholar]
  88. Yuan L, Liu J-H, Hu G-Z, Pan Y-S, Liu Z-M et al. Molecular characterization of extended-spectrum β-lactamase-producing Escherichia coli isolates from chickens in Henan Province, China. J Med Microbiol 2009; 58:1449–1453 [View Article]
    [Google Scholar]
  89. Farajzadeh Sheikh A, Goodarzi H, Yadyad MJ, Aslani S, Amin M et al. Virulence-associated genes and drug susceptibility patterns of uropathogenic Escherichia coli isolated from patients with urinary tract infection. Infect Drug Resist 2019; 12:2039–2047 [View Article]
    [Google Scholar]
  90. Ramírez-Castillo FY, Moreno-Flores AC, Avelar-González FJ, Márquez-Díaz F, Harel J et 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 [View Article]
    [Google Scholar]
  91. Ochoa SA, Cruz-Córdova A, Luna-Pineda VM, Reyes-Grajeda JP, Cázares-Domínguez V et al. Multidrug- and extensively drug-resistant uropathogenic Escherichia coli clinical strains: phylogenetic groups widely associated with integrons maintain high genetic diversity. Front Microbiol 2016; 7:02042 [View Article]
    [Google Scholar]
  92. Li L-G, Xia Y, Zhang T. Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection. ISME J 2017; 11:651–662 [View Article][PubMed]
    [Google Scholar]
  93. Yang S, Deng W, Liu S, Yu X, Mustafa GR et al. Presence of heavy metal resistance genes in Escherichia coli and Salmonella isolates and analysis of resistance gene structure in E. coli E308. J Glob Antimicrob Resist 2020; 21:420–426 [View Article][PubMed]
    [Google Scholar]
  94. Nguyen CC, Hugie CN, Kile ML, Navab-Daneshmand T. Association between heavy metals and antibiotic-resistant human pathogens in environmental reservoirs: a review. Front Environ Sci Eng 2019; 13:46 [View Article]
    [Google Scholar]
  95. Department of Primary Industries Central West Region Pilot Area Agricultural Profile (www.dpi.nsw.gov.au/__data/assets/pdf_file/0010/457588/Agricultural-profile-central-west-region.pdf) Sydney: NSW Government; 2012
    [Google Scholar]
  96. Knapp CW, McCluskey SM, Singh BK, Campbell CD, Hudson G et al. Antibiotic resistance gene abundances correlate with metal and geochemical conditions in archived Scottish soils. PLoS One 2011; 6:e27300 [View Article][PubMed]
    [Google Scholar]
  97. Gillings MR. Integrons: past, present, and future. Microbiol Mol Biol Rev 2014; 78:257–277 [View Article][PubMed]
    [Google Scholar]
  98. Dawes FE, Kuzevski A, Bettelheim KA, Hornitzky MA, Djordjevic SP et al. Distribution of class 1 integrons with IS26-mediated deletions in their 3'-conserved segments in Escherichia coli of human and animal origin. PLoS One 2010; 5:e12754 [View Article][PubMed]
    [Google Scholar]
  99. Brolund A, Rajer F, Giske CG, Melefors Ö, Titelman E et al. Dynamics of resistance plasmids in extended-spectrum-β-lactamase-producing Enterobacteriaceae during postinfection colonization. Antimicrob Agents Chemother 2019; 63:e02201-18 [View Article][PubMed]
    [Google Scholar]
  100. Toulouse JL, Edens TJ, Alejaldre L, Manges AR, Pelletier JN. Integron-associated DfrB4, a previously uncharacterized member of the trimethoprim-resistant dihydrofolate reductase B family, is a clinically identified emergent source of antibiotic resistance. Antimicrob Agents Chemother 2017; 61:e02665-16 [View Article][PubMed]
    [Google Scholar]
  101. Venturini C, Hassan KA, Chowdhury PR, Paulsen IT, Walker MJ et al. Sequences of two related multiple antibiotic resistance virulence plasmids sharing a unique IS26-related molecular signature isolated from different Escherichia coli pathotypes from different hosts. PLoS One 2013; 8:e78862 [View Article]
    [Google Scholar]
  102. McKinnon J, Chowdhury PR, Djordjevic SP. Genomic analysis of multidrug-resistant Escherichia coli ST58 causing urosepsis. Int J Antimicrob Agents 2018; 52:430–435 [View Article]
    [Google Scholar]
  103. McKinnon J, Chowdhury PR, Djordjevic SP. Molecular analysis of an IncF ColV-Like plasmid lineage that carries a complex resistance locus with a trackable genetic signature. Microb Drug Resist 2020; 26:787–793 [View Article][PubMed]
    [Google Scholar]
  104. Bie L, Fang M, Li Z, Wang M, Xu H. Identification and characterization of new resistance-conferring SGI1s (Salmonella genomic island 1) in Proteus mirabilis . Front Microbiol 2018; 9:03172 [View Article]
    [Google Scholar]
  105. Alonso CA, González-Barrio D, Tenorio C, Ruiz-Fons F, Torres C. Antimicrobial resistance in faecal Escherichia coli isolates from farmed red deer and wild small mammals. Detection of a multiresistant E. coli producing extended-spectrum beta-lactamase. Comp Immunol Microbiol Infect Dis 2016; 45:34–39 [View Article]
    [Google Scholar]
  106. Mendes Moreira A, Couvé-Deacon E, Bousquet P, Chainier D, Jové T et al. Proteae: a reservoir of class 2 integrons?. J Antimicrob Chemother 2019; 74:1560–1562 [View Article]
    [Google Scholar]
  107. Mora-Rillo M, Fernández-Romero N, Navarro-San Francisco C, Díez-Sebastián J, Romero-Gómez MP et al. Impact of virulence genes on sepsis severity and survival in Escherichia coli bacteremia. Virulence 2015; 6:93–100 [View Article][PubMed]
    [Google Scholar]
  108. Bonacorsi S, Houdouin V, Mariani-Kurkdjian P, Mahjoub-Messai F, Bingen E. Comparative prevalence of virulence factors in Escherichia coli causing urinary tract infection in male infants with and without bacteremia. J Clin Microbiol 2006; 44:1156–1158 [View Article][PubMed]
    [Google Scholar]
  109. Lefort A, Panhard X, Clermont O, Woerther P-L, Branger C et al. Host factors and portal of entry outweigh bacterial determinants to predict the severity of Escherichia coli bacteremia. J Clin Microbiol 2011; 49:777–783 [View Article][PubMed]
    [Google Scholar]
  110. Jauréguy F, Carbonnelle E, Bonacorsi S, Clec'h C, Casassus P et al. Host and bacterial determinants of initial severity and outcome of Escherichia coli sepsis. Clin Microbiol Infect 2007; 13:854–862 [View Article][PubMed]
    [Google Scholar]
  111. Brumbaugh AR, Smith SN, Mobley HLT. Immunization with the yersiniabactin receptor, FyuA, protects against pyelonephritis in a murine model of urinary tract infection. Infect Immun 2013; 81:3309–3316 [View Article][PubMed]
    [Google Scholar]
  112. Wright KJ, Hultgren SJ. Sticky fibers and uropathogenesis: bacterial adhesins in the urinary tract. Future Microbiol 2006; 1:75–87 [View Article][PubMed]
    [Google Scholar]
  113. Miajlovic H, Mac Aogáin M, Collins CJ, Rogers TR, Smith SGJ. Characterization of Escherichia coli bloodstream isolates associated with mortality. J Med Microbiol 2016; 65:71–79 [View Article][PubMed]
    [Google Scholar]
  114. Dale AP, Pandey AK, Hesp RJ, Belogiannis K, Laver JR et al. Genomes of Escherichia coli bacteraemia isolates originating from urinary tract foci contain more virulence-associated genes than those from non-urinary foci and neutropaenic hosts. J Infect 2018; 77:534–543 [View Article][PubMed]
    [Google Scholar]
  115. Croxen MA, Finlay BB. Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 2010; 8:26–38 [View Article][PubMed]
    [Google Scholar]
  116. Chowdhury PR, McKinnon J, Liu M, Djordjevic SP. Multidrug resistant uropathogenic Escherichia coli ST405 with a novel, composite IS26 transposon in a unique chromosomal location. Front Microbiol 2018; 9:3212 [View Article][PubMed]
    [Google Scholar]
  117. Johnson JR, Johnston BD, Porter SB, Clabots C, Bender TL et al. Rapid emergence, subsidence, and molecular detection of Escherichia coli sequence type 1193-fimH64, a new disseminated multidrug-resistant commensal and extraintestinal pathogen. J Clin Microbiol 2019; 57:e01664-18 [View Article][PubMed]
    [Google Scholar]
  118. Blanco J, Mora A, Mamani R, López C, Blanco M et al. Four main virotypes among extended-spectrum-β-lactamase-producing isolates of Escherichia coli O25b:H4-B2-ST131: bacterial, epidemiological, and clinical characteristics. J Clin Microbiol 2013; 51:3358–3367 [View Article][PubMed]
    [Google Scholar]
  119. Olesen B, Scheutz F, Andersen RL, Menard M, Boisen N et al. Enteroaggregative Escherichia coli O78:H10, the cause of an outbreak of urinary tract infection. J Clin Microbiol 2012; 50:3703–3711 [View Article][PubMed]
    [Google Scholar]
  120. Boll EJ, Stegger M, Hasman H, Roer L, Overballe-Petersen S et al. Emergence of enteroaggregative Escherichia coli within the ST131 lineage as a cause of extraintestinal infections. bioRxiv 2018; 435941:
    [Google Scholar]
  121. Lara FBM, Nery DR, de Oliveira PM, Araujo ML, Carvalho FRQ et al. Virulence markers and phylogenetic analysis of Escherichia coli strains with hybrid EAEC/UPEC genotypes recovered from sporadic cases of extraintestinal infections. Front Microbiol 2017; 8:146 [View Article][PubMed]
    [Google Scholar]
  122. Boll EJ, Struve C, Boisen N, Olesen B, Stahlhut SG et al. Role of enteroaggregative Escherichia coli virulence factors in uropathogenesis. Infect Immun 2013; 81:1164–1171 [View Article][PubMed]
    [Google Scholar]
  123. Dobrindt U, Chowdary MG, Krumbholz G, Hacker J. Genome dynamics and its impact on evolution of Escherichia coli . Med Microbiol Immunol 2010; 199:145–154 [View Article][PubMed]
    [Google Scholar]
  124. Calhau V, Ribeiro G, Mendonça N, Da Silva GJ. Prevalent combination of virulence and plasmidic-encoded resistance in ST 131 Escherichia coli strains. Virulence 2013; 4:726–729 [View Article][PubMed]
    [Google Scholar]
  125. Rodriguez-Siek KE, Giddings CW, Doetkott C, Johnson TJ, Nolan LK. Characterizing the APEC pathotype. Vet Res 2005; 36:241–256 [View Article][PubMed]
    [Google Scholar]
  126. Johnson TJ, Wannemuehler Y, Johnson SJ, Stell AL, Doetkott C et al. Comparison of extraintestinal pathogenic Escherichia coli strains from human and avian sources reveals a mixed subset representing potential zoonotic pathogens. Appl Environ Microbiol 2008; 74:7043–7050 [View Article][PubMed]
    [Google Scholar]
  127. Gérard F, Pradel N, Wu L-F. Bactericidal activity of colicin V is mediated by an inner membrane protein, SdaC, of Escherichia coli . J Bacteriol 2005; 187:1945–1950 [View Article][PubMed]
    [Google Scholar]
  128. Chattopadhyay S, Weissman SJ, Minin VN, Russo TA, Dykhuizen DE et al. High frequency of hotspot mutations in core genes of Escherichia coli due to short-term positive selection. Proc Natl Acad Sci USA 2009; 106:12412–12417 [View Article][PubMed]
    [Google Scholar]
  129. Denamur E, Bonacorsi S, Giraud A, Duriez P, Hilali F et al. High frequency of mutator strains among human uropathogenic Escherichia coli isolates. J Bacteriol 2002; 184:605–609 [View Article][PubMed]
    [Google Scholar]
  130. Chen SL, Hung C-S, Xu J, Reigstad CS, Magrini V et al. Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. Proc Natl Acad Sci USA 2006; 103:5977–5982 [View Article][PubMed]
    [Google Scholar]
  131. Nielsen KL, Stegger M, Godfrey PA, Feldgarden M, Andersen PS et al. Adaptation of Escherichia coli traversing from the faecal environment to the urinary tract. Int J Med Microbiol 2016; 306:595–603 [View Article][PubMed]
    [Google Scholar]
  132. Eddy SR. Where did the BLOSUM62 alignment score matrix come from?. Nat Biotechnol 2004; 22:1035–1036 [View Article][PubMed]
    [Google Scholar]
  133. Ragheb MN, Thomason MK, Hsu C, Nugent P, Gage J et al. Inhibiting the evolution of antibiotic resistance. Mol Cell 2019; 73:157–165 [View Article][PubMed]
    [Google Scholar]
  134. Selby CP. Mfd protein and transcription-repair coupling in Escherichia coli . Photochem Photobiol 2017; 93:280–295 [View Article][PubMed]
    [Google Scholar]
  135. Thorpe HA, Bayliss SC, Hurst LD, Feil EJ. Comparative analyses of selection operating on nontranslated intergenic regions of diverse bacterial species. Genetics 2017; 206:363–376 [View Article][PubMed]
    [Google Scholar]
  136. Guttman DS, Dykhuizen DE. Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science 1994; 266:1380–1383 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000475
Loading
/content/journal/mgen/10.1099/mgen.0.000475
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error