1887

Abstract

Antimicrobial resistance in enteric or urinary is a risk factor for invasive infections. Due to widespread trimethoprim resistance amongst urinary and increased bacteraemia incidence, a national recommendation to prescribe nitrofurantoin for uncomplicated urinary tract infection was made in 2014. Nitrofurantoin resistance is reported in <6% urinary isolates in the UK, however, mechanisms underpinning nitrofurantoin resistance in these isolates remain unknown. This study aimed to identify the genetic basis of nitrofurantoin resistance in urinary isolates collected from north west London and then elucidate resistance-associated genetic alterations in available UK genomes. As a result, an algorithm was developed to predict nitrofurantoin susceptibility. Deleterious mutations and gene-inactivating insertion sequences in chromosomal nitroreductase genes and/or were identified in genomes of nine confirmed nitrofurantoin-resistant urinary isolates and additional 11 isolates that were highlighted by the prediction algorithm and subsequently validated to be nitrofurantoin-resistant. Eight categories of allelic changes in , , and the associated gene were detected in 12412 genomes from the UK. Evolutionary analysis of these three genes revealed homoplasic mutations and explained the previously reported order of stepwise mutations. The mobile gene complex , which is associated with reduced nitrofurantoin susceptibility, was identified in only one of the 12412 genomes. In conclusion, mutations and insertion sequences in and were leading causes of nitrofurantoin resistance in UK . As nitrofurantoin exposure increases in human populations, the prevalence of nitrofurantoin resistance in carriage isolates and those from urinary and bloodstream infections should be monitored.

Funding
This study was supported by the:
  • Medical Research Council (Award MR/T016434/1)
    • Principle Award Recipient: NicholasJ. Croucher
  • Wellcome Trust (Award 104169/Z/14/A)
    • Principle Award Recipient: NicholasJ. Croucher
  • Rosetrees Trust (Award M683)
    • Principle Award Recipient: ElitaJauneikaite
  • National Institute for Health Research (Award HPRU-2012-10047)
    • Principle Award Recipient: NotApplicable
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000702
2021-12-03
2024-05-11
Loading full text...

Full text loading...

/deliver/fulltext/mgen/7/12/mgen000702.html?itemId=/content/journal/mgen/10.1099/mgen.0.000702&mimeType=html&fmt=ahah

References

  1. Waisbren BA, Crowley W. Nitrofurantoin: Clinical and laboratory evaluation. AMA Arch Intern Med 1955; 95:653–661 [View Article]
    [Google Scholar]
  2. Nickel JC. Management of urinary tract infections: historical perspective and current strategies: Part 1—Before antibiotics. J Urol 2005; 173:21–26 [View Article]
    [Google Scholar]
  3. Cunha BA. Nitrofurantoin—current concepts. Urology 1988; 32:67–71 [View Article]
    [Google Scholar]
  4. Garau J. Other antimicrobials of interest in the era of extended-spectrum beta-lactamases: fosfomycin, nitrofurantoin and tigecycline. Clin Microbiol Infect 2008; 14 Suppl 1:198–202 [View Article]
    [Google Scholar]
  5. Wijma RA, Huttner A, Koch BCP, Mouton JW, Muller AE. Review of the pharmacokinetic properties of nitrofurantoin and nitroxoline. J Antimicrob Chemother 2018; 73:2916–2926 [View Article]
    [Google Scholar]
  6. McOsker CC, Fitzpatrick PM. Nitrofurantoin: Mechanism of action and implications for resistance development in common uropathogens. J Antimicrob Chemother 1994; 33:23–30 [View Article]
    [Google Scholar]
  7. Whiteway J, Koziarz P, Veall J, Sandhu N, Kumar P et al. Oxygen-insensitive nitroreductases: Analysis of the roles of nfsA and nfsB in development of resistance to 5-nitrofuran derivatives in Escherichia coli . J Bacteriol 1998; 180:5529–5539 [View Article]
    [Google Scholar]
  8. Vervoort J, Xavier BB, Stewardson A, Coenen S, Godycki-Cwirko M et al. An in vitro deletion in ribe encoding lumazine synthase contributes to nitrofurantoin resistance in Escherichia coli . Antimicrob Agents Chemother 2014; 58:7225–7233 [View Article] [PubMed]
    [Google Scholar]
  9. Lishman H, Costelloe C, Hopkins S, Johnson AP, Hope R et al. Exploring the relationship between primary care antibiotic prescribing for urinary tract infections, Escherichia coli bacteraemia incidence and antimicrobial resistance: an ecological study. Int J Antimicrob Agents 2018; 52:790–798 [View Article]
    [Google Scholar]
  10. Giske CG. Contemporary resistance trends and mechanisms for the old antibiotics colistin, temocillin, fosfomycin, mecillinam and nitrofurantoin. Clin Microbiol Infect 2015; 21:899–905 [View Article]
    [Google Scholar]
  11. Honsbeek M, Tjon-A-Tsien A, Stobberingh E, de Steenwinkel J, Melles DC et al. Low antimicrobial resistance in general practice patients in Rotterdam, the city with the largest proportion of immigrants in the Netherlands. Eur J Clin Microbiol Infect Dis 2020; 39:929–935 [View Article]
    [Google Scholar]
  12. Barisić Z, Babić-Erceg A, Borzić E, Zoranić V, Kaliterna V et al. Urinary tract infections in South Croatia: aetiology and antimicrobial resistance. Int J Antimicrob Agents 2003; 22:61–64 [View Article]
    [Google Scholar]
  13. Caracciolo A, Bettinelli A, Bonato C, Isimbaldi C, Tagliabue A et al. Antimicrobial resistance among Escherichia coli that cause childhood community-acquired urinary tract infections in Northern Italy. Ital J Pediatr 2011; 37:3 [View Article]
    [Google Scholar]
  14. Bollestad M, Vik I, Grude N, Blix HS, Brekke H et al. Bacteriology in uncomplicated urinary tract infections in Norwegian general practice from 2001–2015. BJGP Open 2018; 1:bjgpopen17X101145 [View Article]
    [Google Scholar]
  15. Bean DC, Krahe D, Wareham DW. Antimicrobial resistance in community and nosocomial Escherichia coli urinary tract isolates, London 2005-2006. Ann Clin Microbiol Antimicrob 2008; 7:13 [View Article]
    [Google Scholar]
  16. Blandy O, Honeyford K, Gharbi M, Thomas A, Ramzan F et al. Factors that impact on the burden of Escherichia coli bacteraemia: multivariable regression analysis of 2011-2015 data from West London. J Hosp Infect 2019; 101:120–128 [View Article]
    [Google Scholar]
  17. Public Health England English surveillance programme for antimicrobial utilisation and resistance (ESPAUR) Report 2016. PHE; 2016 https://www.gov.uk/government/publications/english-surveillance-programme-antimicrobial-utilisation-and-resistance-espaur-report
  18. Linkevicius M, Sandegren L, Andersson DI. Mechanisms and fitness costs of tigecycline resistance in Escherichia coli . J Antimicrob Chemother 2013; 68:2809–2819 [View Article]
    [Google Scholar]
  19. Ho P-L, Ng K-Y, Lo W-U, Law PY, Lai EL-Y et al. Plasmid-mediated OqxAB is an important mechanism for nitrofurantoin resistance in Escherichia coli . Antimicrob Agents Chemother 2016; 60:537–543 [View Article]
    [Google Scholar]
  20. Jenkins ST, Bennett PM. Effect of mutations in deoxyribonucleic acid repair pathways on the sensitivity of Escherichia coli K-12 strains to nitrofurantoin. J Bacteriol 1976; 125:1214–1216 [View Article]
    [Google Scholar]
  21. Obaseiki-Ebor EE. Resistance to nitrofurantoin and UV-irradiation in recA; uvrA; and uvrA, lexA, Escherichia coli mutants conferred by an R-plasmid from an Escherichia coli clinical isolate. Mutation Research Letters 1984; 139:5–8 [View Article]
    [Google Scholar]
  22. European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters version 10.0. [Internet]; 2020 http://www.eucast.org
  23. He F. E. coli genomic DNA extraction. Bio Protoc 2011; 1:e97 [View Article]
    [Google Scholar]
  24. Xavier BB, Vervoort J, Stewardson A, Adriaenssens N, Coenen S et al. Complete genome sequences of nitrofurantoin-sensitive and -resistant Genome Sequences of Nitrofurantoin-Sensitive and -Resistant Escherichia coli ST540 and ST2747 sStrains. Genome Announc 2014; 2:14 [View Article]
    [Google Scholar]
  25. McKinnon J, Roy Chowdhury P, Djordjevic SP. Genomic analysis of multidrug-resistant Escherichia coli ST58 causing urosepsis. Int J Antimicrob Agents 2018; 52:430–435 [View Article]
    [Google Scholar]
  26. Zhou Z, Alikhan N-F, Mohamed K, Fan Y et al. The EnteroBase user’s guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity. Genome Res 2020; 30:138–152 [View Article]
    [Google Scholar]
  27. Public Health England NCTC 3000 project: A comprehensive resource of bacterial type and reference genomes [Internet]; 2021 https://www.phe-culturecollections.org.uk/products/bacteria/nctc-3000-project-a-comprehensive-resource-of-bacterial-type-and-reference-genomes.aspx
  28. Andrews S. FastQC: A quality control tool for high throughput sequence data Ref Source; 2010
    [Google Scholar]
  29. Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 2016; 32:3047–3048 [View Article]
    [Google Scholar]
  30. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article]
    [Google Scholar]
  31. Shen W, Le S, Li Y, Hu F, Zou Q. SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS ONE 2016; 11:e0163962 [View Article]
    [Google Scholar]
  32. Touchon M, Perrin A, de Sousa JAM, Vangchhia B, Burn S et al. Phylogenetic background and habitat drive the genetic diversification of Escherichia coli . PLoS Genet 2020; 16:e1008866 [View Article]
    [Google Scholar]
  33. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol 2019; 20:257 [View Article]
    [Google Scholar]
  34. Wick RR, Judd LM, Gorrie CL, Holt KE, Phillippy AM. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article]
    [Google Scholar]
  35. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article]
    [Google Scholar]
  36. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article]
    [Google Scholar]
  37. Wick RR, Schultz MB, Zobel J, Holt KE. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 2015; 31:3350–3352 [View Article]
    [Google Scholar]
  38. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
    [Google Scholar]
  39. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006; 22:1658–1659 [View Article]
    [Google Scholar]
  40. 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:e000131 [View Article]
    [Google Scholar]
  41. Lees JA, Harris SR, Tonkin-Hill G, Gladstone RA, Lo SW et al. Fast and flexible bacterial genomic epidemiology with PopPUNK. Genome Res 2019; 29:304–316 [View Article]
    [Google Scholar]
  42. Beghain J, Bridier-Nahmias A, Le Nagard H, Denamur E, Clermont O. ClermonTyping: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping. Microb Genom 2018; 4:e000192 [View Article]
    [Google Scholar]
  43. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article]
    [Google Scholar]
  44. Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V et al. Twelve years of SAMtools and BCFtools. GigaScience 2021; 10:giab008 [View Article]
    [Google Scholar]
  45. Wan Y, Wick RR, Zobel J, Ingle DJ, Inouye M et al. GeneMates: an R package for detecting horizontal gene co-transfer between bacteria using gene-gene associations controlled for population structure. BMC Genomics 2020; 21:658 [View Article]
    [Google Scholar]
  46. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article]
    [Google Scholar]
  47. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5:R12 [View Article]
    [Google Scholar]
  48. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly (Austin) 2014; 6:80–92 [View Article]
    [Google Scholar]
  49. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 2006; 34:D32–6 [View Article]
    [Google Scholar]
  50. Hawkey J, Hamidian M, Wick RR, Edwards DJ, Billman-Jacobe H et al. ISMapper: identifying transposase insertion sites in bacterial genomes from short read sequence data. BMC Genomics 2015; 16:1–11 [View Article]
    [Google Scholar]
  51. Brynildsrud O, Snipen L-G, Bohlin J. CNOGpro: detection and quantification of CNVs in prokaryotic whole-genome sequencing data. Bioinformatics 2015; 31:1708–1715 [View Article]
    [Google Scholar]
  52. Brynildsrud O. Read Depth Analysis to Identify CNV in Bacteria Using CNOGpro. In Bickhart DM. eds Copy Number Variants: Methods and Protocols Springer; 2018 pp 73–81
    [Google Scholar]
  53. Thompson JD, Gibson TJ, Higgins DG. Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics 2002; 00: [View Article]
    [Google Scholar]
  54. Kumar S, Stecher G, Li M, Knyaz C, Tamura K et al. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article]
    [Google Scholar]
  55. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC et al. Primer3—new capabilities and interfaces. Nucleic Acids Res 2012; 40:e115 [View Article] [PubMed]
    [Google Scholar]
  56. 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]
  57. Seemann T. Abricate GitHub; 2020 https://github.com/tseemann/abricate
  58. 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]
  59. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article]
    [Google Scholar]
  60. Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 2006; 34:W609–12 [View Article]
    [Google Scholar]
  61. Kryazhimskiy S, Plotkin JB, Gojobori T. The population genetics of dN/dS. PLoS Genet 2008; 4:e1000304 [View Article]
    [Google Scholar]
  62. Wilson DJ. CRyPTIC Consortium GenomegaMap: within-species genome-wide dN/dS estimation from over 10,000 genomes. Mol Biol Evol 2020; 37:2450–2460 [View Article]
    [Google Scholar]
  63. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article]
    [Google Scholar]
  64. Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genom 2016; 2:e000056 [View Article]
    [Google Scholar]
  65. Crispell J, Balaz D, Gordon SV. HomoplasyFinder: a simple tool to identify homoplasies on a phylogeny. Microb Genom 2019; 5:e000245 [View Article]
    [Google Scholar]
  66. Bruen TC, Philippe H, Bryant D. A simple and robust statistical test for detecting the presence of recombination. Genetics 2006; 172:2665–2681 [View Article]
    [Google Scholar]
  67. European Committee on Antimicrobial Susceptibility Testing Antimicrobial susceptibility testing EUCAST disk diffusion method Version 8.0; 2020 https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Disk_test_documents/2020_manuals/Manual_v_8.0_EUCAST_Disk_Test_2020.pdf
  68. Choi Y, Chan AP. PROVEAN web server: a tool to predict the functional effect of amino acid substitutions and indels. Bioinformatics 2015; 31:2745–2747 [View Article]
    [Google Scholar]
  69. Chalmers R, Sewitz S, Lipkow K, Crellin P. Complete nucleotide sequence of Tn10 . J Bacteriol 2000; 182:2970–2972 [View Article]
    [Google Scholar]
  70. 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]
  71. Brodrick HJ, Raven KE, Kallonen T, Jamrozy D, Blane B et al. Longitudinal genomic surveillance of multidrug-resistant Escherichia coli carriage in a long-term care facility in the United Kingdom. Genome Med 2017; 9:70 [View Article]
    [Google Scholar]
  72. Goswami C, Fox S, Holden M, Connor M, Leanord A et al. Genetic analysis of invasive Escherichia coli in Scotland reveals determinants of healthcare-associated versus community-acquired infections. Microb Genom 2018; 4: [View Article]
    [Google Scholar]
  73. Sandegren L, Lindqvist A, Kahlmeter G, Andersson DI. Nitrofurantoin resistance mechanism and fitness cost in Escherichia coli . J Antimicrob Chemother 2008; 62:495–503 [View Article]
    [Google Scholar]
  74. Mottaghizadeh F, Mohajjel Shoja H, Haeili M, Darban-Sarokhalil D. Molecular epidemiology and nitrofurantoin resistance determinants of nitrofurantoin-non-susceptible Escherichia coli isolated from urinary tract infections. J Glob Antimicrob Resist 2020; 21:335–339 [View Article]
    [Google Scholar]
  75. Kobori T, Sasaki H, Lee WC, Zenno S, Saigo K et al. Structure and site-directed mutagenesis of a flavoprotein from Escherichia coli that reduces nitrocompounds: alteration of pyridine nucleotide binding by a single amino acid substitution. J Biol Chem 2001; 276:2816–2823 [View Article]
    [Google Scholar]
  76. Yang J, Zhan J, Bai J, Liu P, Xue Y et al. Residue Phe42 is critical for the catalytic activity of Escherichia coli major nitroreductase NfsA. Biotechnol Lett 2013; 35:1693–1700 [View Article]
    [Google Scholar]
  77. Kahlmeter G. The ECO.SENS Project: a prospective, multinational, multicentre epidemiological survey of the prevalence and antimicrobial susceptibility of urinary tract pathogens--interim report. J Antimicrob Chemother 2000; 46 Suppl 1:15–22 [View Article]
    [Google Scholar]
  78. Race PR, Lovering AL, Green RM, Ossor A, White SA et al. Structural and mechanistic studies of Escherichia coli nitroreductase with the antibiotic nitrofurazone. Reversed binding orientations in different redox states of the enzyme. J Biol Chem 2005; 280:13256–13264 [View Article]
    [Google Scholar]
  79. Zhang X, Zhang Y, Wang F, Wang C, Chen L et al. Unravelling mechanisms of nitrofurantoin resistance and epidemiological characteristics among Escherichia coli clinical isolates. Int J Antimicrob Agents 2018; 52:226–232 [View Article]
    [Google Scholar]
  80. Meyer J, Iida S, Arber W. Does the insertion element IS1 transpose preferentially into A+T-rich DNA segments?. Mol Gen Genet 1980; 178:471–473 [View Article]
    [Google Scholar]
  81. Foster TJ, Davis MA, Roberts DE, Takeshita K, Kleckner N. Genetic organization of transposon Tn10 . Cell 1981; 23:201–213 [View Article]
    [Google Scholar]
  82. Hawkey J, Monk JM, Billman-Jacobe H, Palsson B, Holt KE et al. Impact of insertion sequences on convergent evolution of Shigella species. PLoS Genet 2020; 16:e1008931 [View Article]
    [Google Scholar]
  83. Yamazaki Y, Niki H, Kato J. Profiling of Escherichia coli Chromosome database. In Microbial Gene Essentiality: Protocols and Bioinformatics Springer; 2008 pp 385–389
    [Google Scholar]
  84. Jordan IK, Rogozin IB, Wolf YI, Koonin EV. Essential genes are more evolutionarily conserved than are nonessential genes in Bacteria. Genome Res 2002; 12:962–968 [View Article]
    [Google Scholar]
  85. Rocha EPC, Danchin A. An analysis of determinants of amino acids substitution rates in bacterial proteins. Mol Biol Evol 2004; 21:108–116 [View Article]
    [Google Scholar]
  86. Public Health England English surveillance programme for antimicrobial utilisation and resistance (ESPAUR) report 2018 to 2019. PHE; 2019 https://www.gov.uk/government/publications/english-surveillance-programme-antimicrobial-utilisation-and-resistance-espaur-report
  87. Doumith M, Day M, Ciesielczuk H, Hope R, Underwood A et al. Rapid identification of major Escherichia coli sequence types causing urinary tract and bloodstream infections. J Clin Microbiol 2015; 53:160–166 [View Article]
    [Google Scholar]
  88. Abram K, Udaondo Z, Bleker C, Wanchai V, Wassenaar TM et al. Mash-based analyses of Escherichia coli genomes reveal 14 distinct phylogroups. Commun Biol 2021; 4:117 [View Article]
    [Google Scholar]
  89. Reid CJ, DeMaere MZ, Djordjevic SP. Australian porcine clonal complex 10 (CC10) Escherichia coli belong to multiple sublineages of a highly diverse global CC10 phylogeny. Microb Genom 2019; 5: [View Article]
    [Google Scholar]
  90. Gladstone RA, McNally A, Pöntinen AK, Tonkin-Hill G, Lees JA et al. Emergence and dissemination of antimicrobial resistance in Escherichia coli causing bloodstream infections in Norway in 2002–17: a nationwide, longitudinal, microbial population genomic study. The Lancet Microbe 2021; 2:e331–e341 [View Article]
    [Google Scholar]
  91. Rafii F, Hansen EB. Isolation of nitrofurantoin-resistant mutants of nitroreductase-producing Clostridium sp. strains from the human intestinal tract. Antimicrob Agents Chemother 1998; 42:1121–1126 [View Article]
    [Google Scholar]
  92. Tedijanto C, Olesen SW, Grad YH, Lipsitch M. Estimating the proportion of bystander selection for antibiotic resistance among potentially pathogenic bacterial flora. Proc Natl Acad Sci USA 2018; 115:E11988–E11995 [View Article]
    [Google Scholar]
  93. London N, Nijsten R, Bogaard A v. d., Stobberingh E. Carriage of antibiotic-resistant Escherichia coli by healthy volunteers during a 15-week period. Infection 1994; 22:187–192 [View Article]
    [Google Scholar]
  94. Calva JJ, Sifuentes-Osornio J, Cerón C. Antimicrobial resistance in fecal flora: longitudinal community-based surveillance of children from urban Mexico. Antimicrob Agents Chemother 1996; 40:1699–1702 [View Article] [PubMed]
    [Google Scholar]
  95. Nijsten R, London N, van den Bogaard A, Stobberingh E. Antibiotic resistance among Escherichia coli isolated from faecal samples of pig farmers and pigs. J Antimicrob Chemother 1996; 37:1131–1140 [View Article]
    [Google Scholar]
  96. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 2015; 13:269–284 [View Article]
    [Google Scholar]
  97. Solgi H, Giske CG, Badmasti F, Aghamohammad S, Havaei SA et al. Emergence of carbapenem resistant Escherichia coli isolates producing blaNDM and blaOXA-48-like carried on IncA/C and IncL/M plasmids at two Iranian university hospitals. Infect Genet Evol 2017; 55:318–323 [View Article] [PubMed]
    [Google Scholar]
  98. Loncaric I, Misic D, Szostak MP, Künzel F, Schäfer-Somi S et al. Broad-Spectrum Cephalosporin-Resistant and/or Fluoroquinolone-Resistant Enterobacterales Associated with Canine and Feline Urogenital Infections. Antibiotics 2020 [View Article]
    [Google Scholar]
  99. Cheng P, Yang Y, Cao S, Liu H, Li X et al. Prevalence and characteristic of swine-origin mcr-1-positive Escherichia coli in Northeastern China. Front Microbiol 20211986 [View Article]
    [Google Scholar]
  100. Kubelová M, Koláčková I, Gelbíčová T, Florianová M, Kalová A et al. Virulence properties of mcr-1-positive Escherichia coli isolated from retail poultry meat. Microorganisms 2021; 9: [View Article]
    [Google Scholar]
  101. Blaak H, van Hoek A, Hamidjaja RA, van der Plaats RQJ, Kerkhof-de Heer L et al. Distribution, numbers, and diversity of ESBL-producing E. coli in the poultry farm environment. PLoS ONE 2015; 10:e0135402 [View Article]
    [Google Scholar]
  102. RESET Study Group Pietsch M, Irrgang A, Roschanski N, Brenner Michael G et al. Whole genome analyses of CMY-2-producing Escherichia coli isolates from humans, animals and food in Germany. BMC Genomics 2018; 19: [View Article]
    [Google Scholar]
  103. Poulsen HO, Johansson A, Granholm S, Kahlmeter G, Sundqvist M. High genetic diversity of nitrofurantoin- or mecillinam-resistant Escherichia coli indicates low propensity for clonal spread. J Antimicrob Chemother 2013; 68:1974–1977 [View Article]
    [Google Scholar]
  104. Argimón S, Abudahab K, Goater RJE, Fedosejev A, Bhai J et al. Microreact: visualizing and sharing data for genomic epidemiology and phylogeography. Microbial Genomics 2016; 2:e000093 [View Article]
    [Google Scholar]
  105. Bolmström A, Arvidson S, Ericsson M, Karlsson A. A novel technique for direct quantification of antimicrobial susceptibility of microorganisms, abstr. 1209. In: Program and abstracts of the 28th Interscience Conference on Antimicrobial Agents and Chemotherapy American Society for Microbiology, Washington, DC; 1988325
  106. Wan Y, Mills E, Leung RCY, Vieira A, Zhi X et al. Alterations in chromosomal genes nfsa, nfsb, and ribe are associated with nitrofurantoin resistance in escherichia coli from the UK Figshare 2021 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000702
Loading
/content/journal/mgen/10.1099/mgen.0.000702
Loading

Data & Media loading...

Supplements

Loading data from figshare Loading data from figshare
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