1887

Abstract

This study sought to assess the genetic variability of isolated from bloodstream infections (BSIs) presenting at Concord Hospital, Sydney during 2013–2016. Whole-genome sequencing was used to characterize 81 isolates sourced from community-onset (CO) and hospital-onset (HO) BSIs. The cohort comprised 64 CO and 17 HO isolates, including 35 multidrug-resistant (MDR) isolates exhibiting phenotypic resistance to three or more antibiotic classes. Phylogenetic analysis identified two major ancestral clades. One was genetically diverse with 25 isolates distributed in 16 different sequence types (STs) representing phylogroups A, B1, B2, C and F, while the other comprised phylogroup B2 isolates in subclades representing the ST131, ST73 and ST95 lineages. Forty-seven isolates contained a class 1 integron, of which 14 carried gene. Isolates with a class 1 integron carried more antibiotic resistance genes than isolates without an integron and, in most instances, resistance genes were localized within complex resistance loci (CRL). Resistance to fluoroquinolones could be attributed to point mutations in chromosomal and genes and, in addition, two isolates carried a plasmid-associated gene. Co-resistance to fluoroquinolone and broad-spectrum beta-lactam antibiotics was associated with ST131 (HO and CO), ST38 (HO), ST393 (CO), ST2003 (CO) and ST8196 (CO and HO), a novel ST identified in this study. Notably, 10/81 (12.3 %) isolates with ST95 (5 isolates), ST131 (2 isolates), ST88 (2 isolates) and a ST540 likely carry IncFII–IncFIB plasmid replicons with a full spectrum of virulence genes consistent with the carriage of ColV-like plasmids. Our data indicate that IncF plasmids play an important role in shaping virulence and resistance gene carriage in BSI in Australia.

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2020-05-06
2020-06-04
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References

  1. Diekema DJ, Hsueh P-R, Mendes RE, Pfaller MA, Rolston KV et al. The microbiology of bloodstream infection: 20-year trends from the SENTRY antimicrobial surveillance program. Antimicrob Agents Chemother 2019; 63: [CrossRef][PubMed][PubMed]
    [Google Scholar]
  2. Institute TG Stopping Sepsis A National Action Plan Sydney, Australia: Australian Sepsis Network; 2017
    [Google Scholar]
  3. Coombs G, Bell JM, Daley D, Collingnon P, Cooley L et al. Australian group on antimicrobial resistance sepsis outcomes programs: 2017 report. report. Sydney2019. Report No.: Sydney: ACSQHC; 2019
  4. Turnidge J, Gottlieb T, Bell JM. Enterobacteriaceae sepsis outcome programme (EnSOP) 2013 antimicrobial susceptibility report; 2014
  5. Ananias M, Yano T. Serogroups and virulence genotypes of Escherichia coli isolated from patients with sepsis. Braz J Med Biol Res 2008; 41:877–883 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  6. Johnson JR. Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev 1991; 4:80–128 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  7. Coombs G, Bell JM, Daley D, Collingnon P, Cooley L et al. Australian group on antimicrobial resistance. sepsis outcome programs 2016 report. Sydney2018 Contract No.: Sydney: ACSQHC 2018
    [Google Scholar]
  8. Abernethy J, Guy R, Sheridan EA, Hopkins S, Kiernan M et al. Epidemiology of Escherichia coli bacteraemia in England: results of an enhanced sentinel surveillance programme. J Hosp Infect 2017; 95:365–375 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  9. Gillings M, Boucher Y, Labbate M, Holmes A, Krishnan S et al. The evolution of class 1 integrons and the rise of antibiotic resistance. J Bacteriol 2008; 190:5095–5100 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  10. Hall RM, Stokes HW. Integrons: novel DNA elements which capture genes by site-specific recombination. Genetica 1993; 90:115–132 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  11. Gündoğdu A, Long YB, Vollmerhausen TL, Katouli M. Antimicrobial resistance and distribution of sul genes and integron-associated intI genes among uropathogenic Escherichia coli in Queensland, Australia. J Med Microbiol 2011; 60:1633–1642 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  12. Leverstein-van Hall MA, M Blok HE, T Donders AR, Paauw A, Fluit AC et al. Multidrug resistance among Enterobacteriaceae is strongly associated with the presence of integrons and is independent of species or isolate origin. J Infect Dis 2003; 187:251–259 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  13. Cummins ML, Reid CJ, Roy Chowdhury P, Bushell RN, Esbert N et al. Whole genome sequence analysis of Australian avian pathogenic Escherichia coli that carry the class 1 integrase gene. Microb Genom 2019; 5: [CrossRef][PubMed][PubMed]
    [Google Scholar]
  14. Djordjevic SP, Stokes HW, Roy Chowdhury P. 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 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  15. Reid CJ, Wyrsch ER, Roy Chowdhury P, Zingali T, Liu M et al. Porcine commensal Escherichia coli: a reservoir for class 1 integrons associated with IS26. Microb Genom 2017; 3: [CrossRef][PubMed][PubMed]
    [Google Scholar]
  16. Gillings MR. Integrons: past, present, and future. Microbiol Mol Biol Rev 2014; 78:257–277 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  17. Copur-Cicek A, Ozgumus OB, Saral A, Sandalli C. Antimicrobial resistance patterns and integron carriage of Escherichia coli isolates causing community-acquired infections in Turkey. Ann Lab Med 2014; 34:139–144 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  18. Horcajada JP, Soto S, Gajewski A, Smithson A, Jiménez de Anta MT et al. Quinolone-resistant uropathogenic Escherichia coli strains from phylogenetic group B2 have fewer virulence factors than their susceptible counterparts. J Clin Microbiol 2005; 43:2962–2964 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  19. Johnson JR, Kuskowski MA, O'Bryan TT, Maslow JN. Epidemiological correlates of virulence genotype and phylogenetic background among Escherichia coli blood isolates from adults with diverse-source bacteremia. J Infect Dis 2002; 185:1439–1447 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  20. Johnson JR, Kuskowski MA, Owens K, Gajewski A, Winokur PL. Phylogenetic origin and virulence genotype in relation to resistance to fluoroquinolones and/or extended-spectrum cephalosporins and cephamycins among Escherichia coli isolates from animals and humans. J Infect Dis 2003; 188:759–768 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  21. Moreno E, Prats G, Sabaté M, Pérez T, Johnson JR et al. Quinolone, fluoroquinolone and trimethoprim/sulfamethoxazole resistance in relation to virulence determinants and phylogenetic background among uropathogenic Escherichia coli. J Antimicrob Chemother 2006; 57:204–211 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  22. Carattoli A. Plasmids and the spread of resistance. Int J Med Microbiol 2013; 303:298–304 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  23. Rozwandowicz M, Brouwer MSM, Fischer J, Wagenaar JA, Gonzalez-Zorn B et al. Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. J Antimicrob Chemother 2018; 73:1121–1137 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  24. Crossman LC, Chaudhuri RR, Beatson SA, Wells TJ, Desvaux M et al. A commensal gone bad: complete genome sequence of the prototypical enterotoxigenic Escherichia coli strain H10407. J Bacteriol 2010; 192:5822–5831 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  25. Gaastra W, Svennerholm AM. Colonization factors of human enterotoxigenic Escherichia coli (ETEC). Trends Microbiol 1996; 4:444–452 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  26. Pasqua M, Michelacci V, Di Martino ML, Tozzoli R, Grossi M et al. The Intriguing Evolutionary Journey of Enteroinvasive E. coli (EIEC) toward Pathogenicity. Front Microbiol 2017; 8:2390 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  27. Croxall G, Hale J, Weston V, Manning G, Cheetham P et al. Molecular epidemiology of extraintestinal pathogenic Escherichia coli isolates from a regional cohort of elderly patients highlights the prevalence of ST131 strains with increased antimicrobial resistance in both community and hospital care settings. J Antimicrob Chemother 2011; 66:2501–2508 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  28. Riley LW. Pandemic lineages of extraintestinal pathogenic Escherichia coli. Clin Microbiol Infect 2014; 20:380–390 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  29. Andersen PS, Stegger M, Aziz M, Contente-Cuomo T, Gibbons HS et al. Complete Genome Sequence of the Epidemic and Highly Virulent CTX-M-15-Producing H30-Rx Subclone of Escherichia coli ST131. Genome Announc 2013; 1:e00988-13 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  30. 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:e00377–00313 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  31. Petty NK, Ben Zakour NL, Stanton-Cook M, Skippington E, Totsika M et al. Global dissemination of a multidrug resistant Escherichia coli clone. Proc Natl Acad Sci U S A 2014; 111:5694–5699 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  32. Totsika M, Beatson SA, Sarkar S, Phan M-D, Petty NK et al. Insights into a multidrug resistant Escherichia coli pathogen of the globally disseminated ST131 lineage: genome analysis and virulence mechanisms. PLoS One 2011; 6:e26578 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  33. Poirel L, Gniadkowski M, Nordmann P. Biochemical analysis of the ceftazidime-hydrolysing extended-spectrum beta-lactamase CTX-M-15 and of its structurally related beta-lactamase CTX-M-3. J Antimicrob Chemother 2002; 50:1031–1034 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  34. Poirel L, Kämpfer P, Nordmann P. Chromosome-encoded Ambler class A beta-lactamase of Kluyvera georgiana, a probable progenitor of a subgroup of CTX-M extended-spectrum beta-lactamases. Antimicrob Agents Chemother 2002; 46:4038–4040 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  35. Shaikh S, Fatima J, Shakil S, Rizvi SMD, Kamal MA. Antibiotic resistance and extended spectrum beta-lactamases: types, epidemiology and treatment. Saudi J Biol Sci 2015; 22:90–101 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  36. 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 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  37. Hwang J-H, Shin G-W, Hwang J-H, Lee C-S. Bloodstream infection due to CTX-M-15 and TEM-1 extended-spectrum β-lactamase-producing Salmonella enterica serovar Virchow ST16. Jpn J Infect Dis 2017; 70:308–310 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  38. Paterson DL, Bonomo RA. Extended-Spectrum beta-lactamases: a clinical update. Clin Microbiol Rev 2005; 18:657–686 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  39. Paterson DL, Hujer KM, Hujer AM, Yeiser B, Bonomo MD et al. Extended-spectrum beta-lactamases in Klebsiella pneumoniae bloodstream isolates from seven countries: dominance and widespread prevalence of SHV- and CTX-M-type beta-lactamases. Antimicrob Agents Chemother 2003; 47:3554–3560 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  40. Third Australian report on antimicrobial use and resistance in human health- AURA 2019-May 2019; [database on the Internet] 2019. Available from. https://www.safetyandquality.gov.au/our-work/antimicrobial-resistance/antimicrobial-use-and-resistance-australia-surveillance-system-aura/aura-2019
  41. Bell JM, Turnidge JD, Coombs GW, Daley DA, Gottlieb T et al. Australian group on antimicrobial resistance Australian Enterobacteriaceae sepsis outcome programme, annual report 2014. Australia: the Department of Health2016 contract No.: 2..
  42. Magiorakos A-P, Srinivasan A, Carey RB, Carmeli Y, Falagas ME et al. Multidrug-Resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012; 18:268–281 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  43. Darling AE, McKinnon J, Worden P, Santos J, Charles IG et al. A draft genome of Escherichia coli sequence type 127 strain 2009-46. Gut Pathog 2014; 6:32 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  44. Coil D, Jospin G, Darling AE. A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics 2015; 31:587–589 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  45. Brettin RastTK. Scientific Reports 2015; 8365:
    [Google Scholar]
  46. 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 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  47. 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 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  48. Darling AE, Jospin G, Lowe E, Matsen FA, Bik HM et al. PhyloSift: phylogenetic analysis of genomes and metagenomes. PeerJ 2014; 2:e243 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  49. Wickham H, Sievert C. ggplot 2: : Elegant Graphics for Data Analysis New York: Springer; 2016
    [Google Scholar]
  50. 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 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  51. Vangchhia B, Abraham S, Bell JM, Collignon P, Gibson JS et al. Phylogenetic diversity, antimicrobial susceptibility and virulence characteristics of phylogroup F Escherichia coli in Australia. Microbiology 2016; 162:1904–1912 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  52. Santos ACM, Zidko ACM, Pignatari AC, Silva RM. Assessing the diversity of the virulence potential of Escherichia coli isolated from bacteremia in São Paulo, Brazil. Braz J Med Biol Res 2013; 46:968–973 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  53. 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 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  54. Moran RA, Hall RM. Evolution of regions containing antibiotic resistance genes in FII-2-FIB-1 ColV-Colla virulence plasmids. Microb Drug Resist 2018; 24:411–421 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  55. 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 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  56. Day MJ, Doumith M, Abernethy J, Hope R, Reynolds R et al. Population structure of Escherichia coli causing bacteraemia in the UK and Ireland between 2001 and 2010. J Antimicrob Chemother 2016; 71:2139–2142 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  57. Coque TM, Novais A, Carattoli A, Poirel L, Pitout J et al. Dissemination of clonally related Escherichia coli strains expressing extended-spectrum beta-lactamase CTX-M-15. Emerg Infect Dis 2008; 14:195–200 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  58. 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; 27:14371449 [CrossRef]
    [Google Scholar]
  59. Bogema DR, McKinnon J, Liu M, Hitchick N, Miller N et al. Whole-genome analysis of extraintestinal Escherichia coli sequence type 73 from a single hospital over a 2 year period identified different circulating clonal groups. Microb Genom 2019
    [Google Scholar]
  60. Johnson TJ, Siek KE, Johnson SJ, Nolan LK. DNA sequence of a ColV plasmid and prevalence of selected plasmid-encoded virulence genes among avian Escherichia coli strains. J Bacteriol 2006; 188:745–758 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  61. 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 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  62. Peigne C, Bidet P, Mahjoub-Messai F, Plainvert C, Barbe V et al. The plasmid of Escherichia coli strain S88 (O45:K1:H7) that causes neonatal meningitis is closely related to avian pathogenic E. coli plasmids and is associated with high-level bacteremia in a neonatal rat meningitis model. Infect Immun 2009; 77:2272–2284 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  63. Ron EZ. Host specificity of septicemic Escherichia coli: human and avian pathogens. Curr Opin Microbiol 2006; 9:28–32 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  64. Reid CJ, McKinnon J, Djordjevic SP. Clonal ST131-H22 Escherichia coli strains from a healthy pig and a human urinary tract infection carry highly similar resistance and virulence plasmids. Microb Genom 2019; 5: [CrossRef]
    [Google Scholar]
  65. Skyberg JA, Johnson TJ, Johnson JR, Clabots C, Logue CM et al. Acquisition of avian pathogenic Escherichia coli plasmids by a commensal E. coli isolate enhances its abilities to kill chicken embryos, grow in human urine, and colonize the murine kidney. Infect Immun 2006; 74:6287–6292 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  66. Zhu Ge X, Jiang J, Pan Z, Hu L, Wang S et al. Comparative genomic analysis shows that avian pathogenic Escherichia coli isolate IMT5155 (O2:K1:H5; ST complex 95, ST140) shares close relationship with ST95 APEC O1:K1 and human ExPEC O18:K1 strains. PLoS One 2014; 9:e112048 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  67. Partridge SR, Tsafnat G, Coiera E, Iredell JR. Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 2009; 33:757–784 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  68. An X-L, Chen Q-L, Zhu D, Zhu Y-G, Gillings MR et al. Impact of wastewater treatment on the prevalence of integrons and the genetic diversity of integron gene cassettes. Appl Environ Microbiol 2018; 84: 01 05 2018 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  69. Reid CJ, Roy Chowdhury P, Djordjevic SP. Tn6026 and Tn6029 are found in complex resistance regions mobilised by diverse plasmids and chromosomal islands in multiple antibiotic resistant Enterobacteriaceae. Plasmid 2015; 80:127–137 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  70. Roy Chowdhury P, Charles IG, Djordjevic SP. A role for Tn6029 in the evolution of the complex antibiotic resistance gene loci in genomic island 3 in enteroaggregative hemorrhagic Escherichia coli O104:H4. PLoS One 2015; 10:e0115781 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  71. Roy Chowdhury P, Ingold A, Vanegas N, Martínez E, Merlino J et al. Dissemination of multiple drug resistance genes by class 1 integrons in Klebsiella pneumoniae isolates from four countries: a comparative study. Antimicrob Agents Chemother 2011; 55:3140–3149 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  72. Roy Chowdhury P, 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 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  73. 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 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  74. Gillings MR. Class 1 integrons as invasive species. Curr Opin Microbiol 2017; 38:10–15 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  75. Harmer CJ, Hall RM. IS26-mediated precise excision of the IS26-aphA1a translocatable unit. mBio 2015; 6:e01866–01815 [CrossRef][PubMed][PubMed]
    [Google Scholar]
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