1887

Abstract

We examined whether genomic surveillance of Escherichia coli in wastewater could capture the dominant E. coli lineages associated with bloodstream infection and livestock in the East of England, together with the antibiotic-resistance genes circulating in the wider E. coli population. Treated and untreated wastewater was taken from 20 municipal treatment plants in the East of England, half in direct receipt of acute hospital waste. All samples were culture positive for E. coli , and all but one were positive for extended-spectrum β-lactamase (ESBL)-producing E. coli . The most stringent wastewater treatment (tertiary including UV light) did not eradicate ESBL- E. coli in 2/3 cases. We sequenced 388 E. coli (192 ESBL, 196 non-ESBL). Multilocus sequence type (ST) diversity was similar between plants in direct receipt of hospital waste versus the remainder (93 vs 95 STs, respectively). We compared the genomes of wastewater E. coli with isolates from bloodstream infection (n=437), and livestock farms and retail meat (n=431) in the East of England. A total of 19/20 wastewater plants contained one or more of the three most common STs associated with bloodstream infection (ST131, ST73, ST95), and 14/20 contained the most common livestock ST (ST10). In an analysis of 1254 genomes (2 cryptic E. coli were excluded), wastewater isolates were distributed across the phylogeny and intermixed with isolates from humans and livestock. Ten bla CTX-M elements were identified in E. coli isolated from wastewater, together with a further 47 genes encoding resistance to the major antibiotic drug groups. Genes encoding resistance to colistin and the carbapenems were not detected. Genomic surveillance of E. coli in wastewater could be used to monitor new and circulating lineages and resistance determinants of public-health importance.

Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000267
2019-05-20
2019-08-22
Loading full text...

Full text loading...

/deliver/fulltext/mgen/5/5/mgen000267.html?itemId=/content/journal/mgen/10.1099/mgen.0.000267&mimeType=html&fmt=ahah

References

  1. Tumbarello M, Spanu T, Di Bidino R, Marchetti M, Ruggeri M et al. Costs of bloodstream infections caused by Escherichia coli and influence of extended-spectrum-β-lactamase production and inadequate initial antibiotic therapy. Antimicrob Agents Chemother 2010;54:4085–4091 [CrossRef]
    [Google Scholar]
  2. Public Health England English Surveillance Programme for Antimicrobial Utilisation and Resistance (ESPAUR) Report London: Public Health England; 2017
  3. Schwaber MJ, Carmeli Y. Mortality and delay in effective therapy associated with extended-spectrum β-lactamase production in Enterobacteriaceae bacteraemia: a systematic review and meta-analysis. J Antimicrob Chemother 2007;60:913–920 [CrossRef]
    [Google Scholar]
  4. Roberts RR, Hota B, Ahmad I, Scott RD, Foster SD et al. Hospital and societal costs of antimicrobial-resistant infections in a Chicago teaching hospital: implications for antibiotic stewardship. Clin Infect Dis 2009;49:1175–1184 [CrossRef]
    [Google Scholar]
  5. Larsson DGJ, Andremont A, Bengtsson-Palme J, Brandt KK, de Roda Husman AM et al. Critical knowledge gaps and research needs related to the environmental dimensions of antibiotic resistance. Environ Int 2018;117:132–138 [CrossRef]
    [Google Scholar]
  6. Kwak Y-K, Colque P, Byfors S, Giske CG, Möllby R et al. Surveillance of antimicrobial resistance among Escherichia coli in wastewater in Stockholm during 1 year: does it reflect the resistance trends in the society?. Int J Antimicrob Agents 2015;45:25–32 [CrossRef]
    [Google Scholar]
  7. Galvin S, Boyle F, Hickey P, Vellinga A, Morris D et al. Enumeration and characterization of antimicrobial-resistant Escherichia coli bacteria in effluent from municipal, hospital, and secondary treatment facility sources. Appl Environ Microbiol 2010;76:4772–4779 [CrossRef]
    [Google Scholar]
  8. Blaak H, Lynch G, Italiaander R, Hamidjaja RA, Schets FM et al. Multidrug-resistant and extended spectrum beta-lactamase-producing Escherichia coli in Dutch surface water and wastewater. PLoS One 2015;10:e0127752 [CrossRef]
    [Google Scholar]
  9. Su J-Q, An X-L, Li B, Chen Q-L, Gillings MR et al. Metagenomics of urban sewage identifies an extensively shared antibiotic resistome in China. Microbiome 2017;5:84 [CrossRef]
    [Google Scholar]
  10. Jørgensen SB, Søraas AV, Arnesen LS, Leegaard TM, Sundsfjord A et al. A comparison of extended spectrum β-lactamase producing Escherichia coli from clinical, recreational water and wastewater samples associated in time and location. PLoS One 2017;12:e0186576 [CrossRef]
    [Google Scholar]
  11. Runcharoen C, Raven KE, Reuter S, Kallonen T, Paksanont S et al. Whole genome sequencing of ESBL-producing Escherichia coli isolated from patients, farm waste and canals in Thailand. Genome Med 2017;9:81 [CrossRef]
    [Google Scholar]
  12. DEFRA Waste Water Treatment in the United Kingdom – 2012: Implementation of the European Union Urban Waste Water Treatment Directive – 91/271/EEC London: DEFRA; 2012
  13. 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 [CrossRef]
    [Google Scholar]
  14. Ludden C, Raven KE, Jamrozy D, Gouliouris T, Blane B et al. One health genomic surveillance of Escherichia coli demonstrates distinct lineages and mobile genetic elements in isolates from humans versus livestock. MBio 2019;10:e02693-18 [CrossRef]
    [Google Scholar]
  15. Page AJ, Keane JA, Delaney AJ, Taylor B, Seemann T et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genom 2016;2:000056 [CrossRef]
    [Google Scholar]
  16. 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 [CrossRef]
    [Google Scholar]
  17. Bréchet C, Plantin J, Sauget M, Thouverez M, Talon D et al. Wastewater treatment plants release large amounts of extended-spectrum β-lactamase-producing Escherichia coli into the environment. Clin Infect Dis 2014;58:1658–1665 [CrossRef]
    [Google Scholar]
  18. Colomer-Lluch M, Mora A, López C, Mamani R, Dahbi G et al. Detection of quinolone-resistant Escherichia coli isolates belonging to clonal groups O25b:H4-B2-ST131 and O25b:H4-D-ST69 in raw sewage and river water in Barcelona, Spain. J Antimicrob Chemother 2013;68:758–765 [CrossRef]
    [Google Scholar]
  19. Dhanji H, Murphy NM, Akhigbe C, Doumith M, Hope R et al. Isolation of fluoroquinolone-resistant O25b:H4-ST131 Escherichia coli with CTX-M-14 extended-spectrum β-lactamase from UK river water. J Antimicrob Chemother 2011;66:512–516 [CrossRef]
    [Google Scholar]
  20. Dolejska M, Frolkova P, Florek M, Jamborova I, Purgertova M et al. CTX-M-15-producing Escherichia coli clone B2-O25b-ST131 and Klebsiella spp. isolates in municipal wastewater treatment plant effluents. J Antimicrob Chemother 2011;66:2784–2790 [CrossRef]
    [Google Scholar]
  21. Ben Zakour NL, Alsheikh-Hussain AS, Ashcroft MM, Khanh Nhu NT, Roberts LW et al. Sequential acquisition of virulence and fluoroquinolone resistance has shaped the evolution of Escherichia coli ST131. mBio 2016;7:e00347-16
    [Google Scholar]
  22. Hu Y-Y, Cai J-C, Zhou H-W, Chi D, Zhang X-F et al. Molecular typing of CTX-M-producing Escherichia coli isolates from environmental water, swine feces, specimens from healthy humans, and human patients. Appl Environ Microbiol 2013;79:5988–5996 [CrossRef]
    [Google Scholar]
  23. Bäumlisberger M, Youssar L, Schilhabel MB, Jonas D. Influence of a non-hospital medical care facility on antimicrobial resistance in wastewater. PLoS One 2015;10:e0122635 [CrossRef]
    [Google Scholar]
  24. Doumith M, Godbole G, Ashton P, Larkin L, Dallman T et al. Detection of the plasmid-mediated mcr-1 gene conferring colistin resistance in human and food isolates of Salmonella enterica and Escherichia coli in England and Wales. J Antimicrob Chemother 2016;71:2300–2305 [CrossRef]
    [Google Scholar]
  25. Cai L, Ju F, Zhang T. Tracking human sewage microbiome in a municipal wastewater treatment plant. Appl Microbiol Biotechnol 2014;98:3317–3326
    [Google Scholar]
  26. Public Health England Preventing Healthcare Associated Gram-negative Bloodstream Infections: an Improvement Resource London: Public Health England; 2017
  27. Mahon BM, Brehony C, McGrath E, Killeen J, Cormican M et al. Indistinguishable NDM-producing Escherichia coli isolated from recreational waters, sewage, and a clinical specimen in Ireland, 2016 to 2017. Eurosurveillance 2017;22:30513 [CrossRef]
    [Google Scholar]
  28. Amos GCA, Hawkey PM, Gaze WH, Wellington EM. Waste water effluent contributes to the dissemination of CTX-M-15 in the natural environment. J Antimicrob Chemother 2014;69:1785–1791 [CrossRef]
    [Google Scholar]
  29. Reeves PR, Liu B, Zhou Z, Li D, Guo D et al. Rates of mutation and host transmission for an Escherichia coli clone over 3 years. PLoS One 2011;6:e26907 [CrossRef]
    [Google Scholar]
  30. Stoesser N, Sheppard AE, Pankhurst L, De Maio N, Moore CE et al. Evolutionary history of the global emergence of the Escherichia coli epidemic clone ST131. MBio 2016;7:e02162 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000267
Loading
/content/journal/mgen/10.1099/mgen.0.000267
Loading

Data & Media loading...

Supplementary material 1

PDF

Supplementary material 1

Most Cited This Month

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