Analysis of Escherichia coli O157 strains in cattle and humans between Scotland and England & Wales: implications for human health

Margo Chase-Topping*, Timothy J. Dallman, Lesley Allison, Nadejda Lupolova, Louise Matthews, Sonia Mitchell, Christopher J. Banks, Jamie Prentice, Helen Brown, Sue Tongue, Madeleine Henry, Judith Evans, George Gunn, Deborah Hoyle, Tom N. McNeilly, Stephen Fitzgerald, Alison Smith-Palmer, Sharif Shaaban, Anne Holmes, Mary HansonMark Woolhouse, Xavier Didelot, Claire Jenkins, David L. Gally

*Corresponding author for this work

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Abstract

For the last two decades, the human infection frequency of Escherichia coli O157 (O157) in Scotland has been 2.5-fold higher than in England and Wales. Results from national cattle surveys conducted in Scotland and England and Wales in 2014/2015 were combined with data on reported human clinical cases from the same time frame to determine if strain differences in national populations of O157 in cattle could be associated with higher human infection rates in Scotland. Shiga toxin subtype (Stx) and phage type (PT) were examined within and between host (cattle vs human) and nation (Scotland vs England and Wales). For a subset of the strains, whole genome sequencing (WGS) provided further insights into geographical and host association. All three major O157 lineages (I, II, I/II) and most sub-lineages (Ia, Ib, Ic, IIa, IIb, IIc) were represented in cattle and humans in both nations. While the relative contribution of different reservoir hosts to human infection is unknown, WGS analysis indicated that the majority of O157 diversity in human cases was captured by isolates from cattle. Despite comparable cattle O157 prevalence between nations, strain types were localized. PT21/28 (sub-lineage Ic, Stx2a+) was significantly more prevalent in Scottish cattle [odds ratio (OR) 8.7 (2.3-33.7; P<0.001] and humans [OR 2.2 (1.5-3.2); P<0.001]. In England and Wales, cattle had a significantly higher association with sub-lineage IIa strains [PT54, Stx2c; OR 5.6 (1.27-33.3); P=0.011] while humans were significantly more closely associated with sub-lineage IIb [PT8, Stx1 and Stx2c; OR 29 (4.9-1161); P<0.001]. Therefore, cattle farms in Scotland were more likely to harbour Stx2a+O157 strains compared to farms in E and W (P<0.001). There was evidence of limited cattle strain migration between nations and clinical isolates from one nation were more similar to cattle isolates from the same nation, with sub-lineage Ic (mainly PT21/28) exhibiting clear national association and evidence of local transmission in Scotland. While we propose the higher rate of O157 clinical cases in Scotland, compared to England and Wales, is a consequence of the nationally higher level of Stx2a+O157 strains in Scottish cattle, we discuss the multiple additional factors that may also contribute to the different infection rates between these nations.

Original languageEnglish
Article number001090
JournalMicrobial Genomics
Volume9
Issue number9
Early online date6 Sept 2023
DOIs
Publication statusFirst published - 6 Sept 2023

Keywords

  • E. coli O157
  • phage type
  • STEC
  • whole genome sequencing
  • Scotland/epidemiology
  • Animals
  • Cattle
  • Farms
  • Humans
  • Escherichia coli O157/genetics
  • England/epidemiology
  • Wales/epidemiology

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