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

Author:

Chase-Topping Margo1ORCID,Dallman Timothy J.21,Allison Lesley3,Lupolova Nadejda1,Matthews Louise4,Mitchell Sonia4ORCID,Banks Christopher J.1,Prentice Jamie4,Brown Helen1,Tongue Sue5,Henry Madeleine5,Evans Judith5,Gunn George5,Hoyle Deborah1,McNeilly Tom N.6,Fitzgerald Stephen61,Smith-Palmer Alison7,Shaaban Sharif3,Holmes Anne3,Hanson Mary3,Woolhouse Mark8,Didelot Xavier9,Jenkins Claire2,Gally David L.1

Affiliation:

1. The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh EH25 9RG, UK

2. Gastrointestinal Bacteria Reference Unit, Public Health England, London NW9 5HT, UK

3. Scottish E. coli O157/STEC Reference Laboratory, Royal Infirmary of Edinburgh, Edinburgh EH16 4SA, UK

4. Institute of Biodiversity, Animal Health & Comparative Medicine, University of Glasgow, Glasgow G12 8QQ, UK

5. Epidemiology Research Unit, Scotland’s Rural College, Inverness IV2 5NA, UK

6. Moredun Research Institute, Pentlands Science Park, Penicuik EH26 0PZ, UK

7. Public Health Scotland, Glasgow G2 6QE, UK

8. Usher Institute, University of Edinburgh, Edinburgh EH9 3DL, UK

9. School of Life Sciences and Department of Statistics, University of Warwick, Warwick CV4 7AL, UK

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.

Funder

Food Standards Agency

BBSRC

Publisher

Microbiology Society

Subject

General Medicine

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