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 Hanson; Mark Woolhouse; Xavier Didelot; Claire Jenkins; David L Gally

doi:10.1099/mgen.0.001090

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

Research output: Contribution to journal › Article › Academic › peer-review

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 language	English
Article number	001090
Number of pages	12
Journal	Microbial genomics
Volume	9
Issue number	9
DOIs	https://doi.org/10.1099/mgen.0.001090
Publication status	Published - 1 Sept 2023

Bibliographical note

Publisher Copyright:
© 2023, Microbiology Society. All rights reserved.

Funding

Food Standards Scotland and Food Standards Agency (Project No. FS101055) BBSRC grant no: BB/P02095X/1. Timothy Dallman, Xavier Didelot and Claire Jenkins are affiliated to the National Institute for Health Research Health Protection Research Unit (NIHR HPRU) in Gastrointestinal Infections at the University of Liverpool in partnership with Public Health England (PHE), in collaboration with the University of Warwick. Timothy Dallman and Xavier Didelot are affiliated to the NIHR HPRU in Genomics and Enabling Data. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR, the Department of Health and Social Care or Public Health England. For the purpose of open access, the author has applied a CC-BY public copyright licence to any Author Accepted Manuscript version arising from this submission.

Funders	Funder number
Biotechnology and Biological Sciences Research Council	BB/P02095X/1
National Institute for Health and Care Research
University of Warwick
University of Liverpool
Public Health England

Keywords

E. coli O157
STEC
phage type
whole genome sequencing

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1099/mgen.0.001090Licence: CC BY

mgen001090Final published version, 997 KBLicence: CC BY

Cite this

Chase-Topping, M., Dallman, T. J., Allison, L., Lupolova, N., Matthews, L., Mitchell, S., Banks, C. J., Prentice, J., Brown, H., Tongue, S., Henry, M., Evans, J., Gunn, G., Hoyle, D., McNeilly, T. N., Fitzgerald, S., Smith-Palmer, A., Shaaban, S., Holmes, A., ... Gally, D. L. (2023). Analysis of Escherichia coli O157 strains in cattle and humans between Scotland and England & Wales: implications for human health. Microbial genomics, 9(9), Article 001090. https://doi.org/10.1099/mgen.0.001090

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

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. ",

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Chase-Topping, M, Dallman, TJ, Allison, L, Lupolova, N, Matthews, L, Mitchell, S, Banks, CJ, Prentice, J, Brown, H, Tongue, S, Henry, M, Evans, J, Gunn, G, Hoyle, D, McNeilly, TN, Fitzgerald, S, Smith-Palmer, A, Shaaban, S, Holmes, A, Hanson, M, Woolhouse, M, Didelot, X, Jenkins, C & Gally, DL 2023, 'Analysis of Escherichia coli O157 strains in cattle and humans between Scotland and England & Wales: implications for human health.', Microbial genomics, vol. 9, no. 9, 001090. https://doi.org/10.1099/mgen.0.001090

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T2 - implications for human health.

AU - Chase-Topping, Margo

AU - Dallman, Timothy J

AU - Allison, Lesley

AU - Lupolova, Nadejda

AU - Matthews, Louise

AU - Mitchell, Sonia

AU - Banks, Christopher J

AU - Prentice, Jamie

AU - Brown, Helen

AU - Tongue, Sue

AU - Henry, Madeleine

AU - Evans, Judith

AU - Gunn, George

AU - Hoyle, Deborah

AU - McNeilly, Tom N

AU - Fitzgerald, Stephen

AU - Smith-Palmer, Alison

AU - Shaaban, Sharif

AU - Holmes, Anne

AU - Hanson, Mary

AU - Woolhouse, Mark

AU - Didelot, Xavier

AU - Jenkins, Claire

AU - Gally, David L

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N2 - 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.

AB - 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.

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