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

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 cas...

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Autores principales: Chase-Topping, Margo, Dallman, Timothy J., Allison, Lesley, Lupolova, Nadejda, Matthews, Louise, Mitchell, Sonia, Banks, Christopher J., Prentice, Jamie, Brown, Helen, Tongue, Sue, Henry, Madeleine, Evans, Judith, Gunn, George, Hoyle, Deborah, McNeilly, Tom N., Fitzgerald, Stephen, Smith-Palmer, Alison, Shaaban, Sharif, Holmes, Anne, Hanson, Mary, Woolhouse, Mark, Didelot, Xavier, Jenkins, Claire, Gally, David L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Microbiology Society 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10569735/
https://www.ncbi.nlm.nih.gov/pubmed/37672388
http://dx.doi.org/10.1099/mgen.0.001090
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author Chase-Topping, Margo
Dallman, Timothy J.
Allison, Lesley
Lupolova, Nadejda
Matthews, Louise
Mitchell, Sonia
Banks, Christopher J.
Prentice, Jamie
Brown, Helen
Tongue, Sue
Henry, Madeleine
Evans, Judith
Gunn, George
Hoyle, Deborah
McNeilly, Tom N.
Fitzgerald, Stephen
Smith-Palmer, Alison
Shaaban, Sharif
Holmes, Anne
Hanson, Mary
Woolhouse, Mark
Didelot, Xavier
Jenkins, Claire
Gally, David L.
author_facet Chase-Topping, Margo
Dallman, Timothy J.
Allison, Lesley
Lupolova, Nadejda
Matthews, Louise
Mitchell, Sonia
Banks, Christopher J.
Prentice, Jamie
Brown, Helen
Tongue, Sue
Henry, Madeleine
Evans, Judith
Gunn, George
Hoyle, Deborah
McNeilly, Tom N.
Fitzgerald, Stephen
Smith-Palmer, Alison
Shaaban, Sharif
Holmes, Anne
Hanson, Mary
Woolhouse, Mark
Didelot, Xavier
Jenkins, Claire
Gally, David L.
author_sort Chase-Topping, Margo
collection PubMed
description 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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spelling pubmed-105697352023-10-13 Analysis of Escherichia coli O157 strains in cattle and humans between Scotland and England & Wales: implications for human health Chase-Topping, Margo Dallman, Timothy J. Allison, Lesley Lupolova, Nadejda Matthews, Louise Mitchell, Sonia Banks, Christopher J. Prentice, Jamie Brown, Helen Tongue, Sue Henry, Madeleine Evans, Judith Gunn, George Hoyle, Deborah McNeilly, Tom N. Fitzgerald, Stephen Smith-Palmer, Alison Shaaban, Sharif Holmes, Anne Hanson, Mary Woolhouse, Mark Didelot, Xavier Jenkins, Claire Gally, David L. Microb Genom Research Articles 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. Microbiology Society 2023-09-06 /pmc/articles/PMC10569735/ /pubmed/37672388 http://dx.doi.org/10.1099/mgen.0.001090 Text en © 2023 The Authors https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
spellingShingle Research Articles
Chase-Topping, Margo
Dallman, Timothy J.
Allison, Lesley
Lupolova, Nadejda
Matthews, Louise
Mitchell, Sonia
Banks, Christopher J.
Prentice, Jamie
Brown, Helen
Tongue, Sue
Henry, Madeleine
Evans, Judith
Gunn, George
Hoyle, Deborah
McNeilly, Tom N.
Fitzgerald, Stephen
Smith-Palmer, Alison
Shaaban, Sharif
Holmes, Anne
Hanson, Mary
Woolhouse, Mark
Didelot, Xavier
Jenkins, Claire
Gally, David L.
Analysis of Escherichia coli O157 strains in cattle and humans between Scotland and England & Wales: implications for human health
title Analysis of Escherichia coli O157 strains in cattle and humans between Scotland and England & Wales: implications for human health
title_full Analysis of Escherichia coli O157 strains in cattle and humans between Scotland and England & Wales: implications for human health
title_fullStr Analysis of Escherichia coli O157 strains in cattle and humans between Scotland and England & Wales: implications for human health
title_full_unstemmed Analysis of Escherichia coli O157 strains in cattle and humans between Scotland and England & Wales: implications for human health
title_short Analysis of Escherichia coli O157 strains in cattle and humans between Scotland and England & Wales: implications for human health
title_sort analysis of escherichia coli o157 strains in cattle and humans between scotland and england & wales: implications for human health
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10569735/
https://www.ncbi.nlm.nih.gov/pubmed/37672388
http://dx.doi.org/10.1099/mgen.0.001090
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