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Prevalence and Epidemiology of Non-O157 Escherichia coli Serogroups O26, O103, O111, and O145 and Shiga Toxin Gene Carriage in Scottish Cattle, 2014–2015

Cattle are a reservoir for Shiga toxin-producing Escherichia coli (STEC), zoonotic pathogens that cause serious clinical disease. Scotland has a higher incidence of STEC infection in the human population than the European average. The aim of this study was to investigate the prevalence and epidemiol...

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Autores principales: Hoyle, Deborah V., Keith, Marianne, Williamson, Helen, Macleod, Kareen, Mathie, Heather, Handel, Ian, Currie, Carol, Holmes, Anne, Allison, Lesley, McLean, Rebecca, Callaby, Rebecca, Porphyre, Thibaud, Tongue, Sue C., Henry, Madeleine K., Evans, Judith, Gunn, George J., Gally, David L., Silva, Nuno, Chase-Topping, Margo E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8117755/
https://www.ncbi.nlm.nih.gov/pubmed/33712425
http://dx.doi.org/10.1128/AEM.03142-20
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author Hoyle, Deborah V.
Keith, Marianne
Williamson, Helen
Macleod, Kareen
Mathie, Heather
Handel, Ian
Currie, Carol
Holmes, Anne
Allison, Lesley
McLean, Rebecca
Callaby, Rebecca
Porphyre, Thibaud
Tongue, Sue C.
Henry, Madeleine K.
Evans, Judith
Gunn, George J.
Gally, David L.
Silva, Nuno
Chase-Topping, Margo E.
author_facet Hoyle, Deborah V.
Keith, Marianne
Williamson, Helen
Macleod, Kareen
Mathie, Heather
Handel, Ian
Currie, Carol
Holmes, Anne
Allison, Lesley
McLean, Rebecca
Callaby, Rebecca
Porphyre, Thibaud
Tongue, Sue C.
Henry, Madeleine K.
Evans, Judith
Gunn, George J.
Gally, David L.
Silva, Nuno
Chase-Topping, Margo E.
author_sort Hoyle, Deborah V.
collection PubMed
description Cattle are a reservoir for Shiga toxin-producing Escherichia coli (STEC), zoonotic pathogens that cause serious clinical disease. Scotland has a higher incidence of STEC infection in the human population than the European average. The aim of this study was to investigate the prevalence and epidemiology of non-O157 serogroups O26, O103, O111, and O145 and Shiga toxin gene carriage in Scottish cattle. Fecal samples (n = 2783) were collected from 110 herds in 2014 and 2015 and screened by real-time PCR. Herd-level prevalence (95% confidence interval [CI]) for O103, O26, and O145 was estimated as 0.71 (0.62, 0.79), 0.43 (0.34, 0.52), and 0.23 (0.16, 0.32), respectively. Only two herds were positive for O111. Shiga toxin prevalence was high in both herds and pats, particularly for stx(2) (herd level: 0.99; 95% CI: 0.94, 1.0). O26 bacterial strains were isolated from 36 herds on culture. Fifteen herds yielded O26 stx-positive isolates that additionally harbored the intimin gene; six of these herds shed highly pathogenic stx(2)-positive strains. Multiple serogroups were detected in herds and pats, with only 25 herds negative for all serogroups. Despite overlap in detection, regional and seasonal effects were observed. Higher herd prevalence for O26, O103, and stx(1) occurred in the South West, and this region was significant for stx(2) at the pat level (P = 0.015). Significant seasonal variation was observed for O145 prevalence, with the highest prevalence in autumn (P = 0.032). Negative herds were associated with Central Scotland and winter. Herds positive for all serogroups were associated with autumn and larger herd size and were not housed at sampling. IMPORTANCE Cattle are reservoirs for Shiga toxin-producing Escherichia coli (STEC), bacteria shed in animal feces. Humans are infected through consumption of contaminated food or water and by direct contact, resulting in serious disease and kidney failure in the most vulnerable. The contribution of non-O157 serogroups to STEC illness was underestimated for many years due to the lack of specific tests. Recently, non-O157 human cases have increased, with O26 STEC of particular note. It is therefore vital to investigate the level and composition of non-O157 in the cattle reservoir and to compare them historically and by the clinical situation. In this study, we found cattle prevalence high for toxin, as well as for O103 and O26 serogroups. Pathogenic O26 STEC were isolated from 14% of study herds, with toxin subtypes similar to those seen in Scottish clinical cases. This study highlights the current risk to public health from non-O157 STEC in Scottish cattle.
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spelling pubmed-81177552021-05-18 Prevalence and Epidemiology of Non-O157 Escherichia coli Serogroups O26, O103, O111, and O145 and Shiga Toxin Gene Carriage in Scottish Cattle, 2014–2015 Hoyle, Deborah V. Keith, Marianne Williamson, Helen Macleod, Kareen Mathie, Heather Handel, Ian Currie, Carol Holmes, Anne Allison, Lesley McLean, Rebecca Callaby, Rebecca Porphyre, Thibaud Tongue, Sue C. Henry, Madeleine K. Evans, Judith Gunn, George J. Gally, David L. Silva, Nuno Chase-Topping, Margo E. Appl Environ Microbiol Public and Environmental Health Microbiology Cattle are a reservoir for Shiga toxin-producing Escherichia coli (STEC), zoonotic pathogens that cause serious clinical disease. Scotland has a higher incidence of STEC infection in the human population than the European average. The aim of this study was to investigate the prevalence and epidemiology of non-O157 serogroups O26, O103, O111, and O145 and Shiga toxin gene carriage in Scottish cattle. Fecal samples (n = 2783) were collected from 110 herds in 2014 and 2015 and screened by real-time PCR. Herd-level prevalence (95% confidence interval [CI]) for O103, O26, and O145 was estimated as 0.71 (0.62, 0.79), 0.43 (0.34, 0.52), and 0.23 (0.16, 0.32), respectively. Only two herds were positive for O111. Shiga toxin prevalence was high in both herds and pats, particularly for stx(2) (herd level: 0.99; 95% CI: 0.94, 1.0). O26 bacterial strains were isolated from 36 herds on culture. Fifteen herds yielded O26 stx-positive isolates that additionally harbored the intimin gene; six of these herds shed highly pathogenic stx(2)-positive strains. Multiple serogroups were detected in herds and pats, with only 25 herds negative for all serogroups. Despite overlap in detection, regional and seasonal effects were observed. Higher herd prevalence for O26, O103, and stx(1) occurred in the South West, and this region was significant for stx(2) at the pat level (P = 0.015). Significant seasonal variation was observed for O145 prevalence, with the highest prevalence in autumn (P = 0.032). Negative herds were associated with Central Scotland and winter. Herds positive for all serogroups were associated with autumn and larger herd size and were not housed at sampling. IMPORTANCE Cattle are reservoirs for Shiga toxin-producing Escherichia coli (STEC), bacteria shed in animal feces. Humans are infected through consumption of contaminated food or water and by direct contact, resulting in serious disease and kidney failure in the most vulnerable. The contribution of non-O157 serogroups to STEC illness was underestimated for many years due to the lack of specific tests. Recently, non-O157 human cases have increased, with O26 STEC of particular note. It is therefore vital to investigate the level and composition of non-O157 in the cattle reservoir and to compare them historically and by the clinical situation. In this study, we found cattle prevalence high for toxin, as well as for O103 and O26 serogroups. Pathogenic O26 STEC were isolated from 14% of study herds, with toxin subtypes similar to those seen in Scottish clinical cases. This study highlights the current risk to public health from non-O157 STEC in Scottish cattle. American Society for Microbiology 2021-04-27 /pmc/articles/PMC8117755/ /pubmed/33712425 http://dx.doi.org/10.1128/AEM.03142-20 Text en Copyright © 2021 Hoyle et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Public and Environmental Health Microbiology
Hoyle, Deborah V.
Keith, Marianne
Williamson, Helen
Macleod, Kareen
Mathie, Heather
Handel, Ian
Currie, Carol
Holmes, Anne
Allison, Lesley
McLean, Rebecca
Callaby, Rebecca
Porphyre, Thibaud
Tongue, Sue C.
Henry, Madeleine K.
Evans, Judith
Gunn, George J.
Gally, David L.
Silva, Nuno
Chase-Topping, Margo E.
Prevalence and Epidemiology of Non-O157 Escherichia coli Serogroups O26, O103, O111, and O145 and Shiga Toxin Gene Carriage in Scottish Cattle, 2014–2015
title Prevalence and Epidemiology of Non-O157 Escherichia coli Serogroups O26, O103, O111, and O145 and Shiga Toxin Gene Carriage in Scottish Cattle, 2014–2015
title_full Prevalence and Epidemiology of Non-O157 Escherichia coli Serogroups O26, O103, O111, and O145 and Shiga Toxin Gene Carriage in Scottish Cattle, 2014–2015
title_fullStr Prevalence and Epidemiology of Non-O157 Escherichia coli Serogroups O26, O103, O111, and O145 and Shiga Toxin Gene Carriage in Scottish Cattle, 2014–2015
title_full_unstemmed Prevalence and Epidemiology of Non-O157 Escherichia coli Serogroups O26, O103, O111, and O145 and Shiga Toxin Gene Carriage in Scottish Cattle, 2014–2015
title_short Prevalence and Epidemiology of Non-O157 Escherichia coli Serogroups O26, O103, O111, and O145 and Shiga Toxin Gene Carriage in Scottish Cattle, 2014–2015
title_sort prevalence and epidemiology of non-o157 escherichia coli serogroups o26, o103, o111, and o145 and shiga toxin gene carriage in scottish cattle, 2014–2015
topic Public and Environmental Health Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8117755/
https://www.ncbi.nlm.nih.gov/pubmed/33712425
http://dx.doi.org/10.1128/AEM.03142-20
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