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Cross-Border Transmission of Salmonella Choleraesuis var. Kunzendorf in European Pigs and Wild Boar: Infection, Genetics, and Evolution

Salmonella enterica subspecies enterica serotype Choleraesuis is a swine adapted serovar. S. Choleraesuis variant Kunzendorf is responsible for the majority of outbreaks among pigs. S. Choleraesuis is rare in Europe, although there have been serious outbreaks in pigs including two outbreaks in Denma...

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Autores principales: Leekitcharoenphon, Pimlapas, Sørensen, Gitte, Löfström, Charlotta, Battisti, Antonio, Szabo, Istvan, Wasyl, Dariusz, Slowey, Rosemarie, Zhao, Shaohua, Brisabois, Anne, Kornschober, Christian, Kärssin, Age, Szilárd, Jánosi, Černý, Tomáš, Svendsen, Christina Aaby, Pedersen, Karl, Aarestrup, Frank M., Hendriksen, Rene S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6373457/
https://www.ncbi.nlm.nih.gov/pubmed/30787923
http://dx.doi.org/10.3389/fmicb.2019.00179
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author Leekitcharoenphon, Pimlapas
Sørensen, Gitte
Löfström, Charlotta
Battisti, Antonio
Szabo, Istvan
Wasyl, Dariusz
Slowey, Rosemarie
Zhao, Shaohua
Brisabois, Anne
Kornschober, Christian
Kärssin, Age
Szilárd, Jánosi
Černý, Tomáš
Svendsen, Christina Aaby
Pedersen, Karl
Aarestrup, Frank M.
Hendriksen, Rene S.
author_facet Leekitcharoenphon, Pimlapas
Sørensen, Gitte
Löfström, Charlotta
Battisti, Antonio
Szabo, Istvan
Wasyl, Dariusz
Slowey, Rosemarie
Zhao, Shaohua
Brisabois, Anne
Kornschober, Christian
Kärssin, Age
Szilárd, Jánosi
Černý, Tomáš
Svendsen, Christina Aaby
Pedersen, Karl
Aarestrup, Frank M.
Hendriksen, Rene S.
author_sort Leekitcharoenphon, Pimlapas
collection PubMed
description Salmonella enterica subspecies enterica serotype Choleraesuis is a swine adapted serovar. S. Choleraesuis variant Kunzendorf is responsible for the majority of outbreaks among pigs. S. Choleraesuis is rare in Europe, although there have been serious outbreaks in pigs including two outbreaks in Denmark in 1999–2000 and 2012–2013. Here, we elucidate the epidemiology, possible transmission routes and sources, and clonality of European S. Choleraesuis isolates including the Danish outbreak isolates. A total of 102 S. Choleraesuis isolates from different European countries and the United States, covering available isolates from the last two decades were selected for whole genome sequencing. We applied a temporally structured sequence analysis within a Bayesian framework to reconstruct a temporal and spatial phylogenetic tree. MLST type, resistance genes, plasmid replicons, and accessory genes were identified using bioinformatics tools. Fifty-eight isolates including 11 out of 12 strains from wild boars were pan-susceptible. The remaining isolates carried multiple resistance genes. Eleven different plasmid replicons in eight plasmids were determined among the isolates. Accessory genes were associated to the identified resistance genes and plasmids. The European S. Choleraesuis was estimated to have emerged in ∼1837 (95% credible interval, 1733–1983) with the mutation rate of 1.02 SNPs/genome/year. The isolates were clustered according to countries and neighbor countries. There were transmission events between strains from the United States and European countries. Wild boar and pig isolates were genetically linked suggesting cross-border transmission and transmission due to a wildlife reservoir. The phylogenetic tree shows that multiple introductions were responsible for the outbreak of 2012–2013 in Denmark, and suggests that poorly disinfected vehicles crossing the border into Denmark were potentially the source of the outbreak. Low levels of single nucleotide polymorphisms (SNPs) differences (0–4 SNPs) can be observed between clonal strains isolated from different organs of the same animal. Proper disinfection of livestock vehicles and improved quality control of livestock feed could help to prevent future spread of S. Choleraesuis or other more serious infectious diseases such as African swine fever (ASF) in the European pig production system.
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spelling pubmed-63734572019-02-20 Cross-Border Transmission of Salmonella Choleraesuis var. Kunzendorf in European Pigs and Wild Boar: Infection, Genetics, and Evolution Leekitcharoenphon, Pimlapas Sørensen, Gitte Löfström, Charlotta Battisti, Antonio Szabo, Istvan Wasyl, Dariusz Slowey, Rosemarie Zhao, Shaohua Brisabois, Anne Kornschober, Christian Kärssin, Age Szilárd, Jánosi Černý, Tomáš Svendsen, Christina Aaby Pedersen, Karl Aarestrup, Frank M. Hendriksen, Rene S. Front Microbiol Microbiology Salmonella enterica subspecies enterica serotype Choleraesuis is a swine adapted serovar. S. Choleraesuis variant Kunzendorf is responsible for the majority of outbreaks among pigs. S. Choleraesuis is rare in Europe, although there have been serious outbreaks in pigs including two outbreaks in Denmark in 1999–2000 and 2012–2013. Here, we elucidate the epidemiology, possible transmission routes and sources, and clonality of European S. Choleraesuis isolates including the Danish outbreak isolates. A total of 102 S. Choleraesuis isolates from different European countries and the United States, covering available isolates from the last two decades were selected for whole genome sequencing. We applied a temporally structured sequence analysis within a Bayesian framework to reconstruct a temporal and spatial phylogenetic tree. MLST type, resistance genes, plasmid replicons, and accessory genes were identified using bioinformatics tools. Fifty-eight isolates including 11 out of 12 strains from wild boars were pan-susceptible. The remaining isolates carried multiple resistance genes. Eleven different plasmid replicons in eight plasmids were determined among the isolates. Accessory genes were associated to the identified resistance genes and plasmids. The European S. Choleraesuis was estimated to have emerged in ∼1837 (95% credible interval, 1733–1983) with the mutation rate of 1.02 SNPs/genome/year. The isolates were clustered according to countries and neighbor countries. There were transmission events between strains from the United States and European countries. Wild boar and pig isolates were genetically linked suggesting cross-border transmission and transmission due to a wildlife reservoir. The phylogenetic tree shows that multiple introductions were responsible for the outbreak of 2012–2013 in Denmark, and suggests that poorly disinfected vehicles crossing the border into Denmark were potentially the source of the outbreak. Low levels of single nucleotide polymorphisms (SNPs) differences (0–4 SNPs) can be observed between clonal strains isolated from different organs of the same animal. Proper disinfection of livestock vehicles and improved quality control of livestock feed could help to prevent future spread of S. Choleraesuis or other more serious infectious diseases such as African swine fever (ASF) in the European pig production system. Frontiers Media S.A. 2019-02-06 /pmc/articles/PMC6373457/ /pubmed/30787923 http://dx.doi.org/10.3389/fmicb.2019.00179 Text en Copyright © 2019 Leekitcharoenphon, Sørensen, Löfström, Battisti, Szabo, Wasyl, Slowey, Zhao, Brisabois, Kornschober, Kärssin, Szilárd, Černý, Svendsen, Pedersen, Aarestrup and Hendriksen. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Leekitcharoenphon, Pimlapas
Sørensen, Gitte
Löfström, Charlotta
Battisti, Antonio
Szabo, Istvan
Wasyl, Dariusz
Slowey, Rosemarie
Zhao, Shaohua
Brisabois, Anne
Kornschober, Christian
Kärssin, Age
Szilárd, Jánosi
Černý, Tomáš
Svendsen, Christina Aaby
Pedersen, Karl
Aarestrup, Frank M.
Hendriksen, Rene S.
Cross-Border Transmission of Salmonella Choleraesuis var. Kunzendorf in European Pigs and Wild Boar: Infection, Genetics, and Evolution
title Cross-Border Transmission of Salmonella Choleraesuis var. Kunzendorf in European Pigs and Wild Boar: Infection, Genetics, and Evolution
title_full Cross-Border Transmission of Salmonella Choleraesuis var. Kunzendorf in European Pigs and Wild Boar: Infection, Genetics, and Evolution
title_fullStr Cross-Border Transmission of Salmonella Choleraesuis var. Kunzendorf in European Pigs and Wild Boar: Infection, Genetics, and Evolution
title_full_unstemmed Cross-Border Transmission of Salmonella Choleraesuis var. Kunzendorf in European Pigs and Wild Boar: Infection, Genetics, and Evolution
title_short Cross-Border Transmission of Salmonella Choleraesuis var. Kunzendorf in European Pigs and Wild Boar: Infection, Genetics, and Evolution
title_sort cross-border transmission of salmonella choleraesuis var. kunzendorf in european pigs and wild boar: infection, genetics, and evolution
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6373457/
https://www.ncbi.nlm.nih.gov/pubmed/30787923
http://dx.doi.org/10.3389/fmicb.2019.00179
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