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

Pimlapas Leekitcharoenphon*, Gitte Sørensen, Charlotta Lofstrom, Antonio Battisti, Istvan Szabo, Dariusz Wasyl, Rosemarie Slowey, Shaohua Zhao, Anne Brisabois, Christian Kornschober, Age Karssin, Janosi Szilard, Tomas Cerny, Christina Aaby Svendsen, Karl Pedersen, Frank Møller Aarestrup, Rene S. Hendriksen

*Corresponding author for this work

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Abstract

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.
Original languageEnglish
Article number179
JournalFrontiers in Microbiology
Volume10
Number of pages12
ISSN1664-302X
DOIs
Publication statusPublished - 2019

Keywords

  • Salmonella Choleraesuis
  • Kunzendorf
  • epidemiology
  • whole genome sequencing
  • phylogenetics transmission
  • wild boar
  • antimicrobial resistance genes

Cite this

Leekitcharoenphon, Pimlapas ; Sørensen, Gitte ; Lofstrom, Charlotta ; Battisti, Antonio ; Szabo, Istvan ; Wasyl, Dariusz ; Slowey, Rosemarie ; Zhao, Shaohua ; Brisabois, Anne ; Kornschober, Christian ; Karssin, Age ; Szilard, Janosi ; Cerny, Tomas ; Svendsen, Christina Aaby ; Pedersen, Karl ; Aarestrup, Frank Møller ; Hendriksen, Rene S. / Cross-Border Transmission of Salmonella Choleraesuis var. Kunzendorf in European Pigs and Wild Boar: Infection, Genetics, and Evolution. In: Frontiers in Microbiology. 2019 ; Vol. 10.
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abstract = "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.",
keywords = "Salmonella Choleraesuis, Kunzendorf, epidemiology, whole genome sequencing, phylogenetics transmission, wild boar, antimicrobial resistance genes",
author = "Pimlapas Leekitcharoenphon and Gitte S{\o}rensen and Charlotta Lofstrom and Antonio Battisti and Istvan Szabo and Dariusz Wasyl and Rosemarie Slowey and Shaohua Zhao and Anne Brisabois and Christian Kornschober and Age Karssin and Janosi Szilard and Tomas Cerny and Svendsen, {Christina Aaby} and Karl Pedersen and Aarestrup, {Frank M{\o}ller} and Hendriksen, {Rene S.}",
year = "2019",
doi = "10.3389/fmicb.2019.00179",
language = "English",
volume = "10",
journal = "Frontiers in Microbiology",
issn = "1664-302X",
publisher = "Frontiers Media S.A.",

}

Leekitcharoenphon, P, Sørensen, G, Lofstrom, C, Battisti, A, Szabo, I, Wasyl, D, Slowey, R, Zhao, S, Brisabois, A, Kornschober, C, Karssin, A, Szilard, J, Cerny, T, Svendsen, CA, Pedersen, K, Aarestrup, FM & Hendriksen, RS 2019, 'Cross-Border Transmission of Salmonella Choleraesuis var. Kunzendorf in European Pigs and Wild Boar: Infection, Genetics, and Evolution', Frontiers in Microbiology, vol. 10, 179. https://doi.org/10.3389/fmicb.2019.00179

Cross-Border Transmission of Salmonella Choleraesuis var. Kunzendorf in European Pigs and Wild Boar: Infection, Genetics, and Evolution. / Leekitcharoenphon, Pimlapas; Sørensen, Gitte; Lofstrom, Charlotta; Battisti, Antonio; Szabo, Istvan; Wasyl, Dariusz; Slowey, Rosemarie; Zhao, Shaohua; Brisabois, Anne; Kornschober, Christian; Karssin, Age; Szilard, Janosi; Cerny, Tomas; Svendsen, Christina Aaby; Pedersen, Karl; Aarestrup, Frank Møller; Hendriksen, Rene S.

In: Frontiers in Microbiology, Vol. 10, 179, 2019.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Cross-Border Transmission of Salmonella Choleraesuis var. Kunzendorf in European Pigs and Wild Boar: Infection, Genetics, and Evolution

AU - Leekitcharoenphon, Pimlapas

AU - Sørensen, Gitte

AU - Lofstrom, Charlotta

AU - Battisti, Antonio

AU - Szabo, Istvan

AU - Wasyl, Dariusz

AU - Slowey, Rosemarie

AU - Zhao, Shaohua

AU - Brisabois, Anne

AU - Kornschober, Christian

AU - Karssin, Age

AU - Szilard, Janosi

AU - Cerny, Tomas

AU - Svendsen, Christina Aaby

AU - Pedersen, Karl

AU - Aarestrup, Frank Møller

AU - Hendriksen, Rene S.

PY - 2019

Y1 - 2019

N2 - 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.

AB - 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.

KW - Salmonella Choleraesuis

KW - Kunzendorf

KW - epidemiology

KW - whole genome sequencing

KW - phylogenetics transmission

KW - wild boar

KW - antimicrobial resistance genes

U2 - 10.3389/fmicb.2019.00179

DO - 10.3389/fmicb.2019.00179

M3 - Journal article

VL - 10

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

M1 - 179

ER -