Epidemiology of Salmonella enterica Serovar Dublin in Cattle and Humans in Denmark, 1996 to 2016: a Retrospective Whole-Genome-Based Study

Eglė Kudirkiene, Gitte Sørensen, Mia Torpdahl, Leonardo de Knegt, Liza R. Nielsen, Erik Rattenborg, Shahana Ahmed, John E Olsen*

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

Abstract

Salmonella Dublin is a cattle-adapted S. enterica serovar causing intestinal as well as systemic infection in its bovine host, and it is also a serious threat to human health. The present study was aimed to determine the population structure of S Dublin isolates obtained from Danish cattle herds, and to investigate how cattle isolates relate to Danish human isolates, as well as to non-Danish human and bovine isolates. Phylogenetic analysis of 197 Danish cattle isolates from 1996-2016 identified three major clades corresponding to distinct geographical regions of cattle herds. Persistence of closely related isolates within the same herd and their circulation between epidemiologically linked herds was demonstrated for a period of more than 20 years. These findings suggest that the lack of internal biosecurity, but to some extend also external biosecurity in the herds, have played an important role in long term persistence of S. Dublin in Danish cattle herds in the period investigated. The global population analysis revealed that Danish cattle isolates clustered separately from bovine isolates from other countries, whereas human isolates were geographically spread. Resistance genes were peculiar to Danish bovine isolates, only the isolates within one Danish clade were found to often harbour two plasmids of IncFII/IncFIB and IncN types, the latter plasmid encoding blaTEM-1, tetA and strA, strB antibiotic resistance genes.IMPORTANCE S. Dublin causes economic losses in cattle production and the bacterium is a public health concern. A surveillance and control program has been in place in Denmark since 2002 with the ultimate goal to eradicate S. Dublin from Danish cattle herds, however, a small proportion of herds have remained positive for many years. In this study, we demonstrated that herds with persistent infection often were infected with the same strain for many years, indicating that internal biosecurity has to be improved to curb the infection. Further, domestic human cases of S. Dublin infection in humans was found to be caused both by Danish cattle isolates and isolates acquired abroad. The study shows the strength of whole genome sequencing to obtain detailed information on epidemiology of S. Dublin, and allowed us to suggest internal biosecurity as a main mean to control this bacterium in Danish cattle herds.
Original languageEnglish
JournalApplied and Environmental Microbiology
ISSN0099-2240
DOIs
Publication statusAccepted/In press - 2020

Cite this

Kudirkiene, Eglė ; Sørensen, Gitte ; Torpdahl, Mia ; de Knegt, Leonardo ; Nielsen, Liza R. ; Rattenborg, Erik ; Ahmed, Shahana ; Olsen, John E. / Epidemiology of Salmonella enterica Serovar Dublin in Cattle and Humans in Denmark, 1996 to 2016: a Retrospective Whole-Genome-Based Study. In: Applied and Environmental Microbiology. 2020.
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title = "Epidemiology of Salmonella enterica Serovar Dublin in Cattle and Humans in Denmark, 1996 to 2016: a Retrospective Whole-Genome-Based Study",
abstract = "Salmonella Dublin is a cattle-adapted S. enterica serovar causing intestinal as well as systemic infection in its bovine host, and it is also a serious threat to human health. The present study was aimed to determine the population structure of S Dublin isolates obtained from Danish cattle herds, and to investigate how cattle isolates relate to Danish human isolates, as well as to non-Danish human and bovine isolates. Phylogenetic analysis of 197 Danish cattle isolates from 1996-2016 identified three major clades corresponding to distinct geographical regions of cattle herds. Persistence of closely related isolates within the same herd and their circulation between epidemiologically linked herds was demonstrated for a period of more than 20 years. These findings suggest that the lack of internal biosecurity, but to some extend also external biosecurity in the herds, have played an important role in long term persistence of S. Dublin in Danish cattle herds in the period investigated. The global population analysis revealed that Danish cattle isolates clustered separately from bovine isolates from other countries, whereas human isolates were geographically spread. Resistance genes were peculiar to Danish bovine isolates, only the isolates within one Danish clade were found to often harbour two plasmids of IncFII/IncFIB and IncN types, the latter plasmid encoding blaTEM-1, tetA and strA, strB antibiotic resistance genes.IMPORTANCE S. Dublin causes economic losses in cattle production and the bacterium is a public health concern. A surveillance and control program has been in place in Denmark since 2002 with the ultimate goal to eradicate S. Dublin from Danish cattle herds, however, a small proportion of herds have remained positive for many years. In this study, we demonstrated that herds with persistent infection often were infected with the same strain for many years, indicating that internal biosecurity has to be improved to curb the infection. Further, domestic human cases of S. Dublin infection in humans was found to be caused both by Danish cattle isolates and isolates acquired abroad. The study shows the strength of whole genome sequencing to obtain detailed information on epidemiology of S. Dublin, and allowed us to suggest internal biosecurity as a main mean to control this bacterium in Danish cattle herds.",
author = "Eglė Kudirkiene and Gitte S{\o}rensen and Mia Torpdahl and {de Knegt}, Leonardo and Nielsen, {Liza R.} and Erik Rattenborg and Shahana Ahmed and Olsen, {John E}",
year = "2020",
doi = "10.1128/aem.01894-19",
language = "English",
journal = "Applied and Environmental Microbiology",
issn = "0099-2240",
publisher = "American Society for Microbiology",

}

Epidemiology of Salmonella enterica Serovar Dublin in Cattle and Humans in Denmark, 1996 to 2016: a Retrospective Whole-Genome-Based Study. / Kudirkiene, Eglė; Sørensen, Gitte; Torpdahl, Mia; de Knegt, Leonardo ; Nielsen, Liza R.; Rattenborg, Erik; Ahmed, Shahana; Olsen, John E.

In: Applied and Environmental Microbiology, 2020.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Epidemiology of Salmonella enterica Serovar Dublin in Cattle and Humans in Denmark, 1996 to 2016: a Retrospective Whole-Genome-Based Study

AU - Kudirkiene, Eglė

AU - Sørensen, Gitte

AU - Torpdahl, Mia

AU - de Knegt, Leonardo

AU - Nielsen, Liza R.

AU - Rattenborg, Erik

AU - Ahmed, Shahana

AU - Olsen, John E

PY - 2020

Y1 - 2020

N2 - Salmonella Dublin is a cattle-adapted S. enterica serovar causing intestinal as well as systemic infection in its bovine host, and it is also a serious threat to human health. The present study was aimed to determine the population structure of S Dublin isolates obtained from Danish cattle herds, and to investigate how cattle isolates relate to Danish human isolates, as well as to non-Danish human and bovine isolates. Phylogenetic analysis of 197 Danish cattle isolates from 1996-2016 identified three major clades corresponding to distinct geographical regions of cattle herds. Persistence of closely related isolates within the same herd and their circulation between epidemiologically linked herds was demonstrated for a period of more than 20 years. These findings suggest that the lack of internal biosecurity, but to some extend also external biosecurity in the herds, have played an important role in long term persistence of S. Dublin in Danish cattle herds in the period investigated. The global population analysis revealed that Danish cattle isolates clustered separately from bovine isolates from other countries, whereas human isolates were geographically spread. Resistance genes were peculiar to Danish bovine isolates, only the isolates within one Danish clade were found to often harbour two plasmids of IncFII/IncFIB and IncN types, the latter plasmid encoding blaTEM-1, tetA and strA, strB antibiotic resistance genes.IMPORTANCE S. Dublin causes economic losses in cattle production and the bacterium is a public health concern. A surveillance and control program has been in place in Denmark since 2002 with the ultimate goal to eradicate S. Dublin from Danish cattle herds, however, a small proportion of herds have remained positive for many years. In this study, we demonstrated that herds with persistent infection often were infected with the same strain for many years, indicating that internal biosecurity has to be improved to curb the infection. Further, domestic human cases of S. Dublin infection in humans was found to be caused both by Danish cattle isolates and isolates acquired abroad. The study shows the strength of whole genome sequencing to obtain detailed information on epidemiology of S. Dublin, and allowed us to suggest internal biosecurity as a main mean to control this bacterium in Danish cattle herds.

AB - Salmonella Dublin is a cattle-adapted S. enterica serovar causing intestinal as well as systemic infection in its bovine host, and it is also a serious threat to human health. The present study was aimed to determine the population structure of S Dublin isolates obtained from Danish cattle herds, and to investigate how cattle isolates relate to Danish human isolates, as well as to non-Danish human and bovine isolates. Phylogenetic analysis of 197 Danish cattle isolates from 1996-2016 identified three major clades corresponding to distinct geographical regions of cattle herds. Persistence of closely related isolates within the same herd and their circulation between epidemiologically linked herds was demonstrated for a period of more than 20 years. These findings suggest that the lack of internal biosecurity, but to some extend also external biosecurity in the herds, have played an important role in long term persistence of S. Dublin in Danish cattle herds in the period investigated. The global population analysis revealed that Danish cattle isolates clustered separately from bovine isolates from other countries, whereas human isolates were geographically spread. Resistance genes were peculiar to Danish bovine isolates, only the isolates within one Danish clade were found to often harbour two plasmids of IncFII/IncFIB and IncN types, the latter plasmid encoding blaTEM-1, tetA and strA, strB antibiotic resistance genes.IMPORTANCE S. Dublin causes economic losses in cattle production and the bacterium is a public health concern. A surveillance and control program has been in place in Denmark since 2002 with the ultimate goal to eradicate S. Dublin from Danish cattle herds, however, a small proportion of herds have remained positive for many years. In this study, we demonstrated that herds with persistent infection often were infected with the same strain for many years, indicating that internal biosecurity has to be improved to curb the infection. Further, domestic human cases of S. Dublin infection in humans was found to be caused both by Danish cattle isolates and isolates acquired abroad. The study shows the strength of whole genome sequencing to obtain detailed information on epidemiology of S. Dublin, and allowed us to suggest internal biosecurity as a main mean to control this bacterium in Danish cattle herds.

U2 - 10.1128/aem.01894-19

DO - 10.1128/aem.01894-19

M3 - Journal article

JO - Applied and Environmental Microbiology

JF - Applied and Environmental Microbiology

SN - 0099-2240

ER -