Analysis of the population structure of Anaplasma phagocytophilum using multilocus sequence typing

Christian Huhn, Christina Winter, Timo Wolfsperger, Nicole Wüppenhorst, Katja Strašek Smrdel, Jasmin Skuballa, Miriam Pfäffle, Trevor Petney, Cornelia Silaghi, Viktor Dyachenko, Nikola Pantchev, Reinhard K. Straubinger, Daniel Schaarschmidt-Kiener, Martin Ganter, Matthew Aardema, Friederike D. Von Loewenich

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Anaplasma phagocytophilum is a Gram-negative obligate intracellular bacterium that replicates in neutrophils. It is transmitted via tick-bite and causes febrile disease in humans and animals. Human granulocytic anaplasmosis is regarded as an emerging infectious disease in North America, Europe and Asia. However, although increasingly detected, it is still rare in Europe. Clinically apparent A. phagocytophilum infections in animals are mainly found in horses, dogs, cats, sheep and cattle. Evidence from cross-infection experiments that A. phagocytophilum isolates of distinct host origin are not uniformly infectious for heterologous hosts has led to several approaches of molecular strain characterization. Unfortunately, the results of these studies are not always easily comparable, because different gene regions and fragment lengths were investigated. Multilocus sequence typing is a widely accepted method for molecular characterization of bacteria. We here provide for the first time a universal typing method that is easily transferable between different laboratories. We validated our approach on an unprecedented large data set of almost 400 A. phagocytophilum strains from humans and animals mostly from Europe. The typability was 74% (284/383). One major clonal complex containing 177 strains was detected. However, 54% (49/90) of the sequence types were not part of a clonal complex indicating that the population structure of A. phagocytophilum is probably semiclonal. All strains from humans, dogs and horses from Europe belonged to the same clonal complex. As canine and equine granulocytic anaplasmosis occurs frequently in Europe, human granulocytic anaplasmosis is likely to be underdiagnosed in Europe. Further, wild boars and hedgehogs may serve as reservoir hosts of the disease in humans and domestic animals in Europe, because their strains belonged to the same clonal complex. In contrast, as they were only distantly related, roe deer, voles and shrews are unlikely to harbor A. phagocytophilum strains infectious for humans, domestic or farm animals.

Original languageEnglish
Article numbere93725
JournalPLoS ONE
Volume9
Issue number4
DOIs
StatePublished - 3 Apr 2014

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Anaplasma phagocytophilum
Multilocus Sequence Typing
population structure
Animals
Anaplasmosis
anaplasmosis
Domestic Animals
Population
Horses
Bacteria
horses
domestic animals
dogs
Disease Reservoirs
Northern Asia
Ports and harbors
Dogs
tick bites
Emerging Communicable Diseases
Shrews

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Huhn, C., Winter, C., Wolfsperger, T., Wüppenhorst, N., Strašek Smrdel, K., Skuballa, J., ... Von Loewenich, F. D. (2014). Analysis of the population structure of Anaplasma phagocytophilum using multilocus sequence typing. PLoS ONE, 9(4), [e93725]. https://doi.org/10.1371/journal.pone.0093725
Huhn, Christian ; Winter, Christina ; Wolfsperger, Timo ; Wüppenhorst, Nicole ; Strašek Smrdel, Katja ; Skuballa, Jasmin ; Pfäffle, Miriam ; Petney, Trevor ; Silaghi, Cornelia ; Dyachenko, Viktor ; Pantchev, Nikola ; Straubinger, Reinhard K. ; Schaarschmidt-Kiener, Daniel ; Ganter, Martin ; Aardema, Matthew ; Von Loewenich, Friederike D. / Analysis of the population structure of Anaplasma phagocytophilum using multilocus sequence typing. In: PLoS ONE. 2014 ; Vol. 9, No. 4.
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abstract = "Anaplasma phagocytophilum is a Gram-negative obligate intracellular bacterium that replicates in neutrophils. It is transmitted via tick-bite and causes febrile disease in humans and animals. Human granulocytic anaplasmosis is regarded as an emerging infectious disease in North America, Europe and Asia. However, although increasingly detected, it is still rare in Europe. Clinically apparent A. phagocytophilum infections in animals are mainly found in horses, dogs, cats, sheep and cattle. Evidence from cross-infection experiments that A. phagocytophilum isolates of distinct host origin are not uniformly infectious for heterologous hosts has led to several approaches of molecular strain characterization. Unfortunately, the results of these studies are not always easily comparable, because different gene regions and fragment lengths were investigated. Multilocus sequence typing is a widely accepted method for molecular characterization of bacteria. We here provide for the first time a universal typing method that is easily transferable between different laboratories. We validated our approach on an unprecedented large data set of almost 400 A. phagocytophilum strains from humans and animals mostly from Europe. The typability was 74{\%} (284/383). One major clonal complex containing 177 strains was detected. However, 54{\%} (49/90) of the sequence types were not part of a clonal complex indicating that the population structure of A. phagocytophilum is probably semiclonal. All strains from humans, dogs and horses from Europe belonged to the same clonal complex. As canine and equine granulocytic anaplasmosis occurs frequently in Europe, human granulocytic anaplasmosis is likely to be underdiagnosed in Europe. Further, wild boars and hedgehogs may serve as reservoir hosts of the disease in humans and domestic animals in Europe, because their strains belonged to the same clonal complex. In contrast, as they were only distantly related, roe deer, voles and shrews are unlikely to harbor A. phagocytophilum strains infectious for humans, domestic or farm animals.",
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Huhn, C, Winter, C, Wolfsperger, T, Wüppenhorst, N, Strašek Smrdel, K, Skuballa, J, Pfäffle, M, Petney, T, Silaghi, C, Dyachenko, V, Pantchev, N, Straubinger, RK, Schaarschmidt-Kiener, D, Ganter, M, Aardema, M & Von Loewenich, FD 2014, 'Analysis of the population structure of Anaplasma phagocytophilum using multilocus sequence typing', PLoS ONE, vol. 9, no. 4, e93725. https://doi.org/10.1371/journal.pone.0093725

Analysis of the population structure of Anaplasma phagocytophilum using multilocus sequence typing. / Huhn, Christian; Winter, Christina; Wolfsperger, Timo; Wüppenhorst, Nicole; Strašek Smrdel, Katja; Skuballa, Jasmin; Pfäffle, Miriam; Petney, Trevor; Silaghi, Cornelia; Dyachenko, Viktor; Pantchev, Nikola; Straubinger, Reinhard K.; Schaarschmidt-Kiener, Daniel; Ganter, Martin; Aardema, Matthew; Von Loewenich, Friederike D.

In: PLoS ONE, Vol. 9, No. 4, e93725, 03.04.2014.

Research output: Contribution to journalArticleResearchpeer-review

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AU - Winter, Christina

AU - Wolfsperger, Timo

AU - Wüppenhorst, Nicole

AU - Strašek Smrdel, Katja

AU - Skuballa, Jasmin

AU - Pfäffle, Miriam

AU - Petney, Trevor

AU - Silaghi, Cornelia

AU - Dyachenko, Viktor

AU - Pantchev, Nikola

AU - Straubinger, Reinhard K.

AU - Schaarschmidt-Kiener, Daniel

AU - Ganter, Martin

AU - Aardema, Matthew

AU - Von Loewenich, Friederike D.

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N2 - Anaplasma phagocytophilum is a Gram-negative obligate intracellular bacterium that replicates in neutrophils. It is transmitted via tick-bite and causes febrile disease in humans and animals. Human granulocytic anaplasmosis is regarded as an emerging infectious disease in North America, Europe and Asia. However, although increasingly detected, it is still rare in Europe. Clinically apparent A. phagocytophilum infections in animals are mainly found in horses, dogs, cats, sheep and cattle. Evidence from cross-infection experiments that A. phagocytophilum isolates of distinct host origin are not uniformly infectious for heterologous hosts has led to several approaches of molecular strain characterization. Unfortunately, the results of these studies are not always easily comparable, because different gene regions and fragment lengths were investigated. Multilocus sequence typing is a widely accepted method for molecular characterization of bacteria. We here provide for the first time a universal typing method that is easily transferable between different laboratories. We validated our approach on an unprecedented large data set of almost 400 A. phagocytophilum strains from humans and animals mostly from Europe. The typability was 74% (284/383). One major clonal complex containing 177 strains was detected. However, 54% (49/90) of the sequence types were not part of a clonal complex indicating that the population structure of A. phagocytophilum is probably semiclonal. All strains from humans, dogs and horses from Europe belonged to the same clonal complex. As canine and equine granulocytic anaplasmosis occurs frequently in Europe, human granulocytic anaplasmosis is likely to be underdiagnosed in Europe. Further, wild boars and hedgehogs may serve as reservoir hosts of the disease in humans and domestic animals in Europe, because their strains belonged to the same clonal complex. In contrast, as they were only distantly related, roe deer, voles and shrews are unlikely to harbor A. phagocytophilum strains infectious for humans, domestic or farm animals.

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Huhn C, Winter C, Wolfsperger T, Wüppenhorst N, Strašek Smrdel K, Skuballa J et al. Analysis of the population structure of Anaplasma phagocytophilum using multilocus sequence typing. PLoS ONE. 2014 Apr 3;9(4). e93725. https://doi.org/10.1371/journal.pone.0093725