Circulation of four Anaplasma phagocytophilum ecotypes in Europe

Setareh Jahfari, E. Claudia Coipan, Manoj Fonville, Arieke Docters Van Leeuwen, Paul Hengeveld, Dieter Heylen, Paul Heyman, Cees Van Maanen, Catherine M. Butler, G. Földvári, Sándor Szekeres, Gilian Van Duijvendijk, Wesley Tack, Jolianne M. Rijks, Joke Van Der Giessen, Willem Takken, Sipke E. Van Wieren, Katsuhisa Takumi, Hein Sprong

Research output: Contribution to journalArticle

86 Citations (Scopus)

Abstract

Background: Anaplasma phagocytophilum is the etiological agent of granulocytic anaplasmosis in humans and animals. Wild animals and ticks play key roles in the enzootic cycles of the pathogen. Potential ecotypes of A. phagocytophilum have been characterized genetically, but their host range, zoonotic potential and transmission dynamics has only incompletely been resolved. Methods. The presence of A. phagocytophilum DNA was determined in more than 6000 ixodid ticks collected from the vegetation and wildlife, in 289 tissue samples from wild and domestic animals, and 69 keds collected from deer, originating from various geographic locations in The Netherlands and Belgium. From the qPCR-positive lysates, a fragment of the groEL-gene was amplified and sequenced. Additional groEL sequences from ticks and animals from Europe were obtained from GenBank, and sequences from human cases were obtained through literature searches. Statistical analyses were performed to identify A. phagocytophilum ecotypes, to assess their host range and their zoonotic potential. The population dynamics of A. phagocytophilum ecotypes was investigated using population genetic analyses. Results: DNA of A. phagocytophilum was present in all stages of questing and feeding Ixodes ricinus, feeding I. hexagonus, I. frontalis, I. trianguliceps, and deer keds, but was absent in questing I. arboricola and Dermacentor reticulatus. DNA of A. phagocytophilum was present in feeding ticks and tissues from many vertebrates, including roe deer, mouflon, red foxes, wild boar, sheep and hedgehogs but was rarely found in rodents and birds and was absent in badgers and lizards. Four geographically dispersed A. phagocytophilum ecotypes were identified, that had significantly different host ranges. All sequences from human cases belonged to only one of these ecotypes. Based on population genetic parameters, the potentially zoonotic ecotype showed significant expansion. Conclusion: Four ecotypes of A. phagocytophilum with differential enzootic cycles were identified. So far, all human cases clustered in only one of these ecotypes. The zoonotic ecotype has the broadest range of wildlife hosts. The expansion of the zoonotic A. phagocytophilum ecotype indicates a recent increase of the acarological risk of exposure of humans and animals.

Original languageEnglish
Article number365
JournalParasites and Vectors
Volume7
Issue number1
DOIs
Publication statusPublished - Aug 15 2014

Fingerprint

Anaplasma phagocytophilum
Ecotype
Zoonoses
Host Specificity
Ticks
Deer
Wild Animals
Population Genetics
DNA
Anaplasmosis
Dermacentor
Domestic Sheep
Mustelidae
Geographic Locations
Ixodes
Sus scrofa
Lizards
Hedgehogs
Belgium
Nucleic Acid Databases

Keywords

  • Anaplasma phagocytophilum
  • Epidemiology
  • Ixodes ricinus
  • Wildlife
  • Zoonoses

ASJC Scopus subject areas

  • Parasitology
  • Infectious Diseases
  • Medicine(all)

Cite this

Jahfari, S., Coipan, E. C., Fonville, M., Van Leeuwen, A. D., Hengeveld, P., Heylen, D., ... Sprong, H. (2014). Circulation of four Anaplasma phagocytophilum ecotypes in Europe. Parasites and Vectors, 7(1), [365]. https://doi.org/10.1186/1756-3305-7-365

Circulation of four Anaplasma phagocytophilum ecotypes in Europe. / Jahfari, Setareh; Coipan, E. Claudia; Fonville, Manoj; Van Leeuwen, Arieke Docters; Hengeveld, Paul; Heylen, Dieter; Heyman, Paul; Van Maanen, Cees; Butler, Catherine M.; Földvári, G.; Szekeres, Sándor; Van Duijvendijk, Gilian; Tack, Wesley; Rijks, Jolianne M.; Van Der Giessen, Joke; Takken, Willem; Van Wieren, Sipke E.; Takumi, Katsuhisa; Sprong, Hein.

In: Parasites and Vectors, Vol. 7, No. 1, 365, 15.08.2014.

Research output: Contribution to journalArticle

Jahfari, S, Coipan, EC, Fonville, M, Van Leeuwen, AD, Hengeveld, P, Heylen, D, Heyman, P, Van Maanen, C, Butler, CM, Földvári, G, Szekeres, S, Van Duijvendijk, G, Tack, W, Rijks, JM, Van Der Giessen, J, Takken, W, Van Wieren, SE, Takumi, K & Sprong, H 2014, 'Circulation of four Anaplasma phagocytophilum ecotypes in Europe', Parasites and Vectors, vol. 7, no. 1, 365. https://doi.org/10.1186/1756-3305-7-365
Jahfari S, Coipan EC, Fonville M, Van Leeuwen AD, Hengeveld P, Heylen D et al. Circulation of four Anaplasma phagocytophilum ecotypes in Europe. Parasites and Vectors. 2014 Aug 15;7(1). 365. https://doi.org/10.1186/1756-3305-7-365
Jahfari, Setareh ; Coipan, E. Claudia ; Fonville, Manoj ; Van Leeuwen, Arieke Docters ; Hengeveld, Paul ; Heylen, Dieter ; Heyman, Paul ; Van Maanen, Cees ; Butler, Catherine M. ; Földvári, G. ; Szekeres, Sándor ; Van Duijvendijk, Gilian ; Tack, Wesley ; Rijks, Jolianne M. ; Van Der Giessen, Joke ; Takken, Willem ; Van Wieren, Sipke E. ; Takumi, Katsuhisa ; Sprong, Hein. / Circulation of four Anaplasma phagocytophilum ecotypes in Europe. In: Parasites and Vectors. 2014 ; Vol. 7, No. 1.
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abstract = "Background: Anaplasma phagocytophilum is the etiological agent of granulocytic anaplasmosis in humans and animals. Wild animals and ticks play key roles in the enzootic cycles of the pathogen. Potential ecotypes of A. phagocytophilum have been characterized genetically, but their host range, zoonotic potential and transmission dynamics has only incompletely been resolved. Methods. The presence of A. phagocytophilum DNA was determined in more than 6000 ixodid ticks collected from the vegetation and wildlife, in 289 tissue samples from wild and domestic animals, and 69 keds collected from deer, originating from various geographic locations in The Netherlands and Belgium. From the qPCR-positive lysates, a fragment of the groEL-gene was amplified and sequenced. Additional groEL sequences from ticks and animals from Europe were obtained from GenBank, and sequences from human cases were obtained through literature searches. Statistical analyses were performed to identify A. phagocytophilum ecotypes, to assess their host range and their zoonotic potential. The population dynamics of A. phagocytophilum ecotypes was investigated using population genetic analyses. Results: DNA of A. phagocytophilum was present in all stages of questing and feeding Ixodes ricinus, feeding I. hexagonus, I. frontalis, I. trianguliceps, and deer keds, but was absent in questing I. arboricola and Dermacentor reticulatus. DNA of A. phagocytophilum was present in feeding ticks and tissues from many vertebrates, including roe deer, mouflon, red foxes, wild boar, sheep and hedgehogs but was rarely found in rodents and birds and was absent in badgers and lizards. Four geographically dispersed A. phagocytophilum ecotypes were identified, that had significantly different host ranges. All sequences from human cases belonged to only one of these ecotypes. Based on population genetic parameters, the potentially zoonotic ecotype showed significant expansion. Conclusion: Four ecotypes of A. phagocytophilum with differential enzootic cycles were identified. So far, all human cases clustered in only one of these ecotypes. The zoonotic ecotype has the broadest range of wildlife hosts. The expansion of the zoonotic A. phagocytophilum ecotype indicates a recent increase of the acarological risk of exposure of humans and animals.",
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author = "Setareh Jahfari and Coipan, {E. Claudia} and Manoj Fonville and {Van Leeuwen}, {Arieke Docters} and Paul Hengeveld and Dieter Heylen and Paul Heyman and {Van Maanen}, Cees and Butler, {Catherine M.} and G. F{\"o}ldv{\'a}ri and S{\'a}ndor Szekeres and {Van Duijvendijk}, Gilian and Wesley Tack and Rijks, {Jolianne M.} and {Van Der Giessen}, Joke and Willem Takken and {Van Wieren}, {Sipke E.} and Katsuhisa Takumi and Hein Sprong",
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T1 - Circulation of four Anaplasma phagocytophilum ecotypes in Europe

AU - Jahfari, Setareh

AU - Coipan, E. Claudia

AU - Fonville, Manoj

AU - Van Leeuwen, Arieke Docters

AU - Hengeveld, Paul

AU - Heylen, Dieter

AU - Heyman, Paul

AU - Van Maanen, Cees

AU - Butler, Catherine M.

AU - Földvári, G.

AU - Szekeres, Sándor

AU - Van Duijvendijk, Gilian

AU - Tack, Wesley

AU - Rijks, Jolianne M.

AU - Van Der Giessen, Joke

AU - Takken, Willem

AU - Van Wieren, Sipke E.

AU - Takumi, Katsuhisa

AU - Sprong, Hein

PY - 2014/8/15

Y1 - 2014/8/15

N2 - Background: Anaplasma phagocytophilum is the etiological agent of granulocytic anaplasmosis in humans and animals. Wild animals and ticks play key roles in the enzootic cycles of the pathogen. Potential ecotypes of A. phagocytophilum have been characterized genetically, but their host range, zoonotic potential and transmission dynamics has only incompletely been resolved. Methods. The presence of A. phagocytophilum DNA was determined in more than 6000 ixodid ticks collected from the vegetation and wildlife, in 289 tissue samples from wild and domestic animals, and 69 keds collected from deer, originating from various geographic locations in The Netherlands and Belgium. From the qPCR-positive lysates, a fragment of the groEL-gene was amplified and sequenced. Additional groEL sequences from ticks and animals from Europe were obtained from GenBank, and sequences from human cases were obtained through literature searches. Statistical analyses were performed to identify A. phagocytophilum ecotypes, to assess their host range and their zoonotic potential. The population dynamics of A. phagocytophilum ecotypes was investigated using population genetic analyses. Results: DNA of A. phagocytophilum was present in all stages of questing and feeding Ixodes ricinus, feeding I. hexagonus, I. frontalis, I. trianguliceps, and deer keds, but was absent in questing I. arboricola and Dermacentor reticulatus. DNA of A. phagocytophilum was present in feeding ticks and tissues from many vertebrates, including roe deer, mouflon, red foxes, wild boar, sheep and hedgehogs but was rarely found in rodents and birds and was absent in badgers and lizards. Four geographically dispersed A. phagocytophilum ecotypes were identified, that had significantly different host ranges. All sequences from human cases belonged to only one of these ecotypes. Based on population genetic parameters, the potentially zoonotic ecotype showed significant expansion. Conclusion: Four ecotypes of A. phagocytophilum with differential enzootic cycles were identified. So far, all human cases clustered in only one of these ecotypes. The zoonotic ecotype has the broadest range of wildlife hosts. The expansion of the zoonotic A. phagocytophilum ecotype indicates a recent increase of the acarological risk of exposure of humans and animals.

AB - Background: Anaplasma phagocytophilum is the etiological agent of granulocytic anaplasmosis in humans and animals. Wild animals and ticks play key roles in the enzootic cycles of the pathogen. Potential ecotypes of A. phagocytophilum have been characterized genetically, but their host range, zoonotic potential and transmission dynamics has only incompletely been resolved. Methods. The presence of A. phagocytophilum DNA was determined in more than 6000 ixodid ticks collected from the vegetation and wildlife, in 289 tissue samples from wild and domestic animals, and 69 keds collected from deer, originating from various geographic locations in The Netherlands and Belgium. From the qPCR-positive lysates, a fragment of the groEL-gene was amplified and sequenced. Additional groEL sequences from ticks and animals from Europe were obtained from GenBank, and sequences from human cases were obtained through literature searches. Statistical analyses were performed to identify A. phagocytophilum ecotypes, to assess their host range and their zoonotic potential. The population dynamics of A. phagocytophilum ecotypes was investigated using population genetic analyses. Results: DNA of A. phagocytophilum was present in all stages of questing and feeding Ixodes ricinus, feeding I. hexagonus, I. frontalis, I. trianguliceps, and deer keds, but was absent in questing I. arboricola and Dermacentor reticulatus. DNA of A. phagocytophilum was present in feeding ticks and tissues from many vertebrates, including roe deer, mouflon, red foxes, wild boar, sheep and hedgehogs but was rarely found in rodents and birds and was absent in badgers and lizards. Four geographically dispersed A. phagocytophilum ecotypes were identified, that had significantly different host ranges. All sequences from human cases belonged to only one of these ecotypes. Based on population genetic parameters, the potentially zoonotic ecotype showed significant expansion. Conclusion: Four ecotypes of A. phagocytophilum with differential enzootic cycles were identified. So far, all human cases clustered in only one of these ecotypes. The zoonotic ecotype has the broadest range of wildlife hosts. The expansion of the zoonotic A. phagocytophilum ecotype indicates a recent increase of the acarological risk of exposure of humans and animals.

KW - Anaplasma phagocytophilum

KW - Epidemiology

KW - Ixodes ricinus

KW - Wildlife

KW - Zoonoses

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