Circulation of four Anaplasma phagocytophilum ecotypes in Europe

S. Jahfari, E.C. Coipan, M. Fonville, A.D. van Leeuwen, P. Hengeveld, D. Heylen, P. Heyman, C. van Maanen, C.M. Butler, G. Foldvari, S. Szekeres, L.A.G. van Duijvendijk, W. Tack, J.M. Rijks, J. van der Giessen, W. Takken, S.E. van Wieren, K. Takumi, H. Sprong

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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.
Original languageEnglish
Article number365
JournalParasites & Vectors
Volume7
Issue number1
DOIs
Publication statusPublished - 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

  • candidatus neoehrlichia mikurensis
  • human granulocytic anaplasmosis
  • ixodes-ricinus ticks
  • borrelia-burgdorferi
  • borne diseases
  • phylogenetic analyses
  • sequence-analysis
  • ehrlichiosis
  • strains
  • gene

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 & Vectors, 7(1), [365]. https://doi.org/10.1186/1756-3305-7-365
Jahfari, S. ; Coipan, E.C. ; Fonville, M. ; van Leeuwen, A.D. ; Hengeveld, P. ; Heylen, D. ; Heyman, P. ; van Maanen, C. ; Butler, C.M. ; Foldvari, G. ; Szekeres, S. ; van Duijvendijk, L.A.G. ; Tack, W. ; Rijks, J.M. ; van der Giessen, J. ; Takken, W. ; van Wieren, S.E. ; Takumi, K. ; Sprong, H. / Circulation of four Anaplasma phagocytophilum ecotypes in Europe. In: Parasites & Vectors. 2014 ; Vol. 7, No. 1.
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title = "Circulation of four Anaplasma phagocytophilum ecotypes in Europe",
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.",
keywords = "candidatus neoehrlichia mikurensis, human granulocytic anaplasmosis, ixodes-ricinus ticks, borrelia-burgdorferi, borne diseases, phylogenetic analyses, sequence-analysis, ehrlichiosis, strains, gene",
author = "S. Jahfari and E.C. Coipan and M. Fonville and {van Leeuwen}, A.D. and P. Hengeveld and D. Heylen and P. Heyman and {van Maanen}, C. and C.M. Butler and G. Foldvari and S. Szekeres and {van Duijvendijk}, L.A.G. and W. Tack and J.M. Rijks and {van der Giessen}, J. and W. Takken and {van Wieren}, S.E. and K. Takumi and H. Sprong",
year = "2014",
doi = "10.1186/1756-3305-7-365",
language = "English",
volume = "7",
journal = "Parasites & Vectors",
issn = "1756-3305",
publisher = "Springer Verlag",
number = "1",

}

Jahfari, S, Coipan, EC, Fonville, M, van Leeuwen, AD, Hengeveld, P, Heylen, D, Heyman, P, van Maanen, C, Butler, CM, Foldvari, G, Szekeres, S, van Duijvendijk, LAG, 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 & Vectors, vol. 7, no. 1, 365. https://doi.org/10.1186/1756-3305-7-365

Circulation of four Anaplasma phagocytophilum ecotypes in Europe. / Jahfari, S.; Coipan, E.C.; Fonville, M.; van Leeuwen, A.D.; Hengeveld, P.; Heylen, D.; Heyman, P.; van Maanen, C.; Butler, C.M.; Foldvari, G.; Szekeres, S.; van Duijvendijk, L.A.G.; Tack, W.; Rijks, J.M.; van der Giessen, J.; Takken, W.; van Wieren, S.E.; Takumi, K.; Sprong, H.

In: Parasites & Vectors, Vol. 7, No. 1, 365, 2014.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Circulation of four Anaplasma phagocytophilum ecotypes in Europe

AU - Jahfari, S.

AU - Coipan, E.C.

AU - Fonville, M.

AU - van Leeuwen, A.D.

AU - Hengeveld, P.

AU - Heylen, D.

AU - Heyman, P.

AU - van Maanen, C.

AU - Butler, C.M.

AU - Foldvari, G.

AU - Szekeres, S.

AU - van Duijvendijk, L.A.G.

AU - Tack, W.

AU - Rijks, J.M.

AU - van der Giessen, J.

AU - Takken, W.

AU - van Wieren, S.E.

AU - Takumi, K.

AU - Sprong, H.

PY - 2014

Y1 - 2014

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 - candidatus neoehrlichia mikurensis

KW - human granulocytic anaplasmosis

KW - ixodes-ricinus ticks

KW - borrelia-burgdorferi

KW - borne diseases

KW - phylogenetic analyses

KW - sequence-analysis

KW - ehrlichiosis

KW - strains

KW - gene

U2 - 10.1186/1756-3305-7-365

DO - 10.1186/1756-3305-7-365

M3 - Article

VL - 7

JO - Parasites & Vectors

JF - Parasites & Vectors

SN - 1756-3305

IS - 1

M1 - 365

ER -

Jahfari S, Coipan EC, Fonville M, van Leeuwen AD, Hengeveld P, Heylen D et al. Circulation of four Anaplasma phagocytophilum ecotypes in Europe. Parasites & Vectors. 2014;7(1). 365. https://doi.org/10.1186/1756-3305-7-365