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Home / Equine Research Bank / Parasit Vectors / Imported Hyalomma ticks in the Netherlands 2018-2020.
Parasites & vectors2021; 14(1); 244; doi: 10.1186/s13071-021-04738-x

Imported Hyalomma ticks in the Netherlands 2018-2020.

Abstract: Ticks of the genus Hyalomma, which are vectors for several tick-borne diseases, are occasionally found in areas outside their endemic range including northern parts of Europe. The objective of this study was to analyse adult Hyalomma ticks that were recently found in the Netherlands. Methods: Hyalomma ticks were morphologically identified. Cluster analysis, based upon sequence data (cox1 barcoding) for molecular identification, and pathogen detection were performed. Additionally, a cross-sectional survey of horses was conducted to actively search for Hyalomma ticks in summer 2019. Analysis of temperature was done to assess the possibility of (i) introduced engorged nymphs moulting to adults and (ii) establishment of populations in the Netherlands. Results: Seventeen adult Hyalomma ticks (one in 2018, eleven in 2019, five in 2020) were found by citizens and reported. Fifteen ticks were detected on horses and two on humans. Twelve were identified as H. marginatum, one as H. rufipes and four, of which only photographic images were available, as Hyalomma sp. No Crimean-Congo haemorrhagic fever virus or Babesia/Theileria parasites were detected. One adult tick tested positive for Rickettsia aeschlimannii. In the cross-sectional horse survey, no Hyalomma ticks were found. Analysis of temperatures showed that engorged nymphs arriving on migratory birds in spring were able to moult to adults in 2019 and 2020, and that cumulative daily temperatures in the Netherlands were lower than in areas with established H. marginatum populations. Conclusions: Our results show that Hyalomma ticks are regularly introduced in the Netherlands as nymphs. Under the Dutch weather conditions, these nymphs are able to develop to the adult stage, which can be sighted by vigilant citizens. Only one human pathogen, Rickettsia aeschlimannii, was found in one of the ticks. The risk of introduction of tick-borne diseases via Hyalomma ticks on migratory birds is considered to be low. Establishment of permanent Hyalomma populations is considered unlikely under the current Dutch climatic conditions.
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Publication Date: 2021-05-07 PubMed ID: 33962655PubMed Central: PMC8106226DOI: 10.1186/s13071-021-04738-xGoogle Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research investigates Hyalomma ticks in the Netherlands from 2018 to 2020, identifying their species and checking for diseases they may carry. Despite being frequently brought into the Netherlands, these ticks are unable to establish permanent populations due to the country’s climate. Furthermore, they pose a low risk for the introduction of tick-borne diseases.

Methodology of the Study

  • The researchers carried out a thorough inspection and analysis of Hyalomma tick specimens found in the Netherlands. The methods employed included morphological identification and molecular identification with sequence data.
  • A horseriding cross-sectional survey was conducted to actively search for Hyalomma ticks during the summer season in 2019.
  • Various temperatures were analyzed to assess the chances of introduced engorged nymphs (immature ticks) moulting into adults. Also, this study includes an estimate of whether permanent Hyalomma tick populations could establish in the Netherlands.

Research Findings

  • The study recovered seventeen adult Hyalomma ticks between 2018 and 2020. Most of them were found on horses, while two were found attached to humans.
  • The majority of ticks were identified as H. marginatum. However, there was also one H. rufipes and four Hyalomma species that couldn’t be definitively classified.
  • Upon testing for diseases, no tick was found to carry Crimean-Congo haemorrhagic fever virus or Babesia/Theileria parasites. Only one tick tested positive for carrying the Rickettsia aeschlimannii pathogen.
  • In the horse survey, researchers did not find any Hyalomma ticks.
  • Temperature analysis revealed that nymphs brought to the Netherlands by migratory birds were able to moult into adults during 2019 and 2020. However, the Dutch climate’s cumulative daily temperatures were still lower than those areas where H. marginatum populations are established, implying that the ticks are unlikely to establish permanent populations in the Netherlands.

Conclusions of the Study

  • The study concluded that Hyalomma ticks are often introduced into the Netherlands as nymphs, and under certain circumstances, these nymphs can develop into adults.
  • The potential health risk appears to be low, with only one found carrying a known human pathogen, Rickettsia aeschlimannii.
  • The climate of the Netherlands, in its current state, is not conducive to the establishment of permanent Hyalomma populations, making the introduction of tick-borne diseases via these ticks a low threat.

Cite This Article

APA
Uiterwijk M, Ibáñez-Justicia A, van de Vossenberg B, Jacobs F, Overgaauw P, Nijsse R, Dabekaussen C, Stroo A, Sprong H. (2021). Imported Hyalomma ticks in the Netherlands 2018-2020. Parasit Vectors, 14(1), 244. https://doi.org/10.1186/s13071-021-04738-x

Publication

Parasites & vectors
ISSN: 1756-3305
NlmUniqueID: 101462774
Country: England
Language: English
Volume: 14
Issue: 1
Pages: 244
PII: 244

Researcher Affiliations

Uiterwijk, Mathilde
  • Centre for Monitoring of Vectors (CMV), National Reference Laboratory, Netherlands Food and Consumer Product Safety Authority (NVWA), Wageningen, the Netherlands. m.uiterwijk@nvwa.nl.
Ibáñez-Justicia, Adolfo
  • Centre for Monitoring of Vectors (CMV), National Reference Laboratory, Netherlands Food and Consumer Product Safety Authority (NVWA), Wageningen, the Netherlands.
van de Vossenberg, Bart
  • National Plant Protection Organization (NPPO-NL), National Reference Laboratory, Netherlands Food and Consumer Product Safety Authority (NVWA), Wageningen, the Netherlands.
Jacobs, Frans
  • Centre for Monitoring of Vectors (CMV), National Reference Laboratory, Netherlands Food and Consumer Product Safety Authority (NVWA), Wageningen, the Netherlands.
Overgaauw, Paul
  • Institute for Risk Assessment Sciences (IRAS), Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands.
Nijsse, Rolf
  • Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands.
Dabekaussen, Charlotte
  • Institute for Risk Assessment Sciences (IRAS), Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands.
Stroo, Arjan
  • Centre for Monitoring of Vectors (CMV), National Reference Laboratory, Netherlands Food and Consumer Product Safety Authority (NVWA), Wageningen, the Netherlands.
Sprong, Hein
  • Centre for Infectious Disease Control (CIb), National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands.

MeSH Terms

  • Animal Migration
  • Animals
  • Bird Diseases / epidemiology
  • Bird Diseases / parasitology
  • Birds / parasitology
  • Cross-Sectional Studies
  • Female
  • Horse Diseases / epidemiology
  • Horse Diseases / parasitology
  • Horses / parasitology
  • Humans
  • Ixodidae / classification
  • Ixodidae / genetics
  • Male
  • Netherlands / epidemiology
  • Phylogeny
  • Tick Infestations / epidemiology
  • Tick Infestations / parasitology
  • Tick Infestations / veterinary

Conflict of Interest Statement

The authors declare that they have no competing interests.

References

This article includes 76 references
  1. Gargili A, Thangamani S, Bente D. Influence of laboratory animal hosts on the life cycle of Hyalomma marginatum and implications for an in vivo transmission model for Crimean-Congo hemorrhagic fever virus.. Front Cell Infect Microbiol 2013;3:39.
    doi: 10.3389/fcimb.2013.00039pmc: PMC3747357pubmed: 23971007google scholar: lookup
  2. Vial L, Stachurski F, Leblond A, Huber K, Vourc'h G, René-Martellet M, Desjardins I, Balança G, Grosbois V, Pradier S, Gély M, Appelgren A, Estrada-Peña A. Strong evidence for the presence of the tick Hyalomma marginatum Koch, 1844 in southern continental France.. Ticks Tick Borne Dis 2016 Oct;7(6):1162-1167.
    doi: 10.1016/j.ttbdis.2016.08.002pubmed: 27568169google scholar: lookup
  3. ECDC. Hyalomma marginatum—current known distribution: May 2020 ECDC. https://www.ecdc.europa.eu/en/publications-data/hyalomma-marginatum-current-known-distribution-may-2020
  4. HOOGSTRAAL H, KAISER MN, TRAYLOR MA, GABER S, GUINDY E. Ticks (Ixodoidea) on birds migrating from Africa to Europe and Asia.. Bull World Health Organ 1961;24(2):197-212.
    pmc: PMC2555510pubmed: 13715709
  5. Capek M, Literak I, Kocianova E, Sychra O, Najer T, Trnka A, Kverek P. Ticks of the Hyalomma marginatum complex transported by migratory birds into Central Europe.. Ticks Tick Borne Dis 2014 Sep;5(5):489-93.
    doi: 10.1016/j.ttbdis.2014.03.002pubmed: 24877976google scholar: lookup
  6. Marie-Angèle P, Lommano E, Humair PF, Douet V, Rais O, Schaad M, Jenni L, Gern L. Prevalence of Borrelia burgdorferi sensu lato in ticks collected from migratory birds in Switzerland.. Appl Environ Microbiol 2006 Jan;72(1):976-9.
    doi: 10.1128/AEM.72.1.976-979.2006pmc: PMC1352204pubmed: 16391149google scholar: lookup
  7. Toma L, Mancini F, Di Luca M, Cecere JG, Bianchi R, Khoury C, Quarchioni E, Manzia F, Rezza G, Ciervo A. Detection of microbial agents in ticks collected from migratory birds in central Italy.. Vector Borne Zoonotic Dis 2014 Mar;14(3):199-205.
    doi: 10.1089/vbz.2013.1458pmc: PMC3952585pubmed: 24576218google scholar: lookup
  8. Mancuso E, Toma L, Polci A, d'Alessio SG, Di Luca M, Orsini M, Di Domenico M, Marcacci M, Mancini G, Spina F, Goffredo M, Monaco F. Crimean-Congo Hemorrhagic Fever Virus Genome in Tick from Migratory Bird, Italy.. Emerg Infect Dis 2019 Jul;25(7):1418-1420.
    doi: 10.3201/eid2507.181345pmc: PMC6590740pubmed: 31211933google scholar: lookup
  9. England ME, Phipps P, Medlock JM, Atkinson PM, Atkinson B, Hewson R, Gale P. Hyalomma ticks on northward migrating birds in southern Spain: Implications for the risk of entry of Crimean-Congo haemorrhagic fever virus to Great Britain.. J Vector Ecol 2016 Jun;41(1):128-34.
    doi: 10.1111/jvec.12204pubmed: 27232135google scholar: lookup
  10. Sparagano O, George D, Giangaspero A, Špitalská E. Arthropods and associated arthropod-borne diseases transmitted by migrating birds. The case of ticks and tick-borne pathogens.. Vet Parasitol 2015 Sep 30;213(1-2):61-6.
    doi: 10.1016/j.vetpar.2015.08.028pubmed: 26343302google scholar: lookup
  11. Jameson LJ, Morgan PJ, Medlock JM, Watola G, Vaux AG. Importation of Hyalomma marginatum, vector of Crimean-Congo haemorrhagic fever virus, into the United Kingdom by migratory birds.. Ticks Tick Borne Dis 2012 Apr;3(2):95-9.
    doi: 10.1016/j.ttbdis.2011.12.002pubmed: 22300969google scholar: lookup
  12. Labbé Sandelin L, Tolf C, Larsson S, Wilhelmsson P, Salaneck E, Jaenson TG, Lindgren PE, Olsen B, Waldenström J. Candidatus Neoehrlichia mikurensis in Ticks from Migrating Birds in Sweden.. PLoS One 2015;10(7):e0133250.
    doi: 10.1371/journal.pone.0133250pmc: PMC4514885pubmed: 26207834google scholar: lookup
  13. Hasle G, Bjune G, Edvardsen E, Jakobsen C, Linnehol B, Røer JE, Mehl R, Røed KH, Pedersen J, Leinaas HP. Transport of ticks by migratory passerine birds to Norway.. J Parasitol 2009 Dec;95(6):1342-51.
    doi: 10.1645/GE-2146.1pubmed: 19658452google scholar: lookup
  14. Battisti E, Urach K, Hodžić A, Fusani L, Hufnagl P, Felsberger G, Ferroglio E, Duscher GG. Zoonotic Pathogens in Ticks from Migratory Birds, Italy.. Emerg Infect Dis 2020 Dec;26(12):2986-2988.
    doi: 10.3201/eid2612.181686pmc: PMC7706978pubmed: 33219656google scholar: lookup
  15. Heylen D, Fonville M, Docters van Leeuwen A, Stroo A, Duisterwinkel M, van Wieren S, Diuk-Wasser M, de Bruin A, Sprong H. Pathogen communities of songbird-derived ticks in Europe's low countries.. Parasit Vectors 2017 Oct 18;10(1):497.
    doi: 10.1186/s13071-017-2423-ypmc: PMC5648423pubmed: 29047399google scholar: lookup
  16. Chitimia-Dobler L, Nava S, Bestehorn M, Dobler G, Wölfel S. First detection of Hyalomma rufipes in Germany.. Ticks Tick Borne Dis 2016 Oct;7(6):1135-1138.
    doi: 10.1016/j.ttbdis.2016.08.008pubmed: 27567111google scholar: lookup
  17. Chitimia-Dobler L, Schaper S, Rieß R, Bitterwolf K, Frangoulidis D, Bestehorn M, Springer A, Oehme R, Drehmann M, Lindau A, Mackenstedt U, Strube C, Dobler G. Imported Hyalomma ticks in Germany in 2018.. Parasit Vectors 2019 Mar 26;12(1):134.
    doi: 10.1186/s13071-019-3380-4pmc: PMC6434826pubmed: 30909964google scholar: lookup
  18. Hansford KM, Carter D, Gillingham EL, Hernandez-Triana LM, Chamberlain J, Cull B, McGinley L, Paul Phipps L, Medlock JM. Hyalomma rufipes on an untraveled horse: Is this the first evidence of Hyalomma nymphs successfully moulting in the United Kingdom?. Ticks Tick Borne Dis 2019 Apr;10(3):704-708.
    doi: 10.1016/j.ttbdis.2019.03.003pubmed: 30876825google scholar: lookup
  19. Rumer L, Graser E, Hillebrand T, Talaska T, Dautel H, Mediannikov O, Roy-Chowdhury P, Sheshukova O, Donoso Mantke O, Niedrig M. Rickettsia aeschlimannii in Hyalomma marginatum ticks, Germany.. Emerg Infect Dis 2011 Feb;17(2):325-6.
    doi: 10.3201/eid1702.100308pmc: PMC3204748pubmed: 21291625google scholar: lookup
  20. Grandi G, Chitimia-Dobler L, Choklikitumnuey P, Strube C, Springer A, Albihn A, Jaenson TGT, Omazic A. First records of adult Hyalomma marginatum and H. rufipes ticks (Acari: Ixodidae) in Sweden.. Ticks Tick Borne Dis 2020 May;11(3):101403.
    doi: 10.1016/j.ttbdis.2020.101403pubmed: 32037097google scholar: lookup
  21. McGinley L, Hansford KM, Cull B, Gillingham EL, Carter DP, Chamberlain JF, Hernandez-Triana LM, Phipps LP, Medlock JM. First report of human exposure to Hyalomma marginatum in England: Further evidence of a Hyalomma moulting event in north-western Europe?. Ticks Tick Borne Dis 2021 Jan;12(1):101541.
    doi: 10.1016/j.ttbdis.2020.101541pubmed: 33007668google scholar: lookup
  22. Oehme R, Bestehorn M, Wölfel S, Chitimia-Dobler L. Hyalomma marginatum in Tübingen, Germany.. SystAppl Acarol 2017;22:1–6.
    doi: 10.11158/saa.22.1.1google scholar: lookup
  23. Duscher GG, Hodžić A, Hufnagl P, Wille-Piazzai W, Schötta AM, Markowicz MA, Estrada-Peña A, Stanek G, Allerberger F. Adult Hyalomma marginatum tick positive for Rickettsia aeschlimannii in Austria, October 2018.. Euro Surveill 2018 Nov;23(48).
    doi: 10.2807/1560-7917.ES.2018.23.48.1800595pmc: PMC6280420pubmed: 30621821google scholar: lookup
  24. Nijhof AM, Bodaan C, Postigo M, Nieuwenhuijs H, Opsteegh M, Franssen L, Jebbink F, Jongejan F. Ticks and associated pathogens collected from domestic animals in the Netherlands.. Vector Borne Zoonotic Dis 2007 Winter;7(4):585-95.
    doi: 10.1089/vbz.2007.0130pubmed: 17979540google scholar: lookup
  25. Butler CM, Sloet van Oldruitenborgh-Oosterbaan M, Werners AH, Stout TAE, Jongejan F, Houwers D. Classification of ticks collected from horses in the Netherlands in2008–2009 and identification of the (zoonotic) agents they contain.. Pferdeheilkunde 2016;32(4):329.
  26. Graveland H, Roest H, Stenvers O, Valkenburgh S, Friesema I, van der Giessen J. Staat van Zoönosen 2012.. RIVM The Netherlands 2013: 44.
  27. Estrada-Peña A, Pfäffle M, Baneth G, Kleinerman G, Petney TN. Ixodoidea of the Western Palaearctic: A review of available literature for identification of species.. Ticks Tick Borne Dis 2017 Jun;8(4):512-525.
    doi: 10.1016/j.ttbdis.2017.02.013pubmed: 28286142google scholar: lookup
  28. Spengler JR, Estrada-Peña A. Host preferences support the prominent role of Hyalomma ticks in the ecology of Crimean-Congo hemorrhagic fever.. PLoS Negl Trop Dis 2018 Feb;12(2):e0006248.
    doi: 10.1371/journal.pntd.0006248pmc: PMC5821391pubmed: 29420542google scholar: lookup
  29. Estrada-Peña A, de la Fuente J. The ecology of ticks and epidemiology of tick-borne viral diseases.. Antiviral Res 2014 Aug;108:104-28.
    doi: 10.1016/j.antiviral.2014.05.016pubmed: 24925264google scholar: lookup
  30. Hoogstraal H. The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa.. J Med Entomol 1979 May 22;15(4):307-417.
    doi: 10.1093/jmedent/15.4.307pubmed: 113533google scholar: lookup
  31. Valcárcel F, González J, González MG, Sánchez M, Tercero JM, Elhachimi L, Carbonell JD, Olmeda AS. Comparative Ecology of Hyalomma lusitanicum and Hyalomma marginatum Koch, 1844 (Acarina: Ixodidae).. Insects 2020 May 13;11(5).
    doi: 10.3390/insects11050303pmc: PMC7290797pubmed: 32414220google scholar: lookup
  32. Bakheit MA, Latif AA, Vatansever Z, Seitzer U, Ahmed J. The huge risks due to hyalomma ticks.. Arthropods as vectors of emerging diseases parasitol res monographs Berlin, Heidelberg: Springer; 2012.
  33. EFSA Panel on Animal Health and Welfare (AHAW). Scientific opinion on the role of tick vectors in the epidemiology of Crimean-Congo hemorrhagic fever and African swine fever in Eurasia. EFSA J 2010;8:156.
  34. Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Abdad MY, Stenos J, Bitam I, Fournier PE, Raoult D. Update on tick-borne rickettsioses around the world: a geographic approach.. Clin Microbiol Rev 2013 Oct;26(4):657-702.
    doi: 10.1128/CMR.00032-13pmc: PMC3811236pubmed: 24092850google scholar: lookup
  35. Estrada-Peña A, Mihalca AD, Petney TN. Ticks of Europe and North America.. Springer International Publishing 2017.
  36. Walker AR, Bouattour A, Camicas JL, Estrada-Peña A, Horak IG, Latif AA. Ticks of domestic animals in Africa: a guide to identification of species.. Bioscience Reports Edinburgh Scotland, U.K.: 2014.
  37. Hebert PD, Cywinska A, Ball SL, deWaard JR. Biological identifications through DNA barcodes.. Proc Biol Sci 2003 Feb 7;270(1512):313-21.
    doi: 10.1098/rspb.2002.2218pmc: PMC1691236pubmed: 12614582google scholar: lookup
  38. EPPO/OEPP. DNA barcoding as an identification tool for a number of regulated pests.. EPPO Bull 2016;46:501–37.
  39. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform.. Nucleic Acids Res 2002 Jul 15;30(14):3059-66.
    doi: 10.1093/nar/gkf436pmc: PMC135756pubmed: 12136088google scholar: lookup
  40. Wölfel R, Paweska JT, Petersen N, Grobbelaar AA, Leman PA, Hewson R, Georges-Courbot MC, Papa A, Günther S, Drosten C. Virus detection and monitoring of viral load in Crimean-Congo hemorrhagic fever virus patients.. Emerg Infect Dis 2007 Jul;13(7):1097-100.
    doi: 10.3201/eid1307.070068pmc: PMC2878241pubmed: 18214191google scholar: lookup
  41. Wielinga PR, Fonville M, Sprong H, Gaasenbeek C, Borgsteede F, van der Giessen JW. Persistent detection of Babesia EU1 and Babesia microti in Ixodes ricinus in the Netherlands during a 5-year surveillance: 2003-2007.. Vector Borne Zoonotic Dis 2009 Feb;9(1):119-22.
    doi: 10.1089/vbz.2008.0047pubmed: 18759637google scholar: lookup
  42. Stenos J, Graves SR, Unsworth NB. A highly sensitive and specific real-time PCR assay for the detection of spotted fever and typhus group Rickettsiae.. Am J Trop Med Hyg 2005 Dec;73(6):1083-5.
    doi: 10.4269/ajtmh.2005.73.1083pubmed: 16354816google scholar: lookup
  43. Roux V, Raoult D. Phylogenetic analysis of members of the genus Rickettsia using the gene encoding the outer-membrane protein rOmpB (ompB).. Int J Syst Evol Microbiol 2000 Jul;50 Pt 4:1449-1455.
    doi: 10.1099/00207713-50-4-1449pubmed: 10939649google scholar: lookup
  44. Emelyanova N. Seasonal changes and host adaptability of ticks of the species Hyalomma marginatum in the Stavropol territory.. Zurnal Mikrobiologii Epidemiologii I Immunobiologii 2005;4:115–118.
  45. Gale P, Stephenson B, Brouwer A, Martinez M, de la Torre A, Bosch J, Foley-Fisher M, Bonilauri P, Lindström A, Ulrich RG, de Vos CJ, Scremin M, Liu Z, Kelly L, Muñoz MJ. Impact of climate change on risk of incursion of Crimean-Congo haemorrhagic fever virus in livestock in Europe through migratory birds.. J Appl Microbiol 2012 Feb;112(2):246-57.
    doi: 10.1111/j.1365-2672.2011.05203.xpubmed: 22118269google scholar: lookup
  46. Gray JS, Dautel H, Estrada-Peña A, Kahl O, Lindgren E. Effects of climate change on ticks and tick-borne diseases in europe.. Interdiscip Perspect Infect Dis 2009;2009:593232.
    doi: 10.1155/2009/593232pmc: PMC2648658pubmed: 19277106google scholar: lookup
  47. Höhenheim U. Tropische Zecken: Neu eingewanderte Art überwintert erstmals in Deutschland.. 2019.
  48. Rees DJ, Dioli M, Kirkendall LR. Molecules and morphology: evidence for cryptic hybridization in African Hyalomma (Acari: Ixodidae).. Mol Phylogenet Evol 2003 Apr;27(1):131-42.
    doi: 10.1016/S1055-7903(02)00374-3pubmed: 12679078google scholar: lookup
  49. Bosch J, Muñoz MJ, Martínez M, de la Torre A, Estrada-Peña A. Vector-borne pathogen spread through ticks on migratory birds: a probabilistic spatial risk model for South-Western europe.. Transbound Emerg Dis 2013 Oct;60(5):403-15.
    doi: 10.1111/j.1865-1682.2012.01358.xpubmed: 22781365google scholar: lookup
  50. Wallménius K, Barboutis C, Fransson T, Jaenson TG, Lindgren PE, Nyström F, Olsen B, Salaneck E, Nilsson K. Spotted fever Rickettsia species in Hyalomma and Ixodes ticks infesting migratory birds in the European Mediterranean area.. Parasit Vectors 2014 Jul 10;7:318.
    doi: 10.1186/1756-3305-7-318pmc: PMC4230250pubmed: 25011617google scholar: lookup
  51. Socolovschi C, Reynaud P, Kernif T, Raoult D, Parola P. Rickettsiae of spotted fever group, Borrelia valaisiana, and Coxiella burnetii in ticks on passerine birds and mammals from the Camargue in the south of France.. Ticks Tick Borne Dis 2012 Dec;3(5-6):355-60.
    doi: 10.1016/j.ttbdis.2012.10.019pubmed: 23141104google scholar: lookup
  52. Hubálek Z, Sedláček P, Estrada-Peña A, Vojtíšek J, Rudolf I. First record of Hyalomma rufipes in the Czech Republic, with a review of relevant cases in other parts of Europe.. Ticks Tick Borne Dis 2020 Jul;11(4):101421.
    doi: 10.1016/j.ttbdis.2020.101421pubmed: 32360146google scholar: lookup
  53. Estrada-Peña A, Martínez Avilés M, Muñoz Reoyo MJ. A population model to describe the distribution and seasonal dynamics of the tick Hyalomma marginatum in the Mediterranean Basin.. Transbound Emerg Dis 2011 Jun;58(3):213-23.
    doi: 10.1111/j.1865-1682.2010.01198.xpubmed: 21223534google scholar: lookup
  54. Ogden NH, Mechai S, Margos G. Changing geographic ranges of ticks and tick-borne pathogens: drivers, mechanisms and consequences for pathogen diversity.. Front Cell Infect Microbiol 2013;3:46.
    doi: 10.3389/fcimb.2013.00046pmc: PMC3756306pubmed: 24010124google scholar: lookup
  55. Lampert A, Liebhold AM. Combining multiple tactics over time for cost-effective eradication of invading insect populations.. Ecol Lett 2021 Feb;24(2):279-287.
    doi: 10.1111/ele.13640pubmed: 33169526google scholar: lookup
  56. Tobin PC, Berec L, Liebhold AM. Exploiting Allee effects for managing biological invasions.. Ecol Lett 2011 Jun;14(6):615-24.
    doi: 10.1111/j.1461-0248.2011.01614.xpubmed: 21418493google scholar: lookup
  57. MacLeod A, Korycinska A. Detailing Köppen-Geiger climate zones at sub-national to continental scale: a resource for pest risk analysis.. EPPO Bull 2019;49:73–82.
    doi: 10.1111/epp.12549google scholar: lookup
  58. Azagi T, Klement E, Perlman G, Lustig Y, Mumcuoglu KY, Apanaskevich DA, Gottlieb Y. Francisella-Like Endosymbionts and Rickettsia Species in Local and Imported Hyalomma Ticks.. Appl Environ Microbiol 2017 Sep 15;83(18).
    doi: 10.1128/AEM.01302-17pmc: PMC5583492pubmed: 28710265google scholar: lookup
  59. Vescio FM, Busani L, Mughini-Gras L, Khoury C, Avellis L, Taseva E, Rezza G, Christova I. Environmental correlates of Crimean-Congo haemorrhagic fever incidence in Bulgaria.. BMC Public Health 2012 Dec 27;12:1116.
    doi: 10.1186/1471-2458-12-1116pmc: PMC3547815pubmed: 23270399google scholar: lookup
  60. Estrada-Peña A, Jameson L, Medlock J, Vatansever Z, Tishkova F. Unraveling the ecological complexities of tick-associated Crimean-Congo hemorrhagic fever virus transmission: a gap analysis for the western Palearctic.. Vector Borne Zoonotic Dis 2012 Sep;12(9):743-52.
    doi: 10.1089/vbz.2011.0767pubmed: 22448676google scholar: lookup
  61. Estrada-Peña A, Palomar AM, Santibáñez P, Sánchez N, Habela MA, Portillo A, Romero L, Oteo JA. Crimean-Congo hemorrhagic fever virus in ticks, Southwestern Europe, 2010.. Emerg Infect Dis 2012 Jan;18(1):179-80.
    doi: 10.3201/eid1801.111040pmc: PMC3310114pubmed: 22261502google scholar: lookup
  62. Negredo A, de la Calle-Prieto F, Palencia-Herrejón E, Mora-Rillo M, Astray-Mochales J, Sánchez-Seco MP, Bermejo Lopez E, Menárguez J, Fernández-Cruz A, Sánchez-Artola B, Keough-Delgado E, Ramírez de Arellano E, Lasala F, Milla J, Fraile JL, Ordobás Gavín M, Martinez de la Gándara A, López Perez L, Diaz-Diaz D, López-García MA, Delgado-Jimenez P, Martín-Quirós A, Trigo E, Figueira JC, Manzanares J, Rodriguez-Baena E, Garcia-Comas L, Rodríguez-Fraga O, García-Arenzana N, Fernández-Díaz MV, Cornejo VM, Emmerich P, Schmidt-Chanasit J, Arribas JR. Autochthonous Crimean-Congo Hemorrhagic Fever in Spain.. N Engl J Med 2017 Jul 13;377(2):154-161.
    doi: 10.1056/NEJMoa1615162pubmed: 28700843google scholar: lookup
  63. Monsalve Arteaga L, Muñoz Bellido JL, Vieira Lista MC, Vicente Santiago MB, Fernández Soto P, Bas I, Leralta N, de Ory Manchón F, Negredo AI, Sánchez Seco MP, Alonso Sardón M, Pérez González S, Jiménez Del Bianco A, Blanco Peris L, Alamo-Sanz R, Hewson R, Belhassen-García M, Muro A. Crimean-Congo haemorrhagic fever (CCHF) virus-specific antibody detection in blood donors, Castile-León, Spain, summer 2017 and 2018.. Euro Surveill 2020 Mar;25(10).
    doi: 10.2807/1560-7917.ES.2020.25.10.1900507pmc: PMC7078822pubmed: 32183933google scholar: lookup
  64. Cajimat MNB, Rodriguez SE, Schuster IUE, Swetnam DM, Ksiazek TG, Habela MA, Negredo AI, Estrada-Peña A, Barrett ADT, Bente DA. Genomic Characterization of Crimean-Congo Hemorrhagic Fever Virus in Hyalomma Tick from Spain, 2014.. Vector Borne Zoonotic Dis 2017 Oct;17(10):714-719.
    doi: 10.1089/vbz.2017.2190pmc: PMC7643767pubmed: 28836897google scholar: lookup
  65. Monsalve-Arteaga L, Alonso-Sardón M, Muñoz Bellido JL, Vicente Santiago MB, Vieira Lista MC, López Abán J, Muro A, Belhassen-García M. Seroprevalence of Crimean-Congo hemorrhagic fever in humans in the World Health Organization European region: A systematic review.. PLoS Negl Trop Dis 2020 Mar;14(3):e0008094.
    doi: 10.1371/journal.pntd.0008094pmc: PMC7067482pubmed: 32119682google scholar: lookup
  66. Gargili A, Estrada-Peña A, Spengler JR, Lukashev A, Nuttall PA, Bente DA. The role of ticks in the maintenance and transmission of Crimean-Congo hemorrhagic fever virus: A review of published field and laboratory studies.. Antiviral Res 2017 Aug;144:93-119.
    doi: 10.1016/j.antiviral.2017.05.010pmc: PMC6047067pubmed: 28579441google scholar: lookup
  67. Hawman DW, Feldmann H. Recent advances in understanding Crimean-Congo hemorrhagic fever virus.. F1000Res 2018;7.
    doi: 10.12688/f1000research.16189.1pmc: PMC6206615pubmed: 30416710google scholar: lookup
  68. Zeller HG, Cornet JP, Camicas JL. Experimental transmission of Crimean-Congo hemorrhagic fever virus by west African wild ground-feeding birds to Hyalomma marginatum rufipes ticks.. Am J Trop Med Hyg 1994 Jun;50(6):676-81.
    doi: 10.4269/ajtmh.1994.50.676pubmed: 8024058google scholar: lookup
  69. Palomar AM, Portillo A, Mazuelas D, Roncero L, Arizaga J, Crespo A, Gutiérrez Ó, Márquez FJ, Cuadrado JF, Eiros JM, Oteo JA. Molecular analysis of Crimean-Congo hemorrhagic fever virus and Rickettsia in Hyalomma marginatum ticks removed from patients (Spain) and birds (Spain and Morocco), 2009-2015.. Ticks Tick Borne Dis 2016 Jul;7(5):983-987.
    doi: 10.1016/j.ttbdis.2016.05.004pubmed: 27215620google scholar: lookup
  70. Spiegelaar N. The role of birds in disseminating ticks and tick-borne diseases of veterinary and medical importance.. Thesis Utrecht University, The Netherlands 2015.
  71. Parola P, Paddock CD, Raoult D. Tick-borne rickettsioses around the world: emerging diseases challenging old concepts.. Clin Microbiol Rev 2005 Oct;18(4):719-56.
    doi: 10.1128/CMR.18.4.719-756.2005pmc: PMC1265907pubmed: 16223955google scholar: lookup
  72. Alberdi MP, Dalby MJ, Rodriguez-Andres J, Fazakerley JK, Kohl A, Bell-Sakyi L. Detection and identification of putative bacterial endosymbionts and endogenous viruses in tick cell lines.. Ticks Tick Borne Dis 2012 Jun;3(3):137-46.
    doi: 10.1016/j.ttbdis.2012.05.002pmc: PMC3431536pubmed: 22743047google scholar: lookup
  73. OIE: WAHIS Interface World Animal Health Disease Information.
  74. Butler CM, Sloet van Oldruitenborgh-Oosterbaan MM, Stout TA, van der Kolk JH, Wollenberg Lv, Nielen M, Jongejan F, Werners AH, Houwers DJ. Prevalence of the causative agents of equine piroplasmosis in the South West of The Netherlands and the identification of two autochthonous clinical Theileria equi infections.. Vet J 2012 Aug;193(2):381-5.
    pubmed: 22266019doi: 10.1016/j.tvjl.2011.12.014google scholar: lookup
  75. Jongejan F, Ringenier M, Putting M, Berger L, Burgers S, Kortekaas R, Lenssen J, van Roessel M, Wijnveld M, Madder M. Novel foci of Dermacentor reticulatus ticks infected with Babesia canis and Babesia caballi in the Netherlands and in Belgium.. Parasit Vectors 2015 Apr 17;8:232.
    doi: 10.1186/s13071-015-0841-2pmc: PMC4404102pubmed: 25889392google scholar: lookup
  76. Onyiche TE, Suganuma K, Igarashi I, Yokoyama N, Xuan X, Thekisoe O. A Review on Equine Piroplasmosis: Epidemiology, Vector Ecology, Risk Factors, Host Immunity, Diagnosis and Control.. Int J Environ Res Public Health 2019 May 16;16(10).
    doi: 10.3390/ijerph16101736pmc: PMC6572709pubmed: 31100920google scholar: lookup

Citations

This article has been cited 23 times.
  1. Keve G, Csörgő T, Benke A, Huber A, Mórocz A, Németh Á, Kalocsa B, Tamás EA, Gyurácz J, Kiss O, Kováts D, Sándor AD, Karcza Z, Hornok S. Ornithological and molecular evidence of a reproducing Hyalomma rufipes population under continental climate in Europe. Front Vet Sci 2023;10:1147186.
    doi: 10.3389/fvets.2023.1147186pubmed: 37035818google scholar: lookup
  2. Guccione C, Colomba C, Iaria C, Cascio A. Rickettsiales in the WHO European Region: an update from a One Health perspective. Parasit Vectors 2023 Jan 30;16(1):41.
    doi: 10.1186/s13071-022-05646-4pubmed: 36717936google scholar: lookup
  3. Bonnet SI, Vourc'h G, Raffetin A, Falchi A, Figoni J, Fite J, Hoch T, Moutailler S, Quillery E. The control of Hyalomma ticks, vectors of the Crimean-Congo hemorrhagic fever virus: Where are we now and where are we going?. PLoS Negl Trop Dis 2022 Nov;16(11):e0010846.
    doi: 10.1371/journal.pntd.0010846pubmed: 36395110google scholar: lookup
  4. Hansford KM, Gandy SL, Gillingham EL, McGinley L, Cull B, Johnston C, Catton M, Medlock JM. Mapping and monitoring tick (Acari, Ixodida) distribution, seasonality, and host associations in the United Kingdom between 2017 and 2020. Med Vet Entomol 2023 Mar;37(1):152-163.
    doi: 10.1111/mve.12621pubmed: 36309852google scholar: lookup
  5. Graham H, van Kalsbeek P, van der Goot J, Koene MGJ. Low seroprevalence of equine piroplasmosis in horses exported from the Netherlands between 2015 and 2021. Front Vet Sci 2022;9:954046.
    doi: 10.3389/fvets.2022.954046pubmed: 36299627google scholar: lookup
  6. Duscher GG, Kienberger S, Haslinger K, Holzer B, Zimpernik I, Fuchs R, Schwarz M, Hufnagl P, Schiefer P, Schmoll F. Hyalomma spp. in Austria-The Tick, the Climate, the Diseases and the Risk for Humans and Animals. Microorganisms 2022 Aug 31;10(9).
    doi: 10.3390/microorganisms10091761pubmed: 36144363google scholar: lookup
  7. Garcia-Vozmediano A, De Meneghi D, Sprong H, Portillo A, Oteo JA, Tomassone L. A One Health Evaluation of the Surveillance Systems on Tick-Borne Diseases in the Netherlands, Spain and Italy. Vet Sci 2022 Sep 14;9(9).
    doi: 10.3390/vetsci9090504pubmed: 36136720google scholar: lookup
  8. Onstwedder C, Lock-Wah-Hoon J, van Dorp S, Braks M, van Asten L, Zheng Y, Krafft T, Tong Y, van der Hoek W, Liu QY, Pilot E, Wang Q, Fanoy E. Comparing Vector-Borne Disease Surveillance and Response in Beijing and the Netherlands. Ann Glob Health 2022;88(1):59.
    doi: 10.5334/aogh.3672pubmed: 35974985google scholar: lookup
  9. Földvári G, Szabó É, Tóth GE, Lanszki Z, Zana B, Varga Z, Kemenesi G. Emergence of Hyalomma marginatum and Hyalomma rufipes adults revealed by citizen science tick monitoring in Hungary. Transbound Emerg Dis 2022 Sep;69(5):e2240-e2248.
    doi: 10.1111/tbed.14563pubmed: 35436033google scholar: lookup
  10. Stroffolini G, Segala FV, Lupia T, Faraoni S, Rossi L, Tomassone L, Zanet S, De Rosa FG, Di Perri G, Calcagno A. Serology for Borrelia spp. in Northwest Italy: A Climate-Matched 10-Year Trend. Life (Basel) 2021 Nov 27;11(12).
    doi: 10.3390/life11121310pubmed: 34947841google scholar: lookup
  11. Dwużnik-Szarek D, Mierzejewska EJ, Bajer A. Occurrence of juvenile Dermacentor reticulatus ticks in three regions in Poland: the final evidence of the conquest. Parasit Vectors 2021 Oct 14;14(1):536.
    doi: 10.1186/s13071-021-05039-zpubmed: 34649613google scholar: lookup
  12. Ahmad H, Aool W, Anyango V, Nakayaki TM, Mulwa F, Chelangat B, Lutwama JJ, Kayondo JK, Lukindu M, Mutisya J, Lutomiah J, Hensley LE, Cohnstaedt LW, Onyango MG, Brelsfoard CL. Development and Characterization of Microsatellite Genetic Markers for Hyalomma rufipes, a Tick Vector of Crimean-Congo Hemorrhagic Fever Virus. Ecol Evol 2026 Feb;16(2):e73064.
    doi: 10.1002/ece3.73064pubmed: 41659308google scholar: lookup
  13. Giupponi C, Jourdan-Pineau H, Bernard C, Blanda V, Bourquia M, Bru D, Cabezón O, Carrera-Faja L, Espunyes J, Gottlieb Y, Joly-Kukla C, Malandrin L, Mechouk N, Mihalca AD, Pollet T, Saengram P, Torina A, Valcárcel F, Vatansever Z, Vial L, Zahri A, Verheyden H, Huber K. Tracking invasion events: phylogeography of Hyalomma marginatum in the Mediterranean basin with a focus on Southern France. Parasit Vectors 2025 Oct 14;18(1):407.
    doi: 10.1186/s13071-025-06927-4pubmed: 41088284google scholar: lookup
  14. Abdelali SK, Aissaoui L, Cano-Argüelles AL, Piloto-Sardiñas E, Abuin-Denis L, Maitre A, Foucault-Simonin A, Mateos-Hernández L, Kratou M, Wu-Chuang A, Obregon D, Cabezas-Cruz A. Seasonal Variations in the Microbiome of Hyalomma excavatum Ticks in Algeria. Microb Ecol 2025 Sep 30;88(1):96.
    doi: 10.1007/s00248-025-02597-ypubmed: 41026240google scholar: lookup
  15. Romanek W, Dwużnik-Szarek D, Wężyk D, Małaszewicz W, Alsarraf M, Myczka AW, Bajer A. The first finding of Hyalomma rufipes in Poland in 2024: the promising start of a citizen science project. Parasit Vectors 2025 Sep 24;18(1):383.
    doi: 10.1186/s13071-025-07022-4pubmed: 40993823google scholar: lookup
  16. Bylińska K, Rapczyński J, Górski P, Obuch-Woszczatyńska O, Pietrzak D, Korzekwa K, Krzyżowska M, Bąska P. Identification of Hyalomma Ticks on Migratory Birds in Poland During the 2023 and 2024 Spring Seasons. Life (Basel) 2025 Aug 19;15(8).
    doi: 10.3390/life15081311pubmed: 40868958google scholar: lookup
  17. Celina SS, Černý J. Hyalomma marginatum in Europe: The Past, Current Status, and Future Challenges-A Systematic Review. Transbound Emerg Dis 2025;2025:7771431.
    doi: 10.1155/tbed/7771431pubmed: 40765715google scholar: lookup
  18. Tonk-Rügen M, Kratou M, Cabezas-Cruz A. A Warming World, a Growing Threat: The Spread of Ticks and Emerging Tick-Borne Diseases. Pathogens 2025 Feb 21;14(3).
    doi: 10.3390/pathogens14030213pubmed: 40137698google scholar: lookup
  19. Ullah Z, Liaqat I, Khan M, Alouffi A, Almutairi MM, Apanaskevich DA, Tanaka T, Ali A. Investigation of Hyalomma turanicum and Hyalomma asiaticum in Pakistan, with notes on the detection of tickborne Rickettsiales. Front Vet Sci 2024;11:1500930.
    doi: 10.3389/fvets.2024.1500930pubmed: 39764368google scholar: lookup
  20. Menzano A, Tizzani P, Farber MD, Garcia-Vozmediano A, Martinelli L, Rossi L, Tomassone L. Zoonotic Tick-Borne Pathogens in Ticks from Vegetation and Alpine Ibex (Capra ibex) in the Maritime Alps, Italy. Animals (Basel) 2024 Aug 2;14(15).
    doi: 10.3390/ani14152251pubmed: 39123777google scholar: lookup
  21. Fair JM, Al-Hmoud N, Alrwashdeh M, Bartlow AW, Balkhamishvili S, Daraselia I, Elshoff A, Fakhouri L, Javakhishvili Z, Khoury F, Muzyka D, Ninua L, Tsao J, Urushadze L, Owen J. Transboundary determinants of avian zoonotic infectious diseases: challenges for strengthening research capacity and connecting surveillance networks. Front Microbiol 2024;15:1341842.
    doi: 10.3389/fmicb.2024.1341842pubmed: 38435695google scholar: lookup
  22. Bacak E, Ozsemir AC, Akyildiz G, Gungor U, Bente D, Keles AG, Beskardes V, Kar S. Bidirectional tick transport by migratory birds of the African-Western Palearctic flyway over Turkish Thrace: observation of the current situation and future projection. Parasitol Res 2023 Dec 13;123(1):37.
    doi: 10.1007/s00436-023-08069-xpubmed: 38087074google scholar: lookup
  23. Beermann S, Dobler G, Faber M, Frank C, Habedank B, Hagedorn P, Kampen H, Kuhn C, Nygren T, Schmidt-Chanasit J, Schmolz E, Stark K, Ulrich RG, Weiss S, Wilking H. Impact of climate change on vector- and rodent-borne infectious diseases. J Health Monit 2023 Jun;8(Suppl 3):33-61.
    doi: 10.25646/11401pubmed: 37342429google scholar: lookup
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