Analyze Diet
Viruses2019; 12(1); doi: 10.3390/v12010023

Viral Equine Encephalitis, a Growing Threat to the Horse Population in Europe?

Abstract: Neurological disorders represent an important sanitary and economic threat for the equine industry worldwide. Among nervous diseases, viral encephalitis is of growing concern, due to the emergence of arboviruses and to the high contagiosity of herpesvirus-infected horses. The nature, severity and duration of the clinical signs could be different depending on the etiological agent and its virulence. However, definite diagnosis generally requires the implementation of combinations of direct and/or indirect screening assays in specialized laboratories. The equine practitioner, involved in a mission of prevention and surveillance, plays an important role in the clinical diagnosis of viral encephalitis. The general management of the horse is essentially supportive, focused on controlling pain and inflammation within the central nervous system, preventing injuries and providing supportive care. Despite its high medical relevance and economic impact in the equine industry, vaccines are not always available and there is no specific antiviral therapy. In this review, the major virological, clinical and epidemiological features of the main neuropathogenic viruses inducing encephalitis in equids in Europe, including rabies virus (Rhabdoviridae), Equid herpesviruses (Herpesviridae), Borna disease virus (Bornaviridae) and West Nile virus (Flaviviridae), as well as exotic viruses, will be presented.
Publication Date: 2019-12-24 PubMed ID: 31878129PubMed Central: PMC7019608DOI: 10.3390/v12010023Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • Non-U.S. Gov't
  • Review

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 researchers are investigating the increased concern of viral encephalitis, a neurological disorder, in horses due to rising numbers of arbovirus and highly contagious herpesvirus. The study includes the major characteristics, clinical symptoms, and epidemiology of various viruses causing encephalitis, such as rabies, Equid herpesviruses, Borna disease virus, and West Nile virus. However, there is currently no specific antiviral therapy, and vaccines are not always available.

Understanding Viral Encephalitis in Horses

  • The authors of this research article state that neurological disorders, particularly viral encephalitis, are posing a significant health and economic risk to the global equine industry. Viral encephalitis in horses is an increasing concern mainly due to the emergence of arboviruses and the high contagion level of herpesvirus-infected horses.
  • The symptoms’ nature, severity, and duration can vary widely depending upon the causative agent and its virulence. Confirming the diagnosis typically requires a mix of direct or indirect screening tests conducted in specialized labs.
  • The equine practitioner has a central role in diagnosing viral encephalitis given their interaction with horses. Interactions focused on prevention, regular surveillance, and noting any unusual behavior or symptoms.

The Management and Prevention of Equine Viral Encephalitis

  • According to the article, the general management of equine viral encephalitis is predominantly supportive. It’s mainly geared towards controlling pain, reducing inflammation in the CNS (central nervous system), preventing injuries, and offering palliative care.
  • As the disease has notable medical significance and affects the equine industry economically, the lack of specific antiviral therapy makes effective management all the more critical. Vaccines also aren’t always available, which further reinforces the importance of appropriate management and prevention strategies.

Analysis of Viruses Inducing Encephalitis in Europe

  • The review presents an in-depth analysis of the significant virological, clinical, and epidemiological features of the neuropathogenic viruses that cause encephalitis in horses. Some common examples include the rabies virus, Equid herpesviruses, Borna disease virus, and West Nile virus. It also provides a glimpse of different types of exotic viruses.
  • Through this comprehensive study of these viruses, the research attempts to increase understanding of the growing threat they present and highlight areas that may require more research to develop effective treatments and preventive tools.

Cite This Article

APA
Lecollinet S, Pronost S, Coulpier M, Beck C, Gonzalez G, Leblond A, Tritz P. (2019). Viral Equine Encephalitis, a Growing Threat to the Horse Population in Europe? Viruses, 12(1). https://doi.org/10.3390/v12010023

Publication

ISSN: 1999-4915
NlmUniqueID: 101509722
Country: Switzerland
Language: English
Volume: 12
Issue: 1

Researcher Affiliations

Lecollinet, Sylvie
  • UMR (Unité Mixte de Recherche) 1161 Virologie, Anses (the French Agency for Food, Environmental and Occupational Health and Safety), INRAE (French National Institute of Agricultural, Food and Environmental Research), Ecole Nationale Vétérinaire d'Alfort, Université Paris-Est, 94700 Maisons-Alfort, France.
  • RESPE (Réseau d'épidémio-surveillance en pathologie équine), 14280 Saint-Contest, France.
Pronost, Stéphane
  • RESPE (Réseau d'épidémio-surveillance en pathologie équine), 14280 Saint-Contest, France.
  • LABÉO, 14280 Saint-Contest, France.
  • BIOTARGEN, UNICAEN, NORMANDIE UNIV, 14000 Caen, France.
Coulpier, Muriel
  • UMR (Unité Mixte de Recherche) 1161 Virologie, Anses (the French Agency for Food, Environmental and Occupational Health and Safety), INRAE (French National Institute of Agricultural, Food and Environmental Research), Ecole Nationale Vétérinaire d'Alfort, Université Paris-Est, 94700 Maisons-Alfort, France.
Beck, Cécile
  • UMR (Unité Mixte de Recherche) 1161 Virologie, Anses (the French Agency for Food, Environmental and Occupational Health and Safety), INRAE (French National Institute of Agricultural, Food and Environmental Research), Ecole Nationale Vétérinaire d'Alfort, Université Paris-Est, 94700 Maisons-Alfort, France.
  • RESPE (Réseau d'épidémio-surveillance en pathologie équine), 14280 Saint-Contest, France.
Gonzalez, Gaelle
  • UMR (Unité Mixte de Recherche) 1161 Virologie, Anses (the French Agency for Food, Environmental and Occupational Health and Safety), INRAE (French National Institute of Agricultural, Food and Environmental Research), Ecole Nationale Vétérinaire d'Alfort, Université Paris-Est, 94700 Maisons-Alfort, France.
Leblond, Agnès
  • UMR EPIA (Epidémiologie des Maladies Animales et Zoonotiques), INRAE, VetAgro Sup, Université de Lyon, 69280 Marcy L'Etoile, France.
Tritz, Pierre
  • RESPE (Réseau d'épidémio-surveillance en pathologie équine), 14280 Saint-Contest, France.
  • Clinique Vétérinaire, 19 rue de Créhange, 57380 Faulquemont, France.
  • AVEF (Association Vétérinaire Equine Française), Committee on Infectious Diseases, 75011 Paris, France.

MeSH Terms

  • Animals
  • Arboviruses / pathogenicity
  • Bornaviridae / pathogenicity
  • Encephalomyelitis, Equine / complications
  • Encephalomyelitis, Equine / epidemiology
  • Encephalomyelitis, Equine / veterinary
  • Europe / epidemiology
  • Herpesviridae / pathogenicity
  • Horse Diseases / epidemiology
  • Horse Diseases / virology
  • Horses
  • Humans
  • Rhabdoviridae / pathogenicity
  • Viruses / classification
  • Viruses / pathogenicity
  • West Nile virus / pathogenicity

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 193 references
  1. Pellegrini-Masini A., Livesey L.C.. Meningitis and encephalomyelitis in horses. Vet. Clin. N. Am. Equine Pract. 2006;22:553–589.
    doi: 10.1016/j.cveq.2006.03.003pubmed: 16882487google scholar: lookup
  2. Leblond A., Villard I., Leblond L., Sabatier P., Sasco A.J.. A retrospective evaluation of the causes of death of 448 insured French horses in 1995. Vet. Res. Commun. 2000;24:85–102.
    doi: 10.1023/A:1006408522233pubmed: 10720095google scholar: lookup
  3. Tyler C.M., Davis R.E., Begg A.P., Hutchins D.R., Hodgson D.R.. A survey of neurological diseases in horses. Aust. Vet. J. 1993;70:445–449.
  4. Laugier C.T., Tapprest J.. Fréquence de la pathologie nerveuse et de ses différentes causes dans un effectif de 4319 chevaux autopsiés. Bull. Epidémiologique St. Anim. Et Aliment. Spécial Équidé 2012;19:9.
  5. Kumar B., Manuja A., Gulati B.R., Virmani N., Tripathi B.N.. Zoonotic Viral Diseases of Equines and Their Impact on Human and Animal Health. Open Virol. J. 2018;12:80–98.
    doi: 10.2174/1874357901812010080pmc: PMC6142672pubmed: 30288197google scholar: lookup
  6. Walker P.J., Siddell S.G., Lefkowitz E.J., Mushegian A.R., Dempsey D.M., Dutilh B.E., Harrach B., Harrison R.L., Hendrickson R.C., Junglen S.. Changes to virus taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2019). Arch. Virol. 2019;164:2417–2429.
    doi: 10.1007/s00705-019-04306-wpubmed: 31187277google scholar: lookup
  7. Viralzone, SIB Swiss Institute of Bioinformatics. [(accessed on 15 December 2019)]; Available online: www.expasy.org/viralzone.
  8. Mayhew I.G., de Lahunta A., Whitlock R.H., Krook L., Tasker J.B.. Spinal cord disease in the horse. Cornell. Vet. 1978;68:1–207.
    pubmed: 618720
  9. Porter R.S., Leblond A., Lecollinet S., Tritz P., Cantile C., Kutasi O., Zientara S., Pradier S., van Galen G., Speybroek N.. Clinical diagnosis of West Nile Fever in Equids by classification and regression tree (CART) analysis and comparative study of clinical appearance in three European countries. Transbound. Emerg. Dis. 2011;58:197–205.
  10. Van Galen G., Leblond A., Tritz P., Martinelle L., Pronost S., Saegerman C.. A retrospective study on equine herpesvirus type-1 associated myeloencephalopathy in France (2008–2011). Vet. Microbiol. 2015;179:304–309.
    doi: 10.1016/j.vetmic.2015.07.003pubmed: 26228835google scholar: lookup
  11. Pronost S., Legrand L., Pitel P.H., Wegge B., Lissens J., Freymuth F., Richard E., Fortier G.. Outbreak of equine herpesvirus myeloencephalopathy in France: A clinical and molecular investigation. Transbound. Emerg. Dis. 2012;59:256–263.
  12. Knox J., Cowan R.U., Doyle J.S., Ligtermoet M.K., Archer J.S., Burrow J.N., Tong S.Y., Currie B.J., Mackenzie J.S., Smith D.W.. Murray Valley encephalitis: A review of clinical features, diagnosis and treatment. Med. J. Aust. 2012;196:322–326.
    doi: 10.5694/mja11.11026pubmed: 22432670google scholar: lookup
  13. RESPE. [(accessed on 15 December 2019)]; Available online: http://www.respe.net.
  14. EQUINELLA. [(accessed on 15 December 2019)]; Available online: http://www.equinella.ch.
  15. World Organisation for Animal Health (OIE), Animal Health Information. [(accessed on 15 December 2019)]; Available online: https://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/Immsummary.
  16. Promed, International Society for Infectious Diseases. [(accessed on 15 December 2019)]; Available online: https://promedmail.org/
  17. ECDC Epidemiological Update: West Nile Virus Transmission Season in Europe. [(accessed on 28 November 2019)]; Available online: https://www.ecdc.europa.eu/en/news-events/epidemiological-update-west-nile-virus-transmission-season-europe-2018.
  18. Dunowska M.. A review of equid herpesvirus 1 for the veterinary practitioner. Part B: Pathogenesis and epidemiology. N. Z. Vet. J. 2014;62:179–188.
    doi: 10.1080/00480169.2014.899946pubmed: 24597839google scholar: lookup
  19. BioRender. [(accessed on 15 December 2019)]; Available online: https//app.biorender.com/
  20. Weaver S.C., Reisen W.K.. Present and future arboviral threats. Antiviral Res. 2010;85:328–345.
  21. Chapman G.E., Baylis M., Archer D., Daly J.M.. The challenges posed by equine arboviruses. Equine Vet. J. 2018;50:436–445.
    doi: 10.1111/evj.12829pubmed: 29517814google scholar: lookup
  22. Davison A.J., Eberle R., Ehlers B., Hayward G.S., McGeoch D.J., Minson A.C., Pellett P.E., Roizman B., Studdert M.J., Thiry E.. The order Herpesvirales. Arch. Virol. 2009;154:171–177.
    doi: 10.1007/s00705-008-0278-4pmc: PMC3552636pubmed: 19066710google scholar: lookup
  23. Abdelgawad A., Damiani A., Ho S.Y., Strauss G., Szentiks C.A., East M.L., Osterrieder N., Greenwood A.D.. Zebra Alphaherpesviruses (EHV-1 and EHV-9): Genetic Diversity, Latency and Co-Infections. Viruses 2016;8:262.
    doi: 10.3390/v8090262pmc: PMC5035975pubmed: 27657113google scholar: lookup
  24. Garvey M., Suarez N.M., Kerr K., Hector R., Moloney-Quinn L., Arkins S., Davison A.J., Cullinane A.. Equid herpesvirus 8: Complete genome sequence and association with abortion in mares. PLoS ONE 2018;13:e0192301.
  25. Saxegaard F.. Isolation and identification of equine rhinopneumonitis virus (equine abortion virus) from cases of abortion and paralysis. Nord. Vet. Med. 1966;18:504–516.
  26. Ma G., Azab W., Osterrieder N.. Equine herpesviruses type 1 (EHV-1) and 4 (EHV-4)—Masters of co-evolution and a constant threat to equids and beyond. Vet. Microbiol. 2013;167:123–134.
    doi: 10.1016/j.vetmic.2013.06.018pubmed: 23890672google scholar: lookup
  27. Chesters P.M., Allsop R., Purewal A., Edington N.. Detection of latency-associated transcripts of equid herpesvirus 1 in equine leukocytes but not in trigeminal ganglia. J. Virol. 1997;71:3437–3443.
    pmc: PMC191489pubmed: 9094614
  28. Oladunni F.S., Horohov D.W., Chambers T.M.. EHV-1: A constant threat to the horse industry. Front. Microbiol. 2019;10:2668.
    doi: 10.3389/fmicb.2019.02668pmc: PMC6901505pubmed: 31849857google scholar: lookup
  29. Telford E.A., Watson M.S., McBride K., Davison A.J.. The DNA sequence of equine herpesvirus-1. Virology 1992;189:304–316.
    doi: 10.1016/0042-6822(92)90706-Upubmed: 1318606google scholar: lookup
  30. Dayaram A., Franz M., Schattschneider A., Damiani A.M., Bischofberger S., Osterrieder N., Greenwood A.D.. Long term stability and infectivity of herpesviruses in water. Sci. Rep. 2017;7:46559.
    doi: 10.1038/srep46559pmc: PMC5399353pubmed: 28429732google scholar: lookup
  31. Foote C.E., Love D.N., Gilkerson J.R., Whalley J.M.. Detection of EHV-1 and EHV-4 DNA in unweaned Thoroughbred foals from vaccinated mares on a large stud farm. Equine Vet. J. 2004;36:341–345.
    doi: 10.2746/0425164044890634pubmed: 15163042google scholar: lookup
  32. Kydd J.H., Lunn D.P., Osterrieder K.. Report of the Fourth International Havemeyer Workshop on Equid Herpesviruses (EHV) EHV-1, EHV-2 and EHV-5. Equine Vet. J. 2019;51:565–568.
    doi: 10.1111/evj.13141pubmed: 31373057google scholar: lookup
  33. Vissani M.A., Becerra M.L., Olguin Perglione C., Tordoya M.S., Mino S., Barrandeguy M.. Neuropathogenic and non-neuropathogenic genotypes of Equid Herpesvirus type 1 in Argentina. Vet. Microbiol. 2009;139:361–364.
    doi: 10.1016/j.vetmic.2009.06.025pubmed: 19589651google scholar: lookup
  34. Paillot R.C., Case R., Ross J., Newton R., Nugent J.. Equine Herpes Virus-1: Virus, Immunity and Vaccines. TOVSJ 2008;2:68–91.
  35. Crabb B.S., Studdert M.J.. Equine herpesviruses 4 (equine rhinopneumonitis virus) and 1 (equine abortion virus). Adv. Virus Res. 1995;45:153–190.
    pubmed: 7793324
  36. Edington N., Smyth B., Griffiths L.. The role of endothelial cell infection in the endometrium, placenta and foetus of equid herpesvirus 1 (EHV-1) abortions. J. Comp. Pathol. 1991;104:379–387.
    doi: 10.1016/S0021-9975(08)80148-Xpubmed: 1651960google scholar: lookup
  37. Whitwell K.E., Blunden A.S.. Pathological findings in horses dying during an outbreak of the paralytic form of Equid herpesvirus type 1 (EHV-1) infection. Equine Vet. J. 1992;24:13–19.
  38. Slater J.D., Lunn D.P., Horohov D.W., Antczak D.F., Babiuk L., Breathnach C., Chang Y.W., Davis-Poynter N., Edington N., Ellis S.. Report of the equine herpesvirus-1 Havermeyer Workshop, San Gimignano, Tuscany, June 2004. Vet. Immunol. Immunopathol. 2006;111:3–13.
    doi: 10.1016/j.vetimm.2006.01.004pubmed: 16542736google scholar: lookup
  39. Van Maanen C.. Equine herpesvirus 1 and 4 infections: An update. Vet. Q. 2002;24:58–78.
    doi: 10.1080/01652176.2002.9695126pubmed: 12095082google scholar: lookup
  40. Kydd J.H., Slater J., Osterrieder N., Antczak D.F., Lunn D.P.. Report of the Second Havemeyer EHV-1 Workshop, Steamboat Springs, Colorado, USA, September 2008. Equine Vet. J. 2010;42:572–575.
  41. Lunn D.P., Davis-Poynter N., Flaminio M.J., Horohov D.W., Osterrieder K., Pusterla N., Townsend H.G.. Equine herpesvirus-1 consensus statement. J. Vet. Intern. Med. 2009;23:450–461.
  42. Goehring L.S., van Winden S.C., van Maanen C., Sloet van Oldruitenborgh-Oosterbaan M.M.. Equine herpesvirus type 1-associated myeloencephalopathy in The Netherlands: A four-year retrospective study (1999–2003). J. Vet. Intern. Med. 2006;20:601–607.
  43. Pronost S., Leon A., Legrand L., Fortier C., Miszczak F., Freymuth F., Fortier G.. Neuropathogenic and non-neuropathogenic variants of equine herpesvirus 1 in France. Vet. Microbiol. 2010;145:329–333.
    doi: 10.1016/j.vetmic.2010.03.031pubmed: 20427133google scholar: lookup
  44. Sutton G., Garvey M., Cullinane A., Jourdan M., Fortier C., Moreau P., Foursin M., Gryspeerdt A., Maisonnier V., Marcillaud-Pitel C.. Molecular Surveillance of EHV-1 Strains Circulating in France during and after the Major 2009 Outbreak in Normandy Involving Respiratory Infection, Neurological Disorder, and Abortion. Viruses 2019;11:916.
    doi: 10.3390/v11100916pmc: PMC6832873pubmed: 31590336google scholar: lookup
  45. Allen G.P.. Risk factors for development of neurologic disease after experimental exposure to equine herpesvirus-1 in horses. Am. J. Vet. Res. 2008;69:1595–1600.
    doi: 10.2460/ajvr.69.12.1595pubmed: 19046006google scholar: lookup
  46. Goodman L.B., Loregian A., Perkins G.A., Nugent J., Buckles E.L., Mercorelli B., Kydd J.H., Palu G., Smith K.C., Osterrieder N.. A point mutation in a herpesvirus polymerase determines neuropathogenicity. PLoS Pathog. 2007;3:e160.
  47. Goehring L.S., van Maanen C., Berendsen M., Cullinane A., de Groot R.J., Rottier P.J., Wesselingh J.J., Sloet van Oldruitenborgh-Oosterbaan M.M.. Experimental infection with neuropathogenic equid herpesvirus type 1 (EHV-1) in adult horses. Vet. J. 2010;186:180–187.
    doi: 10.1016/j.tvjl.2009.08.007pubmed: 19726209google scholar: lookup
  48. Nugent J., Birch-Machin I., Smith K.C., Mumford J.A., Swann Z., Newton J.R., Bowden R.J., Allen G.P., Davis-Poynter N.. Analysis of equid herpesvirus 1 strain variation reveals a point mutation of the DNA polymerase strongly associated with neuropathogenic versus nonneuropathogenic disease outbreaks. J. Virol. 2006;80:4047–4060.
  49. Allen G.P., Breathnach C.C.. Quantification by real-time PCR of the magnitude and duration of leucocyte-associated viraemia in horses infected with neuropathogenic vs. non-neuropathogenic strains of EHV-1. Equine Vet. J. 2006;38:252–257.
    doi: 10.2746/042516406776866453pubmed: 16706281google scholar: lookup
  50. Allen G.P.. Development of a real-time polymerase chain reaction assay for rapid diagnosis of neuropathogenic strains of equine herpesvirus-1. J. Vet. Diagn. Investig. 2007;19:69–72.
    doi: 10.1177/104063870701900110pubmed: 17459834google scholar: lookup
  51. Perkins G.A., Goodman L.B., Tsujimura K., Van de Walle G.R., Kim S.G., Dubovi E.J., Osterrieder N.. Investigation of the prevalence of neurologic equine herpes virus type 1 (EHV-1) in a 23-year retrospective analysis (1984–2007). Vet. Microbiol. 2009;139:375–378.
    doi: 10.1016/j.vetmic.2009.06.033pubmed: 19615831google scholar: lookup
  52. Pronost S., Cook R.F., Fortier G., Timoney P.J., Balasuriya U.B.. Relationship between equine herpesvirus-1 myeloencephalopathy and viral genotype. Equine Vet. J. 2010;42:672–674.
  53. Patel J.R., Heldens J.. Equine herpesviruses 1 (EHV-1) and 4 (EHV-4)—Epidemiology, disease and immunoprophylaxis: A brief review. Vet. J. 2005;170:14–23.
    doi: 10.1016/j.tvjl.2004.04.018pubmed: 15993786google scholar: lookup
  54. Goodman L.B., Wagner B., Flaminio M.J., Sussman K.H., Metzger S.M., Holland R., Osterrieder N.. Comparison of the efficacy of inactivated combination and modified-live virus vaccines against challenge infection with neuropathogenic equine herpesvirus type 1 (EHV-1). Vaccine 2006;24:3636–3645.
    doi: 10.1016/j.vaccine.2006.01.062pubmed: 16513225google scholar: lookup
  55. Garre B., Gryspeerdt A., Croubels S., De Backer P., Nauwynck H.. Evaluation of orally administered valacyclovir in experimentally EHV1-infected ponies. Vet. Microbiol. 2009;135:214–221.
    doi: 10.1016/j.vetmic.2008.09.062pubmed: 18986780google scholar: lookup
  56. Thieulent C.J., Hue E.S., Fortier C.I., Dallemagne P., Zientara S., Munier-Lehmann H., Hans A., Fortier G.D., Pitel P.H., Vidalain P.O.. Screening and evaluation of antiviral compounds against Equid alpha-herpesviruses using an impedance-based cellular assay. Virology 2019;526:105–116.
    doi: 10.1016/j.virol.2018.10.013pubmed: 30388626google scholar: lookup
  57. Vissani M.A., Thiry E., Dal Pozzo F., Barrandeguy M.. Antiviral agents against equid alphaherpesviruses: Current status and perspectives. Vet. J. 2016;207:38–44.
    doi: 10.1016/j.tvjl.2015.06.010pubmed: 26654843google scholar: lookup
  58. Nolden T., Banyard A.C., Finke S., Fooks A.R., Hanke D., Hoper D., Horton D.L., Mettenleiter T.C., Muller T., Teifke J.P.. Comparative studies on the genetic, antigenic and pathogenic characteristics of Bokeloh bat lyssavirus. J. Gen. Virol. 2014;95:1647–1653.
    doi: 10.1099/vir.0.065953-0pmc: PMC4103065pubmed: 24828330google scholar: lookup
  59. Malerczyk C., Freuling C., Gniel D., Giesen A., Selhorst T., Muller T.. Cross-neutralization of antibodies induced by vaccination with Purified Chick Embryo Cell Vaccine (PCECV) against different Lyssavirus species. Hum. Vaccin. Immunother. 2014;10:2799–2804.
  60. Gunawardena P.S., Marston D.A., Ellis R.J., Wise E.L., Karawita A.C., Breed A.C., McElhinney L.M., Johnson N., Banyard A.C., Fooks A.R.. Lyssavirus in Indian Flying Foxes, Sri Lanka. Emerg. Infect. Dis. 2016;22:1456–1459.
    doi: 10.3201/eid2208.151986pmc: PMC4982157pubmed: 27434858google scholar: lookup
  61. Hayman D.T., Fooks A.R., Marston D.A., Garcia R.J.. The Global Phylogeography of Lyssaviruses-Challenging the ‘Out of Africa’ Hypothesis. PLoS Negl. Trop. Dis. 2016;10:e0005266.
  62. Rupprecht C.E., Turmelle A., Kuzmin I.V.. A perspective on lyssavirus emergence and perpetuation. Curr. Opin. Virol. 2011;1:662–670.
    doi: 10.1016/j.coviro.2011.10.014pubmed: 22440925google scholar: lookup
  63. Johnson N., Vos A., Freuling C., Tordo N., Fooks A.R., Muller T.. Human rabies due to lyssavirus infection of bat origin. Vet. Microbiol. 2010;142:151–159.
    doi: 10.1016/j.vetmic.2010.02.001pubmed: 20188498google scholar: lookup
  64. WHO. WHO Expert Consultation on Rabies: Third Report. WHO Technical Report Series 2018;1–183.
  65. Barecha C.B.G., Girzaw F., Kandi V., Pal M.. Epidemiology and Public Health Significance of Rabies. Perspect. Med. Res. 2017;5:55–67.
  66. Green S.L.. Equine rabies. Vet. Clin. N. Am. Equine Pract. 1993;9:337–347.
    doi: 10.1016/S0749-0739(17)30400-5pubmed: 8358647google scholar: lookup
  67. Sato G., Itou T., Shoji Y., Miura Y., Mikami T., Ito M., Kurane I., Samara S.I., Carvalho A.A., Nociti D.P.. Genetic and phylogenetic analysis of glycoprotein of rabies virus isolated from several species in Brazil. J. Vet. Med. Sci. 2004;66:747–753.
    doi: 10.1292/jvms.66.747pubmed: 15297743google scholar: lookup
  68. Dyer J.L., Yager P., Orciari L., Greenberg L., Wallace R., Hanlon C.A., Blanton J.D.. Rabies surveillance in the United States during 2013. J. Am. Vet. Med. Assoc. 2014;245:1111–1123.
    doi: 10.2460/javma.245.10.1111pmc: PMC5120391pubmed: 25356711google scholar: lookup
  69. Ali Y., Intisar S., Wegdan H., Ali E.. Epidemiology of Rabies in Sudan. J. Anim. Vet. Adv. 2006;5:266–270.
  70. Weir D.L., Annand E.J., Reid P.A., Broder C.C.. Recent observations on Australian bat lyssavirus tropism and viral entry. Viruses 2014;6:909–926.
    doi: 10.3390/v6020909pmc: PMC3939488pubmed: 24556791google scholar: lookup
  71. WHO Rabies Bulletin Europe. [(accessed on 15 December 2019)];2010–2019 Available online: https://www.who-rabies-bulletin.org/
  72. Rech R., Barros C.. Neurologic Diseases in Horses. Vet. Clin. N. Am. Equine Pract. 2015;31:281–306.
    doi: 10.1016/j.cveq.2015.04.010pubmed: 26210953google scholar: lookup
  73. Kumar R., Patil R.D.. Cryptic etiopathological conditions of equine nervous system with special emphasis on viral diseases. Vet. World. 2017;10:1427–1438.
  74. Meyer E.E., Morris P.G., Elcock L.H., Weil J.. Hindlimb hyperesthesia associated with rabies in two horses. J. Am. Vet. Med. Assoc. 1986;188:629–632.
    pubmed: 3957776
  75. OIE. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2019, Chapter 3.1.17. OIE 2019;1–35.
  76. Appolinario C., Allendorf S.D., Vicente A.F., Ribeiro B.D., Fonseca C.R., Antunes J.M., Peres M.G., Kotait I., Carrieri M.L., Megid J.. Fluorescent antibody test, quantitative polymerase chain reaction pattern and clinical aspects of rabies virus strains isolated from main reservoirs in Brazil. Braz. J. Infect. Dis. 2015;19:479–485.
    doi: 10.1016/j.bjid.2015.06.012pmc: PMC9427647pubmed: 26303004google scholar: lookup
  77. Muller F.T., Freuling C.M.. Rabies control in Europe: An overview of past, current and future strategies. Rev. Sci. Tech. 2018;37:409–419.
    doi: 10.20506/rst.37.2.2811pubmed: 30747138google scholar: lookup
  78. Harvey A.M., Watson J.L., Brault S.A., Edman J.M., Moore S.M., Kass P.H., Wilson W.D.. Duration of serum antibody response to rabies vaccination in horses. J. Am. Vet. Med. Assoc. 2016;249:411–418.
    doi: 10.2460/javma.249.4.411pubmed: 27479286google scholar: lookup
  79. De la Torre J.C.. Molecular biology of borna disease virus: Prototype of a new group of animal viruses. J. Virol. 1994;68:7669–7675.
    pmc: PMC237226pubmed: 7966555
  80. Kuhn J.H., Durrwald R., Bao Y., Briese T., Carbone K., Clawson A.N., deRisi J.L., Garten W., Jahrling P.B., Kolodziejek J.. Taxonomic reorganization of the family Bornaviridae. Arch. Virol. 2015;160:621–632.
    doi: 10.1007/s00705-014-2276-zpmc: PMC4315759pubmed: 25449305google scholar: lookup
  81. Honkavuori K.S., Shivaprasad H.L., Williams B.L., Quan P.L., Hornig M., Street C., Palacios G., Hutchison S.K., Franca M., Egholm M.. Novel borna virus in psittacine birds with proventricular dilatation disease. Emerg. Infect. Dis. 2008;14:1883–1886.
    doi: 10.3201/eid1412.080984pmc: PMC2634650pubmed: 19046511google scholar: lookup
  82. Hoffmann B., Tappe D., Hoper D., Herden C., Boldt A., Mawrin C., Niederstrasser O., Muller T., Jenckel M., van der Grinten E.. A Variegated Squirrel Bornavirus Associated with Fatal Human Encephalitis. N. Engl. J. Med. 2015;373:154–162.
    doi: 10.1056/NEJMoa1415627pubmed: 26154788google scholar: lookup
  83. Gonzalez-Dunia D., Cubitt B., de la Torre J.C.. Mechanism of Borna disease virus entry into cells. J. Virol. 1998;72:783–788.
    pmc: PMC109436pubmed: 9420287
  84. Rott R., Becht H.. Natural and experimental Borna disease in animals. Curr. Top. Microbiol. Immunol. 1995;190:17–30.
    doi: 10.1007/978-3-642-78618-1_2pubmed: 7789148google scholar: lookup
  85. Berg M., Johansson M., Montell H., Berg A.L.. Wild birds as a possible natural reservoir of Borna disease virus. Epidemiol. Infect. 2001;127:173–178.
    doi: 10.1017/S0950268801005702pmc: PMC2869725pubmed: 11561971google scholar: lookup
  86. Bode L., Durrwald R., Ludwig H.. Borna virus infections in cattle associated with fatal neurological disease. Vet. Rec. 1994;135:283–284.
    doi: 10.1136/vr.135.12.283pubmed: 7817508google scholar: lookup
  87. Hagiwara K., Tsuge Y., Asakawa M., Kabaya H., Okamoto M., Miyasho T., Taniyama H., Ishihara C., de la Torre J.C., Ikuta K.. Borna disease virus RNA detected in Japanese macaques (Macaca fuscata). Primates 2008;49:57–64.
    doi: 10.1007/s10329-007-0068-8pubmed: 17929110google scholar: lookup
  88. Hilbe M., Herrsche R., Kolodziejek J., Nowotny N., Zlinszky K., Ehrensperger F.. Shrews as reservoir hosts of borna disease virus. Emerg. Infect. Dis. 2006;12:675–677.
    doi: 10.3201/eid1204.051418pmc: PMC3294707pubmed: 16704819google scholar: lookup
  89. Kinnunen P.M., Billich C., Ek-Kommonen C., Henttonen H., Kallio R.K., Niemimaa J., Palva A., Staeheli P., Vaheri A., Vapalahti O.. Serological evidence for Borna disease virus infection in humans, wild rodents and other vertebrates in Finland. J. Clin. Virol. 2007;38:64–69.
    doi: 10.1016/j.jcv.2006.10.003pubmed: 17129759google scholar: lookup
  90. Lundgren A.L., Zimmermann W., Bode L., Czech G., Gosztonyi G., Lindberg R., Ludwig H.. Staggering disease in cats: Isolation and characterization of the feline Borna disease virus. J. Gen. Virol. 1995;76:2215–2222.
    doi: 10.1099/0022-1317-76-9-2215pubmed: 7561758google scholar: lookup
  91. Malkinson M., Weisman Y., Ashash E., Bode L., Ludwig H.. Borna disease in ostriches. Vet. Rec. 1993;133:304.
    doi: 10.1136/vr.133.12.304-bpubmed: 8204140google scholar: lookup
  92. Durrwald R., Kolodziejek J., Muluneh A., Herzog S., Nowotny N.. Epidemiological pattern of classical Borna disease and regional genetic clustering of Borna disease viruses point towards the existence of to-date unknown endemic reservoir host populations. Microbes Infect. 2006;8:917–929.
    doi: 10.1016/j.micinf.2005.08.013pubmed: 16469519google scholar: lookup
  93. Staeheli P., Sauder C., Hausmann J., Ehrensperger F., Schwemmle M.. Epidemiology of Borna disease virus. J. Gen. Virol. 2000;81:2123–2135.
    doi: 10.1099/0022-1317-81-9-2123pubmed: 10950968google scholar: lookup
  94. Weissenbock H., Bago Z., Kolodziejek J., Hager B., Palmetzhofer G., Durrwald R., Nowotny N.. Infections of horses and shrews with Bornaviruses in Upper Austria: A novel endemic area of Borna disease. Emerg. Microbes Infect. 2017;6:e52.
    doi: 10.1038/emi.2017.36pmc: PMC5520313pubmed: 28634359google scholar: lookup
  95. Bourg M., Herzog S., Encarnacao J.A., Nobach D., Lange-Herbst H., Eickmann M., Herden C.. Bicolored white-toothed shrews as reservoir for borna disease virus, Bavaria, Germany. Emerg. Infect. Dis. 2013;19:2064–2066.
    doi: 10.3201/eid1912.131076pmc: PMC3840852pubmed: 24274262google scholar: lookup
  96. Nobach D., Bourg M., Herzog S., Lange-Herbst H., Encarnacao J.A., Eickmann M., Herden C.. Shedding of Infectious Borna Disease Virus-1 in Living Bicolored White-Toothed Shrews. PLoS ONE 2015;10:e0137018.
  97. Ludwig H., Bode L., Gosztonyi G.. Borna disease: A persistent virus infection of the central nervous system. Prog. Med. Virol. 1988;35:107–151.
    pubmed: 3051132
  98. Herzog S., Pfeuffer I., Haberzettl K., Feldmann H., Frese K., Bechter K., Richt J.A.. Molecular characterization of Borna disease virus from naturally infected animals and possible links to human disorders. Arch. Virol. Suppl. 1997;13:183–190.
    pubmed: 9413537
  99. Hagiwara K., Kamitani W., Takamura S., Taniyama H., Nakaya T., Tanaka H., Kirisawa R., Iwai H., Ikuta K.. Detection of Borna disease virus in a pregnant mare and her fetus. Vet. Microbiol. 2000;72:207–216.
    doi: 10.1016/S0378-1135(99)00206-0pubmed: 10727831google scholar: lookup
  100. Okamoto M., Hagiwara K., Kamitani W., Sako T., Hirayama K., Kirisawa R., Tsuji M., Ishihara C., Iwai H., Kobayashi T.. Experimental vertical transmission of Borna disease virus in the mouse. Arch. Virol. 2003;148:1557–1568.
    doi: 10.1007/s00705-003-0120-ypubmed: 12898331google scholar: lookup
  101. Chalmers R.M., Thomas D.R., Salmon R.L.. Borna disease virus and the evidence for human pathogenicity: A systematic review. QJM 2005;98:255–274.
    doi: 10.1093/qjmed/hci039pubmed: 15760926google scholar: lookup
  102. Nakamura Y., Takahashi H., Shoya Y., Nakaya T., Watanabe M., Tomonaga K., Iwahashi K., Ameno K., Momiyama N., Taniyama H.. Isolation of Borna disease virus from human brain tissue. J. Virol. 2000;74:4601–4611.
  103. Brnic D., Stevanovic V., Cochet M., Agier C., Richardson J., Montero-Menei C.N., Milhavet O., Eloit M., Coulpier M.. Borna disease virus infects human neural progenitor cells and impairs neurogenesis. J. Virol. 2012;86:2512–2522.
    doi: 10.1128/JVI.05663-11pmc: PMC3302287pubmed: 22190725google scholar: lookup
  104. Scordel C., Huttin A., Cochet-Bernoin M., Szelechowski M., Poulet A., Richardson J., Benchoua A., Gonzalez-Dunia D., Eloit M., Coulpier M.. Borna disease virus phosphoprotein impairs the developmental program controlling neurogenesis and reduces human GABAergic neurogenesis. PLoS Pathog. 2015;11:e1004859.
  105. Schwemmle M., Jehle C., Formella S., Staeheli P.. Sequence similarities between human bornavirus isolates and laboratory strains question human origin. Lancet 1999;354:1973–1974.
    doi: 10.1016/S0140-6736(99)04703-0pubmed: 10622306google scholar: lookup
  106. Hornig M., Briese T., Licinio J., Khabbaz R.F., Altshuler L.L., Potkin S.G., Schwemmle M., Siemetzki U., Mintz J., Honkavuori K.. Absence of evidence for bornavirus infection in schizophrenia, bipolar disorder and major depressive disorder. Mol. Psychiatry 2012;17:486–493.
    doi: 10.1038/mp.2011.179pmc: PMC3622588pubmed: 22290118google scholar: lookup
  107. Korn K., Coras R., Bobinger T., Herzog S.M., Lucking H., Stohr R., Huttner H.B., Hartmann A., Ensser A.. Fatal Encephalitis Associated with Borna Disease Virus 1. N. Engl. J. Med. 2018;379:1375–1377.
    doi: 10.1056/NEJMc1800724pubmed: 30281979google scholar: lookup
  108. Schlottau K., Forth L., Angstwurm K., Hoper D., Zecher D., Liesche F., Hoffmann B., Kegel V., Seehofer D., Platen S.. Fatal Encephalitic Borna Disease Virus 1 in Solid-Organ Transplant Recipients. N. Engl. J. Med. 2018;379:1377–1379.
    doi: 10.1056/NEJMc1803115pubmed: 30281984google scholar: lookup
  109. Richt J.A., Grabner A., Herzog S.. Borna disease in horses. Vet. Clin. N. Am. Equine Pract. 2000;16:579–595.
    doi: 10.1016/S0749-0739(17)30097-4pubmed: 11219351google scholar: lookup
  110. Ludwig H., Bode L.. Borna disease virus: New aspects on infection, disease, diagnosis and epidemiology. Rev. Sci. Tech. 2000;19:259–288.
    doi: 10.20506/rst.19.1.1217pubmed: 11189720google scholar: lookup
  111. Beck C., Jimenez-Clavero M.A., Leblond A., Durand B., Nowotny N., Leparc-Goffart I., Zientara S., Jourdain E., Lecollinet S.. Flaviviruses in Europe: Complex circulation patterns and their consequences for the diagnosis and control of West Nile disease. Int. J. Environ. Res. Public Health 2013;10:6049–6083.
    doi: 10.3390/ijerph10116049pmc: PMC3863887pubmed: 24225644google scholar: lookup
  112. Melian E.B., Hinzman E., Nagasaki T., Firth A.E., Wills N.M., Nouwens A.S., Blitvich B.J., Leung J., Funk A., Atkins J.F.. NS1’ of flaviviruses in the Japanese encephalitis virus serogroup is a product of ribosomal frameshifting and plays a role in viral neuroinvasiveness. J. Virol. 2010;84:1641–1647.
    doi: 10.1128/JVI.01979-09pmc: PMC2812330pubmed: 19906906google scholar: lookup
  113. Pradier S., Lecollinet S., Leblond A.. West Nile virus epidemiology and factors triggering change in its distribution in Europe. Rev. Sci. Tech. 2012;31:829–844.
    doi: 10.20506/rst.31.3.2167pubmed: 23520737google scholar: lookup
  114. Gardner I.A., Wong S.J., Ferraro G.L., Balasuriya U.B., Hullinger P.J., Wilson W.D., Shi P.Y., MacLachlan N.J.. Incidence and effects of West Nile virus infection in vaccinated and unvaccinated horses in California. Vet. Res. 2007;38:109–116.
    doi: 10.1051/vetres:2006045pubmed: 17274156google scholar: lookup
  115. Zeller H.G., Schuffenecker I.. West Nile virus: An overview of its spread in Europe and the Mediterranean basin in contrast to its spread in the Americas. Eur. J. Clin. Microbiol. Infect. Dis. 2004;23:147–156.
    doi: 10.1007/s10096-003-1085-1pubmed: 14986160google scholar: lookup
  116. Autorino G.L., Battisti A., Deubel V., Ferrari G., Forletta R., Giovannini A., Lelli R., Murri S., Scicluna M.T.. West Nile virus epidemic in horses, Tuscany region, Italy. Emerg. Infect. Dis. 2002;8:1372–1378.
    doi: 10.3201/eid0812.020234pmc: PMC2738505pubmed: 12498650google scholar: lookup
  117. Ceianu C.S., Ungureanu A., Nicolescu G., Cernescu C., Nitescu L., Tardei G., Petrescu A., Pitigoi D., Martin D., Ciulacu-Purcarea V.. West nile virus surveillance in Romania: 1997–2000. Viral Immunol. 2001;14:251–262.
    doi: 10.1089/088282401753266765pubmed: 11572635google scholar: lookup
  118. Murgue B., Murri S., Triki H., Deubel V., Zeller H.G.. West Nile in the Mediterranean basin: 1950–2000. Ann. N. Y. Acad. Sci. 2001;951:117–126.
  119. Chancey C., Grinev A., Volkova E., Rios M.. The global ecology and epidemiology of West Nile virus. BioMed Res. Int. 2015;2015:376230.
    doi: 10.1155/2015/376230pmc: PMC4383390pubmed: 25866777google scholar: lookup
  120. Bakonyi T., Hubalek Z., Rudolf I., Nowotny N.. Novel flavivirus or new lineage of West Nile virus, central Europe. Emerg. Infect. Dis. 2005;11:225–231.
    doi: 10.3201/eid1102.041028pmc: PMC3320449pubmed: 15752439google scholar: lookup
  121. Hernandez-Triana L.M., Jeffries C.L., Mansfield K.L., Carnell G., Fooks A.R., Johnson N.. Emergence of west nile virus lineage 2 in europe: A review on the introduction and spread of a mosquito-borne disease. Front. Public Health 2014;2:271.
    doi: 10.3389/fpubh.2014.00271pmc: PMC4258884pubmed: 25538937google scholar: lookup
  122. Michel F., Sieg M., Fischer D., Keller M., Eiden M., Reuschel M., Schmidt V., Schwehn R., Rinder M., Urbaniak S.. Evidence for West Nile Virus and Usutu Virus Infections in Wild and Resident Birds in Germany, 2017 and 2018. Viruses 2019;11:674.
    doi: 10.3390/v11070674pmc: PMC6669720pubmed: 31340516google scholar: lookup
  123. Van den Hurk A.F., Hall-Mendelin S., Webb C.E., Tan C.S., Frentiu F.D., Prow N.A., Hall R.A.. Role of enhanced vector transmission of a new West Nile virus strain in an outbreak of equine disease in Australia in 2011. Parasites Vectors 2014;7:586.
    doi: 10.1186/s13071-014-0586-3pmc: PMC4280035pubmed: 25499981google scholar: lookup
  124. Kaiser J.A., Wang T., Barrett A.D.. Virulence determinants of West Nile virus: How can these be used for vaccine design?. Future Virol. 2017;12:283–295.
    doi: 10.2217/fvl-2016-0141pmc: PMC5592643pubmed: 28919920google scholar: lookup
  125. Langevin S.A., Bowen R.A., Reisen W.K., Andrade C.C., Ramey W.N., Maharaj P.D., Anishchenko M., Kenney J.L., Duggal N.K., Romo H.. Host competence and helicase activity differences exhibited by West Nile viral variants expressing NS3-249 amino acid polymorphisms. PLoS ONE 2014;9:e100802.
  126. Brault A.C., Huang C.Y., Langevin S.A., Kinney R.M., Bowen R.A., Ramey W.N., Panella N.A., Holmes E.C., Powers A.M., Miller B.R.. A single positively selected West Nile viral mutation confers increased virogenesis in American crows. Nat. Genet. 2007;39:1162–1166.
    doi: 10.1038/ng2097pmc: PMC2291521pubmed: 17694056google scholar: lookup
  127. Dridi M., Van Den Berg T., Lecollinet S., Lambrecht B.. Evaluation of the pathogenicity of West Nile virus (WNV) lineage 2 strains in a SPF chicken model of infection: NS3-249Pro mutation is neither sufficient nor necessary for conferring virulence. Vet. Res. 2015;46:130.
    doi: 10.1186/s13567-015-0257-1pmc: PMC4628354pubmed: 26518144google scholar: lookup
  128. Randolph S.E., Gern L., Nuttall P.A.. Co-feeding ticks: Epidemiological significance for tick-borne pathogen transmission. Parasitol. Today 1996;12:472–479.
    doi: 10.1016/S0169-4758(96)10072-7pubmed: 15275266google scholar: lookup
  129. Labuda M., Jones L.D., Williams T., Nuttall P.A.. Enhancement of tick-borne encephalitis virus transmission by tick salivary gland extracts. Med. Vet. Entomol. 1993;7:193–196.
  130. Holzmann H., Aberle S.W., Stiasny K., Werner P., Mischak A., Zainer B., Netzer M., Koppi S., Bechter E., Heinz F.X.. Tick-borne encephalitis from eating goat cheese in a mountain region of Austria. Emerg. Infect. Dis. 2009;15:1671–1673.
    doi: 10.3201/eid1510.090743pmc: PMC2866415pubmed: 19861072google scholar: lookup
  131. Jones L.D., Gaunt M., Hails R.S., Laurenson K., Hudson P.J., Reid H., Henbest P., Gould E.A.. Transmission of louping ill virus between infected and uninfected ticks co-feeding on mountain hares. Med. Vet. Entomol. 1997;11:172–176.
  132. Jeffries C.L., Mansfield K.L., Phipps L.P., Wakeley P.R., Mearns R., Schock A., Bell S., Breed A.C., Fooks A.R., Johnson N.. Louping ill virus: An endemic tick-borne disease of Great Britain. J. Gen. Virol. 2014;95:1005–1014.
    doi: 10.1099/vir.0.062356-0pmc: PMC4811648pubmed: 24552787google scholar: lookup
  133. Timoney P.J., Donnelly W.J., Clements L.O., Fenlon M.. Encephalitis caused by louping ill virus in a group of horses in Ireland. Equine Vet. J. 1976;8:113–117.
  134. Klaus C., Horugel U., Hoffmann B., Beer M.. Tick-borne encephalitis virus (TBEV) infection in horses: Clinical and laboratory findings and epidemiological investigations. Vet. Microbiol. 2013;163:368–372.
    doi: 10.1016/j.vetmic.2012.12.041pubmed: 23395291google scholar: lookup
  135. Waldvogel A., Matile H., Wegmann C., Wyler R., Kunz C.. Tick-borne encephalitis in the horse. Schweiz. Arch. Tierheilkd. 1981;123:227–233.
    pubmed: 7256233
  136. Rushton J.O., Lecollinet S., Hubalek Z., Svobodova P., Lussy H., Nowotny N.. Tick-borne encephalitis virus in horses, Austria, 2011. Emerg. Infect. Dis. 2013;19:635–637.
    doi: 10.3201/eid1904.121450pmc: PMC3647421pubmed: 23631894google scholar: lookup
  137. Csank T., Drzewniokova P., Korytar L., Major P., Gyuranecz M., Pistl J., Bakonyi T.. A Serosurvey of Flavivirus Infection in Horses and Birds in Slovakia. Vector Borne Zoonotic Dis. 2018;18:206–213.
    doi: 10.1089/vbz.2017.2216pubmed: 29437548google scholar: lookup
  138. Suss J.. Tick-borne encephalitis 2010: Epidemiology, risk areas, and virus strains in Europe and Asia-An overview. Ticks Tick-Borne Dis. 2011;2:2–15.
    doi: 10.1016/j.ttbdis.2010.10.007pubmed: 21771531google scholar: lookup
  139. Jaaskelainen A.E., Sironen T., Murueva G.B., Subbotina N., Alekseev A.N., Castren J., Alitalo I., Vaheri A., Vapalahti O.. Tick-borne encephalitis virus in ticks in Finland, Russian Karelia and Buryatia. J. Gen. Virol. 2010;91:2706–2712.
    doi: 10.1099/vir.0.023663-0pubmed: 20660147google scholar: lookup
  140. Balseiro A., Royo L.J., Martinez C.P., Fernandez de Mera I.G., Hofle U., Polledo L., Marreros N., Casais R., Marin J.F.. Louping ill in goats, Spain, 2011. Emerg. Infect. Dis. 2012;18:976–978.
    doi: 10.3201/eid1806.120220pmc: PMC3358175pubmed: 22607689google scholar: lookup
  141. Ytrehus B., Vainio K., Dudman S.G., Gilray J., Willoughby K.. Tick-borne encephalitis virus and louping-ill virus may co-circulate in Southern Norway. Vector Borne Zoonotic Dis. (Larchmt. N.Y.) 2013;13:762–768.
    doi: 10.1089/vbz.2012.1023pubmed: 23808981google scholar: lookup
  142. Mustafa Y.M., Meuren L.M., Coelho S.V.A., de Arruda L.B.. Pathways Exploited by Flaviviruses to Counteract the Blood-Brain Barrier and Invade the Central Nervous System. Front. Microbiol. 2019;10:525.
    doi: 10.3389/fmicb.2019.00525pmc: PMC6447710pubmed: 30984122google scholar: lookup
  143. Verma S., Lo Y., Chapagain M., Lum S., Kumar M., Gurjav U., Luo H., Nakatsuka A., Nerurkar V.R.. West Nile virus infection modulates human brain microvascular endothelial cells tight junction proteins and cell adhesion molecules: Transmigration across the in vitro blood-brain barrier. Virology 2009;385:425–433.
    doi: 10.1016/j.virol.2008.11.047pmc: PMC2684466pubmed: 19135695google scholar: lookup
  144. Wang P., Dai J., Bai F., Kong K.F., Wong S.J., Montgomery R.R., Madri J.A., Fikrig E.. Matrix metalloproteinase 9 facilitates West Nile virus entry into the brain. J. Virol. 2008;82:8978–8985.
    doi: 10.1128/JVI.00314-08pmc: PMC2546894pubmed: 18632868google scholar: lookup
  145. Palus M., Vancova M., Sirmarova J., Elsterova J., Perner J., Ruzek D.. Tick-borne encephalitis virus infects human brain microvascular endothelial cells without compromising blood-brain barrier integrity. Virology 2017;507:110–122.
    doi: 10.1016/j.virol.2017.04.012pubmed: 28432926google scholar: lookup
  146. Cho H., Diamond M.S.. Immune responses to West Nile virus infection in the central nervous system. Viruses 2012;4:3812–3830.
    doi: 10.3390/v4123812pmc: PMC3528292pubmed: 23247502google scholar: lookup
  147. Samuel M.A., Wang H., Siddharthan V., Morrey J.D., Diamond M.S.. Axonal transport mediates West Nile virus entry into the central nervous system and induces acute flaccid paralysis. Proc. Natl. Acad. Sci. USA 2007;104:17140–17145.
    doi: 10.1073/pnas.0705837104pmc: PMC2040476pubmed: 17939996google scholar: lookup
  148. Xiao S.Y., Guzman H., Zhang H., Travassos da Rosa A.P., Tesh R.B.. West Nile virus infection in the golden hamster (Mesocricetus auratus): A model for West Nile encephalitis. Emerg. Infect. Dis. 2001;7:714–721.
    doi: 10.3201/eid0704.017420pmc: PMC2631753pubmed: 11585537google scholar: lookup
  149. Potokar M., Jorgacevski J., Zorec R.. Astrocytes in Flavivirus Infections. Int. J. Mol. Sci. 2019;20:691.
    doi: 10.3390/ijms20030691pmc: PMC6386967pubmed: 30736273google scholar: lookup
  150. Palus M., Bily T., Elsterova J., Langhansova H., Salat J., Vancova M., Ruzek D.. Infection and injury of human astrocytes by tick-borne encephalitis virus. J. Gen. Virol. 2014;95:2411–2426.
    doi: 10.1099/vir.0.068411-0pubmed: 25000960google scholar: lookup
  151. Donadieu E., Lowenski S., Servely J.L., Laloy E., Lilin T., Nowotny N., Richardson J., Zientara S., Lecollinet S., Coulpier M.. Comparison of the neuropathology induced by two West Nile virus strains. PLoS ONE 2013;8:e84473.
  152. Hyde J., Nettleton P., Marriott L., Willoughby K.. Louping ill in horses. Vet. Rec. 2007;160:532.
    doi: 10.1136/vr.160.15.532pubmed: 17435106google scholar: lookup
  153. Beck C., Lowenski S., Durand B., Bahuon C., Zientara S., Lecollinet S.. Improved reliability of serological tools for the diagnosis of West Nile fever in horses within Europe. PLoS Negl. Trop. Dis. 2017;11:e0005936.
  154. Chaskopoulou A., L’Ambert G., Petric D., Bellini R., Zgomba M., Groen T.A., Marrama L., Bicout D.J.. Ecology of West Nile virus across four European countries: Review of weather profiles, vector population dynamics and vector control response. Parasites Vectors 2016;9:482.
    doi: 10.1186/s13071-016-1736-6pmc: PMC5009705pubmed: 27590848google scholar: lookup
  155. Gossner C.M., Marrama L., Carson M., Allerberger F., Calistri P., Dilaveris D., Lecollinet S., Morgan D., Nowotny N., Paty M.C.. West Nile virus surveillance in Europe: Moving towards an integrated animal-human-vector approach. Euro Surveill. 2017;22.
  156. European Medicines Agency. [(accessed on 12 September 2019)];EPAR Product Information: Equip WNV 2015. Available online: http://www.ema.europa.eu/docs/en_GB/document_library/EPAR_-_Product_Information/veterinary/000137/WC500063683.pdf.
  157. Minke J.M., Siger L., Karaca K., Austgen L., Gordy P., Bowen R., Renshaw R.W., Loosmore S., Audonnet J.C., Nordgren B.. Recombinant canarypoxvirus vaccine carrying the prM/E genes of West Nile virus protects horses against a West Nile virus-mosquito challenge. Arch. Virol. Suppl. 2004;18:221–230.
    pubmed: 15119777
  158. El Garch H., Minke J.M., Rehder J., Richard S., Edlund Toulemonde C., Dinic S., Andreoni C., Audonnet J.C., Nordgren R., Juillard V.. A West Nile virus (WNV) recombinant canarypox virus vaccine elicits WNV-specific neutralizing antibodies and cell-mediated immune responses in the horse. Vet. Immunol. Immunopathol. 2008;123:230–239.
    doi: 10.1016/j.vetimm.2008.02.002pubmed: 18372050google scholar: lookup
  159. Guy B., Guirakhoo F., Barban V., Higgs S., Monath T.P., Lang J.. Preclinical and clinical development of YFV 17D-based chimeric vaccines against dengue, West Nile and Japanese encephalitis viruses. Vaccine 2010;28:632–649.
    doi: 10.1016/j.vaccine.2009.09.098pubmed: 19808029google scholar: lookup
  160. Durand B., Lecollinet S., Beck C., Martinez-Lopez B., Balenghien T., Chevalier V.. Identification of hotspots in the European union for the introduction of four zoonotic arboviroses by live animal trade. PLoS ONE 2013;8:e70000.
  161. Pfeffer M., Dobler G.. Emergence of zoonotic arboviruses by animal trade and migration. Parasites Vectors 2010;3:35.
    doi: 10.1186/1756-3305-3-35pmc: PMC2868497pubmed: 20377873google scholar: lookup
  162. Diaz A., Coffey L.L., Burkett-Cadena N., Day J.F.. Reemergence of St. Louis Encephalitis Virus in the Americas. Emerg. Infect. Dis. 2018;24.
    doi: 10.3201/eid2412.180372pmc: PMC6256408pubmed: 30457961google scholar: lookup
  163. Mansfield K.L., Hernandez-Triana L.M., Banyard A.C., Fooks A.R., Johnson N.. Japanese encephalitis virus infection, diagnosis and control in domestic animals. Vet. Microbiol. 2017;201:85–92.
    doi: 10.1016/j.vetmic.2017.01.014pubmed: 28284628google scholar: lookup
  164. Prow N.A., Tan C.S., Wang W., Hobson-Peters J., Kidd L., Barton A., Wright J., Hall R.A., Bielefeldt-Ohmann H.. Natural exposure of horses to mosquito-borne flaviviruses in south-east Queensland, Australia. Int. J. Environ. Res. Public Health 2013;10:4432–4443.
    doi: 10.3390/ijerph10094432pmc: PMC3799510pubmed: 24048209google scholar: lookup
  165. Morita K., Nabeshima T., Buerano C.C.. Japanese encephalitis. Rev. Sci. Tech. 2015;34:441–452.
    doi: 10.20506/rst.34.2.2370pubmed: 26601447google scholar: lookup
  166. Ravanini P., Huhtamo E., Ilaria V., Crobu M.G., Nicosia A.M., Servino L., Rivasi F., Allegrini S., Miglio U., Magri A.. Japanese encephalitis virus RNA detected in Culex pipiens mosquitoes in Italy. Euro Surveill. 2012;17.
    doi: 10.2807/ese.17.28.20221-enpubmed: 22835438google scholar: lookup
  167. Preziuso S., Mari S., Mariotti F., Rossi G.. Detection of Japanese Encephalitis Virus in bone marrow of healthy young wild birds collected in 1997-2000 in Central Italy. Zoonoses Public Health 2018;65:798–804.
    doi: 10.1111/zph.12501pubmed: 29974677google scholar: lookup
  168. Reisen W.K., Lothrop H.D., Wheeler S.S., Kennsington M., Gutierrez A., Fang Y., Garcia S., Lothrop B.. Persistent West Nile virus transmission and the apparent displacement St. Louis encephalitis virus in southeastern California, 2003–2006. J. Med. Entomol. 2008;45:494–508.
  169. Fang Y., Reisen W.K.. Previous infection with West Nile or St. Louis encephalitis viruses provides cross protection during reinfection in house finches. Am. J. Trop. Med. Hyg. 2006;75:480–485.
    doi: 10.4269/ajtmh.2006.75.480pubmed: 16968925google scholar: lookup
  170. Spinsanti L.I., Diaz L.A., Glatstein N., Arselan S., Morales M.A., Farias A.A., Fabbri C., Aguilar J.J., Re V., Frias M.. Human outbreak of St. Louis encephalitis detected in Argentina, 2005. J. Clin. Virol. 2008;42:27–33.
    doi: 10.1016/j.jcv.2007.11.022pubmed: 18249032google scholar: lookup
  171. Rico-Hesse R.. Venezuelan equine encephalomyelitis. Vet. Clin. N. Am. Equine Pract. 2000;16:553–563.
    doi: 10.1016/S0749-0739(17)30095-0pubmed: 11219349google scholar: lookup
  172. Bergren N.A., Auguste A.J., Forrester N.L., Negi S.S., Braun W.A., Weaver S.C.. Western equine encephalitis virus: Evolutionary analysis of a declining alphavirus based on complete genome sequences. J. Virol. 2014;88:9260–9267.
    doi: 10.1128/JVI.01463-14pmc: PMC4136285pubmed: 24899192google scholar: lookup
  173. Brault A.C., Powers A.M., Holmes E.C., Woelk C.H., Weaver S.C.. Positively charged amino acid substitutions in the e2 envelope glycoprotein are associated with the emergence of venezuelan equine encephalitis virus. J. Virol. 2002;76:1718–1730.
  174. Arechiga-Ceballos N., Aguilar-Setien A.. Alphaviral equine encephalomyelitis (Eastern, Western and Venezuelan). Rev. Sci. Tech. 2015;34:491–501.
    doi: 10.20506/rst.34.2.2374pubmed: 26601451google scholar: lookup
  175. Deardorff E.R., Forrester N.L., Travassos-da-Rosa A.P., Estrada-Franco J.G., Navarro-Lopez R., Tesh R.B., Weaver S.C.. Experimental infection of potential reservoir hosts with Venezuelan equine encephalitis virus, Mexico. Emerg. Infect. Dis. 2009;15:519–525.
    doi: 10.3201/eid1504.081008pmc: PMC2671456pubmed: 19331726google scholar: lookup
  176. Aguilar P.V., Paessler S., Carrara A.S., Baron S., Poast J., Wang E., Moncayo A.C., Anishchenko M., Watts D., Tesh R.B.. Variation in interferon sensitivity and induction among strains of eastern equine encephalitis virus. J. Virol. 2005;79:11300–11310.
  177. Weaver S.C., Powers A.M., Brault A.C., Barrett A.D.. Molecular epidemiological studies of veterinary arboviral encephalitides. Vet. J. 1999;157:123–138.
    doi: 10.1053/tvjl.1998.0289pubmed: 10204408google scholar: lookup
  178. Zientara S., Weyer C.T., Lecollinet S.. African horse sickness. Rev. Sci. Tech. 2015;34:315–327.
    doi: 10.20506/rst.34.2.2359pubmed: 26601437google scholar: lookup
  179. Wilson A., Mellor P.. Bluetongue in Europe: Vectors, epidemiology and climate change. Parasitol. Res. 2008;103:S69–S77.
    doi: 10.1007/s00436-008-1053-xpubmed: 19030888google scholar: lookup
  180. Aharonson-Raz K., Steinman A., Bumbarov V., Maan S., Maan N.S., Nomikou K., Batten C., Potgieter C., Gottlieb Y., Mertens P.. Isolation and phylogenetic grouping of equine encephalosis virus in Israel. Emerg. Infect. Dis. 2011;17:1883–1886.
    doi: 10.3201/eid1710.110350pmc: PMC3310674pubmed: 22000361google scholar: lookup
  181. Reed S.M., Toribio R.E.. Equine herpesvirus 1 and 4. Vet. Clin. N. Am. Equine Pract. 2004;20:631–642.
    doi: 10.1016/j.cveq.2004.09.001pubmed: 15519823google scholar: lookup
  182. Slater J.D., Borchers K., Thackray A.M., Field H.J.. The trigeminal ganglion is a location for equine herpesvirus 1 latency and reactivation in the horse. J. Gen. Virol. 1994;75:2007–2016.
    doi: 10.1099/0022-1317-75-8-2007pubmed: 8046404google scholar: lookup
  183. Roehrig J.T.. West nile virus in the United States—A historical perspective. Viruses 2013;5:3088–3108.
    doi: 10.3390/v5123088pmc: PMC3967162pubmed: 24335779google scholar: lookup
  184. Beck C., Despres P., Paulous S., Vanhomwegen J., Lowenski S., Nowotny N., Durand B., Garnier A., Blaise-Boisseau S., Guitton E.. A High-Performance Multiplex Immunoassay for Serodiagnosis of Flavivirus-Associated Neurological Diseases in Horses. BioMed Res. Int. 2015;2015:678084.
    doi: 10.1155/2015/678084pmc: PMC4589573pubmed: 26457301google scholar: lookup
  185. Cleton N.B., van Maanen K., Bergervoet S.A., Bon N., Beck C., Godeke G.J., Lecollinet S., Bowen R., Lelli D., Nowotny N.. A Serological Protein Microarray for Detection of Multiple Cross-Reactive Flavivirus Infections in Horses for Veterinary and Public Health Surveillance. Transbound. Emerg. Dis. 2017;64:1801–1812.
    doi: 10.1111/tbed.12569pubmed: 27633257google scholar: lookup
  186. Van Eeden C., Williams J.H., Gerdes T.G., van Wilpe E., Viljoen A., Swanepoel R., Venter M.. Shuni virus as cause of neurologic disease in horses. Emerg. Infect. Dis. 2012;18:318–321.
    doi: 10.3201/eid1802.111403pmc: PMC3310469pubmed: 22305525google scholar: lookup
  187. Altan E., Li Y., Sabino-Santos G. Jr., Sawaswong V., Barnum S., Pusterla N., Deng X., Delwart E.. Viruses in Horses with Neurologic and Respiratory Diseases. Viruses 2019;11:942.
    doi: 10.3390/v11100942pmc: PMC6832430pubmed: 31614994google scholar: lookup
  188. Cohen M.L.. Changing patterns of infectious disease. Nature 2000;406:762–767.
    doi: 10.1038/35021206pubmed: 10963605google scholar: lookup
  189. Martinet J.P., Ferte H., Failloux A.B., Schaffner F., Depaquit J.. Mosquitoes of North-Western Europe as Potential Vectors of Arboviruses: A Review. Viruses 2019;11:1059.
    doi: 10.3390/v11111059pmc: PMC6893686pubmed: 31739553google scholar: lookup
  190. Cunze S., Koch L.K., Kochmann J., Klimpel S.. Aedes albopictus and Aedes japonicus—Two invasive mosquito species with different temperature niches in Europe. Parasites Vectors 2016;9:573.
    doi: 10.1186/s13071-016-1853-2pmc: PMC5097377pubmed: 27814747google scholar: lookup
  191. Vogels C.B., Goertz G.P., Pijlman G.P., Koenraadt C.J.. Vector competence of European mosquitoes for West Nile virus. Emerg. Microbes Infect. 2017;6:e96.
    doi: 10.1038/emi.2017.82pmc: PMC5717085pubmed: 29116220google scholar: lookup
  192. De Wispelaere M., Despres P., Choumet V.. European Aedes albopictus and Culex pipiens Are Competent Vectors for Japanese Encephalitis Virus. PLoS Negl. Trop. Dis. 2017;11:e0005294.
  193. Huber K., Jansen S., Leggewie M., Badusche M., Schmidt-Chanasit J., Becker N., Tannich E., Becker S.C.. Aedes japonicus japonicus (Diptera: Culicidae) from Germany have vector competence for Japan encephalitis virus but are refractory to infection with West Nile virus. Parasitol. Res. 2014;113:3195–3199.
    doi: 10.1007/s00436-014-3983-9pubmed: 24948103google scholar: lookup

Citations

This article has been cited 30 times.