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Viruses2023; 15(5); 1108; doi: 10.3390/v15051108

Horses as Sentinels for the Circulation of Flaviviruses in Eastern-Central Germany.

Abstract: Since 2018, autochthonous West Nile virus (WNV) infections have been regularly reported in eastern-central Germany. While clinically apparent infections in humans and horses are not frequent, seroprevalence studies in horses may allow the tracing of WNV and related flaviviruses transmission, such as tick-borne encephalitis virus (TBEV) and Usutu virus (USUV), and consequently help to estimate the risk of human infections. Hence, the aim of our study was to follow the seropositive ratio against these three viruses in horses in Saxony, Saxony Anhalt, and Brandenburg and to describe their geographic distribution for the year 2021. In early 2022, i.e., before the virus transmission season, sera from 1232 unvaccinated horses were tested using a competitive pan-flavivirus ELISA (cELISA). In order to estimate the true seropositive ratio of infection with WNV, TBEV, and USUV for 2021, positive and equivocal results were confirmed by a virus neutralization test (VNT). In addition, possible risk factors for seropositivity using questionnaires were analyzed using logistic regression based on questionnaires similar to our previous study from 2020. In total, 125 horse sera reacted positive in the cELISA. Based on the VNT, 40 sera showed neutralizing antibodies against WNV, 69 against TBEV, and 5 against USUV. Three sera showed antibodies against more than one virus, and eight were negative based on the VNT. The overall seropositive ratio was 3.3% (95% CI: 2.38-4.40) for WNV, 5.6% (95% CI: 4.44-7.04) for TBEV, and 0.4% (95% CI: 0.14-0.98) for USUV infections. While age and number of horses on the holding were factors predicting TBEV seropositivity, no risk factors were discovered for WNV seropositivity. We conclude that horses are useful sentinels to determine the flavivirus circulation in eastern-central Germany, as long as they are not vaccinated against WNV.
Publication Date: 2023-04-30 PubMed ID: 37243194PubMed Central: PMC10222594DOI: 10.3390/v15051108Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • Non-U.S. Gov't

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 article discusses a study conducted in Germany that uses horses as a means of tracking the circulation of Flaviviruses, specifically West Nile Virus (WNV), Tick-Borne Encephalitis Virus (TBEV), and Usutu Virus (USUV). The study analyzes if the presence of these viruses can be traced through horse’s antibodies.

Research Methodology

  • This research study was carried out in eastern-central Germany, with specific focus on Saxony, Saxony Anhalt, and Brandenburg.
  • The researchers conducted seroprevalence studies on horses, testing their blood samples for antibodies against WNV, TBEV, and USUV.
  • A total of 1232 unvaccinated horse sera were tested using a method known as competitive pan-flavivirus Enzyme-Linked Immunosorbent Assay (cELISA) in early 2022, before the virus transmission season.
  • To validate the cELISA results and estimate the true positive ratio of infection with the three types of viruses, virus neutralization test (VNT) was conducted on samples that tested positive or showed equivocal results.
  • The study also investigated possible risk factors for seropositivity using questionnaires. The results were analyzed using logistic regression.

Research Findings

  • The research found that 125 horse sera out of the 1232 tested reacted positively in the cELISA.
  • Based on the VNT, 40 sera showed neutralizing antibodies against WNV, 69 against TBEV, and 5 against USUV. Three sera showed antibodies against more than one virus, and eight were negative based on the VNT.
  • The overall seropositive ratio was 3.3% for WNV, 5.6% for TBEV, and 0.4% for USUV infections.
  • Regarding risk factors, age and the number of horses in the holding were factors predicting TBEV seropositivity, while no risk factors were discovered for WNV seropositivity.

Conclusion

  • From these findings, the research concluded that horses can serve as useful indicators or “sentinels” to determine the circulation of Flaviviruses in the region of eastern-central Germany, as long as they are not vaccinated against WNV.
  • This research provides valuable insight and understanding of the prevalent circulation and distribution of these viruses, which is particularly important for estimating the risk of human infections.

Cite This Article

APA
Gothe LMR, Ganzenberg S, Ziegler U, Obiegala A, Lohmann KL, Sieg M, Vahlenkamp TW, Groschup MH, Hörügel U, Pfeffer M. (2023). Horses as Sentinels for the Circulation of Flaviviruses in Eastern-Central Germany. Viruses, 15(5), 1108. https://doi.org/10.3390/v15051108

Publication

ISSN: 1999-4915
NlmUniqueID: 101509722
Country: Switzerland
Language: English
Volume: 15
Issue: 5
PII: 1108

Researcher Affiliations

Gothe, Leonard M R
  • Institute of Animal Hygiene and Veterinary Public Health, Faculty of Veterinary Medicine, Leipzig University, 04103 Leipzig, Germany.
Ganzenberg, Stefanie
  • Department for Horses, Faculty of Veterinary Medicine, Leipzig University, 04103 Leipzig, Germany.
Ziegler, Ute
  • Friedrich-Loeffler Institut (FLI), Federal Research Institute for Animal Health, Institute of Novel and Emerging Infectious Diseases, 17493 Greifswald-Insel Riems, Germany.
Obiegala, Anna
  • Institute of Animal Hygiene and Veterinary Public Health, Faculty of Veterinary Medicine, Leipzig University, 04103 Leipzig, Germany.
Lohmann, Katharina L
  • Department for Horses, Faculty of Veterinary Medicine, Leipzig University, 04103 Leipzig, Germany.
Sieg, Michael
  • Institute of Virology, Faculty of Veterinary Medicine, Leipzig University, 04103 Leipzig, Germany.
Vahlenkamp, Thomas W
  • Institute of Virology, Faculty of Veterinary Medicine, Leipzig University, 04103 Leipzig, Germany.
Groschup, Martin H
  • Friedrich-Loeffler Institut (FLI), Federal Research Institute for Animal Health, Institute of Novel and Emerging Infectious Diseases, 17493 Greifswald-Insel Riems, Germany.
Hörügel, Uwe
  • Animal Diseases Fund Saxony, Horse Health Service, 01099 Dresden, Germany.
Pfeffer, Martin
  • Institute of Animal Hygiene and Veterinary Public Health, Faculty of Veterinary Medicine, Leipzig University, 04103 Leipzig, Germany.

MeSH Terms

  • Horses
  • Animals
  • Humans
  • West Nile virus
  • Seroepidemiologic Studies
  • Horse Diseases / epidemiology
  • Antibodies, Viral
  • Flavivirus
  • West Nile Fever / epidemiology
  • West Nile Fever / veterinary
  • Encephalitis Viruses, Tick-Borne
  • Flavivirus Infections / epidemiology
  • Flavivirus Infections / veterinary

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 98 references
  1. Deubel V, Fiette L, Gounon P, Drouet MT, Khun H, Huerre M, Banet C, Malkinson M, Desprès P. Variations in biological features of West Nile viruses.. Ann N Y Acad Sci 2001 Dec;951:195-206.
  2. Castle E, Wengler G. Nucleotide sequence of the 5'-terminal untranslated part of the genome of the flavivirus West Nile virus.. Arch Virol 1987;92(3-4):309-13.
    doi: 10.1007/BF01317487pubmed: 3813889google scholar: lookup
  3. Füzik T, Formanová P, Růžek D, Yoshii K, Niedrig M, Plevka P. Structure of tick-borne encephalitis virus and its neutralization by a monoclonal antibody.. Nat Commun 2018 Jan 30;9(1):436.
    doi: 10.1038/s41467-018-02882-0pmc: PMC5789857pubmed: 29382836google scholar: lookup
  4. Bakonyi T, Gould EA, Kolodziejek J, Weissenböck H, Nowotny N. Complete genome analysis and molecular characterization of Usutu virus that emerged in Austria in 2001: comparison with the South African strain SAAR-1776 and other flaviviruses.. Virology 2004 Oct 25;328(2):301-10.
    doi: 10.1016/j.virol.2004.08.005pubmed: 15464850google scholar: lookup
  5. Smithburn KC, Hughes TP, Burke AW, Paul JH. A Neurotropic Virus Isolated from the Blood of a Native of Uganda. Am. J. Trop. Med. Hyg. 1940;20:471–492.
  6. 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
  7. Pachler K, Lebl K, Berer D, Rudolf I, Hubalek Z, Nowotny N. Putative new West Nile virus lineage in Uranotaenia unguiculata mosquitoes, Austria, 2013.. Emerg Infect Dis 2014 Dec;20(12):2119-22.
    doi: 10.3201/eid2012.140921pmc: PMC4257835pubmed: 25418009google scholar: lookup
  8. Fall G, Di Paola N, Faye M, Dia M, Freire CCM, Loucoubar C, Zanotto PMA, Faye O, Sall AA. Biological and phylogenetic characteristics of West African lineages of West Nile virus.. PLoS Negl Trop Dis 2017 Nov;11(11):e0006078.
  9. van der Meulen KM, Pensaert MB, Nauwynck HJ. West Nile virus in the vertebrate world.. Arch Virol 2005 Apr;150(4):637-57.
    doi: 10.1007/s00705-004-0463-zpubmed: 15662484google scholar: lookup
  10. Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, Davis B, Bowen R, Bunning M. Experimental infection of North American birds with the New York 1999 strain of West Nile virus.. Emerg Infect Dis 2003 Mar;9(3):311-22.
    doi: 10.3201/eid0903.020628pmc: PMC2958552pubmed: 12643825google scholar: lookup
  11. Kilpatrick AM, Kramer LD, Campbell SR, Alleyne EO, Dobson AP, Daszak P. West Nile virus risk assessment and the bridge vector paradigm.. Emerg Infect Dis 2005 Mar;11(3):425-9.
    doi: 10.3201/eid1103.040364pmc: PMC3298247pubmed: 15757558google scholar: lookup
  12. Savage HM, Ceianu C, Nicolescu G, Karabatsos N, Lanciotti R, Vladimirescu A, Laiv L, Ungureanu A, Romanca C, Tsai TF. Entomologic and avian investigations of an epidemic of West Nile fever in Romania in 1996, with serologic and molecular characterization of a virus isolate from mosquitoes.. Am J Trop Med Hyg 1999 Oct;61(4):600-11.
    pubmed: 10548295doi: 10.4269/ajtmh.1999.61.600google scholar: lookup
  13. Turell MJ, Dohm DJ, Sardelis MR, Oguinn ML, Andreadis TG, Blow JA. An update on the potential of north American mosquitoes (Diptera: Culicidae) to transmit West Nile Virus.. J Med Entomol 2005 Jan;42(1):57-62.
    doi: 10.1093/jmedent/42.1.57pubmed: 15691009google scholar: lookup
  14. Root JJ, Bosco-Lauth AM. West Nile Virus Associations in Wild Mammals: An Update.. Viruses 2019 May 21;11(5).
    doi: 10.3390/v11050459pmc: PMC6563505pubmed: 31117189google scholar: lookup
  15. Bunning ML, Bowen RA, Cropp CB, Sullivan KG, Davis BS, Komar N, Godsey MS, Baker D, Hettler DL, Holmes DA, Biggerstaff BJ, Mitchell CJ. Experimental infection of horses with West Nile virus.. Emerg Infect Dis 2002 Apr;8(4):380-6.
    doi: 10.3201/eid0804.010239pmc: PMC3393377pubmed: 11971771google scholar: lookup
  16. Mencattelli G, Ndione MHD, Rosà R, Marini G, Diagne CT, Diagne MM, Fall G, Faye O, Diallo M, Faye O, Savini G, Rizzoli A. Epidemiology of West Nile virus in Africa: An underestimated threat.. PLoS Negl Trop Dis 2022 Jan;16(1):e0010075.
  17. Zeller HG, 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 Mar;23(3):147-56.
    doi: 10.1007/s10096-003-1085-1pubmed: 14986160google scholar: lookup
  18. Bakonyi T, Ivanics E, Erdélyi K, Ursu K, Ferenczi E, Weissenböck H, Nowotny N. Lineage 1 and 2 strains of encephalitic West Nile virus, central Europe.. Emerg Infect Dis 2006 Apr;12(4):618-23.
    doi: 10.3201/eid1204.051379pmc: PMC3294705pubmed: 16704810google scholar: lookup
  19. de Heus P, Kolodziejek J, Camp JV, Dimmel K, Bagó Z, Hubálek Z, van den Hoven R, Cavalleri JV, Nowotny N. Emergence of West Nile virus lineage 2 in Europe: Characteristics of the first seven cases of West Nile neuroinvasive disease in horses in Austria.. Transbound Emerg Dis 2020 May;67(3):1189-1197.
    doi: 10.1111/tbed.13452pmc: PMC7317211pubmed: 31840920google scholar: lookup
  20. Bakonyi T, Ferenczi E, Erdélyi K, Kutasi O, Csörgő T, Seidel B, Weissenböck H, Brugger K, Bán E, Nowotny N. Explosive spread of a neuroinvasive lineage 2 West Nile virus in Central Europe, 2008/2009.. Vet Microbiol 2013 Jul 26;165(1-2):61-70.
    doi: 10.1016/j.vetmic.2013.03.005pubmed: 23570864google scholar: lookup
  21. Papa A, Xanthopoulou K, Gewehr S, Mourelatos S. Detection of West Nile virus lineage 2 in mosquitoes during a human outbreak in Greece.. Clin Microbiol Infect 2011 Aug;17(8):1176-80.
  22. Sirbu A, Ceianu CS, Panculescu-Gatej RI, Vazquez A, Tenorio A, Rebreanu R, Niedrig M, Nicolescu G, Pistol A. Outbreak of West Nile virus infection in humans, Romania, July to October 2010.. Euro Surveill 2011 Jan 13;16(2).
    doi: 10.2807/ese.16.02.19762-enpubmed: 21251489google scholar: lookup
  23. Busquets N, Laranjo-González M, Soler M, Nicolás O, Rivas R, Talavera S, Villalba R, San Miguel E, Torner N, Aranda C, Napp S. Detection of West Nile virus lineage 2 in North-Eastern Spain (Catalonia).. Transbound Emerg Dis 2019 Mar;66(2):617-621.
    doi: 10.1111/tbed.13086pmc: PMC7380044pubmed: 30506625google scholar: lookup
  24. Ziegler U, Lühken R, Keller M, Cadar D, van der Grinten E, Michel F, Albrecht K, Eiden M, Rinder M, Lachmann L, Höper D, Vina-Rodriguez A, Gaede W, Pohl A, Schmidt-Chanasit J, Groschup MH. West Nile virus epizootic in Germany, 2018.. Antiviral Res 2019 Feb;162:39-43.
  25. Wodak E, Richter S, Bagó Z, Revilla-Fernández S, Weissenböck H, Nowotny N, Winter P. Detection and molecular analysis of West Nile virus infections in birds of prey in the eastern part of Austria in 2008 and 2009.. Vet Microbiol 2011 May 5;149(3-4):358-66.
    doi: 10.1016/j.vetmic.2010.12.012pubmed: 21276665google scholar: lookup
  26. Pietsch C, Michalski D, Münch J, Petros S, Bergs S, Trawinski H, Lübbert C, Liebert UG. Autochthonous West Nile virus infection outbreak in humans, Leipzig, Germany, August to September 2020.. Euro Surveill 2020 Nov;25(46).
  27. Ziegler U, Santos PD, Groschup MH, Hattendorf C, Eiden M, Höper D, Eisermann P, Keller M, Michel F, Klopfleisch R, Müller K, Werner D, Kampen H, Beer M, Frank C, Lachmann R, Tews BA, Wylezich C, Rinder M, Lachmann L, Grünewald T, Szentiks CA, Sieg M, Schmidt-Chanasit J, Cadar D, Lühken R. West Nile Virus Epidemic in Germany Triggered by Epizootic Emergence, 2019.. Viruses 2020 Apr 15;12(4).
    doi: 10.3390/v12040448pmc: PMC7232143pubmed: 32326472google scholar: lookup
  28. Ziegler U, Bergmann F, Fischer D, Müller K, Holicki CM, Sadeghi B, Sieg M, Keller M, Schwehn R, Reuschel M, Fischer L, Krone O, Rinder M, Schütte K, Schmidt V, Eiden M, Fast C, Günther A, Globig A, Conraths FJ, Staubach C, Brandes F, Lierz M, Korbel R, Vahlenkamp TW, Groschup MH. Spread of West Nile Virus and Usutu Virus in the German Bird Population, 2019-2020.. Microorganisms 2022 Apr 12;10(4).
  29. Gardner IA, Wong SJ, Ferraro GL, Balasuriya UB, Hullinger PJ, Wilson WD, Shi PY, MacLachlan NJ. Incidence and effects of West Nile virus infection in vaccinated and unvaccinated horses in California.. Vet Res 2007 Jan-Feb;38(1):109-16.
    doi: 10.1051/vetres:2006045pubmed: 17274156google scholar: lookup
  30. Ostlund EN, Andresen JE, Andresen M. West Nile encephalitis.. Vet Clin North Am Equine Pract 2000 Dec;16(3):427-41.
    doi: 10.1016/S0749-0739(17)30087-1pubmed: 11219341google scholar: lookup
  31. Lohmann KL, Sieg M, Landmann M, Ganzenberg S, Arnold C, Vahlenkamp T, Ulrich RG. [West-Nile-Virus infections in 12 horses in east-central Germany].. Tierarztl Prax Ausg G Grosstiere Nutztiere 2022 Dec;50(6):362-376.
    doi: 10.1055/a-1965-0307pubmed: 36516822google scholar: lookup
  32. Seino KK, Long MT, Gibbs EP, Bowen RA, Beachboard SE, Humphrey PP, Dixon MA, Bourgeois MA. Comparative efficacies of three commercially available vaccines against West Nile Virus (WNV) in a short-duration challenge trial involving an equine WNV encephalitis model.. Clin Vaccine Immunol 2007 Nov;14(11):1465-71.
    doi: 10.1128/CVI.00249-07pmc: PMC2168174pubmed: 17687109google scholar: lookup
  33. Minke JM, Siger L, Cupillard L, Powers B, Bakonyi T, Boyum S, Nowotny N, Bowen R. Protection provided by a recombinant ALVAC(®)-WNV vaccine expressing the prM/E genes of a lineage 1 strain of WNV against a virulent challenge with a lineage 2 strain.. Vaccine 2011 Jun 20;29(28):4608-12.
    doi: 10.1016/j.vaccine.2011.04.058pubmed: 21549780google scholar: lookup
  34. Long MT, Gibbs EP, Mellencamp MW, Bowen RA, Seino KK, Zhang S, Beachboard SE, Humphrey PP. Efficacy, duration, and onset of immunogenicity of a West Nile virus vaccine, live Flavivirus chimera, in horses with a clinical disease challenge model.. Equine Vet J 2007 Nov;39(6):491-7.
    doi: 10.2746/042516407X217416pubmed: 18065305google scholar: lookup
  35. Long MT, Gibbs EP, Mellencamp MW, Zhang S, Barnett DC, Seino KK, Beachboard SE, Humphrey PP. Safety of an attenuated West Nile virus vaccine, live Flavivirus chimera in horses.. Equine Vet J 2007 Nov;39(6):486-90.
    doi: 10.2746/042516407X214473pubmed: 18065304google scholar: lookup
  36. Bergmann F, Trachsel DS, Stoeckle SD, Bernis Sierra J, Lübke S, Groschup MH, Gehlen H, Ziegler U. Seroepidemiological Survey of West Nile Virus Infections in Horses from Berlin/Brandenburg and North Rhine-Westphalia, Germany.. Viruses 2022 Jan 25;14(2).
    doi: 10.3390/v14020243pmc: PMC8877243pubmed: 35215837google scholar: lookup
  37. Ziegler U, Angenvoort J, Klaus C, Nagel-Kohl U, Sauerwald C, Thalheim S, Horner S, Braun B, Kenklies S, Tyczka J, Keller M, Groschup MH. Use of competition ELISA for monitoring of West Nile virus infections in horses in Germany.. Int J Environ Res Public Health 2013 Jul 24;10(8):3112-20.
    doi: 10.3390/ijerph10083112pmc: PMC3774427pubmed: 23887620google scholar: lookup
  38. Ganzenberg S, Sieg M, Ziegler U, Pfeffer M, Vahlenkamp TW, Hörügel U, Groschup MH, Lohmann KL. Seroprevalence and Risk Factors for Equine West Nile Virus Infections in Eastern Germany, 2020.. Viruses 2022 May 30;14(6).
    doi: 10.3390/v14061191pmc: PMC9229339pubmed: 35746662google scholar: lookup
  39. WILLIAMS MC, SIMPSON DI, HADDOW AJ, KNIGHT EM. THE ISOLATION OF WEST NILE VIRUS FROM MAN AND OF USUTU VIRUS FROM THE BIRD-BITING MOSQUITO MANSONIA AURITES (THEOBALD) IN THE ENTEBBE AREA OF UGANDA.. Ann Trop Med Parasitol 1964 Sep;58:367-74.
  40. Weissenböck H, Kolodziejek J, Url A, Lussy H, Rebel-Bauder B, Nowotny N. Emergence of Usutu virus, an African mosquito-borne flavivirus of the Japanese encephalitis virus group, central Europe.. Emerg Infect Dis 2002 Jul;8(7):652-6.
    doi: 10.3201/eid0807.020094pmc: PMC2730324pubmed: 12095429google scholar: lookup
  41. Vilibic-Cavlek T, Petrovic T, Savic V, Barbic L, Tabain I, Stevanovic V, Klobucar A, Mrzljak A, Ilic M, Bogdanic M, Benvin I, Santini M, Capak K, Monaco F, Listes E, Savini G. Epidemiology of Usutu Virus: The European Scenario.. Pathogens 2020 Aug 26;9(9).
    doi: 10.3390/pathogens9090699pmc: PMC7560012pubmed: 32858963google scholar: lookup
  42. Weissenböck H, Bakonyi T, Rossi G, Mani P, Nowotny N. Usutu virus, Italy, 1996.. Emerg Infect Dis 2013 Feb;19(2):274-7.
    doi: 10.3201/eid1902.121191pmc: PMC3559058pubmed: 23347844google scholar: lookup
  43. Nikolay B. A review of West Nile and Usutu virus co-circulation in Europe: how much do transmission cycles overlap?. Trans R Soc Trop Med Hyg 2015 Oct;109(10):609-18.
    doi: 10.1093/trstmh/trv066pubmed: 26286946google scholar: lookup
  44. Chvala S, Bakonyi T, Bukovsky C, Meister T, Brugger K, Rubel F, Nowotny N, Weissenböck H. Monitoring of Usutu virus activity and spread by using dead bird surveillance in Austria, 2003-2005.. Vet Microbiol 2007 Jun 21;122(3-4):237-45.
    doi: 10.1016/j.vetmic.2007.01.029pubmed: 17346908google scholar: lookup
  45. Weissenböck H, Hubálek Z, Halouzka J, Pichlmair A, Maderner A, Fragner K, Kolodziejek J, Loupal G, Kölbl S, Nowotny N. Screening for West Nile virus infections of susceptible animal species in Austria.. Epidemiol Infect 2003 Oct;131(2):1023-7.
    doi: 10.1017/S0950268803001031pmc: PMC2870048pubmed: 14596545google scholar: lookup
  46. Cook CL, Huang YS, Lyons AC, Alto BW, Unlu I, Higgs S, Vanlandingham DL. North American Culex pipiens and Culex quinquefasciatus are competent vectors for Usutu virus.. PLoS Negl Trop Dis 2018 Aug;12(8):e0006732.
  47. Holicki CM, Scheuch DE, Ziegler U, Lettow J, Kampen H, Werner D, Groschup MH. German Culex pipiens biotype molestus and Culex torrentium are vector-competent for Usutu virus.. Parasit Vectors 2020 Dec 30;13(1):625.
    doi: 10.1186/s13071-020-04532-1pmc: PMC7774236pubmed: 33380339google scholar: lookup
  48. Zannoli S, Sambri V. West Nile Virus and Usutu Virus Co-Circulation in Europe: Epidemiology and Implications.. Microorganisms 2019 Jun 26;7(7).
  49. Constant O, Gil P, Barthelemy J, Bolloré K, Foulongne V, Desmetz C, Leblond A, Desjardins I, Pradier S, Joulié A, Sandoz A, Amaral R, Boisseau M, Rakotoarivony I, Baldet T, Marie A, Frances B, Reboul Salze F, Tinto B, Van de Perre P, Salinas S, Beck C, Lecollinet S, Gutierrez S, Simonin Y. One Health surveillance of West Nile and Usutu viruses: a repeated cross-sectional study exploring seroprevalence and endemicity in Southern France, 2016 to 2020.. Euro Surveill 2022 Jun;27(25).
  50. Cavalleri JV, Korbacska-Kutasi O, Leblond A, Paillot R, Pusterla N, Steinmann E, Tomlinson J. European College of Equine Internal Medicine consensus statement on equine flaviviridae infections in Europe.. J Vet Intern Med 2022 Nov;36(6):1858-1871.
    doi: 10.1111/jvim.16581pmc: PMC9708432pubmed: 36367340google scholar: lookup
  51. Santini M, Vilibic-Cavlek T, Barsic B, Barbic L, Savic V, Stevanovic V, Listes E, Di Gennaro A, Savini G. First cases of human Usutu virus neuroinvasive infection in Croatia, August-September 2013: clinical and laboratory features.. J Neurovirol 2015 Feb;21(1):92-7.
    doi: 10.1007/s13365-014-0300-4pubmed: 25361698google scholar: lookup
  52. Pecorari M, Longo G, Gennari W, Grottola A, Sabbatini A, Tagliazucchi S, Savini G, Monaco F, Simone M, Lelli R, Rumpianesi F. First human case of Usutu virus neuroinvasive infection, Italy, August-September 2009.. Euro Surveill 2009 Dec 17;14(50).
    doi: 10.2807/ese.14.50.19446-enpubmed: 20070936google scholar: lookup
  53. Holbrook MR, Shope RE, Barrett AD. Use of recombinant E protein domain III-based enzyme-linked immunosorbent assays for differentiation of tick-borne encephalitis serocomplex flaviviruses from mosquito-borne flaviviruses.. J Clin Microbiol 2004 Sep;42(9):4101-10.
  54. Wondim MA, Czupryna P, Pancewicz S, Kruszewska E, Groth M, Moniuszko-Malinowska A. Epidemiological Trends of Trans-Boundary Tick-Borne Encephalitis in Europe, 2000-2019.. Pathogens 2022 Jun 18;11(6).
    doi: 10.3390/pathogens11060704pmc: PMC9228375pubmed: 35745558google scholar: lookup
  55. Tonteri E, Kipar A, Voutilainen L, Vene S, Vaheri A, Vapalahti O, Lundkvist Å. The three subtypes of tick-borne encephalitis virus induce encephalitis in a natural host, the bank vole (Myodes glareolus).. PLoS One 2013;8(12):e81214.
  56. Imhoff M, Hagedorn P, Schulze Y, Hellenbrand W, Pfeffer M, Niedrig M. Review: Sentinels of tick-borne encephalitis risk.. Ticks Tick Borne Dis 2015 Jul;6(5):592-600.
    doi: 10.1016/j.ttbdis.2015.05.001pubmed: 26005107google scholar: lookup
  57. Brandenburg PJ, Obiegala A, Schmuck HM, Dobler G, Chitimia-Dobler L, Pfeffer M. Seroprevalence of Tick-Borne Encephalitis (TBE) Virus Antibodies in Wild Rodents from Two Natural TBE Foci in Bavaria, Germany.. Pathogens 2023 Jan 25;12(2).
    doi: 10.3390/pathogens12020185pmc: PMC9962257pubmed: 36839457google scholar: lookup
  58. 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.
  59. Deviatkin AA, Kholodilov IS, Vakulenko YA, Karganova GG, Lukashev AN. Tick-Borne Encephalitis Virus: An Emerging Ancient Zoonosis?. Viruses 2020 Feb 23;12(2).
    doi: 10.3390/v12020247pmc: PMC7077300pubmed: 32102228google scholar: lookup
  60. Dobler G. Zoonotic tick-borne flaviviruses.. Vet Microbiol 2010 Jan 27;140(3-4):221-8.
    doi: 10.1016/j.vetmic.2009.08.024pubmed: 19765917google scholar: lookup
  61. Kaiser R. [Tick-borne encephalitis].. Nervenarzt 2016 Jun;87(6):667-80.
    doi: 10.1007/s00115-016-0134-9pubmed: 27225401google scholar: lookup
  62. Klaus C, Hörügel U, Hoffmann B, Beer M. Tick-borne encephalitis virus (TBEV) infection in horses: clinical and laboratory findings and epidemiological investigations.. Vet Microbiol 2013 May 3;163(3-4):368-72.
    doi: 10.1016/j.vetmic.2012.12.041pubmed: 23395291google scholar: lookup
  63. Pautienius A, Armonaite A, Simkute E, Zagrabskaite R, Buitkuviene J, Alpizar-Jara R, Grigas J, Zakiene I, Zienius D, Salomskas A, Stankevicius A. Cross-Sectional Study on the Prevalence and Factors Influencing Occurrence of Tick-Borne Encephalitis in Horses in Lithuania.. Pathogens 2021 Jan 31;10(2).
    doi: 10.3390/pathogens10020140pmc: PMC7911650pubmed: 33572628google scholar: lookup
  64. Magouras I, Schoster A, Fouché N, Gerber V, Groschup MH, Ziegler U, Fricker R, Griot C, Vögtlin A. Neurological disease suspected to be caused by tick-borne encephalitis virus infection in 6 horses in Switzerland.. J Vet Intern Med 2022 Nov;36(6):2254-2262.
    doi: 10.1111/jvim.16533pmc: PMC9708414pubmed: 36093849google scholar: lookup
  65. Angelini P, Tamba M, Finarelli AC, Bellini R, Albieri A, Bonilauri P, Cavrini F, Dottori M, Gaibani P, Martini E, Mattivi A, Pierro AM, Rugna G, Sambri V, Squintani G, Macini P. West Nile virus circulation in Emilia-Romagna, Italy: the integrated surveillance system 2009.. Euro Surveill 2010 Apr 22;15(16).
    doi: 10.2807/ese.15.16.19547-enpubmed: 20430000google scholar: lookup
  66. Paternoster G, Babo Martins S, Mattivi A, Cagarelli R, Angelini P, Bellini R, Santi A, Galletti G, Pupella S, Marano G, Copello F, Rushton J, Stärk KDC, Tamba M. Economics of One Health: Costs and benefits of integrated West Nile virus surveillance in Emilia-Romagna.. PLoS One 2017;12(11):e0188156.
  67. Leblond A, Hendrikx P, Sabatier P. West Nile virus outbreak detection using syndromic monitoring in horses.. Vector Borne Zoonotic Dis 2007 Fall;7(3):403-10.
    doi: 10.1089/vbz.2006.0593pubmed: 17767410google scholar: lookup
  68. Klaus C, Beer M, Saier R, Schubert H, Bischoff S, Süss J. Evaluation of serological tests for detecting tick-borne encephalitis virus (TBEV) antibodies in animals.. Berl Munch Tierarztl Wochenschr 2011 Nov-Dec;124(11-12):443-9.
    doi: 10.2376/0005-9366-124-443pubmed: 22191165google scholar: lookup
  69. Seidowski D, Ziegler U, von Rönn JA, Müller K, Hüppop K, Müller T, Freuling C, Mühle RU, Nowotny N, Ulrich RG, Niedrig M, Groschup MH. West Nile virus monitoring of migratory and resident birds in Germany.. Vector Borne Zoonotic Dis 2010 Oct;10(7):639-47.
    doi: 10.1089/vbz.2009.0236pubmed: 20854016google scholar: lookup
  70. de Heus P, Kolodziejek J, Hubálek Z, Dimmel K, Racher V, Nowotny N, Cavalleri JV. West Nile Virus and Tick-Borne Encephalitis Virus Are Endemic in Equids in Eastern Austria.. Viruses 2021 Sep 19;13(9).
    doi: 10.3390/v13091873pmc: PMC8473302pubmed: 34578454google scholar: lookup
  71. Barbić L, Listeš E, Katić S, Stevanović V, Madić J, Starešina V, Labrović A, Di Gennaro A, Savini G. Spreading of West Nile virus infection in Croatia.. Vet Microbiol 2012 Oct 12;159(3-4):504-8.
    doi: 10.1016/j.vetmic.2012.04.038pubmed: 22609103google scholar: lookup
  72. Mangana-Vougiouka O, Boutsini S, Ntousi D, Patakakis M, Orfanou E, Zafiropoulou K, Dilaveris D, Panagiotatos D, Nomikou K. Epizootiological investigation of the most important infectious equine diseases in Greece.. Rev Sci Tech 2013 Dec;32(3):775-87.
    doi: 10.20506/rst.32.2.2217pubmed: 24761730google scholar: lookup
  73. Napp S, Llorente F, Beck C, Jose-Cunilleras E, Soler M, Pailler-García L, Amaral R, Aguilera-Sepúlveda P, Pifarré M, Molina-López R, Obón E, Nicolás O, Lecollinet S, Jiménez-Clavero MÁ, Busquets N. Widespread Circulation of Flaviviruses in Horses and Birds in Northeastern Spain (Catalonia) between 2010 and 2019.. Viruses 2021 Nov 30;13(12).
    doi: 10.3390/v13122404pmc: PMC8708358pubmed: 34960673google scholar: lookup
  74. Jiménez-Clavero MA, Llorente F, Sotelo E, Soriguer R, Gómez-Tejedor C, Figuerola J. West Nile virus serosurveillance in horses in Donana, Spain, 2005 to 2008.. Vet Rec 2010 Sep 4;167(10):379-80.
    doi: 10.1136/vr.c3155pubmed: 20817900google scholar: lookup
  75. García-Bocanegra I, Arenas-Montes A, Napp S, Jaén-Téllez JA, Fernández-Morente M, Fernández-Molera V, Arenas A. Seroprevalence and risk factors associated to West Nile virus in horses from Andalusia, Southern Spain.. Vet Microbiol 2012 Dec 7;160(3-4):341-6.
    doi: 10.1016/j.vetmic.2012.06.027pubmed: 22776513google scholar: lookup
  76. Rexhepi A, Sherifi K, Berxholi K, Xhekaj B, Muja-Bajraktari N, Özkul A, von Possel R, Emmerich P. First Serological Evidence of West Nile Virus Among Equines and Birds in Kosovo, 2018-2019.. Vector Borne Zoonotic Dis 2021 Feb;21(2):116-120.
    doi: 10.1089/vbz.2020.2673pubmed: 33090084google scholar: lookup
  77. Ziegler U, Skrypnyk A, Keller M, Staubach C, Bezymennyi M, Damiani AM, Osterrieder N, Groschup MH. West nile virus antibody prevalence in horses of Ukraine.. Viruses 2013 Oct 4;5(10):2469-82.
    doi: 10.3390/v5102469pmc: PMC3814598pubmed: 24100889google scholar: lookup
  78. Bażanów B, Jansen van Vuren P, Szymański P, Stygar D, Frącka A, Twardoń J, Kozdrowski R, Pawęska JT. A Survey on West Nile and Usutu Viruses in Horses and Birds in Poland.. Viruses 2018 Feb 17;10(2).
    doi: 10.3390/v10020087pmc: PMC5850394pubmed: 29462983google scholar: lookup
  79. Maquart M, Dahmani M, Marié JL, Gravier P, Leparc-Goffart I, Davoust B. First Serological Evidence of West Nile Virus in Horses and Dogs from Corsica Island, France.. Vector Borne Zoonotic Dis 2017 Apr;17(4):275-277.
    doi: 10.1089/vbz.2016.2024pubmed: 28075236google scholar: lookup
  80. Lupulovic D, Martín-Acebes MA, Lazic S, Alonso-Padilla J, Blázquez AB, Escribano-Romero E, Petrovic T, Saiz JC. First serological evidence of West Nile virus activity in horses in Serbia.. Vector Borne Zoonotic Dis 2011 Sep;11(9):1303-5.
    doi: 10.1089/vbz.2010.0249pubmed: 21438694google scholar: lookup
  81. Guerrero-Carvajal F, Bravo-Barriga D, Martín-Cuervo M, Aguilera-Sepúlveda P, Ferraguti M, Jiménez-Clavero MÁ, Llorente F, Alonso JM, Frontera E. Serological evidence of co-circulation of West Nile and Usutu viruses in equids from western Spain.. Transbound Emerg Dis 2021 May;68(3):1432-1444.
    doi: 10.1111/tbed.13810pubmed: 32853452google scholar: lookup
  82. Berxholi K, Ziegler U, Rexhepi A, Schmidt K, Mertens M, Korro K, Cuko A, Angenvoort J, Groschup MH. Indigenous West Nile virus infections in horses in Albania.. Transbound Emerg Dis 2013 Nov;60 Suppl 2:45-50.
    doi: 10.1111/tbed.12141pubmed: 24589101google scholar: lookup
  83. Folly AJ, Waller ESL, McCracken F, McElhinney LM, Roberts H, Johnson N. Equine seroprevalence of West Nile virus antibodies in the UK in 2019.. Parasit Vectors 2020 Nov 26;13(1):596.
    doi: 10.1186/s13071-020-04481-9pmc: PMC7690108pubmed: 33243297google scholar: lookup
  84. Niczyporuk JS, Samorek-Salamonowicz E, Lecollinet S, Pancewicz SA, Kozdruń W, Czekaj H. Occurrence of West Nile virus antibodies in wild birds, horses, and humans in Poland.. Biomed Res Int 2015;2015:234181.
    doi: 10.1155/2015/234181pmc: PMC4383358pubmed: 25866767google scholar: lookup
  85. Madić J, Savini G, Di Gennaro A, Monaco F, Jukić B, Kovac S, Rudan N, Listes E. Serological evidence for West Nile virus infection in horses in Croatia.. Vet Rec 2007 Jun 2;160(22):772-3.
    doi: 10.1136/vr.160.22.772pubmed: 17545649google scholar: lookup
  86. Angenvoort J, Brault AC, Bowen RA, Groschup MH. West Nile viral infection of equids.. Vet Microbiol 2013 Nov 29;167(1-2):168-80.
  87. Nielsen CF, Reisen WK, Armijos MV, Maclachlan NJ, Scott TW. High subclinical West Nile virus incidence among nonvaccinated horses in northern California associated with low vector abundance and infection.. Am J Trop Med Hyg 2008 Jan;78(1):45-52.
    doi: 10.4269/ajtmh.2008.78.45pubmed: 18187784google scholar: lookup
  88. Beck C, Jimenez-Clavero MA, 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 Nov 12;10(11):6049-83.
    doi: 10.3390/ijerph10116049pmc: PMC3863887pubmed: 24225644google scholar: lookup
  89. Vinogradova E.B. Culex Pipiens Pipiens Mosquitoes: Taxonomy, Distribution, Ecology, Physiology, Genetics, Applied Importance and Control. Pensoft; Moscow and Sofia, Russia: 2000. p. 250.
  90. Camino E, Schmid S, Weber F, Pozo P, de Juan L, König M, Cruz-Lopez F. Detection of antibodies against tick-borne encephalitis flaviviruses in breeding and sport horses from Spain.. Ticks Tick Borne Dis 2020 Sep;11(5):101487.
    doi: 10.1016/j.ttbdis.2020.101487pubmed: 32723662google scholar: lookup
  91. Müller K. Untersuchung zum Vorkommen von Antikörpern gegen das “Tick Borne Encephalitis Virus” (TBEV) beim Pferd im Endemiegebiet Marburg-Biedenkopf. Ph.D. Thesis. Fachbereich Veterinärmedizin der Justus-Liebig-Universität Giessen; Giessen, Germany: 2006. VVB Laufersweiler.
  92. Rushton JO, Lecollinet S, Hubálek Z, Svobodová P, Lussy H, Nowotny N. Tick-borne encephalitis virus in horses, Austria, 2011.. Emerg Infect Dis 2013 Apr;19(4):635-7.
    doi: 10.3201/eid1904.121450pmc: PMC3647421pubmed: 23631894google scholar: lookup
  93. Janitza-Futterer D. Serologische Untersuchungen zur endemischen Situation der Infektion mit dem FSME-Virus in einer südbadischen Pferde- und Hundepopulation. Ph.D. Thesis. Tierärztliche Fakultät der Ludwig-Maximillians-Universität; München, Germany: 2003.
  94. Sikutová S, Hornok S, Hubálek Z, Dolezálková I, Juricová Z, Rudolf I. Serological survey of domestic animals for tick-borne encephalitis and Bhanja viruses in northeastern Hungary.. Vet Microbiol 2009 Mar 30;135(3-4):267-71.
    doi: 10.1016/j.vetmic.2008.09.082pubmed: 19036537google scholar: lookup
  95. Mburu MM, Zembere K, Mzilahowa T, Terlouw AD, Malenga T, van den Berg H, Takken W, McCann RS. Impact of cattle on the abundance of indoor and outdoor resting malaria vectors in southern Malawi.. Malar J 2021 Aug 26;20(1):353.
    doi: 10.1186/s12936-021-03885-xpmc: PMC8390081pubmed: 34446033google scholar: lookup
  96. Huang CI, Kay SC, Davis S, Tufts DM, Gaffett K, Tefft B, Diuk-Wasser MA. High burdens of Ixodes scapularis larval ticks on white-tailed deer may limit Lyme disease risk in a low biodiversity setting.. Ticks Tick Borne Dis 2019 Feb;10(2):258-268.
  97. Klaus C, Beer M, Saier R, Schau U, Moog U, Hoffmann B, Diller R, Süss J. Goats and sheep as sentinels for tick-borne encephalitis (TBE) virus--epidemiological studies in areas endemic and non-endemic for TBE virus in Germany.. Ticks Tick Borne Dis 2012 Feb;3(1):27-37.
    doi: 10.1016/j.ttbdis.2011.09.011pubmed: 22309856google scholar: lookup
  98. RKI Karte der FSME-Risikogebiete. [(accessed on 17 January 2023)]; Available online: https://www.rki.de/DE/Content/InfAZ/F/FSME/Karte_Tab.html.

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