Neurotropic Tick-Borne Flavivirus in Alpine Chamois (Rupicapra rupicapra rupicapra), Austria, 2017, Italy, 2023
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
Project no. PE00000007, INF-ACT
Government of the Czech Republic
grant agreement number 871029
Horizon 2020
Ricerca Finalizzata GR-2021-12374932
Italian Ministry of Health
PubMed
39861911
PubMed Central
PMC11769369
DOI
10.3390/v17010122
PII: v17010122
Knihovny.cz E-zdroje
- Klíčová slova
- Alpine chamois, Flaviviridae, Ixodes ricinus, Rupicapra rupicapra, Spanish goat encephalitis virus, encephalitis, flavivirus, louping ill virus, neurotropic, tick-borne encephalitis virus,
- MeSH
- Flavivirus izolace a purifikace klasifikace genetika MeSH
- fylogeneze * MeSH
- genom virový MeSH
- infekce viry z rodu Flavivirus veterinární virologie epidemiologie MeSH
- klíšťata virologie MeSH
- klíšťová encefalitida virologie MeSH
- nemoci koz virologie MeSH
- Rupicapra * virologie MeSH
- viry klíšťové encefalitidy * izolace a purifikace klasifikace genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Itálie MeSH
- Rakousko MeSH
The European subtype of tick-borne encephalitis virus (TBEV-Eur; species Orthoflavivirus encephalitidis, family Flaviviridae) was the only tick-borne flavivirus present in central Europe known to cause neurologic disease in humans and several animal species. Here, we report a tick-borne flavivirus isolated from Alpine chamois (Rupicapra rupicapra rupicapra) with encephalitis and attached ticks, present over a wide area in the Alps. Cases were detected in 2017 in Salzburg, Austria, and 2023 in Lombardy and Piedmont, Italy. The virus strains exhibit 94.8-97.3% nucleotide identities to each other and are more closely related to Louping ill viruses (LIV; Orthoflavivirus loupingi; 90-92% identities) than to TBEV-Eur (less than 88%). The chamois-derived virus strains, tentatively termed "Alpine chamois encephalitis virus", form a well-supported independent genetic clade with Spanish goat encephalitis virus, clearly separated from other LIV. This supports its designation as a new virus subtype with the proposed shared taxonomic name "Spanish goat and Alpine chamois encephalitis virus subtype" within the species Orthoflavivirus loupingi. The zoonotic potential of this newly identified virus subtype as well as its host range in other animal species including farm animals needs to be further investigated.
Center for Virology Medical University of Vienna 1090 Vienna Austria
Department of Veterinary Sciences University of Pisa 56124 Pisa Italy
Institute of Vertebrate Biology Czech Academy of Sciences 60365 Brno Czech Republic
Istituto Zooprofilattico Sperimentale del Piemonte Liguria e Valle d'Aosta 10154 Torino Italy
Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia Romagna 25124 Brescia Italy
Istituto Zooprofilattico Sperimentale delle Venezie 35020 Legnaro Italy
Zobrazit více v PubMed
Lange M., Chitimia-Dobler L., Dobler G. Dr. Hans (Johann) Schneider—Medical officer and first describer of tick born encephlitis (TBE) Wehrmed. Montasschrift. 2021;65:294–301.
Schneider H. Über epidemische akute “Meningitis serosa”. Wien. Klin. Wochenschr. 1931;44:350–352.
Ruzek D., Kaucka K. A brief tale of two pioneering moments: Europe’s first discovery of Tick-Borne Encephalitis (TBE) virus beyond the Soviet Union and the largest alimentary TBE outbreak in history. Ticks Tick Borne Dis. 2024;15:102314. doi: 10.1016/j.ttbdis.2024.102314. PubMed DOI
Gallia F., Rampas J., Hollender L. Laboratory infection with encephalitis virus. Cas. Lek. Cesk. 1949;88:224–229.
Krejčí J. Epidemic of viral meningoencephalitis cases in Vyškov region. Lékařské Listy. 1949;4:132–134.
Hubálek Z. History of Arbovirus Research in the Czech Republic. Viruses. 2021;13:2334. doi: 10.3390/v13112334. PubMed DOI PMC
Simmonds P., Becher P., Bukh J., Gould E.A., Meyers G., Monath T., Muerhoff S., Pletnev A., Rico-Hesse R., Smith D.B., et al. ICTV Virus Taxonomy Profile: Flaviviridae. J. Gen. Virol. 2017;98:2–3. doi: 10.1099/jgv.0.000672. PubMed DOI PMC
Kovalev S.Y., Mukhacheva T.A. Reconsidering the classification of tick-borne encephalitis virus within the Siberian subtype gives new insights into its evolutionary history. Infect. Genet. Evol. 2017;55:159–165. doi: 10.1016/j.meegid.2017.09.014. PubMed DOI
Dai X., Shang G., Lu S., Yang J., Xu J. A new subtype of eastern tick-borne encephalitis virus discovered in Qinghai-Tibet Plateau, China. Emerg. Microbes Infect. 2018;7:74. doi: 10.1038/s41426-018-0081-6. PubMed DOI PMC
Hubálek Z., Rudolf I. Tick-borne viruses in Europe. Parasitol. Res. 2012;111:9–36. doi: 10.1007/s00436-012-2910-1. PubMed DOI
Van Heuverswyn J., Hallmaier-Wacker L.K., Beauté J., Gomes Dias J., Haussig J.M., Busch K., Kerlik J., Markowicz M., Mäkelä H., Nygren T.M., et al. Spatiotemporal spread of tick-borne encephalitis in the EU/EEA, 2012 to 2020. Euro Surveill. 2023;28:2200543. doi: 10.2807/1560-7917.ES.2023.28.11.2200543. PubMed DOI PMC
Król N., Chitimia-Dobler L., Dobler G., Kiewra D., Czułowska A., Obiegala A., Zajkowska J., Juretzek T., Pfeffer M. Identification of New Microfoci and Genetic Characterization of Tick-Borne Encephalitis Virus Isolates from Eastern Germany and Western Poland. Viruses. 2024;16:637. doi: 10.3390/v16040637. PubMed DOI PMC
Rubel F., Brugger K. Operational TBE incidence forecasts for Austria, Germany, and Switzerland 2019–2021. Ticks Tick Borne Dis. 2021;12:101579. doi: 10.1016/j.ttbdis.2020.101579. PubMed DOI
Dagostin F., Tagliapietra V., Marini G., Cataldo C., Bellenghi M., Pizzarelli S., Cammarano R.R., Wint W., Alexander N.S., Neteler M., et al. Ecological and environmental factors affecting the risk of tick-borne encephalitis in Europe, 2017 to 2021. Euro Surveill. 2023;28:2300121. doi: 10.2807/1560-7917.ES.2023.28.42.2300121. PubMed DOI PMC
Saegerman C., Humblet M.F., Leandri M., Gonzalez G., Heyman P., Sprong H., L’Hostis M., Moutailler S., Bonnet S.I., Haddad N., et al. First Expert Elicitation of Knowledge on Possible Drivers of Observed Increasing Human Cases of Tick-Borne Encephalitis in Europe. Viruses. 2023;15:791. doi: 10.3390/v15030791. PubMed DOI PMC
Stiasny K., Santonja I., Holzmann H., Essl A., Stanek G., Kundi M., Heinz F.X. The regional decline and rise of tick-borne encephalitis incidence do not correlate with Lyme borreliosis, Austria, 2005 to 2018. Euro Surveill. 2021;26:2002108. doi: 10.2807/1560-7917.ES.2021.26.35.2002108. PubMed DOI PMC
Esser H.J., Lim S.M., de Vries A., Sprong H., Dekker D.J., Pascoe E.L., Bakker J.W., Suin V., Franz E., Martina B.E.E., et al. Continued Circulation of Tick-Borne Encephalitis Virus Variants and Detection of Novel Transmission Foci, the Netherlands. Emerg. Infect. Dis. 2022;28:2416–2424. doi: 10.3201/eid2812.220552. PubMed DOI PMC
Holzmann H., Aberle S.W., Stiasny K., Werner P., Mischak A., Zainer B., Netzer M., Koppi S., Bechter E., Heinz F.X., et al. Tick-borne encephalitis from eating goat cheese in a mountain region of Austria. Emerg. Infect. Dis. 2009;15:1671–1673. doi: 10.3201/eid1510.090743. PubMed DOI PMC
Slunge D., Boman A., Studahl M. Burden of Tick-Borne Encephalitis, Sweden. Emerg. Infect. Dis. 2022;28:314–322. doi: 10.3201/eid2802.204324. PubMed DOI PMC
Barp N., Cappi C., Meschiari M., Battistel M., Libbra M.V., Ferri M.A., Ballestri S., Gallerani A., Ferrari F., Meacci M., et al. First Human Case of Tick-Borne Encephalitis in Non-Endemic Region in Italy: A Case Report. Pathogens. 2022;11:854. doi: 10.3390/pathogens11080854. PubMed DOI PMC
Gaffuri A., Sassera D., Calzolari M., Gibelli L., Lelli D., Tebaldi A., Vicari N., Bianchi A., Pigoli C., Cerioli M., et al. Tick-Borne Encephalitis, Lombardy, Italy. Emerg. Infect. Dis. 2024;30:341–344. doi: 10.3201/eid3002.231016. PubMed DOI PMC
Hubálek Z., Rudolf I., Nowotny N. Arboviruses pathogenic for domestic and wild animals. Adv. Virus Res. 2014;89:201–275. doi: 10.1016/B978-0-12-800172-1.00005-7. PubMed DOI
Martello E., Gillingham E.L., Phalkey R., Vardavas C., Nikitara K., Bakonyi T., Gossner C.M., Leonardi-Bee J. Systematic review on the non-vectorial transmission of Tick-borne encephalitis virus (TBEv) Ticks Tick Borne Dis. 2022;13:102028. doi: 10.1016/j.ttbdis.2022.102028. PubMed DOI
de Heus P., Kolodziejek J., Hubalek Z., Dimmel K., Racher V., Nowotny N., Cavalleri J.V. West Nile Virus and Tick-Borne Encephalitis Virus Are Endemic in Equids in Eastern Austria. Viruses. 2021;13:1873. doi: 10.3390/v13091873. PubMed DOI PMC
Pfeffer M., Dobler G. Tick-borne encephalitis virus in dogs—Is this an issue? Parasit. Vectors. 2011;4:59. doi: 10.1186/1756-3305-4-59. PubMed DOI PMC
Rushton J.O., Lecollinet S., Hubalek Z., Svobodová P., Lussy H., Nowotny N. Tick-borne encephalitis virus in horses, Austria, 2011. Emerg Infect Dis. 2013;19:635–637. doi: 10.3201/eid1904.121450. PubMed DOI PMC
de Heus P., Bagó Z., Weidinger P., Lale D., Trachsel D.S., Revilla-Fernández S., Matiasek K., Nowotny N. Severe Neurologic Disease in a Horse Caused by Tick-Borne Encephalitis Virus, Austria, 2021. Viruses. 2023;15:22. doi: 10.3390/v15102022. PubMed DOI PMC
Salat J., Hunady M., Schanilec P., Strakova P., Stefanik M., Svoboda P., Strelcova L., Bojcukova J., Palus M., Růžek D. Experimental and Natural Infections of Tick-Borne Encephalitis Virus in Dogs. Viruses. 2021;13:39. doi: 10.3390/v13102039. PubMed DOI PMC
Weissenböck H., Suchy A., Holzmann H. Tick-borne encephalitis in dogs: Neuropathological findings and distribution of antigen. Acta Neuropathol. 1998;95:361–366. doi: 10.1007/s004010050811. PubMed DOI
Bagó Z., Bauder B., Kolodziejek J., Nowotny N., Weissenböck H. Tickborne encephalitis in a mouflon (Ovis ammon musimon) Vet. Rec. 2002;150:218–220. doi: 10.1136/vr.150.7.218. PubMed DOI
Da Rold G., Obber F., Monne I., Milani A., Ravagnan S., Toniolo F., Sgubin S., Zamperin G., Foiani G., Vascellari M., et al. Clinical Tick-Borne Encephalitis in a Roe Deer (Capreolus capreolus L.) Viruses. 2022;14:300. doi: 10.3390/v14020300. PubMed DOI PMC
Grassi L., Drigo M., Zelena H., Pasotto D., Cassini R., Mondin A., Franzo G., Tucciarone C.M., Ossola M., Vidorin E., et al. Wild ungulates as sentinels of flaviviruses and tick-borne zoonotic pathogen circulation: An Italian perspective. BMC Vet. Res. 2023;19:155. doi: 10.1186/s12917-023-03717-x. PubMed DOI PMC
Chiffi G., Grandgirard D., Leib S.L., Chrdle A., Růžek D. Tick-borne encephalitis: A comprehensive review of the epidemiology, virology, and clinical picture. Rev. Med. Virol. 2023;33:e2470. doi: 10.1002/rmv.2470. PubMed DOI
Kohlmaier B., Schweintzger N.A., Sagmeister M.G., Švendová V., Kohlfürst D.S., Sonnleitner A., Leitner M., Berghold A., Schmiedberger E., Fazekas F., et al. Clinical Characteristics of Patients with Tick-Borne Encephalitis (TBE): A European Multicentre Study from 2010 to 2017. Microorganisms. 2021;9:1420. doi: 10.3390/microorganisms9071420. PubMed DOI PMC
Angulo F.J., Zhang P., Halsby K., Kelly P., Pilz A., Madhava H., Moïsi J.C., Jodar L. A systematic literature review of the effectiveness of tick-borne encephalitis vaccines in Europe. Vaccine. 2023;41:6914–6921. doi: 10.1016/j.vaccine.2023.10.014. PubMed DOI
Heinz F.X. Development of a highly purified tick-borne encephalitis vaccine: A personal historical account. Wien. Klin. Wochenschr. 2024;136:215–219. doi: 10.1007/s00508-023-02240-1. PubMed DOI PMC
Schröder W., von Elsner-Schack I.V. Correct age determination in chamois. In: Lovari S., editor. The Biology and Management of Mountain Ungulates. Croom Helm; London, UK: 1985. pp. 67–70.
Patel P., Landt O., Kaiser M., Faye O., Koppe T., Lass U., Sall A.A., Niedrig M. Development of one-step quantitative reverse transcription PCR for the rapid detection of flaviviruses. Virol. J. 2013;10:58. doi: 10.1186/1743-422X-10-58. PubMed DOI PMC
Mansfield K.L., Morales A.B., Johnson N., Ayllón N., Höfle U., Alberdi P., Fernández de Mera I.G., Marín J.F., Gortázar C., de la Fuente J., et al. Identification and characterization of a novel tick-borne flavivirus subtype in goats (Capra hircus) in Spain. Pt 7J. Gen. Virol. 2015;96:1676–1681. doi: 10.1099/vir.0.000096. PubMed DOI
Estrada-Pena A., Pfaffle M., Baneth G., Kleinerman G., Petney T.N. Ixodoidea of the Western Palaearctic: A review of available literature for identification of species. Ticks Tick Borne Dis. 2017;8:512–525. doi: 10.1016/j.ttbdis.2017.02.013. PubMed DOI
Schwaiger M., Cassinotti P. Development of a quantitative real-time RT-PCR assay with internal control for the laboratory detection of tick borne encephalitis virus (TBEV) RNA. J. Clin. Virol. 2003;27:136–145. doi: 10.1016/S1386-6532(02)00168-3. PubMed DOI
Kalantar K.L., Carvalho T., de Bourcy C.F.A., Dimitrov B., Dingle G., Egger R., Han J., Holmes O.B., Juan Y.F., King R., et al. IDseq-An open source cloud-based pipeline and analysis service for metagenomic pathogen detection and monitoring. Gigascience. 2020;9:giaa111. doi: 10.1093/gigascience/giaa111. PubMed DOI PMC
Scaramozzino N., Crance J.M., Jouan A., DeBriel D.A., Stoll F., Garin D. Comparison of flavivirus universal primer pairs and development of a rapid, highly sensitive heminested reverse transcription-PCR assay for detection of flaviviruses targeted to a conserved region of the NS5 gene sequences. J. Clin. Microbiol. 2001;39:1922–1927. doi: 10.1128/JCM.39.5.1922-1927.2001. PubMed DOI PMC
Trifinopoulos J., Nguyen L.T., von Haeseler A., Minh B.Q. W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 2016;44:W232–W235. doi: 10.1093/nar/gkw256. PubMed DOI PMC
Robert X., Gouet P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 2014;42:W320–W324. doi: 10.1093/nar/gku316. PubMed DOI PMC
Marin M.S., McKenzie J., Gao G.F., Reid H.W., Antoniadis A., Gould E.A. The virus causing encephalomyelitis in sheep in Spain: A new member of the tick-borne encephalitis group. Res. Vet. Sci. 1995;58:11–13. doi: 10.1016/0034-5288(95)90081-0. PubMed DOI
Menzano A., Tizzani P., Farber M.D., Garcia-Vozmediano A., Martinelli L., Rossi L., Tomassone L. Zoonotic Tick-Borne Pathogens in Ticks from Vegetation and Alpine Ibex (Capra ibex) in the Maritime Alps, Italy. Animals. 2024;14:2251. doi: 10.3390/ani14152251. PubMed DOI PMC
Habib J., Zenner L., Garel M., Mercier A., Poirel M.T., Itty C., Appolinaire J., Amblard T., Benedetti P., Sanchis F., et al. Prevalence of tick-borne pathogens in ticks collected from the wild mountain ungulates mouflon and chamois in 4 regions of France. Parasite. 2024;31:21. doi: 10.1051/parasite/2024011. PubMed DOI PMC
Kutschera L.S., Wolfinger M.T. Evolutionary traits of Tick-borne encephalitis virus: Pervasive non-coding RNA structure conservation and molecular epidemiology. Virus Evol. 2022;8:veac051. doi: 10.1093/ve/veac051. PubMed DOI PMC
Balseiro A., Perez-Martinez C., Dagleish M.P., Royo L.J., Polledo L., García Marín J.F. Goats Naturally Infected with the Spanish Goat Encephalitis Virus (SGEV): Pathological Features and An Outbreak. Animals. 2022;13:72. doi: 10.3390/ani13010072. PubMed DOI PMC
Balseiro A., Royo L.J., Martinez C.P., Fernández de Mera I.G., Höfle Ú., Polledo L., Marreros N., Casais R., Marín J.F. Louping ill in goats, Spain, 2011. Emerg Infect Dis. 2012;18:976–978. doi: 10.3201/eid1806.120220. PubMed DOI PMC
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. Pt 5J. Gen. Virol. 2014;95:1005–1014. doi: 10.1099/vir.0.062356-0. PubMed DOI PMC
Gonzalez L., Reid H.W., Pow I., Gilmour J.S. A disease resembling louping-ill in sheep in the Basque region of Spain. Vet. Rec. 1987;121:12–13. doi: 10.1136/vr.121.1.12. PubMed DOI
Salinas L.M., Casais R., Garcia Marin J.F., Dalton K.P., Royo L.J., Del Cerro A., Gayo E., Dagleish M.P., Juste R.A., Balseiro A. Lambs are Susceptible to Experimental Challenge with Spanish Goat Encephalitis Virus. J. Comp. Pathol. 2017;156:400–408. doi: 10.1016/j.jcpa.2017.03.003. PubMed DOI
Salinas L.M., Casais R., Garcia Marin J.F., Dalton K.P., Royo L.J., Del Cerro A., Gayo E., Dagleish M.P., Alberdi P., Juste R.A., et al. Vaccination against Louping Ill Virus Protects Goats from Experimental Challenge with Spanish Goat Encephalitis Virus. J. Comp. Pathol. 2017;156:409–418. doi: 10.1016/j.jcpa.2017.03.004. PubMed DOI
Santonja I., Stiasny K., Essl A., Heinz F.X., Kundi M., Holzmann H. Tick-Borne Encephalitis in Vaccinated Patients: A Retrospective Case-Control Study and Analysis of Vaccination Field Effectiveness in Austria from 2000 to 2018. J. Infect. Dis. 2023;227:512–521. doi: 10.1093/infdis/jiac075. PubMed DOI