Clinical, pathological and virological aspects of fatal West Nile virus infections in ten free-ranging goshawks (Accipiter gentilis) in Germany.
West Nile virus
birds of prey
flavivirus
goshawk
neurology
vector-borne disease
Journal
Transboundary and emerging diseases
ISSN: 1865-1682
Titre abrégé: Transbound Emerg Dis
Pays: Germany
ID NLM: 101319538
Informations de publication
Date de publication:
Mar 2021
Mar 2021
Historique:
revised:
09
07
2020
received:
28
04
2020
accepted:
26
07
2020
pubmed:
4
8
2020
medline:
1
7
2021
entrez:
4
8
2020
Statut:
ppublish
Résumé
West Nile virus (WNV), a zoonotic arbovirus, is a new epizootic disease in Germany and caused increasing avian and equine mortality since its first detection in 2018. The northern goshawk (Accipiter gentilis) is highly susceptible to fatal WNV disease and thus is considered as an indicator species for WNV emergence in European countries. Therefore, information regarding clinical presentation and pathological findings is important for identifying suspect cases and initiating further virological diagnostics. Between July and September 2019, ten free-ranging goshawks were admitted to the Small Animal Clinic of the Freie Universität Berlin with later confirmed WNV infection. Clinical, pathological and virological findings are summarized in this report. All birds were presented obtunded and in poor to cachectic body condition. Most of the birds were juveniles (8/10) and females (9/10). Neurologic abnormalities were observed in all birds and included stupor (3/10), seizures (3/10), head tremor (2/10), head tilt (2/10), ataxia (2/10) and monoplegia (2/10). Concurrent diseases like aerosacculitis/pneumonia (7/10), clinical infections with Eucoleus spp. and Trichomonas spp. (3/10), trauma-related injuries (3/10) and myiasis (2/10) were found. Blood analysis results were unspecific considering concurrent diseases. Median time of survival was two days. The most common pathological findings were meningoencephalitis (9/10), myocarditis (8/10), iridocyclitis (8/8) and myositis (7/10). WNV infection was diagnosed by real-time quantitative reverse transcription polymerase chain reaction and confirmed by serology and immunohistochemistry.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
907-919Informations de copyright
© 2020 Wiley-VCH GmbH.
Références
Altenkamp, R. (2002). Bestandsentwicklung, Reproduktion und Brutbiologie einer urbanen Population des Habichts Accipiter gentilis (Linné 1758). Berlin, Germany: University of Berlin. (Unpublished diploma thesis).
Altenkamp, R. (2015). Die urbanen Habichte in Berlin. Paper presented at the Tagung zum Vogel des Jahres 2015, Recklinghausen.
Angenvoort, J., Fischer, D., Fast, C., Ziegler, U., Eiden, M., de La Fuente, J. G., … Groschup, M. H. (2014). Limited efficacy of West Nile virus vaccines in large falcons (Falco spp.). Veterinary Research, 45(1), 41. https://doi.org/10.1186/1297-9716-45-41
Bakonyi, T., Ferenczi, E., Erdelyi, K., Kutasi, O., Csorgo, T., Seidel, B., … Nowotny, N. (2013). Explosive spread of a neuroinvasive lineage 2 West Nile virus in Central Europe, 2008/2009. Veterinary Microbiology, 165(1-2), 61-70. https://doi.org/10.1016/j.vetmic.2013.03.005
Bakonyi, T., Ivanics, E., Erdelyi, K., Ursu, K., Ferenczi, E., Weissenbock, H., & Nowotny, N. (2006). Lineage 1 and 2 strains of encephalitic West Nile virus, central Europe. Emerging Infectious Diseases, 12(4), 618-623. https://doi.org/10.3201/eid1204.051379
Bernard, K. A., Maffei, J. G., Jones, S. A., Kauffman, E. B., Ebel, G., Dupuis, A. P. 2nd, … Shi, P.-Y. (2001). West Nile virus infection in birds and mosquitoes, New York State, 2000. Emerging Infectious Diseases, 7(4), 679. https://doi.org/10.3201/eid0704.010415
Boal, C. W., & Mannan, R. W. (1996). Prey sizes of male and female northern goshawks. The Southwestern Naturalist, 41, 355-358.
Burkett-Cadena, N. D., Bingham, A. M., & Unnasch, T. R. (2014). Sex-biased avian host use by arbovirus vectors. Royal Society Open Science, 1(3), 140262. https://doi.org/10.1098/rsos.140262
Burkett-Cadena, N. D., Ligon, R. A., Liu, M., Hassan, H. K., Hill, G. E., Eubanks, M. D., & Unnasch, T. R. (2010). Vector-host interactions in avian nests: Do mosquitoes prefer nestlings over adults? The American Journal of Tropical Medicine and Hygiene, 83(2), 395-399. https://doi.org/10.4269/ajtmh.2010.10-0048
Busquets, N., Laranjo-González, M., Soler, M., Nicolás, O., Rivas, R., Talavera, S., … Aranda, C. (2019). Detection of West Nile virus lineage 2 in North-Eastern Spain (Catalonia). Transboundary and Emerging Diseases, 66(2), 617-621. https://doi.org/10.1111/tbed.13086
Caffrey, C., Smith, S. C. R., & Weston, T. J. (2005). West Nile virus devastates an American crow population. The Condor, 107(1), 128-132. https://doi.org/10.1650/7646
Centers for Disease Control and Prevention (1999-2016). Species of dead birds in which West Nile virus has been detected, United States, 1999-2016. Retrieved from https://www.cdc.gov/westnile/resources/pdfs/BirdSpecies1999-2016.pdf
Chowers, M. Y., Lang, R., Nassar, F., Ben-David, D., Giladi, M., Rubinshtein, E., … Kitzes, R. (2001). Clinical characteristics of the West Nile fever outbreak, Israel, 2000. Emerging Infectious Diseases, 7(4), 675. https://doi.org/10.3201/eid0704.017414
Cozzarolo, C.-S., Sironi, N., Glaizot, O., Pigeault, R., & Christe, P. (2019). Sex-biased parasitism in vector-borne disease: Vector preference? PLoS One, 14(5), e0216360. https://doi.org/10.1371/journal.pone.0007861
Csank, T., Bhide, K., Bencurova, E., Dolinska, S., Drzewniokova, P., Major, P., … Pistl, J. (2016). Detection of West Nile virus and tick-borne encephalitis virus in birds in Slovakia, using a universal primer set. Archives of Virology, 161(6), 1679-1683. https://doi.org/10.1007/s00705-016-2828-5
D'Agostino, J. J., & Isaza, R. (2004). Clinical signs and results of specific diagnostic testing among captive birds housed at zoological institutions and infected with West Nile virus. Journal of the American Veterinary Medical Association, 224(10), 1640-1643, 1606. https://doi.org/10.2460/javma.2004.224.1640
Egizi, A. M., Farajollahi, A., & Fonseca, D. M. (2014). Diverse host feeding on nesting birds may limit early-season West Nile virus amplification. Vector Borne and Zoonotic Diseases, 14(6), 447-453. https://doi.org/10.1089/vbz.2013.1536
Eiden, M., Vina-Rodriguez, A., Hoffmann, B., Ziegler, U., & Groschup, M. H. (2010). Two new real-time quantitative reverse transcription polymerase chain reaction assays with unique target sites for the specific and sensitive detection of lineages 1 and 2 West Nile virus strains. Journal of Veterinary Diagnostic Investigation, 22(5), 748-753. https://doi.org/10.1177/104063871002200515
Erdelyi, K., Ursu, K., Ferenczi, E., Szeredi, L., Ratz, F., Skare, J., & Bakonyi, T. (2007). Clinical and pathologic features of lineage 2 West Nile virus infections in birds of prey in Hungary. Vector Borne and Zoonotic Diseases, 7(2), 181-188. https://doi.org/10.1089/vbz.2006.0586
Friedrich-Loeffler-Institut (2019a, October 7). Erster Fall von West-Nil-Virus Infektion 2019 [Press release]. Retrieved from https://www.fli.de/en/news/short-messages/short-message/erster-fall-von-west-nil-virus-infektion-2019/
Friedrich-Loeffler-Institut (2019b, September 12). Weitere Ausbreitung des West-Nil-Virus: Fünf Infektionen bei Pferden und erhöhte Fallzahlen bei Vögeln festgestellt [Press release]. Retrieved from https://www.fli.de/de/presse/pressemitteilungen/presse-einzelansicht/weitere-ausbreitung-des-west-nil-virus-fuenf-infektionen-bei-pferden-und-erhoehte-fallzahlen-bei-voege/
Gancz, A. Y., Barker, I. K., Lindsay, R., Dibernardo, A., McKeever, K., & Hunter, B. (2004). West Nile virus outbreak in north American owls, Ontario, 2002. Emerging Infectious Diseases, 10(12), 2135. https://doi.org/10.3201/eid1012.040167
Garmendia, A. E., Van Kruiningen, H. J., French, R. A., Anderson, J. F., Andreadis, T. G., Kumar, A., & West, A. B. (2000). Recovery and identification of West Nile virus from a hawk in winter. Journal of Clinical Microbiology, 38(8), 3110-3111. https://doi.org/10.1128/JCM.38.8.3110-3111.2000
Garvin, M. C., Austin, A., Boyer, K., Gefke, M., Wright, C., Pryor, Y., … Whelan, R. J. (2018). Attraction of Culex pipiens to house sparrows is influenced by host age but not uropygial gland secretions. Insects, 9(4), 127. https://doi.org/10.3390/insects9040127
George, T. L., Harrigan, R. J., LaManna, J. A., DeSante, D. F., Saracco, J. F., & Smith, T. B. (2015). Persistent impacts of West Nile virus on North American bird populations. Proceedings of the National Academy of Sciences, 112(46), 14290-14294. https://doi.org/10.1073/pnas.1507747112
Heym, E. C., Kampen, H., Krone, O., Schäfer, M., & Werner, D. (2019). Molecular detection of vector-borne pathogens from mosquitoes collected in two zoological gardens in Germany. Parasitology Research, 118(7), 2097-2105. https://doi.org/10.1007/s00436-019-06327-5
Hubalek, Z., Kosina, M., Rudolf, I., Mendel, J., Strakova, P., & Tomesek, M. (2018). Mortality of goshawks (Accipiter gentilis) due to West Nile virus lineage 2. Vector Borne and Zoonotic Diseases, 18(11), 624-627. https://doi.org/10.1089/vbz.2018.2289
Hubálek, Z., Tomešek, M., Kosina, M., Šikutová, S., Straková, P., & Rudolf, I. (2019). West Nile virus outbreak in captive and wild raptors, Czech Republic, 2018. Zoonoses and Public Health, 66(8), 978-981. https://doi.org/10.1111/zph.12638
Jansen, S., Heitmann, A., Lühken, R., Leggewie, M., Helms, M., Badusche, M., … Tannich, E. (2019). Culex torrentium: A potent vector for the transmission of West Nile virus in Central Europe. Viruses, 11(6), 492. https://doi.org/10.3390/v11060492
Johnson, N., Fernández de Marco, M., Giovannini, A., Ippoliti, C., Danzetta, M., Svartz, G., … Mirazimi, A. (2018). Emerging mosquito-borne threats and the response from European and Eastern Mediterranean Countries. International Journal of Environmental Research and Public Health, 15(12), 2775. https://doi.org/10.3390/ijerph15122775
Jöst, H., Bialonski, A., Maus, D., Sambri, V., Eiden, M., Groschup, M. H., … Schmidt-Chanasit, J. (2011). Isolation of Usutu virus in Germany. The American Journal of Tropical Medicine and Hygiene, 85(3), 551-553. https://doi.org/10.4269/ajtmh.2011.11-0248
Joyner, P. H., Kelly, S., Shreve, A. A., Snead, S. E., Sleeman, J. M., & Pettit, D. A. (2006). West Nile virus in raptors from Virginia during 2003: Clinical, diagnostic, and epidemiologic findings. Journal of Wildlife Diseases, 42(2), 335-344. https://doi.org/10.7589/0090-3558-42.2.335
Kampen, H., Holicki, C. M., Ziegler, U., Groschup, M. H., Tews, B. A., & Werner, D. (2020). West Nile virus mosquito vectors (Diptera: Culicidae) in Germany. Viruses, 12(5), 493. https://doi.org/10.3390/v12050493
Kenward, R., Marcström, V., & Karlbom, M. (1999). Demographic estimates from radio-tagging: Models of age-specific survival and breeding in the goshawk. Journal of Animal Ecology, 68(5), 1020-1033. https://doi.org/10.1046/j.1365-2656.1999.00347.x
Komar, N., Langevin, S., Hinten, S., Nemeth, N., Edwards, E., Hettler, D., … Bunning, M. (2003). Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerging Infectious Diseases, 9(3), 311. https://doi.org/10.3201/eid0903.020628
Kramer, L. D., & Bernard, K. A. (2001). West Nile virus infection in birds and mammals. Annals of the New York Academy of Sciences, 951, 84-93. https://doi.org/10.1111/j.1749-6632.2001.tb02687.x
Leggewie, M., Badusche, M., Rudolf, M., Jansen, S., Börstler, J., Krumkamp, R., … Tannich, E. (2016). Culex pipiens and Culex torrentium populations from Central Europe are susceptible to West Nile virus infection. One Health, 2, 88-94. https://doi.org/10.1016/j.onehlt.2016.04.001
Lopes, H., Redig, P., Glaser, A., Armien, A., & Wünschmann, A. (2007). Clinical findings, lesions, and viral antigen distribution in great gray owls (Strix nebulosa) and barred owls (Strix varia) with spontaneous West Nile virus infection. Avian Diseases, 51(1), 140-145. https://doi.org/10.1637/0005-2086(2007)051[0140:CFLAVA]2.0.CO;2
Mueller, H. C., Berger, D. D., & Allez, G. (1976). Age and sex variation in the size of goshawks. Bird-Banding, 47(4), 310-318. https://doi.org/10.2307/4512266
Müller, K. (2012). Untersuchungen zur Hämatologie, Blutchemie und dem Vitaminstoffwechsel frei lebender mitteleuropäischer Greifvögel. Berlin, Germany: University of Berlin. (Unpublished habilitation thesis).
Nemeth, N., Gould, D., Bowen, R., & Komar, N. (2006). Natural and experimental West Nile virus infection in five raptor species. Journal of Wildlife Diseases, 42(1), 1-13. https://doi.org/10.7589/0090-3558-42.1.1
Nemeth, N. M., Kratz, G. E., Bates, R., Scherpelz, J. A., Bowen, R. A., & Komar, N. (2009). Clinical evaluation and outcomes of naturally acquired West Nile virus infection in raptors. Journal of Zoo and Wildlife Medicine, 40(1), 51-63. https://doi.org/10.1638/2007-0109.1
Petrovic, T., Blazquez, A. B., Lupulovic, D., Lazic, G., Escribano-Romero, E., Fabijan, D., … Saiz, J. (2013). Monitoring West Nile virus (WNV) infection in wild birds in Serbia during 2012: First isolation and characterisation of WNV strains from Serbia. Eurosurveillance, 18(44), 20622. https://doi.org/10.2807/1560-7917.es2013.18.44.20622
Rappole, J. H., & Hubalek, Z. (2003). Migratory birds and West Nile virus. Journal of Applied Microbiology, 94, 47-58. https://doi.org/10.1046/j.1365-2672.94.s1.6.x
Reisen, W. K., Fang, Y., Lothrop, H. D., Martinez, V. M., Wilson, J., O’Connor, P., … Brault, A. C. (2014). Overwintering of West Nile virus in southern California. Journal of Medical Entomology, 43(2), 344-355. https://doi.org/10.1093/jmedent/43.2.344
Robert Koch-Institut. (2019, October 24). Epidemiologisches Bulletin [Press release]. Retrieved from https://www.rki.de/DE/Content/Infekt/EpidBull/Archiv/2019/Ausgaben/43_19.pdf?__blob=publicationFile
Savini, G., Puggioni, G., Di gennaro, A., Di francesco, G., Rocchigiani, A. M., Polci, A., … Monaco, F. (2013). West Nile virus lineage 2 in Sardinian wild birds in 2012: A further threat to public health. Epidemiology and Infection, 141(11), 2313-2316. https://doi.org/10.1017/S0950268812003147
Scheuch, D. E., Schäfer, M., Eiden, M., Heym, E. C., Ziegler, U., Walther, D., … Kampen, H. (2018). Detection of Usutu, Sindbis, and Batai viruses in mosquitoes (Diptera: Culicidae) collected in Germany, 2011-2016. Viruses, 10(7), 389. https://doi.org/10.3390/v10070389
Seidowski, D., Ziegler, U., Von Rönn, J. A., Müller, K., Hüppop, K., Müller, T., … Ulrich, R. G. (2010). West Nile virus monitoring of migratory and resident birds in Germany. Vector-Borne and Zoonotic Diseases, 10(7), 639-647. https://doi.org/10.1089/vbz.2009.0236
Sovada, M. A., Pietz, P. J., Converse, K. A., King, D. T., Hofmeister, E. K., Scherr, P., & Ip, H. S. (2008). Impact of West Nile virus and other mortality factors on American white pelicans at breeding colonies in the northern plains of North America. Biological Conservation, 141(4), 1021-1031. https://doi.org/10.1016/j.biocon.2008.01.019
Spedicato, M., Carmine, I., Bellacicco, A. L., Marruchella, G., Marini, V., Pisciella, M., … Savini, G. (2016). Experimental infection of rock pigeons (Columba livia) with three West Nile virus lineage 1 strains isolated in Italy between 2009 and 2012. Epidemiology and Infection, 144(6), 1301-1311. https://doi.org/10.1017/S0950268815002642
Steele, K. E., Linn, M. J., Schoepp, R. J., Komar, N., Geisbert, T. W., Manduca, R. M., … McNamara, T. S. (2000). Pathology of fatal West Nile virus infections in native and exotic birds during the 1999 outbreak in New York City, New York. Veterinary Pathology, 37(3), 208-224. https://doi.org/10.1354/vp.37-3-208
Swayne, D. E., Beck, J. R., Smith, C. S., Shieh, W.-J., & Zaki, S. R. (2001). Fatal encephalitis and myocarditis in young domestic geese (Anser anser domesticus) caused by West Nile virus. Emerging Infectious Diseases, 7(4), 751. https://doi.org/10.3201/eid0704.017429
Weissenböck, H., Hubálek, Z., Bakonyi, T., & Nowotny, N. (2010). Zoonotic mosquito-borne flaviviruses: Worldwide presence of agents with proven pathogenicity and potential candidates of future emerging diseases. Veterinary Microbiology, 140(3-4), 271-280. https://doi.org/10.1016/j.vetmic.2009.08.025
Wiens, J. D., Noon, B. R., & Reynolds, R. T. (2006). Post-fledging survival of northern goshawks: The importance of prey abundance, weather, and dispersal. Ecological Applications, 16(1), 406-418. https://doi.org/10.1890/04-1915
Wodak, E., Richter, S., Bago, Z., Revilla-Fernandez, S., Weissenbock, H., Nowotny, N., & Winter, P. (2011). Detection and molecular analysis of West Nile virus infections in birds of prey in the eastern part of Austria in 2008 and 2009. Veterinary Microbiology, 149(3-4), 358-366. https://doi.org/10.1016/j.vetmic.2010.12.012
Wünschmann, A., Shivers, J., Bender, J., Carroll, L., Fuller, S., Saggese, M., … Redig, P. (2004). Pathologic findings in red-tailed hawks (Buteo jamaicensis) and Cooper's hawks (Accipiter cooperi) naturally infected with West Nile virus. Avian Diseases, 48(3), 570-580. https://doi.org/10.1637/7170-022004R
Wünschmann, A., Shivers, J., Bender, J., Carroll, L., Fuller, S., Saggese, M., … Redig, P. (2005). Pathologic and immunohistochemical findings in goshawks (Accipiter gentilis) and great horned owls (Bubo virginianus) naturally infected with West Nile virus. Avian Diseases, 49(2), 252-259. https://doi.org/10.1637/7297-103104R
Yaremych, S. A., Levengood, J. M., Novak, R. J., Mankin, P. C., & Warner, R. E. (2004). Gender determination and lack of sex-specific West Nile virus mortality in American crows. Wildlife Society Bulletin, 32(3), 893-899. https://doi.org/10.2193/0091-7648(2004)032[0893:GDALOS]2.0.CO;2
Ziegler, U., Angenvoort, J., Fischer, D., Fast, C., Eiden, M., Rodriguez, A. V., … Groschup, M. H. (2013). Pathogenesis of West Nile virus lineage 1 and 2 in experimentally infected large falcons. Veterinary Microbiology, 161(3-4), 263-273. https://doi.org/10.1016/j.vetmic.2012.07.041
Ziegler, U., Luhken, R., Keller, M., Cadar, D., van der Grinten, E., Michel, F., … Groschup, M. H. (2019). West Nile virus epizootic in Germany, 2018. Antiviral Research, 162, 39-43. https://doi.org/10.1016/j.antiviral.2018.12.005
Ziegler, U., Santos, P., Groschup, M. H., Hattendorf, C., Eiden, M., Höper, D., Lühken, R. (2020). West Nile virus epidemic in Germany triggered by epizootic emergence, 2019. Viruses, 12(4), 448. https://doi.org/10.3390/v12040448