Pathogenesis and shedding of Usutu virus in juvenile chickens

References

• Kuno G, Chang G-JJ, Tsuchiya KR, et al. Phylogeny of the genus Flavivirus. J Virol. 1998;72(1):73–83.
   PubMed Web of Science ®Google Scholar
• Roesch F, Fajardo A, Moratorio G, et al. Usutu virus: an arbovirus on the rise. Viruses. 2019;11(7):640, 1–14.
   Web of Science ®Google Scholar
• Williams MC, Simpson DIH, Haddow AJ, et al. 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;58(3):367–374.
   PubMed Web of Science ®Google Scholar
• Cle M, Beck C, Salinas S, et al. Usutu virus: a new threat? Epidemiol Infect. 2019;147:e232, 1–11.
   PubMed Web of Science ®Google Scholar
• Fros JJ, Miesen P, Vogels CB, et al. Comparative Usutu and West Nile virus transmission potential by local Culex pipiens mosquitoes in north-western Europe. One Health. 2015;1:31–36.
   PubMed Web of Science ®Google Scholar
• Calzolari M, Gaibani P, Bellini R, et al. Mosquito, bird and human surveillance of West Nile and Usutu Viruses in Emilia-Romagna region (Italy) in 2010. PLOS ONE. 2012;7(5):e38058, 1–12.
   Web of Science ®Google Scholar
• 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;109(10):609–618.
   PubMed Web of Science ®Google Scholar
• Cadar D, Becker N, Campos Rde M, et al. Usutu virus in bats, Germany, 2013. Emerg Infect Dis. 2014;20(10):1771–1773.
   Web of Science ®Google Scholar
• Diagne MM, Ndione MHD, Di Paola N, et al. Usutu virus isolated from rodents in Senegal. Viruses. 2019;11(2):181, 1–13.
   Web of Science ®Google Scholar
• Garcia-Bocanegra I, Paniagua J, Gutierrez-Guzman AV, et al. Spatio-temporal trends and risk factors affecting West Nile virus and related flavivirus exposure in Spanish wild ruminants. BMC Vet Res. 2016;12(1):249, 1–9.
   Web of Science ®Google Scholar
• Durand B, Haskouri H, Lowenski S, et al. Seroprevalence of West Nile and Usutu viruses in military working horses and dogs, Morocco, 2012: dog as an alternative WNV sentinel species? Epidemiol Infect. 2016;144(9):1857–1864.
   Web of Science ®Google Scholar
• Percivalle E, Cassaniti I, Sarasini A, et al. West Nile or Usutu virus? A three-year follow-up of humoral and cellular response in a group of asymptomatic blood donors. Viruses. 2020;12(2):157, 1–11.
   Web of Science ®Google Scholar
• Carletti F, Colavita F, Rovida F, et al. Expanding Usutu virus circulation in Italy: detection in the lazio region, central Italy, 2017 to 2018. Eurosurveillance. 2019;24(3):1800649.
   Web of Science ®Google Scholar
• Nagy A, Mezei E, Nagy O, et al. Extraordinary increase in West Nile virus cases and first confirmed human Usutu virus infection in Hungary, 2018. Eurosurveillance. 2019;24(28):1900038.
   Web of Science ®Google Scholar
• Zaaijer HL, Slot E, Molier M, et al. Usutu virus infection in Dutch blood donors. Transfusion. 2019;59(9):2931–2937.
   Web of Science ®Google Scholar
• Caracciolo I, Mora-Cardenas E, Aloise C, et al. Comprehensive response to Usutu virus following first isolation in blood donors in the Friuli Venezia Giulia region of Italy: development of recombinant NS1-based serology and sensitivity to antiviral drugs. PLoS Negl Trop Dis. 2020;14(3):e0008156.
   Web of Science ®Google Scholar
• Pacenti M, Sinigaglia A, Martello T, et al. Clinical and virological findings in patients with Usutu virus infection, northern Italy, 2018. Eurosurveillance. 2019;24(47):1900180.
   Web of Science ®Google Scholar
• Weissenbock H, Kolodziejek J, Url A, et al. Emergence of Usutu virus, an African mosquito-borne flavivirus of the Japanese encephalitis virus group, central Europe. Emerg Infect Dis. 2002;8(7):652–656.
   PubMed Web of Science ®Google Scholar
• Weissenbock H, Bakonyi T, Rossi G, et al. Usutu virus, Italy, 1996. Emerg Infect Dis. 2013;19(2):274–277.
   PubMed Web of Science ®Google Scholar
• Luhken R, Jost H, Cadar D, et al. Distribution of Usutu virus in Germany and its effect on breeding bird populations. Emerg Infect Dis. 2017;23(12):1994–2001.
   Web of Science ®Google Scholar
• Rijks JM, Kik ML, Slaterus R, et al. Widespread Usutu virus outbreak in birds in the Netherlands, 2016. Euro Surveill. 2016;21(45):1–6.
   Google Scholar
• Chvala S, Bakonyi T, Bukovsky C, et al. Monitoring of Usutu virus activity and spread by using dead bird surveillance in Austria, 2003–2005. Vet Microbiol. 2007;122(3):237–245.
   Web of Science ®Google Scholar
• Steinmetz HW, Bakonyi T, Weissenböck H, et al. Emergence and establishment of Usutu virus infection in wild and captive avian species in and around Zurich, Switzerland—genomic and pathologic comparison to other central European outbreaks. Vet Microbiol. 2011;148(2):207–212.
   Web of Science ®Google Scholar
• Blazquez AB, Escribano-Romero E, Martin-Acebes MA, et al. Limited susceptibility of mice to Usutu virus (USUV) infection and induction of flavivirus cross-protective immunity. Virology. 2015;482:67–71.
   Web of Science ®Google Scholar
• Weissenbock H, Bakonyi T, Chvala S, et al. Experimental Usutu virus infection of suckling mice causes neuronal and glial cell apoptosis and demyelination. Acta Neuropathol. 2004;108(5):453–460.
   Web of Science ®Google Scholar
• Segura Guerrero NA, Sharma S, Neyts J, et al. Favipiravir inhibits in vitro Usutu virus replication and delays disease progression in an infection model in mice. Antiviral Res. 2018;160:137–142.
   PubMed Web of Science ®Google Scholar
• Martin-Acebes MA, Blazquez AB, Canas-Arranz R, et al. A recombinant DNA vaccine protects mice deficient in the alpha/beta interferon receptor against lethal challenge with Usutu virus. Vaccine. 2016;34(18):2066–2073.
   Web of Science ®Google Scholar
• Kuchinsky SC, Hawks SA, Mossel EC, et al. Differential pathogenesis of Usutu virus isolates in mice. PLoS Negl Trop Dis. 2020;14(10):e0008765, 1–15.
   Web of Science ®Google Scholar
• Chvala S, Bakonyi T, Hackl R, et al. Limited pathogenicity of Usutu virus for the domestic goose (Anser anser f. domestica) following experimental inoculation. J Vet Med B Infect Dis Vet Public Health. 2006;53(4):171–175.
   Google Scholar
• Chvala S, Bakonyi T, Hackl R, et al. Limited pathogenicity of Usutu virus for the domestic chicken (Gallus domesticus). Avian Pathol. 2005;34(5):392–395.
   PubMed Web of Science ®Google Scholar
• Benzarti E, Rivas J, Sarlet M, et al. Experimental Usutu virus infection in domestic canaries Serinus canaria. Viruses. 2020;12(2):1–14.
   Web of Science ®Google Scholar
• Chung YS. Viraemia and antibody response in chickens infected with arboviruses. J Comp Pathol. 1970;80(2):311-314.
   Web of Science ®Google Scholar
• Campbell J, Hore DE. Isolation of Murray Valley encephalitis virus from sentinel chickens. Aust Vet J. 1975;51(1):1–3.
   Web of Science ®Google Scholar
• Reisen WK, Lundstrom JO, Scott TW, et al. Patterns of avian Seroprevalence to western equine encephalomyelitis and Saint Louis encephalitis Viruses in California, USA. J Med Entomol. 2000;37(4):507–527.
   Web of Science ®Google Scholar
• Patiris PJ, Oceguera LF 3rd, Peck GW, et al. Serologic diagnosis of West Nile and St. Louis encephalitis virus infections in domestic chickens. Am J Trop Med Hyg. 2008;78(3):434–441.
   Web of Science ®Google Scholar
• Langevin SA, Bunning M, Davis B, et al. Experimental infection of chickens as candidate sentinels for West Nile virus. Emerg Infect Dis. 2001;7(4):726–729.
   PubMed Web of Science ®Google Scholar
• Styer LM, Bernard KA, Kramer LD. Enhanced early West Nile virus infection in young chickens infected by mosquito bite: effect of viral dose. Am J Trop Med Hyg. 2006;75(2):337–345.
   PubMed Web of Science ®Google Scholar
• Buckley A, Dawson A, Gould EA. Detection of seroconversion to West Nile virus, Usutu virus and sindbis virus in UK sentinel chickens. Virol J. 2006;3(1):71, 1–6.
   Web of Science ®Google Scholar
• Dridi M, Rauw F, Muylkens B, et al. Setting up a SPF chicken model for the pathotyping of West Nile virus (WNV) strains. Transbound Emerg Dis. 2013;60(Suppl 2):51–62.
   Web of Science ®Google Scholar
• Siegel PB, Gross WB. Production and persistence of antibodies in chickens to sheep erythrocytes. 1. Directional selection. Poult Sci. 1980;59(1):1–5.
   Web of Science ®Google Scholar
• Gross WG, Siegel PB, Hall RW, et al. Production and persistence of antibodies in chickens to sheep erythrocytes. 2. Resistance to infectious diseases. Poult Sci. 1980;59(2):205–210.
   Web of Science ®Google Scholar
• Lillie M, Sheng Z, Honaker CF, et al. Genome-wide standing variation facilitates long-term response to bidirectional selection for antibody response in chickens. BMC Genomics. 2017;18(1):99–99.
   Web of Science ®Google Scholar
• Vazquez A, Ruiz S, Herrero L, et al. West Nile and Usutu viruses in mosquitoes in Spain, 2008–2009. Am J Trop Med Hyg. 2011;85(1):178–181.
   Web of Science ®Google Scholar
• Mossel EC, Crabtree MB, Mutebi JP, et al. Arboviruses isolated from mosquitoes collected in Uganda, 2008–2012. J Med Entomol. 2017;54(5):1403–1409.
   Web of Science ®Google Scholar
• FAO. Chapter 5 Disease sampling procedures. In: Whitworth D, Newman S, Mundkur T, et al., editors. Wild birds and avian influenza: an introduction to applied field research and disease sampling techniques. FAO Animal Production and Health Manual 5th ed. Rome: FAO Animal Production and Health Manual; 2007.
   Google Scholar
• Duggal NK, Ritter JM, Pestorius SE, et al. Frequent zika virus sexual transmission and prolonged viral RNA shedding in an immunodeficient mouse model. Cell Rep. 2017;18(7):1751–1760.
   Web of Science ®Google Scholar
• Chvala S, Kolodziejek J, Nowotny N, et al. Pathology and viral distribution in fatal Usutu virus infections of birds from the 2001 and 2002 outbreaks in Austria. J Comp Pathol. 2004;131(2):176–185.
   Web of Science ®Google Scholar
• Manarolla G, Bakonyi T, Gallazzi D, et al. Usutu virus in wild birds in northern Italy. Vet Microbiol. 2010;141(1):159–163.
   Web of Science ®Google Scholar
• Komar N, Langevin S, Hinten S, et al. Experimental infection of north American birds with the New York 1999 strain of West Nile virus. Emerging Infect. Dis. 2003;9(3):311–322.
   PubMed Web of Science ®Google Scholar
• Banet-Noach C, Simanov L, Malkinson M. Direct (non-vector) transmission of West Nile virus in geese. Avian Pathol. 2003;32(5):489–494.
   Web of Science ®Google Scholar
• McLean RG, Ubico SR, Docherty DE, et al. West Nile virus transmission and ecology in birds. Ann NY Acad Sci. 2001;951:54–57.
   PubMed Web of Science ®Google Scholar
• Bowen GS, Monath TP, Kemp GE, et al. Geographic variation among St. Louis encephalitis virus strains in the viremic responses of avian hosts. Am J Trop Med Hyg. 1980;29(6):1411–1419.
   Web of Science ®Google Scholar
• Reisen WK, Fang Y, Martinez VM. Avian host and mosquito (Diptera: Culicidae) vector competence determine the efficiency of West Nile and St. Louis encephalitis virus transmission. J Med Entomol. 2005;42(3):367–375.
   Web of Science ®Google Scholar
• VanDalen KK, Hall JS, Clark L, et al. West Nile virus infection in American robins: new insights on dose response. PLOS ONE. 2013;8(7):e68537, 1–8.
   Web of Science ®Google Scholar
• Pérez-Ramírez E, Llorente F, Jiménez-Clavero MÁ. Experimental infections of wild birds with West Nile virus. Viruses. 2014;6(2):752–781.
   PubMed Web of Science ®Google Scholar
• Miller MM, Taylor RL Jr. Brief review of the chicken major histocompatibility complex: the genes, their distribution on chromosome 16, and their contributions to disease resistance. Poult Sci. 2016;95(2):375–392.
   PubMed Web of Science ®Google Scholar
• Nemeth NM, Oesterle PT, Bowen RA. Humoral immunity to West Nile virus is long-lasting and protective in the house sparrow (Passer domesticus). Am J Trop Med Hyg. 2009;80(5):864–869.
   Web of Science ®Google Scholar
• Panella NA, Young G, Komar N. Experimental infection of Eurasian collared-dove (Streptopelia decaocto) with West Nile virus. J Vector Ecol. 2013;38(2):210–214.
   Web of Science ®Google Scholar
• Newhouse DJ, Hofmeister EK, Balakrishnan CN. Transcriptional response to West Nile virus infection in the zebra finch (Taeniopygia guttata). R Soc Open Sci. 2017;4(6):170296–170296.
   Web of Science ®Google Scholar
• Colpitts TM, Conway MJ, Montgomery RR, et al. West Nile virus: biology, transmission, and human infection. Clin Microbiol Rev. 2012;25(4):635–648.
   PubMed Web of Science ®Google Scholar