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Archives of Virology

, Volume 154, Issue 5, pp 783–789 | Cite as

Persistent West Nile virus infection in the house sparrow (Passer domesticus)

  • Nicole NemethEmail author
  • Ginger Young
  • Christina Ndaluka
  • Helle Bielefeldt-Ohmann
  • Nicholas Komar
  • Richard Bowen
Original Article

Abstract

Long-term persistence of West Nile virus (WNV) infection within vertebrate reservoir hosts is a potential mechanism for overwintering of this (and other) arbovirus(es) at temperate latitudes. The house sparrow (Passer domesticus), an established amplifying host for WNV and other arboviruses, was used as a model to confirm chronicity of WNV infection in passerine birds and to evaluate the feasibility of two overwintering mechanisms: blood-borne infection of arthropod vectors (recrudescence) and oral infection of vertebrate reservoir hosts (ingestion of infected tissues through predation). WNV-inoculated sparrows were monitored for persistent infection for up to 2 years. Infectious virus persisted in tissues through 43 days, but not in sera beyond 6 days. Viral RNA persisted in tissues through 65 days. Chronicity of WNV infection in some tissues, but not blood, supports the predation mechanism of WNV overwintering, but not recrudescence. RNA persistence impacts interpretation and etiologic determination of avian mortality.

Keywords

West Nile Virus House Sparrow West Nile Virus Infection Cloacal Swab Oral Swab 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We are grateful to P. Gordy, A. Bosco-Lauth, K. Jones, P. Oesterle, N. Roberts and others for logistical support. K. Burkhalter provided advice on RT-PCR and R. McLean provided editorial comments. This research was funded by National Institutes of Health contract N01-AI25489, Emerging Infectious Viral Disease Unit.

References

  1. 1.
    Anderson JF, Main AJ (2006) Importance of vertical and horizontal transmission of West Nile virus by Culex pipiens in the Northeastern United States. J Infect Dis 194:1577–1579PubMedCrossRefGoogle Scholar
  2. 2.
    Austgen LE, Bowen R, Bunning ML, Davis BS, Mitchell CJ, Chang G-JJ (2004) Experimental infection of cats and dogs with West Nile virus. Emerg Infect Dis 10:82–86PubMedGoogle Scholar
  3. 3.
    Beaty BJ, Calisher CH, Shope RE (1995) Arboviruses. In: Lennette EH, Lennette DA, Lennette ET (eds) Diagnostic procedures for viral, rickettsial, and chlamydial infections, 7th edn. American Public Health Association, Washington, pp 189–212Google Scholar
  4. 4.
    Bolling BG, Moore CG, Anderson SL, Blair CD, Beaty BJ (2007) Entomological studies along the Colorado front range during a period of intense West Nile virus activity. J Am Mosq Control Assoc 23:37–46PubMedCrossRefGoogle Scholar
  5. 5.
    Bunning ML, Bowen RA, Cropp CB, Sullivan KG, Davis BS, Komar N, Godsey MS, Baker D, Hettler DL, Holmes DA, Biggerstaff BJ, Mitchell CJ (2002) Experimental infection of horses with West Nile virus. Emerg Infect Dis 8:380–386PubMedGoogle Scholar
  6. 6.
    Dawson JR, Stone WB, Ebel GD, Young DS, Galinski DS, Pensabene JP, Franke MA, Eidson M, Kramer LD (2007) Crow deaths caused by West Nile virus during winter. Emerg Infect Dis 13:1912–1914PubMedGoogle Scholar
  7. 7.
    Diamond MS, Shrestha B, Mehlhop E, Sitati E, Engle M (2003) Innate and adaptive immune responses determine protection against disseminated infection by West Nile encephalitis virus. Viral Immunol 16:259–278PubMedCrossRefGoogle Scholar
  8. 8.
    Farajollahi A, Crans WJ, Bryant P, Wolf B, Burkhalter KL, Godsey MS, Aspen SE, Nasci RS (2005) Detection of West Nile viral RNA from an overwintering pool of Culex pipiens pipiens (Diptera: Culicidae) in New Jersey, 2003. J Med Entomol 42:490–494PubMedCrossRefGoogle Scholar
  9. 9.
    Fedorova TN, Stavskiy AV (1972) Latent infection of wild ducks with Omsk hemorrhagic fever and West Nile viruses. In: Chumakov MP (ed) Aktualnye problemy virusologii i profilaktiki virusnykh zabolevaniy. Institute of Poliomyelitis Virus and Encephalitis AMN SSSR, Moscow, p 226 (in Russian)Google Scholar
  10. 10.
    Garmendia AE, Van Kruiningen HJ, French RA, Anderson JF, Andreadis TG, Kumar A, West B (2000) Recovery and identification of West Nile virus from a hawk in winter. J Clin Microbiol 38:3110–3111PubMedGoogle Scholar
  11. 11.
    Gerhold RW, Tate CM, Gibbs SE, Mead DG, Allison AB, Fischer JR (2007) Necropsy findings and arbovirus surveillance in mourning doves from the southeastern United States. J Wildl Dis 43:129–135PubMedGoogle Scholar
  12. 12.
    Godsey MS, Blackmore MS, Panella NA, Burkhalter K, Gottfried K, Halsey LA, Rutledge R, Langevin SA, Gates R, Lamonte KM, Lambert A, Lanciotti RS, Blackmore CGM, Loyless T, Stark L, Oliveri R, Conti L, Komar N (2005) West Nile virus epizootiology in the southeastern United States, 2001. Vector Borne Zoonotic Dis 5:82–89PubMedCrossRefGoogle Scholar
  13. 13.
    Klenk K, Snow J, Morgan K, Bowen R, Stephens M, Foster F, Gordy P, Beckett S, Komar N, Gubler D, Bunning M (2004) Alligators as West Nile virus amplifiers. Emerg Infect Dis 10:2150–2155PubMedGoogle Scholar
  14. 14.
    Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, Davis B, Bowen R, Bunning M (2003) Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis 9:311–322PubMedGoogle Scholar
  15. 15.
    Komar N, Panella NA, Burns JE, Dusza SW, Mascarenhas TM, Talbot TO (2001) Serologic evidence for West Nile virus infection in birds in the New York City vicinity during an outbreak in 1999. Emerg Infect Dis 7:621–625PubMedCrossRefGoogle Scholar
  16. 16.
    Komar N, Panella NA, Langevin SA, Brault AC, Amador M, Edwards E, Owen JC (2005) Avian hosts for West Nile virus in St. Tammany Parish, Louisiana, 2002. Am J Trop Med Hyg 73:1031–1037PubMedGoogle Scholar
  17. 17.
    Kruszewicz AG (1995) The epizootic role of the house sparrow (Passer domesticus) and the tree sparrow (Passer montanus). Literature Review. In: Pinowski J, Kavanagh BP, Pinowska B (eds) Nestling mortality of granivorous birds due to microorganisms and toxic substances: Synthesis. Polish Scientific Publishers, Warsaw, pp 339–351Google Scholar
  18. 18.
    Kuno G (2001) Persistence of arboviruses and antiviral antibodies in vertebrate hosts: its occurrence and impacts. Rev Med Virol 11:165–190PubMedCrossRefGoogle Scholar
  19. 19.
    Lanciotti RS, Kerst AJ, Nasci RS, Godsey MS, Mitchell CJ, Savage HM, Komar N, Panella NA, Allen BC, Volpe KE, Davis BS, Roehrig JT (2000) Rapid detection of West Nile virus from human clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay. J Clin Microbiol 38:4066–4071PubMedGoogle Scholar
  20. 20.
    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 Dis 51:140–145PubMedCrossRefGoogle Scholar
  21. 21.
    Miura TA, Travanty EA, Oko L, Bielefeldt-Ohmann H, Weiss S, Beauchemin N, Holmes KV (2008) The spike glycoprotein of murine coronavirus MHV-JHM mediates receptor-independent infection and spread in the central nervous system of Ceacam1a −/− mice. J Virol 82:755–763PubMedCrossRefGoogle Scholar
  22. 22.
    Nasci RS, Savage HM, White DJ, Miller JR, Cropp BC, Godsey MS, Kerst AJ, Bennett P, Gottfried K, Lanciotti RS (2001) West Nile virus in overwintering Culex mosquitoes, New York City, 2000. Emerg Infect Dis 7:1–3CrossRefGoogle Scholar
  23. 23.
    Nemeth NM, Beckett S, Edwards E, Klenk K, Komar N (2007) Avian mortality surveillance for West Nile virus in Colorado. Am J Trop Med Hyg 76:431–437PubMedGoogle Scholar
  24. 24.
    Nemeth N, Gould D, Bowen R, Komar N (2006) Natural and experimental West Nile virus infection in five raptor species. J Wildl Dis 42:1–13PubMedGoogle Scholar
  25. 25.
    Nemeth NM, Kratz GE, Bates R, Scherpelz JA, Bowen RA, Komar N (2008) Naturally induced humoral immunity to West Nile virus infection in raptors. Ecohealth 5:298–304PubMedCrossRefGoogle Scholar
  26. 26.
    Peiris JSM, Amerasinghe FP (1994) West Nile fever. In: Beran GW, Steele JH (eds) Handbook of zoonoses, section B. viral, 2nd edn. CRC Press, Boca Raton, pp 139–148Google Scholar
  27. 27.
    Phillips RA, Christensen K (2006) Field-caught Culex erythrothorax larvae found naturally infected with West Nile virus in Grand County, Utah. J Mosq Control Assoc 22:561–562CrossRefGoogle Scholar
  28. 28.
    Pogodina VV, Frolova MP, Malenko GV, Fokina GI, Koreshkova GV, Kiseleva LL, Bochkova NG, Ralph NM (1983) Study on West Nile virus persistence in monkeys. Arch Virol 75:71–86PubMedCrossRefGoogle Scholar
  29. 29.
    Reeves WC (1990) Overwintering of arboviruses. In: Reeves WC (ed) Epidemiology and control of mosquito-borne arboviruses in California, 1943–1987. California Mosquito and Vector Control Association, Sacramento, pp 357–382Google Scholar
  30. 30.
    Reisen WK, Chiles RE, Green EN, Fang Y, Mahmood F (2003) Previous infection protects house finches from re-infection with St. Louis encephalitis virus. J Med Entomol 40:300–305PubMedCrossRefGoogle Scholar
  31. 31.
    Reisen WK, Chiles RE, Martinez V, Fang Y, Green E, Clark S (2004) Effect of dose on house finch infection with Western equine encephalomyelitis and St. Louis encephalitis viruses. J Med Entomol 41:978–981PubMedCrossRefGoogle Scholar
  32. 32.
    Reisen WK, Fang Y, Lothrop HD, Martinez VM, Wilson J, O’Connor P, Carney R, Cahoon-Young B, Shafii M, Brault A (2006) Overwintering of West Nile virus in southern California. J Med Entomol 43:344–355PubMedCrossRefGoogle Scholar
  33. 33.
    Reisen WK, Kramer LD, Chiles RE, Green E-GN, Martinez VM (2001) Encephalitis virus persistence in California birds: preliminary studies with house finches. J Med Entomol 38:393–399PubMedCrossRefGoogle Scholar
  34. 34.
    Semenov BF, Chunikhin SP, Karmysheva VI, Iakovleva NI (1973) Study of chronic forms of arbovirus infections in birds. 1. Experiments with West Nile, Sindbis, Bhandja and Sicilian mosquito fever viruses. Vestn Akad Med Nauk SSSR 28:79–83 (in Russian)PubMedGoogle Scholar
  35. 35.
    Shrestha B, Diamond MS (2004) Role of CD8+ T cells in control of West Nile virus infection. J Virol 78:8312–8321PubMedCrossRefGoogle Scholar
  36. 36.
    Taylor FM, Work TH, Hurlbut HS, Rizk F (1956) A study of the ecology of West Nile virus in Egypt. Am J Trop Med Hyg 5:579–620PubMedGoogle Scholar
  37. 37.
    Tesh RB, Parsons R, Siirin M, Randle Y, Sargent C, Guzman H, Wuithiranyagool T, Higgs S, Vanlandingham DL, Bala AA, Haas K, Zerinque B (2004) Year-round West Nile virus activity, Gulf Coast region, Texas and Louisiana. Emerg Infect Dis 10:1649–1652PubMedGoogle Scholar
  38. 38.
    Tesh RB, Siirin M, Guzman H, Travassos da Rosa APA, Wu X, Duan T, Lei H, Nunes MR, Xiao S-Y (2005) Persistent West Nile virus infection in the golden hamster: studies on its mechanism and possible implications for other flavivirus infections. J Infect Dis 192:287–295PubMedCrossRefGoogle Scholar
  39. 39.
    Yaremych SA, Warner RE, Mankin PC, Brawn JD, Raim A, Novak R (2004) West Nile virus and high death rate in American crows. Emerg Infect Dis 10:709–711PubMedGoogle Scholar

Copyright information

© US Government 2009

Authors and Affiliations

  • Nicole Nemeth
    • 1
    • 2
    Email author
  • Ginger Young
    • 3
  • Christina Ndaluka
    • 2
  • Helle Bielefeldt-Ohmann
    • 2
  • Nicholas Komar
    • 3
  • Richard Bowen
    • 4
  1. 1.National Wildlife Research CenterFort CollinsUSA
  2. 2.Department of Microbiology, Immunology and PathologyColorado State UniversityFort CollinsUSA
  3. 3.Division of Vector-Borne Infectious DiseasesCenters for Disease Control and PreventionFort CollinsUSA
  4. 4.Department of Biomedical SciencesColorado State UniversityFort CollinsUSA

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