Surveillance Potential of Non-Native Hawaiian Birds for Detection of West Nile Virus

Erik K. Hofmeister USGS National Wildlife Health Center, Madison, Wisconsin

Search for other papers by Erik K. Hofmeister in
Current site
Google Scholar
PubMed
Close
,
Robert J. Dusek USGS National Wildlife Health Center, Madison, Wisconsin

Search for other papers by Robert J. Dusek in
Current site
Google Scholar
PubMed
Close
, and
Christopher J. Brand USGS National Wildlife Health Center, Madison, Wisconsin

Search for other papers by Christopher J. Brand in
Current site
Google Scholar
PubMed
Close
Restricted access

West Nile virus (WNV) was first detected in North America in 1999. Alaska and Hawaii (HI) remain the only U.S. states in which transmission of WNV has not been detected. Dead bird surveillance has played an important role in the detection of the virus geographically, as well as temporally. In North America, corvids have played a major role in WNV surveillance; however, the only corvid in HI is the endangered Hawaiian crow that exists only in captivity, thus precluding the use of this species for WNV surveillance in HI. To evaluate the suitability of alternate avian species for WNV surveillance, we experimentally challenged seven abundant non-native bird species present in HI with WNV and compared mortality, viremia, oral shedding of virus, and seroconversion. For detection of WNV in oral swabs, we compared viral culture, reverse-transcriptase polymerase chain reaction, and the RAMP® test. For detection of antibodies to WNV, we compared an indirect and a competitive enzyme-linked immunoassay. We found four species (house sparrow, house finch, Japanese white-eye, and Java sparrow) that may be useful in dead bird surveillance for WNV; while common myna, zebra dove, and spotted dove survived infection and may be useful in serosurveillance.

Author Notes

* Address correspondence to Erik K. Hofmeister, USGS National Wildlife Health Center, 6006 Schroeder Road, Madison, WI 53711. E-mail: ehofmeister@usgs.gov

Financial support: This work was conducted with support from the Hawaii Department of Health and from the U.S. Fish and Wildlife Service.

Authors' addresses: Erik K. Hofmeister, Robert J. Dusek, and Christopher J. Brand, USGS National Wildlife Health Center, Madison, WI, E-mails: ehofmeister@usgs.gov, rdusek@usgs.gov, and cbrand@usgs.gov.

  • 1.

    Smithburn KC, Hughes TP, Burke AW, Paul JH, 1940. A neurotropic virus isolated from the blood of a native of Uganda. Am J Trop Med Hyg 20: 471492.

    • Search Google Scholar
    • Export Citation
  • 2.

    Gubler DJ, 2001. Human arbovirus infections worldwide. Ann N Y Acad Sci 951: 1324.

  • 3.

    Reiter P, 2010. West Nile virus in Europe: understanding the present to gauge the future. Euro Surveill 15: 19508.

  • 4.

    Sambri V, Capobianchi M, Charrel R, Fyodorova M, Gaibani P, Gould E, Niedrig M, Papa A, Pierro A, Rossini G, Varani S, Vocale C, Landini MP, 2013. West Nile virus in Europe: emergence, epidemiology, diagnosis, treatment, and prevention. Clin Microbiol Infect 19: 699704.

    • Search Google Scholar
    • Export Citation
  • 5.

    Kilpatrick AM, 2011. Globalization, land use, and the invasion of West Nile virus. Science 334: 323327.

  • 6.

    Hofmeister EK, 2011. West Nile virus: North American experience. Integr Zool 6: 279289.

  • 7.

    Reisen WK, 2013. Ecology of West Nile virus in North America. Viruses-Basel 5: 20792105.

  • 8.

    Petersen LR, Brault AC, Nasci RS, 2013. West Nile virus: review of the literature. JAMA 310: 308315.

  • 9.

    Lindsey N, Lehman JA, Staples JE, Fischer M, 2014. West Nile virus and other arboviral diseases—United States, 2013. MMWR Morb Mortal Wkly Rep 24: 521526.

    • Search Google Scholar
    • Export Citation
  • 10.

    Leong MKH, Grace JK, 2009. Occurrence and distribution of mosquitoes (Diptera: Culicidae) of public health importance on the Island of Oahu. Proc Hawaii Entomol Soc 41: 5770.

    • Search Google Scholar
    • Export Citation
  • 11.

    Lapointe DA, Hofmeister EK, Atkinson CT, Porter RE, Dusek RJ, 2009. Experimental infection of Hawai'i 'amakihi (Hemignathus virens) with West Nile virus and competence of a co-occurring vector, Culex quinquefasciatus: potential impacts on endemic Hawaiian avifauna. J Wildl Dis 45: 257271.

    • Search Google Scholar
    • Export Citation
  • 12.

    Ahumada JA, Lapointe D, Samuel MD, 2004. Modeling the population dynamics of Culex quinquefasciatus (Diptera: Culicidae), along an elevational gradient in Hawaii. J Med Entomol 41: 11571170.

    • Search Google Scholar
    • Export Citation
  • 13.

    Benning TL, Lapointe D, Atkinson CT, Vitousek PM, 2002. Interactions of climate change with biological invasions and land use in the Hawaiian Islands: modeling the fate of endemic birds using a geographic information system. Proc Natl Acad Sci USA 99: 1424614249.

    • Search Google Scholar
    • Export Citation
  • 14.

    Woodworth BL, Atkinson CT, LaPointe DA, Hart PJ, Spiegel CS, Tweed EJ, Henneman C, LeBrun J, Denette T, DeMots R, Kozar KL, Triglia D, Lease D, Gregor A, Smith T, Duffy D, 2005. Host population persistence in the face of introduced vector-borne diseases: Hawaii amakihi and avian malaria. Proc Natl Acad Sci USA 102: 15311536.

    • Search Google Scholar
    • Export Citation
  • 15.

    Atkinson CT, LaPointe DA, 2009. Introduced avian diseases, climate change, and the future of Hawaiian honeycreepers. J Avian Med Surg 23: 5363.

    • Search Google Scholar
    • Export Citation
  • 16.

    Atkinson CT, Samuel MD, 2010. Avian malaria Plasmodium relictum in native Hawaiian forest birds: epizootiology and demographic impacts on 'apapane Himatione sanguinea. J Avian Biol 41: 357366.

    • Search Google Scholar
    • Export Citation
  • 17.

    Kilpatrick MA, Gluzberg Y, Burgett J, Daszak P, 2004. Quantitative risk assessment of the pathways by which West Nile virus could reach Hawaii. EcoHealth 1: 205209.

    • Search Google Scholar
    • Export Citation
  • 18.

    Centers for Disease Control and Prevention, 2013. West Nile virus in the United States: Guidelines for Surveillance, Prevention, and Control Services. Fort Collins, CO: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention.

    • Search Google Scholar
    • Export Citation
  • 19.

    Barker CM, Kramer VL, Reisen WK, 2010. Decision Support System for Mosquito and Arbovirus Control in California. Available at: http://www.earthzine.org/2010/09/24/decision-support-system-for-mosquito-and-arbovirus-control-in-california.

    • Search Google Scholar
    • Export Citation
  • 20.

    Reisen WK, Wheeler SS, Garcia S, Fang Y, 2010. Migratory birds and the dispersal of arboviruses in California. Am J Trop Med Hyg 83: 808815.

  • 21.

    Styer LM, Kent KA, Albright RG, Bennett CJ, Kramer LD, Bernard KA, 2007. Mosquitoes inoculate high doses of West Nile virus as they probe and feed on live hosts. PLoS Pathog 3: 12621270.

    • Search Google Scholar
    • Export Citation
  • 22.

    Fassbinder-Orth CA, Hofmeister EK, Weeks-Levy C, Karasov WH, 2009. Oral and parenteral immunization of chickens (Gallus gallus) against West Nile virus with recombinant envelope protein. Avian Dis 53: 502509.

    • Search Google Scholar
    • Export Citation
  • 23.

    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: 40664071.

    • Search Google Scholar
    • Export Citation
  • 24.

    Beaty B, Calisher C, Shope R, 1989. Arboviruses. Schmidt N, Emmons R, eds. Diagnostic Procedures for Viral, Rickettsial and Chlamydial Infections. Washington, DC: American Public Health Association, 797855.

    • Search Google Scholar
    • Export Citation
  • 25.

    Blitvich BJ, Marlenee NL, Hall RA, Calisher CH, Bowen RA, Roehrig JT, Komar N, Langevin SA, Beaty BJ, 2003. Epitope-blocking enzyme-linked immunosorbent assays for the detection of serum antibodies to West Nile virus in multiple avian species. J Clin Microbiol 41: 10411047.

    • Search Google Scholar
    • Export Citation
  • 26.

    Ebel GD, Dupuis AP II, Nicholas D, Young D, Maffei J, Kramer LD, 2002. Detection by enzyme-linked immunosorbent assay of antibodies to West Nile virus in birds. Emerg Infect Dis 8: 979982.

    • Search Google Scholar
    • Export Citation
  • 27.

    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: 311322.

    • Search Google Scholar
    • Export Citation
  • 28.

    Lowry R, 2014. VassarStats: Web Site for Statistical Computation. Available at: http://faculty.vassar.edu/lowry/VassarStats.html. Accessed June 6, 2014.

    • Search Google Scholar
    • Export Citation
  • 29.

    Sovada MA, Pietz PJ, Converse KA, King DT, Hofmeister EK, Scherr P, Ip HS, 2008. Impact of West Nile virus and other mortality factors on American white pelicans at breeding colonies in the northern plains of North America. Biol Conserv 141: 10211031.

    • Search Google Scholar
    • Export Citation
  • 30.

    Sovada MA, Pietz PJ, Hofmeister EK, Bartos AJ, 2013. West Nile virus in American white pelican chicks: transmission, immunity, and survival. Am J Trop Med Hyg 88: 11521158.

    • Search Google Scholar
    • Export Citation
  • 31.

    Ip H, Van Wettere A, McFarlan L, Shearn-Bochsler V, Dickson SJB, Hatch G, Cavender K, Long R, Bodenstein B, 2014. West Nile virus transmission in winter: the 2013 Great Salt Lake bald eagle and eared grebes mortality event. PLOS Curr 18: 6.

    • Search Google Scholar
    • Export Citation
  • 32.

    Nemeth N, Young G, Ndaluka C, Bielefeldt-Ohmann H, Komar N, Bowen R, 2009. Persistent West Nile virus infection in the house sparrow (Passer domesticus). Arch Virol 154: 783789.

    • Search Google Scholar
    • Export Citation
  • 33.

    Fang Y, Reisen WK, 2006. Previous infection with West Nile or St. Louis encephalitis viruses provides cross protection during reinfection in house finches. Am J Trop Med Hyg 75: 480485.

    • Search Google Scholar
    • Export Citation
  • 34.

    Oesterle PT, Nemeth NM, VanDalen K, Sullivan H, Bentler KT, Young GR, McLean RG, Clark L, Smeraski C, Hall JS, 2009. Experimental Infection of cliff swallows (Petrochelidon pyrrhonota) with varying doses of West Nile virus. Am J Trop Med Hyg 81: 11591164.

    • Search Google Scholar
    • Export Citation
  • 35.

    Reisen WK, Fang Y, Martinez VM, 2005. Avian host and mosquito (Diptera: Culicidae) vector competence determine the efficiency of West Nile and St. Louis Encephalitis virus transmission. J Med Entomol 42: 367375.

    • Search Google Scholar
    • Export Citation
  • 36.

    VanDalen KK, Hall JS, Clark L, McLean RG, Smeraski C, 2013. West Nile virus infection in American robins: new insights on dose response. PLoS One 8: 18.

    • Search Google Scholar
    • Export Citation
  • 37.

    Owen J, Moore F, Panella N, Edwards E, Bru R, Hughes M, Komar N, 2006. Migrating birds as dispersal vehicles for West Nile virus. EcoHealth 3: 7985.

  • 38.

    Nemeth NM, Oesterle PT, Bowen RA, 2009. Humoral immunity to West Nile virus is long-lasting and protective in the house sparrow (Passer domesticus). Am J Trop Med Hyg 80: 864869.

    • Search Google Scholar
    • Export Citation
  • 39.

    Padgett KA, Cahoon-Young B, Carney R, Woods L, Read D, Husted S, Kramer V, 2006. Field and laboratory evaluation of diagnostic assays for detecting West Nile virus in oropharyngeal swabs from California wild birds. Vector Borne Zoonotic Dis 6: 183191.

    • Search Google Scholar
    • Export Citation
  • 40.

    Lord CC, Rutledge CR, Tabachnick WJ, 2006. Relationships between host viremia and vector susceptibility for arboviruses. J Med Entomol 43: 623630.

    • Search Google Scholar
    • Export Citation
  • 41.

    Sardelis MR, Turell MJ, Dohm DJ, O'Guinn ML, 2001. Vector competence of selected North American Culex and Coquillettidia mosquitoes for West Nile virus. Emerg Infect Dis 7: 10181022.

    • Search Google Scholar
    • Export Citation
  • 42.

    Turell MJ, Dohm DJ, Sardelis MR, O'Guinn ML, 2005. An update on the potential of North American mosquitoes (Diptera: Culicidae) to transmit West Nile virus. J Med Entomol 42: 5762.

    • Search Google Scholar
    • Export Citation
  • 43.

    Tiawsirisup S, Platt KB, Evans RB, Rowley WA, 2005. A comparision of West Nile virus transmission by Ochlerotatus trivttatus (Coq.), Culex pipiens (L.), and Aedes albopictus (Skuse). Vector Borne Zoonotic Dis 5: 4047.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 26 26 7
Full Text Views 297 120 0
PDF Downloads 44 4 0
 
Membership Banner
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save