Advertisement

Archives of Virology

, Volume 158, Issue 4, pp 735–752 | Cite as

West Nile virus associations in wild mammals: a synthesis

  • J. Jeffrey RootEmail author
Brief Review

Abstract

Exposures to West Nile virus (WNV) have been documented in a variety of wild mammals in both the New and Old Worlds. This review tabulates at least 100 mammal species with evidence of WNV exposure. Many of these exposures were detected in free-ranging mammals, while several were noted in captive individuals. In addition to exposures, this review discusses experimental infections in terms of the potential for reservoir competence of select wild mammal species. Overall, few experimental infections have been conducted on wild mammals. As such, the role of most wild mammals as potential amplifying hosts for WNV is, to date, uncertain. In most instances, experimental infections of wild mammals with WNV have resulted in no or low-level viremia. Some recent studies have indicated that certain species of tree squirrels (Sciurus spp.), eastern chipmunks (Tamias striatus), and eastern cottontail rabbits (Sylvilagus floridanus) develop viremia sufficient for infecting some mosquito species. Certain mammalian species, such as tree squirrels, mesopredators, and deer have been suggested as useful species for WNV surveillance. In this review article, the information pertaining to wild mammal associations with WNV is synthesized.

Keywords

West Nile Virus West Nile Virus Infection Wild Mammal Tree Squirrel Eastern Chipmunk 
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

I thank K. Bentler and R. McLean for excellent reviews of an earlier version of this manuscript, and A. Lavelle for assistance in obtaining literature. The opinions and conclusions of this article are those of the author and do not necessarily represent those of the U.S. Department of Agriculture.

References

  1. 1.
    Abdel-Wahab KS, Imam IZ (1970) Antibodies to arboviruses in rodent sera. J Egypt Public Health Assoc 45:370–375PubMedGoogle Scholar
  2. 2.
    Akov Y, Goldwasser R (1966) Prevalence of antibodies to arboviruses in various animals in Israel. Bull World Health Organ 34:901–909PubMedGoogle Scholar
  3. 3.
    Andral L, Brès P, Sérié C, Casals J, Panthier R (1968) Etudes sur la fièvre jaune en Ethiopie. 3. Etude sérologique et virologique de la faune sylvatique. Bull World Health Organ 38:855–861PubMedGoogle Scholar
  4. 4.
    Austgen LE, Bowen RA, Bunning ML, Davis BS, Mitchell CJ, Chang GJJ (2004) Experimental infection of cats and dogs with West Nile virus. Emerg Infect Dis 10:82–86PubMedCrossRefGoogle Scholar
  5. 5.
    Bakonyi T, Ivanics É, Erdélyi K, Ursu K, Ferenczi E, Weissenböck H, Nowotny N (2006) Lineage 1 and 2 strains of encephalitic West Nile virus, Central Europe. Emerg Infect Dis 12:618–623PubMedCrossRefGoogle Scholar
  6. 6.
    Bentler KT, Hall JS, Root JJ, Klenk K, Schmit B, Blackwell BF, Ramey PC, Clark L (2007) Serologic evidence of West Nile virus exposure in North American mesopredators. Am J Trop Med Hyg 76:173–179PubMedGoogle Scholar
  7. 7.
    Blitvich BJ (2008) Transmission dynamics and changing epidemiology of West Nile virus. Anim Health Res Rev 9:71–86PubMedCrossRefGoogle Scholar
  8. 8.
    Blitvich BJ, Juarez LI, Tucker BJ, Rowley WA, Platt KB (2009) Antibodies to West Nile virus in raccoons and other wild peridomestic mammals in Iowa. J Wildl Dis 45:1163–1168PubMedGoogle Scholar
  9. 9.
    Bowen RA, Nemeth NM (2007) Experimental infections with West Nile virus. Curr Opin Infect Dis 20:293–297PubMedCrossRefGoogle Scholar
  10. 10.
    Brault AC, Langevin SA, Bowen RA, Panella NA, Biggerstaff BJ, Miller BR, Komar N (2004) Differential virulence of West Nile strains for American crows. Emerg Infect Dis 10:2161–2168PubMedCrossRefGoogle Scholar
  11. 11.
    Bunde JM, Heske EJ, Mateus-Pinilla NE, Hofmann JE, Novak RJ (2006) A survey for West Nile virus in bats from Illinois. J Wildl Dis 42:455–458PubMedGoogle Scholar
  12. 12.
    Bunning ML, Bowen RA, Bruce Cropp C, 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 8:380–386PubMedCrossRefGoogle Scholar
  13. 13.
    Chastel C, Rogues G, Beaucournu-Saguez F (1977) Enquête séro-épidémiologique mixte arbovirus-arénavirus chez les petits mammifères de Tunisie. Bull Soc Pathol Exot Filiales 70:471–479PubMedGoogle Scholar
  14. 14.
    Chastel C, Launay H, Rogues G, Beaucournu JC (1980) Infections à arbovirus en Espagne: enquête sérologique chez les petits mammifères. Bull Soc Pathol Exot Filiales 73:384–390PubMedGoogle Scholar
  15. 15.
    Chastel C, Launay H, Bailly Choumara H (1982) Infections à arbovirus au Maroc: sondage sérologique chez les petis mammifères du nord du pays. Bull Soc Pathol Exot Filiales 75:466–475PubMedGoogle Scholar
  16. 16.
    Chippaux-Hyppolite C, Chippaux A (1969) Contribution à l’étude d’un réservoir de virus animal dans le cycle de certains arbovirus en Centrafrique. I. Etude immunologique chez divers animaux domestiques et sauvages. Bull Soc Pathol Exot Filiales 62:1034–1045PubMedGoogle Scholar
  17. 17.
    Clerc Y, Rodhain F, Digoutte JP, Albignac R, Coulanges P (1982) Le programme exploratoire arbovirus de l’Institut Pasteur de Madagascar: bilan 1976–1980. Arch Inst Pasteur Madagascar 49:65–78PubMedGoogle Scholar
  18. 18.
    Cohen JK, Kilpatrick AM, Stroud FC, Paul K, Wolf F, Else JG (2007) Seroprevalence of West Nile virus in nonhuman primates as related to mosquito abundance at two national primate research centers. Comp Med 57:115–119PubMedGoogle Scholar
  19. 19.
    Darwish MA, Hoogstraal H, Roberts TJ, Ahmed IP, Omar F (1983) A sero-epidemiological survey for certain arboviruses (Togaviridae) in Pakistan. Trans R Soc Trop Med Hyg 77:442–445PubMedCrossRefGoogle Scholar
  20. 20.
    Davis A, Bunning M, Gordy P, Panella N, Blitvich B, Bowen R (2005) Experimental and natural infection of North American bats with West Nile virus. Am J Trop Med Hyg 73:467–469PubMedGoogle Scholar
  21. 21.
    Dietrich G, Montenieri JA, Panella NA, Langevin S, Lasater SE, Klenk K, Kile JC, Komar N (2005) Serologic evidence of West Nile virus infection in free-ranging mammals, Slidell, Louisiana, 2002. Vector Borne Zoonotic Dis 5:288–292PubMedCrossRefGoogle Scholar
  22. 22.
    Docherty DE, Samuel MD, Nolden CA, Egstad KF, Griffin KM (2006) West Nile virus antibody prevalence in wild mammals, Southern Wisconsin. Emerg Infect Dis 12:1982–1984PubMedCrossRefGoogle Scholar
  23. 23.
    Docherty DE, Samuel MD, Egstad KF, Griffin KM, Nolden CA, Karwal L, Ip HS (2009) Short report: changes in West Nile virus seroprevalence and antibody titers among Wisconsin mesopredators 2003–2006. Am J Trop Med Hyg 81:177–179PubMedGoogle Scholar
  24. 24.
    Drebot MA, Lindsay R, Barker IK, Buck PA, Fearon M, Hunter F, Sockett P, Artsob H (2003) West Nile virus surveillance and diagnostics: a Canadian perspective. Can J Infect Dis 14:105–114PubMedGoogle Scholar
  25. 25.
    Duca M, Duca E, Buiuc D, Luca V (1989) Studiul seroepidemiologic şi virologic al prezenţei unor arbovirusuri pe teritoriul Moldovei, 1961–1982. Rev Med Chir Soc Med Nat Iasi 93:719–733PubMedGoogle Scholar
  26. 26.
    Dutton CJ, Quinnell M, Lindsay R, Delay J, Barker IK (2009) Paraparesis in a polar bear (Ursus maritimus) associated with West Nile virus infection. J Zoo Wildl Med 40:568–571PubMedCrossRefGoogle Scholar
  27. 27.
    Farajollahi A, Panella NA, Carr P, Crans W, Burguess K, Komar N (2003) Serologic evidence of West Nile virus infection in black bears (Ursus americanus) from New Jersey. J Wildl Dis 39:894–896PubMedGoogle Scholar
  28. 28.
    Farajollahi A, Gates R, Crans W, Komar N (2004) Serologic evidence of West Nile virus and St. Louis encephalitis virus infections in white-tailed deer (Odocoileus virginianus) from New Jersey, 2001. Vector Borne Zoonotic Dis 4:379–383PubMedCrossRefGoogle Scholar
  29. 29.
    Farfán-Ale JA, Blitvich BJ, Marlenee NL, Loroño-Pino MA, Puerto-Manzano F, García-Rejón JE, Rosado-Paredes EP, Flores-Flores LF, Ortega-Salazar A, Chávez-Medina J, Cremieux-Grimaldi JC, Correa-Morales F, Hernández-Gaona G, Méndez-Galván JF, Beaty BJ (2006) Antibodies to West Nile virus in asymptomatic mammals, birds, and reptiles in the Yucatan Peninsula of Mexico. Am J Trop Med Hyg 74:908–914PubMedGoogle Scholar
  30. 30.
    Fontenille D, Rodhain F, Digoutte JP, Mathiot C, Morvan J, Coulanges P (1989) Les cycles de transmission du virus West-Nile à Madagascar, Océan Indien. Ann Soc Belg Med Trop 69:233–243PubMedGoogle Scholar
  31. 31.
    Franson JC, Hofmeister EK, Collins GH, Dusek RJ (2011) Short report: Seroprevalence of West Nile virus in feral horses on Sheldon National Wildlife Refuge, Nevada, United States. Am J Trop Med Hyg 84:637–640PubMedCrossRefGoogle Scholar
  32. 32.
    Gibbs SEJ, Marlenee NL, Romines J, Kavanaugh D, Corn JL, Stallknecht DE (2006) Antibodies to West Nile virus in feral swine from Florida, Georgia, and Texas, USA. Vector Borne Zoonotic Dis 6:261–265PubMedCrossRefGoogle Scholar
  33. 33.
    Gómez A, Kilpatrick AM, Kramer LD, Dupuis Ii AP, Maffei JG, Goetz SJ, Marra PP, Daszak P, Aguirre AA (2008) Land use and West Nile virus seroprevalence in wild mammals. Emerg Infect Dis 14:962–965PubMedCrossRefGoogle Scholar
  34. 34.
    Gómez A, Kramer LD, Dupuis Ii AP, Kilpatrick AM, Davis LJ, Jones MJ, Daszak P, Aguirre AA (2008) Experimental infection of eastern gray squirrels (Sciurus carolinensis) with West Nile virus. Am J Trop Med Hyg 79:447–451PubMedGoogle Scholar
  35. 35.
    Goverdhan MK, Kulkarni AB, Gupta AK, Tupe CD, Rodrigues JJ (1992) Two-way cross-protection between West Nile and Japanese encephalitis viruses in bonnet macaques. Acta Virol 36:277–283PubMedGoogle Scholar
  36. 36.
    Halouzka J, Juricova Z, Jankova J, Hubalek Z (2008) Serologic survey of wild boars for mosquito-borne viruses in South Moravia (Czech Republic). Vet Med (Praha) 53:266–271Google Scholar
  37. 37.
    Hayes CG, Baqar S, Ahmed T, Chowdhry MA, Reisen WK (1982) West Nile virus in Pakistan. 1. Sero-epidemiological studies in Punjab Province. Trans R Soc Trop Med Hyg 76:431–436PubMedCrossRefGoogle Scholar
  38. 38.
    Hayes CG (1988) West Nile Fever. In: Monath TP (ed) The Arboviruses: epidemiology and ecology. CRC Press, Boca Raton, pp 59–88Google Scholar
  39. 39.
    Heinz-Taheny KM, Andrews JJ, Kinsel MJ, Pessier AP, Pinkerton ME, Lemberger KY, Novak RJ, Dizikes GJ, Edwards E, Komar N (2004) West Nile virus infection in free-ranging squirrels in Illinois. J Vet Diagn Invest 16:186–190PubMedCrossRefGoogle Scholar
  40. 40.
    Henderson BE, Cheshire PP, Kirya GB, Lule M (1970) Immunologic studies with yellow fever and selected African group B arboviruses in rhesus and vervet monkeys. Am J Trop Med Hyg 19:110–118PubMedGoogle Scholar
  41. 41.
    Higgs S, Schneider BS, Vanlandingham DL, Klingler KA, Gould EA (2005) Nonviremic transmission of West Nile virus. Proc Natl Acad Sci USA 102:8871–8874PubMedCrossRefGoogle Scholar
  42. 42.
    Hukkanen RR, Liggitt HD, Kelley ST, Grant R, Anderson DM, Hall RA, Tesh RB, DaRosa APT, Bielefeldt-Ohmann H (2006) West Nile and St. Louis encephalitis virus antibody seroconversion, prevalence, and persistence in naturally infected pig-tailed macaques (Macaca nemestrina). Clin Vaccine Immunol 13:711–714PubMedCrossRefGoogle Scholar
  43. 43.
    Johnson BK, Chanas AC, Shockley P, Squires EJ, Gardner P, Wallace C, Simpson DIH, Bowen ETW, Platt GS, Way H, Parsons J, Grainger WE (1977) Arbovirus isolations from, and serological studies on, wild and domestic vertebrates from Kano Plain, Kenya. Trans R Soc Trop Med Hyg 71:512–517PubMedCrossRefGoogle Scholar
  44. 44.
    Juřicová Z (1992) Protilátky proti arbovirům u lovné zvěre odchycené na Moravě. Vet Med (Praha) 37:633–636Google Scholar
  45. 45.
    Juřicová Z, Hubálek Z (1999) Serological surveys for arboviruses in the game animals of southern Moravia (Czech Republic). Folia Zool 48:185–189Google Scholar
  46. 46.
    Karabatos N (ed) (1985) International catalogue of arboviruses, including certain other viruses of vertebrates, 3rd edn. American Society of Tropical Medicine and Hygiene, San AntonioGoogle Scholar
  47. 47.
    Kaul HN, Venkateshan CN, Mishra AC (1976) Serological evidence of arbovirus activity in birds and small mammals in Japanese encephalitis affected areas of Bankura District, West Bengal. Indian J Med Res 64:1735–1739PubMedGoogle Scholar
  48. 48.
    Keller M (2005) Development of a competitive inhibition enzyme-linked immunosorbent assay (CI ELISA) for serosurvey of wildlife species for West Nile virus emphasizing marine mammals. Veterinary Medicine. University of Florida, p 102Google Scholar
  49. 49.
    Kemp GE, Causey OR, Setzer HW, Moore DL (1974) Isolation of viruses from wild mammals in West Africa, 1966–1970. J Wildl Dis 10:279–293PubMedGoogle Scholar
  50. 50.
    Kiupel M, Simmons HA, Fitzgerald SD, Wise A, Sikarskie JG, Cooley TM, Hollamby SR, Maes R (2003) West Nile virus infection in eastern fox squirrels (Sciurus niger). Vet Pathol 40:703–707PubMedCrossRefGoogle Scholar
  51. 51.
    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 9:311–322PubMedCrossRefGoogle Scholar
  52. 52.
    Komar N, Clark GG (2006) West Nile virus activity in Latin America and the Caribbean. Rev Panam Salud Publica 19:112–117PubMedCrossRefGoogle Scholar
  53. 53.
    Konstantinov OK, Diallo SM, Inapogi AP, Ba A, Kamara SK (2006) The mammals of Guinea as reservoirs and carriers of arboviruses. Med Parazitol (Mosk):34–39Google Scholar
  54. 54.
    Koptopoulos G, Papadopoulos O (1980) Zooanthroponoses in Greece. A serological survey for antibodies to the arboviruses of tick-borne encephalitis and West Nile. In: Vesenjak-Hirjan J (ed) Arboviruses in the Mediterranean Countries, Zbl Bakt Suppl 9. Gustav Fischer Verlag, Stuttgart, pp 185–188Google Scholar
  55. 55.
    Kramer LD, Bernard KA (2001) West Nile virus infection in birds and mammals. Ann N Y Acad Sci 951:84–93PubMedCrossRefGoogle Scholar
  56. 56.
    Kramer LD, Styer LM, Ebel GD (2008) A global perspective on the epidemiology of West Nile virus. Annu Rev Entomol 53:61–81PubMedCrossRefGoogle Scholar
  57. 57.
    Lanthier I, Hébert M, Tremblay D, Harel J, Dallaire AD, Girard C (2004) Natural West Nile virus infection in a captive juvenile Arctic wolf (Canis lupus). J Vet Diagn Invest 16:326–329PubMedCrossRefGoogle Scholar
  58. 58.
    Le Lay-Rogues G, Arthur CP, Vanderwalle P, Hardy E, Chasterl C (1990) Wild rabbit, Oryctolagus cuniculus L., and arboviruses in southeast France. Results of two serologic investigations. Bull Soc Pathol Exot 83:446–457PubMedGoogle Scholar
  59. 59.
    Le Lay Rogues G, Valle M, Chastel C, Beaucournu JC (1983) Petits mammiferes sauvages et arbovirus en Italie. Bull Soc Pathol Exot 76:333–345Google Scholar
  60. 60.
    Lichtensteiger CA, Heinz-Taheny K, Osborne TS, Novak RJ, Lewis BA, Firth ML (2003) West Nile virus encephalitis and myocarditis in wolf and dog. Emerg Infect Dis 9:1303–1306PubMedCrossRefGoogle Scholar
  61. 61.
    Ludwig GV, Calle PP, Mangiafico JA, Raphael BL, Danner DK, Hile JA, Clippinger TL, Smith JF, Cook RA, McNamara T (2002) An outbreak of West Nile virus in a New York City captive wildlife population. Am J Trop Med Hyg 67:67–75PubMedGoogle Scholar
  62. 62.
    Madić J, Huber D, Lugović B (1993) Serologic survey for selected viral and rickettsial agents of brown bears (Ursus arctos) in Croatia. J Wildl Dis 29:572–576PubMedGoogle Scholar
  63. 63.
    Marfin AA, Petersen LR, Eidson M, Miller J, Hadler J, Farello C, Werner B, Campbell GL, Layton M, Smith P, Bresnitz E, Cartter M, Scaletta J, Obiri G, Bunning M, Craven RC, Roehrig JT, Julian KG, Hinten SR, Gubler DJ, Hilger T, Jones JE, Lehman JA, Medlin K, Morris T, Perilla MJ, Sutliff S, Withum D, Sorhage F, Tan C, Beckett G, Gensheimer K, Greenblatt J, Montero J, Galbraith P, Tassler P, DeMaria A, Matyas B, Timperi R, Bandy U, Breslosky T, Andreadis T, McCarthy T, Backenson B, Hagiwara Y, Kramer L, Morse D, Wallace B, White D, Willsey A, Wong S, Cherry B, Fine A, Kellachan J, Kulakasera V, Poshni I, Rankin J, Hathcock L, Wolfe D, Roche J, Jenkins S, Levy M, MacCormack JN, Gibson J, Blake P, Kramer S, Lance-Parker S, Conti L, Hopkins RS, Oliveri R, Lofgren JP, Woernle CH, Currier M, Slavinski S, Kelso K, Rawlings J (2001) Widespread West Nile virus activity, eastern United States, 2000. Emerg Infect Dis 7:730–735PubMedGoogle Scholar
  64. 64.
    McIntosh BM (1961) Susceptibility of some African wild rodents to infection with various arthropod-borne viruses. Trans R Soc Trop Med Hyg 55:63–68PubMedCrossRefGoogle Scholar
  65. 65.
    McLean RG, Mullenix J, Kerschner J, Hamm J (1983) The house sparrow (Passer domesticus) as a sentinel for St. Louis encephalitis virus. Am J Trop Med Hyg 32:1120–1129PubMedGoogle Scholar
  66. 66.
    McLean RG, Ubico SR, Bourne D, Komar N (2002) West Nile virus in livestock and wildlife. Curr Top Microbiol Immunol 267:271–308PubMedCrossRefGoogle Scholar
  67. 67.
    Miller DL, Radi ZA, Baldwin C, Ingram D (2005) Fatal West Nile virus infection in a white-tailed deer (Odocoileus virginianus). J Wildl Dis 41:246–249PubMedGoogle Scholar
  68. 68.
    MMWR (2000) Update: West Nile Virus Activity—Eastern United States, 2000. Morb Mortal Wkly Rep 49:1044–1047Google Scholar
  69. 69.
    MMWR (2002) Provisional surveillance summary of the West Nile virus epidemic—United States, January–November 2002. Morb Mortal Wkly Rep 51:1129–1133Google Scholar
  70. 70.
    MMWR (2004) West Nile Virus Activity—United States, November 3–8, 2004. Morb Mortal Wkly Rep 53:1050–1051Google Scholar
  71. 71.
    MMWR (2006) West Nile Virus Activity—United States, January 1–August 15, 2006. Morb Mortal Wkly Rep 55:879–880Google Scholar
  72. 72.
    Molnár E, Gresíková M, Kubásova T, Kubinyi L, Szabó JB (1973) Arboviruses in Hungary. J Hyg Epidemiol Microbiol Immunol 17:1–10PubMedGoogle Scholar
  73. 73.
    Molnár E, Gulyás MS, Kubinyi L, Nosek J, Kozuch O, Ernek E, Labuda M, Grulich I (1976) Studies on the occurrence of tick-borne encephalitis in Hungary. Acta Vet Acad Sci Hung 26:419–437PubMedGoogle Scholar
  74. 74.
    Ølberg RA, Barker IK, Crawshaw GJ, Bertelsen MF, Drebot MA, Andonova M (2004) West Nile virus encephalitis in a barbary macaque (Macaca sylvanus). Emerg Infect Dis 10:712–714PubMedCrossRefGoogle Scholar
  75. 75.
    Osterrieth PM, Deleplanque-Liegeois P (1961) Presence d’ anticorps vis ~ a~vis des virus transmis par arthropodes chez le chimpanze (Pan troglodites). Comparaison de leur etat immunitaire a celui de l’homme. Ann Soc Belg Med Trop 1:63–72Google Scholar
  76. 76.
    Padgett KA, Reisen WK, Kahl-Purcell N, Fang Y, Cahoon-Young B, Carney R, Anderson N, Zucca L, Woods L, Husted S, Kramer VL (2007) West Nile virus infection in tree squirrels (Rodentia: Sciuridae) in California, 2004–2005. Am J Trop Med Hyg 76:810–813PubMedGoogle Scholar
  77. 77.
    Palmer MV, Stoffregen WC, Rogers DG, Hamir AN, Richt JA, Pedersen DD, Waters WR (2004) West Nile virus infection in reindeer (Rangifer tarandus). J Vet Diagn Invest 16:219–222PubMedCrossRefGoogle Scholar
  78. 78.
    Papa A, Bakonyi T, Xanthopoulou K, Vázquez A, Tenorio A, Nowotny N (2011) Genetic characterization of West Nile virus lineage 2, Greece, 2010. Emerg Infect Dis 17:920–922PubMedCrossRefGoogle Scholar
  79. 79.
    Paul SD, Rajagopalan PK, Sreenivasan MA (1970) Isolation of the West Nile virus from the frugivorous bat, Rousettus leschenaulti. Indian J Med Res 58:1169–1171PubMedGoogle Scholar
  80. 80.
    Petersen LR, Roehrig JT (2001) West Nile virus: a reemerging global pathogen. Emerg Infect Dis 7:611–614PubMedGoogle Scholar
  81. 81.
    Pilipski JD, Pilipski LM, Risley LS (2004) West Nile virus antibodies in bats from New Jersey and New York. J Wildl Dis 40:335–337PubMedGoogle Scholar
  82. 82.
    Platt KB, Tucker BJ, Halbur PG, Tiawsirisup S, Blitvich BJ, Fabiosa FG, Bartholomay LC, Rowley WA (2007) West Nile virus viremia in eastern chipmunks (Tamias striatus) sufficient for infecting different mosquitoes. Emerg Infect Dis 13:831–837PubMedCrossRefGoogle Scholar
  83. 83.
    Platt KB, Tucker BJ, Halbur PG, Blitvich BJ, Fabiosa FG, Mullin K, Parikh GR, Kitikoon P, Bartholomay LC, Rowley WA (2008) Fox squirrels (Sciurus niger) develop West Nile virus viremias sufficient for infecting select mosquito species. Vector Borne Zoonotic Dis 8:225–233PubMedCrossRefGoogle Scholar
  84. 84.
    Pogodina VV, Frolova MP, Malenko GV (1983) Study on West Nile virus persistence in monkeys. Arch Virol 75:71–86PubMedCrossRefGoogle Scholar
  85. 85.
    ProMED-mail (2002) West Nile virus update 2002-USA (28). ProMED-mail Archive number 20021031.5674Google Scholar
  86. 86.
    ProMED-mail (2002) West Nile virus, Caprine and Ovine-USA (NE) (04). ProMED-mail Archive number 20020920.5368Google Scholar
  87. 87.
    Ratterree MS, Travassos da Rosa APA, Bohm RP Jr, Cogswell FB, Phillippi KM, Caillouet K, Schwanberger S, Shope RE, Tesh RB (2003) West Nile virus infection in nonhuman primate breeding colony, concurrent with human epidemic, southern Louisiana. Emerg Infect Dis 9:1388–1394PubMedCrossRefGoogle Scholar
  88. 88.
    Ratterree MS, Gutierrez RA, Travassos Da Rosa APA, Dille BJ, Beasley DWC, Bohm RP, Desai SM, Didier PJ, Bikenmeyer LG, Dawson GJ, Leary TP, Schochetman G, Phillippi-Falkenstein K, Arroyo J, Barrett ADT, Tesh RB (2004) Experimental infection of rhesus macaques with West Nile virus: level and duration of viremia and kinetics of the antibody response after Infection. J Infect Dis 189:669–676PubMedCrossRefGoogle Scholar
  89. 89.
    Rodhain F, Clerc Y, Albignac R, Ricklin B, Ranaivosata J, Coulanges P (1982) Arboviruses and lemurs in Madagascar: a preliminary note. Trans R Soc Trop Med Hyg 76:227–231PubMedCrossRefGoogle Scholar
  90. 90.
    Rodhain F, Petter JJ, Albignac R (1985) Arboviruses and lemurs in Madagascar: experimental infection of Lemur fulvus with yellow fever and West Nile viruses. Am J Trop Med Hyg 34:816–822PubMedGoogle Scholar
  91. 91.
    Root JJ, Hall JS, McLean RG, Marlenee NL, Beaty BJ, Gansowski J, Clark L (2005) Serologic evidence of exposure of wild mammals to flaviviruses in the central and eastern United States. Am J Trop Med Hyg 72:622–630PubMedGoogle Scholar
  92. 92.
    Root JJ, Oesterle PT, Nemeth NM, Klenk K, Gould DH, McLean RG, Clark L, Hall JS (2006) Experimental infection of fox squirrels (Sciurus niger) with West Nile virus. Am J Trop Med Hyg 75:697–701PubMedGoogle Scholar
  93. 93.
    Root JJ, Oesterle PT, Sullivan HJ, Hall JS, Marlenee NL, McLean RG, Montenieri JA, Clark L (2007) Fox squirrel (Sciurus niger) associations with West Nile virus. Am J Trop Med Hyg 76:782–784PubMedGoogle Scholar
  94. 94.
    Root JJ, Bentler KT, Nemeth NM, Gidlewski T, Spraker TR, Franklin AB (2010) Experimental infection of raccoons (Procyon lotor) with West Nile virus. Am J Trop Med Hyg 83:803–807PubMedCrossRefGoogle Scholar
  95. 95.
    Santaella J, McLean R, Hall JS, Gill JS, Bowen RA, Hadow HH, Clark L (2005) West Nile virus serosurveillance in Iowa white-tailed deer (1999–2003). Am J Trop Med Hyg 73:1038–1042PubMedGoogle Scholar
  96. 96.
    Savage HM, Anderson M, Gordon E, McMillen L, Colton L, Delorey M, Sutherland G, Aspen S, Charnetzky D, Burkhalter K, Godsey M (2008) Host-seeking heights, host-seeking activity patterns, and West Nile virus infection rates for members of the Culex pipiens complex at different habitat types within the hybrid zone, Shelby County, TN, 2002 (Diptera: Culicidae). J Med Entomol 45:276–288PubMedCrossRefGoogle Scholar
  97. 97.
    Schaefer AM, Reif JS, Goldstein JD, Ryan CN, Fair PA, Bossart GD (2009) Serological evidence of exposure to selected viral, bacterial, and protozoal pathogens in free-ranging atlantic bottlenose dolphins (Tursiops truncatus) from the Indian River Lagoon, Florida, and Charleston, South Carolina. Aquat Mamm 35:163–170CrossRefGoogle Scholar
  98. 98.
    Shepherd RC, Williams MC (1964) Studies on viruses in East African bats (Chiroptera). 1. Haemagglutination inhibition and circulation of arboviruses. Zoonoses Res 3:125–139PubMedGoogle Scholar
  99. 99.
    Sherif NEDH (2007) Serological evidence of antibodies to certain arboviruses in desert rodent sera in Egypt. Egypt J Hosp Med 28:342–346Google Scholar
  100. 100.
    Simpson DI, O’Sullivan JP (1968) Studies on arboviruses and bats (Chiroptera) in East Africa. I. Experimental infection of bats and virus transssion attempts in Aedes (Stegomyia) aegypti (Linnaeus). Ann Trop Med Parasitol 62:422–431PubMedGoogle Scholar
  101. 101.
    Simpson DI, Williams MC, O’Sullivan JP, Cunningham JC, Mutere FA (1968) Studies on arboviruses and bats (Chiroptera) in East Africa. II. Isolation and haemagglutination-inhibition studies on bats collected in Kenya and throughout Uganda. Ann Trop Med Parasitol 62:432–440PubMedGoogle Scholar
  102. 102.
    Sixl W, Kock M, Withalm H, Stunzner D, Sixl-Voigt B (1989) Serological investigations of small mammals in waste disposal sites in Austria. Geographia Medica Suppl 2:65–68Google Scholar
  103. 103.
    Smithburn KC, Hughes TP, Burke AW, Paul JH (1940) A neurotropic virus isolated form the blood of a native of Uganda. Am J Trop Med Hyg 20:471–492Google Scholar
  104. 104.
    Sondgeroth K, Blitvich B, Blair C, Terwee J, Junge R, Sauther M, VandeWoude S (2007) Assessing flavivirus, lentivirus, and herpesvirus exposure in free-ranging ring-tailed lemurs in southwestern Madagascar. J Wildl Dis 43:40–47PubMedGoogle Scholar
  105. 105.
    St. Leger J, Wu G, Anderson M, Dalton L, Nilson E, Wang D (2011) West Nile virus infection in killer whale, Texas, USA, 2007. Emerg Infect Dis 17:1531–1533PubMedGoogle Scholar
  106. 106.
    Taylor RM, 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
  107. 107.
    Tesh RB, Siirin M, Guzman H, Travassos Da Rosa APA, Wu X, Duan T, Lei H, Nunes MR, Xiao SY (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
  108. 108.
    Tiawsirisup S, Platt KB, Tucker BJ, Rowley WA (2005) Eastern cottontail rabbits (Sylvilagus floridanus) develop West Nile virus viremias sufficient for infecting select mosquito species. Vector Borne Zoonotic Dis 5:342–350PubMedCrossRefGoogle Scholar
  109. 109.
    Tiawsirisup S, Blitvich BJ, Tucker BJ, Halbur PG, Bartholomay LC, Rowley WA, Platt KB (2010) Susceptibility of fox squirrels (Sciurus niger) to West Nile virus by oral exposure. Vector Borne Zoonotic Dis 10:207–209PubMedCrossRefGoogle Scholar
  110. 110.
    Tonry JH, Xiao SY, Siirin M, Chen H, Travassos Da Rosa APA, Tesh RB (2005) Persistent shedding of West Nile virus in urine of experimentally infected hamsters. Am J Trop Med Hyg 72:320–324PubMedGoogle Scholar
  111. 111.
    Wertheimer AM, Uhrlaub JL, Hirsch A, Medigeshi G, Sprague J, Legasse A, Wilk J, Wiley CA, Didier P, Tesh RB, Murray KO, Axthelm MK, Wong SW, Nikolich-Žugich J (2010) Immune response to the West Nile virus in aged non-human primates. PLoS ONE 5:e15514PubMedCrossRefGoogle Scholar
  112. 112.
    Wilson DE, Reeder DM (2005) Mammal species of the world. A taxonomic and geographic reference, 3rd edn. Johns Hopkins University Press, BaltimoreGoogle Scholar
  113. 113.
    Wolf RF, Papin JF, Hines-Boykin R, Chavez-Suarez M, White GL, Sakalian M, Dittmer DP (2006) Baboon model for West Nile virus infection and vaccine evaluation. Virology 355:44–51PubMedCrossRefGoogle Scholar
  114. 114.
    Zeller HG, Schuffenecker I (2004) West Nile virus: an overview of its spread in Europe and the Mediterranean basin in contrast to its spread in the Americas. Eur J Clin Microbiol Infect Dis 23:147–156PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag (outside the USA) 2012

Authors and Affiliations

  1. 1.US Department of AgricultureNational Wildlife Research CenterFort CollinsUSA

Personalised recommendations