Migratory Birds and Spread of West Nile Virus in the Western Hemisphere

Perspectives Migratory Birds and Spread of West Nile Virus in the Western Hemisphere John H. Rappole,* Scott R. Derrickson,* and Zdenek Hubálek† *Conservation and Research Center, National Zoological Park, Smithsonian Institution, Front Royal, Virginia, USA; and †Institute of Vertebrate Biology, Academy of Sciences, Valtice, Czech Republic West Nile virus, an Old World flavivirus related to St. Louis encephalitis virus, was first recorded in the New World during August 1999 in the borough of Queens, New York City. Through October 1999, 62 patients, 7 of whom died, had confirmed infections with the virus. Ornithophilic mosquitoes are the principal vectors of West Nile virus in the Old World, and birds of several species, chiefly migrants, appear to be the major introductory or amplifying hosts. If transovarial transmission or survival in overwintering mosquitoes were the principal means for its persistence, West Nile virus might not become established in the New World because of aggressive mosquito suppression campaigns conducted in the New York area. However, the pattern of outbreaks in southern Europe suggests that viremic migratory birds may also contribute to movement of the virus. If so, West Nile virus has the potential to cause outbreaks throughout both temperate and tropical regions of the Western Hemisphere. The first known human case of West Nile [Pica pica], Bronze-winged Ducks [Anas virus infection recorded in the Western Hemi- specularis], Impeyan Pheasants [Lophophorus sphere was reported in August 1999 (1). impeyanus], Blyth’s Tragopans [Tragopan blythi], Eventually, 62 cases of the disease were and Snowy Owls [Nyctea scandia]) (6). confirmed; no new cases have been reported since The spatial and temporal juxtaposition of October 16, 1999 (2). Of the human cases avian and human infections in this instance and laboratory-confirmed as of October 8, 1999, 70% historically has led many epidemiologists to occurred within a circle 10 km in radius centered conclude that birds act as introductory hosts, in the northern end of the New York City borough perhaps by infecting ornithophilic mosquitoes, of Queens (1). Coincident in both space and time which in turn infect amplifying hosts and with the human outbreak was a substantial die- eventually humans (3,7). Despite the fact that off of birds, particularly American Crows (Corvus migratory birds have long been suspected as brachyrhynchos) (3). Unusual bird deaths were critical agents in outbreaks of this and other noted around the Bronx Zoo in mid-August (4), arboviruses, the link remains conjectural be- approximately 8 km north of the epicenter of the cause of the difficulty in determining the human epidemic. Several thousand crows and intensity and duration of viremia in naturally other avian species are presumed to have died of infected wild birds (8,9). the virus, mostly in and around the New York We present an overview of the association of City area (5). In addition to wild birds, the die-off West Nile virus with birds, focusing in particular included specimens in the Bronx and Queens zoo on the advent and movement of the virus in the collections (including Chilean Flamingos Western Hemisphere. [Phoenicopterus chilensis], Guanay Cormorants [Phalacrocorax bougainvillei], Bald Eagles History of West Nile Virus [Haliaeetus leucocephalus], Black-billed Magpies West Nile virus was first isolated and identified as a distinct pathogen from the blood of Address for correspondence: John H. Rappole, 1500 Remount a woman in the West Nile region of Uganda in Road, Front Royal, VA 22630, USA; fax: 540-635-6551; e-mail: 1937 (10). Cross-neutralization tests have been [email protected]. used to classify the virus as a Flavivirus (Family Vol. 6, No. 4, July–August 2000 319 Emerging Infectious Diseases Perspectives Flaviviridae) closely related to Japanese en- immunosuppression and enhanced replication of cephalitis virus, eastern Asia; Kunjin virus, West Nile virus in rodents (30). Australia and Southeast Asia; and St. Louis Further support for the possibility that encephalitis virus, North and South America migratory birds play a major role in virus (11,12). Several genetic lineages of the virus have transport comes from study of related viruses. been identified in different geographic locations. For instance, both Eastern (EEE) and Western The lineage associated with the New York equine encephalomyelitis alphaviruses, ecologic outbreak has been identified as virtually relatives of West Nile virus, have been isolated identical with an Israeli strain of the virus by from actively migrating birds in the United phylogenetic analysis of E-glycoprotein nucleic States (25,26). Evidence also indicates that the acid sequence data (13). West Nile virus was one 1962 epidemic of EEE in Jamaica resulted from of the most widespread flaviviruses, even before transport of the virus by birds from the its recent entry into North America. Its continental United States (31). distribution extends throughout Africa, the Middle Unlike the 1999 New York City epidemic, East, and southern temperate and tropical during which large numbers of dead and dying Eurasia (14,15). During the 1950s, an estimated birds, especially crows, were observed concur- 40% of the human population in Egypt’s Nile rently with clinical reports of human infection Delta was seropositive for the virus (16). The with the virus (3), the Old World epidemics of largest human epidemic occurred in Cape West Nile virus had few concurrent reports of Province, South Africa, in 1974, when approxi- deaths of infected birds (7). This difference could mately 3,000 clinical cases of the virus were indicate lack of both exposure and adaptation to recorded (17). the virus among New World avian populations compared with Old World species. Old World Migratory Birds and West Nile Virus data indicate that susceptibility to fatal infection in the Old World with the virus varies markedly for adult and Migratory birds have long been suspected as young birds, with high death rates in juveniles the principal introductory hosts of West Nile and high incidence of circulating antibodies in virus into new regions for the following reasons: adult birds (19). Susceptibility to infection also Outbreaks of the virus in temperate regions varies considerably among species. Hooded generally occur during late summer or early fall, Crows (Corvus corone) had both a high death rate coinciding with the arrival of large concentrations in young birds in laboratory experiments and of migratory birds (and mosquitoes) (18-20); high levels of circulating antibodies in adults, these outbreaks often occur among humans while Rock Doves (Columba livia) appeared to be living in or near wetlands where high much less susceptible to both infection and death concentrations of birds come into contact with from the virus (19). large numbers of ornithophilic mosquitoes (7,21,22); the principal vectors from which the Migratory Birds and West Nile Virus virus has been isolated are mainly ornithophilic in the New World mosquitoes (Culex univittatus in the Middle East As was the case for humans, the first birds and C. pipiens in Europe) (7,13,14,18,22); documented as infected with West Nile virus in antibodies to the virus have been found in the the Western Hemisphere were identified in blood of many migratory bird species in Eurasia August 1999 (6). Thereafter, large die-offs of wild (14,15,22-24); migratory birds have been linked and captive birds at the Bronx Zoo and other with transporting related viruses in the Western parts of the New York area coincided with the Hemisphere (9,25,26); West Nile virus has been increasing number of human cases reported from isolated from some species of actively migrating the same region (1,4,6). As in several European birds (e.g., the Barred Warbler [Sylvia risoria] in outbreaks, the main vector in the New York City Cyprus and the Turtle Dove [Streptopelia turtur] epidemic was identified as the ornithophilic in Slovakia (20,23,24); viremia sufficiently long- mosquito C. pipiens (4). Furthermore, the term to infect vector mosquitoes has been outbreak in humans occurred at urban sites near documented in several bird species (18,19,27-29); wetlands where migratory birds, ornithophilic and migration places substantial physiologic mosquitoes, and humans were concentrated. stress on birds. Stress has been shown to promote These circumstances, in conjunction with the Emerging Infectious Diseases 320 Vol. 6, No. 4, July–August 2000 Perspectives ecology of the virus in the Old World, support the contact with West Nile virus is possible. conjecture that zoo, pet, domestic, or wild birds However, a few Eurasian Wigeons, presumably were responsible for introducing the virus to the from the Icelandic breeding population, winter New World. If so, birds could have served as the regularly along the coast of eastern North source by normal migration, displacement from America (32,33). These birds could contract the normal range by storms, or importation (legal virus from vector mosquitoes infected by biting and illegal). other members of the breeding population that winter in areas where West Nile virus is Normal Interhemispheric Migration prevalent and bring infectious blood to the New A small percentage of the populations of a few World on their winter migrations. bird species migrate regularly in August and Eurasian Wigeons are not the only species September from breeding grounds in the Old with such a migration pattern. Eurasian World to wintering grounds along the eastern populations of several species in which evidence seaboard of North America. An example of this of exposure (e.g., antibodies) to the virus has been group is the Eurasian Wigeon (Anas penelope), detected are rare migrants along the eastern which breeds across the entire Palearctic region seaboard of North America (Table 1). However, if from Iceland to Siberia’s Kamchatka Peninsula normal migration were a likely pathway, the and winters primarily in the temperate and virus would likely have become established tropical zones of the Old World (32), where earlier in this hemisphere, since individual birds Table 1.

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