West Nile virus outbreak in North American Owls, Ontario, 2002

Emerging Infectious Diseases, Dec, 2004 by Ady Y. Gancz, Ian K. Barker, Robbin Lindsay, Antonia Dibernardo, Katherine McKeever, Bruce Hunter

From July to September 2002, an outbreak of West Nile virus (WNV) caused a high number of deaths in captive owls at the Owl Foundation, Vineland, Ontario, Canada. Peak death rates occurred in mid-August, and the epidemiologic curve resembled that of corvids in the surrounding Niagara region. The outbreak occurred in the midst of a louse fly (Icosta americana, family Hippoboscidae) infestation. Of the flies tested, 16 (88.9%) of 18 contained WNV RNA. Species with northern native breeding range and birds >1 year of age were at significantly higher risk for WNV-related deaths. Species with northern native breeding range and of medium-to-large body size were at significantly higher risk for exposure to WNV. Taxonomic relations (at the subfamily level) did not significantly affect exposure to WNV or WNV-related deaths. Northern native breeding range and medium-to-large body size were associated with earlier death within the outbreak period. Of the survivors, 69 (75.8%) of 91 were seropositive for WNV.

**********

Since its initial detection in the New York City area in 1999 (1), West Nile virus (WNV) has emerged as a health risk for humans and has been associated with illness and death in a wide variety of North American birds, mammals, and reptiles (2,3). In addition, serologic evidence of exposure to this arthropodborne flavivirus (family Flaviviridae) has been reported in many other North American species in which disease had not been previously recorded (4-6).

While severe clinical disease develops in a minority of humans and horses with WNV infection (7,8), the situation in birds appears to be different in North America. Some North American birds are highly susceptible to this virus, as shown by large-scale local deaths of American Crows (Corvus brachyrhynchos, family Corvidae) (1,9). This finding was further demonstrated recently by experimental infection (10). The factors that make some species highly susceptible to WNV remain largely unknown.

Studying the effect of taxonomic, geographic, and demographic background on susceptibility to WNV is potentially useful for predicting and modeling the effect of WNV on host populations. So far, taxonomy alone has offered limited help in predicting susceptibility to WNV, as some closely related species (e.g., within the same genus) show different susceptibility patterns. For example, Fish Crows (C. ossifragus) appear less susceptible to WNV than do American Crows (10).

Geographic distribution could explain susceptibility patterns if a species has had previous exposure to the same or similar agent. Exposure to St. Louis encephalitis virus (SLEV) has been suggested as a possible mechanism of acquired immunity against WNV (2). In addition, species that have evolved in areas where other flaviviruses, such as SLEV, are common may have undergone selection for an innate immune response that may offer protection against WNV.

Age-related differences in susceptibility to WNV have been described for chickens (2) and domesticated geese (11). These age-related differences have not been reported in wild birds, perhaps because of the difficulty determining their age.

From July to September 2002, high death rates occurred in captive owls (family Strigidae) kept at the Owl Foundation, Vineland, Ontario, Canada. At the time, many of the birds were infested with adult hematophagous louse flies (order Diptera, family Hippoboscidae); some had loads >400 flies per bird. Initially, the deaths were attributed to this infestation. On August 9, the authors examined three dead owls. Necropsy findings included marked hepatomegaly, splenomegaly, and cerebral hemorrhage. A rapid antigen-capture assay for WNV detection (Vec Test, Medical Analysis Systems, Camarillo, CA) was used for initial screening of oropharyngeal swabs from these birds; however, all samples were negative. On August 16, tissue samples from eight owls, including the initial three, were found to be positive for WNV by reverse transcription--polymerase chain reaction (RT-PCR) test.

Beginning August 23, the remaining birds were vaccinated with a killed WNV vaccine (West Nile Innovator Vaccine, Fort Dodge Animal Health, Fort Dodge, IA). However, from July 26 to September 28, a total of 108 (44%) of 245 owls died.

To our knowledge, the outbreak at the foundation is the largest WNV outbreak in captive wildlife collections in North America since 1999 (12-14) and the first in Canada. These outbreaks offer a unique and transient opportunity to study the effect and epidemiologic features of WNV infection in multiple species under quasinatural conditions. With the implementation of preventative measures against WNV (e.g., vector control and vaccination), this opportunity will disappear.

The objective of this study was to describe the epidemiologic features of the WNV outbreak at the foundation in 2002. Specifically, we studied the effect of outdoor housing, age, body size, taxonomy, and native breeding range on exposure to WNV and on WNV-related deaths.

Materials and Methods

Study Site

The Owl Foundation specializes in breeding and rehabilitating North American owls. Its facility in the Niagara region (Vineland, Ontario; 43[degrees]10' N, 79[degrees]20' W) has [approximately equal to] 3,340 [m.sup.2] of specially designed outdoor cages and a few indoor cages.

Records and Observations

The Owl Foundation maintains detailed records of all birds in the facility, which includes each bird's history, date admitted, species, cage in which it is housed, movements, and medical history. These data were used in the epidemiologic analysis of this outbreak. For most birds in this study, sex had not been determined.

Data summarizing dead corvid sightings in the Niagara region (1,896 [km.sup.2] in size, map available at http://www.regional.niagara.on.ca/exploring/pdf/regionalniagara.pdf) were obtained from the Canadian Cooperative Wildlife Health Center national WNV surveillance database. These data were gathered by the Niagara Region Health Unit from May 14 to October 12, 2002.