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CHANGES IN SEROPREVALENCE OF WEST NILE VIRUS ACROSS ILLINOIS IN FREE-RANGING BIRDS FROM 2001 THROUGH 2004

ABSTRACT

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Of the 5,236 birds sampled for antibodies to West Nile virus (WNV) in Illinois from 2001 through 2004, 348 (6.6%) birds were seropositive. Our multiple year surveillance identified several avian species that had particularly high percentages of seropositive individuals. The importance of these species in the enzootic and/or epizootic transmission of WNV is discussed relative to their regional abundance and literature on host competency. The species with the highest exposure rates to WNV differed both temporally and regionally. In general, birds that bred or were born in Illinois were more likely to have antibodies than transient birds. There was also a significant difference in the seroprevalence between adults (12.1%) and juveniles (5.5%), indicating that the acquired antibody response from previous years is a critical concern when interpreting seroprevalence rates in wild-caught birds. The most common hosts for St. Louis encephalitis virus were also the most common hosts for WNV, which strongly supports the role of similar vectors for both flaviviruses. Avian species with high WNV seroprevalence rates tended to be those that bred throughout the year, have open cup nests, and live in close proximity to humans.

INTRODUCTION

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West Nile Virus (WNV) is a mosquito-borne flavivirus (family Flaviviridae) that was first isolated in Africa in 1937.¹ It was first reported in North America in New York City in 1999 and in just five years spread throughout most of North and Central America.² In Illinois, WNV was first reported in September 2001 with an initial distribution limited to seven counties, primarily in the northeastern section of the state.³ Since then, WNV has been detected in all but 2 of the 102 counties in Illinois.³ In 2002, Illinois had the highest number of WNV human cases (884) and deaths (66) in the United States. Although WNV poses a serious long-term health threat, little is known about the impact WNV has on birds, the primary reservoir hosts, and the role that specific bird species have on the distribution and amplification of WNV transmission.⁴ Since seropositive/seroprevalence rates are a measure of exposure and survival, they can be interpreted in conjunction with ancillary information. Using seropositive/seroprevalence rates, we present the findings of a four-year study that documents the spatial and temporal changes in avian seroprevalence within Illinois.

Although almost 300 bird species have been reported as WNV positive, a much smaller number are likely to be reservoir hosts.⁵ The significance of a species or group of species in WNV transmission is related to their host competency, their natural exposure rates to mosquito vectors, host serology, and their temporal and spatial availability (e.g., relative abundance) to the mosquitoes.^1,6–9 For example, Apperson and others found that Culex pipiens (the species most often reported as the principal zoonotic vector of WNV in the east-central United States) has a broad avian host range, but this vector species did not randomly feed on bird species based on their abundance as predicted by breeding bird surveys.⁶ In addition, viremic transient birds have been suggested as the means by which WNV has rapidly spread across North and Central America,^10–12 while resident breeding birds are probably critical to maintain and amplify the zoonotic cycle.^1,13,14

The presence of seropositive birds may not be an indication of current WNV activity, but is an indication of exposure to WNV-carrying mosquitoes and survivorship, as seen in research with St. Louis encephalitis.¹⁴ Recent research suggests that persistence of antibody to WNV was at least 60 weeks in rock pigeons.⁸ Other studies on St. Louis encephalitis virus (SLEV), a closely related virus, found that birds may retain antibodies throughout their life.^4,15 Therefore, after the initial introduction of WNV to an area, juvenile rather than adult seroprevalence data may provide a better index of current WNV activity in an area.

Seroprevalence in adult avian species can be used to determine the initial spread of WNV across a region, an approach taken by a study on seroprevalence during the spread of the virus across Illinois in 2002.¹⁴ We can now determine if seroprevalence rates have changed over time between regions and species. The number of human cases of WNV in Illinois decreased by more than 10-fold after 2002; however, reports of infected birds and mosquitoes remained relatively high.³ This study investigates the annual distribution and extent of WNV exposure in avian species after the initial outbreak in humans as enzootic cycles appear to become established within the wildlife of Illinois. With these seroprevalence data, we can begin to address the long-term effect of WNV on birds and to identify what makes specific species more likely to be exposed to WNV.

MATERIALS AND METHODS

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Field collection. Wild birds were captured at 60 different sampling sites from September 2001 through November 2004. Not all 60 sites were sampled every year. Nine of the sites were sampled two or more of the four years. Of these nine, two were in northern Illinois, four in central Illinois, and three in southern Illinois. These three regional divisions represent a latitudinal gradient that corresponds to climatic and ecologic differences. Sampling sites were changed yearly based on how successful we were at catching birds at them, coordination with mosquito sampling, and differences in the amount of personnel available. In addition, game birds were only sampled over a short time span, in conjunction with activities of the Illinois Department of Natural Resources. All other sites were sampled every two weeks. Birds were primarily captured using mist nets and potter traps (small four-chambered box traps). At some sites, birds were captured year-round; however, at other sites birds were only captured during the breeding season. Captured birds were identified by species and, if possible, by sex and age.^16–18 Individuals were classified as adults (those born the previous breeding seasons) and as juveniles (those born during the current breeding season). In addition, species were classified as those that were thought to be migrating through Illinois (transients) versus individuals believed to have bred within the area. Individuals that were captured during the breeding season (May–August) and that were captured in suitable habitat were considered breeding individuals. Individuals that are known not to breed in the state or to only have a small breeding area, not near where the individuals were captured, were considered transients. Once captured, a blood sample was taken from the jugular or brachial vein, depending on the size of the bird, using a 27-gauge -inch needle attached to a syringe. Depending on the size of the bird, quantities of blood taken from each bird ranged from 0.1 to 0.2 mL. Birds were banded with U.S. Geological Survey aluminum leg bands (Permit no. 06507) to ensure that a bird was only used once in the analysis, and to obtain data for future research on how long antibodies persist within an individual.

Statistical analysis. To determine what percentage of each species were seropositive in each region, we divided the number of seropositive individuals of a species by the total number of seropositive individuals. When comparing the most seropositive species in each region, we used only species that had a sample size of 15 (14 species). All other comparisons were analyzed using either chi-square or Fisher’s exact tests (Statview, SAS, Cary, NC). When determining the abundance of particular species, we used spring bird count data.¹⁹ Other studies have used a breeding bird survey⁶; however, these censuses are typically not conducted in urban areas. Therefore, we believe they do not represent the true regional abundance. The spring bird count is conducted throughout the entire state by more than 1,000 volunteers early in the breeding season and in all habitats. Thus, we believe it provides a better representation of the relative species abundance.¹⁹

Laboratory testing. After capture and bleeding of the birds, blood samples were brought back to the laboratory to be tested for antibodies to WNV. An epitope-blocking enzyme-linked immunosorbent assay was used to detect the presence of antibodies to WNV using three different monoclonal antibodies (MAbs): 3.1112G, 2B2, and 6B6C-1.¹⁴ Monoclonal antibody 3.1112G is specific for NV, while MAbs 2B2 and 6B6C-1 can react with other viruses, including WNV. For a serum sample to be considered positive for antibodies to WNV, it had to block the binding of all three MAbs by > 30% relative to the negative control, normal chicken serum (Vector Laboratories, Burlingame, CA), which readily allows the binding of MAbs.⁷ Serum from WNV-infected horses was used as a positive control.²⁰

RESULTS

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Over the course of this study, 5,236 wild, free-ranging birds belonging to 11 orders, 36 families, and 145 species were sampled. Positive wild birds represented 6 orders, 19 families, and 38 species (Table 1). Despite the diversity of species exposed to WNV, the top five species (of those with more than 15 individuals sampled) throughout the state, in terms of the percentage that were seropositive, were Wild Turkey (40.5%, n = 37), Mourning Dove (38.1%, n = 97), Northern Cardinal (24.7%, n = 389), American Robin (15.2%, n = 341), and House Sparrow (9.6%, n = 1,207). Several species never tested positive for antibodies to WNV, including, Downy Woodpecker (n = 39), Tufted Titmouse (n = 49), and BlackCapped or Carolina Chickadee (because of difficulty in identifying chickadee species, we combined the data for the two; n = 76). The species with the highest exposure rates differed both temporally and regionally. In 2002, data (i.e., both adult and juveniles) from Ringia and others¹⁴ showed that the species with the highest seroprevalence was Northern Cardinal (12.4%), while in 2003 Wild Turkey and Mourning Dove (40.5%) were the highest, and in 2004 Mourning Dove (42.1%) was the highest (Table 1).

View larger version (7K): [in this window] [in a new window]       FIGURE 1. Species whose juveniles have the highest West Nile virus seroprevalence from 2002 through 2004. Line with = American Cardinal; Line with = House Sparrow; Line with = American Robin.

Not all of the 15 most common species in Illinois were found to be equally exposed to WNV. The American Robin, House Sparrow, Mourning Dove, and Northern Cardinal, ranked fourth, fifth, ninth, and tenth, respectively; each share some common natural history traits (Table 3). All are multiple brooded (more than one brood of young per year), closely associated with humans, and able to breed throughout the bird breeding season.^21,23 In contrast, the 2 most common species in Illinois the Red-winged Blackbird and the Common Grackle had low WNV seroprevalence. These 2 species are single brooded, not strongly associated with urban areas, and breed early in the year (April–June).^21,23

DISCUSSION

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The temporal variation in seroprevalence from 2001 to 2004 in Illinois may reflect the spread and establishment of WNV in Illinois. Although the WNV epidemic occurred in 2002, our data suggest a WNV epizootic among birds occurred in 2003 followed by a marked decrease in WNV activity in 2004. There are two plausible explanations for the decrease in 2004. The first is that climatic factors resulted in lower mosquito abundance and WNV activity in mosquitoes.²⁴ The second is that the increase in seroprevalence in 2003 reduced the number of available hosts in 2004, thus regulating the intensity of transmission. This feedback loop, where the increasing seroprevalence decreases the likelihood of an infectious vector finding a susceptible host, is only valid if the rate of turnover is relatively low.²⁵ Although this may be unlikely, given the usually high turnover in most bird species, we believe it does deserve additional attention.

Although the data suggest that adults are more likely to be seropositive than juveniles, juvenile data provides a much better index of the temporal and regional transmission levels because antibodies persist for at least one year.^4,8 Therefore, the use of seroprevalence data from adult birds may suggest that birds are being exposed at a greater rate at one site than another, but these differences in exposure may not represent the year from which they were sampled. This is because in many species adults exhibit high site fidelity.²⁶ Therefore, one outbreak year may result in adult seroprevalence being relatively high for several years, whereas juvenile seroprevalence data would provide a better index of transmission levels that year.

Our research suggests that breeding birds, in addition to juveniles, should also be used when accessing WNV activity. Although transient birds have been implicated as a means by which WNV rapidly spreads across regions,^11,12,22 several recent studies have suggested that transient birds may play a relatively small role in the dispersal of viruses.^4,10,27 Although this remains one of the major epidemiologic questions still to be answered about WNV,²⁸ we were not investigating the role transient birds play in the spread of the virus. Our data only suggest that few transients were exposed to WNV relative to that of breeding birds. A possible explanation for the low seroprevalence of transients is that fewer transient were exposed to WNV because most breed farther to the north where there are decreased levels of WNV activity.

Seropositive individuals are not necessarily good reservoir hosts. Laboratory studies reported by Komar and others² and Reisen and others⁹ suggested that certain species are more competent (higher and longer viremia) than others as reservoir hosts for WNV. Reisen and others⁹ found that although corvids produce the highest viremias, House Sparrows and House Finches, which are more evenly distributed, may also be important hosts for effective WNV transmission. We found that many of the species that Komar and others² and Reisen and others⁹ found to be possible competent hosts have high WNV seroprevalence. Whereas some birds, such as corvids, exhibit a high mortality from WNV and thus tend to have a low seroprevalence rate, it seems reasonable to assume that birds with high seroprevalence rates experience a much lower mortality from the virus. For example, Reisen and others⁹ found that although only 16% of House Sparrows died of exposure to WNV, 63% of House Finches died. Three of our top five WNV seroprevalent species (American Robin, Mourning Dove, House Sparrow) were also considered by Komar and others² and Reisen and others⁹ to be competent hosts. In our study, the Northern Cardinal and the Wild Turkey both exhibited high WNV seroprevalence rates, but their competency were not determined in the studies of Komar and others² or Reisen and others.⁹ Because of the high seroprevalence of Northern Cardinals, we believe that this species should receive additional attention to determine its host competency to evaluate its potential role in WNV zoonotic cycles in Illinois. Although Komar and others² considered the Mourning Dove to be a poor candidate as a reservoir host because of its short viremia, the high seroprevalence rates in our study indicate that this species has some behavioral characteristic(s) that result in it being frequently exposed to infected mosquitoes. In Illinois, the high seroprevalence of Mourning Doves, coupled with high abundance, may offset their low competency in regard to their importance in as a reservoir host. Species abundance must be taken into account when determining how important species are in the zoonotic cycle.²⁹ This is best illustrated by House Sparrows. Although they are not experiencing the highest exposure (9.6%) in Illinois, their high abundance, particularly in urban areas, may result in them being a very important species in the zoonotic cycle, as seen in research with SLEV.²⁶

Many of the characteristics of the WNV epizootic are remarkably similar to what has been reported during outbreaks of SLEV. The activity of both viruses peak in late summer, their major vector in the midwest is Cx. pipiens, there is regional variation in preferred bird hosts, and the primary hosts are most often in the orders Columbiformes (i.e., doves) and Passeriformes (e.g., sparrow, robins, cardinals, etc.).¹⁵ In the Midwest, the common hosts for SLEV are House Sparrow, Blue Jay, American Robin, Northern Mockingbird, and Northern Cardinal.³⁰ In the 1975 SLEV epidemic in Chicago, America Robins were implicated as the major reservoir host for SLEV.¹⁵ It is interesting that four of the five birds with the greatest exposure to WNV in our study were also important species in SLEV epizootics. The obvious difference between the two viruses is that bird mortality associated with WNV appears to be much greater. This high mortality may result in WNV persisting in an area longer than SLEV. When birds are removed from an area other, non-territorial, birds rapidly move in. This replacement of removed birds by new birds has been observed in 63 experiments with 53 species.³¹ The replacement can occur as fast as a few minutes or take up to two days.³¹ Therefore, although birds in an area infected with SLEV might acquire immunity, the mortality associated with WNV might result in a net influx of susceptible hosts, possibly perpetuating the epizootic cycle.

There appears to be common natural history traits among the species with high seropositive rates and those with low seropositive rates. Four of the five species with the highest seroprevalence rates have commonalities among them. As previously stated, they are all multiple brooded, breed throughout the breeding season, and have a strong association with humans due to their habitulization in residential/urban areas.^21,23,31 Also, all of the species are residents, except American Robins, which are short-distance migrants.

A good example of the differences in seroprevalence between species is illustrated by Common Grackles and American Robins. These species nest in close proximity, often in the same tree; however, Common Grackles nest much earlier.²³ This difference in breeding phenology may explain why the proportion of grackles with antibodies to WNV is approximately 3%, while approximately 12% of Robins have antibodies to this virus. This difference may be related to how lethal WNV is to a species, but it may also be due to the behavior of the species, particularly when the species nests and form communal roosts. Grackles breed extremely early (April), form large communal roosts in mid-summer, and begin migrating in mid to late summer. American Robins breed throughout the summer months and form communal roosts late in the summer.^21,23,31 Because roosting probably occurs when birds are exposed to WNV-carrying mosquitoes (i.e., Cx. pipiens), the roosting behavior of birds, especially when communal roosts are formed, may provide an explanation for the difference in seroprevalence between species.¹⁵ Grackles may not be exposed to mosquitoes that carry WNV because they breed when fewer infected mosquitoes are present, and their roost behavior in Illinois does not predispose them to being exposed to WNV, while the communal roosts of American Robins late in the summer may attract large numbers of mosquitoes.

Because WNV is new to North America it is important to determine how the avifauna acclimates to its presence. Long-term studies are needed to characterize the enzootic cycle of WNV. However, it is also important to determine if the species that are not seropositive are in areas where other species that are experiencing high exposure rates are refractory, not being exposed, or dying after being exposed. For example, several cavity nesting species never tested positive for antibodies to WNV in our study, including, Downy Woodpecker, Tufted Titmouse, and Black-capped or Carolina Chickadee, despite a reasonable capture rate for each species. Although, seroprevalence data provide an insight into how WNV activity differs both temporally and spatially, and which species may be most important in an enzootic cycle, more research is needed on the transmission dynamics of WNV.

Received March 22, 2005. Accepted for publication July 14, 2005.

Acknowledgments: We thank the Forest Preserve Districts of Illinois, the Illinois State Parks, Southern Illinois University, and the University of Illinois at Champaign-Urbana for use of research sites; the field crew (Brad Danner, Evette Vlach, Stephanie Eicholz, Bill Anderson, Brett Amdor, Joe Heisinger, Jennifer Wise, Arlo Raim, Sarah Yaremych, Christine LaPointe, Bill Stewart, Derrick Robertson, and Amanda Kamradt) for their help with this study; and Weidong Gu and David Enstrom for reviewing the manuscript. This study was conducted under animal use (collecting) permit no. 04010.

Financial support: This study was supported by grants to Robert J. Novak from the Illinois Department of Natural Resources Waste Tire Act, the Centers for Disease Control and Prevention (PHS U50/CCU 52051), and the U.S. Department of Agriculture Cooperative State Research, Educational, and Extension Service (PHS U50 CCU52051: West Nile Virus, Illinois).

^* Address correspondence to Robert J. Novak, Medical Entomology Laboratory, Illinois Natural History Survey, 1910 Griffith Drive, North 104 Annex, Champaign, IL 61820. E-mail: rjnovak{at}uiuc.edu

Authors’ addresses: Tara A. Beveroth, Michael P. Ward, Richard L. Lampman, and Robert J. Novak, Medical Entomology Laboratory, Illinois Natural History Survey, 1910 Griffith Drive, North 104 Annex, Champaign, IL 61820, Telephone: 217-333-1186, Fax: 217-333-2359, E-mails: beveroth{at}uiuc.edu, mpward{at}uiuc.edu, rlampman{at}uiuc.edu, and rjnovak{at}uiuc.edu. Adam M. Ringia, U.S. Fish and Wildlife Service, 1590 Williamsbridge Road, Bronx, NY 10461, Telephone: 718-415-3451, E-mail: ringia{at}yahoo.com.

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