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Culex flavivirus (CxFV) is an insect-specific flavivirus infecting Culex mosquitoes, which are important vectors of West Nile virus (WNV). CxFV and WNV cocirculate in nature and coinfect Culex mosquitoes, including in a WNV "hotspot" in suburban Chicago. We previously identified a positive association between CxFV and WNV in mosquito pools collected from suburban Chicago in 2006. To further investigate this phenomenon, we compared the spatial and temporal distribution of CxFV during an interepidemic year (2011) and an epidemic year (2012) for WNV. Both viruses were more prevalent in mosquito pools in 2012 compared to 2011. During both years, the CxFV infection status of mosquito pools was associated with environmental factors such as habitat type and precipitation frequency rather than coinfection with WNV. These results support the idea that WNV and CxFV are ecologically associated, perhaps because both viruses respond to similar environmental drivers of mosquito populations.

Background: The dilution effect is the reduction in vector-borne pathogen transmission associated with the presence of diverse potential host species, some of which are incompetent. It is popularized as the notion that increased biodiversity leads to decreased rates of disease. West Nile virus (WNV) is an endemic mosquito-borne virus in the United States that is maintained in a zoonotic cycle involving various avian host species. In Atlanta, Georgia, substantial WNV presence in the vector and host species has not translated into a high number of human cases., Methods: To determine whether a dilution effect was contributing to this reduced transmission, we characterized the host species community composition and performed WNV surveillance of hosts and vectors in urban Atlanta between 2010 and 2011. We tested the relationship between host diversity and both host seroprevalence and vector infection rates using a negative binomial generalized linear mixed model., Results: Regardless of how we measured host diversity or whether we considered host seroprevalence and vector infection rates as predictor variables or outcome variables, we did not detect a dilution effect. Rather, we detected an amplification effect, in which increased host diversity resulted in increased seroprevalence or infection rates; this is the first empirical evidence for this effect in a mosquito-borne system., Conclusions: We suggest that this effect may be driven by an over-abundance of moderately- to poorly-competent host species, such as northern cardinals and members of the Mimid family, which cause optimal hosts to become rarer and present primarily in species-rich areas. Our results support the notion that dilution or amplification effects depend more on the identities of the species comprising the host community than on the absolute diversity of hosts.

In the eastern United States, human cases of West Nile virus (WNV) result from spillover from urban epizootic transmission between passerine birds and Culex mosquitoes. In Atlanta, GA, substantial WNV presence in hosts and vectors has not resulted in the human disease burden observed in cities with similar infection pressure. Our study goal was to investigate extrinsic ecological conditions that potentially contribute to these reduced transmission rates. We conducted WNV surveillance among hosts and vectors in urban Atlanta and recorded an overall avian seroprevalence of nearly 30%, which was significantly higher among northern cardinals, blue jays, and members of the mimid family, and notably low among American robins. Examination of temporal Culex feeding patterns showed a marked feeding shift from American robins in the early season to northern cardinals in the late season. We therefore rule out American robins as superspreaders in the Atlanta area and suggest instead that northern cardinals and mimids act as WNV "supersuppressor" species, which slow WNV transmission by drawing many infectious bites during the critical virus amplification period, yet failing to amplify transmission due to low host competencies. Of particular interest, urban forest patches provide spillover protection by increasing the WNV amplification fraction on supersuppressor species., (© The American Society of Tropical Medicine and Hygiene.)

Antibody duration, following a humoral immune response to West Nile virus (WNV) infection, is poorly understood in free-ranging avian hosts. Quantifying antibody decay rate is important for interpreting serologic results and for understanding the potential for birds to serorevert and become susceptible again. We sampled free-ranging birds in Chicago, Illinois, US, from 2005 to 2011 and Atlanta, Georgia, US, from 2010 to 2012 to examine the dynamics of antibody decay following natural WNV infection. Using serial dilutions in a blocking enzyme-linked immunosorbent assay, we quantified WNV antibody titer in repeated blood samples from individual birds over time. We quantified a rate of antibody decay for 23 Northern Cardinals (Cardinalis cardinalis) of 0.198 natural log units per month and 24 individuals of other bird species of 0.178 natural log units per month. Our results suggest that juveniles had a higher rate of antibody decay than adults, which is consistent with nonlinear antibody decay at different times postexposure. Overall, most birds had undetectable titers 2 yr postexposure. Nonuniform WNV antibody decay rates in free-ranging birds underscore the need for cautious interpretation of avian serology results in the context of arbovirus surveillance and epidemiology.

Animals can decrease their individual risk of predation by forming groups. The encounter-dilution hypothesis extends the potential benefits of gregariousness to biting insects and vector-borne disease by predicting that the per capita number of insect bites should decrease within larger host groups. Although vector-borne diseases are common and can exert strong selective pressures on hosts, there have been few tests of the encounter-dilution effect in natural systems. We conducted an experimental test of the encounter-dilution hypothesis using the American robin (Turdus migratorius), a common host species for the West Nile virus (WNV), a mosquito-borne pathogen. By using sentinel hosts (house sparrows, Passer domesticus) caged in naturally occurring communal roosts in the suburbs of Chicago, we assessed sentinel host risk of WNV exposure inside and outside of roosts. We also estimated per capita host exposure to infected vectors inside roosts and outside of roosts. Sentinel birds caged inside roosts seroconverted to WNV more slowly than those outside of roosts, suggesting that social groups decrease per capita exposure to infected mosquitoes. These results therefore support the encounter-dilution hypothesis in a vector-borne disease system. Our results suggest that disease-related selective pressures on sociality may depend on the mode of disease transmission., (© 2014 The Author(s) Published by the Royal Society. All rights reserved.)

Background: Various ecological and physiological mechanisms might influence the probability that two or more pathogens may simultaneously or sequentially infect a host individual. Concurrent infections can have important consequences for host condition and fitness, including elevated mortality risks. In addition, interactions between coinfecting pathogens may have important implications for transmission dynamics., Methods: Here, we explore patterns of association between two common avian pathogens (West Nile virus and avian malaria parasites) among a suburban bird community in Chicago, IL, USA that share mosquito vectors. We surveyed 1714 individual birds across 13 species for both pathogens through established molecular protocols., Results: Field investigations of haemosporidian and West Nile virus (WNV) infections among sampled birds yielded an inverse association between WNV serostatus and Plasmodium infection status. This relationship occurred in adult birds but not in juveniles. There was no evidence for a relationship between Haemoproteus infection and WNV serostatus. We detected similar prevalence of Plasmodium among birds captured with active WNV infections and spatiotemporally paired WNV-naïve individuals of the same species, demonstrating that the two pathogens can co-infect hosts., Conclusions: Mechanisms explaining the negative association between WNV serostatus and Plasmodium infection status remain unclear and must be resolved through experimental infection procedures. However, our results highlight potential interactions between two common avian pathogens that may influence their transmission among hosts. This is especially relevant considering that West Nile virus is a common zoonotic pathogen with public health implications. Moreover, both pathogens are instructive models in infectious disease ecology, and infection with either has fitness consequences for their avian hosts.

West Nile Virus (WNV) is a mosquito-borne pathogen that impacts the health of its passerine bird hosts as well as incidentally infected humans in the United States. Intensive enzootic activity among the hosts and vectors does not always lead to human outbreaks, as is the situation throughout much of the southeastern United States. In Georgia, substantial yearly evidence of WNV in the mosquito vectors and avian hosts since 2001 has only led to 324 human cases. Although virus has been consistently isolated from mosquitoes trapped in Atlanta, GA, little is known about viral activity among the passerine hosts. A possible reason for the suppression of WNV spillover to humans is that viremic birds are absent from high human-use areas of the city. To test this hypothesis, multiseason, multihabitat, longitudinal WNV surveillance for active WNV viremia was conducted within the avian host community of urban Atlanta by collection of blood samples from wild passerine birds in five urban microhabitats. WNV was isolated from the serum of six blood samples collected from 630 (0.95%) wild passerine birds in Atlanta during 2010-2012, a proportion similar to that found in the Chicago, IL, area in 2005, when over 200 human cases were reported. Most of the viremic birds were Northern Cardinals, suggesting they may be of particular importance to the WNV transmission cycle in Georgia. Results indicated active WNV transmission in all microhabitats of urban Atlanta, except in the old-growth forest patches. The number of viremic birds was highest in Zoo Atlanta, where 3.5% of samples were viremic. Although not significant, these observations may suggest a possible transmission reduction effect of urban old-growth forests and a potential role in WNV amplification for Zoo Atlanta. Overall, spillover to humans remains a rare occurrence in urban Atlanta settings despite active WNV transmission in the avian population.

Culex flavivirus (CxFV) is an insect-specific flavivirus globally distributed in mosquitoes of the genus Culex. CxFV was positively associated with West Nile virus (WNV) infection in a case-control study of 268 mosquito pools from an endemic focus of WNV transmission in Chicago, United States. Specifically, WNV-positive Culex mosquito pools were four times more likely also to be infected with CxFV than were spatiotemporally matched WNV-negative pools. In addition, mosquito pools from residential sites characterized by dense housing and impermeable surfaces were more likely to be infected with CxFV than were pools from nearby urban green spaces. Further, 6/15 (40%) WNV-positive individual mosquitoes were also CxFV positive, demonstrating that both viruses can coinfect mosquitoes in nature. Phylogenetic analysis of CxFV from Chicago demonstrated a pattern similar to WNV, consisting of low global viral diversity and lack of geographic clustering. These results illustrate a positive ecological association between CxFV and WNV, and that coinfection of individual mosquitoes can occur naturally in areas of high flaviviral transmission. These conclusions represent a challenge to the hypothesis of super-infection exclusion in the CxFV/WNV system, whereby an established infection with one virus may interfere with secondary viral infection with a similar virus. This study suggests that infection with insect-specific flaviviruses such as CxFV may not exclude secondary infection with genetically distinct flaviviruses such as WNV, and that both viruses can naturally coinfect mosquitoes that are epidemic bridge vectors of WNV to humans.

The influence of host diversity on multi-host pathogen transmission and persistence can be confounded by the large number of species and biological interactions that can characterize many transmission systems. For vector-borne pathogens, the composition of host communities has been hypothesized to affect transmission; however, the specific characteristics of host communities that affect transmission remain largely unknown. We tested the hypothesis that vector host use and force of infection (i.e., the summed number of infectious mosquitoes resulting from feeding upon each vertebrate host within a community of hosts), and not simply host diversity or richness, determine local infection rates of West Nile virus (WNV) in mosquito vectors. In suburban Chicago, Illinois, USA, we estimated community force of infection for West Nile virus using data on Culex pipiens mosquito host selection and WNV vertebrate reservoir competence for each host species in multiple residential and semi-natural study sites. We found host community force of infection interacted with avian diversity to influence WNV infection in Culex mosquitoes across the study area. Two avian species, the American robin (Turdus migratorius) and the house sparrow (Passer domesticus), produced 95.8% of the infectious Cx. pipiens mosquitoes and showed a significant positive association with WNV infection in Culex spp. mosquitoes. Therefore, indices of community structure, such as species diversity or richness, may not be reliable indicators of transmission risk at fine spatial scales in vector-borne disease systems. Rather, robust assessment of local transmission risk should incorporate heterogeneity in vector host feeding and variation in vertebrate reservoir competence at the spatial scale of vector-host interaction.

West Nile virus has evolved in concert with its expansion across North America, but little is known about the evolutionary dynamics of the virus on local scales. We analysed viral nucleotide sequences from mosquitoes collected in 2005, 2006, and 2007 from a known transmission 'hot spot' in suburban Chicago, USA. Within this approximately 11 x 14 km area, the viral envelope gene has increased approximately 0.1% yr(-1) in nucleotide-level genetic diversity. In each year, viral diversity was higher in 'residential' sites characterized by dense housing than in more open 'urban green space' sites such as cemeteries and parks. Phylodynamic analyses showed an increase in incidence around 2005, consistent with a higher-than-average peak in mosquito and human infection rates that year. Analyses of times to most recent common ancestor suggest that WNV in 2005 and 2006 may have arisen predominantly from viruses present during 2004 and 2005, respectively, but that WNV in 2007 had an older common ancestor, perhaps indicating a predominantly mixed or exogenous origin. These results show that the population of WNV in suburban Chicago is an admixture of viruses that are both locally derived and introduced from elsewhere, containing evolutionary information aggregated across a breadth of spatial and temporal scales.

Nestling birds have been hypothesized to be important hosts for mosquito-borne arboviruses, but the role of nestlings for West Nile virus (WNV) amplification remains unclear. We sampled open-cup and cavity-nesting passerines in Chicago, Illinois, an area of intense WNV transmission, to determine infection rates in nestlings and mosquitoes, and to test whether mosquitoes are attracted to nesting birds. Analysis of Culex pipiens mosquito populations demonstrated WNV amplification to high mosquito infection rates during both years of the study near the locations where nestlings were sampled. Nevertheless, of 194 nestlings representing 12 species, only one 8-day-old house wren was positive for WNV RNA, and only one 10-day-old mourning dove was seropositive for antibodies to WNV, but at a low titer (1:20). The number of mosquitoes captured in nest box traps and control traps was not significantly different. These combined results suggest that nestling passerines play no evident role in WNV amplification and transmission in the Chicago area.

Recent field studies have suggested that the dynamics of West Nile virus (WNV) transmission are influenced strongly by a few key super spreader bird species that function both as primary blood hosts of the vector mosquitoes (in particular Culex pipiens) and as reservoir-competent virus hosts. It has been hypothesized that human cases result from a shift in mosquito feeding from these key bird species to humans after abundance of the key birds species decreases. To test this paradigm, we performed a mosquito blood meal analysis integrating host-feeding patterns of Cx. pipiens, the principal vector of WNV in the eastern United States north of the latitude 36 degrees N and other mosquito species with robust measures of host availability, to determine host selection in a WNV-endemic area of suburban Chicago, Illinois, during 2005-2007. Results showed that Cx. pipiens fed predominantly (83%) on birds with a high diversity of species used as hosts (25 species). American robins (Turdus migratorius) were marginally overused and several species were underused on the basis of relative abundance measures, including the common grackle (Quiscalus quiscula), house sparrow (Passer domesticus), and European starling (Sturnus vulgaris). Culex pipiens also fed substantially on mammals (19%; 7 species with humans representing 16%). West Nile virus transmission intensified in July of both years at times when American robins were heavily fed upon, and then decreased when robin abundance decreased, after which other birds species were selected as hosts. There was no shift in feeding from birds to mammals coincident with emergence of human cases. Rather, bird feeding predominated when the onset of the human cases occurred. Measures of host abundance and competence and Cx. pipiens feeding preference were combined to estimate the amplification fractions of the different bird species. Predictions were that approximately 66% of WNV-infectious Cx. pipiens became infected from feeding on just a few species of birds, including American robins (35%), blue jays (17%, Cyanocitta cristata), and house finches (15%, Carpodacus mexicanus).

Mosquitoes and birds were sampled for West Nile virus (WNV) in suburban Chicago, USA, in a "hot spot" of arboviral transmission. Viral genetic diversity within this area was similar to that within Illinois and the United States. Diversity was higher among viruses from mosquitoes than from birds, higher among viruses from birds in urban "green spaces" than from birds in residential areas, but lower among viruses from mosquitoes in green spaces than from mosquitoes in residential areas. Viral transmission was distance-limited, as evidenced by decreasing autocorrelation of WNV sequences with increasing geographic separation. The evolutionary rate of WNV within the study area between 21 July and 4 October 2005 was ten times higher than that for WNV across North America between 2002 and 2005. These results indicate that WNV transmission and evolutionary dynamics can vary seasonally and in response to fine-scale environmental conditions and landscape characteristics related to urbanization.

Epizootic transmission of West Nile virus (WNV) often intensifies rapidly leading to increasing risk of human infection, but the processes underlying amplification remain poorly understood. We quantified epizootic WNV transmission in communities of mosquitoes and birds in the Chicago, Illinois (USA) region during 2005 and 2006. Using quantitative polymerase chain reaction (PCR) methods, we detected WNV in 227 of 1195 mosquito pools (19%) in 2005 and 205 of 1685 (12%) in 2006; nearly all were Culex pipiens. In both years, mosquito infection rates increased rapidly in the second half of July to a peak of 59/1000 mosquitoes in 2005 and 33/1000 in 2006, and then declined slowly. Viral RNA was detected in 11 of 998 bird sera (1.1%) in 2005 and 3 of 1285 bird sera (<1%) in 2006; 11 of the 14 virus-positive birds were hatch-year birds. Of 540 hatch-year birds, 100 (18.5%) were seropositive in 2005, but only 2.8% (14/493) tested seropositive in 2006 for WNV antibodies using inhibition enzyme-linked immunosorbent assay (ELISA). We observed significant time series cross-correlations between mosquito infection rate and proportion of virus-positive birds, proportion of hatch-year birds captured in mist nets (significant in 2006 only), seroprevalence of hatch-year birds, and number of human cases in both seasons. These associations, coupled with the predominance of WNV infection and seropositivity in hatch-year birds, indicate a key role for hatch-year birds in the amplification of epizootic transmission of WNV, and in increasing human infection risk by facilitating local viral amplification.

Host-feeding patterns of Culex pipiens L. collected in southwest suburban Chicago in 2005 were studied using polymerase chain reaction (PCR) and DNA sequencing techniques. Culex spp. mosquitoes, most identified to Cx. pipiens and the remainder to Cx. restuans by PCR, had fed on 18 avian species, most commonly American robin (Turdus migratorious), house sparrow (Passer domesticus), and mourning dove (Zenaida macroura). Additional blood meals were derived from four mammal species, primarily humans and raccoons (Procyon lotor). During a West Nile virus (WNV) epidemic in 2005, West Nile virus (WNV) RNA was detected in heads and thoraces of five Cx. pipiens (n = 335, 1.5%) using quantitative PCR. The hosts of these virus-infected, blood-fed mosquitoes included two American robins, one house sparrow, and one human. This is the first report of a WNV-infected Cx. pipiens mosquito collected during an epidemic of WNV that was found to have bitten a human. These results fulfill a criterion for incrimination of Cx. pipiens as a bridge vector.

Background: West Nile virus infection in humans in urban areas of the Midwestern United States has exhibited strong spatial clustering during epidemic years. We derived urban landscape classes from the physical and socio-economic factors hypothesized to be associated with West Nile Virus (WNV) transmission and compared those to human cases of illness in 2002 in Chicago and Detroit. The objectives were to improve understanding of human exposure to virus-infected mosquitoes in the urban context, and to assess the degree to which environmental factors found to be important in Chicago were also found in Detroit., Results: Five urban classes that partitioned the urban space were developed for each city region. The classes had many similarities in the two settings. In both regions, the WNV case rate was considerably higher in the urban class associated with the Inner Suburbs, where 1940-1960 era housing dominates, vegetation cover is moderate, and population density is moderate. The land cover mapping approach played an important role in the successful and consistent classification of the urban areas., Conclusion: The analysis demonstrates how urban form and past land use decisions can influence transmission of a vector-borne virus. In addition, the results are helpful to develop hypotheses regarding urban landscape features and WNV transmission, they provide a structured method to stratify the urban areas to locate representative field study sites specifically for WNV, and this analysis contributes to the question of how the urban environment affects human health.