Apparent increase of reported hemorrhagic disease in the midwestern and northeastern USA.

We investigated temporal and spatial trends in reporting of hemorrhagic disease (HD) in the midwestern and northeastern US using a 33-yr (1980-2012) questionnaire-based data set. This data set was supported by an additional 19 yr (1994-2012) of bluetongue virus (BTV) and epizootic hemorrhagic disease virus (EHDV) isolation results from clinically affected white-tailed deer (Odocoileus virginianus) in these regions. Both the number of counties that were reported positive for HD and the northern latitudinal range of reported HD increased with time. A similar increase was observed with both the number of states annually reporting HD and the number of counties where HD was reported. Large-scale outbreaks occurred in 1988, 1996, 2007, and 2012, and the scale of these individual outbreaks also increased with time. The predominant virus isolated from these regions was EHDV-2, but the prevalence of EHDV-6, which was first detected in 2006, appears to be increasing. Temporally, the extent of regional HD reporting was correlated with regional drought conditions. The significance of increases in reported HD and the incursions and establishment of new BTV and EHDV in the US currently are unknown.

Annual survival of ruddy turnstones is not affected by natural infection with low pathogenicity avian influenza viruses.

The population of ruddy turnstones (Arenaria interpres morinella) that migrates through Delaware Bay has undergone severe declines in recent years, attributable to reduced availability of horseshoe crab (Limulus polyphemus) eggs at this critical spring migration stopover site. Concurrently, this population has experienced annual low pathogenicity avian influenza virus (AIV) epidemics at this same site. Using a prospective cohort study design with birds individually flagged during May-June 2006-2008, we evaluated resighting rates (a proxy for annual survival) between AIV-infected and uninfected birds at 1 yr after capture, testing, and measurement. Overall resighting rate was 46%, which varied by year and increased with relative mass of the bird when captured. Resighting rates were not different between AIV-infected and uninfected birds in any period. In multivariate analyses, infection status was also unrelated to resighting rate after controlling for year, day, state, sex, body size, mass index, or whether the bird was blood-sampled. Thus, apparent annual survival in ruddy turnstones was not reduced by AIV infection at this migratory stopover. However, it is unknown whether intestinal AIV infection might cause subtle reductions in weight gain which could negatively influence reproduction.

Avian influenza virus infection dynamics in shorebird hosts.

To gain insight into avian influenza virus (AIV) transmission, exposure, and maintenance patterns in shorebirds at Delaware Bay during spring migration, we examined temporal AIV prevalence trends in four Charadriiformes species with the use of serial cross-sectional data from 2000 through 2008 and generalized linear and additive models. Prevalence of AIV in Ruddy Turnstones (Arenaria interpres morinella) increased after arrival, peaked in mid-late May, and decreased prior to departure. Antibody prevalence also increased over this period; together, these results suggested local infection and recovery prior to departure. Red Knots (Calidris canutus rufa), Sanderlings (Calidris alba), and Laughing Gulls (Leucophaeus atricilla) were rarely infected, but dynamic changes in antibody prevalence differed among species. In Red Knots, declining antibody prevalence over the stopover period suggested AIV exposure prior to arrival at Delaware Bay with limited infection at this site. Antibody prevalence was consistently high in Laughing Gulls and low in Sanderlings. Both viral prevalence and antibody prevalence in Sanderlings varied directly with those in turnstones, suggesting virus spillover to Sanderlings. Results indicate that, although hundreds of thousands of birds concentrate at Delaware Bay during spring, dynamics of AIV infection differ among species, perhaps due to differences in susceptibility, potential for contact with AIV at this site, or prior exposure. Additionally, Ruddy Turnstones possibly act as a local AIV amplifying host rather than a reservoir.

Avian influenza viruses and avian paramyxoviruses in wintering and breeding waterfowl populations in North Carolina, USA.

Although wild ducks are recognized reservoirs for avian influenza viruses (AIVs) and avian paramyxoviruses (APMVs), information related to the prevalence of these viruses in breeding and migratory duck populations on North American wintering grounds is limited. Wintering (n=2,889) and resident breeding (n=524) ducks were sampled in North Carolina during winter 2004-2006 and summer 2005-2006, respectively. Overall prevalence of AIV was 0.8% and restricted to the winter sample; however, prevalence in species within the genus Anas was 1.3% and was highest in Black Ducks (7%; Anas rubripes) and Northern Shovelers (8%; Anas clypeata). Of the 24 AIVs, 16 subtypes were detected, representing nine hemagglutinin and seven neuraminidase subtypes. Avian paramyxoviruses detected in wintering birds included 18 APMV-1s, 15 APMV-4s, and one APMV-6. During summers 2005 and 2006, a high prevalence of APMV-1 infection was observed in resident breeding Wood Ducks (Aix sponsa) and Mallards (Anas platyrhynchos).

Avian paramyxoviruses in shorebirds and gulls.

There are nine serotypes of avian paramyxovirus (APMV), including APMV-1, or Newcastle disease virus. Although free-flying ducks and geese have been extensively monitored for APMV, limited information is available for species in the order Charadriiformes. From 2000 to 2005 we tested cloacal swabs from 9,128 shorebirds and gulls (33 species, five families) captured in 10 states within the USA and in three countries in the Caribbean and South America. Avian paramyxoviruses were isolated from 60 (0.7%) samples by inoculation of embryonating chicken eggs; isolates only included APMV-1 and APMV-2. Two isolates (APMV-2) were made from gulls and 58 isolates (APMV-1 [41 isolates] and APMV-2 [17 isolates]) were made from shorebirds. All of the positive shorebirds were sampled at Delaware Bay (Delaware and New Jersey) and 45 (78%) of these isolates came from Ruddy Turnstones (Arenaria interpres). The APMV-1 infection rate was higher among Ruddy Turnstones compared with other shorebird species and varied by year. Avian paramyxovirus-2 was isolated from two of 394 (0.5%) Ruddy Turnstones at Delaware Bay in 2001 and from 13 of 735 (1.8%) Ruddy Turnstones during 2002. For both APMV-1 and APMV-2, infection rates were higher among Ruddy Turnstones sampled on the south shore of Delaware Bay compared to north shore populations. This spatial variation may be related to local movements of Ruddy Turnstones within this ecosystem. The higher prevalence of APMV in Ruddy Turnstones mirrors results observed for avian influenza viruses in shorebirds and may suggest similar modes of transmission.

Canada geese and the epidemiology of avian influenza viruses.

Canada geese (Branta canadensis) are numerous, highly visible, and widely distributed in both migratory and resident populations in North America; as a member of the order Anseriformes, they are often suggested as a potential reservoir and source for avian influenza (AI) viruses. To further examine the role of Canada Geese in the ecology of AI, we re-evaluated existing literature related to AI virus in this species and tested breeding populations of Canada Geese from three states (Georgia, West Virginia, and Minnesota, USA) by virus isolation and serology. The ability of AI virus to persist in goose feces under experimental conditions also was evaluated as an additional measure of the potential for this species to serve as an AI virus reservoir. Virus was not isolated from 1,668 cloacal swabs and type-specific antibody prevalence was low (4/335, 1.2%). Finally, under experimental conditions, AI virus persistence in goose feces and in water contaminated with goose feces was limited as compared to published estimates from duck feces and water. Our results are consistent with historic reports of a low prevalence of AI virus infection in this species, and we suggest that Canada Geese play a minor, if any, role as a reservoir for low pathogenic AI viruses that naturally circulate in wild bird populations.

Avian influenza virus in aquatic habitats: what do we need to learn?

Although aquatic habitats utilized by wild and domestic birds potentially can provide a bridge for avian influenza virus (AIV) transmission among many diverse hosts, the factors controlling environmental persistence and transmission via these habitats are poorly understood. AIV has been detected in water samples collected in the field, and under experimental laboratory conditions, these viruses can remain infective in water for periods of time that would be consistent with an environmental reservoir. However, the application of laboratory results to field realities is complicated by the complexity and scale of these systems. In this brief review, we present a summary of existing research on the environmental tenacity of AIV, provide an example of the challenges associated with the application of laboratory results to the field realities associated with detection of AIV from environmental sources, and identify gaps in our current understanding of the factors potentially affecting AIV infectivity in the environment, specifically from aquatic habitats utilized by wild birds.

Phylogenetic comparison of the S10 genes of recent isolates of bluetongue virus from the United States and French Martinique Island.

The sequences of the S10 genes of 28 recent isolates (1994-2004) of bluetongue virus (BTV) from the United States (US) and French Martinique Island (2006) in the Caribbean Basin were compared in phylogenetic analyses to those of viruses previously isolated in the same regions. Although the analyses segregated the recent virus isolates from the two regions into distinct topotype clusters, the analyses also confirm that viruses from the US and the Caribbean Basin/Central America can share similar S10 genes despite the fact that distinct constellations of BTV serotypes occur in the two regions.

First report of bluetongue virus serotype 1 isolated from a white-tailed deer in the United States.

In November 2004, tissues were collected from a hunter-killed white-tailed deer in St. Mary Parish, Louisiana. Bluetongue virus (BTV) was isolated from the tissues; however, the isolate could not be identified as any of the US domestic serotypes. Subsequent testing by virus neutralization using serotype-specific antiserum tentatively identified the isolate as BTV serotype 1 (BTV-1), which had not previously been found in the United States. Primers were designed based on the sequence of an outer capsid protein gene of a South African BTV-1 strain. Reverse transcription-polymerase chain reaction testing with the BTV-1 primers and product sequencing confirmed the Louisiana isolate as BTV-1. This is the first report of BTV-1 in the United States.