Duck plague epizootics in the United States, 1967-1995

In 1967, the first confirmed diagnosis of duck plague (DP) in the USA was made from pekin ducks (Anas platyrhynchos domesticus) on commercial duck farms on Long Island, New York. Within 10 mo, DP was confirmed as the cause of death in migratory waterfowl on a Long Island bay. This paper reviews 120 DP epizootics reported from 1967 to 1995 that involved waterfowl species native to North America or were reported in areas with free-flying waterfowl at risk. Duck plague epizootics occurred in 21 states with the greatest number reported in Maryland (29), New York (18), California (16), and Pennsylvania (13). The greatest frequency of epizootics (86%) was detected during the months of March to June. At least 40 waterfowl species were affected with the highest frequency of epizootics reported in captive or captive-reared ducks including muscovy ducks (Cairina moschata) (68%), mallard ducks (A. platyrhynchos) (18%) and black ducks (A. rubripes) (14%). The greatest number of waterfowl died in three epizootics that involved primarily migratory birds in 1967 and 1994 in New York (USA) and 1973 in South Dakota (USA). The greatest number of DP epizootics reported since 1967 appear to have involved flocks of non-migratory rather than migratory waterfowl; therefore, in our opinion it remains unknown if DP is enzootic in either non-migratory or migratory waterfowl.     

Oseltamivir-Resistant Influenza A (H1N1) Virus Strain with an H274Y Mutation in Neuraminidase Persists without Drug Pressure in Infected Mallards

Influenza A virus (IAV) has its natural reservoir in wild waterfowl, and emerging human IAVs often contain gene segments from avian viruses. The active drug metabolite of oseltamivir (oseltamivir carboxylate [OC]), stockpiled as Tamiflu for influenza pandemic preparedness, is not removed by conventional sewage treatment and has been detected in river water. There, it may exert evolutionary pressure on avian IAV in waterfowl, resulting in the development of resistant viral variants. A resistant avian IAV can circulate among wild birds only if resistance does not restrict viral fitness and if the resistant virus can persist without continuous drug pressure. In this in vivo mallard (Anas platyrhynchos) study, we tested whether an OC-resistant avian IAV (H1N1) strain with an H274Y mutation in the neuraminidase (NA-H274Y) could retain resistance while drug pressure was gradually removed. Successively infected mallards were exposed to decreasing levels of OC, and fecal samples were analyzed for the neuraminidase sequence and phenotypic resistance. No reversion to wild-type virus was observed during the experiment, which included 17 days of viral transmission among 10 ducks exposed to OC concentrations below resistance induction levels. We conclude that resistance in avian IAV that is induced by exposure of the natural host to OC can persist in the absence of the drug. Thus, there is a risk that human-pathogenic IAVs that evolve from IAVs circulating among wild birds may contain resistance mutations. An oseltamivir-resistant pandemic IAV would pose a substantial public health threat. Therefore, our observations underscore the need for prudent oseltamivir use, upgraded sewage treatment, and surveillance for resistant IAVs in wild birds.     

An epornitic of duck plague on a Wisconsin game farm.

In April, 1973, an acute disease with a high rate of mortality appeared in a flock of 233 ducks and geese at a private game farm. Most of the flock (220) were black ducks (Anas rubripes) and mortality was restricted to them. In May, the remaining live birds were placed in isolation but mortality continued in black ducks and occurred in other species. The overall rate of mortality for black ducks was 93% and the case fatality rate was 97%. No hemorrhaging from either the bill or vent was observed. The most commonly observed gross lesions were extensive fibrino-necrotic plaques covering the mucosal surface of the esophagus, posterior colon and cloaca. Petechial and ecchymotic hemorrhages on visceral organs, particularly the heart, were also common. Virus isolation was attempted from tissues of three black ducks. Duck plague virus was isolated from liver, kidney, spleen and intestine of each. Sixteen black ducks survived the outbreak. Seven of these birds had significant levels of neutralizing antibody to duck plague virus.     

Complete genome sequence of an H7N3 avian influenza virus isolated from ducks in southern China

We report here the complete genomic sequence of an H7N3 avian influenza virus (AIV) isolate, which was obtained from duck in 1996. This is the first report of this subtype of AIV being isolated from duck in Guangdong of Southern China. Genomic sequence and phylogenetic analyses showed that it was highly homologous with the wild bird virus A/ruddy turnstone/Delaware Bay/135/1996 (H7N3) and that all eight genes of this virus belonged to the North America gene pool. The availability of genome sequences is helpful to further investigations of epidemiology and evolution of AIV between waterfowl and wild birds.     

Do Canada geese (Branta canadensis Linnaeus, 1758) carry infectious agents for birds and man?

Currently, large groups of Canada geese (Branta canadensis Linnaeus, 1758) aggregate in recreational areas of north-western Germany. Questions have arisen as to whether these birds represent a special risk factor as a source of zoonotic agents for humans and as a source of viruses, causing notifiable or reportable diseases, for domestic poultry and waterfowl. To answer these questions, a total of 289 eggs were collected in 2002 and 2003 on a recreation site and assayed. Chlamydia psittaci was not isolated and neither was chlamydial antigen detected by polymerase chain reaction. All virus-isolation attempts were unsuccessful. Neither Salmonella spp. nor Campylobacter spp. was isolated from embryonic tissues, chorioallantoic membranes or yolk-sac membranes. The presence of antibodies against Newcastle disease virus and influenza A virus (haemagglutinin subtypes H5 and H7) was demonstrated in egg yolk. Antibodies were also detected against the egg-drop syndrome 1976 and duck plague viruses. It is concluded that further surveillance studies are needed for a reliable risk assessment.     

Oseltamivir Resistance in Influenza A(H6N2) Caused by an R292K Substitution in Neuraminidase Is Not Maintained in Mallards without Drug Pressure

Background

Wild waterfowl is the natural reservoir of influenza A virus (IAV); hosted viruses are very variable and provide a source for genetic segments which can reassort with poultry or mammalian adapted IAVs to generate novel species crossing viruses. Additionally, wild waterfowl act as a reservoir for highly pathogenic IAVs. Exposure of wild birds to the antiviral drug oseltamivir may occur in the environment as its active metabolite can be released from sewage treatment plants to river water. Resistance to oseltamivir, or to other neuraminidase inhibitors (NAIs), in IAVs of wild waterfowl has not been extensively studied.

Aim and Methods

In a previous in vivo Mallard experiment, an influenza A(H6N2) virus developed oseltamivir resistance by the R292K substitution in the neuraminidase (NA), when the birds were exposed to oseltamivir. In this study we tested if the resistance could be maintained in Mallards without drug exposure. Three variants of resistant H6N2/R292K virus were each propagated during 17 days in five successive pairs of naïve Mallards, while oseltamivir exposure was decreased and removed. Daily fecal samples were analyzed for viral presence, genotype and phenotype.

Results and Conclusion

Within three days without drug exposure no resistant viruses could be detected by NA sequencing, which was confirmed by functional NAI sensitivity testing. We conclude that this resistant N2 virus could not compete in fitness with wild type subpopulations without oseltamivir drug pressure, and thus has no potential to circulate among wild birds. The results of this study contrast to previous observations of drug induced resistance in an avian H1N1 virus, which was maintained also without drug exposure in Mallards. Experimental observations on persistence of NAI resistance in avian IAVs resemble NAI resistance seen in human IAVs, in which resistant N2 subtypes do not circulate, while N1 subtypes with permissive mutations can circulate without drug pressure. We speculate that the phylogenetic group N1 NAs may easier compensate for NAI resistance than group N2 NAs, though further studies are needed to confirm such conclusions.     

The epidemiology of the highly pathogenic H5N1 avian influenza in Mute Swan (Cygnus olor) and other Anatidae in the Dombes region (France), 2006

In February 2006, a highly pathogenic avian influenza (HPAI) H5N1 virus was isolated from Common Pochards (Aythia ferina) in the Dombes region of France, an important migrating and wintering waterfowl area. Thereafter, HPAI H5N1 virus was isolated from 39 swab pools collected from dead waterfowl found in the Dombes, but only from three pooled samples collected outside of this area but located on the same migration flyway. A single turkey farm was infected in the Dombes. The epizootic lasted 2 mo and was restricted to the Dombes area. Virus-positive pools were detected in 20 of 1,200 ponds and infected Mute Swans (Cygnus olor) represented 82% of the virus-positive pools. Other infected species included Common Pochard (n=4), Grey Heron (Ardea cinerea, n=1), Eurasian Buzzard (Buteo buteo, n=1), and Greylag Goose (Anser anser, n=1). Despite intensive monitoring during and after the outbreak, HPAI H5N1 virus was not isolated from healthy wild birds. Our results are consistent with an HPAI H5N1-virus introduction into the Dombes via migrating ducks. These birds could have been pushed west by a severe cold spell in central Europe where the virus had already been detected. The Mute Swan served as an excellent epidemiologic sentinel during this outbreak; swans appear to be highly sensitive to infection with these viruses and swan mortality was easy to detect. During the outbreak, the mortality rates for wild birds remained moderate and the virus affected a limited number of species.     

A solitary case of duck plague in a wild mallard

Duck plague was diagnosed on the basis of pathology and virus isolation in a wild female mallard Anas platyrhynchos found dead near Saskatoon, Saskatchewan. Day-old Pekin ducklings and one of two adult mallards died with lesions typical of duck plague following inoculation of tissue from the wild bird. This is believed to be the only reported case of duck plague in a wild bird since a major outbreak occurred in South Dakota in 1973, and the fourth such report in North America.     

Environmental and demographic determinants of avian influenza viruses in waterfowl across the contiguous United States

Outbreaks of avian influenza in North American poultry have been linked to wild waterfowl. A first step towards understanding where and when avian influenza viruses might emerge from North American waterfowl is to identify environmental and demographic determinants of infection in their populations. Laboratory studies indicate water temperature as one determinant of environmental viral persistence and we explored this hypothesis at the landscape scale. We also hypothesized that the interval apparent prevalence in ducks within a local watershed during the overwintering season would influence infection probabilities during the following breeding season within the same local watershed. Using avian influenza virus surveillance data collected from 19,965 wild waterfowl across the contiguous United States between October 2006 and September 2009 We fit Logistic regression models relating the infection status of individual birds sampled on their breeding grounds to demographic characteristics, temperature, and interval apparent prevalence during the preceding overwintering season at the local watershed scale. We found strong support for sex, age, and species differences in the probability an individual duck tested positive for avian influenza virus. In addition, we found that for every seven days the local minimum temperature fell below zero, the chance an individual would test positive for avian influenza virus increased by 5.9 percent. We also found a twelve percent increase in the chance an individual would test positive during the breeding season for every ten percent increase in the interval apparent prevalence during the prior overwintering season. These results suggest that viral deposition in water and sub-freezing temperatures during the overwintering season may act as determinants of individual level infection risk during the subsequent breeding season. Our findings have implications for future surveillance activities in waterfowl and domestic poultry populations. Further study is needed to identify how these drivers might interact with other host-specific infection determinants, such as species phylogeny, immunological status, and behavioral characteristics.     

Australia as a global sink for the genetic diversity of avian influenza A virus

Most of our understanding of the ecology and evolution of avian influenza A virus (AIV) in wild birds is derived from studies conducted in the northern hemisphere on waterfowl, with a substantial bias towards dabbling ducks. However, relevant environmental conditions and patterns of avian migration and reproduction are substantially different in the southern hemisphere. Through the sequencing and analysis of 333 unique AIV genomes collected from wild birds collected over 15 years we show that Australia is a global sink for AIV diversity and not integrally linked with the Eurasian gene pool. Rather, AIV are infrequently introduced to Australia, followed by decades of isolated circulation and eventual extinction. The number of co-circulating viral lineages varies per subtype. AIV haemagglutinin (HA) subtypes that are rarely identified at duck-centric study sites (H8-12) had more detected introductions and contemporary co-circulating lineages in Australia. Combined with a lack of duck migration beyond the Australian-Papuan region, these findings suggest introductions by long-distance migratory shorebirds. In addition, on the available data we found no evidence of directional or consistent patterns in virus movement across the Australian continent. This feature corresponds to patterns of bird movement, whereby waterfowl have nomadic and erratic rainfall-dependant distributions rather than consistent intra-continental migratory routes. Finally, we detected high levels of virus gene segment reassortment, with a high diversity of AIV genome constellations across years and locations. These data, in addition to those from other studies in Africa and South America, clearly show that patterns of AIV dynamics in the Southern Hemisphere are distinct from those in the temperate north.     

Spatial and temporal changes in prevalence of a cloacal cestode in wintering waterfowl along the Gulf Coast of Texas

The cloacal cestode Cloacotaenia megalops is one of the most common helminths of waterfowl. We investigated the effect of this parasite on the body condition of wintering waterfowl populations and compared prevalence among age-sex classes, over time and between habitat types on the upper Gulf Coast of Texas (USA) from October 1986-February 2000. Greater than 9,500 birds of 25 waterfowl species were examined for the parasite. There was no statistical difference (P > 0.05) in body condition between birds with and without the parasite. Average prevalence was lowest for geese (mean = 3.7%) versus 21 to 71% in duck species. Average prevalence was similar (P = 0.81) between diving ducks (mean = 46.9%) and puddle ducks (mean = 43.9%). Prevalence varied among age-sex classes and was related to sex rather than age. Variation among age-sex classes suggests differences in diet between sexes of duck species on the wintering grounds. There was no evidence for declining prevalence over the wintering period. Prevalence differed (P < 0.05) between collection sites, and thereby habitat types, for several species. Temporal trends indicate stable prevalence of C. megalops for diving ducks and increasing prevalence for puddle ducks. The increasing trend for puddle ducks may indicate declining habitat conditions resulting in increased exposure to the intermediate ostracod host.     

An outbreak of duck virus enteritis (duck plague) in Alberta.

Duck plague (Duck virus enteritis) was disgnosed in a resident population of Muscovy ducks (Cairina moschata) on a small game farm in Alberta. This disease has not been reported previously in Canada. Clinical signs consisted of cyanosis, depression and acute death. Necropsy of two Muscovy ducks revealed lesions typical of the disease. There were ulcerations with pseudomembranes in the small intestine, ulcerations with caseous plaques in the esophagus and eosinophilic intranuclear inclusion bodies in the spleen. Clinical disease with mortality was reproduced in young ducklings injected with tissue homogenates from field cases. All surviving inoculated ducklings seroconverted to highly significant titres of neutralizing antibodies to duck virus enteritis (DVE) virus. All attempts to isolate the agent in embryonating duck eggs or primary tissues cultures of duck and chicken kidney were negative. Identification of the DVE virus was accomplished by serum neutralization with ducklings as the host system.     

Duck hepatitis B virus infection of Muscovy duck hepatocytes and nature of virus resistance in vivo.

To test the hypothesis that in vivo resistance to hepadnavirus infection was due to resistance of host hepatocytes, we isolated hepatocytes from Muscovy ducklings and chickens, birds that have been shown to be resistant to duck hepatitis B virus (DHBV) infection, and attempted to infect them in vitro with virus from congenitally infected Pekin ducks. Chicken hepatocytes were resistant to infection, but we were able to infect approximately 1% of Muscovy duck hepatocytes in culture. Infection requires prolonged incubation with virus at 37 degrees C. Virus spread occurs in the Muscovy cultures, resulting in 5 to 10% DHBV-infected hepatocytes by 3 weeks after infection. The relatively low rate of accumulation of DHBV DNA in infected Muscovy hepatocyte cultures is most likely due to inefficient spread of virus infection; in the absence of virus spread, the rates of DHBV replication in Pekin and Muscovy hepatocyte cultures are similar. 5-Azacytidine treatment can induce susceptibility to DHBV infection in resistant primary Pekin hepatocytes but appears to have no similar effect in Muscovy cultures. The relatively inefficient infection of Muscovy duck hepatocytes that we have described may account for the absence of a detectable viremia in Muscovy ducklings experimentally infected with DHBV.     

Are ducks contributing to the endemicity of highly pathogenic H5N1 influenza virus in Asia?

Wild waterfowl are the natural reservoir of all influenza A viruses, and these viruses are usually nonpathogenic in these birds. However, since late 2002, H5N1 outbreaks in Asia have resulted in mortality among waterfowl in recreational parks, domestic flocks, and wild migratory birds. The evolutionary stasis between influenza virus and its natural host may have been disrupted, prompting us to ask whether waterfowl are resistant to H5N1 influenza virus disease and whether they can still act as a reservoir for these viruses. To better understand the biology of H5N1 viruses in ducks and attempt to answer this question, we inoculated juvenile mallards with 23 different H5N1 influenza viruses isolated in Asia between 2003 and 2004. All virus isolates replicated efficiently in inoculated ducks, and 22 were transmitted to susceptible contacts. Viruses replicated to higher levels in the trachea than in the cloaca of both inoculated and contact birds, suggesting that the digestive tract is not the main site of H5N1 influenza virus replication in ducks and that the fecal-oral route may no longer be the main transmission path. The virus isolates' pathogenicities varied from completely nonpathogenic to highly lethal and were positively correlated with tracheal virus titers. Nevertheless, the eight virus isolates that were nonpathogenic in ducks replicated and transmitted efficiently to na?ve contacts, suggesting that highly pathogenic H5N1 viruses causing minimal signs of disease in ducks can propagate silently and efficiently among domestic and wild ducks in Asia and that they represent a serious threat to human and veterinary public health.     

The Recent Establishment of North American H10 Lineage Influenza Viruses in Australian Wild Waterfowl and the Evolution of Australian Avian Influenza Viruses

Influenza A H10N7 virus with a hemagglutinin gene of North American origin was detected in Australian chickens and poultry abattoir workers in New South Wales, Australia, in 2010 and in chickens in Queensland, Australia, on a mixed chicken and domestic duck farm in 2012. We investigated their genomic origins by sequencing full and partial genomes of H10 viruses isolated from wild aquatic birds and poultry in Australia and analyzed them with all available avian influenza virus sequences from Oceania and representative viruses from North America and Eurasia. Our analysis showed that the H10N7 viruses isolated from poultry were similar to those that have been circulating since 2009 in Australian aquatic birds and that their initial transmission into Australia occurred during 2007 and 2008. The H10 viruses that appear to have developed endemicity in Australian wild aquatic birds were derived from several viruses circulating in waterfowl along various flyways. Their hemagglutinin gene was derived from aquatic birds in the western states of the United States, whereas the neuraminidase was closely related to that from viruses previously detected in waterfowl in Japan. The remaining genes were derived from Eurasian avian influenza virus lineages. Our analysis of virological data spanning 40 years in Oceania indicates that the long-term evolutionary dynamics of avian influenza viruses in Australia may be determined by climatic changes. The introduction and long-term persistence of avian influenza virus lineages were observed during periods with increased rainfall, whereas bottlenecks and extinction were observed during phases of widespread decreases in rainfall. These results extend our understanding of factors affecting the dynamics of avian influenza and provide important considerations for surveillance and disease control strategies.     

Building the Foundation for International Conservation Planning for Breeding Ducks across the U.S. and Canadian Border

We used publically available data on duck breeding distribution and recently compiled geospatial data on upland habitat and environmental conditions to develop a spatially explicit model of breeding duck populations across the entire Prairie Pothole Region (PPR). Our spatial population models were able to identify key areas for duck conservation across the PPR and predict between 62.1 – 79.1% (68.4% avg.) of the variation in duck counts by year from 2002 – 2010. The median difference in observed vs. predicted duck counts at a transect segment level was 4.6 ducks. Our models are the first seamless spatially explicit models of waterfowl abundance across the entire PPR and represent an initial step toward joint conservation planning between Prairie Pothole and Prairie Habitat Joint Ventures. Our work demonstrates that when spatial and temporal variation for highly mobile birds is incorporated into conservation planning it will likely increase the habitat area required to support defined population goals. A major goal of the current North American Waterfowl Management Plan and subsequent action plan is the linking of harvest and habitat management. We contend incorporation of spatial aspects will increase the likelihood of coherent joint harvest and habitat management decisions. Our results show at a minimum, it is possible to produce spatially explicit waterfowl abundance models that when summed across survey strata will produce similar strata level population estimates as the design-based Waterfowl Breeding Pair and Habitat Survey (r² = 0.977). This is important because these design-based population estimates are currently used to set duck harvest regulations and to set duck population and habitat goals for the North American Waterfowl Management Plan. We hope this effort generates discussion on the important linkages between spatial and temporal variation in population size, and distribution relative to habitat quantity and quality when linking habitat and population goals across this important region.     

An annotated checklist of pathogenic microorganisms associated with migratory birds

The potential for transport and dissemination of certain pathogenic microorganisms by migratory birds is of concern. Migratory birds might be involved in dispersal of microorganisms as their biological carriers, mechanical carriers, or as carriers of infected hematophagous ecto-parasites (e.g., ixodid ticks). Many species of microorganisms pathogenic to homeothermic vertebrates including humans have been associated with free-living migratory birds. Migratory birds of diverse species can play significant roles in the ecology and circulation of some arboviruses (e.g., eastern and western equine encephalomyelitis and Sindbis alphaviruses, West Nile and St. Louis encephalitis flaviviruses), influenza A virus, Newcastle disease virus, duck plague herpes-virus, Chlamydophila psittaci, Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato, Campylobacter jejuni, Salmonella enterica, Pasteurella multocida, Mycobacterium avium, Candida spp., and avian hematozoans. The efficiency of dispersal of pathogenic microorganisms depends on a wide variety of biotic and abiotic factors affecting the survival of the agent in, or disappearance from, a habitat or ecosystem in a new geographic area.     

The role of breeding phenology and aggregation of waterfowl on avian influenza dynamics in southern Africa

Recent outbreaks of highly pathogenic avian influenza virus (AIV) in birds, humans and other mammalian species calls for a better understanding of virus dynamics in wild bird species and populations that act as maintenance hosts. Host ecology influences the transmission of pathogens and can be used to explore and infer pathogen dynamics. Most of the ecological processes proposed to explain AIV transmission in wild birds have been derived from studies conducted in the temperate and boreal regions of the northern hemisphere. We evaluate the role of two key drivers of AIV dynamics in a waterfowl community in Zimbabwe (southern Africa): (1) the recruitment of young birds and (2) the seasonal aggregation of birds. We analyse the seasonal variation of AIV prevalence in waterfowl and overlay these data with the phenology of reproduction and the seasonal variation in the local abundance of these species. We find that the breeding period of southern Afrotropical waterfowl species is more extended and somewhat less synchronized among species in the community than is the case in temperate and boreal waterfowl communities. Young birds are recorded at most times of the year, and these immunologically naïve individuals can therefore act as new hosts for AIV throughout the year within the wild bird population. Although host aggregation peaks in the cold‐dry to hot‐dry season, birds still aggregate throughout the year and this potentially spreads the opportunities for first infection of juveniles and other naïve birds temporally. We did not find a relationship between season, AIV prevalence in waterfowl, the influx of juveniles or the gradual aggregation of birds during the dry season. Therefore, the main drivers of AIV dynamics (juvenile influx and host abundance/aggregation), although present in Afrotropical regions, could not explain the AIV seasonal patterns in our study in contrast to results reported from temperate and boreal regions. These differences imply variation in the risk of AIV circulation in waterfowl and in the risk of spread to poultry, other animals or humans.     

Hunting disturbance on a large shallow lake: the effectiveness of waterfowl refuges

Disturbance is most likely to have an impact during those periods of the annual cycle when food is scarce and birds have difficulty in meeting their energy requirements. The provision of disturbance-free refuges has been shown to enhance the abundance and diversity of waterfowl wintering on such sites. Lough Neagh, a large shallow lake in Northern Ireland, hosts internationally important numbers of wintering waterfowl, the most numerous being Common Pochard Aythya ferina , Tufted Duck A. fuligula , Greater Scaup A. marila and Common Goldeneye Bucephala clangula. Hunting is the predominant winter recreational activity. A small number of refuges have been provided to limit the effects of shooting disturbance on the wintering populations. The use of one of these refuges (Doss Bay) was studied during the winter of 1997/8 and compared with a non-refuge site (Brockish Bay) during the winter of 1998/9. Shooting intensity was greater at weekends than midweek, and significantly more birds used the refuge at weekends than midweek during the shooting season. In contrast, significantly fewer birds were observed in Brockish Bay at weekends. This trend ceased when the shooting season closed, suggesting that the effect was due to shooting disturbance. Furthermore, significantly fewer birds used Doss Bay after the shooting season had closed, whereas significantly more birds were observed at Brockish Bay. Shooting disturbance had the greatest impact on dabbling duck species and rails at both sites. Diving ducks moved away from shoreline disturbance to shallow areas where they could still feed. The value of shoreline refuges for waterfowl populations on lakes is discussed.