Dataset Information

Disease dynamics and bird migration--linking mallards Anas platyrhynchos and subtype diversity of the influenza A virus in time and space.

ABSTRACT: The mallard Anas platyrhynchos is a reservoir species for influenza A virus in the northern hemisphere, with particularly high prevalence rates prior to as well as during its prolonged autumn migration. It has been proposed that the virus is brought from the breeding grounds and transmitted to conspecifics during subsequent staging during migration, and so a better understanding of the natal origin of staging ducks is vital to deciphering the dynamics of viral movement pathways. Ottenby is an important stopover site in southeast Sweden almost halfway downstream in the major Northwest European flyway, and is used by millions of waterfowl each year. Here, mallards were captured and sampled for influenza A virus infection, and positive samples were subtyped in order to study possible links to the natal area, which were determined by a novel approach combining banding recovery data and isotopic measurements (?(2)H) of feathers grown on breeding grounds. Geographic assignments showed that the core natal areas of studied mallards were in Estonia, southern and central Finland, and northwestern Russia. This study demonstrates a clear temporal succession of latitudes of natal origin during the course of autumn migration. We also demonstrate a corresponding and concomitant shift in virus subtypes. Acknowledging that these two different patterns were based in part upon different data, a likely interpretation worth further testing is that the early arriving birds with more proximate origins have different influenza A subtypes than the more distantly originating late autumn birds. If true, this knowledge would allow novel insight into the origins and transmission of the influenza A virus among migratory hosts previously unavailable through conventional approaches.

SUBMITTER: Gunnarsson G

PROVIDER: S-EPMC3335010 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Disease dynamics and bird migration--linking mallards Anas platyrhynchos and subtype diversity of the influenza A virus in time and space.

Gunnarsson Gunnar G Latorre-Margalef Neus N Hobson Keith A KA Van Wilgenburg Steven L SL Elmberg Johan J Olsen Björn B Fouchier Ron A M RA Waldenström Jonas J

PloS one 20120420 4

The mallard Anas platyrhynchos is a reservoir species for influenza A virus in the northern hemisphere, with particularly high prevalence rates prior to as well as during its prolonged autumn migration. It has been proposed that the virus is brought from the breeding grounds and transmitted to conspecifics during subsequent staging during migration, and so a better understanding of the natal origin of staging ducks is vital to deciphering the dynamics of viral movement pathways. Ottenby is an im ...[more]

PMID: 22536424

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Project description:Recent repeated isolation of H14 hemagglutinin subtype influenza A viruses (IAVs) in the New World waterfowl provides evidence to suggest that host and/or geographic ranges for viruses of this subtype may be expanding. In this study, we used genomic analyses to gain inference on the origin and evolution of H14 viruses in New World waterfowl and conducted an experimental challenge study in mallards (Anas platyrhynchos) to evaluate pathogenicity, viral replication, and transmissibility of a representative viral strain in a natural host species. Genomic characterization of H14 subtype IAVs isolated from New World waterfowl, including three isolates sequenced specifically for this study, revealed high nucleotide identity among individual gene segments (e.g. ≥95% shared identity among H14 HA gene segments). In contrast, lower shared identity was observed among internal gene segments. Furthermore, multiple neuraminidase subtypes were observed for H14 IAVs isolated in the New World. Gene segments of H14 viruses isolated after 2010 shared ancestral genetic lineages with IAVs isolated from wild birds throughout North America. Thus, genomic characterization provided evidence for viral evolution in New World waterfowl through genetic drift and genetic shift since purported introduction from Eurasia. In the challenge study, no clinical disease or lesions were observed among mallards experimentally inoculated with A/blue-winged teal/Texas/AI13-1028/2013(H14N5) or exposed via contact with infected birds. Titers of viral shedding for mallards challenged with the H14N5 IAV were highest at two days post-inoculation (DPI); however shedding was detected up to nine DPI using cloacal swabs. The distribution of viral antigen among mallards infected with H14N5 IAV was largely restricted to enterocytes lining the villi in the lower intestinal tract and in the epithelium of the bursa of Fabricius. Characterization of the infectivity of A/blue-winged teal/Texas/AI13-1028/2013(H14N5) in mallards provides support for similarities in viral replication and shedding as compared to previously described waterfowl-adapted, low pathogenic IAV strains in ducks.

Project description:Prevalence of influenza A virus (IAV) infections in northern-breeding waterfowl has previously been reported to reach an annual peak during late summer or autumn; however, little is known about IAV infection dynamics in waterfowl populations persisting at high-latitude regions such as Alaska, during winter. We captured mallards (Anas platyrhynchos) throughout the non-breeding season (August-April) of 2012-2015 in Fairbanks and Anchorage, the two largest cities in Alaska, to assess patterns of IAV infection and antibody production using molecular methods and a standard serologic assay. In addition, we used virus isolation, genetic sequencing, and a virus microneutralization assay to characterize viral subtypes and to evaluate the immune response of mallards captured on multiple occasions through time. We captured 923 mallards during three successive sampling years: Fairbanks in 2012/13 and 2013/14, and Anchorage in 2014/15. Prevalence varied by age, season, and year/site with high and relatively stable estimates throughout the non-breeding season. Infected birds were detected in all locations/seasons except early-winter in Fairbanks during 2013/14. IAVs with 17 combinations of hemagglutinin (H1-5, H7-9, H11, H12) and neuraminidase (N1-6, N8, N9) subtypes were isolated. Antibodies to IAVs were detected throughout autumn and winter for all sampling locations and years, however, seroprevalence was higher among adults and varied among years. Mallards exhibited individual heterogeneity with regard to immune response, providing instances of both seroconversion and seroreversion to detected viral subtypes. The probability that an individual transitioned from one serostatus to another varied by age, with juvenile mallards having higher rates of seroconversion and seroreversion than adults. Our study provides evidence that a diversity of IAVs circulate in populations of mallards wintering at urban locations in Alaska, and we suggest waterfowl wintering at high-latitudes may play an important role in maintenance of viruses across breeding seasons.

Project description:BACKGROUND:Individual heterogeneity in pathogen load can affect disease transmission dynamics; therefore, identifying intrinsic factors responsible for variation in pathogen load is necessary for determining which individuals are prone to be most infectious. Because low pathogenic avian influenza viruses (LPAIV) preferentially bind to alpha-2,3 sialic acid receptors (SA?2,3Gal) in the intestines and bursa of Fabricius in wild ducks (Anas and Spatula spp.), we investigated juvenile mallards (Anas platyrhyncos) and blue-winged teals (Anas discors) orally inoculated with A/northern pintail/California/44221-761/2006 (H5N9) and the virus titer relationship to occurrence frequency of SA?2,3Gal in the intestines and bursa. To test the natural variation of free-ranging duck populations, birds were hatched and raised in captivity from eggs collected from nests of free-ranging birds in North Dakota, USA. Data generated from qPCR were used to quantify virus titers in cloacal swabs, ileum tissue, and bursa of Fabricius tissue, and lectin histochemistry was used to quantify the occurrence frequency of SA?2,3Gal. Linear mixed models were used to analyze infection status, species, and sex-based differences. Multiple linear regression was used to analyze the relationship between virus titer and SA?2,3Gal occurrence frequency. RESULTS:In mallards, we found high individual variation in virus titers significantly related to high variation of SA?2,3Gal in the ileum. In contrast to mallards, individual variation in teals was minimal and significant relationships between virus titers and SA?2,3Gal were not determined. Collectively, teals had both higher virus titers and a higher occurrence frequency of SA?2,3Gal compared to mallards, which may indicate a positive association between viral load and SA?2,3Gal. Statistically significant differences were observed between infected and control birds indicating that LPAIV infection may influence the occurrence frequency of SA?2,3Gal, or vice versa, but only in specific tissues. CONCLUSIONS:The results of this study provide quantitative evidence that SA?2,3Gal abundance is related to LPAIV titers; thus, SA?2,3Gal should be considered a potential intrinsic factor influencing variation in LPAIV load.

Project description:This research project had the aim to validate the possible alternative and less-painful sampling method of cutting feathers close to the skin instead of plucking them for subsequent feather corticosterone analysis, confirming recently-published results for other species in captivity. Analyzing CORTf is often used in animal welfare studies in combination with behavioral monitoring. The background of this idea was to act in the sense of animal welfare and reduce the burden of animal studies according to the 3-R-Principle (Replacement, Reduction, and Refinement) by refining procedures. To confirm the hypothesis that the sampling method itself has no influence on CORTf levels measured, plucked and cut samples of the respective bird were collected. Birds of two wild species were used: the Mallard (Anas platyrhynchos) and the Greater Flamingo (Phoenicopterus roseus). The CORTf was measured by using an enzyme-linked immunosorbent assay (ELISA). The determined values were inspected for their mean values, standard deviation (SD), and average differences. Afterwards, the CORTf levels of both species were compared, according to the sampling method, with the concordance correlation coefficient (CCC). In the Bland-Altman (BA) plot the differences of the methods were displayed against the mean values. Additionally, sex, as a possible factor influencing CORTf, was analyzed using the Mann-Whitney U test. The values of CCC showed poor agreement in the comparability of the two methods, whereas the concordance of the BA plot was decent. The average differences between the methods were marginal for both species (Mallards: -0.16 pg/mm, Flamingos -0.13 pg/mm). In summary, all anomalies or differences between the methods were negligible. Therefore, the alternative sampling method seems to be as suitable as the common standard method. No significant difference was found between females and males. Nevertheless, our results suggest that CORTf should not be interpreted in just considering the values themselves, but the results they should be analyzed in the context of a wider set of parameters. Hence, further studies are encouraged to create a larger data pool.

Dataset Information

Disease dynamics and bird migration--linking mallards Anas platyrhynchos and subtype diversity of the influenza A virus in time and space.

Publications

Disease dynamics and bird migration--linking mallards Anas platyrhynchos and subtype diversity of the influenza A virus in time and space.

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