Influenza A Virus Migration and Persistence in North American Wild Birds

Bahl, Justin; Krauss, Scott; Kühnert, Denise; Fourment, Mathieu; Raven, Garnet; Pryor, Sydney; Niles, Lawrence J.; Danner, Angela; Walker, David; Mendenhall, Ian H.; Su, Yvonne C. F.; Dugan, Vivien G.; Halpin, Rebecca; Stockwell, Timothy B.; Webby, Richard J.; Wentworth, David E.; Drummond, Alexei J.; Smith, Gavin J. D.; Webster, Robert G.

doi:10.1371/journal.ppat.1003570

Cited by 87 publications

(119 citation statements)

References 43 publications

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“…Similarly, the HA and NA genes of AIVs in Argentina differ from those of viruses circulating in North America and Eurasia 13. The main subtypes of AIV consistently reported to circulate in other countries14, 15, 16, 17, 18, 19 have not been reported in Brazil. However, an H11N9 influenza virus was recently identified for the first time in South American migratory birds in the Amazon region, and this virus showed great similarity to viruses of North American, rather than South American, lineages 20…”

Section: Introductionmentioning

confidence: 98%

Migratory birds in southern Brazil are a source of multiple avian influenza virus subtypes

Araújo

Petry

Fabrizio

et al. 2017

Influenza Resp Viruses

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BackgroundThere is insufficient knowledge about the relation of avian influenza virus (AIV) to migratory birds in South America. Accordingly, we studied samples obtained over a 4‐year period (2009‐2012) from wild birds at a major wintering site in southern Brazil.MethodsWe obtained 1212 oropharyngeal/cloacal samples from wild birds at Lagoa do Peixe National Park and screened them for influenza A virus by RT‐PCR amplification of the matrix gene. Virus isolates were subjected to genomic sequencing and antigenic characterization.ResultsForty‐eight samples of 1212 (3.96%) contained detectable influenza virus RNA. Partial viral sequences were obtained from 12 of these samples, showing the presence of H2N2 (1), H6Nx (1), H6N1 (8), H9N2 (1), and H12N5 (1) viruses. As H6 viruses predominated, we generated complete genomes from all 9 H6 viruses. Phylogenetic analyses showed that they were most similar to viruses of South American lineage. The H6N1 viruses caused no disease signs in infected ferrets and, despite genetic differences, were antigenically similar to North American isolates.ConclusionsLagoa do Peixe National Park is a source of multiple AIV subtypes, with the levels of influenza virus in birds being highest at the end of their wintering period in this region. H6N1 viruses were the predominant subtype identified. These viruses were more similar to viruses of South American lineage than to those of North American lineage.

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Section: Introductionmentioning

confidence: 98%

Migratory birds in southern Brazil are a source of multiple avian influenza virus subtypes

Araújo

Petry

Fabrizio

et al. 2017

Influenza Resp Viruses

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“…In fact, these mallards were captured for surveillance for influenza in 2001, and analysis of data between 2001 and 2006 reveals that 16.6% of Alberta ducks are influenza carriers (68). Alberta is the convergence point for four major North American flyways, and the majority of genetic diversity observed in the influenza gene pool has been recovered over time in Alberta (69). We might predict that pressure from duck CD8 + T cell immunity and viral escape is partially responsible for diversity of viral proteins, just as Ab responses to hemagglutinin may explain prevalence of multiple viral subtypes.…”

Section: Discussionmentioning

confidence: 99%

Extensive Allelic Diversity of MHC Class I in Wild Mallard Ducks

Fleming-Canepa

Jensen

Mesa

et al. 2016

The Journal of Immunology

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MHC class I is critically involved in defense against viruses, and diversity from polygeny and polymorphism contributes to the breadth of the immune response and health of the population. In this article, we examine MHC class I diversity in wild mallard ducks, the natural host and reservoir of influenza A viruses. We previously showed domestic ducks predominantly use UAA, one of five MHC class I genes, but whether biased expression is also true for wild mallards is unknown. Using RT-PCR from blood, we examined expressed MHC class I alleles from 38 wild mallards (Anas platyrhynchos) and identified 61 unique alleles, typically 1 or 2 expressed alleles in each individual. To determine whether expressed alleles correspond to UAA adjacent to TAP2 as in domestic ducks, we cloned and sequenced genomic UAA-TAP2 fragments from all mallards, which matched transcripts recovered and allowed us to assign most alleles as UAA. Allelic differences are primarily located in α1 and α2 domains in the residues known to interact with peptide in mammalian MHC class I, suggesting the diversity is functional. Most UAA alleles have unique residues in the cleft predicting distinct specificity; however, six alleles have an unusual conserved cleft with two cysteine residues. Residues that influence peptide-loading properties and tapasin involvement in chicken are fixed in duck alleles and suggest tapasin independence. Biased expression of one MHC class I gene may make viral escape within an individual easy, but high diversity in the population places continual pressure on the virus in the reservoir species.

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“…Furthermore, even though we followed bird populations as they migrated down the river, due to the high levels of reassortment in AIV, we recovered only four isolates containing the same virus constellations. Studies investigating North American AIV movement over much broader geographic and temporal scales suggested that the initial movement of AIVs is likely to occur along migratory routes, but these studies were limited by the availability of surveillance samples from these flyways and may have underestimated the amount of movement occurring within the flyways themselves (19,20). The present study provides empirical evidence suggesting that waterfowl in the MMF disperse AIV genetic diversity quickly within the migratory corridor and that surveillance efforts to detect AIV threats to human and domestic animal health should pay particular attention to these routes in initially responding to epidemics/epizootics.…”

Section: Discussionmentioning

confidence: 99%

“…LPAIVs in the MMF. Studies have shown that LPAIVs can be genetically structured within and between North American migratory flyways (20,35,45,46), even in light of relatively high levels of gene flow measured between flyways (19). In the present study, while we observed a pattern of increased dispersal of AIVs within the MMF over short time frames, we also observed signatures of regional persistence of gene diversity across multiple sea- sons, which suggests a temporal effect on the genetic structuring of AIV diversity both within and among flyways.…”

Section: Discussionmentioning

confidence: 99%

“…However, there is limited evidence for the spread of diverse AIV strains by wild birds, especially over shorter periods; thus, the significance of host waterfowl in spreading AIV is still debated (17,18). Recent studies described the movement of AIV genetic diversity in North America over decade-long time frames (19,20). To better understand influenza A virus evolution in the natural host and to aid in our ability to effectively respond to viral threats to public and animal health, the movement of AIVs must be understood for shorter time frames that are relevant to disease events.…”

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confidence: 99%

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Spread and Persistence of Influenza A Viruses in Waterfowl Hosts in the North American Mississippi Migratory Flyway

Fries

Nolting

Bowman

et al. 2015

J Virol

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While geographic distance often restricts the spread of pathogens via hosts, this barrier may be compromised when host species are mobile. Migratory waterfowl in the order Anseriformes are important reservoir hosts for diverse populations of avian-origin influenza A viruses (AIVs) and are assumed to spread AIVs during their annual continental-scale migrations. However, support for this hypothesis is limited, and it is rarely tested using data from comprehensive surveillance efforts incorporating both the temporal and spatial aspects of host migratory patterns. We conducted intensive AIV surveillance of waterfowl using the North American Mississippi Migratory Flyway (MMF) over three autumn migratory seasons. Viral isolates (n ‫؍‬ 297) from multiple host species were sequenced and analyzed for patterns of gene dispersal between northern staging and southern wintering locations. Using a phylogenetic and nucleotide identity framework, we observed a larger amount of gene dispersal within this flyway rather than between the other three longitudinally identified North American flyways. Across seasons, we observed patterns of regional persistence of diversity for each genomic segment, along with limited survival of dispersed AIV gene lineages. Reassortment increased with both time and distance, resulting in transient AIV constellations. This study shows that within the MMF, AIV gene flow favors spread along the migratory corridor within a season, and also that intensive surveillance during bird migration is important for identifying virus dispersal on time scales relevant to pandemic responsiveness. In addition, this study indicates that comprehensive monitoring programs to capture AIV diversity are critical for providing insight into AIV evolution and ecology in a major natural reservoir. IMPORTANCEMigratory birds are a reservoir for antigenic and genetic diversity of influenza A viruses (AIVs) and are implicated in the spread of virus diversity that has contributed to previous pandemic events. Evidence for dispersal of avian-origin AIVs by migratory birds is rarely examined on temporal scales relevant to pandemic or panzootic threats. Therefore, characterizing AIV movement by hosts within a migratory season is important for implementing effective surveillance strategies. We conducted surveillance following birds along a major North American migratory route and observed that within a migratory season, AIVs rapidly reassorted and gene lineages were dispersed primarily within the migratory corridor. Patterns of regional persistence were observed across seasons for each gene segment. We show that dispersal of AIV gene lineages by migratory birds occurs quickly along migratory routes and that surveillance for AIVs threatening human and animal health should focus attention on these routes.

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Influenza A Virus Migration and Persistence in North American Wild Birds

Cited by 87 publications

References 43 publications

Migratory birds in southern Brazil are a source of multiple avian influenza virus subtypes

Migratory birds in southern Brazil are a source of multiple avian influenza virus subtypes

Extensive Allelic Diversity of MHC Class I in Wild Mallard Ducks

Spread and Persistence of Influenza A Viruses in Waterfowl Hosts in the North American Mississippi Migratory Flyway

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