Influenza A Viruses in Ruddy Turnstones (Arenaria interpres); Connecting Wintering and Migratory Sites with an Ecological Hotspot at Delaware Bay

Each May for over three decades, avian influenza A viruses (IAVs) have been isolated from shorebirds and gulls (order Charadriiformes) at Delaware Bay (DE Bay), USA, which is a critical stopover site for shorebirds on their spring migration to arctic breeding grounds. At DE Bay, most isolates have been recovered from ruddy turnstones (Arenaria interpres), but it is unknown if this species is involved in either the maintenance or movement of these viruses outside of this site. We collected and tested fecal samples from 2823 ruddy turnstones in Florida and Georgia in the southeastern United States during four winter/spring sample periods—2010, 2011, 2012, and 2013—and during the winters of 2014/2015 and 2015/2016. Twenty-five low pathogenicity IAVs were recovered representing five subtypes (H3N4, H3N8, H5N9, H6N1, and H12N2). Many of these subtypes matched those recovered at DE Bay during the previous year or that year’s migratory cycle, suggesting that IAVs present on these southern wintering areas represent a source of virus introduction to DE Bay via migrating ruddy turnstones. Analyses of all IAV gene segments of H5N9 and H6N1 viruses recovered from ruddy turnstones at DE Bay during May 2012 and from the southeast during the spring of 2012 revealed a high level of genetic relatedness at the nucleotide level, suggesting that migrating ruddy turnstones move IAVs from wintering grounds to the DE Bay ecosystem.

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Evolution of the NS genes of the influenza a viruses. I. The genetic relatedness of the NS genes of animal influenza viruses

Virus Genes ◽

10.1007/bf00308561 ◽

1990 ◽

Vol 4 (1) ◽

pp. 5-13 ◽

Cited By ~ 10

Author(s):

Katsuhisa Nakajima ◽

Eri Nobusawa ◽

Takashi Ogawa ◽

Setsuko Nakajima

Keyword(s):

Influenza A ◽

Genetic Relatedness ◽

Influenza Viruses ◽

Influenza A Viruses

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Matrix Gene of Influenza A Viruses Isolated from Wild Aquatic Birds: Ecology and Emergence of Influenza A Viruses

Journal of Virology ◽

10.1128/jvi.78.16.8771-8779.2004 ◽

2004 ◽

Vol 78 (16) ◽

pp. 8771-8779 ◽

Cited By ~ 78

Author(s):

Linda Widjaja ◽

Scott L. Krauss ◽

Richard J. Webby ◽

Tao Xie ◽

Robert G. Webster

Keyword(s):

North American ◽

Influenza A ◽

Delaware Bay ◽

Influenza Viruses ◽

Aquatic Birds ◽

Influenza A Viruses ◽

M Gene ◽

Matrix Gene ◽

Distinct Lineage ◽

Wild Waterfowl

ABSTRACT Wild aquatic birds are the primary reservoir of influenza A viruses, but little is known about the viruses' gene pool in wild birds. Therefore, we investigated the ecology and emergence of influenza viruses by conducting phylogenetic analysis of 70 matrix (M) genes of influenza viruses isolated from shorebirds and gulls in the Delaware Bay region and from ducks in Alberta, Canada, during >18 years of surveillance. In our analysis, we included 61 published M genes of isolates from various hosts. We showed that M genes of Canadian duck viruses and those of shorebird and gull viruses in the Delaware Bay shared ancestors with the M genes of North American poultry viruses. We found that North American and Eurasian avian-like lineages are divided into sublineages, indicating that multiple branches of virus evolution may be maintained in wild aquatic birds. The presence of non-H13 gull viruses in the gull-like lineage and of H13 gull viruses in other avian lineages suggested that gulls' M genes do not preferentially associate with the H13 subtype or segregate into a distinct lineage. Some North American avian influenza viruses contained M genes closely related to those of Eurasian avian viruses. Therefore, there may be interregional mixing of the two clades. Reassortment of shorebird M and HA genes was evident, but there was no correlation among the HA or NA subtype, M gene sequence, and isolation time. Overall, these results support the hypothesis that influenza viruses in wild waterfowl contain distinguishable lineages of M genes.

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Evidence for history-dependence of influenza pandemic emergence

Scientific Reports ◽

10.1038/srep43623 ◽

2017 ◽

Vol 7 (1) ◽

Cited By ~ 2

Author(s):

Edward M. Hill ◽

Michael J. Tildesley ◽

Thomas House

Keyword(s):

Influenza A ◽

Influenza Pandemic ◽

Influenza A Viruses ◽

History Dependence ◽

Influenza Pandemics ◽

Gamma Distributions ◽

Time Periods ◽

Pandemic Strains ◽

Modelling Assumptions ◽

High Level

Abstract Influenza A viruses have caused a number of global pandemics, with considerable mortality in humans. Here, we analyse the time periods between influenza pandemics since 1700 under different assumptions to determine whether the emergence of new pandemic strains is a memoryless or history-dependent process. Bayesian model selection between exponential and gamma distributions for these time periods gives support to the hypothesis of history-dependence under eight out of nine sets of modelling assumptions. Using the fitted parameters to make predictions shows a high level of variability in the modelled number of pandemics from 2010–2110. The approach we take here relies on limited data, so is uncertain, but it provides cheap, safe and direct evidence relating to pandemic emergence, a field where indirect measurements are often made at great risk and cost.

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Influenza A virus: sampling of the unique shorebird habitat at Delaware Bay, USA

Royal Society Open Science ◽

10.1098/rsos.171420 ◽

2017 ◽

Vol 4 (11) ◽

pp. 171420 ◽

Cited By ~ 7

Author(s):

Rebecca L. Poulson ◽

Page M. Luttrell ◽

Morgan J. Slusher ◽

Benjamin R. Wilcox ◽

Lawrence J. Niles ◽

...

Keyword(s):

Influenza A Virus ◽

Environmental Samples ◽

Influenza A ◽

Coastal Region ◽

The Arctic ◽

Long Distance ◽

Stopover Site ◽

Sand Surface ◽

Avian Influenza A Virus ◽

Breeding Grounds

Delaware (DE) Bay, in the northeastern USA, has long been recognized as a hotspot for avian influenza A virus (IAV); every spring, this coastal region serves as a brief stopover site for thousands of long-distance migrating shorebirds, en route to breeding grounds in the Arctic. During these stopovers, IAV has been consistently recovered from ruddy turnstones ( Arenaria interpres ) that are likely to become infected as they feed by probing sand and cobble in search of food. In May 2010–2012, we successfully isolated 19 IAV from environmental samples (sand, n = 18; horseshoe crab eggs, n = 1) obtained from DE Bay sites. Two of these viruses were subjected to laboratory conditions similar to those in the DE Bay spring-time environment, and remained infectious for 7 days. Here, through the recovery of IAV from environmental samples, temperature monitoring at and below the sand surface and simulated laboratory trials, we provide evidence that the beach environment may enable localized transmission and short-term maintenance of IAV in this unique ecosystem.

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Subtype Diversity of Influenza A Virus in North American Waterfowl: a Multidecade Study

Journal of Virology ◽

10.1128/jvi.02022-19 ◽

2020 ◽

Vol 94 (11) ◽

Cited By ~ 1

Author(s):

Elena R. Diskin ◽

Kimberly Friedman ◽

Scott Krauss ◽

Jacqueline M. Nolting ◽

Rebecca L. Poulson ◽

...

Keyword(s):

North American ◽

Influenza A ◽

The United States ◽

Surveillance Data ◽

Aquatic Birds ◽

Influenza A Viruses ◽

Wintering Grounds ◽

Annual Trend ◽

Continental Scale ◽

Breeding Grounds

ABSTRACT The discovery in 1976 of waterfowl as the primary reservoir of influenza A viruses (IAVs) has since spurred decades of waterfowl surveillance efforts by researchers dedicated to understanding the ecology of IAV and its subsequent threat to human and animal health. Here, we employed a multidecade, continental-scale approach of surveillance data to understand trends of seasonal IAV subtype diversity. Between 1976 and 2015, IAVs were detected in 8,427 (10.8%) of 77,969 samples from migratory waterfowl throughout the Central and Mississippi Migratory Flyways in the United States and Canada. A total of 96 hemagglutinin (HA)/neuraminidase (NA) subtype combinations were isolated, which included most HA (H1 to H14) and all 9 NA subtypes. We observed an annual trend of high influenza prevalence, involving a few dominant subtypes, on northern breeding grounds during summer with progressively lowered influenza prevalence, comprised of a highly diverse profile of subtypes, as waterfowl migrate toward southern wintering grounds. Isolates recovered during winter had the highest proportion of mixed and rare HA/NA combinations, indicating increased opportunity for reassortment of IAVs. In addition, 70% of H5 and 49% of H7 IAV isolates were recovered from samples collected during fall and spring, respectively; these are subtypes that can have significant implications for public health and agriculture sectors. Annual cyclical dominance of subtypes on northern breeding grounds is revealed through the longitudinal nature of this study. Our novel findings exhibit the unrealized potential for discovery using existing IAV surveillance data. IMPORTANCE Wild aquatic birds are the primary natural reservoir of influenza A viruses (IAVs) and are therefore responsible for the dispersal and maintenance of IAVs representing a broad range of antigenic and genetic diversity. The aims of IAV surveillance in waterfowl not only relate to understanding the risk of spillover risk to humans, but also to improving our understanding of basic questions related to IAV evolution and ecology. By evaluating several decades of surveillance data from wild aquatic birds sampled along North American migratory flyways, we discovered an annual trend of increasing subtype diversity during southbound migration, peaking on southern wintering grounds. Winter sampling revealed the highest proportion of mixed and rare infections that suggest higher opportunity for spillover. These findings allow improvements to surveillance efforts to robustly capture IAV diversity that will be used for vaccine development and cultivate a more thorough understanding of IAV evolution and persistence mechanisms.

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Grafting Methionine on 1F1 Ab Increases the Broad-Activity on HA Structural-Conserved Residues of H1, H2, and H3 Influenza a Viruses

Evolutionary Bioinformatics ◽

10.1177/11769343211003082 ◽

2021 ◽

Vol 17 ◽

pp. 117693432110030

Author(s):

Hoa Thanh Le ◽

Phuc-Chau Do ◽

Ly Le

Keyword(s):

Amino Acid ◽

Influenza A Virus ◽

Broad Spectrum ◽

Influenza A ◽

Structural Alignment ◽

Peptide Inhibitors ◽

Influenza A Viruses ◽

Conserved Residues ◽

High Level ◽

Cellular Fusion

A high level of mutation enables the influenza A virus to resist antibiotics previously effective against the influenza A virus. A portion of the structure of hemagglutinin HA is assumed to be well-conserved to maintain its role in cellular fusion, and the structure tends to be more conserved than sequence. We designed peptide inhibitors to target the conserved residues on the HA surface, which were identified based on structural alignment. Most of the conserved and strongly similar residues are located in the receptor-binding and esterase regions on the HA1 domain In a later step, fragments of anti-HA antibodies were gathered and screened for the binding ability to the found conserved residues. As a result, Methionine amino acid got the best docking score within the −2.8 Å radius of Van der Waals when it is interacting with Tyrosine, Arginine, and Glutamic acid. Then, the binding affinity and spectrum of the fragments were enhanced by grafting hotspot amino acid into the fragments to form peptide inhibitors. Our peptide inhibitor was able to form in silico contact with a structurally conserved region across H1, H2, and H3 HA, with the binding site at the boundary between HA1 and HA2 domains, spreading across different monomers, suggesting a new target for designing broad-spectrum antibody and vaccine. This research presents an affordable method to design broad-spectrum peptide inhibitors using fragments of an antibody as a scaffold.

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Does influenza A virus infection affect movement behaviour during stopover in its wild reservoir host?

Royal Society Open Science ◽

10.1098/rsos.150633 ◽

2016 ◽

Vol 3 (2) ◽

pp. 150633 ◽

Cited By ~ 20

Author(s):

Daniel Bengtsson ◽

Kamran Safi ◽

Alexis Avril ◽

Wolfgang Fiedler ◽

Martin Wikelski ◽

...

Keyword(s):

Avian Influenza ◽

Influenza A ◽

Three Dimensional ◽

Reservoir Host ◽

Migration Route ◽

Influenza A Viruses ◽

Natural Habitats ◽

Stopover Site ◽

Geographical Regions ◽

Natural Hosts

The last decade has seen a surge in research on avian influenza A viruses (IAVs), in part fuelled by the emergence, spread and potential zoonotic importance of highly pathogenic virus subtypes. The mallard ( Anas platyrhynchos ) is the most numerous and widespread dabbling duck in the world, and one of the most important natural hosts for studying IAV transmission dynamics. In order to predict the likelihood of IAV transmission between individual ducks and to other hosts, as well as between geographical regions, it is important to understand how IAV infection affects the host. In this study, we analysed the movements of 40 mallards equipped with GPS transmitters and three-dimensional accelerometers, of which 20 were naturally infected with low pathogenic avian influenza virus (LPAIV), at a major stopover site in the Northwest European flyway. Movements differed substantially between day and night, as well as between mallards returning to the capture site and those feeding in natural habitats. However, movement patterns did not differ between LPAIV infected and uninfected birds. Hence, LPAIV infection probably does not affect mallard movements during stopover, with high possibility of virus spread along the migration route as a consequence.

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Evaluation of three strains of influenza A virus in humans and in owl, cebus, and squirrel monkeys

Infection and Immunity ◽

10.1128/iai.28.3.688-691.1980 ◽

1980 ◽

Vol 28 (3) ◽

pp. 688-691

Author(s):

B R Murphy ◽

D L Sly ◽

N T Hosier ◽

W T London ◽

R M Chanock

Keyword(s):

Influenza A ◽

Genetic Basis ◽

Squirrel Monkeys ◽

Upper Respiratory Tract ◽

Influenza A Viruses ◽

Virus Shedding ◽

Respiratory Tract Illness ◽

Cebus Monkeys ◽

Owl Monkeys ◽

High Level

The virulence of three cloned influenza A viruses was compared in humans and in three readily available species of nonhuman primates (owl, squirrel, and cebus monkeys) in an attempt to identify a species of monkey that could be used to investigate the genetic basis of attenuation of influenza A viruses for humans. Three influenza A viruses from two subtypes, i.e., the A/Udorn/72 (H3N2), A/Alaska/77 (H3H2), and A/Hong Kong/77 (H1H1) viruses, produced febrile influenzal illness in humans. Squirrel monkeys developed mild upper respiratory tract illness in response to each of the three viruses. Illness was accompanied by a high level of virus shedding; each of nine squirrel monkeys that shed equal to or greater than 10(5.0) 50% tissue culture infective doses of virus became ill, whereas those that shed less remained well. In contrast, the cebus and owl monkeys remained clinically well despite infection with each of the three viruses. Thus, squirrel monkeys appear to be moderately permissive primate hosts in which to investigate the genetic basis of virulence of human influenza A viruses.

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Substantial Antigenic Drift in the Hemagglutinin Protein of Swine Influenza A Viruses

Viruses ◽

10.3390/v12020248 ◽

2020 ◽

Vol 12 (2) ◽

pp. 248 ◽

Cited By ~ 7

Author(s):

Pia Ryt-Hansen ◽

Anders Gorm Pedersen ◽

Inge Larsen ◽

Charlotte Sonne Kristensen ◽

Jesper Schak Krog ◽

...

Keyword(s):

Genetic Drift ◽

Influenza A ◽

Immune Escape ◽

Swine Influenza ◽

Antigenic Drift ◽

Influenza A Viruses ◽

Hemagglutinin Protein ◽

One Year ◽

High Level ◽

Ha Protein

The degree of antigenic drift in swine influenza A viruses (swIAV) has historically been regarded as minimal compared to that of human influenza A virus strains. However, as surveillance activities on swIAV have increased, more isolates have been characterized, revealing a high level of genetic and antigenic differences even within the same swIAV lineage. The objective of this study was to investigate the level of genetic drift in one enzootically infected swine herd over one year. Nasal swabs were collected monthly from sows (n = 4) and piglets (n = 40) in the farrowing unit, and from weaners (n = 20) in the nursery. Virus from 1–4 animals were sequenced per month. Analyses of the sequences revealed that the hemagglutinin (HA) gene was the main target for genetic drift with a substitution rate of 7.6 × 10−3 substitutions/site/year and evidence of positive selection. The majority of the mutations occurred in the globular head of the HA protein and in antigenic sites. The phylogenetic tree of the HA sequences displayed a pectinate typology, where only a single lineage persists and forms the ancestor for subsequent lineages. This was most likely caused by repeated selection of a single immune-escape variant, which subsequently became the founder of the next wave of infections.

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