Characterization of Subtype H6 Avian Influenza A Viruses Isolated From Wild Birds in Poyang Lake, China

Subtype H6 avian influenza A viruses (IAVs) are enzootic and genetically diverse in both domestic poultry and wild waterfowl and may cause spillovers in both pigs and humans. Thus, it is important to understand the genetic diversity of H6 IAVs in birds and their zoonotic potential. Compared with that in domestic poultry, the genetic diversity of H6 viruses in wild birds in China has not been well-understood. In this study, five H6 viruses were isolated from wild birds in Poyang Lake, China, and genetic analyses showed that these isolates are clustered into four genotypes associated with reassortments among avian IAVs from domestic poultry and wild birds in China and those from Eurasia and North America and that these viruses exhibited distinct phenotypes in growth kinetics analyses with avian and mammalian cells lines and in mouse challenge experiments. Of interest is that two H6 isolates from the Eurasian teal replicated effectively in the mouse lung without prior adaptation, whereas the other three did not. Our study suggested that there are variations in the mammalian viral replication efficiency phenotypic among genetically diverse H6 IAVs in wild birds and that both intra- and inter-continental movements of IAVs through wild bird migration may facilitate the emergence of novel H6 IAV reassortants with the potential for replicating in mammals, including humans. Continued surveillance to monitor the diversity of H6 IAVs in wild birds is necessary to increase our understanding of the natural history of IAVs.

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Genetic Evidence Supports Sporadic and Independent Introductions of Subtype H5 Low-Pathogenic Avian Influenza A Viruses from Wild Birds to Domestic Poultry in North America

Journal of Virology ◽

10.1128/jvi.00913-18 ◽

2018 ◽

Vol 92 (19) ◽

Cited By ~ 10

Author(s):

Lei Li ◽

Andrew S. Bowman ◽

Thomas J. DeLiberto ◽

Mary L. Killian ◽

Scott Krauss ◽

...

Keyword(s):

United States ◽

Avian Influenza ◽

Influenza A ◽

The United States ◽

Wild Birds ◽

Influenza A Viruses ◽

Pathogenic Avian Influenza ◽

Live Bird Markets ◽

Domestic Poultry ◽

Live Bird

ABSTRACTWild-bird origin influenza A viruses (IAVs or avian influenza) have led to sporadic outbreaks among domestic poultry in the United States and Canada, resulting in economic losses through the implementation of costly containment practices and destruction of birds. We used evolutionary analyses of virus sequence data to determine that 78 H5 low-pathogenic avian influenza viruses (LPAIVs) isolated from domestic poultry in the United States and Canada during 2001 to 2017 resulted from 18 independent virus introductions from wild birds. Within the wild-bird reservoir, the hemagglutinin gene segments of H5 LPAIVs exist primarily as two cocirculating genetic sublineages, and our findings suggest that the H5 gene segments flow within each migratory bird flyway and among adjacent flyways, with limited exchange between the nonadjacent Atlantic and Pacific Flyways. Phylogeographic analyses provided evidence that IAVs from dabbling ducks and swans/geese contributed to the emergence of viruses among domestic poultry. H5 LPAIVs isolated from commercial farm poultry (i.e., turkey) that were descended from a single introduction typically remained a single genotype, whereas those from live-bird markets sometimes led to multiple genotypes, reflecting the potential for reassortment with other IAVs circulating within live-bird markets. H5 LPAIVs introduced from wild birds to domestic poultry represent economic threats to the U.S. poultry industry, and our data suggest that such introductions have been sporadic, controlled effectively through production monitoring and a stamping-out policy, and are, therefore, unlikely to result in sustained detections in commercial poultry operations.IMPORTANCEIntegration of viral genome sequencing into influenza surveillance for wild birds and domestic poultry can elucidate evolutionary pathways of economically costly poultry pathogens. Evolutionary analyses of H5 LPAIVs detected in domestic poultry in the United States and Canada during 2001 to 2017 suggest that these viruses originated from repeated introductions of IAVs from wild birds, followed by various degrees of reassortment. Reassortment was observed where biosecurity was low and where opportunities for more than one virus to circulate existed (e.g., congregations of birds from different premises, such as live-bird markets). None of the H5 lineages identified were maintained for the long term in domestic poultry, suggesting that management strategies have been effective in minimizing the impacts of virus introductions on U.S. poultry production.

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Reassortment and persistence of influenza A viruses from diverse geographic origins within Australian wild birds: evidence from a small, isolated population of Ruddy turnstones

Journal of Virology ◽

10.1128/jvi.02193-20 ◽

2021 ◽

Author(s):

Bethany J. Hoye ◽

Celeste M. Donato ◽

Simeon Lisovski ◽

Yi-Mo Deng ◽

Simone Warner ◽

...

Keyword(s):

Avian Influenza ◽

Influenza A ◽

Wild Birds ◽

Influenza Viruses ◽

Low Density ◽

Isolated Population ◽

Influenza A Viruses ◽

Geographic Origins ◽

Eastern Australia

Australian lineages of avian influenza A viruses (AIVs) are thought to be phylogenetically distinct from those circulating in Eurasia and the Americas, suggesting the circulation of endemic viruses seeded by occasional introductions from other regions. However, processes underlying the introduction, evolution and maintenance of AIVs in Australia remain poorly understood. Waders (Order Charadriiformes, Family Scolopacidae) may play a unique role in the ecology and evolution of AIVs, particularly in Australia, where ducks, geese and swans (Order Anseriformes, Family Anatidae) rarely undertake intercontinental migrations. Across a five-year surveillance period (2011–2015), Ruddy turnstones (Arenaria interpres) that ‘overwinter’ during the Austral summer in south eastern Australia showed generally low levels of AIV prevalence (0–2%). However, in March 2014 we detected AIVs in 32% (95% CI; 25–39%) of individuals in a small, low-density, island population 90km from the Australian mainland. This epizootic comprised three distinct AIV genotypes, each of which represent a unique reassortment of Australian, recently introduced Eurasian, and recently introduced American-lineage gene segments. Strikingly, the Australian-lineage gene segments showed high similarity to H10N7 viruses isolated in 2010 and 2012 from poultry outbreaks 900–1500km to the north. Together with the diverse geographic origins of the American and Eurasian gene segments, these findings suggest extensive circulation and reassortment of AIVs within Australian wild birds over vast geographic distances. Our findings indicate that long-term surveillance in waders may yield unique insights into AIV gene flow, especially in geographic regions like Oceania where Anatidae do not display regular inter- or intracontinental migration. IMPORTANCE High prevalence of avian influenza viruses (AIVs) was detected in a small, low-density, isolated population of Ruddy turnstones in Australia. Analysis of these viruses revealed relatively recent introductions of viral gene segments from both Eurasia and North America, as well as long-term persistence of introduced gene segments in Australian wild birds. These data demonstrate that the flow of viruses into Australia may be more common than initially thought and that, once introduced, these AIVs have the potential to be maintained within the continent. These findings add to a growing body of evidence suggesting Australian wild birds are unlikely to be ecologically-isolated from the highly pathogenic H5Nx viruses circulating among wild birds throughout the northern hemisphere.

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A High Diversity of Eurasian Lineage Low Pathogenicity Avian Influenza A Viruses Circulate among Wild Birds Sampled in Egypt

PLoS ONE ◽

10.1371/journal.pone.0068522 ◽

2013 ◽

Vol 8 (7) ◽

pp. e68522 ◽

Cited By ~ 14

Author(s):

Nancy A. Gerloff ◽

Joyce Jones ◽

Natosha Simpson ◽

Amanda Balish ◽

Maha Adel ElBadry ◽

...

Keyword(s):

Avian Influenza ◽

Influenza A ◽

Wild Birds ◽

Influenza A Viruses ◽

Eurasian Lineage ◽

High Diversity

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The Genetic Diversity of Influenza A Viruses in Wild Birds in Peru

PLoS ONE ◽

10.1371/journal.pone.0146059 ◽

2016 ◽

Vol 11 (1) ◽

pp. e0146059 ◽

Cited By ~ 14

Author(s):

Martha I. Nelson ◽

Simon Pollett ◽

Bruno Ghersi ◽

Maria Silva ◽

Mark P. Simons ◽

...

Keyword(s):

Genetic Diversity ◽

Influenza A ◽

Wild Birds ◽

Influenza A Viruses

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Systemic infection with highly pathogenic H5N8 of avian origin produces encephalitis and mortality in wild mammals at a UK rehabilitation centre

10.1101/2021.05.26.445666 ◽

2021 ◽

Author(s):

Tobias Floyd ◽

Ashley C Banyard ◽

Fabian ZX Lean ◽

Alexander MP Byrne ◽

Edward Fullick ◽

...

Keyword(s):

Avian Influenza ◽

Influenza A ◽

Wild Bird ◽

Influenza A Viruses ◽

Rehabilitation Centre ◽

Highly Pathogenic ◽

Wild Mammals ◽

Domestic Poultry ◽

Avian Origin ◽

The Impact

Europe has experienced extensive outbreaks of highly pathogenic avian influenza (HPAI) during the autumn/winter 2020/21 season. These avian influenza A viruses are highly transmissible and have infected over 1000 commercial and backyard poultry premises in Europe in this period causing high mortality. The impact on wild bird populations has also been significant, with over 400 detections in at least 47 different species reported across Europe as being positive with the H5N8 virus. Although different H5Nx combinations within the H5 clade 2.3.4.4b have been detected, the H5N8 subtype has predominated both in wild birds and domestic poultry outbreaks. In the UK there have been 22 outbreaks of H5N8 in domestic poultry and captive birds and more than 300 wild bird detections involving H5N8 over the autumn/winter 2020/21 period to April 2021. Here we detail the series of events surrounding the detection of an H5N8 influenza A virus of avian origin in five swans, a fox and three seals in a wildlife rehabilitation centre.

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Detection of Resistance Mutations to Antivirals Oseltamivir and Zanamivir in Avian Influenza A Viruses Isolated from Wild Birds

PLoS ONE ◽

10.1371/journal.pone.0016028 ◽

2011 ◽

Vol 6 (1) ◽

pp. e16028 ◽

Cited By ~ 42

Author(s):

Goran Orozovic ◽

Kanita Orozovic ◽

Johan Lennerstrand ◽

Björn Olsen

Keyword(s):

Avian Influenza ◽

Influenza A ◽

Wild Birds ◽

Resistance Mutations ◽

Influenza A Viruses

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Genetic evolution and transmission dynamics of clade 2.3.2.1a highly pathogenic avian influenza A/H5N1 viruses in Bangladesh

Virus Evolution ◽

10.1093/ve/veaa046 ◽

2020 ◽

Vol 6 (2) ◽

Author(s):

Jung-Hoon Kwon ◽

Dong-Hun Lee ◽

Miria Ferreira Criado ◽

Lindsay Killmaster ◽

Md Zulfekar Ali ◽

...

Keyword(s):

Genetic Diversity ◽

Avian Influenza ◽

Influenza A ◽

Highly Pathogenic Avian Influenza ◽

Influenza Viruses ◽

Effective Control ◽

Highly Pathogenic ◽

Pathogenic Avian Influenza ◽

History Of ◽

Genetic Sequences

Abstract Asian lineage A/H5N1 highly pathogenic avian influenza viruses (HPAIVs) have been responsible for continuous outbreaks in Bangladesh since 2007. Although clades 2.2.2 and 2.3.4.2 HPAIVs have disappeared since poultry vaccination was introduced in 2012, clade 2.3.2.1a viruses have continued to be detected in Bangladesh. In this study, we identified A/H9N2 (n = 15), A/H5N1 (n = 19), and A/H5N1-A/H9N2 (n = 18) mixed viruses from live bird markets, chicken farms, and wild house crows (Corvus splendens) in Bangladesh from 2016 to 2018. We analyzed the genetic sequences of the H5 HPAIVs, to better understand the evolutionary history of clade 2.3.2.1a viruses in Bangladesh. Although seven HA genetic subgroups (B1–B7) and six genotypes (G1, G1.1, G1.2, G2, G2.1, and G2.2) have been identified in Bangladesh, only subgroup B7 and genotypes G2, G2.1, and G2.2 were detected after 2016. The replacement of G1 genotype by G2 in Bangladesh was possibly due to vaccination and viral competition in duck populations. Initially, genetic diversity decreased after introduction of vaccination in 2012, but in 2015, genetic diversity increased and was associated with the emergence of genotype G2. Our phylodynamic analysis suggests that domestic Anseriformes, including ducks and geese, may have played a major role in persistence, spread, evolution, and genotype replacement of clade 2.3.2.1a HPAIVs in Bangladesh. Thus, improvements in biosecurity and monitoring of domestic Anseriformes are needed for more effective control of HPAI in Bangladesh.

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Diversity of avian influenza A(H5N6) viruses in wild birds in southern China

Journal of General Virology ◽

10.1099/jgv.0.001449 ◽

2020 ◽

Vol 101 (9) ◽

pp. 902-909

Author(s):

Tao Zhang ◽

Kai Fan ◽

Xue Zhang ◽

Yujuan Xu ◽

Jian Xu ◽

...

Keyword(s):

Avian Influenza ◽

Influenza A ◽

Wild Bird ◽

Poyang Lake ◽

Southern China ◽

Evolutionary Relationship ◽

Wild Birds ◽

Influenza Viruses ◽

Jiangxi Province ◽

Lake Area

The predominance of H5N6 in ducks and continuous human cases have heightened its potential threat to public health in China. Therefore, the detection of emerging variants of H5N6 avian influenza viruses has become a priority for pandemic preparedness. Questions remain as to its origin and circulation within the wild bird reservoir and interactions at the wild–domestic interface. Samples were collected from migratory birds in Poyang Lake, Jiangxi Province, PR China during the routine bird ring survey in 2014–16. Phylogenetic and coalescent analyses were conducted to uncover the evolutionary relationship among viruses circulating in wild birds. Here, we report the potential origin and phylogenetic diversity of H5N6 viruses isolated from wild birds in Poyang Lake. Sequence analyses indicated that Jiangxi H5N6 viruses most likely evolved from Eurasian-derived H5Nx and H6N6 viruses through multiple reassortment events. Crucially, the diversity of the HA gene implies that these Jiangxi H5N6 viruses have diverged into two primary clades − clade 2.3.4.4 and clade 2.3.2.1 c. Phylogenetic analysis revealed two independent pathways of reassortment during 2014–16 that might have facilitated the generation of emerging variants within wild bird populations as well as inter-species infections. Our findings contribute to our understanding of the genetic diversification of H5N6 viruses in the wild bird population. These results highlight the necessity of large-scale surveillance of wild birds in the Poyang Lake area to address the threat of regional epizootic epidemics and attendant pandemics.

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Wild birds in Chile Harbor diverse avian influenza A viruses

Emerging Microbes & Infections ◽

10.1038/s41426-018-0046-9 ◽

2018 ◽

Vol 7 (1) ◽

pp. 1-4 ◽

Cited By ~ 11

Author(s):

Pedro Jiménez-Bluhm ◽

Erik A. Karlsson ◽

Pamela Freiden ◽

Bridgett Sharp ◽

Francisca Di Pillo ◽

...

Keyword(s):

Avian Influenza ◽

Influenza A ◽

Wild Birds ◽

Influenza A Viruses

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Evaluating the role of wild songbirds or rodents in spreading avian influenza virus across an agricultural landscape

PeerJ ◽

10.7717/peerj.4060 ◽

2017 ◽

Vol 5 ◽

pp. e4060 ◽

Cited By ~ 4

Author(s):

Derek D. Houston ◽

Shahan Azeem ◽

Coady W. Lundy ◽

Yuko Sato ◽

Baoqing Guo ◽

...

Keyword(s):

Influenza Virus ◽

Avian Influenza ◽

Avian Influenza Virus ◽

Influenza A Virus ◽

Influenza A ◽

Agricultural Landscape ◽

Clinical Signs ◽

The United States ◽

Wild Birds ◽

Influenza A Viruses

Background Avian influenza virus (AIV) infections occur naturally in wild bird populations and can cross the wildlife-domestic animal interface, often with devastating impacts on commercial poultry. Migratory waterfowl and shorebirds are natural AIV reservoirs and can carry the virus along migratory pathways, often without exhibiting clinical signs. However, these species rarely inhabit poultry farms, so transmission into domestic birds likely occurs through other means. In many cases, human activities are thought to spread the virus into domestic populations. Consequently, biosecurity measures have been implemented to limit human-facilitated outbreaks. The 2015 avian influenza outbreak in the United States, which occurred among poultry operations with strict biosecurity controls, suggests that alternative routes of virus infiltration may exist, including bridge hosts: wild animals that transfer virus from areas of high waterfowl and shorebird densities. Methods Here, we examined small, wild birds (songbirds, woodpeckers, etc.) and mammals in Iowa, one of the regions hit hardest by the 2015 avian influenza epizootic, to determine whether these animals carry AIV. To assess whether influenza A virus was present in other species in Iowa during our sampling period, we also present results from surveillance of waterfowl by the Iowa Department of Natural Resources and Unites Stated Department of Agriculture. Results Capturing animals at wetlands and near poultry facilities, we swabbed 449 individuals, internally and externally, for the presence of influenza A virus and no samples tested positive by qPCR. Similarly, serology from 402 animals showed no antibodies against influenza A. Although several species were captured at both wetland and poultry sites, the overall community structure of wild species differed significantly between these types of sites. In contrast, 83 out of 527 sampled waterfowl tested positive for influenza A via qPCR. Discussion These results suggest that even though influenza A viruses were present on the Iowa landscape at the time of our sampling, small, wild birds and rodents were unlikely to be frequent bridge hosts.

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