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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.

ABSTRACT: Wild-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.IMPORTANCE Integration 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.

SUBMITTER: Li L

PROVIDER: S-EPMC6146819 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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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.

Li Lei L Bowman Andrew S AS DeLiberto Thomas J TJ Killian Mary L ML Krauss Scott S Nolting Jacqueline M JM Torchetti Mia Kim MK Ramey Andrew M AM Reeves Andrew B AB Stallknecht David E DE Webby Richard J RJ Wan Xiu-Feng XF

Journal of virology 20180912 19

Wild-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 ...[more]

PMID: 30045988

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Project description:The 2014 outbreak of clade 2.3.4.4A highly pathogenic avian influenza (HPAI) led to the culling of millions of commercial chickens and turkeys and death of various wild bird species. In this outbreak, older chickens and turkeys were commonly infected, and succumbed to clinical disease compared to younger aged birds such chicken broilers. Some experimental studies using waterfowl species have shown age-related differences in susceptibility to clinical disease with HPAI viruses. Here, we evaluate differences in H5 Hemagglutinin (HA) tissue binding across age groups, using recombinant H5 HA (rHA) proteins generated using gene sequences from low pathogenic (A/mallard/MN/410/2000(H5N2 (LPAIV)) and a HPAIV (A/Northern pintail/Washington/40964/2014(H5N2)) influenza A virus (IAV). Respiratory and intestinal tracts from chickens, ducks (Mallard, Pekin, Muscovy) and turkeys of different age groups were used to detect rHA binding with protein histochemistry, which was quantified as the median area of binding (MAB) used for statistical analysis. There were species and tissue specific differences in the rHA binding among the age groups; however, turkeys had significant differences in the HPAIV rHA binding in the respiratory tract, with younger turkeys having higher levels of binding in the lung compared to the older group. In addition, in the intestinal tract, younger turkeys had higher levels of binding compared to the older birds. Using LPAIV, similar species and tissues, specific differences were seen among the age groups; however, only turkeys had overall significant differences in the respiratory tract MAB, with the older birds having higher levels of binding compared to the younger group. No age-related differences were seen in the overall intestinal tract rHA binding. Age-related differences in rHA binding of the LPAIV and HPAIV demonstrated in this study may partially, but not completely, explain differences in host susceptibility to infection observed during avian influenza outbreaks and in experimental infection studies.

Project description:Highly pathogenic avian influenza (HPAI) viruses of subtype H5Nx caused outbreaks in poultry, captive birds, and wild birds in the Netherlands between October 2020 and June 2021. The full genome sequences of 143 viruses were analyzed. HPAI viruses were mainly of subtype H5N8, followed by H5N1, but also viruses of subtypes H5N3, H5N4, and H5N5 were detected. At least seven distinct genotypes were found, carrying closely related H5 segments belonging to clade 2.3.4.4b. Molecular clock analysis suggests that the reassortments of the NA gene segments likely occurred before the introduction of these viruses into the Netherlands. Genetic analysis suggested that multiple independent introductions of HPAI H5N8 viruses occurred in the Netherlands, likely followed by local spread resulting in at least two clusters of related viruses. The analysis provided evidence for independent introductions from wild birds at 10 poultry farms, whereas for two outbreaks transmission between farms could not be excluded. HPAI H5Nx viruses were detected in dead wild birds of 33 species, but mostly infected geese and swans were found. The pathogenicity of the H5N8 virus was determined for chickens and Pekin ducks, showing reduced mortality for ducks. This study provides more insight into the genetic diversity of HPAI H5Nx viruses generated by reassortment and evolution, and the spread of these viruses between wild birds and poultry. The fast and continuing evolution of H5 clade 2.3.4.4b may provide opportunities for these viruses to adapt to specific bird species, or possibly mammalian species and humans. IMPORTANCE Highly pathogenic avian influenza (HPAI) viruses are spread by migratory wild birds. Viruses causing outbreaks in wild birds and poultry in the Netherlands in 2020-2021 were genetically analyzed, which suggested that multiple virus incursions occurred. The outbreaks in poultry were likely caused by independent introductions from wild birds; only in one case virus spread between farms could not be excluded. Viruses of subtype H5N8 were mainly observed, but also other subtypes were detected that likely evolved by exchange of genetic information before these viruses were introduced into the Netherlands. Viruses were detected in many species of dead wild birds, but mostly in geese and swans. We showed that the H5N8 virus causes a higher mortality in chickens compared to ducks. This is consistent with the fact that not many wild ducks were found dead. This study provides more insight in the evolution and spread of HPAI viruses in wild birds and poultry.

Dataset Information

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.

Publications

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.

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