Efficient and Informative Laboratory Testing for Rapid Confirmation of H5N1 (Clade 2.3.4.4) High-Pathogenicity Avian Influenza Outbreaks in the United Kingdom

Slomka, Marek J.; Reid, Scott M.; Byrne, Alexander M. P.; Coward, Vivien; Seekings, James; Cooper, Jayne; Peers-Dent, Jacob; Agyeman-Dua, Eric; Silva, Dilhani de; Hansen, Rowena; Banyard, Ashley C.; Brown, Ian H.

doi:10.3390/v15061344

Cited by 8 publications

(4 citation statements)

References 65 publications

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“…If sampling for live virus, we recommend cloacal swabs be taken in conjunction with oropharyngeal swabs (van den Brand et al 2018, Suarez et al 2000 because of possible differences in virus genotype detectability (Slomka et al 2023). Primary flight feathers can also be used as a diagnostic indication of systemic viral infection as infectious virus can be detected in these samples (Nuradji et al 2015).…”

Section: Discussionmentioning

confidence: 99%

High pathogenicity avian influenza (H5N1) in Northern Gannets (Morus bassanus): Global spread, clinical signs and demographic consequences

Lane,

Jeglinski,

Avery‐Gomm

et al. 2023

Ibis

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During 2021 and 2022 High Pathogenicity Avian Influenza (HPAI) killed thousands of wild birds across Europe and North America, suggesting a change in infection dynamics and a shift to new hosts, including seabirds. Northern Gannets (Morus bassanus) appeared especially severely impacted, but a detailed account of the data available is required to help understand how the virus spread across the metapopulation, and the ensuing demographic consequences. Accordingly, we analyse information on confirmed and suspected HPAIV outbreaks across most North Atlantic Gannet colonies and for the largest colony (Bass Rock, UK), provide impacts on population size, breeding success, and preliminary results on apparent adult survival and serology. Unusually high numbers of dead Gannets were first noted at colonies in Iceland during April 2022. Outbreaks in May occurred in many Scottish colonies, followed by colonies in Canada, Germany and Norway. By the end of June, outbreaks had occurred in colonies in Canada and the English Channel. Outbreaks in 12 UK and Ireland colonies appeared to follow a clockwise pattern with the last infected colonies recorded in late August/September. Unusually high mortality was recorded at 40 colonies (75% of global total colonies). Dead birds testing positive for HPAIV H5N1 were associated with 58% of these colonies. At Bass Rock, the number of occupied nest sites decreased by at least 71%, breeding success declined by ~66% compared to the long‐term UK mean and the resighting of marked individuals suggested that apparent adult survival between 2021 and 2022 could have been substantially lower than the preceding 10‐year average. Serological investigation detected antibodies specific to H5 in apparently healthy birds indicating that some Gannets recover from HPAIV infection. Further, most of these recovered birds had black irises, suggestive of a phenotypic indicator of previous infection. Untangling the impacts of HPAIV infection from other challenges faced by seabirds is key to establishing effective conservation strategies for threatened seabird populations as the likelihood of further epizootics increases, due to increasing habitat loss and the industrialization of poultry production.

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Section: Discussionmentioning

confidence: 99%

High pathogenicity avian influenza (H5N1) in Northern Gannets (Morus bassanus): Global spread, clinical signs and demographic consequences

Lane,

Jeglinski,

Avery‐Gomm

et al. 2023

Ibis

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“…In view of the significant number of UK commercial layer premises that have been affected by H5N1 clade 2.3.4.4b HPAIVs since autumn 2021 [ 34 , 35 ], these in vivo investigations were carried out using a commercial layer breed. However, due to welfare considerations concerning the permitted housing density of the chickens, which is governed by their size (age), it was not possible to use adult point-of-lay hens; hence, 4-week-old layers were used.…”

Section: Discussionmentioning

confidence: 99%

“…The numbers of chickens in each transmission group are clearly very small compared with those observed during recent H5N1 clade 2.3.4.4b HPAIV outbreaks in large commercial poultry premises, which have included spread within layer chickens in the UK [ 35 ]. James et al (2023) also investigated the chicken transmission of the clade 2.3.4.4b descendent H5N1-2021 HPAIV by using six chickens in the respective D0 and R1 groups, with initial infections carried out at different doses, along with an additional transmission attempt where 15 D0 and 15 R1 chickens were cohoused at a greater density [ 25 ].…”

Section: Discussionmentioning

confidence: 99%

Different Outcomes of Chicken Infection with UK-Origin H5N1-2020 and H5N8-2020 High-Pathogenicity Avian Influenza Viruses (Clade 2.3.4.4b)

Seekings,

Warren,

Thomas

et al. 2023

Viruses

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Clade 2.3.4.4 H5Nx highly pathogenic avian influenza viruses (HPAIVs) of the “goose/Guangdong” lineage have caused a series of European epizootics since 2014. During autumn/winter 2020–2021, several H5Nx subtypes were detected in the UK, with H5N8 being the dominant subtype in wild birds and poultry. Despite the greater subtype diversity (due to viral neuraminidase gene reassortment) reported in wild birds, only H5N8 and H5N1 subtypes caused clade 2.3.4.4 UK HPAIV poultry outbreaks during this period. The direct inoculation of layer chickens showed that H5N8-2020 was more infectious than H5N1-2020, which supported the European H5N8 dominance during that season. However, the mean death time was longer for H5N8-2020 (3.42 days) than for H5N1-2020 (2.17 days). Transmission from directly infected to naive in-contact chickens was inefficient for both subtypes. Histological lesions, the tissue dissemination of viral antigen, and nucleic acid were more extensive and abundant and accumulated more rapidly for H5N1-2020 compared with H5N8-2020. Although inefficient, H5N1-2020 transmission was faster, with its greater virulence indicating that this subtype posed a major concern, as subsequently shown during H5N1 dominance of the clade 2.3.4.4 epizootic since autumn 2021. An evaluation of these in vivo viral characteristics is key to understanding the continuing poultry threats posed by clade 2.3.4.4 H5Nx HPAIVs.

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“…In an in vivo investigation, H5N6 HPAIV direct infection of pheasants initiated efficient onward transmission via introduced contact pheasants, despite high mortality [27]. H5Nx HPAIV caused high mortalities in farmed pheasants in the UK, Denmark and Finland during the 2020–2021 and 2021–2022 clade 2.3.4.4b epizootics, but very few infected wild partridges were reported [28–32]. Direct experimental inoculation of closely related chukar partridges ( Alectoris chukar ) with both the North American (2014) H5N8 and H5N2 clade 2.3.4.4 HPAIVs also caused mortality [24].…”

Section: Introductionmentioning

confidence: 99%

Transmission dynamics and pathogenesis differ between pheasants and partridges infected with clade 2.3.4.4b H5N8 and H5N1 high-pathogenicity avian influenza viruses

Seekings,

Liang,

Warren

et al. 2024

Journal of General Virology

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During the UK 2020–2021 epizootic of H5Nx clade 2.3.4.4b high-pathogenicity avian influenza viruses (HPAIVs), high mortality occurred during incursions in commercially farmed common pheasants (Phasianus colchicus). Two pheasant farms, affected separately by H5N8 and H5N1 subtypes, included adjacently housed red-legged partridges (Alectoris rufa), which appeared to be unaffected. Despite extensive ongoing epizootics, H5Nx HPAIV partridge outbreaks were not reported during 2020–2021 and 2021–2022 in the UK, so it is postulated that partridges are more resistant to HPAIV infection than other gamebirds. To assess this, pathogenesis and both intra- and inter-species transmission of UK pheasant-origin H5N8-2021 and H5N1-2021 HPAIVs were investigated. Onward transmission to chickens was also assessed to better understand the risk of spread from gamebirds to other commercial poultry sectors. A lower infectious dose was required to infect pheasants with H5N8-2021 compared to H5N1-2021. However, HPAIV systemic dissemination to multiple organs within pheasants was more rapid following infection with H5N1-2021 than H5N8-2021, with the former attaining generally higher viral RNA levels in tissues. Intraspecies transmission to contact pheasants was successful for both viruses and associated with viral environmental contamination, while interspecies transmission to a first chicken-contact group was also efficient. However, further onward transmission to additional chicken contacts was only achieved with H5N1-2021. Intra-partridge transmission was only successful when high-dose H5N1-2021 was administered, while partridges inoculated with H5N8-2021 failed to shed and transmit, although extensive tissue tropism was observed for both viruses. Mortalities among infected partridges featured a longer incubation period compared to that in pheasants, for both viruses. Therefore, the susceptibility of different gamebird species and pathogenicity outcomes to the ongoing H5Nx clade 2.3.4.4b HPAIVs varies, but pheasants represent a greater likelihood of H5Nx HPAIV introduction into galliforme poultry settings. Consequently, viral maintenance within gamebird populations and risks to poultry species warrant enhanced investigation.

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Efficient and Informative Laboratory Testing for Rapid Confirmation of H5N1 (Clade 2.3.4.4) High-Pathogenicity Avian Influenza Outbreaks in the United Kingdom

Cited by 8 publications

References 65 publications

High pathogenicity avian influenza (H5N1) in Northern Gannets (Morus bassanus): Global spread, clinical signs and demographic consequences

High pathogenicity avian influenza (H5N1) in Northern Gannets (Morus bassanus): Global spread, clinical signs and demographic consequences

Different Outcomes of Chicken Infection with UK-Origin H5N1-2020 and H5N8-2020 High-Pathogenicity Avian Influenza Viruses (Clade 2.3.4.4b)

Transmission dynamics and pathogenesis differ between pheasants and partridges infected with clade 2.3.4.4b H5N8 and H5N1 high-pathogenicity avian influenza viruses

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