J Gen Virol . Emergence of highly pathogenic avian influenza viruses H5N1 and H5N5 in white-tailed eagles, 2021-2023

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J Gen Virol


. 2024 Nov;105(11).
doi: 10.1099/jgv.0.002035. Emergence of highly pathogenic avian influenza viruses H5N1 and H5N5 in white-tailed eagles, 2021-2023

Cathrine Arnason Bøe[SUP] 1 [/SUP], Eve Marie Louise Zeyl Fiskebeck[SUP] 1 [/SUP], Malin Rokseth Reiten[SUP] 1 [/SUP], Johan Åkerstedt[SUP] 1 [/SUP], Maryam Saghafian[SUP] 1 [/SUP], Ragnhild Tønnessen[SUP] 1 [/SUP], Britt Gjerset[SUP] 1 [/SUP], Kjersti Sturød[SUP] 1 [/SUP], Torfinn Moldal[SUP] 1 [/SUP], Grim Rømo[SUP] 1 [/SUP], Morten Helberg[SUP] 2 [/SUP], Duncan Halley[SUP] 3 [/SUP], Lars-Erik Lundblad Rondestveit[SUP] 4 [/SUP], Knut Madslien[SUP] 1 [/SUP], Silje Granstad[SUP] 1 [/SUP]



Affiliations

• PMID: 39485726
• DOI: 10.1099/jgv.0.002035

Abstract

Highly pathogenic avian influenza (HPAI) poses a substantial threat to several raptors. Between 2021 and 2023, HPAI viruses (HPAIVs) of the Goose/Guangdong lineage H5 clade 2.3.4.4b became widespread in wild birds in Norway, and H5N1 and H5N5 viruses were detected in 31 white-tailed eagles (Haliaeetus albicilla, WTEs). Post-mortem examinations of four WTEs revealed no macroscopic pathological findings. Microscopic examinations showed the presence of myocardial and splenic necroses and a few lesions in the brain. In situ hybridization revealed the presence of the virus in several organs, suggesting a multisystemic infection. The detection of HPAIV H5N5 in a WTE in February 2022 marked the first recorded occurrence of this subtype in Norway. Since then, the virus has persisted, sporadically being detected in WTEs and other wild bird species. Phylogenetic analyses reveal that at least two distinct incursions of HPAIV H5N1 Eurasian (EA) genotype C affected WTEs, likely introduced by migratory birds from Eurasia and seabirds entering from Western and Central Europe. Some WTE isolates from 2021 to 2022 clustered with those from Canada and Ireland, aligning with the transatlantic spread of H5N1. Others were related to the 2021 mass mortality of great skuas in the UK or outbreaks in seabird populations, including gannets, gulls and terns, during 2022 in the North Sea region. This suggests that the WTEs were likely preying on the affected birds. Our study highlights that WTEs can act as sentinels for some HPAIV strains, but the absence of several known circulating genotypes in WTEs suggests varying pathogenic effects on this species.

Keywords: H5N1; H5N5; HPAI; Haliaeetus albicilla; histopathology; surveillance.

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Detection and persistence of subtype H5N5 (EA-2021-I) in WTEs and other wild birds on mainland Norway

The subtypes H5N1 and H5N5 were detected in WTEs from the west coast and north along the coastline, overlapping with the known geographic distribution of WTEs in Norway. An HPAIV isolate detected in a WTE found in Bodø (Nordland County) in February 2022 represents the index case of subtype H5N5 (genotype I) in Norway. Strikingly, all detections of genotype I in other wild birds on mainland Norway were limited to Finnmark, the northernmost county of Norway. Our phylogenetic analyses of both the HA and NA gene segments show that the H5N5 viruses from WTEs and the other wild birds on mainland Norway cluster tightly together and are most closely related to H5N5 viruses identified in Russia in November 2021 (EPI_ISL_16209277 and EPI_ISL_16209278). The link between the index case of H5N5 in a Norwegian WTE and Russian isolates has been previously reported by Zinyakov et al. [82], where they suggest the Caspian Region (Russia) as the possible origin of this H5N5 strain. Transmission into Norway could have occurred via migratory birds with flyways from the region around the Caspian Sea to the northwest and northern parts of Norway. Viruses of genotype I have likely persisted in Norway, as they were detected in both 2022 and late 2023 in WTEs and sporadically detected in other avian species (gulls and other raptors) throughout 2023 and 2024 (Fig. 1b) [64]. In September 2022, HPAIV H5N5 was detected in a sample obtained from a WTE in Finland [83], but we were not able to retrieve the sequences from this isolate and thus could not include it in our phylogenetic analyses. Through 2023 and into 2024, genotype I has reached Iceland, the UK, Germany, Greenland, the Faroe Islands, Canada and Japan [64, 84]. We cannot exclude the possibility that some wildlife species may serve as a reservoir for this genotype in Norway. It is possible that certain bird species escape detection in the passive surveillance programme due to subclinical or mild infections caused by genotype I. Such species could be prey for scavenging birds like raptors and gulls, as genotype I has been detected in these bird groups. The sustained presence of genotype I in Norway could also be attributed to favourable conditions for viral longevity, particularly in colder climates. Influenza A virus can retain its infectivity for up to a year in cold and wet environments [85, 86].
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