Mass Mortality Caused by Highly Pathogenic Influenza A(H5N1) Virus in Sandwich Terns, the Netherlands, 2022

Abstract

T he 2021-2022 epidemic of highly pathogenic avian influenza (HPAI) A(H5N1) virus clade 2.3.4.4b has been unprecedented in terms of numbers of dead wild birds, species affected, spatial extent, and incidence in spring 2022 (1). Across Europe, multiple colony-breeding seabirds experienced HPAI H5N1-associated mass mortalities during the breeding period, including the Sandwich tern (Thalasseus sandvicensis) (1,2). The Netherlands constitutes a major though vulnerable stronghold of the Sandwich tern in Europe; 15,000-20,000 breeding pairs have been documented across ≈10 colonies (https://stats. sovon.nl/stats/soort/6110). We sought to establish the scale of mortality occurring in Sandwich terns breeding in the Netherlands in 2022, characterize the associated HPAI H5N1 viruses and pathology, report on the carcass removal effort relative to survival, and investigate intracolony transmission dynamics. The StudyWe determined breeding colony locations and initial sizes in May 2022 through drone or ground counts (3). To establish breeding success and minimum estimates of mortality, we compiled data from late May through early July 2022 on numbers of live adults, chicks, fledglings, and late clutches in colonies, as well as on numbers of carcasses found in and around colonies, carcasses removed for destruction, and abandoned nests (Appendix 1 Table 1, https:// wwwnc.cdc.gov/EID/article/28/12/22-1292-App1. xlsx). Sandwich terns lay 1-2 eggs and incubate for 21-29 days. Chicks fledge 25-30 days after hatching; annual fledging success is ≈0.5 per breeding pair (4-6). We used wild bird mortality databases to establish minimum estimates of adult mortality outside the colonies. Finally, we used data from the migration tracking website Trektellen (https://www.trektellen. nl) to compare the hourly averages of Sandwich tern passing rates at coastal observation points per week in 2022 to 2016-2021.

Pathology of naturally acquired high pathogenicity avian influenza virus H5N1 infection in seabirds

“…Such lesions are like those reported from experimentally challenged common gulls with H5N1, plus naturally infected black headed gulls and herring gulls, together with a recent report of naturally infected sandwich terns ( Thalasseus sandvicensis ). 9,23,43,44,46 Although RT-PCR was not conducted on tissues from the current investigation, the abundance of virus antigens in the heart, brain, kidney, spleen, lung, pancreas, and liver strongly suggests the utility of these organs for diagnostic evaluation.…”

“…The pathway of incursion in free-ranging seabirds is not understood but has been proposed to be either independent incursion or onward introductions from species movements between colonies and the movement of seabirds between mainland and islands particularly during the breeding season. 16,44 Herring gull and great skua can opportunistically predate or scavenge on other birds, 16,26,31,51 and this was observed in the outbreak in gannet colonies. Further, contact transmission between common gulls ( Larus canus ) and European herring gulls have been documented previously with experimental infection with HPAIV H5N1 clade 2.2 and H5N8 clade 2.3.4.4b.…”

“…19 The pathway of incursion in free-ranging seabirds is not understood but has been proposed to be either independent incursion or onward introductions from species movements between colonies and the movement of seabirds between mainland and islands particularly during the breeding season. 16,44 Herring gull and great skua can opportunistically predate or scavenge on other birds, 16,26,31,51 to infectious materials either directly or indirectly through the environment. 17 The distribution and ecology of seabird populations also challenge the current understanding of HPAIV transmission at a global level.…”

“…1,2,12,15,34,36,37,39 More recently there has been an increased detection of HPAI positive seabirds or Charadriiformes, 16,27 and critically, mortality events in seabirds associated with HPAIV infection reported in the UK, Europe and North America. 5,6,44 Data collected through the avian influenza wild bird passive surveillance in Great Britain have shown a rise in high pathogenicity H5Nx positive birds within the Laridae family from 1.3% during the 2020-2021 season and up to 15% within the 2021-2022 season. The potential maintenance of HPAIV in seabirds introduces further uncertainty on the transmission dynamics at both the local and global levels.…”

“…1,2,12,15,34,36,37,39 More recently there has been an increased detection of HPAI positive seabirds or Charadriiformes, 16,27 and critically, mortality events in seabirds associated with HPAIV infection reported in the UK, Europe and North America. 5,6,44 One of the hypotheses for the enzootic transmission of HPAIV in wild birds in Europe is the maintenance in wild birds during summer in Northern Europe. 41 Previously Anseriformes were thought to be responsible for transmission given potential virus adaptation in the host 10,11 but the expansion of avian taxa susceptibility for HPAIV and increased incidence of disease also challenges the status quo.…”