Early Release – Effect of 2020–21 and 2021–22 Highly Pathogenic Avian Influenza H5 Epidemics on Wild Birds, the Netherlands – Quantity 30, #1—January 2024 – Rising Infectious Illnesses journal

The strategies for this research had been just like these utilized by Kleyheeg et al. (11). In transient, we collected wild chicken mortality information from 2 full chicken influenza seasons, October 1, 2020–September 30, 2021, and October 1, 2021–September 30, 2022. The nationwide competent authorities reported useless wild birds to the AI-Impact consortium as a part of the nationwide animal infectious illness surveillance program and by citizen scientists who had been invited to report sightings of useless birds on the internet platforms of the AI-Impact members (https://dwhc.nl/dode-vogels-melden/, https://www.sovon.nl/nl/content/vogelgriep, https://www.nvwa.nl/onderwerpen/vogelgriep-preventie-en-bestrijding, https://waarneming.nl). In addition, all seabird strandings information alongside the Dutch North Sea and Wadden Sea coasts had been analyzed as a part of a long-term monitoring undertaking and checked for unusually excessive numbers of stranded birds with effort correction (quantity per km of shoreline searched, n km^–1) (12,13). Unusually excessive densities (i.e., stranded birds per space) had been >5 instances background densities, as measured utilizing similar surveys from the earlier 40 years in any given month. Double counts didn’t happen on this dataset as a result of carcasses had been marked.

We categorized reviews by chicken species, date, and placement of discovering. Double counts (e.g., a number of entries for a similar species on the identical date, on the similar location from the identical observer) had been excluded as a lot as attainable. Consistent with related research, we discovered it extremely seemingly that the variety of reported carcasses considerably underestimates precise deaths; for instance, assortment charges of water chicken carcasses throughout typical avian botulism outbreaks are 10%–25% (14).

We categorized wild chicken mortality reviews into 4 teams: Anatidae (i.e., geese, swans, geese), different water birds (together with gulls, grebes, herons, cormorants, waders, rallids), raptors, and different land birds. We labeled birds of the households Podicipedidae, Laridae, Stercorariidae, Alcidae, Gaviidae, Procellariidae, Sulidae, and Phalacrocoracidae, in 1 subgroup, sea birds. We analyzed mortality information of chosen species individually, as a result of they skilled significantly excessive mortality charges throughout both the 2020–21 epidemic (i.e., barnacle goose [Branta leucopsis], widespread buzzard [Buteo buteo], peregrine falcon [Falco peregrinus], nice black-backed gull [Larus marinus], or through the 2021–22 epidemic (i.e., Sandwich tern [Thalasseus sandvicensis], northern gannet [Morus bassanus]). We used information from the general public database of Sovon (Dutch Centre for Field Ornithology, Nijmegen, the Netherlands; https://www.sovon.nl) to check the variety of reported useless wild birds per avian group throughout October–March (labeled as winter mortality) and April–September (labeled as summer season mortality) between the 2020–21 and 2021–22 epidemics; we then in contrast information for a similar months of 2010–11 with 2015–16 as described by Kleyheeg et al. (11). In the later interval (2010–2016), there had been no outbreaks of HPAI in wild birds within the Netherlands. We examined a restricted variety of wild chicken carcasses (Appendix 1 Table) for HPAI virus by real-time reverse transcription PCR on oropharyngeal and cloacal swabs as beforehand described (15,16). We submitted teams of >3 useless wild birds of sure classes (i.e., Anatidae, water birds) discovered useless on the similar location, and single birds of different prone species (i.e., raptors) that had been suspected of being HPAI virus-infected, for virologic evaluation.

We used species information on dwell inhabitants estimates from the general public database of Sovon to judge mortality charges by chicken species (Table; Appendix 1 Table). Population dimension represents the estimated lowest and highest variety of birds wintering within the Netherlands, primarily based on census information for 2013–2020 from Sovon. For summer season migratory species, inhabitants dimension represents the estimated lowest and highest variety of birds migrating to the Netherlands, primarily based on census information for 2016–2021 from Sovon.

A complete of 16,631 wild birds of 160 species had been reported useless within the Netherlands in October 1, 2020–September 30, 2021. Water birds together with Anatidae accounted for 70% of the whole deaths reported and land birds, together with raptors, the remaining 30% (Table 1).

Anatidae by themselves represented 50% of the whole deaths reported. Of the chicken carcasses recognized to species, by far the very best variety of deaths had been reported for barnacle geese (n = 3,435). The subsequent highest numbers of useless animals had been reported for graylag geese (n = 390), widespread buzzards (n = 365), and mute swans (Cygnus olor) (n = 305). HPAI virus an infection was reported in 45 species (Appendix 1 Table). The species with the very best numbers of reported useless and contaminated birds had been throughout the Anatidae group: barnacle geese, graylag geese, and mute swans. Common buzzard was the species with the very best numbers of reported useless and contaminated birds throughout the raptor group. Expressed as fraction of the nonbreeding inhabitants, and after accounting for detection likelihood, the reported useless birds represented as much as 4.8% of barnacle geese, 0.7% of graylag geese, and seven.4% of mute swans (Table 1). We discovered the very best mortality charges occurred in raptors and scavenging species: relative to their wintering populations, as much as 54% of peregrine falcons, 12.1% of widespread buzzards, and 5.4% of nice black-backed gulls might have died.

Figure 1

Figure 1. Relative variety of reported deaths through the extremely pathogenic avian influenza epidemics of 2020–21 (crimson asterisks), and 2021–22 (blue asterisks), the Netherlands. Deaths are relative to the normalized variety of…

A complete of 41,519 wild birds of 158 species had been reported useless within the Netherlands throughout October 1, 2021–September 30, 2022. Water birds together with Anatidae accounted for 80% and land birds together with raptors for the remaining 20% of the whole deaths reported (Table 1). Sea birds represented >40% and Anatidae 30% of the whole deaths. Of the chicken carcasses recognized to species, the very best quantity was reported for the barnacle goose (n = 5,310). The subsequent highest numbers of useless people had been reported for Sandwich terns (n = 5,166), and northern gannets (n = 2,215). HPAI virus an infection was confirmed in 51 species (Appendix 1 Table). The species with the very best numbers of reported useless and contaminated birds had been throughout the sea chicken and Anatidae teams, and the species most represented had been the Sandwich tern and the barnacle goose. Expressed as a fraction of the nonbreeding inhabitants, and after accounting for detection likelihood, the reported useless birds represented 32.8%–90% of northern gannets and as much as 7.4% of barnacle geese (Table 1). The Sandwich tern seems as a summer season breeder within the Netherlands; after accounting for detection likelihood, the reported useless birds represented 17.2%–90% of the estimated migrant inhabitants of Sandwich terns. We discovered that prime mortality charges additionally occurred in raptors: as much as 56% of wintering populations of peregrine falcons and 12.1% of widespread buzzards might have died. Mortality charges in winter or summer season months had been larger than the common estimates in earlier years (i.e., in comparison with the identical timeframe in 2011–2016, years by which main wild chicken mortalities from outbreaks of HPAI virus didn’t happen). In explicit, the variety of reported carcasses was >50 instances larger for geese in winter 2022 and >1,000 instances larger for Sandwich terns in summer season 2022 (Figure 1).

Figure 2

Figure 2. Temporal sample of untamed chicken deaths through the 2020–21 and 2021–22 extremely pathogenic avian influenza epidemics, the Netherlands. Sea birds embrace the chicken households of Podicipedidae, Laridae, Stercorariidae, Alcidae, Gaviidae,…

During the 2020–21 epidemic within the Netherlands, wild chicken deaths clustered in 2 peaks, the primary in November 2020 and the second, smaller peak in April–May 2021 (Figure 2). During each peaks, barnacle geese had been among the many species most severely affected. During the 2021–22 epidemic within the Netherlands, wild chicken deaths additionally confirmed 2 peaks, the primary in January 2022 and the second in June 2022 (Figure 2). During the primary peak, barnacle geese had been once more among the many species most severely affected, and through the second peak, sea birds had been probably the most severely affected. The virus was nonetheless detected in October 2022, however that date was thought of the beginning of the brand new HPAI 2022–23 outbreak.

HPAI dynamics in wild birds are continually evolving. The 2020–21 HPAI H5 epidemic was extra devastating than earlier HPAI H5 epidemics in Europe, inflicting excessive numbers of HPAI infections and deaths in lots of species of untamed birds (4,9,17–19). Goose species, such because the barnacle goose, accounted for the very best variety of casualties. During that epidemic, excessive prevalence of an infection in geese was additionally reported in Germany and United Kingdom (2). In our research, a number of duck species constantly examined constructive for HPAI H5 virus through the epidemic; nonetheless, reported deaths for these species had been decrease than for goose species. This discovering represents a distinct state of affairs than that of the 2016–17 HPAI H5 epidemic, by which duck species, similar to Eurasian wigeons (Mareca penelope) and tufted geese (Aythya fuligula), skilled the very best variety of deaths (11). The excessive mortality price of barnacle geese through the 2020–21 HPAI H5 epidemic is unprecedented. Barnacle geese are one of the plentiful geese species within the Netherlands (19,20); they’re gregarious, herbivorous birds with a desire for coastal grassland and water-rich agricultural fields (21,22). Barnacle geese share their wintering habitat with different herbivorous birds, similar to Eurasian wigeons and mute swans (Cygnus olor). The massive variety of geese and their gregarious conduct seemingly enabled the intraspecies transmission of the virus by direct or oblique contact (e.g., contaminated grass, contaminated water). The plentiful circulation of HPAI H5 virus in new host species signifies that the virus has develop into properly tailored to transmission in these species. During the 2020–21 epidemic, HPAI H5 virus was recovered from wild chicken populations within the Netherlands for >1 yr, indicating that it may be unfold and maintained long-term in these populations (4,9), a brand new commentary for the reason that 2016–17 HPAI H5 epidemic, by which viral circulation was primarily restricted to autumn and winter (11). A consequence of the bizarre persistence of the virus into summer season was that naive, newly hatched birds, particularly juvenile Anseriformes similar to mute swans and graylag geese and raptors similar to white-tailed eagle (Haliaeetus albicilla), had been uncovered to the virus and died from an infection throughout spring and summer season 2021 (9). The massive variety of contaminated wild birds, both unwell or useless, was a probable determinant for interspecies viral transmission to looking or scavenger chicken species. Raptors, for instance, are uncovered to an infection by ingesting contaminated prey (23). During the epidemic, 11 totally different raptor species had been discovered to be contaminated, and the very best variety of infections and deaths occurred within the widespread buzzard (Table; Appendix 1 Table). Among the nonraptor scavenger species, we discovered 6 totally different species of gulls (Laridae) and 4 species of corvid (Corvidae) to be contaminated (Table; Appendix). Because the populations sure raptor species, such because the peregrine falcon, are comparatively small, HPAI might characterize a brand new risk for his or her conservation. Clinical indicators of the an infection in wild raptors had been primarily neurologic, similar to incoordination, physique tremors, and torticollis, and had been related to mind lesions and a excessive stage of neurotropism (23).

The 2021–22 HPAI H5 virus epidemic has prompted the very best variety of casualties amongst wild birds ever recorded in Europe (4). A major change within the dynamic of the infections was that, since summer season 2021, the virus has been enzootic in wild chicken populations in Europe (1,2). This unprecedented, steady circulation of virus throughout spring and summer season additionally uncovered colonial sea birds to an infection (5). During the spring, colonial sea birds congregate in excessive quantity at their coastal breeding grounds. In this setting the virus may unfold extensively inside and between breeding colonies, inflicting outbreaks that resulted in excessive grownup and chick deaths (6,7). Sandwich terns had been among the many sea chicken species that had been extra severely affected by the HPAI epidemic within the Netherlands. The sandwich tern is a vulnerable, migratory species that solely breeds in a restricted variety of colonies throughout Europe seasonally, throughout April–September. Infection-associated mass mortality, with a mortality peak in June, was seen in 9 of the ten Sandwich tern breeding colonies within the Netherlands (6). The HPAI-associated mass mortality occasion is a extreme risk for the conservation of this species. Mass dieoffs within the breeding colonies will most probably have long-term repercussions for the Sandwich tern inhabitants (6). Constant monitoring of the surviving birds will probably be essential to assess the long-term impact of HPAI on this species within the coming years.

The northern gannet is one other colonial sea chicken species that seasonally happens off the coast of the Netherlands, though it doesn’t breed within the Netherlands, and that was severely affected by the HPAI epidemic. The HPAI-associated infections began in April and reached a peak in July 2022. We recorded excessive mortality of breeding gannets on nests; massive numbers of carcasses of gannets had been sighted afloat close to a number of of the biggest or most vital breeding colonies and widespread within the North Sea basin (7). The ecology and sample of mortalities of northern gannets have been studied within the Netherlands since 1980. Data from this long-term research enabled correct analysis of the 2022 mortality occasion in relation to background mortality and corrected per observer effort (24). For the northern gannet the variety of reported corpses in July 2022 was 66 instances bigger than common in earlier years, the very best spike in deaths over the previous 40 years (24).

During the 2021–22 epidemic, excessive mortality charges in sea chicken species had been additionally reported in different nations in and out of doors of Europe. For instance, Dalmatian pelicans (Pelecanus crispus) in Greece and nice skuas (Stercorarius skua) on Foula, United Kingdom, each had 60%–70% declines of their populations due to HPAI virus an infection throughout colonial breeding (7,8,25). The excessive density of birds and their shut contact throughout colonial breeding in all probability enabled the speedy unfold of the an infection throughout the colonies. Field information recommend that HPAI-positive birds may shed virus for some interval earlier than demise, offering alternatives for direct bird-to-bird or environmental transmission (26). Bird species similar to nice skuas have been reported to wash and socialize at freshwater lochs and swimming pools, offering attainable alternatives for conspecific an infection (7). Scavenging actions are one other attainable supply of an infection. Unattended chicks from useless mother and father most probably died due to lack of parental care. Maternal antibodies have been described in chicks of beforehand contaminated mother and father, however medical safety is short-lived and requires excessive maternal antibody titers (27,28). Furthermore, maternal antibodies are solely related if the an infection has occurred earlier than egg laying. Infected birds of sure Anatidae species can survive HPAI virus an infection with restricted medical penalties (29,30). Experimentally serially contaminated geese can develop a long-term immunity that confers safety from subsequent HPAI virus an infection (29). It is feasible that sea chicken species can even develop flock immunity protecting at future reinfection. The surviving birds must be examined for the presence of serum antibodies to assemble information about flock immunity over the subsequent a number of years.

The huge variety of useless birds at colonies posed a biosecurity subject by way of the danger for viral spillover; cleansing up was an amazing activity for the concerned authorities. The AI-Impact consortium, along with the competent well being authorities, offered a call tree for the cleanup of useless birds to cut back the environmental contamination with minimal disturbance for the remaining birds (Appendix 2; Appendix 3). Carcass elimination is critical to cut back the quantity of contaminated materials that might unfold the an infection within the atmosphere (6). Thus, we suggest managed research to optimize carcass elimination.

During spring 2021, for the primary time for the reason that 2005–06 HPAI H5 epidemic, the virus was detected in Europe in a number of carnivore species, European foxes (Vulpes vulpes), grey seals (Halichoerus grypus), and harbor seals (Phoca vitulina); they had been most probably contaminated by way of contact with or ingestion of contaminated wild birds (9,31). HPAI H5 viruses had been as soon as once more detected in wild mammal species in Europe through the 2021–22 season and confirmed genetic markers of adaptation to replication in mammals (16). Therefore, we suggest deliberate year-round lively and passive surveillance of untamed mammals. The zoonotic threat for an infection for people of this explicit H5 virus pressure is taken into account low for the final inhabitants and low to medium for occupationally uncovered employees, similar to culling operators, wild animal rehabilitators, and employees concerned in carcass elimination (16). Persons at occupational threat ought to put on satisfactory private protecting tools and be immunized with preventive annual vaccination towards human influenza to keep away from reassortment with HPAI H5 virus. In case of potential an infection, these individuals must be monitored for respiratory signs, neurologic signs, or conjunctivitis for 10 days after publicity (16), and diagnostic testing, if needed, must be carried out on the competent nationwide well being authority.

Since the top of 2016, mass mortality occasions amongst wild birds attributable to HPAI H5 an infection within the Netherlands have occurred in varied species in varied years, together with Eurasian wigeon (2016), tufted duck (2016), barnacle goose (2020–2022), Sandwich tern (2022), and black-headed gull (Chroicocephalus ridibundus) (2023) (16). One attribute these species have in widespread is that they dwell in dense teams at sure instances of the yr (10) and dwell near open water. We suspected that this mixture is a vital threat issue for an infection, as a result of such teams have extra alternatives for virus publicity and transmission and for attainable species-specific adaptation of the virus (10). However, susceptibility to illness from HPAI virus an infection appears to range enormously between species. For instance, illness and demise can peak in a single species whereas different species equally current in the identical space present hardly any indicators of illness (10).

Because it stays tough to anticipate and to mannequin the longer term traits of HPAI amongst wild birds, we suggest fixed monitoring of dwell and useless wild birds as an important software for surveillance of the evolving dynamics of HPAI. This methodology has a number of limitations; one is that it’s tough to exclude double-counted reviews. Another is that not all of the reported useless birds could be examined for HPAI virus an infection, and never all could have died from HPAI an infection. Two principal enhancements that we suggest for HPAI surveillance in wild birds are long-term monitoring of HPAI-associated wild chicken deaths, corrected for observer effort, and testing apparently wholesome wild birds, significantly candidate reservoir species, for each HPAI virus and antibodies to HPAI virus. For the fixed monitoring of untamed chicken deaths within the Netherlands through the 2020–21 and 2021–22 HPAI H5 epidemics, citizen scientists had been a elementary useful resource and made it attainable to acquire a wider impression of the particular scale of mortality in wild birds, which in any other case would have been restricted to the info from official surveillance. In addition to surveillance for HPAI, we suggest recording of untamed chicken deaths and inspiring and systematically endorsing the work of citizen scientists and worldwide citizen-science platforms.