A Review of Coronaviruses in Wild Birds and Opportunities for Future Research on Migratory Waterfowl

BackgroundThe aim of the study was to explore the ecological diversity of wild birds in Siberia, which are the natural reservoir of avian influenza virus (AIV).MethodsCloacal swabs and intestinal fragments were collected from wild migratory birds from 2007‒2014. Isolated viruses were grown in the allantoic cavity of embryonated chicken eggs. The presence of virus was determined using hemagglutination assays. Primary identification and subtyping of influenza viruses was confirmed by RT-PCR.ResultsA total of 2300 samples obtained from wild migratory birds of 8 orders were collected and tested. Influenza was detected in 185 birds of 3 orders. Species of family Anatidae (order Anseriformes) such as European Teal (Anas crecca), Garganey Teal (A. querquedula), and Shoveler (A. clypeata) play the main role in AIV circulation in the south of Western Siberia. The proportion of viral carriers among waterfowl ranged from 5.6 to 20% in 2007‒2014. The order Charadriiformes had lower virus isolation rates of not more than 1.4%.ConclusionsWild migratory waterfowl of orders Anseriformes and Charadriiformes are the main reservoir of AIV in the south of Western Siberia. This area plays a key role in persistence, evolution, and geographical distribution of avian influenza.

Event Abstract Back to Event Identification of highly pathogenic avian influenza suitable areas for wild birds using species distribution models in South Korea. Lee Kyuyoung1*, Dae-sung Yu2*, Beatriz Martínez-López1, Jaber A. Belkhiria1, Sung-il Kang2, Hachung Yoon2, Seong-Keun Hong2, ILSEOB LEE2, Han-Mo Son2 and Kwangnyeong Lee2 1 Department of Medicine & Epidemiology, School of Veterinary Medicine, University of California, Davis, United States 2 Animal and Plant Quarantine Agency (South Korea), Republic of Korea Highly pathogenic avian influenza (HPAI) virus is influenza A type virus with high mortality and morbidity in the broad range of host species domestic and wild birds to humans. HPAI infection has been a high-priority concern in global poultry industry because of consistent generation and circulation of novel HPAI strains, and consequent tremendous financial losses. Wild birds are considered one of the most important sources of novel HPAI introductions in poultry farms due to the experimental evidence of their asymptomatic infection with viral shedding, genetic closeness of HPAI virus identified in domestic poultry and wild birds, and spatial and temporal coincidence of identification of HPAI in wild birds and domestic poultry. The poultry industry in South Korea has annually suffered from the introduction of novel HPAI strains since early 2000s. HPAI infection in annually migrated wild birds has been carefully monitored to rapidly establish preventive measures of HPAI introduction into poultry farms in South Korea. However, current understanding of highly risk areas or suitable areas for HPAI in wild birds and contribution of other geographical and environmental factors contributing to HPAI vírus suitability is limited. Application of species distribution models based on digitalized geographical and environmental information facilitates our understanding about suitability of wild species’ habitat and its association with environmental and geographical factors. Furthermore, species distribution modelling can be applied to identify high-risk areas of potential disease transmission at the interface between wild species and domestic animals. Our study aimed to evaluate the areas with higher suitability/risk for HPAI identification in wild birds in South Korea and to describe what is the influence or association with the different environmental and geographical factors. Our results will help to not only have a better understanding of the ecology of HPAI in wild birds but also to establish more effective, risk-based, surveillance to prevent novel HPAI introductions into domestic poultry farms in South Korea We obtained land cover, monthly climate (precipitation, temperature and wind speed) and ecological preservation area (Level 1-3) data of South Korea in digitalized form as environmental and geographical data. The observation records of 7 species of wild birds (Baikal teal, white-front goose, common teal, mandarin duck, mallard, bean goose, spot-billed duck) in 206 habitats in South Korea from 1999 to 2017 were used to estimate the suitability map for the wild bird distribution in South Korea. The geographical records of wild bird HPAI surveillance from 2014 to 2018 was combined with 7 wild birds species distribution and environmental and geographical data to estimate the suitability map of HPAI identification in wild birds. Each suitability maps was estimated by maximum entropy approach (Maxent model) via the “dismo” package in R studio. 3. Results and Discussion Our study presents the suitability map of HPAI identification in wild birds and how geographical, environmental factors and 7 wild birds species distributions are contributing to the prediction. These results will not only provide a high-resolution map for the target allocation of surveillance and rapid detection of HPAI in wild birds but also will allow the improvement of the cost-effectiveness of risk-based surveillance of HPAI introduction into domestic poultry farms in South Korea. Acknowledgements This study was supported by the 2019-20 cooperative research grant from the veterinary epidemiology Division in the Animal and Plant Quarantine Agency (APQA) in South Korea and the fellowship of the graduate student support program (GSSP) at UC Davis

Migratory waterfowl and shorebirds are known to be important reservoirs for influenza A viruses (IAV) and they have been repeatedly implicated as causing avian influenza virus (AIV) outbreaks in domestic poultry flocks worldwide. In recent years, wild birds have been implicated in spreading zoonotic H5 influenza viruses to many countries, which has generated high levels of public health concern. Trinidad and Tobago (T&T) is positioned along the wintering route of migratory birds from the Americas; every year, many species of wild birds stopover on the islands of T&T, potentially carrying AIVs and exposing local populations of wild and domestic birds, including commercial poultry, to infection. The aim of this study was to trap, sample, and test as many wild bird species as possible to see whether they were actively infected or previously exposed to AIV. A total of 38 wild birds were trapped, sampled, and tested for IAV RNA, antibodies specific for influenza A nucleoprotein (NP) and antibodies that were specific for H5 and H7 subtypes. Five of the samples tested antibody positive for IAV, while three of these samples had positive titres (≥16) for the H5 subtype, indicating that they were likely to have been previously infected with an H5 IAV subtype. One of the samples tested positive for IAV (M gene) RNA. These results highlight the potential threat that is posed by wild birds to backyard and commercial poultry in T&T and emphasise the importance of maintaining high levels of biosecurity on poultry farms, ensuring that domestic and wild birds are not in direct or indirect contact. The results also underline the need to carry out routine surveillance for AIV in domestic and wild birds in T&T and the wider Caribbean region.

Highly pathogenic avian influenza viruses (HPAIV) can be carried long distances by migratory wild birds and by poultry trade. Highly pathogenic avian influenza (HPAI) is often lethal in domestic poultry and can sporadically infect and cause severe respiratory or systemic disease in other species including humans. Since 2003, the H5 subtype of HPAIV have spread from epicenters in China to neighboring regions in East and Southeast Asia, and across Central Asia to the Indian subcontinent, Europe, Africa, and North America. Outbreaks of H5N1 HPAIV struck poultry in Ukraine in 2005. In 2016, A H5N8 clade 2.3.4.4b HPAIV outbreaks occurred in wild and domestic birds in Ukraine concurrently with outbreaks in Central Europe, Russia, and the Middle East. We report outbreaks of HPAI in domestic backyard poultry in (2016-2017) in the southern region of Ukraine, in proximity to mass gathering sites for migratory waterfowl including mute swans (Cygnus olor). All eight genome segments of three novel H5N8 HPAIV isolated in November 2016 from two domestic backyard chickens (Gallus gallus) and one backyard mallard duck (Anas platyrhynchos) found dead of HPAI in Azov-Black Sea region of Ukraine were cladistically related to H5N8 2.3.4.4b HPAI viruses isolated from wild shelduck (Tadorna tadorna) and white-fronted goose (Anser albifrons) in Askania Nova Biopreserve (Kherson district, Ukraine) in 2016-2017 and to other contemporary H5N8 HPAIV strains sequenced from wild birds and poultry in Eurasia. Amino acid variations in hemagglutinin were outside of the polybasic cleavage site (PLREKRRKR/GLF), and D224G suggested avian-like receptor binding specificity; neuraminidase did not have mutations characteristic of oseltamivir drug resistance. Outbreaks of HPAI in Ukraine highlight the continual need for biosurveillance and genomic sequencing of avian influenza viruses along wild bird flyways and interfaces with domestic poultry in Eurasia.

The Avulavirus within the family Paramyxoviridae includes at least 22 different species, and is known to cause different types of infections and even be fatal in multiple avian species. There is limited knowledge of the genetic and biological information of Avulavirus species 2 to 22 in domestic and wild birds and the disease significance of these viruses in birds is not fully determined, although as many as 10 new distinct species have been identified from wild birds and domestic poultry around the world in the last decade. This study aimed to use PCR, virus isolation, and sequencing to genetically and biologically characterize Avian Orthoavulavirus 16 (AOAV-16) in wild birds and domestic poultry collected from different locations in China between 2014 and 2022. Of five isolated AOAV-16 strains (Y1 to Y5), only the Y4 strain had a haemagglutination (HA)-negative result. All of these isolates were low virulent viruses for chickens, except Y3 which was detected simultaneously with avian influenza virus (AIV) of H9N2 subtype. Furthermore, at least four different types of intergenic sequences (IGS) between the HN and L genes junction, and recombination events, as well as interspecific transmission by wild migratory birds, existed within the species AOAV-16. These findings and results of other reported AOAV-16 strains recommend strict control measures to limit contact between wild migratory birds and domestic poultry and imply potential threats to commercial poultry and even public health challenges worldwide. RESEARCH HIGHLIGHTS First confirmation of AOAV-16 in domestic and wild birds in China. AOAV-16 are low virulent viruses for chickens. Co-circulation/co-infection of AOAV-16 and H9N2 subtype AIV enhanced pathogenicity. Different intergenic sequences and recombination events exist within AOAV-16.

Disease surveillance in England and Wales, April 2021

The aim is to explore the ecological diversity of wild birds in Siberia, which are carriers of the Avian Influenza Virus (AIV). Methods. Biological material in the form of cloacal swabs and intestinal fragments from wild migratory birds were collected in the period 2007-2014 years. The virus has been gained in the allantoic cavity of developing chicken embryos. The presence of virus was determined in hemagglutination and primary identification and subtyping of influenza virus was confirmed by RT-PCR (reverse transcription polymerase chain reaction). Results. It was collected and investigated 2300 samples obtained from wild migratory birds 8 Orders. The influenza virus was detected in 185 birds of the three groups. The main role in the circulation of the AIV in the south of Western Siberia, playing members of the family Anatidae Order Anseriformes, namely species - Teal (Anas crecca), garganey (Anas querquedula), and shoveler (Anas clypeata). In the period from 2007 to 2014, the percentage of virus infection in waterfowl ranged from 5.6 to 20%. Order Charadriiformes was characterized by a lower percentage of virus isolation, of not more than 1.4%. Conclusion. Wild migratory waterfowl orders Anseriformes and Charadriiformes are the main reservoir of AIV in the south of Western Siberia. The area south of Western Siberia plays a key role in the persistence of avian influenza viruses, their evolution and geographical distribution.

Zoonotic transmission of an H5N1 avian influenza A virus to humans in 2003-present has generated increased public health and scientific interest in the prevalence and variability of influenza A viruses in wild birds and their potential threat to human health. Migratory waterfowl and shorebirds are regarded as the primordial reservoir of all influenza A viral subtypes and have been repeatedly implicated in avian influenza outbreaks in domestic poultry and swine. All of the 16 hemagglutinin and nine neuraminidase influenza subtypes have been isolated from wild birds, but waterfowl of the order Anseriformes are the most commonly infected. Using 9-to-11-day-old embryonating chicken egg culture, virus isolation attempts were conducted on 168 cloacal swabs from various resident, imported, and migratory bird species in Barbados during the months of July to October of 2003 and 2004. Hemagglutination assay and reverse transcription-polymerase chain reaction were used to screen all allantoic fluids for the presence of hemagglutinating agents and influenza A virus. Hemagglutination positive-influenza negative samples were also tested for Newcastle disease virus (NDV), which is also found in waterfowl. Two influenza A viruses and one NDV were isolated from Anseriformes (40/168), with isolation rates of 5.0% (2/40) and 2.5% (1/40), respectively, for influenza A and NDV. Sequence analysis of the influenza A virus isolates showed them to be H4N3 viruses that clustered with other North American avian influenza viruses. This is the first report of the presence of influenza A virus and NDV in wild birds in the English-speaking Caribbean.

ABSTRACTRelatively little is known about the distribution of avian paramyxoviruses (APMVs) among wild birds in Japan. Surveillance of APMV in migratory waterfowl was conducted in the San-in region of western Japan during winters of 2006 to 2012. A total of 16 avian paramyxoviruses consisting of 3 lentogenic Newcastle disease viruses (NDVs), 12 APMV-4 and 1 APMV-8 were isolated from 1,967 wild-bird fecal samples. The results show that NDV and APMV-4 are relatively widely distributed among wild waterfowl that migrate to Japan from northern regions. Phylogenetic analysis revealed that there was no genetic relationship between the isolates from wild birds and domestic poultry in Japan. However, surveillance of APMVs in wild waterfowl needs to be conducted due to the pathogenic potential of these isolates in domestic poultry.

Highly Pathogenic Avian Influenza Virus, Midwestern United States.

Avian influenza (AI) viruses have been routinely isolated from a wide diversity of free-living avian species, representing numerous taxonomic orders. Birds in orders Anseriformes and Charadriiformes are considered the natural reservoirs for all AI viruses; it is from these orders that AI viruses have been most frequently isolated. Since first recognized in the late 1800s, AI viruses have been an important cause of disease in poultry and, occasionally, in non-gallinaceous birds and mammals. While AI viruses tend to be of low pathogenicity (LP) in wild birds, the 2014-2015 incursion of highly pathogenic avian influenza (HPAI) clade 2.3.4.4 H5Nx viruses into North America and the recent circulation of HPAI H5 viruses in European wild birds highlight the need for targeted, thorough, and continuous surveillance programs in the wild bird reservoir. Such programs are crucial to understanding the potential risk for the incursion of AI into human and domestic animal populations. The aim of this chapter is to provide general concepts and guidelines for the planning and implementation of surveillance plans for AI viruses in wild birds.

1. Modes of transmission and the origin of H5N1 virusesAvian Influenza (A.I.) is transmitted by infected birds and their excrements. Also, AI is mechanically transmitted by surface means via contaminated food, water, feeds, soil, vehicles, humans, animals, flies, feathers etc. AI viruses can be spread by national or international trades of infected birds and contaminated products. Wild birds, especially migratory waterfowl, are a recognized source and reservoir for all subtypes of AI viruses. Some mammals such as dogs and cats are susceptible to the virus, but they are usually considered as the dead ends.In 1996, H5N1 virus was first detected in Guangdong Province, China. In 1997 the virus became widespread in poultry markets in Hong Kong, and killed 6 of 18 infected persons. The virus was wiped out by culling all domestic poultry in Hong Kong. In 2002, a new H5N1 genotype appeared again in Hong Kong, and the variant strains spread across Southeast Asia and South Asia between 2002 and 2007. The viruses can be divided into several clades such as V1, V2, V3 and Indonesian clades. The strains of H5N1 virus appeared in Korea (2003) and Japan (2004) were closely related to Guangdong strain/174/04 which is distinct from the abov 4 clades.In April 2005, a new variant H5N1 virus, which caused high mortality in both wild birds and poultry, was observed in Quinghai Lake, China. The virus was spread westward through migratory birds into Siberia, Kazakhstan and Turkey. This unprecedented mortality of wild birds associated with H5N1 viruses opened a new window for its movement within wild and domestic birds across Eurasia, the Near East and Africa. Virus strains are divided into 3 clades (EMA 1, 2, 3). The virus isolated in 2007 in Japan is closely related to one of those viruses of Quinghai origin (EMA clades).2. AI situation in EuropeThe European Union decided to make risk assessments of H5N1 virus entering via migratory birds into Europe, and active and passive surveillance for AI virus in wild birds started in July 2005. The conclusion of this study indicated a high risk of introducing the virus via migratory birds, and also a risk of the infection to become enzootic in Europe.The EU encouraged each member country (a) to make an extensive survey of AI viruses in both wild and domestic birds, (b) to vaccinate zoo birds and poultry that cannot be kept in houses (c) to keep all domestic birds in closed housing in high risk areas or zones and (d) to vaccinate domestic birds that cannot be housed.Between 2005 and 2006, H5N1 viruses were detected in wild birds in 25 countries. AI outbreaks in poultry farms were reported from 13 countries in Eastern Europe, and 4 countries in Western Europe (Sweden, Denmark, France and Germany). It is considered that migratory birds played a major role in spreading H5N1 viruses in Europe.The results of the risk control measures in Western Europe can be summarized as follows : (i) It was successful to protect the zoo birds by vaccination, but several birds died due to trauma of vaccination.(ii) Surveillance of wild birds was useful in improving early warning systems for poultry producers, and was effective in reducing the exposure risks of poultry.(iii) Mass culling of poultry and ornamental birds could be avoided.In 2007, H5N1 virus surfaced again in Hungary, UK, Czech R., Germany and France. It seems that H5N1 viruses became enzootic in some countries in Eastern Europe including Russia.(View PDF for the rest of the abstract.)

Avian Influenza (H5N1) Outbreak among Wild Birds, Russia, 2009

Avian influenza is one of the largest known threats to domestic poultry. Influenza outbreaks on poultry farms typically lead to the complete slaughter of the entire domestic bird population, causing severe economic losses worldwide. Moreover, there are highly pathogenic avian influenza (HPAI) strains that are able to infect the swine or human population in addition to their primary avian host and, as such, have the potential of being a global zoonotic and pandemic threat. Migratory birds, especially waterfowl, are a natural reservoir of the avian influenza virus; they carry and exchange different virus strains along their migration routes, leading to antigenic drift and antigenic shift, which results in the emergence of novel HPAI viruses. This requires monitoring over time and in different locations to allow for the upkeep of relevant knowledge on avian influenza virus evolution and the prevention of novel epizootic and epidemic outbreaks. In this review, we assess the role of migratory birds in the spread and introduction of influenza strains on a global level, based on recent data. Our analysis sheds light on the details of viral dissemination linked to avian migration, the viral exchange between migratory waterfowl and domestic poultry, virus ecology in general, and viral evolution as a process tightly linked to bird migration. We also provide insight into methods used to detect and quantify avian influenza in the wild. This review may be beneficial for the influenza research community and may pave the way to novel strategies of avian influenza and HPAI zoonosis outbreak monitoring and prevention.

Coronaviruses (CoVs) are found in a wide variety of wild and domestic animals, and constitute a risk for zoonotic and emerging infectious disease. In poultry, the genetic diversity, evolution, distribution and taxonomy of some coronaviruses have been well described, but little is known about the features of CoVs in wild birds. In this study we screened 764 samples from 22 avian species of the orders Anseriformes and Charadriiformes in Sweden collected in 2006/2007 for CoV, with an overall CoV prevalence of 18.7%, which is higher than many other wild bird surveys. The highest prevalence was found in the diving ducks—mainly Greater Scaup (Aythya marila; 51.5%)—and the dabbling duck Mallard (Anas platyrhynchos; 19.2%). Sequences from two of the Greater Scaup CoV fell into an infrequently detected lineage, shared only with a Tufted Duck (Aythya fuligula) CoV. Coronavirus sequences from Mallards in this study were highly similar to CoV sequences from the sample species and location in 2011, suggesting long-term maintenance in this population. A single Black-headed Gull represented the only positive sample from the order Charadriiformes. Globally, Anas species represent the largest fraction of avian CoV sequences, and there seems to be no host species, geographical or temporal structure. To better understand the eitiology, epidemiology and ecology of these viruses more systematic surveillance of wild birds and subsequent sequencing of detected CoV is imperative.