Highly pathogenic avian influenza (HPAI) H5N1 was first encountered in 1996 in Guangdong province (China) and started spreading throughout Asia and the western Palearctic in 2004-2006. Compared to ...several other countries where the HPAI H5N1 distribution has been studied in some detail, little is known about the environmental correlates of the HPAI H5N1 distribution in China. HPAI H5N1 clinical disease outbreaks, and HPAI virus (HPAIV) H5N1 isolated from active risk-based surveillance sampling of domestic poultry (referred to as HPAIV H5N1 surveillance positives in this manuscript) were modeled separately using seven risk variables: chicken, domestic waterfowl population density, proportion of land covered by rice or surface water, cropping intensity, elevation, and human population density. We used bootstrapped logistic regression and boosted regression trees (BRT) with cross-validation to identify the weight of each variable, to assess the predictive power of the models, and to map the distribution of HPAI H5N1 risk. HPAI H5N1 clinical disease outbreak occurrence in domestic poultry was mainly associated with chicken density, human population density, and elevation. In contrast, HPAIV H5N1 infection identified by risk-based surveillance was associated with domestic waterfowl density, human population density, and the proportion of land covered by surface water. Both models had a high explanatory power (mean AUC ranging from 0.864 to 0.967). The map of HPAIV H5N1 risk distribution based on active surveillance data emphasized areas south of the Yangtze River, while the distribution of reported outbreak risk extended further North, where the density of poultry and humans is higher. We quantified the statistical association between HPAI H5N1 outbreak, HPAIV distribution and post-vaccination levels of seropositivity (percentage of effective post-vaccination seroconversion in vaccinated birds) and found that provinces with either outbreaks or HPAIV H5N1 surveillance positives in 2007-2009 appeared to have had lower antibody response to vaccination. The distribution of HPAI H5N1 risk in China appears more limited geographically than previously assessed, offering prospects for better targeted surveillance and control interventions.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Wild waterbirds, the natural reservoirs for avian influenza viruses, undergo migratory movements each year, connecting breeding and wintering grounds within broad corridors known as flyways. In a ...continental or global view, the study of virus movements within and across flyways is important to understanding virus diversity, evolution, and movement. From 2015 to 2017, we sampled waterfowl from breeding (Maine) and wintering (Maryland) areas within the Atlantic Flyway (AF) along the east coast of North America to investigate the spatio-temporal trends in persistence and spread of influenza A viruses (IAV). We isolated 109 IAVs from 1,821 cloacal / oropharyngeal samples targeting mallards (Anas platyrhynchos) and American black ducks (Anas rubripes), two species having ecological and conservation importance in the flyway that are also host reservoirs of IAV. Isolates with >99% nucleotide similarity at all gene segments were found between eight pairs of birds in the northern site across years, indicating some degree of stability among genome constellations and the possibility of environmental persistence. No movement of whole genome constellations were identified between the two parts of the flyway, however, virus gene flow between the northern and southern study locations was evident. Examination of banding records indicate direct migratory waterfowl movements between the two locations within an annual season, providing a mechanism for the inferred viral gene flow. Bayesian phylogenetic analyses provided evidence for virus dissemination from other North American wild birds to AF dabbling ducks (Anatinae), shorebirds (Charidriformes), and poultry (Galliformes). Evidence was found for virus dissemination from shorebirds to gulls (Laridae), and dabbling ducks to shorebirds and poultry. The findings from this study contribute to the understanding of IAV ecology in waterfowl within the AF.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Significance Highly pathogenic avian influenza virus H5N1 first emerged in Asia and subsequently unfolded into the first avian influenza panzootic, causing major economic losses in the poultry ...sector. However, we still do not understand the regional long-distance transmission and seasonal patterns of H5N1. In this study, we addressed this issue by combining H5N1 outbreak records, whole-genome sequences of viral samples, and satellite tracking data for four species of migratory birds in Asia. We show that timing of H5N1 outbreaks and viral migration are closely associated with known bird migration routes. The flyway is the major viral transmission barrier to the intracontinental spread of H5N1 by migratory birds in Asia, whereas geographic distances within the flyways have little effect on H5N1 transmission.
The spatial spread of the highly pathogenic avian influenza virus H5N1 and its long-term persistence in Asia have resulted in avian influenza panzootics and enormous economic losses in the poultry sector. However, an understanding of the regional long-distance transmission and seasonal patterns of the virus is still lacking. In this study, we present a phylogeographic approach to reconstruct the viral migration network. We show that within each wild fowl migratory flyway, the timing of H5N1 outbreaks and viral migrations are closely associated, but little viral transmission was observed between the flyways. The bird migration network is shown to better reflect the observed viral gene sequence data than other networks and contributes to seasonal H5N1 epidemics in local regions and its large-scale transmission along flyways. These findings have potentially far-reaching consequences, improving our understanding of how bird migration drives the periodic reemergence of H5N1 in Asia.
Qinghai Lake in central China has been at the center of debate on whether wild birds play a role in circulation of highly pathogenic avian influenza virus H5N1. In 2005, an unprecedented epizootic at ...Qinghai Lake killed more than 6000 migratory birds including over 3000 bar-headed geese (Anser indicus). H5N1 subsequently spread to Europe and Africa, and in following years has re-emerged in wild birds along the Central Asia flyway several times.
To better understand the potential involvement of wild birds in the spread of H5N1, we studied the movements of bar-headed geese marked with GPS satellite transmitters at Qinghai Lake in relation to virus outbreaks and disease risk factors. We discovered a previously undocumented migratory pathway between Qinghai Lake and the Lhasa Valley of Tibet where 93% of the 29 marked geese overwintered. From 2003-2009, sixteen outbreaks in poultry or wild birds were confirmed on the Qinghai-Tibet Plateau, and the majority were located within the migratory pathway of the geese. Spatial and temporal concordance between goose movements and three potential H5N1 virus sources (poultry farms, a captive bar-headed goose facility, and H5N1 outbreak locations) indicated ample opportunities existed for virus spillover and infection of migratory geese on the wintering grounds. Their potential as a vector of H5N1 was supported by rapid migration movements of some geese and genetic relatedness of H5N1 virus isolated from geese in Tibet and Qinghai Lake.
This is the first study to compare phylogenetics of the virus with spatial ecology of its host, and the combined results suggest that wild birds play a role in the spread of H5N1 in this region. However, the strength of the evidence would be improved with additional sequences from both poultry and wild birds on the Qinghai-Tibet Plateau where H5N1 has a clear stronghold.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Habitat loss can trigger migration network collapse by isolating migratory bird breeding grounds from nonbreeding grounds. Theoretically, habitat loss can have vastly different impacts depending on ...the site's importance within the migratory corridor. However, migration‐network connectivity and the impacts of site loss are not completely understood. We used GPS tracking data on 4 bird species in the Asian flyways to construct migration networks and proposed a framework for assessing network connectivity for migratory species. We used a node‐removal process to identify stopover sites with the highest impact on connectivity. In general, migration networks with fewer stopover sites were more vulnerable to habitat loss. Node removal in order from the highest to lowest degree of habitat loss yielded an increase of network resistance similar to random removal. In contrast, resistance increased more rapidly when removing nodes in order from the highest to lowest betweenness value (quantified by the number of shortest paths passing through the specific node). We quantified the risk of migration network collapse and identified crucial sites by first selecting sites with large contributions to network connectivity and then identifying which of those sites were likely to be removed from the network (i.e., sites with habitat loss). Among these crucial sites, 42% were not designated as protected areas. Setting priorities for site protection should account for a site's position in the migration network, rather than only site‐specific characteristics. Our framework for assessing migration‐network connectivity enables site prioritization for conservation of migratory species.
Un Enfoque de Redes para Priorizar los Esfuerzos de Conservación para las Aves Migratorias
Resumen
La pérdida del hábitat puede disparar el colapso de las redes de migración al aislar los sitios de reproducción de las aves migratorias de aquellos sitios que no se usan para la reproducción. En teoría, la pérdida del hábitat puede tener impactos muy diferentes dependiendo de la importancia del sitio dentro del corredor migratorio. Sin embargo, la conectividad entre las redes de migración y los impactos de la pérdida de los sitios no están del todo comprendidos. Usamos los datos de seguimiento por GPS de cuatro especies de aves en las rutas de vuelo de Asia para construir redes de migración y propusimos un marco de trabajo para evaluar la conectividad de las redes en las especies migratorias. Usamos un proceso de extracción de nodos para identificar los sitios de escala con el mayor impacto sobre la conectividad. En general, las redes de migración con menos sitios de escala fueron más vulnerables a la pérdida del hábitat. La extracción de nodos en orden del grado más alto al más bajo resultó en un incremento de resistencia de la red similar a la extracción al azar. Al contrario, la resistencia incrementó más rápidamente cuando la extracción de los nodos fue en orden del más alto al más bajo valor de intermediación (cuantificado por el número de caminos más cortos que pasan por un nodo específico). Cuantificamos el riesgo de colapso de la red de migración e identificamos sitios cruciales al seleccionar primero los sitios con mayores contribuciones a la conectividad de la red y después identificar cuáles de esos sitios tenían probabilidad de ser removidos de la red (es decir, sitios con pérdida de hábitat). Entre estos sitios cruciales, el 42% no estaban designados como áreas protegidas. El establecimiento de prioridades para la protección de un sitio debería considerar la posición del sitio dentro de la red de migración, en lugar de sólo considerar las características específicas del sitio. Nuestro marco de trabajo para la evaluación de la conectividad de la red de migración permite la priorización de sitios para la conservación de las especies migratorias.
摘要
栖息地丧失导致的迁徙鸟类繁殖地和非繁殖地隔离会引发迁徙网络的瓦解。理论上, 取决于该栖息地在迁徙廊道里的重要性, 不同栖息地节点的丧失会对迁徙网络造成不同的影响, 但目前对迁徙网络连通性以及栖息地丧失对迁徙网络影响的理解还不完善。本研究基于亚洲迁徙路线上4 种迁徙鸟类物种的 GPS 追踪数据, 分别构建了迁徙网络并提出了衡量迁徙物种迁徙网络连通性的方法体系。我们使用节点去除法来确定高重要性中途停歇地。具有较少停歇地的迁徙网络通常受栖息地丧失的威胁更严重。我们发现, 依据栖息地丧失程度由高到低的顺序去除栖息地, 迁徙网络阻力的增加趋势与随机去除栖息地结果基本一致。而如果依据栖息地节点的中间值 (表征通过该节点的最短路径数量) 由高到低的顺序去除栖息地节点, 迁徙阻力则呈现快速上升。我们量化了迁徙网络瓦解的风险并基于栖息地节点对迁徙网络连通性的贡献和节点的脆弱性 (栖息地退化程度) 识别了关键栖息地。其中 42% 的关键栖息地处于非保护地状态。我们建议设定栖息地优先保护级别时需要考虑该栖息地在迁徙网络中的位置和作用, 而不是仅依据该栖息地的本身特征。本研究提出的栖息地网络连通性评价体系为迁徙物种栖息地优先保护提供了重要理论和方法依据。
Article impact statement: Analysis of migration‐network connectivity enables the prioritization for site conservation.
Abstract The wild to domestic bird interface is an important nexus for emergence and transmission of highly pathogenic avian influenza (HPAI) viruses. Although the recent incursion of HPAI H5N1 Clade ...2.3.4.4b into North America calls for emergency response and planning given the unprecedented scale, readily available data-driven models are lacking. Here, we provide high resolution spatial and temporal transmission risk models for the contiguous United States. Considering virus host ecology, we included weekly species-level wild waterfowl (Anatidae) abundance and endemic low pathogenic avian influenza virus prevalence metrics in combination with number of poultry farms per commodity type and relative biosecurity risks at two spatial scales: 3 km and county-level. Spillover risk varied across the annual cycle of waterfowl migration and some locations exhibited persistent risk throughout the year given higher poultry production. Validation using wild bird introduction events identified by phylogenetic analysis from 2022 to 2023 HPAI poultry outbreaks indicate strong model performance. The modular nature of our approach lends itself to building upon updated datasets under evolving conditions, testing hypothetical scenarios, or customizing results with proprietary data. This research demonstrates an adaptive approach for developing models to inform preparedness and response as novel outbreaks occur, viruses evolve, and additional data become available.
A unique pattern of highly pathogenic avian influenza (HPAI) H5N1 outbreaks has emerged along the Central Asia Flyway, where infection of wild birds has been reported with steady frequency since ...2005. We assessed the potential for two hosts of HPAI H5N1, the bar-headed goose (Anser indicus) and ruddy shelduck (Tadorna tadorna), to act as agents for virus dispersal along this 'thoroughfare'. We used an eco-virological approach to compare the migration of 141 birds marked with GPS satellite transmitters during 2005-2010 with: 1) the spatio-temporal patterns of poultry and wild bird outbreaks of HPAI H5N1, and 2) the trajectory of the virus in the outbreak region based on phylogeographic mapping. We found that biweekly utilization distributions (UDs) for 19.2% of bar-headed geese and 46.2% of ruddy shelduck were significantly associated with outbreaks. Ruddy shelduck showed highest correlation with poultry outbreaks owing to their wintering distribution in South Asia, where there is considerable opportunity for HPAI H5N1 spillover from poultry. Both species showed correlation with wild bird outbreaks during the spring migration, suggesting they may be involved in the northward movement of the virus. However, phylogeographic mapping of HPAI H5N1 clades 2.2 and 2.3 did not support dissemination of the virus in a northern direction along the migration corridor. In particular, two subclades (2.2.1 and 2.3.2) moved in a strictly southern direction in contrast to our spatio-temporal analysis of bird migration. Our attempt to reconcile the disciplines of wild bird ecology and HPAI H5N1 virology highlights prospects offered by both approaches as well as their limitations.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
In Bangladesh, the poultry industry is an economically and socially important sector, but it is persistently threatened by the effects of H5N1 highly pathogenic avian influenza. Thus, identifying the ...optimal control policy in response to an emerging disease outbreak is a key challenge for policy-makers. To inform this aim, a common approach is to carry out simulation studies comparing plausible strategies, while accounting for known capacity restrictions. In this study we perform simulations of a previously developed H5N1 influenza transmission model framework, fitted to two separate historical outbreaks, to assess specific control objectives related to the burden or duration of H5N1 outbreaks among poultry farms in the Dhaka division of Bangladesh. In particular, we explore the optimal implementation of ring culling, ring vaccination and active surveillance measures when presuming disease transmission predominately occurs from premises-to-premises, versus a setting requiring the inclusion of external factors. Additionally, we determine the sensitivity of the management actions under consideration to differing levels of capacity constraints and outbreaks with disparate transmission dynamics. While we find that reactive culling and vaccination policies should pay close attention to these factors to ensure intervention targeting is optimised, across multiple settings the top performing control action amongst those under consideration were targeted proactive surveillance schemes. Our findings may advise the type of control measure, plus its intensity, that could potentially be applied in the event of a developing outbreak of H5N1 amongst originally H5N1 virus-free commercially-reared poultry in the Dhaka division of Bangladesh.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Prior to the emergence of the A/goose/Guangdong/1/1996 (Gs/GD) H5N1 influenza A virus, the long‐held and well‐supported paradigm was that highly pathogenic avian influenza (HPAI) outbreaks were ...restricted to poultry, the result of cross‐species transmission of precursor viruses from wild aquatic birds that subsequently gained pathogenicity in domestic birds. Therefore, management agencies typically adopted a prevention, control, and eradication strategy that included strict biosecurity for domestic bird production, isolation of infected and exposed flocks, and prompt depopulation. In most cases, this strategy has proved sufficient for eradicating HPAI. Since 2002, this paradigm has been challenged with many detections of viral descendants of the Gs/GD lineage among wild birds, most of which have been associated with sporadic mortality events. Since the emergence and evolution of the genetically distinct clade 2.3.4.4 Gs/GD lineage HPAI viruses in approximately 2010, there have been further increases in the occurrence of HPAI in wild birds and geographic spread through migratory bird movement. A prominent example is the introduction of clade 2.3.4.4 Gs/GD HPAI viruses from East Asia to North America via migratory birds in autumn 2014 that ultimately led to the largest outbreak of HPAI in the history of the United States. Given the apparent maintenance of Gs/GD lineage HPAI viruses in a global avian reservoir; bidirectional virus exchange between wild and domestic birds facilitating the continued adaptation of Gs/GD HPAI viruses in wild bird hosts; the current frequency of HPAI outbreaks in wild birds globally, and particularly in Eurasia where Gs/GD HPAI viruses may now be enzootic; and ongoing dispersal of AI viruses from East Asia to North America via migratory birds, HPAI now represents an emerging disease threat to North American wildlife. This recent paradigm shift implies that management of HPAI in domestic birds alone may no longer be sufficient to eradicate HPAI viruses from a given country or region. Rather, agencies managing wild birds and their habitats may consider the development or adoption of mitigation strategies to minimize introductions to poultry, to reduce negative impacts on wild bird populations, and to diminish adverse effects to stakeholders using wildlife resources. The main objective of this review is, therefore, to provide information that will assist wildlife managers in developing mitigation strategies or approaches for dealing with outbreaks of Gs/GD HPAI in wild birds in the form of preparedness, surveillance, research, communications, and targeted management actions. Resultant outbreak response plans and actions may represent meaningful steps of wildlife managers toward the use of collaborative and multi‐jurisdictional One Health approaches when it comes to the detection, investigation, and mitigation of emerging viruses at the human‐domestic animal‐wildlife interface.
Highly pathogenic avian influenza has become sufficiently common and geographically widespread in wild birds such that it now represents an emergent disease threat to North American wildlife. This review aims to provide information that will assist wildlife managers in developing mitigation strategies or approaches for dealing with future outbreaks in wild birds in the form of preparedness, surveillance, research, communications, and targeted management actions.
For pathogens known to transmit across host species, strategic investment in disease control requires knowledge about where and when spillover transmission is likely. One approach to estimating ...spillover is to directly correlate observed spillover events with covariates. An alternative is to mechanistically combine information on host density, distribution and pathogen prevalence to predict where and when spillover events are expected to occur. We use several case studies at the wildlife-livestock disease interface to highlight the challenges, and potential solutions, to estimating spatio-temporal variation in spillover risk. Datasets on multiple host species often do not align in space, time or resolution, and may have no estimates of observation error. Linking these datasets requires they be related to a common spatial and temporal resolution and appropriately propagating errors in predictions can be difficult. Hierarchical models are one potential solution, but for fine-resolution predictions at broad spatial scales, many models become computationally challenging. Despite these limitations, the confrontation of mechanistic predictions with observed events is an important avenue for developing a better understanding of pathogen spillover. Systems where data have been collected at all levels in the spillover process are rare, or non-existent, and require investment and sustained effort across disciplines. This article is part of the theme issue 'Dynamic and integrative approaches to understanding pathogen spillover'.
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