Migration in the Western Palearctic and Spread of Avian Influenza H5N1

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Migration in the Western Palearctic and Spread of Avian Influenza H5N1

Abstract and Introduction

Abstract


During the second half of 2005, highly pathogenic avian influenza (HPAI) H5N1 virus spread rapidly from central Asia to eastern Europe. The relative roles of wild migratory birds and the poultry trade are still unclear, given that little is yet known about the range of virus hosts, precise movements of migratory birds, or routes of illegal poultry trade. We document and discuss the spread of the HPAI H5N1 virus in relation to species-specific flyways of Anatidae species (ducks, geese, and swans) and climate. We conclude that the spread of HPAI H5N1 virus from Russia and Kazakhstan to the Black Sea basin is consistent in space and time with the hypothesis that birds in the Anatidae family have seeded the virus along their autumn migration routes.

Introduction


The spread of highly pathogenic avian influenza (HPAI) H5N1 virus during 2003-2004 in eastern and southeastern Asia, and, in 2005-2006 westward across Asia into Europe, the Middle East, and Africa is not typical of other HPAI epizootics. Until recent events, HPAI outbreaks or epizootics were assumed to first require transmission of a low pathogenic avian influenza (LPAI) virus from wild birds to domestic poultry. Preventive measures thus focused on surveillance and control in poultry and on stopping transmission to noninfected premises. Usually this strategy successfully extinguished an outbreak, often within the year. The spread of the disease back to wild birds from domestic fowl was considered relatively rare. The HPAI H5N1 virus is unusual in that virus infections in wild bird populations may cause a high proportion of deaths. A list of species that have been infected with HPAI H5N1 virus can be found in Appendix Table. The virus also is persisting in Asia longer than most previous HPAI epizootics, which suggests a local reservoir.

Epidemiologic studies during 2004-05 mainly focused on HPAI H5N1 virus persistence in relation to the agro-ecology of poultry and duck production systems, and little attention was paid to the role of wild birds in local viral persistence or long-distance spread during that period. Because of 3 major events during mid- to late 2005, wild birds are now suspected of spreading the HPAI H5N1 virus over long distances through migration. First, in May 2005, a major HPAI HN51 virus outbreak was discovered in wild birds in Lake Qinghai (western People's Republic of China), an important breeding place for migratory bird species in eastern Asia. Within a few weeks, several hundred birds, mainly bar-headed geese, had died of the disease. Eventually, other bird species also became affected, and several virus introductions may have occurred. Soon after the Lake Qinghai episode, HPAI H5N1 virus was detected in wild birds in Mongolia, to the north of Lake Qinghai along the central migration route, and in an area where domestic poultry were scarce. Second, in October 2005, HPAI H5N1 virus spread westward across Eurasia; outbreaks were recorded in Turkey, Romania, and Ukraine, usually in or near known wintering sites for migratory birds. This long-distance spread took place through areas with no record of any virus presence. Third, in spring 2006, the virus infected large numbers of mute swans and other wild bird species across western Europe, also in areas where no outbreaks had previously been detected in domestic poultry, despite continual and intensive surveillance. These incursions occurred after unusual waterfowl movements that were associated with a spell of cold weather in the Black Sea area where HPAI H5N1 virus is believed to have been endemic since autumn 2005.

Arguments may also be raised against the hypothesis that HPAI H5N1 virus is transmitted by wild birds. Invariably, wild birds found to be infected with the virus were either dead or moribund and may not have been able to spread the virus over long distances. Furthermore, in several cases, no straightforward match was found between the appearance of the virus and the presence of the wild birds suspected of spreading it. For example, HPAI H5N1 virus outbreaks that took place in Russia and Kazakhstan during summer 2005 were distributed along important trade routes that link western People's Republic of China to Russia, rather than any direct migration pathway.

We document and discuss the possible role of migratory birds in the spread of HPAI H5N1 virus during the second half of 2005, on the basis of information and data concerning the role of waterfowl in the ecology of avian influenza viruses; the pattern of Anatidae bird migrations across the western Palearctic, and contemporary, satellite-derived temperature data.

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