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Persistence of HPAI Viruses in Natural Ecosystems | CDC EID
EID Journal Home > Volume 16, Number 7–July 2010
Volume 16, Number 7–July 2010 Perspective Persistence of Highly Pathogenic Avian Influenza Viruses in Natural Ecosystems Camille Lebarbenchon,1 Chris J. Feare, François Renaud, Frédéric Thomas, and Michel Gauthier-Clerc Author affiliations: Centre de Recherche de la Tour du Valat, Arles, France (C. Lebarbenchon, M. Gauthier-Clerc); Institut de Recherche pour le Développement, Montpellier, France (C. Lebarbenchon, F. Renaud, F. Thomas); WildWings Bird Management, Haslemere, United Kingdom (C.J. Feare); and Université de Montréal, Montréal, Québec, Canada (F. Thomas)
Suggested citation for this article
Abstract Understanding of ecologic factors favoring emergence and maintenance of highly pathogenic avian influenza (HPAI) viruses is limited. Although low pathogenic avian influenza viruses persist and evolve in wild populations, HPAI viruses evolve in domestic birds and cause economically serious epizootics that only occasionally infect wild populations. We propose that evolutionary ecology considerations can explain this apparent paradox. Host structure and transmission possibilities differ considerably between wild and domestic birds and are likely to be major determinants of virulence. Because viral fitness is highly dependent on host survival and dispersal in nature, virulent forms are unlikely to persist in wild populations if they kill hosts quickly or affect predation risk or migratory performance. Interhost transmission in water has evolved in low pathogenic influenza viruses in wild waterfowl populations. However, oropharyngeal shedding and transmission by aerosols appear more efficient for HPAI viruses among domestic birds. Wild birds, especially waterbirds of the orders Anseriformes (ducks, geese, and swans) and Charadriiformes (gulls, terns, and waders), are natural hosts for influenza A (avian influenza) viruses. Avian influenza viruses are classified on the basis of genetic, antigenic, and structural characteristics of hemagglutinin and neuraminidase proteins. These proteins are involved in binding of virus to host cells and release of new virions from these cells, respectively. Sixteen hemagglutinins (H1–H16) and 9 neuraminidases (N1–N9) have been described. For avian influenza viruses of subtypes H5 and H7, there are 2 types of virulence: low pathogenic avian influenza (LPAI) virus generally produces benign intestinal tract or respiratory infections; highly pathogenic avian influenza (HPAI) virus generally produces multiorgan systemic infections.
LPAI viruses naturally infect wild waterbirds according to host species, age, immune status, feeding behavior, premigration aggregation, and aquatic survival of the virus. Long-term studies in Europe and North America also identified seasonal variation in prevalences of infection of LPAI virus and circulating subtypes. HPAI viruses primarily infect poultry in which viruses of subtypes H5 and H7, presumably from wild birds or contact with their derivatives, sporadically switch to highly virulent strains.
At the end of the 19th century, a disease that caused high mortality rates and spread rapidly was described in domestic birds in Italy. This fowl plague spread through Europe in the early 20th century, most likely through trading of domestic birds. In 1955, the pathogen responsible for the disease was classified as an influenza A virus, and its relationship to human influenza viruses was recognized. Domestic birds have been affected by recurrent outbreaks of HPAI viruses, generally limited to localized geographic areas but responsible for high mortality rates and substantial economic losses. In contrast, wild birds have rarely been involved in HPAI virus infections. Before 1996, only 1 HPAI virus outbreak was documented in the wild, resulting in the death of ≈;1,300 common terns (Sterna hirundo) in South Africa (1). Since then, emergence and spread of the HPAI virus lineage from Asia (H5N1), first discovered in domestic geese in southern People's Republic of China in 1996, has been responsible for the death of thousands of wild birds, occasionally through mass mortality events (e.g., Lake Quinghai, People's Republic of China, in May–June 2005). Extensive surveillance of apparently healthy wild populations has rarely detected HPAI virus (H5N1), even in areas where the virus is endemic in domestic birds (2). In addition, some reports of asymptomatic infection by HPAI virus (H5N1) in apparently healthy free-living wild birds lack important substantiating information and such cases of infection have yet to be convincingly demonstrated (3).
Although recent studies have focused on environmental factors that contributed to the persistence and spread of HPAI virus (H5N1) in southeastern Asia, Europe, and Africa (4–6), general knowledge concerning mechanisms of emergence and persistence of HPAI viruses is limited. We propose that because the ecologic landscape in which avian influenza viruses evolve differs markedly between natural (i.e., wild birds) and artificial (e.g., intensive poultry farming, free-grazing ducks, and live bird markets) conditions, selective pressures differ. These phenomena are likely to explain virulence heterogeneity among avian influenza viruses and why HPAI viruses do not naturally emerge or persist in natural ecosystems.
Suggested Citation for this Article Lebarbenchon C, Feare CJ, Renaud F, Thomas F, Gauthier-Clerc M. Persistence of highly pathogenic avian influenza viruses in natural ecosystems. Emerg Infect Dis [serial on the Internet]. 2010 Jul [date cited]. http://www.cdc.gov/EID/content/16/7/1057.htm
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