Ecology of avian influenza viruses in a changing world

Abstract

Influenza A virus infections result in approximately 500,000 human deaths per year and many more sublethal infections. Wild birds are recognized as the ancestral host of influenza A viruses, and avian viruses have contributed genetic material to most human viruses, including subtypes H5N1 and H1N1. Thus, influenza virus transmission in wild and domestic animals and humans is intimately connected. Here we review how anthropogenic change, including human population growth, land use, climate change, globalization of trade, agricultural intensification, and changes in vaccine technology may alter the evolution and transmission of influenza viruses. Evidence suggests that viral transmission in domestic poultry, spillover to other domestic animals, wild birds and humans, and the potential for subsequent pandemic spread, are all increasing. We highlight four areas in need of research: drivers of viral subtype dynamics; ecological and evolutionary determinants of transmissibility and virulence in birds and humans; the impact of changing land use and climate on hosts, viruses, and transmission; and the impact of influenza viruses on wild bird hosts, including their ability to migrate while shedding virus.

Figure 1. Presence and prevalence of influenza virus subtypes in shorebirds (charadriiforms) and ducks (anseriforms) from a 25 year study in North America

A) Presence and absence of viral subtypes in the two groups of birds. B) Fraction of birds shedding virus of each of 44 influenza virus subtypes for shorebirds and ducks. Shorebirds were sampled during spring migration (May) in Delaware Bay, New Jersey, USA, whereas ducks were sampled in the late summer and fall (July –September) in Alberta, Canada.

Figure 2. Intercontinental shorebird and Anseriform connections and H5N1 avian influenza distribution

Global map indicates countries (in red) that have had outbreaks of H5N1 avian influenza in poultry or wild birds between Jan 1, 2003 and August 15, 2009. Overlaid, in blue are links between breeding and wintering habitats of shorebirds (solid lines; Order charadriiforms, including gulls, plovers, sandpipers, etc.), and ducks, geese, and swans (dashed lines; Order anseriforms). Thickness of line indicates relative number of birds migrating between continents (e.g. thousands of Anseriform birds migrate from Siberia to the Pacific coast of California whereas millions of anseriforms migrate between Asia and Europe). Note also the distance each group migrates as indicated in the figure (shorebirds reach southern S. America, S. Africa, and Australia, none of which are reached by anseriforms from northern N. America, Europe, or Asia). Arrows do not necessarily indicate actually flyway used by birds, but merely indicate connections between regions.

Figure 3. Temporal patterns of H5N1 outbreaks by continent

The number of countries in each of three continents reporting new H5N1 avian influenza outbreaks for each six month period from late 2003 through early 2009.

Figure 4. Production of four different stocks, from 1961 to 2005 based on FAO data

a) Global production of poultry (ducks and chickens), cattle, and swine. b) Production of ducks and chickens by geographic region over the same period.