Predicting the global spread of H5N1 avian influenza

Abstract

The spread of highly pathogenic H5N1 avian influenza into Asia, Europe, and Africa has resulted in enormous impacts on the poultry industry and presents an important threat to human health. The pathways by which the virus has and will spread between countries have been debated extensively, but have yet to be analyzed comprehensively and quantitatively. We integrated data on phylogenetic relationships of virus isolates, migratory bird movements, and trade in poultry and wild birds to determine the pathway for 52 individual introduction events into countries and predict future spread. We show that 9 of 21 of H5N1 introductions to countries in Asia were most likely through poultry, and 3 of 21 were most likely through migrating birds. In contrast, spread to most (20/23) countries in Europe was most likely through migratory birds. Spread in Africa was likely partly by poultry (2/8 introductions) and partly by migrating birds (3/8). Our analyses predict that H5N1 is more likely to be introduced into the Western Hemisphere through infected poultry and into the mainland United States by subsequent movement of migrating birds from neighboring countries, rather than from eastern Siberia. These results highlight the potential synergism between trade and wild animal movement in the emergence and pandemic spread of pathogens and demonstrate the value of predictive models for disease control.

Fig. 1.

Spread of H5N1 avian influenza and phylogenetic relationship of viral isolates. (a) Spread of H5N1 in Asia, Europe, and Africa. Pie charts show the total number of infectious bird days (number of infected birds × days shedding virus) and fraction from each pathway for birds moving between previous H5N1 outbreak countries and the focal country. Arrows give the month of the outbreak and hypothesized direction of spread for 2003–2005 introductions. The introductions of H5N1 into some countries (white pie charts) were inconsistent with reported wild bird and poultry trade (no imports from an H5N1-infected country were reported) and the direction of migratory birds in the months of the outbreaks (outbreaks occurred outside periods of bird movement; see Methods). Introductions into Belgium and Taiwan through the trade in wild birds were intercepted and did not lead to outbreaks in poultry or wild birds. (b) Maximum-likelihood phylogram showing the genetic relationship between samples of strains of H5N1 avian influenza isolated between 1997 and 2006 (with England 1991 as an outgroup) for the hemagglutinin gene. Nodes with thick, gray lines have bootstrap support >70%, based on 100 replicates.

Fig. 2.

Predicted risk of H5N1 avian influenza introduction from countries that have had H5N1 outbreaks (in blue). (a–c) Risk was estimated as the number of infectious bird days (number of infected birds × days shedding virus) caused by trade (presented as yearly totals/12 months) in: live poultry with no trade restrictions (a), live poultry with no exports from countries reporting H5N1 in poultry (France, Denmark, Sweden, and Germany are considered H5N1-free) (b), and captive wild birds with no exports from countries reporting H5N1 in poultry (c) as in b. (d) Estimated number of ducks, geese, and swans migrating between mainland continents, number of infectious bird days, and number of species (in parentheses). Numbers given between Asia and North America include only those that breed on mainland Asia and winter in North America south of Alaska; an additional 200,000–400,000 ducks breed in Siberia and molt or winter in or off the coast of Alaska. In addition, ≈20,000 geese migrate between Ireland and North America.