Ganseerpel
Advisory Board, Senior Moderator
Predicting the global spread of H5N1 avian influenza
A. Marm Kilpatrick*
?, Aleksei A. Chmura*, David W. Gibbons?, Robert C. Fleischer?, Peter P. Marra?, and Peter Daszak*
*Consortium for Conservation Medicine, New York, NY 10001;
?Royal Society for the Protection of Birds, Sandy, Bedfordshire SG19 2DL, United Kingdom;
and ?National Museum of Natural History, and ?Smithsonian Migratory Bird Center, National Zoological Park, Smithsonian Institution,
Washington, DC 20008
Communicated by Hans R. Herren, Millennium Institute, Arlington, VA, October 19, 2006 (received for review April 26, 2006)
and ?National Museum of Natural History, and ?Smithsonian Migratory Bird Center, National Zoological Park, Smithsonian Institution,
Washington, DC 20008
Communicated by Hans R. Herren, Millennium Institute, Arlington, VA, October 19, 2006 (received for review April 26, 2006)
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.
emerging
introduced species model trade zoonotic disease
H
ighly pathogenic H5N1 avian influenza emerged in Hong
Kong in 1996?1997 (1) and by early October 2006 had subsequently caused outbreaks in poultry or wild birds in 53 countries and 256 human cases, including 151 deaths (www. who.int/csr/disease/avianinfluenza/en/). Hundreds of millions of chickens, ducks, turkeys, and geese have died or have been culled to prevent the spread of the virus. Coupled with export bans on affected countries the disease has had an economic
impact of $10 billion (2). Despite efforts to eradicate H5N1 in southeast Asia it has spread to central Asia, Europe, and Africa. Migratory birds, the transport of poultry and poultry products, and the trade in wild birds all have been hypothesized as pathways of introduction. However, their role in individual H5N1 introduction events and in future spread is not well understood and has been debated extensively (3?9).
Determining the pathways by which H5N1 is spread has critical implications for predicting and preventing the future spread of this virus (10). If the risk of H5N1 spread to a country is highest through the movement of migratory birds, then surveillance at migratory stopovers such as Alaska will likely yield the first evidence of introduction, a strategy that matches current U.S. Department of Interior and Agriculture policy (11). In this scenario, the timing of the highest risk of introduction would coincide with periods of peak bird movement and pathways of migration (12). Prevention of future outbreaks would be facilitated by eliminating contact between
farmed poultry and migrating birds, as was attempted by several European countries in 2005?2006. Alternatively, if the risk of H5N1 introduction is higher via the trade in poultry and poultry products, then monitoring poultry imports and eliminating imports from high-risk countries should be a higher priority for reducing the probability of H5N1 introduction. Finally, H5N1 has been found in wild birds imported into Europe and other countries as part of commercial trade in wild birds (4), making this another potentially important pathway unless all imported birds are quarantined, tested for avian influenza, and culled where necessary. We determined the most likely pathways for the introduction of H5N1 into each of 52 countries by using global data on country-to-country imports and exports of live poultry, trade in wild birds, and the migratory and cold weather movements of wild ducks, geese, and swans, which are considered to be the main reservoirs for highly pathogenic H5 and H7 subtypes of avian influenza, including H5N1 (6, 13, 14). For each of these three pathways we estimated risk as the number of H5N1- infectious bird days for an introduction by multiplying the number of birds entering or passing through a country by an estimate of the prevalence of H5N1 and by an estimate of the number of days that each bird would shed virus. We then used data on the trade in poultry and wild birds and the migration patterns of wild birds to predict the future risk of spread of H5N1 to new countries. Because of the variability in trade restrictions and the delays of several days to over a month between the start of an H5N1 outbreak and the implementation of trade bans, we predicted future spread under two scenarios. First, we estimated the number of infectious bird days caused by the poultry trade assuming no restrictions on the poultry trade were imposed on H5N1-infected countries. Second, we predicted the risk of
introduction assuming that no country would import poultry from another country that had reported H5N1 in poultry (unless that country was considered H5N1-free), but that countries reporting H5N1 in wild birds could export poultry freely, and that these exports might contain infected birds.
Kong in 1996?1997 (1) and by early October 2006 had subsequently caused outbreaks in poultry or wild birds in 53 countries and 256 human cases, including 151 deaths (www. who.int/csr/disease/avianinfluenza/en/). Hundreds of millions of chickens, ducks, turkeys, and geese have died or have been culled to prevent the spread of the virus. Coupled with export bans on affected countries the disease has had an economic
impact of $10 billion (2). Despite efforts to eradicate H5N1 in southeast Asia it has spread to central Asia, Europe, and Africa. Migratory birds, the transport of poultry and poultry products, and the trade in wild birds all have been hypothesized as pathways of introduction. However, their role in individual H5N1 introduction events and in future spread is not well understood and has been debated extensively (3?9).
Determining the pathways by which H5N1 is spread has critical implications for predicting and preventing the future spread of this virus (10). If the risk of H5N1 spread to a country is highest through the movement of migratory birds, then surveillance at migratory stopovers such as Alaska will likely yield the first evidence of introduction, a strategy that matches current U.S. Department of Interior and Agriculture policy (11). In this scenario, the timing of the highest risk of introduction would coincide with periods of peak bird movement and pathways of migration (12). Prevention of future outbreaks would be facilitated by eliminating contact between
farmed poultry and migrating birds, as was attempted by several European countries in 2005?2006. Alternatively, if the risk of H5N1 introduction is higher via the trade in poultry and poultry products, then monitoring poultry imports and eliminating imports from high-risk countries should be a higher priority for reducing the probability of H5N1 introduction. Finally, H5N1 has been found in wild birds imported into Europe and other countries as part of commercial trade in wild birds (4), making this another potentially important pathway unless all imported birds are quarantined, tested for avian influenza, and culled where necessary. We determined the most likely pathways for the introduction of H5N1 into each of 52 countries by using global data on country-to-country imports and exports of live poultry, trade in wild birds, and the migratory and cold weather movements of wild ducks, geese, and swans, which are considered to be the main reservoirs for highly pathogenic H5 and H7 subtypes of avian influenza, including H5N1 (6, 13, 14). For each of these three pathways we estimated risk as the number of H5N1- infectious bird days for an introduction by multiplying the number of birds entering or passing through a country by an estimate of the prevalence of H5N1 and by an estimate of the number of days that each bird would shed virus. We then used data on the trade in poultry and wild birds and the migration patterns of wild birds to predict the future risk of spread of H5N1 to new countries. Because of the variability in trade restrictions and the delays of several days to over a month between the start of an H5N1 outbreak and the implementation of trade bans, we predicted future spread under two scenarios. First, we estimated the number of infectious bird days caused by the poultry trade assuming no restrictions on the poultry trade were imposed on H5N1-infected countries. Second, we predicted the risk of
introduction assuming that no country would import poultry from another country that had reported H5N1 in poultry (unless that country was considered H5N1-free), but that countries reporting H5N1 in wild birds could export poultry freely, and that these exports might contain infected birds.
www.pnas.orgcgidoi10.1073pnas.0609227103
http://www.pnas.org/cgi/content/abstract/103/51/19368?maxtoshow=&HITS=10&hits=10&RESULTFORMAT=1&andorexacttitle=and&andorexacttitleabs=and&andorexactfulltext=and&searchid=1&FIRSTINDEX=0&sortspec=relevance&volume=103&resourcetype=HWCIT
http://www.pnas.org/cgi/content/abstract/103/51/19368?maxtoshow=&HITS=10&hits=10&RESULTFORMAT=1&andorexacttitle=and&andorexacttitleabs=and&andorexactfulltext=and&searchid=1&FIRSTINDEX=0&sortspec=relevance&volume=103&resourcetype=HWCIT
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