Spatial and Temporal Association of Outbreaks of H5N1 Influenza Virus Infection in Wild Birds with the 0°C Isotherm

Wild bird movements and aggregations following spells of cold weather may have resulted in the spread of highly pathogenic avian influenza virus (HPAIV) H5N1 in Europe during the winter of 2005–2006. Waterbirds are constrained in winter to areas where bodies of water remain unfrozen in order to feed. On the one hand, waterbirds may choose to winter as close as possible to their breeding grounds in order to conserve energy for subsequent reproduction, and may be displaced by cold fronts. On the other hand, waterbirds may choose to winter in regions where adverse weather conditions are rare, and may be slowed by cold fronts upon their journey back to the breeding grounds, which typically starts before the end of winter. Waterbirds will thus tend to aggregate along cold fronts close to the 0°C isotherm during winter, creating conditions that favour HPAIV H5N1 transmission and spread. We determined that the occurrence of outbreaks of HPAIV H5N1 infection in waterbirds in Europe during the winter of 2005–2006 was associated with temperatures close to 0°C. The analysis suggests a significant spatial and temporal association of outbreaks caused by HPAIV H5N1 in wild birds with maximum surface air temperatures of 0°C–2°C on the day of the outbreaks and the two preceding days. At locations where waterbird census data have been collected since 1990, maximum mallard counts occurred when average and maximum surface air temperatures were 0°C and 3°C, respectively. Overall, the abundance of mallards (Anas platyrhynchos) and common pochards (Aythya ferina) was highest when surface air temperatures were lower than the mean temperatures of the region investigated. The analysis implies that waterbird movements associated with cold weather, and congregation of waterbirds along the 0°C isotherm likely contributed to the spread and geographical distribution of outbreaks of HPAIV H5N1 infection in wild birds in Europe during the winter of 2005–2006.

[1]  M Beer,et al.  Epidemiological and ornithological aspects of outbreaks of highly pathogenic avian influenza virus H5N1 of Asian lineage in wild birds in Germany, 2006 and 2007. , 2009, Transboundary and emerging diseases.

[2]  Stephan Hülsmann,et al.  The impact of climate change on lakes in the Netherlands: a review , 2005, Aquatic Ecology.

[3]  Gunnar Gunnarsson,et al.  Effects of influenza A virus infection on migrating mallard ducks , 2009, Proceedings of the Royal Society B: Biological Sciences.

[4]  C. Lebarbenchon,et al.  Recent expansion of highly pathogenic avian influenza H5N1: a critical review , 2007 .

[5]  T. Alerstam Spring predictability and leap-frog migration , 1980 .

[6]  J. Guégan,et al.  Water-borne transmission drives avian influenza dynamics in wild birds: the case of the 2005-2006 epidemics in the Camargue area. , 2009, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[7]  M. Gilbert,et al.  Anatidae Migration in the Western Palearctic and Spread of Highly Pathogenic Avian Influenza H5N1 Virus , 2006, Emerging infectious diseases.

[8]  I. Brown,et al.  Surveillance, prevention and disease management of avian influenza in the European Union , 2006 .

[9]  D. Stallknecht,et al.  Tenacity of avian influenza viruses. , 2009, Revue scientifique et technique.

[10]  John M Drake,et al.  Environmental transmission of low pathogenicity avian influenza viruses and its implications for pathogen invasion , 2009, Proceedings of the National Academy of Sciences.

[11]  D. Stallknecht,et al.  Experimental Infection of Swans and Geese with Highly Pathogenic Avian Influenza Virus (H5N1) of Asian Lineage , 2008, Emerging infectious diseases.

[12]  Steve Valeika,et al.  Avian influenza virus in water: infectivity is dependent on pH, salinity and temperature. , 2009, Veterinary microbiology.

[13]  V. Jestin,et al.  THE EPIDEMIOLOGY OF THE HIGHLY PATHOGENIC H5N1 AVIAN INFLUENZA IN MUTE SWAN (CYGNUS OLOR) AND OTHER ANATIDAE IN THE DOMBES REGION (FRANCE), 2006 , 2008, Journal of wildlife diseases.

[14]  Nikolaos I. Stilianakis,et al.  Ecologic Immunology of Avian Influenza (H5N1) in Migratory Birds , 2007, Emerging infectious diseases.

[15]  G. Vaitkus Spatial Dynamics of Wintering Seabird Populations in the Baltic Proper: A Review of Factors and Adaptations , 1999 .

[16]  D. Scott,et al.  Atlas of Anatidae Populations in Africa and Western Eurasia , 1996 .

[17]  T. Kuiken,et al.  Wild Ducks as Long-Distance Vectors of Highly Pathogenic Avian Influenza Virus (H5N1) , 2008, Emerging infectious diseases.

[18]  Martin Beer,et al.  Pathogenicity of Highly Pathogenic Avian Influenza Virus (H5N1) in Adult Mute Swans , 2008, Emerging Infectious Diseases.

[19]  L. Nilsson Habitat Selection, Food Choice, and Feeding Habits of Diving Ducks in Coastal Waters of South Sweden during the Non-Breeding Season , 1972 .

[20]  Pejman Rohani,et al.  The Role of Environmental Transmission in Recurrent Avian Influenza Epidemics , 2009, PLoS Comput. Biol..

[21]  D. Shoham,et al.  Evidence of Influenza A Virus RNA in Siberian Lake Ice , 2006, Journal of Virology.

[22]  A. Osterhaus,et al.  Practical Considerations for High-Throughput Influenza A Virus Surveillance Studies of Wild Birds by Use of Molecular Diagnostic Tests , 2009, Journal of Clinical Microbiology.

[23]  Trevor D. Davies,et al.  Atmospheric circulation and surface temperature in Europe from the 18th century to 1995 , 2001 .

[24]  Matthieu Guillemain,et al.  Spread of Avian Influenza Viruses by Common Teal (Anas crecca) in Europe , 2009, PloS one.

[25]  M. Beer,et al.  Highly pathogenic avian influenza virus (H5N1) in experimentally infected adult mute swans. , 2008, Emerging infectious diseases.

[26]  J. V. van Gils,et al.  Hampered Foraging and Migratory Performance in Swans Infected with Low-Pathogenic Avian Influenza A Virus , 2007, PloS one.

[27]  P. Daszak,et al.  Predicting the global spread of H5N1 avian influenza , 2006, Proceedings of the National Academy of Sciences.

[28]  D. Stallknecht,et al.  Persistence of H5 and H7 Avian Influenza Viruses in Water , 2007, Avian diseases.

[29]  W. Fiedler,et al.  Urgent preliminary assessment of ornithological data relevant to the spread of Avian Influenza in Europe , 2006 .

[30]  M. Kanamitsu,et al.  NCEP–DOE AMIP-II Reanalysis (R-2) , 2002 .

[31]  F. Korner‐Nievergelt,et al.  Within-winter movements: a common phenomenon in the Common Pochard Aythya ferina , 2009, Journal of Ornithology.