Role for migratory wild birds in the global spread of avian influenza H5N8
Migration of influenza in wild birds
Virus surveillance in wild birds could offer an early warning system that, combined with adequate farm hygiene, would lead to effective influenza control in poultry units. The Global Consortium for H5N8 and Related Influenza Viruses found that the H5 segment common to the highly pathogenic avian influenza viruses readily reassorts with other influenza viruses (see the Perspective by Russell). H5 is thus a continual source of new pathogenic variants. These data also show that the H5N8 virus that recently caused serious outbreaks in European and North American poultry farms came from migrant ducks, swans, and geese that meet at their Arctic breeding grounds. Because the virus is so infectious, culling wild birds is not an effective control measure.
Abstract
Avian influenza viruses affect both poultry production and public health. A subtype H5N8 (clade 2.3.4.4) virus, following an outbreak in poultry in South Korea in January 2014, rapidly spread worldwide in 2014–2015. Our analysis of H5N8 viral sequences, epidemiological investigations, waterfowl migration, and poultry trade showed that long-distance migratory birds can play a major role in the global spread of avian influenza viruses. Further, we found that the hemagglutinin of clade 2.3.4.4 virus was remarkably promiscuous, creating reassortants with multiple neuraminidase subtypes. Improving our understanding of the circumpolar circulation of avian influenza viruses in migratory waterfowl will help to provide early warning of threats from avian influenza to poultry, and potentially human, health.
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Supplementary Material
Summary
Materials and Methods
Figs. S1 to S6
Tables S1 to S10
Movie S1
Resources
References and Notes
1
Lee Y.-J., Kang H. M., Lee E. K., Song B. M., Jeong J., Kwon Y. K., Kim H. R., Lee K. J., Hong M. S., Jang I., Choi K. S., Kim J. Y., Lee H. J., Kang M. S., Jeong O. M., Baek J. H., Joo Y. S., Park Y. H., and Lee H. S., Novel reassortant influenza A(H5N8) viruses, South Korea, 2014. Emerg. Infect. Dis. 20, 1087–1089 (2014).
2
Lee D.-H., Torchetti M. K., Winker K., Ip H. S., Song C. S., and Swayne D. E., Intercontinental Spread of Asian-Origin H5N8 to North America through Beringia by Migratory Birds. J. Virol. 89, 6521–6524 (2015).
3
Verhagen J. H., Herfst S., and Fouchier R. A. M., How a virus travels the world. Science 347, 616–617 (2015).
4
Richard M., de Graaf M., and Herfst S., Avian influenza A viruses: From zoonosis to pandemic. Future Virol. 9, 513–524 (2014).
5
Xu X., Subbarao N. J., Cox N. J., and Guo Y., Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: Similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virology 261, 15–19 (1999).
6
Olsen B., Munster V. J., Wallensten A., Waldenström J., Osterhaus A. D., and Fouchier R. A., Global patterns of influenza a virus in wild birds. Science 312, 384–388 (2006).
7
World Health Organization (WHO), Evolution of the influenza A(H5) haemagglutinin: WHO/OIE/FAO H5 Working Group reports a new clade designated 2.3.4.4 (2015); www.who.int/influenza/gisrs_laboratory/h5_nomenclature_clade2344/en/.
8
de Vries E., Guo H., Dai M., Rottier P. J., van Kuppeveld F. J., and de Haan C. A., Rapid emergence of highly pathogenic avian influenza subtypes from a subtype H5N1 hemagglutinin variant. Emerg. Infect. Dis. 21, 842–846 (2015).
9
Hall J. S., Dusek R. J., and Spackman E., Rapidly expanding range of highly pathogenic avian influenza viruses. Emerg. Infect. Dis. 21, 1251–1252 (2015).
10
Hill S. C., Lee Y. J., Song B. M., Kang H. M., Lee E. K., Hanna A., Gilbert M., Brown I. H., and Pybus O. G., Wild waterfowl migration and domestic duck density shape the epidemiology of highly pathogenic H5N8 influenza in the Republic of Korea. Infect. Genet. Evol. 34, 267–277 (2015).
11
Materials and methods are available as supplementary materials on Science Online.
12
Food and Agriculture Organization of the United Nations (FAO), FAOSTAT; http://faostat3.fao.org.
13
Drummond A. J., Suchard M. A., Xie D., and Rambaut A., Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).
14
Lemey P., Rambaut A., Drummond A. J., and Suchard M. A., Bayesian phylogeography finds its roots. PLOS Comput. Biol. 5, e1000520 (2009).
15
Lemey P., Rambaut A., Welch J. J., and Suchard M. A., Phylogeography takes a relaxed random walk in continuous space and time. Mol. Biol. Evol. 27, 1877–1885 (2010).
16
Gill M. S., Lemey P., Faria N. R., Rambaut A., Shapiro B., and Suchard M. A., Improving Bayesian population dynamics inference: A coalescent-based model for multiple loci. Mol. Biol. Evol. 30, 713–724 (2013).
17
BEAST Tutorials, Increasing ESSs (2014); http://beast.bio.ed.ac.uk/Increasing-ESSs.
18
World Organisation for Animal Health (OiE), Update on highly pathogenic avian influenza in animals (type H5 and H7); http://www.oie.int/en/animal-health-in-the-world/update-on-avian-influenza/.
19
Conraths F. J., Sauter-Louis C., Globig A., Dietze K., Pannwitz G., Albrecht K., Höreth-Böntgen D., Beer M., Staubach C., and Homeier-Bachmann T., Highly pathogenic avian influenza H5N8 in Germany: Outbreak investigations. Transbound. Emerg. Dis. 63, 10–13 (2016).
20
Harder T., Maurer-Stroh S., Pohlmann A., Starick E., Höreth-Böntgen D., Albrecht K., Pannwitz G., Teifke J., Gunalan V., Lee R. T., Sauter-Louis C., Homeier T., Staubach C., Wolf C., Strebelow G., Höper D., Grund C., Conraths F. J., Mettenleiter T. C., and Beer M., Influenza A(H5N8) virus similar to strain in Korea causing highly pathogenic avian influenza in Germany. Emerg. Infect. Dis. 21, 860–863 (2015).
21
Standing Committee on Plants, Animals, Food and Feed of the European Union (SCoPAFF). Highly pathogenic avian influenza A subtype H5N8 in poultry in Germany. EFSA Journal 12, 3941 (2014).
22
Standing Committee on Plants, Animals, Food and Feed of the European Union (SCoPAFF), Update on highly pathogenic avian influenza of subtype H5N8 in poultry and other captive birds in Germany (2015); http://ec.europa.eu/food/animals/docs/reg-com_ahw_20150204_pres_hpai_h5n8_germany.pdf
23
Bouwstra R. J., Koch G., Heutink R., Harders F., van der Spek A., Elbers A. R., and Bossers A., Phylogenetic analysis of highly pathogenic avian influenza A(H5N8) virus outbreak strains provides evidence for four separate introductions and one between-poultry farm transmission in the Netherlands, November 2014. Euro Surveill. 20, 21174 (2015).
24
Hanna A., Banks J., Marston D. A., Ellis R. J., Brookes S. M., and Brown I. H., Genetic characterization of highly pathogenic avian influenza (H5N8) virus from domestic ducks, England, November 2014. Emerg. Infect. Dis. 21, 879–882 (2015).
25
Standing Committee on Plants, Animals, Food and Feed of the European Union (SCoPAFF), Update on HPAI H5N8 in the United Kingdom (2014); (http://ec.europa.eu/food/animals/docs/reg-com_ahw_20141205_pres_hpai_h5n8_gbr.pdf).
26
Standing Committee on Plants, Animals, Food and Feed of the European Union (SCoPAFF), Highly Pathogenic Avian Influenza (H5N8) in Italy H5N8 HPAI Outbreak in Italy (2015) (http://ec.europa.eu/food/animals/docs/reg-com_ahw_20150113_pres_avian_influenza_italy.pdf).
27
The Hortobagy National Park (2016); http://www.hnp.hu/uploads/documents/the-hortobagy-national-park–the-puszta.pdf.
28
Standing Committee on Plants, Animals, Food and Feed of the European Union (SCoPAFF), H5N8 HPAI in Hungary (2015) (http://ec.europa.eu/food/animals/docs/reg-com_ahw_20150416_pres_hpai_hungary.pdf).
29
World Organisation for Animal Health (OiE), OiE Immediate notification report: highly pathogenic avian influenza, Sweden (2015) (http://www.oie.int/wahis_2/temp/reports/en_imm_0000017393_20150320_191405.pdf).
30
United States Department of Agriculture-Animal and Plant Health Inspection Service (USDA-APHIS), Epidemiologic and Other Analyses of HPAI-Affected Poultry Flocks: September 9, 2015 Report (2015); https://www.aphis.usda.gov/animal_health/animal_dis_spec/poultry/downloads/Epidemiologic-Analysis-Sept-2015.pdf.
31
United States Department of Agriculture, Wild bird highly pathogenic avian influenza cases in the United States (USDA, 2015); https://www.aphis.usda.gov/wildlife_damage/downloads/WILD%20BIRD%20POSITIVE%20HIGHLY%20PATHOGENIC%20AVIAN%20INFLUENZA%20CASES%20IN%20THE%20UNITED%20STATES.pdf.
32
Zhao K., Gu M., Zhong L., Duan Z., Zhang Y., Zhu Y., Zhao G., Zhao M., Chen Z., Hu S., Liu W., Liu X., Peng D., and Liu X., Characterization of three H5N5 and one H5N8 highly pathogenic avian influenza viruses in China. Vet. Microbiol. 163, 351–357 (2013).
33
Jeong J., Kang H. M., Lee E. K., Song B. M., Kwon Y. K., Kim H. R., Choi K. S., Kim J. Y., Lee H. J., Moon O. K., Jeong W., Choi J., Baek J. H., Joo Y. S., Park Y. H., Lee H. S., and Lee Y. J., Highly pathogenic avian influenza virus (H5N8) in domestic poultry and its relationship with migratory birds in South Korea during 2014. Vet. Microbiol. 173, 249–257 (2014).
34
Kanehira K., Uchida Y., Takemae N., Hikono H., Tsunekuni R., and Saito T., Characterization of an H5N8 influenza A virus isolated from chickens during an outbreak of severe avian influenza in Japan in April 2014. Arch. Virol. 160, 1629–1643 (2015).
35
Marchenko V. Y., Susloparov I. M., Kolosova N. P., Goncharova N. I., Shipovalov A. V., Durymanov A. G., Ilyicheva T. N., Budatsirenova L. V., Ivanova V. K., Ignatyev G. A., Ershova S. N., Tulyahova V. S., Mikheev V. N., and Ryzhikov A. B., Influenza A(H5N8) virus isolation in Russia, 2014. Arch. Virol. 160, 2857–2860 (2015).
36
Bouwstra R., Heutink R., Bossers A., Harders F., Koch G., and Elbers A., Full-genome sequence of influenza A(H5N8) virus in poultry linked to sequences of strains from Asia, the Netherlands, 2014. Emerg. Infect. Dis. 21, 872–874 (2015).
37
Standing Committee on Plants, Animals, Food and Feed of the European Union (SCoPAFF), HPAI in Hungary (2015); http://ec.europa.eu/food/animals/docs/reg-com_ahw_20150416_pres_hpai_hungary.pdf.
38
Standing Committee on Plants, Animals, Food and Feed of the European Union (SCoPAFF), Highly Pathogenic Avian Influenza (H5N8) in Italy (2015); http://ec.europa.eu/food/animals/docs/reg-com_ahw_20150113_pres_avian_influenza_italy.pdf.
39
Pasick J., Berhane Y., Joseph T., Bowes V., Hisanaga T., Handel K., and Alexandersen S., Reassortant highly pathogenic influenza A H5N2 virus containing gene segments related to Eurasian H5N8 in British Columbia, Canada, 2014. Sci. Rep. 5, 9484 (2015).
40
International Union for Conservation of Nature (IUCN), The IUCN Red List of Threatened Species; http://www.iucnredlist.org.
41
BirdLife International, Sibirionetta formosa (Baikal Teal), The IUCN Red List of Threatened Species; http://www.iucnredlist.org/details/22680317/0.
42
BirdLife International, Anser fabalis (Bean goose), The IUCN Red List of Threatened Species; http://www.iucnredlist.org/details/22679875/0.
43
BirdLife International, Anas crecca (Common Teal, Eurasian Teal, Green-winged Teal, Teal), The IUCN Red List of Threatened Species; http://www.iucnredlist.org/details/22729717/0.
44
BirdLife International, Anser albifrons (Greater White-fronted Goose, White-fronted Goose), The IUCN Red List of Threatened Species; http://www.iucnredlist.org/details/22679881/0.
45
BirdLife International, Cygnus columbianus (Bewick’s Swan, Tundra Swan), The IUCN Red List of Threatened Species; http://www.iucnredlist.org/details/22679862/0.
46
D. A. Scott, P. M. Rose, Atlas of Anatidae Populations in Africa and Western Eurasia (1996).
47
Philip W Atkinson, Jacquie A Clark, Simon Delany, Cheikh Hamalla Diagana, Chris du Feu, Wolfgang Fiedler, Thord Fransson, Michel Gaulthier-Clerc, Mark Grantham, Marion Gschweng, Ward Hagemeijer, Toon Helmink, Alan Johnson, Sergey Khomenko, Georgios Martakis, Otto Overdijk, Robert A. Robinson, Alexander Solokha, Fernando Spina, Seydina Issa Sylla, Jan Veen, Dick Visser, “Urgent preliminary assessment of ornithological data relevant to the spread of Avian Influenza in Europe: Eurasian Wigeon movements” (2006); http://ec.europa.eu/environment/nature/conservation/wildbirds/birdflue/docs/rep_spread_avian_influenza_report.pdf.
48
BirdLife International, American Wigeon (Mareca americana), The IUCN Red List of Threatened Species; http://www.iucnredlist.org/details/22680163/0.
49
Seattle Audubon Society, American Wigeon (Anas americana); http://www.birdweb.org/birdweb/bird/american_wigeon.
50
M. R. Miller, Spring migration of Northern Pintails assessed with satellite telemetry; http://www.werc.usgs.gov/OLDsitedata/pubbriefs/millerpbsep2006.html
51
BirdLife International, Northern Pintail (Anas acuta), The IUCN Red List of Threatened Species; http://www.birdlife.org/datazone/speciesfactsheet.php?id=457.
52
Hashimoto H. and Sugawa H., Population trends of wintering Eurasian coot Fulica atra in East Asia. Ornitholog. Sci. 12, 91–105 (2013).
53
BirdLife International, Gadwall (Mareca strepera) - BirdLife species factsheet; http://www.birdlife.org/datazone/species/factsheet/22680149.
54
Yamaguchi N., Hiraoka E., Fujita M., Hijikata N., Ueta M., Takagi K., Konno S., Okuyama M., Watanabe Y., Osa Y., Morishita E., Tokita K., Umada K., Fujita G., and Higuchi H., Spring migration routes of mallards (Anas platyrhynchos) that winter in Japan, determined from satellite telemetry. Zoolog. Sci. 25, 875–881 (2008).
55
BirdLife International, White-naped Crane (Antigone vipio) - BirdLife species factsheet; http://www.birdlife.org/datazone/species/factsheet/22692073.
56
BirdLife International, Hooded Crane (Grus monacha) - BirdLife species factsheet; http://www.birdlife.org/datazone/species/factsheet/22692151.
57
BirdLife International, Mute Swan (Cygnus olor) - BirdLife species factsheet; http://www.birdlife.org/datazone/species/factsheet/22679839.
58
BirdLife International, Falco rusticolus (Gyrfalcon). The IUCN Red List of Threatened Species; http://www.iucnredlist.org/details/22696500/0.
59
BirdLife International, Branta canadensis. The IUCN Red List of Threatened Species; http://www.iucnredlist.org/details/22679935/0.
Information & Authors
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Published In
Science
Volume 354 | Issue 6309
14 October 2016
14 October 2016
Copyright
Copyright © 2016, American Association for the Advancement of Science.
Submission history
Received: 21 April 2016
Accepted: 7 September 2016
Published in print: 14 October 2016
Acknowledgments
This study was financially supported by the European Commission H2020 program under contract number 643476 (www.compare-europe.eu) (to A.P., J.B., A.B., I.B., M.P.K., A.R., R.A.M.F., M.B., M.W., and T.K.), European Commission FP7 program under contract number 278433 (PREDEMICS) (to A.R.), the U. S. Geological Survey Ecosystems Mission Area (to H.S.I.), National Institutes of Health grant number 1R01AI101028-02A1 (to M.G.), United Kingdom Research Council Environmental and Social Ecology of Human Infectious Diseases UrbanZoo program (G1100783/1), Biotechnology and Biological Sciences Research Council (BBSRC) Zoonoses in Livestock in Kenya ZooLinK (BB/L019019/1) programs (to T.P.R. and M.W.), CGIAR Research Programme on Agriculture for Nutrition and Health (A4NH) (to T.P.R.), Canadian Food Inspection Agency (to J.P.), Hungarian Academy of Sciences Lendület (Momentum) program (to K.B.) and the Wellcome Trust (grant number 093724/B/10/Z) (to M.W. and A.R.). S.J.L. is supported by the University of Edinburgh Chancellor’s Fellowship scheme, the Roslin Institute BBSRC strategic program grant (BB/J004227/1), and the Centre of Expertise in Animal Disease Outbreaks (EPIC). We gratefully acknowledge the the originating laboratories, where specimens were first obtained, and the submitting laboratories, where sequence data were generated and submitted to the EpiFlu Database of the Global Initiative on Sharing All Influenza Data (GISAID), on which this research is based. All contributors of data may be contacted directly via the GISAID website (http://platform.gisaid.org). The accession numbers (GenBank, GISAID, and/or workset identification numbers) of all genetic sequences used in this study are provided in table S9 and are accessible from the website of GISAID (http://platform.gisaid.org). We acknowledge Y. Berhane and T. Hisanaga for sequencing the Canadian virus isolates and G. Koch for his technical advice on the poultry outbreaks in the Netherlands. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Any use of trade products or firm names is for descriptive purposes and does not imply endorsement by the U.S. government.
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