Literature detail

Genesis and spread of multiple reassortants during the 2016/2017 H5 avian influenza epidemic in Eurasia.

Samantha J Lycett¹ Anne Pohlmann² Christoph Staubach³ Valentina Caliendo⁴ Mark Woolhouse⁵ Martin Beer² Thijs Kuiken^6,7 Global Consortium for H5N8 and Related Influenza Viruses

Affiliations 7 institutions

The Roslin Institute, University of Edinburgh, EH25 9RG Edinburgh, United Kingdom.
Institute of Diagnostic Virology, Friedrich Loeffler Institut, D-17493 Greifswald-Insel Riems, Germany.
Institute of Epidemiology, Friedrich Loeffler Institut, D-17493 Greifswald-Insel Riems, Germany.
Department of Viroscience, Erasmus University Medical Center, 3015 NC Rotterdam, the Netherlands.
Usher Institute, University of Edinburgh, EH9 3FL Edinburgh, United Kingdom.
Department of Viroscience, Erasmus University Medical Center, 3015 NC Rotterdam, the Netherlands
[email protected].

PMID 32769208 2020 Proc Natl Acad Sci U S A eng ppublish

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Article

Publication summary

Highly pathogenic avian influenza (HPAI) viruses of the H5 A/goose/Guangdong/1/96 lineage can cause severe disease in poultry and wild birds, and occasionally in humans. In recent years, H5 HPAI viruses of this lineage infecting poultry in Asia have spilled over into wild birds and spread via bird migration to countries in Europe, Africa, and North America. In 2016/2017, this spillover resulted in the largest HPAI epidemic on record in Europe and was associated with an unusually high frequency of reassortments between H5 HPAI viruses and cocirculating low-pathogenic avian influenza viruses. Here, we show that the seven main H5 reassortant viruses had various combinations of gene segments 1, 2, 3, 5, and 6. Using detailed time-resolved phylogenetic analysis, most of these gene segments likely originated from wild birds and at dates and locations that corresponded to their hosts' migratory cycles. However, some gene segments in two reassortant viruses likely originated from domestic anseriforms, either in spring 2016 in east China or in autumn 2016 in central Europe. Our results demonstrate that, in addition to domestic anseriforms in Asia, both migratory wild birds and domestic anseriforms in Europe are relevant sources of gene segments for recent reassortant H5 HPAI viruses. The ease with which these H5 HPAI viruses reassort, in combination with repeated spillovers of H5 HPAI viruses into wild birds, increases the risk of emergence of a reassortant virus that persists in wild bird populations yet remains highly pathogenic for poultry.

emerging infectious diseases highly pathogenic avian influenza phylogenetic analysis poultry wild birds Animals Animals, Wild Asia Birds Epidemics Europe Influenza A Virus, H5N1 Subtype Influenza in Birds Phylogeny Poultry Reassortant Viruses

Structured evidence records

Evidence records

6 total

Cross Species Transmission 2 records

Cross Species Transmission Extraction confidence 0.85

Key finding

H5 highly pathogenic avian influenza viruses transmitted from poultry to wild birds, indicating cross-species transmission among non-human avian hosts.

Virus

Host

Location

Supporting text

In recent years, H5 HPAI viruses of this lineage infecting poultry in Asia have spilled over into wild birds and spread via bird migration to countries in Europe, Africa, and North America.

Method: phylogenetic analysis
Study design: phylogenetic analysis
Transmission direction: animal-to-animal
Geographic raw: Asia

Cross Species Transmission Extraction confidence 0.85

Key finding

Reassortant H5 highly pathogenic avian influenza viruses showed gene exchanges between domestic anseriforms and migratory wild birds, indicating recurrent animal-to-animal cross-species transmission among bird hosts.

Virus

Host

Location

Supporting text

Some gene segments in two reassortant viruses likely originated from domestic anseriforms, either in spring 2016 in east China or in autumn 2016 in central Europe. Our results demonstrate that, in addition to domestic anseriforms in Asia, both migratory wild birds and domestic anseriforms in Europe are relevant sources of gene segments for recent reassortant H5 HPAI viruses.

Method: phylogenetic analysis
Study design: phylogenetic analysis
Transmission direction: animal-to-animal
Geographic raw: east China or central Europe

Genomic Evolution 2 records

Genomic Evolution Extraction confidence 0.95

Key finding

Phylogenetic analysis revealed that seven H5 reassortant avian influenza viruses contained distinct combinations of gene segments derived mainly from wild birds, indicating their genomic evolution through reassortment.

Virus

Host

Location

Supporting text

Here, we show that the seven main H5 reassortant viruses had various combinations of gene segments 1, 2, 3, 5, and 6. Using detailed time-resolved phylogenetic analysis, most of these gene segments likely originated from wild birds and at dates and locations that corresponded to their hosts' migratory cycles.

Genes or proteins: gene segments 1; gene segments 2; gene segments 3; gene segments 5; gene segments 6
Analysis methods: time-resolved phylogenetic analysis

Genomic Evolution Extraction confidence 0.95

Key finding

Phylogenetic analysis indicated that certain gene segments in two H5 reassortant viruses originated from domestic anseriforms in east China or central Europe, showing region-specific genomic contributions to reassortment.

Virus

Host

Location

Supporting text

Some gene segments in two reassortant viruses likely originated from domestic anseriforms, either in spring 2016 in east China or in autumn 2016 in central Europe.

Genes or proteins: gene segments
Analysis methods: phylogenetic analysis

Recombination Or Reassortment 1 records

Recombination Or Reassortment Extraction confidence 1.00

Key finding

Multiple H5 highly pathogenic avian influenza reassortant viruses emerged during the 2016/2017 epidemic, acquiring gene segments 1, 2, 3, 5, and 6 from cocirculating low-pathogenic avian influenza viruses.

Virus

Host

Location

Supporting text

In 2016/2017, this spillover resulted in the largest HPAI epidemic on record in Europe and was associated with an unusually high frequency of reassortments between H5 HPAI viruses and cocirculating low-pathogenic avian influenza viruses. Here, we show that the seven main H5 reassortant viruses had various combinations of gene segments 1, 2, 3, 5, and 6.

Event type: reassortment
Genes or segments: segment 1; segment 2; segment 3; segment 5; segment 6

Spillover Event 1 records

Spillover Event Extraction confidence 0.95

Key finding

H5 highly pathogenic avian influenza viruses spilled over from poultry into wild birds during recent years, contributing to the 2016/2017 epidemic in Eurasia.

Virus

Host

Location

Supporting text

In recent years, H5 HPAI viruses of this lineage infecting poultry in Asia have spilled over into wild birds and spread via bird migration to countries in Europe, Africa, and North America.

Method: phylogenetic analysis
Transmission direction: unknown
Geographic raw: Asia; Europe; Africa; North America

Citation context

References

57 references

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PMID 29670093	M	van den Brand	2018
PMID 30154345	C., The pandemic threat of emerging H5 and H7 avian influenza viruses	Sutton	2018
PMID 27738169	et al.; Global Consortium for H5N8 and Related Influenza Viruses , Role for migratory wild birds in the global spread of avian influenza H5N8	Lycett	2016
PMID 19267878	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	Globig	2009
PMID 26159311	et al., 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	Bouwstra	2015
PMID 25898126	et al., Genetic characterization of highly pathogenic avian influenza (H5N8) virus from domestic ducks, England, November 2014	Hanna	2015
PMID 26519355	et al., Highly pathogenic avian influenza H5N8 in Germany: Outbreak investigations	Conraths	2016
PMID 29148372	et al., Deaths among wild birds during highly pathogenic avian influenza A(H5N8) virus outbreak, The Netherlands	Kleyheeg	2017
PMID 30205456	et al., White-tailed sea eagle ( Haliaeetus albicilla ) die-off due to infection with highly pathogenic avian influenza virus, subtype H5N8, in Germany	Krone	2018
PMID 27314845	et al., Highly pathogenic avian influenza viruses and generation of novel reassortants, United States, 2014-2015	Lee	2016
-	3	World Health Organization	2020
PMID 25966311	D., Donis R. O.; World Health Organization/World Organisation for Animal Health/Food and Agriculture Organization (WHO/OIE/FAO) H5 Evolution Working Group , Nomenclature updates resulting from the evolution of avian influenza A(H5) virus clades 2.1.3.2a, 2.2.1, and 2.3.4 during 2013-2014. Influenza Other Respir	Smith	2015
PMID 31056053	J., Duchatel F., Digard P., A brief history of bird flu. Philos. Trans. R	Lycett	2019
PMID 17283615	D., Stallknecht D. E., Beck J. R., Suarez D. L., Swayne D. E., Susceptibility of North American ducks and gulls to H5N1 highly pathogenic avian influenza viruses	Brown	2006
PMID 18394278	et al., Wild ducks as long-distance vectors of highly pathogenic avian influenza virus (H5N1)	Keawcharoen	2008
PMID 23735616	et al., Experimental infection of bar-headed geese ( Anser indicus ) and ruddy shelducks ( Tadorna ferruginea ) with a clade 2.3.2 H5N1 highly pathogenic avian influenza virus	Nemeth	2013
PMID 29726612	et al., Experimental infection of H5N1 and H5N8 highly pathogenic avian influenza viruses in Northern Pintail ( Anas acuta )	Kwon	2018
PMID 32625308	et al., Scientific report on the avian influenza overview October 2016–August 2017	Brown	2017
PMID 25897703	et al., Influenza A(H5N8) virus similar to strain in Korea causing highly pathogenic avian influenza in Germany	Harder	2015
PMID 29311555	et al., Swarm incursions of reassortants of highly pathogenic avian influenza virus strains H5N8 and H5N5, clade 2.3.4.4b, Germany, winter 2016/17	Pohlmann	2018
PMID 25007845	C., Influenza A virus reassortment	Steel	2014
PMID 29942656	et al., Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10	Suchard	2018
PMID 16221896	H., Bryant D., Application of phylogenetic networks in evolutionary studies	Huson	2006
PMID 27875109	et al., Novel reassortant clade 2.3.4.4 avian influenza A(H5N8) virus in wild aquatic birds, Russia, 2016	Lee	2017
PMID 28169827	et al., Highly pathogenic avian influenza A(H5N8) virus in wild migratory birds, Qinghai Lake, China	Li	2017
PMID 29912707	, Highly pathogenic avian influenza A(H5N8) virus, Democratic Republic of the Congo, 2017	Twabela	2018
PMID 27684783	et al., Lack of virological and serological evidence for continued circulation of highly pathogenic avian influenza H5N8 virus in wild birds in The Netherlands, 14 November 2014 to 31 January 2016	Poen	2016
PMID 29148396	et al., Multiple reassorted viruses as cause of highly pathogenic avian influenza A(H5N8) virus epidemic, The Netherlands, 2016	Beerens	2017
PMID 28661831	et al., Genetic diversity of highly pathogenic avian influenza A(H5N8/H5N5) viruses in Italy, 2016-17	Fusaro	2017
PMID 28055819	et al., Outbreaks among wild birds and domestic poultry caused by reassorted influenza A(H5N8) clade 2.3.4.4 viruses, Germany, 2016	Pohlmann	2017
PMID 28518040	et al., Highly pathogenic avian influenza virus (H5N8) clade 2.3.4.4 infection in migratory birds, Egypt	Selim	2017
PMID 30575785	et al., Integration of genetic and epidemiological data to infer H5N8 HPAI virus transmission dynamics during the 2016-2017 epidemic in Italy	Mulatti	2018
PMID 29920971	, Śmietanka K	Świętoń	2018
-	A., Rose P. M., Atlas of Anatidae Populations in Africa and Western Eurasia, (Wetlands International, 1996)	Scott	1996
-	, Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic Volume V: Tyrant Flycatchers to Thrushes, (Oxford University Press, New York, NY, 1988)	Cramp	1988
PMID 30457528	et al., Comparison of 2016-17 and previous epizootics of highly pathogenic avian influenza H5 Guangdong lineage in Europe	Alarcon	2018
-	https://www	USDA	2020
PMID 31056057	et al., Comparative micro-epidemiology of pathogenic avian influenza virus outbreaks in a wild bird population. Philos. Trans. R	Hill	2019
PMID 27309079	, High rates of detection of clade 2.3.4.4 highly pathogenic avian influenza H5 viruses in wild birds in the Pacific Northwest during the winter of 2014-15	Ip	2016
PMID 30026505 In OmniVira	A novel European H5N8 influenza A virus has increased virulence in ducks but low zoonotic potential.	Grund	2018
PMID 19196383	, Hurford A	Alizon	2009
PMID 31538926	et al., Genetic characterization and zoonotic potential of highly pathogenic avian influenza virus A(H5N6/H5N5), Germany, 2017-2018	Pohlmann	2019
PMID 30226167	et al., Transmission dynamics of highly pathogenic avian influenza virus A(H5Nx) clade 2.3.4.4, North America, 2014-2015	Lee	2018
PMID 24033258	G	van Dijk	2014
PMID 16627734	, Global patterns of influenza A virus in wild birds	Olsen	2006
PMID 23740783	, Is low pathogenic avian influenza virus virulent for wild waterbirds? Proc	Kuiken	2013
PMID 31586866	J., Inferring host roles in bayesian phylodynamics of global avian influenza A virus H9N2. Virology 538, 86–96 (2019)	Yang	2019
PMID 24798745	, Isel C	Gerber	2014
PMID 24043788	et al., Critical role of segment-specific packaging signals in genetic reassortment of influenza A viruses	Essere	2013
PMID 23180580	et al., Improving Bayesian population dynamics inference: A coalescent-based model for multiple loci	Gill	2013
PMID 17874105	N., Suchard M. A., Counting labeled transitions in continuous-time Markov models of evolution	Minin	2008
PMID 29790921	F., Rasmussen D., Stadler T., MASCOT: Parameter and state inference under the marginal structured coalescent approximation	Müller	2018
PMID 23329690	M., MAFFT multiple sequence alignment software version 7: Improvements in performance and usability	Katoh	2013
PMID 24451623	, RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies	Stamatakis	2014
PMID 18218099	H., Huson D. H., Drawing explicit phylogenetic networks and their integration into SplitsTree	Kloepper	2008
PMID 30375994	et al., Global distribution data for cattle, buffaloes, horses, sheep, goats, pigs, chickens and ducks in 2010. Sci. Data 5, 180227 (2018)	Gilbert	2018
-	” Avian Influenza Portal	OIE	2020

Evidence overview

Evidence 6

Types 4

Virus 1

Host 2

Evidence types

Cross Species Transmission 2 Genomic Evolution 2 Recombination Or Reassortment 1 Spillover Event 1

Linked entities

Viruses

Hosts

Locations

Publication metadata

Journal: Proceedings of the National Academy of Sciences of the United States of America
Volume / Issue / Pages: 117 / 34 / 20814-20825
ISSN: 1091-6490
Journal country: United States
DOI: 10.1073/pnas.2001813117