High pathogenic avian influenza A(H5) viruses of clade 2.3.4.4b in Europe—Why trends of virus evolution are more difficult to predict-Reference-Cited by-同舟云学术

High pathogenic avian influenza A(H5) viruses of clade 2.3.4.4b in Europe—Why trends of virus evolution are more difficult to predict

Published:2024-01-01 Issue:1 Volume:10 Page:
ISSN:2057-1577
Container-title:Virus Evolution
language:en
Short-container-title:

Author:

Fusaro Alice¹^ORCID,Zecchin Bianca¹^ORCID,Giussani Edoardo¹,Palumbo Elisa¹^ORCID,Agüero-García Montserrat²,Bachofen Claudia³,Bálint Ádám⁴,Banihashem Fereshteh⁵,Banyard Ashley C⁶,Beerens Nancy⁷^ORCID,Bourg Manon⁸,Briand Francois-Xavier⁹,Bröjer Caroline¹⁰,Brown Ian H⁶,Brugger Brigitte¹¹^ORCID,Byrne Alexander M P⁶,Cana Armend¹²,Christodoulou Vasiliki¹³,Dirbakova Zuzana¹⁴,Fagulha Teresa¹⁵,Fouchier Ron A M¹⁶,Garza-Cuartero Laura¹⁷,Georgiades George¹⁸,Gjerset Britt¹⁹,Grasland Beatrice⁹,Groza Oxana²⁰,Harder Timm²¹,Henriques Ana Margarida¹⁵,Hjulsager Charlotte Kristiane²²^ORCID,Ivanova Emiliya²³,Janeliunas Zygimantas²⁴,Krivko Laura²⁵,Lemon Ken²⁶^ORCID,Liang Yuan²⁷,Lika Aldin²⁸,Malik Péter⁴,McMenamy Michael J²⁶,Nagy Alexander²⁹,Nurmoja Imbi³⁰,Onita Iuliana³¹,Pohlmann Anne²¹^ORCID,Revilla-Fernández Sandra³²,Sánchez-Sánchez Azucena²,Savic Vladimir³³,Slavec Brigita³⁴,Smietanka Krzysztof³⁵,Snoeck Chantal J³⁶^ORCID,Steensels Mieke³⁷,Svansson Vilhjálmur³⁸,Swieton Edyta³⁵,Tammiranta Niina³⁹,Tinak Martin¹⁴,Van Borm Steven³⁷,Zohari Siamak⁵,Adlhoch Cornelia⁴⁰^ORCID,Baldinelli Francesca⁴¹,Terregino Calogero¹,Monne Isabella¹

Affiliation:

1. European Reference Laboratory (EURL) for Avian Influenza and Newcastle Disease, Istituto Zooprofilattico Sperimentale delle Venezie , viale dell'universita 10, Legnaro, Padua 35020, Italy

2. Ministry of Agriculture, Fisheries and Food, Laboratorio Central de Veterinaria (LCV) , Ctra. M-106, Km 1,4 Algete, Madrid 28110, Spain

3. Federal Department of Home Affairs FDHA Institute of Virology and Immunology IVI , Sensemattstrasse 293, Mittelhäusern 3147, Switzerland

4. Veterinary Diagnostic Directorate (NEBIH), Laboratory of Virology, National Food Chain Safety Office , Tábornok utca 2, Budapest 1143, Hungary

5. Department of Microbiology, National Veterinary Institute (SVA) , Travvägen 20, Uppsala 75189, Sweden

6. WOAH/FAO international reference laboratory for Avian Influenza and Newcastle Disease, Virology Department, Animal and Plant Health Agency-Weybridge , Woodham Lane, New Haw, Addlestone KT15 3NB, United Kingdom

7. Department of Virology Wageningen Bioveterinary Research , Houtribweg 39, Lelystad 8221 RA, The Netherlands

8. Luxembourgish Veterinary and Food Administration (ALVA), State Veterinary Laboratory , 1 Rue Louis Rech, Dudelange 3555, Luxembourg

9. Agence Nationale de Sécurité Sanitaire, de l’Alimentation, de l’Environnement et du Travail, Laboratoire de Ploufragan-Plouzané-Niort, Unité de Virologie, Immunologie, Parasitologie Avaires et Cunicoles , 41 Rue de Beaucemaine – BP 53, Ploufragan 22440, France

10. Department of Pathology and Wildlife Disease, National Veterinary Institute (SVA) , Travvägen 20, Uppsala 75189, Sweden

11. Icelandic Food and Veterinary Authority , Austurvegur 64, Selfoss 800, Iceland

12. Kosovo Food and Veterinary Agency, Sector of Serology and Molecular Diagnostics, Kosovo Food and Veterinary Laboratory , Str Lidhja e Pejes, Prishtina 10000, Kosovo

13. Laboratory for Animal Health Virology Section Veterinary Services (1417) , 79, Athalassa Avenue Aglantzia, Nicosia 2109, Cyprus

14. Department of Animal Health, State Veterinary Institute , Pod Dráhami 918, Zvolen 96086, Slovakia

15. I.P. (INIAV, I.P.), Avenida da República, Instituto Nacional de Investigação Agrária e Veterinária , Quinta do Marquês, Oeiras 2780 – 157, Portugal

16. Department of Viroscience, Erasmus MC , Dr. Molewaterplein 40, Rotterdam 3015 GD, The Netherlands

17. Department of Agriculture, Food and the Marine, Central Veterinary Research Laboratory (CVRL) , Backweston Campus, Stacumny Lane, Celbridge, Co. Kildare W23 X3PH, Ireland

18. Thessaloniki Veterinary Centre (TVC), Department of Avian Diseases , 26th October Street 80, Thessaloniki 54627, Greece

19. Immunology & Virology department, Norwegian Veterinary Institute , Arboretveien 57, Oslo Pb 64, N-1431 Ås, Norway

20. Republican Center for Veterinary Diagnostics (NRL) , 3 street Murelor, Chisinau 2051, Republic of Moldova

21. Institute of Diagnostic Virology, Friedrich-Loeffler-Institut , Südufer 10, Greifswald-Insel Riems 17493, Germany

22. Department for Virus and Microbiological Special Diagnostics, Statens Serum Institut , 5 Artillerivej, Copenhagen DK-2300, Denmark

23. National Reference Laboratory for Avian Influenza and Newcastle Disease, National Diagnostic and Research Veterinary Medical Institute (NDRVMI) , 190 Lomsko Shose Blvd., Sofia 1231, Bulgaria

24. National Food and Veterinary Risk Assessment Institute (NFVRAI) , Kairiukscio str. 10, Vilnius 08409, Lithuania

25. Institute of Food Safety, Animal Health and Environment (BIOR), Laboratory of Microbilogy and Pathology , 3 Lejupes Street, Riga 1076, Latvia

26. Virological Molecular Diagnostic Laboratory, Veterinary Sciences Division, Department of Virology, Agri-Food and Bioscience Institute (AFBI) , Stoney Road, Belfast BT4 3SD, Northern Ireland

27. Department of Veterinary and Animal Sciences, University of Copenhagen , Grønnegårdsvej 15, Frederiksberg 1870, Denmark

28. Animal Health Department, Food Safety and Veterinary Institute , Rruga Aleksandër Moisiu 10, Tirana 1001, Albania

29. Department of Molecular Biology, State Veterinary Institute Prague , Sídlištní 136/24, Praha 6-Lysolaje 16503, Czech Republic

30. National Centre for Laboratory Research and Risk Assessment (LABRIS) , Kreutzwaldi 30, Tartu 51006, Estonia

31. Institute for Diagnosis and Animal Health (IDAH) , Str. Dr. Staicovici 63, Bucharest 050557, Romania

32. Austrian Agency for Health and Food Safety (AGES), Institute for Veterinary Disease Control , Robert Koch Gasse 17, Mödling 2340, Austria

33. Croatian Veterinary Institute, Poultry Centre , Heinzelova 55, Zagreb 10000, Croatia

34. University of Ljubljana – Veterinary Faculty/National Veterinary Institute , Gerbičeva 60, Ljubljana 1000, Slovenia

35. Department of Poultry Diseases, National Veterinary Research Institute , Al. Partyzantow 57, Puławy 24-100, Poland

36. Luxembourg Institute of Health (LIH), Department of Infection and Immunity , 29 Rue Henri Koch, Esch-sur-Alzette 4354, Luxembourg

37. Avian Virology and Immunology, Sciensano , Rue Groeselenberg 99, Ukkel 1180, Ukkel, Belgium

38. Biomedical Center, Institute for Experimental Pathology, University of Iceland , Keldnavegi 3 112 Reykjavík Ssn. 650269 4549, Keldur 851, Iceland

39. Finnish Food Authority, Animal Health Diagnostic Unit, Veterinary Virology , Mustialankatu 3, Helsinki FI-00790, Finland

40. European Centre for Disease Prevention and Control , Gustav III:s boulevard 40, Solna 169 73, Sweden

41. European Food Safety Authority (EFSA) , Via Carlo Magno 1A, Parma 43126, Italy

Abstract

Abstract Since 2016, A(H5Nx) high pathogenic avian influenza (HPAI) virus of clade 2.3.4.4b has become one of the most serious global threats not only to wild and domestic birds, but also to public health. In recent years, important changes in the ecology, epidemiology, and evolution of this virus have been reported, with an unprecedented global diffusion and variety of affected birds and mammalian species. After the two consecutive and devastating epidemic waves in Europe in 2020–2021 and 2021–2022, with the second one recognized as one of the largest epidemics recorded so far, this clade has begun to circulate endemically in European wild bird populations. This study used the complete genomes of 1,956 European HPAI A(H5Nx) viruses to investigate the virus evolution during this varying epidemiological outline. We investigated the spatiotemporal patterns of A(H5Nx) virus diffusion to/from and within Europe during the 2020–2021 and 2021–2022 epidemic waves, providing evidence of ongoing changes in transmission dynamics and disease epidemiology. We demonstrated the high genetic diversity of the circulating viruses, which have undergone frequent reassortment events, providing for the first time a complete overview and a proposed nomenclature of the multiple genotypes circulating in Europe in 2020–2022. We described the emergence of a new genotype with gull adapted genes, which offered the virus the opportunity to occupy new ecological niches, driving the disease endemicity in the European wild bird population. The high propensity of the virus for reassortment, its jumps to a progressively wider number of host species, including mammals, and the rapid acquisition of adaptive mutations make the trend of virus evolution and spread difficult to predict in this unfailing evolving scenario.

Funder

HORIZON EUROPE Food, Bioeconomy, Natural Resources, Agriculture and Environment

Animal Health and Welfare ERA-Net

Biotechnology and Biological Sciences Research Council

Department for Environment, Food and Rural Affairs, UK Government

Publisher

Oxford University Press (OUP)

Link

https://academic.oup.com/ve/advance-article-pdf/doi/10.1093/ve/veae027/57176125/veae027.pdf

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