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Viruses
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Highly Pathogenic Avian Influenza Virus Emergence
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Highly Pathogenic Avian Influenza Virus Emergence

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Animal Viruses".

Deadline for manuscript submissions: closed (31 May 2022) | Viewed by 33678

Special Issue Editor

Dr. Mathilde Richard

E-Mail Website
Guest Editor
Viroscience Department, Erasmus MC, Rotterdam, The Netherlands
Interests: molecular virology; viral pathogenesis; viral evolution; virus–host interactions; influenza viruses; polymerase; viral transmission; zoonosis; pandemics

Special Issue Information

Dear Colleagues,

Highly pathogenic avian influenza virus (HPAIV) outbreaks have resulted in billions of poultry deaths through the culling of infected or potentially exposed poultry. HPAIVs emerge from low pathogenic avian influenza viruses (LPAIVs) upon transmission from wild waterfowl to terrestrial poultry. Since 1959, a total of 47 independent transitions from LPAIV to HPAIV have been recorded, all in influenza viruses of the H5 and H7 subtypes. Drastic measures, such as the culling of infected and exposed poultry, are needed to control HPAIVs and reduce the risk of zoonotic transmission. However, despite rigorous interventions, some HPAIVs (e.g. H5 HPAIVs from the A/goose/Guangdong/1/1996 (GsGd) lineage) disseminated globally, leading to devastating economic losses and consequences. They constitute the only lineage of HPAIV that has become endemic in poultry and is circulating in wild birds in many countries of the world. Besides these devastating consequences on animal welfare and the poultry industry, spill-over events of HPAIVs to humans pose a continuous pandemic threat.

Understanding the main drivers of HPAIV emergence is critical for the design and implementation of strategies to mitigate their impact on animal species. The scope of this Special Issue is to gather articles (research articles, short communications, reviews, and commentaries) on the viral, host, and environmental factors that drive HPAIV emergence, regarding both the transition from LPAIV to HPAIV as well as HPAIV emergence, natural selection, and establishment in different animal species.

Dr. M. Richard
Guest Editor

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Keywords

  • highly pathogenic avian influenza
  • virus emergence
  • virus evolution
  • natural selection
  • reservoir
  • spill-over hosts
  • birds

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Published Papers (7 papers)

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Research

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16 pages, 5022 KiB  
Article
Silent Infection of Highly Pathogenic Avian Influenza Virus (H5N1) Clade 2.3.4.4b in a Commercial Chicken Broiler Flock in Italy
by Federica Gobbo, Claudia Zanardello, Marco Bottinelli, Jane Budai, Francesca Bruno, Roberta De Nardi, Tommaso Patregnani, Salvatore Catania and Calogero Terregino
Viruses 2022, 14(8), 1600; https://doi.org/10.3390/v14081600 - 22 Jul 2022
Cited by 15 | Viewed by 3745
Abstract
From October 2021 to January 2022, different incursions of clade 2.3.4.4b H5N1 HPAIV (Highly Pathogenic Avian Influenza Virus) occurred in several Italian regions with its main diffusion in Densely Poultry Populated Areas (DPPAs) of north-eastern Italy. Monitoring and control activities applied in the [...] Read more.
From October 2021 to January 2022, different incursions of clade 2.3.4.4b H5N1 HPAIV (Highly Pathogenic Avian Influenza Virus) occurred in several Italian regions with its main diffusion in Densely Poultry Populated Areas (DPPAs) of north-eastern Italy. Monitoring and control activities applied in the affected area clearly evidenced that turkeys and broilers were the most affected species, although several flocks of broilers at times resulted HPAIV H5N1 infected in absence of increased mortality and/or clinical signs. Thus, an approach based on sampling dead birds was adopted in the broiler sector to improve the early detection of infection; this protocol allowed us to confirm that 15 farms were HPAIV-infected with birds ready to be delivered to the slaughterhouse. The aim of this report is to describe the results of the diagnostic activities carried out in one HPAIV H5N1-infected broiler farm, three days after laboratory confirmation during the pre-movement testing without showing increased mortality or clinical signs. Thus, clinical signs, daily cumulative mortality rate (CMR), virus shedding, seroconversion, pathobiology of clade 2.3.4.4b H5N1 HPAIV as well as Avian Influenza Viruses (AIVs) environmental contamination were thoroughly examined in the infected holding. Such in-depth investigation demonstrated low infection prevalence in live birds, low environmental contamination, no seroconversion for AIVs, gross and microscopic findings compatible with systemic infection with peracute death in H5N1 HPAIV-infected birds. Full article
(This article belongs to the Special Issue Highly Pathogenic Avian Influenza Virus Emergence)
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21 pages, 3236 KiB  
Article
In Silico Analyses of the Role of Codon Usage at the Hemagglutinin Cleavage Site in Highly Pathogenic Avian Influenza Genesis
by Mathis Funk, Anja C. M. de Bruin, Monique I. Spronken, Alexander P. Gultyaev and Mathilde Richard
Viruses 2022, 14(7), 1352; https://doi.org/10.3390/v14071352 - 21 Jun 2022
Cited by 3 | Viewed by 2752
Abstract
A vast diversity of 16 influenza hemagglutinin (HA) subtypes are found in birds. Interestingly, viruses from only two subtypes, H5 and H7, have so far evolved into highly pathogenic avian influenza viruses (HPAIVs) following insertions or substitutions at the HA cleavage site by [...] Read more.
A vast diversity of 16 influenza hemagglutinin (HA) subtypes are found in birds. Interestingly, viruses from only two subtypes, H5 and H7, have so far evolved into highly pathogenic avian influenza viruses (HPAIVs) following insertions or substitutions at the HA cleavage site by the viral polymerase. The mechanisms underlying this striking subtype specificity are still unknown. Here, we compiled a comprehensive dataset of 20,488 avian influenza virus HA sequences to investigate differences in nucleotide and amino acid usage at the HA cleavage site between subtypes and how these might impact the genesis of HPAIVs by polymerase stuttering and realignment. We found that sequences of the H5 and H7 subtypes stand out by their high purine content at the HA cleavage site. In addition, fewer substitutions were necessary in H5 and H7 HAs than in HAs from other subtypes to acquire an insertion-prone HA cleavage site sequence, as defined based on in vitro and in vivo data from the literature. Codon usage was more favorable for HPAIV genesis in sequences of viruses isolated from species or geographical regions in which HPAIV genesis is more frequently observed in nature. The results of the present analyses suggest that the subtype restriction of HPAIV genesis to H5 and H7 influenza viruses might be due to the particular codon usage at the HA cleavage site in these subtypes. Full article
(This article belongs to the Special Issue Highly Pathogenic Avian Influenza Virus Emergence)
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11 pages, 926 KiB  
Article
Tropism of Highly Pathogenic Avian Influenza H5 Viruses from the 2020/2021 Epizootic in Wild Ducks and Geese
by Valentina Caliendo, Lonneke Leijten, Marco van de Bildt, Evelien Germeraad, Ron A. M. Fouchier, Nancy Beerens and Thijs Kuiken
Viruses 2022, 14(2), 280; https://doi.org/10.3390/v14020280 - 28 Jan 2022
Cited by 17 | Viewed by 4088
Abstract
Highly pathogenic avian influenza (HPAI) outbreaks have become increasingly frequent in wild bird populations and have caused mass mortality in many wild bird species. The 2020/2021 epizootic was the largest and most deadly ever reported in Europe, and many new bird species tested [...] Read more.
Highly pathogenic avian influenza (HPAI) outbreaks have become increasingly frequent in wild bird populations and have caused mass mortality in many wild bird species. The 2020/2021 epizootic was the largest and most deadly ever reported in Europe, and many new bird species tested positive for HPAI virus for the first time. This study investigated the tropism of HPAI virus in wild birds. We tested the pattern of virus attachment of 2020 H5N8 virus to intestinal and respiratory tissues of key bird species; and characterized pathology of naturally infected Eurasian wigeons (Mareca penelope) and barnacle geese (Branta leucopsis). This study determined that 2020 H5N8 virus had a high level of attachment to the intestinal epithelium (enterotropism) of dabbling ducks and geese and retained attachment to airway epithelium (respirotropism). Natural HPAI 2020 H5 virus infection in Eurasian wigeons and barnacle geese also showed a high level of neurotropism, as both species presented with brain lesions that co-localized with virus antigen expression. We concluded that the combination of respirotropism, neurotropism, and possibly enterotropism, contributed to the successful adaptation of 2020/2021 HPAI H5 viruses to wild waterbird populations. Full article
(This article belongs to the Special Issue Highly Pathogenic Avian Influenza Virus Emergence)
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10 pages, 1581 KiB  
Communication
Detection of Highly Pathogenic Avian Influenza Virus H5N1 Clade 2.3.4.4b in Great Skuas: A Species of Conservation Concern in Great Britain
by Ashley C. Banyard, Fabian Z. X. Lean, Caroline Robinson, Fiona Howie, Glen Tyler, Craig Nisbet, James Seekings, Stephanie Meyer, Elliot Whittard, Henry F. Ashpitel, Mehmet Bas, Alexander M. P. Byrne, Tom Lewis, Joe James, Levon Stephan, Nicola S. Lewis, Ian H. Brown, Rowena D. E. Hansen and Scott M. Reid
Viruses 2022, 14(2), 212; https://doi.org/10.3390/v14020212 - 21 Jan 2022
Cited by 54 | Viewed by 6494
Abstract
The UK and Europe have seen successive outbreaks of highly pathogenic avian influenza across the 2020/21 and 2021/22 autumn/winter seasons. Understanding both the epidemiology and transmission of these viruses in different species is critical to aid mitigating measures where outbreaks cause extensive mortalities [...] Read more.
The UK and Europe have seen successive outbreaks of highly pathogenic avian influenza across the 2020/21 and 2021/22 autumn/winter seasons. Understanding both the epidemiology and transmission of these viruses in different species is critical to aid mitigating measures where outbreaks cause extensive mortalities in both land- and waterfowl. Infection of different species can result in mild or asymptomatic outcomes, or acute infections that result in high morbidity and mortality levels. Definition of disease outcome in different species is of great importance to understanding the role different species play in the maintenance and transmission of these pathogens. Further, the infection of species that have conservation value is also important to recognise and characterise to understand the impact on what might be limited wild populations. Highly pathogenic avian influenza virus H5N1 clade 2.3.4.4b has been detected in great skuas (Stercorarius skua) across different colonies on islands off the shore of Scotland, Great Britain during summer 2021. A large number of great skuas were observed as developing severe clinical disease and dying during the epizootic and mortalities were estimated to be high where monitored. Of eight skuas submitted for post-mortem examination, seven were confirmed as being infected with this virus using a range of diagnostic assays. Here we overview the outbreak event that occurred in this species, listed as species of conservation concern in Great Britain and outline the importance of this finding with respect to virus transmission and maintenance. Full article
(This article belongs to the Special Issue Highly Pathogenic Avian Influenza Virus Emergence)
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18 pages, 1864 KiB  
Article
The Pathobiology of H7N3 Low and High Pathogenicity Avian Influenza Viruses from the United States Outbreak in 2020 Differs between Turkeys and Chickens
by Miriã F. Criado, Christina M. Leyson, Sungsu Youk, Suzanne DeBlois, Tim Olivier, Mary Lea Killian, Mia L. Torchetti, Darren J. Parris, Erica Spackman, Darrell R. Kapczynski, David L. Suarez, David E. Swayne and Mary J. Pantin-Jackwood
Viruses 2021, 13(9), 1851; https://doi.org/10.3390/v13091851 - 16 Sep 2021
Cited by 8 | Viewed by 4161
Abstract
An outbreak caused by H7N3 low pathogenicity avian influenza virus (LPAIV) occurred in commercial turkey farms in the states of North Carolina (NC) and South Carolina (SC), United States in March of 2020. Subsequently, H7N3 high pathogenicity avian influenza virus (HPAIV) was detected [...] Read more.
An outbreak caused by H7N3 low pathogenicity avian influenza virus (LPAIV) occurred in commercial turkey farms in the states of North Carolina (NC) and South Carolina (SC), United States in March of 2020. Subsequently, H7N3 high pathogenicity avian influenza virus (HPAIV) was detected on a turkey farm in SC. The infectivity, transmissibility, and pathogenicity of the H7N3 HPAIV and two LPAIV isolates, including one with a deletion in the neuraminidase (NA) protein stalk, were studied in turkeys and chickens. High infectivity [<2 log10 50% bird infectious dose (BID50)] and transmission to birds exposed by direct contact were observed with the HPAIV in turkeys. In contrast, the HPAIV dose to infect chickens was higher than for turkeys (3.7 log10 BID50), and no transmission was observed. Similarly, higher infectivity (<2–2.5 log10 BID50) and transmissibility were observed with the H7N3 LPAIVs in turkeys compared to chickens, which required higher virus doses to become infected (5.4–5.7 log10 BID50). The LPAIV with the NA stalk deletion was more infectious in turkeys but did not have enhanced infectivity in chickens. These results show clear differences in the pathobiology of AIVs in turkeys and chickens and corroborate the high susceptibility of turkeys to both LPAIV and HPAIV infections. Full article
(This article belongs to the Special Issue Highly Pathogenic Avian Influenza Virus Emergence)
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15 pages, 2746 KiB  
Article
Genetic Characterization of Highly Pathogenic Avian Influenza A(H5N8) Virus in Pakistani Live Bird Markets Reveals Rapid Diversification of Clade 2.3.4.4b Viruses
by Muzaffar Ali, Tahir Yaqub, Muhammad Furqan Shahid, Foong Ying Wong, Nadia Mukhtar, Muhammad Naeem, Pauline Lam, Jayanthi Jayakumar, Gavin J. D. Smith and Yvonne C. F. Su
Viruses 2021, 13(8), 1633; https://doi.org/10.3390/v13081633 - 18 Aug 2021
Cited by 7 | Viewed by 5174
Abstract
The highly pathogenic (HPAI) avian influenza A(H5N1) viruses have undergone reassortment with multiple non-N1-subtype neuraminidase genes since 2008, leading to the emergence of H5Nx viruses. H5Nx viruses established themselves quickly in birds and disseminated from China to Africa, the Middle East, Europe and [...] Read more.
The highly pathogenic (HPAI) avian influenza A(H5N1) viruses have undergone reassortment with multiple non-N1-subtype neuraminidase genes since 2008, leading to the emergence of H5Nx viruses. H5Nx viruses established themselves quickly in birds and disseminated from China to Africa, the Middle East, Europe and North America. Multiple genetic clades have successively evolved through frequent mutations and reassortment, posing a continuous threat to domestic poultry and causing substantial economic losses. Live bird markets are recognized as major sources of avian-to-human infection and for the emergence of zoonotic influenza. In Pakistan, the A(H5N1) virus was first reported in domestic birds in 2007; however, avian influenza surveillance is limited and there is a lack of knowledge on the evolution and transmission of the A(H5) virus in the country. We collected oropharyngeal swabs from domestic poultry and environmental samples from six different live bird markets during 2018–2019. We detected and sequenced HPAI A(H5N8) viruses from two chickens, one quail and one environmental sample in two markets. Temporal phylogenetics indicated that all novel HPAI A(H5N8) viruses belonged to clade 2.3.4.4b, with all eight genes of Pakistan A(H5N8) viruses most closely related to 2017 Saudi Arabia A(H5N8) viruses, which were likely introduced via cross-border transmission from neighboring regions approximately three months prior to virus detection into domestic poultry. Our data further revealed that clade 2.3.4.4b viruses underwent rapid lineage expansion in 2017 and acquired significant amino acid mutations, including mutations associated with increased haemagglutinin affinity to human α-2,6 receptors, prior to the first human A(H5N8) infection in Russian poultry workers in 2020. These results highlight the need for systematic avian influenza surveillance in live bird markets in Pakistan to monitor for potential A(H5Nx) variants that may arise from poultry populations. Full article
(This article belongs to the Special Issue Highly Pathogenic Avian Influenza Virus Emergence)
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Review

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29 pages, 2223 KiB  
Review
Hemagglutinin Subtype Specificity and Mechanisms of Highly Pathogenic Avian Influenza Virus Genesis
by Anja C. M. de Bruin, Mathis Funk, Monique I. Spronken, Alexander P. Gultyaev, Ron A. M. Fouchier and Mathilde Richard
Viruses 2022, 14(7), 1566; https://doi.org/10.3390/v14071566 - 19 Jul 2022
Cited by 22 | Viewed by 5599
Abstract
Highly Pathogenic Avian Influenza Viruses (HPAIVs) arise from low pathogenic precursors following spillover from wild waterfowl into poultry populations. The main virulence determinant of HPAIVs is the presence of a multi-basic cleavage site (MBCS) in the hemagglutinin (HA) glycoprotein. The MBCS allows for [...] Read more.
Highly Pathogenic Avian Influenza Viruses (HPAIVs) arise from low pathogenic precursors following spillover from wild waterfowl into poultry populations. The main virulence determinant of HPAIVs is the presence of a multi-basic cleavage site (MBCS) in the hemagglutinin (HA) glycoprotein. The MBCS allows for HA cleavage and, consequently, activation by ubiquitous proteases, which results in systemic dissemination in terrestrial poultry. Since 1959, 51 independent MBCS acquisition events have been documented, virtually all in HA from the H5 and H7 subtypes. In the present article, data from natural LPAIV to HPAIV conversions and experimental in vitro and in vivo studies were reviewed in order to compile recent advances in understanding HA cleavage efficiency, protease usage, and MBCS acquisition mechanisms. Finally, recent hypotheses that might explain the unique predisposition of the H5 and H7 HA sequences to obtain an MBCS in nature are discussed. Full article
(This article belongs to the Special Issue Highly Pathogenic Avian Influenza Virus Emergence)
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