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Filling Knowledge Gaps: Understanding the Impact of Low Pathogenicity Avian...
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Filling Knowledge Gaps: Understanding the Impact of Low Pathogenicity Avian Influenza Viruses and Their Role in Novel Virus Emergence

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

Deadline for manuscript submissions: closed (30 June 2024) | Viewed by 14383

Special Issue Editors

Dr. Ashley C. Banyard

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Guest Editor
Animal and Plant Health Agency (APHA), Woodham Lane, Weybridge KT15 3NB, UK
Interests: RNA viruses with an emphasis on avian and mammalian influenza viruses; avian paramyxoviruses and pathogens of zoonotic significance
Special Issues, Collections and Topics in MDPI journals
Dr. Joe James

E-Mail Website
Guest Editor
Animal and Plant Health Agency (APHA), Woodham Lane, Weybridge KT15 3NB, Surrey, UK
Interests: avian and mammalian influenza; Newcastle disease virus

Special Issue Information

Dear Colleagues,

Avian influenza viruses (AIVs) are high-consequence pathogens causing globally significant sectorial losses within the poultry industry. AIVs are capable of infection and transmission, irrespective of whether morbidity or mortality is observed, with outcomes of infection likely being linked to host (species susceptibility, age etc.) and viral (virulence factors, infectivity etc.) factors. These viruses circulate freely within wild bird reservoirs, mixing genetic material during coinfection events to drive the emergence of novel reassortants.

Avian influenza virus infection of poultry is categorised as being either high pathogenicity (HP), resulting in high morbidity and mortality rates, or low pathogenicity (LP) where disease outcomes can be minimal. The emergence of influenza A viruses can result from two key activities: genetic drift, whereby mutations can lead to altered species tropism or virulence; and genetic shift whereby coinfection can result in viruses exchanging genetic material to drive the emergence of viruses with dramatically altered genotypes and/or a phenotypes. As such, whilst the majority of information on AIVs in the literature details outbreaks of significant disease events involving HPAIV, the circulation and genetic relevance of LPAIVs is also significant. Importantly, LPAIVs often spread silently, causing either very mild clinical disease or being entirely asymptomatic. As such, they are generally only detected where clinical impact involves measurable parameters such as egg drop or comorbidities. However, silent circulation of LPAIVs may contribute to the emergence of viruses with increased virulence, or, where epizootics of HPAIV occur, may drive the emergence of multiple genotypes of HPAIV with donor genes from LPAIVs, potentially impacting on the clinical outcome. Significant knowledge gaps regarding the circulation and genetic characterisation of these LPAIVs exist. This Special Issue seeks to fill that void by calling for individual case studies where LPAIV infection has impacted upon avian populations, including both the detection and characterisation of LPAIVs and the potential for emergence of HPAIVs from LPAIV progenitors.

Dr. Ashley C. Banyard
Dr. Joe James
Guest Editors

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Keywords

  • avian influenza
  • low pathogenicity
  • high pathogenicity
  • epidemiology
  • reassortants
  • disease emergence

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Published Papers (6 papers)

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Research

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15 pages, 2577 KiB  
Article
Evaluating the Impact of Low-Pathogenicity Avian Influenza H6N1 Outbreaks in United Kingdom and Republic of Ireland Poultry Farms during 2020
by Michael J. McMenamy, Robyn McKenna, Valerie B. Bailie, Ben Cunningham, Adam Jeffers, Kelly McCullough, Catherine Forsythe, Laura Garza Cuartero, Orla Flynn, Christina Byrne, Emily Connaghan, John Moriarty, June Fanning, Stephanie Ronan, Damien Barrett, Alice Fusaro, Isabella Monne, Calogero Terregino, Joe James, Alexander M. P. Byrne, Fabian Z. X. Lean, Alejandro Núñez, Scott M. Reid, Rowena Hansen, Ian H. Brown, Ashley C. Banyard and Ken Lemonadd Show full author list remove Hide full author list
Viruses 2024, 16(7), 1147; https://doi.org/10.3390/v16071147 - 16 Jul 2024
Viewed by 1747
Abstract
In January 2020, increased mortality was reported in a small broiler breeder flock in County Fermanagh, Northern Ireland. Gross pathological findings included coelomitis, oophoritis, salpingitis, visceral gout, splenomegaly, and renomegaly. Clinical presentation included inappetence, pronounced diarrhoea, and increased egg deformation. These signs, in [...] Read more.
In January 2020, increased mortality was reported in a small broiler breeder flock in County Fermanagh, Northern Ireland. Gross pathological findings included coelomitis, oophoritis, salpingitis, visceral gout, splenomegaly, and renomegaly. Clinical presentation included inappetence, pronounced diarrhoea, and increased egg deformation. These signs, in combination with increased mortality, triggered a notifiable avian disease investigation. High pathogenicity avian influenza virus (HPAIV) was not suspected, as mortality levels and clinical signs were not consistent with HPAIV. Laboratory investigation demonstrated the causative agent to be a low-pathogenicity avian influenza virus (LPAIV), subtype H6N1, resulting in an outbreak that affected 15 premises in Northern Ireland. The H6N1 virus was also associated with infection on 13 premises in the Republic of Ireland and six in Great Britain. The close genetic relationship between the viruses in Ireland and Northern Ireland suggested a direct causal link whereas those in Great Britain were associated with exposure to a common ancestral virus. Overall, this rapidly spreading outbreak required the culling of over 2 million birds across the United Kingdom and the Republic of Ireland to stamp out the incursion. This report demonstrates the importance of investigating LPAIV outbreaks promptly, given their substantial economic impacts. Full article
(This article belongs to the Special Issue Filling Knowledge Gaps: Understanding the Impact of Low Pathogenicity Avian Influenza Viruses and Their Role in Novel Virus Emergence)
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24 pages, 25327 KiB  
Article
Avian Influenza Virus and Avian Paramyxoviruses in Wild Waterfowl of the Western Coast of the Caspian Sea (2017–2020)
by Tatyana Murashkina, Kirill Sharshov, Alimurad Gadzhiev, Guy Petherbridge, Anastasiya Derko, Ivan Sobolev, Nikita Dubovitskiy, Arina Loginova, Olga Kurskaya, Nikita Kasianov, Marsel Kabilov, Junki Mine, Yuko Uchida, Ryota Tsunekuni, Takehiko Saito, Alexander Alekseev and Alexander Shestopalov
Viruses 2024, 16(4), 598; https://doi.org/10.3390/v16040598 - 12 Apr 2024
Viewed by 1869
Abstract
The flyways of many different wild waterfowl pass through the Caspian Sea region. The western coast of the middle Caspian Sea is an area with many wetlands, where wintering grounds with large concentrations of birds are located. It is known that wild waterfowl [...] Read more.
The flyways of many different wild waterfowl pass through the Caspian Sea region. The western coast of the middle Caspian Sea is an area with many wetlands, where wintering grounds with large concentrations of birds are located. It is known that wild waterfowl are a natural reservoir of the influenza A virus. In the mid-2000s, in the north of this region, the mass deaths of swans, gulls, and pelicans from high pathogenicity avian influenza virus (HPAIV) were noted. At present, there is still little known about the presence of avian influenza virus (AIVs) and different avian paramyxoviruses (APMVs) in the region’s waterfowl bird populations. Here, we report the results of monitoring these viruses in the wild waterfowl of the western coast of the middle Caspian Sea from 2017 to 2020. Samples from 1438 individuals of 26 bird species of 7 orders were collected, from which 21 strains of AIV were isolated, amounting to a 1.46% isolation rate of the total number of samples analyzed (none of these birds exhibited external signs of disease). The following subtypes were determined and whole-genome nucleotide sequences of the isolated strains were obtained: H1N1 (n = 2), H3N8 (n = 8), H4N6 (n = 2), H7N3 (n = 2), H8N4 (n = 1), H10N5 (n = 1), and H12N5 (n = 1). No high pathogenicity influenza virus H5 subtype was detected. Phylogenetic analysis of AIV genomes did not reveal any specific pattern for viruses in the Caspian Sea region, showing that all segments belong to the Eurasian clades of classic avian-like influenza viruses. We also did not find the amino acid substitutions in the polymerase complex (PA, PB1, and PB2) that are critical for the increase in virulence or adaptation to mammals. In total, 23 hemagglutinating viruses not related to influenza A virus were also isolated, of which 15 belonged to avian paramyxoviruses. We were able to sequence 12 avian paramyxoviruses of three species, as follows: Newcastle disease virus (n = 4); Avian paramyxovirus 4 (n = 5); and Avian paramyxovirus 6 (n = 3). In the Russian Federation, the Newcastle disease virus of the VII.1.1 sub-genotype was first isolated from a wild bird (common pheasant) in the Caspian Sea region. The five avian paramyxovirus 4 isolates obtained belonged to the common clade in Genotype I, whereas phylogenetic analysis of three isolates of Avian paramyxovirus 6 showed that two isolates, isolated in 2017, belonged to Genotype I and that an isolate identified in 2020 belonged to Genotype II. The continued regular monitoring of AIVs and APMVs, the obtaining of data on the biological properties of isolated strains, and the accumulation of information on virus host species will allow for the adequate planning of epidemiological measures, suggest the most likely routes of spread of the virus, and assist in the prediction of the introduction of the viruses in the western coastal region of the middle Caspian Sea. Full article
(This article belongs to the Special Issue Filling Knowledge Gaps: Understanding the Impact of Low Pathogenicity Avian Influenza Viruses and Their Role in Novel Virus Emergence)
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18 pages, 1886 KiB  
Article
First Report of Low Pathogenic Avian Influenza Subtype H9N2 in African Houbara Bustards (Chlamydotis undulata undulata) and Gamebirds in Morocco: Clinico-Pathological Findings, Molecular Characterization, and Associated Coinfections
by Yassmina Bidoudan, Mohamed Mouahid, Ouafaa Fassi Fihri, Enrico Bollo, Oumayma Arbani, Mariette Ducatez, Brahim Banni, Noursaid Tligui and Siham Fellahi
Viruses 2023, 15(12), 2374; https://doi.org/10.3390/v15122374 - 1 Dec 2023
Viewed by 1547
Abstract
We report in this paper the first detection of low pathogenic avian influenza (LPAI) subtype H9N2 in houbara bustards and in gamebirds in Morocco. Starting in 2019, an increase in mortality rates related to respiratory distress was recorded in these species. Necropsy of [...] Read more.
We report in this paper the first detection of low pathogenic avian influenza (LPAI) subtype H9N2 in houbara bustards and in gamebirds in Morocco. Starting in 2019, an increase in mortality rates related to respiratory distress was recorded in these species. Necropsy of the specimens revealed fibrinous sinusitis and tracheitis with intra-bronchial fibrin casts, which are consistent with H9N2 infection in chickens; therefore, implication of the virus in these outbreaks was strongly suspected. Consequently, between January 2020 and June 2023, birds with respiratory signs were necropsied for pathological lesions, tissue samples were examined by histopathology, and samples of trachea, lungs, and cecal tonsils were analyzed using quantitative real-time PCR for the detection of H9N2 virus. In addition, the sequencing of isolates was performed and lastly differential diagnosis with other respiratory pathogens was carried out. During the study period, 93 samples were collected from suspected H9N2 outbreaks, of which 30 tested positive for H9N2 virus: 23 Houbara bustards, 4 partridges, 2 quails, and 1 pheasant. Moreover, sequencing of the HA gene of the virus showed 97.33% nucleotide identity with strains reported previously in broilers in Morocco in 2017 and in 2022. Phylogenetic analysis grouped the Moroccan partridge isolates in the same cluster as viruses isolated in Morocco between 2016 and 2022, Algeria (2017), Burkina Faso (2017), Nigeria (2019), and Togo (2020). Additionally, 10 house sparrows from the premises of these birds were examined for the presence of H9N2 virus, revealing a 30% positivity rate. In conclusion, LPAIV H9N2 is circulating in houbara bustards and gamebirds in Morocco, and house sparrows might be a possible source of the infection. To our knowledge, this is the first report of LPAI H9N2 in the African species of houbara bustards worldwide and in gamebirds in Morocco. Full article
(This article belongs to the Special Issue Filling Knowledge Gaps: Understanding the Impact of Low Pathogenicity Avian Influenza Viruses and Their Role in Novel Virus Emergence)
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16 pages, 2865 KiB  
Article
Low Pathogenic Avian Influenza H9N2 Viruses in Morocco: Antigenic and Molecular Evolution from 2021 to 2023
by Oumayma Arbani, Mariette F. Ducatez, Salma Mahmoudi, Faiçal Salamat, Slimane Khayi, Mohamed Mouahid, Karim M. Selim, Faouzi Kichou, Ikram Ouchhour, Mohammed El Houadfi and Siham Fellahi
Viruses 2023, 15(12), 2355; https://doi.org/10.3390/v15122355 - 30 Nov 2023
Cited by 1 | Viewed by 2018
Abstract
Avian influenza viruses pose significant threats to both the poultry industry and public health worldwide. Among them, the H9N2 subtype has gained substantial attention due to its high prevalence, especially in Asia, the Middle East, and Africa; its ability to reassort with other [...] Read more.
Avian influenza viruses pose significant threats to both the poultry industry and public health worldwide. Among them, the H9N2 subtype has gained substantial attention due to its high prevalence, especially in Asia, the Middle East, and Africa; its ability to reassort with other influenza viruses; and its potential to infect humans. This study presents a comprehensive phylogenetic and molecular analysis of H9N2 avian influenza viruses circulating in Morocco from 2021 to 2023. Through an active epidemiological survey, a total of 1140 samples (trachea and lungs) and oropharyngeal swabs pooled into 283 pools, collected from 205 farms located in 7 regions of Morocco known for having a high density of poultry farms, were analyzed. Various poultry farms were investigated (159 broiler farms, 24 layer farms, 10 breeder farms, and 12 turkey breeder farms). A total of 21 AI H9N2 strains were isolated, and in order to understand the molecular evolution of the H9N2 avian influenza virus, their genetic sequences were determined using the Sanger sequencing technique. Phylogenetic analysis was performed using a dataset comprising global H9N2 sequences to determine the genetic relatedness and evolutionary dynamics of the Moroccan strains. The results revealed the continued circulation and diversification of H9N2 avian influenza viruses in Morocco during the study period. Real-time RT-PCR showed a positivity rate of 35.6% (73/205), with cycle threshold values ranging from 19.2 to 34.9. The phylogenetic analysis indicated that all Moroccan strains belonged to a G1-like lineage and regrouped into two distinct clusters. Our newly detected isolates aggregated distinctly from the genotypes previously isolated in Morocco, North and West Africa, and the Middle East. This indicats the potential of virus evolution resulting from both national circulation and cross-border transmission. A high genetic diversity at both nucleotide and amino-acid levels was observed among all the strains isolated in this study, as compared to H9N2 strains isolated in Morocco since 2016, which suggests the co-circulation of genetically diverse H9N2 variants. Newly discovered mutations were detected in hemagglutinin positions 226, 227, and 193 (H3 numbering), which highlights the genetic evolution of the H9N2 AIVs. These findings contribute to our understanding of the evolution and epidemiology of H9N2 in the region and provide valuable insights for the development of effective prevention and control strategies against this emerging avian influenza subtype. Full article
(This article belongs to the Special Issue Filling Knowledge Gaps: Understanding the Impact of Low Pathogenicity Avian Influenza Viruses and Their Role in Novel Virus Emergence)
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20 pages, 5141 KiB  
Article
Virological and Genetic Characterization of the Unusual Avian Influenza H14Nx Viruses in the Northern Asia
by Nikita Dubovitskiy, Anastasiya Derko, Ivan Sobolev, Elena Prokopyeva, Tatyana Murashkina, Maria Solomatina, Olga Kurskaya, Andrey Komissarov, Artem Fadeev, Daria Danilenko, Polina Petrova, Junki Mine, Ryota Tsunekuni, Yuko Uchida, Takehiko Saito, Alexander Shestopalov and Kirill Sharshov
Viruses 2023, 15(3), 734; https://doi.org/10.3390/v15030734 - 11 Mar 2023
Cited by 1 | Viewed by 2603
Abstract
Wild aquatic birds are generally identified as a natural reservoir of avian influenza viruses (AIVs), where a high diversity of subtypes has been detected. Some AIV subtypes are considered to have relatively low prevalence in wild bird populations. Six-year AIV surveillance in Siberia [...] Read more.
Wild aquatic birds are generally identified as a natural reservoir of avian influenza viruses (AIVs), where a high diversity of subtypes has been detected. Some AIV subtypes are considered to have relatively low prevalence in wild bird populations. Six-year AIV surveillance in Siberia revealed sporadic cases of the rarely identified H14-subtype AIV circulation. Complete genome sequencing of three H14 isolates were performed, and the analysis indicated interconnections between low pathogenic avian influenza (LPAI) viruses. We conducted hemagglutination inhibition and virus neutralization assays, estimated the susceptibility of isolates to neuraminidase inhibitors, and characterized receptor specificity. Our study revealed circulation of a new H14N9 subtype described for the first time. However, the low prevalence of the H14-subtype AIV population may be the reason for the underestimation of the diversity of H14-subtype AIVs. According to the available data, a region in which H14-subtype viruses were detected several times in 2007–2022 in the Eastern Hemisphere is Western Siberia, while the virus was also detected once in South Asia (Pakistan). Phylogenetic analysis of HA segment sequences revealed the circulation of two clades of H14-subtype viruses originated from initial 1980s Eurasian clade; the first was detected in Northern America and the second in Eurasia. Full article
(This article belongs to the Special Issue Filling Knowledge Gaps: Understanding the Impact of Low Pathogenicity Avian Influenza Viruses and Their Role in Novel Virus Emergence)
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Review

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19 pages, 3366 KiB  
Review
Multiple Vaccines and Strategies for Pandemic Preparedness of Avian Influenza Virus
by Hai Xu, Shanyuan Zhu, Roshini Govinden and Hafizah Y. Chenia
Viruses 2023, 15(8), 1694; https://doi.org/10.3390/v15081694 - 4 Aug 2023
Cited by 5 | Viewed by 3427
Abstract
Avian influenza viruses (AIV) are a continuous cause of concern due to their pandemic potential and devasting effects on poultry, birds, and human health. The low pathogenic avian influenza virus has the potential to evolve into a highly pathogenic avian influenza virus, resulting [...] Read more.
Avian influenza viruses (AIV) are a continuous cause of concern due to their pandemic potential and devasting effects on poultry, birds, and human health. The low pathogenic avian influenza virus has the potential to evolve into a highly pathogenic avian influenza virus, resulting in its rapid spread and significant outbreaks in poultry. Over the years, a wide array of traditional and novel strategies has been implemented to prevent the transmission of AIV in poultry. Mass vaccination is still an economical and effective approach to establish immune protection against clinical virus infection. At present, some AIV vaccines have been licensed for large-scale production and use in the poultry industry; however, other new types of AIV vaccines are currently under research and development. In this review, we assess the recent progress surrounding the various types of AIV vaccines, which are based on the classical and next-generation platforms. Additionally, the delivery systems for nucleic acid vaccines are discussed, since these vaccines have attracted significant attention following their significant role in the fight against COVID-19. We also provide a general introduction to the dendritic targeting strategy, which can be used to enhance the immune efficiency of AIV vaccines. This review may be beneficial for the avian influenza research community, providing ideas for the design and development of new AIV vaccines. Full article
(This article belongs to the Special Issue Filling Knowledge Gaps: Understanding the Impact of Low Pathogenicity Avian Influenza Viruses and Their Role in Novel Virus Emergence)
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