Advances in Animal Influenza Virus Research: Volume II

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

Deadline for manuscript submissions: closed (20 November 2023) | Viewed by 12665

Special Issue Editors

Virology Department, Istituto Zooprofilattico Sperimentale della Lombardia ed Emilia-Romagna, Via Bianchi 9, 25124 Brescia, Italy
Interests: avian and swine influenza A viruses; influenza D viruses; coronaviruses; suid herpesvirus
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Guest Editor
WOAH Reference Laboratory for Swine Influenza, Istituto Zooprofilattico Sperimentale della Lombardia ed Emilia-Romagna, 25124 Brescia, Italy
Interests: swine influenza; virus NGS sequencing; influenza D virus; influenza A virus
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

In recent years, there has been a significant increase in the number of influenza A virus infections globally in both humans and animals. Recently, the worldwide spread of HPAIV H5 has been of particular concern, involving a large number of domestic and wild avian species and with recent reports of infections in mammals and wild animals. In 2009, there was a new influenza pandemic from a virus of swine origin, and since 2013, there have been several cases of HP and LPAIV H7N9 viruses in poultry, with subsequent transmission to humans in China. Swine influenza viruses are also of great concern due to the frequent occurrence of reassortment events and the high antigenic and genetic variability of the circulating strains, with negative implications for both the pig industry and public health. The ecology of influenza A viruses is very complex and involves a wide range of avian and mammalian host species. Influenza viruses have high mutation rates and are constantly evolving, allowing the virus to adapt rapidly to changes in the host environment, thus crossing the species barrier and leading to the emergence of new viruses with a pandemic potential.

Other influenza B, C and D viruses are also to be considered, and their importance should not be underestimated. Influenza D viruses, discovered only in 2011, were found to be present in cattle, but their ability to infect other species, including humans, is not yet well understood.

The aim of this second volume of the Special Issue is to provide a complete overview of all aspects relating to animal influenza viruses, such as the ecology of infection, epidemiology and populations at risk, pathogenesis, diagnosis, genetic and antigenic characterization of circulating viruses, phylogenetic analyses, and reassortment and spillover events. Human cases of animal influenza viruses are encouraged, and research papers, review articles and short communications are invited.

Dr. Ana Moreno
Dr. Chiara Chiapponi
Guest Editors

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Keywords

  • animal influenza viruses
  • human infections
  • animal infections
  • epidemiology
  • pathogenesis
  • genetic characterization
  • antigenic characterization
  • reassortment events
  • spillover

Published Papers (9 papers)

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Research

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11 pages, 1366 KiB  
Article
The Chinese Hamster Ovary Cell-Based H9 HA Subunit Avian Influenza Vaccine Provides Complete Protection against the H9N2 Virus Challenge in Chickens
by Shunfan Zhu, Zhenyu Nie, Ying Che, Jianhong Shu, Sufang Wu, Yulong He, Youqiang Wu, Hong Qian, Huapeng Feng and Qiang Zhang
Viruses 2024, 16(1), 163; https://doi.org/10.3390/v16010163 - 22 Jan 2024
Viewed by 1242
Abstract
(1) Background: Avian influenza has attracted widespread attention because of its severe effect on the poultry industry and potential threat to human health. The H9N2 subtype of avian influenza viruses was the most prevalent in chickens, and there are several commercial vaccines available [...] Read more.
(1) Background: Avian influenza has attracted widespread attention because of its severe effect on the poultry industry and potential threat to human health. The H9N2 subtype of avian influenza viruses was the most prevalent in chickens, and there are several commercial vaccines available for the prevention of the H9N2 subtype of avian influenza viruses. However, due to the prompt antigenic drift and antigenic shift of influenza viruses, outbreaks of H9N2 viruses still continuously occur, so surveillance and vaccine updates for H9N2 subtype avian influenza viruses are particularly important. (2) Methods: In this study, we constructed a stable Chinese hamster ovary cell line (CHO) to express the H9 hemagglutinin (HA) protein of the major prevalent H9N2 strain A/chicken/Daye/DY0602/2017 with genetic engineering technology, and then a subunit H9 avian influenza vaccine was prepared using the purified HA protein with a water-in-oil adjuvant. (3) Results: The results showed that the HI antibodies significantly increased after vaccination with the H9 subunit vaccine in specific-pathogen-free (SPF) chickens with a dose–dependent potency of the immunized HA protein, and the 50 μg or more per dose HA protein could provide complete protection against the H9N2 virus challenge. (4) Conclusions: These results indicate that the CHO expression system could be a platform used to develop the subunit vaccine against H9 influenza viruses in chickens. Full article
(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Volume II)
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14 pages, 993 KiB  
Article
Pre-Clinical Evaluation of the Antiviral Activity of Epigalocatechin-3-Gallate, a Component of Green Tea, against Influenza A(H1N1)pdm Viruses
by Harry Stannard, Paulina Koszalka, Nikita Deshpande, Yves Desjardins and Mariana Baz
Viruses 2023, 15(12), 2447; https://doi.org/10.3390/v15122447 - 16 Dec 2023
Viewed by 1217
Abstract
Influenza antiviral drugs are important tools in our fight against both annual influenza epidemics and pandemics. Polyphenols are a group of compounds found in plants, some of which have demonstrated promising antiviral activity. Previous in vitro and mouse studies have outlined the anti-influenza [...] Read more.
Influenza antiviral drugs are important tools in our fight against both annual influenza epidemics and pandemics. Polyphenols are a group of compounds found in plants, some of which have demonstrated promising antiviral activity. Previous in vitro and mouse studies have outlined the anti-influenza virus effectiveness of the polyphenol epigallocatechin-3-gallate (EGCG); however, no study has utilised the ferret model, which is considered the gold-standard for influenza antiviral studies. This study aimed to explore the antiviral efficacy of EGCG in vitro and in ferrets. We first performed studies in Madin-Darby Canine Kidney (MDCK) and human lung carcinoma (Calu-3) cells, which demonstrated antiviral activity. In MDCK cells, we observed a selective index (SI, CC50/IC50) of 77 (290 µM/3.8 µM) and 96 (290 µM/3.0 µM) against A/California/07/2009 and A/Victoria/2570/2019 (H1N1)pdm09 influenza virus, respectively. Calu-3 cells demonstrated a SI of 16 (420 µM/26 µM) and 18 (420 µM/24 µM). Ferrets infected with A/California/07/2009 influenza virus and treated with EGCG (500 mg/kg/day for 4 days) had no change in respiratory tissue viral titres, in contrast to oseltamivir treatment, which significantly reduced viral load in the lungs of treated animals. Therefore, we demonstrated that although EGCG showed antiviral activity in vitro against influenza viruses, the drug failed to impair viral replication in the respiratory tract of ferrets. Full article
(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Volume II)
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15 pages, 1946 KiB  
Article
The Mobility of Eurasian Avian-like M2 Is Determined by Residue E79 Which Is Essential for Pathogenicity of 2009 Pandemic H1N1 Influenza Virus in Mice
by Rujuan Wu, Xinyu Zeng, Mingqing Wu, Lixiang Xie, Guanlong Xu, Yaqing Mao, Zhaofei Wang, Yuqiang Cheng, Heng’an Wang, Yaxian Yan, Jianhe Sun and Jingjiao Ma
Viruses 2023, 15(12), 2365; https://doi.org/10.3390/v15122365 - 30 Nov 2023
Viewed by 843
Abstract
In 2009, a novel H1N1 influenza virus caused the first influenza pandemic of the 21st century. Studies have shown that the influenza M gene played important roles in the pathogenicity and transmissibility of the 2009 H1N1 pandemic ((H1N1)pdm09), whilst the underlying mechanism remains [...] Read more.
In 2009, a novel H1N1 influenza virus caused the first influenza pandemic of the 21st century. Studies have shown that the influenza M gene played important roles in the pathogenicity and transmissibility of the 2009 H1N1 pandemic ((H1N1)pdm09), whilst the underlying mechanism remains unclear. The influenza M gene encodes two proteins, matrix protein 1 and matrix protein 2, which play important roles in viral replication and assembly. In this study, it is found that the M2 protein of the (H1N1)pdm09 virus showed a lower mobility rate than the North America triple-reassortant influenza M2 protein in Polyacrylamide Gel Electrophoresis (PAGE). The site-directed mutations of the amino acids of (H1N1)pdm09 M2 revealed that E79 is responsible for the mobility rate change. Further animal studies showed that the (H1N1)pdm09 containing a single M2-E79K was significantly attenuated compared with the wild-type virus in mice and induced lower proinflammatory cytokines and IFNs in mouse lungs. Further in vitro studies indicated that this mutation also affected NLRP3 inflammasome activation. To reveal the reason why they have different mobility rates, a circular dichroism spectra assay was employed and showed that the two M2 proteins displayed different secondary structures. Overall, our findings suggest that M2 E79 is important for the virus replication and pathogenicity of (H1N1)pdm09 through NLRP3 inflammasome and proinflammatory response. Full article
(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Volume II)
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11 pages, 1584 KiB  
Article
Experimental Infection of Chickens with H5N8 High Pathogenicity Avian Influenza Viruses Isolated in Japan in the Winter of 2020–2021
by Saki Sakuma, Taichiro Tanikawa, Ryota Tsunekuni, Junki Mine, Asuka Kumagai, Kohtaro Miyazawa, Yoshihiro Takadate and Yuko Uchida
Viruses 2023, 15(12), 2293; https://doi.org/10.3390/v15122293 - 23 Nov 2023
Viewed by 991
Abstract
During the winter of 2020–2021, numerous outbreaks of high pathogenicity avian influenza (HPAI) were caused by viruses of the subtype H5N8 in poultry over a wide region in Japan. The virus can be divided into five genotypes—E1, E2, E3, E5, and E7. The [...] Read more.
During the winter of 2020–2021, numerous outbreaks of high pathogenicity avian influenza (HPAI) were caused by viruses of the subtype H5N8 in poultry over a wide region in Japan. The virus can be divided into five genotypes—E1, E2, E3, E5, and E7. The major genotype responsible for the outbreaks was E3, followed by E2. To investigate the cause of these outbreaks, we experimentally infected chickens with five representative strains of each genotype. We found that the 50% chicken infectious dose differed by up to 75 times among the five strains, and the titer of the E3 strains (102.75 50% egg infectious dose (EID50)) was the lowest, followed by that of the E2 strains (103.50 EID50). In viral transmission experiments, in addition to the E3 and E2 strains, the E5 strain was transmitted to naïve chickens with high efficiency (>80%), whereas the other strains had low efficiencies (<20%). We observed a clear difference in the virological characteristics among the five strains isolated in the same season. The higher infectivity of the E3 and E2 viruses in chickens may have caused the large number of HPAI outbreaks in Japan during this season. Full article
(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Volume II)
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11 pages, 1287 KiB  
Article
Assessment of Equine Influenza Virus Status in the Republic of Korea from 2020 to 2022
by Seong-In Lim, Min Ji Kim, Min-Ji Kim, Sang-Kyu Lee, Hyoung-Seok Yang, MiJung Kwon, Eui Hyeon Lim, In-Ohk Ouh, Eun-Jung Kim, Bang-Hun Hyun and Yoon-Hee Lee
Viruses 2023, 15(10), 2135; https://doi.org/10.3390/v15102135 - 23 Oct 2023
Viewed by 1147
Abstract
Equine influenza virus (EIV) causes acute respiratory disease in horses and belongs to the influenza A virus family Orthomyxoviridae, genus Orthomyxovirus. This virus may have severe financial implications for the horse industry owing to its highly contagious nature and rapid transmission. [...] Read more.
Equine influenza virus (EIV) causes acute respiratory disease in horses and belongs to the influenza A virus family Orthomyxoviridae, genus Orthomyxovirus. This virus may have severe financial implications for the horse industry owing to its highly contagious nature and rapid transmission. In the Republic of Korea, vaccination against EIV has been practiced with the active involvement of the Korea Racing Authority since 1974. In this study, we monitored the viral RNA for EIV using PCR, as well as the antibody levels against ‘A/equine/South Africa/4/03 (H3N8, clade 1)’, from 2020 to 2022. EIV was not detected using RT-PCR. The seropositivity rates detected using a hemagglutination inhibition assay were 90.3% in 2020, 96.7% in 2021, and 91.8% in 2022. The geometric mean of antibody titer (GMT) was 83.4 in 2020, 135.7 in 2021, and 95.6 in 2022. Yearlings and two-year-olds in training exhibited lower positive rates (59.1% in 2020, 38.9% in 2021, and 44.1% in 2022) than the average. These younger horses may require more attention for vaccination and vaccine responses against EIV. Continuous surveillance of EIV should be performed to monitor the prevalence and spread of this disease. Full article
(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Volume II)
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18 pages, 6521 KiB  
Article
Diversity and Complexity of Internally Deleted Viral Genomes in Influenza A Virus Subpopulations with Enhanced Interferon-Inducing Phenotypes
by Amir Ghorbani, John M. Ngunjiri, Gloria Rendon, Christopher B. Brooke, Scott P. Kenney and Chang-Won Lee
Viruses 2023, 15(10), 2107; https://doi.org/10.3390/v15102107 - 17 Oct 2023
Cited by 2 | Viewed by 1368
Abstract
Influenza A virus (IAV) populations harbor large subpopulations of defective-interfering particles characterized by internally deleted viral genomes. These internally deleted genomes have demonstrated the ability to suppress infectivity and boost innate immunity, rendering them promising for therapeutic and immunogenic applications. In this study, [...] Read more.
Influenza A virus (IAV) populations harbor large subpopulations of defective-interfering particles characterized by internally deleted viral genomes. These internally deleted genomes have demonstrated the ability to suppress infectivity and boost innate immunity, rendering them promising for therapeutic and immunogenic applications. In this study, we aimed to investigate the diversity and complexity of the internally deleted IAV genomes within a panel of plaque-purified avian influenza viruses selected for their enhanced interferon-inducing phenotypes. Our findings unveiled that the abundance and diversity of internally deleted viral genomes were contingent upon the viral subculture and plaque purification processes. We observed a heightened occurrence of internally deleted genomes with distinct junctions in viral clones exhibiting enhanced interferon-inducing phenotypes, accompanied by additional truncation in the nonstructural 1 protein linker region (NS1Δ76-86). Computational analyses suggest the internally deleted IAV genomes can encode a broad range of carboxy-terminally truncated and intrinsically disordered proteins with variable lengths and amino acid composition. Further research is imperative to unravel the underlying mechanisms driving the increased diversity of internal deletions within the genomes of viral clones exhibiting enhanced interferon-inducing capacities and to explore their potential for modulating cellular processes and immunity. Full article
(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Volume II)
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18 pages, 3120 KiB  
Article
Different Outcomes of Chicken Infection with UK-Origin H5N1-2020 and H5N8-2020 High-Pathogenicity Avian Influenza Viruses (Clade 2.3.4.4b)
by Amanda H. Seekings, Caroline J. Warren, Saumya S. Thomas, Fabian Z. X. Lean, David Selden, Benjamin C. Mollett, Pauline M. van Diemen, Ashley C. Banyard and Marek J. Slomka
Viruses 2023, 15(9), 1909; https://doi.org/10.3390/v15091909 - 12 Sep 2023
Cited by 2 | Viewed by 1595
Abstract
Clade 2.3.4.4 H5Nx highly pathogenic avian influenza viruses (HPAIVs) of the “goose/Guangdong” lineage have caused a series of European epizootics since 2014. During autumn/winter 2020–2021, several H5Nx subtypes were detected in the UK, with H5N8 being the dominant subtype in wild birds and [...] Read more.
Clade 2.3.4.4 H5Nx highly pathogenic avian influenza viruses (HPAIVs) of the “goose/Guangdong” lineage have caused a series of European epizootics since 2014. During autumn/winter 2020–2021, several H5Nx subtypes were detected in the UK, with H5N8 being the dominant subtype in wild birds and poultry. Despite the greater subtype diversity (due to viral neuraminidase gene reassortment) reported in wild birds, only H5N8 and H5N1 subtypes caused clade 2.3.4.4 UK HPAIV poultry outbreaks during this period. The direct inoculation of layer chickens showed that H5N8-2020 was more infectious than H5N1-2020, which supported the European H5N8 dominance during that season. However, the mean death time was longer for H5N8-2020 (3.42 days) than for H5N1-2020 (2.17 days). Transmission from directly infected to naive in-contact chickens was inefficient for both subtypes. Histological lesions, the tissue dissemination of viral antigen, and nucleic acid were more extensive and abundant and accumulated more rapidly for H5N1-2020 compared with H5N8-2020. Although inefficient, H5N1-2020 transmission was faster, with its greater virulence indicating that this subtype posed a major concern, as subsequently shown during H5N1 dominance of the clade 2.3.4.4 epizootic since autumn 2021. An evaluation of these in vivo viral characteristics is key to understanding the continuing poultry threats posed by clade 2.3.4.4 H5Nx HPAIVs. Full article
(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Volume II)
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13 pages, 1632 KiB  
Article
Spreading of the High-Pathogenicity Avian Influenza (H5N1) Virus of Clade 2.3.4.4b into Uruguay
by Ana Marandino, Gonzalo Tomás, Yanina Panzera, Carmen Leizagoyen, Ramiro Pérez, Lucía Bassetti, Raúl Negro, Sirley Rodríguez and Ruben Pérez
Viruses 2023, 15(9), 1906; https://doi.org/10.3390/v15091906 - 11 Sep 2023
Cited by 3 | Viewed by 2128
Abstract
Background: Avian influenza viruses (genus Alphainfluenzavirus, family Orthomyxoviridae) infect avian and mammal hosts. In 2022, the high pathogenicity avian influenza virus (H5N1) spread to South America, resulting in the loss of thousands of wild birds, including endangered species, and severely impacting [...] Read more.
Background: Avian influenza viruses (genus Alphainfluenzavirus, family Orthomyxoviridae) infect avian and mammal hosts. In 2022, the high pathogenicity avian influenza virus (H5N1) spread to South America, resulting in the loss of thousands of wild birds, including endangered species, and severely impacting the global poultry industry. Objectives: We analyzed the complete genomes of influenza viruses obtained from wild birds and backyard poultry in Uruguay between February and May 2023. Methods: Twelve complete genomes were obtained in 2023 from cloacal swabs using Illumina sequencing. Genomes were phylogenetically analyzed with regional and global strains. Findings: The identified strains have multiple basic amino acids at the hemagglutinin cleavage sites, which is typical for highly pathogenic strains. The Uruguayan viruses belonged to hemagglutinin clade 2.3.4.4b of the H5N1 subtype. A reassortment in North America has resulted in some segments of South American strains being of Eurasian or North American origins. The Uruguayan viruses shared a common ancestor with South American strains from Argentina and Chile. The influenza viruses displayed a spatiotemporal divergence pattern rather than being host-specific. Main Conclusions: The arrival of the 2.3.4.4b clade in Uruguay may have been mediated by birds that acquired the virus from Argentine and Chilean waterfowl migrating in the Pacific Flyway. Full article
(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Volume II)
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18 pages, 3083 KiB  
Perspective
New Patterns for Highly Pathogenic Avian Influenza and Adjustment of Prevention, Control and Surveillance Strategies: The Example of France
by Axelle Scoizec, Eric Niqueux, Audrey Schmitz, Béatrice Grasland, Loïc Palumbo, Adeline Huneau-Salaün and Sophie Le Bouquin
Viruses 2024, 16(1), 101; https://doi.org/10.3390/v16010101 - 10 Jan 2024
Viewed by 1431
Abstract
From 2020 up to summer 2023, there was a substantial change in the situation concerning the high pathogenic avian influenza (HPAI) virus in Europe. This change concerned mainly virus circulation within wildlife, both in wild birds and wild mammals. It involved the seasonality [...] Read more.
From 2020 up to summer 2023, there was a substantial change in the situation concerning the high pathogenic avian influenza (HPAI) virus in Europe. This change concerned mainly virus circulation within wildlife, both in wild birds and wild mammals. It involved the seasonality of HPAI detections, the species affected, excess mortality events, and the apparent increased level of contamination in wild birds. The knock-on effect concerned new impacts and challenges for the poultry sector, which is affected by repeated annual waves of HPAI arriving with wild migratory birds and by risks due to viral circulation within resident wild birds across the year. Indeed, exceeding expectations, new poultry sectors and production areas have been affected during the recent HPAI seasons in France. The HPAI virus strains involved also generate considerable concern about human health because of enhanced risks of species barrier crossing. In this article, we present these changes in detail, along with the required adjustment of prevention, control, and surveillance strategies, focusing specifically on the situation in France. Full article
(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Volume II)
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