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Advances in Animal Influenza Virus Research: Third Edition

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

Deadline for manuscript submissions: 30 January 2025 | Viewed by 17722

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Dr. Ana Moreno

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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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Dr. Chiara Chiapponi

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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. Of particular concern recently has been the worldwide spread of HPAIV H5, 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 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 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 third 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. Reports of human cases of animal influenza viruses are encouraged. 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

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Published Papers (12 papers)

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Research

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15 pages, 4884 KiB

Open AccessArticle

Surveillance for Avian Influenza in Wild Birds in the Lombardy Region (Italy) in the Period 2022–2024

by Tiziana Trogu, Silvia Bellini, Sabrina Canziani, Maya Carrera, Chiara Chiapponi, Mario Chiari, Marco Farioli, Alice Fusaro, Enrico Savegnago, Ambra Nucci, Laura Soliani, Alessio Bortolami, Antonio Lavazza, Calogero Terregino and Ana Moreno

Viruses 2024, 16(11), 1668; https://doi.org/10.3390/v16111668 - 24 Oct 2024

Viewed by 554

Abstract

Influenza A virus (AIV) circulation was investigated in the Lombardy region, during 2022–2024, in wild ducks (through hunting and sampling of faecal samples within natural parks) and wild birds found dead. Samples were analysed through real-time RT-PCRs for Influenza A virus, H5 and H7. Whole genome sequencing was performed on AIV-positive samples. Screening of 3497 hunted Anatidae revealed a total of 184 positive samples. Complete sequencing of 136 samples highlighted the presence of 21 different subtypes ranging from H1N1 to H12N5. The H5N1 HPAIV (high pathogenic AIV) subtype, clade 2.3.4.4b, was the most common during the 2022–2023 winter season (31.8%), while H5 LPAI (low pathogenic AIV) strains were the most prevalent (28.6%) in the 2023–2024 season. The molecular survey on wild birds found dead (n = 481) showed two positive buzzards (14%, 2/14), one grey heron (5.5%, 1/18) and one kestrel (7.6%, 1/13). Regarding the order of Charadriiformes, the dead gulls sampled in 2022 (17 birds) were all negative, whereas 85 out of 167 (51%) individuals were positive in 2023. All positives were caused by an H5N1 HPAIV clade 2.3.4.4b virus belonging to genotype BB. All the faecal samples (1699) received from passive surveillance in nature parks were analysed for AIV with negative results. Full article

(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Third Edition)

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22 pages, 10735 KiB

Open AccessArticle

Phylogenetic Characterization of Novel Reassortant 2.3.4.4b H5N8 Highly Pathogenic Avian Influenza Viruses Isolated from Domestic Ducks in Egypt During the Winter Season 2021–2022

by Noha Saad, Mana Esaki, Isshu Kojima, Ahmed Magdy Khalil, Shiori Osuga, Momtaz A. Shahein, Kosuke Okuya, Makoto Ozawa and Bader Y. Alhatlani

Viruses 2024, 16(11), 1655; https://doi.org/10.3390/v16111655 - 23 Oct 2024

Viewed by 776

Abstract

Avian influenza (AI) is an extremely contagious viral disease of domestic and wild birds that can spread rapidly among bird populations, inducing serious economic losses in the poultry industry. During the winter season 2021–2022, we isolated seventeen highly pathogenic avian influenza (HPAI) H5N8 viruses from outbreaks involving ducks in Egypt, occurring in both backyard and farm settings. The aim of this study was to pinpoint genetic key substitutions (KSs) that could heighten the risk of a human pandemic by influencing the virus’s virulence, replication ability, host specificity, susceptibility to drugs, or transmissibility. To understand their evolution, origin, and potential risks for a human pandemic, whole-genome sequencing and phylogenetic analysis were conducted. Our analysis identified numerous distinctive mutations in the Egyptian H5N8 viruses, suggesting potential enhancements in virulence, resistance to antiviral drugs, and facilitation of transmission in mammals. In this study, at least five genotypes within one genome constellation of H5N8 viruses were identified, raising concerns about the potential emergence of novel viruses with altered characteristics through reassortment between different genotypes and distinct groups. These findings underscore the role of ducks in the virus’s evolutionary process and emphasize the urgent need for enhanced biosecurity measures in domestic duck farms to mitigate pandemic risk. Full article

(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Third Edition)

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14 pages, 391 KiB

Open AccessArticle

Discriminating North American Swine Influenza Viruses with a Portable, One-Step, Triplex Real-Time RT-PCR Assay, and Portable Sequencing

by Marie K. Kirby, Bo Shu, Matthew W. Keller, Malania M. Wilson, Benjamin L. Rambo-Martin, Yunho Jang, Jimma Liddell, Eduardo Salinas Duron, Jacqueline M. Nolting, Andrew S. Bowman, C. Todd Davis, David E. Wentworth and John R. Barnes

Viruses 2024, 16(10), 1557; https://doi.org/10.3390/v16101557 - 30 Sep 2024

Viewed by 590

Abstract

Swine harbors a genetically diverse population of swine influenza A viruses (IAV-S), with demonstrated potential to transmit to the human population, causing outbreaks and pandemics. Here, we describe the development of a one-step, triplex real-time reverse transcription-polymerase chain reaction (rRT-PCR) assay that detects and distinguishes the majority of the antigenically distinct influenza A virus hemagglutinin (HA) clades currently circulating in North American swine, including the IAV-S H1 1A.1 (α), 1A.2 (β), 1A.3 (γ), 1B.2.2 (δ1) and 1B.2.1 (δ2) clades, and the IAV-S H3 2010.1 clade. We performed an in-field test at an exhibition swine show using in-field viral concentration and RNA extraction methodologies and a portable real-time PCR instrument, and rapidly identified three distinct IAV-S clades circulating within the N.A. swine population. Portable sequencing is used to further confirm the results of the in-field test of the swine triplex assay. The IAV-S triplex rRT-PCR assay can be easily transported and used in-field to characterize circulating IAV-S clades in North America, allowing for surveillance and early detection of North American IAV-S with human outbreak and pandemic potential. Full article

(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Third Edition)

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12 pages, 1425 KiB

Open AccessArticle

Comparison of Extraction Methods for the Detection of Avian Influenza Virus RNA in Cattle Milk

by Chantal J. Snoeck, Aurélie Sausy, Manon Bourg and Judith M. Hübschen

Viruses 2024, 16(9), 1442; https://doi.org/10.3390/v16091442 - 10 Sep 2024

Viewed by 930

Abstract

Since early 2024, a multistate outbreak of highly pathogenic avian influenza H5N1 has been affecting dairy cattle in the USA. The influenza viral RNA concentrations in milk make it an ideal matrix for surveillance purposes. However, viral RNA detection in multi-component fluids such as milk can be complex, and optimization of influenza detection methods is thus required. Raw bulk tank milk and mastitis milk samples were artificially contaminated with an avian influenza strain and subjected to five extraction methods. HCoV-229E and synthetic RNA were included as exogenous internal process controls. Given the high viral load usually observed in individual raw milk samples, four out of five tested methods would enable influenza detection in milk with normal texture, over a time window of at least 2 weeks post-onset of clinical signs. Nevertheless, sample dilution 1:3 in molecular transport medium prior to RNA extraction provided the best results for dilution of inhibitory substances and a good recovery rate of influenza RNA, that reached 12.5 ± 1.2% and 10.4 ± 3.8% in two independent experiments in bulk milk and 11.2 ± 3.6% and 10.0 ± 2.9% on two cohorts of mastitis milk samples. We have also shown compatibility of an influenza RT-qPCR system with synthetic RNA detection for simultaneous validation of the RNA extraction and RT-qPCR processes. Full article

(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Third Edition)

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9 pages, 903 KiB

Open AccessArticle

Detection and Monitoring of Highly Pathogenic Influenza A Virus 2.3.4.4b Outbreak in Dairy Cattle in the United States

by Luis G. Giménez-Lirola, Brooklyn Cauwels, Juan Carlos Mora-Díaz, Ronaldo Magtoto, Jesús Hernández, Maritza Cordero-Ortiz, Rahul K. Nelli, Patrick J. Gorden, Drew R. Magstadt and David H. Baum

Viruses 2024, 16(9), 1376; https://doi.org/10.3390/v16091376 - 29 Aug 2024

Viewed by 1447

Abstract

The emergence and spread of highly pathogenic avian influenza virus A subtype H5N1 (HP H5N1-IAV), particularly clade H5N1 2.3.4.4b, pose a severe global health threat, affecting various species, including mammals. Historically, cattle have been considered less susceptible to IAV, but recent outbreaks of H5N1-IAV 2.3.4.4b in dairy farms suggest a shift in host tropism, underscoring the urgency of expanded surveillance and the need for adaptable diagnostic tools in outbreak management. This study investigated the presence of anti-nucleoprotein (NP) antibodies in serum and milk and viral RNA in milk on dairy farms affected by outbreaks in Texas, Kansas, and Michigan using a multi-species IAV ELISA and RT-qPCR. The analysis of ELISA results from a Michigan dairy farm outbreak demonstrated a positive correlation between paired serum and milk sample results, confirming the reliability of both specimen types. Our findings also revealed high diagnostic performance during the convalescent phase (up to 96%), further improving sensitivity through serial sampling. Additionally, the evaluation of diagnostic specificity using serum and milk samples from IAV-free farms showed an excellent performance (99.6%). This study underscores the efficacy of the IAV NP-blocking ELISA for detecting and monitoring H5N1-IAV 2.3.4.4b circulation in dairy farms, whose recent emergence raises significant animal welfare and zoonotic concerns, necessitating expanded surveillance efforts. Full article

(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Third Edition)

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22 pages, 4569 KiB

Open AccessArticle

Spontaneous Lethal Outbreak of Influenza A Virus Infection in Vaccinated Sows on Two Farms Suggesting the Occurrence of Vaccine-Associated Enhanced Respiratory Disease with Eosinophilic Lung Pathology

by Wencke Reineking, Isabel Hennig-Pauka, Ludger Schröder, Ulf Höner, Elena Schreiber, Lukas Geiping, Simon Lassnig, Marta C. Bonilla, Marion Hewicker-Trautwein and Nicole de Buhr

Viruses 2024, 16(6), 955; https://doi.org/10.3390/v16060955 - 13 Jun 2024

Viewed by 1327

Abstract

Influenza A virus (IAV) infections in swine are usually subclinical, but they can reach high morbidity rates. The mortality rate is normally low. In this study, six vaccinated, spontaneously deceased sows revealed IAV infection and enhanced neutrophilic bronchopneumonia with unexpectedly large numbers of infiltrating eosinophils. The purpose of this study was to characterize these lung lesions with special emphasis on the phenotypes of inflammatory cells, the presence of eosinophilic peroxidase (EPO), and neutrophil extracellular traps (NETs). The number of Sirius red-stained eosinophils was significantly higher in the lungs of IAV-infected sows compared to healthy pigs, indicating a migration of eosinophils from blood vessels into the lung tissue stimulated by IAV infection. The detection of intra- and extracellular EPO in the lungs suggests its contribution to pulmonary damage. The presence of CD3⁺ T lymphocytes, CD20⁺ B lymphocytes, and Iba-1⁺ macrophages indicates the involvement of cell-mediated immune responses in disease progression. Furthermore, high numbers of myeloperoxidase-positive cells were detected. However, DNA-histone-1 complexes were reduced in IAV-infected sows, leading to the hypothesis that NETs are not formed in the IAV-infected sows. In conclusion, our findings in the lungs of IAV-infected vaccinated sows suggest the presence of so far unreported field cases of vaccine-associated enhanced respiratory disease. Full article

(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Third Edition)

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17 pages, 802 KiB

Open AccessArticle

Detection and Characterization of Influenza A Virus Endemic Circulation in Suckling and Nursery Pigs Originating from Vaccinated Farms in the Same Production System

by Alessandra Silva Dias, Amy L. Vincent Baker, Rodney B. Baker, Jianqiang Zhang, Michael A. Zeller, Pravina Kitikoon and Phillip C. Gauger

Viruses 2024, 16(4), 626; https://doi.org/10.3390/v16040626 - 18 Apr 2024

Viewed by 1597

Abstract

Inactivated influenza A virus (IAV) vaccines help reduce clinical disease in suckling piglets, although endemic infections still exist. The objective of this study was to evaluate the detection of IAV in suckling and nursery piglets from IAV-vaccinated sows from farms with endemic IAV infections. Eight nasal swab collections were obtained from 135 two-week-old suckling piglets from four farms every other week from March to September 2013. Oral fluid samples were collected from the same group of nursery piglets. IAV RNA was detected in 1.64% and 31.01% of individual nasal swabs and oral fluids, respectively. H1N2 was detected most often, with sporadic detection of H1N1 and H3N2. Whole-genome sequences of IAV isolated from suckling piglets revealed an H1 hemagglutinin (HA) from the 1B.2.2.2 clade and N2 neuraminidase (NA) from the 2002A clade. The internal gene constellation of the endemic H1N2 was TTTTPT with a pandemic lineage matrix. The HA gene had 97.59% and 97.52% nucleotide and amino acid identities, respectively, to the H1 1B.2.2.2 used in the farm-specific vaccine. A similar H1 1B.2.2.2 was detected in the downstream nursery. These data demonstrate the low frequency of IAV detection in suckling piglets and downstream nurseries from farms with endemic infections in spite of using farm-specific IAV vaccines in sows. Full article

(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Third Edition)

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14 pages, 1106 KiB

Open AccessArticle

In Ovo Models to Predict Virulence of Highly Pathogenic Avian Influenza H5-Viruses for Chickens and Ducks

by Luca Bordes, José L. Gonzales, Sandra Vreman, Sandra Venema, Nadia Portier, Evelien A. Germeraad, Wim H. M. van der Poel and Nancy Beerens

Viruses 2024, 16(4), 563; https://doi.org/10.3390/v16040563 - 4 Apr 2024

Viewed by 1415

Abstract

Highly pathogenic avian influenza (HPAI) H5-viruses are circulating in wild birds and are repeatedly introduced to poultry causing outbreaks in the Netherlands since 2014. The largest epizootic ever recorded in Europe was caused by HPAI H5N1 clade 2.3.4.4b viruses in the period 2021–2022. The recent H5-clade 2.3.4.4 viruses were found to differ in their virulence for chickens and ducks. Viruses causing only mild disease may remain undetected, increasing the risk of virus spread to other farms, wild birds and mammals. We developed in ovo models to determine the virulence of HPAI viruses for chickens and ducks, which are fast and have low costs. The virulence of five contemporary H5-viruses was compared studying replication rate, average time to death and virus spread in the embryo. Remarkable differences in virulence were observed between H5-viruses and between poultry species. The H5N1-2021 virus was found to have a fast replication rate in both the chicken and duck in ovo models, but a slower systemic virus dissemination compared to three other H5-clade 2.3.4.4b viruses. The results show the potential of in ovo models to quickly determine the virulence of novel HPAI viruses, and study potential virulence factors which can help to better guide the surveillance in poultry. Full article

(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Third Edition)

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17 pages, 6911 KiB

Open AccessArticle

Proteomic and Lipidomic Profiling of Calves Experimentally Co-Infected with Influenza D Virus and Mycoplasma bovis: Insights into the Host–Pathogen Interactions

by Ignacio Alvarez, Mariette Ducatez, Yongzhi Guo, Adrien Lion, Anna Widgren, Marc Dubourdeau, Vincent Baillif, Laure Saias, Siamak Zohari, Jonas Bergquist, Gilles Meyer, Jean-Francois Valarcher and Sara Hägglund

Viruses 2024, 16(3), 361; https://doi.org/10.3390/v16030361 - 27 Feb 2024

Cited by 3 | Viewed by 1425

Abstract

The role of Influenza D virus (IDV) in bovine respiratory disease remains unclear. An in vivo experiment resulted in increased clinical signs, lesions, and pathogen replication in calves co-infected with IDV and Mycoplasma bovis (M. bovis), compared to single-infected calves. The present study aimed to elucidate the host–pathogen interactions and profile the kinetics of lipid mediators in the airways of these calves. Bronchoalveolar lavage (BAL) samples collected at 2 days post-infection (dpi) were used for proteomic analyses by liquid chromatography-tandem mass spectrometry (LC-MS/MS). Additionally, lipidomic analyses were performed by LC-MS/MS on BAL samples collected at 2, 7 and 14 dpi. Whereas M. bovis induced the expression of proteins involved in fibrin formation, IDV co-infection counteracted this coagulation mechanism and downregulated other acute-phase response proteins, such as complement component 4 (C4) and plasminogen (PLG). The reduced inflammatory response against M. bovis likely resulted in increased M. bovis replication and delayed M. bovis clearance, which led to a significantly increased abundance of oxylipids in co-infected calves. The identified induced oxylipids mainly derived from arachidonic acid; were likely oxidized by COX-1, COX-2, and LOX-5; and peaked at 7 dpi. This paper presents the first characterization of BAL proteome and lipid mediator kinetics in response to IDV and M. bovis infection in cattle and raises hypotheses regarding how IDV acts as a co-pathogen in bovine respiratory disease. Full article

(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Third Edition)

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Review

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14 pages, 1005 KiB

Open AccessReview

Exploring Potential Intermediates in the Cross-Species Transmission of Influenza A Virus to Humans

by Chung-Young Lee

Viruses 2024, 16(7), 1129; https://doi.org/10.3390/v16071129 - 14 Jul 2024

Viewed by 1879

Abstract

The influenza A virus (IAV) has been a major cause of several pandemics, underscoring the importance of elucidating its transmission dynamics. This review investigates potential intermediate hosts in the cross-species transmission of IAV to humans, focusing on the factors that facilitate zoonotic events. We evaluate the roles of various animal hosts, including pigs, galliformes, companion animals, minks, marine mammals, and other animals, in the spread of IAV to humans. Full article

(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Third Edition)

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14 pages, 565 KiB

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Role of miRNA in Highly Pathogenic H5 Avian Influenza Virus Infection: An Emphasis on Cellular and Chicken Models

by Dibakar Chowdhury, Md. Nayeem, Hillary A. Vanderven and Subir Sarker

Viruses 2024, 16(7), 1102; https://doi.org/10.3390/v16071102 - 9 Jul 2024

Cited by 2 | Viewed by 1499

Abstract

The avian influenza virus, particularly the H5N1 strain, poses a significant and ongoing threat to both human and animal health. Recent outbreaks have affected domestic and wild birds on a massive scale, raising concerns about the virus’ spread to mammals. This review focuses on the critical role of microRNAs (miRNAs) in modulating pro-inflammatory signaling pathways during the pathogenesis of influenza A virus (IAV), with an emphasis on highly pathogenic avian influenza (HPAI) H5 viral infections. Current research indicates that miRNAs play a significant role in HPAI H5 infections, influencing various aspects of the disease process. This review aims to synthesize recent findings on the impact of different miRNAs on immune function, viral cytopathogenicity, and respiratory viral replication. Understanding these mechanisms is essential for developing new therapeutic strategies to combat avian influenza and mitigate its effects on both human and animal populations. Full article

(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Third Edition)

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Other

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7 pages, 688 KiB

Open AccessCase Report

Natural Infection with Highly Pathogenic Avian Influenza A/H5N1 Virus in Pet Ferrets

by Anna Golke, Dawid Jańczak, Olga Szaluś-Jordanow, Tomasz Dzieciątkowski, Rafał Sapierzyński, Agata Moroz-Fik, Marcin Mickiewicz and Tadeusz Frymus

Viruses 2024, 16(6), 931; https://doi.org/10.3390/v16060931 - 8 Jun 2024

Cited by 3 | Viewed by 3198

Abstract

The study involved five ferrets from one household in Poland, comprising three sick 9-week-old juveniles, their healthy mother, and another clinically normal adult, admitted to the veterinary clinic in June 2023. The juvenile ferrets displayed significant lethargy and a pronounced unwillingness to move with accompanying pulmonary distress. Prompted by concurrent outbreaks of A/H5N1 influenza virus infections in Polish cats, point-of-care tests were conducted that revealed type A influenza antigens in the throat swabs of all five ferrets. Despite treatment, one juvenile ferret exhibited dyspnea and neurological symptoms and eventually died. The two remaining ferrets recovered fully, including one severely affected showing persistent dyspnea and incoordination without fever that recovered after 11 days of treatment. In the RT-qPCR, the throat swabs collected from all surviving ferrets as well as the samples of lungs, trachea, heart, brain, pancreas, liver, and intestine of the succumbed ferret were found positive for A/H5N1 virus RNA. To our best knowledge, this is the first documented natural A/H5N1 avian influenza in domestic ferrets kept as pets. In addition, this outbreak suggests the possibility of asymptomatic A/H5N1 virus shedding by ferrets, highlighting their zoonotic potential and the advisability of excluding fresh or frozen poultry from their diet to reduce the A/H5N1 virus transmission risks. Full article

(This article belongs to the Special Issue Advances in Animal Influenza Virus Research: Third Edition)

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