Pathogenesis, Epidemiology, and Control of Animal Influenza Viruses

A special issue of Pathogens (ISSN 2076-0817). This special issue belongs to the section "Viral Pathogens".

Deadline for manuscript submissions: closed (31 August 2024) | Viewed by 11397

Special Issue Editors


E-Mail Website1 Website2
Guest Editor
1. Balik Scientist Program, Department of Science and Technology, Metro Manila, Philippines
2. Southeast Poultry Research Laboratory, Agricultural Research Service, USDA, Athens, GA 30605, USA
Interests: respiratory viruses; influenza virus; virus evolution; next generation sequencing

E-Mail Website
Guest Editor
Department of Population Health, College of Veterinary Medicine, University of Georgia, Athens, GA 30602, USA
Interests: veterinary pathology; pathogenesis; virology; influenza virus

Special Issue Information

Dear Colleagues,

Influenza viruses can be classified into four distinct virus species. Influenza B and C primarily infect humans, whereas influenza A and D viruses can affect non-human animal species. Among influenza viruses, influenza virus A has the broadest host range that includes many species of birds and mammals.

Due to their broad host range, influenza viruses have a significant impact on multiple fields, including agriculture, public health, and wildlife health. To prevent and mitigate the consequences of influenza virus infections, it is imperative to better elucidate their epidemiology and mechanisms of disease progression and to further develop novel strategies for control and treatment in different hosts.

It is our pleasure to announce the launch of this Pathogens Special Issue on the “Pathogenesis, Epidemiology, and Control of Animal Influenza Viruses”. Our focus will be on influenza viruses of non-human animal species, especially those of poultry, swine, and equine; as well as those of wild migratory birds and marine mammals. Approaches that will be considered include classical virology, vaccinology, genomic analysis, case reports, epidemiology, and ecology of animal influenza viruses. Multi-disciplinary research works are especially welcome. Both original research and review articles will be considered for publication.

We look forward to receiving your submissions and to hearing about your exciting research.

Dr. Christina M. Leyson
Dr. Silvia Carnaccini
Guest Editors

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Keywords

  • avian influenza
  • swine influenza
  • equine influenza
  • animal influenza
  • influenza epidemiology
  • pathogenesis
  • influenza vaccines
  • influenza phylogenetics

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Published Papers (8 papers)

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Research

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10 pages, 4026 KiB  
Communication
Molecular Characterization of a Clade 2.3.4.4b H5N1 High Pathogenicity Avian Influenza Virus from a 2022 Outbreak in Layer Chickens in the Philippines
by Zyne Baybay, Andrew Montecillo, Airish Pantua, Milagros Mananggit, Generoso Rene Romo, Jr., Esmeraldo San Pedro, Homer Pantua and Christina Lora Leyson
Pathogens 2024, 13(10), 844; https://doi.org/10.3390/pathogens13100844 - 28 Sep 2024
Viewed by 793
Abstract
H5 subtype high-pathogenicity avian influenza (HPAI) viruses continue to devastate the poultry industry and threaten food security and public health. The first outbreak of H5 HPAI in the Philippines was reported in 2017. Since then, H5 HPAI outbreaks have been reported in 2020, [...] Read more.
H5 subtype high-pathogenicity avian influenza (HPAI) viruses continue to devastate the poultry industry and threaten food security and public health. The first outbreak of H5 HPAI in the Philippines was reported in 2017. Since then, H5 HPAI outbreaks have been reported in 2020, 2022, and 2023. Here, we report the first publicly available complete whole-genome sequence of an H5N1 high-pathogenicity avian influenza virus from a case in Central Luzon. Samples were collected from a flock of layer chickens exhibiting signs of lethargy, droopy wings, and ecchymotic hemorrhages in trachea with excessive mucus exudates. A high mortality rate of 96–100% was observed within the week. Days prior to the high mortality event, migratory birds were observed around the chicken farm. Lungs, spleen, cloacal swabs, and oropharyngeal–tracheal swabs were taken from two chickens from this flock. These samples were positive in quantitative RT-PCR assays for influenza matrix and H5 hemagglutinin (HA) genes. To further characterize the virus, the same samples were subjected to whole-virus-genome amplification and sequencing using the Oxford Nanopore method with mean coverages of 19,190 and 2984, respectively. A phylogenetic analysis of the HA genes revealed that the H5N1 HPAI virus from Central Luzon belongs to the Goose/Guangdong lineage clade 2.3.4.4b viruses. Other segments also have high sequence identity and the same genetic lineages as other clade 2.3.4.4b viruses from Asia. Collectively, these data indicate that wild migratory birds are the likely source of H5N1 viruses from the 2022 outbreaks in the Philippines. Thus, biosecurity practices and surveillance for HPAI viruses in both domestic and wild birds should be increased to prevent and mitigate HPAI outbreaks. Full article
(This article belongs to the Special Issue Pathogenesis, Epidemiology, and Control of Animal Influenza Viruses)
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19 pages, 1470 KiB  
Article
Quantitative Risk Assessment of Wind-Supported Transmission of Highly Pathogenic Avian Influenza Virus to Dutch Poultry Farms via Fecal Particles from Infected Wild Birds in the Environment
by Clazien J. de Vos and Armin R. W. Elbers
Pathogens 2024, 13(7), 571; https://doi.org/10.3390/pathogens13070571 - 8 Jul 2024
Viewed by 1544
Abstract
A quantitative microbial risk assessment model was developed to estimate the probability that the aerosolization of fecal droppings from wild birds in the vicinity of poultry farms would result in the infection of indoor-housed poultry with highly pathogenic avian influenza virus (HPAIv) in [...] Read more.
A quantitative microbial risk assessment model was developed to estimate the probability that the aerosolization of fecal droppings from wild birds in the vicinity of poultry farms would result in the infection of indoor-housed poultry with highly pathogenic avian influenza virus (HPAIv) in the Netherlands. Model input parameters were sourced from the scientific literature and experimental data. The availability of data was diverse across input parameters, and especially parameters on the aerosolization of fecal droppings, survival of HPAIv and dispersal of aerosols were uncertain. Model results indicated that the daily probability of infection of a single poultry farm is very low, with a median value of 7.5 × 10−9. Accounting for the total number of poultry farms and the length of the bird-flu season, the median overall probability of at least one HPAIv-infected poultry farm during the bird-flu season is 2.2 × 10−3 (approximately once every 455 years). This is an overall estimate, averaged over different farm types, virus strains and wild bird species, and results indicate that uncertainty is relatively high. Based on these model results, we conclude that it is unlikely that this introduction route plays an important role in the occurrence of HPAIv outbreaks in indoor-housed poultry. Full article
(This article belongs to the Special Issue Pathogenesis, Epidemiology, and Control of Animal Influenza Viruses)
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15 pages, 5079 KiB  
Article
Infectivity of Wild-Bird Origin Influenza A Viruses in Minnesota Wetlands across Seasons
by Rebecca L. Poulson, Andrew B. Reeves, Christina A. Ahlstrom, Laura C. Scott, Laura E. Hubbard, Alinde Fojtik, Deborah L. Carter, David E. Stallknecht and Andrew M. Ramey
Pathogens 2024, 13(5), 406; https://doi.org/10.3390/pathogens13050406 - 14 May 2024
Viewed by 1263
Abstract
The environmental tenacity of influenza A viruses (IAVs) in the environment likely plays a role in their transmission; IAVs are able to remain infectious in aquatic habitats and may have the capacity to seed outbreaks when susceptible wild bird hosts utilize these same [...] Read more.
The environmental tenacity of influenza A viruses (IAVs) in the environment likely plays a role in their transmission; IAVs are able to remain infectious in aquatic habitats and may have the capacity to seed outbreaks when susceptible wild bird hosts utilize these same environments months or even seasons later. Here, we aimed to assess the persistence of low-pathogenicity IAVs from naturally infected ducks in Northwestern Minnesota through a field experiment. Viral infectivity was measured using replicate samples maintained in distilled water in a laboratory setting as well as in filtered water from four natural water bodies maintained in steel perforated drums (hereafter, mesocosms) within the field from autumn 2020 to spring 2021. There was limited evidence for the extended persistence of IAVs held in mesocosms; from 65 initial IAV-positive samples, only six IAVs persisted to at least 202 days in the mesocosms compared to 17 viruses persisting at least this long when held under temperature-controlled laboratory settings in distilled water. When accounting for the initial titer of samples, viruses detected at a higher concentration at the initiation of the experiment persisted longer than those with a lower starting titer. A parallel experimental laboratory model was used to further explore the effects of water type on viral persistence, and the results supported the finding of reduced tenacity of IAVs held in mesocosms compared to distilled water. The results of this investigation provide evidence that many factors, including temperature and physicochemical properties, impact the duration of viral infectivity in natural settings, further extending our understanding of the potential and limitations of environmental-based methodologies to recover infectious IAVs. Full article
(This article belongs to the Special Issue Pathogenesis, Epidemiology, and Control of Animal Influenza Viruses)
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21 pages, 1517 KiB  
Article
Molecular Characterization of Non-H5 and Non-H7 Avian Influenza Viruses from Non-Mallard Migratory Waterbirds of the North American Flyways, 2006–2011
by Shahan Azeem, John Baroch, Deepanker Tewari, Kristy L. Pabilonia, Mary Killian, Birgit Bradel-Tretheway, Dong Sun, Sara Ghorbani-Nezami and Kyoung-Jin Yoon
Pathogens 2024, 13(4), 333; https://doi.org/10.3390/pathogens13040333 - 17 Apr 2024
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Abstract
The surveillance of migratory waterbirds (MWs) for avian influenza virus (AIV) is indispensable for the early detection of a potential AIV incursion into poultry. Surveying AIV infections and virus subtypes in understudied MW species could elucidate their role in AIV ecology. Oropharyngeal–cloacal (OPC) [...] Read more.
The surveillance of migratory waterbirds (MWs) for avian influenza virus (AIV) is indispensable for the early detection of a potential AIV incursion into poultry. Surveying AIV infections and virus subtypes in understudied MW species could elucidate their role in AIV ecology. Oropharyngeal–cloacal (OPC) swabs were collected from non-mallard MWs between 2006 and 2011. OPC swabs (n = 1158) that molecularly tested positive for AIV (Cts ≤ 32) but tested negative for H5 and H7 subtypes were selected for virus isolation (VI). The selected samples evenly represented birds from all four North American flyways (Pacific, Central, Mississippi, and Atlantic). Eighty-seven low pathogenic AIV isolates, representing 31 sites in 17 states, were recovered from the samples. All isolates belonged to the North American lineage. The samples representing birds from the Central Flyway had the highest VI positive rate (57.5%) compared to those from the other flyways (10.3–17.2%), suggesting that future surveillance can focus on the Central Flyway. Of the isolates, 43.7%, 12.6%, and 10.3% were obtained from blue-winged teal, American wigeon, and American black duck species, respectively. Hatch-year MWs represented the majority of the isolates (70.1%). The most common H and N combinations were H3N8 (23.0%), H4N6 (18.4%), and H4N8 (18.4%). The HA gene between non-mallard and mallard MW isolates during the same time period shared 85.5–99.5% H3 identity and 89.3–99.7% H4 identity. Comparisons between MW (mallard and non-mallard) and poultry H3 and H4 isolates also revealed high similarity (79.0–99.0% and 88.7–98.4%), emphasizing the need for continued AIV surveillance in MWs. Full article
(This article belongs to the Special Issue Pathogenesis, Epidemiology, and Control of Animal Influenza Viruses)
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20 pages, 2778 KiB  
Article
Comparison of the Clinical Manifestation of HPAI H5Nx in Different Poultry Types in the Netherlands, 2014–2022
by Wendy J. Wolters, J. C. M. Vernooij, Thomas M. Spliethof, Jeanine Wiegel, Armin R. W. Elbers, Marcel A. H. Spierenburg, J. Arjan Stegeman and Francisca C. Velkers
Pathogens 2024, 13(4), 280; https://doi.org/10.3390/pathogens13040280 - 26 Mar 2024
Cited by 2 | Viewed by 1868
Abstract
This study describes clinical manifestations of highly pathogenic avian influenza (HPAI) H5N1, H5N8 and H5N6 outbreaks between 2014 and 2018 and 2020 and 2022 in the Netherlands for different poultry types and age groups. Adult duck (breeder) farms and juvenile chicken (broiler and [...] Read more.
This study describes clinical manifestations of highly pathogenic avian influenza (HPAI) H5N1, H5N8 and H5N6 outbreaks between 2014 and 2018 and 2020 and 2022 in the Netherlands for different poultry types and age groups. Adult duck (breeder) farms and juvenile chicken (broiler and laying pullet) farms were not diagnosed before 2020. Outbreaks in ducks decreased in 2020–2022 vs. 2014–2018, but increased for meat-type poultry. Neurological, locomotor and reproductive tract signs were often observed in ducks, whereas laying- and meat-type poultry more often showed mucosal membrane and skin signs, including cyanosis and hemorrhagic conjunctiva. Juveniles (chickens and ducks) showed neurological and locomotor signs more often than adults. Diarrhea occurred more often in adult chickens and juvenile ducks. Mortality increased exponentially within four days before notification in chickens and ducks, with a more fluctuating trend in ducks and meat-type poultry than in layers. For ducks, a mortality ratio (MR) > 3, compared to the average mortality of the previous week, was reached less often than in chickens. A lower percentage of laying flocks with MR > 3 was found for 2020–2022 vs. 2014–2018, but without significant differences in clinical signs. This study provides a basis for improvements in mortality- and clinical-sign-based early warning criteria, especially for juvenile chickens and ducks. Full article
(This article belongs to the Special Issue Pathogenesis, Epidemiology, and Control of Animal Influenza Viruses)
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13 pages, 2409 KiB  
Article
Differing Expression and Potential Immunological Role of C-Type Lectin Receptors of Two Different Chicken Breeds against Low Pathogenic H9N2 Avian Influenza Virus
by Sungsu Youk, Dong-Hun Lee and Chang-Seon Song
Pathogens 2024, 13(1), 95; https://doi.org/10.3390/pathogens13010095 - 22 Jan 2024
Viewed by 1555
Abstract
Diverse immune responses in different chicken lines can result in varying clinical consequences following avian influenza virus (AIV) infection. We compared two widely used layer breeds, Lohmann Brown (LB) and Lohmann White (LW), to examine virus replication and immune responses against H9N2 AIV [...] Read more.
Diverse immune responses in different chicken lines can result in varying clinical consequences following avian influenza virus (AIV) infection. We compared two widely used layer breeds, Lohmann Brown (LB) and Lohmann White (LW), to examine virus replication and immune responses against H9N2 AIV infection. The transcription profile in the spleen of H9N2-infected chickens was compared using a microarray. Confirmatory real-time RT-PCR was used to measure the expression of C-type lectin, OASL, and MX1 genes. Additionally, to investigate the role of chicken lectin receptors in vitro, two C-type lectin receptors (CLRs) were expressed in DF-1 cells, and the early growth of the H9N2 virus was evaluated. The LB chickens shed a lower amount of virus from the cloaca compared with the LW chickens. Different expression levels of C-type lectin-like genes were observed in the transcription profile, with no significant differences in OASL or MX gene expression. Real-time RT-PCR indicated a sharp decrease in C-type lectin levels in the spleen of H9N2-infected LW chickens. In vitro studies demonstrated that cells overexpressing CLR exhibited lower virus replication, while silencing of homeostatic CLR had no effect on AIV replication. This study demonstrated distinct immune responses to H9N2 avian influenza in LB and LW chickens, particularly with differences in C-type lectin expression, potentially leading to lower virus shedding in LB chickens. Full article
(This article belongs to the Special Issue Pathogenesis, Epidemiology, and Control of Animal Influenza Viruses)
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Review

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9 pages, 1531 KiB  
Review
Review of the Highly Pathogenic Avian Influenza in Argentina in 2023: Chronicle of Its Emergence and Control in Poultry
by Ariel E. Vagnozzi
Pathogens 2024, 13(9), 810; https://doi.org/10.3390/pathogens13090810 - 19 Sep 2024
Viewed by 728
Abstract
Highly pathogenic avian influenza (HPAI) is a highly contagious viral disease that represents a significant threat to poultry production worldwide. Variants of the HPAI virus (HPAIV) H5A/Goose/GuangDong/1/96 (H5 Gs/GD/96) lineage have caused five intercontinental epizootic waves, with the most recent, clade 2.3.4.4b, reaching [...] Read more.
Highly pathogenic avian influenza (HPAI) is a highly contagious viral disease that represents a significant threat to poultry production worldwide. Variants of the HPAI virus (HPAIV) H5A/Goose/GuangDong/1/96 (H5 Gs/GD/96) lineage have caused five intercontinental epizootic waves, with the most recent, clade 2.3.4.4b, reaching Argentina in February 2023. Initially detected in wild birds, the virus quickly spread to backyard and commercial poultry farms, leading to economic losses, including the loss of influenza-free status (IFS). By March/April 2023 the epidemic had peaked and vaccination was seriously considered. However, the success of strict stamping-out measures dissuaded the National Animal Health Authority (SENASA) from authorizing any vaccine. Suspected cases sharply declined by May, and the last detection in commercial poultry was reported in June. The effective control and potential eradication of HPAIV in Argentina were due to SENASA’s early detection and rapid response, supported by private companies, veterinarians, and other stakeholders. Stamping-out measures have been effective for virus elimination and reduced farm-to-farm transmission; however, as the virus of this clade may remain present in wild birds, the risk of reintroduction into poultry production is high. Therefore, maintaining continuous active surveillance will be crucial for promptly detecting any new HPAIV incursion and taking appropriate action to contain virus dissemination. Full article
(This article belongs to the Special Issue Pathogenesis, Epidemiology, and Control of Animal Influenza Viruses)
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Other

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32 pages, 838 KiB  
Systematic Review
Mechanistic Models of Influenza Transmission in Commercial Swine Populations: A Systematic Review
by Dana C. Pittman Ratterree, Sapna Chitlapilly Dass and Martial L. Ndeffo-Mbah
Pathogens 2024, 13(9), 746; https://doi.org/10.3390/pathogens13090746 - 31 Aug 2024
Viewed by 970
Abstract
Influenza in commercial swine populations leads to reduced gain in fattening pigs and reproductive issues in sows. This literature review aims to analyze the contributions of mathematical modeling in understanding influenza transmission and control among domestic swine. Twenty-two full-text research articles from seven [...] Read more.
Influenza in commercial swine populations leads to reduced gain in fattening pigs and reproductive issues in sows. This literature review aims to analyze the contributions of mathematical modeling in understanding influenza transmission and control among domestic swine. Twenty-two full-text research articles from seven databases were reviewed, categorized into swine-only (n = 13), swine–avian (n = 3), and swine–human models (n = 6). Strains of influenza models were limited to H1N1 (n = 7) and H3N2 (n = 1), with many studies generalizing the disease as influenza A. Half of the studies (n = 14) considered at least one control strategy, with vaccination being the primary investigated strategy. Vaccination was shown to reduce disease prevalence in single animal cohorts. With a continuous flow of new susceptible animals, such as in farrow-to-finish farms, it was shown that influenza became endemic despite vaccination strategies such as mass or batch-to-batch vaccination. Human vaccination was shown to be effective at mitigating human-to-human influenza transmission and to reduce spillover events from pigs. Current control strategies cannot stop influenza in livestock or prevent viral reassortment in swine, so mechanistic models are crucial for developing and testing new biosecurity measures to prevent future swine pandemics. Full article
(This article belongs to the Special Issue Pathogenesis, Epidemiology, and Control of Animal Influenza Viruses)
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