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Microorganisms
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Ecology of Influenza A Viruses
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Ecology of Influenza A Viruses

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Virology".

Deadline for manuscript submissions: closed (30 June 2022) | Viewed by 14881

Special Issue Editors

Dr. Maria Alessandra De Marco

E-Mail Website
Guest Editor
Institute for Enviromental Protection and Research (ISPRA), Ozzano dell’Emilia, BO, Italy
Interests: influenza virus ecology; emerging coronaviruses; zoonoses; wildlife infectious diseases; wildlife conservation
Special Issues, Collections and Topics in MDPI journals
Dr. Claudia Cotti

E-Mail Website
Guest Editor
Department of Veterinary Medical Sciences, University of Bologna, Ozzano Emilia, BO, Italy
Interests: ecology; invasive species; wildlife infectious diseases; viral laboratory diagnosis
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear colleagues,

Wild aquatic birds represent the major natural reservoir of the influenza A virus (IAV) gene pool from which novel IAVs can emerge to infect other avian and mammalian species, humans included. From an ecological point of view, IAVs are natural components of wetland ecosystems in which they occupy trophic niches represented by susceptible hosts while interacting with other biotic and environmental components. However, ecosystem interactions underlie possible bidirectional viral flows between natural and anthropogenic habitats.

It has long been known that natural avian reservoirs enable the perpetuation of low-pathogenic avian influenza viruses (LPAIVs) that, in poultry, can occasionally evolve into highly pathogenic (HP) strains, posing a risk for animal and public health. Nevertheless, in recent years, a new scenario has emerged with the increasing potential involvement of wild birds in HP avian influenza caused by H5 subtype circulation and long-distance spread by migratory populations. Many unanswered questions remain in relation to this scenario.

The aim of this Special Issue is to provide a multidisciplinary collection of original research, communication and review articles related to IAV ecology and evolutionary adaptation to natural reservoir and spillover hosts in the context of the current climatic and anthropogenic system change. Manuscripts covering all aspects of research relating to IAV–host–environment interactions are of interest, including work from surveillance and research activities based on molecular, virological and serological findings.

Dr. Maria Alessandra De Marco
Dr. Claudia Cotti
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Microorganisms is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • Influenza A Virus
  • ecology
  • ecological interfaces
  • virus–host–environment interactions
  • wild aquatic birds
  • reservoir hosts
  • spillover hosts
  • migratory birds
  • LPAIV
  • HPAIV

Published Papers (7 papers)

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Editorial

Jump to: Research

4 pages, 207 KiB  
Editorial
Special Issue “Ecology of Influenza A Viruses”: Editorial
by Maria Alessandra De Marco, Mauro Delogu and Claudia Cotti
Microorganisms 2023, 11(5), 1287; https://doi.org/10.3390/microorganisms11051287 - 15 May 2023
Viewed by 1024
Abstract
Wild aquatic birds constitute the main natural reservoir of the influenza A virus (IAV) gene pool, from which novel IAVs can emerge to infect other animals including avian and mammalian species [...] Full article
(This article belongs to the Special Issue Ecology of Influenza A Viruses)

Research

Jump to: Editorial

15 pages, 2243 KiB  
Article
Long-Term Serological Investigations of Influenza A Virus in Free-Living Wild Boars (Sus scrofa) from Northern Italy (2007–2014)
by Maria Alessandra De Marco, Claudia Cotti, Elisabetta Raffini, Matteo Frasnelli, Alice Prosperi, Irene Zanni, Chiara Romanini, Maria Rita Castrucci, Chiara Chiapponi and Mauro Delogu
Microorganisms 2022, 10(9), 1768; https://doi.org/10.3390/microorganisms10091768 - 01 Sep 2022
Cited by 2 | Viewed by 1370
Abstract
Influenza A viruses (IAV) have been repeatedly demonstrated to circulate in wild suid populations. In this study, serum samples were collected from 2618 free-ranging wild boars in a protected area of Northern Italy between 2007 and 2014, and firstly screened by enzyme-linked immunosorbent [...] Read more.
Influenza A viruses (IAV) have been repeatedly demonstrated to circulate in wild suid populations. In this study, serum samples were collected from 2618 free-ranging wild boars in a protected area of Northern Italy between 2007 and 2014, and firstly screened by enzyme-linked immunosorbent assay (ELISA) for the presence of antibodies against IAV. The ELISA-positive samples were further tested by hemagglutination inhibition (HI) assays performed using antigen strains representative of the four major swine IAV (sIAV) lineages circulating in Italy: avian-like swine H1N1, pandemic-like swine H1N1, human-like swine H1N2 and human-like swine H3N2. An overall seroprevalence of 5.5% (145/2618) was detected by ELISA, with 56.7% (80/141) of screened sera tests positive by HI assay. Antibodies against H1N1 subtypes were the most prevalent beginning in 2009—with the highest detection in the first quarter of the year—until 2013, although at a low level. In addition, antibodies to H3N2 subtype were found during six years (2007, 2009, 2010, 2011, 2012 and 2014) whereas H1N2 antibodies were detected in 2012 only. Of the HI-positive samples, 30% showed reactivity to both H1N1 and H3N2 subtypes. These results provide additional insight into the circulation dynamics of IAV in wild suid populations, suggesting the occurrence of sIAV spillover events from pigs to wild boars. Full article
(This article belongs to the Special Issue Ecology of Influenza A Viruses)
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9 pages, 636 KiB  
Article
Avian Influenza Virus Status and Maternal Antibodies in Nestling White Ibis (Eudocimus albus)
by Katherine F. Christie, Rebecca L. Poulson, Julia Silva Seixas and Sonia M. Hernandez
Microorganisms 2021, 9(12), 2468; https://doi.org/10.3390/microorganisms9122468 - 30 Nov 2021
Cited by 5 | Viewed by 1624
Abstract
The White Ibis (Eudocimus albus), a nomadic wading bird, has increased its exploitation of urban habitats in South Florida, United States, and has recently established several urban breeding colonies. Certain characteristics of ibis ecology could position them in the natural cycle [...] Read more.
The White Ibis (Eudocimus albus), a nomadic wading bird, has increased its exploitation of urban habitats in South Florida, United States, and has recently established several urban breeding colonies. Certain characteristics of ibis ecology could position them in the natural cycle of the avian influenza virus (AIV). In fact, experimentally infected ibises were shown to be competent hosts for multiple AIV subtypes, and seroconversion to AIV has been documented in adult ibises in natural populations. However, the mechanisms of transmission and the timing of infection are unclear as we have yet to isolate AIV from a free-living ibis. To investigate the age-specific AIV dynamics of ibis, we captured nestlings (n = 115) weekly for 1–4 weeks from urban and natural settings in 2020 and 2021. We collected choanal/cloacal swabs for rRT-PCR and virus isolation, and plasma to screen for maternal AIV antibodies. AIV was not detected in any individual by virus isolation; however, maternal antibodies to AIV were detected in 95% of nestlings, with varying rates of catabolism. These results confirm that nestlings are afforded maternal antibodies from adults at rates reflective of higher adult seroprevalence than previously documented and that nestlings in breeding colonies may have some degree of protection and are unlikely to become infected with AIV. Full article
(This article belongs to the Special Issue Ecology of Influenza A Viruses)
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22 pages, 8591 KiB  
Article
Active Surveillance for Highly Pathogenic Avian Influenza Viruses in Wintering Waterbirds in Northeast Italy, 2020–2021
by Federica Gobbo, Diletta Fornasiero, Maria Alessandra De Marco, Bianca Zecchin, Paolo Mulatti, Mauro Delogu and Calogero Terregino
Microorganisms 2021, 9(11), 2188; https://doi.org/10.3390/microorganisms9112188 - 20 Oct 2021
Cited by 18 | Viewed by 2514
Abstract
The increasing involvement of wild waterfowl in H5 Highly Pathogenic Avian Influenza Virus (HPAIV) circulation continues to pose a threat to animal and public health worldwide. In winter 2020–2021, two field surveillance activities were carried out on a weekly basis, through virological and [...] Read more.
The increasing involvement of wild waterfowl in H5 Highly Pathogenic Avian Influenza Virus (HPAIV) circulation continues to pose a threat to animal and public health worldwide. In winter 2020–2021, two field surveillance activities were carried out on a weekly basis, through virological and serological analyses, in 823 hunted and 521 trapped migratory aquatic birds in northeast Italy. Sixty Eurasian teals were recaptured several times, which allowed us to follow the progression of the HPAI H5 infection in naturally infected wild waterfowl. Oropharyngeal, cloacal, and feather swabs (OS, CS and FS) were collected from each duck and tested by real time rRT-PCR Type A influenza. The identified viruses were characterized and pathotyped by sequencing. Several viruses belonging to three different HPAI H5 subtypes were detected: H5N8, H5N5, and H5N1. High prevalence of infection with HPAI H5 clade 2.3.4.4b during November–December 2020 (up to 27.1%) was observed in captured Eurasian teals, while infection rates in hunted dabbling ducks, mainly Eurasian wigeons, showed the highest prevalence of infection in November 2020 (8.9%) and January 2021 (10.2%). All HPAI positive birds were also clinically healthy when recaptured weeks apart. The OS and FS showed the highest detection efficiency of HPAIV. Our results highlight that HPAI passive surveillance should be complemented by a targeted active surveillance to more efficiently detect novel HPAI viruses. Full article
(This article belongs to the Special Issue Ecology of Influenza A Viruses)
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18 pages, 1072 KiB  
Article
Serologic Evidence of Occupational Exposure to Avian Influenza Viruses at the Wildfowl/Poultry/Human Interface
by Maria Alessandra De Marco, Mauro Delogu, Marzia Facchini, Livia Di Trani, Arianna Boni, Claudia Cotti, Giulia Graziosi, Diana Venturini, Denise Regazzi, Valentina Ravaioli, Fausto Marzadori, Matteo Frasnelli, Maria Rita Castrucci and Elisabetta Raffini
Microorganisms 2021, 9(10), 2153; https://doi.org/10.3390/microorganisms9102153 - 15 Oct 2021
Cited by 10 | Viewed by 2188
Abstract
Ecological interactions between wild aquatic birds and outdoor-housed poultry can enhance spillover events of avian influenza viruses (AIVs) from wild reservoirs to domestic birds, thus increasing the related zoonotic risk to occupationally exposed workers. To assess serological evidence of AIV infection in workers [...] Read more.
Ecological interactions between wild aquatic birds and outdoor-housed poultry can enhance spillover events of avian influenza viruses (AIVs) from wild reservoirs to domestic birds, thus increasing the related zoonotic risk to occupationally exposed workers. To assess serological evidence of AIV infection in workers operating in Northern Italy at the wildfowl/poultry interface or directly exposed to wildfowl, serum samples were collected between April 2005 and November 2006 from 57 bird-exposed workers (BEWs) and from 7 unexposed controls (Cs), planning three sample collections from each individual. Concurrently, AIV surveillance of 3587 reared birds identified 4 AIVs belonging to H10N7, H4N6 and H2N2 subtypes while serological analysis by hemagglutination inhibition (HI) assay showed recent infections caused by H1, H2, H4, H6, H10, H11, H12, and H13 subtypes. Human sera were analyzed for specific antibodies against AIVs belonging to antigenic subtypes from H1 to H14 by using HI and virus microneutralization (MN) assays as a screening and a confirmatory test, respectively. Overall, antibodies specific to AIV-H3, AIV-H6, AIV-H8, and AIV-H9 were found in three poultry workers (PWs) and seropositivity to AIV-11, AIV-H13—still detectable in October 2017—in one wildlife professional (WP). Furthermore, seropositivity to AIV-H2, accounting for previous exposure to the “extinct” H2N2 human influenza viruses, was found in both BEWs and Cs groups. These data further emphasize the occupational risk posed by zoonotic AIV strains and show the possible occurrence of long-lived antibody-based immunity following AIV infections in humans. Full article
(This article belongs to the Special Issue Ecology of Influenza A Viruses)
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16 pages, 8286 KiB  
Article
Longitudinal Analysis of Influenza A(H5) Sero-Surveillance in Myanmar Ducks, 2006–2019
by Hla Hla Mon, David Hadrill, Aurélie Brioudes, Cho Cho Su Mon, Leslie Sims, Htay Htay Win, Way Zin Thein, Wing Sum Mok, Maung Maung Kyin, Min Thein Maw and Ye Tun Win
Microorganisms 2021, 9(10), 2114; https://doi.org/10.3390/microorganisms9102114 - 07 Oct 2021
Cited by 1 | Viewed by 1878
Abstract
Between 2006 and 2019, serological surveys in unvaccinated domestic ducks reared outdoors in Myanmar were performed, using a haemagglutination inhibition (HI) test, to confirm H5 avian influenza virus circulation and assess temporal and spatial distribution. Positive test results occurred every year that samples [...] Read more.
Between 2006 and 2019, serological surveys in unvaccinated domestic ducks reared outdoors in Myanmar were performed, using a haemagglutination inhibition (HI) test, to confirm H5 avian influenza virus circulation and assess temporal and spatial distribution. Positive test results occurred every year that samples were collected. The annual proportion of positive farms ranged from 7.1% to 77.2%. The results revealed silent/sub-clinical influenza A (H5) virus circulation, even in years and States/Regions with no highly pathogenic avian influenza (HPAI) outbreaks reported. Further analysis of the 2018/19 results revealed considerable differences in seroconversion rates between four targeted States/Regions and between years, and showed seroconversion before and during the sampling period. By the end of the trial, a high proportion of farms were seronegative, leaving birds vulnerable to infection when sold. Positive results likely indicate infection with Gs/GD/96-lineage H5Nx HPAI viruses rather than other H5 subtype low-pathogenicity avian influenza viruses. The findings suggested persistent, but intermittent, circulation of Gs/GD/96-lineage H5Nx HPAI viruses in domestic ducks, despite the veterinary services’ outbreak detection and control efforts. The role of wild birds in transmission remains unclear but there is potential for spill-over in both directions. The findings of this study assist the national authorities in the design of appropriate, holistic avian influenza control programs. Full article
(This article belongs to the Special Issue Ecology of Influenza A Viruses)
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12 pages, 1302 KiB  
Communication
Biological Properties and Genetic Characterization of Novel Low Pathogenic H7N3 Avian Influenza Viruses Isolated from Mallard Ducks in the Caspian Region, Dagestan, Russia
by Marina Gulyaeva, Maria Alessandra De Marco, Ganna Kovalenko, Eric Bortz, Tatiana Murashkina, Kseniya Yurchenko, Marzia Facchini, Mauro Delogu, Ivan Sobolev, Alimurad Gadzhiev, Kirill Sharshov and Alexander Shestopalov
Microorganisms 2021, 9(4), 864; https://doi.org/10.3390/microorganisms9040864 - 17 Apr 2021
Cited by 2 | Viewed by 2467
Abstract
Avian influenza viruses (AIVs) are maintained in wild bird reservoirs, particularly in mallard ducks and other waterfowl. Novel evolutionary lineages of AIV that arise through genetic drift or reassortment can spread with wild bird migrations to new regions, infect a wide variety of [...] Read more.
Avian influenza viruses (AIVs) are maintained in wild bird reservoirs, particularly in mallard ducks and other waterfowl. Novel evolutionary lineages of AIV that arise through genetic drift or reassortment can spread with wild bird migrations to new regions, infect a wide variety of resident bird species, and spillover to domestic poultry. The vast continental reservoir of AIVs in Eurasia harbors a wide diversity of influenza subtypes, including both highly pathogenic (HP) and low pathogenic (LP) H7 AIV. The Caspian Sea region is positioned at the intersection of major migratory flyways connecting Central Asia, Europe, the Black and Mediterranean Sea regions and Africa and holds a rich wetland and avian ecology. To understand genetic reservoirs present in the Caspian Sea region, we collected 559 cloacal swabs from Anseriformes and other species during the annual autumn migration periods in 2017 and 2018. We isolated two novel H7N3 LPAIV from mallard ducks whose H7 hemagglutinin (HA) gene was phylogenetically related to contemporaneous strains from distant Mongolia, and more closely Georgia and Ukraine, and predated the spread of this H7 LPAIV sublineage into East Asia in 2019. The N3 neuraminidase gene and internal genes were prototypical of AIV widely dispersed in wild bird reservoirs sampled along flyways connected to the Caspian region. The polymerase and nucleoprotein segments clustered with contemporaneous H5 HPAI (clade 2.3.4.4b) isolates, suggesting the wide dispersal of H7 LPAIV and the potential of this subtype for reassortment. These findings highlight the need for deeper surveillance of AIV in wild birds to better understand the extent of infection spread and evolution along spatial and temporal flyways in Eurasia. Full article
(This article belongs to the Special Issue Ecology of Influenza A Viruses)
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