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      Year-Round Influenza a Virus Surveillance in Mallards ( Anas platyrhynchos) Reveals Genetic Persistence During the Under-Sampled Spring Season

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          Abstract

          Active influenza A virus (IAV) surveillance in wild waterfowl in the United States has revolved around convenience-based sampling methods, resulting in gaps in surveillance during the spring season. We conducted active IAV surveillance in mallards continuously from July 2017 to July 2019 in the coastal marshes of Lake Erie near Port Clinton, Ohio. We aimed to understand ecological and evolutionary dynamics of IAV across multiple seasons, including the under-sampled spring season. We collected 2096 cloacal swabs and estimated a 6.1% (95% confidence interval (CI): 0.050–0.071) prevalence during the study period. Prevalence was lowest during spring (1.0%, 95% CI: 0.004–0.015). Time-stamped phylogenetic analyses revealed local persistence of genetic lineages of multiple gene segments. The PA segment consists of a lineage detected in multiple seasons with a time to most recent common ancestor of 2.48 years (95% highest posterior density: 2.16–2.74). Analysis of the H3 and H6 segments showed close relation between IAVs detected in spring and the following autumn migration. Though the mechanisms behind viral persistence in a single location are not well understood, we provide evidence that viruses can persist across several seasons. Current surveillance methods should be evaluated to ensure they are capturing the breadth of genetic diversity of IAV in waterfowl and prepare for IAV outbreaks in both animals and humans.

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          Most cited references32

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          Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics.

          We determined the origin and evolutionary pathways of the PB1 genes of influenza A viruses responsible for the 1957 and 1968 human pandemics and obtained information on the variable or conserved region of the PB1 protein. The evolutionary tree constructed from nucleotide sequences suggested the following: (i) the PB1 gene of the 1957 human pandemic strain, A/Singapore/1/57 (H2N2), was probably introduced from avian species and was maintained in humans until 1968; (ii) in the 1968 pandemic strain, A/NT/60/68 (H3N2), the PB1 gene was not derived from the previously circulating virus in humans but probably from another avian virus; and (iii) a current human H3N2 virus inherited the PB1 gene from an A/NT/60/68-like virus. Nucleotide sequence analysis also showed that the avian PB1 gene was introduced into pigs. Hence, transmission of the PB1 gene from avian to mammalian species is a relatively frequent event. Comparative analysis of deduced amino acid sequences disclosed highly conserved regions in PB1 proteins, which may be key structures required for PB1 activities.
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            Persistence of H5 and H7 avian influenza viruses in water.

            Although fecal-oral transmission of avian influenza viruses (AIV) via contaminated water represents a recognized mechanism for transmission within wild waterfowl populations, little is known about viral persistence in this medium. In order to provide initial data on persistence of H5 and H7 AIVs in water, we evaluated eight wild-type low-pathogenicity H5 and H7 AIVs isolated from species representing the two major influenza reservoirs (Anseriformes and Charadriiformes). In addition, the persistence of two highly pathogenic avian influenza (HPAI) H5N1 viruses from Asia was examined to provide some insight into the potential for these viruses to be transmitted and maintained in the environments of wild bird populations. Viruses were tested at two temperatures (17 C and 28 C) and three salinity levels (0, 15, and 30 parts per thousand sea salt). The wild-type H5 and H7 AIV persistence data to date indicate the following: 1) that H5 and H7 AIVs can persist for extended periods of time in water, with a duration of infectivity comparable to AIVs of other subtypes; 2) that the persistence of H5 and H7 AIVs is inversely proportional to temperature and salinity of water; and 3) that a significant interaction exists between the effects of temperature and salinity on the persistence of AIV, with the effect of salinity more prominent at lower temperatures. Results from the two HPAI H5N1 viruses from Asia indicate that these viruses did not persist as long as the wild-type AIVs.
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              Avian influenza virus in water: infectivity is dependent on pH, salinity and temperature.

              Wild birds in the Orders Anseriformes and Charadriiformes are the natural reservoir for avian influenza (AI) viruses. Transmission within these aquatic bird populations occurs through an indirect fecal-oral route involving contaminated water on shared aquatic habitats. In order to better understand the influence that aquatic environments exert on AI transmission and maintenance in the wild-bird reservoir system, we determined the duration of persistence for 12 wild-bird origin AI viruses under natural ranges of pH, salinity, and temperature. Viral persistence was measured using a laboratory-based distilled water model system. The AI viruses varied in their response to each of the examined variables, but, generally, the viruses were most stable at a slightly basic pH (7.4-8.2), low temperatures ( 32 degrees C), and high salinity (>25,000 ppm). The results of this research suggest that the pH, temperature, and salinity in natural aquatic habitats can influence the ability of AI viruses to remain infective within these environments. Furthermore, these results provide insight into chemical and physical properties of water that could enhance or restrict AI virus transmission on an aquatic bird habitat.
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                Author and article information

                Journal
                Viruses
                Viruses
                viruses
                Viruses
                MDPI
                1999-4915
                11 June 2020
                June 2020
                : 12
                : 6
                : 632
                Affiliations
                [1 ]Department of Veterinary Preventive Medicine, College of Veterinary Medicine, The Ohio State University, Columbus, OH 43210, USA; lauterbach.7@ 123456osu.edu (S.E.L.); mcbride.338@ 123456osu.edu (D.S.M.); nolting.4@ 123456osu.edu (J.M.N.)
                [2 ]Winous Point Marsh Conservancy, Port Clinton, OH 43452, USA; brendan@ 123456winous.org
                Author notes
                [* ]Correspondence: bowman.214@ 123456osu.edu ; Tel.: +1-614-292-6923
                Author information
                https://orcid.org/0000-0002-2705-4805
                https://orcid.org/0000-0002-0738-8453
                Article
                viruses-12-00632
                10.3390/v12060632
                7354581
                32545281
                1453555b-7a2b-4584-b9a4-f0b751728045
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 20 May 2020
                : 09 June 2020
                Categories
                Article

                Microbiology & Virology
                anas platyrhynchos,influenza a virus,mallards,surveillance,spring migration,phylogenetics

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