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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: closed (30 September 2020) | Viewed by 53800

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Dr. Ignacio (Nacho) Mena

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Icahn School of Medicine at Mount Sinai, New York, USA

Special Issue Information

All known subtypes of conventional influenza A viruses (not including the recently discovered bat influenzas) can be found in wild birds. From this original natural reservoir, a few subtypes have been able to successfully replicate and circulate in domestic birds and several mammalian hosts, including humans. Therefore, influenza surveillance in wild birds is important for understanding viral diversity, but also to prevent or mitigate influenza outbreaks in poultry and other livestock, and to identify strains with zoonotic and pandemic potential. Migratory aquatic wild birds are especially important in the ecology of influenza A viruses because they can disseminate the virus to very long distances through their migratory flyways, and they can congregate in very high numbers at stopovers during migration and at their wintering and breeding sites. These multispecies gatherings provide an optimal hotspot for viral dissemination and for the reassortment of genetic segments between different co-circulating strains and subtypes. Marine mammals are susceptible to infection by influenza viruses of avian and human origin, and outbreaks can result in significant mortality. The recent discovery of influenza A-like viruses in bats has challenged some general concepts in the influenza field. The implementation of next-generation sequencing technology has opened the possibility of acquiring full genome sequences from large numbers of samples almost in real time, and has greatly increased our ability to conduct influenza surveillance in wildlife. Nevertheless, surveillance can only cover a minuscule proportion of species, individuals, and locations and, therefore, careful choice of sampling strategies is important.

In this Special Issue, we aim to discuss recent findings of influenza surveillance and research in wildlife in different parts of the world and in different species. Of interest are the unique features of bat influenza viruses and their role in the big picture of influenza virus evolution. Moreover, how new methods and technology in genome sequencing and phylogenetic analysis can improve our understanding of influenza circulation in wildlife and be better prepared for future outbreaks in livestock and humans are also of interest.

Dr. Ignacio (Nacho) Mena
Guest Editor

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Keywords

avian influenza
bat influenza
migratory birds
marine mammals
highly pathogenic avian influenza
aquatic birds
migratory flyways
influenza surveillance
influenza subtypes

Published Papers (11 papers)

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Research

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10 pages, 467 KiB

Open AccessArticle

Influenza A Viruses in Whistling Ducks (Subfamily Dendrocygninae)

by Deborah L. Carter, Paul Link, Gene Tan, David E. Stallknecht and Rebecca L. Poulson

Viruses 2021, 13(2), 192; https://doi.org/10.3390/v13020192 - 28 Jan 2021

Viewed by 2421

Abstract

As compared to other Anseriformes, data related to influenza A virus (IAV) detection and isolation, and IAV antibody detection in whistling ducks (Dendrocygna spp. and Thalassornis leuconotus; subfamily Dendrocygninae) are limited. To better evaluate the potential role of whistling ducks in the epidemiology of IAV, we (1) conducted surveillance for IAV from black-bellied whistling ducks (BBWD, Dendrocygnaautumnalis) sampled in coastal Louisiana, USA, during February 2018 and 2019, and (2) reviewed the published literature and Influenza Resource Database (IRD) that reported results of IAV surveillance of whistling ducks. In the prospective study, from 166 BBWD sampled, one H10N7 IAV was isolated (0.6% prevalence), and overall blocking enzyme-linked immunosorbent assay (bELISA) antibody seroprevalence was 10%. The literature review included publications and data in the IRD from 1984 to 2020 that reported results from nearly 5000 collected samples. For any given collection, the IAV isolation rate never exceeded 5.5%, and seroprevalence estimates ranged from 0 to 42%. Results from our prospective study in Louisiana are consistent with this historic literature; however, although all data consistently demonstrated a low prevalence of infection, the potential role of this species in the epidemiology of IAV should not be totally discounted. In sum, whistling ducks can be infected with IAV, they represent important species on many areas where waterfowl winter, and their distribution across the globe appears to be changing. Full article

(This article belongs to the Special Issue Influenza Viruses in Wildlife)

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23 pages, 11711 KiB

Open AccessArticle

Emergence of Novel Reassortant H1N1 Avian Influenza Viruses in Korean Wild Ducks in 2018 and 2019

by Thuy-Tien Thi Trinh, Bao Tuan Duong, Anh Thi Viet Nguyen, Hien Thi Tuong, Vui Thi Hoang, Duong Duc Than, SunJeong Nam, Haan Woo Sung, Ki-Jung Yun, Seon-Ju Yeo and Hyun Park

Viruses 2021, 13(1), 30; https://doi.org/10.3390/v13010030 - 26 Dec 2020

Cited by 7 | Viewed by 4380

Abstract

Influenza A virus subtype H1N1 has caused global pandemics like the “Spanish flu” in 1918 and the 2009 H1N1 pandemic several times. H1N1 remains in circulation and survives in multiple animal sources, including wild birds. Surveillance during the winter of 2018–2019 in Korea revealed two H1N1 isolates in samples collected from wild bird feces: KNU18-64 (A/Greater white-fronted goose/South Korea/KNU18-64/2018(H1N1)) and WKU19-4 (A/wild bird/South Korea/WKU19-4/2019(H1N1)). Phylogenetic analysis indicated that M gene of KNU18-64(H1N1) isolate resembles that of the Alaskan avian influenza virus, whereas WKU19-4(H1N1) appears to be closer to the Mongolian virus. Molecular characterization revealed that they harbor the amino acid sequence PSIQRS↓GLF and are low-pathogenicity influenza viruses. In particular, the two isolates harbored three different mutation sites, indicating that they have different virulence characteristics. The mutations in the PB1-F2 and PA protein of WKU19-4(H1N1) indicate increasing polymerase activity. These results corroborate the kinetic growth data for WKU19-4 in MDCK cells: a dramatic increase in the viral titer after 12 h post-inoculation compared with that in the control group H1N1 (CA/04/09(pdm09)). The KNU18-64(H1N1) isolate carries mutations indicating an increase in mammal adaptation; this characterization was confirmed by the animal study in mice. The KNU18-64(H1N1) group showed the presence of viruses in the lungs at days 3 and 6 post-infection, with titers of 2.71 ± 0.16 and 3.71 ± 0.25 log10(TCID50/mL), respectively, whereas the virus was only detected in the WKU19-4(H1N1) group at day 6 post-infection, with a lower titer of 2.75 ± 0.51 log10(TCID50/mL). The present study supports the theory that there is a relationship between Korea and America with regard to reassortment to produce novel viral strains. Therefore, there is a need for increased surveillance of influenza virus circulation in free-flying and wild land-based birds in Korea, particularly with regard to Alaskan and Asian strains. Full article

(This article belongs to the Special Issue Influenza Viruses in Wildlife)

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14 pages, 1740 KiB

Open AccessArticle

Influenza A Viruses in Ruddy Turnstones (Arenaria interpres); Connecting Wintering and Migratory Sites with an Ecological Hotspot at Delaware Bay

by Rebecca Poulson, Deborah Carter, Shelley Beville, Lawrence Niles, Amanda Dey, Clive Minton, Pamela McKenzie, Scott Krauss, Richard Webby, Robert Webster and David E. Stallknecht

Viruses 2020, 12(11), 1205; https://doi.org/10.3390/v12111205 - 22 Oct 2020

Cited by 6 | Viewed by 2775

Abstract

Each May for over three decades, avian influenza A viruses (IAVs) have been isolated from shorebirds and gulls (order Charadriiformes) at Delaware Bay (DE Bay), USA, which is a critical stopover site for shorebirds on their spring migration to arctic breeding grounds. At DE Bay, most isolates have been recovered from ruddy turnstones (Arenaria interpres), but it is unknown if this species is involved in either the maintenance or movement of these viruses outside of this site. We collected and tested fecal samples from 2823 ruddy turnstones in Florida and Georgia in the southeastern United States during four winter/spring sample periods—2010, 2011, 2012, and 2013—and during the winters of 2014/2015 and 2015/2016. Twenty-five low pathogenicity IAVs were recovered representing five subtypes (H3N4, H3N8, H5N9, H6N1, and H12N2). Many of these subtypes matched those recovered at DE Bay during the previous year or that year’s migratory cycle, suggesting that IAVs present on these southern wintering areas represent a source of virus introduction to DE Bay via migrating ruddy turnstones. Analyses of all IAV gene segments of H5N9 and H6N1 viruses recovered from ruddy turnstones at DE Bay during May 2012 and from the southeast during the spring of 2012 revealed a high level of genetic relatedness at the nucleotide level, suggesting that migrating ruddy turnstones move IAVs from wintering grounds to the DE Bay ecosystem. Full article

(This article belongs to the Special Issue Influenza Viruses in Wildlife)

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17 pages, 8165 KiB

Open AccessCommunication

Characterization of Avian Influenza Virus H10–H12 Subtypes Isolated from Wild Birds in Shanghai, China from 2016 to 2019

by Ling Tang, Wangjun Tang, Le Ming, Jianming Gu, Kai Qian, Xiaofang Li, Tianhou Wang and Guimei He

Viruses 2020, 12(10), 1085; https://doi.org/10.3390/v12101085 - 25 Sep 2020

Cited by 6 | Viewed by 2761

Abstract

H10, H11 and H12 (H10–H12) subtypes of the avian influenza virus (AIV) are associated with waterfowl. Although these subtypes of AIV are infrequently detected in nature, they can undergo reassortment with other AIV subtypes. Few H10–H12 subtypes of AIV have been isolated from wild birds in China. In this study, 12 AIV isolates of H10–H12 subtypes were identified via routine surveillance of wild birds in Shanghai, China from 2016 to 2019, including two H10, three H11 and seven H12 isolates. Sequence and phylogenetic analyses revealed that the genomic segments of the 12 isolates are highly diverse. These 12 isolates are closely related to those in the Eurasian lineage and share a high degree of sequence identity with those from wild birds and domestic ducks in countries in the East Asian–Australasian Flyway, including Japan, Korea, Bangladesh, Vietnam and China. However, parts of the genomic segments of two H12N2 isolates (NH112319-H12N2 and NH101807-H12N2) belong to the North American lineage, suggesting intercontinental reassortment among H12 AIVs in Eurasia and North American. To better understand the ecological and phylodynamic features of H10–H12 subtypes in wild birds, a large-scale surveillance of AIVs in wild birds is warranted. Full article

(This article belongs to the Special Issue Influenza Viruses in Wildlife)

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14 pages, 1819 KiB

Open AccessArticle

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

by Sarah E. Lauterbach, Dillon S. McBride, Brendan T. Shirkey, Jacqueline M. Nolting and Andrew S. Bowman

Viruses 2020, 12(6), 632; https://doi.org/10.3390/v12060632 - 11 Jun 2020

Cited by 6 | Viewed by 2605

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. Full article

(This article belongs to the Special Issue Influenza Viruses in Wildlife)

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17 pages, 3381 KiB

Open AccessArticle

Eco-Epidemiological Evidence of the Transmission of Avian and Human Influenza A Viruses in Wild Pigs in Campeche, Mexico

by Brenda Aline Maya-Badillo, Rafael Ojeda-Flores, Andrea Chaves, Saul Reveles-Félix, Guillermo Orta-Pineda, María José Martínez-Mercado, Manuel Saavedra-Montañez, René Segura-Velázquez, Mauro Sanvicente and José Iván Sánchez-Betancourt

Viruses 2020, 12(5), 528; https://doi.org/10.3390/v12050528 - 11 May 2020

Cited by 8 | Viewed by 3405

Abstract

Influenza, a zoonosis caused by various influenza A virus subtypes, affects a wide range of species, including humans. Pig cells express both sialyl-α-2,3-Gal and sialyl-α-2,6-Gal receptors, which make them susceptible to infection by avian and human viruses, respectively. To date, it is not known whether wild pigs in Mexico are affected by influenza virus subtypes, nor whether this would make them a potential risk of influenza transmission to humans. In this work, 61 hogs from two municipalities in Campeche, Mexico, were sampled. Hemagglutination inhibition assays were performed in 61 serum samples, and positive results were found for human H1N1 (11.47%), swine H1N1 (8.19%), and avian H5N2 (1.63%) virus variants. qRT-PCR assays were performed on the nasal swab, tracheal, and lung samples, and 19.67% of all hogs were positive to these assays. An avian H5N2 virus, first reported in 1994, was identified by sequencing. Our results demonstrate that wild pigs are participating in the exposure, transmission, maintenance, and possible diversification of influenza viruses in fragmented habitats, highlighting the synanthropic behavior of this species, which has been poorly studied in Mexico. Full article

(This article belongs to the Special Issue Influenza Viruses in Wildlife)

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Review

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13 pages, 2177 KiB

Open AccessReview

Bat Influenza Viruses: Current Status and Perspective

by Wenyu Yang, Tony Schountz and Wenjun Ma

Viruses 2021, 13(4), 547; https://doi.org/10.3390/v13040547 - 25 Mar 2021

Cited by 20 | Viewed by 3660

Abstract

Bats are natural reservoirs for many viruses, including several that are zoonotic. Two unusual H17N10 and H18N11 influenza viruses have been found in New World bats. Although neither of these viruses have been isolated, infectious clone technology has permitted significant progress to understand their biology, which include unique features compared to all other known influenza A viruses. In addition, an H9N2-like influenza A virus was isolated from Old World bats and it shows similar characteristics of normal influenza A viruses. In this review, current status and perspective on influenza A viruses identified in bats is reviewed and discussed. Full article

(This article belongs to the Special Issue Influenza Viruses in Wildlife)

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34 pages, 1496 KiB

Open AccessReview

Highly Pathogenic Avian Influenza Viruses at the Wild–Domestic Bird Interface in Europe: Future Directions for Research and Surveillance

by Josanne H. Verhagen, Ron A. M. Fouchier and Nicola Lewis

Viruses 2021, 13(2), 212; https://doi.org/10.3390/v13020212 - 30 Jan 2021

Cited by 123 | Viewed by 14943

Abstract

Highly pathogenic avian influenza (HPAI) outbreaks in wild birds and poultry are no longer a rare phenomenon in Europe. In the past 15 years, HPAI outbreaks—in particular those caused by H5 viruses derived from the A/Goose/Guangdong/1/1996 lineage that emerged in southeast Asia in 1996—have been occuring with increasing frequency in Europe. Between 2005 and 2020, at least ten HPAI H5 incursions were identified in Europe resulting in mass mortalities among poultry and wild birds. Until 2009, the HPAI H5 virus outbreaks in Europe were caused by HPAI H5N1 clade 2.2 viruses, while from 2014 onwards HPAI H5 clade 2.3.4.4 viruses dominated outbreaks, with abundant genetic reassortments yielding subtypes H5N1, H5N2, H5N3, H5N4, H5N5, H5N6 and H5N8. The majority of HPAI H5 virus detections in wild and domestic birds within Europe coincide with southwest/westward fall migration and large local waterbird aggregations during wintering. In this review we provide an overview of HPAI H5 virus epidemiology, ecology and evolution at the interface between poultry and wild birds based on 15 years of avian influenza virus surveillance in Europe, and assess future directions for HPAI virus research and surveillance, including the integration of whole genome sequencing, host identification and avian ecology into risk-based surveillance and analyses. Full article

(This article belongs to the Special Issue Influenza Viruses in Wildlife)

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20 pages, 2922 KiB

Open AccessReview

Avian Influenza A Virus Associations in Wild, Terrestrial Mammals: A Review of Potential Synanthropic Vectors to Poultry Facilities

by J. Jeffrey Root and Susan A. Shriner

Viruses 2020, 12(12), 1352; https://doi.org/10.3390/v12121352 - 26 Nov 2020

Cited by 12 | Viewed by 3279

Abstract

The potential role of wild mammals in the epidemiology of influenza A viruses (IAVs) at the farm-side level has gained increasing consideration over the past two decades. In some instances, select mammals may be more likely to visit riparian areas (both close and distant to farms) as well as poultry farms, as compared to traditional reservoir hosts, such as waterfowl. Of significance, many mammalian species can successfully replicate and shed multiple avian IAVs to high titers without prior virus adaptation and often can shed virus in greater quantities than synanthropic avian species. Within this review, we summarize and discuss the potential risks that synanthropic mammals could pose by trafficking IAVs to poultry operations based on current and historic literature. Full article

(This article belongs to the Special Issue Influenza Viruses in Wildlife)

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19 pages, 1183 KiB

Open AccessReview

A Review of Avian Influenza A Virus Associations in Synanthropic Birds

by Susan A. Shriner and J. Jeffrey Root

Viruses 2020, 12(11), 1209; https://doi.org/10.3390/v12111209 - 23 Oct 2020

Cited by 33 | Viewed by 5939

Abstract

Avian influenza A viruses (IAV) have received significant attention due to the threat they pose to human, livestock, and wildlife health. In this review, we focus on what is known about IAV dynamics in less common avian species that may play a role in trafficking IAVs to poultry operations. Specifically, we focus on synanthropic bird species. Synanthropic species, otherwise known as peridomestic, are species that are ecologically associated with humans and anthropogenically modified landscapes, such as agricultural and urban areas. Aquatic birds such as waterfowl and shorebirds are the species most commonly associated with avian IAVs, and are generally considered the reservoir or maintenance hosts in the natural ecology of these viruses. Waterfowl and shorebirds are occasionally associated with poultry facilities, but are uncommon or absent in many areas, especially large commercial operations. In these cases, spillover hosts that share resources with both maintenance hosts and target hosts such as poultry may play an important role in introducing wild bird viruses onto farms. Consequently, our focus here is on what is known about IAV dynamics in synanthropic hosts that are commonly found on both farms and in nearby habitats, such as fields, lakes, wetlands, or riparian areas occupied by waterfowl or shorebirds. Full article

(This article belongs to the Special Issue Influenza Viruses in Wildlife)

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22 pages, 1824 KiB

Open AccessReview

Avian Influenza Viruses Detected in Birds in Sub-Saharan Africa: A Systematic Review

by Annie Kalonda, Ngonda Saasa, Panji Nkhoma, Masahiro Kajihara, Hirofumi Sawa, Ayato Takada and Edgar Simulundu

Viruses 2020, 12(9), 993; https://doi.org/10.3390/v12090993 - 7 Sep 2020

Cited by 12 | Viewed by 6492

Abstract

In the recent past, sub-Saharan Africa has not escaped the devastating effects of avian influenza virus (AIV) in poultry and wild birds. This systematic review describes the prevalence, spatiotemporal distribution, and virus subtypes detected in domestic and wild birds for the past two decades (2000–2019). We collected data from three electronic databases, PubMed, SpringerLink electronic journals and African Journals Online, using the Preferred Reporting Items for Systematic reviews and Meta-Analyses protocol. A total of 1656 articles were reviewed, from which 68 were selected. An overall prevalence of 3.0% AIV in birds was observed. The prevalence varied between regions and ranged from 1.1% to 7.1%. The Kruskal–Wallis and Wilcoxon signed-rank sum test showed no significant difference in the prevalence of AIV across regions, χ²(3) = 5.237, p = 0.1553 and seasons, T = 820, z = −1.244, p = 0.2136. Nineteen hemagglutinin/neuraminidase subtype combinations were detected during the reviewed period, with southern Africa recording more diverse AIV subtypes than other regions. The most detected subtype was H5N1, followed by H9N2, H5N2, H5N8 and H6N2. Whilst these predominant subtypes were mostly detected in domestic poultry, H1N6, H3N6, H4N6, H4N8, H9N1 and H11N9 were exclusively detected in wild birds. Meanwhile, H5N1, H5N2 and H5N8 were detected in both wild and domestic birds suggesting circulation of these subtypes among wild and domestic birds. Our findings provide critical information on the eco-epidemiology of AIVs that can be used to improve surveillance strategies for the prevention and control of avian influenza in sub-Saharan Africa. Full article

(This article belongs to the Special Issue Influenza Viruses in Wildlife)

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