Jeffrey Hall - Academia.edu (original) (raw)

Papers by Jeffrey Hall

Research paper thumbnail of Highly pathogenic avian influenza virus H5N2 (clade 2.3.4.4) challenge of mallards age appropriate to the 2015 midwestern poultry outbreak

Influenza and Other Respiratory Viruses, 2021

BackgroundThe 2015 highly pathogenic avian influenza virus (HPAIV) H5N2 clade 2.3.4.4 outbreak in... more BackgroundThe 2015 highly pathogenic avian influenza virus (HPAIV) H5N2 clade 2.3.4.4 outbreak in upper midwestern U.S. poultry operations was not detected in wild birds to any great degree during the outbreak, despite wild waterfowl being implicated in the introduction, reassortment, and movement of the virus into North America from Asia. This outbreak led to the demise of over 50 million domestic birds and occurred mainly during the northward spring migration of adult avian populations.ObjectivesThere have been no experimental examinations of the pathogenesis, transmission, and population impacts of this virus in adult wild waterfowl with varying exposure histories—the most relevant age class.MethodsWe captured, housed, and challenged adult wild mallards (Anas platyrhynchos) with HPAIV H5N2 clade 2.3.4.4 and measured viral infection, viral excretion, and transmission to other mallards.ResultsAll inoculated birds became infected and excreted moderate amounts of virus, primarily ora...

Research paper thumbnail of Experimental Infection of Fox Squirrels (Sciurus Niger) with West Nile Virus

The American Journal of Tropical Medicine and Hygiene, 2006

Research paper thumbnail of Influenza Exposure in United States Feral Swine Populations

Journal of Wildlife Diseases, 2008

Swine play an important role in the disease ecology of influenza. Having cellular receptors in co... more Swine play an important role in the disease ecology of influenza. Having cellular receptors in common with birds and humans, swine provide opportunities for mixed infections and potential for genetic reassortment between avian, human, and porcine influenza. Feral swine populations are rapidly expanding in both numbers and range and are increasingly coming into contact with waterfowl, humans, and agricultural operations. In this study, over 875 feral swine were sampled from six states across the United States for serologic evidence of exposure to influenza. In Oklahoma, Florida, and Missouri, USA, no seropositive feral swine were detected. Seropositive swine were detected in California, Mississippi, and Texas, USA. Antibody prevalences in these states were 1% in Mississippi, 5% in California, and 14.4% in Texas. All seropositive swine were exposed to H3N2 subtype, the predominant subtype currently circulating in domestic swine. The only exceptions were in San Saba County, Texas, where of the 15 seropositive samples, four were positive for H1N1 and seven for both H1N1 and H3N2. In Texas, there was large geographical and temporal variation in antibody prevalence and no obvious connection to domestic swine operations. No evidence of exposure to avian influenza in feral swine was uncovered. From these results it is apparent that influenza in feral swine poses a risk primarily to swine production operations. However, because feral swine share habitat with waterfowl, prey on and scavenge dead and dying birds, are highly mobile, and are increasingly coming into contact with humans, the potential for these animals to become infected with avian or human influenza in addition to swine influenza is a distinct possibility.

Research paper thumbnail of Tissues from American kestrels experimentally inoculated with highly pathogenic avian influenza virus H5N1

<p>A. Pancreas with multifocal to coalescing areas of necrosis (arrows) (HE stain). B. Brai... more <p>A. Pancreas with multifocal to coalescing areas of necrosis (arrows) (HE stain). B. Brain with multifocal cerebral necrosis (arrows) accompanied by a mild infiltration of heterophils (HE stain). C. Section of same pancreatic tissue as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0007555#pone-0007555-g002&quot; target="_blank">Fig. 2A</a>, stained by immunohistochemistry to identify influenza A virus antigen. Staining of influenza A antigen is intense in areas of necrosis (arrows). D. Immunohistochemical staining of influenza A virus antigen in brain tissue. Areas of brain necrosis are strongly positive (arrows).</p

Research paper thumbnail of Influenza A virus recovery, diversity, and intercontinental exchange: A multi-year assessment of wild bird sampling at Izembek National Wildlife Refuge, Alaska

PloS one, 2018

Western Alaska is a potential point-of-entry for foreign-origin influenza A viruses (IAVs) into N... more Western Alaska is a potential point-of-entry for foreign-origin influenza A viruses (IAVs) into North America via migratory birds. We sampled waterfowl and gulls for IAVs at Izembek National Wildlife Refuge (NWR) in western Alaska, USA, during late summer and autumn months of 2011-2015, to evaluate the abundance and diversity of viruses at this site. We collected 4842 samples across five years from 25 species of wild birds resulting in the recovery, isolation, and sequencing of 172 IAVs. With the intent of optimizing sampling efficiencies, we used information derived from this multi-year effort to: 1) evaluate from which species we consistently recover viruses, 2) describe viral subtypes of isolates by host species and year, 3) characterize viral gene segment sequence diversity with respect to host species, and assess potential differences in the viral lineages among the host groups, and 4) examine how evidence of intercontinental exchange of IAVs relates to host species. We consist...

Research paper thumbnail of Prevalence and Distribution of Wellfleet Bay Virus Exposure in the Common Eider (Somateria Mollissima)

Journal of Wildlife Diseases, 2017

BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access t... more BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access titles in the biological, ecological, and environmental sciences published by nonprofit societies, associations, museums, institutions, and presses.

Research paper thumbnail of No Evidence of Infection or Exposure to Highly Pathogenic Avian Influenzas in Peridomestic Wildlife on an Affected Poultry Facility

Journal of wildlife diseases, Jan 31, 2016

We evaluated the potential transmission of avian influenza viruses (AIV) in wildlife species in ... more We evaluated the potential transmission of avian influenza viruses (AIV) in wildlife species in three settings in association with an outbreak at a poultry facility: 1) small birds and small mammals on a poultry facility that was affected with highly pathogenic AIV (HPAIV) in April 2015; 2) small birds and small mammals on a nearby poultry facility that was unaffected by HPAIV; and 3) small birds, small mammals, and waterfowl in a nearby natural area. We live-captured small birds and small mammals and collected samples from hunter-harvested waterfowl to test for active viral shedding and evidence of exposure (serum antibody) to AIV and the H5N2 HPAIV that affected the poultry facility. We detected no evidence of shedding or specific antibody to AIV in small mammals and small birds 5 mo after depopulation of the poultry. We detected viral shedding and exposure to AIV in waterfowl and estimated approximately 15% viral shedding and 60% antibody prevalence. In waterfowl, we did not det...

Research paper thumbnail of Antigenic Characterization of H3 Subtypes of Avian Influenza A Viruses from North America

Avian Diseases, 2016

Besides humans, H3 subtypes of influenza A viruses (IAVs) can infect various animal hosts, includ... more Besides humans, H3 subtypes of influenza A viruses (IAVs) can infect various animal hosts, including avian, swine, equine, canine, and sea mammal species. These H3 viruses are both antigenically and genetically diverse. Here, we characterized the antigenic diversity of contemporary H3 avian IAVs recovered from migratory birds in North America. Hemagglutination inhibition (HI) assays were performed on 37 H3 isolates of avian IAVs recovered from 2007 to 2011 using generated reference chicken sera. These isolates were recovered from samples taken in the Atlantic, Mississippi, Central, and Pacific waterfowl migration flyways. Antisera to all the tested H3 isolates cross-reacted with each other and, to a lesser extent, with those to H3 canine and H3 equine IAVs. Antigenic cartography showed that the largest antigenic distance among the 37 avian IAVs is about four units, and each unit corresponds to a 2 log  2 difference in the HI titer. However, none of the tested H3 IAVs cross-reacted with ferret sera derived from contemporary swine and human IAVs. Our results showed that the H3 avian IAVs we tested lacked significant antigenic diversity, and these viruses were antigenically different from those circulating in swine and human populations. This suggests that H3 avian IAVs in North American waterfowl are antigenically relatively stable.

Research paper thumbnail of Limited evidence of intercontinental dispersal of avian paramyxovirus serotype 4 by migratory birds

Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases, Jun 27, 2016

Avian paramyxovirus serotype 4 (APMV-4) is a single stranded RNA virus that has most often been i... more Avian paramyxovirus serotype 4 (APMV-4) is a single stranded RNA virus that has most often been isolated from waterfowl. Limited information has been reported regarding the prevalence, pathogenicity, and genetic diversity of AMPV-4. To assess the intercontinental dispersal of this viral agent, we sequenced the fusion gene of 58 APMV-4 isolates collected in the United States, Japan and the Ukraine and compared them to all available sequences on GenBank. With only a single exception the phylogenetic clades of APMV-4 sequences were monophyletic with respect to their continents of origin (North America, Asia and Europe). Thus, we detected limited evidence for recent intercontinental dispersal of APMV-4 in this study.

Research paper thumbnail of Demographic and Spatiotemporal Patterns of Avian Influenza Infection at the Continental Scale, and in Relation to Annual Life Cycle of a Migratory Host

PLOS ONE, 2015

Since the spread of highly pathogenic avian influenza (HPAI) H5N1 in the eastern hemisphere, nume... more Since the spread of highly pathogenic avian influenza (HPAI) H5N1 in the eastern hemisphere, numerous surveillance programs and studies have been undertaken to detect the occurrence, distribution, or spread of avian influenza viruses (AIV) in wild bird populations worldwide. To identify demographic determinants and spatiotemporal patterns of AIV infection in long distance migratory waterfowl in North America, we fitted generalized linear models with binominal distribution to analyze results from 13,574 blue-winged teal (Anas discors, BWTE) sampled in 2007 to 2010 year round during AIV surveillance programs in Canada and the United States. Our analyses revealed that during late summer staging (July-August) and fall migration (September-October), hatch year (HY) birds were more likely to be infected than after hatch year (AHY) birds, however there was no difference between age categories for the remainder of the year (winter, spring migration, and breeding period), likely due to maturing immune systems and newly acquired immunity of HY birds. Probability of infection increased non-linearly with latitude, and was highest in late summer prior to fall migration when densities of birds and the proportion of susceptible HY birds in the population are highest. Birds in the Central and Mississippi flyways were more likely to be infected compared to those in the Atlantic flyway. Seasonal cycles and spatial variation of AIV infection were largely driven by the dynamics of AIV infection in HY birds,

Research paper thumbnail of Rapidly Expanding Range of Highly Pathogenic Avian Influenza Viruses

Emerging Infectious Diseases, 2015

The movement of highly pathogenic avian influenza (H5N8) virus across Eurasia and into North Amer... more The movement of highly pathogenic avian influenza (H5N8) virus across Eurasia and into North America and the virus' propensity to reassort with co-circulating low pathogenicity viruses raise concerns among poultry producers, wildlife biologists, aviculturists, and public health personnel worldwide. Surveillance, modeling, and experimental research will provide the knowledge required for intelligent policy and management decisions.

Research paper thumbnail of Respiratory transmission of an avian H3N8 influenza virus isolated from a harbour seal

Nature Communications, 2014

The ongoing human H7N9 influenza infections highlight the threat of emerging avian influenza viru... more The ongoing human H7N9 influenza infections highlight the threat of emerging avian influenza viruses. In 2011, an avian H3N8 influenza virus isolated from moribund New England harbour seals was shown to have naturally acquired mutations known to increase the transmissibility of highly pathogenic H5N1 influenza viruses. To elucidate the potential human health threat, here we evaluate a panel of avian H3N8 viruses and find that the harbour seal virus displays increased affinity for mammalian receptors, transmits via respiratory droplets in ferrets and replicates in human lung cells. Analysis of a panel of human sera for H3N8 neutralizing antibodies suggests that there is no population-wide immunity to these viruses. The prevalence of H3N8 viruses in birds and multiple mammalian species including recent isolations from pigs and evidence that it was a past human pandemic virus make the need for surveillance and risk analysis of these viruses of public health importance.

Research paper thumbnail of Evolution of a reassortant North American gull influenza virus lineage: drift, shift and stability

Virology Journal, 2013

Background: The role of gulls in the ecology of avian influenza (AI) is different than that of wa... more Background: The role of gulls in the ecology of avian influenza (AI) is different than that of waterfowl. Different constellations of subtypes circulate within the two groups of birds and AI viruses isolated from North American gulls frequently possess reassortant genomes with genetic elements from both North America and Eurasian lineages. A 2008 isolate from a Newfoundland Great Black-backed Gull contained a mix of North American waterfowl, North American gull and Eurasian lineage genes. Methods: We isolated, sequenced and phylogenetically compared avian influenza viruses from 2009 Canadian wild birds. Results: We analyzed six 2009 virus isolates from Canada and found the same phylogenetic lineage had persisted over a larger geographic area, with an expanded host range that included dabbling and diving ducks as well as gulls. All of the 2009 virus isolates contained an internal protein coding set of genes of the same Eurasian lineage genes except PB1 that was from a North American lineage, and these genes continued to evolve by genetic drift. We show evidence that the 2008 Great Black-backed Gull virus was derived from this lineage with a reassortment of a North American PA gene into the more stable core set of internal protein coding genes that has circulated in avian populations for at least 2 years. From this core, the surface glycoprotein genes have switched several times creating H13N6, H13N2, and H16N3 subtypes. These gene segments were from North American lineages except for the H16 and N3 vRNAs. Conclusions: This process appears similar to genetic shifts seen with swine influenza where a stable "triple reassortant internal gene" core has circulated in swine populations with genetic shifts occurring with hemaggluttinin and neuraminidase proteins getting periodically switched. Thus gulls may serve as genetic mixing vessels for different lineages of avian influenza, similar to the role of swine with regards to human influenza. These findings illustrate the need for continued surveillance in gull and waterfowl populations, both on the Pacific and especially Atlantic coasts of North America, to document virus intercontinental movement and the role of gull species in the evolution and epidemiology of AI.

Research paper thumbnail of Experimental challenge and pathology of highly pathogenic avian influenza virus H5N1 in dunlin (Calidris alpina), an intercontinental migrant shorebird species

Influenza and Other Respiratory Viruses, 2011

Background Shorebirds (Charadriiformes) are considered one of the primary reservoirs of avian inf... more Background Shorebirds (Charadriiformes) are considered one of the primary reservoirs of avian influenza. Because these species are highly migratory, there is concern that infected shorebirds may be a mechanism by which highly pathogenic avian influenza virus (HPAIV) H5N1 could be introduced into North America from Asia. Large numbers of dunlin (Calidris alpina) migrate from wintering areas in central and eastern Asia, where HPAIV H5N1 is endemic, across the Bering Sea to breeding areas in Alaska. Low pathogenic avian influenza virus has been previously detected in dunlin, and thus, dunlin represent a potential risk to transport HPAIV to North America. To date no experimental challenge studies have been performed in shorebirds. Methods Wild dunlin were inoculated intranasally and intrachoanally various doses of HPAIV H5N1. The birds were monitored daily for virus excretion, disease signs, morbidity, and mortality. Results The infectious dose of HPAIV H5N1 in dunlin was determined to be 10 1.7 EID 50 /100 ll and that the lethal dose was 10 1.83 EID 50 /100 ll. Clinical signs were consistent with neurotropic disease, and histochemical analyses revealed that infection was systemic with viral antigen and RNA most consistently found in brain tissues. Infected birds excreted relatively large amounts of virus orally (10 4 EID 50) and smaller amounts cloacally. Conclusions Dunlin are highly susceptible to infection with HPAIV H5N1. They become infected after exposure to relatively small doses of the virus and if they become infected, they are most likely to suffer mortality within 3-5 days. These results have important implications regarding the risks of transport and transmission of HPAIV H5N1 to North America by this species and raises questions for further investigation.

Research paper thumbnail of Evidence for common ancestry among viruses isolated from wild birds in Beringia and highly pathogenic intercontinental reassortant H5N1 and H5N2 influenza A viruses

Infection, Genetics and Evolution, 2016

Highly pathogenic clade 2.3.4.4 H5N8, H5N2, and H5N1 influenza A viruses were first detected in w... more Highly pathogenic clade 2.3.4.4 H5N8, H5N2, and H5N1 influenza A viruses were first detected in wild, captive, and domestic birds in North America in November-December 2014. In this study, we used wild waterbird samples collected in Alaska prior to the initial detection of clade 2.3.4.4 H5 influenza A viruses in North America to assess the evidence for: (1) dispersal of highly pathogenic influenza A viruses from East Asia to North America by migratory birds via Alaska and (2) ancestral origins of clade 2.3.4.4 H5 reassortant viruses in Beringia. Although we did not detect highly pathogenic influenza A viruses in our sample collection from western Alaska, we did identify viruses that contained gene segments sharing recent common ancestry with intercontinental reassortant H5N2 and H5N1 viruses. Results of phylogenetic analyses and estimates for times of most recent common ancestry support migratory birds sampled in Beringia as maintaining viral diversity closely related to the novel highly pathogenic influenza A virus genotypes detected in North America. Although our results do not elucidate the route by which highly pathogenic influenza A viruses were introduced into North America, genetic evidence is consistent with the hypothesized trans-Beringian route of introduction via migratory birds.

Research paper thumbnail of Avian Influenza Ecology in North Atlantic Sea Ducks: Not All Ducks Are Created Equal

PloS one, 2015

Wild waterfowl are primary reservoirs of avian influenza viruses (AIV). However the role of sea d... more Wild waterfowl are primary reservoirs of avian influenza viruses (AIV). However the role of sea ducks in the ecology of avian influenza, and how that role differs from freshwater ducks, has not been examined. We obtained and analyzed sera from North Atlantic sea ducks and determined the seroprevalence in those populations. We also tested swab samples from North Atlantic sea ducks for the presence of AIV. We found relatively high serological prevalence (61%) in these sea duck populations but low virus prevalence (0.3%). Using these data we estimated that an antibody half-life of 141 weeks (3.2 years) would be required to attain these prevalences. These findings are much different than what is known in freshwater waterfowl and have implications for surveillance efforts, AIV in marine environments, and the roles of sea ducks and other long-lived waterfowl in avian influenza ecology.

Research paper thumbnail of Experimental Challenge of a Peridomestic Avian Species, European Starlings ( Sturnus vulgaris ), with Novel Influenza A H7N9 Virus from China

Journal of wildlife diseases, Jan 10, 2016

In 2013 a novel avian influenza H7N9 virus was isolated from several critically ill patients in C... more In 2013 a novel avian influenza H7N9 virus was isolated from several critically ill patients in China, and infection with this virus has since caused more than 200 human deaths. Live poultry markets are the likely locations of virus exposure to humans. Peridomestic avian species also may play important roles in the transmission and maintenance of H7N9 at live poultry markets. We experimentally challenged wild European Starlings ( Sturnus vulgaris ) with the novel H7N9 virus and measured virus excretion, clinical signs, and infectious dose. We found that European Starlings can be infected with this virus when inoculated with relatively high doses, and we predict that infected birds excrete sufficient amounts of virus to transmit to other birds, including domestic chickens. Infected European Starlings showed no clinical signs or mortality after infection with H7N9. This abundant peridomestic bird may be a source of the novel H7N9 virus in live poultry markets and may have roles in vir...

Research paper thumbnail of Experimental Infection of a North American Raptor, American Kestrel (Falco sparverius), with Highly Pathogenic Avian Influenza Virus (H5N1)

PLoS ONE, 2009

Several species of wild raptors have been found in Eurasia infected with highly pathogenic avian ... more Several species of wild raptors have been found in Eurasia infected with highly pathogenic avian influenza virus (HPAIV) subtype H5N1. Should HPAIV (H5N1) reach North America in migratory birds, species of raptors are at risk not only from environmental exposure, but also from consuming infected birds and carcasses. In this study we used American kestrels as a representative species of a North American raptor to examine the effects of HPAIV (H5N1) infection in terms of dose response, viral shedding, pathology, and survival. Our data showed that kestrels are highly susceptible to HPAIV (H5N1). All birds typically died or were euthanized due to severe neurologic disease within 4-5 days of inoculation and shed significant amounts of virus both orally and cloacally, regardless of dose administered. The most consistent microscopic lesions were necrosis in the brain and pancreas. This is the first experimental study of HPAIV infection in a North American raptor and highlights the potential risks to birds of prey if HPAIV (H5N1) is introduced into North America.

Research paper thumbnail of Avian Influenza Ecology in North Atlantic Sea Ducks: Not All Ducks Are Created Equal

Wild waterfowl are primary reservoirs of avian influenza viruses (AIV). However the role of sea d... more Wild waterfowl are primary reservoirs of avian influenza viruses (AIV). However the role of sea ducks in the ecology of avian influenza, and how that role differs from freshwater ducks, has not been examined. We obtained and analyzed sera from North Atlantic sea ducks and determined the seroprevalence in those populations. We also tested swab samples from North Atlantic sea ducks for the presence of AIV. We found relatively high serological prevalence (61%) in these sea duck populations but low virus prevalence (0.3%). Using these data we estimated that an antibody half-life of 141 weeks (3.2 years) would be required to attain these prevalences. These findings are much different than what is known in freshwater waterfowl and have implications for surveillance efforts, AIV in marine environments, and the roles of sea ducks and other long-lived waterfowl in avian influenza ecology.

Research paper thumbnail of Dispersal of H9N2 influenza A viruses between East Asia and North America by wild birds

Virology, Jan 27, 2015

Samples were collected from wild birds in western Alaska to assess dispersal of influenza A virus... more Samples were collected from wild birds in western Alaska to assess dispersal of influenza A viruses between East Asia and North America. Two isolates shared nearly identical nucleotide identity at eight genomic segments with H9N2 viruses isolated from China and South Korea providing evidence for intercontinental dispersal by migratory birds.

Research paper thumbnail of Highly pathogenic avian influenza virus H5N2 (clade 2.3.4.4) challenge of mallards age appropriate to the 2015 midwestern poultry outbreak

Influenza and Other Respiratory Viruses, 2021

BackgroundThe 2015 highly pathogenic avian influenza virus (HPAIV) H5N2 clade 2.3.4.4 outbreak in... more BackgroundThe 2015 highly pathogenic avian influenza virus (HPAIV) H5N2 clade 2.3.4.4 outbreak in upper midwestern U.S. poultry operations was not detected in wild birds to any great degree during the outbreak, despite wild waterfowl being implicated in the introduction, reassortment, and movement of the virus into North America from Asia. This outbreak led to the demise of over 50 million domestic birds and occurred mainly during the northward spring migration of adult avian populations.ObjectivesThere have been no experimental examinations of the pathogenesis, transmission, and population impacts of this virus in adult wild waterfowl with varying exposure histories—the most relevant age class.MethodsWe captured, housed, and challenged adult wild mallards (Anas platyrhynchos) with HPAIV H5N2 clade 2.3.4.4 and measured viral infection, viral excretion, and transmission to other mallards.ResultsAll inoculated birds became infected and excreted moderate amounts of virus, primarily ora...

Research paper thumbnail of Experimental Infection of Fox Squirrels (Sciurus Niger) with West Nile Virus

The American Journal of Tropical Medicine and Hygiene, 2006

Research paper thumbnail of Influenza Exposure in United States Feral Swine Populations

Journal of Wildlife Diseases, 2008

Swine play an important role in the disease ecology of influenza. Having cellular receptors in co... more Swine play an important role in the disease ecology of influenza. Having cellular receptors in common with birds and humans, swine provide opportunities for mixed infections and potential for genetic reassortment between avian, human, and porcine influenza. Feral swine populations are rapidly expanding in both numbers and range and are increasingly coming into contact with waterfowl, humans, and agricultural operations. In this study, over 875 feral swine were sampled from six states across the United States for serologic evidence of exposure to influenza. In Oklahoma, Florida, and Missouri, USA, no seropositive feral swine were detected. Seropositive swine were detected in California, Mississippi, and Texas, USA. Antibody prevalences in these states were 1% in Mississippi, 5% in California, and 14.4% in Texas. All seropositive swine were exposed to H3N2 subtype, the predominant subtype currently circulating in domestic swine. The only exceptions were in San Saba County, Texas, where of the 15 seropositive samples, four were positive for H1N1 and seven for both H1N1 and H3N2. In Texas, there was large geographical and temporal variation in antibody prevalence and no obvious connection to domestic swine operations. No evidence of exposure to avian influenza in feral swine was uncovered. From these results it is apparent that influenza in feral swine poses a risk primarily to swine production operations. However, because feral swine share habitat with waterfowl, prey on and scavenge dead and dying birds, are highly mobile, and are increasingly coming into contact with humans, the potential for these animals to become infected with avian or human influenza in addition to swine influenza is a distinct possibility.

Research paper thumbnail of Tissues from American kestrels experimentally inoculated with highly pathogenic avian influenza virus H5N1

<p>A. Pancreas with multifocal to coalescing areas of necrosis (arrows) (HE stain). B. Brai... more <p>A. Pancreas with multifocal to coalescing areas of necrosis (arrows) (HE stain). B. Brain with multifocal cerebral necrosis (arrows) accompanied by a mild infiltration of heterophils (HE stain). C. Section of same pancreatic tissue as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0007555#pone-0007555-g002&quot; target="_blank">Fig. 2A</a>, stained by immunohistochemistry to identify influenza A virus antigen. Staining of influenza A antigen is intense in areas of necrosis (arrows). D. Immunohistochemical staining of influenza A virus antigen in brain tissue. Areas of brain necrosis are strongly positive (arrows).</p

Research paper thumbnail of Influenza A virus recovery, diversity, and intercontinental exchange: A multi-year assessment of wild bird sampling at Izembek National Wildlife Refuge, Alaska

PloS one, 2018

Western Alaska is a potential point-of-entry for foreign-origin influenza A viruses (IAVs) into N... more Western Alaska is a potential point-of-entry for foreign-origin influenza A viruses (IAVs) into North America via migratory birds. We sampled waterfowl and gulls for IAVs at Izembek National Wildlife Refuge (NWR) in western Alaska, USA, during late summer and autumn months of 2011-2015, to evaluate the abundance and diversity of viruses at this site. We collected 4842 samples across five years from 25 species of wild birds resulting in the recovery, isolation, and sequencing of 172 IAVs. With the intent of optimizing sampling efficiencies, we used information derived from this multi-year effort to: 1) evaluate from which species we consistently recover viruses, 2) describe viral subtypes of isolates by host species and year, 3) characterize viral gene segment sequence diversity with respect to host species, and assess potential differences in the viral lineages among the host groups, and 4) examine how evidence of intercontinental exchange of IAVs relates to host species. We consist...

Research paper thumbnail of Prevalence and Distribution of Wellfleet Bay Virus Exposure in the Common Eider (Somateria Mollissima)

Journal of Wildlife Diseases, 2017

BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access t... more BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access titles in the biological, ecological, and environmental sciences published by nonprofit societies, associations, museums, institutions, and presses.

Research paper thumbnail of No Evidence of Infection or Exposure to Highly Pathogenic Avian Influenzas in Peridomestic Wildlife on an Affected Poultry Facility

Journal of wildlife diseases, Jan 31, 2016

We evaluated the potential transmission of avian influenza viruses (AIV) in wildlife species in ... more We evaluated the potential transmission of avian influenza viruses (AIV) in wildlife species in three settings in association with an outbreak at a poultry facility: 1) small birds and small mammals on a poultry facility that was affected with highly pathogenic AIV (HPAIV) in April 2015; 2) small birds and small mammals on a nearby poultry facility that was unaffected by HPAIV; and 3) small birds, small mammals, and waterfowl in a nearby natural area. We live-captured small birds and small mammals and collected samples from hunter-harvested waterfowl to test for active viral shedding and evidence of exposure (serum antibody) to AIV and the H5N2 HPAIV that affected the poultry facility. We detected no evidence of shedding or specific antibody to AIV in small mammals and small birds 5 mo after depopulation of the poultry. We detected viral shedding and exposure to AIV in waterfowl and estimated approximately 15% viral shedding and 60% antibody prevalence. In waterfowl, we did not det...

Research paper thumbnail of Antigenic Characterization of H3 Subtypes of Avian Influenza A Viruses from North America

Avian Diseases, 2016

Besides humans, H3 subtypes of influenza A viruses (IAVs) can infect various animal hosts, includ... more Besides humans, H3 subtypes of influenza A viruses (IAVs) can infect various animal hosts, including avian, swine, equine, canine, and sea mammal species. These H3 viruses are both antigenically and genetically diverse. Here, we characterized the antigenic diversity of contemporary H3 avian IAVs recovered from migratory birds in North America. Hemagglutination inhibition (HI) assays were performed on 37 H3 isolates of avian IAVs recovered from 2007 to 2011 using generated reference chicken sera. These isolates were recovered from samples taken in the Atlantic, Mississippi, Central, and Pacific waterfowl migration flyways. Antisera to all the tested H3 isolates cross-reacted with each other and, to a lesser extent, with those to H3 canine and H3 equine IAVs. Antigenic cartography showed that the largest antigenic distance among the 37 avian IAVs is about four units, and each unit corresponds to a 2 log  2 difference in the HI titer. However, none of the tested H3 IAVs cross-reacted with ferret sera derived from contemporary swine and human IAVs. Our results showed that the H3 avian IAVs we tested lacked significant antigenic diversity, and these viruses were antigenically different from those circulating in swine and human populations. This suggests that H3 avian IAVs in North American waterfowl are antigenically relatively stable.

Research paper thumbnail of Limited evidence of intercontinental dispersal of avian paramyxovirus serotype 4 by migratory birds

Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases, Jun 27, 2016

Avian paramyxovirus serotype 4 (APMV-4) is a single stranded RNA virus that has most often been i... more Avian paramyxovirus serotype 4 (APMV-4) is a single stranded RNA virus that has most often been isolated from waterfowl. Limited information has been reported regarding the prevalence, pathogenicity, and genetic diversity of AMPV-4. To assess the intercontinental dispersal of this viral agent, we sequenced the fusion gene of 58 APMV-4 isolates collected in the United States, Japan and the Ukraine and compared them to all available sequences on GenBank. With only a single exception the phylogenetic clades of APMV-4 sequences were monophyletic with respect to their continents of origin (North America, Asia and Europe). Thus, we detected limited evidence for recent intercontinental dispersal of APMV-4 in this study.

Research paper thumbnail of Demographic and Spatiotemporal Patterns of Avian Influenza Infection at the Continental Scale, and in Relation to Annual Life Cycle of a Migratory Host

PLOS ONE, 2015

Since the spread of highly pathogenic avian influenza (HPAI) H5N1 in the eastern hemisphere, nume... more Since the spread of highly pathogenic avian influenza (HPAI) H5N1 in the eastern hemisphere, numerous surveillance programs and studies have been undertaken to detect the occurrence, distribution, or spread of avian influenza viruses (AIV) in wild bird populations worldwide. To identify demographic determinants and spatiotemporal patterns of AIV infection in long distance migratory waterfowl in North America, we fitted generalized linear models with binominal distribution to analyze results from 13,574 blue-winged teal (Anas discors, BWTE) sampled in 2007 to 2010 year round during AIV surveillance programs in Canada and the United States. Our analyses revealed that during late summer staging (July-August) and fall migration (September-October), hatch year (HY) birds were more likely to be infected than after hatch year (AHY) birds, however there was no difference between age categories for the remainder of the year (winter, spring migration, and breeding period), likely due to maturing immune systems and newly acquired immunity of HY birds. Probability of infection increased non-linearly with latitude, and was highest in late summer prior to fall migration when densities of birds and the proportion of susceptible HY birds in the population are highest. Birds in the Central and Mississippi flyways were more likely to be infected compared to those in the Atlantic flyway. Seasonal cycles and spatial variation of AIV infection were largely driven by the dynamics of AIV infection in HY birds,

Research paper thumbnail of Rapidly Expanding Range of Highly Pathogenic Avian Influenza Viruses

Emerging Infectious Diseases, 2015

The movement of highly pathogenic avian influenza (H5N8) virus across Eurasia and into North Amer... more The movement of highly pathogenic avian influenza (H5N8) virus across Eurasia and into North America and the virus' propensity to reassort with co-circulating low pathogenicity viruses raise concerns among poultry producers, wildlife biologists, aviculturists, and public health personnel worldwide. Surveillance, modeling, and experimental research will provide the knowledge required for intelligent policy and management decisions.

Research paper thumbnail of Respiratory transmission of an avian H3N8 influenza virus isolated from a harbour seal

Nature Communications, 2014

The ongoing human H7N9 influenza infections highlight the threat of emerging avian influenza viru... more The ongoing human H7N9 influenza infections highlight the threat of emerging avian influenza viruses. In 2011, an avian H3N8 influenza virus isolated from moribund New England harbour seals was shown to have naturally acquired mutations known to increase the transmissibility of highly pathogenic H5N1 influenza viruses. To elucidate the potential human health threat, here we evaluate a panel of avian H3N8 viruses and find that the harbour seal virus displays increased affinity for mammalian receptors, transmits via respiratory droplets in ferrets and replicates in human lung cells. Analysis of a panel of human sera for H3N8 neutralizing antibodies suggests that there is no population-wide immunity to these viruses. The prevalence of H3N8 viruses in birds and multiple mammalian species including recent isolations from pigs and evidence that it was a past human pandemic virus make the need for surveillance and risk analysis of these viruses of public health importance.

Research paper thumbnail of Evolution of a reassortant North American gull influenza virus lineage: drift, shift and stability

Virology Journal, 2013

Background: The role of gulls in the ecology of avian influenza (AI) is different than that of wa... more Background: The role of gulls in the ecology of avian influenza (AI) is different than that of waterfowl. Different constellations of subtypes circulate within the two groups of birds and AI viruses isolated from North American gulls frequently possess reassortant genomes with genetic elements from both North America and Eurasian lineages. A 2008 isolate from a Newfoundland Great Black-backed Gull contained a mix of North American waterfowl, North American gull and Eurasian lineage genes. Methods: We isolated, sequenced and phylogenetically compared avian influenza viruses from 2009 Canadian wild birds. Results: We analyzed six 2009 virus isolates from Canada and found the same phylogenetic lineage had persisted over a larger geographic area, with an expanded host range that included dabbling and diving ducks as well as gulls. All of the 2009 virus isolates contained an internal protein coding set of genes of the same Eurasian lineage genes except PB1 that was from a North American lineage, and these genes continued to evolve by genetic drift. We show evidence that the 2008 Great Black-backed Gull virus was derived from this lineage with a reassortment of a North American PA gene into the more stable core set of internal protein coding genes that has circulated in avian populations for at least 2 years. From this core, the surface glycoprotein genes have switched several times creating H13N6, H13N2, and H16N3 subtypes. These gene segments were from North American lineages except for the H16 and N3 vRNAs. Conclusions: This process appears similar to genetic shifts seen with swine influenza where a stable "triple reassortant internal gene" core has circulated in swine populations with genetic shifts occurring with hemaggluttinin and neuraminidase proteins getting periodically switched. Thus gulls may serve as genetic mixing vessels for different lineages of avian influenza, similar to the role of swine with regards to human influenza. These findings illustrate the need for continued surveillance in gull and waterfowl populations, both on the Pacific and especially Atlantic coasts of North America, to document virus intercontinental movement and the role of gull species in the evolution and epidemiology of AI.

Research paper thumbnail of Experimental challenge and pathology of highly pathogenic avian influenza virus H5N1 in dunlin (Calidris alpina), an intercontinental migrant shorebird species

Influenza and Other Respiratory Viruses, 2011

Background Shorebirds (Charadriiformes) are considered one of the primary reservoirs of avian inf... more Background Shorebirds (Charadriiformes) are considered one of the primary reservoirs of avian influenza. Because these species are highly migratory, there is concern that infected shorebirds may be a mechanism by which highly pathogenic avian influenza virus (HPAIV) H5N1 could be introduced into North America from Asia. Large numbers of dunlin (Calidris alpina) migrate from wintering areas in central and eastern Asia, where HPAIV H5N1 is endemic, across the Bering Sea to breeding areas in Alaska. Low pathogenic avian influenza virus has been previously detected in dunlin, and thus, dunlin represent a potential risk to transport HPAIV to North America. To date no experimental challenge studies have been performed in shorebirds. Methods Wild dunlin were inoculated intranasally and intrachoanally various doses of HPAIV H5N1. The birds were monitored daily for virus excretion, disease signs, morbidity, and mortality. Results The infectious dose of HPAIV H5N1 in dunlin was determined to be 10 1.7 EID 50 /100 ll and that the lethal dose was 10 1.83 EID 50 /100 ll. Clinical signs were consistent with neurotropic disease, and histochemical analyses revealed that infection was systemic with viral antigen and RNA most consistently found in brain tissues. Infected birds excreted relatively large amounts of virus orally (10 4 EID 50) and smaller amounts cloacally. Conclusions Dunlin are highly susceptible to infection with HPAIV H5N1. They become infected after exposure to relatively small doses of the virus and if they become infected, they are most likely to suffer mortality within 3-5 days. These results have important implications regarding the risks of transport and transmission of HPAIV H5N1 to North America by this species and raises questions for further investigation.

Research paper thumbnail of Evidence for common ancestry among viruses isolated from wild birds in Beringia and highly pathogenic intercontinental reassortant H5N1 and H5N2 influenza A viruses

Infection, Genetics and Evolution, 2016

Highly pathogenic clade 2.3.4.4 H5N8, H5N2, and H5N1 influenza A viruses were first detected in w... more Highly pathogenic clade 2.3.4.4 H5N8, H5N2, and H5N1 influenza A viruses were first detected in wild, captive, and domestic birds in North America in November-December 2014. In this study, we used wild waterbird samples collected in Alaska prior to the initial detection of clade 2.3.4.4 H5 influenza A viruses in North America to assess the evidence for: (1) dispersal of highly pathogenic influenza A viruses from East Asia to North America by migratory birds via Alaska and (2) ancestral origins of clade 2.3.4.4 H5 reassortant viruses in Beringia. Although we did not detect highly pathogenic influenza A viruses in our sample collection from western Alaska, we did identify viruses that contained gene segments sharing recent common ancestry with intercontinental reassortant H5N2 and H5N1 viruses. Results of phylogenetic analyses and estimates for times of most recent common ancestry support migratory birds sampled in Beringia as maintaining viral diversity closely related to the novel highly pathogenic influenza A virus genotypes detected in North America. Although our results do not elucidate the route by which highly pathogenic influenza A viruses were introduced into North America, genetic evidence is consistent with the hypothesized trans-Beringian route of introduction via migratory birds.

Research paper thumbnail of Avian Influenza Ecology in North Atlantic Sea Ducks: Not All Ducks Are Created Equal

PloS one, 2015

Wild waterfowl are primary reservoirs of avian influenza viruses (AIV). However the role of sea d... more Wild waterfowl are primary reservoirs of avian influenza viruses (AIV). However the role of sea ducks in the ecology of avian influenza, and how that role differs from freshwater ducks, has not been examined. We obtained and analyzed sera from North Atlantic sea ducks and determined the seroprevalence in those populations. We also tested swab samples from North Atlantic sea ducks for the presence of AIV. We found relatively high serological prevalence (61%) in these sea duck populations but low virus prevalence (0.3%). Using these data we estimated that an antibody half-life of 141 weeks (3.2 years) would be required to attain these prevalences. These findings are much different than what is known in freshwater waterfowl and have implications for surveillance efforts, AIV in marine environments, and the roles of sea ducks and other long-lived waterfowl in avian influenza ecology.

Research paper thumbnail of Experimental Challenge of a Peridomestic Avian Species, European Starlings ( Sturnus vulgaris ), with Novel Influenza A H7N9 Virus from China

Journal of wildlife diseases, Jan 10, 2016

In 2013 a novel avian influenza H7N9 virus was isolated from several critically ill patients in C... more In 2013 a novel avian influenza H7N9 virus was isolated from several critically ill patients in China, and infection with this virus has since caused more than 200 human deaths. Live poultry markets are the likely locations of virus exposure to humans. Peridomestic avian species also may play important roles in the transmission and maintenance of H7N9 at live poultry markets. We experimentally challenged wild European Starlings ( Sturnus vulgaris ) with the novel H7N9 virus and measured virus excretion, clinical signs, and infectious dose. We found that European Starlings can be infected with this virus when inoculated with relatively high doses, and we predict that infected birds excrete sufficient amounts of virus to transmit to other birds, including domestic chickens. Infected European Starlings showed no clinical signs or mortality after infection with H7N9. This abundant peridomestic bird may be a source of the novel H7N9 virus in live poultry markets and may have roles in vir...

Research paper thumbnail of Experimental Infection of a North American Raptor, American Kestrel (Falco sparverius), with Highly Pathogenic Avian Influenza Virus (H5N1)

PLoS ONE, 2009

Several species of wild raptors have been found in Eurasia infected with highly pathogenic avian ... more Several species of wild raptors have been found in Eurasia infected with highly pathogenic avian influenza virus (HPAIV) subtype H5N1. Should HPAIV (H5N1) reach North America in migratory birds, species of raptors are at risk not only from environmental exposure, but also from consuming infected birds and carcasses. In this study we used American kestrels as a representative species of a North American raptor to examine the effects of HPAIV (H5N1) infection in terms of dose response, viral shedding, pathology, and survival. Our data showed that kestrels are highly susceptible to HPAIV (H5N1). All birds typically died or were euthanized due to severe neurologic disease within 4-5 days of inoculation and shed significant amounts of virus both orally and cloacally, regardless of dose administered. The most consistent microscopic lesions were necrosis in the brain and pancreas. This is the first experimental study of HPAIV infection in a North American raptor and highlights the potential risks to birds of prey if HPAIV (H5N1) is introduced into North America.

Research paper thumbnail of Avian Influenza Ecology in North Atlantic Sea Ducks: Not All Ducks Are Created Equal

Wild waterfowl are primary reservoirs of avian influenza viruses (AIV). However the role of sea d... more Wild waterfowl are primary reservoirs of avian influenza viruses (AIV). However the role of sea ducks in the ecology of avian influenza, and how that role differs from freshwater ducks, has not been examined. We obtained and analyzed sera from North Atlantic sea ducks and determined the seroprevalence in those populations. We also tested swab samples from North Atlantic sea ducks for the presence of AIV. We found relatively high serological prevalence (61%) in these sea duck populations but low virus prevalence (0.3%). Using these data we estimated that an antibody half-life of 141 weeks (3.2 years) would be required to attain these prevalences. These findings are much different than what is known in freshwater waterfowl and have implications for surveillance efforts, AIV in marine environments, and the roles of sea ducks and other long-lived waterfowl in avian influenza ecology.

Research paper thumbnail of Dispersal of H9N2 influenza A viruses between East Asia and North America by wild birds

Virology, Jan 27, 2015

Samples were collected from wild birds in western Alaska to assess dispersal of influenza A virus... more Samples were collected from wild birds in western Alaska to assess dispersal of influenza A viruses between East Asia and North America. Two isolates shared nearly identical nucleotide identity at eight genomic segments with H9N2 viruses isolated from China and South Korea providing evidence for intercontinental dispersal by migratory birds.