Species-specific emergence of H7 highly pathogenic avian influenza virus is driven by intrahost selection differences between chickens and ducks

Highly pathogenic avian influenza viruses (HPAIVs) cause severe hemorrhagic disease in terrestrial poultry and are a threat to the poultry industry, wild life, and human health. HPAIVs arise from low pathogenic avian influenza viruses (LPAIVs), which circulate in wild aquatic birds. HPAIV emergence...

Full description

Saved in:
Bibliographic Details
Published inPLoS pathogens Vol. 20; no. 2; p. e1011942
Main Authors de Bruin, Anja C. M., Spronken, Monique I., Kok, Adinda, Rosu, Miruna E., de Meulder, Dennis, van Nieuwkoop, Stefan, Lexmond, Pascal, Funk, Mathis, Leijten, Lonneke M., Bestebroer, Theo M., Herfst, Sander, van Riel, Debby, Fouchier, Ron A. M., Richard, Mathilde
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.02.2024
Public Library of Science (PLoS)
Subjects
Animals
Animals, Wild
Aquatic birds
Avian flu
Biology and Life Sciences
Chickens
Drinking water
Ducks
Ecology and Environmental Sciences
Epitopes
Fibroblasts
Flow cytometry
Hemagglutinins
Hemorrhagic disease
Humans
Hypotheses
Infections
Influenza
Influenza A virus - genetics
Influenza A Virus, H7N7 Subtype
Influenza in Birds
Medicine and Health Sciences
Orthomyxoviridae
Peptides
Poultry
Poultry Diseases
Proteins
Replication
Systemic diseases
Tropism
Viruses
Waterfowl
Wildfowl
Netherlands
Online AccessGet full text

Cover

Abstract Highly pathogenic avian influenza viruses (HPAIVs) cause severe hemorrhagic disease in terrestrial poultry and are a threat to the poultry industry, wild life, and human health. HPAIVs arise from low pathogenic avian influenza viruses (LPAIVs), which circulate in wild aquatic birds. HPAIV emergence is thought to occur in poultry and not wild aquatic birds, but the reason for this species-restriction is not known. We hypothesized that, due to species-specific tropism and replication, intrahost HPAIV selection is favored in poultry and disfavored in wild aquatic birds. We tested this hypothesis by co-inoculating chickens, representative of poultry, and ducks, representative of wild aquatic birds, with a mixture of H7N7 HPAIV and LPAIV, mimicking HPAIV emergence in an experimental setting. Virus selection was monitored in swabs and tissues by RT-qPCR and immunostaining of differential N-terminal epitope tags that were added to the hemagglutinin protein. HPAIV was selected in four of six co-inoculated chickens, whereas LPAIV remained the major population in co-inoculated ducks on the long-term, despite detection of infectious HPAIV in tissues at early time points. Collectively, our data support the hypothesis that HPAIVs are more likely to be selected at the intrahost level in poultry than in wild aquatic birds and point towards species-specific differences in HPAIV and LPAIV tropism and replication levels as possible explanations.
AbstractList Highly pathogenic avian influenza viruses (HPAIVs) cause severe hemorrhagic disease in terrestrial poultry and are a threat to the poultry industry, wild life, and human health. HPAIVs arise from low pathogenic avian influenza viruses (LPAIVs), which circulate in wild aquatic birds. HPAIV emergence is thought to occur in poultry and not wild aquatic birds, but the reason for this species-restriction is not known. We hypothesized that, due to species-specific tropism and replication, intrahost HPAIV selection is favored in poultry and disfavored in wild aquatic birds. We tested this hypothesis by co-inoculating chickens, representative of poultry, and ducks, representative of wild aquatic birds, with a mixture of H7N7 HPAIV and LPAIV, mimicking HPAIV emergence in an experimental setting. Virus selection was monitored in swabs and tissues by RT-qPCR and immunostaining of differential N-terminal epitope tags that were added to the hemagglutinin protein. HPAIV was selected in four of six co-inoculated chickens, whereas LPAIV remained the major population in co-inoculated ducks on the long-term, despite detection of infectious HPAIV in tissues at early time points. Collectively, our data support the hypothesis that HPAIVs are more likely to be selected at the intrahost level in poultry than in wild aquatic birds and point towards species-specific differences in HPAIV and LPAIV tropism and replication levels as possible explanations.
Highly pathogenic avian influenza viruses (HPAIVs) cause severe hemorrhagic disease in terrestrial poultry and are a threat to the poultry industry, wild life, and human health. HPAIVs arise from low pathogenic avian influenza viruses (LPAIVs), which circulate in wild aquatic birds. HPAIV emergence is thought to occur in poultry and not wild aquatic birds, but the reason for this species-restriction is not known. We hypothesized that, due to species-specific tropism and replication, intrahost HPAIV selection is favored in poultry and disfavored in wild aquatic birds. We tested this hypothesis by co-inoculating chickens, representative of poultry, and ducks, representative of wild aquatic birds, with a mixture of H7N7 HPAIV and LPAIV, mimicking HPAIV emergence in an experimental setting. Virus selection was monitored in swabs and tissues by RT-qPCR and immunostaining of differential N-terminal epitope tags that were added to the hemagglutinin protein. HPAIV was selected in four of six co-inoculated chickens, whereas LPAIV remained the major population in co-inoculated ducks on the long-term, despite detection of infectious HPAIV in tissues at early time points. Collectively, our data support the hypothesis that HPAIVs are more likely to be selected at the intrahost level in poultry than in wild aquatic birds and point towards species-specific differences in HPAIV and LPAIV tropism and replication levels as possible explanations.Highly pathogenic avian influenza viruses (HPAIVs) cause severe hemorrhagic disease in terrestrial poultry and are a threat to the poultry industry, wild life, and human health. HPAIVs arise from low pathogenic avian influenza viruses (LPAIVs), which circulate in wild aquatic birds. HPAIV emergence is thought to occur in poultry and not wild aquatic birds, but the reason for this species-restriction is not known. We hypothesized that, due to species-specific tropism and replication, intrahost HPAIV selection is favored in poultry and disfavored in wild aquatic birds. We tested this hypothesis by co-inoculating chickens, representative of poultry, and ducks, representative of wild aquatic birds, with a mixture of H7N7 HPAIV and LPAIV, mimicking HPAIV emergence in an experimental setting. Virus selection was monitored in swabs and tissues by RT-qPCR and immunostaining of differential N-terminal epitope tags that were added to the hemagglutinin protein. HPAIV was selected in four of six co-inoculated chickens, whereas LPAIV remained the major population in co-inoculated ducks on the long-term, despite detection of infectious HPAIV in tissues at early time points. Collectively, our data support the hypothesis that HPAIVs are more likely to be selected at the intrahost level in poultry than in wild aquatic birds and point towards species-specific differences in HPAIV and LPAIV tropism and replication levels as possible explanations.
Highly pathogenic avian influenza viruses (HPAIVs) cause severe hemorrhagic disease in terrestrial poultry and are a threat to the poultry industry, wild life, and human health. HPAIVs arise from low pathogenic avian influenza viruses (LPAIVs), which circulate in wild aquatic birds. HPAIV emergence is thought to occur in poultry and not wild aquatic birds, but the reason for this species-restriction is not known. We hypothesized that, due to species-specific tropism and replication, intrahost HPAIV selection is favored in poultry and disfavored in wild aquatic birds. We tested this hypothesis by co-inoculating chickens, representative of poultry, and ducks, representative of wild aquatic birds, with a mixture of H7N7 HPAIV and LPAIV, mimicking HPAIV emergence in an experimental setting. Virus selection was monitored in swabs and tissues by RT-qPCR and immunostaining of differential N-terminal epitope tags that were added to the hemagglutinin protein. HPAIV was selected in four of six co-inoculated chickens, whereas LPAIV remained the major population in co-inoculated ducks on the long-term, despite detection of infectious HPAIV in tissues at early time points. Collectively, our data support the hypothesis that HPAIVs are more likely to be selected at the intrahost level in poultry than in wild aquatic birds and point towards species-specific differences in HPAIV and LPAIV tropism and replication levels as possible explanations. Highly pathogenic avian influenza viruses (HPAIVs) cause severe disease in poultry with mortality rates reaching 100% and, therefore, pose a large burden on the poultry industry. Additionally, some HPAIVs have spilled back from poultry into wild bird populations, increasing their geographic spread. HPAIVs arise from low pathogenic avian influenza viruses (LPAIVs), which circulate in wild aquatic birds and occasionally spillover into poultry. LPAIV to HPAIV conversion is associated with terrestrial poultry species, but the reasons underlying this species-restriction are unknown. The second step of HPAIV emergence, following HPAIV genesis, constitutes of the intrahost selection of the HPAIV from the large pool of replicating LPAIVs. Here, we investigated whether the intrahost selection efficiency differs between chickens and ducks, models for poultry and wild aquatic birds respectively, by co-inoculating them with HPAIV and LPAIV. Tagged viruses were utilized to monitor LPAIV and HPAIV frequencies at both the RNA and protein level. The HPAIV was selected in a majority of the chickens, demonstrated by the development of canonical HPAI disease and infectious HPAIV shedding, whereas all ducks solely shed infectious LPAIV. These results confirm that intrahost selection of HPAIVs is species-specific, which likely contributes to the restriction of HPAIV-emergence to poultry populations.
Author Spronken, Monique I.
van Riel, Debby
de Meulder, Dennis
Herfst, Sander
van Nieuwkoop, Stefan
Lexmond, Pascal
de Bruin, Anja C. M.
Kok, Adinda
Fouchier, Ron A. M.
Rosu, Miruna E.
Bestebroer, Theo M.
Funk, Mathis
Leijten, Lonneke M.
Richard, Mathilde
AuthorAffiliation Department of Viroscience, Erasmus Medical Center, Rotterdam, The Netherlands
University of Georgia, UNITED STATES
AuthorAffiliation_xml – name: Department of Viroscience, Erasmus Medical Center, Rotterdam, The Netherlands
– name: University of Georgia, UNITED STATES
Author_xml – sequence: 1
  givenname: Anja C. M.
  surname: de Bruin
  fullname: de Bruin, Anja C. M.
– sequence: 2
  givenname: Monique I.
  surname: Spronken
  fullname: Spronken, Monique I.
– sequence: 3
  givenname: Adinda
  surname: Kok
  fullname: Kok, Adinda
– sequence: 4
  givenname: Miruna E.
  surname: Rosu
  fullname: Rosu, Miruna E.
– sequence: 5
  givenname: Dennis
  surname: de Meulder
  fullname: de Meulder, Dennis
– sequence: 6
  givenname: Stefan
  surname: van Nieuwkoop
  fullname: van Nieuwkoop, Stefan
– sequence: 7
  givenname: Pascal
  surname: Lexmond
  fullname: Lexmond, Pascal
– sequence: 8
  givenname: Mathis
  surname: Funk
  fullname: Funk, Mathis
– sequence: 9
  givenname: Lonneke M.
  surname: Leijten
  fullname: Leijten, Lonneke M.
– sequence: 10
  givenname: Theo M.
  surname: Bestebroer
  fullname: Bestebroer, Theo M.
– sequence: 11
  givenname: Sander
  surname: Herfst
  fullname: Herfst, Sander
– sequence: 12
  givenname: Debby
  surname: van Riel
  fullname: van Riel, Debby
– sequence: 13
  givenname: Ron A. M.
  surname: Fouchier
  fullname: Fouchier, Ron A. M.
– sequence: 14
  givenname: Mathilde
  orcidid: 0000-0003-0240-9312
  surname: Richard
  fullname: Richard, Mathilde
BackLink https://www.ncbi.nlm.nih.gov/pubmed/38408092$$D View this record in MEDLINE/PubMed
BookMark eNp9Uk1vEzEQXaEi2gb-AQJLXLgk-HM_uCBUFVqpEgd6t7z2OOt0Ywd7Nyj8Cn5yvSRBbYU4jTXz5s3zzDsvTnzwUBSvCV4QVpEPqzBGr_rFZqOGBcGENJw-K86IEGxesYqfPHifFucprTDmhJHyRXHKao5r3NCz4vf3DWgHaZ6maJ1GsIa4BK8BBYuuKtS5ZdfvUJ7ShZzPCLV1yiPnbT-C_6XQ1sUxIZeQiW4LHrW7XByi6kIaUIIe9OCCR8ZZC3FiTqiF4SdkqO6cvgOfkPIGmVHfpZfFc6v6BK8OcVbcfrm8vbia33z7en3x-WauBa2GuaBWCF2TRhgFDc7MuKqg1AQMABWWK2yhYqJkpVW21armrDYVrkta05ydFW_3tJs-JHnYZZIMlw2pacNxRlzvESaoldxEt1ZxJ4Ny8k8ixKVUcXC6B6lMVsKJUYwRTuuyFaVlbSlKo01tQGeuT4dpY7sGo2FaT_-I9HHFu04uw1YS3JCmzmebFe8PDDH8GCENcu2Shr5XHsKYJG0Y5UxwTDP03RPov7_35qGkv1qO1siAj3uAjiGlCFZqN6jpklmh67M0OfnwSC4nH8qDD3Mzf9J85P9v2z1eN-iF
CitedBy_id crossref_primary_10_1071_MA24040
crossref_primary_10_1371_journal_ppat_1012608
Cites_doi 10.1146/annurev.bi.56.070187.002053
10.3390/vetsci6010005
10.1177/030098588902600101
10.3201/eid1404.071016
10.1186/1743-422X-10-23
10.1080/03079450802499118
10.1126/science.1122438
10.4049/jimmunol.1003712
10.3201/eid1607.090389
10.1002/j.1460-2075.1992.tb05305.x
10.1128/JVI.00742-11
10.3201/eid2612.202790
10.1016/0021-9975(92)90009-J
10.3390/v14010165
10.1016/S0092-8674(00)81771-7
10.1080/03079459608419142
10.3390/genes12060901
10.1016/0042-6822(85)90059-5
10.1007/BF00362792
10.1128/JVI.78.9.4892-4901.2004
10.1111/tbed.12906
10.1128/jvi.68.5.3120-3128.1994
10.3201/eid1004.030396
10.1084/jem.78.5.407
10.3201/eid1012.040743
10.1637/7080
10.1016/S0034-5288(18)33080-7
10.1637/7260-081104R
10.3201/eid2311.171013
10.1080/03079458608436328
10.1186/s12917-019-1899-4
10.1371/journal.ppat.1003421
10.1128/JVI.79.17.11269-11279.2005
10.1073/pnas.0308352100
10.3389/fmicb.2014.00653
10.1637/9228-010410-ResNote.1
10.3390/pathogens10121597
10.3390/v14071566
10.1371/journal.pone.0177265
10.4161/rna.29730
10.1073/pnas.1001755107
10.1038/s41598-019-47938-3
10.1111/tbed.13291
10.1080/03079457.2010.492825
10.1354/vp.08-VP-0215-K-BC
10.3390/v12090920
10.1017/S0022172400040596
10.1371/journal.ppat.1000127
10.1128/jvi.68.9.6074-6078.1994
10.1128/JVI.01165-16
10.1080/03079459508419093
10.1177/0300985812469633
10.1016/j.virusres.2004.02.028
ContentType Journal Article
Copyright Copyright: © 2024 de Bruin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
2024 de Bruin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2024 de Bruin et al 2024 de Bruin et al
2024 de Bruin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Copyright_xml – notice: Copyright: © 2024 de Bruin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
– notice: 2024 de Bruin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2024 de Bruin et al 2024 de Bruin et al
– notice: 2024 de Bruin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
3V.
7QL
7U9
7X7
7XB
88E
8FE
8FH
8FI
8FJ
8FK
ABUWG
AEUYN
AFKRA
AZQEC
BBNVY
BENPR
BHPHI
C1K
CCPQU
COVID
DWQXO
FYUFA
GHDGH
GNUQQ
H94
HCIFZ
K9.
LK8
M0S
M1P
M7P
PHGZM
PHGZT
PIMPY
PJZUB
PKEHL
PPXIY
PQEST
PQGLB
PQQKQ
PQUKI
PRINS
7X8
5PM
DOA
DOI 10.1371/journal.ppat.1011942
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
ProQuest Central (Corporate)
Bacteriology Abstracts (Microbiology B)
Virology and AIDS Abstracts
Health & Medical Collection
ProQuest Central (purchase pre-March 2016)
Medical Database (Alumni Edition)
ProQuest SciTech Collection
ProQuest Natural Science Collection
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest One Sustainability
ProQuest Central UK/Ireland
ProQuest Central Essentials
Biological Science Collection
ProQuest Central
Natural Science Collection
Environmental Sciences and Pollution Management
ProQuest One
Coronavirus Research Database
ProQuest Central Korea
Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
AIDS and Cancer Research Abstracts
SciTech Premium Collection
ProQuest Health & Medical Complete (Alumni)
Biological Sciences
ProQuest Health & Medical Collection
Medical Database
Biological Science Database
ProQuest Central Premium
ProQuest One Academic (New)
Publicly Available Content Database
ProQuest Health & Medical Research Collection
ProQuest One Academic Middle East (New)
ProQuest One Health & Nursing
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Applied & Life Sciences
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central China
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
Publicly Available Content Database
ProQuest Central Student
ProQuest One Academic Middle East (New)
ProQuest Central Essentials
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest One Health & Nursing
ProQuest Natural Science Collection
ProQuest Central China
Environmental Sciences and Pollution Management
ProQuest Central
ProQuest One Applied & Life Sciences
ProQuest One Sustainability
ProQuest Health & Medical Research Collection
Health Research Premium Collection
Health and Medicine Complete (Alumni Edition)
Natural Science Collection
ProQuest Central Korea
Bacteriology Abstracts (Microbiology B)
Health & Medical Research Collection
Biological Science Collection
AIDS and Cancer Research Abstracts
ProQuest Central (New)
ProQuest Medical Library (Alumni)
Virology and AIDS Abstracts
ProQuest Biological Science Collection
ProQuest One Academic Eastern Edition
Coronavirus Research Database
ProQuest Hospital Collection
Health Research Premium Collection (Alumni)
Biological Science Database
ProQuest SciTech Collection
ProQuest Hospital Collection (Alumni)
ProQuest Health & Medical Complete
ProQuest Medical Library
ProQuest One Academic UKI Edition
ProQuest One Academic
ProQuest One Academic (New)
ProQuest Central (Alumni)
MEDLINE - Academic
DatabaseTitleList
CrossRef
MEDLINE

MEDLINE - Academic

Publicly Available Content Database
Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 3
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
– sequence: 4
  dbid: BENPR
  name: ProQuest Central
  url: https://www.proquest.com/central
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
DocumentTitleAlternate Highly pathogenic avian influenza virus intrahost selection in chickens and ducks
EISSN 1553-7374
ExternalDocumentID 3069182940
oai_doaj_org_article_adc8141da3314286b56f3b656dcd8dec
PMC10919841
38408092
10_1371_journal_ppat_1011942
Genre Journal Article
GeographicLocations Netherlands
GeographicLocations_xml – name: Netherlands
GrantInformation_xml – fundername: NIAID NIH HHS
  grantid: HHSN272201400008C
– fundername: ;
  grantid: 727922
– fundername: ;
  grantid: HHSN272201400008C
GroupedDBID ---
123
29O
2WC
53G
5VS
7X7
88E
8FE
8FH
8FI
8FJ
AAFWJ
AAUCC
AAWOE
AAYXX
ABDBF
ABUWG
ACGFO
ACIHN
ACPRK
ACUHS
ADBBV
AEAQA
AENEX
AEUYN
AFKRA
AFPKN
AFRAH
AHMBA
ALMA_UNASSIGNED_HOLDINGS
AOIJS
B0M
BAWUL
BBNVY
BCNDV
BENPR
BHPHI
BPHCQ
BVXVI
BWKFM
CCPQU
CITATION
CS3
DIK
DU5
E3Z
EAP
EAS
EBD
EMK
EMOBN
ESX
F5P
FPL
FYUFA
GROUPED_DOAJ
GX1
HCIFZ
HMCUK
HYE
IAO
IHR
INH
INR
ISN
ISR
ITC
KQ8
LK8
M1P
M48
M7P
MM.
O5R
O5S
OK1
OVT
P2P
PGMZT
PHGZM
PHGZT
PIMPY
PQQKQ
PROAC
PSQYO
PV9
QF4
QN7
RNS
RPM
RZL
SV3
TR2
TUS
UKHRP
WOW
~8M
ADRAZ
CGR
CUY
CVF
ECM
EIF
H13
IPNFZ
NPM
PJZUB
PPXIY
PQGLB
RIG
WOQ
3V.
7QL
7U9
7XB
8FK
AZQEC
C1K
COVID
DWQXO
GNUQQ
H94
K9.
PKEHL
PQEST
PQUKI
PRINS
7X8
5PM
PUEGO
M~E
ID FETCH-LOGICAL-c527t-52f55c8195dae90ffe077e6c1edee25f4a0fe735636fafbca8438d7086282563
IEDL.DBID M48
ISSN 1553-7374
1553-7366
IngestDate Fri Nov 29 00:48:05 EST 2024
Wed Aug 27 01:32:10 EDT 2025
Thu Aug 21 18:35:35 EDT 2025
Fri Jul 11 05:32:16 EDT 2025
Fri Jul 25 10:35:26 EDT 2025
Mon Jul 21 06:05:41 EDT 2025
Thu Apr 24 23:07:18 EDT 2025
Tue Jul 01 03:52:23 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 2
Language English
License Copyright: © 2024 de Bruin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Creative Commons Attribution License
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c527t-52f55c8195dae90ffe077e6c1edee25f4a0fe735636fafbca8438d7086282563
Notes new_version
ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
The authors have declared that no competing interests exist.
ORCID 0000-0003-0240-9312
OpenAccessLink http://journals.scholarsportal.info/openUrl.xqy?doi=10.1371/journal.ppat.1011942
PMID 38408092
PQID 3069182940
PQPubID 1436335
ParticipantIDs plos_journals_3069182940
doaj_primary_oai_doaj_org_article_adc8141da3314286b56f3b656dcd8dec
pubmedcentral_primary_oai_pubmedcentral_nih_gov_10919841
proquest_miscellaneous_2932435402
proquest_journals_3069182940
pubmed_primary_38408092
crossref_citationtrail_10_1371_journal_ppat_1011942
crossref_primary_10_1371_journal_ppat_1011942
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2024-02-01
PublicationDateYYYYMMDD 2024-02-01
PublicationDate_xml – month: 02
  year: 2024
  text: 2024-02-01
  day: 01
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: San Francisco
– name: San Francisco, CA USA
PublicationTitle PLoS pathogens
PublicationTitleAlternate PLoS Pathog
PublicationYear 2024
Publisher Public Library of Science
Public Library of Science (PLoS)
Publisher_xml – name: Public Library of Science
– name: Public Library of Science (PLoS)
References K Dietze (ppat.1011942.ref016) 2018; 65
N Gaidet (ppat.1011942.ref055) 2008; 4
KR Short (ppat.1011942.ref031) 2014; 5
P Bessière (ppat.1011942.ref036) 2022
DH Lee (ppat.1011942.ref018) 2017; 23
ZWM Tong (ppat.1011942.ref050) 2021; 12
DE Swayne (ppat.1011942.ref040) 2005; 49
DE Stallknecht (ppat.1011942.ref002) 1988; 12
D Scheibner (ppat.1011942.ref047) 2019; 15
B Olsen (ppat.1011942.ref001) 2006; 312
YL Jones (ppat.1011942.ref020) 2004; 48
DJ Alexander (ppat.1011942.ref044) 1978; 24
PY Daoust (ppat.1011942.ref048) 2013; 50
MS França (ppat.1011942.ref003) 2014; 385
D Evseev (ppat.1011942.ref054) 2019; 6
S Youk (ppat.1011942.ref017) 2020; 26
J Post (ppat.1011942.ref039) 2013; 10
M Richard (ppat.1011942.ref041) 2017; 14
M Hirst (ppat.1011942.ref015) 2004; 10
T Horimoto (ppat.1011942.ref005) 1994; 68
MJ Pantin-Jackwood (ppat.1011942.ref025) 2016; 90
GW Wood (ppat.1011942.ref026) 1995; 24
T Horimoto (ppat.1011942.ref011) 1994; 68
RAM Fouchier (ppat.1011942.ref033) 2004; 101
A Stieneke-Grober (ppat.1011942.ref010) 1992; 11
AR Spickler (ppat.1011942.ref007) 2008; 37
AJ Cooley (ppat.1011942.ref023) 1989; 26
KM Sturm-Ramirez (ppat.1011942.ref030) 2005; 79
MRW Barber (ppat.1011942.ref051) 2010; 107
CC Brown (ppat.1011942.ref019) 1992; 107
N Marshall (ppat.1011942.ref034) 2013; 9
M Perdue (ppat.1011942.ref009) 2003; 47
GK Hirst (ppat.1011942.ref062) 1943; 78
S-S Youk (ppat.1011942.ref032) 2019
DC Wiley (ppat.1011942.ref006) 1987; 56
C Lebarbenchon (ppat.1011942.ref058) 2010; 16
M Liniger (ppat.1011942.ref053) 2012; 86
D Scheibner (ppat.1011942.ref043) 2019; 9
ACM de Bruin (ppat.1011942.ref049) 2022; 14
E De Wit (ppat.1011942.ref060) 2004; 103
DJ Alexander (ppat.1011942.ref045) 1986; 15
A Graaf (ppat.1011942.ref035) 2018
AP Gultyaev (ppat.1011942.ref061) 2014; 11
Y Kida (ppat.1011942.ref057) 2021; 10
N Beerens (ppat.1011942.ref013) 2020; 94
MJ Pantin-Jackwood (ppat.1011942.ref024) 2017; 12
H Il Kwon (ppat.1011942.ref038) 2019; 10
AH Seekings (ppat.1011942.ref042) 2020; 12
J Chen (ppat.1011942.ref004) 1998; 95
M Nakayama (ppat.1011942.ref027) 2019; 66
Y Kawaoka (ppat.1011942.ref012) 1985; 146
KM Sturm-Ramirez (ppat.1011942.ref029) 2004; 78
AJ Karpala (ppat.1011942.ref052) 2011; 186
J Keawcharoen (ppat.1011942.ref028) 2008; 14
Y Kobayashi (ppat.1011942.ref022) 1996; 25
BS Ladman (ppat.1011942.ref037) 2010; 54
D van Riel (ppat.1011942.ref021) 2009; 46
EW Aldous (ppat.1011942.ref046) 2010; 39
M Richard (ppat.1011942.ref063) 2020; 11
DL Suarez (ppat.1011942.ref014) 2004; 10
WB Becker (ppat.1011942.ref056) 1966; 64
ACM de Bruin (ppat.1011942.ref008) 2022; 14
R Hernandez (ppat.1011942.ref059) 2010
References_xml – volume: 56
  start-page: 365
  year: 1987
  ident: ppat.1011942.ref006
  article-title: The structure and function of the hemagglutinin membrane glycoprotein of influenza virus
  publication-title: Annu Rev Biochem
  doi: 10.1146/annurev.bi.56.070187.002053
– volume: 6
  start-page: 5
  year: 2019
  ident: ppat.1011942.ref054
  article-title: Innate immune responses to avian influenza viruses in ducks and chickens.
  publication-title: Vet Sci
  doi: 10.3390/vetsci6010005
– volume: 385
  start-page: 221
  year: 2014
  ident: ppat.1011942.ref003
  article-title: Influenza pathobiology and pathogenesis in avian species
  publication-title: Curr Top Microbiol Immunol
– volume: 26
  start-page: 1
  year: 1989
  ident: ppat.1011942.ref023
  article-title: Pathological Lesions in the Lungs of Ducks Infected with Influenza A Viruses
  publication-title: Vet Pathol
  doi: 10.1177/030098588902600101
– volume: 14
  start-page: 600
  year: 2008
  ident: ppat.1011942.ref028
  article-title: Wild ducks as long-distance vectors of highly pathogenic avian influenza virus (H5N1).
  publication-title: Emerg Infect Dis
  doi: 10.3201/eid1404.071016
– volume: 10
  start-page: 1
  year: 2013
  ident: ppat.1011942.ref039
  article-title: Systemic distribution of different low pathogenic avian influenza (LPAI) viruses in chicken.
  publication-title: Virol J
  doi: 10.1186/1743-422X-10-23
– volume: 47
  start-page: 182
  year: 2003
  ident: ppat.1011942.ref009
  article-title: Occurrence and Possible Mechanisms of Cleavage-Site Insertions in the Avian Influenza Hemagglutinin Gene
  publication-title: Avian Dis
– volume: 37
  start-page: 555
  year: 2008
  ident: ppat.1011942.ref007
  article-title: The onset of virus shedding and clinical signs in chickens infected with high-pathogenicity and low-pathogenicity avian influenza viruses
  publication-title: Avian Pathol
  doi: 10.1080/03079450802499118
– volume: 312
  start-page: 384
  year: 2006
  ident: ppat.1011942.ref001
  article-title: Global patterns of influenza A virus in wild birds
  publication-title: Science
  doi: 10.1126/science.1122438
– volume: 186
  start-page: 5397
  year: 2011
  ident: ppat.1011942.ref052
  article-title: Characterization of chicken Mda5 activity: regulation of IFN-β in the absence of RIG-I functionality
  publication-title: J Immunol
  doi: 10.4049/jimmunol.1003712
– volume: 16
  start-page: 1057
  year: 2010
  ident: ppat.1011942.ref058
  article-title: Persistence of highly pathogenic avian influenza viruses in natural ecosystems
  publication-title: Emerg Infect Dis
  doi: 10.3201/eid1607.090389
– volume: 11
  start-page: 2407
  year: 1992
  ident: ppat.1011942.ref010
  article-title: Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease
  publication-title: EMBO J
  doi: 10.1002/j.1460-2075.1992.tb05305.x
– volume: 86
  start-page: 705
  year: 2012
  ident: ppat.1011942.ref053
  article-title: Chicken Cells Sense Influenza A Virus Infection through MDA5 and CARDIF Signaling Involving LGP2
  publication-title: J Virol
  doi: 10.1128/JVI.00742-11
– volume: 26
  start-page: 2966
  year: 2020
  ident: ppat.1011942.ref017
  article-title: Highly Pathogenic Avian Influenza A(H7N3) Virus in Poultry, United States, 2020.
  publication-title: Emerg Infect Dis
  doi: 10.3201/eid2612.202790
– volume: 107
  start-page: 341
  year: 1992
  ident: ppat.1011942.ref019
  article-title: A pathogenesis study of highly pathogenic avian influenza virus H5N2 in chickens, using immunohistochemistry
  publication-title: J Comp Pathol
  doi: 10.1016/0021-9975(92)90009-J
– volume: 14
  start-page: 165
  year: 2022
  ident: ppat.1011942.ref049
  article-title: Reduced Replication of Highly Pathogenic Avian Influenza Virus in Duck Endothelial Cells Compared to Chicken Endothelial Cells Is Associated with Stronger Antiviral Responses.
  publication-title: Viruses.
  doi: 10.3390/v14010165
– volume: 95
  start-page: 409
  year: 1998
  ident: ppat.1011942.ref004
  article-title: Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation
  publication-title: Cell
  doi: 10.1016/S0092-8674(00)81771-7
– volume: 25
  start-page: 285
  year: 1996
  ident: ppat.1011942.ref022
  article-title: Pathological studies of chickens experimentally infected with two highly pathogenic avian influenza viruses
  publication-title: Avian Pathol
  doi: 10.1080/03079459608419142
– volume: 12
  start-page: 901
  year: 2021
  ident: ppat.1011942.ref050
  article-title: Primary chicken and duck endothelial cells display a differential response to infection with highly pathogenic avian influenza virus
  publication-title: Genes (Basel).
  doi: 10.3390/genes12060901
– volume: 146
  start-page: 130
  year: 1985
  ident: ppat.1011942.ref012
  article-title: Evolution of the a/chicken/Pennsylvania/83 (H5N2) influenza virus.
  publication-title: Virology
  doi: 10.1016/0042-6822(85)90059-5
– volume: 12
  start-page: 125
  year: 1988
  ident: ppat.1011942.ref002
  article-title: Host range of avian influenza virus in free-living birds
  publication-title: Vet Res Commun
  doi: 10.1007/BF00362792
– volume: 94
  start-page: e01818
  year: 2020
  ident: ppat.1011942.ref013
  article-title: Emergence and Selection of a Highly Pathogenic Avian Influenza H7N3
  publication-title: Virus. J Virol
– volume: 78
  start-page: 4892
  year: 2004
  ident: ppat.1011942.ref029
  article-title: Reemerging H5N1 Influenza Viruses in Hong Kong in 2002 Are Highly Pathogenic to Ducks
  publication-title: J Virol
  doi: 10.1128/JVI.78.9.4892-4901.2004
– volume: 65
  start-page: 1576
  year: 2018
  ident: ppat.1011942.ref016
  article-title: From low to high pathogenicity—Characterization of H7N7 avian influenza viruses in two epidemiologically linked outbreaks.
  publication-title: Transbound Emerg Dis.
  doi: 10.1111/tbed.12906
– volume: 68
  start-page: 3120
  year: 1994
  ident: ppat.1011942.ref005
  article-title: Reverse genetics provides direct evidence for a correlation of hemagglutinin cleavability and virulence of an avian influenza A virus
  publication-title: J Virol
  doi: 10.1128/jvi.68.5.3120-3128.1994
– volume: 10
  start-page: 693
  year: 2004
  ident: ppat.1011942.ref014
  article-title: Recombination Resulting in Virulence Shift in Avian Influenza Outbreak, Chile
  publication-title: Emerg Infect Dis
  doi: 10.3201/eid1004.030396
– year: 2010
  ident: ppat.1011942.ref059
  article-title: Growth and maintenance of chick embryo fibroblasts (CEF).
  publication-title: Curr Protoc Microbiol.
– volume: 78
  start-page: 407
  year: 1943
  ident: ppat.1011942.ref062
  article-title: Studies of antigenic differences among strains of influenza a by means of red cell agglutination
  publication-title: J Exp Med
  doi: 10.1084/jem.78.5.407
– volume: 10
  start-page: 2192
  year: 2004
  ident: ppat.1011942.ref015
  article-title: Novel avian influenza H7N3 strain outbreak, British Columbia
  publication-title: Emerg Infect Dis
  doi: 10.3201/eid1012.040743
– volume: 48
  start-page: 119
  year: 2004
  ident: ppat.1011942.ref020
  article-title: Comparative pathobiology of low and high pathogenicity H7N3 Chilean avian influenza viruses in chickens
  publication-title: Avian Dis
  doi: 10.1637/7080
– volume: 24
  start-page: 242
  year: 1978
  ident: ppat.1011942.ref044
  article-title: The pathogenicity of four avian influenza viruses for fowls, turkeys and ducks
  publication-title: Res Vet Sci
  doi: 10.1016/S0034-5288(18)33080-7
– volume: 49
  start-page: 81
  year: 2005
  ident: ppat.1011942.ref040
  article-title: Experimental Study to Determine if Low-Pathogenicity and High-Pathogenicity Avian Influenza Viruses Can Be Present in Chicken Breast and Thigh Meat Following Intranasal Virus Inoculation
  publication-title: Avian Dis
  doi: 10.1637/7260-081104R
– volume: 23
  start-page: 1860
  year: 2017
  ident: ppat.1011942.ref018
  article-title: Highly pathogenic avian influenza A(H7N9) virus, Tennessee, USA, March 2017.
  publication-title: Emerg Infect Dis
  doi: 10.3201/eid2311.171013
– volume: 15
  start-page: 647
  year: 1986
  ident: ppat.1011942.ref045
  article-title: Experimental Assessment Of The Pathogenicity Of Eight Avian Influenza A Viruses Of H5 Subtype For Chickens, Turkeys
  publication-title: Ducks And Quail. Avian Pathol
  doi: 10.1080/03079458608436328
– volume: 15
  start-page: 142
  year: 2019
  ident: ppat.1011942.ref047
  article-title: Virulence of three European highly pathogenic H7N1 and H7N7 avian influenza viruses in Pekin and Muscovy ducks
  publication-title: BMC Vet Res
  doi: 10.1186/s12917-019-1899-4
– volume: 9
  start-page: 1003421
  year: 2013
  ident: ppat.1011942.ref034
  article-title: Influenza Virus Reassortment Occurs with High Frequency in the Absence of Segment Mismatch.
  publication-title: PLoS Pathog.
  doi: 10.1371/journal.ppat.1003421
– volume: 79
  start-page: 11269
  year: 2005
  ident: ppat.1011942.ref030
  article-title: Are Ducks Contributing to the Endemicity of Highly Pathogenic H5N1 Influenza Virus in Asia
  publication-title: J Virol
  doi: 10.1128/JVI.79.17.11269-11279.2005
– volume: 101
  start-page: 1356
  year: 2004
  ident: ppat.1011942.ref033
  article-title: Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.0308352100
– volume: 5
  start-page: 653
  year: 2014
  ident: ppat.1011942.ref031
  article-title: Influenza virus and endothelial cells: A species specific relationship.
  publication-title: Front Microbiol
  doi: 10.3389/fmicb.2014.00653
– volume: 54
  start-page: 1091
  year: 2010
  ident: ppat.1011942.ref037
  article-title: Potential of low pathogenicity avian influenza viruses of wild bird origin to establish experimental infections in turkeys and chickens
  publication-title: Avian Dis
  doi: 10.1637/9228-010410-ResNote.1
– volume: 10
  start-page: 1597
  year: 2021
  ident: ppat.1011942.ref057
  article-title: Structural Requirements in the Hemagglutinin Cleavage Site-Coding RNA Region for the Generation of Highly Pathogenic Avian Influenza Virus.
  publication-title: Pathogens
  doi: 10.3390/pathogens10121597
– volume: 14
  start-page: 1566
  year: 2022
  ident: ppat.1011942.ref008
  article-title: Hemagglutinin Subtype Specificity and Mechanisms of Highly Pathogenic Avian Influenza Virus Genesis
  publication-title: Viruses
  doi: 10.3390/v14071566
– start-page: 96
  year: 2022
  ident: ppat.1011942.ref036
  article-title: Opposite Outcomes of the Within-Host Competition between High- and Low-Pathogenic H5N8 Avian Influenza Viruses in Chickens Compared to Ducks
  publication-title: J Virol
– start-page: 7
  year: 2018
  ident: ppat.1011942.ref035
  article-title: A viral race for primacy: co-infection of a natural pair of low and highly pathogenic H7N7 avian influenza viruses in chickens and embryonated chicken eggs
  publication-title: Emerg Microbes Infect
– volume: 12
  start-page: e0177265
  year: 2017
  ident: ppat.1011942.ref024
  article-title: The pathogenesis of H7N8 low and highly pathogenic avian influenza viruses from the United States 2016 outbreak in chickens, turkeys and mallards.
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0177265
– volume: 14
  start-page: 1287E
  year: 2017
  ident: ppat.1011942.ref041
  article-title: Mechanisms and risk factors for mutation from low to highly pathogenic avian influenza virus.
  publication-title: EFSA Support Publ.
– volume: 11
  start-page: 942
  year: 2014
  ident: ppat.1011942.ref061
  article-title: RNA structural constraints in the evolution of the influenza A virus genome NP segment
  publication-title: RNA Biol
  doi: 10.4161/rna.29730
– volume: 10
  year: 2019
  ident: ppat.1011942.ref038
  article-title: A novel neuraminidase-dependent hemagglutinin cleavage mechanism enables the systemic spread of an H7N6 avian influenza virus.
  publication-title: MBio.
– volume: 107
  start-page: 5913
  year: 2010
  ident: ppat.1011942.ref051
  article-title: Association of RIG-I with innate immunity of ducks to influenza
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.1001755107
– volume: 9
  start-page: 11556
  year: 2019
  ident: ppat.1011942.ref043
  article-title: Variable impact of the hemagglutinin polybasic cleavage site on virulence and pathogenesis of avian influenza H7N7 virus in chickens, turkeys and ducks.
  publication-title: Sci Rep
  doi: 10.1038/s41598-019-47938-3
– volume: 66
  start-page: 2342
  year: 2019
  ident: ppat.1011942.ref027
  article-title: A novel H7N3 reassortant originating from the zoonotic H7N9 highly pathogenic avian influenza viruses that has adapted to ducks.
  publication-title: Transbound Emerg Dis
  doi: 10.1111/tbed.13291
– volume: 39
  start-page: 265
  year: 2010
  ident: ppat.1011942.ref046
  article-title: Infection dynamics of highly pathogenic avian influenza and virulent avian paramyxovirus type 1 viruses in chickens, turkeys and ducks
  publication-title: Avian Pathol
  doi: 10.1080/03079457.2010.492825
– start-page: 93
  year: 2019
  ident: ppat.1011942.ref032
  article-title: Loss of Fitness of Mexican H7N3 Highly Pathogenic Avian Influenza Virus in Mallards after Circulating in Chickens
  publication-title: J Virol
– volume: 11
  start-page: 1
  year: 2020
  ident: ppat.1011942.ref063
  article-title: SARS-CoV-2 is transmitted via contact and via the air between ferrets.
  publication-title: Nat Commun 2020 111
– volume: 46
  start-page: 971
  year: 2009
  ident: ppat.1011942.ref021
  article-title: Pathology and virus distribution in chickens naturally infected with highly pathogenic avian influenza A virus (H7N7) During the 2003 outbreak in The Netherlands.
  publication-title: Vet Pathol
  doi: 10.1354/vp.08-VP-0215-K-BC
– volume: 12
  start-page: 920
  year: 2020
  ident: ppat.1011942.ref042
  article-title: The emergence of H7N7 highly pathogenic avian influenza virus from low pathogenicity avian influenza virus using an in ovo embryo culture model.
  publication-title: Viruses.
  doi: 10.3390/v12090920
– volume: 64
  start-page: 309
  year: 1966
  ident: ppat.1011942.ref056
  article-title: The isolation and classification of Tern virus: Influenza Virus A/Tern/South Africa/1961
  publication-title: J Hyg (Lond).
  doi: 10.1017/S0022172400040596
– volume: 4
  start-page: e1000127
  year: 2008
  ident: ppat.1011942.ref055
  article-title: Evidence of infection by H5N2 highly pathogenic avian influenza viruses in healthy wild waterfowl.
  publication-title: PLoS Pathog.
  doi: 10.1371/journal.ppat.1000127
– volume: 68
  start-page: 6074
  year: 1994
  ident: ppat.1011942.ref011
  article-title: Proprotein-processing endoproteases PC6 and furin both activate hemagglutinin of virulent avian influenza viruses
  publication-title: J Virol
  doi: 10.1128/jvi.68.9.6074-6078.1994
– volume: 90
  start-page: 9967
  year: 2016
  ident: ppat.1011942.ref025
  article-title: Pathogenicity and Transmission of H5 and H7 Highly Pathogenic Avian Influenza Viruses in Mallards
  publication-title: J Virol
  doi: 10.1128/JVI.01165-16
– volume: 24
  start-page: 545
  year: 1995
  ident: ppat.1011942.ref026
  article-title: Replication of influenza A viruses of high and low pathogenicity for chickens at different sites in chickens and ducks following intranasal inoculation
  publication-title: Avian Pathol
  doi: 10.1080/03079459508419093
– volume: 50
  start-page: 548
  year: 2013
  ident: ppat.1011942.ref048
  article-title: Replication of 2 subtypes of low-pathogenicity avian influenza virus of duck and gull origins in experimentally infected Mallard ducks
  publication-title: Vet Pathol
  doi: 10.1177/0300985812469633
– volume: 103
  start-page: 155
  year: 2004
  ident: ppat.1011942.ref060
  article-title: Efficient generation and growth of influenza virus A/PR/8/34 from eight cDNA fragments
  publication-title: Virus Res
  doi: 10.1016/j.virusres.2004.02.028
SSID ssj0041316
Score 2.4451494
Snippet Highly pathogenic avian influenza viruses (HPAIVs) cause severe hemorrhagic disease in terrestrial poultry and are a threat to the poultry industry, wild life,...
SourceID plos
doaj
pubmedcentral
proquest
pubmed
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage e1011942
SubjectTerms Animals
Animals, Wild
Aquatic birds
Avian flu
Biology and Life Sciences
Chickens
Drinking water
Ducks
Ecology and Environmental Sciences
Epitopes
Fibroblasts
Flow cytometry
Hemagglutinins
Hemorrhagic disease
Humans
Hypotheses
Infections
Influenza
Influenza A virus - genetics
Influenza A Virus, H7N7 Subtype
Influenza in Birds
Medicine and Health Sciences
Orthomyxoviridae
Peptides
Poultry
Poultry Diseases
Proteins
Replication
Systemic diseases
Tropism
Viruses
Waterfowl
Wildfowl
SummonAdditionalLinks – databaseName: DOAJ Directory of Open Access Journals
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1La9tAEF5KoNBL6Ttu07CFXtVI2qeObUkwhfaUQm5in9TESMayA-6vyE_OzK5k4hLIpVfN2t7HaHY-7-z3EfIZYKyAwB8LFnksuGS-0MzFAnY-WTLWaJe49H7-kvPf_MeVuLon9YU1YZkeOE_cmfFOV7zyhjEkB5NWyMgsZCHeee2Dw-gLe94EpnIMhsicRE9RFKdQTMrx0hxT1dm4Rl9WK5PoowHF1webUuLuR67TZT88lHf-Wz55bz-6eEGej4kk_ZoH8JI8Cd0r8jRLS-5ek9skLB-GAq9SYjkQDeNFy0D7SOeKIlHxckdRkriH59DC3ICv0EWWLflr6M1ivR3oYqB-jTGR2h0YoS94MYQOSUAHVpVOGisQcehY9kVRYeUaEDI1nad-666HN-Ty4vzy-7wY1RcKJ2q1AYQahXB4zOZNaEr4plKpIF0VfAi1iNyUMSgmJJPRROuM5kx7hRAJUKdkb8lR13fhmFBro2HchYY3kvtKaAkgzGjrfKWsr8sZYdPst25kJkeBjGWbjtsUIJQ8py2uWTuu2YwU-0-tMjPHI-2_4cLu2yKvdnoA3taO3tY-5m0zcoxuMf3A0ALiagCiNRxGcTK5ysPmT3szvMF4LGO60G-HFhKumuPfb9DFd9mz9p1kgL912YBFH_jcwSgOLd3iT2IJR8bXRvPq_f8Y9wfyrIZsLpern5CjzXobPkI2trGn6cW7AypgNpk
  priority: 102
  providerName: Directory of Open Access Journals
– databaseName: Health & Medical Collection
  dbid: 7X7
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwhV1Lj9MwELZgERIXxHu7LMhIXM0msWM7JwSIVYUEp0XqLXL8gGqrpDTtSuVX8JN3xnECRSu4ZpzEyYzHM_b4-wh5DWlsCY4_MB5EYEJyxzS3gcHMJzPOK20jlt7nL3L-VXxalIu04NanssrRJ0ZH7TqLa-RnENpWEAtXInu7_sGQNQp3VxOFxm1yB6HLsKRLLaaEC_xzpD5FahymuJTp6BxX-VnS1Jv12kQQacjli4OpKSL4I-Lpqutvij7_LqL8Y1Y6f0Dup3CSvhv0_5Dc8u0jcncgmNw_Jr8ivbzvGR6oxKIg6tNxS0-7QOeKIlzxak-RmLiD69DCXIHF0OVAXvLT0KvlZtfTZU_dBj0jbfYghL7g8RDaRxod0C0dmVbA79BU_EWRZ-US8mRqWkfdzl72T8jF-ceLD3OWOBiYLQu1hTw1lKXFzTZnfJXBkzKlvLS5d94XZRAmC17xUnIZTGis0YJrpzBRgtxT8qfkqO1af0xo0wTDhfWVqKRweaklpGJGN9blqnFFNiN8_Pu1TfjkSJOxquOmm4I8ZfinNeqsTjqbETbdtR7wOf7T_j0qdmqL6NrxQrf5VqfBWhsHXyxyZzhHQDrZlDLwBiJfZ5123s7IMZrF-IK-_m2cM3I6msrN4leTGMYxbs6Y1ne7voawqxC4CAddfDZY1tRJDlm4ziqQ6AObO_iKQ0m7_B6xwhH3tdIiP_l3v56TewVEa0M5-ik52m52_gVEW9vmZRxS1xvOLUw
  priority: 102
  providerName: ProQuest
Title Species-specific emergence of H7 highly pathogenic avian influenza virus is driven by intrahost selection differences between chickens and ducks
URI https://www.ncbi.nlm.nih.gov/pubmed/38408092
https://www.proquest.com/docview/3069182940
https://www.proquest.com/docview/2932435402
https://pubmed.ncbi.nlm.nih.gov/PMC10919841
https://doaj.org/article/adc8141da3314286b56f3b656dcd8dec
http://dx.doi.org/10.1371/journal.ppat.1011942
Volume 20
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwhV1bb9MwFLbGJtBeENetMCoj8ZopiR3beUCIoU0V0iaENqlvkeMLVKuSkrQT5VfwkznHSSqKOvEa24kv59jni-3vI-QdwNgMJn4fMc99xAWzkWLGR7DyiZixXJnApXd5JSY3_PM0m-6RQbO178B2J7RDPambZn7688f6Azj8-6DaIJOh0OlioQMhNOBymJQPYG2S6KqXfLOvADN2IvoLdPeVPCSPGKAeFefp1loVKP2RAnVet7vC0X9PVf61TF08IY_7-JJ-7AziKdlz1TPysFOcXD8nv4PevGsjvGGJp4So6-9fOlp7OpEU-Yvna4pKxTU8hxz6DkyIzjo1k1-a3s2aVUtnLbUNTpW0XEMi1AXvi9A26OrAYNNBegUmItqfBqMovHILwJnqylK7MrftC3J9cX79aRL1ogyRyVK5BODqs8zg7pvVLo_hTbGUTpjEWefSzHMdeydZJpjw2pdGK86UlYicAIwK9pLsV3XljgktS68ZNy7nueA2yZQAbKZVaWwiS5vGI8KG3i9MT1iOuhnzIuzCSQAuXZ8WOHxFP3wjEm1KLTrCjv_kP8OB3eRFuu3woG6-Fb33FtpCi3liNWPIUCfKTHhWQihsjVXWmRE5RrMYPtAWAMRyQG45h1acDKayO_ntJhkcG3drdOXqVVtAHJZy_CsHVTzqLGtTycFAR0Rt2dxWK7ZTqtn3QB6ORLC54smre1_6mhymELl1R9NPyP6yWbk3EHktyzF5IKdyTA7Ozq--fB2H_xfj4GB_APkrNIU
linkProvider Scholars Portal
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV1fb9MwELdGJwQvE3-3jgFGgsewJHbs5AEhBps6tlUIFWlvkeM_UK1KStMOlU_BF-E7cpc4haIJnvaac1ondz7fxXe_HyHPIY1NwPG7gDnuAi6YCVKmXQA7nwgZy1LdYOmdDcXgE39_npxvkJ9dLwyWVXY-sXHUptL4jXwfQtsMYuGMh6-nXwNkjcLT1Y5CozWLE7v8Bilb_er4Hej3RRwfHY7eDgLPKhDoJJZzyLxckmg8PjLKZqFzNpTSCh1ZY22cOK5CZyVLBBNOuUKrlLPUSAz9IZsSDH72BtnkDDKZHtk8OBx--Ni5ftgQGq5V5OIJJBPC9-oxGe1703g5naoGtTrKeLy2FzaUAQixOqnqq8Ldv6s2_9gGj-6QLR-_0jetwd0lG7a8R262jJbL--RHw2dv6wA7OLEKiVrf32lp5ehAUsRHniwpMiFXcB1GqEswUTpu2VK-K3o5ni1qOq6pmaErpsUShDAX7EehdcPbA8ZEO2oXcHTUV5tRJHa5gMScqtJQs9AX9QMyug71PCS9sirtDqFF4RTj2mY8E9xESSog91NpoU0kCxOHfcK6t59rD4iOvByTvDnlk5AYte80R53lXmd9EqzumraAIP8Zf4CKXY1FOO_mQjX7nHvvkCsDT8wjoxhDBDxRJMKxAkJto01qrO6THTSL7g_q_Pdq6JO9zlSuFj9bicFx4GmQKm21qHOI82KOX_1gitutZa0mySDtT8MMJOmaza09xbqkHH9pwMkRaDZLebT773k9JbcGo7PT_PR4ePKI3I4hVGxr4fdIbz5b2McQ6s2LJ36BUZJf85L-BRJFa30
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV1Lj9MwELaWRSAuiPcWFjASHEOT2LGTA0LAUnVZWHFYpN4ixw-otkpK0y4qv4K_w79jxnEKRSs47TXjtE7m4fni8XyEPAUYm0HgdxFz3EVcMBPlTLsIVj4RM1bk2vfS-3Asxp_4u0k22SE_-7MwWFbZx0QfqE2j8Rv5EFLbAnLhgsdDF8oiPh6MXs6_RsgghTutPZ1GZyJHdv0N4Fv74vAAdP0sTUdvT96Mo8AwEOkslUtAYS7LNG4lGWWL2DkbS2mFTqyxNs0cV7GzkmWCCadcpVXOWW4kwgBAVoLBz14il2FAgi4mJxusB0uDZ11FVp5IMiHCqT0mk2EwkufzufL9q5OCp1uroicPwGars6Y9L_H9u37zjwVxdINcD5ksfdWZ3k2yY-tb5ErHbbm-TX54ZnvbRniWE-uRqA0nPS1tHB1Lip2SZ2uKnMgNXIcR6gyMlU473pTvip5NF6uWTltqFhiUabUGIcwFT6bQ1jP4gFnRnuQFQh4NdWcUKV5OAaJTVRtqVvq0vUNOLkI5d8lu3dR2j9CqcopxbQteCG6SLBeAAlVeaZPIyqTxgLD-7Zc6tEZHho5Z6ff7JECk7p2WqLMy6GxAos1d8641yH_Gv0bFbsZiY29_oVl8LkOcKJWBJ-aJUYxhLzxRZcKxCpJuo01urB6QPTSL_g_a8rdfDMh-byrni59sxBBCcF9I1bZZtSVkfCnH738wxXudZW0myXIOmKIASb5lc1tPsS2pp198m3JsOVvkPLn_73k9JlfBkcv3h8dHD8i1FHLGrih-n-wuFyv7EHK-ZfXIexcl5QV78y-hOG5N
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Species-specific+emergence+of+H7+highly+pathogenic+avian+influenza+virus+is+driven+by+intrahost+selection+differences+between+chickens+and+ducks&rft.jtitle=PLoS+pathogens&rft.au=de+Bruin%2C+Anja+C+M&rft.au=Spronken%2C+Monique+I&rft.au=Kok%2C+Adinda&rft.au=Rosu%2C+Miruna+E&rft.date=2024-02-01&rft.eissn=1553-7374&rft.volume=20&rft.issue=2&rft.spage=e1011942&rft_id=info:doi/10.1371%2Fjournal.ppat.1011942&rft_id=info%3Apmid%2F38408092&rft.externalDocID=38408092
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1553-7374&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1553-7374&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1553-7374&client=summon