Heterosubtypic immunity to influenza A virus infections in mallards may explain existence of multiple virus subtypes.

Wild birds, particularly duck species, are the main reservoir of influenza A virus (IAV) in nature. However, knowledge of IAV infection dynamics in the wild bird reservoir, and the development of immune responses, are essentially absent. Importantly, a detailed understanding of how subtype diversity...

Full description

Bibliographic Details
Main Authors: Neus Latorre-Margalef, Vladimir Grosbois, John Wahlgren, Vincent J Munster, Conny Tolf, Ron A M Fouchier, Albert D M E Osterhaus, Björn Olsen, Jonas Waldenström
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS Pathogens
Online Access:http://europepmc.org/articles/PMC3688562?pdf=render
_version_ 1818033636375527424
author Neus Latorre-Margalef
Vladimir Grosbois
John Wahlgren
Vincent J Munster
Conny Tolf
Ron A M Fouchier
Albert D M E Osterhaus
Björn Olsen
Jonas Waldenström
author_facet Neus Latorre-Margalef
Vladimir Grosbois
John Wahlgren
Vincent J Munster
Conny Tolf
Ron A M Fouchier
Albert D M E Osterhaus
Björn Olsen
Jonas Waldenström
author_sort Neus Latorre-Margalef
collection DOAJ
description Wild birds, particularly duck species, are the main reservoir of influenza A virus (IAV) in nature. However, knowledge of IAV infection dynamics in the wild bird reservoir, and the development of immune responses, are essentially absent. Importantly, a detailed understanding of how subtype diversity is generated and maintained is lacking. To address this, 18,679 samples from 7728 Mallard ducks captured between 2002 and 2009 at a single stopover site in Sweden were screened for IAV infections, and the resulting 1081 virus isolates were analyzed for patterns of immunity. We found support for development of homosubtypic hemagglutinin (HA) immunity during the peak of IAV infections in the fall. Moreover, re-infections with the same HA subtype and related prevalent HA subtypes were uncommon, suggesting the development of natural homosubtypic and heterosubtypic immunity (p-value = 0.02). Heterosubtypic immunity followed phylogenetic relatedness of HA subtypes, both at the level of HA clades (p-value = 0.04) and the level of HA groups (p-value = 0.05). In contrast, infection patterns did not support specific immunity for neuraminidase (NA) subtypes. For the H1 and H3 Clades, heterosubtypic immunity showed a clear temporal pattern and we estimated within-clade immunity to last at least 30 days. The strength and duration of heterosubtypic immunity has important implications for transmission dynamics of IAV in the natural reservoir, where immune escape and disruptive selection may increase HA antigenic variation and explain IAV subtype diversity.
first_indexed 2024-12-10T06:26:25Z
format Article
id doaj.art-22982aa75247493b9368ffc64f6b2a67
institution Directory Open Access Journal
issn 1553-7366
1553-7374
language English
last_indexed 2024-12-10T06:26:25Z
publishDate 2013-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Pathogens
spelling doaj.art-22982aa75247493b9368ffc64f6b2a672022-12-22T01:59:12ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742013-01-0196e100344310.1371/journal.ppat.1003443Heterosubtypic immunity to influenza A virus infections in mallards may explain existence of multiple virus subtypes.Neus Latorre-MargalefVladimir GrosboisJohn WahlgrenVincent J MunsterConny TolfRon A M FouchierAlbert D M E OsterhausBjörn OlsenJonas WaldenströmWild birds, particularly duck species, are the main reservoir of influenza A virus (IAV) in nature. However, knowledge of IAV infection dynamics in the wild bird reservoir, and the development of immune responses, are essentially absent. Importantly, a detailed understanding of how subtype diversity is generated and maintained is lacking. To address this, 18,679 samples from 7728 Mallard ducks captured between 2002 and 2009 at a single stopover site in Sweden were screened for IAV infections, and the resulting 1081 virus isolates were analyzed for patterns of immunity. We found support for development of homosubtypic hemagglutinin (HA) immunity during the peak of IAV infections in the fall. Moreover, re-infections with the same HA subtype and related prevalent HA subtypes were uncommon, suggesting the development of natural homosubtypic and heterosubtypic immunity (p-value = 0.02). Heterosubtypic immunity followed phylogenetic relatedness of HA subtypes, both at the level of HA clades (p-value = 0.04) and the level of HA groups (p-value = 0.05). In contrast, infection patterns did not support specific immunity for neuraminidase (NA) subtypes. For the H1 and H3 Clades, heterosubtypic immunity showed a clear temporal pattern and we estimated within-clade immunity to last at least 30 days. The strength and duration of heterosubtypic immunity has important implications for transmission dynamics of IAV in the natural reservoir, where immune escape and disruptive selection may increase HA antigenic variation and explain IAV subtype diversity.http://europepmc.org/articles/PMC3688562?pdf=render
spellingShingle Neus Latorre-Margalef
Vladimir Grosbois
John Wahlgren
Vincent J Munster
Conny Tolf
Ron A M Fouchier
Albert D M E Osterhaus
Björn Olsen
Jonas Waldenström
Heterosubtypic immunity to influenza A virus infections in mallards may explain existence of multiple virus subtypes.
PLoS Pathogens
title Heterosubtypic immunity to influenza A virus infections in mallards may explain existence of multiple virus subtypes.
title_full Heterosubtypic immunity to influenza A virus infections in mallards may explain existence of multiple virus subtypes.
title_fullStr Heterosubtypic immunity to influenza A virus infections in mallards may explain existence of multiple virus subtypes.
title_full_unstemmed Heterosubtypic immunity to influenza A virus infections in mallards may explain existence of multiple virus subtypes.
title_short Heterosubtypic immunity to influenza A virus infections in mallards may explain existence of multiple virus subtypes.
title_sort heterosubtypic immunity to influenza a virus infections in mallards may explain existence of multiple virus subtypes
url http://europepmc.org/articles/PMC3688562?pdf=render
work_keys_str_mv AT neuslatorremargalef heterosubtypicimmunitytoinfluenzaavirusinfectionsinmallardsmayexplainexistenceofmultiplevirussubtypes
AT vladimirgrosbois heterosubtypicimmunitytoinfluenzaavirusinfectionsinmallardsmayexplainexistenceofmultiplevirussubtypes
AT johnwahlgren heterosubtypicimmunitytoinfluenzaavirusinfectionsinmallardsmayexplainexistenceofmultiplevirussubtypes
AT vincentjmunster heterosubtypicimmunitytoinfluenzaavirusinfectionsinmallardsmayexplainexistenceofmultiplevirussubtypes
AT connytolf heterosubtypicimmunitytoinfluenzaavirusinfectionsinmallardsmayexplainexistenceofmultiplevirussubtypes
AT ronamfouchier heterosubtypicimmunitytoinfluenzaavirusinfectionsinmallardsmayexplainexistenceofmultiplevirussubtypes
AT albertdmeosterhaus heterosubtypicimmunitytoinfluenzaavirusinfectionsinmallardsmayexplainexistenceofmultiplevirussubtypes
AT bjornolsen heterosubtypicimmunitytoinfluenzaavirusinfectionsinmallardsmayexplainexistenceofmultiplevirussubtypes
AT jonaswaldenstrom heterosubtypicimmunitytoinfluenzaavirusinfectionsinmallardsmayexplainexistenceofmultiplevirussubtypes