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PLOS: Evidence of Infection by H5N2 Highly Pathogenic Avian Influenza Viruses in Healthy Wild Waterfowl
Evidence of Infection by H5N2 Highly Pathogenic Avian Influenza Viruses in Healthy Wild Waterfowl
Nicolas Gaidet 1#*, Giovanni Cattoli 2#, Saliha Hammoumi 1, Scott H. Newman 3, Ward Hagemeijer 4, John Y. Takekawa 5, Julien Cappelle 1, Tim Dodman 4, Tony Joannis 6, Patricia Gil 1, Isabella Monne 2, Alice Fusaro 2, Ilaria Capua 2, Shiiwuua Manu 7, Pierfrancesco Micheloni 8, Ulf Ottosson 9, John H. Mshelbwala 10, Juan Lubroth 3, Joseph Domenech 3, François Monicat 1
1 Centre de Coopération Internationale en Recherche Agronomique pour le Développement, Montpellier, France2 Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro, Italy3 Food and Agriculture Organization of the United Nations, Animal Production and Health Division, Rome, Italy4 Wetlands International, Wageningen, The Netherlands5 U.S. Geological Survey, Western Ecological Research Center, Vallejo California, United States of America6 National Veterinary Research Institute, Vom, Nigeria7 AP Leventis Ornithological Research Institute, Jos, Nigeria8 Istituto Nazionale per la Fauna Selvatica, Bologna, Italy9 Ottenby Bird Observatory, Kehlen, Luxembourg10 Federal Department of Forestry, Abuja, Nigeria
Abstract
The potential existence of a wild bird reservoir for highly pathogenic avian influenza (HPAI) has been recently questioned by the spread and the persisting circulation of H5N1 HPAI viruses, responsible for concurrent outbreaks in migratory and domestic birds over Asia, Europe, and Africa.
During a large-scale surveillance programme over Eastern Europe, the Middle East, and Africa, we detected avian influenza viruses of H5N2 subtype with a highly pathogenic (HP) viral genotype in healthy birds of two wild waterfowl species sampled in Nigeria.
We monitored the survival and regional movements of one of the infected birds through satellite telemetry, providing a rare evidence of a non-lethal natural infection by an HP viral genotype in wild birds.
Phylogenetic analysis of the H5N2 viruses revealed close genetic relationships with H5 viruses of low pathogenicity circulating in Eurasian wild and domestic ducks.
In addition, genetic analysis did not reveal known gallinaceous poultry adaptive mutations, suggesting that the emergence of HP strains could have taken place in either wild or domestic ducks or in non-gallinaceous species.
The presence of coexisting but genetically distinguishable avian influenza viruses with an HP viral genotype in two cohabiting species of wild waterfowl, with evidence of non-lethal infection at least in one species and without evidence of prior extensive circulation of the virus in domestic poultry, suggest that some strains with a potential high pathogenicity for poultry could be maintained in a community of wild waterfowl.
Author Summary
Until recently, the highly pathogenic avian influenza (HPAI) viruses responsible for high mortality in some domestic poultry were considered not to have a wild bird reservoir, but to emerge in domestic poultry populations from low pathogenic viruses perpetuated in wild waterbirds.
The rapid spread of H5N1 HPAI virus in 2005–2006, with concurrent outbreaks reported in both domestic and wild birds over Asia, Europe, and Africa, has raised concerns about the potential role of migratory birds in the epidemiology of the HPAI infection.
Wild birds were sampled in Africa and tested by molecular and virological methods in an attempt to trace the circulation of HPAI viruses.
In addition, some of these wild birds were equipped with satellite transmitters to track their local and migratory movements in relation to the potential spread of avian diseases.
Avian influenza viruses (H5N2) were detected in wild waterfowl in Nigeria, and were subsequently characterized as highly pathogenic by molecular sequencing (HPAI viral genotype).
Movements of one infected bird tracked by satellite telemetry revealed that it survived infection by an HP viral genotype. This result constitutes a rare finding of infection by an AIV with an HPAI viral genotype in healthy wild birds.
Citation: Gaidet N, Cattoli G, Hammoumi S, Newman SH, Hagemeijer W, et al. (2008) Evidence of Infection by H5N2 Highly Pathogenic Avian Influenza Viruses in Healthy Wild Waterfowl. PLoS Pathog 4(8): e1000127. doi:10.1371/journal.ppat.1000127
Editor: Ron A. M. Fouchier, Erasmus Medical Center, Netherlands
Received: March 10, 2008; Accepted: July 16, 2008; Published: August 15, 2008
This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
Funding: This extensive survey has been implemented in the framework of an FAO Technical Cooperation Programme, and has been made possible by additional financial resources received from the governments of France and Sweden. We also acknowledge the Global Avian Influenza Network for Surveillance (GAINS) program, funded in part by USAID Grant No. LAG-A-00-99-00047-00, for the larger joint wild bird surveillance activities in Nigeria. The opinions expressed herein are those of the authors and do not necessarily reflect the views of the U.S. Agency for International Development.
Competing interests: The authors have declared that no competing interests exist.
* E-mail: nicolas.gaidet@cirad.fr
# These authors contributed equally to this work.
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http://www.plospathogens.org/article/info%3Adoi%2F10.1371%2Fjournal.ppat.1000127
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Nicolas Gaidet 1#*, Giovanni Cattoli 2#, Saliha Hammoumi 1, Scott H. Newman 3, Ward Hagemeijer 4, John Y. Takekawa 5, Julien Cappelle 1, Tim Dodman 4, Tony Joannis 6, Patricia Gil 1, Isabella Monne 2, Alice Fusaro 2, Ilaria Capua 2, Shiiwuua Manu 7, Pierfrancesco Micheloni 8, Ulf Ottosson 9, John H. Mshelbwala 10, Juan Lubroth 3, Joseph Domenech 3, François Monicat 1
1 Centre de Coopération Internationale en Recherche Agronomique pour le Développement, Montpellier, France2 Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro, Italy3 Food and Agriculture Organization of the United Nations, Animal Production and Health Division, Rome, Italy4 Wetlands International, Wageningen, The Netherlands5 U.S. Geological Survey, Western Ecological Research Center, Vallejo California, United States of America6 National Veterinary Research Institute, Vom, Nigeria7 AP Leventis Ornithological Research Institute, Jos, Nigeria8 Istituto Nazionale per la Fauna Selvatica, Bologna, Italy9 Ottenby Bird Observatory, Kehlen, Luxembourg10 Federal Department of Forestry, Abuja, Nigeria
Abstract
The potential existence of a wild bird reservoir for highly pathogenic avian influenza (HPAI) has been recently questioned by the spread and the persisting circulation of H5N1 HPAI viruses, responsible for concurrent outbreaks in migratory and domestic birds over Asia, Europe, and Africa.
During a large-scale surveillance programme over Eastern Europe, the Middle East, and Africa, we detected avian influenza viruses of H5N2 subtype with a highly pathogenic (HP) viral genotype in healthy birds of two wild waterfowl species sampled in Nigeria.
We monitored the survival and regional movements of one of the infected birds through satellite telemetry, providing a rare evidence of a non-lethal natural infection by an HP viral genotype in wild birds.
Phylogenetic analysis of the H5N2 viruses revealed close genetic relationships with H5 viruses of low pathogenicity circulating in Eurasian wild and domestic ducks.
In addition, genetic analysis did not reveal known gallinaceous poultry adaptive mutations, suggesting that the emergence of HP strains could have taken place in either wild or domestic ducks or in non-gallinaceous species.
The presence of coexisting but genetically distinguishable avian influenza viruses with an HP viral genotype in two cohabiting species of wild waterfowl, with evidence of non-lethal infection at least in one species and without evidence of prior extensive circulation of the virus in domestic poultry, suggest that some strains with a potential high pathogenicity for poultry could be maintained in a community of wild waterfowl.
Author Summary
Until recently, the highly pathogenic avian influenza (HPAI) viruses responsible for high mortality in some domestic poultry were considered not to have a wild bird reservoir, but to emerge in domestic poultry populations from low pathogenic viruses perpetuated in wild waterbirds.
The rapid spread of H5N1 HPAI virus in 2005–2006, with concurrent outbreaks reported in both domestic and wild birds over Asia, Europe, and Africa, has raised concerns about the potential role of migratory birds in the epidemiology of the HPAI infection.
Wild birds were sampled in Africa and tested by molecular and virological methods in an attempt to trace the circulation of HPAI viruses.
In addition, some of these wild birds were equipped with satellite transmitters to track their local and migratory movements in relation to the potential spread of avian diseases.
Avian influenza viruses (H5N2) were detected in wild waterfowl in Nigeria, and were subsequently characterized as highly pathogenic by molecular sequencing (HPAI viral genotype).
Movements of one infected bird tracked by satellite telemetry revealed that it survived infection by an HP viral genotype. This result constitutes a rare finding of infection by an AIV with an HPAI viral genotype in healthy wild birds.
Citation: Gaidet N, Cattoli G, Hammoumi S, Newman SH, Hagemeijer W, et al. (2008) Evidence of Infection by H5N2 Highly Pathogenic Avian Influenza Viruses in Healthy Wild Waterfowl. PLoS Pathog 4(8): e1000127. doi:10.1371/journal.ppat.1000127
Editor: Ron A. M. Fouchier, Erasmus Medical Center, Netherlands
Received: March 10, 2008; Accepted: July 16, 2008; Published: August 15, 2008
This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
Funding: This extensive survey has been implemented in the framework of an FAO Technical Cooperation Programme, and has been made possible by additional financial resources received from the governments of France and Sweden. We also acknowledge the Global Avian Influenza Network for Surveillance (GAINS) program, funded in part by USAID Grant No. LAG-A-00-99-00047-00, for the larger joint wild bird surveillance activities in Nigeria. The opinions expressed herein are those of the authors and do not necessarily reflect the views of the U.S. Agency for International Development.
Competing interests: The authors have declared that no competing interests exist.
* E-mail: nicolas.gaidet@cirad.fr
# These authors contributed equally to this work.
-
http://www.plospathogens.org/article/info%3Adoi%2F10.1371%2Fjournal.ppat.1000127
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