Parasitology

Research Article

The ecology and age structure of a highly pathogenic avian influenza virus outbreak in wild mute swans

O. G. PYBUSa1 c1 , C. M. PERRINSa1a2 , B. CHOUDHURYa3 , R. J. MANVELLa3, A. NUNEZa3, B. SCHULENBURGa1, B. C. SHELDONa1a2 and I. H. BROWNa3

a1 Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS

a2 Edward Grey Institute of Field Ornithology, Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS

a3 Virology Department, Animal Health and Veterinary Laboratories Agency, Weybridge, Addlestone, Surrey KT153NB

SUMMARY

The first UK epizootic of highly pathogenic (HP) H5N1 influenza in wild birds occurred in 2008, in a population of mute swans that had been the subject of ornithological study for decades. Here we use an innovative combination of ornithological, phylogenetic and immunological approaches to investigate the ecology and age structure of HP H5N1 in nature. We screened samples from swans and waterbirds using PCR and sequenced HP H5N1-positive samples. The outbreak's origin was investigated by linking bird count data with a molecular clock analysis of sampled virus sequences. We used ringing records to reconstruct the age-structure of outbreak mortality, and we estimated the age distribution of prior exposure to avian influenza. Outbreak mortality was low and all HP H5N1-positive mute swans in the affected population were <3 years old. Only the youngest age classes contained an appreciable number of individuals with no detectable antibody responses to viral nucleoprotein. Phylogenetic analysis indicated that the outbreak strain circulated locally for ∼1 month before detection and arrived when the immigration rate of migrant waterbirds was highest. Our data are consistent with the hypothesis that HP H5N1 epizootics in wild swans exhibit limited mortality due to immune protection arising from previous exposure. Our study population may represent a valuable resource for investigating the natural ecology and epidemiology of avian influenza.

(Received November 27 2011)

(Revised January 20 2012)

(Accepted January 23 2012)

(Online publication February 20 2012)

Key words

  • Avian influenza virus;
  • age structure;
  • serology;
  • molecular clock;
  • phylogenetics;
  • swans

Correspondence:

c1 Corresponding author: oliver.pybus@zoo.ox.ac.uk (01865 271274).

Footnotes

  These authors contributed equally.

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