Highly pathogenic avian influenza virus H5N1 infection in a long-distance migrant shorebird under migratory and non-migratory states.

Leslie A Reperant,Albert D M E Osterhaus,Debbie M Buehler,Susi Jenni-Eiermann,Geert Van Amerongen,Theunis Piersma,Thijs Kuiken,Marco W G Van De Bildt,Todd Davis

doi:10.1371/journal.pone.0027814

Abstract

Corticosterone regulates physiological changes preparing wild birds for migration. It also modulates the immune system and may lead to increased susceptibility to infection, with implications for the spread of pathogens, including highly pathogenic avian influenza virus (HPAIV) H5N1. The red knot (Calidris canutus islandica) displays migratory changes in captivity and was used as a model to assess the effect of high plasma concentration of corticosterone on HPAIV H5N1 infection. We inoculated knots during pre-migration (N = 6), fueling (N = 5), migration (N = 9) and post-migration periods (N = 6). Knots from all groups shed similar viral titers for up to 5 days post-inoculation (dpi), peaking at 1 to 3 dpi. Lesions of acute encephalitis, associated with virus replication in neurons, were seen in 1 to 2 knots per group, leading to neurological disease and death at 5 to 11 dpi. Therefore, the risk of HPAIV H5N1 infection in wild birds and of potential transmission between wild birds and poultry may be similar at different times of the year, irrespective of wild birds' migratory status. However, in knots inoculated during the migration period, viral shedding levels positively correlated with pre-inoculation plasma concentration of corticosterone. Of these, knots that did not become productively infected had lower plasma concentration of corticosterone. Conversely, elevated plasma concentration of corticosterone did not result in an increased probability to develop clinical disease. These results suggest that birds with elevated plasma concentration of corticosterone at the time of migration (ready to migrate) may be more susceptible to acquisition of infection and shed higher viral titers—before the onset of clinical disease—than birds with low concentration of corticosterone (not ready for take-off). Yet, they may not be more prone to the development of clinical disease. Therefore, assuming no effect of sub-clinical infection on the likelihood of migratory take-off, this may favor the spread of HPAIV H5N1 by migratory birds over long distances.

Highlights

Wild bird species susceptibility to infection and disease caused by highly pathogenic avian influenza virus H5N1 (HPAIV H5N1) has been studied [1,2,3,4,5], their role in dispersing the virus over long distances is difficult to assess
In order to demonstrate any effect of corticosterone on infection with HPAIV H5N1 under the migratory state, several prerequisites must be met by the chosen model
Such outcome depends on the bird species, and on the infection dose and route of inoculation. This prerequisite is important to maximize our ability to detect any effect of corticosterone on HPAIV H5N1 infection under the migratory state

Summary

Introduction

Wild bird species susceptibility to infection and disease caused by highly pathogenic avian influenza virus H5N1 (HPAIV H5N1) has been studied [1,2,3,4,5], their role in dispersing the virus over long distances is difficult to assess. The effect of physiological changes associated with migration on virus-host interactions, which may interfere with the ability of wild birds to disperse the virus over long distances, is not well understood [8,10,11]. Important physiological changes prepare migratory birds for long-distance flights, and are essential for the development and maintenance of the migratory state [12,13,14]. Some migratory bird species increase their body mass by up to. 50% of their lean mass [15] They put on fat stores that will serve as fuel during migratory flights [14]. Elevated plasma concentration of corticosterone has been reported in wild songbirds and shorebirds caught just prior to or during migration [12,13,18,20]

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