Absence of detection of highly pathogenic H5N1 in migratory waterfowl in southern France in 2005–2006

Abstract

During fall 2005, the rapid and wide spread of highly pathogenic (HP) H5N1 avian influenza viruses (AIV) outside Asia alerted European health authorities. Because of abnormal and recurrent field mortality, wild migratory birds were considered to be the main dispersing agent of the virus at an intercontinental scale. European wintering wetlands, such as the Camargue (Rhône delta, France), are identified as potential hot spots for the risk of introduction and transmission of bird-borne diseases. In this study, we investigated the role of migratory waterbirds (mainly ducks) in the spread of HP H5N1 viruses. We combined molecular analysis of living and freshly killed birds with population surveillance (aerial censuses and death surveillance). We sampled 1345 birds belonging to 17 waterbird species (3 orders) in the Camargue between September 2005 and March 2006. The prevalence of AIV was 1.8%. We did not detect HP H5N1 virus. Population censuses did not reveal any population decreases nor abnormal mortalities. We discuss, in the light of these results, the implication of wild migratory ducks in the arrival of HP H5N1 AIV in Europe.

Introduction

The threat of an influenza pandemic following the recent spread of the H5N1 avian influenza viruses (AIV) is currently a matter of concern for health authorities. Wild birds, and especially waterbirds in the Anseriforms and Charadriiforms orders, are natural hosts for influenza A viruses (Webster et al., 1992, Olsen et al., 2006). Avian influenza viruses can be sorted on the basis of virulence (Garten and Klenk, 1999, Horimoto and Kawaoka, 2005). Low pathogenic avian influenza (LPAI) viruses lead to benign respiratory and/or intestinal tract infections. Highly pathogenic avian influenza (HPAI) viruses cause a multi-organ systemic infection responsible for high levels of mortality. These viruses are rarely isolated in wild birds (Swayne and Suarez, 2000). Conversely, domestic birds, especially poultry, are victims of recurrent outbreaks due to HPAI viruses of subtypes H5 and H7 (Alexander, 2000, Olsen et al., 2006). In poultry, AIV evolve independently of the wild bird reservoir (Suarez, 2000). Outbreaks caused by HPAI viruses are generally limited to small geographic areas, but cause the death of a considerable number of domestic birds and important economic losses.

Highly pathogenic (HP) H5N1 viruses have been detected in China since 1996 (Tang et al., 1998, Xu et al., 1999). Outbreaks were reported almost simultaneously in eight neighbouring Asian countries between December 2003 and January 2004, suggesting that the viruses had spread recently and rapidly (Sims et al., 2005). In July 2005, HP H5N1 viruses started their westward progression by crossing the Russian border (Kilpatrick et al., 2006, Gauthier-Clerc et al., 2007): outbreaks were first detected in Western Siberia, and almost simultaneously in Kazakhstan and Mongolia (O.I.E., 2006). In October, it was found in Romania, Croatia and the Western edge of Turkey. From February 2006 onwards a second phase started, characterized by numerous sporadic outbreaks affecting mainly wild birds in European countries, but also poultry in Africa (e.g. Nigeria) and the Middle East (e.g. Iraq).

Migratory waterbirds were at the top of the list of suspects for the spread of HP H5N1 viruses (Webster et al., 2006, Normile, 2005, Normile, 2006), especially after the discovery of thousands of bar-headed geese killed by HP H5N1 in Qinghai Lake (Western China, Chen et al., 2005, Liu et al., 2005). However, the relative contribution of migratory birds, and especially waterbirds, in the spread of HP AIV remains unclear (Gauthier-Clerc et al., 2007). For instance, the recent report by Chen et al. (2006) showed that only a small proportion of wild ducks and geese might be involved in the spread of the virus compared to domestic species. Nevertheless, the potential role of wild birds in the HP H5N1 crisis is still put forward (e.g. FAO, 2006, Gauthier-Clerc et al., 2007), calling for multidisciplinary research towards a better understanding of the ecology of avian influenza viruses and to assess the risks linked to the circulation of HP viruses (Melville and Shortridge, 2006, Capua and Alexander, 2006, Munster et al., 2006).

The Camargue is an alluvial wetland covering some 140,000 ha in the Rhône delta (South of France). It is situated at the crossroads of numerous migratory routes of Palaearctic birds (Berthold, 2001, Blondel and Isenmann, 1981) and is recognized as one of their main Mediterranean wintering area. During fall and spring migrations, hundreds of thousands of wild waterbirds stop in the Camargue to forage, and during winter this area is considered to be a particularly important wintering site for species belonging to the Anseriform order (e.g. wild ducks, geese and swans; Tamisier and Dehorter, 1999). Anseriforms represent a central element of the ecology of avian influenza viruses because a particularly wide variety of subtypes have been isolated from these species (Deibel et al., 1985, Webster et al., 1992, Alexander, 2000), especially for the Mallard (Anas platyrhynchos, Munster et al., 2005).

The main objective of our study was to investigate the role of migratory waterbirds in the spread of HP H5N1 influenza viruses by combining different data sets (bird census, death surveillance and virus detection), closely taking into account the cascade of events characterising the first arrival of the HP H5N1 viruses in Western Europe.