Terrestrial Bird Migration and West Nile Virus Circulation, United States

Daniele Swetnam; Steven G. Widen; Thomas G. Wood; Martin Reyna; Lauren Wilkerson; Mustapha Debboun; Dreda A. Symonds; Daniel G. Mead; Barry J. Beaty; Hilda Guzman; Robert B. Tesh; Alan D.T. Barrett

Disclosures

Emerging Infectious Diseases. 2018;24(12):2184-2194. 

In This Article

Abstract and Introduction

Abstract

Host migration and emerging pathogens are strongly associated, especially with regard to zoonotic diseases. West Nile virus (WNV), a mosquitoborne pathogen capable of causing severe, sometimes fatal, neuroinvasive disease in humans, is maintained in highly mobile avian hosts. Using phylogeographic approaches, we investigated the relationship between WNV circulation in the United States and the flight paths of terrestrial birds. We demonstrated southward migration of WNV in the eastern flyway and northward migration in the central flyway, which is consistent with the looped flight paths of many terrestrial birds. We also identified 3 optimal locations for targeted WNV surveillance campaigns in the United States—Illinois, New York, and Texas. These results illustrate the value of multidisciplinary approaches to surveillance of infectious diseases, especially zoonotic diseases.

Introduction

West Nile virus (WNV) is a mosquitoborne virus that can cause severe and even fatal disease in humans. After WNV introduction into New York, NY, USA, its geographic range expanded quickly, reaching the West Coast in 2003. Previous studies have shown that the spread of WNV occurred faster than could be explained by contiguous diffusion[1–4] and demonstrated that its expansion occurred heterogeneously, consisting of contiguous diffusion and long distance translocations.[2,5] Since then, phylogeographic studies have reported frequent mixing of WNV strains from local and distant locations. The most notable exception is California, where several genetic studies have shown limited movement into and out of the state.[6,7]

The rapid expansion of WNV in the United States probably cannot be attributed to the movement of humans because humans are dead-end hosts. However, in nature, WNV is maintained in an enzootic transmission cycle involving mosquito vectors and highly mobile avian reservoirs. Hyalomma marginatum ticks have also been implicated in the transmission of WNV.[8]

Although evidence of WNV infection has been identified in many species of birds, deaths and disease among birds vary greatly, ranging from asymptomatic to fatal infections; peak viremia potentially reaches >1012 PFU/mL.[9] WNV RNA has been detected in bird spleen and kidneys as long as 36 weeks after infection[10] and in brains of Nestor notabilis kea up to 72 months after infection.[11]

Although phylogenetic evidence of geographic clustering by location is limited, a recent study reported that WNV isolates clustered according to avian flyway.[12] Because birds are the primary reservoirs for WNV, this finding was not surprising, but it is relevant because bird migration has also been implicated in the movement of influenza A virus,[13] Borrelia burgdorferi (Lyme disease agent),[14] other pathogenic organisms,[1] and even invasive invertebrate organisms.[15] Several serologic studies (e.g., ELISA, plaque reduction neutralization test) have been used to determine the direction of WNV movement within the Atlantic, Mississippi, and Pacific flyways and demonstrated WNV in birds migrating southward, whereas evidence of the virus in birds during northward migration is limited.[16,17]

Studies of virus movement associated with avian hosts in the United States have concentrated on the migration of waterfowl and excluded terrestrial birds, largely because the migratory patterns of waterfowl have been thoroughly characterized by banding studies. However, passerine birds, the primary reservoir for WNV, are terrestrial birds, not waterfowl. Terrestrial birds and waterfowl fly along similar but distinct flyways. Although waterfowl follow regular paths bounded by mountains and rivers, terrestrial birds often follow looped routes that enable them to maximize tail winds, avoid head winds, and correlate with seasonal fluctuations in food availability.[18,19] Although looped migration paths have been described for several species of birds (Selasphorus rufus hummingbirds,[20]Circus aeruginosus western marsh harriers,[21]Falco eleonorae Eleonora's falcons,[22]Cuculus canorus common cuckoos[23]), the general flyways of terrestrial birds have been inadequately studied. However, in 2014, La Sorte et al. provided a general description of terrestrial bird flyways in North America.[18] They defined 3 flyways: the single distinct Western flyway and 2 overlapping flyways, the Central and Eastern flyways. A similar 3-flyways system (Pacific, Central, and Atlantic flyways) has been described for waterfowl;[24] however, most studies have relied on the more common 4-flyways system (Pacific, Central, Mississippi, and Atlantic flyways). In this study, we used phylogeographic approaches to investigate the relationship between WNV circulation in the United States and the flight paths of terrestrial birds.

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