Ecology of West Nile Virus Transmission

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Ecology of West Nile Virus Transmission
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  1121 The Auk  A Quarterly  Journal of Ornithology Vol. 124 No. 4 October 2007 W   N      (WNV) was introduced into the western hemisphere in 1999 near New York City, where it caused substantial mortality in corvids and a small number of human cases (Nash et al. 2001). Genetic analysis showed that the introduced virus was most similar to a geno-type isolated in Israel in 1998 (Lancio t i et al. 1999), and more virulent for some bird species (but not for others) than genotypes from Kenya and Australia (Kunjin virus) (Brault et al. 2004, 2007; Langevin et al. 2005). The virus is a plus-sense single-stranded RNA virus in the family Flaviviridae, which also includes Japanese encephalitis, St. Louis encephalitis, yellow fever, and dengue fever viruses (Hayes 1989).From 1999 to 2006, WNV caused 26,274 reported human cases in the United States and Canada, including 9,942 cases of encephalitis, and 1,008 deaths (Centers for Disease Control and Prevention [CDC] 2007, Health Canada 2007). The actual number of infections, based on serosurveys, is estimated to be more than 1.4 million, with ∼ 280,000 illnesses (Petersen and Hayes 2004, CDC 2007). West Nile virus has also caused widespread disease in horses in North America (with ∼ 40% of cases being fatal) and tens of thousands of deaths before the advent of vaccination (Hall and Khromykh 2004). Several human vaccines are being devel-oped, but so far none have been approved for use by the Federal Drug Administration (FDA) (Kramer et al. 2007). In contrast to the situation in North America, few human or horse ill-nesses have been observed in the tropics. The reasons for the absence of WNV in the tropics are unknown, but several hypothetical explana-tions have been put forth, including the idea that protective immunity has been conferred from other circulating fl aviviruses, di ff  erences in the avian-host and mosquito-vector com-munities, and di ff  erences in the virulence of the virus when it circulates in the tropics (Tesh et al. 2002, Weaver and Barre t  2004, Fang and Reisen 2006, Komar and Clark 2006).Substantial research has been done on many aspects of WNV virology, ecology, and public health since its introduction in 1999. There have  been several recent reviews of the ecology of WNV transmission (Komar 2003, Marra et al. 2004, Weaver and Barre t  2004, Hayes et al. 2005), and a large body of literature is available on a closely related virus, the St. Louis encepha-litis virus (Monath 1980). However, since the most recent reviews were published, substantial work has been done that greatly increases our understanding of the distribution and ecology of transmission of this virus and its e ff  ect on 3 E-mail: kilpatrick@conservationmedicine.org The Auk  124(4):1121–1136, 2007© The American Ornithologists’ Union, 2007. Printed in USA. PERSPECTIVES IN ORNITHOLOGY  ECOLOGY OF WEST NILE VIRUS TRANSMISSION AND ITS IMPACT ON BIRDS IN THE WESTERN HEMISPHERE A. M arm  K ilpatrick  , 1,3  S hannon  L. L a D eau  , 2   and  P eter  P. M arra 2 1 Consortium for Conservation Medicine, 460 West 34th Street, 17th  fl oor, New York, New York 10001, USA; and 2 Smithsonian Migratory Bird Center, National Zoological Park, P.O. Box 37012, MRC 5508, Washington, D.C. 20013, USA  Perspectives in Ornithology 1122 [Auk, Vol. 124  bird populations. The present review focuses on insights gained in these areas and highlights several areas of research that require immediate a t ention.S pread Distribution .—By 2004, just fi ve years a  er its introduction, WNV had spread throughout much of the United States, including 47 of the 48 lower states, into 9 provinces in Canada, throughout Mexico, onto several islands in the Caribbean, and into several countries in Central and South America (Dupuis et al. 2003, 2005; Estrada-Franco et al. 2003; Cruz et al. 2005; Ma t ar et al. 2005; Farfan-Ale et al. 2006; Komar and Clark 2006; Morales et al. 2006; Bosch et al. 2007) (Fig. 1). Its apparent absence from countries in Central and South America is more likely a t ributable to a lack of e ff  ort to detect it than to the absence of the virus, because all these countries share migratory birds and other pathways (see below) with countries where it has been shown to be circulating (Fig. 1). In the United States, Canada, Mexico, and Argentina, the virus has been isolated from mosquitoes,  birds, humans, or horses. However, within the tropical latitudes south of Mexico, no viral isolates have been obtained except for a recent (2007) isolate from Puerto Rico (L. D. Kramer pers. comm.). Evidence of local transmission has been based primarily on the presence of WNV-speci fi c antibodies in resident birds or horses. Comparison of antibody titres using F ig . 1. Year of first detection of West Nile virus (WNV) in the Western Hemisphere. The virus may have been introduced months or even years earlier than when it was first detected.  Perspectives in Ornithology October 2007] 1123 plaque-reduction neutralization assays has  been used to exclude the possibility that WNV- neutralizing antibodies resulted from exposure to other cross-reacting fl aviviruses. Pathways of spread. —The pathways by which WNV has and will spread are di ffi  cult to determine but likely include migrating birds, dispersal of nonmigratory birds, movement of mosquitoes by fl ight or wind, and human transport of mosquitoes, birds, or other ani-mals (Rappole et al. 2000; Peterson et al. 2003; Kilpatrick et al. 2004, 2006b; Reisen et al. 2004). E ff  orts to determine the role of migrating birds in the spread of WNV have included labora-tory infection studies with birds in migratory condition (Owen et al. 2006), e ff  orts to isolate virus from birds during migratory periods (R. McLean et al. unpubl. data), sampling of birds killed by communication towers and skyscrap-ers (P. Marra and A. DuPuis unpubl. data), and modeling e ff  orts (Peterson et al. 2003). So far, none of these studies have provided conclusive evidence that migratory birds are transporting the virus long distances. De fi nitive evidence would require tracking a known viremic (virus in the blood) bird in the process of migration.E cology   of  T ransmission Transmission cycle. —West Nile virus is  believed to be transmi t ed primarily between mosquitoes and birds in a bird-to-mosquito-to-bird cycle (see below for a discussion of the role of mammals). When mosquitoes feed on an infected or viremic bird, some fraction may become infected, depending on the mag-nitude of viremia and the susceptibility of the mosquito (Turell et al. 2002). A  er 1–14 days (depending on temperature; L. D. Kramer et al. unpubl. data), the virus may escape the midgut of the mosquito and infect the salivary glands, resulting in an infectious mosquito (Turell et al. 2002). Following a bite from this infectious mos-quito, nearly all birds and mammals become infected, and most exhibit a viremic period of one to seven days (occasionally longer; Komar et al. 2003) that completes the cycle.For birds that survive (death usually occurs  between days 4 and 8 postinfection; Komar et al. 2003), antibodies begin to appear a  er day 4 (Styer et al. 2006). These antibodies are long-lasting and confer protection against re-infection with WNV (Fang and Reisen 2006). In addition, there appears to be some cross-protection against several fl aviviruses, including WNV and St. Louis and Japanese encephalitis viruses (Tesh et al. 2002, Fang and Reisen 2006). Other modes of transmission have been demonstrated, including direct bird-to-bird transmission (Komar et al. 2003), vertical transmission in mosquitoes (that may facilitate overwintering of the virus) (Nasci et al. 2001, Dohm et al. 2002b), and nearly instantaneous transmission between infected and uninfected mosquitoes simultaneously feeding on the same host. This last mode was srcinally believed to  be nonviremic transmission (Higgs et al. 2005). Recent evidence suggests that infection of these cofeeding mosquitoes appears to be caused by a transient viremia from virus injected into the host by the infected mosquito, rather than by nonviremic transmission (Reisen et al. 2007b). Vectors. —At least 62 species of mosquitoes have tested positive for WNV infection in North America (CDC 2007). However, fi nd-ing a mosquito infected with WNV does not imply transmission or importance in transmis-sion dynamics. Determining the importance of each species in local transmission requires quantitatively integrating mosquito abundance, prevalence of infection, vector competence, feeding behavior and, where possible, longev-ity (Reeves 1965, Kilpatrick et al. 2005). The results of such an analysis suggest that only a few (one to three) species at each site play important roles in enzootic (bird-to-bird) or epi-demic (bird-to-human) transmission (Kilpatrick et al. 2005). The primary enzootic and epizootic vectors in northeast and north-central North America appear to be Culex pipiens  and Cx. restuans  (Kilpatrick et al. 2005). These species are o  en relatively abundant, are moderately competent, frequently show the highest preva-lence of infection, and feed in large part on  birds but also, sometimes, on humans and other mammals (Bernard et al. 2001; Andreadis et al. 2004; Kilpatrick et al. 2005, 2006c, d). In some locations, Cx. salinarius  may also be an impor-tant epizootic or bridge vector (Andreadis et al. 2004), because it feeds frequently on both birds and mammals (Kilpatrick et al. 2005).Quantitative analyses of vector importance are lacking for other regions, but species believed to be important on the basis of available data include Cx. quinquefasciatus  across southern  Perspectives in Ornithology 1124 [Auk, Vol. 124 North America and in Central and South America (Turell et al. 2005), Cx. nigripalpus  and Cx. errati-cus  in southeastern parts of the United States (Blackmore et al. 2003, Cupp et al. 2007), and C. tarsalis  across much of western North America (Reisen et al. 2004, Turell et al. 2005). Culex pipi-ens  may also be important in urban areas in the western United States (Bolling et al. 2007). Other species of mosquitoes, including  Aedes albopictus  and  Ae. vexans  , have been proposed as potential epizootic or bridge vectors (Turell et al. 2005), but the only quantitative analysis performed so far suggested that  Ae. vexans  and other non- Culex  species were relatively unimportant in transmis-sion to humans and other mammals (Kilpatrick et al. 2005) and would be even less important for  bird-to-bird transmission.Vectors other than mosquitoes have also  been considered in the transmission of WNV. Laboratory transmission was demonstrated in so   ticks (Hutcheson et al. 2005) but did not occur in hard ixodid ticks (Reisen et al. 2007a). In general, ticks are not believed to play a major role in enzootic transmission but may act as a reservoir, because they can remain infected for long periods (Lawrie et al. 2004). Hosts. —The importance of each vertebrate host in viral transmission depends on (1) host-reservoir competence, which is a function of the intensity and duration of viremia and survival of WNV-infected birds; and (2) contact rates  between that host and competent mosquito vec-tors (Hammon et al. 1943, Sco t  1988). Although ≥ 317 species of birds and ≥ 30 species of mammals have been found infected with WNV (Marra et al. 2004, CDC 2007), only a very small subset of these are likely to play important roles in WNV transmission. The only analysis, so far, to quantitatively integrate data on these two factors showed that a single relatively uncommon spe-cies, American Robin ( Turdus migratorius ), was responsible for ∼ 60% of WNV-infectious mos-quitoes across fi ve residential and urban sites in the mid-Atlantic United States (Kilpatrick et al. 2006c).Laboratory infection studies to estimate host competence have been published for 44 species of nondomesticated birds in 23 families and 11 orders (Komar et al. 2003, 2005; Reisen et al. 2005a, b, 2006, 2007a; Clark et al. 2006; Nemeth et al. 2006; Owen et al. 2006; Reisen and Hahn 2007; Pla t  et al. 2008), 3 species of wild mam-mals (Tiawsirisup et al. 2005b, Root et al. 2006, Pla t  et al. 2007), and 5 species of reptiles and one amphibian (Klenk and Komar 2003, Klenk et al. 2004). In these experiments, animals are infected by either allowing infectious mosqui-toes to feed on them or by an intramuscular or subcutaneous injection of virus. Blood samples are then taken approximately daily until animals die or clear the virus from their blood (usually one to seven days a  er infection). These data can then be used to estimate host competence or the fraction of vectors biting an infected host that is likely to become infectious. Vertebrate host competence. —Host competence is a term that describes the infectiousness of an infected host. For WNV, it can be quanti fi ed for an individual as the sum (over the viremic period) of the daily probabilities that a mosquito  biting that bird will become infectious for WNV (Komar et al. 2003). Thus, hosts that have long viremic periods and high-titred viremias (and, thus, high infectiousness to biting mosquitoes) are highly competent. The host-competence index for a species should estimate the average infectiousness of several individuals and weigh the infectiousness of each individual equally. Calculating a numerical value of host compe-tence (e.g., the “competence index”; Komar et al. 2003) for a species requires an equation for the fraction of mosquitoes that will become infectious a  er feeding on a host as a function of host viremia. Although the viremia–infectiousness relationships appear to di ff  er for di ff  erent mosquito species, the lowest viremia that leads to any infectious–transmi t ing mos-quitoes appears to be in the range of 10 4  to 10 5  plaque-forming units (PFU) mL –1  (Sardelis et al. 2001, Reisen et al. 2005a, Tiawsirisup et al. 2005a, Turell et al. 2005 and references therein). However, this threshold is of limited impor-tance, and a t ention should be focused on the actual fraction of mosquitoes that become infec-tious, which starts at zero at ∼ 10 4.6  PFU mL –1  for Cx. pipiens  and increases linearly with the loga-rithm of host viremia (Tiawsirisup et al. 2005a). We calculated a competence index for each of the 53 wild vertebrate species that have been studied by experimental infection. We used a viremia–infectiousness relationship for Cx. pipi-ens  that was based on data from three studies of mosquitoes held at 26–27°C a  er feeding (Turell et al. 2000, Dohm et al. 2002a, Tiawsirisup et al. 2005a): % infectious (transmi t ing) = 0.1349 ×  Log10 (Viremia) – 0.6235 ( R 2  = 0.66, P  = 0.001, n  =
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