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Epidemiology of La Crosse Virus Emergence, Appalachia Region, United States Sharon Bewick, Folashade Agusto, Justin M

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Epidemiology of La Crosse Virus Emergence, Appalachia Region, United States Sharon Bewick, Folashade Agusto, Justin M Epidemiology of La Crosse Virus Emergence, Appalachia Region, United States Sharon Bewick, Folashade Agusto, Justin M. Calabrese, Ephantus J. Muturi, William F. Fagan La Crosse encephalitis is a viral disease that has emerged becoming a leading cause of encephalitis in the United in new locations across the Appalachian region of the Unit- States (7,8). For patients with severe cases, LACV disease ed States. Conventional wisdom suggests that ongoing has lifelong neurologic consequences (6) and carries an es- emergence of La Crosse virus (LACV) could stem from the timated fatality rate of 0.5%–1.9% (6,9). invasive Asian tiger (Aedes albopictus) mosquito. Efforts Previously, most LACV disease cases were associ- to prove this, however, are complicated by the numerous ated with forested areas in the midwestern United States transmission routes and species interactions involved in LACV dynamics. To analyze LACV transmission by Asian (10), where LACV was maintained through a cycle in- tiger mosquitoes, we constructed epidemiologic models. volving the eastern tree-hole mosquito (Ochlerotatus These models accurately predict empirical infection rates. triseriatus), hereafter called the tree-hole mosquito, and They do not, however, support the hypothesis that Asian mammals of 3 species: eastern chipmunks (Tamias stria- tiger mosquitoes are responsible for the recent emergence tus), gray squirrels (Sciurus carolinensis), and fox squir- of LACV at new foci. Consequently, we conclude that other rels (Sciurus niger) (10,11). However, since the mid- factors, including different invasive mosquitoes, changes in 1990s, Appalachia has emerged as a new focus for the climate variables, or changes in wildlife densities, should be disease (8,12–14). One potential explanation is the in- considered as alternative explanations for recent increases troduction of the invasive Asian tiger mosquito (Aedes in La Crosse encephalitis. albopictus), hereafter called the tiger mosquito (15). This suggestion is based on the laboratory-demonstrated n recent years, several vectorborne diseases have re- competence of the tiger mosquito (16,17), isolation of Iemerged either at new locations or to new levels in loca- LACV from field-collected tiger mosquito pools 18( ), tions where they have historically ranged. Commonly cited observation of LACV-positive tiger mosquitoes at sites factors for reemergence include evolution of novel vector of LACV infections of humans (19), and the coincidental or pathogen strains (1), increased human mobility or dis- link between tiger mosquito invasion and the emergence ease spread by infected travelers, decreased herd immunity of LACV in the Appalachian region (12). Unfortunately, (2), landscape change (3), climate change (4), and invasion although these observations demonstrate the potential of new regions by competent disease vectors (5). Although for the tiger mosquito to influence LACV dynamics, the disease translocations across continents are almost always contribution of this mosquito to observed increases in a result of human transport, pathogens that exhibit novel LACV transmission remains unclear. One obstacle to regional spread, increased transmission in preexisting loca- identifying the role of the tiger mosquito in LACV emer- tions, or both are more difficult to explain. Such is the case gence is our limited understanding of the interaction with La Crosse encephalitis, a mosquitoborne viral disease between invasive species and native disease cycles and currently emerging in the US Appalachian region (Appala- how this interaction affects disease transmission, both chia, comprising Tennessee, North Carolina, Virginia, and within natural reservoirs and to human hosts. Epidemio- West Virginia). With 30–180 cases of severe LACV disease logic modeling is a powerful tool, useful for understand- reported annually (6) and an estimated total disease an- ing the outcomes of different transmission pathways in nual incidence as high as 300,000 cases, LACV is rapidly other disease systems. To our knowledge, however, no dynamic models for LACV disease have been devel- Author affiliations: University of Maryland, College Park, Maryland, oped, even for regions where the tree-hole mosquito is USA (S. Bewick, W.F. Fagan); University of Kansas, Lawrence, the only disease vector. We therefore developed a series Kansas, USA (F. Agusto); Smithsonian Conservation Biology of compartmental models (Figure 1) for LACV. Using Institute, Front Royal, Virginia, USA (J.M. Calabrese); Illinois these models, we then explored LACV dynamics in sys- Natural History Survey, Champaign, Illinois, USA (E.J. Muturi) tems with (native) and without (invaded) tiger mosqui- toes to assess the likelihood that the tiger mosquito is DOI: http://dx.doi.org/10.3201/eid2211.160308 responsible for the emergence of LACV in Appalachia. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 22, No.11, November 2016 1921 RESEARCH Figure 1. Schematic illustrating transitions/interactions in the compartmental model for La Crosse virus disease. Subscripted 1, 2, and C denote parameters and state variables for the eastern tree-hole mosquito, Asian tiger mosquito, and host populations, respectively. State variables and parameters are described elsewhere (see Basic Model and Table A1, at http://www. clfs.umd.edu/biology/faganlab/ disease-ecology.html). Black boxes indicate infected classes; gray boxes, exposed classes; and white boxes, susceptible/recovered classes. Dashed box with gray shading demarks the subset of transitions/interactions that define the native system before tiger mosquito invasion. Methods accounts for 2 vector species and, thus, 4 transmission pathways: 1) horizontal transmission between tree-hole Model mosquitoes and chipmunks, 2) vertical (transovarial) trans- We built 3 models: 1) the tree-hole model, in which the tree- mission by tree-hole mosquitoes, 3) horizontal transmission hole mosquito is the only LACV vector; 2) the tiger model, between tiger mosquitoes and chipmunks, and 4) vertical in which the tiger mosquito is the only LACV vector; and transmission by tiger mosquitoes. To determine the relative 3) the tree-hole/tiger model, in which mosquitoes of both contributions of the different transmission pathways to R0, species simultaneously serve as LACV vectors. In the third we used elasticity analyses (20). Large elasticities indicate model, mosquitoes of either species may be driven extinct transmission routes that contribute most to disease mainte- through competitive exclusion; thus, although both vectors nance and spread (see Elasticity Analysis of Transmission are potentially present, it is possible that only 1 persists. For Pathways, at http://www.clfs.umd.edu/biology/faganlab/ all models, we assumed that the vertebrate host was the east- disease-ecology.html). ern chipmunk. The basic dynamic system (Figure 1), includ- ing all relevant assumptions and system parameterizations, is LAC Dynamics fully described elsewhere (see Basic Model, at http://www. R0 analyses reflect equilibrium conditions, which are good clfs.umd.edu/biology/faganlab/disease-ecology.html). approximations of full system behavior when seasonality is weak or when the system reaches equilibrium rapidly Basic Reproduction Number, R0 within a single season. Because the relevance of seasonal- To determine whether sustained LACV transmission is pre- ity for LACV is unknown, we also considered fully dynam- dicted, we considered the basic reproduction number, R0, ic multiseason extensions to each of our models (see LAC for each of the 3 models (see Basic Reproduction Numbers, Dynamics, at http://www.clfs.umd.edu/biology/faganlab/ R0, at http://www.clfs.umd.edu/biology/faganlab/disease- disease-ecology.html). Using dynamic simulations, we es- ecology.html). For R0>1, LACV transmission can be sus- timated the fraction of scenarios (i.e., parameter combina- tained. For R0<1, LACV will go extinct. tions) resulting in sustained LACV transmission above a critical threshold. This is the numerical equivalent of R0 but Transmission Pathways may differ as a result of seasonality. For dynamic simula- The tree-hole/tiger model, which represents current LACV tions in which LACV persists, we also quantified season- spread throughout much of Appalachia and the Midwest, long host seroprevalence rates, peak rates of mosquito 1922 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 22, No.11, November 2016 La Crosse Virus, Appalachia infection, and the timing of peak transmission to humans. true. Moreover, even when tiger and tree-hole mosquitoes Last, we considered the potential for the tiger mosquito to were predicted to coexist, the tree-hole mosquito popula- act as a bridge vector, linking LACV transmission in wild- tion declined by an average of 63% through interspecific life reservoirs to infections in human populations. competition. By contrast, interspecific competition re- duced the tiger mosquito population by an average of only Latin Hypercube Sampling 16%. Not surprisingly, then, when both mosquito species Measurements of system parameters vary, for example, as were present, most (average 78%) were tiger mosquitoes. a result of geographic differences in abiotic variables, dif- Because the tiger mosquito is the less competent of the 2 ferences in local mosquito or chipmunk populations, dif- LACV vectors, its invasion actually reduces the likelihood ferences in circulating virus strains, or measurement error. of LACV transmission. To capture model predictions over empirically determined
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