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      Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA

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          Abstract

          Background

          Models of the effects of environmental factors on West Nile virus disease risk have yielded conflicting outcomes. The role of precipitation has been especially difficult to discern from existing studies, due in part to habitat and behavior characteristics of specific vector species and because of differences in the temporal and spatial scales of the published studies. We used spatial and statistical modeling techniques to analyze and forecast fine scale spatial (2000 m grid) and temporal (weekly) patterns of West Nile virus mosquito infection relative to changing weather conditions in the urban landscape of the greater Chicago, Illinois, region for the years from 2004 to 2008.

          Results

          Increased air temperature was the strongest temporal predictor of increased infection in Culex pipiens and Culex restuans mosquitoes, with cumulative high temperature differences being a key factor distinguishing years with higher mosquito infection and higher human illness rates from those with lower rates. Drier conditions in the spring followed by wetter conditions just prior to an increase in infection were factors in some but not all years. Overall, 80% of the weekly variation in mosquito infection was explained by prior weather conditions. Spatially, lower precipitation was the most important variable predicting stronger mosquito infection; precipitation and temperature alone could explain the pattern of spatial variability better than could other environmental variables (79% explained in the best model). Variables related to impervious surfaces and elevation differences were of modest importance in the spatial model.

          Conclusion

          Finely grained temporal and spatial patterns of precipitation and air temperature have a consistent and significant impact on the timing and location of increased mosquito infection in the northeastern Illinois study area. The use of local weather data at multiple monitoring locations and the integration of mosquito infection data from numerous sources across several years are important to the strength of the models presented. The other spatial environmental factors that tended to be important, including impervious surfaces and elevation measures, would mediate the effect of rainfall on soils and in urban catch basins. Changes in weather patterns with global climate change make it especially important to improve our ability to predict how inter-related local weather and environmental factors affect vectors and vector-borne disease risk.

          Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA.

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          Most cited references 62

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          Spatial epidemiology: an emerging (or re-emerging) discipline.

          Spatial epidemiology is the study of spatial variation in disease risk or incidence. Several ecological processes can result in strong spatial patterns of such risk or incidence: for example, pathogen dispersal might be highly localized, vectors or reservoirs for pathogens might be spatially restricted, or susceptible hosts might be clumped. Here, we briefly describe approaches to spatial epidemiology that are spatially implicit, such as metapopulation models of disease transmission, and then focus on research in spatial epidemiology that is spatially explicit, such as the creation of risk maps for particular geographical areas. Although the spatial dynamics of infectious diseases are the subject of intensive study, the impacts of landscape structure on epidemiological processes have so far been neglected. The few studies that demonstrate how landscape composition (types of elements) and configuration (spatial positions of those elements) influence disease risk or incidence suggest that a true integration of landscape ecology with epidemiology will be fruitful.
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            Epidemiology and Transmission Dynamics of West Nile Virus Disease

            West Nile virus (WNV) was first detected in the Western Hemisphere in 1999 during an outbreak of encephalitis in New York City. Over the next 5 years, the virus spread across the continental United States as well as north into Canada, and southward into the Caribbean Islands and Latin America (1). This article highlights new information about the epidemiology and transmission dynamics of human WNV disease obtained over the past 5 years of intensified research. Epidemiology WNV is transmitted primarily by the bite of infected mosquitoes that acquire the virus by feeding on infected birds. The intensity of transmission to humans is dependent on abundance and feeding patterns of infected mosquitoes and on local ecology and behavior that influence human exposure to mosquitoes. Although up to 55% of affected populations became infected during epidemics in Africa, more recent outbreaks in Europe and North America have yielded much lower attack rates (1,2). In the area of most intense WNV transmission in Queens, New York, in 1999, ≈2.6% of residents were infected (most of these were asymptomatic infections), and similarly low prevalence of infection has been seen in other areas of the United States (3,4). WNV outbreaks in Europe and the Middle East since 1995 appear to have caused infection in 1,000 potentially WNV-viremic blood donations were identified, and the corresponding blood components were sequestered. Nevertheless, 6 WNV cases due to transfusion were documented in 2003, and at least 1 was documented in 2004, indicating that infectious blood components with low concentrations of WNV may escape current screening tests (19). One instance of possible WNV transmission through dialysis has been reported (20). WNV transmission through organ transplantation was also first described during the 2002 epidemic (15). Chronically immunosuppressed organ transplant patients appear to have an increased risk for severe WNV disease, even after mosquito-acquired infection (16). During 2002, the estimated risk of neuroinvasive WNV disease in solid organ transplant patients in Toronto, Canada, was approximately 40 times greater than in the general population (16). Whether other immunosuppressed or immunocompromised patients are at increased risk for severe WNV disease is uncertain, but severe WNV disease has been described among immunocompromised patients. WNV infection has been occupationally acquired by laboratory workers through percutaneous inoculation and possibly through aerosol exposure (21,22). An outbreak of WNV disease among turkey handlers at a turkey farm raised the possibility of aerosol exposure (17). Dynamics of Transmission: Vectors WNV is transmitted primarily by Culex mosquitoes, but other genera may also be vectors (23). In Europe and Africa, the principal vectors are Cx. pipiens, Cx. univittatus, and Cx. antennatus, and in India, species of the Cx. vishnui complex (6,24). In Australia, Kunjin virus is transmitted primarily by Cx. annulirostris (11). In North America, WNV has been found in 59 different mosquito species with diverse ecology and behavior; however, 40%. Field studies during and after WNV outbreaks in several areas of the United States have confirmed that house sparrows were abundant and frequently infected with WNV, characteristics that would allow them to serve as important amplifying hosts (23,25,37). The importance of birds in dispersing WNV remains speculative. Local movements of resident, nonmigratory birds and long-range travel of migratory birds may both contribute to the spread of WNV (38,39). Although WNV was isolated from rodents in Nigeria and a bat in India, most mammals do not appear to generate viremia levels of sufficient titer to contribute to transmission (24,40–42). Three reptilian and 1 amphibian species (red-ear slider, garter snake, green iguana, and North American bullfrog) were found to be incompetent as amplifying hosts of a North American WNV strain, and no signs of illness developed in these animals (43). Viremia levels of sufficient titer to infect mosquitoes were found after experimental infection of young alligators (Alligator mississippiensis) (44). In Russia, the lake frog (Rana ridibunda) appears to be a competent reservoir (45). Nonmosquitoborne WNV transmission has been observed or strongly suspected among farmed alligators, domestic turkeys in Wisconsin, and domestic geese in Canada (17,46,47). Transmission through close contact has been confirmed in both birds and alligators in laboratory conditions but has yet to be documented in wild vertebrate populations (23,36,44). Control of WNV Transmission Avoiding human exposure to WNV-infected mosquitoes remains the cornerstone for preventing WNV disease. Source reduction, application of larvicides, and targeted spraying of pesticides to kill adult mosquitoes can reduce the abundance of mosquitoes, but demonstrating their impact on the incidence of human WNV disease is challenging because of the difficulty in accounting for all determinants of mosquito abundance and human exposure. One study indicated that clustering of human WNV disease in Chicago varied between mosquito abatement districts, suggesting that mosquito control may have some impact on transmission to humans (14). Persons in WNV-endemic areas should wear insect repellent on skin and clothes when exposed to mosquitoes and avoid being outdoors during dusk to dawn when mosquito vectors of WNV are abundant. Of insect repellents recommended for use on skin, those containing N,N-diethyl-m-toluamide (DEET), picaridin (KBR-3023), or oil of lemon eucalyptus (p-menthane-3,8 diol) provide long-lasting protection (48). Both DEET and permethrin provide effective protection against mosquitoes when applied to clothing. Persons' willingness to use DEET as a repellent appears to be influenced primarily by their level of concern about being bitten by mosquitoes and by their concern that DEET may be harmful to health, despite its good safety record (49). To prevent transmission of WNV through blood transfusion, blood donations in WNV-endemic areas should be screened by using nucleic acid amplification tests. Screening of organ donors for WNV infection has not been universally implemented because of concern about rejecting essential organs after false-positive screening results (50). Pregnant women should avoid exposure to mosquito bites to reduce the risk for intrauterine WNV transmission. Future Directions WNV disease will likely continue to be a public health concern for the foreseeable future; the virus has become established in a broad range of ecologic settings and is transmitted by a relatively large number of mosquito species. WNV will also likely continue to spread into Central and South America, but the public health implications of this spread remain uncertain. Observations thus far in North America indicate that circulation of other flaviviruses, such as dengue, viral mutation, and differing ecologic conditions may yield different clinical manifestations and transmission dynamics. Over the next few years, research efforts might well be focused in several areas. Research into new methods to reduce human exposure to mosquitoes is crucial and can help prevent other mosquitoborne illnesses. This should include development of new methods to reduce mosquito abundance, development of new repellents, and behavioral research to enhance the use of existing effective repellents and other personal protective measures against mosquito bites. A better understanding of the dynamics of nonmosquitoborne transmission is essential to prevent disease among infants of infected mothers and recipients of blood transfusions and transplanted organs. Currently available prevention strategies such as the dissemination of knowledge and products for personal protection from mosquito exposure and the application of existing techniques for reducing mosquito abundance in communities at risk of WNV transmission need to be vigorously implemented. National and international surveillance for WNV transmission will be important to monitor spread of the virus and the effect of control strategies. Finally, further research into the ecologic determinants of WNV transmission, including climatic factors and dynamics of reservoir and vector populations, could help in determining geographic areas of higher risk for WNV disease.
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              Machine learning methods without tears: a primer for ecologists.

              Machine learning methods, a family of statistical techniques with origins in the field of artificial intelligence, are recognized as holding great promise for the advancement of understanding and prediction about ecological phenomena. These modeling techniques are flexible enough to handle complex problems with multiple interacting elements and typically outcompete traditional approaches (e.g., generalized linear models), making them ideal for modeling ecological systems. Despite their inherent advantages, a review of the literature reveals only a modest use of these approaches in ecology as compared to other disciplines. One potential explanation for this lack of interest is that machine learning techniques do not fall neatly into the class of statistical modeling approaches with which most ecologists are familiar. In this paper, we provide an introduction to three machine learning approaches that can be broadly used by ecologists: classification and regression trees, artificial neural networks, and evolutionary computation. For each approach, we provide a brief background to the methodology, give examples of its application in ecology, describe model development and implementation, discuss strengths and weaknesses, explore the availability of statistical software, and provide an illustrative example. Although the ecological application of machine learning approaches has increased, there remains considerable skepticism with respect to the role of these techniques in ecology. Our review encourages a greater understanding of machin learning approaches and promotes their future application and utilization, while also providing a basis from which ecologists can make informed decisions about whether to select or avoid these approaches in their future modeling endeavors.
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                Author and article information

                Journal
                Parasit Vectors
                Parasites & Vectors
                BioMed Central
                1756-3305
                2010
                19 March 2010
                : 3
                : 19
                Affiliations
                [1 ]Department of Pathobiology, University of Illinois, Urbana, Illinois, USA
                [2 ]Department of Environmental Studies, Emory University, Atlanta, Georgia, USA
                [3 ]Department of Pathobiological Sciences, University of Wisconsin, Madison, Wisconsin, USA
                [4 ]Department of Microbiology and Molecular Genetics, Michigan State University, Lansing, MI. USA
                [5 ]Vector Control Program, Illinois Department of Public Health, Springfield, Illinois, USA
                [6 ]Fogarty International Center, National Institutes of Health, Bethesda, MD 20892, USA
                Article
                1756-3305-3-19
                10.1186/1756-3305-3-19
                2856545
                20302617
                Copyright ©2010 Ruiz et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Categories
                Research

                Parasitology

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