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      Modeling Routes of Chronic Wasting Disease Transmission: Environmental Prion Persistence Promotes Deer Population Decline and Extinction

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          Abstract

          Chronic wasting disease (CWD) is a fatal disease of deer, elk, and moose transmitted through direct, animal-to-animal contact, and indirectly, via environmental contamination. Considerable attention has been paid to modeling direct transmission, but despite the fact that CWD prions can remain infectious in the environment for years, relatively little information exists about the potential effects of indirect transmission on CWD dynamics. In the present study, we use simulation models to demonstrate how indirect transmission and the duration of environmental prion persistence may affect epidemics of CWD and populations of North American deer. Existing data from Colorado, Wyoming, and Wisconsin's CWD epidemics were used to define plausible short-term outcomes and associated parameter spaces. Resulting long-term outcomes range from relatively low disease prevalence and limited host-population decline to host-population collapse and extinction. Our models suggest that disease prevalence and the severity of population decline is driven by the duration that prions remain infectious in the environment. Despite relatively low epidemic growth rates, the basic reproductive number, R 0, may be much larger than expected under the direct-transmission paradigm because the infectious period can vastly exceed the host's life span. High prion persistence is expected to lead to an increasing environmental pool of prions during the early phases (i.e. approximately during the first 50 years) of the epidemic. As a consequence, over this period of time, disease dynamics will become more heavily influenced by indirect transmission, which may explain some of the observed regional differences in age and sex-specific disease patterns. This suggests management interventions, such as culling or vaccination, will become increasingly less effective as CWD epidemics progress.

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          Environmental Sources of Prion Transmission in Mule Deer

          Whether transmission of the chronic wasting disease (CWD) prion among cervids requires direct interaction with infected animals has been unclear. We report that CWD can be transmitted to susceptible animals indirectly, from environments contaminated by excreta or decomposed carcasses. Under experimental conditions, mule deer (Odocoileus hemionus) became infected in two of three paddocks containing naturally infected deer, in two of three paddocks where infected deer carcasses had decomposed in situ ≈1.8 years earlier, and in one of three paddocks where infected deer had last resided 2.2 years earlier. Indirect transmission and environmental persistence of infectious prions will complicate efforts to control CWD and perhaps other animal prion diseases.
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            Realistic distributions of infectious periods in epidemic models: changing patterns of persistence and dynamics.

            Most mathematical models used to study the epidemiology of childhood viral diseases, such as measles, describe the period of infectiousness by an exponential distribution. The effects of including more realistic descriptions of the infectious period within SIR (susceptible/infectious/recovered) models are studied. Less dispersed distributions are seen to have two important epidemiological consequences. First, less stable behaviour is seen within the model: incidence patterns become more complex. Second, disease persistence is diminished: in models with a finite population, the minimum population size needed to allow disease persistence increases. The assumption made concerning the infectious period distribution is of a kind routinely made in the formulation of mathematical models in population biology. Since it has a major effect on the central issues of population persistence and dynamics, the results of this study have broad implications for mathematical modellers of a wide range of biological systems. Copyright 2001 Academic Press.
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              Infectious Diseases and Extinction Risk in Wild Mammals

              Abstract:  Parasite‐driven declines in wildlife have become increasingly common and can pose significant risks to natural populations. We used the IUCN Red List of Threatened and Endangered Species and compiled data on hosts threatened by infectious disease and their parasites to better understand the role of infectious disease in contemporary host extinctions. The majority of mammal species considered threatened by parasites were either carnivores or artiodactyls, two clades that include the majority of domesticated animals. Parasites affecting host threat status were predominantly viruses and bacteria that infect a wide range of host species, including domesticated animals. Counter to our predictions, parasites transmitted by close contact were more likely to cause extinction risk than those transmitted by other routes. Mammal species threatened by parasites were not better studied for infectious diseases than other threatened mammals and did not have more parasites or differ in four key traits demonstrated to affect parasite species richness in other comparative studies. Our findings underscore the need for better information concerning the distribution and impacts of infectious diseases in populations of endangered mammals. In addition, our results suggest that evolutionary similarity to domesticated animals may be a key factor associated with parasite‐mediated declines; thus, efforts to limit contact between domesticated hosts and wildlife could reduce extinction risk.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                13 May 2011
                : 6
                : 5
                : e19896
                Affiliations
                [1 ]Northern Rocky Mountain Science Center, United States Geological Survey, Bozeman, Montana, United States of America
                [2 ]The Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, Pennsylvania, United States of America
                [3 ]Prion Research Laboratory, National Wildlife Health Center, United States Geological Survey, Madison, Wisconsin, United States of America
                [4 ]National Wildlife Health Center, United States Geological Survey, Madison, Wisconsin, United States of America
                Albert Einstein College of Medicine, United States of America
                Author notes

                Conceived and designed the experiments: ESA PCC. Performed the experiments: ESA PCC. Analyzed the data: ESA PCC CJJ DMH BJR. Contributed reagents/materials/analysis tools: BJR CJJ DMH. Wrote the paper: ESA PCC CJJ DMH BJR.

                Article
                PONE-D-10-04610
                10.1371/journal.pone.0019896
                3094393
                21603638
                fd17f23e-70a3-4a3f-add6-54f2717a767b
                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
                History
                : 10 November 2010
                : 19 April 2011
                Page count
                Pages: 11
                Categories
                Research Article
                Biology
                Ecology
                Conservation Science
                Population Ecology
                Population Biology
                Population Dynamics
                Disease Dynamics
                Population Modeling

                Uncategorized
                Uncategorized

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