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Modeling routes of chronic wasting disease transmission: environmental prion persistence promotes deer population decline and extinction.

Almberg ES, Cross PC, Johnson CJ, Heisey DM, Richards BJ - PLoS ONE (2011)

Bottom Line: 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.This suggests management interventions, such as culling or vaccination, will become increasingly less effective as CWD epidemics progress.

View Article: PubMed Central - PubMed

Affiliation: Northern Rocky Mountain Science Center, United States Geological Survey, Bozeman, Montana, United States of America. esa5046@psu.edu

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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Schematic of density (DD) and frequency (FD) dependent transmission applied to direct and indirect transmission.Dots and circles represent deer and their home ranges, and red stars represent infectious prions in the environment. Deer and prion contacts (means denoted by and cd and cp) are defined by shared or overlapping home range edges, and home range overlap with prions, respectively. A) Under DD direct transmission, increasing host density (by a factor of 4) is assumed to increase host contact rates. B) Under FD direct transmission, spatial or social structuring keeps contact rates largely independent of host density (the slight increase displayed is due to edge effects). C) Under DD indirect transmission, increasing prion density (by a factor of 4) increases prion contacts. D) Under FD indirect transmission, prion contacts scale with host density; as host density increases, spatial structuring reduces home range size and hence per capita rates of prion contact.
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pone-0019896-g001: Schematic of density (DD) and frequency (FD) dependent transmission applied to direct and indirect transmission.Dots and circles represent deer and their home ranges, and red stars represent infectious prions in the environment. Deer and prion contacts (means denoted by and cd and cp) are defined by shared or overlapping home range edges, and home range overlap with prions, respectively. A) Under DD direct transmission, increasing host density (by a factor of 4) is assumed to increase host contact rates. B) Under FD direct transmission, spatial or social structuring keeps contact rates largely independent of host density (the slight increase displayed is due to edge effects). C) Under DD indirect transmission, increasing prion density (by a factor of 4) increases prion contacts. D) Under FD indirect transmission, prion contacts scale with host density; as host density increases, spatial structuring reduces home range size and hence per capita rates of prion contact.

Mentions: We modeled transmission to include both direct and indirect transmission over a range of functional forms and aggregation. We temporarily ignore births and deaths as we develop our transmission model below. Let Z and S be the infectious and susceptible counts, respectively, where Z = I+C and N = S+E+I+C. Let the environmental concentration of prions be V. The force-of-infection, λ, is the instantaneous per capita infection rate, and can be modeled as λ = βdZ+βiV where βd and βi are, respectively, the direct and indirect transmission coefficients. Such a model is appropriate for systems where the direct and indirect transmission rates are dependent on the density of hosts and the concentration of prions in the environment, respectively. This model generalizes the classical concept of density-dependent transmission to both direct and indirect transmission. An alternative model, which similarly generalizes the classic concept of frequency-dependence, is λ = (βdZ+βiV )/N. Such a model is appropriate if spatial partitioning, such as social grouping or rigid territories, makes the direct contact rate independent of total population density. However, under this model formulation, the indirect contact rate becomes dependent on total population density. We suggest that although contact rates with the environment might be fixed, the proportion of contaminated environment encountered may be inversely related to total host density. As N increases, individual home ranges may decrease in size [45], [46], reducing the proportion of the landscape encountered on a per capita basis. As a result environmental transmission rates may decrease with increasing deer numbers for a given level of prion contamination (Figure 1).


Modeling routes of chronic wasting disease transmission: environmental prion persistence promotes deer population decline and extinction.

Almberg ES, Cross PC, Johnson CJ, Heisey DM, Richards BJ - PLoS ONE (2011)

Schematic of density (DD) and frequency (FD) dependent transmission applied to direct and indirect transmission.Dots and circles represent deer and their home ranges, and red stars represent infectious prions in the environment. Deer and prion contacts (means denoted by and cd and cp) are defined by shared or overlapping home range edges, and home range overlap with prions, respectively. A) Under DD direct transmission, increasing host density (by a factor of 4) is assumed to increase host contact rates. B) Under FD direct transmission, spatial or social structuring keeps contact rates largely independent of host density (the slight increase displayed is due to edge effects). C) Under DD indirect transmission, increasing prion density (by a factor of 4) increases prion contacts. D) Under FD indirect transmission, prion contacts scale with host density; as host density increases, spatial structuring reduces home range size and hence per capita rates of prion contact.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3094393&req=5

pone-0019896-g001: Schematic of density (DD) and frequency (FD) dependent transmission applied to direct and indirect transmission.Dots and circles represent deer and their home ranges, and red stars represent infectious prions in the environment. Deer and prion contacts (means denoted by and cd and cp) are defined by shared or overlapping home range edges, and home range overlap with prions, respectively. A) Under DD direct transmission, increasing host density (by a factor of 4) is assumed to increase host contact rates. B) Under FD direct transmission, spatial or social structuring keeps contact rates largely independent of host density (the slight increase displayed is due to edge effects). C) Under DD indirect transmission, increasing prion density (by a factor of 4) increases prion contacts. D) Under FD indirect transmission, prion contacts scale with host density; as host density increases, spatial structuring reduces home range size and hence per capita rates of prion contact.
Mentions: We modeled transmission to include both direct and indirect transmission over a range of functional forms and aggregation. We temporarily ignore births and deaths as we develop our transmission model below. Let Z and S be the infectious and susceptible counts, respectively, where Z = I+C and N = S+E+I+C. Let the environmental concentration of prions be V. The force-of-infection, λ, is the instantaneous per capita infection rate, and can be modeled as λ = βdZ+βiV where βd and βi are, respectively, the direct and indirect transmission coefficients. Such a model is appropriate for systems where the direct and indirect transmission rates are dependent on the density of hosts and the concentration of prions in the environment, respectively. This model generalizes the classical concept of density-dependent transmission to both direct and indirect transmission. An alternative model, which similarly generalizes the classic concept of frequency-dependence, is λ = (βdZ+βiV )/N. Such a model is appropriate if spatial partitioning, such as social grouping or rigid territories, makes the direct contact rate independent of total population density. However, under this model formulation, the indirect contact rate becomes dependent on total population density. We suggest that although contact rates with the environment might be fixed, the proportion of contaminated environment encountered may be inversely related to total host density. As N increases, individual home ranges may decrease in size [45], [46], reducing the proportion of the landscape encountered on a per capita basis. As a result environmental transmission rates may decrease with increasing deer numbers for a given level of prion contamination (Figure 1).

Bottom Line: 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.This suggests management interventions, such as culling or vaccination, will become increasingly less effective as CWD epidemics progress.

View Article: PubMed Central - PubMed

Affiliation: Northern Rocky Mountain Science Center, United States Geological Survey, Bozeman, Montana, United States of America. esa5046@psu.edu

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.

Show MeSH
Related in: MedlinePlus