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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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The relationship between peak prevalence and prevalence growth rate is modulated by prion persistence and the functional form of transmission.The mean prevalence growth rate calculated as the average growth rate during the first 10 years of the CWD epidemic, is plotted against the peak prevalence reached over the course of the entire CWD epidemic for (A) density-dependent (ε = 0), (B) intermediate (ε = 0.0001), and (C) frequency-dependent (ε = 1) transmission scenarios that assume both direct and indirect transmission. Plots include simulations with aggregated (k = 0.01, 1) and non-aggregated (k = 10000) transmission risk. Prion persistence is represented by color (cyan = direct transmission only, red = 3 month half life (HL), dark blue = 1 yr HL, green = 4 yr HL, yellow = 6 yr HL, black = 8 yr HL). Gray symbols represent model simulations that were not considered plausible given the epidemic characteristics observed in Colorado, Wyoming, and Wisconsin. Note the scale difference in the y-axis between plots A, B, and C. See Table 1 for βd and βi values employed in these simulations.
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pone-0019896-g004: The relationship between peak prevalence and prevalence growth rate is modulated by prion persistence and the functional form of transmission.The mean prevalence growth rate calculated as the average growth rate during the first 10 years of the CWD epidemic, is plotted against the peak prevalence reached over the course of the entire CWD epidemic for (A) density-dependent (ε = 0), (B) intermediate (ε = 0.0001), and (C) frequency-dependent (ε = 1) transmission scenarios that assume both direct and indirect transmission. Plots include simulations with aggregated (k = 0.01, 1) and non-aggregated (k = 10000) transmission risk. Prion persistence is represented by color (cyan = direct transmission only, red = 3 month half life (HL), dark blue = 1 yr HL, green = 4 yr HL, yellow = 6 yr HL, black = 8 yr HL). Gray symbols represent model simulations that were not considered plausible given the epidemic characteristics observed in Colorado, Wyoming, and Wisconsin. Note the scale difference in the y-axis between plots A, B, and C. See Table 1 for βd and βi values employed in these simulations.

Mentions: When we assumed that CWD is spread only through direct transmission, there were very few simulations that yielded plausible dynamics (Figure 3). Density-dependent (ε = 0) transmission generally produced oscillations in disease prevalence and host population size which dampened over time, converging on an endemic equilibrium (that is, if the initial oscillation did not result in host extinction) (Figure 3, column 1). We found that the initial prevalence growth rate and peak prevalence were tightly and positively correlated (Figure 4, cyan markers). Under direct, frequency-dependent transmission (ε = 1), the relationship between the initial prevalence growth rate and peak prevalence was variable, and host extinction was a much more probable outcome when compared to the other functional forms of transmission (Figure 3, column 3). Slightly frequency-dependent transmission (ε = 0.0001) yielded intermediate results where CWD prevalence often reached endemic equilibrium, but with greater propensities for more severe host population declines. Aggregation (k = 0.01 or 1) had the effect of dampening or eliminating oscillations in prevalence and host population size when we assumed transmission to be either density-dependent or weakly frequency-dependent (Figure S3).


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)

The relationship between peak prevalence and prevalence growth rate is modulated by prion persistence and the functional form of transmission.The mean prevalence growth rate calculated as the average growth rate during the first 10 years of the CWD epidemic, is plotted against the peak prevalence reached over the course of the entire CWD epidemic for (A) density-dependent (ε = 0), (B) intermediate (ε = 0.0001), and (C) frequency-dependent (ε = 1) transmission scenarios that assume both direct and indirect transmission. Plots include simulations with aggregated (k = 0.01, 1) and non-aggregated (k = 10000) transmission risk. Prion persistence is represented by color (cyan = direct transmission only, red = 3 month half life (HL), dark blue = 1 yr HL, green = 4 yr HL, yellow = 6 yr HL, black = 8 yr HL). Gray symbols represent model simulations that were not considered plausible given the epidemic characteristics observed in Colorado, Wyoming, and Wisconsin. Note the scale difference in the y-axis between plots A, B, and C. See Table 1 for βd and βi values employed in these simulations.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0019896-g004: The relationship between peak prevalence and prevalence growth rate is modulated by prion persistence and the functional form of transmission.The mean prevalence growth rate calculated as the average growth rate during the first 10 years of the CWD epidemic, is plotted against the peak prevalence reached over the course of the entire CWD epidemic for (A) density-dependent (ε = 0), (B) intermediate (ε = 0.0001), and (C) frequency-dependent (ε = 1) transmission scenarios that assume both direct and indirect transmission. Plots include simulations with aggregated (k = 0.01, 1) and non-aggregated (k = 10000) transmission risk. Prion persistence is represented by color (cyan = direct transmission only, red = 3 month half life (HL), dark blue = 1 yr HL, green = 4 yr HL, yellow = 6 yr HL, black = 8 yr HL). Gray symbols represent model simulations that were not considered plausible given the epidemic characteristics observed in Colorado, Wyoming, and Wisconsin. Note the scale difference in the y-axis between plots A, B, and C. See Table 1 for βd and βi values employed in these simulations.
Mentions: When we assumed that CWD is spread only through direct transmission, there were very few simulations that yielded plausible dynamics (Figure 3). Density-dependent (ε = 0) transmission generally produced oscillations in disease prevalence and host population size which dampened over time, converging on an endemic equilibrium (that is, if the initial oscillation did not result in host extinction) (Figure 3, column 1). We found that the initial prevalence growth rate and peak prevalence were tightly and positively correlated (Figure 4, cyan markers). Under direct, frequency-dependent transmission (ε = 1), the relationship between the initial prevalence growth rate and peak prevalence was variable, and host extinction was a much more probable outcome when compared to the other functional forms of transmission (Figure 3, column 3). Slightly frequency-dependent transmission (ε = 0.0001) yielded intermediate results where CWD prevalence often reached endemic equilibrium, but with greater propensities for more severe host population declines. Aggregation (k = 0.01 or 1) had the effect of dampening or eliminating oscillations in prevalence and host population size when we assumed transmission to be either density-dependent or weakly frequency-dependent (Figure S3).

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