Persistence of pathogens with short infectious periods in seasonal tick populations: the relative importance of three transmission routes.

The flaviviruses causing tick-borne encephalitis (TBE) persist at low but consistent levels in tick populations, despite short infectious periods in their mammalian hosts and transmission periods constrained by distinctly seasonal tick life cycles. In addition to systemic and vertical transmission,...

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Main Authors: Etsuko Nonaka, Gregory D Ebel, Helen J Wearing
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2010-07-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC2909195?pdf=render
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spelling doaj-5964360cfcbe4d27a2ccba4bf389af7e2020-11-25T01:21:22ZengPublic Library of Science (PLoS)PLoS ONE1932-62032010-07-0157e1174510.1371/journal.pone.0011745Persistence of pathogens with short infectious periods in seasonal tick populations: the relative importance of three transmission routes.Etsuko NonakaGregory D EbelHelen J WearingThe flaviviruses causing tick-borne encephalitis (TBE) persist at low but consistent levels in tick populations, despite short infectious periods in their mammalian hosts and transmission periods constrained by distinctly seasonal tick life cycles. In addition to systemic and vertical transmission, cofeeding transmission has been proposed as an important route for the persistence of TBE-causing viruses. Because cofeeding transmission requires ticks to feed simultaneously, the timing of tick activity may be critical to pathogen persistence. Existing models of tick-borne diseases do not incorporate all transmission routes and tick seasonality. Our aim is to evaluate the influence of seasonality on the relative importance of different transmission routes by using a comprehensive mathematical model.We developed a stage-structured population model that includes tick seasonality and evaluated the relative importance of the transmission routes for pathogens with short infectious periods, in particular Powassan virus (POWV) and the related "deer tick virus," emergent encephalitis-causing flaviviruses in North America. We used the next generation matrix method to calculate the basic reproductive ratio and performed elasticity analyses. We confirmed that cofeeding transmission is critically important for such pathogens to persist in seasonal tick populations over the reasonable range of parameter values. At higher but still plausible rates of vertical transmission, our model suggests that vertical transmission can strongly enhance pathogen prevalence when it operates in combination with cofeeding transmission.Our results demonstrate that the consistent prevalence of POWV observed in tick populations could be maintained by a combination of low vertical, intermediate cofeeding and high systemic transmission rates. When vertical transmission is weak, nymphal ticks support integral parts of the transmission cycle that are critical for maintaining the pathogen. We also extended the model to pathogens that cause chronic infections in hosts and found that cofeeding transmission could contribute to elevating prevalence even in these systems. Therefore, the common assumption that cofeeding transmission is not relevant in models of chronic host infection, such as Lyme disease, could lead to underestimating pathogen prevalence.http://europepmc.org/articles/PMC2909195?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Etsuko Nonaka
Gregory D Ebel
Helen J Wearing
spellingShingle Etsuko Nonaka
Gregory D Ebel
Helen J Wearing
Persistence of pathogens with short infectious periods in seasonal tick populations: the relative importance of three transmission routes.
PLoS ONE
author_facet Etsuko Nonaka
Gregory D Ebel
Helen J Wearing
author_sort Etsuko Nonaka
title Persistence of pathogens with short infectious periods in seasonal tick populations: the relative importance of three transmission routes.
title_short Persistence of pathogens with short infectious periods in seasonal tick populations: the relative importance of three transmission routes.
title_full Persistence of pathogens with short infectious periods in seasonal tick populations: the relative importance of three transmission routes.
title_fullStr Persistence of pathogens with short infectious periods in seasonal tick populations: the relative importance of three transmission routes.
title_full_unstemmed Persistence of pathogens with short infectious periods in seasonal tick populations: the relative importance of three transmission routes.
title_sort persistence of pathogens with short infectious periods in seasonal tick populations: the relative importance of three transmission routes.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2010-07-01
description The flaviviruses causing tick-borne encephalitis (TBE) persist at low but consistent levels in tick populations, despite short infectious periods in their mammalian hosts and transmission periods constrained by distinctly seasonal tick life cycles. In addition to systemic and vertical transmission, cofeeding transmission has been proposed as an important route for the persistence of TBE-causing viruses. Because cofeeding transmission requires ticks to feed simultaneously, the timing of tick activity may be critical to pathogen persistence. Existing models of tick-borne diseases do not incorporate all transmission routes and tick seasonality. Our aim is to evaluate the influence of seasonality on the relative importance of different transmission routes by using a comprehensive mathematical model.We developed a stage-structured population model that includes tick seasonality and evaluated the relative importance of the transmission routes for pathogens with short infectious periods, in particular Powassan virus (POWV) and the related "deer tick virus," emergent encephalitis-causing flaviviruses in North America. We used the next generation matrix method to calculate the basic reproductive ratio and performed elasticity analyses. We confirmed that cofeeding transmission is critically important for such pathogens to persist in seasonal tick populations over the reasonable range of parameter values. At higher but still plausible rates of vertical transmission, our model suggests that vertical transmission can strongly enhance pathogen prevalence when it operates in combination with cofeeding transmission.Our results demonstrate that the consistent prevalence of POWV observed in tick populations could be maintained by a combination of low vertical, intermediate cofeeding and high systemic transmission rates. When vertical transmission is weak, nymphal ticks support integral parts of the transmission cycle that are critical for maintaining the pathogen. We also extended the model to pathogens that cause chronic infections in hosts and found that cofeeding transmission could contribute to elevating prevalence even in these systems. Therefore, the common assumption that cofeeding transmission is not relevant in models of chronic host infection, such as Lyme disease, could lead to underestimating pathogen prevalence.
url http://europepmc.org/articles/PMC2909195?pdf=render
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