Persistence of Pathogens with Short Infectious Periods in
Seasonal Tick Populations: The Relative Importance of
Three Transmission Routes
Etsuko Nonaka1*°Ë, Gregory D. Ebel2, Helen J. Wearing1
1 Department of Biology and Department of Mathematics and Statistics,
University of New Mexico, Albuquerque, New Mexico, United States of America, 2
Department of
Pathology, University of New Mexico Medical School, Albuquerque, New
Mexico, United States of America
Abstract
Background: 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.
Methodology/Principal Findings: 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.
Conclusions/Significance: 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.
Citation: Nonaka E, Ebel GD, Wearing HJ (2010) Persistence of Pathogens
with Short Infectious Periods in Seasonal Tick Populations: The Relative
Importance of
Three Transmission Routes. PLoS ONE 5(7): e11745.
doi:10.1371/journal.pone.0011745
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