Abstract

BackgroundThe 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 FindingsWe 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/SignificanceOur 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.

Highlights

  • Tick-borne encephalitis virus (TBEV) causes thousands of human cases of tick-borne encephalitis (TBE) in Europe and Asia every year [1,2,3]

  • Tick life cycle We mainly focus on the ecology of the transmission cycle of Powassan virus (POWV) involving I. scapularis in upper mid-western and northeastern regions of the United States, where ticks typically have a two year life cycle (Fig. 1)

  • Tick-borne flaviviruses are known to occur at relatively consistent, low prevalence in tick populations [11,12]

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Summary

Introduction

Tick-borne encephalitis virus (TBEV) causes thousands of human cases of tick-borne encephalitis (TBE) in Europe and Asia every year [1,2,3]. Reports of TBE due to infection with other members of the tick-borne encephalitis serological complex – Powassan virus and the related ‘‘deer tick virus’’ [both referred to hereafter as Powassan virus (POWV)] – have been increasing in the north-eastern and north central United States and south-eastern Canada [4,5]. This group of encephalitis-causing viruses belongs to the genus Flavivirus and infection can result in severe morbidity, long-term neurological sequelae, and possible death [6,7,8]. Our aim is to evaluate the influence of seasonality on the relative importance of different transmission routes by using a comprehensive mathematical model

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