The importance of wildlife in the ecology and epidemiology of the TBE virus in Sweden: incidence of human TBE correlates with abundance of deer and hares

Abstract

BackgroundTick-borne encephalitis (TBE) is one tick-transmitted disease where the human incidence has increased in some European regions during the last two decades. We aim to find the most important factors causing the increasing incidence of human TBE in Sweden. Based on a review of published data we presume that certain temperature-related variables and the population densities of transmission hosts, i.e. small mammals, and of primary tick maintenance hosts, i.e. cervids and lagomorphs, of the TBE virus vector Ixodes ricinus, are among the potentially most important factors affecting the TBE incidence. Therefore, we compare hunting data of the major tick maintenance hosts and two of their important predators, and four climatic variables with the annual numbers of human cases of neuroinvasive TBE. Data for six Swedish regions where human TBE incidence is high or has recently increased are examined by a time-series analysis. Results from the six regions are combined using a meta-analytical method.ResultsWith a one-year time lag, the roe deer (Capreolus capreolus), red deer (Cervus elaphus), mountain hare (Lepus timidus) and European hare (Lepus europaeus) showed positive covariance; the Eurasian elk (moose, Alces alces) and fallow deer (Dama dama) negative covariance; whereas the wild boar (Sus scrofa), lynx (Lynx lynx), red fox (Vulpes vulpes) and the four climate parameters showed no significant covariance with TBE incidence. All game species combined showed positive covariance.ConclusionsThe epidemiology of TBE varies with time and geography and depends on numerous factors, i.a. climate, virus genotypes, and densities of vectors, tick maintenance hosts and transmission hosts. This study suggests that the increased availability of deer to I. ricinus over large areas of potential tick habitats in southern Sweden increased the density and range of I. ricinus and created new TBEV foci, which resulted in increased incidence of human TBE. New foci may be established by TBE virus-infected birds, or by birds or migrating mammals infested with TBEV-infected ticks. Generally, persistence of TBE virus foci appears to require presence of transmission-competent small mammals, especially mice (Apodemus spp.) or bank voles (Myodes glareolus).Electronic supplementary materialThe online version of this article (10.1186/s13071-018-3057-4) contains supplementary material, which is available to authorized users.

Revealing new tick-borne encephalitis virus foci by screening antibodies in sheep milk

“…The endemic area has expanded from the area around Stockholm to provinces in the south-west and south of Sweden, regions that are far from previously known endemic areas [8]. A recent study suggests that new TBEV foci have emerged as the density and range of the virus vector Ixodes ricinus tick has increased due to the increased availability of the roe deer (Capreolus capreolus), thus creating large areas of potential tick habitats in southern Sweden, which in turn is likely to have contributed to the increase of human TBE cases [10]. However, the circulation of the virus in nature and the epidemiology of TBE is dependent on a number of different factors.…”

“…However, the circulation of the virus in nature and the epidemiology of TBE is dependent on a number of different factors. TBEV is sensitive to various environmental factors, such as the microclimate and the population density of different host animals [8,10]. A humidity rate of > 85%, air temperatures of > 6 °C to 7 °C, and access to hosts are the vital prerequisites for tick survival [11].…”

“…A humidity rate of > 85%, air temperatures of > 6 °C to 7 °C, and access to hosts are the vital prerequisites for tick survival [11]. Climate changes with warmer temperatures during winter may also be beneficial to both ticks and hosts, and could thus possibly increase the transmission of the virus [10].…”

“…Joinpoint regression model (Joinpoint trend analysis software [28]) was used to analyse the incidence trends. The average annual percental change (AAPC) was calculated using 95% confidence interval (P < 0.05) transmission depends on the prevalence of infection in the tick population, the density of host-seeking infected ticks and the availability of tick-maintaining hosts [10]. Furthermore, socioeconomic factors and the increasing rate of human outdoor activities also have roles in the expansion of TBE disease in Europe [11].…”

Recent establishment of tick-borne encephalitis foci with distinct viral lineages in the Helsinki area, Finland

“…TBEV circulation in nature is very sensitive to various environmental factors such as microclimate and host animal population density [21,[47][48][49]. Intriguingly, the sequence variation within the two foci of which more than one strain was sequenced was rather high, suggesting that the introduction of TBEV into these two foci has occurred most likely decades ago.…”