Tick-Borne Encephalitis Virus: Seasonal and Annual Variation of Epidemiological Parameters Related to Nymph-to-Larva Transmission and Exposure of Small Mammals

Abstract

<jats:p>A greater knowledge of the ecology of the natural foci of tick-borne encephalitis virus (TBEV) is essential to better assess the temporal variations of the risk of tick-borne encephalitis for humans. To describe the seasonal and inter-annual variations of the TBEV-cycle and the epidemiological parameters related to TBEV nymph-to-larva transmission, exposure of small mammals to TBEV, and tick aggregation on small mammals, a longitudinal survey in ticks and small mammals was conducted over a 3-year period in a mountain forest in Alsace, eastern France. TBEV prevalence in questing nymphs was lower in 2013 than in 2012 and 2014, probably because small mammals (Myodes glareolus and Apodemus flavicollis) were more abundant in 2012, which reduced tick aggregation and co-feeding transmission between ticks. The prevalence of TBEV in questing nymphs was higher in autumn than spring. Despite these variations in prevalence, the density of infected questing nymphs was constant over time, leading to a constant risk for humans. The seroprevalence of small mammals was also constant over time, although the proportion of rodents infested with ticks varied between years and seasons. Our results draw attention to the importance of considering the complex relationship between small mammal densities, tick aggregation on small mammals, density of infected questing nymphs, and prevalence of infected nymphs in order to forecast the risk of TBEV for humans.</jats:p>

Disappearance of TBEV Circulation among Rodents in a Natural Focus in Alsace, Eastern France

“…The seasonal abundance of small mammals was also the highest at the end of spring to early summer. This confirmed the results previously described on the same study site over a shorter timespan [ 16 ]. The synchronous activity of larvae and nymphs, as observed at other sites at risk for TBEV [ 11 , 20 , 21 ], is usually recognized to be essential for the maintenance of TBEV by favouring transmission through co-feeding [ 3 , 4 , 7 , 22 ].…”

“…TBEV dynamics on this site might also be very sensitive to stochastic processes influencing the probability of contact between infected nymphs and rodents that can sometimes lead to virus extinction via endemic fadeouts [ 31 ], given the marked fluctuation in the rodent population and the low tick infestation of rodents. The number of ticks per rodent on this site observed in 2012 (a year with a high rodent density) and 2013 (a year with a low rodent density) was low (with a median of fewer than five ticks/rodents infested by ticks [ 16 ]) compared to other sites in Central Europe where TBEV is present (where the median ranges from ten to 80 ticks per infested rodent [ 11 , 21 , 32 ]). With the low number of feeding ticks per rodent observed in this study and the high density of deer present on the site, even a small variation in the number of questing nymphs or deer density could disrupt the virus transmission cycle by decreasing the number of infected nymphs feeding on rodents [ 13 ].…”

“…This may reflect either a local disappearance of TBEV after 2015 or a low, undetected, exposure of rodents to TBEV, with a seroprevalence below 0.8% in 2017. Our previous results showed that the density of infected nymphs was constant from 2012 to 2014 [ 16 ]. The ticks collected since 2015 were also tested for TBEV, but the number of tested samples was too low to have a high probability of detecting TBEV if the virus was present ( Supplementary Material 1 ).…”

“…The study took place in the same area as described in [ 16 ]. Briefly, the study site covers an area of 4 ha at Murbach (altitude of 630 m) in Guebwiller valley in the French region of Alsace (47°55′03 N, 07°08′46 E).…”

“…We had previously investigated the characteristics of the epidemiological cycle of TBEV in a Vosgian forest in Alsace (Murbach) from 2012 to 2014. The site was already known as a high-risk site for human contamination, and our investigations revealed that both the density of infected questing nymphs and the seroprevalence among small rodents were constant over time [ 16 ]. In the current study, our objective was to monitor the persistence of TBEV circulation between small mammals and ticks on the same site and to discuss it in relation to the synchronous activity of larvae and nymphs, to the densities of questing nymphs and small mammals, and to potential changes in meteorological conditions and deer density.…”