Increased Relative Risk of Tick-Borne Encephalitis in Warmer Weather

Abstract

Tick-borne encephalitis (TBE) is a serious acute neuroinfection of humans caused by a tick-borne flavivirus. The disease is typically seasonal, linked to the host-seeking activity of Ixodes ricinus (predominantly nymphs), the principal European tick vector species. To address the need for accurate risk predictions of contracting TBE, data on 4,044 TBE cases reported in the Czech Republic during 2001-2006 were compared with questing activity of I. ricinus nymphs monitored weekly at a defined location for the same 6-year period. A time shift of 21 days between infected tick bite and recorded disease onset provided the optimal model for comparing the number of cases of TBE with numbers of questing nymphs. Mean annual distribution of TBE cases and tick counts showed a similar bimodal distribution. Significantly, the ratio of TBE cases to questing nymphs was highest in the summer-autumn period even though the number of questing nymphs peaked in the spring-summer period. However, this pattern changed during a period of extreme meteorological events of flooding and abnormally high temperatures, indicating that changes in climate affect the incidence of TBE. Previous studies failed to link human behavior with changes in incidence of TBE but showed extrinsic temperature impacts arbovirus replication. Hence, we hypothesize the apparent discrepancy between peak nymphal tick activity and greatest risk of contracting TBE is due to the effect of temperature on virus replication in the tick vector. Relative proportions of questing nymphs and the numbers of weeks in which they were found were greater in summer-autumn compared with spring-summer at near-ground temperatures >5°C and at standard day and weekly average temperatures of >15°C. Thus, during the summer-autumn period, the virus dose in infected tick bites is likely greater owing to increased virus replication at higher microclimatic temperatures, consequently increasing the relative risk of contracting TBE per summer-autumn tick bite. The data support the use of weather-based forecasts of tick attack risk (based on daytime ambient temperature) supplemented with weekly average temperature (as a proxy for virus replication) to provide much-needed real-time forecasts of TBE risk.

Keywords: Ixodes ricinus; TBEV; arbovirus; climate change; seasonality; tick-borne encephalitis.

Figure 1

Cases of TBE in the Czech Republic by calendar week of onset of clinical symptoms. Data from the Czech EPIDAT database for 2001–2006.

Figure 2

Seasonal activity of Ixodes ricinus nymphs by week of collection and incidence of TBE by week of onset. Data for 2001–2006 are compared using a 3-week shift in alignment. Spring-summer and summer-autumn periods are distinguished by the sharp drop in number of questing nymphs around week 22 and fall in near ground temperature to 10–12°C (Daniel et al., 2015).

Figure 3

Analysis of the effect of a 1–6 week time shift on the estimated time of infection using Akaike's (AIC) and Bayesian (BIC) information criteria. The two criteria were used to select the best model in the group of models (1–6 week shift) compared. Lower criterion values indicate the preferred model.

Figure 4

Inter-seasonal comparison of the linear regression relationship between numbers of host-questing Ixodes ricinus nymphs and cases of TBE. Square root transformation was used for both axes together with a 3-week shift in alignment.

Figure 5

Inter-annual comparison of the linear regression relationship between numbers of host-questing Ixodes ricinus nymphs and cases of TBE. Year-on-year comparison for 2001–2006 of the regression lines for (A) the spring-summer period, and (B) the summer- autumn period. Square root transformation was used for both axes with a 3-week shift in alignment.

Figure 6

Host-questing Ixodes ricinus nymphs in spring-summer and summer-autumn compared with near-ground, standard day, and weekly average temperatures. Data for 2006.

Figure 7

Proportions of host-questing Ixodes ricinus nymphs active at different temperature categories in spring-summer compared with summer-autumn periods. Proportions are expressed as % questing nymphs evaluated against near-ground, standard day, and weekly average temperatures.

Figure 8

Relative proportions of nymphs and numbers of weeks in which they were found at different temperature categories in spring-summer and summer-autumn. Based on (A) near-ground temperature measured in the tick habitat, (B) standard day temperature measured by the CHMI observatory, and (C) weekly average of temperature derived from the CHMI database.