Forest structure and roe deer abundance predict tick-borne encephalitis risk in Italy

Abstract

Background: The Western Tick-borne encephalitis (TBE) virus often causes devastating or lethal disease. In Europe, the number of human TBE cases has increased dramatically over the last decade, risk areas are expanding and new foci are being discovered every year. The early localisation of new TBE foci and the identification of the main risk factors associated with disease emergence represent a priority for the public health community. Although a number of socio-economic parameters have been suggested to explain TBE upsurges in eastern Europe, the principal driving factors in relatively stable western European countries have not been identified.

Methodology/principal findings: In this paper, we analyse the correlation between the upsurge of TBE in 17 alpine provinces in northern Italy from 1992 to 2006 with climatic variables, forest structure (as a proxy for small mammal reservoir host abundance), and abundance of the principal large vertebrate tick host (roe deer), using datasets available for the last 40 years. No significant differences between the pattern of changes in climatic variables in provinces where TBE has emerged compared to provinces were no clinical TBE cases have been observed to date. Instead, the best model for explaining the increase in TBE incidence in humans in this area include changes in forest structure, in particular the ratio of coppice to high stand forest, and the density of roe deer.

Conclusion/significance: Substantial changes in vegetation structure that improve habitat suitability for the main TBE reservoir hosts (small mammals), as well as an increase in roe deer abundance due to changes in land and wildlife management practices, are likely to be among the most crucial factors affecting the circulation potential of Western TBE virus and, consequently, the risk of TBE emergence in humans in western Europe. We believe our approach will be useful in predicting TBE risk on a wider scale.

Figure 1. TBE-positive and TBE-negative provinces in northern Italy.

(AL = Alessandria; AO = Aosta; BG = Bergamo; BL = Belluno; BS = Brescia; BZ = Bolzano; CN = Cuneo; GO = Gorizia; NO = Novara; PN = Pordenone; TN = Trento; TO = Torino; TV = Treviso; UD = Udine; VA = Varese; VI = Vicenza; VR = Verona).

Figure 2. TBE incidence.

Mean annual TBE incidence (number of cases/100 000 inhabitants) and annual TBE confirmed human cases in the TBE-positive provinces.

Figure 3. TBE human cases aggregated per age class.

Figure 4. Trends in climatic variables.

Annual total precipitation (top), annual minimum (middle) and maximum (bottom) daily air temperature in the TBE-negative provinces (panels A) and TBE-positive provinces (panels B) in northern Italy from 1950 to 2006 (see also Fig. 1).

Figure 5. Forest variables.

Total coppices and high forest surface coverage recorded in TBE-negative provinces (panel A) and TBE-positive provinces (panel B) (see also Fig. 1).

Figure 6. Wildlife variables.

Boxplot of mean values of coppice to high forest ratio (cop.hfor) (panel A) and roe deer abundance (panel B) in TBE-positive and TBE-negative provinces of northern Italy (see also Fig. 1).