Determinants of Crimean-Congo haemorrhagic fever virus exposure dynamics in Mediterranean environments

Abstract

Crimean-Congo haemorrhagic fever (CCHF) is an emerging tick-borne human disease in Spain. Understanding the spatiotemporal dynamics and exposure risk determinants of CCHF virus (CCHFV) in animal models is essential to predict the time and areas of highest transmission risk. With this goal, we designed a longitudinal survey of two wild ungulate species, the red deer (Cervus elaphus) and the Eurasian wild boar (Sus scrofa), in Doñana National Park, a protected Mediterranean biodiversity hotspot with high ungulate and CCHFV vector abundance, and which is also one of the main stopover sites for migratory birds between Africa and western Europe. Both ungulates are hosts to the principal CCHFV vector in Spain, Hyalomma lusitanicum. We sampled wild ungulates annually from 2005 to 2020 and analysed the frequency of exposure to CCHFV by a double-antigen ELISA. The annual exposure risk was modelled as a function of environmental traits in an approach to understanding exposure risk determinants that allow us to predict the most likely places and years for CCHFV transmission. The main findings show that H. lusitanicum abundance is a fundamental driver of the fine-scale spatial CCHFV transmission risk, while inter-annual risk variation is conditioned by virus/vector hosts, host community structure and weather variations. The most relevant conclusion of the study is that the emergence of CCHF in Spain might be associated with recent wild ungulate population changes promoting higher vector abundance. This work provides relevant insights into the transmission dynamics of CCHFV in enzootic scenarios that would allow deepening the understanding of the ecology of CCHFV and its major determinants.

Keywords: disease ecology; host-tick-pathogen interactions; tick; wild ungulates; zoonosis.

FIGURE 1

Location of Doñana National Park in peninsular Spain (right) and the exact location of red deer (white dots) and Eurasian wild boar (grey dots) at the sampling time. The boundaries of the five livestock management areas in which the Park is divided to its West are shown (dotted lines)

FIGURE 2

Charts displaying the comparative dynamics of Crimean–Congo haemorrhagic fever virus transmission throughout host species (top chart) and host age class (bottom chart)

FIGURE 3

Spatial relationship between predicted Hyalomma lusitanicum abundance (average number of ticks per individual wild ungulate host) at UTM 250 × 250 m and the patterns of exposure to Crimean–Congo haemorrhagic fever virus of red deer (a) and Eurasian wild boar (b)