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.

Epidemiologic Survey of Crimean-Congo Hemorrhagic Fever Virus in Suids, Spain

“…Adults were at 3.6 times higher risk of CCHFV exposure than yearlings, which could be associated with the higher probability of tick bites throughout the life of adult wild boar and with the persistence of CCHFV antibodies over time. This finding is in line with those of Cuadrado-Matías et al ( 13 ) and with previous studies that linked the age of cattle with greater seropositivity to CCHFV antibodies ( 35 – 37 ). On the other hand, female wild boar had significantly higher seroprevalence than males.…”

“…As of February 2024, all surveys conducted worldwide in wild boar have been done in Spain, except for 1 in Turkey, where 2.5% of wild boar were exposed to the virus ( 28 ). The seroprevalence detected in this species in our study (39.7%) is in accordance with the 40.6% obtained in this species in Doñana National Park in southwestern Spain ( 13 ) and indicates a high exposure of wild boar populations to CCHFV in this region of Spain. In contrast, lower frequencies of seropositivity were found in northeastern Spain, where 3.2% of wild boar showed antibodies against CCHFV ( 15 ), and eastern Spain, where 15.3% of wild boar had antibodies ( 16 ).…”

Animal Exposure Model for Mapping Crimean-Congo Hemorrhagic Fever Virus Emergence Risk

“…Although some of the human cases of CCHF in Spain could be associated with farm animals, research on domestic species is limited ( 38 ). Most studies in Spain have focused on wild ungulates because of their relevance to CCHFV ( 24 , 25 ), but even so, farm animals and their ticks may pose a risk for humans through closer contact. By selecting small domestic ruminants, we aimed to identify the areas of greatest risk for transmission to persons in contact with them and thus complement the risk maps previously obtained by using red deer ( 13 ).…”

“…Cattle and horses are relevant hosts for H. marginatum ticks ( 6 , 23 , 32 , 41 ) and may be more abundant than wild ungulates in the vicinity of small ruminant farms, so their association with CCHFV was not unexpected. Previous studies already described the relevant role of farm animals in the risk for exposure to CCHFV ( 24 , 43 ). Among domestic animals, global CCHFV seroprevalence is second highest among cattle, after camels ( 44 ).…”

“…Because seroepidemiologic studies in animals, along with identification of CCHFV ecologic drivers, can provide insights into CCHFV transmission dynamics ( 13 ), resulting in better preventive strategies for the human population at risk, we designed a cross-sectional serosurvey of domestic small ruminants in a CCHFV-enzootic region of Spain, Andalusia ( 17 , 24 ), and statistically modeled exposure risk with environment-associated predictors to map infection risk hotspots. Our working hypothesis was that estimating ecologic drivers of CCHFV exposure risk in small domestic ruminants would reveal the spatial risk for virus transmission to humans.…”