Red deer reveal spatial risks of Crimean‐Congo haemorrhagic fever virus infection

Abstract

Crimean‐Congo haemorrhagic fever virus (CCHFV) continues to cause new human cases in Iberia while its spatial distribution and ecological determinants remain unknown. The virus remains active in a silent tick‐animal cycle to which animals contribute maintaining the tick populations and the virus itself. Wild ungulates, in particular red deer, are essential hosts for Hyalomma ticks in Iberia, which are the principal competent vector of CCHFV. Red deer could be an excellent model to understand the ecological determinants of CCHFV as well as to predict infection risks for humans because it is large, gregarious, abundant and the principal host for Hyalomma lusitanicum. We designed a cross‐sectional study, analysed the presence of CCHFV antibodies in 1444 deer from 82 populations, and statistically modelled exposure risk with host and environmental predictors. The best‐fitted statistical model was projected for peninsular Spain to map infection risks. Fifty out of 82 deer populations were seropositive, with individual population prevalence as high as 88%. The highest prevalence of exposure to CCHFV occurred in the southwest of the Iberian Peninsula. Climate and ungulate abundance were the most influential predictors of the risk of exposure to the virus. The highest risk regions were those where H. lusitanicum is most abundant. Eight of the nine primary human cases occurred in or bordering these regions, demonstrating that the model predicts human infection risk accurately. A recent human case of CCHF occurred in northwestern Spain, a region that the model predicted as low risk, pointing out that it needs improvement to capture all determinants of the CCHFV infection risk. In this study, we have been able to identify the main ecological determinants of CCHFV, and we have also managed to create an accurate model to assess the risk of CCHFV infection.

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

“…Species abundance data are generally limited in space and time, especially invertebrates. Only in cases where invertebrates are of conservation interest (Micó et al, 2013), or relevant as pests (Ørsted et al, 2021), or if they are vectors of health-threatening pathogens (Jaenson et al, 2012), is there inter- We recently demonstrated the relevance of the main H. lusitanicum host in Iberia, the red deer, to map CCHFV transmission risk (Cuadrado-Matías et al, 2022). However, most infectious processes are dynamic and linked to the wide variety of environmental and population determinants that modulate the inter-and intraspecific interactions between animal species, or with pathogen vectors (Casades-Martí et al, 2020;González-Barrio, Almería, et al, 2015).…”

The spatial pattern of human exposure to Crimean–Congo haemorrhagic fever virus is not consistent with red deer‐based risk predictions

“…This study was carried out as a representative survey of the risk for the overall human population in an area where CCHFV circulates enzootically in an animal‐tick silent cycle (Cuadrado‐Matías et al., 2022 ; Moraga‐Fernández et al., 2021 ). The 0.4% of the surface of Ciudad Real province was identified as under very high risk of CCHFV infection based on the red deer exposure risk model.…”

“…Spatial representation of the serosurvey performed in Ciudad Real province according to a gradient of increasing risk of Crimean–Congo haemorrhagic fever virus (CCHFV) infection based on a predictive model built with data from red deer ( Cervus elaphus ) surveyed across the Iberian Peninsula (Cuadrado‐Matías et al., 2022). (a) The 2020 human census ( www.ine.es/) against sample size per municipality.…”

“…The present study was designed based on the map of CCHFV predicted exposure risk from a virus‐red deer model at the UTM 10 × 10 km spatial resolution (Cuadrado‐Matías et al., 2022 ; Figure 1 ) and on the availability of samples from the four different risk gradients identified in the region. The province of Ciudad Real is environmentally very heterogeneous, including densely forested areas on the west and large areas of cereal crop plains on the north‐east.…”

“…Since 2013, confirmed CCHF human cases have emerged in Spain: one in 2013; two in 2016; two in 2018; three in 2020 and two in 2021 (Negredo et al., 2017 , 2021a , 2021b ), pointing out the need to assess the rate of exposure to the virus of humans in risk areas (Monsalve‐Arteaga et al., 2021 , 2020 ). A recent study performed by our group (Cuadrado‐Matías et al., 2022 ) mapped the risk of exposure to CCHFV in peninsular Spain using the red deer ( Cervus elaphus ) as a model, a widespread and abundant wild ungulate in Spain that hosts high burdens of Hyalomma ticks. This study identified the southwestern quarter of Spain as the highest risk region in the country.…”