Dynamics of Crimean-Congo hemorrhagic fever virus in two wild ungulate hosts in northeastern Spain
Crimean-Congo hemorrhagic fever virus (CCHFV) is a pathogen transmitted by ticks, mostly from the genus Hyalomma, which are in expansion in southern Europe. The natural cycle of CCHFV involves ticks of different stages that feed on several domestic and wild animal species, and occasionally on humans. Although animals do not develop symptoms, they can get infected by CCHFV and produce antibodies. Therefore, detecting CCHFV antibodies in animals is a useful tool for evaluating in which areas this virus is circulating.
In humans, CCHFV infection can cause a fatal hemorrhagic systemic disease. In Spain, Crimean-Congo hemorrhagic fever (CCHF) is considered an emerging disease and, by 2022, twelve human cases have been diagnosed since 2013, three of them being fatal. All these cases were concentrated in western and southern Spain. There, CCHFV epidemiology and transmission in animals have been thoroughly studied and the presence of red deer (Cervus elaphus) is considered an indicator of CCHFV infection risk for humans.
In the north-eastern Mediterranean regions of Spain, where red deer density is very low, no CCHF human cases have been detected so far. However, an antibody survey in wildlife detected a hotspot of high seropositivity in Iberian ibex (Capra pyrenaica) in the Ports de Tortosa i Beseit Natural Park (PTiBNP) in Tarragona, with a lower seroprevalence in Eurasian wild boar (Sus scrofa), indicating that the virus was circulating in this area.
In 2014, an outbreak of sarcoptic mange was detected in Iberian ibex from the PTiBNP and reduced its population by more than 85% in 2021. Since the abundance of wild ungulates seemed to have an effect on the risk of exposure to CCHFV, this sarcoptic mange outbreak represented an interesting scenario to evaluate whether this population decline had any effect on CCHFV circulation in PTiBNP.
Therefore, a team of researchers from the Wildlife Conservation Medicine research group (WildCoM) from the UAB and from IRTA-CReSA conducted a study to evaluate the trends of annual CCHFV seroprevalence in Iberian ibex and wild boar between 2013 and 2021, as well as their population trends. We observed that, while wild boar population size remained constant over time, the Iberian ibex population declined from more than 3,000 individuals before the sarcoptic mange outbreak, to less than 500 by 2021. Interestingly, this population decline was correlated with a decline in CCHFV antibodies in wild boar, while the Iberian ibex seroprevalence remained at 100% for the whole study period. The correlation between the Iberian ibex population and the proportion of wild boars with antibodies against CCHFV suggests that both species have a common CCHFV transmission cycle, probably through the sharing of the same tick vectors.
Since the tick species community parasitizing wild boar and Iberian ibex in this area was unknown, we also performed a tick survey. Between May and July 2023, we sampled ticks from the environment and hunted Iberian ibex and wild boars. Moreover, meteorological factors can also influence CCHFV transmission, either through the effect on viral replication and spread within the tick (mainly determined by temperature), or through the effect of meteorological factors on tick abundance. Thus, we also evaluated whether changes in ambient temperature and vapor pressure deficit (VPD) in the atmosphere, considered the most influential meteorological factors, may have influenced the dynamics of CCHFV transmission in the PTiBNP throughout the study period. As the pattern of temperature and VPD remained quite regular throughout the study period, these meteorological factors do not seem to have played a role in the reduction of CCHFV seroprevalence in wild boars.
We observed that Rhipicephalus bursa was the most abundant tick in the environment (89.2%), Iberian ibex (89.8%) and wild boar (44.9%); while Hyalomma spp. abundance was lower in the environment (1.0%), Iberian ibex (0.2%) and wild boar (25.6%). Hyalomma spp. are considered the main vectors of CCHFV in southern and western Spain, but with the very low abundance of these ticks in Iberian ibex in the PTiBNP, they are unlikely responsible for the 100% of seroprevalence detected in this species.
In contrast, Rhipicephalus bursa, the most abundant tick in PTiBNP, has also been suggested as an important CCHFV tick vector in other countries, although experimental studies are needed to confirm its efficiency in transmitting the virus. Considering this and the results of our study, we suspect that there is a connection between CCHFV transmission cycles in Iberian ibex and wild boars involving R. bursa (rather than Hyalomma spp.).
This study evidence that CCHFV epidemiology in Spain is complex and spatiotemporally heterogeneous, and highlights the importance of identifying the drivers of CCHFV transmission in each different ecosystem since both biotic (vectors, hosts, pathogens) and abiotic (climate, habitat) factors differ among areas. As such, CCHFV circulation in northeastern Spain seems to differ from southern and western Spain. A deeper understanding of the drivers of CCHFV circulation in northeastern Spain is needed in order to help prevent the emergence of human cases in this region.
Authors: Sebastian Napp and Oscar Cabezón
