A systematic review of the occurrence of Hyalomma ticks associated with birds migrating between Africa and the Northern Hemisphere

BACKGROUND: Crimean-Congo haemorrhagic fever (CCHF) is a tick-borne disease endemic to Africa, Southern Europe, and Western Asia. Its main vectors, Hyalomma ticks, can spread to and possibly establish populations in non-endemic regions via migratory birds. METHODS: We summarized the association between migratory birds and Hyalomma ticks by analysing spatial and temporal patterns in tick prevalence and infestation intensity on migratory birds through a systematic review of studies conducted in Europe, Western Asia, and Northern Africa between 1954 and 2022. RESULTS: We reviewed 37 studies and retrieved data from one additional unpublished datasets. Overall, we collected data on the occurrence of 3876 ticks, most of which were in immature life stages, from 1553 individuals of 75 migratory bird species. The prevalence of ticks from both the Hyalomma genus and Hyalomma marginatum complex ticks (H. marginatum and H. rufipes) on migrating birds declined significantly with increasing latitude of the sampling sites in spring. Additionally, we found that the infestation intensity of both tick groups on migratory birds was significantly higher among intra-Palearctic migrants than in Afro-Palearctic migrants. CONCLUSIONS: This review underscores the role of migratory bird species in spreading Hyalomma ticks across the Northern Hemisphere and highlights their potential as an early warning system for CCHF outbreaks. This study demonstrates the need to integrate migratory birds into CCHF surveillance systems as sentinels of Hyalomma tick dispersal, providing a reference framework for monitoring tick-borne risks along avian migration routes.