Paper

Spatial patterns of Hyalomma marginatum-borne pathogens in the Occitanie region (France), a focus on the intriguing dynamics of Rickettsia aeschlimannii

Pollet, Thomas, Riggi, Camille, Vial, Laurence, Clemence Galon, Bru, David, Malandrin, Laurence, Bernard, Celia, Moutailler, Sara, Huber, Karine, Rakotoarivony, Ignace, Jourdan-Pineau, Helene, Charlotte Joly Kukla, Giupponi, Carla

2024

Overview

Hyalomma marginatum is an invasive tick species reported in regions bordering the Mediterranean Sea. It has recently become established in mainland France in 2016. H. marginatum hosts a diverse range of human and animal pathogens such as Rickettsia aeschlimannii, Theileria equi, Anaplasma phagocytophilum, Anaplasma marginale, Ehrlichia minasensis and West Nile virus. The objective of this study was to characterize the current spatial distribution of H. marginatum-borne pathogens in the region Occitanie, southern France and the influence of other factors (tick sex, engorgement status). A large-scale tick collection program was organized in the region Occitanie to answer these questions. A total of 510 ticks from 27 sites of four departments were analysed for pathogens presences and loads using both a high-throughput microfluidic real time PCR system and quantitative PCR. In the analysed ticks, we identified the tick-borne pathogens and their prevalence: Theileria equi (9.2%), Theileria orientalis (0.2%), Anaplasma phagocytophilum (1.6%), Anaplasma marginale (0.8%) and Rickettsia aeschlimannii (87.3%). Interestingly, we highlighted a spatial clustered distribution for the pathogen R. aeschlimannii between two geographically isolated areas with infection rates and bacterial loads significantly lower in Herault/Gard departments (infection rate 78.6% in average) compared to Aude/Pyrenees-Orientales (infection rate 92.3% in average). R. aeschlimannii infection rates varied from one site to another, ranging from 29% to 100%, highlighting the importance of the sampling effort to better characterize the circulation of pathogens. Such high infection rate (87.3% in average) and the effective maternal transmission of R. aeschlimannii suggest a role as a tick symbiont in H. marginatum. On the other hand, currently identified as a human pathogen, its pathogenic status in humans is questioned given the low number of human cases. Further studies are thus needed to understand both the status and the role of R. aeschlimannii in H. marginatum ticks.Competing Interest StatementThe authors have declared no competing interest.

• Publisher: Cold Spring Harbor Laboratory Press,Cold Spring Harbor Laboratory
• Subject: Anaplasma marginale / Anaplasma phagocytophilum / Arachnids / Engorgement / Hyalomma marginatum / Infections / Introduced species / Invasive species / Microbiology / Microfluidics / Pathogens / Rickettsia / Spatial distribution / Theileria equi / West Nile virus