Molecular assessment of Theileria equi and Babesia caballi prevalence in horses and ticks on horses in southeastern France

Abstract

Equine piroplasmosis (EP) is a tick-borne disease caused by Babesia caballi and Theileria equi that is potentially emerging in non-endemic countries. We conducted a descriptive study to investigate EP prevalence and spatial distribution in an endemic region: the Camargue and the Plain of La Crau in France. In spring 2015 and 2016, we carried out sampling at stables (total n = 46) with a history of horses presenting chronic fever or weight loss. Overall, we collected blood from 632 horses, which were also inspected for ticks; these horses had been housed in the target stables for at least 1 year. We obtained 585 ticks from these horses and described land use around the stables. Real-time PCR was employed to assess T. equi and B. caballi prevalence in the horses and in the ticks found on the horses. For the horses, T. equi and B. caballi prevalence was 68.6% and 6.3%, respectively. For the ticks found on the horses, prevalence was 28.8% for T. equi and 0.85% for B. caballi. The most common tick species were, in order of frequency, Rhipicephalus bursa, R. sanguineus sl., Hyalomma marginatum, Haemaphysalis punctata, and Dermacentor sp. Horses bearing Rhipicephalus ticks occurred in wetter zones, closer to agricultural areas, permanent crops, and ditches, as well as in drier zones, in the more northern countryside. Compared to horses bearing R. bursa, horses bearing R. sanguineus sl. more frequently occurred near the Rhone River. Prevalence of T. equi in the ticks was as follows: Hyalomma marginatum (43%), Dermacentor sp. (40%), R. bursa (33%), R. sanguineus sl. (19%), and Haemaphysalis punctata (17%). In contrast, B. caballi only occurred in Dermacentor sp. (20%) and R. bursa (1%).

Tick-borne pathogens identified inHyalomma marginatum(Acari: Ixodidae) collected from various vertebrate hosts in the South of France

“…This is not the first time that this apicomplexan parasite has been identified in H. marginatum in France, as 43% of ticks collected previously on horses in Camargue were found positive in 2022 (Rocafort-Ferrer et al 2022). EP is known to be widely distributed in France, particularly in the South (Rocafort-Ferrer et al 2022). If the majority of horses on which ticks engorged were positive and ticks could be infected via the blood meal, then they would have been almost all positive.…”

“…Although equine piroplasmosis is commonly reported in horses from the South of France (Rocafort-Ferrer et al 2022) and ticks were mainly collected on horses, T. equi was detected in a very small number of ticks, 17 individual ticks from mainland France and 9 pools from Corsica, and no B. caballi was detected in the analyzed ticks. However, B. occultans was detected in nine individual ticks collected on cattle from Corsica.…”

“…aechlimannii and finally viruses such as Thogoto, Dhori and Bhanja viruses (RNA for these viruses has already been detected in ticks), in addition to CCHFV. We then identified microorganisms from scientific literature that mentioned the detection of pathogens in H. marginatum , which could be transmitted by this tick or just reflect the infectious status of the animal host on which the tick was collected, as shown in Corsica or other regions of the world: A. phagocytophilum, A. marginale (Grech-Angelini et al 2020), E. minasensis (Vincent Cicculli et al 2019), T. equi (Rocafort-Ferrer et al 2022) , the West Nile Virus (Formosinho et Santos-Silva 2006; Kolodziejek et al 2014) , the symbiotic form of Coxiella burnetii and Francisella tularensis : Coxiella -like endosymbiont CLE and Francisella -like endosymbiont FLE (Kilicoglu et al 2020; Selmi et al 2019; Buysse et al 2021; Demir et al 2020) . Then, some pathogens known to be transmitted by ticks of the genus Hyalomma but not necessarily H. marginatum , or even by other tick genera but with a likelihood to replicate in Hyalomma ticks, were also added to the chip: Alkhurma virus transmitted by H. rufipes (Horton et al 2016; Hoffman et al 2018) , as well as Nairobi sheep disease and Hazara viruses that are genetically close to CCHFV (Garrison et al ., 2020, Borrelia miyamotoi and Bartonella henselae that circulate in France in other tick species or even other arthropoda such as fleas (Cosson et al 2014; Grech-Angelini et al 2020) .…”

Systematic Review on Crimean–Congo Hemorrhagic Fever Enzootic Cycle and Factors Favoring Virus Transmission: Special Focus on France, an Apparently Free-Disease Area in Europe

“…Regarding Rh. bursa , Gargili et al ( 8 ) suggested that its bioecology could be favorable for CCHFV transmission but in absence of the relevant virological evidence, we did not consider this species as a suitable vector, despite its abundance in the South of France ( 17 , 41 , 54 ).…”

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

“…Quantitative PCR Tick samples were also screened for the detection and quantification of T. equi and R. aeschlimannii using a second detection method by qPCR with primers and probes targeting different genes to those used in the BioMark TM assay (Table 2) (Kim et al 2008;Rocafort-Ferrer et al 2022). There are five known genotypes for T. equi (designated A-E) circulating in Europe, so we wanted to be sure that we could detect all of those five genotypes if present (Nagore et al 2004;Bhoora et al 2009;Salim et al 2010;Qablan et al 2013).…”