Tick-borne pathogen distribution in tick tissues collected from dromedary camels in Kenya: Predicting vector competence

Abstract

Surveillance studies on tick-borne pathogens (TBPs) frequently use whole-tick homogenates to understand associations between ticks and pathogens. However, understanding the distribution of TBP infection within specific tick tissues (saliva, hemolymph, salivary glands, and midgut) can help unravel pathogen transmission mechanisms and disentangle pathogen detection from vector competence. We screened for Anaplasma, Ehrilichia, Coxiella, Rickettsia, Theileria, and Babesia pathogens by PCR-HRM analysis of 278 camel blood samples and 504 tick tissues derived from 126 camel ticks sampled in Kenya (Laikipia and Marsabit counties). Candidatus Anaplasma camelii infections were prevalent in camels (91%) yet absent in all ticks (Rhipicephalus pullchelus, Amblyomma gemma, Hyalomma dromedarii and Hyalomma rufipes). We detected Ehrlichia chaffeensis, responsible for human monocytic ehrlichiosis, for the first time in the blood of one camel. Ehrlichia ruminantium was detected in all tissues of the four tick species. Rickettsia africae exhibited the highest prevalence in Am. gemma (62.5%), primarily in the hemolymph (45%) and less frequently in the midgut (27.5%). Conversely, the lowest occurrence of R. africae was observed in Rh. pulchellus (29.4%) midgut (17.6%) and hemolymph (11.8%). Similarly, R. africae was predominantly detected in the midgut of Hyalomma dromedarii (41.7%), but was absent in the hemolymph. Rickettsia aeschlimannii was found only in Hy. rufipes, mainly in the hemolymph (80%), which is congruent with the role of this tick species as its transmission vector. Our findings suggest that presence of TBPs in tick hemolymph may serve as an indicator of vector competence, particularly in comparison to detection in the midgut from which they must cross tissue barriers for effective replication and dissemination across tick tissues. Studies should focus on exploring the distribution of TBPs within tick tissues to enhance knowledge of TBP epidemiology and to distinguish competent vectors from dead-end hosts.