Tissue-specific localization of tick-borne pathogens in ticks collected from camels in Kenya: insights into vector competence

Front Cell Infect Microbiol. 2024 Apr 18:14:1382228. doi: 10.3389/fcimb.2024.1382228. eCollection 2024.

Abstract

Background: Tick-borne pathogen (TBP) surveillance studies often use whole-tick homogenates when inferring tick-pathogen associations. However, localized TBP infections within tick tissues (saliva, hemolymph, salivary glands, and midgut) can inform pathogen transmission mechanisms and are key to disentangling pathogen detection from vector competence.

Methods: We screened 278 camel blood samples and 504 tick tissue samples derived from 126 camel ticks sampled in two Kenyan counties (Laikipia and Marsabit) for Anaplasma, Ehrlichia, Coxiella, Rickettsia, Theileria, and Babesia by PCR-HRM analysis.

Results: Candidatus Anaplasma camelii infections were common in camels (91%), but absent in all samples from Rhipicephalus pulchellus, Amblyomma gemma, Hyalomma dromedarii, and Hyalomma rufipes ticks. We detected Ehrlichia ruminantium in all tissues of the four tick species, but Rickettsia aeschlimannii was only found in Hy. rufipes (all tissues). Rickettsia africae was highest in Am. gemma (62.5%), mainly in the hemolymph (45%) and less frequently in the midgut (27.5%) and lowest in Rh. pulchellus (29.4%), where midgut and hemolymph detection rates were 17.6% and 11.8%, respectively. Similarly, in Hy. dromedarii, R. africae was mainly detected in the midgut (41.7%) but was absent in the hemolymph. Rickettsia africae was not detected in Hy. rufipes. No Coxiella, Theileria, or Babesia spp. were detected in this study.

Conclusions: The tissue-specific localization of R. africae, found mainly in the hemolymph of Am. gemma, is congruent with the role of this tick species as its transmission vector. Thus, occurrence of TBPs in the hemolymph could serve as a predictor of vector competence of TBP transmission, especially in comparison to detection rates in the midgut, from which they must cross tissue barriers to effectively replicate and disseminate across tick tissues. Further 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.

Keywords: Amblyomma gemma; Ehrlichia; Hyalomma dromedarii; Hyalomma rufipes; Rhipicephalus pulchellus; Rickettsia; dromedary camels; tick tissues.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anaplasma / genetics
  • Anaplasma / isolation & purification
  • Animals
  • Babesia* / genetics
  • Babesia* / isolation & purification
  • Camelus* / microbiology
  • Camelus* / parasitology
  • Coxiella / genetics
  • Coxiella / isolation & purification
  • Ehrlichia* / genetics
  • Ehrlichia* / isolation & purification
  • Hemolymph / microbiology
  • Hemolymph / parasitology
  • Kenya / epidemiology
  • Rickettsia / genetics
  • Rickettsia / isolation & purification
  • Salivary Glands / microbiology
  • Salivary Glands / parasitology
  • Theileria* / genetics
  • Theileria* / isolation & purification
  • Tick-Borne Diseases / epidemiology
  • Tick-Borne Diseases / microbiology
  • Tick-Borne Diseases / parasitology
  • Ticks* / microbiology
  • Ticks* / parasitology

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program under grant agreement No 101000365 (PREPARE4VBD), and icipe institutional funding from the Swedish International Development Cooperation Agency (Sida), the Swiss Agency for Development and Cooperation (SDC), the Australian Centre for International Agricultural Research (ACIAR), the Norwegian Agency for Development Cooperation (Norad), the Federal Democratic Republic of Ethiopia, and the Government of the Republic of Kenya. RK was supported by a German Academic Exchange Service (DAAD) through the icipe ARPPIS-DAAD scholarship and through a UP post-graduate bursary. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.