Roles of tick-cofeeding hedgehogs in the natural transmission of spotted fever group Rickettsia

Tick-borne spotted fever group Rickettsia (SFGR) poses a significant threat to public health worldwide. The cofeeding behavior of ticks attaching host animals, such as hedgehogs, has been identified as a potential mechanism for transmitting SFGR between infected and uninfected ticks, potentially increasing the prevalence of SFGR. However, the overall positive rate of SFGR in free-living ticks remains relatively low, suggesting that the role of tick-cofeeding in amplifying SFGR prevalence may not be as substantial as previously believed. To explore the impact of tick-cofeeding hedgehogs on the natural transmission of SFGR, to clarify the underlying hypotheses, and to provide robust data to support targeted prevention and control strategies for spotted fever, this study developed a transmission model using tick-cofeeding hedgehogs that simulates the natural transmission process. Both Rickettsia-infected and uninfected tick populations were established and used for cofeeding on mice or hedgehogs. Among formerly uninfected nymphs that cofed on mice, 75.61% acquired Rickettsia after engorgement, but this infection rate dropped sharply to 9.68% after molting. In contrast, formerly uninfected adults that cofed on hedgehogs showed a 100% infection rate after engorgement. However, the infection rates declined significantly in their offspring, with only 11.12% of normal-hatching eggs and 3.12% of larvae testing positive. Additionally, we observed mortality in infected engorged adults and their eggs. Our results demonstrate that while tick-cofeeding on hedgehogs can lead to a high positive rate of Rickettsia in ticks, the infections acquired through cofeeding fail to sustain this high positivity rate due to several mechanisms. Firstly, rickettsiae obtained through cofeeding or blood meals do not consistently establish infections in all recipient ticks, resulting in a significant decline in positive rates as ticks progress to subsequent developmental stages. Secondly, adult ticks infected via cofeeding tend to reduce the infection rate in their offspring through various mechanisms, including tick mortality caused by rickettsiae, egg hatching failure, and a low transovarial transmission rate. Additionally, in natural settings, infections from other pathogens may similarly contribute to tick mortality and reduced egg hatching. This study elucidates why rickettsiae maintain a low prevalence in nature and evaluates the actual effects of tick-cofeeding on pathogen distribution among ticks. While tick-cofeeding on host animals have been considered important amplifiers of SFGR prevalence, our findings indicate that their impact is not as significant as previously assumed.