Eco-epidemiology of Rickettsia amblyommatis and Rickettsia parkeri in naturally infected ticks (Acari: Ixodida) from South Carolina

Background Spotted fever group Rickettsia (SFGR) is the largest group of Rickettsia species of clinical and veterinary importance emerging worldwide. Historically, SFGR cases were linked to Rickettsia rickettsii, the causal agent of Rocky Mountain spotted fever; however, recently discovered species Rickettsia parkeri and Rickettsia amblyommatis have been shown to cause a wide range of clinical symptoms. The role of R. amblyommatis in SFGR eco-epidemiology and the possible public health implications remain unknown. Methods This study evaluated statewide tick surveillance and land-use classification data to define the eco-epidemiological relationships between R. amblyommatis and R. parkeri among questing and feeding ticks collected across South Carolina between 2021 and 2022. Questing ticks from state parks and feeding ticks from animal shelters were evaluated for R. parkeri and R. amblyommatis using reverse transcriptase quantitative polymerase chain reaction (RT-qPCR) on pooled samples. A Bayesian multivariable logistic regression model for pool testing data was used to assess associations between R. parkeri or R. amblyommatis infection and land-use classification variables among questing ticks. The Spearman correlation was used to evaluate the relationship between the two tested pathogens. Results The infection prevalence for R. amblyommatis was 24.8% (23.4-26.3%) among questing ticks, and 39.5% (37.4-42.0%) among feeding ticks; conversely, for R. parkeri it was 19.0% (17.6-20.5%) among questing ticks and 22.4% (20.3-24.5%) among feeding ticks. A negative, refractory correlation was found between the species, with ticks significantly more likely to contain one or the other pathogen, but not both simultaneously. The Bayesian analysis revealed that R. amblyommatis infection was positively associated with deciduous, evergreen, and mixed forests, and negatively associated with hay and pasture fields, and emergent herbaceous wetlands. Rickettsia parkeri infection was positively associated with deciduous, mixed, and evergreen forests, herbaceous vegetation, cultivated cropland, woody wetlands, and emergent herbaceous wetlands, and negatively associated with hay and pasture fields. Conclusions This is the first study to evaluate the eco-epidemiological factors driving tick pathogenicity in South Carolina. The negative interactions between SFGR species suggest the possible inhibition between the two pathogens tested, which could have important public health implications. Moreover, land-use classification factors revealed environments associated with tick pathogenicity, highlighting the need for tick vector control in these areas.