Role of reptiles and associated arthropods in the epidemiology of rickettsioses: A one health paradigm

Abstract

We assessed the presence of Rickettsia spp., Coxiella burnetii and Anaplasma phagocytophilum in reptiles, their ectoparasites and in questing ticks collected in a nature preserve park in southern Italy, as well as in a peri-urban area in another region. We also investigated the exposure to these pathogens in forestry workers, farmers and livestock breeders living or working in the nature preserve park given the report of anecdotal cases of spotted fever rickettsioses. Rickettsia spp. were molecularly detected in Podarcis muralis and Podarcis siculus lizards (i.e., 3.1%), in Ixodes ricinus (up to 87.5%) and in Neotrombicula autumnalis (up to 8.3%) collected from them as well as in I. ricinus collected from the environment (up to 28.4%). Rickettsia monacensis was the most prevalent species followed by Rickettsia helvetica. An undescribed member of the family Anaplasmataceae was detected in 2.4% and 0.8% of the reptiles and ectoparasites, respectively. Sera from human subjects (n = 50) were serologically screened and antibodies to Rickettsia spp. (n = 4; 8%), C. burnetti (n = 8; 16%) and A. phagocytophilum (n = 11; 22%) were detected. Two ticks collected from two forestry workers were positive for spotted fever group (SFG) rickettsiae. Ixodes ricinus is involved in the transmission of SFG rickettsiae (R. monacensis and R. helvetica) in southern Europe and lizards could play a role in the sylvatic cycle of R. monacensis, as amplifying hosts. Meanwhile, N. autumnalis could be involved in the enzootic cycle of some SFG rickettsiae among these animals. People living or working in the southern Italian nature preserve park investigated are exposed to SFG rickettsiae, C. burnetii and A. phagocytophilum. Zoonotic pathogens such as Rickettsia spp., Coxiella burnetii and Anaplasma phagocytophilum are associated with ticks, lice, fleas and mites and may infect a wide range of vertebrate species. There are still many knowledge gaps concerning the arthropod vectors and amplifying hosts of these pathogens. Reptiles are known to host infected ticks with these zoonotic pathogens and eventually become infected themselves by these bacteria. Hence to address this question from a broad One-Health perspective, we assessed the molecular prevalence of Rickettsia spp., C. burnetii and A. phagocytophilum in reptiles, ticks and mites from both hosts and environment and seroprevalence in humans living or working near the same area. Rickettsia DNA was detected in lizards’ tails, Ixodes ricinus ticks and in Neotrombicula autumnalis mites collected from them and in questing ticks. Although DNA of C. burnetii and A. phagocytophilum was not detected in lizards and their ectoparasites, sera samples of human subjects tested positive for the antibodies against these zoonotic pathogens. These findings indicate the epidemiological role of lizards in spreading SFG rickettsiae as well as I. ricinus, and hence representing a potential public health concern in geographical areas where lizards, ticks and humans share the same environment.