Comparative Susceptibility of Different Populations of Amblyomma sculptum to Rickettsia rickettsii

Abstract

The bacterium Rickettsia rickettsii is the etiological agent of Brazilian spotted fever (BSF), which is transmitted in Brazil mainly by the tick Amblyomma sculptum. Herein, larvae and nymphs of six populations of A. sculptum were exposed to R. rickettsii by feeding on needle-inoculated guinea pigs, and thereafter reared on uninfected guinea pigs or rabbits. Two tick populations were exposed to autochthone R. rickettsii strains, whereas four tick populations were exposed to non-autochthone strains. The six geographically different populations of A. sculptum showed different susceptibilities to R. rickettsii , higher among the two tick populations that were exposed to their autochthone R. rickettsii strain. In addition, higher rates of transovarial transmission of R. rickettsii and vector competence success also included the two tick populations that were exposed to autochthone R. rickettsii strains. These results indicate that the susceptibility of A. sculptum to R. rickettsii varies among different tick populations, with a clear bias for higher susceptibility to an autochthone R. rickettsii strain that has already coevolved with a tick population for some time. Our results demonstrated that the R. rickettsii infection induces higher mortality of engorged larvae and nymphs, and tend to reduce the reproductive fitness of engorged females. All together, these results might explain the low R. rickettsii- infection rates of A. sculptum under natural conditions (usually <1%), and indicate that an A. sculptum population should not be able to sustain a R. rickettsii infection for successive tick generations without the creation of new cohorts of infected ticks via horizontal transmission on vertebrate rickettsemic hosts (amplifying hosts). Finally, despite of the ubiquitous distribution of A. sculptum in southeastern and central-western Brazil, most of the populations of this tick species are devoid of R. rickettsii infection. This scenario might be related to two major factors: (i) insufficient numbers of susceptible amplifying hosts; and (ii) lower susceptibilities of many tick populations. While the first factor has been demonstrated by mathematical models in previous studies, the second is highlighted by the results observed in the present study.

Clinical and serological evaluation of capybaras (Hydrochoerus hydrochaeris) successively exposed to an Amblyomma sculptum-derived strain of Rickettsia rickettsii

“…In addition, our tick colony of A. sculptum was also derived from this same BSF-endemic area. Indeed, this information supports strong field applicability of our results, especially because it was recently demonstrated that the susceptibility of A. sculptum to R. rickettsii varies among different tick populations, with a clear bias for higher susceptibility to an autochthone R. rickettsii strain that has already coevolved with a tick population for some time 8 .…”

“…Regardless, it must be emphasized that techniques employing the direct detection of rickettsial DNA in bloodstream are not sensitive enough to determine bacteremic periods, especially in less severe infection courses. www.nature.com/scientificreports www.nature.com/scientificreports/ Rickettsia DNA amplification was achieved in skin samples from all capybaras during primary infection (6-26 DPI), which is similar with those results registered by Levin et al 34 in skin biopsies from R. rickettsii-infected guinea pigs (3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22). It is remarkable that in some capybaras (no.…”

“…These adult ticks derived from the fifth generation (F 5 ) of a tick colony that was established in the laboratory from a population adapted to capybaras, collected in Itu municipality (São Paulo) in 2012 16 . These adult ticks were previously exposed to rickettsial infection as larvae and nymphs through feeding on guinea pigs in bacteremia that were intraperitoneally inoculated with R. rickettsii strain Itu, as described 8 . This rickettsial strain was isolated from A. sculptum ticks collected in the same area of origin of the progenitor ticks that generated our tick colony 16 .…”

“…Serology: Indirect immunofluorescence assay (IFA). Sera obtained from capybaras, guinea pigs and rabbits were tested by IFA using R. rickettsii (strain Taiaçu) crude antigen and fluorescein isothiocyanate-labelled sheep anti-capybara IgG (CCZ, São Paulo, SP, Brazil), goat anti-rabbit IgG (Sigma, St. Louis, MO, USA) and rabbit anti-guinea pig IgG (Sigma), respectively, as previously described 7,8,14 . Samples were initially tested in a 1:64 dilution (with PBS) as cut-off and those reactive, further diluted in twofold increments to the endpoint titre, as reported earlier 20 .…”

“…www.nature.com/scientificreports www.nature.com/scientificreports/ Ticks function as the main reservoirs of R. rickettsii in nature, nonetheless, due to bacterial pathogenic effects on ticks 5,6 and some degree of tick refractoriness to bacterial infection 7,8 , low natural infectious rates (<1%) are commonly found in endemic areas. Therefore, amplifying hosts (vertebrate animals developing bacteremia for some days) are essential in maintaining the pathogen by its transmission to non-infected ticks and creating new cohorts of infected ticks within the population 3,9 .…”