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

ABSTRACT: Brazilian spotted fever (BSF), caused by Rickettsia rickettsii, is the most lethal tick-borne disease in the western hemisphere. In Brazil, Amblyomma sculptum ticks are the main vector. Capybaras (Hydrochoerus hydrochaeris), the largest living rodents of the world (adults weighing up to 100 Kg), have been recognized as amplifying hosts of R. rickettsii for A. sculptum in BSF-endemic areas; i.e., once primarily infected, capybaras develop bacteremia for a few days, when feeding ticks acquire rickettsial infection. We conducted experimental infections of five capybaras with an A. sculptum-derived strain of R. rickettsii and performed clinical and bacteremia evaluation during primary and subsequent infections. Bacteremia was detected in all capybaras during primary infection, but not in subsequent infections. All animals seroconverted to R. rickettsii (titres range: 64-32,768), and remained seropositive throughout the study. Primary infection resulted in clinical spotted fever illness in four capybaras, of which two had a fatal outcome. Subsequent infections in seropositive capybaras resulted in no clinical signs. Capybaras developed a sustained immune response that prevented a second bacteremia. This condition may imply a high reproduction rate of capybaras in BSF-endemic areas, in order to continuously generate capybaras susceptible to bacteremia during primary infection.

SUBMITTER: Ramirez-Hernandez A

PROVIDER: S-EPMC6976648 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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

Ramírez-Hernández Alejandro A Uchoa Francisco F de Azevedo Serpa Maria Carolina MC Binder Lina C LC Rodrigues Alessandra Castro AC Szabó Matias P J MPJ Fogaça Andrea A Souza Celso Eduardo CE Labruna Marcelo B MB

Scientific reports 20200122 1

Brazilian spotted fever (BSF), caused by Rickettsia rickettsii, is the most lethal tick-borne disease in the western hemisphere. In Brazil, Amblyomma sculptum ticks are the main vector. Capybaras (Hydrochoerus hydrochaeris), the largest living rodents of the world (adults weighing up to 100 Kg), have been recognized as amplifying hosts of R. rickettsii for A. sculptum in BSF-endemic areas; i.e., once primarily infected, capybaras develop bacteremia for a few days, when feeding ticks acquire rick ...[more]

PMID: 31969607

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Project description:BackgroundBrazilian spotted fever (BSF), caused by the bacterium Rickettsia rickettsii, is the deadliest spotted fever of the world. In most of the BSF-endemic areas, capybaras (Hydrochoerus hydrochaeris) are the principal host for the tick Amblyomma cajennense, which is the main vector of BSF.MethodsIn 2012, a BSF case was confirmed in a child that was bitten by ticks in a residential park area inhabited by A. cajennense-infested capybaras in Itú municipality, southeastern Brazil. Host questing A. cajennense adult ticks were collected in the residential park and brought alive to the laboratory, where they were macerated and intraperitoneally inoculated into guinea pigs. A tick-inoculated guinea pig that presented high fever was euthanized and its internal organs were macerated and inoculated into additional guinea pigs (guinea pig passage). Tissue samples from guinea pig passages were also used to inoculate Vero cells through the shell vial technique. Infected cells were used for molecular characterization of the rickettsial isolate through PCR and DNA sequencing of fragments of three rickettsial genes (gltA, ompA, and ompB). Blood serum samples were collected from 172 capybaras that inhabited the residential park. Sera were tested through the immunofluorescence assay using R. rickettsii antigen.ResultsA tick-inoculated guinea pig presented high fever accompanied by scrotal reactions (edema and marked redness). These signs were reproduced by consecutive guinea pig passages. Rickettsia was successfully isolated in Vero cells that were inoculated with brain homogenate derived from a 3rd passage-febrile guinea pig. Molecular characterization of this rickettsial isolate (designated as strain ITU) yielded DNA sequences that were all 100% identical to corresponding sequences of R. rickettsii in Genbank. A total of 83 (48.3%) out of 172 capybaras were seroreactive to R. rickettsii, with endpoint titers ranging from 64 to 8192.ConclusionsA viable isolate of R. rickettsii was obtained from the tick A. cajennense, comprising the first viable R. rickettsi isolate from this tick species during the last 60 years. Nearly half of the capybara population of the residential park was seroreactive to R. rickettsii, corroborating the findings that the local A. cajennense population was infected by R. rickettsii.

Project description: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.

Dataset Information

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

Publications

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

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