Ecology of Rickettsia in South America Labruna, Marcelo B.
Annals of the New York Academy of Sciences,
20/May , Letnik:
1166, Številka:
1
Journal Article
Recenzirano
Until the year 2000, only three Rickettsia species were known in South America: (i) Rickettsia rickettsii, transmitted by the ticks Amblyomma cajennense, and Amblyomma aureolatum, reported in ...Colombia, Argentina, and Brazil, where it is the etiological agent of Rocky Mountain spotted fever; (ii) Rickettsia prowazekii, transmitted by body lice and causing epidemic typhus in highland areas, mainly in Peru; (iii) Rickettsia typhi, transmitted by fleas and causing endemic typhus in many countries. During this new century, at least seven other rickettsiae were reported in South America: Rickettsia felis infecting fleas and the tick‐associated agents Rickettsia parkeri, Rickettsia massiliae, Candidatus“Rickettsia amblyommii,”Rickettsia bellii, Rickettsia rhipicephali, and Candidatus“Rickettsia andeanae.” Among these other rickettsiae, only R. felis, R. parkeri, and R. massiliae are currently recognized as human pathogens. R. rickettsii is a rare agent in nature, infecting ≤1% individuals in a few tick populations. Contrastingly, R. parkeri, Candidatus“R. amblyommii,” R. rhipicephali, and R. bellii are usually found infecting 10 to 100% individuals in different tick populations. Despite rickettsiae being transmitted transovarially through tick generations, low infection rates for R. rickettsii are possibly related to pathogenic effect of R. rickettsii for ticks, as shown for A. aureolatum under laboratory conditions. This scenario implies that R. rickettsii needs amplifier vertebrate hosts for its perpetuation in nature, in order to create new lines of infected ticks (horizontal transmission). In Brazil, capybaras and opossums are the most probable amplifier hosts for R. rickettsii, among A. cajennense ticks, and small rodents for A. aureolatum.
This study compared the vector competence of four populations of Rhipicephalus sanguineus group ticks for the bacterium Ehrlichia canis, the agent of canine monocytic ehrlichiosis (CME). Ticks ...(larvae and nymphs) from the four populations-one from São Paulo state, southeastern Brazil (BSP), one from Rio Grande do Sul state, southern Brazil (BRS), one from Argentina (ARG), and one from Uruguay (URU)-were exposed to E. canis infection by feeding on dogs that were experimentally infected with E. canis. Engorged ticks (larvae and nymphs) were allowed to molt to nymphs and adults, respectively, which were tested by molecular analysis (E. canis-specific PCR assay) and used to infest naïve dogs. Through infestation of adult ticks on naïve dogs, after nymphal acquisition feeding on E. canis-infected dogs, only the BSP population was shown to be competent vectors of E. canis, i.e., only the dogs infested with BSP adult ticks developed clinical illness, seroconverted to E. canis, and yielded E. canis DNA by PCR. This result, demonstrated by two independent replications, is congruent with epidemiological data, since BSP ticks were derived from São Paulo state, Brazil, where CME is highly endemic. On the other hand, BRS, ARG, and URU ticks were derived from a geographical region (South America southern cone) where CME has never been properly documented. Molecular analysis of unfed adults at 30 days post molting support these transmission results, since none of the BRS, ARG, and URU ticks were PCR positive, whereas 1% of the BSP nymphs and 31.8% of the BSP adults contained E. canis DNA. We conclude that the absence or scarcity of cases of CME due to E. canis in the South America southern cone is a result of vector incompetence of the R. sanguineus group ticks that prevail on dogs in this part of South America.
The tropical lineage within the Rhipicephalus sanguineus species complex is cause for growing concern in the U.S. based on its prominent role in creating and perpetuating multiple recently identified ...outbreaks of Rocky Mountain spotted fever in the southwestern United States and northern Mexico. This lineage is undergoing a northward range expansion in the United States, necessitating the need for enhanced surveillance for Rh. sanguineus. To inform more focused surveillance efforts we use species distribution models (SDMs) to predict current (2015-2019) and future (2021-2040) habitat for the tropical lineage. Models using the MaxEnt algorithm were informed using geolocations of ticks genetically confirmed to be of the tropical lineage, for which data on 23 climatic and ecological variables were extracted. Models predicted that suitability was optimal where temperatures are relatively warm and stable, and there is minimal precipitation. This translated into habitat being predicted along much of the coast of southern states including California, Texas, Louisiana, and Florida. Although the endophilic nature of tropical Rh. sanguineus somewhat violates the assumptions of SDMs, our models correctly predicted known locations of this tick and provide a starting point for increased surveillance efforts. Furthermore, we highlight the importance of using molecular methods to distinguish between ticks in the Rh. sanguineus species complex.
Brazilian Spotted Fever (BSF), caused by the bacterium Rickettsia rickettsii, is the tick-borne disease that generates the largest number of human deaths in the world. In Brazil, the current increase ...of BSF human cases has been associated with the presence and expansion of capybaras Hydrochoerus hydrochaeris, which act as primary hosts for the tick Amblyomma sculptum, vector of the R. rickettsii in this area.
We proposed a semi-discrete-time stochastic model to evaluate the role of capybaras in the transmission dynamics of R. rickettsii. Through a sensitivity analysis, we identified the parameters with significant influence on the R. rickettsii establishment. Afterward, we implemented the Gillespie's algorithm to simulate the impact of potential public health interventions to prevent BSF human cases.
The introduction of a single infected capybara with at least one infected attached tick is enough to trigger the disease in a non-endemic area. We found that to avoid the formation of new BSF-endemic areas, it is crucial to impede the emigration of capybaras from endemic areas by reducing their birth rate by more than 58%. Model results were corroborated by ex-situ data generated from field studies, and this supports our proposal to prevent BSF human cases by implementing control strategies focused on capybaras.
The proposed stochastic model illustrates how strategies for the control and prevention of vector-borne infectious diseases can be focused on amplifier hosts management practices. This work provides a basis for future prevention strategies for other neglected vector-borne diseases.
There are a huge number of pathogens with multi-component transmission cycles, involving amplifier hosts, vectors or complex pathogen life cycles. These complex systems present challenges in terms of ...modeling and policy development. A lethal tick-borne infectious disease, the Brazilian Spotted Fever (BSF), is a relevant example of that. The current increase of human cases of BSF has been associated with the presence and expansion of the capybara Hydrochoerus hydrochaeris, amplifier host for the agent Rickettsia rickettsii and primary host for the tick vector Amblyomma sculptum. We introduce a stochastic dynamical model that captures the spatial distribution of capybaras and ticks to gain a better understanding of the spatial spread of the R. rickettsii and potentially predict future epidemic outcomes. We implemented a reaction-diffusion process in which individuals were divided into classes denoting their state with respect to the disease. The model considered bidirectional movements between base and destination locations limited by the carrying capacity of the environment. We performed systematic stochastic simulations and numerical analysis of the model and investigate the impact of potential interventions to mitigate the spatial spread of the disease. The mobility of capybaras and their attached ticks was significantly influenced by the birth rate of capybaras and therefore, disease propagation velocity was higher in places with higher carrying capacity. Some geographical barriers, generated for example by riparian reforesting, can impede the spatial spread of BSF. The results of this work will allow the formulation of public actions focused on the prevention of BSF human cases.
•R0 calculation is crucial to design control interventions.•There is a low impact of larvae population in the maintenance of R. rickettsii.•Disease transmission between nymphs/adults and capybara is ...the major contributor to changes in the R0.•Brazilian Spotted Fever control strategies should focus on the nymphs and adult seasons.
Brazilian Spotted Fever (BSF) is an emerging and lethal disease in South America which basic reproduction number (R0) is unknown. Calculating R0 for this disease is crucial to design control interventions and prevent human deaths. BSF endemic areas are related to the presence of capybaras Hydrochoerus hydrochaeris, amplifier hosts of Rickettsia rickettsii and primary hosts of the tick Amblyomma sculptum, main vector of the agent in this area. Because of the complexity of its dynamics, we calculated R0 for the BSF system by constructing a next-generation matrix considering different categories of vectors and hosts. Each matrix element was considered as the expected number of infected individuals of one category produced by a single infected individual of a second category. We used field and experimental data to parameterize the next-generation matrix and obtain the final calculation (R0 ≈ 1.7). We demonstrated the low impact of the matrix elements corresponding to the transovarial transmission and the transmission from infected larvae in the maintenance of R. rickettsii. Sensitivity and elasticity analyzes were performed to quantify the perturbations of each matrix element in R0. We noted that the elements equivalent to the number of infected attached nymphs produced by an infected capybara, and the number of infected capybaras produced by an infected attached nymph or adult are the major contributors to changes in R0. Our results provide insights into the strategic design of preventive interventions in BSF endemic areas.
The brown dog tick, Rhipicephalus sanguineus sensu stricto, is a species with considerable public health and economic importance. However, the taxonomic status of this species is far from resolved. ...After more than 110 years of scientific work on R. sanguineus s.s., the situation is that there is no type, no solid description, nor is there a consensus about the range of morphological variability within the species. Recent findings based on laboratory crosses and molecular genetics strongly suggest that there are several entities grouped under the same name. Here we review the history of the taxon, and we point out the caveats behind any further work on this tick. The current taxonomic status of R. sanguineus s.s. thus lacks an informative original description, and is based on the existence of several morphological descriptions based on ticks originating from different populations, which show, in some cases, biological incompatibility and significant genetic divergence. We suggests that as a result it is not possible to assign the specific name R. sanguineus s.s. to any population. Further work is required based on the rules issued by the International Code of Zoological Nomenclature to clearly define the morphological range of the different populations.
This study was performed in Maranhão state, a transition area two Brazilian biomes, Amazon and Cerrado. During 2011-2013, 1,560 domestic dogs were sampled for collection of serum blood samples and ...ticks in eight counties (3 within the Amazon and 5 within the Cerrado). A total of 959 ticks were collected on 150 dogs (9.6%). Rhipicephalus sanguineus sensu lato (s.l.) was the most abundant tick (68% of all collected specimens), followed by Amblyomma cajennense sensu lato (s.l.) (12.9%), Amblyomma parvum (9.2%), and Amblyomma ovale (5.2%). Other less abundant species (<1%) were Amblyomma oblongoguttatum, Rhipicephalus microplus, Haemaphysalis juxtakochi, and Amblyomma rotundatum. Females of A. cajennense s.l. ticks were morphologically identified as A. cajennense sensu stricto (s.s.) or A. sculptum. Molecular analyses of 779 canine ticks revealed three Rickettsia species: Rickettsia amblyommatis in 1% (1/100) A. cajennense s.l., 'Candidatus Rickettsia andeanae' in 20.7% (12/58) A. parvum, Rickettsia bellii in 6.8% (3/44) A. ovale and 100% (1/1) A. rotundatum ticks. An additional collection of A. sculptum from horses in a Cerrado area, and A. cajennense s.s. from pigs in an Amazon area revealed R. amblyommatis infecting only the A. cajennense s.s. ticks. Serological analysis of the 1,560 canine blood samples revealed 12.6% canine seroreactivity to Rickettsia spp., with the highest specific seroreactivity rate (10.2%) for R. amblyommatis. Endpoint titers to R. amblyommatis were significantly higher than those for the other Rickettsia antigens, suggesting that most of the seroreactive dogs were exposed to R. amblyommatis-infected ticks. Highest canine seroreactivity rates per locality (13.1-30.8%) were found in Amazon biome, where A. cajennense s.s. predominated. Lowest seroreactivity rates (1.9-6.5%) were found in Cerrado localities that were further from the Amazon, where A. sculptum predominated. Multivariate analyses revealed that canine seroreactivity to Rickettsia spp. or R. amblyommatis was statistically associated with rural dogs, exposed to Amblyomma ticks.
Amblyomma aureolatum ticks are vectors of Rickettsia rickettsii, the etiologic agent of Rocky Mountain spotted fever in Brazil. Maintenance of R. rickettsii in nature depends on horizontal ...transmission along tick generations. Although such transmission is known to occur when uninfected and infected ticks feed simultaneously on susceptible animals (co-feeding systemic transmission), we investigated co-feeding nonsystemic transmission, which was based on R. rickettsii-infected and -uninfected A. aureolatum ticks feeding simultaneously on guinea pigs immune to R. rickettsii. Our acquisition and transmission infestations demonstrated that horizontal transmission of R. rickettsii by co-feeding ticks on immune hosts with no systemic infection did not occur when uninfected larvae fed distantly from infected nymphs but did occur in a few cases when uninfected larvae fed side-by-side with infected nymphs, suggesting that they shared the same feeding site. The co-feeding nonsystemic transmission type might have no epidemiologic importance for Rocky Mountain spotted fever.
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