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Ecology, biology and distribution of spotted-fever tick vectors in Brazil

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      Abstract

      Spotted-fever-caused Rickettsia rickettsii infection is in Brazil the major tick-borne zoonotic disease. Recently, a second and milder human rickettsiosis caused by an agent genetically related to R. parkeri was discovered in the country (Atlantic rainforest strain). Both diseases clearly have an ecological background linked to a few tick species and their environment. Capybaras ( Hydrochoerus hydrochaeris) and Amblyomma cajennense ticks in urban and rural areas close to water sources are the main and long-known epidemiological feature behind R. rickettsii-caused spotted-fever. Unfortunately, this ecological background seems to be increasing in the country and disease spreading may be foreseen. Metropolitan area of São Paulo, the most populous of the country, is embedded in Atlantic rainforest that harbors another important R. rickettsii vector, the tick Amblyomma aureolatum. Thus, at the city–forest interface, dogs carry infected ticks to human dwellings and human infection occurs. A role for R. rickettsii vectoring to humans of a third tick species, Rhipicephalus sanguineus in Brazil, has not been proven; however, there is circumstantial evidence for that. A R. parkeri-like strain was found in A. ovale ticks from Atlantic rainforest and was shown to be responsible for a milder febrile human disease. Rickettsia-infected A. ovale ticks are known to be spread over large areas along the Atlantic coast of the country, and diagnosis of human infection is increasing with awareness and proper diagnostic tools. In this review, ecological features of the tick species mentioned, and that are important for Rickettsia transmission to humans, are updated and discussed. Specific knowledge gaps in the epidemiology of such diseases are highlighted to guide forthcoming research.

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      Ecology of rickettsia in South America.

      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 < or =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.
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        Ticks (Ixodidae) on humans in South America.

        Twenty eight species of Ixodidae have been found on man in South America (21 Amblyomma, 1 Boophilus, 2 Dermacentor, 2 Haemaphysalis, 1 Ixodes and 1 Rhipicephalus species). Most of them are rarely found on man. However, three species frequently parasitize humans in restricted areas of Argentina (A. neumanni reported from 46 localities), Uruguay (A. triste from 21 sites) and Argentina-Brazil (A. parvum from 27 localities). The most widespread ticks are A. cajennense (134 localities in Argentina, Bolivia, Brazil, Colombia, Ecuador, French Guiana, Guyana, Paraguay, Suriname and Venezuela), A. ovale (37 localities in Argentina, Brazil, Ecuador, French Guiana, Guyana, Paraguay, Suriname and Venezuela) and A. oblongoguttatum (28 sites in Brazil, Colombia, French Guiana, Guyana, Suriname and Venezuela). Amblyomma aureolatum (18 localities in Argentina, Brazil, French Guiana and Paraguay), A. cajennense, and A. triste are vectors of rickettsioses to man in South America. A better understanding of the respective roles of these and other tick species in transmitting pathogens to humans will require further local investigations. Amblyomma ticks should be the main subjects of these studies followed by species of Boophilus, Dermacentor, Haemaphysalis and Rhipicephalus species. In contrast with North America, Europe and Asia, ticks of the genus Ixodes do not appear to be major players in transmitting diseases to human. Indeed, there is only one record of an Ixodes collected while feeding on man for all South America.
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          Rocky Mountain spotted fever from an unexpected tick vector in Arizona.

          Rocky Mountain spotted fever is a life-threatening, tick-borne disease caused by Rickettsia rickettsii. This disease is rarely reported in Arizona, and the principal vectors, Dermacentor species ticks, are uncommon in the state. From 2002 through 2004, a focus of Rocky Mountain spotted fever was investigated in rural eastern Arizona. We obtained blood and tissue specimens from patients with suspected Rocky Mountain spotted fever and ticks from patients' homesites. Serologic, molecular, immunohistochemical, and culture assays were performed to identify the causative agent. On the basis of specific laboratory criteria, patients were classified as having confirmed or probable Rocky Mountain spotted fever infection. A total of 16 patients with Rocky Mountain spotted fever infection (11 with confirmed and 5 with probable infection) were identified. Of these patients, 13 (81 percent) were children 12 years of age or younger, 15 (94 percent) were hospitalized, and 2 (12 percent) died. Dense populations of Rhipicephalus sanguineus ticks were found on dogs and in the yards of patients' homesites. All patients with confirmed Rocky Mountain spotted fever had contact with tick-infested dogs, and four had a reported history of tick bite preceding the illness. R. rickettsii DNA was detected in nonengorged R. sanguineus ticks collected at one home, and R. rickettsii isolates were cultured from these ticks. This investigation documents the presence of Rocky Mountain spotted fever in eastern Arizona, with common brown dog ticks (R. sanguineus) implicated as a vector of R. rickettsii. The broad distribution of this common tick raises concern about its potential to transmit R. rickettsii in other settings. Copyright 2005 Massachusetts Medical Society.
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            Author and article information

            Affiliations
            1Laboratório de Ixodologia, Faculdade de Medicina Veterinária, Universidade Federal de Uberlândia Uberlândia, Brazil
            2Núcleo de Estudos de Doenças Transmitidas por Carrapatos, Superintendência de Controle de Endemias São Paulo, Brazil
            3Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo São Paulo, Brazil
            Author notes

            Edited by: Agustín Estrada-Peña, University of Zaragoza, Spain

            Reviewed by: Jose De La Fuente, Instituto de Investigacion en Recursos Cinegeticos, Spain; Angel Sainz, Universidad Complutense de Madrid, Spain

            *Correspondence: Matias P. J. Szabó, Laboratório de Ixodologia, Faculdade de Medicina Veterinária, Universidade Federal de Uberlândia, Av. Pará, 1720/Campus Umuarama-Bloco 2T, 38400-902 Uberlândia, Brazil e-mail: szabo@ 123456famev.ufu.br
            Journal
            Front Cell Infect Microbiol
            Front Cell Infect Microbiol
            Front. Cell. Infect. Microbiol.
            Frontiers in Cellular and Infection Microbiology
            Frontiers Media S.A.
            2235-2988
            12 July 2013
            2013
            : 3
            23875178 3709097 10.3389/fcimb.2013.00027
            Copyright © 2013 Szabó, Pinter and Labruna.

            This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.

            Counts
            Figures: 3, Tables: 0, Equations: 0, References: 82, Pages: 9, Words: 8173
            Categories
            Microbiology
            Review Article

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