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      Ticks and serosurvey of anti- Rickettsia spp. antibodies in wild boars ( Sus scrofa), hunting dogs and hunters of Brazil

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          Abstract

          Background

          Rickettsia bacteria are responsible for diseases in humans and animals around the world, however few details are available regarding its ecology and circulation among wild animals and human populations at high transmission risk in Brazil. The aim of this study was to investigate the occurrence of ticks and Rickettsia spp. in wild boars, corresponding hunting dogs and hunters.

          Methods

          Serum samples and ticks were collected from 80 free-range wild boars, 170 hunting dogs and 34 hunters from southern and central-western Brazil, from the Atlantic Forest and Cerrado biomes, respectively, between 2016 and 2018. Serum samples were tested by indirect immunofluorescent-antibody assay (IFA) to detect IgG antibodies against Rickettsia rickettsii, Rickettsia parkeri, Rickettsia bellii, Rickettsia rhipicephali and Rickettsia amblyommatis. Tick species were identified by morphological taxonomic keys, as previously described. A total of 164 ticks including A. sculptum, A. brasiliense and A. aureolatum were tested in PCR assays for Spotted Fever Group (SFG) Rickettsia spp.

          Results

          A total of 58/80 (72.5%) wild boars, 24/170 (14.1%) hunting dogs and 5/34 (14.7%) hunters were positive (titers ≥ 64) to at least one Rickettsia species. A total of 669/1,584 (42.2%) ticks from wild boars were identified as Amblyomma sculptum, 910/1,584 (57.4%) as Amblyomma brasiliense, 4/1,584(0.24%) larvae of Amblyomma spp. and 1/1,584 (0.06%) nymph as Amblyolmma dubitatum. All 9 ticks found on hunting dogs were identified as Amblyomma aureolatum and all 22 ticks on hunters as A. sculptum. No tested tick was positive by standard PCR to SFG Rickettsia spp.

          Conclusions

          The present study was the concomitant report of wild boar, hunting dog and hunter exposure to SFG rickettsiae agents, performed in two different Brazilian biomes. Wild boar hunting may increase the risk of human exposure and consequently tick-borne disease Wild boars may be carrying and spreading capybara ticks from their original habitats to other ecosystems. Further studies can be required to explore the ability of wild boars to infecting ticks and be part of transmission cycle of Rickettsia spp.

          Author summary

          The present study reported serological findings and molecular assays of Rickettsia spp and ticks of wild boars, simultaneous to their correspondent hunting dogs and hunters. Seropositivity for Rickettsia spp. was higher in wild boars when compared to dogs and humans but was similar between dogs and humans. Despite Rickettsia spp. prevalence was statistically higher in southern than central-western Brazil for wild boars, no significance was observed in hunting dogs and hunters. For the first time, A. sculptum ticks were founded in wild boars from the subtropical climate of southern Brazil. Despite human beings have been considered less exposed to ticks (and therefore rickettsiae) than animals, specific human activities such as wild boar hunting may increase the risk of exposure and consequently tick-borne disease. Wild boars may be carrying and spreading capybara ticks from their original habitats to other ecosystems. These results may provide important findings for public action planning to prevent neglected vector-borne diseases in overlapping areas of wild boars, hunting dogs and hunters. Further studies can be required to explore the ability of wild boars to infecting ticks and be part of transmission cycle of Rickettsia spp.

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          Most cited references48

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          Ticks and tickborne bacterial diseases in humans: an emerging infectious threat.

          Ticks are currently considered to be second only to mosquitoes as vectors of human infectious diseases in the world. Each tick species has preferred environmental conditions and biotopes that determine the geographic distribution of the ticks and, consequently, the risk areas for tickborne diseases. This is particularly the case when ticks are vectors and reservoirs of the pathogens. Since the identification of Borrelia burgdorferi as the agent of Lyme disease in 1982, 15 ixodid-borne bacterial pathogens have been described throughout the world, including 8 rickettsiae, 3 ehrlichiae, and 4 species of the Borrelia burgdorferi complex. This article reviews and illustrate various aspects of the biology of ticks and the tickborne bacterial diseases (rickettsioses, ehrlichioses, Lyme disease, relapsing fever borrelioses, tularemia, Q fever), particularly those regarded as emerging diseases. Methods are described for the detection and isolation of bacteria from ticks and advice is given on how tick bites may be prevented and how clinicians should deal with patients who have been bitten by ticks.
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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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              Laboratory diagnosis of rickettsioses: current approaches to diagnosis of old and new rickettsial diseases.

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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: ResourcesRole: Validation
                Role: ConceptualizationRole: InvestigationRole: ValidationRole: Writing – review & editing
                Role: ResourcesRole: Writing – review & editing
                Role: Formal analysisRole: SoftwareRole: Writing – review & editing
                Role: ResourcesRole: ValidationRole: Writing – review & editing
                Role: ResourcesRole: Writing – review & editing
                Role: ResourcesRole: ValidationRole: Writing – review & editing
                Role: ResourcesRole: ValidationRole: Writing – review & editing
                Role: ResourcesRole: Writing – review & editing
                Role: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: ValidationRole: Writing – review & editing
                Role: Funding acquisitionRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: ValidationRole: Writing – review & editing
                Role: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                30 May 2019
                May 2019
                : 13
                : 5
                : e0007405
                Affiliations
                [1 ] Department of Cellular and Molecular Biology, Federal University of Paraná, Curitiba, Paraná, Brazil
                [2 ] Department of Veterinary Medicine, School of Veterinary Medicine and Animal Science, Federal University of Goiás, Goiânia, Goiás, Brazil
                [3 ] Department of Veterinary Science, Federal University of Paraná, Curitiba, Paraná, Brazil
                [4 ] Department of Veterinary Population Medicine, University of Minnesota, St. Paul, Minnesota, United States of America
                [5 ] Department of Preventive Veterinary Medicine and Animal Health, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil
                [6 ] Department of Medicine, State University of Ponta Grossa, Paraná, Brazil
                [7 ] Assistant professor, Department of Comparative Pathobiology, Purdue University, West Lafayette, Indiana, United States of America
                [8 ] Adjunct professor, Department of Comparative Pathobiology, Purdue University, West Lafayette, Indiana, United States of America
                Faculty of Science, Ain Shams University (ASU), EGYPT
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-1037-970X
                Article
                PNTD-D-18-01995
                10.1371/journal.pntd.0007405
                6542515
                31145746
                f270abdd-ace8-42f0-b82c-46a71f45588b
                © 2019 Kmetiuk et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 18 December 2018
                : 22 April 2019
                Page count
                Figures: 1, Tables: 2, Pages: 14
                Funding
                Funded by: Higher Education Improvement Coordination (CAPES-DS)
                Award ID: 40001016007P8
                This work has been supported by the Higher Education Improvement Coordination (CAPES-DS/ protocol number 40001016007P8), Brazil. Dr. Kmetiuk has been supported by a PhD fellowship and research funding from Capes DS through the Graduate College of Cellular and Molecular Biology, Federal University of Paraná. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
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                Animals
                Vertebrates
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