Log in

Molecular Detection of Rickettsia parkeri Strain Atlantic Rainforest in Ticks Parasitizing Small Mammals in Northeastern Brazil

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Purpose

Small mammals are important reservoirs of ticks and their pathogens in nature. However, studies reporting these associations are still rare in Brazil. In the present study, we investigated the presence of Rickettsia DNA in ticks parasitizing rodents and marsupials captured in different areas throughout the Atlantic rainforest biome, Bahia, Northeastern (NE), Brazil.

Methods

The study was conducted in five municipalities within of the Atlantic Forest biome, Bahia state, in NE Brazil. Two campaigns were done in each municipality. For host captures Sherman and Tomahawk traps were used, and pitfall traps. After being captured, the hosts were anesthetized and their entire body examined for ticks. When ticks were detected, they were manually removed and stored in eppendorf tubes (1.5 ml) containing absolute PA ethanol for future laboratory analysis (identification of ticks and detection of Rickettsia spp.).

Results

A total of 609 mammals were captured. Overall, 208 ticks of the genus Amblyomma and Ixodes were collected: A. ovale, I. loricatus and A. varium. Rickettsia DNA was detected in A. ovale and it was 99–100% of identity to the sequence deposited in GenBank as Rickettsia parkeri strain Atlantica rainforest.

Conclusion

These results suggest that R. parkeri strain Atlantic rainforest occurs in the region, and A. ovale is likely the vector.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Data Availability Statement

The data supporting the conclusions of this article are included withinthe article.

References

  1. Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Abdad MY, Stenos J, Bitam I, Fournier PE, Raoult D (2013) Update on Tick-Borne Rickettsioses around the World: a geographic approach. Clin Microbiol Rev 26:657–702. https://doi.org/10.1128/CMR.00032-13

    Article  PubMed  PubMed Central  Google Scholar 

  2. Spolidorio MG, Labruna MB, Mantovani E, Brandao PE, Richtzenhain LJ, Yoshinari NH (2010) Novel spotted fever group rickettsiosis, Brazil. Emerg Infect Dis 16:521–523. https://doi.org/10.3201/eid1603.091338

    Article  PubMed  PubMed Central  Google Scholar 

  3. Romer Y, Nava S, Govedic F, Cicuttin G, Denison AM, Singleton J, Kelly AJ, Kato CY, Paddock CD (2014) Rickettsia parkeri rickettsiosis in different ecological regions of Argentina and its association with Amblyomma tigrinum as a potential vector. Am J Trop Med Hyg 91:1156–1160. https://doi.org/10.4269/ajtmh.14-0334

    Article  PubMed  PubMed Central  Google Scholar 

  4. Faccini-Martínez Á, de Oliveira SV, Cerutti Junior C, Labruna MB (2018) Rickettsia parkeri spotted fever in Brazil: epidemiological surveillance, diagnosis and treatment. J Health Biol Sci 6: 299–312. https://doi.org/10.12662/2317-3076jhbs.v6i3.1940.

  5. Faccini-Martínez Á, Félix ML, Armua-Fernandez MT, Venzal JM (2018) An autochthonous confirmed case of Rickettsia parkeri rickettsiosis in Uruguay. Ticks Tick Borne Dis 9:718–719. https://doi.org/10.1016/j.ttbdis.2018.02.015

    Article  PubMed  Google Scholar 

  6. Luz HR, Costa FB, Benatti HR, Ramos VN, Serpa MCA, Martins TF (2019) Epidemiology of capybara-associated Brazilian spotted fever. PLoS Negl Trop Dis 13:e0007734. https://doi.org/10.1371/journal.pntd.0007734

    Article  PubMed  PubMed Central  Google Scholar 

  7. Horta MC, Moraes-Filho J, Casagrande RA, Saito TB, Rosa SC, Ogrzewalska M, Matushima ER, Labruna MB (2009) Experimental Infection of opossums Didelphis aurita by Rickettsia rickettsii and evaluation of the transmission of the infection to ticks Amblyomma cajennense. Vector Born Zoon Dis 9:109–118. https://doi.org/10.1089/vbz.2008.0114

    Article  Google Scholar 

  8. Krawczak FS, Agostinho WC, Polo G, Moraes-Filho J, Labruna MB (2016) Comparative evaluation of Amblyomma ovale ticks infected and noninfected by Rickettsia sp. strain Atlantic rainforest, the agent of na emerging rickettsiosis in Brazil. Ticks Tick Borne Dis 7:502–507. https://doi.org/10.1016/j.ttbdis.2016.02.007

    Article  PubMed  Google Scholar 

  9. Szabó MP, Nieri-Bastos FA, Spolidorio MG, Martins TF, Barbieri AM, Labruna MB (2013) In vitro isolation from Amblyomma ovale (Acari: Ixodidae) and eco-logical aspects of the Atlantic rainforest Rickettsia, the causative agent of a novel spotted fever rickettsiosis in Brazil. Parasitology 140:719–728

    Article  PubMed  Google Scholar 

  10. Szabó MPJ, Pinter A, Labruna MB (2013) Ecology, biology and distribution of spotted-fever tick vectors in Brazil. Front Cell Infect Microbiol 3:27

    Article  PubMed  PubMed Central  Google Scholar 

  11. Krawczak FS, Muñoz-Leal S, Guztzazky AC, Oliveira SV, Santos FC, Angerami RN, Moraes-Filho J, de Souza JC (2016) Rickettsia sp. strain atlantic rainforest infection in a patient from a spotted fever-endemic area in southern Brazil. Am J Trop Med Hyg 95:551–553. https://doi.org/10.4269/ajtmh.16-0192

    Article  PubMed  PubMed Central  Google Scholar 

  12. Sevá AP, Martins T F, Muñoz-Leal S, Rodrigues AC, Pinter A, Luz HR, Angerami RN, Labruna MB (2019) Angerami and Marcelo B. Labruna. A human case of spotted fever caused by Rickettsia parkeri strain Atlantic rainforest and its association to the tick Amblyomma ovale. Parasit Vectors 12: 471. https://doi.org/10.1186/s13071-019-3730-2

  13. Martiniano NODM, Sato TP, Vizzoni VF, Ventura SDF, Oliveira SVD, Amorim M, Gazêta GS (2022) A new focus of spotted fever caused by Rickettsia parkeri in Brazil. Rev Instit Med Trop São Paulo, 64

  14. Maia MO, Koppe VC, Muñoz-Leal S, Martins TF, Marcili A, Labruna MB, Pacheco RC (2018) Detection of Rickettsia spp. in ticks associated to wild mammals in Northeastern Brazil, with notes on an undetermined Ornithodoros sp. collected from marsupials. Exp Appl Acarol 76:523–535

    Article  PubMed  Google Scholar 

  15. Mori SA, Boom BM, Carvalho AM, Santos TS (1983) Southern Bahia moist Forest. Bot Rev. https://doi.org/10.1007/BF02861011

    Article  Google Scholar 

  16. Cirino BS, Costa Neto SF, Maldonado Júnior A, Gentile R (2020) First study on the helminth community structure of the neotropical marsupial Metachirus myosuros (Didelphimorphia, Didelphidae). Braz J Vet Parasitol 29:e005420. https://doi.org/10.1590/S1984-29612020064

    Article  CAS  Google Scholar 

  17. Silva AADS, Alvarez MRDV, Mariano-Neto E, Cassano CR (2020) Is shadier better? The effect of agroforestry management on small mammal diversity. Biotropica 52:470–479. https://doi.org/10.1111/btp.12750

    Article  Google Scholar 

  18. Kersul MG, Costa NA, Boullosa RG, Silva AAS, Rios EO, Munhoz AD, Andrade-Silva BE, Maldonado Junior A, Gentile R, Alvarez MR (2020) Helminth communities of sigmonontine rodents in cocoa agroforestry systems in Brazil. IJP: Paras Wildlife 11: 62–71. https://doi.org/10.1016/j.ijppaw.2019.11.008

  19. Abreu EF, Casali DM, Garbino GST, Libardi GS, Loretto D, Loss AC, Marmontel M, Nascimento MC, Oliveira ML, Pavan SE, Tirelli FP (2021) Lista de Mamíferos do Brasil, versão 2021–1 (Abril). Comitê de Taxonomia da Sociedade Brasileira de Mastozoologia (CT-SBMz). Disponível em: <https://www.sbmz.org/mamiferos-do-brasil/>. Acessado em: 28/08/2021

  20. Barros-Battesti DM, Arzua M, Bechara GH (2006) Carrapatos de importância médico-veterinária da região neotropical: um guia ilustrado para identificação de espécies. Vox/ICTTD-3/Butantan, São Paulo, p 223

  21. Onofrio VC, Barros-Battesti DM, Labruna MB, Faccini JL (2009) Diagnoses of and illustrated key to the species of Ixodes Latreille, 1795 (Acari: Ixodidae) from Brazil. Syst Parasitol 72:143–157. https://doi.org/10.1007/s11230-008-9169-z

    Article  PubMed  Google Scholar 

  22. Martins TF, Onofrio VC, Barros-Battesti DM, Labruna MB (2010) Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key. Ticks Tick Borne Dis 1:75–99. https://doi.org/10.1016/j.ttbdis.2010.03.002

    Article  PubMed  Google Scholar 

  23. Sangioni LA, Horta MC, Vianna MCB, Gennari SM, Soares RS, Galvão MAM, Schumaker TTS, Ferreira F, Vidotto O, Labruna MB (2005) Rickettsial infection in animals and Brazilian spotted fever endemicity. Emerg Infect Dis 11:265–270. https://doi.org/10.3201/eid1102.040656

    Article  PubMed  PubMed Central  Google Scholar 

  24. Mangold AJ, Bargues MD, Mas-Coma S (1998) Mitochondrial 16S rDNA sequences and phylogenetic relationships of species of Rhipicephalus and other tick genera among Metastriata (Acari: Ixodidae). Parasitol Res 84:478–484. https://doi.org/10.1007/s004360050433

    Article  CAS  PubMed  Google Scholar 

  25. Labruna MB, Whitworth T, Bouyer DH, McBride J, Camargo LMA, Camargo EP, Popov V, Walker DH (2004) Rickettsia belli and Rickettsia amblyommii in Amblyomma ticks from the State of Rondônia, Western Amazon, Brazil. J Med Entomol 41:1073–1081. https://doi.org/10.1603/0022-2585-41.6.1073

    Article  PubMed  Google Scholar 

  26. Regnery RL, Spruill CL, Plikaytis BD (1991) Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. Int J Bacteriol 173:1576–1589

    Article  CAS  Google Scholar 

  27. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  28. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms. J Parasitol 83:575–583

    Article  CAS  PubMed  Google Scholar 

  29. Sikes RS (2016) Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J Mamm 97:663–688. https://doi.org/10.1093/jmammal/gyw078

    Article  Google Scholar 

  30. Cáceres NC (2001) Food habits, home range and activity of Didelphis aurita (Mammalia, Marsupialia) in a forest fragment of southern Brazil. Stud Neotr Fauna Environ 36:85–92

    Article  Google Scholar 

  31. Miziara SR, Paiva F, Andreotti R, Koller WW, Lopes VA, Pontes NT, Bitencourt K (2008) Occurrence of Ixodes loricatus Neumann, 1899 (Acari: Ixodidae) parasitizing Didelphis albiventris (Lund, 1841) (Didelphimorphia: Didelphidae) in Campo Grande, MS. Rev Bras Parasitol Vet 17:158–160. https://doi.org/10.1590/S1984-38329612008000300008

    Article  PubMed  Google Scholar 

  32. Saraiva DG, Fournier GF, Martins TF, Leal KP, Vieira FN, Câmara EM, Costa CG, Onofrio VC, Barros-Battesti DM, Guglielmone AA, Labruna MB (2012) Ticks (Acari: Ixodidae) associated with small terrestrial mammals in the state of Minas Gerais, southeastern Brazil. Exp Appl Acarol 58:159–166. https://doi.org/10.1007/s10493-012-9570-9

    Article  PubMed  Google Scholar 

  33. Guglielmone AA, Robbins RG, Apanaskevich DA, PetneyTN, Estrada-Peña A, Horak IG (2014) The hard ticks of the world: (Acari: Ixodida: Ixodidae). London: Springer; p 738. https://doi.org/10.1007/978-94-007-7497-1

  34. Nava S, Venzal JM, González-Acuña D, Martins TF, Guglielmone AA (2017) Ticks of the Southern Cone of America: diagnosis, distribution and hosts with taxonomy, ecology and sanitary importance. Elsevier, London

    Google Scholar 

  35. De Sá EFGG, Rodrigues VS, Garcia MV, Zimmermann NP, Ramos VN, Blecha IMZ, Duarte PO, Martins TF, Bordignon MO, Andreotti R (2018) Ticks on Didelphis albiventris from a Cerrado area in the Midwestern Brazil. Syst Appl Acarol 23(5):935–945

    Google Scholar 

  36. Tarragona EL, Sebastian PS, Bottero MNS, Martinez EI, Debarbora VN, Mangold AJ, Guglielmone AA, Nava S (2018) Seasonal dynamics, geographical range size, hosts, genetic diversity and phylogeography of Amblyomma sculptum in Argentina. T T Born Dis 9:1264–1274

    Google Scholar 

  37. Horta MC, Pinter A, Schumaker TT, Labruna MB (2006) Natural infection, transovarial transmission, and transstadial survival of Rickettsia bellii in the Tick Ixodes loricatus (Acari: Ixodidae) from Brazil. Ann NY Acad Sci 1078:285–290

    Article  CAS  PubMed  Google Scholar 

  38. Grisard EC, Carvalho-Pinto CJ, Scholz AF, Toma HK, Schlemper BR Jr, Steindel M (2000) Trypanosoma cruzi infection in Didelphis marsupialis in Santa Catarina and Arvoredo Islands, southern Brazil. Mem Inst Oswaldo Cruz 95:795–800

    Article  CAS  PubMed  Google Scholar 

  39. Horta MC, Labruna MB, Pinter A, Linardi PM, Schumaker TTS (2007) Rickettsia infection in five areas of the state of São Paulo, Brazil. Mem Inst Oswaldo Cruz 102:793–801. https://doi.org/10.1590/S0074-02762007000700003.PMid:18094887

    Article  PubMed  Google Scholar 

  40. Milagres BS, Padilha AF, Barcelos RM, Gomes GG, Montandon CE, Pena DC (2010) Rickettsia in synanthropic and domestic animals and their hosts from two areas of low endemicity for Brazilian spotted fever in the eastern region of Minas Gerais, Brazil. Am J Trop Med Hyg 83:1305–1307. https://doi.org/10.4269/ajtmh.2010.10-0239

    Article  PubMed  PubMed Central  Google Scholar 

  41. Silveira I, Martins TF, Olegário MM, Peterka C, Guedes E, Ferreira F, Labruna MB (2015) Rickettsial infection in animals, humans and ticks in Paulicéia, Brazil. Zoon Pub Healt 62:525–533. https://doi.org/10.1111/zph.12180

    Article  CAS  Google Scholar 

  42. Luz HR, Neto SFC, Weksler M, Gentile R, Faccini JLH (2018) Ticks parasitizing wild mammals in Atlantic Forest areas in the state of Rio de Janeiro, Brazil. Braz J Vet Parasitol 27:409–414

    Google Scholar 

  43. Luz HR, Faccini JLH, McIntosh D (2017) Molecular analyses reveal an abundant diversity of ticks and rickettsial agents associated with wild birds in two regions of primary Brazilian Atlantic Rainforest. Ticks Tick Borne Dis 8:657–665

    Article  PubMed  Google Scholar 

  44. Labruna MB, Jorge RS, Sana DA, Jácomo AT, Kashivakura CK, Furtado MM, Ferro C, Perez SA, Silveira L, Santos TS, Marques SR, Morato RG, Nava A, Adania CH, Teixeira RH, Gomes AA, Conforti VA, Azevedo FC, Prada CS, Silva JC, Batista AF, Marvulo MF, Morato RL, Alho CJ, Pinter A, Ferreira PM, Ferreira F, Barros-Battesti DM (2005) Ticks (Acari: Ixodida) on wild carnivores in Brazil. Exp Appl Acarol 36:149–163. https://doi.org/10.1007/s10493-005-2563-1

    Article  PubMed  Google Scholar 

  45. Martins TF, Moura MM, Labruna MB (2012) Life-cycle and host preference of Amblyomma ovale (Acari: Ixodidae) under laboratory conditions. Exp Appl Acarol 56:151–158. https://doi.org/10.1007/s10493-011-9506-9

    Article  PubMed  Google Scholar 

  46. de Oliveira PB, Harvey TV, Fehlberg HF, Rocha JM, Martins TF, Acosta ICL (2019) Serologic and molecular survey of Rickettsia spp. in dogs, horses and ticks from the Atlantic rainforest of the state of Bahia, Brazil. Exp Appl Acarol 78:431–442. https://doi.org/10.1007/s10493-019-00397-x

    Article  PubMed  Google Scholar 

  47. Fournier GFDSR, Pinter A, Muñoz-Leal S, Labruna MB, Lopes MG, Martins TF, Dias RA (2020) Implications of domestic dogs in the epidemiology of Rickettsia parkeri strain Atlantic rainforest and Rangelia vitalii in Southeastern Brazil. Rev Bras Parasitol Vet 29:1–17

    Article  Google Scholar 

  48. Krawczak FS, Labruna MB (2018) The rice rat Euryoryzomys russatus, a competent amplifying host of Rickettsia parkeri strain Atlantic rainforest for the tick Amblyomma ovale. Ticks Ticks-borne dis 9:1133–1136

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank the staff and students of Laboratory of Biology and Parasitology of Wild Mammals Reservoirs from Oswaldo Cruz Foundation (FIOCRUZ) and to all of them who helped in field works, specially to Élson O. Rios and the Caipora's and Rhip's fraternities. We thank the anonymous reviewers who improved the manuscript, and to Santiago Alvarez Martinez for English revision. We also thank Dr. Rui Cerqueira (UFRJ) and Dr. Pedro Cordeiro Estrela (UFPB) for general coordination of the PPBio Rede BioMA (CNPq 457524/2012-0). This work was also supported by UESC [00220.1100.1264; 00220.1100.1645 and 00220.1100.1536], Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES) [Finance Code 001], Fundação de Amparo a Pesquisa do Estado da Bahia (FAPESB) [PNE0001/2014 and PPP0008/2011], and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) [Grant 306308/2015-0]. CAPES/Brazil) – Finance Code 001. CAPES/DPG—“Amazônia-Legal” (Support Program for Postgraduate Studies in the Legal Amazon), number- 088.990.417-09 for HRL.

Funding

This work was supported by the UESC [00220.1100.1264; 00220.1100.1645 and 00220.1100.1536], Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES) [Finance Code 001], Fundação de Amparo a Pesquisa do Estado da Bahia (FAPESB) [PNE0001/2014 and PPP0008/2011], and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) [Grant 306308/2015–0]. CAPES/Brazil) – Finance Code 001. CAPES/DPG—“Amazônia-Legal” (Support Program for Postgraduate Studies in the Legal Amazon), number- 088.990.417–09 for HRL.

Author information

Authors and Affiliations

Authors

Contributions

JMR, SFCN, PBO, HRL, GRA, JLHF, MHO, TFM: formal analysis, methodology and review & editing. HRL, JLHF, GRA: writing – original draft.

Corresponding author

Correspondence to Hermes R. Luz.

Ethics declarations

Conflict of Interest

The authors declare that they have no competing interests.

Ethical Approval

The animals were captured under authorization from the Chico Mendes Institute for Biodiversity Conservation (ICMBio, License numbers 17131–4, 49238–1 and 38515–2). All procedures followed the Oswaldo Cruz Foundation Ethics Committee on Animal Use (CEUA LW Nº 39/2014) and approved by the Ethics Committee on Animal Use (CEUA-UESC N° 003/2013 and 015/2015). The collected mammals are housed in the Mammalian Collection “Alexandre Rodrigues Ferreira” of the State University of Santa Cruz (CMARF-UESC).

Consent for Publication

All authors read and approved the final draft of the paper.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLS 58 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rocha, J.M., de Oliveira, P.B., da Costa-Neto, S.F. et al. Molecular Detection of Rickettsia parkeri Strain Atlantic Rainforest in Ticks Parasitizing Small Mammals in Northeastern Brazil. Acta Parasit. 67, 1657–1666 (2022). https://doi.org/10.1007/s11686-022-00617-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11686-022-00617-2

Keywords

Navigation