Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link

Disclaimer: Early release articles are not considered as final versions. Any changes will be reflected in the online version in the month the article is officially released.

Volume 25, Number 12—December 2019
Research Letter

Human Parasitism by Amblyomma parkeri Ticks Infected with Candidatus Rickettsia paranaensis, Brazil

Ana Beatriz P. Borsoi, Karla BitencourthComments to Author , Stefan V. de Oliveira, Marinete Amorim, and Gilberto S. Gazêta
Author affiliations: Instituto Oswaldo Cruz, Rio de Janeiro, Brazil (A.B.P. Borsoi, K. Bitencourth, M. Amorim, G.S. Gazêta); Universidade Federal de Uberlândia, Uberlândia, Brazil (S.V. de Oliveira); Ministério da Saúde do Brasil, Brasília, Brazil (S.V. de Oliveira)

Suggested citation for this article

Abstract

Spotted fever is the main rickettsial disease in Brazil. We report 12 cases of human parasitism by Amblyomma parkeri in the Atlantic rainforest, an area of Brazil to which spotted fever is endemic. Nine of the ticks were infected with Candidatus Rickettsia paranaensis.

Spotted fever is considered the main tickborne disease in South America (1). In Brazil, spotted fever has been reported since the 1920s and is known to show great clinical diversity and ecoepidemiologic scenario complexity, involving Rickettsia rickettsii transmitted by Amblyomma sculptum and A. aureolatum ticks and Rickettsia parkeri strain Atlantic rainforest vectored by A. ovale ticks (2). However, several studies have identified different Rickettsia species infecting a variety of tick species in Brazil, indicating the possibility of newly emerging spotted fever scenarios in Brazil (13).

In southern Brazil, in addition to the scenario already established for the Atlantic forest region, studies indicate the possibility of a unique cycle developing in the Pampa biome, in which R. parkeri sensu stricto might be associated with spotted fever cases involving an A. tigrinum tick vector (3). Accordingly, to expand the understanding of the spotted fever scenario in Brazil, we conducted a molecular study of Rickettsia in A. parkeri ticks as parasites of humans in an area of Brazil to which spotted fever is endemic.

During 2013–2018, in an investigation and surveillance of spotted fever cases in urban areas near Atlantic rainforest fragments in the Parana, Santa Catarina, and Rio Grande do Sul states in southern Brazil, we collected 12 tick nymphs parasitizing humans and morphologically identified these ticks as A. parkeri (4). We individually processed 11 specimens for DNA extraction (5), subjected this DNA to PCR for molecular confirmation of tick species (6), and isolated gltA, htrA, ompA, and ompB gene fragments (Appendix Table). We purified PCR products, sequenced them, and compared them with rickettsial sequences available in GenBank. We subjected concatenated aligned rickettsial sequences to maximum-likelihood analysis.

Figure

Thumbnail of Concatenated phylogenetic analysis of rickettsia gene fragments detected in Amblyomma parkeri ticks in Brazil. Gene fragments gltA (1,013 bp), htrA (370 bp), ompA (494 bp), and ompB (822 bp) were inferred by maximum-likelihood analysis with the evolution model T92 + G (Tamura model). Values on the branches indicate bootstrap values (cutoff value 70%). Stars indicate sequences obtained in this study. GenBank accession numbers are given in parentheses. Scale bar indicates nucleotide s

Figure. Concatenated phylogenetic analysis of rickettsia gene fragments detected in Amblyomma parkeri ticks in Brazil. Gene fragments gltA (1,013 bp), htrA (370 bp), ompA (494 bp), and ompB (822 bp) were inferred...

We identified A. parkeri ticks with containing rickettsia in all 3 states studied. Nine samples amplified fragments from >1 of the 4 rickettsia gene markers studied. All sequences for ompB and ompA gene fragments showed 100% similarity with Candidatus Rickettsia paranaensis (GenBank accession nos. KX018050, JN126322, and JN126321). The htrA and gltA sequences had 100% similarity to many of the spotted fever group rickettsia, including Candidatus R. paranaensis (GenBank accession nos. KX018052 and JN126320). Phylogenetic analysis showed that bacteria detected in A. parkeri ticks from southern Brazil were in the same clade as Candidatus R. paranaensis (Figure).

The pathogenicity of Candidatus R. paranaensis is unknown. However, Peckle et al. (7) placed it close to the Old World species R. africae and R. sibirica, both of which are proven pathogenic species (1). A. parkeri nymphs infected by Candidatus R. paranaensis are not uncommon (7) and might have high frequencies of infection. Luz et al. (8) reported that 75% of passariform birds in southeastern Brazil were infected with ticks, a value similar to that obtained in this study (81.81%) for humans in the southern region. Thus, circulation of Candidatus R. paranaensis in the Atlantic Forest biome might be closely associated with the presence of A. parkeri immature tick stages and passeriform birds.

Although reports of human parasitism by tick species of the genus Amblyomma are increasing, A. parkeri ticks have been rarely reported from humans, although there are reports of parasitism in the Atlantic rainforest area of southeastern Brazil, including a high prevalence of this ixodid (nymphs) on humans in Rio Grande do Sul State (9,10). Although these reports were for a region to which spotted fever is endemic, there was no study of the associated rickettsia. However, our results show 12 humans parasitized by A. parkeri nymphs in the 3 states that compose the southern region of Brazil, indicating that the parasitism of humans by such ticks is more common than that reported. Examples of Candidatus R. paranaensis in A. parkeri parasiting humans in an area to which spotted fever is endemic, with milder clinical characteristics (2), highlight the need to investigate the role of vector and rickettsia in spotted fever in southern Brazil. This investigation should help in formulating appropriate public health responses by existing surveillance programs.

Ms. Borsoi is a PhD student at the Oswaldo Cruz Institute, Rio de Janeiro, Brazil. Her primary research interests are tick taxonomy and rickettsia, with an emphasis on tick–human interactions.

Top

Acknowledgments

We thank the epidemiologic and environmental surveillance teams and technicians of the Central Public Health Laboratories of the states of Paraná, Santa Catarina, and Rio Grande do Sul for providing material used in this study; the Department of Health Surveillance of the Ministry of Health of Brazil for assistance; and Adrian Barnett for assistance with English.

This study was supported by Ministry of Health of Brazil.

Top

References

  1. Parola  P, Paddock  CD, Socolovschi  C, Labruna  MB, Mediannikov  O, Kernif  T, et al. Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev. 2013;26:657702. DOIPubMed
  2. de Oliveira  SV, Guimarães  JN, Reckziegel  GC, Neves  BM, Araújo-Vilges  KM, Fonseca  LX, et al. An update on the epidemiological situation of spotted fever in Brazil. J Venom Anim Toxins Incl Trop Dis. 2016;22:22. DOIPubMed
  3. Weck  B, Dall’Agnol  B, Souza  U, Webster  A, Stenzel  B, Klafke  G, et al. Spotted fever group Rickettsia in the pampa biome, Brazil, 2015–2016. Emerg Infect Dis. 2016;22:20146. DOIPubMed
  4. Martins  TF, Onofrio  VC, Barros-Battesti  DM, Labruna  MB. Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key. Ticks Tick Borne Dis. 2010;1:7599. DOIPubMed
  5. Aljanabi  SM, Martinez  I. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res. 1997;25:46923. DOIPubMed
  6. Mangold  AJ, Bargues  MD, Mas-Coma  S. Mitochondrial 16S rDNA sequences and phylogenetic relationships of species of Rhipicephalus and other tick genera among Metastriata (Acari: Ixodidae). Parasitol Res. 1998;84:47884. DOIPubMed
  7. Peckle  M, Luz  HR, Labruna  MB, Serpa  MCA, Lima  S, Maturano  R, et al. Multi-locus phylogenetic analysis groups the New World bacterium Rickettsia sp. strain ApPR with the Old World species R. africae; proposal of “Candidatus Rickettsia paranaensis”. Ticks Tick Borne Dis. 2019;10:101261. DOIPubMed
  8. Luz  HR, Faccini  JLH, McIntosh  D. 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. 2017;8:65765. DOIPubMed
  9. Martins  TF, Scofield  A, Oliveira  WBL, Nunes  PH, Ramirez  DG, Barros-Battesti  DM, et al. Morphological description of the nymphal stage of Amblyomma geayi and new nymphal records of Amblyomma parkeri. Ticks Tick Borne Dis. 2013;4:1814. DOIPubMed
  10. Reck  J, Souza  U, Souza  G, Kieling  E, Dall’Agnol  B, Webster  A, et al. Records of ticks on humans in Rio Grande do Sul state, Brazil. Ticks Tick Borne Dis. 2018;9:1296301. DOIPubMed

Top

Figure

Top

Suggested citation for this article: Borsoi ABP, Bitencourth K, de Oliveira SV, Amorim M, Gazêta GS. Human parasitism by Amblyomma parkeri ticks infected with Candidatus Rickettsia paranaensis, Brazil. Emerg Infect Dis. 2019 Dec [date cited]. https://doi.org/10.3201/eid2512.190988

DOI: 10.3201/eid2512.190988

Original Publication Date: 11/7/2019

Table of Contents – Volume 25, Number 12—December 2019

Comments

Please use the form below to submit correspondence to the authors or contact them at the following address:

Karla Bitencourth, Laboratório de Referência Nacional em Vetores das Riquetsioses, Anexo Posterior ao Pavilhão Lauro Travassos, Sala 8, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil, 4.365, Manguinhos, Rio de Janeiro RJ 21040-900, Brazil

Send To

character(s) remaining.

Comment submitted successfully, thank you for your feedback.

Top

Page created: November 07, 2019
Page updated: November 07, 2019
Page reviewed: November 07, 2019
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external