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

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 (). 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 (). 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 (–).

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 (). 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 (). We individually processed 11 specimens for DNA extraction (), subjected this DNA to PCR for molecular confirmation of tick species (), 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.

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).

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 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 substitutions per site.

The pathogenicity of Candidatus R. paranaensis is unknown. However, Peckle et al. () placed it close to the Old World species R. africae and R. sibirica, both of which are proven pathogenic species (). A. parkeri nymphs infected by Candidatus R. paranaensis are not uncommon () and might have high frequencies of infection. Luz et al. () 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 (,). 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 comprise 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 parasitizing humans in an area to which spotted fever is endemic, with milder clinical characteristics (), 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.

Appendix

Additional information on human parasitism by Amblyomma parkeri ticks infected with Candidatus Rickettsia paranaensis, Brazil.