Serological exposure of spotted fever group Rickettsia in capybaras (Hydrochoerus hydrochaeris) from urban parks in Campo Grande, Brazilian Midwest

ABSTRACT

Background:

Rickettsia of the spotted fever group (SFG) has been reported in ticks and domestic animals in Campo Grande (CG), Midwest Brazil.

Methods:

We searched for Rickettsia in the SFG in capybaras and their ticks in an urban park in the CG.

Results:

The seropositivity rate was 88.2% (15/17). Although 87.7% of the capybaras sampled showed infestations with Amblyomma sculptum, A. dubitatum, and Amblyomma spp., no molecular results were detected in ticks.

Conclusions:

Since Rickettsia from the SFG circulates among capybaras in the urban parks of Campo Grande, this large rodent species should be monitored within the One Health Agenda.

Keywords:
Capybaras; Rickettsia spp.; Urban parks; One health; Brazilian mildest

Rickettsia rickettsii is the etiological agent of Brazilian spotted fever, an emerging zoonosis of great public health importance¹. Campo Grande (CG), the capital of Mato Grosso do Sul (MS) state, Brazil, has approximately one million inhabitants. This city has several urban parks, green areas, and conservation units formed by cerrado sensu stricto (savanna), cerradão (woodland savanna), and riparian forest². Rickettsia, belonging to the spotted fever group (SFG), has been found in CG and its surroundings, showing molecular evidence for R. parkeri in A. sculptum³, R. parkeri strain Atlantic rainforest in A. ovale⁴, R. parkeri, R. africae, and R. sibirica in A. dubitatum⁵. Furthermore, Campos et al.⁶ reported a general seroprevalence of Rickettsia spp. in 25.6% of horses sampled in the CG (n=262); 19.8% were exposed to R. rickettsii, 16.7% to R. parkeri, and 17.5% to R. amblyommatis.

Caviomorph rodent capybaras (Hydrochoerus hydrochaeris) play a central role in the epidemiology of Rickettsia in urban areas, as they have high reproduction rates and continually maintain active infections in vector ticks^7,8,9. Indeed, after primary infection, young animals have high rates of bacteremia⁸. In addition, their extraordinary adaptation to urban areas results in high population densities^2,7. In CG, capybaras typically rest inside forest patches during the day, moving to open grasslands to graze in the twilight, and spending the night in these open areas², thus, playing an important role in dispersing ticks between forest and grassland areas. In urban parks in CG, humans are acclimatized to capybaras, approaching them, walking near them, and spending their daytime recreational time in the same pastures grazed by capybaras at night².

The scenario found in urban fragments areas in CG was as follows: (a) circulation of Rickettsia from the SFG group, (b) high density of capybaras, and (c) spatial sharing between humans and capybaras. This scenario raises a red flag concerning the possibility of rickettsia transmission from the SFG group of capybaras to humans. Therefore, it is necessary to investigate the presence of Rickettsia circulating in urban capybaras, mainly those living within urban parks, for the adequate surveillance and epidemiological control of spotted fever in large cities in Brazil. Therefore, this study aimed to investigate the serological occurrence of Rickettsia spp. belonging to SFG in capybaras from urban parks in the CG.

This study was performed in two urban areas of CG: (i) the Indigenous Nations Park (PNI) and (ii) the Private Reserve of the Federal University of Mato Grosso do Sul. Between May 2017 and August 2018, 17 capybaras were treated with tiletamine and zolazepam (Zoletil ®Vibrac) using a rifle ( J.M.DB13 ®Daninject). Ticks parasitizing capybaras were collected after visual inspection for 60 s and identified using previously published dichotomous keys¹⁰. We used an indirect immunofluorescence antibody test (IFAT) to detect IgG antibodies against Rickettsia spp. in the SFG according to Campos et al⁶. We used slides containing crude antigens derived from Rickettsia isolates from R. rickettsii strain Taiacu, R. parkeri strain At24, and R. amblyommatis strain Ac37, which are available at the Laboratory of Parasitic Diseases (University of São Paulo, Department of Preventive Veterinary Medicine and Animal Health). All field procedures and laboratory studies were conducted under a license granted by the Instituto Chico Mendes de Conservação da Biodiversidade (license number 70946-3). This study was approved by the Ethics Committee for Animal Use at the Universidade Católica Dom Bosco (license number 013/2020).

Our results showed that 88.2% (15/17) of sampled capybaras were seropositive for Rickettsia spp. Among these, 64.7% (11/17) were R. rickettsii, 88.2% (15/17) were R. parkeri, and 41.1% (7/17) were R. amblyommatis. We observed that six animals displayed seropositivity for R. rickettsii and R. parkeri, two for R. parkeri and R. amblyommatis, and five all three species (R. rickettsia, R. parkeri, and R. amblyommatis). Only two animals had a single exposure to R. parkeri, and we observed four animals with high IgG antibody titers ranging from 1:512 to 1:2048 (Table 1). Moreover, 88.2% (15/17) of the sampled capybaras were infested with ticks (n=80), including 25 specimens of A. dubitatum (19 males and 6 females), 29 specimens of A. sculptum (16 males and 13 females), and 26 immature forms of Amblyomma spp. (24 nymphs and 2 larvae).

TABLE 1:
End point titers of indirect immunofluorescence assay for three rickettsia species of capybaras (Hydrochoerus hydrochaeris) (n=17) sampled in Campo Grande, midwestern Brazil.

Capybara sera	IFAT titers for the following Rickettsia antigens			PAIHR
	Rickettsia rickettsii	Rickettsia parkeri	Rickettsia amblyommatis
1	1/128	1/128	NR
2	NR	1/64	NR	R. parkeri
3	NR	NR	NR
4	NR	1/256	1/128
5	1/128	1/128	NR
6	1/128	1/128	NR
7	1/128	1/128	1/128
8	NR	1/128	1/256
9	1/2048	1/2048	1/512
10	1/256	1/1024	1/256	R. parkeri
11	1/256	1/512	NR
12	1/256	1/256	NR
13	NR	NR	NR
14	1/256	1/512	NR
15	1/128	1/2048	1/1024
16	1/64	1/256	1/64	R. parkeri
17	NR	1/128	NR	R. parkeri

• PAIHR: A possible antigen involved in a homologous reaction (serum showing a Rickettsia species titer at least fourfold higher than that observed for any other Rickettsia species was considered homologous to the first Rickettsia species). NR: nonreactive at titer 64 or higher; IFAT: indirect immunofluorescence antibody test.

Our results showed that capybaras exposed to Rickettsia spp. belonging to the SFG were more widely distributed in the Brazilian Midwest than previously reported¹¹. Although we investigated a low number of capybaras, the high seropositivity rates of 88.2% (15/17), with high titers ranging from 1:512 to 1:2048, indicate that capybaras may play an important role in the epidemiology of Rickettsia spp. in the studied area. Serological confirmation of Rickettsia species that may infect capybaras should be observed with caution due to cross-reactions between different rickettsia species belonging to SFG⁷. However, our results showed that the four capybaras sampled were parasitized by R. parkeri (Table 1), a species already recorded parasitizing A. dubitatum in the studied area⁵.

Capybaras are the central host species for Brazilian spotted fever because (i) they develop high rickettsemias (amplifier hosts), ensuring a constant infection of tick vectors, (ii) they have a high reproduction rate, and (iii) they are parasitized by different species of Amblyomma^8,12. Indeed, the high rate of infestation by A. sculptum, the main tick vector species for Rickettsia spp.¹³, observed in the sampled capybaras suggests a potential risk for transmission of Rickettsia spp. Furthermore, since A. sculptum has already been reported to parasitize humans¹ and PNI urban parks are visited daily by hundreds of people², there is a possibility of spillover of Rickettsia from the SFG to humans.

Although A. dubitatum has been reported to parasitize Rickettsia spp. belonging to the SFG in urban parks in CG⁵, this is the first time this tick species has been found to parasitize capybaras in urban parks in CG, suggesting that A. dubitatum may play an important role in the transmission cycles of these rickettsial agents in the study area. Additionally, despite A. dubitatum not being a tick species associated with humans¹⁴, it has been reported that opportunities for pathogen transmission via larvae and nymphs of Amblyomma species are higher in degraded habitats¹⁵ such as urban parks.

Additionally, capybaras that inhabited urban green areas in the CG presented large home ranges, bimodal daily activity patterns, and remarkable changes in habitat selection throughout the day². Indeed, the wide home ranges, larger than those estimated in natural environments, together with the increase in selectivity patterns for forest areas on days of high human presence reported by Medeiros et al.², strongly favor the spread of ticks infected with Rickettsia spp. through urban green areas by capybaras.

We highlight that the capybaras that inhabit the urban parks of CG are the target of constant discussions about translocation to native areas of the Cerrado and Pantanal biomes because of the risk of spillover of zoonotic agents. This topic should be discussed carefully because it has been demonstrated that the introduction of a single infected capybara with at least one infected attached tick is sufficient for the spillover of Brazilian spotted fever in a non-endemic area¹².

Campo Grande, in the Midwest region of Brazil, should be monitored since because (i) capybaras that live in urban green areas are highly exposed to Rickettsia of the SFG; (ii) these capybaras presented high tick infestations; (iii) the tick species found parasitizing capybaras have anthropophilic habits; (iv) urban green fragments areas of CG have an intense people flow²; (v) A. dubitatum parasitizing capybaras were found to be infected by Rickettsia of the SFG in the studied areas⁵; and (vi) Campos et al.⁶ noticed that 25.6% of 262 sampled horses in the CG were exposed to rickettsia agents of the SFG. Owing to the latent risk of transmission, a surveillance and contingency plan for rickettsioses should be considered for the study area.

ACKNOWLEDGMENTS

First author thanks the “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior” and “Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul” (FUNDECT grant PRONEX ; 006/2015) (FUNDECT/DECIT-MS/CNPq/SES Nº 03/2016 - PPSUS-MS, nº 59/300.069/2017).

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• Financial Support: This work was supported by the National Council for Scientific and Technological Development (CNPq) [Productivity grant number 308768/2017-5], the Foundation for Support to the Development of Education, Science and Technology of the State of Mato Grosso do Sul [grant number 59/300.187/2016], and the Foundation for Research Support of the State of São Paulo [grant number 2018/02753-0].

Publication Dates

• Publication in this collection
  19 Sept 2022
• Date of issue
  2022

History

• Received
  08 Apr 2022
• Accepted
  01 July 2022