Experimental infection of capybaras Hydrochoerus hydrochaeris by Rickettsia rickettsii and evaluation of the transmission of the infection to ticks Amblyomma cajennense

https://doi.org/10.1016/j.vetpar.2008.12.010Get rights and content

Abstract

The present study evaluated the infection of capybaras (Hydrochoerus hydrochaeris) by Rickettsia rickettsii and their role as amplifier hosts for horizontal transmission of R. rickettsii to Amblyomma cajennense ticks. Two groups of two capybaras each were evaluated: on day 0, group 1 (G1) was infested by R. rickettsii-infected ticks, and group 2 (G2) was inoculated intraperitoneally with R. rickettsii. Two additional groups were control groups, not exposed to R. rickettsii, being CG1 group the control of G1, and CG2 group the control of G2. Capybara rectal temperature was measured daily. Blood samples were collected every 3 days during 30 days, and used to (i) inoculate guinea pigs intraperitoneally; (ii) DNA extraction followed by real-time PCR targeting the rickettsial gene gltA; (iii) hematology; (iv) detection of R. rickettsii-reactive antibodies by indirect immunofluorescence assay (IFA). Blood was also collected from G1 capybaras every ≈10–30 days till the 146th day, to be tested by serology. Capybaras were infested by uninfected A. cajennense nymphs from the 3rd to the 18th day. Engorged nymphs were collected, allowed to molt to adults in an incubator. Thereafter, the subsequent flat ticks were tested by PCR. All G1 and G2 capybaras became infected by R. rickettsii, as demonstrated by guinea pig inoculation and seroconversion, but they showed no fever. Rickettsemia was continually detected from the 6th (G2 capybaras) or 9th (G1 capybaras) to the 18th day post inoculation or infestation with R. rickettsii-infected ticks. A total of 20–25% and 30–35% of the flat ticks previously fed on G1 and G2 capybaras, respectively, became infected by R. rickettsii. The study demonstrated that R. rickettsii was capable to infect capybaras without causing clinical illness, inducing rickettsemia capable to cause infection in guinea pigs and ticks. Our results indicate that capybaras act as amplifier host of R. rickettsii for A. cajennense ticks in Brazil.

Introduction

The bacterium Rickettsia rickettsii is the etiological agent of Rocky Mountain spotted fever (RMSF), an acute febrile, tick-borne disease that has been reported in Canada, United States, Mexico, Costa Rica, Panama, Colombia, Brazil, and Argentina (Dumler and Walker, 2005, Paddock et al., 2008). There has been a clear reemergence of RMSF in Brazil. For example, from 1988 to 1997, there were 25 laboratory-confirmed cases distributed among six municipalities in the state of São Paulo. During the subsequent decade, from 1998 to 2007, there were 255 confirmed cases distributed among 54 municipalities of the state (official data from the São Paulo State Health Secretary at http://www.cve.saude.sp.gov.br). Indeed, this increase is partially attributed to a much more efficient surveillance, especially after the disease became nationally notifiable in 2001 (Silva and Galvão, 2004). However, it is possible that ecological factors have played a major role in this disease reemergence.

Studies in the United States demonstrated that R. rickettsii is transmitted transovarially and transestadially in several tick species, however infection rates by R. rickettsii in ticks are very low (usually <1%) under natural conditions, mainly because R. rickettsii is pathogenic for ticks (Burgdorfer, 1988, Niebylski et al., 1999). Thus, the role of amplifier hosts in the ecology of RMSF is crucial. Amplifier hosts are vertebrate animals that develop rickettsemia for some days, when new uninfected ticks become infected and start new lineages of infected ticks within the tick population (Burgdorfer, 1988, Dumler and Walker, 2005). In the United States, several small rodent species have been implicated to act as amplifier hosts of R. rickettsii, as for example, Microtus pennsylvanicus in the eastern part of the country (Burgdorfer et al., 1966, McDade and Newhouse, 1986). In Brazil, the opossum Didelphis aurita is the only vertebrate that has been shown to be a competent amplifier host of R. rickettsii for Amblyomma cajennense ticks (Horta et al., 2009).

The tick A. cajennense is the main vector of R. rickettsii in Brazil, where horses and capybaras (Hydrochoerus hydrochaeris) are among the most important primary hosts for all parasitic stages of the tick (Vieira et al., 2004, Guedes et al., 2005). In the state of São Paulo, capybaras were considered threatened of extinction during the 1950s. During subsequent decades, capybara populations increased in many areas, and nowadays it is considered a major cause of crop damage in the state (Verdade and Ferraz, 2006), besides various complains of high environmental burdens by A. cajennense due to increased capybara populations. Since capybaras have been suspected to be amplifier hosts for R. rickettsii since the 1940s (Travassos and Vallejo, 1942), the increasing capybara population in the state of São Paulo has also been suspected to be related to the reemergence of RMSF. Based on these statements, the present study performed experimental infection of capybaras by R. rickettsii, and evaluated the role of these animals as amplifier hosts for A. cajennense ticks, under laboratory conditions.

Section snippets

Capybaras

Eight capybaras, 3 months old, provided by a commercial breeding were kept in individual boxes (3 m × 3 m) for the experiment in Mogi Guaçu, state of São Paulo. Capybaras were fed daily with fresh green forage and commercial pellets for rodents, and water ad libitum. Before starting the experiments, capybaras were clinically healthy and their paired serum samples (14 days interval) were shown to contain no reactive antibodies to R. rickettsii, Rickettsia parkeri, Rickettsia felis and Rickettsia

Results

During the study, capybaras of the control groups (CG1 and CG2) remained uninfected because no Rickettsia DNA or R. rickettsii-reactive antibodies were detected in their blood. In contrast, rickettsial infection was evident in both G1 (infected through infestation with R. rickettsii-infected ticks) and G2 (inoculated intraperitoneally with R. rickettsii) capybaras, since they all seroconverted (Fig. 1) and their blood caused rickettsial infection in inoculated guinea pigs (Table 1, Table 2). In

Discussion

The present study showed that capybaras are susceptible to the infection by R. rickettsii. In contrast to other mammal species (humans, dogs, guinea pigs, and domestic rabbits), in which R. rickettsii usually induces high fever and even death (McDade and Newhouse, 1986), capybaras showed no signs of fever. Decades ago, Travassos and Vallejo (1942) reported that R. rickettsii-inoculated capybaras developed no fever during the rickettsemic period of the study. On the other hand, our results

Acknowledgements

We thank the Centro de Controle de Zoonoses (CCZ) of São Paulo Municipality for providing conjugate anti-capybara IgG and Usina Colombo S/A for donating the capybaras. This work was supported by FAPESP (Grants 06/50650-8 to M.C.H. and 06/50918-0 to M.B.L.) and SUCEN (Grant 01/05 to C.E.S.).

References (21)

  • M.E. Arouca et al.

    Valores hematológicos de capivaras (Hydrochoerus hydrochaeris) criadas em cativeiro no Município de Botucatu, SP

    Cienc. Rural

    (2000)
  • E.B. Breitschwerdt et al.

    Clinical, hematologic and humoral immune response in female dogs inoculated with Rickettsia rickettsii and Rickettsia montana

    Am. J. Vet. Res.

    (1988)
  • W. Burgdorfer

    Ecological and epidemiological considerations of Rocky Mountain spotted fever and scrub typhus

  • W. Burgdorfer et al.

    Natural history of tick-borne spotted fever in the USA. Susceptibility of small mammals to virulent Rickettsia rickettsii

    Bull. World Health Organ.

    (1966)
  • J.S. Dumler et al.

    Rocky Mountain spotted fever-changing ecology and persisting virulence

    N. Engl. J. Med.

    (2005)
  • E. Guedes et al.

    Detection of Rickettsia rickettsii in the tick Amblyomma cajennense in a new Brazilian spotted fever-endemic area in the state of Minas Gerais

    Mem. Inst. Oswaldo Cruz

    (2005)
  • M.C. Horta et al.

    Experimental Infection of Opossums Didelphis aurita by Rickettsia rickettsii and Evaluation of the Transmission of the Infection to Ticks Amblyomma cajennense

    Vector Borne Zoonotic Dis.

    (2009)
  • M.B. Labruna et al.

    Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of Sao Paulo, Brazil, where Brazilian spotted fever is endemic

    J. Clin. Microbiol.

    (2004)
  • M.B. Labruna et al.

    Comparative susceptibility of larval stages of Amblyomma aureolatum, Amblyomma cajennense, and Rhipicephalus sanguineus to infection by Rickettsia rickettsii

    J. Med. Entomol.

    (2008)
  • B. La Scola et al.

    Laboratory diagnosis of rickettsioses: current approaches to diagnosis of old and new rickettsial diseases

    J. Clin. Microbiol.

    (1997)
There are more references available in the full text version of this article.

Cited by (94)

  • Rickettsial infection in free-ranging capybaras (Hydrochoerus hydrochaeris) and their ticks (Acari, Ixodidae) in the Caatinga and Atlantic forest biomes, Northeastern Brazil

    2021, Veterinary Parasitology: Regional Studies and Reports
    Citation Excerpt :

    According to Weck et al. (2017), the most significant part of the knowledge about BSF is based on studies on the ecology of vector ticks, since in Brazil the clinical data of patients do not provide enough information for the identification of the Rickettsia species and the vectors involved. In this regard, capybaras act as sentinels of the BSF mainly in nonendemic or unknown endemic areas, since these rodents play an important role in the epidemiology of this disease, they are considered as amplifying host of R. rickettsii (Souza et al., 2009; Ramírez-Hernández et al., 2020) and live in close contact with humans in some areas of Brazil (Fortes et al., 2011). Furthermore, A. sculptum is an efficient vector of zoonotic pathogens due to its generalist behavior and affinity for humans (Pajuaba Neto et al., 2018), although parasitism by A. dubitatum in humans should not be disregarded (Labruna et al., 2007; Pajuaba Neto et al., 2018).

  • Parasites and health status of free-ranging capybaras (Hydrochoerus hydrochaeris) in the Atlantic Forest and Caatinga biomes of Brazil

    2021, Veterinary Parasitology: Regional Studies and Reports
    Citation Excerpt :

    The information concerning A. sculptum and A. dubitatum should be considered for the evaluation of the role of these ticks in the transmission of the zoonotic Rickettsia species. Capybaras are of great importance in the epidemiology of the disease because they are considered reservoirs of Rickettsia spp. and main hosts of vector ticks (Souza et al. 2009; Luz et al. 2019; Ramírez-Hernández et al. 2020). This calls for wildlife and public health professionals to make a great effort to reduce the potential negative impact on the image of these animals for the population, important for the One Health approach (Cunningham et al. 2017).

  • Molecular detection of vector-borne agents in ectoparasites and reptiles from Brazil

    2021, Ticks and Tick-borne Diseases
    Citation Excerpt :

    The nucleotide ompA sequences of Rickettsia sp. from G. harrisi mites from Tropidurus catalanensis lizard, from São Paulo, were related (98 % nucleotide identity) to sequences of R. rickettsii from humans in southeastern Brazil (Espírito Santo state). In the same geographical area, R. rickettsii is reported as the causative agent of the Brazilian spotted fever (BSF) being associated to Amblyomma cajennense sensu lato (A. sculptum) tick and capybara hosts (Souza et al., 2009; Polo et al., 2017; Rocha et al., 2017; Faccini-Martínez et al., 2018). This finding represents the first record of Rickettsia spp. in Pterygosomatidae mites and it deserves further investigation considering the role of reptiles as hosts of ectoparasites infected with other SFG Rickettsia in Asia and Australia (Vilcins et al., 2009; Sumrandee et al., 2014; Kho et al., 2015).

View all citing articles on Scopus
View full text