Acessibilidade / Reportar erro

Parasitism on domestic cats by Amblyomma auricularium and serological evidence of exposure to Rickettsia amblyommatis

Parasitismo em gatos doméstico por Amblyomma auricularium e evidência sorológica de exposição a Rickettsia amblyommatis

Abstract

The domestic cat is not considered a primary host for any specific tick species; however, it can be affected by some Ixodidae species, such as Rhipicephalus sanguineus sensu lato and Amblyomma spp. The study reports parasitism by Amblyomma auricularium and the detection of anti-Rickettsia spp. antibodies in domestic cats from a rural property in the Afrânio municipality, Pernambuco, Brazil. Amblyomma auricularium (24 nymphs, six females, and four males) and Amblyomma sp. (42 larvae) parasitized three cats, and 73 free-living ticks were captured in armadillo burrows: A. auricularium (36 nymphs, six females, five males) and Amblyomma sp. (26 larvae). Blood samples from cats were collected and the obtained plasma were subjected to indirect immunofluorescence assay (IFA) to detect antibodies against Rickettsia antigens. Thus, anti-Rickettsia spp. antibodies were determined (titers ranging from 128 to 512) and showed a predominant antibody response to Rickettsia amblyommatis or a very closely related genotype. This study reports the first infestation of nymphs and adults of A. auricularium on cats in a new area of occurrence in the semi-arid region of Northeastern Brazil and reports for the first time the presence of anti-Ricketsia antibodies in cats in the region, with R. amblyommatis as the probable infectious agent.

Keywords:
Ixodida; Rickettsia ; Felis catus domesticus ; serology; northeast

Resumo

O gato doméstico não é considerado hospedeiro para nenhuma espécie de carrapato. Pode, entretanto, ser afetado por algumas espécies de Ixodídeos, como Rhipicephalus sanguineus e Amblyomma spp. Este estudo relata o parasitismo por Amblyomma auricularium e detecção de anticorpos anti-Rickettsia spp. em gatos domésticos, em uma propriedade rural no município de Afrânio, Pernambuco, Brasil. Amblyomma auricularium (24 ninfas, seis fêmeas e quatro machos) e Amblyomma sp. (42 larvas) parasitavam os gatos, e 73 carrapatos de vida-livre foram capturados em tocas de tatus: A. auricularium (36 ninfas, seis fêmeas, cindo machos) e Amblyomma sp. (26 larvas). Amostras de sangue dos três gatos foram coletadas, e os plasmas obtidos foram submetidos à reação de imunofluorescência indireta (RIFI) para a detecção de anticorpos contra antígenos de Rickettsia. Dessa forma, anticorpos anti-Rickettsia spp. foram determinados (títulos variando de 256 a 512) e demonstraram uma resposta predominante para Rickettsia amblyommatis ou genótipo próximo. Este estudo relata, pela primeira vez, infestação de ninfas e adultos A. auricularium em gatos em uma nova área de ocorrência na região semiárida do nordeste do Brasil. E, também relata, pela primeira vez, a presença de anticorpos anti-Ricketsia em gatos na região, com R. amblyommatis como agente provável pela infecção.

Palavras-chave:
Ixodida; Rickettsia ; Felis catus domesticus ; sorologia; nordeste

Domestic cats (Felis catus domesticus) are parasitized by a variety of ectoparasites including mites, lice, fleas, and ticks (Dantas-Torres & Otranto, 2014Dantas-Torres F, Otranto D. Dogs, cats, parasites, and humans in Brazil: opening the black box. Parasit Vectors 2014; 7(1): 22. http://dx.doi.org/10.1186/1756-3305-7-22. PMid:24423244.
http://dx.doi.org/10.1186/1756-3305-7-22...
), which are of great importance in feline medicine (Ferreira et al., 2010Ferreira DRA, Alves LC, Faustino MAG. Ectoparasitos de Felis catus domesticus (Linnaeus, 1758) na cidade de João Pessoa, Paraíba, Brasil. Biotemas 2010; 23(4): 43-50. http://dx.doi.org/10.5007/2175-7925.2010v23n4p43.
http://dx.doi.org/10.5007/2175-7925.2010...
). Felines are reservoirs for various pathogens with zoonotic potential for humans, including Bartonella henselae, which causes cat scratch disease and Rickettsia typhi, which causes murine typhus (Case et al., 2006Case JB, Chomel B, Nicholson W, Foley JE. Serological survey of vector-borne zoonotic pathogens in pet cats and cats from animal shelters and feral colonies. J Feline Med Surg 2006; 8(2): 111-117. http://dx.doi.org/10.1016/j.jfms.2005.10.004. PMid:16434226.
http://dx.doi.org/10.1016/j.jfms.2005.10...
), both of which are transmitted by fleas.

Ticks are of great importance to human and animal health as they are vectors of pathogens, and many species feed on a wide range of vertebrate hosts, including cats (Mendes-de-Almeida et al., 2011Mendes-de-Almeida F, Crissiuma AL, Gershony LC, Willi LMV, Paiva JP, Guerrero J, et al. Characterization of ectoparasites in an urban cat (Felis catus Linnaeus, 1758) population of Rio de Janeiro, Brazil. Parasitol Res 2011; 108(6): 1431-1435. http://dx.doi.org/10.1007/s00436-010-2189-z. PMid:21181196.
http://dx.doi.org/10.1007/s00436-010-218...
). The domestic cat is not considered the primary host of any tick species, however, ectoparasitism has already been reported by some ixodids, including Rhipicephalus sanguineus sensu lato (s.l.) (Horta et al., 2007Horta MC, Labruna MB, Pinter A, Linardi PM, Schumaker TTS. Rickettsia infection in five areas of the state of São Paulo, Brazil. Mem Inst Oswaldo Cruz 2007; 102(7): 793-801. http://dx.doi.org/10.1590/S0074-02762007000700003. PMid:18094887.
http://dx.doi.org/10.1590/S0074-02762007...
; Ferreira et al., 2010Ferreira DRA, Alves LC, Faustino MAG. Ectoparasitos de Felis catus domesticus (Linnaeus, 1758) na cidade de João Pessoa, Paraíba, Brasil. Biotemas 2010; 23(4): 43-50. http://dx.doi.org/10.5007/2175-7925.2010v23n4p43.
http://dx.doi.org/10.5007/2175-7925.2010...
; Mendes-de-Almeida et al., 2011Mendes-de-Almeida F, Crissiuma AL, Gershony LC, Willi LMV, Paiva JP, Guerrero J, et al. Characterization of ectoparasites in an urban cat (Felis catus Linnaeus, 1758) population of Rio de Janeiro, Brazil. Parasitol Res 2011; 108(6): 1431-1435. http://dx.doi.org/10.1007/s00436-010-2189-z. PMid:21181196.
http://dx.doi.org/10.1007/s00436-010-218...
), Amblyomma triste (Silva et al., 2007Silva AS, Silva MK, Monteiro SG. Parasitismo por Amblyomma triste em gato doméstico. Rev Bras Parasitol Vet 2007; 16(2): 108-109. PMid:17706014.), Amblyomma sculptum, Amblyomma aureolatum, and Amblyomma ovale (Horta et al., 2007Horta MC, Labruna MB, Pinter A, Linardi PM, Schumaker TTS. Rickettsia infection in five areas of the state of São Paulo, Brazil. Mem Inst Oswaldo Cruz 2007; 102(7): 793-801. http://dx.doi.org/10.1590/S0074-02762007000700003. PMid:18094887.
http://dx.doi.org/10.1590/S0074-02762007...
; Dantas-Torres & Otranto, 2014Dantas-Torres F, Otranto D. Dogs, cats, parasites, and humans in Brazil: opening the black box. Parasit Vectors 2014; 7(1): 22. http://dx.doi.org/10.1186/1756-3305-7-22. PMid:24423244.
http://dx.doi.org/10.1186/1756-3305-7-22...
).

The genus Amblyomma has the greatest species diversity in Brazil, and its distribution has been reported worldwide (Barros-Battesti et al., 2006Barros-Battesti DM, Arzua M, Bechara GH. Carrapatos de importância médico-veterinária da região neotropical: um guia ilustrado para identificação de espécies. 1. ed. São Paulo: Vox/ICTTD-3/Butantan; 2006.). Rickettsiae are a group of obligate intracellular Gram-negative bacteria that cause a variety of diseases called rickettsioses, transmitted by hematophagous arthropods (Hiraoka et al., 2005Hiraoka H, Shimada Y, Sakata Y, Watanabe M, Itamoto K, Okuda M, et al. Detection of Rickettsial DNA in ixodid ticks recovered from dogs and cats in Japan. J Vet Med Sci 2005; 67(12): 1217-1222. http://dx.doi.org/10.1292/jvms.67.1217. PMid:16397379.
http://dx.doi.org/10.1292/jvms.67.1217...
). There have been reports of hemoparasitoses in cats caused by Ehrlichia canis (Oliveira et al., 2009Oliveira LS, Mourão LC, Oliveira KA, da Matta Agostini M, Oliveira AC, Almeida MR, et al. Molecular detection of Ehrlichia canis in cats in Brazil. Clin Microbiol Infect 2009; 15(Suppl 2): 53-54. http://dx.doi.org/10.1111/j.1469-0691.2008.02175.x. PMid:19374643.
http://dx.doi.org/10.1111/j.1469-0691.20...
; André et al., 2017André MR, Filgueira KD, Calchi AC, Sousa KCM, Gonçalves LR, Medeiros VB, et al. Co-infection with arthropod-borne pathogens in domestic cats. Rev Bras Parasitol Vet 2017; 26(4): 525-531. http://dx.doi.org/10.1590/s1984-29612017064. PMid:29160357.
http://dx.doi.org/10.1590/s1984-29612017...
), Anaplasma spp. (André et al., 2014André MR, Denardi NCB, Sousa KCM, Gonçalves LR, Henrique PC, Ontivero CRGR, et al. Arthropod-borne pathogens circulating in free-roaming domestic cats in a zoo environment in Brazil. Ticks Tick Borne Dis 2014; 5(5): 545-551. http://dx.doi.org/10.1016/j.ttbdis.2014.03.011. PMid:24889035.
http://dx.doi.org/10.1016/j.ttbdis.2014....
, 2017André MR, Filgueira KD, Calchi AC, Sousa KCM, Gonçalves LR, Medeiros VB, et al. Co-infection with arthropod-borne pathogens in domestic cats. Rev Bras Parasitol Vet 2017; 26(4): 525-531. http://dx.doi.org/10.1590/s1984-29612017064. PMid:29160357.
http://dx.doi.org/10.1590/s1984-29612017...
), Mycoplasma spp. (André et al., 2017André MR, Filgueira KD, Calchi AC, Sousa KCM, Gonçalves LR, Medeiros VB, et al. Co-infection with arthropod-borne pathogens in domestic cats. Rev Bras Parasitol Vet 2017; 26(4): 525-531. http://dx.doi.org/10.1590/s1984-29612017064. PMid:29160357.
http://dx.doi.org/10.1590/s1984-29612017...
; Pesqueira et al., 2023Pesqueira TR, Martins GFS, Farias IF, Evaristo AMCF, Sento Sé FS, Oliveira FRB, et al. Diagnóstico molecular de agentes parasitários e coronavírus em gatos no Nordeste do Brasil. Braz J Global Health 2023; 3(10): 1-7. http://dx.doi.org/10.56242/globalhealth;;2023;3;10;1-7.
http://dx.doi.org/10.56242/globalhealth;...
), Babesia spp., Hepatozoon spp. (André et al., 2015André MR, Herrera HM, Fernandes SJ, Sousa KCM, Gonçalves LR, Domingos IH, et al. Tick-borne agents in domesticated and stray cats from the city of Campo Grande, state of Mato Grosso do Sul, midwestern Brazil. Ticks Tick Borne Dis 2015; 6(6): 779-786. http://dx.doi.org/10.1016/j.ttbdis.2015.07.004. PMid:26187416.
http://dx.doi.org/10.1016/j.ttbdis.2015....
), Theileria spp. (André et al., 2014André MR, Denardi NCB, Sousa KCM, Gonçalves LR, Henrique PC, Ontivero CRGR, et al. Arthropod-borne pathogens circulating in free-roaming domestic cats in a zoo environment in Brazil. Ticks Tick Borne Dis 2014; 5(5): 545-551. http://dx.doi.org/10.1016/j.ttbdis.2014.03.011. PMid:24889035.
http://dx.doi.org/10.1016/j.ttbdis.2014....
, 2015André MR, Herrera HM, Fernandes SJ, Sousa KCM, Gonçalves LR, Domingos IH, et al. Tick-borne agents in domesticated and stray cats from the city of Campo Grande, state of Mato Grosso do Sul, midwestern Brazil. Ticks Tick Borne Dis 2015; 6(6): 779-786. http://dx.doi.org/10.1016/j.ttbdis.2015.07.004. PMid:26187416.
http://dx.doi.org/10.1016/j.ttbdis.2015....
), Bartonella spp. (André et al., 2014André MR, Denardi NCB, Sousa KCM, Gonçalves LR, Henrique PC, Ontivero CRGR, et al. Arthropod-borne pathogens circulating in free-roaming domestic cats in a zoo environment in Brazil. Ticks Tick Borne Dis 2014; 5(5): 545-551. http://dx.doi.org/10.1016/j.ttbdis.2014.03.011. PMid:24889035.
http://dx.doi.org/10.1016/j.ttbdis.2014....
), and Cytauxzoon (André et al., 2017André MR, Filgueira KD, Calchi AC, Sousa KCM, Gonçalves LR, Medeiros VB, et al. Co-infection with arthropod-borne pathogens in domestic cats. Rev Bras Parasitol Vet 2017; 26(4): 525-531. http://dx.doi.org/10.1590/s1984-29612017064. PMid:29160357.
http://dx.doi.org/10.1590/s1984-29612017...
). However, few studies in Brazil have described Amblyomma spp. infestations and the determination of anti-Rickettsia antibodies (Horta et al., 2007Horta MC, Labruna MB, Pinter A, Linardi PM, Schumaker TTS. Rickettsia infection in five areas of the state of São Paulo, Brazil. Mem Inst Oswaldo Cruz 2007; 102(7): 793-801. http://dx.doi.org/10.1590/S0074-02762007000700003. PMid:18094887.
http://dx.doi.org/10.1590/S0074-02762007...
).

Thus, this study reports the parasitism by Amblyomma auricularium in three domestic cats from a farm in the municipality of Afrânio, state of Pernambuco, Brazil, in addition to the detection of anti-Rickettsia spp. antibodies in plasma samples.

From September to December 2021, 76 specimens of ticks were collected from the three domestic cats that used to live on a farm in the municipality of Afrânio. In addition, 73 tick specimens were collected from inside six burrows previously inhabited by six-banded armadillos (Euphractus sexcinctus) on the same farm. To collect ticks from the burrows, we used a flannel with a rod inserted into the burrows, and when the flannel was removed, the ticks were visualized on it. All the ticks were placed in tubes containing 70% ethanol and transported to the laboratory for taxonomic identification. Ticks were separated by stages and identified according to Barros-Battesti et al. (2006)Barros-Battesti DM, Arzua M, Bechara GH. Carrapatos de importância médico-veterinária da região neotropical: um guia ilustrado para identificação de espécies. 1. ed. São Paulo: Vox/ICTTD-3/Butantan; 2006. and Martins et al. (2010)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(2): 75-99. http://dx.doi.org/10.1016/j.ttbdis.2010.03.002. PMid:21771514.
http://dx.doi.org/10.1016/j.ttbdis.2010....
.

Blood samples were collected through venipuncture of the cephalic vein, previously disinfected with ethanol 70%, using 0.55 × 20 mm needles and sterile syringes. Samples were stored in sterile tubes containing anticoagulants at room temperature. Blood samples were centrifuged at 5,000 rpm for 15 min to obtain plasma, which was stored at -20ºC until laboratory analysis. Plasma samples from cats were individually tested by IFA to verify their reactivity to Rickettsia spp., according to Horta et al. (2007)Horta MC, Labruna MB, Pinter A, Linardi PM, Schumaker TTS. Rickettsia infection in five areas of the state of São Paulo, Brazil. Mem Inst Oswaldo Cruz 2007; 102(7): 793-801. http://dx.doi.org/10.1590/S0074-02762007000700003. PMid:18094887.
http://dx.doi.org/10.1590/S0074-02762007...
, using crude antigens of Rickettsia rickettsii strain Taiaçu, Rickettsia parkeri strain At24, Rickettsia amblyommatis strain Ac37, Rickettsia rhipicephali strain HJ5, and Rickettsia bellii strain Mogi. Each Rickettsia strain was cultivated in Vero cells and harvested when nearly 100% of the cells were infected. The infected cells were centrifuged at 4,000 g for 10 min, and pellet was washed in 0.1 M phosphate-buffered saline (PBS), pH 7.4, centrifuged again, and resuspended in PBS containing 1% bovine calf serum and 0.1% sodium azide. Ten microliters of rickettsiae-infected cells were applied onto each of 12 wells on microscopic slides, air-dried, fixed in acetone for 10 min, and stored at -80ºC until used. Feline plasma was diluted in two-fold increments with PBS starting from a 1:64 dilution. Ten microliters of diluted plasma were added to each well of the antigen slides. The slides were incubated at 37ºC for 30 min in a humid chamber. The slides were rinsed once, and then washed twice for 15 min per wash in PBS. The slides were incubated with fluorescein isothiocyanate-labeled goat anti-cat IgG (Sigma, St Louis, USA) from a 1:1,000 dilution, and washed as described earlier. The slides were mounted with buffered glycerin under coverslips. The slides were read using an ultraviolet microscope (Olympus, Tokyo, Japan) at 400x magnification. Plasma was considered to contain antibodies against the rickettsiae if it displayed a reaction at the 1:64 dilution. End-point titers against each Rickettsia strain were determined by testing serial plasma dilutions. In each slide, a serum previously shown to be non-reactive (negative control) and a known reactive cat serum (positive control) were tested (Horta et al., 2007Horta MC, Labruna MB, Pinter A, Linardi PM, Schumaker TTS. Rickettsia infection in five areas of the state of São Paulo, Brazil. Mem Inst Oswaldo Cruz 2007; 102(7): 793-801. http://dx.doi.org/10.1590/S0074-02762007000700003. PMid:18094887.
http://dx.doi.org/10.1590/S0074-02762007...
).

The ticks collected from cats were identified as A. auricularium (24 nymphs, six females, four males) and Amblyomma sp. (42 larvae). The ticks collected from the armadillo burrows were identified as A. auricularium (36 nymphs, six females, and five males) and Amblyomma sp. (26 larvae). The presence of anti-Rickettsia spp. antibodies was detected in all cats: cat#1 reacted to R. amblyommatis (titer 512) and R. rhipicephali (128); cat#2 reacted to R. rickettsii (128), R. amblyommatis (512), and R. rhipicephali (256); and cat#3 reacted to R. amblyommatis (titer 512) and R. rhipicephali (256). Cat#1 showed antibody titers for R. amblyommatis that were at least four-fold higher than those for the other three rickettsial antigens (titer 512), indicating a predominant antibody response to R. amblyommatis or a very closely related genotype.

This study assessed one male and two female healthy adult felines. The three cats had free access to a wooded area where wild animals such as rodents, marsupials, and armadillos were present, and it was possible to visualize and count six empty armadillo burrows near the property. The coexistence of domestic animals with wildlife in forest areas can favor tick infestation, thus facilitating the transmission of pathogens from wild animals to domestic animals and humans (Little et al., 2018Little SE, Barrett AW, Nagamori Y, Herrin BH, Normile D, Heaney K, et al. Ticks from cats in the United States: patterns of infestation and infection with pathogens. Vet Parasitol 2018; 257: 15-20. http://dx.doi.org/10.1016/j.vetpar.2018.05.002. PMid:29907187.
http://dx.doi.org/10.1016/j.vetpar.2018....
).

The A. auricularium tick is a parasite of armadillos (Chlamyphoridae and Dasypodidae), which occur in the Neotropical and Nearctic regions (Guglielmone et al., 2003Guglielmone AA, Estrada-Peña A, Luciani CA, Mangold AJ, Keirans JE. Hosts and distribution of Amblyomma auricularium (Conil 1878) and Amblyomma pseudoconcolor Aragão, 1908 (Acari: ixodidae). Exp Appl Acarol 2003; 29(1-2): 131-139. http://dx.doi.org/10.1023/A:1024251020035. PMid:14580065.
http://dx.doi.org/10.1023/A:102425102003...
). However, despite its moderate specificity for armadillo species such as Dasypus novemcinctus Linnaeus 1758 (Guglielmone et al., 2003Guglielmone AA, Estrada-Peña A, Luciani CA, Mangold AJ, Keirans JE. Hosts and distribution of Amblyomma auricularium (Conil 1878) and Amblyomma pseudoconcolor Aragão, 1908 (Acari: ixodidae). Exp Appl Acarol 2003; 29(1-2): 131-139. http://dx.doi.org/10.1023/A:1024251020035. PMid:14580065.
http://dx.doi.org/10.1023/A:102425102003...
), there are reports of parasitism on other wild animals: Conepatus semistriatus Boddaert, 1785 (Saraiva et al., 2013Saraiva DG, Nieri-Bastos FA, Horta MC, Soares HS, Nicola PA, Pereira LCM, et al. Rickettsia amblyommii infecting Amblyomma auricularium ticks in Pernambuco, Northeastern Brazil: isolation, transovarial transmission, and transstadial perpetuation. Vector Borne Zoonotic Dis 2013; 13(9): 615-618. http://dx.doi.org/10.1089/vbz.2012.1223. PMid:23705586.
http://dx.doi.org/10.1089/vbz.2012.1223...
), Tamandua tetradactyla Linnaeus, 1758 (Costa et al., 2020Costa FB, Martins TF, Muñoz-Leal S, de Azevedo Serpa MC, Ogrzewalska M, Luz HR, et al. Retrospective and new records of ticks (Acari: Argasidae, Ixodidae) from the state of Maranhão, an Amazon-Cerrado transition area of Brazil. Vet Parasitol Reg Stud Rep 2020; 21: 100413. http://dx.doi.org/10.1016/j.vprsr.2020.100413. PMid:32862893.
http://dx.doi.org/10.1016/j.vprsr.2020.1...
), Thrichomys apereoides Lund, 1839, Monodelphis domestica Wagner, 1842, Galea spixii Wagler, 1831 (Horta et al., 2011Horta MC, Nascimento GF, Martins TF, Labruna MB, Machado LCP, Nicola PA. Ticks (Acari: Ixodida) parasitizing free-living wild animals in the Caatinga biome in the State of Pernambuco, northeastern Brazil. Syst Appl Acarol 2011; 16(3): 207-211. http://dx.doi.org/10.11158/saa.16.3.3.
http://dx.doi.org/10.11158/saa.16.3.3...
), Nasua narica Linnaeus, 1766 (Bermúdez et al., 2021Bermúdez S, Martínez-Mandiche J, Dominguez L, Gonzalez C, Chavarria O, Moreno A, et al. Diversity of Rickettsia in ticks collected from wild animals in Panama. Ticks Tick Borne Dis 2021; 12(4): 101723. http://dx.doi.org/10.1016/j.ttbdis.2021.101723. PMid:33857748.
http://dx.doi.org/10.1016/j.ttbdis.2021....
), Thrichomys laurentius Thomas, 1904 (Oliveira et al., 2020Oliveira GMB, Silva IWG, Evaristo AMCF, Serpa MCA, Campos ANS, Dutra V, et al. Tick-borne pathogens in dogs, wild small mammals and their ectoparasites in the semi-arid Caatinga biome, northeastern Brazil. Ticks Tick Borne Dis 2020; 11(4): 101409. http://dx.doi.org/10.1016/j.ttbdis.2020.101409. PMid:32111546.
http://dx.doi.org/10.1016/j.ttbdis.2020....
), Thrichomys inermis Pictet, Monodelphis domestica Wagner, 1842, (Maia et al., 2018Maia MO, Koppe VC, Muñoz-Leal S, Martins TF, Marcili A, Labruna MB, et al. 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 2018; 76(4): 523-535. http://dx.doi.org/10.1007/s10493-018-0323-2. PMid:30443697.
http://dx.doi.org/10.1007/s10493-018-032...
) Lycalopex vetulus Lund 1842, Dicotyles tajacu Lineu, 1758 (Martins et al., 2020Martins TF, Reis JL, Viana EB, Luz HR, Oda FH, Dantas SP, et al. Ticks (Acari: Ixodidae) on captive and free-ranging wild animals in Tocantins State, a Cerrado-Amazon transition region of northern Brazil. Int J Acarol 2020; 46(4): 254-257. http://dx.doi.org/10.1080/01647954.2020.1757756.
http://dx.doi.org/10.1080/01647954.2020....
) various bird species (Lugarini et al., 2015Lugarini C, Martins TF, Ogrzewalska M, de Vasconcelos NCT, Ellis VA, Oliveira JB, et al. Rickettsial agents in avian ixodid ticks in northeast Brazil. Ticks Tick Borne Dis 2015; 6(3): 364-375. http://dx.doi.org/10.1016/j.ttbdis.2015.02.011. PMid:25800099.
http://dx.doi.org/10.1016/j.ttbdis.2015....
). In domestic animals, parasitism has been reported on cattle, dogs, and horses (Guglielmone et al., 2003Guglielmone AA, Estrada-Peña A, Luciani CA, Mangold AJ, Keirans JE. Hosts and distribution of Amblyomma auricularium (Conil 1878) and Amblyomma pseudoconcolor Aragão, 1908 (Acari: ixodidae). Exp Appl Acarol 2003; 29(1-2): 131-139. http://dx.doi.org/10.1023/A:1024251020035. PMid:14580065.
http://dx.doi.org/10.1023/A:102425102003...
). In the present study, we report for the first time the infestation of A. auricularium on domestic cats.

Studies reporting tick parasitism and serological evidence of exposure to Rickettsia spp. in cats are very rare in Brazil because cats are not the primary hosts of any tick species and thus far have no importance in the epidemiological cycle of Rickettsiae. A study carried out by da Silva et al. (2007)Silva AS, Silva MK, Monteiro SG. Parasitismo por Amblyomma triste em gato doméstico. Rev Bras Parasitol Vet 2007; 16(2): 108-109. PMid:17706014. in the state of Rio Grande do Sul reported parasitism of a cat by Amblyomma triste, while Mendes et al. (2019)Mendes JCR, Kmetiuk LB, Martins CM, Canavessi AMO, Jimenez T, Pellizzaro M, et al. Serosurvey of Rickettsia spp. in cats from a Brazilian spotted fever-endemic area. Rev Bras Parasitol Vet 2019; 28(4): 713-721. http://dx.doi.org/10.1590/s1984-29612019092. PMid:31721931.
http://dx.doi.org/10.1590/s1984-29612019...
reported parasitism by Amblyomma sculptum in the state of Rio de Janeiro; however, no diagnosis was made to prove exposure to agents from the Rickettsiae group.

In a previous study conducted in the same region as the present study, Saraiva et al. (2013)Saraiva DG, Nieri-Bastos FA, Horta MC, Soares HS, Nicola PA, Pereira LCM, et al. Rickettsia amblyommii infecting Amblyomma auricularium ticks in Pernambuco, Northeastern Brazil: isolation, transovarial transmission, and transstadial perpetuation. Vector Borne Zoonotic Dis 2013; 13(9): 615-618. http://dx.doi.org/10.1089/vbz.2012.1223. PMid:23705586.
http://dx.doi.org/10.1089/vbz.2012.1223...
demonstrated the infection and vectorial competence of A. auricularium to R. amblyommatis. In this study, we confirmed, for the first time, the exposure of cats to the spotted fever group Rickettsiae, likely R. amblyommatis, using IFA. Generally, studies that detect anti-Rickettsia antibodies included included dogs, horses, ruminants, or wild animals, and those dealing with domestic cats in Brazil are scarce. Studies from other countries have reported Rickettsiae in cats and ticks, highlighting their epidemiological importance (Hiraoka et al., 2005Hiraoka H, Shimada Y, Sakata Y, Watanabe M, Itamoto K, Okuda M, et al. Detection of Rickettsial DNA in ixodid ticks recovered from dogs and cats in Japan. J Vet Med Sci 2005; 67(12): 1217-1222. http://dx.doi.org/10.1292/jvms.67.1217. PMid:16397379.
http://dx.doi.org/10.1292/jvms.67.1217...
; Case et al., 2006Case JB, Chomel B, Nicholson W, Foley JE. Serological survey of vector-borne zoonotic pathogens in pet cats and cats from animal shelters and feral colonies. J Feline Med Surg 2006; 8(2): 111-117. http://dx.doi.org/10.1016/j.jfms.2005.10.004. PMid:16434226.
http://dx.doi.org/10.1016/j.jfms.2005.10...
; Segura et al., 2014Segura F, Pons I, Miret J, Pla J, Ortuño A, Nogueras MM. The role of cats in the eco-epidemiology of spotted fever group diseases. Parasit Vectors 2014; 7: 353. http://dx.doi.org/10.1186/1756-3305-7-353. PMid:25084969.
http://dx.doi.org/10.1186/1756-3305-7-35...
; Little et al., 2018Little SE, Barrett AW, Nagamori Y, Herrin BH, Normile D, Heaney K, et al. Ticks from cats in the United States: patterns of infestation and infection with pathogens. Vet Parasitol 2018; 257: 15-20. http://dx.doi.org/10.1016/j.vetpar.2018.05.002. PMid:29907187.
http://dx.doi.org/10.1016/j.vetpar.2018....
).

Lopes et al. (2018)Lopes MG, Muñoz-Leal S, Lima JTR, Fournier GFSR, Acosta ICL, Martins TF, et al. Ticks, rickettsial and erlichial infection in small mammals from Atlantic Forest remnants in northeastern Brazil. Int J Parasitol Parasites Wildl 2018; 7(3): 380-385. http://dx.doi.org/10.1016/j.ijppaw.2018.10.001. PMid:30370217.
http://dx.doi.org/10.1016/j.ijppaw.2018....
and Oliveira et al. (2020)Oliveira GMB, Silva IWG, Evaristo AMCF, Serpa MCA, Campos ANS, Dutra V, et al. Tick-borne pathogens in dogs, wild small mammals and their ectoparasites in the semi-arid Caatinga biome, northeastern Brazil. Ticks Tick Borne Dis 2020; 11(4): 101409. http://dx.doi.org/10.1016/j.ttbdis.2020.101409. PMid:32111546.
http://dx.doi.org/10.1016/j.ttbdis.2020....
reported the presence of anti-R. amblyommatis antibodies in Didelphis albiventris and Rattus rattus. Here, we found anti- R. amblyommatis antibodies in domestic cats, thus suggesting the likely circulation of R. amblyommatis in both wild and domestic animals. R. amblyommatis, initially considered a non-pathogenic bacterium for humans, has already been considered a possible human pathogen based on serological evidence of human infection in the United States (Apperson et al., 2008Apperson CS, Engber B, Nicholson WL, Mead DG, Engel J, Yabsley MJ, et al. Tick-Borne Diseases in North Carolina: is “Rickettsia amblyommii” a possible cause of rickettsiosis reported as Rocky Mountain Spotted Fever? Vector Borne Zoonotic Dis 2008; 8(5): 597-606. http://dx.doi.org/10.1089/vbz.2007.0271. PMid:18447622.
http://dx.doi.org/10.1089/vbz.2007.0271...
).

In Brazil, there are at least two distinct reports of A. auricularium parasitism on humans (Lopes et al., 2018Lopes MG, Muñoz-Leal S, Lima JTR, Fournier GFSR, Acosta ICL, Martins TF, et al. Ticks, rickettsial and erlichial infection in small mammals from Atlantic Forest remnants in northeastern Brazil. Int J Parasitol Parasites Wildl 2018; 7(3): 380-385. http://dx.doi.org/10.1016/j.ijppaw.2018.10.001. PMid:30370217.
http://dx.doi.org/10.1016/j.ijppaw.2018....
; Szabó et al., 2020Szabó MPJ, Martins TF, Barbieri ARM, Costa FB, Soares HS, Tolesano-Pascoli GV, et al. Ticks biting humans in the Brazilian savannah: attachment sites and exposure risk in relation to species, life stage and season. Ticks Tick Borne Dis 2020; 11(2): 101328. http://dx.doi.org/10.1016/j.ttbdis.2019.101328. PMid:31767495.
http://dx.doi.org/10.1016/j.ttbdis.2019....
). As a result, the true zoonotic potential of these findings remains unclear. However, it underscores the importance of implementing epidemiological surveillance to monitor the prevalence of this spotted fever group Rickettsiae and its vector in the region, using felines with free access to forest areas and hunting habits as sentinels for this pathogen.

The study reports for the first time the infestation of nymphs and adults of A. auricularium on domestic cats in a new area of occurrence in the semi-arid region of Northeast. Additionally, the study also focused on the detection of anti-Rickettsia spp. antibodies in parasitized cats, with R. amblyommatis identified as the probable infectious agent.

Acknowledgements

To the Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) for granting the postgraduate scholarship (IBPG-0404-5.05/22) to Ila Farias; to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for Scientific Productivity Grant to MBL and MCH (grant number: 301641/2019-6 and 314019/2021-9, respectively).

  • How to cite: Farias IF, Oliveira GMB, Lima EVM, Labruna MB, Horta MC. Parasitism on domestic cats by Amblyomma auricularium and serological evidence of exposure to Rickettsia amblyommatis. Braz J Vet Parasitol 2024; 33(1): e018123. https://doi.org/10.1590/S1984-29612024015

References

  • André MR, Denardi NCB, Sousa KCM, Gonçalves LR, Henrique PC, Ontivero CRGR, et al. Arthropod-borne pathogens circulating in free-roaming domestic cats in a zoo environment in Brazil. Ticks Tick Borne Dis 2014; 5(5): 545-551. http://dx.doi.org/10.1016/j.ttbdis.2014.03.011 PMid:24889035.
    » http://dx.doi.org/10.1016/j.ttbdis.2014.03.011
  • André MR, Filgueira KD, Calchi AC, Sousa KCM, Gonçalves LR, Medeiros VB, et al. Co-infection with arthropod-borne pathogens in domestic cats. Rev Bras Parasitol Vet 2017; 26(4): 525-531. http://dx.doi.org/10.1590/s1984-29612017064 PMid:29160357.
    » http://dx.doi.org/10.1590/s1984-29612017064
  • André MR, Herrera HM, Fernandes SJ, Sousa KCM, Gonçalves LR, Domingos IH, et al. Tick-borne agents in domesticated and stray cats from the city of Campo Grande, state of Mato Grosso do Sul, midwestern Brazil. Ticks Tick Borne Dis 2015; 6(6): 779-786. http://dx.doi.org/10.1016/j.ttbdis.2015.07.004 PMid:26187416.
    » http://dx.doi.org/10.1016/j.ttbdis.2015.07.004
  • Apperson CS, Engber B, Nicholson WL, Mead DG, Engel J, Yabsley MJ, et al. Tick-Borne Diseases in North Carolina: is “Rickettsia amblyommii” a possible cause of rickettsiosis reported as Rocky Mountain Spotted Fever? Vector Borne Zoonotic Dis 2008; 8(5): 597-606. http://dx.doi.org/10.1089/vbz.2007.0271 PMid:18447622.
    » http://dx.doi.org/10.1089/vbz.2007.0271
  • Barros-Battesti DM, Arzua M, Bechara GH. Carrapatos de importância médico-veterinária da região neotropical: um guia ilustrado para identificação de espécies 1. ed. São Paulo: Vox/ICTTD-3/Butantan; 2006.
  • Bermúdez S, Martínez-Mandiche J, Dominguez L, Gonzalez C, Chavarria O, Moreno A, et al. Diversity of Rickettsia in ticks collected from wild animals in Panama. Ticks Tick Borne Dis 2021; 12(4): 101723. http://dx.doi.org/10.1016/j.ttbdis.2021.101723 PMid:33857748.
    » http://dx.doi.org/10.1016/j.ttbdis.2021.101723
  • Case JB, Chomel B, Nicholson W, Foley JE. Serological survey of vector-borne zoonotic pathogens in pet cats and cats from animal shelters and feral colonies. J Feline Med Surg 2006; 8(2): 111-117. http://dx.doi.org/10.1016/j.jfms.2005.10.004 PMid:16434226.
    » http://dx.doi.org/10.1016/j.jfms.2005.10.004
  • Costa FB, Martins TF, Muñoz-Leal S, de Azevedo Serpa MC, Ogrzewalska M, Luz HR, et al. Retrospective and new records of ticks (Acari: Argasidae, Ixodidae) from the state of Maranhão, an Amazon-Cerrado transition area of Brazil. Vet Parasitol Reg Stud Rep 2020; 21: 100413. http://dx.doi.org/10.1016/j.vprsr.2020.100413 PMid:32862893.
    » http://dx.doi.org/10.1016/j.vprsr.2020.100413
  • Dantas-Torres F, Otranto D. Dogs, cats, parasites, and humans in Brazil: opening the black box. Parasit Vectors 2014; 7(1): 22. http://dx.doi.org/10.1186/1756-3305-7-22 PMid:24423244.
    » http://dx.doi.org/10.1186/1756-3305-7-22
  • Ferreira DRA, Alves LC, Faustino MAG. Ectoparasitos de Felis catus domesticus (Linnaeus, 1758) na cidade de João Pessoa, Paraíba, Brasil. Biotemas 2010; 23(4): 43-50. http://dx.doi.org/10.5007/2175-7925.2010v23n4p43
    » http://dx.doi.org/10.5007/2175-7925.2010v23n4p43
  • Guglielmone AA, Estrada-Peña A, Luciani CA, Mangold AJ, Keirans JE. Hosts and distribution of Amblyomma auricularium (Conil 1878) and Amblyomma pseudoconcolor Aragão, 1908 (Acari: ixodidae). Exp Appl Acarol 2003; 29(1-2): 131-139. http://dx.doi.org/10.1023/A:1024251020035 PMid:14580065.
    » http://dx.doi.org/10.1023/A:1024251020035
  • Hiraoka H, Shimada Y, Sakata Y, Watanabe M, Itamoto K, Okuda M, et al. Detection of Rickettsial DNA in ixodid ticks recovered from dogs and cats in Japan. J Vet Med Sci 2005; 67(12): 1217-1222. http://dx.doi.org/10.1292/jvms.67.1217 PMid:16397379.
    » http://dx.doi.org/10.1292/jvms.67.1217
  • Horta MC, Labruna MB, Pinter A, Linardi PM, Schumaker TTS. Rickettsia infection in five areas of the state of São Paulo, Brazil. Mem Inst Oswaldo Cruz 2007; 102(7): 793-801. http://dx.doi.org/10.1590/S0074-02762007000700003 PMid:18094887.
    » http://dx.doi.org/10.1590/S0074-02762007000700003
  • Horta MC, Nascimento GF, Martins TF, Labruna MB, Machado LCP, Nicola PA. Ticks (Acari: Ixodida) parasitizing free-living wild animals in the Caatinga biome in the State of Pernambuco, northeastern Brazil. Syst Appl Acarol 2011; 16(3): 207-211. http://dx.doi.org/10.11158/saa.16.3.3
    » http://dx.doi.org/10.11158/saa.16.3.3
  • Little SE, Barrett AW, Nagamori Y, Herrin BH, Normile D, Heaney K, et al. Ticks from cats in the United States: patterns of infestation and infection with pathogens. Vet Parasitol 2018; 257: 15-20. http://dx.doi.org/10.1016/j.vetpar.2018.05.002 PMid:29907187.
    » http://dx.doi.org/10.1016/j.vetpar.2018.05.002
  • Lopes MG, Muñoz-Leal S, Lima JTR, Fournier GFSR, Acosta ICL, Martins TF, et al. Ticks, rickettsial and erlichial infection in small mammals from Atlantic Forest remnants in northeastern Brazil. Int J Parasitol Parasites Wildl 2018; 7(3): 380-385. http://dx.doi.org/10.1016/j.ijppaw.2018.10.001 PMid:30370217.
    » http://dx.doi.org/10.1016/j.ijppaw.2018.10.001
  • Lugarini C, Martins TF, Ogrzewalska M, de Vasconcelos NCT, Ellis VA, Oliveira JB, et al. Rickettsial agents in avian ixodid ticks in northeast Brazil. Ticks Tick Borne Dis 2015; 6(3): 364-375. http://dx.doi.org/10.1016/j.ttbdis.2015.02.011 PMid:25800099.
    » http://dx.doi.org/10.1016/j.ttbdis.2015.02.011
  • Maia MO, Koppe VC, Muñoz-Leal S, Martins TF, Marcili A, Labruna MB, et al. 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 2018; 76(4): 523-535. http://dx.doi.org/10.1007/s10493-018-0323-2 PMid:30443697.
    » http://dx.doi.org/10.1007/s10493-018-0323-2
  • 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(2): 75-99. http://dx.doi.org/10.1016/j.ttbdis.2010.03.002 PMid:21771514.
    » http://dx.doi.org/10.1016/j.ttbdis.2010.03.002
  • Martins TF, Reis JL, Viana EB, Luz HR, Oda FH, Dantas SP, et al. Ticks (Acari: Ixodidae) on captive and free-ranging wild animals in Tocantins State, a Cerrado-Amazon transition region of northern Brazil. Int J Acarol 2020; 46(4): 254-257. http://dx.doi.org/10.1080/01647954.2020.1757756
    » http://dx.doi.org/10.1080/01647954.2020.1757756
  • Mendes JCR, Kmetiuk LB, Martins CM, Canavessi AMO, Jimenez T, Pellizzaro M, et al. Serosurvey of Rickettsia spp. in cats from a Brazilian spotted fever-endemic area. Rev Bras Parasitol Vet 2019; 28(4): 713-721. http://dx.doi.org/10.1590/s1984-29612019092 PMid:31721931.
    » http://dx.doi.org/10.1590/s1984-29612019092
  • Mendes-de-Almeida F, Crissiuma AL, Gershony LC, Willi LMV, Paiva JP, Guerrero J, et al. Characterization of ectoparasites in an urban cat (Felis catus Linnaeus, 1758) population of Rio de Janeiro, Brazil. Parasitol Res 2011; 108(6): 1431-1435. http://dx.doi.org/10.1007/s00436-010-2189-z PMid:21181196.
    » http://dx.doi.org/10.1007/s00436-010-2189-z
  • Oliveira GMB, Silva IWG, Evaristo AMCF, Serpa MCA, Campos ANS, Dutra V, et al. Tick-borne pathogens in dogs, wild small mammals and their ectoparasites in the semi-arid Caatinga biome, northeastern Brazil. Ticks Tick Borne Dis 2020; 11(4): 101409. http://dx.doi.org/10.1016/j.ttbdis.2020.101409 PMid:32111546.
    » http://dx.doi.org/10.1016/j.ttbdis.2020.101409
  • Oliveira LS, Mourão LC, Oliveira KA, da Matta Agostini M, Oliveira AC, Almeida MR, et al. Molecular detection of Ehrlichia canis in cats in Brazil. Clin Microbiol Infect 2009; 15(Suppl 2): 53-54. http://dx.doi.org/10.1111/j.1469-0691.2008.02175.x PMid:19374643.
    » http://dx.doi.org/10.1111/j.1469-0691.2008.02175.x
  • Pesqueira TR, Martins GFS, Farias IF, Evaristo AMCF, Sento Sé FS, Oliveira FRB, et al. Diagnóstico molecular de agentes parasitários e coronavírus em gatos no Nordeste do Brasil. Braz J Global Health 2023; 3(10): 1-7. http://dx.doi.org/10.56242/globalhealth;;2023;3;10;1-7
    » http://dx.doi.org/10.56242/globalhealth;;2023;3;10;1-7
  • Saraiva DG, Nieri-Bastos FA, Horta MC, Soares HS, Nicola PA, Pereira LCM, et al. Rickettsia amblyommii infecting Amblyomma auricularium ticks in Pernambuco, Northeastern Brazil: isolation, transovarial transmission, and transstadial perpetuation. Vector Borne Zoonotic Dis 2013; 13(9): 615-618. http://dx.doi.org/10.1089/vbz.2012.1223 PMid:23705586.
    » http://dx.doi.org/10.1089/vbz.2012.1223
  • Segura F, Pons I, Miret J, Pla J, Ortuño A, Nogueras MM. The role of cats in the eco-epidemiology of spotted fever group diseases. Parasit Vectors 2014; 7: 353. http://dx.doi.org/10.1186/1756-3305-7-353 PMid:25084969.
    » http://dx.doi.org/10.1186/1756-3305-7-353
  • Silva AS, Silva MK, Monteiro SG. Parasitismo por Amblyomma triste em gato doméstico. Rev Bras Parasitol Vet 2007; 16(2): 108-109. PMid:17706014.
  • Szabó MPJ, Martins TF, Barbieri ARM, Costa FB, Soares HS, Tolesano-Pascoli GV, et al. Ticks biting humans in the Brazilian savannah: attachment sites and exposure risk in relation to species, life stage and season. Ticks Tick Borne Dis 2020; 11(2): 101328. http://dx.doi.org/10.1016/j.ttbdis.2019.101328 PMid:31767495.
    » http://dx.doi.org/10.1016/j.ttbdis.2019.101328

Publication Dates

  • Publication in this collection
    18 Mar 2024
  • Date of issue
    2024

History

  • Received
    07 Nov 2023
  • Accepted
    25 Jan 2024
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
E-mail: cbpv_rbpv.fcav@unesp.br