Hemoparasites in Didelphis aurita from Seropédica, Rio de Janeiro State, Brazil

Authors

DOI:

https://doi.org/10.5433/1679-0359.2022v43n6p2403

Keywords:

Marsupial, Theileria, Ticks, Fleas, Vector-borne.

Abstract

The present study aimed to use polymerase chain reaction (PCR) to detect species of the order Piroplasmida, such as Anaplasma spp., Borrelia spp., and Ehrlichia spp., circulating in the blood of Didelphis aurita in a peridomiciliary environment. Blood samples collected from big-eared opossum (Didelphis aurita) were screened for hemoparasites using PCR. The extracted DNA was tested for tick-borne hemoparasites. We were unable to detect hemoparasites, such as Ehrlichia spp., Babesia spp., Anaplasma spp., and Borrelia spp. Theileria DNA was detected in only one sample screened using PCR for an approximately 650-base pair fragment of the 18S rRNA gene. Sequencing and BLAST analysis of a subset of the PCR amplicons revealed 97% (535/553 bp) identity with Theileria bicornis. The detection of Theileria sp. in D. aurita challenges us to pursue more in-depth studies of marsupial piroplasmosids and to evaluate the morphological aspects of the findings and their possible involvement in zoonoses.

Downloads

Download data is not yet available.

Author Biographies

Matheus Dias Cordeiro, Universidade Federal Rural do Rio de Janeiro

Researcher of the Post-Graduate Program in Practice in Sustainable Development, Universidade Federal do Rio de Janeiro, UFRRJ, Seropédica, RJ, Brazil.

Izabela Mesquita Araújo, Universidade Federal Rural do Rio de Janeiro

Researcher of the Post-Graduate Program in Veterinary Sciences, UFRRJ, Seropédica, RJ, Brazil.

Claúdia Bezerra da Silva, Universidade Federal Rural do Rio de Janeiro

Researcher of the Post-Graduate Program in Veterinary Sciences, UFRRJ, Seropédica, RJ, Brazil.

Alexandro Guterres, Instituto Oswaldo Cruz

Researcher of the Laboratory of Hantaviruses and Rickettsiosis of Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, RJ, Brazil.

Adivaldo Henrique da Fonseca, Universidade Federal Rural do Rio de Janeiro

Researcher of the Post-Graduate Program in Veterinary Sciences, UFRRJ, Seropédica, RJ, Brazil.

Bruna de Azevedo Baêta, Universidade Federal Rural do Rio de Janeiro

Researcher of the Post-Graduate Program in Veterinary Sciences, UFRRJ, Seropédica, RJ, Brazil.

References

Almeida, A. P., Souza, T. D., Marcili, A., & Labruna, M. B. (2013). Novel Ehrlichia and Hepatozoon agents infecting thecrab-eating fox (Cerdocyon thous) in southeastern Brazil. Journal of Medical Entomology, 50(3), 640-646. doi: 10.1603/me12272 DOI: https://doi.org/10.1603/ME12272

Birkenheuer, A. J., Levy, M. G., & Breitschwerdt, E. B. (2003). Development and evaluation of a seminested PCR for detection and differentiation of Babesia gibsoni (Asian genotype) and B. canis DNA in canine blood samples. Journal of Clinical Microbiology, 41(9), 4172-4177. doi: 10.1128/JCM.41.9.4172-4177. 2003 DOI: https://doi.org/10.1128/JCM.41.9.4172-4177.2003

Blanco, C. M., Teixeira, B. R., Silva, A. G. da, Oliveira, R. C. de, Strecht, L., Ogrzewalska, M., & Lemos, E. R. S. de. (2017). Microorganisms in ticks (Acari: Ixodidae) collected on marsupials and rodents from Santa Catarina, Paraná and Mato Grosso do Sul states, Brazil. Ticks Tick-Borne Diseases, 8(1), 90-98. doi: 10.1016/j.ttbdis.2016.10.003 DOI: https://doi.org/10.1016/j.ttbdis.2016.10.003

Cáceres, N. C. (2012). Os marsupiais do Brasil: biologia, ecologia e conservação. Editora UFMS.

Colle, A. C., Mendonça F. B. R. de, Maia, M. O., Freitas, L. C., Witter, R., Marcili, A., Aguiar, D. M., Muñoz-Leal, M., Labruna, M. B., Rossi, R. V., & Pacheco, R. C. (2019). Molecular survey of tick-borne pathogens in small mammals from Brazilian Amazonia. Revista Brasileira de Parasitologia Veterinária, 28(4), 592-604. doi: 10.1590/S1984-29612019086 DOI: https://doi.org/10.1590/s1984-29612019086

Dantas-Torres, F. (2008). Canine vector-borne diseases in Brazil. Parasites and Vectors, 1(25), 1-17. doi: 10. 1186/1756-3305-1-25 DOI: https://doi.org/10.1186/1756-3305-1-25

Dantas-Torres, F., Aléssio, F., Siqueira, D., Mauffrey, J., Marvulo, M., Martins, T., & Silva, J. (2012). Exposure of small mammals to ticks and rickettsiae in Atlantic Forest patches in the metropolitan area of Recife, North-eastern Brazil. Parasitology, 139(1), 83-91. doi: 10.1017/S0031182011001740 DOI: https://doi.org/10.1017/S0031182011001740

Dantas-Torres, F., & Otranto, D. (2016). Best practices for preventing vector-borne diseases in dogs and humans. Trends in Parasitology, 32(1), 43-55. doi: 10.1016/j.pt.2015.09.004 DOI: https://doi.org/10.1016/j.pt.2015.09.004

Dubey, J. P., Lindsay, D. S., Saville, W. J., Reed, S. M., Granstrom, D. E., & Speer, C. A. (2001). A review of Sarcocystis neurona and equine protozoal myeloencephalitis (EPM). Veterinary Parasitology, 95(2-4), 89-131. doi: 10.1016/s0304-4017(00)00384-8 DOI: https://doi.org/10.1016/S0304-4017(00)00384-8

Gonçalves, L. R., Paludo, G., Bisol, T. B., Perles, L., Oliveira, L. B. de, Oliveira, C. M. Silva, T. M. V., Nantes, W. A. G., Duarte, M. A., Santos, F. M. Porfírio, G. E. O., Hirano, L. Q. L., Herrera, H. M., Barros-Battesti, D. M., Machado, R. Z., & André, M. R. (2021). Molecular detection of piroplasmids in synanthropic rodents, marsupials, and associated ticks from Brazil, with phylogenetic inference of a putative novel Babesia sp. from white-eared opossum (Didelphis albiventris). Parasitology Research, 120(1), 3537-3546. doi: 10.1007/s00436-021-07284-8 DOI: https://doi.org/10.1007/s00436-021-07284-8

Gouy, M., Tannier, E., Comte, N., & Parsons, D. P. (2021). Seaview version 5: a multiplatform software for multiple sequence alignment, molecular phylogenetic analyses, and tree reconciliation. Methods in Molecular Biology, 2231(1), 241-260. doi: 10.1007/978-1-0716-1036-7_15 DOI: https://doi.org/10.1007/978-1-0716-1036-7_15

Guimarães, A., Raimundo, J. M., Silva, A. T., Carpintero, F. M., Pires, J. R., Benevenute, J. L., Machado, R. Z., André, M. R., & Baldani, C. D. (2019). Detection of a putative novel genotype of Ehrlichia sp. from opossums (Didelphis aurita) from Brazil. Revista Brasileira de Parasitologia Veterinária, 28(1), 140-144. doi: 10.1590/S1984-296120180068 DOI: https://doi.org/10.1590/s1984-296120180068

Guitton, N., Araújo, N. A., F., & Sherlock, Í. R. D. A. (1986). Ectoparasitas de roedores e marsupiais no ambiente silvestre da Ilha Grande, Estado do Rio de Janeiro, Brasil. Memórias do Instituto Oswaldo Cruz, 81(2), 233-234. doi: 10.1590/S0074-02761986000200014 DOI: https://doi.org/10.1590/S0074-02761986000200014

Horta, M. C., Moraes, J., Casagrande, R. A., Saito, T. B., Rosa, S. C., Ogrzewalska, M., Matushima, E. R., & Labruna, M. B. (2009). Experimental infection of opossums Didelphis aurita by rickettsia rickettsii and evaluation of the transmission of the infection to ticks Amblyomma cajennense. Vector-Borne and Zoonotic Diseases, 9(1), 109-117. doi: 10.1089/vbz.2008.0114 DOI: https://doi.org/10.1089/vbz.2008.0114

Horta, M. C., Sabatini, G. S., Moraes, J., Fº., Ogrzewalska, M., Canal, R. B., Pacheco, R. C., Martins, T. F., Matushima, E. R., Labruna, M. B., & Moraes, J., Fº. (2010). Experimental infection of the opossum Didelphis aurita by Rickettsia felis, Rickettsia bellii, and Rickettsia parkeri and evaluation of the transmission of the infection to ticks Amblyomma cajennense and Amblyomma dubitatum. Vector-Borne and Zoonotic Diseases, 10(10), 959-967. doi: 10.1089/vbz.2009.0149 DOI: https://doi.org/10.1089/vbz.2009.0149

Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772-780. doi: 10.1093/molbev/ mst010 DOI: https://doi.org/10.1093/molbev/mst010

Krawczak, F., Nieri-Bastos, F. A., Nunes, F., Soares, J. P. G., Moraes, J., Fº., & Labruna, M. B. (2014). Rickettsial infection in Amblyomma cajennense ticks and capybaras (Hydrochoerus hydrochaeris) in a Brazilian spotted fever-endemic area. Parasites & Vectors, 7(7), 1-7. doi: 10.1186/1756-3305-7-7 DOI: https://doi.org/10.1186/1756-3305-7-7

Labruna, M. B., Kerber, C. E., Ferreira, F., Faccini, J. L. H., De Waal, D. T., & Gennari, S. M. (2001). Risk factors to tick infestations and their occurrence on horses in the state of São Paulo, Brazil. Veterinary Parasitology, 97(1), 1-14. doi: 10.1016/s0304-4017(01)00387-9 DOI: https://doi.org/10.1016/S0304-4017(01)00387-9

Linardi, P. M. & Guimarães, L. R. (2000). Sifonápteros do Brasil. São Paulo, Museu de Zoologia da USP/Fapesp.

Maia, M. O., Koppe, V. C., Muñoz-Leal, S., Martins, T. F., Marcili, A., Labruna, M. B., & Pacheco, R. C. (2018). Detection of Rickettsia spp. in ticks associated to wild mammals in Northeastern Brazil, with notes on an undetermined Ornithodoros sp. collected from marsupials. Experimental Applied Acarolology, 76(4), 523-535. doi: 10.1007/s10493-018-0323-2 DOI: https://doi.org/10.1007/s10493-018-0323-2

Martins, T. F., Onofrio, V. C., Barros-Battesti, D. M., & Labruna, M. B. (2010). Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key. Ticks and Tick-Borne Diseases, 1(2), 75-99. doi: 10.1016/j.ttbdis.2010.03.002 DOI: https://doi.org/10.1016/j.ttbdis.2010.03.002

Massung, R. F., Slater, K., Owens, J. H., Nicholson, W. L., Mather, T. N., Solberg, V. B., & Olson, J. G. (1998). Nested PCR assay for detection of granulocytic ehrlichiae. Journal of Clinical Microbiology, 36(4), 1090-1095. doi: 10.1128/JCM.36.4.1090-1095.1998 DOI: https://doi.org/10.1128/JCM.36.4.1090-1095.1998

McFarlane, R., Sleigh, A., & McMichael, T. (2012). Synanthropy of wild mammals as a determinant of emerging infectious diseases in the Asian-Australasian Region. EcoHealth, 9(1), 24-35. doi: 10.1007/s 10393-012-0763-9 DOI: https://doi.org/10.1007/s10393-012-0763-9

Mendonça, R. F. B., Colle, A. C., Freitas, L. C., Martins, T. F., Horta, M. C., Oliveira, G. M. B., Pacheco, R. C., Mateus, L. A. F., & Rossi, R. V. (2020). Ectoparasites of small mammals in a fragmented area of the southern Amazonia: interaction networks and correlations with seasonality and host sex. Experimental Applied Acarology, 81(1), 117-134. doi: doi: 10.1007/s10493-020-00491-5 DOI: https://doi.org/10.1007/s10493-020-00491-5

Milagres, B. S., Padilha, A. F., Barcelos, R. M., Gomes, G. G., Montandon, C. E., Pena, D. C. H., Bastos, F. A. N., Silveira, I., Pacheco, R., Labruna, M. B., Bouyer, D. H., Freitas, R. N., Walker, D. H., Mafra, C. L., & Galvao, M. A. M. (2010). Rickettsia in synanthropic and domestic animals and their hosts from two areas of low endemicity for brazilian spotted fever in the eastern region of Minas Gerais, Brazil. American Journal Tropical Medicine and Hygiene, 83(6), 1305-1307. doi: 10.4269/ajtmh.2010.10-0239 DOI: https://doi.org/10.4269/ajtmh.2010.10-0239

Müller, G., Brum, J., Langone, P., Michels, G., & Pesenti, T. (2005). Amblyomma aureolatum (Acari: Ixodidae) parasitizing Didelphis albiventris (Marsupialia: Didelphidae) in the state of Rio Grande do Sul. Arquivo do Instituto de Biologia, 72(1), 115-116. doi: 10.1590/1808-1657v72p1152005 DOI: https://doi.org/10.1590/1808-1657v72p1152005

Paparini, A., Ryan, U. M., Warren, K., McInnes, L. M., Tores, P. de, & Irwin, P. J. (2012). Identification of novel Babesia and Theileria genotypes in the endangered marsupials, the woylie (Bettongia penicillata ogilbyi) and boodie (Bettongia lesueur). Experimental Parasitology, 131(1), 25-30. doi: 10.1016/j. exppara 2012.02.021 DOI: https://doi.org/10.1016/j.exppara.2012.02.021

Reck, J., Souza, U., Souza, G., Kieling, E., Dall'Agnol, B., Webster, A., Michel, T., Doyle, R., Martins, T. F., Labruna, M. B., Marks, F., Ott, R., & Martins, J. R. (2018). Records of ticks on humans in Rio Grande do Sul state, Brazil. Ticks and Tick-Borne Diseases, 9(5), 1296-1301. 10.1016/j.ttbdis.2018.05.010 DOI: https://doi.org/10.1016/j.ttbdis.2018.05.010

Regendanz, P., & Kikuth, W. (1928). Sur un parasite du sang des quica (Metachirus quica), Nuttallia brasiliensis n. sp., et influence de la rate sur les infections latentes du sang. Comptes Rendus des Séances et Mémoires de la Société de Biologie, 98(1), 1567-1569.

Reichenow, E. (1953). Doflein's lehrbuch der protozoenkunde. (6a ed). Fisher, Jena.

Reis, F. S., Barros, M. C., Fraga, E. D. C., Penha, T. A. da, Teixeira, W. C., Santos, A. C. G. dos, & Cassia, R. M. S. (2008). Ectoparasitos de pequenos mamíferos silvestres de áreas adjacentes ao rio Itapecuru e área de preservação ambiental do Inhamum, estado do Maranhão, Brasil. Revista Brasileira de Parasitologia Veterinária, 17(1), 69-74. https://www.redalyc.org/articulo.oa?id=397841469014

Reis, N. R., Peracchi, A. L., Fregonezi, M. N., & Rossaneis, B. K. (Orgs.). (2010). Mamíferos do Brasil: guia de identificação. Technical Books.

Sampaio, M. X., & Massard, C. L. (2003). Nuttallia brasiliensis e Theileria brasiliensis, sinonímias de Babesia brasiliensis (Piroplasmida: Babesiidae) hemoparasito de marsupiais Didelphidae. Parasitología Latino-Americana, 58(1-2), 89-91. doi: 10.4067/S0717-77122003000100018 DOI: https://doi.org/10.4067/S0717-77122003000100018

Sanger, F., Nicklen, S., & Coulson, A. R. (1977). DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Science, 74(12), 5463-7. doi: 10.1073/pnas.74.12.5463 DOI: https://doi.org/10.1073/pnas.74.12.5463

Seo, M. G., Yun, S. H., Choi, S.-K., Cho, G.-J., Park, Y.-S., Cho, K.-H., & Kwak, D. (2013). Molecular and phylogenetic analysis of equine piroplasms in the Republic of Korea. Research Veterinary Science, 94(3), 579-583. doi: 10.1016/j.rvsc.2013.01.014 DOI: https://doi.org/10.1016/j.rvsc.2013.01.014

Silva, M. R., Fornazari, L. F.. Demoner, L. C.. Teixeira, C. R., Langoni, H. & O’Dwyer, L. H. Didelphis albiventris naturally infected with Hepatozoon canis in southeastern Brazil. Ticks and Tick-borne Diseases, 8(6), 878-881, 2017. doi: 10.1016/j.ttbdis.2017.07.005 DOI: https://doi.org/10.1016/j.ttbdis.2017.07.005

Soares, H. S., Marcili, A., Barbieri, A. R. M., Minervino, A. H. H., Moreira, T. R., Gennari, S. M., & Labruna, M. B. (2017). Novel piroplasmid and Hepatozoon organisms infecting the wildlife of two regions of the Brazilian Amazon. International Journal for Parasitology: Parasites Wild Life, 6(2), 115-121. doi: 10. 1016/j.ijppaw.2017.05.002 DOI: https://doi.org/10.1016/j.ijppaw.2017.05.002

Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38(7), 3022-3027. doi: 10.1093/molbev/msab120 DOI: https://doi.org/10.1093/molbev/msab120

Ueno, T. E. H., Cutolo, T. A. A., Martins, T. F., Moraes, J., F., Azevedo, S. S., & Labruna, M. B. (2020). Rickettsial infection in equids, opossums and ticks in the municipality of Monte Mor, state of São Paulo, Brazil. Revista Brasileira de Parasitologia Veterinária, 29(4), e015420. doi: 10.1590/S1984-296120200 73 DOI: https://doi.org/10.1590/s1984-29612020073

Wolf, R. W., Aragona, M., Muñoz-Leal, S., Pinto, L. B., Melo, A. L. T., Braga, I. A., Costa, J. S., Martins, T. F., Marcili, A., Pacheco, R. C., Labruna, M. B., & Aguiar, D. M. (2016). Novel Babesia and Hepatozoon agents infecting non-volant small mammals in the Brazilian Pantanal, with the first record of the tick Ornithodoros guaporensis in Brazil. Ticks and Tick-borne Diseases, 7(3), 449-456. doi: 10.1016/j.ttbdis. 2016 01.005 DOI: https://doi.org/10.1016/j.ttbdis.2016.01.005

Yoshinari, N. H., Mantovani, E., Bonoldi, V. L., Marangoni, R. G., & Gauditano, G. (2010). Brazilian Lyme-like disease or Baggio-Yoshinari syndrome: exotic and emerging Brazilian tick-borne zoonosis. Revista da Associação de Medicina Brasileira, 56(3), 363-369. doi: 10.1590/s0104-4230201000030 DOI: https://doi.org/10.1590/S0104-42302010000300025

Downloads

Published

2022-11-29

How to Cite

Cordeiro, M. D., Araújo, I. M., Silva, C. B. da, Guterres, A., Fonseca, A. H. da, & Baêta, B. de A. (2022). Hemoparasites in Didelphis aurita from Seropédica, Rio de Janeiro State, Brazil. Semina: Ciências Agrárias, 43(6), 2403–2414. https://doi.org/10.5433/1679-0359.2022v43n6p2403

Issue

Section

Articles

Most read articles by the same author(s)