Molecular, serological, and parasitological detection of Babesia vogeli in dogs in the state of Piauí, Brazil
DOI:
https://doi.org/10.5433/1679-0359.2019v40n6Supl2p3035Keywords:
Molecular analysis, Babesiosis, Blood parasites, PCR, IFA.Abstract
Studies on canine babesiosis in northeastern Brazil are scarce, although the weather conditions in this region are favorable for the development of the tick vector. This study determined the prevalence of Babesia vogeli in dogs sampled in Teresina, state of Piauí, northeast Brazil, using direct and indirect diagnostic methods and performed a phylogenetic analysis of 18S rRNA sequences. A total of 315 dogs were screened during routine care regardless of clinical suspicion. Blood was collected by jugular venipuncture to perform indirect immunofluorescence assay (IFA) and polymerase chain reaction (PCR) and for parasite screening in peripheral blood smears. Positivity was 2.2% (7/315) by microscopy, 4.8% (15/315) by PCR, and 48.6% (153/315) by IFA. PCR amplified a 602-bp fragment of the piroplasmid 18S rRNA gene, and sequence alignment and analysis revealed 99% homology with B. vogeli isolates from other regions of Brazil and other countries. In addition, there was high variability among sequences from other northeast states of Brazil. This study is the first to perform the molecular analysis of B. vogeli in Piauí. The results demonstrate that canine babesiosis is endemic in dogs sampled in Teresina and that PCR may be the method of choice to perform parasite screening in this region.Downloads
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References
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SAITOU, N.; NEI, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, New York, v. 4, n. 4, p. 406-425, 1987. DOI: 10.1093/oxfordjournals.molbev.a040454
SCHNITTGER, L.; RODRIGUEZ, A. E.; FLORIN-CHRISTENSEN, M.; MORRISON, D. A. Babesia: a world emerging. Infection, Genetics and Evolution, Amsterdam, v. 12, n. 8, p. 1788-809, 2012. DOI: 10.1016/j.meegid.2012.07.004
SILVA, L. S. Erliquiose e anaplasmose canina em Teresina, Piauí. 2010. Dissertação (Mestrado em Ciência Animal) - Universidade Federal do Piauí, Teresina.
SOUSA, K. C. M.; FERNANDES, M. P.; HERRERA, H. M.; FRESCHI, C. R.; MACHADO, R. Z.; ANDRÉ, M. R. Diversity of piroplasmids among wild and domestic mammals and ectoparasites in Pantanal wetland, Brazil. Ticks and Tick-Borne Diseases, Amsterdam, v. 9, n. 2, p. 245-253, 2018. DOI: 10.1016/j.ttbdis.2017.09.010
SOUSA, K. C. M.; ANDRÉ, M. R.; HERRERA, H. M.; ANDRADE, G. B.; JUSI, M. M.; SANTOS, L. L.; BARRETO, W. T.; MACHADO, R. Z.; OLIVEIRA, G. P. Molecular and serological detection of tick-borne pathogens in dogs from an area endemic for Leishmania infantum in Mato Grosso do Sul, Brazil. Revista Brasileira de Parasitologia Veterinária, Jaboticabal, v. 22, n. 4, p. 525-531, 2013. DOI: 10.1590/S1984-29612013000400012
SPIEWAK, G. Aspectos epidemiológicos, clínicos e de diagnóstico da infecção por Babesia canis em cães atendidos em clínicas veterinárias em Belo Horizonte. 1992. Dissertação (Mestrado em Medicina Veterinária) - Escola de Veterinária da Universidade Federal de Minas Gerais, Belo Horizonte.
TAMURA, K.; STECHER. G.; PETERSON, D.; FILIPSKI, A.; KUMAR, S. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, New York, v. 30, n. 12, p. 2725-2729, 2013. DOI: 10.1093/molbev/mst197
THOMPSON, J. D.; HIGGINS, D. G.; GIBSON, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic acids research, Oxford, v. 22, n. 22, p. 4673-4680, 1994. DOI: 10.1093/nar/22.22.4673
TODOROVIC, R. A. Serological diagnosis of babesiosis: a review. Tropical Animal Health and Production, Heidelberg, v. 7, n. 1, p. 1-14, 1975. DOI: 10.1007/BF02383236
TRAPP, S. M.; DAGNONE, A. S.; VIDOTTO, O.; FREIRE, R. L.; AMUDE, A. M.; MORAIS, H. S. Seroepidemiology of canine babesiosis and ehrlichiosis in a Hospital population. Veterinary Parasitology, Amsterdam, v. 140, n. 3-4, p. 223-230, 2006. DOI: 10.1016/j.vetpar.2006.03.030
TROSKIE, M.; VILLIERSB, L.; LEISEWITZB, A.; OOSTHUIZENA, M. C.; QUANA, M. Development and validation of a multiplex, real-time PCR assay for Babesia rossi and Babesia vogeli. Ticks and Tick-Borne Diseases, Amsterdam, v. 10, n. 2, p. 421-432, 2018. DOI: 10.1016/j.ttbdis.2018.12.004
UILENBERG, G. Babesia - a historical overview. Veterinary Parasitology, Amsterdam, v. 138, n. 1-2, p. 3-10, 2006. DOI: 10.1016/j.vetpar.2006.01.035
ZAHLER, M.; SCHEIN, E.; RINDER, H.; GOTHE, R. Characteristic genotypes discriminate between Babesia canis isolates of differing vector specificity and pathogenicity to dogs. Parasitology Research, Berlin, v. 84, n. 7, p. 544-548, 1998. DOI: 10.1007/s004360050
BICALHO, K. A.; PASSOS, L. M. F.; RIBEIRO, M. F. B. Infecção experimental de cães com amostras de Babesia canis isoladas em Minas Gerais. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, Belo Horizonte, v. 54, n. 5, p. 546-548, 2002. DOI: 10.1590/S0102-09352002000500016
BOOZER, A. L.; MACINTIRE, D. K. Canine babesiosis. Veterinary Clinics of North America-Small Animal Practice, London, v. 33, n. 4, p. 885-904, 2003. DOI: 10.1016/S0195-5616(03)00039-1
BOURDOISEAU, G. Canine babesiosis in France. Veterinary Parasitology, Amsterdam, v. 138, n. 1-2, p. 118-125, 2006. DOI: 10.1016/j.vetpar.2006.01.046
BREITSCHWERDT, E. B.; MALONE, J. B.; MACWILLIANS, P.; LEVY, M. G.; QUALLS JUNIOR, C. W.; PRUDICH, M. J. Babesiosis in the greyhound. Journal of the American Veterinary Medical Association, Ithaca, v. 182, n. 9, p. 978-982, 1983.
CACCIÒ, S. M.; ANTUNOVIC, B.; MORETTI, A.; MANGILI, V.; MARINCULIC, A.; BARIC, R. R.; SLEMENDA, S. B.; PIENIAZEK, N. J. Molecular characterization of Babesia canis canis and Babesia canis vogeli from naturally infected European dogs. Veterinary Parasitology, Amsterdam, v. 106, n. 4, p. 285-292, 2002. DOI: 10.1016/S0304-4017(02)00112-7
CARDOSO, L.; COSTA, A.; TUNA, J.; VIEIRA, L.; EYAL, O.; YISASCHAR-MEKUZAS, Y.; BANETH, G. Babesia canis canis and Babesia canis vogeli infections in dogs from northern Portugal. Veterinary Parasitology, Amsterdam, v. 156, n. 3-4, p. 199-204, 2008. DOI: 10.1016/j.vetpar.2008.05.027
CARLI, E.; TASCA, S.; TROTTA, M.; FURLANELLO, T.; CALDIN, M.; SOLANO-GALLEGO, L. Detection of erythrocyte binding IgM and IgG by flow cytometry in sick dogs with Babesia canis canis or Babesia canis vogeli infection. Veterinary Parasitology, Amsterdam, v. 162, n. 1-2, p. 51-57, 2009. DOI: 10.1016/j.vetpar.2009.02.002
CENTRO PANAMERICANO DE ZOONOSIS - Procedimentos para estudios de prevalencia de enfermidades cronicas en el ganado. Buenos Aires: Ramos Mejia, 1973. 33 p. (Nota técnica, 18).
DANTAS-TORRES, F. Canine vector-borne diseases in Brazil. Parasites & Vectors, Londres, v. 1, n. 25, p. 1-17, 2008b. DOI: 10.1186/1756-3305-1-25
DANTAS-TORRES, F. Causative agents of canine babesiosis in Brazil. Preventive Veterinary Medicine, Amsterdam, v. 83, n. 2, p. 210-211, 2008a. DOI: 10.1016/j.prevetmed.2007.03.008
DANTAS-TORRES, F.; FIGUEREDO, L. A. Canine babesiosis: a Brazilian perspective. Veterinary Parasitology, Amsterdam, v. 141, n. 3-4, p. 197-203, 2006. DOI: 10.1016/j.vetpar.2006.07.030
DRUMOND, K. O.; COSTA, F. A. L. Forty years of visceral leishmaniasis in the state of Piauí: a review. Revista do Instituto de Medicina Tropical de São Paulo, São Paulo, v. 53, n. 1, p. 3-11, 2011. DOI: 10.1590/S0036-46652011000100002
DUARTE, S. C.; LINHARES, G. F. C.; ROMANOWSKY, T. N.; SILVEIRA NETO, O. J.; BORGES, L. M. F. Assessment of primers designed for the subspecies-specific discrimination among Babesia canis canis, Babesia canis vogeli and Babesia canis rossi by PCR assay. Veterinary Parasitology, Amsterdam, v. 152, n. 1-2, p. 16-20, 2008. DOI: 10.1016/j.vetpar.2007.12.013
FURLANELLO, T.; FIORIO, F.; CALDIN, M.; LUBAS, G.; SOLANO-GALLEGO, L. Clinicopathological findings in naturally occurring cases of babesiosis caused by large form Babesia from dogs of northeastern Italy. Veterinary Parasitology, Amsterdam, v. 134, n. 1-2, p. 77-85, 2005. DOI: 10.1016/j.vetpar.2005.07.016
FURUTA, P. I.; OLIVEIRA, T. M.; THEIXEIRA, M. C.; ROCHA, A. G.; MACHADO, R. Z.; TINUCCI-COSTA, M. G. Comparison between a soluble antigen-based ELISA and IFAT in detecting antibodies against Babesia canis in dogs. Revista Brasileira de Parasitologia Veterinária, Jaboticabal, v. 18, n. 3, p. 41-45, 2009. DOI: 10.4322/rbpv.01803007
GOPEGUI, R. R.; PENALBA, B.; GOICOA, A.; ESPADA, Y.; FIDALGO, L. E.; ESPINO, L. Clinicopathological findings and coagulation disorders in 45 cases of canine babesiosis in Spain. The Veterinary Journal, Londres, v. 174, n. 1, p. 129-132, 2007. DOI: 10.1016/j.tvjl.2006.05.017
GUIMARÃES, J. C.; ALBERNAZ, A. P.; MACHADO, J. A.; MELO JÚNIOR, O. A.; GARCIA, L. N. N. Aspectos clínico-laboratoriais da babesiose canina na cidade de Campos do Goytacazes, RJ. Revista Brasileira de Parasitologia Veterinária, Jaboticabal, v. 13, p. 229, 2004. Supplement 1.
INSTITUTO INTERAMERICANO DE COOPERACIÓN PARA LA AGRICULTURA - IICA. Técnicas para el diagnóstico de babesioses y anaplasmosis bovina. San José: IICA, 1987. 79 p.
M’GHIRBI, Y.; BOUATTOUR, A. Detection and molecular characterization of Babesia canis vogeli from naturally infected dogs and Rhipicephalus sanguineus ticks in Tunisia. Veterinary Parasitology, Amsterdam, v. 152, n. 1-2, p. 1-7, 2008. DOI: 10.1016/j.vetpar.2007.12.018
MARTIN, A. R.; DUNSTAN, R. H.; ROBERTS, T. K.; BROWN, G. K. Babesia canis vogeli: a novel PCR for its detection in dogs in Australia. Experimental Parasitology, Orlando, v. 112, n. 1, p. 63-65, 2006. DOI: 10.1016/j.exppara.2005.09.001
MEDEIROS, R. M. Estudo Agrometeorológico para o Estado do Piauí. Teresina: Secretaria do Meio Ambiente e Recursos Hídricos do Estado do Piauí, 2004. 113 p.
O’DWYER, L. H.; LOPES, V. V. A.; RUBINI, A. S.; PADUAN, K. S.; RIBOLLA, P. E. M. Babesia spp. infection in dogs from rural areas of São Paulo State, Brazil. Revista Brasileira de Parasitologia Veterinária, Jaboticabal, v. 18, n. 2, p. 23-26, 2009. DOI: 10.4322/rbpv.01802005
PASSOS, L. M.; GEIGER, S. M.; RIBEIRO, M. F. B.; PfiSTER, K.; ZAHLER-RINDER, M. First molecular detection of Babesia vogeli in dogs from Brazil. Veterinary Parasitology, Amsterdam, v. 127, n. 1, p. 81-85, 2005. DOI: 10.1016/j.vetpar.2004.07.028
PETRA, B.; JOSIPA, K.; RENATA, B. R.; VLADIMIR, M. Canine babesiosis: where do we stand? A Acta Veterinaria-Beograd, Belgrade, v. 68, n. 2, p. 127-160, 2018. DOI: 10.2478/acve-2018-0011
RIBEIRO, M. F. B.; PASSOS, L. M. F.; LIMA, J. D.; GUIMARÃES, A. M. Frequency of anti-Babesia canis antibodies in dogs, in Belo Horizonte, Minas Gerais. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, Belo Horizonte, v. 42, n. 6, p. 511-517, 1990.
SAITOU, N.; NEI, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, New York, v. 4, n. 4, p. 406-425, 1987. DOI: 10.1093/oxfordjournals.molbev.a040454
SCHNITTGER, L.; RODRIGUEZ, A. E.; FLORIN-CHRISTENSEN, M.; MORRISON, D. A. Babesia: a world emerging. Infection, Genetics and Evolution, Amsterdam, v. 12, n. 8, p. 1788-809, 2012. DOI: 10.1016/j.meegid.2012.07.004
SILVA, L. S. Erliquiose e anaplasmose canina em Teresina, Piauí. 2010. Dissertação (Mestrado em Ciência Animal) - Universidade Federal do Piauí, Teresina.
SOUSA, K. C. M.; FERNANDES, M. P.; HERRERA, H. M.; FRESCHI, C. R.; MACHADO, R. Z.; ANDRÉ, M. R. Diversity of piroplasmids among wild and domestic mammals and ectoparasites in Pantanal wetland, Brazil. Ticks and Tick-Borne Diseases, Amsterdam, v. 9, n. 2, p. 245-253, 2018. DOI: 10.1016/j.ttbdis.2017.09.010
SOUSA, K. C. M.; ANDRÉ, M. R.; HERRERA, H. M.; ANDRADE, G. B.; JUSI, M. M.; SANTOS, L. L.; BARRETO, W. T.; MACHADO, R. Z.; OLIVEIRA, G. P. Molecular and serological detection of tick-borne pathogens in dogs from an area endemic for Leishmania infantum in Mato Grosso do Sul, Brazil. Revista Brasileira de Parasitologia Veterinária, Jaboticabal, v. 22, n. 4, p. 525-531, 2013. DOI: 10.1590/S1984-29612013000400012
SPIEWAK, G. Aspectos epidemiológicos, clínicos e de diagnóstico da infecção por Babesia canis em cães atendidos em clínicas veterinárias em Belo Horizonte. 1992. Dissertação (Mestrado em Medicina Veterinária) - Escola de Veterinária da Universidade Federal de Minas Gerais, Belo Horizonte.
TAMURA, K.; STECHER. G.; PETERSON, D.; FILIPSKI, A.; KUMAR, S. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, New York, v. 30, n. 12, p. 2725-2729, 2013. DOI: 10.1093/molbev/mst197
THOMPSON, J. D.; HIGGINS, D. G.; GIBSON, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic acids research, Oxford, v. 22, n. 22, p. 4673-4680, 1994. DOI: 10.1093/nar/22.22.4673
TODOROVIC, R. A. Serological diagnosis of babesiosis: a review. Tropical Animal Health and Production, Heidelberg, v. 7, n. 1, p. 1-14, 1975. DOI: 10.1007/BF02383236
TRAPP, S. M.; DAGNONE, A. S.; VIDOTTO, O.; FREIRE, R. L.; AMUDE, A. M.; MORAIS, H. S. Seroepidemiology of canine babesiosis and ehrlichiosis in a Hospital population. Veterinary Parasitology, Amsterdam, v. 140, n. 3-4, p. 223-230, 2006. DOI: 10.1016/j.vetpar.2006.03.030
TROSKIE, M.; VILLIERSB, L.; LEISEWITZB, A.; OOSTHUIZENA, M. C.; QUANA, M. Development and validation of a multiplex, real-time PCR assay for Babesia rossi and Babesia vogeli. Ticks and Tick-Borne Diseases, Amsterdam, v. 10, n. 2, p. 421-432, 2018. DOI: 10.1016/j.ttbdis.2018.12.004
UILENBERG, G. Babesia - a historical overview. Veterinary Parasitology, Amsterdam, v. 138, n. 1-2, p. 3-10, 2006. DOI: 10.1016/j.vetpar.2006.01.035
ZAHLER, M.; SCHEIN, E.; RINDER, H.; GOTHE, R. Characteristic genotypes discriminate between Babesia canis isolates of differing vector specificity and pathogenicity to dogs. Parasitology Research, Berlin, v. 84, n. 7, p. 544-548, 1998. DOI: 10.1007/s004360050
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2019-09-30
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Braga, J. F. V., Souza, F. de A. L., Silva, L. dos S., Fonseca, L. S. da, Pinho, F. A. de, Fotoran, W. L., … Silva, S. M. M. de S. (2019). Molecular, serological, and parasitological detection of Babesia vogeli in dogs in the state of Piauí, Brazil. Semina: Ciências Agrárias, 40(6Supl2), 3035–3044. https://doi.org/10.5433/1679-0359.2019v40n6Supl2p3035
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