SEROLOGICAL, PARASITOLOGICAL AND MOLECULAR ASSESSMENT OF Babesia bovis AND Babesia bigemina IN CATTLE FROM STATE OF MARANHÃO
Keywords:
Dairy cattle. Babesiosis. Diagnose.Abstract
The aim of the present study was to determine the prevalence of Babesia bovis and Babesia bigemina in dairy cattle from São Luis Island in the state of Maranhão, Brazil. A total of 281 blood samples were collected. In total, 275 (97.9%) animals were B. bovis-reactive and B. bigemina-reactive in the Enzyme-Linked Immunosorbent Assay (ELISA). The microscopy examination detected 22 (7.8%) animals that were positive for Babesia sp. and the Polymerase Chain Reaction (PCR) analysis showed that 91 animals (32.38%) and 23 animals (8.18%) were positive for B. bovis and B. bigemina, respectively, while 17 animals (6.04%) were co-infected. There is a high level of transmission of these protozoa in Maranhão, and the animals were naturally exposed. Therefore, it is possible to characterize the island as enzootic stability for babesiosis, indicating a risk of financial losses when susceptible animals are introduced from areas of enzootic instability or free regions of B. bovis and B. bigemina.Downloads
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References
ALFREDO, A. A. N. et al. Serological survey of Babesia bovis and Anaplasma marginale in cattle in Tete Province, Mozambique.Tropical Animal Health and Production, Edinburgh, v. 33, n. 2, p. 121-131, 2005.
ALMERIA, S. et al. Bovine piroplasms in Minorca (Balearic Islands, Spain): a comparison of PCR-based and light microscopy detection. Veterinary Parasitology, Duluth, v.99, n. 3, p. 249-259, 2001.
ANTONIASSI, N. A. B. et al. Surto de babesiose cerebral em bovinos no Estado do Rio Grande do Sul. Ciência Rural, Santa Maria, v. 39, n. 3, p. 933–936, 2009.
BARROS, S. L. et al. Serological survey of Babesia bovis, Babesia bigemina, and Anaplasma marginale antibodies in cattle from the semi-arid region of the state of Bahia, Brazil, by enzyme-linked immunosorbent assays. Memórias do Instituto Oswaldo Cruz, Rio de Janeiro, v. 100, n. 6, p. 613-617, 2005.
BASTOS, R. G. et al. The Ripicephalus (Boophilus) microplus Bm86 gene plays a critical role in the fitness of ticks fed on cattle during acute Babesia bovis infection. Parasites & Vector, London, v.3, n. 11, p. 1-11, 2010.
BOCK, R. E. et al. Effect of breed of cattle on innate resistance to infection with Babesia bovis, B. bigemina and Anaplasma marginale. Australian Veterinary Journal, v. 75, n. 5, p. 337-340, 1997.
BOCK, R. E. et al. Babesiosis of cattle. Parasitology, v. 129, p. 247-269, 2004.
BRITO, L. G. et al. Babesia bovis infection in the southwestern Brazilian Amazon.Ticks and Tick-borne Disesases, v. 4, n. 1-2, p.78-82, 2013.
BROWN, W. C. et al. Prospects for recombinant vaccines against Babesia bovis and related parasites. Parasite Immunology, v. 28, n. 7, p. 315–327, 2006.
CALDER, J. A. et al. Monitoring Babesia bovis infections in cattle by using PCR-based tests. Journal Clinic Microbiology, v. 34, n. 11, p. 2748–2755, 1996.
CÂMARA, A. C. L. et al. Surtos de babesiose cerebral em bovinos leiteiros no nordeste brasileiro. Ciencia Animal Brasileira, Goiânia, v. 1, p. 619–624, 2009.
CENTRO PAN-AMERICANO DE ZOONOSIS. Procedimentos para estúdios de prevalência por muestro. Buenos Aires: Ramos Mejia, 1979. Nota Técnica n.18.
CHAUDHRY, Z. I. et al. Molecular detection of Babesia bigemina and Babesia bovis in crossbred Carrier cattle trough PCR. Pakistan Journal of Zoology, Lahore, v. 42, n. 2, p. 201-204, 2010.
CRINGOLI, G. et al. Epidemiology of bovine tickborne diseases in southern Italy. Veterinary Research, London, v. 33, n. 4, p. 421-426, 2002.
FIGUEROA, J. V. et al. Multiplex polymerase chain reaction based assay for the detection of Babesia bigemina, Babesia bovis and Anaplasma marginale DNA in bovine blood. Veterinary Parasitology, Duluth, v. 50, n. 1-2, p. 69-81, 1993.
GOFF, W. L. et al. Validation of a competitive enzyme-linked immunosorbent assay for detection of Babesia bigemina antibodies in cattle. Clinical and Vaccine Immunology, v. 15, n. 9, p. 1316-1321, 2008.
GUEDES-JÚNIOR, D. S. G. et al. Frequency of antibodies to Babesia bigemina, B. bovis, Anaplasma marginale, Trypanosoma vivax and Borrelia burdgorferi in cattle from the Northeastern Region of the State of Pará, Brazil. Revista Brasileira de Parasitologia Veterinária, Jaboticabal, v. 17, n. 2, p. 105- 109, 2008.
GUERRA, R. M. S. N. C.; BRITO, D. R. B. Ixodofauna de mamíferos domésticos da Ilha de São Luis, MA. Entomología y Vector, Rio de Janeiro, v. 11, n. 2, p. 435-444, 2004.
IÇA, A.; INCI, A.; YILDIRIM, A.Parasitological and molecular prevalence of bovine Theileria and Babesia species in the vicinity of Kayseri. Turkish Journal of Veterinary & Animal Sciences, Ankara, v. 31, n. 1, p. 33-38, 2007.
JAMES, M.A. et al. Seroepidemiology of bovine anaplasmosis and babesiosis in Venezuela. Tropical Animal Health Production, v. 17, n. 1, p. 9-18, 1985.
JONSSON, N. N.; BOCK R. E.; JORGENSEN, W. K. Productivity and health effects of anaplasmosis and babesiosis on Bos indicus cattle and their crosses, and the effects of differing intensity of tick control in Australia. Veterinary Parasitology, Duluth, v. 155, n. 1-2, p. 1-9, 2008.
KALKAN, K.; ÖZÇELİK, S.; MALATYALI, E. Seroprevalence of babesiosis in cattle in Sivas. Türkiye Parazitoloji Dergisi, v. 34, n. 1, p. 11 16, 2010.
LOWRY, O. H. et al. Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry, Rockville, v. 193, n. 1, p. 265-275, 1951.
MADRUGA, C. R; AYCARDI, E; PUTT, N. Epidemiologia da anaplasmose e babesioses em bovinos da Região do Cerrado do Estado do Mato grosso do sul: I – Prevalência. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, Belo Horizonte, v.35, n. 5, p. 631-640, 1983.
MADRUGA, C. R. et al. Desenvolvimento de uma prova de imunoadsorção enzimática para detecção de anticorpos contra Babesia bovis. Pesquisa Veterinária Brasileira, Rio de Janeiro, v. 20, n. 4, p. 167-170, 2000.
MADRUGA, C. R. et al. Evaluation of an ELISA for detection of antibodies to Babesia bigemina in cattle and application in an epidemiological survey in Brazil. Pesquisa Veterinária Brasileira, Rio de Janeiro, v. 21, n. 2, p. 72-76, 2001.
MAHONEY, D. F.; ROSS, D. R. Epizootiological factors in the control of bovine babesiosis. Australian Veterinary Journal, v. 48, n. 1, p. 292-298, 1972.
MAS, J. J. C. et al. Risk of babesiosis and anaplasmosis in different ecological zones of Santa Cruz Department, Bolivia.Veterinary Parasitology, Duluth, v. 93, n. 1, p. 29–38, 2000.
OSAKI, S. C. et al. Ocorrência de anticorpos anti Babesia bovis e estudo sobre a infecção natural em bovinos da raça nelore, na região de Umuarama, Paraná, Brasil. Revista Brasileira de Parasitologia Veterinária, Jaboticabal, v. 11, n. 2, p. 77-83, 2002.
PAYNE, R. C.; OSÓRIO, O. Tick-borne diseases in Paraguay. I. Seroepidemiological studies on anaplasmosis and babesiosis. Tropical Animal Health and Production, Edinburgh, v. 22, n. 2, p. 53–60, 1990.
PIPANO, E. et al. Babesia bovis and B. bigemina: persistence of infection in friesian cows following vaccination with live antibabesial vaccines. Veterinary Journal, v. 164, n. 1, p. 64- 68, 2002.
RAMOS, J.A. et al. Evaluation of Calorimetric Babesia bigemina-DNA Probe Within an Epidemiological Survey. Memórias do Instituto Oswaldo Cruz, Rio de Janeiro, v. 87, (Suppl 3), p. 213-217, 1992.
SAHIB, H. et al. Bovine Babesiosis: Seroprevalence and Ticks Associated with Cattle from Two Different Regions of Morocco. Annals of the New York Academy of Sciences, v. 849, n. 1, p. 213-218, 1998.
SILVA, R.A. et al. Infecção natural por hemoparasitos em bezerros submetidos à quimio-profilaxia aos 30 dias de idade. Revista Brasileirade Parasitologia Veterinária, Jaboticabal, v. 16, n. 3, p. 163-165, 2007.
SILVA, M. G. et al. First survey for Babesia bovis and Babesia bigemina infection in cattle from Central and Southern regions of Portugal using serological and DNA detection methods. Veterinary Parasitology, Duluth, v. 166, n. 1-2, p. 66-72, 2009.
SILVA, J. B. et al. Ocorrência sorológica de Babesia bovis, Babesia bigemina e Anaplasma marginale em bovinos e bubalinos no estado do Pará, Brasil. Semina: Ciências Agrárias, Londrina, v. 35, n. 5, p. 2495-2500, 2014.
SOARES, C. O. et al. Seroprevalence of Babesia bovis in cattle in the North Fluminense mesoregion, Brazil. Pesquisa Veterinária Brasileira, Rio de Janeiro, v. 20, n. 2, p. 75-79, 2000.
SOUZA, F. A. L. et al. Babesiosis and anaplasmosis in dairly cattle in Northeastern Brazil. Pesquisa Veterinária Brasileira, Rio de Janeiro, v. 33, n. 9, p. 1057-1061, 2013.
SOUZA, J. C. P. et al. Soroprevalência de Babesia bigemina em bovinos na mesorregião Norte Fluminense. Pesquisa Veterinária Brasileira, Rio de Janeiro, v. 20, n. 1, p. 26-30, 2000.
TEGLAS, M. et al. Ticks and tick-borne disease in Guatemalan cattle and horses.Veterinary Parasitology. Duluth, v. 131, n. 1-2, p. 119-127, 2005.
TJORNEHOJ, K. et al. Field observations on the duration of immunity in cattle after vaccination against Anaplasma and Babesia species. Journal Veterinary Research, London, v. 63, n. 1, p. 1-5, 1996.
TEMBUE, A. A. et al. Risk factors associated with the frequency of antibodies against Babesia bovis and Babesia bigemina in cattle in southern Mozambique. Pesquisa Veterinária Brasileira, Rio de Janeiro, v. 31, n. 8, p. 663-666, 2011.
TERKAWI, M. A. et al. Molecular and serological prevalence of Babesia bovis and Babesia bigemina in cattle from central region of Syria. Veterinary Parasitology, Duluth, v. 187, n. 1-2, p. 307-311, 2012.
TERKAWI, M. A. et al. Molecular and serological prevalence of Babesia bovis and Babesia bigemina in water buffaloes in the northeast region of Thailand. Veterinary Parasitology, Duluth, v. 178, n. 3-4, 201–207, 2011.
TRINDADE, H. I. et al. Detection of antibodies against Babesia bovis and Babesia bigemina in calves from the region of Araguaína, State of Tocantins, Brazil. Revista Brasileira de Parasitologia Veterinária, Jaboticabal, v. 19, n. 3, p. 169-173, 2010.
ALMERIA, S. et al. Bovine piroplasms in Minorca (Balearic Islands, Spain): a comparison of PCR-based and light microscopy detection. Veterinary Parasitology, Duluth, v.99, n. 3, p. 249-259, 2001.
ANTONIASSI, N. A. B. et al. Surto de babesiose cerebral em bovinos no Estado do Rio Grande do Sul. Ciência Rural, Santa Maria, v. 39, n. 3, p. 933–936, 2009.
BARROS, S. L. et al. Serological survey of Babesia bovis, Babesia bigemina, and Anaplasma marginale antibodies in cattle from the semi-arid region of the state of Bahia, Brazil, by enzyme-linked immunosorbent assays. Memórias do Instituto Oswaldo Cruz, Rio de Janeiro, v. 100, n. 6, p. 613-617, 2005.
BASTOS, R. G. et al. The Ripicephalus (Boophilus) microplus Bm86 gene plays a critical role in the fitness of ticks fed on cattle during acute Babesia bovis infection. Parasites & Vector, London, v.3, n. 11, p. 1-11, 2010.
BOCK, R. E. et al. Effect of breed of cattle on innate resistance to infection with Babesia bovis, B. bigemina and Anaplasma marginale. Australian Veterinary Journal, v. 75, n. 5, p. 337-340, 1997.
BOCK, R. E. et al. Babesiosis of cattle. Parasitology, v. 129, p. 247-269, 2004.
BRITO, L. G. et al. Babesia bovis infection in the southwestern Brazilian Amazon.Ticks and Tick-borne Disesases, v. 4, n. 1-2, p.78-82, 2013.
BROWN, W. C. et al. Prospects for recombinant vaccines against Babesia bovis and related parasites. Parasite Immunology, v. 28, n. 7, p. 315–327, 2006.
CALDER, J. A. et al. Monitoring Babesia bovis infections in cattle by using PCR-based tests. Journal Clinic Microbiology, v. 34, n. 11, p. 2748–2755, 1996.
CÂMARA, A. C. L. et al. Surtos de babesiose cerebral em bovinos leiteiros no nordeste brasileiro. Ciencia Animal Brasileira, Goiânia, v. 1, p. 619–624, 2009.
CENTRO PAN-AMERICANO DE ZOONOSIS. Procedimentos para estúdios de prevalência por muestro. Buenos Aires: Ramos Mejia, 1979. Nota Técnica n.18.
CHAUDHRY, Z. I. et al. Molecular detection of Babesia bigemina and Babesia bovis in crossbred Carrier cattle trough PCR. Pakistan Journal of Zoology, Lahore, v. 42, n. 2, p. 201-204, 2010.
CRINGOLI, G. et al. Epidemiology of bovine tickborne diseases in southern Italy. Veterinary Research, London, v. 33, n. 4, p. 421-426, 2002.
FIGUEROA, J. V. et al. Multiplex polymerase chain reaction based assay for the detection of Babesia bigemina, Babesia bovis and Anaplasma marginale DNA in bovine blood. Veterinary Parasitology, Duluth, v. 50, n. 1-2, p. 69-81, 1993.
GOFF, W. L. et al. Validation of a competitive enzyme-linked immunosorbent assay for detection of Babesia bigemina antibodies in cattle. Clinical and Vaccine Immunology, v. 15, n. 9, p. 1316-1321, 2008.
GUEDES-JÚNIOR, D. S. G. et al. Frequency of antibodies to Babesia bigemina, B. bovis, Anaplasma marginale, Trypanosoma vivax and Borrelia burdgorferi in cattle from the Northeastern Region of the State of Pará, Brazil. Revista Brasileira de Parasitologia Veterinária, Jaboticabal, v. 17, n. 2, p. 105- 109, 2008.
GUERRA, R. M. S. N. C.; BRITO, D. R. B. Ixodofauna de mamíferos domésticos da Ilha de São Luis, MA. Entomología y Vector, Rio de Janeiro, v. 11, n. 2, p. 435-444, 2004.
IÇA, A.; INCI, A.; YILDIRIM, A.Parasitological and molecular prevalence of bovine Theileria and Babesia species in the vicinity of Kayseri. Turkish Journal of Veterinary & Animal Sciences, Ankara, v. 31, n. 1, p. 33-38, 2007.
JAMES, M.A. et al. Seroepidemiology of bovine anaplasmosis and babesiosis in Venezuela. Tropical Animal Health Production, v. 17, n. 1, p. 9-18, 1985.
JONSSON, N. N.; BOCK R. E.; JORGENSEN, W. K. Productivity and health effects of anaplasmosis and babesiosis on Bos indicus cattle and their crosses, and the effects of differing intensity of tick control in Australia. Veterinary Parasitology, Duluth, v. 155, n. 1-2, p. 1-9, 2008.
KALKAN, K.; ÖZÇELİK, S.; MALATYALI, E. Seroprevalence of babesiosis in cattle in Sivas. Türkiye Parazitoloji Dergisi, v. 34, n. 1, p. 11 16, 2010.
LOWRY, O. H. et al. Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry, Rockville, v. 193, n. 1, p. 265-275, 1951.
MADRUGA, C. R; AYCARDI, E; PUTT, N. Epidemiologia da anaplasmose e babesioses em bovinos da Região do Cerrado do Estado do Mato grosso do sul: I – Prevalência. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, Belo Horizonte, v.35, n. 5, p. 631-640, 1983.
MADRUGA, C. R. et al. Desenvolvimento de uma prova de imunoadsorção enzimática para detecção de anticorpos contra Babesia bovis. Pesquisa Veterinária Brasileira, Rio de Janeiro, v. 20, n. 4, p. 167-170, 2000.
MADRUGA, C. R. et al. Evaluation of an ELISA for detection of antibodies to Babesia bigemina in cattle and application in an epidemiological survey in Brazil. Pesquisa Veterinária Brasileira, Rio de Janeiro, v. 21, n. 2, p. 72-76, 2001.
MAHONEY, D. F.; ROSS, D. R. Epizootiological factors in the control of bovine babesiosis. Australian Veterinary Journal, v. 48, n. 1, p. 292-298, 1972.
MAS, J. J. C. et al. Risk of babesiosis and anaplasmosis in different ecological zones of Santa Cruz Department, Bolivia.Veterinary Parasitology, Duluth, v. 93, n. 1, p. 29–38, 2000.
OSAKI, S. C. et al. Ocorrência de anticorpos anti Babesia bovis e estudo sobre a infecção natural em bovinos da raça nelore, na região de Umuarama, Paraná, Brasil. Revista Brasileira de Parasitologia Veterinária, Jaboticabal, v. 11, n. 2, p. 77-83, 2002.
PAYNE, R. C.; OSÓRIO, O. Tick-borne diseases in Paraguay. I. Seroepidemiological studies on anaplasmosis and babesiosis. Tropical Animal Health and Production, Edinburgh, v. 22, n. 2, p. 53–60, 1990.
PIPANO, E. et al. Babesia bovis and B. bigemina: persistence of infection in friesian cows following vaccination with live antibabesial vaccines. Veterinary Journal, v. 164, n. 1, p. 64- 68, 2002.
RAMOS, J.A. et al. Evaluation of Calorimetric Babesia bigemina-DNA Probe Within an Epidemiological Survey. Memórias do Instituto Oswaldo Cruz, Rio de Janeiro, v. 87, (Suppl 3), p. 213-217, 1992.
SAHIB, H. et al. Bovine Babesiosis: Seroprevalence and Ticks Associated with Cattle from Two Different Regions of Morocco. Annals of the New York Academy of Sciences, v. 849, n. 1, p. 213-218, 1998.
SILVA, R.A. et al. Infecção natural por hemoparasitos em bezerros submetidos à quimio-profilaxia aos 30 dias de idade. Revista Brasileirade Parasitologia Veterinária, Jaboticabal, v. 16, n. 3, p. 163-165, 2007.
SILVA, M. G. et al. First survey for Babesia bovis and Babesia bigemina infection in cattle from Central and Southern regions of Portugal using serological and DNA detection methods. Veterinary Parasitology, Duluth, v. 166, n. 1-2, p. 66-72, 2009.
SILVA, J. B. et al. Ocorrência sorológica de Babesia bovis, Babesia bigemina e Anaplasma marginale em bovinos e bubalinos no estado do Pará, Brasil. Semina: Ciências Agrárias, Londrina, v. 35, n. 5, p. 2495-2500, 2014.
SOARES, C. O. et al. Seroprevalence of Babesia bovis in cattle in the North Fluminense mesoregion, Brazil. Pesquisa Veterinária Brasileira, Rio de Janeiro, v. 20, n. 2, p. 75-79, 2000.
SOUZA, F. A. L. et al. Babesiosis and anaplasmosis in dairly cattle in Northeastern Brazil. Pesquisa Veterinária Brasileira, Rio de Janeiro, v. 33, n. 9, p. 1057-1061, 2013.
SOUZA, J. C. P. et al. Soroprevalência de Babesia bigemina em bovinos na mesorregião Norte Fluminense. Pesquisa Veterinária Brasileira, Rio de Janeiro, v. 20, n. 1, p. 26-30, 2000.
TEGLAS, M. et al. Ticks and tick-borne disease in Guatemalan cattle and horses.Veterinary Parasitology. Duluth, v. 131, n. 1-2, p. 119-127, 2005.
TJORNEHOJ, K. et al. Field observations on the duration of immunity in cattle after vaccination against Anaplasma and Babesia species. Journal Veterinary Research, London, v. 63, n. 1, p. 1-5, 1996.
TEMBUE, A. A. et al. Risk factors associated with the frequency of antibodies against Babesia bovis and Babesia bigemina in cattle in southern Mozambique. Pesquisa Veterinária Brasileira, Rio de Janeiro, v. 31, n. 8, p. 663-666, 2011.
TERKAWI, M. A. et al. Molecular and serological prevalence of Babesia bovis and Babesia bigemina in cattle from central region of Syria. Veterinary Parasitology, Duluth, v. 187, n. 1-2, p. 307-311, 2012.
TERKAWI, M. A. et al. Molecular and serological prevalence of Babesia bovis and Babesia bigemina in water buffaloes in the northeast region of Thailand. Veterinary Parasitology, Duluth, v. 178, n. 3-4, 201–207, 2011.
TRINDADE, H. I. et al. Detection of antibodies against Babesia bovis and Babesia bigemina in calves from the region of Araguaína, State of Tocantins, Brazil. Revista Brasileira de Parasitologia Veterinária, Jaboticabal, v. 19, n. 3, p. 169-173, 2010.
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20-05-2015
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