Seroprevalence and associated risk factors of ovine neosporosis worldwide: a systematic review and meta-analysis
DOI:
https://doi.org/10.5433/1679-0359.2021v42n3Supl1p2111Keywords:
Neosporosis, Sheep, Heterogeneity, Diagnosis method.Abstract
Neosporosis, caused by the protozoan Neospora caninum, has been widely reported and discussed as a major disease associated with reproductive problems in herds of various animal species. This study aimed to perform a systematic review and meta-analysis on the prevalence and risk factors associated with ovine neosporosis worldwide. This is the first systematic review, which was performed according to the established preferred reporting items in systematic reviews and meta-analyses (PRISMA) guidelines to address ovine neosporosis. Four databases were used in this study: PubMed, SciELO, Web of Science, and Scopus. The selected keywords were “neospora AND sheep,” “neosporosis AND sheep,” “neospora AND lamb,” “neosporosis AND lamb,” “neospora AND ewe,” and “neosporosis AND ewe.” The meta-analysis calculations were performed with random-effects models for proportions, and heterogeneity was tested using the I2 test. This study identified 24 studies on ovine neosporosis, nine of which evaluated the factors associated with the risk of seropositivity. After meta-analysis, the pooled estimated prevalence was 12% (95% CI, 8-16%; I² p-value < 0.01). The evaluation of the included studies allowed the identification of ovine neosporosis distribution in continents according to demonstrated prevalence rates. We confirmed via meta-analysis that the use of indirect immunofluorescence assay (IFAT) or enzyme-linked immunosorbent assay (ELISA) in the diagnosis of ovine neosporosis was not a source of data heterogeneity. The presence of dogs on the properties was reported as the main risk factor associated with the occurrence of ovine neosporosis; however, this was not confirmed by the meta-analysis.Downloads
Download data is not yet available.
References
Abo-Shehada, M., & Abu-Halaweh, M. (2010). Flock-level seroprevalence of, and risk factors for, Neospora caninum among sheep and goats in northern Jordan. Preventive Veterinary Medicine, 93(1), 25-32. doi: 10.1016/j.prevetmed.2009.08.004
Al-Majali, A. M., Jawasreh, K. I., Talafha, H. A., & Talafha, A. Q. (2008). Neosporosis in sheep and different breeds of goats from southern jordan: prevalence and risk factors analysis. American Journal of Animal and Veterinary Sciences, 3(2), 47-52.
Almeida, J. C. de, Kim, P. de C. P., Melo, R. P. B. de, Nogueira, J. F., Martins, F. D. C., Garcia, J. L.,... Mota, R. A. (2019). Neospora caninum DNA in feces of crab-eating fox (Cerdocyon thous - Linnaeus, 1776) from northeastern Brazil. Acta Tropica, 197, 105068. doi: 10.1016/j.actatropica.2019.105068
Andrade, G. S., Bruhna, F. R. P, Rocha, C. M. B. M., Guimarães, A. S., Gouveia, A. M. G., & Guimarães, A. M. (2012). Seroprevalence and risk factors for Neospora caninum in sheep in the state Minas Gerais, southeastern Brazil. Veterinary Parasitology, 188(1-2), 168-171. doi: 10.1016/j.vetpar.2012.03.006
Arraes-Santos, A. I., Araújo, A. C., Guimarães, M. F., Santos, J. R., Pena, H. F. J., Gennari, S. M.,... Horta, M. C. (2016). Seroprevalence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in domestic mammals from two distinct regions in the semi-arid region of Northeastern Brazil. Veterinary Parasitology: Regional Studies and Reports, 5, 14-18. doi: 10.1016/j.vprsr.2016.08.007
Arranz-Solís, D., Benavides, J., Regidor-Cerrillo, J., Horcajo, P., Castaño, P., Del Carmen-Ferreras, M.,… Ortega-Mora, L. M. (2016). Systemic and local immune responses in sheep after Neospora caninum experimental infection at early, mid and late gestation. Veterinary Research, 47(1), 1-13. doi: 10.1186 s 13567-015-0290-0
Barling, K. S., Mcneill, J. W., Paschal, J. C., Mccollum, F. T., Craig, T. M., Adams, L. G., & Thompson, J. A. (2001). Ranch-management factors associated with antibody seropositivity for Neospora caninum in consignments of beef calves in Texas, USA. Preventive Veterinary Medicine, 52(1), 53-61. doi: 10.10 16/S0167-5877(01)00233-1
Castañeda-Hernández, A., Cruz-Vázquez, C., & Medina-Esparza, L. (2014). Neospora caninum: Seroprevalence and DNA detection in blood of sheep from Aguascalientes, Mexico. Small Ruminant Research, 119(1-3), 182-186. doi: 10.1016/j.smallrumres.2014.03.002
Cavalcante, A. C. R., Carneiro, M., Gouveia, A. M. G., Pinheiro, R. R., & Vitor, R. W. (2008). A. Risk factors for infection by Toxoplasma gondii in herds of goats in Ceará, Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 60(1), 36-41. doi: 10.1590/S0102-09352008000100006
Díaz, J. M., Fernández, G., Prieto, A., Valverde, S., Lago, N., Díaz, P.,... Díez-Baños, P. (2014). Epidemiology of reproductive pathogens in semi-intensive lamb-producing flocks in North-West Spain: a comparative serological study. Veterinary Journal, 200(2), 335-338. doi: 10.1016/j.tvjl.2014.02.022
Dijkstra, T. H., Barkema, H. W., Bjorkman, C., & Wouda, W. (2002). A high rate of seroconversion for Neospora caninum in a dairy herd without an obvious increased incidence of abortions. Veterinary Parasitology, 109(3-4), 203-211. doi: 10.1016/S0304-4017(02)00303-5
Dubey, J. P., & Schares, G. (2011). Neosporosis in animals - the last five years. Veterinary Parasitology, 180(1-2), 90-108. doi: 1016/j. vetpar.2011.05.031
Dubey, J. P., Hartley, W. J., Lindsay, D. S., & Topper, M. J. (1990). Fatal congenital Neospora caninum infection in a lamb. Journal of Parasitology, 76(1), 127-130. doi: 10.2307/3282640
Faria, E. B. E. F. T. S. F., Medeiros, E. S., Pinheiro, J. W., Jr., Azevedo, S. S., Atahayde, A. C. R., & Mota, R. A. (2010). Risk factors associated with Neospora caninum seropositivity in sheep from the state of Alagoas, in the northeast region of Brazil. Journal of Parasitology, 96(1), 197-199. doi: 10.1645/GE-21 76.1
Ferreira, M. S. T., Vogel, F. S. F., Sangioni, L. A., Cezar, A. S., & Menezes, F. R. (2016). Neospora spp. and Toxoplasma gondii infection in sheep flocks from Rio Grande do Sul, Brazil. Semina: Ciências Agrárias, 37(3), 1397-1406. doi: 10.5433/1679-0359.2016v37n3p1397
Figliuolo, L. P. C., Kasai, N., Ragozo, A. M. A., Paula, V. S. O., Dias, R. A., Souza, S. L. P., & Gennari, S. M. (2004). Prevalence of anti-Toxoplasma gondii and anti- Neospora caninum antibodies in ovine from São Paulo State, Brazil. Veterinary Parasitology, 123(3-4), 161-166. doi: 10.1016/j.vetpar.2004.06.006
Gazzonis, A. L., Garcia, G. A., Zanzania, S. A., Morab, L. M. O., Invernizzic, A., & Manfredia, M. T. (2016). Neospora caninum infection in sheep and goats from north-eastern Italy and associated risk factors. Small Ruminant Research, 140, 7-12. doi: 10.1016/j.smallrumres.2016.05.010
Gharekhani, J., Tavoosidana, G. R., & Zandieh, M. (2013). Seroprevalence of Neospora caninum in sheep from western Iran. Veterinary World, 6(10), 709-710. doi: 10.14202/vetworld.2013.709-710
Gheller, J. M., Carniel, R., Carrasco, A. O. T., & Seki, M. C. (2016). Occurrence and risk factors for Toxoplasma gondii and Neospora caninum in sheep of the Guarapuava region, Paraná, Brazil. Brazilian Journal of Veterinary Research and Animal Science, 53(2), 177-181. doi: 10.11606/issn.1678-4456 v53 i2p177-181
Guimarães, A., Raimundo, J. M., Moares, L. M. B., Silva, A. T., Santos, H. A., Pires, M. S.,... Baldani, C. D. (2015). Occurrences of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in sheep from four districts of Tocantins state, Brazilian Legal Amazon Region. Pesquisa Veterinária Brasileira, 35(2), 110-114. doi: 10.1590/S0100-736X2015000200002
Hecker, Y. P., Moore, D. P., Manazza, J. A., Unzaga, J. M., Späth, J. A., Pardini, L. L.,... Campero, C. M. (2013). First report of seroprevalence of Toxoplasma gondii and Neospora caninum in dairy sheep from Humid Pampa, Argentina. Tropical Animal Health and Production, 45(7), 1645-1647. doi: 10.1007s1 1250-013-0396-1
Helmick, B., Otter, A., Mcgarry, J., & Buxton, D. (2002). Serological investigation of aborted sheep and pigs for infection by Neospora caninum. Research in Veterinary Science, 73(2), 187-189. doi: 10.1016/S003 4-5288(02)00093-0
Liu, Z. K. B. C., Li, J. Y., & Pan, H. (2015). Seroprevalence and risk factors of Toxoplasma gondii and Neospora caninum infections in small ruminants in China. Preventive Veterinary Medicine, 118(4), 488-492. doi: 10.1016/j.prevetmed.2014.12.017
Maganga, G. D. B., Abessoloa, A. L., Okouyib, C. S. M., Laboubaa, I., Beyemeb, A. M. M., Mavoungoub, J. F.,… Akue, J. P. (2016). Seroprevalence and risk factors of two abortive diseases, toxoplasmosis and neosporosis, in small ruminants of the Mongo County, southern Gabon. Small Ruminant Research, 144, 56-61. doi: /10.1016/j.smallrumres.2016.07.022
Mcallister, M. M., Lindsay, D. S., Jolley, W. R., Wills, R. A., Mcguire, A. M., Tress, A. J., & Stobart, R. H. (1996). Experimental neosporosis in pregnant ewes and their offspring. Veterinary Pathology, 33(6), 647-655. doi: 10.1177/030098589603300603
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., Altman, D., Antes, G., & Tugwell, P. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Plos Medicine, 6(7), e1000097. doi: 10.1371/journal.pmed.1000097
Moraes, L. M. M. B., Raimundo, J. M., Guimarães, A., Santos, H. A., Macedo, G. L., Jr., Massard, C. L.,... Baldani,C.D. (2011). Occurrence of anti-Neospora caninum and anti-Toxoplasma gondii IgG antibodies in goats and sheep in western maranhão, Brazil. Revista Brasileira de Parasitologia Veterinaria, 20(4), 312-317. doi: 10.1590/S1984-29612011000400010
Moura, A. B. M., Güths, M. F., Farias, J. A., Souza, A. P., Sartor, A. A., & Quadros, R. M. (2014) Neospora caninum seroprevalence and risk factors for ewes from Santa Catarina Plateau, Brazil. Semina: Ciências Agrárias, 35(5), 2591-2600. doi: 10.5433/1679-0359.2014v35n5p2591
Munhóz, K. F., Luca, M. M. de, Neto, Almeida-Santos, S. M. de, Garcia, J. L., Silva-Guimarães, J. da, Vidotto, O., & Yamamura, M. H. (2010). Occurrence of anti-Neospora caninum antibodies in sheep from farms located in northern Parana, Brazil. Semina: Ciencias Agrarias, 31(4), 1031-1040.
R Core Team (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from URL https://www.R-project.org/
Rocha, D. D. S., Guimarães, L. A., Bezerra, R. A., Mendonça, C. E. A., Dórea, T. G., Munhoz, A. D., & Albuquerque, G. R. (2014). Seroprevalence and factors associated with Neospora caninum infection in sheep from southeastern Bahia, Brazil. Revista Brasileira de Medicina Veterinaria, 36(4), 1-5.
Romanelli, P. R., Freire, R. L., Vidotto, O., Marana, E. R., Ogawa, L., Paula, V. S. O. de,... Navarro, I. T. (2007). Prevalence of Neospora caninum and Toxoplasma gondii in sheep and dogs from Guarapuava farms, Paraná State, Brazil. Research in Veterinary Science, 82(2), 202-207. doi: 10.1016/j.rvsc.2006.0 4.001
Romanelli, P. R. (2002). Avaliação soroepidemiológica de Neospora caninum e Toxoplasma gondii em ovinos do município de Guarapuava-Paraná. Dissertação de mestrado em SanidadeAnimal, Faculdade de Medicina Veterinária, Universidade Estadual de Londrina, PR, Brasil.
Salaberry, S. R. S., Okuda, L. H., Nassar, A. F. C., Castro, J. R., Lima-Ribeiro, A. M. C. (2010). Prevalence of Neospora caninum antibodies in sheep flocks of Uberlandia county, MG. Revista Brasileira de Parasitologia Veterinária, 19(3), 148-151. doi: 10.1590/S1984-29612010000300004
Schwarzer, G. (2007). Meta: An R package for meta-analysis. R news, 7(3), 40-45.
Silva, A. P. S. P., Santos, D. V., Kohek, I., Machado, G., Hein, H. E., Vidor, A. C. M., & Corbellini, L. G. (2013). Ovinocultura do Rio Grande do Sul: descrição do sistema produtivo e dos principais aspectos sanitários e reprodutivos. Pesquisa Veterinaria Brasileira, 33(12), 1453-1458. doi: 10.1590/S0100-736 X2013001200010
Tembue, A. A. S. M., Ramos, R. A. N., Sousa, T. R., Alburquerque, A. R., Costa, A. J., Meunier, I. M. J.,... Alves, L.C. (2011). Serological survey of Neospora caninum in small ruminants from Pernambuco State, Brazil. Revista Brasileira de Parasitologia Veterinária, 20(3), 246-248. doi: 10.1590/S1984-2961 2011000300013
Tzanidakis, N., Maksimov, P., Conraths, F. J., Kiossis, E., Brozos, C., Sotiraki, S., & Schares, G. (2012). Toxoplasma gondii in sheep and goats: Seroprevalence and potential risk factors under dairy husbandry practices. Veterinary Parasitology, 190(3-4), 340-348. doi: 10.1016/j.vetpar.2012.07.020
Ueno, T. E. H., Gonçalves, V. S. P., Heinemann, M. B., Dilli, T. L. B., Akimoto, B. M., Souza, S. L. P.,… Soares, R. M. (2009). Prevalence of Toxoplasma gondii and Neospora caninum infections in sheep from Federal District, central region of Brazil. Tropical Animal Health Production, 41, 547-552. doi: 10.100 7/s11250-008-9220-8
Viechtbauer, W. (2010). Conducting meta-analyses in R with the metaphor package. Journal of Statistical Software, 36(3), 1-48. doi: 10.18637/jss.v036.i03
Al-Majali, A. M., Jawasreh, K. I., Talafha, H. A., & Talafha, A. Q. (2008). Neosporosis in sheep and different breeds of goats from southern jordan: prevalence and risk factors analysis. American Journal of Animal and Veterinary Sciences, 3(2), 47-52.
Almeida, J. C. de, Kim, P. de C. P., Melo, R. P. B. de, Nogueira, J. F., Martins, F. D. C., Garcia, J. L.,... Mota, R. A. (2019). Neospora caninum DNA in feces of crab-eating fox (Cerdocyon thous - Linnaeus, 1776) from northeastern Brazil. Acta Tropica, 197, 105068. doi: 10.1016/j.actatropica.2019.105068
Andrade, G. S., Bruhna, F. R. P, Rocha, C. M. B. M., Guimarães, A. S., Gouveia, A. M. G., & Guimarães, A. M. (2012). Seroprevalence and risk factors for Neospora caninum in sheep in the state Minas Gerais, southeastern Brazil. Veterinary Parasitology, 188(1-2), 168-171. doi: 10.1016/j.vetpar.2012.03.006
Arraes-Santos, A. I., Araújo, A. C., Guimarães, M. F., Santos, J. R., Pena, H. F. J., Gennari, S. M.,... Horta, M. C. (2016). Seroprevalence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in domestic mammals from two distinct regions in the semi-arid region of Northeastern Brazil. Veterinary Parasitology: Regional Studies and Reports, 5, 14-18. doi: 10.1016/j.vprsr.2016.08.007
Arranz-Solís, D., Benavides, J., Regidor-Cerrillo, J., Horcajo, P., Castaño, P., Del Carmen-Ferreras, M.,… Ortega-Mora, L. M. (2016). Systemic and local immune responses in sheep after Neospora caninum experimental infection at early, mid and late gestation. Veterinary Research, 47(1), 1-13. doi: 10.1186 s 13567-015-0290-0
Barling, K. S., Mcneill, J. W., Paschal, J. C., Mccollum, F. T., Craig, T. M., Adams, L. G., & Thompson, J. A. (2001). Ranch-management factors associated with antibody seropositivity for Neospora caninum in consignments of beef calves in Texas, USA. Preventive Veterinary Medicine, 52(1), 53-61. doi: 10.10 16/S0167-5877(01)00233-1
Castañeda-Hernández, A., Cruz-Vázquez, C., & Medina-Esparza, L. (2014). Neospora caninum: Seroprevalence and DNA detection in blood of sheep from Aguascalientes, Mexico. Small Ruminant Research, 119(1-3), 182-186. doi: 10.1016/j.smallrumres.2014.03.002
Cavalcante, A. C. R., Carneiro, M., Gouveia, A. M. G., Pinheiro, R. R., & Vitor, R. W. (2008). A. Risk factors for infection by Toxoplasma gondii in herds of goats in Ceará, Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 60(1), 36-41. doi: 10.1590/S0102-09352008000100006
Díaz, J. M., Fernández, G., Prieto, A., Valverde, S., Lago, N., Díaz, P.,... Díez-Baños, P. (2014). Epidemiology of reproductive pathogens in semi-intensive lamb-producing flocks in North-West Spain: a comparative serological study. Veterinary Journal, 200(2), 335-338. doi: 10.1016/j.tvjl.2014.02.022
Dijkstra, T. H., Barkema, H. W., Bjorkman, C., & Wouda, W. (2002). A high rate of seroconversion for Neospora caninum in a dairy herd without an obvious increased incidence of abortions. Veterinary Parasitology, 109(3-4), 203-211. doi: 10.1016/S0304-4017(02)00303-5
Dubey, J. P., & Schares, G. (2011). Neosporosis in animals - the last five years. Veterinary Parasitology, 180(1-2), 90-108. doi: 1016/j. vetpar.2011.05.031
Dubey, J. P., Hartley, W. J., Lindsay, D. S., & Topper, M. J. (1990). Fatal congenital Neospora caninum infection in a lamb. Journal of Parasitology, 76(1), 127-130. doi: 10.2307/3282640
Faria, E. B. E. F. T. S. F., Medeiros, E. S., Pinheiro, J. W., Jr., Azevedo, S. S., Atahayde, A. C. R., & Mota, R. A. (2010). Risk factors associated with Neospora caninum seropositivity in sheep from the state of Alagoas, in the northeast region of Brazil. Journal of Parasitology, 96(1), 197-199. doi: 10.1645/GE-21 76.1
Ferreira, M. S. T., Vogel, F. S. F., Sangioni, L. A., Cezar, A. S., & Menezes, F. R. (2016). Neospora spp. and Toxoplasma gondii infection in sheep flocks from Rio Grande do Sul, Brazil. Semina: Ciências Agrárias, 37(3), 1397-1406. doi: 10.5433/1679-0359.2016v37n3p1397
Figliuolo, L. P. C., Kasai, N., Ragozo, A. M. A., Paula, V. S. O., Dias, R. A., Souza, S. L. P., & Gennari, S. M. (2004). Prevalence of anti-Toxoplasma gondii and anti- Neospora caninum antibodies in ovine from São Paulo State, Brazil. Veterinary Parasitology, 123(3-4), 161-166. doi: 10.1016/j.vetpar.2004.06.006
Gazzonis, A. L., Garcia, G. A., Zanzania, S. A., Morab, L. M. O., Invernizzic, A., & Manfredia, M. T. (2016). Neospora caninum infection in sheep and goats from north-eastern Italy and associated risk factors. Small Ruminant Research, 140, 7-12. doi: 10.1016/j.smallrumres.2016.05.010
Gharekhani, J., Tavoosidana, G. R., & Zandieh, M. (2013). Seroprevalence of Neospora caninum in sheep from western Iran. Veterinary World, 6(10), 709-710. doi: 10.14202/vetworld.2013.709-710
Gheller, J. M., Carniel, R., Carrasco, A. O. T., & Seki, M. C. (2016). Occurrence and risk factors for Toxoplasma gondii and Neospora caninum in sheep of the Guarapuava region, Paraná, Brazil. Brazilian Journal of Veterinary Research and Animal Science, 53(2), 177-181. doi: 10.11606/issn.1678-4456 v53 i2p177-181
Guimarães, A., Raimundo, J. M., Moares, L. M. B., Silva, A. T., Santos, H. A., Pires, M. S.,... Baldani, C. D. (2015). Occurrences of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in sheep from four districts of Tocantins state, Brazilian Legal Amazon Region. Pesquisa Veterinária Brasileira, 35(2), 110-114. doi: 10.1590/S0100-736X2015000200002
Hecker, Y. P., Moore, D. P., Manazza, J. A., Unzaga, J. M., Späth, J. A., Pardini, L. L.,... Campero, C. M. (2013). First report of seroprevalence of Toxoplasma gondii and Neospora caninum in dairy sheep from Humid Pampa, Argentina. Tropical Animal Health and Production, 45(7), 1645-1647. doi: 10.1007s1 1250-013-0396-1
Helmick, B., Otter, A., Mcgarry, J., & Buxton, D. (2002). Serological investigation of aborted sheep and pigs for infection by Neospora caninum. Research in Veterinary Science, 73(2), 187-189. doi: 10.1016/S003 4-5288(02)00093-0
Liu, Z. K. B. C., Li, J. Y., & Pan, H. (2015). Seroprevalence and risk factors of Toxoplasma gondii and Neospora caninum infections in small ruminants in China. Preventive Veterinary Medicine, 118(4), 488-492. doi: 10.1016/j.prevetmed.2014.12.017
Maganga, G. D. B., Abessoloa, A. L., Okouyib, C. S. M., Laboubaa, I., Beyemeb, A. M. M., Mavoungoub, J. F.,… Akue, J. P. (2016). Seroprevalence and risk factors of two abortive diseases, toxoplasmosis and neosporosis, in small ruminants of the Mongo County, southern Gabon. Small Ruminant Research, 144, 56-61. doi: /10.1016/j.smallrumres.2016.07.022
Mcallister, M. M., Lindsay, D. S., Jolley, W. R., Wills, R. A., Mcguire, A. M., Tress, A. J., & Stobart, R. H. (1996). Experimental neosporosis in pregnant ewes and their offspring. Veterinary Pathology, 33(6), 647-655. doi: 10.1177/030098589603300603
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., Altman, D., Antes, G., & Tugwell, P. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Plos Medicine, 6(7), e1000097. doi: 10.1371/journal.pmed.1000097
Moraes, L. M. M. B., Raimundo, J. M., Guimarães, A., Santos, H. A., Macedo, G. L., Jr., Massard, C. L.,... Baldani,C.D. (2011). Occurrence of anti-Neospora caninum and anti-Toxoplasma gondii IgG antibodies in goats and sheep in western maranhão, Brazil. Revista Brasileira de Parasitologia Veterinaria, 20(4), 312-317. doi: 10.1590/S1984-29612011000400010
Moura, A. B. M., Güths, M. F., Farias, J. A., Souza, A. P., Sartor, A. A., & Quadros, R. M. (2014) Neospora caninum seroprevalence and risk factors for ewes from Santa Catarina Plateau, Brazil. Semina: Ciências Agrárias, 35(5), 2591-2600. doi: 10.5433/1679-0359.2014v35n5p2591
Munhóz, K. F., Luca, M. M. de, Neto, Almeida-Santos, S. M. de, Garcia, J. L., Silva-Guimarães, J. da, Vidotto, O., & Yamamura, M. H. (2010). Occurrence of anti-Neospora caninum antibodies in sheep from farms located in northern Parana, Brazil. Semina: Ciencias Agrarias, 31(4), 1031-1040.
R Core Team (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from URL https://www.R-project.org/
Rocha, D. D. S., Guimarães, L. A., Bezerra, R. A., Mendonça, C. E. A., Dórea, T. G., Munhoz, A. D., & Albuquerque, G. R. (2014). Seroprevalence and factors associated with Neospora caninum infection in sheep from southeastern Bahia, Brazil. Revista Brasileira de Medicina Veterinaria, 36(4), 1-5.
Romanelli, P. R., Freire, R. L., Vidotto, O., Marana, E. R., Ogawa, L., Paula, V. S. O. de,... Navarro, I. T. (2007). Prevalence of Neospora caninum and Toxoplasma gondii in sheep and dogs from Guarapuava farms, Paraná State, Brazil. Research in Veterinary Science, 82(2), 202-207. doi: 10.1016/j.rvsc.2006.0 4.001
Romanelli, P. R. (2002). Avaliação soroepidemiológica de Neospora caninum e Toxoplasma gondii em ovinos do município de Guarapuava-Paraná. Dissertação de mestrado em SanidadeAnimal, Faculdade de Medicina Veterinária, Universidade Estadual de Londrina, PR, Brasil.
Salaberry, S. R. S., Okuda, L. H., Nassar, A. F. C., Castro, J. R., Lima-Ribeiro, A. M. C. (2010). Prevalence of Neospora caninum antibodies in sheep flocks of Uberlandia county, MG. Revista Brasileira de Parasitologia Veterinária, 19(3), 148-151. doi: 10.1590/S1984-29612010000300004
Schwarzer, G. (2007). Meta: An R package for meta-analysis. R news, 7(3), 40-45.
Silva, A. P. S. P., Santos, D. V., Kohek, I., Machado, G., Hein, H. E., Vidor, A. C. M., & Corbellini, L. G. (2013). Ovinocultura do Rio Grande do Sul: descrição do sistema produtivo e dos principais aspectos sanitários e reprodutivos. Pesquisa Veterinaria Brasileira, 33(12), 1453-1458. doi: 10.1590/S0100-736 X2013001200010
Tembue, A. A. S. M., Ramos, R. A. N., Sousa, T. R., Alburquerque, A. R., Costa, A. J., Meunier, I. M. J.,... Alves, L.C. (2011). Serological survey of Neospora caninum in small ruminants from Pernambuco State, Brazil. Revista Brasileira de Parasitologia Veterinária, 20(3), 246-248. doi: 10.1590/S1984-2961 2011000300013
Tzanidakis, N., Maksimov, P., Conraths, F. J., Kiossis, E., Brozos, C., Sotiraki, S., & Schares, G. (2012). Toxoplasma gondii in sheep and goats: Seroprevalence and potential risk factors under dairy husbandry practices. Veterinary Parasitology, 190(3-4), 340-348. doi: 10.1016/j.vetpar.2012.07.020
Ueno, T. E. H., Gonçalves, V. S. P., Heinemann, M. B., Dilli, T. L. B., Akimoto, B. M., Souza, S. L. P.,… Soares, R. M. (2009). Prevalence of Toxoplasma gondii and Neospora caninum infections in sheep from Federal District, central region of Brazil. Tropical Animal Health Production, 41, 547-552. doi: 10.100 7/s11250-008-9220-8
Viechtbauer, W. (2010). Conducting meta-analyses in R with the metaphor package. Journal of Statistical Software, 36(3), 1-48. doi: 10.18637/jss.v036.i03
Downloads
Published
2021-04-22
How to Cite
Romanelli, P. R., Caldart, E. T., Martins, F. D. C., Martins, C. M., Matos, A. M. R. N. de, Pinto-Ferreira, F., … Navarro, I. T. (2021). Seroprevalence and associated risk factors of ovine neosporosis worldwide: a systematic review and meta-analysis. Semina: Ciências Agrárias, 42(3Supl1), 2111–2126. https://doi.org/10.5433/1679-0359.2021v42n3Supl1p2111
Issue
Section
Review Article
License
Copyright (c) 2021 Semina: Ciências Agrárias
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Semina: Ciências Agrárias adopts the CC-BY-NC license for its publications, the copyright being held by the author, in cases of republication we recommend that authors indicate first publication in this journal.
This license allows you to copy and redistribute the material in any medium or format, remix, transform and develop the material, as long as it is not for commercial purposes. And due credit must be given to the creator.
The opinions expressed by the authors of the articles are their sole responsibility.
The magazine reserves the right to make normative, orthographic and grammatical changes to the originals in order to maintain the cultured standard of the language and the credibility of the vehicle. However, it will respect the writing style of the authors. Changes, corrections or suggestions of a conceptual nature will be sent to the authors when necessary.
