Advertisement

Tropical Animal Health and Production

, Volume 51, Issue 7, pp 1783–1800 | Cite as

Meta-analysis of the prevalence and risk factors associated with bovine neosporosis

  • Claudia Mello RibeiroEmail author
  • Isabela Ribeiro Soares
  • Rodrigo Guerrero Mendes
  • Paula Andrea de Santis Bastos
  • Satie Katagiri
  • Renato Bacarin Zavilenski
  • Hudson Felipe Porto de Abreu
  • Vera Afreixo
Reviews
  • 119 Downloads

Abstract

Neospora caninum is one of the main infectious agents that cause reproductive disorders in cattle. However, knowledge about the prevalence and causal factors of bovine neosporosis is needed in order to establish control measures. The purpose of this study was to estimate the pooled prevalence and determine the risk factors of bovine neosporosis using meta-analytic methods. Searches for data on N. caninum seroprevalence and potential risk factors were conducted in the PubMed, LILACS, and SciElo databases. The random effects model was used for the meta-analysis of the included studies. The pooled prevalence of N. caninum in cattle was 24% (95% confidence interval (CI), 19–29) in North and Central America, 24% (95% CI, 20–28) in South America, 18% (95% CI, 14–21) in Asia, 15% (95% CI, 12–18) in Europe, 13% (95% CI, 11–16) in Africa, and 8% (95% CI, 4–14) in Oceania. A significant correlation was found between N. caninum infection and abortion in cows (odds ratio (OR) = 2.66, 95% CI, 1.97–3.59). The following risk factors were signicantly associated with N. caninum seroprevalence: presence of dogs on the farm (OR = 2.84; 95% CI, 1.40–5.80) and the type of cattle production system, with dairy cattle being more susceptible to bovine neosporosis (OR = 1.60; 95% CI, 1.16–2.19) than beef cattle. The adoption of measures to prevent the dissemination of N. caninum in cattle herds is suggested, aiming to reduce the economic losses incurred to the dairy and beef industry.

Keywords

Bovine neosporosis Prevalence Risk factors Meta-analysis 

Notes

Acknowledgements

We thank the Center for Research and Development in Mathematics and Applications (University of Aveiro) and the Portuguese Foundation for Science and Technology for grants to support this project (UID/MAT/04106/2013).

Compliance with ethical standards

Conflict interest

The authors declare that they have no conflict of interest.

References

  1. Achour, K., Ben-Mahdi, M.H., Akkou, M., and Teniou, R., 2012. Seroprevalence of Neospora caninum in dairy cattle farms in Algeria’s central northern region. Revue Scientifique et Technique, 31, 953–958Google Scholar
  2. Aguiar, D.M., Cavalcante, G.T., Rodrigues, A.A., Labruna, M.B., Camargo, L.M., Camargo, E.P., and Gennari, S.M., 2006. Prevalence of anti-Neospora caninum antibodies in cattle and dogs from Western Amazon, Brazil, in association with some possible risk factors. Veterinary Parasitology, 142, 71–77Google Scholar
  3. Akca, A., Gokce, H.I., Guy, C.S., McGarry, J.W., and Williams, D.J., 2005. Prevalence of antibodies to Neospora caninum in local and imported cattle breeds in the Kars province of Turkey. Research in Veterinary Science, 78, 123–126Google Scholar
  4. Almería, S., López-Gatius, F., García-Ispierto, I., Nogareda, C., Bech-Sàbat, G., Serrano, B., Santolaria, P., and Yániz, J.L., 2009. Effects of crossbreed pregnancies on the abortion risk of Neospora caninum-infected dairy cows. Veterinary Parasitology, 163, 323–329Google Scholar
  5. Amaral, R.L.G., Silva, L.B.G., Pinheiro Júnior, J.W., Souza Neto, O.L., Leal, C.A.S., Porto, W.J.N., Barbosa, J.M.P., and Mota, R.A., 2012. Neospora caninum em bovinos em matadouros de Pernambuco e Alagoas. Pesquisa Veteterinária Brasileira, 32, 953–966Google Scholar
  6. Ansari-Lari, M., Rowshan-Ghasrodashti, A., Jesmani, H., Masoudian, M., and Badkoobeh, M., 2017. Association of Neospora caninum with reproductive performance in dairy cows: a prospective study from Iran. Veterinary Research Forum: an International Quarterly Journal, 8, 109–114Google Scholar
  7. Armengol, R., Pabón, M., Santolaria, P., Cabezón, O., Adelantado, C., Yániz, J., López-Gatius, F., and Almería, S., 2007. Low seroprevalence of Neospora caninum infection associated with the limousin breed in cow-calf herds in Andorra, Europe. Journal of Parasitology, 93, 1029–1032Google Scholar
  8. Arreola-Camberos, S., Garcia-Marquez, L.J., Macedo-Barragan, R., Morales-Salinas, E., and Figueroa-Chavez, D., 2012. Risk factors and seroprevalence against Neospora caninum in dual-purpose and beef cattle in Colima, Mexico. Journal of Animal and Veterinary Advances: JAVA, 11, 2440–2444Google Scholar
  9. Asmare, K., Regassa, F., Robertson, L.J., and Skjerve, E., 2013. Seroprevalence of Neospora caninum and associated risk factors in intensive or semi-intensively managed dairy and breeding cattle of Ethiopia. Veterinary Parasitology, 193, 85–94Google Scholar
  10. Atkinson, R.A., Cook, R.W., Reddacliff, L.A., Rothwell, J., Broady, K.W., Harper, P., and Ellis, J.T., 2000. Seroprevalence of Neospora caninum infection following an abortion outbreak in a dairy cattle herd. Australian Veterinary Journal, 78, 262–266Google Scholar
  11. Atoccsa, J.H., Chávez, A.V., Casas, E.A., and Falcón, N.P., 2005. Seroprevalencia de Neospora caninum en bovinos lecheros criados al pastoreo en la provincia de Melgar, Puno. Revista de Investigaciones Veterinarias del Perú, 16, 71–75Google Scholar
  12. Ayinmode, A., Akinseye, V., Schares, G., and Cadmus, S., 2017. Serological survey of toxoplasmosis, neosporosis and brucellosis among cattle herds in Oyo State, south-western Nigeria. African Journal of Infectious Diseases, 11, 95–101Google Scholar
  13. Bae, J.S., Kim, D.Y., Hwang, W.S., Kim, J.H., Lee, N.S., and Nam, H.W., 2000. Detection of IgG antibody against Neospora caninum in cattle in Korea. The Korean Journal of Parasitology, 38, 245–249Google Scholar
  14. Bañales, P., Fernandez, L., Repiso, M.V., Gil, A., Dargatz, D.A., and Osawa, T., 2006. A nationwide survey on seroprevalence of Neospora caninum infection in beef cattle in Uruguay. Veterinary Parasitology, 139, 15–20Google Scholar
  15. Barling, K.S., McNeill, J.W., Thompson, J.A., Paschal, J.C., McCollum, F.T. 3rd, Craig, T.M., and Adams, L.G., 2000. Association of serologic status for Neospora caninum with postweaning weight gain and carcass measurements in beef calves. Journal of the American Veterinary Medical Association, 217, 1356–1360Google Scholar
  16. Barling, K.S., McNeill, J.W., Paschal, J.C., McCollum, F.T. 3rd, Craig, T.M., Adams, L.G., and 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, 53–61Google Scholar
  17. Bártová, E., Sedlak, K., and Budíková, M., 2015. A study of Neospora caninum and Toxoplasma gondii antibody seroprevalence in healthy cattle in the Czech Republic. Annals of Agricultural and Environmental Medicine: AAEM, 22, 32–34Google Scholar
  18. Beck, R., Marinculić, A., Mihaljević, Z., Benić, M., and Martinković, F., 2010. Seroprevalence and potential risk factors of Neospora caninum infection in dairy cattle in Croatia. Veterinarski Arhiv, 80, 163–171Google Scholar
  19. Benetti, A.H., Schein, F.B., dos Santos, T.R., Toniollo, G.H., da Costa, A.J., Mineo, J.R., Lobato, J., de Oliveira Silva, D.A., and Gennari, S.M., 2009. Pesquisa de anticorpos anti-Neospora caninum em bovinos leiteiros, cães e trabalhadores rurais da região Sudoeste do Estado de Mato Grosso. Revista Brasileira de Parasitologia Veterinária, 1, 29–133Google Scholar
  20. Bergeron, N., Fecteau, G., Paré, J., Martineau, R., and Villeneuve, A., 2000. Vertical and horizontal transmission of Neospora caninum in dairy herds in Québec. Canadian Veterinary Journal, 41, 464–467Google Scholar
  21. Björkman, C., Johansson, O., Stenlund, S., Holmdahl, O.J., and Uggla, A., 1996. Neospora species infection in a herd of dairy cattle. Journal of the American Veterinary Medical Association, 208, 1441–1444Google Scholar
  22. Björkman, C., Alenius, S., Manuelsson, U., and Uggla, A., 2000. Neospora caninum and bovine virus diarrhoea virus infections in Swedish dairy cows in relation to abortion. The Veterinary Journal, 159, 201–206Google Scholar
  23. Boas, R.V., Pacheco, T.A., Melo, A.L., de Oliveira, A.C., de Aguiar, D.M., and Pacheco, R.C., 2015. Infecção por Neospora caninum em bovinos leiteiros de agricultores familiares da região norte do Brasil. Revista Brasileria de Parasitologia Veterinária, 24, 204–208Google Scholar
  24. Brickell, J.S., McGowan, M.M., and Wathes, D.C., 2010. Association between Neospora caninum seropositivity and perinatal mortality in dairy heifers at first calving. The Veterinary Record, 167, 82–85Google Scholar
  25. Bruhn, F.R., Daher, D.O., Lopes, E., Barbieri, J.M., da Rocha, C.M., and Guimarães, A.M., 2013. Factors associated with seroprevalence of Neospora caninum in dairy cattle in southeastern Brazil. Tropical Animal Health and Production, 45, 1093–1098Google Scholar
  26. Buxton, D., Caldow, G.L., Maley, S.W., Marks, J., and Innes, E.A., 1997. Neosporosis and bovine abortion in Scotland. The Veterinary Record, 141, 649–651Google Scholar
  27. Cadore, G.C., Vogel, F.S.F., Sangioni, L.A., Pena, H.F.J., and Gennari, S.M., 2010. IgM e IgG como marcadores da infecção transplacentária por Neospora caninum em fetos bovinos. Pesquisa Veterinária Brasileira, 30, 551–553Google Scholar
  28. Caetano-da-Silva, A., Ferre, I., Aduriz, G., Alvarez-García, G., del Pozo, I., Atxaerandio, R., Regidor-Cerrillo, J., Ugarte-Garagalza, C., Ortega-Mora, L.M., 2004. Neospora caninum infection in breeder bulls: seroprevalence and comparison of serological methods used for diagnosis. Veterinay Parasitology, 124, 19–24Google Scholar
  29. Camillo, G., Cadore, G., Cezar, A.S., Toscan, G., Bräunig, P., Sangioni, L.A., and Vogel, F.S.F., 2010. Anticorpos anti-Neospora caninum em bovinos de leite do sudoeste do estado do Paraná. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 62, 1511–1513Google Scholar
  30. Castilleja, Y.M.S., Rodríguez, D.J.G., and Pedroso, M., 2010. Correlación serológica de Brucella abortus y Neospora caninum en ganado bovino en el estado de hidalgo, México. The Journal Salud Animal, 32, 57–59Google Scholar
  31. Chahan, B., Gaturaga, I., Huang, X., Liao, M., Fukumoto, S., Hirata, H., Nishikawa, Y., Suzuki, H., Sugimoto, C., Nagasawa, H., Fujisaki, K., Igarashi, I., Mikami, T., Xuan, X., 2003. Serodiagnosis of Neospora caninum infection in cattle by enzyme-linked immunosorbent assay with recombinant truncated NcSAG1. Veterinary Parasitology, 118,177–185Google Scholar
  32. Chiebao, D.P., Valadas, S.Y., Minervino, A.H., Castro, V., Romaldini, A.H., Calhau, A.S., De Souza, R.A., Gennari, S.M., Keid, L.B., and Soares, R.M., 2015. Variables associated with infections of cattle by Brucella abortus, Leptospira spp. and Neospora spp. in Amazon Region in Brazil. Transboundary and Emerging Diseases, 62, e30–36Google Scholar
  33. Corbellini, L.G., Driemeier, D., Cruz, C.F., Gondim, L.F., and Wald, V., 2002. Neosporosis as a cause of abortion in dairy cattle in Rio Grande do Sul, southern Brazil. Veterinary Parasitology, 103, 195–202Google Scholar
  34. Corbellini, L.G., Smith, D.R., Pescador, C.A., Schmitz, M., Correa, A., Steffen, D.J., and Driemeier, D., 2006. Herd-level risk factors for Neospora caninum seroprevalence in dairy farms in southern Brazil. Preventive Veterinary Medicine, 74, 130–141Google Scholar
  35. Costa, G.H.N., Cabral, D.D., Varandas, N.P., Sobral, E.A., Borges, F.A., and Castagnolli, K.C., 2001. Frequence of antibodies for Neospora caninum and Toxoplasma gondii in cattle, São Paulo and Minas Gerais States. Semina: Ciências Agrárias, 22, 61–66Google Scholar
  36. Cramer, G., Kelton, D., Duffield, T.F., Hobson, J.C., Lissemore, K., Hietala, S.K., and Peregrine, A.S., 2002. Neospora caninum serostatus and culling of Holstein cattle. Journal of the American Veterinary Medical Association 221, 1165–1168Google Scholar
  37. De Meerschman, F., Focant, C., Boreux, R., Leclipteux, T., Losson, B., and Czaplicki, G., 2000. Cattle neosporosis in Belgium: a case-control study in dairy and beef cattle. The International Journal for Parasitology, 30, 887–890Google Scholar
  38. De Meerschman, F., Speybroeck, N., Berkvens, D., Rettignera, C., Focant, C., Leclipteux, T., Cassart, D., and Losson, B., 2002. Fetal infection with Neospora caninum in dairy and beef cattle in Belgium. Theriogenology, 58, 933–945Google Scholar
  39. Deng, L., and He, C., 2013. First report of Neospora caninum seroprevalence in dairy cattle in Jiangxi Province, Southeastern China. Journal of Animal and Veterinary Advances: JAVA, 12, 1131–1133Google Scholar
  40. Derdour, S.Y., Hafsi, F., Azzag, N., Tennah, S., Laamari, A., China, B., and Ghalmi, F., 2017. Prevalence of the main infectious causes of abortion in dairy cattle in Algeria. Journal of Veterinary Research, 61, 337–343Google Scholar
  41. DerSimonian, R., and Laird, N., 2015. Meta-analysis in clinical trials revisited. Contemporary Clinical Trials, 45, 139–145Google Scholar
  42. Duong, M.C., Alenius, S., Huong, L.T., and Björkman, C., 2008. Prevalence of Neospora caninum and bovine viral diarrhoea virus in dairy cows in Southern Vietnam. The Veterinary Journal, 175, 390–394Google Scholar
  43. Eiras, C., Arnaiz, I., Alvarez-García, G., Ortega-Mora, L.M., Sanjuánl, M.L., Yus, E., and Diéguez, F.J., 2011. Neospora caninum seroprevalence in dairy and beef cattle from the northwest region of Spain, Galicia. Preventive Veterinary Medicine, 98, 128–132Google Scholar
  44. Enachescu, V., Ionita, M., and Mitrea, I.L., 2014. Comparative study for the detection of antibodies to Neospora caninum in milk and sera in dairy cattle in southern Romania. Acta Parasitologica, 59, 5–10Google Scholar
  45. Fávero, J.F., Da Silva, A.S., Campigotto, G., Machado, G., Daniel, B.L., Garcia, J.L., Vogel, F.F., Mende, R.E., and Stefani, L.M., 2017. Risk factors for Neospora caninum infection in dairy cattle and their possible cause-effect relation for disease. Microbial Pathogenesis, 110, 202–207Google Scholar
  46. Fereig, R.M., AbouLaila, M.R., Mohamed, S.G.A., Mahmoud, H.Y.A.H., Ali, A.O., Ali, A.F., Hilali, M., Zaid, A., Mohamed, A.E.A., and Nishikawa, Y., 2016. Serological detection and epidemiology of Neospora caninum and Cryptosporidium parvum antibodies in cattle in southern Egypt. Acta Tropica, 162, 206–211Google Scholar
  47. Fort, M., Edelsten, M., Maley, S., and Innes, E., 2015. Seroepidemiological study of Neospora caninum in beef and dairy cattle in La Pampa, Argentina. Acta Parasitologica, 60, 275–282Google Scholar
  48. Furtado, A., Rosadilla, D., Cattáneo, M., Bermúdez, J., and Puentes, R., 2011. Ocorrência de anticorpos anti-Neospora caninum em pequenas propriedades leiteiras do Uruguai. Ciência Rural, 41, 673–675Google Scholar
  49. García-Vázquez, Z., Cruz-Vázquez, C., Medina-Espinoza, L., García-Tapia, D., and Chavarria-Martinez, B., 2002. Serological survey of Neospora caninum infection in dairy cattle herds in Aguascalientes, Mexico. Veterinary Parasitology, 106, 115–120Google Scholar
  50. Garcia-Vazquez, Z., Rosario-Cruz, R., Mejia-Estrada, F., Rodriguez-Vivas, I., Romero-Salas, D., Fernandez-Ruvalcaba, M., and Cruz-Vazquez, C., 2009. Seroprevalence of Neospora caninum antibodies in beef cattle in three southern states of Mexico. Tropical Animal Health and Production, 41, 749–753Google Scholar
  51. Gavrea, R.R., Iovu, A., Losson, B., and Cozma, V., 2011. Seroprevalence of Neospora caninum in dairy cattle from north-west and centre of Romania. Parasite, 18, 349–351Google Scholar
  52. Ghalmi, F., China, B., Ghalmi, A., Hammitouche, D., and Losson, B., 2012. Study of the risk factors associated with Neospora caninum seroprevalence in Algerian cattle populations. Research in Veterinary Science, 93, 655–661Google Scholar
  53. Gharekhani, J., Haddadzadeh, H., and Bahonar, A., 2014. Prevalence of immunoglobulin G (IgG) antibody to Neospora caninum in dairy cattle of Hamedan province, west of Iran. Veterinary Research Forum: an International Quarterly Journal, 5, 149–152Google Scholar
  54. Gindri, P.C., Mion, B., Pradieé, J., Bialves, T.S., Souza, G.N., Dellagostin, O.A., Schneider, A., and Pegoraro, L.M.C., 2018. Estimativa da soroprevalência e fatores de risco para neosporose em rebanhos leiteiros na região Noroeste do estado do Rio Grande do Sul, Brasil. Ciência Rural, 48, e20170921Google Scholar
  55. Gondim, L.F., Sartor, I.F., Hasegawa, M., and Yamane, I., 1999. Seroprevalence of Neospora caninum in dairy cattle in Bahia, Brazil. Veterinary Parasitology, 86, 71–75Google Scholar
  56. González, J.J.G., Cruz-Vázquez, C., Esparza, L.M., Flores, A.V., Ojeda, E.I., and García-Vázquez, Z., 2007. Management factors associated with seroprevalence to Neospora caninum infection in dairy cattle in Aguascalientes, Mexico. Veterinaria México, 38, 261–270Google Scholar
  57. González-Warleta, M., Castro-Hermida, J.A., Carro-Corral, C., Cortizo-Mella, J., and Mezo, M., 2008. Epidemiology of neosporosis in dairy cattle in Galicia (NW Spain). Parasitology Research, 102, 243–249Google Scholar
  58. Goodswen, S.J., Kennedy, P.J., and Ellis, J.T., 2013. A review of the infection, genetics, and evolution of Neospora caninum: from the past to the present. Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 13, 133–150Google Scholar
  59. Gottstein, B., Hentrich, B., Wyss, R., Thür, B., Busato, A., Stärk, K.D., and Müller, N., 1998. Molecular and immunodiagnostic investigations on bovine neosporosis in Switzerland. International Journal for Parasitology, 28, 679–691Google Scholar
  60. Guedes, M.H.P., Guimarães, A.M., Rocha, C.M.B.M., and Hirsch, C., 2008. Freqüência de anticorpos anti-Neospora caninum em vacas e fetos provenientes de municípios do sul de Minas Gerais. Revista Brasileira de Parasitologia Veterinária, 17, 189–194Google Scholar
  61. Guimarães, J.S. Jr, Souza, S.L., Bergamaschi, D.P., and Gennari, S.M., 2004. Prevalence of Neospora caninum antibodies and factors associated with their presence in dairy cattle of the north of Paraná state, Brazil. Veterinary Parasitology, 124, 1–8Google Scholar
  62. Hasegawa, M.Y., Sartor, I.F., Canavessi, A.M.O., and Pinckney, R.D., 2004. Ocorrência de anticorpos anti-Neospora caninum em bovinos de corte e em cães rurais da região de Avaré, Estado de São Paulo, Brasil. Semina: Ciências Agrárias, 25, 45–50Google Scholar
  63. Heidari, H., Mohammadzadeh, A., and Gharekhani, J., 2014. Seroprevalence of Neospora caninum in slaughtered native cattle in Kurdistan province, Iran. Veterinary Research Forum: an International Quarterly Journal, 5, 69–72Google Scholar
  64. Higgins, J.P., Thompson, S.G., Deeks, J.J., and Altman, D.G., 2003. Measuring inconsistency in meta-analyses. BMJ (Clinical research edn.), 327, 557–560Google Scholar
  65. Hobson, J.C., Duffield, T.F., Kelton, D., Lissemore, K., Hietala, S.K., Leslie, K.E., McEwen, B., Cramer, G., and Peregrine, A.S., 2002. Neospora caninum serostatus and milk production of Holstein cattle. Journal of the American Veterinary Medical Association, 221, 1160–1164Google Scholar
  66. Hobson, J.C., Duffield, T.F., Kelton, D., Lissemore, K., Hietala, S.K., Leslie, K.E., McEwen, B., and Peregrine, A.S., 2005. Risk factors associated with Neospora caninum abortion in Ontario Holstein dairy herds. Veterinary Parasitology, 127, 177–188Google Scholar
  67. Hornok, S., Edelhofer, R., and Hajtós, I., 2006. Seroprevalence of neosporosis in beef and dairy cattle breeds in Northeast Hungary. Acta Veterinaria Hungarica, 54, 485–491Google Scholar
  68. Hosseininejad, M., Mahzounieh, M., and Shams Esfandabadi, N., 2017. Neospora caninum suspects as one of the most important causes of abortion in large dairy farms in Isfahan, Iran. Iranian Journal of Parasitology, 12, 408–412Google Scholar
  69. Huong, L.T., Ljungström, B.L., Uggla, A., and Björkman, C., 1998. Prevalence of antibodies to Neospora caninum and Toxoplasma gondii in cattle and water buffaloes in southern Vietnam. Veterinary Parasitology, 75, 53–57Google Scholar
  70. Ibrahim, H.M., Huang, P., Salem, T.A., Talaat, R.M., Nasr, M.I., Xuan, X., and Nishikawa, Y., 2009. Short report: prevalence of Neospora caninum and Toxoplasma gondii antibodies in northern Egypt. The American Journal of Tropical Medicine and Hygiene, 80, 263–267Google Scholar
  71. Ibrahim, A.M., Elfahal, A.M., and El Hussein, A.R., 2012. First report of Neospora caninum infection in cattle in Sudan. Tropical Animal Health and Production, 44, 769–772Google Scholar
  72. Ichikawa-Seki, M., Guswanto, A., Allamanda, P., Mariamah, E.S., Wibowo, P.E., and Nishikawa, Y., 2016. Seroprevalence of antibody to NcSAG1 antigen of Neospora caninum in cattle from Western Java, Indonesia. The Journal of Veterinary Medical Science, 78, 121–123Google Scholar
  73. İça, A., Yildirim, A., Düzlü, O., and İnci, A., 2006. Kayseri yöresinde sığırlarda Neospora caninum’un seroprevalansı. Türkiye Parazitoloji Dergisi, 30, 92–94Google Scholar
  74. Imre, K., Morariu, S., Ilie, M.S., Imre, M., Ferrari N., Genchi C., and Dărăbuş G., 2012. Serological survey of Neospora caninum infection in cattle herds from Western Romania. Journal of Parasitolog, 98, 683–685Google Scholar
  75. Inpankaew, T., Jittapalapong, S., Mitchell, T.J., Sununta, C., Igarashi, I., and Xuan, X., 2014. Seroprevalence of Neospora caninum infection in dairy cows in Northern provinces, Thailand. Acta Parasitologica, 59, 305–309Google Scholar
  76. Jenkins, M.C., Caver, J.A., Björkman, C., Anderson, T.C., Romand, S., Vinyard, B., Uggla, A., Thulliez, P., and Dubey, J.P., 2000. Serological investigation of an outbreak of Neospora caninum-associated abortion in a dairy herd in southeastern United States. Veterinary Parasitology, 94, 17–26Google Scholar
  77. Jensen, A.M., Björkman, C., Kjeldsen, A.M., Wedderkopp, A., Willadsen, C., Uggla, A., and Lind, P., 1999. Associations of Neospora caninum seropositivity with gestation number and pregnancy outcome in Danish dairy herds. Preventive Veterinary Medicine, 40, 151–163Google Scholar
  78. Justo, R.V., Manfio, J.B., Galhardo, J.A., Garcia, J.L., and Campos, A.K., 2013. Inquérito soro-epidemiológico sobre neosporose bovina no norte do estado de Mato Grosso, Brasil. Semina: Ciências Agrárias, 34, 3897–3902Google Scholar
  79. Kamga-Waladjo, A.R., Gbati, O.B., Kone, P., Lapo, R.A., Chatagnon, G., Bakou, S.N., Pangui, L.J., Diop Pel, H., Akakpo, J.A., and Tainturier, D., 2010. Seroprevalence of Neospora caninum antibodies and its consequences for reproductive parameters in dairy cows from Dakar-Senegal, West Africa. Tropical Animal Health and Production, 42, 953–959Google Scholar
  80. Kim, J.H., Lee, J.K., Hwang, E.K., and Kim, D.Y., 2002. Prevalence of antibodies to Neospora caninum in Korean native beef cattle. The Journal of Veterinary Medical Science, 64, 941–943Google Scholar
  81. Koiwai, M., Hamaoka, T., Haritani, M., Shimizu, S., Tsutsui, T., Eto, M., and Yamane, I., 2005. Seroprevalence of Neospora caninum in dairy and beef cattle with reproductive disorders in Japan. Veterinary Parasitology, 130, 15–18Google Scholar
  82. Koiwai, M., Hamaoka, T., Haritani, M., Shimizu, S., Zeniya, Y., Eto, M., Yokoyama, R., Tsutsui, T., Kimura, K., and Yamane, I., 2006. Nationwide seroprevalence of Neospora caninum among dairy cattle in Japan. Veterinary Parasitology, 135, 175–179Google Scholar
  83. Konnai, S., Mingala, C.N., Sato, M., Abes, N.S., Venturina, F.A., Gutierrez, C.A., Sano, T., Omata, Y., Cruz, L.C., Onuma, M., and Ohashi K., 2008. A survey of abortifacient infectious agents in livestock in Luzon, the Philippines, with emphasis on the situation in a cattle herd with abortion problems. Acta Tropica, 105, 269–273Google Scholar
  84. Kowalczyk, S.J., Czopowicz, M., Weber, C.N., Müller, E., Witkowski, L., and Kabam, J., 2016. Herd-level seroprevalence of Neospora caninum infection in dairy cattle in central and northeastern Poland. Acta Parasitologica, 61, 63–65Google Scholar
  85. Kuruca, L., Spasojević-Kosić, L., Simin, S., Savović, M., Lauš, S., and Lalošević, V., 2013. Neospora caninum antibodies in dairy cows and domestic dogs from Vojvodina, Serbia. Parasite, 20, 40Google Scholar
  86. Kyaw, T., Virakul, P., Muangyai, M., and Suwimonteerabutr, J., 2004. Neospora caninum seroprevalence in dairy cattle in central Thailand. Veterinary Parasitology, 121, 255–263Google Scholar
  87. Lee, M.K., Park, J.S., Kim, M.H., Park, D.Y., Kim, C.H., Kim, G.H., and Cho, J.H., 2011. Seroprevalence of antibodies to Neospora caninum and Toxoplasma gondii in cattle in northern area of Gyeongnam. Korean Journal of Veterinary Service, 34, 245–250Google Scholar
  88. Lista-Alves, D., Palomares-Naveda, R., Garcia, F., Obando, C., Arrieta, D., and Hoet, A.E., 2006. Serological evidence of Neospora caninum in dual-purpose cattle herds in Venezuela. Veterinary Parasitology, 136, 347–349Google Scholar
  89. Locatelli-Dittrich, R., Soccol, V.T., Richartz, R.R., Gasino-Joineau, M.E., Vinne, R., and Pinckney, R.D., 2001. Serological diagnosis of neosporosis in a herd of dairy cattle in southern Brazil. Journal of Parasitology, 87, 1493–1494Google Scholar
  90. Locatelli-Dittrich, R., Machado, P.C. Jr, Fridlund-Plugge, N., Richartz, R.R., Montiani-Ferreira, F., Patrício, L.F., Patrício, M.A., Joineau, M.G., and Pieppe, M., 2008. Determination and correlation of anti-Neospora caninum antibodies in cattle and dogs from Paraná, Brazil. Revista Brasileira de Parasitologia Veterinária, 1, 191–196Google Scholar
  91. Loobuyck, M., Frössling, J., Lindberg, A., and Björkman, C., 2009. Seroprevalence and spatial distribution of Neospora caninum in a population of beef cattle. Preventive Veterinary Medicine, 92, 116–122Google Scholar
  92. López-Gatius, F., Santolaria, P., Yániz, J.L., Garbayo, J.M., and Almería, S., 2005. The use of beef bull semen reduced the risk of abortion in Neospora-seropositive dairy cows. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health, 52, 88–92Google Scholar
  93. Lucchese, L., Benkirane, A., Hakimi, I., El Idrissi, A., and Natale, A., 2016. Seroprevalence study of the main causes of abortion in dairy cattle in Morocco. Veterinaria Italiana, 52, 13–19Google Scholar
  94. Macedo, C.A.B., Macedo, M.F.S.B., Cardim, S.T., Paiva, M.C., Taroda, A., Barros, L.D., Cunha, I.A., Zulpo, D.L., and Garcia, J.L., 2013. Neospora caninum: evaluation of vertical transmission in slaughtered dairy cows (Bos taurus). Revista Brasileira de Parasitologia Veterinaria, 22, 13–7Google Scholar
  95. Macedo, C.A.B., Macedo, M.F.S.B., Miura, A.C., Taroda, A., Cardim, S.T., Innes, E.A., Katzer, F., Cantón, G.J., Chianini, F., Headley, S.A., and Garcia, J.L., 2017. Occurrence of abortions induced by Neospora caninum in dairy cattle from Santa Catarina, southern Brazil. Revista Brasileira de Parasitologia Veterinaria, 26, 292–298Google Scholar
  96. Marques, F.A., Headley, A.S., Figueredo-Pereira, V., Taroda, A., Barros, L.D., Cunha, I.A., Munhoz, K., Bugni, F.M., Zulpo, D.L., Igarashi, M., Vidotto, O., Guimarães, J.S. Jr, and Garcia, J.L., 2011. Neospora caninum: evaluation of vertical transmission in slaughtered beef cows (Bos indicus). Parasitology Research, 108, 1015–1019Google Scholar
  97. Martinez, B.A., Leotti, V.B., Borba, M.R., Silva, G.S., and Corbellini, L.G., 2017. Can hierarchical modeling improve our understanding of bovine abortion due to Neospora caninum infection? Veterinary Parasitology, 237, 77–82Google Scholar
  98. Martins, A.A., Zamprogna, T.O., Lucas, T.M., Cunha, I.A.L., Garcia, J.L., and Silva, A.V., 2012. Frequency and risk factors for neosporosis in dairy farms of Umuarama, Pr, Brazil. Arquivos de Ciências Veterinárias e Zoologia da UNIPAR, 15, 137–142Google Scholar
  99. McAllister, M.M., 2016. Diagnosis and control of bovine neosporosis. Veterinary Clinics of North America: Food Animal Practice, 32, 443–463Google Scholar
  100. McNamee, P.T., Trees, A.J., Guy, F., Moffett, D., and Kilpatrick, D., 1996. Diagnosis and prevalence of neosporosis in cattle in Northern Ireland. The Veterinary Record, 138, 419–420Google Scholar
  101. Medellín, M.O.P., Anaya, A.M.D., García, D.J., and Becerra, R.J.A., 2013. Determinación de anticuerpos anti Neospora caninum en vacas de la provincia de Sugamuxi, Colombia. Revista Mexicana de Ciencias Pecuarias, 4, 501–506Google Scholar
  102. Meenakshi, Sandhu, K.S., Ball, M.S., Kumar, H., Sharma, S., Sidhu, P.K., Sreekumar, C., and Dubey, J.P., 2007. Seroprevalence of Neospora caninum antibodies in cattle and water buffaloes in India. The Journal of Parasitology, 93, 1374–1377Google Scholar
  103. Meirelles, A.C.F., Locatelli-Dittrich, R., Castilhos, B., and Busch, A.P.B., 2014. Concordância na detecção de anticorpos anti-Toxoplasma gondii e anti-Neospora caninum no sangue e no leite bovino pela reação de imunofluorescência indireta. Ciência Rural, 44, 2204–2209Google Scholar
  104. Mello, R.C., Andreotti, R., Barros, J.C., Tomich, R.G., Mello, A.K., Campolim, A.I., and Pellegrin, A.O., 2008. Epidemiologic survey of Neospora caninum in bovines of rural settlements in Corumbá, MS. Revista Brasileira de Parasitologia Veterinária, 17, 311–316Google Scholar
  105. Melo, C.B., Leite, R.C., Souza, G.N., and Leite, R.C., 2001. Freqüência de infecção por Neospora caninum em dois diferentes sistemas de produção de leite e fatores predisponentes à infecção em bovinos em Minas Gerais. Revista Brasileira de Parasitologia Veterinária, 10, 67–74Google Scholar
  106. Melo, C.B., Leite, R.C., Lobato, Z.I., and Leite, R.C., 2004. Infection by Neospora caninum associated with bovine herpesvirus 1 and bovine viral diarrhea virus in cattle from Minas Gerais State, Brazil. Veterinary Parasitology, 119, 97–105Google Scholar
  107. Melo, D.P., da Silva, A.C., Ortega-Mora, L.M., Bastos, S.A., Boaventura, C.M., 2006. Prevalence of antibodies anti-Neospora caninum in bovines from Anápolis and Goiânia microregions, Goiás, Brazil. Revista Brasileira de Parasitologia Veterinária, 15, 105–109Google Scholar
  108. Mineo, T.W.P., Alenius, S., Näslund, K., Montassier, H.J., and Björkman, C., 2006. Distribuição de anticorpos contra Neospora caninum, BVD e BHV-1 entre vacas de rebanhos leiteiros brasileiros com desordens reprodutivas. Revista Brasileira de Parasitologia Veterinária, 15, 188–119Google Scholar
  109. Minervino, A.H., Ragozo, A.M., Monteiro, R.M., Ortolani, E.L., and Gennari, S.M., 2008. Prevalence of Neospora caninum antibodies in cattle from Santarém, Pará, Brazil. Research in Veterinary Science, 84, 254–256Google Scholar
  110. Mitrea, I.L., Enachescu, V., Radulescu, R., and Ionita, M., 2012. Seroprevalence of Neospora caninum infection on dairy cattle in farms from Southern Romania. Journal of Parasitology, 98, 69–72Google Scholar
  111. Moher, D., Liberati, A., Tetzlaff, J., Altman, D.G., and PRISMA Group, 2009. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Medicine, 6, e1000097Google Scholar
  112. Moloney, B.J., Kirkland, P.D., and Heuer, C., 2017. Neospora caninum in beef herds in New South Wales, Australia. 1: seroprevalence study. Australian Veterinary Journal, 95, 72–79Google Scholar
  113. Moore, D.P., Campero, C.M., Odeón, A.C., Posso, M.A., Cano, D., Leunda, M.R., Basso, W., Venturini, M.C., Späth, E., 2002. Seroepidemiology of beef and dairy herds and fetal study of Neospora caninum in Argentina. Veterinary Parasitology, 107, 303–316Google Scholar
  114. Moore, D.P., Draghi, M.G., Campero, C.M., Cetrá, B., Odeón, A.C., Alcaraz, E., and Späth, E.A., 2003. Serological evidence of Neospora caninum infections in beef bulls in six counties of the Corrientes province, Argentina. Veterinary Parasitology, 114, 247–252Google Scholar
  115. Moore, D.P., Konrad, J.L., San Martino, S., Reichel, M.P., Cano, D.B., Méndez, S., Späth, E.J., Odeón, A.C., Crudeli, G., and Campero, C.M., 2014. Neospora caninum serostatus is affected by age and species variables in cohabiting water buffaloes and beef cattle. Veterinary Parasitology, 203, 259–263Google Scholar
  116. Morales, E., Trigo, F.J., Ibarra, F., Puente, E., and Santacruz, M., 2001. Seroprevalence study of bovine neosporosis in Mexico. Journal of Veterinary Diagnostic Investigation: Official Publication of the American Association of Veterinary Laboratory Diagnosticians, Inc, 13, 413–415Google Scholar
  117. Moré, G., Bacigalupe, D., Basso, W., Rambeaud, M., Beltrame, F., Ramirez, B., Venturini, M.C., and Venturini, L., 2009. Frequency of horizontal and vertical transmission for Sarcocystis cruzi and Neospora caninum in dairy cattle. Veterinary Parasitology, 160, 51–54Google Scholar
  118. Moura, A.B., Souza, A.P., Sartor, A.A., Bellato, V., and Teixeira, E.B., 2012. Neospora caninum antibodies in dairy cattle of Lages Municipality, Santa Catarina State, Brazil. Archivos de Medicina Veterinaria, 44, 117–122Google Scholar
  119. Munhoz, A.D., Flausino, W., Silva, R.T., Almeida, C.R.R., and Lopes, C.W.G., 2006. Distribuição de anticorpos contra Neospora caninum em vacas leiteiras dos municípios de Resende e Rio Claro, Estado do Rio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veterinária, 15, 101–104Google Scholar
  120. Nasir, A., Lanyon, S.R., Schares, G., Anderson, M.L., and Reichel, M.P., 2012. Sero-prevalence of Neospora caninum and Besnoitia besnoiti in South Australian beef and dairy cattle. Veterinary Parasitology, 186, 480–485Google Scholar
  121. Nazir, M.M., Maqbool, A., Khan, M.S., Sajjid, A., and Lindsay, D.S., 2013. Effects of age and breed on the prevalence of Neospora caninum in commercial dairy cattle from Pakistan. Journal of Parasitology, 99, 368–370Google Scholar
  122. Nematollahi, A., Jaafari, R., and Moghaddam, G., 2011. Seroprevalence of Neospora caninum infection in dairy cattle in Tabriz, Northwest Iran. Iranian Journal of Parasitology, 6, 95–98Google Scholar
  123. Nematollahi, A., Moghaddam, G.H., Jaafari, R., Helan, J.A., and Norouzi, M., 2013. Study on outbreak of Neospora caninum-associated abortion in dairy cows in Tabriz (Northwest Iran) by serological, molecular and histopathologic methods. Asian Pacific Journal of Tropical Medicine, 6, 942–946Google Scholar
  124. Njiro, S.M., Kidanemariam, A.G., Tsotetsi, A.M., Katsande, T.C., Mnisi, M., Lubisi, B.A., Potts, A.D., Baloyi, F., Moyo, G., Mpofu, J., Kalake, A., and Williams, R., 2011. A study of some infectious causes of reproductive disorders in cattle owned by resource-poor farmers in Gauteng Province, South Africa. Journal of the South African Veterinary Association, 82, 213–218Google Scholar
  125. Ogawa, L., Freire, R.L., Vidotto, O., Gondim, L.F.P., and Navarro, I.T., 2005. Occurrence of antibodies to Neospora caninum and Toxoplasma gondii in dairy cattle from the northern region of the Paraná State, Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 57, 312–316Google Scholar
  126. Ooi, H.K., Huang, C.C., Yang, C.H., and Lee, S.H., 2000. Serological survey and first finding of Neospora caninum in Taiwan, and the detection of its antibodies in various body fluids of cattle. Veterinary Parasitology, 90, 47–55Google Scholar
  127. Ortega, Y.R., Torres, M.P., and Mena, K.D., 2007. Presence of Neospora caninum specific antibodies in three dairy farms in Georgia and two in Texas. Veterinary Parasitology, 144, 353–355Google Scholar
  128. Osawa, T., Wastling, J., Acosta, L., Ortellado, C., Ibarra, J., and Innes, E.A., 2002. Seroprevalence of Neospora caninum infection in dairy and beef cattle in Paraguay. Veterinary Parasitology, 110, 17–23Google Scholar
  129. Oshiro, L.M., Matos, M.F., de Oliveira, J.M., Monteiro, L.A., and Andreotti, R., 2007. Prevalence of anti-Neospora caninum antibodies in cattle from the state of Mato Grosso do Sul, Brazil. Revista Brasileria de Parasitologia Veterinária, 16, 133–138Google Scholar
  130. Otranto, D., Llazari, A., Testini, G., Traversa, D., Frangipane di Regalbono, A., Badan, M., and Capelli, G., 2003. Seroprevalence and associated risk factors of neosporosis in beef and dairy cattle in Italy. Veterinary Parasitology, 118, 7–18Google Scholar
  131. Otter, A., Jeffrey, M., Scholes, S.F., Helmick, B., Wilesmith, J.W., and Trees, A.J., 1997. Comparison of histology with maternal and fetal serology for the diagnosis of abortion due to bovine neosporosis. The Veterinary Record, 141, 487–489Google Scholar
  132. Ould-Amrouche, A., Klein, F., Osdoit, C., Mohammed, H.O., Touratier, A., Sanaa, M., and Mialot, J.P., 1999. Estimation of Neospora caninum seroprevalence in dairy cattle from Normandy, France. Veterinary Research, 30, 531–538Google Scholar
  133. Padilha, M.A.C., Wasen, G., Souza, A.P., Milczewski, V., Luz, T.V.B., Sartor, A.A., Farias, J.A., and Moura, A.B., 2017. Neospora caninum: soroprevalência em bovinos de corte na região serrana de Santa Catarina, Brasil. Semina: Ciências Agrárias, 38, 273–282Google Scholar
  134. Panadero, R., Painceira, A., López, C., Vázquez, L., Paz, A., Díaz, P., Dacal, V., Cienfuegos, S., Fernández, G., Lago, N., Díez-Baños, P., and Morrondo, P., 2010. Seroprevalence of Toxoplasma gondii and Neospora caninum in wild and domestic ruminants sharing pastures in Galicia (Northwest Spain). Research in Veterinary Science, 88, 111–115Google Scholar
  135. Paré, J., Fecteau, G., Fortin, M., and Marsolais, G., 1998. Seroepidemiologic study of Neospora caninum in dairy herds. Journal of the American Veterinary Medical Association, 213, 1595–1598Google Scholar
  136. Patitucci, A.N., Perez, M.J., Israel, K.F., and Rozas, M.A., 2000. Prevalencia de anticuerpos séricos contra Neospora caninum en dos rebaños lecheros de la IX Región de Chile. Archivos de Medicina Veterinaria, 32, 209–214Google Scholar
  137. Paz, G.F., Leite, R.C., and Rocha, M.A., 2007. Associação entre sorologia para Neospora caninum e taxa de prenhez em vacas receptoras de embriões. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 59, 1323–1325Google Scholar
  138. Peregrine, A.S., Martin, S.W., Hopwood, D.A., Duffield, T.F., McEwen, B., Hobson, J.C., and Hietala, S.K., 2006. Neospora caninum and Leptospira serovar serostatus in dairy cattle in Ontario. Canadian Veterinary Journal, 47, 467–470Google Scholar
  139. Pessoa, G.A., Martini, A.P., Trentin, J.M., Dalcin, V.C., Leonardi, C.E., Vogel, F.S., de Sá Filho, M.F., Rubin, M.I., and Silva, C.A., 2016. Impact of spontaneous Neospora caninum infection on pregnancy loss and subsequent pregnancy in grazing lactating dairy cows. Theriogenology, 85, 519–527Google Scholar
  140. Pitel, P.H., Pronost, S., Chatagnon, G., Tainturier, D., Fortier, G., and Ballet, J.J., 2001. Neosporosis in bovine dairy herds from the west of France: detection of Neospora caninum DNA in aborted fetuses, seroepidemiology of N. caninum in cattle and dogs. Veterinary Parasitology, 102, 269–277Google Scholar
  141. Pruvot, M., Kutz, S., Barkema, H.W., De Buck, J., Orsel, K., 2014. Occurrence of Mycobacterium avium subspecies paratuberculosis and Neospora caninum in Alberta cow-calf operations. Preventive Veterinary Medicine, 117, 95–102Google Scholar
  142. Quevedo, V.J., Chávez, V.A., Rivera, G.H., Casas, A.E., and Serrano, M.E., 2003. Neosporosis en bovinos lecheros en dos distritos de la provincia de Chachapoyas. Revista de Pesquisas Veterinárias do Peru, 14, 33–37Google Scholar
  143. Qian, W., Wang, T., Yan, W., Zhang, M., Han, L., Xue, R., Song, S., and Lv, C., 2017. Seroprevalence and first multilocus microsatellite genotyping of Neospora caninum in dairy cattle in Henan, central China. Veterinary Parasitology, 244, 81–84Google Scholar
  144. Quintanilla-Gozalo, A., Pereira-Bueno, J., Tabarés, E., Innes, E.A., González-Paniello, R., and Ortega-Moram L.M., 1999. Seroprevalence of Neospora caninum infection in dairy and beef cattle in Spain. International Journal for Parasitology, 29, 1201–1208Google Scholar
  145. Rábago-Castro, J.L., Jasso-Obregón, J.O., Zertuche-Rodríguez, J.L., Sánchez-Martínez, J.G., Loredo-Osti, J., and Domínguez-Muñoz, M.A., 2017. Detection of Neospora caninum antibodies in beef cattle in Tamaulipas, Mexico. Case report. Austral Journal of Veterinary Sciences, 49, 205–207Google Scholar
  146. Ragozo, A.M.A., Paula, V.S.O., Souza, S.L.P., Bergsmasch, D.P., and Gennari, S.M., 2003. Ocorrência de anticorpos anti-Neospora caninum em soros bovinos procedentes de seis estados brasileiros. Revista Brasileira de Parasitologia Veterinária, 12, 33–37Google Scholar
  147. Razmi, G.R., Mohammadi, G.R., Garrosi, T., Farzaneh, N., Fallah, A.H., and Maleki, M., 2006. Seroepidemiology of Neospora caninum infection in dairy cattle herds in Mashhad area, Iranian Journal of Parasitology, 135, 187–189Google Scholar
  148. Reichel, M.P., Alejandra Ayanegui-Alcérreca, M., Gondim, L.F., and Ellis, J.T., 2013. What is the global economic impact of Neospora caninum in cattle—the billion dollar question. International Journal for Parasitology, 43, 133–142Google Scholar
  149. Reiterová, K., Spilovská, S., Antolová, D., and Dubinský, P., 2009. Neospora caninum, potential cause of abortions in dairy cows: the current serological follow-up in Slovakia. Veterinary Parasitology, 159, 1–6Google Scholar
  150. Rinaldi, L., Fusco, G., Musella, V., Veneziano, V., Guarino, A., Taddei, R., and Cringoli, G., 2005. Neospora caninum in pastured cattle: determination of climatic, environmental, farm management and individual animal risk factors using remote sensing and geographical information systems. Veterinary Parasitology, 128, 219–230Google Scholar
  151. Rinaldi, L., Pacelli, F., Iovane, G., Pagnini, U., Veneziano, V., Fusco, G., and Cringoli, G., 2007. Survey of Neospora caninum and bovine herpes virus 1 coinfection in cattle. Parasitology Research, 100, 359–364Google Scholar
  152. Rivera, H.G., Benito, A.Z., Ramos, O.C., and Manchego, A.S., 2004. Prevalencia de enfermedades de impacto reproductivo en bovinos de la Estación Experimental de Trópico del Centro de Investigaciones IVITA. Revista de Pesquisas Veterinárias do Peru, 15, 120–126Google Scholar
  153. Rodrigues, R.S., Igarashi, M., Muraro, L.S., Gomes, A.H.B., Aguiar, D.M., Pacheco, T.A., Okano, W., Barro, M.P., and Santos, M.D., 2016. Ocorrência de anticorpos anti-Neospora caninum em fêmeas e fetos da espécie bovina do município de Nossa Senhora do Livramento, Mato Grosso. Semina: Ciências Agrárias, 37, 4161–4166Google Scholar
  154. Rodriguez, I., Choromanski, L., Rodgers, S.J., and Weinstock, D., 2002. Survey of Neospora caninum antibodies in dairy and beef cattle from five regions of the United States. Veterinary Therapeutics: Research in Applied Veterinary Medicine, 3, 396–401Google Scholar
  155. Romero, J.J., Perez, E., Dolz, G., and Frankena, K., 2002. Factors associated with Neospora caninum serostatus in cattle of 20 specialised Costa Rican dairy herds. Preventive Veterinary Medicine, 53, 263–273Google Scholar
  156. Romero, J.J., Breda, S.V., Vargas, B., Dolz, G., and Frankena, K., 2005. Effect of neosporosis on productive and reproductive performance of dairy cattle in Costa Rica. Theriogenology, 64, 1928–1939Google Scholar
  157. Romero-Salas, D., García-Vázquez, Z., Montiel-Palacios, F., Montiel-Peña, T., Aguilar-Domínguez, M., Medina-Esparza, L., and Cruz-Vázquez, C., 2010. Seroprevalence of Neospora caninum antibodies in cattle in Veracruz, Mexico. Journal of Animal and Veterinary Advances, 9, 1445–1451Google Scholar
  158. Sadrebazzaz, A., Haddadzadeh, H., Esmailnia, K., Habibi, G., Vojgani, M., and Hashemifesharaki, R., 2004. Serological prevalence of Neospora caninum in healthy and aborted dairy cattle in Mashhad, Iran. Veterinary Parasitology, 124, 201–204Google Scholar
  159. Salehi, N., Haddadzadeh, H.R., Shayan, P., Vodjgani, M., and Bolourchi, M., 2010. Serological study of Neospora caninum in pregnant dairy cattle in Tehran, Iran. International Journal of Veterinary Science, 2, 113–116Google Scholar
  160. Salinas-Melendez, J.A., Zarate-Ramos, J.J., Avalos-Ramirez, R., Hernandez-Escareno, J.J., Hernandez-Vidal, G., Gonzalez-Hernandez, C.S., and Riojas-Valdes, V.M., 2011. Prevalence of antibodies against of Neospora caninum in dairy cattle in Nuevo Leon, Mexico. Journal of Animal and Veterinary Advances, 10, 1389–1393Google Scholar
  161. Sanderson, M.W., Gay, J.M., and Baszler, T.V., 2000. Neospora caninum seroprevalence and associated risk factors in beef cattle in the northwestern United States. Veterinary Parasitology, 90, 15–24Google Scholar
  162. Santin, A.P.I., Juliano, R.S., Silva, A.C., Oliveira, V.S.F., Junqueira-Kipnis, A.P., Brito, W.M.E.D., and Fioravanti, M.C.S., 2017. Soroepidemiologia de Neospora caninum e Toxoplasma gondii em bovinos da raça curraleiro. Ciência Animal Brasileira, 18, e-44649Google Scholar
  163. Santos, S.L., de Souza Costa, K., Gondim, L.Q., da Silva, M.S., Uzêda, R.S., Abe-Sandes, K., and Gondim, L.F., 2010. Investigation of Neospora caninum, Hammondia sp., and Toxoplasma gondii in tissues from slaughtered beef cattle in Bahia, Brazil. Parasitology Research, 106, 457–461Google Scholar
  164. Santos, R.R., da Rocha, C.M., Gonçalves, T.M., and Guimarães, A.M., 2012. Quantification of vertical transmission of Neospora caninum in dairy cows in Minas Gerais, Brazil. Revista Brasileira de Parasitologia Veterinária, 21, 294–297Google Scholar
  165. Sengupta, P.P., Balumahendiran, M., Raghavendra, A.G., Honnappa, T.G., Gajendragad, M.R., and Prabhudas, K., 2013. Prevalence of Neospora caninum antibodies in dairy cattle and water buffaloes and associated abortions in the plateau of Southern Peninsular India. Tropical Animal Health and Production, 45, 205–210Google Scholar
  166. Shabbir, M.Z., Nazir, M.M., Maqbool, A., Lateef, M., Shabbir, M.A., Ahmad, A., Rabbani, M., Yaqub, T., Sohail, M.U., and Ijaz, M., 2011. Seroprevalence of Neospora caninum and Brucella abortus in dairy cattle herds with high abortion rates. The Journal of Parasitology, 97, 740–742Google Scholar
  167. Silva, C.L., Freitas, J.A., Garcia, J.L., Araújo, C.V., Zulpo, D.L., and Cunha, I.A.L., 2015. Inquérito soroepidemiológico sobre Neospora caninum em rebanhos leiteiros de Parauapebas, Estado do Pará. Semina: Ciência Agrárias, 36, 231–238Google Scholar
  168. Snak, A., Garcia, F.G., Lara, A.A., Pena, H.F.J., and Osaki, S.C., 2018. Neospora caninum in properties in the west region of Paraná, Brazil: prevalence and risk factors. Revista Brasileira de Parasitologia Veterinária, 27, 52–60Google Scholar
  169. Sousa, M.E., Wagnner, J.N.P., Albuquerque, P.P.F., Souza Neto, O.L., Faria, E.B., Pinheiro Júnior, J.W., and Mota, R.A., 2012. Soroprevalência e fatores de risco associados à infecção por Neospora caninum em bovinos leiteiros no estado de Alagoas. Pesquisa Veterinária Brasileira, 32, 1009–1013Google Scholar
  170. Špilovská, S., Reiterová, K., and Antolová, D., 2015. Neospora caninum—associated abortions in Slovak dairy farm. Iranian Journal of Parasitology, 10, 96–101Google Scholar
  171. Sun, W.W., Meng, Q.F., Cong, W., Shan, X.F., Wang, C.F., and Qian, A.D., 2015. Herd-level prevalence and associated risk factors for Toxoplasma gondii, Neospora caninum, Chlamydia abortus and bovine viral diarrhoea virus in commercial dairy and beef cattle in eastern, northern and northeastern China. Parasitology Research, 114, 4211–4218Google Scholar
  172. Stoessel, Z., Taylor, L.F., McGowan, M.R., Coleman, G.T., and Landmann, J.K., 2003. Prevalence of antibodies to Neospora caninum within central Queensland beef cattle. Australian Veterinary Journal, 81, 165–166Google Scholar
  173. Suteeraparp, P., Pholpark, S., Pholpark, M., Charoenchai, A., Chompoochan, T., Yamane, I., and Kashiwazaki, Y., 1999. Seroprevalence of antibodies to Neospora caninum and associated abortion in dairy cattle from central Thailand. Veterinary Parasitology, 86, 49–57Google Scholar
  174. Talafha, A.Q., and Al-Majali, A.M., 2013. Prevalence and risk factors associated with Neospora caninum infection in dairy herds in Jordan. Tropical Animal Health and Production, 45, 479–485Google Scholar
  175. Teixeira, W.C., Uzêda, R.S., Gondim, L.F.P., Silva, M.I.S., Pereira, H.M., Alves, L.C., and Faustino, M.A.G., 2010. Prevalência de anticorpos anti-Neospora caninum (Apicomplexa: Sarcocystidae) em bovinos leiteiros de propriedades rurais em três microrregiões no estado do Maranhão. Pesquisa Veterinária Brasileira, 30, 729–734Google Scholar
  176. Tennent-Brown, B.S., Pomroy, W.E., Reichel, M.P., Gray, P.L., Marshall, T.S., Moffat, P.A., Rogers, M., Driscoll, V.A., Reeve, O.F., Ridler, A.L., and Ritaven, S., 2000. Prevalence of Neospora antibodies in beef cattle in New Zealand. New Zealand Veterinary Journal, 48, 149–150Google Scholar
  177. Trees, A.J., Guy, F., Low, J.C., Roberts, L., Buxton, D., and Dubey, J.P., 1994. Serological evidence implicating Neospora species as a cause of abortion in British cattle. The Veterinary Record, 134, 405–407Google Scholar
  178. Tuemmers, C., Valenzuela, G., Nuñez, C., De la Cruz, R., Meyer, J., Andaur, M., Leyan, P., and Mora, C., 2017. Seroprevalencia de Neospora caninum en bovinos de una Feria Ganadera de la Región de la Araucanía, Chile. Revista de Pesquisas Veterinárias do Peru, 28, 629–635Google Scholar
  179. Václavek, P., Koudela, B., Modrý, D., and Sedlák, K., 2003. Seroprevalence of Neospora caninum in aborting dairy cattle in the Czech Republic. Veterinary Parasitology, 115, 239–245Google Scholar
  180. Vangeel, I., Méroc, E., Roelandt, S., Welby, S., Riocreux, F., Stede, Y.V., Driessche, E.V., Schoubroeck, L.V., Czaplicki, G., Quinet, C., Hooyberghs, J., Houdart, P., and Stede, Y.V., 2012. Seroprevalence of Neospora caninum, paratuberculosis and Q fever in cattle in Belgium in 2009–2010. The Veterinary Record, 171, 477Google Scholar
  181. VanLeeuwen, J.A., Forsythe, L., Tiwari, A., and Chartier, R., 2005. Seroprevalence of antibodies against bovine leukemia virus, bovine viral diarrhea virus, Mycobacterium avium subspecies paratuberculosis, and Neospora caninum in dairy cattle in Saskatchewan. Canadian Veterinary Journal, 46, 56–58Google Scholar
  182. Vanleeuwen, J.A., Haddad, J.P., Dohoo, I.R., Keefe, G.P., Tiwari, A., and Scott, H.M., 2010. Risk factors associated with Neospora caninum seropositivity in randomly sampled Canadian dairy cows and herds. Preventive Vetrinary Medicine, 93, 129–138Google Scholar
  183. Venturini, M.C., Venturini, L., Bacigalupe, D., Machuca, M., Echaide, I., Basso, W., Unzaga, J.M., Di Lorenzo, C., Guglielmone, A., Jenkins, M.C., and Dubey, J.P., 1999. Neospora caninum infections in bovine foetuses and dairy cows with abortions in Argentina. International Journal for Parasitology, 29, 1705–1708Google Scholar
  184. Vianna, L.C., Sartor, I.F., Pituco, E.M., Okuda, L.H., Camargo, C.N., and Kronka, S.N., 2008. Incidência e transmissão transplacentária de Neospora caninum em fêmeas primíparas da raça Bos indicus abatidos em Presidente Prudente, São Paulo, Brasil. Semina: Ciências Agrárias, 29, 387–392Google Scholar
  185. Vogel, F.S.F., Arenhart, S., and Bauermann, F., 2006. Anticorpos anti-Neospora caninum em bovinos, ovinos e bubalinos no Estado do Rio Grande do Sul. Ciência Rural, 36, 1948–1951Google Scholar
  186. Vural, G., Aksoy, E., Bozkir, M., Kuçukayan, U., and Erturk, A., 2006. Seroprevalence of Neospora caninum in dairy cattle herds in Central Anatolia, Turkey. Veterinarski Arhiv, 76, 343–349Google Scholar
  187. Waldner, C.L., Janzen, E.D., Henderson, J., and Haines, D.M., 1999. Outbreak of abortion associated with Neospora caninum infection in a beef herd. Journal of the American Veterinary Medical Association, 215, 1485–1490Google Scholar
  188. Waldner, C.L., Henderson, J., Wu, J.T., Coupland, R., and Chow, E.Y., 2001. Seroprevalence of Neospora caninum in beef cattle in northern Alberta. Canadian Veterinary Journal, 42, 130–132Google Scholar
  189. Waldner, C., Wildman, B.K., Hill, B.W., Fenton, R.K., Pittman, T.J., Schunicht, O.C., Jim, G.K,, Guichon, P.T., and Booker, C.W., 2004. Determination of the seroprevalence of Neospora caninum in feedlot steers in Alberta. Canadian Veterinary Journal, 45, 218–224Google Scholar
  190. Walsh, R.B., Kelton, D.F., Hietala, S.K., and Duffield, T.F., 2013. Evaluation of enzyme-linked immunosorbent assays performed on milk and serum samples for detection of neosporosis and leukosis in lactating dairy cows. Canadian Veterinary Journal, 54, 347–352Google Scholar
  191. Wang, C., Wang, Y., Zou, X., Zhai, Y., Gao, J., Hou, M., and Zhu, X.Q., 2010. Seroprevalence of Neospora caninum infection in dairy cattle in northeastern China. The Journal of Parasitology, 96, 451–452Google Scholar
  192. Weston, J.F., Heuer, C., Parkinson, T.J., and Williamson, N.B., 2012. Causes of abortion on New Zealand dairy farms with a history of abortion associated with Neospora caninum. New Zealand Veterinary Journal, 60, 27–34Google Scholar
  193. Wiengcharoen, J., Nakthong, C., Mitchaothai, J., Udonsom, R., and Sukthana, Y., 2012. Toxoplasmosis and neosporosis among beef cattle slaughtered for food in Western Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health, 43, 1087–1093Google Scholar
  194. Xia, H.Y., Zhou, D.H., Jia, K., Zeng, X.B., Zhang, D.W., She, L.X., Lin, R.Q., Yuan, Z.G., Li, S.J., and Zhu, X.Q., 2011. Seroprevalence of Neospora caninum infection in dairy cattle of Southern China. The Journal of Parasitology, 97, 172–173Google Scholar
  195. Xu, M.J., Liu, Q.Y., Fu, J.H., Nisbet, A.J., Shi, D.S., He, X.H., Pan, Y., Zhou, D.H., Song, H.Q., and Zhu, X.Q., 2012. Seroprevalence of Toxoplasma gondii and Neospora caninum infection in dairy cows in subtropical southern China. Parasitology, 139, 1425–1428Google Scholar
  196. Yao, L., Yang, N., Liu, Q., Wang, M., Zhang, W., Qian, W.F., Hu, Y.F., and Ding, J., 2009. Detection of Neospora caninum in aborted bovine fetuses and dam blood samples by nested PCR and ELISA and seroprevalence in Beijing and Tianjin, China. Parasitology, 2136, 1251–1256Google Scholar
  197. Yildiz, K., Kul, O., Babur, C., Kilic, S., Gazyagci, A.N., Celebi, B., and Gurcan, I.S., 2009. Seroprevalence of Neospora caninum in dairy cattle ranches with high abortion rate: special emphasis to serologic co-existence with Toxoplasma gondii, Brucella abortus and Listeria monocytogenes. Veterinary Parasitology, 164, 306–310Google Scholar
  198. Yıldız, K., Gökpınar, S., Sürsal, N., and Değirmenci, R., 2017. Seroprevalence of Neospora caninum in dairy cattle raised in Çiçekdaği District of Kırşehir Province. Türkiye Parazitoloji Dergisi, 41, 135–138Google Scholar
  199. Yu, J., Xia, Z., Liu, Q., Liu, J., Ding, J., and Zhang, W., 2007. Seroepidemiology of Neospora caninum and Toxoplasma gondii in cattle and water buffaloes (Bubalus bubalis) in the People’s Republic of China. Veterinary Parasitology, 143, 79–85Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Claudia Mello Ribeiro
    • 1
    Email author
  • Isabela Ribeiro Soares
    • 2
  • Rodrigo Guerrero Mendes
    • 1
  • Paula Andrea de Santis Bastos
    • 3
    • 4
  • Satie Katagiri
    • 5
  • Renato Bacarin Zavilenski
    • 2
  • Hudson Felipe Porto de Abreu
    • 2
  • Vera Afreixo
    • 6
  1. 1.Universidade Nove de JulhoSão PauloBrazil
  2. 2.Faculdade de Ciências Sociais e Agrárias de ItapevaItapevaBrazil
  3. 3.Centro Universitário das Faculdades Metropolitanas UnidasSão PauloBrazil
  4. 4.Universidade Metropolitana de SantosSantosBrazil
  5. 5.Universidade Federal de Mato GrossoBarra do GarçasBrazil
  6. 6.Department of MathematicsUniversidade de AveiroDistrict of AveiroPortugal

Personalised recommendations