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Tropical Animal Health and Production

, Volume 50, Issue 1, pp 75–84 | Cite as

An Ibero-American inter-laboratory trial to evaluate serological tests for the detection of anti-Neospora caninum antibodies in cattle

  • Lucía M. Campero
  • Javier Moreno-Gonzalo
  • María C. Venturini
  • Gastón Moré
  • Andrea Dellarupe
  • Magdalena Rambeaud
  • Ignacio E. Echaide
  • Beatriz Valentini
  • Carlos M. Campero
  • Dadín P. Moore
  • Dora B. Cano
  • Marcelo Fort
  • Rinaldo A. Mota
  • Marcos E. Serrano-Martínez
  • Carlos Cruz-Vázquez
  • Luis M. Ortega-Mora
  • Gema Álvarez-GarcíaEmail author
Regular Articles
  • 276 Downloads

Abstract

We carried out an inter-laboratory trial to compare the serological tests commonly used for the detection of specific Neospora caninum antibodies in cattle in Ibero-American countries. A total of eight laboratories participated from the following countries: Argentina (n = 4), Brazil (n = 1), Peru (n = 1), Mexico (n = 1), and Spain (n = 1). A blind panel of well-characterized cattle sera (n = 143) and sera representative of the target population (n = 351) was tested by seven in-house indirect fluorescent antibody tests (IFATs 1–7) and three enzyme-linked immunosorbent assays (ELISAs 1–3; two in-house and one commercial). Diagnostic performance of the serological tests was calculated and compared according to the following criteria: (1) the “Pre-test information,” which uses previous epidemiological and serological data; (2) the “Majority of tests,” which classifies a serum as positive or negative according to the results obtained by most tests evaluated. Unexpectedly, six tests showed either sensitivity (Se) or specificity (Sp) values lower than 90%. In contrast, the best tests in terms of Se, Sp, and area under the ROC curve (AUC) values were IFAT 1 and optimized ELISA 1 and ELISA 2. We evaluated a high number of IFATs, which are the most widely used tests in Ibero-America. The significant discordances observed among the tests regardless of the criteria employed hinder control programs and urge the use of a common test or with similar performances to either the optimized IFAT 1 and ELISAs 1 and 2.

Keywords

Bovine neosporosis Serological assay trial Ibero-America 

Notes

Acknowledgements

We wish to acknowledge Isidoro Ercoli and Marco Quispe Huacho for their excellent technical assistance. This work was supported by several research projects (Programa Iberoamericano de Ciencia y Tecnología Thematic Network 113RT0469 Protozoovac, PLATESA S20137ABI-2906, and Proyectos de Investigación Científica y Tecnológica 2011-1179 Préstamo Banco Interamericano de Desarrollo). Lucía M. Campero has been financially supported by Proyectos de Investigación Científica y Tecnológica-2012-0355 and resources from Immunoparasitology Laboratory. Javier Moreno-Gonzalo has been financially supported by Saluvet-Innova S.L.

Author contributions

G. Álvarez-García and M.C. Venturini contributed to conception and design of the study. L.M. Campero, G. Moré, A. Dellarupe, and M. Rambeaud prepared the blind-coded panel of sera. L.M. Campero and J. Moreno-Gonzalo drafted the manuscript. All authors contributed to serological analysis, analysis and interpretation of data, and critical revision of the manuscript.

Compliance with ethical standards

Conflict of interests

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

11250_2017_1401_MOESM1_ESM.doc (624 kb)
Supplementary Figure 1 Receiver operating characteristic (ROC) PLOT of tests relative to Pre-test information criteria of reference sera (Group 2) for all tests. (DOC 624 kb)
11250_2017_1401_MOESM2_ESM.docx (28 kb)
ESM 1 (DOCX 28 kb)

References

  1. Aguado-Martínez, A., Álvarez-García, G., Fernández-García, A., Risco-Castillo, V., Arnaiz-Seco, I., Rebordosa-Trigueros, X., Navarro-Lozano, V., Ortega-Mora, L.M., 2008. Usefulness of rNcGRA7- and rNcSAG4-based ELISA tests for distinguishing primo-infection, recrudescence, and chronic bovine neosporosis. Veterinary Parasitology, 57, 182–195.CrossRefGoogle Scholar
  2. Almería, S., 2013. Neospora caninum and wildlife. ISRN Parasitology, 13, 947347.Google Scholar
  3. Álvarez-García, G., 2016. From the mainland to Ireland - bovine besnoitiosis and its spread in Europe. Veterinary Record, 2016, 178, 605–607.CrossRefGoogle Scholar
  4. Álvarez-García, G., Collantes-Fernández, E., Costas, E., Rebordosa, X., Ortega-Mora, L.M., 2003. Influence of age and purpose for testing on the cut-off selection of serological methods in bovine neosporosis. Veterinary Research, 34, 341–352.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Álvarez-García, G., García-Culebras, A., Gutiérrez-Expósito, D., Navarro-Lozano, V., Pastor-Fernández, I., Ortega-Mora, L.M., 2013. Serological diagnosis of bovine neosporosis: a comparative study of commercially available ELISA tests. Veterinary Parasitology, 198, 85–95.CrossRefGoogle Scholar
  6. Bañales, P., Fernandez, L., Repiso, M.V., Gil, A., Dargatz, D.A., Osawa, T., 2006. A nationwide survey on seroprevalence of Neospora caninum infection in beef cattle in Uruguay. Veterinary Parasitology, 2006, 139, 15–20.CrossRefGoogle Scholar
  7. Barr, B.C., Anderson, M.L., Sverlow, K.W., Conrad, P.A., 1995. Diagnosis of bovine fetal Neospora infection with an indirect fluorescent antibody test. Veterinary Record, 137, 611–613.PubMedGoogle Scholar
  8. Bartels, C.J., Arnaiz-Seco, J.I., Ruiz-Santa-Quitera, A., Björkman, C., Frössling, J., von Blumröder, D., Conraths, F.J., Schares, G., van Maanen, C., Wouda, W., Ortega-Mora, L.M., 2006. Supranational comparison of Neospora caninum seroprevalences in cattle in Germany, The Netherlands, Spain and Sweeden. Veterinary Parasitology, 137, 17–27.CrossRefGoogle Scholar
  9. Baszler, T.V., Knowles, D.P., Dubey, J.P., Gay, J.M., Mathison, B.A., McElwain, T.F., 1996. Serological diagnosis of bovine neosporosis by Neospora caninum monoclonal antibody-based competitive inhibition enzyme-linked immunosorbent assay. Journal of Clinical Microbiology, 34, 1423–1428.PubMedPubMedCentralGoogle Scholar
  10. Björkman, C., Alvarez-Garcia, G., Conraths, F.J., Mattsson, J.G., Ortega-Mora, L.M., Sager, H., Schares, G., 2006. Neospora caninum IgG avidity tests: an interlaboratory comparison. Veterinary Parasitology, 140, 273–280.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Boas, R.V., Pacheco Tdos, A., Melo, A.L., de Oliveira, A.C., de Aguiar, D.M., Pacheco Rde, C., 2015. Infection by Neospora caninum in dairy cattle belonging to family farmers in the northern region of Brazil. Revista Brasileira de Parasitologia Veterinaria, 24, 204–208.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Campero, L.M., Minke, L., Moré, G., Rambeaud, M., Bacigalupe, D., Moore, D.P., Hecker, Y., Campero, C.M., ,Schares, G., Venturin M.C., 2015. Evaluation and comparison of serological methods for the detection of bovine neosporosis in Argentina. Revista Argentina de Microbiología, 47, 295–301.CrossRefPubMedPubMedCentralGoogle Scholar
  13. de Yaniz, M.G., Moore, D.P., Odeón, A.C., Cano, A., Cano, D.B., Leunda, M.R., Campero, C.M., 2007. Humoral immune response in pregnant heifers inoculated with Neospora caninum tachyzoites by conjunctival route. Veterinary Parasitolology, 148, 213–218.CrossRefGoogle Scholar
  14. Donahoe, S.L., Lindsay, S.A., Krockenberger, M., Phalen, D., Šlapeta, J., 2015. A review of neosporosis and pathologic findings of Neospora caninum infection in wildlife. International Journal of Parasitology: Parasites and Wildlife, 4, 216–238.Google Scholar
  15. Dubey, J.P., Hattel, A.L., Lindsay, D.S., Topper, M.J., 1988. Neonatal Neospora caninum infection in dogs: isolation of the causative agent and experimental transmission. Journal of the American Veterinary Medical Association, 193, 1259–1263.PubMedPubMedCentralGoogle Scholar
  16. Dubey, J.P., Schares, G., Ortega-Mora, L.M., 2007. Epidemiology and control of neosporosis and Neospora caninum. Clinical Microbiology Reviews, 20, 323–367.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Fort, M., Edelsten, M., Maley, S., Innes, E., 2015. Seroepidemiological study of Neospora caninum in beef and dairy cattle in La Pampa, Argentina. Acta Parasitologica, 60, 275–282.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Frössling, J., Bonnett, B., Lindberg, A., Björkman, C., 2003. Validation of a Neospora caninum iscom ELISA without a gold standard. Preventive Veterinary Medicine, 57, 141–153.CrossRefPubMedPubMedCentralGoogle Scholar
  19. García-Lunar, P., Moré, G., Campero, L., Ortega-Mora, L.M., Álvarez-García, G., 2015. Anti-Neospora caninum and anti-Sarcocystis spp. specific antibodies cross-react with Besnoitia besnoiti and influence the serological diagnosis of bovine besnoitiosis. Veterinary Parasitology, 214, 49–54.CrossRefPubMedPubMedCentralGoogle Scholar
  20. García-Lunar, P., Ortega-Mora, L.M., Schares, G., Gollnick, N.S., Jacquiet, P., Grisez, C., Prevot, F., Frey, C.F., Gottstein, B., Alvarez-García, G.., 2013 An inter-laboratory comparative study of serological tools employed in the diagnosis of Besnoitia besnoiti infection in bovines. Transboundary and Emerging Diseases, 60, 59–68.CrossRefPubMedPubMedCentralGoogle Scholar
  21. García-Vázquez, Z., Rosario-Cruz, R., Mejia-Estrada, F., Rodriguez-Vivas, I., Romero-Salas, D., Fernandez-Ruvalcaba, M., Cruz-Vazquez, C., 2009. Seroprevalence of Neospora caninum antibodies in beef cattle in three southern states of Mexico. Tropical Animal Health and Production, 41, 749–753.CrossRefPubMedPubMedCentralGoogle Scholar
  22. García-Vázquez, Z., Rosario-Cruz, R., Ramos-Aragon, A., Cruz-Vazquez, C., Mapes-Sanchez, G., 2005. Neospora caninum seropositivity and association with abortions in dairy cows in Mexico. Veterinary Parasitology, 134, 61–65.CrossRefGoogle Scholar
  23. Granados, Z., Rivera, G.H., Casas, A.E., Suárez, F.A., Arana D.C., Chávez V.A., 2014. Seroprevalencia de Neospora caninum en bovinos lecheros de cuatro distritos del Valle del Mantaro, Junín. Revistas de Investigaciones Veterinarias del Perú, 25, 58–64.Google Scholar
  24. Guido, S., Katzer, F., Nanjiani, I., Milne, E., Innes, E.A., 2016. Serology-based diagnostics for the control of bovine neosporosis. Trends in Parasitology, 32, 131–143.CrossRefGoogle Scholar
  25. Hall, C.A., Reichel, M.P., Ellis, J.T., 2006. Prevalence of Neospora caninum infection in Australian (NSW) dairy cattle estimated by a newly validated ELISA for milk. Veterinary Parasitology, 142, 173–178.CrossRefGoogle Scholar
  26. Hecker, Y.P., Moore, D.P., Quattrocchi, V., Regidor-Cerrillo, J., Verna, A., Leunda, M.R., Morrell, E., Ortega-Mora, L.M., Zamorano, P., Venturini, M.C., Campero, C.M., 2013. Immune response and protection provided by live tachyzoites and native antigens from the NC-6 Argentina strain of Neospora caninum in pregnant heifers. Veterinary Parasitology, 197, 436–446.CrossRefGoogle Scholar
  27. Jacobson, R.H., 1998. Validation of serological assays for diagnosis of infectious diseases. Revue Scientifique Technique, 17, 469–526.CrossRefGoogle Scholar
  28. McAllister, M.M., 2016. Diagnosis and control of bovine neosporosis. Veterinary Clinics of North America: Food Animal Practice, 32, 443–463.PubMedGoogle Scholar
  29. Moore, D.P., 2005. Neosporosis in South America. Veterinary Parasitology, 127, 87–97.CrossRefGoogle Scholar
  30. Moore, D.P., Echaide, I., Verna, A.E., Leunda, M.R., Cano, A., Pereyra, S., Zamorano, P.I., Odeón, A.C., Campero, C.M., 2011. Immune response to Neospora caninum native antigens formulated with immune stimulating complexes in calves. Veterinary Parasitology, 175, 245–251.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Moraveji, M., Hosseini, A., Moghaddar, N., Namavari, M.M., Eskandari, M.H., 2012. Development of latex agglutination test with recombinant NcSAG1 for the rapid detection of antibodies to Neospora caninum in cattle. Veterinary Parasitology, 189, 211–217.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Moré, G., Bacigalupe, D., Basso, W., Rambeaud, M., Beltrame, F., Ramirez, B., Venturini, M.C., Venturini, L., 2009. Frequency of horizontal and vertical transmission for Sarcocystis cruzi and Neospora caninum in dairy cattle. Veterinary Parasitology, 160, 51–54.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Nielsen, S.S., Toft, N., Gardner, I.A., 2011. Structured approach to design of diagnostic test evaluation studies for chronic progressive infections in animals. Veterinary Microbiology, 150115–125.Google Scholar
  34. Ortega-Mora, L.M., Fernández-García, A., Gómez-Bautista, M., 2006. Diagnosis of bovine neosporosis: recent advances and perspectives. Acta Parasitologica, 51, 1–14.CrossRefGoogle Scholar
  35. Paré, J., Hietala, S.K., Thurmond, M.C., 1995. Interpretation of an indirect fluorescent antibody test for diagnosis of Neospora sp. infection in cattle. Journal of Veterinary Diagnostic Investigation, 7, 273–275.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Regidor-Cerrillo, J., Arranz-Solís, D., Benavides, J., Gómez-Bautista, M., Castro-Hermida, J.A., Mezo, M., Pérez, V., Ortega-Mora, L.M., González-Warleta, M., 2014. Neospora caninum infection during early pregnancy in cattle: how the isolate influences infection dynamics, clinical outcome and peripheral and local immune responses. Veterinary Research, 45:10.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Reichel, M.P, Alejandra Ayanegui-Alcérreca, M., Gondim, L.F., Ellis, J.T., 2013.What is the global economic impact of Neospora caninum in cattle - the billion dollar question. International Journal of Parasitology, 43, 133–142.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Reichel, M.P., Moore, D.P., Hemphill, A., Ortega-Mora, L.M., Dubey, J.P., Ellis, J.T., 2015. A live vaccine against Neospora caninum abortions in cattle. Vaccine, 33, 1299–1301.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Roelandt, S., Van der Stede, Y., Czaplicki, G., Van Loo, H., Van Driessche, E., Dewulf, J., Hooyberghs, J., Faes, C., 2015. Serological diagnosis of bovine neosporosis: a Bayesian evaluation of two antibody ELISA tests for in vivo diagnosis in purchased and abortion cattle. Veterinary Record, 176, 598.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Shkap, V., Reske, A., Pipano, E., Fish, L., Baszler, T., 2002. Immunological relationship between Neospora caninum and Besnoitia besnoiti. Veterinary Parasitology, 106, 35–43.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Swets, J.A., 1988. Measuring the accuracy of diagnostic systems. Science, 240, 1285–1293.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Thrusfield, M.V., 2007. Diagnositic testing in veterinary epidemiology, 3rd ed. (Oxford, UK Blackwell, 624).Google Scholar
  43. von Blumröder, D., Schares, G., Norton, R., Williams, D.J., Esteban-Redondo, I., Wright, S., Björkman, C., Frössling, J., Risco-Castillo, V., Fernández-García, A., Ortega-Mora, L.M., Sager, H, Hemphill, A., van Maanen, C., Wouda, W., Conraths, F.J., 2004. Comparison and standardisation of serological methods for the diagnosis of Neospora caninum infection in bovines. Veterinary Parasitology, 120, 11–22.CrossRefGoogle Scholar
  44. Waldner, C.L., Cunningham, G., Campbell, J.R., 2004. Agreement between three serological tests for Neospora caninum in beef cattle. Journal of Veterinary Diagnostic Investigation, 16, 313–315.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Wapenaar, W., Barkema, H.W., Vanleeuwen, J.A., McClure, J.T., O'Handley, R.M., Kwok, O.C., Thulliez, P., Dubey, J.P., Jenkins, M.C., 2007. Comparison of serological methods for the diagnosis of Neospora caninum infection in cattle. Veterinary Parasitology, 143, 166–173.CrossRefGoogle Scholar
  46. World Organization for Animal Health (OIE), 2013. Principles and methods of validation of diagnostic assays for infectious, Chapter 1.1.5 (Office International des Epizooties (OIE), Paris, France).Google Scholar
  47. Wu, J.T., Dreger, S., Chow, E.Y., Bowlby, E.E., 2002. Validation of 2 commercial Neospora caninum antibody enzyme linked immunosorbent assays. Canadian Journal of Veterinary Research, 66, 264–271.PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Lucía M. Campero
    • 1
    • 2
  • Javier Moreno-Gonzalo
    • 3
  • María C. Venturini
    • 1
  • Gastón Moré
    • 1
    • 2
  • Andrea Dellarupe
    • 1
    • 2
  • Magdalena Rambeaud
    • 1
  • Ignacio E. Echaide
    • 4
  • Beatriz Valentini
    • 4
  • Carlos M. Campero
    • 5
  • Dadín P. Moore
    • 2
    • 5
  • Dora B. Cano
    • 5
  • Marcelo Fort
    • 6
  • Rinaldo A. Mota
    • 7
  • Marcos E. Serrano-Martínez
    • 8
  • Carlos Cruz-Vázquez
    • 9
  • Luis M. Ortega-Mora
    • 3
  • Gema Álvarez-García
    • 3
    Email author
  1. 1.Immunoparasitology Laboratory, School of Veterinary SciencesNational University of La PlataLa PlataArgentina
  2. 2.National Scientific and Technical Research CouncilBuenos AiresArgentina
  3. 3.SALUVET, Animal Health Department, Faculty of Veterinary SciencesComplutense University of MadridMadridSpain
  4. 4.Rafaela Agricultural Experimental StationNational Institute of Agricultural TechnologySanta FeArgentina
  5. 5.Balcarce Agricultural Experimental StationNational Institute of Agricultural TechnologyBuenos AiresArgentina
  6. 6.Anguil Agricultural Experimental StationNational Institute of Agricultural TechnologyLa PampaArgentina
  7. 7.Veterinary Medicine DepartmentRural Federal University of PernambucoRecifeBrazil
  8. 8.Veterinary Medicine and Zootechny FacultyCayetano Heredia Peruvian UniversityLimaPeru
  9. 9.El Llano Technical InstituteAguascalientesMexico

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