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Experimental ruminant models for bovine neosporosis: what is known and what is needed

Published online by Cambridge University Press:  13 June 2014

JULIO BENAVIDES ,
ESTHER COLLANTES-FERNÁNDEZ ,
IGNACIO FERRE ,
VALENTÍN PÉREZ ,
CARLOS CAMPERO ,
RINALDO MOTA ,
ELISABETH INNES  and
LUIS M. ORTEGA-MORA
JULIO BENAVIDES
Affiliation:
Departamento de Sanidad Animal, Instituto de Ganadería de Montaña (CSIC-ULE), Facultad de Veterinaria, Universidad de León, Campus de Vegazana s/n, 24071 León, Spain
ESTHER COLLANTES-FERNÁNDEZ
Affiliation:
SALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Ciudad Universitaria s/n, 28040-Madrid, Spain
IGNACIO FERRE
Affiliation:
SALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Ciudad Universitaria s/n, 28040-Madrid, Spain
VALENTÍN PÉREZ
Affiliation:
Departamento de Sanidad Animal, Instituto de Ganadería de Montaña (CSIC-ULE), Facultad de Veterinaria, Universidad de León, Campus de Vegazana s/n, 24071 León, Spain
CARLOS CAMPERO
Affiliation:
Instituto Nacional de Tecnología Agropecuaria (INTA), 7620 Balcarce, Argentina
RINALDO MOTA
Affiliation:
Departamento de Medicina Veterinaria, Universidade Federal Rural de Pernambuco, Brazil
ELISABETH INNES
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Edinburgh, EH26 0PZ, UK
LUIS M. ORTEGA-MORA*
Affiliation:
SALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Ciudad Universitaria s/n, 28040-Madrid, Spain
*
*Corresponding author: SALUVET, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Ciudad Universitaria s/n, 28040-Madrid, Spain. E-mail: luis.ortega@vet.ucm.es
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Summary

At present, bovine neosporosis is an important worldwide concern because of its wide geographic distribution and economic impact. Abortion is the main clinical sign of bovine neosporosis in both dairy and beef cattle. Ruminant challenge models are critical to evaluate potential vaccine candidates to help tackle bovine neosporosis and to study pathogenesis and host responses to infection. Several research groups have developed ruminant models of Neospora caninum infection independently of others, resulting in a high degree of variability due to the use of different species of animals, breeds, strains/isolates of N. caninum, doses, routes and times of inoculation. Standardization is greatly needed to advance research in a more collaborative, timely and efficient manner. In the absence of widely accepted international guidelines, this manuscript serves to summarize and discuss the different models and parameters currently in use. Parameters essential for the development of non-pregnant and pregnant ruminant models are outlined and the main knowledge gaps are identified. This information could act as the basis to develop a consensus for international standard guidelines for ruminant models of neosporosis that would be helpful for researchers in this field worldwide.

Keywords

bovine neosporosisruminant modelsharmonizationknowledge gaps
Type
Special Issue Article
Information
Parasitology , Volume 141 , Special Issue 11: ApiCOWplexa 2013 – 2nd International Meeting on Apicomplexan Parasites in Farm Animals , September 2014 , pp. 1471 - 1488
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Aguado-Martinez, A., Alvarez-Garcia, G., Fernandez-Garcia, A., Risco-Castillo, V., Arnaiz-Seco, I., Rebordosa-Trigueros, X., Navarro-Lozano, V. and Ortega-Mora, L. M. (2008). Usefulness of rNcGRA7- and rNcSAG4-based ELISA tests for distinguishing primo-infection, recrudescence, and chronic bovine neosporosis. Veterinary Parasitology 157, 182–195. doi: 10.1016/j.vetpar.2008.08.002.Google Scholar
Aguado-Martinez, A., Alvarez-Garcia, G., Fernandez-Garcia, A., Risco-Castillo, V., Marugan-Hernandez, V. and Ortega-Mora, L. M. (2009). Failure of a vaccine using immunogenic recombinant proteins rNcSAG4 and rNcGRA7 against neosporosis in mice. Vaccine 27, 7331–7338. doi: 10.1016/j.vaccine.2009.09.050.Google Scholar
Almeria, S. and Lopez-Gatius, F. (2013). Bovine neosporosis: clinical and practical aspects. Research in Veterinary Science 95, 303–309. doi: 10.1016/j.rvsc.2013.04.008.Google Scholar
Almeria, S., De Marez, T., Dawson, H., Araujo, R., Dubey, J. P. and Gasbarre, L. C. (2003). Cytokine gene expression in dams and foetuses after experimental Neospora caninum infection of heifers at 110 days of gestation. Parasite Immunology 25, 383–392.CrossRefGoogle ScholarPubMed
Almeria, S., Araujo, R., Tuo, W., Lopez-Gatius, F., Dubey, J. P. and Gasbarre, L. C. (2010). Fetal death in cows experimentally infected with Neospora caninum at 110 days of gestation. Veterinary Parasitology 169, 304–311. doi: 10.1016/j.vetpar.2009.12.044.Google Scholar
Almeria, S., Araujo, R. N., Darwich, L., Dubey, J. P. and Gasbarre, L. C. (2011). Cytokine gene expression at the materno-foetal interface after experimental Neospora caninum infection of heifers at 110 days of gestation. Parasite Immunology 33, 517–523. doi: 10.1111/j.1365-3024.2011.01307.x.Google Scholar
Andrianarivo, A. G., Choromanski, L., McDonough, S. P., Packham, A. E. and Conrad, P. A. (1999). Immunogenicity of a killed whole Neospora caninum tachyzoite preparation formulated with different adjuvants. International Journal for Parasitology 29, 1613–1625.Google Scholar
Andrianarivo, A. G., Rowe, J. D., Barr, B. C., Anderson, M. L., Packham, A. E., Sverlow, K. W., Choromanski, L., Loui, C., Grace, A. and Conrad, P. A. (2000). A POLYGEN-adjuvanted killed Neospora caninum tachyzoite preparation failed to prevent foetal infection in pregnant cattle following i.v./i.m. experimental tachyzoite challenge. International Journal for Parasitology 30, 985–990.Google Scholar
Andrianarivo, A. G., Barr, B. C., Anderson, M. L., Rowe, J. D., Packham, A. E., Sverlow, K. W. and Conrad, P. A. (2001). Immune responses in pregnant cattle and bovine fetuses following experimental infection with Neospora caninum . Parasitology Research 87, 817–825.Google Scholar
Armengol, R., Pabon, M., Santolaria, P., Cabezon, O., Adelantado, C., Yaniz, J., Lopez-Gatius, F. and Almeria, S. (2007). Low seroprevalence of Neospora caninum infection associated with the limousin breed in cow-calf herds in Andorra, Europe. Journal of Parasitology 93, 1029–1032. doi: 10.1645/GE-1242R.1.CrossRefGoogle ScholarPubMed
Bacigalupe, D., Basso, W., Caspe, S. G., More, G., Lischinsky, L., Gos, M. L., Leunda, M., Campero, L., Moore, D. P., Schares, G., Campero, C. M. and Venturini, M. C. (2013). Neospora caninum NC-6 Argentina induces fetopathy in both serologically positive and negative experimentally inoculated pregnant dams. Parasitology Research 112, 2585–2592. doi: 10.1007/s00436-013-3424-1.Google Scholar
Barber, J. S., Holmdahl, O. J., Owen, M. R., Guy, F., Uggla, A. and Trees, A. J. (1995). Characterization of the first European isolate of Neospora caninum (Dubey, Carpenter, Speer, Topper and Uggla). Parasitology 111, 563–568.Google Scholar
Barr, B. C., Conrad, P. A., Dubey, J. P. and Anderson, M. L. (1991). Neospora-like encephalomyelitis in a calf: pathology, ultrastructure, and immunoreactivity. Journal of Veterinary Diagnostic Investigation 3, 39–46.Google Scholar
Barr, B. C., Rowe, J. D., Sverlow, K. W., BonDurant, R. H., Ardans, A. A., Oliver, M. N. and Conrad, P. A. (1994). Experimental reproduction of bovine fetal Neospora infection and death with a bovine Neospora isolate. Journal of Veterinary Diagnostic Investigation 6, 207–215.Google Scholar
Bartels, C. J., Arnaiz-Seco, J. I., Ruiz-Santa-Quitera, A., Bjorkman, C., Frossling, J., von Blumroder, D., Conraths, F. J., Schares, G., van Maanen, C., Wouda, W. and Ortega-Mora, L. M. (2006). Supranational comparison of Neospora caninum seroprevalences in cattle in Germany, the Netherlands, Spain and Sweden. Veterinary Parasitology 137, 17–27. doi: 10.1016/j.vetpar.2005.12.016.Google Scholar
Bartley, P. M., Kirvar, E., Wright, S., Swales, C., Esteban-Redondo, I., Buxton, D., Maley, S. W., Schock, A., Rae, A. G., Hamilton, C. and Innes, E. A. (2004). Maternal and fetal immune responses of cattle inoculated with Neospora caninum at mid-gestation. Journal of Comparative Pathology 130, 81–91. doi: 10.1016/j.jcpa.2003.08.003.CrossRefGoogle ScholarPubMed
Bartley, P. M., Wright, S., Chianini, F., Buxton, D. and Innes, E. A. (2008). Inoculation of Balb/c mice with live attenuated tachyzoites protects against a lethal challenge of Neospora caninum . Parasitology 135, 13–21. doi: 10.1017/S0031182007003526.Google Scholar
Bartley, P. M., Wright, S. E., Maley, S. W., Macaldowie, C. N., Nath, M., Hamilton, C. M., Katzer, F., Buxton, D. and Innes, E. A. (2012). Maternal and foetal immune responses of cattle following an experimental challenge with Neospora caninum at day 70 of gestation. Veterinary Research 43, 38. doi: 10.1186/1297-9716-43-38.Google Scholar
Bartley, P. M., Katzer, F., Rocchi, M. S., Maley, S. W., Benavides, J., Nath, M., Pang, Y., Canton, G., Thomson, J., Chianini, F. and Innes, E. A. (2013). Development of maternal and foetal immune responses in cattle following experimental challenge with Neospora caninum at day 210 of gestation. Veterinary Research 44, 91. doi: 10.1186/1297-9716-44-91.Google Scholar
Basso, W., Venturini, L., Venturini, M. C., Hill, D. E., Kwok, O. C., Shen, S. K. and Dubey, J. P. (2001). First isolation of Neospora caninum from the feces of a naturally infected dog. Journal of Parasitology 87, 612–618.Google Scholar
Baszler, T. V., Shkap, V., Mwangi, W., Davies, C. J., Mathison, B. A., Mazuz, M., Resnikov, D., Fish, L., Leibovitch, B., Staska, L. M. and Savitsky, I. (2008). Bovine immune response to inoculation with Neospora caninum surface antigen SRS2 lipopeptides mimics immune response to infection with live parasites. Clinical and Vaccine Immunology 15, 659–667. doi: 10.1128/CVI.00436-07.CrossRefGoogle ScholarPubMed
Benavides, J., Katzer, F., Maley, S. W., Bartley, P. M., Canton, G., Palarea-Albaladejo, J., Purslow, C. A., Pang, Y., Rocchi, M. S., Chianini, F., Buxton, D. and Innes, E. A. (2012). High rate of transplacental infection and transmission of Neospora caninum following experimental challenge of cattle at day 210 of gestation. Veterinary Research 43, 83. doi: 10.1186/1297-9716-43-83.CrossRefGoogle ScholarPubMed
Bjorkman, C., Alvarez-Garcia, G., Conraths, F. J., Mattsson, J. G., Ortega-Mora, L. M., Sager, H. and Schares, G. (2006). Neospora caninum IgG avidity tests: an interlaboratory comparison. Veterinary Parasitology 140, 273–280. doi: 10.1016/j.vetpar.2006.04.030.Google Scholar
Boysen, P., Klevar, S., Olsen, I. and Storset, A. K. (2006). The protozoan Neospora caninum directly triggers bovine NK cells to produce gamma interferon and to kill infected fibroblasts. Infection and Immunity 74, 953–960. doi: 10.1128/IAI.74.2.953-960.2006.Google Scholar
Buxton, D., Maley, S. W., Thomson, K. M., Trees, A. J. and Innes, E. A. (1997). Experimental infection of non-pregnant and pregnant sheep with Neospora caninum . Journal of Comparative Pathology 117, 1–16.Google Scholar
Buxton, D., Maley, S. W., Wright, S., Thomson, K. M., Rae, A. G. and Innes, E. A. (1998). The pathogenesis of experimental neosporosis in pregnant sheep. Journal of Comparative Pathology 118, 267–279.CrossRefGoogle ScholarPubMed
Buxton, D., Wright, S., Maley, S. W., Rae, A. G., Lunden, A. and Innes, E. A. (2001). Immunity to experimental neosporosis in pregnant sheep. Parasite Immunology 23, 85–91.Google Scholar
Canada, N., Meireles, C. S., Ferreira, P., Correia da Costa, J. M. and Rocha, A. (2006). Artificial insemination of cows with semen in vitro contaminated with Neospora caninum tachyzoites failed to induce neosporosis. Veterinary Parasitology 139, 109–114. doi: 10.1016/j.vetpar.2006.02.014.CrossRefGoogle ScholarPubMed
Caspe, S. G., Moore, D. P., Leunda, M. R., Cano, D. B., Lischinsky, L., Regidor-Cerrillo, J., Alvarez-Garcia, G., Echaide, I. G., Bacigalupe, D., Ortega Mora, L. M., Odeon, A. C. and Campero, C. M. (2012). The Neospora caninum-Spain 7 isolate induces placental damage, fetal death and abortion in cattle when inoculated in early gestation. Veterinary Parasitology 189, 171–181. doi: 10.1016/j.vetpar.2012.04.034.Google Scholar
Collantes-Fernandez, E., Lopez-Perez, I., Alvarez-Garcia, G. and Ortega-Mora, L. M. (2006). Temporal distribution and parasite load kinetics in blood and tissues during Neospora caninum infection in mice. Infection and Immunity 74, 2491–2494. doi: 10.1128/IAI.74.4.2491-2494.2006.Google Scholar
Conrad, P. A., Sverlow, K., Anderson, M., Rowe, J., BonDurant, R., Tuter, G., Breitmeyer, R., Palmer, C., Thurmond, M. and Ardans, A. (1993). Detection of serum antibody responses in cattle with natural or experimental Neospora infections. Journal of Veterinary Diagnostic Investigation 5, 572–578.Google Scholar
Davison, H. C., Guy, C. S., McGarry, J. W., Guy, F., Williams, D. J., Kelly, D. F. and Trees, A. J. (2001). Experimental studies on the transmission of Neospora caninum between cattle. Research in Veterinary Science 70, 163–168. doi: 10.1053/rvsc.2001.0457.Google Scholar
De Marez, T., Liddell, S., Dubey, J. P., Jenkins, M. C. and Gasbarre, L. (1999). Oral infection of calves with Neospora caninum oocysts from dogs: humoral and cellular immune responses. International Journal for Parasitology 29, 1647–1657.Google Scholar
de Yaniz, M. G., Moore, D. P., Odeon, A. C., Cano, A., Cano, D. B., Leunda, M. R. and Campero, C. M. (2007). Humoral immune response in pregnant heifers inoculated with Neospora caninum tachyzoites by conjunctival route. Veterinary Parasitology 148, 213–218. doi: 10.1016/j.vetpar.2007.06.030.CrossRefGoogle ScholarPubMed
Dijkstra, T., Barkema, H. W., Eysker, M. and Wouda, W. (2001 a). Evidence of post-natal transmission of Neospora caninum in Dutch dairy herds. International Journal for Parasitology 31, 209–215.Google Scholar
Dijkstra, T., Eysker, M., Schares, G., Conraths, F. J., Wouda, W. and Barkema, H. W. (2001 b). Dogs shed Neospora caninum oocysts after ingestion of naturally infected bovine placenta but not after ingestion of colostrum spiked with Neospora caninum tachyzoites. International Journal for Parasitology 31, 747–752.Google Scholar
Dijkstra, T., Lam, T. J., Bartels, C. J., Eysker, M. and Wouda, W. (2008). Natural postnatal Neospora caninum infection in cattle can persist and lead to endogenous transplacental infection. Veterinary Parasitology 152, 220–225. doi: 10.1016/j.vetpar.2007.12.034.Google Scholar
Dubey, J. P. (2009). Toxoplasmosis in sheep – the last 20 years. Veterinary Parasitology 163, 1–14. doi: 10.1016/j.vetpar.2009.02.026.Google Scholar
Dubey, J. P. and Lindsay, D. S. (1990). Neospora caninum induced abortion in sheep. Journal of Veterinary Diagnostic Investigation 2, 230–233.Google Scholar
Dubey, J. P. and Schares, G. (2006). Diagnosis of bovine neosporosis. Veterinary Parasitology 140, 1–34. doi: 10.1016/j.vetpar.2006.03.035.Google Scholar
Dubey, J. P. and Schares, G. (2011). Neosporosis in animals – the last five years. Veterinary Parasitology 180, 90–108. doi: 10.1016/j.vetpar.2011.05.031.Google Scholar
Dubey, J. P., Hattel, A. L., Lindsay, D. S. and 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.Google ScholarPubMed
Dubey, J. P., Lindsay, D. S., Anderson, M. L., Davis, S. W. and Shen, S. K. (1992). Induced transplacental transmission of Neospora caninum in cattle. Journal of the American Veterinary Medical Association 201, 709–713.Google Scholar
Dubey, J. P., Chapman, J. L., Rosenthal, B. M., Mense, M. and Schueler, R. L. (2006). Clinical Sarcocystis neurona, Sarcocystis canis, Toxoplasma gondii, and Neospora caninum infections in dogs. Veterinary Parasitology 137, 36–49. doi: 10.1016/j.vetpar.2005.12.017.Google Scholar
Dubey, J. P., Schares, G. and Ortega-Mora, L. M. (2007). Epidemiology and control of neosporosis and Neospora caninum . Clinical Microbiology Reviews 20, 323–367. doi: 10.1128/CMR.00031-06.Google Scholar
Dubey, J. P., Jenkins, M. C., Rajendran, C., Miska, K., Ferreira, L. R., Martins, J., Kwok, O. C. and Choudhary, S. (2011). Gray wolf (Canis lupus) is a natural definitive host for Neospora caninum . Veterinary Parasitology 181, 382–387. doi: 10.1016/j.vetpar.2011.05.018.Google Scholar
Eiras, C., Arnaiz, I., Alvarez-Garcia, G., Ortega-Mora, L. M., Sanjuanl, M. L., Yus, E. and Dieguez, F. J. (2011). Neospora caninum seroprevalence in dairy and beef cattle from the northwest region of Spain, Galicia. Preventive Veterinary Medicine 98, 128–132. doi: 10.1016/j.prevetmed.2010.10.014.Google Scholar
Ferre, I., Serrano-Martinez, E., Martinez, A., Osoro, K., Mateos-Sanz, A., Del-Pozo, I., Aduriz, G., Tamargo, C., Hidalgo, C. O. and Ortega-Mora, L. M. (2008). Effects of re-infection with Neospora caninum in bulls on parasite detection in semen and blood and immunological responses. Theriogenology 69, 905–911. doi: 10.1016/j.theriogenology.2007.11.006.Google Scholar
Gibney, E. H., Kipar, A., Rosbottom, A., Guy, C. S., Smith, R. F., Hetzel, U., Trees, A. J. and Williams, D. J. (2008). The extent of parasite-associated necrosis in the placenta and foetal tissues of cattle following Neospora caninum infection in early and late gestation correlates with foetal death. International Journal for Parasitology 38, 579–588. doi: 10.1016/j.ijpara.2007.09.015.Google Scholar
Gondim, L. F., Gao, L. and McAllister, M. M. (2002). Improved production of Neospora caninum oocysts, cyclical oral transmission between dogs and cattle, and in vitro isolation from oocysts. Journal of Parasitology 88, 1159–1163. doi: 10.1645/0022-3395(2002)088[1159:IPONCO]2.0.CO;2.Google Scholar
Gondim, L. F., McAllister, M. M., Anderson-Sprecher, R. C., Bjorkman, C., Lock, T. F., Firkins, L. D., Gao, L. and Fischer, W. R. (2004). Transplacental transmission and abortion in cows administered Neospora caninum oocysts. Journal of Parasitology 90, 1394–1400. doi: 10.1645/GE-359R.Google Scholar
Hall, C. A., Reichel, M. P. and Ellis, J. T. (2005). Neospora abortions in dairy cattle: diagnosis, mode of transmission and control. Veterinary Parasitology 128, 231–241. doi: 10.1016/j.vetpar.2004.12.012.Google Scholar
Harkins, D., Clements, D. N., Maley, S., Marks, J., Wright, S., Esteban, I., Innes, E. A. and Buxton, D. (1998). Western blot analysis of the IgG responses of ruminants infected with Neospora caninum and with Toxoplasma gondii . Journal of Comparative Pathology 119, 45–55.Google Scholar
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. and 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. doi: 10.1016/j.vetpar.2013.07.027.Google Scholar
Innes, E. A. and Vermeulen, A. N. (2006). Vaccination as a control strategy against the coccidial parasites Eimeria, Toxoplasma and Neospora . Parasitology 133 (Suppl.), S145–S168. doi: 10.1017/S0031182006001855.Google Scholar
Innes, E. A., Panton, W. R., Marks, J., Trees, A. J., Holmdahl, J. and Buxton, D. (1995). Interferon gamma inhibits the intracellular multiplication of Neospora caninum, as shown by incorporation of 3H uracil. Journal of Comparative Pathology 113, 95–100.Google Scholar
Innes, E. A., Wright, S. E., Maley, S., Rae, A., Schock, A., Kirvar, E., Bartley, P., Hamilton, C., Carey, I. M. and Buxton, D. (2001). Protection against vertical transmission in bovine neosporosis. International Journal for Parasitology 31, 1523–1534.Google Scholar
Innes, E. A., Bartley, P. M., Rocchi, M., Benavidas-Silvan, J., Burrells, A., Hotchkiss, E., Chianini, F., Canton, G. and Katzer, F. (2011). Developing vaccines to control protozoan parasites in ruminants: dead or alive? Veterinary Parasitology 180, 155–163. doi: 10.1016/j.vetpar.2011.05.036.Google Scholar
Jenkins, M. C., Tuo, W. and Dubey, J. P. (2004). Evaluation of vaccination with Neospora caninum protein for prevention of fetal loss associated with experimentally induced neosporosis in sheep. American Journal of Veterinary Research 65, 1404–1408.Google Scholar
Jimenez-Ruiz, E., Alvarez-Garcia, G., Aguado-Martinez, A. and Ortega-Mora, L. M. (2013 a). Low rates of Neospora caninum infection reactivation during gestation are observed in both chronically and congenitally infected mice. Parasitology 140, 220–228. doi: 10.1017/S0031182012001515.Google Scholar
Jimenez-Ruiz, E., Alvarez-Garcia, G., Aguado-Martinez, A. and Ortega-Mora, L. M. (2013 b). Mice congenitally infected with low-to-moderate virulence Neospora caninum isolates exhibited clinical reactivation during the mating period without transmission to the next generation. Experimental Parasitology 134, 244–248. doi: 10.1016/j.exppara.2013.03.002.Google Scholar
Klevar, S., Kulberg, S., Boysen, P., Storset, A. K., Moldal, T., Bjorkman, C. and Olsen, I. (2007). Natural killer cells act as early responders in an experimental infection with Neospora caninum in calves. International Journal for Parasitology 37, 329–339. doi: 10.1016/j.ijpara.2006.11.002.Google Scholar
Konrad, J. L., Moore, D. P., Crudeli, G., Caspe, S. G., Cano, D. B., Leunda, M. R., Lischinsky, L., Regidor-Cerrillo, J., Odeon, A. C., Ortega-Mora, L. M., Echaide, I. and Campero, C. M. (2012). Experimental inoculation of Neospora caninum in pregnant water buffalo. Veterinary Parasitology 187, 72–78. doi: 10.1016/j.vetpar.2011.12.030.Google Scholar
Kritzner, S., Sager, H., Blum, J., Krebber, R., Greif, G. and Gottstein, B. (2002). An explorative study to assess the efficacy of toltrazuril-sulfone (ponazuril) in calves experimentally infected with Neospora caninum . Annals of Clinical Microbiology and Antimicrobials 1, 4.Google Scholar
Lindsay, D. S., Rippey, N. S., Powe, T. A., Sartin, E. A., Dubey, J. P. and Blagburn, B. L. (1995). Abortions, fetal death, and stillbirths in pregnant pygmy goats inoculated with tachyzoites of Neospora caninum . American Journal of Veterinary Research 56, 1176–1180.Google Scholar
Lopez-Gatius, F., Pabon, M. and Almeria, S. (2004). Neospora caninum infection does not affect early pregnancy in dairy cattle. Theriogenology 62, 606–613. doi: 10.1016/j.theriogenology.2003.11.002.Google Scholar
Lopez-Gatius, F., Garcia-Ispierto, I., Santolaria, P., Yaniz, J. L., Lopez-Bejar, M., Nogareda, C. and Almeria, S. (2005 a). Relationship between rainfall and Neospora caninum-associated abortion in two dairy herds in a dry environment. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health 52, 147–152. doi: 10.1111/j.1439-0450.2005.00831.x.Google Scholar
Lopez-Gatius, F., Santolaria, P., Yaniz, J. L., Garbayo, J. M. and Almeria, S. (2005 b). 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, 88–92. doi: 10.1111/j.1439-0450.2004.00818.x.Google Scholar
Lopez-Perez, I. C., Risco-Castillo, V., Collantes-Fernandez, E. and Ortega-Mora, L. M. (2006). Comparative effect of Neospora caninum infection in BALB/c mice at three different gestation periods. Journal of Parasitology 92, 1286–1291. doi: 10.1645/GE-883R.1.Google Scholar
Lopez-Perez, I. C., Collantes-Fernandez, E., Aguado-Martinez, A., Rodriguez-Bertos, A. and Ortega-Mora, L. M. (2008). Influence of Neospora caninum infection in BALB/c mice during pregnancy in post-natal development. Veterinary Parasitology 155, 175–183. doi: 10.1016/j.vetpar.2008.05.018.Google Scholar
Lunden, A., Marks, J., Maley, S. W. and Innes, E. A. (1998). Cellular immune responses in cattle experimentally infected with Neospora caninum . Parasite Immunology 20, 519–526.Google Scholar
Macaldowie, C., Maley, S. W., Wright, S., Bartley, P., Esteban-Redondo, I., Buxton, D. and Innes, E. A. (2004). Placental pathology associated with fetal death in cattle inoculated with Neospora caninum by two different routes in early pregnancy. Journal of Comparative Pathology 131, 142–156. doi: 10.1016/j.jcpa.2004.02.005.Google Scholar
Maley, S. W., Buxton, D., Thomson, K. M., Schriefer, C. E. and Innes, E. A. (2001). Serological analysis of calves experimentally infected with Neospora caninum: a 1-year study. Veterinary Parasitology 96, 1–9.Google Scholar
Maley, S. W., Buxton, D., Rae, A. G., Wright, S. E., Schock, A., Bartley, P. M., Esteban-Redondo, I., Swales, C., Hamilton, C. M., Sales, J. and Innes, E. A. (2003). The pathogenesis of neosporosis in pregnant cattle: inoculation at mid-gestation. Journal of Comparative Pathology 129, 186–195.Google Scholar
Maley, S. W., Buxton, D., Macaldowie, C. N., Anderson, I. E., Wright, S. E., Bartley, P. M., Esteban-Redondo, I., Hamilton, C. M., Storset, A. K. and Innes, E. A. (2006). Characterization of the immune response in the placenta of cattle experimentally infected with Neospora caninum in early gestation. Journal of Comparative Pathology 135, 130–141. doi: 10.1016/j.jcpa.2006.07.001.Google Scholar
Marks, J., Lunden, A., Harkins, D. and Innes, E. (1998). Identification of Neospora antigens recognized by CD4+ T cells and immune sera from experimentally infected cattle. Parasite Immunology 20, 303–309.Google Scholar
McAllister, M. M., McGuire, A. M., Jolley, W. R., Lindsay, D. S., Trees, A. J. and Stobart, R. H. (1996). Experimental neosporosis in pregnant ewes and their offspring. Veterinary Pathology 33, 647–655.Google Scholar
McAllister, M. M., Bjorkman, C., Anderson-Sprecher, R. and Rogers, D. G. (2000). Evidence of point-source exposure to Neospora caninum and protective immunity in a herd of beef cows. Journal of the American Veterinary Medical Association 217, 881–887.Google Scholar
McCann, C. M., McAllister, M. M., Gondim, L. F., Smith, R. F., Cripps, P. J., Kipar, A., Williams, D. J. and Trees, A. J. (2007). Neospora caninum in cattle: experimental infection with oocysts can result in exogenous transplacental infection, but not endogenous transplacental infection in the subsequent pregnancy. International Journal for Parasitology 37, 1631–1639. doi: 10.1016/j.ijpara.2007.05.012.Google Scholar
Miller, C. M., Quinn, H. E., Windsor, P. A. and Ellis, J. T. (2002). Characterisation of the first Australian isolate of Neospora caninum from cattle. Australian Veterinary Journal 80, 620–625.Google Scholar
Moore, D. P., Leunda, M. R., Zamorano, P. I., Odeon, A. C., Romera, S. A., Cano, A., de Yaniz, G., Venturini, M. C. and Campero, C. M. (2005). Immune response to Neospora caninum in naturally infected heifers and heifers vaccinated with inactivated antigen during the second trimester of gestation. Veterinary Parasitology 130, 29–39. doi: 10.1016/j.vetpar.2005.03.010.Google Scholar
Moore, D. P., Echaide, I., Verna, A. E., Leunda, M. R., Cano, A., Pereyra, S., Zamorano, P. I., Odeon, A. C. and Campero, C. M. (2011). Immune response to Neospora caninum native antigens formulated with immune stimulating complexes in calves. Veterinary Parasitology 175, 245–251. doi: 10.1016/j.vetpar.2010.10.020.CrossRefGoogle ScholarPubMed
Moore, D. P., Alvarez-Garcia, G., Chiapparrone, M. L., Regidor-Cerrillo, J., Lischinsky, L. H., de Yaniz, M. G., Odeon, A. C., Ortega-Mora, L. M. and Campero, C. M. (2014). Neospora caninum tachyzoites inoculated by the conjunctival route are not vertically transmitted in pregnant cattle: a descriptive study. Veterinary Parasitology 199, 1–7. doi: 10.1016/j.vetpar.2013.10.006.Google Scholar
Moskwa, B., Pastusiak, K., Bien, J. and Cabaj, W. (2007). The first detection of Neospora caninum DNA in the colostrum of infected cows. Parasitology Research 100, 633–636. doi: 10.1007/s00436-006-0288-7.Google Scholar
Muller, J. and Hemphill, A. (2013). In vitro culture systems for the study of apicomplexan parasites in farm animals. International Journal for Parasitology 43, 115–124. doi: 10.1016/j.ijpara.2012.08.004.Google Scholar
Nishimura, M., Kohara, J., Hiasa, J., Muroi, Y., Yokoyama, N., Kida, K., Xuan, X., Furuoka, H. and Nishikawa, Y. (2013). Tissue distribution of Neospora caninum in experimentally infected cattle. Clinical and Vaccine Immunology 20, 309–312. doi: 10.1128/CVI.00556-12; 10.1128/CVI.00556-12.Google Scholar
O'Handley, R., Liddell, S., Parker, C., Jenkins, M. C. and Dubey, J. P. (2002). Experimental infection of sheep with Neospora caninum oocysts. Journal of Parasitology 88, 1120–1123. doi: 10.1645/0022-3395(2002)088[1120:EIOSWN]2.0.CO;2.Google Scholar
O'Handley, R. M., Morgan, S. A., Parker, C., Jenkins, M. C. and Dubey, J. P. (2003). Vaccination of ewes for prevention of vertical transmission of Neospora caninum . American Journal of Veterinary Research 64, 449–452.Google Scholar
Ortega-Mora, L. M., Ferre, I., del-Pozo, I., Caetano-da-Silva, A., Collantes-Fernandez, E., Regidor-Cerrillo, J., Ugarte-Garagalza, C. and Aduriz, G. (2003). Detection of Neospora caninum in semen of bulls. Veterinary Parasitology 117, 301–308.Google Scholar
Ortega-Mora, L. M., Regidor-Cerrillo, J., Rojo-Montejo, S., Collantes-Fernandez, E. and Alvarez-Garcia, G. (2012). Vaccine development against bovine neosporosis: present situation and in vitro and in vivo models to test safety and efficacy. In Proceedings of the 1st Apicowplexa. Apicomplexa in Farm Animals Meeting, Lisbon, October 2012, p. 57.Google Scholar
Osoro, K., Ortega-Mora, L. M., Martinez, A., Serrano-Martinez, E. and Ferre, I. (2009). Natural breeding with bulls experimentally infected with Neospora caninum failed to induce seroconversion in dams. Theriogenology 71, 639–642. doi: 10.1016/j.theriogenology.2008.09.035.Google Scholar
Pan, Y., Jansen, G. B., Duffield, T. F., Hietala, S., Kelton, D., Lin, C. Y. and Peregrine, A. S. (2004). Genetic susceptibility to Neospora caninum infection in Holstein cattle in Ontario. Journal of Dairy Science 87, 3967–3975. doi: S0022-0302(04)73537-7.Google Scholar
Pare, J., Thurmond, M. C. and Hietala, S. K. (1997). Neospora caninum antibodies in cows during pregnancy as a predictor of congenital infection and abortion. Journal of Parasitology 83, 82–87.Google Scholar
Pereira, G. R., Vogel, F. S., Bohrer, R. C., da Nobrega, J. E. Jr, Ilha, G. F., da Rosa, P. R., Glanzner, W. G., Camillo, G., Braunig, P., de Oliveira, J. F. and Goncalves, P. B. (2014). Neospora caninum DNA detection by TaqMan real-time PCR assay in experimentally infected pregnant heifers. Veterinary Parasitology 199, 129–135. doi: 10.1016/j.vetpar.2013.10.018.Google Scholar
Pereira-Bueno, J., Quintanilla-Gozalo, A., Perez-Perez, V., Espi-Felgueroso, A., Alvarez-Garcia, G., Collantes-Fernandez, E. and Ortega-Mora, L. M. (2003). Evaluation by different diagnostic techniques of bovine abortion associated with Neospora caninum in Spain. Veterinary Parasitology 111, 143–152.Google Scholar
Peters, M., Lutkefels, E., Heckeroth, A. R. and Schares, G. (2001). Immunohistochemical and ultrastructural evidence for Neospora caninum tissue cysts in skeletal muscles of naturally infected dogs and cattle. International Journal for Parasitology 31, 1144–1148.Google Scholar
Quintanilla-Gozalo, A., Pereira-Bueno, J., Seijas-Carballedo, A., Costas, E. and Ortega-Mora, L. M. (2000). Observational studies in Neospora caninum infected dairy cattle: relationship between infection/abortion and gestational antibody fluctuations. International Journal for Parasitology 30, 900–906.Google Scholar
Regidor-Cerrillo, J., Gomez-Bautista, M., Del Pozo, I., Jimenez-Ruiz, E., Aduriz, G. and Ortega-Mora, L. M. (2010). Influence of Neospora caninum intra-specific variability in the outcome of infection in a pregnant BALB/c mouse model. Veterinary Research 41, 52. doi: 10.1051/vetres/2010024.Google Scholar
Regidor-Cerrillo, J., Gomez-Bautista, M., Sodupe, I., Aduriz, G., Alvarez-Garcia, G., Del Pozo, I. and Ortega-Mora, L. M. (2011). In vitro invasion efficiency and intracellular proliferation rate comprise virulence-related phenotypic traits of Neospora caninum . Veterinary Research 42, 41. doi: 10.1186/1297-9716-42-41.Google Scholar
Regidor-Cerrillo, J., Alvarez-Garcia, G., Pastor-Fernandez, I., Marugan-Hernandez, V., Gomez-Bautista, M. and Ortega-Mora, L. M. (2012). Proteome expression changes among virulent and attenuated Neospora caninum isolates. Journal of Proteomics 75, 2306–2318. doi: 10.1016/j.jprot.2012.01.039.Google Scholar
Regidor-Cerrillo, J., Arranz-Solis, D., Benavides, J., Gomez-Bautista, M., Castro-Hermida, J. A., Mezo, M., Pére, z V., Ortega-Mora, L. M. and 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. doi: 10.1186/1297-9716-45-10.Google Scholar
Reichel, M. P. and Ellis, J. T. (2002). Control options for Neospora caninum infections in cattle – current state of knowledge. New Zealand Veterinary Journal 50, 86–92. doi: 10.1080/00480169.2002.36288.Google Scholar
Reichel, M. P., Alejandra Ayanegui-Alcerreca, 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, 133–142. doi: 10.1016/j.ijpara.2012.10.022.Google Scholar
Rettigner, C., Lasri, S., De Meerschman, F., Focant, C., Beckers, J. F. and Losson, B. (2004). Immune response and antigen recognition in non-pregnant ewes experimentally infected with Neospora caninum tachyzoites. Veterinary Parasitology 122, 261–271. doi: 10.1016/j.vetpar.2003.12.017.Google Scholar
Rocchi, M. S., Bartley, P. M., Inglis, N. F., Collantes-Fernandez, E., Entrican, G., Katzer, F. and Innes, E. A. (2011). Selection of Neospora caninum antigens stimulating bovine CD4+ve T cell responses through immuno-potency screening and proteomic approaches. Veterinary Research 42, 91. doi: 10.1186/1297-9716-42-91.CrossRefGoogle ScholarPubMed
Rojo-Montejo, S., Collantes-Fernandez, E., Blanco-Murcia, J., Rodriguez-Bertos, A., Risco-Castillo, V. and Ortega-Mora, L. M. (2009). Experimental infection with a low virulence isolate of Neospora caninum at 70 days gestation in cattle did not result in foetopathy. Veterinary Research 40, 49. doi: 10.1051/vetres/2009032.Google Scholar
Rojo-Montejo, S., Collantes-Fernandez, E., Regidor-Cerrillo, J., Rodriguez-Bertos, A., Prenafeta, A., Gomez-Bautista, M. and Ortega-Mora, L. M. (2011). Influence of adjuvant and antigen dose on protection induced by an inactivated whole vaccine against Neospora caninum infection in mice. Veterinary Parasitology 175, 220–229. doi: 10.1016/j.vetpar.2010.10.028.Google Scholar
Rojo-Montejo, S., Collantes-Fernandez, E., Perez-Zaballos, F., Rodriguez-Marcos, S., Blanco-Murcia, J., Rodriguez-Bertos, A., Prenafeta, A. and Ortega-Mora, L. M. (2013). Effect of vaccination of cattle with the low virulence Nc-Spain 1H isolate of Neospora caninum against a heterologous challenge in early and mid-gestation. Veterinary Research 44, 106. doi: 10.1186/1297-9716-44-106.Google Scholar
Rosbottom, A., Guy, C. S., Gibney, E. H., Smith, R. F., Valarcher, J. F., Taylor, G. and Williams, D. J. (2007). Peripheral immune responses in pregnant cattle following Neospora caninum infection. Parasite Immunology 29, 219–228. doi: 10.1111/j.1365-3024.2007.00936.x.Google Scholar
Rosbottom, A., Gibney, E. H., Guy, C. S., Kipar, A., Smith, R. F., Kaiser, P., Trees, A. J. and Williams, D. J. (2008). Upregulation of cytokines is detected in the placentas of cattle infected with Neospora caninum and is more marked early in gestation when fetal death is observed. Infection and Immunity 76, 2352–2361. doi: 10.1128/IAI.01780-06.Google Scholar
Rosbottom, A., Gibney, H., Kaiser, P., Hartley, C., Smith, R. F., Robinson, R., Kipar, A. and Williams, D. J. (2011). Up regulation of the maternal immune response in the placenta of cattle naturally infected with Neospora caninum . PLOS ONE 6, e15799. doi: 10.1371/journal.pone.0015799.Google Scholar
Schares, G., Peters, M., Wurm, R., Barwald, A. and Conraths, F. J. (1998). The efficiency of vertical transmission of Neospora caninum in dairy cattle analysed by serological techniques. Veterinary Parasitology 80, 87–98.Google Scholar
Schares, G., Heydorn, A. O., Cuppers, A., Conraths, F. J. and Mehlhorn, H. (2001). Hammondia heydorni-like oocysts shed by a naturally infected dog and Neospora caninum NC-1 cannot be distinguished. Parasitology Research 87, 808–816.Google Scholar
Serrano, E., Ferre, I., Osoro, K., Aduriz, G., Mateos-Sanz, A., Martinez, A., Atxaerandio, R., Hidalgo, C. O. and Ortega-Mora, L. M. (2006). Intrauterine Neospora caninum inoculation of heifers. Veterinary Parasitology 135, 197–203. doi: 10.1016/j.vetpar.2005.10.003.Google Scholar
Serrano-Martinez, E., Ferre, I., Martinez, A., Osoro, K., Mateos-Sanz, A., Del-Pozo, I., Aduriz, G., Tamargo, C., Hidalgo, C. O. and Ortega-Mora, L. M. (2007 a). Experimental neosporosis in bulls: parasite detection in semen and blood and specific antibody and interferon-gamma responses. Theriogenology 67, 1175–1184. doi: 10.1016/j.theriogenology.2007.01.010.Google Scholar
Serrano-Martinez, E., Ferre, I., Osoro, K., Aduriz, G., Mota, R. A., Martinez, A., Del-Pozo, I., Hidalgo, C. O. and Ortega-Mora, L. M. (2007 b). Intrauterine Neospora caninum inoculation of heifers and cows using contaminated semen with different numbers of tachyzoites. Theriogenology 67, 729–737. doi: 10.1016/j.theriogenology.2006.10.004.Google Scholar
Staska, L. M., McGuire, T. C., Davies, C. J., Lewin, H. A. and Baszler, T. V. (2003). Neospora caninum-infected cattle develop parasite-specific CD4+ cytotoxic T lymphocytes. Infection and Immunity 71, 3272–3279.Google Scholar
Stenlund, S., Kindahl, H., Magnusson, U., Uggla, A. and Bjorkman, C. (1999). Serum antibody profile and reproductive performance during two consecutive pregnancies of cows naturally infected with Neospora caninum . Veterinary Parasitology 85, 227–234.Google Scholar
Syed-Hussain, S. S., Howe, L., Pomroy, W. E., West, D. M., Smith, S. L. and Williamson, N. B. (2013). Detection of Neospora caninum DNA in semen of experimental infected rams with no evidence of horizontal transmission in ewes. Veterinary Parasitology 197, 534–542. doi: 10.1016/j.vetpar.2013.06.002.Google Scholar
Thurmond, M. C. and Hietala, S. K. (1997). Effect of congenitally acquired Neospora caninum infection on risk of abortion and subsequent abortions in dairy cattle. American Journal of Veterinary Research 58, 1381–1385.Google Scholar
Trees, A. J. and Williams, D. J. (2005). Endogenous and exogenous transplacental infection in Neospora caninum and Toxoplasma gondii . Trends in Parasitology 21, 558–561. doi: 10.1016/j.pt.2005.09.005.Google Scholar
Trees, A. J., Davison, H. C., Innes, E. A. and Wastling, J. M. (1999). Towards evaluating the economic impact of bovine neosporosis. International Journal for Parasitology 29, 1195–1200.CrossRefGoogle ScholarPubMed
Trees, A. J., McAllister, M. M., Guy, C. S., McGarry, J. W., Smith, R. F. and Williams, D. J. (2002). Neospora caninum: oocyst challenge of pregnant cows. Veterinary Parasitology 109, 147–154.Google Scholar
Tuo, W., Fetterer, R., Jenkins, M. and Dubey, J. P. (2005). Identification and characterization of Neospora caninum cyclophilin that elicits gamma interferon production. Infection and Immunity 73, 5093–5100. doi: 10.1128/IAI.73.8.5093-5100.2005.Google Scholar
Uggla, A., Stenlund, S., Holmdahl, O. J., Jakubek, E. B., Thebo, P., Kindahl, H. and Bjorkman, C. (1998). Oral Neospora caninum inoculation of neonatal calves. International Journal for Parasitology 28, 1467–1472.Google Scholar
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 Veterinary Medicine 93, 129–138. doi: 10.1016/j.prevetmed.2009.11.013.Google Scholar
VanLeeuwen, J. A., Greenwood, S., Clark, F., Acorn, A., Markham, F., McCarron, J. and O'Handley, R. (2011). Monensin use against Neospora caninum challenge in dairy cattle. Veterinary Parasitology 175, 372–376. doi: 10.1016/j.vetpar.2010.10.016.Google Scholar
Weber, F. H., Jackson, J. A., Sobecki, B., Choromanski, L., Olsen, M., Meinert, T., Frank, R., Reichel, M. P. and Ellis, J. T. (2013). On the efficacy and safety of vaccination with live tachyzoites of Neospora caninum for prevention of neospora-associated fetal loss in cattle. Clinical and Vaccine Immunology 20, 99–105. doi: 10.1128/CVI.00225-12.CrossRefGoogle ScholarPubMed
Weston, J. F., Howe, L., Collett, M. G., Pattison, R. S., Williamson, N. B., West, D. M., Pomroy, W. E., Syed-Hussain, S. S., Morris, S. T. and Kenyon, P. R. (2009). Dose-titration challenge of young pregnant sheep with Neospora caninum tachyzoites. Veterinary Parasitology 164, 183–191. doi: 10.1016/j.vetpar.2009.05.013.Google Scholar
Wiengcharoen, J., Thompson, R. C., Nakthong, C., Rattanakorn, P. and Sukthana, Y. (2011). Transplacental transmission in cattle: is Toxoplasma gondii less potent than Neospora caninum? Parasitology Research 108, 1235–1241. doi: 10.1007/s00436-010-2172-8.Google Scholar
Williams, D. J. and Trees, A. J. (2006). Protecting babies: vaccine strategies to prevent foetopathy in Neospora caninum-infected cattle. Parasite Immunology 28, 61–67.Google Scholar
Williams, D. J., Guy, C. S., McGarry, J. W., Guy, F., Tasker, L., Smith, R. F., MacEachern, K., Cripps, P. J., Kelly, D. F. and Trees, A. J. (2000). Neospora caninum-associated abortion in cattle: the time of experimentally-induced parasitaemia during gestation determines foetal survival. Parasitology 121, 347–358.Google Scholar
Williams, D. J., Guy, C. S., Smith, R. F., Guy, F., McGarry, J. W., McKay, J. S. and Trees, A. J. (2003). First demonstration of protective immunity against foetopathy in cattle with latent Neospora caninum infection. International Journal for Parasitology 33, 1059–1065.Google Scholar
Williams, D. J., Guy, C. S., Smith, R. F., Ellis, J., Bjorkman, C., Reichel, M. P. and Trees, A. J. (2007). Immunization of cattle with live tachyzoites of Neospora caninum confers protection against fetal death. Infection and Immunity 75, 1343–1348. doi: 10.1128/IAI.00777-06.Google Scholar
Williams, D. J., Hartley, C. S., Bjorkman, C. and Trees, A. J. (2009). Endogenous and exogenous transplacental transmission of Neospora caninum – how the route of transmission impacts on epidemiology and control of disease. Parasitology 136, 1895–1900. doi: 10.1017/S0031182009990588.CrossRefGoogle ScholarPubMed
Wouda, W., Moen, A. R., Visser, I. J. and van Knapen, F. (1997). Bovine fetal neosporosis: a comparison of epizootic and sporadic abortion cases and different age classes with regard to lesion severity and immunohistochemical identification of organisms in brain, heart, and liver. Journal of Veterinary Diagnostic Investigation 9, 180–185.Google Scholar
Wouda, W., Moen, A. R. and Schukken, Y. H. (1998). Abortion risk in progeny of cows after a Neospora caninum epidemic. Theriogenology 49, 1311–1316. doi: 10.1016/S0093-691X(98)00078-8.Google Scholar
Yin, J., Qu, G., Cao, L., Li, Q., Fetterer, R., Feng, X., Liu, Q., Wang, G., Qi, D., Zhang, X., Miramontes, E., Jenkins, M., Zhang, N. and Tuo, W. (2012). Characterization of Neospora caninum microneme protein 10 (NcMIC10) and its potential use as a diagnostic marker for neosporosis. Veterinary Parasitology 187, 28–35. doi: 10.1016/j.vetpar.2012.01.003.Google Scholar