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Vaccination as a control strategy against the coccidial parasites Eimeria, Toxoplasma and Neospora

Published online by Cambridge University Press:  02 February 2007

E. A. INNES
Affiliation:
Moredun Research Institute, Pentlands Science Park, Edinburgh EH26 OPZ, UK
A. N. VERMEULEN
Affiliation:
Intervet International, Boxmeer, The Netherlands

Abstract

The protozoan parasites Eimeria spp. Toxoplasma gondii and Neospora caninum are significant causes of disease in livestock worldwide and T. gondii is also an important human pathogen. Drugs have been used with varying success to help control aspects of these diseases and commercial vaccines are available for all three groups of parasites. However, there are issues with increasing development of resistance to many of the anti-coccidial drugs used to help control avian eimeriosis and public concerns about the use of drugs in food animals. In addition there are no drugs available that can act against the tissue cyst stage of either T. gondii or N. caninum and thus cure animals or people of infection. All three groups of parasites multiply within the cells of their host species and therefore cell mediated immune mechanisms are thought to be an important component of host protective immunity. Successful vaccination strategies for both Eimeria and Toxoplasma have relied on using a live vaccination approach using attenuated parasites which allows correct processing and presentation of antigen to the host immune system to stimulate appropriate cell mediated immune responses. However, live vaccines can have problems with safety, short shelf-life and large-scale production; therefore there is continued interest in devising new vaccines using defined recombinant antigens. The major challenges in devising novel vaccines are to select relevant antigens and then present them to the immune system in an appropriate manner to enable the induction of protective immune responses. With all three groups of parasites, vaccine preparations comprising antigens from the different life cycle stages may also be advantageous. In the case of Eimeria parasites there are also problems with strain-specific immunity therefore a cocktail of antigens from different parasite strains may be required. Improving our knowledge of the different parasite transmission routes, host-parasite relationships, disease pathogenesis and determining the various roles of the host immune response being at times host-protective, parasite protective and in causing immunopathology will help to tailor a vaccination strategy against a particular disease target. This paper discusses current vaccination strategies to help combat infections with Eimeria, Toxoplasma and Neospora and recent research looking towards developing new vaccine targets and approaches.

Type
Research Article
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Alaeddine, F., Keller, N., Leepin, A. and Hemphill, A. ( 2005). Reduced infection and protection from clinical signs of cerebral neosporosis in C57BL/6 mice vaccinated with recombinant microneme antigen NcMIC1. Journal of Parasitology 91, 657665.CrossRefGoogle Scholar
Alexander, J., Jebbari, H., Bluethmann, H., Satoskar, A. and Roberts, C. W. ( 1996). Immunological control of Toxoplasma gondii and appropriate vaccine design. Current Topics in Microbiology and Immunology 219, 183195.CrossRefGoogle 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, 383392.CrossRefGoogle Scholar
Ammassari, A., Murri, R., Cingolani, A., De Luca, A. and Antinori, A. ( 1996). AIDS-associated cerebral toxoplasmosis: an update on diagnosis and treatment. Current Topics in Microbiology and Immunology 219, 209222.CrossRefGoogle Scholar
Anderson, M. L., Blanchard, P. C., Barr, B. C., Dubey, J. P., Hoffman, R. L. and Conrad, P. A. ( 1991). Neospora-like protozoan infection as a major cause of abortion in California dairy cattle. Journal of the American Veterinary Medical Association 198, 241244.Google Scholar
Anderson, M. L., Palmer, C. W., Thurmond, M. C., Picanso, J. P., Blanchard, P. C., Breitmeyer, R. E., Layton, A. W., McAllister, M., Daft, B. and Kinde, H. ( 1995). Evaluation of abortions in cattle attributable to neosporosis in selected dairy herds in California. Journal of the American Veterinary Medical Association 207, 12061210.Google Scholar
Andrianarivo, A. G., Anderson, M. L., Rowe, J. D., Gardner, I. A., Reynolds, J. P., Choromanski, L. and Conrad, P. A. ( 2005). Immune responses during pregnancy in heifers naturally infected with Neospora caninum with and without immunization. Parasitology Research 96, 2431.CrossRefGoogle 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, 817825.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, 985990.Google Scholar
Angus, C. W., Klivington-Evans, D., Dubey, J. P and Kovacs, J. A. ( 2000). Immunisation with a DNA plasmid encoding the SAG1 (P30) protein of Toxoplasma gondii is immunogenic and protective in rodents. Journal of Infectious Diseases 181, 317324.CrossRefGoogle Scholar
Avelino, M. M., Campos, D. Jr., Parada, J. B. and Castro, A. M. ( 2004). Risk factors for Toxoplasma gondii infection in women of childbearing age. Brazilian Journal of Infectious Diseases 8, 164174.CrossRefGoogle Scholar
Bahia-Oliveira, L. M., Jones, J. L., Zevedo-Silva, J., Alves, C. C., Orefice, F. and Addiss, D. G. ( 2003). Highly endemic, waterborne toxoplasmosis in north Rio de Janeiro state, Brazil. Emerging Infectious Diseases 9, 5562.CrossRefGoogle Scholar
Barber, J. S. and Trees, A. J. ( 1996). Clinical aspects of 27 cases of neosporosis in dogs. Veterinary Record 139, 439443.CrossRefGoogle Scholar
Barr, B. C., Conrad, P. A., Breitmeyer, R., Sverlow, K., Anderson, M. L., Reynolds, J., Chauvet, A. E., Dubey, J. P. and Ardans, A. A. ( 1993). Congenital Neospora infection in calves born from cows that had previously aborted Neospora-infected fetuses: four cases (1990–1992). Journal of the American Veterinary Medical Association 202, 113117.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, 207215.CrossRefGoogle 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, 8191.CrossRefGoogle 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, 612618.CrossRefGoogle Scholar
Baszler, T. V., Long, M. T., McElwain, T. F. and Mathison, B. A. ( 1999). Interferon-gamma and interleukin-12 mediate protection to acute Neospora caninum infection in BALB/c mice. International Journal for Parasitology 29, 16351646.CrossRefGoogle Scholar
Baszler, T. V., McElwain, T. F. and Mathison, B. A. ( 2000). Immunization of BALB/c mice with killed Neospora caninum tachyzoite antigen induces a type 2 immune response and exacerbates encephalitis and neurological disease. Clinical and Diagnostic Laboratory Immunology 7, 893898.CrossRefGoogle Scholar
Beghetto, E., Nielsen, H. V., Del Porto, P., Buffolano, W., Guglietta, S., Felici, F., Petersen, E. and Gargano, N. ( 2005). A combination of antigenic regions of Toxoplasma gondii microneme proteins induces protective immunity against oral infection with parasite cysts. Journal of Infectious Diseases 191, 637645.CrossRefGoogle Scholar
Bjerkas, I., Mohn, S. F. and Presthus, J. ( 1984). Unidentified cyst-forming sporozoon causing encephalomyelitis and myositis in dogs. Zeitschrift für Parasitenkunde 70, 271274.CrossRefGoogle Scholar
Bjorkman, 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, 14411444.Google Scholar
Bourguin, I., Chardes, T. and Bout, D. ( 1993). Oral immunization with Toxoplasma gondii antigens in association with cholera toxin induces enhanced protective and cell-mediated immunity in C57BL/6 mice. Infection and Immunity 61, 20822088.Google Scholar
Bowie, W. R., King, A. S., Werker, D. H., Isaac-Renton, J. L., Bell, A., Eng, S. B. and Marion, S. A. ( 1997). Outbreak of toxoplasmosis associated with municipal drinking water. The BC Toxoplasma Investigation Team. The Lancet 350, 173177.CrossRefGoogle Scholar
Boyle, D. B. and Heine, H. G. ( 1993). Recombinant fowlpox virus vaccines for poultry. Immunology and Cell Biology 71, 391397.CrossRefGoogle 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, 953960.CrossRefGoogle Scholar
Bozzette, S. A., Forthal, D., Sattler, F. R., Kemper, C., Richman, D. D., Tilles, J. G., Leedom, J. and McCutchan, J. A. ( 1995). The tolerance for zidovudine plus thrice weekly or daily trimethoprim-sulfamethoxazole with and without leucovorin for primary prophylaxis in advanced HIV disease. California Collaborative Treatment Group. American Journal of Medicine 98, 177182.CrossRefGoogle Scholar
Breed, D. G., Schetters, T. P., Verhoeven, N. A. and Vermeulen, A. N. ( 1997). Characterization of phenotype related responsiveness of peripheral blood lymphocytes from Eimeria tenella infected chickens. Parasite Immunology 19, 563569.CrossRefGoogle Scholar
Bulow, R. and Boothroyd, J. C. ( 1991). Protection of mice from fatal Toxoplasma gondii infection by immunization with p30 antigen in liposomes. Journal of Immunology 147, 34963500.Google Scholar
Buxton, D. ( 1998). Protozoan infections (Toxoplasma gondii, Neospora caninum and Sarcocystis spp.) in sheep and goats: recent advances. Veterinary Research 29, 289310.Google Scholar
Buxton, D. and Innes, E. A. ( 1995). A commercial vaccine for ovine toxoplasmosis. Parasitology 110 (Suppl), S11S16.CrossRefGoogle 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, 267279.CrossRefGoogle Scholar
Buxton, D., McAllister, M. M. and Dubey, J. P. ( 2002). The comparative pathogenesis of neosporosis. Trends in Parasitology 18, 546552.CrossRefGoogle Scholar
Buxton, D., Thomson, K. M., Maley, S., Wright, S. and Bos, H. J. ( 1993). Experimental challenge of sheep 18 months after vaccination with a live (S48) Toxoplasma gondii vaccine. Veterinary Record 133, 310312.CrossRefGoogle Scholar
Buxton, D., Uggla, A., Lovgren, K., Thomson, K., Lunden, A., Morein, B. and Blewett, D. A. ( 1989). Trial of a novel experimental Toxoplasma iscom vaccine in pregnant sheep. British Veterinary Journal 145, 451457.CrossRefGoogle Scholar
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, 8591.CrossRefGoogle Scholar
Buzoni-Gatel, D., Lepage, A. C., Mier-Poisson, I. H., Bout, D. T. and Kasper, L. H. ( 1997). Adoptive transfer of gut intraepithelial lymphocytes protects against murine infection with Toxoplasma gondii. Journal of Immunology 158, 58835889.Google Scholar
Cannas, A., Naguleswaran, A., Muller, N., Eperon, S., Gottstein, B. and Hemphill, A. ( 2003 b). Vaccination of mice against experimental Neospora caninum infection using NcSAG1- and NcSRS2-based recombinant antigens and DNA vaccines. Parasitology 126, 303312.Google Scholar
Cannas, A., Naguleswaran, A., Muller, N., Gottstein, B. and Hemphill, A. ( 2003 a). Reduced cerebral infection of Neospora caninum-infected mice after vaccination with recombinant microneme protein NcMIC3 and ribi adjuvant. Journal of Parasitology 89, 4450.Google Scholar
Chaouat, G., Menu, E., Clark, D. A., Dy, M., Minkowski, M. and Wegmann, T. G. ( 1990). Control of fetal survival in CBA×DBA/2 mice by lymphokine therapy. Journal of Reproductive Fertility 89, 447458.CrossRefGoogle Scholar
Cho, J. H., Chung, W. S., Song, K. J., Na, B. K., Kang, S. W., Song, C. Y. and Kim, T. S. ( 2005). Protective efficacy of vaccination with Neospora caninum multiple recombinant antigens against experimental Neospora caninum infection. Korean Journal of Parasitology 43, 1925.CrossRefGoogle Scholar
Choromanski, L., Freyre, A., Popiel, R., Brown, K., Grieve, R. and Shibley, G. ( 1995). Safety and efficacy of modified live feline Toxoplasma gondii vaccine. Developments in Biological Standardization 84, 269281.Google Scholar
Coombs, G. H. and Muller, S. ( 2002). Recent advances in the search for new anti-coccidial drugs. International Journal for Parasitology 32, 497508.CrossRefGoogle Scholar
Couper, K. N., Nielsen, H. V., Petersen, E., Roberts, F., Roberts, C. W. and Alexander, J. ( 2003). DNA vaccination with the immunodominant tachyzoite surface antigen (SAG-1) protects against adult acquired Toxoplasma gondii infection but does not prevent maternofoetal transmission. Vaccine 21, 28132820.CrossRefGoogle Scholar
Crane, M. S., Murray, P. K., Gnozzio, M. J. and MacDonald, T. T. ( 1988). Passive protection of chickens against Eimeria tenella infection by monoclonal antibody. Infection and Immunity 56, 972976.Google Scholar
Cronenberg, A. M., Van Geffen, C. E., Dorrestein, J., Vermeulen, A. N. and Sondermeijer, P. J. ( 1999). Vaccination of broilers with HVT expressing an Eimeria acervulina antigen improves performance after challenge with Eimeria. Acta Virologica 43, 192197.Google Scholar
Curiel, T. J., Krug, E. C., Purner, M. B., Poignard, P. and Berens, R. L. ( 1993). Cloned human CD4+ cytotoxic T lymphocytes specific for Toxoplasma gondii lyse tachyzoite-infected target cells. Journal of Immunology 151, 20242031.Google Scholar
Dalloul, R. A. and Lillehoj, H. S. ( 2005). Recent advances in immunomodulation and vaccination strategies against coccidiosis. Avian Diseases 49, 18.CrossRefGoogle Scholar
Dalloul, R. A., Lillehoj, H. S., Klinman, D. M., Ding, X., Min, W., Heckert, R. A. and Lillehoj, E. P. ( 2005). In ovo administration of CpG oligodeoxynucleotides and the recombinant microneme protein MIC2 protects against Eimeria infections. Vaccine 23, 31083113.CrossRefGoogle Scholar
Davison, H. C., Otter, A. and Trees, A. J. ( 1999). Estimation of vertical and horizontal transmission parameters of Neospora caninum infections in dairy cattle. International Journal for Parasitology 29, 16831689.CrossRefGoogle Scholar
Debard, N., Buzoni-Gatel, D. and Bout, D. ( 1996). Intranasal immunization with SAG1 protein of Toxoplasma gondii in association with cholera toxin dramatically reduces development of cerebral cysts after oral infection. Infection and Immunity 64, 21582166.Google Scholar
Derouin, F. ( 2000). Drugs effective against Toxoplasma gondii. Present status and future prospective. In Congenital Toxoplasmosis ( ed. Ambroise-Thomas, P. and Peterson, E.), pp. 95110. Springer-Verlag France.
Desmonts, G. and Couvreur, J. ( 1979). Congenital toxoplasmosis: a prospective study of the offspring of 542 women who acquired toxoplasmosis during pregnancy: pathophysiology of congenital disease. In Perinatal Medicine: Sixth European Congress ( ed. Thalhammer, O., Baumgarten, K. and Pollak, A.), pp. 5160. Georg Thieme Verlag.
Dijkstra, T., Eysker, M., Schares, G., Conraths, F. J., Wouda, W. and Barkema, H. W. ( 2001). 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, 747752.CrossRefGoogle Scholar
Ding, X., Lillehoj, H. S., Dalloul, R. A., Min, W., Sato, T., Yasuda, A. and Lillehoj, E. P. ( 2005). In ovo vaccination with the Eimeria tenella EtMIC2 gene induces protective immunity against coccidiosis. Vaccine 23, 37333740.CrossRefGoogle Scholar
Du, A. and Wang, S. ( 2005). Efficacy of a DNA vaccine delivered in attenuated Salmonella typhimurium against Eimeria tenella infection in chickens. International Journal for Parasitology 35, 777785.CrossRefGoogle Scholar
Dubey, J. P. ( 1986). A review of toxoplasmosis in cattle. Veterinary Parasitology 22, 177202.CrossRefGoogle Scholar
Dubey, J. P. ( 1999). Recent advances in Neospora and neosporosis. Veterinary Parasitology 84, 349367.CrossRefGoogle Scholar
Dubey, J. P. ( 2003). Neosporosis in Cattle. Journal of Parasitology 89, S42S56.Google Scholar
Dubey, J. P. and Beattie, C. P. ( 1988). Toxoplasmosis of Animals and Man. CRC Press, Boca Raton, Florida.
Dubey, J. P., Carpenter, J. L., Speer, C. A., Topper, M. J. and Uggla, A. ( 1988 a). Newly recognized fatal protozoan disease of dogs. Journal of the American Veterinary Medical Association 192, 12691285.Google Scholar
Dubey, J. P., Dorough, K. R., Jenkins, M. C., Liddell, S., Speer, C. A., Kwok, O. C. H and Shen, S. K. ( 1998). Canine neosporosis: clinical signs, diagnosis, treatment and isolation of Neospora caninum in mice and cell culture. International Journal for Parasitology 28, 12931304.CrossRefGoogle Scholar
Dubey, J. P., Hattel, A. L., Lindsay, D. S. and Topper, M. J. ( 1988 b). Neonatal Neospora caninum infection in dogs: isolation of the causative agent and experimental transmission. Journal of the American Veterinary Medical Association 193, 12591263.Google Scholar
Dubey, J. P. and Lindsay, D. S. ( 1996). A review of Neospora caninum and neosporosis. Veterinary Parasitology 67, 159.CrossRefGoogle Scholar
Dubey, J. P. and Urban, J. F. Jr. ( 1990). Diagnosis of transplacentally induced toxoplasmosis in pigs. American Journal of Veterinary Research 51, 12951299.Google Scholar
Dubey, J. P., Urban, J. F. Jr. and Davis, S. W. ( 1991). Protective immunity to toxoplasmosis in pigs vaccinated with a nonpersistent strain of Toxoplasma gondii. American Journal of Veterinary Research 52, 13161319.Google Scholar
Dubey, J. P., Zarnke, R., Thomas, N. J., Wong, S. K., Van, Bonn W., Briggs, M., Davis, J. W., Ewing, R., Mense, M., Kwok, O. C., Romand, S. and Thulliez, P. ( 2003). Toxoplasma gondii, Neospora caninum, Sarcocystis neurona and Sarcocystis canis like infections in marine mammals. Veterinary Parasitology 116, 275296.CrossRefGoogle Scholar
Entrican, G. ( 2002). Immune regulation during pregnancy and host-pathogen interactions in infectious abortion. Journal of Comparative Pathology 126, 7994.CrossRefGoogle Scholar
Eperon, S., Bronnimann, K., Hemphill, A. and Gottstein, B. ( 1999). Susceptibility of B-cell deficient C57BL/6 (microMT) mice to Neospora caninum infection. Parasite Immunology 21, 225236.CrossRefGoogle Scholar
Esteban-Redondo, I. and Innes, E. A. ( 1997). Toxoplasma gondii infection in sheep and cattle. Comparative Immunology Microbiology and Infectious Diseases 20, 191196.CrossRefGoogle Scholar
Frenkel, J. K. ( 2000). Biology of Toxoplasma gondii. In Congenital Toxoplasmosis ( ed. Ambroise-Thomas, P. and Peterson, E.), pp. 925. Springer-Verlag France.CrossRef
Frenkel, J. K., Pfefferkorn, E. R., Smith, D. D. and Fishback, J. L. ( 1991). Prospective vaccine prepared from a new mutant of Toxoplasma gondii for use in cats. Journal of Immunology 52, 759763.Google Scholar
Freyre, A., Choromanski, L., Fishback, J. L. and Popiel, I. ( 1993). Immunization of cats with tissue cysts, bradyzoites, and tachyzoites of the T-263 strain of Toxoplasma gondii. Journal of Parasitology 79, 716719.CrossRefGoogle Scholar
Garcia, J. L., Gennari, S. M., Navarro, I. T., MacHado, R. Z., Sinhorini, I. L., Freire, R. L., Marana, E. R., Tsutsui, V., Contente, A. P. and Begale, L. P. ( 2005). Partial protection against tissue cysts formation in pigs vaccinated with crude rhoptry proteins of Toxoplasma gondii. Veterinary Parasitology 129, 209217.CrossRefGoogle Scholar
Gazzinelli, R. T., Hakim, F. T., Hieny, S., Shearer, G. M. and Sher, A. ( 1991). Synergistic role of CD4+ and CD8+ T lymphocytes in IFN-gamma production and protective immunity induced by an attenuated Toxoplasma gondii vaccine. Journal of Immunology 146, 286292.Google Scholar
Gazzinelli, R. T., Hieny, S., Wynn, T. A., Wolf, S. and Sher, A. ( 1993). Interleukin 12 is required for the T-lymphocyte-independent induction of interferon gamma by an intracellular parasite and induces resistance in T-cell-deficient hosts. Proceedings of the National Academy of Sciences, USA 90, 61156119.CrossRefGoogle Scholar
Gazzinelli, R. T., Wysocka, M., Hieny, S., Scharton-Kersten, T., Cheever, A., Kuhn, R., Muller, W., Trinchieri, G. and Sher, A. ( 1996). In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha. Journal of Immunology 157, 798805.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, 11591163.CrossRefGoogle Scholar
Gondim, L. F., McAllister, M. M., Anerson-Sprecher, R. C., Bjorkman, C., Lock, T. F., Firkins, L. D., Gao, L. and Fischer, W. R. ( 2004 b). Transplacental transmission and abortion in cows administered Neospora caninum oocysts. Journal of Parasitology 90, 13944000.Google Scholar
Gondim, L. F. P., McAllister, M. M., Pitt, W. C. and Zemlicka, D. E. ( 2004 a). Coyotes (Canis latrans) are definitive hosts of Neospora caninum. International Journal for Parasitology 34, 159161.Google Scholar
Gonzalez, L., Buxton, D., Atxaerandio, R., Aduriz, G., Maley, S., Marco, J. C and Cuervo, L. A. ( 1999). Bovine abortion associated with Neospora caninum in northern Spain. Veterinary Record 144, 145150.CrossRefGoogle Scholar
Gore, T. C., Long, P. L., Kogut, M. and Johnson, J. ( 1983). Attenuation of Eimeria necatrix and E. tenella of US origin by serial embryo passage. Avian Diseases 27, 569576.Google Scholar
Gottstein, B., Eperon, S., Dai, W. J., Cannas, A., Hemphill, A. and Greif, G. ( 2001). Efficacy of toltrazuril and ponazuril against experimental Neospora caninum infection in mice. Parasitology Research 87, 4348.CrossRefGoogle Scholar
Graat, E. A., Ploeger, H. W., Henken, A. M., De Vries - Reilingh, G., Noordhuizen, J. P. and Van Beek, P. N. ( 1996). Effects of initial litter contamination level with Eimeria acervulina on population dynamics and production characteristics in broilers. Veterinary Parasitology 65, 223232.CrossRefGoogle Scholar
Graham, D. A., Calvert, V., Whyte, M. and Marks, J. ( 1999). Absence of serological evidence for human Neospora caninum infection. Veterinary Record 144, 672673.CrossRefGoogle Scholar
Guy, C. S., Williams, D. J. L., Kelly, D. F., McGarry, J. W., Guy, F., Bjorkman, C., Smith, R. F. and Trees, A. J. ( 2001). Neospora caninum in persistently infected, pregnant cows: spontaneous transplacental infection is associated with an acute increase in maternal antibody. Veterinary Record 149, 443449.CrossRefGoogle Scholar
Hakim, F. T., Gazzinelli, R. T., Denkers, E., Hieny, S., Shearer, G. M. and Sher, A. ( 1991). CD8+ T-cells from mice vaccinated against Toxoplasma gondii are cytotoxic for parasite-infected or antigen pulsed host cells. Journal of Immunology 147, 23102316.Google Scholar
Hemphill, A. ( 1999). The host-parasite relationship in neosporosis. Advances in Parasitology 43, 47104.CrossRefGoogle Scholar
Hill, D. and Dubey, J. P. ( 2002). Toxoplasma gondii: transmission, diagnosis and prevention. Clinical Microbiology and Infection 8, 634640.CrossRefGoogle Scholar
Holland, G. N. ( 1999). Reconsidering the pathogenesis of ocular toxoplasmosis. American Journal of Ophthalmology 128, 502505.CrossRefGoogle Scholar
Honda, Y., Waithaka, M., Taracha, E. L., Duchateau, L., Musoke, A. J. and McKeever, D. J. ( 1998). Delivery of the Theileria parva p67 antigen to cattle using recombinant vaccinia virus: IL-2 enhances protection. Vaccine 16, 12761282.CrossRefGoogle Scholar
Horton-Smith, C., Long, P. L., Pierce, A. E. and Rose, M. E. ( 1963). Immunity to Coccidia in domestic animals. In Immunity to Protozoa ( ed. Garnham, P. C. C., Pierce, A. E. and Roitt, I.), pp. 273295. Blackwell Scientific Publications Ltd. Oxford UK.
Howe, D. K., Crawford, A. C., Lindsay, D. and Sibley, L. D. ( 1998). The p29 and p35 immunodominant antigens of Neospora caninum tachyzoites are homologous to the family of surface antigens of Toxoplasma gondii. Infection and Immunity 66, 53225328.Google Scholar
Huskinson-Mark, J., Araujo, F. G. and Remington, J. S. ( 1991). Evaluation of the effect of drugs on the cyst form of Toxoplasma gondii. Journal of Infectious Diseases 164, 170171.CrossRefGoogle Scholar
Innes, E. A. ( 1997). Toxoplasmosis: comparative species susceptibility and host immune response. Comparative Immunology Microbiology and Infectious Diseases 20, 131138.CrossRefGoogle Scholar
Innes, E. A., Andrianarivo, A. G., Bjorkman, C., Williams, D. J. L. and Conrad, P. A. ( 2002). Immune responses to Neospora caninum and prospects for vaccination. Trends in Parasitology 18, 497504.CrossRefGoogle Scholar
Innes, E. A., Bartley, P. M., Wright, S. E., Maley, S., MacAldowie, C. and Buxton, D. ( 2005 b). Foetal immune responses in cattle challenged with Neospora caninum at different stages of gestation. Proceedings of the 20th International Conference of the World Association for the Advancement of Veterinary Parasitology, Christchurch, New Zealand, 16–20th October. p. 215.
Innes, E. A., Panton, W. R., Marks, J., Trees, A. J., Holmdahl, J. and Buxton, D. ( 1995 c). Interferon gamma inhibits the intracellular multiplication of Neospora caninum, as shown by incorporation of 3H Uracil. Journal of Comparative Pathology 113, 95100.Google Scholar
Innes, E. A., Panton, W. R., Sanderson, A., Thomson, K. M., Wastling, J. M., Maley, S. and Buxton, D. ( 1995 b). Induction of CD4+ and CD8+ T cell responses in efferent lymph responding to Toxoplasma gondii infection: analysis of phenotype and function. Parasite Immunology 17, 151160.Google Scholar
Innes, E. A., Panton, W. R., Thomson, K. M., Maley, S., and Buxton, D. ( 1995 a). Kinetics of interferon gamma production in vivo during infection with the S48 vaccine strain of Toxoplasma gondii. Journal of Comparative Pathology 113, 8994.Google Scholar
Innes, E. A and Wastling, J. M. ( 1995). Analysis of in vivo immune responses during Toxoplasma gondii infection using the technique of lymphatic cannulation. Parasitology Today 11, 268271.CrossRefGoogle Scholar
Innes, E. A., Wright, S., Bartley, P., Maley, S., MacAldowie, C., Esteban-Redondo, I. and Buxton, D. ( 2005 a). The host-parasite relationship in bovine neosporosis. Veterinary Immunology and Immunopathology 108, 2936.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, 15231534.CrossRefGoogle Scholar
Jeffers, T. K. ( 1975). Attenuation of Eimeria tenella through selection for precociousness. Journal of Parasitology 61, 10831090.CrossRefGoogle Scholar
Jenkins, M. C. ( 1988). A cDNA encoding a merozoite surface protein of the protozoan Eimeria acervulina contains tandem-repeated sequences. Nucleic Acids Research 16, 9863.Google Scholar
Jenkins, M. C. ( 2001). Advances and prospects for subunit vaccines against protozoa of veterinary importance. Veterinary Parasitology 101, 291310.CrossRefGoogle Scholar
Jenkins, M. C., Augustine, P. C., Danforth, H. D. and Barta, J. R. ( 1991). X-irradiation of Eimeria tenella oocysts provides direct evidence that sporozoite invasion and early schizont development induce a protective immune response(s). Infection and Immunity 59, 40424048.Google Scholar
Jenkins, M. C., Chute, M. B. and Danforth, H. D. ( 1997). Protection against coccidiosis in outbred chickens elicited by gamma-irradiated Eimeria maxima. Avian Disease 41, 702708.CrossRefGoogle Scholar
Jenkins, M., Parker, C., Tuo, W., Vinyard, B. and Dubey, J. P. ( 2004). Inclusion of CpG adjuvant with plasmid DNA coding for NcGRA7 improves protection against congenital neosporosis. Infection and Immunity 72, 18171819.CrossRefGoogle Scholar
Johnson, A. M., McDonald, P. J. and Neoh, S. H. ( 1983). Monoclonal antibodies to Toxoplasma cell membrane surface antigens protect mice from toxoplasmosis. Journal of Protozoology 30, 351356.CrossRefGoogle Scholar
Kaiser, P., Hughes, S. and Bumstead, N. ( 1999). The chicken 9E3/CEF4 CXC chemokine is the avian orthologue of IL8 and maps to chicken chromosome 4 syntenic with genes flanking the mammalian chemokine cluster. Immunogenetics 49, 673684.CrossRefGoogle Scholar
Kalinski, P., Hilkens, C. M., Snijders, A., Snijdewint, F. G. and Kapsenberg, M. L. ( 1997). IL-12-deficient dendritic cells, generated in the presence of prostaglandin E2, promote type 2 cytokine production in maturing human naive T helper cells. Journal of Immunology 159, 2835.Google Scholar
Kang, H., Remington, J. S. and Suzuki, Y. ( 2000). Decreased resistance of B cell-deficient mice to infection with Toxoplasma gondii despite unimpaired expression of IFN-gamma, TNF-alpha, and inducible nitric oxide synthase. Journal of Immunology 164, 26292634.CrossRefGoogle Scholar
Karim, M. J., Begum, N. and Khan, M. S. R. ( 1994). Heterogeneity among strains of Eimeria tenella isolated from Bangladesh. Journal of Protozoology Research 4, 5661.Google Scholar
Kawazoe, U., Bordin, E. L., De Lima, C. A. and Dias, L. A. V. ( 2005). Characterisation and histopathological observations of a selected Brazilian precocious line of Eimeria acervulina. Veterinary Parasitology 131, 514.CrossRefGoogle Scholar
Khan, I. A., Ely, K. H. and Kasper, L. H. ( 1994). Antigen-specific CD8+ T cell clone protects against acute Toxoplasma gondii infection in mice. Journal of Immunology 152, 18561860.Google Scholar
Khan, I. A., Schwartzman, J. D., Fonseka, S. and Kasper, L. H. ( 1997). Neospora caninum: role for immune cytokines in host immunity. Experimental Parasitology 85, 2434.CrossRefGoogle Scholar
Khan, I. A., Smith, K. A. and Kasper, L. H. ( 1988). Induction of antigen-specific parasiticidal cytotoxic T cell splenocytes by a major membrane protein (P30) of Toxoplasma gondii. Journal of Immunology 141, 36003605.Google Scholar
Kim, K. S., Jenkins, M. C. and Lillehoj, H. S. ( 1989). Immunization of chickens with live Escherichia coli expressing Eimeria acervulina merozoite recombinant antigen induces partial protection against coccidiosis. Infection and Immunity 57, 24342440.Google Scholar
Klinman, D. M. ( 2003). CpG DNA as a vaccine adjuvant. Expert Review of Vaccines 2, 305315.CrossRefGoogle Scholar
Krahenbuhl, J. L., Gaines, J. D. and Remington, J. S. ( 1972). Lymphocyte transformation in human toxoplasmosis. Journal of Infectious Diseases 125, 283288.CrossRefGoogle Scholar
Kreuder, C., Miller, M. A., Jessup, D. A., Lowenstine, L. J., Harris, M. D., Ames, J. A., Carpenter, T. E., Conrad, P. A. and Mazet, J. A. ( 2003). Patterns of mortality in southern sea otters (Enhydra lutris nereis) from 1998–2001. Journal of Wildlife Diseases 39, 495509.CrossRefGoogle Scholar
Krieg, A. M. ( 1995). CpG DNA: a pathogenic factor in systemic lupus erythematosus? Journal of Clinical Immunology 15, 284292.Google Scholar
Kringel, H., Dubey, J. P., Beshah, E., Hecker, R. and Urban, J. F. Jr. ( 2004). CpG-oligodeoxynucleotides enhance porcine immunity to Toxoplasma gondii. Veterinary Parasitology 123, 5566.CrossRefGoogle Scholar
Krishnan, L., Guilbert, L. J., Russell, A. S., Wegmann, T. G., Mosmann, T. R. and Belosevic, M. ( 1996). Pregnancy impairs resistance of C57BL/6 mice to Leishmania major infection and causes decreased antigen-specific IFN-gamma response and increased production of T helper 2 cytokines. Journal of Immunology 156, 644652.Google Scholar
Kuiper, C. M., Roosmalen-Vos, S. V., Beek-Verhoeven, N. V. D., Schaap, T. C. and Vermeulen, A. N. ( 2001). Eimeria tenella anti-oxidant proteins: differentially expressed enzymes with immunogenic properties. Proceedings of the VIIIth International Coccidiosis Conference, Palm Cove, Australia. 102103.
Kyaw, T., Suwimonteerabutr, J., Virakul, P., Lohachit, C. and Kalpravidh, W. ( 2005). Seronegative conversion in four Neospora caninum-infected cows, with a low rate of transplacental transmission. Veterinary Parasitology 131, 145150.CrossRefGoogle Scholar
Li, G. Q., Kanu, S., Xiang, F. Y., Xiao, S. M., Zhang, L., Chen, H. W. and Ye, H. J. ( 2004). Isolation and selection of ionophore-tolerant Eimeria precocious lines: E. tenella, E. maxima and E. acervulina. Veterinary Parasitology 119, 261276.Google Scholar
Liddell, S., Jenkins, M. C., Collica, C. M. and Dubey, J. P. ( 1999). Prevention of vertical transfer of Neospora caninum in BALB/c mice by vaccination. Journal of Parasitology 85, 10721075.CrossRefGoogle Scholar
Liddell, S., Parker, C., Vinyard, B., Jenkins, M. and Dubey, J. P. ( 2003). Immunization of mice with plasmid DNA coding for NcGRA7 or NcsHSP33 confers partial protection against vertical transmission of Neospora caninum. Journal of Parasitology 89, 496500.CrossRefGoogle Scholar
Lillehoj, H. S. ( 1987). Effects of immunosuppression on avian coccidiosis: cyclosporin A but not hormonal bursectomy abrogates host protective immunity. Infection and Immunity 55, 16161621.Google Scholar
Lillehoj, H. S. ( 1994). Analysis of Eimeria acervulina-induced changes in the intestinal T lymphocyte subpopulations in two chicken strains showing different levels of susceptibility to coccidiosis. Research in Veterinary Science 56, 17.CrossRefGoogle Scholar
Lillehoj, H. S. ( 2005). Immune response to Coccidia. Proceedings of the IXth International Coccidiosis Conference, Foz do Iguassu, Brazil. September 19–23rd. pp. 6383.
Lillehoj, H. S. and Choi, K. D. ( 1998). Recombinant chicken interferon-gamma-mediated inhibition of Eimeria tenella development in vitro and reduction of oocyst production and body weight loss following Eimeria acervulina challenge infection. Avian Diseases 42, 307314.CrossRefGoogle Scholar
Lind, P. and Buxton, D. ( 2000). Veterinary aspects of Toxoplasma infection. In Congenital Toxoplasmosis ( ed. Ambroise-Thomas, P. and Petersen, E.), pp. 261269. Springer-Verlag France.CrossRef
Lindsay, D. S., Butler, J. M., Rippey, N. S. and Blagburn, B. L. ( 1996). Demonstration of synergistic effects of sulfonamides and dihydrofolate reductase/thymidylate synthase inhibitors against Neospora caninum tachyzoites in cultured cells, and characterization of mutants resistant to pyrimethamine. American Journal of Veterinary Research 57, 6872.Google Scholar
Lindsay, D. S., Lenz, S. D., Blagburn, B. L. and Brake, D. A. ( 1999). Characterization of temperature-sensitive strains of Neospora caninum in mice. Journal of Parasitology 85, 6467.CrossRefGoogle Scholar
Lingelbach, K. and Joiner, K. A. ( 1998). The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells. Journal of Cell Science 111, 14671475.Google Scholar
Long, P. L. and Horton-Smith, C. ( 1968). Coccidia and coccidiosis in the domestic fowl. Advances in Parasitology 6, 313325.CrossRefGoogle Scholar
Long, P. L. and Rose, M. E. ( 1965). Active and passive immunization of chickens against intravenously induced infections of Eimeria tenella. Experimental Parasitology 16, 17.CrossRefGoogle Scholar
Luft, B. J., Brooks, R. G., Conley, F. K., McCabe, R. E. and Remington, J. S. ( 1984). Toxoplasmic encephalitis in patients with acquired immune deficiency syndrome. Journal of the American Medical Association 252, 913917.CrossRefGoogle Scholar
Lunden, A., Wright, S., Allen, J. E. and Buxton, D. ( 2002). Immunisation of mice against neosporosis. International Journal for Parasitology 32, 867876.CrossRefGoogle 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, 142156.CrossRefGoogle Scholar
Maley, S., Buxton, D., MacAldowie, C., Anderson, I., Wright, S., Bartley, P., Esteban-Redondo, I., Hamilton, C., Storset, A. and Innes, E. ( 2005). Characterization of the immune response generated in the placenta of cattle experimentally infected with Neospora caninum in early gestation. Proceedings of the COST Action 854 Conference: Protozoal reproduction losses in farm ruminants, Warsaw, Poland, 2–4th September, S26.
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, 186195.CrossRefGoogle 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, 303309.CrossRefGoogle Scholar
Marsh, A. E., Barr, B. C., Packham, A. E. and Conrad, P. A. ( 1998). Description of a new Neospora species (Protozoa: Apicomplexa: Sarcocystidae). Journal of Parasitology 84, 983991.CrossRefGoogle Scholar
Mateus-Pinilla, N. E., Dubey, J. P., Choromanski, L. and Weigel, R. M. ( 1999). A field trial of the effectiveness of a feline Toxoplasma gondii vaccine in reducing T. gondii exposure for swine. Journal of Parasitology 85, 855860.Google Scholar
Mateus-Pinilla, N. E., Hannon, B. and Weigel, R. M. ( 2002). A computer simulation of the prevention of the transmission of Toxoplasma gondii on swine farms using a feline T. gondii vaccine. Preventative Veterinary Medicine 55, 1736.CrossRefGoogle Scholar
McAllister, M. M. ( 2005). A decade of discoveries in veterinary protozoology changes our concept of “subclinical” toxoplasmosis. Veterinary Parasitology 132, 241247.CrossRefGoogle 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, 881887.CrossRefGoogle Scholar
McAllister, M. M., Dubey, J. P., Lindsay, D. S., Jolley, W. R., Wills, R. A and McGuire, A. M. ( 1998). Dogs are definitive hosts of Neospora caninum. International Journal for Parasitology 28, 14731478.CrossRefGoogle Scholar
McClurkin, A. W., Littledike, E. T., Cutlip, R. C., Frank, G. H., Coria, M. F. and Bolin, S. R. ( 1984). Production of cattle immunotolerant to bovine viral diarrhea virus. Canadian Journal of Comparative Medicine 48, 156161.Google Scholar
Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., Shapiro, C., Griffin, P. M. and Tauxe, R. V. ( 1999). Food-related illness and death in the United States. Emerging Infectious Diseases 5, 607625.CrossRefGoogle Scholar
Mevelec, M. N., Bout, D., Benoit, D., Herve, M., Magne, R., Bruneel, O. and Buzoni-Gatel, D. ( 2005). Evaluation of protective effect of DNA vaccination with genes encoding antigens GRA4 and SAG1 associated with GM-CSF plasmid, against acute, chronical and congenital toxoplasmosis in mice. Vaccine 23, 44894499.CrossRefGoogle Scholar
Miller, C., Quinn, H., Ryce, C., Reichel, M. P. and Ellis, J. T. ( 2005). Reduction in transplacental transmission of Neospora caninum in outbred mice by vaccination. International Journal for Parasitology 35, 821828.CrossRefGoogle Scholar
Min, W., Lillehoj, H. S., Ashwell, C. M., Van Tassell, C. P., Dalloul, R. A., Matukumalli, L. K., Han, J. Y. and Lillehoj, E. P. ( 2005). Expressed sequence tag analysis of Eimeria-stimulated intestinal intraepithelial lymphocytes in chickens. Molecular Biotechnology 30, 143150.CrossRefGoogle Scholar
Min, W., Lillehoj, H. S., Burnside, J., Weining, K. C., Staeheli, P. and Zhu, J. J. ( 2001). Adjuvant effects of IL-1β, IL-2, IL-8, IL-15, IFN-α, IFN-γ TGF-β4 and lymphotactin on DNA vaccination against Eimeria acervulina. Vaccine 20 267274.CrossRefGoogle Scholar
Mineo, J. R., McLeod, R., Mack, D., Smith, J., Khan, I. A., Ely, K. H. and Kasper, L. H. ( 1993). Antibodies to Toxoplasma gondii major surface protein (SAG-1, P30) inhibit infection of host cells and are produced in murine intestine after peroral infection. Journal of Immunology 150, 39513964.Google Scholar
Mishima, M., Xuan, X., Yokoyama, N., Igarashi, I., Fujisaki, K., Nagasawa, H. and Mikami, T. ( 2002). Recombinant feline herpesvirus type 1 expressing Toxoplasma gondi ROP2 antigen inducible protective immunity in cats. Parasitology Research 88, 144149.CrossRefGoogle Scholar
Moen, A. R., Wouda, W., Mul, M. F., Graat, E. A. and Van Werven, T. ( 1998). Increased risk of abortion following Neospora caninum abortion outbreaks: a retrospective and prospective cohort study in four dairy herds. Theriogenology 49, 13011309.CrossRefGoogle Scholar
Montoya, J. G., Lowe, K. E., Clayberger, C., Moody, D., Do, D., Remington, J. S., Talib, S. and Subauste, C. S. ( 1996). Human CD4+ and CD8+T lymphocytes are both cytotoxic to Toxoplasma gondii-infected cells. Infection and Immunity 64, 176181.Google Scholar
Mutwiri, G., Pontarollo, R., Babiuk, S., Griebel, P., van Drunen Littel-van den Hurk, S., Mena, A., Tsang, C., Alcon, V., Nichani, A., Ioannou, X., Gomis, S., Townsend, H., Hecker, R., Potter, A. and Babiuk, L. A. ( 2003). Biological activity of immunostimulatory CpG DNA motifs in domestic animals. Veterinary Immunology and Immunopathology 91, 89103.CrossRefGoogle Scholar
Nishikawa, Y., Inoue, N., Xuan, X., Nagasawa, H., Igarashi, I., Fujisaki, K., Otsuka, H. and Mikami, T. ( 2001 a). Protective efficacy of vaccination by recombinant vaccinia virus against Neospora caninum infection. Vaccine 19, 13811390.Google Scholar
Nishikawa, Y., Xuan, X., Nagasawa, H., Igarashi, I., Fujisaki, K., Otsuka, H. and Mikami, T. ( 2001 b). Prevention of vertical transmission of Neospora caninum in BALB/c mice by recombinant vaccinia virus carrying NcSRS2 gene. Vaccine 19, 17101716.Google Scholar
O'Connell, E., Wilkins, M. F., and Te Punga, W. A. ( 1988). Toxoplasmosis in sheep. II. The ability of a live vaccine to prevent lamb losses after an intravenous challenge with Toxoplasma gondii. New Zealand Veterinary Journal 36, 14.Google Scholar
Okeoma, C. M., Williamson, N. B., Pomroy, W. E., Stowell, K. M. and Gillespie, L. ( 2004). The use of PCR to detect Neospora caninum DNA in the blood of naturally infected cows. Veterinary Parasitology 122, 307315.CrossRefGoogle Scholar
Oliveira-Ferreira, J., Miyahira, Y., Layton, G. T., Savage, N., Esteban, M., Rodriguez, D., Rodriguez, J. R., Nussenzweig, R. S. and Zavala, F. ( 2000). Immunogenicity of Ty-VLP bearing a CD8(+) T cell epitope of the CS protein of P. yoelii: enhanced memory response by boosting with recombinant vaccinia virus. Vaccine 18, 18631869.Google Scholar
Osburn, B. I., MacLachlan, N. J. and Terrell, T. G. ( 1982). Ontogeny of the immune system. Journal of the American Veterinary Medical Association 181 10491052.Google Scholar
Ovington, K. S., Alleva, L. M. and Kerr, E. A. ( 1995). Cytokines and immunological control of Eimeria spp. International Journal for Parasitology 25, 13311351.CrossRefGoogle Scholar
Pare, J., Thurmond, M. C. and Hietala, S. K. ( 1996). Congenital Neospora caninum infection in dairy cattle and associated calfhood mortality. Canadian Journal of Veterinary Research 60, 133139.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, 8287.CrossRefGoogle Scholar
Parker, S. J., Roberts, C. W. and Alexander, J. ( 1991). CD8+ T cells are the major lymphocyte subpopulation involved in the protective immune response to Toxoplasma gondii in mice. Clinical Experimental Immunology 84, 207212.Google Scholar
Parmley, S., Slifer, T. and Araujo, F. ( 2002). Protective effects of immunization with a recombinant cyst antigen in mouse models of infection with Toxoplasma gondii tissue cysts. Journal of Infectious Diseases 185, 9095.CrossRefGoogle Scholar
Parmley, S. F., Yang, S., Harth, G., Sibley, L. D., Sucharczuk, A. and Remington, J. S. ( 1994). Molecular characterisation of a 65-kilodalton Toxoplasma gondii antigen expressed abundantly in the matrix of tissue cysts. Molecular and Biochemical Parasitology 66, 283296.CrossRefGoogle Scholar
Pinitkiatisakul, S., Mattsson, J. G., Wikman, M., Friedman, M., Bengtsson, K. L., Stahl, S. and Lunden, A. ( 2005). Immunisation of mice against neosporosis with recombinant NcSRS2 iscoms. Veterinary Parasitology 129, 2534.CrossRefGoogle Scholar
Podzamczer, D., Miro, J. M., Bolao, F., Gatell, J. M., Cosin, J., Sirera, G., Domingo, P., Laguna, F., Santamaria, J. and Verdejo, J. ( 1995). Twice-weekly maintenance therapy with sulfadiazine-pyrimethamine to prevent recurrent toxoplasmic encephalitis in patients with AIDS. Spanish Toxoplasmosis Study Group. Annals of Internal Medicine 123, 175180.CrossRefGoogle Scholar
Pope, G. S., Gupta, S. K. and Munro, I. B. ( 1969). Progesterone levels in the systemic plasma of pregnant, cycling and ovariectomized cows. Journal of Reproduction and Fertility 20, 369381.CrossRefGoogle Scholar
Raghupathy, R. ( 1997). Th1-type immunity is incompatible with successful pregnancy. Immunology Today 18, 478482.CrossRefGoogle Scholar
Remington, J. S. and Desmonts, G. ( 1990). Toxoplasmosis. In Infectious Diseases of the Foetus and Newborn Infant, 3rd edition ( ed. Remington, J. S. and Klein, J. O.), pp. 89195. WB Saunders, Philadelphia.
Reyes-Sandoval, A. and Ertl, H. C. ( 2001). DNA vaccines. Current Molecular Medicine 1, 217243.CrossRefGoogle Scholar
Roberts, C. W., Brewer, J. M. and Alexander, J. ( 1994). Congenital toxoplasmosis in the Balb/c mouse: prevention of vertical disease transmission and fetal death by vaccination. Vaccine 12, 13891394.CrossRefGoogle Scholar
Roberts, F. and McLeod, R. ( 1999). Pathogenesis of Toxoplasmic retinochoroiditis. Parasitology Today 15, 5157.CrossRefGoogle Scholar
Roberts, S. J., Smith, A. L., West, A. B., Wen, L., Findly, R. C., Owen, M. J. and Hayday, A. C. ( 1996). T-cell alpha beta+ and gamma delta+ deficient mice display abnormal but distinct phenotypes toward a natural, widespread infection of the intestinal epithelium. Proceedings of the National Academy of Sciences, USA 93, 1177411779.CrossRefGoogle Scholar
Roque-Resendiz, J. L., Rosales, R. and Herion, P. ( 2004). MVA ROP2 vaccinia virus recombinant as a vaccine candidate for toxoplasmosis. Parasitology 128, 397405.CrossRefGoogle Scholar
Rose, M. E. ( 1982). Host immune responses. In The Biology of the Coccidia ( ed. Long, P. L.), pp. 329371. University Park Press, USA.
Rose, M. E. ( 1996). Immunity to Coccidia. In Poultry Immunology ( ed. Davison, T. F., Morris, T. R and Payne, L. N.), pp. 265299. Carfax Publishing Company, Oxfordshire, UK.
Rose, M. E. and Hesketh, P. ( 1982). Immunity to coccidia in chickens: adoptive transfer with peripheral blood lymphocytes and spleen cells. Parasite Immunology 4, 171185.CrossRefGoogle Scholar
Rose, M. E. and Long, P. L. ( 1970). Resistance to Eimeria infections in the chicken: the effects of thymectomy, bursectomy, whole body irradiation and cortisone treatment. Parasitology 60, 291299.CrossRefGoogle Scholar
Rose, M. E., Hesketh, P. and Wakelin, D. ( 1992). Immune control of murine coccidiosis: CD4+ and CD8+ T lymphocytes contribute differentially in resistance to primary and secondary infections. Parasitology 105, 349354.CrossRefGoogle Scholar
Rose, M. E., Wakelin, D., Joysey, H. S. and Hesketh, P. ( 1988). Immunity to coccidiosis: adoptive transfer in NIH mice challenged with Eimeria vermiformis. Parasite Immunology 10, 5969.CrossRefGoogle Scholar
Ryan, R., Shirley, M. and Tomley, F. ( 2000). Mapping and expression of microneme genes in Eimeria tenella. International Journal for Parasitology 30, 14931499.CrossRefGoogle Scholar
Sakai, T., Hisaeda, H., Nakano, Y., Zhang, M., Takashima, M., Ishii, K., Maekawa, Y., Matsumoto, S., Nitta, Y., Miyazaki, J., Yamamoto, S. and Himeno, K. ( 2003). Gene gun-based co-immunization of merozoite surface protein-1 cDNA with IL-12 expression plasmid confers protection against lethal Plasmodium yoelii in A/J mice. Vaccine 21, 14321444.CrossRefGoogle Scholar
Scharton-Kersten, T. M., Wynn, T. A., Denkers, E. Y., Bala, S., Grunvald, E., Hieny, S., Gazzinelli, R. T., and Sher, A. ( 1996). In the absence of endogenous IFN-gamma, mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. Journal of Immunology 157, 40454054.Google Scholar
Schetters, T., Dubey, J. P., Adrianarivo, A., Frankena, K., Romero, J. J., PÉRez, E., Heuer, C., Nicholson, C., Russell, D. and Weston, J. ( 2004). Intervet Symposium: Bovine Neosporosis. Veterinary Parasitology 125, 137146.Google Scholar
Schneider, J., Gilbert, S. C., Blanchard, T. J., Hanke, T., Robson, K. J., Hannan, C. M., Becker, M., Sinden, R., Smith, G. L. and Hill, A. V. ( 1998). Enhanced immunogenicity for CD8+ T cell induction and complete protective efficacy of malaria DNA vaccination by boosting with modified vaccinia virus Ankara. Nature Medicine 4, 397402.CrossRefGoogle Scholar
Shirley, M. W. ( 1992). Research on avian coccidia: an update. Brazilian Veterinary Journal 148, 479499.CrossRefGoogle Scholar
Shirley, M. W., Bushell, A. C., Bushell, J. E., McDonald, V. and Roberts, B. ( 1995). A live attenuated vaccine for the control of avian coccidiosis: trials in broiler breeders and replacement layer flocks in the United Kingdom. Veterinary Record 137, 453457.CrossRefGoogle Scholar
Shirley, M. W. and Long, P. L. ( 1990). Control of coccidiosis in chickens: immunisation with live vaccines. In Coccidiosis of Man and Domestic Animals ( ed. Long, P. L.), pp. 321341. CRC Press, Boca Raton, Florida.
Shirley, M. W., Smith, A. L. and Tomley, F. M. ( 2005). The biology of avian Eimeria with an emphasis on their control by vaccination. Advances in Parasitology 60, 285330.CrossRefGoogle Scholar
Smith, A. L., Hesketh, P., Archer, A. and Shirley, M. W. ( 2002). Antigenic diversity in Eimeria maxima and the influence of host genetics and immunization schedule on cross-protective immunity. Infection and Immunity 70, 24722479.CrossRefGoogle Scholar
Smith, D. D. and Frenkel, J. K. ( 2003). Immunological comparison of 124 isolates of Toxoplasma gondii. Parasitology Research 91, 332337.CrossRefGoogle Scholar
Song, K. D., Lillehoj, H. S., Choi, K. D., Yun, C. H., Parcells, M. S., Huynh, J. T. and Han, J. Y. ( 2000). A DNA vaccine encoding a conserved Eimeria protein induces protective immunity against live Eimeria acervulina challenge. Vaccine 19, 243252.CrossRefGoogle Scholar
Stanley, A. C., Buxton, D., Innes, E. A. and Huntley, J. F. ( 2004). Intranasal immunisation with Toxoplasma gondii tachyzoite antigen encapsulated into PLG microspheres induces humoral and cell-mediated immunity in sheep. Vaccine 22, 39293941.CrossRefGoogle Scholar
Staska, L. M., Davies, C. J., Brown, W. C., McGuire, T. C., Suarez, C. E., Park, J. Y., Mathison, B. A., Abbott, J. R. and Baszler, T. V. ( 2005). Identification of vaccine candidate peptides in the NcSRS2 surface protein of Neospora caninum by using CD4+ cytotoxic T lymphocytes and gamma interferon-secreting T lymphocytes of infected holstein cattle. Infection and Immunity 73, 13211329.CrossRefGoogle 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, 32723279.CrossRefGoogle 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, 227234.CrossRefGoogle Scholar
Subauste, C. S., Koniaris, A. H. and Remington, J. S. ( 1991). Murine CD8+ cytotoxic T lymphocytes lyse Toxoplasma gondii-infected cells. Journal of Immunology 147, 39553959.Google Scholar
Suzuki, Y. and Remington, J. S. ( 1988). Dual regulation of resistance against Toxoplasma gondii infection by Lyt-2+ and Lyt-1+, L3T4+ T cells in mice. Journal of Immunology 140, 39433946.Google Scholar
Suzuki, Y. and Remington, J. S. ( 1990). The effect of anti-IFN-gamma antibody on the protective effect of Lyt-2+ immune T cells against toxoplasmosis in mice. Journal of Immunology 144, 19541956.Google Scholar
Tanaka, T., Hamada, T., Inoue, N., Nagasawa, H., Fujisaki, K., Suzuki, N. and Mikami, T. ( 2000). The role of CD4(+) or CD8(+) T cells in the protective immune response of BALB/c mice to Neospora caninum infection. Veterinary Parasitology 90, 183191.CrossRefGoogle Scholar
Tangri, S. and Raghupathy, R. ( 1993). Expression of cytokines in placentas of mice undergoing immunologically mediated spontaneous fetal resorptions. Biology of Reproduction 49, 850856.CrossRefGoogle Scholar
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. ( 2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 12171258.CrossRefGoogle Scholar
Tenter, A. M. and Johnson, A. M. ( 1997). Phylogeny of the tissue cyst-forming coccidia. Advances in Parasitology 39, 69139.CrossRefGoogle Scholar
Thurmond, M. C. and Hietala, S. K. ( 1997 a). Effect of congenitally acquired Neospora caninum infection on risk of abortion and subsequent abortions in dairy cattle. American Journal of Veterinary Research 58, 13811385.Google Scholar
Thurmond, M. C. and Hietala, S. K. ( 1997 b). Effect of Neospora caninum infection on milk production in first-lactation dairy cows. Journal of the American Veterinary Medical Association 210, 672674.Google Scholar
Tomley, F. M., Bumstead, J. M., Billington, K. J. and Dunn, P. P. ( 1996). Molecular cloning and characterization of a novel acidic microneme protein (Etmic-2) from the apicomplexan protozoan parasite, Eimeria tenella. Molecular and Biochemical Parasitology 79, 195206.CrossRefGoogle 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, 11951200.CrossRefGoogle Scholar
Trout, J. M. and Lillehoj, H. S. ( 1996). T lymphocyte roles during Eimeria acervulina and Eimeria tenella infections. Veterinary Immunology and Immunopathology 53, 163172.CrossRefGoogle Scholar
Tuo, W., Fetterer, R. H., Davis, W. C., Jenkins, M. C. and Dubey, J. P. ( 2005). Neospora caninum antigens defined by antigen-dependent bovine CD4+ T cells. Journal of Parasitology 91, 564568.CrossRefGoogle Scholar
Uggla, A., Araujo, F. G., Lunden, A., Lovgren, K., Remington, J. S. and Morein, B. ( 1988). Immunizing effects in mice of two Toxoplasma gondii iscom preparations. Journal of Veterinary Medicine 35, 311314.CrossRefGoogle Scholar
Vercammen, M., Scorza, T., Huygen, K., De Braekeleer, J., Diet, R., Jacobs, D., Saman, E. and Verschueren, H. ( 2000). DNA vaccination with genes encoding Toxoplasma gondii antigens GRA1, GRA7, and ROP2 induces partially protective immunity against lethal challenge in mice. Infection and Immunity 68, 3845.CrossRefGoogle Scholar
Vermeulen, A. N. ( 1998). Progress in recombinant vaccine development against coccidiosis. A review and prospects into the next millennium. International Journal for Parasitology 28, 11211130.Google Scholar
Vermeulen, A. N. ( 2004). Avian coccidiosis: a disturbed host-parasite relationship to be restored. Symposia of the Society for Experimental Biology 55, 211241.Google Scholar
Vermeulen, A. N., Schaap, D. C. and Schetters, T. ( 2001). Control of coccidiosis in chickens by vaccination. Veterinary Parasitology 100, 1320.CrossRefGoogle Scholar
Vervelde, L., Vermeulen, A. N. and Jeurissen, S. H. ( 1996). In situ characterization of leucocyte subpopulations after infection with Eimeria tenella in chickens. Parasite Immunology 18, 247256.CrossRefGoogle Scholar
Wallach, M., Halabi, A., Pillemer, G., Sar-Shalom, O., Mencher, D., Gilad, M., Bendheim, U., Danforth, H. D. and Augustine, P. C. ( 1992). Maternal immunization with gametocyte antigens as a means of providing protective immunity against Eimeria maxima in chickens. Infection and Immunity 60, 20362039.Google Scholar
Wegmann, T. G., Lin, H., Guilbert, L. and Mosmann, T. R. ( 1993). Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunology Today 14, 353356.Google Scholar
Wilkins, M. F., O'Connell, E. and Te Punga, W. A. ( 1988). Toxoplasmosis in sheep III. Further evaluation of the ability of a live Toxoplasma gondii vaccine to prevent lamb losses and reduce congenital infection following experimental oral challenge. New Zealand Veterinary Journal 36, 8689.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, 347358.CrossRefGoogle Scholar
Williams, D. J. L., 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, 10591065.CrossRefGoogle Scholar
Williams, R. B. ( 2002). Fifty years of anticoccidial vaccines for poultry (1952–2002). Avian Diseases 46, 775802.CrossRefGoogle Scholar
Wouda, W., Moen, A. R. and Schukken, Y. H. ( 1998). Abortion risk in progeny of cows after a Neospora caninum epidemic. Theriogenology 49, 13111316.CrossRefGoogle Scholar
Wu, S. Q., Wang, M., Liu, Q., Zhu, Y. J., Suo, X. and Jiang, J. S. ( 2004). Construction of DNA vaccines and their induced protective immunity against experimental Eimeria tenella infection. Parasitology Research 94, 332336.CrossRefGoogle Scholar
Yamane, I., Kitani, H., Kokuho, T., Shibahara, T., Haritani, M., Hamaoka, T., Shimizu, S., Koiwai, M., Shimura, K. and Yokomizo, Y. ( 2000). The inhibitory effect of interferon gamma and tumor necrosis factor alpha on intracellular multiplication of Neospora caninum in primary bovine brain cells. Journal of Veterinary Medical Science 62, 347351.CrossRefGoogle Scholar
Zenner, L., Darcy, F., Cesbron-Delauw, M. F. and Capron, A. ( 1993). Rat model of congenital toxoplasmosis: rate of transmission of three Toxoplasma gondii strains to foetuses and protective effect of a chronic infection. Infection and Immunity 61, 360363.Google Scholar