Comparative host-parasite relationships in ovine toxoplasmosis and bovine neosporosis and strategies for vaccination

Vaccine

Volumn 25, Issue 30 SPEC. ISS., 2007, Pages 5495-5503

  Innes, Elisabeth A ^a   Bartley, Paul M ^a   Maley, Stephen W ^a   Wright, Stephen E ^a   Buxton, David ^a  

^a MOREDUN RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Immune response; Neospora caninum; Toxoplasma gondii; Vaccination

Indexed keywords

BOVILIS; NEOSPORA CANINUM VACCINE; OVILIS; PROTOZOAL VACCINE; TOXOPLASMA GONDII VACCINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CATTLE; CATTLE DISEASE; CONTROLLED STUDY; COW; HOST PARASITE INTERACTION; NEOSPORA CANINUM; NEOSPOROSIS; NONHUMAN; PARASITOSIS; PATHOGENESIS; PRIORITY JOURNAL; SHEEP; TOXOPLASMA GONDII; TOXOPLASMOSIS; VACCINATION;

EID: 34447098446     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2007.02.044     Document Type: Article

References (120)

1. Dubey J.P., and Beattie C.P. Toxoplasmosis of animals and man (1988), CRC Press, Boca Raton, FL
2. Innes E.A. Toxoplasmosis: comparative species susceptibility and host immune response. Comp Immunol Microbiol Infect Dis 20 2 (1997) 131-138
3. Dubey J.P., and Lindsay D.S. A review of Neospora caninum and neosporosis. Vet Parasitol 67 1-2 (1996) 1-59
4. Dubey J.P. Neosporosis in cattle. J Parasitol 89 (2003) S42-S56
5. Otter A., Wilson B.W., Scholes S.F., Jeffrey M., Helmick B., and Trees A.J. Results of a survey to determine whether Neospora is a significant cause of ovine abortion in England and Wales. Vet Rec 140 7 (1997) 175-177
6. Dubey J.P. A review of toxoplasmosis in cattle. Vet Parasitol 22 3-4 (1986) 177-202
7. Esteban-Redondo I., and Innes E.A. Toxoplasma gondii infection in sheep and cattle. Comp Immunol Microbiol Infect Dis 20 2 (1997) 191-196
8. Buxton D. Protozoan infections (Toxoplasma gondii, Neospora caninum and Sarcocystis spp.) in sheep and goats: recent advances. Vet Res 29 3-4 (1998) 289-310
9. Graham D.A., Calvert V., Whyte M., and Marks J. Absence of serological evidence for human Neospora caninum infection. Vet Rec 144 24 (1999) 672-673
10. Lind P., and Buxton D. Veterinary aspects of Toxoplasma infection. In: Ambroise-Thomas P., and Peterson E. (Eds). Congenital toxoplasmosis (2000), Springer-Verlag, France 261-269
11. Eurostat Statistics in Focus, 20/2005.
12. Blewett D.A., and Trees A.J. The epidemiology of ovine toxoplasmosis with especial respect to control. Br Vet J 143 2 (1987) 128-135
13. Bjerkas I., Mohn S.F., and Presthus J. Unidentified cyst-forming sporozoon causing encephalomyelitis and myositis in dogs. Z Parasitenkd 70 2 (1984) 271-274
14. Dubey J.P., Carpenter J.L., Speer C.A., Topper M.J., and Uggla A. Newly recognized fatal protozoan disease of dogs. J Am Vet Med Assoc 192 9 (1988) 1269-1285
15. Dubey J.P., Hattel A.L., Lindsay D.S., and Topper M.J. Neonatal Neospora caninum infection in dogs: isolation of the causative agent and experimental transmission. J Am Vet Med Assoc 193 10 (1988) 1259-1263
16. Buxton D., Caldow G.L., Maley S.W., Marks J., and Innes E.A. Neosporosis and bovine abortion in Scotland. Vet Rec 141 25 (1997) 649-651
17. Hemphill A., and Gottstein B. A European perspective on Neospora caninum. Int J Parasitol 30 8 (2000) 877-924
18. Bartels C.J., Arnaiz-Seco J.I., Ruiz-Santa-Quitera A., Bjorkman C., Frossling J., von Blumroder D., et al. Supranational comparison of Neospora caninum seroprevalences in cattle in Germany, The Netherlands, Spain and Sweden. Vet Parasitol 137 1-2 (2006) 17-27
19. Thurmond M.C., and Hietala S.K. Effect of congenitally acquired Neospora caninum infection on risk of abortion and subsequent abortions in dairy cattle. Am J Vet Res 58 12 (1997) 1381-1385
20. Moen A.R., Wouda W., Mul M.F., Graat E.A., and van Werven T. Increased risk of abortion following Neospora caninum abortion outbreaks: a retrospective and prospective cohort study in four dairy herds. Theriogenology 49 7 (1998) 1301-1309
21. Wouda W., Moen A.R., and Schukken Y.H. Abortion risk in progeny of cows after a Neospora caninum epidemic. Theriogenology 49 7 (1998) 1311-1316
22. Trees A.J., Davison H.C., Innes E.A., and Wastling J.M. Towards evaluating the economic impact of bovine neosporosis. Int J Parasitol 29 8 (1999) 1195-1200
23. Watson W.A., and Beverley J.K.A. Epizootics of toxoplasmosis causing ovine abortion. Vet Rec 88 (1971) 120-124
24. Hartley W.J., and Moyle G.G. Further observations on the epidemiology of ovine Toxoplasma infection. Aust J Exp Biol Med Sci 52 4 (1974) 647-653
25. Blewett D.A., Miller J.K., and Buxton D. Response of immune and susceptible ewes to infection with Toxoplasma gondii. Vet Rec 111 9 (1982) 175-178
26. Dubey J.P., Buxton D., and Wouda W. Pathogenesis of bovine neosporosis. J Comp Pathol 134 4 (2006) 267-289
27. Williams D.J., Guy C.S., McGarry J.W., Guy F., Tasker L., Smith R.F., et al. Neospora caninum-associated abortion in cattle: the time of experimentally-induced parasitaemia during gestation determines foetal survival. Parasitology 121 Pt 4 (2000) 347-358
28. Macaldowie C., Maley S.W., Wright S., Bartley P., Buxton D., and Innes E.A. Placental pathology associated with fetal death in cattle inoculated with Neospora caninum by two different routes in early pregnancy. J Comp Pathol 131 2-3 (2004) 142-156
29. Latham S. The epidemiology of Neospora caninum. PhD Thesis. University of Glasgow; 2003.
30. Barr B.C., Rowe J.D., Sverlow K.W., BonDurant R.H., Ardans A.A., Oliver M.N., et al. Experimental reproduction of bovine fetal Neospora infection and death with a bovine Neospora isolate. J Vet Diagn Invest 6 2 (1994) 207-215
31. Maley S.W., Buxton D., Rae A.G., Wright S.E., Schock A., Bartley P., et al. The pathogenesis of neosporosis in pregnant cattle: inoculation at mid-gestation. J Comp Pathol 129 2-3 (2003) 186-195
32. Innes E.A., Wright S., Bartley P., Maley S., Macaldowie C., and Buxton D. The host-parasite relationship in bovine neosporosis. Vet Immunol Immunopathol 108 1-2 (2005) 29-36
33. Wouda W., Bartels C.J., and Moen A.R. Characteristics of Neospora caninum-associated abortion storms in diary herds in The Netherlands (1995 to 1997). Theriogenology 52 2 (1999) 233-245
34. Schares G., Barwald A., Staubach C., Sondgen P., Rauser M., Schroder R., et al. p38-avidity-ELISA: examination of herds experiencing epidemic or endemic Neospora caninum-associated bovine abortion. Vet Parasitol 106 4 (2002) 293-305
35. Plant J.W., Richardson N., and Moyle G.G. Toxoplasma infection and abortion in sheep associated with feeding of grain contaminated with cat faeces. Aust Vet J 50 (1974) 19-21
36. Faull W.B., Clarkson M.J., and Winter A.C. Toxoplasmosis in a flock of sheep: some investigations into its source and control. Vet Rec 119 (1986) 491-493
37. Skjerve E., Waldeland H., Nesbakken T., and Kapperud G. Risk factors for the presence of antibodies to Toxoplasma gondii in Norwegian slaughter lambs. Prev Vet Med 35 3 (1998) 219-227
38. Waldeland H. Toxoplasmosis in sheep. Influence of various factors on the antibody contents. Acta Vet Scand 18 2 (1977) 237-247
39. Lunden A., Nasholm A., and Uggla A. Long-term study of Toxoplasma gondii infection in a Swedish sheep flock. Acta Vet Scand 35 3 (1994) 273-281
40. Owen MR. Molecular approaches to the epidemiology and diagnosis of ovine toxoplasmosis. PhD Thesis. University of Liverpool; 1996.
41. Duncanson P., Terry R.S., Smith J.E., and Hide G. High levels of congenital transmission of Toxoplasma gondii in a commercial sheep flock. Int J Parasitol 31 14 (2001) 1699-1703
42. Morley E.K., Williams R.H., Hughes J.M., Terry R.S., Duncanson P., and Hide G. Significant familial differences in the frequency of abortion and Toxoplasma gondii infection within a flock of Charollais sheep. Parasitology 131 Pt 2 (2005) 181-185
43. Rodger S.M., Maley S.W., Wright S.E., Mackellar A., Wesley F., Sales J., et al. Ovine toxoplasmosis; the role of endogenous transmission. Vet Rec 159 (2006) 768-772
44. Pare J., Thurmond M.C., and Hietala S.K. Congenital Neospora caninum infection in dairy cattle and associated calfhood mortality. Can J Vet Res 60 2 (1996) 133-139
45. Davison H.C., Otter A., and Trees A.J. Estimation of vertical and horizontal transmission parameters of Neospora caninum infections in dairy cattle. Int J Parasitol 29 10 (1999) 1683-1689
46. Bjorkman C., Johansson O., Stenlund S., Holmdahl O.J., and Uggla A. Neospora species infection in a herd of dairy cattle. J Am Vet Med Assoc 208 9 (1996) 1441-1444
47. Fioretti D.P., Pasquai P., Diaferia M., Mangili V., and Rosignoli L. Neospora caninum infection and congenital transmission: serological and parasitological study of cows up to the fourth gestation. J Vet Med 50 (2003) 399-404
48. Trees A.J., and Williams D.J. Endogenous and exogenous transplacental infection in Neospora caninum and Toxoplasma gondii. Trends Parasitol 21 12 (2005) 558-561
49. Dubey J.P., and Sharma S.P. Parasitaemia and tissue infection in sheep fed Toxoplasma gondii oocysts. J Parasitol 66 1 (1980) 111-114
50. Reid H.W., Buxton D., Gardiner A.C., Pow I., Finlayson J., and MacLean M.J. Immunosuppression in toxoplasmosis: studies in lambs and sheep infected with louping-ill virus. J Comp Pathol 92 2 (1982) 181-190
51. Wastling J.M., Nicoll S., and Buxton D. Comparison of two gene amplification methods for the detection of Toxoplasma gondii in experimentally infected sheep. J Med Microbiol 38 5 (1993) 360-365
52. Innes E.A., Panton W.R., Thomson K.M., Maley S., and Buxton D. Kinetics of interferon gamma production in vivo during infection with the S48 vaccine strain of Toxoplasma gondii. J Comp Pathol 113 1 (1995) 89-94
53. Oura C.A., Innes E.A., Wastling J.M., Entrican G., and Panton W.R. The inhibitory effect of ovine recombinant interferon-gamma on intracellular replication of Toxoplasma gondii. Parasite Immunol 15 9 (1993) 535-538
54. Gazzinelli R.T., Hieny S., Wynn T.A., Wolf S., and Sher A. 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. Proc Natl Acad Sci USA 90 13 (1993) 6115-6119
55. Gazzinelli R.T., Amichay D., Sharton-Kersten T., Grunwald E., Farber J.M., and Sher A. Role of macrophage-derived cytokines in the induction and regulation of cell-mediated immunity to Toxoplasma gondii. In: Gross U. (Ed). Toxoplasma gondii (1996), Springer-Verlag, Heidelberg 127-139
56. Yarovinsky F., and Sher A. Toll-like receptor recognition of Toxoplasma gondii. Int J Parasitol 36 3 (2006) 255-259
57. Buxton D., Thomson K.M., Maley S., Wastling J.M., Innes E.A., Panton W.R.M., et al. Primary and secondary responses of the ovine lymph node to Toxoplasma gondii: cell output in efferent lymph and parasite detection. J Comp Pathol 111 3 (1994) 231-241
58. Innes E.A., Panton W.R., Sanderson A., Thomson K.M., Wastling J.M., Maley S.W., et al. Induction of CD4+ and CD8+ T cell responses in efferent lymph responding to Toxoplasma gondii infection: analysis of phenotype and function. Parasite Immunol 17 3 (1995) 151-160
59. Suzuki Y., and Remington J.S. Dual regulation of resistance against Toxoplasma gondii infection by Lyt-2+ and Lyt-1+, L3T4+ T cells in mice. J Immunol 140 11 (1988) 3943-3946
60. Suzuki Y., and Remington J.S. The effect of anti-IFN-gamma antibody on the protective effect of Lyt-2+ immune T cells against toxoplasmosis in mice. J Immunol 144 5 (1990) 1954-1956
61. Gazzinelli R.T., Hakim F.T., Hieny S., Shearer G.M., and Sher A. Synergistic role of CD4+ and CD8+ T lymphocytes in IFN-gamma production and protective immunity induced by an attenuated Toxoplasma gondii vaccine. J Immunol 146 1 (1991) 286-292
62. Parker S.J., Roberts C.W., and Alexander J. CD8+ T cells are the major lymphocyte subpopulation involved in the protective immune response to Toxoplasma gondii in mice. Clin Exp Immunol 84 2 (1991) 207-212
63. Hakim F.T., Gazzinelli R.T., Denkers E., Hieny S., Shearer G.M., and Sher A. CD8+ T cells from mice vaccinated against Toxoplasma gondii are cytotoxic for parasite-infected or antigen-pulsed host cells. J Immunol 147 7 (1991) 2310-2316
64. Subauste C.S., Koniaris A.H., and Remington J.S. Murine CD8+ cytotoxic T lymphocytes lyse Toxoplasma gondii-infected cells. J Immunol 147 11 (1991) 3955-3959
65. Curiel T.J., Krug E.C., Purner M.B., Poignard P., and Berens R.L. Cloned human CD4+ cytotoxic T lymphocytes specific for Toxoplasma gondii lyse tachyzoite-infected target cells. J Immunol 151 4 (1993) 2024-2031
66. Khan I.A., Ely K.H., and Kasper L.H. Antigen-specific CD8+ T cell clone protects against acute Toxoplasma gondii infection in mice. J Immunol 152 4 (1994) 1856-1860
67. Scharton-Kersten T.M., Wynn T.A., Denkers E.Y., Bala S., Grunvald E., Hieny S., et al. In the absence of endogenous IFN-gamma, mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. J Immunol 157 9 (1996) 4045-4054
68. Buzoni-Gatel D., Lepage A.C., Mier-Poisson I.H., Bout D.T., and Kasper L.H. Adoptive transfer of gut intraepithelial lymphocytes protects against murine infection with Toxoplasma gondii. J Immunol 158 12 (1997) 5883-5889
69. Frenkel J.K. Biology of Toxoplasma gondii. In: Ambroise-Thomas P., and Peterson E. (Eds). Congenital toxoplasmosis (2000), Springer-Verlag, France 9-25
70. Buxton D., and Innes E.A. A commercial vaccine for ovine toxoplasmosis. Parasitology 110 Suppl (1995) S11-S16
71. Krahenbuhl J.L., Gaines J.D., and Remington J.S. Lymphocyte transformation in human toxoplasmosis. J Infect Dis 125 3 (1972) 283-288
72. Johnson A.M., McDonald P.J., and Neoh S.H. Monoclonal antibodies to Toxoplasma cell membrane surface antigens protect mice from toxoplasmosis. J Protozool 30 2 (1983) 351-356
73. Innes E.A., and Wastling J.M. Analysis of in vivo immune responses during Toxoplasma gondii infection using the technique of lymphatic cannulation. Parasitol Today 11 7 (1995) 268-271
74. Kang H., Remington J.S., and Suzuki Y. 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. J Immunol 164 5 (2000) 2629-2634
75. Buxton D., and Finlayson J. Experimental infection of pregnant sheep with Toxoplasma gondii: pathological and immunological observations on the placenta and foetus. J Comp Pathol 96 3 (1986) 319-333
76. Entrican G., and Wheelhouse N.M. Immunity in the female sheep reproductive tract. Vet Res 37 3 (2006) 295-309
77. Buxton D., Maley S.W., Thomson K.M., Trees A.J., and Innes E.A. Experimental infection of non-pregnant and pregnant sheep with Neospora caninum. J Comp Pathol 117 1 (1997) 1-16
78. Buxton D., Maley S.W., Wright S., Thomson K.M., Rae A.G., and Innes E.A. The pathogenesis of experimental neosporosis in pregnant sheep. J Comp Pathol 118 4 (1998) 267-279
79. Okeoma C.M., Williamson N.B., Pomroy W.E., Stowell K.M., and Gillespie L. The use of PCR to detect Neospora caninum DNA in the blood of naturally infected cows. Vet Parasitol 122 4 (2004) 307-315
80. Pare J., Thurmond M.C., and Hietala S.K. Neospora caninum antibodies in cows during pregnancy as a predictor of congenital infection and abortion. J Parasitol 83 1 (1997) 82-87
81. Stenlund S., Kindahl H., Magnusson U., Uggla A., and Bjorkman C. Serum antibody profile and reproductive performance during two consecutive pregnancies of cows naturally infected with Neospora caninum. Vet Parasitol 85 4 (1999) 227-234
82. Guy C.S., Williams D.J.L., Kelly D.F., McGarry J.W., Guy F., Bjorkman C., et al. Neospora caninum in persistently infected, pregnant cows: spontaneous transplacental infection is associated with an acute increase in maternal antibody. Vet Rec 149 15 (2001) 443-449
83. Innes E.A., Panton W.R., Marks J., Trees A.J., Holmdahl J., and Buxton D. Interferon gamma inhibits the intracellular multiplication of Neospora caninum, as shown by incorporation of 3H uracil. J Comp Pathol 113 1 (1995) 95-100
84. Khan I.A., Schwartzman J.D., Fonseka S., and Kasper L.H. Neospora caninum: role for immune cytokines in host immunity. Exp Parasitol 85 1 (1997) 24-34
85. Baszler T.V., Long M.T., McElwain T.F., and Mathison B.A. Interferon-gamma and interleukin-12 mediate protection to acute Neospora caninum infection in BALB/c mice. Int J Parasitol 29 10 (1999) 1635-1646
86. Staska L.M., McGuire T.C., Davies C.J., Lewin H.A., and Baszler T.V. Neospora caninum-infected cattle develop parasite-specific CD4+ cytotoxic T lymphocytes. Infect Immun 71 6 (2003) 3272-3279
87. Staska L.M., Davies C.J., Brown W.C., McGuire T.C., Suarez C.E., Park J.Y., et al. 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. Infect Immun 73 3 (2005) 1321-1329
88. Boysen P., Klevar S., Olsen I., and Storset A.K. The protozoan Neospora caninum directly triggers bovine NK cells to produce gamma interferon and to kill infected fibroblasts. Infect Immun 74 2 (2006) 953-960
89. Entrican G. Immune regulation during pregnancy and host-pathogen interactions in infectious abortion. J Comp Pathol 126 2-3 (2002) 79-94
90. Innes E.A., Andrianarivo A.G., Bjorkman C., Williams D.J., and Conrad P.A. Immune responses to Neospora caninum and prospects for vaccination. Trends Parasitol 18 11 (2002) 497-504
91. Innes E.A., Wright S.E., Maley S., Rae A., Schock A., Kirvar E., et al. Protection against vertical transmission in bovine neosporosis. Int J Parasitol 31 13 (2001) 1523-1534
92. Hemphill A., Vonlaufen N., and Naguleswaran A. Cellular and immunological basis of the host-parasite relationship during infection with Neospora caninum. Parasitology 133 (2006) 261-278
93. Maley S.W., Buxton D., Macaldowie C.N., Anderson I.E., Wright S.E., Bartley P.M., et al. Characterisation of the immune response generated in the placenta of cattle experimentally-infected with Neospora caninum in early gestation. J Comp Pathol 135 (2006) 130-141
94. Osburn B.I., MacLachlan N.J., and Terrell T.G. Ontogeny of the immune system. J Am Vet Med Assoc 181 10 (1982) 1049-1052
95. Andrianarivo A.G., Barr B.C., Anderson M.L., et al. Immune responses in pregnant cattle and bovine fetuses following experimental infection with Neospora caninum. Parasitol Res 87 10 (2001) 817-825
96. Almeria S., De M.T., Dawson H., Araujo R., Dubey J.P., and Gasbarre L.C. Cytokine gene expression in dams and foetuses after experimental Neospora caninum infection of heifers at 110 days of gestation. Parasite Immunol 25 7 (2003) 383-392
97. Bartley P.M., Kirvar E., Wright S., Swales C., Esteban-Redondo I., Buxton D., et al. Maternal and fetal immune responses of cattle inoculated with Neospora caninum at mid-gestation. J Comp Pathol 130 2-3 (2004) 81-91
98. Smith D.D., and Frenkel J.K. Immunological comparison of 124 isolates of Toxoplasma gondii. Parasitol Res 91 4 (2003) 332-337
99. Buxton D. Toxoplasmosis: the first commercial vaccine. Parasitol Today 9 9 (1993) 335-337
100. Dubey J.P., Urban Jr. J.F., and Davis S.W. Protective immunity to toxoplasmosis in pigs vaccinated with a nonpersistent strain of Toxoplasma gondii. Am J Vet Res 52 8 (1991) 1316-1319
101. Kringel H., Dubey J.P., Beshah E., Hecker R., and Urban Jr. J.F. CpG-oligodeoxynucleotides enhance porcine immunity to Toxoplasma gondii. Vet Parasitol 123 1-2 (2004) 55-66
102. Frenkel J.K., Pfefferkorn E.R., Smith D.D., and Fishback J.L. Prospective vaccine prepared from a new mutant of Toxoplasma gondii for use in cats. Am J Vet Res 52 5 (1991) 759-763
103. Mateus-Pinilla N.E., Dubey J.P., Choromanski L., and Weigel R.M. A field trial of the effectiveness of a feline Toxoplasma gondii vaccine in reducing T. gondii exposure for swine. J Parasitol 85 5 (1999) 855-860
104. O'Connell E., Wilkins M.F., and Te Punga W.A. Toxoplasmosis in sheep. II. The ability of a live vaccine to prevent lamb losses after an intravenous challenge with Toxoplasma gondii. N Z Vet J 36 1 (1988) 1-4
105. Wilkins M.F., O'Connell E., and Te Punga W.A. 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. N Z Vet J 36 2 (1988) 86-89
106. Buxton D., Thomson K.M., Maley S., Wright S., and Bos H.J. Experimental challenge of sheep 18 months after vaccination with a live (S48) Toxoplasma gondii vaccine. Vet Rec 133 13 (1993) 310-312
107. Neilsen H.V., Innes E.A., Peterson E., and Buxton D. Strategies for development of vaccines against Toxoplasma gondii. In: Ambroise-Thomas P., and Peterson E. (Eds). Congenital toxoplasmosis (2000), Springer-Verlag, France 313-322
108. Jenkins M. Advances and prospects for subunit vaccines against protozoa of veterinary importance. Vet Parasitol 101 3-4 (2001) 291-310
109. Anderson M.L., Palmer C.W., Thurmond M.C., Picanso J.P., Blanchard P.C., Breitmeyer R.E., et al. Evaluation of abortions in cattle attributable to neosporosis in selected dairy herds in California. J Am Vet Med Assoc 207 9 (1995) 1206-1210
110. McAllister M.M., Bjorkman C., Anderson-Sprecher R., and Rogers D.G. Evidence of point-source exposure to Neospora caninum and protective immunity in a herd of beef cows. J Am Vet Med Assoc 217 6 (2000) 881-887
111. Williams D.J., Guy C.S., Smith R.F., Guy F., McGarry J.W., McKay J., et al. First demonstration of protective immunity against foetopathy in cattle with latent Neospora caninum infection. Int J Parasitol 33 10 (2003) 1059-1065
112. Lindsay D.S., Lenz S.D., Blagburn B.L., and Brake D.A. Characterization of temperature-sensitive strains of Neospora caninum in mice. J Parasitol 85 1 (1999) 64-67
113. Ramamoorthy S., Lindsay D.S., Schurig G.G., Boyle S.M., Duncan R.B., Vemulapalli R., et al. Vaccination with gamma-irradiated Neospora caninum tachyzoites protects mice against acute challenge with N. caninum. J Eukaryot Microbiol 53 2 (2006) 151-156
114. Bartley P.M., Wright S., Sales J., Chianini F., Buxton D., and Innes E.A. Long-term passage of tachyzoites in tissue culture can attenuate virulence of Neospora caninum in vivo. Parasitology 133 Pt 4 (2006) 421-432
115. Hemphill A. The host-parasite relationship in neosporosis. Adv Parasitol 43 (1999) 47-104
116. Nishikawa Y., Inoue N., Xuan X., Nagasawa H., Igarashi I., Fujisaki K., et al. Protective efficacy of vaccination by recombinant vaccinia virus against Neospora caninum infection. Vaccine 19 11-12 (2001) 1381-1390
117. Nishikawa Y., Xuan X., Nagasawa H., Igarashi I., Fujisaki K., Otsuka H., et al. Prevention of vertical transmission of Neospora caninum in BALB/c mice by recombinant vaccinia virus carrying NcSRS2 gene. Vaccine 19 13-14 (2001) 1710-1716
118. Liddell S., Parker C., Vinyard B., Jenkins M., and Dubey J.P. Immunization of mice with plasmid DNA coding for NcGRA7 or NcsHSP33 confers partial protection against vertical transmission of Neospora caninum. J Parasitol 89 3 (2003) 496-500
119. Cannas A., Naguleswaran A., Muller N., Eperon S., Gottstein B., and Hemphill A. Vaccination of mice against experimental Neospora caninum infection using NcSAG1 and NcSRS2 based recombinant antigens and DNA vaccines. Parasitology 126 Pt 4 (2003) 303-312
120. Schetters T., Dubey J.P., Adrianarivo A., Frankena K., Romero J.J., Perez E., et al. Intervet symposium: bovine neosporosis. Vet Parasitol 125 (2004) 137-146