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The host-parasite relationship in pregnant cattle infected with Neospora caninum

Published online by Cambridge University Press:  25 October 2007

ELISABETH A. INNES
ELISABETH A. INNES*
Affiliation:
Moredun Research Institute, Pentlands Science Park, Edinburgh, EH26 OPZ, UK
*
Corresponding author: [email protected]
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Summary

The protozoan parasite Neospora caninum is an important cause of reproductive disease in cattle worldwide. The dog is a definitive host for the parasite and the oocyst stage, shed in the faeces, is a source of infection for cattle through consumption of contaminated feed or water. In addition, transplacental transmission of N. caninum is a very efficient means of the parasite infecting a new host and this can occur in successive pregnancies and over several generations. Neospora parasites may cause disease during pregnancy resulting in death of the foetus or birth of live congenitally infected calves that may show some neurological clinical signs at birth. The stage of pregnancy at which infection/parasitaemia occurs is an important factor in determining disease severity. Neospora infection in the first trimester of pregnancy may have more severe consequences for the foetus compared with infection occurring in the final trimester. The host-parasite relationship during pregnancy is a fascinating interaction and research in this area will improve understanding of disease pathogenesis and the various consequences of the host immune response, being host-protective, parasite protective and contributing to disease pathology. Pregnancy poses an interesting problem for the immune system of the dam as she is essentially carrying a semi-allogeneic tissue graft (the foetus) without immunological rejection taking place. To facilitate the pregnancy the cytokine environment in the placenta favours the regulatory Th-2-type cytokines, whose role is to counteract the pro-inflammatory Th1-type immune responses. Protective immunity to N. caninum, similar to many other intracellular parasites, involves Th1-type immune responses, which may pose problems for the dam trying to control a Neospora infection during pregnancy.

This paper will discuss the host-parasite relationship at different stages of gestation in pregnant cattle and review the implications of this research for our understanding of disease pathogenesis, parasite transmission and host protection.

Keywords

Neospora caninumcattlepregnancyimmune response
Type
Research Article
Information
Parasitology , Volume 134 , Special Issue 13: PARASITES IN PREGNANCY , December 2007 , pp. 1903 - 1910
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

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.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, 24–31.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
Barber, J. S. and Trees, A. J. (1996). Clinical aspects of twenty-seven cases of neosporosis in dogs. Veterinary Record 139, 439–443.CrossRefGoogle ScholarPubMed
Barr, B. C., Rowe, J. D., Sverlow, K. W., Bon Durant, 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 a). Supranational comparison of Neospora caninum seroprevalences in cattle in Germany, The Netherlands, Spain and Sweden. Veterinary Parasitology 137, 17–27.CrossRefGoogle ScholarPubMed
Bartels, C. J., van Schaik, G., Veldhuisen, J. P., van den Borne, B. H., Wouda, W. and Dijkstra, T. (2006 b). Effect of Neospora caninum-serostatus on culling, reproductive performance and milk production in Dutch dairy herds with and without a history of Neospora caninum-associated abortion epidemics. Preventative Veterinary Medicine 77, 186–198.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.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.CrossRefGoogle ScholarPubMed
Bjerkas, I., Mohn, S. F. and Presthus, J. (1984). Unidentified cyst-forming sporozoon causing encephalomyelitis and myositis in dogs. Zeitschrift für Parasitenkunde 70, 271–274.Google 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, 1441–1444.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.CrossRefGoogle ScholarPubMed
Brown, W. C., Rice-Ficht, A. C. and Estes, D. M. (1998). Bovine type 1 and type 2 responses. Veterinary Immunology and Immunopathology 63, 45–55.Google Scholar
Brownlie, J. and Clarke, M. C. (1993). Experimental and spontaneous mucosal disease of cattle: a validation of Koch's postulates in the definition of pathogenesis. Intervirology 35, 51–59.CrossRefGoogle ScholarPubMed
Buxton, D. (1990). Toxoplasmosis. Practitioner 234, 42–44.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.Google Scholar
Collantes-Fernandez, E., Arnaiz-Seco, I., Burgos, B. M., Rodriguez-Bertos, A., Aduriz, G., Fernandez-Garcia, A. and Ortega-Mora, L. M. (2006). Comparison of Neospora caninum distribution, parasite loads and lesions between epidemic and endemic bovine abortion cases. Veterinary Parasitology 142, 187–191.Google 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, 1683–1689.CrossRefGoogle Scholar
DeMarez, 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.CrossRefGoogle Scholar
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, 747–752.Google Scholar
Dubey, J. P. (2003). Review of Neospora caninum and neosporosis in animals. The Korean Journal of Parasitology 41, 1–16.Google Scholar
Dubey, J. P., Buxton, D. and Wouda, W. (2006). Pathogenesis of bovine neosporosis. Journal of Comparative Pathology 134, 267–289.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 Scholar
Dubey, J. P., Leathers, C. W. and Lindsay, D. S. (1989). Neospora caninum-like protozoon associated with fatal myelitis in newborn calves. Journal of Parasitology 75, 146–148.Google Scholar
Dubey, J. P. and Lindsay, D. S. (1996). A review of Neospora caninum and neosporosis. Veterinary Parasitology 67, 1–59.Google Scholar
Entrican, G. (2002). Immune regulation during pregnancy and host-pathogen interactions in infectious abortion. Journal of Comparative Pathology 126, 79–94.Google 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, 225–236.Google Scholar
Gazzinelli, R. T., Amichay, D., Sharton-Kersten, T., Grunwald, E., Farber, J. M. and Sher, A. (1996). Role of macrophage-derived cytokines in the induction and regulation of cell-mediated immunity to Toxoplasma gondii. In Toxoplasma gondii (Gross, U editor). Heidelberg: Springer-verlag; 1996. pp. 127–139.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.Google Scholar
Gondim, L. F. P., McAllister, M. M., Pitt, W. C. and Zemlicka, D. E. (2004). Coyotes (Canis latrans) are definitive hosts of Neospora caninum. International Journal for Parasitology 34, 159–161.CrossRefGoogle ScholarPubMed
Graham, D. A., Calvert, V., Whyte, M. and Marks, J. (1999). Absence of serological evidence for human Neospora caninum infection. Veterinary Record 144, 672–673.Google 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, 443–449.Google Scholar
Haldorson, G. J., Stanton, J. B., Mathison, B. A., Suarez, C. E and Baszler, T. V. (2006). Neospora caninum: Antibodies directed against tachyzoite surface protein NcSRS2 inhibit parasite attachment and invasion of placental trophoblasts in vitro. Experimental Parasitology 112, 172–178.CrossRefGoogle ScholarPubMed
Hemphill, A., Vonlaufen, N. and Naguleswaran, A. (2006). Cellular and immunological basis of the host-parasite relationship during infection with Neospora caninum. Parasitology 133, 261–278.Google 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, 497–504.Google Scholar
Innes, E. A., Buxton, D., Eperon, S. and Gottstein, B. (2000). Immunology of Neospora caninum infection in cattle and mice. International Journal for Parasitology 30, 896–900.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., Bartley, P., Maley, S., Macaldowie, C., Esteban-Redondo, I. and Buxton, D. (2005). The host-parasite relationship in bovine neosporosis. Veterinary Immunology and Immunopathology 108, 29–36.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
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, 644–652.Google Scholar
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, 145–150.Google Scholar
Latham, S. (2003). The epidemiology of Neospora caninum. PhD Thesis. University of Glasgow.Google 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, 913–917.Google Scholar
Lunden, A., Marks, J., Maley, S. 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.Google Scholar
Machado, R. Z., Mineo, T. W., Landim, L. P., Carvalho, A. F., Gennari, S. M. and Miglino, M. A. (2007). Possible role of bovine trophoblast giant cells in transplacental transmission of Neospora caninum in cattle. Revista Brasileira de Parasitologia Veterinaria 16, 21–25.Google Scholar
Maley, S., Buxton, D., Macaldowie, C., Anderson, I., Wright, S., Bartley, P., Esteban-Redondo, I., Hamilton, C., Storset, A. and Innes, E. (2006). Characterization of the immune response generated in the placenta of cattle experimentally infected with Neospora caninum in early gestation. Journal of Comparative Pathology 135, 130–141.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
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., 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
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, 1473–1478.Google 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, 1301–1309.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, 307–315.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, 1049–1052.Google 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, 133–139.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
Peterson, E., Lebech, M., Jensen, L., Lind, P., Rask, M., Bagger, P., Bjorkman, C. and Uggla, A. (1999). Neospora caninum infection and repeated abortions in humans. Emerging Infectious Diseases 5, 278–280.Google Scholar
Rosbottom, A., Guy, C. S., Gibney, E. H., smith, R. F., Valarcher, J. F., Taylor, G. and Williams, D. (2007). Peripheral immune responses in pregnant cattle following Neospora caninum infection. Parasite Immunology 29, 219–228.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, 137–146.Google 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, 1321–1329.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
Tangri, S. and Raghupathy, R. (1993). Expression of cytokines in placentas of mice undergoing immunologically mediated spontaneous fetal resorptions. Biology of Reproduction 49, 850–856.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., 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.Google Scholar
Trees, A. J., McAllister, M. M., Guy, C. S., McGarry, J. W., Smith, R. F. and Williams, D. (2002). Neospora caninum: oocyst challenge of pregnant cows. Veterinary Parasitology 109, 147–154.Google Scholar
Trees, A. J. and Williams, D. J. L. (2005). Endogenous and exogenous transplacental infection in Neospora caninum and Toxoplasma gondii. Trends in Parasitology 21, 558–561.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
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.CrossRefGoogle ScholarPubMed
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, 347–351.Google Scholar