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Ovine toxoplasmosis

Published online by Cambridge University Press:  08 December 2009

ELISABETH A. INNES*
Affiliation:
Moredun Research Institute, Pentlands Science Park, Edinburgh EH26 OPZ
PAUL M. BARTLEY
Affiliation:
Moredun Research Institute, Pentlands Science Park, Edinburgh EH26 OPZ
DAVID BUXTON
Affiliation:
Moredun Research Institute, Pentlands Science Park, Edinburgh EH26 OPZ
FRANK KATZER
Affiliation:
Moredun Research Institute, Pentlands Science Park, Edinburgh EH26 OPZ
*
Corresponding author: E-mail: lee.innes@moredun.ac.uk

Summary

Congenital infection with Toxoplasma gondii is an important cause of abortion in sheep worldwide. The cat is the definitive host of the parasite, and infected cats may shed millions of oocysts in their faeces resulting in extensive environmental contamination and an important source of infection for grazing herbivorous animals. Studies looking at development of specific antibodies in sheep, as an indicator of exposure to T. gondii, have shown that there is an increase in seroprevalence associated with age indicating that most infections in sheep occur following birth. The stage of gestation when transplacental transmission of T. gondii to the developing foetus occurs is critical in determining the clinical outcome. The importance of endogenous transplacental transmission in persistently infected ewes and its clinical importance is a subject of current debate. Ewes infected prior to mating develop immune responses that help protect against disease in a subsequent pregnancy and also against experimental challenge administered during pregnancy. Both innate and adaptive immune responses are activated following T. gondii infection and experiments involving the chronic cannulation of peripheral lymph nodes in sheep have allowed the dynamics of the immune responses to be analysed in real time. A live vaccine, Toxovax® is the only commercially available vaccine worldwide to protect against congenital toxoplasmosis.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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References

Blewett, D. A. (1983). The epidemiology of ovine toxoplasmosis I. The interpretation of data for the prevalence of antibody in sheep and other host species. British Veterinary Journal 139, 537545.CrossRefGoogle ScholarPubMed
Blewett, D. A., Miller, J. K. and Buxton, D. (1982). Response of immune and susceptible ewes to infection with Toxoplasma gondii. Veterinary Record 111, 175178.CrossRefGoogle ScholarPubMed
Blewett, D. A. and Trees, A. J. (1987). The epidemiology of ovine toxoplasmosis with special respect to control. British Veterinary Journal 143, 128135.CrossRefGoogle Scholar
Buxton, D. (1990). Ovine toxoplasmosis: a review. Journal of the Royal Society of Medicine 83, 509511.CrossRefGoogle ScholarPubMed
Buxton, D. (1993). Toxoplasmosis: the first commercial vaccine. Parasitology Today 9, 335337.CrossRefGoogle ScholarPubMed
Buxton, D. and Finlayson, J. (1986). Experimental infection of pregnant sheep with Toxoplasma gondii: pathological and immunological observations on the placenta and foetus. Journal of Comparative Pathology 96, 319333.CrossRefGoogle ScholarPubMed
Buxton, D. and Innes, E. A. (1995). A commercial vaccine for ovine toxoplasmosis. Parasitology 110, 1116.CrossRefGoogle ScholarPubMed
Buxton, D. and Rodger, S. M. (2008). Toxoplasmosis and neosporosis. In Diseases of Sheep. 4th Ed (ed. Aitken, I. D.) Wiley-Blackwell, Hoboken, p. 112118.Google Scholar
Buxton, D., Thomson, K. M., Maley, S., Wastling, J. M., Innes, E. A. and Panton, W. R. M. (1994). Primary and secondary responses of the ovine lymph node to Toxoplasma gondii: cell output in efferent lymph and parasite detection. Journal of Comparative Pathology 111, 231241.Google 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 ScholarPubMed
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 ScholarPubMed
Dabritz, H. A., Miller, M. A., Atwill, E. R., Gardner, I. A., Leutenegger, C. M., Melli, A. C. and Conrad, P. A. (2007). Detection of Toxoplasma gondii like oocysts in cat faeces and estimates of the environmental oocyst burden. Journal of the American Veterinary Medical Association 231, 16761684.Google Scholar
Dubey, J. P. (1984). Experimental toxoplasmosis in sheep fed Toxoplasma gondii oocysts. International Goat and Sheep Research 2, 93104.Google Scholar
Dubey, J. P. and Beattie, C. P. (1988). Toxoplasmosis of Animals and Man. Boca Raton, Florida: CRC Press.Google Scholar
Dubey, J. P. and Sharma, S. P. (1980). Parasitaemia and tissue infection in sheep fed Toxoplasma gondii oocysts. Journal of Parasitology 66, 111114.CrossRefGoogle ScholarPubMed
Duncanson, P., Terry, R. S., Smith, J. E. and Hide, G. (2001). High levels of congenital transmission of Toxoplasma gondii in a commercial sheep flock. International Journal for Parasitology 31, 16991703.CrossRefGoogle Scholar
Entrican, G. and Wheelhouse, N. M. (2006). Immunity in the female sheep reproductive tract. Veterinary Research 37, 295309.CrossRefGoogle ScholarPubMed
Faull, W. B., Clarkson, M. J. and Winter, A. C. (1986). Toxoplasmosis in a flock of sheep: some investigations into its source and control. Veterinary Record 119, 491493.CrossRefGoogle Scholar
Ferguson, D. J. P. (2009). Toxoplasma gondii: 1908–2008, homage to Nicolle, Manceaux and Splendore. Memorias do Instituto Oswaldo Cruz 104, 133148.CrossRefGoogle ScholarPubMed
Ferguson, D. J. P., Hutchison, W. M., Dunachie, J. F. and Sim, J. C. (1974). Ultrastructural study of early stages of asexual multiplication and microgametogony of Toxoplasma gondii in the small intestine of the cat. Acta Pathology Microbiology Scandinavian Microbiology and Immunology 82, 167181.Google Scholar
Frenkel, J. K., Dubey, J. P. and Miller, N. L. (1970). Toxoplasma gondii in cats: faecal stages identified as coccidian oocysts. Science 167, 893896.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Hartley, W. J. (1961). Experimental transmission of toxoplasmosis in sheep. New Zealand Veterinary Journal 9, 17.CrossRefGoogle Scholar
Hartley, W. J., Jebson, J. L. and McFarlane, D. (1954). New Zealand type II abortions in ewes. Australian Veterinary Journal 30, 216218.CrossRefGoogle Scholar
Hartley, W. J. and Marshall, S. C. (1957). Toxoplasmosis as a cause of ovine perinatal mortality. New Zealand Veterinary Journal 5, 119124.CrossRefGoogle Scholar
Hartley, W. J. and Moyle, G. G. (1974). Further observations on the epidemiology of ovine toxoplasma infection. Australian Journal of Experimental Biology and Medical Science 52, 647653.CrossRefGoogle ScholarPubMed
Hide, G., Morley, E. K., Hughes, J. M., Gerwash, O., Elmahaishi, M. S., Elmahaishi, K. H., Thomasson, D., Wright, E. A., Williams, R. H., Murphy, R. G. and Smith, J. E. (2009). Evidence for high levels of vertical transmission in Toxoplamsa gondii. Parasitology 136, 18771885.Google Scholar
Hutchison, W. M. (1965). Experimental transmission of Toxoplasma gondii. Nature 206, 961962.CrossRefGoogle ScholarPubMed
Hutchison, W. M., Dunachie, J. F., Sim, J. C. and Work, K. (1970). Coccidian-like nature of Toxoplasma gondii. British Medical Journal 1, 142144.Google Scholar
Innes, E. A. (2010). A brief history and overview of Toxoplasma gondii. Zoonoses and Public Health (In Press).CrossRefGoogle ScholarPubMed
Innes, E. A., Panton, W. R., Sanderson, A., Thomson, K. M., Wastling, J. M., Maley, S. W. 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Innes, E. A. and Vermeulen, A. N. (2006). Vaccination as a control strategy against the coccidial parasites Eimeria, Toxoplasma and Neospora. Parasitology 133, 145168.CrossRefGoogle ScholarPubMed
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.Google Scholar
Innes, E. A., Wright, S. E., 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, 2936.CrossRefGoogle ScholarPubMed
Lunden, A., Nasholm, A. and Uggla, A. (1994). Long-term study of Toxoplasma gondii infection in a Swedish sheep flock. Acta Veterinary Scandinavia 35, 273281.CrossRefGoogle Scholar
McColgan, C., Buxton, D. and Blewett, D. (1988). Titration of Toxoplasma gondii oocysts in non-pregnant sheep and the effects of subsequent challenge during pregnancy. Veterinary Record 123, 467470.CrossRefGoogle ScholarPubMed
Morley, E. K., Williams, R. H., Hughes, J. M., Terry, R. S., Duncanson, P., Smith, R. S. and Hide, G. (2005). Significant familial differnces in the frequency of abortion and Toxoplasma gondii infection within a flock of Charollais sheep. Parasitology 131, 181185.CrossRefGoogle Scholar
Morley, E. K., Williams, R. H., Hughes, J. M., Thomasson, D., Terry, R. S., Duncanson, P., Smith, J. E. and Hide, G. (2008). Evidence that primary infection of Charollais sheep with Toxoplasma gondii may not prevent foetal infection and abortion in subsequent lambings. Parasitology 135, 169173.CrossRefGoogle Scholar
Munday, B. L. (1972). Transmission of Toxoplasma infection from chronically infected ewes to their lambs. British Veterinary Journal 128, 7172.Google ScholarPubMed
Nicolle, C. and Manceaux, L. (1908). Sur une infection a corps de Leishman (ou organisms voisons) du gondii. Comptes Rendues. Academy of Sciences 147, 736.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
Oura, C. A., Innes, E. A., Wastling, J. M., Entrican, G. and Panton, W. R. (1993). The inhibitory effect of ovine recombinant interferon-gamma on intracellular replication of Toxoplasma gondii. Parasite Immunology 15, 535538.CrossRefGoogle ScholarPubMed
Plant, J. W., Richardson, N. and Moyle, G. G. (1974). Toxoplasma infection and abortion in sheep associated with feeding of grain contaminated with cat faeces. Australian Veterinary Journal 50, 1921.CrossRefGoogle ScholarPubMed
Rodger, S. M., Maley, S. W., Wright, S. E., Mackellar, A., Wesley, F., Sales, J. and Buxton, D. (2006). Ovine toxoplasmosis; the role of endogenous transmission. Veterinary Record 159, 768772.Google Scholar
Skjerve, E., Waldeland, H., Nesbakken, T. and Kapperud, G. (1998). Risk factors for the presence of antibodies to Toxoplasma gondii in Norwegian slaughter lambs. Preventative Veterinary Medicine 35, 219227.CrossRefGoogle ScholarPubMed
Splendore, A. (1908). Un nuovo protozoa parassita deconigli incontrato nelle lesioni anatomiche d'une malattia che ricorda in molti punti il Kala–azar dell'uoma. Nota preliminare pel. Review of the Societie of Sciences Sao Paulo 3, 109112.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, 558651.CrossRefGoogle ScholarPubMed
Waldeland, H. (1977). Toxoplasmosis in sheep. Influence of various factors on the antibody contents. Acta Veterinaria Scandinavia 18, 237247.CrossRefGoogle ScholarPubMed
Wastling, J. M., Nicoll, S. and Buxton, D. (1993). Comparison of two gene amplification methods for the detection of Toxoplasma gondii in experimentally infected sheep. Journal of Medical Microbiology 38, 360565.CrossRefGoogle ScholarPubMed
Watson, W. A. and Beverley, J. K. A. (1971). Epizootics of toxoplasmosis causing ovine abortion. Veterinary Record 88, 120124.CrossRefGoogle ScholarPubMed
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 lamb losses and reduce congenital infection following experimental oral challenge. New Zealand Veterinary Journal 36, 8689.Google Scholar
Williams, D. J. L., Hartley, C. S., Bjorkman, C. and Trees, A. J. (2009). Endogenous and exogenous transplacental transmission of Neospora caninum – how the route of transmission impacts on epidemiology and control of disease. Parasitology 136, 18951900.Google Scholar
Williams, R. H., Morley, E. K., Hughes, J. M., Duncanson, P., Terry, R. S., Smith, J. E. and Hide, G. (2005). High levels of congenital transmission of Toxoplasma gondii in longitudinal and cross sectional studies on sheep farms provides evidence of vertical transmission in ovine hosts. Parasitology 130, 301307.CrossRefGoogle ScholarPubMed