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Evidence for high levels of vertical transmission in Toxoplasma gondii

Published online by Cambridge University Press:  21 September 2009

G. HIDE*
Affiliation:
Centre for Parasitology and Disease Research, School of Environment and Life Sciences, University of Salford, Salford, M5 4WT, UK
E. K. MORLEY
Affiliation:
Centre for Parasitology and Disease Research, School of Environment and Life Sciences, University of Salford, Salford, M5 4WT, UK
J. M. HUGHES
Affiliation:
Centre for Parasitology and Disease Research, School of Environment and Life Sciences, University of Salford, Salford, M5 4WT, UK
O. GERWASH
Affiliation:
Centre for Parasitology and Disease Research, School of Environment and Life Sciences, University of Salford, Salford, M5 4WT, UK
M. S. ELMAHAISHI
Affiliation:
Misurata Central Hospital, PO Box 65 Misurata, Libya
K. H. ELMAHAISHI
Affiliation:
Misurata Central Hospital, PO Box 65 Misurata, Libya
D. THOMASSON
Affiliation:
Centre for Parasitology and Disease Research, School of Environment and Life Sciences, University of Salford, Salford, M5 4WT, UK
E. A. WRIGHT
Affiliation:
Centre for Parasitology and Disease Research, School of Environment and Life Sciences, University of Salford, Salford, M5 4WT, UK
R. H. WILLIAMS
Affiliation:
Centre for Parasitology and Disease Research, School of Environment and Life Sciences, University of Salford, Salford, M5 4WT, UK
R. G. MURPHY
Affiliation:
Centre for Parasitology and Disease Research, School of Environment and Life Sciences, University of Salford, Salford, M5 4WT, UK
J. E. SMITH
Affiliation:
Faculty of Biological Sciences, University of Leeds, Leeds, LS2 9JT, UK
*
*Corresponding author: Geoff Hide, Centre for Parasitology and Disease, School of Environment and Life Sciences, University of Salford, Salford, UK, M5 4WT. Tel: 0044-161-295-3371. Fascimile No: 0044-161-295-5015. E-mail: g.hide@salford.ac.uk

Summary

Toxoplasma gondii is a highly ubiquitous and prevalent parasite. Despite the cat being the only definitive host, it is found in almost all geographical areas and warm blooded animals. Three routes of transmission are recognised: ingestion of oocysts shed by the cat, carnivory and congenital transmission. In natural populations, it is difficult to establish the relative importance of these routes. This paper reviews recent work in our laboratory which suggests that congenital transmission may be much more important than previously thought. Using PCR detection of the parasite, studies in sheep show that congenital transmission may occur in as many as 66% of pregnancies. Furthermore, in families of sheep on the same farm, exposed to the same sources of oocysts, significant divergent prevalences of Toxoplasma infection and abortion are found between different families. The data suggest that breeding from infected ewes increases the risk of subsequent abortion and infection in lambs. Congenital transmission rates in a natural population of mice were found to be 75%. Interestingly, congenital transmission rates in humans were measured at 19·8%. The results presented in these studies differ from those of other published studies and suggest that vertical transmission may be much more important than previously thought.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Aspinall, T. V., Marlee, D., Hyde, J. E. and Sims, P. F. G. (2002). Prevalence of Toxoplasma gondii in commercial meat products as monitored by polymerase chain reaction – food for thought? International Journal for Parasitology 32, 11931199.CrossRefGoogle ScholarPubMed
Beverley, J. K. A. (1959). Congenital transmission of Toxoplasmosis through successive generation of mice. Nature 183, 13481349.CrossRefGoogle ScholarPubMed
Beverley, J. K. A. and Watson, W. A. (1971). Prevention of experimental and naturally occurring ovine abortion due to toxoplasmosis. Veterinary Record 88, 3941.CrossRefGoogle ScholarPubMed
Boyer, K. M., Holfels, E., Roizen, N., Swisher, C., Mack, D., Remington, J., Withers, S., Meier, P. and McLeod, R. (2005). Risk factors for Toxoplasma gondii infection in mothers of infants with congenital toxoplasmosis: implications for prenatal management and screening. American Journal of Obstetrics and Gynecology 192, 564571.CrossRefGoogle ScholarPubMed
Buxton, D. and Innes, E. A. (1995). A commercial vaccine for ovine toxoplasmosis. Parasitology 110, 1116.CrossRefGoogle ScholarPubMed
Buxton, D., Maley, S. W., Wright, S. E., Rodger, S., Bartley, P. and Innes, E. A. (2007 a). Toxoplasma gondii and ovine toxoplasmosis: New aspects of an old story. Veterinary Parasitology 149, 2528.CrossRefGoogle ScholarPubMed
Buxton, D., Maley, S. W., Wright, S. E., Rodger, S., Bartley, P. and Innes, E. A. (2007 b). Ovine toxoplasmosis: transmission, clinical outcome and control. Parassitologia 49, 219221.Google ScholarPubMed
Buxton, D., Rodger, S. M., Maley, S. W. and Wright, S. E. (2006). Toxoplasmosis: The possibility of vertical transmission. Small Ruminant Research 62, 4346.CrossRefGoogle Scholar
Cook, A. J. C., Gilbert, R. E., Buffolano, W., Zufferey, J., Petersen, E., Jenum, P. A., Foulon, W., Semprini, A. E. and Dunn, D. T. (2000). Sources of Toxoplasma infection in pregnant women: European multicentre case control study. British Medical Journal 321, 142147.CrossRefGoogle ScholarPubMed
DEFRA (2007). Veterinary Surveillance Report 2007 – VIDA. Veterinary Laboratories Agency. ISBN 1 8995 1331 0.Google Scholar
Dubey, J. P. (2009 a). History of the discovery of the life cycle of Toxoplasma gondii. International Journal for Parasitology 39, 877882.CrossRefGoogle ScholarPubMed
Dubey, J. P. (2009 b). Toxoplasmosis in sheep – The last 20 years. Veterinary Parasitology 163, 114.CrossRefGoogle ScholarPubMed
Dubey, J. P. and Beattie, C. P. (1988). Toxoplasmosis of Animals and Man, CRC Press, Boca Raton, Florida.Google Scholar
Dubey, J. P., Hill, D. E., Jones, J. L., Hightower, A. W., Kirkland, E., Roberts, J. M., Marcet, P. L., Lehmann, T., Vianna, M. C. B., Miska, K., Sreekumar, C., Kwok, O. C. H., Shen, S. K. and Gamble, H. R. (2005). Prevalence of viable Toxoplasma gondii in beef, chicken and pork from retail meat stores in the United States: risk assessment to consumers. Journal of Parasitology 91, 10821093.CrossRefGoogle ScholarPubMed
Dubey, J. P. and Jones, J. L. (2008). Toxoplasma gondii infection in humans and animals in the United States. International Journal for Parasitology 38, 12571278.CrossRefGoogle ScholarPubMed
Dubey, J. P., Miller, N. L. and Frenkel, J. K. (1970). The Toxoplasma gondii oocyst from cat feces. Journal of Experimental Medicine 132, 636662.CrossRefGoogle ScholarPubMed
Dubey, J. P., Shen, S. K., Kwok, O. C. and Thulliez, P. (1997). Toxoplasmosis in rats (Rattus norvegicus): congenital transmission to first and second generation offspring and isolation Toxoplasma gondii from seronegative rats. Parasitology 115, 914.CrossRefGoogle ScholarPubMed
Dubey, J. P., Weigel, R. M., Siegel, A. M., Thulliez, P., Kitron, U. D., Mitchell, M. A., Mannelli, A., Mateuspinillia, N. E., Shen, S. K., Kwok, O. C. H. and Todd, K. S. (1995). Sources and reservoirs of Toxoplasma gondii infection on 47 swine farms in Illinois. Journal of Parasitology. 81, 723729.CrossRefGoogle ScholarPubMed
Dubey, J. P., Zarnke, R., Thomas, N. J., Wong, S. K., Van Bonn, W., Briggs, M., Davis, J. W., Ewing, R., Mensea, M., Kwok, O. C. H., 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 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
Frenkel, J. K., Dubey, J. P. and Miller, N. L. (1970). Toxoplasma gondii in cats: fecal stages identified as coccidian oocysts. Science 167, 893896.CrossRefGoogle ScholarPubMed
Grigg, M. E. and Sundar, N. (2009). Sexual recombination punctuated by outbreaks and clonal expansions predicts Toxoplasma gondii population genetics. International Journal for Parasitology 39, 925933.CrossRefGoogle ScholarPubMed
Hartley, W. J. and Marshall, S. C. (1957). Toxoplasmosis as a cause of ovine perinatal mortality. New Zealand Veterinary Journal 5, 119124.CrossRefGoogle Scholar
Hide, G., Gerwash, O., Morley, E. K., Williams, R. H., Hughes, J. M., Thomasson, D., Elmahaishi, M. S., Elmahaishi, K. H., Terry, R. S. and Smith, J. E. (2007). Does vertical transmission contribute to the prevalence of toxoplasmosis? Parassitologia 49, 223226.Google Scholar
Hughes, J. M., Thomasson, D., Craig, P. S., Georgin, S., Pickles, A. and Hide, G. (2008). Neospora caninum: detection in wild rabbits and investigation of co-infection with Toxoplasma gondii by PCR analysis. Experimental Parasitology 120, 255260.CrossRefGoogle ScholarPubMed
Hughes, J. M., Williams, R. H., Morley, E. K., Cook, D. A. N., Terry, R. S., Murphy, R. G., Smith, J. E. and Hide, G. (2006). The Prevalence of Neospora caninum and co-infection with Toxoplasma gondii by PCR analysis in naturally occurring mammal populations. Parasitology 132, 2936.CrossRefGoogle ScholarPubMed
Hutchison, W. M., Dunachie, J. F., Siim, J. C. and Work, K. (1969). Life cycle of Toxoplasma gondii. British Medical Journal 4, 806806.CrossRefGoogle ScholarPubMed
Innes, E. A., Bartley, P. M., Buxton, D. and Katzer, F. (2009). Ovine toxoplasmosis. Parasitology 136, 1887–1894.CrossRefGoogle ScholarPubMed
Kijlstra, A., Meerburg, B., Cornelissen, J., De Craeye, S., Vereijken, P. and Jongert, E. (2008). The role of rodents and shrews in the transmission of Toxoplasma gondii to pigs. Veterinary Parasitology 156, 183190.CrossRefGoogle ScholarPubMed
Marshall, P. A., Hughes, J. M., Williams, R. H., Smith, J. E., Murphy, R. G. and Hide, G. (2004). Detection of high levels of congenital transmission of Toxoplasma gondii in natural urban populations of Mus domesticus. Parasitology 128, 3942.CrossRefGoogle ScholarPubMed
McColgan, C., Buxton, D. and Blewett, D. A. (1988). Titration of Toxoplasma gondii oocysts in non-pregnant sheep and the effects of subsequent challenge during pregnancy. Veterinary Record 123, 467470.CrossRefGoogle ScholarPubMed
Miller, M. A., Gardner, I. A., Kreuder, C., Paradies, D. M., Worcester, K. R., Jessup, D. A., Dodd, E., Harris, M. D., Ames, J. A., Packham, A. E. and Conrad, P. A. (2002). Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis). International Journal for Parasitology 32, 9971006.CrossRefGoogle ScholarPubMed
Morley, E. K., Williams, R. H., Hughes, J. M., Terry, R. S., Duncanson, P., Smith, J. E. and Hide, G. (2005). Significant familial differences in the frequency of abortion and Toxoplasma gondii infection within a flock of Charollais sheep. Parasitology 131, 181185.CrossRefGoogle ScholarPubMed
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
Murphy, R. G., Williams, R. H., Hughes, J. M., Hide, G., Ford, N. J. and Oldbury, D. J. (2008). The urban house mouse (Mus domesticus) as a reservoir of infection for the human parasite Toxoplasma gondii: an unrecognised public health issue? International Journal of Environmental Health Research 18, 177185.CrossRefGoogle ScholarPubMed
Owen, M. R. and Trees, A. J. (1998). Vertical transmission of Toxoplasma gondii from chronically infected house (Mus musculus) and field (Apodemus sylvaticus) mice determined by polymerase chain reaction. Parasitology 116, 299304.CrossRefGoogle ScholarPubMed
Prestrud, K. W., Asbakk, K., Mørk, T., Fuglei, E., Tryland, M. and Su, C. (2008 b). Direct high-resolution genotyping of Toxoplasma gondii in arctic foxes (Vulpes lagopus) in the remote arctic Svalbard archipelago reveals widespread clonal Type II lineage. Veterinary Parasitology 158, 121128.CrossRefGoogle ScholarPubMed
Prestrud, K. W., Dubey, J. P., Asbakk, K., Fuglei, E. and Su, C. (2008 a). First isolate of Toxoplasma gondii from arctic fox (Vulpes lagopus) from Svalbard. Veterinary Parasitology 151, 110114.CrossRefGoogle ScholarPubMed
Rawal, B. D. (1959). Toxoplasmosis. A dye-test on sera from vegetarians and meat eaters in Bombay. Transactions of the Royal Society for Tropical Medicine and Hygiene 53, 6163.CrossRefGoogle ScholarPubMed
Rodger, S. M., Maley, S. W., Wright, S. E., Mackellar, A., Wesley, F., Sales, J. and Buxton, D. (2006). Role of endogenous transplacental transmission in toxoplasmosis in sheep. Veterinary Record 159, 768772.Google ScholarPubMed
Sibley, L. D. and Boothroyd, J. C. (1992). Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature 359, 8285.CrossRefGoogle ScholarPubMed
Su, C., Evans, D., Cole, R. H., Kissinger, J. C., Ajioka, J. W. and Sibley, L. D. (2003). Recent expansion of Toxoplasma through enhanced oral transmission. Science 299, 414416.CrossRefGoogle ScholarPubMed
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 12171258.CrossRefGoogle ScholarPubMed
Terry, R. S., Smith, J. E., Duncanson, P. and Hide, G. (2001). MGE-PCR: a novel approach to the analysis of Toxoplasma gondii strain differentiation using mobile genetic elements. International Journal for Parasitology 31, 155161.CrossRefGoogle 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, 558561.CrossRefGoogle ScholarPubMed
Weiss, L. M. and Dubey, J. P. (2009). Toxoplasmosis: A history of clinical observations. International Journal for Parasitology 39, 895901.CrossRefGoogle ScholarPubMed
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