Hostname: page-component-7c8c6479df-nwzlb Total loading time: 0 Render date: 2024-03-28T09:50:47.671Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  21 October 2004

R. H. WILLIAMS
Affiliation:
Centre for Parasitology, Molecular Epidemiology and Ecology, Bioscience Research Institute, School of Environment and Life Sciences, University of Salford, Salford M5 4WT, UK
E. K. MORLEY
Affiliation:
Centre for Parasitology, Molecular Epidemiology and Ecology, Bioscience Research Institute, School of Environment and Life Sciences, University of Salford, Salford M5 4WT, UK
J. M. HUGHES
Affiliation:
Centre for Parasitology, Molecular Epidemiology and Ecology, Bioscience Research Institute, School of Environment and Life Sciences, University of Salford, Salford M5 4WT, UK
P. DUNCANSON
Affiliation:
Centre for Parasitology, Molecular Epidemiology and Ecology, Bioscience Research Institute, School of Environment and Life Sciences, University of Salford, Salford M5 4WT, UK
R. S. TERRY
Affiliation:
School of Biology, University of Leeds, Leeds LS2 9TJ, UK
J. E. SMITH
Affiliation:
School of Biology, University of Leeds, Leeds LS2 9TJ, UK
G. HIDE
Affiliation:
Centre for Parasitology, Molecular Epidemiology and Ecology, Bioscience Research Institute, School of Environment and Life Sciences, University of Salford, Salford M5 4WT, UK

Abstract

Recent research suggests that vertical transmission may play an important role in sustaining Toxoplasma gondii infection in some species. We report here that congenital transmission occurs at consistently high levels in pedigree Charollais and outbred sheep flocks sampled over a 3-year period. Overall rates of transmission per pregnancy determined by PCR based diagnosis, were consistent over time in a commercial sheep flock (69%) and in sympatric (60%) and allopatric (41%) populations of Charollais sheep. The result of this was that 53·7% of lambs were acquiring an infection prior to birth: 46·4% of live lambs and 90·0% of dead lambs (in agreement with the association made between T. gondii and abortion). No significant differences were observed between lamb sexes. Although we cannot distinguish between congenital transmission occurring due to primary infection at pregnancy or reactivation of chronic infection during pregnancy, our observations of consistently high levels of congenital transmission over successive lambings favour the latter.

Type
Research Article
Copyright
2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

AVELINO, M. M. & CAMPOS, Jr. D. ( 2002). Pregnancy as a risk factor for acute toxoplasmosis seroconversion. European Journal of Obstetrics, Gynaecology and Reproductive Biology 4417, 16.Google Scholar
BARBER, J. S. & TREES, A. J. ( 1998). Naturally occurring vertical transmission of Neospora caninum in dogs. International Journal for Parasitology 28, 5764.CrossRefGoogle Scholar
BEVERLEY, J. K. A. ( 1959). Congenital transmission of Toxoplasmosis through successive generations of mice. Nature, London 183, 13481349.CrossRefGoogle Scholar
BEVERLEY, J. K. A. & WATSON, W. A. ( 1971). Prevention of experimental and of naturally occurring ovine abortion due to toxoplasmosis. Veterinary Record 88, 3941.CrossRefGoogle Scholar
BJORKMAN, C., JOHANSSON, O., STENLUND, S., HOLMDAHL, O. J. & UGGLA, A. ( 1996). Neospora species infection in a herd of dairy cattle. Journal of the American Veterinary Medicine Association 208, 14411444.Google Scholar
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.Google Scholar
BUXTON, D. ( 1990). Ovine toxoplasmosis: a review. Journal of the Royal Society of Medicine 83, 509511.CrossRefGoogle Scholar
COLE, R. A., LINDSAY, D. S., BLAGBURN, B. L. & DUBEY, J. P. ( 1995). Vertical transmission of Neospora caninum in mice. Journal of Parasitology 81, 730732.CrossRefGoogle Scholar
DAVISON, H. C., OTTER, A. & TREES, A. J. ( 1999). Estimation of vertical and horizontal transmission parameters in Neospora caninum infections in dairy cattle. International Journal for Parasitology 29, 16831689.CrossRefGoogle Scholar
DUBEY, J. P. & BEATTIE, C. P. ( 1988). Toxoplasmosis of Animal and Man. CRC Press, Boca Raton, Fl, USA.
DUBEY, J. P. & SHEN, S. K. ( 1991). Rat model of congenital toxoplasmosis. Infection and Immunity 59, 33013302.Google Scholar
DUBEY, J. P., SHEN, S. K., KWOK, O. C. H. & THULLIEZ, P. ( 1997). Toxoplasmosis in rats (Rattus norvegicus): congenital transmission to first and second generation offspring and isolation of Toxoplasma gondii from seronegative rats. Parasitology 115, 914.CrossRefGoogle Scholar
DUNCANSON, P., TERRY, R. S., SMITH, J. E. & HIDE, G. ( 2001). High levels of congenital transmission of Toxoplasma gondii in a commercial sheep flock. International Journal for Parasitology 31, 16991703.CrossRefGoogle Scholar
HAFID, J., FLORI, P., RABERIN, H. & TRAN MANH SUNG, R. ( 2001). Comparison of PCR, capture ELISA and immunoblotting for detection of Toxoplasma gondii in infected mice. Journal of Medical Microbiology 50, 11001104.CrossRefGoogle Scholar
HARTLEY, W. J. & MARSHALL, S. C. ( 1957). Toxoplasmosis as a cause of ovine perinatal mortality. New Zealand Veterinary Journal 5, 119124.CrossRefGoogle Scholar
HUTCHISON, W. M. ( 1965). Experimental transmission of Toxoplasma gondii. Nature, London 206, 961962.CrossRefGoogle Scholar
JOHNSON, A. M. ( 1997). Speculation on possible life cycles for the clonal lineages in the genus Toxoplasma. Parasitology Today 13, 393397.CrossRefGoogle Scholar
LEGUIA, G. & HERBERT, I. V. ( 1979). The prevalence of Sarcocytis spp. in dogs, foxes and sheep and Toxoplasma gondii in sheep and the use of the indirect haemagglutination reaction in serodiagnosis. Research in Veterinary Science 27, 390391.Google Scholar
MARSHALL, P. A., HUGHES, J. M., WILLIAMS, R. H., SMITH, J. E., MURPHY, R. G. & HIDE, G. ( 2004). Detection of high levels of congenital transmission of Toxoplasma gondii in natural populations of Mus domesticus. Parasitology 128, 14.CrossRefGoogle Scholar
OWEN, M. R. & 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 Scholar
OWEN, M. R., CLARKSON, M. J. & TREES, A. J. ( 1997). Diagnosis of ovine Toxoplasma abortion by polymerase chain reaction. Veterinary Record 142, 445448.Google Scholar
ROEVER-BONNET, H. DE ( 1969). Congenital Toxoplasma infections in mice and hamsters infected with avirulent and virulent strains. Tropical and Geographical Medicine 21, 443450.Google Scholar
SAC. VETERINARY SCIENCE DIVISION. ( 1999). Sheep abortion figures analysed as the 1999 lambing season ends in Scotland. Veterinary Record 145, 240242.
SAMAD, M. A. & CLARKSON, M. J. ( 1994). Seroconversion to natural Toxoplasma gondii infection during reproductive cycle and its effect on reproduction on sheep. Bangladesh Veterinary Journal 28, 16.Google Scholar
SAVVA, D., MORRIS, J. C., JOHNSON, J. D. & HOLLIMAN, R. E. ( 1990). Polymerase chain reaction for the detection of Toxoplasma gondii. Journal of Medical Microbiology 32, 2531.CrossRefGoogle Scholar
SCHARES, G., WENZEL, U., MULLER, T. & CONRATHS, F. J. ( 2001). Serological evidence for naturally occurring transmission of Neospora caninum among foxes (Vulpes vulpes). International Journal for Parasitology 31, 418423.CrossRefGoogle Scholar
SKJERVE, E., WALDELAND, H., NESBAKKEN, T. & KAPPERUD, G. ( 1998). Risk factors for the presence of antibodies to Toxoplasma gondii in Norwegian slaughter lambs. Preventative Veterinary Medicine 35, 219227.CrossRefGoogle Scholar
SU, C., EVANS, D., COLE, R. H., KISSINGER, J. C., AJIOKA, J. W. & SIBLEY, L. D. ( 2003). Recent expansion of Toxoplasma through oral transmission. Science 299, 414416.CrossRefGoogle Scholar
SUZUKI, Y. & KOBAYASHI, A. ( 1990). Induction of tolerance of Toxoplasma gondii in newborn mice by maternal antibody. Parasitology Research 76, 424427.CrossRefGoogle Scholar
TENTER, A. M., HECKEROTH, A. R. & WEISS, L. M. ( 2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 12171258.CrossRefGoogle Scholar
TERRY, R. S., SMITH, J. E., DUNCANSON, P. & 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
VAN DER PUIJE, W. N., BOSOMPEM, K. M., CANACOO, E. A., WASTLING, J. M. & AKANMORI, B. D. ( 2000). The prevalence of anti-Toxoplasma gondii antibodies in Ghanaian sheep and goats. Acta Tropica 76, 2126.CrossRefGoogle Scholar
WALDELAND, H. ( 1977). Toxoplasmosis in sheep – influence of various factors on antibody contents. Acta veterinaria scandinavica 18, 237247.Google Scholar
ZENNER, L., DARCY, F., CESBRON-DELAUW, M. F. & CAPRON, A. ( 1993). Rat model of congenital toxoplasmosis- rate of transmission of 3 Toxoplasma gondii strains to foetuses and protective effect of a chronic infection. Infection and Immunity 61, 360363.Google Scholar