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Prevalence and co-infection of Toxoplasma gondii and Neospora caninum in Apodemus sylvaticus in an area relatively free of cats

  • D. THOMASSON (a1), E. A. WRIGHT (a1), J. M. HUGHES (a1), N. S. DODD (a1), A. P. COX (a2), K. BOYCE (a1), O. GERWASH (a1), M. ABUSHAHMA (a1), Z.-R. LUN (a3), R. G. MURPHY (a1), M. T. ROGAN (a1) and G. HIDE (a1)...
Summary
SUMMARY

The protozoan parasite Toxoplasma gondii is prevalent worldwide and can infect a remarkably wide range of hosts despite felids being the only definitive host. As cats play a major role in transmission to secondary mammalian hosts, the interaction between cats and these hosts should be a major factor determining final prevalence in the secondary host. This study investigates the prevalence of T. gondii in a natural population of Apodemus sylvaticus collected from an area with low cat density (<2·5 cats/km2). A surprisingly high prevalence of 40·78% (95% CI: 34·07%–47·79%) was observed despite this. A comparable level of prevalence was observed in a previously published study using the same approaches where a prevalence of 59% (95% CI: 50·13%–67·87%) was observed in a natural population of Mus domesticus from an area with high cat density (>500 cats/km2). Detection of infected foetuses from pregnant dams in both populations suggests that congenital transmission may enable persistence of infection in the absence of cats. The prevalences of the related parasite, Neospora caninum were found to be low in both populations (A. sylvaticus: 3·39% (95% CI: 0·12%–6·66%); M. domesticus: 3·08% (95% CI: 0·11%–6·05%)). These results suggest that cat density may have a lower than expected effect on final prevalence in these ecosystems.

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Corresponding author
*Corresponding author: Centre for Parasitology and Disease, School of Environment and Life Sciences, University of Salford, Salford M5 4WT, UK. Tel: 0044 161 295 3371. Fax: 0044 161 295 5015. E-mail: g.hide@salford.ac.uk
References
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Araujo J. B., da Silva A. V., Rosa R. C., Mattie R. J., da Silva R. C., Richini-Pereira V. B. and Langoni H. (2010). Isolation of multilocus genotyping of Toxoplasma gondii in seronegative rodents in Brazil. Veterinary Parasitology 174, 328331.
Beverley J. K. A. (1959). Congenital transmission of toxoplasmosis through successive generation of mice. Nature, London 183, 13481349.
Cole R. A., Lindsay D. S., Blagburn B. L. and Dubey J. P. (1995). Vertical transmission of Neospora caninum in mice. Journal of Parasitology 81, 730732.
Dabritz H. A., Miller M. A., Gardner I. A., Packham A. E., Atwill E. R. and Conrad P. A. (2008). Risk factors for Toxoplasma gondii infection in wild rodents from central coastal California and a review of T. gondii prevalence in rodents. Journal of Parasitology 94, 675683.
Dubey J. P. (1995). Duration of immunity to shedding of Toxoplasma gondii oocysts by cats. Journal of Parasitology 81, 410415.
Dubey J. P. (2009 a). History of the discovery of the life cycle of Toxoplasma gondii. International Journal for Parasitology 39, 877882.
Dubey J. P. (2009 b). The evolution of the knowledge of cat and dog coccidia. Parasitology 136, 14691475.
Dubey J. P. and Beattie C. P. (1988). Toxoplasmosis of Animals and Man. CRC Press, Boca Raton, FL, USA.
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.
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.
Dubey J. P., Miller N. L. and Frenkel J. K. (1970). Toxoplasma gondii life cycle in cats. Journal of the American Veterinary Medical Association 157, 12551255.
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.
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.
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.
Ferroglio E., Pasino M., Romano A., Grande D., Pregel P. and Trisciuogjio A. (2007). Evidence of Neospora caninum DNA in wild rodents. Veterinary Parasitology 148, 346349.
Franti C. E., Riemann H. P., Behmeyer D. E., Suther D., Howarth J. A. and Ruppanner R. (1976). Prevalence of Toxoplasma gondii antibodies in wild and domestic animals in northern California. Journal of the American Veterinary Medical Association. 169, 901906.
Grigg M. E., Ganatra J., Boothroyd J. C. and Margolis T. P. (2001). Unusual abundance of atypical strains associated with human ocular toxoplasmosis. Journal of Infectious Diseases 184, 633639.
Hejlicek K. and Literak I. (1998). Long-term study of Toxoplasma gondii prevalence in small mammals (Insectivora and Rodentia). Folia Zoologica 47, 93101.
Hejlicek K., Literak I. and Nezval J. (1997). Toxoplasmosis in wild mammals from the Czech Republic. Journal of Wildlife Diseases 33, 480485.
Herrmann D. C., Pantchev N., Vrhovec M. G., Barutzki D., Wilking H., Fröhlich A., Lüder C. G., Conraths F. J. and Schares G. (2010). Atypical Toxoplasma gondii genotypes identified in oocysts shed by cats in Germany. International Journal for Parasitology 40, 285292.
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.
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 Toxoplasma gondii. Parasitology 136, 18771885.
Higgs S. and Nowell F. (2000). Population biology of Eimeria (protozoa: Apicomplexa) in Apodemus sylvaticus: a capture study. Parasitology 120, 355363.
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.
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.
Innes E. A., Bartley P. M., Buxton D. and Katzer F. (2009). Ovine toxoplasmosis. Parasitology 136, 18871894.
Jackson M. H., Hutchison W. M. and Siim J. C. (1986). Toxoplasmosis in a wild rodent population of Central Scotland and a possible explanation of the mode of transmission. Journal of Zoology 209, 549557.
Jacobs L. (1964). The occurrence of Toxoplasma infection in the absence of demonstrable antibodies. In First International Congress of Parasitology, Vol. 1 (ed. Caorradetti A.), pp. 176177. Pergamon Press. Rome, Italy.
Jeon S. H. and Yong T. S. (2000). Serological observation of Toxoplasma gondii prevalence in Apodemus agrarius, a dominant species of field rodents in Korea. Yonsei Medical Journal 41, 491496.
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.
McAllister M. M., Dubey J. P., Lindsay D. S., Jolley W. R., Wills R. A. and McGuire A. M. (1998). Dogs are the definitive hosts of Neospora caninum. International Journal for Parasitology 28, 14731478.
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.
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.
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.
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.
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.
Rejmanek D., Vanwormer E., Mazet J. A. K., Packham A. E., Aguilar B. and Conrad P. A. (2010). Congenital transmission of Toxoplasma gondii in deer mice (Peromyscus maniculatus) after oral oocyst infection. Journal of Parasitology 96, 516520.
Schares G., Vrhovec M. G., Pantchev N., Herrmann D. C. and Conraths F. J. (2008). Occurrence of Toxoplasma gondii and Hammondia hammondi oocysts in the faeces of cats from Germany and other European countries. Veterinary Parasitology 152, 3445.
Smith D. D. and Frenkel J. K. (1995). Prevalence of antibodies to Toxoplasma gondii in wild mammals of Missouri and East Central Kansas – biologic and ecologic considerations of transmission. Journal of Wildlife Diseases 31, 1521.
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.
Tenter A. M., Heckeroth A. R. and Weiss L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 12171258.
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.
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.
Webster J. P. (1994). Prevalence and transmission of Toxoplasma gondii in wild brownrats, Rattus norvegicus. Parasitology 108, 407411.
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.
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.
Zhang S. Y., Jiang S. F., He Y. Y., Pan C. E., Zhu M. and Wei M. X. (2004). Serologic prevalence of Toxoplasma gondii in field mice, Microtus fortis, from Yuanjiang, Hunan province, People's Republic of China. Journal of Parasitology 90, 437438.
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