Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-26T12:17:23.820Z Has data issue: false hasContentIssue false
  • English
  • Français

The prevalence of Neospora caninum and co-infection with Toxoplasma gondii by PCR analysis in naturally occurring mammal populations

Published online by Cambridge University Press:  15 September 2005

J. M. HUGHES ,
R. H. WILLIAMS ,
E. K. MORLEY ,
D. A. N. COOK ,
R. S. TERRY ,
R. G. MURPHY ,
J. E. SMITH  and
G. HIDE
J. M. HUGHES
Affiliation:
Centre for Parasitology, Molecular Epidemiology and Ecology, Biosciences Research Institute, School of Environment and Life Sciences, University of Salford, Salford M5 4WT
R. H. WILLIAMS
Affiliation:
Centre for Parasitology, Molecular Epidemiology and Ecology, Biosciences Research Institute, School of Environment and Life Sciences, University of Salford, Salford M5 4WT
E. K. MORLEY
Affiliation:
Centre for Parasitology, Molecular Epidemiology and Ecology, Biosciences Research Institute, School of Environment and Life Sciences, University of Salford, Salford M5 4WT
D. A. N. COOK
Affiliation:
Centre for Parasitology, Molecular Epidemiology and Ecology, Biosciences Research Institute, School of Environment and Life Sciences, University of Salford, Salford M5 4WT
R. S. TERRY
Affiliation:
School of Biology, University of Leeds, Leeds LS2 9JT
R. G. MURPHY
Affiliation:
Research Institute for the Built and Human Environment, University of Salford, Salford M5 4WT
J. E. SMITH
Affiliation:
School of Biology, University of Leeds, Leeds LS2 9JT
G. HIDE
Affiliation:
Centre for Parasitology, Molecular Epidemiology and Ecology, Biosciences Research Institute, School of Environment and Life Sciences, University of Salford, Salford M5 4WT
Get access Rights & Permissions [Opens in a new window]

Abstract

Neospora caninum and Toxoplasma gondii are closely related intracellular protozoan parasites associated with bovine and ovine abortion respectively. Little is known about the extent of Neospora/Toxoplasma co-infection in naturally infected populations of animals. Using nested PCR techniques, based on primers from the Nc5 region of N. caninum and SAG1 for T. gondii, the prevalence of N. caninum and its co-infection with T. gondii were investigated in populations of Mus domesticus, Rattus norvegicus and aborted lambs (Ovis aries). A low frequency of infection with N. caninum was detected in the Mus domesticus (3%) and Rattus norvegicus (4·4%) populations. A relatively high frequency of infection with N. caninum was detected in the brains of aborted lambs (18·9%). There was no significant relationship between N. caninum and T. gondii co-infection. Investigation of the tissue distribution of Neospora, in aborted lambs, showed that Neospora could not be detected in tissues other than brain and this was in contrast to Toxoplasma where the parasite could be frequently detected in a range of tissues.

Keywords

Neospora caninumToxoplasma gondiiPCRco-infectionnaturally acquired infectionmouseratsheep
Type
Research Article
Information
Parasitology , Volume 132 , Issue 1 , January 2006 , pp. 29 - 36
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

Almeria, S., Ferrer, D., Pabon, M, Castella, J. and Manas, S. ( 2002). Red foxes (Vulpes vulpes) are a natural intermediate host of Neospora caninum. Veterinary Parasitology 107, 287–294.CrossRefGoogle Scholar
Baszler, T. V., Gay, L. J. C., Long, M. T. and Mathison, B. A. ( 1999). Detection by PCR of Neospora caninum in fetal tissues from spontaneous bovine abortions. Journal of Clinical Microbiology 37, 4059–4064.Google Scholar
Cheadle, M. A., Spencer, J. A. and Blagburn, B. L. ( 1999). Seroprevalences of Neospora caninum and Toxoplasma gondii in nondomestic felids from southern Africa. Journal of Zoo and Wildlife Medicine 30, 248–251.Google Scholar
Davison, H. C., Otter, A. and Trees, A. J. ( 1999). Estimation of vertical and horizontal transmission parameters of Neospora caninum in dairy cattle. International Journal for Parasitology 29, 1683–1689.CrossRefGoogle Scholar
Dubey, J. P. ( 1999). Recent advances in Neospora and Neosporosis. Veterinary Parasitology 84, 349–367.CrossRefGoogle Scholar
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, 1699–1703.CrossRefGoogle Scholar
Ellis, J. T., Amoyl, G., Ryce, C., Harper, P. A. W., Clough, K. A., Homan, W. L. and Brindley, P. J. ( 1998). Comparison of the large subunit ribosomal DNA of Neospora and Toxoplasma and development of a new genetic marker for their differentiation based on the D2 domain. Molecular and Cellular Probes 12, 1–13.Google Scholar
Figliuolo, L. P. C., Kasai, N., Ragozo, A. M. A., de Paula, V. S. O., Dias, R. A., Souza, S. L. A., Gennari, S. M. ( 2004). Prevalence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in ovine from Sao Paulo State, Brazil. Veterinary Parasitology 123 161–166.CrossRefGoogle 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 Scholar
Gottstein, B., Hentrrich, B., Wyss, R., Thur, B., Busato, A., Stark, K. D. C. and Muller, N. ( 1998). Molecular and immunodiagnostic investigations on bovine neosporosis in Switzerland. International Journal for Parasitology 28, 679–691.CrossRefGoogle Scholar
Graham, D. A., Calvert, V., Whyte, M., Marks, J. ( 1999). Absence of serological evidence for human Neospora caninum infection. Veterinary Record 144, 672–673.CrossRefGoogle Scholar
Hamilton, C. M., Gray, R, Wright, S. E., Gangadharan, B., Laurenson, K., Innes, E. A. ( 2005). Prevalence of antibodies to Toxoplasma gondii and Neospora caninum in red foxes (Vulpes vulpes) from around the UK. Veterinary Parasitology 130, 169–173.CrossRefGoogle Scholar
Hassig, M., Sager, H., Reitt, K., Ziegler, D., Strabel, D. and Gottstein, B. ( 2003). Neospora caninum in sheep: a herd case report. Veterinary Parasitology 117, 213–220.CrossRefGoogle Scholar
Hilali, M., Romand, S., Thulliez, P., Kwok, O. C. and Dubey, J. P. ( 1998). Prevalence of Neospora caninum and Toxoplasma gondii antibodies in sera from camels from Egypt. Veterinary Parasitology 75, 269–271.CrossRefGoogle Scholar
Hemphill, A. and Gottstein, B. ( 2000). A European perspective on Neospora caninum. International Journal for Parasitology 30, 877–924.CrossRefGoogle Scholar
Ho, M. S. Y., Barr, B. C., Rowe, J. D., Anderson, M. L., Sverlow, K. W., Packham, A., Marsh, A. E. and Conrad, P. A. ( 1997). Detection of Neospora sp. From infected bovine tissues by PCR and probe hybridization. Journal of Parasitology 83, 508–514.Google Scholar
Howe, D. K. and Sibley, D. ( 1999). Comparison of the major antigens of Neospora caninum and Toxoplasma gondii. International Journal for Parasitology 29 1489–1496.CrossRefGoogle Scholar
Huang, C. C., Yang, C. H., Watanabe, Y., Laio, Y. K. and Ooi, H. K. ( 2004). Finding of Neospora caninum in the wild brown rat (Rattus norvegicus). Veterinary Research 35, 283–290.CrossRefGoogle Scholar
Hutchinson W. M. ( 1965). Experimental transmission of Toxoplasma gondii. Nature, London 206, 961–962.CrossRefGoogle Scholar
Innes, E. A., Lunden, A., Esteban, I., Marks, J., Maley, S., Wright, S., Rae, A., Harkins, D., Vermeulen, A., McKendrick, I. J. and Buxton, D. ( 2001). A previous infection with Toxoplasma gondii does not protect against a challenge with Neospora caninum in pregnant sheep. Parasite Immunology 23, 121–132.CrossRefGoogle Scholar
Jakubek, E. B., Brojer, C., Regnersen, C., Uggla, A., Schares, G. and Bjorkman, C. ( 2001). Seroprevalences of Toxoplasma gondii and Neospora caninum in Swedish red foxes (Vulpes vulpes). Veterinary Parasitology 102, 167–172.CrossRefGoogle Scholar
Kaufmann, H., Yamage, M., Roditi, I., Dobbelaere, D., Dubey, J. P., Holmdahl, O. J. M., Trees, A. and Gottstein, B. ( 1996). Discrimination of Neospora caninum from Toxoplasma gondii and other apicomplexan parasites by hybridization and PCR. Molecular and Cellular Probes 10, 289–297.CrossRefGoogle Scholar
Lally, N. C., Jenkins, M. C. and Dubey, J. P. ( 1996). Development of a polymerase chain reaction assay for the diagnosis of neosporosis using the Neospora caninum 14-3-3 gene. Molecular and Biochemical Parasitology 75, 169–178.CrossRefGoogle Scholar
Liddell, S., Jenkins, M. C. and Dubey, J. P. ( 1999). A competitive PCR assay for the quantitative detection of Neospora caninum. International Journal for Parasitology 29, 1583–1587.CrossRefGoogle Scholar
Lindsay, D. S., Kelly, E. J., McKown, R. D., Stein, F. J., Plozer, J., Herman, J., Blagburn, B. L. and Dubey, J. P. ( 1996). Prevalence of Neospora caninum and Toxoplasma gondii antibodies in coyotes (Canis latrans) and experimental infection of coyotes with Neospora caninum. Journal of Parasitology 82, 657–659.CrossRefGoogle Scholar
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, 39–42.CrossRefGoogle Scholar
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 of Parasitology 28, 1473–1478.CrossRefGoogle Scholar
Morley, E. K., Williams, R. H., Hughes, J. M., Terry, R. S., Duncanson, P., Smith, R. S. and Hide, G. ( 2005). Significant familial differences in the frequency of abortion and Toxoplasma gondii infection within a flock of Charollais sheep. Parasitology 131, 181–185.CrossRefGoogle Scholar
Payne, S. and Ellis, J. ( 1996). Detection of Neospora caninum DNA by the polymerase chain reaction. International Journal for Parasitology 26, 347–351.CrossRefGoogle Scholar
Pereira-Bueno, J., Quintanilla-Gozalo, A., Perez-Perez, V., Espi-Felgueroso, A., Alvarez-Garcia, G., Collantes-Fernandez, E. and Ortega-Mora, L. M. ( 2002). Evaluation by different diagnostic techniques of bovine abortion associated with Neospora caninum in Spain. Veterinary Parasitology 111, 143–152.Google Scholar
Savva, D., Morris, J. C., Johnson, J. D. and Holliman, R. E. ( 1990). Polymerase chain reaction for detection of Toxoplasma gondii. Journal of Medical Microbiology 32 25–31.CrossRefGoogle Scholar
Speer, C. A., Dubey, J., McAllister, M. M. and Blixt, J. A. ( 1999). Comparative ultrastructure of tachyzoites, bradyzoites and tissue cysts of Neospora caninum and Toxoplasma gondii. International Journal for Parasitology 29, 1509–1519.CrossRefGoogle Scholar
Sundermann, C. A. and Estridge, B. H. ( 1999). Growth and competition between Neospora caninum and Toxoplasma gondii in vitro. International Journal for Parasitology 29, 1725–1732.CrossRefGoogle Scholar
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. ( 2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 1217–1258.CrossRefGoogle Scholar
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, 155–161.CrossRefGoogle Scholar
Wastling, J. M., Nicoll, S. and Buxton, D. ( 1993) Comparison of 2 gene Amplification methods for the detection of Toxoplasma gondii in experimentally infected sheep. Journal of Medical Microbiology 38, 360–365.CrossRefGoogle 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, 301–307.CrossRefGoogle Scholar
Yamage, M., Flechner, O. and Gottstein, B. ( 1996). Neospora caninum: specific oligonucleotide primers for the detection of brain “cyst” DNA of experimentally-infected nude mice by the polymerase chain reaction (PCR). Journal of Parasitology 82, 272–279.CrossRefGoogle Scholar