Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-18T01:26:25.650Z Has data issue: false hasContentIssue false

Characterization of Theileria parva which infects waterbuck (Kobus defassa)

Published online by Cambridge University Press:  06 April 2009

D. A. Stagg
Affiliation:
National Veterinary Research Centre, Muguga, Kenya Agricultural Research Institute, P.O. Box 32, Kikuyu, Kenya
R. P. Bishop
Affiliation:
International Laboratory for Research on Animal Diseases, P.O. Box 30709, Nairobi, Kenya
S. P. Morzaria
Affiliation:
International Laboratory for Research on Animal Diseases, P.O. Box 30709, Nairobi, Kenya
M. K. Shaw
Affiliation:
International Laboratory for Research on Animal Diseases, P.O. Box 30709, Nairobi, Kenya
D. Wesonga
Affiliation:
Wildlife Disease Section, Veterinary Research Centre, Kenya Agricultural Research Institute, P.O. Kabete, Kenya
G. O. Orinda
Affiliation:
Wildlife Disease Section, Veterinary Research Centre, Kenya Agricultural Research Institute, P.O. Kabete, Kenya
J. G. Grootenhuis
Affiliation:
Wildlife Disease Section, Veterinary Research Centre, Kenya Agricultural Research Institute, P.O. Kabete, Kenya
D. H. Molyneux
Affiliation:
Department of Biological Sciences, Salford University, UK
A. S. Young
Affiliation:
National Veterinary Research Centre, Muguga, Kenya Agricultural Research Institute, P.O. Box 32, Kikuyu, Kenya International Laboratory for Research on Animal Diseases, P.O. Box 30709, Nairobi, Kenya

Summary

Theileria-free waterbuck (Kobus defassa) born in captivity were successfully infected with Theileria parva sporozoites derived from ticks infected by feeding on African buffalo (Syncerus caffer). All waterbuck underwent mild infections with the development of sporadic schizont and piroplasm parasitosis when inoculated with sporozoite doses lethal to cattle. A carrier state of T. parva was demonstrated by feeding clean R. appendiculatus nymphs on two of these infected waterbuck. Tick batches from these waterbuck on 2 of 5 occasions transmitted lethal Theileria infections to cattle. In a separate experiment, waterbuck cells were infected and transformed in vitro by T. parva sporozoites derived from buffalo but not by cattle-derived T. parva (Muguga) sporozoites. Waterbuck cells infected in vitro with T. parva isolated from buffalo were inoculated into autologous waterbuck but no infections developed. Theileria parva isolates generated in this study from various sources were characterized using anti-T. parva schizont monoclonal antibodies (MAbs), and it was found that buffalo-derived and waterbuck-passaged isolates had different profiles. Species-specific synthetic oligonucleotide probes, restriction fragment length polymorphism (RFLP) analysis with cloned T. parva DNA probes, and DNA sequence analysis of the p67 sporozoite antigen gene confirmed that the waterbuck-passaged parasite was T. parva. The Tpr repetitive probe hybridization patterns from the waterbuck-passaged parasites were different from the other samples tested. The ribosomal genotype of the waterbuck-passaged T. parva was similar to that of cattle-derived T. parva Muguga. Analyses with both probes and MAbs suggested that a minor parasite population present within the T. parva 7014 buffalo- derived stock had been selected during waterbuck passage. A variable region of the p67 sporozoite antigen gene of the waterbuck-passaged T. parva was similar to that of cattle-derived T. parva stocks and different from that of buffalo- derived parasites. Based on these results, methods were suggested to confirm and quantitate the involvement of waterbuck in the epidemiology of cattle theileriosis.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1994

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

Allsopp, B. A. & Allsopp, M. T. E. P. (1988). Theileria parva: genomic DNA studies reveal intra-specific diversity. Molecular and Biochemical Parasitology 28, 7784.CrossRefGoogle Scholar
Allsopp, B. A., Baylis, H. A., Allsopp, M. T. E. P., Cavalier-Smith, T., Bishop, R. P., Carrington, D. M., Sohanpal, B. K. & Spooner, P. R. (1993). Discrimination between six species of Theileria using oligonucleotide probes which detect small ribosomal RNA sequences. Parasitology 107, 157–65.CrossRefGoogle ScholarPubMed
Bailey, K. P. (1960). Notes on the rearing of Rhipicephalus appendiculatus and their infection with Theileria parva for experimental transmission. Bulletin of Epizootic Diseases of Africa 8, 3343.Google Scholar
Bishop, R. P., Sohanpal, B. K., Allsopp, B. A., Spooner, P. R., Dolan, T. T. & Morzaria, S. P. (1993). Detection of polymorphisms among Theileria parva stocks using repetitive, telomeric and ribosomal DNA probes and anti-schizont monoclonal antibodies. Parasitology 107, 1931.CrossRefGoogle ScholarPubMed
Bishop, R. P., Sohanpal, B. K., Kariuki, O. P., Young, A. S., Nene, V., Baylis, H., Allsopp, B. A., Spooner, P. R., Dolan, T. T. & Morzaria, S. P. (1992). Detection of a carrier state in Theileria parva infected cattle using the polymerase chain reaction. Parasitology 104, 215–32.CrossRefGoogle ScholarPubMed
Brocklesby, D. W. (1962). Cytauxzoon taurotragi Martin & Brocklesby, 1960, a piroplasm of eland (Taurotragus oryx pattersonianus Lydekker, 1906). Research in Veterinary Science 3, 334–44.CrossRefGoogle Scholar
Brown, C. G. D., Stagg, D. A., Purnell, R. E., Kanhai, G. K. & Payne, R. C. (1973). Infection and transformation of bovine lymphoid cells in vitro by infective particles of Theileria parva. Nature, London 245, 101.CrossRefGoogle ScholarPubMed
Burridge, M. J. & Kimber, C. D. (1972). The indirect fluorescent antibody test for experimental East Coast fever (Theileria parva infection in cattle): evaluation of a cell culture schizont antigen. Research in Veterinary Science 13, 451–5.CrossRefGoogle ScholarPubMed
Conrad, P. A., Ole-Moiyoi, O. K., Baldwin, C. L., Dolan, T. T., O'callaghan, C. J., Njammungeh, R. E. G., Grootenhuis, J. G., Stagg, D. A., Leitch, B. L. & Young, A. S. (1989). Characterization of buffalo-derived theilerial parasites with monoclonal antibodies and DNA probes. Parasitology 98, 179–98.CrossRefGoogle ScholarPubMed
Corbet, G. B. & Hill, J. E. (1991). A World List of Mammalian Species, 3rd Edn.London and Oxford: Natural History Museum and Oxford University Press.Google Scholar
Dolan, T. T., Young, A. S., Losos, G. J., McMillan, I., Minder, C. E. & Soulsby, K. (1984). Dose dependent response of cattle to Theileria parva stabilate inoculation. International Journal for Parasitology 14, 8995.CrossRefGoogle Scholar
Fawcett, D. W., Conrad, P. A., Grootenhuis, J. G. & Morzaria, S. P. (1987). Ultrastructure of the intraerythrocytic stage of Theileria species from cattle and waterbuck. Tissue and Cell 19, 643–55.CrossRefGoogle ScholarPubMed
Hulliger, L., Wilde, J. K. H., Brown, C. G. D. & Turner, L. (1964). Mode of multiplication of Theileria in cultures of bovine lymphocytic cells. Nature, London 203, 728–30.CrossRefGoogle ScholarPubMed
Ibrahim, K. M. & Kabuye, C. H. S. (1988). An Illustrated Manual of Kenya Grasses. Rome: Food and Agriculture Organization of the United Nations.Google Scholar
Malmquist, W. A., Nyindo, M. B. A. & Brown, C. G. D. (1970). East Coast fever: cultivation in vitro of bovine spleen cell lines infected and transformed by Theileria parva. Tropical Animal Health and Production 2, 139–45.CrossRefGoogle Scholar
Maritim, A. C., Young, A. S., Lesan, A. C., Nduncu, S. G., Stagg, D. A. & Ncumi, P. N. (1992). Transformation of Theileria parva derived from African buffalo (Syncerus caffer) by tick passage in cattle and its use in infection and treatment immunization. Veterinary Parasitology 43, 1524.CrossRefGoogle ScholarPubMed
Mason, J. L. & Maule, J. P. (1960). The Indigenous Livestock of Eastern and Southern Africa. Farnham Royal, Slough: Commonwealth Agricultural Bureaux.Google Scholar
McCosker, P. J. (1992). Foreword. In The Epidemiology of Theileriosis in Africa (ed. Norval, R. A. I., Perry, B. D. & Young, A. S.). London: Academic Press.Google Scholar
Morrison, W. I., Büscher, G., Emery, D. L., Nelson, R. T. & Murray, M. (1981). The kinetics of infection with Theileria parva in cattle and the relevance of the development of immunity. In Advances in the Control of Theileriosis (ed. Irvin, A. D., Cunningham, M. P. & Young, A. S.), pp. 311–26. The Hague: Martinus Nijhoff.CrossRefGoogle Scholar
Morzaria, S., Spooner, P., Gobright, E. & Nene, V. (1992). Characterization of cattle and buffalo-derived Theileria parva sporozoite stabilates using p67 primers as markers. In Annual Scientific Report, p. 5. Nairobi: International Laboratory for Research on Animal Diseases.Google Scholar
Mukhebi, A. W., Perry, B. D. & Kruska, R. (1992). Estimated economics of theileriosis control in Africa. Preventive Veterinary Medicine 12, 7385.CrossRefGoogle Scholar
Neitz, W. O. (1957). Theileriosis, gonderioses and cytauxzoonoses: a review. Onderstepoort Journal of Veterinary Research 27, 275430.Google Scholar
Nene, V., Iams, K. P., Gobright, E. & Musoke, A. J. (1992). Characterization of the gene encoding a candidate vaccine antigen of Theileria parva sporozoites. Molecular and Biochemical Parasitology 51, 1727.CrossRefGoogle ScholarPubMed
Norval, R. A. I., Perry, B. D. & Young, A. S. (1992). The Epidemiology of Theileriosis in Africa. London: Academic Press.Google Scholar
Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd Edn.New York: Cold Spring Harbor Laboratory.Google Scholar
Shaw, M. K., Tilney, L. G. & Musoke, A. J. (1991). The entry of Theileria parva sporozoites in to bovine lymphocytes: evidence for MHC class I involvement. Journal of Cell Biology 113, 87101.CrossRefGoogle ScholarPubMed
Stagg, D. A. (1992). Studies of theilerial parasites of waterbuck (Kobus defassa) and their possible role in the epidemiology of East Coast fever. Ph.D. thesis, University of Salford.Google Scholar
Stagg, D. A., Dolan, T. T., Leitch, B. L. & Young, A. S. (1981). The initial stages of infection of cattle cells with Theileria parva sporozoites in vitro. Parasitology 83, 191–7.CrossRefGoogle ScholarPubMed
Stagg, D. A., Kanhai, G. K., Young, A. S. & Brown, C. G. D. (1976). The establishment of Theileria infected cell lines from an eland (Taurotragus oryx Lydekker, 1906). Research in Veterinary Science 20, 122–6.CrossRefGoogle ScholarPubMed
Stagg, D. A., Young, A. S., Leitch, B. L., Grootenhuis, J. G. & Dolan, T. T. (1983). Infection of mammalian cells with Theileria species. Parasitology 86, 243–54.CrossRefGoogle ScholarPubMed
Walker, J. B. (1974). The Ixodid Ticks of Kenya. London: Commonwealth Institute of Entomology.Google Scholar
Young, A. S., Brown, C. G. D., Burridge, M. J., Cunningham, M. P., Payne, R. C. & Purnell, R. E. (1977 a). Establishment of an experimental field population of Theileria lawrencei infected ticks maintained by Africa buffalo (Syncerus caffer). Journal of Parasitology 65, 903–7.CrossRefGoogle Scholar
Young, A. S., Groocock, C. M. & Kariuki, D. P. (1988). Integrated control of tick and tick-borne diseases in Africa. Parasitology 96, 403–32.CrossRefGoogle ScholarPubMed
Young, A. S. & Grootenhuis, J. G. (1985). Influence of wildlife on immunization of cattle against theileriosis in East Africa. In Immunization Against Theileriosis in Africa (ed. Irvin, A. D.), pp. 104–9. Nairobi: International Laboratory for Research on Animal Diseases.Google Scholar
Young, A. S., Grootenhuis, J. G., Kimber, C. D., Kanhai, G. K. & Stagg, D. A. (1977 b). Isolation of a Theileria species from eland (Taurotragus oryx) infective for cattle. Tropenmedizin und Parasitologie 27, 185–94.Google Scholar
Young, A. S. & Leitch, B. L. (1981). Epidemiology of East Coast fever: some effects of temperature on the development of Theileria parva in the tick vector, Rhipicephalus appendiculatus. Parasitology 81, 199211.CrossRefGoogle Scholar
Young, A. S., Mutugi, J. J., Kariuki, D. P., Lampard, D., Maritim, A. C., Ngumi, P. N., Linyonyi, A., Leitch, B. L., Ndungu, S. G., Lesan, A. C., Mining, S. K., Grootenhuis, J. G., Orinda, G. O. & Wesonga, D. (1992). Immunization of cattle against theileriosis in Nakuru District of Kenya by infection and treatment and introduction of unconventional tick control. Veterinary Parasitology 42, 225–40.CrossRefGoogle ScholarPubMed
Young, A. S. & Newson, R. M. (1973). An improved method of handling ticks collected in the field. Research in Veterinary Science 15, 133–5.CrossRefGoogle Scholar