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Theileria parva: influence of vector, parasite and host relationships on the epidemiology of theileriosis in southern Africa

Published online by Cambridge University Press:  06 April 2009

R. A. I. Norval
Affiliation:
International Laboratory for Research on Animal Diseases, (ILRAD), P.O. Box 30709, Nairobi, Kenya
J. A. Lawrence
Affiliation:
P.O. Box 30750, Lilongwe 3, Malawi
A. S. Young
Affiliation:
Overseas Development Administration of U.K., Protozoology Division, National Veterinary Research Centre, Muguga, Kenya Agricultural Research Institute, P.O. Box 32, Kikuyu, Kenya
B. D. Perry
Affiliation:
International Laboratory for Research on Animal Diseases, (ILRAD), P.O. Box 30709, Nairobi, Kenya
T. T. Dolan
Affiliation:
International Laboratory for Research on Animal Diseases, (ILRAD), P.O. Box 30709, Nairobi, Kenya
J. Scott
Affiliation:
International Laboratory for Research on Animal Diseases, (ILRAD), P.O. Box 30709, Nairobi, Kenya

Extract

The protozoan parasite Theileria parva, transmitted by the ixodid tick Rhipicephalus appendiculatus, is the cause of East Coast fever (ECF) and the related syndromes of Corridor disease and January disease in cattle of eastern, central and southern Africa. It is likely that buffalo (Syncerus caffer) are the natural host of T. parva. In eastern and southern Africa, there exist both buffalo-adapted and cattle-adapted T. parva. Disease caused by buffalo-adapted parasites is called Corridor disease, and that caused by cattle-adapted parasites is termed East Coast fever. In eastern Africa, it has been shown experimentally that buffalo-adapted T. parva can, after serial passage in cattle, become adapted to cattle, in which it can then be maintained and cause ECF. This adaptation has been termed transformation. The transformation of buffalo-adapted T. parva to a cattle-adapted parasite has not been reported in southern Africa, and ECF, eradicated from South Africa, Swaziland and southern Mozambique by 1960, has not reappeared in the subcontinent. This paper discusses the possible reasons for this, and hypothesizes that vector population dynamics and the susceptibility of the vector population to infection with T. parva are among the most important factors which influence the expression of ECF as a disease entity, and the likelihood of transformation occurring. It also considers the possibility that disappearance of ECF from southern Africa resulted from the extinction, as a result of vigorous control measures and unfavourable climatic conditions, of non-diapausing populations of R. appendiculatus that may have been introduced from eastern Africa with cattle imported in 1901.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1991

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References

Anon (1974). Annual Report of the Department of Veterinary and Tsetse Control Services, 1972. Government of Zambia, Government Printer, Lusaka.Google Scholar
Anon (1981). The eradication of East Coast fever in South Africa. Journal of the South African Veterinary Association 52, 71–3.Google Scholar
Anon (1989). Nomenclature in Theileria. In Theileriosis in Eastern, Central and Southern Africa, (ed. Dolan, T. T.), pp. 182–6. Nairobi: International Laboratory for Research on Animal Disease.Google Scholar
Barnett, S. F. (1968). Theileriasis. In Infectious Blood Diseases of Man and Animals. Vol. 2. The Pathogens, the Infections, and the Consequences, (ed. Weinman, D. & Ristic, M.), pp. 269328. New York: Academic Press.Google Scholar
Barnett, S. F. & Brocklesby, D. W. (1966). The passage of ‘Theileria lawrencei (Kenya)’ through cattle. British Veterinary Journal 122, 396409.CrossRefGoogle Scholar
Barnett, S. F. & Brocklesby, D. W. (1969). Some piroplasms of wild mammals. In Diseases in Free living Wild Animals. Symposium of the Zoological Society of London 24, 147–69.Google Scholar
Berkvens, D. L., Geysen, D. M. & Lynen, G. M. (1989). East Coast fever immunization in the Eastern Province of Zambia. In Theileriosis in Eastern, Central and Southern Africa, (ed. Dolan, T. T.), pp. 83–6. Nairobi: International Laboratory for Research on Animal Diseases.Google Scholar
Blouin, E. C. F. & Stoltsz, W. H. (1989). Comparative infection rates of Theileria parva lawrencei in salivary glands of Rhipicephalus appendiculatus and Rhipicephalus zambeziensis. Onderstepoort Journal of Veterinary Research 54, 211–13.Google Scholar
Branagan, D. (1973 a). Observations on the development and survival of the ixodid tick Rhipicephalus appendiculatus Neumann 1901 under quasi-natural conditions in Kenya. Tropical Animal Health and Production 5, 153–65.CrossRefGoogle ScholarPubMed
Branagan, D. (1973 b). The feeding performance of the ixodid Rhipicephalus appendiculatus (Neumann) on rabbits, cattle and other hosts. Bulletin of Entomological Research 63, 387400.Google Scholar
Brocklesby, D. W. (1964). Parasites of the family Theileridae of the African buffalo occurring in East Africa. DVM thesis, University of Zurich.Google Scholar
Chizyuka, H. G. B. & Mangani, M. P. C. (1984). Theileriosis in Zambia. In Immunization against Theileriosis in Africa, (ed. Irvin, A. D.), pp. 41–7. Nairobi: International Laboratory for Research on Animal Diseases.Google Scholar
Conrad, P. A., Stagg, D. A., Grootenhuis, J. G., Irvin, A. D., Newson, J., Njamunggeh, R. E. G., Rossiter, P. B. & Young, A. S. (1987). Isolation of Theileria parasites from African buffalo (Syncerus caffer) and characterization with antischizont monoclonal antibodies. Parasitology 94, 413–24.CrossRefGoogle ScholarPubMed
Conrad, P. A., Ole-Moiyoi, O. K., Baldwin, C. L., Dolan, T. T., O'Callaghan, C. J., Njamunggeh, R. E. G., Grootenhuis, J. G., Stagg, P. A., Leitch, B. L. & Young, A. S (1989). Characterization of buffalo-derived theilerial parasites with monoclonal antibodies and DNA probes. Parasitology 98, 179–88.CrossRefGoogle ScholarPubMed
De Vos, A. J. (1982). The identity of bovine Theileria spp. in South Africa. M. Med. Vet. thesis, University of Pretoria.Google Scholar
Diesel, A. M. (1948). The campaign against East Coast fever in South Africa. Onderstepoort Journal of Veterinary Science and Animal Industry 23, 1931.Google ScholarPubMed
Dolan, T. T. (1986 a). Chemotherapy of East Coast fever. The long term weight changes, carrier state and disease manifestations of parvaquone treated cattle. Journal of Comparative Pathology 96, 137–46.CrossRefGoogle Scholar
Dolan, T. T. (1986 b). Chemotherapy of East Coast fever. Treatment of infections induced by isolates of Theileria parva with halofuginone. Acta Tropica 43, 165–73.Google ScholarPubMed
Du Toit, P. J. (1931). Immunity in East Coast fever. 17th Report of the Director of Veterinary Services and Animal Industries, Pretoria, pp. 325.Google Scholar
Grootenhuis, J. G. (1989). The role of wildlife in the epidemiology of Theileriosis. In Theileriosis in Eastern, Central and Southern Africa, (ed. Dolan, T. T.), pp. 129–36. Nairobi: International Laboratory for Research on Animal Diseases.Google Scholar
Grootenhuis, J. G., Young, A. S., Stagg, D. A., Leitch, B. L., Dolan, T. T. & Conrad, P. A. (1987 a). Infection of African buffalo (Syncerus caffer) and cattle with Theileria parva lawrencei after serial passage in cattle. Research in Veterinary Science 42, 326–30.CrossRefGoogle ScholarPubMed
Henning, M. W. (1956). Animal Diseases in South Africa. Cape Town, Central News Agency Ltd.Google Scholar
Howell, C. J., De Vos, A. J., Bezuidenhout, J. D., Potgeiter, F. T. & Barrowman, P. R. (1981). The role of chemical tick eradication in the control or prevention of tick transmitted disease in cattle. In Tick Biology and Control, (ed. Whitehead, G. B. & Gibson, J. D.), pp. 61–6. Grahamstown: Rhodes University.Google Scholar
Irvin, A. D., Morzaria, S. P., Munatswa, F. C. & Norval, R. A. I. (1989). Immunization of cattle with a Theileria parva bovis stock from Zimbabwe protects against challenge with virulent T. p. parva and T. p. lawrencei stocks from Kenya. Veterinary Parasitology 32, 271–8.CrossRefGoogle Scholar
Kubasu, S. S. (1990). Biological diversity of stocks of Rhipicephalus appendiculatus in relationship to transmission of East Coast fever. M.Sc. thesis, University of Nairobi.Google Scholar
King, D., Gettinby, G. & Newson, R. M. (1988). A climate-based model for the development of the ixodid tick, Rhipicephalus appendiculatus in East Coast fever zones. Veterinary Parasitology 29, 4151.CrossRefGoogle ScholarPubMed
Koch, R. (1903). On Rhodesian red water or African Coast fever. Journal of Comparative Pathology and Therapeutics 16, 273.Google Scholar
Koch, H. T., Norval, R. A. I., Ocama, J. G. R. & Munatswa, F. C. (1991). Transmission of Theileria parva bovis by nymphs of the tick Rhipicephalus appendiculatus. Preventive Veterinary Medicine (in the Press).Google Scholar
Lawrence, D. A. (1938). Report of the Director of Veterinary Research for the Year 1937. Salisbury: South Rhodesia.Google Scholar
Lawrence, J. A. (1979). The differential diagnosis of the bovine theilerias of southern Africa. Journal of the South African Veterinary Association 50, 311–13.Google ScholarPubMed
Lawrence, J. A. (1991 a). The history of bovine theileriosis in southern Africa. In The Epidemiology of Theileriosis in Africa, (Norval, R. A. I., Perry, B. D. & Young, A. S.). London: Academic Press, (in the Press).Google Scholar
Lawrence, J. A. (1991 b). Retrospective observations on the transmission of East Coast fever in Zimbabwe. Tropical Animal Health and Production (in the Press).CrossRefGoogle ScholarPubMed
Lawrence, J. A. & Norval, R. A. I. (1979). A history of ticks and tick-borne diseases of cattle in Rhodesia. Rhodesia Veterinary Journal 10, 2840.Google Scholar
Lawrence, J. A., Norval, R. A. I. & Uilenberg, G. (1983). Rhipicephalus zambeziensis as a vector of bovine Theileridae. Tropical Animal Health and Production 15, 3942.CrossRefGoogle Scholar
Lessard, P., L'Eplattenier, R., Norval, R. A. I., Kundert, K., Dolan, T. T., Croze, H., Walker, J. B., Irvin, A. D. & Perry, B. D. (1990). Geographical information systems for studying the epidemiology of cattle diseases caused by Theileria parva. Veterinary Record 126, 255–62.Google ScholarPubMed
Lewis, E. A. & Fotheringham, W. (1941). The transmission of Theileria parva by ticks. Parasitology 33, 251–7.CrossRefGoogle Scholar
Lounsbury, C. P. (1904). Transmission of African Coast fever. Agricultural Journal of the Cape of Good Hope 24, 428–32.Google Scholar
Maritim, A. C., Young, A. S., Lesan, A. C., Ndungu, S. G., Mutugi, J. J. & Stagg, D. A. (1989 a). Theilerial parasites isolated from carrier cattle after immunization with Theileria parva by the infection and treatment method. Parasitology 99, 139–47.Google ScholarPubMed
Maritim, A. C., Karikuki, D. P., Young, A. S. & Mutugi, J. J. (1989 b). The importance of the carrier state of Theileria parva in the epidemiology of theileriosis and its control by immunization. In Theileriosis in Eastern, Central and Southern Africa, (ed. Dolan, T. T.), pp. 121–8. Nairobi: International Laboratory for Research on Animal Diseases.Google Scholar
Matson, B. A. (1967). Theileriosis in Rhodesia: 1. A study of diagnostic specimens over two seasons. Journal of the South African Veterinary Medical Association 38, 93102.Google Scholar
Moll, G., Lohding, A. & Young, A. S. (1984). Epidemiology of theileriosis in the Trans-mara Division, Kenya. Husbandry and disease background and preliminary observation on theileriosis in calves. Preventive Veterinary Medicine 2, 801–31.CrossRefGoogle Scholar
Moll, G., Lohding, A., Young, A. S. & Leitch, B. L. (1986). Epidemiology of theileriosis in calves in an endemic area of Kenya. Veterinary Parasitology 19, 255–73.CrossRefGoogle Scholar
Mutugi, J. J., Young, A. S., Maritim, A. C., Linyonyi, A., Mbogo, S. K. & Leitch, B. L. (1988 a). Immunization of cattle using varying infective doses of Theileria parva lawrencei sporozoites derived from an African buffalo (Syncerus caffer) and treatment with bupavaquone. Parasitology 96, 391402.CrossRefGoogle Scholar
Mutugi, J. J., Young, A. S., Maritim, A. C., Ndungu, S. G., Stagg, D. A., Grootenhuis, J. G. & Leitch, B. L. (1988 b). Immunization of cattle against theileriosis using varying doses of Theileria parva lawrencei and T. parva parva sporozoites and oxytetracycline treatment. International Journal for Parasitology 18, 453–61.CrossRefGoogle Scholar
Neitz, W. O. (1955). Corridor disease: a fatal form of bovine theileriosis encountered in Zululand. Bulletin of Epizootic Diseases of Africa 3, 121–3.Google Scholar
Neitz, W. O. (1957). Theileriosis, gonderioses and cytauxzoonoses: a review. Onderstepoort Journal of Veterinary Research 27, 275430.Google Scholar
Neitz, W. O. (1958). Can Corridor disease-recovered cattle serve as reservoirs of Gonderia lawrencei? Bulletin of Epizootic Diseases of Africa 6, 151–4.Google Scholar
Newson, R. M., Chiera, J. W., Young, A. S., Dolan, T. T., Cunningham, M. P. & Radley, D. E. (1984). Survival of Rhipicephalus appendiculatus (Acarina: Ixodidae) and persistence of Theileria parva (Apicomplexa: Theileriidae) in the field. International Journal for Parasitology 14, 483–9.CrossRefGoogle ScholarPubMed
Norval, R. A. I., Walker, J. B. & Colborne, J. (1982). The ecology of Rhipicephalus zambeziensis and Rhipicephalus appendiculatus (Acarina, Ixodidae) with particular reference to Zimbabwe. Onderstepoort Journal of Veterinary Research 49, 181–90.Google ScholarPubMed
Norval, R. A. I., Fivaz, B. H., Lawrence, J. A. & Brown, A. F. (1985). Epidemiology of tick-borne diseases of cattle in Zimbabwe. III. Theileria parva group. Tropical Animal Health and Production 17, 1928.CrossRefGoogle ScholarPubMed
Norval, R. A. I. & Perry, B. D. (1990). The introduction, spread and subsequent disappearance of the brown ear tick Rhipicephalus appendiculatus from the southern lowveld of Zimbabwe. Experimental and Applied Acarology 9, 103–11.CrossRefGoogle ScholarPubMed
Norval, R. A. I., Perry, B. D. & Young, A. S. (1991). The Epidemiology of Theileriosis in Africa. London: Academic Press, (in the Press).Google Scholar
Pegram, R. G., Perry, B. D., Musisi, F. L. & Mwanaumo, B. (1986). Ecology and phenology of ticks in Zambia: Seasonal dynamics on cattle. Experimental and Applied Acarology 2, 2545.CrossRefGoogle ScholarPubMed
Perry, B. D., Lessard, P., Norval, R. A. I., Kundert, K. & Kruska, R. (1990). The effect of climate and vegetation on the distribution of Rhicephalus appendiculatus in Africa. Parasitology Today 6, 100–4.CrossRefGoogle Scholar
Potgeiter, F. T., Stoltsz, W. H., Blouin, E. F. & Roos, J. A. (1988). Corridor disease in South Africa: A review of the current status. Journal of the South African Veterinary Association 59, 155–60.Google Scholar
Purnell, R. E., Young, A. S., Brown, C. G. D., Burridge, M. J. & Payne, R. C. (1974). Comparative infectivity for cattle of stabilates of Theileria lawrencei (Serengeti) derived from adult and nymphal ticks. Journal of Comparative Pathology 84, 533–7.CrossRefGoogle ScholarPubMed
Rechav, Y. (1981). Ecological factors affecting the seasonal activity of the brown ear tick Rhipicephalus appendiculatus. In Tick Biology and Control (ed. Whitehead, G. B. & Gibson, J. D.), pp. 187–91. Grahamstown: Rhodes University.Google Scholar
Rechav, Y. (1982). Dynamics of tick populations (Acari: Ixodidae) in the Eastern Cape Province of South Africa. Journal of Medical Entomology 19, 679700.CrossRefGoogle Scholar
Short, N. J., Floyd, R. B., Norval, R. A. I. & Sutherst, R. W. (1989). Survival and behaviour of unfed stages of the ticks Rhipicephalus appendiculatus, Boophilus decoloratus and B. microplus under field conditions in Zimbabwe. Experimental and Applied Acarology 6, 215–36.CrossRefGoogle Scholar
Short, N. J. & Norval, R. A. I. (1981 a). The seasonal activity of Rhipicephalus appendiculatus Neumann 1901 (Acarina: Ixodidae) in the highveld of Zimbabwe Rhodesia. Journal of Parasitology 67, 7784.CrossRefGoogle ScholarPubMed
Short, N. J. & Norval, R. A. I. (1981 b). Regulation of seasonal occurrence in the tick Rhipicephalus appendiculatus Neumann (1901). Tropical Animal Health and Production 13, 1926.CrossRefGoogle ScholarPubMed
Sutherst, R. W. & Maywald, G. F. (1985). A computerised system for matching climates in ecology. Agriculture Ecosystems and Environment 13, 281–99.CrossRefGoogle Scholar
Theiler, A. (1904). Rhodesian tick fever. Transvaal Agricultural Journal 2, 421–38.Google Scholar
Uilenberg, G. (1976). Tick-borne livestock diseases and their vectors. 2. Epizootiology of tick-borne diseases. World Animal Review 17, 815.Google Scholar
Uilenberg, G. (1981). Theilerial species of livestock. In Advances in the Control of Theileriosis, (ed. Irvin, A. D., Cunningham, M. P. & Young, A. S.), pp. 437. The Hague: Martinus Nijhoff Publishers.CrossRefGoogle Scholar
Young, A. S. (1981). The epidemiology of theileriosis in East Africa. In Advances in the Control of Theileriosis, (ed. Irvin, A. D., Cunningham, M. P. & Young, A. S.), pp. 3855. The Hague: Martinus Nijhoff Publishers.CrossRefGoogle Scholar
Young, A. S., Branagan, D., Brown, C. G. D., Burridge, M. J., Cunningham, M. P. & Purnell, R. E. (1973). Preliminary observations on a theilerial species pathogenic to cattle isolated from buffalo (Syncerus caffer) in Tanzania. British Veterinary Journal 129, 382–9.CrossRefGoogle ScholarPubMed
Young, A. S., Brown, C. G. D., Burridge, M. J., Grootenhuis, J. G., Kanhai, G. K., Purnell, R. E. & Stagg, D. A. (1978). The incidence of theilerial parasites in East African buffalo (Syncerus caffer). Tropenmedizin und Parasitologie 29, 281–8.Google ScholarPubMed
Young, A. S. & Grootenhuis, J. G. (1985). The influence of wildlife on immunization of cattle against theileriosis. 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., Leitch, B. L., Dolan, T. T., Newson, R. M., Ngumi, P. N. & Omwoyo, P. L. (1983). Transmission of Theileria parva by Rhipicephalus appendiculatus under simulated natural conditions. Parasitology 86, 255–68.CrossRefGoogle ScholarPubMed
Young, A. S., Leitch, B. L., Morzaria, S. P., Irvin, A. D., Omwoyo, P. L. & De Castro, J. J. (1987). Development and survival of Theileria parva parva in Rhipicephalus appendiculatus exposed in the Trans-Mara, Kenya. Parasitology 94, 433–41.CrossRefGoogle ScholarPubMed
Young, A. S., Leitch, B. L. & Newson, R. M. (1981). The occurrence of a Theileria parva carrier state in cattle from an East Coast fever endemic area of Kenya. In Advances in the Control of Theileriosis, (ed. Irvin, A. D., Cunningham, M. P. & Young, A. S.), pp. 60–2. The Hague: Martinus Nijhoff Publishers.CrossRefGoogle Scholar
Young, A. S., Leitch, B. L., Newson, R. M. & Cunningham, M. P. (1986). Maintenance of Theileria parva parva infection in an endemic area of Kenya. Parasitology 93, 916.CrossRefGoogle Scholar
Young, A. S. & Purnell, R. E. (1973). Transmission of Theileria lawrencei (Serengeti) by the ixodid tick, Rhipicephalus appendiculatus. Tropical Animal Health and Production 5, 146–52.CrossRefGoogle ScholarPubMed