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A model of tsetse-transmitted animal trypanosomiasis

Published online by Cambridge University Press:  06 April 2009

P. J. M. Milligan
Affiliation:
Department of Biological Sciences, University of Salford, Salford M5 4WT
R. D. Baker
Affiliation:
Computing Services Section, Computing Laboratory, University of Salford, Salford M5 4WT

Summary

The data needed to develop analytical models of trypanosomiasis transmission have become available only recently. By making some simplifying assumptions, models of the dynamics of the disease in vector, cattle and wild mammal populations can be constructed in order to determine criteria for successful disease control by mass and targetted chemotherapy, and by vector control. The heterogeneity in transmission due to tsetse fly feeding preferences and the variability of immunological characteristics among the vertebrate hosts account for differences in prevalence of Trypanosoma vivax and T. congolense, and also lead to an increase in the basic reproductive rates of the parasites and a corresponding decrease in the vector population density threshold for disease eradication or persistence. The long life-span of the vectors relative to the duration of the parasites' developmental period lead to high infection rates in the vector and high values of R0. The efficacy of chemotherapeutic regimes depends on the relationship between treatment rate and the duration of prophylaxis conferred by the drugs used. The model's predictions of the effects of vector control are shown to be in broad agreement with published field data for Mkwaja Ranch, Tanzania. Vector control programmes are frequently blighted by reinvasion, and the implications of this are discussed in terms of a model for fly immigration. With immigration of vectors, the disease is always endemic, though the infection rate in the fly population is modified by the effect of differential mortalities inside and outside the controlled area on cohorts of incubating flies. Sensitivity analysis of the model, using Monte-Carlo methods, enables an assessment of the relative importance of the parameters to be made. The results emphasize the need for studies of the wild animal reservoir to be carried out alongside entomological surveys. The relative accuracy with which field measurements need to be made in order to minimize the uncertainty in predictions of trypanosomiasis prevalence is discussed.

Type
Trends and Perspectives
Copyright
Copyright © Cambridge University Press 1988

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References

REFERENCES

Adelheim, R. & Bruckle, F. (1983). Trypanosomiasis control – aspects of project work. In Beiträge: Zur Evaluierung von Vorhaben der Tsetsehekämpfung. GTZ-IEMUT 1083. GTZ, D6236, Eschborn 1, West Germany.Google Scholar
Allsopp, R. (1972). The role of game animals in the maintenance of endemic and enzootic trypanosomiases in the Lambwe Valley, South Nyanza District, Kenya. Bulletin of the World Health Organization 47, 735–46.Google ScholarPubMed
Anderson, R. M. (1981). Population dynamics of indirectly transmitted disease agents: the vector component. In Vectors of Disease Agents: Interactions with Plants, Animals and Man (ed. McKelvey, J., Eldridge, B. and Maramorosch, K.), pp. 1343. New York: Praeger.Google Scholar
Aron, J. L. & May, R. M. (1980). The population dynamics of malaria. In The Population Dynamics of Infectious Diseases (ed. Anderson, R. M.), pp. 138179. London: Chapman and Hall.Google Scholar
Ashcroft, M. T., Burtt, E. & Fairbairn, H. (1959). The experimental infection of some African wild animals with Trypanosoma rhodesiense, T. brucei and T. congolense. Annals of Tropical Medicine and Parasitology 53, 147–147.CrossRefGoogle ScholarPubMed
Bakuli, B., Gates, D. B., Cobb, P. E. & Williamson, D. L. (1981). Integration of insect sterility and insecticides for control of Glossina morsitans morsitans Westw. in Tanzania (Diptera, Glossinidae). III. Test site characteristics and the natural distribution of tsetse flies. In The 17th Meeting of ISCTRC, Arusha, Tanzania, pp. 643649. Nairobi, Kenya: OAU/STRC.Google Scholar
Baldry, D. A. T. (1970). Observations on the peridomestic breeding behaviour and resting sites of Glossina tachinoides Westwood, near Nsukka, East Central State, Nigeria. Bulletin of Entomological Research 59, 585–93.CrossRefGoogle Scholar
Baldry, D. A. T., Taze, Y. & Bushrod, F. M. (1981). Preliminary observations on the feeding habits of Glossina morsitans centralis Machdo in Mwumbwa District, Zambia. In The 17th Meeting of ISCTRC, Arusha, Tanzania, pp. 419422. Nairobi, Kenya: OAU/STRC.Google Scholar
Barry, J. D. (1988). Antigenic variation during Trypanosoma vivax infections of different host species. Parasitology 92, 5165.CrossRefGoogle Scholar
Bushrod, F. M. & Evison, C. (1981). The value of game exclusion measures in the control of Glossina morsitans centralis in Zambia. In The 17th Meeting of ISCTRC, Arusha, Tanzania, pp. 637642. Nairobi, Kenya: OAU/STRC.Google Scholar
Clifford, D. (1980). Aspects of research on trypanosomiasis in The Gambia. In Report of the Expert Consultation on Research on Trypanosomiases, Rome, 1–5 10 1979, AGA-801 (1979), pp. 6869. Rome: FAO.Google Scholar
Clifford, D. J. & Sanyang, B. (1977). An epidemiological study of trypanosomiasis in N'dama cattle in The Gambia. In The 15th Meeting of ISCTRC, Banjul, The Gambia, pp. 152154. Nairobi, Kenya: OAU/STRC.Google Scholar
Dillman, J. S. S. & Townsend, A. J. (1979). A trypanosomiasis survey of wild animals in the Luangwa Valley, Zambia. Acta Tropica 36, 349–56.Google Scholar
Drager, N. & Mehlitz, D. (1978). Investigations on the prevalence of trypanosome carriers and the antibody response in wildlife in Northern Botswana. Tropenmedizin und Parasiiologie 29, 223–33.Google ScholarPubMed
England, E. C. & Baldry, D. A. T. (1972). The hosts and trypanosome infection rates of Glossina pallidipes in the Lambwe and Roo Valleys. Bulletin of the World Health Organization 47, 785–8.Google ScholarPubMed
Gates, D. B., Cobb, P. E., Williamson, D. L., Bakuli, B., Blaser, E. & Dame, D. A. (1983). Integration of insect sterility and insecticide for control of Glossina morsitans morsilans Westwood (Diptera: Glossinidae) in Tanzania. III. Test site characteristics and the natural distribution of tsetse flies. Bulletin of Entomological Research 73, 373–81.CrossRefGoogle Scholar
Golder, T. K., Otieno, L. H., Patel, N. Y. & Onyango, P. (1982). Increased sensitivity to endosulfan of Trypanosoma-infected Glossina morsitans. Annals of Tropical Medicine and Parasitology 76, 483–483.CrossRefGoogle ScholarPubMed
Gray, A. R. & Roberts, C. J. (1971). The cyclical transmission of strains of Trypanosoma congolense and T. vivax resistant to normal therapeutic doses of trypanocidal drugs. Parasitology 63, 6789.CrossRefGoogle Scholar
Hoare, C. A. (1967). Evolutionary trends in mammalian trypanosomes. In Advances in Parasitology, vol. 5 (ed. Dawes, B.), pp. 4791. London and New York: Academic Press.Google Scholar
Jenni, L., Molyneux, D. H., Livesey, J. L. & Galun, R. (1980). Feeding behaviour of tsetse flies infected with salivarian trypanosomes. Nature, London 283, 383–5.CrossRefGoogle ScholarPubMed
Jordan, A. M. (1974). Recent developments in the ecology and methods for control of tsetse flies (Glossina spp.) (Dipt., Glossinidae) – a review. Bulletin of Entomological Research 63, 361–99.CrossRefGoogle Scholar
Killick-Kendrick, R. & Godfrey, D. G. (1983). Bovine trypanosomiasis in Nigeria. II. The incidence among some migrating cattle, with observations on the examination of wet blood preparations as a method of survey. Annals of Tropical Medicine and Parasitology 57, 117.CrossRefGoogle Scholar
MacLennan, K. J. R. (1970). The epizootiology of trypansomiasis in livestock in West Africa. In The African Trypanosomiases (ed. Mulligan, H. W. and Potts, W. H.), pp. 751765. London: ODA/Allen and Unwin.Google Scholar
Mehlitz, D. (1981). Trypanosomes in African wild mammals. In Perspectives in Trypanosomiasis Research, Proceedings of the 21st Trypanosomiasis Seminar, London, 24 09 1981 (ed. Baker, J. R.), pp. 2535. London: Research Studies Press.Google Scholar
Moloo, S. K. (1982). Feeding behaviour of Glossina morsitans morsitans infected with Trypanosoma vivax, T. congolense or T. brucei. Parasitology 86, 51–6.CrossRefGoogle Scholar
Molyneux, D. H. & Jenni, L. (1981). Mechanoreceptors, feeding behaviour and trypanosome transmission in Glossina. Transactions of the Royal Society for Tropical Medicine and Hygiene 75, 160–2.CrossRefGoogle ScholarPubMed
Molyneux, D. H., Lavin, D. R. & Elce, B. (1979). A possible relationship between salivarian trypanosomes and Glossina labrum mechano-receptors. Annals of Tropical Medicine and Parasitology 73, 287–90.CrossRefGoogle ScholarPubMed
Murray, M., Clifford, D. J., Gettinby, G., Snow, W. F. & McIntyre, W. I. M. (1981). Susceptibility to African trypanosomiasis of N'Dama and Zebu cattle in an area of Glossina morsitans submorsitans challenge. The Veterinary Record 12 5, 1981, pp. 503–11.Google Scholar
Nantulya, V. M., Musoke, A. J., Ruranoirwa, F. R. & Moloo, S. K. (1984). Resistance of cattle to tsetse-transmitted challenge with Trypanosoma brucei or Trypanosoma congolense after spontaneous recovery from syringe-passaged infections. Infection and Immunity 43, 735–8.CrossRefGoogle ScholarPubMed
Randolph, S. E., Rogers, D. J. & Kuzoe, F. A. S. (1984). Local variation in the population dynamics of Glossina palpalis palpalis (Robineau-Desvoidy) (Diptera: Glossinidae). II. The effect of insecticidal spray programmes. Bulletin of Entomological Research 74, 425–38.CrossRefGoogle Scholar
Rogers, D. J. (1980). Epizootiology: the tsetse-cattle interface. In Report of the Expert Consultation on Research on Trypanosomiases, Rome, 1–5 10 1979, AGA-801 (1979), pp. 6167. Rome: FAO.Google Scholar
Rogers, D. J. (1985). Trypanosomiasis ‘risk’ or ‘challenge’: a review. Ada Tropica 42, 523.Google ScholarPubMed
Rogers, D. J. & Boreham, P. F. L. (1973). Sleeping sickness survey in the Serengeti area (Tanzania) 1971. II. The vector role of Glossina swynnertoni Austen. Acta Tropica 30, 2435.Google ScholarPubMed
Rogers, D. J. & Randolph, S. E. (1985). Population ecology of tsetse. Annual Reviews of Entomology 30, 197216.CrossRefGoogle ScholarPubMed
Rogers, D. J., Randolph, S. E. & Kuzoe, F. A. S. (1984). Local variation in the population dynamics of Glossina palpalis palpalis (Robineau-Desvoidy) (Diptera: Glossinidae). I. Natural population regulation. Bulletin of Entomological Research 74, 403–23.CrossRefGoogle Scholar
Rottcher, D. & Schillinger, D. (1985). Multiple drug resistance in Trypanosoma vivax in the Tana River district of Kenya. The Veterinary Record 117, 557–8.CrossRefGoogle ScholarPubMed
Rurangirwa, F. R., Musoke, A. J., Nantulya, V. M., Nkonge, C., Njuguna, L. & Mushi, E. Z. (1986). Immune effector mechanisms involved in the control of parasitaemia in Trypanosoma brucei – infected wildebeest (Connochaetes laurinus). Immunology 58, 231–7.Google Scholar
Ryan, L. (1984). The effect of trypanosome infection on a natural population of Glossina longipalpis Wiedemann (Diptera: Glossinidae) in Ivory Coast. Acta Tropica 41, 355–9.Google ScholarPubMed
Ryan, L., Kupper, W., Molyneux, D. H. & Clair, M. (1988). Relationships between geographical and dietary factors and trypanosome infection rates of tsetse flies in the field (Diptera: Glossinidae). Entomologia Generalis 12, 7781.CrossRefGoogle Scholar
Snow, W. F. (1979). Tsetse ecology and epidemiology of trypanosomiasis in The Gambia and on the south Kenya coast: a comparison. In The 16th Meeting of ISCTRC, Yaounde, Cameroun, 1979, pp. 389–381. Nairobi, Kenya: OAU/STRC.Google Scholar
Snow, W. F. & Tarimo, S. A. (1983). A quantification of the risk of trypanosomiasis infection to cattle on the south Kenya coast. Acta Tropica 40, 331340.Google ScholarPubMed
Tarimo, C. S., Gates, B. D. & Williamson, D. L. (1981). Feeding preference of Glossina in Northeastern Tanzania. In The 17th Meeting of ISCTRC, Arusha, Tanzania, pp. 415418. Nairobi, Kenya: OAU/STRC.Google Scholar
Tarimo, S. A., Snow, W. F., Butler, L. & Dransfield, R. (1985). The probability of tsetse acquiring trypanosome infection from single blood meal in different localities in Kenya. Acta Tropica 42, 199207.Google ScholarPubMed
Trail, J. C. M., Sones, K., Jibbo, J. M. C., Durkin, J., Light, D. E. & Murray, M. (1985). Productivity of Boran cattle maintained by chemoprophylaxis under trypanosomiasis risk. ILCA Research Report No. 9, 02 1985. Addis Ababa, Ethiopia: International Livestock Centre for Africa.Google Scholar
Wijers, D. J. B. (1958). Factors that may influence the infection rate of Glossina palpalis with Trypanosoma gambiense. The age of the fly at the time of the infective feed. Annals of Tropical Medicine and Parasitology 52, 385–90.CrossRefGoogle ScholarPubMed
Willett, K. C. (1972). An observation on the unexpected frequency of some multiple infections. Bulletin of the World Health Organization 47, 747–9.Google ScholarPubMed
Williamson, D. L., Dame, D. A., Gates, D. B., Cobb, P. E., Bakuli, B. & Warner, P. V. (1983 a). Integration of insect sterility and insecticides for control of Glossina morsitans morsitans Westwood (Diptera: Glossinidae) in Tanzania. V. The impact of sequential releases of sterilised tsetse flies. Bulletin of Entomological Research 73, 391–391.CrossRefGoogle Scholar
Williamson, D. L., Dame, D. A., Lee, C. W., Gates, D. B. & Cobb, P. E. (1983 b). Integration of insect sterility and insecticides for control of Glossina morsitans morsitans Weatwood (Diptera: Glossinidae) in Tanzania. IV. Application of endosulfan as an aerosol prior to release of sterile males. Bulletin of Entomological Research 73, 383–383.CrossRefGoogle Scholar