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A general model for the African trypanosomiases

Published online by Cambridge University Press:  06 April 2009

D. J. Rogers
D. J. Rogers
Affiliation:
Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS
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Summary

A general mathematical model of a vector-borne disease involving two vertebrate host species and one insect vector species is described. The model is easily extended to other situations involving more than two hosts and one vector species. The model, which was developed from the single-host model for malaria described by Aron & May (1982), is applied to the African trypanosomiases and allows for incubation and immune periods in the two host species and for variable efficiency of transmission of different trypanosome species from the vertebrates to the vectors and vice versa. Equations are derived for equilibrium disease prevalence in each of the species involved. Model predictions are examined by 3-dimensional phase-plane analysis, which is presented as a simple extension of the 2-dimensional phase-plane analysis of the malaria model. Parameter values appropriate for the African trypanosomiases are derived from the literature, and a typical West African village situation is considered, with 300 humans, 50 domestic animals and an average population of 5000 tsetse flies. The model predicts equilibrium prevalences of Trypanosoma vivax, T. congolense and T. brucei of 47·0, 45·8 and 28·7% respectively in the animal hosts, 24·2, 3·4 and 0·15% in the tsetse vectors, and a 7·0% infection of humans with human-infective T. brucei. The contribution to the basic rate of reproduction of the human-infective T. brucei is only 0·11 from the human hosts and 2·54 from the animal hosts, indicating that in the situation modelled human sleeping sickness cannot be maintained in the human hosts alone. The animal reservoir is therefore crucial in determining not only the continued occurrence of the disease in humans, but its prevalence in these hosts as well. The effect of changing average fly density on equilibrium disease prevalences is examined, together with the effect of seasonal changes in fly numbers on disease incidence. In a seasonal situation changes in fly mortality rates affect both future population size and infection rate. Peak disease incidence lags behind peak fly numbers, and that in the less favoured host lags behind that in the more favoured host. Near the threshold fly density for disease transmission disease incidence is more changeable than at higher fly densities and may even exceed equilibrium prevalence at the same average fly density (because most hosts are susceptible at the time that fly numbers begin their annual increase). The implications of the model for disease control are discussed. Identifying the precise role of the animal reservoir may suggest that treating such animals will achieve a greater reduction of human sleeping sickness than direct treatment of the humans alone. Statistically significant results of control campaigns may also be more easily shown by monitoring the non-human reservoirs. The model provides a means by which a correct perspective view can be obtained of the complex epidemiology and epizootiology of the African trypanosomiases.

Type
Trends and Perspectives
Information
Parasitology , Volume 97 , Issue 1 , August 1988 , pp. 193 - 212
Copyright
Copyright © Cambridge University Press 1988

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References

REFERENCES

Anderson, R. M. (1982). Population Dynamics of Infectious Diseases. London: Chapman and Hall.Google Scholar
Aron, J. L. & May, R. M. (1982). The population dynamics of malaria. In Population Dynamics of Infectious Diseases (ed. Anderson, R. M.), pp. 139–79. London: Chapman and Hall.CrossRefGoogle 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, 147–61.CrossRefGoogle ScholarPubMed
Bailey, N. M. (1966). The mechanical transmission by Glossina morsitans of Trypanosoma brucei subgroup trypanosomes. In Annual Report 1965, East Africa Trypanosomiasis Research Organization, pp. 24–7. Entebbe: Government Printer.Google Scholar
Bailey, N. T. J. (1982). The Biomathematics of Malaria. London: Griffin.Google Scholar
Baldry, D. A. T. (1980). Local distribution and ecology of Glossina palpalis and G. tachinoides in forest foci of West African human trypanosomiasis, with special reference to associations between peri-domestic tsetse and their hosts. Insect Science and its Application 1, 85–93.Google Scholar
Bruce, D., Hamerton, A. E., Bateman, H. R. & Mackie, F. P. (1910). Mechanical transmission of Sleeping Sickness by the tsetse fly. Proceedings of the Royal Society of London, B 82, 498–501.Google Scholar
Cawdery, M. J. H. (1958). Estimation of trypanosome challenge. In Annual Report 1956–57. East African Trypanosomiasis Research Organization, p. 18. Nairobi: East African High Commission.Google Scholar
Duggan, A. J. (1970). An historical perspective. In The African Trypanosomiases (ed. Mulligan, H. W.), pp. 41–88. London: George Allen and Unwin Ltd.Google Scholar
Fao-Who-Oie. (1982) Animal Health Yearbook, 1981. Rome: FAO.Google Scholar
Geigy, R., Mwambu, P. M. & Kauffmann, M. (1971). Sleeping sickness survey in Musoma district, Tanzania. IV. Examination of wild animals as potential reservoir of T. rhodesiense. Acta Tropica 28, 211–20.Google ScholarPubMed
Gingrich, J. B., Ward, R. A., Macken, L. M. & Schoenbechler, M. J. (1982 a). Trypanosoma brucei rhodesiense (Trypanosomatidae): factors influencing infection rates of a recent human isolate in the tsetse Glossina morsitans (Diptera, Glossinidae). Journal of Medical Entomology 19, 268–74.CrossRefGoogle ScholarPubMed
Gingrich, J. B., Ward, R. A., Macken, L. M. & Esser, K. M. (1982 b). African sleeping sickness: new evidence that mature tsetse flies (Glossina morsitans) can become potent vectors. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 479–81.CrossRefGoogle ScholarPubMed
Gingrich, J. B., Roberts, L. W. & Macken, L. M. (1983). Trypanosoma brucei rhodesiense: mechanical transmission by tsetse, Glossina morsitans (Diptera, Glossinidae), in the laboratory. Journal of Medical Entomology 20, 673–6.CrossRefGoogle ScholarPubMed
Gouteux, J.-P. & Laveissière, C. (1982). Écologie des glossines en secteur pré-forestier de Côte d'Ivoire. 4. Dynamique de l'écodistribution en terroir villageois. Cahiers de l'Office de la Recherche Scientifique et Technique Outre-Mer, Série Entomologie Médicale et Parasitologie 20, 199–229.Google Scholar
Gouteux, J.-P., LaveissiÈre, C. & Boreham, P. F. L. (1982 a). Écologie des glossines en secteur préforestier de Côte d'Ivoire. 2. Les préférences trophiques de Glossina palpalis s.l. Cahiers de l'Office de la Recherche Scientifique et Technique Outre-Mer, Série Entomologie Médicale et Parasitologie 20, 3–18.Google Scholar
Gouteux, J.-P., Laveissière, C. & Boreham, P. F. L. (1982 b). Écologie des glossines en secteur préforestier de Côte d'Ivoire. 3. Les préférences trophiques de Glossina pallicera et G. nigrofusca. Comparaison avec G. palpalis et implications épidémiologiques. Cahiers de l'Office de la Recherche Scientifique et Technique Outre-Mer, Série Entomologie Médicale et Parasitologie 20, 109–24.Google Scholar
Habtemariam, T., Ruppanner, R., Riemann, H. P. & Theis, J. H. (1983 a). An epidemiologic systems analysis model for African trypanosomiasis. Preventive Veterinary Medicine 1, 125–36.CrossRefGoogle Scholar
Habtemariam, T., Ruppanner, R., Riemann, H. P. & Theis, J. H. (1983 b). Epidemic and endemic characteristics of trypanosomiasis in cattle: a simulation model. Preventive Veterinary Medicine 1, 137–45.CrossRefGoogle Scholar
Habtemariam, T., Ruppanner, R., Riemann, H. P. & Theis, J. H. (1983 c). Evaluation of trypanosomiasis control alternatives using an epidemiologic simulation model. Preventive Veterinary Medicine 1, 147–56.CrossRefGoogle Scholar
Hoare, C. A. (1972). The Trypanosomes of Mammals. Oxford: Blackwell Scientific Publications.Google Scholar
Jackson, C. H. N. (1933). The causes and implications of hunger in tsetse flies. Bulletin of Entomological Research 24, 443–82.CrossRefGoogle 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
Macdonald, G. (1952). The analysis of equilibrium in malaria. Tropical Diseases Bulletin 49, 813–28.Google ScholarPubMed
Macdonald, G. (1957). The Epidemiology and Control of Malaria. London: Oxford University Press.Google Scholar
Macdonald, G. (1973). Dynamics of Tropical Disease. (Collected papers, edited by Bruce-Chwatt, L. J. and Glanville, V. J..) London: Oxford University Press.Google Scholar
Maynard Smith, J. & Slatkin, M. (1973). The stability of predator-prey systems. Ecology 54, 384–91.CrossRefGoogle Scholar
Mehlitz, D. (1982). Trypanosomes in African wild mammals. In Perspectives in Trypanosomiasis Research (ed. Baker, J. R.), pp. 25–35. Chichester: Research Studies Press.Google Scholar
Mehlitz, D. (1986). Le réservoir animal de la maladie du sommeil a Trypanosoma brucei gambiense. Etudes et Syntheses de l'I.E.M.V.T. 18. Maisons-Alfort: Institut d'Elevage et de Medecine Veterinaire des Pays Tropicaux.Google Scholar
Milligan, P. J. M. & Baker, R. D. (1988). A model of tsetse-transmitted animal trypanosomiasis. Parasitology 96, 211–39.CrossRefGoogle Scholar
Moloo, S. K. (1983). Feeding behaviour of Glossina morsitans morsitans infected with Trypanosoma vivax, T. congolense or T. brucei. Parasitology 86, 51–6.CrossRefGoogle ScholarPubMed
Moloo, S. K. & Dar, F. (1985). Probing by Glossina morsitans centralis infected with pathogenic Trypanosoma species. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 119.CrossRefGoogle ScholarPubMed
Morris, K. R. S. (1946). The control of trypanosomiasis by entomological means. Bulletin of Entomological Research 37, 201–50.CrossRefGoogle ScholarPubMed
Murray, M. & Gray, A. R. (1984). The current situation on animal trypanosomiasis in Africa. Preventive Veterinary Medicine 2, 23–30.CrossRefGoogle Scholar
Murray, M., Grootenhuis, J. G., Akol, G. W. O., Emery, D. L., Shapiro, S. Z., Moloo, S. K., Dar, F., Bovell, D. L. & Paris, J. (1981). Potential application of research on African trypanosomiases in wildlife and preliminary studies on animals exposed to tsetse infected with Trypanosoma congolense. In Wildlife Disease Research and Economic Development (ed. E., Karstad, B., Nestel and M., Graham), pp. 40–5. Ottawa: International Development Research Centre.Google Scholar
Murray, M., Morrison, W. I. & Whitelaw, D. D. (1982). Host susceptibility to African trypanosomiasis: trypanotolerance. Advances in Parasitology 21, 1–68.CrossRefGoogle ScholarPubMed
Otieno, L. H. & Darji, N. (1979). The abundance of pathogenic African trypanosomes in the salivary secretions of wild Glossina pallidipes. Annals of Tropical Medicine and Parasitology 73, 583–8.CrossRefGoogle ScholarPubMed
Randolph, S. E. & Rogers, D. J. (1984). Movement patterns of the tsetse fly Glossina palpalis palpalis (Robineau-Desvoidy) around villages in the pre-forest zone of Ivory Coast. Bulletin of Entomological Research 74, 689–705.CrossRefGoogle Scholar
Roberts, L. W. (1981). Probing by Glossina morsitans morsitans and transmission of Trypanosoma (Nannomonas) congolense. American Journal of Tropical Medicine and Hygiene 30, 948–51.CrossRefGoogle ScholarPubMed
Rogers, D. (1977). Study of a natural population of Glossina fuscipes fuscipes Newstead and a model of fly movement. Journal of Animal Ecology 46, 309–30.CrossRefGoogle Scholar
Rogers, D. J. (1980). Epizootiology: the tsetse-cattle interface. Report of the Expert Consultation on Research on Trypanosomiases, 1–5 October 1979, Appendix VI, pp. 61–7. Rome: FAO (AGA–801).Google Scholar
Rogers, D. J. (1985). Trypanosomiasis ‘risk’ or ‘challenge’: a review. Acta Tropica 42, 5–23.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, 24–35.Google 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
Ross, R. (1911). The Prevention of Malaria, 2nd Ed. London: Murray.Google ScholarPubMed
Ross, R. (1916). An application of the theory of probabilities to the study of a priori pathometry. I. Proceedings of the Royal Society of London, A 92, 204–30.Google Scholar
Sachs, R., Mehlitz, D. & Staak, C. (1980). Host preference and trypanosome infection of three tsetse species (Glossina palpalis, G. pallicera and G. nigrofusca) in rain forest zones of Liberia, West Africa. In Tenth International Congress on Tropical Medicine and Malaria, Manila, Philippines, pp. 216–17.Google Scholar
Varley, G. C., Gradwell, G. R. & Hassell, M. P. (1973). Insect Population Ecology. Oxford: Blackwell Scientific Publications.Google Scholar
Watson, H. J. C. (1963). The domestic pig as a reservoir of T. gambiense. In International Scientific Committee for Trypanosomiasis Research, Ninth Meeting, Conakry, 1962, p. 327. Lagos: Commission for Technical Co-operation in Africa.Google Scholar
Wells, E. A. (1972). The importance of mechanical transmission in the epidemiology of nagana: a review. Tropical Animal Health and Production 4, 74–88.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
Wilson, A. J., Dar, F. K. & Paris, J. (1972). A study on the transmission of salivarian trypanosomes isolated from wild tsetse flies. Tropical Animal Health and Production 4, 14–22.CrossRefGoogle Scholar
W.H.O. (1986). Epidemiology and control of African trypanosomiasis. Report of a W.H.O. Expert Committee. W.H.O. Technical Report Series, no. 739. Geneva: World Health Organization.Google Scholar
Wijers, D. J. B. (1960). The importance of the age of G. palpalis at the time of the infective feed with T. gambiense. In International Scientific Committee for Trypanosomiasis Research, Seventh Meeting, Bruxelles, 1958, pp. 319–20. London: Commission for Technical Co-operation in Africa South of the Sahara.Google Scholar