Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-23T19:43:06.572Z Has data issue: false hasContentIssue false

Population genetics of Trypanosoma brucei and the epidemiology of human sleeping sickness in the Lambwe Valley, Kenya

Published online by Cambridge University Press:  06 April 2009

S. Mihok
Affiliation:
International Centre of Insect Physiology and Ecology, P.O. Box 30772, Nairobi, Kenya
L. H. Otieno
Affiliation:
International Centre of Insect Physiology and Ecology, P.O. Box 30772, Nairobi, Kenya
N. Darji
Affiliation:
International Centre of Insect Physiology and Ecology, P.O. Box 30772, Nairobi, Kenya

Summary

Numerical taxonomy was used to review isoenzyme variation in isolates of Trypanosoma brucei obtained from cattle, tsetse, humans and wildlife from the Lambwe Valley, Kenya. From isoenzyme information alone, it was possible to classify isolates as to source through the use of linear discriminant functions analysis, with an error rate of only 2% in humans, and 14% over all groups. Differentiation was mostly dependent on patterns in the enzymes ASAT, PEPI, and ICD. Parasites from non-human sources, especially tsetse, were characterized by high isoenzyme diversity, and many unique zymodemes. Observed frequencies of genotypes for ICD, ALAT, and ASAT did not agree with expected frequencies based on random mating of a diploid organism. Deviations were particularly large for tsetse isolates, and were mostly due to a deficiency of one homozygote. Cluster analysis revealed complex relationships among isolates, with patterns evolving through time. Major human zymodemes from the 1970s clustered together with most wildlife isolates from East Africa. This chronic human-wildlife transmission cycle was characterized by ASAT pattern I. Other, minor human zymodemes were associated with a human-cattle transmission cycle characterized by ASAT pattern VII. These original chronic transmission cycles appeared to change in 1980 with the appearance of two new zymodemes in humans. These zymodemes involved changes in ALAT and/or PGM to patterns typical of tsetse and cattle isolates. A resultant epidemic was halted with repeated aerial spraying of endosulfan in 1981. Since then, a variety of new zymodemes of unknown human infectivity have appeared. The origins of these changes are discussed in terms of genetic exchange in tsetse, adaptation to human and cattle transmission cycles, and selection resulting from chronic use of insecticides.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

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

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
Allsopp, R., Baldry, D. A. T. & Rodrigues, C. (1972). The influence of game animals on the distribution and feeding habits of Glossina pallidipes in the Lambwe Valley. Bulletin of the World Health Organization 47, 795809.Google ScholarPubMed
Baldry, D. A. T. (1972). A history of Rhodesian sleeping sickness in the Lambwe Valley. Bulletin of the World Health Organization 47, 699718.Google ScholarPubMed
Bertram, B. C. R. (1973). Sleeping sickness survey in the Serengeti area (Tanzania). 1971. III. Discussion of the relevance of the trypanosome survey to the biology of large mammals in the Serengeti. Acta Tropica 30, 3648.Google Scholar
Cibulskis, R. E. (1988). Origins and genetic diversity in natural populations of Trypanosoma brucei. Parasitology 96, 303–22.Google Scholar
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, 78 5–8.Google ScholarPubMed
Ford, J. (1971). The Role of Trypanosomiases in African Ecology. A Study of the Tsetse Fly Problem. Oxford: Clarendon Press.Google Scholar
Gibson, W. C. & Gashumba, J. K. (1983). Isoenzyme characterization of some Trypanozoon stocks from a recent trypanosomiasis epidemic in Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 114–18.CrossRefGoogle ScholarPubMed
Gibson, W. C., Marshall, T. F. DE C. & Godfrey, D. G. (1980). Numerical analysis of enzyme polymorphism: a new approach to the epidemiology and taxonomy of trypanosomes of the subgenus Trypanozoon. Advances in Parasitology 13, 175246.Google Scholar
Gibson, W. C. & Wellde, B. T. (1985). Characterization of Trvpanozoon stocks from the South Nyanza sleeping sickness focus in Western Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 671–6.Google Scholar
Godfrey, D. G., Scott, C. M., Gibson, W. C., Mehlitz, D. & Zillmann, U. (1987). Enzyme polymorphism and the identity of Trypanosoma brucei gambiense. Parasitology 94, 337 –47.CrossRefGoogle ScholarPubMed
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, 483–4.Google Scholar
Harley, J. M. B. (1971). Comparison of the susceptibility to infection with Trypanosoma rhodesiense of Glossina pallidipes, G. morsitans, G. fuscipes, and G. brevipalpis. Annals of Tropical Medicine and Parasitology 65, 185–9.CrossRefGoogle ScholarPubMed
Harris, H. & Hopkinson, D. A. (1976). Handbook of Enzyme Electrophoresis in Human Genetics. Amsterdam: North-Holland.Google Scholar
Jenni, L., Marti, S., Schweizer, J., Betschart, B., Lepage, R. W. F., Wells, J. M., Tait, A., Paindavoine, P., Pays, E. & Steinert, M. (1986). Hybrid formation between African trypanosomes during cyclical transmission. Nature, London 322, 173–5.CrossRefGoogle ScholarPubMed
Moloo, S. K. & Kutuza, S. B. (1988). Comparative study on the susceptibility of different Glossina species to Trypanosoma brucei brucei infection. Tropical Medicine and Parasitology 39, 211–13.Google ScholarPubMed
Moloo, S. K. & Shaw, M. K. (1989). Rickettsial infections of midgut cells are not associated with susceptibility of Glossina morsitans centralis to Trypanosoma congolense infection. Acta Tropica 46, 223–7.CrossRefGoogle Scholar
Omerod, W. E. (1961). The epidemic spread of Rhodesian sleeping sickness 1908—1960. Transactions of the Royal Society of Tropical Medicine and Hygiene 55, 525–38.Google Scholar
Otieno, L. H. & Darji, N. (1985). Characterization of potentially man-infective Trypanosoma brucei from an endemic area of sleeping sickness in Kenya. Tropical Medicine and Parasitology 36, 123–6.Google ScholarPubMed
Otieno, L. H. & Darji, N. (1987). The investigation of Trypanosoma brucei isolates obtained from Glossina pallidipes in South Nyanza, Kenya. Journal of Tropical Medicine and Hygiene 90, 259–63.Google Scholar
Otieno, L. H., Darji, N. & Onyango, P. (1990). Electrophoretic analysis of Trypanosoma brucei isolates from cattle, tsetse and humans from the Lambwe Valley, Western Kenya. Insect Science and its Application. (in the Press).Google Scholar
Otieno, L. H., Darji, N., Onyango, P. & Mpanga, E. (1983). Some observations on factors associated with the development of Trypanosoma brucei brucei infections in Glossina morsitans. Acta Tropica 40, 113–20.Google Scholar
Paindavoine, P., Pays, E., Laurent, M., Geltmeyer, Y., Le ray, D., Mehlitz, D. & Steinert, M. (1986). The use of DNA hybridization and numerical taxonomy in determining relationships between Trypanosoma brucei stocks and subspecies. Parasitology 92, 31–50.CrossRefGoogle ScholarPubMed
Paindavoine, P., Zampetti-Bosseler, F., Coquelet, H., Pays, E. & Steinert, M. (1989). Different allele frequencies in Trypanosoma brucei brucei and Trypanosoma brucei gambiense populations. Molecular and Biochemical Parasitology 32, 6172.CrossRefGoogle ScholarPubMed
Poole, R. W. (1974). An Introduction to Quantitative Ecology. New York: McGraw-Hill.Google Scholar
Schweizer, J., Tait, A. & Jenni, L. (1988). The timing and frequency of hybrid formation in African trypanosomes during cyclical transmission. Parasitology Research 75, 98101.CrossRefGoogle ScholarPubMed
Sneath, P. H. A. & Sokal, R. R. (1973). Numerical Taxonomy. The Principles and Practice of Numerical Classification. San Francisco: W. H. Freeman.Google Scholar
Sternberg, J., Tait, A., Haley, S., Wells, J. M., Lbpage, R. W. F., Schweizer, J. & Jenni, L. (1988). Gene exchange in African trypanosomes: characterisation of a new hybrid genotype. Molecular Biochemistry and Parasitology 27, 191200.CrossRefGoogle ScholarPubMed
Tait, A. (1980). Evidence for diploidy and mating in trypansomes. Nature, London 287, 536–8.Google Scholar
Tait, A., Barry, J. D., Wink, R., Sanderson, A. & Crowe, J. S. (1985). Enzyme variation in T. brucei spp. II. Evidence for T. b. rhodesiense being a set of variants of T. b. brucei. Parasitology 90, 89100.Google Scholar
Turner, D. A. (1986). Tsetse and trypanosomiasis in the Lambwe Valley, Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 592–5.CrossRefGoogle ScholarPubMed
Turner, D. A. & Brightwell, R. (1986). An evaluation of a sequential aerial spraying operation against Glossina pallidipes Austen (Diptera: Glossinidae) in the Lambwe Valley of Kenya: aspects of the post-spray recovery and evidence of natural population regulation. Bulletin of Entomological Research 76, 331–49.Google Scholar
Turner, D. A. & Golder, T. K. (1986). Susceptibility to topical applications of endosulfan and dieldrin in sprayed and unsprayed populations of Glossina pallidipes Austen (Diptera: Glossinidae) in Kenya. Bulletin of Entomological Research 76, 519–27.Google Scholar
Watson, H. J. C. (1972). The epidemiology of human sleeping sickness in the Lambwe Valley, South Nyanza, Kenya. Bulletin of the World Health Organization 47, 719–26.Google Scholar
Welburn, S. C. & Gibson, W. C. (1989). Cloning of a repetitive DNA from rickettsia-like organisms of tsetse flies (Glossina spp.). Parasitology 98, 81–4.CrossRefGoogle ScholarPubMed
Willett, K. C. (1965). Some observations on the recent epidemiology of sleeping sickness in Nyanza region, Kenya, and its relation to the general epidemiology of Gambian and Rhodesian sleeping sickness in Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 59, 374–94.Google Scholar