Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-27T00:06:34.475Z Has data issue: false hasContentIssue false

Epidemiological relationships of Trypanosoma brucei stocks from South East Uganda: evidence for different population structures in human infective and non-human infective isolates

Published online by Cambridge University Press:  06 April 2009

G. Hide
Affiliation:
Wellcome Unit of Molecular Parasitology, Department of Veterinary Parasitology, Glasgow University Veterinary School, Bearsden Road, Glasgow G61 IQH
S. C. Welburn
Affiliation:
Tsetse Research Laboratory, ODA/University of Bristol, Department of Veterinary Medicine, Langford House, Langford, Bristol BS18 7DU
A. Tait
Affiliation:
Wellcome Unit of Molecular Parasitology, Department of Veterinary Parasitology, Glasgow University Veterinary School, Bearsden Road, Glasgow G61 IQH
I. Maudlin
Affiliation:
Tsetse Research Laboratory, ODA/University of Bristol, Department of Veterinary Medicine, Langford House, Langford, Bristol BS18 7DU

Summary

This study represents an analysis of trypanosome strains circulating within a confined location over a short period of time during a sleeping sickness epidemic in S.E. Uganda. A large number of Trypanosoma brucei isolates (88) were collected from a variety of hosts (man, cattle, pigs and tsetse) from villages within a 10 km radius and were analysed for variation in isoenzyme patterns, restriction fragment length polymorphism (RFLP) in repetitive DNA sequences and susceptibility to human serum. The human infective stocks form a clearly distinguishable population when compared with other stocks circulating in the domestic cattle reservoir. The data here support the occurrence of genetic exchange between the cattle stocks while an ‘epidemic’ population structure involving limited genetic exchange is a characteristic of the human infective stocks. Furthermore, it is shown that when both RFLP and isoenzyme analysis are carried out most stocks appear to have individual genotypes. Stocks which were formerly grouped as zymodemes are better considered as a collection of distinct individuals.

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

Abaru, D. E. (1985). Sleeping sickness in Busoga, Uganda, 1876–1983. Tropical Medicine and Parasitology 36, 72–6.Google Scholar
Brun, R. & Jenni, L. (1987). Human serum resistance of metacyclic forms of Trypanosoma brucei brucei, T. brucei rhodesiense and T. brucei gambiense. Zeitschrift für Parasitenkunde 73, 218–23.Google ScholarPubMed
Cibulskis, R. (1987). Mutation and recombination in the Trypanosomatidae. Leishmania. Taxonomie et phylogenèse. Applications éco-épidémiologiques. (Coll. int CNRS/INSERM). Montpellier: IMEEE.Google Scholar
Cibulskis, R. E. (1992). Genetic variation in Trypanosoma brucei and the epidemiology of sleeping sickness in the Lambwe Valley, Kenya. Parasitology 104, 99109.CrossRefGoogle ScholarPubMed
Day, K. P., Koella, J. C., Nee, S., Gupta, S. & Read, A. F. (1992). Population genetics and dynamics of Plasmodium falciparum: an ecological view. Parasitology 104, S35S52.CrossRefGoogle ScholarPubMed
Enyaru, J. C. K., Odiit, M., Gashumba, J. K., Carasco, J. F. & Rwendeire, A. J. (1992). Characterisation by isoenzyme electrophoresis of Trypanozoon stocks from sleeping sickness endemic areas of south-east Uganda. Bulletin of the World Health Organization 70, 631–6.Google ScholarPubMed
Enyaru, J. C. K., Allingham, R., Bromidge, T., Kanmogne, G. D. & Carasco, J. F. (1993 a). The isolation and genetic heterogeneity of Trypanosoma brucei gambiense from north-west Uganda. Acta Tropica 54, 31–9.CrossRefGoogle ScholarPubMed
Enyaru, J. C. K., Stevens, J. R., Odiit, M., Okuna, N. M. & Carasco, J. F. (1993 b). Isoenzyme comparison of Trypanozoon isolates from two sleeping sickness areas of south-eastern Uganda. Acta Tropica 55, 97115.CrossRefGoogle ScholarPubMed
Gibson, W. C. (1989). Analysis of a genetic cross between Trypanosoma brucei rhodesiense and T. b. brucei. Parasitology 99, 391402.CrossRefGoogle ScholarPubMed
Gibson, W. C., Borst, P. & Fase-Fowler, F. (1985). Further analysis of intraspecific variation in Trypanosoma brucei using restriction site polymorphisms in the maxicircle of kinetoplast DNA. Molecular and Biochemical Parasitology 15, 2136.CrossRefGoogle ScholarPubMed
Gibson, W. C. & Gashumba, J. K. (1983). Isoenzyme characterisation of some Trypanozoon stocks from a recent trypanosomiasis epidemic in Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 671–6.CrossRefGoogle Scholar
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 18, 175245.CrossRefGoogle Scholar
Gibson, W. C., Mehlitz, D., Lanham, S. M. & Godfrey, D. G. (1978). The identification of Trypanosoma brucei gambiense in Liberian pigs and dogs by isoenzymes and by resistance to human plasma. Tropenmedizin und Parasitologie 29, 335–45.Google ScholarPubMed
Godfrey, D. G., Baker, R. D., Rickman, L. R. & Mehlitz, D. (1990). The distribution, relationships and identification of enzymic variants within the subgenus Trypanozoon. Advances in Parasitology 29, 174.CrossRefGoogle ScholarPubMed
Hide, G., Cattand, P., Le Ray, D., Barry, J. D. & Tait, A. (1990). The identification of Trypanosoma brucei subspecies using repetitive DNA sequences. Molecular and Biochemical Parasitology 39, 213–26.CrossRefGoogle ScholarPubMed
Hide, G., Buchanan, N, Welburn, S. C., Maudlin, I., Barry, J. D. & Tait, A. (1991). Trypanosoma brucei rhodesiense: characterisation of stocks from Zambia, Kenya and Uganda using repetitive DNA probes. Experimental Parasitology 72, 430–9.CrossRefGoogle ScholarPubMed
Jenni, L., Marti, S., Schweizer, J., Betschart, B., Le Page, 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
Kaukas, A., Gashumba, J. K., Lanham, S. M. & Dukes, P. (1990). The substitution of procyclic for bloodstream form Trypanosoma brucei gambiense in isoenzyme studies. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 242–5.CrossRefGoogle ScholarPubMed
Lanham, S. M. & Godfrey, D. G. (1970). Isolation of salivarian trypanosomes from man and other animals using DEAE cellulose. Experimental Parasitology 28, 521–4.CrossRefGoogle ScholarPubMed
Lanham, S. M., Grendon, J. M., Miles, M. A., Povoa, M. M. & De Souza, A. A. A. (1981). A comparison of electrophoretic methods for isoenzyme characterisation of trypanosomatids. 1. Standard stocks of Trypanosoma cruzi zymodemes from northeast Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 542–50.CrossRefGoogle Scholar
MacKichan, I. W. (1944). Rhodesian sleeping sickness in Eastern Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 38, 49.CrossRefGoogle Scholar
Maudlin, I., Welburn, S. C., Gashumba, J. K., Okuna, N. & Kalunda, M. (1990). The role of cattle in the epidemiology of sleeping sickness in Uganda. Bulletin de la Société Française de Parasitologie 8 (Suppl. 2), 788.Google Scholar
Maynard-Smith, J., Smith, N. H., O'Rouke, M. & Spratt, B. (1993). How clonal are bacteria? Proceedings of the National Academy of Sciences, USA 90, 4384–8.CrossRefGoogle Scholar
Mbulamberi, D. B. (1989). Possible causes leading to an epidemic outbreak of sleeping sickness: Facts and hypotheses. Annales de la Société Beige de Médecine Tropical 69 (Suppl.), 173–9.Google Scholar
Mbulamberi, D. B. (1991). The sleeping sickness situation in Uganda: past and present. National Sleeping Sickness Control Program, Ministry of Health, Government of Uganda report.Google Scholar
Mihok, S., Otieno, L. H. & Darji, N. (1990). Population genetics of Trypanosoma brucei and the epidemiology of human sleeping sickness in the Lambwe Valley, Kenya. Parasitology 100, 219–33.CrossRefGoogle ScholarPubMed
Morrison, W. I., Wells, P. W., Moloo, S. K., Paris, J. & Murray, M. (1982). Interference in the establishment of superinfections with Trypanosoma congolense in cattle. Journal of Parasitology 68, 755–74.CrossRefGoogle ScholarPubMed
Onyango, R. J., Van Hoeve, K. & De Raadt, P. (1966). The epidemiology of Trypanosoma rhodesiense sleeping sickness in Alego location, Central Nyanza, Kenya. Evidence that cattle may act as a reservoir host of trypanosomes infectious to man. Transactions of the Royal Society of Tropical Medicine and Hygiene 60, 175–82.CrossRefGoogle Scholar
Paindavoine, P., Pays, E., Laurent, M., Geltmeyer, Y., Le Ray, D., Mehlitz, D. & Steinert, M. (1986). The use of DNA hybridisation and numerical taxonomy in determining relationships between Trypanosoma brucei stocks and subspecies. Parasitology 92, 3150.CrossRefGoogle ScholarPubMed
Stevens, J. R., Lanham, S. M., Allincham, R. & Gashumba, J. K (1992). A simplified method for identifying subspecies and strain groups in Trypanozoon by isoenzymes. Annals of Tropical Medicine and Parasitology 86, 928.CrossRefGoogle ScholarPubMed
Stevens, J. R. & Welburn, S. C. (1993). Genetic process within an endemic of sleeping sickness in Uganda. Parasitology Research 79, 421–7.CrossRefGoogle ScholarPubMed
Tait, A. (1980). Evidence for diploidy and mating in trypanosomes. Nature, London 287, 536–8.CrossRefGoogle ScholarPubMed
Tait, A., Barry, J. D., Wink, R., Sanderson, A. & Crowe, J. S. (1985). Enzyme variation in T. brucei ssp. II. Evidence for T. b. rhodesiense being a set of variants of T. b. brucei. Parasitology 90, 89100.CrossRefGoogle Scholar
Tait, A. & Turner, C. M. R. (1990). Genetic exchange in Trypanosoma brucei. Parasitology Today 6, 70–5.CrossRefGoogle ScholarPubMed
Tibayrenc, M. & Ayala, F. J. (1991). Towards a population genetics of microorganisms: the clonal theory of parasite protozoa. Parasitology Today 7, 228–32.CrossRefGoogle Scholar
Tibayrenc, M., Kjellberg, F. & Ayala, F. J. (1990). A clonal theory of parasitic protozoa: the population structures of Entamoeba, Giardia, Leishmania, Naegleria, Plasmodium, Trichomonas and Trypanosoma and their medical and taxonomical consequences. Proceedings of the National Academy of Sciences, USA 87, 2414–18.CrossRefGoogle ScholarPubMed
Walliker, D. (1991). Malaria parasites: randomly interbreeding or clonal populations? Parasitology Today 7, 232–5.CrossRefGoogle ScholarPubMed
Walliker, D., Quakyi, L. A., Wellems, T. E., McCutchan, T. F., Szarfman, A., London, W. T., Corcoran, L. M., Burkot, T. R. & Carter, R. (1987). Genetic analysis of the human malaria parasite Plasmodium falciparum. Science 236, 1661–6.CrossRefGoogle ScholarPubMed
Welburn, S. C. & Maudlin, I. (1987). A simple in vitro method for infecting tsetse with trypansomes. Annals of Tropical Medicine and Parasitology 81, 453–5.CrossRefGoogle Scholar
Welburn, S. C. & Maudlin, I. (1992). The nature of the teneral state in Glossina and its role in the acquisition of trypanosome infection in tsetse. Annals of Tropical Medicine and Parasitology 86, 529–36.CrossRefGoogle Scholar