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Molecular epidemiology of African sleeping sickness

Published online by Cambridge University Press:  26 June 2009

G. HIDE  and
A. TAIT
G. HIDE*
Affiliation:
Centre for Parasitology and Disease, Biomedical Sciences Research Institute, School of Environment and Life Sciences, University of Salford, Salford M5 4WT, UK
A. TAIT
Affiliation:
Faculty of Veterinary Medicine, Division of Infection and Immunity, University of Glasgow, Bearsden Road, Glasgow G61 1QH, Scotland, UK
*
*Corresponding author: Centre for Parasitology and Disease, Biomedical Sciences Research Institute, School of Environment and Life Sciences, University of Salford, Salford M5 4WT, UK. Tel: +0161 295 3371. Fax: +0161 295 5015. E-mail: [email protected]
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Summary

Human sleeping sickness in Africa, caused by Trypanosoma brucei spp. raises a number of questions. Despite the widespread distribution of the tsetse vectors and animal trypanosomiasis, human disease is only found in discrete foci which periodically give rise to epidemics followed by periods of endemicity A key to unravelling this puzzle is a detailed knowledge of the aetiological agents responsible for different patterns of disease – knowledge that is difficult to achieve using traditional microscopy. The science of molecular epidemiology has developed a range of tools which have enabled us to accurately identify taxonomic groups at all levels (species, subspecies, populations, strains and isolates). Using these tools, we can now investigate the genetic interactions within and between populations of Trypanosoma brucei and gain an understanding of the distinction between human- and nonhuman-infective subspecies. In this review, we discuss the development of these tools, their advantages and disadvantages and describe how they have been used to understand parasite genetic diversity, the origin of epidemics, the role of reservoir hosts and the population structure. Using the specific case of T.b. rhodesiense in Uganda, we illustrate how molecular epidemiology has enabled us to construct a more detailed understanding of the origins, generation and dynamics of sleeping sickness epidemics.

Keywords

African trypanosomiasisTrypanosoma bruceisleeping sicknessmolecular epidemiologyepidemicsmicrosatellitesgeneticspopulation structure
Type
Research Article
Information
Parasitology , Volume 136 , Special Issue 12: Special Centenary Issue – Parasitology 1908–2008 , October 2009 , pp. 1491 - 1500
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Agbo, E. E. C., Majiwa, P. A. O., Claassen, H. J. and Te Pas, M. F. W. (2002). Molecular variation of Trypanosoma brucei subspecies as revealed by AFLP fingerprinting. Parasitology 124, 249–358.CrossRefGoogle ScholarPubMed
Biteau, N., Bringaud, F., Gibson, W. C., Truc, P. and Baltz, T. (2000). Characterization of Trypanozoon isolates using a repeated coding sequence and microsatellite markers. Molecular and Biochemical Parasitology 105, 185–201.CrossRefGoogle ScholarPubMed
Borst, P., Fase-Fowler, F. and Gibson, W. C. (1981). Quantitation of genetic differences between Trypanosoma brucei gambiense, rhodesiense and brucei by restriction enzyme analysis of kinetoplast DNA. Molecular and Biochemical Parasitology 3, 117–131.CrossRefGoogle ScholarPubMed
Carter, R. and Walliker, D. (1975). New observations on the malaria parasites of rodents of the Central African Republic – Plasmodium vinckei petteri subsp. nov. and Plasmodium chabaudi Landau, 1965. Annals of Tropical Medicine and Parasitology 69, 187–196.CrossRefGoogle ScholarPubMed
Checchi, F., Filipe, J. A., Barrett, M. P. and Chandramohan, D. (2008). The natural progression of gambiense sleeping sickness: what is the evidence? PLoS Neglected Tropical Diseases 2, 303.CrossRefGoogle ScholarPubMed
Cox, A., Tilley, A., Mcodimba, F., Fyfe, J., Hide, G. and Welburn, S. C. (2005). A PCR based assay for detection and differentiation of African trypanosome species in blood. Experimental Parasitology 111, 24–29.CrossRefGoogle ScholarPubMed
De Greef, C., Imberechts, H., Matthyssens, G., Van Meirvenne, N. and Hamers, R. (1989). A gene expressed only in serum-resistant variants of Trypanosoma brucei rhodesiense. Molecular and Biochemical Parasitology 36, 169–176.CrossRefGoogle ScholarPubMed
Fèvre, E. M., Coleman, P. G., Odiit, M. D., Magona, J., Welburn, S. C. and Woolhouse, M. E. J. (2001). The origins of a new sleeping sickness outbreak (caused by Trypanosoma brucei infection) in eastern Uganda. The Lancet 358, 625–628.CrossRefGoogle ScholarPubMed
Fèvre, E. M., Picozzi, K., Fyfe, J., Waiswa, C., Odiit, M., Coleman, P. G. and Welburn, S. C. (2005). A burgeoning epidemic of sleeping sickness in Uganda. The Lancet 366, 745–747.CrossRefGoogle ScholarPubMed
Garcia, A., Courtin, D., Solano, P., Koffi, M. and Jamonneau, V. (2006). Human African trypanosomiasis: connecting parasite and host genetics. Trends in Parasitology 22, 405–409.CrossRefGoogle ScholarPubMed
Gibson, W. C. (1986). Will the real Trypansoma brucei gambiense please stand up? Parasitology Today 2, 255–257.CrossRefGoogle Scholar
Gibson, W. C. (1989). Analysis of a genetic cross between Trypanosoma brucei rhodesiense and T.b. brucei. Parasitology 99, 391–402.CrossRefGoogle ScholarPubMed
Gibson, W. C. (2007). Resolution of the species problem in African trypanosomes. International Journal for Parasitology 37, 829–838.CrossRefGoogle ScholarPubMed
Gibson, W. C. (2009). Species-specific probes for the identification of the African tsetse-transmitted trypanosomes. Parasitology 136, (this issue).CrossRefGoogle ScholarPubMed
Gibson, W. C., Backhouse, T. and Griffiths, A. (2002). The human serum resistance associated gene is ubiquitous and conserved in Trypanosoma brucei rhodesiense throughout East Africa. Infection, Genetics and Evolution 1, 207–214.CrossRefGoogle ScholarPubMed
Gibson, W., Borst, P. and Fase-Fowler, F. (1985). Further analysis of intraspecific variation in Trypanosoma brucei using restriction site polymorphisms in the maxi-circle of kinetoplast DNA. Molecular and Biochemical Parasitology 15, 21–36.CrossRefGoogle ScholarPubMed
Gibson, W. C., Marshall, T. F., De, C. and Godfrey, D. G. (1980). Numerical analysis of enzyme polymorphism. A new approach to the epidemiology and taxonomy of trypanosomes of the genus Trypanozoon. Advances in Parasitology 18, 175–245.CrossRefGoogle Scholar
Gibson, W., Mehlitz, D., Lanham, S. M. and 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, 335–345.Google ScholarPubMed
Godfrey, D. G. (1978). Identification of economically important parasites. Nature, London 273, 600–604.CrossRefGoogle ScholarPubMed
Hide, G. (1999). The history of sleeping sickness in East Africa. Clinical Microbiological Reviews 12, 112–125.CrossRefGoogle ScholarPubMed
Hide, G., Angus, S., Holmes, P. H., Maudlin, I. and Welburn, S. C. (1998). Comparison of Trypanosoma brucei strains circulating in an endemic and an epidemic sleeping sickness focus. Experimental Parasitology 89, 21–29.CrossRefGoogle Scholar
Hide, G., Buchanan, N., Welburn, S. C., Maudlin, I., Barry, J. D. and Tait, A. (1991). Trypanosoma brucei rhodesiense: Characterization of stocks from Zambia, Kenya and Uganda using repetitive DNA probes. Experimental Parasitology 72, 430–439.CrossRefGoogle ScholarPubMed
Hide, G., Cattand, P., Le Ray, D., Barry, J. D. and Tait, A. (1990). The identification of T. brucei subspecies using repetitive DNA sequences. Molecular and Biochemical Parasitology 39, 213–226.CrossRefGoogle ScholarPubMed
Hide, G. and Tait, A. (1991). The molecular epidemiology of parasites. Experientia 47, 128–142.CrossRefGoogle ScholarPubMed
Hide, G., Tait, A., Maudlin, I. and Welburn, S. C. (1996). The origins, dynamics and generation of Trypanosoma brucei rhodesiense epidemics in East Africa. Parasitology Today 12, 50–55.CrossRefGoogle ScholarPubMed
Hide, G. and Tilley, A. (2001). Use of mobile genetic elements as tools for molecular epidemiology. International Journal for Parasitology 31, 599–602.CrossRefGoogle ScholarPubMed
Hide, G., Tilley, A., Welburn, S., Maudlin, I. and Tait, A. (2000). Trypanosoma brucei: identification of trypanosomes with genotypic similarity to human infective isolates in tsetse isolated from a region free of human sleeping sickness. Experimental Parasitology 96, 67–74.CrossRefGoogle ScholarPubMed
Hide, G., Welburn, S. C., Tait, A. and Maudlin, I. (1994). Epidemiological relationships of Trypanosoma brucei stocks from South East Uganda: Evidence for different population structures in human and non-human trypanosomes. Parasitology 109, 95–111.CrossRefGoogle Scholar
Jamonneau, V., Garcia, A., Ravel, S., Cuny, G., Oury, B., Solano, P., N'Guessan, P., N'Dri, L., Sanon, R., Frézil, J. L. and Truc, P. (2002). Genetic characterization of Trypanosoma brucei gambiense and clinical evolution of human African trypanosomiasis in Côte d'Ivoire. Tropical Medicine and International Health 7, 610–621.CrossRefGoogle ScholarPubMed
Jamonneau, V., Ravel, S., Garcia, A., Koffi, M., Truc, P., Laveissière, C., Herder, S., Grébaut, P., Cuny, G. and Solano, P. (2004 a). Characterization of Trypanosoma brucei s.l. infecting asymptomatic sleeping-sickness patients in Côte d'Ivoire: a new genetic group? Annals of Tropical Medicine and Parasitology 98, 329–337.CrossRefGoogle ScholarPubMed
Jamonneau, V., Ravel, S., Koffi, M., Kaba, D., Zeze, D. G., Ndri, L., Sane, B., Coulibaly, B., Cuny, G. and Solano, P. (2004 b). Mixed infections of trypanosomes in tsetse and pigs and their epidemiological significance in a sleeping sickness focus of Côte d'Ivoire. Parasitology 129, 693–702.CrossRefGoogle Scholar
Jenni, L., Marti, S., Schweizer, J., Betschart, B., Le Page, R. W. F., Wells, J. M., Tait, A., Paindavoine, P., Pays, E. and Steinert, M. (1986). Hybrid formation between African trypanosomes during cyclical transmission. Nature, London 322, 173–175.CrossRefGoogle ScholarPubMed
Kilgour, V. and Godfrey, D. G. (1973). Isoenzymes of alanine aminotransferase as possible specific characters of trypanosomes. Transactions of the Royal Society of Tropical Medicine and Hygiene 67, 11–11.CrossRefGoogle ScholarPubMed
Koffi, M., Solano, P., Barnabé, C., De Meeûs, T., Bucheton, B., Cuny, G. and Jamonneau, V. (2007). Genetic characterisation of Trypanosoma brucei s.l. using microsatellite typing: new perspectives for the molecular epidemiology of human African trypanosomiasis. Infection Genetics and Evolution 7, 675–684.CrossRefGoogle ScholarPubMed
Koffi, M., De Meeûs, T., Bucheton, B., Solano, P., Camara, M., Kaba, D., Cuny, G., Ayala, F. J. and Jamonneau, V. (2009). Population genetics of Trypanosoma brucei gambiense, the agent of sleeping sickness in Western Africa. Proceedings of the National Academy of Sciences, USA 106, 209–214.CrossRefGoogle ScholarPubMed
MacLean, L., Chisi, J. E., Odiit, M., Gibson, W. C., Ferris, V., Picozzi, K. and Sternberg, J. M. (2004). Severity of human african trypanosomiasis in East Africa is associated with geographic location, parasite genotype, and host inflammatory cytokine response profile. Infection and Immunity 72, 7040–7044.CrossRefGoogle ScholarPubMed
MacLean, L., Odiit, M., MacLeod, A., Morrison, L., Sweeney, L., Cooper, A., Kennedy, P. G. and Sternberg, J. M. (2007). Spatially and genetically distinct African trypanosome virulence variants defined by host interferon-gamma response. Journal of Infectious Diseases 196, 1620–1628.CrossRefGoogle ScholarPubMed
MacLeod, A., Tait, A. and Turner, C. M. (2001 b). The population genetics of Trypanosoma brucei and the origin of human infectivity. Philosophical Transactions of the Royal Society of London, B 356, 1035–1044.CrossRefGoogle ScholarPubMed
MacLeod, A., Turner, C. M. R. and Tait, A. (1997). Detection of single copy gene sequences from single trypanosomes. Molecular and Biochemical Parasitology 84, 267–270.CrossRefGoogle ScholarPubMed
MacLeod, A., Turner, C. M. R. and Tait, A. (1999). A high level of mixed Trypanosoma brucei infections in tsetse flies detected by three hypervariable minisatellites. Molecular and Biochemical Parasitology 102, 237–248.CrossRefGoogle ScholarPubMed
MacLeod, A., Turner, C. M. R. and Tait, A. (2001 a). The detection of geographical substructuring of Trypanosoma brucei populations by the analysis of minisatellite polymorphisms. Parasitology 123, 475–482.CrossRefGoogle ScholarPubMed
MacLeod, A., Tweedie, A., Welburn, S. C., Maudlin, I., Turner, M. J. and Tait, A. (2000). Minisatellite marker analysis of Trypanosoma brucei: reconciliation of clonal, panmictic and epidemic population genetic theories. Proceedings of the National Academy of Sciences, USA 97, 13442–13447.CrossRefGoogle Scholar
MacLeod, A., Welburn, S., Maudlin, I., Turner, C. M. and Tait, A. (2001 c). Evidence for multiple origins of human infectivity in Trypanosoma brucei revealed by minisatellite variant repeat mapping. Journal of Molecular Evolution 52, 290–301.CrossRefGoogle ScholarPubMed
Mathieu-Daudé, F. and Tibayrenc, M. (1994). Isozyme variability of Trypanosoma brucei s.l.: genetic, taxonomic, and epidemiological significance. Experimental Parasitology 78, 1–19.CrossRefGoogle ScholarPubMed
Mathieu-Daude, F., Stevens, J., Welsh, J., Tibayrenc, M. and McLelland, M. (1995). Genetic diversity and population structure of Trypanosoma brucei: clonality versus sexuality. Molecular and Biochemical Parasitology 72, 89–101.CrossRefGoogle ScholarPubMed
Maynard Smith, J., Smith, N. H., O'Rourke, M. and Spratt, B. G. (1993). How clonal are bacteria? Proceedings of the National Academy of Sciences, USA 90, 4384–4388.CrossRefGoogle Scholar
Mehlitz, D., Zillmann, U., Scott, C. M., and Godfrey, D. G. (1982). Epidemiological studies on the animal reservoir of Gambiense sleeping sickness. Part III. Characterization of trypanozoon stocks by isoenzymes and sensitivity to human serum. Tropenmedizin und Parasitologie 33, 113–118.Google ScholarPubMed
Miles, M. A., Toye, P. J., Oswald, S. C. and Godfrey, D. G. (1977). The identification by isoenzyme patterns of two distinct strain-groups of Trypanosoma cruzi, circulating independently in a rural area of Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 217–225.CrossRefGoogle Scholar
Morrison, L. J., McCormack, G., Sweeney, L., Likeufack, A. C., Truc, P., Turner, C. M., Tait, A. and MacLeod, A. (2007). Use of multiple displacement amplification to increase the detection and genotyping of trypanosoma species samples immobilized on FTA filters. American Journal of Tropical Medicine and Hygiene 76, 1132–1137.CrossRefGoogle ScholarPubMed
Morrison, L. J., Tait, A., McCormack, G., Sweeney, L., Black, A., Truc, P., Likeufack, A. C., Turner, C. M. and MacLeod, A. (2008). Trypanosoma brucei gambiense Type 1 populations from human patients are clonal and display geographical genetic differentiation. Infection Genetics and Evolution 8, 847–854.CrossRefGoogle ScholarPubMed
Njiokou, F., Laveissière, C., Simo, G., Nkinin, S., Grébaut, P., Cuny, G. and Herder, S. (2006). Wild fauna as a probable animal reservoir for Trypanosoma brucei gambiense in Cameroon. Infection Genetics and Evolution 6, 147–153.CrossRefGoogle ScholarPubMed
Paindavoine, P., Pays, E., Laurent, M., Geltmeyer, Y., Le Ray, D., Mehlitz, D. and 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. and Steinert, M. (1989). Different allele frequencies in Trypanosoma brucei brucei and Trypanosoma brucei gambiense populations. Molecular and Biochemical Parasitology 32, 61–71.CrossRefGoogle ScholarPubMed
Simo, G., Asonganyi, T., Nkinin, S. W., Njiokou, F. and Herder, S. (2006). High prevalence of Trypanosoma brucei gambiense group 1 in pigs from the Fontem sleeping sickness focus in Cameroon. Veterinary Parasitology 139, 57–66.CrossRefGoogle ScholarPubMed
Simo, G., Cuny, G., Demonchy, R. and Herder, S. (2008). Trypanosoma brucei gambiense: study of population genetic structure of Central African stocks using amplified fragment length polymorphism (AFLP). Experimental Parasitology 118, 172–180.CrossRefGoogle ScholarPubMed
Simo, G., Herder, S., Njiokou, F., Asonganyi, T., Tilley, A. and Cuny, G. (2005). Trypanosoma brucei s.l.: characterisation of stocks from Central Africa by PCR analysis of mobile genetic elements. Experimental Parasitology 110, 353–362.CrossRefGoogle ScholarPubMed
Stevens, J. R. and Tibayrenc, M. (1995). Detection of linkage disequilibrium in Trypanosoma brucei isolated from tsetse flies and characterized by RAPD analysis and isoenzymes. Parasitology 110, 181–186.CrossRefGoogle ScholarPubMed
Tait, A. (1970 a). Genetics of NADP isocitrate dehydrogenase in Paramecium aurelia. Nature, London 225, 181–182.CrossRefGoogle ScholarPubMed
Tait, A. (1970 b). Enzyme variation between syngens in Paramecium aurelia. Biochemical Genetics 4, 461–470.CrossRefGoogle ScholarPubMed
Tait, A. (1980). Evidence for diploidy and mating in trypanosomes. Nature, London 287, 536–538.CrossRefGoogle ScholarPubMed
Tait, A., Babiker, E. A. and Le Ray, D. (1984). Enzyme variation in Trypanosoma brucei ssp. I. Evidence for the subspeciation of Trypanosoma brucei gambiense. Parasitology 89, 311–326.CrossRefGoogle ScholarPubMed
Tait, A., Barry, J. D., Wink, R., Sanderson, A. and Crowe, J. S. (1985). Enzyme variation in Trypanosoma brucei ssp. II. Evidence for T.b. rhodesiense being a subset of variants of T.b. brucei. Parasitology 90, 89–100.CrossRefGoogle Scholar
Tait, A. and Turner, C. M. R. (1990). Genetic exchange in Trypanosoma brucei. Parasitology Today 6, 70–75.CrossRefGoogle ScholarPubMed
Terry, R. S., Smith, J. E., Duncanson, P. and Hide, G. (2001). MGE-PCR: a novel approach to the analysis of Toxoplasma gondii strain differentiation using mobile genetic elements. International Journal for Parasitology 31, 155–161.CrossRefGoogle Scholar
Tibayrenc, M., Kjellberg, F. and 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 taxonomic consequences. Proceedings of the National Academy of Sciences, USA 87, 2414–2418.CrossRefGoogle Scholar
Tilley, A. and Hide, G. (2001). Characterization of Trypanosoma brucei stocks by Intergenic Region Typing. Annals of Tropical Medicine and Parasitology 95, 617–621.CrossRefGoogle Scholar
Tilley, A, Welburn, S. C., Fevre, E., Feil, E. J. and Hide, G. (2003). Trypanosoma brucei: Trypanosome strain typing using PCR analysis of mobile genetic elements (MGE-PCR). Experimental Parasitology 104, 26–32.CrossRefGoogle ScholarPubMed
Truc, P., Aerts, D., McNamara, J. J., Claes, Y., Allingham, R., Le Ray, D. and Godfrey, D. G. (1992). Direct isolation in vitro of Typanosoma brucei from man and other animals, and its potential value for the diagnosis of gambian trypanosomiasis. Transactions of the Royol Society of Tropical Medicine and Hygiene 86, 627–629.CrossRefGoogle Scholar
Truc, P., Ravel, S., Jamonneau, V., N'Guessan, P. and Cuny, G. (2002). Genetic variability within Trypanosoma brucei gambiense: evidence for the circulation of different genotypes in human African trypanosomiasis patients in Côte d'Ivoire. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 52–55.CrossRefGoogle ScholarPubMed
Turner, C. M., McLellan, S., Lindergard, L. A., Bisoni, L., Tait, A. and MacLeod, A. (2004). Human infectivity trait in Trypanosoma brucei: stability, heritability and relationship to SRA expression. Parasitology 129, 445–454.CrossRefGoogle ScholarPubMed
Walliker, D., Carter, R. and Morgan, S. (1971). Genetic recombination in malaria parasites. Nature, London 232, 561–562.CrossRefGoogle ScholarPubMed
Walliker, D., Carter, R. and Morgan, S. (1973). Genetic recombination in Plasmodium berghei. Parasitology 66, 309–320.CrossRefGoogle ScholarPubMed
Welburn, S. C., Picozzi, K., Fèvre, E. M., Coleman, P. G., Odiit, M., Carrington, M. and Maudlin, I. (2001). Identification of human infective trypanosomes in animal reservoirs of sleeping sickness in Uganda by means of serum-resistance-associated (SRA) gene. The Lancet 358, 2017–2019.CrossRefGoogle ScholarPubMed
Xong, H. V., Vanhamme, L., Chamekh, M., Chimfwembe, C. E., Van Den Abbeele, J., Pays, A., Van Meirvenne, N., Hamers, R., De Baetselier, P. and Pays, E. (1998). A VSG expression site-associated gene confers resistance to human serum in Trypanosoma rhodesiense. Cell 95, 839–346.CrossRefGoogle ScholarPubMed