Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-24T09:47:32.430Z Has data issue: false hasContentIssue false
  • English
  • Français

An isoenzyme survey of Trypanosoma brucei s.l. from the Central African subregion: population structure, taxonomic and epidemiological considerations

Published online by Cambridge University Press:  13 May 2004

F. NJIOKOU ,
S. W. NKININ ,
P. GRÉBAUT ,
L. PENCHENIER ,
C. BARNABÉ ,
M. TIBAYRENC  and
S. HERDER
F. NJIOKOU
Affiliation:
OCEAC, Laboratoire de Recherche sur les Trypanosomoses, BP 288, Yaoundé, Cameroun Université de Yaoundé I, Faculté des Sciences, BP 812, Yaoundé, Cameroun
S. W. NKININ
Affiliation:
OCEAC, Laboratoire de Recherche sur les Trypanosomoses, BP 288, Yaoundé, Cameroun
P. GRÉBAUT
Affiliation:
Laboratoire de Recherche et de Coordination sur les Trypanosomoses (IRD-CIRAD) TA 207/G, Campus international de Baillarguet, 34398 Montpellier Cedex 5, France
L. PENCHENIER
Affiliation:
Laboratoire de Recherche et de Coordination sur les Trypanosomoses (IRD-CIRAD) TA 207/G, Campus international de Baillarguet, 34398 Montpellier Cedex 5, France
C. BARNABÉ
Affiliation:
Génétique des Maladies Infectieuses, Unité Mixte de Recherche Centre National de la Recherche Scientifique (CNRS)/Institut de Recherche pour le Développement (IRD) n°9926, IRD, BP 64501, 34394 Montpellier Cedex 05, France
M. TIBAYRENC
Affiliation:
Génétique des Maladies Infectieuses, Unité Mixte de Recherche Centre National de la Recherche Scientifique (CNRS)/Institut de Recherche pour le Développement (IRD) n°9926, IRD, BP 64501, 34394 Montpellier Cedex 05, France
S. HERDER
Affiliation:
Laboratoire de Recherche et de Coordination sur les Trypanosomoses (IRD-CIRAD) TA 207/G, Campus international de Baillarguet, 34398 Montpellier Cedex 5, France
Get access Rights & Permissions [Opens in a new window]

Abstract

In order to improve our knowledge about the taxonomic status and the population structure of the causative agent of Human African Trypanosomiasis in the Central African subregion, 169 newly isolated stocks, of which 16 came from pigs, and 5 reference stocks, were characterized by multilocus enzyme electrophoresis, for 17 genetic loci. We identified 22 different isoenzyme profiles or zymodemes, many of which showed limited differences between them. These zymodemes were equated to multilocus genotypes. UPGMA dendrograms revealed one main group: Trypanosoma brucei gambiense group I and 3 T. brucei ‘non-gambiense’ stocks. T. b. gambiense group I zymodemes were very homogenous, grouping all the human stocks and 31% of the pig stocks. Two main zymodemes (Z1 and Z3) grouping 74% of the stocks were found in different remote countries. The genetic distances were relatively high in T. brucei ‘non-gambiense’ zymodemes, regrouping 69% of pig stocks. The analysis of linkage disequilibrium was in favour of a predominantly clonal population structure. This was supported by the ubiquitous occurrence of the main zymodemes, suggesting genetic stability in time and space of this parasite's natural clones. However, in some cases an epidemic population structure could not be ruled out. Our study also suggested that the domestic pig was a probable reservoir host for T. b. gambiense group I in Cameroon.

Keywords

Human African TrypanosomiasisTrypanosoma brucei s.lmultilocus isoenzyme electrophoresisclonal population structure
Type
Research Article
Information
Parasitology , Volume 128 , Issue 6 , June 2004 , pp. 645 - 653
Copyright
2004 Cambridge University Press

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

AERTS, D., TRUC, P., PENCHENIER, L., CLAES, Y. & LE RAY, D. ( 1992). A kit for in vitro isolation of trypanosomes in the field: first trial with sleeping sickness patients in the Congo Republic. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 394–395.CrossRefGoogle Scholar
BARNABÉ, C., BRISSE, S. & TIBAYRENC, M. ( 2000). Population structure and genetic typing of Trypanosoma cruzi, the agent of Chagas disease: a multilocus enzyme electrophoresis approach. Parasitology 120, 1–14.CrossRefGoogle Scholar
BUREAU, P., LUCAS, P. & NANGOUMA, A. ( 2000). La Trypanosomiase Humaine Africaine (THA) en Republique Centrafricaine: quelques données pour 1999. Bulletin de Liaison et de Documentation de l'OCEAC 33, 47–48.Google Scholar
BURRI, C., NKUNKU, S., MEROLLE, A., SMITH, T., BLUM, J. & BRUN, R. ( 2000). Efficacy of new, concise schedule for melarsoprol in treatment of sleeping sickness caused by Trypanosoma brucei gambiense: a randomised trial. The Lancet 335, 1419–1425.CrossRefGoogle Scholar
CATTAND, P. ( 1994). Trypanosomiase Humaine Africaine. Situation épidémiologique actuelle, une recrudescence alarmante de la maladie. Bulletin de la Société de Pathologie Exotique 87, 307–310.Google Scholar
CIBULSKIS, R. E. ( 1992). Genetic variation in Trypanosoma brucei and the epidemiology of sleeping sickness in the Lambwe valley, Kenya. Parasitology 104, 15–34.CrossRefGoogle Scholar
CUNNINGHAM, I. ( 1977). New culture medium for maintenance of tsetse tissues and growth of trypanosomatids. Journal of Protozoology 24, 325–329.CrossRefGoogle Scholar
FELSENSTEIN, J. ( 1989). PHYLIP – Phylogeny Inference Package (Version 3.2). Cladistics 5, 164–166.Google Scholar
GIBSON, W. C. ( 1986). Will the real Trypanosoma brucei gambiense please stand up. Parasitology Today 2, 255–257.CrossRefGoogle Scholar
GIBSON, W. C., MEHLITZ, D., LANHAM, S. & 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 Scholar
GIBSON, W. C. & STEVENS, J. ( 1999). Genetic exchange in the trypanosomatidae. Advances in Parasitology 43, 1–46.CrossRefGoogle Scholar
GODFREY, D. G., BAKER, R. D., RICKMAN, L. R. & MEHLITZ, D. ( 1990). The distribution, relationships and identification of enzymatic variants within the subgenus Trypanozoon. Advances in Parasitology 29, 1–39.Google Scholar
HIDE, G., WELBURN, S. C., TAIT, A. & MAUDLIN, M. ( 1994). Epidemiological relationships of Trypanosoma brucei stocks from South East Uganda: evidence for different population structure in human infective and non-human infective isolates. Parasitology 109, 95–111.CrossRefGoogle Scholar
JACCARD, P. ( 1908). Nouvelles recherches sur la distribution florale. Bulletin de la Société Vaudoise de Sciences Naturelles 44, 223–270.Google Scholar
JAMONNEAU, V., N'GUESSAN, P., N'DRI, L., SIMARRO, P. & TRUC, P. ( 2000). Exploration of the distribution of Trypanosoma brucei ssp in West Africa, by multilocus enzyme electrophoresis. Annals of Tropical Medicine and Parasitology 94, 643–649.CrossRefGoogle Scholar
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, 173–175.CrossRefGoogle Scholar
LE MARDELEY, P., CATTAND, P., LOUIS, F. J. & CHAMBON, R. ( 1995). Situation de la Trypanosomiase Humaine en Afrique Centrale en 1994. Interprétation pragmatique des données. Bulletin de Liaison et de Documentation de lOCEAC 28, 153–157.Google Scholar
MAYNARDSMITH, J., SMITH, N. H., O'ROURKE, M. & SPRATT, B. G. ( 1993). How clonal are bacteria? Proceedings of the National Academy of Sciences, USA 90, 84–88.Google Scholar
MacLEOD, A., TWEEDIE, A., WELBURN, I., TURNER, C. M. R. & TAIT, A. ( 2000). Minisatellite marker analysis of Trypanosoma brucei: reconciliation of clonal, panmictic and epidemic population genetic structures. Proceedings of the National Academy of Sciences, USA 97, 13442–13447.CrossRefGoogle Scholar
McNAMARA, J. J., BAILEY, J. W., SMITH, D. H., WAKHOOLI, S. & GODFREY, D. G. ( 1995). Isolation of Trypanosoma brucei gambiense from Northern Uganda: Evaluation of the Kit for in vitro isolation (KIVI) in an epidemic focus. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 388–389.CrossRefGoogle Scholar
MEHLITZ, D., ZILLMANN, U., SCOTT, C. M. & GODFREY, D. G. ( 1982). Epidemiological studies on the animal reservoir of gambiense sleeping sickness. 3: Characterization of Trypanozoon stocks by isoenzyme and sensitivity to human serum. Tropenmedizin und Parasitologie 33, 113–118.Google Scholar
NEI, M. ( 1972). Genetic distances between populations. The American Naturalist 106, 283–292.CrossRefGoogle Scholar
NKININ, S. W., NJIOKOU, F., GRÉBAUT, P., PENCHENIER, L., BUREAU, P., SIMO, G. & HERDER, S. ( 1999). Isoenzyme characterization of Trypanosoma brucei s.l. stocks from different foci in the Central African Region. Bulletin de Liaison et de Documentation de l'OCEAC 32, 9–16.Google Scholar
NKININ, S. W., NJIOKOU, F., PENCHENIER, L., GRÉBAUT, P., SIMO, G. & HERDER, S. ( 2002). Characterization of Trypanosoma brucei s.l. subspecies by isoenzymes in domestic pigs from the Fontem sleeping sickness focus of Cameroon. Acta Tropica 81, 225–232.Google Scholar
PAINDAVOINE, P., ZAMPETTI-BOSSELER, F., COQUELET, H., PAYS, E. & STEINERT, M. ( 1989). Different alleles frequencies in Trypanosoma brucei brucei and Trypanosoma brucei gambiense populations. Molecular Biochemical and Parasitology 32, 61–72.CrossRefGoogle Scholar
SMITH, D. H., PEPIN, J. & STICH, A. H. R. ( 1998). Human african trypanosomiasis: an emerging public health crisis. British Medical Bulletin 54, 341–355.CrossRefGoogle Scholar
SNEATH, P. H. A. & SOKAL, R. R. ( 1973). The principle and practice of numerical classification. In Numerical Taxonomy ( ed. Kennedy, D. & Park, R. B.), pp. 537. Freeman, San Francisco.
TAIT, A. ( 1980). Evidence for diploidy and mating in trypanosomes. Nature, London 237, 536–538.CrossRefGoogle Scholar
TIBAYRENC, M. ( 1995). Population genetics of parasitic protozoa and other microorganisms. Advances in Parasitology 36, 47–115.CrossRefGoogle Scholar
TIBAYRENC, M. ( 1999). Toward an integrated genetic epidemiology of parasitic protozoa and other pathogens. Annual Review of Genetics 33, 449–477.CrossRefGoogle Scholar
TIBAYRENC, M. & AYALA, F. J. ( 1988). Isoenzyme variability in Trypanosoma cruzi, the agent of Chagas' disease: genetical, taxonomical and epidemiological significance. Evolution 42, 227–292.Google Scholar
TIBAYRENC, M. & AYALA, F. J. ( 1991). Towards a population genetics of microorganisms: the clonal theory of parasitic protozoa. Parasitology Today 7, 228–232.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, 2414–2418.CrossRefGoogle Scholar
TIBAYRENC, M., KJELLBER, G.F., ARNAUD, J., OURY, B., BRENIERE, S. F., DARDE, M. & AYALA, F. J. ( 1991). Are eucaryotic microorganisms clonal or sexual? A population genetics vantage. Proceedings of the National Academy of Sciences, USA 88, 5129–5133.CrossRefGoogle Scholar
TIBAYRENC, M., WARD, P., MOYA, A. & AYALA, F. J. ( 1986). Natural populations of Trypanosoma cruzi, the agent of Chagas' disease, have a complex multiclonal structure. Proceedings of the National Academy of Sciences, USA 83, 115–119.CrossRefGoogle Scholar
TRUC, P., MATHIAU-DAUDE, F. & TIBAYRENC, M. ( 1991). Multilocus isoenzyme identification of Trypanosoma brucei stocks isolated in Central Africa: evidence for an animal reservoir of sleeping sickness in Congo. Acta Tropica 49, 127–135.CrossRefGoogle Scholar
TRUC, P., AERTS, D., McNAMARA, J. J., CLAES, Y., ALLINGHAM, R., LE RAY, D. & GODFREY, D. G. ( 1992). Direct isolation in vitro of Trypanosoma brucei from man and other animals, and its potential value for the diagnosis of gambian trypanosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 627–629.CrossRefGoogle Scholar
TRUC, P. & TIBAYRENC, M. ( 1993). Population genetics of Trypanosoma brucei in Central Africa: taxonomic and epidemiological significance. Parasitology 106, 137–149.CrossRefGoogle Scholar
TRUC, P., FORMENTY, P., DIALLO, P. B., KOMOIN-OKA, C. & LAUGINIE, F. ( 1997 a). Identification of trypanosomes isolated by KIVI from wild animals in Côte d'Ivoire: diagnostic, taxonomic and epidemiological considerations. Acta Tropica 67, 1–10.Google Scholar
TRUC, P., FORMENTY, P., DIALLO, P. B., KOMOIN-OKA, C. & LAUGINIE, F. ( 1997 b). Confirmation of two distinct classes of zymodemes infecting man and wild animals in Côte d'Ivoire: suspected differences in pathogenicity. Annals of Tropical Medicine and Parasitology 91, 951–956.Google Scholar
WORLD HEALTH ORGANIZATON ( 1998). Control and Surveillance of African Trypanosomiasis.WHO Technical Report Series No. 881, Geneva.