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Mixed infections of trypanosomes in tsetse and pigs and their epidemiological significance in a sleeping sickness focus of Côte d'Ivoire

Published online by Cambridge University Press:  18 November 2004

V. JAMONNEAU
Affiliation:
Institut Pierre Richet, BP 1500, Bouake, Côte d'Ivoire, France IRD UR 035, LRCT IRD/CIRAD, Montpellier, France
S. RAVEL
Affiliation:
IRD UR 035, LRCT IRD/CIRAD, Montpellier, France
M. KOFFI
Affiliation:
Institut Pierre Richet, BP 1500, Bouake, Côte d'Ivoire, France IRD UR 035, LRCT IRD/CIRAD, Montpellier, France
D. KABA
Affiliation:
Institut Pierre Richet, BP 1500, Bouake, Côte d'Ivoire, France
D. G. ZEZE
Affiliation:
Institut Pierre Richet, BP 1500, Bouake, Côte d'Ivoire, France
L. NDRI
Affiliation:
Institut Pierre Richet, BP 1500, Bouake, Côte d'Ivoire, France
B. SANE
Affiliation:
Institut Pierre Richet, BP 1500, Bouake, Côte d'Ivoire, France
B. COULIBALY
Affiliation:
Institut Pierre Richet, BP 1500, Bouake, Côte d'Ivoire, France
G. CUNY
Affiliation:
IRD UR 035, LRCT IRD/CIRAD, Montpellier, France
P. SOLANO
Affiliation:
Institut Pierre Richet, BP 1500, Bouake, Côte d'Ivoire, France IRD UR 035, LRCT IRD/CIRAD, Montpellier, France

Abstract

In a sleeping sickness focus of Côte d'Ivoire, trypanosomes were characterized in humans, pigs and tsetse using various techniques. Out of 74 patients, all the 43 stocks isolated by KIVI (Kit for In Vitro Isolation) appeared to belong to only one zymodeme of Trypanosoma brucei gambiense group 1 (the major zymodeme Z3). The only stock isolated on rodents belonged to a different, new, zymodeme (Z50), of T. b. gambiense group 1. From 18 pigs sampled in the same locations as the patients, PCR showed a high proportion of mixed infections of T. brucei s. l. and T. congolense riverine-forest. Zymodemes of T. brucei s. l. from these pigs were different from those found in humans. From a total of 16260 captured tsetse (Glossina palpalis palpalis), 1701 were dissected and 28% were found to be infected by trypanosomes. The most prevalent trypanosome was T. congolense riverine-forest type, followed by T. vivax, T. brucei s. l. and T. congolense savannah type, this latter being associated to the forest type of T. congolense in most cases. Mixed infections by 2 or 3 of these trypanosomes were also found. Use of a microsatellite marker allowed us to distinguish T. b. gambiense group 1 in some of the mature infections in tsetse. Differences in infection rates and in trypanosome genotypes according to the host might indicate that the pig may not be an active animal reservoir for humans in this focus.

Type
Research Article
Copyright
© 2004 Cambridge University Press

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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, 394395.CrossRefGoogle Scholar
CROFT, S. L., KUZOE, F. A. S., RYAN, L. & MOLYNEUX, D. H. ( 1984). Trypanosome infection rates of Glossina spp. in transitional forest-savannah near Bouflé, Ivory Coast. Tropical Medicine and Parasitology 35, 247250.Google Scholar
CUNNINGHAM, I. ( 1977). New culture medium for maintenance of tsetse tissues and growth of trypanosomatids. Journal of Protozoology 21, 325329.CrossRefGoogle Scholar
FRÉZIL, J. L. & CUISANCE, D. ( 1994). Trypanosomiases, maladies d'avenir: leurs perspectives et leurs inconnues. Bulletin de la Société de Pathologie Exotique 87, 391393.Google Scholar
GIBSON, W. C. ( 1986). Will the real Trypanosoma brucei gambiense please stand up? Parasitology today 2, 255257.Google Scholar
GIBSON, W. C., MEHLITZ, D., LANHAM, S. & GODFREY, D. G. ( 1978). The identification of Trypanosoma brucei gambiense in liberian pigs and dogs by resistance to human plasma. Tropical Medicine and Parasitology 29, 335345.Google 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, 174.Google Scholar
HERDER, S., SIMO, G., NKININ, S. & NJIOKOU, F. ( 2002). Identification of trypanosomes in wild animals from Southern Cameroon using the PCR. Parasite 9, 345349.CrossRefGoogle Scholar
HOARE, C. A. ( 1972). The Trypanosomes of Mammalsa Zoological Monograph. Blackwell Scientific Publications, Oxford.
JACCARD, P. ( 1908). Nouvelles recherches sur la distribution florale. Bulletin de la Société Vaudoise de Sciences Naturelles 44, 223270.Google Scholar
JAMONNEAU, V., BARNABE, C., KOFFI, M., N'GUESSAN, P., KOFFI, A., SANE, B., CUNY, G. & SOLANO, P. ( 2003). Identification of Trypanosoma brucei circulating in a sleeping sickness focus in Côte d'Ivoire: assessment of genotype selection by the isolation method. Infection, Genetics and Evolution 3, 143149.CrossRefGoogle Scholar
JAMONNEAU, V., GARCIA, A., RAVEL, S., CUNY, G., OURY, B., SOLANO, P., N'GUESSAN, P., N'DRI, L., SANON, R., FREZIL, J. L. & TRUC, P. ( 2002). Genetic characterisation of Trypanosoma brucei ssp. and clinical evolution of Human African Trypanosomiasis in Côte d'Ivoire. Tropical Medicine and International Health 7, 610621.Google Scholar
JAMONNEAU, V., RAVEL, S., GARCIA, A., KOFFI, M., LAVEISSIERE, C., HERDER, S., GREBAUT, P., CUNY, G. & SOLANO, P. ( 2004). Genetic characterization of trypanosomes infecting untreated but asymptomatic sleeping sickness patients in Côte d'Ivoire: a new genetic group? Annals of Tropical Medicine and Parasitology 98, 329337.Google Scholar
JORDAN, A. M. ( 1964). Trypanosome infection rates in Glossina morsitans submorsitans newst. in Northern Nigeria. Bulletin of Entomological Research 55, 219231.CrossRefGoogle Scholar
KAGERUKA, P. ( 1987). Trypanosomose dans les élevages porcins du Bas-Zaïre. Revue d'Elevage et de Médecine Vétérinaire des Pays Tropicaux 40, 4953.Google Scholar
KUKLA, B. A., MAJIWA, P. A. O., YOUNG, J. R., MOLOO, S. K. & OLE-MOI YOI, O. ( 1987). Use of species-specific DNA probes for detection and identification of trypanosome infections in tsetse flies. Parasitology 95, 116.CrossRefGoogle Scholar
LAVEISSIERE, C. & GREBAUT, P. ( 1990). Recherches sur les pièges à glossines. Mise au point d'un modèle économique: le piège “Vavoua”. Tropical Medicine and Parasitology 41, 185192.Google Scholar
LEFRANÇOIS, T., SOLANO, P., DE LA ROCQUE, S., BENGALY, Z., REIFENBERG, J. M., KABORE, I. & CUISANCE, D. ( 1998). New epidemiological features on animal trypanosomosis by molecular analysis in the pastoral zone of Sidéradougou, Burkina Faso. Molecular Ecology 7, 897904.CrossRefGoogle Scholar
LEHANE, M. J., MSANGI, A. R., WHITACKER, C. J. & LEHANE, S. M. ( 2000). Grouping of trypanosome species in mixed infections in Glossina pallidipes. Parasitology 120, 583592.CrossRefGoogle Scholar
LETCH, C. A. ( 1984). A mixed population of Trypanozoon in Glossina palpalis palpalis from Ivory Coast. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 627630.CrossRefGoogle Scholar
LUMSDEN, W. H. R., KIMBER, C. D., EVANS, D. A. & DOIG, S. J. ( 1979). Trypanosoma brucei: miniature anion-exchange centrifugation technique for detection of low parasitaemias: adaptation for field-use. Transactions of the Royal Society of Tropical Medecine and Hygiene 73, 312317.CrossRefGoogle Scholar
MAGNUS, E., VERVOORT, T. & VAN MEIRVENNE, N. ( 1978). A Card-Agglutination Test with stained Trypanosomes (C.A.T.T.) for the serological diagnosis of T. b. gambiense trypanosomiasis. Annales de la Société belge de Médecine Tropicale 58, 169176.Google Scholar
MAJIWA, P. A. O., MAINA, M., WAITUMBI, J. N., MIHOK, S. & ZWEYGARTH, E. ( 1993). Trypanosoma (Nannomonas) congolense: molecular characterization of a new genotype from Tsavo, Kenya. Parasitology 106, 151162.CrossRefGoogle Scholar
MAJIWA, P. A. O. & OTIENO, L. H. ( 1990). Recombinant DNA probes reveal simultaneous infection of tsetse flies with different species. Molecular and Biochemical Parasitology 40, 245254.CrossRefGoogle Scholar
MAJIWA, P. A. O., THATTHI, R., MOLOO, S. K., NYEKO, J. H. P., OTIENO, L. H. & MALOO, S. ( 1994). Detection of trypanosome infections in the saliva of tsetse flies and buffy-coat samples from antigenemic but aparasitaemic cattle. Parasitology 108, 313322.CrossRefGoogle Scholar
MASIGA, D. K., McNAMARA, J. J., LAVEISSIÈRE, C., TRUC, P. & GIBSON, W. C. ( 1996). A high prevalence of mixed trypanosome infections in tsetse flies in Sinfra, Côte d'Ivoire, detected by DNA amplification. Parasitology 112, 7580.CrossRefGoogle Scholar
MASIGA, D. K., SMYTH, A. J., HAYES, P., BROMIDGE, T. J. & GIBSON, W. C. ( 1992). Sensitive detection of trypanosomes in tsetse flies by DNA amplification. International Journal of Parasitology 22, 909918.CrossRefGoogle Scholar
MAUDLIN, I. & WELBURN, S. C. ( 1994). Maturation of trypanosome infections in tsetse. Experimental Parasitology 79, 202205.CrossRefGoogle Scholar
McNAMARA, J. J., LAVEISSIERE, C. & MASIGA, D. K. ( 1995). Multiple trypanosome infections in wild tsetse in Côte d'Ivoire detected by PCR analysis and DNA probes. Acta Tropica 59, 8592.CrossRefGoogle Scholar
MEHLITZ, D. ( 1986). Le réservoir animal de la maladie du sommeil à Trypanosoma brucei gambiense. Etudes et synthèses de l'IEMVT, N°18.
MEHLITZ, D., ZILLMANN, U., SCOTT, C. M. & 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. Tropical and Medicine Parasitology 33, 113118.Google Scholar
MORLAIS, I., GREBAUT, P., BODO, J. M., DJOHA, S., CUNY, G. & HERDER, S. ( 1998). Detection and amplification of trypanosomes by PCR in wild tsetse flies in Cameroon. Acta Tropica 70, 109117.CrossRefGoogle Scholar
MOSER, D. R., COOK, G. A., OCHS, D. E., BAILEY, C. P., McKANE, M. R. & DONELSON, J. E. ( 1989). Detection of Trypanosoma congolense and T. brucei subspecies by DNA amplification using the Polymerase Chain Reaction. Parasitology 99, 5766.Google Scholar
MURRAY, M., MURRAY, P. K. & McINTYRE, W. I. M. ( 1977). An improved parasitological technique for the diagnosis of African trypanosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 325326.CrossRefGoogle Scholar
NEKPENI, E. B., EOUZAN, J. P. & DAGNOGO, M. ( 1991). Infection de Glossina palpalis palpalis par les trypanosomes en zone forestière de Gagnoa en Côte d'Ivoire. Tropical Medicine and Parasitology 42, 399403.Google Scholar
NOIREAU, F., GOUTEUX, J. P., TOUDIC, A., SAMBA, F. & FREZIL, J. L. ( 1986). Importance épidémiologique du réservoir animal à Trypanosoma brucei gambiense au Congo. 1. Prévalence des trypanosomoses animales dans les foyers de maladie du sommeil. Tropical Medicine and Parasitology 37, 393398.Google Scholar
RADWANSKA, M., CHAMEKH, M., VANHAMME, L., CLAES, F., MAGEZ, S., MAGNUS, E., DE BAETSELIER, P., BUSCHER, P. & PAYS, E. ( 2002). The serum resistance-associated gene as a diagnostic tool for the detection of Trypanosoma brucei rhodesiense. American Journal of Tropical Medicine and Hygiene 67, 684690.CrossRefGoogle Scholar
RAVEL, S., GREBAUT, P., CUISANCE, D. & CUNY, G. ( 2003). Monitoring the developmental status of Trypanosoma brucei gambiense in the tsetse fly by means of PCR analysis of anal and saliva drops. Acta Tropica 88, 161165.CrossRefGoogle Scholar
RAVEL, S., MARIANI, C., GREBAUT, P., JAMONNEAU, V., CUISANCE, D. & CUNY, G. ( 2004). Inhibition of the DNA amplification of trypanosomes present in tsetse flies midguts: implications for the identification of trypanosome species in wild tsetse flies. Parasite 11, (in the Press).CrossRefGoogle Scholar
SANE, B., LAVEISSIERE, C. & MEDA, H. A. ( 2000). Répartition spatiale et préférences trophiques de Glossina palpalis palpalis dans le foyer forestier de Zoukougbeu (Côte d'Ivoire). Implications épidémiologiques. Parasite 7, 241244.Google Scholar
SNEATH, P. H. A. & SOKAL, R. R. ( 1973). Numerical taxonomy. In The Principles and Practice of Numerical Classification (ed. Kennedy, D. & Park, R. B.), p. 573. W.H. Freeman and Co, San Francisco.
SOLANO, P., ARGIRO, L., YAO, Y., REIFENBERG, J. M. & DUVALLET, G. ( 1995). Field application of the Polymerase Chain Reaction to the detection and characterization of trypanosomes in Glossina longipalpis (Diptera: Glossinidae) in Côte d'Ivoire. Molecular Ecology 4, 781785.CrossRefGoogle Scholar
SOLANO, P., GUÉGAN, J. F., REIFENBERG, J. M. & THOMAS, F. ( 2001). Trying to identify, predict and explain the presence of african trypanosomes in tsetse flies. Journal of Parasitology 87, 10581063.CrossRefGoogle Scholar
SOLANO, P., KONE, A., GARCIA, A., SANE, B., MICHEL, V., MICHEL, J. F., COULIBALY, B., JAMONNEAU, V., KABA, D., DUPONT, S. & FOURNET, F. ( 2003). Rôle des déplacements des malades dans l'épidémiologie de la Trypanosomose Humaine Africaine dans le foyer de Bonon, Côte d'Ivoire. Médecine Tropicale 63, 577582.Google Scholar
SOLANO, P., MICHEL, J. F., LEFRANÇOIS, T., DE LA ROCQUE, S., SIDIBÉ, I., ZOUNGRANA, A. & CUISANCE, D. ( 1999). Polymerase Chain Reaction as a diagnosis tool for detecting trypanosomes in naturally infected cattle in Burkina Faso. Veterinary Parasitology 86, 95103.CrossRefGoogle Scholar
SQUIRE, F. A. ( 1954). Observations on the incidence of trypanosomes in Glossina palpalis in Sierra Leone. Bulletin of Entomological Research 45, 797801.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, 627629.CrossRefGoogle Scholar
TRUC, P., FORMENTY, P., DIALLO, P. B., KOMOIN-OKA, C. & LAUGINIÉ, F. ( 1997). Confirmation of two distinct classes of zymodemes of Trypanosoma brucei infecting man and wild mammals in Côte d'Ivoire: suspected difference in pathogenicity. Annals of Tropical Medicine and Parasitology 91, 951956.CrossRefGoogle Scholar
TRUC, P., MATHIEU-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, 127135.CrossRefGoogle Scholar
TRUC, P., RAVEL, S., JAMONNEAU, V., N'GUESSAN, P. & 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, 14.CrossRefGoogle Scholar
VAN HOOF, L., HENRARD, C. & PEEL, E. ( 1937). Rôle du porc comme réservoir de Trypanosoma gambiense. Comptes Rendus de la Société de Biologie 126, 7275.Google Scholar
WALSH, P. S., METZGER, D. A. & HIGUCHI, R. ( 1991). Chelex® 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10, 506513.Google Scholar
WELBURN, S. C., PICOZZI, K., FEVRE, E. M., COLEMAN, P. G., ODIIT, M., CARRINGTON, M. & MAUDLIN, I. ( 2001). Identification of human-infective trypanosomes in animal reservoir of sleeping sickness in Uganda by means of serum-resistance-associated (SRA) gene. Lancet 358, 20172019.CrossRefGoogle Scholar
WORLD HEALTH ORGANIZATION ( 1998). La Trypanosomiase Africaine: Lutte et Surveillance. WHO Technical Report Series, No. 881. WHO, Geneva.
WOOLHOUSE, M. E. J., McNAMARA, J. J., HARGROVE, J. W. & BEALBY, K. A. ( 1996). Distribution and abundance of trypanosome (subgenus Nannomonas) infections of the tsetse fly Glossina pallidipes in Southern Africa. Molecular Ecology 5, 1118.CrossRefGoogle Scholar