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Emerging trends in the diagnosis of Human African Trypanosomiasis

Published online by Cambridge University Press:  12 April 2010

MAGDALENA RADWANSKA*
Affiliation:
Science Officer for Strategic Activities, European Cooperation for Science and Technology, COST Office, Avenue Louise 149, B-1050Brussels, Belgium
*
*Corresponding author: Tel: +32-2-533.38.13 Fax: +32-2-533.38.90. E-mail: mradwanska@cost.esf.org

Summary

Human African trypanosomiasis (HAT) or sleeping sickness is caused by protozoan parasites Trypanosoma brucei gambiense and T. b. rhodesiense. Despite the enormous technological progress in molecular parasitology in recent years, the diagnosis of HAT is still problematic due to the lack of specific tools. To date, there are two realities when it comes to HAT; the first one being the world of modern experimental laboratories, equipped with the latest state-of-the-art technology, and the second being the world of HAT diagnosis, where the latest semi-commercial test was introduced 30 years ago (Magnus et al.1978). Hence, it appears that the lack of progress in HAT diagnosis is not primarily due to a lack of scientific interest or a lack of research funds, but mainly results from the many obstacles encountered in the translation of basic research into field-applicable diagnostics. This review will provide an overview of current diagnostic methods and highlight specific difficulties in solving the shortcomings of these methods. Future perspectives for accurate, robust, affordable diagnostics will be discussed as well.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Asonganyi, T., Bedifeh, B. A., Ade, S. S. and Ngu, J. L. (1994). An evaluation of the reactivity of the card agglutination test for trypanosomiasis (CATT) reagent in the Fontem sleeping sickness focus, Cameroon. African Journal of Medicine and Medical Science 23, 3946.Google ScholarPubMed
Authié, E., Muteti, D. K., Mbawa, Z. R., Lonsdale-Eccles, J. D., Webster, P. and Wells, C. W. (1992). Identification of a 33-kilodalton immunodominant antigen of Trypanosoma congolense as a cysteine protease. Molecular and Biochemical Parasitology 56, 103116.CrossRefGoogle ScholarPubMed
Balasegaram, M., Young, H., Chappuis, F., Priotto, G., Raguenaud, M. E. and Checchi, F. (2009). Effectiveness of melarsoprol and eflornithine as first-line regimens for gambiense sleeping sickness in nine Medecins Sans Frontieres programmes. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 280290.CrossRefGoogle Scholar
Baral, T. N., Magez, S., Stijlemans, B., Conrath, K., Vanhollebeke, B., Pays, E., Muyldermans, S. and De Baetselier, P. (2006). Experimental therapy of African trypanosomiasis with a nanobody-conjugated human trypanolytic factor. Nature Medicine 12, 580584.CrossRefGoogle ScholarPubMed
Chappuis, F., Loutan, L., Simarro, P., Lejon, V. and Büscher, P. (2005). Options for field diagnosis of human african trypanosomiasis. Clinical Microbiology Reviews 18, 133146.Google Scholar
Cortez-Retamozo, V., Backmann, N., Senter, P. D., Wernery, U., De Baetselier, P., Muyldermans, S. and Revets, H. (2004). Efficient cancer therapy with a nanobody-based conjugate. Cancer Research 64, 28532857.Google Scholar
Courtioux, B., Boda, C., Vatunga, G., Pervieux, L., Josenando, T., M'Eyi, P. M., Bouteille, B., Jauberteau-Marchan, M. O. and Bisser, S. (2006). A link between chemokine levels and disease severity in human African trypanosomiasis. International Journal for Parasitology 36, 10571065.Google Scholar
Cox, A., Tilley, A., McOdimba, F., Fyfe, J., Eisler, M., Hide, G. and Welburn, S. (2005). A PCR based assay for detection and differentiation of African trypanosome species in blood. Experimental Parasitology 111, 2429.Google Scholar
Deborggraeve, S., Claes, F., Laurent, T., Mertens, P., Leclipteux, T., Dujardin, J. C., Herdewijn, P. and Büscher, P. (2006). Molecular dipstick test for diagnosis of sleeping sickness. Journal of Clinical Microbiology 44, 28842889.Google Scholar
Deckers, N., Saerens, D., Kanobana, K., Conrath, K., Victor, B., Wernery, U., Vercruysse, J., Muyldermans, S. and Dorny, P. (2009). Nanobodies, a promising tool for species-specific diagnosis of Taenia solium cysticercosis. International Journal for Parasitology 39, 625633.CrossRefGoogle ScholarPubMed
Djoba Siawaya, J. F., Beyers, N., van Helden, P. and Walzl, G. (2009). Differential cytokine secretion and early treatment response in patients with pulmonary tuberculosis. Clinical Experimental Immunology 156, 6977.Google Scholar
Docampo, R. and Moreno, S. N. (2003). Current chemotherapy of human African trypanosomiasis. Parasitology Research 90 (Supp 1), S10S13.Google Scholar
Dukes, P., Gibson, W. C., Gashumba, J. K., Hudson, K. M., Bromidge, T. J., Kaukus, A., Asonganyi, T. and Magnus, E. (1992). Absence of the LiTat 1.3 (CATT antigen) gene in Trypanosoma brucei gambiense stocks from Cameroon. Acta Tropica 51, 123134.CrossRefGoogle ScholarPubMed
Dukes, P., Rickman, L. R., Killick-Kendrick, R., Kakoma, I., Wurapa, F. K., de Raadt, P. and Morrow, R. (1984). A field comparison of seven diagnostic techniques for human trypanosomiasis in the Luangwa Valley, Zambia. Tropenmedizin und Parasitologie 35, 141147.Google Scholar
Ellie, E., Vital, A., Steck, A. J., Julien, J., Henry, P. and Vital, C. (1995). High-grade B-cell cerebral lymphoma in a patient with anti-myelin-associated glycoprotein IgM paraproteinemic neuropathy. Neurology 45, 378381.CrossRefGoogle Scholar
Enyaru, J. C., Matovu, E., Akol, M., Sebikali, C., Kyambadde, J., Schmidt, C., Brun, R., Kaminsky, R., Ogwal, L. M. and Kansiime, F. (1998). Parasitological detection of Trypanosoma brucei gambiense in serologically negative sleeping-sickness suspects from north-western Uganda. Annals of Tropical Medicine and Parasitology 92, 845850.Google Scholar
Fairlamb, A. H., Henderson, G. B. and Cerami, A. (1989). Trypanothione is the primary target for arsenical drugs against African trypanosomes. Proceedings of the National Academy of Sciences, USA 86, 26072611.CrossRefGoogle ScholarPubMed
Garcia, A., Jamonneau, V., Magnus, E., Laveissière, C., Lejon, V., N'Guessan, P., N'Dri, L., Van Meirvenne, N. and Büscher, P. (2000). Follow-up of Card Agglutination Trypanosomiasis Test (CATT) positive but apparently aparasitaemic individuals in Cote d'Ivoire: evidence for a complex and heterogeneous population. Tropical Medicine and International Health 5, 786793.CrossRefGoogle ScholarPubMed
Goringer, H. U., Homann, M. and Lorger, M. (2003). In vitro selection of high-affinity nucleic acid ligands to parasite target molecules. International Journal for Parasitology 33, 13091317.CrossRefGoogle ScholarPubMed
Gutierrez, C., Corbera, J. A., Doreste, F. and Büscher, P. (2004). Use of the miniature anion exchange centrifugation technique to isolate Trypanosoma evansi from goats. Annals of the New York Academy of Science 1026, 149151.CrossRefGoogle ScholarPubMed
Hainard, A., Tiberti, N., Robin, X., Lejon, V., Ngoyi, D. M., Matovu, E., Enyaru, J. C., Fouda, C., Ndung'u, J. M., Lisacek, F., Müller, M., Turck, N. and Sanchez, J. C. (2009). A combined CXCL10, CXCL8 and H-FABP panel for the staging of Human African Trypanosomiasis patients. PLoS Neglected Tropical Diseases 3, e459.Google Scholar
Hamers-Casterman, C., Atarhouch, T., Muyldermans, S., Robinson, G., Hamers, C., Songa, E. B., Bendahman, N. and Hamers, R. (1993). Naturally occurring antibodies devoid of light chains. Nature 363, 446448.CrossRefGoogle ScholarPubMed
Heby, O., Persson, L. and Rentala, M. (2007). Targeting the polyamine biosynthetic enzymes: a promising approach to therapy of African sleeping sickness, Chagas' disease, and leishmaniasis. Amino Acids 33, 359366.Google Scholar
Hide, G. and Tilley, A. (2001). Use of mobile genetic elements as tools for molecular epidemiology. International Journal for Parasitology 31, 599602.CrossRefGoogle ScholarPubMed
Homann, M., Lorger, M., Engstler, M., Zacharias, M. and Goringer, H. U. (2006). Serum-stable RNA aptamers to an invariant surface domain of live African trypanosomes. Combinatorial Chemistry and High Throughput Screening 9, 491499.Google Scholar
Iten, M., Matovu, E., Brun, R. and Kaminsky, R. (1995). Innate lack of susceptibility of Ugandan Trypanosoma brucei rhodesiense to DL-alpha-difluoromethylornithine (DFMO). Tropical Medicine and Parasitology 46, 190194.Google Scholar
Jackson, D. G., Windle, H. J. and Voorheis, H. P. (1993). The identification, purification, and characterization of two invariant surface glycoproteins located beneath the surface coat barrier of bloodstreamforms of Trypanosoma brucei. Journal of Biological Chemistry 268, 80858095.CrossRefGoogle Scholar
Jamonneau, V., Truc, P., Garcia, A., Magnus, E. and Büscher, P. (2000). Preliminary evaluation of LATEX/T. b. gambiense and alternative versions of CATT/T. b. gambiense for the serodiagnosis of human african trypanosomiasis of a population at risk in Cote d'Ivoire: considerations for mass-screening. Acta Tropica 76, 175183.Google Scholar
Juffermans, N. P., Verbon, A., van Deventer, S. J., van Deutekom, H., Belisle, J. T., Ellis, M. E., Speelman, P. and van der Poll, T. (1999). Elevated chemokine concentrations in sera of human immunodeficiency virus (HIV)-seropositive and HIV-seronegative patients with tuberculosis: a possible role for mycobacterial lipoarabinomannan. Infection and Immunity 67, 42954297.CrossRefGoogle ScholarPubMed
Kabiri, M., Franco, J. R., Simarro, P. P., Ruiz, J. A., Sarsa, M. and Steverding, D. (1999). Detection of Trypanosoma brucei gambiense in sleeping sickness suspects by PCR amplification of expression-site-associated genes 6 and 7. Tropical Medicine and International Health 4, 658661.Google Scholar
Kennedy, P. G. (2004). Human African trypanosomiasis of the CNS: current issues and challenges. Journal of Clinical Investigation 113, 496504.Google Scholar
Kimber, C. D. (1984). Further improvements in the miniature anion/exchange centrifugation technique (mAECT) for field work. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 702703.Google Scholar
Kuboki, N., Inoue, N., Sakurai, T., Di Cello, F., Grab, D. J., Suzuki, H., Sugimoto, C. and Igarashi, I. (2003). Loop-mediated isothermal amplification for detection of African trypanosomes. Journal of Clinical Microbiology 41, 55175524.CrossRefGoogle ScholarPubMed
Lang, D. S., Zeiser, T., Schultz, H., Stellmacher, F., Vollmer, E., Zabel, P. and Goldmann, T. (2008). LED-FISH: Fluorescence microscopy based on light emitting diodes for the molecular analysis of Her-2/neu oncogene amplification. Diagnostic Pathology 3, 49.CrossRefGoogle ScholarPubMed
Lanham, S. M. (1968). Separation of trypanosomes from the blood of infected rats and mice by anion-exchangers. Nature 218, 12731274.Google Scholar
Lauwereys, M., Arbabi Ghahroudi, M., Desmyter, A., Kinne, J., Hölzer, W., De Genst, E., Wyns, L. and Muyldermans, S. (1998). Potent enzyme inhibitors derived from dromedary heavy-chain antibodies. EMBO Journal 17, 35123520.Google Scholar
Lejon, V., Lardon, J., Kenis, G., Pinoges, L., Legros, D., Bisser, S., N'Siesi, X., Bosmans, E. and Büscher, P. (2002 a). Interleukin (IL)-6, IL-8 and IL-10 in serum and CSF of Trypanosoma brucei gambiense sleeping sickness patients before and after treatment. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 329333.CrossRefGoogle ScholarPubMed
Lejon, V., Legros, D., Richer, M., Ruiz, J. A., Jamonneau, V., Truc, P., Doua, F., Djé, N., N'Siesi, F. X., Bisser, S., Magnus, E., Wouters, I., Konings, J., Vervoort, T, Sultan, F. and Büscher, P. (2002 b). IgM quantification in the cerebrospinal fluid of sleeping sickness patients by a latex card agglutination test. Tropical Medicine and International Health 7, 685692.Google Scholar
Lejon, V., Reiber, H., Legros, D., Djé, N., Magnus, E., Wouters, I., Sindic, C. J. and Büscher, P. (2003). Intrathecal immune response pattern for improved diagnosis of central nervous system involvement in trypanosomiasis. Journal of Infectious Diseases 187, 14751483.CrossRefGoogle ScholarPubMed
Lejon, V., Roger, I., Mumba Ngoyi, D., Menten, J., Robays, J., N'siesi, F. X., Bisser, S., Boelaert, M. and Büscher, P. (2008). Novel markers for treatment outcome in late-stage Trypanosoma brucei gambiense trypanosomiasis. Clinical Infectious Diseases 47, 1522.Google Scholar
Levine, R. A., Wardlaw, S. C. and Patton, C. L. (1989). Detection of haematoparasites using quantitative buffy coat analysis tubes. Parasitology Today 5, 132134.Google Scholar
Lorger, M., Engstler, M., Homann, M. and Göringer, H. U. (2003). Targeting the variable surface of African trypanosomes with variant surface glycoprotein-specific, serum-stable RNA aptamers. Eukaryotic Cell 2, 8494.Google Scholar
Magnus, E., Vervoort, T. and 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 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, 70407044.Google Scholar
Meena, M., Joshi, D., Joshi, R., Sridhar, S., Waghdhare, S., Gangane, N. and Kalantri, S. P. (2009). Accuracy of a multispecies rapid diagnostic test kit for detection of malarial parasite at the point of care in a low endemicity region. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 12371244.Google Scholar
Miezan, T. W., Meda, H. A., Doua, F., Yapo, F. B. and Baltz, T. (1998). Assessment of central nervous system involvement in gambiense trypanosomiasis: value of the cerebro-spinal white cell count. Tropical Medicine and International Health 3, 571575.CrossRefGoogle ScholarPubMed
Muyldermans, S., Baral, T. N., Retamozzo, V. C., De Baetselier, P., De Genst, E., Kinne, J., Leonhardt, H., Magez, S., Nguyen, V. K., Revets, H., Rothbauer, U., Stijlemans, B., Tillib, S., Wernery, U., Wyns, L., Hassanzadeh-Ghassabeh, G. and Saerens, D. (2009). Camelid immunoglobulins and nanobody technology. Veterinary Immunology and Immunopathology 128, 178183.Google Scholar
Njiru, Z. K., Constantine, C. C., Guya, S., Crowther, J., Kiragu, J. M., Thompson, R. C. and Dávila, A. M. (2005). The use of ITS1 rDNA PCR in detecting pathogenic African trypanosomes. Parasitology Research 95, 186192.Google Scholar
Njiru, Z. K., Mikosza, A. S., Matovu, E., Enyaru, J. C., Ouma, J. O., Kibona, S. N., Thompson, R. C. and Ndung'u, J. M. (2008). African trypanosomiasis: sensitive and rapid detection of the sub-genus Trypanozoon by loop-mediated isothermal amplification (LAMP) of parasite DNA. International Journal for Parasitology 38, 589599.CrossRefGoogle ScholarPubMed
Nolan, D. P., Jackson, D. G., Windle, H. J., Pays, A., Geuskens, M., Michel, A., Voorheis, H. P. and Pays, E. (1997). Characterization of a novel, stage-specific, invariant surface protein in Trypanosoma brucei containing an internal, serine-rich, repetitive motif. Journal of Biological Chemistry 272, 2921229221.Google Scholar
Notomi, T., Okayama, H., Masubuchi, H., Yonekawa, T., Watanabe, K., Amino, N. and Hase, T. (2000). Loop-mediated isothermal amplification of DNA. Nucleic Acids Research 28, E63.Google Scholar
Odiit, M., Kansiime, F. and Enyaru, J. C. (1997). Duration of symptoms and case fatality of sleeping sickness caused by Trypanosoma brucei rhodesiense in Tororo, Uganda. East African Medical Journal 74, 792795.Google Scholar
Okenu, D. M., Opara, K. N., Nwuba, R. I. and Nwagwu, M. (1999). Purification and characterisation of an extracellularly released protease of Trypanosoma brucei. Parasitology Research 85, 424428.Google Scholar
Pamer, E. G., So, M. and Davis, C. E. (1989). Identification of a developmentally regulated cysteine protease of Trypanosoma brucei. Molecular and Biochemical Parasitology 33, 2732.Google Scholar
Paquet, C., Ancelle, T., Gastellu-Etchegorry, M., Castilla, J. and Harndt, I. (1992). Persistence of antibodies to Trypanosoma brucei gambiense after treatment of human trypanosomiasis in Uganda. Lancet 340, 250.CrossRefGoogle ScholarPubMed
Penchenier, L., Grébaut, P., Njokou, F., Eboo Eyenga, V. and Büscher, P. (2003). Evaluation of LATEX/T. b. gambiense for mass screening of Trypanosoma brucei gambiense sleeping sickness in Central Africa. Acta Tropica 85, 3137.Google Scholar
Pepin, J. and Milford, F. (1994). The treatment of human African trypanosomiasis. Advances in Parasitology 33, 147.Google Scholar
Picozzi, K., Fèvre, E. M., Odiit, M., Carrington, M., Eisler, M. C., Maudlin, I. and Welburn, S. C. (2005). Sleeping sickness in Uganda: a thin line between two fatal diseases. British Medical Journal 331, 12381241.CrossRefGoogle ScholarPubMed
Radwanska, M., Claes, F., Magez, S., Magnus, E., Perez-Morga, D., Pays, E. and Büscher, P. (2002 b). Novel primer sequences for polymerase chain reaction-based detection of Trypanosoma brucei gambiense. American Journal of Tropical Medicine and Hygiene 67, 289295.CrossRefGoogle ScholarPubMed
Radwanska, M., Chamekh, M., Vanhamme, L., Claes, F., Magez, S., Magnus, E., De Baetselier, P., Büscher, P. and Pays, E. (2002 c). 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.Google Scholar
Radwanska, M., Magez, S., Perry-O'Keefe, H., Stender, H., Coull, J., Sternberg, J. M., Büscher, P. and Hyldig-Nielsen, J. J. (2002 a). Direct detection and identification of African trypanosomes by fluorescence in situ hybridization with peptide nucleic acid probes. Journal of Clinical Microbiology 40, 42954297.Google Scholar
Rawal, A., Gavin, P. J. and Sturgis, C. D. (2006). Cerebrospinal fluid cytology in seasonal epidemic West Nile virus meningo-encephalitis. Diagnostic Cytopathology 34, 127129.Google Scholar
Ruhwald, M., Bjerregaard-Andersen, M., Rabna, P., Eugen-Olsen, J. and Ravn, P. (2009). IP-10, MCP-1, MCP-2, MCP-3, and IL-1RA hold promise as biomarkers for infection with M. tuberculosis in a whole blood based T-cell assay. BMC Research Notes 2, 19.Google Scholar
Saerens, D., Stijlemans, B., Baral, T. N., Nguyen Thi, G. T., Wernery, U., Magez, S., De Baetselier, P., Muyldermans, S. and Conrath, K. (2008). Parallel selection of multiple anti-infectome Nanobodies without access to purified antigens. Journal of Immunological Methods 329, 138150.CrossRefGoogle ScholarPubMed
Sanderson, L., Dogruel, M., Rodgers, J., De Koning, H. P. and Thomas, S. A. (2009). Pentamidine movement across the murine blood-brain and blood-cerebrospinal fluid barriers: effect of trypanosome infection, combination therapy, P-glycoprotein, and multidrug resistance-associated protein. Journal of Pharmacology and Experimental Therapeutics 329, 967977.Google Scholar
Schutzer, S. E., Coyle, P. K., Krupp, L. B., Deng, Z., Belman, A. L., Dattwyler, R. and Luft, B. J. (1997). Simultaneous expression of Borrelia OspA and OspC and IgM response in cerebrospinal fluid in early neurologic Lyme disease. Journal of Clinical Investigation 100, 763767.Google Scholar
Simarro, P. P., Jannin, J. and Cattand, P. (2008). Eliminating human African trypanosomiasis: where do we stand and what comes next? PLoS Medicine 5, e55.Google Scholar
Simarro, P. P., Ruiz, J. A., Franco, J. R. and Josenando, T. (1999). Attitude towards CATT-positive individuals without parasitological confirmation in the African Trypanosomiasis (T. b. gambiense) focus of Quicama (Angola). Tropical Medicine and International Health 4, 858861.Google Scholar
Sindic, C. J., Monteyne, P. and Laterre, E. C. (1994). Occurrence of oligoclonal IgM bands in the cerebrospinal fluid of neurological patients: an immunoaffinity-mediated capillary blot study. Journal of Neurological Sciences 124, 215219.Google Scholar
Stanghellini, A. and Josenando, T. (2001). The situation of sleeping sickness in Angola: a calamity. Tropical Medicine and International Health 6, 330334.Google Scholar
Stijlemans, B., Conrath, K., Cortez-Retamozo, V., Van Xong, H., Wyns, L., Senter, P., Revets, H., De Baetselier, P., Muyldermans, S. and Magez, S. (2004). Efficient targeting of conserved cryptic epitopes of infectious agents by single domain antibodies. African trypanosomes as paradigm. Journal of Biological Chemistry 279, 12561261.Google Scholar
Swensen, J. S., Xiao, Y., Ferguson, B. S., Lubin, A. A., Lai, R. Y., Heeger, A. J., Plaxco, K. W. and Soh, H. T. (2009). Continuous, real-time monitoring of cocaine in undiluted blood serum via a microfluidic, electrochemical aptamer-based sensor. Journal of the American Chemical Society 131, 42624266.Google Scholar
Thekisoe, O. M., Kuboki, N., Nambota, A., Fujisaki, K., Sugimoto, C., Igarashi, I., Yasuda, J. and Inoue, N. (2007). Species-specific loop-mediated isothermal amplification (LAMP) for diagnosis of trypanosomosis. Acta Tropica 102, 182189.Google Scholar
Tijink, B. M., Laeremans, T., Budde, M., Stigter-van Walsum, M., Dreier, T., de Haard, H. J., Leemans, C. R. and van Dongen, G. A. (2008). Improved tumor targeting of anti-epidermal growth factor receptor Nanobodies through albumin binding: taking advantage of modular Nanobody technology. Molecular Cancer Therapeutics 7, 22882297.Google Scholar
Troeberg, L., Pike, R. N., Morty, R. E., Berry, R. K., Coetzer, T. H. and Lonsdale-Eccles, J. D. (1996). Proteases from Trypanosoma brucei brucei. Purification, characterisation and interactions with host regulatory molecules. European Journal of Biochemistry 238, 728736.Google Scholar
Truc, P., Lejon, V., Magnus, E., Jamonneau, V., Nangouma, A., Verloo, D., Penchenier, L. and Büscher, P. (2002). Evaluation of the micro-CATT, CATT/Trypanosoma brucei gambiense, and LATEX/T b gambiense methods for serodiagnosis and surveillance of human African trypanosomiasis in West and Central Africa. Bulletin of the World Health Organization 80, 882886.Google Scholar
Vincke, C., Loris, R., Saerens, D., Martinez-Rodriguez, S., Muyldermans, S. and Conrath, K. (2009). General strategy to humanize a camelid single-domain antibody and identification of a universal humanized nanobody scaffold. Journal of Biological Chemistry 284, 32733284.CrossRefGoogle ScholarPubMed
Woo, P. T. (1970). The haematocrit centrifuge technique for the diagnosis of African trypanosomiasis. Acta Tropica 27, 384386.Google Scholar
Ziegelbauer, K., Multhaup, G. and Overath, P. (1992). Molecular characterization of two invariant surface glycoproteins specific for the bloodstream stage of Trypanosoma brucei. Journal of Biological Chemistry 267, 1079710803.Google Scholar
Ziegelbauer, K. and Overath, P. (1992). Identification of invariant surface glycoproteins in the bloodstream stage of Trypanosoma brucei. Journal of Biological Chemistry 267, 1079110796.CrossRefGoogle ScholarPubMed