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Trypanosoma (Duttonella) vivax and Typanosomosis in Latin America: Secadera/Huequera/Cacho Hueco

  • Mary Isabel GonzattiEmail author
  • Bernardo González-Baradat
  • Pedro M. Aso
  • Armando Reyna-Bello
Chapter

Abstract

The disease caused by T. vivax is commonly called Nagana in Africa and “secadera/cachera/cacho hueco/huequera” in parts of South America. This chapter will focus on the disease and its causative agent, reviewing new diagnostic methods, economic impact, chemotherapy, phylogenetic analysis of T. vivax isolates from Africa and South America, epidemiological studies in Latin America, and the analysis of recent genomic and transcriptomic data. T. vivax has a significant economic impact on livestock production in sub-Saharan Africa, where it is transmitted by the tsetse fly, and elsewhere in the African continent and in Central and South America, where it is transmitted mechanically. T. vivax is enzootic in most Latin American countries, and recurrent epizootic outbreaks causing significant morbidity and mortality have been reported over the past decades. Several significant landmarks in T. vivax research have been achieved in the last 2 years, including the publication of high-quality draft genome sequences and partial RNA-seq data for the Y486 strain, as well as the complete transcriptome of the LIEM-176 strain. Comparative analysis of the T. vivax, T. brucei, and T. congolense genomes revealed important differences in the surface proteins responsible for host immune response evasion in these species, and data from the T. vivax LIEM-76 transcriptome support the participation of other surface proteins, in addition to the VSG, in immune evasion. Proteins of the trans-sialidase family have been identified as important virulence factors that catalyze the desialylation of the host red blood cell, which in turn triggers the erythrophagocytosis that results in anemia. These findings will provide novel tools to tackle the challenge of controlling animal trypanosomosis caused by T. vivax in the developing world.

Keywords

Vivax Infection Variable Surface Glycoprotein Vivax Isolate African Trypanosome Diminazene Aceturate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

Our work was supported by DID-USB (GID21); FONACIT project G-98003462, Misión Ciencia project 2007-1425, and INCO project Trypadvac2-003716.

References

  1. Abrão D, de Carvalho A, Facury E et al (2009) Impacto económico causado por Trypanosoma vivax em rebanho boviono leiteiro no estado de Minas Gerais Ciência Animal Brasileira – Suplemento 1, – Anais do VIII Congresso Brasileiro de BuiatriaGoogle Scholar
  2. Adams ER, Hamilton PB, Malele II et al (2008) The identification, diversity and prevalence of trypanosomes in field caught tsetse in Tanzania using ITS-1 primers and fluorescent fragment length barcoding. Infect Genet Evol 8:439–444PubMedCrossRefGoogle Scholar
  3. Adams E, Hamilton P, Rodrigues A et al (2010) New Trypanosoma (Duttonella) vivax genotypes from tsetse flies in East Africa. Parasitology 137:641–645PubMedCrossRefGoogle Scholar
  4. Adamu S, Fatihu MY, Useh NM et al (2006) Sequential testicular and epididymal damage in Zebu bulls experimentally infected with Trypanosoma vivax. Vet Parasitol 143:29–34PubMedCrossRefGoogle Scholar
  5. Anosa VO (1988) Haematological and biochemical changes in human and animal Trypanosomiasis. Part II. Rev Elev Med Vet Pays Trop 41:151–164PubMedGoogle Scholar
  6. Auty H, Anderson NE, Picozzi K et al (2012) Trypanosome diversity in wildlife species from the serengeti and Luangwa Valley ecosystems. PLoS Negl Trop Dis 6:e1828PubMedCrossRefGoogle Scholar
  7. Barry JD (1997) The relative significance of mechanism of antigenic variation in African Trypanosomes. Parasitol Today 13:212–218PubMedCrossRefGoogle Scholar
  8. Barry JD, Hall JP, Plenderleith L (2012) Genome hyperevolution and the success of a parasite. Ann NY Acad Sci 1267:11–17PubMedCrossRefGoogle Scholar
  9. Batista JS, Riet-Correa F, Teixeira MM, Madruga CR, Simões SD, Maia TF (2007) Trypanosomiasis by Trypanosoma vivax in cattle in the Brazilian semiarid: description of an outbreak and lesions in the nervous system. Vet Parasitol 143:174–181PubMedCrossRefGoogle Scholar
  10. Batista JS, Rodrigues CM, García HA et al (2011) Association of Trypanosoma vivax in extracellular sites with central nervous system lesions and changes in cerebrospinal fluid in experimentally infected goats. Vet Res 42:63–69PubMedCrossRefGoogle Scholar
  11. Benavides E, López M, Alayón L (2011) Enfermedades del ganado en la región de La Macarena (Meta). Un ejercicio de epidemiología participativa. Rev Med Vet 21:41–62Google Scholar
  12. Betancourt A, Wells E (1979) Pérdidas económicas en un brote de tripanosomosis bovina causada por Trypanosoma vivax. Rev Acovez 3: 6–9Google Scholar
  13. Biryomumaisho S, Katunguka-Rwakishaya E, Lubega G et al (2011) Identification of Trypanosoma vivax subtypes isolated from cattle and goats using microsatellite markers. Vet Arhiv 81:13–24Google Scholar
  14. Boada-Sucre A (2010) Histopatología y Patología Ultraestructural de la Glándula Adrenal, el Hígado y el Testículo de Ovinos Infectados Experimentalmente con Trypanosoma vivax. Tesis Doctorado, Universidad Central de Venezuela. Facultad de CienciasGoogle Scholar
  15. Borst P, Fase-Fowler F, Weijers PJ, Barry JD, Tetley L, Vickerman K (1985) Kinetoplast DNA from Trypanosoma vivax and T. congolense. Mol Biochem Parasitol 15:129–142PubMedCrossRefGoogle Scholar
  16. Bossard G, Boulangé A, Holzmuller P et al (2010) Serodiagnosis of bovine trypanosomosis based on HSP70/BiP inhibition ELISA. Vet Parasitol 173:39–47PubMedCrossRefGoogle Scholar
  17. Cadioli F, de Barnabé PA, Machado R et al (2012) First report of Trypanosoma vivax outbreak in dairy cattle in São Paulo state, Brazil. Rev Bras Parasitol Vet 21:118–124PubMedCrossRefGoogle Scholar
  18. Carougeau M (1929) Trypanosomiase bovine à la Martinique. Bull Soc Pathol Exot 22:246–247Google Scholar
  19. Chamond N, Cosson A, Blom-Potar MC, Jouvion G, D’Archivio S, Medina M, Droin-Bergère S, Huerre M, Goyard S, Minoprio P (2010) Trypanosoma vivax infections: pushing ahead with mouse models for the study of Nagana. I. Parasitological, hematological and pathological parameters. PLoS Negl Trop Dis 4:e792PubMedCrossRefGoogle Scholar
  20. Cherenet T, Sani R, Speybroeck N et al (2006) A comparative longitudinal study of bovine trypanosomiasis in tsetse-free and tsetse-infested zones of the Amhara Region, northwest Ethiopia. Vet Parasitol 140:251–258PubMedCrossRefGoogle Scholar
  21. Cortez AP, Ventura R, Rodrigues A et al (2006) The taxonomic and phylogenetic relationships of Trypanosoma vivax from South America and Africa. Parasitology 133:159–169PubMedCrossRefGoogle Scholar
  22. Cortez AP, Rodrigues A, Garcia H et al (2009) Cathepsin L-like genes of Trypanosoma vivax from Africa and South America – characterization, relationships and diagnostic implications. Mol Cell Probes 23:44–51PubMedCrossRefGoogle Scholar
  23. D’Archivio S, Medina M, Cosson A, Chamond N, Rotureau B, Minoprio P, Goyard S (2011) Genetic engineering of Trypanosoma (Dutonella) vivax and in vitro differentiation under axenic conditions. PLoS Negl Trop Dis 5:e1461PubMedCrossRefGoogle Scholar
  24. Dávila AM, Silva RA (2000) Animal trypanosomiasis in South America. Current status, partnership, and information technology. Ann NY Acad Sci 916:199–212PubMedCrossRefGoogle Scholar
  25. De Stefano H, González B, Boada-Sucre A et al (1999) Efecto de la infección con Trypanosoma vivax sobre la calidad espermática de toros Siboney. Rev Cient FCV-LUZ IX:411–417Google Scholar
  26. Desquesnes M (2004) Livestock trypanosomes and their vectors in Latin America. OIE. World Organization for Animal Health, ParisGoogle Scholar
  27. Desquesnes M, Dia ML (2003) Mechanical transmission of Trypanosoma congolense in cattle by the African tabanid Atylotus agrestis. Exp Parasitol 105:226–231PubMedCrossRefGoogle Scholar
  28. Desquesnes M, Dia ML (2004) Mechanical transmission of Trypanosoma vivax in cattle by the African tabanid Atylotus fuscipes. Vet Parasitol 119(1):9–19PubMedCrossRefGoogle Scholar
  29. Desquesnes M, McLaughlin G, Zoungrana A et al (2001) Detection and identification of Trypanosoma of African livestock through a single PCR based on internal transcribed spacer 1 of rDNA. Int J Parasitol 31:610–614PubMedCrossRefGoogle Scholar
  30. Desquesnes M, Biteau-Coroller F, Bouyer J et al (2009) Development of a mathematical model for mechanical transmission of trypanosomes and other pathogens of cattle transmitted by tabanids. Int J Parasitol 39:333–346PubMedCrossRefGoogle Scholar
  31. Desquesnes M, Kamyingkird K, Vergne T et al (2011) An evaluation of melarsomine hydrochloride efficacy for parasitological cure in experimental infection of dairy cattle with Trypanosoma evansi in Thailand. Parasitology 138:1134–1142PubMedCrossRefGoogle Scholar
  32. Dickin SK, Gibson WC (1989) Hybridisation with a repetitive DNA probe reveals the presence of small chromosomes in Trypanosoma vivax. Mol Biochem Parasitol 33:135–142PubMedCrossRefGoogle Scholar
  33. Dirie MF, Otte MJ, Thatthi R et al (1993) Comparative studies of Trypanosoma (Duttonella) vivax isolates from Colombia. Parasitology 106(Pt 1):21–29PubMedCrossRefGoogle Scholar
  34. Duffy C, Morrison L, Black A et al (2009) Trypanosoma vivax displays a clonal population structure. Int J Parasitol 39:1475–1483PubMedCrossRefGoogle Scholar
  35. Duno F, Garcia F, Rivera M (1992) Epidemiological aspects of bovine tripanosomosis in Falcón State, Venezuela. In: Premier Séminaire International sur les Trypanosomoses Animales Non Transmises par les Glossines, Annecy, 14–16 Oct 1992, 184 ppGoogle Scholar
  36. Eleizalde MC, Gómez-Piñeres E, Tavares-Márquez LM et al (2012) Determination by PCR of the animal trypanosomiasis caused by T. evansi in samples from cattle in the San Casimiro Municipality Aragua State, Venezuela. Congreso Panamericano de Ciencias Veterinaria. Cartagena, ColombiaGoogle Scholar
  37. Espinoza E, González N, Aso P, Perrone T (1999) Incidencia serológica de Trypanosoma vivax en becerros a pastoreo en sabanas del Estado Guárico. Vet Trop 24:5–15Google Scholar
  38. FAO (2004). The state of food and agriculture 2003–2004. Food and Agriculture Organisation of the United Nations (FAO), Rome, Italy. Accessed 5 Mar 2013Google Scholar
  39. Fasogbon A, Knowles G, Gardiner P (1990) A comparison of the isoenzymes of Trypanosoma (Duttonella) vivax isolates from East and West Africa. Int J Parasitol 20:389–394PubMedCrossRefGoogle Scholar
  40. Fernández D, González-Baradat B, Eleizalde M et al (2008) Trypanosoma evansi: a comparison of PCR and parasitological diagnostic tests in experimentally infected mice. Exp Parasitol 121:1–7PubMedCrossRefGoogle Scholar
  41. Fikru R, Goddeeris B, Delespaux V et al (2012) Widespread occurrence of Trypanosoma vivax in bovines of tsetse- as well as non-tsetse-infested regions of Ethiopia: a reason for concern? Vet Parasitol 190:355–361PubMedCrossRefGoogle Scholar
  42. Foil L (1983) A mark-recapture method for measuring effects of spatial separation of horses on tabanid (Diptera) movement between hosts. J Med Entomol 20:301–305PubMedGoogle Scholar
  43. Foil L, Adams W, Mcmanus J et al (1987) Bloodmeal residues on mouthpart of Tabanus fuscicostatus and the potential for mechanical transmission of pathogens. J Med Entomol 24:613–616PubMedGoogle Scholar
  44. Galiza GJ, Garcia HA, Assis AC et al (2011) High mortality and lesions of the central nervous system in Trypanosomosis by Trypanosoma vivax in Brazilian hair sheep. Vet Parasitol 182:359–363PubMedCrossRefGoogle Scholar
  45. García H, Aguirre A, Pérez G et al (2001) Diagnóstico parasitológico y serológico de infecciones por Trypanosoma sp en dos rebaños bufalinos (Bubalus bubalis) del estado Guárico. Rev Fac Cien Vet UCV 42:15–28Google Scholar
  46. García FA, Alfaro EC, Reyna A et al (2008) Evaluación de la eficacia de un producto a base de cloruro de isometamidium y clorhidrato de oxitetraciclina en un rebaño de ceba del Edo. Monagas naturalmente infectado con Trypanosoma vivax y Anaplasma marginale. Venezuela Bovina 23:34–43Google Scholar
  47. Gardiner PR (1989) Recent studies of the biology of Trypanosoma vivax. Adv Parasitol 28:229–317PubMedCrossRefGoogle Scholar
  48. Gardiner PR, Nene V, Barry MM et al (1996) Characterization of a small variable surface glycoprotein from Trypanosoma vivax. Mol Biochem Parasitol 82:1–11PubMedCrossRefGoogle Scholar
  49. Gibson W (2007) Resolution of the species problem in African trypanosomes. Int J Parasitol 37:829–838PubMedCrossRefGoogle Scholar
  50. Gibson W (2009) Species-specific probes for the identification of the African tsetse-transmitted trypanosomes. Parasitology 136:1501–1507PubMedCrossRefGoogle Scholar
  51. Gibson W (2012) The origins of the trypanosome genome strains Trypanosoma brucei brucei TREU 927, T. b. gambiense DAL 972, T. vivax Y486 and T. congolense IL3000. Parasit Vectors 5:71–76PubMedCrossRefGoogle Scholar
  52. Gohil S, Herrmann S, Günther S, Cooke BM (2012) Bovine babesiosis in the 21st century: advances in biology and functional genomics. Int J Parasitol 43:125–132PubMedCrossRefGoogle Scholar
  53. Gómez-Piñeres E, Boada-Sucre A, Bretaña A et al (2013) Morphometric characterization of Trypanosoma vivax isolates from Venezuela. Rev Fac Cien Vet (UCV) (in press)Google Scholar
  54. Gonzales JL, Loza A, Chacon E et al (2006) Sensitivity of different Trypanosoma vivax specific primers for the diagnosis of livestock trypanosomosis using different DNA extraction methods. Vet Parasitol 136:119–126PubMedCrossRefGoogle Scholar
  55. Gonzales JL, Chacon E, Miranda M et al (2007) Bovine trypanosomosis in the Bolivian Pantanal. Vet Parasitol 146:9–16PubMedCrossRefGoogle Scholar
  56. Greif G, de Leon MP, Lamolle G et al (2013) Transcriptome analysis of the bloodstream stage from the parasite Trypanosoma vivax. BMC Genomics 14(1):149PubMedCrossRefGoogle Scholar
  57. Guegan F, Plazolles N, Baltz T et al (2013) Erythrophagocytosis of desialylated red blood cells is responsible for anaemia during Trypanosoma vivax infection. Cell Microbiol. doi: 10.1111/cmi.12123 PubMedGoogle Scholar
  58. Haag J, O'hUigin C, Overath P (1998) The molecular phylogeny of trypanosomes: evidence for an early divergence of the Salivaria. Mol Biochem Parasitol 91:37–49PubMedCrossRefGoogle Scholar
  59. Hamilton P, Gibson W, Stevens J (2007) Patterns of co-evolution between trypanosomes and their hosts deduced from ribosomal RNA and protein-coding gene phylogenies. Mol Phylogenet Evol 44:15–25PubMedCrossRefGoogle Scholar
  60. Hoare C (1972) The trypanosomes of mammals. A zoological monograph. Blackwell Scientific Publications, Oxford, 749 ppGoogle Scholar
  61. Holmes PH, Eisler MC, Geerts S (2004) Current chemotherapy of animal trypanosomiasis. In: Maudlin I, Holmes P, Miles M (eds) The Tripanosomiases, 1st edn. CABI Publishing, Boston, MA, pp 431–464CrossRefGoogle Scholar
  62. Jackson AP, Berry A, Aslett M et al (2012) Antigenic diversity is generated by distinct evolutionary mechanisms in African trypamosome species. Proc Natl Acad Sci USA 109:3416–3421PubMedCrossRefGoogle Scholar
  63. Jackson AP, Allison H, Barry JD et al (2013) A cell-surface phylome for African Trypanosomes. PLoS Negl Trop Dis 7:e2121PubMedCrossRefGoogle Scholar
  64. Jones TW, Davila AM (2001) Trypanosoma vivax-out of Africa. Trends Parasitol 17:99–101PubMedCrossRefGoogle Scholar
  65. Kubes V (1944) El Trypanosoma vivax Americano. Agente de la tripanosomiasis bovina en Venezuela. Su comparación con el del Africa, Instituto de Investigaciones Veterinarias. Ed, Grafolit, Caracas, VenezuelaGoogle Scholar
  66. Kuboki N, Inoue N, Sakurai T et al (2003) Loop-mediated isothermal amplification for detection of African trypanosomes. J Clin Microbiol 41:5517–5524PubMedCrossRefGoogle Scholar
  67. Kukla B, Majiwa P, Young J et al (1987) Use of species-specific DNA probes for detection and identification of trypanosome infection in tsetse flies. Parasitology 95:1–16PubMedCrossRefGoogle Scholar
  68. Leeflang P, Buys J, Blotkamp C (1976) Studies on Trypanosoma vivax: infectivity and serial maintenance of natural bovine isolates in mice. Int J Parasitol 6:413–417PubMedCrossRefGoogle Scholar
  69. Leger L, Vienne M (1919) Epizootie à trypanosomes chez les Bovidés de la Guyane Française. Bull Soc Pathol Exot 12:258–266Google Scholar
  70. Madruga C, Araújo F, Cavalcante-Goes G et al (2006) The development of an enzyme-linked immunosorbent assay for Trypanosoma vivax antibodies and its use in epidemiological surveys. Mem Inst Oswaldo Cruz 101:801–807PubMedCrossRefGoogle Scholar
  71. Maillard N, Maillard J (1998) Historique du peuplement bovin et de l′introduction de la tique Amblyomma variegatum dans les îles françaises des Antilles: synthèse bibliographique. Ethnozootech 61:19–36Google Scholar
  72. Malele I, Craske L, Knight C et al (2003) Identification of new trypanosome species from wild tsetse flies in Tanzania. infection. Infect Genet Evol 3:271–279PubMedCrossRefGoogle Scholar
  73. Masake RA, Nantulya VM, Pellé R, Makau JM, Gathuo H, ole-MoiYoi OK (1994) A species-specific antigen of Trypanosoma (Duttonella) vivax detectable in the course of infection is encoded by a differentially expressed tandemly reiterated gene. Mol Biochem Parasitol 64:207–218PubMedCrossRefGoogle Scholar
  74. Masake RA, Majiwa PA, Moloo SK et al (1997) Sensitive and specific detection of Trypanosoma vivax using the polymerase chain reaction. Exp Parasitol 85:193–205PubMedCrossRefGoogle Scholar
  75. Masiga DK, Gibson WC (1990) Specific probes for Trypanosoma (Trypanozoon) evansi based on kinetoplast DNA minicircles. Mol Biochem Parasitol 40:279–283PubMedCrossRefGoogle Scholar
  76. Masiga D, Smyth A, Hayes P et al (1992) Sensitive detection of trypanosomes in tsetse flies by DNA amplification. Int J Parasitol 22:909–918PubMedCrossRefGoogle Scholar
  77. Mateus G, González M (1991) Características de un brote de Trypanosoma vivax en Colombia. Rev Cuba Cien Vet 22:167–172Google Scholar
  78. Matovu E, Kuepfer I, Boobo A, Kibona S, Burri C (2010) Comparatitve detection of trypanosomal DNA by loop-mediated isothermal amplification and PCR from flinders technology associates cards spotted with patient blood. J Clin Microbiol 48(6):2087–2090PubMedCrossRefGoogle Scholar
  79. Mekata H, Konnai S, Witola WH et al (2009) Molecular detection of trypanosomes in cattle in South America and genetic diversity of Trypanosoma evansi based on expression-site-associated gene 6. Infect Genet Evol 9:1301–1305PubMedCrossRefGoogle Scholar
  80. Mekata H, Konnai S, Mingala CN, Abes NS, Gutierrez CA, Dargantes AP, Witola WH, Inoue N, Onuma M, Murata S, Ohashi K (2013) Isolation, cloning and pathologic analysis of Trypanosoma evansi field isolates. Parasitol Res 112:1513–1521PubMedCrossRefGoogle Scholar
  81. Morlais I, Ravel S, Grébaut P et al (2001) New molecular marker for Trypanosoma (Duttonella) vivax identification. Acta Trop 80:207–213PubMedCrossRefGoogle Scholar
  82. Mosqueda J, Olvera-Ramírez A, Aguilar-Tipacamú G et al (2012) Current advances in detection and treatment of babesiosis. Curr Med Chem 19:1504–1518PubMedCrossRefGoogle Scholar
  83. Njiru Z (2011) Rapid and sensitive detection of human African trypanosomiasis by loop-mediated isothermal amplification combined with a lateral-flow dipstick. Diagn Microbiol Infect Dis 69:205–209PubMedCrossRefGoogle Scholar
  84. Njiru Z, Constantine C, Guya S et al (2005) The use of ITS1 rDNA PCR in detecting pathogenic African trypanosomes. Parasitol Res 95:186–192PubMedCrossRefGoogle Scholar
  85. Njiru Z, Mikosza A, Armstrong T et al (2008) Loop-mediated isothermal amplification (LAMP) method for rapid detection of Trypanosoma brucei rhodesiense. PLoS Negl Trop Dis 2:e147. doi: 10.1371/journal.pntd.0000147 PubMedCrossRefGoogle Scholar
  86. Njiru Z, Ouma J, Enyaru J et al (2010) Loop-mediated isothermal amplification (LAMP) test for detection of Trypanosoma evansi strain B. Exp Parasitol 125:196–201PubMedCrossRefGoogle Scholar
  87. Njiru Z, Traub R, Ouma J, Enyaru JC et al (2011a) Detection of group 1 Trypanosoma brucei gambiense by loop-mediated isothermal amplification. J Clin Microbiol 49:1530–1536PubMedCrossRefGoogle Scholar
  88. Njiru Z, Ouma J, Bateta R et al (2011b) Loop-mediated isothermal amplification test for Trypanosoma vivax based on satellite repeat DNA. Vet Parasitol 180:358–362PubMedCrossRefGoogle Scholar
  89. Notomi T, Okayama H, Masubuchi H et al (2000) Loop-mediated isothermal amplification of DNA. Nucleic Acids Res 28:E63PubMedCrossRefGoogle Scholar
  90. OIE (2008) Terrestrial manual. Chapter 2. 4.1 8. Trypanosomosis (tsetse-transmitted). http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.04.18_TRYPANOSOMOSIS.pdf. Accessed 25 Sep 2012
  91. OIE (2008a) Terrestrial manual. Chapter 2.5.3. Dourine. http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.05.03_DOURINE.pdfdf. Accessed 11 Mar 2013
  92. Oliveira J, Hernández-Gamboa J, Jiménez-Alfaro C et al (2009) First report of Trypanosoma vivax infection in dairy cattle from Costa Rica. Vet Parasitol 163:136–139PubMedCrossRefGoogle Scholar
  93. Osório A, Madruga C, Desquesnes M et al (2008) Trypanosoma (Duttonella) vivax: its biology, epidemiology, pathogenesis, and introduction in the new world—a review. Mem Inst Oswaldo Cruz 103:1–13PubMedCrossRefGoogle Scholar
  94. Otte M, Abuabara J, Nieto MI et al (1988) Incidence of Trypanosoma vivax infection on three cattle farms on the north coast of Colombia. Acta Vet Scand Suppl 84:104–106PubMedGoogle Scholar
  95. Perrone T, Lesseur M, Reveron I et al (1992) Seroepidemiology of bovine trypanosomosis in the area of Santa Maria de Ipire, Venezuela. In: Premier séminaire international sur les trypanosomoses animales non transmises par les Glossines, Annecy, 14–16 Oct 1992, p 196Google Scholar
  96. Ramírez-Iglesias JR, Eleizalde MC, Gómez-Piñeres E et al (2011) Trypanosoma evansi: a comparative study of four diagnostic techniques for trypanosomosis using rabbit as an experimental model. Exp Parasitol 128:91–96PubMedCrossRefGoogle Scholar
  97. Rey C (2004) Hemoparasitosis en América Latina: El Caso Venezuela. Red Electrónica de Garrapatas y Enfermedades Transmitidas por Garrapatas para América Latina y el Caribe, RedEctopar. Cuarta Conferencia ElectrónicaGoogle Scholar
  98. Reyna-Bello A, García FA, Rivera M et al (1998) Enzyme-linked immunosorbent assay (ELISA) for detection of anti-Trypanosoma evansi equine antibodies. Vet Parasitol 80:149–157PubMedCrossRefGoogle Scholar
  99. Rivera M (1996) Hemoparasitosis Bovinas. Consejo de Desarrollo Científico y Humanístico UCV. Colección Estudios. Caracas, Venezuela, 238 ppGoogle Scholar
  100. Roberts W, Wellde B, Reardon M et al (1989) Mechanical transmission of Trypanosoma brucei rhodesiense by Glossina morsitans morsitans (Diptera:Glossinidae). Ann Trop Med Parasitol 83(Suppl 1):127–131PubMedGoogle Scholar
  101. Rodrigues A, Neves L, Garcia H et al (2008) Phylogenetic analysis of Trypanosoma vivax supports the separation of South American/West African from East African isolates and a new T. vivax-like genotype infecting a nyala antelope from Mozambique. Parasitology 135:1317–1328PubMedCrossRefGoogle Scholar
  102. Seidl A, Dávila AMR, Silva RA (1999) Estimated financial impact of Trypanosoma vivax on the Brazilian Pantanal and Bolivian lowlands. Mem Inst Oswaldo Cruz 94:269–272PubMedCrossRefGoogle Scholar
  103. Sekoni VO (1994) Reproductive disorders caused by animal trypanosomiases: a review. Theriogenology 42:557–570PubMedCrossRefGoogle Scholar
  104. Shaw J, Lainson R (1972) Trypanosoma vivax in Brazil. Ann Trop Med Parasitol 66:25–32PubMedGoogle Scholar
  105. Silva RA, da Silva JA, Schneider RC et al (1996) Outbreak of Trypanosomiasis due to Trypanosoma vivax Ziemann, 1905. in bovines of the Pantanal, Brazil. Mem Inst Oswaldo Cruz 52:561–562CrossRefGoogle Scholar
  106. Silva RA, Equez A, Morales G et al (1998) Bovine trypanosomosis in Bolivian and Brazilian lowlands. Mem Inst Oswaldo Cruz 93:29–32PubMedCrossRefGoogle Scholar
  107. Simoes D, Sánchez M, González Y, Rivera F, Parra R, Gil M, García ME, Quijada J y García F (2009) Brote de tripanosomosis en un rebaño doble propósito del municipio Mara del estado Zulia, Venezuela. CIENCIA 17:124–132Google Scholar
  108. Simpson AG, Stevens JR, Lukes J (2006) The evolution and diversity of kinetoplastid flagellates. Trends Parasitol 22:168–174PubMedCrossRefGoogle Scholar
  109. Sow A, Sidibé I, Bengaly Z et al (2012) Field detection of resistance to isometamidium chloride and diminazene aceturate in Trypanosoma vivax from the region of the Boucle du Mouhoun in Burkina Faso. Vet Parasitol 187:105–111PubMedCrossRefGoogle Scholar
  110. Stevens JR (2008) Kinetoplastid phylogenetics, with special reference to the evolution of parasitic trypanosomes. Parasite 15:226–232PubMedCrossRefGoogle Scholar
  111. Stevens J, Rambaut A (2001) Evolutionary rate differences in trypanosomes. Infect Genet Evol 1:143–150PubMedCrossRefGoogle Scholar
  112. Stevens J, Brisse S (2004) Systematics of Trypanosomes of medical and veterinary importance. In: Maudlin I, Holmes P, Miles M (eds) The Tripanosomiases, 1st edn. CABI Publishing, Boston, MA, pp 1–24CrossRefGoogle Scholar
  113. Suárez C, García F, Román D et al (2009) Factores de riesgo asociados a la tripanosomosis bovina en explotaciones ganaderas de Venezuela. Zootecnia Trop 27:363–372Google Scholar
  114. Tait A, Morrison L, Duffy C et al (2011) Trypanosome genetics: populations, phenotypes and diversity. Vet Parasitol 181:61–68PubMedCrossRefGoogle Scholar
  115. Tamasaukas R, Roa N, Cobo M (2006) Trypanosomosis por Trypanosoma vivax en búfalos (Bubalis bubalis), en dos fincas del estado Guárico, Venezuela. Rev Cient FCV-LUZ XVI:575–578Google Scholar
  116. Taylor K, Authié EM-L (2004) Pathogenesis of animal Trypanosomiasis. In: Maudlin I, Holmes P, Miles M (eds) The Tripanosomiases, 1st edn. CABI Publishing, Boston, MA, pp 331–353CrossRefGoogle Scholar
  117. Thekisoe O, Inoue N, Kuboki N et al (2005) Evaluation of loop-mediated isothermal amplification (LAMP), PCR and parasitological tests for detection of Trypanosoma evansi in experimentally infected pigs. Vet Parasitol 130:327–330PubMedCrossRefGoogle Scholar
  118. Thekisoe OM, Kuboki N, Nambota A et al (2007) Species-specific loop-mediated isothermal amplification (LAMP) for diagnosis of trypanosomosis. Acta Trop 102:182–189PubMedCrossRefGoogle Scholar
  119. Thekisoe O, Rodriguez C, Rivas F et al (2010) Detection of Trypanosoma cruzi and T. rangeli infections from Rhodnius pallescens bugs by loop-mediated isothermal amplification (LAMP). Am J Trop Med Hyg 82:855–860PubMedCrossRefGoogle Scholar
  120. Toro M (1990) Seroepidemiología de las hemoparasitosis en Venezuela. In: Giardina S, and, Garcia F (eds.) Hemoparásitos: Biología y Diagnóstico. Cuadernos Serie Biología No. 1. Universidad Simón Bolívar, Caracas, VenezuelaGoogle Scholar
  121. Touratier L (1993) First International Seminar on Non Tsetse-Transmitted Animal Trypanosomoses:conclusions and recommendations. Rev Sci Tech 12:273–281PubMedGoogle Scholar
  122. Touratier L (1999) The Office International des epizooties ad hoc group on non tsetse animal Trypanosomoses: its origin, scope and perspectives. Mem Inst Oswaldo Cruz 94:191–194PubMedCrossRefGoogle Scholar
  123. Touratier L (2000) Challenges of non-tsetse transmitted animal trypanosomoses (NTTAT). An outline and some perspectives. Ann NY Acad Sci 916:237–239PubMedCrossRefGoogle Scholar
  124. Truc P, Buscher P, Cuny G et al (2013) Atypical human infections by animal trypanosomes: new emerging diseases? PLoS Negl Trop Dis (in press)Google Scholar
  125. Turner CM (1999) Antigenic variation in Trypanosoma brucei infections: a holistic view. J Cell Sci 112:3187–3192PubMedGoogle Scholar
  126. Turner CMR, Aslam N, Dye C (1995) Replication, diferentiation, growth and virulence of Trypanosoma brucei infections. Parasitology 111:289–300PubMedCrossRefGoogle Scholar
  127. Uilenberg G (1998) A field guide for the diagnosis, treatment and prevention of African animal Trypanosomosis. Food and Agriculture Organization of the United Nations. Rome -FAO 1998. http://www.fao.org/DOCREP/006/X0413E/X0413E00.HTM. Accessed 17 Mar 2013
  128. Ventura R, Paiva F, Silva R et al (2001) Trypanosoma vivax: characterization of the spliced-leader gene of a Brazilian stock and species-specific detection by PCR amplification of an intergenic spacer sequence. Exp Parasitol 99:37–48PubMedCrossRefGoogle Scholar
  129. Wells E, Betancourt A, Ramirez L (1977) Serological evidence for the geographical distribution of Trypanosoma vivax in the New World. Trans R Soc Trop Med Hyg 71:448–449PubMedCrossRefGoogle Scholar
  130. Wells E, Ramirez L, Betancourt A (1982) Trypanosoma vivax in Colombia: interpretation of field results. Trop Anim Health Prod 14:141–150PubMedCrossRefGoogle Scholar
  131. Woo PTK (1969) The haematocrit centrifuge for detection of trypanosomes in blood. Can J Zool 47:921–923PubMedCrossRefGoogle Scholar
  132. Yurchenko VY, Kolesnikov AA (2001) Minicircular kinetoplast DNA of Trypanosomatidae. Mol Biol 35:1–10CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  • Mary Isabel Gonzatti
    • 1
    Email author
  • Bernardo González-Baradat
    • 1
    • 2
  • Pedro M. Aso
    • 1
  • Armando Reyna-Bello
    • 2
  1. 1.Departamento de Biología Celular, Grupo de Bioquímica e Inmunología de HemoparásitosUniversidad Simón BolívarCaracasVenezuela
  2. 2.Centro de Estudios Biomédicos y Veterinarios Grupo de InmunobiologíaUniversidad Nacional Experimental Simón Rodríguez-IDECYTCaracasVenezuela

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