HUMAN TRYPANOSOMIASIS CAUSED BY TRYPANOSOMA EVANSI IN INDIA: THE FIRST CASE REPORT
Prashant JoshiVIJAY R. SHEGOKARR M PowarStéphane HerderRAHUL KATTIHarsha R. SalkarVibhawari DaniAradhana BhargavaJ JanninPhilippe Truc
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We report an Indian farmer who had fluctuating trypanosome parasitemia associated with febrile episodes for five months. Morphologic examination of the parasites indicated the presence of large numbers of trypanosomes belonging to the species Trypanosoma evansi, which is normally a causative agent of animal trypanosomiasis known as surra. Basic clinical and biologic examinations are described, using several assays, including parasitologic, serologic, and molecular biologic tests, all of which confirmed the infecting species as T. evansi. Analysis of cerebrospinal fluid indicated no invasion of the central nervous system (CNS) by trypanosomes. Suramin, a drug used exclusively for treatment of early-stage human African trypanosomiasis with no CNS involvement, effected apparent cure in the patient. This is the first case reported of human infection due to Trypanosoma evansi, which was probably caused by transmission of blood from an infected animal.Keywords:
Trypanosoma evansi
Trypanosoma vivax
Trypanosoma evansi
Trypanosoma vivax
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Human African trypanosomiasis (HAT) is a neglected tropical disease still endemic in the Republic of Congo. Despite the continuous detection of HAT cases in the country, there is still not enough data on trypanosome infections in tsetse flies, trypanosome species and tsetse flies' species distribution in endemic foci. The present study was intended to fill this gap and improve understanding of trypanosome circulation in three active foci in the centre and south of Congo.
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Trypanosoma vivax
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There are three trypanosoma species of veterinary importance in South America: (1) Trypanosoma evansi, the causative agent of derrengadera mechanically transmitted by bloodsucking insects such as tabanids, (2) Trypanosoma vivax, also mechanically transmitted by some dipteras hematophages as tabanids and/or Stomoxys, and (3) T. equiperdum, a tissue parasite adapted to sexual transmission and the causative agent of dourine, a distinctive disease that affects only Equidae. In order to evaluate the parasitological, hematological, and serological response of sheep infected with T. vivax, T. evansi, and T. equiperdum, four female sheep were experimentally infected with Venezuelan trypanosome field isolates: two T. evansi of differing virulences, one T. equiperdum; one T. vivax. Parasitemia and clinical parameters such as hematocrit, red blood cell count, hemoglobin, and body temperature were measured. T. evansi caused a chronic disease with undulant parasitemia alternating with some cryptic periods of at least 54 days, with no clinical signs. T. equiperdum, never described as infectious to ruminants, also caused a chronic disease with low undulant parasitemia. T. vivax caused an acute infection with severe anemia showing a drop of more than 70% of the hematocrit value, high fever, and rapid deterioration of physical condition, for 36 days of infection. Indirect ELISAs using crude extracts of the three species of trypanosomes as antigens were performed for detection of anti-trypanosome antibodies in sheep sera. Cross-reaction was observed between the three parasite species. These results show that sheep are susceptible to the three-trypanosome species and suggest they can act as a reservoir when sheep are raised and managed with other important livestock such as cattle, horses, buffalos, or goats. These findings are especially interesting for T. equiperdum, a species that has not been reported as infective to sheep.
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The Malanga sleeping sickness focus of the Democratic Republic of Congo has shown an epidemic evolution of disease during the last century. However, following case detection and treatment, the prevalence of the disease decreased considerably. No active survey has been undertaken in this focus for a couple of years. To understand the current epidemiological status of sleeping sickness as well as the animal African trypanosomiasis in the Malanga focus, we undertook the identification of tsetse blood meals as well as different trypanosome species in flies trapped in this focus. Pyramidal traps were use to trap tsetse flies. All flies caught were identified and live flies were dissected and their mid-guts collected. Fly mid-gut was used for the molecular identification of the blood meal source, as well as for the presence of different trypanosome species. About 949 Glossina palpalis palpalis were trapped; 296 (31.2%) of which were dissected, 60 (20.3%) blood meals collected and 57 (19.3%) trypanosome infections identified. The infection rates were 13.4%, 5.1%, 3.5% and 0.4% for Trypanosoma congolense savannah type, Trypanosoma brucei s.l., Trypanosoma congolense forest type and Trypanosoma vivax, respectively. Three mixed infections including Trypanosoma brucei s.l. and Trypanosoma congolense savannah type, and one mixed infection of Trypanosoma vivax and Trypanosoma congolense savannah type were identified. Eleven Trypanosoma brucei gambiense infections were identified; indicating an active circulation of this trypanosome subspecies. Of all the identified blood meals, about 58.3% were identified as being taken on pigs, while 33.3% and 8.3% were from man and other mammals, respectively. The presence of Trypanosoma brucei in tsetse mid-guts associated with human blood meals is indicative of an active transmission of this parasite between tsetse and man. The considerable number of pig blood meals combined with the circulation of Trypanosoma brucei gambiense in this focus suggests a transmission cycle involving humans and domestic animals and could hamper eradication strategies. The various species of trypanosomes identified in the Malanga sleeping sickness focus indicates the coexistence of animal and human African Trypanosomiasis. The development of new strategies integrating control measures for human and animal trypanosomiasis may enable the reduction of the control costs in this locality.
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Salivarian trypanosomes sequentially express only one variant surface glycoprotein (VSG) on their cell surface from a large repertoire of VSG genes. Seven cryopreserved animal trypanosome isolates known as TeAp-ElFrio01, TEVA1 (or TeAp-N/D1), TeGu-N/D1, TeAp-Mantecal01, TeGu-TerecayTrino, TeGu-Terecay03 and TeGu-Terecay323, which had been isolated from different hosts identified in several geographical areas of Venezuela were expanded using adult albino rats. Soluble forms of predominant VSGs expressed during the early infection stages were purified and corresponded to concanavalin A-binding proteins with molecular masses of 48-67 kDa by sodium dodecyl sulfate-polyacrylamide gel electropohoresis, and pI values between 6.1 and 7.5. The biochemical characterization of all purified soluble VSGs revealed that they were dimers in their native form and represented different gene products. Sequencing of some of these proteins yielded peptides homologous to VSGs from Trypanosoma (Trypanozoon) brucei and Trypanosoma (Trypanozoon) evansi and established that they most likely are mosaics generated by homologous recombination. Western blot analysis showed that all purified VSGs were cross-reacting antigens that were recognized by sera from animals infected with either T. evansi or Trypanosoma (Dutonella) vivax. The VSG glycosyl-phosphatidylinositol cross-reacting determinant epitope was only partially responsible for the cross-reactivity of the purified proteins, and antibodies appeared to recognize cross-reacting conformational epitopes from the various soluble VSGs. ELISA experiments were performed using infected bovine sera collected from cattle in a Venezuelan trypanosome-endemic area. In particular, soluble VSGs from two trypanosome isolates, TeGu-N/D1 and TeGu-TeracayTrino, were recognized by 93.38% and 73.55% of naturally T. vivax-infected bovine sera, respectively. However, approximately 70% of the sera samples did not recognize all seven purified proteins. Hence, the use of a combination of various VSGs for the diagnosis of animal trypanosomosis is recommended.
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The growth inhibition test in vitro was conducted to detect the sensitivities for suramin of Trypanosoma evansi AHB,GDB1,GDB2,GDH,GXM,HBM,HNB,JSB1,JSB2,XJCA,YNB and ZJB strains,the drug concentration inhibiting incorporation by 50% IC 50 were 0.114 mg/L,0.041 mg/L, 0.120 mg/L,0.149 mg/L,0.752 mg/L,0.252 mg/L,0.171 mg/L,0.127 mg/L,0.339 mg/L,0.094 mg/L,0.106 mg/L,0.118 mg/L respectively.The results showed that Trypanosoma evansi of different strains had different sensitivities for suramin and suggested that Trypanosoma evansi from China had difference in drug resistance.GXM strain for suramin showed comparatively high level of drug resistance among 12 Trypanosoma evansi isolates.The mice treatment test in vivo showed GXM isolate could not be cured with dosages 10 mg/kg suramin and GXM strain had comparatively clear drug resistance;GDB1 was cured completely with dosages 10 mg/kg.We concluded that the mice treatment test in vivo matched the growth inhibition test in vitro,which suggested that most of T.evansi isolates from China existed low sensitivities to suramin and a few strains had drug resistance for suramin to a certain extent.
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In order to identify pathogenic trypanosomes responsible for African trypanosomiasis, and to better understand tsetse-trypanosome relationships, surveys were undertaken in three sites located in different eco-climatic areas in Côte d'Ivoire during the dry and rainy seasons. Tsetse flies were caught during five consecutive days using biconical traps, dissected and microscopically examined looking for trypanosome infection. Samples from infected flies were tested by PCR using specific primers for Trypanosoma brucei s.l., T. congolense savannah type, T. congolense forest type and T. vivax. Of 1941 tsetse flies caught including four species, i.e. Glossina palpalis palpalis, G. p. gambiensis, G. tachinoides and G. medicorum, 513 (26%) were dissected and 60 (12%) were found positive by microscopy. Up to 41% of the infections were due to T. congolense savannah type, 30% to T. vivax, 20% to T. congolense forest type and 9% due to T. brucei s.l. All four trypanosome species and subgroups were identified from G. tachinoides and G. p. palpalis, while only two were isolated from G. p. gambiensis (T. brucei s.l., T. congolense savannah type) and G. medicorum (T. congolense forest, savannah types). Mixed infections were found in 25% of cases and all involved T. congolense savannah type with another trypanosome species. The simultaneous occurrence of T. brucei s.l., and tsetse from the palpalis group may suggest that human trypanosomiasis can still be a constraint in these localities, while high rates of T. congolense and T. vivax in the area suggest a potential risk of animal trypanosomiasis in livestock along the Comoé River.
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In previous papers published in the ‘Proceedings,’ the morphology of various trypanosomes, such as Trypanosoma pecorum, vivax, uniforme, nanum , and brucei , has been described somewhat more fully than is usually done. It is proposed to do the same for Trypanosoma evansi in this paper. This trypanosome causes the disease in elephants, camels, horses, cattle, and dogs, known in India as Surra. It was discovered in 1880, by Evans, in the Punjab.
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The delta region of Southern Nigeria is believed to be endemic for animal trypanosomiasis. Occasionally, cases of suspected human trypanosomiasis based on clinical presentation have been reported, thus we undertook survey of tsetse flies from the area with the purposes of typing the trypanosomes in the locality and demonstrating the possibility that human trypanosomiasis may be present in the area if the vector Trypanosoma gambiense is seen. A total of 429 flies were trapped; all were of Glossina palpalis palpalis specie. Sixty or 14.0% of them were found to be infected by trypanosomes. The infection rates were 7.7%, 1.6%, 1.6% and 6.3% for Trypanosoma vivax, Trypanosoma brucei brucei, Trypanosoma simiae and Trypanosoma congolense respectively. Mixed infections in various combinations were observed. There was no evidence of human infective Trypanosoma gambiense. The presence of various species of animal trypanosomes even as mixed infections confirms that the area is indeed endemic for animal trypanosomiasis. The simultaneous occurrence of Glossina palpalis. palpalis and Trypanosoma brucei brucei, however, makes it imperative to monitor the area continuously for human trypanosomiasis.
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