Endotrypanum^ a Unique Intraerythrocytic Flagellate of New World Tree Sloths
Total Page：16
File Type：pdf, Size：1020Kb
ECO 92: Vrotozooíogy InTíkAmazm. Endotrypanum^ a unique intraerythrocytic flagellate of New World tree sloths. An evolutionary link or an evolutionary backwater? JEFFREY J. SHAW Wellcome Parasítology Unit, Instituto Evandro Chagas, Fundação Nacional de Saúde, Belém, PA 66017-970, Brasil Endotrypanum is principally a parasite of forest dwelling two-toed sloths, Choloepus species, and apart from being the first trypanosomatid to be named in the neotropics it is also the only haemoflagellate that has an intraerythrocytic phase. In culture it grows as a promastigote and in phlebotomine sandflies it has a peripylarian type development, similar to Leishmania of the sub- genus Vianna. This review covers the geographical distribution, morphology, ultrastructure, trans- mission, life cycle, vector specificity, antigenic and molecular characterization, taxonomy and phylogeny of Endotrypanum. Attention is drawn to similarities between certain epitopes of Endotrypanum and some rodent Leishmania and it is also suggested that the former may represent a Miocene parasite group. Besides the importance of developing simple methods to distinguish Endotrypanum and Leishmania for epidemiologícal purposes, Endotrypanum^s unique characters also make it a usefui model for both field and laboratory studies on different aspects of trypanosomatid biology especially those related to evolution. Endotrypanum é principalmente um parasita das preguiças reais da flo•taxonomia e filogenia. As similaridades entre alguns epitopos de resta, além de ser o primeiro tripanosomatídeo a ser descrito noEndotrypanum Novo e algumas Leishmania de roedores são salientadas e Mundo e o único hemoflagelado encontrado em células vermelhas. Cres•sugerem também que Endotrypanum representa um grupo de parasitas ce em cultura na forma promastigota e, em flebotomineos, seu desen• da época Mioceno. Além da importância do desenvolvimento de métodos volvimento é do tipo peripilaria como leishmanias do subgênero Vianna. simples para diferenciar entre Endotrypanum e Leishmania em pes• Nesta revisão os seguintes tópicos sobre Endotrypanum são tratados: quisas epidemiológicas, o Endotrypanum é também um bom modelo para distribuição geográfica, moifologia, ultraestrutura, transmissão, cicloestudos de campo e de laboratório sobre vários aspectos da biologia de evolutivo, especificidade vetorial, caracterização antigênica e molecular. tripanosomatídeos, especialmente os relacionados à evolução. ithout doubt Endotrypanum is one of the most was described a year later by Chagas (2) and Leishmania extraordinary flagellates in the world. It belongs braziliensis was named by Vianna in 1911 (3). to the family Trypanosomatidae that includes The literature on Endotrypanum is extremely limited W parasites, such as trypanosomes and leishmania, compared to that of T. cruzi and Leishmania, but this is which produce disease in both man and domestic animais perfectly understandable because of the public health im• in the tropical regions of the New and Old World. Few peo- portance of the latter two parasites. However, the finding ple realize, however, that Endotrypanum was the first that sloths are important reservoirs of Leishmania (4,5,6), member of the family to be described in the neotropics. It and that Endotiypanum also infects sandflies (7), that are was named by Mesnil and Brimont in 1908 (1), the same also the vectors of the former parasite, has led to an in- year that Chagas discovered the first cases of Chagas's dis• creased interest in Endotrypanum during recent years. ease amongst people living along the track of the Central Brazilian railway in Minas Gerais State. Ttypanosoma cruzi Geographical distribution and epízootiology Correspondence to: Jeffrey J. Shaw, Wellcome Parasítology Unit, Instituto The first records of Endotiypanum were in two-toed sloths Evandro Chagas, Fundação Nacional de Saúde, Caixa Postal 3, Belém, PA (Fig. 1), Choloepus didactylus, from French Guiana (1), 66017-970, Brasil and subsequently it was recorded in the three-toed sloth in Volume 44(2/3) • March/June 1992 Ciência e Cultura (Journal ot the Brazilian Association for the Advancement of Science) • 107 .ECO 92: Frotozooío0y InTíieAtrujzm. 1953 (8) and the two-toed sloth in 1956 (9) from Costa Rica, and in two-toed sloths from Panamá in 1914 (10) and Brazil in 1925 (11). Sloths of both genera Choloepus and Bradypus, occur in other South American countries, but there is just one record of this parasite from Colômbia (12). This might be considered as surprising, especially as sloths have been examined, and found infected with Leishmania in Colômbia (13) and Ecuador (14). However, in both cases very few animais were examined and Endotrypanum al- most certainly occurs throughout the geographical distribu- tion of two-toed sloths. Habitat preference of any animal plays a key role in determining what infections it is likely to acquire, particu- larly in the case of vector borne parasites. Often important clues in pinpointing the vector of a parasite can be gained by relating incidence of infection to habitats. Both two and three-toed sloths occur in neotropical forests, but they have different habitat preferences, the former being generally commoner in higher forests. Infection rates of Endo• trypanum vary between the two genera of sloths as well as between different geographical áreas, such as Panamá and Costa Rica. This is either a reflection of different habitat preferences of the two genera of sloths or Endotrypanum'^ vector. In Panamá, for example, I found (15) Endo• trypanum in 37/100 two-toed sloths and in 0/39 three-toed sloths, and later workers at the Gorgas Memorial Labora- loepus didactylus. rhe major hosi of tory (4,16) found infections in 49/157 Choloepus and 1/77 in rlie Amazon region. Bradypus. However, if the figures are broken down accord- ing to the ecological background of the sloths, 50% of the two-toed sloths from forested áreas as compared to only Muniz (19) described infections in two-toed sloths from 3% of those from the more open áreas were positive. An Pará State, one of which had been seen in 1936. Infections analysis of the data from Costa Rica (9,10,15,17,18) shows in two-toed sloths have been found in different regions of that 23/63 two-toed sloths were infected with the State, including those to the north of the Amazon river Endotrypanum as were 7/86 three-toed sloths. This infec• and in ali there are records of Endotiypanum in 83/137 two- tion rate in Bradypus is higher than anywhere else in the toed sloths and 1/72 three-toed sloths (5,16,20,21). Américas and may reflect different habitat preferences of The overall picture which emerges throughout most of either the vector or the sloth. Central and South America is that infection rates are signifi- The first record of Endotrypanum (11) in Brazil gave cantly higher in two-toed sloths, reaching almost 50% in ani• no details of the origin of the sloth, but in 1944 Cunha & mais from forested áreas, strongly suggesting that the vector(s) are commoner in this habitat. The size of a piece of forest and the number of sloths that are required to maintain the infection cycle are unknown, but infections have been found in sloths captured in small patches of forest very near . - . f to the city of Belém located in reserved áreas that belong to the Belém water company. The cutting of the forest for ar- ^ i ^ able and cattle farming has ied to the formation of pockets of d forest over large áreas of Pará State, which may or may not be big enough to support a sufficient number of sloths to maintain Endotrypanum infections. Figure 2. Imraeiylhrocytic epimastigotes of Endotrypanum Morphology, ultrastructure schaudinni (1-13) from Panamanian and virai particles sloths. Choloepus hoffmanni, and The blood forms are morphologically either epimastigotes or trypomastigotes of E. monterogeii trypomastigotes (Figs. 2 and 3) and those seen in sandflies (14-25) from and cultures are typical promastigotes. Early studies on the Costa Rican slotfis morphology of the bloodstream forms of Endotrypanum in 10 u (Ref 15). Panamá (10) and French Guiana (22) showed that they were 108 • Ciência e Cultura (Journal of the Brazilian Association for ttie Advancement of Science) Volume 44(2/3) . Marcti/June 1992 ECO 92: Vrotozootogy InTtieAntazm. Figure 3. Huemoflagellates found in the "hlood of the two-toed stoth. Choloepus hoffmanni, from Central America: Epimasligoies of Endo• Figure 4. Cultural forms of Endotrypanum schaudinni seen in a pri- trypanum schaudinni tl-3i and young forms of the same parasite (6,7;, mary culture in Tohie's hiphasic médium. Forms seen durini; lhe first 4 nypomasiigotes ofE. monterogeii (3-5) from Costa Rica. trypomastigoles days (1-13), after 10 days (14-17) and after 28 days (22-27). Flagel- of Trypanosnma preguici (9-11) and T. leeuwenlioeki 112.131 and lhe lates from colonies on the surface of lhe agar (28-34) with truncated same speçies (14-17) in the blood of a mouse (Ref. 15). ^ anterior ends (Ref. 15). basically the same, having a short free flagellum and some- subsequently in 1941 by Emanuel Dias (19). Cunha and times a poorly developed undulating membrane. In fresh Muniz examined the cultures of these two isolates of Endo• films extracellular forms were noted and in some cases it trypanum and noted that they were predominantly com- was considered that these forms were larger and that the posed of promastigotes, but they also mentioned finding kinetoplasts migrated posteriorly. This is contrary to devel- small numbers of trypomastigotes, Subsequent workers opment seen in primary culturas in which the initial phase (9,15) confirmed the promastigote nature (Fig. 4) of the of multiplication is as amastigotes and subsequently as culture forms of Endotrypanum strains from Central these become more elongated the kinetoplast is anterior in America, but found no trypomastigotes. In cultures of the typical promastigote position. Differences in the mor- Endotrypanum strains that have been shown to be pure in- phology of the actual bloodstream forms are due to varia- fections, by biochemical and immunological techniques, no tions in the position of the nucleus.