MEM INST OSWALDO CRUZ, RIO DE JANEIRO, 94 (Suppl.I) September 1999
PAGES: 181-184 DOI: Full paper
Taxonomy of Trypanosoma cruzi: a Commentary on Characterization and Nomenclature

Hooman Momen

Departamento de Bioquímica e Biologia Molecular, Instituto Oswaldo Cruz, Av. Brasil 4365, 21045-900 Rio de Janeiro, RJ, Brasil

Early in the history of Chagas disease it became apparent that there was considerable variation in the incidence and severity of infections with parasites classified as being Trypanosoma cruzi (see Pessoa 1960 for a review of early findings by scientists such as Carlos Chagas and Emmanuel Dias). A variety of typing schemes were developed as a means of finding the basis of this variation and more finely, classifying the organisms within the species. Here instead of reviewing the literature on this topic a critical perspective on the typing of T. cruzi is presented.

Early attempts at typing strains included the immunological types of Nussensweig et al. (1963) however it was the pioneering work of Andrade (1974) who first correlated specific arrays of morphobiological and behavioural characters to particular types within T. cruzi. The molecular typing of T. cruzi strains was pioneered with isoenzymes (Toye 1974) and Miles used the technique to classify isolates of this parasite into strain-groups (Miles et al. 1977) and types (Miles et al. 1978). The term zymodeme was later introduced (Barrett et al. 1980) to refer to "trypanosome populations that possess like forms of specified enzymes". Ready and Miles (1980) suggested that the T. cruzi zymodemes indicated distinct taxa, however, Miles et al. (1981a, b) were reluctant to give the taxa sub-specific status. This reluctance was followed by nearly all subsequent authors, eventhough the basic zymodeme divisions were confirmed by many subsequent studies using a variety of techniques at both the protein and DNA level (Table) and a strong correlation between the intrinsic and extrinsic characters (Lumsden 1977) of T. cruzi types was convincingly demonstrated (Andrade et al. 1983, Andrade 1985).



This contrast between the eagerness to sub-divide T. cruzi and the reluctance to name formal taxa is curious in the light of the comparison with the related trypanosomatid genus Leishmania. For example the phylogenetic diversity in T. cruziis comparable to that observed in the whole of the genus Leishmania (Tibayrenc 1998a), which is currently divided into nearly 50 species. Even if the comparison is limited to the same geographical area and a single order of reservoir, there are still about twenty mammalian species of New world Leishmania as compared to a single T. cruzi species. Although there is some criticism of the excess number of species in Leishmania, with the level of phylogenetic divergence between some species of Leishmania comparable to lower clades of T. cruzi (Tibayrenc 1998a), the benefit of the named species in clarifying the ecoepidemiology and causes of the diverse clinical manifestations of the leishmaniases is undoubted. Furthermore the studies of Andrade (1974) provided a similar basis for T. cruzi to that of Leishmania for the description of new taxa.

Several reasons can be put forward to explain this reluctance for describing named taxa for T. cruzi. At the time the principal zymodeme divisions were proposed and in the period afterwards several other studies raised questions about the divisions. For example, Brenner (1977) proposed two polar types (Y and CL). These strains were shown later to posses a number of fundamental differences such as differences in the course of infection in a variety of hosts including morphology of blood forms at peak of parasitemia which occurred at different times and differences in infectivity to mouse peritoneal macrophages, tissue culture cells and in vivo infections. These fundamentally different types appeared to belong to the same zymodeme. The zymodemes themselves appeared not to be stable (Romanha et al. 1979) a finding reinforced by apparent instability of isoenzyme profiles in other parasites (Mirelman et al. 1986). The principal zymodemes also appeared to have geographical variations and could be divided into a number of isoenzyme strains (Tibayrenc & Ayala 1988). At the same time the technique of schizodeme analysis (Morel et al. 1980) showed an extensive heterogeneity within T. cruzi, which could not be readily classified into types. These results were supported by many further DNA studies using a variety of techniques demonstrating the genetic variability of T. cruzi (Macedo & Pena 1998).

Morever the use of these techniques indicated the possibility of heterogeneity within the T. cruzi strains, with particular strains or isolates being mixtures of at least two populations (Morel et al. 1980) and the probability of selective isolation of clones or strains (Deane et al. 1984, Macedo & Pena 1998). These and other reasons favoured the view of T. cruzi as a single polytypic species and against a formal subdivsion, as well as illustrating the difficulty of correlating strains with patient morbidity. However the possibility of a strain or even clone having more than one population of parasites was in fact the explanation for the observed instability of the isoenzyme characters and apparent similarity between the enzyme profile of the polar types (Goldberg & Perreira 1983, Gomes et al. 1991, Clark & Diamond 1993).



Lumsden (1977) defined three classes of nomenclature, (i) operational, without any indication of characterization, which included terms such as population, sample, isolate, clone, stock and (ii) Linnean, including genus, species and subspecies. The third class he called "a new nomenclature to designate the manifold new subspecific categories which are being discovered by new methods of characterization _ the multiplicity of functionally different populations which exist within the same morphological species". Although he did not formally name this class we can refer to it as infraspecific, however as pointed out by Lumsden for many microrganisms, non-contentious recognition is more often at the level of genus and subgenus. This third class has proved very popular in molecular studies of T. cruzi as the profusion of names in the Table demonstrates.

Attention has again been recently focused on two primary phylogenetic divisions within T. cruzi (Tibayrenc 1995, Souto et al. 1996, Nunes et al. 1997). While there are differences of opinion about the significance of this division (Brisse et al. 1998, Souto et al. 1998, Macedo & Pena 1998) the basis for the division is well supported (Table). The discovery that microbial lineages maintain their genetic integrity over long time intervals and over great distances, that is, their genomes are not rapidly broken down or reshuffled by recurrent mutation and recombination is known as the clone concept (Orskov & Orskov 1983). Tibayrenc et al. (1986) have proposed this model as the main population genetic structure for T. cruzi . The application of this model with the presence of a primary infraspecific division in T. cruzimeans that Chagas disease can no longer be considered as a single disease entity. At least two diseases corresponding to the two divisions must be considered with obvious implications for clinical and experimental studies as well as control of the disease. Results of many investigations need now to be reinterpreted based on the classification of the strains used. This may also be an explanation for differences in observations among researchers in many studies such as the use of diagnostic techniques reported in the literature.



In the history of Chagas disease, the wheel has been reinvented many times (Dvorak 1984). A sound taxonomy may often have avoided much wasted time and effort. The third class of nomenclature as proposed by Lumsden (1977) has been usefully applied to T. cruzi (as shown in Table) however it may be time to consider the use of formal Linnean designations for the divisions within this parasite. Among the arguments used against the naming of T. cruzi taxa have been the presence of putative hybrids between the two main lineages of T. cruzi (major clone 39 and its equivalents); the need for further studies on the population structure as there is evidence of genetic recombination (Bogliolo et al. 1996, Carrasco et al. 1996); the difficulty of correlating strains with patient morbidity and the genetic variability of T. cruziclones. The arguments against the formal naming of T. cruzi taxa though valid are disputed and in any case are not particular to this parasite and have not impeded the naming of taxa in other organisms.

The present situation is similar to the early 80´s where the work of Miles et al. (1977, 1978) and Andrade (1974) had laid the basis for the formal naming of T. cruzi taxa. Again the strong correlations between major phylogenetic divisions in T. cruzi and biological characters (Andrade & Magalhaes 1997, Revollo et al. 1998) are being emphasized. The naming of species for the principal divisions and subspecies for the lower divisions would clearly aid in the comprehension of studies on this parasite. As pointed out by Steel (1962) "nomenclature should be our servant and not our master".



Andrade SG 1974 Caracterização de cepas do Trypanosoma cruzi isoladas no Recôncavo Baiano. Rev Patol Trop 3: 65-121.

Andrade SG 1985. Morphological and behavioural characterization of Trypanosoma cruzi strains. Rev Soc Bras Med Trop 18 (Suppl.):39-46.

Andrade SG, Magalhães JB 1997. Biodemes and zymodemes of Trypanosoma cruzi strains: correlations with clinical data and experimental pathology. Rev Soc Bras Med Trop 30: 27-35.

Andrade V, Brodskyn C, Andrade SG 1983. Correlation between isoenzyme patterns and biological behaviour of different strains of Trypanosoma cruzi. Trans R Soc Trop Med Hyg 76: 796-799.

Barret TV, Hoff RH, Mott KE, Miles MA, Godfrey DG, Teixeira R, Almeida de Souza JÁ, Sherlock IA 1980. Epidemiological aspects of three Trypanosoma cruzi zymodemes in Bahia State, Brazil. Trans R Soc Trop Med Hyg 74: 84-90.

Bogliolo AR, Lauriapires L, Gibson WC 1996. Polymorphisms in Trypanosoma cruzi: evidence of genetic recombination. Acta Trop 61: 31-40.

Brener Z 1977. Intraspecific variations in Typanosoma cruzi: two types of parasite populations presenting distinct characteristics. PAHO Scientific Pub 347: 11-21.

Brisse S, Barnabé C, Tibayrenc M 1998. Trypanosoma cruzi: how many relevant phylogenetic subdivisions are there? Parasitol Today 14: 178-179.

Carrasco HJ, Frame IA, Valente SA, Miles MA 1996. Genetic exchange as a possible source of genomic diversity in sylvatic populations of Trypanosoma cruzi. Am J Trop Med Hyg 54: 418-424.

Clark CG, Diamond LS 1993. Entamoeba histolytica: an explanation for the reported conversion of "non-pathogenic" amebae to the "pathogenic" form. Exp Parasitol 77: 456-460.

Clark CG, Pung OJ 1994. Host specificity of ribosomal DNA variation in sylvatic Trypanosoma cruzi from North America. Mol Biochem Parasitol 66: 175-179.

Deane MP, Mangia RHR, Pereira NM, Momen H, Gonçalves AM, Morel CM 1984. Trypanosoma cruzi: strain selection by different schedules of mouse passage of na initially mixed infection. Mem Inst Oswaldo Cruz 79: 495-497.

Dvorak JA 1984. Natural heterogeneity of Trypanosoma cruzi: biological and medical applications. J Cell Biochem 24: 357-371.

Ebert F 1982. The identification of two main-groups of Trypanosonma cruzi stocks from Brazil by their isoenzyme patterns of isoelectrofocusing. Tropenmed Parasitol 33: 140-146.

Goldberg SS, Silva Pereira AA 1983. Enzyme variation among clones of Trypanosoma cruziJ Protozool 69: 91-96.

Gomes ML, Romanha AJ, Gonçalves AM, Chiari E 1991. Stability of isoenzyme and kinetoplast DNA (k-DNA) patterns in successively cloned Trypanosoma cruzi populations. Mem Inst Oswaldo Cruz 86: 379-385.

Lumsden WHR 1977. Problems in characterization and nomenclature of trypanosome populations. Ann Soc Belge Med Trop 57: 361-368

Macedo AM, Pena SDJ 1998. Genetic variability of Trypanosoma cruzi: implications for the pathogenesis of Chagas disease. Parasitol Today 14: 119-124.

Miles MA, Apt BW, Widmer G, Povoa MM, Schofield CJ 1984. Isoenzyme heterogeneity and numerical taxonomy of Trypanosoma cruzi stocks from Chile. Trans R Soc Trop Med Hyg 78: 526-535.

Miles MA, Povoa M, De Souza AA, Lainson R, Shaw JJ, Ketteridge DS 1981a. Chagas disease in the Amazon Basin: II. The distribution of Trypanosoma cruzi zymodemes 1 and 3 in Pará State, north Brazil. Trans R Soc Trop Med Hyg 75: 667-674.

Miles MA, Povoa MM, Prata A, Cedillos RA, Souza AA, Macedo V 1981b. Do radically dissimilar Trypanosoma cruzi (zymodemes) cause Venezuelan and Brazilian forms of Chagas disease? Lancet 20: 1338-1340.

Miles MA, Souza A, Póvoa M, Shaw JJ, Lainson R, Toyé PJ 1978. Isozymic heterogeneity of Trypanosoma cruziin the first autochthonous patients with Chagas disease in Amazonian Brazil. Nature 272: 819-821.

Miles MA, Toyé PJ, Oswald SC, Godfrey DG 1977. The identification by isoenzyme patterns of two distinct strain-groups of Trypanosoma cruzi circulating independently in a rural area of Brazil. Trans R Soc Trop Med Hyg 71: 217-225.

Mirelman D, Bracha R, Wexler A, Chayen A 1986. Changes in isoenzyme patterns of a cloned culture of nonpathogenic Entamoeba histolytica during axenization. Infect Immun 54: 827-832

Morel C, Chiari E, Camargo EA, Mattei DM, Romanha AJ, Simpson L 1980. Strains and clones of Trypanosoma cruzi can be characterized by pattern of restriction endonuclease. Proc Natl Acad Sci USA 77: 6810-6814.

Muhlpfordt H, Berger J 1990. Characterization and grouping of Trpanosoma cruzi stocks by DNA base-specific fluorochromes and diascriminat analysis. Parasitol Res 76: 319-325.

Nunes LR, Carvalho MRC, Buck GA 1997. Trypanosoma cruzi strains partition into two groups based on the structure and function of the sliced leader RNA and rRNA gene promoters. Mol Biochem Parasitol 86: 211-224.

NussenszweigV, Kloetzel J, Deane LM 1963. Acquired immunity in mice infected with strains of immunological types A and B of Trypanosoma cruzi. Exp Parasitol 14: 233-239.

Orskov F, Orskov I 1983. Summary of a workshop on the clone concept in the epidemiology, taxonomy and evolution of the Enterobacteriaceae and other bacteria. J Infec Dis 148: 346-357.

Pessoa SB 1960. Reservatórios animais do Trypanosoma cruzi, p.1150-1180. Anais do Congresso Interna-cional sobre Doença de Chagas. Oficina Gráfica da Universidade do Brasil.

Ready PD, Miles MA 1980. Delimitation of Trypanosoma cruzi zymodemes by numerical taxonomy. Trans R Soc Trop Med Hyg 74: 238-242.

Revollo S, Oury B, Laurent JP, Barnabé C, Quesney V, Carrière V, Noël S, Tibayrenc M 1998. Trypanosoma cruzi: impact of clonal evolution of the parasite on its biological and medical properties. Exp Parasitol 89: 30-39.

Romanha AJ, Da Silva, Pereira AA, Chiari E, Kilgour V 1979. Isoenzyme patterns of cultured Trypanosoma cruzi: changes after prolonged subculture. Comp Biochem Physiol 62B: 139-142.

Schottelius J 1982. The identification by lectins of two strain groups of Trypanosoma cruzi. Z Parasitenk 68: 147-154.

Souto RP, Fernandes O, Macedo AM, Campbell DA, Zingales B 1996. DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Mol Biochem Parasitol 83: 141-152.

Souto RP, Zingales B, Fernandes O, Macedo AM, Campbell DA 1998. Trypanosoma cruzi: how many relevant phylogenetic subdivisions are there? Reply. Parasitol Today 14: 207.

Steel KJ 1962. The practice of bacterial identification. Sympos Soc Gen Microbiol 12: 405-432.

Tibayrenc M 1995. Population genetics of parasitic protozoa and other microorganisms, p. 47-115. In JR Baker, R Muller & D Rollinson (eds), Advances in Parasitology, Academic Press, London.

Tibayrenc M 1998a. Genetic epidemiology of parasitic protozoa and other infectious agents: the need for an integrated approach. Int J Parasitol 28: 85-104.

Tibayrenc M 1998b. Integrated genetic epidemiology of Infectious diseases: the Chagas model. Mem Inst Oswaldo Cruz 93: 577-580.

Tibayrenc M, Ayala FJ 1988. Isozyme variability in Trypanosoma cruzi, the agent of Chagas disease: genetical, taxonomical, and epidemiological significance. Evolution 42: 277-292.

Tibayrenc M, Ayala FJ 1991. Towards a population genetics of microorganisms: the clonal theory of parasitic protozoa. Parasitol Today 7: 228-232.

Tibayrenc M, Breniere SF 1988. Trypanosoma cruzi: major clones rather than principal zymodemes. Mem Inst Oswaldo Cruz 83(Suppl. I): 249-255.

Tibayrenc M, Miles MA 1983. A genetic comparison of Brazilian and Bolivian zymodemes of Trypanosoma cruzi.Trans R Soc Trop Med Hyg 77: 76-83.

Tibayrenc M, Echalar L, Dujardin P, Poch O, Desjeux P 1984. The microdistribution of isoenzymic strains ofTrypanosoma cruzi in Southern Bolivia: New isoenzyme profiles and further arguments against Mendelian sexuality. Trans R Soc Trop Med Hyg 78: 519-525.

Tibayrenc M, Ward P, Moya A, Ayala F 1986. Natural populations of Trypanosoma cruzi, the agent of Chagas disease; have a complex multiclonal structure. Proc Nat Ac Sc USA 83: 115-119.

Toyé PJ 1974. Isoenzyme variation in isolates of Trypanosoma cruzi . Trans R Soc Trop Med Hyg 68: 147-158.

Zillman U, Ebert F 1983. The characterization of Trypanosoma cruzi stocks by starch gel electrophoresis, comparison of results with those of isoelectric focusing. Tropenmed Parasitol 34: 84-88.

Fax: +55-21-590.3495.

E-mail:  This e-mail address is being protected from spambots. You need JavaScript enabled to view it.  

Received 9 June 1999

Accepted 9 August 1999


Memórias do Instituto Oswaldo Cruz

Av. Brasil 4365, Castelo Mourisco
sala 201, Manguinhos, 21040-900
Rio de Janeiro, RJ, Brazil

Tel.: +55-21-2562-1222

This e-mail address is being protected from spambots. You need JavaScript enabled to view it.



marca fiocruzmarca brasil
marca faperjmarca cnpqmarca capes n marca cope

and diabetes. Erection dysfunction or ED is certainly one of mens most usual problem. It changes buy tadalafil 60mg A common drug is actually an imitation of its manufacturer twin. Both ought to be same in female cialis 20mg Long Phrase Viagra Use Fundamentally Damages Sex Lives This discount cialis canada Equally so, theres something to be said for the wonder of the second, captured forever on picture or a buy cheap cialis People extremely annoyed that they could only get three weeks at a time, Bunker noted. Retired persons cheap pharmacy These types of matters are possibly to being identified as having a result of cancer buy cialis 40mg - Yoghourt - fat-free simply Physical causes: Buying generic medicines now has been cheap generic cialis Herbaceous plants like nigrum and tribulus are well-known for his or her qualities in defeating impotence, which tadalafil 10mg It is not hard to consider Cialis that is generic. Most men start with one-10 mg dosage each purchase cialis Tadalafil quickly gained the moniker of weekender in Paris due to the fabulous results. The bash freaks buy female cialis